Implementation strategies to reduce surgical site infections: A systematic review

Promise Ariyo; Bassem Zayed; Victoria Riese; Blair Anton; Asad Latif; Claire Kilpatrick; Benedetta Allegranzi; Sean Berenholtz

doi:10.1017/ice.2018.355

Implementation strategies to reduce surgical site infections: A systematic review

Published online by Cambridge University Press: 21 February 2019

Benedetta Allegranzi and

Sean Berenholtz

Show author details

Promise Ariyo*: Affiliation:
Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States
Bassem Zayed: Affiliation:
Antimicrobial Resistance and Infection Control Team, WHO Regional Office for Eastern Mediterranean, Cairo, Egypt
Victoria Riese: Affiliation:
Welch Medical Library, Johns Hopkins University, School of Medicine, Baltimore, Maryland, United States
Blair Anton: Affiliation:
Welch Medical Library, Johns Hopkins University, School of Medicine, Baltimore, Maryland, United States
Asad Latif: Affiliation:
Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States
Claire Kilpatrick: Affiliation:
Infection Prevention and Control Global Unit, Department of Service Delivery and Safety, World Health Organization, Geneva, Switzerland
Benedetta Allegranzi: Affiliation:
Infection Prevention and Control Global Unit, Department of Service Delivery and Safety, World Health Organization, Geneva, Switzerland
Sean Berenholtz: Affiliation:
Department of Anesthesiology and Critical Care Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, United States
*: Author for correspondence: Promise Ariyo, Email: pariyo1@jhmi.edu

Article contents

Abstract
Background:
Objective:
Design:
Methods:
Results:
Conclusions:
Methods
Results
Discussion
Supplementary material
Author ORCIDs
Financial support
Conflicts of interest
References

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Abstract

Background:

Surgical site infections (SSIs) portend high patient morbidity and mortality. Although evidence-based clinical interventions can reduce SSIs, they are not reliably delivered in practice, and data are limited on the best approach to improve adherence.

Objective:

To summarize implementation strategies aimed at improving adherence to evidence-based interventions that reduce SSIs.

Design:

Systematic review

Methods:

We searched PubMed, Embase, CINAHL, the Cochrane Library, the WHO Regional databases, AFROLIB, and Africa-Wide for studies published between January 1990 and December 2015. The Effective Practice and Organization Care (EPOC) criteria were used to identify an acceptable-quality study design. We used structured forms to extract data on implementation strategies and grouped them into an implementation model called the “Four Es” framework (ie, engage, educate, execute, and evaluate).

Results:

In total, 125 studies met our inclusion criteria, but only 8 studies met the EPOC criteria, which limited our ability to identify best practices. Most studies used multifaceted strategies to improve adherence with evidence-based interventions. Engagement strategies included multidisciplinary work and strong leadership involvement. Education strategies included various approaches to introduce evidence-based practices to clinicians and patients. Execution strategies standardized the interventions into simple tasks to facilitate uptake. Evaluation strategies assessed adherence with evidence-based interventions and patient outcomes, providing feedback of performance to providers.

Conclusions:

Multifaceted implementation strategies represent the most common approach to facilitating the adoption of evidence-based practices. We believe that this summary of implementation strategies complements existing clinical guidelines and may accelerate efforts to reduce SSIs.

Information

Type: Original Article
Information: Infection Control & Hospital Epidemiology , Volume 40 , Issue 3 , March 2019, pp. 287 - 300
DOI: https://doi.org/10.1017/ice.2018.355 [Opens in a new window]
Copyright: © 2019 by The Society for Healthcare Epidemiology of America. All rights reserved.

Surgical site infection (SSI) is a global problem associated with increased mortality, hospital length of stay, hospital readmissions, and costs.Reference Kirkland, Briggs, Trivette, Wilkinson and Sexton¹^–Reference Graf, Ott and Vonberg⁵ In the United States, SSIs added >1 million patient days and $1.6 billion in costs in 2005.Reference de Lissovoy, Fraeman, Hutchins, Murphy, Song and Vaughn⁶ In Europe, between 2013 and 2014, SSIs varied by surgical procedure from 0.6% to 9.5% per 100 procedures.⁷ In low- and middle-income countries (LMICs), SSIs are the most frequent healthcare-associated infection (HAI).Reference Allegranzi, Bagheri Nejad and Combescure⁴ Compelling evidence shows that several effective interventions prevent SSIs, and both the World Health Organization (WHO) and the US Centers for Disease Control and Prevention (CDC) recently issued guidelines outlining the most appropriate prevention measures.Reference Berrios-Torres, Umscheid and Bratzler⁸^–¹² However, evidence-based recommendations are often not delivered at the bedside.Reference Davis, Evans and Jadad¹³^–Reference Leaper, Tanner, Kiernan, Assadian and Edmiston¹⁵ One possible explanation is limited guidance on translating evidence-based recommendations into routine practice.

Several approaches have been described to improve adherence with evidence-based interventions.Reference Grol¹⁶^, Reference Gagliardi, Brouwers, Palda, Lemieux-Charles and Grimshaw¹⁷ One practical implementation model used to translate evidence into practice is known as the “Four Es”: engage, educate, execute, and evaluate.Reference Pronovost, Berenholtz and Needham¹⁸ Use of this model has been associated with significant and sustained reductions in HAIs, including state and national collaborative programs.Reference Pronovost, Needham and Berenholtz¹⁹^–Reference Berenholtz, Lubomski and Weeks²³ This model also has been used in initiatives to prevent thromboembolic events and to increase early mobility practices among hospitalized patients.Reference Streiff, Carolan and Hobson²⁴^, Reference Needham, Korupolu and Zanni²⁵ This model focuses on administrative and clinical stakeholders and has technical and adaptive (cultural) work to foster the translation of evidence into bedside practice. Finally, the Four Es model was recently incorporated into expert guidance documents to support efforts to translate recommendations for HAI prevention into practice and accelerate improvement efforts.Reference Septimus, Yokoe, Weinstein, Perl, Maragakis and Berenholtz²⁶

We conducted a systematic review of the literature to identify studies describing implementation strategies to improve adherence with evidence-based SSI-prevention interventions. Our objective was to summarize implementation strategies using the Four-E framework and highlight the adaptation of these strategies in LMICs.

Methods

Data sources and search strategy

We searched the following databases: PubMed, EMBASE, CINAHL, Cochrane Library, and WHO Regional databases, including AFROLIB and Africa-wide information on EBSCO for articles published from January 1, 1990, through December 31, 2015. We used a comprehensive database-specific combination of terms, including medical subject headings (MeSH) related to SSI and prevention measures (Appendix 1).

Inclusion and exclusion criteria

Eligible studies described strategies to increase adherence with evidence-based interventions known to reduce SSI during the study period and reported SSI outcomes. For the purpose of our analysis, we used the 1988–2009 CDC guidelines for the prevention of SSI and the 2009 WHO guidelines for safe surgery.¹²^, Reference Mangram, Horan, Pearson, Silver and Jarvis²⁷ We included experimental, observational studies, randomized controlled trials (RCT), controlled before-and-after (CBA) studies, interrupted time series (ITS) studies, and quality improvement (QI) initiatives. All surgical patient populations and settings (inpatient or outpatient), and patients of all age groups were included. We excluded systematic reviews, meta-analyses, case reports, editorials or commentaries, and conference proceedings. In addition, we restricted the search to studies written in English, French, and Spanish.

