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Opportunities for system level improvement in antibiotic use across the surgical pathway

  • E. Charani
    Correspondence
    Corresponding author at: NIHR Health Protection Research Unit in Antimicrobial Resistance and Healthcare Associated Infection, Imperial College London, Department of Medicine, 8th Floor Commonwealth Building, Du Cane Road, London W12 OHS, UK. Tel: 02033132732.
    Affiliations
    NIHR Health Protection Research Unit in Antimicrobial Resistance and Healthcare Associated Infection, Imperial College London, Department of Medicine, London, UK
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  • R. Ahmad
    Affiliations
    NIHR Health Protection Research Unit in Antimicrobial Resistance and Healthcare Associated Infection, Imperial College London, Department of Medicine, London, UK
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  • C. Tarrant
    Affiliations
    Department of Health Sciences, University of Leicester, Centre for Medicine, Leicester, UK
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  • G. Birgand
    Affiliations
    NIHR Health Protection Research Unit in Antimicrobial Resistance and Healthcare Associated Infection, Imperial College London, Department of Medicine, London, UK
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  • A. Leather
    Affiliations
    King’s Centre for Global Health & Health Partnerships, Division of Health & Social Care Research, Faculty of Life Sciences & Medicine, King’s College London, UK
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  • M. Mendelson
    Affiliations
    Division of Infectious Diseases and HIV Medicine, Department of Medicine, University of Cape Town, Groote Schuur Hospital Observatory, Cape Town, South Africa
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  • S.R. Moonesinghe
    Affiliations
    Centre for Anaesthesia Critical Care and Pain Medicine, University College London Hospitals, London, UK
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  • N. Sevdalis
    Affiliations
    Centre for Implementation Science, Institute of Psychiatry, King’s College London, Denmark Hill, UK
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  • S. Singh
    Affiliations
    School of Medicine, Amrita University, Tamilnadu, Kochi, India
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  • A. Holmes
    Affiliations
    NIHR Health Protection Research Unit in Antimicrobial Resistance and Healthcare Associated Infection, Imperial College London, Department of Medicine, London, UK
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Open AccessPublished:May 05, 2017DOI:https://doi.org/10.1016/j.ijid.2017.04.020

      Highlights

      • Optimizing antibiotic prescribing across the surgical pathway is key to tackling the important drivers antimicrobial resistance.
      • Evidence from around the world indicates that antibiotics for surgical prophylaxis are administered ineffectively.
      • Much of the evidence in infection management in surgery is related to infection prevention and control, surgical prophylaxis and the management of surgical site infections.
      • This article provides an overview of the surgical pathway and considers infection management and antibiotic prescribing at each step of the pathway.

      Summary

      Optimizing antibiotic prescribing across the surgical pathway (before, during, and after surgery) is a key aspect of tackling important drivers of antimicrobial resistance and simultaneously decreasing the burden of infection at the global level. In the UK alone, 10 million patients undergo surgery every year, which is equivalent to 60% of the annual hospital admissions having a surgical intervention. The overwhelming majority of surgical procedures require effectively limited delivery of antibiotic prophylaxis to prevent infections. Evidence from around the world indicates that antibiotics for surgical prophylaxis are administered ineffectively, or are extended for an inappropriate duration of time postoperatively. Ineffective antibiotic prophylaxis can contribute to the development of surgical site infections (SSIs), which represent a significant global burden of disease. The World Health Organization estimates SSI rates of up to 50% in postoperative surgical patients (depending on the type of surgery), with a particular problem in low- and middle-income countries, where SSIs are the most frequently reported healthcare-associated infections. Across European hospitals, SSIs alone comprise 19.6% of all healthcare-acquired infections. Much of the scientific research in infection management in surgery is related to infection prevention and control in the operating room, surgical prophylaxis, and the management of SSIs, with many studies focusing on infection within the 30-day postoperative period. However it is important to note that SSIs represent only one of the many types of infection that can occur postoperatively. This article provides an overview of the surgical pathway and considers infection management and antibiotic prescribing at each step of the pathway. The aim was to identify the implications for research and opportunities for system improvement.

