Abstract

Despite advances in reconstruction techniques, sacral pressure ulcers continue to present a challenge to the plastic surgeon. The flap from the gluteal crease derives blood supply from the inferior gluteal artery perforator (IGAP) and reliably preserves the entire contralateral side as a donor site. To incorporate the IGAP in the reconstruction of sacral pressure ulcers, a skin paddle over the gluteal crease was created and implemented by the authors.

Data from 11 patients (8 men, 3 women; mean age 67 [range 44–85] years old) whose sacral ulcers were closed with an IGAP flap between June 2006 and May 2012 were retrieved and reviewed. All patients were bedridden; 1 patient in a vegetative state with a diagnosis of carbon monoxide intoxication was referred from a local clinic, 2 patients had Parkinson’s disease, and 8 patients had a history of stroke. The average defect size was 120 cm² (range 88–144 cm²). The average flap size was 85.8 cm² (range 56–121 cm²). Only 1 flap failure occurred during surgery and was converted into V-Y advancement flap; 10 of the 11 flaps survived. After surgery, the patients’ position was changed every 2 hours; patients remained prone or on their side for approximately 2 weeks until the flap was healed. After healing was confirmed, patients were discharged. Complications were relatively minor and included 1 donor site wound dehiscence that required wound reapproximation. No surgery-related mortality was noted; the longest follow-up period was 24 months. In this case series, flaps from the gluteal crease were successfully used for surgical closure of sacral pressure ulcers. This flap design should be used with caution in patients with hip contractures. Studies with larger sample sizes are needed to ascertain which type of flap is best suited to surgically manage extensive pressure ulcers in a variety of patient populations. 

Managing sacral pressure ulcers is a common problem for reconstructive surgeons. Local flaps created from the gluteal region are preferred when wound closure is needed due to their reliability and short learning curve for surgeons. Gluteal muscle perforator-based flaps have been used to cover sacral defects for more than 10 years. This flap construct has become increasingly popular because of its versatility and low incidence of donor site complications.^1-3

Three types of flaps involving the gluteal crease based on different terminal branches of the inferior gluteal artery have been described in the literature: the infragluteal flap,⁴ the inferior gluteal artery perforator (IGAP) flap,^5,6 and the inferior gluteal artery myocutaneous flap.⁷ Many clinicians harvest free flaps from the gluteal crease region for breast reconstruction because of its fatty composition.^4-6 Gluteal crease flaps also provide positive aesthetic results for both the breast reconstruction and donor site scar without sacrificing muscle at a donor site. According to the case studies of Scheufler et al⁸ (N = 13) and Higgins et al’s case report,⁹ gluteal crease flaps also may be harvested for ischial pressure ulcer coverage.^8,9

Two mechanisms contribute to pressure ulcer development: external pressure that compresses blood vessels and friction and shearing forces that tear and injure blood vessels. The sacral pressure ulcer is susceptible to recurrence if the underlying mechanisms are not addressed.

In the authors’ facility, a local, unilateral, gluteus maximus myocutaneous advancement flap is the usual choice for sacral defects. Gluteus maximus myocutaneous flap surgery is technically easy to perform. However, the gluteus maximus muscle should be partially split to allow for advancement of the flap and tension-free closure, which introduces the potential for gait instability in an ambulatory patient. The derived flap seldom crosses the midline of the gluteal region; a bilateral gluteus maximus myocutaneous advancement flap is needed for larger defects.¹

The purpose of this case study is to describe the outcomes of patients in whom a gluteal crease flap was used for reconstruction of sacral pressure ulcers.

Patients and Methods

The authors treated 350 sacral pressure ulcers in 289 total patients with 332 flaps from June 2006 to May 2012 in the Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan. From among these, they retrospectively analyzed the 11 patients (8 men, 3 women; mean age 67 [range 44–85] years old) whose sacral pressure ulcers had been reconstructed using IGAP flaps. The IRB committee of Tri-Service General Hospital approved all procedures for obtaining informed consent, reviewing records, and publishing data and photographs. All defects contained extensive destruction, tissue necrosis, and/or damage to muscle, bone, or supporting structures with or without full-thickness skin loss, a stage IV pressure ulcer according to the definition developed by Shea.¹⁰ All patients were bedridden; 1 patient was in a vegetative state following carbon monoxide poisoning, 2 patients had Parkinson’s disease, and the remaining 8 patients had a history of stroke. The patient summary is shown in Table 1. 

Surgical procedure. Surgical repair of the defect was performed with the patient in a prone position under general anesthesia. The surgical field was sterilized, the sacral pressure ulcer was debrided, and the bony prominence of the sacral bone was removed using an osteotome. The wound then was covered with epinephrine-soaked gauze, and the defect size was measured. An elliptical flap was created from the gluteal crease region; the authors’ preference is to harvest the flap from the side closest to the sacral pressure ulcer if the ulcer is not centrally located, according to the recommendations of Scheufler et al⁸ and Higgins et al.⁹ The axis of the flap was fashioned along the natural gluteal crease, the length of the flap was determined according to the vertical length of the defect, and the width of the flap was 3–5 cm less than the horizontal width of the defect so as not to interfere with flap inset as well as to facilitate donor site closure (see Figures 1, 2). The incision was made along the inferior flap margin to identify the inferior border of the gluteus maximus muscle. The length of the dissected pedicle was determined by the arc of movement of the flap.

Care was taken to identify the cutaneous branch from the descending branch of the inferior gluteal artery at the inferior margin of the gluteus maximus muscle. If the descending branch was of suitable size (>12 mm), the cutaneous branch was isolated and traced along the descending branch toward the origin of the inferior gluteal artery. If the cutaneous branch was absent or too small, the superior margin of the flap was incised. The incision was carried down to the subfascial level, and subfascial dissection was performed caudally to identify the myocutaneous perforator of the inferior gluteal artery. If the perforator was of adequate size (>1–2 mm), intramuscular dissection of the perforator was performed, and the vessel was traced proximally. The flap then was elevated and transferred to the defect either through a subcutaneous tunnel or by incising the skin between the flap and the sacral defect. The flap was set into the defect without tension or twisting on the pedicle. Usually, the flap is rotated 90˚ using the horizontal length of the flap to approximate the vertical length of the defect.

After surgery, vital signs were monitored every 4 hours in unstable patients and every 8 hours in stable patients. The incision and dressing were monitored for signs of infection, and the amount of drainage was noted. Wet gauze dressing changes were performed using sterile technique throughout the hospitalization, and patients’ positions were changed every 2 hours. Some patients were placed on air-fluidized beds to decrease the frequency of patient repositioning. Patients were instructed to lay in the supine position during the day and to remain prone at night for approximately 2 weeks until the flap healed, after which they were discharged to a nursing facility or returned home. Patients were instructed to transition to full supine bed rest 4 weeks after surgery and continue this until wound healing without dehiscence was achieved.

Patients were reexamined and the wound photographed every week in the outpatient department; alternatively, telephone interviews were conducted by the authors’ medical staff if the patients did not return for follow-up.

Results

The average defect size was 120 cm² (range 88–144 cm²). The average flap size was 85.8 cm² (range 56–121 cm²). Seven (7) flaps were harvested from the left gluteal crease region and 4 from the right gluteal crease region. Although venous congestion commonly caused flaps to become purple and swollen immediately following surgery, 10 flaps survived completely and achieved wound healing without complications. One patient (patient 6) suffered a traction injury to the pedicle during the transfer of the flap through the subcutaneous tunnel; the flap was abandoned and immediately converted to a local gluteus maximus myocutaneous advancement flap. The skin between the sacral pressure ulcer and the donor site was incised for flap transfer in 3 patients; in 8 patients, the flaps were transferred through a subcutaneous tunnel. One wound dehiscence (patient 5) occurred over the donor site, requiring further wound reapproximation. No surgery-related mortality was noted. The longest follow-up was 24 months. No adverse outcomes were noted, but 1 pressure ulcer recurred (patient 2) 5 months after surgery (see Table 1).

Two case reports of the patients studied, exemplifying the use of IGAP flaps, are presented.

Case Reports

Patient 3. Mr. Q was an 85-year-old man who had been bedridden for 2 years due to a cerebrovascular accident. A grade IV sacral pressure ulcer developed 3 months before admission to the authors’ facility. Surgical debridement created an 11 cm x 10 cm defect, and a flap of corresponding size was designed from the left gluteal crease. During surgery, the cutaneous branch from the descending branch of inferior gluteal artery was identified, and the flap was harvested and transferred to the sacral region (see Figure 3). After surgery, the gauze dressing was changed daily to keep the wound clean; a single closed suction drain was used to monitor excessive bleeding from beneath the flap. Mr. Q was repositioned every 2 hours to prevent pressure ulcer development at other sites, pressure necrosis of the flap, or wound dehiscence. In addition, clinicians took steps to keep excess moisture and fecal contamination away from the wound by checking the wound dressings every 2 hours during repositioning. At 3 months post-surgery, the sacral defect was almost completely healed (ie, without wound dehiscence, discharge, and infection), and Mr. Q was left with an inconspicuous scar over the natural gluteal crease (see Figure 4). 

Patient 10. Mr. K was a 69-year-old man who had been bedridden for 3 years before admission following an ischemic cerebrovascular accident. A grade IV pressure ulcer was present over his sacral region, resulting in a 10 cm x 10 cm defect after 2 debridements. A 10 cm x 7 cm flap was designed at the right gluteal crease to cover the defect (see Figures 5, 6, 7). After surgery, the gauze dressing was changed daily to keep the wound clean; a single closed suction drain was used to monitor excessive bleeding from beneath the flap. At his 5-month follow-up visit, both the sacral wound and gluteal wound were healing without ulcer recurrence.

Discussion

Managing sacral pressure ulcers is a common task for reconstructive surgeons. Several types of flaps have been developed to cover sacral pressure ulcers.^1,11-14 Coskunfirat et al¹³ presented the largest case series in the literature, with 32 gluteal artery perforator flaps for pressure ulcer reconstruction. The perforator flap provides a reliable fasciocutaneous flap for sacral pressure ulcer closure and spares the underlying muscle. However, according to Coskunfirat et al’s¹³ study, unlike other gluteal perforator flaps, the unpredictable perforator artery location often necessitates a change of flap design intraoperatively.

Harvesting the flap is technically demanding. Creating the IGAP flap involves a dissection of the perforator penetrating the gluteus maximus muscle underneath the piriformis muscle. By separating the dissected pedicle for an island flap, the defect site can be replaced without any tension on the flap. Using the flap from the gluteal crease has several advantages.^5-9 First, the constant circulation always ensures successful flap harvesting from the gluteal crease despite having only tiny (<1–2 mm) perforators. Coskunfirat et al¹³ suggest this flap can be used as a primary choice in sacral pressure ulcer coverage; Doppler has been found to be unreliable in detecting perforators in the gluteal region, and the perforator is typically identified directly through subfascial dissection.¹³ Second, according to case-control studies,^7,8 the infragluteal perforator flap minimizes donor-site morbidity by sparing the gluteal muscles and eliminating the need for primary closure of the donor site; the resulting scar avoids maximal pressure zones over bony prominences. This is beneficial for ambulatory patients for walking or sitting; however, most of the patients in the current study were bedridden. Third, the IGAP minimizes donor site morbidity by sparing the gluteal muscle and primary closure of the donor site, leaving a scar that avoids maximal pressure zones over bony prominences and allowing the scar to remain well hidden in the natural gluteal crease.⁸ Fourth, in the event of a recurrent ulcer or flap failure, the flap can be raised from an area other than the previous operative site; this technique provides a secondary option for salvage in such cases, as described in the case control study of Higgins et al.⁹

The major disadvantage of this flap is vascular variation. According to a large case series (N = 118),¹⁴ the descending branch of the inferior gluteal artery is present with variable prevalence.^8,14 In the Windhofer et al¹⁴ study, the descending branch was present in 91.5% of patients. When the descending branch was absent, the cutaneous branch came from the medial or lateral circumflex femoral artery or as a perforator of the deep artery of the thigh.

Hip contracture occurs frequently in the long-term bedridden patient.¹⁵ This increases wound tension over the donor site and increases the chance of wound dehiscence. In the current patient series, wound dehiscence of 1 donor site occurred in a patient with hip contracture. In addition, hip flexion might cause undue tension on the flap pedicle, requiring caution in a patient with hip contracture. During the postoperative care period, the caregiver should prevent overflexion of the hip joint for at least 2 weeks. An added consideration is the relatively technical nature of flap creation owing to the demands of intramuscular dissection.

Using the gluteal perforator flap is controversial because published anatomical studies state the blood supply to the gluteal skin is inadequate. In their case control study, Ahmadzadeh et al¹⁶ performed a detailed dissection of the gluteal region and determined the vascular territory of a single perforator from the inferior gluteal artery is approximately 24 cm². However, Koshima et al’s¹⁷ case-control study demonstrated a flap in the gluteal region can be nourished even by a single perforator; similarly, Nojima et al’s¹⁸ case-control study reported a vascular territory of mean size of 15 cm x 12 cm in the superior gluteal artery perforator flap can be nourished using single perforator with the dye injection method. Skin in the gluteal region also has been shown to be richly vascularized with perforators connected by long and voluminous subcutaneous anastomoses.¹⁸ In light of these factors, the authors of the current study concluded the determinant factor for flap size is whether the donor site can be primarily closed.

Limitations

As with all case studies, the outcomes described cannot be generalized to other patient populations. Although the IGAP flaps were found to be reliable and provided a viable option for primary sacral pressure ulcer reconstruction, the flaps should be used with caution in patients who may be at risk for an ischial pressure ulcer (eg, wheelchair users).

Conclusion

Sacral pressure ulcer management is challenging in plastic surgery, and patients and flaps both must be carefully selected. In this case series, the IGAP flap was found to be reliable and provided a viable option for primary sacral pressure ulcer reconstruction. Other advantages included minimal blood loss, mild donor site morbidity, and preservation of muscle function. Similar to other perforator flaps, pedicle dissection must be meticulous to avoid damaging the perforator vessels. The flap is raised from an area different from the previous operation site and can serve as a secondary option in difficult cases, such as a recurrent ulcer or flap failure. Studies with larger sample sizes are needed to ascertain which type of flap is best suited to surgically manage extensive pressure ulcers in a variety of patient populations. n

References

1.         Ohjimi H, Ogata K, Setsu Y, Haraga I. Modification of the gluteus maximus V-Y advancement flap for sacral ulcers: the gluteal fasciocutaneous flap method. Plast Reconstr Surg. 1996;98(7):1247–1252.

2.         Wong CH, Tan BK, Song C. The perforator-sparing buttock rotation flap for coverage of pressure sores. Plast Reconstr Surg. 2007;119(4):1259–1266.

3.         Balakrishnan C, Brotherston TM. Transverse lumbar flap for sacral bed sores. Plast Reconstr Surg. 1992;89(5):998–999.

4.         Papp C, Windhofer C, Gruber S. Breast reconstruction with the fasciocutaneous infragluteal free flap (FCI). Ann Plast Surg. 2007;58(2):131–136.

5.         Beshlian KM, Paige KT. Inferior gluteal artery perforator flap breast reconstruction. Am J Surg. 2008;195(5):651–653.

6.         Allen RJ, Levine JL, Granzow JW. The in-the-crease inferior gluteal artery perforator flap for breast reconstruction. Plast Reconstr Surg. 2006;118(2):333–339.

7.         Hurwitz DJ. Closure of a large defect of the pelvic cavity by an extended compound myocutaneous flap based on the inferior gluteal artery. Br J Plast Surg. 1980;33(2):256–261.

8.         Scheufler O, Farhadi J, Kovach SJ, Kukies S, Pierer G, Levin LS, Erdmann D. Anatomical basis and clinical application of the infragluteal perforator flap. Plast Reconstr Surg. 2006;118(6):1389–1400.

9.         Higgins JP, Orlando GS, Blondeel PN. Ischial pressure sore reconstruction using an inferior gluteal artery perforator (IGAP) flap. Br J Plast Surg. 2002;55(1):83–85.

10.       Shea JD. Pressure sores: classification and management. Clin Orthop Relat Res. 1975;(112):89–100.

11.       Heywood AJ, Quaba AA. Modified gluteus maximus V-Y advancement flaps. Br J Plast Surg. 1989;42(3):263–265.

12.       Lee HB, Kim SW, Lew DH, Skin KS. Unilateral multilayered musculocutaneous V-Y advancement flap for the treatment of pressure sore. Plast Reconstr Surg. 1997;100(2):340–345.

13.       Coskunfirat OK, Ozgentas HE. Gluteal perforator flaps for coverage of pressure sores at various locations. Plast Reconstr Surg. 2004;113(7):2012–2017.

14.       Windhofer C, Brenner E, Moriggl B, Papp C. Relationship between the descending branch of the inferior gluteal artery and the posterior femoral cutaneous nerve applicable to flap surgery. Surg Radiol Anat. 2002;24(5):253–257.

15.       Vanwanseele B, Lucchinetti E, Stüssi E. The effects of immobilization on the characteristics of articular cartilage: current concepts and future directions. Osteoarthritis Cartilage. 2002;10(5):408–419.

16.       Ahmadzadeh R, Bergeron L, Tang M, Morris SF. The superior and inferior gluteal artery perforator flaps. Plast Reconstr Surg. 2007;120(6):1551–1556.

17.       Koshima I, Moriguchi T, Soeda S, Kawata S, Ohta S, Ikeda A. The gluteal perforator-based flap for repair of sacral pressure sores. Plast Reconstr Surg. 1993;91(4):678–683.

18.       Nojima K, Brown SA, Acikel C, Arbique G, Ozturk S, Chao J, et al. Defining vascular supply and territory of thinned perforator flaps: part I. Anterolateral thigh perforator flap. Plast Reconstr Surg. 2005;116(1):182–193.

Potential Conflicts of Interest: none disclosed. The Civilian Administration Division of Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan funded the project.

Dr. Lin and Dr. Ou are attending physicians; Dr. Chiao, Dr. Wang, and Dr. Chou are resident physicians; and Dr. Chen and Dr. Lee are attending physicians, Division of Plastic and Reconstructive Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan. Please address correspondence to: Tzu-Peng Lee, MD, Division of Plastic and Reconstructive Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, No. 325, Section 2, Cheng-Gung Road, Taipei, 11490, Taiwan; email: aarondakimo@yahoo.com.tw.

Abstract

Pressure ulcers do not develop only in areas with bony prominences; they can develop in any tissue under pressure, including pressure exerted by medical devices. A prospective, descriptive study was conducted from December 15, 2013 to March 25, 2014 to determine the prevalence, risk factors, and characteristics of medical device-related hospital-acquired pressure ulcers (MDR HAPUs) among all patients  (N = 175) in 5 adult intensive care units (ICUs) in a university hospital in Turkey.

The previously established point prevalence of hospital-acquired pressure ulcers (HAPUs) in these ICUs was 15%. Patients were evaluated in the first 24 hours after admission and observed 6 times thereafter in intervals of 48 hours. Demographic (eg, age, gender, body mass index) and medical device-related pressure ulcer data (eg, location, device type, stage), and Braden Scale scores were collected and analyzed; frequencies and percentages were calculated and Mann-Whitney U Test, t-test, and odds ratios were applied. Twenty-seven (27) patients (15.4%) developed nonMDR HAPUs and 70 (40.0%) developed MDR HAPUs. MDR HAPUs occurred most frequently (45.0%) in patients with an endotracheal tube. The most frequent type (42.6%) was Stage II. The highest rates of MDR HAPUs were observed among internal medicine ICU patients (OR 7.041), patients who also had a nonMDR HAPU (OR 6.6), patients in the high Braden risk score group (OR 1.8), or patients who received enteral feeding (OR 2.12). Because of the high rate of MDR HAPUs noted, policies and procedures aimed at preventing medical device-related pressure ulcers are needed. 

Despite advancements in medical treatment, care, and technology, pressure ulcers (PUs) remain an important health problem worldwide.^1,2 PUs commonly occur at bony prominences such as the sacrum or heels,³ but recent research shows PUs also occur in mucous membranes and skin lying over soft tissue. Because of external pressure on the tissue on which they are positioned, medical devices such as nasal cannulas, endotracheal tubes (ETs), and continuous positive airway pressure (CPAP) masks cause tissue damage, resulting in medical device-related pressure ulcers (MDR PUs).^3,4 Despite numerous studies on PUs,^1,5-8 studies on MDR hospital-acquired pressure ulcers (HAPUs) are limited in number.^3,4,9 The proportion of MDR HAPUs to general PUs reported in these studies is high: a cross-sectional point prevalence study³ conducted on 2,178 patients in the United States to determine PU incidence and prevalence reported the overall prevalence of MDR HAPUs was 34.5%, one third of all PUs reported in this study.

A variety of medical devices can cause MDR HAPUs. In a prospective, clinical evaluation study (N = 166) by Davis et al¹⁰ among patients wearing a cervical collar <5 days, 33% developed MDR PUs; among patients whose wear time exceeded 5 days, 44% developed MDR PUs. A nonexperimental, descriptive study¹¹ conducted on 148 trauma patients reported wearing a cervical collar for >2 days is the second most important cause of skin damage (23.7%) and the tracheostomy-related PU rate is 10.5%.

In a prospective, descriptive study by Wille et al¹² involving 125 surgical intensive care unit (ICU) patients attached to pulse oximeter probes, 6 (5%) developed a device-related ulcer. In Jaul’s¹³ cohort study of patients treated at a psychogeriatric inpatient health care facility (N = 174), 166 atypical PUs were observed, of which 23 (35%) were related to medical devices.

Due to their immobility, sensory perception loss, and insufficient circulation, patients receiving care in an ICU are at high risk of developing PUs.³ ICU patients generally receive treatment involving multiple medical devices more than nonICU patients.^2,14,15 ICU patient characteristics increase their vulnerability to the numerous medical devices used during treatment. The different degrees of pressure exerted by the medical device and the tolerance level of the patient’s skin also affect PUs occurrence.³ PUs reduce patient quality of life and increase treatment costs; upon discharge from ICU, recovery from PUs may take several months.^6,16,17

Many medical devices such as nasal cannulas, oxygen masks, ETs, CPAP masks, nasogastric (NG) tubes, Foley catheters, peripheral oxygen saturation of hemoglobin (SpO₂) probes, blood pressure (BP) cuffs, cervical collars, and splints are used for the treatment and monitoring of patients in ICUs.^3,4 These devices exert pressure on the tissue on which they are positioned and cause changes  in  tissue humidity and temperature. The increase in temperature and moisture between the medical device and skin causes microchanges in the skin.^3,4 Moreover, the moisture that occurs causes the skin to become more susceptible to compromise³; furthermore, a medical device attached to the skin may hinder assessment of the skin beneath it.³ The materials used to fasten the devices compress the tissue, can disturb the blood and lymph circulation, and cause edema. All of these factors are thought to increase the risk for MDR HAPUs.^3,4,9

For effective treatment, a health problem needs to be diagnosed at an early stage and available preventive measures must be implemented.⁵ Nurses need to be vigilant in preventing MDR HAPUs in ICU patients. As with nonMDR HAPUs, nurses play an important role in MDR HAPU prevention. When MDR HAPUs are prevented, the prevalence and incidence rates of HAPUs will be reduced as well.³

As far as the authors could determine, no publication is available on the rate of MDR PUs in Turkey. The purpose of this prospective, descriptive study was to address the following research questions:

1.         What is the prevalence of MDR HAPUs in ICUs?

2.         What are the characteristics of MDR HAPUs?

3.         What are the risk factors for MDR HAPUs?

Methods

Ethical considerations. This study was conducted according to the ethical guidelines and principles of the International Declaration of Helsinki. Before the study, the approval of Gazi University Faculty of Medicine Ethics Board for Non-invasive Clinical Research was obtained. Written consent was obtained from the chairpersons of the departments of the relevant ICUs included in the study via the Gazi University Health Research and Application Center Directory. During the study, conscious patients were informed about the aim of the study and their oral consent to participate was obtained. Unconscious patients were consented via their guardians.

Study setting and sample. The research sample consisted of anesthesia reanimation, cardiovascular surgery, internal medicine, neurosurgery, and thoracic disease patients treated in the 5 ICUs. The literature reports patients treated in ICUs are at high risk of developing PUs^2,3,14,15 and that ICUs are among the units with the highest PU rates.^4,9,16,17 Moreover, more medical devices are used in the treatment and monitoring of patients in ICUs  than nonICUs,^3,4 guiding the choice of patient sample.

To determine which ICUs should be included in the study sample, the hospital’s 2012 PU point prevalence records were examined; these records showed PU prevalence rates were 100% in the anesthesia-reanimation, 71.4% in the thoracic diseases and surgery, 43.9% in internal medicine, 42.9% in the neurosurgery, and 16.7% in the cardiovascular surgery ICUs.¹⁸ Following expert opinion, the other units, including neurology, general surgery, and coronary ICUs, with PU prevalence rates below 15% were excluded from the study.

The number of participants was determined using the following formula¹⁹:

where n = number of individuals to be sampled, p = frequency of incidence occurrence (probability), q = frequency of nonobservance of the phenomenon (1-p), t = theoretical value t from the table at a certain standard error and degree of freedom, and d = the standard deviation from incidence frequency. When numerical values were inserted, P = 0.11.

A review of the literature^3,10-13  revealed MDR HAPU prevalence rates range between 5% and 44%. Based on these data, a statistician suggested setting the frequency of incidence occurrence at 11%: q = 0.78,  t = 1.96, d =0.05 (± 5% deviation was desired), (1.96)² x 0.11 x 0.89/(0.05)², n = 150. According to this formula, the sample size was calculated to be 150.

Data collection. Data were collected using the systematic observation method. To obtain the data, a Patient Characteristics Form, an MDR PU Form, the Braden Scale for Predicting Pressure Ulcer Risk, and the Pressure Ulcer Staging Form were used. Forms were completed by the researcher, a certified stoma and wound nurse.

Patient characteristics. The patient characteristics form was developed by the researchers based on the literature.^1,3,20,21 The form consisted of 25 items regarding demographic information (eg, gender, age, body mass index [BMI]) and information on health conditions (eg, diagnosis, accompanying diseases, nutrition).

PU characteristics. The MDR PU form was developed based on the literature^{3,4,9,13,21,22} and included 5 questions regarding PU characteristics (eg, occurrence of nonMDR HAPU and MDR PU), as well as the observations and related information such as type of medical device, PU location on the body, and PU stage obtained at each observation. To facilitate the data recording, the form included codes to refer to medical device, body site, and ulcer stage. Both the patient characteristics and PU forms were developed specifically for and used for the first time in this study.

PU risk. The Braden Scale for Predicting Pressure Ulcer Risk was used to assess the risk of PUs. The total possible score on the scale ranges from 6 to 23. Accordingly, a score of 12 points or lower indicates very high risk, 13–14 points high risk, and 15–16 points low risk. For patients 75 years and older, 15–18 points is considered low risk for PU.²³

PU staging. PU staging was based on the National Pressure Ulcer Advisory Panel/European Pressure Ulcer Advisory Panel²⁴ (NPUAP-EPUAP) staging system standards of 2009. The stages include Stage I, Stage II, Stage III, Stage IV, unstageable, and suspected deep tissue injury.

Procedure. After obtaining the necessary approval and consent of the Hospital Directorate (IRB-equivalent), a pilot study was conducted with 15 patients from the cardiovascular surgery, internal medicine, neurosurgery, and thoracic surgery ICUs to determine the applicability and comprehensibility of the data collection forms. No changes were made to the forms after pilot study. In a prospective, cross-sectional study conducted in ICUs in the US and Australia, Coyer et al⁴ found MDR PUs developed within 3 to 13 days following admission to the unit; therefore, data for the study were collected from patients newly admitted (<24 hours) to the ICUs included in the study. Patients then were observed for PUs at 48-hour intervals. Data collection took place between November 15, 2013 and March 25, 2014.

Each study participant was examined at least once to a maximum of 6 times (2 weeks). Once a person was examined 6 times, data collection stopped, even if he/she was not discharged from the ICU. Assessment of MDR PUs was limited to only those body sites to which a medical device was attached at the first examination. Any information regarding any medical device attached to the patient after the initial examination was disregarded.

Examination. The patient’s skin was evaluated completely from head to toe, paying special attention to bony prominences, and the tissue under and around all attached medical devices was examined and palpated. Removing devices that can be unattached for a short period of time, such as oxygen masks, nasal cannulas, and SpO₂ probes, allowed for examination of the tissue underneath. Using the Braden Scale, the patient’s PU risk was assessed; staging information was recorded for patients who had developed PUs. BMI data were grouped according to the World Health Organization²⁵ (WHO) classification criteria. Accordingly, low BMI was considered <18.50, normal BMI 18.50–24.99, heavy BMI 25.00–29.99, and obese 30.00.

Data analysis. The data obtained from each patient were coded and entered into Statistical Packages for Social Sciences (SPSS) by the researcher. Data were stored according to research and publishing ethics and analyzed using SPSS for Windows, Version 20.0 (SPSS Inc, Chicago, IL, USA).The frequency and percentage distributions of the items pertaining to patient characteristics information were calculated. Group differences were evaluated using the normality test, and the Mann Whitney U test was used for paired group variables exhibiting nonnormal distribution. To evaluate the relationship among variables, the chi-square (²) and Fisher exact tests were used. The statistical significance level was determined to be 0.05, and significant differences among groups were observed when P <0.05. Data for risk factors were presented as crude or adjusted odds ratios (ORs) with 95% confidence intervals (95% CI).

Results

Patient demographics. From the 5 participating ICUs, 175 persons were assessed. Participant mean age was 62.50  ± 16.67 years, average BMI was 26.49 ± 5.26, and 57.1% of the patients were men. ICU breakout included internal medicine (26.2%), cardiovascular surgical (24.5%), and neurosurgical (23.4%). The most common primary patient diagnoses were cardiovascular (28.0%) and neurological (28.0%) system diseases. Prescribed medications included antibiotics (79.4%), steroids (56.0%), and anticoagulant medication (53.7%); 39.4% received oral feeding and 36.0% were attached to mechanical ventilation (see Table 1). 

Ulcer data. Of the 175 patients included in the study, 27 (15.4%) developed nonMDR HAPUs, 70 (40.0%) developed MDR HAPUs, 16 (9.1%) developed pre-ICU nonMDR PUs, and 14 (8.0%) developed pre-ICU MDR PUs (see Table 2). 

Of the 175 participants, 70 (40%) developed a total of 211 device-caused MDR HAPUs, which were caused by ETs (95, 45.0%), CPAP masks (22, 10.4 %), SpO₂ probes (17, 8.0%), oxygen masks (15, 7.1 %), and nasal cannulas (14, 6.6%). No MDR HAPUs were observed in patients with orogastric tubes, cervical collars, splints, and percutaneous endoscopic gastrostomy tubes (see Table 3). 

The MDR HAPU stages encountered were assessed initially as Stage II (42.6%), Stage I (37.9%), unstageable (17.5%), and suspected deep tissue injury (1.9%) (see Figure 1). In terms of MDR HAPU rate, the difference in the observations between 11.8% and 60.2% was found to be statistically significant (P <0.05). The rate of MDR PUs at Stage I (1.2%), Stage II (3.3%), and unstageable (2.7%), determined at the first screening, increased to 60.0%, 67.7%, and 64.8%, respectively, at the sixth observation. 

MDR PUs occurred on the lips (44.0%), nose (15.6%), fingers (7.5%), ears (6.1%), and other sites (17.6%) (see Figure 2). 

Risk factors. Generally, patients that developed nonMDR HAPUs were 6.60 times more likely to develop MDR HAPUs; specifically, patients in the internal medicine, neurosurgery, and thoracic disease ICUs were, respectively, 7.04, 6.22, and 6.01 times more likely to increase MDR HAPUs risk, a statistically significant difference (P <0.05). Moreover, for enterally fed patients, PU risk increased 2.12 times and as the Braden risk score moved from low to high risk, MDR HAPU risk increased 1.81 times (P <0.5).

Although not statistically significant, MDR HAPUs occurred 1.23 times more often in male patients, 2.07 times more in patients attached to a mechanical ventilator, 2.07 times more in patients on anticoagulants, and 2.56 times more in patients receiving sedation. Although not statistically significant, MDR HAPU development was 1.02 higher as age increased and 1.17 higher as hemoglobin levels dropped (P >0.05) (see Table 4). 

Length of stay. In this study, 340 (60.2%) of MDR HAPUs developed with a total of 211 devices. More MDR HAPUs developed as the number of days in hospital increased: 11.8% occurred during the first 24 hours (7/59 sites); on the fourth day, the number of occurrences rose to 48.0% (37/77 sites) and on the eleventh day to 82.3% (215/261 sites) (P <0.05)  (see Table 5). 

Discussion

Prevalence. The prevalence rate for MDR HAPUs in this study was 40.0% — approximately 1 in 2 patients admitted to an ICU developed a MDR HAPU. This rate was higher than nonMDR HAPUs prevalence (15.4%), which corresponds to the findings in the relevant literature. In a cross-sectional point prevalence study by Black et al³ conducted on 2,079 patients, nonMDR HAPU prevalence was 5.4% and MDR HAPU prevalence was 34.5%. In a cross-sectional study by Coyer et al⁴ conducted on 483 ICU patients in Australia and the US, the MDR PU rate was 12.8% (17/132) for Australian patients and 8.8% (3/351) for American patients. In a descriptive study by Apold and Rydrych²² among 255 cases of severe PUs, 74 (29%) were caused by medical devices. In a study by Jaul¹³ conducted among 174 patients in a geriatric ICU, 35 developed atypical PUs, of which 10 (28.5%) were medical device-related. In a cross-sectional study by van Gilder et al²⁶ conducted in ICUs and other wards, 149 out of 1,631 PUs (9.1%) were caused by medical devices.

Location. MDR HAPU location varies depending on where a medical device is attached to a patient. In the present study, MDR HAPUs developed most commonly on the lips (44.0%), followed by nose (15.6%), fingers (7.5%), and ears (6.11%), whereas nonMDR HAPUs occurred in the sacrum, ischium-sacrum, and sacrum-ischium-trochanter regions. This is underscored in the literature; MDR PUs develop at sites of medical device use. In Black et al’s study,³ the locations of most MDR HAPUs were the ears (35%), lower leg (11%), and heels (8%). In the study by VanGilder et al,²⁶ the most observed MDR PUs locations were the ears (20%), sacrum (17%), heels (12%), and buttocks (10%). In the studies by Watts et al¹¹ and Apold and Rydrych,²²  the most common location of PUs was the cervical collar region. These studies support that nonMDR HAPUs and MDR HAPUs occur in different locations from one another.

Stages. PU stages vary in the literature as well. In the current study, the most frequently observed PU stages of MDR HAPUs were Stage II, Stage I, and unstageable, respectively. In the study by Apold and Rydrych,²² the most observed MDR PUs stages were unstageable (52.7%), Stage II and Stage III (20.3%), and Stage I (5.4%). The MDR PU stages reported in Black et al³ are Stage I (35%), Stage II (32%), and unstageable (24%). The different frequencies in MDR HAPU stages reported is thought to be due to the differences in medical device use, differences and indefiniteness with respect to tissue examination scope and frequency, and the inability to determine the presence of MDR HAPUs until they have reached an advanced stage.²² Methodological differences in research also may account for these differences.^3,4,22 In Apold and Rydrych,²² one fourth of MDR PUs (74%) was not identified until they reached Stage III, Stage IV, and unstageable, versus 54% for nonMDR HAPUs. The Stage I MDR PU identification rate is 5.0% and 20.0% for Stage I nonMDR HAPUs. In addition, the fact MDR PUs develop in relatively lean body sites with little fat tissue under the skin (eg, nostrils, behind the ears, neck, back of the head, nose bone) also allows the ulcers to reach Stage III, Stage IV, and unstageable faster than nonMDR HAPUs.²² Furthermore, in some cases, early-stage MDR PUs are mistakenly identified as dried exudate (oral, nasal, gastric) instead of PUs. These misidentifications tend to delay the timely and appropriate staging of PUs and thus their treatment.²² As with nonMDR HAPUs, the prevention and early diagnosis of MDR HAPUs greatly depends on nurses’ accurate staging and recording of ulcers forming on the skin on which medical devices are positioned.^3,4,22

The MDR HAPU literature focuses mainly on skin ulcers.^3,11,22,25 Coyer et al⁴ state to accurately determine the rate of MDR PUs, evaluations of mucous membrane ulcers as well as skin ulcers need be conducted in order to avoid classifying mucous ulcers as coagulum.

Devices. With advancements in medical technology, the number of available medical devices that may cause MDR PUs has increased. In the current study, more than 20 medical devices were used, among which ETs, CPAP masks, SpO₂ probes, and oxygen masks caused the most MDR PUs. The device causing the most MDR PUs, the intubation tube is also a device widely used in ICUs, findings that correspond to those of Coyer et al.⁴

Risk factors. Although the literature includes studies on MDR HAPUs, no study to determine the impact of the relevant risk factors has been found. Therefore, the results of the present study provide important data for the literature. Advanced age, obesity, low hemoglobin, low albumin, lower Braden risk scores, chronic diseases, medications used, length of hospital stay, and the type of clinic are factors reported to influence the occurrence of nonMDR HAPUs.^3,22,26 According to the literature, nonMDR HAPUs and MDR HAPUs share common risk factors, the most important of which is the use of a medical device. Studies^3,4,22,26 report MDR PUs develop in high-risk patients whose risk evaluation score on the Braden Scale is low. The findings of the current study are supported by the literature: patients in internal medicine ICUs developed 7 times more MDR HAPUs, and those in neurosurgical and chest disease ICUs 6 times more than other ICUs. Moreover, in enterally fed patients, and as the Braden risk scores move from low risk to high risk, MDR HAPU rates doubled. Patients developed MDR HAPUs 7 times more than nonMDR HAPUs (P <0.05) (see Table 4). In addition, advanced age (67.4 ± 16.1 years); attachment to a mechanical ventilator; low hemoglobin and albumin values; and the use of steroid, anticoagulant, and sedative medications were found to be risk factors influencing MDR PU development (see Table 4).

NonMDR HAPU development risk is high in ICUs, where high-risk patients are treated.^4,26 In this study, the highest MDR HAPU development rate was observed in patients admitted to the internal medicine ICU, followed by chest disease ICU and neurosurgical ICU. In the study by VanGilder et al,²⁶ general ICU ranked first, followed by coronary ICU and surgical ICU. However, in these studies, ICU data are reported in terms of ulcers rather than patients, which limits the possibility of comparing studies with respect to MDR PU developing patient numbers. Yet in a study by Black et al,³ no difference was found between ICU and nonICU patients in terms of MDR PU development. Moreover, nonMDR HAPU development risk is higher in patients with medical devices.

Among the patients in the current study, fewer than half (63/175) were attached to a mechanical ventilator or received enteral feeding (43/175) (see Table 1). Although the number of mechanical ventilator-attached patients was smaller, a higher rate of MDR HAPU development was observed in these patients (see Table 4). The literature⁴ supports that ventilation devices cause more MDR PUs than other devices. Similarly, despite the small number of enteral feeding patients (see Table 1), MDR PUs were observed at high rates in these patients (see Table 4). In the study by Jaul,¹³ the incidence rate of MDR PUs was higher in enteral feeding  patients. This may be attributed to the fact that patients who receive enteral feeding and are attached to ventilation devices are usually also those at higher risk with respect to life functions, and thus more often exposed to treatments with more medical devices.

In the current study, patients at advanced ages (67.4 ± 16.1 years) developed MDR HAPUs at a high rate. This is supported by Coyer et al,⁴ where the average age of patients developing a MDR PU was 60.5 ± 20.6 years.

Low hemoglobin (9.7 ± 1.7) and albumin (2.8 ± 0.7) values, use of medication (eg, sedatives, steroids), and high PU risk scale score increase MDR PU risk.^3,4,22,27  Low hemoglobin negatively affects circulation and thus leads to insufficient blood flow to tissues.^6,28 Low albumin leads to interstitial leakage and thus to edema, which in turn results in increased pressure and deterioration in the nutrient exchange in tissues. This situation may facilitate the formation of MDR HAPUs in edematous tissue.²⁸ The use of steroids prevents the formation of collagen fibers, and the use of sedatives impairs the patients’ sensory perception of pain. Therefore, patients on these medications do not feel the pain resulting from medical device-related tissue damage and thus do not adequately voice their discomfort. Because patients are usually prescribed anticoagulants to address circulation problems, MDR PUs may be more likely to develop in these patients.^3,29

Patients in the high Braden Scale score risk group have low activity levels, nourishment problems, and weak stimulus perception and are mostly bedbound and attached to 1 or more medical devices. All these risk factors associated with nonMDR HAPUs occurrence are considered to be relevant for MDR HAPU occurrence as well.

Timing. In this study, MDR HAPUs occurred as early as 24 hours after admission to the ICU and continued to occur through to day 11. Within the first 24 hours, MDR HAPUs developed most commonly on persons using nasal cannulas and ETs. In Coyer et al,⁴ MDR PUs were found to develop between 3 and 13 days after admission.

Location as a factor of time. In the patients participating in the study, the rate of body sites where MDR HAPUs developed in the first 24 hours of hospitalization (11.8%) increased 7 times by the eleventh day. As the patients’ length of stay in the ICU increased, their days attached to medical devices increased as well, along with the risk of medical device pressure on the body site. As the pressure time increases, blood and lymph circulation in the compressed tissue decreases, resulting in inadequate tissue nourishment and thus increased PU risk.^30-32 The same hypothesis appears to be valid for MDR PUs. As the time a medical device stays attached to the tissue increases, circulation under the tissue decreases. Moreover, factors related to the medical device such as the friction/shear and local temperature increase, the edema caused by tight attachment straps, skin softening, and maceration caused by excessive moisture accumulation are all considered to decrease skin tolerance and to contribute to MDR PU development.^3,9,13,33

Limitations 

In this study, patients newly admitted to the ICU and examined within 24 hours were included. The evaluation of skin beneath medical devices was limited to the first examination — the skin beneath whichever medical device was present in the first examination was evaluated for MDR HAPU development in subsequent examinations. The skin sites of other medical devices attached to the patients after the first examination or later in their treatment and MDR HAPU due to these devices were excluded from the study. Due to the differences in the death, discharge from hospital, and transfer of patients to other departments, the observation periods of these patients were different. The observation period was limited to a maximum of 2 weeks. In addition, after completing the observation period  (a total of 6 examinations), patients were not evaluated again, even if their stay in the same ICU continued. Because this study was limited to patients in the internal medicine, cardiovascular surgery, neurosurgical, and anesthesia-resuscitation ICUs in an academic hospital with a MDR HAPU prevalence rate of 15%, the results cannot be generalized to other ICUs. Moreover, preventive measures taken by nurses to prevent MDR HAPUs were not evaluated.

Conclusion

The findings of this study, conducted to determine the prevalence of MDR HAPUs and to identify risk factors for and characteristics of MDR HAPUs development rate through systematic observation, showed MDR HAPUs occurred 3 times more often than nonMDR HAPUs. MDR HAPUs occurred most frequently due to ET, CPAP masks, and SpO₂ probes and mostly on the lips, nose, and fingers. The stages of the MDR HAPUs observed were Stage II, Stage I, and unstageable, respectively.

In this study, the MDR HAPU development rate in patients treated in internal medicine, neurosurgical, and chest disease ICUs, who exhibited high Braden risk values, who were enterally fed, who developed nonMDR HAPUs, and who stayed in hospital for a greater number of days, were found to have a higher MDR PU development rate (P <0.05). Based on the findings, additional studies are needed to help develop evidence-based policies and procedures aimed at preventing MDR HAPUs. 