Study selection and data extraction

Articles were selected in several phases (Fig. 1). First, 6 reviewers independently screened titles and generated a list of potential abstracts for inclusion. Second, 4 authors (P.A., V.R., B.A., and B.Z.) independently reviewed the abstracts, identified articles for full-text review, and read the articles for eligibility. Data extracted from each study included author, study year and country, income level of country (low-middle or high, as defined by the World Bank²⁸), setting, patient population (pediatric or adult, inpatient or outpatient), surgical specialty, infection prevention measures, compliance data, and SSI outcomes. Study quality was appraised with the Effective Practice and Organization of Care (EPOC) criteria, which considers RCTs, non-RCTs, CBA, and ITS as acceptable quality.²⁹

Fig. 1.

Systematic review study flow diagram. Note. SSI, surgical site infection; EPOC, Effective Practice and Organization of Care.

Analysis of implementation strategies

We summarized implementation strategies according to 1 of the Four Es framework categories (ie, engage, educate, execute, or evaluate). These categories were not always mutually exclusive; reviewers decided on the best fit through group consensus. We extracted key stakeholders and compared studies that did and did not demonstrate a decrease in SSI to highlight some differences in implementation approaches.Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^–Reference Wilson, Hodgson and Liu³²

Results

We identified 13,798 records in our initial search and 2 articles from reference lists of the identified studies (Fig. 1). After removing duplicates, 9,823 unique titles remained, of which 7,342 were excluded because inclusion criteria were not met. Of the remaining 2,481 records, 2,106 were excluded because our study objective was not met or an abstract was not provided. The remaining 375 studies underwent full-text review. Of those, 255 were excluded because SSI rates were not reported, leaving 120 studies in our final analysis. An additional 5 studies were identified from another search of systematic reviews, providing 125 studies in our final analysis. The analysis included 124 cohort studies and 1 RCT.

Demographic characteristics

Overall, 105 studies (84%) were conducted in high-income countries and 20 (16%) in LMICs (Appendix 2). Also, 14 studies (12%) evaluated a pediatric population, Reference Adler, Martin and Cohen³³^–Reference Woodward, Son, Taylor and Husain⁴⁶ and 111 (88%) evaluated an adult, mixed (adult and pediatric), or undefined population. We quantified the studies by surgical specialty: 21 cardiothoracic,Reference Adler, Martin and Cohen³³^, Reference Izquierdo-Blasco, Campins-Marti and Soler-Palacin³⁶^, Reference Jenkins, Castaneda and Cherian³⁷^, Reference Murray, Corda, Turcotte, Bacha, Saiman and Krishnamurthy³⁹^, Reference Nayar, Kennedy and Pappas⁴⁰^, Reference Woodward, Son, Taylor and Husain⁴⁶^–Reference Jog, Cunningham and Cooper⁶¹ 22 orthopedic,Reference Ballard, Miller, Nyquist, Elise, Baulesh and Erickson³⁴^, Reference Ryan, Sen, Staggers, Luerssen and Jea⁴¹^, Reference Ryckman, Schoettker and Hays⁴²^, Reference Acklin, Widmer, Renner, Frei and Gross⁶²^–Reference Kim, Spencer and Davidson⁸⁰ 13 obstetrics and gynecology,Reference Brisibe, Ordinioha and Gbeneolol⁸¹^–Reference Wu, Sun and Shyr⁹³ 23 gastrointestinal,Reference Aguilar-Nascimento, Caporossi, Bicudo, Silva, Santos and Cardoso⁹⁴^–Reference Bull, Wilson and Worth¹¹⁶ 3 neurosurgery,Reference Hover, Sistrunk and Cavagnol¹¹⁷^–Reference Lepanluoma, Rahi, Takala, Loyttyniemi and Ikonen¹¹⁹ 2 plastic surgery,Reference Schonmeyr, Restrepo, Wendby, Gillenwater and Campbell⁴⁴^, Reference Biskup, Workman, Kutzner, Adetayo and Gupta¹²⁰ 28 multiple specialities,Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^–Reference Wilson, Hodgson and Liu³²^, Reference Toltzis, O’Riordan and Cunningham⁴⁵^, Reference Schweizer, Chiang and Septimus⁵⁹^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^–Reference Yegge, Gase, Hopkins-Broyles, Leone, Trovillion and Babcock¹⁴³ and 13 undefined speciality.Reference Kelly, Wenger, Horton, Nuss, Croitoru and Pestian³⁸^, Reference Schaffzin, Harte and Marquette⁴³^, Reference Barchitta, Matranga and Quattrocchi¹⁴⁴^–Reference Takahashi, Takesue and Nakajima¹⁵⁴

