A Two-year Retrospective Review of Suspected Deep Tissue Injury Evolution in Adult Acute Care Patients

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Ostomy Wound Manage. 2013;59(9):30–39.
Rhonda Sullivan, PhD, RN, CWON, LNCC

Abstract

  Suspected deep tissue injury (sDTI) was recently defined as a pressure ulcer category, and knowledge about the evolution of these ulcers is limited. The purpose of this single-site, 2-year, retrospective, IRB-approved study was to increase understanding of the evolution and outcomes of sDTI.

Inclusion criteria were hospitalized patients, 18 years or older, with a sDTI confirmed by a wound care nurse. Patient charts and WOC nurse notes were examined and patient demographics and DTI variables abstracted. All patients received standardized, comprehensive care for pressure ulcer prevention and treatment. Seventy-seven (77) patients, average age 67.5 years (range 32–91 years), with 128 sDTIs were identified and included in the study. The majority were men (52, 67.5%) and non-Hispanic Caucasian (68, 88.3%). Twenty-three (23, 31%) were overweight. The most common comorbidities were coronary artery disease (38, 50%) and diabetes mellitus (33, 43%), and the vast majority (67, 88.1%) had altered mobility (67, 88.1%), spent time in the intensive care unit (64, 84.2%), and were incontinent (64, 84.2%). The most common areas involved were the sacrum (51, 39.8%) and the heel/Achilles region (37, 28.9%). Maroon-purple discoloration of intact skin was the most commonly documented presentation (115 ulcers, 89.9%). Average length of follow-up was 6 days (range 1 day to 14 weeks). At the final assessment, 85 sDTIs (66.4%) completely resolved or were progressing toward resolution, 31 remained unchanged and were still documented as purple-maroon discoloration or a blood-filled blister, and deterioration to full-thickness tissue loss occurred in 12 (9.3%). These observations may offer important insights into the evolution of sDTIs. Research is needed to identify sDTI risk factors and most effective protocols of care.

 Potential Conflicts of Interest: none disclosed

Introduction

  Pressure ulcers result in devastating emotional, financial, and medical consequences for patients. Each year, more than 2.5 million US patients develop pressure ulcers. More patients develop pressure ulcers than cancer.1 Pressure ulcers often result in pain, impede return to full functioning, and are directly associated with an extended length of stay, sepsis, and increased mortality.2,3 The length of hospitalization for pressure ulcers is nearly three times longer than hospitalization without a pressure ulcer diagnosis; nearly 60,000 US hospital patients die each year from complications due to hospital-acquired pressure ulcers.1

  The cost associated with pressure ulcers, especially those that advance to substantial tissue loss, puts a strain on healthcare facilities and the healthcare industry as a whole. The annual cost of pressure ulcers in the US ranges from $9.1 billion to $11.6 billion.1 The average cost to treat an individual with a suspected deep tissue injury (sDTI) pressure ulcer is an estimated $43,180 but can exceed $100,000 if the ulcer progresses to a Stage III or Stage IV.3,4 In addition to direct costs, pressure ulcers result in more than 17,000 lawsuits and are the second most common claim for wrongful death.1

  According to an actuarial analysis that examined medical claims from January 1, 2000 to September 30, 2008,5 pressure ulcers are the number one preventable medical error. The Centers for Medicare and Medicaid Services (CMS) consider Stage III and Stage IV pressure ulcers acquired after admission to a healthcare facility or hospital-acquired pressure ulcers (HAPUs) “never events.” The CMS asserts that Stage III and Stage IV pressure ulcers should never occur because they can be reasonably prevented by applying evidence-based guidelines for care. Consequently, the CMS halted healthcare reimbursement of HAPUs as of October 2008. This offered an additional incentive for hospitals to prevent pressure ulcers from occurring and to prevent deterioration of those present on admission.

  Results of a 2010 demographic analysis6 show that the proportion of sDTIs is 9% of all ulcers in 2009; they are more prevalent than either Stage III or Stage IV ulcers. Based on the consensus statement from the National Pressure Ulcer Advisory Panel (NPUAP),7 the prevailing sDTI presentation in the clinical setting has been evolution from purple or maroon discoloration of intact skin to a thin blister over a dark wound bed, thin eschar, and often rapid deterioration to expose the deeper tissue layers, even with optimal treatment. With increased sDTI incidence comes the increased potential for tissue destruction and resultant complications.4 However, as recently as February 2013, more than 200 wound care providers and industry experts in attendance at the NPUAP sDTI Consensus Conference could not reach a consensus regarding the pathophysiology and natural history of sDTI. The difficulty in interrupting the evolution of sDTI is likely the result of a relatively small body of knowledge surrounding this complex yet poorly understood phenomenon.