References

1.         Karadağ A. Basınç ülserleri: değerlendirme, önleme ve tedavi. C.Ü.Hemşirelik Yüksek Okulu Dergisi. 2003;7(2):41–46.

2.         Elliott R, McKinley S, Fox V. Quality improvement program to reduce the prevalence of pressure ulcers in an intensive care unit. Am J Crit Care. 2008;17(4):328–335.

3.         Black JM, Cuddigan JE, Walko MA, Didier LA, Lander MJ, Kelpe MR. Medical device related pressure ulcers in hospitalised patients. Int Wound J. 2010;7(5):358–365.

4.         Coyer FM, Stotts NA, Blackman VS. A prospective window into medical device related pressure ulcers in intensive care. Int Wound J. 2013;11(6):656–664.

5.         Lindgren M, Unosson M, Krantz MA. A risk assessment scale for the prediction of pressure sores development: reliability and validity. J Adv Nurs. 2002;38(2):190–199.

6.         Lindgren M, Unosson M, Fredrikson M, Ek AC. Immobility—a major risk factor for development of pressure ulcers among adult hospitalized patients: a prospective study. Scand J Caring Sci. 2004;18(1):57–64.

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

8.         Schoonhoven L, Bousema MT, Buskens E. The prevalence and ıncidence of  pressure ulcers in hospitalised patients in the Netherlands: a prospective inception cohort study. Int J Nurs Stud. 2007;44(6):927–935.

9.         Black J, Alves P, Brindle CT, Dealey C, Santamaria N, Call E, Clark M. Use of wound dressings to enhance prevention of pressure ulcers caused by medical devices. Int Wound J. 2015;12(3):322–327.

10.       Davis JW, Parks SN. Detlefs CL, Williams GG, Williams JL, Smith RW. Clearing the cervical spine in obtunded patients: the use of dynamic fluoroscopy. J Trauma Nurs. 1995;39(3):435–438.

11.       Watts D, Abrahams E, MacMillan C, Sanat J, Silver R, Van Gorder S, et al. Insult after injury: pressure ulcers in trauma patients. Orthop Nurs J. 1998;17(4):84–91.

12.       Wille J, Braams R, van Harren W, van der Werken C. Pulse oximeter-induced digital injury: frequency rate and possible causative factors. Crit Care Med. 2000;28(10):3555–3557.

13.       Jaul E. Cohort study of atypical pressure ulcers development. Int Wound J. 2014;11(6):696–700.

14.       Strand T, Lindgren M. Knowledge, attitudes and barriers towards prevention of pressure ulcers in intensive care units: a descriptive cross-sectional study. Intensive Crit Care Nurs. 2010;26(6):335–342.

15.       Mattox E. Medical devices and patient safety. Crit Care Nurs. 2012;32(4):60–68.

16.       Tel H, Özden D. Güneş ÇP. Yatağa bağımlı hastalarda basınç yarası gelişme riski ve hemşirelerin bu hastalara uyguladıkları önleyici bakım. Hemşirelikte Araştırma Geliştirme Dergisi. 2006;1(2):35–45.

17.       Schoonhoven L, Defloor T, Grypdonck MH. Incidence of pressure ulcers due to surgery. J Clin Nurs. 2002;11(4):479-487.

18.       Karadağ A, Baykara ZG, Özaltan G. Bir üniversite hastanesinde nokta prevalans çalışması. In: 15 Ulusal İç Hastalıkları Kongresi 2013. Antalya, Turkey: MİKİ Matbaacılık; 2013:429.

19.       Karataş N. Araştırmada Örnekleme. In: Erefe İ (ed). Hemşirelikte Araştırma İlke, Süreç ve. Yöntemleri, Ankara, Turkey: Hemar Ge Yayınevi;2012:124–125

20.       Black J, Baharestani MM, Cuddigan J, Dorner  B, Edsberg L, Langemo D. National Pressure Ulcer Advisory Panel’s updated pressure ulcer staging system. Adv Skin Wound Care. 2007;20(5):269–274.

21.       Karadağ M, Gümüşkaya N. The incidence of pressure ulcers in surgical patients: a sample hospital in Turkey. J Clin Nurs. 2006;15(4):413–421.

22.       Apold J, Rydrych D. Preventing device-related pressure ulcers: using data to guide statewide change. J Nurs Care Qual. 2012;27(1):28–34.

23.       Pınar R, Oğuz S. Norton ve Braden Bası Yarası Değerlendirme Ölçeklerinin yatağa bağımlı aynı hasta grubunda güvenirlilik ve geçerliliklerinin sınanması. In: Uluslararsı katılımlı VI. Ulusal Hemşirelik Kongresi 1998. Kongre kitabı. Ankara, Turkey: Damla Matbaacılık;1998:172–175.

24.       National Pressure Ulcer Advisory Panel and European Pressure Ulcer Advisory Panel. Prevention and treatment of pressure ulcers: clinical practice guideline. Washington: National Pressure Ulcer Advisory Panel, 2009.  Available at: www.npuap.org/resources. Accessed October 10, 2014.

25.       World Health Organization. Global Data Base on Body Mass Index. Available at: http://apps.who.int/bmi/index.jsp?introPage=intro_3.html. Accessed October 7, 2014.

26.       VanGilder C, Amlung S, Harrison P, Meyer S. Results of the 2008–2009 International Pressure Ulcer Prevalence Survey and a 3-year, acute care, unit-specific  analysis. Ostomy Wound Manage. 2009;55(11):39–45.

27.       Karadağ A, Karabağ Aydın, A. Basınç Ülserlerinde Etiyoloji ve Fizyopataloji. In: Baktıroğlu S, Aktaş Ş (ed). Kronik yarada güncel yaklaşımlar. İstanbul, Turkey: İstanbul Üniversitesi Kronik Yara Konseyi;2013:120–125.

28.       Kozier B, Erb GL. Fundamentals of Nursing. Pearson International Edition, 2009. Sidney, Australia: Mosby Elsevier;2009:904–910.

29.       Wolverton CL, Hobbs LA, Beeson T, Benjamin M, Campbell K, Forbes C, et al. Nosocomial pressure ulcer rates in critical care. J Nurs Care Qual. 2004;20(1):56–62.

30.       Bryant RA, Shannon ML, Pieper B, Braden BJ and Morris DJ. Pressure ulcers. In: Bryant RA. Acute and Chronic Wounds – Nursing Management. St Louis, MO: Mosby;1992:105–163.

31.       Morison JM. The Prevention and Treatment of Pressure Ulcers. Toronto, Canada: Mosby;2001:20–32.

32.       Myers BA. Wound Management Principles and Practice. Upper Saddle River, NJ: Pearson Prentice Hall;2004:260–296.

33.       Jaul E. A prospective pilot study of a typical pressure ulcer presentation in skilled geriatric nursing unit. Ostomy Wound Manage. 2011;57(2):49–57.

Potential Conflicts of Interest: none disclosed

Ms. Hanonu is a research assistant, Gazi University Faculty of Health Sciences, Department of Nursing, Ankara, Turkey. Dr. Karadag is a Professor, Koç University School of Nursing, Istanbul, Turkey. Please address correspondence to: Seval Hanonu, RN, MSN, Emniyet Mah, Muammer Yasar Bostancı Sokak No:1606560 Besevler/Akara, Turkey; email:sevalhanonu@yahoo.com.

Abstract

Although the Jackson/Cubbin pressure ulcer (PU) risk scale performs best among risk scales used in intensive care units (ICUs), its performance was not fully satisfactory. In 2010, a minimally modified Jackson/Cubbin (mJ/C) PU risk scale was introduced to formalize PU risk assessment in a large medical-surgical ICU in Finland. The purpose of this secondary analysis was to examine whether individual categories of the mJ/C scale have similar weight and whether the scores within each category (from 1 to 4; 1 equaling highest risk and 4 equaling lowest risk) are linear, as is assumed for the original and  modified scales.

Using data from a cohort of 1,616 consecutively admitted patients retrieved from the ICU database, a detailed secondary analysis of each of the 12 main scoring categories of the Jackson/Cubbin risk scale was performed using logistic regression and analysis of linearity and weight. Of the 1,616 admitted patients, 168 developed a PU during their ICU stay. Among the risk categories, body mass index, nutrition, respiration, age, and transportation during the 48 hours before scoring did not contribute significantly (P>0.05) to the total risk score or the actual development of a PU. The 7 other main categories — incontinence, mobility, medical history, oxygen requirement, need for assistance with hygiene, hemodynamics, and general skin condition — were the main risk contributors. Although only the linearity of the different categories correlated significantly with the predictive value of the categories, the linearity as well as the weights of the categories were at variance from what was assumed originally. The mJ/C scale needs refinement to be a more accurate instrument for PU risk assessment of ICU patients. Not all mJ/C categories were found to contribute to the risk and, when they do, their weight and linearity vary from what has been assumed. The categories respiration and oxygen requirement and the categories mental condition, mobility, and hygiene may overlap. The importance of the incontinence category depends on the frequency of urinary and fecal incontinence management system usage. A simpler, more valid and more sensitive risk assessment scale than the current Jackson/Cubbin scale is needed for ICU patients. 

Patients in intensive care units (ICUs) are at high risk of developing pressure ulcers (PUs).^1-5 Several risk scales have been developed for general PU risk assessment.^6,7 The Braden Scale often is used in ICUs.^3,5,8 A survey by VanGilder et al^5,8 comprising ~11,000 patients in more than 500 ICUs showed PU incidence varied between 8.8% and 12.3% and close to half of the patients had a Braden score above 14, indicating low to medium risk.

A specific risk scale for intensive care patients, the Jackson/Cubbin (J/C) pressure area risk calculator⁹ includes 4 out of the 5 Norton and 5 out of the 6 Braden categories (the missing Braden category involves friction and shear). The J/C pressure area risk calculator consists of 12 categories, each of which is graded linearly from 1 point (highest risk) to 4 points (lowest risk) to describe the clinical risk of PU for ICU patients⁹ (see Table 1). The lower the score, the higher the PU risk — a total score 29 signifies extremely high risk. Among the additional main categories in the J/C scale are age, weight, past medical history, and skin condition plus ICU-specific categories such as respiration, oxygen requirements, and hemodynamics. 

The J/C scale has not gained wide acceptance, although its receiver operating characteristic (ROC), curve and sensitivity, and specificity have been the best of several scales proposed for ICU use.^5,10-12 Specifically, the validation study by Seongsook et al¹⁰ comparing the J/C, Braden, and Douglas Scales included 112 ICU patients and found the specificity (61%) and positive predictive value (51%) of the J/C scale to be better than those of the Braden (26% and 37%, respectively) and Douglas scales (18%, 34% respectively). The review by Shanin et al¹¹ compared the J/C, Braden, Douglas, Waterloo, and Norton scales and included 1,150 ICU patients in 7 studies; it concluded only the J/C scale was developed for assessment of PU risk in ICU patients, and the assessment of validity of different risk scales varied. The systematic review by García-Fernández et al¹² presented 15 scales and 5,187 patients in 26 studies; the Braden scale was examined in 13 studies (1,458 patients) and J/C scale in 5 studies (629 patients). The authors recommended the Braden scale for use in PU risk assessment in ICUs. Both the Braden Scale and J/C risk scale are based on the Norton scale.¹³  

In 2010, a retrospective research program utilizing the ICU database was launched by the present study team to study the epidemiology and risk factors related to PUs in a large medical-surgical ICU. The program included introduction of a modified version of the J/C (mJ/C) risk scale in an attempt to formalize PU risk assessment¹⁴ based on previous studies.^10,11 Briefly, the previous results implied the J/C risk scale and its predefined cut-off score of 29 do not sufficiently identify extremely high-risk patients because 55.8% of patients with PUs fell into the ≤29 score group, while 46.6% patients without PUs had a similar score.¹³ The sensitivity of the mJ/C scale was 55.8%, the specificity was 53.4%, the positive predictive value was 13.4%, and the negative predictive value was 90.3%. The total incidence of PUs was 11.1% (181/1,629); 13 patients with exclusively nasal PUs were excluded from the analysis.

Due to the limited mJ/C scale score separation of PU from nonPU patients and to the modest sensitivity and specificity, this retrospective secondary analysis was conducted to examine whether the individual categories of the mJ/C scale have similar weight (ie, each subcategory is scored from 1 to 4) and whether the scores within each category from 1 to 4 (1 meaning highest risk and 4 meaning lowest risk) are linear, as is assumed for the J/C scale. The hypothesis was not all factors contribute equally to PU development, as originally described by Jackson in 1999.⁹ A specific examination was conducted to determine more specifically what factors are related to the development of PUs in the ICU.

Methods

Patients. The Turku University Hospital serves a population of 700,000. The adult ICU has 24 beds. The hospital serves as a national center for hyperbaric oxygen therapy. All surgical and medical intensive care patients in the region are treated in this hospital, except patients with major burns and patients undergoing solid organ transplantation, who are treated elsewhere. Based on the treatment needs on admission, patients are classified as ICU-patients or as patients needing high-dependency (ie, step down) care.

Patient data from all 2010 ICU admissions (1,629 patients >18 years old, mean age 60.5 years [range 18–95 years], average length of stay 3.7 days) were retrospectively analyzed to study the occurrence of PUs and their risk factors in medical and surgical patients.¹⁴ Patients with nasal PUs only (n = 13) were excluded from the analysis, leaving 1,616 patients for the current secondary analysis.

The main categories of the J/C scale are presented in Table 1. In addition to these 12 main categories, 3 additional assessments are made that may lower the PU risk score (see Table 1, “deduct points”). The J/C risk scale⁹ from 1999 was back-translated and forward-translated into Finnish for validation purposes, and some of the categories were more precisely defined (mJ/C risk scale) to improve the clarity and reproducibility of the assessments (revised sections are marked as bolded in Table 1). The age and body mass index (BMI) values are automatically calculated by the clinical documentation and information system used by the ICU (Clinisoft, GE Healthcare, Buckinghamshire, UK). It takes 2 to 3 minutes for an ICU nurse to calculate risk and enter the information into the ICU database.

All data used in this study were retrieved from records, abstracted (ie, checked by computer for their correct format), and entered into a database for analysis.

The study plan was approved by the Ethics Committee of the Hospital District of Southwest Finland.

Statistical methods. Statistical evaluation of the main categories of the mJ/C risk scale was based on exploratory analysis and regression modeling. Linearity was scored from +4 (arbitrary unit) when linearity was as described in the J/C scale⁹ (see Table 1) to -4 if linearity was reversed. The relative weight of each individual J/C category was determined by multiplying each subcategory score point by the number of patients in that subcategory and then summing the 4 scores together and dividing the sum by the total number of patients in that category.

Logistic regression modeling was applied to evaluate the association between PUs and the categories of the J/C PU risk calculator. A proportional-odds cumulative logit model¹⁵ was used because all of the J/C PU risk categories are ordinal (1, 2, 3, 4) and the risk for PUs is expected to increase with lower scores (ie, 1 point represents the highest risk value of an individual risk category⁹). Separate analyses were performed for all risk categories to evaluate the marginal independence/association of PUs and individual risk categories. Odds ratio (OR) and the Wald chi-square (²) test, based on logistic regression modeling, were used to evaluate the association between PUs and the risk categories. Wald ² is calculated as:

(MLE(PU)/standard error)²

MLE (PU) is the maximum likelihood estimated logistic odds of PUs effect. OR, the Wald ²-test, and the related P values (same for both) were used to evaluate the statistical null hypothesis, H₀.  The distribution of mJ/C PU risk category values in a population with PUs was equal to the distribution in a population with no PUs. A P value <0.05 indicated sufficient evidence in favor of the alternative hypothesis, H:  values of a mJ/C PU risk category were statistically significantly higher in a population with PUs than in a population with no PUs. Fisher’s exact test¹⁶ and the ² test were used to test statistical significance of the contingency tables. Both tests were used to determine whether the incidence rates of PUs were the same in 2 groups that were compared (ie, if the incidence of PUs was independent of the risk factor or of other predictive variables^15,16).

Fisher’s exact test is designed to test the significance of contingency tables when the sample size is small or some cells of a contingency table number <5. This test is more conservative than the ² test and may yield higher P values.¹⁶

Results

The results of the secondary analysis of each individual risk category of the mJ/C scale showed mobility, medical history, oxygen requirements, hygiene, hemodynamics (linearity score +2, relative weight 2.0; OR 2.232, P<0.001) and general skin condition (linearity score +4, relative weight 3.6; OR 3.272, P <0.001) significantly predicted PU development (see Tables 2 and 3). Incontinence (linearity score 0, relative weight 4.0; OR 3.910, P = 0.0126) and mental condition (linearity score +1, relative weight 2.2; OR 1.481, P = 0.0116) were significant predictors of PU, while BMI, nutrition, respiration, and age were not associated with the development of PUs (see Tables 2 and 3). 

A trend was noted toward a linearity of the risk score point distribution of the categories that were significantly associated with the PU risk (see Table 2, Table 3, Figure 1a). The linearity of the incontinence category could not be determined due to too few patients in the score point groups 1 to 3 (see Table 3). Only general skin condition contributed linearly to PU risk, as defined in the J/C risk scale (see Table 1, Table 3, Figure 1a). Oxygen requirements and hygiene contributed almost linearly, and BMI, nutrition, and respiration were almost the opposite (ie, contralinear) (see Table 3, Figure 1a). A significant correlation was noted between linearity and the predictive value of the categories (OR): rs = 0.694 (P =  0.0123, Spearman’s rank correlation¹⁷). 

The J/C risk scale assumes the relative weight of each J/C category is 2.5. The weights of the different risk categories that contributed to the PU risk differed from 2.5 and from each other (see Table 3, Figure1b). The relative weight of the hygiene category (1.6) was 3 times that of the nutrition (3.9) and incontinence (4.0) categories (see Figure 1b). The weight contribution of the other categories fell somewhere between these values. No correlation was noted between the relative weights of the categories and their predictive value (OR): rs = 0 (P = 1, Spearman’s rank correlation¹⁷). 

Two thirds of patients were transported within the hospital either to surgery or for examinations, but only a small number of patients (n = 20) qualified for the transportation group, because transportation had to have occurred within 48 hours of mJ/C scoring (see Table 4). All of the 20 patients who had been transported developed a PU (P<0.001, Fisher’s exact test) compared to the nontransport (PU n = 43, 8.5% of that group) and transport group (PU n = 105, 10% of that group). Of the patients who had been transported, 14 were in the high-risk group, as defined by the current J/C risk score (29), 3 patients were very close to the cut-off limit with a J/C score of 30–31, and 3 had scores of 34, 37, and 39 when transportation and other conditions requiring application of the deduction of points were considered (see Table 1). 

Discussion

Because development of PUs is a multicausal problem, an adequate PU risk scale combined with clinical evaluation is important for overall PU risk assessment. The J/C risk scale is specifically designed for intensive care and has performed optimally for ICU patients.^10,11 However, its performance in an unselected ICU population is satisfactory only to some extent, as shown by the previous study¹⁴: the separation of low-risk and high-risk patient groups and its sensitivity and specificity were suboptimal.¹⁴ Therefore, in this study, each of the scoring categories⁹ of the J/C risk scale were analyzed critically.

Among the general population and ICU patients, the prevalence of PUs increases with age.^2,5,18 This observation is corroborated by the results of the present study among patients older than 70 years, but, as a whole, the importance of age as a predictor is negligible. In this study, low BMI values (<18 kg/m²) contributed to the PU risk and high BMI values did not, even though both are linked to PU development in the general population.^19-21 A low BMI may be a PU risk factor (see Table 3) because it is associated with a minimal amount of subcutaneous fat, which may increase the deleterious effects of pressure from underlying osseous protuberances on the tissues.^21,22 The mental condition, mobility, and hygiene categories contained definitions that are not sufficiently stringent; they are partly interchangeable or superfluous and this impairs their value.^9,21,23 Still, it is understandable that mobility does contribute to PU risk because mobility is a crucial consideration in general risk assessment scales.^20,23 ICU patients are rarely able to take care of themselves and need much assistance from staff due to their limited mobility and limited ability to independently maintain hygiene. Not surprising, most PUs develop in patients that need assistance when friction and shear on the skin can occur if the procedures to assist the recumbent patient are not performed correctly (see Table 3).

Moist skin, especially due to urine and feces, is a major risk factor for PUs.^6,23,24 In the ICU of the Turku University Hospital, most patients have urinary catheters, and fecal catheters are used  when needed to keep the skin as dry as possible. This is represented in the point distribution in the incontinence category (see Table 3). Despite a wide confidence interval, the incontinence category reached significance (see Table 2).

The point distribution of the general skin condition category correctly reflects the PU risk: the risk is lowest when the skin is intact and highest when deep or secreting wounds are present⁹ (see Table 3). This is in accordance with what is known about the pathophysiology of PUs, because wounds are associated with an inflammatory reaction and often with infection and fever, release of free radicals, and pro-inflammatory cytokines.^25-27 Wounds often produce high volumes of fluid, which keeps the skin moist and severely impairs positioning therapy because patients cannot be positioned on their large wounds.

Although definitions regarding respiration and oxygen are partly interchangeable or superfluous (see Table 1), both are related to tissue oxygenation, which has been examined only minimally as a risk factor for PU development.²⁸ The contribution of respiration and oxygen requirements to PU risk differed significantly from each other (see Tables 2 and 3), probably because the respiration mode does not correlate with tissue oxygenation in practice. Oxygen requirements contributed to the risk of PU development in this study, especially the highest risk (1 point = >60% O2) (see Table 3). This probably reflects the situation where lower oxygen concentrations keep the tissue oxygen levels sufficiently stable, while patients needing a great deal of oxygen are so ill their tissue oxygen tension is insufficient to support tissue viability and prevent PUs. This assumption is supported by the findings in the hemodynamics category. Although the current scoring order was not optimal (see Table 3), the incidence of PUs is higher in patients who are unstable regardless of whether they are on or off inotropes (see Table 3).

With respect to PU risk score point deduction, anemia and hemoglobin concentration scoring may replace the need for blood products as an assessment category.^6,29 Although 20 patients underwent transportation within 48 hours (see Table 4) before scoring, most of them also were otherwise classified as high risk based on their mJ/C score (29). Because, overall, two thirds of the patients were transported (most earlier than 48 hours before scoring), the contribution of this part of the mJ/C score seems to be insignificant relative to the overall score.

Although only the linearity of the mJ/C categories correlates significantly with the predictive values of PU development, the results show point order (1 as highest and 4 as lowest risk) is not correct in most categories. The J/C risk scale assumes the relative weight of each of the categories is 2.5, which was not the case, because the patients are distributed differently within each of the categories. A 3-fold difference was noted between the highest and lowest relative weight categories, and no correlation was found between the relative weights and predictive values of the mJ/C categories, meaning differences exist among the various categories of the mJ/C scale but this is not a reflection of the true weights of the different categories. This matter requires additional research.

Limitations

The retrospective retrieval of the data infers individual contributions of the nurses to the actual risk assessment could not be controlled. However, this is the largest single study of a consecutive ICU patient population. Also, the number of PUs was only 168, which leaves room for some chance effects in the results, because the number of both PU and nonPU patients is quite small in some of the mJ/C subcategories.

Conclusion

It is not an easy task to identify specific risk indicators for severely ill ICU patients with multiple disorders. The J/C risk scale is based on certain categories that have been assumed to be linear and of equal weight with regard to the risk of acquiring a PU. In this study, these assumptions were found to be invalid. Seven of the categories contribute substantially to the overall score and actual risk: incontinence, mobility, medical history, oxygen requirement, hygiene, hemodynamics, and general skin condition. This also indicates several risk categories of the J/C risk scale correlate and associate among each other, although this specific matter was not examined in this study. Because of this association, some categories measure the same pathophysiological phenomena. In addition, it was found the order of the risk points is suboptimal within the categories of the J/C risk scale. These results should prompt future research aimed at introducing an individualized order and weight of individual risk categories into the assessment of the risk of PUs with the mJ/C scale. Furthermore, numerous other PU risk factors³⁰ such as admission diagnosis, body temperature, Sequential Organ Failure Assessment score, and hemoglobin concentration should be tested either by prospective cohort studies or retrospective analyses of existing large patient cohorts to identify the most important PU risk factors in the ICU setting. These variables were not examined in this study because they are not part of the risk evaluation scale.

There seems to be room for a simpler scale for PU risk assessment and risk prediction for ICU patients. Such a scale should include only those risk indicators that constitute separate, predictive risk categories. This study shows that, currently, the mJ/C risk scale in combination with clinical assessment is a feasible way to assess the risk of PU among ICU patients, but more research is needed to identify the most effective predictors.

References

1.         Takala J, Varmavuo S, Soppi E. Prevention of pressure sores in acute respiratory failure: a randomized, controlled trial. Clin Intensive Care. 1996;7(5):228–235.

2.         Bours GJ, De Laat E, Halfens RJ, Lubbers M. Prevalence, risk factors and prevention of pressure ulcers in Dutch intensive care units. Results of a cross-sectional survey. Intensive Care Med. 2001;27(10):1599–1605.

3.         Kottner J, Wilborn D, Dassen T, Lahmann N. The trend of pressure ulcer prevalence rates in German hospitals: results of seven cross sectional studies. J Tissue Viability. 2009;18(2):36–46.

4.         Terekeci H, Kucukardali J, Top C, Onem Y, Celik S, Öktenli C. Risk assessment study of the pressure ulcers in intensive care unit patients. Eur J Int Med. 2009;20(4):394–397.

5.         VanGilder C, Amlung S, Harrison P, Meyer S. Results of the 2008 – 2009 International Pressure Ulcer Prevalence Survey and a 3-year, acute care, unit-specific analysis. Ostomy Wound Manage. 2009;55(11):39–45.

6.         National Pressure Ulcer Advisory Panel and European Pressure Ulcer Advisory Panel. Pressure Ulcer Prevention and Treatment: Clinical Practice Guideline. Washington DC: National Pressure Ulcer Advisory Panel 2009.  Available at: www.epuap.org. Accessed January 15, 2016.

7.         García-Fernández FP, Soldevilla Agreda JJ, Verdú J, Pancorbo-Hidalgo PL. A new theoretical model for the development of pressure ulcers and other dependence-related lesions. J Nurs Scholar. 2014;46(1):28–38.

8.         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.

9.         Jackson C. The revised Jackson/Cubbin Pressure Area Risk Calculator. Intensive Crit Care Nurs. 1999;15(3):169–175.

10.       Seongsook J, Ihnsook J, Younghee L. Validity of pressure ulcer risk assessment scales; Cubbin and Jackson, Braden, and Douglas scale. Int  J Nurs Stud. 2004;41(2):199–204.

11.       Dassen T, Halfens RJ, Shanin ES. Predictive validity of pressure ulcer risk assessment tools in intensive care patients. World Crit Care Nurs. 2007;5(3):75–79.

12.       García-Fernández FP, Pancorbo-Hidalgo PL, Soldevilla Argeda JJ, Rodrigez Torres MC. Risk assessment scales for pressure ulcers in intensive care units: a systematic review with meta-analysis. EWMA J. 2013;13(2):7–13.

13.       Norton D, McLaren R, Exton-Smith AN. An Investigation of Geriatric Nursing Problems in Hospital. London, UK: National Corporation for the Care of Old People (now Centre for Policy on Ageing);1962. [Available as loan through special libraries.]

14.       Ahtiala M, Soppi E, Wiksten A, Koskela H, Grönlund J. Occurrence of pressure ulcers and their risk factors in mixed medical-surgical ICU — a cohort study. J Intensive Care Soc. 2014;15(4):2–4.

15.       McCullagh P. Regression models for ordinal data. J R Stat Soc. Series B (Methodological), 1980;42(2):109–142.

16.       Fisher R. A. On the interpretation of ² from contingency tables, and the calculation of P. J R Stat Soc 1922;85(1): 87–94.

17.       Myers JL, Well AD. Research Design and Statistical Analysis, 2nd ed. London, UK: Lawrence Erlbaum Publisher;2003:508.

18.       Theaker C, Mannan M, Ives N, Soni N. Risk factors for pressure sores in the critically ill. Anaesthesia. 2000;55(3):221-224.

19.       VanGilder C, MacFarlane G, Meyer S, Lachenbruch C. Body mass index, weight, and pressure ulcer prevalence: an analysis of the 2006-2007 International Pressure Ulcer Prevalence Surveys. J Nurs Care Qual. 2009;24(2):127–135.

20.       Soppi E, Iivanainen A, Korhonen P. Concordance of Shape Risk Scale, a new pressure ulcer risk tool, with the Braden scale. Int Wound J. 2014;11(6):611–615.

21.       Kottner J, Gefen A, Lahmann N. Weight and pressure ulcer occurrence: a secondary data analysis. Int J Nurs Stud. 2011;48(11):1339–1348.

22. Cubbin B, Jackson C. Trial of a pressure area risk calculator for intensive therapy patients. Intensive Care Nurs. 1991;7(1):40–44.

23.       Braden B, Bergstrom N.  A conceptual schema for the study of the etiology of pressure sores. Rehabil Nurs. 1987;12(1):8–12.

24.       Bayón García C, Binks R, De Luca E, Dierke C, Franci A, Gallert E, et al. Expert recommendations for managing acute faecal incontinence with diarrhea in the intensive care unit. JICS. 2013;14(suppl 2):1–9.

25.       Friedland JS, Porter JC, Daryanani S, Bland JM, Screaton NJ, Vesely MJJ, et al. Plasma proinflammatory cytokine concentrations, Acute Physiology and Chronic Health Evaluation (APACHE) III scores and survival in patients in an intensive care unit. Crit Care Med. 1996;24(11):1775–1781.

26.       Vande Berg JS, Rose MA, Haywood-Reid PL, Rudolph R, Payne WG, Robson MC. Cultured pressure ulcer fibroblasts show replicative senescence with elevated production of plasmin, plasminogen activator inhibitor-1, and transforming growth factor-1. Wound Repair Regen. 2005;13(1):76–83.

27.       Bronneberg D. Biochemical markers for early detection of superficial pressure ulcers. Academic dissertation 2007, Technische Universiteit Eindhoven, Eindhoven, Holland.

28.       Manzano F, Navarro MJ, Roldán D, Moral MA, Leyva I, Guerrero C, et al. Pressure ulcer incidence and risk factors in ventilated intensive care patients. J Crit Care. 2010;25(3):469–476.

29.       Nixon J, Nelson EA, Cranny G, et al on behalf of the PRESSURE Trial Group. Pressure relieving support surfaces: a randomised evaluation. Health Technol Assess. 2006;10(22):1–179.

30.       García-Fernández FP, Soldevilla Agreda JJ, Verdú J, Pancorbo-Hidalgo PL. A new theoretical model for the development of pressure ulcers and other dependence-related lesions. J Nurs Scholar. 2014;46(1):28–38.

Potential Conflicts of Interest: Dr. Soppi is the chairman of the board of Carital Group, Helsinki, Finland, a group of companies manufacturing and marketing support surfaces.

Ms. Ahtiala is an intensive care unit RN and an authorized wound nurse, Turku University Hospital, Turku, Finland. Dr. Soppi is a consultant in internal medicine, Eira Hospital, Helsinki, Finland. Mr. Kivimäki is a statistician, StatFinn Ltd, Turku, Finalnd. Please address correspondence to: Maarit H. Ahtiala, RN, Intensive Care Unit, Turku University Hospital, Hämeentie 11, Turku 20520 Finland; email: maarit.ahtiala@tyks.fi.

Abstract

Risk evaluation scales are used as part of prevention strategies for pressure ulcers (PUs). Two of the more used scales, the Braden and Waterlow Pressure Ulcer Risk Assessment Scales (B-PURAS and W-PURAS, respectively) are used in Turkey and worldwide, and their validity in terms of sensitivity, specificity, and predictive validity have been examined in various studies. To determine nurses’ opinions of B-PURAS and W-PURAS in terms of administration time, practicality, clarity, and perceived ability to encompass PU risks and accurately predict PUs, a descriptive study was conducted from October 15, 2011 to November 20, 2011 at a university hospital among nurses who volunteered to participate.

Demographic information collected and assessed included age, highest degree of education completed, and practice area. Participants were trained to use both scales by researchers during a 1-hour session and asked to use them for 2 weeks in their daily practice. The nurses then completed a paper-and-pencil, 12-item questionnaire measuring agreement with general questions about PURAS with options to provide comments. In addition, the questionnaire contained 3 open-ended questions on scale preference, 1 question to rate perceived scale accuracy in predicting PUs, and the opportunity to recommend changes to the scales. Data were analyzed using SPSS 20.0. Frequencies, percentages, and Spearman’s rank correlations were calculated. Eighty-three (83) registered nurses (mean age 27.46 ± 3.73, mean nursing experience 6.53 ± 3.25 [range 0.5–16] years) participated; 18.1% of the nurses had prior experience using such scales, and none of the clinics in the study facility had used PU risk scales previously. Most participants (71, 85.5%) had a bachelor’s degree, 62 (74.7%) worked in a facility that admitted patients at high risk for developing PU, but 66 (almost 80%) saw fewer than 4 ulcers per week. Each nurse performed an average of 22 assessments during the study for a total of 1,826 assessments. Participants generally found both scales practical and appropriate; almost 75% thought the B-PURAS was acceptable for use in all clinics, compared to 51% for the W-PURAS; only 20 participants questioned the scales’ accuracy in predicting PUs. While 43% preferred the B-PURAS for precision, clarity, and practicability, 25% preferred the W-PURAS because it was more comprehensive. Also, the older the nurse, the more likely the preference for the B-PURAS (P <0.019). Some nurses (13%) suggested adding different risk factors such as serum albumin. Overall, 61.4% stated they would prefer to use the B-PURAS over the W-PURAS. Nurses’ recommendations should be considered for practice and new scale development and testing, ideally in different patient populations. 

Pressure ulcers (PUs) are frequently encountered in individuals with acute and chronic diseases.^1-5 According to a bottom-up costing approach study by Bennett et al⁶ and a literature review by Ayello and Braden,⁷ the care and management of PUs are difficult, they are costly to treat, and they require extensive recovery time, prolonging the duration of hospitalization. In terms of quality, cost, and nursing care, preventing PUs is easier and cheaper than treating them.^5-7

PU prevalence rates vary markedly among different countries. In the United States, the National Patient Care Safety Monitoring Study,⁸ which covered more than 51,000 patients, found 4.5% of Medicare beneficiaries developed a PU during their hospital stay and 5.8% had a PU on admission. In Canada, PU prevalence was estimated at 25% in acute care settings.⁹ In the UK, a point-prevalence study for estimating the prevalence of wounds in general (including surgical wounds, diabetic leg and foot ulcers, cancer, and PUs) found the prevalence of PUs alone was 17%.¹⁰ In descriptive PU prevalence studies^11-15 in Turkey (N = 84), the prevalence of surgery-related PUs was 54.8%, and in intensive care units (ICUs) the rate was between 14.3% and 20.56%; point-prevalence studies revealed a prevalence between 8.1% and 8.3%. Although the literature overall (including descriptive and prospective studies and literature reviews^7,16-26) suggests PUs are largely preventable, they remain a considerable problem. In the current authors’ opinion, the lack of a preventive approach and the much greater focus on the pathophysiology of PUs may be considered factors contributing to the overall failure to find a desirable solution to this problem.

The first preventive intervention involves assessment of the risk of developing a PU.^7,16-22 According to a literature review by Ayello and Braden,⁷ if a risk assessment is performed systematically, PU occurrence can decrease by 60% commensurate with the risk level, and the cost of care also decreases markedly. According to various descriptive studies and literature reviews,^3,6,20 identifying the risk of PU development decreases the immediate care costs and allows for higher quality and more effective patient care.

Many nurse investigators have developed various PU risk assessment scales (PURASs) to determine patient risk of developing PUs.^21-24 The first PURAS was developed by Doreen Norton in 1962 for the selection of elderly participants for research on PUs.^25,26 Numerous PURASs were developed in the 1980s; currently, at least 40 different PURASs are available.¹⁷ Hidalgo et al’s²⁶ systematic review reported the most commonly known scales are the Braden (1987), Norton (1962), Gosnell (1973), and Waterlow Pressure Ulcer Risk Assessment Scales (1985); among these, the Norton and Braden scales are most commonly used throughout the world. However, although guidelines typically recommend the use of PURASs, these scales are not without critics. For instance, the scales do not include all risk factors associated with PUs, they sometimes are used as alternatives rather than to supplement clinical evaluations, and they have generally poor validity and reliability.^25,26 As such, hospital guidelines nowadays recommend the use of clinical assessment and a PURAS together.^27-30

Nurses can employ one of these scales while providing care or can develop one of their own. Developing a new scale and testing its reliability and validity requires expertise on the issue or the support of experts. Furthermore, the importance of the clinical decision-making of nurses themselves in risk evaluation cannot be overlooked, especially the clinical decision-making ability of experienced nurses who are experts in their fields. Thus, it may be easier to use scales already developed for nurses in clinical practice.¹⁹

Clinical and home care nurses who are certified in wound, ostomy, and continence nursing are legally responsible for the prevention and care of PUs in Turkey.^31,32 Although the importance of using a PURAS and preventive care is frequently stressed in the literature, PURASs are not commonly used in acute care units or long-term care facilities in Turkey; furthermore, only limited care aimed at preventing PUs is generally provided because assessments are not frequently performed.^2,13,19 In some countries, making a risk evaluation within the first 6 or 24 hours following admission may not be required. In Turkey, only the Braden, Norton, and Waterlow PURASs, which have undergone reliability and validity analyses in Turkey, are accepted for use.^33-35

To the authors’ knowledge, around the world no studies have been conducted to examine nurses’ opinions regarding the use of these scales. The clinical observations and expertise of nurses are important for developing scales for PU risk evaluation, because nurse opinions are critical in determining the risk factors to be included in a scale. Nurse input is also necessary for determining the characteristics of the scale, such as the clarity and practicability of items that need to be included.^{7,17,19,20,25} Therefore, instead of merely asking nurses to accept the developed scales as wholly complete and accurate, researchers might obtain nurse opinions and allow them to contribute to scale development, which in turn may improve the buy-in and benefit of these scales to nursing care. In the authors’ opinion, PURASs based on nurses’ opinions tend to cover a more extensive range of relevant risk factors and are more applicable and responsive to nurses’ needs in planning patient care; furthermore, nurses’ opinions affect the use of evidence-based PU risk assessment.

The purpose of this descriptive pilot study was to determine the opinions and preferences of nurses regarding the Braden and Waterlow PURASs (B-PURAS and W-PURAS, respectively).

Methods and Procedures

The study was performed at a 1,100-bed university hospital. Written permission to conduct the study was obtained from the hospital directorate, which is also the hospital’s institutional review board. Study data were collected between October 15 and November 20, 2011 from participating nurses working in ICUs at the university hospital (including the anesthesia, neurosurgery, internal medicine, general surgery, chest diseases, cardiology, cardiovascular surgery, and neurology ICUs) as well as in the physical therapy, rehabilitation and orthopedics clinics. Nurses who worked in these areas  determined PU risk using their own professional knowledge and experience. Nurses were informed about the study and were invited to volunteer. Nurses who consented to participate in the study were given individual training by one of the researchers, who provided a 1-hour training session that addressed PUs, PU risk assessment, and use of the Braden and Waterlow PURASs. Following training, the nurses administered these 2 scales at the same time each day on the same patients for 2 weeks. Both scales were completed for each patient. After these 2 weeks, the questionnaires were completed by the participants and collected by the researchers.

Questionnaires.

Demographic data. The questionnaire on demographic characteristics comprised 12 items on nurses’ personal characteristics (eg, age, highest degree completed), their status in PURAS training, and their previous experience with using PURASs. The nurses completed the paper-and-pencil instrument independently (see Table 1). 

Risk scale comparison. Researchers (experts interested in PUs and scale development) developed this questionnaire based on a review of the literature; it was not tested for validity or reliability. The survey instrument included 12 statements that allowed participants to compare the 2 scales/assessment on time to completion, practicality, clarity, coverage of PU risks, and perceived ability to predict PUs. Participants indicated their level of agreement with survey items (“I agree,” “I partly agree,” and “I do not agree”) and were asked to explain their answers when they selected “I partly agree” or “I do not agree” (see Table 2). Participants also indicated their level of agreement with the statement, “Risk assessment scales that have established validity and reliability should be used to prevent PUs.” The questionnaire also included 1 item that asked nurses how accurately they believed the scales predicted PUs; this item was rated using a visual analog scale ranging from 0 (worse at predicting) to 10 (better at predicting). Questions included, “Which PURAS do nurses prefer by area of practice?” “What are reasons for preferring one scale over the other?” “What are risk factors nurses believe should be included PURAS?” 

The questionnaire initially was sent to 5 experts on PUs and scale development who evaluated the items in terms of comprehensibility, scientific content and criteria, ability to quantify the questions, and rating scale method. Necessary revisions were made according to the experts’ opinions. 

Data analysis. The data obtained in the study were analyzed using Statistical Packages for Social Sciences (SPSS) for Windows, Version 20.0 (SPSS Inc, Chicago, II, IL, USA). The frequency and percentages of nurses’ responses and Spearman’s rho were calculated to analyze the correlation between scale preference, work experience, and age. The open-ended questions were individually assessed and similar statements were grouped; data on the frequency and percentages were calculated  by SPSS.

Results           

Out of a total of 122 nurses in the participating departments, 83 (68%, mean age 27.46 ± 3.73, mean nursing experience 6.53 ± 3.25 [range 0.5–16] years) took part in the study. Nonparticipation was due to workload (27) or being on leave during the study period (12). None of these nurses used any kind of PURAS in their daily work, but 18.1% stated they had prior experience using such scales. Participants’ demographic characteristics are summarized in Table 1. Most nurses (71, 85.5%) had a bachelor’s degree in nursing, 62 (74.7%) had worked previously at clinics where patients with a high risk of PUs were admitted, and 40 (48.2%) provided care to an average of 1 to 2 patients with PUs weekly. Most had not received additional PU prevention/treatment (67, 80.7%) or training on risk assessment scales (81, 97.6%) after graduation. Each nurse performed an average of 22 assessments during the study for a total of 1,826 assessments. Most participants (80.7%) agreed with the statement, “Risk assessment scales that have established validity and reliability should be used to prevent PUs.”

B-PURAS. Most participants (66, 79.5%) thought the B-PURAS was easy to understand, 62 (74.7%) thought the B-PURAS was practical in terms of time consumption, and 56 (67.4%) thought it was practical to use. Only 8 (9.6%) of the participants thought the B-PURAS did not accurately identify patients at risk of PUs. The majority of participants (59, 71%) did not have difficulty choosing from among answer options while using the B-PURAS, and (19) 23% thought the B-PURAS was not suitable for all clinics (see Table 2).

W-PURAS. In assessing the W-PURAS, 53 (63.8%) thought it encompasses all risks associated with PUs, 22 (26.5%) had difficulty choosing from among the answer options, 36 (43.3%) thought it was important for identifying patients at risk but 12 (14.4%) thought it does not accurately identify which patients are at risk of PUs, and 42 (51.2%) found it suitable for use in all clinics (see Table 2).

More than half of the participants (51, 61.4 %) stated they would prefer to use the B-PURAS in their clinics. However, 7 participants (77.7%) working in the cardiovascular surgery ICU preferred the W-PURAS. All of the nurses working at the physiotherapy rehabilitation clinic, 87.5% of those working at the coronary ICU, and 83.3% of those working at the general surgery ICU preferred the B-PURAS (see Table 3). 

Open-ended questions. Open-ended items regarding reasons for preferring one scale over the other were classified under the following categories: precision, clarity, and practicability.