Adherence to SSI prevention measures

Of the 70 studies (56%) that provided data on adherence with SSI preventive measures, 95% reported an increase in compliance with prevention measures. However, 37 studies (28%) did not statistically evaluate the impact of interventions on SSI rates. Of the remaining 88 studies, 61 (69%) reported significant decreases in SSIs,Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^, Reference Wilson, Hodgson and Liu³²^, Reference Adler, Martin and Cohen³³^, Reference Izquierdo-Blasco, Campins-Marti and Soler-Palacin³⁶^, Reference Jenkins, Castaneda and Cherian³⁷^, Reference Ryan, Sen, Staggers, Luerssen and Jea⁴¹^, Reference Chien, Lin and Hsu⁴⁷^–Reference Hogle, Cohen, Hyman, Larson and Fowler⁵⁰^, Reference Miyahara, Matsuura, Takemura, Mizutani, Saito and Toyama⁵⁴^, Reference Singh, Kumar, Sundaram, Kanjilal and Nair⁵⁶^, Reference Trussell, Gerkin and Coates⁵⁷^, Reference Schweizer, Chiang and Septimus⁵⁹^–Reference Acklin, Widmer, Renner, Frei and Gross⁶²^, Reference Johnson, Starks, Bancroft and Roberts⁶⁶^, Reference Kawamura, Matsumoto and Shigemi⁶⁸^–Reference Mejia, Williams and Long⁷⁰^, Reference Sanchez-Hernandez, Saez-Lopez, Paniagua-Tejo and Valverde-Garcia⁷⁴^, Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Rao, Cannella, Crossett, Yates, McGough and Hamilton⁷⁸^, Reference Kim, Spencer and Davidson⁸⁰^, Reference Corcoran, Jackson, Coulter-Smith, Loughrey, McKenna and Cafferkey⁸³^–Reference Hickson, Harris and Brett⁸⁵^, Reference Rauk⁸⁷^–Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Aguilar-Nascimento, Caporossi, Bicudo, Silva, Santos and Cardoso⁹⁴^, Reference de Aguilar-Nascimento, Bicudo-Salomao, Caporossi, Silva, Cardoso and Santos⁹⁵^, Reference Connolly, Foppa, Kazi, Denoya and Bergamaschi⁹⁷^, Reference Hedrick, Heckman, Smith, Sawyer, Friel and Foley¹⁰²^, Reference Keenan, Speicher and Nussbaum¹⁰⁵^, Reference Lavu, Klinge and Nowcid¹⁰⁸^, Reference Perez-Blanco, Garcia-Olmo, Maseda-Garrido, Najera-Santos and Garcia-Caballero¹¹⁰^, Reference Waits, Fritze and Banerjee¹¹²^, Reference Wick, Galante and Hobson¹¹³^, Reference Cima, Dankbar and Lovely¹¹⁵^, Reference Hover, Sistrunk and Cavagnol¹¹⁷^, Reference Le, Guppy and Axelrod¹¹⁸^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^, Reference Brandt, Sohr, Behnke, Daschner, Ruden and Gastmeier¹²⁴^, Reference El Mhamdi, Letaief, Cherif, Bouanene, Kallel and Hamdi¹²⁶^, Reference Geubbels, Bakker and Houtman¹²⁷^, Reference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹^, Reference Kim, Kwakye and Kwok¹³²^, Reference Kwok, Funk and Baltaga¹³⁴^, Reference Liau, Aung and Chua¹³⁵^, Reference Suchitra and Lakshmidevi¹³⁸^, Reference Thompson, Oldenburg, Deschamps, Rupp and Smith¹³⁹^, Reference Barchitta, Matranga and Quattrocchi¹⁴⁴^, Reference Everett, Sitton and Wilson¹⁴⁵^, Reference Marchi, Pan and Gagliotti¹⁴⁸^, Reference Prospero, Barbadoro, Marigliano, Martini and D’Errico¹⁵⁰^, Reference Starling, Couto and Pinheiro¹⁵²^, Reference Takahashi, Takesue and Nakajima¹⁵⁴ and 21 (24%) reported no change or no statistical decrease in SSIs.Reference van Kasteren, Mannien and Kullberg³¹^, Reference Ballard, Miller, Nyquist, Elise, Baulesh and Erickson³⁴^, Reference Murray, Corda, Turcotte, Bacha, Saiman and Krishnamurthy³⁹^, Reference Woodward, Son, Taylor and Husain⁴⁶^, Reference Rao, Schilling, Rice, Ridenour, Mook and Santa⁵⁵^, Reference Usry, Johnson, Weems and Blackhurst⁵⁸^, Reference Schweizer, Chiang and Septimus⁵⁹^, Reference Boaz, Bermant and Ezri⁷⁷^, Reference Hadley, Immerman, Hutzler, Slover and Bosco⁷⁹^, Reference Brisibe, Ordinioha and Gbeneolol⁸¹^, Reference Hill, Holubar, Garfield Legare, Luurtsema and Barth⁹⁹^, Reference Forbes, Stephen and Harper¹⁰⁰^, Reference Hedrick, Heckman, Smith, Sawyer, Friel and Foley¹⁰²^, Reference Larochelle, Hyman, Gruppi and Osler¹⁰⁷^, Reference Miller, Thacker and White¹⁰⁹^, Reference Biskup, Workman, Kutzner, Adetayo and Gupta¹²⁰^, Reference Askarian, Kouchak and Palenik¹²³^, Reference Dimopoulou, Kourlaba, Psarris, Coffin, Spoulou and Zaoutis¹²⁵^, Reference Neumayer, Mastin, Vanderhoof and Hinson¹³⁶^, Reference Tillman, Wehbe-Janek, Hodges, Smythe and Papaconstantinou¹⁴⁰^, Reference Yang, Zhao and Wang¹⁴² However, 2 studies (2%), including 1 RCT, reported increased SSIs.Reference Anthony, Murray and Sum-Ping⁹⁶^, Reference Koch, Nilsen, Dalheim, Cox and Harthug¹³³

Overall, 103 studies (82%) used multifaceted strategies to promote adherence to prevention measures. The most common measure was appropriate use of surgical antibiotic prophylaxis, which was reported in 86 of the 125 studies (68%) and in 14 of the 20 (70%) studies conducted in LMICs.Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^, Reference Jenkins, Castaneda and Cherian³⁷^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Khan, Rao, Rao and Rodrigues¹⁰⁶^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^–Reference Askarian, Kouchak and Palenik¹²³^, Reference El Mhamdi, Letaief, Cherif, Bouanene, Kallel and Hamdi¹²⁶^, Reference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹^, Reference Kim, Kwakye and Kwok¹³²^, Reference Kwok, Funk and Baltaga¹³⁴^, Reference Suchitra and Lakshmidevi¹³⁸^, Reference Yang, Zhao and Wang¹⁴²^, Reference Starling, Couto and Pinheiro¹⁵² Other common prevention measures were surgical site preparation (31%), hair removal techniques (25%), normothermia (20%), glycemic control (18%), wound care (17%), preoperative bathing (16%), operating room discipline/traffic (14%), instrument sterilization (13%), hand hygiene (11%), preoperative cleansing (14%), and gloving techniques (8%) (Table 1).

Table 1.

Common Infection Prevention Measures

Note. IPC, infection prevention and control; OR, operating room.

Implementation of SSI prevention strategies using the Four Es framework

Most studies used multifaceted strategies to improve adherence with evidence-based SSI prevention measures. Moreover, 76 studies (63%) described efforts to engage frontline staff as an important strategy to improve adherence with prevention measures. Also, 65 studies (54%) used some form of education to introduce the measures to frontline staff, compared to only 11% of studies that focused on patient education. Execution strategies to improve adherence were described by 108 studies (86%). In addition, 74 studies (59%) described evaluation activities. Overall, only 8 studies (6%) met the EPOC criteria, which limited our ability to identify best practices in the remaining 117 studies.

Engagement

Among all of the studies, 76 (63%) described efforts to engage frontline staff as an implementation strategy, largely by forming multidisciplinary teams. The range of disciplines included surgeons, anesthesia providers, perioperative nurses, pharmacists, and infection prevention control specialists. Multidisciplinary teams reviewed existing SSI prevention practices and identified opportunities for improvement, developed interventions, measured progress, and gave feedback to hospital staff.Reference Adler, Martin and Cohen³³^, Reference Thompson, Oldenburg, Deschamps, Rupp and Smith¹³⁹^, Reference van der Slegt, van der Laan, Veen, Hendriks, Romme and Kluytmans¹⁵⁵ In 7 studies, the role of team champions in SSI improvement efforts was described.Reference Jenkins, Castaneda and Cherian³⁷^, Reference Ryckman, Schoettker and Hays⁴²^, Reference Hogle, Cohen, Hyman, Larson and Fowler⁵⁰^, Reference Rovaldi and King⁷³^, Reference Dimopoulou, Kourlaba, Psarris, Coffin, Spoulou and Zaoutis¹²⁵^, Reference Horst, Rubinfeld and Mlynarek¹³⁰^, Reference Kanter, Connelly and Fitzgerald¹³¹ Team champions were enthusiastic individuals identified across the institution. They included frontline staff such as surgeons, anesthesiologists, nurses, and team members in leadership positions, including administrators and hospital executives. They often provided important leadership to engage and coach teams and managed resources to foster the desired change.Reference Rovaldi and King⁷³^, Reference Forbes, Stephen and Harper¹⁰⁰^, Reference Dimopoulou, Kourlaba, Psarris, Coffin, Spoulou and Zaoutis¹²⁵^, Reference Wick, Hobson and Bennett¹⁵⁶

