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Empirical Studies

The Development and Content Validation of a Multidisciplinary, Evidence-based Wound Infection Prevention and Treatment Guideline

Abstract

Acute and chronic wound infections create clinical, economic, and patient-centered challenges best met by multidisciplinary wound care teams providing consistent, valid, clinically relevant, safe, evidence-based management across settings. To develop an evidence-based wound infection guideline, PubMed, Cochrane Library, and Cumulative Index to Nursing and Allied Health Literature databases were searched from inception through August 1, 2017 using the terms (or synonyms) wound infection and risk factor, significant, diagnosis, prevention, treatment, or surveillance.Studies on parasitic infections, in vitro studies, and non-English publications were excluded. The 19-member International Consolidated Wound Infection Guideline Task Force (ICWIG TF), hosted by the Association for the Advancement of Wound Care (AAWC), reviewed publications/assessed levels of evidence, developed recommendations, and verified representation of all major recommendations from 27 multidisciplinary wound infection documents. Using a web-based survey, practitioners were invited to assess the clinical relevance and strength of each recommendation using standardized scores. Survey responses from 42 practitioners, including registered nurses (RNs), Wound Care Certified and advanced practice RNs, physical therapists, physicians, podiatrists, and scientists from 6 countries were returned to AAWC staff, tabulated in a spreadsheet, and analyzed for content validity. Respondents had a median of >15 years of military or civilian practice and managed an average of 15.9 ± 23 patients with infected wounds per week. Recommendations supported by strong evidence and/or content validated as relevant by at least 75% of respondents qualified for guideline inclusion. Most (159, 88.8%) of the 179 ICWIG recommendations met these criteria and were summarized as a checklist to harmonize team wound infection management across specialties and settings. Most of the 20 recommendations found not to be valid were related to the use of antibiotics and antiseptics. After final ICWIG TF review of best evidence supporting each recommendation, the guideline will be published on the AAWC website. 

Introduction

Surgical site infection (SSI) increases patient mortality by up to 3%1,2 and prolongs postsurgical hospital stays by 7 to 10 days,1,3 raising related costs by $20 000 to $27 600 per United States hospital admission.3 For US hospital inpatients, SSIs are the most common health care-associated infections currently monitored by the Centers for Disease Control and Prevention (CDC) National Healthcare Safety Network (NHSN); SSIs represent 31% of the total number of infections,with incidence rising in the last 10 years from 2% to 5% in 2016.4-7 In low and middle-income countries, the burden of SSI is much higher.8 

Although these statistics are alarming and merit the rigorous efforts (underway) to reduce SSI, they are only part of the wound infection story. Infections are just as likely in nonsurgical wounds, with rates increasing with population age. Estimates of wound infection incidence vary among settings and countries that use differing criteria and reporting systems, highlighting the need for increased consistency of infection diagnosis, definitions, and surveillance recording tools.9-12 A prospective SSI surveillance survey, standardized to CDC criteria,13 reported that 28% of SSIs occurred during the hospital stay for 1324 patients undergoing coronary artery bypass grafts; the remaining 72% of SSIs were reported when SSI surveillance was extended to 30 days post-discharge.14 This finding suggests the need for community-based surveillance for all acute and chronic wounds across all care settings. To explore this issue, focused literature searches were conducted of the MEDLINE database from inception to June, 2017, addressing the topic wound infection incidence for each wound type listed in Table 1. Example studies cited included registries, meta-analyses, or clinical trials reporting 100 or more patients.14-28 Diabetic foot ulcers, burns, and pressure ulcers all have higher reported infection incidence than clean/contaminated surgical wounds. However, the only chronic wound subject to CDC NHSN standardized infection surveillance4 is the “decubitus ulcer” (ie, pressure injury). It remains to be explored whether parallel standardized surveillance and feedback programs for nonsurgical wound infections may improve chronic wound, burn wound, or trauma wound infection outcomes. 

Acute and chronic wound infection similarities. Most definitions of chronic or acute surgical, trauma, or burn wound infection include 2 or more of the classic clinical signs and symptoms of infection (ie, increased tenderness or pain, local heat, erythema, edema, or purulent or excessive drainage4,29-32), although wound infection is not recognized as a primary outcome for clinical trials.30,33 Also, the wording of the SSI criterion “dehiscence and separation of surgical wound edges”34 is applied to chronic wounds when stated as, “unexplained chronic wound breakdown despite addressing all causative host or environmental factors.”35 These criteria demonstrate potential for harmonizing acute and chronic wound infection measurement. 

Infection depth classification differs somewhat between chronic and acute wounds. SSI is classified by depth of infected tissue and noted as superficial incisional, deep incisional, and organ space.4 Chronic wound infections may use these criteria or report the level of tissue involvement as partial-thickness or full-thickness or involving underlying tendon, joint, or bone.9 To support risk-adjusted SSI surveillance in its National Nosocomial Infection Surveillance Risk Index,4 the CDC classifies surgeries according to wound contamination level, severity of patient systemic disease, and duration of surgery, adding 1 risk point on a 0 to 3 scale for each of the following: 1) the wound is contaminated or dirty-infected, 2) the patient has severe systemic disease, and 3) the surgery lasted longer than 75% of the average duration for that surgical procedure.36 Margolis et al37 have validated a risk scale for chronic venous ulcer delayed healing based on “wound duration >6 months” that parallels the third qualification for wound infection risk, but parallels between chronic and acute wound infection risk classification remain unclear.

Acute and chronic wound parallel management strategies. Preventing and treating wound infection requires management of patient, environmental, and microbial infection risk factors.38,39 Typically, wound infection, identified using clinical signs, is confirmed by microbial culture and sensitivity testing and leukocytosis.40,41 Although these signs vary subtly with wound etiology,40,41 chronic and acute surgical, burn, or trauma wounds typically are diagnosed by at least 2 of the 5 common signs and symptoms of wound infection.41-43 Life-threatening situations are exceptions to the “culture only if infected” rule. These include necrotizing fasciitis, for which standard therapy involves immediate, high-dosage, broad-spectrum antibiotics followed by life-saving surgery and subsequent narrow-spectrum antibiotics focused on microbes identified from appropriately cultured involved tissue. Similar procedures are followed for patients with large burn wounds because of the elevated infection/sepsis risk and resulting need for preventing potentially lethal infection.38,39 

Although validating research is needed, the parallels noted  in chronic and acute wound infection burdens, definitions, risk classification schema, and outcome measures signal opportunities to harmonize diagnostic language, practice, and outcome measures by multidisciplinary wound care teams as they manage patients with various acute or chronic wound infections across settings. The purpose of this work was to describe derivation from published literature and content validation of a set of wound infection diagnosis, prevention, and treatment recommendations to serve multidisciplinary wound care teams as they manage patients with acute or chronic wounds across settings. 