 Among all participants, 43% preferred the B-PURAS for its precision, clarity, and practicability, while 25% reported their reason for preferring the W-PURAS was its elaborateness and comprehensiveness (see Table 3). The mean score on the visual analog scale regarding the B-PURAS’s perceived ability to predict PUs was 7.4 ± 1.7, while for W-PURAS it was 6.8 ± 1.8 (see Table 3). Twelve (12) nurses recommended that in addition to the risk factors found in the 2 scales, factors such as serum albumin value, arterial blood pressure, infection, connection with respirator, amputation, and dehydration should be added.

A significant correlation was found between participant preference for the B-PURAS and age (P<0.05) (see Table 4). Although a significant correlation between years of service and scale preference was not found (P>0.05), a significant negative correlation was found between age and B-PURAS preference (P<0.05); namely, with increasing age, nurses expressed a stronger preference for the B-PURAS (see Table 4). 

Discussion

Although they had limited experience using risk assessment scales, the majority of the participants thought PURASs should be employed in the prevention of PUs. The importance of PURASs and preventive care practices has been frequently emphasized in the literature. The Agency for Health Care Policy Research²⁷ issued the first guidelines on PU prevention, which stated PURASs with established validity and reliability should be used for the prevention of PUs. Guidelines^27-30 also recommended the use of PURASs to identify and manage the risk factors of PUs. According to a systematic review by Walsh and Demsey,³⁶ offering care commensurate with risk level by using a PURAS decreases the risk of PUs and improves the cost-effectiveness of care. Furthermore, recording and performing regular evaluations of a patients’ care requirements facilitates quantification of the patient’s improvement.^26,37 Notably, a correlational study³⁸ of critically ill patients indicated nurses’ subjective global risk estimates and total scores on risk assessment scales shared a 60% variance, suggesting nurses’ subjective assessments of risk exposure differ markedly from their risk estimates derived using standardized risk assessment tools. One explanation for this may be nurses draw on factors other than those captured by the standardized tools when making clinical decisions or they weigh certain patient conditions differently.³⁸ It should be noted that recommending the use of scales does not necessarily mean that nurses’ identification and classification of patients’ risk according to their own knowledge and experiences is unimportant.

One third of participants thought the B-PURAS covered PU risks better than the W-PURAS. A possible explanation for this result is the B-PURAS is based upon risk factors for patients who are cared for at home,³⁹ although with proven validity and reliability, the scale now is used widely in acute and long-term care settings. Braden and Bergstrom³⁹ regarded the intensity of the pressure and the tolerance of the tissue to pressure as the main etiological factors, and thereby developed the B-PURAS with 6 subscales. B-PURAS has been found to have the highest validity and reliability of all PURASs.⁴⁰ Specifically, the B-PURAS has satisfactory reliability and validity and appears to be effective for assessing risk of PUs.^33,34,41-45 According to Hidalgo et al’s²⁶ review, 22 studies have been performed to assess the validity and reliability of the B-PURAS. In these studies, the coefficient of consistency between observers was found to be between 0.83 and 0.99; the sensitivity was between 38.9% and 100%; the specificity was between 26% and 100%; the positive predictive value was 4%–100%; and the negative predictive value was 50%–100%.

In this study, most participants (79.5%) stated B-PURAS was easy to understand, while only 38.5% of them thought the same about the W-PURAS. For a PURAS to be easily comprehended, the statements should be clear and the scale itself should yield consistent results. The results of numerous studies^33,34,40-44 on B-PURAS with varying sample sizes have indicated the scale can consistently assess the risk of PUs successfully. In contrast, fewer validity and reliability studies have been performed on the W-PURAS; it has commonly been criticized for having a low level of reliability.³⁶ Based on the results of their methodological review, Papanikolaou et al⁴⁴ stated varying interpretations can evolve from the W-PURAS results because its subscales are not clear. In the current study, nurses’ opinions were compatible with these criticisms of the scale.

No true agreement was reached as to whether either scale was more practical. In this study, nurses thought the scales took an approximately equal amount of time to complete. Practicality and time for completion are interrelated — PURASs that can be quickly completed may be considered more practical. These results may be attributed to the fact the B-PURAS is easier to understand because it has fewer subscales than the W-PURAS, where “neurological deficits” and “medication” subscales require more nurse interpretation and the “skin type/visual risk areas” and “tissue malnutrition” subscales contain items for which multiple answers can be given. The majority of the participants stated they had difficulty choosing answer options when using the W-PURAS; some subscales require nurses’ interpretations and more than one option must be scored for a given item, which may have been influenced nurses’ answers.

Arguably, the most important findings of the present study are that nurses rated both scales as 7 (out of 10) on perceived predictive ability for PUs and that the items of these scales are not best prediction (10) for determining the risk of PUs in the patients they care for at the clinics. Nevertheless, more than half of the nurses believed PURASs that have established validity and reliability through empirical study should be used in the prevention of PUs. Nurses also recommended (with similar frequency for all items) that risk factors such as serum albumin level, blood pressure, amputation, infection status, and connection with ventilator should be added to these scales. Based on these findings, further studies aiming to develop new PURASs that include other risk factors in accordance with nurses’ recommendations should be performed to determine if additional independent risk factors should be considered.

More than half of the participants preferred the B-PURAS, with the remainder preferring the W-PURAS. Nurses who favored the B-PURAS ascribed their preference to its greater clarity and practicality, while those who favored the W-PURAS cited its comprehensiveness. The nurses working at the cardiovascular surgery ICU preferred the W-PURAS. In a literature review by Feuchtinger et al⁴⁵ on the risk of PUs in patients undergoing cardiovascular surgery, factors such as age; time spent on the operating table; having diabetes mellitus, multiple organ failure, anemia, or neurological conditions; and smoking status — all of which are subscales of the W-PURAS — were deemed significant. Hence, these nurses’ preferences may be associated with the fact there are more risk factors for PUs in cardiovascular surgery patients. Additionally, the W-PURAS layout includes a scoring system to determine risk level on its front side, while on the back side, items on the prevention of PUs, nursing practices, and classifications of PUs are presented. This arrangement provides guidance on nursing care, types of preventative aids associated with the 3 levels of risk status, wound assessment, and dressings.

Limitations

The nurses whose opinions were solicited were limited to those working in ICUs and orthopedics and physiotherapy-rehabilitation clinics of a single university hospital. As such, the views of nurses working at other clinics or in state and private hospitals were not included, which makes generalization of the results more difficult.

Another limitation is the small sample size and number of assessments. However, despite this, the general results were similar to those reported in national statistics.

Future research to determine whether nurses are able to score these scales accurately and then act according to patients’ results would be beneficial.

Conclusion

The findings of this descriptive pilot study indicated the majority of nurses working at clinics where the risk of PUs was high believed use of a PURAS is necessary, and as they became  familiar with the 2 PURAS utilized during the study, most of them preferred using the B-PURAS over the W-PURAS. The opinions of a larger sample of nurses who have used PURASs in clinics should be obtained and the findings of this study should be verified in a larger study population. 

References

1.         Lewis M, Pearson A, Ward C. Pressure ulcer prevention and treatment: transforming research findings into consensus based clinical guidelines. Int J Nurs Pract. 2003;9(2):92–102.

2.         Dealey C, Posnett J, Walker A. The cost of pressure ulcers in the United Kingdom. J Wound Care. 2012;21(6):261–266.

3.         Aydın KA, Karadag A. Assessment of nurses’ knowledge and practice in prevention and management of deep tissue injury and stage 1 pressure ulcer. J Wound Ostomy Continence Nurs. 2010;37(5):487–494.

4.         Clarke H, Bradley C, Whytock S, et al. Pressure ulcers: implementation of evidence-based nursing practice. J Adv Nurs. 2005;49(6):578–590.

5.         Ramanelli M. Science and Practice of Pressure Ulcer Management. London, England: Springer-Verlag; 2006.

6.         Bennett G, Dealey C, Posnett J. The cost of pressure ulcers in the UK. Age Ageing. 2004;33(3):230–235.

7.         Ayello EA, Braden B. How and why to do pressure ulcer risk assessment. Adv Skin Wound Care. 2002;15(3):125–133.

8.         Lyder CH, Wang Y, Metersky M, et al. Hospital-acquired pressure ulcers: results from the national Medicare Patient Safety Monitoring System study. J Am Geriatr Soc. 2012;60(9):1603–1608.

9.         Woodbury MG, Houghton PE. Prevalence of pressure ulcers in Canadian healthcare settings. Ostomy Wound Manage. 2004;50(10):22–38.

10.       Srinivasaiah N, Dugdall H, Barrett S. A point prevalence survey of wounds in northeast England. J Wound Care. 2007;16(10):413–419.

11.       Karadağ M, Gümüşkaya N. The incidence of pressure ulcer in surgical patients: a sample in Turkey. J Clin Nurs. 2005;15(4):413–421.

12.       Sayar S, Turgut S, Doğan H, et al. Incidence of pressure ulcers in intensive care unit patients at risk according to the Waterlow scale and factors influencing the development of pressure ulcers. J Clin Nurs. 2008;18(5):765–774.

13.       Katran HB. Pressure Sore Observation Frequency in a Surgical Intensive Care Unit and Addressing Risk Factors Effective on Pressure Sore Development [postgraduate thesis]. Istanbul, Turkey: Haliç University;2008.

14.       Akıl Y, Kabukçu N, Karadag A. Pressure Ulcer Point Prevalence Example: Çukurova University Balcalı Hospital, III. Presented at the National Wound Care Congress. Çesme, Turkey. November 26–29, 2008.

15.       Karadağ A, Gocmen Baykara Z, Özden G. Pressure Ulcers Point Prevalence Study in a University Hospital. Presented at the 15th National Internal Diseases Congress (Nursing program). Antalya, Turkey. October 2-6, 2013.

16.       Waterlow J. Prevention is cheaper than cure. Nurs. Times. 1988;2284(25):69–70.

17.       Keast DH, Parslow N, Houghton PE, Norton L, Fraser C. Best practice recommendations for the prevention and treatment of pressure ulcers: update 2006. Adv Skin Wound Care. 2007;20(8):447–460.

18.       Schoonhoven L, Defloor T, Grypdonck, MHF. Incidence of pressure ulcers due to surgery. J Clin Nurs. 2002;11(4):479–487.

19.       Karadag A. Pressure ulcers: evaluation, prevention and treatment. Cumhuriyet Univ Nurs Coll J. 2003;7(2):41–46.

20.       Brandeis GH, Berlowitz DR, Katz P. Are pressure ulcers preventable? A survey of experts. Adv Skin Wound Care. 2001;14(5):244–248.

21.       Bergstrom N, Braden B, Laguzza A, Holman V. The Braden Scale for predicting pressure sore risk. Nursing Research. 1987;36(4):205–210.

22.       Defloor T, Grypdonck M. Pressure ulcers: validation of two risk assessment scales. J Clin Nurs. 2005;14(3):373–382.

23.       Özdemir H, Karadag A. Prevention of pressure ulcers: a descriptive study in 3 intensive care units in Turkey. J Wound Ostomy Continence Nurs. 2008;35(3):293–300.

24.       Lindgren M, Unosson M, Krantz AM, Ek AC. A risk assessment scale for the prediction of pressure sore development: reliability and validity. J Adv Nurs. 2002;38(2):190–199.

25.       Anthony D, Parboteeah S, Saleh M, Papanikolaou P. Norton, Waterlow and Braden scores: a review of the literature and a comparison between the scores and clinical judgement. J Nurs. 2008;17(5):646–653.

26.       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.

27.       Agency for Health Care Policy and Research (AHCPR) Supported Clinical Practice Guidelines. Pressure Ulcers in Adults: Prediction and Prevention. Available at: www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=hstat2.section.4521. Accessed May 22, 2011.

28.       European Pressure Ulcer Advisory Panel and National Pressure Ulcer Advisory Panel. Treatment of Pressure Ulcers: Quick Reference Guide 2009. Available at: www.epuap.org/guidelines/Final_Quick_Treatment.pdf. Accessed May 27, 2011.

29.       Murray LD, Magazinovic N, Stacey MC. Clinical Practice Guidelines for the Prediction and Prevention of Pressure Ulcers. Available at: www.awma.com.au/journal/0903_01.pdf. Accessed May 27, 2011.

30.       Wound, Ostomy and Continence Nurses Society. Guideline for Prevention and Management of Pressure Ulcers. Glenview, IL: Wound, Ostomy and Continence Nurses Society;2003. Available at: www.guideline.gov/summary/summary.aspx?doc_id=3860&nbr=003071&string=pre.... Accessed May 27, 2011.

31.       Nursing Regulation. Available at: www.turkhemsirelerdernegi.org.tr/menu/yonetmelikler/hemsirelik-yonetmeligi. Accessed July 22, 2012.

32.       Regulation on Home Care Services 2005. Available at: www.saglik.gov.tr/TR/belge/1-337/yonetmelikler.html. Accessed July 22, 2012.

33.       Oğuz S, Olgun N. Determination of patient risks by Braden Scale and determination of effectiveness of planned nursing care for prevention of pressure sore. Hemşirelik Forumu Dergisi. 1998;1(2):131–135.

34.       Pınar R, Oğuz S. Reliability and Validity Testing of Norton and Braden Pressure Sore Evaluation Scales in the Same Patient Group Confined to Bed. VI. National Nursing Congress. Ankara, Turkey: Damla typography; 1998:172-175. 

35.       Avşar P, Karadağ A, Alaca R. Waterlow Validity and reliability study of pressure ulcer risk evaluation. VI. Wound Care Congress Book. Antalya, Turkey; 2011:13.

36.       Walsh B, Demsey L. Investigating the reliability and validity of the Waterlow Risk Assessment Scale: a literature review. Clin Nurs Res. 2011;20(2):197–208.

37.       Waterlow J. Pressure sores: a risk assessment card. Nurs Times. 1985;81(48):49–55.

38.       Balzer K, Kremer L, Junghans A, et al. What patient characteristics guide nurses’ clinical judgement on pressure ulcer risk? A mixed methods study. Int J Nurs Stud. 2014;51(5):703–716.

39.       Braden B, Bergstrom B. A conceptual schema for the study of the etiology of pressure sores. Rehabil Nurs. 1987;12(1):8–12.

40.       Seongsook J, Ihnsook J, Younghee L. Validity of pressure ulcer risk assessment scales; Cubbin and Jackson, Braden and Douglas Scale. Int J Nurs Stud. 2004;4(2):199–204.

41.       Pang SM, Wong TK. Predicting pressure sore risk with the Norton, Braden and Waterlow scales in a Hong Kong rehabilitation hospital. Nurs Res. 1998;47(3):147–153.

42.       Jalali R, Rezaie M. Predicting pressure ulcer risk: comparing the predictive validity of 4 scales. Adv Skin Wound Care. 2005;18(2):92–97.

43.       Serpa LF, Santos V, Peres G, Cavicchioli M, Hermida M. Validity of the Braden and Waterlow subscales in predicting pressure ulcer risk in hospitalized patients. Appl Nurs Res. 2010;24(4):6–12.

44.       Papanikolaou P, Lyne P, Anthony D. Risk assessment scales for pressure ulcers: a methodological review. Int J Nurs Stud. 2007;44(2):285–296.

45.       Feuchtinger J, Halfens JG, Dassen T. Pressure ulcer risk factors in cardiac surgery: a review of the research literature. Heart Lung. 2005;34(6):375–385.

Potential Conflicts of Interest: This research was supported by Scientific Research Projects of Gazi University, Ankara, Turkey. (Project No.47/2011-0).

Ms. Avsar is a research assistant, Yıldırım Beyazıt University Faculty of Health Sciences, Department of Nursing, Ankara, Turkey. Dr. Karadag is a Professor, Koç University School of Nursing, Istanbul, Turkey. Please address correspondence to: Pinar Avsar, RN, MSN, Faculty of Health Science, Yıldırım Beyazıt University, Bilkent Yolu 3.Km Bilkent/Çankaya, Ankara 06010 Turkey; email: p.avsar.ank@gmail.com.

Abstract

Research suggests high-voltage, pulsed-current electric therapy (HVPC) is safe and effective for treating chronic wounds, and some data suggest silver- and collagen-based dressings may facilitate healing. A combination therapy utilizing both HVPC and silver-collagen dressing may present clinical advantages. To explore the effect of the combined therapy for chronic full-thickness wounds, a prospective, consecutive case series study was conducted. All participants were adults with wounds of at least 6 weeks’ duration.

After obtaining informed consent, patient and wound characteristics were obtained, wounds were assessed and measured, and patients received 2 to 3 HVPC treatments per week followed by application of the silver- and collagen-based dressing for a period of 2 weeks. Data were analyzed descriptively, and changes in wound size and volume from baseline were analyzed using Wilcoxon Signed Rank Test. The dressings were saturated with normal saline, used simultaneously during the 45-minute HVPC treatment, and left on top of the wound after treatment. The HVPC electro pads (stainless steel electrodes with a sponge interface) also were moistened with normal saline and the cathode placed on top of the wound. If the patient had more than 1 wound on the same leg, the anode was placed on the additional wound (otherwise over the intact skin nearby). Secondary dressings (eg, foam and/or gauze) were used as clinically appropriate, and a 4-layer compression wrap was used, if indicated, for patients with venous ulcers. Ten (10) patients (3 women, 7 men, 57.30 ± 9.70 years old with 14 wounds of 273.10 ± 292.03 days’ duration before study) completed the study and were included in the final analyses. Average wound surface area decreased from 13.78 ± 21.35 cm² to 9.07 ± 16.81 cm² (42.52% ± 34.16% decrease, P = 0.002) and wound volume decreased from 3.39 ± 4.31 cm³ to 1.28 ± 2.25 cm³ (66.84% ± 25.07% decrease, P = 0.001). One (1) patient was discharged with complete wound closure. No serious adverse events were noted, but a diagnosis of osteomyelitis in 1 patient and increased pain in a patient with significant Reynaud’s syndrome suggest clinicians should be cautious using HVPC in these instances. The combined intervention utilizing both HVPC and silver-collagen dressing was effective in the treatment of chronic full-thickness wounds in this patient population. Controlled clinical studies of longer duration are needed to further explore the safety, effectiveness, and efficacy of this treatment. 

Abstract

Diabetic foot ulcers (DFUs) have a significant impact on patient quality of life. A prospective, descriptive pilot study was conducted between May 2012 and December 2013 through the dermatology outpatient unit in a Brazilian hospital to evaluate the clinical benefits of using Calendula officinalis hydroglycolic extract in the treatment of DFUs.

Patients diagnosed with a stable neuropathic ulcer of  >3 months’ duration; ranging in size from 0.5–40 cm²; without osteomyelitis, gangrene, bone exposure, cancer, or deep tissue infection; ages 18–90 years; with adequate glycemic control and no history of an allergy to C. officinalis were enrolled. Patients provided demographic and diabetes-related information and were evaluated biweekly for 30 weeks or until healing (ie, full epithelialization with no wound drainage). DFUs were measured and clinically examined for microbiological flora and presence of odor, tissue type (eg, granulation, fibrin sloth, necrosis), exudate, and retraction rate using planimetry images. Patients’ blood tests and neuropathic pain assessment (the latter by clinician-directed questionnaire) were performed at baseline and the end of treatment; pain also was assessed during dressing changes using a 10-point rating scale. Patients’ ulcers were treated twice daily with C. officinalis hydroglycolic extract spray solution and covered with saline-moistened, sterile, nonadherent gauze and bandages followed by foot offloading with adequate protective footwear. Patients received their first treatment in the clinic then performed care at home. From a potential population of 109 patients, 25 did not meet the inclusion criteria. Of the remaining 84 participants enrolled, 43 withdrew before study completion; cited reasons included lost to follow-up (16), medical judgment (2), failure to attend >3 scheduled visits (17), protocol violation (5), and death (3). Forty-one (41) — 17 women, average age 62 years (range 44–82 years), average glycemic level 153 mg/dL (range 82–395 mg/dL), most (34) with Wagner type 1 ulcers — completed the study. The proportions of patients who achieved complete wound closure after 11, 20, and 30 weeks of treatment was 54%, 68%, and 78%, respectively; mean healing time was 15.5 ± 6.7 weeks. When individual weekly healing rates (the percentage reduction in wound area per week) were corrected for variability in initial DFU area, the values were nearly 6-fold higher for complete wound closure (7.8% ± 3.6%) than for incomplete wound closure (1.4% ± 0.7%) (Student t-test; P = 0.001). After 30 weeks of treatment, the number of colonized wounds decreased from 29 at baseline to 5, and the number of odorous wounds decreased from 19 to 1. Ulcer bed planimetry data showed a significant reduction in the amount of exudate, fibrin slough, and necrotic tissue after the treatment with C. officinalis hydroglycolic extract (χ² test; P = 0.001). No adverse events were observed during treatment. The study findings suggest C. officinalis extract is safe and has a beneficial effect on DFU healing. Randomized, controlled studies using C. officinalis hydroglycolic extract are warranted to confirm its safety and establish its clinical efficacy and effectiveness for the topical treatment of DFUs.

Diabetic foot syndrome is a common and severe complication worldwide with a cumulative lifetime incidence of up to 25%. The rapidly increasing rates of diabetes make diabetic foot ulcers (DFUs) a major public health issue. These ulcers have been shown to reduce patient quality of life and may ultimately lead to severe pain, prolonged hospitalization, and/or amputation of the lower extremities.¹ 

Chronic DFUs are complicated by delayed wound healing processes related to impaired glucose metabolism and neurovascular complications.² The standard treatment plan for DFUs is designed to eliminate infection; maintain a moist wound bed; and offload pressure with protective footwear such as custom cushioned shoes, diabetic boots, and forefoot- and heel-relief shoes, as well as orthotic walkers, wheelchairs, and crutches. Periodic debridement to facilitate healing and topical medication such as preparations made of recombinant human platelet-derived growth factor are also important.³ According to a meta-analysis,⁴ many patients with persistent DFUs do not respond to commonly provided care. In such patients, a prospective, randomized controlled study⁵ reports the only available option to prevent amputation is skin replacement therapies. Because skin replacement therapy is expensive and not widely available, more effective treatments for chronic DFUs are desperately needed for patients with diabetes. 

A systematic review⁶ that included 60 studies (N = 24,747 patients) suggested topical medications and dressings such as cadexomer iodine, zinc oxide, hydrocolloids, alginates, and hydrogels provide no additional benefit to interventions used to treat DFUs such as sharp debridement, larvae therapy, hyperbaric oxygen, skin grafts, electrical and magnetic stimulations, and ultrasound. However, most topical pharmacological agents that are currently available or in development generally address a single aspect of DFU pathology. Examples of research include a randomized, double-blind, placebo-controlled (RDBPC) study⁷ (N = 87) of abnormal coagulation involving dalteparin, a case series⁸ (N = 21) using homologous platelet gel, a RDBPC study⁹ (N = 62) in which infection was treated using a photo-activated gel containing the antimicrobial agent RLP068, and a RDBPC study¹⁰ (N = 40) among patients with xerosis treated with a urea-lactic acid moisturizer. 

An emerging trend involves identifying natural extracts with healing properties that address all aspects of DFUs, especially with the new extraction methods designed to optimize their yield, purity, and bioactivity (eg, anti-inflammatory, wound healing, and antitumor properties).^11–15 A prospective, randomized controlled trial¹⁶ with 37 patients with diabetes demonstrated topical kiwifruit extract reduced the size of DFUs by ~50% in 3 weeks compared to patients who received the standard treatment of surgical debridement, blood sugar control, and oral antibiotic therapy. Additionally, in a prospective, randomized controlled study,¹⁷ oak bark extract (QRB7) was found to be more efficient than polyherbal silver sulfadiazine cream for reducing the size of DFUs in 40 patients with diabetes, with 72.5% and 54.7% reduction in wound size after a 6-week treatment. However, none of these agents was proven to support complete wound closure (the duration of the study was not long enough).

The genus Calendula has been recognized for decades as a rich source of medicinal plants with strong healing potencies.¹⁶ Among them, Calendulaofficinalis flowers are used in numerous over-the-counter botanical preparations for external use as an anti-inflammatory wound healing agent and indicated for the treatment of herpes, solar erythemas, burns, and dermatitis. The phytopreparation Plenusdermax^® (Phytoplenus Bioativos S.A., Pinhais, Paraná, Brazil) from C. officinalis is rich in various bioactive compounds with wound healing and anti-inflammatory properties, including terpene alcohols, monoester triterpenoids (ie, faradiol and arnidiol calenduladiol), and antioxidant flavonoids (ie, quercetin, rutin, kaempferol, and narcissine). According to animal studies,^18–22 the monoesters triterpenoids (ie, isopropyl myristate, palmitate, and laurate) are considered the most effective topical agents in terms of anti-inflammation and wound healing capacity. However, the effects of hydroglycolic extract have not been tested on chronic diabetic ulcers.

Study Purpose

A prospective, descriptive clinical study was conducted to evaluate the effect of C. officinalis hydroglycolic extract on the healing rate of DFUs in patients with diabetes until complete wound closure and during a 30-week follow-up period to monitor the long-term effects of the treatment.

Methods and Procedures

Participants. The study was conducted between May 2012 and December 2013 in the outpatient unit of the Department of Dermatology, Hospital da Santa Casa de Misericórdia de Curitiba, Pontifícia Universidade Católica do Paraná (PUC-PR), Brazil. One hundred, nine (109) patients with diabetes and foot ulcers from the Curitiba metropolitan region were screened according to the inclusion and exclusion criteria presented in Table 1. The study was approved by the Institutional Research Ethics Committee of the PUC-PR (protocol no. 22.670) and was registered in Plataforma Brazil with the National Commission of Ethics in Research (no. 0.1051212.0.0000.0020). Written informed consent was obtained from all patients before screening. 

At the initial visit, a full medical history and assessment of the patients’ present condition were recorded. Study variables were collected on a paper/pencil instrument and evaluated; information included sociodemographic data, clinical history, and clinical evaluation of the wounds and amputations. The diabetic status of patients (ie, type, duration, glycemic management, including the determination of plasma glucose and glycated hemoglobin levels, current activity level, nutritional status, neuropathic pain assessment,²³ and blood tests) also was recorded. Blood test results included glucose levels, glycated hemoglobin, serum albumin, blood count, erythrocyte sedimentation rate, and ulcer bacterioscopy and culture were obtained at baseline and at the study conclusion.

Treatment with C. officinalis hydroglycolic extract. All enrolled patients were treated with the C. officinalis hydroglycolic 4% extract. The extract composition included C. officinalis L. 4% and excipients (butylated hydroxytoluene, parabens, ethanol, polyethylene glycol, and purified water). The spray solution was prepared by authorized compounding pharmacies using commercial ingredients. The certificated analysis of the C. officinalis hydroglycolic extract included the following compounds from dichloromethane fraction: β-amyrin (6.7%), lupeol (4.7%), ψ-taraxasterol (8.1%), calenduladiol monoesters (5.5%), arnidiol monoesters (15.7%), faradiol monoesters (35.2%), others (24.1%), and from aqueous fraction: total flavonoids content of 120 mg/mL. Bioactivity was previously demonstrated using high-performance liquid chromatography.^19,20 The DFU was cleaned twice daily with 25 mL of sterile physiological saline solution, after which 0.018 mL/cm² of wound area of C. officinalis extract was sprayed on the wound. After allowing the solution to dry in the wound bed for 5 minutes, sterile, nonadherent, saline-moistened gauze and bandages were applied. Patients were provided cushioned footwear, diabetic boots, crutches, and wheelchairs to offload the affected areas. None of the patients used additional wound healing medication, phytopreparation, hydrogels, hydrocolloids, or supportive therapy (ie, electrotherapy, vacuum therapy, laser therapy, phototherapy). The nursing team instructed patients or their caregivers to use sterile gauze dressings after each C. officinalis extract application and to avoid bearing weight on the affected limb by using adequate footwear. Patients received their first treatment in clinic then performed care at home. The nursing team monitored whether the instructions for treatment were adequately followed through weekly phone calls to patients or their caregivers. Footwear such as cushioned shoes and diabetic boots was distributed by the local public health system and customized for the study patients. 

Assessment of C. officinalis hydroglycolic extract on DFU healing. DFUs were assessed at baseline and then twice a week during visits by the nursing staff. At each visit, the DFUs were clinically assessed for appearance, size, and size reduction rate using photographs analyzed by computerized planimetry, according to a methodology described previously.²⁴ Photographs of each ulcer were taken with a Sony DSC-H1 digital camera (Sony USA, New York, NY, USA) at every nurse visit. Image capture was standardized using a tripod frame to support the camera fixed perpendicularly to the ulcer. A circular self-adhesive label with a known area was placed close to the ulcer as a calibrator used by the software for area quantification. Digital images obtained were analyzed using Image J^® software (National Institutes of Health, Bethesda, MD, USA). The software delineates the margin of each ulcer and uses different shades of color to define and calculate areas with different types of tissue.

The clinical appearance of the ulcers was assessed for different tissue types such as granulation, epithelialization, fibrin slough, and necrosis. The presence of a specific tissue type was confirmed if computerized planimetry showed a relative area >20% of the total ulcer area. The presence of exudate was confirmed by the appearance of moist gauze during dressing changes. The presence of odor was noted. The ulcer was classified according to the Wagner Grading System,²⁵ which was used to establish DFU depth and presence of infection. Microbiological flora of the DFUs was identified using a biogram/antibiogram of a swab from the wound bed. A validated quantitative swab technique was performed to assess wound contamination and infection.²⁶ A wound was considered infected if a high level of bacteria (1 × 10⁶ CFU) and signs of increased erythema, exudate, odor, warmth, edema, and/or pain were present. Patients with infected wounds were treated with systemic antimicrobials; patients who had a fever and other complications from wound infections during the treatment were discontinued during the study.

Complete wound closure (ie, healing) was defined as full epithelialization of the ulcer with the absence of drainage. Patients were monitored biweekly by the study physician and trained nursing staff for 30 weeks or until healing. Healing was confirmed 1 week following closure, and the patient was monitored for another 2 weeks.

If a patient experienced an allergic reaction to the C. officinalis hydroglycolic extract, an evaluation by the principal investigator was conducted, and the patient was removed from the clinical test. 

Pain assessment. Pain was assessed in 2 ways. Patients were asked to complete the paper/pencil Neuropathic Pain Scale Questionnaire (NPSQ) on the first visit (baseline) and after completion of the 30-week treatment under the guidance of the nursing staff for evaluation and discrimination of neuropathic pain, according to the methodology described previously.²³ Briefly, patients were rated for numbness (no numbness sensation = 0, worst numbness imaginable = 100), tingling pain (no tingling pain = 0, worst tingling pain imaginable = 100), and increased pain due to touch (no increase at all = 0, greatest increase imaginable = 100). The NPSQ scores for these symptoms were multiplied by its specific coefficients, summed, and then subtracted by a constant to obtain the discriminant function score (DFS). DFS <0 predicted no neuropathic pain, whereas DFS ≥0 indicated neuropathic pain.

For pain related to DFU dressing changes, patients were asked to rate their pain using a numerical rating scale (NRS) that ranged from no pain (0) to the worst possible pain (10).²⁷ The NRS questionnaire was completed at baseline and then once a month during the nursing visits.

Statistical analysis. Descriptive and analytical data were collected and stored using a Microsoft Office Access 2010 database, drawn from documents used in medical evaluations and nursing. Data were analyzed by importing Access files to the database to the Statistical Package for Social Sciences (SPSS) version 20 (SPSS, Inc, Chicago, IL, USA). All data were verified by double key entry as entered and stored in the Access database. The Access database was stored in a computer with an Intel Core 2 Duo processor, 2.2 GHz, and 2G of RAM.

Quantitative variables were analyzed using descriptive statistics. Unless otherwise indicated, data are presented as mean ± standard deviation. Qualitative variables were described as frequencies and percentages.

To evaluate the association between gender and outcomes of healing at 30 weeks, Fisher’s exact test was used. The wound contraction per week (WCw) was calculated as the baseline wound area (Ai) − final wound area (Af) ÷ the number of weeks.²⁸

The percentage reduction in wound area per week (%RWAw) was calculated as follows:

To compare the groups defined by healing within 30 weeks, the quantitative variables were analyzed using Student’s t-test, and the nonparametric variables were analyzed using the Mann-Whitney U test. Time to complete ulcer healing was measured as the number of days from the start of treatment to the date a patient achieved complete wound closure. Wound healing was observed on a weekly basis, and the time until complete healing was estimated by calculating a cumulative frequency chart. P<0.05 was considered to be statistically significant.

Results

The participants’ flow through the study is presented in Figure 1. Of the 109 subjects enrolled, 25 did not meet the inclusion criteria. Of the remaining 84 participants enrolled into the treatment phase, 43 withdrew before study completion. The main reasons for withdrawal were lost to follow-up (16), medical judgment (2), failure to attend >3 scheduled visits (17), violation of the protocol (5), and death (3). Three (3) patients died from complications due to diabetes (eg, DFU, acute myocardial infarction, kidney failure, and stroke). Forty-one (41) patients completed the trial and were included in the analysis.

Baseline characteristics. Patient demographics and ulcer characteristics at baseline and after the 30-week treatment are presented in Table 2. Of 41 patients treated with C. officinalis hydroglycolic extract, 17 (41%) were female and 24 (59%) were male. The average age of the patients was 62 (range 44–82) years. Laboratory clinical tests showed 35 (80.5%) were hyperglycemic with an average blood glucose level of 152.9 ± 76.01 mg/dL (range 82–395 mg/dL). Glycated hemoglobin was in the range of 6.4%. Serum albumin and hemoglobin levels at baseline of the patients who achieved total wound closure were 4.03 ± 0.49 g/dL and 12.9 ± 1.37 g/dL, respectively, which were not statistically different (P = 0.509, Student’s t-test) from those that did not achieve complete wound healing (albumin = 4.24 ± 0.32, hemoglobin = 12.7 ± 1.75 g/dL). 

Most patients (34) exhibited Wagner type 1 ulcers (82.9%), which were generally located in the plantar, lateral face, and malleolus regions. All DFUs were characterized as chronic lesions because they were present an average of 71.1 ± 41.7 (range 17–156) weeks before the onset of this study. The baseline wound area was 8.68 ± 8.55 cm² (range 1.2–43.1 cm²). The biogram/antibiogram tests from the swabs collected from the wound beds showed 31 (76%) of the ulcers were either colonized or infected. Twenty (20) DFUs (48.8%) showed high levels of bacteria ( >1 × 10⁶ CFU) and were considered infected. The predominant clinical signs of the infected wounds were odor, exudate, erythema, and edema. Eleven (11) DFUs (26.8%) were colonized with low bacteria level and were not considered infected. Staphylococcus aureus was the predominant pathogen (11, 27%), followed by Pseudomonas sp. (4, 10%), Klebsiella sp. and Escherichia coli (3, 8% each). Of the 33 patients with colonized DFUs at the beginning of the study, 21 were treated with ciprofloxacin 500 mg twice daily for 30 days and 12 with gentamycin 80 mg intramuscularly once a day for 10 days. Two (2) patients did not satisfactorily respond to antibiotics, so they were excluded from the study.

Ulcer area reduction and healing rate. The time-course analysis indicated a linear increase in the proportion of patients achieving complete would closure after 11–30 weeks of treatment (see Figure 2). Thus, a minimum treatment period of 10 weeks was required for complete wound closure, and the average healing time was approximately 15.5 ± 6.7 weeks. After 11 weeks of treatment, 22 (54%) of the wounds were completely healed, with an average reduction in the wound area of 64% and noticeable improvements in the ulcer appearance from the baseline, including an increase in epithelialization and reduction of exudate, fibrin slough, necrosis, edema, erythema, and odor. After 20 weeks, 28 wounds (68%) were completely healed; after 30 weeks, 32 patients (78%) achieved complete healing and the remaining 9 (22%) achieved an overall reduction in the wound area of 75%. Figure 3 illustrates the process of diabetic ulcer healing in 3 patients treated with C. officinalis hydroglycolic extract. Photographs of patients’ DFUs showed complete epithelialization without apparent excess of anomalous tissue such as keloids and hypertrophic scars. 

Patients were separated into complete DFU closure (coDFU group) and incomplete DFU closure (inDFU group) after 30 weeks of treatment. The inDFU group had mean baseline DFU areas (mean 10.28 ± 6.91 cm²; median: 8.43 cm²) similar to those of the coDFU group (mean 8.23 ± 9.02 cm²; median 5.72 cm²) (P = 0.105, Mann-Whitney U test) (see Table 3). In contrast, the wound contraction rate for the coDFU group was 3-fold higher (54.4 mm²/week; range, 5.2–168.7 mm²/week) than for the inDFU group (16.1 mm²/week; range 2.3–64.3 mm²/week) (Mann-Whitney U test; P = 0.001) (see Table 3). When the individual healing rates were corrected for baseline DFU area, the rates were nearly 6-fold higher in the coDFU group (7.75 ± 3.37%) than in the DFU group (1.38 ± 0.69%) (Mann-Whitney U test; P = 0.001). 

Ulcer infection and inflammation. After 30 weeks of treatment with C. officinalis hydroglycolic extract, the total number of colonized DFUs significantly decreased from 29 (70.7%) to 5 (12.1%) (χ2 test; P = 0.012; see Table 2). C. officinalis extract was equally effective against all pathogens identified in the DFUs. Accordingly, the proportion of wounds presenting with unpleasant odor at baseline (19, 46.3%) was considerably lower after 2 weeks and ultimately decreased to1 (2.4%) after completion of the treatment. Ulcer bed planimetry data showed a significant reduction of exudate, fibrin slough, and necrotic tissue after the treatment with C. officinalis hydroglycolic extract (χ² test; P = 0.001) (see Table 2). 

Pain assessment. Data from the NPSQ showed patients had a positive DFS for neuropathic pain of 0.543 ± 0.213 at baseline. All patients had a positive score for tingling pain, numbness, and increased pain due to touch. After 30 weeks of treatment, the average score for neuropathic pain was positive (0.552 ± 0.200) with no significant differences from the baseline score. The average patient pain score at baseline was 6.953 ± 2.160; at the end of 30 weeks of treatment, this was significantly reduced to 0.767 ± 0.477 (χ² test; P = 0.001).

No adverse events with the C. officinalis hydroglycolic extract were observed during the treatment.

Discussion

C. officinalis hydroglycolic extract for the treatment of DFUs was assessed by having patients use it in their regular life at home with minimal influence from hospital/outpatient interventions. All patients received their first treatment in clinic then performed care at home. 

A systematic review of the literature⁴ that included 10 clinical trials on the performance of standard DFU treatments reported completely healed wounds in an average of 24% of patients at 12 weeks and in 30% of patients at 20 weeks; these data are used to benchmark DFU wound treatment therapies. The current study demonstrated 54% of DFUs were completely healed at 11 weeks and 68% at 20 weeks using C. officinalis extract. The average healing time to complete reepithelialization was approximately 16 weeks. At the study’s conclusion (30 weeks), 78% of all wounds had achieved complete closure. However, it should be noted that most studies utilized an intent-to-treat analysis method and the current study did not, which limits the ability to compare the results.

Several therapies are currently used to treat DFUs, including topical active solutions and ointments, silver, alginate- and cellulose-containing dressings, acellular protein dressings, autologous platelet-rich plasma, and bioengineered cell-based tissue grafts.²⁹ Table 4 shows the percentage of healed DFUs in several previous prospective studies with different treatments.^4,5,30-37 A direct comparison of the healing rates between the studies conducted with different therapies is not possible because of the differences in the demographics, comorbidities, wound complexities, study endpoints, and data analysis methods used. In general, prospective, randomized controlled and retrospective studies involving advanced therapies such as acellular protein dressings, autologous platelet-rich plasma, and bioengineered cell-based tissue grafts for treating DFUs achieve complete healing in 45% to 68% of wounds in 12 weeks²⁹; however, with commonly used methods of care, this rate is roughly 30%.⁴ The average percentage of completely healed wounds in the present study is comparable to these other effective therapies.

The anti-inflammatory and healing properties of C. officinalis are associated with a greater diversity of bioactives, specifically triterpene alcohols, triterpene oligoglycosides, monoesters, triterpenoids, and flavonoids.^{18–22,38–41} Chromatographic analysis from the dichloromethane fraction of C. officinalis flowers demonstrated 9 anti-inflammatory bioactive triterpenoids (ie, faradiol-3-O-palmitate, faradiol-3-O-myristate, faradiol-3-O-laurate, arnidiol-3-O-palmitate, arnidiol-3-O-myristate, arnidiol-3-O-laurate, calenduladiol-3-O-palmitate, calenduladiol-3-O-myristate, and calenduladiol-3-O-laurate) are commonly found in many varieties of Calendula flowers.^19,20,41 The hydroglycolic extract of C. officinalis used in the present study was rich in these compounds.

Generating new blood vessels in the wound is an essential component of the wound healing process. Observational cohort studies^42,43 of diabetic neuropathic foot ulcers indicated angiogenic activity may be insufficient for promoting expansion of new blood vessels into the wound site and restricting the entry of inflammatory cells and oxygen supply. The wound healing properties of C. officinalis may be associated with the activation of angiogenesis in the injured tissue. In addition to the known anti-inflammatory and antiseptic activity of the C. officinalis extract, the authors of the current study suggest the components present in C. officinalis extract, such as the monoesters triterpenoids, are able to stimulate vascular growth in DFUs through the release of angiogenic factors, particularly the vascular endothelial growth factor (VEGF), thus promoting granulation, tissue growth, and epithelialization. Although the presence and activity of VEGF in the wound bed through sampling and analysis of ulcer fluids and tissues was not possible in this study, evidence from animal studies^44,45 supports angiogenesis is stimulated in the presence of C. officinalis extract: one study⁴⁴ used aqueous extract from C. officinalis flowers to show an induction of vascularization in the chick chorioallantoic membrane and one study⁴⁵ used C. officinalis extract to demonstrate accentuated angiogenic activity in both chicken chorioallantoic membranes and rat cutaneous wound models.

The importance of matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs (TIMPs) to the integrity of the extracellular matrix (ECM), which tightly control its metabolism in the normal healing process, has been shown in cell culture study.⁴⁶ These proteolytic enzymes have been shown in animal studies⁴² to act on ECM, enabling migration of cells into the wound site and penetration of new blood vessels, which results in the deposition of new ECMs and the formation of new tissue, facilitating reepithelialization and wound contraction. In diabetic ulcers, an excessive activity of MMPs on ECM and deficiency of TIMPs result in the destruction of new ECMs, which consequently always delays wound healing. In a preclinical study, C. officinalis extract was used to prevent ultraviolet irradiation-induced oxidative stress in rat skin and was observed to increase the activity and secretion of MMPs 2 and 9, which may be associated with procollagen synthesis, regulation of inflammatory responses, and rearrangement of damaged skin.⁴⁷ Studies^39,48 using cultures of human and mouse fibroblasts demonstrated extracts of C. officinalis stimulated fibroblast proliferation and cellular metabolism through an increase in mitochondrial dehydrogenase activity, suggesting that several compounds of C. officinalis, particularly monoesters and triterpenoids, possess synergistic action in the reepithelialization process. In the present study, the observed removal of necrotic tissue in favor of granulation tissue, significant reduction in bacterial counts, and rate of epithelialization suggest bioactive components of C. officinalis extract can stimulate the entire tissue repair process.