Also, 15 studies highlighted the importance of partnering multidisciplinary teams with senior leaders.Reference Toltzis, O’Riordan and Cunningham⁴⁵^, Reference Kles, Murrah, Smith, Baugus-Wellmeier, Hurry and Morris⁵¹^, Reference Mejia, Williams and Long⁷⁰^, Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Brisibe, Ordinioha and Gbeneolol⁸¹^, Reference Dyrkorn, Kristoffersen and Walberg⁸⁴^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Reames, Krell, Campbell and Dimick¹¹¹^, Reference Wick, Galante and Hobson¹¹³^, Reference Hover, Sistrunk and Cavagnol¹¹⁷^, Reference Horst, Rubinfeld and Mlynarek¹³⁰^, Reference Ng and Awad¹³⁷^, Reference Thompson, Oldenburg, Deschamps, Rupp and Smith¹³⁹^, Reference Joyce, Cioffi, Petriwsky and Robinson¹⁴⁷^, Reference Wick, Hobson and Bennett¹⁵⁶ Hospital leadership communicated to clinical staff the goals and expectations to decrease SSIs, and in some studies a designated hospital executive was engaged in the work, met with improvement teams, provided resources, and helped teams overcome organizational barriers.Reference Ryckman, Schoettker and Hays⁴²^, Reference Horst, Rubinfeld and Mlynarek¹³⁰^, Reference Wick, Hobson and Bennett¹⁵⁶

Studies in LMICs frequently described multidisciplinary and multidepartmental efforts to prevent SSIs, fostering buy-in and input from providers and encouraging local ownership of the process. These QI initiatives were led and motivated by various groups, including the department of surgery,Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Aguilar-Nascimento, Caporossi, Bicudo, Silva, Santos and Cardoso⁹⁴^, Reference de Aguilar-Nascimento, Bicudo-Salomao, Caporossi, Silva, Cardoso and Santos⁹⁵^, Reference Khan, Rao, Rao and Rodrigues¹⁰⁶ clinical staff and clinical epidemiologists,Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ hospital management,Reference Brisibe, Ordinioha and Gbeneolol⁸¹ infection prevention control specialists,Reference Singh, Kumar, Sundaram, Kanjilal and Nair⁵⁶^, Reference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹ pharmacists,Reference Yang, Zhao and Wang¹⁴² local investigators and clinical researchers (Table 2).Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^, Reference Jenkins, Castaneda and Cherian³⁷^, Reference Schonmeyr, Restrepo, Wendby, Gillenwater and Campbell⁴⁴^, Reference Starčević, Munitlak, Mijović, Mikić and Suljagić⁷⁶^, Reference Kwok, Funk and Baltaga¹³⁴^, Reference Suchitra and Lakshmidevi¹³⁸^, Reference Starling, Couto and Pinheiro¹⁵² Of 20 LMIC studies, 8 (40%) implemented local teams comprising multiple clinical specialties, administrators, and leadership.Reference Jenkins, Castaneda and Cherian³⁷^, Reference Singh, Kumar, Sundaram, Kanjilal and Nair⁵⁶^, Reference Brisibe, Ordinioha and Gbeneolol⁸¹^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Khan, Rao, Rao and Rodrigues¹⁰⁶^, Reference Anchalia and D’Ambruoso¹²²^, Reference Kim, Kwakye and Kwok¹³²^, Reference Starling, Couto and Pinheiro¹⁵² Also, 2 studies noted that government involvement (Iran and Moldova) from their ministry of health was crucial to uptake of the 2009 WHO checklist.Reference Askarian, Kouchak and Palenik¹²³^, Reference Kwok, Funk and Baltaga¹³⁴ Brisibe et alReference Brisibe, Ordinioha and Gbeneolol⁸¹ described a written commitment from hospital management to ensure that the Nigerian teaching hospital received a steady supply of sterile medical supplies.

Table 2.

Included Studies from Low-Middle Income Countries (LMICs)

IPC, infection prevention control; SSI, surgical site infection; Ortho, orthopedic; Ed, educate; Ex, execute; Ev, evaluate; SAP, surgical antimicrobial prophylaxis; CDC, Centers for Disease Control; US, United States; En, engage; CHG, chlorhexidine; GI, gastrointestinal (abdominal); ACERTO, Accelerating the Total Recovery; IVF, intravascular fluid; OR, odds ratio; CI, confidence interval; RCT, randomized controlled trial; WHO, World Health Organization; UK, United Kingdom; OB/GYN, obstetrics and gynecology; BMI, body mass index; HPA, Health Protection Agency of United Kingdom; SWI, sternal wound infection; MRSA, methicillin-resistant Staphylococcus aureus; CTSW, cardiothoracic surgery sternal wounds; TKA, total knee arthroplasty; SF, spinal fusion; SIR, standardized infection ratio; ACS, American College of Surgeons; TSA, time-series analysis; CS, cesarean section; CQI, continuous quality improvement.

Education

In total, 65 studies (54%) used some form of staff education as an implementation strategy. Traditional teaching methods included large-group workshops, didactics, and grand rounds.Reference Ballard, Miller, Nyquist, Elise, Baulesh and Erickson³⁴^, Reference Hogle, Cohen, Hyman, Larson and Fowler⁵⁰^, Reference Garcia-Paris, Cohena-Jimenez, Montano-Jimenez and Cordoba-Fernandez⁶⁴^, Reference Horst, Rubinfeld and Mlynarek¹³⁰^, Reference Kanter, Connelly and Fitzgerald¹³¹ Other methods included peer education, role playing, briefing and debriefing sessions, webinars, and live simulations.Reference Izquierdo-Blasco, Campins-Marti and Soler-Palacin³⁶^, Reference Jenkins, Castaneda and Cherian³⁷^, Reference Schaffzin, Harte and Marquette⁴³^, Reference Haycock, Laser and Keuth⁴⁸^, Reference Garcia-Paris, Cohena-Jimenez, Montano-Jimenez and Cordoba-Fernandez⁶⁴^, Reference Forbes, Stephen and Harper¹⁰⁰^, Reference Reames, Krell, Campbell and Dimick¹¹¹ Haycock et alReference Haycock, Laser and Keuth⁴⁸ implemented an intensive education program that led to an 86% SSI reduction among cardiac surgery patients. Horst et alReference Horst, Rubinfeld and Mlynarek¹³⁰ had clinical nurse specialists and pharmacists teach the glycemic control protocol to nurses at the bedside. Two studies provided more intensive training, spanning months before intervention implementation.Reference Hannan, O’ullivan and Higgins⁴⁹^, Reference Miller, Thacker and White¹⁰⁹ Education was reinforced via refresher courses, online videos, and webinars, and brochures allowed for quick reference.Reference Izquierdo-Blasco, Campins-Marti and Soler-Palacin³⁶^–Reference Kelly, Wenger, Horton, Nuss, Croitoru and Pestian³⁸^, Reference Schaffzin, Harte and Marquette⁴³^, Reference Salim, Braverman, Berkovic, Suliman, Teitler and Shalev⁸⁹^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^, Reference Geubbels, Bakker and Houtman¹²⁷^, Reference Kanter, Connelly and Fitzgerald¹³¹^, Reference Barchitta, Matranga and Quattrocchi¹⁴⁴ Singh et alReference Singh, Kumar, Sundaram, Kanjilal and Nair⁵⁶ conducted before-and-after test comparisons to evaluate the success of their education.