Methods

To identify evidence-based wound infection management recommendations from structured systematic literature searches, 19 multidisciplinary wound care professional members of the Association for the Advancement of Wound Care (AAWC, the host society), the Wound Healing Society, the Canadian Association for Enterostomal Therapy, and the Mexican Wound Healing Society (AMCICHAC) collaborating as part of the International Consolidated Wound Infection Guideline Task Force (ICWIG TF) explored barriers to evidence-based wound infection practice; conducted structured literature searches to identify evidence supporting recommendations for wound infection diagnosis, prevention, and treatment; evaluated each recommendation’s multidisciplinary construct validity; and content-validated clinical relevance and strength of recommendation (SOR), described as benefit-to-harm derived from implementing the recommendation.

Exploring evidence-based practice barriers. Many simple, low-cost techniques have been known for decades to prevent SSIs.1 These include hand washing,7,8 preoperative clipping rather than shaving hair from the surgical site,8,44 using a sterile swab to remove subincision fluid postoperatively until drainage subsides,45 and avoiding gauze-type topical acute or chronic wound dressings.46-48 Despite ample evidence, research that includes a review of microbiologic diagnostic procedures for chronic wounds in Germany,49 a 7-week observational study of elective pediatric surgical cases at a US hospital,50 and a qualitative thematic analysis of institutional tools and protocols and transcripts of interviews with infection control supervisors at 7 Canadian hospitals51 shows guideline interventions for reducing chances of wound infection are inconsistently used. 

To address this inconsistency of use, ICWIG TF members used brainstorming based on their experience to identify reasons for gaps between science and practice. In the course of their discussions, they realized that reducing wound infections would be feasible only if concerns and practices of each professional specialty involved in managing wound infection across settings were adequately served. As such, the ICWIG TF resolved to examine the construct validity of all evidence-based wound infection recommendations found in structured literature searches to ensure each final recommendation also was congruent with wound infection guidelines previously developed by individual specialties, such as infectious disease, dermatology, surgical, advanced practice nursing, or other specialists or by organizations devoted to specialized settings, such as acute care, home care, or military settings.

Literature review. Using recognized guideline development processes,52,53 the 19 members (ie, physicians, nursing professionals, and related doctoral candidates) of the ICWIG TF searched PubMed, Cochrane Library, and the Cumulative Index to Nursing and Allied Health Literature (CINAHL) databases from inception through November 30, 2013, including up to 400 of the most recent English publications using the search term wound infection combined with the search terms or synonyms risk factor, significant, diagnosis, prevention, treatment, or surveillance. Auxiliary related searches were conducted in Google Scholar to obtain full text and to expand evidence on specific recommendations as needed. Studies on parasitic infections or in vitro studies were excluded. The final step of selecting best available evidence from these and added searches supporting each ICWIG recommendation according to standardized criteria (listed in Table 2) was ongoing at the time of this publication. 

Interdisciplinary relevance and construct validity. To ensure interdisciplinary ICWIG relevance for all specialties managing wound infection across all settings, ICWIG TF members verified that all unique major recommendations from 21 post-2000, interdisciplinary wound infection reviews, position papers, or guidelines were addressed by ICWIG recommendations identified by evidence found in the literature searches. Additionally, they evaluated each ICWIG recommendation’s construct validity by checking “Yes” if it was included in at least 1 interdisciplinary post-2000 wound infection guideline or review or “No” if not. Ensuring consistency with published interdisciplinary guidelines, reviews, and position papers of all ICWIG wound infection recommendations addressed Institute of Medicine (IOM) criteria52 for developing trustworthy guidelines while supporting each ICWIG recommendation’s capacity to harmonize wound infection practices for all members of interdisciplinary wound care teams across settings and specialties. 

Content validation. ICWIG developers abstracted recommendations from evidence found in the initial literature searches, removed redundancy, and condensed all recommendations into a comprehensive list of 179 actionable recommendations. To ensure interdisciplinary clinical relevance of these recommendations, formal content validity54,55 was established by voluntary respondents to an online survey using judgment quantification to rate each recommendation’s clinical relevance on the 4-point scale shown in Table 2. Safety was estimated as SOR by each respondent rating the recommendation as “1” if more benefit than harm would be derived by implementing the recommendation or “0” if not as recommended by the IOM.52 Private ratings avoided potential bias from social pressures associated with consensus discussions. The content validation survey of recommendations compiled through November 30, 2013 was accessible online from December 1, 2013 through December 31, 2014. Invitations to complete the survey were published in major wound journals serving >40 000 readers and sent as eblasts to >5000 members of wound care societies in the United States, Europe, Asia, Australia, Canada, and Mexico. 

Respondents downloaded the survey, completed it on their computers, then emailed the completed survey to an AAWC staff member who compiled all surveys into an Excel file for later analysis by an ICWIG TF member. In addition to the ratings described, the survey requested respondent credentials and practice demographics, along with their suggested changes or additions to the recommendations. 

Updated literature searches. After the survey, the ICWIG TF conducted updated literature searches of PubMed and Google Scholar databases from December 31, 2014 through August 1, 2017, for the term wound infection combined with synonyms or derivatives of the terms reliable, valid, and significant, plus appropriate key words in each recommendation. Best available evidence from these and the prior searches currently is being reviewed, evaluated according to criteria in Table 2, added as appropriate supporting evidence to corresponding ICWIG recommendations, and abstracted into ICWIG evidence tables describing study patients, interventions, comparators, design, and outcomes of each of up to 5 best references supporting an ICWIG recommendation. 

