Abstract

Pressure ulcers (PrUs) are among the most common secondary complications following spinal cord injury (SCI). External electrical current applied to a wound is believed to mimic the body’s natural bioelectricity and to restart and stimulate endogenous electrical fields to promote wound healing. A systematic review was conducted to critically appraise and synthesize updated evidence on the impact of electrical stimulation (ES) versus standard wound care (comprising cleansing, dressing, nutrition, and debridement as necessary) and/or sham stimulation on PrU healing rates in persons with SCIs.

Medline, Embase, the Cumulative Index for Nursing and Allied Health Literature (CINAHL), PsycINFO, and Cochrane Central were searched using the terms spinal cord injury, electrical stimulation, and pressure ulcer in free text and MESH terms. Publications were limited to peer-reviewed, randomized controlled trials (RCTs) and non-RCTs (CCTs) published in English from 1985 to 2014. The methodological quality of the RCTs was evaluated using the Jadad scale; CCTs were assessed using the Downs and Black tool. Pooled analyses were performed to calculate the mean difference (MD) for continuous data, odds ratio (OR) for dichotomous data, and 95% confidence intervals (CI). A total of 8 trials were reviewed — 6 RCTs and 2 CCTs included a total of 517 SCI participants who had at least 1 PrU. The number of patients per study ranged from 7 to 150 and the number of wounds from 7 to 192. Comparison models included ES irrespective of current type and placement of electrodes against sham/no ES (7 trials), ES delivered by electrodes overlaid on the ulcer versus sham/no ES (4 trials), ES delivered by electrodes placed on intact skin around the ulcer versus sham/no ES (4 trials), ES delivered by electrodes overlaid on the wound bed versus placed on intact skin around the ulcer (1 trial), ES with pulsed current versus sham/no ES (6 trials), ES with constant current versus sham/no ES (2 trials), pulsed current ES versus constant current ES (1 trial), number of PrUs closed (2 trials), and incidence of PrU worsened by ES versus sham/no ES (2 trials). The overall quality of studies was moderate; 2 trials were rated as good quality, 2 were poor quality, and 4 were moderate. Evidence showed ES increased the rate of PrU healing in patients with SCI (MD 4.97, 95% CI 1.97–7.98, P = 0.00; N = 7 studies and 559 ulcers), and a higher proportion of ulcers healed (OR 2.68, 95% CI 1.17–6.14, P = 0.02; N = 2 studies and 226 ulcers). The data suggest pulsed current ES increased the healing rate (MD 6.27, 95% CI 2.77–9.78, P = 0.0005; N = 6 studies and 509 ulcers) more than constant current (MD 4.50, 95% CI 1.19–10.18, P = 0.12; N = 2 studies and 200 ulcers). In addition, wounds with electrodes overlaying the wound bed seemed to heal ulcer faster than wounds with electrodes placed on intact skin around the ulcer. Future preclinical, in vivo models and clinical trials examining the impact of electrodes configuration for PrU healing are warranted. 

The National Pressure Ulcer Advisory Panel/European Pressure Ulcer Advisory Panel (NPUAP/EPUAP)¹ describes a pressure ulcer (PrU) as an area of localized damage to the skin as a result of prolonged pressure alone or pressure in combination with shearing forces. A PrU is typically categorized into 4 key stages depending on ulcer depth and severity. PrUs are among the most common secondary complications following spinal cord injury (SCI). According to the Model SCI System Statistical Centre,² the annual incidence rate of PrUs is 14.7% in the first post-injury year and noted to steadily increase thereafter. It is estimated that up to 85% of people living with SCI develop a PrU during their lifetime.^3-5

According to the NPUAP/EPUAP guideline,¹ a systematic review of 12 studies,⁶ and a survey⁷ once a PrU has developed, it significantly increases the burden on the individual with SCI and/or his/her caregivers and has substantial detrimental impact on the quality of life, independence, and dignity of the patient. If a PrU is severe, it can lead to further disabilities, need for surgical interventions, and fatal infections. Krause et al⁷ surveyed 1017 patients with SCI to examine the relationship between PrU and life adjustment after SCI and found PrUs adversely impacted nearly every area of life studied, including quality of life and independent living. 

Apart from personal consequences, PrUs also represent a significant cost burden for health and social care systems. According to the National Institute of Health and Care Excellence (NICE) guideline,⁸ in addition to the costs of standard care, the daily costs of treating a PrU are estimated to range from £43 to £374 in the United Kingdom. Resources required for treating a PrU include nursing time, dressings, antibiotics, diagnostic tests, and high-specification, pressure-redistributing devices. Although the exact cost of PrU management in SCI is unknown, the total cost of treating PrUs has been estimated to be between £1.4 billion and £2.1 billion per year; the average cost to treat 1 Stage IV PrU is £14,108 per episode in the general population.⁹ 

Treatment for PrUs can vary depending on the grade/stage of the ulcer. The standard care of PrUs varies across individual settings. Although the management of PrUs recommended by clinical guidelines^5,8 includes offloading, improving nutrition, cleansing, debridement, and dressing, the general principles of Stage I ulcer treatment incorporate pressure relief, careful clinical monitoring, cleansing, and dressings to promote hydration; Stage II ulcers may require pressure relief using a high-specification foam mattress/cushion or dynamic support surface and a moist dressing for reepithelialization; and Stage III and Stage IV ulcers usually require advanced nonsurgical or surgical treatment in addition to pressure relief; they also may require debridement and antibacterial treatment if systemic sepsis, cellulitis, or underlying osteomyelitis is clinically evident.

Electrical stimulation (ES) was proposed as a therapeutic modality for wound healing more than a century ago, and its use has been well documented in clinical studies since the 1960s, especially for wounds not responding to standard forms of treatment.^10-16 Despite the fact ES has been demonstrated in clinical studies^13-16 to accelerate wound healing compared to no ES as conjunctive therapy, the understanding of the exact physiological mechanism remains incomplete. Animal models and in vitro preclinical studies^9,17-31 provide some indication of the mechanism of ulcer healing enhanced by ES. Endogenous electrical fields (which measure electrical potentials) are known to naturally exist in the human body and are vital for tissue development and repair.^17-19 The electrical potential at the epidermis (transepithelial potential) is generated by intact skin through directional active ion transportation, leading to the concentration of negative chlorine ions at the surface and positive sodium and potassium ions in the tissues. The epithelial layer of intact skin acts as an electrical barrier. When a wound occurs, the epithelial barrier is broken, allowing the current to flow out of the wound. The transepithelial potential collapses and ions immediately begin to leak out, establishing a weak but measurable current between the skin and inner tissues (the current of injury). The current is thought to continue until the skin defect is repaired.^17-19 

Two main types of ES currents commonly noted in the literature are pulsed current (PC) and direct current (DC).¹⁷ Constant, low-intensity DC involves applying continuous, unidirectional flow of current of low intensity (<1 mA) for at least 1 second. PC includes monophasic and biphasic waveforms: monophasic PC involves brief pulses of unidirectional flow of current followed by a finite off period, and biphasic PC consists of brief pulses of bidirectional current that has either a symmetric or asymmetrical biphasic waveform.¹⁷ In symmetric biphasic PC, the bidirectional PC is equal and balanced, whereas asymmetric biphasic PC produces a bidirectional current that is unequal and may or may not be balanced. Balanced asymmetric biphasic PC has no net positive or negative charge; unbalanced asymmetric biphasic PC creates a net positive or negative charge over time.¹⁷   

Application of an external electrical current to a wound is believed to mimic the body’s natural bioelectricity and to restart and stimulate endogenous electrical fields and as such, promote wound healing.^20-22 ES has been demonstrated in both in vitro^23-26 and animal in vivo²⁷ studies to enhance cellular activities such as collagen and DNA synthesis, ATP concentration, and generation of chemotaxic factors.^24-27 ES also has been shown in vitro and in vivo studies^25,27-31 to increase tissue perfusion, decrease edema, and promote angiogenesis and galvanotaxis compared to no ES stimulation, directing and accelerating the process of endothelial migration in the wound tissue to promote wound healing.

In a clinical study, Baker et al¹³ assessed 3 different forms of ES current for pressure healing among 192 PrUs in 80 patients with SCI who were treated for 45 minutes/day for 4 weeks. The authors reported ES enhanced PrU healing by measuring percentage changes of wound surface area per week in comparison with no ES in SCI. In addition, the authors identified asymmetric biphasic waveform of electrical current as the optimal wound healing protocol in comparison with microcurrent and without ES. Mittmann et al³² constructed a decision analytic model over a 1-year period to determine the incremental cost effectiveness of ES plus standard wound care (SWC), typically comprised of nonsurgical procedures such as debridement, dressing, nutritional, physical therapies, and surgical procedures for the management of complications in comparison with SWC alone in SCI with Stage III and Stage IV (per the NPUAP) PrUs. The authors assessed PrU healing using healing rates, recurrence rates, and complication rates; ES also reduced the cost of care in the SCI population. Furthermore, the most recent NPUAP/EPUAP clinical guideline⁵ recommends the use of ES to facilitate wound healing in recalcitrant Category/Stage II PrUs as well as any Category/Stage III and Stage IV PrUs in patients with SCI. However, the lack of consistency in the use of stimulation mode and parameters, together with the small sample size in the individual published trials, makes it difficult for health professionals and health providers to make clinical decisions on the implementation of ES treatment for PrU. 

Purpose

The purpose of this quantitative meta-analysis was to increase understanding of how different settings of ES affect PrU healing. Pooled analysis that quantitatively calculates weighted averages of findings across multiple trials can increase the statistical power of the existing small sample size of individual studies, enriching understanding of inconsistent results encountered across individual studies.

The aims of this review were 1) to assess the effect of ES as an adjunctive therapy for PrU on the weekly healing rate in people with SCI when compared to sham stimulation or no ES treatment; 2) to explore whether different types of ES currents and electrode placement have any influence on the healing rate of PrUs; and 3) to examine whether ES treatment worsens PrU in SCI as compared to no ES treatment.

Methods

Literature search. The original systematic review protocol³³ registered in the PROSPERO database in July 2013 (www.crd.york.ac.uk/PROSPERO; registration number CRD42013005088) was updated to include more recent research up to July 3, 2014. Material from the original study plus new findings are analyzed. As before, full reports of randomized, controlled trials (RCTs) and nonrandomized, clinical controlled trials (CCTs) were identified through searches of the Medline, Embase, the Cumulative Index for Nursing and Allied Health Literature (CINAHL), PsycINFO, and the Cochrane Central Register of Controlled Trials without language restrictions. Search terms included spinal cord injury, electrical stimulation, and pressure ulcer. All searched hits were exported to Endnote (Endnote version X7 for Windows, Thomson Reuters). All titles and abstracts were screened for eligibility, and the full text of potentially relevant articles was retrieved and considered for inclusion by the first author. Each stage of the selection process was cross-checked by the second author.  Any disagreement was discussed or consulted by the third author.

Literature inclusion/exclusion criteria. 

Target population. Persons with SCI and any categorical grade or any number of PrUs irrespective of age, gender, and level and degree of severity of traumatic or nontraumatic injury were included. Studies with a mixed-study population that included individuals with SCI were included if the ulcer outcomes were reported/analyzed separately for SCI participants. 

Type of intervention. All types of ES using 2 or more surface electrodes placed on the wound bed or in the edge of wound bed were included.

Type of studies. RCTs and CCTs that compared any type of ES against SWC consisting of cleansing, dressing, debridement and nutrition without ES or sham ES that were published in an indexed, peer-reviewed journal between January 1985 and July 2014 were included. Conference abstracts and university theses were excluded. 

Outcome. The publication needed to report ulcer outcome measurement (eg, wound size or average healing rate per day, per week, or during whole study period).

Data extraction and methodological quality. The following data were extracted from eligible articles by 1 reviewer (LL) and cross-checked by the second reviewer: year of publication, country of author, and type of study design. All other data, including quality assessment, were assessed independently by 2 reviewers. This included sample size; participant age, gender, and type and level of SCI; the type of ES; the duration and pattern of stimulation; electrode placement; follow-up duration; and adverse events. Additionally, data extraction included outcome measures on the percentage change in wound surface area or changes in ulcer size. Any disagreement in assessed findings between the 2 independent reviewers was resolved by discussion or through consultation with a third reviewer. 

Each publication was subjected to a quality assessment. For RCTs, a Jadad score (University of Oxford, Oxford, UK) was used together with the item allocation concealment and consideration as to whether the analysis was based on the randomized groups.^33-35 A modified Downs and Black tool (London School of Hygiene and Tropical Medicine, London, UK) was used for CCTs.^36,37 Both scales are well-established tools for assessing and reporting the quality of clinical and health-related studies in the literature. The Jadad score independently assesses the methodological quality of a clinical trial and has known reliability and external validity.³⁷ It contains an assessment — namely, risk of bias (selection bias, performance bias, detection bias, attrition bias) — and is relatively easy to use. The Jadad score addresses items relating to randomization, blinding, and description of withdrawals and dropouts, with scores ranging from 0 to 5 (trials scoring 3 or greater are considered to be of reasonably good quality). In addition to the Jadad score, 2 extra items were added: allocation concealment and intent-to-treat (ITT) analysis, which deal with reporting bias and performance bias for open-label (nonblinded) trials. Allocation concealment was considered adequate if patients and investigators who enrolled patients could not foresee treatment assignment. ITT is defined as an analysis that demonstrates inclusivity of all randomized participants based on specified criteria and includes all randomized patients in the groups to which they were randomly assigned, regardless of 1) their adherence with the entry criteria, 2) the treatment they actually received, and 3) subsequent withdrawal from treatment or deviation from the protocol.³⁴ The Downs and Black tool³⁷ consists of 27 questions that evaluate the level of 4 domains: reporting, external validity, internal validity (both bias and confounding), and power. Each question was scored as Yes (1) or No/Unknown (0). Because question 5 addressed 2 components (Are the distributions of principal confounders in each group of subjects to be compared clearly described? A list of principal confounders is provided), the full score for the question was 2. Question 27 was modified slightly due to an ambiguity in the first component (Did the study have sufficient power to detect a clinically important effect where the probability value for a difference being due to chance is <5%? Sample sizes have been calculated?); only the second part of the question was assessed. For example, if the sample size was calculated by a trial, it was scored yes (1). The total score of the 27 questions was calculated by adding up the scores; thus, the highest score any reviewed article could receive was 28. It should be noted that scores increased in line with the methodological quality of the study; higher scores indicated higher methodological quality.³⁷ 

Data analysis. Data were extracted to a spreadsheet. A quantitative pooled analysis was performed to estimate the pooled ES treatment effect on weekly healing rates, the number of ulcers healed, and the incidence of ulcers worsening. All trials included in this review defined ulcer healing in terms of changes in wound surface area either per week, per day, or during the whole study follow-up. Because the daily healing rate has limited clinical relevance, for those trials that reported percentage of ulcer decrease per day or during the whole study period, the weekly healing rate was calculated and used for pooled analysis. Weekly healing rate was defined as the mean percentage change in ulcer size per week. Review Manager (Review Manager (RevMan), Version 5.3. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014) was used to pool the healing rate per week and the number of ulcers completely healed and ulcers that worsened among the studies. 

All data irrespective of the length of treatment and follow-up were analyzed. Weekly healing rate was compared between patients who had ES and patients who had no ES treatment. Subgroup analysis was performed for good quality RCTs. The weekly healing rate between PC and constant DC and electrode overlaid versus placed at edge of ulcer were compared. For those trials with more than 2 arms, the ES arm with the largest sample was included for comparison with the control arm (no ES/sham ES). Treatment effect was significant if P<0.05. Heterogeneity between studies was tested with the use of the chi-square test (significant if P <0.1) and I² test (with substantial heterogeneity defined as values >50%). When studies showed significant heterogeneity (I² >50%), the Mantel–Haenszel random effects model was used to calculate mean difference. Otherwise, the fixed effects model (I²  <50%) was used to calculate the pooled effect sizes when studies did not show heterogeneity.

Results

Studies. The literature search identified a total of 407 unique references; all were exported to Endnote, along with 3 additional articles identified from other sources. Of these 410 articles, 127 were identified as duplicates, resulting 283 abstracts and titles. These were further screened for eligibility, generating 80 potentially relevant abstracts that were retrieved and considered for inclusion in the final review. Of these, 8 (6 RCTs^13,38-42 and 2 nonrandomized CCTs^43,44) met the inclusion criteria and were subjected to full-data extraction and quantitative analysis. Figure 1 provides a flow chart of the process and results for screening eligibility and study selection. 

All 8 studies described the study target population as persons with SCIs who had at least 1 PrU. The number of patients per study ranged from 7 to 150, with the number of ulcers studied ranging from 7 to 192. Four (4) studies (N = 415 ulcers) measured mean daily percentage change in ulcer size,^41-44 1 study (N = 192 ulcers) measured the mean weekly percentage change in ulcer size,¹³ and 3 studies (N = 58 ulcers) measured mean percentage change in ulcer size across the entire study period.^38-40 Six (6) out of 8 trials (N = 509 ulcers) compared PC ES to sham/no ES treatment,^13,38-41,44 1 trial (N = 50 ulcers) compared constant current ES to sham ES treatment,⁴² and 1 (N = 150 ulcers) compared PC ES to constant current ES therapy or sham ES.⁴³ For stimulus pulse settings, stimulation varied from 40 Hz to 100 Hz in frequency and from 50 V to 150 V (or 4 mA to 45 mA) in intensity.

In terms of electrodes placement, in 3 studies^38-40 (N = 58 ulcers) the electrodes were overlaid on wound bed, in 4 studies (N = 557 ulcers) the electrodes were applied to intact skin around the wound,^13,41,43,44 and in 1 (N = 50 ulcers) ES treatment compared electrodes overlaid on the wound bed to electrodes placed on intact skin around the ulcers.⁴² Details of sample characteristics are shown in Table 1. 

Methodological quality. One (1) of the 6 RCTs described an appropriate method to generate the randomization sequence,⁴⁰ 2 were double-blinded and described the method of double-blinding,^39,42 3 adequately described allocation concealment,^38-40 and 2 used ITT to analyze the data.^40,41 Two (2) RCTs were considered to be of reasonably good methodological quality according to the Jadad score along with 2 other items; hence, they were classified as low risk of bias trials.^39,40 The remaining 4 RCTs were considered to exhibit moderate risk of bias.^13,38,41,42 Two (2) nonrandomized CCTs were assessed for their reporting quality using the Down and Black tool, scoring 13 and 8, respectively, out of a total achievable score of 28 and subsequently considered relative high risk of bias trials.^43,44 

Data pooling and meta-analysis.

Effectiveness of ES. ES effectiveness was assessed according to mean weekly healing rate (ie, average percentage change per week in ulcer size), the number of ulcers healed, and the incidence of ulcers worsening (defined as wound size increased during study period), comparing different ES settings and/or how ES performed versus sham or no treatment. 

With regard to overall healing rate by ES versus sham/no ES, the pooled analyses of the 7 relevant trials showed people receiving ES treatment in addition to conventional wound treatment (which involved cleansing, dressing, nutrition, and debridement as necessary) reporting a higher weekly healing rate than those without ES treatment by 4.97% (MD 4.97, 95% CI 1.97-7.98, P = 0.001) (see Figure 2). However, heterogeneity among the studies was substantial (I² = 83%, P<0.00001). A subgroup analysis of RCTs considered to be of good methodological quality showed a trend toward a higher weekly healing rate in people treated with ES than people without ES treatment, but the pooled effect was not significant (P = 0.07). 

When healing rate by PC ES versus sham/no ES was assessed, the pooled analysis of the 6 trials^13,38-41,43 showed a significantly higher weekly healing rate in people who were treated with PC ES than those without ES treatment (MD 6.27, 95% CI 2.77-9.78, P = 0.0005, I²  = 74%( (see Figure 3). 

When healing rate by constant DC versus sham/no ES was compared, the pooled analysis of the 2 trials in which constant current ES was applied showed a nonsignificantly higher weekly healing rate in people treated with constant current than those without ES (MD 4.50, 95% CI 1.19-10.18, P = 0.12, I²  = 0% (see Figure 4). 

With regard to healing rate by PC versus DC ES treatment, 1 CCT⁴³ compared PC ES treatment versus DC for PrU healing. A higher weekly healing rate was achieved by PC ES: 5.43% to 4.40% per day versus 3.11% to 3.83% per day, respectively (P = 0.03). 

Healing rate by electrode placement also was assessed (ie, active electrode overlaid the wound bed versus sham/no ES). A meta-analysis of the 4 trials^38-40,42 that applied the active electrodes directly on the wound found a significantly higher rate with ES irrespective of current type than without ES (MD 9.01, 95% CI 2.02-16.00, P = 0.01, I² = 90%) (see Figure 5).  

When electrode placement on intact skin was analyzed, the pooled analysis of the healing rate for the 4 trials^13,41-43 where both electrodes were placed on intact skin/the edge of wound versus sham/no ES showed a significantly higher weekly healing rate in people who received ES than those who received no ES (MD 7.71, 95% CI 1.59-13.83; P = 0.01, I2 = 79%) (see Figure 6). 

The healing rate when the active electrode overlaid the wound bed was compared to electrodes placed on intact skin/the edge of wound. One (1) study⁴² compared the effect of ES delivered by applying the electrodes either directly on the wound bed or on the edge/intact skin around the ulcer versus sham ES treatment. In group 1, the positive electrode overlaid the ulcer and 4 negative electrodes were laid around the ulcer; in group 2, 2 electrodes were laid on intact skin at the ulcer edge across the wound; and in group 3, 2 electrodes were laid on intact skin at the ulcer edge across the wound without ES delivery. The authors reported electrodes that overlaid wound bed achieved a higher healing rate than electrodes placed on intact skin around the ulcer or sham ES group (1.6%/day overlaid versus 4.8±1.5%/day versus 4.2±11%/day). 

Two (2) trials^13,40 addressed the number of ulcers completely healed by ES versus sham/no ES. Both trials reported a higher number of ulcers completely healed in the ES treatment group (52% and 37%, respectively^13,40) compared to sham/no ES treatment (24% and 28%, respectively^13,40). Pooled analysis of these 2 trials showed significantly higher numbers of ulcers (N = 226 ulcers) healed with ES treatment (OR 2.68, 95% CI 1.17–6.14, P = 0.02, I²  = 0%) (see Figure 7). 

Two (2) studies^40,41 reported the incidence of ulcers that worsened during the study period compared to sham/no treatment. Both trials reported lower number of ulcers worsened in individuals who had ES treatment (N = 143 ulcers). However, the pooled analysis of these 2 trials showed the difference was nonsignificant (OR 0.38, 95% CI 0.12–1.24, P = 0.11, I²  = 18%) (see Figure 8). 

Adverse events. Only 1 of the 8 studies⁴⁰ reported adverse events. The authors indicated some patients experienced minor adverse reactions related to ES, which included red, raised, itchy skin beneath the large dispersive electrode. One (1) patient had a persistent (>24 hour) redness or burn under the active electrode, presumably from too high a stimulus intensity, which resolved within 48 hours.

Discussion

ES has been recommended for use in the treatment of PrUs in recent (2014) NPUAP/EPUAP guidelines, yet the specifics for ES are not clear. The comparison of ES current types and placement of electrodes reported in the present review should provide new insights for clinicians who treat PrU in the SCI population. Of the 8 studies that met inclusion criteria and were included in this review, 6 were RCTs^{13, 38-42} and 2 were nonrandomized CCTs.^43,44 Two (2) of the 6 RCTs^39,40 were classified as having good quality of evidence according to the Jadad scale; they used allocation concealment and ITT analysis. The other 4 RCTs^13,38,41,42 were classified as moderate quality, and the remaining 2 nonrandomized^43,44 CCTs provided a relatively low level of evidence. As a whole, the 8 trials provided a moderate level of evidence.

In terms of effectiveness, the quantitative pooled analysis of the 7 controlled trials showed an average higher weekly healing rate during the treatment period when patients received ES in addition to SWC of cleansing, dressing, nutrition, and debridement as necessary. Of the 8 trials included in the review, 2 studies^13,40 (N = 226 ulcers) reported the number of ulcers completely healed during the study period (OR 2.68, 95% CI 1.17–6.14); significantly more PrUs healed with ES treatment in comparison to sham ES or no ES treatment (P = 0.02). Two (2) trials^40,41 reported fewer ulcers worsening when patients received ES treatment. These 2 trials also showed a trend toward higher weekly healing in the ES group, although the difference was not significant between ES treatment and control groups. 

In addition to supporting the recommendations of the most recent NPUAP/EPUAP clinical guidelines⁵ regarding the application of ES for recalcitrant PrU healing in persons with SCI, the current findings are also in agreement with previous studies demonstrating ES enhances PrU healing in the SCI population⁴⁵ and chronic wound healing in the non-SCI population.^11-16 A systematic review conducted by Lala et al⁴⁵ reported the risk of PrU healing during the study period (20 days to 3 months) together with daily healing rate (percentage decreased per day) in SCI. The authors concluded ES seems to be an effective adjunctive therapy to accelerate and increase PrU closure in individuals with SCI. In the current review, the calculated weekly healing rate was anecdotally suggested by clinicians and tissue viability specialists to be more clinically relevant than simply describing the positive outcomes of previous research. In addition, the types of ES current and placements of electrodes, presented along with the incidence of worsening PrUs, should be of interest to clinicians.  

The constant DC that involves unidirectional continuous flow of current for longer than 1 second has been associated with an antibacterial effect in PrU healing, but it can cause chemical and thermal burns.⁴⁶ This type of ES was employed in 2 of the studies^42,43 reviewed. The most commonly used ES for PrU healing in the review was PC that involved no sinusoidal, interrupted current flow for a brief period of time. It is suggested that PC ES more closely mimics the “current of injury” necessary for triggering tissue healing by sustained activation of the voltage-gated sodium channels in the surrounding tissues.²⁴ As compared with continuous DC stimulation, PC ES may carry a lower risk of possible skin burns and a greater depth of penetration.^10,24,46,47 PC ES was utilized in 6 out of 8 studies (N = 465 ulcers).^13,38-42 Pooled analysis of 6 trials showed PC ES significantly improved weekly healing rate compared with no ES. 

Three (3) studies involved placing the active electrode directly on the wound bed and the negative electrode on the intact skin around the edge of the ulcer.^38-40 Four (4) studies reported the negative and positive electrodes were placed on opposite sides of the PrU on intact skin.^13,41,43,44  One (1) study⁴² compared electrode placement (1 group of participants received ES by applying the ES with positive electrode overlaid on the ulcer and 4 negative electrodes laid around ulcer, while the other group received ES by applying same ES program with 2 electrodes laid on the intact skin at the ulcer edge across wound; the participants in the control group received sham ES treatment with 2 electrodes laid on the intact skin at the ulcer edge across wound). The authors found participants who received ES by electrodes overlaid on the wound bed had a higher healing rate than the participants who received ES by electrode placed surrounding the wound. 

Electrode polarity has long been thought a complex issue in the literature. For instance, anodal stimulation was shown to increase fibroblast migration,^31,48 while cathode stimulation enhanced keratinocyte migration²² and increased fibroblast proliferation.⁴⁶ Both anodal and cathode stimulation have an antibacterial effect, with cathode stimulation seeming to have greater antibacterial effects.^48,49 In the current endeavor, only 1 study⁴² compared electrode configuration by either placing the active electrode in the wound and the dispersive electrode at a distance from the ulcer versus placing both electrodes on the edge of ulcer. Although the average weekly healing rate was significantly higher when active electrodes overlaid the wound surface than when electrodes were placed surrounding the wound, this study was not a RCT and was classified as low level of evidence with high risk of bias. Such results should be interpreted with caution. Thus, the assessment of the different effects between 2 types of electrodes placement for PrU healing is inconclusive. Future preclinical, in vivo models and clinical trials examining the impact of electrode configuration on PrU healing are warranted.

Limitations

Although systematic reviews and meta-analyses have their own merits in terms of increasing the statistical power of the small sample size of individual studies, conducting such analyses often presents a number of limitations. These include publication bias (particularly against negative findings), language restrictions, heterogeneity across each studies, and coding of keywords. The small number of relevant trials, together with substantial heterogeneity in this review, made it difficult to interpret some findings and draw firm conclusions. Higher heterogeneities evident across the trials in this review can be explained by the variation of study design and stimulation parameters (stimulation frequency, intensity, waveform) and stimulation device used. 

Another limitation of the study was the use of the Jadad scale for assessing methodology quality of RCTs. Although the Jadad scale is a well-established tool and is widely used for assessing and reporting the quality of clinical and health-related studies in the literature, it has shortcomings. The Jadad scale is criticized for being oversimplistic, placing too much emphasis on blinding and exhibiting low consistency between different raters. Furthermore, it does not take into account allocation concealment. However, in this review, 2 assessment items (allocation concealment and ITT analysis) were added. The methodological quality of CCTs was assessed using the Downs and Blacks tool, a well-established assessment tool used in SCI literature³⁵; however, it features no cut-off point for definition of good or poor CCTs. Future reviews should consider using 1 assessment tool for both RCTs and CCTs. Nevertheless, the methodology for each article also was assessed independently by 2 authors, and consensus was achieved and disagreement was discussed between them.  

A further limitation is the exclusion of non-English language literature. Although adding non-English articles may have strengthened the current review, the language restriction cannot be avoided due to lack of interpretation resources. To minimize the limitation, the authors adopted a well-structured search strategy that was approved by a clinical librarian, supplemented all “explode” functions, and utilized hand searches as well as contacting specialists to minimize the potential bias. 

In addition to types of ES current and electrode placement, other parameters (such as material, size of electrodes, level of injury, quality of life, hospital stay, pain, and cost to patients and carers) also may have an impact on PrU healing. Unfortunately, incomplete reporting of such data was identified in the current review — for instance, only 1 trial⁴⁰ in this review reported the level of injury and the majority of trials failed to report the size or material of electrodes used for ES treatment. Such data should be reported in future clinical studies.

Conclusion

ES appears to help facilitate PrU healing in the SCI population. Pulsed DC ES confers better benefits for PrU healing than constant DC. PrUs in people who had ES treatment seem more likely to completely close and less likely to worsen than ulcers in people who had no ES treatment. ES has been recommended for Stage III and Stage IV ulcers and for recalcitrant Stage II PrU healing by the NPUAP/EPUAP, yet the NICE guideline⁸ recommends not to use ES for PrU healing. Health professionals and the health service need well-designed clinical studies involving large sample populations to determine the optimal stimulation parameters and stimulation location with the most beneficial effect on the enhancement of PrU healing in SCI. Although an electrode directly placed on the wound bed may be more efficient than all electrodes placed on intact skin around the wound, more rigorous preclinical studies and clinical trials on determining the optimal stimulation parameters (eg, type of ES current  — in particular, constant DC versus PC that were commonly used for PrU healing in SCI), locations of electrodes, material, and size of electrodes are warranted. To better understand the exact physiological basis of ES for enhancing PrU healing, research is urgently needed in the form of more preclinical in vivo models to identify the optimal mode of ES current and electrode placement (polarity). 

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Potential Conflicts of Interest: none disclosed 

Dr. Liu is a research fellow, Centre for Critical Research in Nursing and Midwifery; and Ms. Moody is a senior lecture in adult nursing, Department of Adult, Child and Midwifery, School of Health and Education, Middlesex University, London, UK. Dr. Gall is a consultant physician, London Spinal Cord Injury Centre, Royal National Orthopaedic Hospital, London, UK. Please address correspondence to: Liang Q. Liu, MBBS, PhD, Middlesex University, London, UK, Department of Adult, Child and Midwifery, The Burrghs, Hendon Campus, London  NW4 4BT UK; email: liangqinl@hotmail.com.

Abstract

Enteroatmospheric fistulas (EAFs) represent a challenging problem in patients with an open abdomen (OA). A retrospective, descriptive study was conducted to evaluate the effects of enteral alimentation on wound status and management and nutrition.

All patients with an EAF in an OA treated between October 2012 and December 2014 at a university hospital in Germany were included without criteria for exclusions. Demographic and morbidity-related data collected included age, gender, surgeries, OA grading, body mass index (BMI), serum albumin, and serum creatinin. Underlying diseases and time between the index operation and the formation of the OA and EAFs were analyzed in relation to the initiation of enteral nutrition (EN), which can aggravate and contaminate the OA due to intestinal secretions necessary for digestion. The OA was described in size and area of the fascia defect and classified according to the Björck Scale. The number and location of the fistulas and the duration of negative pressure wound therapy (NPWT) were documented. Outcome parameters included fistula volume, wound management (eg, dressing change frequency, need for wound revision), feeding tolerance, systemic impact of nutrition, nutrition status at discharge, and mortality. Data were analyzed using primary descriptive statistics. The Mann-Whitney test was used to evaluate changes in fistula volume and BMI; categorical data were compared using Fisher’s exact test. A P value <0.05 was considered significant. Ten (10) patients (8 women, median age of participants 55.4 [range 44–71] years) were treated during the study time period. Seven (7) patients had the first fistula orifice in the upper jejunum (UJF); 8 had more than 1 fistula. EN was initiated with high caloric liquid nutrition and gradually increased to a 25 kcal/kg/day liquid or solid nutrition. All patients were provided NPWT at 75 mm Hg to 100 mm Hg. EN was not followed by a significant increase of median daily fistula volume (1880 mL versus 2520 mL, P = 0.25) or the need for more frequent changes of NPWT dressings (days between changes 2.6 versus 2.9, P = 0.19). In 9 patients, the severity of wound complications such as inflammation or skin erosion decreased both in frequency and magnitude (eg, affected area). All patients achieved a sufficient oral intake, but only 3 were discharged from the hospital without parenteral nutrition. In this study, EN did not cause additional problems in wound management but did not provide sufficient alimentation in patients with a UJF. Prospective studies are needed to clarify associations between EN, nutrition, and wound management. 

Abstract

Mucosal discoloration of an intestinal stoma may indicate self-limited venous congestion or necrosis necessitating operative revision. A common bedside technique to assess stoma viability is the “test tube test”.

A clear tube is inserted into the stoma and a hand-held light is used to assess the color of the stoma. A technique (video-assisted test tube test [VATTT]) developed by the authors utilizes a standard video bronchoscope inserted into a clear plastic blood collection tube to visually inspect and assess the mucosa. This technique was evaluated in 4 patients (age range 49–72 years, all critically ill) with a discolored stoma after emergency surgery. In each case, physical exam revealed ischemic mucosa at the surface either immediately after surgery or after worsening hypotension weeks later. Serial test tube test assessments were ambiguous when trying to assess deeper mucosa. The VATTT assessment showed viable pink mucosa beneath the surface and until the fascia was revealed in 3 patients. One (1) patient had mucosal ischemia down to the fascia, which prompted operative revision of the stoma. The new stoma was assessed with a VATTT and was viable for the entire length of the stoma. VATTT provided an enhanced, magnified, and clearer way to visually assess stoma viability in the postoperative period that can be performed at the bedside with no adverse events. It may prevent unnecessary relaparotomy or enable earlier diagnosis of deep ostomy necrosis. Validity and reliability studies are warranted. 

Abstract

Surgical site infection (SSI) is one of the most frequent postoperative complications among patients undergoing elective colorectal surgery. A multisite, prospective cohort study was conducted to investigate whether the thickness of subcutaneous fat (TSF) influences the occurrence of SSI in patients undergoing colorectal surgery. Participants included patients scheduled to receive colorectal laparotomy for colorectal cancer and who were under the care of a wound ostomy continence nurse at 17 participating general hospitals in Japan.

Patients were not eligible to participate if they had undergone emergency surgery, reoperation, or laparoscopic surgery. Demographic, wound, and surgical data and American Society of Anesthesiologists (ASA) scale scores were collected and assessed, along with nutritional status, TSF, body mass index, and risk factors for SSI (ie, length of surgery and wound classification). The incidence of SSI and nutritional conditions was assessed weekly for 30 days after surgery. Of the 155 participants (mean age 68.9 ± 10.8 years, 53 [34.2%] of whom were women), 90 (58.1%) underwent rectal surgery, and the remaining 65 underwent colon surgery. Seventy-two (72, 46.5%) of the 155 patients underwent colostomy surgery; 24 (15.5%) developed a SSI. The mean onset of SSI was 7.3 ± 2.9 days after surgery and commonly observed in the stoma group when the ASA score was 3 or higher (P = 0.02). Patients who developed SSI resumed oral dietary intake later than those without SSI (7.4 days versus 4.6 days, P = 0.02). Multivariate analysis indicated TSF >15 mm (P = 0.01), Alb level <3.5 g/dL at postoperative days 14 (P = 0.03) and 21 (P = 0.02), and total protein level <6.8 g/dL at postoperative day 7 (P = 0.02) were statistically significantly correlated with SSI occurrence. These results suggest preoperative TSF and preoperative and postoperative serum albumin levels are independent risk factors for SSI in patients undergoing colorectal surgery, confirming current recommendations to maximize the preoperative nutritional status of patients in order to prevent major complications. The results also confirm obesity/TSF should be assessed preoperatively to ascertain the risk of SSI in patients undergoing colorectal surgery.  

Surgical site infection (SSI) is the most common health care-related infection, affecting approximately 31% of all hospitalized patients regardless of cause of admission.¹ According to the Japanese Healthcare Associated Infections Surveillance² (JHAIS) of 103 institutions and 6818 cases, between 1998 and 2011 the SSI rates among patients undergoing colorectal, colon, and rectal surgeries were 16.33%, 15.03%, and 19.02%, respectively. Higher rates of SSI associated with colon and rectal surgeries have been reported in Japan than in the United States according to the data provided by the National Healthcare Safety Network (NHSN) Report.³ However, the data collection period differed between the 2 countries in that study; patients were tested for SSI for an average of 5.7 days after surgery⁴ in the United States and for 29.8 days after surgery⁵ in Japan. This methodological difference may have increased identification of SSI in the Japanese study.

Among all surgical procedures, several risk factors of SSI have been identified, including length of surgery >180 minutes, wound classification according to the Centers for Disease Control and Prevention (CDC) guideline higher than class III, and an American Society of Anesthesiologists (ASA) score >3.^6-8 Because these risk factors are recognized, efforts have been made to control them nationally and internationally. Furthermore, several cohort studies^9-15 have indicated stoma placement and obesity may be associated with SSI risk. Utsumi et al¹¹ prospectively examined 12,015 Japanese patients who underwent gastrointestinal surgery and found stoma placement was a risk factor for the development of SSI. A prospective, observational multicenter study¹² (N = 61) conducted in Spain supports Utsumi’s findings; stoma placement was found to be an independent risk factor for SSI. Tang et al¹⁵ prospectively examined 2809 patients who underwent elective colorectal surgery and stoma placement and found an ASA score >2 was a risk factor for SSI. A prospective cohort study¹³ of 556 patients who underwent colorectal surgery identified stoma placement as an independent risk factor for SSI.

Body mass index (BMI) is a well-known indicator of obesity. However, because BMI is calculated from the patient’s height and weight, it may not accurately reflect thickness of subcutaneous fat tissue.

Recent SSI studies have focused on thickness of subcutaneous fat (TSF), which can be more objectively measured than BMI by using computer tomography.^16,17 A cohort study¹⁶ (N = 655) of patients who underwent midline laparostomy reported increased subcutaneous fat (odds ratio [OR] = 1.76 per 10% increase) was an independent risk factor for superficial incisional SSI. A cohort study¹⁷ examined 152 patients with colorectal surgery and found TSF was an independent risk factor for SSI.

However, a comprehensive investigation of the association between SSI and TSF has not been conducted. The purpose of this prospective cohort study was to determine whether perioperative TSF in patients undergoing selective colorectal laparotomy is associated with SSI.

Methods

Study settings. The institutional level inclusion criteria used in the prospective comparison in this cohort study stipulated participating institutions should be hospitals 1) where certified wound, ostomy, and continence (WOC) nurses care for digestive organ cancer patients; 2) where infection control practitioners manage infection across the institution; and 3) that participate in the Japan Nosocomial Infections Surveillance¹⁸ (JANIS) or JHAIS² studies conducted in accordance CDC guidelines⁸ for SSI prevention. WOC nurses working at 25 institutions that met the inclusion criteria were mailed invitation letters; 8 institutions declined participation. WOC nurses at the 17 remaining hospitals recruited consecutive patient participants who were scheduled to undergo a colorectal laparotomy for colorectal cancer. Patients were excluded from recruitment if they had undergone emergency surgery, reoperation, or laparoscopic surgery. All surgeries performed in the participating institutions were managed according to the World Health Organization (WHO) Guidelines for Safe Surgery¹⁹ and the CDC guidelines for SSI prevention and management.⁸ Thus, the perisurgical procedures in each hospital were considered standardized with regard to environmental, perioperative, and intraoperative procedures.

Ethical considerations. The study procedures were reviewed and approved by the internal review boards of the Graduate School of the International University of Health and Welfare and the 17 participating hospitals. Oral and written informed consent was obtained from each participant.

Measurements. Nutritional status, TSF, and BMI were assessed, along with SSI risk factors that included duration of the surgery, wound classification according to CDC guidelines, and ASA score >3. To evaluate nutritional status, subjective global assessment (SGA) was used, which comprised 3 categorical states: well nourished, moderate or suspected malnutrition, and severe malnutrition.²⁰ The SGA score was determined by nutritionists at admission.

TSF was measured using CT scan data initially obtained to confirm the cancer diagnosis before surgery. Subcutaneous tissue thickness under the umbilicus was automatically calculated by WOC nurses using the measuring tool of the CT machine. A likelihood-ratio test determined the TSF cutoff point as 15 mm.

BMI was categorized in accordance with the WHO guidelines²¹: underweight <18.5 kg/m²; normal, between 18.5 and 25 kg/m²; and overweight >30 kg/m².

Risk factors. Surgical duration was considered a risk factor if it exceeded the 75th percentile of the NHSN or JANIS standard. Wound classification was considered a risk factor if the wound was assessed as either contaminated or purulent/infected. The SSI risk score has been widely utilized by the NHSN and in other countries.^3,7,8

Data collection. Demographic data collected included age, gender, smoking status, history of diabetes, site and duration of surgery, surgical wound classification, stoma replacement, and the date oral intake resumed. Baseline data (including TSF, BMI, and serum Alb [albumin] and total protein [TP] levels) were collected before admission. Blood laboratory variables were followed-up weekly until 30 days after surgery. BMI was reassessed at postoperative days 7 and 14. SSI and the degree of contamination were diagnosed by the board-certified Infection Control Pharmacy specialist according to the NHSN criteria³ by physicians. All other variables were collected by WOC nurses. Once the participants were discharged, they were followed-up for 30 days after surgery. Data were collected from August 2011 to May 2013 and entered directly into a computer database. 

Statistical analysis. Normality of variables was verified using the Shapiro-Wilk test. The chi-square test was used to determine demographic differences between the patients who developed SSI and those who did not. Analysis of variance (ANOVA) was used to determine the correlation among the 3 SGA states to Alb level, TP level, TSF, and BMI. The Mann-Whitney test was used to compare the Alb level, TP level, TSF, and BMI. Significant variables derived from the t-test were included as independent variables in the univariate analysis. The final analysis was a multivariate analysis of variables found significant in the univariate analysis. In addition, 95% confidence intervals (CIs) also were calculated. Power analysis was performed before data collection with power and sample size calculations. The required minimum sample cases were 104 (power = 0.8, alpha = 0.1). All data were analyzed using standard statistical software (SPSS 21.0 for Windows, Chicago, IL).

Results

Participant demographics. In this study, 155 patients (53 [34.2%] women) were enrolled and followed-up until 30 days after surgery (see Table 1). Mean age (68.9 ± 10.8 years) did not differ significantly between the 2 groups. Of the 155 patients, 34.2% were women; 90 (58.1%) underwent rectal surgery, and the remaining 65 underwent colon surgery. Seventy-two (72, 46.5%) of the 155 patients underwent colostomy surgery. 

SSI rates. Nine (9) patients (5.8%) who underwent colon surgery and 15 patients (9.7%) who underwent rectal surgery developed SSI for an overall SSI rate of 15.5%. Among the 24 patients with SSI, 16 underwent colostomy surgery (22.2%; chi 0.67; P = 0.04). The mean onset of SSI was 7.3 ± 2.9 days after surgery. SSI was commonly observed in the stoma group when the ASA score was 3 or higher (P = 0.02).