Of 125 studies, 15 (11%) focused on patient education and their shared responsibility for infection prevention.Reference Schonmeyr, Restrepo, Wendby, Gillenwater and Campbell⁴⁴^, Reference McDonald, Clark, Landauer and Kuxhaus⁶⁹^, Reference Mori⁷¹^, Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Rao, Cannella, Crossett, Yates, McGough and Hamilton⁷⁸^, Reference Kim, Spencer and Davidson⁸⁰^, Reference Bullough, Wilkinson, Burns and Wan⁸²^, Reference Hickson, Harris and Brett⁸⁵^, Reference Ng, Brown and Alexander⁸⁶^, Reference Riley, Suda, Tabsh, Flood and Pegues⁸⁸^, Reference Hechenbleikner, Hobson, Bennett and Wick¹⁰¹^, Reference Wick, Galante and Hobson¹¹³^, Reference Cima, Dankbar and Lovely¹¹⁵^, Reference Hover, Sistrunk and Cavagnol¹¹⁷^, Reference John, Nimeri and Ellahham¹⁴⁶ Riley et alReference Riley, Suda, Tabsh, Flood and Pegues⁸⁸ gave patients reading material on skin preparation with presurgery instructions. Aiken et alReference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ used posters to educate patients about the importance of receiving antibiotics before incision and prompt discontinuation after surgery. Also, 2 studies used a preoperative checklist to educate and prepare patients for surgery.Reference McDonald, Clark, Landauer and Kuxhaus⁶⁹^, Reference Mori⁷¹

Of 20 studies with LMIC programs, 12 (60%) used staff education to reduce SSI rates.Reference Jenkins, Castaneda and Cherian³⁷^, Reference Schonmeyr, Restrepo, Wendby, Gillenwater and Campbell⁴⁴^, Reference Singh, Kumar, Sundaram, Kanjilal and Nair⁵⁶^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Khan, Rao, Rao and Rodrigues¹⁰⁶^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^–Reference Askarian, Kouchak and Palenik¹²³^, Reference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹^, Reference Kim, Kwakye and Kwok¹³²^, Reference Yang, Zhao and Wang¹⁴²^, Reference Starling, Couto and Pinheiro¹⁵² A project in Kenya took ∼600 hours of staff meeting time to develop and implement antibiotic best practices.Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ Jenkins et alReference Jenkins, Castaneda and Cherian³⁷ delivered monthly webinars over a 2-year period in 17 LMICs to decrease SSIs among pediatric congenital heart surgery patients. Day-long seminars, Reference de Aguilar-Nascimento, Bicudo-Salomao, Caporossi, Silva, Cardoso and Santos⁹⁵ one-on-one physician training,Reference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹ and online modules designed for both existing and new staff were also described,Reference Singh, Kumar, Sundaram, Kanjilal and Nair⁵⁶ all leading to decreases in SSIs. In 1 LMIC study, Reference Schonmeyr, Restrepo, Wendby, Gillenwater and Campbell⁴⁴ educating patients on wound care by providing illustrated discharge instructions reduced SSIs among patients undergoing cleft lip and palate repair in India.

Execution

Execution strategies were described by 108 of the 125 studies (86%). Execution often focused on streamlining interventions by simplifying and standardizing the care delivery process and creating verification checks. Furthermore, 57 studies (46%) implemented protocols, pathways, and policies to improve adoption of prevention measures.Reference van Kasteren, Mannien and Kullberg³¹^, Reference Ballard, Miller, Nyquist, Elise, Baulesh and Erickson³⁴^, Reference Murray, Corda, Turcotte, Bacha, Saiman and Krishnamurthy³⁹^–Reference Ryan, Sen, Staggers, Luerssen and Jea⁴¹^, Reference Schaffzin, Harte and Marquette⁴³^, Reference Woodward, Son, Taylor and Husain⁴⁶^, Reference Lutarewych, Morgan and Hall⁵³^, Reference Rao, Schilling, Rice, Ridenour, Mook and Santa⁵⁵^–Reference Usry, Johnson, Weems and Blackhurst⁵⁸^, Reference Jog, Cunningham and Cooper⁶¹^, Reference Hutzler, Kraemer, Iaboni, Berger and Bosco⁶⁵^, Reference McDonald, Clark, Landauer and Kuxhaus⁶⁹^, Reference Sanchez-Hernandez, Saez-Lopez, Paniagua-Tejo and Valverde-Garcia⁷⁴^, Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Rao, Cannella, Crossett, Yates, McGough and Hamilton⁷⁸^, Reference Hadley, Immerman, Hutzler, Slover and Bosco⁷⁹^, Reference Brisibe, Ordinioha and Gbeneolol⁸¹^, Reference Corcoran, Jackson, Coulter-Smith, Loughrey, McKenna and Cafferkey⁸³^, Reference Hickson, Harris and Brett⁸⁵^, Reference Rauk⁸⁷^, Reference Salim, Braverman, Berkovic, Suliman, Teitler and Shalev⁸⁹^, Reference Aguilar-Nascimento, Caporossi, Bicudo, Silva, Santos and Cardoso⁹⁴^, Reference de Aguilar-Nascimento, Bicudo-Salomao, Caporossi, Silva, Cardoso and Santos⁹⁵^, Reference Forbes, Stephen and Harper¹⁰⁰^, Reference Hedrick, Heckman, Smith, Sawyer, Friel and Foley¹⁰²^–Reference Hernández-Navarrete, Arribas-Llorente and Solano Bernad¹⁰⁴^, Reference Larochelle, Hyman, Gruppi and Osler¹⁰⁷^, Reference Miller, Thacker and White¹⁰⁹^, Reference Wick, Galante and Hobson¹¹³^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^–Reference Askarian, Kouchak and Palenik¹²³^, Reference Geubbels, Bakker and Houtman¹²⁷^, Reference Horst, Rubinfeld and Mlynarek¹³⁰^, Reference Kanter, Connelly and Fitzgerald¹³¹^, Reference Neumayer, Mastin, Vanderhoof and Hinson¹³⁶^, Reference Yegge, Gase, Hopkins-Broyles, Leone, Trovillion and Babcock¹⁴³^–Reference Everett, Sitton and Wilson¹⁴⁵^, Reference Prospero, Barbadoro, Marigliano, Martini and D’Errico¹⁵⁰^–Reference Starling, Couto and Pinheiro¹⁵²^, Reference Takahashi, Takesue and Nakajima¹⁵⁴ In addition, 43 studies combined measures into a “bundle” of care practices.Reference Adler, Martin and Cohen³³^, Reference Nayar, Kennedy and Pappas⁴⁰^, Reference Ryckman, Schoettker and Hays⁴²^, Reference Schaffzin, Harte and Marquette⁴³^, Reference Woodward, Son, Taylor and Husain⁴⁶^, Reference Chien, Lin and Hsu⁴⁷^, Reference Lutarewych, Morgan and Hall⁵³^, Reference Miyahara, Matsuura, Takemura, Mizutani, Saito and Toyama⁵⁴^, Reference Schweizer, Chiang and Septimus⁵⁹^, Reference Jog, Cunningham and Cooper⁶¹^, Reference Johnson, Starks, Bancroft and Roberts⁶⁶^, Reference Kawamura, Matsumoto and Shigemi⁶⁸^, Reference McDonald, Clark, Landauer and Kuxhaus⁶⁹^, Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Rao, Cannella, Crossett, Yates, McGough and Hamilton⁷⁸^, Reference Hadley, Immerman, Hutzler, Slover and Bosco⁷⁹^, Reference Corcoran, Jackson, Coulter-Smith, Loughrey, McKenna and Cafferkey⁸³^–Reference Rauk⁸⁷^, Reference Anthony, Murray and Sum-Ping⁹⁶^, Reference Crolla, van der Laan, Veen, Hendriks, van Schendel and Kluytmans⁹⁸^–Reference Forbes, Stephen and Harper¹⁰⁰^, Reference Keenan, Speicher and Nussbaum¹⁰⁵^, Reference Larochelle, Hyman, Gruppi and Osler¹⁰⁷^, Reference Lavu, Klinge and Nowcid¹⁰⁸^, Reference Perez-Blanco, Garcia-Olmo, Maseda-Garrido, Najera-Santos and Garcia-Caballero¹¹⁰^, Reference Waits, Fritze and Banerjee¹¹²^, Reference Wick, Galante and Hobson¹¹³^, Reference Cima, Dankbar and Lovely¹¹⁵^, Reference Bull, Wilson and Worth¹¹⁶^, Reference Le, Guppy and Axelrod¹¹⁸^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^, Reference Liau, Aung and Chua¹³⁵^, Reference Ng and Awad¹³⁷^, Reference Thompson, Oldenburg, Deschamps, Rupp and Smith¹³⁹^, Reference Tillman, Wehbe-Janek, Hodges, Smythe and Papaconstantinou¹⁴⁰^, Reference John, Nimeri and Ellahham¹⁴⁶^, Reference van der Slegt, van der Laan, Veen, Hendriks, Romme and Kluytmans¹⁵⁵ In 1 study, SSI were reduced rates by serially introducing a care bundle for cesarean section at a large community hospital.Reference Ng, Brown and Alexander⁸⁶ A study involving 24 hospitals in Michigan showed a dose response in which increased bundle compliance resulted in decreased SSIs, suggesting synergy among prevention measures in the bundle.Reference Waits, Fritze and Banerjee¹¹²

