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Do surgical care bundles reduce the risk of surgical site infections in patients undergoing colorectal surgery? A systematic review and cohort meta-analysis of 8,515 patients

Open AccessPublished:April 24, 2015DOI:https://doi.org/10.1016/j.surg.2015.03.009

      Background

      Care bundles are a strategy that can be used to reduce the risk of surgical site infection (SSI), but individual studies of care bundles report conflicting outcomes. This study assesses the effectiveness of care bundles to reduce SSI among patients undergoing colorectal surgery.

      Methods

      We performed a systematic review and meta-analysis of randomized controlled trials, quasi-experimental studies, and cohort studies of care bundles to reduce SSI. The search strategy included database and clinical trials register searches from 2012 until June 2014, searching reference lists of retrieved studies and contacting study authors to obtain missing data. The Downs and Black checklist was used to assess the quality of all studies. Raw data were used to calculate pooled relative risk (RR) estimates using Cochrane Review Manager. The I2 statistic and funnel plots were performed to identify publication bias. Sensitivity analysis was carried out to examine the influence of individual data sets on pooled RRs.

      Results

      Sixteen studies were included in the analysis, with 13 providing sufficient data for a meta-analysis. Most study bundles included core interventions such as antibiotic administration, appropriate hair removal, glycemic control, and normothermia. The SSI rate in the bundle group was 7.0% (328/4,649) compared with 15.1% (585/3,866) in a standard care group. The pooled effect of 13 studies with a total sample of 8,515 patients shows that surgical care bundles have a clinically important impact on reducing the risk of SSI compared to standard care with a CI of 0.55 (0.39–0.77; P = .0005).

      Conclusion

      The systematic review and meta-analysis documents that use of an evidence-based, surgical care bundle in patients undergoing colorectal surgery significantly reduced the risk of SSI.
      Surgical site infections (SSIs) are associated with increased morbidity, increased duration of hospitalization, re-admission, and excess utilization of health care resources. Each year >600,000 operative procedures are performed in the United States to treat colon-related diseases; as a surgical specialty, colorectal surgery has one of the highest rates of SSI. This rate as measured by several independent investigators is highly variable, ranging from 15 to 30%.
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Petrosillo N.
      • Drapeau C.M.J.
      • Nicastri E.
      • et al.
      Surgical site infections in Italian hospitals: a prospective multicenter study.
      • Darouiche R.O.
      • Wall M.
      • Itani K.M.K.
      • et al.
      Chlorhexidine–alcohol versus povidone–iodine for surgical-site antisepsis.
      • Tanner J.
      • Khan D.
      • Ball J.
      • et al.
      Post discharge surveillance to identify colorectal surgical site infection rates and costs.
      A recent collaborative study by the Joint Commission Center for Transforming Healthcare and the American College of Surgeons (ACS) found a baseline rate of 15.8% among 7 US institutions participating in a multidisciplinary effort to reduce the risk of infections after colorectal surgery.
      Joint Commission Center for Transforming Healthcare and American College of Surgeons Collaborative
      Reducing Colorectal Infection Rates. Colorectal Surgical Site Infections Project.
      The financial cost of treating SSIs can be substantial. The Joint Commission/ACS collaborative study estimated that the use of evidence-based practices can prevent >30,000 infections, with an estimated collective saving of $834 million.
      Joint Commission Center for Transforming Healthcare and American College of Surgeons Collaborative
      Reducing Colorectal Infection Rates. Colorectal Surgical Site Infections Project.
      After discharge, patients who develop an SSI often experience an impairment of both physical and mental well-being.
      • Tanner J.
      • Padley W.
      • Davey S.
      • et al.
      Patients’ narratives of surgical site infection; implications for practice.
      This process is exacerbated in patients undergoing colorectal resection of cancer, further impacting their health-related quality of life.
      Numerous clinical interventions with varying levels of supporting evidence have been implemented to reduce SSIs among colorectal patients. A recent approach to improving patient outcomes is the use of care bundles. Care bundles were first introduced by the Institute for Healthcare Improvement (IHI) in 2001 to improve clinical outcomes in the critical care population.
      • Institute for Healthcare Improvement (IHI)
      The concept of a care bundle was developed from evidence documenting that a structured approach to performing 3–5 evidence-based collective interventions could lead to an improved patient outcome. While specific interventions may vary between bundles, it is the bundle approach that ensures consistent implementation of all measures that is claimed to be successful. Surgical care bundles have been developed to reduce SSI after the success of care bundles in reducing catheter-related bacteremia and ventilator-associated pneumonia.
      • Provonost P.
      • Needham D.
      • Berenholtz S.
      • et al.
      An intervention to decrease catheter related bloodstream infections in the ICU.
      • Resar R.
      • Pronovost P.
      • Haraden C.
      • et al.
      Using a bundle approach to improve ventilator care processes and reduce ventilator-associated pneumonia.
      To date, there has been no systematic review of the effect of care bundles to reduce SSIs, and individual studies report conflicting findings of successes and failures.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Hedrick T.L.
      • Heckman J.A.
      • Smith R.L.
      • et al.
      Efficacy of protocol implementation on incidence of wound infection in colorectal operations.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Stulberg J.J.
      • Delaney C.P.
      • Neuhauser D.V.
      • et al.
      Adherence to surgical care improvement project measures and the association with postoperative measures.
      Our analysis represents the first systematic review of the effectiveness of surgical care bundles to reduce SSIs among patients undergoing colorectal surgery.