Factors associated with SSI. The SGA score was lower in patients who underwent colostomy surgery than in those who did not (P<0.01); however, in colostomy surgery patients only, no significant relationship was found between SGA score and SSI incidence (P = 0.28). 

TSF >15 mm (P = 0.01), Alb level <3.5 g/dL at postoperative days 14 (P = 0.03) and 21 (P = 0.02), and TP level <6.8 g/dL at postoperative day 7 (P = 0.02) were statistically significantly correlated with SSI occurrence (see Table 2). The patients who developed SSI resumed oral dietary intake later than those without SSI (7.4 days versus 4.6 days, P = 0.02). The univariate analyses of stoma construction and low TSF, Alb level, and TP level as independent variables confirmed these variables were significantly associated with SSI. Logistic regression analysis showed Alb level (P = 0.02, adjusted OR [AOR] 0.29; 95% CI, 0.10–0.87) and TSF >15 mm (P = 0.01; AOR, 0.23; 95% CI, 0.07–0.78) were independent risk factors for SSI (see Table 3).

Discussion

The NHSN⁶ reported 1.9% of patients underwent 1 of 39 types of surgery, including colon surgery. The JHAIS reported that 16.3% of patients who underwent colorectal surgery had a SSI.² The overall SSI rate in this study was similar to the JHAIS rate. The results of this study suggest TSF before surgery and serum Alb level after colorectal surgery may be associated with an increased risk of SSI. 

This study showed TSF is an independent risk factor for SSI; this is consistent with other studies. An American study¹⁶ reported TSF >22.8 mm is a risk factor for SSI. One Japanese study¹⁷ reported TSF >20 mm is a risk factor for SSI. Of the 24 patients with SSI in the current study, 16 had TSF >15 mm. It is interesting that the SGA scores of 12 of the 16 patients with SSI classified them as well nourished, and none of the patients had a score of 0 (ie, severe malnutrition). This might indicate that SGA score does not precisely predict a likelihood of SSI after colorectal surgery but that preoperative TSF, a noninvasive and easily calculable index, might help clinicians estimate SSI risk. Clinicians might calculate TSF once the surgery is planned and provide support to the patient with regard to losing weight before surgery; the authors have developed a preoperative weight-loss program. Comprehensive SSI risk assessment according to TSF, patient weight, and SGA score would be beneficial.

This study showed patients who developed SSI resumed oral dietary intake later than those who did not develop SSI. The Enhanced Recovery After Surgery Program²² recommends minimizing the fasting period and resuming oral intake within 24 hours unless contraindicated. Furthermore, a systematic review²³ showed prolonged fasting reduces intragestational immunity. The results of this study support these existing recommendations. 

Stoma placement minimally influences the anastomosis site, compared with upper digestive tract surgery. Guidelines²² support its safety and effectiveness.²⁴ Perioperative malnutrition worsens the likelihood of infection by affecting immunity. The colon provides a specific barrier and immune functions.²⁵ The results of this study suggest the potential of early resumption of oral dietary intake helps avoid SSI in elective colorectal surgery.²⁶

CDC guidelines⁸ do not include malnutrition as a predictor of SSI. However, these guidelines recommend the use of nutritional assessment parameters such as serum Alb level to screen for malnutrition.⁸ Serum Alb level should not be used as the only index because levels readily fluctuate owing to other factors such as intracellular fluid status and surgical invasion. The European Society for Clinical Nutrition and Metabolism²⁴ sets thresholds for requiring perioperative nutrition management, which includes an Alb level of >3.0 g/dL. A clinical study²⁷ suggests surgical invasion demands double the level of protein catabolism and increasing energy consumption. Improving Alb level after surgery is challenging, but a continuity of care that addresses the importance of a well-balanced diet and exercise and providing education to patients before surgery would be a potentially beneficial nursing intervention. A clinical trial regarding preoperative education is warranted.

Limitations

This study has several clinically relevant limitations. The first involves the issue with generalizability because of the use of a convenience sampling method. Therefore, further studies with randomly selected patients are needed to confirm these results. In addition, because the half-life of serum Alb is 21 days, this index does not reflect immediate nutritional status. However, serum Alb is commonly examined in patients undergoing colorectal surgeries before surgery; thus, practitioners can conveniently evaluate the patient’s nutritional status.

Conclusion

A prospective cohort study involving 155 patients in 17 hospitals showed TSF >15 mm and low Alb levels are independent risk factors for SSI occurrence among patients undergoing colorectal surgeries. These study results confirm current recommendations to maximize the preoperative nutritional status of patients in order to prevent major complications and confirm that being overweight is a risk factor for SSI in patients undergoing colorectal surgery.

Acknowledgments

The authors acknowledge the nurses and surgeons of the 17 hospitals that participated in the data collection for this study. 

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25. Gustafsson UO, Scott MJ, Schwenk W, et al. Guidelines for perioperative care in elective colonic surgery: Enhanced Recovery After Surgery (ERAS^®) Society recommendations. Clin Nutr. 2012;31(6):783–800.

26. Lewis SJ, Andersen HK, Thomas S. Early enteral nutrition within 24 hours of intestinal surgery versus later commencement of feeding: a systematic review and meta-analysis. J Gastrointest Surg. 2009;13(3):569–575.

27. Brandi LS, Frediani M, Oleggini M, et al. Insulin resistance after surgery: normalization by insulin treatment. Clin Sci. 1990;79(5):443–450.

Dr. Nakagawa is Assistant Professor, The Jikei University Graduate School of Medicine Program in Nursing, Kokuryocho Chofu, Tokyo. Ms. Ohno, Dr. Ikeda, and Dr. Muto are Professors, Graduate School, International University of Health and Welfare, Tokyo, Japan. Please address correspondence to: Hiromi Nakagawa, Assistant Professor, The Jikei University Graduate School of Medicine Program in Nursing, 8-3 Kokuryocho, Chofu, Tokyo 182-8570; email: hiromin4@mail.goo.ne.jp.

Abstract

Although loop ileostomies are created to mitigate the risk of anastomotic leaks, their reversal is associated with significant morbidity. Complications such as ileostomy site hernia and wound infections are not uncommon. A retrospective study was conducted among 176 consecutive patients who had undergone ileostomy reversal between September 2009 and November 2012 at a tertiary care teaching hospital. The main purpose of the study was to compare differences in short-term outcomes associated with hand-sewn versus stapled anastomotic techniques and purse-string versus stapled/sutured skin closure versus wounds left to heal by secondary intention.

Primary outcomes analyzed were length of stay (LOS), wound infection rates, and incisional hernia occurrence. All variables were abstracted from electronic medical records. Surgical techniques used were based on surgeon preference. Categorical variables were compared using Pearson chi-square test or Fisher’s exact test. ANOVA and the Kruskal-Wallis test were used to compare closure technique, age, body mass index (BMI), and hemoglobin; ANOVA was used to compare the remaining continuous/ordinal variables. Anastomotic technique, age, BMI, and hemoglobin were compared using the t-test, and the Wilcoxon rank-sum test was used to compare the remaining continuous/ordinal variables. Age, BMI, and hemoglobin were compared using t-test, and Wilcoxon rank-sum test was used to compare the remaining continuous/ordinal variables. Univariate analysis for preoperative factors associated with postoperative hernia was performed as a secondary analysis due to hernia rates higher than reported in the literature. A P value <0.05 was considered statistically significant. Of the 176 patients (median age 53, median BMI 26), 53% were male. The number of hand-sewn and stapled anastomoses were similar (89 versus 87, respectively) and purse-string skin closures were more common (n = 108) than stapled (n = 45) closures or wounds left to heal by secondary intention (n = 23). The mean follow up time for all patients was 16.9 months (508 days, range 8–1406 days); the overall complication rate was 35.4%. LOS was shorter in the hand-sewn anastomoses than in the stapled anastomoses’ group (3.36 days versus 3.82 days, P = 0.028) due to a greater proportion of patients with shorter stay (44 out of 89 [49%] 1 to 2 days versus 28 out of 87 [32%], hand-sewn versus stapled, respectively). No statistically significant differences were found in short-term outcomes among the 3 skin closure techniques, including wound infections (8 out of 108 [7%] in purse-string versus 2 out of 45 [4%] in stapled/sutured versus 0 out of 23 [0%] in open wounds, P = 0.84). Ileostomy site hernia (16.5%) was associated with a significantly higher BMI (32.2 with hernia versus 26.1 without, P<0.0001) and longer follow-up time (25.1 months with hernia versus 11.5 months without, P = 0.0003). In this study, anastomotic and skin closure technique did not result in clinically important differences in short-term outcomes. The results suggest that, depending on BMI, preoperative loop ileostomy closure counseling of patients should include the risk of developing an incisional hernia.  

Abstract

Surgical repair of soft tissue defects of the knee and leg remains challenging. Using a case study approach, the anatomy of the popliteo-posterior intermediate cutaneous artery was examined, and a reverse island flap method was developed and implemented. After obtaining informed consent, 5 patients (1 woman, 4 men, age range 31 to 57 years) underwent the experimental use of a reverse island flap with a posterior thigh flap pedicled on the cutaneous vessels arising from the popliteo-posterior intermediate artery to repair soft-tissue defects of the knee and leg.

The defects were caused by burned skin below the knee (n = 1), progressive skin necrosis in the knee after fracture surgery (n = 2), and skin infections associated with diabetes mellitus (n = 2). Skin defect sizes ranged from 15 cm x 5 cm to 30 cm x 12 cm. These large defects did not heal spontaneously; wound duration ranged from 1 week to 1 year, and all patients had refused defect repair with free flaps. Patients received posterior thigh flaps pedicled on the popliteo-posterior intermediate artery with areas ranging from 17 cm x 6 cm to 25 cm x 12 cm. All patients were treated with antibiotics and local dressings (iodoform and alcohol) changed daily post surgery, and blood supply was monitored by assessing the texture and color of the flap and venous regurgitation (ie, vein drainage disturbance). Four (4) of the five flaps survived completely. In 1 patient, partial survival of the flap, which had a good blood supply despite a venous circulation disorder, occurred: in this case, complete survival was achieved after treatment with a retrograde fascial flap and skin grafting. The appearance and texture of all flaps were satisfactory (ie, patients underwent only 1 operation, healing time was approximately 2 weeks, flap quality was close to normal skin, the donor site closed directly, and the shape and function of the knee and leg recovered well). No donor site abnormality was observed, and no postsurgical infection occurred. More research is needed, but the use of a reverse island flap with a posterior thigh flap pedicled on the cutaneous vessels arising from the popliteo-posterior intermediate artery may be a feasible option to repair soft tissue defects of the knee and leg. 

Skin defects of the knee and leg are not common in the authors’ clinical practice where it has been observed that in patients who have undergone surgical knee reconstruction, soft tissue necrosis around the knee can rapidly lead to deep infection at the arthroplasty site, requiring prosthesis replacement or, in extreme cases, amputation. 

Currently, numerous surgical approaches utilize flaps for reconstruction in cases of lower limb soft tissue necrosis. A case study by Ries and Bozic¹ found a medial gastrocnemius transposition flap effectively covered distal defects over the tibial tubercle or patellar tendon in 11 patients with skin necrosis. Some case studies have recommended the use of anterolateral thigh flaps.^2-4 Chen et al² reported the use of an anterolateral thigh perforator flap achieved a satisfactory outcome in a 46-year-old man with a defect around the knee; Wang et al³ found reverse anterolateral adipofascial thigh flaps survived well and covered defects of the knee and proximal calf in 5 patients; and Yildirim et al⁴ reported anterolateral thigh flaps achieved good clinical outcomes in 8 patients with post-burn flexion contractures of the knee. Case reports of local muscle flaps such as medial gastrocnemius, distal sartorius, vastus lateralis medialis, and gracilis flaps also have been used for the repair of large defects in the knee and leg.^5-9 Jepegnanam et al⁵ reported the use of gastrocnemius flaps resulted in excellent or good outcomes in 8 patients with high-velocity, open-knee injuries. Busfield et al⁶ found extended medial gastrocnemius rotational flaps allowed effective reconstruction of chronic knee extensor mechanism deficiencies in 9 patients with and without total knee arthroplasty. Clavert et al⁷ noted the distal sartorius flap was effective for the treatment of a long-term, nonhealing wound below the tibial tubercle. In approximately 9 out of 13 patients, Larson et al⁸ reported reconstruction with vastus lateralis muscle flaps after Girdlestone arthroplasty for ulcers or chronic wounds affecting the hip joint resulted in satisfactory healing, with no need for further operative intervention. Tiengo et al⁹ reported distally based, secondary pedicle gracilis flaps allowed effective reconstruction of large soft-tissue, total-knee defects in 3 patients.

However, posterior and superior thigh flaps are pedicled on the medial popliteal, lateral popliteal, or popliteo-posterior intermediate artery, and thus have a wide pedicle that restricts flap rotation. Therefore, these flaps have limited utility for the treatment of skin defects in the anterior knee and leg. For patients who have undergone amputation, free flaps or anterior or posterior thigh flaps are required to repair the large skin defects of the stump. For poorly vascularized patients who are not transplanted with free flaps, anterior or posterior thigh flaps are the only choice to repair skin defects. In addition, anterior thigh flaps cannot cover large skin defects in the posterior popliteal fossa.^10,11 Thus, a novel flap is needed to provide an alternative method for the coverage of large skin defects on the knee and leg.

In 2006, the authors noted during resection of popliteal cysts that the cutaneous artery arising from the popliteo-posterior intermediate artery was large; subsequently, the authors hypothesized a posterior thigh flap pedicled on the cutaneous vessels would be suitable for the repair of soft-tissue defects of the knee and leg. Ten (10) cadavers were used to characterize the anatomy of the popliteo-posterior intermediate cutaneous artery, and a reverse island flap method was developed. Utilizing a case study approach, the anatomy was examined and the procedure subsequently was implemented in 5 patients. 

Methods and Procedures 

Anatomy. Ten (10) cadavers were used to confirm the anatomy of the popliteo-posterior intermediate cutaneous artery. The cadavers were donated by family members, and their use was approved by the Ethics Committee of First Hospital of Jilin University, China. The popliteo-posterior intermediate cutaneous arteries were evident in all 10 cadavers in this series. Seven (7) of the 10 arteries originated directly from the popliteal artery and 3 arose from its muscular branches, which terminate at the semimembranosus muscle (see Figure 1). Using vernier and micrometer calipers (Wollschlaeger, Germany), all measurements were recorded and standard deviation (SD) calculated (see Tables 1 and 2). Artery origins were located a mean of 28.50 ± 4.92 mm proximal to the midpoint between the medial and lateral femoral condyles. The average outer diameter of the branches at the origin site was 1.72 ± 0.12 mm. In 3 cases, a muscular branch supplying the semimembranosus extended medially from the artery 22.06 ± 3.77 mm distal to the origin. The average outer diameter and length of the muscular branches were 0.56 ± 0.05 mm and 17.42 ± 5.20 mm, respectively. 

The popliteo-posterior intermediate cutaneous artery passed between the medial and lateral gastrocnemius heads and penetrated the deep fascia 33.36 ± 5.39 mm distal to the origin. The average outer diameter of the branch at this point was 1.35 ± 0.12 mm. The artery then divided into descending and ascending branches. The descending artery accompanied the small saphenous vein and sural nerve along the posterior midline of the leg with no obvious branch. The average outer diameters of the descending artery were 0.59 ± 0.12 mm at the origin and 0.27 ± 0.12 mm at the terminus, and its average length was 161.58 ± 9.67 mm. The ascending artery passed along the intermuscular space between the semimembranosus, semitendinosus, and biceps femoris; it had 18 to 25 branches and a length >5.6 cm. Its average outer diameters were 0.95 ± 0.16 mm at the origin and 0.46 ± 0.15 mm at the branching point. The branches extended medially and laterally toward the back of the thigh, forming anastomoses with one another. The ascending artery anastomosed with the descending branch of the third perforating artery of the deep femoral artery 110.84 ± 9.18 mm proximal to the midpoint between the medial and lateral femoral condyles. The average outer diameter of the ascending artery at the anastomosis point was 0.84 ± 0.12 mm (see Figure 2). 

Clinical study. A reverse island flap with a posterior thigh flap pedicled on the cutaneous vessels arising from the popliteo-posterior intermediate artery was designed to repair soft-tissue defects of the knee and leg in 5 patients (1 woman, 4 men, ages 31 to 57 [mean 42] years) (see Figure 3). These patients were selected because the defects were caused by amputation, located in the posterior fossa, or were the result of poor vascularization due to diabetes mellitus, making the defect more difficult to treat. The defects were caused by scalded skin below the knee (n = 1), progressive skin necrosis in the knee after fracture surgery (n = 2), and skin infections associated with diabetes mellitus (n = 2). Skin defect sizes ranged from 15 cm x 5 cm to 30 cm x 12 cm, and flap areas ranged from 17 cm x 6 cm to 25 cm x 12 cm (see Table 3). The use of the reverse island flap was most suitable to repair the skin defects in these cases, based on anatomical characteristics and improved chances, in the authors’ experience, of surgical success. 

Insulin was used to control blood glucose concentration (<8 mmol/L) before surgery in patients with diabetes. In all patients, the most sensitive antibiotic was selected preoperatively based on the results of bacterial culture and drug sensitivity testing of wound secretions. Surgery was performed after antibiotic use had reduced wound secretion and fresh granulation tissue had formed. Antibiotics were continued for 1 week postoperatively. 

This study was approved by the Ethics Committee of Jilin University. The patients agreed to this surgical approach and provided written informed consent. The experimental protocol was established according to the ethical guidelines of the Helsinki Declaration and was approved by the Ethics Committee of First Hospital of Jilin University, China.

Surgical procedure. Under epidural anesthesia, each patient was placed in a lateral position. The flap was harvested from the back of the thigh according to defect size and shape. The flap axis was marked along the midline of the posterior aspect of the thigh, crossing the midpoint between the medial and lateral femoral condyles. The rotation point was located on the flap axis 3 cm above this midpoint. 

An incision was made from the medial edge of the flap to expose the subcutaneous and deep fascia. The deep fascia then was elevated, and the flap was dissected between the deep fascia and the muscle. Dissection continued until the midline of the posterior aspect of the thigh (the flap axis) was reached. The third perforating artery of the deep femoral artery was identified 11 cm proximal to the midpoint between the medial and lateral femoral condyles, and its proximal end, which penetrated the deep fascia, was cut and ligated. The lateral edge of the flap then was incised. The free flap was elevated from the proximal end toward the popliteal fossae, and the flap was dissected to the rotation point without exposing the vascular pedicle. The flap was rotated over the skin defect area and sutured in layers. Donor site defects involving <10 cm skin were sutured directly, and larger defects (>10 cm skin) were repaired by full-thickness skin grafts from contralateral inguinal regions. Inguinal region defects were sutured directly 10 days after skin grafting. All surgeries were performed by the same surgeons/authors; one handled all general postsurgical care. The incisions were topically treated with iodophor and alcohol daily, and patients received prophylactic oral antibiotics. Because none of the patients showed signs of infection, cultures were not taken.

Outcomes. All the patients experienced satisfactory outcomes: 1) they underwent a single operation and a short treatment period, taking 14 days to heal; 2) skin flap quality was close to normal skin; 3) the donor site closed directly, and seemed less traumatic than other type flaps; and 4) the shape  and function of the knee and leg recovered well.

Case Reports 

Case 1. Mr. K, an otherwise healthy 57-year-old patient, had undergone amputation of the right lower leg and developed cutaneous necrosis of 2 months’ duration. After surgical repair of the defect using the flap, blood circulation was determined to be good based on consideration of flap texture and color of the flap and venous regurgitation (ie, vein drainage disturbance). Mr. K was treated with orally administered cefuroxime (2.0 g) twice a day for 1 week. The incision received routine postsurgical topical treatment consisting of iodophor and alcohol daily. The sutures were removed after 14 days. The donor site was not primarily closed and healed after full-thickness skin grafting. During the 1-month follow-up period, the texture and color of the flap were normal, and the length of the knee was maintained for artificial limb installation (see Figure 4). 

Case 2. Ms. L is an obese 37-year-old woman (body mass index 33 kg/m²) with type 2 diabetes who developed scar contraction in the right popliteal fossa at the site of a deep second-degree burn sustained when she was 14 years old. Insulin was used to control the blood glucose concentration (<8 mmol/L) before surgery. After surgical repair of the defect using the flap, blood circulation (determined by flap texture and color and venous regurgitation) was good, but a venous circulation disorder developed on postoperative day 1 in a 7-cm x 3-cm area of the flap pinnacle. The flap was dark purple and swollen, and a line of demarcation between the normal flap and flap tip was noted. The affected skin was necrotic but was reactivated after treatment with a retrograde fascial flap with superagenual cutaneous artery pedicles and skin grafting. Ms. L was treated with orally administered cefathiamidine (2.0 g twice a day for 1 week). The incision was treated topically with iodophor and alcohol daily. Three (3) weeks postoperatively, flap texture and color were normal (see Figure 5). The donor site was closed primarily. 

Case 3. Mr. M, 31 years old and otherwise healthy, developed a skin infection and necrosis on the right lower limb 10 days after a traffic accident. After surgical repair of the defect using the flap, blood circulation was good. Mr. M was treated with orally administered cefathiamidine (2.0 g) twice a day for 1 week. The incision was topically treated with iodophor and alcohol daily. The sutures were removed after 14 days. During the 1-month follow-up period, the texture and color of the flap were normal (see Figure 6). The donor site was primarily closed. 

Case 4. Mr. N, a 46-year-old patient with type 2 diabetes, had skin necrosis of 40 days’ duration on the lower leg. Insulin was used to normalize the blood glucose concentration before surgery. After surgical repair of the defect using the flap, good blood circulation was observed. Mr. N was treated with orally administered cefuroxime for 1 week. The incision was topically treated with iodophor and alcohol daily. The sutures were removed after 14 days. The texture and color of the flap were normal postoperatively. The donor site was closed primarily.

Case 5. Otherwise healthy 40-year-old Mr. O developed skin necrosis 1 week after a traffic accident. After surgical repair of the defect using the flap, blood circulation was good. Mr. O was treated with orally administered cefuroxime (2.0 g) twice a day for 1 week. The incision was topically treated with iodophor and alcohol daily. The sutures were removed after 14 days. The texture and color of the flap were normal postoperatively. The donor site was closed primarily.

Discussion

This study describes the use of a reverse island flap with a posterior thigh flap pedicled on the cutaneous vessels arising from the popliteo-posterior intermediate artery. Because this flap is not a main artery flap, harvesting does not affect the blood supply of the thigh. In addition, cutaneous vessels arising from the popliteo-posterior intermediate artery are readily separated and rotated. This flap is sufficiently large to cover the entire knee and the middle and upper sections of the leg (see Figure 3). Overall, this type of operation is able to protect the arteries; in the authors’ experience, use of this surgical method to repair soft-tissue defects of the knee and leg arising from various causes, including chronic ulcers and sinuses, is feasible and safe. No postoperative infection occurred in any patient, possibly attributed to the prophylactic use of antibiotics.

To reduce the possibility of flap necrosis, damage to the blood vessel was carefully avoided by not exposing the pedicle excessively during separation. The pedicle also should not be rotated >180˚ or placed under excessive traction. If the donor site defect cannot be directly sutured, the flap should be free to avoid compression of the pedicle. In addition, the anatomic study showed the blood supply of the popliteo-posterior intermediate cutaneous arteries in the thigh extends 25 cm proximal of the popliteal crease and 5.5 cm lateral of the vascular axis. The largest flap created in this study was 30 cm x 12 cm, and no necrosis was observed. Thus, transplanted tissues should survive when a smaller area is involved. The authors’ preliminary anatomic study of cadavers showed the average pedicle length was 250.03 ± 9.24 mm, with no necrosis. Thus, flaps with pedicle lengths <250 mm should survive. In case 2, only partial flap survival was achieved due to poor venous circulation, possibly due to compression of the pedicle by thick fat tissue in this obese patient. Necrosis developed in the flap due to poor venous return. Thus, care should be taken to avoid pedicle compression in obese patients.

Barret et al¹² recommended the use of skin autografting, Z-plasties, and flaps to repair defects in the skin and subcutaneous tissues. The authors reached a conclusion based on personal experience that flaps should be considered for the reconstruction of defects that involve tissues underlying subcutaneous tissues; suitable flaps include direct cutaneous, musculocutaneous, perforator-based, expanded, and free flaps (microvascular tissue transfer). Flap selection is based on individual patients’ conditions. In case 2 described here, the removal of scar tissue from the popliteal fossa created large soft-tissue defects. Z-plasty was not suitable for the repair of these defects due to the poor elasticity of the surrounding skin; also, Z-plasty could not improve knee joint function in this patient. The use of a reverse island flap with a posterior thigh flap pedicled on the popliteo-posterior intermediate artery achieved a satisfactory outcome in this obese patient with post-burn scar contraction.

Advantages. In the authors’ experience, this flap has several advantages. First, a local random-pattern skin flap has indistinct perfusion and is limited in size. The random-pattern skin flap aspect ratio is 2:1; if it is greater than the proportion, necrosis occurs. Defect repair using a cross-leg flap requires a long period of immobilization (eg, for 1 month post surgery) and several operative stages. Although a free flap can cover a defect successfully in a single-stage operation, the operating time is long and this procedure can be technically difficult due to the presence of deep recipient vessels.³ Because the popliteo-posterior intermediate cutaneous artery is located in the intermuscular space in the popliteal fossa and passes along the intermuscular septum, in patients with trauma on the back of the leg, the artery is readily separated and rotated.

This is first study of this surgical procedure to repair anterior soft-tissue defects of the knee and lower leg; the approach was found to be simple, safe, and reliable and shows great potential for clinical application. Also, the flap is supplied by the popliteo-posterior artery, which is located in the posterior compartment of the thigh and does not affect the normal anatomical structure. The medial gastrocnemius flap is most effective for coverage of distal defects over the tibial tubercle or patellar tendon,¹ but the removal of this flap thins the leg. In addition, the gastrocnemious flap can be used to repair large skin defects on the knee because the harvest area is large and located close to the knee. The anterolateral thigh flap is very large and thin, but the difficulty of perforator dissection and vascular anatomical variability constitute major disadvantages for their use.⁴ Finally, wounds with areas of <10 cm can close with no further treatment after the secondary skin graft.

Disadvantages. Use of the popliteo-posterior intermediate artery flap also is associated with several disadvantages. The distally based vastus lateralis muscle flap is too bulky to cover a knee defect, and donor site morbidity is a consideration.¹⁰ Fat is abundant in this region, especially in women, resulting in a thick flap that may cause venous circulatory disorders. For this reason, in the authors’ experience a secondary surgery is commonly required for skin transplantation and in case 2 was due to: 1) poor quality of the blood vessel due to a primary disease, such as diabetes (patients with rheumatoid arthritis, diabetes, or peripheral vascular disease have increased risks of wound healing complications¹¹); 2) poor local soft-tissue conditions because of bruising; and/or 3) poor refluence of the vein due to the large flap size.

Limitations

This study has several limitations. First, the sample was small (N = 5). Further studies with larger samples are required to confirm the efficacy and safety of this method and to confer a better understanding of when such surgery would be indicated. Second, this was a single-center study and the method has not been used in other centers. Some factors, such as the source of the patient, operation skills, and economic conditions may be center-specific and not generalizable to other facilities. Third, the hemodynamics of the flap’s blood supply have not been studied. A hemodynamic study should be performed to confirm the blood supply to the flap, thereby facilitating its accurate removal. Fourth, a long-term view of this surgical technique and prognoses is warranted.

Conclusion

This report is the first description of the use of the posterior thigh flap pedicled on the cutaneous vessels arising from the popliteo-posterior intermediate artery for the reconstruction of knee and proximal calf defects. In the authors’ experience, the advantages of this novel approach include the ability to repair large soft-tissue defects in this region and that it is a relatively easy surgical procedure. This approach seems to be most suitable for soft-tissue defects measuring <30 cm x 12 cm after amputation or in the posterior fossa in nonobese patients. Additional studies involving this surgical approach in more diverse populations and with long-term follow up are warranted. 

References

1. Ries MD, Bozic KJ. Medial gastrocnemius flap coverage for treatment of skin necrosis after total knee arthroplasty. Clin Orthop Relat Res. 2006;446(1)186–192.

2. Chen CY, Hsieh CH, Kuo YR, Jeng SF. An anterolateral thigh perforator flap from the ipsilateral thigh for soft-tissue reconstruction around the knee. Plast Reconstr Surg. 2007;120(2):470–473.

3. Wang XC, Lu Q, Li XF, et al. Reversed anterolateral thigh adipofascial flap for knee and proximal calf defects. Burns. 2008;34(6):868–872.

4. Yildirim S, Avci G, Akan M, Misirlioglu A, Akoz T. Anterolateral thigh flap in the treatment of postburn flexion contractures of the knee. Plast Reconstr Surg. 2003;111(5):1630–1637.

5. Jepegnanam TS, Boopalan PR, Nithyananth M, Titus VT. Reconstruction of complete knee extensor mechanism loss with gastrocnemius flaps. Clin Orthop Relat Res. 2009;467(10):2662–2667.

6. Busfield BT, Huffman GR, Nahai F, Hoffman W, Ries MD. Extended medial gastrocnemius rotational flap for treatment of chronic knee extensor mechanism deficiency in patients with and without total knee arthroplasty. Clin Orthop Relat Res. 2004;428(1):190–197.

7. Clavert P, Cognet JM, Baley S, et al. Anatomical basis for distal sartorius muscle flap for reconstructive surgery below the knee. Anatomical study and case report. J Plast Reconstr Aesthet Surg. 2008;61(1):50–54.

8. Larson DL, Machol JA 4th, King DM. Vastus lateralis flap reconstruction after girdlestone arthroplasty: thirteen consecutive cases and outcomes. Ann Plast Surg. 2013;71(4):398–401.

9. Tiengo C, Macchi V, Vigato E, et al. Reversed gracilis pedicle flap for coverage of a total knee prosthesis. J Bone Joint Surg Am. 2010;92(7):1640–1646.

10. Swartz WM, Ramasastry SS, McGill JR, Noonan JD. Distally based vastus lateralis muscle flap for coverage of wounds about the knee. Plast Reconstr Surg. 1987;80(2):255–265. 

11. Hemphill ES, Ebert FR, Muench AG. The medial gastrocnemius muscle flap in the treatment of wound complications following total knee arthroplasty. Orthopedics. 1992;15(4):477–480. 

12.  Barret JP. Burns reconstruction. BMJ. 2004;329(7460):274–276.

Potential Conflicts of Interest: This work was supported, in part, by the State Plan for Technology Research and Development of Jilin Province (no. 201101045).  

Dr. Sun is associate chief physician; Dr. Gong is chief physician; Dr. Song is visiting staff; Dr. Cui is associate chief physician; Dr. Yu is visiting staff; and Dr. Liu and Dr. Lu are chief physicians, Department of Hand Surgery, First Hospital of Jilin University, Jilin, China. Please address correspondence to: Lai-Jin Lu, MD, PhD, Department of Hand Surgery, First Hospital of Jilin University, Xin Min Avenue 1008, Changchun 130021, Jilin, China; email: kjkliubin@126.com. 

Abstract

Although it is among the most commonly used pressure ulcer risk assessment tools, the Braden Scale may lack strong predictive validity when used in the long-term care setting. A meta-analysis was conducted of English-language articles published in the PubMed database and Web of Science from the indices’ inception through July 2015 to assess the predictive validity of the Braden Scale for pressure ulcers in long-term care residents.

Search terms included pressure ulcer, pressure sore, bedsore, decubitus, long-term care, nursing home, skilled nursing facility, hospice, and Braden. Data extracted from the publications included sample and setting characteristics and predictive value indices. The pooled sensitivities, specificities, diagnostic odds ratios (DOR), and constructed summary receiver operating characteristic (SROC) curves were calculated. Eight studies (2 prospective cohorts and 6 cross-sectional studies) with 41 489 residents met selection criteria for inclusion in the analysis. The pooled sensitivity and specificity were 0.80 (95% CI: 0.79-0.81) and 0.42 (95% CI: 0.42-0.43), respectively, yielding a combined DOR of 5.66 (95% CI: 3.77-8.48). The area under the ROC curve (AUC) was 0.7686 ± 0.0478 (95% CI: 0.6749-0.8623), and the overall diagnostic accuracy (Q*) was 0.7090 ± 0.0402 (95% CI: 0.6302-0.7878). Significant heterogeneity was noted among the included studies; Q value was 302.54 (P = 0.000), and I² for pooled sensitivity, pooled specificity, and pooled DOR was 97.4%, 98.7% and 96.4%, respectively. Meta-regression analysis showed no heterogeneity was noted among Braden scale cut-offs (P = 0.123) and pressure ulcer prevalence P = 0.547). The evidence showed the Braden Scale has moderate predictive validity and low predictive specificity for pressure ulcers in long-term care residents. The development and testing of new risk assessment scales for this population is warranted.

Pressure ulcers are common in long-term care residents.¹ According to the 2004 National Nursing Home Survey² (NCHS), 159,000 nursing home residents (11%) in the United States had a pressure ulcer, most commonly Stage II. According to a case review,³ long-term care residents with pressure ulcers suffer pain, disfigurement, and decreased quality of life, and their risk of illness and death increases. A retrospective cohort study⁴ (N = 1539) shows residents in long-term care with pressure ulcers had a relative risk for dying of 1.45 (95% confidence interval [CI]: 1.30-1.65) as compared to those without ulcers after adjusting for clinical and functional status. The same study also shows litigation involving pressure ulcers is costly; residents realized some type of recovery against the facility in 87% of the cases (verdicts for the resident plus settlements) and were awarded amounts as high as $312 million in damages. 

Risk assessment is the first step in pressure ulcer prevention. The Braden Scale, the most widely used risk assessment scale, evaluates skin breakdown in 6 domains: sensory perception, moisture, activity, mobility, nutrition, and friction and shear.⁵ A systematic review⁶ showed the Braden Scale has optimal validation and the best sensitivity/specificity balance (57.1%/67.5%, respectively) and accurately predicts pressure ulcer risk (odds ratio = 4.08, CI 95%: 2.56-6.48). Many studies have examined the use of the Braden Scale for pressure ulcer prevention in long-term care. In a prospective cohort study, de Souza et al⁷ found the Braden Scale to have good predictive validity in elderly, long-term care residents, with sensitivity of 75.9% and 74.1%, specificity of 70.3% and 75.4% in cutoff scores of 18 and 17, and area under the receiver operating characteristic curve (AUC-ROC) of 0.79 and 0.81 at the first and last assessments. Braden and Bergstrom⁸ also reported a good predictive validity in long-term care, with sensitivity of 79%, specificity of 74%, 54% predictive value of a positive test, 90% predictive value of a negative test, and 75% correct classification rate. However, a prospective cohort study by Ramundo⁹ found the Braden Scale has limited predictive ability in long-term care. At a score of 18, the sensitivity of the tool was 100%, but the specificity was only 34%. The sample size in these studies was small; thus, use of the Braden Scale in long-term care remains controversial. 

The aim of this meta-analysis was to assess the predictive validity of the Braden Scale for pressure ulcers in long-term care residents.

Methods

Search strategy. Two (2) databases, PubMed and Web of Science, were searched for relevant English-language entries from database inception through July 2015. The search terms included pressure ulcer, pressure sore, bedsore, decubitus, long-term care, nursing home, skilled nursing facility, hospice, and Braden. The search strategy in PubMed was (“pressure ulcer” [MeSH Terms] OR “pressure ulcer*” [title/abstract] OR “pressure sore*” [title/abstract] OR “bedsore*” [title/abstract] OR “decubitus” [title/abstract]) AND (“long-term care” [title/abstract] OR “nursing home” [title/abstract] OR “skilled nursing facility” [title/abstract] OR “hospice” [title/abstract]) AND “Braden” [TW]. The search strategy in Web of Science was TS= (pressure ulcer* OR pressure sore* OR bedsore* OR decubitus) AND TS = (long-term care OR nursing home OR skilled nursing facility OR hospice) AND TS = Braden. The “related articles” function in PubMed and the “citing articles” or “cited articles” function in Web of Science also were utilized to broaden the search. 

Inclusion and exclusion criteria. Studies were considered for inclusion when they met the following criteria: 1) they discussed assessing the predictive validity of Braden Scale for pressure ulcer risk in long-term care residents; 2) they provided true positive (TP), false positive (FP), false negative (FN), and true negative (TN) for predicting pressure ulcer risk at different Braden Scale cut-offs; 3) they provided sensitivity and specificity, positive likelihood ratio, and negative likelihood ratio, and TP, FP, FN, and TN were calculated using a web-based program (ie, diagnostic test calculator, available at: http://araw.mede.uic.edu/cgi-bin/testcalc.pl). Two (2) authors independently judged study eligibility while screening the citations. Disagreements were resolved by a third author.        Data extraction and quality assessment. A spreadsheet developed by the authors was used to extract and record data on first author, year of publication, country in which the study was carried out, study design, year of participant enrollment, location, number of residents, gender and age of the participants, when in the pressure ulcer process the Braden Scale was used, pressure ulcer prevalence, Braden Scale cut-off, and the predictive TP, FP, FN, TN.

The Quality Assessment of Diagnostic Accuracy Studies¹⁰ (QUADAS) tool was used to assess the quality of the predictive validity studies. The QUADAS included 14 items. Each item of QUADAS is answered with “yes”, “no”, or “unclear”. Two (2) authors independently assessed study quality. Disagreements were resolved by a third author.

Statistical analysis. The overall pooled sensitivity, specificity, and diagnostic odds ratio (DOR), with 95% CI, were estimated using DerSimonian and Laird’s¹¹ random-effects model. In addition, summary receiver operator characteristic (SROC) analysis was performed to examine the interaction between sensitivity and specificity and to quantify test performance using the area under the curve (AUC) and overall diagnostic accuracy (Q*) value.¹² Heterogeneity was analyzed by Cochran’s Q test and I² statistic; a P value <0.05 by Cochran’s Q test and I²>50% indicated substantial heterogeneity. Meta-regression analysis was conducted to explore the heterogeneity. All analyses were performed using Meta DiSc 1.4 (version 0.6; accessed at www.hrc.es/investigacion/metadisc_en.htm).¹³ 

Results

Eligible studies. Eight (8) cross-sectional or prospective cohort studies^7,8,14-19 (total sample 41 489 residents) met inclusion criteria for meta-analysis. Figure 1 shows the flow diagram of study selection. The included studies were conducted in 7 countries: Brazil, The Netherlands, Germany, the United States, Canada, Saudi Arabia, and Australia. The participants were residents of nursing homes, long-term care facilities, tertiary care hospitals, veterans’ administration medical centers, and skilled nursing facilities. The pressure ulcer diagnoses all were based on the National Pressure Ulcer Advisory Panel²⁰ (NPUAP) guide and included Stage I through Stage IV. Pressure ulcer prevalence ranged from 6.4% to 30.1%. The Braden scale cutoff ranged from 17 to 20. The details of all 8 studies are shown in Table 1. The quality assessment results according to the QUADAS list for the individual studies can be found in Table 2. All 8 included studies met 80% “yes” in all 14 items.

Predictive validity in long-term care facilities. The predictive validities of the included studies are listed in the Table 3. The pooled sensitivity of the studies was 0.80 (95% CI: 0.79-0.81; χ² (11)= 420.74, P = 0.000), shown graphically in the forest plot in Figure 2a. The pooled specificity was 0.42 (95% CI: 0. 42-0.43; χ² (11) = 859.80, P = 0.000) (see Figure 2b), and the pooled DOR was 5.66 (95% CI: 3.77 to 8.48) (see Figure 2c). The overall weighted AUC was 0.7686 ± 0.0478 (95% CI: 0.6749-0.8623), and the Q* value was 0.7090 ± 0.0402 (95% CI: 0.6302-0.7878). The SROC curve is shown in Figure 2d. 

Study heterogeneity. The Cochran’s Q test value was 302.54 (P = 0.000). I² for pooled sensitivity, pooled specificity, and pooled DOR was 97.4%, 98.7% and 96.4%, respectively. The results showed significant heterogeneity among the studies; meta-regression analysis showed heterogeneity between Braden scale cut-offs (P = 0.123) and pressure ulcer prevalence (P = 0.547).

Discussion

A meta-analysis found the overall weighted AUC for Braden Scale assessment in long-term care was 0.7686 ± 0.0478 (95% CI: 0.6749-0.8623). An AUC value of 0.5 indicates the test has no discriminatory ability, whereas an AUC value of 1.0 indicates perfect diagnostic capability.²¹ The SROC curve was used in meta-analysis for diagnostic accuracy. An AUC of 0.97 or above indicates excellent accuracy, 0.93 to 0.96 is good and 0.75 to 0.92 is moderate, but an AUC <0.75 suggests obvious deficiencies in diagnostic accuracy.²² Thus, the results of this study indicate the Braden Scale has moderate predictive validity for pressure ulcers in long-term care residents. However, the predictive specificity is low, with the pooled specificity 0.42 (95% CI: 0.42-0.43), suggesting some deficiency of the Braden Scale for pressure ulcer risk assessment in long-term care residents. This result was the same as the study results reported by Ramundo.⁹ In that prospective cohort study involving 48 home care residents, the optimal predictive sensitivity was 100% and the specificity was 34% when Braden scale at cut-off was 18.

The Braden Scale evaluates skin breakdown in 6 domains: sensory perception, moisture, activity, mobility, nutrition, and friction and shear. In the 2004 NCHS,² some characteristics were found to increase the risk for pressure ulcer development in long-term care residents: age 64 years and younger, duration <1 year, and a history of recent weight loss. In a prospective cohort study conducted among 175 nursing home residents, Akca et al²³ found residents who were underweight, had lived at the rehabilitation center for a longer time, and followed feeding regimens had a higher risk of developing pressure ulcers (P<0.001). In a prospective cohort study involving 346 residents, Kwong et al²⁴ reported bedbound or chairbound residents, especially persons with comorbidities (renal failure and stroke), who lived in nursing homes where more nursing assistants than nurses provided care were at higher risk for pressure ulcer development. However, these risk factors are not included in the Braden Scale. 

The Braden Scale design was based on expert consensus.⁵ A recent data analysis of 6 pressure ulcer prevalence studies (2004–2009)²⁵ used Classification Tree Analysis (CHAID) to show all Braden Scale items are not equally important; for residents in long-term care facilities, friction and shear had the strongest association with pressure ulcer prevalence. 

Because a new risk assessment scale for long-term care residents may have better predictive validity than the Braden Scale, some new scales have been designed for this population. The interRAI Pressure Ulcer Risk Scale (interRAI PURS) is based on a logistic model and includes 7 independent variables: impaired in-bed mobility, impaired in walking, bowel incontinence, weight loss, history of resolved pressure ulcers, and shortness of breath. This scale has been shown in a retrospective cohort study²⁶ to have good distributional characteristics, and the c-statistic (a measure of discrimination among models) was 0.708, compared with a c-statistic 0.676 for the Braden scale. However, these results need to be confirmed by other large-sample prospective studies.

Limitations

The current meta-analysis has some limitations. First, significant heterogeneity was found among the studies. Meta-regression analysis showed the heterogeneity among the studies may be the consequence of different Braden scale assessment times (at admission, 48 to 72 hours after admission, and pre-breakdown), different facilities (long-term care, nursing home, and skilled nursing facility), different study enrollment times, and different countries, among other reasons. Second, because the included studies provided limited information, subgroup analysis according to different Braden scale assessment time, facilities, enrollment time, and country were not conducted. These limitations should be considered when evaluating the results.

Conclusion

A meta-analysis showed the Braden Scale has moderate predictive validity and low predictive specificity for pressure ulcers in long-term care residents. Additional research regarding more suitable scales for predicting pressure ulcer risk in this population are warranted. 

References

1. White-Chu EF, Flock P, Struck B, Aronson L. Pressure ulcers in long-term care. Clin Geriatr Med. 2011;27(2):241–258. 

2. Park-Lee E, Caffrey C. Pressure ulcers among nursing home residents: United States, 2004. NCHS Data Brief. 2009;(14):1–8.

3. Voss AC, Bender SA, Ferguson ML, Sauer AC, Bennett RG, Hahn PW. Long-term care liability for pressure ulcers. J Am Geriatr Soc. 2005;53(9):1587–1592. 