      Keywords

      Introduction

      Optimizing antibiotic prescribing across the surgical pathway (before, during, and after surgery) is a key aspect of tackling important drivers of antimicrobial resistance (AMR) and simultaneously decreasing the burden of infection at the global level. In the UK alone, 10 million patients undergo surgery every year (
      • The Royal College of Anaesthetists
      Perioperative Medicine the Pathway to Better Surgical Care London.
      ), which is equivalent to 60% of the annual hospital admissions having a surgical intervention (
      NHS. NHS Confed..
      ). The overwhelming majority of surgical procedures require effectively limited delivery of antibiotic prophylaxis to prevent infections (
      • Boucher H.W.
      • Talbot G.H.
      • Bradley J.S.
      • Edwards J.E.
      • Gilbert D.
      • Rice L.B.
      • et al.
      Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America.
      ,
      • Bratzler D.W.
      • Dellinger E.P.
      • Olsen K.M.
      • Perl T.M.
      • Auwaerter P.G.
      • Bolon M.K.
      • et al.
      Clinical practice guidelines for antimicrobial prophylaxis in surgery.
      ). Evidence from around the world indicates that antibiotics for surgical prophylaxis are administered ineffectively, or are extended for an inappropriate duration of time postoperatively (
      • Leeds I.L.
      • Fabrizio A.
      • Cosgrove S.E.
      • Wick E.C.
      Treating Wisely: The Surgeon’s Role in Antibiotic Stewardship.
      ,
      • Tan J.A.
      • Naik V.N.
      • Lingard L.
      • Sussman J.A.
      • Mccaffrey C.B.
      • Leary D.B.
      • et al.
      Exploring obstacles to proper timing of prophylactic antibiotics for surgical site infections.
      ). Ineffective antibiotic prophylaxis can contribute to the development of surgical site infections (SSIs), which represent a significant global burden of disease. The World Health Organization (WHO) estimates SSI rates of up to 50% in postoperative surgical patients (depending on the type of surgery), with a particular problem in low- and middle-income countries (LMICs), where SSIs are the most frequently reported healthcare-associated infections (HCAIs) (
      • Aveling E.-L.
      • McCulloch P.
      • Dixon-Woods M.
      A qualitative study comparing experiences of the surgical safety checklist in hospitals in high-income and low-income countries.
      ,
      • Aiken A.M.
      • Wanyoro A.K.
      • Mwangi J.
      • Juma F.
      • Mugoya I.K.
      • Scott J.A.G.
      Changing use of surgical antibiotic prophylaxis in Thika Hospital, Kenya: A quality improvement intervention with an interrupted time series design.
      ,
      • World Health Organization
      Global guidelines for the prevention of surgical site infection.
      ). Across European hospitals, SSIs alone comprise 19.6% of all healthcare-acquired infections (
      • A
      Point Prevalence Survey of Healthcare- Associated Infections and Antimicrobial Use in European Hospitals 2011–2012.
      ). Much of the scientific research in infection management in surgery is related to infection prevention and control in the operating room (
      • Birgand G.
      • Azevedo C.
      • Toupet G.
      • Pissard-Gibollet R.
      • Grandbastien B.
      • Fleury E.
      • et al.
      Attitudes, risk of infection and behaviours in the operating room (the ARIBO Project): a prospective, cross-sectional study.
      ,
      • Cosgrove M.S.
      Infection control in the operating room.
      ,
      • Allo M.D.
      • Tedesco M.
      Operating room management: Operative suite considerations, infection control.
      ), surgical prophylaxis (
      • Bratzler D.W.
      • Dellinger E.P.
      • Olsen K.M.
      • Perl T.M.
      • Auwaerter P.G.
      • Bolon M.K.
      • et al.
      Clinical practice guidelines for antimicrobial prophylaxis in surgery.
      ,
      • Cusini A.
      • Rampini S.K.
      • Bansal V.
      • Ledergerber B.
      • Kuster S.P.
      • Ruef C.
      • et al.
      Different patterns of inappropriate antimicrobial use in surgical and medical units at a tertiary care hospital in Switzerland: A prevalence survey.
      ,
      • Davey P.
      • Brown E.
      • Charani E.
      • Fenelon L.
      • Im G.
      • Holmes A.
      • et al.
      Interventions to improve antibiotic prescribing practices for hospital inpatients (Review).
      ), and the management of SSIs (
      • Gaynes R.
      • Culver D.
      • Horan T.
      • Edwards J.
      • Richards C.
      • Tolson J.
      Surgical Site Infection (SSI) rates in the United States, 1992–1998: The National Nosocomial Infections Surveillance System Basic SSI Risk Index.
      ,
      • Bergs J.
      • Hellings J.
      • Cleemput I.
      • Zurel O.
      • De Troyer V.
      • Van Hiel M.
      • et al.
      Systematic review and meta-analysis of the effect of the World Health Organization surgical safety checklist on postoperative complications.
      ), with many studies focusing on infection within the 30-day postoperative period (
      • World Health Organization
      Global guidelines for the prevention of surgical site infection.
      ,
      • Løwer H.L.
      • Eriksen H.M.
      • Aavitsland P.
      • Skjeldestad F.E.
      Methodology of the Norwegian Surveillance System for Healthcare-Associated Infections: The value of a mandatory system, automated data collection, and active postdischarge surveillance.
      ). However it is important to note that SSIs represent only one of the many types of infection that can occur postoperatively.
      This article provides an overview of the surgical pathway and considers infection management and antibiotic prescribing at each step of the pathway. The aim was to identify the implications for research and opportunities for system improvement.