      Methods

      This systematic review was conducted and is reported in accordance with the PRISMA statement.
      • Moher D.
      • Liberati A.
      • Tetzlaff J.
      • et al.
      The PRISMA Group (2009)
      Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement.

      Research question

      The aim of this study was to determine if implementation of an SSI care bundle reduced the rate of SSIs among patients having colorectal surgery.

      Inclusion and exclusion criteria

      We included all studies that compared a care bundle designed to reduce SSI against a control group, baseline group, or early implementation group, and reported SSIs among colorectal patients as an outcome for both groups. While randomized trials are usually the focus of a meta-analysis, meta-analysis can also be applied to cohort studies. This is a common practice, although the Cochrane Collaboration cautions that meta-analyses of cohort studies are more likely to be subject to selection bias where not all patients receive the intervention.
      We decided to extend the inclusion criterion beyond randomized trials, because care bundles comprise existing best practice interventions such as appropriate antibiotic management and implementing a non-intervention group may be unethical. The inclusion of cohort studies also added to the breadth of clinical data.
      The IHI defines care bundles as ≥3 evidence-based interventions with the potential to prevent SSI that are implemented in a consistent manner for all patients. Importance is placed on the consistent and systematic application of all elements within a bundle rather than on individual selective elements. For this reason, all bundles designed to reduce SSI were included in this review, despite variations among individual interventions. Only patients undergoing colorectal surgery were included. No constraints were placed on language of the publication.

      Outcomes of interest

      SSI among patients having colorectal surgery was the primary outcome.

      Search strategy

      A member of the research team (W.P.) performed a comprehensive literature search using terms identified and agreed by the authors. PubMed, Embase, CINAHL, Scopus, the Cochrane Database of Systematic Reviews, the Central Register of Controlled Trials, Academic Search Premier, and clinicaltrials.gov were searched from 2002 to June 2014 using the keywords: “surgical site infection,” “compliance” or “adherence,” “care bundle,” “care package,” “care checklist,” “care pathway,” “care intervention,” “prevention bundle,” “surgical care improvement,” “5 million lives,” “SCIP,” “100000 lives,” and “colorectal.” We also reviewed the reference lists of retrieved studies to identify studies that had not been identified by the search strategy. If studies were identified as potentially able to answer the study question but contained missing data, authors were contacted in an attempt to fill in the missing variables.

      Data extraction and risk of bias assessment

      Two review authors independently assessed the titles and abstracts of 518 potentially relevant studies. If it was unclear from the title or abstract whether a study met the criteria or there was a disagreement over eligibility, the study was retrieved in full and assessed further by all 6 review authors independently. Two review authors independently extracted details from eligible studies onto data extraction forms which were cross-checked and used to create Tables I and II. The Downs and Black quality checklist was used to assess all studies.
      • Downs S.H.
      • Black N.
      The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions.
      This checklist was designed to meet the increasing demand for the use of evidence in systematic reviews and meta-analyses by enabling the quality of both randomized and non-randomized studies to be assessed. It provides an overall numeric score out of 30 points based on 5 themed sections. The 5 sections comprise study quality (overall quality), external validity (ability to generalize findings), study bias (in interventions and outcome measures), confounding and selection bias (in sampling), and power (sample size). The National Collaborating Center for Methods and Tools, Canada describes the Downs and Black system as valid, reliable, and methodologically strong.
      National Collaborating Centre for Methods and Tools Quality Checklist for Health Care Intervention Studies
      Table IStudy description
      First author and yearStudy designData collection periodSample groupSample size (patients)Compliance with interventionsSSI data and surveillanceSSI outcome
      Anthony 2011RCT2 y, 8 monthsColorectal