4. Berlowitz DR, Brandeis GH, Anderson J, Du W, Brand H. Effect of pressure ulcers on the survival of long-term care residents. J Gerontol A Biol Sci Med Sci. 1997;52(2):M106–M110.

5. Bergstrom N, Braden BJ, Laguzza A, Holman V. The Braden Scale for Predicting Pressure Sore Risk. Nurs Res. 1987;36(4):205–210.

6. Pancorbo-Hidalgo PL, Garcia-Fernandez FP, Lopez-Medina IM, Alvarez-Nieto C. Risk assessment scales for pressure ulcer prevention: a systematic review. J Adv Nurs. 2006;54(1):94–110. 

7. de Souza DM, Santos VL, Iri HK, Sadasue Oguri MY. Predictive validity of the Braden Scale for Pressure Ulcer Risk in elderly residents of long-term care facilities. Geriatr Nurs. 2010;31(2):95–104.  

8. Braden BJ, Bergstrom N. Predictive validity of the Braden Scale for pressure sore risk in a nursing home population. Res Nurs Health. 1994;17(6):459–470. 

9. Ramundo JM. Reliability and validity of the Braden Scale in the home care setting. J Wound Ostomy Continence Nurs. 1995;22(3):128–134. 

10. Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;10(3):25–38.

11. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1996,7(3):177-188.

12. Walter SD. Properties of the summary receiver operating characteristic (sROC) curve for diagnostic test data. Stat Med. 2002;21(9):1237–1256. 

13. ZJ, Abraira V, Muriel A, Khan K, Coomarasamy A. Meta-Disc: a software for meta analysis of test accuracy data. BMC Med Res Methodol. 2006;6:31–47.

14. VanGilder C, Macfarlane GD, Meyer S. Results of nine international pressure ulcer prevalence surveys: 1989 to 2005. Ostomy Wound Manage. 2008;54(2):40–54.

15. Tannen A, Dassen T, Halfens R. Differences in prevalence of pressure ulcers between the Netherlands and Germany — associations between risk, prevention and occurrence of pressure ulcers in hospitals and nursing homes. J Clin Nurs. 2008;17(9):1237–1244. 

16. Lahmann NA, Halfens RJ, Dassen T. Pressure ulcers in German nursing homes and acute care hospitals: prevalence, frequency, and ulcer characteristics. Ostomy Wound Manage. 2006;52(2):20–33.

17. Tannen A, Bours G, Halfens R, Dassen T. A comparison of pressure ulcer prevalence rates in nursing homes in the Netherlands and Germany, adjusted for population characteristics. Res Nurs Health. 2006;29(6):588–596. 

18. Lahmann NA, Halfens RJ, Dassen T. Prevalence of pressure ulcers in Germany. J Clin Nurs. 2005;14(2):165–172. 

19. Bergstrom N, Braden B, Kemp M, Champagne M, Ruby E. Predicting pressure ulcer risk: a multisite study of the predictive validity of the Braden Scale. Nurs Res. 1998;47(5):261–269. 

20. National Pressure Ulcer Advisory Panel (NPUAP). Prevention and Treatment of Pressure Ulcers: Quick Reference Guide. Available at: www.npuap.org/wp-content/uploads/2014/08/Quick-Reference-Guide-DIGITAL-N.... Accessed August 5, 2016.

21. Swets JA. Measuring the accuracy of diagnostic systems. Science. 1988;240(4857):1285–1293. 

22. Jones CM, Athanasiou T. Summary receiver operating characteristic curve analysis techniques in the evaluation of diagnostic tests. Ann Thorac Surg. 2005;79(1):16–20. 

23. Akca NK, Aydin G, Gümüs K. Pressure ulcers and their associated factors in nursing home inmates. J Coll Physicians Surg Pak. 2015;25(1):27–30. 

24. Kwong EW, Pang SM, Aboo GH, Law SS. Pressure ulcer development in older residents in nursing homes: influencing factors. J Adv Nurs. 2009;65(12):2608–2620. 

25. Lahmann NA, Tannen A, Dassen T, Kottner J. Friction and shear highly associated with pressure ulcers of residents in long-term care — Classification Tree Analysis (CHAID) of Braden items. J Eval Clin Pract. 2011;17(1):168–173.

26. Poss J, Murphy KM, Woodbury MG, et al. Development of the interRAI Pressure Ulcer Risk Scale (PURS) for use in long-term care and home care settings. BMC Geriatr. 2010;10:67.

Dr. Chen, Dr. Shen, and Dr. Liu are associate professors, School of Nursing, Nantong University, Nantong, Jiangsu, PR China. Please address correspondence to: Peng Liu, MD, Nantong University, Qi Xiu Road 19# Nantong City, Jiangsu Province. 226001 China PR: email: pphss@126.com. 

Abstract

Infection following orthopedic implants for bone fixation or joint replacement is always serious and may require removal of the osteosynthetic material. Negative pressure wound therapy with instillation and dwell time (NPWTi-d) is an emerging therapy for the treatment of complex wounds, including infected wounds with osteosynthetic material. The purpose of this case study was to evaluate the outcomes of 4 patients (1 man, 3 women; age range 49 to 71 years) with a postoperative wound infection (POWI) following fracture repair and internal fixation. All patients were at high risk for surgical complications, including infections. Standard infection treatments (antibiotics) had been unsuccessful. Based on the available literature, a NPWTi-d protocol was developed.

Following surgical debridement, wounds were instilled with polyhexanide biguanide with a set dwell time of 15 minutes, followed by continuous NPWTi-d of -125 mm Hg for 4 hours. The system was changed every 3 to 4 days until sufficient granulation tissue was evident and negative pressure without instillation could be used. Systemic antibiotics were continued in all patients. Granulation tissue was found to be sufficient in 12 to 35 days in the 4 cases, no recurrence of infection was noted, and the osteosynthesis material remained in place. No adverse events were observed. Research is needed to compare the safety and effectiveness of this adjunct treatment in the management of challenging wounds to other patient and wound management approaches. 

Abstract

The certified nursing assistant (CNA) is the caregiver who frequently identifies the first signs and symptoms of pressure ulcers (PUs) in the long-term care setting. A quality improvement effort was implemented to explore the effect of a 1-hour CNA education program about early identification, treatment, and prevention of PUs on PU knowledge, PU incidence, and PU prevention interventions, including skin checks. All 33 CNAs employed in a care facility for residents 55+ years old were invited to participate.

CNA demographic and PU education variables were obtained. PU knowledge was assessed using the Pressure Ulcer Toolkit questionnaire before, immediately after, and 3 months following the educational intervention about PU prevention. PU incidence data were abstracted from monthly quality assurance reports for the 3 months pre-intervention and 3 months post intervention. Patient medical records were mined for data on turning/repositioning, skin checks, and informing care staff of suspicious areas of skin for the 3 months pre- and post educational intervention. Data for percent of short-stay residents (<90 days) with PUs were collected via the quarterly Medicare Nursing Home Compare Quality Measures report for this facility before and 3 months after the educational intervention. Pre-intervention and post-intervention PU incidence was statistically analyzed using the t-test. The CNA demographic survey was administered using an anonymous pencil-and-paper format and hand-tabulated by the primary investigator. Of the 31 CNAs surveyed (mean age 32 years [range 18–65], mean years of experience 7.7 years [SD = 8.1, range 0.5–40], 26 (84%) reported they received training regarding PU prevention in the classroom during their initial CNA training, and 81% received on-the-job training at some point in their careers regarding PU prevention. The Quality Indicator report showed a reduction from 5 PUs to 0 (12.3%) in the 3 months pre-intervention to 0% in the 3 months post-intervention. CNA reporting of skin breakdown increased by 68% from 8 reports to 17. CNA training regarding PU identification and prevention measures did not significantly improve knowledge scores, but the rate of PU development was significantly lower and the number of documented skin assessments and PU interventions higher after the education program. Additional studies to evaluate the effect of CNA education on the rate of PU development in nursing homes are warranted.  

Abstract

Hypergranulation tissue formation around a gastrostomy tube insertion site is a common feeding tube-related complication that affects patients who receive long-term enteral nutrition. Some clinicians recommend use of a topical corticosteroid in patients with gastrostomy tube insertion site hypergranulation. However, documentation is scant regarding appropriate treatment for this condition. This case report describes a 67-year-old bedridden man with spinocerebellar degeneration who presented with hypergranulation at the site of the gastrostomy tube, inserted 1 week earlier. The tissue was raw and inflamed, with bleeding and exudation.

The gastrostomy site was gently cleansed with gauze dampened with tap water, and topical 0.05% clobetasol propionate ointment was applied directly to the hypergranulation tissue twice daily. After 4 days of treatment, the hypergranulation tissue almost completely disappeared, redness markedly decreased, and bleeding and exudation ceased, with no recurrence observed during the 6 months of follow-up. This case study supports other reports that short-term corticosteroid treatment may be a safe, quick, noninvasive, and effective treatment for hypergranulation at the gastrostomy tube insertion site. Further studies are needed to evaluate the safety, effectiveness, appropriate dosage, and duration of topical corticosteroid for the treatment of hypergranulation tissue. 

Abstract

Despite advancements in the creation and care of stomas, ostomy and peristomal skin complications are common immediately following surgery as well as in the months and years thereafter. A prospective study to determine the prevalence of ostomy and peristomal skin complications and the influence of ostomy configuration on such complications was conducted 1 year after ostomy surgery among all patients at a university hospital in Sweden.

All participants received regular (10 to 14 days post discharge, 6 weeks, 3 months, 6 months, and 1 year post surgery) ostomy follow-up care by a wound ostomy continence (WOC) nurse. All consecutive elective and emergency patients who had undergone surgery to create a colostomy (end colostomy), end ileostomy, or loop ileostomy were eligible to participate. Patients who were reoperated during their first year post-surgery, patients with a urostomy, and patients with double ostomies were excluded from the study. Patient data collected included age, gender, diagnosis, elective or emergency surgery, open or laparoscopic surgical procedure, presence of a colorectal surgeon specialist at surgery, type of ostomy (colostomy, end ileostomy, loop ileostomy), preoperative ostomy siting, counseling, body mass index, American Society of Anesthesiologists classification, and radiation and/or chemotherapy status. Ostomies were evaluated by 4 WOC nurses as to stoma configuration, convexity use, patient self-sufficiency in stoma care, and complications. All 207 patients (53% women) who were eligible agreed to participate in the study. Patient median age was 70 years (range 19–94); 74% underwent elective surgery. Main diagnoses were colorectal cancer (62%) and inflammatory bowel disease (19%). Ostomy types were: colostomy (71%), end ileostomy (26%), and loop ileostomy (3%). One or more complications occurred in 35% of the patients (27% ostomy complications, 11% peristomal skin complications). A colostomy hernia was the most common surgical complication (20%), and significantly more women (69%) and emergency surgeries were noted among patients with a colostomy and an ostomy height of ≤5 mm. The use of convexity was significantly more common among patients with a stoma height of ≤5 mm than patients with stomas >5 mm (P = 0.016) and among patients having emergency operations than among patients having elective surgery (P = 0.045). Of the emergency surgeries, 37% had not been ostomy-sited (P<0.0001). With regular WOC nurse follow-up, the prevalence of peristomal skin complications in this population was low, and adequate ostomy height might have prevented the frequent use of convexity. Explorative studies are needed that consider differences in body configuration when determining optimal stoma height, especially for patients who require emergency surgery. 

According to retrospective and prospective studies, review articles, and best practice guidelines in the ostomy field,^1-3 ostomy-related complications can affect daily life for the patient. Assessment, management, and follow-up of ostomy and peristomal skin complications such as parastomal hernia, stomal prolapse, stomal stenosis, peristomal irritant contact dermatitis, and peristomal candidiasis dermatitis are critical to help patients succeed in adapting to a new life with an ostomy.^1-3 Although significant advances, such as the enhanced recovery after surgery protocol⁴ to optimize recovery (key components include preoperative carbohydrate loading, no overnight fasting, immediate postoperative diet, no nasogastric tubing, avoidance of drainage and early postoperative structured mobilization, and pain control) and new surgical techniques such as laparoscopic surgery⁵ and laparoscopic stoma formation⁶ that are now available for ostomy surgery along with newly developed ostomy equipment and ostomy care, ostomy-related complications are common. A systematic British review¹ reported complication occurrence of between 10% and 82%. Evaluating and comparing studies is difficult due to factors such as study design, retrospectivity, patient selection, and differences in follow-up time. Systematic reviews of clinical retrospective and prospective studies and clinical guidelines^1,2,8-10 demonstrate ostomy and peristomal skin complications also differ as to their definition and association with the different ostomy types. 

Correct preoperative ostomy siting, surgical construction of the ostomy, and careful follow-up of patients have been described in retrospective and prospective studies and systematic reviews^8,11,12 as the most important factors in the prevention of ostomy-related complications. In a recent British retrospective study¹³ to determine the incidence of and risk factors for intestinal ostomy complications, significantly more complications were shown in patients who had not been preoperatively sited. The time of onset and presence of 10 specific complications were recorded for 1216 patients (mean age 64 years) with an intestinal stoma over 10 years at 2 hospitals; musculoskeletal comorbidity, diagnosis of cancer, emergency surgery, and high American Association of Anesthesiologists (ASA) score,¹⁴ which assesses the fitness of patients before surgery, also were associated with an increased risk of complications in the study. 

In a prospective British study¹⁵ that included 3970 stomas in patients from 93 ostomy care services, 34% were evaluated as problematic within 3 weeks of surgery. Ostomy height had the greatest individual influence on the incidence of a problematic ostomy; body mass index (BMI) and emergency surgery were shown to be significant risk factors for developing ostomy-related complications. In a previous prospective study¹⁶ at the authors’ institution, 180 patients with a colostomy (n = 122, median age 69), end ileostomy (n = 20, median age 59), or loop ileostomy (n = 38, median age 61) were followed over a 2-year period regarding ostomy height and diameter and its relation to complications. The results showed that 3 months after surgery, the end colostomies and end ileostomies had decreased in diameter by a mean of 10 mm and in height by 4 to 5 mm. The height and diameter of the stoma decreased postoperatively as part of the healing process, including reduction of mucosal edema of the stoma itself and postoperative abdominal edema. After 3 months, the size and shape of the stoma were generally established. However, almost all patients with an end ileostomy or loop ileostomy and with an ostomy height <20 mm had leakage and skin problems, as did half of the patients with an end colostomy and an ostomy height <5 mm. Thus, the height of the ostomy may affect the outcome of ostomy-related complications.^15,16 

Findings from a systematic review³ including 4 different cross-sectional studies (N = unclear) and 3 longitudinal studies (N = 5037) to determine the influence of intestinal ostomy surgery on health-related quality of life (HRQOL) showed impairment regarding HRQOL domains was most severe during the immediate postoperative period,  improved most dramatically during the third postoperative month, and continued to improve gradually during the first operative year. This is in line with a previous explorative prospective study¹⁷ at the authors’ institution where 57 patients who received an end colostomy because of rectal cancer completed a validated HRQOL questionnaire (Short-Form-36) preoperatively and 3 times during the 6-month follow-up period. The HRQOL post surgery (3 times) showed a significant drop in HRQOL occurred at 1 month compared to preoperatively; at 6 months, significant differences were noted in physical and emotional role functions and social function compared to a matched reference population. As reported in these studies,^3,17 HRQOL tends to steadily rise during the first postoperative year after ostomy surgery. Moreover, 1 year after ostomy surgery, patients could be expected to have recovered from their surgery and after any necessary additional treatments could start their new life. 

The aim of this study was to prospectively describe the prevalence of ostomy and peristomal skin complications 1 year after ostomy surgery. A secondary aim was to describe ostomy configuration (diameter, height, and shape) and its influence on ostomy and peristomal skin complications. 

Methods

This explorative study was based on clinical assessments of ostomy and peristomal skin complications 1-year post surgery, with patients consecutively included from September 2009 to March 2012. The study took place at a university hospital in Sweden. All elective and emergency patients who had undergone surgery to create a colostomy (end colostomy), end ileostomy, or loop ileostomy were prospectively included. Patients who were reoperated during their first year post surgery, patients with a urostomy, and patients with double ostomies were excluded from the study. The included patients had regular postoperative follow-up by a wound ostomy continence (WOC) nurse on the ward and at the outpatient WOC nurse clinic at the following intervals: 10 to 14 days post-discharge, 6 weeks, 3 months, 6 months, and 1 year post surgery. Four (4) WOC nurses with a median professional experience of 15 years (range 5–23) in evaluating ostomy and peristomal skin complications performed the assessment 1 year post surgery.

Study variables and assessment. All variables included in the study were based on a review of the literature and an earlier study performed at the authors’ institution.¹⁶ The study variables were evaluated and recorded on a specially designed case report form developed for the study by the researchers. Demographic data included age, gender, diagnosis, elective or emergency surgery, open or laparoscopic surgical procedure, presence of a colorectal surgeon specialist at surgery, type of ostomy (colostomy, end ileostomy, loop ileostomy), preoperative ostomy siting (Yes/No), and counseling (Yes/No). The preoperative ostomy siting was performed according to recommendations from the Wound Ostomy Continence Nurses Society and the American Society of Colon and Rectal Surgeons.¹⁸ Variables to assess patient physical condition at the time of surgery were BMI and ASA classification,¹⁴ the latter a measurement of physical health, coexisting medical disease, and physiological stability (grade I = healthy person, grade II = mild systemic disease, grade III = severe systemic disease,  and grade IV = severe systemic disease that is a constant threat to life). The presence or absence of preoperative radiation treatment and chemotherapy treatment also were recorded due to possible influence on complications (see Table 1).^2,19,20 

Ostomy complications. Ostomy complications were assessed using the definitions established by validation in the study by Colwell and Beitz.⁹ The stomal and peristomal definitions was content-validated by 686 WOC nurses. The overall content validity index was 0.91, demonstrating high consensus validation on the stomal and peristomal definitions. The ostomy complications evaluated in the present study included parastomal hernia (a defect in abdominal fascia that allows the intestine to bulge into the parastomal area), stomal retraction (the disappearance of normal stomal protrusion in line with or below skin level), stomal stenosis (impairment of effluent drainage to narrowing or contracting of the stoma tissue at skin of fascia level), and stomal prolapse (telescoping of the intestine through the stoma and granuloma). According to Lyon,²¹ a specialist dermatologist in stoma care, granulomas are characterized by papular, benign tumors appearing around stomas; they have a cauliflower appearance, are friable, bleed easily, usually occur at the mucocutaneous junction, and often precipitate stoma appliance leaks. They are caused mainly by fecal irritation.²¹ At the time of the present study, prophylactic mesh was not used for prevention of a parastomal hernia. When the WOC nurse detected a parastomal hernia at follow-up, the colorectal surgeon was consulted to determine the final diagnosis. A CT was not used routinely in the clinical setting in the diagnosis of a parastomal hernia. 

Peristomal skin complications. Peristomal skin complications were evaluated according to Classification of the Peristomal Skin (CPS).²² The variables included in CPS are detailed in Table 2. The classification was developed by a WOC nurse and a dermatologist who evaluated peristomal skin in 57 patients with ileal conduit urinary diversions (37 men and 20 women, mean age 61 years, time after surgery 3 to 14 years). The peristomal skin was evaluated at 2 unspecified separate occasions, and the macroscopic status of the peristomal skin was recorded on a case report form and further documented by color photographs of the peristomal skin. Analyses of these observations and color photographs formed the basis for a CPS. 

Peristomal skin status was categorized as: 1) no signs of irritative skin lesions E0/P0; 2) erythematous-erosive skin lesions, divided into mild, E+, and severe E++; and 3) pseudoverrucouse lesions divided into mild, P+, and severe P++. The different type of skin lesions can appear separately or in combination. Peristomal skin complication in the present study was documented in the case report form according to Table 2; if an ulcer was not included in the CPS, an open-ended question was added to document possible causes for peristomal skin complications. The CPS has been used to follow-up ostomy complications in both urinary and fecal ostomies by WOC nurses in Sweden since its development.

Ostomy configuration. A half-circular ostomy guide consisting of different sizes in mm was used to measure ostomy diameter and height as in a previous study.¹⁶ The diameter of the ostomy was measured at the base and the shape (round or oval), and >3-mm differences in diameter (using a clock-style guide) and height (distance of the ostomy lumen from the skin) noted. This ostomy guide is generally used at the follow-up of all patients with an ostomy at the clinic and was not developed specifically for this study. A low ostomy was classified as ≤5 mm for an end colostomy and ≤20 mm for an ileostomy. 

Skin care and self-sufficiency in ostomy care. Skin care instructions were provided during preoperative counseling as well as postoperatively in the hospital when the patient started learning about the stoma and stoma care. The WOC nurse provided at least 1 patient education session postoperatively and also a discharge consultation. Skin care also was discussed and assessed during counseling at follow-ups during the first year. The patient’s ability to manage the ostomy by him/herself was evaluated by the WOC nurse at every follow-up at the clinic through conversation with the patient and observation. 

Type of appliance. Convexity was assessed for patients using a 1-piece or 2-piece appliance. Convexity was defined according to an overview²³ of peristomal skin complications as the outward curving of a baseplate that provides support to the ostomy and prevents the ostomy from lying flush to the skin or retracting. Convex appliances are used with retracted and low ostomies to prevent leakage and peristomal skin complications. 

Data and statistical analysis. All study variables were transferred to a data file and divided into 2 categories: patients with complications and patients without complications 1 year post surgery. Descriptive statistics were reported as mean, SD, median, interquartile range, and range based on the level of measurement for the outcome variable. Because the data were not distributed normally, inferential analysis was based on nonparametric analysis techniques. Continuous variables were analyzed using the Mann-Whitney U test. Categorical data were analyzed with Fisher’s Exact and chi-squared tests. A P value of <0.05 was considered significant. Data were analyzed using IBM SPSS Statistics for Windows, Version 22.0 (Armonk, NY). 

Ethical considerations. The patients were informed about the study both orally and in writing at the outpatient clinic and gave their informed consent in writing. Patient confidentiality was secured by assigning a unique code that was entered into the data sheet. The coding list was stored separately in a locked cabinet. The research project was approved by the regional ethical review board in Gothenburg (Reg. no. Ö176-03) and followed the declaration of Helsinki guidelines. 

Results 

Clinical data. The study included 207 patients (53% women) with a median age of 70 years (range 19–94 years) of whom 153 (74%) underwent elective surgery. The main diagnoses were colorectal cancer (128, 62%) and inflammatory bowel disease (40, 19%). A colorectal surgeon specialist participated in all elective and emergency operations. Ostomy types included colostomy (146, 71%), end ileostomy (54, 26%), and loop ileostomy (7, 3%). Among participants, 182 (88%) had their ostomy location evaluated and marked preoperatively, 164 (79%) received preoperative counseling by a WOC nurse, and 183 (88%) were self-sufficient in ostomy care (see Table 1). 

Complications. Of the 207 patients, 73 (35%) had 1 or more complications, 56 (27%) had ostomy complications, and 23 (11%) had peristomal skin complications. No significant differences were noted between patients who had undergone elective surgery versus emergency surgery or those who had or had not been preoperatively ostomy sited (see Table 1). Of the 54 (26%) patients that had undergone emergency surgery, 20 (37%) were not sited preoperatively compared to 5 of 153 (3%) patients who had nonemergent surgery (P<0.0001). Of the emergency surgeries, 24 (44%) had an ASA classification of III+IV, compared to 41 (27%) in the elective group (P = 0.03). 

Ostomy complications. Overall, 56 stomas (27%) had ostomy complications at 1 year: 29 (20%) with a colostomy and 3 (6%) with an end ileostomy had a parastomal hernia evaluated by the WOC nurse. Of the 29 patients with a colostomy, 24 were evaluated as having a parastomal hernia by the surgeon, 4 were not examined, and for 1 patient the surgeon was uncertain of the diagnosis. The 4 patients that were not examined by a surgeon did not experience any problems with the colostomy hernia and were residing in nursing homes. Twenty-two (22) patients (76%) with a colostomy hernia experienced complications that included a dragging/heavy sensation, a dull ache, leakage (3), bowel evacuation problems, clothing problems, and anxiety. Sixteen (16) patients used a hernia belt, and 6 used a support belt. All 3 patients with an end ileostomy and a hernia were worried and concerned about their hernia. 

Additional complications at 1-year follow-up included granulomas almost equally distributed between the ostomies (13 patients, 6.3%), retraction (5 patients, 2.4%), stenosis (3 patients, 1.4%), and prolapse (2 patients with a colostomy, 1%). 

Peristomal skin complications. Among all patients with peristomal skin complications (23, 11%), 9 patients (6%) had a colostomy and 14 (23%) had an end ileostomy or loop ileostomy (P = 0.002). Among the patients with peristomal skin complications, 16 had mild erythematous-erosive skin lesions (E+), 5 had severe erythematous-erosive skin lesions (E++), and 2 had ulcerations diagnosed as pyoderma gangrenosum (see Table 2).

Peristomal skin complications were related to 3 factors (see Figure 1): the construction of the ostomy (stenosis, sliding ostomy, ostomy opening/lumen at skin level); peristomal skin disease (unspecific dermatitis around the ostomy, candidiasis, pyoderma gangrenosum, no obvious reason, and skin irritation at the outer part of the appliance); or appliance- or routine-related issues (pressure from convexity, ostomy appliance worn for too long, rich hair growth, leakage, or the ostomy appliance opening was too large). 

Ostomy shape and height and clinical variables. The majority of colostomy and end ileostomy sites in this study were round (89%, 130 colostomies and 48 ileostomies ). The ostomy configurations in different ostomy types are shown in Table 3. Sixty-one (61) patients (41.8%) with a colostomy had an ostomy height ≤5 mm (see Table 4); these included significantly more women (P = 0.002). In addition, significantly more emergency surgeries were noted among persons with an ostomy height of ≤5 mm (P<0.045). A colostomy height of ≤5 mm was significantly associated with the presence of a parastomal hernia (P = 0.020) and use of convexity (P = 0.016). No significant differences in complications were noted in end ileostomies ≤20 mm compared to >20 mm, although 15 patients (39.5%) used convexity in ostomies with a lower ostomy height compared to 3 (18.8%) of the ileostomies >20 mm (see Table 4).

Type of ostomy appliance. The majority of patients (103 [71%] colostomy, 48 [78%] ileostomy/loop ileostomy) used a 1-piece appliance. Overall, use of convexity included 43 patients (29%) with an end colostomy, 18 patients (33%) with an end colostomy, and 3 patients (43%) with a loop ileostomy. Of the patients that had undergone emergency surgery, 25 (46%) used convexity compared to 38 (25%) having nonemergent surgery (P = 0.006). 

Discussion  

The principal findings of this prospective study in which 207 patients received regular and standardized follow-up care by a WOC nurse during the first year after stoma surgery are that, after 1 year, 35% of this patient population had 1 or more complications. More than a quarter of the patients (27%) had ostomy complications, and 11% had peristomal skin complications. The majority (88%) of all patients had their ostomy location evaluated and marked preoperatively and were able to manage their ostomy themselves, but 20 (37%) patients that had undergone emergency surgery had not had their ostomy preoperatively sited. 

A colostomy height of ≤5 mm (versus >5 mm) was more common in women (69%) (P = 0.002) and in patients who had emergency surgery (P = 0.045), and this was associated with a parastomal hernia (P = 0.020) and use of convexity (P = 0.016). Regular follow-up during the first year after ostomy surgery meant patients’ ostomy-related problems were evaluated, diagnosed, and treated or referred to a dermatologist. This, in addition to the shorter patient follow-up time in the cited studies, may help explain the low prevalence of peristomal skin complications (11%) in this study compared to 2 previously published studies  — a prospective cohort study from the United Kingdom²⁴ and a cross-sectional study from Denmark²⁵ in which patients did not receive regular follow-up care. In the British study,²⁴ patients that had been operated during a 10-year period and did not have regular follow-up regarding their stoma were invited to attend a clinic to have their skin problems assessed by a dermatologist and a stoma care specialist nurse. Of the 323 participating patients, 73% had skin problems that affected normal ostomy appliance use. In the Danish study,²⁵ all individuals with a permanent stoma in a Danish community population (N = 630) were invited to participate. The study reported peristomal skin disorders were higher for participants with an ileostomy (57%) or urostomy (48%) than a colostomy (35%). Of the diagnoses of skin disorders, 77% could be related to contact with stoma effluent. More than 80% of the participants did not seek professional health care. The authors concluded more education and annual follow-up visits at local stoma care clinics were needed. 

The present study also included causes for peristomal skin complications (see Figure 1) rarely reported in literature. The peristomal skin complications in the present study were related to 3 factors (see Figure 1): the construction of the ostomy (stenosis, sliding ostomy, ostomy opening/lumen at skin level); peristomal skin disease (unspecific dermatitis around the ostomy, candidiasis, pyoderma gangrenosum, no obvious reason, and skin irritation at the outer part of the appliance); or appliance- or routine-related (pressure from convexity, ostomy appliance worn for too long, rich hair growth, leakage, or the ostomy appliance opening was too large). 

Previous studies^24,25 have shown a high number of peristomal skin complications, in contrast to the present study, where stoma-related complications were more frequent (27%) and parastomal hernia was the most frequent complication (20%) in patients with a colostomy. The incidence of a parastomal hernia increases over time. A literature review by Shabbir and Britton⁷ of studies addressing complications associated with stoma formation published between 1980 and 2008 showed an occurrence of parastomal hernia ranging from 4% to 48%. In a previous longitudinal study¹⁶ at the authors’ institution, 122 patients with a colostomy were included, but only 67 remained to follow-up at the 1-year visit, and prevalence of parastomal hernia after 1 year was 10%. In the present study, 3 times as many patients were evaluated than in the previous study,¹⁶ the majority (22 of 29) of whom experienced a parastomal colostomy hernia and were concerned about the hernia, which influenced clothing choice and caused a dragging sensation, aches, and anxiety. A nonsystematic review of American literature by Kwiatt and Kawata⁸ showed hernia repair or relocation of the ostomy to the other side of the abdomen to surgically fix the parastomal hernia did not show promising results; recurrence rates ranging from 46% to 100% in hernia repair and 24% and 40% in relocation have been reported. 

Granulomas can influence ostomy appliance fit, and patients worry because they cause bleeding. In the present study, 6.3% of patients had granulomas, which was lower than in 2 previous prospective studies  — 1 from the Netherlands²⁶ reporting 10% and 1 from the authors’ institution¹⁶ reporting 9% granulomas, respectively. Two (2) patients (1%) in the current study developed colostomy prolapse, which is lower than the 6% reported 1-year post-surgery study in the Netherlands’ study that included 100 patients (mean age 67, 48% women and 41% emergency surgery) and 8 follow-up time points. 

It is important to distinguish between peristomal skin complications in colostomies (6% in this study) and end ileostomies (23% in this study), a statistically significant difference. However, the majority (70%) of complications in this study were classified as mild. The regular follow-up by the 4 WOC nurses may have prevented difficult cases of peristomal skin complications from occurring. In the present study, only 6% of patients with a colostomy had peristomal skin complications and only 2% of patients had problems with leakage compared to 41% and 59%, respectively, in a recent population-based, cross-sectional Danish survey study²⁷ that included 644 patients (response rate 88%) with a permanent ostomy created due to rectal cancer (median age 72, 64% men). The study used a nonvalidated patient questionnaire developed by experts (no WOC nurse) that was revised after patient evaluation. Quality of life was reported to be affected by the stoma in 68% of patients; the authors concluded that the high number of patients reporting leakage and skin problems indicated a need for restructuring patient counseling. Likewise, in a systematic review from the US,³ patients reporting severe peristomal skin complications, severe leakage, and severe problems adjusting to the ostomy were noted to have significantly lower HRQOL scores than patients reporting less severe or no problems.³ 

The number of patients preoperatively sited before ostomy surgery varies. In 2 large retrospective studies, 1 from Turkey¹² where only 38% were preoperatively sited and 1 from the United Kingdom¹³ where 89% were preoperatively sited, complication rates were significantly higher in patients that were not preoperatively sited. The Turkish study sought to determine the effect of stoma site marking on stomal and peristomal complications and included 748 patients (mean age 56.6, men 54.5%). Complications were significantly higher in patients where the stoma site was not marked than among those whose stoma site was marked (22.9% and 46%, respectively, P<0.001). Stomal/peristomal complications developed in 248 patients; the most frequently observed complications were peristomal skin complications (49%) followed by mucocutaneous separation (18.6%) and retraction (11%).  

A 2-year, prospective study from Israel¹¹ that included 105 patients with a colostomy or ileostomy (median age 65, 57% men) undergoing elective surgery studied the impact of preoperative ostomy site marking on different parameters. The results showed the stoma site of 49.5% of patients was preoperatively selected. In the preoperatively sited patients, complication rates were significantly lower and independence parameters and quality-of-life scores were significantly higher than in those whose stoma site was not preoperatively selected. In the present study, 88% were preoperatively ostomy-sited, similar to the study by Nastro,¹³ but no differences in complications between groups were noted. 

One of the most important issues for a patient to be able to start a new life with an ostomy is managing its care. In the present study, 88% were self-sufficient in ostomy care compared to only 15% in the previously cited study from Israel.¹¹ The protective influence preoperatively and continued involvement of a WOC nurse have been reported to prevent progression of relatively common minor problems to more severe conditions.^1,2,8,18

In a Danish case control study,²⁸ BMI >30 was directly associated with skin complications. In that study, the importance of suggested risk factors for developing skin complications was studied in a group of patients with an ostomy from the general population. Of the 199 participants, 45% exhibited a skin problem for which they had not sought help.   The retrospective study by Nastro et al,¹³ with a minimum 2-year follow-up, found that a BMI >25 was a risk factor for the development of a parastomal hernia. A prospective study by Cottam et al¹⁵ of 3970 ostomies found problematic stomas when patients had a mean BMI of 25.4. The current study found no association between a higher BMI and complications. However, BMI may not be the only important variable because the body configuration of men and women can differ. In a cross sectional Finnish study²⁹ of 132 patients in their early forties, women were reported to have twice as much subcutaneous abdominal fat as men (P<0.0001). This could be one of the reasons why significantly more women had a colostomy height ≤5 mm in the present study. 

The risk of developing a major ostomy complication has been calculated to be about 1 in 3 patients with ASA I or II and no musculoskeletal comorbidities whose ostomy was preoperatively sited before operation and who underwent surgery for indications other than cancer.¹³ In the present study, 35% of the participants had complications and more patients presented with ASA III+IV among those who underwent emergency surgery, but no differences in stoma-related complications were noted (see Table 1). One contributing factor could be that a colorectal surgeon specialist participated in all elective and emergency operations. 

Selecting ostomy appliances that are appropriate for the type of stoma, the size and contour of the stoma, and type and volume of effluent is important to preventing peristomal skin complications related to product selection. The appliances may need to be refitted in the recovery period after surgery or when the body weight increases or decreases significantly.¹ The WOC nurse has numerous options to address complications such as leakage, ostomy complication or peristomal skin compromise, adjusting the appliance to fit the size and contour of the ostomy, and using different aids adapted for ostomy care. 

An ostomy appliance with convexity can be of help in avoiding stool leakage because it allows the ostomy to protrude more when the ostomy height is low. Convex appliances are more expensive but can solve problems such as stoma retraction and low ostomy and prevent leakage, especially if surgical revision of an ostomy is not possible. The present study data related to convexity use show a higher rate of convexity usage than in a previous study performed at the authors’ institution¹⁶ and also in comparison to the prospective study by Arumugam et al¹⁰ that was designed to determine the nature of complications and their relationship with various risk-factors and their management. Among the 97 patients (mean age 65) studied, complications developed in 50.5% of ostomies and 22% of patients (colostomy and ileostomy) used convexity compared to 31% in the same ostomy types in the present study where convexity use was related to ostomy height. Patients with an end colostomy with a height of ≤5 mm had significantly more use of convexity (P = 0.016), and patients with an ileostomy with an ostomy height of ≤20 mm used convexity more frequently (39.5%) than patients with an ileostomy height >20 mm (18.8%), although the difference was not significant. In cases of emergency surgery, as many as 46% of patients used an appliance with convexity 1 year post surgery. Despite the high use of convexity and its reported risk of causing pressure to the skin,^2,21 only 1 patient in the study had a peristomal skin complication related to convexity use (see Figure 1). The patients in the present study were carefully followed by a WOC nurse, and their ostomy-related problems were treated (eg, topical medications, adjusting the size of the appliance to fit the size and contour of the ostomy, use of convexity) during the 1-year follow-up period, which probably contributes to the low number of peristomal skin complications compared to other studies.^24,25,27 

The frequency of parastomal hernia needs to be reduced. However, the responsibility for the construction of an ostomy lies with the surgeon. Several studies of the prevention of parastomal hernias are ongoing at the authors’ institution³⁰ and worldwide (personal communication). According to best practice guidelines from the WOCN,² several factors may reduce the risk of developing a hernia: patients should lose excess weight before surgery, stop smoking, use abdominal support belts and garments when doing heavy lifting or heavy work, and abstain from active abdominal exercises or lifting heavy objects for at least 3 months following surgery. However, the evidence is not strong for some of these recommendations (eg, support belts, lifting heavy objects) and further studies are needed. Of note: convexity is not (but can address problems) related to parastomal hernia.

An ostomy should be constructed to an adequate length^15,16 that takes into account differences in body configuration, especially during emergency surgery. Surgeons and WOC nurses also need to develop strategies for enabling preoperative ostomy siting on patients regardless of time of day. These measures could significantly improve the situation for patients undergoing ostomy surgery.^12-14 Moreover, WOC nurses need to address ostomy-related complications as well as investigate their underlying causes. In the present study, the 3 factors most commonly noted for patients with peristomal skin complications were related to 1) the construction of the stoma, 2) the presence of peristomal skin disease, and/or 3) the ostomy appliance or appliance routines used by patients (see Figure 1). Surgeons¹³ and WOC nurses³ believe the number of ostomy-related complications described in the literature underestimate the actual incidence because many ostomy-related problems are solved by a WOC nurse and not brought to the surgeon’s attention. If problems are related to ostomy construction, WOC nurses should communicate and discuss this with the surgeons so improvements can be made; surgeons need to collaborate more with WOC nurses when performing studies regarding ostomy-related complications. This, in turn, may help prevent complications, which will reduce health care costs for ostomy equipment (number of pouches used, convexity use) and outpatient visits while ultimately, improving patient quality of life. More studies are needed that use a prospective design, are consistent operational definitions, use valid and reliable measurement methods, and involve colorectal surgeons and WOC nurses as equal partners. These recommendations will help increase the availability of standardized data to make comparisons among studies possible.

Limitations

A limitation of the study is that surgeons knew WOC nurses had diagnosed a parastomal hernia when they conducted their evaluation. The surgeon and WOC nurse should have assessed the hernia simultaneously but independently of each other, and a further CT scan would have strengthened the diagnosis. The study was conducted in 1 hospital with 4 experienced WOC nurses following a detailed protocol of patient follow-up. The external validity of these study results remain to be examined. 

Conclusion

In a clinical study that investigated ostomy and peristomal complications 1 year post surgery, the number of peristomal skin complications was low (11%) compared to other studies. Regular follow-up by a WOC nurse and standardized measures after ostomy construction seemed to be a factor in the low prevalence of peristomal skin complications observed. Convexity use was related to ostomy height, suggesting the need for increased ostomy height. Explorative prospective studies are needed that consider differences in body configuration when determining stoma height at the time of ostomy construction with special attention to patients requiring emergency surgery. 

References 

1. Stelton S, Zulkowski K, Ayello EA. Practice implications for peristomal skin assessment and care from the 2014 World Council of Enterostomal Therapists International Ostomy Guideline. Adv Skin Wound Care. 2015;28(6):275–284.

2. Wound Ostomy and Continence Nurses Society. Stoma Complications: Best Practice for Clinicians. Mt. Laurel, NJ;2014.  

3. Pittman J, Kozell K, Gray M. Should WOC nurses measure health-related quality of life in patients undergoing intestinal ostomy surgery? J Wound Ostomy Continence Nurs. 2009;36(3):254–265.

4. Kehlet H, Wilmore DW. Multimodal strategies to improve surgical outcome. Am J Surg. 2002;183(6):630–641.

5. Bonjer HJ, Deijen CL, Abis GA, et al. A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med. 2015;372(14):1324–1332.

6. Abbas MA, Tejirian T. Laparoscopic stoma formation. J Soc Laparoscop Surg. 2008;12(2):159–161.

7. Shabbir J, Britton DC. Stoma complications: a literature overview. Colorectal Dis. 2010;12(10):958–964.

8. Kwiatt M, Kawata M. Avoidance and management of stomal complications. Clin Colon Rectal Surg. 2013;26(2):112–121.

9. Colwell JC, Beitz J. Survey of wound, ostomy and continence (WOC) nurse clinicians on stomal and peristomal complications: a content validation study. J Wound Ostomy Continence Nurs. 2007;34(1):57–69.

10. Arumugam PJ, Bevan L, Macdonald L, et al. A prospective audit of stomas—analysis of risk factors and complications and their management. Colorectal Dis. 2003;5(1):49–52.

11. Person B, Ifargan R, Lachter J, Duek SD, Kluger Y, Assalia A. The impact of preoperative stoma site marking on the incidence of complications, quality of life, and patient’s independence. Dis Colon Rectum. 2012;55(7):783–787.

12. Baykara ZG, Demir SG, Karadag A, et al. A multicenter, retrospective study to evaluate the effect of preoperative stoma site marking on stomal and peristomal complications. Ostomy Wound Manage. 2014;60(5):16–26.

13. Nastro P, Knowles CH, McGrath A, Heyman B, Porrett TR, Lunniss PJ. Complications of intestinal stomas. Br J Surg. 2010;97(12):1885–1889.

14. The American Society of Anesthesiologists. ASA. New classification of physical status. Anesthesiology. 1963(24):111.

15. Cottam J, Richards K, Hasted A, Blackman A. Results of a nationwide prospective audit of stoma complications within 3 weeks of surgery. Colorectal Dis. 2007;9(9):834–838.

16. Persson E, Berndtsson I, Carlsson E, Hallen AM, Lindholm E. Ostomy related complications and ostomy size — a two year follow-up. Colorectal Dis. 2010;12(10):971–976.

17. Carlsson E, Berndtsson I, Hallen AM, Lindholm E, Persson E. Concerns and quality of life before surgery and during the recovery period in patients with rectal cancer and an ostomy. J Wound Ostomy Continence Nurs. 2010;37(6):654–661.

18. Wound Ostomy Continence Nurses Society (WOCN). ASCRS and WOCN joint position statement on the value of preoperative stoma marking for patients undergoing fecal ostomy surgery. J Wound Ostomy Continence Nurs. 2007;34(6):627–628.

19. Rolstad BS, Erwin-Toth PL. Peristomal skin complications: prevention and management. Ostomy Wound Manage. 2004;50(9):68–77.

20. Lavery I, Erwin-Toth PL. Stoma therapy. In: Cataldo P, MacKeigan J, eds. Intestinal Stomas: Principles, Techniques, and Management, 2nd ed. New York, NY: Marcel Dekker;2004.

21. Lyon CC, Smith A. Abdominal Stomas and Their Skin Disorders: An Atlas of Diagnosis and Management, 2nd ed. London, UK: Informa Healthcare;2010.

22. Borglund E, Nordstrom G, Nyman CR. Classification of peristomal skin changes in patients with urostomy. J Am Acad Dermatol. 1988;19(4):623–628.

23. Erwin-Toth P, Stricker LJ, Rijswijk L. Wound wise: peristomal skin complications. Am J Nurs. 2010;110(2):43–48.

24. Lyon CC, Smith AJ, Griffiths CE, Beck MH. The spectrum of skin disorders in abdominal stoma patients. Br J Dermatol. 2000;143(6):1248–1260.

25. Herlufsen P, Olsen AG, Carlsen B, et al. Study of peristomal skin disorders in patients with permanent stomas. Br J Nurs. 2006;15(16):854–862.

26. Formijne Jonkers HA, Draaisma WA, Roskott AM, van Overbeeke AJ, Broeders IA, Consten EC. Early complications after stoma formation: a prospective cohort study in 100 patients with 1-year follow-up. Int J Colorectal Dis. 2012;27(8):1095–1099.

27. Feddern ML, Emmertsen KJ, Laurberg S. Life with a stoma after curative resection for rectal cancer. A population-based, cross-sectional study. Colorectal Dis. 2015;17(11):1011–1017.