      Infection management in surgery

      To date, research on surgical antibiotic prescribing has focused on the preoperative period and has largely been confined to prophylaxis, hospital inpatients, and SSIs. The WHO has recently published guidelines for the prevention of SSIs (
      • World Health Organization
      Global guidelines for the prevention of surgical site infection.
      ). The guidelines provide detailed and evidence-based recommendations for the prevention of SSIs, including surgical antibiotic prophylaxis. The guidelines reinforce the recommendation against prolongation of surgical antibiotic prophylaxis beyond the surgical procedure as a means to prevent SSIs. In addition, they recommend worldwide surveillance of SSIs as a key component of any infection prevention and control programme. However, they do reflect that SSI surveillance is commonly poorly performed, with inconsistencies in practice, including in the type, duration, and quality of the surveillance (Table 1).
      Table 1Gaps in the surgical pathway and opportunities for system change that will impact infection management and antibiotic prescribing.
      The surgical pathway
      Perioperative periodPostoperative periodFollow-up care (primary/social/home) and surveillance
      Gaps in practice that potentially impact infection management and antibiotic prescribingLack of clarity on whose responsibility it is to decide on the choice, dose, and timing of antibiotic prophylaxisGaps in the diagnosis and management of hospital-acquired infections in the postoperative patientFollow-up care:
      Lack of clear understanding of the influence of culture and team dynamics (
      • Tschan F.
      • Seelandt J.
      • Keller S.
      • Semmer N.
      • Kurmann A.
      • Candinas D.
      • et al.
      Impact of case-relevant and case-irrelevant communication within the surgical team on surgical-site infection.
      ) on the implementation of the surgical checklists, e.g., WHO checklist
      Lack of leadership in antibiotic decision-makingCommunity follow-up of care in the postoperative period to ensure patient recovery
      Operating room design issues, e.g., thoroughfare, airflow disruption, or poor temperature control, or poorly designed surfacesLack of knowledge on the influence of culture and team dynamics on antibiotic prescribing decisions in surgerySurveillance:
      LMIC-specific: lack of equipment to avoid infection, lack of access to antibioticsLMIC-specific: lack of access to antibioticsLack of consistency in the method of SSI surveillance, e.g.:
      Duration of surveillance
      Type of surveillance
      Quality of surveillance
      Feedback to surgical teams
      Impact on clinical processes and patient outcomesInappropriate antibiotic prophylaxis resulting in increased risk of SSIsInappropriate management of hospital-acquired infections in the postoperative patient, including prolonged duration of antibiotic therapyNo system for linking SSI outcomes to antibiotic prescribing behaviours before, during, and after surgery
      Ineffective environmental precautions to prevent HCAIsLack of postoperative critical care training leading to over-diagnosis of sepsis in the postoperative periodLack of adherence to SSI programmes
      Opportunities for changeSimple solutions such as:Provision of education and training at post-graduate levelDeveloping a co-ordinated package of follow-up care in the community
      Clarity on roles and responsibilities for antibiotic prophylaxis in the operating roomProvision of national and local guidelines for antibiotic prescribing in surgeryBuilding on existing surveillance and developing new surveillance systems using a pragmatic approach, e.g., National Surgical Quality Improvement Programme (USA) or using mobile phone-based surveillance (LMIC)
      Monitoring operating room traffic and airflow to improve the operating room environment and prevent infectionsInclusion of and engagement with surgical teams in antibiotic stewardship interventions
      Organizational support and leadership in implementing the changesDeveloping better routes of access to antibiotics
      A greater understanding of the influence of culture and context on antibiotic prescribing behaviours
      Development of context-specific antimicrobial stewardship interventions
      Across the entire pathwayLack of engagement with, and involvement of, the surgical teams in antibiotic prescribing interventions, together with a lack of knowledge on the optimization of antibiotic use in surgery (
      • Charani E.
      • Tarrant C.
      • Moorthy K.
      • Sevdalis N.
      • Brennan L.
      • Holmes A.H.
      Understanding antibiotic decision making in surgery − a qualitative analysis.
      )
      Opportunity for change: Defining a role for antimicrobial stewardship within the surgical team, and developing targeted antibiotic prescribing interventions in surgery