The observed reduction in unpleasant odor, edema, erythema, exudate, bacterial colonization, and necrotic tissue may be due to the anti-inflammatory and bacteriostatic properties of the C. officinalis extract. Extracts of C. officinalis have been shown in in vitro microbiology study⁴⁹ to have bactericidal and fungicidal effects against microorganisms isolated from hospital patients. The extract used in the present study showed anti-inflammatory, antimicrobial, and wound healing properties, which corroborate with previous clinical and experimental studies using C. officinalis phytopreparations.^49–52 The clinical benefits of C. officinalis hydroglycolic extract in healing DFUs may be due to its chemical constituents such as monoesters, triterpenoids, triterpene alcohols, triterpene oligoglycosides, and flavonoids, which may act synergistically to promote wound healing.

It also may be advantageous that C. officinalis hydroglycolic extract is an aqueous preparation that leaves no adherent solid residue on the wound bed. This facilitates the process of cleaning and dressing changes and minimizes friction and potential small trauma to the emergent granulation tissue. 

Limitations

This study was limited by the small number of patients meeting the inclusion/exclusion criteria, which prevented the adequate fractionation of subgroups with a more regular baseline wound size. The intent-to-treat method of analysis was unsuitable for this study because a large majority of dropouts and noncompliant events (n = 33) occurred in the early phase of the research (first 3 weeks), which may have drastically diluted the treatment effect observed over 30 weeks. However, not using the intent-to-treat analysis method increases the risk of overestimating the effect of treatment. 

Conclusion

In this patient population, the use of extract of C. officinalis hydroglycolic extract was associated with a high percentage (78%) of DFUs healed. Although not a direct comparison, the proportion of healed DFUs was 2 to 3 times higher than the reported benchmark for assessing topical treatments for DFUs. No adverse events occurred, and the percentage of wounds with an unpleasant wound odor and wound pain ratings were significantly reduced at the end of the treatment period. No adverse events occurred. A randomized, controlled trial with a greater number of patients is needed to confirm the clinical efficacy of C. officinalis extract for the treatment of DFUs. Although pain at baseline and final assessment was reported, it is not known whether reduced average pain scores were the result of treatment or from the wound being healed. 

Acknowledgments

The authors acknowledge Alvaro Quintas, MD from PUC-PR for his help on the project; Marcia Olandoski, PhD for the statistical analysis; and Luiz Carlos Pereira, MD, Ney Alencar, MD, and Sergio Tarlet, MD from the Department of Dermatology at the Hospital, Santa Casa de Misericórdia of Curitiba, for their expert dermatology advice. The authors also thank Maurício Centa, MD from Hospital São Lucas and the nurse team, especially Flavia Pontes, NA for helping with the patients.

References

1. Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers. Clin Rev. 2005;293(2):217–228.

2. Tsourdi E, Barthel A, Rietzsch H, Reichel A, Bornstein SR. Current aspects in the pathophysiology and treatment of chronic wounds in diabetes mellitus. Biomed Res Int. 2013;2013:1–6. 

3. Steed DL, Attinger C, Colaizzi T, Crossland M, Franz M, Harkless L, et al. Guidelines for the treatment of diabetic ulcers. Wound Repair Regen. 2006;14(6):680–692.

4. Margolis DJ, Kantor J, Berlin JA. Healing of diabetic neuropathic foot ulcers receiving standard treatment. A meta-analysis. Diabetes Care. 1999;22(5):692–695.

5. Edmonds M. Apligraf in the treatment of neuropathic diabetic foot ulcers. Int J Low Extrem Wounds. 2009;8(1):11–18.

6. Hinchliffe R, Valk G, Apelqvist J, Armstrong D, Bakker K, Game F, et al. A systematic review of the effectiveness of interventions to enhance the healing of chronic ulcers of the foot in diabetes. Diabetes Metab Res Rev. 2008;24(1 suppl):S119–S144.

7. Kalani M, Silveira A, Blombäck M, Apelqvist J, Eliasson B, Eriksson J, et al. Beneficial effects of dalteparin on haemostatic function and local tissue oxygenation in patients with diabetes, severe vascular disease and foot ulcers. Thromb Res. 2007;120(5):653–661. 

8. Shan G-Q, Zhang YN, Ma J, Li YH, Zuo DM, Qiu JL, et al. Evaluation of the effects of homologous platelet gel on healing lower extremity wounds in patients with diabetes. Int J Low Extrem Wounds. 2013;12(1):22–29.

9. Mannucci E, Genovese S, Monami M, Navalesi G, Dotta F, Anichini R, et al. Photodynamic topical antimicrobial therapy for infected foot ulcers in patients with diabetes: a randomized, double-blind, placebo-controlled study—the DANTE (Diabetic ulcer Antimicrobial New Topical treatment Evaluation) study. Acta Diabetol. 2014;51(3):435–440.

10. Pham H, Exelbert L, Segal-Owens A, Veves A. A prospective, randomized, controlled double-blind study of a moisturizer for xerosis of the feet in patients with diabetes. Ostomy Wound Manage. 2002;48(5):30–36.

11. Huie CW. A review of modern sample-preparation techniques for the extraction and analysis of medicinal plants. Anal Bioanal Chem. 2002;373(1-2):23–30.

12. Barzana E, Rubio D, Santamaria RI, Garcia-Correa O, Garcia F, Ridaura Sanz VE, et al. Enzyme-mediated solvent extraction of carotenoids from marigold flower (Tagetes erecta). J Agric Food Chem. 2002;50(16):4491–4496.

13. Jiménez-Medina E, Garcia-Lora A, Paco L, Algarra I, Collado A, Garrido F. A new extract of the plant Calendula officinalis produces a dual in vitro effect: cytotoxic anti-tumor activity and lymphocyte activation. BMC Cancer. 2006;6:119.

14. Puri M, Sharma D, Barrow CJ. Enzyme-assisted extraction of bioactives from plants. Trends Biotechnol. 2012;30(1):37–44.

15. Baumann D, Adler S, Griiner S, Otto F, Weinreich B, Hamburger M. Supercritical carbon dioxide extraction of marigold at high pressures: comparison of analytical and pilot-scale extraction. Phytochem Anal. 2004;15(4):226–230.

16. Mohajeri G, Safaee M, Sanei MH. Effects of topical Kiwifruit on healing of neuropathic diabetic foot ulcer. J Res Med Sci. 2014;19(6):520–524.

17. Jacobs A, Tomczak R. Evaluation of Bensal HP for the treatment of diabetic foot ulcers. Adv Skin Wound Care. 2008;21(10):461–465.

18. Arora D, Rani A, Sharma A. A review on phytochemistry and ethnopharmacological aspects of genus Calendula. Pharmacogn Rev. 2013;7(14):179–187.

19. Hamburger M, Adler S, Baumann D, Förg A, Weinreich B. Preparative purification of the major anti-inflammatory triterpenoid esters from Marigold (Calendula officinalis). Fitoterapia. 2003;74(4):328–338.

20. Neukirch H, D’Ambrosio M, Dalla Via J, Guerriero A. Simultaneous quantitative determination of eight triterpenoid monoesters from flowers of 10 varieties of Calendula officinalis L. and characterisation of a new triterpenoid monoester. Phytochem Anal. 2004;15(1):30–35.

21. Zitterl-Eglseer K, Sosa S, Jurenitsch J, Schubert-Zsilavecz M, Della Loggia R, Tubaro A, et al. Anti-oedematous activities of the main triterpendiol esters of marigold (Calendula officinalis L.). J Ethnopharmacol. 1997;57(2):139–144.

22. Della Loggia R, Tubaro A, Sosa S, Becker H, Saar S, Isaac O. The role of triterpenoids in the topical anti-inflammatory activity of Calendula officinalis flowers. Planta Med. 1994;60(6):516–520.

23. Backonja M, Krause S. Neuropathic Pain Questionnaire—Short Form. Clin J Pain. 2003;19(5):315–316. 

24. Caetano KS, Frade MAC, Minatel DG, Santana LA, Enwemeka CS. Phototherapy improves healing of chronic venous ulcers. Photomed Laser Surg. 2009;27(1):111–118. 

25. Wagner FW. The dysvascular foot: a system for diagnosis and treatment. Foot Ankle 1981;2(2):64–122.

26. Levine NS, Lindberg RB, Mason AD Jr, Pruitt BA Jr. The quantitative swab culture and smear: a quick, simple method for determining the number of viable aerobic bacteria on open wounds. J Trauma.1976;16(2):89–94. 

27. Hawker GA, Mian S, Kendzerska T, Franch M. Measures of adult pain. Arthritis Care Res. 2011;63(11 suppl):s240–s252.

28. Robson MC, Hill D, Woodske ME, Steed DL. Wound healing trajectories as predictors of effectiveness of therapeutic agents. Arch Surg. 2000;135(7):773–777.

29. Richmond NA, Vivas AC, Kirsner RS. Topical and biologic therapies for diabetic foot ulcers. Med Clin North Am. 2013;97(5):883–898.

30. Reyzelman A, Crews RT, Moore JC, Mukker JS, Offutt S, Tallis A, et al. Clinical effectiveness of an acellular dermal regenerative tissue matrix compared to standard wound management in healing diabetic foot ulcers: a prospective, randomised, multicentre study. Int Wound J. 2009;6(3):196–208. 

31. Marston W, Hanft J, Norwood P, Pollak R. The efficacy and safety of dermagraft in improving the healing of chronic diabetic foot ulcers. Diabetes Care. 2003;26(6):1701–1705.

32. Wieman TJ, Smiell J, Yachin S. Efficacy and safely of a topical gel formulation of recombinant human platelet-derived growth factor-BB (becaplermin) in patients with chronic neuropathic diabetic ulcers. Diabetes Care. 1998;21(5):822–827.

33. Driver VR, Hanft J, Fylling CP, Beriou JM. A prospective, randomized, controlled trial of autologous platelet-rich plasma gel for the treatment of diabetic foot ulcers. Ostomy Wound Manage. 2006;52(6):68–87.

34. Margolis DJ, Kantor J, Santanna J, Strom BL, Berlin JA. Effectiveness of platelet releasate for the treatment of diabetic neuropathic foot ulcers. Diabetes Care. 2001;24(3):483–488.

35. Caravaggi C, De Giglio R, Pritelli C, Sommaria M, Dalla Noce S, Faglia E, et al. HYAFF 11-based autologous dermal and epidermal grafts in the treatment of noninfected diabetic plantar and dorsal. Diabetes Care. 2003;26(10):2853–2859.

36. Uccioli L, Giurato L, Ruotolo V, Ciavarella A, Grimaldi MS, Piaggesi A, et al. Two-step autologous grafting using HYAFF scaffolds in treating difficult diabetic foot ulcers: results of a multicenter, randomized controlled clinical trial with long-term follow-up. Int J Low Extrem Wounds. 2011;10(2):80–85.

37. Veves A, Sheehan P, Pham HT. A randomized, controlled trial of Promogran (a collagen/oxidized regenerated cellulose dressing) vs standard treatment in the management of diabetic foot ulcers. Arch Surg. 2002;137(7):822–827. 

38. Akihisa T, Yasukawa K, Oinuma H, Kasahara Y, Yamanouchi S, Takido M, et al. Triterpene alcohols from the flowers of compositae and their anti-inflammatory effects. Phytochemistry. 1996;43(6):1255–1260.

39. Matysik G, Wójciak-Kosior M, Paduch R. The influence of Calendulae officinalis flos extracts on cell cultures, and the chromatographic analysis of extracts. J Pharm Biomed Anal. 2005;38(2):285–292.

40. Yoshikawa M, Murakami T, Kishi A, Kageura T, Matsuda H. Medicinal flowers. III. Marigold. (1): hypoglycemic, gastric emptying inhibitory, and gastroprotective principles and new oleanane-type triterpene oligoglycosides, calendasaponins A, B, C, and D, from Egyptian Calendula officinalis. Chem Pharm Bull (Tokyo). 2001;49(7):863–870. 

41. Zitterl-Eglseer K, Reznicek G, Jurenitsch J, Novak J, Zitterl W, Franz C. Morphogenetic variability of faradiol monoesters in marigold Calendula officinalis L. Phytochem Anal. 2001;12(3):199–201.

42. Blakytny R, Jude E. The molecular biology of chronic wounds and delayed healing in diabetes. Diabet Med. 2006;23(6):594–608.

43. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(6):1615–1625. 

44. Patrick KF, Kumar S, Edwardson PA, Hutchinson JJ. Induction of vascularisation by an aqueous extract of the flowers of Calendula officinalis L. the European marigold. Phytomedicine. 1996;3(1):11–18. 

45. Parente LML, Andrade MA, Brito LAB, Dignani de Moura VMB, Miguel MP, de Souza Lino Jr. R, et al. Angiogenic activity of Calendula officinalis flowers L. in rats [Atividade angiogênica das flores da Calendula officinalis L. em ratos]. Acta Cirúrgica Brasileira. 2011;26(1):19–25.

46. Armstrong DG, Jude EB. The role of matrix metalloproteinases in wound healing. J Am Podiatr Med Assoc. 2002;92(1):12–18.

47. Fonseca YM, Catini CD, Vicentini FTMC, Nomizo A, Gerlach RF, Fonseca MJV. Protective effect of Calendula officinalis extract against UVB-induced oxidative stress in skin: evaluation of reduced glutathione levels and matrix metalloproteinase secretion. J Ethnopharmacol. 2010;127(3):596–601.

48. Fronza M, Heinzmann B, Hamburger M, Laufer S, Merfort I. Determination of the wound healing effect of Calendula extracts using the scratch assay with 3T3 fibroblasts. J Ethnopharmacol. 2009;126(3):463–467. 

49. Efstratiou E, Hussain AI, Nigam PS, Moore JE, Ayub MA, Rao JR. Antimicrobial activity of Calendula officinalis petal extracts against fungi, as well as Gram-negative and Gram-positive clinical pathogens. Complement Ther Clin Pract. 2012;18(3):173–176. 

50. Babaee N, Moslemi D, Khalilpour M, Vejdani F, Moghadamnia Y, Bijani A, et al. Antioxidant capacity of Calendula officinalis flowers extract and prevention of radiation induced oropharyngeal mucositis in patients with head and neck cancers: a randomized controlled clinical study. Daru. 2013;21(1):18. 

51. Duran V, Matic M, Jovanovć M, Mimica N, Gajinov Z, Poljacki M, Boza P. Results of the clinical examination of an ointment with marigold (Calendula officinalis) extract in the treatment of venous leg ulcers. Int J Tissue React. 2005;27(3):101–106.

52. Lavagna SM, Secci D, Chimenti P, Bonsignore L, Ottaviani A, Bizzarri B. Efficacy of Hypericum and Calendula oils in the epithelial reconstruction of surgical wounds in childbirth with caesarean section. Farmaco. 2001;56(5-7):451–453.

Abstract

Salmonella can cause extra-intestinal focal infections as well as gastrointestinal problems. A few cases of Salmonella skin and soft tissue infection have been documented in immunocompromised patients such as persons with type 2 diabetes and poor glycemic control.

A case study is presented of a 30-year-old man with a 10-year history of poorly controlled (HbA1C 11.7%) diabetes mellitus who presented with a ruptured nodule resulting in a wound with signs of infection over his anterior chest region of 1-month duration. He had been taking amoxycillin/clavulanate for the week previous to presentation at the authors’ facility. Following sharp debridement, the ulcerative wound deteriorated and a chest wall abscess developed. Bacterial culture results were positive for Salmonella group D, resistant to ampicillin and susceptible to ceftriaxone and ciprofloxacin. The patient underwent surgical debridement, resulting in a wound 7 cm x 4 cm, and was provided ceftriaxone 2.0 g intravenously daily along with insulin therapy. After surgical debridement, a local rotational flap was created for wound closure and reconstruction. The patient was discharged 1 week later on oral antibiotic therapy for 1 week. His wound was completely healed without recurrence at his 4-month follow-up. For this patient, addressing glycemic issues, identifying the infectious organism, and providing appropriate therapy, radical debridement, and flap surgery helped heal an advanced soft tissue infection. In immunocompromised patients with skin or soft tissue infections, the presence of Salmonella should be considered. 

Abstract

Foot complications in persons with diabetes mellitus (DM) are associated with substantial costs and loss of quality of life. Increasing evidence suggests changes in skin temperature, measured using an infrared thermographic system (IRT), may be a predictor of foot ulcer development in patients with DM. The purpose of this case study is to describe the long-term IRT findings and overall clinical outcomes of a patient with DM and peripheral vascular disease.

Foot temperature measurements using IRT were obtained slightly more than 1 year before and immediately following endovascular treatment of a 76-year-old man, a nonsmoker with type 2 DM, hypertension, and ischemic heart disease with cardiac arrhythmia. Although he was otherwise asymptomatic, the infrared measurement showed an average temperature difference of 2.3˚ C between the left and right foot until he developed a small, trauma-induced wound on the left foot, at which time left foot temperature increased. He was diagnosed with rectosigmoid adenocarcinoma, underwent surgery and chemotherapy, and subsequently was evaluated for peripheral vascular disease. Before undergoing peripheral angiography and percutaneous transluminal angioplasty, IRT evaluation showed a hot spot on the left heel. Immediately following endovascular treatment, the mean temperature difference between the right and left foot was low (0.2˚ C), but a Stage I pressure ulcer was visible on the left heel. Skin breakdown in that area was observed 2 months later, and the wound continued to increase in size and depth. The patient died shortly thereafter due to complications of cancer. In this case study, a series of infrared images of foot skin temperatures appeared to show a relationship with blood circulation and wound/ulcer development and presentation. IRT has the ability to instantaneously measure the absolute temperature of the skin surface over a large area without direct skin contact. However, the devices are very sensitive and prospective clinical studies to determine the validity, reliability, sensitivity, and specificity of these measurements for routine use in patients who are at risk for vascular disease and/or foot ulcers are needed.  

Early diagnosis of disease complications associated with diabetes mellitus (DM) is the first prerequisite for saving the lower limb. According to an analysis by Al-Maskari and El-Sadig,¹ which was part of a general cross-sectional survey conducted to assess the prevalence of DM, great attention must be paid to risk factors such as a diabetic neuropathy and diabetic angiopathy. Predictors of ulceration include the presence of peripheral neuropathy, peripheral vascular disease, and a history of ulceration.² In a cross-sectional study, Pound et al³ showed ulcers often recur after a median duration of 126 days in 40% of patients with a history of ulceration. Other risk factors for diabetic foot ulcers are foot infection, foot deformity, high plantar pressures during walking, male gender, and HbA1c >9%.^4-6 These factors are considered to be the leading causes of diabetic foot syndrome. 

Accurate diagnosis is the foundation of ulcer care. Patients with DM should be tested for neuropathy; in addition, proper vascular assessment is critical to the evaluation of the diabetic foot.⁷ A simple test to diagnose patients at risk for ulcer formation due to peripheral sensory neuropathy is the nylon monofilament test; an inability to detect the monofilament when applied under the metatarsal heads or digits is indicative of neuropathy.⁸ During vascular examination, the dorsalis pedis and posterior tibial pulses should be palpated, and a general inspection of the extremities should be performed. Noninvasive vascular tests include the ankle-brachial index, which is determined by dividing the higher systolic pressure of the anterior tibial or posterior tibial vessels by the highest systolic brachial pressure.^9-11 

Skin temperature is one of the most reliable indicators of body and foot blood perfusion. The systematic analysis of the literature by Houghton et al¹² suggests the use of skin temperature monitoring is an effective way to predict, and possibly prevent, diabetic foot ulceration. In their systematic review, Bharara et al¹³ compared various thermal measurement techniques in the assessment of the diabetic neuropathic foot and showed thermal measurement is a useful technique in the clinical management of the diabetic foot. In a descriptive review, Ring¹⁴ focused on the medical use of an infrared thermographic system (IRT) and its general relevance to DM as a useful tool in the assessment of tissue viability and peripheral circulation. Ring concluded IRT is especially suitable for serial measurements used in the follow-up of response to treatment. In a preliminary study, Brånemark et al¹⁵ used IRT to study 16 persons with DM with or without vascular complications, together with the action of a vasodilator. The authors showed characteristic abnormalities exhibited by the patients in the thermal patterns over the hands and feet that deviated from those of healthy subjects.

Recently, IRT has been widely used in DM-related diagnostics. In an observational study of 60 patients, Sivanandam et al¹⁶ applied IRT to measure skin temperature from the various body regions (ie, the contralateral regions of the inner canthus of the eye; tympanic region of the ear; and the forehead, neck, and upper and lower extremities) and noted the device can be used as a mass screening tool for the accurate estimation of HbA1c by which a sensitivity of 90% and negative predictive value of 85% could be achieved. Clinical studies regarding the role of IRT in the diagnostics of diabetic foot include Liu et al’s case study,¹⁷ which indicated dermal thermography can be a screening modality to detect presigns of ulceration in a timely manner. The pilot study by Van Netten et al¹⁸ examined 15 patients with DM and diffuse complications using IRT and demonstrated differences in mean temperature of >3˚ C between the ipsilateral and contralateral foot.

The clinical studies of Lavery et al^19,20 have shown thermometry is a useful monitoring tool for preventing diabetic foot ulcers and amputations. In a physician-blinded, 18-month randomized controlled trial study, Armstrong et al²¹ monitored 225 persons with DM and found in patients who developed an ulcer, foot skin temperature was 4.8 times higher at the site of ulceration in the week before ulceration than the temperature of patients who did not develop an ulcer. In their physician-blinded, randomized, 15-month, multicenter trial, Lavery et al²⁰ quantified data from 173 patients with a history of diabetic foot ulceration. An infrared skin thermometer was used by the enhanced therapy group of patients to measure temperatures on 6 foot sites each day. Temperature differences (>2.2˚ C) observed between left and right corresponding sites triggered patients to reduce activity until temperatures normalized. The enhanced therapy group had fewer foot ulcers than the standard therapy group without temperature monitoring.

According to the studies mentioned, thermal symmetry is normal in healthy study groups; temperature gradients between feet may predict the formation of ischemic changes. 

IRT, unlike many other imaging techniques used in medicine, is not an internal imaging system for anatomical information; infrared imaging provides information on skin temperature distribution. The great advantage of IRT is that it is both noncontact and noninvasive and a real-time temperature measurement. Any object at a temperature above absolute zero (ie, T >0 K) emits infrared radiation. By remote temperature sensing, the camera is merely receiving the natural thermal energy emitted by the body and transforming it into an electronic signal.²² In their critical review, Lahiri et al²³ focused on the basics of medical IRT, the procedures adopted for various measurements, and successful applications of IRT diagnosis in various medical fields. However, IRT can provide only an image of skin temperature distribution; it does not provide data at a specific depth inside the body. 

The purpose of this case study is to describe the long-term IRT findings and overall clinical outcomes of a patient with DM and peripheral vascular disease. The patient was chosen due to his willingness to cooperate with the study duration. 

Case Report

Mr. D, a 76-year-old nonsmoker with DM type 2, hypertension, and ischemic heart disease with cardiac arrhythmia, was monitored several times at home over a period of 1 year (from March 2012 until February 2013) using IRT before he was examined in the outpatient vascular surgery department. Intervals of monitoring were based on the patient’s availability. He received no treatment on his lower limbs before the February 2013 examination. Mr. D had no visible defects on the foot; his only complaint was that his feet felt cold. During home visits, the soles and the forefoot were scanned by IRT. Thermograms were recorded with an FLIR B200 infrared camera (Flir Systems, Danderyd, Sweden). The thermal images obtained were processed using QuickReport 1.2 software (Flir Systems, Danderyd, Sweden). All images were standardized to the same temperature range (20˚ C – 35˚ C). Temperature measurement points were selected along a line connecting the first toe and the heel or from the square area as is shown in Figure 1. The mean temperatures along the line and from the area of interest were calculated by the software. The same value of emissivity (ie, the measure of an object’s ability to emit infrared energy, ε = 0.98) was used for all thermograms. Standard conditions in IRT imaging have been documented by Vollmer and Möllman²⁴ and Ring and Ammer²⁵; according to these conditions, the thermal images were captured at a distance of 1 m from the body region in a restricted, temperature-controlled environment. The thermal equilibration of the patient was 15 minutes. 

IRT home monitoring. The infrared images (see Figure 2) show a temperature map of the feet. The first and second IRT assessments were obtained in March and May 2012 (see Figure 2a,b). The highest mean temperature difference between the left and right foot was 2.3˚ C (see Table 1), but no difference was noted during the next assessment in October (see Figure 2c). At that time, a small wound was noted on the nail of the first left toe after the patient injured himself in September 2012. Figures 2a–f show a colder upper part of the left foot. Lower limb ischemic, vascular, or wound complications were not present during this period of time. The highest temperature difference between the right and left foot toes was 4.6˚ C (see Figure 2e and Table 2). In February 2013, the temperature of the left foot increased (see Figure 2f); specifically, the mean temperature in the square area on the heel was 25.3˚ C for the right foot and 29.2˚ C for the left foot.

Clinical examination, treatment, and follow-up. Mr. D was first examined in the outpatient department in February 2013 for an ischemic defect on the first left toe with a diameter of ~1-cm necrotic base and phlegmon around the defect. According to Mr. D, the defect had appeared 4 months earlier (October 2012) when he injured himself and gradually worsened. In December 2012, Mr. D underwent a rectosigmoid resection for adenocarcinoma (T3N1bM1, diagnosed in December 2012) with metastatic liver disease. Overall, he was in good condition, without claudication; he received chemotherapy treatment (5-fluorouracil and leucovorin; FU/FA de Gramont) (see Table 3).

Left leg pulses were palpable in the groin on the superficial femoral artery (SFA) and on the popliteal artery (PA). Peripheral arteries were not palpable. An audible pulse was detected in the posterior tibial artery (PTA) by ultrasonic Doppler probe. The right leg dorsalis pedal artery (DPA) was palpable. CT angiographic examination warranted the need for peripheral angiography of the left limb and a percutaneous transluminal angioplasty was performed in April 2013. Specifically, CT angiography showed evidence of patent SFA with PA and significant atherosclerotic disease of the tibial arteries (eg, stenotic anterior tibial artery with closure of the middle part) to the farther PTA with distal closure. The middle of the peroneal artery was stenotic with distal closure (see Figure 3). The plantaris communis artery (PCA) and DAP were not noted in CT angiographic images — that is, the distal parts of the lower leg and foot were perfused only by minor collateral vessels, mostly dilated muscular branches forming a collateral pathway around both ankles (see Figure 4). A percutaneous transluminal angioplasty of the anterior tibial artery (ATA) and peroneal artery was performed (see Figure 5). The control angiography showed good results after endovascular treatment at the site of dilatation, with slightly better collateral supplied peripherals — the dilated branches from revascularized parts of tibial arteries supplying peripheral parts of tibial and foot vascular system showed a hint of efflux in the common plantar artery (see Figure 6). A palpable pulse was clinically detected on the SFA/PA at the time of hospital discharge. Audible flows in the PTA and the peroneal artery were detected by ultrasound Doppler probe; lower limb mobility and sensitivity were not compromised.

One (1) month after the endovascular surgery, an extensive pseudo-aneurysm in the tibial area overlying the left ATA was detected by ultrasound duplex. This observation was confirmed by control CT angiographic examination (see Figure 7). An asymptomatic pseudo-aneurysm in this area is not a medical emergency requiring immediate surgery and due to the serious overall condition of the patient (cancer with metastases), conservative therapy was continued. 

Infrared images were taken before (see Figure 8a) and 1 day after revascularization (see Figure 8b). The mean temperatures of the right and left foot were 32.3˚ C and 32.1˚ C, respectively, before and 33.6˚ C and 33.2˚ C 1 day after the procedure (see Figure 8b). Thirteen (13) days following angioplasty, an area of warmth on the left foot heel was apparent (see Figure 8c). The highest temperature was 33.6˚ C on the left heel and 32.3˚ C on the right heel. The left heel hot point area affected the mean temperature, which was up to 0.6˚ C higher in the treated limb (see Table 4). At the time of discharge following endovascular treatment, the wound on the left foot toe was dry with a diameter of ~1 cm with no signs of active infection, and the wound base showed granulation tissue without any signs of wound widening. A discoloration of the skin was visible on the left foot heel, and intermittent pain occurred at rest. Local treatment of the wound on the left toe continued twice a week in the outpatient department. The condition of the wound gradually improved, its size decreased, and by May 2013 it was reduced to its original size. The wound was dry with no signs of suppuration or inflammation (aggressive infection, phlegmon). Although the toe wound was healing well, by the end of May/beginning of June 2013 a nonblanchable erythema pressure ulcer (Stage I) had developed on the left heel. Clinically palpable pulsation in the limbs remained unchanged after the initial treatment. 

Mr. D’s overall condition gradually deteriorated while he was being monitored due to the cancer. The condition of his limbs also worsened in July. The defect on the toe was small with no signs of active infection, granulation tissue was noted in the wound base, and there were no signs of increasing wound size, but the heel pressure ulcer became necrotic and was 6 cm in diameter. The ulcer on the heel was treated using moist wound therapy twice a week. During the treatment, necrotic tissue was removed. By September 2013, the lesion progressed to Stage II; it was 2 cm deep with no signs of infection or inflammation around the ulcer. 

Mr. D’s overall condition worsened in September and October 2013. He developed ascites and died at the end of October due to cancer-related complications (see Table 3). 

Discussion

This is the first case study describing clinical outcomes and IRT scanning results over an extended period of time and provides observations that suggest a relationship among vascular supply, skin temperature changes, and the development of wounds. Before developing any symptoms, a mean temperature difference of 1.8˚ C between the left and right foot was detected at the first (March 2012) and second (May 2012) IRT assessments (see Figure 2a,b). According to the pilot study of van Netten et al¹⁸ and the randomized multicenter study of Lavery et al,²⁰ a difference in temperature contralaterally of the feet of patients with diabetes often was observed. No temperature difference was observed for Mr. D in October 2012 (see Figure 2c). At that time, Mr. D had a small wound on the nail of the first left toe after he injured himself. A mean temperature difference between feet showed a gradual increase of 2.1˚C (see Figure 2e). During the last IRT measurement, the hot point area of heel on the left foot was observed with a mean temperature difference 4.7˚ C between the left and right heels (see Figure 2f). This increase in temperature could have been the first indicator of heel pressure; a heel pressure ulcer was diagnosed 2 months later (May 2013). Evidence from Gatt’s²⁶ single-center, randomized, prospective study among 63 healthy adults suggests the normal temperature difference between plantar feet is no greater than 0.84˚ C. 

IRT may be a useful tool for monitoring skin temperature changes influenced by blood circulation. This point was observed before and after Mr. D’s endovascular treatment. Foot skin temperature was affected by revascularization. Despite the 15-minute acclimatization period of thermal equilibration of the foot, an increased temperature in both limbs was detected. This increase could have been affected by the fact the image was taken early in the morning, immediately after Mr. D awakened when more time for acclimatization might be necessary. The warmer bearing on the left heel was where the pressure ulcer formed.

Limitations of Thermography

IRT is a very sensitive device for measuring variations in heat patterns; however, thermograms can be influenced by many ambient factors, as proposed in the review by Fernández-Cuevas et al.²⁷ Thus, thermography images should be obtained under controlled environmental conditions, per the observational study of Zaproudina et al.²⁸ The recommended option is to report data from scanned images as a difference between affected and healthy contralateral anatomical structures to define the consistency of abnormality. 

Another important consideration of IRT measurement is the preparation of patients. Fifteen (15) minutes of acclimatization are needed for thermal equilibration of the patient, and the skin surface has to be dry and free of any artifacts (ie, topical ointments, solutions, bandages or dressings). Ignoring these factors has a negative impact on the evaluation of resulting infrared images, because these artifacts can affect the characteristics of the skin (ie, emissivity and reflexivity).^29,30 Based on authors experience and Gatt et al’s study,²⁶ a nonreflective plate can be placed behind the area of interest, which leads to better evaluation of the infrared images due to the patient´s temperature filtration in the background.

Conclusion

In this case study, infrared images of foot skin temperatures appeared to show a relationship between blood circulation and wound/ulcer presentation. IRT has the ability to instantaneously measure the absolute temperature of the skin surface over a large area without direct skin contact. In this and other studies, IRT has been found to reveal physiological changes before they are clinically apparent. The infrared images can be used to monitor temperature differences between the lower limbs of patients over a long time period and have the potential to be used as an indicator of vascular disease or predictor of foot ulcer formation. However, IRT devices are very sensitive, and prospective clinical studies to determine the validity, reliability, sensitivity, and specificity of these measurements for routine use in specific populations are needed. 

References

1. Al-Maskari F, El-Sadig M. Prevalence of risk factors for diabetic foot complications. BMC Family Pract. 2007;8(1):59.

2. Pecoraro RE, Reiber GE, Burgess EM. Pathways to diabetic limb amputation. Basis for prevention. Diabetes Care. 1990;13(5):513–521.

3. Pound N, Chipchase S, Treece K, Game F, Jeffcoate W. Ulcer-free survival following management of foot ulcers in diabetes. Diabetes Med. 2005;22(10):1306–1309.

4. Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJ. Predictive value of foot pressure assessment as part of a population based diabetes disease management program. Diabetes Care. 2003;26(4):1069–1073.

5. Veves A, Murray HJ, Young MJ, Boulton AJ. The risk of foot ulceration in diabetic patients with high foot pressure: a prospective study. Diabetologia. 1992;35(7):660–663.

6. Lavery LA, Armstrong DG, Vela SA, Quebedeaux TL, Fleischli JG. Practical criteria for screening patients at high risk for diabetic foot ulceration. Arch Internal Med. 1998;158(2):157–162.

7. Wu SC, Driver VR, Wrobel JS, Armstrong DG. Foot ulcers in the diabetic patient, prevention and treatment. Vasc Health Risk Manage. 2007;3(1):65–76.

8. Armstrong DG, Lavery LA. Diabetic foot ulcers: prevention, diagnosis and classification. Am Family Phys. 1998;57(6):1325–1358.

9. Hiatt WR, Goldstone J, Smith SC, et al; American Heart Association Writing Group !. Atherosclerotic Peripheral Vascular Disease Symposium II Nomenclature for Vascular Diseases. Circulation. 2008;118(25):2826–2829.

10. Orchard TJ, Strandness DE Jr. Assessment of peripheral vascular disease in diabetes. Report and recommendation of an international workshop sponsored by the American Heart Association and the American Diabetes Association. Diabetes Care. 1993;16(8):1199–1209.

11. Kunimoto B, Cooling M, Gulliver W, Houghton P, Orsted H, Sibbald RG. Best practices for the prevention and treatment of venous leg ulcers. Ostomy Wound Manage. 2001;47(2):34–51.

12. Houghton VJ, Bower VM, Chant DC. Is an increase in skin temperature predictive of neuropathic foot ulceration in people with diabetes? A systematic review and meta-analysis. J Foot Ankle Res. 2013;6(1):31.

13. Bharara M, Cobb JE, Claremont DJ. Thermography and thermometry in the assessment of diabetic neuropathic foot: a case for furthering the role of thermal techniques. Int J Lower Extremity Wounds. 2006;5(4):250–260.

14. Ring F. Thermal imaging today and its relevance to diabetes. J Diabetes Sci Technol. 2010;4(4):857–862. 

15. Brånemark PI, Fagerberg SE, Langer L, Säve-Söderbergh J. Infrared thermography in diabetes mellitus. A preliminary study. Diabetologia. 1967;3(6):529–532.

16. Sivanandam S, Anburajan M, Venkatraman B, Menaka M, Sharath D. Estimation of blood glucose by non-invasive infrared thermography for diagnosis of type 2 diabetes: an alternative for blood sample extraction. Molecular  Cellular Endocrinol. 2013;367(12):57–63.

17. Liu C, Heijden F, Klein ME, van Baal JG, Bus SA, van Netten JJ. Infrared dermal thermography on diabetic feet soles to predict ulcerations: a case study. Presented at: the Conference of Advanced Biomedical and Clinical Diagnostic Systems XI. San Francisco, CA. January 2–7, 2013.

18. van Netten JJ, van Baal JG, Liu C, van der Heijden F, Bus SA. Infrared thermal imaging for automated detection of diabetic foot complications. J Diabetes Sci Technol. 2013;(7):1122–1129.

19. Lavery LA, Higgins KR, Lanctot DR, et al. Home monitoring of foot skin temperatures to prevent ulceration. Diabetes Care. 2004;27(11):2642–2647.

20. Lavery LA, Higgins KR, Lanctot DR, et al. Preventing diabetic foot ulcer recurrence in high-risk patients: use of temperature monitoring as a self-assessment tool. Diabetes Care. 2007;30(1):14–20.

21. Armstrong DG, Holtz-Neiderer K, Wendel C, Mohler MJ, Kimbriel HR, Lavery LA. Skin temperature monitoring reduces the risk for diabetic foot ulceration in high-risk patients. Am J Med. 2007;120(12):1042–1046.

22. Modest MF. Fundamentals of thermal radiation. In: Waltham MA (ed). Radiative Heat Transfer. Amsterdam, The Netherlands: Academic Press;2013.

23. Lahiri BB, Bagavathiappan S, Jayakumar T, Philip J. Medical applications of infrared thermography: a review. Infrared Phys Technol. 2012;55(4):221–235.

24. Vollmer M, Möllmann KP. Selected applications in other fields. In: Vollmer M, Möllmann KP. Infrared Thermal Imaging: Fundamentals, Research and Applications. Weinheim, Germany: John Wiley & Sons;2010.

25. Ring EFJ, Ammer K. The technique of infrared imaging in medicine. In: Ring EFJ, Ammer K. Infrared Imaging. A Casebook in Clinical Medicine. London, UK: IOP Publishing;2015.

26. Gatt A, Formosa C, Cassar K, et al. Thermographic patterns of the upper and lower limbs: baseline data. Int J Vasc Med. 2015; doi: 1155/2015/831369. 

27. Fernández-Cuevas I, Marins JCB, Lastras JA, et al. Classification of factors influencing the use of infrared thermography in humans: a review. Infrared Physics Technol. 2015;71(7):28–55.

28. Zaproudina N, Varmavuo V, Airaksinen O, Narhi M. Reproducibility of infrared thermography measurements in healthy individuals. Physiol Measure. 2008;29(4):515–524.

29. Bagavathiappan S, Saravanan T, Philip J, et al. Investigation of peripheral vascular disorders using thermal imaging. Br J Diabetes Vasc Dis. 2008;8(2):102–104.

30. Bernard V, Staffa E, Mornstein V, Bourek A. Infrared camera assessment of skin surface temperature — effect of emissivity. Physica Medica-European J Med Physics. 2013;29(6):583–591.

Potential Conflicts of Interest: This research was supported by a specific grant from Masaryk University, Brno, Czech Republic (MUNI/A/1449/2014 and MUNI/A/0894/2015). 

Mr. Erik Staffa is a researcher and specialist, and Dr. Bernard is assistant professor and researcher, Department of Biophysics, Faculty of Medicine, Masaryk University; Dr. Kubíček is an assistant and vascular surgeon, and Dr. Vlachovský is an assistant professor and vascular surgeon, 2nd Department of Surgery, St. Anne’s University Hospital, Faculty of Medicine; Dr. Vlk is assistant professor and researcher, and Dr. Mornstein is a professor and head of the department, Department of Biophysics, Faculty of Medicine; and Dr. Robert Staffa is a professor and head of the department, 2nd Department of Surgery, St. Anne’s University Hospital, Faculty of Medicine, Masaryk University, Brno, Czech Republic. Please address correspondence to: Erik Staffa, Department of Biophysics, Faculty of Medicine, Masaryk University, Kamenice 5, Brno, 62500 Czech Republic; email: staffa@mail.muni.cz.

Abstract

Because nurses frequently participate in decisions related to wound care, learning about wounds and their care during undergraduate education is critical. A cross-sectional, descriptive, quality improvement project was conducted in an introductory baccalaureate nursing course to identify: 1) the types of patients with wounds assigned to beginning students, 2) patient wound care procedures and dressings, and 3) student level of participation in wound care.

Data were collected from the weekly notes recorded about students’ (N = 49) patient care experiences in 3 acute care hospitals for 9 clinical days during 1 semester. Data were recorded on a paper-and-pencil form by instructors at the end of the clinical day and included type of wound, wound irrigation, dressing, technique of care, and student’s participation. Descriptive statistics were used to examine the frequency and distribution of the wound characteristics and care assessed. Of the 284 patients assigned to students, 75 (26.4%) had a wound. The most common wound was a surgical incision (49, 65%) and was closed (36, 73.5%). Twenty-six (26) patients had a pressure ulcer, most commonly Stage II. The most common dressing was dry gauze (29). Damp gauze was used on 18 wounds. Wound irrigation was recorded for 24 wound protocols and performed with a bulb syringe or by pouring the solution from a container. Generally, nonsterile wound care was performed. Twenty-five (25) students performed wound care with the instructor, 16 watched the care performed by another clinician, and 10 participated with another nurse in the wound care. For 22 patients, the wound care was neither observed nor performed because either it was not time for the dressing to be changed or it was only to be changed by a medical team. From these data, it was concluded beginning nursing students had some, but limited, clinical experience with patients with wounds. Students’ wound care experiences need further examination, especially across multiple educational courses. 

Abstract

Educational intervention programs are an important element to improve nurses’ knowledge of pressure ulcer (PU) prevention. Various teaching methods have been used with diverse results but none have been analyzed in Nigeria. A quasi-experimental study using a pretest/post test design was conducted among 193 registered nurses with >6 months experience who worked in purposefully selected wards (neuroscience, orthopedics, renal, and cardiac) in 3 teaching hospitals to examine the level of knowledge retention after interactive instruction.

Participants were randomized to intervention (IG, n = 127 from 2 hospitals) and control (CG, n = 66 from 1 hospital) groups; the IG was provided a 5-day, face-to-face interactive lecture, and the CG engaged in a 1-day, 4-hour discussion of PU prevention practices. The Pressure Ulcer Knowledge Tool, a 47-item questionnaire in which a correct answer = 1 point and an incorrect/“I don’t know” answer = 0 (maximum score 47), was used to assess and compare knowledge retention at 3 time points: baseline (T1), immediately after instruction (T2), and after 3 months (T3). Three trained research assistants assisted with registration of participants and distribution and collection of the questionnaires. All questionnaires were retrieved at T1 before the intervention began. Respondents were encouraged to respond to all questions. Data were analyzed using t-test and ANOVA (P = 0.05). At T1, knowledge scores were comparable between the IG and CG (32.5 ± 4.2 and 30.8  ± 5.0 for IG and CG, respectively). At T2, knowledge scores increased significantly only in the IG to 40.7 ± 3.4 (d = 1.94, P<0.05). The mean difference between T1 and T2 was  -8.2 ± 5.4, t = -17.0, P = 0.000. Similarly, mean scores increased significantly from T2 to T3 in the IG (mean= -2.0 ± 5.5, t = -4.1, P = 0.000); scores in the CG were -6.2 ± 7.2, t = -6.3 (P = 0.000). A face-to-face interactive lecture was shown to be an effective method of program delivery for nurses; other educational methods should be assessed and their effects on PU prevention practices and outcomes evaluated.  

Pressure ulcers (PUs) are a significant threat to the safety of patients and have a major negative impact on patients, their families, and the health care system.^1,2 Findings from a cross-sectional observational study¹ conducted among 2,000 patients in a tertiary care hospital in Australia confirm PUs were responsible for prolonged hospital stay and increased economic cost. According to a systematic review and meta-synthesis,³ PUs have a substantial impact on health-related quality of life among older patients. A prevalence study by Mclnerney⁴ showed the risk of mortality is 2 to 6 times greater in patients with PUs as opposed to persons without PUs.^3,4 The negative effects may be even greater in the poorer nations of the world, particularly among patients with spinal cord injury. According to Zakrasek et al’s review of the literature⁵ on risk factors and cost of PU in low- and middle-income countries, the prevalence of PUs is high and comes with increasing complications.  