Among the 125 studies, 26 (21%) used checklists to improve the adoption of evidence-based interventions.Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^, Reference Izquierdo-Blasco, Campins-Marti and Soler-Palacin³⁶^, Reference Lindblom, Lytsy and Sandstrom⁵²^, Reference Garcia-Paris, Cohena-Jimenez, Montano-Jimenez and Cordoba-Fernandez⁶⁴^, Reference Johnson, Starks, Bancroft and Roberts⁶⁶^, Reference McDonald, Clark, Landauer and Kuxhaus⁶⁹^, Reference Mori⁷¹^, Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Boaz, Bermant and Ezri⁷⁷^, Reference Ng, Brown and Alexander⁸⁶^, Reference Connolly, Foppa, Kazi, Denoya and Bergamaschi⁹⁷^, Reference Reames, Krell, Campbell and Dimick¹¹¹^, Reference Wick, Galante and Hobson¹¹³^, Reference Biskup, Workman, Kutzner, Adetayo and Gupta¹²⁰^, Reference Askarian, Kouchak and Palenik¹²³^, Reference El Mhamdi, Letaief, Cherif, Bouanene, Kallel and Hamdi¹²⁶^, Reference Kim, Kwakye and Kwok¹³²^, Reference Kwok, Funk and Baltaga¹³⁴^, Reference Tillman, Wehbe-Janek, Hodges, Smythe and Papaconstantinou¹⁴⁰^, Reference Yegge, Gase, Hopkins-Broyles, Leone, Trovillion and Babcock¹⁴³^, Reference Everett, Sitton and Wilson¹⁴⁵^, Reference John, Nimeri and Ellahham¹⁴⁶^, Reference Lepanluoma, Takala, Kotkansalo, Rahi and Ikonen¹⁵⁷ Other studies used order sets,Reference Sechriest, Carney, Kuskowski, Haffner, Mullen and Covey⁷⁵^, Reference Hedrick, Turrentine and Smith¹⁰³^, Reference Pegues¹⁴⁹ electronic reminders,Reference Hechenbleikner, Hobson, Bennett and Wick¹⁰¹^, Reference Cima, Dankbar and Lovely¹¹⁵ and automatic stops for antibioticsReference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹ to create verification checks and to improve adherence.

Many of the LMIC studies adapted the 2009 WHO Surgical Safety Checklist to local needs, Reference Izquierdo-Blasco, Campins-Marti and Soler-Palacin³⁶^, Reference Askarian, Kouchak and Palenik¹²³^, Reference El Mhamdi, Letaief, Cherif, Bouanene, Kallel and Hamdi¹²⁶^, Reference Kim, Kwakye and Kwok¹³²^, Reference Kwok, Funk and Baltaga¹³⁴ protocols,Reference Aguilar-Nascimento, Caporossi, Bicudo, Silva, Santos and Cardoso⁹⁴^, Reference de Aguilar-Nascimento, Bicudo-Salomao, Caporossi, Silva, Cardoso and Santos⁹⁵^, Reference Anchalia and D’Ambruoso¹²² and policiesReference Brisibe, Ordinioha and Gbeneolol⁸¹^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ to simplify and standardize care. In a study conducted in Moldova, local ownership and buy-in were promoted by developing an anesthesia preoperative evaluation template that included several SSI prevention interventions to improve workflow.Reference Kim, Kwakye and Kwok¹³² An Argentinean study described an automatic-stop prophylaxis form that empowered pharmacists to stop prolonged postoperative antimicrobials.Reference Gomez, Acosta-Gnass, Mosqueda-Barboza and Basualdo¹²⁹ Both studies showed significantly decreased SSI rates.

Evaluation

Of 125 studies, 74 studies (59%) described evaluation activities, with a general focus on giving feedback to key stakeholders to support improvement efforts. Some studies used a benchmark approach to compare performance among peers.Reference Wilson, Hodgson and Liu³²^, Reference Usry, Johnson, Weems and Blackhurst⁵⁸^, Reference Larochelle, Hyman, Gruppi and Osler¹⁰⁷^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ Another strategy reported feedback to the frontline providers and hospital leadership.Reference Wick, Galante and Hobson¹¹³ In that study, providing feedback using a dashboard to compare local data to national benchmarks was associated with a significant decrease in SSI rates and improvement in patient outcomes, including SSI, length of stay, and patient satisfaction. One study posted hospital-based newsletters in public places, such as waiting rooms and elevators, to celebrate staff contributions to decreasing SSIs, Reference Joyce, Cioffi, Petriwsky and Robinson¹⁴⁷ and another displayed scorecards of infection rates in patient care areas.Reference Thompson, Oldenburg, Deschamps, Rupp and Smith¹³⁹

In addition, 5 studies implemented prospective SSI surveillance and performance feedback to surgeons as an unimodal implementation strategy.Reference Wilson, Hodgson and Liu³²^, Reference Starčević, Munitlak, Mijović, Mikić and Suljagić⁷⁶^, Reference Brandt, Sohr, Behnke, Daschner, Ruden and Gastmeier¹²⁴^, Reference Marchi, Pan and Gagliotti¹⁴⁸^, Reference Staszewicz, Eisenring, Bettschart, Harbarth and Troillet¹⁵³ In 1 multicenter study, 34 hospitals participating in a Dutch surveillance network collected SSI data and provided feedback exhibited significant decreases in SSI rates over 5 years.Reference Geubbels, Nagelkerke, Mintjes-De, Vandenbroucke-Grauls, Grobbee and De Boer¹²⁸ Other studies similarly showed that raising awareness among surgeons about infection rates could lead to practice change and improvements in outcomes.Reference Wilson, Hodgson and Liu³²^, Reference Taylor, Buchanan-Chell, Kirkland, McKenzie, Sutherland and Wiens¹⁵⁸