      WHO, World Health Organization; LMIC, low- and middle-income countries; SSI, surgical site infection; HCAI, healthcare-associated infection.
      Beyond SSIs, there remains little research on the broader management of postoperative HCAIs. In order to significantly mitigate against the drivers of AMR and simultaneously reduce infection rates, it is critical to optimize antibiotic use before, during, and after surgery, and to look at care settings beyond the hospital − where most patients originate from and return to. Many factors impact the risk of subsequent infection in a person who undergoes surgery; the patient’s baseline health and wellbeing, patient’s comorbidities, the healthcare professionals involved, and how these professionals work as a team can all influence infection-related surgical outcomes (
      • Undre S.
      • Sevdalis N.
      • Healey A.N.
      • Darzi A.
      • Vincent C.A.
      Teamwork in the operating theatre: Cohesion or confusion?.
      ,
      • Hull L.
      • Arora S.
      • Kassab E.
      • Kneebone R.
      • Sevdalis N.
      Observational teamwork assessment for surgery: content validation and tool refinement.
      ). The management of the patient in the immediate postoperative period is critical, as is their hospital length of stay. The risk of acquiring an HCAI, e.g. hospital-acquired pneumonia (
      • Garibaldi R.A.
      • Britt M.R.
      • Coleman M.L.
      • Reading J.C.
      • Pace N.L.
      Risk factors for postoperative pneumonia.
      ,
      • Conde M.
      • Lawrence V.
      Post-operative pulmonary infections.
      ), device-related bacteraemia, or Clostridium difficile-associated diarrhoea, is high in the surgical patient (
      • Krapohl G.L.
      • Morris A.M.
      • Cai S.
      • Englesbe M.J.
      • Aronoff D.M.
      • Campbell D.A.
      • et al.
      Preoperative risk factors for postoperative Clostridium difficile infection in colectomy patients.
      ) (Table 2). The use of invasive devices such as intravenous lines, urinary catheters, and mechanical ventilation increases the risk of postoperative infection. In addition to this, the use of neuromuscular blocking agents during surgery to aid anaesthesia, together with reduced mobility in the immediate postoperative period, increases the risk of pneumonia (
      • Bulka C.M.
      • Terekhov M.A.
      • Martin B.J.
      • Dmochowski R.R.
      • Hayes R.M.
      • Ehrenfeld J.M.
      Nondepolarizing Neuromuscular Blocking Agents, Reversal, and Risk of Postoperative Pneumonia.
      ,
      • Sachdev G.
      • Napolitano L.M.
      Postoperative Pulmonary Complications: Pneumonia and Acute Respiratory Failure.
      ), which carries an estimated mortality of between 10% and 18%, even with appropriate antibiotic treatment ().
      Table 2The incidence of the most commonly occurring healthcare-associated infections in postoperative patients.
      Type of hospital-acquired infectionIncidence range (as a percentage of postoperative patients) reported in the literature
      Depends on the type of surgery and patient population; figures are from the published literature.
      Hospital-acquired pneumonia2.5% (
      • Conde M.
      • Lawrence V.
      Post-operative pulmonary infections.
      ) to 17.5% (
      • Garibaldi R.A.
      • Britt M.R.
      • Coleman M.L.
      • Reading J.C.
      • Pace N.L.
      Risk factors for postoperative pneumonia.
      )
      Surgical site infections1% to 9.8% (
      • England PH
      Surveillance of Surgical Site Infections in NHS Hospitals in England.
      )
      Urinary tract infections2% (
      • Chan J.Y.K.
      • Semenov Y.R.
      • Gourin C.G.
      Postoperative Urinary Tract Infection and {Short-Term} Outcomes and Costs in Head and Neck Cancer Surgery.
      ) to 10% (
      • Stéphan F.
      • Sax H.
      • Wachsmuth M.
      • Hoffmeyer P.
      • Clergue F.
      • Pittet D.
      Reduction of urinary tract infection and antibiotic use after surgery: a controlled, prospective, before-after intervention study.
      )
      Clostridium difficile-associated diarrhoea0.28% to 7.2% (
      • Masgala A.
      • Chronopoulos E.
      • Nikolopoulos G.
      • Sourlas J.
      • Lallos S.
      • Brilakis E.
      • et al.
      Risk factors affecting the incidence of infection after orthopaedic surgery: The role of chemoprophylaxis.
      ,
      • Flagg A.
      • Koch C.G.
      • Schiltz N.
      • Chandran Pillai A.
      • Gordon S.M.
      • Pettersson G.B.
      • et al.
      Analysis of Clostridium difficile infections after cardiac surgery: epidemiologic and economic implications from national data.
      )
      a Depends on the type of surgery and patient population; figures are from the published literature.