Literature Review

  The presentation of deep tissue injury is represented in the literature as early as 1873 when Sir James Paget described purple areas of intact skin that sloughed and evolved into cavities.8 However, in 2013 clinical data on this ulcer type remain sparse. In an effort to better understand the history, etiology, and clinical presentation of sDTI and to prevent the duplication of evidence, a literature search was performed. A research request was generated with key words from the research population (P), intervention (I), comparison (C) and outcome(s) (O) (PICO) question, “In adult hospitalized patients, does a common evolutionary pattern exist for sDTI pressure ulcers that can be used to drive early intervention, treatment, and reimbursement?” CINAHL, Medline, and Scopus were searched for articles published within the last 5 years, yielding 35 sources, but only four related directly to sDTI pressure ulcers in adult hospitalized patients. In light of minimal evidence, a second search was generated using the term intra-operative pressure ulcer, because these ulcers generally present as sDTI ulcers. The second search yielded seven results and no relevant information. In addition, a general search was initiated for articles relevant to pressure ulcer incidence, cost, and impact.2,3,9-11 For this search, the terms cost of pressure ulcers and cost of suspected deep tissue injury were used. No time frame was specified for the second and third searches.

  All abstracts and guidelines were assessed for relevance to the research question by the primary investigator (PI), who is credentialed through the Wound, Ostomy, Continence Nurse Society Certification Board as a Certified Wound Ostomy Nurse. Articles not relevant to the research question or to sDTI pressure ulcers in adult hospitalized patients were excluded. Standardized appraisal forms were used for relevant articles, and the strength of the evidence was appraised using Melnyk’s and Fineout-Overholt’s (2005) criteria.12 Melnyk’s criterion is an evidence categorization model that includes seven levels of evidence rated from strongest to weakest. The stronger the evidence, the higher the likelihood it is valid and relevant for a particular clinical situation. The strength of the quality improvement (QI) evidence was subjectively determined.

  All four articles relevant to sDTI pressure ulcers in adult, hospitalized patients were reviewed in detail. They included three Level IV, quantitative, case-controlled and cohort studies8,13,14 and one qualitative Level I research study, a meta-analysis of all relevant randomized, controlled trials (RCTs).15 Only one of the four relevant articles related directly to the proposed research topic of evolution of sDTI pressure ulcers in adult hospitalized patients; unfortunately, this descriptive study by Richbourg et al8 was unsuccessful at identifying a pattern of evolution.

Study Purpose

  The principal goal of this study was to increase understanding of the evolution of sDTI as a catalyst for improved patient outcomes and to examine the potential role of early identification and intervention in preventing deterioration and minimizing tissue destruction.

  In light of the absence of robust evidence related to sDTI pressure ulcers, this study was designed to answer the following questions: 1) Does a common pattern of evolution exist for sDTI pressure ulcers? 2) Do commonalities in contributing risks and comorbidities exist among patients with sDTI pressure ulcers? 3) Can the evolution of sDTI pressure ulcers be interrupted and tissue damage minimized through early intervention?

Methods

  Setting. Study procedures for this 24-month, single-site, retrospective study were approved by the Institutional Review Board (IRB) and the EBP (Evidence-Based Practice) Nursing Research Council at Mayo Clinic. The study setting was an acute care health facility where wound, ostomy, continence (WOC) nurses perform consultative services for patients with pressure ulcers. Patterns of evolution were assessed, and progression of the ulcer was determined by comparing findings, including wound measurements, on the initial presentation to the same variables at each ulcer’s endpoint

.   Participants and wounds. Inclusion criteria were hospitalized, adult patients, 18 years or older, with a sDTI pressure ulcer confirmed by the WOC nurse. There were no exclusions; patients meeting the inclusion criteria were identified from a pre-existing database. NPUAP pressure ulcer staging guidelines were used as a basis for sDTI identification. The NPUAP7 defines a sDTI pressure ulcer as a “purple or maroon localized area of discolored intact skin or blood-filled blister due to damage of underlying soft tissue from pressure and/or shear. The area may be preceded by tissue that is painful, firm, mushy, boggy, warmer, or cooler as compared to adjacent tissue. Deep tissue injury may be difficult to detect in individuals with dark skin tones. Evolution may include a thin blister over a dark wound bed. The wound may further evolve and become covered by thin eschar. Evolution may be rapid, exposing additional layers of tissue even with optimal treatment.”