      Single center
      Baseline 97

      Cohort 100
      Compliance data for composite bundle in both groupsCDC definition. Surveillance at 30 days.Control 24.7%

      Intervention 45%
      Berenguer 2010Cohort (before and after implementation)Baseline 1 y

      Cohort 1 y
      Colorectal

      Single center
      Baseline 113

      Cohort 84
      Compliance data for composite bundle in baseline and cohortSuperficial SSIs only. NSQIP definition, collected by dedicated nurseSuperficial SSI data only

      Baseline 13.3%

      Cohort 8.3%
      Bull 2011
      Study authors provided additional information.
      Cohort (before and after implementation)Baseline 1 y

      Cohort 1 y
      Colorectal

      Single center
      Baseline 180

      Cohort 275
      Compliance data for composite bundle and quarterly for individual interventions for cohortAustralian NHSN definition. No additional information.Baseline 15%

      Cohort 7%
      Cima 2013Cohort (before and after implementation)Baseline 1 y

      Cohort 2 y
      Colorectal

      Single center
      Baseline 531

      Cohort 198
      Compliance data for individual interventions for baseline and cohortNSQIP defined outcomesBaseline 9.8%

      Cohort 4.0%
      Crolla 2012
      Data from 2009 and 2010 was excluded as bundle implementation was incomplete during this time.
      Cohort (before and after implementation)Baseline 1.5 y

      Cohort 2.5 y
      Colorectal

      Single center
      Baseline 394

      Cohort 377
      Compliance data for composite bundle and individual interventions for baseline and cohortCDC definition. Surveillance by dedicated infection control staff until 30 daysBaseline 21.5%

      Cohort 16.1%
      Hawn 2011
      Colorectal data extracted.
      ,
      Insufficient data to be included in the meta-analysis.
      CohortBaseline 1 y

      Cohort 3 y
      Colorectal, CABG, cardiac, orthopedic.

      Multicenter
      Baseline not known

      Cohort 15,444
      Compliance data for composite bundle and individual interventions for cohort onlyCDC definition. Surveillance at 30 days.No baseline data

      Cohort 14.2%
      Hedrick 2007Cohort (before and after implementation)Baseline 2 y

      Cohort 6 months
      Colorectal

      Single center
      Baseline 175

      Cohort 132
      Compliance data for individual interventions for baseline and cohortCDC definition. 90 days follow-upBaseline 25.6%

      Cohort 15.9%
      Keenan 2014Cohort (before and after implementation)Baseline 3 y

      Cohort 1.5 y
      Colorectal

      Single center
      Baseline 212

      Cohort 212
      No data presented. Narrative reports that ‘compliance with some interventions approached 100%’NSQIP defined outcomes. Surveillance at 30 days.Baseline 25.9%

      Cohort 8.4%
      Larochelle 2011
      Insufficient data to be included in the meta-analysis.
      Cohort (before and after implementation)Baseline 2 y

      Cohort 4 y
      Colorectal

      Single center
      706 Not clear if this is Cohort only or Baseline and Cohort combinedCompliance data for individual interventions for baseline and cohortInternational Classification of Diseases. Follow-up performed by surgeon (time of surveillance unknown).No baseline data

      Cohort 12.3%
      Liau 2010
      Study authors provided additional information.
      Cohort (before and after implementation)Baseline 1 y

      Cohort 2 y
      Gastrointestinal

      Single center
      Baseline 1,040

      Cohort 2,408
      Compliance data for individual interventions for cohort onlyCDC definition. In patient case note review, clinic review, post discharge phone calls.Baseline 3.1%

      Cohort 0.5%
      Lutfiyya 2012Cohort (before and after implementation)Baseline 4 y

      Cohort 1.5 y
      Colorectal

      Single center
      Baseline 430

      Cohort 195
      No information on compliance dataNSQIP definition. Data collected by trained nursesBaseline 21%

      Cohort 6.6%
      Pastor 2010Cohort (early implementation versus late implementation)Early 14 months

      Late 14 months
      Colorectal

      Single center
      Early 238

      Late 243
      Compliance data for composite bundle and individual interventions for early and lateCDC definition.Early 18.9%

      Late 19.4%
      Tillman 2013
      Colorectal data extracted.
      Cohort (before and after implementation)Baseline 1 y

      Cohort 1 y
      Cardiac, colorectal, general, gynecologic, orthopedic, thoracic, vascular Single centerBaseline 79