Various strategies regarding education and training for nurses have been shown to be factors in PU prevention.^6-8 For example, Tweed and Tweed⁶ conducted an educational intervention study among critical care nurses (N = 62) and reported an increase in knowledge for PU prevention post intervention. Using a pretest/post test design, Cox et al⁷ compared the effectiveness of 2 methods of instruction on PU prevention among critical care and medical surgical nurses and found knowledge retention can be maintained by a quarterly educational program. These educational programs have produced good outcomes, such as reduced PU incidence,^6,9 effective risk assessment, successful  planning, and implementation of interventions.^10-12 

Despite these findings, evidence from the literature suggests nurses’ level of PU knowledge is not yet optimal.^13,14 For example, although a systematic review¹³ of the effectiveness of educational programs in promoting knowledge among nurses for PU prevention showed educational programs have positive effects on nurses’ knowledge of PU prevention, similar reports of descriptive studies^15,16 in Nigeria suggested inadequate knowledge of PU prevention among nurses in Nigeria. Such reports point to a need for repeated education and training as new information on PUs emerges for Nigerian nurses. 

Literature Review

The joint international organization for PUs¹⁷ asserts a number of contributing or confounding factors, yet to be fully elucidated, are associated with PU development, underscoring a need for consistent attention to issues regarding PUs. Patient quality care and safety organizations have focused on PU prevention issues. For example, the American Nurses Association Quality Forum¹⁸ recognized PUs as largely preventable, nursing-sensitive adverse events. The Joint Commission on Accreditation of Healthcare Organization¹⁹ included PU prevention as one of the National Patient Safety Goals. The strong position on PU prevention taken by these organizations commends programs that provide PU updates for nurses because nurses play significant roles in PU prevention. Quasi-experimental, pretest/post test and descriptive studies^20,21 confirm that inadequate knowledge and skills for PU prevention among nurses working in acute care facilities can significantly influence PU rates¹³ and patients’ clinical outcomes. This is evident in Nigeria, where hospital-based surveys^22-25 reported increased PU incidence rates are attributed partly to inadequate knowledge of evidence-based preventive interventions among care providers, particularly nurses. This conclusion was corroborated by other authors,^15,16 who reported knowledge about PU prevention among nurses was less than optimal. 

Continuing education is vital to consistent, safe, and effective care delivery and also a prerequisite for reconfirmation of practice licenses in most countries.^26,27 Specifically, continuing education comprises activities that increase the knowledge of workers toward improved performance.²⁸ Different strategies including face-to-face lectures are employed in continuing education programs. Traditional lectures are typically teacher-focused, one-way communication, which leaves the learners inactive and passive.^29,30 According to quasi-experimental studies involving nurses,^28,31,32 the duration of knowledge retention by learners participating in the lecture method is short, usually no longer than 8 weeks, even with the use of PowerPoint® delivery. Based on this limitation, educational experts³³ suggest integrating diverse or blended methods in any one teaching session for better outcomes.

Teaching theories. Adult, professional learners such as nurses would benefit from blended strategies, because these learners are self-directed and need to have control over their learning needs.³⁴ Nursing professionals need to incorporate learning into their busy schedules to effectively  understand and be current with increasing research evidence in health care, which also drives health care improvements. Some descriptive studies^35,36 involving medical students suggest when professionals are engaged in learning, they reflect on previous experiences to bring meaning to the new knowledge, enhancing the learning experience. To facilitate reflection and better understanding of new knowledge, particular delivery strategies should be incorporated into a professional continuing education program. According to Sandars’³⁷ review on the concept of reflection,³⁷ reflection is a metacognitive process that creates better understanding of both the self and the situation to inform future actions. As such, reflection is a major component of life-long learning and believed to improve professional competence. Experience is significant in professional learning, but it is not a stand-alone phenomenon. Drawing from Kolb’s³⁸ theory of experiential learning, experience must be integrated into an existing knowledge structure to become new and expanded knowledge. This process requires the skill of reflection for a higher level of personal learning, such as when an individual learns about the side effects of a drug by observing reactions (experience) from a patient on the drug or when the clinician becomes more adept at a clinical skill after an experience demonstrating ineffective application of the skill. 

Interactive lecture is a form of inquiry learning that allows active learner participation and reduces the monotony of passive learning that occurs with the traditional lecture.³⁹ Interactive lecture is implemented using methods such as brainstorming, small group discussion, role play, and simulations,⁴⁰ enhancing student engagement with their course materials. Interactive lectures also may take the form of questioning the audience or using engagement triggers to stimulate interest and arouse the learner’s attention and serve as ice breakers.⁴¹ In his review of the literature describing the indicators of interactive learning, Steinert and Snell⁴¹ noted active participation of learners is a prerequisite for learning beyond the recall of facts. On a broader perspective, Lee⁴² acknowledged interactive learning  encompasses every method except traditional lecture. The effectiveness of the interactive mode of learning has been well documented as a preferred method to the traditional lecture. However, to the best of the authors’ knowledge, its effectiveness in delivering PU prevention education in Nigeria has not been documented. 

The aim of this study was to examine the effectiveness of a face-to-face, interactive lecture approach to education on knowledge retention among nurses in selected teaching hospitals in southwest Nigeria.

Four (4) research questions were raised: 

1. What is the knowledge of PU prevention strategies of the intervention and control groups at baseline?

2. What is the effect of interactive lecture on post test knowledge score in intervention and control groups?

3. What is the difference in post test scores immediately (T2) and 3 months (T3) post intervention in the intervention group?

4. What is the effect of selected demographic characteristics (years of experience, professional cadre based on profession, previous exposure to PU lecture) on knowledge score in the 2 groups before and after educational intervention?

Methods and Procedures 

The study adopted a nonequivalent control group, pretest/post test design and was conducted in 3 selected teaching hospitals in 3 (Oyo, Osun, and Lagos) of the 6 states in the southwest geopolitical zone in Nigeria. The hospitals included the University College Hospital (UCH) and Lagos State University Teaching Hospital (LASUTH), Ibadan; and Obafemi Awolowo University Teaching Hospital Complex (OAUTHC), Ile Ife. The hospitals were under 2 main clusters based on proprietorship: state government-owned and federal government-owned, publicly funded institutions. All of  the hospitals are large tertiary institutions, with a minimum of 300 beds each. Ethical approval was sought and obtained from the Health Research and Ethics Boards of each institution. 

A purposive sampling of the hospital was conducted based on inclusion criterion of providing care for patients with complex health problems. Balloting was done to determine which hospitals served as intervention and control groups. The intervention group (IG) included nurses from LASUTH and UCH, and the control group (CG) included nurses from OAUTHC. To limit inadvertent influence of treatment condition on the CG, the IG was completely separate from the CG. 

Participating wards also were selected purposively to reflect patients with health problems that would likely place them at risk for PUs; as such, all nurses from the surgical (orthopedics), medical, and neurological wards (except nurses on vacation) were invited to participate. 

Testing instrument. The Pressure Ulcer Knowledge Test (PUKT)⁴³ was used to assess knowledge and information acquisition at the 3 testing time points. The tool is composed of 47 items that measure respondents’ knowledge of risk factors, preventive strategies, and PU staging. Correct Yes/No responses are scored 1 and incorrect responses of Yes, No, or I don’t know are scored 0. The maximum score is 47 (100%).  

The PUKT has been used in other countries^9,44 with reported good reliability levels. A pilot survey was conducted in a different state teaching hospital (Ogun state) among 111 nurses 6 months before the main study to examine the feasibility of the study and to test the reliability of the testing tool.¹⁶ Findings from the pilot study led to the revision and rewording of some items in the instrument for clarity and in relation to the care environment. For example, in the local hospital, nurses use water-filled gloves to elevate the heels. Therefore, the item in  the original document that reads Heel protectors relieve pressure on the heels  was reworded to read A heel protector such as water-filled glove effectively relieves pressure on the heels. In addition, the item that relates to the appointment of a governmental panel to study PU risk, prevention, and treatment were removed because it was not applicable to Nigeria. This was the first time the PUKT was validated in Nigeria. The reliability coefficient was found to be 0.82. 

General procedure. In each setting, with the support of the Director of Nursing services, the pretest (paper-and-pencil PUKT) was administered to all participants at the same time. This was to ensure the uniformity of nurses’ entry behavior and to establish their level of PU knowledge at baseline (T1) to accurately examine the effect of the program. Each participant signed a register to document attendance. The researcher recruited and trained 3 research assistants (RAs) to assist with participant registration and to monitor and retrieve completed questionnaires. 

Study group procedure. The nature, purpose, and procedure of the study were explained to nurses who provided written consent for participation. The IG participants  (UCH and LASUTH) were invited to attend the educational workshop organized in the respective hospitals. 

The program was structured to accommodate various nursing schedules because it was not possible to take all nurses off the wards at the same time to attend the 4-hour workshop. In UCH, the nurses were divided into 2 groups. Each group attended the workshop for 5 consecutive days. In LASUTH, all participants attended the same 5-day workshop facilitated by a labor conflict that decreased patient load.

Intervention fidelity was maintained because the module curriculum was followed strictly by the principal investigator, who also delivered all the sessions. 

The interactive educational program. Participants were provided the program of events for each day. They were encouraged to choose an identification number to facilitate analysis in matching each participant’s pretest with post test scores, to assess full participation, and to easily identify missing questionnaires. The intervention was an interactive lecture that involved small group discussions and brainstorming. Participants were grouped based on the wards where they work to facilitate continual cooperative work on the wards. During the first 15 minutes of each module, participants brainstormed on specific questions and answers and shared experiences and practical ideas on PU prevention. The remaining period was used for lectures and discussion on current trends regarding PU prevention and related clinical correlations. For example, the researcher projected pictures of different stages of PUs and participants were asked to determine the stages. This helped actively involve participants in the sessions. Lectures were projected using PowerPoint® slides. The principles of adult learning³⁴ guided the interaction with the participants (ie, learners connect learning with past experience). To facilitate this connection, the researcher also displayed different skin care products (eg, dimethicone-based barrier creams and sprays, dressings, foams, and corn starch) to stimulate discussions on nurses’ practices. At the end of the sessions, paper versions of the PowerPoint® slides were provided to participants. The level of each respondent’s participation was not documented or measured.

All modules were presented by the principal investigator in the 2 hospitals. Each session lasted for 4 hours per day. The curriculum consisted of 5 modules as shown in Table 1. 

Assessment. A pencil-and-paper PUKT was readministered on day 5 as an immediate post test (T2). The test was completed under supervision, and participants did not refer to the paper versions of the slides. Completed tests were retrieved on the spot. Participants were informed they would be invited to a third round of testing after 12 weeks (T3).  

Participants returned to their respective wards but maintained the groupings to facilitate cooperative problem-solving while providing care. Over the 12-week between-test period, the researcher reinforced what was covered in the module with hands-on demonstrations. At the end of 12 weeks, participants were contacted by telephone, Short Message Services, and email for the second post test. The same test (PUKT) was administered at all 3 time points. 

Control group procedure. The CG also was provided study details. The PUKT questionnaire was distributed to the participants to examine their baseline knowledge. The participants engaged in a general 1-day, 4-hour discussion on their usual practices for PU prevention. The session was facilitated by the RAs under the supervision of the principal investigator. This was followed by a second test (T2). Participants were contacted for the second post test at 3 months (T3). 

At the end of the third data collection (which marked the end of the study), the CG was provided the same package of educational materials as the IG on PU prevention for ethical reasons. 

Data analysis. Data from the PUKT instrument were collected and entered into a database, the Statistical Package for Social Sciences (SPSS) (Version 17.0, Chicago, IL), for analysis. Data were checked to ensure consistency and to determine where information was missing. A complete case-wise analysis was performed for missing data because the proportion of missing data categorized as Missing Completely at Random (MCAR) was <10% and  was observed only at the 3-month post test (T3). Descriptive statistics using absolute number and relative frequencies (percentages) to describe the sample characteristics were used. Means and standard deviations were computed to ascertain nurses’ PU knowledge scores. A paired sample t-test was used to compare the differences in knowledge between IG and CG pre- and post intervention. Cohen’s d was calculated to determine the strength of the intervention effect. The effect of selected demographic variables on participants’ knowledge scores was examined using ANOVA, and the effect size (eta squared) also was computed. The level of significance was set at α = 0.05% 

Results

Demographic characteristics. The sample consisted of 193 registered nurses, 127 in the IG and 66 in the CG. The level of education and areas of practice are described in Table 2. The majority of the respondents were basic diploma-certified registered nurses (RN) (133, 68%) and degreed nurses (BNSc) (26, 13.5%); a statistically significant difference was noted in both the IG (36.8 ± 10.3, P = 0.03) and CG (35.2 ± 11.9, P = 0.04). A similar trend was found with years of experience between IG and CG (14.5 ± 13.7, P = 0.04 and 12.6 ± 12.0, P = 0.03, respectively).

Baseline knowledge. The mean knowledge score at baseline was comparable in both IG (32.5, SD = 4.2) and CG (30.8, SD = 5.0), as shown in Table 3. 

Knowledge retention. The score at T2 significantly increased only in the IG from 32.5 ± 4.2 to 40.7 ± 3.4. In the CG, the T2 score did not increase significantly (31.2 ± 5.2, effect size, Cohen d = 1.94). At 3 months (T3), a further increase in knowledge score was observed in the IG from 40.7 ± 3.4 to 42.7 ± 4.0, P<0.001) and in the CG from 31.2 ± 5.2 to 37.8 ± -6.3 (P<0.001) (see Table 3).

Using a paired sample t-test to compare results between the IG and CG from T1 to T2 and T3, the increased mean difference in knowledge scores was noted to be significantly higher in the IG than in the CG (-8.2  ± 5.4, t = -17.0, P<0.001, d = 0.385) (see Table 4), suggesting the intervention accounted for 38.5% of the change in knowledge scores. 

Effect of selected demographic characteristic. The effect of selected demographic characteristics (eg, years of experience, professional cadre, and previous exposure to a PU lecture) on respondents’ scores pre- and post intervention was determined using one-way ANOVA. Findings were not significant (see Table 5). An examination⁴⁵ of the combined effect (interaction) of selected respondents’ factors (eg, years of experience, previous exposure to PU lecture) on the post test scores using a one-way ANOVA showed a significant interaction effect with previous exposure to PU education (F[1,192] = 2.781, P<0.05). However, the interaction effect with both years of experience and professional cadre was not significant (P>0.05).

Discussion  

The aim of this study was to examine the effectiveness of a face-to-face, interactive PU lecture approach to education on knowledge retention among nurses by comparing pretest and post test knowledge scores. The major hypothesis was that nurses will be able to retain knowledge for 3 months post intervention better than nurses who were not exposed to a similar learning method. The intervention was carried out in the same manner by the researcher in all the settings using the modules designed for the program. Participants were selected from neurology, orthopedic surgery, and medical inpatients units because reports from previous studies indicated the risk of PU was higher in patients admitted to these units as a consequence of impaired physical mobility.⁴⁵ Results of Niederhauser et al’s⁴⁶ systematic review of literature underscored the importance of PU educational programs in successful implementation of preventive protocols.  

The current study showed nurses had some basic knowledge about PU prevention because they were experienced practitioners. However, after the interactive lecture, the knowledge level increased significantly in the IG as compared to what was observed in the CG.   In addition, participants were able to retain the knowledge acquired as indicated by the mean scores at the 3-month follow-up. This suggests the intervention was effective. In contrast to these findings, reports from previous quasi-experimental studies^30,31 involving nursing and medical science students showed students tend to forget ~80% of presented education within 8 weeks of a lecture. The current findings showed knowledge of PU prevention was sustained for 12 weeks (3 months) post intervention among the study cohort, as well as in the CG. This sustained knowledge retention may be linked to the fact respondents in both groups were adult learners, with varied previous experiences and learning they brought to the fore. In addition, hands-on experience and reinforcement of what was learned during the follow-up period in the IG could have contributed to the sustained knowledge 

Khatoni et al’s⁴⁷ pretest/post test study among nurses (N = 140) suggested both lecture and elearning methods are effective in increasing students’ knowledge. Although opinions tend to differ regarding the most effective method of teaching, evidence supports the effectiveness of interactive lectures, which enhance active student engagement and participation and demonstrate more positive learning gains than traditional lecture methods. For example, from results of their study, Prince and Felder³⁹ proposed inductive learning methods, including cooperative or team learning, active learning, case studies, projects, or presentations, are more effective than the traditional lecture. 

In this study, sustained knowledge retention may be explained using the principles of cooperative learning as proposed by Johnson et al.⁴⁸ Accordingly, the authors described cooperative learning as the instructional use of small groups to facilitate students’ working together to maximize their learning through mutual dependence rather than competition. It is proposed such learning strategy promotes deep understanding of the subject matter and enhances knowledge retention. It follows that within the small groups, participants can easily exchange views and develop self-confidence. Johnson and Johnson⁴⁹ also believed working/learning in small groups works among health care professionals to help develop communication skills essential for building stronger communication with patients.  

In the current study, participants worked in small groups based on their respective wards. During the 3-month follow-up period, the researcher visited the nurse participants on the wards weekly, and teaching was reinforced at the bedside to promote evidence-based practice. The practice component is not part of this current report. The authors strongly believe the small group discussions and the supplemental printed materials (ie, PowerPoint® slides) sustained the interactive learning and also enhanced self-instruction and knowledge retention. Additionally, participants were experienced practitioners. Goldberg et al’s⁵⁰ pretest/post test study (N = 130) noted interactive lecture increased students’ self-efficacy, which is  associated with academic achievement. Similarly, Knight and Wood’s⁵¹ pretest post test study (N = 700) to compare the learning gains between traditionally taught lecture and interactive classroom format concluded collaborative work in student groupings and discussions significantly increased learning gains and conceptual understanding. Furthermore, Prince and Felder³⁹ noted a strong motivation to learn when learners clearly perceive a need to know. It follows that learners’ perception of their specific learning needs influences the motivation to learn. The findings in the current study also can be explained by Kolb’s³⁸ model of experiential learning, which hypothesized that concrete experience allows for reflection (ie, incorporation of experience with teaching). The current study authors assert such reflection was demonstrated by study participants, which possibly also strengthened their ability to recall new knowledge, as observed only in the IG. 

Adult learners have previous experiences that help illuminate a new learning situation. As such, the current study examined the interaction effect of treatment, years of experience, and exposure to previous PU lectures on post test scores in the IG and CG. The findings indicated a significant difference, suggesting the educational intervention accounted for the difference in post test scores and was not independently determined by demographic characteristics. This finding is consistent with Hulsenboom et al,⁵² whose cross-sectional, comparative study among nurses (N = 522) concluded demographics, including age and nurse experience, had no significant influence on knowledge of PU preventive interventions. 

Nurses play a significant role in PU prevention, requiring ongoing acquisition of knowledge. Because the interactive lecture contributed significantly to knowledge retention, a more consistent use of interactive methods of teaching, such as case presentations, brainstorming, and small group discussions, is suggested for continuing nurse education.  

Limitations 

The present study was conducted among nurses in 3 tertiary institutions. A study with a wider scope that may include nurses in secondary care facilities is warranted. In addition, comparison of the effectiveness of lecture with other methods of program delivery also should be considered. 

Limitations also include the fact the interactive face-to-face lecture method was compared with only 1 other method of program delivery (discussion group), so the findings should be interpreted with caution. Additionally, the pretest/post test design of this study limits the degree to which the results may be attributed to the effects of the intervention (ie, the authors had no control over natural events in the comparison group hospital). Therefore the effects of history may be a threat to internal validity. In this vein, history describes events that occur concurrently with the treatment, which the researcher may not have control over, thereby influencing the results obtained. In the current study, the possibility of another educational program in the CG institution during the period of this study that could provide information on the subject matter to respondents cannot be ruled out. To the best of the authors’ knowledge, the CG participants were not exposed to another learning situation except that the intervention package was provided at the end of the study to the CG participants. Finally, knowledge retention was monitored for only 3 months post intervention.

Conclusion 

A pretest/post test study was conducted to measure gains in knowledge retention for nurses following an interactive lecture on PU prevention. The results demonstrate an interactive lecture using small groups can effectively facilitate knowledge retention among nurses in a continuing education program. The effect of intervention was significantly higher in the IG than in the CG. Interactive engagement of nurses and inductive methods of instruction for program delivery appear to be successful approaches in continuing education programs for nurses. Future studies are needed to examine how acquired knowledge translates into effective PU prevention practices and influences clinical outcomes. 

References

1. Graves N, Birrell F, Whitby M. Effect of pressure ulcers on length of hospital stay. Infect Control Hosp Epidemiol. 2005;26(3):293–297.

2. Gorecki C, Brown JM, Nelson EA, et al; European Quality of Life Pressure Ulcer Project group. Impact of pressure ulcers on quality of life in older patients: a systematic review. J Am Geriatr Soc. 2009;57(7):1175–1183.

3. National Quality Measures Clearinghouse. Pressure ulcers: percentage of patients with documented assessment of risks for possible pressure ulcer development, 2005. Available at: www.qualitymeasures.ahrq.gov/summary.aspx?ss=1&doc_id=6428.  Accessed February 12, 2015. 

4. McInerney JA. Reducing hospital-acquired pressure ulcer prevalence through focused prevention program. Adv Skin Wound Care. 2008;21(2):75–78. 

5. Zakrasek EC, Creasey G, Crew JD. Pressure ulcers in people with spinal cord injury in developing nations. Spinal Cord. 2015;53(1):7–13.

6. Tweed C, Tweed M. Intensive care nurses knowledge of pressure ulcers: development of an assessment tool and effect of an educational program. Am J Crit Care. 2008;17(4):338–346.

7. Cox JR, Roche S, Van Wynen E. The effect of various instructional methods on retention of knowledge about pressure ulcer among critical care and medical surgical nurses. J Continuing Ed Nurs. 2011;42(2):71–78. 

8. Andrade EMLR, Cavalcanti PAL, Monteiro AKC, et al. Effect of educational intervention by attendance and distance on nurses’ knowledge about pressure ulcer. Creative Ed. 2014;5(18):1673–1677.

9. Miyazaki MY, Caliri MH, dos Santos CB. Knowledge on pressure ulcer prevention among nursing professionals. Rev Lat Am Enfermagem. 2010;18(6):1203–1211.

10. Magnan MA, Maklebust J. The nursing process and pressure ulcer prevention: making the connection. Adv Skin Wound Care. 2009;22(2):83–92.

11. Hopkins B, Hanlon M, Yauk S, Sykes S, Rose T, Cleary A. Reducing nosocomial pressure ulcers in acute care facility. J Nurs Care Qual. 2000;14(3):28–36.

12. Padula CA, Osborne E, Williams J. Wound care: prevention and early detection of pressure ulcers in hospitalized patients. J Wound Ostomy Continence Nurs. 2008;35(1):66–75.

13. Mei-Yu H, Wen-Yi T, Huei-chuan C. The effectiveness of educational programs in promoting nurses’ knowledge of pressure ulcers: a systematic review protocol. JBI Database Syst Rev Implementation Reports (SI). 2013;11(5):132–139.

14. Chianca TC, Resende JF, Borges EL, Nogueira VL, Caliri MH. Pressure ulcer among nurses in Brazilian university hospital. Ostomy Wound Manage. 2010;56(10):58–64. 

15. Adejumo PO. Nurses perception of activities at preventing pressure sore among selected patients at the University College Hospital, Ibadan. West African J Nurs. 2010;21(2):90–98.

16. Ilesanmi RE, Ofi BA, Adejumo PO. Nurses’ knowledge of pressure ulcer prevention in Ogun state, Nigeria: result of a pilot survey. Ostomy Wound Manage. 2012;58(2):24–32. 

17. Haesler E (ed). European Pressure Ulcer Advisory Panel, National Pressure Ulcer Advisory Panel and Pan-Pacific Pressure Injury Alliance. Prevention and Treatment of Pressure Ulcers:Clinical Practice Guideline. Perth, Australia: Cambridge Media;2014.

18. American Nurses Association National Quality Forum (ANANQF). Nursing-Sensitive Indicators, 2015. Available at: www.nursingworld.org.  Accessed April 12, 2015.

19. The Joint Commission on Accreditation of Healthcare Organization (JCAHO).  National Patient Safety Goals. 2012, Available at: www.jointcommission.org/standards information/npsgs.aspx. Accessed March, 5, 2015. 

20. Gunningberg L. Pressure ulcer prevention: evaluation of an education program for Swedish nurses. J Wound Care. 2004;13(3):85–89.

21. Qaddumi J, Khawaldeh.  Pressure ulcer prevention knowledge among Jordanian nurses: a cross-sectional study. BMC Nurs. 2014;13(6). Available at: www.biomedcentral.com/1472-6955/13/6. Accessed March 13, 2015.

22. Lepistö M, Eriksson E, Hietanen H, Asko-Seljavaara S. Patients with pressure ulcer in Finnish hospitals. Int J Nurs Pract. 2001;7(4):280-287.

23. Ikechukwu EC, Ayodiipo IO, Emeka AD, Kayode AJ, Michael NI, Deborah OT. Prevalence and factors associated with healing outcomes of hospital-acquired pressure ulcers among patients with spinal cord injury. J Pub Health Epidermiol. 2012;4(2):44–47. 

24. Onigbinde AT, Ogunsanya GI, Oniyangi SO. Pressure ulcer incidence among high risk in-patients in Nigeria. Br J Nurs. 2012;21(12):S4–S10.

25. Awwal LM, Ngaski GS, Khalid SD,  Hadiza SM, Farouk MA. Pressure ulcer stages among bed-ridden patients in ABUTH, Zaria. IOSR J Nurs Health Sci. 2014;3(1):61–68.

26. Eustace LW. Mandatory continuing education: past, present, and future trends and issues. J Continuing Ed Nurs. 2001;32(3):133–137.

27. Chong MC, Francis K, Cooper S, Abdullah K. Current continuing education practice among Malaysian nurses. Nurs Res Pract. Available at: www.hindawi.com. Accessed March 17, 2015.

28. Abbasi K, Hazrah M. Mohamadi NP, Rajaeefard A. The effects of learning via modules versus lecture teaching methods on knowledge and practice of oncology nurses about safety standards with cytotoxic drugs in Shiraz University of medical Sciences. IranianJ Nurs Midwifery Res. 2013;18(6):483–487.

29. Norouzi HM, Mohsenizadeh SM, Jafary SH, Ebrahimzadeh S. The effect of teaching using a blend of collaborative and mastery of learning models, on learning of vital signs: an experiment on nursing and operation room students of Mashhad University of Medical Sciences. Iranian J Med Ed. 2011;11(5):544–553.

30. Sadeghi R, Sedaghat MM, Ahmadi F. Comparison of effect of lecture and blended teaching methods on students learning and satisfaction. J Adv Med Ed Profession. 2014;2(4):146–150. 

31. Safari M, Yazdanpanah B, Ghafarian HR, Yazdanpanah S. Comparing effect of lecture and discussion methods on students’ learning and satisfaction. Iran J Med Ed. 2006;6(1):59–64.

32. Beeckam D, Schoonhoven L, Boucqué H, Van Maele G,  Defloor T. Pressure ulcers: e-learning to improve classification by nurses and nursing students. J Clin Nurs.2008;17(13):1697–1707.

33. Garrison DR, Kanuka H. Blended learning: uncovering its transformative potential in higher education. Internet Higher Ed. 2004:7(2):95–105.

34. Knowles M. The Adult Learner: A Neglected Species. Houston, TX: Gulf Publishing Company;1990.

35. Sobral D. An appraisal of medical students’ reflection-in-learning. Med Ed. 2000;34(3):182–187.

36. Grant A, Kinnersley P, Metcalf E, Pill R, Housten H. Students’ view of reflective learning techniques: an efficacy study at UK medical school. Med Ed. 2006;40(6):376–388.

37. Sandars J. The Use of Reflection in Medical Education: AMEE Guide NO.4. 2009. Available at: www.medsqueensu.ca. Accessed March 7, 2015.

38. Kolb DA. Experiential Learning: Experiences as the Source of Learning and Development. Englewood Cliffs, NJ: Prentice Hall;1984.

39. Prince MP, Felder RM. Inductive teaching and learning methods: definitions, compositions and research bases. J Engineer Ed. 2006;95(2):123–138.

40. Eidin YKZ. Implementing interactive nursing administration lectures and identifying its influence on students’ learning gains. J Nurs Ed Pract. 2014;4(5):107–115.

41. Steinert Y, Snell LS. Interactive lecturing: strategies for increasing participation in large group presentations. Med Teacher. 1999;21(1):37–42.

42. Lee VS (ed). Teaching and Learning Through Inquiry: A Guidebook for Institutions and Instructors. Sterling, VA: Stylus Publishing;2004.

43. Pieper B, Mott M. Nurses’ knowledge of pressure ulcer prevention, staging and description. Adv Wound Care. 1995;8(3):34–48.

44. Sinclair L, Berwiczonek H, Thurston N, et al.  Evaluation of an evidence-based education program for pressure ulcer prevention. J Wound Ostomy Continence Nurs. 2004;31(1):43–50.

45. Adyin AK, Karadag A. Assessment of nurses’ knowledge and practice in prevention and management of deep tissue injury and stage I pressure ulcer. J Wound Ostomy Continence Nurs. 2010;37(5):487–494.

46. Niederhauser A, Lukas V, Parker V, Ayello EA, Zulkowski K, Berlowitz D.  Comprehensive programs for preventing pressure ulcers: a review of the literature.  Adv Skin Wound Care. 2012;25(4):167–188.

47. Khatoni A, Nayery N. D, Ahmady F, Haghani H. Comparison of effect of web-based education and traditional education on nurses knowledge about bird flu in continuing education. Iranian J Med Ed. 2011;11(2):140–148.

48. Johnson D, Johnson RT, Smith KA. Active Learning: Cooperative in the College Classroom, 2nd ed. Edina, MN: Interaction Books Company;1998.

49. Johnson DH, Johnson FP.  Joining Together: Group Theory and Group Skills, 8th ed. Boston, MA: Allyn and Bacon;2003.

50. Goldberg HR, Haase E, Shoukas A, Schramm L. Redefining classroom instruction. Adv Physiol Ed. 2006;30(3):124–127.

51. Knight JK, Wood WB. Teaching more by lecturing less. Cell Biol Ed. 2005;4:298–310.

52. Hulsenboom MA, Bours GJ, Halfans RJ. Knowledge of pressure ulcer prevention: a cross-sectional and comparative study among nurses. BMC Nurs. 2007;6(2). doi: 10.1186/1472-6955-6-2

Dr. Ilesanmi is a lecturer and a certified wound care nurse, Department of Nursing; and Prof Oluwatosin is a Professor of Plastic and Reconstructive Surgery, Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria. Please address correspondence to: Dr. Rose Ekama Ilesanmi, Department of Nursing, University of Ibadan, Ibadan, Nigeria; email: ekamailesanmi@yahoo.com.

Potential Conflicts of Interest: none disclosed 

Abstract

Heels are susceptible to pressure ulcer (PU) development. Some evidence suggests dressings may provide mechanical cushioning, reduce friction with support, and lower localized internal tissue loading, which together may minimize the risk for heel ulcers (HUs). To examine the effect of dressing application on pressure ulcer prevention, 20 computer simulations were performed.

Volumetric exposure of soft tissues to effective and shear strains and stresses, with and without a multilayered foam dressing, were assessed, with the extent of tissue exposure considered as measures of the theoretical risk for PUs. The simulations, conducted using the finite element method, provided the mechanical strain and stress magnitudes and distributions in the weight-bearing tissues of the heel, which were visualized and analyzed post-hoc for comparing diabetic to healthy tissue loads with/without prophylactic dressings and at different foot (plantar flexion) postures. The volumetric exposure of the soft tissues of the heel to elevated strains and stresses was considerably reduced by the presence of the dressing, whether diabetic or nondiabetic tissue conditions existed, and for the entire range of the simulated plantar flexion positions. Further, greater plantar flexion, which occurs with elevation of the head of the bed, reduced the volumetric exposure of subcutaneous fat to increased effective strains and stresses, again, particularly when the dressing was on. Specifically, peak (maximum of raw data) effective strains in the soft tissues of the heel decreased by 14.8% and 13.5% with the use of the dressing for healthy persons and persons with diabetes, respectively. Additionally, volumetric exposures of the soft tissues to large effective strains, defined as exposures to >50% strain, decreased substantially, by at least a factor of 2, with the angle of plantar flexion and with respect to a neutral foot posture. Volumetric exposures to midrange (<50%) strains were more mildly affected by the foot posture (ie, <10% difference was noted across plantar flexion angles). The differences in tissue exposures to strains and stresses between the dressing and nondressing models suggest this dressing provides an important biomechanical protective effect, specifically when diabetic tissue conditions exist. In addition, the data suggest alleviating shear by repositioning the heels after elevating the head of the bed may be critical in order to limit the increase in tissue stress and subsequent PU risk. Randomized, controlled clinical studies to examine the efficacy of dressings for the prevention of heel PUs are warranted. 

Surveys^1-4 show heel ulcers (HUs) are the most common type of facility-acquired pressure ulcers (PUs), and the heels are the most common site for deep tissue injury (DTI).Clinical trials have identified PUs as generally being associated with a number of contributing or confounding factors, such as impaired mobility and sensory capacities, compromised perfusion, increased body mass index, and type 2 diabetes, to name a few.^5,6 During prolonged supine bed rest, the weight of the foot and ankle is transferred through the calcaneus bone to the support surface, subjecting subcutaneous fat and skin near the heel-support contact site to sustained mechanical loads, as demonstrated theoretically and in computer simulations.⁷ In lack of mobility or sensitivity or both, the sustained tissue loads may exceed tissue tolerance levels, increasing the risk for HUs.⁷ In persons with type 2 diabetes, in particular, peripheral sensory neuropathy may prevent patients from detecting the onset and progression of tissue damage, which has been documented in numerous clinical cases.⁸ 

Finite element (FE) computational modeling is a powerful tool in PU research (see Sidebar: Finite Element Computational Modeling). FE modeling facilitates quantification of internal tissue strains and stresses in weight-bearing body parts such as the heels and buttocks.^6,9-12 This method is further able to isolate the influence of specific intrinsic and extrinsic biomechanical factors on the resulting risk for PUs and DTIs, as demonstrated in various previous computational modeling studies.^10-13 Briefly, the 3-dimensional (3D) anatomical model, usually derived from medical imaging such as magnetic resonance imaging (MRI), is divided into hundreds of thousands of small elements in the computer. The material properties and loading configuration is defined for each simulation; the computer then is able to calculate the mechanical reaction of the model for each element with respect to its neighboring elements, ultimately constructing the solution of the biomechanical problem for the entire structure. For example, in a previous study from the authors’ group, Sopher et al¹² employed FE computational modeling to investigate how variation of tissue stiffness properties and degree of external rotation of the foot may affect the internal state of fat and skin strains and stresses in the resting heel for supine body postures. The authors demonstrated how lateral inclination of the foot might jeopardize tissue integrity by exerting higher strains and stresses on the soft tissues of the lateral aspect of the heel; however, their study did not include representation of the anatomical site of insertion of the Achilles tendon into the calcaneus bone nor did it examine the effect of diabetic tissue conditions or shearing forces acting on the foot.

Type 2 diabetes has been experimentally associated with stiffening of collagen-rich soft tissues, an effect demonstrated in both animal models and testing of human tissue specimens, as reviewed in detail in the modeling study of Gefen,⁸ which was focused on the influence of such connective tissue stiffening on the function of the foot. Mechanical testing^8,14-16 consistently demonstrated stiffening of fat and skin; however, Connizzo et al¹⁷ reported reduced stiffness of the tendon tissue at the insertion site of the Achilles tendon into the calcaneus of mice. Because this insertion site is compositionally and structurally different from the midsubstance of the tendon, diabetes-related alterations at the insertion region may be expressed differently than at other parts of the tendon.

Given that PUs (and HUs in particular) are a major burden for health care facilities and that apart from their devastating impact on the quality of life of sufferers these wounds are known to be difficult and costly to treat, all of which has been documented extensively in patient safety, quality-of-life and health-economy human studies,^18-20 great efforts are focused on prevention. Although complete offloading of the heels still is considered the most effective method for preventing HUs,⁷ it is not always feasible in the long-term, especially when considering patient movement. An illustrative example is a patient who can be immobile for hours but from time to time suffers seizures that cause his legs to move and change position. 

A prevention concept that is attracting the attention of several research groups around the world is the prophylactic use of dressings in order to protect the heels from HUs.^7,21,22 In the past few years, the efficacy of such dressings in preventing HUs has been confirmed by more than 20 different clinical studies summarized in a recent systematic review²² that included randomized controlled trials (RCTs), cohort, and case series studies. In addition, positive reports have been published of contact pressure and shear measurements in experimental (laboratory) models.^23-26  Recently, the development was reported of a 3D, MRI-based FE computational model for investigating the internal mechanical strains and stresses in the soft tissues of the supported heel and how these are influenced by the use of a prophylactic dressing.²⁷ Although this research did not consider diabetic tissue conditions, clinicians often consider diabetes as a risk factor for HUs⁶ more because of the patient’s impaired sensation and perfusion and less because the biomechanics of the soft tissues are altered. Nevertheless, theory and computer modeling show abnormal biomechanical properties of diabetic connective soft tissues, where the tissues cannot adequately deform to dissipate the body loads, play a role in the overall risk of injury.⁸

In addition to prophylactic dressing use, another consideration is the posture of the ankle relative to bed elevation. A case-control study by Singer et al²⁸ suggested the relaxed posture of the ankle in supine lying is external rotation with relative plantar flexion, but elevation of the head of the bed may increase the angle of plantar flexion in the relaxed ankle joint. Furthermore, in a review of relevant case series studies, guidelines, observational studies, and expert opinions, Fowler et al²⁹ concluded elevating the head of the bed may induce additional shearing forces on the weight-bearing soft tissues of the heels, which should be examined in combination with diabetic tissue conditions given the fragility of the diabetic heel. 

Mepilex^® Border Heel (Mölnlycke Health Care, Gothenburg, Sweden) is a 5-layer dressing consisting of 1) a backing film which faces the support, 2) an airlaid layer, 3) a nonwoven layer, 4) a polyurethane foam layer, and 5) a Safetac^® layer that adheres to the skin.²⁷ This specific dressing is indicated for both prevention and treatment of pressure ulcers and has already been used in randomized clinical trials^5,24 where it was shown to be effective as a prophylactic intervention. 

The purpose of this study is to expand the authors’ previously published work²⁷ that demonstrated the biomechanical efficacy of a prophylactic dressing in protecting the heels in order to account for diabetic tissue conditions. For this purpose, sets of computational model variants of the heel in supine lying were developed to represent patients with diabetes with their heels resting in a range of plantar flexion positions, as well as corresponding simulations of healthy tissue conditions.  

Methods 

Geometry. A set of 20 FE computational model variants was developed, representing diabetic tissue conditions and comparable healthy tissue cases at different foot postures, as specified in Table 1. Each model variant captured the anatomy of the posterior aspect of the heel, including the calcaneus bone, distal Achilles tendon, fat, and skin (see Figure 1a). Flat elastic foam was modeled as the support surface (see Figure 1a). Ten (10) of the model variants did not include the multilayered dressing and were used as reference cases, which then could be compared to cases where the foam dressing was incorporated (see Table 1). Variants 1–4 were set to a neutral foot position (0˚ plantar flexion) and variants 5–8, 9–12, and 13–20 were set to 10˚, 20˚, and 30˚ of plantar flexion, respectively (see Table 1, Figure 1). For each position of the foot tested, either diabetic or healthy soft tissues properties were assigned. 

The anatomical structures of the posterior heel from the MRI dataset, as well as geometrical modeling of the dressing, were segmented as described in the authors’ previous work.²⁷ Briefly, 56 T1-weighted axial MRI slices from the suspended left heel of a healthy man were used to develop an anatomically realistic, 3D, undeformed model geometry, using the ScanIP^® module of the Simpleware^® software package^30,31(Simpleware, Exeter, United Kingdom). For clinical relevance, the study dressing was modeled (the specific considerations regarding the geometrical and material modeling of the dressing have been published previously²⁷). The innermost and outermost layers of the dressing were modeled as contact conditions and used according to the manufacturer’s specifications to describe the airlaid (layer 2), nonwoven (layer 3), and polyurethane foam (layer 4) as physical layers in the modeling. The flat foam support (10-mm thickness) was added to all the heel model variants at the preprocessing stage in the PreView module of the FEBio software package.³² 

Mechanical properties of the tissues and dressing. Constitutive laws and mechanical properties of all the tissues included in the heel model were adopted from the literature (see Table 2). Specifically, the healthy Achilles tendon and calcaneus bone were assumed to be linear-elastic isotropic materials (ie, having a constant stiffness that does not depend on the extent of deformation nor does it depend on the direction of the deformation) with instantaneous elastic moduli of 205 kPa and 7 GPa, and Poisson’s ratios (indicating a material’s deformation at a direction perpendicular to the loading direction) of 0.49 and 0.3, respectively^33,34 (see Table 2). Skin and fat tissues were assumed to be nearly incompressible (Poisson’s ratio of 0.495), nonlinear isotropic materials. The large deformation mechanical behavior of skin and fat was described by an uncoupled Neo-Hookean material model³⁵ with instantaneous shear moduli^33,36 (see Table 2). Based on the literature, the instantaneous shear moduli of diabetic skin and fat tissues were assumed to be 40% stiffer than the corresponding healthy tissue¹⁴; likewise, the diabetic Achilles tendon was assigned a 40% softer instantaneous elastic modulus¹⁷ (see Table 2). The flat foam support was assumed to be isotropic linear elastic with a Poisson’s ratio of 0.3 and an elastic modulus of 45 kPa, which are within the range of hospital mattress properties.³⁷ Layers 2, 3, and 4 were assigned instantaneous elastic moduli of 15.3, 75, and 12 kPa, respectively, according to the measurements described previously²⁷ (see Table 2). The Poisson’s ratios of all dressing materials³⁸ were set as 0.258 (see Table 2). 