Updated interdisciplinary relevance and construct validity. The power of interdisciplinary teamwork in improving wound outcomes has been affirmed by expert consensus,9 randomized clinical trials,56 and longitudinal cohort studies.57,58 To ensure ICWIG interdisciplinary currency in empowering wound care team members to speak and act in harmony, ICWIG TF members evaluated a total of 27 interdisciplinary publications (literature reviews, position documents, or guidelines) to ensure 1) that each ICWIG recommendation was represented in at least 1 prior evidence-based published summary of wound infection recommendations, and 2) that every recommendation in these published summaries was addressed appropriately in the ICWIG. The construct validity check had been performed before the content validity survey for 21 publications59-80 and was repeated for 6 more recent publications accessed after completion of the last content validation survey.8,78,81-84 

Data analysis and statistical methods. Relevance and benefit (SOR) content validity indexes (CVI) were calculated for each recommendation from all surveys returned as the percent of respondents rating that recommendation as 3 (relevant but needs minor improvement) or 4 (relevant and succinct) to their own clinical practice. A CVI of at least 0.75 is considered as having content validity,55 calculated as follows:

Relevance CVI = (number of 3 ratings + number of 4 ratings)/total N responding for the recommendation. 

Benefit (SOR) validity was the percentage of respondents rating the recommendation’s implementation as 1 (beneficial) = (number of 1 ratings)/total N responding with a rating of 0 or 1 for the recommendation. 

A 1-page ICWIG Checklist was compiled of the guideline recommendations with the highest CVI and SOR ratings (>0.75) for patient and wound assessment to diagnose and manage wound infection risk factors, wound infection prevention, and treatment. 

In the final guideline (accessible at aawconline.org once best evidence is summarized and aligned with each recommendation), each recommendation will be displayed with its evidence rating from Table 2, up to its 5 best supporting references, CVI, and SOR.

Results

Barriers to evidence-based management. Current guidelines reviewed differed in clarity, stated professional roles and accountability, and criteria for SOR, resulting in credibility gaps between specialties and across settings. Team members agreed with prior research49-51 that evidence-based guideline interventions are inconsistently followed due to limited communication between specialties or across settings; confused perceptions about safety and efficacy of interventions such as timing of antibiotic use; and inadequate training, resources, or reimbursement. Patient and wound outcomes are not consistently measured and rarely tracked across settings, so wound professionals are rarely held accountable or receive feedback about the outcomes of their wound care.51 

It was concluded that an adequately developed,53 evidence-based wound infection guideline (ICWIG) meeting IOM standards for a trustworthy guideline52 designed to unify and serve all wound care team members and the patient with an acute or chronic wound would help resolve many barriers and subsequently enhance the consistency of care and outcomes for those at risk of or with a wound infection. 

Interdisciplinary validation. All ICWIG recommendations were represented in at least 1 prior publication of evidence-based wound infection recommendations and, conversely, all evidence-based recommendations in the 27 reviews or guidelines evaluated8,59-84 with different wound, specialty, or setting focus were represented in the ICWIG. Although these documents differed from each other in their recommendations (often due to their focus on a specific specialty or acute or chronic wound etiology), many commonalities were observed among recommendations for wound infection diagnosis, prevention, and treatment. 

Content validation. Forty-two (42) clinicians with a median of >15 years of military or civilian practice on wounds completed and returned the content validation survey. They included 12 registered nurses (RNs); 10 RNs certified in wound ostomy continence (WOC) care; 8 physical therapists; 7 advanced practice nurses; 4 physicians specializing in surgical, dermatologic, or endocrinological care; 4 doctors of podiatric medicine (DPMs); 3 (2 RNs and one MD) Certified Wound Specialists; 3 specialists with PhDs in microbiology or authors of peer-reviewed continuing medical education literature reviews on wound infection; and 1 PhD patient advocate. Several respondents had more than one credential.

These participants managed an average of ~16 wound infections per week. Participant practice settings included acute (inpatient) care (43%), separate wound clinic (25%), acute (outpatient) care (21%), long-term acute care (17%), skilled nursing facility (17%), office practice (15%), medical school (11%), subacute care (7%), home care (3%), or extended care (2%), with <1% of respondents in a group practice organization or government agency. Most of the participants’ practice time was devoted to surgical wounds (29%), pressure ulcers (27%), diabetic foot ulcers (23%), venous ulcers (15%), burn/trauma or other acute open wounds healing by secondary intention (10%), mixed etiology wounds (eg, venous and arterial ulcers) (9%), dermatologic conditions (5%), or other wounds (3%) such as cancer, fungating, or lymphedema wounds or other unusual wounds. Respondents practiced in Australia, Canada, Slovenia, Sweden, Switzerland, the United Kingdom, and 13 of the United States, representing all regions except Hawaii. 

Of the 179 recommendations, 159 (88%) were rated as relevant and recommended (CVI >0.75). Among the 179 recommendations, 82 (45.8%) had robust content validity with high relevance (CVI >0.90) and SOR >0.75. The 20 recommendations with the highest ratings focused mainly on consistent wound monitoring with feedback to care providers, avoiding contamination, and preventing tissue damage (see Table 3). Twenty (20) recommendations were judged to be of questionable relevance (CVI <0.75) and low SOR or not clearly beneficial in ratings from >75% of respondents (see Table 4). These recommendations mainly addressed the use of antibiotics or topical antimicrobial agents. 

Wound Infection Checklist. A Wound Infection Checklist containing ICWIG recommendations with CVI and SOR >0.75 was developed as an implementation tool to simplify ICWIG use by interdisciplinary wound care teams, including patients, families, and all care providers across settings (see Figure 1). The Checklist organized recommendations into 3 columns. The first column lists actions recommended to identify wound infection risk factors during patient and wound assessment and evaluation. The second column lists actions recommended to prevent acute or chronic wound infection. The third column lists actions recommended to manage patients with wounds until wound healing occurs. 

Discussion

To be useful and trustworthy for health care providers, a guideline requires clear, evidence-based, actionable recommendations with consistently defined parameters and measurable outcomes.52,53 Specialty-, setting-, or wound-related discrepancies among wound infection definitions, assessment, or diagnostic parameters and prevention or treatment interventions can confuse professional caregivers and reduce the consistency of management and quality of outcomes. For example, a provider with mainly acute wound experience may assume increased pain, erythema, and discharge of a venous ulcer signals infection and prescribe unneeded antibiotics. The same patient receiving care designed to harmonize multidisciplinary team members in addressing all host, environmental, and organism risk factors would receive prompt, appropriate referral(s) to identify and address more likely needs for improved compression, nourishment, or vascular perfusion to resolve the problem without increasing patient risk of developing antibiotic-resistant microbes. Using trustworthy, content-validated guidelines that harmonize wound care team communications and actions may avoid costly errors and improve patient outcomes. 

