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Surgical Perspectives

ACOI Surgical Site Infections Management Academy (ACOISSIMA)

Recommendations on the prevention of surgical site infections

Sartelli, Massimoa,*; Cortese, Francescob; Scatizzi, Marcoc; Labricciosa, Francesco Mariad; Bartoli, Stefanoe; Nardacchione, Francescof; Sganga, Gabrieleg; Cillara, Nicolah; Luridiana, Gianluigii; Murri, Ritaj; Campli, Mariok; Catarci, Marcol; Borghi, Felicem; Di Marzo, Francescon; Siquini, Waltera; Catena, Faustoo; Coccolini, Federicop; Armellino, Mariano Fortunatoq; Baldazzi, Gianandrear; Basti, Massimos; Ciaccio, Giovannit; Bottino, Vincenzou; Marini, Pierluigiv

Author Information
Il Giornale di Chirurgia – Journal of the Italian Surgical Association: August 2022 - Volume 42 - Issue 2 - p e12
doi: 10.1097/IA9.0000000000000002
  • Open

Abstract

Introduction

Antimicrobial resistance (AMR) has recently emerged as one of the most serious public health issues of the 21st century. Despite the multifaceted nature of AMR affecting humans, animals and the environment, healthcare workers play a critical role in containing the spread of AMR.

In a study published in 2019, Cassini et al1 examined the weight of infections caused by multidrug-resistant bacteria (MDRB) in invasive isolates in Europe. Processing the 2015 data of the European Antimicrobial Resistance Surveillance Network (EARS-Net), the authors published the first estimate of the impact of AMR on the European population. They estimated 671,689 infections with MDRB, of which 63.5% were healthcare-associated infections (HAIs). The infections caused by MDRB had the potential to cause 33,110 attributable deaths each year in Europe (equal to the sum of deaths caused by influenza, AIDS, and tuberculosis) and 874,541 disability-adjusted life-years. The study demonstrated that Italy and Greece had the most infections caused by MDRB in Europe. Although the Italian population is of a medium-high age, it is notable that about a third of deaths due to MDRB infections in Europe had been in Italy.

To tackle the burden of AMR, the Italian Ministry of Health in 2017 published the “National Antimicrobial Resistance Contrast Plan (PNCAR) 2017–2020,”2 addressing the AMR burden according to the general One Health strategy and identifying strategies and actions to be implemented at different levels: national, regional, and local. In 2020, the program was extended to 2021 because of the COVID-19 pandemic and will be updated with a new plan that will be valid for the years 2022–2025.

During the elaboration of the PNCAR, the Ministry of Health invited the European Centre for Disease Prevention and Control (ECDC) to plan a visit to Italy with a team of experts. In December 2017, the ECDC published a report on the prevention and control of AMR in Italy.3 The report summarized visits and meetings that ECDC experts had in Italy to discuss and specifically assess the situation regarding AMR in Italy. The visit took place from 9 January 2017, to 13 January 2017, and, after visiting three different regions, and some hospitals, speaking with experts and representatives of the institutions, the ECDC delegates wrote their conclusions. The experts highlighted the threat represented by the AMR, and the need for coordination to address this phenomenon, so that the good practices already consolidated in some areas of the country could become a common heritage in the daily practice of all healthcare workers in Italy.

According to a report by the Organization for Economic Co-operation and Development (OECD),4 in Italy, the proportion of antibiotic-resistant infections has grown from 17% in 2005 to 30% in 2015, and will reach 32% in 2030, if antibiotic consumption continues to follow the same trends.

In Italy, since 2001, the Italian National Institute of Health5 has been coordinating the surveillance system of the sistema nazionale di sorveglianza sentinella dell’antibiotico-resistenza antibiotic resistance in the human sphere, consisting of a network of hospital laboratories recruited voluntarily, with the primary aim of describing the frequency and trend of AMR in a selected group of bacteria isolated from infections of clinical relevance (above all bacteremia), representing both community-acquired infections and healthcare-associated infections (Staphylococcus aureus, Enterococcus faecium and E. faecalis, Klebsiella pneumoniae, Pseudomonas aeruginosa, Escherichia coli, Acinetobacter baumannii).

The percentage of E. coli resistant to third-generation cephalosporins was decreasing in 2020 (26.4%) compared with 2019 (30.8%), while a decreasing trend in the last 6 years (2015–2020) was observed for aminoglycosides (from 18.4% in 2015 to 15.2% in 2020), and fluoroquinolones (from 44.4% in 2015 to 37.6% in 2020). For the second consecutive year, there was an increase in the percentage of isolates of K. pneumoniae resistant to carbapenems (29.5% in 2020 vs. 28.5% in 2019), after a slight decline observed in previous years. Resistance to carbapenems was confirmed to be very low in E. coli (0.5%) but increased in P. aeruginosa (15.9%) and in Acinetobacter spp. (80.8%). Among Gram-negative bacteria, 33.1% of K. pneumoniae isolates and 10.0% of E. coli isolates were found to be multiresistant (resistant to third-generation cephalosporins, aminoglycosides, and fluoroquinolones). In 2020, both of these values were decreasing compared with previous years. Regarding P. aeruginosa, the percentage of resistance to three or more antibiotics including piperacillin-tazobactam, ceftazidime, carbapenems, aminoglycosides, and fluoroquinolones was 12.5%, also in decrease compared with previous years, while a percentage of multi-resistance (fluoroquinolones, aminoglycosides, and carbapenems) was found very high (78.8%) and increasing for Acinetobacter spp. Regarding S. aureus, the percentage of methicillin-resistant isolates remained stable, around 34%, while a worrying trend continued to increase in the percentage of E. faecium isolates resistant to vancomycin, which in 2020 was 23.6%.