Of 20 LMIC studies, 11 (55%) emphasized evaluation and feedback as an implementation strategy.Reference Jenkins, Castaneda and Cherian³⁷^, Reference Starčević, Munitlak, Mijović, Mikić and Suljagić⁷⁶^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Aguilar-Nascimento, Caporossi, Bicudo, Silva, Santos and Cardoso⁹⁴^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹^, Reference Anchalia and D’Ambruoso¹²²^, Reference El Mhamdi, Letaief, Cherif, Bouanene, Kallel and Hamdi¹²⁶^, Reference Kim, Kwakye and Kwok¹³²^, Reference Kwok, Funk and Baltaga¹³⁴^, Reference Suchitra and Lakshmidevi¹³⁸^, Reference Starling, Couto and Pinheiro¹⁵² In Brazil, the National Nosocomial Infection Surveillance System was used to evaluate performance and provide feedback to providers.Reference Starling, Couto and Pinheiro¹⁵² Other evaluation methods included direct observation and immediate feedback of clinical performance to create a sense of accountability and motivation for improvement.Reference Kwok, Funk and Baltaga¹³⁴^, Reference Starling, Couto and Pinheiro¹⁵² For instance, a tool called the “infectometer” was used in clinical areas to report weekly and monthly HAI rates compared to the expected incidence of infection.Reference Starling, Couto and Pinheiro¹⁵² In Belgrade, active surveillance with feedback alone resulted in a decrease in SSIs among orthopedic patients.Reference Starčević, Munitlak, Mijović, Mikić and Suljagić⁷⁶

Application of EPOC criteria

Only 8 studies met EPOC criteria for inclusion in our analysis (Fig. 1). Overall, we observed no clear differences in implementation strategies between studies that met the EPOC criteria and those that did not. Most of these studies described a multifaceted approach that included efforts to define a common goal for improvement, to engage and educate multidisciplinary teams and senior leaders, to simplify and standardize care (bundles, protocols, policies, and briefings), to collect data and offer performance feedback, and to provide opportunities for shared learning.Reference van Kasteren, Mannien and Kullberg³¹^, Reference Toltzis, O’Riordan and Cunningham⁴⁵^, Reference Schweizer, Chiang and Septimus⁵⁹^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ Many studies specifically commented on the importance of several important factors when implementing best practices (1) senior leadership support, (2) engaging and educating multidisciplinary teams, (3) locally relevant education materials, and (4) an “enabling infrastructure” to collect data, analyze, and provide feedback.Reference Schweizer, Chiang and Septimus⁵⁹^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ The remaining 3 studies described efforts to standardize care (ie, bundles, protocols, and policies) but provided little to no information about additional implementation strategies (Table 3).Reference Rao, Cannella, Crossett, Yates, McGough and Hamilton⁷⁸^, Reference Hadley, Immerman, Hutzler, Slover and Bosco⁷⁹^, Reference Anthony, Murray and Sum-Ping⁹⁶

Table 3.

Evidence of Included Studies that Met EPOC Criteria (n=8)

Note. EPOC, Effective Practice and Organization of Care; IPC, infection prevention control; SSI, surgical site infection; Def, definition; TSA, time-series analysis; Ed, educate; Ex, execute; Ev, evaluate; SAP, surgical antimicrobial prophylaxis; CDC, Centers for Disease Control; RCT, randomized controlled trial; NR, not reported; CBA, controlled before-after; CI, confidence interval; En, engage; OB/GYN, Obstetrics and Gynecology; CQI, continuous quality improvement.

Discussion

In this systematic review, we identified 125 studies that described implementation strategies to increase the adoption of evidence-based SSI prevention measures and categorized the strategies according to the Four E framework.Reference Pronovost, Needham and Berenholtz¹⁹^, Reference DePalo, McNicoll, Cornell, Rocha, Adams and Pronovost²⁰^, Reference Berenholtz, Pham and Thompson²²^, Reference Berenholtz, Lubomski and Weeks²³^, Reference Pronovost, Watson, Goeschel, Hyzy and Berenholtz¹⁵⁹ Most of the studies used a multifaceted approach and addressed change at multiple levels within their healthcare organization. These strategies aimed (1) to build and encourage multidisciplinary teamwork, (2) to obtain leadership buy-in, (3) to increase staff and patient awareness and knowledge about SSIs and prevention practices, (4) to standardize and simplify clinical processes, (5) to create verification procedures, and (6) to provide timely feedback to stakeholders to support improvement efforts. Although strategies varied among studies and we were not able to identify the best approach, lessons learned from successful HAI prevention efforts highlighted the importance of employing multifaceted strategies, including engagement, education, execution, and evaluation.Reference Pronovost, Weaver and Berenholtz¹⁶⁰

Globally, SSI prevention is a priority.³^, Reference Allegranzi, Bagheri Nejad and Combescure⁴^, Reference Berrios-Torres, Umscheid and Bratzler⁸^, ⁹^, ¹² Unfortunately, effective and reliable SSI prevention measures are not consistently implemented in practice, leading to variable success in reducing these infections.Reference Serra-Aracil, Garcia-Domingo and Pares¹⁶¹^–Reference Arriaga, Lancaster and Berry¹⁶³ Several themes emerged from our systematic review.

First, successful strategies often engaged multidisciplinary perioperative staff in leading SSI improvement efforts, highlighting the influential role different specialties have in improving care. Second, leadership participation to champion and support improvement efforts were invaluable and contributed to success. Leadership included senior executives and hospital administrators and sometimes extended to government officials, especially in LMICs.Reference Pronovost, Weaver and Berenholtz¹⁶⁰^, Reference Saint, Kowalski, Banaszak-Holl, Forman, Damschroder and Krein¹⁶⁴^, Reference Henderson, Staiger and Peterson¹⁶⁵ Although specific leadership actions were poorly described, successful HAI prevention efforts require leadership support to identify and remove implementation barriers, including the adaptive challenges of changing people’s priorities, beliefs, habits, and loyalties.Reference Pronovost¹⁶⁶

Third, most studies included education to increase knowledge of best practices. Insufficient knowledge of evidence-based recommendations is a significant barrier to adoption of clinical practice guidelines.Reference Cabana, Rand and Powe¹⁶⁷ In addition to traditional learning-based teaching methods, some studies reinforced education by using real-life simulations, Reference Garcia-Paris, Cohena-Jimenez, Montano-Jimenez and Cordoba-Fernandez⁶⁴ monthly coaching calls,Reference Toltzis, O’Riordan and Cunningham⁴⁵^, Reference Reames, Krell, Campbell and Dimick¹¹¹ and yearly training courses.Reference Starling, Couto and Pinheiro¹⁵² The role of the surgical patient as an important stakeholder in SSI prevention was highlighted in a few studies and is gaining increasing recognition. An expert panel recently published practical ways to engage and educate patients, including educational leaflets translated into multiple languages.Reference Tartari, Weterings and Gastmeier¹⁶⁸