The literature reviewed documented an array of contradictions in wound infection management recommendations. Wound infection diagnostic criteria were varied and included clinical signs such as pain or increased discharge34 and deep tissue biopsy harboring >105 colony forming units.31 Despite commonalities in the evidence-generated recommendations, discrepancies were noted on how to diagnose, prevent, and treat wound infection.9,34,36,38 These differences signaled the need for a wound infection guideline that could unify interdisciplinary wound care teams. Until communication and actions related to wound infections are seamless across specialties and settings, patients with or at risk of developing a wound infection are unlikely to receive recognized benefits of consistent care and outcomes derived from interdisciplinary teams adhering to evidence-based practice and sharing information about wound progress.56,57 

Two (2) European Wound Management Association publications addressed multidisciplinary wound infection management,9,85 but the ICWIG literature review found no structured guidelines developed to meet IOM standards that fulfill that purpose. The ICWIG is designed to fill this void. Generally high CVI values for most recommendations’ relevance and SOR values reflecting safety supported the feasibility of developing such a guideline to harmonize wound infection management. This is underscored by the ICWIG’s congruence with prior guidelines for individual specialties and verifies its interdisciplinary functionality for acute and chronic wound infection diagnosis, risk management, prevention, and treatment. 

However, sufficient commonality was found among acute and chronic wound infection diagnosis, prevention, treatment, and published risk factors to enable development of many relevant, beneficial recommendations supporting most aspects of managing chronic and acute wound infections, such as those in the Checklist (see Figure 1). Highly relevant and beneficial recommendations spanned wound etiology, professional specialties, and settings. Wound experts from a variety of professions, settings, and countries almost universally agreed that increased wound pain and discharge are key signals of infection for both acute and chronic wounds and that consistently monitoring and measuring wound area would help multidisciplinary wound care teams improve the consistency and quality of care and outcomes for their patients with acute and/or chronic wounds across care settings. 

Acute and chronic wound infections share most of the common signs and symptoms and arise from the same interacting host, environmental, and organism risk factors. Microorganisms invade healthy tissue only when compromised host and environmental factors favor infection.9,38 Optimizing patient and wound infection outcomes takes a multidisciplinary team reinforcing each other’s work to manage all these risk factors for acute or chronic wounds across all settings.85 

Implications for Practice

The ICWIG Checklist (see Figure 1) summarizes the content-validated ICWIG recommendations with high SOR, and Table 5A and 5B illustrates measureable aspects of adherence to and outcomes derived from example recommendations. Researchers are continuing to compile newly published evidence to verify if all 179 recommendations represent good clinical practice and to identify which need more research. Twenty (20, 11.2%) recommendations were rated neither relevant nor beneficial by >75% of respondents and as such failed to meet acceptable standards of content validity (see Table 4), thus requiring careful consideration of available evidence and/or further research before use in clinical practice. 

Resolving barriers to evidence-based wound infection practice. Infection-related costs and reimbursement vary across settings, states, regions, or provinces and may drive care decisions toward least expensive gauze wound dressings despite RCT evidence that their use doubles infection rates.46-48 Encouraging use of or adequately reimbursing clearly defined,86 moisture-retentive dressings could encourage their timely and appropriate use, preventing costly wound infections. 

Highly relevant and beneficial guideline recommendations described in the ICWIG Checklist (see Figure 1) merit consistent use with reporting of adherence measures, documenting that the recommendation was followed, and measures of expected outcomes if the recommendation is followed, as illustrated in Table 5A and 5B. These illustrate how to customize ICWIG recommendations for use in institutional protocols, practice settings, or as quality measures for wound registries,87 informing all collaborating wound care team members what action was taken, when, and with what related outcomes. 

Ready access to evidence-based ICWIG recommendations embedded in implementation tools or electronic health records could alert a primary provider to the need for specialist referral or help a patient understand  importance of adhering to the plan of care. Hierarchical medical structure may obstruct team approaches to guideline use by promoting disputes instead of supporting team synergy and by limiting the authority of evidence users. Just as implementing wound infection prevention “bundles” has reduced SSI rates and costs,44 embedding key ICWIG recommendations in protocols and medical records could support a cost effective, mutually respectful team approach, reducing delays between assessments and interventions. Developing a wound infection guideline to harmonize multidisciplinary teams is a small first step. Only consistent ICWIG use and documentation can measure and find ways to enhance its potential to improve clinical and economic outcomes. 

It was not surprising that all recommendations in the 27 interdisciplinary guidelines and evidence-based position documents tested already were addressed in the ICWIG. All were based on the same evidence found in the ICWIG searches. This result supported the ICWIG’s comprehensive and interdisciplinary qualities. Ensuring that a guideline serves all wound care team members encourages a harmonized, team-based approach with timely referrals for wound infection diagnosis, prevention, or treatment by appropriate specialists applying their more detailed specialty evidence-based guidelines in time to optimize patient outcomes and reduce costs. 

The literature reviewed clarified what is known and not known about wound infection. The implication for practice is that it benefits patients to avoid infection harm and costs (reported in Table 1) by rigorously managing host and environmental factors to prevent wound infection; doing so before surgery or developing a chronic wound also can limit unnecessary use of antibiotics to address inflamed or non-healing wounds. 

Future ICWIG steps. The best 5 or fewer publications supporting each recommendation are currently being selected according to criteria listed in Table 2. The final ICWIG will feature each recommendation, CVI for clinical relevance and benefit, and up to 5 best available supporting references, plus an ICWIG Evidence Table summarizing those references and patient and professional implementation tools will be accessible at: aawconline.org/professional resources after ICWIG completion. 

Future ICWIG updates will continuously improve its capacity to inform clinical decisions related to wound infection and identify related research and education gaps. For now, need is evident for research and clarification of the recommendations in Table 4. Methods are needed to differentiate wound infection from other causes of inflammation with improved diagnostic and screening validity.88 It is time to answer questions regarding if/when to extract sutures or dressing fibers embedded in wounds89 and whether CDC rules for antibiotic prophylaxis apply to surgical debridement of chronic wounds and if so, how to avoid proliferation of drug-resistant microorganisms90 or delayed healing associated with prophylactic administration of antibiotics to uninfected chronic wounds.91 Harmonized care and collaborative research across specialties and settings should help answer these questions and improve consistency and quality of wound infection surveillance and outcomes as aging patients traverse settings with increasing frequency.