28. Nybaek H, Bang Knudsen D, Norgaard Laursen T, Karlsmark T, Jemec GB. Skin problems in ostomy patients: a case-control study of risk factors. Acta Derm Venereol. 2009;89(1):64–67.

29. Westerbacka J, Corner A, Tiikkainen M, et al. Women and men have similar amounts of liver and intra-abdominal fat, despite more subcutaneous fat in women: implications for sex differences in markers of cardiovascular risk. Diabetologia. 2004;47(8):1360–1369.

30. Correa Marinez A, Erestam S, Haglind E, et al. Stoma—the technical aspects of stoma construction: study protocol for a randomised controlled trial. Trials. 2014;15(254):1–7.

Potential Conflicts of Interest: none disclosed

Dr. Carlsson is a registered nurse, enterostomal therapist, and lecturer, Surgical Department, Institute of Clinical Sciences, Sahlgrenska University Hospital/Östra and Institute of Health and Care Sciences, The Sahlgrenska Academy, University of Gothenburg, Sweden. Ms. Fingren, Ms. Hallén, and Ms. Petersén are registered nurses and enterostomal therapists, Surgical Department, Institute of Clinical Sciences, Sahlgrenska University Hospital/Östra. Ms. Lindholm is a registered nurse and research nurse, Surgical Department, Institute of Clinical Sciences, Sahlgrenska University Hospital/Östra. Please address correspondence to: Eva Carlsson, PhD, RN, ET, Surgical Department, Colorectal Unit, Sahlgrenska University Hospital/Östra Diagnosvägen 11, Gothenburg 416 85 Sweden; email: eva.k.carlsson@vgregion.se.

Abstract

Skin temperature may help prospectively determine whether an area of skin discoloration will evolve into necrosis. A prospective, observational study was conducted in 7 skilled nursing facilities to determine if skin temperature measured using infrared thermography could predict the progression of discolored intact skin (blanchable erythema, Stage 1 pressure ulcer, or suspected deep tissue injury [sDTI]) to necrosis and to evaluate if nurses could effectively integrate thermography into the clinical setting.

Patients residing in or presenting to the facility between October 2014 and August 2015 with a pressure-related area of discolored skin determined to be blanchable erythema, a Stage 1 pressure ulcer, or sDTI and anticipated length of stay >6 days were assessed at initial presentation of the discolored area and after 7 and 14 days by facility nurses trained on camera operation and study protocol. Variables included patient demographic and clinical data, data related to the discolored area (eg, size, date of initial discovery), and temperature and appearance differences between discolored and adjacent intact skin. Skin temperatures at the discolored and adjacent areas were measured during the initial assessment. All facility pressure ulcer prevention and treatment protocols derived from evidence-based clinical practice guidelines remained in use during the study time period. Participating nurses completed a 2-part, pencil/paper survey to examine the feasibility of incorporating thermography for skin assessment into practice. Data analyses were performed using descriptive statistics (frequency analyses) and bivariate analysis (t-tests and chi-squared tests); logistic regression was used to assess associations among patient and pressure ulcer variables. Of the 67 patients studied, the overall mean age was 85 years (SD 10); 52 were women; 63 were Caucasian; and the top 3 diagnoses, accounting for 60% of the study sample, included neurologic (ie, cardiovascular accident/dementia [14, 21%]), cardiac-related (14, 21%), and orthopedic (13, 19%) conditions. Twenty-eight (28) participants were long-term care patients, and 39 were admitted as short-stay patients. The most frequently reported location of discolored intact skin on presentation was the heel (27, 40%). The mean temperature at the site of the discolored skin was 33.6˚ C (SD 3) and at the adjacent skin was 33.5˚ C (SD 2.5). The mean size of the areas of discoloration was 11 cm² (SD 21). Capillary refill of the discolored area was absent on initial presentation in 49 patients (72%), and demarcation of the discolored borders was evident for 45 (66%). Of the 67 patients, 30 (45%) experienced complete resolution of the discolored area. At day 7, 8 (16%) of the remaining 50 patients in the sample exhibited skin necrosis and at day 14, a total of 12 patients of the remaining 37 (32%) exhibited skin necrosis. At day 7, skin necrosis was significantly associated with admission to a subacute unit (P = 0.01) and at day 14 to negative capillary refill at initial presentation (P = 0.02). Regardless of skin temperature, negative capillary refill at presentation was significantly associated with skin necrosis at day 7 (P = 0.04). A dichotomous variable was constructed to examine patients with cooler temperatures at the site as compared to their adjacent skin and persons with warmer skin temperatures at the center of the discolored skin for the presence of skin necrosis at both day 7 and day 14. In multivariate analysis, patients with cooler rather than warmer skin temperatures at the center of the discolored area as compared to the adjacent skin were more likely to develop necrosis by day 7 (OR 18.8; P = 0.05; CI: 104-342.44). Participating nurses were uncertain about the feasibility of integrating thermography into practice. Larger prospective studies with more heterogeneous samples are needed to determine the validity of skin temperature measurement as a predictor of skin necrosis and the utility of implementing thermography into clinical practice.

Pressure ulcers are a clinical concern across the care continuum. Despite advances in technology and the implementation of formalized prevention programs, pressure ulcer prevalence rates in skilled nursing facilities (SNFs) across the United States are reported to range from 4.1% to 32.3%.^1,2 According to the results of the National Nursing Home Survey,^3-5 1 in 10 nursing home residents in the US acquires a pressure ulcer and more than half of hospitalized patients with a primary or secondary diagnosis of a pressure ulcer when discharged are admitted to a long-term care facility. 

The Advancing Excellence in America’s Nursing Home campaign⁶ states nearly 1.5 million Americans reside in nursing homes. Given that pressure ulcers occur most frequently in patients over the age of 65 and that older adults are the fastest growing segment of the population in the nation, pressure ulcer rates in this at-risk population likely will continue to rise over the coming decades.^4,7 Moreover, the financial burden for pressure ulcer care in the United States tops $11 billion,⁸ which includes the increase in both hospital length of stay⁹ and the risk of mortality.^10,11 

Pressure-related areas of discolored intact skin are classified as blanchable erythema, a Stage 1 pressure ulcer, or suspected deep tissue injury (sDTI). The presence of blanchable erythema denotes an area with exposure to pressure with a high probability of resolving once the source of pressure is removed.¹² Although a Stage 1 pressure ulcer, defined by the National Pressure Ulcer Advisory Panel¹³ (NPUAP) as nonblanchable erythema of localized intact skin usually over a bony prominence, is considered a heralding sign of pressure ulcer risk, it also is characterized as a potentially reversible, localized area of injury. According to a current guideline,¹³ deep tissue injuries begin at the muscle-bone interface and occur as a result of tissue deformation due to a short period of intense pressure and/or as a result of tissue ischemia due to prolonged periods of immobility.^14,15 These injuries present as purple or maroon areas of discolored intact skin or a blood-filled blister from damage to underlying soft tissue damage due to pressure and/or shear.¹³ Deep tissue injury can create a serious clinical problem because it cannot be detected using current evidence-based clinical assessment techniques at an early stage and can rapidly deteriorate into a deep, full-thickness pressure ulcer even when pressure ulcer prevention strategies have been implemented.¹³ Thus, the degree of tissue destruction referred to as sDTI can only be currently determined ex post facto of pressure ulcer occurrence. 

The science supporting the pathophysiologic changes inherent to the evolution in sDTI continues to advance; however, the timeframe from the time of initial injury to the appearance of the sDTI has not been firmly established at this juncture. Expert opinion based on clinical experience and case studies in the area of sDTI evolution have postulated a 48-hour timeframe from injury to first appearance and from 7 to 10 days to a full-thickness wound.¹⁴ Using the principles of forensic science, Farid¹⁶ proposed a 7-day to 14-day window from the time of injury until the emergence of visible signs of injury and the progression to necrosis. 

The current level of evidence and available assessment techniques make it difficult for the bedside practitioner to expediently distinguish whether a pressure-related area of discolored intact skin will ultimately resolve or whether it potentially represents sDTI in evolution. Additionally, blanchable erythema, Stage 1 pressure ulcers, and emerging areas of sDTI are difficult to detect in individuals with darker skin tones because changes in skin color may not be evident and may be easily missed by clinicians.¹³ 

One potential method proposed to help prospectively determine whether an area of skin discoloration will evolve into necrosis has been the measurement of skin temperature. Physiologically, nonviable tissue is not perfused; thus, the area exhibits a cooler temperature due to lack of blood flow. Therefore, in areas of sDTI that progress to full-thickness ulceration and necrosis, skin temperature is hypothesized to be cooler due to the lack of perfusion.¹⁷ 

The use of thermography has been studied for decades for its efficacy in pressure ulcer detection; it was introduced in the 1970s by Verhonick et al.¹⁸ In a small preliminary methodological study¹⁸ of 3 subjects, these researchers outlined the application of thermography as a modality to assist with the objective quantification of pressure ulcer development by examining the relationship between pressure and skin temperature. Sprigle et al,¹⁹ using a repeated measure design among a study sample of 65 inpatients and outpatients in the rehabilitation setting, measured skin temperature using perfusion monitors and temperature strips placed on the skin to validate temperature differentials. These researchers found temperature differences (cooler or warmer) at the site of the erythematous skin center as compared to the adjacent normal skin could indicate impending changes in skin integrity. In an observational, retrospective study of 85 hospitalized patients, Farid et al¹⁷ studied skin temperature using noninvasive infrared thermography as an adjunct to current visual (skin color) and tactile assessment (capillary refill) in acute care patients exhibiting pressure-related areas of discolored intact skin. Results of this study showed areas with a cooler skin temperature at the site of the discoloration as compared to the adjacent normal tissue significantly predicted the progression of the discolored area to necrosis by day 7 (OR 31.8, P = 0.001, CI: 3.8-263.1). In addition, discolored areas that exhibited both cooler temperatures and negative capillary refill were found to be positively associated with skin necrosis by day 7 (P<0.0002). 

The purpose of this study was to determine if skin temperature, measured using infrared thermography, could predict the progression of pressure-related areas of discolored intact skin to necrosis in SNF patients. The following research questions were addressed in this study: 

1. What is the timeframe from initial presentation of a pressure-related area of discolored skin to necrosis in a sample of SNF patients?
2. Is there a relationship between skin temperature at the site of a pressure-related area of discolored intact skin and progression to skin necrosis in a sample of SNF patients?
3. What factors predict the progression of a pressure-related area of discolored intact skin to necrosis?
4. Can thermography be efficiently integrated into clinical use by practitioners in SNFs? 

Methods

A prospective, observational study was conducted to determine the relationship between skin temperature at the site of a pressure-related area of discolored intact skin and the progression to skin necrosis. The study methodology was derived from the methodology previously employed by Farid et al.¹⁷ Institutional Review Board approval was obtained from all participating SNFs before study initiation. 

Setting. This study was conducted in 7 SNFs in a northeastern state of the US, with a geographic distribution representing the north, mid, and southern sections of the state. All SNFs included had earned a 5-star quality rating on Nursing Home Compare and at least a 4-star rating attained for RN staff at the time of the study inception.²⁰ 

Inclusion/Exclusion criteria. Patients (long-term care and subacute care) residing in or admitted to any of the study sites were considered for study participation if the following inclusion criteria were met: observed pressure-related area of discolored intact skin determined to be blanchable erythema, a Stage 1 pressure ulcer, or sDTI at initial presentation; and 2) anticipated length of stay >6 days (shorter lengths of stay would preclude follow-up assessments on day 7 and day 14). Exclusion criteria were patients: 1) with pressure ulcers involving observed alterations in skin integrity, including intact blisters (this study was to determine the progression of discolored intact skin); 2) with ulcerations suspected to be from an etiology other than pressure (ie, neuropathic ulcers, venous ulcerations, arterial ulcerations, vasculitic lesions, and moisture-associated skin damage); 3) actively dying; or 4) with a history of a pressure ulcer or other tissue damage at the site of the current area of discolored intact skin (the composition of scar tissue may preclude an accurate temperature reading). 

Data collection procedures. Data were collected from each participating facility over a 10-month time period from October 2014 through August 2015. All data were collected by nursing employees at each of the SNFs who were responsible for pressure ulcer assessment within their institutions. The nurses were educated on the data collection procedures and use of the thermographic camera by the research team and the research study consultant via formalized training sessions conducted before the study began. All data were recorded on paper/pencil data collection records designed for this study by the research team. All data recorded were de-identified to protect confidentiality of the patients.

The nurse data collectors at the individual sites identified patients who presented with or developed a pressure-related area of discolored intact skin. If the inclusion/exclusion criteria were satisfied, the data collectors completed the initial patient assessment with follow-up assessments conducted on day 7 and day 14.

All patients received the usual standard of care during the study period. All facility pressure ulcer prevention and treatment protocols (derived from evidence-based clinical practice guidelines) remained in use during the study. Evidence of adherence to current pressure ulcer prevention was determined through documentation in the patient’s medical record, through observation at the time of discovery of the area of discolored intact skin, and at each follow-up assessment. 

Variables collected at initial assessment only. The following variables were collected only at the initial assessment of the pressure-related area of discolored skin: 1) date/time of initial discovery of discolored skin (if the patient had more than 1 area, only the largest area was recorded and used for analysis); 2) size (cm²), measured with a paper measuring device; 3) anatomic location; 4) skin temperature of the pressure-related area of discolored intact skin assessed using the infrared thermographic device; 5) skin temperature assessed using the thermographic device of the normal adjacent skin area; and 6) ambient room temperature (measured using thermographic device). In order to improve the visibility and identification of the area in the camera lens, adhesive stars were applied to the margins of the discolored skin (see Figure 1). The adjacent skin area was defined as the area within 5 cm to 10 cm of the outer margin of the area of discolored intact skin. 

Other data abstracted from the medical record at the time of the initial assessment included age, gender, race, admitting diagnosis, long-term care or subacute care admission, comorbid conditions (defined as any of the following: cardiovascular disease, diabetes mellitus, chronic pulmonary disease, peripheral vascular disease, end-stage renal disease), and Braden pressure ulcer risk assessment scale scores (on admission to the facility and at the time of the initial study assessment). Data regarding body temperature (measured using standard facility thermometer), body mass index, body weight, and serum albumin or prealbumin closest to the time of the discovery of the pressure-related area of discolored intact skin also were collected on initial assessment. 

Variables collected at all 3 assessments. The following variables were collected on initial assessment of the pressure-related area of discolored skin and repeated on day 7 and day 14: 1) presence or absence of demarcation; 2) color of the pressure-related area of intact skin; 3) presence or absence of capillary refill assessed using direct palpation of the area of discoloration skin and defined as positive (<3 seconds) or negative (>3 seconds or no visible blanching); and 4) evidence of the use of pressure ulcer prevention strategies as described above. 

The presence/absence of skin necrosis and pressure ulcer stage (if present) also were recorded on day 7 and day 14. 

Device. The thermographic device employed for this study was the Flir i^™ (Flir Systems, Boston, MA).²¹ This thermographic instrument is a hand-held, noninvasive, noncontact infrared detection device with a temperature sensitivity of <0.1˚ C at a distance of 2 feet. Inter-rater reliability of the use of the thermography camera was performed at the initiation of the study and periodically during the study period to confirm user accuracy and to validate that operational issues were not influencing the temperatures obtained. This device was chosen because it was previously employed in a clinical study¹⁷; however, the reliability and validity of this device have not been established in the context of a clinical setting to date.

Integration into practice. In order to determine if thermography could be successfully integrated into practice in the SNFs, a pencil/paper survey was designed and distributed to the 7 primary nurse users (1 from each of the participating facilities) during the final 3 months of data collection. This survey was comprised of 2 sections: the first section addressed 10 aspects related to operationalization of the specific thermography camera using the ratings satisfactory/unsatisfactory/unsure, and the second part of the survey included 3 open-ended questions addressing the feasibility of integrating thermography into the existing clinical setting. 

Sample size calculation. Sample size calculation was based on previous work by Farid et al.¹⁷ Assuming a sample with a ratio of warmer discolored areas to cooler discolored areas to be 2:1, a sample size of 60 was required to achieve statistical power.

Data analysis. Data were entered into SPSS statistical software package for Windows, Version 21 (IBM, Armonk, NY) and exported into Stata 14 (Stata Corp., College Station, TX). Data analysis was performed using SPSS for descriptive statistics and Stata 14 for bivariate analysis and multivariate analysis. Descriptive statistics including frequency distributions for all study variables were calculated. T-tests and chi-squared tests were conducted to detect differences in the study variables between patients with skin necrosis and those that remained necrosis-free. The presence of necrosis at both day 7 and day 14 was compared among patients with cooler pressure-related areas of discolored intact skin to patients with warmer pressure-related areas of discolored intact skin using chi-squared and t-tests. In order to conduct this comparison, a dichotomous variable was constructed to identify patients with lower temperatures at the site of discolored skin than the adjacent skin and persons with higher skin temperatures at the center of the discolored skin. Logistic regressions were used to capture associations among patient and pressure ulcer variables and the development of skin necrosis.

Results

Patient sample description. Seventy-three (73) patients were entered into the study; 6 were eliminated from the sample due either to transfer out of the facility or patient death before the second assessment on day 7, yielding a sample size of 67 patients for analysis. The overall mean age was 85 years (SD 10). The sample was predominantly female (52, 78%) and Caucasian (63, 94%). The top 3 diagnoses, accounting for 60% of the study sample, included neurologic (ie, cardiovascular accident/dementia [14, 21%]), cardiac-related (14, 21%), and orthopedic (13, 19%) conditions. Of the 67 patients in this study, 28 (42%) were long-term care patients and 39 (58%) were admitted as short-stay patients (see Table 1). 

The most frequently reported location of discolored intact skin on presentation was the heel (27, 40%). The mean temperature at the site of the discolored skin was 33.6˚ C (SD 3) and at the adjacent skin was 33.5˚ C (SD 2.5). The mean size of the areas of discoloration was 11 cm² (SD 21). Capillary refill was absent on initial presentation of the area of discoloration in 49 patients (72%), and demarcation of the discolored borders was evident for 45 (66%) (see Table 2). 

The discolored area completely resolved in 30 patients by either day 7 (17, 25%) or day 14 (13, 19%). The 2 most common stages of pressure ulcer, reported at both day 7 and day 14, were sDTI (19 [38%] and 10 [27%], respectively) and unstageable (8 [16%] and 11 [30%], respectively) (see Table 2). The skin color most frequently reported on initial presentation was purple (29, 43%); of the 29 patients who presented with purple discoloration at the first assessment, 10 (34%) of these areas resolved, 6 (21%) by day 7 and 4 (14%) by day 14. By day 7, 12 (54%) of the initial purple discolored areas were staged as sDTI and 6 (27%) were staged as unstageable pressure ulcers. At day 14, 5 (26%) were staged as sDTI and 8 (42%) were staged as unstageable pressure ulcers. Of the remaining skin colors on presentation, red and deep red, respectively, were found to be the subsequent 2 colors most frequently reported (19 [28%] and 10 [15%]) in this sample. Of those with deep red discoloration on presentation, 2 (20%) had resolved by day 7 and 1 (10%) by day 14. The most frequently reported pressure ulcer stage at day 7 for patients with deep red discoloration on presentation was sDTI (3, 30%). For persons with red discoloration at presentation, 5 (26%) resolved by day 7 and 4 (21%) by day 14. The most frequently reported stage of pressure ulcer for those with red discoloration at day 7 was Stage 2 (3, 16%). 

The temperature of discolored skin as compared to the adjacent area was warmer in 41 (61%) and cooler in 26 (39%). The analysis of the dichotomous variable constructed to differentiate patients with cooler from those with warmer areas of discolored skin as compared to the adjacent skin showed centers categorized as cooler had a mean temperature of 31.2˚ C (SD 3.7); for those categorized as warmer, the mean temperature was 35.2˚ C. Thus, the mean temperature difference between patients with warmer temperatures versus cooler temperatures was 3.99˚ C. 

Time between initial presentation of a pressure-related area of discolored skin and development of necrosis. Patients that did and did not develop skin necrosis were compared on all study variables on day 7 and day 14 (see Table 3). By day 7, 17 discolored areas had resolved. Of the 50 patients remaining in the study sample, 8 (16%) had skin necrosis. At day 7, all 8 patients who developed skin necrosis were subacute or short-stay patients (χ² = 6.52; P = 0.016) and admitted to the SNF with an emerging area of discoloration, suggesting the areas of discoloration were already evolving at the time of admission to the SNF. By day 14, 13 additional pressure-related areas had resolved. Of the 37 patients remaining in the sample, 12 (32%) had skin necrosis. 

Capillary refill. A statistically significant difference was found at day 14 between patients who did and did not develop skin necrosis with regard to capillary refill. Overall, 49 of the study participants (72%) had negative capillary refill on initial presentation of the discolored area. All of the 12 patients that developed skin necrosis by day 14 had negative capillary refill evident on the initial presentation of the area of discoloration (P = 0.02). Statistically significant differences both at day 7 and day 14 also were found between the stage of pressure ulcer reported (χ² = 25.17, P = 0.000; χ²= 13.1, P = 0.002, respectively); patients with negative capillary refill at the initial presentation of the area of discoloration more frequently developed pressure ulcers categorized as sDTI or unstageable (see Tables 4 and 5). 

Relationship between skin temperature at the site of a pressure-related area of discolored intact skin and progression to skin necrosis. No statistically significant difference was found between cooler and warmer temperatures on presentation and the development of skin necrosis at day 7 (P = 0.93) or day 14 (P = 0.38) in univariate analysis. Additionally, no statistically significant differences were found in univariate analysis for any of the study variables between patients with cooler versus warmer skin temperatures on initial presentation (see Table 6). 

Predicting the progression from discolored intact skin to necrosis. Multivariate analysis of the study variables showed admitting diagnosis and cooler discolored intact skin temperatures were explanatory variables. Cooler skin temperature increased the odds of experiencing necrosis at day 7 at the 92% confidence level (odds ratio [OR] = 6.3; P = 0.08, CI: 0.83-48.00). When demographic (eg, age and admitting diagnosis) and environmental variables (eg, ambient room temperature) were added to the baseline model, the OR for development of skin necrosis substantially increased and was statistically significant at the 95% confidence level (OR = 18.8, P = 0.05, CI: 1.04-342.44) (see Table 7). Although a statistically significant Pearson correlation was found between capillary refill and necrosis at day 14, this association did not emerge in regression analysis (see Table 3). 

Integrating thermography into clinical use. Results of the survey distributed to the participating nurses found the camera was easy to operate and the infrared images easy to retrieve. The average amount of time needed to incorporate thermography into the clinical assessment of an area of discolored skin was 3 to 5 minutes. However, when asked if they believed thermography could be easily implemented into practice, 5 of the 7 participating nurses (more than 70%) were unsure or believed thermography could not be easily integrated into practice. Some uncertainties stemmed from specific clinical situations, such as the amount of time required for patient set-up to acquire the temperature reading and the need for more than 1 caregiver to position a patient depending on the anatomical location of the discolored area. 

The possible null effect on current pressure ulcer prevention strategies also was identified; adding skin temperature to the assessment of pressure-related areas of skin had the potential to have no impact on current pressure ulcer practices. Compliance with camera use by future users, the possibility of camera breakage and loss, as well as the overall cost of the modality also were cited as possible concerns. 

Discussion

Overall, results of this multivariate analysis suggest a relationship between lower skin temperatures of discolored intact skin as compared to the adjacent skin and skin necrosis by day 7 but not day 14. 

Review of the relevant literature offers varied results on the use of skin temperature as an adjunct to present clinical assessment techniques to detect deep tissue injury and pressure ulcer development. In the study by Farid et al,¹⁷ patients assessed using thermography who exhibited cooler rather than warmer skin temperatures were almost 32 times more likely to experience skin necrosis. In 2 previous clinical studies,^19,22 temperature variations either cooler or warmer at the site of the discoloration as compared to the surrounding skin were found to be associated with pressure ulceration. Sprigle et al¹⁹ found a 1˚ C difference in temperature (either warmer or cooler) between an area categorized as a Stage 1 pressure ulcer and the adjacent skin could herald a change in skin integrity. Similarly, Judy et al²² compared the use of the Braden scale to temperature measurement obtained through the use of infrared technology to determine pressure ulcer risk in a small study of hospitalized patients (N = 5) using a repeated measures design and found that a variance in skin temperature of 1.5˚ C (either cooler or warmer) between the bony prominence and the adjacent skin was more accurate in predicting pressure ulcer development of the heels and the sacrum in patients at risk for pressure ulcers than use of the Braden Scale alone. 

Laboratory studies of the efficacy of skin temperature measurement have shown variations in skin temperature (either warmer or cooler) were associated with skin necrosis; in one,²³ the use of infrared thermography was determined by the researchers to be a useful modality for the objective measure of early sDTI of the heel. However, the researchers concluded the temperature of the sDTI could be normal, elevated, or decreased when compared to adjacent healthy tissue, with increases in temperature observed with inflammation and temperature decreases with tissue ischemia. The researchers concluded temperatures in a suspected area of DTI were initially cooler, but with reperfusion and the presence of a severe inflammatory response, the temperature could increase in an ischemic area. Thus, the time at which the temperature is taken can be crucial to the determination of evolving necrosis. The challenge this presents in the clinical arena is proactively identifying patients at high risk for sDTI, accurately timing the measurement of skin temperature (initial moment of presentation or in the reperfusion phase) at which to capture the temperature fluctuation that the researchers purported to occur, and translating this finding to bedside practitioners so as to be clinically relevant. 

Interestingly, in another laboratory study using laser Doppler flowmetry,²⁴ reactive hyperemia characterized by higher temperatures in combination with pressure were found to be potential contributors to skin ischemia. The researchers proposed that lowering skin temperature proactively may have the potential to prevent pressure ulcer development; however, this study was limited by the participation of healthy persons who did not have the same comorbid burden of illness characterized by many patients, especially SNF patients who are at high risk for pressure ulcer development. 

In the current study, the pressure ulcer stages sDTI and unstageable were the 2 most common at both day 7 and day 14, with purple discoloration reported as the most common skin color at initial presentation of the discolored area. Among patients with areas of purple discoloration of intact skin on initial presentation, 6 (21%) had resolved at day 7, 12 (41%) were staged as sDTI, and 6 (21%) were categorized as unstageable. In other studies examining the evolutionary timeframe of sDTI, results have been varied. In a prospective, exploratory study of 40 hospitalized patients, Richbourg et al²⁵ found that of the patients who presented with purple discoloration, 2 (5%) had reepithealized, 18 (43%) had no change in this color, and 7 (17%) had progressed to slough or eschar. However, time to follow-up in this study varied from 1 to 20 days (average of 6 days). Moreover, in a retrospective study of 77 hospitalized patients conducted over a 2-year period, Sullivan²⁶ found that at follow-up (average 6 days, range 1 day to 4 weeks) from initial presentation 85 (66.4%) of the areas of sDTI had resolved or were moving toward resolution, 31 (24.2%) remained unchanged in appearance, and 12 (9.3%) had evolved into full-thickness wounds. 

The divergent findings between the previous and current research could be a reflection of different methodologies used, or they may suggest that DTI evolution may be variable. Factors that affect the evolution of sDTI still need to be elucidated, and staging a sDTI in evolution can be challenging.¹⁴ Thus, further empirical investigations that will contribute to the body of knowledge regarding the underlying pathogenesis of sDTI are needed. 

In the current study, negative capillary refill on initial presentation was found to be significantly associated with necrosis at day 14 and more frequently associated with pressure ulcers staged sDTI and unstageable at both day 7 and day 14. Farid et al¹⁷ found negative capillary refill in combination with cooler temperatures to be strongly associated with skin necrosis at day 7 (P<0.0002). Current results also revealed 18 patients (100%) with positive capillary refill with either warmer or cooler skin temperatures did not develop skin necrosis by day 7. Moreover, all 8 patients who developed skin necrosis by day 7 had negative capillary refill at initial presentation, regardless of skin temperature (χ² = 8.2055, P = 0.04) (see Table 8). 

Capillary refill is used as a measurement of peripheral perfusion. Obstruction of capillary blood flow can result in tissue ischemia.¹² Once the pressure is relieved, reactive hyperemia can ensue, resulting in erythematous appearance of the skin. On palpation, this erythema can be blanchable, with probable resolution if the source of pressure is relieved. However, nonblanchable erythema and corresponding changes in skin color to dark red or purple has the potential to be an indicator of deeper tissue damage.¹² Consistent with this description, the current study found 39 of the patients (82%) who had negative capillary refill of the discolored area on initial presentation exhibited initial skin color changes described as deep red, purple, or brown, although these initial skin color changes were not statistically significantly associated with necrosis at either day 7 (P = 0.20) or day 14 (P = 0.15). Regardless of the presenting color of the skin or temperature, the current study found capillary refill was better able to detect the progression of a discolored area of skin to necrosis.

Based on the results of the survey conducted with the nurses regarding use of thermography in the SNFs, a degree of uncertainty exists as to whether thermography could realistically be operationalized in the SNF setting. In previously published studies,^17,19,22 thermography was primarily used as a research tool, with camera use limited to the primary study investigator and trained research assistants. This appears to be the first study to involve nurses trained on the use of the thermography cameras. Although the cameras were found to be easy to operate, participating clinicians suggested cameras should be small enough to fit into the pocket in order to expedite the assessment. The need for an additional caregiver to assist in positioning the patient for the thermographic reading was cited as a disadvantage, increasing the time required to obtain the temperature of the discolored area. Cost for each camera (approximately $2000.00) and the potential for camera breakage and loss also were cited as potential concerns for implementation. Thus, based on the feedback of these users and coupled with the results of this study, the ability to successfully integrate thermography as part of a routine physical assessment at this time remains questionable. As technology continues to advance, future research will be warranted to explore use of thermography cameras that have greater portability (ie, pocket-sized), are less costly, and provide for greater ease in patient positioning in order to fully evaluate the pragmatic use of this modality in the clinical setting. 

Limitations

The sample size may be considered a limitation of this study; however, the minimum sample size required based on the calculation proposed by Farid et al¹⁷ was achieved. Also, the lack of darker-skinned patients in the sample could be considered a limitation because it remains unknown whether the use of thermography may be able to detect early skin changes that can lead to necrosis in patients in which changes in skin color and capillary refill are difficult to assess. Longer observation periods also may be warranted to detect further deterioration in discolored areas to necrosis. In addition, the type of infrared thermography device selected may have been a limitation; however, the authors employed the same device used in the study by Farid et al¹⁷ to remain consistent in methodology. The homogeneity of the sample in SNF setting presented a challenge to establishing associations between some of the independent variables and the outcome and thus limits the generalizability of the findings. All findings should be interpreted with this in mind. Further research is warranted using larger and more heterogeneous sampling. 

Conclusion

Cooler skin temperature at the site of the discoloration emerged as a significant predictor of the evolution of an area of discoloration to necrosis at day 7 of the 14-day study period. In addition, negative capillary refill, measured by detection of skin blanching, was significantly associated with skin necrosis by day 14. Notably, 100% of patients with positive capillary refill on presentation of the pressure-related areas of discoloration did not progress to skin necrosis at the discolored site, suggesting capillary refill is a reliable and simple technique that remains an important parameter when assessing pressure-related areas in patients with lighter skin tones. Assessment of capillary refill, currently part of the standard skin assessment for patients that present with areas of discolored skin, is a procedure that takes <1 minute to perform and can provide the clinician with real-time information regarding the potential viability of the skin. 

Infrared thermography continues to gain popularity but is still in its infancy with regard to its practicality and effectiveness as a screening tool for the development of necrosis in pressure ulcers in the real-world clinical setting. Moreover, the utility of successfully assimilating thermography into broad clinical practice remains largely unknown at this time because of a lack of an empirically established temperature differential between the adjacent skin and the area of skin discoloration that would guide clinicians in making the determination if any area of discoloration would progress to necrosis from those areas that may ultimately resolve. Larger studies across diverse clinical settings are warranted. 

Whether all pressure ulcers are avoidable or if the effects of pressure can be mitigated in certain clinical situations has been debated and scrutinized.^27,28 Continued empirical study into innovative, prospective, objective clinical assessment tools will aid in answering this question. If the clinical progression of a pressure-related area of discolored intact skin can be determined earlier in the course of ulcer evolution, earlier application of current pressure ulcer prevention strategies holds the possibility of improving patient outcomes, or conversely, earlier detection may add to the current knowledge base regarding the unavoidable pressure ulcer. The challenge remaining for researchers and clinicians is to identify proactive pressure ulcer assessment techniques that are reliable and valid, yet clinically feasible, and easily integrated into practice across diverse patient care settings. 

Acknowledgments 

The authors acknowledge the following nurses for their assistance and diligence in the data collection process for this study: Edward Acquah Jr, Kathy Brady, Sirner Dhaliwal, Judy Dedio, Kristin Melbourne, Sarah Robinson, Evelyn Savarese, Theresa Smith, and Norman Taclob.

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28. Edsberg LE, Langemo D, Baharestani MM, Posthauer ME, Goldberg M. Unavoidable pressure injury: state of the science and consensus outcome. J Wound Ostomy Continence Nurs. 2014;41(4):313–334.

Potential Conflicts of Interest: Funding for this study was provided by the Centers for Medicare and Medicaid Services. 

Dr. Cox is an assistant professor of nursing, Rutgers University School of Nursing, Newark, NJ; and an advanced practice wound, ostomy, continence nurse, Englewood Hospital and Medical Center, Englewood, NJ. Ms. Kaes is Director of Quality Improvement and Clinical Services, Health Care Association of New Jersey, Hamilton, NJ. At the time of this study, Mr. Martinez was the Institutional Research Specialist, Rutgers University, School of Nursing, Newark, NJ; he is now a Senior Institutional Research Analyst, Emory University, Atlanta, GA. Mr. Moles is President, TRANSITION HealthCare Consultants; and President, Nursing Home Expert Opinion Services, Monroe Township, NJ. Please address correspondence to: Jill M. Cox, PhD, RN, APN-C, CWOCN, Rutgers University, 869 Rivervale Road, River Vale, NJ 07675; email: jillcox@sn.rutgers.edu.

Abstract

Ostomy-specific adjustment may or may not predict health-related quality of life (HRQoL) and/or overall quality of life (QoL). A cross-sectional study was conducted among patients recruited from the customer registers of 8 surgical suppliers and pharmacies across Norway between November 2010 and March 2011 to determine which of the 34 items of the Ostomy Adjustment Scale (OAS) are the strongest predictors for HRQoL and overall QoL and to determine the HRQoL and overall QoL of individuals with an ostomy compared to a control group representing the general population.

Persons who were >18 years old; had a permanent colostomy, ileostomy, or urostomy for >3 months; and could read and write Norwegian were invited to participate. The participants received information about the study in a letter from the researcher and returned their demographic information (addressing gender, age, marital status, education, diagnosis, time since surgery, and ostomy type) and study questionnaires using prepaid envelopes. The 158 participants (mean age 64 years [range 29–91], 89 [56%] men and 69 [44%] women) completed and returned by mail a sociodemographic questionnaire, the 34-item OAS (questions scored on a scale of 1 to 6, totally disagree to totally agree, score range 34 to 204), the Short Form-36 (SF-36, including 2 main components [physical and mental issues] divided into 8 subscales, scored from 0 to 100), and the 16-item Quality of Life Scale (QOLS) instrument (each response scored 1 to 7, from very dissatisfied to very satisfied; total score ranging from 16 to 112). Statistical analysis, including ordinary least square regression analyses, assessed whether the OAS independently predicted the sum scores of the SF-36 (physical component summary [PCS] and mental component summary [MCS]) and the QOLS score after adjusting for age, gender, marital status, education, diagnosis, time since surgery, and ostomy type. The OAS significantly predicted the SF-36 (PCS and MCS) and QOLS scores (P<0.001). Five (5) OAS items (“living a fulfilling life,” “being free to travel where I want despite my ostomy,” “realizing that this ostomy will be there forever,” “worries about being left alone,” and “embarrassing accidents in sexual activities”) strongly predicted the composite score of the SF-36 (PCS and MCS) and QOLS measurements. The SF-36 scores in physical role functioning, general health, vitality, and MCS were lower in ostomy patients than controls (P<0.05), whereas no difference was found for QOLS. Overall, ostomy-specific adjustment may be an important predictor of HRQoL and overall QoL, with the OAS factors described above having greater influence. More research such as prospective cohort studies are needed regarding patient adjustment to an ostomy. 

Several qualitative studies describe how surgical ostomies can impact all aspects of life; their themes include being different from others and learning how to live with a stoma¹ and coping with an altered sense of self, living a restricted life, and overcoming resulting restrictions.² Research regarding quality of life (QoL), including a prospective, longitudinal, multicenter study³ of follow-up programs for patients with an ostomy, seek to gain a better understanding of the impact of living with an ostomy and to develop appropriate care and long-term plans for patients with ostomies. Overall, QoL is understood to encompass satisfaction in all aspects of life, including material comfort, health, independency, recreation, and relationships with others,^4,5 whereas the more specific concept of health-related quality of life (HRQoL) relates only to the effects of illness on health and well-being.⁶ 

Several instruments have been used to assess QoL related to health conditions. The 34-item Ostomy Adjustment Scale (OAS) includes the patient’s care of the ostomy, feelings about having an ostomy, leisure and work ability, opinions regarding instructions received for the ostomy, and feelings about the enterostomal therapist (ET nurse) or physician.⁷ Items are scored from 1 to 6 (1 = totally disagree and 6 = totally agree); the total score ranges from 34 to 204 with higher scores associated with better levels of adjustment. The psychometric properties of the OAS have shown good levels of internal consistency, as illustrated by Cronbach alpha values ranging from 0.87 to 0.95.^7,8-11 Furthermore, the test-retest reliability of the OAS has been calculated in several studies using Pearson correlation with reported values ranging from 0.59-0.82.^7,8,10,11 The OAS has been validated in a Norwegian population⁸ but has not been further validated in a clinical context. 

The Short Form-36 (SF-36) measures the symptoms and functions known to be most affected by disease and treatment.¹² The scale includes 8 subscales that can be divided into 2 summary scores: the physical component summary (PCS), including physical functioning, physical role functioning, bodily pain, and general health subscales; and the mental component summary (MCS), including vitality, social functioning, emotional role function, and mental health subscales. The question responses are on an ordinal scale. The subdomains are calculated into a continuous scale that ranges from 0 to 100, and the summary scores are calculated so a score of 50 with a standard deviation of 10 equals the average scores of the United States population. Higher scores are associated with better HRQoL. The SF-36 has been previously validated in Norway, and the Norwegian population norm scores for the SF-36 have been published.¹³

Overall QoL can be measured using the Quality of Life Scale (QOLS)¹⁴ questionnaire, which facilitates assessment of an individual’s overall satisfaction with life, such as material comfort, health, independence, recreation, and relationships with others. The 16 items are scored on a scale from 1 to 7 (1 = very dissatisfied and 7 = very satisfied, with cumulative scores ranging from 16 to 112. Higher scores are associated with a better QoL. The QOLS has been found to be valid for measuring domains of QoL across patient groups and cultures. The scale has been validated in Norway,¹⁵ and scores are available for comparison.^15-17 

Many cross-sectional studies have investigated HRQoL in patients with an ostomy using the SF-36 instrument and compared results with scores from a control group within the general population: a survey¹⁸ from Japan of 102 colostomy patients found significantly lower SF-36 scores in physical role functioning and social functioning scales than in the general population scores; and a study¹⁹ of 64 urostomy patients showed all SF-36 scores (except for pain) were lower than the general population. A descriptive study²⁰ (N = 44 colostomy patients) found scores of all SF-36 scales were lower than general population scores. A longitudinal, prospective study²¹ among 57 patients with a loop ileostomy or permanent colostomy who completed the SF-36 found scores decreased 1 month following surgery, but all scores were higher than preoperative scores after 6 months. However, the physical role functioning, social functioning, emotional role functioning, and mental health scores were still lower than the general (reference) population after 6 months (P<0.05). A cross-sectional study²² using the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ-C30) and the EORTC colorectal quality of life questionnaire (QLQ-CR38) examined the physical and mental consequences of an ostomy in 1019 rectal cancer survivors; the health status/QoL was lower in the 408 patients with an ostomy compared to those without. 

The general finding is that HRQoL is slightly reduced in patients who require an ostomy, typically in the role functioning and social domain items of the instrument(s).^18-21 Although knowledge is lacking regarding how ostomy-specific measures are associated with and predict HRQoL and overall QoL outcomes in patients with an ostomy, studies have found sociodemographic and clinical factors were related to HRQoL and overall QoL. The study by Furukawa et al¹⁹ of 64 urostomy patients using the SF-36 found the presence of a supportive person at home and participation in a support group were associated with better HRQoL. The descriptive survey study by Kement et al²⁰ among 44 patients using the SF-36 indicated that gender, marital status, and household (living alone or together with partner or family) affected several SF-36 scores. The cross-sectional study by Mahjoubi et al²³ found a significantly higher QoL in 38 patients with an appropriate stoma site compared to 174 patients with an inappropriate stoma site selection as measured with the EORTC 30. A cross-sectional study²⁴ used an ostomy-specific QoL instrument in 105 patients and found significantly higher QoL in patients in whom the stoma site was marked preoperatively. In a multicenter, descriptive study of 748 patients, Baykara et al²⁵ found significantly more skin problems, separation, and retraction of the ostomy in patients where the stoma site was not marked. Fear of leakage and altered sexual function that negatively affected QoL were noted in 1 cross-sectional study²⁶; in another²⁷ that used the City of Hope Quality of Life Questionnaire among 307 patients with urinary diversions, skin problems, difficulties in managing the ostomy, fear of recurrence, financial worries, family stress, and uncertainty about the future were found to negatively affect QoL. Additional cross-sectional studies found poor sleeping patterns, which may be related to fear of leakage from the equipment, were implicated in reducing HRQoL and overall QoL²⁸; and improving self-care and inspiring hope were important factors in increasing stoma-related QoL (N = 76 ostomy patients).²⁹ A longitudinal study¹¹ found the fear of being dependent on other people and the uncertain nature of living with cancer are the most frequent concerns in the first 6 months after surgery. 

In general, studies that have used a qualitative approach or disease-specific or health-related scales have shown patients with a stoma with limitations in their everyday living have lower HRQoL  or overall QoL scores than patients unaffected by these issues.^2,19,29 A case-control study³⁰ found HRQoL can be improved if patients attend a patient education group. 

In summary, a large body of research^19-21,24-30 has assessed overall QoL, HRQoL, and ostomy-specific QoL in ostomy patients and several variables were noted to influence scores. However, to the authors’ knowledge, no studies have assessed ostomy-specific adjustments, HRQoL, and overall QoL in the same population of individuals and related these findings to population norms. It is also unknown whether an ostomy-specific adjustment is a predictor of HRQoL and overall QoL, which could lead to strategies that can improve the QoL of patients living with an ostomy. 

Proposed relationships between ostomy-specific QoL as measured with the OAS, HRQoL as measured by the SF-36, and overall QoL measured with the QOLS are shown in Figure 1. The main purpose of this study was to assess whether ostomy-specific adjustment, assessed by the total OAS score, was a predictor for HRQoL and overall QoL, and if any specific ostomy-specific adjustments were strongly related. In addition, HRQoL and overall QoL scores were compared in a cross-sectional study among Norwegian patients with an ostomy and a control group of individuals selected from the general Norwegian population. Specifically, research questions focused on: 

1. Does ostomy-specific adjustment measured with the OAS predict HRQoL measured with SF-36 and overall QoL measured with the QOLS?
2. Which issues of the ostomy-specific adjustments are most strongly related to HRQoL and overall QoL?
3. How do ostomy patients evaluate their HRQoL  and overall QoL compared to the normal Norwegian population?

Materials and Methods

Participants. In this cross-sectional survey, participants were recruited from patient registers maintained by surgical suppliers and pharmacies across Norway between November 2010 and March 2011. In Norway, all ostomy patients receive their ostomy supplies from pharmacies/ostomy suppliers. In order to reach a sufficient number of participants, 13 pharmacies/ostomy suppliers in different regions of Norway were asked to participate in the study. Study materials were sent from the pharmacies/surgical suppliers to patients who had received ostomy supplies for >3 months. Persons who were >18 years old; had a permanent colostomy, ileostomy, or urostomy for >3 months; and could read and write Norwegian were included. The exclusion criterion was having the ostomy for <3 months. The participants received information about the study in a letter from the researcher and returned their demographic information (addressing gender, age, marital status, education, diagnosis, time since surgery, and ostomy type) and study questionnaires using prepaid envelopes. Reminders were sent if materials were not returned within 3 weeks. An informed consent document was included in the cover letter for participants to sign if they decided to participate in the study. The study was conducted in accordance with the Helsinki Declaration and was approved by the Regional Committee for Medical Research Ethics in Western Norway (reference number: 2013/2029). 