One of the crucial aspects of combating AMR is the implementation of infection prevention and control (IPC) programs. HAIs are infections occurring while patients receive healthcare, and many of them are caused by MDRB. Patients with medical devices (central lines, urinary catheters, ventilators) or who undergo surgical procedures are at risk of HAIs.

In Italy, there is no systematic national surveillance system for HAIs, but a point prevalence surveillance study was conducted during the period October 2016–November 2016: it included 56 facilities and selected 14,773 patients distributed in various departments (medicine, surgery, intensive care, gynecology and obstetrics, pediatrics, rehabilitation, neonatology, geriatrics, psychiatry, long-term care).6 The prevalence of patients with at least one HAI was 8.03%.

The occurrence of HAIs such as surgical site infections (SSIs), catheter-associated urinary tract infections (CAUTIs), central line-associated bloodstream infections (CLABSIs), ventilator-associated pneumonia (VAP), hospital-acquired pneumonia (HAP), and Clostridioides difficile infection continues to escalate at an alarming rate. These infections result in significant patient illnesses and deaths, prolong the duration of hospital stays, and often necessitate additional diagnostic and therapeutic interventions, generating added costs to those already incurred by the patient’s underlying disease.7 However, the perception of the phenomenon is not yet sufficiently high among healthcare workers, resulting in a low level of adequate responses.

Many SSIs may be preventable if simple rules are respected. Both the World Health Organization (WHO),8–10 and the Centers for Disease Control and Prevention (CDC)11 have published guidelines for the prevention of SSIs. In 2016, the American College of Surgeons and the Surgical Infection Society updated their surgical site infection guidelines.12 In 2019, the National Institute for Health and Care Excellence (NICE) updated its guidelines for the management of SSIs.13

Despite all the published guidelines, knowledge and awareness of IPC measures among surgeons are frequently insufficient, and there is a significant gap between the evidence-based practice and clinical practice regarding to the prevention of SSIs.

The WHO Global guidelines for the prevention of SSIs are evidence-based, addressing the global burden of SSIs on both patients and healthcare systems. They have been designed to be suitable for any country and can be locally adapted, including 13 recommendations for preventing infections before surgery and 16 for preventing infections during and after surgery.10

Classification and definition

SSIs are the most common cause of HAIs in surgical patients. SSIs are generally classified according to universal criteria.14 SSIs are divided into incisional and organ/space infections. Incisional infections are further classified as superficial involving skin and subcutaneous tissue, and deep involving deep soft tissue muscle and fascia. Deep and organ/space infections represent the SSIs causing the most morbidity.

To compare SSI rates between hospitals and avoid subjective interpretation, an accurate standardization of the case definitions is crucial. To reduce subjectivity and ensure standardization of definitions across Europe, in 2017, ECDC published the HAI-Net SSI protocol version 2.2.15

Superficial incisional infections are classified as infections occurring within 30 days after the surgical procedure involving only skin and subcutaneous tissue of the incision and at least one of the following criteria:

  • purulent drainage with or without laboratory confirmation,
  • organisms isolated by an aseptically obtained culture of fluid or tissue,
  • at least one of the following signs or symptoms of infection including pain or tenderness, localized swelling, redness, or heat and the superficial incision is deliberately opened by a surgeon (unless culture of incision is negative),
  • diagnosis of superficial incisional SSI made by a surgeon or a physician.

Deep incisional infections are classified as infections occurring within 30 days after the surgical procedure if no implant is left in place or within 90 days if implant is in place and the infection appears to be related to the operation and infection involves deep soft tissue (e.g., fascia, muscle) of the incision and at least one of the following criteria:

  • purulent drainage from the deep incision,
  • dehiscence or deliberate opening by the surgeon from the deep incision when the patient has at least one of the following signs or symptoms of clinical infection: fever (> 38 °C), localized pain or tenderness, unless incision is culture-negative,
  • an abscess or other evidence of infection involving the deep incision is found on direct examination, during reoperation, or by histopathologic or radiologic examination,
  • diagnosis of deep incisional SSI made by a surgeon or attending physician.