      Cohort 104
      Compliance data for individual interventions for baseline and cohortSSI definition unclear but presumably based on NSQIP.Baseline 24.0%

      Cohort 11.5%
      Waits 2014Cohort (comparison of increasing number of interventions within bundle)Cohort 3 yColorectal

      Multicenter
      1 intervention, 99; 2 interventions, 552; 3 interventions, 1,179; 4 interventions, 1,438; 5 interventions, 730; 6 interventions, 87Compliance data for individual interventions and composite bundleInternational Classification of Diseases. Surveillance at 30 days1 17.1%

      2 14.1%

      3 8.3%

      4 6.1%

      5 2.6%

      6 2.1%
      Wick 2008
      Insufficient data to be included in the meta-analysis.
      CohortCohort 11 monthsColorectal

      Single center
      Cohort 298Compliance data for individual interventions for baseline and cohortCDC definition.

      Surveillance at 30 days by attending surgeon
      No baseline data

      Cohort 20%
      Wick 2012Cohort (before and after implementation)Baseline 1 y

      Cohort 1 y
      Colorectal

      Single center
      Baseline 278

      Cohort 324
      Compliance data for individual interventions for baseline and cohortNSQIP defined outcomes

      Surveillance unknown
      Baseline 27.3%

      Cohort 18.2%
      CABG, Coronary artery bypass grafting; CDC, Centers for Disease Control and Prevention; NHSN, National Healthcare Safety Network; NSQIP, National Surgical Quality Improvement Program; RCT, randomized, controlled trial; SSI, surgical site infection.
      Study authors provided additional information.
      Data from 2009 and 2010 was excluded as bundle implementation was incomplete during this time.
      Colorectal data extracted.
      § Insufficient data to be included in the meta-analysis.
      Table IIBundle interventions
      SSI bundle interventionsAnthony 2011Berenguer 2010Bull 2011Cima 2013Crolla 2012Hawn 2011Hedrick 2007Keenan 2014Larochelle 2011Liau 2010Lutfiyya 2012Pastor 2010Tillman 2013Waits 2014Wick 2008Wick 2012
      Appropriate antibiotic selection/dose
      Prophylactic antibiotics within 60 min before surgery
      Prophylactic antibiotics discontinued within 24 h
      Antibiotic re-dose within 3–4 h after incision
      Glycemic control
      Normothermia pre-operatively
      Normothermia intra-operatively
      Normothermia post-operatively
      Appropriate hair removal
      Supplemental oxygen
      Systolic pressure ≥90 mmHg
      Reduction in intravenous fluids during operation
      Wound edge protector
      CHG cloths on admission
      Preoperative CHG wipes or shower
      CHG in alcohol skin preparation
      Double gloving
      Glove and/or gown change
      Theatre discipline/restricted traffic
      Smoking cessation
      Patient SSI education
      Tray for closure of fascia and skin
      Omission of mechanical bowel preparation
      Omission of mechanical bowel preparation was revised during study to mechanical bowel preparation plus oral antibiotics.
      Mechanical bowel preparation plus oral antibiotics
      Omission of mechanical bowel preparation was revised during study to mechanical bowel preparation plus oral antibiotics.
      Oral antibiotics given with mechanical bowel prep if used
      Penrose drain for patients with BMI ≥25 kg/m2
      Pulse lavage of subcutaneous tissue
      Minimally invasive surgery
      Short duration of surgery
      Silver dressings for 5 days
      Removal of sterile dressing within 48 h
      Postoperative washing of wound with CHG
      BMI, Body mass index; CHG, chlorhexidine gluconate; SSI, surgical site infection.
      Omission of mechanical bowel preparation was revised during study to mechanical bowel preparation plus oral antibiotics.

      Statistical analysis

      Raw data only were used to calculate pooled relative risk (RR) estimates from random effects models using Cochrane Review Manager version 5.2.

      Sensitivity analysis and publication bias assessment

      To minimize possible publication bias, the I2 statistic was used to assess heterogeneity, and funnel plots were inspected for symmetry to identify possible publication bias. A sensitivity analysis was carried out by deleting 1 study each time to examine the influence of individual data sets on the pooled RRs. The National Library of Medicine's clinical trial registry (www.clinicaltrials.gov) was screened to discover whether any studies had been conducted that remained unpublished. Our search did not identify any relevant “closed” studies. One study investigating the effect of bathing bundle regimens in reducing SSIs started in April 2011 and closed data collection in February 2014, but no results have been published to date, and this study was not included in the analysis.