Among the strengths of this method of content-validating recommendation relevance and safety is that it replaces the social interactions of group consensus with independently expressed standardized ratings as a measure of the strength of opinion supporting the recommendation. Each professional with his/her own patients in mind contributes equally to the CVI, expressing the capacity of each recommendation to benefit (or harm) patients. This leaves little opportunity for the personal opinions of guideline developers to distort recommendations. 

Limitations

This report’s focus on harmonizing acute and chronic wound infection management is not intended to minimize the vital importance of emergency management of severe burns, trauma, necrotizing fasciitis, or other serious conditions that threaten immunologic competence or homeostasis. These require immediate, appropriate referral to and management by experts in life and limb salvage and wound infection management. Additional resources provide more information regarding management of these wounds.70,92 

The sample of 42 respondents to the ICWIG content validation survey appears small but is ample in comparison to the 5 or more independent reviewers required to establish formal content validity of a practice recommendation.55 Independence of respondents, the breadth and duration of their wound care practices, and the variety of civilian and military practice settings and wounds they managed support this survey as a robust content validation process with broad relevance. 

 The ICWIG still needs best available evidence supporting the efficacy and safety of each recommendation before it becomes an evidence-based guideline. This vital step, currently being completed, will allow assessment of research and educational gaps, while placing it among the ICGTF guidelines accessible at aawconline.com later this year as a multidisciplinary resource supporting content-validated science-based practice.

Multidisciplinary wound care teams improve the consistency and quality of care and outcomes for patients with wounds. Multinational ICWIG guideline developers searched wound infection literature, confirming the need to develop an interdisciplinary wound infection guideline to harmonize team wound infection management across specialties and settings. Literature reviews found 179 ICWIG recommendations informing decisions about acute and chronic wound infection risk factors, diagnostic criteria, and prevention and treatment interventions. Standardized independent ratings by 42 multidisciplinary online survey respondents supported content validity and SOR of 159 (88.8%) of the recommendations for clinical relevance and patient benefit. These were condensed into a Wound Infection Checklist designed to harmonize interdisciplinary teams practicing across settings to improve the consistency and quality of care and outcomes for patients with or at risk of chronic or acute wound infection.

Acknowledgement

The authors gratefully acknowledge the AAWC for supporting the teleconferences needed to develop ICWIG and the ICGTF collaborating organizations who helped develop ICWIG, as well as the thoughtful diligence of all 42 participants who completed the ICWIG content validation survey, for graciously sharing their time and expertise to benefit patients. In addition to the authors, the following ICWIG TF members selflessly donated considerable effort to conducting the literature searches and reviewing the results on which these wound infection clinical practice recommendations are based: Karen Bruton, RN, CETN(C), CAET Liaison; Vickie Driver, MS, DPM, FACFAS; Jerold Kaplan, MD, FACS; Michael Kerzner, DPM; Jordan Radandt, MD; and Renae Simpson, CWOCN.

Affiliations

Dr. Zakhary is Medical Director, Valley Vein and Vascular Surgeons, Glendale, AZ. Dr. Davey is a family practice physician, St Petersburg, FL. Ms. Bari, Mr. Bean, and Mr. Reber are Doctor of Podiatric Medicine candidates, Midwestern University, Glendale, AZ. Dr. Gallagher is a Nurse Practioner Specialist and Acute Surgical Wound Service Coordinator, Christiana Care Health System, Newark, DE. Ms. Couch is a Nurse Practioner, Wound Healing and Limb Preservation Center, The George Washington University Hospital, Arlington, VA. Ms. Hurlow is a Nurse Practitioner, Faculty of Health and Wellbeing, Canterbury Christ Church University, School of Nursing, Tonbridge, United Kingdom. Ms. Laforet is Director, Clinical Services, Calea Home Care, Mississauga, ON, Canada. Ms. McIsaac is an Associate Professor of Nursing, Cape Breton University, New Waterford, NS Canada. Ms. Napier is a Clinical Nurse Specialist Enterostomal Therapy, Alberta Health Services, Sturgeon Community Hospital, St Albert, AB, Canada. Dr. Vilar-Compte is a professor, Depto de Infectologia, Instituto Nacional de Cancerologia, Tlalpan, México. Ms. Zakhary is a first-year student of osteopathic medicine, Texas College of Osteopathic Medicine, University of North Texas Health Science Center, Fort Worth, TX. Dr. Hermans is President and Owner, Hermans Consulting, LLC, Miami, FL. Dr. Bolton is an Adjunct Associate Professor of Surgery, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ.

Correspondence

Please address correspondence to: Laura Bolton, PhD, 15 Franklyn Place, Metuchen, NJ 08840; email: llbolton@gmail.com.

References

1. Owens PL, Barrett ML, Raetzman S, Maggard-Gibbons MK, Steiner CA. Surgical site infections following ambulatory surgery procedures. JAMA. 2014;311(7):709–716.

2. Perencevich EN, Sands KE, Cosgrove S, Guadagnoli E, Meara E, Platt R. Health and economic impact of surgical site infections diagnosed after hospital discharge. Emerging Infect Dis. 2003;9(2):196–203.

3. De Lissovoy G, Fraeman K, Hutchins V, Murphy D, Song D, Vaughn BB. Surgical site infection: incidence and impact on hospital utilization and treatment costs. Am J Infect Control. 2009;37(5):387–397.

4. Centers for Disease Control and Prevention. Procedure-associated Module: SSI January 2017. Available at: www.cdc.gov/nhsn/pdfs/pscmanual/9pscssicurrent.pdf. Accessed May 3, 2017.

5. Magill SSl, Hellinger W, Cohen J, et al. Prevalence of healthcare-associated infections in acute care hospitals in Jacksonville, Florida. Infect Control Hosp Epidemiol. 2012;33(3):283–291.

6. Mu Y, Edwards JR, Horan TC, Berrios-Torres SI, Fridkin SK. Improving risk-adjusted measures of surgical site infection for the national healthcare safety network. Infect Control Hosp Epidemiol. 2011;32(10):970–986.

7. Anderson D, Podgorny K, Berríos-Torres S, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 Update. Infect Control Hosp Epidemiol. 2014;35(6):605–627.