Body loads applied to the model, shear, and friction conditions. The loads applied to the model were chosen to simulate the descent of the calcaneus bone against a flat foam support during supine weight-bearing. For calibration, tissue deformations were measured from a weight-bearing MRI of the heel of the same subject to find the weight force the heel applied on the support. Because the total reaction force should be equal to the weight of the foot/ankle in the supine position, this datum was used to produce the same heel-support reaction forces in all the model variants. The resulting compressive (downward) displacements after imposing the same foot/ankle weight value in all the model variants were in the 4.7-mm to 5.2-mm range. Additionally, in order to represent shearing forces acting on the foot when the head of the bed is elevated, and by doing so to evaluate the importance of subsequent heel repositioning in patients with and without diabetes, model variants 17–20 were used. In these specific variants, a combination of compression and shear loading was employed, where shear displacements were taken as equal to the compressive ones²⁷ (see Table 1). The bottom surface of the elastic foam support was fixed for all motions. Tied (fixed) interfaces were defined between all tissue components as well as between the skin and the polyurethane foam layer of the dressing (layer 4) to account for the adherence properties of the innermost Safetac^® layer of the dressing that interfaces the skin (layer 5). Frictional contact between the support and either the skin of the bare heel or the outer surface of the dressing was defined, with the coefficients of friction set as 0.43 and 0.35 for the skin-support and dressing-support contacts, respectively.^27,38,39 

Creating the computational simulations. The tissues and dressing were meshed using the ScanIP^® module of Simpleware^®,³⁰ with mesh refinements that were applied in the skin and dressing materials near the contact area with the support (see Figure 1a). Meshing the support was performed in the Preview module of FEBio.³² All of the above FE simulations were set up using the PreView module of FEBio (Version 1.14), analyzed using the Pardiso linear solver of FEBio (http://mrl.sci.utah.edu/software/febio) (Version 1.7.1) and post-processed using the PostView tool of FEBio (Version 1.4).³² 

Biomechanical outcome measures. The volumetric exposures of the soft tissues to mechanical strains were systematically compared using the effective Green-Lagrange strain as the strain measure.³⁵ The effective Green-Lagrange strain is an adequate measure of large tissue deformations and the consequent risk for HUs because it is simultaneously considering tissue deformations in all loading modes (ie, compression, tension and shear) using a single weighed (scalar) measure. The strain data were pooled together from tendon, fat, and skin tissues for all elements in a consistent volume of interest in the meshes, which was defined by the circumference of the calcaneus and its projection at the retrocalcaneal region, as illustrated in Figure 1b. Additionally, peak effective and maximal shear stresses (shear stresses arise from shape distortion of the tissues due to forces parallel to the cross-sections of the tissues) in fat and skin tissues were compared separately as a second measure of the risk for HUs. For clarification, effective strain and stress measures consider compression, tension, and shear loads altogether, as opposed to just the aforementioned (maximal) shear measures, which do not consider tension and compression loads. The stress data were pooled from all the elements of skin or separately from those of fat. Converged time steps for data collection were chosen so the resulting reaction forces acting back from the support were within <3% difference from the predefined target reaction force (as explained previously). Hence, the biomechanical efficacy of the dressing was evaluated in diabetic and healthy tissue conditions based on the criteria of reduction in volumetric exposures of the soft tissues to critical effective and shear strains and stresses. The verification of the reference model variant based on the calculated interface pressures under the heel and corresponding compressive strains in the support, which have been compared to published experimental data, is described in a previous paper by the authors that fully validates the present modeling framework.²⁷ 

Data collection and analyses. Excel software (Microsoft Co, Spokane, WA) was used for the post-hoc analyses of the finite element simulations and for plotting and quantitatively comparing the results of all simulations. It should be mentioned that means and standard deviations are not provided because no variability in the modeling outcomes exists when the parameters of the models are set at a certain way (see Sidebar). Accordingly, no variance around the mean and no average values are reported — just a single value of each parameter that is calculated from a predefined set of simulation parameters (eg, peak tissue strain is calculated based on a simulated set of specific tissue mechanical properties and whether a dressing is present or not). The standard deviations are zero; each time the same simulation is run, the same outcome is obtained. 

Results

Effective strain distributions in the soft tissues of the heel in a neutral position and in 10˚, 20˚, and 30˚ plantar flexion, without and with the protection of the dressing, are shown in Figure 2 and Figure 3, respectively. Consistent with the authors’ previous work,²⁷ peak effective strains were found at the bone-fat interface in all the model variants and these were shifted distally with an increase in plantar flexion (see Figures 2, 3). Specifically, peak (maximum of raw data) effective strains in the soft tissues of the heel decreased in presence of the dressing by 14.8% and 13.5% for the healthy persons and persons with diabetes, respectively. Additionally, volumetric exposures of the soft tissues to large effective strains, defined as exposures to >50% strain, decreased by at least a factor of 2 with the angle of plantar flexion and with respect to the neutral position of the foot. Volumetric exposures to midrange (<50%) strains were more mildly affected by the foot posture (ie, <10% was noted difference across plantar flexion angles) (see Figure 4).

Substantial alleviation of internal peak effective tissue stresses when the dressing was on, with respect to corresponding conditions when it was off, was evident in all foot positions for both the diabetic and healthy tissue conditions (see Figure 5); the most pronounced effect occurred in skin tissue that was subjected to less intense deformation exposures (see Figure 5 – dressing on versus dressing off). Specifically, peak effective stresses in the soft tissues of the heel decreased by 25.5% and 22.2% in the presence of the dressing for healthy and diabetic cases, respectively. Overall, diabetic tissue conditions yielded greater effective and shear stresses in skin and fat tissues and lower stresses in the Achilles tendon with respect to healthy corresponding tissues (see Figure 5). 

Effective stress distributions on the exterior skin surface in a neutral foot position after simulated elevation of the head of the bed and following subsequent repositioning of the heel are shown in Figure 6. The substantial increases in effective and shear stresses on the skin with the elevation of the head of the bed are considerably restrained by the use of the dressing; exposure to skin stresses is reduced by a factor of 2 to 3, and exposure to fat stresses is reduced by a factor of ~1.5 with application of the dressing, in either nondiabetic or diabetic tissue conditions (see Figures 6, 7). Furthermore, shear alleviation through repositioning of the heel was able to reduce the effective and shear stresses developing in skin tissues in diabetic and healthy cases between 20% and 40% across the different cases (see Figure 7), which is substantial. This occurred either with or without the presence of the dressing (see Figures 6, 7a,b), which points to the importance of offloading (elevating) the heels whenever shear in tissues is suspected (eg, immediately after the head of the bed is elevated). 

In general, volumetric exposure of fat tissue to effective stresses decreased with the angle of plantar flexion with respect to a neutral foot position and with elevation of the head of the bed. Nevertheless, alleviating shear by repositioning the heels was able to further reduce the volumetric exposures of fat tissues to effective stresses exceeding critical levels¹² with regard to a state where no offloading has been performed (see Figure 7c). This again points to the importance of repositioning the heels — elevating and then gently resting them on the mattress again whenever internal tissue shear is suspected, such as in cases where the head of the bed has been lifted or where a patient appeared to have slipped down in the bed. Doing so is still important even if prophylactic dressings are being used (see Figure 7). 

Discussion

This study employed 20 MRI-based FE model variants of the heel in a supine posture for a range of plantar flexion positions in order to investigate the biomechanical efficacy of a prophylactic heel dressing in preventing HUs if diabetic tissue conditions exist. In accordance with the authors’ previous work,²⁷ the heel dressing was found to consistently and considerably reduce the volumetric exposure of the soft tissues of the heel to elevated strains and stresses with respect to a bare heel condition (see Figures 2–7), whether diabetic or nondiabetic tissue conditions existed, and for the entire range of the simulated plantar flexion positions. Further, greater plantar flexion reduced the volumetric exposure of subcutaneous fat to increased effective strains and stresses. This finding can be explained by the thicker subcutaneous fat layer facing the support surface and the growing distance of the heel-support contact site from the insertion area of the (stiffer) Achilles tendon as the degree of plantar flexion increases.^12,31 However, skin tissues seem to be conversely affected. As the angle of plantar flexion increases and subcutaneous fat deformations decrease, greater effective and shear stresses occur in skin tissues (see Figure 7a,b). Nevertheless, the dressing was able to considerably limit that increase in effective and shear stresses in the skin with respect to a bare heel condition to the point where the use of the dressing in plantar flexion of 30˚ resulted in lower skin stresses than for a neutral position without the dressing. This result was consistently observed for both diabetic and nondiabetic tissue conditions, which may suggest the use of bed footrests to maintain the foot in minimal plantar flexion is redundant if the dressing is placed for protection. However, this is subject to additional clinical studies. 

Elevating the head of the bed, some spontaneous movements of the patient, or repositioning that has not been carefully performed all can result in an increased plantar flexion angle of the foot and the addition of shear forces acting on the supported posterior heel. As expected, such additional shear forces were shown in this study to substantially exacerbate the states of effective and shear stresses in skin tissues. Based on this study, temporarily lifting (offloading) and then repositioning the heels on the support surface immediately after elevating the head of the bed or, in general, after repositioning, is crucial to tempering this increase in skin stresses. Furthermore, patients who are positioned in bed with their heads elevated (eg, to improve respiration) tend to slide down on the bed over time due to gravity, which then causes the development of recurrent shear loads in the weight-bearing soft tissues of the heels (and in the buttocks as well).⁴⁰ Based on the present findings, the use of the dressing should theoretically minimize skin and subcutaneous fat stresses, even if shear loads redevelop over time (see Figure 7).

Questions have been raised regarding the modes of action and the sustainability of the protective effect of the dressing, and some bench tests were performed in this regard.³⁸ In the current simulations, the cushioning effect of the dressing is formally calculated for a short period (in the order of minutes) following a positioning/repositioning action; however, results can still be generalized and extrapolated to longer times (ie, in the order of several hours) of immobility, within which transient viscoelastic phenomena typically plateau in tissues. This theoretical extrapolation can be made because the instantaneous dressing and tissue stiffness properties were considered, thereby describing the worst-case scenario in terms of exposure to internal tissue strains and stresses.^6,27,41 Also, the authors’ previously published laboratory findings²⁷ show negligible viscoelasticity of the dressing materials, so the cushioning effect of the dressing should persist, which further supports the above point.  

Based on animal model studies as well as mechanical tests of human tissue specimens, which are reviewed in Gefen,^6,8 the altered mechanical properties of the skin, subdermal fat, and Achilles tendon in diabetes appear to play an important role in the etiology of HUs (and PUs in general). Although increased soft tissue stiffness (as in skin and fat) increases the risk of elevated tissue stresses, abnormal softening of tissues (such as at the insertion of the Achilles) exposes the affected and nearby tissues to an increased risk of deformation-inflicted injury. Reducing localized tissue deformation is particularly important in diabetes, because low deformation levels are needed to protect the vasculature in a situation where perfusion often already is compromised.^42,43   

Limitations

Computational FE modeling is a powerful tool in PU research but it is not without limitations that originate from the assumptions and omissions made. First, the mechanical properties of the tissues are taken from animal studies. Furthermore, skin and fat tissues are considered hyperelastic. The Achilles tendon and the dressing materials are considered linear elastic; hence, any transient biomechanical viscoelastic phenomena are omitted in the modeling. 

Additionally, the reference model variant is based on anatomical data of a single young healthy subject, which does not necessarily represent all possible heel structures in terms of dimensions, sites, neutral external rotation, and the like. Moreover, the mechanical properties of healthy and diabetic soft tissues are considered homogeneous, although the alterations in tissue stiffness properties associated with diabetes are hardly homogeneous. Local stiffening of connective tissues is occurring as mechanical lesions, which exert greater localized tissue stresses as well as greater strains in the softer, adjacent regions of the affected tissues, and which then act to increase the risk of local tissue damage. 

Conclusion

In this study, the differences between models of a bare heel and models covered with the modeled dressing were considerably different in soft tissue exposures to internal tissue loads, where loads in presence of the dressing were lower. This suggests the dressings provide a cushioning effect to the soft tissues of the heel, as well as that they temper deformations from the tissues by deforming internally themselves in shear mode, hence consistently lowering exposure to hazardous levels of strains and stresses in the simulations in a variety of foot postures and tissue conditions including the case of diabetic tissue conditions. Increasing plantar flexion angles of the resting foot was found to result in safer mechanical states (lower tissue strain and stress exposures) for subcutaneous fat, but more plantar flexion also could worsen the loading state in skin if offloading the heels is not performed in a timely manner. However, the use of the dressing protected skin tissues by lowering the effective and shear stresses in skin for these plantar flexed positions compared to a bare heel state. It is still recommended to offload (ie, temporarily elevate) the heels immediately after elevation of the head of the bed, even if the dressings are used to protect the heels. This is in order to minimize shear loads in the soft tissues of the heels (and buttocks), which are formed as a consequence of elevating the head of the bed or other repositioning maneuvers, as the body tends to slide down in the bed, due to gravity.⁴⁰ The results of this study suggest repositioning the heels immediately after elevating the head of the bed to mitigate the effects of gravity and then repeating this repositioning from time to time afterwards may be an important measure to reduce the risk of PU development. Randomized controlled clinical studies to examine the efficacy of dressings for the prevention of heel PUs are warranted. 

References 

1. Salcido R. Editorial: What is the purple heel? Adv Skin Wound Care. 2006;19(11):3-15. 

2. Fowler E, Scott-Williams S, McGuire JB. Practice recommendations for preventing heel pressure ulcers. Ostomy Wound Manage. 2008;54(10):42–57.

3. 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.

4. Black J. Preventing pressure ulcers occurring on the heel. Wounds Int. 2012;3(3):1–4.

5. Santamaria N, Liu W, Gerdtz M, et al. The cost-benefit of using soft silicone multilayered foam dressings to prevent sacral and heel pressure ulcers in trauma and critically ill patients: a within-trial analysis of the Border Trial. Int Wound J. 2015;12(3):344–350.

6. Gefen A. The biomechanics of heel ulcers. J Tissue Viabil. 2010;19(4):124-131.

7. Butcher M, Thompson G. Can the use of dressing materials actually prevent pressure ulcers: presenting the evidence. Wounds UK. 2010;6(1):119–125.

8. Gefen A. Plantar soft tissue loading under the medial metatarsals in the standing diabetic foot. Med Eng Phys. 2003;25(6):491–499.

9. Bader DL. Editorial. J Tissue Viability. 2013;22(2):23–24.

10. Levy A, Kopplin K, Gefen A. Simulations of skin and subcutaneous tissue loading in the buttocks while regaining weight-bearing after a push-up in wheelchair users. J Mech Behav Biomed Mater. 2013;28:436-447; doi: doi: 10.1016/j.jmbbm.2013.04.015.

11. Levy A, Kopplin K, Gefen A. An air-cell-based cushion for pressure ulcer protection remarkably reduces tissue stresses in the seated buttocks with respect to foams: Finite element studies. J Tissue Viabil. 2014;23(1):13–23.

12. Sopher R, Nixon J, McGinnis E, Gefen A. The influence of foot posture, support stiffness, heel pad loading and tissue mechanical properties on biomechanical factors associated with a risk of heel ulceration. J Mech Behav Biomed Mater. 2011;4(4):572–582.

13. Sopher R, Nixon J, Gorecki C, Gefen A. Exposure to internal muscle tissue loads under the ischial tuberosities during sitting is elevated at abnormally high or low body mass indices. J Biomech. 2010;43(2):280–286.

14. Pai S, Ledoux WR. The shear mechanical properties of diabetic and non-diabetic plantar soft tissue. J Biomech. 2012;45(2):364–370.

15. Andreassen TT, Seyer-Hansen K, Oxlund HB. Biomechanical changes in connective tissues induced by experimental diabetes. Acta Endocrinol. 1981;98(3):432–436.

16. Goodfield MJD, Millard LG. The skin in diabetes mellitus. Diabetologia. 1988;31(8):567–575.

17. Connizzo BK, Bhatt PR, Liechty KW, Soslowsky LJ. Diabetes alters mechanical properties and collagen fiber re-alignment in multiple mouse tendons. Ann Biomed Eng. 2014;42(9):1880–1888.

18. European Pressure Ulcer Advisory Panel (EPUAP), National Pressure Ulcer Advisory Panel (NPUAP) and the Pan-Pacific Alliance (PPA) International Guidelines, 2014. Aetiology. Available at: www.epuap.org/guidelines. Accessed March 5, 2016. 

19. Dealey C, Brindle CT, Black J, Alves P, Santamaria N, Call E, Clark M. Challenges in pressure ulcer prevention. Int Wound J. 2015;12(3):309–312. 

20. Duncan KD. Preventing pressure ulcers: the goal is zero. Jt Comm J Qual Patient Saf. 2007;33(10):605–610.

21. Clark M, Black J, Alves P, et al. Systematic review of the use of prophylactic dressings in the prevention of pressure ulcers. Int Wound J. 2014;11(5):460–471.

22. Butcher M, Thompson G. Dressings can prevent pressure ulcers: fact or fallacy? The problem of pressure ulcer prevention. Wounds UK. 2009;5(4):80–93.

23. Forni C, Loro L, Tremosini M, et al. Use of polyurethane foam inside plaster casts to prevent the onset of heel sores in the population at risk. A controlled clinical study. J Clin Nurs. 2011;20(5-6):675–680.

24. Santamaria N, Gerdtz M, Sage S, et al. A randomized controlled trial of the effectiveness of soft silicone foam multi-layer dressings in the prevention of sacral and heel pressure ulcers in trauma and critically ill patients: the border trial. Int Wound J. 2015;12(3):302–308.

25. Ohura T, Takahashi M, Ohura N Jr. Influence of external forces (pressure and shear force) on superficial layer and subcutis of porcine skin and effects of dressing materials: are dressing materials beneficial for reducing pressure and shear force in tissues? Wound Repair Regen. 2008;16(1):102–107.

26. Nakagami G, Sanada H, Konya C, Kitagawa A, Tadaka E, Matsuyama Y. Evaluation of a new pressure ulcer preventive dressing containing ceramide 2 with low frictional outer layer. J Adv Nurs. 2007;59(5):520–529.

27. Levy A, Frank MB, Gefen A. The biomechanical efficacy of dressings in preventing heel ulcers. J Tissue Viability. 2015;24(1):1–11.

28. Singer B, Dunne L, Singer KP, Allison G. Evaluation of triceps surae muscle length and resistance to passive lengthening in patients with acquired brain injury. Clin Biomech. 2002;17(2);152–161.

29. Fowler E, Scott-Williams S, McGuire JB. Practice recommendations for preventing heel pressure ulcers. Ostomy Wound Manage. 2008;54(10):42–57. 

30. Simpleware^® Ltd. ScanIP, +FE, +NURBS and +CAD Reference Guide ver. 5.1, 2012. Available at: www.simpleware.com/software/. Accessed March 5, 2016.

31. Tenenbaum S, Shabshin N, Levy A, Herman A, Gefen A. The effects of foot posture and heel padding devices on soft tissue deformations under the heel in a supine position: MRI studies. J Rehabil Res Dev. 2013;50(8):1149–1156.

32. Maas SA, Ellis BJ, Ateshian GA, Weiss JA. FEBio: Finite elements for biomechanics. J Biomech Eng. 2012;134(1):5–11.

33. Sopher R, Nixon J, Gorecki C, Gefen A. Exposure to internal muscle tissue loads under the ischial tuberosities during sitting is elevated at abnormally high or low body mass indices. J Biomech. 2010;43(2):280–286. 

34. Kuo PL, Li PC, Li ML. Elastic properties of tendon measured by two different approaches. Ultrasound Med Biol. 2001;27(9):1275–1284.

35. FEBio: Finite element for biomechanics, Theory manual ver. 1.5, 2012. http://mrl.sci.utah.edu/software/febio. Accessed March 5, 2016. 

36. Linder-Ganz E, Shabahin N, Itzchak Y, Gefen A. Assessment of mechanical conditions in sub-dermal tissues during sitting: a combined experimental-MRI and finite element approach. J Biomech. 2007;40(7):1443–1454.

37. Shabshin N, Zoizner G, Herman A, Ougortsin V, Gefen A. Use of weight-bearing MRI for evaluating wheelchair cushions based on internal soft-tissue deformations under ischial tuberosities. J Rehabil Res Dev. 2010;47(1):31–42.

38. Call E, Pedersen J, Bill B, et al. Enhancing pressure ulcer prevention using wound dressings: what are the modes of action? Int Wound J. 2015;12(4):408–413.

39. Zhang M, Mak AF. In vivo friction properties of human skin. Prosthet Orthot Int. 1999;23(2):135–141.

40. Shaked E, Gefen A. Modeling the effects of moisture-related skin-support friction on the risk for superficial pressure ulcers during patient repositioning in bed. Front Bioeng Biotechnol. 2013;1(9):1–7. 

41. Gefen A, Haberman E. Viscoelastic properties of ovine adipose tissue covering the gluteus muscles. J Biomech Eng. 2007;129(6):924–930.

42. Laing P. The development and complications of diabetic foot ulcers. Am J Surg. 1998;176(2A suppl):11S–19S. 

43. Sumpio BE, Lee T, Blume PA. Vascular evaluation and arterial reconstruction of the diabetic foot. Clin Podiatr Med Surg. 2003;20(4):689–708. 

Potential Conflicts of Interest: Dr. Gefen is Chair of the Scientific Advisory Board of Mölnlycke Health Care, Gothenburg, Sweden and is funded by Mölnlycke Health Care for investigating the effects of dressing materials and designs on soft tissues during weight-bearing. 

Ms. Levy is a doctoral student; and Dr. Gefen is a Professor in Biomedical Engineering, Department of Biomedical Engineering, Faculty of Engineering, Tel Aviv University, Tel Aviv, Israel. Please address correspondence to: Amit Gefen, PhD, Tel Aviv University, Biomedical Engineering, Ramat Aviv, Tel Aviv 6997801 Israel; email: gefen@eng.tau.ac.il.

Abstract

Diseases or anomalies of the genitourinary or gastrointestinal tract often require removal of organs and creation of an artificial opening (stoma) to allow for elimination of urine or stool. Preoperative stoma site marking can affect quality of life (QoL). A descriptive study was conducted to assess the relationship between QoL and preoperative stoma site marking in adults with a permanent ostomy.

Using convenience sampling methods, 230 eligible participants attending a United Ostomy Association of America conference were invited to complete a survey of demographics regarding age, gender, time since surgeries, and ostomy type and the City of Hope National Medical Center Quality of Life Ostomy Questionnaire. The latter contains 2 sections of 30 and 43 items each that address life impact and quality of life, respectively. The researcher explained the study and provided a study packet to volunteers who were interested in participating. Volunteers were to complete the surveys over a 4-day period while at the conference; the investigator collected all study materials. Inclusion criteria stipulated study participants must be English writing/reading persons at least 18 years of age with a colostomy, ileostomy, or urostomy. All descriptive statistics (means, standard deviation, frequency, and percents) used to describe demographic and surgical history and quantitative data (logistic regression, cross-tabulation, Pearson product moment correlations, and analysis of covariance) used to determine relationships among factors were entered and analyzed using a computer software program. Of the 140 participants who met inclusion criteria and provided data, the majority (85, 60.7%) had their stoma site marked by a wound, ostomy, continence (WOC) nurse. WOC nurse marking was more likely in recent years, and WOC nurse marking was 1.03 times more likely for each year since stoma surgery (M = 13.44, SD = 13.48). Mean QoL was 7.56 (SD = 1.59, range 3.84–10.00) and was positively correlated with age (r [137] = 0.27, P = 0.001), years since first surgery (r (138) = 0.25, P = 0.003), and years since most recent surgery (r [137] =0.28, P = 0.001). The total number of surgeries was unrelated to QoL. More than 75% of the participants received preoperative marking, with a significant difference in QoL for persons marked by a surgeon (M = 7.71, SE = 0.16) or a WOC nurse (M = 8.82, SE = 0.37) versus another professional (M = 4.83, SE = 1.05) (F [3.118] = 3.44, P = 0.19). The increasing prevalence of preoperative stoma site marking by a WOC nurse over time serves as a benchmark for this centerpiece of WOC nursing practice. The findings confirm the need for stoma site marking and validate the impact of stoma site marking by the WOC nurse. 

Despite advances in medical treatment of urothelial and colorectal cancers, inflammatory bowel disease, and diverticular disease, many ostomy surgeries are still performed in the United States each year.¹ Creation of an ostomy (stoma) influences urine or fecal elimination and obliges patients to adjust to a new way of life.² Disease-specific, quality-of-life (QoL) investigations have been conducted, but research linking outcomes for patients who receive preoperative stoma site marking by a wound, ostomy, continence (WOC) nurse or another clinician with specialized training in the principles of ostomy management is sparse. Additional research is needed to provide a base of evidence for the relationships between QoL, preoperative stoma site marking, and long-term adjustment.³

Background

Exact numbers of individuals living with a permanent stoma, or ostomy, are difficult to ascertain for a variety of reasons, including the way diseases are coded in the United States (US). Cooke¹ provided a range of estimates of individuals currently living with an ostomy (650,000 to 730,000) and further estimated that more than 120,000 ostomy surgeries are performed each year. It is believed that more than 700,000 Americans, ranging from infants to senior citizens, have had fecal or urinary ostomy surgery.⁴

In 2004, the International Ostomy Association (IOA) House of Delegates⁵ issued the “Charter of Ostomate’s Rights” for individuals with an ostomy. According to this document, individuals who undergo ostomy surgery should receive preoperative counseling and be provided with facts about living with a stoma. The individual also should have a well-constructed stoma placed at an appropriate site and receive medical support, ostomy nursing care, and psychological support during the preoperative and postoperative phases, both in the hospital and in the community.

Historically, WOC nurses have advocated for preparing patients for ostomy surgery by performing preoperative stoma site marking and providing preoperative education.³ Recently, the American Society of Colon and Rectal Surgeons, the Wound, Ostomy and Continence Nurses Society, and the American Urological Association issued joint statements advocating a preoperative visit before ostomy surgery by a WOC nurse or another qualified, experienced, educated, and competent clinician.^6,7 The preoperative visit should include assessment and education for both the individual scheduled for ostomy surgery and his/her significant others. Beginning to learn about ostomy care and ostomy appliances before surgery rather than during the immediate postoperative period is preferred. In addition to teaching about the ostomy surgery itself, selecting a site for the stoma should be a priority and should be performed during the preoperative visit.⁸ 

Management guidelines^6-8 state preoperative stoma site marking should be performed after a careful assessment of the abdomen in lying, sitting, and standing positions and should avoid folds and creases; placing a stoma in a fold, near a crease, or in a location that is not visible to the individual predisposes that person to postoperative problems that include pouch leakage, skin irritation, pain, clothing concerns, and the inability to see the stoma and be independent in self-care, issues that may lead to excessive supply use, the need for expensive customized ostomy pouches, and emotional and psychological distress.^8-11 

Surveys^12,13 of ostomates found preoperative stoma site marking can impact QoL and long-term adjustment. Person et al¹³ conducted a comparative, descriptive study to investigate the impact of preoperative stoma site marking on QoL, independence, and complication rates using a structured, validated stoma QoL questionnaire.¹⁴ Of the 105 participants (60 men and 45 women) with 60 (57%) permanent and 45 (43%) temporary stomas, 52 (49.5%) received preoperative stoma site marking and their QoL was significantly better than that of patients who did not receive preoperative stoma site marking (P<0.05), regardless of stoma type. The authors concluded preoperative stoma site marking is crucial for improving QoL, promoting independence, and reducing postoperative complications. 

Haugen et al¹² conducted a descriptive study and researched perioperative factors associated with adjustment over time in a sample of individuals with incontinent stomas in the Midwestern US. An incontinent stoma leaves the individual without the ability to control and evacuate feces, flatus, or urine at times and places considered socially acceptable.⁸ The researchers mailed a survey packet including The Ostomy Adjustment Scale¹⁵ (OAS) and a survey for demographics to 200 eligible participants; the response rate was 73% (N = 146). Using a stepwise, multivariate regression analysis of the association of perioperative factors with the OAS, the authors found certain perioperative factors to be associated with more positive ostomy adjustment, including preoperative education by a WOC nurse that was “helpful,” ostomy creation by a colon and rectal surgeon or a urology surgeon, and ongoing/recurrent illness. Preoperative education by the ostomy nurse was associated with a statistically significant improved adjustment (P = 0.04).

In a comparative, descriptive study, Marquis et al¹⁶ investigated the effect of ostomy surgery on health-related QoL using the Stoma Quality of Life Index (SQLI). The self-administered questionnaire was completed immediately after surgery and then again at 3, 6, 9, and 12 months; 4,739 patients with stomas and 618 stoma care nurses from 16 European countries responded. The Montreux Study¹⁶ included analysis of 11,097 questionnaires in 12 languages. All patients had a fairly consistent SQLI immediately after surgery. QoL was found to improve over time, but time was not the only factor to influence QoL — patient satisfaction with the care received, confidence in changing the appliance, and the patient’s relationship with the ostomy nurse all affected QoL. Patients who reported a WOC nurse took a genuine interest in them had higher QoL index scores. The authors suggested these findings support the belief that a WOC nurse exerts a positive influence on adaptation and QoL. The authors concluded by advocating for increased access to specialist care for the first 3 to 6 postoperative months.

Although preoperative stoma site marking is receiving increased attention in the literature and it is generally agreed that preoperative stoma site marking and teaching before ostomy surgery are beneficial,^17,18 documenting who provided preoperative stoma site marking (eg, a WOC nurse or another clinician with specialized training in principles of ostomy management) is important.³ Additional research is needed to provide a base of evidence for the relationships between QoL, preoperative stoma site marking, and long-term adjustment.³

The purpose of this comparative, descriptive study was to assess the relationship between QoL and preoperative stoma site marking in a sample of adults with a permanent ostomy.

Methods and Procedures

Institutional review board approval was obtained from Teachers College, Columbia University, New York, NY after the proposal for dissertation research was approved. 

The investigator attended the 2009 United Ostomy Association of America (UOAA) Second National Conference in New Orleans, LA for the sole purpose of soliciting volunteers for study participation using convenience sampling methods. At the beginning of the conference, the coordinator of the UOAA informed attendees about the research and invited them to participate. A room was available for participants to complete the study any time during the 4-day conference. Interested individuals were provided a cover letter informing them participation was voluntary and anonymous, they had the right to withdraw at any time, and they could omit questions. Before surveys and consent forms were distributed, a description of the research study and participants rights was provided to each attendee by the program coordinator. 

Persons who volunteered to participate were given a consent form and survey packet. The self-report surveys were stapled into one packet and were randomly ordered.  The order was rotated to establish different sets, which then were labeled and assigned an identification number. A survey packet was handed to each voluntary participant with appropriate instructions.  

Each participant received a blue or black pen, a large brown envelope in which to place their completed survey, and a survey packet containing the City of Hope-Quality of Life-Ostomy Questionnaire¹⁹ (COH-QOL-OQ) and a Demographic Data Survey. The consents and survey packets took approximately 30 minutes for the respondent to complete. The investigator stayed available to answer any questions and collected all completed consents separately from the survey packets. Respondents placed the survey instruments in a sealed brown envelope, which the investigator collected before leaving the conference venue.  

Criteria for inclusion were: 1) age 18 years or older; 2) having a permanent colostomy, ileostomy, or urostomy; and 3) being able to read and write English.

Instruments. COH-QOL-OQ¹⁹ is a comprehensive, multidimensional, self-report instrument designed to assess QoL for individuals with intestinal ostomies. The instrument contains 2 quantitative sections: The Lifestyle Impact and the Quality of Life Impact sections. Both quantitative sections of the instrument were utilized for data collection; reliability and validity have been demonstrated on these sections.²⁰ 

Lifestyle impact. The Lifestyle Impact Section consists of 31 descriptive Yes/No items organized into the following themes: 1) work-related, 2) health insurance, 3) sexual activity, 4) psychological support/concerns, 5) clothing, 6) diet, 7) time since surgery and adjustment (how long it took to be comfortable with ostomy care, diet, and how long it took your appetite to return), and 8) food groups. Each item answered Yes = 1 point and each No response = 0. 

QoL impact. The QOL Impact Section is divided into 4 domains with 43 items as conceptualized in the COH-QOL Model (see Figure 1): physical well-being (items 1 to 11), psychological well-being (items 12 to 24), social concerns (items 26 to 36), and spiritual well-being (items 37 to 43). Each item is scored using a linear analogue scale in terms of problem severity, rated from 0 to 10.²⁰ For example, respondents can rate physical strength between 0 (no problem) and 10 (severe problem). A number of items are reverse scored to protect against response bias, including items 1–12, 15, 18, 19, 22, 30, 32–34, and 37. A mean QoL score was obtained by adding all scaled times and dividing by 43. Scores range from 0 to 10, with 10 being the best quality of life.  

Grant et al²⁰ reported the psychometric analysis of the revised COH QOL OQ confirmed a 4-dimensional model and established initial reliability and validity; the authors also confirmed the scale may be utilized to describe adjustment to colostomy, ileostomy, or urostomy for adults.²⁰

Demographic survey. The demographic data survey included information such as gender, year of birth, height, weight, race, and education, as well as illness/reason for surgery, years since first surgery, number of surgeries, ostomy type (colostomy, ileostomy or urostomy), and who performed preoperative stoma site marking.

Data analysis. Data were entered into the Statistical Package for Social Sciences, version 17 (SPSS, Chicago IL) and analyzed. Study variables included participant demographics, QoL scores, illness or reason for surgery, years since first surgery, number of surgeries, ostomy type (colostomy, ileostomy or urostomy), preoperative stoma site marking, and length of time to 3 adjustment points (ie, how long before they were comfortable with their ostomy, how long before they were comfortable with their diet, and how long before appetite returned).

Descriptive statistics (means, SDs, frequencies, percentages) were used to describe the demographic makeup of the sample as well as participant surgical history. Logistic regression analysis was used to determine the relationship between being marked by a WOC nurse and year of first stoma creation. Cross-tabulation analyses were conducted to determine the relationship between being marked by a WOC nurse and adjustment items from the Lifestyle Impact section. Pearson product moment correlations were used to assess the relationship between COH-QOL-OQ score and background variables of age, years since stoma was created, and years since most recent surgery. These correlations led to selection of covariates.  

Analyses of covariance (ANCOVA) with Bonferroni post-hoc tests were used to determine the relationships between QoL and preoperative stoma site marking. These outcomes were compared among 4 groups: respondents who received no preoperative stoma site marking, persons who received preoperative stoma site marking by a WOC nurse, persons who received preoperative stoma site marking by a surgeon, and persons who received preoperative stoma site marking by someone other than an ostomy nurse or surgeon. Covariates of age, number of years since first surgery, and number of years since last surgery were used in all QoL analyses.  

Results

Of the 230 packets distributed, 149 were returned (response rate of 64.8%). One-hundred, forty (140) respondents met inclusion criteria, had complete data on 1 or more independent and dependent variables, and had provided sufficient demographic data to be part of the proposed sample (age, ostomy status, and preoperative stoma site marking). One participant did not complete a significant part of the QoL section in the COH-QOL-OQ and was not included in the data analysis. In order to maximize the sample size, all 140 cases with completed demographic data questionnaires were analyzed. Demographic characteristics of the sample are summarized in Table 1. 

The vast majority of the respondents in this survey were Caucasian (134; 95.7%). The mean ages for female and male respondents were 59.06 ± 13.62 and 65.02 ± 13.06, respectively. The majority of the respondents (69.3%) reported being married before surgery; of those who had a change in marital status after surgery, 27 (84.37%) said the change was unrelated to the surgery. More than half of the respondents (61.4%) had an ileostomy and were more likely to be women; those with a colostomy were more likely to be employed full time; and those with an ileostomy were more likely to work part time or be unemployed (see Table 1). 

Slightly more than half of the sample (87, 63.0%) reported 1 surgery, and more than one third of the sample (51, 37.0%) reported multiple surgeries. The respondents reported a range of 0–62 years (M = 13.44, SD = 13.48) since their first surgery; the number of surgeries ranged between 1 and 32 (M = 2.12, SD = 3.50); and years since most recent surgery was between 0 and 58 years (M = 10.15, SD = 11.40). The majority of respondents (99, 70.7%) reported their surgery was planned; close to 75% of the respondents reported the stoma site was marked preoperatively, and most received preoperative marking by an ostomy nurse (see Table 2). 

Using year of first surgery to predict whether a WOC nurse marked the stoma site, logistic regression analysis revealed that WOC nurse marking was more likely in more recent years, (B = .031, Wald = 4.06, P = 0.04, OR = 1.032 (95% CI: 1.001, 1.064), with WOC nurse marking 1.03 times more likely for each successive year. For example, a participant having surgery in 2016 was 1.32 times more likely to be marked by a WOC nurse than someone having surgery in 2006 (10 years ago) and 1.64 times more likely than someone having surgery in 1996 (20 years ago).

Lifestyle impact: length of time to adjustment points. Cross-tabulation analyses showed a significant association between being marked preoperatively by a WOC nurse and length of time until appetite returned (Somer’s d = -0.135, T = -2.32, P  = 0.02) and length of time until patients were comfortable with their diet (Somer’s d = -0.244, T = -2.706, P = 0.007), with WOC nurse-marked patients showing earlier return of appetite and comfort with diet than patients who were not marked by a WOC nurse. For example, in terms of comfort with their diet, those marked by a WOC nurse were more likely to report feeling “immediately” comfortable (8.6% compared to 0.0% for the WOC nurse-marked and non-marked patients, respectively) and less likely to report “never feeling comfortable” (9.9% compared to 20.0% for the WOC nurse-marked and non-marked, respectively). More WOC nurse-marked participants reported their appetite returned “immediately” (10.0% compared to 0.0% for non-marked), and fewer reported it took “years” (1.3% compared to 7.3%, WOC nurse-marked versus non-marked, respectively). No association was noted between being marked by a WOC nurse and how long it took to adjust to daily care (Somer’s d = -0.126, t = -1.521, P  = 0.13).

Quality-of-life impact. Mean COH-QOL-OQ score for the total sample was 7.56 (SD 1.59, range of 3.84–10.00). QoL total was positively correlated with age (r [137] = 0.27, P  = 0.001), years since first surgery (r [138] = 0.25, P = 0.003), and years since most recent surgery (r [137] = 0.28, P = 0.001). These correlations indicate that as age, time since first surgery, and time since most recent surgery increase, scores on the QoL measure also increase. Although years since first and last surgery were highly intercorrelated, only years since first surgery and age were used as covariates in QoL analyses. Total number of surgeries was unrelated to QoL total scores (r [137] = -0.09, P = 0.29). 

Relationships between QoL and preoperative stoma site marking. The 4 groups of individuals assessed included persons who received no preoperative stoma site marking (24, 19.4%) and persons who received preoperative stoma site marking by an ostomy nurse (83, 66.9%), surgeon (15, 12.6%), or “other” person (2, 1.6%). ANCOVA analyses, controlling for age and number of years since first surgery, revealed significant differences in QoL based on who marked the site (F [3, 118] = 3.44, P = 0.019). Bonferroni adjusted post-hoc tests showed the WOC nurse-marked group (M = 7.705, SE = 0.160) and the surgeon-marked group (M = 8.185, SE = 0.374) had a higher QoL than the “other” group (M = 4.831, SE = 1.049). The surgeon-marked and WOC nurse-marked groups did not differ, and patients whose stoma was marked by a WOC nurse or surgeon had the highest QoL scores.

Discussion 

The results of this descriptive study support the premise that preoperative stoma site marking is beneficial and should be done by someone qualified to perform the procedure.^6,7,10,11,21 The significant differences in QoL based on who marked the site demonstrated that the WOC nurse-marked group and the surgeon-marked group had a higher QoL than the “other” group; this evidence further supports the need for preoperative stoma site marking.^6,7   

This result is consistent with findings by Macdonald et al,²¹ who investigated the ability of surgeons to chose a stoma site against the gold standard (the ability of WOC nurses to chose a stoma site). The researchers found surgeons with a colorectal subspecialty chose sites consistent with WOC specialty nurses. In addition, persons who were not preoperatively marked or were marked by someone other than the surgeon or the WOC nurse had lower QoL scores; the authors concluded general surgeons may not be trained in stoma site marking and therefore results may be inconsistent. Stoma site marking is a skill often taught in the education, practice, and training of urologists, colorectal surgeons, and WOC nurses (ie, specialists).^10,11 

QoL scores in this investigation are consistent with the range of QoL scores reported by others using the COH-QOL-OQ. Anaraki et al²² reported a mean score of 7.48; Gemmill et al²³ reported a mean score of 7.7; and Grant et al²⁰ reported a mean score of 7.65. In general, overall QoL scores have been reported to be lower for all patients with ostomies, but comparing populations that are slightly different must be done cautiously.^24,25 The positive correlations with age, years since first surgery, and years since last surgery also are consistent with findings of others who reported QoL improves over time.¹⁶ 

Although many have investigated the impact of an ostomy on QoL, only a few have specifically examined the impact of preoperative stoma site marking on QoL. The results of this study provide a glimpse into the prevalence of preoperative stoma site marking by a WOC nurse and may be the first to document that WOC preoperative stoma site marking has increased over time. Although studies have addressed preoperative stoma site marking,¹³ preoperative education by a WOC nurse,¹² and preoperative education and stoma site marking,¹⁷ no data are available to use as a benchmark to describe the prevalence of preoperative stoma site marking by WOC nurses. 

The significant association between being marked by a WOC nurse preoperatively, length of time until patient appetite returned, and length of time until patients were comfortable with diet was an interesting and unexpected finding. Krouse et al²⁶ investigated QoL for patients with cancer and patients without cancer with a colostomy and found patients without cancer reported diet-related issues were more problematic and required dietary adjustments, including avoiding certain foods such as dairy products, vegetables, and fruits. Although many participants in both these study groups altered their diet, the authors suggested the difference might be associated with dietary changes necessary for irritable bowel disease or diverticulosis or that more patients without cancer might avoid foods such as dairy products, fruits, and vegetables.  

In the current study, more than 75% of the respondents had either Crohn’s disease or ulcerative colitis and more than 50% had an ileostomy; thus, it is possible the surgery itself led to the return of their appetite and comfort with their diet.  

Although the majority of individuals in this study were marked by a WOC nurse, preoperative education was not assessed. Haugen et al¹² reported postoperative adjustment improved with preoperative education provided by a WOC nurse.  In general, a preoperative stoma site marking session by a WOC nurse may allow time to provide education, but it is difficult to gauge the education provided and assess its impact on QoL.²⁷ Furthermore, many patients continue to require ongoing education and support long after surgery.^{9,10,12,13,16,28} 

The majority of the participants in this study belonged to an ostomy support group or another type of support group and may have had the opportunity to talk with someone else who was going to have or had an ostomy. The effects of these factors are elusive and deserve additional exploration.

Recommendations for further research include designing quantitative and qualitative studies to investigate ethnically diverse participants who are unable to travel or attend a national conference to identify variables that impact QoL. Further investigation in the form of a qualitative study might provide an additional avenue for the “voice” of the individuals with an ostomy to be heard. The voice of experience of living with an ostomy has great potential for teaching health care professionals about the individual needs for this patient population. Further investigation with regard to the elements of the preoperative visit for stoma site marking and the impact upon QoL should be undertaken. The return of appetite and comfort with diet should be further investigated to elucidate the information necessary for teaching and counseling patients with an ostomy.

Limitations

Several limitations of this investigation should be considered when interpreting the results. First, the sample was limited to adults who were motivated and physically and financially able to attend the conference. A potential for bias in the results exists because most participants were Caucasian college graduates. Results of this investigation can only be generalized to individuals between the ages of 23 and 89 years old with a permanent ostomy who were represented in this sample.  

Next, the instruments in this investigation were self-report surveys; recall bias may be a factor for participants because they had ostomy surgery an average of more than 13 years before this study. Additionally, when measuring an individual’s QoL, certain items may represent different levels of importance to the respondents. It is also possible the location and nature of the conference may have had an effect with regard to the participants’ state of mind, feelings of well-being, and sense of control.

Lastly, information was not elicited about surgical specialty (ie, general surgeon, colorectal surgeon, or urologist), which is now recommended by the American Society of Colorectal Surgeons, the American Urological Association, and the Wound, Ostomy and Continence Nurses Association.^6,7 

Conclusion

A descriptive study was conducted to explore the relationship between QoL and preoperative stoma site marking for individuals with a permanent ostomy. The findings show living with an ostomy influences QoL. The majority of the study participants received stoma site marking, most were marked by a WOC nurse, and the prevalence of WOC nurse preoperative stoma site marking has increased over time. A significant difference in QoL was dependent on who marked the site; the surgeon-marked group and WOC nurse-marked group had the highest QoL scores when compared to the “other” group.  

The findings confirm the need for stoma site marking and validate the impact of stoma site marking by the WOC nurse. Findings of this investigation add to the current evidence base and provide a foundation for future research. Outcomes related to ostomy nursing interventions such as preoperative stoma site marking provide endless opportunity for additional research-related activities. n

Acknowledgment

The author is grateful for the warm welcome she received while attending the United Ostomy Associations of America Second National Conference in New Orleans, LA, August 5–8, 2009 and the sincere interest shown this project. She thanks each and every individual who willingly and enthusiastically participated in this study and hopes this work helps improve the care provided.