      Results

      Of the 95 articles retrieved, 16 studies (1 randomised trial and 15 cohort studies) assessed the effect of implementing care bundles among patients undergoing colorectal surgery on SSIs (Fig 1).
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Hedrick T.L.
      • Heckman J.A.
      • Smith R.L.
      • et al.
      Efficacy of protocol implementation on incidence of wound infection in colorectal operations.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Anthony T.
      • Murray B.W.
      • Sum-Ping J.
      • et al.
      Evaluating an evidence-based bundle for preventing surgical site infection: a randomized trial.
      • Bull A.
      • Wilson J.
      • Worth L.J.
      • et al.
      A bundle of care to reduce colorectal surgical infections: An Australian experience.
      • Cima R.
      • Dankbar E.
      • Lovely J.
      • et al.
      Colorectal surgery surgical site infection reduction programme: a national surgical quality improvement program-driven multidisciplinary single-institution experience.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      • Larochelle M.
      • Hyman N.
      • Gruppi L.
      • et al.
      Diminishing surgical site infection after colorectal surgery with surgical care improvement project: is it time to move on?.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      • Lutfiyya W.
      • Parsons D.
      • Breen J.
      A colorectal “care bundle” to reduce surgical site infections in colorectal surgeries: a single-center experience.
      • Pastor C.
      • Artinyan A.
      • Varma M.G.
      • et al.
      An increase in compliance with the surgical care improvement project measures does not prevent surgical site infection in colorectal surgery.
      • Tillman M.
      • Wehbe-Janek H.
      • Hodges B.
      • et al.
      Surgical care improvement project and surgical site infections: can integration in the surgical safety checklist improve quality performance and clinical outcomes?.
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      • Wick E.C.
      • Gibbs L.
      • Indorf L.A.
      • et al.
      Implementation of quality measures to reduce surgical site infection in colorectal patients.
      • Wick E.C.
      • Hobson D.B.
      • Bennett J.L.
      • et al.
      Implementation of a surgical comprehensive unit-based safety program to reduce surgical site infections.
      Study characteristics are described in Table I, and bundle interventions are listed in Table II. None of the studies implemented identical SSI care bundles; however, all studies included elements from a core group of evidence-based interventions including appropriate antibiotic prophylaxis, normothermia, appropriate hair removal, and glycemic control for hyperglycemic patients. The studies were assessed as medium to high quality (Table III).
      Table IIIDowns and Black quality checklist
      First author and yearReporting (10)External validity (3)Internal validity bias (7)Internal validity – selection bias (6)Subtotal score (26)Sufficiently powered?
      Anthony 20111037525Yes
      Berenguer 2010835319No
      Bull 2011734216No
      Cima 20131035119No
      Crolla 2012935219No
      Hawn 20111035422Not known
      Hedrick 20071035321No
      Keenan 2014935522Yes
      Larochelle 2011634417Not known
      Liau 2010935219Yes
      Lutfiyya 2012935320Yes
      Pastor 20101036423No
      Tillman 2013836421No
      Waits 2014936523No
      Wick 20081036423Not known
      Wick 20121034219No
      Values in parentheses indicate total scores available.
      Five authors were contacted to provide additional data required for the meta-analysis. Two authors provided additional data that were included in the meta-analysis.
      • Bull A.
      • Wilson J.
      • Worth L.J.
      • et al.
      A bundle of care to reduce colorectal surgical infections: An Australian experience.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      One author was unable to provide the requested data, and attempts to contact the remaining 2 study authors were unsuccessful.
      • Larochelle M.
      • Hyman N.
      • Gruppi L.
      • et al.
      Diminishing surgical site infection after colorectal surgery with surgical care improvement project: is it time to move on?.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Wick E.C.
      • Gibbs L.
      • Indorf L.A.
      • et al.
      Implementation of quality measures to reduce surgical site infection in colorectal patients.
      Thirteen studies provided sufficient raw data to be grouped together in a meta-analysis (Fig 2).
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Hedrick T.L.
      • Heckman J.A.
      • Smith R.L.
      • et al.
      Efficacy of protocol implementation on incidence of wound infection in colorectal operations.
      • Anthony T.
      • Murray B.W.
      • Sum-Ping J.
      • et al.
      Evaluating an evidence-based bundle for preventing surgical site infection: a randomized trial.
      • Bull A.
      • Wilson J.