      Antibiotic prescribing in surgery—culture and context

      The surgical pathway has many actors, steps, and actions specifically related to the management of infection and antibiotic use. Nurses, surgeons, anaesthetists, pharmacists, and allied healthcare professionals in the pre-assessment clinic, in the operating room, on the ward, and in the community during postoperative follow-up, all contribute to the care of the surgical patient. Within this complex pathway, the responsibility for the management of infection remains poorly defined at each step. In the operating room, it is unclear whether it is the anaesthetist or the operating surgeon who should assume responsibility for the timing, choice, and dose (or the need for a second dose) of the prophylactic antibiotic (
      • Grocott M.P.W.
      • Pearse R.M.
      Perioperative medicine: The future of anaesthesia?.
      ,
      • Parker B.M.
      • Tetzlaff J.E.
      • Litaker D.L.
      • Maurer W.G.
      Redefining the preoperative evaluation process and the role of the anesthesiologist.
      ) (Table 1).
      In the past few years, surgery has turned to aviation-inspired checklists to improve the reliability of the processes of care, and subsequently their outcomes. A number of checklists have been published and evaluated in some detail, with the best known one perhaps being the checklist developed by the WHO (
      • Haynes A.
      • Weiser T.G.
      • Berry W.R.
      • Lipsitz S.
      • Breizat A.-H.
      • Dellinger E.
      • et al.
      A Surgical Safety Checklist to Reduce Morbidity and Mortality in a Global Population.
      ). These checklists have identified antibiotic prophylaxis to be one of the objectives for safe surgery (
      • World Health Organization
      WHO Surgical Safety Checklist Implementation Manual (First Edition).
      ). In the checklist, the requirement is that in the presence of the nurse, anaesthetist, and surgeon, the ‘surgical team’ confirm that antibiotic prophylaxis, where appropriate, is administered within 60 min of incision. However, the boundaries of responsibility for surgical antibiotic prophylaxis are not clear, specifically whose responsibility it is to decide what antibiotic prophylaxis is given and at what time (
      • Tan J.A.
      • Naik V.N.
      • Lingard L.
      • Sussman J.A.
      • Mccaffrey C.B.
      • Leary D.B.
      • et al.
      Exploring obstacles to proper timing of prophylactic antibiotics for surgical site infections.
      ). This is reported to be due in part to the culture and hierarchies that influence the behaviour of staff in the operating room, and also to the workflow and the environment of the operating room, which can act as obstacles to appropriate surgical antibiotic prophylaxis (
      • Tan J.A.
      • Naik V.N.
      • Lingard L.
      • Sussman J.A.
      • Mccaffrey C.B.
      • Leary D.B.
      • et al.
      Exploring obstacles to proper timing of prophylactic antibiotics for surgical site infections.
      ).
      The lack of clarity around responsibility for antibiotic prescribing carries over into the postoperative period (
      • Charani E.
      • Tarrant C.
      • Moorthy K.
      • Sevdalis N.
      • Brennan L.
      • Holmes A.H.
      Understanding antibiotic decision making in surgery − a qualitative analysis.
      ). The responsibility for antibiotic prescribing in surgical teams is dispersed and the optimization of antibiotic therapy is often not prioritized. This leads to inappropriate antibiotic use with a prolonged duration (
      • Leeds I.L.
      • Fabrizio A.
      • Cosgrove S.E.
      • Wick E.C.
      Treating Wisely: The Surgeon’s Role in Antibiotic Stewardship.
      ) (Table 1). This prevalent culture surrounding antibiotic decision-making in surgery needs to be understood and the expectation of surgical teams in relation to stewardship should be adjusted in view of this culture. Interventions in surgery should target the specific behaviour determinants and they should be developed in closer collaboration with surgical leaders.
      Historically, most antibiotic stewardship programmes have been focused on medical specialties (
      • Davey P.
      • Brown E.
      • Charani E.
      • Fenelon L.
      • Im G.
      • Holmes A.
      • et al.
      Interventions to improve antibiotic prescribing practices for hospital inpatients (Review).
      ,
      • Davey P.
      • Brown E.
      • Charani E.
      • Fenelon L.
      • Im G.
      • Holmes A.
      • et al.
      Interventions to improve antibiotic prescribing practices for hospital inpatients.
      ,
      • Charani E.
      • Gharbi M.
      • Moore L.S.P.
      • Castro-Sanchéz E.
      • Lawson W.
      • Gilchrist M.
      • et al.
      Effect of adding a mobile health intervention to a multimodal antimicrobial stewardship programme across three teaching hospitals: an interrupted time series study.
      ). Within surgery, the ‘low hanging fruit’ is surgical antibiotic prophylaxis, with the majority of stewardship interventions targeting this single step (
      • World Health Organization