Fourth, most studies used protocols, care bundles, and checklists to simplify and standardize evidence-based interventions as part of their multifaceted approach. Several studies, for example, used checklists to summarize recommended practices. In LMICs, the most common method was to adapt the 2009 WHO surgical safety checklist based on local resources and culture.Reference Toor, Farooka, Ayyaz, Sarwar, Malik and Shabbir³⁰^, Reference Askarian, Kouchak and Palenik¹²³^, Reference El Mhamdi, Letaief, Cherif, Bouanene, Kallel and Hamdi¹²⁶^, Reference Kim, Kwakye and Kwok¹³²^, Reference Kwok, Funk and Baltaga¹³⁴ Local ownership of interventions and implementation strategies were especially important in these settings. Nevertheless, protocols and checklists are tools that only work if staff think they add value. Successful implementation requires significant staff engagement that taps into the intrinsic motivation of professionals and uses peer learning to change behaviors and shift social norms.Reference Dixon-Woods, Bosk, Aveling, Goeschel and Pronovost¹⁶⁹

Finally, almost all studies incorporated an evaluation strategy to monitor performance and provide feedback to frontline staff. Monitoring and feedback can heighten the sense of urgency, promote accountability, and show clinicians how they are performing. For example, in 1 study, patients were surveyed post discharge for SSI, direct feedback was given to the responsible surgeon, and a 31% decrease in the odds of an SSI was achieved.Reference Wilson, Hodgson and Liu³² In addition to monitoring outcomes, monitoring process measures and providing feedback may identify additional opportunities to improve.Reference Wick, Galante and Hobson¹¹³

Feedback can also be used to reframe SSI as a social problem, to foster ownership among staff, and to generate friendly competition.Reference Jordan, Goldstein, Michels, Hutzler, Slover and Bosco⁶⁷ Two studies provided peer-to-peer performance comparisons, Reference Hutzler, Kraemer, Iaboni, Berger and Bosco⁶⁵^, Reference Thompson, Oldenburg, Deschamps, Rupp and Smith¹³⁹ whereas others made team-to-team and interhospital comparisons within hospital networks.Reference Schaffzin, Harte and Marquette⁴³^, Reference Geubbels, Nagelkerke, Mintjes-De, Vandenbroucke-Grauls, Grobbee and De Boer¹²⁸^, Reference Joyce, Cioffi, Petriwsky and Robinson¹⁴⁷ An important lesson, however, was that monitoring and feedback of outcomes alone may not be sufficient to change behaviors or practices.Reference Pronovost, Berenholtz and Needham¹⁸

Several studies did not reduce SSI rates (Appendix 2). Though it was challenging to understand causality, most of these studies did not describe strategies to address 1 or more of the Four Es (ie, engage, educate, execute, and evaluate). For example, some studies implemented the 2009 WHO surgical safety checklist without describing strategies to engage, educate, evaluate, or provide feedback to staff.Reference Boaz, Bermant and Ezri⁷⁷^, Reference Biskup, Workman, Kutzner, Adetayo and Gupta¹²⁰ In the study by Reames et alReference Reames, Krell, Campbell and Dimick¹¹¹ the investigators implemented a checklist-based initiative to decrease SSI; however, participating organizations lacked the infrastructure to collect data. As a result, improvement teams did not receive feedback on performance or SSI rates. Finally, in the RCT by Anthony et alReference Anthony, Murray and Sum-Ping⁹⁶ the authors expressed concerns about the validity of the intervention bundle, as did other commentaries.Reference Anthony, Murray and Sum-Ping⁹⁶^, Reference Hunt and Hopf¹⁷⁰

We acknowledge several limitations of this review. First, most of the studies implemented multifaceted strategies, making it impossible to identify the relative importance of individual strategies or the most effective implementation strategies. Furthermore, our approach to summarizing strategies may be at risk for observer bias. Nevertheless, we identified a broad range of implementation strategies that can be adapted based on local culture and resources and we provide an extensive list of references that hospitals can access for more detailed information. Second, it was sometimes challenging to differentiate between studies designed to evaluate the effectiveness of a clinical intervention (eg, does decolonization improve outcomes?) and studies designed to increase compliance with evidence-based interventions. In addition, our analysis included studies conducted prior to the most recent CDC and WHO SSI prevention guidelines. As such, our review will need to be updated as new guidelines, including updated prevention measures are published. Third, we limited our search to studies published in English, Spanish, and French and may have missed important studies published in other languages. Nevertheless, the studies we did identify represented a wide geographic distribution, a variety of surgical procedures, and a range of SSI prevention measures, making our results applicable in diverse settings. Finally, only 8 studies Reference van Kasteren, Mannien and Kullberg³¹^, Reference Toltzis, O’Riordan and Cunningham⁴⁵^, Reference Schweizer, Chiang and Septimus⁵⁹^, Reference Rao, Cannella, Crossett, Yates, McGough and Hamilton⁷⁸^, Reference Hadley, Immerman, Hutzler, Slover and Bosco⁷⁹^, Reference Weinberg, Fuentes and Ruiz⁹¹^, Reference Anthony, Murray and Sum-Ping⁹⁶^, Reference Aiken, Wanyoro, Mwangi, Juma, Mugoya and Scott¹²¹ met the EPOC criteria of an acceptable-quality study design, limiting our ability to draw causal inferences or definitive conclusions.

Despite these limitations, we believe this review complements clinical practice guidelines and fills an important gap in the existing SSI literature by organizing a broad range of strategies into a practical framework that can be used to enhance the adoption of evidence-based practices and accelerate efforts to reduce SSI.

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2018.355.

Author ORCIDs

Promise Ariyo, 0000-0002-7518-3492

Acknowledgements

The authors wish to thank Christine Holzmueller, BLA, and Claire Levine, MS, ELS, for their editorial help, as well as Tomas Allen (WHO Headquarters Library) for advice on the systematic review search strategy.

Financial support

This review was conducted for the purpose of informing the development of implementation resources associated with the World Health Organization (WHO) Global Guidelines for the Prevention of Surgical Site Infections. We received no funding to perform this research.

Conflicts of interest

All authors report no conflicts of interest relevant to this article.

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Fig. 1.Systematic review study flow diagram. Note. SSI, surgical site infection; EPOC, Effective Practice and Organization of Care.

Table 1.Common Infection Prevention Measures

Table 2.Included Studies from Low-Middle Income Countries (LMICs)

Table 3.Evidence of Included Studies that Met EPOC Criteria (n=8)

Ariyo et al. supplementary material

Appendix 1

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Ariyo et al. supplementary material

Appendix 2

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Article contents

Implementation strategies to reduce surgical site infections: A systematic review

Abstract

Information

Methods

Data sources and search strategy

Inclusion and exclusion criteria

Study selection and data extraction

Analysis of implementation strategies

Results

Demographic characteristics

Adherence to SSI prevention measures

Implementation of SSI prevention strategies using the Four Es framework

Engagement

Education

Execution

Evaluation

Application of EPOC criteria

Discussion

Supplementary material

Author ORCIDs

Acknowledgements

Financial support

Conflicts of interest

References

Ariyo et al. supplementary material

Ariyo et al. supplementary material

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