      • Worth L.J.
      • et al.
      A bundle of care to reduce colorectal surgical infections: An Australian experience.
      • Cima R.
      • Dankbar E.
      • Lovely J.
      • et al.
      Colorectal surgery surgical site infection reduction programme: a national surgical quality improvement program-driven multidisciplinary single-institution experience.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      • Wick E.C.
      • Gibbs L.
      • Indorf L.A.
      • et al.
      Implementation of quality measures to reduce surgical site infection in colorectal patients.
      • Wick E.C.
      • Hobson D.B.
      • Bennett J.L.
      • et al.
      Implementation of a surgical comprehensive unit-based safety program to reduce surgical site infections.
      Baseline data were taken from the control groups, pre-implementation groups, early implementation groups, and single intervention only groups.
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Hedrick T.L.
      • Heckman J.A.
      • Smith R.L.
      • et al.
      Efficacy of protocol implementation on incidence of wound infection in colorectal operations.
      • Anthony T.
      • Murray B.W.
      • Sum-Ping J.
      • et al.
      Evaluating an evidence-based bundle for preventing surgical site infection: a randomized trial.
      • Bull A.
      • Wilson J.
      • Worth L.J.
      • et al.
      A bundle of care to reduce colorectal surgical infections: An Australian experience.
      • Cima R.
      • Dankbar E.
      • Lovely J.
      • et al.
      Colorectal surgery surgical site infection reduction programme: a national surgical quality improvement program-driven multidisciplinary single-institution experience.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      • Wick E.C.
      • Gibbs L.
      • Indorf L.A.
      • et al.
      Implementation of quality measures to reduce surgical site infection in colorectal patients.
      • Wick E.C.
      • Hobson D.B.
      • Bennett J.L.
      • et al.
      Implementation of a surgical comprehensive unit-based safety program to reduce surgical site infections.
      Intervention data were taken from the care bundle intervention groups, post-implementation groups, late implementation groups, and complete bundle implementation groups.
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Hedrick T.L.
      • Heckman J.A.
      • Smith R.L.
      • et al.
      Efficacy of protocol implementation on incidence of wound infection in colorectal operations.
      • Anthony T.
      • Murray B.W.
      • Sum-Ping J.
      • et al.
      Evaluating an evidence-based bundle for preventing surgical site infection: a randomized trial.
      • Bull A.
      • Wilson J.
      • Worth L.J.
      • et al.
      A bundle of care to reduce colorectal surgical infections: An Australian experience.
      • Cima R.
      • Dankbar E.
      • Lovely J.
      • et al.
      Colorectal surgery surgical site infection reduction programme: a national surgical quality improvement program-driven multidisciplinary single-institution experience.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      • Wick E.C.
      • Hobson D.B.
      • Bennett J.L.
      • et al.
      Implementation of a surgical comprehensive unit-based safety program to reduce surgical site infections.
      The meta-analysis included 8,515 patients and found an SSI rate in the surgical care bundle group of 7.0% (328/4,649) compared with 15.1% (585/3,866) in the baseline with a CI of 0.55 (0.39 to 0.77; P = .0005); the I2 test for homogeneity was 84%.
      Figure thumbnail gr2
      Fig 2Forest plot. Surgical care bundles to reduce the risk of surgical site infections.
      The 3 studies that did not provide sufficient data to be included in the meta-analysis had varying findings.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Larochelle M.
      • Hyman N.
      • Gruppi L.
      • et al.
      Diminishing surgical site infection after colorectal surgery with surgical care improvement project: is it time to move on?.
      • Wick E.C.
      • Gibbs L.
      • Indorf L.A.
      • et al.
      Implementation of quality measures to reduce surgical site infection in colorectal patients.
      One study, which focused on improving compliance, reported a sample size that was too small to draw any definite conclusions.
      • Wick E.C.
      • Gibbs L.
      • Indorf L.A.
      • et al.
      Implementation of quality measures to reduce surgical site infection in colorectal patients.
      The second study found no increase in compliance with any bundle interventions and found no change in SSI rates.
      • Larochelle M.
      • Hyman N.
      • Gruppi L.
      • et al.
      Diminishing surgical site infection after colorectal surgery with surgical care improvement project: is it time to move on?.
      The third study found that, although reported adherence to core interventions increased, SSI rates remained unchanged.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.