Sociodemographic and clinical data. Sociodemographic and clinical data were collected using a standardized form. Ostomy-specific adjustments were measured using the OAS; the SF-36 and QOLS were used to measure HRQOL and provided assessment of an individual’s overall satisfaction with life.

Statistical analysis. Continuous variables were described using means and standard deviations; categorical variables were described using numbers and percentages. For missing items in the OAS and QOLS, the average score was substituted for the mean overall score if at least half of the items were answered in both scales.^15,33 Similarly, for missing items in the SF-36, the average score was used if at least half of the items in a domain were answered across the completed items with the same score.^13,34 The SF-36 and QOLS scores in the cohort were compared with scores from the general population norm, adjusted for age and gender,^13,15 using a 1-sample t-test. Effect sizes of these differences were calculated by subtracting the average scores of the patients from average population scores and dividing by the SDs of the patient group. These SD units were judged against the standard criteria proposed by Cohen³⁵ as follows: trivial (<0.2), small (0.2 to <0.5), moderate (0.5 to <0.8), and large (≥0.8). Simple and multiple ordinary least square regression analyses were used to study whether the OAS sum score was a predictor of the SF-36 scores (PCS and MCS) and the QOLS score. The multiple regression analysis was adjusted for gender, age, marital status, education, diagnosis, time since surgery, and ostomy type. A model of whether the 34 OAS items predicted PCS, MCS, and QOLS and whether a composite score of these outcomes, using partial least square (PLS) regression allowing for multivariate modeling of highly correlated independent variables, also was studied.³⁶ No independent variables other than the 34 OAS items were included in the PLS analyses. In these analyses, the outcomes all were standardized to a mean equal to zero and a SD of 1. 

To assess the robustness of the findings, all models were cross-validated, excluding every fourth subject, to compare the models with each other. Statistical analyses for the PLS regression were conducted using Sirius v. 8.0 software (Pattern Recognition Systems, Bergen, Norway); all other analyses were conducted with SPSS software (version 21; IBM, Armonk, NY). P values were 2-sided, and values <0.05 were considered significant.

Results

Eight (8) out of a possible 13 pharmacies participated. Of 217 initial questionnaires, 5 were returned to the surgical/pharmacy suppliers because of changes in the person’s health status, 54 had no response, and 158 completed questionnaires were returned (74%). The mean age of participants was 64 years (range 29–91). Overall, 89 (56%) men and 69 (44%) women participated in the study; 117 (74%) of the participants were married or cohabiting, 41 (26%) lived alone or with children or parents, 100 (63%) had primary or high school education, and 50 (32%) had college or university education. The main reason for stoma creation was cancer (77.5%), followed by inflammatory bowel disease (IBD; 59.4%) and diverticulosis, interstitial cystitis, and bowel ischemia (19.1%). Most of the respondents (130) had a fecal ostomy; the other 26 had a urostomy. One hundred, five (105, 70%) had their surgery >1 year previous, and 45 (30%) had their surgery <1 year ago. Slightly more than 3% of the questionnaires had too many omissions to be included.

OAS prediction of HRQoL and overall QoL. The average OAS score was 150.2 (SD 30.1). In the linear least square ordinary regression analysis, the OAS significantly predicted the 2 summary scores of the SF-36 and the QOLS (P<0.001 (see Table 1). This finding showed a higher OAS score indicates better levels of HRQoL and overall QoL. 

Ostomy-specific adjustment and relation to HRQoL and overall QoL. Further analysis showed items regarding “living a fulfilling life,” “being free to travel where I want despite my ostomy,” “realizing that this ostomy will be there forever,” “worries about being left alone,” and “embarrassing accidents in sexual activities” were strong predictors of the composite scores of PCS, MCS, and QOLS (see Table 2). 

HRQoL and overall QoL among ostomy patients compared to the control population. The average QOLS score for ostomy patients in the present study was similar to the score of a Norwegian population norm, but the ostomy patients scored significantly lower on the SF-36 domains of physical role functioning, general health, vitality, and MCS (P <0.05) (see Table 3). 

Discussion 

To the authors’ knowledge, this is the first study to show an association between ostomy adjustment and QoL outcomes. This study found the total OAS score was an important predictor of the summary score of the SF-36 and the QOLS, corresponding to moderate effect sizes.¹⁸ Some of the OAS items were better predictors for QoL than others, such as “living a fulfilling life,” “being free to travel,” “realizing that my ostomy will be permanent,” “worries about being left alone,” and “worries about sexual function.” Although the SF-36 scores regarding physical role functioning, general health, vitality, and MCS were significantly lower compared with those of the general population, no significant difference was found regarding the other SF-36 measures and QOLS results. 

Observational studies have investigated associations between symptoms, diagnosis, or sociodemographic factors and QoL²⁴ or the prevalence of complications. Such studies include the descriptive study by Mahjoubi et al³⁷ of 330 patients with a colostomy; however, this study was not specific to the adjustment of patients to life with an ostomy. The adjustment to the ostomy is an ongoing process and, in using the OAS, the degree of adjustment and its impact on QoL outcomes can be measured. The findings of the current study can be used to understand how the patient adjusts to life with an ostomy in general and how the process impacts QoL outcomes. A low total OAS score indicates QoL scores also are lowered. The strongest predictors of QoL outcomes in this study can be thought of as an important group of factors regarding how patients adjust to the physical, psychological, and social impact of having an ostomy. In the analysis, items in the OAS that were the most important regarding QoL outcomes were determined. The association between a low score in OAS items, such as “living a fulfilling life,” “being free to travel,” “realizing that this ostomy will be permanent,” “worries about being left alone,” and “worries about sexual function” significantly influenced both physical and mental health status and overall QoL levels. 

No direct comparative studies have been published, but other observational studies ranging from 57 to 178 patients have found factors such as fear of stoma leaks, skin problems in the parastomal area, and reduced sexual function negatively influence HRQoL.^19-21,23,33 The HRQoL of ostomy patients was compared with the general population in the present study, and the findings were consistent with the longitudinal study by Ito et al³⁸ of 18 successfully treated rectal cancer patients. In both studies, physical role function in ostomy patients was lower than in the general population; Ito et al also found in a cross-sectional study¹⁸ that physical role function (P<0.001)and social role function (P<0.01) were significantly lower than the general population. Furthermore, the mental function score of ostomy patients was statistically significantly lower (P = 0.016) than the control group score in the present study, which also is consistent with findings from the longitudinal study by Carlsson et al,²¹ where ostomy patients scored significantly lower than the norm population in emotional role function, social function, and mental health domains at 1 and 3 months after surgery. With the exception of the mental health domain, HRQoL scores were consistently lower than the general population 6 months postoperatively. As a result of the ostomy, the patient may experience poorer health status or be aware of the limitations related to taking on physical roles, such as manual labor, physical activities that involve sweating and movements that increase the risk of the ostomy pouch becoming loose, or complications such as parastomal hernias. 

Significantly poorer general health and vitality domains compared to the control group scores are more difficult to explain. Ito et al³⁸ addressed lower scores in the physical, social, and role-emotional functioning in their study; these findings may be explained by the physical burden caused by the surgery and the uncertainty that patients perceive in trying to integrate ostomy-related self-care skills into their daily activities. The persistently lower HRQoL  scores in the ostomy patients who participated in this study were also consistent with findings of other studies.^19,21 No significant difference was found in overall QoL levels between ostomy patients and the healthy control group, which was in contrast to the differences in HRQoL scores. This difference may reflect the concept that it is possible to be satisfied with life in general and at the same time report problems with specific aspects of HRQoL associated with living with a stoma. 

The adjustment process to life with an ostomy takes time. The OAS, used several times following surgery, may be useful both directly in the clinic and as an evaluation measure used by nurses and in follow-up care. Using the OAS scale as a supplement in the patient consultation may be a starting point for the discussion between the patient and the clinician in the areas that the patient experiences as most challenging. By using the OAS in measuring adjustment and as a predictor for QoL in ostomy patients, care and follow-up plans for ostomy patients can be evaluated and developed. A valid instrument for assessment is needed. ET therapists and other health care providers should be aware that some domains of HRQoL in ostomy patients may be significantly lower than the norm population, even many years after the operation. This knowledge may help clinicians balance the information they give to patients and may help the patient have realistic expectations of life with an ostomy.

Limitations  

The study design was cross-sectional; as such, OAS and QoL outcomes were simultaneously assessed, and causal interferences cannot be made. Most participants were older than 60 years; therefore it is unknown how a younger population would have scored. Also, only 26 (16%) participants had a urostomy. Finally, 26% of those invited did not participate in the study, so selection bias is possible.

Conclusion

The degree of ostomy-specific adjustment appears to be an important predictor for HRQoL and overall QoL in this group of Norwegian ostomy patients. The OAS measurement tool can be used to evaluate patient adjustment to the ostomy and their QoL and supplement clinical consultation. The results of this study indicate ostomy patients have slightly lower SF-36 scores in physical role functioning, general health, vitality, and MCS levels than the normal population, but the same overall QoL. Further longitudinal studies should explore how ostomy patients adjust to life with an ostomy over time, and how follow-up plans can be further developed and individualized. 

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Potential Conflicts of Interest: none disclosed

Ms. Indrebø is a enterostomal therapist, Department of Surgery, Førde Central Hospital, Førde, Norway. Dr. Natvig is a professor, Department of Global Public Health and Primary Care, University of Bergen, Bergen, Norway. Dr. Andersen is an associate professor, Department of Surgery, Førde Central Hospital; and a Faculty of Health Studies, Sogn and Fjordane University College, Førde, Norway. Please address correspondence to: Kirsten Lerum Indrebø, MSc, Førde Sentralsjukehus, Kirurgisk, Avdeling, Svanehaugvegen 2 Førde 6814, Norway; email: Kirsten.indrebo@gmail.com.

Abstract

Pressure ulcers are common, increase patient morbidity and mortality, and costly for patients, their families, and the health care system. A retrospective study was conducted to evaluate the impact of pressure ulcers on short-term outcomes in United States inpatient populations and to identify patient characteristics associated with having 1 or more pressure ulcers.

The US Nationwide Inpatient Sample (NIS) database was analyzed using the International Classification of Disease, 9th Revision, Clinical Modification (ICD-9 CM) diagnosis codes as the screening tool for all inpatient pressure ulcers recorded from 2008 to 2012. Patient demographics and comorbid conditions, as identified by ICD-9 code, were extracted, along with primary outcomes of length of stay (LOS), total hospital charge (TC), inhospital mortality, and discharge disposition. Continuous variables with normal distribution were expressed in terms of mean and standard deviation. Group comparisons were performed using t-test or ANOVA test. Continuous nonnormal distributed variables such as LOS and TC were expressed in terms of median, and nonparametric tests were used to compare the differences between groups. Categorical data were presented in terms of percentages of the number of cases within each group. Chi-squared tests were used to compare categorical data in different groups. For multivariate analysis, linear regressions (for continuous variable) and logistic regression (for categorical variables) were used to analyze the possible risk factors for the investigated outcomes of LOS, TC, inhospital mortality, and patient disposition. Coefficients were calculated with multivariate regression with all included patients versus patients with pressure ulcers alone. The 5-year average number of admitted patients with at least 1 pressure ulcer was determined to be 670 767 (average overall rate: 1.8%). Statistically significant differences between patients with and without pressure ulcers were observed for median LOS (7 days [mean 11.1 ± 15] compared to 3 days [mean 4.6 ± 6.8]) and median TC ($36 500 [mean $72 000 ± $122 900] compared to $17 200 [mean $32 200 ± $57 500]). The mortality rate in patients with a pressure ulcer was significantly higher than in patients without a pressure ulcer (9.1% versus 1.8%, OR = 5.08, CI: 5.03-5.1, P<0.001). Pressure ulcers were significantly more common in patients who were older or had malnutrition. The results of this study confirm the importance of prevention initiatives to help reduce the negative impact of pressure ulcers on patient outcomes and costs of care. 

Pressure ulcers are one of the most common health conditions in the United States. The Agency for Healthcare Research & Quality (AHRQ) estimates more than 2.5 million individuals in the US develop pressure ulcers annually. The magnitude of this issue is evident in the fact that it spurred the AHRQ (supported by the Health Services Research and Development Service of the Department of Veterans Affairs and the Boston University School of Public Health) to form a panel of pressure ulcer experts from 6 medical centers to develop a pressure ulcer prevention toolkit to be used in acute care settings with a goal to decrease the incidence of pressure ulcers.¹ 

As a result of the subsequent increased health care utilization, medical management of pressure ulcers costs the US health care system $9.1 billion to $11.6 billion per year.¹ Since 2008, the Centers for Medicare and Medicaid Services (CMS) has discontinued hospital reimbursement for charges related to hospital-acquired conditions, which includes patients who acquire pressure ulcers during admission. A hospital stay involving a pressure ulcer may incur additional annual charges of up to $700 000.¹ Treatment costs for a Stage 3 pressure ulcer range from $5900 to $14 840; treatment of a Stage 4 ulcer may cost between $18 730 and $21 410.² 

In addition to direct costs, pressure ulcers incur costs in the form of litigation, penalties, and patient costs. More than 17 000 pressure ulcer-related lawsuits (with an average cost of $250 000) are filed per year.³ Under the Affordable Care Act,³ hospitals also may be penalized up to 1% of their full reimbursement from Medicare if they have high nosocomial infection rates (includes infected pressure ulcers). The cost to the patient who develops a pressure ulcer is of utmost importance. It is estimated that up to 60 000 Americans die each year as a direct result of pressure ulcer-related complications³; a recent white paper² notes pressure ulcers negatively affect a person’s quality of life and contribute to substantial psychological stress, pain, loss of work, burden to family, and mortality. 

Much of the current focus regarding this public health issue is centered on the importance of prevention. Prevention and management of pressure ulcers require an interdisciplinary approach.¹ As the AHRQ pressure ulcer toolkit exemplifies, many health care systems are implementing improved care plans to deliver coordinated, high-quality care to patients with or at risk of developing pressure ulcers.¹ 

The purpose of this retrospective descriptive study was to evaluate the impact of pressure ulcers on short-term outcomes in US inpatient populations and identify patient characteristics associated with having 1 or more pressure ulcers. 

Methods

Data source. Hospital admissions from 2008 to 2012 listed in the National Inpatient Sample (NIS) database (www.hcup-us.ahrq.gov/nisoverview.jsp) were culled. The NIS is the largest national all-payer hospital inpatient care database in the US and is supported by the Healthcare Cost and Utilization Project (HCUP) of the AHRQ. The NIS contains data from more than 1000 community hospitals in the 47 states that participate in HCUP, which represents more than 95% of the US population. The database estimates a 20% stratified sample population of all nonfederal acute care hospitals throughout the US (excluding long-term care acute hospitals and rehabilitation centers). The NIS includes patients with Medicare and Medicaid, persons who are privately insured, and those who are uninsured. Hospital discharge data are collected annually, and the weighted data represent more than 7 million hospital admissions nationally. All patient and physician identifiers have been removed from this data set. Approval from the institutional review board was not required to conduct this analysis. 

Patient selection. Within the HCUP database, patients with pressure ulcers were identified using the International Classification of Disease, 9th Revision, Clinical Modification (ICD-9 CM). Data for all patients having a diagnosis code for pressure ulcer (707.00 through 707.09) during a hospital admission from 2008–2012 were selected with no exclusion criteria. Patient demographics and comorbid conditions were recorded. The comorbidities were calculated with the comorbidity software developed by HCUP (www.hcup-us.ahrq.gov/toolssoftware/comorbidity/comorbidity.jsp#download) based on the study by Elixhauser et al.⁴ In addition, the following risk factors for pressure ulcer development were abstracted based on ICD-9 codes: malnutrition, shock/hypotension, peripheral vascular disease (PVD), incontinence, cerebrovascular disease (CVD), diabetes mellitus, and fractures (vertebral and femur) (see Table 1). Endpoints evaluated were length of stay (LOS, days), total hospital charge (TC), inhospital mortality (Yes/No), and setting to which patient was discharged. The NIS database represents data collected during hospital stay; no postdischarge information was available or analyzed for this study. 

Statistical analysis. Continuous variables with normal distribution were expressed in terms of mean and standard deviation. Group comparisons were performed using t-test or ANOVA test. Continuous nonnormal distributed variables such as LOS and TC were expressed in terms of median, and nonparametric tests were used to compare the differences between groups. Categorical data were presented in terms of percentages of the number of cases within each group. Chi-squared tests were used to compare categorical data in different groups. For multivariate analysis, linear regressions (for continuous variable) and logistic regression (for categorical variables) were used to analyze the possible risk factors for the investigated outcomes of LOS, TC, inhospital mortality, and patient disposition. Coefficients were calculated with multivariate regression with all included patients versus patients with pressure ulcers alone. All statistical analysis was performed using IBM’s Statistical Package for Social Sciences (SPSS) software version 21 (IBM Corp, Armonk, NY). Type I error rate was set at 0.05. 

Results

Patient demographics and prevalence rates. The 5-year average number of admitted patients with 1 or more pressure ulcers in the US from 2008 to 2012 was determined to be 670 767. The total number of annual cases remained stable: 685 526; 678 026; 662 111; 718 550; and 609 620 in the years 2008 to 2012, respectively (see Figure 1). The average overall rate of patients with at least 1 pressure ulcer across all 5 years was 1.8%. Mean overall age of patients with a pressure ulcer was 71.2 ± 16.8 years (male 68 ± 17.4, female 74.1 ± 15.5) (see Table 2). Patients with a pressure ulcer were significantly older than persons without pressure ulcers (P<0.001). The rate of patients with pressure ulcers increased with increasing age. Men had a significantly higher rate than women across all age groups (P<0.001), except for admissions in the youngest age group (see Figure 2). The average overall pressure ulcer rate in men (2.0%, n = 325 293) was significantly higher than in women (n = 351 110, 1.6%) (OR: 1.282, 95% CI: 1.276-1.288, P<0.001).

African Americans had a significantly higher rate (2.4%, n = 119 113 out of 4 979 112) compared to all other races (P<0.05). The rate in Caucasians was the second highest (1.8%, n = 407 006 out of 22 621 329) followed by Native American (1.4%), Asian/Pacific Islander (1.3%), Hispanic (1.2%), and others (1.4%). The rate was highest in individuals with Medicare coverage (3.5%, P<0.05). Patients with Medicaid had a rate of 0.8%; privately insured patients (0.6%) and self-pay patients (0.4%) had the lowest rates (see Table 2). Nonelective admissions had a significantly higher rate than elective admissions (1.9% versus 1.1%, P<0.001). 

Risk factors for pressure ulcers. Risk factors were identified by ICD-9 codes. The risk factor with the highest association with pressure ulcers was a diagnosis of malnutrition (11.5%, risk ratio [RR] = 8.45, CI: 8.41-8.5, P<0.001). Other factors associated with the presence of pressure ulcers included hypotension (5.5%, RR = 3.56, CI: 3.53-3.58, P<0.001), PVD (5.1%, RR = 3.22, CI: 3.19-3.24, P<0.001), incontinence (5.4%, RR = 3.16, CI: 3.12-3.21, P<0.001), CVD (3.8%, RR = 2.46, CI: 2.44-2.48, P<0.001), diabetes (3.2%, RR = 2.38, CI: 2.37-2.39, P<0.001), and fractures (2.7%, RR = 1.56, CI: 1.54-1.58, P<0.001) (see Table 3). 

Pressure ulcer site, stage, and debridement. Among 676 435 pressure ulcer patients, 540 073 (79.8%) had 1 recorded pressure ulcer, 105 383 (15.6%) had 2 pressure ulcers, and 30 979 (4.6%) had more than 2. The most common area for pressure ulcers was the patients’ lower back (lower back/sacral/coccygeal areas per ICD-9) (47%); 17% were located on the patients’ buttock, 14% on the heel, 9% other locations, and 5% on the hip. The ankle, upper back, elbow, and locations not otherwise specified each accounted for <5%. Of the 540 073 pressure ulcers identified, 79 026 (16%) were Stage 1, 191 308 (38%) were Stage 2, 101 093 (20%) were Stage 3, 97 083 (19%) were Stage 4, and 36 081 (7%) were unstageable according to ICD-9 coding (see Figure 3). The median stage of pressure ulcers was 2 for men, women, and Caucasians; the median stage in African Americans was 3. Persons concurrently suffering from malnutrition had a median stage of 3; persons with hypotension, PVD, incontinence, CVD, diabetes mellitus, and vertebral/femur fractures had a median stage of 2. A total of 71 418 excisional debridements were performed in 65 582 patients; 5462 patients required multiple procedures. 

Impact on patient outcomes. 

LOS. The median LOS for individuals with at least 1 pressure ulcer was 7 days (mean 11.1 ± 15), compared to a median of 3 days (mean 4.6 ± 6.8) for patients without a pressure ulcer. Patients were significantly more likely to have a longer LOS (all P<0.001) if they had the following risk factors: weight loss (regression coefficient [coef] = 4.88), paralysis (coef = 3.20), coagulopathy (coef = 2.04), congestive heart failure (CHF) (coef = 1.17), fluid/electrolyte disorder (coef = 1.70), and pulmonary/circulation disease (coef = 2.05). 

Cost. Multiple factors contributed to hospital charges. The presence of a pressure ulcer increased costs. The median TC for persons with pressure ulcers was $36 500 (mean $72 000 ± $122 900) compared to persons without pressure ulcers, whose median TC was $17 200 (mean $32 200 ± $57 500). Increased hospital charges were significantly associated (P<0.001) with LOS (coef = 8613), male gender (coef = 4464), African American race (coef = 3483), having private insurance (coef = 7643), or Medicaid beneficiaries (coef = 3729). The following comorbid conditions also significantly affected TCs: pulmonary/circulation disease (coef = 7062), PVD (coef 5887), obesity (coef 4229), hypotension(coef = 2530), and fluid/electrolyte disorders (coef = 3971).

Mortality. Patients with a pressure ulcer had a significantly higher mortality rate than patients without (9.1% versus 1.8%, OR = 5.08, CI: 5.03-5.1, P<0.001); the latter also were more likely to be discharged home (72.5% versus 13.4%, OR =5.42, CI: 5.39-5.45, P<0.001), whereas patients with pressure ulcers were more likely to be transferred to a skilled nursing facility or intermediate care facility or require home health care (76.9% versus 24.7%, OR = 3.116, CI: 3.112-3.121, P<0.001). 

Discussion

The National Pressure Ulcer Advisory Panel⁵ (NPUAP) defines a pressure ulcer as “localized injury to the skin and/or underlying tissue usually over a bony prominence, as a result of pressure, or pressure in combination with shear and/or friction.” 

Although the NPUAP recently changed the term pressure ulcer to pressure injury, the term pressure ulcer is used throughout this article to maintain consistency with the ICD-9 coding used during the study period.

Pressure ulcers occur in up to 23% of patients in long-term and rehabilitation facilities⁶ and at an incidence of 10% to 41% in ICU patients.^7,8 The AHRQ² reported nearly 2.5 million individuals are affected by pressure ulcers, and more than 60 000 patients⁹ in the US die each year as a direct result of pressure ulcers. The costs associated with pressure ulcers are considerable. According to a 1996 prospective, year-long study looking at 30 patients and conducted by Xakellis and Franz,¹⁰ the incremental cost per pressure ulcer in the US was $2731. Per a retrospective review,¹¹ the cost could be as high as $59 000 if the ulcer was associated with osteomyelitis. Medicaid⁹ estimated each pressure ulcer adds $43 180 in costs to an individual’s hospital stay. 

Pressure ulcers also have a significant impact on patient morbidity, mortality, and quality of life.² In their review of pressure ulcers in intensive care patients, Burdette and Kass¹² described pressure ulcers as one of the most expensive and debilitating diseases in the 20th century. In her review of risk factors and the assessment of pressure ulcer risk assessment, Braden¹³ indicated the complexity of the management and treatment of pressure ulcers can greatly reduce the quality of life, resulting in a worldwide economic dilemma. Similarly, in their retrospective review of the 2003 NIS database, Fogerty et al¹⁴ demonstrated the complexity of pressure ulcer development and the multiplicity of contributing risk factors. 

The overall incidence and prevalence of pressure ulcers have been shown in 2 reviews of the literature^15,16 to remain high in the US despite the supposed improvement in the quality of health care in general and the drastic improvement in understanding these ulcers or the improvements in technologies available for prevention of ulcers specifically. The current study found the annual number of pressure ulcers reported in the US inpatient population was 670 767. Overall, the number of annual cases has remained constant at approximately 600 000 to 700 000 patients during the 5-year period of the study, with a rate of 1.8%. These numbers are lower than the 2.5 million reported by the AHRQ⁹ due to the fact the NIS database only accounts for those individuals with pressure ulcers who were hospitalized. Advances in pressure ulcer management have enabled these patients to receive treatment in outpatient care centers, with the goal of decreasing the duration of hospitalization, readmission rates, additional patient morbidity, and total care costs.⁹

In the opinion of the authors, the observed absence of a decrease in pressure ulcer rates may be attributed to: 1) failure or inadequate application of available prevention strategies during hospital admission or in other patient care environments, or 2) improvements in pressure ulcer assessment and reporting. 

Risk factors. Conflict exists as to whether pressure ulcers result from factors largely dependent on caregivers or primarily from factors associated with patient morbidity. It is well established that pressure ulcers continue to be a common health problem, particularly among individuals with physical limitations or persons who are elderly and bedridden. 

Age. Perneger et al¹⁷ evaluated the incidence of pressure ulcers (N = 2373) by conducting 3 cross-sectional surveys in a teaching hospital among patients with no pressure ulcer documented on admission. The authors assessed the development of pressure ulcers and the date on which the ulcer was documented and correlated this with diagnosis and reason for admission, among other factors. They found 247 new pressure ulcers occurred during admission (5.7 per 1000 person-days). The risk of pressure ulcer occurrence increased with age (11.2% of patients ages 70 to 79 years versus 34% in patients >90 years). Their results are consistent with the current study where the mean overall age of patients with a pressure ulcer was 71.2 years (68 years in men and 74 years in women), with increasing rates in older age groups. Jaul¹⁸ described pressure ulcers as chronic and healing in the geriatric population; the author indicated the presence of a pressure ulcer constituted a “geriatric syndrome” that was a result of multiple factors: immobility, poor nutrition, aging skin with poor elasticity, and numerous chronic diseases. 

The US is experiencing a significant increase in the aging population. By the year 2050, the population 65 years of age and older will nearly double. This creates an urgent need for better prevention strategies and management of pressure ulcers.

Gender. In the current study, the prevalence of pressure ulcers was significantly higher in men (2%) than women (1.6%) (OR: 1.282, 95% CI: 1.276-1.288, P<0.001). Inconsistent conclusions have been drawn as to which gender has a higher predilection for pressure ulcer development. The Waterlow score,¹⁹ developed in 1987 as a tool for pressure ulcer risk assessment, accommodates for research showing women are at a greater risk for development of a pressure ulcer; female gender is assigned a score of 2, where men are assigned a score of 1. This scoring system accounts for gender differences in the observation of predisposition of women to pressure ulcers in individuals who had femoral fractures.²⁰ Similar results were found in a 2-phase epidemiological study (N = 327 patients) by Bale et al²¹ that looked specifically at hospice patients. In addition, the authors found decreased pressure ulcer development with the use of a risk assessment tool and subsequent proactive measures such as offloading surfaces. Contrarily, in a prospective cohort study (N = 258), Primiano et al²² observed higher rates of pressure ulcers in men. The authors evaluated preoperative, intraoperative, and postoperative risk factors in cases where surgery lasted >3 hours; using bivariate and logistic regression analyses, male gender was found to be predictive of pressure ulcer development. The authors suggested the difference in distribution of adipose tissue in females was protective against pressure ulcer development. The current authors think the higher prevalence among male patients can be attributed to other associated risk factors as opposed to gender predilection. A multicenter cohort study of 3361 patients by Chen et al²³ noted the higher number of spinal cord injuries observed in men could result in more pressure ulcers when compared to women. Gibson et al²⁴ observed similar results in their 2002 qualitative study. The Braden scale²⁵ does not recognize any difference in pressure ulcer risk associated with gender, which is in accordance with other prevalence/incidence research.^26,27 A review²⁸ of risk assessment found gender difference observed in pressure ulcer development also could be a reflection of the complexity of the overall problem, the multitude of causative events and comorbid conditions, and the lack of a universal risk assessment/classification tool.²⁷

Race/ethnicity. In the US, race/ethnicity, low socioeconomic status, occupation type, and education are consistently related to reduced access to quality health care. Previous studies have reported a significant association between race/ethnicity and pressure ulcer development: a qualitative study by Saladin and Krause²⁹ conducted among post spinal cord injury patients of varying racial-ethnic backgrounds (105 American Indian, 127 Caucasian, 122 Hispanic, 121 African American) found variability in access to treatment may lead to minority populations experiencing higher pressure ulcer prevalence.  A cross-sectional study³⁰ found African American ethnicity was a predictor of pressure ulcer recurrence. However, Furher et al³¹ found no differences in the prevalence of pressure ulcers between African Americans and Caucasians in the general population, although they reported African Americans suffered greater pressure ulcer-related mortality and suffered from more severe, higher-staged ulcers. An age-adjusted descriptive study using matched odds ratio comparisons by Redelings et al³² found African Americans had higher mortality from pressure ulcers than Caucasians. In general, African Americans tend to have less education and higher poverty rates at all ages compared to Caucasians, as shown by the survey analysis of health disparities using the US National Health and Nutrition Survey and follow-up interviews conducted by Farmer and Ferraro.³³ The results were no different in the current study: pressure ulcer incidence rates were higher in African Americans (2.4%, n = 119 113 out of 4 979 112) compared to all the other races (P<0.05). Caucasians had the second highest incidence rate (1.8%, n = 407 006 out of 22 621 329) compared to other minority races such as Native American (1.4%), Asian/Pacific Islander (1.3%), Hispanic (1.2%), and other races (1.4%).

Insurance. In November 2008, the CMS instituted a policy to withhold reimbursement to acute care hospitals for the costs of treating hospital-acquired conditions such as pressure ulcers.³⁴ Despite these policies, pressure ulcer rates were the highest in persons with Medicare coverage (3.5%, P<0.05). The prevalence rates for patients with Medicaid, private insurance, and self-pay patients were 0.8%, 0.6%, and 0.4%, respectively. The high rate of pressure ulcers in Medicare patients may be attributed to the fact that persons eligible for Medicare are 65 years or older, which subsequently places them at higher risk for development of pressure ulcers according to the literature and the current study results. 

Comorbidities. 

Nutrition. According to a descriptive analysis by Duncan³⁵ and a review by Lyder and Ayello,³⁶ immobility, inadequate nutrition, sensory deficiency, multiple comorbid conditions, circulatory abnormalities, dehydration, age, and incontinence are a few of the more than 100 factors identified as placing adults at risk for developing pressure ulcers. Of all the risk factors, malnutrition contributed the most significantly to pressure ulcer prevalence in the current study (11.5%, RR = 8.45, CI: 8.41-8.5, P<0.001). Compromised nutritional status such as unintentional weight loss, undernutrition, protein energy malnutrition, and dehydration are known risk factors for pressure ulcer development.³⁷ As shown in a pilot study³⁸ and a retrospective cohort study,³⁹ additional nutrition-related risk factors associated with increased risk of pressure ulcers include low body mass index, reduced food intake, and impaired ability to eat independently. These factors might reflect poor health and self-care that is associated with higher incidence of pressure ulcers.

Tissue perfusion. Reduced tissue perfusion is known to play an important role in the development and chronicity of pressure ulcers. Mechanical loading may be significant enough to compromise the capillary circulation, causing ischemia and cell death in areas of pressure and, subsequently, ulcer development. Hypotension and PVD play a similar role. In a retrospective cohort study by Man et al,⁴⁰ hypotension was found to be an important risk factor for pressure ulcer development in the geriatric population. In the current study, rate of pressure ulcers was high in patients with hypotension (5.5%; RR = 3.56, CI: 3.53-3.38, P<0.001) and PVD (5.1%; RR = 3.22, CI: 3.19-3.24, P<0.001). 

pH. The pH of normal skin (pH 5.4–5.9) has a bactericidal effect and limits the growth of pathogenic organisms. In the event of urinary incontinence, due to reasons such as CVD, urinary urea decomposes on the skin to form ammonium hydroxide, which raises the skin pH and favors bacterial proliferation. A descriptive study by Leveen et al⁴¹ also shows high pH also negatively impacts the delivery of oxygen to damaged tissue, making wound healing even more challenging. Fecal incontinence also can cause skin irritation and breakdown. The current study showed patients with CVD had a pressure ulcer rate of 3.8% (RR = 2.46, CI 2.44-2.48, P<0.001), and the rate was 5.4% rate (RR = 3.16, CI: 3.12-3.21) among persons with incontinence. 

Diabetes and fractures. Other factors that may contribute to pressure ulcer development include diabetes and fractures. Blood sugar control is known to play an important role in wound healing. Persons with diabetes are at risk for developing both pressure ulcers and diabetic foot ulcers, owing to the neuropathy and tendency for unnoticed trauma. In the current study, the rate of pressure ulcers among patients with diabetes was 3.2% (RR = 2.38, CI 2.37-2.39, P<0.001). A retrospective review of data⁴² found fractures that result in immobilization, such as hip⁴² and femur²⁰ fractures, predispose to the development of pressure ulcers. In the current study, patients with fractures had a pressure ulcer rate of 2.7% (RR = 1.56, CI 1.54-1.58, P<0.001).

Ulcer quantity, site, and stage. Documenting the number, site, and stage of ulcers is crucial in pressure ulcer management. Among the 676 435 patients studied in this NIS database, 540 073 (79.8%) had 1 ulcer recorded, 105 383 (15.6%) had 2 pressure ulcers, and 30 979 (4.6%) had more than 2 ulcers. Bony prominences are more susceptible to pressure ulcers as a result of deformation of deep tissues and muscle atrophy. A review of the literature⁴³ found shear force and friction injury to skin surfaces create a process in which the epidermal and dermal layers adhere to bed surfaces causing destructive events to the underlying areas of the skin. The most vulnerable pressure points depend on the position in which most of the patient’s time is spent. The current data showed a majority (47%) of the pressure ulcers were located on the patients’ lower backs (sacrum). Excessive moisture results in hyperhydration of the skin, rendering it more vulnerable to dermal erosion. The high percentage of lower back pressure ulcers could be an amalgamation of the influence of shear force, friction, and moisture in patients who are bedbound. Patients also had pressure ulcers on the heel (14%), hip (5%), and other locations (9%). The ankle, upper back, elbow, and locations not otherwise specified each accounted for <5%. A systematic review of the literature⁴⁴ (including 3 RCTs and 1 economic study [N = 502]) recommends manual repositioning of these patients for both treatment and prevention of pressure ulcers. However, the ideal repositioning regimen and frequency has yet to be determined, per a systematic review by Moore and Cowman.⁴⁵ 

Pressure ulcer staging affects both treatment and prognosis. The NPUAP⁴⁶ redefined the stages of pressure ulcers in 2007 to include the original 4 stages plus 2 additional stages (deep tissue injury and unstageable). The reported incidence of pressure ulcers Stage 2 or greater is between 8.1% and 12.9%.^47,48 The current data analysis showed both male and female patients had a median pressure ulcer Stage 2. Among Caucasian and other populations, the median stage of pressure ulcers was Stage 2, whereas the median stage for the African American population was Stage 3. The advanced stages seen in African Americans may be attributed to poor general condition or due to difficulty in detecting early pressure ulcers stages due to the clinical difficulty in observing erythema and blanching response in dark skin. The current authors observed patients who suffer from malnutrition had a median ulcer stage of 3, and patients with diabetes, CVD, incontinence, PVD, and hypotension had a median ulcer stage of 2. This could be attributed to frequent surveillance for pressure ulcers in these high-risk patients in nursing homes and hospitals. 

For Stage 1 and Stage 2 pressure ulcers, wound care typically does not involve surgery. Management at these stages may involve topical therapy, offloading, and optimization of nutrition/moisture management, as well as proper management of the underlying cause. For Stage 3 and Stage 4 ulcers, surgical intervention may be required, although a review⁴⁹ has shown some of these lesions might be treated conservatively due to coexisting medical problems. Generally, excisional surgical debridement is the standard care for higher-stage pressure ulcers because these often present with necrosis. In the current data, a total of 71 418 excisional debridement procedures were performed in 65 582 patients; of those, 5462 patients required multiple debridement procedures.

LOS. According to a limited literature review,⁵⁰ prolonged LOS is a significant predictor of functional decline in elderly individuals during hospitalization. A 9-year, prospective observational registry study of 275 pressure ulcers by Lardenoye et al⁵¹ showed 5.5% of all pressure ulcers resulted in prolonged hospitalization and found a strong correlation among pressure ulcer development, reason for hospital admission, gender, and age. In a cross-sectional, observational study (N = 2000), Graves et al⁵² concluded the presence of pressure ulcers was a significant independent contribution to excess length of hospitalization. LOS has been shown to be prolonged an average range of 4 to 6 days, including in the descriptive, comparative study of 2 cross-sectional pressure ulcer surveys^52,53 by Gunningberg and Stotts.⁵⁴ The current study shows the median LOS for individuals with at least 1 pressure ulcer was 7 days (mean 11.1 ± 15) compared to a median of 3 days (mean 4.6 ± 6.8) in patients without pressure ulcers. Patients with significant weight loss, paralysis, coagulopathy, CHF, fluid and electrolyte disorders, and pulmonary and circulation diseases with concurrent diagnosis of at least 1 pressure ulcer were more likely to have a longer LOS.

Cost. Prolonged LOS not only affects the morbidity and mortality of patients, but it also has a significant impact on hospital charges. The current study estimated the median TC to be $17 200 (mean $32 200 ± $57 500) in patients without pressure ulcers. In contrast, the median hospital charges for patients with pressure ulcers were significantly higher at $36 500 (mean $ 72,000 ± $122 900, P<0.001). Along with pressure ulcers, increased LOS (coef = 8613), male gender (coef = ,464), African American race (coef = 3483), private insurance beneficiaries (coef = 7643), and Medicaid beneficiaries (coef = 3729) significantly impacted total hospital charges. Other conditions that contributed to increased hospital charges were pulmonary/circulation disease (coef = 7062), PVD (coef = 5887), obesity (coef = 4229), hypotension (coef = 2530), and fluid and electrolyte disorders (coef = 3971). 

Mortality. Pressure ulcers play a significant role in influencing the mortality rate among hospitalized patients and patients in nursing facilities. A retrospective study by Lyder et al⁵⁵ showed that of 3000 individuals who entered the hospital with a pressure ulcer, 16.7% developed at least 1 new pressure ulcer during their stay. The odds of any patient dying in the hospital were 2.8 times higher if the patient had a pressure ulcer. In the current study, the mortality rate in patients with pressure ulcers was significantly higher than in patients without pressure ulcers (9.1% versus 1.8%, OR = 5.08, CI: 5.03-5.1, P<0.001). The current data analysis also showed 72.5% of patients without pressure ulcers were discharged home compared to 13.4% patients with pressure ulcers (OR 5.42, CI: 5.39 – 5.45, P<0.001). Furthermore, 76.9% patients with pressure ulcers were transferred to a skilled nursing facility or intermediate care facility or required home health care compared to 24.7% patients without pressure ulcers (OR = 3.116, CI: 3.112-3.121, P<0.001). This observation is consistent with previous reviews.^56,57 The additional fees for skilled nursing facilities add to the increase in health care expenditure on treatment and management of this preventable health issue. 

Limitations

The results of this study are limited by the inherent limitations of retrospective analysis of administrative data, which includes the risk of erroneous coding or missing data. Given that ICD-9 codes were used, some error in pressure ulcer diagnosis and description of coding can be assumed. On the other hand, the large sample size is expected to minimize errors associated with data recording and should not interfere with the general conclusion. Also, the authors could not differentiate between pressure ulcers that were hospital-acquired and present on admission; although the aim of the study was not to delineate between them, knowledge about their onset would have enhanced overall conclusions, especially in terms of deep tissue injury and its sometimes slow clinical appearance. Readmission rates, which were not available for this investigation, also may have inflated the number of patients with pressure ulcers. Lastly, while the data facilitated the categorization of patients without pressure ulcers, this may minimally weight the data, because patients at risk are more likely to develop more than 1 pressure ulcer. 

Conclusion

The results of this study show the rate of pressure ulcers among patients in US acute care hospitals was relatively stable from 2008 until 2012 (average 1.5%). Patients who had a pressure ulcer had a significantly longer LOS, higher in-hospital mortality rate, and higher TC than patients without a pressure ulcer. Patients with pressure ulcers were also more likely to be discharged to a skilled nursing facility, while those individuals without pressure ulcers were more likely to be discharged home. The ICD-9 code associated with a significantly higher risk of having a pressure ulcer was for malnutrition. Pressure ulcers have been recognized as being a public health issue in the US that contributes greatly to national health care expenditures. Early treatment and a reduction of pressure ulcer rates have been set as goals by the CMS. The Institute of Healthcare Improvement has created the 5 Million Lives Campaign; 1 of the main goals is to use science-based guidelines for prevention. It is crucial that the severity of this issue be recognized and that health care centers develop an interdisciplinary approach to the delivery of coordinated, high-quality care to patients with, or at risk for, developing pressure ulcers. 

References

1. Berlowitz Dea. Preventing pressure ulcers in hospitals: A toolkit for improving quality of care. Available at: www.ahrq.gov/sites/default/files/publications/files/putoolkit.pdf. Accessed December 30, 2015.

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56. National Quality Measures C. Long-stay nursing home care: percent of high-risk residents with pressure ulcers.  Available at: www.qualitymeasures.ahrq.gov/content.aspx?id=38336. Accessed February 9, 2016.

57. Institute of Healthcare Improvement. Relieve the Pressure and Reduce Harm. Available at: www.ihi.org/resources/pages/improvementstories/relievethepressureandredu... eHarm.htm. Accessed February 9, 2016.

Ms. Bauer is Director of Wound Services, Division of Vascular/Endovascular and Wound Care, University of Toledo Medical Center, Toledo, OH. Dr. Rock is a general surgery resident, St. John’s Hospital and Medical Center, Detroit, MI. Dr. Nazzal is Chief; Ms. Jones is Office Manager; and Dr. Qu. is an Assistant Professor and Director of Vascular Research, Department of Surgery, University of Toledo Medical Center. Please address correspondence to: Karen Bauer, NPC, CSW, CHRN, University of Toledo Medical Center, Division of Vascular/Endovascular and Wound Care, 3064 Arlington Avenue, Toledo, OH 43614; email: Karen.Bauer@utoledo.edu.

Potential Conflicts of Interest: none disclosed

Abstract

Patients in critical care areas are at risk for developing hospital-acquired pressure ulcers (HAPUs) due to their physical conditions and limited ability to reposition themselves. A prospective, 2-phase quality improvement study was conducted from September to November 2011 and from February to April 2012 in 1 medical and 1 surgical ICU to investigate the impact of a turn-and-assist device on the incidence of HAPUs and the time and personnel required to reposition patients reported as person/minutes (staff x minutes).