8. Allegranzi B, Bischoff P, de Jonge S, et al; WHO Guidelines Development Group. New WHO recommendations on preoperative measures for surgical site infection prevention: an evidence-based global perspective. Lancet Infect Dis. 2016;16(12):e276–e287.

9. European Wound Management Association (EWMA). Identifying Criteria for Wound Infection. London, UK: MEP Ltd;2005. Available at: http://ewma.org/fileadmin/user_upload/EWMA.org/Position_documents_2002-2008/English_pos_doc_final.pdf. Accessed June 20, 2012.

10. Petrica A, Brinzeu C, Brinzeu A, Petrica R, Ionac M. Accuracy of surgical wound infection definitions - the first step towards surveillance of surgical site infections. TMJ. 2009;59(3-4):362–365.

11. Rondas AA, Schols JM, Stobberingh EE, Price PE. Definition of infection in chronic wounds by Dutch nursing home physicians. Int Wound J. 2009;6(4):267–274.

12. Wilson APR, Gibbons C, Bruce J. Surgical wound infection as a performance indicator: agreement of common definitions of wound infection in 4773 patients. BMJ. 2004;329:720–723.

13. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control. 1999;27(2):97–132.

14. Avato JL, Lai KK. Impact of post discharge surveillance on surgical-site infection rates for coronary artery bypass procedures. Infect Control Hosp Epidemiol. 2002;23(7):364–367.

15. Rosenthal VD, Richtmann R, Singh S, et al; International Nosocomial Infection Control Consortiuma. Surgical site infections, International Nosocomial Infection Control Consortium (INICC) report. Data summary of 30 countries, 2005-2010. Infect Control Hosp Epidemiol. 2013;34(6):1–8.

16. Edwards JR, Peterson KD, Mu Y, et al. National Healthcare Safety Network (NHSN) report: data summary for 2006 through 2008, issued December 2009. Am J Infect Control. 2009;37(10):783-805.

17. Nakano J, Okabayashi H, Hanyu M, et al. Risk factors for wound infection after off-pump coronary artery bypass grafting: should bilateral internal thoracic arteries be harvested in patients with diabetes? J Thorac Cardiovasc Surg. 2008;135(3):540–545.

18. Shepard J, Ward W, Milstone A, et al. Financial impact of surgical site infections on hospitals: the hospital management perspective. JAMA Surg. 2013;148(10):907–914.

19. Namba RS, Inacio MC, Paxton EW. Risk factors associated with surgical site infection in 30,491 primary total hip replacements. J Bone Joint Surg Br. 2012;94(10):1330–1338.

20. Sherrod BA, Rocque BG. Morbidity associated with 30-day surgical site infection following non-hunt pediatric neurosurgery. J Neurosurg Pediatr. 2017;19(4):421–427.

21. Emami SA, Motevalian SA, Momeni M, Karimi H. The epidemiology of geriatric burns in Iran: a national burn registry-based study. Burns. 2016;42(5):1128–1132.

22. Ostlie DJ, Juang D, Aguayo P, et al. Topical silver sulfadiazine vs collagenase ointment for the treatment of partial thickness burns in children: a prospective randomized trial. J Pediatr Surg. 2012;47(6):1204–1207.

23. Petersen K, Waterman P. Prophylaxis and treatment of infections associated with penetrating traumatic injury. Expert Rev Anti Infect Ther. 2011;9(1):81–96.

24. Prompers L, Huijberts M, Schaper N, et al. Resource utilisation and costs associated with the treatment of diabetic foot ulcers. Prospective data from the Eurodiale Study. Diabetologia. 2008;51(10):1826–1834.

25. Hicks CW, Selvarajah S, Mathioudakis N, et al. Burden of infected diabetic foot ulcers on hospital admissions and costs. Ann Vasc Surg. 2016;33(5)149–158.

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

27. Gloviczki P, Bergan JJ, Menawat SS, et al. Safety, feasibility, and early efficacy of subfascial endoscopic perforator surgery: a preliminary report from the North American registry. J Vasc Surg. 1997;25(1):94–105.

28. Kerstein MD, Gemmen E, van Rijswijk L, et al. Cost and cost effectiveness of venous and pressure ulcer protocols of care. Dis Manage Health Outcomes. 2001;9(11):651–663.

29. Wilson AP, Treasure T, Sturridge MF, Grüneberg RN. A scoring method (ASEPSIS) for postoperative wound infections for use in clinical trials of antibiotic prophylaxis. Lancet. 1986;1(8476):311–313.

30. US Food and Drug Administration. Guidance for Industry: Chronic Cutaneous

Ulcer and Burn Wounds—Developing Products for Treatment. U.S.

Department of Health and Human Services Food and Drug Administration,

Center for Drug Evaluation and Research (CDER), Center for Biologics

Evaluation and Research (CBER), Center for Devices and Radiological

Health (CDRH), June 2006, Clinical/Medical. Available at: www.fda.gov/

downloads/drugs/guidances/ucm071324.pdf. Accessed June 1, 2017.

31. Gardner SE, Frantz RA, Doebbeling BN. The validity of the clinical signs

and symptoms used to identify localized chronic wound infection. Wound

Repair Regen. 2001;9(3):178–186.

32. Cutting KF, Harding KG. Criteria for identifying wound infection. J Wound

Care. 1994;3(4):198–201.

33. Driver VR, Gould LJ, Dotson P, et al. Identification and content validation

of wound therapy clinical endpoints relevant to clinical practice and

patient values for FDA approval. Part 1. Survey of the wound care community.

Wound Repair Regen. 2017;(3):454–465.

34. Bruce J. Russell EM, Mollison J, Krukowski ZH. The quality of measurement

of surgical wound infection as the basis for monitoring: a systematic

review. J Hosp Infect. 2001;49(2):99–108.

35. Ubbink DT, Lindeboom R, Eskes AM, Brull H, Legemate DA, Vermeulen H.

Predicting complex acute wound healing in patients from a wound expertise

centre registry: a prognostic study. Int Wound J. 2015;12(5):531–536.

36. World Union of Wound Healing Societies (WUWHS) Consensus Document.

Closed surgical incision management: understanding the role of

NPWT. Wounds Int. 2016. Available at: www.wuwhs2016.com/files/WUWHS_

SI_consensus_Web.pdf. Accessed June 1, 2017.