      Discussion

      To date, no systematic review has been published in the peer literature examining the effect of care bundles on SSI rates among any surgical patient groups. Our study represents the first systematic review of selective surgical care bundles used to reduce SSIs in patients undergoing colorectal surgery. The current collective meta-analysis comprises >8,500 patients, documenting that use of a surgical care bundle, comprising selective evidence-based interventions, results in a significant reduction in the rate of SSI in the colorectal patient population. One randomized, highly ranked, well-designed study evaluating the use of surgical care bundles found that selected care bundle elements were not effective in decreasing the risk of SSI.
      • Anthony T.
      • Murray B.W.
      • Sum-Ping J.
      • et al.
      Evaluating an evidence-based bundle for preventing surgical site infection: a randomized trial.
      A possible reason for the contrary results of this randomized trial may have been associated with the specific interventions chosen for this particular care bundle; these interventions included the elimination of mechanical bowel preparation, removal of oral antibiotic preparation, restriction of intraoperative fluid administration, and use of wound protectors, which have limited, or conflicting, supportive documentation.
      • Guenaga K.F.
      • Matos D.
      • Wille-Jorgensen P.
      Mechanical bowel preparation for elective colorectal surgery.
      • Morris M.S.
      • Graham L.A.
      • Chu D.I.
      • et al.
      Oral antibiotic bowel preparation significantly reduces surgical site infection rates and readmission rates in elective colorectal surgery.
      The majority of the reviewed studies included a group of “core,” evidence-based interventions, comprising appropriate antibiotic management, appropriate hair removal, maintenance of normothermia, and glycemic control. The justification for inclusion of these 4 core measures, especially in US-based publications, is associated with the Centers for Medicare and Medicaid Services mandating the use of these 4 measures for all patients undergoing colorectal surgery.
      • Fry D.E.
      Surgical site infections and the surgical care improvement project (SCIP): evolution of national quality measures.
      These 4 interventions were also a core requirement for the statewide, surgical care bundle implemented by the Michigan Surgical Quality Collaborative.
      • Henke P.K.
      • Kubus J.
      • Englesbe M.J.
      • et al.
      A statewide consortium of surgical care: a longitudinal investigation of vascular operative procedures at 16 hospitals.
      The evidence to support these selective interventions is relatively strong, based on randomized trials and systematic reviews; however, level 1 evidence is lacking for several of the “non-core” interventions included in many of the care bundles analyzed in this review.
      Assessing the reported compliance rate associated within each bundle intervention was problematic throughout this review. Compliance was particularly important as many bundle interventions were implemented already before the introduction of the full surgical care bundle. It was necessary, therefore, to know baseline and postimplementation compliance rates to determine whether uptake of the selective bundle elements had increased. Although almost all of the studies reported compliance data, 4 studies did not provide a compliance rate for both baseline and cohort groups.
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      • Lutfiyya W.
      • Parsons D.
      • Breen J.
      A colorectal “care bundle” to reduce surgical site infections in colorectal surgeries: a single-center experience.
      Seven studies did report the percentage of patients who received the entire surgical care bundle
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Anthony T.
      • Murray B.W.
      • Sum-Ping J.
      • et al.
      Evaluating an evidence-based bundle for preventing surgical site infection: a randomized trial.
      • Bull A.
      • Wilson J.
      • Worth L.J.
      • et al.
      A bundle of care to reduce colorectal surgical infections: An Australian experience.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      • Pastor C.
      • Artinyan A.
      • Varma M.G.
      • et al.
      An increase in compliance with the surgical care improvement project measures does not prevent surgical site infection in colorectal surgery.
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      ; compliance with the complete bundle was variable with reported rates ranging from 2.1 to 92%.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      This observation suggests that, while there is recognition of the benefit of a surgical care bundle as an effective strategy to improving patient outcomes, full implementation is limited. Furthermore, in the case of the study by Waits et al,
      • Waits S.A.
      • Fritze D.
      • Banerjee M.
      • et al.
      Developing and argument for bundled interventions to reduce surgical site infections in colorectal surgery.
      there was a direct correlation between implementation (full versus partial) of a surgical care bundle and colorectal SSI rate.
      Implementing an effective SSI surgical care bundle requires a fiscal and logistical commitment on the part of the health care institution to cover staff time, effort, and consumables. At present, there are insufficient data to conduct economic modelling to determine the cost-effectiveness of a surgical care bundle for reducing the risk of SSI among colorectal patients. Four of the studies included in this review do, however, discuss the probable cost benefits or expenses associated with executing a surgical care bundle.
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      One Dutch study identified an annual implementation cost of approximately $50,000, although these funds were used for dedicated staff members who were involved in the project.
      • Crolla R.M.P.H.
      • van der Laan L.
      • Veen E.J.