A consecutive, convenience sample of patients was selected from newly admitted ICU patients who were at least 18 years old, nonambulatory, and required 2 or more people to assist with turning and repositioning. Sociodemographic data (patient age, gender, height, weight, body mass index, incontinence status); total Braden score and subscores for Activity, Mobility, and Moisture on admission; length of ICU stay and ventilator days; and sacral pressure ulcer incidence and stage and turn-and-assist data were collected. Fifty (50) patients participated in each phase. In phase 1, standard care for positioning included pillows, underpads, standard low-air-loss beds and additional staff as required for turning. In phase 2, the study product replaced standard care repositioning products including pillows; and a larger disposable moisture-wicking underpad (included as part of the turn study project kit) was substituted for the smaller, standard moisture-wicking disposable underpad. Turning procedures were timed with a stopwatch. Data were collected for a total of 32 hours during the observation periods; all patients were followed from admission until discharge from the ICU for a maximum of 14 days. T-tests were used to compare patient characteristics and person-minutes needed for repositioning differences, and Fisher’s exact test was used to compare the incidence of sacral HAPUs during phase 1 and phase 2 of the study. No statistically significant sociodemographic or clinical differences were noted between the 2 groups. During phase 1, 14 patients (28%) developed a Stage 2 sacral HAPU. During phase 2, no patients developed a sacral HAPU (P<0.0001). The average time spent for repositioning was 16.34 person/minutes (range 4–60, SD 10.08) during phase 1 and 3.58 minutes (range 1.12–8.48, SD 2.31) during phase 2. The mean difference between person/minutes for the 2 phases was 12.76 minutes (P = 0.0006). In this population of ICU patients, the rate of sacral HAPUs and person/time needed for repositioning were significantly lower following implementation of a turn-and-assist product. Future research is indicated on the effect of this type of product on improving outcomes for patients and making the work of patient care safer and more efficient.

Patients in critical care areas are at risk for developing hospital-acquired pressure ulcers (HAPUs) due to their physical conditions and often limited ability to reposition themselves.¹ HAPU data estimate prevalence to range from 10% to 41% in adult ICUs.^1–5 The International Pressure Prevalence Survey⁶ (2008–2009) reported a HAPU prevalence in the medical ICU of 20.7% (N = 1940) and in the surgical ICU of 16.6% (N = 1842). 

Repositioning has been shown in randomized, controlled trials^7,8 to help prevent the development of pressure ulcers. However, additional randomized, controlled trials and observational studies^9-11 have demonstrated that implementing best practices in preventing pressure ulcers in the intensive care unit (ICU) is fraught with numerous obstacles, including nurse perception of the patient’s medical readiness for repositioning and mobility and the physical challenges associated with repositioning patients, which can be complicated by the work environment, including high patient acuity and limited staffing resources. According to a retrospective review,¹¹ patients receiving hemodynamic or oxygen support, multiple vasopressors, continuous renal replacement therapy, extracorporeal membrane oxygenation, or high-flow oscillator ventilation are often physically unstable and may not be able to tolerate turning and repositioning. In other situations (eg, patients with a high body mass index [BMI], critical illness, or isolation), staff may be required to utilize personal protection equipment (PPE) or multiple staff members to safely turn the patient. When staff is limited in number to assist with turning and repositioning due to high patient acuity and care needs, it can be a challenge to meet the recommendations for frequent turning.⁷ 

Although repositioning these patients is essential to their care, it can be challenging for staff to accomplish this safely and efficiently. Safe patient handling is defined by the American Nurses Association¹² (ANA) as “policies and programs that enable nurses to move patients in a way that does not cause musculoskeletal strain or injury to the clinical staff.” Safe patient handling is a concept that is in direct alignment with recommendations in the Occupational Safety and Health Administration¹³ (OSHA) manual stating: “Manual lifting of patients should be minimized in all cases and eliminated when feasible. Employers should put an effective ergonomics process in place that provides management, involves employees, identifies problems, implements solutions, addresses injury reports, provides training, and evaluates ergonomic efforts.”

Lifting is not the only aspect of moving patients that presents physical demands for nursing staff. National labor statistic reporting^14,15 shows lateral transfers (repositioning the patient in the bed, turning the patient in the bed, moving the patient to the head of the bed, and transferring the patient from bed to bed) are the most frequent type of patient transfers; they are reported to require the most exertion for dependent patients. More than half of the injuries attributed to personnel working in health care are due to overexertion and most frequently result from lifting, further emphasizing the need for adhering to Safe Patient Handling best practices.²

The average HAPU rates in 2 of the ICUs in the authors’ hospital were higher than the benchmarks provided by the National Database for Nursing Quality Improvement¹⁶ (NDNQI) and rates for similar units. This was of concern to administration and frontline nurses, and a quality improvement project was designed to reduce the incidence of HAPUs. A study team comprised of the Clinical Nurse Specialist, the nurse researcher, and registered nurses from the ICUs developed a study to enhance turning and repositioning of patients while incorporating concerns for staff safety during this process. 

The study device (Prevalon Turn and Positioning Systems® 2.0 [TAP], Sage Products, Cary, IL) is designed to assist staff with turning and repositioning patients and to help reduce the incidence of pressure ulcers by offloading the sacrum. This is achieved by helping patients maintain a 30˚ side-lying position. The system has 3 components: 1) a low-friction, microclimate glide sheet with integrated handles placed under the patient to help prevent skin injury from shearing and friction forces; 2) a disposable moisture-wicking incontinence underpad to assist with incontinent effluent containment; and 3) 2 foam wedges designed to help bolster the patient’s sacral offloading position. The microclimate glide sheet stays with the patient throughout the duration of the admission, and the disposable moisture-wicking incontinence underpad is replaced every 12 hours or as needed if it becomes soiled. Although data to support that this device reduces the incidence of HAPUs are limited to case study series and anecdotal reports, the device addresses multiple clinical issues commonly correlated to the development of sacral pressure ulcers.

The purpose of this study was to evaluate the impact of this patient repositioning system on 1) the incidence of sacral pressure ulcers and 2) the amount of time required to turn and reposition stable, but immobile ICU patients pre- and post-implementation of the device.

Methods

Setting. This study was conducted in 2 12-bed ICUs (1 medical, 1 surgical) at a Magnet-designated, 703-bed Level I trauma center in western Virginia. These units were selected because of their consistently high HAPU rates and high level of patient acuity, which made their patient population well-suited to the study purposes. The hospital Institutional Review Board deemed this project a quality improvement study, and patient consent was not required.

Sample. A consecutive, convenience sample of patients was selected from newly admitted ICU patients who were at least 18 years old, nonambulatory, and required 2 or more people to assist with turning and repositioning determined by nursing assessment of a Braden Scale mobility subscore <2. Patients who were able to assist with turning or unable to tolerate repositioning (systolic blood pressure decreased ≥10 mm Hg when attempting to turn) were excluded from the study. Patients also were excluded from the study if they had been admitted to the units before initiation of the project or if they had a pressure ulcer on the sacrum/coccyx/buttocks that was present on admission to the ICU. The charge nurse of the units reviewed each admission and determined if the patient met the inclusion criteria. At that time, the nurse caring for the patient was informed the patient was to be included in the study and the appropriate documentation and protocol were implemented. The primary investigator (PI), a doctoral-prepared, wound care Clinical Nurse Specialist, reviewed patient admissions each day to confirm appropriate inclusion and exclusion. 

Outcome measures. The primary outcome measures for the study were the incidence of sacral HAPUs in the ICUs and the time required for turning and repositioning patients following implementation of the TAP. For the purpose of this study, HAPUs were defined as the occurrence of new pressure ulcers during the study period, staged according to the National Pressure Ulcer Advisory Panel Guidelines for Pressure Ulcer Staging.¹⁷ The amount of time required to turn and reposition patients was recorded as person-minutes (ie, the number of minutes to prepare for and reposition the patient, multiplied by the number of staff members performing the task¹⁸). 

Study phases.

Phase 1: assessment. In Phase 1, study nurses reviewed all new admissions to the study ICUs from September to November 2011 to identify patients who met inclusion criteria. Patients included in the study had skin assessments and turning interventions documented within 6 hours of admission. All patients were assessed daily and repositioned at least every 2 hours per facility policy. No study product was provided during this phase of the study; nursing staff provided standard care for turning and repositioning tasks using pillows, underpads, and standard low-air loss ICU beds as well as additional staff for repositioning as required. At the beginning of this phase, the PIs (a Wound Care Clinical Nurse Specialist and the Nurse Researcher) educated staff regarding pressure ulcer staging, wound differentiation, study protocol, and documentation. 

Phase 2: intervention. This phase of the study occurred from February 2012 to April 2012. Before implementing phase 2, the PI educated the staff about proper use of the TAP and ensured the product was available in the ICUs supply rooms. Signs were placed outside the rooms of the patients enrolled in the study to provide visual reminders to the staff to use the TAP. During this phase of the study, patients were placed on standard low-air-loss ICU beds, and the TAP system was used for turning and repositioning in lieu of pillows and standard-size, moisture-wicking disposable underpads. 

Data collection and analysis. All staff members, consisting of Bachelor and Associate Degree Registered Nurses, were trained by the PI on skin assessments, pressure ulcer staging, and study protocol at the beginning of each phase of the study. Turnover on these units during the study period was limited. Only registered nurses provide patient care in these units; assistive personnel did not complete assessments or provide patient care. Nurses completed skin assessments twice daily and recorded data on the paper assessment sheet developed by the PI, who transferred the data to a spreadsheet. Study nurses recorded if patients developed a sacral HAPU and staged the ulcer per NPUAP guidelines.¹⁷ 

The PI conducted daily rounds during both phases of the study to ensure enrolled patients met inclusion criteria and that data collection and patient assessment, including pressure ulcer staging, were accurate. All patients enrolled in the study were followed daily from admission for 14 days or until discharge from the ICU. None of the patients in phase 1 were included in phase 2 of the study. 

Patient characteristics. Patient characteristics recorded included age, gender, height, weight, BMI, incontinence status, total Braden score and subscores (Activity, Mobility, and Moisture) on admission, length of ICU stay, and ventilator days. Data were collected for 100 patients who met inclusion criteria (50 in each phase). 

The PIs observed unit nurses to determine the time required for turning and repositioning patients before and during the implementation of the TAP. The observation period used a modified Work-Sampling Method by Activity Timing (WOMBAT) technique that used manual calculations rather than electronic data input.^19,20 Data were collected for a total of 32 hours (4 4-hour periods during day and evening shifts in each of the phases). Time was measured with a stopwatch and included the physical time and the number of clinicians required to perform a turn and repositioning maneuver, average time per task, and time spent with patients. Timing of the work was stopped during interruptions to this process. 

The time elapsed and the number of clinicians required were recorded on a paper graph form and transferred to a spreadsheet. The PIs collaborated to develop a consistent observation method during a 1-hour time period on 1 of the ICUs to be sure the observations of the work flows were consistent between them. 

Descriptive statistics including range, frequencies (percentages), and means were reported for patient characteristics. T-tests were conducted to determine if the groups were statistically similar on specific characteristics (see Table 1). Fisher’s exact test was performed to determine statistical significance between the incidence of HAPUs in each phase of the study. Person-minutes for the 2 phases were reported as the difference in total time. The t-test was used to calculate significance between means in the 2 phases of the study. 

Results

Patient characteristics. A total of 100 patients were included; 50 in phase 1 for baseline comparison purposes and 50 in Phase 2 for the intervention group. In phase 1, 30 patients (60%) were male, 20 patients (40%) female; in phase 2, 28 patients (56%) were male, 22 (44%) female. In phase 1, 47 (94%) patients had indwelling catheters and 1 (2%) was incontinent of urine. Forty-eight (48) patients (96%) in phase 2 had indwelling catheters and 1 (2%) was incontinent. Patients in both phases had fecal management devices: 27 (54%) patients in phase 1 and 26 (52%) in phase 2. No statistically significant differences (P = 0.05) were noted between the patient populations of phases 1 and 2 in terms of age, weight, Braden scale scores, length of stay in the ICU, and days on the ventilator (see Table 1). 

HAPU rates. During phase 1 of the study, 14 patients (28%) receiving standard care developed a sacral area HAPU, all of which were Stage 2. During phase 2 of the study, following the implementation of the TAP, no patients developed a sacral HAPU. Fisher’s exact test indicated a significant difference (P<0.0001) in the incidence of HAPUs of the sacrum between phase 1 and 2 following implementation of the TAP product for turning patients.

Time for turning and repositioning. During phase 1, 23 turning/repositioning maneuvers were observed and recorded by either the PI or the Nurse Researcher. An average of 2.26 staff members (range 2–5) required an average of 5.89 minutes to reposition a patient (range 2–12 minutes). In terms of person-minutes, the mean time spent on the maneuver was 14.14 minutes (range 4–60, SD 11.55). During phase 2, it took an average of 1.48 staff members (range 1–4) an average of 2.38 minutes (range 1.12–4.06) to reposition a patient. Mean person-minutes for phase 2 was 3.28 minutes (range 1.12–8.48, SD 1.93). The mean difference between person/minutes for phase 1 and 2 was 10.86 minutes. The t-test analysis indicated a statistically significant difference (P = 0.0006) between the means for person/minutes for phases 1 and 2 for turning and repositioning.

Discussion 

This 2-phase study investigated the impact of using a turning and repositioning system on the incidence of sacral pressure ulcers in 2 ICUs and the time and number of staff required to accomplish the task. In this study population, the incidence of sacral HAPUs decreased from 28% to 0% following implementation of the TAP system. The time for turning and repositioning patients decreased significantly, requiring fewer staff and less time overall. 

Regardless of the common, prevalent use of turning and repositioning as a factor in treating and preventing pressure ulcers, no randomized trials have been conducted that correlate the effects of turning and repositioning patients on the incidence or healing rates of pressure ulcers. Consequently, a direct conclusion cannot be made as to whether turning and repositioning patients directly impacts the incidence and healing of pressure ulcers. ² The results of this study indicate the use of a turn-and-assist device may have the potential to reduce sacral HAPUs and decrease the amount of time and personnel required to reposition patients. Although other risk factors for pressure ulcer development for critically ill patients were not studied or correlated to the data collected in this study, general patient characteristics were similar in the pre- and post-intervention groups. 

Anecdotal information from staff participants was not collected as a part of the study, but during phase 1 nursing staff repeatedly reported the difficulty in turning/repositioning critically ill patients based on a variety of factors including patient conditions (patient size, immobility, intubated/sedated, isolation with the need for PPE) and the work environment (lack of resources, not enough nursing/nursing assistant staff). In phase 2, the nurses reported the TAP allowed them to reposition patients easier, with fewer personnel. Nursing staff also noted use of the TAP device may have prevented patients from sliding down in the bed and maintained them in positions with the sacral area offloaded for longer periods of time than with standard care. The nursing staff on the 2 study units was enthusiastic about this product and insisted it be added to the available unit resources; the Chief Nursing Operator was encouraged to round on the units to see this product in use. 

Limitations

Because study findings are based on a small sample of patients in the ICU setting, this study is limited in terms of generalizability. The turn-and-assist device was implemented as part of a quality improvement project in a clinical environment served by many different caregivers, a factor that could influence consistency of care. Although the PIs worked to standardize data collection regarding the time and number of staff members required to turn and reposition patients, they were able to capture only a small portion of the work over the time of the study. The staff also may have modified their behaviors in the presence of the observers. In addition, the time frame and sample size may have limited the ability to determine the full effect of the product for nurses. Future stringent randomized controlled trials are indicated to study the effect of this type of product on improving outcomes for patients and making the work of patient care safer and more efficient. 

Conclusion

Prevention of HAPUs in the critical care patient population remains a challenge for nursing staff due to the high acuity and complex care requirements of these patients. To the authors’ knowledge, this is the first study documenting that a turn-and-assist device may reduce nursing staff time to reposition patients as well as the incidence of sacral HAPUs. 

Further research into comprehensive approaches for HAPU prevention in the critical care patient population is warranted. Although no data were collected on workman’s compensation injuries related to moving/repositioning patients, this would be a valuable topic for future investigation. 

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14. United States Department of Labor, Bureau of Labor Statistics, Nonfatal occupation injuries and illnesses requiring days away from work, press release 2009. Available at: www.bls.gov/news.release/osh2.nr0.htm. Accessed August 16, 2016. 

15. White E. The Elephant in the Room: Huge Rates of Nursing and Healthcare Worker Injury. Available at: www.nhnurses.org/Documents/Announcement-Flyers/Alert.aspx. Accessed August 16, 2016. 

16. National Database for Nursing Quality Indicators (NDNQI) (2015). Pressure Ulcer Survey Guide. Available at: https://members.nursingquality.org/NDNQIPressureUlcerTraining/Module3/De.... Accessed August 16, 2016.

17. European Pressure Ulcer Advisory Panel and National Pressure Ulcer Advisory Panel. Prevention and Treatment of Pressure Ulcers: Quick Reference Guide. Washington DC: National Pressure Ulcer Advisory Panel;2009.

18. McCloskey K. Ergonomics and patient handling. AAOHN J. 2007;55(11):451–462.

19. Capuano T, Bokovoy J, Halkins D, Hitchings K. Work flow analysis: eliminating non-value-added work. JONA. 2004;34(5):246–256.

20. Westbrook JI, Duffield C, Li L, Creswick NJ. How much time do nurses have for patients? A longitudinal study quantifying hospital nurses’ patterns of task time distribution and interactions with health professionals. BMC Health Serv Res. 2011;11:319. doi: 10.1186/1472-6963-11-319.

Potential Conflicts of Interest: Financial support was provided by Sage Products (Cary, IL), who provided products for use during this study.

Dr. Hall is a Wound Care Clinical Nurse Specialist; and Dr. Clark is Senior Director for Nursing Research and Evidence Based Practice, Carilion Clinic, Roanoke, VA. Please address correspondence to: Kimberly D. Hall, DNP, RN, GCNS-BC, CWCN-AP, Carilion Clinic, 1906 Belleview Avenue, Roanoke, VA 24014; email: kdhall2@carilionclinic.org.

Abstract

Infection plays a critical role in health care and impacts the cost of the treatment of diabetic foot ulcers (DFU). To examine the cost reduction associated with the multidisciplinary treatment of infected DFU (IDFU) by obtaining early (ie, within 48 hours of admission) microbiological culture results, a descriptive, longitudinal study was conducted.

Data were collected prospectively from patient medical charts of a cohort of 67 patients (mean age, 56.14 ± 12.3 years; mean duration of diabetes, 14.95 ± 8 years) with IDFU treated at a Mexican public health facility from January 1 to April 30, 2010. Information included demographic data (age, gender, marital status, time elapsed since first diagnosis of diabetes mellitus type 2 [DM2]), and the following clinical records: Wagner classification, bacterium type, antimicrobial resistance, length of hospital stay, and the antibiotic schedule utilized, as well as number and type of laboratory tests, medications, intravenous therapy, surgical and supportive treatment, type and number of specialists, and clinical outcome. Microcosting was used to calculate the unit cost of each medical treatment element. Using the Monte Carlo and Markov predictive simulation economical models, cost reduction associated with early identification of the specific microorganism through bacterial culture in IDFU was estimated. Based on the statistical results, differences between real and estimated costs when including early microbiological culture were identified and the number and type of most common species of infectious bacteria were detected. The total cost observed in the patient cohort was $502 438.04 USD, mean cost per patient was $7177.69 ± $5043.51 USD, and 72.75% of the total cost was associated with the hospital stay length. The cost of the entire treatment including antibiotics was $359 196.16 USD; based on the simulation of early microbiological culture, the model results showed cost could be reduced by 10% to 25% (in this study, the cost could be as low as $304 624.63 USD). The use of early microbiological cultures on IDFU to determine the appropriate antibiotic can reduce treatment costs by >30% if hospital stay is part of the consideration.

Diabetes mellitus type 2 (DM2) is one of the most common chronic diseases worldwide. North America and the Caribbean Region have the highest diabetes prevalence. According to the International Diabetes Federation (IDF),¹ 44.3 million persons between the ages of 20 and 79 years have been diagnosed with diabetes. Treatment of DM2 and its long-term complications are associated with high costs and represent a substantial economic burden for health systems in different countries, particularly for third-party payer health institutions. In North America and the Caribbean Region, the total health expenditure related to DM2 treatment was estimated to be $348 to $610 billion USD, solely for 2015; 14% of the total health budget in the region is spent on diabetes treatment and represents 51.7% of the world health care spending associated with diabetes.^1,2 

In 2015, DM2 affected 383 million persons worldwide. Estimations suggest 592 million individuals will be affected in 2040.¹  In Mexico, according to data provided by the National Health and Nutrition Survey³ in 2012, DM2 prevalence was 9%; this is a 1.25-times higher prevalence rate than the estimation for 2030 calculated by Wild.⁴ Data provided by the IDF¹  showed a prevalence in Mexico of 15.8% (age-adjusted) and 14.7% (raw). Specifically in 2012, DM2 prevalence adjusted by age in Mexico was 8.9% for 40- to 49-year-old patients, 19.2% for patients 50 to 59 years old, and 25.3% for 60- to 69-year-old patients. These data are similar to international reports, where the highest prevalence is observed in persons age 40 to 59 years.¹  These groups represent the economically active population of the country and exert a profound economic impact.¹ 

Diabetic foot ulcers (DFU) are an important long-term complication in patients with DM2. Epidemiological and economic statistics on infected DFU (IDFU) and amputations have been obtained from real-world data and through the use of theoretical mathematical models¹ that describe typical diabetic foot cases with clinical outcomes characterized by different complexity levels ranging from wound healing to transtibial amputation.⁵ Nearly all data on infected foot ulcers in diabetes are obtained from information of developed countries.^5,6 Studies with data deriving from developing countries are scarce. 

Symptoms associated with diabetic foot syndrome include loss of sensation and, when a trauma occurs, loss of capacity to feel pain in the lower limbs. This worsening sensation is a consequence of diabetic neuropathy.^7–12 According to epidemiological data,¹³ 15% of individuals with diabetes will undergo amputation, and 20% to 25% of these patients will be candidates for a second amputation. Prevention programs have been reported to decrease the need for amputation in 80% to 90% of cases.⁴ 

Specific guidelines¹⁴ and descriptive studies on microorganisms associated with IDFU^15,16 with respect to the management of diabetic foot infections describe treatment for wounds in diabetic foot injuries according to the absence or presence of infection and its severity. Consensus guidelines⁸ for treatment consider wound depth (involved tissues) and the presence of clinical data on infection (such as edema, erythema, rubor, heat) and vascular compromise to determine the specific treatment. IDFU must be treated with specific antibiotics according to microbiological cultures from the wound, and these must be provided after debridement to optimize microbiological diagnosis and antibiotic selection.¹⁴ 

For the initial treatment, the guidelines suggest empirical selection of an antibiotic that is active against Gram-positive bacteria. For geographic areas with a high prevalence of Gram-negative bacteria, double antibiotic coverage against Gram-positive and Gram-negative bacteria also is considered (extended-spectrum antibiotics drugs). When a microbiological culture is available, treatment must be modified according to culture results and antibiotic susceptibility under a more specific schedule. Because existing guidelines are based on a limited number of patients,¹⁴ it is difficult make decisions regarding cost-effective antibiotic therapy. 

Some investigators have analyzed the cost-effectiveness of different approaches to IDFU in hypothetical cohorts employing mathematic models (eg, Markov and Monte Carlo tools^17,18) that consider the probability of multiple complications and clinical outcomes according to the proposed treatments.^19,20 However, the theoretical models have not described the role of microbiological cultures in diminishing the hospital stay and costs. 

In view of this gap in the literature, the purpose of this study was to estimate the economic impact (cost reduction) of performing early (within 48 hours of admission) microbiological cultures in the treatment of IDFU by using the Markov and Monte Carlo predictive simulation economical models. 

Methods and Procedures 

The study was conducted in 2 parts. A prospective, descriptive, longitudinal study was performed to analyze real-world data from a group of patients with diabetes with infected foot ulcers; the known prevalence of microorganisms and registered treatment costs were described. In the second step, a hypothetical cohort with 100 iterations (case simulations) at different treatment stages was constructed through the Monte Carlo simulation, employing the data derived from the patients studied in the first phase (this information was utilized for the mathematical basis of the economical tool). The simulations provided predictions of the economic impact of obtaining early microbiological cultures of infected ulcers in order to make an informed decision about a specific antibiotic treatment. 

The study was approved by the CLIEIS No. 1306 (Comité Local de Investigación y Ética en Investigación en Salud: Local Committee of Research and Ethics in Health Research) at the Institute Mexicano del Seguro Social (IMSS) Jalisco. Based on the observational nature of the investigation, the Committee authorized the use of signed informed consent according to the guidelines in the regulation of the General Health Law responsible for health research of studies without risk in Mexico. 

In this study, data were obtained from the medical charts of patients with diabetes with IDFU who were seen at the IMSS Emergency Room (ER) of a second-level facility from January 1 to April 30, 2010. The patients were followed during hospital treatment for the IDFU. Patients with a diagnosis of cancer, hepatic cirrhosis, and/or rheumatic-orthopedic diseases that could impact their walking ability and patients with pressure-associated ulcers or DFU that appeared during their hospital stay were excluded. 

Cost per patient was calculated based on the identification of the antibiotic schedule, the bacterium, and antimicrobial resistance from the patients’ charts. Length of hospital stay (days); number and type of laboratory tests, medications, and intravenous (IV) fluids; costs for surgical and supportive treatment; specialists (type and number of); and clinical outcomes also were abstracted, as well as demographic information and the patient’s history (age, gender, marital status, and time elapsed since first DM2 diagnosis). The Wagner classification of foot ulcers and microbiological culture also were obtained. The cost of each component of the medical treatment was obtained from the IMSS website IMSS compró²¹ (an institutional website that displays for public opinion the cost of drugs, medical technology, wound care material, and other supplies purchased by IMSS at each hospital).

Data collection. Data were collected from the patient’s chart by an emergency medicine physician and subsequently entered into an electronic database. To preserve anonymity, patients were identified by means of a code and their social security number.

Statistical analysis. Using the data collected by Gutiérrez et al,³ the sample size of this study was calculated with a 95% confidence interval (95% CI) and 80% potency. For quantitative data, means, standard deviations (SD), medians, ranks, and intervals were calculated. For qualitative data, percentages and proportions were utilized. All data were processed in SPSS version 16 and Excel 2010 statistical software (SPSS Inc, Chicago, IL). 

In parallel, a descriptive economic analysis using microcosting was performed to evaluate the partial cost of medical treatment by employing the third-party-payer perspective (ie, the IMSS, for this particular study). The time horizon defined was 30 days. Discount rates were not applied. 

Microcosting comprises a cost estimation method that involves the “direct enumeration and costing out of every input consumed in the treatment of a particular patient.”²¹ It employs the aggregation level, which allows knowing the lower-level estimated cost associated with the various treatment elements for a given level within the patient’s treatment. Indirect costs such as buildings, equipment, and maintenance were not considered. In order to estimate unit costs, the resource pattern utilized was identified according to microorganism type and was registered in the medical record of each patient; a monetary value was assigned later. The unit cost was identified for each resource. For health services (consultation, surgeries, hospitalization), cost information was obtained from the Diario Oficial de la Federación (DOF) website²² and the medication cost was obtained from the IMSS website under IMSS compró.²³ The economic expenditure for each resource was calculated as the product of the unit cost multiplied by the number of units used. The monetary value for Mexican pesos was obtained in 2009 and converted into US dollars (USD) with an exchange rate of $12.75 Mexican pesos per $1 USD. 

The following cost-related information was calculated: total cost per patient, total cost for the group of patients with diabetes, and mean cost for each patient.

Markov modeling. This mathematical model is employed in decision analysis to evaluate potential outcomes of a disease process, which are defined as specific health states and transitions that are modeled iteratively. In standard-decision tree analysis, a patient moves through states in a Markov process. Some states cannot be left once entered (the so-called “absorbing states” or natural history of the disease), including death.^24-26 In IDFU, specific issues were considered with the following elements in the process: DM2 without complications; DM2+DFU; DM2+DFU+infection; DM2+DFU+infection+1st amputation; and DM2+DFU+1st amputation+2nd amputation (see Figure 1 and Tables 1 and 2), to estimate (calculated values) the proportion of persons affected by each condition per specific period (eg, proportion of patients with DM2+DFU in the first period [0.25], which corresponds to 25%; while in the second period, 0.297 corresponds to 29.7%). These proportions are utilized to construct the probabilistic mathematical model. 

Monte Carlo modeling. The Monte Carlo method is a nondeterministic statistical method for obtaining a numerical solution for a problem too complicated to be solved analytically. This method solves a problem by generating a set of random or pseudorandom numbers within the domain of the variables under study. The corresponding absolute error decreases as the number of Monte Carlo evaluations increases, using the central limit theorem as a basis.²⁷ The mathematical model allows for containing estimated numeric results through a design of specific clinical sets.²⁸

The Monte Carlo predictive model was used in this study to find the behavior (through extrapolating the data of a specific clinical set) of the phenomenon denoted infected diabetic foot ulcer. Differences between real cost and estimated cost of procedures including early microbiological culture in each patient (eg, surgical procedures, wound healing, culture specimens) were considered based on the statistical results to optimize resources for the patient and for the third-party payer (IMSS) (see Figure 2 and Table 3). The Monte Carlo simulation was employed to estimate the cost reduction associated with early identification of the specific microorganism in the IDFU at the beginning of treatment. Data for the model included species, type of bacterium according to Gram stain, number of infecting microorganisms, and antibiotic sensitivity through bacterial culture.

The information analyzed included the bacterium type identified through microbiological culture; number of microorganisms identified in each microbiological culture and their susceptibility to medications (1–3 different bacteria were identified); unit cost for each medication (purchase of ordinary [eg, public tendering — ie, an administrative procedure where governments select the person or vendor from whom to buy different kind of supplies through public contest; and centralized procurement coordinated through the Acquisitions Department] and extraordinary [eg, items purchased from suppliers without public tendering such as antibiotics) used in the treatment recommended by the physician; length of ER stay (days), mindful of guidelines that have established a maximum time in the ER as 24 hours, while every extra hour generates an increase in financial expenditures per patient; length of hospital stay (days); and cost per day for total hospital stay at a secondary-level hospital. 

The structure of the Monte Carlo model involved medications (antimicrobial spectrum: active against Gram-positive bacteria, Gram-negative bacteria, or anaerobic bacteria); specific antibiotic; cost of each antibiotic; cost of each group of antibiotics; and bacteria (specific bacterium identified through microbiological culture, along with bacterial group [Gram-positive, Gram-negative, anaerobic bacteria, fungus]). 

As part of the Monte Carlo model, the following factors were considered: days of hospital stay (total or overnight and in the ER); hospital-associated costs; type of bacterium or group of bacteria (see Table 4); specific antibiotic or antibiotic groups, and the cost of each antibiotic in ordinary and extraordinary purchasing (see Table 5). One hundred (100) Monte Carlo iterations (simulations) were performed in order to observe the predictive model behavior. Final treatment cost and total cost with the proposed model were ultimately analyzed. 

Results

Data were obtained from the medical charts of 71 patients with IDFU; 4 clinical charts had incomplete data on the microbiological culture and were excluded from pseudorandom iterations, leaving 67 patients (mean age, 56.14 ± 12.3 years; mean time elapsed since initial diagnosis, 14.95 ± 8 years) considered for designing the iterations (simulations) utilized in the Monte Carlo model.

Patients were enrolled between January and April and were followed during 16 months. Infected ulcers in the diabetic foot were found to be more common in patients with 11–20 years of DM2 evolution. Men at the economically productive age (16–65 years old) were more affected than women; the educational level was basic (1–9 academic years). The most common concomitant chronic disease was hypertension (53.6%). Approximately one quarter (24.6%) of the patients with diabetes had undergone a previous lower-limb amputation (see Table 6). 

Average ER length-of-stay was 1.4 ± 0.58 days; hospital stay when treated by other specialists (General Surgery, Angiology, Orthopedics, Traumatology, and Internal Medicine) was 14.7 ± 9.7 days. 

Microcosting analysis results. Total treatment costs for the sample were $502 438.04 USD, mean cost per patient was $7177.69 ± $5043.51 USD, median cost was $6422.99 USD, 25th percentile was $3502.93 USD, 75th percentile was $9,298.33 USD), and 72.75% ($365 527.45 USD) of the total cost was associated with the hospital stay. 

Furthermore, 10.6% ($53 240.86 USD) of expenditure during treatment was directed to wound healing care (eg, debridement procedures, wound healing, lavage), 9.98% ($50 132.94 USD) to surgical procedures, and 1.87% ($9389.27 USD) to antidiabetic drugs and concomitant chronic diseases. With regard to laboratory tests and treatment, 1.79% ($9008.47 USD) was attributed to clinical chemistry tests, 1% each to antibiotics ($5405.98 USD) and imaging studies ($5000.08 USD), 0.66% ($3309.88 USD) to acute phase reactants, 0.19% ($965.65 USD) to microbiological cultures, and the lowest percentage was attributed to IV fluids (see Figure 3). 

The costs were determined according to the resource utilization pattern, which comprised the use of medications, wound healing material, hospital stay, and debridement procedures, modified for individual patients. Resource utilization was determined by the multidisciplinary treatment employed (identification, diagnosis, and treatment) according to the Wagner classification.¹⁴ Results from analyzed cases were included as Wagner grade 3 (30 cases [43.5%]) and Wagner grade 4 (22 [31.9%]). Patients in both groups required supracondylar amputation (13, 19%) or transmetatarsal amputation (20, 14%) (see Table 7). Microbiological culture was not performed in 2 patients; 1 of the remaining patients had a negative bacterial culture. The bacteria most frequently identified were Escherichia coli (20.4%) and Enterococcus faecalis (19.4%) (see Table 4). The most used antibiotic combination employed was ciprofloxacin/clindamycin. 

Bacterial antibiotic susceptibility.

Gram-negative bacteria. In bacterial cultures positive for E. coli, the greatest proportion showed susceptibility to imipenem, amikacin, meropenem, cefotetan, and piperacillin/tazobactam; intermediate susceptibility was demonstrated toward quinolones, and there was resistance to ampicillin/sulbactam and ampicillin. Escherichia faecalis exhibited susceptibility to penicillin, vancomycin, linezolid, and gentamicin, with intermediate susceptibility to ciprofloxacin and resistance to tetracycline and synercid. Proteus mirabilis demonstrated susceptibility to amikacin, cefotetan, and carbapenem and was resistant to quinolones, while Morganella morganii was susceptible to amikacin, gentamicin, and meropenem, and resistant to ciprofloxacin, cefuroxime, cefotetan, moxifloxacin, and piperacillin (see Table 4).

Gram-positive bacteria. Staphylococcus haemolyticus was susceptible to linezolid, synercid, rifampicin, vancomycin, and chloramphenicol and resistant to clindamycin, gentamicin, penicillin, and quinolones. S. epidermidis exhibited susceptibility to linezolid, synercid, vancomycin, and rifampicin and resistance to ciprofloxacin, clindamycin, oxacillin, and amoxicillin. S. aureus displayed susceptibility to cefazolin, imipenem, piperacillin/tazobactam, rifampicin, vancomycin, oxacillin, and amoxicillin and resistance to ampicillin and penicillin. Methicillin-resistant S. aureus was susceptible to tetracycline, linezolid, trimethoprim/sulfamethoxazole, vancomycin, and synercid and resistant to cefazolin, quinolones, penicillin, and amoxicillin (see Table 4). 

Monte Carlo modeling results. This study comprised 67 patients. For each patient, the number of days spent in the ER and in their hospital room was reported. According to the data collected, time in the ER ranged from 0 to 3 days, and time in the hospital room ranged from 0 to 15 days. Average costs per day in the ER and the hospital room were $1001.00 USD and $5,684.00 USD, respectively. 

To implement the Monte Carlo methodology, the number of days the patient could spend in the ER and in the hospital room was randomly selected. Utilizing the average cost per day, the cost of hospitalization for 1 patient was calculated and then repeated 67 times to calculate the total cost for hospitalization. This procedure was performed 100 times, and the corresponding results are illustrated in Figure 4.

The antibiotic cost analysis showed if the physician takes a secretion sample from the IDFU within the first 48 hours of the patient’s admission to the ER and begins empirical antibiotic treatment but modifies the criteria according to the microbiological results from the culture, costs will be reduced (through antibiotic expenditure) by 9% to 15% (see Figure 4); the cost reduction could be as high as 20% to 32% when associated with a reduced number of hospital days, with a 10% to 25% total reduction in costs related with IDFU receiving multidisciplinary treatment. 

Discussion

IDFU are 1 of the most common late-stage complications of DM2²⁹ and inflict a substantial economic burden on society, particularly in developing countries such as Mexico, as well as on worldwide health systems.^2,5 This condition places diabetic foot infection as a public health problem in the microbiological, clinical, epidemiological, and economic context; the American Diabetes Association (ADA)³⁰ concluded diabetic foot complications represent 12% to 15% of the health care budget in developed countries and 40% in developing countries. Therefore, it is important to evaluate economic impact with a health care model that includes early microbiological culture in the care process of IDFU. 

Treatment for DM2 in late-stage complications such as vision loss or blindness, kidney damage or failure, nerve pain and damage, heart and blood vessel disease, high blood pressure, dental problems, hand problems, and foot problems represents an increase from 50% to 700% in the total medical care cost in developed countries, according to data provided by the ADA.^1,28–30 IDFU have a calculated incidence of 7% and are the cause of 80% to 95% of nontraumatic, lower-limb amputations throughout the world. In their descriptive study (N = 80), Gönen et al³³ found higher cost associated with lengthy hospital stay and amputation, similar to the situation observed by the current study, in which 24.6% of patients underwent lower-limb amputation. 

In a clinical setting, providing appropriate antibiotic treatment requires knowing the sensitivity associated with a specific antibiotic through a microbiological culture with an antibiogram for wound secretions with clinical infection data.¹⁴ For public health care systems in medical units of developing countries, it is important to follow the specific clinical guidelines; this situation directly affects hospital length-of-stay and treatment-response time,^14,34 subsequently affecting the economic burden in the clinical care of these patients with diabetes. Clinical guidelines could help clinicians make the best cost-effective decisions concerning antibiotic treatment according to the type of bacterium and its antibiotic sensitivity.^14,34

Employing guidelines for the diagnosis and treatment of patients with diabetes with DFU is associated with the proper use of economic resources and improved patient outcomes. In their descriptive study, Sotto et al³⁵ demonstrated implementation of guidelines was associated with a savings of $20 046 USD related to a reduced microbiology laboratory workload and of $147 536 USD in a reduction in the prescription of extended-spectrum antibiotic drugs. 

Conversely, bias with regard to the diagnosis and treatment guidelines of IDFU could give rise to overdiagnosis or underdiagnosis. This scenario is associated with inadequate use of the antibacterial medication, as well as with potential development of bacterial resistance and presence of adverse events related to medication use and a high amputation rate.²⁹ Each of these situations causes an increase in the length of the hospital stay and the unnecessary waste of financial supplies in developed and developing countries.³⁵ 

International best practice guidelines for DFU management, cost-effectiveness analysis, and direct cost-descriptive studies^28,36,37 report failure of antibiotic treatment associated with a high risk of developing an infection in chronic foot ulcers, as well as a high risk of a nontraumatic amputation, with the associated cost of surgery, prolonged hospital stay, postoperative care, prosthesis use, and orthopedic rehabilitation. These costs are financed by secondary-level hospitals in the Mexican Health-Care System. 

In late-stage complications of DM2, an IDFU is associated with a high social cost. The burden is the result of health care costs and work disability associated with amputations during treatment, which reduce productivity for countries and their governments, impacting expenditures related to pensions and early retirement.³⁸ In the current study, 74.6% of patients were <65 years of age (65 years of age is considered the official retirement age, and younger patients were considered economically active), all with a high risk of nontraumatic, lower-limb amputation.

According to 2007 US statistics,³⁰ health care expenditures for the treatment of DM2 were 2.3 times higher than in patients without diabetes. Similarly, expenditure related with absenteeism from work in this type of patient represented $2.6 million USD. DM2-associated disability exerted an influence on unemployment and decreased productivity. In the US, early death was related with a loss of $26.9 million USD, which reflects a loss of $116 million USD for direct costs. Of these, 33% was caused directly by IDFU.³⁰ 

A group of Swiss and French investigators³⁵ evaluated the economic impact derived from the use of treatment guidelines for the infected diabetic foot. Between 2003 and 2007, these researchers studied the potential effects of bacteriological data (number of microbiologic cultures, number of isolated microorganisms, the frequency of multiresistant bacteria, colonizing flora), costs associated with antibiotic use, and the workload for the microbiology laboratory. The microbiology results and health care costs comprised the most important outcomes in the investigation. The investigators also documented a reduction in the median of bacterial species for each sample (from 4 to 1) was associated with a savings of $20 046 USD derived from a workload reduction for the microbiology laboratory, and $147 536 USD were associated with a reduction in the prescription of unnecessary broad-spectrum antibiotics. Similarly, the current study also found a relationship among use of treatment guidelines at treatment initiation, re-collection of microbiological culture samples, and economic resource savings with an enhanced global quality-of-treatment in IDFU. 

Current treatment and its cost-effectiveness have been analyzed in other developing countries. In Turkey, investigators identified an increase in the cost of infected diabetic foot treatments was related to chronic treatments and surgical procedures, especially if the latter were associated with osteomyelitis and subsequent amputation.³¹ These conditions were associated with therapeutic failure in early microbiological diagnosis and with inefficient use of antibiotics. The investigation also found having an infected diabetic foot was associated with psychosocial trauma and work loss. For third-party payers in Turkey, an increased number of hospital treatments increased total treatment cost. The current study resulted in similar observations: increased percentage of treatment expenditure was associated with prolonged hospital stay. 

With regard to the microbiological cultures, it is important to consider the early sampling at hospital admission (ER) before the use of empirical antibiotic treatment. As has been observed through the current Monte Carlo modeling, costs to the health system could be reduced because of less antibiotic use and consequently fewer hospital days would be required. This situation underscores the need for attention to appropriate antibiotic use to enhance the planning of resource utilization.

Limitation

Observations, disease behavior, or processes are subject to unpredictability. Disease models are often difficult to capture and reproduce, the most important disadvantage being that their probability functions usually cannot be calculated explicitly. Statistical models provide an option to test theories. However, although probabilistic methods such as Monte Carlo modeling attempt to reproduce the disease behavior, in real-life clinic settings, many confounder variables can modify the result. With a specific condition such as an infected ulcer in a diabetic foot, these variable situations usually are related to the human factor in the process of treating a patient. Therefore, model results must be considered carefully. 

Conclusion

Infected diabetic foot treatment requires the application of new operational and process-engineering strategies to enhance treatment outcomes and the cost-effective use of resources³⁹; early microbiological culture (within 48 hours of admittance to a health care facility) can be considered an important operational strategy. The multidisciplinary treatment of infected ulcers in the diabetic foot involves the evaluation and establishment of infection severity as a first step to the choice of a specific treatment. Using mathematical models, investigators analyzed the role of microbiological cultures in reducing hospital stay and costs. Early microbiological culture and subsequent antibiotic selection were found to be ancillary factors for reducing hospital stay, antibiotic expenditure, and amputation rates, reducing treatment costs by >30% and enhancing the patient’s outcome. The current study did not consider patient outcomes such as satisfaction or health-related quality of life; these are issues that warrant future study. 

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20. Habacher W, Rakovac I, Görzer E, et al. A model to analyse costs and benefit of intensified diabetic foot care in Austria. J Eval Clin Pract. 2007;13(6):906–912.

21. Xu X, Grossetta NHK, Ruger JP.  Micro-costing studies in the health and medical literature: protocol for a systematic review. Syst Rev. 2014;21(3):47. doi: 10.1186/2046-4053-3-47.

22. Diario Oficial de la Federación (DOF). Available at: www.portalfiscal.com.mx/pagina/principal/transferencias%20dof/varios/201.... Accessed March 4, 2014.

23. IMSS Compró. Available at: http://compras.imss.gob.mx/?P=imsscompro. Accessed March 4, 2014.

24. Soares MO, Canto e Castro L. Continuous time simulation and discretized models for cost-effectiveness analysis. PharmacoEconomics. 2012;30:1101.OJO doi:10.2165/11599380-000000000-00000.

25. Soares MO, Canto e Castro L. Simulation or cohort models? Continuous time simulation and discretized Markov models to estimate cost-effectiveness. CHE Research Paper 56. Centre for Health Economics. Alcuin College, University of York, UK;2010.

26. Mar J, Antoñanzas F, Pradas R, Arrospide A. (Probabilistic Markov models in economic evaluation of health technologies: a practical guide). [Article in Spanish] Gac Sanit. 2010;24(3):209–214. doi: 10.1016/j.gaceta.2010.02.006. 

27. Weisstein EW. Monte Carlo Method. Available at:. http://mathworld.wolfram.com/MonteCarloMethod.html. Accessed August 23, 2016. 