  Procedure. An existing list of all current and previous WOC team patients was used to identify patients with a sDTI pressure ulcer within the approved research period of March 2010 through March 2012. This list was reviewed based on study inclusion-exclusion criteria. Retrospective chart reviews of WOC nurse-treated sDTI pressure ulcers were completed by the PI. WOC nurse notes were utilized to identify ulcer specifics for all ulcers and included ulcer stage, wound bed characteristics, wound measurements (length [l] x width [w] x depth), ulcer location, presentation, tissue color and consistency, and treatment at each encounter. These variables were abstracted to document the progression of each sDTI for all hospitalized patients with a sDTI pressure ulcer treated in the study time frame. All participants received appropriate pressure ulcer bundle interventions that included patient education, soft-silicone foam dressings for both prevention and treatment as appropriate, timely WOC nurse consultations, and patient-specific pressure redistribution interventions derived from a standardized Mayo Clinic formulary of evidence-based modalities. Soft-silicone foam dressings were used as either primary or secondary dressings depending on ulcer treatment goals. Offloading or barrier cream was used either in combination with soft-silicone dressings or when dressings could not be maintained. Other primary treatments consisted of honey-infused dressings and hypochlorite solution 1.5%, which was used when debridement of necrosis was indicated and/or infection was suspected. Hydrofiber dressings were used when additional moisture management was indicated beyond that provided by the soft-silicone dressing.

  sDTI evolution was assessed based on the appearance of the ulcer upon presentation and at each encounter thereafter; specifically, the nurse assessed purple or maroon discoloration of intact skin, a blood-filled blister, the development of a darker (dark gray, brown, black) discoloration of intact skin, necrosis, or a break in the skin. Healing was analyzed based on the ulcer specifics during the initial WOC nurse assessment compared to the WOC nurse assessment at each ulcer’s endpoint until WOC nurse sign off or discharge from the medical facility.

  Data collection. The data collection tool was developed by the PI and validated through consensus by the Institutional EBP Nursing Research Council. During several meetings with the EBP Nursing Research Council, the findings of the literature review, research goals, and timelines were discussed and revised as needed.

  Patient demographics such as age, body mass index (BMI), and race also were abstracted. Contributing risks including altered mobility, hospitalization in the ICU, incontinence, surgery within seven (7) days of ulcer formation, obesity/overweight, death during the study period, transplantation, malnutrition, smoking, and paraplegia or quadriplegia and relevant comorbidities including coronary artery disease (CAD), diabetes mellitus, renal disease, liver disease, cancer, dementia, peripheral vascular/arterial disease, stroke, and orthopedic deformities were abstracted and evaluated for commonalities. All patient identifiers were removed from the data collection tools. All data were entered into an Excel spreadsheet and analyzed by the PI, who evaluated each ulcer individually based on size and tissue consistency on presentation and at the conclusion of the WOC nurse visits for that ulcer. The WOC nurse assessment was used in lieu of the nursing assessment to increase the probability that normal hyperpigmentation would be clearly distinguished from purple or maroon discoloration of the skin. Not all ulcers were assessed during each WOC nurse encounter, but all ulcers included in the data had at least two WOC nurse assessments: an initial encounter and at least one follow-up encounter.

  Data analysis. Descriptive statistics were used to summarize continuous variables such as age, race, BMI, contributing factors, comorbid conditions, and treatment. Observational data were used to identify patterns of evolution. The percentage of change in size for each ulcer was determined utilizing the following standard formula:

    SAI (initial surface area) - SAC (endpoint surface area) x 100 = % of change
    SAC

Results

  A target sample size of at least 100 ulcers was achieved and the final sample consisted of 122 patients. Of those, 45 were excluded from analysis due to incomplete data (13), evolution on initial presentation (two), and loss of follow-up (30). The remaining 77 patients had a total of 128 sDTIs. Patients were evaluated by the WOC nurse for 1 day to 14 weeks, yielding a sample of 377 encounters with a median follow-up time of 6 days.