37. Margolis DJ, Berlin JA, Strom BL. Which venous leg ulcers will heal with

limb compression bandages? Am J Med. 2000;109(1):15–19.

38. McGuckin M, Goldman R, Bolton L, Salcido R. The clinical relevance

of microbiology in acute and chronic wounds. Adv Skin Wound Care.

2003;16(1):12–23.

39. Gottrup F, Apelqvist J, Price P. Producing precise outcomes in randomized

controlled trials and clinical studies. Wounds. 2012;24(1):3–9.

40. Association for the Advancement of Wound Care. The Association for the

Advancement of Wound Care: Quality of care wound glossary. Available

at: https://aawconline.org/wpcontent/uploads/2015/11/AAWC-Quality-of-

Care-with-I-CVIswebsite-v3.pdf. Accessed December 20, 2015.

41. Gottrup F, Melling A, Hollander A. An overview of surgical site infections:

aetiology, incidence and risk factors. EWMA J. 2005;5(2):11–15.

42. US Department of Health and Human Services Food and Drug Administration

Center for Drug Evaluation and Research (CDER). Guidance for Industry.

Acute Bacterial Skin and Skin Structure Infections: Developing Drugs

for Treatment. October, 2013. Available at: www.fda.gov/ucm/groups/

fdagov-public/@fdagov-drugs-gen/documents/document/ucm071185.

pdf. Accessed May 12, 2017.

43. Lipsky BA, Silverman MH, Joseph WS. A proposed new classification of

skin and soft tissue infections modeled on the subset of diabetic foot infection.

Open Forum Infect Dis. 2016;4(1):ofw255.

44. Tanner J, Norrie P, Melen K. Preoperative hair removal to reduce surgical

site infection. Cochrane Database Syst Rev. 2011;(11):CD004122.

45. Twofigh S, Clarke T, Yacoub W. Significant reduction of wound infections

with daily probing of contaminated wounds: a prospective randomized

clinical trial. Arch Surg. 2011;146(4):448–452.

46. Brölmann FE, Eskes AM, Goslings JC, et al; REMBRANDT study group.

Randomized clinical trial of donor-site wound dressings after split-skin

grafting. Br J Surg. 2013;100(5):619–627.

47. Wiechula R. The use of moist wound-healing dressings in the management

of split-thickness skin graft donor sites: a systematic review. Int J

Nurs Pract. 2003;9:S9–S17.

48. Hutchinson J, McGuckin M. Occlusive dressings: a microbiologic and

clinical review. Am J Infect Control. 1990;18:257–268.

49. Schwarzkopf A, Dissemond J. Indications and practical implementation of

www.o-wm.com

AAWC FEATURE

microbiologic diagnostics in patients with chronic wounds. J Dtsch Dermatol

Ges. 2015;13(3):203–209.

50. Hawkins RB, Levy SM, Senter CE, et al. Beyond surgical care improvement

program compliance: antibiotic prophylaxis implementation gaps.

Am J Surg. 2013;206(4):451–456.

51. Gagliardi AR, Eskicioglu C, McKenzie M, Fenech D, Nathens A, McLeod R.

Identifying opportunities for quality improvement in surgical site infection

prevention. Am J Infect Control. 2009;37(5):398–402.

52. Institute of Medicine. Clinical Practice Guidelines We Can Trust. Standards

of developing trustworthy clinical practice guidelines (CPGs). Standards,

March, 2011. Available at: http://iom.edu/Reports/2011/Clinical-

Practice-Guidelines-We-Can-Trust/Standards.aspx. Accessed December

12, 2011.

53. Rosenfeld RM, Shiffman RN. Clinical practice guideline development manual:

a quality-driven approach for translating evidence into action. Otolaryngol

Head Neck Surg. 2009;140(6S):S1–S43.

54. Yaghmaie F. Content validity and its estimation. J Med Education.

2003;3(1):25–27.

55. Lynn MR. Determination and quantification of content validity. Nurs Res.

1986;35:382–385.

56. Kurd SK, Hoffstad OJ, Bilker WB, Margolis DJ. Evaluation of the use of

prognostic information for the care of individuals with venous leg ulcers or

diabetic neuropathic foot ulcers. Wound Repair Regen. 2009;17(3):318–325.

57. Gottrup F. Optimizing wound treatment through health care structuring

and professional education. Wound Repair Regen. 2004;12(2):129–133.

58. McIsaac C. Managing wound care outcomes. Ostomy Wound Manage.

2005;51(4):54–59.

59. American Society of Plastic Surgeons. Chronic Wounds of the Lower Extremity.

Evidence-based Clinical Practice Guideline: Chronic Wounds of

the Lower Extremity. Arlington Heights, IL: American Society of Plastic

Surgeons;2007. Available at: www1.plasticsurgery.org. Accessed June

12, 2011.

60. Wound, Ostomy and Continence Nurses Society (WOCN) Wound Committee;

Association for Professionals in Infection Control and Epidemiology,

Inc. (APIC) 2000 Guidelines Committee. Clean vs. sterile dressing

techniques for management of chronic wounds: a fact sheet. J Wound

Ostomy Continence Nurs. 2012;39(2 suppl):S30–S34.

61. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Infection Control Practices

Advisory Committee of the Centers for Disease Control and Prevention.

Management of Multidrug-resistant Organisms in Healthcare Settings.

Available at: www.cdc.gov/mrsa/pdf/mdroguideline2006.pdf. Accessed

July 20, 2012.

62. Rutala WA, Weber DJ; Healthcare Infection Control Practices Advisory

Committee of the Centers for Disease Control and Prevention. Guideline

for Disinfection and Sterilization in Healthcare Facilities, 2008. Available

at: www.cdc.gov/infectioncontrol/pdf/guidelines/disinfection-guidelines.

pdf. Accessed July 20, 2012.

63. Centers for Disease Control and Prevention Guideline for Hand Hygiene,

in Health-Care Settings: Recommendations of the Healthcare Infection

Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA

Hand Hygiene Task Force. MMWR. 2002;51(No. RR- 16). Available at

www.cdc.gov/mmwr/pdf/rr/rr5116.pdf. Accessed July 20, 2012.

64. McCoy CE, Chakravarthy B, Lotfipour S. Guidelines for field triage of

injured patients: in conjunction with the morbidity and mortality weekly

report published by the Centers for Disease Control and Prevention. Western

J Emer Med. 2013;14(1):69-76.