Organ/space infections are classified as infections occurring within 30 days after a surgical procedure involving any part of the anatomy other than the incision and at least one of the following criteria:

  • purulent drainage from a drain that is placed through a stab wound into the organ/space,
  • organisms isolated from an aseptically obtained culture of fluid or tissue in the organ/space,
  • an abscess or other evidence of infection involving the organ/space that is found on direct examination,
  • during reoperation, or by histopathologic or radiologic examination diagnosis of organ/space SSI made by a surgeon or attending physician.

Methods

The Italian surgical societies are becoming more conscious of the importance of preventing HAIs across the surgical pathway. In particular, Associazione Chirurghi Ospedalieri Italiani—Italian Surgical Association (ACOI) has included the prevention of SSIs in its training program, setting up a multidisciplinary task force and organizing a series of educational events (ACOI Surgical Site Infections Management Academy [ACOISSIMA]) throughout the whole national territory in order to increase knowledge and awareness on the prevention of SSIs among Italian surgeons. Following expert interventions, each event included the active participation of local surgeons to assess the state-of-the-art in the prevention of SSIs and AMR in various Italian regions.

In order to investigate the awareness of Italian surgeons about the prevention of SSIs, in June 2021, ACOI conducted an anonymous survey addressed to all members. An electronic invitation with a link to the survey was sent to about 3,200 members of ACOI by the weekly newsletter. The survey was Internet-based. Participation was voluntary and anonymous. No incentives were provided to the respondents.

The 15-item self-administered questionnaire collected information about the behavior of Italian surgeons in preventing and treating infections across the surgical pathway.

Among the 3,200 surgeons contacted by email, 371 (11.6%) completed the survey. The overall participation was low, disclosing poor awareness of the problem.

To clarify the key issues in the prevention of SSIs across the surgical pathway, an expert panel designated by the ACOI Board of Directors convened in Rome, Italy, on 16 December 2021, for a consensus conference. The panelists approved 11 evidence-based statements developed for topic questions regarding the prevention of SSIs, aiming to define quality indicators statements to be respected in every Italian surgical unit. To design the statements, a literature search, using the PubMed database, was performed without restriction of time or type of article. The search was limited to English-language publications.

The expert panel drafted and reviewed a article, finally obtaining this document that represents the executive summary of the consensus. It summarizes the ACOI recommendations for SSIs prevention.

The present recommendations were developed according to the grading of recommendations assessment, development and evaluation methodology.16,17 The quality of evidence was marked as high, moderate, low, or very low. The strength of the recommendation was qualified as weak or strong based on the agreement of the expert panel (>80%). The following set of recommendations aims to reinforce best practices among Italian surgeons.

Statement 1

As many HAIs may be preventable, each surgical department should have in place and implement measures aimed at reducing the risk of HAIs including SSIs, before, during, and after surgery.

Multidisciplinary educational projects should be implemented aiming to increase knowledge and raise awareness and accountability (Moderate quality of evidence, strong recommendation).

SSIs are the most common HAIs in surgical departments. The prevention of SSIs should be a priority for all surgical departments worldwide. Bacteria are becoming increasingly resistant to antibiotics, making the prevention of SSIs more important nowadays. SSIs are associated with longer postoperative hospital stays and result in higher attributable morbidity and mortality.12

Safe surgical care requires a range of precautions aimed at reducing the risk of SSIs before, during, and after surgery. Many SSIs may be preventable if simple rules are respected. In 2018, a systematic review and meta-analysis of studies between 2005 and 2016 evaluated the results of multifaceted interventions to prevent CAUTIs, CLABSIs, SSIs, and VAP/HAP in acute care or long-term care settings. Published evidence suggests a potential reduction of HAI rates in the range of 35%–55% associated with multifaceted interventions irrespective of a country’s income level.18

Another systematic review of the interventions to reduce HAIs demonstrated that 65%–70% of cases of CLABSIs and CAUTIs and 55% of cases of VAP and SSIs could be preventable with evidence-based strategies. The authors concluded that 100% prevention of HAIs could not be attainable with evidence-based prevention strategies; however, comprehensive implementation of such strategies could prevent many HAIs and save lives, reducing costs.19

Teamwork is crucial for achieving a comprehensive approach to providing care that is adequate to optimize both individual health outcomes and overall service delivery of healthcare. Effective teamwork can have a positive impact on patient safety. Healthcare teams that communicate effectively result in enhanced patient safety and improved clinical performance.

The IPC teams aim to prevent the acquisition and dissemination of HAIs within healthcare facilities. Many hospital professionals are typically involved in IPC teams, making collaboration essential.20 The multidisciplinary approach reinforces the concept that professionals bring with them their particular expertise and are responsible for their respective contributions to patient care. In this context, the direct involvement of surgeons may be important.

All surgeons should have the necessary knowledge to respect effective IPC practices. Increasing knowledge may influence their perceptions and motivate them to change behavior.

In 2018, the WHO published a document to support the prevention of SSIs around the world.21 The purpose of the document is to present a range of approaches to achieve, in the context of a broader surgical safety climate, successful implementation of SSIs prevention at a facility level.