  Average participant age was 67.5 (range 32–91) years old. sDTIs were more prevalent in men (52, 67.5%) than women (25, 32.4%) and in non-Hispanic Caucasian patients (68, 88.3%) compared to African American (six, 7.7%), Hispanic (one, 1.2%), Asian (one, 1.2%), and other (one, 1.2%) (see Table 1).

  The primary comorbid condition among this sample was CAD (38, 50%), followed by diabetes mellitus (33, 43%). These comorbidities exceeded known contributors to altered mobility and ultimately pressure ulcer development, including neurological diseases such as dementia (12, 15.7%) and stroke (eight, 10.5%). The most prevalent contributing factors were altered mobility (67, 88.1%), time in the ICU (64, 84.2%), and incontinence (64, 84.2%). Forty-six patients (46, 60.5%) had undergone surgery within 7 days of sDTI presentation; 18 (23.6%) patients were post organ transplant. Average BMI was 27.2 (overweight), ranging from 13.4 (underweight) to 51.8 (obese class III). Forty-six patients (46, 59%) were overweight or obese. The most common site of sDTI was the sacrum (51, 39.8%), followed by the heel/Achilles region (37, 28.9%). The most common presentation of the sDTI (115, 89.8%) was a purple-maroon discoloration. Sixty-six patients (66, 85.7%) were on a low-air-loss support surface, and the remaining patients were on pressure-redistributing foam.

  Follow-up assessments. During the study period, WOC nurse assessments occurred once or twice weekly depending on the condition of the ulcer, with a median time for WOC nurse follow-up of 6 days (range 1–41 days), for a total of 377 visits.

  No signs of evolution, as evidenced by a change in the ulcer appearance, including skin discoloration and/or tissue consistency, were observed in any of the ulcers before day 4. At day 4, 46 of the 128 sDTIs were re-evaluated and 24 ulcers had resolved. Resolution was represented by the presence of intact skin and absence of any skin discoloration, including erythema. At day 4, five ulcers were progressing toward resolution, which was represented by Stage II, Stage I, and blanchable redness. This finding suggests that not all sDTI pressure ulcers represent full-thickness tissue loss. At day 4, eight ulcers had developed eschar or slough necrosis and two had developed a break in the skin. Of the 46 ulcers assessed on day 4, seven remained unchanged (see Table 2 and Table 3).

  Continuing patterns of evolution were observed. Purple or maroon discoloration of intact skin or a blood-filled blister was noted in WOC nurse assessments for up to 4 weeks in 70 ulcers. Granulation tissue formation occurred in one ulcer and was not observed until week 6. Necrosis presented as early as day 4 but persisted as long as 13 weeks. Two ulcers took up to 13 weeks to completely resolve. One sDTI, evolved to unstageable, was debrided to a Stage III, and required a surgical flap to achieve complete closure.

  At the end of the follow-up, 31 (24.2%) of the sDTIs remained unchanged and were still documented as purple-maroon discoloration or a blood-filled blister. Deterioration to full-thickness tissue loss occurred in 12 (9.3%) sDTIs as indicated by documentation of unstageable, Stage III, or Stage IV pressure ulcers. Progression toward resolution was noted in 85 sDTIs (66.4%) as indicated by WOC nurse documentation of blanchable redness, Stage I, Stage II, scabbing, or complete resolution. This progression from sDTI to a Stage I or Stage II pressure ulcer is considered healing because of the established notion that the purple discoloration associated with sDTI commonly represents deep tissue ischemia and destruction. Conversely, the progression from sDTI to a Stage I or Stage II challenges this theory. Blanchable redness, though not a pressure ulcer according to the NPUAP, was included because it warranted differentiation from complete resolution in which there were no signs of pressure. Scabbing was included in progressing to resolution because it is the result of friction and indicative of a superficial skin injury. Taking into account each individual ulcer’s endpoint, which was represented by the last available WOCN assessment for each ulcer, 48 sDTIs (37.5%) completely resolved and 37 (28.9%) were progressing toward resolution, for a total of 85 (66.4%) sDTI ulcers.