      Global guidelines for the prevention of surgical site infection.
      ,
      • Davey P.
      • Brown E.
      • Charani E.
      • Fenelon L.
      • Im G.
      • Holmes A.
      • et al.
      Interventions to improve antibiotic prescribing practices for hospital inpatients (Review).
      ). Enhanced recovery after surgery (ERAS) programmes are now in place in many hospitals worldwide, and a recent systematic review has demonstrated that implementing such programmes can reduce HCAIs (
      • Grant M.
      • Yang D.
      • Wu C.
      • Makary M.
      • Wick E.
      Impact of Enhanced Recovery After Surgery and Fast Track Surgery Pathways on Healthcare-associated Infections: Results From a Systematic Review and Meta-analysis.
      ).The ERAS protocols include recommendations for surgical antibiotic prophylaxis, but focus more on the entire perioperative plan for patients to promote rapid recovery and discharge postoperatively (
      • Lassen K.
      • Soop M.
      • Nygren J.
      Consensus Review of Optimal Perioperative Care in Colorectal Surgery.
      ). Engagement with and inclusion of the surgical teams and surgical champions in the development of antimicrobial stewardship programmes is the first step in bringing about better outcomes. Organizations and national bodies can support this through legislation and policies that promote and endorse better antibiotic prescribing across the whole surgical pathway.
      Although surgical checklists are generally shown to have beneficial effects in reducing surgical infections (
      • Treadwell J.R.
      • Lucas S.
      • Tsou A.Y.
      Surgical checklists: a systematic review of impacts and implementation.
      ) − though not always SSIs (
      • Haugen A.S.
      • Søfteland E.
      • Almeland S.K.
      • Sevdalis N.
      • Vonen B.
      • Eide G.E.
      • et al.
      Effect of the World Health Organization checklist on patient outcomes: a stepped wedge cluster randomized controlled trial.
      ) − overall, they have had a mixed reception (
      • Aveling E.-L.
      • McCulloch P.
      • Dixon-Woods M.
      A qualitative study comparing experiences of the surgical safety checklist in hospitals in high-income and low-income countries.
      ,
      • Haynes A.
      • Weiser T.G.
      • Berry W.R.
      • Lipsitz S.
      • Breizat A.-H.
      • Dellinger E.
      • et al.
      A Surgical Safety Checklist to Reduce Morbidity and Mortality in a Global Population.
      ,
      • Russ S.
      • Rout S.
      • Caris J.
      • Mansell J.
      • Davies R.
      • Mayer E.
      • et al.
      Measuring variation in use of the WHO surgical safety checklist in the operating room: a multicenter prospective cross-sectional study.
      ). In India, for example, despite improvements in the use of the surgical site safety checklist, translation of its use in terms of patient safety outcomes has not been measured to understand the differences made in reducing SSIs, morbidity, and mortality (
      • Patel A.
      • Sanghi V.
      • Gupta V.
      Implementation of surgical safety checklist for all invasive procedures.
      ). Historically, LMICs have sub-optimal investment in surgical services, and existing surgical systems are growing too slowly to meet the increasing demand (
      • Ng-Kamstra J.S.
      • Greenberg S.L.M.
      • Abdullah F.
      • Amado V.
      • Anderson G.A.
      • Cossa M.
      • et al.
      Global Surgery 2030: a roadmap for high income country actors.
      ). The success of interventions such as the WHO checklist targeting surgical safety are highly context-dependent and variable, and are influenced by economic, cultural, and social factors, including role identity and hierarchies within healthcare teams (
      • Aveling E.-L.
      • McCulloch P.
      • Dixon-Woods M.
      A qualitative study comparing experiences of the surgical safety checklist in hospitals in high-income and low-income countries.
      ). In particular, LMIC hierarchies have a significantly greater impact on the successful adoption of interventions in surgery (
      • Aveling E.-L.
      • McCulloch P.
      • Dixon-Woods M.
      A qualitative study comparing experiences of the surgical safety checklist in hospitals in high-income and low-income countries.
      ). Importantly, leadership, flexibility, and teamwork are required for the implementation of checklists to be effective in any setting (
      • Walker I.A.
      • Reshamwalla S.
      • Wilson I.H.
      Surgical safety checklists: Do they improve outcomes?.
      ,
      • Gillespie B.M.
      • Marshall A.
      Implementation of safety checklists in surgery: a realist synthesis of evidence.
      ). This lesson applies to the successful implementation of any patient safety initiative, including interventions aiming to optimize antibiotic use (
      • Undre S.
      • Sevdalis N.
      • Healey A.N.
      • Darzi A.
      • Vincent C.A.
      Teamwork in the operating theatre: Cohesion or confusion?.
      ,
      • Dixon-Woods M.
      • Leslie M.
      • Tarrant C.
      • Bion J.
      Explaining Matching Michigan: an ethnographic study of a patient safety program.