Knowledge is fundamental for effective IPC.22 Lack of knowledge about the appropriateness, efficacy, and use of prevention measures determine poor compliance. To overcome these barriers, education and training are the cornerstones of improvement in prevention practices.

Education of surgeons in preventing HAIs should begin at the undergraduate level and should be consolidated with further training throughout the postgraduate years. Surgical societies may have a crucial role in educating surgeons about IPC programs. Efforts to improve educational programs are required, and it is necessary that in Italy, appropriate educational programs will be further reinforced to drive surgeons towards correct behaviors in the prevention of HAIs.

Finally, adequate IPC strategies depend on both healthcare workers’ behaviors and the organizational characteristics of acute healthcare facilities that can promote a behavioral change. Accountability is an essential aspect in preventing HAIs.23 Without accountability, evidence-based strategies cannot be implemented, and are used in a fragmented way, decreasing their effectiveness. Accountability begins with the hospital executive officer and other leaders supporting the imperative for a culture of patient safety, making the prevention of HAIs an organizational priority.

Statement 2

Facility-based surveillance of HAIs, including SSIs, surveillance should be performed to guide interventions with timely feedback of results to surgeons.

Every surgical unit should know the effectiveness of the adopted prevention strategies (Low quality of evidence, strong recommendation).

Surveillance includes monitoring of an event, collection and analysis of the data associated with the event, and timely feedback to healthcare workers who can implement evidence-based strategies to improve patients’ outcomes by decreasing the incidence of the event.24 Surveillance allows hospitals and clinicians to measure the effectiveness of strategies that are implemented to decrease infection rates.25

The surveillance of SSIs is one of the most important components of an effective IPC program and has been shown to be crucial to reduce the risk of SSIs.26,27 Hospitals should perform surveillance for SSIs to identify trends in infection rates, improve infection prevention practices and decrease the incidence and the burden of these costly and common hospital-acquired infections.

An ideal surveillance system should routinely audit and provide confidential feedback on SSI rates and adherence to prevention measures to individual surgeons, the surgical division and/or department chiefs, and hospital leadership.28 However, systematic surveillance of SSIs is challenging and requires expertise and resources because active surveillance is a resource- and time-consuming activity.

In Italy, continuous surveillance of SSIs is routinely performed by only a few regions, and the real impact of SSIs in the country is not known, making impossible to assess the quality of healthcare in preventing and controlling SSIs. Data on nonprosthetic surgery from an Italian surveillance program of SSIs for the period 2009 to 201129 demonstrated that implementation of a national surveillance program was helpful in reducing SSI rates and should be prioritized in all healthcare systems.

Recently the ECDC published the Annual Epidemiological Report,30 sharing data collected in 2017 in hospitals participating in national or regional surveillance of SSIs across Europe. The SSI surveillance protocol included the following nine surgical procedures: coronary artery bypass graft, open and laparoscopic cholecystectomy, open and laparoscopic colon surgery, cesarean section, hip prosthesis, knee prosthesis, and laminectomy. The standardized follow-up period was 31 days except for deep or organ/space infections following orthopedic operations with an implant in place. For these surgical procedures, the follow-up period was extended to 91 days. In 2017, 10,149 SSIs were reported. Of these, 4,739 (46.7%) were superficial, 3,088 (30.4%) deep, and 2,274 (22.4%) organ/space SSIs. In 48 (0.5%) SSIs, the type of SSI was unknown. The percentage of SSIs varied greatly, from 0.5% in knee prosthesis operations to 10.1% in open colon surgery operations. Both in cholecystectomy and colon resections, the percentage of SSIs was lower in laparoscopic procedures than in open procedures. S. aureus (21.5%) and E. coli (13.9%) were the most isolated bacteria. For cholecystectomy and colon resections, the most frequently reported bacteria were Enterobacterales. For all other types of surgical procedures, Gram-positive cocci were the most isolated bacteria.

Statement 3

An approved local protocol of surgical antibiotic prophylaxis (SAP) according to the local microbiological epidemiology should be in place in each surgical unit. Its appropriate application should be periodically verified (Low quality of evidence, strong recommendation).

Surgical antibiotic prophylaxis (SAP) is one of the most important perioperative measures for preventing SSIs. SAP aims to achieve serum and tissue antibiotic levels exceeding the antibiotic’s minimum inhibitory concentration for the duration of the surgical procedure. It allows to counteract the proliferation of bacteria likely to be encountered during the surgical procedure.