28. Hartig F, Calabrese JM, Reineking B, Wiegand T, Huth A. Statistical inference for stochastic simulation models — theory and application. Ecol Lett. 2011;14(8):816–827. doi: 10.1111/j.1461-0248.2011.01640.x. 

29. International Best Practice Guidelines: Wound Management in Diabetic Foot Ulcers. Wounds Int. 2013. Available at: www.woundsinternational.com. Accessed August 23, 2016.

30. American Diabetes Association. Economic costs of diabetes in the U.S. in 2007. Diabetes Care. 2008;31(3):596–615. doi: 10.2337/dc08-9017.

31. Ding D, Lawson KD, Kolbe-Alexander TL, et al; and Lancet Physical Activity Series 2 Executive Committee. The economic burden of physical inactivity: a global analysis of major non-communicable diseases. Lancet. 2016:S0140-6736(16)30383-X. doi: 10.1016/S0140-6736(16)30383-X. 

32. Sancho-Mestre C, Vivas-Consuelo D, Alvis-Estrada L, Romero M, Usó-Talamantes R, Caballer-Tarazona V. Pharmaceutical cost and multimorbidity with type 2 diabetes mellitus using electronic health record data. BMC Health Serv Res. 2016;16(1):394. doi: 10.1186/s12913-016-1649-2.

33. Gönen MS, Çakır M, Gönülalan G, et al. The problems and cost-effectiveness analysis of diabetic foot infections. Turk JEM. 2012;16:10–13.

34. NICE Clinical Guidelines, No. 119. Diabetic Foot Problems: Inpatient Management of Diabetic Foot Problems. Centre for Clinical Practice at NICE (UK). London, UK: National Institute for Health and Clinical Excellence (UK);2011.

35. Sotto A, Richard JL, Combescure C, et al. Beneficial effects of implementing guidelines on microbiology and costs of infected diabetic foot ulcers. Diabetologia. 2010;53(10):2249–2255.

36. Kantor J, Margolis DJ. Treatment options for diabetic neuropathic foot ulcers: a cost-effectiveness analysis. Dermatol Surg. 2001;27:347–351.

37. Alzarani HA. The direct cost of diabetic foot management in some of private hospitals in Jeddah, Saudi Arabia. Int J Diabetes Dev Countries. 2013;33(1):34–39.

38. Boulton AJM, Vileikyte L, Ragnarson Tenvall G, et al. The global burden of diabetic foot infections. Lancet. 2005;366:1719–1724.

39. Tallis A, Motley TA, Wunderlich RP, Dickerson JE Jr, Waycaster C, Slade HB; the Collagenase Diabetic Foot Ulcer Study Group. Clinical and economic assessment of diabetic foot ulcer debridement with collagenase: results of a randomized controlled study. Clin Ther. 2013;35(11):1805–1820. doi: 10.1016/j.clinthera.2013.09.013.

Dr. Balderas-Pena is a titular researcher, Unidad de Investigación Médica en Epidemiología Clínica (UIMEC) of Unidad Médica de Alta Especialidad Hospital de Especialidades Centro Médico Nacional de Occidente (UMAE HE CMNO), Instituto Mexicano del Seguro Social (IMSS), Guadalajara, Jalisco, México. Dr. Sat-Munoz is an associate researcher, UMAE HE CMNO, IMSS; and titular research professor, Departamento de Morfología, Centro Universitario de Ciencias de la Salud, UdG. Ms. Ramírez-Conchas is a research assistant, Unidad de Investigación Social, Epidemiológica y en Servicios de Salud, Delegación Jalisco, IMSS. Mr. Alvarado-Iñiguez is a graduate of and Dr. Garcia de Alba Garciais Head, Unidad de Investigación Social, Epidemiológica y en Servicios de Salud, Delegación Jalisco, Instituto Mexicano del Seguro Social. Mr. Cruz-Corona is a research fellow, UIMEC, UMAE HE CMNO, IMSS. Mr. Chávez-Hurtadois is Asignature Professor, MBA Program, Centro Universitario de Ciencias Económico Administrativas (CUCEA), UdG. Mr. Chagollán-Ramírez is a titular professor, MBA Program, CUCEA, UdG. Please address correspondence to: Luz-Ma-Adriana Balderas-Peña, MD, PhD, MBA, Research Division, UIMEC, UMAE HE CMNO, IMSS, Belisario Domínguez #1000, Colonia Independencia, Guadalajara, Jalisco CP 44340 Mexico; email: lmabp@yahoo.com.mx.  

Abstract

Research regarding the reliability of the Braden Scale and nurses’ perspectives on the instrument for predicting pressure ulcer (PU) risk in acute care settings is limited. A mixed-methods study was conducted in a tertiary acute care facility to examine interrater reliability (IRR) of the Braden Scale and its subscales, and a qualitative survey using semi-structured interviews was conducted among nurses caring for patients in acute care units to gain nurse perspective regarding scale usability.

Data were extracted from a previous retrospective, randomized, controlled trial involving adult patients with compromised mobility receiving care in a tertiary acute care hospital in Canada. One-way, intraclass correlation coefficients (ICCs) were calculated on item and total scores, and kappa statistics were used to determine reliability of categorizing patients on their risk. Interview results were categorized by common themes. Reliability was assessed on 64 patients, where nurses and research staff independently assessed enrolled participants at baseline and after 72 hours using the Braden Scale as it appeared on an electronic medical record. IRR for the total score was high (ICC = 0.807). The friction and shear item had the lowest reliability (ICC = 0.266). Reliability of categorizing patients’ level of risk had moderate agreement (κ = 0.408). Three (3) major and 12 subthemes emerged from the 14 nurse interviews; nurses were aware of the scale’s purpose but were uncertain of its effectiveness, some items were difficult to rate, and questions were raised as to whether using the scale enhanced patient care. Aspects identified by nurses to enhance usability included: 1) changes to the electronic version (incorporating the scale into daily assessment documents with readily available item descriptions), 2) additional training, and 3) easily available resource material to improve reliability and usability of scale. These findings need to be considered when using the Braden Scale in clinical practice. Further study of the value of the total Braden Scale and its subscales is warranted.

Pressure ulcers (PUs) are a common health problem that has a significant impact on morbidity, mortality, and health care utilization and cost.^1-4 As shown in cross-sectional surveys and reliability studies,⁵ factors such as limited mobility, malnutrition, increasing age, and excessive moisture may contribute to PU development. A survey⁴ and a reliability study⁶ suggested that identifying patients at increased risk for PUs can lead to targeted interventions to prevent their occurrence; a systematic review⁷ has shown prevention rather than treatment offers greater hope of a cost-effective way to deal with PUs. 

The Braden Scale is a widely used instrument for predicting PU risk.^8,9 It consists of 6 items (sensory perception, moisture, activity, mobility, nutrition, and friction and shear) that evaluate factors contributing to the development of PUs.^5,8 Descriptions are provided for each item’s subscore category; items are ranked on a scale of 1 to 4 (from greatest to lowest risk), with the exception of the friction and shear item where the scale is 1 to 3.⁸ The individual subscores then are summed to give a total score that corresponds to the patient’s level of risk for PUs. Although the original Braden Scale has defined risk ranges for no risk (19–23), mild (15–18), moderate (13–14), high (10–12), and very high risk (<9), a variety of different categories and score ranges have been used and tested in clinical practice to define risk.^10-17 Risk ranges may differ in clinical practice depending on the facility using the Braden scale. A retrospective quantitative analysis¹⁰ was conducted of Braden scores of patients (N = 2625) admitted in an acute care facility to compare a modified 3-group risk classification with the traditional 5-group classification. The investigators categorized hospitalized patients as being at mild (total Braden score ≥17), moderate (12–16), and high risk (≤11) for developing a PU and found no significant differences between the 3-group and 5-group risk classifications.

As noted by Kottner and Dassen¹⁸ in their literature review, several studies have reported on the validity of the Braden Scale; however, research regarding the interrater reliability (IRR) in terms of intraclass correlation coefficients (ICC) is limited and only a few studies evaluated the reliability of item subscores. This review examined the methods (using Pearson’s product-moment correlation, Cohen’s kappa, overall percentage of agreement) previously used to analyze the IRR of items and total Braden scores and found inconsistencies between the values calculated. Kottner and Dassen recommended using ICC in future studies on IRR of Braden scores. Satisfactory IRR, defined as the concordance of ratings between multiple raters for the same patient, is essential for ensuring the reproducibility of ratings.^18,19 Although the IRR of the Braden Scale has been examined in IRR studies in long-term care⁵ (N = 152), home care²⁰ (N = 691), and intensive care unit²¹ (N = 45) settings, its reliability on general medical and surgical units has not been evaluated. This is an area needing further study, because PUs are common among hospitalized patients.²¹ An observational study²¹ noted IRR research is especially lacking in assessing the scoring of individual items. 

Cross-sectional survey studies in Sweden (N = 85),²² Belgium (N = 553),²³ and Ethiopia (N = 248)²⁴ assessed nurses’ knowledge on PU prevention strategies and found general knowledge was inadequate. A cross-sectional (N =553) study by Beeckman et al²³ suggested nurse attitude toward PU prevention influences the implementation of preventive measures. The situation in Canadian hospitals is unknown because research about nurse perspective and particularly their attitude toward the Braden scale is lacking. A better understanding of nurse perspective regarding the Braden Scale could lead to greater use of the instrument in the implementation of PU prevention strategies. 

The overall aims of this study were to examine the IRR of the item and total scores of the Braden scale in a real-life clinical setting and to determine the perspectives of nurses toward the Braden scale and its use in an acute care setting. 

Methods

IRR. 

Study setting and population. This report uses data from a substudy of a randomized, controlled trial (RCT) (see NCT02325388 at ClinicalTrials.gov for more details) on the efficacy of continuous pressure imaging technology at reducing interface pressure of patients who are at risk of PUs in an acute hospital setting. The RCT was conducted in a tertiary care teaching hospital in Calgary, Alberta, Canada. Participants received care from internal medicine, neurology, spinal injury, or intensive care units and were recruited based on the parent RCT²⁵: participants were either gender, at least 18 years of age, and required assistance or were completely dependent for bed mobility on the “Bed” components in the de Morton Mobility Index, a 15 item unidimensional measure of mobility.²⁶ Participants who voluntarily withdrew from the study, were transferred, were discharged or died within 72 hours of enrollment, or lacked Braden scoring during the study period were excluded from this report. The Conjoint Health Research Ethics Board at the University of Calgary approved the study (REB13-0794). 

The substudy served as an independent examination of the use of the Braden Scale in clinical practice. Braden scores for each enrolled participant were completed for the RCT by 1 of 2 research staff members (one of which was a research nurse) at baseline and after 72 hours. Other members of the research team (N = 13), which consisted of wound care clinicians and researchers, trained the research staff in the administration of the Braden Scale. Unit nurses who worked on internal medicine, neurology, spinal injury, and intensive care units during the study and used the Braden Scale regularly for patient assessments independently determined Braden scores per institutional policy requirement to assess risk for all patients on the units. Because the Braden Scale was used on a regular basis by nurses as a required assessment, and because the study goal was to examine its reliability in a real-life clinical setting, additional training on its administration was not provided by the facility’s research team before the start of this substudy. Unit nurses were trained by the unit nurse educators during their new staff orientation, which was separate from, and not associated with, the RCT. 

The Braden Scale used by nursing staff to chart their assessments was part of the institutional electronic medical record (EMR) system used at this facility. This version included the 6 Braden Scale items along with the rating options identified by number and heading for scores; it did not include full descriptions for each item or scoring options. A printed version of the scale included the 6 items and rating options and full descriptions of each. Both the EMR and paper resources of the Braden Scale had been instituted on the units well before the start of the study and were not initiated by the research team. Because the authors’ main objective was to examine scale usability in a real-life clinical setting as it was being used before the RCT, any differences between the EMR and the paper resources of the scale were not reconciled before the start of the substudy. 

Data collection, sample size determination, and statistical analysis. Data were retrospectively extracted from the EMR of participants enrolled between December 2014 and May 2015. The data collected included participant age, gender, and Charlson comorbidity index score^.27 The Charlson comorbidity index is a “weighted index that takes into account the number and the seriousness of comorbid disease (that is used to) predict risk of death from comorbid disease.”²⁷ A high index predicts an increased cumulative mortality associated to comorbid disease. Braden scores (item and overall) recorded by the research staff and unit nurses on the same participants were collected. The Braden ratings recorded by unit nurses closest to these baseline and 72-hour assessments were used for comparisons in this substudy. All pairs of comparisons were completed for scores done within 1 to 2 days of each other. This led to a total of 2 comparisons (baseline and 72-hour assessment) for each participant. If a comparison was not completed within this time frame, it was not included in the analysis. Braden scores recorded by the research staff were stored on a password-protected electronic database (REDCap, Research Electronic Data Capture) that was separate from the EMR the nurses used for charting. The presence of PUs also was assessed clinically by the research team during a head-to-toe skin assessment and stored on the REDCap electronic database. 

The study population consisted of 93 consecutive participants, and a total of 103 comparisons were made. ICC (1, k) (one-way random model, average measures) and kappa statistics were calculated using IBM SPSS software, version 22 (IBM, Amonk, NY) to determine the IRR of the Braden ratings. Because the Braden Scale is a unique instrument with continuous numerical scores that also can be categorized into risk categories, both calculations provide insight on the reliability of the scale. The ICC is best calculated by treating the scores as continuous variables, while kappa estimates treat the scores as categorical variables.^28,29 ICC was used to determine the IRR for the item and total scores, where each comparison was analyzed as a single independent entry for the given assessment time point (baseline or 72 hours). Kappa statistics were used to determine IRR for categorizing patients being at risk for a PU. Individual total Braden scores assessed at baseline or 72 hours were first categorized using risk ranges before being analyzed using kappa statistics. The 3 risk categories used for kappa testing were mild (total Braden score ≥17), moderate (12–16), and high risk (≤11), which was reflective of the risk ranges used at this facility.¹⁰ This report focuses on ICC calculations because they account for the degree of disagreement for IRR estimates and provide a better representation of the overall IRR for the Braden Scale.^18,29 ICC compares the variability of different ratings of the same patient to the total variation of all ratings of all patients.¹⁸                                                                              However, the kappa values from this study could lay the groundwork for future comparisons.¹⁸ ICC and kappa values were interpreted separately and not compared to each other because the calculation methods differed.^18,29 

Nurse perspectives on the Braden Scale. 

Participants. Volunteer male and female registered nurses (RNs) who worked on the internal medicine, spinal injury, and intensive care units during the study and used the Braden Scale participated in the interviews. 

Interviews. Participants were interviewed one-on-one in a quiet conference room on their patient care unit. These interviews were conducted by a research assistant who was not involved in the quantitative data collection in June 2015. The identity of participants was protected by an impartial interviewer interested in their opinions and experiences. The participants had no previous contact with the interviewer before the interviews. All participants gave written informed consent and were offered the opportunity to contact the interviewer after the interviews to add to their answers or to ask questions regarding the study. The interviews followed a semi-structured format that explored the participants’ understanding and knowledge of the Braden Scale and their views on the significance, effectiveness, and usability of the tool guide (see Table 1). The interviews lasted 15 to 20 minutes and were held during the nurses’ break times. Interviews were audiorecorded with field notes made after each interview. The interviewer transcribed the recordings verbatim. Participants were recruited and interviewed until the interviewer was satisfied each unit was well represented and that data saturation was reached. Field notes and transcripts were referred to and used in the analysis to assist in the interpretation of the data. 

Qualitative data analysis. Qualitative data obtained from interview field notes and transcripts were analyzed thematically. Each transcript was analyzed line-by-line for meaningful themes common among all interviews. The interviewer independently coded 14 interview transcripts using NVivo Software Version 10, 2012 (QSL International Pty Ltd, Burlington, MA) to generate the initial set of themes and subthemes, which were later discussed with another research team member until consensus was reached to form the final set of themes. Participants did not contribute to data analysis and interpretation. 

Results

Quantitative results. 

Sample. The initial sample size of 93 participants was reduced to 64 following 29 exclusions due to voluntarily withdrawal from the study (1), unit transfers (3), death within 72 hours of enrollment (5), or not having Braden score determinations done during the enrollment period (20) (see Figure 1). A total of 103 Braden score comparisons with either 1 or 2 observations were made per participant. Of the sample, 30 participants (47%) had a preexisting PU at the start of the study; the majority were Stage 1 (11 skin sites) and Stage 2 (26 skin sites) PUs. Mean participant age was 67.68 years (SD = 17.45) and median age 71 years (range 24–92). Men were slightly more predominant (38; 59.4%). Mean Charlson comorbidity index score was 3.27 (SD = 2.85). The most prevalent admitting medical diagnoses observed in this population were cerebrovascular diseases (22, 34.4%), hemiplegia or paraplegia (20, 31.3%), and/or diabetes mellitus with or without complications (14, 21.9%). 

The mean total Braden score recorded was 14.03  ± 2.54. The research staff recorded an average total score of 14.25 ± 2.38, and the unit nurses had a mean total score of 13.80 ± 2.68. Of the 103 comparisons made, research staff and unit nurses recorded the same total score for 70 assessments. The unit nurses recorded a higher risk score compared to the research staff for 20 assessments. For 13 assessments, the research staff recorded a higher risk score compared to the unit nurses. 

IRR. IRR of item and total scores for individual units and overall are shown in Table 2. Overall, ICC scores showed excellent agreement for total (0.807) and nutrition (0.722) scores; good agreement for sensory perception (0.726), moisture (0.659), activity (0.595) and mobility (0.691); and poor agreement for friction and shear (0.266). Comparisons across individual units showed a good deal of variability on the ICC values. However, good to excellent agreement was achieved on the overall score for all units. The ICC for Braden scores of participants with no PUs at the start of the study showed excellent agreement (0.871), but scores for persons with PUs at entry demonstrated a fair agreement (0.533). Kappa values for categorizing the level of risk of PU development showed moderate agreement overall (κ = 0.408). 

Qualitative results. Table 3 summarizes the common themes and subthemes identified in the analysis of 14 nursing staff interviews. Thematic analysis revealed concerns on the scale utility and administration, barriers and challenges faced by nurses, and the benefits of using the assessment tool. The friction and shear item was identified by nurses as a difficult item to rate due to its subjectivity. Nurses suggested changes to the scale presentation on the EMR and recommended additional training sessions on the interpretation of scale items and scores.

Discussion

In this study, the IRR of the Braden Scale was assessed in an acute medical care setting where scores recorded by research staff and the unit nurses were compared. To the authors’ knowledge, this study is one of the first to examine the IRR of item and total scores for electronic versions of the Braden Scale. The clinical nurses in this study were not provided additional training on the Braden Scale in order to study the IRR in a real-life setting. Semi-structured interviews were conducted with unit nurses to understand their perspectives on the utility and usability of the scale. The ICC of the total score for all units (0.807) indicated a high level of agreement on the scores recorded by research staff and the unit nurses for the same patient. This finding was comparable to previous studies evaluating ICC for the total Braden score in an ICU setting.^9,21 The kappa values for categorizing the patients’ level of risk were moderate in agreement overall (κ = 0.408). Although the degrees of agreement suggested by the ICC and kappa values differ, it is important to note the methods of calculation are different and the values should not be compared to each other.^18,29 Kappa statistics can be interpreted as the degree of observed agreement that exceeds the expected agreement by chance alone.¹⁸ The researchers chose to calculate the kappa for the 3 Braden Scale risk categories to provide some insight for clinicians on the IRR of classifying patients as mild, moderate, or high risk of PU development because this was the intended use of the instrument in practice. However, kappa only considers the categories of exact agreement and is subject to less flexibility compared to ICC. 

The ICC compares the variability of different ratings of the same patient to the total variation of all ratings, which provides more flexibility in calculations.^18,29 Additionally, Kottner and Dassen¹⁸ recommended the use of ICC for calculating the degree of IRR for individual and total scores over any other method of calculation. For this reason, the authors focused on ICC to analyze the IRR of individual and total scores, while the kappa calculations were used as additional insight on the reliability of categorizing risk patients. 

With regard to item subscores, the friction and shear item had the lowest ICC value (0.266). This is in contrast to a previous study⁶ in an acute care setting where the friction and shear item had 1 of the highest ICC values with a strong degree of agreement. The difference in findings could be due to variations among the sample population (the current study sample had a higher risk of PU formation because of the restricted mobility inclusion criteria of the RCT). This was evident in this study; 47% of the participants had new or preexisting PUs. Thus, it is conceivable this subpopulation of patients may potentially be more prone to IRR issues compared to patients at lower risk. 

From the interviews in this study, nurses identified friction and shear as a difficult item to rate. This was attributed to the subjective wording used to describe the item subscores and a disconnect between titles and specific descriptions. Friction and shear was an item requiring improvement in scoring reliability. Previous studies in home care²⁰ and intensive care settings²¹ have identified sensory perception, activity, nutrition, and moisture as items with the lowest ICC values.⁶ The ICC values for sensory perception, activity, nutrition, and moisture were comparable to what was found in previous studies.²¹ 

Despite the high ICC correlation for the total score, the Braden Scale will not be clinically useful without staff buy-in, the access to use the scale, or a standardized action plan to implement changes in response to the risk assessment. As a result, it is important to understand the usability and compliance of the scale as used in clinical practice. Qualitative data from the interviews with nurses in this study provided insight on their perspectives toward the Braden Scale and its usability. The thematic analysis was based on nurses’ personal experiences with the Braden Scale. A number of the nurses viewed the Braden Scale as a mandatory assessment tool administered on a set time schedule determined by unit policy. 

With regard to the EMR version of the Braden Scale used in this study, the assessment tool was found in a separate flow sheet that differed from the daily assessment sections. Nurses indicated this was inconvenient and prevented them from remembering to chart the Braden scores. Furthermore, the EMR version of the scale includes only the rating headings and numbers for item scoring without the full descriptions. Although nurses were advised by the unit nurse educators to use the paper versions of the original scale provided by the units for the item descriptions, the interviewed nurses indicated these resources were often difficult to find. Through the authors’ observation of scale use in a real-life clinical setting, it is interesting to note that while the nursing staff was mainly using an abridged version of the scale, the IRR of the scale was not compromised (total score ICC = 0.807). However, having the descriptions easily accessible to the nurses to review could have assisted in the rating process by reducing the ambiguity in item and rating interpretations. The interviewed nurses also suggested that incorporating the full descriptions to the EMR version would be helpful. 

Originally, the Braden Scale was designed and tested to be used in its entirety.³¹ Bergstrom³¹ advised against any alterations to the scale because these modifications could add to the subjectivity of the tool. The authors support Bergstrom’s request and suggest all electronic versions of the Braden Scale be consistent with the original paper version, despite having additional paper resources available for reference. Based on the current findings, when implementing an electronic version of the Braden Scale, scale items and descriptions should be readily available.

Several nurses identified friction and shear as a difficult item to rate, which was consistent with the current quantitative findings. Sensory perception, moisture, mobility, and nutrition were items that also posed challenges. Nurses felt the wording used in item titles created difficulties in scoring, which was consistent with the notion that the Braden Scale incorporates subjective wording.³² According to the survey study (N = 102) by Choi et al,³³ the subjective nature of the Braden Scale may lead to difficulties that could affect scale reliability. To compensate for these difficulties, nurses indicated they would choose higher risk score as a precaution. However, this overestimation was not done by all nurses and could have led to discrepancies in the ratings recorded. 

Previous studies have suggested training and experience may be factors underlying discrepancies in Braden Scale ratings. This appears to be particularly true for new staff.⁶ In a cross-sectional study (N = 201), Nuru et al²⁴ reported nurses exposed to formal PU prevention training tended to be more knowledgeable than persons lacking this training. The study⁴ assessing the knowledge, attitudes, and practice regarding general PU prevention of nurses in Sweden found nurses were more knowledgeable if they had frequent training sessions. Although information on years of experience was not collected during the interviews, the nurses had a single inservice education session (separate from the RCT) organized by their corresponding units, along with the training provided by the new staff orientation. The inservice sessions included training on the purpose of the Braden Scale, risk factors of PU, and the full descriptions of each item and rating. As a result, nurses were generally knowledgeable about the purpose of the Braden Scale. However, some of the specific details from the education sessions were difficult to recall because the current study was conducted several months or years later. 

A number of the nurses interviewed questioned the utility of the Braden Scale because research attesting to its validity was not provided in the training session. Another issue was the uncertainty on how to interpret and utilize the Braden scores in the care of patients. As a result, some of the nurses suggested frequent refresher courses regarding the Braden Scale would be beneficial. 

Regarding attitudes toward PU prevention, Kallman and Suserud⁴ suggested nurses were convinced their own clinical judgment was superior to any PU risk assessment tool,⁴ which was also the case in this study. A majority of the nurses interviewed believed the concepts of the Braden Scale existed in standard care and preventative measures were already being implemented. They indicated this was more effective than the Braden Scale in identifying patients at risk and preventing PUs. Nurses also stated other forms of communication, such as verbal and written reports between shifts, worked better in guiding efforts directed at PU prevention compared to the Braden Scale. The nurses interviewed appeared to have a predetermined notion of the patient’s risk for PU development regardless of the scale and emphasized the patient’s level of mobility was the greatest indicator of risk. Although nurses may have an indifferent view toward the use of the Braden Scale, not using this instrument or some other validated tool for PU risk identification could have serious implications.^4,33 Without a formal assessment tool in place, PUs would not be assessed in a standardized manner and at-risk patients may be missed. This could lead to the development of avoidable PUs, because key factors in prevention may be overlooked. 

A majority of the nurses interviewed found the largest benefit of the routine use of the Braden Scale was it served as a reminder of PUs and the importance of identifying factors that predisposed to their development. Nurses also indicated the scale provided PU prevention guidance to new and less experienced staff. It may be possible to capitalize on this in marshalling support for additional training on the utility of the Braden Scale in identifying at-risk patients who would benefit from specific PU prevention measures. Other positive aspects of the Braden Scale nurses identified included its ease of use and the utility of the total sum score in quantifying risk. 

Further research regarding IRR of the Braden Scale would benefit from a multisite design enrolling a larger number of participants where concurrent scores on consecutive patients are compared. Additionally, comprehensive studies comparing units within acute care settings could provide a better understanding of what leads to observed differences between these units.

Limitations

This study may be limited by the small sample size and the different time points of assessment completed by the research team and nursing staff due to the retrospective nature of the study. Any discrepancies between the EMR and the printed version of the Braden scale may be a limitation. Additionally, the study is based on results obtained from 1 hospital, albeit different units in that facility. Researchers also wanted to examine the differences between units in terms of IRR but were limited by the small and inconsistent sample sizes across the 4 different units. However, the authors believe the IRR comparison between units is a potentially fruitful area for future research because they suspect IRR varies from unit-to-unit based on factors such as unit culture and leadership as suggested by the quantitative pilot study by Marchionni et al.³⁴ 

Conclusion

The IRR values in terms of ICC obtained in this study indicated Braden scores in a real-life clinical setting have a high level of agreement comparable to what was found in literature, with the exception of the friction and shear item. Further training regarding the Braden Scale, particularly regarding friction and shear, may be beneficial in improving score reliability. Overall, nurses believed the use of the Braden Scale was based on unit policy. Subjective wording, challenges with the usability of the EMR version, and inaccessible resources led to difficulties in using the scale. In addition to personal experiences with the Braden Scale, training and unfamiliarity of scale validity may have led nurses to believe use of the scale was redundant to the care they were providing. Study findings can be used to direct efforts to enhance the usability of the scale in preventing the PUs. Nurses indicated the Braden Scale serves as a reminder of the factors that predispose to PU development and it provided guidance on assessment. Recommendations to improve its usability would include attention to how it is presented in electronic versions, ensuring the inclusion of item descriptions and ready access to resource material; and further training on the validity, administration, and interpretation of the Braden Scale. Based on these findings, the factors identified in the study need to be considered when using the Braden Scale in clinical practice. By addressing these issues, effective implementation of the instrument may be achieved. 

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17. Stotts N, Gunningberg L. Predicting pressure ulcer risk. Am J Nurs. 2007;107(11):40–48.

18. Kottner J, Dassen T. Interpreting interrater reliability coefficients of the Braden scale: a discussion paper. Int J Nurs Stud. 2008;45(8):1238–1246. 

19. Sullivan G. A primer on the validity of assessment instruments. J Grad Med Educ. 2011;3(2):119–120. 

20. Kottner J, Halfens R, Dassen T. An interrater reliability study of the assessment of pressure ulcer risk using the Braden scale and the classification of pressure ulcers in a home care setting. Int J Nurs Stud. 2009;46(10):1307–1312. 

21. Kottner J, Dassen, T. Pressure ulcer risk assessment in critical care: interrater reliability and validity studies of the Braden and Waterlow scales and subjective ratings in two intensive care units. Int J Nurs Stud. 2010;47(6):671–677. 

22. Gunningberg L, Lindholm C, Carlsson M, Sjoden P. Risk, prevention and treatment of pressure ulcers — nursing staff knowledge and documentation. Scand J Caring Sci. 2001;15(3):257–263.

23. Beeckman D, Defloor T, Schoonhoven L, Vanderwee K. Knowledge and attitudes of nurses on pressure ulcer prevention: a cross-sectional multicenter study in Belgian hospitals. Worldviews Evid Based Nurs. 2011;8(3):166–176.

24. Nuru N, Zewdu F, Amsalu S, Mehretie, Y. Knowledge and practice of nurses towards prevention of pressure ulcer and associated factors in Gondar University Hospital, Northwest Ethiopia. BMC Nurs. 2015;14:34. doi: 10.1186/s12912-015-0076-8.

25. Wong H, Kaufman J, Baylis B, et al. Efficacy of a pressure-sensing mattress cover system for reducing interface pressure: study protocol for a randomized controlled trial. Trials. 2015;16:434. 

26. de Morton N, Davidson M, Keating J. The de Morton Mobility Index (DEMMI): an essential health index for an ageing world. Health Qual Life Outcomes. 2008;6:63.

27. Charlson ME, Pompei P. Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373–383. 

28. McHugh M. Interrater reliability: the kappa statistic. Biochem Med. 2012;22(3):276–282. 

29. Hallgren K. Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol. 2010;8(1):23–34.

30. Bergstrom N. Letter to the editor: the Braden Scale for Predicting Pressure Sore Risk reflections on the perioperative period. J Wound, Ostomy Continence Nurs. 2005;32(2):79–80.

31. Moore Z, Price P. Nurse’s attitudes, behaviours and perceived barriers towards pressure ulcer prevention. J Clin Nurs. 2004;13(8):942–951. 

32. Choi J, Choi J, Kim H. Nurses’ interpretation of patient status Descriptions on the Braden Scale. Clin Nurs Res. 2014;23(3):336–346. 

33. Lewis G, Carville K, Newall N, Phillipson M, Smith J, Prentice J. Determining the effectiveness of implementing the AWMA Guidelines for the Prediction and Prevention of Pressure Ulcers in Silver Chain, a large home care agency. Stage 1: baseline measurement. Primary Intention. 2003;11(2):57–72.

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Potential Conflicts of Interest: The study was funded by the Alberta Innovates Health Solutions Collaborative Research and Innovation Opportunities team grant (number 20130152). 

Dr. Ho is an Associate Professor, Cumming School of Medicine, University of Calgary; and Section Chief, Physical Medicine and Rehabilitation, Department of Clinical Neurosciences, University of Calgary and Alberta Health Services at the Foothills Medical Centre, Calgary, AB, Canada. Ms. Cheung is a Research Assistant, W21C Research and Innovation Centre, Cumming School of Medicine, University of Calgary. Ms. Southern is a Senior Statistician, O’Brien Institute of Public Health; and W21C Research and Innovation Centre, Cumming School of Medicine, University of Calgary. Ms. Ocampo is a Research Associate; and Dr. Kaufman is a Strategic Programs Manager, W21C Research and Innovation Centre, Cumming School of Medicine, University of Calgary. Dr. Hogan is the Chair of the Brenda Strafford Foundation in Geriatric Medicine, University of Calgary. Dr. Baylis is an Executive Co-Leader, W21C Research and Innovation Centre; and a Section member, Department of Medicine, Division of General Internal Medicine, Cumming School of Medicine, University of Calgary. Dr. Conly is the Medical Director, W21C Research and Innovation Centre, Cumming School of Medicine; Professor, Departments of Medicine and Infection Prevention and Control, Alberta Health Services; and a faculty member, O’Brien Institute for Public Health, University of Calgary. Dr. Stelfox is the Scientific Director of Alberta Health Services’ Critical Care Strategic Clinical Network; Associate Professor in the Departments of Critical Care Medicine, Medicine and Community Health Sciences, University of Calgary; and a faculty member, O’Brien Institute for Public Health, Cumming School of Medicine, University of Calgary. Dr. Ghali is the Scientific Director, O’Brien Institute for Public Health, Foothills Medical Centre, University of Calgary; Co-Leader, W21C Research and Innovation Centre; and a Professor, Departments of Community Health Sciences and General Internal Medicine, Cumming School of Medicine. Please address correspondence to: Chester H. Ho, Division of Physical Medicine and Rehabilitation, Department of Clinical Neurosciences, Foothills Hospital, University of Calgary, 1403- 29th Street NW, Calgary, AB, Canada T2N 2T9; email: chester.ho@albertahealthservices.ca.

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Abstract

Wound assessment is essential to manage wound care. The Wound Trend Scale (WTS) is a paper-and-pen instrument comprised of 14 parameters designed to guide assessment of findings relevant to lower leg ulcer management and includes an infection screen and cues for physician consultation. To determine its clinical utility, predictive value, and reliability, data were retrospectively analyzed from a random sampling of medical records of patients seen at a Foot and Leg Clinic between January 1, 2007 and December 31, 2008.

Patients had 1 leg or foot ulcer, 3 consecutive assessments scheduled according to wound status (twice weekly if at high risk for nonhealing or amputation, weekly for moderate risk, or 1 to 2 months if stable), known outcomes, and a maximum treatment period of 3 months. Patient demographics included ulcer etiology, comorbid conditions (diabetes, neuropathy, peripheral arterial disease), and wound outcomes (closed, infection, amputation and surgery). Predictive values, inter- and intrarater reliability (assessed among the authors and 5 additional nurses with expertise using the study instrument), and the impact of WTS education on the wound assessment process were determined using 5 representative cases. Parameters were compared using the t-test. Seventy (70) patient records were examined and subdivided by ulcer site: foot (below ankle, 37) and leg (ankle and above, 33). Of the 13 etiologies, the foot group had 4 and the leg group 10; the foot group had more diabetes (92%), neuropathy (76%), and peripheral arterial disease (95%) than the leg group (52%, 5%, and 70%, respectively). Ulcer duration before referral averaged 16.42 (range 4–144) months. Wound outcomes included closed (57), infection (21), amputation (13), and surgery (3). Healing predictive values were sensitivity (99%), specificity (87%), and positive and negative predictive values and test efficiency (all 96%). Inter- and intrarater reliability were .85 (range .16–.96) and .86 (range .50–1.00), respectively. On admission, leg ulcers had larger surface area (P<0.05), more edema (P<0.01), more granulation (P<0.05), and higher total WTS scores (P<0.05) than foot ulcers, which had more infections (P<0.05). Foot ulcers at the third assessment had decreased tissue depth (P<0.05), increased epithelial tissue (P<0.01), and lower total WTS score (P<0.05). Significant third assessment parameters for leg ulcers were reduced depth (P<0.001), less necrotic tissue (P<0.001), less exudate (P<0.01), improved periwound condition (P<0.05), reduced edema (P<0.001), and increased epithelialization (P<0.01). After exposure to the WTS experience, the number of parameters assessed increased from 2.6 (registered nurses) and 1.5 (student nurses) to both using 15 (P<0.001). Nurses complied 100% with physician consultation for cued risks. Patient outcomes were 81% closure, and 70% had physician consultation for the risks identified. WTS predictive performance was excellent and improved nursing assessment practices. Future research to identify parameter criteria validity is warranted.

A chronic leg ulcer, defined as “any skin damage below the knee that takes more than 4 to 6 weeks to heal,”¹ simplifies the classification of ulcers but fails to alert the clinician to the importance of identifying etiological and comorbid factors essential to optimal care. An Australian epidemiology study² (N = 242) classified chronic leg ulcer etiologies by diagnosis and comorbid disease influences, singly or in combination. The etiologies identified were venous insufficiency, mixed etiology, arterial disease, diabetes, rheumatoid arthritis, thrombocythemia, trauma, skin tumor, chronic osteomyelitis, pyoderma gangrenosum, chronic dermatitis, chronic infected sinus, and Martorell ulcer. Additional types of leg ulcers identified through the authors’ clinical experience are neuropathic ulcers, surgical wound failure, pressure ulcers, vasculitis, deep vein thrombosis, calciphylaxis, burns, lymphedema, lipedema, self-mutilation, septic shock, emboli, Kaposi sarcoma, factor S ulcer, Marjolin’s ulcer, and foot deformity-related ulcers, which can be congenital or secondary to comorbid diseases such as diabetes. 

The multiple etiologies of leg ulcers, combined with individual patient comorbidities and available resources of different clinical care environments, underscore the considerable challenges of their clinical management. Implementation of a periodic nursing questionnaire (1994, 1998, 2004, and 2005) that audited wound care in Sweden enabled longitudinal analysis of prevalence, etiology, treatment of hard-to-heal leg and foot ulcers, and nursing time.^3,4 From 1994 to 2005, wound management improved, ulcer prevalence declined from .22% to .15%, weekly treatment time dropped from 1.7 to 1.3 hours per patient, and annual costs decreased by $6.96 million SEK. Repeated questionnaires, ongoing education, development of a wound healing center, and creation of multidisciplinary wound management recommendations all served to increase interest in and effectiveness of wound management. 

A descriptive survey⁵ of a sample of district nurses in Norway regarding their opinions of their knowledge of foot and leg ulcer treatment (N = 102 completed questionnaires) found most nurses (60%) felt they had inadequate knowledge of wound care. They were uncertain about assessment, etiology, choice of wound healing products, and treatment. Individual clinical experience and colleagues were the main sources of their knowledge of wound care. 

A descriptive observational study⁶ that analyzed 35 ulcer treatments provided to 32 patients with foot and leg ulcers by 31 home care nurses in Norway found no etiologic ulcer diagnosis was made in 16 cases and serious comorbidities were present in 79.9% of cases. Overall, nurses in this study were unsure of their assessment, treatment principles used often were outdated, documentation of treatment was poor, and use of compression on undiagnosed ulcers was sometimes incorrect.

An incidental sampling survey⁷ of podiatrists and nurses in the United Kingdom (N = 102) attending a lower extremity wounds conference explored attitudes, knowledge, and skill in lower extremity wound care to identify training needs and inform wound care education. The majority of respondents participated in continuing professional development, whereas the minority used accredited university courses. Inconsistencies in wound care knowledge and skills that were identified highlighted the importance of educational strategies to standardize wound care. 

Wound assessment is fundamental to diagnosis, appropriate care, and monitoring wound progress, but the aforementioned research^5,7 has found professional training programs for primary care nurses lack sufficient clinical education to provide appropriate care for patients with leg ulcers. A wound assessment tool that provides a common clinical language and encourages consultation could bridge gaps in professional knowledge between primary and specialist care providers.

Foot and Leg Ulcer Clinic. The Foot and Leg Ulcer Clinic in Victoria, British Columbia, Canada is a referral facility for patients with problematic wounds (ie, nonhealing, deteriorating, necrotic tissue, amputation risk, or other clinical problems). The core clinic team consists of 2 advanced wound care nurses and 2 physicians. Nurses admit and monitor patients in collaboration with a physiatrist who follows medical care, and a foot and ankle orthopedic surgeon evaluates and follows patients who may require surgery and postoperative care. A network of disciplines that provides expedited referral access includes vascular surgeons, infectious disease specialists, orthotists, podiatrists, pedorthists, and compression garment fitters. Consultations with physiotherapy, occupational therapy, dietetics, and social services are available on an individual basis. The nurses coordinate wound management with the primary nurses through care plans, consultation, and education. 

Wound Trend Scale (WTS). The WTS, a paper-and-pen instrument developed by clinic wound speciality nurses, evolved through evaluation and modifications to improve relevance to leg ulcers and utility in a working clinic. Wound assessment theory is melded with clinical information to identify findings that are sensitive to wound healing phases, wound bed preparation, and risk identification. 

The WTS systematically guides assessment of findings relevant to leg ulcer management, current wound status, significance of findings, wound trend, wound needs, and changes in the wound using 14 parameters, an infection screen, and cues for physician consultation. Each parameter has identified findings that are assigned a value from low to high corresponding to its potential to impair healing. The nurse examines the wound for each parameter and records the value of the highest finding identified (if absent, the item is left blank on the form). A decrease in value from the previous assessment is interpreted as a positive change that may predict healing or reduce impairment to healing. Increased values indicate deterioration or possibly more impairment to healing. The total WTS score is the combination of influences each parameter contributes. Healing is predicted when the total score is equal to or less than the previous total (closure, defined as complete epithelialization, is 0); an increase in the total score predicts wound deterioration. Infection risk screening is performed at every assessment. High risk of amputation, nonhealing findings, and positive infection screens are cued with an asterisk and require the nurse to consult with a physician. Assessments are recorded on the WTS documentation form and stored in the medical record.

At the authors’ clinic, patient reviews are scheduled according to wound status: twice weekly for high risk, weekly for moderate risk, or 1 to 2 months if stable. Primary care nurses or family physicians are encouraged to communicate concerns.

WTS parameter rationale and use. The WTS documentation form uses a unique number identification for each wound starting with 1, which is recorded on the care plan with the start and end dates recorded as day, month, and year (eg, #1 Left posterior heel, Start 010512, Closure 060712; #2 Left 5th toe, Start 220210, Amputation 060610). Multiple columns allow the identification number of wounds, assessment dates, and values for findings for each wound to be recorded. Wound closure or surgical procedures are recorded as end dates.

A retrospective analysis⁸ of 2350 heel pressure ulcers used data from the United States Wound Registry and regression models to assess factors known to be associated with healing. The analysis identified depth of tissue involved as a significant variable (P<0.05), which then was tested and validated. Variables predicting healing likelihood in nearly all pressure ulcer assessment models were wound size, wound age, number of wounds, evidence of bioburden, tissue type exposed (Wagner grade or stage), nonambulatory status, and need for hospitalization during treatment. The analysis resulted in a wound stratification system and healing index that could predict healing likelihood. With the exception of nonambulatory status and hospitalization, all of these variables are included in the WTS. 

A study by Greatrex-White and Moxey⁹ to evaluate the ability of existing wound assessment tools to meet the needs of nurses performing wound assessment included a literature review that identified criteria of an optimal wound assessment tool. Assessment tools, which were selected using specified inclusion and exclusion criteria, then were evaluated against the optimal criteria. No evaluated tool fulfilled all criteria. The WTS addresses objective wound findings (measurement, tissue type, exudate, surrounding skin, pain and infection) and advanced subjective issues (documentation, communication, and ease of use). Greatrex-White and Moxey’s study elevates the role of wound assessment tools to support nursing practice, a practical issue for the clinic where regular nursing staff are wound specialist nurses and relief staff are not. The ultimate goal is to provide a wound assessment tool that supports both nonwound specialist nurses and specialist nurses to assess wounds systematically and consistently consult with the physician when cued risks are identified. 

Surface area. Surface area is the maximum wound length multiplied by the perpendicular maximum width to the nearest 0.5 cm (a simple way to achieve this is by visualizing a square around the wound). Reduction in surface area is associated with healing, but an increase may indicate tissue loss from infection, ischemia, trauma, pressure injury, factitious injury, nonhealing, or debridement of necrotic tissue. 

A review¹⁰ of the importance of wound measurement found both serial area measurement and percentage area reduction can differentiate responding from nonresponding wounds and help predict outcomes. A reduction over 2 to 4 weeks in wound area predicts healing or advises a reassessment of treatment was demonstrated in a multicenter, randomized controlled trial¹¹ of 90 venous leg ulcers that found the 2-week percentage reduction in wound area was correlated with outcome (P = 0.002) — that is, a >30% reduction by 2 weeks is an accurate predictor of healing.