      ).
      In particular for antibiotic prescribing, studies have described the influence of cultural determinants on prescribing outcomes (
      • Charani E.
      • Castro-Sanchez E.
      • Sevdalis N.
      • Kyratsis Y.
      • Drumright L.
      • Shah N.
      • et al.
      Understanding the determinants of antimicrobial prescribing within hospitals: the role of “prescribing etiquette”.
      ). Antibiotic prescribing is a social act, influenced by the perceived need for clinical autonomy of individual prescribers and the existing hierarchies within teams (
      • Charani E.
      • Castro-Sanchez E.
      • Sevdalis N.
      • Kyratsis Y.
      • Drumright L.
      • Shah N.
      • et al.
      Understanding the determinants of antimicrobial prescribing within hospitals: the role of “prescribing etiquette”.
      ). Changing antibiotic prescribing behaviours, with a view to optimizing patient-related infection outcomes, cannot be done in isolation simply by providing guidelines and policies. Existing guidelines and frameworks do not consider the variance in resources and infrastructure within LMICs (
      • World Health Organization
      Global guidelines for the prevention of surgical site infection.
      ). In LMICs, inconsistencies in available surgical capability and resources is far more pronounced between rural and urban settings and between different LMIC countries, than it is in high-income countries where the minimum standard of care is provided in any setting. Research from different LMIC settings is lacking and is urgently needed to develop contextually sound and driven interventions that are sustainable.
      The culture within specialties, organizations, and countries has the power to influence the outcome of interventions (
      • Hofstede G.
      Dimensionalizing Cultures: The Hofstede Model in Context.
      ,
      • Buzan B.
      Culture and international society.
      ,
      • Al-Bannay H.
      • Jarus T.
      • Jongbloed L.
      • Yazigi M.
      • Dean E.
      Culture as a variable in health research: perspectives and caveats.
      ). Culture refers to how individuals, as members of a team, learn and share knowledge in order to generate behaviours (
      • Spradley J.P.
      Ethnography for What?.
      ). Culture is learned, and in order to influence practice, it needs to be studied. The culture of treatment of infection and antibiotic use in the surgical specialty has distinct features in contrast to acute medicine, because the dynamic of decision-making in the patient surgical pathway is different, as are the causal factors that influence patient-related outcomes. Understanding the contextual and cultural determinants of infection management and antibiotic prescribing in surgery is critical to the development of context-specific interventions that incorporate the need for flexibility, local leadership, and teamwork.
      In an extensive review of the implementation of the Matching Michigan intervention for the prevention of blood stream infections by intensive care units in the UK (
      • Dixon-Woods M.
      • Leslie M.
      • Tarrant C.
      • Bion J.
      Explaining Matching Michigan: an ethnographic study of a patient safety program.
      ), the researchers reported that local culture was ‘highly consequential’ to the intervention outcome. Furthermore, the most successful units were reported to be those that had adapted the intervention to the local context and used local champions to drive and implement it. In surgery, one key step would be better engagement with the surgical leaders and the inclusion of surgeons in antimicrobial stewardship programmes. With the increasing threat of AMR, there is an urgent need to understand how to minimize the burden of infection and optimize antibiotic use across the whole surgical pathway. Addressing the gaps in the surgical pathway will reduce the total antibiotic use and significantly mitigate drivers for AMR and the burden of infection (Table 1). Decision-making within multidisciplinary surgical teams and communication with professionals across organizational boundaries in LMICs remain unexplored. Resource limitations mean that fewer actors are involved in the surgical pathway, but there are also opportunities for innovative team composition. In the global context it is essential to redefine the antibiotic stewardship roles of the entire healthcare team across conventional organizational and professional boundaries. In addition, in LMICs the role of antibiotic stewardship in surgical care pathways is imminent, since the inappropriate use of antibiotic surgical prophylaxis has led to an increase in SSIs (
      • Rana D.A.
      • Malhotra S.D.
      • Patel V.J.
      Inappropriate surgical chemoprophylaxis and surgical site infection rate at a tertiary care teaching hospital.
      ). The need for research on this topic in LMICs is particularly important to bring about efficiencies at the organizational level and to address the huge impact on out-of-pocket health expenditures and loss of earnings through prolonged postoperative recovery for the most vulnerable in society.