      • et al.
      Reduction of surgical site infections after implementation of a bundle of care.
      This bundle was deemed by the authors to be cost effective because there was an estimated annual savings of $234,261 through a reduction in duration of hospitalization. In another study, Keenan et al
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      found that the reduction in superficial SSIs as a result of bundle implementation was associated with a 36% increase in variable direct costs, from $9,779 to $13,253. Variable direct costs were defined as the costs incurred during hospitalization, including operating room time, equipment, drugs, and nursing and laboratory services, but excluding physician's time. Keenen et al
      • Keenan J.E.
      • Speicher P.J.
      • Thacker J.K.
      • et al.
      The Preventative Surgical Site Infection Bundle in Colorectal Surgery: an effective approach to surgical site infection reduction and health care cost savings.
      suggest that the increase in variable direct costs may have been influenced by inflationary health care costs or charges associated directly with post-operative care management unrelated to the care bundle process. Berenguer et al
      • Berenguer C.M.
      • Ochsner M.G.
      • Lord S.A.
      • et al.
      Improving surgical site infections: Using national surgical quality improvement program data to institute surgical care improvement project protocols in improving surgical outcomes.
      calculated the average, in-patient cost of a superficial SSI at $8,900 and assumed that the implementation of the bundle would result in a cost savings. Liau et al
      • Liau K.
      • Aung K.
      • Chua N.
      • et al.
      Outcome of a strategy to reduce surgical site infection in a tertiary-care hospital.
      estimated that the average cost of treating each SSI in Thailand was $1,532 and reported an overall saving of $147,967 during the 2-year study. Alfonso et al
      • Alfonso J.L.
      • Pereperez S.B.
      • Canoves J.M.
      • et al.
      Are we really seeing the total costs of surgical site infections?.
      suggested that the average cost of an SSI, including direct, indirect, and societal costs, has been underestimated grossly and more accurately approaches $100,000, of which the health care cost is approximately 10%. In the effort to calculate the cost of an SSI, few authors factor into the equation the societal cost or the economic impact that an SSI may have on quality of life or economic productivity after infection. While it is difficult to arrive at a consensus of the economic benefit of embracing a strategy of surgical care bundles, enhanced compliance, especially of the core processes, will likely be cost effective for the majority of patients undergoing colorectal surgery.
      The present study has 2 limitations. The first is a failure of some of the studies to report a bundle compliance rate, and the second, a failure in the consistency of SSI data collection, with studies reporting a range of methods used within active and passive programs of surveillance. These 2 limitations could have led to an underestimation of the overall clinical benefit of embracing a strategy of surgical care bundles. That said, a thoughtful and thorough review of the current peer literature suggests that implementation of an approach using surgical care bundles has a significant impact on reducing the risk of SSI in elective colorectal surgery.
      A final comment worthy of consideration is: what comprised the optimal surgical care bundle for decreasing the risk of colorectal SSIs? Selective core elements such as normothermia, glycemic control, timely and appropriate antimicrobial prophylaxis, and appropriate hair removal should be viewed as representing baseline consideration. These selective elements by themselves, however, are not sufficient to provide the comprehensive risk reduction benefit required to reduce the overall risk of infection.
      • Hawn M.T.
      • Vick C.C.
      • Richman J.
      • et al.
      Surgical site infection prevention: time to move beyond the surgical care improvement program.
      • Pastor C.
      • Artinyan A.
      • Varma M.G.
      • et al.
      An increase in compliance with the surgical care improvement project measures does not prevent surgical site infection in colorectal surgery.
      • Edmiston C.E.
      • Spencer M.
      • Lewis B.D.
      • et al.
      Reducing the risk of surgical site infections: did we really think that SCIP would lead us to the promise land?.
      Additional evidence-based interventions warrant further consideration, including supplemental oxygen, chlorhexidine gluconate pre-admission showers or cleansing, wound protectors, a separate surgical tray for fascia and skin closure, antimicrobial sutures for fascial and skin closure, and mechanical bowel preparation plus oral antibiotics. Regardless of the interventions, it is the consistent implementation of all measures within the bundle which ensures the success of the bundle. This review highlights the variation in compliance among the included studies and identifies the systematic implementation of the bundle approach as an area which warrants further study.
      At present, there is no consensus as to what comprises the optimal colorectal surgical care bundle. However, this systematic review suggests that a multidisciplinary approach, utilizing selective, evidence-based core strategies along with adjunctive interventions that enhance wound defense mechanisms while limiting exogenous, intraoperative contamination will result in a reduced risk of infection in the colorectal patient population.
      The authors thank Ann Bull and Kui Hin Liau for contributing additional data from their research, which allowed us to improve the quality of this systematic review. The conclusions of this study represent the collective efforts of JT, OA, MK, WP, DL, and CE and were not influenced by any proprietary party. The authors have no conflict of interest to report.

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