65. Department of Veterans Affairs, Department of Defense Clinical Practice

Guidelines: Rehabilitation of lower limb amputation. 2007. Available at:

www.healthquality.va.gov/guidelines/rehab/amp/amp_v652.pdf. Accessed

October 18, 2017.

66. European Wound Management Association. Position Document: Hard-To-

Heal Wounds: A Holistic Approach. London, UK: MEP Ltd;2008. Available

at: http://ewma.org/fileadmin/user_upload/EWMA.org/Position_documents_

2002-2008/English_pos_doc_final.pdf Accessed June 20, 2012.

67. Hospenthal D, Murray C, Anderson RC, et al; Infectious Diseases Society

of America; Surgical Infection Society. Guidelines for the Prevention of

Infections Associated With Combat-Related Injuries: 2011. Update endorsed

Infectious Diseases Society of America; Surgical Infection Society.

J Trauma. 2011;71:(2 suppl 2):S210–S234.

68. Moran GJ, Abrahamian FM, Lovecchio F, Talan DA. Acute bacterial skin

infections: developments since the 2005 Infectious Diseases Society of

America (IDSA) guidelines. J Emerg Med. 2013;44(6):e397–e412.

69. Japan Community Healthcare Organization. Quality check measure sets for

surgical infection (2011). Available at: www.qualitycheck.org/assets/Hospital_

Prof_USER_GUIDE_June%202011.pdf. References cited in: http://cid.

oxfordjournals.org/content/43/3/322.long:). Accessed November 10, 2011.

70. LeBlanc K, Baranoski S, Christensen D, et al. International Skin Tear Advisory

Panel: a tool kit to aid in the prevention, assessment, and treatment

of skin tears using a Simplified Classification System©. Adv Skin Wound

Care. 2013;26(10):459–476.

71. Lipsky BA, Berendt AR, Cornia PB, et al. 2012 Infectious Diseases Society

of America Clinical practice guideline for the diagnosis and treatment of

diabetic foot infections. J Am Podiatr Med Assoc. 2013;103(1):2–7.

72. National Guideline Clearinghouse Guideline Synthesis: Management of

Microvascular Complications of Type 2 Diabetes Mellitus. Available at:

www.guideline.gov. Accessed June 21, 2012.

73. Brehove T, Joslyn M, Morrison S, Strehlow AJ, Wismer B. Adapting Your

Practice: Treatment and Recommendations for Homeless Patients with Diabetes

Mellitus. Nashville, TN: Health Care for the Homeless Clinicians’ Network.

Available at: www.nhchc.org/wp-content/uploads/2011/09/Diabetes-

Mellitus.pdf. Accessed October 10, 2017.

74. National Institute for Health and Clinical Excellence. Surgical Site Infection:

Prevention and Treatment. Available at: www.nice.org/uk/guidance/

CG74/NiceGuidance/pdf/English. Accessed November 10, 2012.

75. Robson MC, Barbul A. Guidelines for the best care of chronic wounds.

Wound Repair Regen. 2006;14(6):647–648.

76. Whitney J, Phillips L, Aslam R, et al. Guidelines for the treatment of pressure

ulcers. Wound Repair Regen. 2006;14(6):663–679.

77. World Health Organization. WHO Guidelines on Hand Hygiene in Healthcare.

Geneva, Switzerland: World Health Organization Press;2009.

78. World Health Organization. WHO Global Guidelines for the Prevention of

Surgical Site Infection. Geneva, Switzerland: World Health Organization

Press;2016.

79. Ratliff CR, Tomaselli N. WOCN update on evidence-based guideline for

pressure ulcers. J Wound Ostomy Continence Nurs. 2010;37(5):459–460.

80. Wound, Ostomy and Continence Nurses. Clean vs sterile dressing techniques

for management of chronic wounds: a fact sheet. J Wound Ostomy

Continence Nurs. 2012;39(2S):S30–S34.

81. National Institute for Health and Care Excellence (NICE). Surgical Site Infection

Guidance. Available at: www.nice.org.uk/qs49. Accessed February

14, 2014.

82. Anderson DJ, Podgorny K, Berríos-Torres SI, et al. Strategies to prevent

surgical site infections in acute care hospitals: 2014 update. Infect Control

Hosp Epidemiol. 2014;35(6):605–627.

83. Bratzler DW, Dellinger EP, Olsen KM, et al; American Society of Health-

System Pharmacists; Infectious Disease Society of America; Surgical Infection

Society; Society for Healthcare Epidemiology of America. Clinical

practice guidelines for antimicrobial prophylaxis in surgery. Am J Health

Syst Pharm. 2013;70(3):195–283.

84. National Guideline Clearinghouse. Guideline summary: SOLUTIONS®

wound care algorithm. Rockville (MD): Agency for Healthcare Research

and Quality; 2013. Available at: www.guideline.gov. Accessed October 10,

2017.

85. European Wound Management Association. Position Document: Management

of Wound Infection. London, UK: MEP Ltd;2006. Available

at: http://ewma.org/fileadmin/user_upload/EWMA.org/Position_documents_

2002-2008/English_pos_doc_final.pdf. Accessed June 20, 2012.

86. Bolton LL. Evidence-based report card: operational definition of moist

wound healing. J Wound Ostomy Continence Nurs. 2007;34(1):23–29.

87. Fife CE, Walker D, Thomson B. Electronic health records, registries, and

quality measures: What? Why? How? Adv Wound Care (New Rochelle).

2013;2(10):598–604.

88. Hurlow J, Couch K, Laforet K, Bolton L, Metcalf D, Bowler P. Clinical biofilms:

a challenging frontier in wound care. Adv Wound Care (New Rochelle).

2015;4(5):295–301.

89. Wood RAB. Disintegration of cellulose dressings in open granulating

wounds. BMJ. 1976;3:1444–1445.

90. O’Meara S, Al-Kurdi D, Ovington L. Antibiotics and antiseptics for venous

leg ulcers. Cochrane Database Syst Rev. 2008;(1):CD003557.

91. Ennis WJ, Meneses P. Clinical evaluation: outcomes, benchmarking, introspection,

and quality improvement. Ostomy Wound Manage. 1996;42(10A

suppl):40S–47S.

92. Church D, Elsayed S, Reid O, Winston B, Lindsay R. Burn wound infections.

Clin Microbiol Rev. 2006;19(2):403–434.

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