Approximately 15% of all antibiotics in hospitals are prescribed for SAP.31,32 Inadequate SAP prescriptions can be a major driver of “opportunistic” infections such as C. difficile, select MDRB and increase healthcare costs.33,34

Although the principles of SAP are clearly established and guidelines have been published, implementing these guidelines is problematic among surgeons. In 2013, the American Society of Health-System Pharmacists (ASHP), the Infectious Diseases Society of America (IDSA), the Surgical Infection Society (SIS), and the Society for Healthcare Epidemiology of America (SHEA) published a set of clinical practice guidelines for SAP.35

Prolonged administration of antibiotics in the postoperative period is the most common reason for inappropriate SAP.36 An Italian study evaluating the appropriateness of the prescription of SAP demonstrated that only 18.1% of the patients received appropriate SAP.37 A British study described how antibiotic prescription was considered by surgeons as a secondary task,38 while other studies underlined the lack of motivation and time to develop nonsurgical skills among surgeons.39

To define the association of type and duration of SAP with SSIs, acute kidney injury (AKI), and C. difficile infection, a multicenter, national retrospective cohort study was published in 2019.40 Increasing duration of SAP was associated with a higher risk of AKI and C. difficile infection; extended duration did not lead to additional reduction of SSIs.

One way to engage surgeons may be to adapt guidelines into a local protocol defining responsibilities for actions among a multidisciplinary team. Moreover, since the choice of SAP also depends on local epidemiology, a local adaptation of guidelines for SAP should be developed and implemented in each surgical unit. Guidelines for perioperative antibiotic prophylaxis in adults were updated in 2011 by the Italian Institute of Health.41 Local protocols should integrate the statement of these guidelines into a local protocol. Several studies demonstrated that implementation of a SAP program including the creation of a local protocol, the organization of educational sessions, and planning periodic revision of prescriptions was effective in reducing antibiotic consumption, antibiotic prophylaxis cost, and the incidence of SSIs.42,43

However, other studies revealed that implementation of interventions led to improved quality of SAP administration as well as a reduction in antibiotic use and cost without a significant reduction in SSIs.44,45 van Kasteren et al45 in a prospective study of elective surgical procedures in 13 Dutch hospitals, evaluated the quality of SAP before and after an intervention consisting of performance feedback and implementation of national clinical practice guidelines. Antibiotic use decreased from 121 to 79 DDD/100 procedures, and costs were reduced by 25% per procedure. After the intervention, the antibiotic choice was inappropriate in only 37.5% of the cases instead of 93.5% of expected cases in the absence of any intervention. Prolonged prophylaxis was observed in 31.4% instead of 46.8% of expected cases and inappropriate timing in 39.4% instead of the expected 51.8%. Time series analysis showed that all improvements were statistically significant (P < 0.01). The overall SSI rates before and after the intervention were 5.4% (95% confidence interval [CI] = 4.3%, 6.5%) and 4.6% (95% CI = 3.6%, 5.4%), respectively.

To evaluate the impact of an educational, participative and continuing antimicrobial stewardship program on prescription adherence, a study was conducted between 2013 and 2019 on an Italian University Hospital performing more than 40.000 surgical interventions per year.46 Data about SAP were collected from two separate surveys, one at baseline (April 2013) and one after the long-term antimicrobial stewardship intervention (post-intervention, April 2019). Overall, guidelines adherence improved from 36.6% (n = 149) at baseline to 57.9% (n = 221) post-intervention (P < 0.0001). A significant improvement (P < 0.001) was also detected for each category: indication (from 58.5% to 93.2%), selection and dosing (from 58.5% to 80.6%), timing (from 92.4% to 97.6%), duration (from 71% to 80.1%).

Statement 4

Due to their demonstrated efficacy, optimizing patients’ physiologic function by enhanced recovery after surgery (ERAS) protocols and limiting perioperative blood transfusions by patient blood management (PBM) protocols should be implemented to improve the patient’s response to infections (Low quality of evidence, strong recommendation).

Enhanced recovery after surgery (ERAS) programs are evidence-based pathways designed to optimize the perioperative care of surgical patients before, during, and after surgery.47 ERAS Societyconsensus guidelines are powerful tools implemented worldwide across hospitals in order to improve the quality of surgical care 47 and Italian surgical societies such as ACOI and PeriOperative Italian Society (POIS) have already reached a consensus for their implementation in colorectal surgery.48

The basic principles of ERAS include attention:

  • to preoperative measures including preoperative counseling and nutritional strategies;
  • to perioperative measures including regional anesthetic and nonopioid analgesic approaches, fluid balance, maintenance of normothermia; and
  • to postoperative measures including postoperative recovery strategies, including early mobilization, early removal of the urinary catheter and appropriate thromboprophylaxis.

Patient blood management (PBM) is an evidence-based approach aiming to optimize patient outcomes by clinically managing and preserving a patient’s own blood.49 PBM aims to detect and treat anemia, minimize the risk of blood loss and the need for transfusions for each patient through a coordinated multidisciplinary process of care. The three pillars of PBM are the following:

  • diagnosing and treating anemia (especially iron deficiency anemia),
  • minimizing blood loss, and
  • avoiding unnecessary transfusions.50

Several studies described the correlation between perioperative blood transfusion and increased SSIs in both general surgery51,52 and colorectal surgery.53,54

A large population-based retrospective study in Western Australia clearly showed a 21% reduction of HAIs after PBM implementation.55

A meta-analysis and systematic review about the impact of ERAS and fast-track surgery for abdominal or pelvic surgery on HAIs was published in 2017. The results suggested that ERAS protocols were powerful tools to prevent three of the major HAIs, including HAP, CAUTI, and SSIs.56 The role of ERAS in decreasing SSIs has been debated. With the expansion of laparoscopic interventions, ERAS has increasingly incorporated laparoscopic patients, especially in colorectal surgery. Laparoscopic colonic surgery was associated with a lower rate of SSIs in several studies,57,58 and the combination of laparoscopy and ERAS protocols might be even more beneficial.