      The way forward

      Interventions in antibiotic use tend to consider and address only one point at a time on the patient pathway, and in the case of surgical patients, attention has been focused primarily on prophylactic antibiotic use. And yet multiple interventions have the potential to influence infection-related outcomes in the surgical patient. Social science perspectives to understand the structural, cultural contextual determinants of antibiotic use in surgery need exploring, with the potential to inform sustainable quality improvement and surgical safety initiatives. Identifying and mapping current actors and actions in the surgical specialty in different healthcare settings will inform interventions that are context-specific and relevant to the local patient population. They will also help ensure greater equity in access to safe surgery on a global scale.
      Addressing antibiotic prescribing and AMR across sectors and cultures will enable surgical healthcare professionals to mobilize and drive organizational, national, and global change. Engaging with and involving surgeons and anaesthetists in the antibiotic stewardship agenda is essential, especially as it will enable the investigation of a critically unexplored domain in healthcare on a global scale, and optimize interventions within and beyond healthcare environments that have been entrenched in hierarchies and cultural norms. Addressing the gap of infection management in the surgical pathway will also impact on international policy and practice in antibiotic resistance and stewardship. Addressing the factors that influence AMR across the surgical pathway in resource-limited environments has the potential to profoundly impact the health outcomes of the millions of people who undergo surgery each year.

      Funding

      This work is funded by the National Institute of Health Research Imperial Biomedical Research Centre and the National Institute for Health Research Health Protection Research Unit (NIHR HPRU-2012-10047) in Healthcare Associated Infection and Antimicrobial Resistance at Imperial College London in partnership with Public Health England and the NIHR Imperial Patient Safety Translational Research Centre. NS research was supported by the National Institute for Health Research (NIHR) Collaboration for Leadership in Applied Health Research and Care South London at King’s College Hospital NHS Foundation Trust. NS is a member of King’s Improvement Science, which is part of the NIHR CLAHRC South London and comprises a specialist team of improvement scientists and senior researchers based at King's College London. Its work is funded by King’s Health Partners (Guy’s and St Thomas’ NHS Foundation Trust, King’s College Hospital NHS Foundation Trust, King’s College London and South London and Maudsley NHS Foundation Trust), Guy’s and St Thomas’ Charity, the Maudsley Charity and the Health Foundation. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research or the UK Department of Health.

      Conflict of interest

      Charani, Tarrant, Ahmad, Birgand, Mendelson, Leather, Singh, Moonesinghe and Holmes have none to declare. Sevdalis is the Director of London Safety and Training Solutions Ltd, which provides team skills training and advice on a consultancy basis in hospitals and training programmes in the UK and internationally.

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