  At the study site, all pressure ulcers regardless of stage are measured at each encounter. The 128 ulcers ranged in size (l x w) from 0.5 cm x 0.4 cm to 13 cm x 15 cm taking into account all available measurements at all encounters. Depths of the 128 ulcers ranged from 0.1 cm to 1.6 cm taking into account all available depths at all encounters. Three ulcers were excluded from this assessment due to the absence of measurements. Assessment of wound measurements of each ulcer’s endpoint demonstrated that 93 (74%) decreased in size or resolved. The 48 ulcers that decreased in size ranged from 0.5 cm x 0.5 cm with a healing rate of 20% to 13 cm x 15 cm with a healing rate of 69%. The median healing percentage for the 48 ulcers was 61%. The 45 ulcers that completely resolved ranged in size from 0.5 cm x 0.5 cm to 10.5 cm x 15 cm. Twelve (12) sDTIs (9.6%) had no change in size and ranged from 1.2 cm x 1 cm to 9 cm x 7 cm. Twenty (20, 16%) increased in size and ranged from 0.5 cm x 0.4 cm with a surface increase of 96% to 13 cm x 10.5 cm with a surface increase of 10%. The median surface increase for all 45 ulcers was 68%.

Discussion

  The phenomenon of sDTI has only recently been described and defined. Hence, there is very little research to validate the definition, document incidence and prevalence, or help clinicians understand how to best manage this phenomenon. The purpose of this study was to uncover whether a common pattern of evolution exists; what, if anything patients with a sDTI have in common; and if further tissue damage (skin breakdown) can be prevented.

  Consistent with the findings of the descriptive study by Richbourg,8 this study was unable to clearly delineate a consistent pattern of evolution. However, this study was able to identify time frames where evolution begins, resolution occurs, and progression to a break in the skin, necrosis, and granulation may develop. The Richbourg study demonstrated considerable deterioration (26% evolved to full-thickness lesions and 17% evolved to unstageable lesions) and minimal resolution, with only 5% of ulcers resolving. In contrast to those findings, the current study demonstrated minimal deterioration and considerable resolution. Of the 128 sDTIs observed, only one deteriorated to a Stage III; 85 (66.4%) resolved or were resolving at the conclusion of the study period, and only 12 (9.3%) deteriorated. Despite sizeable differences in sDTI outcomes, both study sites utilized evidence-based preventive care and both studies demonstrated the possibility that preventive care may be effective for many sDTI lesions. Because no published data are available for comparison and little is known about their pattern of evolution, it is not known whether the facility’s protocol of care is particularly effective or if most DTIs resolve. Additional research is needed to determine the direct influence of aggressive intervention on the progression of sDTIs to Stage III or Stage IV, but the results of this study are encouraging.

  In this group of patients, early identification and intervention may have stopped sDTI development into Stage III or Stage IV ulcers. The pressure ulcer bundle, a formulary of evidence-based pressure ulcer prevention interventions, was developed following an extensive, multiyear evaluation of the evidence and best practice. The bundle is automated within an electronic medical record (EMR). To induce compliance with the established evidence-based pressure ulcer prevention guidelines, the EMR sends a task to the bedside nurse for Braden subscale scores of 2 or less. This task remains in effect until the nurse selects individualized pressure ulcer prevention interventions from the established formulary. This facilitates timely initiation of an individualized plan of care, empowers the nurse to take an active role in the pressure ulcer prevention, and standardizes care. Automation of the pressure ulcer bundle may have played an important role in early identification, appropriate intervention, and evoking compliance with the established standard of practice.

  Observational data derived from evaluation of each ulcer at each encounter showed two main patterns of evolution with regard to size. One common presentation was a decrease in size as the ulcer evolved toward necrosis. Another frequent presentation was an increase in size as the ulcer evolved from purple to maroon discoloration or nonblanchable redness. However, these observations did not occur in all patients, suggesting that the evolution of DTIs is somewhat unpredictable and warranting frequent re-evaluation and early intervention as appropriate based on the presentation at each encounter. In the current study, it was noted that changes in the appearance of the DTI generally started to occur 4 days following the initial consult and assessment. Unfortunately, the potential time lapsed between initial presentation and the WOC nurse consult makes determining the actual timeframes for evolution difficult to definitively discern. Gefen15 suggests that pressure ulcers in subdermal tissue under bony prominences very likely occur between the first hour and 4 to 6 hours after sustained loading.