Some studies reported that ERAS in colorectal surgery was associated with a reduction in the occurrence of SSIs.59,60 In other studies, it was not possible to demonstrate a benefit of ERAS compliance on SSIs incidence, while laparoscopic surgery was clearly protective.61

The expert panel suggests that ERAS, PBM and IPC are important patient safety interventions that can improve patients’ response to infections.

Statement 5

Hand hygiene is the cornerstone of IPC. When optimally performed, hand hygiene reduces HAIs and the spread of antimicrobial resistance. Correct hand hygiene should always be performed during the surgical pathway. Its appropriateness and the consumption of alcohol-based hand rub used by surgeons should be monitored periodically (Moderate quality of evidence, strong recommendation).

Hand hygiene is an important indicator of patients’ safety and quality of care delivered in all healthcare settings, including surgical departments. The purpose of routine hand hygiene in patient care is to remove dirt and organic material and reduce microbial contamination from transient microbiological flora.

The objective of cleaning hands and forearms prior to surgery is to reduce the bacteria on the skin. Surgical hand preparation is crucial to maintain the lowest possible contamination of the surgical field, especially in the event of sterile glove puncture during the procedure.12

The 2016 WHO guidelines for the prevention of SSIs recommend to perform surgical hand preparation either by scrubbing with a suitable antimicrobial soap and water or using a suitable alcohol-based hand rub solution before donning sterile gloves. The statement is supported by moderate quality of evidence. The meta-analysis conducted by WHO experts included 64 studies. However, among these studies, there were only six studies with SSIs as primary outcome, including three randomized control trials, three observational studies, and two comparative cohorts.62

Surgical hand preparation should be performed either by scrubbing with an adequate antimicrobial soap and water or an adequate alcohol-based hand rub solutions containing 60%–80% alcohol before donning sterile gown and gloves.63

Hand hygiene in healthcare can be monitored directly or indirectly. Direct methods to monitor hand hygiene in healthcare include direct observation, patient assessment, or healthcare workers’ self-reporting. Indirect methods include monitoring the consumption of products, such as soap or hand rubs, and automated monitoring of the use of sinks and hand rub dispensers. However, methods based on product consumption cannot determine if hand hygiene actions are performed at the right moment during care or if the technique is correct. The advantages, however, are that they are simple and can be continuous. The amount of alcohol-based hand rub used by healthcare workers has been selected as one of the indicators by the WHO Guidelines on Hand Hygiene in Health Care.64

Statement 6

Appropriate intravenous SAP (one-shot) should be administered within 120 minutes considering the half-life of the antibiotic. Additional intraoperative doses should be administered for procedures exceeding two half-lives of the antibiotic or with associated significant blood loss (more than 1.5 L). The duration of SAP should not exceed 24 hours. Any antibiotic administration 24 hours after the intervention has to be defined as therapy. (Moderate quality of evidence, strong recommendation).

At the moment, the expert panel has no recommendations on the use of oral antibiotic prophylaxis (No recommendations).

Although SAP plays a pivotal role in reducing the rate of SSIs, other factors such as attention to basic infection prevention and control strategies may have a strong impact on the occurrence of SSIs.65

Although clinical practice guidelines for SAP have been published, high rates of SAP prescribing practices not compliant with guidelines are common and may contribute to suboptimal patients’ outcomes, cause adverse effects, and be an important driver of AMR.35

SAP should be recommended for surgical procedures having a high risk of postoperative SSIs or when foreign material is implanted. Antibiotic agents prescribed for surgical prophylaxis should be nontoxic and inexpensive and should have in vitro activity against the common organisms that can cause the postoperative SSIs after a specific surgical procedure.66 Adequate concentrations of antibiotics should be present in the surgical site for the duration of the procedure. Intravenous SAP should be administered within 120 minutes considering the half-life of the antibiotic.

To value the correct timing of SAP and compare the different timing intervals, a systematic review and meta-analysis were published in 2017.67 The meta-analysis demonstrated that the administration of SAP more than 120 minutes before the incision or after the incision was associated with a higher risk of SSIs than the administration less than 120 minutes before the incision.

Weber et al68 in 2017 published a randomized controlled trial to evaluate the optimal timing of SAP consisting of single-shot, intravenous infusion of 1.5 g of cefuroxime, a cephalosporin of second-generation with a short half-life, associated with 500 mg metronidazole in colorectal surgery. A total of 5,580 patients were randomly assigned to the early group, 30–75 minutes before the incision (2,798 patients), or the late group, 0–30 minutes before the incision (2,782 patients). Five-thousand one-hundred seventy-five patients were analyzed. The authors did not find any significant differences between the two groups.