References

1. Cooke C. American ostomy census: Counting surgeries and ostomy patients in the US. Phoenix. 2009;5:28–29,63,67.

2. Slade D. The voice of experience. J Wound Ostomy Continence Nurs. 2000;27(4):201–206.

3. Colwell JC, Gray M. Does preoperative teaching and stoma site marking affect surgical outcomes in patients undergoing ostomy surgery? J Wound Ostomy Continence Nurs. 2007;34(5):492–496. 

4. Guiding Principles For Sustainable Access to Ostomy Services, Technologies and Innovation. Available at: www.wocn.org/news/211992/Guiding-Principles-For-Sustainable-Access-to-Os.... Accessed April 11, 2016. 

5. International Ostomy Association. Charter of Ostomates Rights. Available at: www.ostomy.org/Ostomate_Bill_of_Rights.html. Accessed April 11, 2016.

6. American Society of Colon and Rectal Surgeons Committee Members; Wound, Ostomy, Continence Nurses Society Committee Members. 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. 

7. American Urological Association Committee Members; Wound, Ostomy, Continence Nurses Society Committee Members. Society joint position statement on the value of preoperative stoma marking for patients undergoing creation of an incontinent urostomy. J Wound Ostomy Continence Nurs. 2009;36(3):267–268. 

8. Carmel JE, Goldberg MT. Preoperative and postoperative management. In: Colwell JC, Goldberg MT, Carmel JE (eds). Fecal and Urinary Diversions: Management Principles. St. Louis, MO: Mosby;2004:207–239.

9. Maydick D. Individuals with a permanent ostomy: quality of life and out-of-pocket financial costs for ostomy management. Nurs Economics. 2014;32(4):204–210, 218. 

10. Salvadalena G, Hendren S, McKenna L, et al. WOCN Society and ASCRS position statement on preoperative stoma site marking for patients undergoing colostomy or ileostomy surgery.  J Wound Ostomy Continence Nurs. 2015;42(3):249–252.

11. Salvadalena G, Hendren S, McKenna L, et al. WOCN Society and AUA position statement on preoperative stoma site marking for patients undergoing urostomy surgery. J Wound Ostomy Continence Nurs. 2015;42(3):252–256. 

12. Haugen V, Bliss DZ, Savik K. Perioperative factors that affect long-term adjustment to an ostomy. J Wound Ostomy Continence Nurs. 2006;33(5):525–535.

13. 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.  

14. Prieto L, Thorsen H, Juul K. Development and validation of an quality of life questionnaire for patients with colostomy or ileostomy. Health Qual Life Outcomes. 2005;3(1):62. 

15. Olsbrisch ME. Development and validation of the Ostomy Adjustment Scale.  Rehab Psyc. 1983;28(1):3–13. 

16. Marquis P, Marrel A, Jambon B. Quality of life in patients with stomas: the Montreux study. Ostomy Wound Manage. 2003;49(2):48–55. 

17. Gulbiniene J, Markelis R, Tamelis A, Saladzinskas, Z. The impact of stoma siting and stoma care education on patient’s quality of life. Medicina. 2004;40(11):1045–1053.

18. Karadaq A, Mentes, BB, Uner A, Irkorucu O, Ayaz S, Ozkan S. Impact of stomatherapy on quality of life in patients with permanent colostomies or ileostomies.  Int J Colorectal Dis. 2003;18(3):234–238.  

19. City of Hope Quality of Life-Ostomy Questionnaire. Available at: http://cityofhope.org/prc/pdf/Quality%20of%20Life%20Ostomy.pdf. Accessed April 11, 2016.

20. Grant M, Ferrell B, Dean G, Uman G, Chu D, Krouse R. Revision and psychometric testing of the City of Hope Quality of Life-Ostomy Questionnaire. Qual Life Res. 2004;13(8):1445–1457.

21. Macdonald A, Chung D, Fell S, Pickford I.  An assessment of surgeons’ abilities to site colostomies accurately. Surg JR Coll Surg Edinb Irel. 2003;1(6):347–349.

22. Anaraki F, Vafaie M, Behboo R, Maghsoodi N, Esmaeipour S, Safaee A. Quality of life outcomes in patients living with a stoma. Indian J Pall Care. 2012;18(3):176–180. 

23. Gemmill R, Sun V, Ferrell B, Krouse RS, Grant M. Going with the flow: quality of life outcomes of cancer survivors with urinary diversion. J Wound Ostomy Continence Nurs. 2010;37(1):65–72. 

24. Krouse RS, Grant M, Wendel CS, et al. A mixed-methods evaluation of health-related quality of life for male veterans with and without intestinal stomas. Dis Colon Rectum. 2007;50(12):2054–2067.  

25. Krouse RS, Mohler M, Wendel C, et al. The VA ostomy health-related quality of life study: objectives, methods, and patient sample. Current Med Res Opin. 2006;22(4):781–791.

26. Krouse R, Grant M, Ferrell B, Dean G, Nelson R, Chu D. Quality of life outcomes in 599 cancer and non-cancer patients with colostomies. J Surg Res. 2007;138(1):79–87.

27. Aronovitch SA, Sharp R, Harduar-Morano L. Quality of life for patients living with ostomies: influence of contact with an ostomy nurse. J Wound Ostomy Continence Nurs. 2010;37(6):65–72.

28. Richbourg L, Thorpe JM, Rapp CG. Difficulties experienced by the ostomate after hospital discharge. J Wound Ostomy Continence Nurs. 2007;34(1):70–79.  

Potential Conflicts of Interest: none disclosed 

Dr. Maydick is an Assistant Professor of Nursing, Long Island University, Harriet Rothkopf Heilbrunn School of Nursing, Long Island, NY. Please address correspondence to: Diane Maydick, EdD, RN, ACNS-BC, CWOCN, 54 Valencia Avenue, Staten Island, NY 10301; email: dmaydick@gmail.com.

Abstract

Diverting stomas are employed for various clinical indications and easier to revert than end stomas. General, plastic, and colorectal surgeons continue to debate whether a diverting loop stoma adequately diverts stool, preventing spillage into the distal limb, which does not receive stool. A retrospective, descriptive study was conducted involving all patients who underwent loop ostomy surgery (colostomy or ileostomy) — defined by current procedural terminology (CPT) codes 44187, 44188, 44153, and 44155–44158 — between April 1, 2002 and October 12, 2010.

The purpose of the study was to determine if a diverting loop stoma is completely diverting with no efflux into the distal limb by examining the rate of distal limb contamination. Two surgeons identified patients at the University of Virginia who had loop ostomy surgery and subsequently underwent computed tomography (CT) scan with oral contrast for clinical suspicion of abnormal pathology. A radiologist reviewed these images to evaluate the presence or absence of oral contrast in the ostomy distal limb. Distal progression of oral contrast was deemed adequate if oral contrast was visualized within the ostomy bag or if contrast was intraluminal distal to the loop ostomy. The loop ostomy was considered diverting if oral contrast was only visualized in the ostomy bag with no oral contrast distally. Of the 202 eligible patients, 26 (13%) underwent 41 postoperative CT scans of the abdomen/pelvis. Four (4) were excluded due to inadequate exam or confounding contrast (rectal contrast, contrast retention from preoperative scan). Of the remaining 22 patients with 35 CT scans (median age 54 [range 26–82] years, 10 men, 18 Caucasian, 18 having elective surgery), no patient (0%) had evidence of distal contrast. In this and other studies, loop stomas were found to provide adequate diversion without spillage into the nonfunctional limb for the vast majority of patients and should strongly be considered as the procedure of choice for temporary diversion.

Colon and rectal surgeons commonly create a protective loop ostomy in order to decrease rates of clinically significant anastomotic leaks in colorectal procedures. Improved techniques in colorectal surgery allow for low (below the anterior peritoneal reflection) and ultra low (1.5 cm–2 cm above the dentate line) anastomoses in lieu of abdominoperineal resections.¹ A low anastomosis allows patients to preserve bowel function without the need for a permanent ostomy. Unfortunately, these low anastomoses come with significant leak rates. Numerous descriptive studies and a randomized, controlled prospective study have demonstrated improved outcomes with a temporary defunctioning stoma when performing a low anastomosis, including lower rates of leakage with diverting ostomies in addition to lower rates of re-intervention with loop stomas.^2-6

Initially popularized to avoid ischemia associated with ileal conduits and urostomies due to mesenteric undercutting,⁷ loop ostomies have increased in prevalence in colorectal procedures over the past 25 years for anastomotic protection.^8,9 A literature review demonstrated fecal diversion decreased the risk of anastomotic leaks by diverting stool proximally; furthermore, diversion reduced the need for urgent re-operation when a leak occurs.^9,10 

Loop ostomies are technically easy to create and are described in several retrospective reviews. Traditionally, the ostomy is sited within the rectus abdominus for loop ostomy formation.^8,9 The mesentery of either the ileum or colon is mobilized and the antimesenteric border is grasped with tissue forceps.⁸ An enterotomy then is created, and the proximal end is anchored with mucocutaneous sutures. An enterotomy that encompasses 4/5 of the circumference will allow the distal bowel to “escape” from the skin.⁹ In addition, loop ostomies also are easy to reverse, especially with the advent of bowel staplers. End ostomies require large laparotomy incisions for reversal, whereas loop ostomies can be reversed directly through the ostomy incision, which should decrease morbidity.^7,11

General, plastic, and colorectal surgeons debate the success of fecal diversion with loop stomas and whether they allow fecal contents to spill into the distal limb. Traditional teaching states loop stomas do not divert as adequately as end ostomies.¹² The colorectal surgery division at the University of Virginia (UVA, Charlottesville, VA) has received referrals for conversion of loop ostomies to end ostomies to prevent sacral wound contamination, which in turn would allow for proper wound healing. To support the hypothesis that all loop ostomies are diverting, a retrospective study was conducted to determine if loop ostomies adequately divert stool without distal limb contamination, as shown via oral contrast and computed tomography (CT) of the abdomen/pelvis. The purpose of this retrospective study was to examine the rate of distal limb contamination following elective loop ostomy surgery.

Materials and Methods

Patient selection. The institutional review board at the UVA Health System approved this retrospective, observational study with a waiver for written informed consent. The general surgery and colorectal databases were queried for all patients undergoing a colorectal procedure between April 1, 2002 and October 12, 2010. Patients were eligible if they underwent ostomy creation and a subsequent CT scan in the study period. Patients undergoing any colorectal procedure between the specified dates had further chart review performed by a surgery resident and attending surgeon to determine the presence or absence of a loop ostomy (ileostomy or colostomy). Patient name, race, gender, medical record number, procedure type, date of operation, elective or emergent operation, current procedural terminology (CPT) code, and reason for surgery were abstracted and recorded in a separate database for all patients. Ostomy reversal was not abstracted, since it was not relevant for the purposes of the current study. Patients undergoing loop colostomy or ileostomy procedures were defined by CPT codes 44187, 44188, 44153, and 44155–44158. 

Information on type and date of CT scan, if any, was collected along with any recent non-oral contrast administration. CT scans were ordered at the discretion of the treating physician based on clinical suspicion for abnormal pathology or for cancer surveillance. Scans were appropriate for inclusion if they occurred after ostomy creation but before stoma reversal. If multiple scans were ordered for a patient, all eligible scans during the study period were included. Chart review was also essential to determine which patients underwent postoperative CT scans of both the abdomen and pelvis with oral contrast (iohexol). A radiologist independently retrieved and reviewed the scans and corroborated the presence or absence of distal contrast. 

This review was performed independently of the clinically indicated image review and was performed for study purposes only. Technically incomplete studies (ie, imaging of only the abdomen or pelvis, cessation of imaging after the scout acquisition and before cross-sectional imaging, or oral contrast not reaching the level of the ostomy) were excluded. Additionally, patients were excluded if they received rectal contrast or oral contrast within 1 week before creation of the loop ostomy. 

Surgical technique. Standard procedure, diverting loop ileostomies or colostomies were created under the supervision of 1 of 8 attending surgeons. One patient had a loop ileostomy created at another institution that was revised by one of the UVA surgeons during a concurrent operation. In general, patients presenting for elective ostomies undergo ostomy site marking by a specified ostomy team before surgery. Bowel preparation with polyethylene glycol for elective patients before colonic surgery was widely practiced during the study period. Emergent ostomies were placed in a location chosen by the attending surgeon. 

A muscle-splitting incision through rectus abdominus muscle and fascia is made at the preferred site. A loop of small or large bowel then is grasped with Babcock forceps and passed through the incision. Bovie electrocautery is used to create a small enterotomy. Typically, loop ileostomies are created using a Brooke technique, whereas loop colostomies are sutured to the skin. A Brooke ileostomy involves suturing a portion of the ileum to the skin so an inside-out portion of ileum serves as the ostomy.¹³ Surgeons at the authors’ institution classically place a supporting rod underneath the ostomy if any tension is noted during creation of the stoma. Stoma appliances then are fitted in the operating room. 

Examination technique. CT scans were performed at the discretion of the physician with a standardized protocol (single-breath hold, spiral-acquisition, 5-mm reconstructed images). Examinations with and without intravenous contrast medium were included. Oral contrast protocol recommends patients receive one oral dose as soon as the CT order is placed; dose 2 is given 30 minutes after completion of the first dose. The third and final dose of oral contrast is administered 15 minutes before transport to CT. Oral contrast dosing was variable given unpredictable patient wait times for an available scanner. A radiologist reviewed the scans in 3 planes on the hospital imaging system (PACS, Carestream Vue PACS, Rochester, NY). Both diagnostic and cancer surveillance scans were used in the study analysis.

Imaging and data analysis. Each CT was examined to determine the most distal extent of oral contrast progression. Distal progression of oral contrast was deemed adequate if oral contrast was visualized within the ostomy bag or if contrast was intraluminal in bowel distal to the loop ostomy. The loop ostomy was considered diverting if oral contrast was visualized only in the ostomy bag with no oral contrast distally. If oral contrast was visualized in the distal bowel, with or without contrast in the ostomy, the ostomy was considered incompletely diverting.

Data recording and analysis. Data were abstracted from retrospective chart review and maintained in a separate Excel database. Because there is no comparison group, no formal statistical analysis was performed. Descriptive summaries are provided for each variable, including overall number of patients and percent of total.

Results

During the study period, the records of 202 patients who underwent a loop colostomy or ileostomy were identified. Of these, 40 underwent a CT exam of the abdomen or pelvis with a total of 77 radiographic studies. Chart review and analysis of the operative reports excluded 1 patient with 2 CT exams who underwent a divided end ostomy. The radiologist reviewed the remaining CT examinations of 39 patients who underwent 75 studies. Of those, 30 studies were excluded due to technically incomplete examinations. An additional 2 patients were excluded for receiving a water-soluble contrast enema and not oral contrast. Lastly, 5 patients with 6 CT scans were excluded for confounding oral contrast (recent preoperative CT with oral contrast and recent rectal contrast). Ultimately, 22 patients (median age 54 [range 26–82] years) with 35 CT studies had adequate examinations for inclusion: 9 patients (41%) had loop colostomies — 7 patients with descending colostomies underwent 11 CT scans (2 patients with ascending colostomies underwent 1 scan each). The remaining 22 scans were from 13 patients (59%) with loop ileostomies (see Table 1). 

The study included an approximately equal number of men and women. The majority of patients were Caucasian (82%), and most stomas were created under elective conditions (82%). Seven (7) patients with a colostomy had a sigmoid colostomy; 2 patients had a right colostomy (see Table 1). 

None (0) of the 22 patients undergoing 35 CT scans of the abdomen/pelvis with oral iohexol contrast administration was identified as having contrast in bowel distal to the level of the loop ostomy, regardless of reason for ostomy formation. 

Discussion

Some colorectal surgeons have received referrals, particularly from plastic surgeons, requesting conversion of a loop to an end ostomy. The referrals frequently come with complaints of anal or rectal leakage, even with a diverting loop stoma. The concern is that the discharge may actually be nondiverted stool, causing contamination of wounds or flaps created in previous procedures. It is known that patients with diverting ostomies, even end stomas, continue to pass mucous discharge, which occurs even in the presence of true fecal diversion.¹⁴ Additionally, the drainage may result from diversion colitis, a term coined by David Glotzer,¹⁵ who first described this phenomenon in 1981 based on a 10-patient sample with inflammatory findings on proctoscopy. A systematic review by Kabir et al¹⁶ of 22 case series, 9 case reports, 2 retrospective, and 2 prospective studies qualitatively demonstrated diversion colitis occurs in colonic segments distal to the diversion and is thought to be a nonspecific inflammation occurring in up to 33% of patients with a diverting ostomy. Diversion colitis can be asymptomatic or can cause symptoms ranging from pelvic/abdominal pain and tenesmus in up to 15% of patients, bloody discharge or mucous discharge in up to 40%, and anorectal pain. 

Few studies have evaluated fecal diversion with loop ostomies. Winslet et al⁸ prospectively evaluated the effectiveness of the defunctioning capacity of the loop stoma by administering radioactive dye orally followed by rectal lavage with a Foley catheter to assess the presence of dye. The authors found a 99% effectiveness of complete diversion in 18 patients. Similarly, in a 10-patient prospective cohort Schofield et al¹⁷ were unable to detect any radiolabeled dye in the distal limb, concluding loop stomas are adequately diverting. Morris et al¹² prospectively assessed diversion through administration of oral barium in 23 patients with loop colostomies followed by mechanical bowel preparation to determine if barium passed to the distal limb; similar to the current study, no patient was found to have barium in the distal portion of bowel.

In this study, CT scans of the abdomen/pelvis were evaluated in 22 patients who had previously undergone diverting stoma and the presence of contrast distal to the ostomy was used as an indicator of distal spillage of stool. The current study demonstrates no patient with either loop ileostomy or loop colostomy had evidence of contrast distal to the anastomosis, regardless of reason for operation. Patients who had distal contrast received oral or rectal contrast shortly before the CT in question and were therefore appropriately excluded from analysis. 

Limitations 

This retrospective, observational study has important limitations. The CT scans excluded for confounding oral contrast may have had contrast in the distal limb from post-ostomy formation iohexal. Although this is a possibility, it seems unlikely because no other patients had distal contrast in the nonfunctional limb. Additionally, the current study included a small sample size of 22 patients, which may limit the ability to identify distal contrast. Furthermore, newer imaging techniques may have greater sensitivity to detect distal contrast or radioactive tracer. The timing between administration of iohexol and initiation of CT imaging is unknown. Lastly, as a single institution, retrospective study, the generalizability to other patient cohorts is limited. 

Conclusion

The results from this and previous research confirm that loop stomas are adequately diverting. Given the ease of reversal, they serve as a preferred method for temporary diversion. n

References 

1. Ludwig KA. Sphincter-sparing resection for rectal cancer. Clin Colon Rectal Surg. 2007;20(3):203–212. 

2. Chude GG, Rayate NV, Patris V, et al. Defunctioning loop ileostomy with low anterior resection for distal rectal cancer: should we make an ileostomy as a routine procedure? A prospective randomized study. Hepatogastroenterology. 2008;55(86-87):1562–1567. 

3. Giuliani D, Willemsen P, Van Elst F, Vanderveken M. A defunctioning stoma in the treatment of lower third rectal carcinoma. Acta Chir Belg. 2006;106(1):40–43. 

4. Matthiessen P, Hallböök O, Rutegård J, Simert G, Sjödahl R. Defunctioning stoma reduces symptomatic anastomotic leakage after low anterior resection of the rectum for cancer: a randomized multicenter trial. Ann Surg. 2007;246(2):207–214. 

5. Marusch F, Koch A, Schmidt U, et al. Value of a protective stoma in low anterior resections for rectal cancer. Dis Colon Rectum. 2002;45(9):1164–1171. 

6. Rondelli F, Reboldi P, Rulli A, et al. Loop ileostomy versus loop colostomy for fecal diversion after colorectal or coloanal anastomosis: a meta-analysis. Int J Colorectal Dis. 2009;24(5):479–488. 

7. Fonkalsrud EW, Thakur A, Roof L. Comparison of loop versus end ileostomy for fecal diversion after restorative proctocolectomy for ulcerative colitis. J Am Coll Surg. 2000;190(4):418–422.

8. Winslet M, Drolc Z, Allan A, Keighley M. Assessment of the defunctioning efficiency of the loop ileostomy. Dis Colon Rectum. 1991;34(8):699–703.

9. Krausz M. Loop ileostomy for complete fecal diversion following colectomy and ileoanal anastomosis. Dis Colon Rectum. 1988;31(10):819–820.

10. Hanna MH, Vinci A, Pigazzi A. Diverting ileostomy in colorectal surgery: when is it necessary? Langenbecks Arch Surg. 2015;400(2):145–152. 

11. Shirley F, Kodner IJ, Fry RD. Loop ileostomy. Techniques and indications. Dis Colon Rectum. 1984;27(6):382–386. 

12. Morris DM, Rayburn D. Loop colostomies are totally diverting in adults. Am J Surg. 1991;161(6):668–671. 

13. Brooke BN. The management of an ileostomy. Lancet. 1952;260(6725):102–104.

14. Haas PA, Fox TA. The fate of the forgotten rectal pouch after Hartmann’s procedure without reconstruction. Am J Surg. 1990;159(1):106–110.

15. Glotzer DJ, Glick ME, Goldman H. Proctitis and colitis following diversion of the fecal stream. Gastroenterology. 1981;80(3):438–441.

16. Kabir SI, Kabir SA, Richards R, Ahmed J, MacFie J. Pathophysiology, clinical presentation and management of diversion colitis: a review of current literature. Int J Surg. 2014;12(10):1088–1092. Epub 2014 Aug 20.

17. Schofield PF, Cade D, Lambert M. Dependent proximal loop colostomy: Does it defunction the distal colon? Br J Surg. 1980;67(3):201–202. 

Dr. Shah is a general surgery resident, University of Virginia, Charlottesville, VA. Dr. Mauro is an internventional radiology fellow, Mount Sinai Hospital, New York, NY. Dr. Friel and Dr. Hedrick are colorectal surgeons, University of Virginia. Please address correspondence to: Puja M. Shah, MD, University of Virginia, Department of Surgery, PO Box 800679, Charlottesville, VA 22908-0679; email: ps5au@virginia.edu. 

Potential Conflicts of Interest: This research was funded by the National Institutes of Health Grant #Surgical Oncology T32 CA163177. The funding was used to provide salary support for the first author. The funder had no role in study design, data collection, or manuscript drafting.

Abstract

Pyoderma gangrenosum (PG) is a neutrophilic dermatosis of unknown etiology characterized by an ulcerative skin condition and confirmed through a diagnosis of exclusion. Management usually consists of systemic drug therapy, such as corticosteroids, sulfones, or immunosuppressants, either alone or in combination. Long-term use of these medications often has untold side effects. Hyperbaric oxygen therapy (HBOT) has been shown effective in the treatment of PG, reducing pain and tempering the need for medication.

A case is presented of a 54-year-old woman with diabetes, hypertension, and a peptic ulcer who presented with painful, purulent ulcers on her buttocks, hands, and lower extremities of 2 weeks’ duration. She was ultimately diagnosed with PG and provided 20 mg/day of oral prednisone for 1 week, tapered to 10 mg/day in the next week and then stopped. In addition, she received 12 sessions of HBOT — she breathed in 100% oxygen under 2.5 atmospheres absolute pressure for 90 minutes over 2 weeks. Her wounds healed without scarring. This excellent outcome including good wound healing, decreased pain, and reduced doses of systemic corticosteroids warrants additional study of the adjunctive use of HBOT for PG. 

Pyoderma gangrenosum (PG) is a painful ulcerative neutrophilic disease of the skin with unknown origin. It was first described by Brunsting et al¹ in 1930. von den Driesch² presented a study of 44 patients with PG with follow-up. Initially, PG clinically presents as a sterile pustule with an inflamed base, an erythematous nodule, or a hemorrhagic bulla on a violaceous base, mostly involving the lower extremities. These lesions evolve to form shallow or painful ulcers with a purulent undermined base and a violaceous gunmetal-colored border that spreads peripherally. With treatment, the borders flatten and the ulcer heals to form a thin cribriform scar.  Based on Ruocco et al’s³ and Dabade and Davis’⁴ reviews, the incidence of PG is 3 to 10 cases per million persons per year globally. Patients are generally between 25 and 50 years of age with a slight female predominance. Oka et al⁵ found interleukin-8 (IL-8) overexpression in skin specimens from patients with PG, and their animal studies suggest an etiologic role of IL-8 in the pathogenesis of PG. 

The etiology of PG remains poorly understood, but a predominantly immunological pathogenesis involving neutrophil dysfunction seems most likely. According to Dabade and Davis’⁴ and Alavi et al’s⁶ reviews, half of the patients with PG have associated systemic diseases, including inflammatory bowel disease, rheumatoid arthritis, myeloproliferative disorders, and connective tissue disease. 

In reviews^7,8 of several prospective, randomized, controlled studies, hyperbaric oxygen therapy (HBOT), the administration of 100% oxygen at 2 to 3 atmospheres absolute pressure, has shown benefits in treating acute and chronic wounds; because multiple cellular mechanisms are triggered by reactive oxygen and reactive nitrogen species, wounds treated with HBOT show improved neovascularization, decreased peripheral edema, and diminished inflammatory and immune responses. Complications (in <0.04% of cases) of HBOT include barotrauma, claustrophobia, myopia, and seizures. These are rare and usually reversible^7,8; however, irreversible nuclear cataracts have been described with HBOT exceeding 150 hours.⁹ Several case reports reviewed by Tutrone et al¹⁰ have shown HBOT to effectively treat PG ulcers and reduce pain associated with PG. 

Treatment of PG with prolonged high-dose systemic corticosteroids (0.5–1 mg/kg/day; more than 1 month) or other immunosuppressants, in addition to careful local wound care, characterizes the mainstay of management.^12-14 The following case study is presented to demonstrate that HBOT plays a role in moderating the dosage of steroids and reducing pain. 

Case Report

Ms. J is a 54-year-old woman weighing 65 kg with a history of type 2 diabetes mellitus, peptic ulcer disease, and hypertension controlled with oral medication. She presented at the authors’ dermatology department with a 2-week history of multiple painful ulcers with violaceous undermined borders and purulent bases located on her buttocks, both hands, and lower extremities (see Figure 1). She was afebrile and denied any history of skin disease or trauma. She was provided surgical debridement using a Goulian knife; wound dressings included povidone-iodine and gauze. Ms. J’s lesions quickly expanded laterally and developed a necrotic ulcerated center, worsening after 1 week of treatment. She rated her pain 8 out of 10 on a subjective visual analogue scale (VAS) and was given tramadol (50 mg) 6 times a day. She was referred to a plastic surgeon in a tertiary hospital for further evaluation who performed a skin biopsy of the lower extremities, 0.5 mm in diameter and deep to subcutaneous fat. All wounds were covered with alginate dressings to address absorption and possible infection. 

Pathology revealed neutrophilic dermatoses (see Figure 2). In order to eliminate other causes of cutaneous ulcers, laboratory testing was performed and included a complete blood cell count, levels of C-reactive protein, fasting blood sugar and lipids, hepatitis screening, evaluation of renal function, and urinalysis. Ms. J’s levels were all normal except for hyperglycemia. Screenings for hypercoagulability factors such as anticardiolipin antibodies, proteins C and S, antithrombin III, Factor V Leiden, and toxicology panel also were negative. Immunological tests including those for antinuclear antibody, rheumatic factor complement, cryoglobulinemia, and anti-SCL-70 and anticentromere antibodies were unremarkable. Wound cultures revealed negative results. PG was diagnosed based on clinical, histopathology, and laboratory findings.¹¹ Colonoscopy and blood tests for hematologic disorders showed no inflammatory bowel disease or hematologic disorders. Ms. J denied having arthritis. She was treated with 20 mg/day of oral prednisone for 1 week; this was tapered down to 10 mg/day in the next week and then stopped. 

The plastic surgeon, also an expert in HBOT, added HBOT to the treatment protocol immediately after receiving the biopsy result. Ms. J breathed 100% oxygen under 2.5 atmospheres absolute pressure for 90 minutes through a facemask. Twelve (12) HBOT sessions were performed daily except on weekends. The pain decreased to a VAS pain score of 2 after 1 week, and Ms. J received no analgesics. The lesions were completely healed with scarring in 2 weeks (see Figure 3). 

Ms. J continued to be monitored at the outpatient department and showed no evidence of relapse over 6 months. Considering the extensive PG observed at presentation, the cosmetic results were excellent with unapparent scars.

Discussion

PG is a rare form of neutrophilic dermatosis that presents as an inflammatory and ulcerative disorder of the skin. Because no diagnostic criteria have been established for clinical use, PG is a diagnosis of exclusion. In their review, Su et al¹¹ proposed major and minor criteria for the diagnosis of PG: the major criteria are rapid progression of a painful, necrolytic cutaneous ulcer and exclusion of other cutaneous disease; the minor criteria are pathergy, systemic disease-associated PG (ie, inflammatory bowel disease, arthritis, IgA gammopathy, or malignancy), and/or rapid response to systemic glucocorticoid treatment. To be considered a definite case of PG, the condition should meet the 2 major criteria and at least 2 minor criteria. von den Driesch² independently used inclusion criteria for the diagnosis of PG patients that are almost identical to Su et al.¹¹ 

Based on Oka et al’s⁵ study and Ahronowitz et al’s¹² review, neutrophil dysfunction, genetic factors, and dysregulation of the immune system might contribute to PG. The condition requires multiple treatment modalities to reduce inflammation and optimize wound healing, in addition to treating any underlying diseases. Prednisone and cyclosporine have been mainstays of the systemic treatment for PG, although several clinical trials¹² support the use of biological therapies such as tumor necrosis factor-α inhibitors for refractory cases of PG. According to Prystowsky et al’s¹³ summary of the management of 22 cases of PG over 4 years and Chow et al’s¹⁴ review of current PG treatment, experience suggests patients should receive 0.5–1 mg/kg per day of oral prednisone or its equivalent. The glucocorticoid treatments should be tapered off and discontinued within 4–10 weeks. 

Bennett et al¹⁵ performed a retrospective analysis of the medical records of 86 patients with PG who were evaluated and treated over 12 years at 2 university-based dermatology departments. Although clinical signs of improvement might be evident within a few days of initial treatment, the 86 PG patients reviewed required a mean 11.5 ± 11.1 months of treatment to achieve complete healing. 

Results of Dodiuk-Gad et al’s¹⁶ review included an evidence-based, strategic approach to the general risk management of systemic glucocorticoid use. Although the potent anti-inflammatory and immunosuppressive effects of systemic glucocorticoids have led to their wide use in the treatment of dermatologic diseases, long-term therapy of weeks or months with systemic glucocorticoids is associated with significant adverse effects, such as osteoporosis, myopathy, peptic ulcer disease, hyperglycemia, hypertension, and edema. For Ms. J, given her medical history, continued use of prednisone could have led to poor control of her diabetes and hypertension, and her peptic ulcer disease could have recurred.

Wound treatment with HBOT is well established. According to a Cochrane database systematic review,⁷ HBOT significantly improved the chance of healing foot ulcers in persons with diabetes mellitus. Dauwe et al⁹ conducted a systematic review of HBOT in the treatment of complicated acute wounds, flaps, and grafts: a total of 8 studies (4 prospective, randomized, controlled trials; 3 prospective, nonrandomized, controlled trials; and 1 retrospective, controlled trial) addressed the use of HBOT for wounds in humans. The results showed HBOT can augment healing in complicated acute wounds, such as skin graft survival, healing of burn injuries, and crush injuries. 

For Ms. J, hypertension, diabetes mellitus, and a history of peptic ulcer precluded long-term steroid use. Using adjuvant HBOT, the wounds heal rapidly in 2 weeks, allowing clinicians to decrease steroid dosage and duration. More studies are needed to increase the evidence base for this treatment approach.

Conclusion

PG is an uncommon inflammatory and ulcerative skin disorder characterized histopathologically by the accumulation of neutrophils in the skin. For patients with extensive PG, systemic glucocorticoids are used as first-line agents. For a patient with diabetes, hypertension, and a history of peptic ulcers, treatment of PG with a systemic glucocorticoid and HBOT allowed a decreased dosage and duration of steroid usage. Wound pain was diminished after 1 week and the wounds were healed after 2 weeks of treatment. Additional research is needed to determine the safety, efficacy, and effectiveness of this treatment approach for patients with PG. 

Acknowledgment

The authors thank the Civilian Administration Division of Tri-Service General Hospital, National Defense Medical Center and Shuang-Ho Hospital, Department of Surgery, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan, Republic of China.

References

1. Brunsting LA, Goeckerman WH, O’Leary PA. Pyoderma (echthyma) gangrenosum: clinical and experimental observations in five cases occurring in adults. Arch Derm Syphilol. 1930;22(4):655–680.

2. von den Driesch P. Pyoderma gangrenosum: a report of 44 cases with follow-up. Br J Dermatol. 1997;137(6):1000–1005.

3. Ruocco E, Sangiuliano S, Gravina AG, Miranda A, Nicoletti G. Pyoderma gangrenosum: an updated review. J Eur Acad Dermatol Venereol. 2009;23(9):1008–1017.

4. Dabade TS, Davis MD. Diagnosis and treatment of the neutrophilic dermatoses (pyoderma gangrenosum, Sweet’s syndrome). Dermatol Ther. 2011;24(2):273–284.

5. Oka M, Berking C, Nesbit M, et al. Interleukin-8 overexpression is present in pyoderma gangrenosum ulcers and leads to ulcer formation in human skin xenografts. Lab Invest. 2000;80(4):595–604.

6. Alavi A, Sajic D, Cerci FB, et al. Neutrophilic dermatoses: an update. Am J Clin Dermatol. 2014;15(5):413–423.

7. Kranke P, Bennett MH, Martyn-St James M, Schnabel A, Debus SF. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst Rev. 2015.6:CD 004123

8. Thom SR. Hyperbaric oxygen: its mechanisms and efficacy. Plast Reconstr Surg. 2011;127(1):131–141.

9. Dauwe PB, Pulikkottil BJ, Lavery L, et al. Does hyperbaric oxygen therapy work in facilitating acute wound healing: a systematic review. Plast Reconstr Surg. 2014;133(2):208e–215e.

10. Tutrone WD, Green K, Weinberg JM, Caglar S, Clarke D. Pyoderma gangrenosum: dermatologic application of hyperbaric oxygen therapy. J Drugs Dermatol. 2007;6(12):1214–1219.

11. Su WP, Davis MD, Weenig RH, Powell FC, Perry HO. Pyoderma gangrenosum: clinicopathologic correlation and proposed diagnostic criteria. Int J Dermatol. 2004;43(11):790–800.

12. Ahronowitz I, Harp J, Shinkai K. Etiology and management of pyoderma gangrenosum: a comprehensive review. Am J Clin Dermatol. 2012;13(3):191–211.

13. Prystowsky JH, Kahn SN, Lazarus GS. Present status of pyoderma gangrenosum. Review of 21 cases. Arch Dermatol. 1989;125(1):57–64.

14. Chow RK, Ho VC. Treatment of pyoderma gangrenosum. J Am Acad Dermatol. 1996;34(6):1047–1060.

15. Bennett ML, Jackson JM, Jorizzo JL, et al. Pyoderma gangrenosum. A comparison of typical and atypical forms with an emphasis on time to remission. Case review of 86 patients from 2 institutions. Medicine (Baltimore). 2000;79(1):37–46.

16. Dodiuk-Gad RP, Ish-Shalom S, Shear NH. Systemic glucocorticoids: important issues and practical guidelines for the dermatologist. Int J Dermatol. 2015;54(6):723-729

Dr. Chiang is a plastic resident, Division of Plastic Surgery, Department of Surgery; Dr. Liao is a pathologist resident, Department of Pathology; Dr. Dai is vice-professor, Chief, and attending plastic physician; Dr Chiao and Dr. Chou are plastic residents; Dr. SG Chen is a vice-president of Tri-Service General Hospital, professor, and attending plastic physician; and Dr. TM Chen is a professor and attending plastic physician, Division of Plastic Surgery, Department of Surgery, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, Republic of China. Dr. Chang is an assistant professor, Chief, and attending physician, Division of Plastic Surgery, Department of Surgery, Hyperbaric Oxygen Therapy Center, Shuang-Ho Hospital, Department of Surgery, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan, Republic of China. Please address correspondence to: Shun-Cheng Chang, No.291, Zhongzheng Rd, Zhonghe Dist, New Taipei City 235, Taiwan, Republic of China; email: csc901515@gmail.com.

Potential Conflicts of Interest: none disclosed 

Abstract

According to Greek mythology, Achilles was fatally wounded in his heel, bled out, and died. Several unproven hypotheses mention poisoning, infection, allergy, hemophilia, thyrotoxic storm (ie, pain and stress), and suicide. The author, a plastic surgeon who often treats chronic wounds, proposes an additional scenario: Although not mortally wounded, Achilles was considered dead, because in his time a wounded hero was as good as a dead hero, so he lived out the remainder of his life as former hero with a chronic wound far away from everyone.

To determine whether his injury was enough to cause fatal bleeding and quick death or if other factors might have been in play, a search of the literature was conducted to enhance what is known about Achilles, basically through the tale related in The Iliad and the clinical impact of an Achilles’ injury. Search terms utilized included bleeding tibialis posterior artery (3 manuscripts were found) and chronic wound, Achilles tendon (631 manuscripts were located). Although science may not be able to explain how and why Achilles died, the literature supported the conjecture that Achilles probably had a chronic wound with skin and paratenon defect, devitalized tendon tissue, bleeding, granulation, and repeated infections. It is interesting to consider the state of his injury and his mind in the making of this legend.   

Abstract

Insulin has been used in wound healing to increase wound collagen, granulation tissue, wound tensile strength, and local production of insulin-like growth factors by fibroblasts. Saline is a widely used irrigating and wound dressing solution. Patients admitted to an acute care facility who had a Grade 2 or Grade 3 pressure ulcer were recruited to participate in a randomized, controlled trial to compare the effect of normal saline-impregnated gauze and insulin dressing in pressure ulcer healing. Persons with immunodeficiency, diabetes mellitus, pregnancy, osteomyelitis, and peripheral vascular illness were not eligible for the study.

Study participants were randomized to receive either normal saline dressing gauze or insulin dressing twice daily for 7 days. At baseline, patient demographic data and ulcer history were recorded. Baseline and follow-up ulcer assessments (days 4 and day 7) included ulcer measurement (length and width) and completion of the Pressure Ulcer Scale for Healing (PUSH version 3.0) tool. Patients in the control group received dressings of sterile gauze soaked with normal saline; patients in the intervention group received topical insulin (1 U/cm² wound area). The insulin was sprayed over the wound surface with an insulin syringe, allowed to dry for 15 minutes, and then covered with sterile gauze. To ascertain the safety of study participants, blood glucose levels were measured with a glucometer 10 minutes before and 1 hour after the topical insulin application in the intervention group. Treatment efficacy was determined by assessing the reduction in wound area and PUSH scores at follow-up. Statistical analysis was performed; data are expressed as mean ± SD and percentage for continuous and categorical variables respectively. The differences in PUSH score and ulcer sizes between the 2 groups were analyzed using independent t-test, and within-group differences were analyzed using ANOVA with repeated measures; Greenhouse-Geisser correction was applied for the 3 consecutive measurements (day 1, day 4 and day 7). Fifty (50) patients (40 men, 10 women), ages 42.46 ± 15.47 years, with 50 ulcers, 25 in each treatment group, were enrolled. At baseline, demographic variables and wound characteristics were comparable between the 2 groups. By day 7, mean wound area had decreased from 11.79 ± 8.97 cm² (day 1) to 11.43 ± 9.06 cm² in the saline group (P = 0.566) and from 9.61 ± 6.39 cm² (day 1) to 6.24 ± 4.33 cm² (P<0.01) in the insulin group. Mean PUSH scores decreased from 10.52 ± 2.37 at baseline to 10.36 ± 2.40 on day 7 in the saline group (P = 0.475), and from 10.28 ± 1.10 to 8.52 ± 1.58 on day 7 (P<0.01) in the insulin group. No significant decrease in blood glucose level before and after insulin application (P>0.05) was observed. Treatment with topical insulin was found be safe and effective in reducing pressure ulcer size as compared to normal saline-soaked gauze. Future studies utilizing larger sample sizes, longer follow-up times, and different types of chronic wounds and control treatments are warranted.  

Abstract

Chronic venous leg ulcers (VLUs) affect up to 1% of the adult population in the developed world and present a significant financial and resource burden to health care systems. Cadexomer iodine (CI) is an antimicrobial dressing indicated for use in chronic exuding wounds. The aim of this study was to estimate the cost utility of using CI + standard care (SC) — ie, high compression multicomponent bandaging including debridement — compared with SC alone in the management of chronic (>6 months’ duration) VLUs from a payer’s perspective.

A Markov model was constructed to evaluate the cost and clinical benefits (healing and decreased infection rates) of the 2 treatment modalities over a 1-year period using data from 4 randomized, controlled clinical studies (RCTs) included in a recent Cochrane review and cost data from a recently published economic evaluation of VLUs. Costs were calculated using 2014 United States dollars; wound outcomes included complete healing in 212 patients reported in the Cochrane meta-analysis and quality-adjusted life years (QALYs), with utility values obtained from 200 patients with VLUs calculated using standard gamble. Treatment with CI over 1 year was $7,259 compared to $7,901 for SC. This resulted in a cost savings of $643/patient in favor of CI compared with SC. More patients treated with CI (61%) had their wounds healed compared to 54% treated with SC. Furthermore, patients treated with CI+SC experienced 6 additional ulcer-free weeks compared to persons treated with SC alone (ie, 25 ulcer-free weeks compared to 19 ulcer-free weeks, respectively). Overall, CI resulted in 0.03 more QALYs (ie, 0.86 QALYs compared to 0.83 for SC). The use of CI in addition to SC compared to SC alone over 52 weeks resulted in more wounds healed and more QALYs along with a decrease of overall costs The results of this study suggest CI is cost effective compared to SC alone in the management of patients with chronic VLUs. Prospective, controlled clinical studies are needed to elucidate the effect and cost effectiveness of CI on VLUs with and without signs of infection as compared to SC, other antiseptics, and more advanced topical treatment modalities.  

Abstract

Patients with acute wounds often delay seeking medical assistance until an incapacitating infection has developed. When such patients come for help at a remote Christian clinic in northern Ghana, West Africa, the goals of care are to resolve and prevent a return of infection, decrease pain, enable an immediate return to normal activities, and facilitate healing. Because the local protocol of care, Edinburgh University Solution of Lime (EUSOL)-soaked gauze, did not meet these goals, the author tried using a variety of donated wound dressing regimens.

Ultimately, polymeric membrane dressings (PMDs) were observed to meet patient care needs while also reducing clinic staff time and resources, and a PMD protocol of care was developed.Three (3) representative patients who presented with acute wounds and infection are described: a 20-year-old man with a hand abscess, a 16-year-old boy with a malleolus wound, and an approximately 20-year-old woman with an injection abscess, all otherwise relatively healthy, albeit undernourished. All 3 patients received oral antibiotics, their wounds were initially cleansed and debrided, and an appropriate configuration of either regular or silver-containing PMDs was applied to all exposed wound surfaces. Dressing changes were scheduled based upon the personalized plan of care. In all 3 patients, the pain-relieving properties of PMDs allowed resumption of activities within 1 day of initiating treatment, the dressings’ continuous wound cleansing system kept the wounds clean and free of infection despite the challenging environment, and the wounds healed steadily. Managing infected acute wounds with PMDs through complete wound closure was time efficient for clinic staff and met all 4 major patient goals of care. Randomized, controlled studies to compare wound and quality of life outcomes in patients whose infected wounds are managed with PMDs compared with those whose wounds are managed with other advanced dressings are warranted.