Depth. The type of tissue (injured, dead, or lost) influences the risk of amputation or nonhealing of leg ulcers. Depth value is the highest finding identified: partial-thickness or full-thickness skin loss; involvement of fascia, muscle, tendon, or bone; presence of a foreign body or medical devices; or obscure when all of the wound base cannot be seen. Anatomic knowledge of the ulcer site, including the location of blood vessels and nerves, is necessary to anticipate findings and identify if probing could be a risk. Patient consent is required before gently examining the wound base with a sterile probe to identify the type and integrity of involved tissues; clinic care standard does not allow probing wounds if the patient cannot cooperate, is at anatomical risk, the procedure causes pain, or if pathergy is known or suspected.

The anatomic structure of the foot and of the leg to a lesser extent limits the clinical significance of depth measurements, because much of the foot and parts of the leg have shallow tissue coverage of tendons and bones. As a result, injury to toes, metatarsal heads, heels, ankles, and the tibia crest may be limb-threatening but appear insignificant. A high-risk cue is assigned to tendon, capsule, bone, foreign body, medical device, or obscure. 

Edge. Edge classifications include indistinct; distinct and attached; rolled and detached; or fibrotic, scar, or callus. Ousey and McIntosh¹² acknowledge reduced vascularity, elasticity, and strength (about 70%) of scar tissue, compared with original tissue, may contribute to delayed healing and a fragile epithelial surface.

Undermining. Undermining, or tissue loss under the skin or between tissue planes, may present as a sinus, fistula, or abscess. The extent of undermining may be estimated by probing the undermined area and marking the end of the probe detected on the skin surface; the value recorded is the maximum length identified in cm. The amount of wound edge undermined is valued as 1: <25%, 2: 25%–50%; 3: 51%–75%; and 4: >76%.

Necrotic tissue and debridement. Debridement of necrotic tissue, such as slough and soft and hard eschar, reduces bioburden and odor, accelerates the inflammatory healing phase, and stimulates quiescent wounds.¹³ Selection of debridement method depends on the nature and amount of necrotic tissue, patient status, and presence of infection. 

Stable eschar is dry, hard, nonfluctuant, and not infected. In cases of suspected arterial insufficiency, guidelines¹⁴ recommend stable eschar be kept dry and intact until vascular investigation of the healing potential of the wound is completed and the physician is consulted regarding debridement method. 

To provide a full description of the wound base, the WTS assigns values to the percentage of necrotic and risk tissues identified in depth: 1: <25%; 2: 26%–50%; 3: 51%–75%; and 4: >76%. 

Exudate. Exudate is identified by type and amount based on dressing presentation: 1) moist — exudate present, nonadherent dressing; 2) small — exudate present to saturated dressing with contained exudate; 3) moderate — exudate strikethrough; 4) large — leaking exudate onto clothing; or 5) uncontrolled — exudate leaking onto the patient, clothing, and/or bed linen within 48 hours of dressing change or dry when moist healing is desired. The need to rehydrate tissues delays healing dry wounds that require a moist environment. 

Bleeding is not an expected finding for chronic wounds; the cause should be investigated. Active bleeding requires physician consultation. The surgeon is notified of serosanguineous or purulent drainage from a previously closed incision, which is an indication of surgical wound failure. 

The World Union of Wound Healing Societies consensus document¹⁵ states the amount of exudate is influenced by the size of the wound and healing phase, with the maximum amount during the inflammatory and proliferative phases and with reduction to 0 with complete epithelialization. Increased exudate is associated with factors that increase capillary leakage such as cardiac, renal, or hepatic failure; edema; inflammation; increased bacterial burden; impaired lymphatic drainage; and specific wound pathology. Exudate color and viscosity are influenced by the type of necrotic tissue present, bacterial colonization, white blood cell presence, and the dressing material used. Managing exudate depends on diagnosing and treating underlying conditions and appropriate dressing selection. Figure 1 illustrates the importance of cleansing the wound before attempting to identify the type of exudate and differentiate pus from accumulated drainage. 

Periwound skin. Periwound skin is examined to identify blanchable and nonblanchable erythema, maceration, tissue breakdown, trauma, or rash. Erythema can be a sign of inflammation or infection, but nonblanchable erythema indicates altered blood flow and impending tissue destruction. An exploratory study¹⁶ comparing blood flow in areas of nonblanchable erythema to undamaged skin found high perfusion in the center of the lesion and normal perfusion in unaffected areas. In her clinical review, Bianchi¹⁷ identified maceration associated with exudate enzymes increases the risk of tissue breakdown and dressing trauma. Rashes and periwound breakdown are investigated for venous eczema, autoimmune disorders, cellulitis, and contact dermatitis.^18,19

Appropriate management of periwound skin includes effective cleansing. A Cochrane review²⁰ found no evidence to suggest the use of potable tap water to cleanse wounds and the periwound skin influences infection or wound healing in acute or chronic wounds, including those with bone exposure. Showering loosens necrotic tissue and removes periwound surface debris, organisms, and exudate. In addition, a retrospective analysis²¹ of cleansing methods for chronic foot and leg ulcers (N = 236) found showering may lower the rate of both toe and major amputations compared with the use of foot baths (P = 0.037). Cooled boiled water, distilled water, or saline solution may be used for chronic wounds when potable water is not available. 

Edema. The practice of scoring pitting edema as 1+ (2 mm), 2+ (4 mm), 3+ (6 mm), and 4+ (8 mm)²² may be unsuitable for many leg ulcers because fibrosis and shallow tissue depth may not allow sufficient tissue expansion from fluid pressure. To overcome these issues, the authors developed an edema scale (see Figure 2). 

Edema has been reported to contribute to ulcer development, delayed healing, cellulitis,²³ amputation risk,²⁴ and surgical wound dehiscence.²⁵ A prospective study²⁴ of 575 patients with an infected diabetic foot ulcer found periwound edema was an independent risk factor for amputation, which was necessary in 159 patients (28%). 

In her clinical review of managing chronic edema, Hedger²⁶ points to the multiple local and systemic causes that require the correct etiologic diagnosis to determine appropriate management. A Cochrane review²⁷ of compression for venous ulcers found compression increased wound healing rates compared with no compression. 

Pain assessment. On admission to the authors’ clinic, comorbidities and age-associated changes that contribute to the patient’s pain experience, singly or in combination, are investigated. Patient perception of pain (presence or absence) is embedded in the infection screening. Nurses must be alert to the possibility of loss of protective sensation due to neuropathy or progression of arterial insufficiency and that infection may trigger a different sensation (eg, ache where sensation previously was absent). 

Infection risk. Every assessment includes infection screening; if positive, physician consultation is required. Infected chronic wounds may increase size, undermining, or exudate amount.²⁸ The classic signs and symptoms of infection are erythema, warmth, swelling, and pain. The Infectious Diseases Society of America’s²⁹ clinical practice guideline for the diagnosis and treatment of diabetic foot infections requires the presence of ≥2 classic signs of infection for diagnosis of infection. Patients with diabetes may have elevated blood glucose when the ulcer is infected. 

At the authors’ clinic, wound cultures are done if signs and symptoms of infection are evident. According to Dow,²⁸ chronic wound response to infection may be subtle and require differentiation from tissue breakdown due to inadequate pressure offloading or insufficient perfusion. Biofilm is a potential source of infection, which may be controlled with maintenance debridement and topical antiseptics.¹³

A 2-year longitudinal cohort study³⁰ compared the accuracy of a diagnosis of osteomyelitis in patients with diabetic wounds (N = 247) using the probe-to-bone (PTB) test and bone culture. During a mean 27.2-month follow-up, 30 patients were diagnosed with osteomyelitis. Overall, the PTB test was both highly sensitive (0.87) and highly specific (0.91). Although the negative predictive value was 0.98, the positive predictive value was only 0.57, indicating the PTB test may be better at ruling out osteomyelitis than at confirming it.

 An observational study³¹ comparing the University of Texas (grade and stage) and Wagner (grade) ulcer classification systems as predictors of outcome in 194 patients with diabetic foot ulcers found increasing ulcer stage (which includes presence of infection) was associated with delayed healing and increased amputation risk.

The purpose of this clinical experience study was to describe lower leg ulcers and analyze wound assessment and associated clinical management data using the WTS. Specific wound assessment tool functions are examined in the following questions:

• What is the predictive performance of the WTS for wound healing or deterioration?

• What is the inter- and intrarater reliability of the WTS for clinic nurses experienced in using the WTS to assess leg ulcers?

• Can the identification or change in WTS findings be used to select or evaluate interventions and monitor response?

• What is the compliance with physician consultation when an asterisk-cued, high-risk finding or positive infection screen is identified? 

Method

The study data were derived from information contained in the medical records of a random, retrospective convenience sample of 70 patients seen at the authors’ clinic between January 1, 2007 and December 31, 2008. Inclusion criteria stipulated patients had 1 leg ulcer (wound below the knee), 3 consecutive WTS assessments, known wound outcomes, and treatment within a maximum of 3 months. The number of patients was an arbitrary decision by the Wound Collaborative Committee. Patient data were reviewed and analyzed in total as well as by subgroups by ulcer site (foot, below the ankle; and leg, ankle and above) to represent wound groups such as diabetic foot ulcers or venous leg ulcers.² The clinical specialist and nursing staff extracted patient and ulcer data, including all WTS parameter findings, from the medical records and entered it into Microsoft Excel spreadsheets.

Patient and ulcer description. Patient records were reviewed for ulcer etiology, distribution of ulcers by site as foot (below the ankle) or leg (ankle and above), and duration of ulcer before clinic referral; outcomes included closure (complete epithelial coverage), infection, surgical procedures other than amputation, and amputation (major, below or above knee; or minor, limb preservation involving digits, rays, and the ability to stand or walk³²). 

Predictive value performance for wound healing. Nursing staff collected data from 3 consecutive WTS assessments, including positive infection screen information and ulcer outcome, on a spreadsheet. The total WTS scores were compared: the second score was compared to the first and the third to the second. Equal or reduced scores identified the prediction as positive for healing. Increased scores identified the prediction as negative for healing (ie, deterioration). Each author independently reviewed the patient information from the medical record to verify the prediction; differences were settled by consensus. Standard formulas for calculating sensitivity, specificity, predictive values (positive and negative, including false values for each), and test efficiency were used to determine predictive value performance. 

Consent and ethics approval. Clinic patients routinely provide consent for treatment and use of their clinical data for clinical, educational, or research purposes. Patients were also routinely consulted and agreed to treatment throughout their care process. As a result, the Research Ethics Committee in Victoria, BC, determined ethics approval was not required for performing the clinical experience study. Nurses participated in the study on a volunteer basis and were assured of anonymity. 

Inter- and intrarater reliability. Collecting inter- and intrarater reliability information with patients was deemed unacceptable because patients would be subject to multiple wound assessments that could increase waiting time for treatment and pain and decrease access to other clinic patient services. An alternative was to develop 5 cases based on typical assessment requirements and common clinical presentations. The Certified Wound Specialist (author) developed the cases. Each case had a wound image and a written description of etiology, relevant history, and findings not accessible from the image (eg, warmth, pain). The cases were reviewed by a second author and trialed by the third before rater reliability was assessed. 

Information on the cases used to determine interrater reliability was emailed to volunteer clinic nurses with WTS experience (N = 5) to be completed at their convenience. A second email requested a repeat assessment for intrarater reliability 24 hours after electronic receipt of completed assessments. Participating nurse anonymity was ensured by assigning the nurses numbers and labeling the case sets as A or B for interrater reliability and intrarater reliability, respectively. Parameter findings, WTS scores, and positive infection screens were compared to the Certified Wound Specialist’s assessment for interrater reliability and the nurses’ first and second case sets for intrarater reliability. Correlation coefficients (median and range) were calculated using the Microsoft Excel 2010 statistic program. 

Change in wound assessment practice. Community registered nurses (N =10) and student nurses (N = 10) volunteered to participate while attending a clinic observation day. Before any wound management discussion, each participant demonstrated his or her wound assessment process on a consenting patient while an author checked assessment parameters observed on a WTS form. Then the lead author provided a 15-minute WTS education session, after which the participant practiced assessment using the WTS form with coaching by an author. Each participant then completed a solo wound assessment using the WTS, during which the author recorded the wound assessment parameters used. The number of wound parameters assessed by each volunteer, including infection screen, was compared for the pre- and post-WTS education wound assessments. 

WTS influence on selection, monitoring, and evaluation of wound interventions. Parameter findings, infection screen, and admission total WTS score were compared for the subgroups (foot and leg) to identify differences in ulcer characteristics. The same factors were compared to identify sensitivity of the WTS to response to wound management between admission (first assessment) and the third assessment for the subgroups. The medical record was reviewed to match the parameter findings with the selection of appropriate wound intervention or compliance with care guidelines. Parameter findings associated with amputation and infection were reviewed to identify a common cluster.

Physician consultation for cued risks and positive infection screens. The number of tissue depth findings and positive infection screens that cued physician consultation was confirmed by reviewing the medical records; compliance was the percentage of confirmed consults. 

Statistical analysis. Determination of true or false predictions provided values for the number of true positives, false positives, true negatives, and false negatives. Standard equations were used to calculate predictive performance of the WTS (sensitivity, specificity, positive and negative predictive values, and test efficiency). Assessment of the inter- and intrarater reliability among WTS-experienced volunteer nurses was performed by calculating the Pearson product-moment correlation coefficient (r) using Microsoft Excel 2010. Change in assessment practice was analyzed with the 2-sample, 2-tailed, unpaired t-test assuming unequal variances in Microsoft Excel 2010. Analysis of WTS parameter findings, including positive infection screens and total score for the group and subgroups by wound site, used an unpaired, 2-sample, 2-tailed t-test assuming equal variances using Microsoft Excel 2010. 

Results

Ulcer etiology and description. The 70 records examined included 37 foot and 33 leg ulcers. Average ulcer duration was 16.42 (range 4–14) months before clinic referral. Table 1 itemizes the primary ulcer etiology and comorbidities based on wound site. Foot wounds had fewer etiologies: 65% were diabetic foot ulcers, 22% were heel ulcers, 8% were related to trauma, and 5% to surgical hardware. Leg wounds included 10 different etiologies: 48% were arterial/venous mixed ulcers, 12% were related to trauma, 9% each involved venous insufficiency and pyoderma gangrenosum, 6% were related to vein harvest, and 1 case each (3%) to malignancy; hematoma; scleroderma; calcinosis, Raynaud’s phenomenon, esophageal dysmotility, sclerodactyly, and elangiectasia (ie, CREST syndrome); and rheumatoid ulcer. Comorbid conditions (diabetes, 92%; neuropathy, 76%, and peripheral arterial disease, 95%) occurred more frequently in foot than leg ulcers (52%, 15%, and 70%, respectively). 

Ulcer outcomes. Fifty-seven (57, 81%) wounds closed, 12 at the third assessment and 45 later. Of the 21 positive infection screens, 15 were in the foot and 6 in the leg. Thirteen (13) amputations (8 foot, 5 leg; all major) were performed. The 3 surgeries that were required all occurred in the foot group; 2 involved removal of surgical hardware closed post surgery, and 1 was a debridement that exposed extensive tissue loss requiring a major amputation.

Predictive value performance. The predictive value of the WTS included sensitivity (99%), specificity (87%), positive predictive value (96%), negative predictive value (96%), and test efficiency (96%). Table 2 presents completed WTS wound assessment data to demonstrate use of the form and real case illustrations of scores for true positive, false negative, and true negative classification. Table 3 provides the distribution of true positives, false positives, true negatives, and false negatives along with the equations and predictive value calculations. Figure 3 provides images and scenario information of the cases A, B, and C as documented in Table 2.

Inter- and interrater reliability. The average Pearson correlation coefficient (r) for interrater reliability was .85 (range .16–.96), and the average Pearson correlation coefficient for intrarater reliability was .86 (range .50–1). One nurse missed surface area and tissue depth for 1 case, which appeared to be an oversight because all other cases submitted by this nurse included these parameters. 

Change in wound assessment practice. Registered nurses used significantly more wound assessment parameters (2.6) than student nurses (1.5) before WTS education and experience (P<0.001). The number of WTS parameters and infection screenings increased to 15 for both registered and student nurse groups (P<0.001) after WTS training and experience (see Table 4). 

WTS parameter influence or response to wound management. On admission, 45% of patients had necrotic tissue. Debridement is standard practice but not clearly reported in the medical record. Maggot debridement therapy was identified for 11 patients; after 1 week of maggot debridement therapy, necrotic tissue was removed with the following outcomes: exposure of surgical hardware (1 case), extensive tissue loss requiring amputation (1), and closure (9); closure of the wounds after surgical removal of hardware was included for the entire group. Edema was identified in 38 patients on admission and successfully reduced with appropriate compression therapy for 14 patients. Two (2) patients with a dry wound bed were provided a semiocclusive dressing to hydrate the wounds. 

Parameters infrequently identified were undermining (15, 21%) and induration (9, 13%), but the nurses responded to these findings with physician consultation resulting in diagnosis and more frequent assessments to monitor progress or detect complications. Of the 15 patients with undermining, 12 required major amputations. Patients with induration had different etiologies or outcomes: diagnosis of inflammatory ulcer (4), trauma (3), and amputation (2).

Infection was identified by culture in 21 wounds (15 foot and 6 leg). Antibiotic therapy was prescribed after physician consultation for all patients. Among the 16 patients with ulcers containing persistent necrotic tissue, a positive infection screen was accompanied by a medical intervention (antibiotics, surgical debridement, monitoring plan). Outcomes for these patients included 11 amputations, 1 surgical hardware removal, and 4 closures.

All patients undergoing amputation (13) had the following findings: total WTS score increased or was 1 point lower, tendon and/or bone tissue involvement was noted, and no epithelial tissue was identified. 

Significant differences were found between foot and leg ulcers on admission. Leg ulcers had a larger surface area (P<0.05), more edema (P<0.01), more granulation (P<0.05), and higher total scores (P<0.05) than foot ulcers. Foot ulcers had more infections (P<0.05). No significant difference in healing (defined as complete epithelialization) was noted. Table 5 provides complete data for this comparison. 

Parameter changes between admission and the third assessment were examined to determine sensitivity of parameters to change during treatment of foot and leg ulcers. Patients with foot ulcers had a significant decrease in tissue depth (P<0.05), increased epithelial tissue (P<0.01), and a lower total score (P<0.05); these outcomes are expected with foot ulcer healing progression when appropriate wound care and offloading are provided. The foot group had 24 (65%) diabetic foot ulcers and 8 (22%) heel ulcers; when combined, 87% of the patients had pressure offloading as standard practice. Significant parameter changes identified for the leg ulcer site group were decreased depth (P<0.001), less necrotic tissue (P<0.001), less exudate (P<0.01), improved periwound (P<0.05), reduced edema (P<0.001), and increased epithelialization (P<0.01). The leg group had more edema (P<0.01); evidence-based practice supports the use of compression for venous ulcer treatment.²⁴ If arterial/venous mixed and venous insufficiency patients are combined, 19 (57%) of the leg ulcers could potentially benefit from compression therapy. Reduced pressure gradient compression was used effectively for 14 patients, resulting in a significant edema parameter change (P<0.001), which may reflect parameter sensitivity to compression therapy. Compression therapy ulcer healing exhibited typical findings: decreased depth, necrotic tissue, and exudate and improved periwound condition.

Physician consultation for cued risks and positive infection screens. Nurses consulted physicians when encountering a cued, high-risk, or positive infection screen in 87 instances (65 tissue depth, 22 positive infection screens) with 100% physician consultation with interventions documented in the medical record; 49 (70%) of the patients had been identified as being at high risk.

Discussion

Predictive value of the WTS to leg ulcer healing or deterioration was high for sensitivity (99%), specificity (87%), positive predictive value (96%), negative predictive value (96%), and test efficiency (96%). These results are encouraging because they represent a real working specialist wound clinic and patient population when ulcers are treated regardless of potential to heal. 

Another leg ulcer assessment tool is the Leg Ulcer Measurement Tool (LUMT), developed by Woodbury et al.³³ In their study, 22 patients with leg ulcers (arterial, venous, diabetic) were assessed by 4 specialist wound nurses and 2 inexperienced nurses over 4 months to determine rater reliability. Responsiveness of the total LUMT score was based on 1-rater assessments of 19 patients (3 did not complete the study). The researchers reported interrater and intrarater reliability >0.75 for total LUMT score and responsiveness to wound status coefficient = 0.84. 

A major difference between the LUMT and WTS is the surface area score and its implication to the total score and interpretation of the findings. Both instruments calculate the surface area as the maximum length multiplied by width in cm², but the WTS assigns the parameter value of the surface area where the LUMT assigns the surface area to unequal interval categories (ie, 1: >2.5 cm², 2: 2.5–5 cm², 3: 5.1–10 cm², and 4: >10.1 cm²). To illustrate the difference in parameter sensitivity and clinical interpretation of this difference, an ulcer with 3 consecutive assessments surface area of 1 cm x 2 cm, 1 cm x 1 cm, and 0.5 cm x 0.5 cm would all be scored 1 and interpreted as no change in the LUMT, but the WTS would assign a parameter value of 2, 1, and 0.25 and interpret the change as a healing trend. The same wound surface area in reverse would be interpreted in the WTS as deterioration but remains as 1 and no change in the LUMT. The largest surface area in the current study was 22 cm x 11 cm, a WTS value of 242 WTS and a LUMT of 4. Ranking findings from least to most potential to impair wound healing to determine parameter value would give maceration a score of 3 (WTS) but it is assigned 1 (LUMT). 

Greatrex-White and Moxey⁹ identified a role for wound assessment tools to assist nurses, wound specialists or general, in their everyday practice. The change in the number of assessment parameters from an average of 2.6 parameters for community nurses and 1.5 parameters for students to 15 parameters for both after WTS education and clinical practice (P<0.001) supports the need for both novice and experienced wound nurses to be consistent and reduce dependence on clinical/colleague experience or misinformed memory. 

WTS findings or changes with intervention selection supported by medical record review were identified and described but lacked statistical support. Statistical differences in parameters between foot and leg site ulcers and response to therapy (per parameters) were noted between admission and the third assessment for both the foot and leg subgroups. WTS parameters identified for all 13 amputation patients was a total score increase or minimal 1 point improvement, tendon or bone involved, and failure to develop detectable epithelial tissue. These changes can be explained partially by expectations of standard practice but require more rigorous study design and statistical analysis to support these assumptions.

Cued findings and risks that require physician consultation for prompt intervention, diagnosis, or specific care directions may address the low rates of consultation identified by McIntosh and Ousey⁷ and improve communication between nurses and physicians. Infection screening and embedded pain inquiry ensured clinical assessment and appropriate intervention for patients with a positive infection screen result. 

Evaluation of the WTS resulted in revising the WTS (version 3) to cue undermining and induration for physician consultation because these findings were found to be present for ulcers of unusual etiology or indicate risk of amputation.

Limitations

The duration of leg ulcers before referral to the clinic ranged between 4 months and 12 years. The delay in referral may increase the frequency of complications, nonhealing, and amputations. A specialist clinic may have a referral bias toward more complex or nonhealable wounds. The focus of the clinical experience and predictive value study was limited to the clinic operational needs and resources. Small sample size and lack of statistical analysis consultation support and design may have weakened parameter analysis. The dependence on documentation in this study may underestimate confirmation of an intervention or response to a finding if not recorded or missed by the auditor.

Conclusion 

The WTS tool for wound assessment and documentation demonstrated the potential to predict the wound trend for healing and deterioration for leg ulcers. Inter- and intrarater reliability was good for wound nurses with WTS clinical experience. The number of wound parameters assessed by general registered nurses and students during a single day wound clinic experience improved. Further research to determine parameter criteria validity and potential as surrogate endpoints for wound research specific to a parameter (ie, debriding agent efficacy) may be warranted. n

Acknowledgments 

The authors thank the clinic team and patients who consented to have their photographs and experiences made available for educational and research purposes. Editorial support was provided by Joanna Gorski of Prescriptum Health Care Communications Inc, Niagara-on-the-Lake, Ontario, Canada. 

References

1. Royal College of Nursing. The Nursing Management of Patients With Venous Leg Ulcers: Clinical Practice Guidelines. 2006. London: RCN.

2. Baker SR, Stacey MC, Singh G, Hoskin SE, Thompson PJ. Aetiology of chronic leg ulcers. Eur J Vasc Surg. 1992;6(3):245–251.

3. Oien RF, Håkansson A, Ovhed I, Hansen BU. Wound management for 287 patients with chronic leg ulcers demands 12 full-time nurses. Leg ulcer epidemiology and care in a well-defined population in southern Sweden. Scand J Prim Health Care. 2000;18(4):220–225.

4. Oien RF, Ragnarson Tennvall G. Accurate diagnosis and effective treatment of leg ulcers reduce prevalence, care time and costs. J Wound Care. 2006;15(6):259–262. 

5. Haram R, Ribu E, Rustøen T. The views of district nurses on their level of knowledge about the treatment of leg and foot ulcers. J Wound Ostomy Continence Nurs. 2003;30(1):25–32.

6. Ribu E, Haram R, Rustoen T. Observations of nurses’ treatment of leg and foot ulcers in community care. J Wound Ostomy Continence Nurs. 2003;30(6):342–350.

7. McIntosh C, Ousey K. A survey of nurses’ and podiatrists’ attitudes, skills and knowledge of lower extremity wound care. Wounds UK. 2008;4(1):59–68. 

8. Horn SD, Fife CE, Smout RJ, Barrett RS, Thomson B. Development of a wound healing index for patients with chronic wounds. Wound Repair Regen. 2013;21(6):823–832. 

9. Greatrex-White S, Moxey H. Wound assessment tools and nurses’ needs: an evaluation study. Int Wound J. 2015;12(3):293–301.

10. Flanagan M. Improving accuracy of wound measurement in clinical practice. Ostomy Wound Manage. 2003;49(10):28–40.

11. Arnold TE, Stanley JC, Fellowes EP, et al. Prospective, multicentre study of managing lower extremity venous ulcers. Ann Vasc Surg. 1994;8(4):356–362.

12. Ousey K, McIntosh C (eds). Lower Extremity Wounds: A Problem-Based Approach. Toronto, ON: John Wiley & Sons; 2008;180. 

13. Leaper DJ, Schultz G, Carville K, Fletcher J, Swanson T, Drake R. Extending the TIME concept: what have we learned in the past 10 years? Int Wound J. 2012;9(suppl 2):1–19. 

14. Hopf HW, Ueno C, Aslam R, et al. Guidelines for the treatment of arterial insufficiency ulcers. Wound Repair Regen. 2006;14(6):693–710.

15. World Union of Wound Healing Societies (WUWHS). Principles of Best Practice: Wound Exudate and the Role of Dressings. A consensus document. London: MEP Ltd;2007. 

16. Lindgren M, Malmqvist LA, Sjöberg F, Ek AC. Altered skin blood perfusion in areas with non blanchable erythema: an explorative study. Int Wound J. 2006;3(3):215–223.

17. Bianchi J. Protecting the integrity of the periwound skin. Wound Essentials. 2012;1:58–64. 

18. Timmons J, Bianchi J. Disease progression in venous and lymphovenous disease: the need for identification and management. Wounds UK. 2008;4(3):59–71.

19. Newton H. Assessment of a venous leg ulcer. Wound Essentials. 2010;5:69–78.

20. Fernandez R, Griffiths R. Water for wound cleansing. Cochrane Database Syst Rev. 2008;23(1):CD003861. 

21. Sano H, Ichioka S. Which cleansing care is better, foot bath or shower? Analysis of 236 limb ulcers. Int Wound J. 2015;12(5):577–580. 

22. Bryant RA, Nix DP. Acute & Chronic Wounds: Current Management Concepts, 4th ed. Toronto, ON: Elsevier;2012:171. 

23. Eagle M. Understanding cellulitis of the lower limb. Wound Essentials. 2007;2:34–44.

24. Pickwell K, Siersma V, Kars M, et al. Predictors of lower-extremity amputation in patients with an infected diabetic foot ulcer. Diabetes Care. 2015;38(5):852–857. 

25. Harker J. Wound healing complications associated with lower limb amputation. World Wide Wounds. 2006. Available at: www.worldwidewounds.com/2006/september/Harker/Wound-Healing-Complication... accessed 140816. Accessed August 14, 2016. 

26. Hedger C. Wound Essentials 3: Recognising chronic oedema and the need for intervention. Wound Essentials. 2008;3. Available at www.wounds-uk.com/pdf/content_9421.pdf. Accessed December 31, 2015. 

27. O’Meara S, Cullum N, Nelson EA, Dumville JC. Compression for venous leg ulcers. Cochrane Database Syst Rev. 2012;11:CD000265. 

28. Dow G. Bacterial swabs and the chronic wound: when, how, and what do they mean? Ostomy Wound Manage. 2003;49(5A suppl):8–13.

29. Lipsky BA, Berendt AR, Cornia PB, et al. Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis. 2012;54(12):132–173. 

30. Lavery LA, Armstrong DG, Peters EJG, Pipsky BA. Probe-to-bone test for diagnosing diabetic foot osteomyelitis. Diabetes Care. 2007;3(2):270–274.

31. Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Harkless LB, Boulton AJ. A comparison of two diabetic foot ulcer classification systems: the Wagner and the University of Texas wound classification systems. Diabetes Care. 2001;24(1):84–88.

32. Diehl KA, Allen L, French M, Driver VR. Lower extremity major and minor amputations in the high risk patient. Podiatry Manage. 2015. Available at: http://podiatrym.com/pdf/2015/aa/Diehl1115web.pdf. Accessed November 19, 2016.

33. Woodbury GM, Houghton PE, Campbell KE, Keast DH. Development, validity, reliability, and responsiveness of a new leg ulcer measurement tool. Adv Skin Wound Care. 2004;17(4):175–187. 

Potential Conflicts of Interest: none disclosed

Ms. N. Campbell was the founder; Ms. D. Campbell was the Nurse Leader (Retired); and Ms. A Turner is a staff Registered Nurse, Foot and Leg Ulcer Clinic, Vancouver Island Health Authority, British Columbia, Canada. Please address correspondence to: Andrea Turner, RN, BSN, HClSc, GNC(c); email: aturner@shaw.ca

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Abstract

Despite advances in surgical techniques and products for stoma care, stoma-related complications are still common. A retrospective analysis was performed of the medical records of 462 consecutive patients (295 [63.9%] female, 167 [36.1 %] male, mean age 55.5 ± 15.1 years, mean body mass index [BMI]  25.1 ± 5.2) who had undergone stoma creation at the Gastroenterological Surgery Clinic of Turkiye Yuksek İhtisas Teaching and Research Hospital between January 2008 and December 2012 to examine the incidence of early (ie, within 30 days after surgery) stoma complications and identify potential risk factors.

Variables abstracted included gender, age, and BMI; existence of malignant disease; comorbidities (diabetes mellitus, hypertension, coronary artery disease, chronic respiratory disease); use of neoadjuvant chemoradiotherapy; permanent or temporary stoma; type of stoma (loop/end stoma); stoma localization; and the use of preoperative marking of the stoma site. Data were entered and analyzed using statistical software. Descriptive statistics, chi-squared, and Mann-Whitney U tests were used to describe and analyze all variables, and logistic regression analysis was used to determine independent risk factors for stoma complications. Ostomy-related complications developed in 131 patients (28.4%) Of these, superficial mucocutaneous separation was the most frequent complication (90 patients, 19.5%), followed by stoma retraction (15 patients, 3.2%). In univariate analysis, malignant disease (P = .025), creation of a colostomy (P = .002), and left lower quadrant stoma location (P<.001) were all significant indicators of stoma complication. Only stoma location was an independent risk factor for the development of a stoma complication (P = .044). The rate of stoma complications was not significantly different between patients who underwent nonemergent surgery (30% in patients preoperatively sited versus 28.4% not sited) and patients who underwent emergency surgery (27.1%). Early stoma complication rates were higher in patients with malignant diseases and with colostomies. The site of the stoma is an independent risk factor for the development of stoma complication. Preoperative marking for stoma creation should be considered to reduce the risk of stoma-related complications. Prospective, randomized controlled studies are needed to enhance understanding of the more prevalent risk factors.

Many colorectal operations involve stoma formation. Despite advances in surgical techniques and products for stoma care, complications are still common; they range between 25% and 60%, affect patient quality of life, and increase the financial cost to the health system, as shown in prospective research and audits.^1-5 According to a prospective analysis of stoma-related complications (N = 408),⁶ the consequences of complications can be complex and life-threatening. 

Complications are classified as early or late. Early complications are defined as those occurring in the first postoperative month; the most common are superficial or deep stoma necrosis, retraction, mucocutaneous separation, dermatitis, bleeding, and parastomal abscess.^7-10 Late complications appear after this period and may include parastomal hernias, stenosis, or stomal prolapse.¹⁰

Patient-related and surgery-related factors contribute to the risk of stomal complications.¹¹ However, although several prospective analyses^12-15 (total number of patients = 5913) have attempted to identify definite risk factors associated with stoma complication, the results are contradictory with regard to the impact of gender, body mass index (BMI), emergency surgery, and preoperative stoma siting. 

The main purpose of the present study was to analyze the incidence of early stoma complications and determine risk factors that may predict stoma complication.

Material and Methods

Patients. After approval of the local ethical committee of Turkiye Yuksek .Ihtisas Teaching and Research Hospital, medical chart data for 462 consecutive patients admitted to the Gastroenterological Surgery Clinic for a stoma creation between January 2008 and December 2012 were collected and retrospectively analyzed. Patients undergoing both emergency and elective procedures were included in the study and compared as to gender, age, and BMI; existence of malignant disease; comorbidities (diabetes mellitus, hypertension, coronary artery disease, chronic respiratory disease); use of neoadjuvant chemoradiotherapy; permanent or temporary stoma; type of stoma (loop/end stoma); stoma localization; and the use of preoperative marking of the stoma site.

Data abstraction. Patient demographics and details of the stoma complications up to 30 days after surgery were abstracted by a stoma care nurse specializing in ambulatory care. Data were collected to a spreadsheet and entered into a software program (SPSS Inc, Chicago, IL). Patients usually were seen 2 times during the first month following surgery. Patients needing reminders for follow-up visits received a call from the stoma nurse. 

Data relevant to the incidence of stoma complications and potential risk factors associated with them as previously noted^1-18 were abstracted. The postoperative complication variable was obtained from the charts as diagnosed at that time. An early postoperative stoma complication was defined as occurring within the first 30 postoperative days. 

Statistical analysis. Data analysis was performed using SPSS 18 for Windows software (SPSS Inc, Chicago, IL), and descriptive statistics were used to summarize the data. The statistical significance of the data was evaluated by applying the Pearson’s chi-squared test for the relationship between categorical variables. The Mann-Whitney U test was used to analyze the difference between the measured values of 2 groups of patients (those undergoing emergent versus those having nonemergent surgery) after confirming with the Kolmogorov-Smirnov test whether the 2 random samples had the same statistical distribution. Logistic regression analysis was used to determine the independent risk factors for stoma complication. A P value <.05 was considered to be statistically significant.

Results

Of the 462 patients, 295 were female (63.9%) and 167 were male (36.1%); the mean age was 55.5 ± 15.1 years, and mean BMI was 25.1 ± 5.2. The BMI was <18.5 in 55 patients (11.9%), between 18.5 and ≤29.9 in 186 patients (40.3%), and ≥30 in 221 patients (47.8%). 

The most common indications for stoma creation were colorectal carcinoma (344 patients, 74.1%) and inflammatory bowel disease (56 patients, 12.1%). The most frequently performed surgical interventions were low anterior resection with diverting (loop) ileostomy (178 patients, 38.5%), followed by total colectomy with end ileostomy (71 patients, 15.3%). Other less common types of surgery and indications for stoma creation are listed in Table 1. 

Ostomy-related complications developed in 131 patients (28.4%). Superficial mucocutaneous separation was the most frequent complication (90 patients, 19.5%), followed by stoma retraction, which developed in 15 patients (3, 2%) (see Table 2). 

Age, gender, BMI, comorbidity, neoadjuvant chemoradiotherapy, emergency surgery, smoking, and preoperative site marking had no significant effect on the occurrence of stoma complication (see Table 3). However, stoma complications were significantly more likely to occur in patients with malignant (31.1%) compared to benign disease (20.3%, P = .0025) and after colostomy rather than ileostomy surgery (P = .002). The complication rate was also significantly higher in patients with a stoma located in the left lower abdominal quadrant (39%) when compared to right lower abdominal quadrant (23.1%, P = .001). 

The complication rate was 24.2% in patients with loop ileostomy, 19.2% in patients with end ileostomy, 35% in patients with loop colostomy, and 37.7% in patients with end colostomy. No significant difference was found in complication rates when comparing loop to end ileostomy (P = .341), loop colostomy (P = .206), and end colostomy (P = .803) (see Table 4).

Factors with significant differences in the rate of complications (malignant disease, creation of colostomy, and stoma location) were further analyzed in multivariate logistic regression analysis. Of these variables, the only independent risk factor was found to be the location of the stoma (P = .016), with the complication rate increasing 1.8 fold when the stoma was in the left lower rather than in the right lower abdominal quadrant (see Table 5). 

Elective and emergency surgery patients were evaluated separately for any effect of preoperative marking of the stoma location. In the elective surgery group, the complication rate was 30% in patients who underwent preoperative marking versus 28.4% in patients who were not preoperatively sited. Only 1 patient in the emergency group underwent preoperative marking; the stoma complication rate was 27.1% and did not significantly differ from the elective surgery group (P = .81) (see Table 6). 

Discussion

The present study demonstrated a high incidence (28.4%) of a variety of stoma problems, with significant risk factors identifiable for complications. In a prospective multicenter study¹³ in the UK including 3970 stomas, a strong association was noted between female gender and higher rates of stoma complications. In the present study, although the stoma complication rate was slightly higher in women (30.5%) than in men (27.1%), the difference was not statistically significant (P = .433). Obesity is frequently cited in some prospective studies^12,13 as having an impact on the development of stoma complications. In the present study, the stoma complication rate also was higher in obese patients (30, 8%). However, on comparison with nonobese  patients (BMI<30), no significant difference was found.

In the present study, the complication rate in patients with malignant disease was significantly higher than in patients with benign disease (20.3% and 31.1%, respectively). Similar results have been reported in the retrospective cohort study by Nastro et al.¹⁴

Some retrospective and prospective studies^2,19,20 including a total of 602 patients have shown the stoma complication rate is lower following ileostomy than following colostomy surgery. Similarly, in the present study, the stoma complication rate was significantly higher among patients with a colostomy than patients with an ileostomy. 

In the present study, although not statistically significant, the complication rate after loop colostomy was higher than after loop ileostomy surgery. This result is in accordance with several prospective randomized and nonrandomized studies.^21,22

A prospective study,⁸ a meta-analysis,²³ and a white paper²⁴ found stoma site is another factor affecting stoma complications. In the present study, stoma location was the only independent risk factor for the development of stoma complications. Ileostomies are ultimately created in the right lower and colostomies are usually localized in the left lower abdominal quadrant. A review by Pine and Stevenson¹⁰ found early complications such as ischemia and necrosis are more common following colostomy than ileostomy formation. Excessive tension on the bowel secondary to insufficient mobilization of the exteriorized distal portion or a large abdominal pannus in an obese patient with a narrow parietal opening through which the colon passes negatively affects the blood supply, with potential ischemic insults. In the retrospective study by Hsu et al,²⁵ risk factors significantly associated with early complications were stoma location, diameter, and height,  as well as peristomal skin condition. Furthermore, in logistic regression analysis, these authors also found stoma diameter and stoma height were predictors for the incidence of early complications. According to several randomized and nonrandomized studies,^22,26,27 higher enlargement capacity and intraluminal pressure of the colon leads to more frequent stoma herniation in the long term, but it also brings a higher risk of incisional hernia after colostomy than after ileostomy closure.

The results of the present study show comorbidity, neoadjuvant chemoradiotherapy, type of surgical procedure, and smoking had no significant effect on the development of stoma complication.

Several retrospective studies^27-31 have demonstrated preoperative marking of the site for stoma creation can reduce the complication rate and facilitate optimal stoma care for the patient during everyday activities. In the present study, only 13.2% of the patients underwent preoperative marking but no significant statistical difference was noted in the rate of stoma complications when persons with and without presurgical marking were compared. This may be a reflection of the small sample size. However, the authors recommend preoperative marking, which they have used routinely in their clinic in recent years.

Limitations

The present study has some limitations. First, because it is retrospective in nature, the data may have inherent flaws unknown to the current researcher. Secondly, stomas were created by different surgeons, which may have had an effect on the complication rates. 

Conclusion

The results of a retrospective review of patient data indicate early stoma complication rates are higher in patients with malignant diseases and after the creation of colostomies and permanent stomas. The site of the stoma is an independent risk factor for the development of stoma complication. Preoperative marking for stoma creation should be considered to reduce the risk of stoma-related complications. Prospective, randomized controlled studies to enhance understanding of the factors influencing stoma complication rates are warranted. 

Acknowledgment

The authors are grateful to Claire Olmez, BEd, MSc for proofreading of and language corrections to the manuscript.

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9. Lindholm E, Persson E, Carlsson E, Hallén AM, Fingren J, Berndtsson I. Ostomy-related complications after emergent abdominal surgery: a 2-year follow-up study. J Wound Ostomy Continence Nurs. 2013;40(6):603–610. 

10. Pine J, Stevenson L. Ileostomy and colostomy. Surgery (Oxford). 2014;32(4):212–217.

11. Hendren S, Hammond K, Glasgow SC, et al. Clinical practice guidelines for ostomy surgery. Dis Colon Rectum. 2015;58(4):375–387. 

12. Arumugam PJ, Bevan L, Macdonald L, et al. A prospective audit of stomas – analysis of risk factors and complications and their management. Colorectal Dis. 2003;5(1):49–52.  

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Potential Conflicts of Interest: none disclosed

Dr. Koc is an Associate Professor, Antalya Teaching and Research Hospital, Department of General Surgery, Antalya, Turkey. Dr. Karaman is an Associate Professor, Sakarya University Faculty of Medicine, Department of General Surgery, Sakarya, Turkey. Dr. Gomceli is an Associate Professor, Antalya Teaching and Research Hospital. Dr. Dalgic is a gastrointestinal surgeon; and Dr. Ozer and Dr. Ulas are Associate Professors, Turkiye Yuksek Ihtisas Teaching and Research Hospital, Department of Gastroenterological Surgery, Ankara, Turkey. Dr. Ercan is an Associate Professor; and Dr. Bostanci and Dr. Akoglu are Professors, Sakarya University Faculty of Medicine, Department of General Surgery. Please address correspondence to: Dr. Umit Koc, Antalya Eğitim ve Araştırma Hastanesi, Varlık Mah, Kazım Karabekir Caddesi, 07100 Soğuksu /Muratpaşa/Antalya Turkey; email: drumitkoc@gmail.com. 

Abstract

Patient experiences pre- and post-ileostomy creation as a result of severe Crohn’s Disease are underresearched. A qualitative phenomenological design involving a purposeful sampling approach was used to capture the lived physical and psychosocial transition of patients with Crohn’s Disease before and after ileostomy formation.

Patients were recruited from the membership of the United Kingdom Ileostomy Association; inclusion criteria stipulated participants must speak English and have a diagnosis of Crohn’s Disease and subsequent stoma formation. Ten (10) patients (6 women, 4 men, ranging in age from 34 to 83 years with Crohn’s Disease and an ileostomy [mean time with stoma 18.3 years, range 3–36 years]) participated in indepth, semistructured interviews with questions on sociodemographic characteristics along with questions informed by the relevant literature regarding life before and after the ileostomy. All interviews were audiorecorded and transcribed verbatim. Interpretative phenomenological analysis was used to examine the data and identify and interpret themes. Participants were asked to comment on these themes to ensure they were a realistic interpretation of their experiences. Two (2) major themes emerged that embodied ileostomy formation: being controlled by Crohn’s and transition to a new life with an ileostomy. Crohn’s symptoms controlled daily activities such as work and socializing due, in part, to the need to be in close proximity to toilet facilities. The ileostomy facilitated a transition to a new life that allowed patients to re-engage with work and social activities. One minor theme emerged: memories of Crohn’s. Participants said their memories of Crohn’s affected life with an ileostomy. Where Crohn’s controlled every aspect of people’s lives pre-ileostomy formation, the creation of the ileostomy was a positive experience because it helped manage Crohn’s symptoms. Memories of life pre-ileostomy may affect individuals’ behavior post-ileostomy formation. In order to offer appropriate support, health professionals may need to be more aware that having Crohn’s may affect patient behavior post-ileostomy.