An observational cohort study conducted in a Dutch tertiary medical center69 was published in 2021 to evaluate if the risk of SSIs differed after administration of SAP within 60–30 or 30–0 minutes before the surgical site incision. There was no conclusive evidence of a difference in risk of SISs after SAP administration 60–30 minutes or 30–0 minutes before incision.

From a pharmacokinetic point of view, additional intraoperative doses should be administered for procedures exceeding two half-lives of the antibiotic or with associated significant blood loss (more than 1.5 L). It was confirmed by a recent meta-analysis.70 The meta-analysis included two randomized controlled trials and eight cohort studies, involving 9,470 patients. Although there was heterogeneity among administered antibiotics, intraoperative redosing of SAP reduced the incidence of SSIs compared with a single dose preoperative SAP in any type of surgery.

There is no evidence to support the use of SAP for more than 24 hours after the surgical procedure.35,71

Increasing duration of SAP was associated with a higher risk of AKI and C. difficile infection, leading to no additional reduction of SSIs in a multicenter, national retrospective cohort study published in 2019.40

Optimal timing for SAP as well as avoiding the prolongation of SAP are strong recommendations in the WHO guidelines for the prevention of SSIs supported by a moderate quality of evidence.12

The role of oral antibiotic prophylaxis and mechanical bowel preparation (MBP) in colorectal surgery remains controversial. Although the use of oral antibiotics in combination with MBP is a strategy employed widely in North America,72 it remains much less common across Europe. The reasons for avoidance of MBP in Europe are difficult to investigate, but the increase in ERAS protocols excluding routine MBP may be a reason.73 Evidence suggests that MBP use in addition to oral antibiotics as part of a bowel-cleansing protocol is beneficial with respect to SSI.12 The impact of the use of oral antibiotics in the absence of MBP with regard to SSIs has not been established.69 Moreover, the value of employing different regimens of oral antibiotics has also not been clearly established. Most trials have used the combination of an aminoglycoside (neomycin or kanamycin) with a macrolide such as erythromycin or with metronidazole.74

At the moment, the expert panel has no recommendations on the use of oral antibiotic prophylaxis.

The increasing frequency of patients’ colonization with extended-spectrum beta-lactamases (ESBLs) producers and other MDRB may threaten the efficacy of routine SAP and perioperative patient pathways.75

Optimizing clinical practice is crucial to mitigate AMR and limit SSIs associated with MDRB. Future research is urgently required to establish effective and appropriate SAP in those patients colonized with MDRB.

Statement 7

Hair should not be removed from the surgical site unless it interferes with the operation. If hair removal is necessary, it should be made by a clipper. Razors for hair removal should not be used because they increase the risk of SSIs (Moderate quality of evidence, strong recommendation).

Adherence to aseptic techniques is integral to the prevention of SSIs. One of the measures to prevent SSIs is the preoperative preparation of the operative site, including not to remove hair from the surgery site unless it interferes with the surgical procedures. A Cochrane systematic review on preoperative hair removal to reduce SSIs was published in 2021.76 The review included 19 randomized and six quasi-randomized trials (8,919 participants). The authors concluded that there were probably fewer SSIs when hair was not removed compared with shaving with a razor (moderate-certainty evidence).

Another meta-analysis of published randomized controlled trials about hair removal for the prevention of SSIs was published in 2017.77 This meta-analysis included 14 trials, 11 randomized controlled trials and three controlled clinical trials. The authors concluded that hair removal should be avoided unless necessary. When hair removal is necessary, the meta-analysis suggests that clipping is more effective in preventing SSIs than shaving or depilatory cream.

The 2016 WHO guidelines12 for the prevention of surgical site infections strongly recommend not to remove the hair from the surgical site unless it interferes with the operation, and if removal is necessary, it should be made by a clipper. The meta-analysis conducted by WHO experts included 15 randomized or quasi-randomized trials comparing the effect of preoperative hair removal versus no hair removal or different methods of hair removal (shaving, clipping, and depilatory cream).12 A moderate quality of evidence demonstrated that clipping or no hair removal has a significant benefit in reducing the risk of SSI when compared with shaving.

Statement 8

Alcohol-based solutions of chlorhexidine for surgical site skin preparation should be used in patients undergoing surgical procedures. Alcohol-based solutions of povidone-iodine may be used as an alternative to alcohol-based solutions of chlorhexidine. If the surgical site is next to a mucous membrane, aqueous solutions should be used (Moderate quality of evidence, strong recommendation).

Another important point of SSI prevention during skin preparation is the meticulous preoperative disinfection of the skin. It aims to reduce the microbial load on the patient’s skin as much as possible before incising the skin. Skin commensals include many bacteria with little pathogenicity but also potentially pathogenic bacteria such as S. aureus. The number of bacteria on the skin can be greatly reduced, limiting the risk of SSIs, by appropriate skin disinfection.