  Another important observation was that 35 (45.4%) of the patients in this study expired within 2 years of their sDTI development. At the study site, persons often present with a multitude of comorbid conditions, making it difficult to clearly delineate whether their medical status contributed to sDTI development or whether the sDTI is an indicator of their deteriorated health status. Although none of the deaths at the study site was directly related to the sDTI, the presence of pressure ulcers may contribute to premature mortality in some patients.16 In the Agency for Healthcare Research and Quality’s Healthcare Cost and Utilization Project17 which consisted of an analysis of 503,300 pressure ulcer-related hospitalizations in 2006, approximately one in 25 admissions involving pressure ulcers as a primary diagnosis ended in death, and the death rate was higher when pressure ulcers were a secondary diagnosis, approximately one in eight cases. This increased risk of mortality associated with pressure ulcer development and the potential for rapid deterioration and substantial tissue loss associated with sDTI pressure ulcers places urgency on the need for a better understanding of the sDTI phenomenon, including etiology, prevention, and treatment.

Limitations

  The small sample size and study design limit the ability to generalize findings to all patients with sDTI. The WOC nurse saw the patient only after the sDTI was identified by staff and a consult was generated. Therefore, the role of potentially delayed identification and intervention cannot be elucidated. Some ulcers already were in the evolution process at the initial WOC nurse assessment as evidenced by dark discoloration and eschar formation within the purple discoloration. sDTI may be difficult to detect in individuals with dark skin tones,7 resulting in variability in staging and other assessment findings. This variability was observed despite the expertise of the WOC nurse staff whose assessments were the foundation of this research. The shorter length of stay for acute care patients limited the degree to which follow-up encounters were available. The study endpoint was limited by the length of stay and/or the degree to which WOC nurse assessments were available.

Conclusion

  This study sought to determine if a common pattern of evolution exists for sDTI pressure ulcers, to explore the impact of contributing risks and comorbid conditions, and to evaluate the feasibility of inhibiting sDTI evolution to Stage III and Stage IV through early intervention. The data showed the vast majority of these ulcers, managed using a standard protocol of supportive and topical care, resolved without deteriorating into Stage II, Stage III, or Stage IV pressure ulcers. This seems to suggest early identification and intervention may help prevent the deterioration of a sDTI and lead to better outcomes for patients.

  This study also confirms that, although not in a large percentage of cases, sDTI can progress to a Stage III or Stage IV ulcer as described in the NPUAP definition. More research is needed to delineate which patients and ulcers are most at risk for this deterioration and best practice for intervening and/or recovering injured tissue.

Dr. Sullivan is a Certified Wound-Ostomy Nurse, Mayo Clinic-Florida Campus, Jacksonville, FL. Please address correspondence to: Rhonda Sullivan, PhD, RN, CWON, LNCC, Mayo Clinic-Florida Campus, 4500 San Pablo Road, Jacksonville, FL 32224; email: sullivan.rhonda@mayo.edu.

References: 

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2. Lyder CH, Ayello EA. Pressure ulcers: a patient safety issue. In: Hughes RG (ed). Patient Safety and Quality: An Evidence-based Handbook for Nurses. Agency for Healthcare Research and Quality (AHRQ). Rockville, MD: AHRQ Publication No. 08-0043. 2008.

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9. Russo CA, Steiner C, Spector W. Hospitalizations Related to Pressure Ulcers among Adults 18 Years and Older, 2006. HCUP Statistical Brief 64. Agency for Healthcare Research and Quality. Available at: www.hcup-us.ahrq.gov/reports/statbriefs/sb64.pdf. Accessed January 6, 2012.

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11. Reddy M, Gill SS, Rochon PA. Preventing pressure ulcers: a systematic review. JAMA. 2006;296(8):974–984.

12. Melynk BM and Fineout-Overholt E. Evidence-Based Practice in Nursing & Healthcare: A Guide to Best Practice. Philadelphia, PA: Lippincott, Williams& Wilkins. Retrieved from Mayo Clinic Intranet: http://mayoweb.edu/nur-ebp/process3-hierarchy.html. Accessed February 6, 2012.

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14. Ohura T, Ohura N, Oka H. Incidence of clinical symptoms of hourglass and sandwich-shaped tissue necrosis in Stage IV pressure ulcers. WOUNDS. 2007;19(11):310–319.

15. Gefen A. How much time does it take to get a pressure ulcer? Integrated evidence from human, animal, and in vitro studies. Ostomy Wound Manage. 2008;54(10):26–35.

16. Ayello EA. Changing systems, changing cultures: reducing pressure ulcers in hospitals. Jt Comm J Qual Patient Saf. 2011;37(3):120–122.

17. Agency for Healthcare Research and Quality. Pressure Ulcers Are Increasing Among Hospital Patients. Available at: www.ahrq.gov/research/jan09/0109RA22.htm. Accessed November 6, 2012. 

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