Abstract

Surgeries conducted with the patient in the prone position are frequent and can be lengthy. Abdominal stomas and suprapubic catheters require protection for the complete duration of the procedure to avoid complications such as stomal ischemia, bleeding, or mucocutaneous separation. Standard protection strategies such as pillows and wedges can easily fail.

In the course of managing several patients who had sustained ostomy complications following surgery in a prone position, a simple method of stoma protection was devised. Instead of discarding the foam headrest typically used during induction by anesthesia staff, this device is placed with its central recess over the stoma and secured to the patient’s abdominal wall with gentle tape just before turning the patient into a prone position. This method, used in more than 80 patients, has been found to effectively relieve pressure, and no complications have been observed. The foam shape also enables unobstructed drainage of fluids, facilitating collection and preventing leakage and contamination of the surgical field. Because the device is widely used by anesthesia, it is readily available and does not add any extra cost.

The incidence of newly formed stomas is estimated to exceed 130,000 yearly, and the number of people in the United States currently living with an ostomy is estimated to be more than 1,000,000.¹ These include colostomies, ileostomies, jejunostomies, gastrostomies, and urostomies; the resulting stomas, as well as suprapubic catheters, generally are positioned on the anterior abdominal wall and can be temporary or permanent. Among the numerous indications for stoma creation are chronic or acute bowel obstruction, trauma or perforation, rectal cancer, radiation, inflammatory bowel diseases, bladder cancer, spinal cord injury, immobility, major surgery of the digestive tract, gastrectomy, and nutritional insufficiency.^2,3 

In the authors’ parent academic institution, prone positioning is commonly employed during trauma, orthopedic, plastic reconstructive, or neurosurgical interventions.⁴ Many surgical and nonsurgical interventions that require protracted periods of prone positioning can prove challenging when faced with a ventrally located conduit or stoma. This is particularly true with a newly created stoma. In addition to meticulous preventive efforts to protect delicate soft tissues such as those over bony prominences, eyes, and face, stoma protection also is needed to prevent complications due to compression, shearing, and inadequate drainage. The latter may lead to stomal injury and/or disruption of the appliance. Stoma complications can include ischemia, bleeding, dermatitis, retraction, and mucocutaneous separation.^5,6 To the authors’ knowledge, the incidence of stoma complications related to surgery has not been reported. However, the authors have observed that kinking of the collection bag may result in inadequate evacuation and drainage as well as inaccurate volumetric recording of output during surgical cases. Damaged or dislodged stomal appliances can result in contamination of the operative field and the surrounding tissues. 

Before considering using the foam head rest for ostomy protection, the senior author had cared for several patients who had suffered ostomy-related complications after prone positioning. These complications included cases of dislodgement of the collection system with local soilage and contamination of the surgical field as well as a case of dehiscence in a newly established stoma. On careful review, several cases showed evidence of local trauma to the stoma and/or hematoma formation following a surgical procedure that required prone positioning. These complications, observed during postoperative patient care and through staff discussions, developed despite careful efforts by the operative team to protect and offload the stoma with the use of pillows and cushions. During the procedure, cushions would migrate, shearing forces would manifest, and local injury, kinking of drains, or obstruction would complicate care management and ostomy integrity. In some observed cases, further supportive attempts utilizing a larger number of additional cushions for further intraoperative stoma protection posed the potential for attenuation of respiratory excursions in paralyzed patients and poor offloading of pressure points. 

The Protective Device

Approximately a decade ago, the senior author developed a technique to protect the stoma when the patient is in the prone position. The technique involves using a standard foam headrest routinely utilized by anesthesia professionals. The headrest has a circular, central recess to stabilize the patient’s head and offload occipital pressure during the induction of anesthesia (see Figure 1). The largest diameter of the foam headrest usually utilized in the authors’ institution is 9 inches (228.6 mm), the diameter of the central recess is 4.5 inches (114.3 mm), and the height of the headrest is 2 inches (50.8 mm). When a patient with a stoma is transferred to a prone position, instead of discarding the device, it is repurposed to protect the stoma. 

The recessed portion of the foam serves as a repository for the stoma appliance and its contents, while the broad cylindrical foam cushion minimizes the likelihood of shearing and offloads compressive forces. The foam can easily be trimmed to fit nearly any stomal appliance or tubing, and given the wide variety available, this “one-size fits all” solution is particularly appropriate.

In the authors’ experience, use of the headrest appears to ensure safe and secure prone patient positioning, particularly if the clinician complies with the following guidelines (see Figure 2 and Figure 3): 

1. The clinicians should empty contents of the ostomy bag before the start of the procedure, either before or after the induction of anesthesia. This will minimize possible spillage and facilitate handling. 
2. The foam headrest should be oriented to surround the appliance. It may be trimmed to fit and accommodate effluent tubing.
3. If the stoma appliance is a bag, it can be accordion-folded into the foam’s central aperture or loosely inset so contents may still collect in the bag.
4. The clinician should ensure adequate space for the stoma appliance and the contents in the vertical plane.
5. Once the device is correctly placed, the foam should be secured to the abdominal wall with gentle tape.
6. Once the patient is positioned prone, the clinician should ensure the headrest is properly positioned with no compressive forces acting on either the stoma or headrest and that respiratory excursion is not impaired.

Discussion

Protecting the stoma is a critical element in the care and positioning of the surgical patient. Injury to these delicate, surgically created structures can have serious consequences. Dislodgement of collection devices and/or soilage of the operative field can compromise the integrity of the surgical field and local tissues while impairing drainage and monitoring efforts of stool, urine, and drainage output.

In the authors’ experience, repurposing the patient’s normally discarded foam headrest has proven to be an effective method of protecting both the patient and his/her stoma during prone positioning. The headrests are readily available; they are repurposed to the same individual at no additional cost to the patient. The foam is easily customized to accommodate a wide variety of applications, tubing, and connectors. The cushion protects the stoma from both direct and indirect trauma, minimizing the likelihood of dislodgement, soilage, maceration, or surgical field contamination while affording drainage and output monitoring when required. The foam ring is disposable, used exclusively on the same patient as well as on intact skin, and never reused. This technique, developed a decade ago, has gained wide acceptance throughout the authors’ institution and over the past 5 years has been adopted by multiple surgical specialties for intraoperative stoma protection in prone positioning. The senior author has utilized this technique in 80 patients for a variety of challenges, particularly in patients who have suffered pressure ulcers as well as patients being treated for major abdominal and spinal injuries. 

Guidelines for pressure relief over bony prominences generally advocate against the use of dense foam products. Moreover, properly designed stomas should be positioned appropriately to decrease chances of pressure injury.⁷ The headrest ring itself does not alter the patient’s positioning and creates minimal pressure on surrounding areas. The authors utilize standard established supportive positioning methods for securing and protecting the patient with particular attention paid to bony prominences, soft tissue, neurovascular structures, and eye protection while optimizing respiratory excursion. As with the application of any medical device or intervention, individualized considerations and judicious management are accordingly prioritized in the care of patients.

The stoma cap offers a preventive option.⁸ However, the foam headrest affords several advantages. The stoma cap does not allow for continued evacuation, drainage, or monitoring of effluences (eg, in the case of a urostomy). In addition, stoma caps are hard, fixed, and insufficiently cushioned to reduce pressure on the stoma or the surrounding skin.⁷ Finally, the stomal cap incurs additional cost to the patient.

In more than a decade of use by the senior author, the authors have not noted any complications from the technique. On rare occasions, an additional piece of tape was needed before turning the patient into the prone position to secure the foam before the start of surgery and after prone positioning to ensure the device is properly positioned.

Many hospitals in the United States utilize the same type of foam headrest during the induction of anesthesia; therefore, it is commonly available, making this technique easily and potentially widely implementable.

Conclusion

In the authors’ experience, using the patient’s discarded foam headrest is an effective method to protect his/her stoma during prolonged surgery in the prone position. Since employing this technique, no stomal complications from surgery have been noted following surgery in prone-positioned patients. This method is inexpensive, easily applied, and involves equipment that is readily available. n

References

1. United Ostomy Associations of America. Inc. About US. 2015. Available at: www.ostomy.org. Accessed April 7, 2015. 

2. Tapia J, Garcia G, Murguia R, Espinoza de los Monteros P, Onate E. Jejunostomy: techniques, indications, and complications. World J Surg. 1999:23(6):596–602.

3. Brand MI, Dujovny N. Preoperative considerations and creation of normal ostomies. Clin Colon Rectal Surg. 2008;21(1):5–16.

4. Rozet I, Vavilala MS. Risks and benefits of patient positioning during neurosurgical care. Anesthesiol Clin. 2007;25(3):631–653.

5. Kim JT, Kumar RR. Reoperation for stoma-related complications. Clin Colon Rectal Surg. 2006;19(4):207–212.

6. Husain SG, Cataldo TE. Late stomal complications. Clin Colon Rectal Surg. 2008;21(1):31–40.

7. Kroshinsky D, Strazzula L. Pressure Ulcers. Available at: www.merckmanuals.com/professional/dermatologic-disorders/pressure-ulcers.... Accessed May 15, 2016.

8. Cronin E. Colostomies and the use of colostomy appliances. Br J Nurs. 2008;17(17):S12–S16.

Potential Conflicts of Interest: none disclosed  

Dr. Mackert is a plastic and reconstructive surgery resident, Department of Hand, Plastic, and Recontructive Surgery, Burn Center, BG Trauma Center, Ludwigshafen, University of Heidelberg, Heidelberg, Germany. Dr. Reid is a plastic and reconstructive surgery resident; Dr. Dobke is Chief; and Dr. Tenenhaus is a Clinical Professor, Department of Surgery, Division of Plastic Surgery, University of California San Diego Medical Center, San Diego, CA. Please address correspondence to: Mayer Tenenhaus, MD, University of California San Diego, Department of Surgery, Division of Plastic Surgery, UC San Diego Medical Center, 200 W. Arbor Drive #8890, San Diego, CA 92103; email: m.tenenhaus@sbcglobal.net. 

Abstract

Educational intervention programs are an important element to improve nurses’ knowledge of pressure ulcer (PU) prevention. Various teaching methods have been used with diverse results but none have been analyzed in Nigeria. A quasi-experimental study using a pretest/post test design was conducted among 193 registered nurses with >6 months experience who worked in purposefully selected wards (neuroscience, orthopedics, renal, and cardiac) in 3 teaching hospitals to examine the level of knowledge retention after interactive instruction.

Participants were randomized to intervention (IG, n = 127 from 2 hospitals) and control (CG, n = 66 from 1 hospital) groups; the IG was provided a 5-day, face-to-face interactive lecture, and the CG engaged in a 1-day, 4-hour discussion of PU prevention practices. The Pressure Ulcer Knowledge Tool, a 47-item questionnaire in which a correct answer = 1 point and an incorrect/“I don’t know” answer = 0 (maximum score 47), was used to assess and compare knowledge retention at 3 time points: baseline (T1), immediately after instruction (T2), and after 3 months (T3). Three trained research assistants assisted with registration of participants and distribution and collection of the questionnaires. All questionnaires were retrieved at T1 before the intervention began. Respondents were encouraged to respond to all questions. Data were analyzed using t-test and ANOVA (P = 0.05). At T1, knowledge scores were comparable between the IG and CG (32.5 ± 4.2 and 30.8  ± 5.0 for IG and CG, respectively). At T2, knowledge scores increased significantly only in the IG to 40.7 ± 3.4 (d = 1.94, P<0.05). The mean difference between T1 and T2 was  -8.2 ± 5.4, t = -17.0, P = 0.000. Similarly, mean scores increased significantly from T2 to T3 in the IG (mean= -2.0 ± 5.5, t = -4.1, P = 0.000); scores in the CG were -6.2 ± 7.2, t = -6.3 (P = 0.000). A face-to-face interactive lecture was shown to be an effective method of program delivery for nurses; other educational methods should be assessed and their effects on PU prevention practices and outcomes evaluated.  

Pressure ulcers (PUs) are a significant threat to the safety of patients and have a major negative impact on patients, their families, and the health care system.^1,2 Findings from a cross-sectional observational study¹ conducted among 2,000 patients in a tertiary care hospital in Australia confirm PUs were responsible for prolonged hospital stay and increased economic cost. According to a systematic review and meta-synthesis,³ PUs have a substantial impact on health-related quality of life among older patients. A prevalence study by Mclnerney⁴ showed the risk of mortality is 2 to 6 times greater in patients with PUs as opposed to persons without PUs.^3,4 The negative effects may be even greater in the poorer nations of the world, particularly among patients with spinal cord injury. According to Zakrasek et al’s review of the literature⁵ on risk factors and cost of PU in low- and middle-income countries, the prevalence of PUs is high and comes with increasing complications.  

Various strategies regarding education and training for nurses have been shown to be factors in PU prevention.^6-8 For example, Tweed and Tweed⁶ conducted an educational intervention study among critical care nurses (N = 62) and reported an increase in knowledge for PU prevention post intervention. Using a pretest/post test design, Cox et al⁷ compared the effectiveness of 2 methods of instruction on PU prevention among critical care and medical surgical nurses and found knowledge retention can be maintained by a quarterly educational program. These educational programs have produced good outcomes, such as reduced PU incidence,^6,9 effective risk assessment, successful  planning, and implementation of interventions.^10-12 

Despite these findings, evidence from the literature suggests nurses’ level of PU knowledge is not yet optimal.^13,14 For example, although a systematic review¹³ of the effectiveness of educational programs in promoting knowledge among nurses for PU prevention showed educational programs have positive effects on nurses’ knowledge of PU prevention, similar reports of descriptive studies^15,16 in Nigeria suggested inadequate knowledge of PU prevention among nurses in Nigeria. Such reports point to a need for repeated education and training as new information on PUs emerges for Nigerian nurses. 

Literature Review

The joint international organization for PUs¹⁷ asserts a number of contributing or confounding factors, yet to be fully elucidated, are associated with PU development, underscoring a need for consistent attention to issues regarding PUs. Patient quality care and safety organizations have focused on PU prevention issues. For example, the American Nurses Association Quality Forum¹⁸ recognized PUs as largely preventable, nursing-sensitive adverse events. The Joint Commission on Accreditation of Healthcare Organization¹⁹ included PU prevention as one of the National Patient Safety Goals. The strong position on PU prevention taken by these organizations commends programs that provide PU updates for nurses because nurses play significant roles in PU prevention. Quasi-experimental, pretest/post test and descriptive studies^20,21 confirm that inadequate knowledge and skills for PU prevention among nurses working in acute care facilities can significantly influence PU rates¹³ and patients’ clinical outcomes. This is evident in Nigeria, where hospital-based surveys^22-25 reported increased PU incidence rates are attributed partly to inadequate knowledge of evidence-based preventive interventions among care providers, particularly nurses. This conclusion was corroborated by other authors,^15,16 who reported knowledge about PU prevention among nurses was less than optimal. 

Continuing education is vital to consistent, safe, and effective care delivery and also a prerequisite for reconfirmation of practice licenses in most countries.^26,27 Specifically, continuing education comprises activities that increase the knowledge of workers toward improved performance.²⁸ Different strategies including face-to-face lectures are employed in continuing education programs. Traditional lectures are typically teacher-focused, one-way communication, which leaves the learners inactive and passive.^29,30 According to quasi-experimental studies involving nurses,^28,31,32 the duration of knowledge retention by learners participating in the lecture method is short, usually no longer than 8 weeks, even with the use of PowerPoint® delivery. Based on this limitation, educational experts³³ suggest integrating diverse or blended methods in any one teaching session for better outcomes.

Teaching theories. Adult, professional learners such as nurses would benefit from blended strategies, because these learners are self-directed and need to have control over their learning needs.³⁴ Nursing professionals need to incorporate learning into their busy schedules to effectively  understand and be current with increasing research evidence in health care, which also drives health care improvements. Some descriptive studies^35,36 involving medical students suggest when professionals are engaged in learning, they reflect on previous experiences to bring meaning to the new knowledge, enhancing the learning experience. To facilitate reflection and better understanding of new knowledge, particular delivery strategies should be incorporated into a professional continuing education program. According to Sandars’³⁷ review on the concept of reflection,³⁷ reflection is a metacognitive process that creates better understanding of both the self and the situation to inform future actions. As such, reflection is a major component of life-long learning and believed to improve professional competence. Experience is significant in professional learning, but it is not a stand-alone phenomenon. Drawing from Kolb’s³⁸ theory of experiential learning, experience must be integrated into an existing knowledge structure to become new and expanded knowledge. This process requires the skill of reflection for a higher level of personal learning, such as when an individual learns about the side effects of a drug by observing reactions (experience) from a patient on the drug or when the clinician becomes more adept at a clinical skill after an experience demonstrating ineffective application of the skill. 

Interactive lecture is a form of inquiry learning that allows active learner participation and reduces the monotony of passive learning that occurs with the traditional lecture.³⁹ Interactive lecture is implemented using methods such as brainstorming, small group discussion, role play, and simulations,⁴⁰ enhancing student engagement with their course materials. Interactive lectures also may take the form of questioning the audience or using engagement triggers to stimulate interest and arouse the learner’s attention and serve as ice breakers.⁴¹ In his review of the literature describing the indicators of interactive learning, Steinert and Snell⁴¹ noted active participation of learners is a prerequisite for learning beyond the recall of facts. On a broader perspective, Lee⁴² acknowledged interactive learning  encompasses every method except traditional lecture. The effectiveness of the interactive mode of learning has been well documented as a preferred method to the traditional lecture. However, to the best of the authors’ knowledge, its effectiveness in delivering PU prevention education in Nigeria has not been documented. 

The aim of this study was to examine the effectiveness of a face-to-face, interactive lecture approach to education on knowledge retention among nurses in selected teaching hospitals in southwest Nigeria.

Four (4) research questions were raised: 

1. What is the knowledge of PU prevention strategies of the intervention and control groups at baseline?

2. What is the effect of interactive lecture on post test knowledge score in intervention and control groups?

3. What is the difference in post test scores immediately (T2) and 3 months (T3) post intervention in the intervention group?

4. What is the effect of selected demographic characteristics (years of experience, professional cadre based on profession, previous exposure to PU lecture) on knowledge score in the 2 groups before and after educational intervention?

Methods and Procedures 

The study adopted a nonequivalent control group, pretest/post test design and was conducted in 3 selected teaching hospitals in 3 (Oyo, Osun, and Lagos) of the 6 states in the southwest geopolitical zone in Nigeria. The hospitals included the University College Hospital (UCH) and Lagos State University Teaching Hospital (LASUTH), Ibadan; and Obafemi Awolowo University Teaching Hospital Complex (OAUTHC), Ile Ife. The hospitals were under 2 main clusters based on proprietorship: state government-owned and federal government-owned, publicly funded institutions. All of  the hospitals are large tertiary institutions, with a minimum of 300 beds each. Ethical approval was sought and obtained from the Health Research and Ethics Boards of each institution. 

A purposive sampling of the hospital was conducted based on inclusion criterion of providing care for patients with complex health problems. Balloting was done to determine which hospitals served as intervention and control groups. The intervention group (IG) included nurses from LASUTH and UCH, and the control group (CG) included nurses from OAUTHC. To limit inadvertent influence of treatment condition on the CG, the IG was completely separate from the CG. 

Participating wards also were selected purposively to reflect patients with health problems that would likely place them at risk for PUs; as such, all nurses from the surgical (orthopedics), medical, and neurological wards (except nurses on vacation) were invited to participate. 

Testing instrument. The Pressure Ulcer Knowledge Test (PUKT)⁴³ was used to assess knowledge and information acquisition at the 3 testing time points. The tool is composed of 47 items that measure respondents’ knowledge of risk factors, preventive strategies, and PU staging. Correct Yes/No responses are scored 1 and incorrect responses of Yes, No, or I don’t know are scored 0. The maximum score is 47 (100%).  

The PUKT has been used in other countries^9,44 with reported good reliability levels. A pilot survey was conducted in a different state teaching hospital (Ogun state) among 111 nurses 6 months before the main study to examine the feasibility of the study and to test the reliability of the testing tool.¹⁶ Findings from the pilot study led to the revision and rewording of some items in the instrument for clarity and in relation to the care environment. For example, in the local hospital, nurses use water-filled gloves to elevate the heels. Therefore, the item in  the original document that reads Heel protectors relieve pressure on the heels  was reworded to read A heel protector such as water-filled glove effectively relieves pressure on the heels. In addition, the item that relates to the appointment of a governmental panel to study PU risk, prevention, and treatment were removed because it was not applicable to Nigeria. This was the first time the PUKT was validated in Nigeria. The reliability coefficient was found to be 0.82. 

General procedure. In each setting, with the support of the Director of Nursing services, the pretest (paper-and-pencil PUKT) was administered to all participants at the same time. This was to ensure the uniformity of nurses’ entry behavior and to establish their level of PU knowledge at baseline (T1) to accurately examine the effect of the program. Each participant signed a register to document attendance. The researcher recruited and trained 3 research assistants (RAs) to assist with participant registration and to monitor and retrieve completed questionnaires. 

Study group procedure. The nature, purpose, and procedure of the study were explained to nurses who provided written consent for participation. The IG participants  (UCH and LASUTH) were invited to attend the educational workshop organized in the respective hospitals. 

The program was structured to accommodate various nursing schedules because it was not possible to take all nurses off the wards at the same time to attend the 4-hour workshop. In UCH, the nurses were divided into 2 groups. Each group attended the workshop for 5 consecutive days. In LASUTH, all participants attended the same 5-day workshop facilitated by a labor conflict that decreased patient load.

Intervention fidelity was maintained because the module curriculum was followed strictly by the principal investigator, who also delivered all the sessions. 

The interactive educational program. Participants were provided the program of events for each day. They were encouraged to choose an identification number to facilitate analysis in matching each participant’s pretest with post test scores, to assess full participation, and to easily identify missing questionnaires. The intervention was an interactive lecture that involved small group discussions and brainstorming. Participants were grouped based on the wards where they work to facilitate continual cooperative work on the wards. During the first 15 minutes of each module, participants brainstormed on specific questions and answers and shared experiences and practical ideas on PU prevention. The remaining period was used for lectures and discussion on current trends regarding PU prevention and related clinical correlations. For example, the researcher projected pictures of different stages of PUs and participants were asked to determine the stages. This helped actively involve participants in the sessions. Lectures were projected using PowerPoint® slides. The principles of adult learning³⁴ guided the interaction with the participants (ie, learners connect learning with past experience). To facilitate this connection, the researcher also displayed different skin care products (eg, dimethicone-based barrier creams and sprays, dressings, foams, and corn starch) to stimulate discussions on nurses’ practices. At the end of the sessions, paper versions of the PowerPoint® slides were provided to participants. The level of each respondent’s participation was not documented or measured.

All modules were presented by the principal investigator in the 2 hospitals. Each session lasted for 4 hours per day. The curriculum consisted of 5 modules as shown in Table 1. 

Assessment. A pencil-and-paper PUKT was readministered on day 5 as an immediate post test (T2). The test was completed under supervision, and participants did not refer to the paper versions of the slides. Completed tests were retrieved on the spot. Participants were informed they would be invited to a third round of testing after 12 weeks (T3).  

Participants returned to their respective wards but maintained the groupings to facilitate cooperative problem-solving while providing care. Over the 12-week between-test period, the researcher reinforced what was covered in the module with hands-on demonstrations. At the end of 12 weeks, participants were contacted by telephone, Short Message Services, and email for the second post test. The same test (PUKT) was administered at all 3 time points. 

Control group procedure. The CG also was provided study details. The PUKT questionnaire was distributed to the participants to examine their baseline knowledge. The participants engaged in a general 1-day, 4-hour discussion on their usual practices for PU prevention. The session was facilitated by the RAs under the supervision of the principal investigator. This was followed by a second test (T2). Participants were contacted for the second post test at 3 months (T3). 

At the end of the third data collection (which marked the end of the study), the CG was provided the same package of educational materials as the IG on PU prevention for ethical reasons. 

Data analysis. Data from the PUKT instrument were collected and entered into a database, the Statistical Package for Social Sciences (SPSS) (Version 17.0, Chicago, IL), for analysis. Data were checked to ensure consistency and to determine where information was missing. A complete case-wise analysis was performed for missing data because the proportion of missing data categorized as Missing Completely at Random (MCAR) was <10% and  was observed only at the 3-month post test (T3). Descriptive statistics using absolute number and relative frequencies (percentages) to describe the sample characteristics were used. Means and standard deviations were computed to ascertain nurses’ PU knowledge scores. A paired sample t-test was used to compare the differences in knowledge between IG and CG pre- and post intervention. Cohen’s d was calculated to determine the strength of the intervention effect. The effect of selected demographic variables on participants’ knowledge scores was examined using ANOVA, and the effect size (eta squared) also was computed. The level of significance was set at α = 0.05% 

Results

Demographic characteristics. The sample consisted of 193 registered nurses, 127 in the IG and 66 in the CG. The level of education and areas of practice are described in Table 2. The majority of the respondents were basic diploma-certified registered nurses (RN) (133, 68%) and degreed nurses (BNSc) (26, 13.5%); a statistically significant difference was noted in both the IG (36.8 ± 10.3, P = 0.03) and CG (35.2 ± 11.9, P = 0.04). A similar trend was found with years of experience between IG and CG (14.5 ± 13.7, P = 0.04 and 12.6 ± 12.0, P = 0.03, respectively).

Baseline knowledge. The mean knowledge score at baseline was comparable in both IG (32.5, SD = 4.2) and CG (30.8, SD = 5.0), as shown in Table 3. 

Knowledge retention. The score at T2 significantly increased only in the IG from 32.5 ± 4.2 to 40.7 ± 3.4. In the CG, the T2 score did not increase significantly (31.2 ± 5.2, effect size, Cohen d = 1.94). At 3 months (T3), a further increase in knowledge score was observed in the IG from 40.7 ± 3.4 to 42.7 ± 4.0, P<0.001) and in the CG from 31.2 ± 5.2 to 37.8 ± -6.3 (P<0.001) (see Table 3).

Using a paired sample t-test to compare results between the IG and CG from T1 to T2 and T3, the increased mean difference in knowledge scores was noted to be significantly higher in the IG than in the CG (-8.2  ± 5.4, t = -17.0, P<0.001, d = 0.385) (see Table 4), suggesting the intervention accounted for 38.5% of the change in knowledge scores. 

Effect of selected demographic characteristic. The effect of selected demographic characteristics (eg, years of experience, professional cadre, and previous exposure to a PU lecture) on respondents’ scores pre- and post intervention was determined using one-way ANOVA. Findings were not significant (see Table 5). An examination⁴⁵ of the combined effect (interaction) of selected respondents’ factors (eg, years of experience, previous exposure to PU lecture) on the post test scores using a one-way ANOVA showed a significant interaction effect with previous exposure to PU education (F[1,192] = 2.781, P<0.05). However, the interaction effect with both years of experience and professional cadre was not significant (P>0.05).

Discussion  

The aim of this study was to examine the effectiveness of a face-to-face, interactive PU lecture approach to education on knowledge retention among nurses by comparing pretest and post test knowledge scores. The major hypothesis was that nurses will be able to retain knowledge for 3 months post intervention better than nurses who were not exposed to a similar learning method. The intervention was carried out in the same manner by the researcher in all the settings using the modules designed for the program. Participants were selected from neurology, orthopedic surgery, and medical inpatients units because reports from previous studies indicated the risk of PU was higher in patients admitted to these units as a consequence of impaired physical mobility.⁴⁵ Results of Niederhauser et al’s⁴⁶ systematic review of literature underscored the importance of PU educational programs in successful implementation of preventive protocols.  

The current study showed nurses had some basic knowledge about PU prevention because they were experienced practitioners. However, after the interactive lecture, the knowledge level increased significantly in the IG as compared to what was observed in the CG.   In addition, participants were able to retain the knowledge acquired as indicated by the mean scores at the 3-month follow-up. This suggests the intervention was effective. In contrast to these findings, reports from previous quasi-experimental studies^30,31 involving nursing and medical science students showed students tend to forget ~80% of presented education within 8 weeks of a lecture. The current findings showed knowledge of PU prevention was sustained for 12 weeks (3 months) post intervention among the study cohort, as well as in the CG. This sustained knowledge retention may be linked to the fact respondents in both groups were adult learners, with varied previous experiences and learning they brought to the fore. In addition, hands-on experience and reinforcement of what was learned during the follow-up period in the IG could have contributed to the sustained knowledge 

Khatoni et al’s⁴⁷ pretest/post test study among nurses (N = 140) suggested both lecture and elearning methods are effective in increasing students’ knowledge. Although opinions tend to differ regarding the most effective method of teaching, evidence supports the effectiveness of interactive lectures, which enhance active student engagement and participation and demonstrate more positive learning gains than traditional lecture methods. For example, from results of their study, Prince and Felder³⁹ proposed inductive learning methods, including cooperative or team learning, active learning, case studies, projects, or presentations, are more effective than the traditional lecture. 

In this study, sustained knowledge retention may be explained using the principles of cooperative learning as proposed by Johnson et al.⁴⁸ Accordingly, the authors described cooperative learning as the instructional use of small groups to facilitate students’ working together to maximize their learning through mutual dependence rather than competition. It is proposed such learning strategy promotes deep understanding of the subject matter and enhances knowledge retention. It follows that within the small groups, participants can easily exchange views and develop self-confidence. Johnson and Johnson⁴⁹ also believed working/learning in small groups works among health care professionals to help develop communication skills essential for building stronger communication with patients.  

In the current study, participants worked in small groups based on their respective wards. During the 3-month follow-up period, the researcher visited the nurse participants on the wards weekly, and teaching was reinforced at the bedside to promote evidence-based practice. The practice component is not part of this current report. The authors strongly believe the small group discussions and the supplemental printed materials (ie, PowerPoint® slides) sustained the interactive learning and also enhanced self-instruction and knowledge retention. Additionally, participants were experienced practitioners. Goldberg et al’s⁵⁰ pretest/post test study (N = 130) noted interactive lecture increased students’ self-efficacy, which is  associated with academic achievement. Similarly, Knight and Wood’s⁵¹ pretest post test study (N = 700) to compare the learning gains between traditionally taught lecture and interactive classroom format concluded collaborative work in student groupings and discussions significantly increased learning gains and conceptual understanding. Furthermore, Prince and Felder³⁹ noted a strong motivation to learn when learners clearly perceive a need to know. It follows that learners’ perception of their specific learning needs influences the motivation to learn. The findings in the current study also can be explained by Kolb’s³⁸ model of experiential learning, which hypothesized that concrete experience allows for reflection (ie, incorporation of experience with teaching). The current study authors assert such reflection was demonstrated by study participants, which possibly also strengthened their ability to recall new knowledge, as observed only in the IG. 

Adult learners have previous experiences that help illuminate a new learning situation. As such, the current study examined the interaction effect of treatment, years of experience, and exposure to previous PU lectures on post test scores in the IG and CG. The findings indicated a significant difference, suggesting the educational intervention accounted for the difference in post test scores and was not independently determined by demographic characteristics. This finding is consistent with Hulsenboom et al,⁵² whose cross-sectional, comparative study among nurses (N = 522) concluded demographics, including age and nurse experience, had no significant influence on knowledge of PU preventive interventions. 

Nurses play a significant role in PU prevention, requiring ongoing acquisition of knowledge. Because the interactive lecture contributed significantly to knowledge retention, a more consistent use of interactive methods of teaching, such as case presentations, brainstorming, and small group discussions, is suggested for continuing nurse education.  

Limitations 

The present study was conducted among nurses in 3 tertiary institutions. A study with a wider scope that may include nurses in secondary care facilities is warranted. In addition, comparison of the effectiveness of lecture with other methods of program delivery also should be considered. 

Limitations also include the fact the interactive face-to-face lecture method was compared with only 1 other method of program delivery (discussion group), so the findings should be interpreted with caution. Additionally, the pretest/post test design of this study limits the degree to which the results may be attributed to the effects of the intervention (ie, the authors had no control over natural events in the comparison group hospital). Therefore the effects of history may be a threat to internal validity. In this vein, history describes events that occur concurrently with the treatment, which the researcher may not have control over, thereby influencing the results obtained. In the current study, the possibility of another educational program in the CG institution during the period of this study that could provide information on the subject matter to respondents cannot be ruled out. To the best of the authors’ knowledge, the CG participants were not exposed to another learning situation except that the intervention package was provided at the end of the study to the CG participants. Finally, knowledge retention was monitored for only 3 months post intervention.

Conclusion 

A pretest/post test study was conducted to measure gains in knowledge retention for nurses following an interactive lecture on PU prevention. The results demonstrate an interactive lecture using small groups can effectively facilitate knowledge retention among nurses in a continuing education program. The effect of intervention was significantly higher in the IG than in the CG. Interactive engagement of nurses and inductive methods of instruction for program delivery appear to be successful approaches in continuing education programs for nurses. Future studies are needed to examine how acquired knowledge translates into effective PU prevention practices and influences clinical outcomes. 

References

1. Graves N, Birrell F, Whitby M. Effect of pressure ulcers on length of hospital stay. Infect Control Hosp Epidemiol. 2005;26(3):293–297.

2. Gorecki C, Brown JM, Nelson EA, et al; European Quality of Life Pressure Ulcer Project group. Impact of pressure ulcers on quality of life in older patients: a systematic review. J Am Geriatr Soc. 2009;57(7):1175–1183.

3. National Quality Measures Clearinghouse. Pressure ulcers: percentage of patients with documented assessment of risks for possible pressure ulcer development, 2005. Available at: www.qualitymeasures.ahrq.gov/summary.aspx?ss=1&doc_id=6428.  Accessed February 12, 2015. 

4. McInerney JA. Reducing hospital-acquired pressure ulcer prevalence through focused prevention program. Adv Skin Wound Care. 2008;21(2):75–78. 

5. Zakrasek EC, Creasey G, Crew JD. Pressure ulcers in people with spinal cord injury in developing nations. Spinal Cord. 2015;53(1):7–13.

6. Tweed C, Tweed M. Intensive care nurses knowledge of pressure ulcers: development of an assessment tool and effect of an educational program. Am J Crit Care. 2008;17(4):338–346.

7. Cox JR, Roche S, Van Wynen E. The effect of various instructional methods on retention of knowledge about pressure ulcer among critical care and medical surgical nurses. J Continuing Ed Nurs. 2011;42(2):71–78. 

8. Andrade EMLR, Cavalcanti PAL, Monteiro AKC, et al. Effect of educational intervention by attendance and distance on nurses’ knowledge about pressure ulcer. Creative Ed. 2014;5(18):1673–1677.

9. Miyazaki MY, Caliri MH, dos Santos CB. Knowledge on pressure ulcer prevention among nursing professionals. Rev Lat Am Enfermagem. 2010;18(6):1203–1211.

10. Magnan MA, Maklebust J. The nursing process and pressure ulcer prevention: making the connection. Adv Skin Wound Care. 2009;22(2):83–92.

11. Hopkins B, Hanlon M, Yauk S, Sykes S, Rose T, Cleary A. Reducing nosocomial pressure ulcers in acute care facility. J Nurs Care Qual. 2000;14(3):28–36.

12. Padula CA, Osborne E, Williams J. Wound care: prevention and early detection of pressure ulcers in hospitalized patients. J Wound Ostomy Continence Nurs. 2008;35(1):66–75.

13. Mei-Yu H, Wen-Yi T, Huei-chuan C. The effectiveness of educational programs in promoting nurses’ knowledge of pressure ulcers: a systematic review protocol. JBI Database Syst Rev Implementation Reports (SI). 2013;11(5):132–139.

14. Chianca TC, Resende JF, Borges EL, Nogueira VL, Caliri MH. Pressure ulcer among nurses in Brazilian university hospital. Ostomy Wound Manage. 2010;56(10):58–64. 

15. Adejumo PO. Nurses perception of activities at preventing pressure sore among selected patients at the University College Hospital, Ibadan. West African J Nurs. 2010;21(2):90–98.

16. Ilesanmi RE, Ofi BA, Adejumo PO. Nurses’ knowledge of pressure ulcer prevention in Ogun state, Nigeria: result of a pilot survey. Ostomy Wound Manage. 2012;58(2):24–32. 

17. Haesler E (ed). European Pressure Ulcer Advisory Panel, National Pressure Ulcer Advisory Panel and Pan-Pacific Pressure Injury Alliance. Prevention and Treatment of Pressure Ulcers:Clinical Practice Guideline. Perth, Australia: Cambridge Media;2014.

18. American Nurses Association National Quality Forum (ANANQF). Nursing-Sensitive Indicators, 2015. Available at: www.nursingworld.org.  Accessed April 12, 2015.

19. The Joint Commission on Accreditation of Healthcare Organization (JCAHO).  National Patient Safety Goals. 2012, Available at: www.jointcommission.org/standards information/npsgs.aspx. Accessed March, 5, 2015. 

20. Gunningberg L. Pressure ulcer prevention: evaluation of an education program for Swedish nurses. J Wound Care. 2004;13(3):85–89.

21. Qaddumi J, Khawaldeh.  Pressure ulcer prevention knowledge among Jordanian nurses: a cross-sectional study. BMC Nurs. 2014;13(6). Available at: www.biomedcentral.com/1472-6955/13/6. Accessed March 13, 2015.

22. Lepistö M, Eriksson E, Hietanen H, Asko-Seljavaara S. Patients with pressure ulcer in Finnish hospitals. Int J Nurs Pract. 2001;7(4):280-287.

23. Ikechukwu EC, Ayodiipo IO, Emeka AD, Kayode AJ, Michael NI, Deborah OT. Prevalence and factors associated with healing outcomes of hospital-acquired pressure ulcers among patients with spinal cord injury. J Pub Health Epidermiol. 2012;4(2):44–47. 

24. Onigbinde AT, Ogunsanya GI, Oniyangi SO. Pressure ulcer incidence among high risk in-patients in Nigeria. Br J Nurs. 2012;21(12):S4–S10.

25. Awwal LM, Ngaski GS, Khalid SD,  Hadiza SM, Farouk MA. Pressure ulcer stages among bed-ridden patients in ABUTH, Zaria. IOSR J Nurs Health Sci. 2014;3(1):61–68.

26. Eustace LW. Mandatory continuing education: past, present, and future trends and issues. J Continuing Ed Nurs. 2001;32(3):133–137.

27. Chong MC, Francis K, Cooper S, Abdullah K. Current continuing education practice among Malaysian nurses. Nurs Res Pract. Available at: www.hindawi.com. Accessed March 17, 2015.

28. Abbasi K, Hazrah M. Mohamadi NP, Rajaeefard A. The effects of learning via modules versus lecture teaching methods on knowledge and practice of oncology nurses about safety standards with cytotoxic drugs in Shiraz University of medical Sciences. IranianJ Nurs Midwifery Res. 2013;18(6):483–487.

29. Norouzi HM, Mohsenizadeh SM, Jafary SH, Ebrahimzadeh S. The effect of teaching using a blend of collaborative and mastery of learning models, on learning of vital signs: an experiment on nursing and operation room students of Mashhad University of Medical Sciences. Iranian J Med Ed. 2011;11(5):544–553.

30. Sadeghi R, Sedaghat MM, Ahmadi F. Comparison of effect of lecture and blended teaching methods on students learning and satisfaction. J Adv Med Ed Profession. 2014;2(4):146–150. 

31. Safari M, Yazdanpanah B, Ghafarian HR, Yazdanpanah S. Comparing effect of lecture and discussion methods on students’ learning and satisfaction. Iran J Med Ed. 2006;6(1):59–64.

32. Beeckam D, Schoonhoven L, Boucqué H, Van Maele G,  Defloor T. Pressure ulcers: e-learning to improve classification by nurses and nursing students. J Clin Nurs.2008;17(13):1697–1707.

33. Garrison DR, Kanuka H. Blended learning: uncovering its transformative potential in higher education. Internet Higher Ed. 2004:7(2):95–105.

34. Knowles M. The Adult Learner: A Neglected Species. Houston, TX: Gulf Publishing Company;1990.

35. Sobral D. An appraisal of medical students’ reflection-in-learning. Med Ed. 2000;34(3):182–187.

36. Grant A, Kinnersley P, Metcalf E, Pill R, Housten H. Students’ view of reflective learning techniques: an efficacy study at UK medical school. Med Ed. 2006;40(6):376–388.

37. Sandars J. The Use of Reflection in Medical Education: AMEE Guide NO.4. 2009. Available at: www.medsqueensu.ca. Accessed March 7, 2015.

38. Kolb DA. Experiential Learning: Experiences as the Source of Learning and Development. Englewood Cliffs, NJ: Prentice Hall;1984.

39. Prince MP, Felder RM. Inductive teaching and learning methods: definitions, compositions and research bases. J Engineer Ed. 2006;95(2):123–138.

40. Eidin YKZ. Implementing interactive nursing administration lectures and identifying its influence on students’ learning gains. J Nurs Ed Pract. 2014;4(5):107–115.

41. Steinert Y, Snell LS. Interactive lecturing: strategies for increasing participation in large group presentations. Med Teacher. 1999;21(1):37–42.

42. Lee VS (ed). Teaching and Learning Through Inquiry: A Guidebook for Institutions and Instructors. Sterling, VA: Stylus Publishing;2004.

43. Pieper B, Mott M. Nurses’ knowledge of pressure ulcer prevention, staging and description. Adv Wound Care. 1995;8(3):34–48.

44. Sinclair L, Berwiczonek H, Thurston N, et al.  Evaluation of an evidence-based education program for pressure ulcer prevention. J Wound Ostomy Continence Nurs. 2004;31(1):43–50.

45. Adyin AK, Karadag A. Assessment of nurses’ knowledge and practice in prevention and management of deep tissue injury and stage I pressure ulcer. J Wound Ostomy Continence Nurs. 2010;37(5):487–494.

46. Niederhauser A, Lukas V, Parker V, Ayello EA, Zulkowski K, Berlowitz D.  Comprehensive programs for preventing pressure ulcers: a review of the literature.  Adv Skin Wound Care. 2012;25(4):167–188.

47. Khatoni A, Nayery N. D, Ahmady F, Haghani H. Comparison of effect of web-based education and traditional education on nurses knowledge about bird flu in continuing education. Iranian J Med Ed. 2011;11(2):140–148.

48. Johnson D, Johnson RT, Smith KA. Active Learning: Cooperative in the College Classroom, 2nd ed. Edina, MN: Interaction Books Company;1998.

49. Johnson DH, Johnson FP.  Joining Together: Group Theory and Group Skills, 8th ed. Boston, MA: Allyn and Bacon;2003.

50. Goldberg HR, Haase E, Shoukas A, Schramm L. Redefining classroom instruction. Adv Physiol Ed. 2006;30(3):124–127.

51. Knight JK, Wood WB. Teaching more by lecturing less. Cell Biol Ed. 2005;4:298–310.

52. Hulsenboom MA, Bours GJ, Halfans RJ. Knowledge of pressure ulcer prevention: a cross-sectional and comparative study among nurses. BMC Nurs. 2007;6(2). doi: 10.1186/1472-6955-6-2

Dr. Ilesanmi is a lecturer and a certified wound care nurse, Department of Nursing; and Prof Oluwatosin is a Professor of Plastic and Reconstructive Surgery, Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria. Please address correspondence to: Dr. Rose Ekama Ilesanmi, Department of Nursing, University of Ibadan, Ibadan, Nigeria; email: ekamailesanmi@yahoo.com.

Potential Conflicts of Interest: none disclosed