Current evidence demonstrates that alcohol-based preparations are more effective than aqueous-based preparations, and should be used, if they are not contraindicated. However, which is the most adequate alcohol-based solution is still a controversial issue.78,79 Many control trials80–84 compared the efficacy of aqueous-based povidone-iodine solutions with alcohol-based chlorhexidine solutions for preventing SSIs and reported alcohol-based chlorhexidine as more effective.

A well-conducted randomized single-center study published in 201685 demonstrated that the use of alcohol-based solution of chlorhexidine for preoperative skin antisepsis resulted in a significantly lower risk of SSIs after cesarean delivery compared with the use of alcohol-based solution of povidone-iodine. On the other hand, another single-center randomized study86 compared alcohol-based solution of chlorhexidine, alcohol-based solution of povidone-iodine, and both applied sequentially, demonstrating that the skin preparation techniques resulted in similar rates of SSIs after cesarean delivery.

The 2016 WHO guidelines for the prevention of surgical site infections recommend, with moderate quality of evidence, alcohol-based solutions of chlorhexidine for surgical site skin preparation in patients undergoing surgical procedures.12 The meta-analysis conducted by the WHO experts included 17 randomized control trials.87 Six randomized controlled trials compared alcohol-based solutions of chlorhexidine with alcohol-based solutions of povidone-iodine and found significantly lower risk of SSIs with alcohol-based solutions of chlorhexidine. However, four of the six randomized control trials did not report SSIs in at least one study arm, and in most studies, the main endpoint was the number of colony-forming units rather than SSIs.

The NICE guidelines suggest alcohol-based solutions of chlorhexidine as the first choice unless contraindicated or the surgical site is next to a mucous membrane.15 The 2017 CDC guidelines for the prevention of SSIs recommend the use of alcohol-based antiseptic solutions without differentiating alcohol-based solutions of chlorhexidine or alcohol-based solutions of povidone-iodine.13 The Asia Pacific Society of Infection Control (APSIC)24 suggests alcohol-based skin antiseptic preparations without differentiating alcohol-based solutions of chlorhexidine or alcohol-based solutions of povidone-iodine.

Alcohol-based antiseptics are flammable. Alcohol-based antiseptics should be allowed time to dry completely (about 3 minutes, longer in areas with excess hair) to limit fire hazard.

Statement 9

Perioperative patient’s clinical condition, including maintaining normal body temperature (normothermia), should be optimized and monitored (Moderate quality of evidence, strong recommendation).

The WHO global guidelines suggest the use of warming devices in the operating room and during the surgical procedure for patient body warming with the purpose of reducing SSIs.12 Even mild degrees of hypothermia can increase SSI rates. Hypothermia may directly impair neutrophil function or impair it indirectly by triggering subcutaneous vasoconstriction and subsequent tissue hypoxia. In addition, hypothermia may increase blood loss, leading to wound hematomas or a need for transfusion, both of which can increase rates of SSIs.88,89 Several randomized controlled trials have shown the benefits of perioperative warming to reduce SSI rates.90–92

The most frequently used technique to prevent perioperative hypothermia is active body surface warming systems, which generate heat mechanically (heating of air, water, or gels) that is transferred to the patient via skin contact. A Cochrane systematic review to evaluate the effectiveness of perioperative active body surface warming systems was published in 2016. The review demonstrated a beneficial effect of warming systems in terms of a lower rate of SSIs and complications, at least in patients undergoing abdominal surgery. A beneficial effect was also demonstrated on major cardiovascular complications in patients with substantial cardiovascular disease, although the evidence was limited.93

The WHO global guidelines for the prevention of SSIs stated that the evidence was insufficient to identify a target temperature to be reached and maintained.12

In 2014 a collaborative document led by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), the American Hospital Association (AHA), the Association for Professionals in Infection Control and Epidemiology (APIC), and The Joint Commission,89 recommended a minimum temperature of 35.5 °C during the perioperative period.

Considering that “hypothermia” is defined as a core temperature <36 °C, the accepted target may be core temperature >36 °C.

Statement 10

Where available, triclosan-coated sutures should be used to prevent SSIs (Moderate quality of evidence, strong recommendation).

SSIs may arise when bacteria colonize the surgical sutures, creating a biofilm. The biofilm establishes immunity from both antibiotic treatment and the host immune system.94 Once this biofilm develops, there is an increased chance of SSIs developing. In vitro and in vivo studies have shown the effectiveness of triclosan-coated sutures95 in inhibiting colonization of sutures.

Triclosan-coated sutures were shown to be nontoxic, noncarcinogenic, and nonteratogenic.96

A large number of randomized controlled trials and meta-analyses have been performed with contrasting results on the effectiveness of triclosan-coated sutures.

In 2014, the largest conducted randomized controlled trial on this topic was published by Diener et al.97 It was performed in 24 German hospitals and demonstrated that triclosan-coated polydioxanone (PDS Plus) did not reduce the occurrence of SSIs after elective midline laparotomy.

Another study, published in 2015,98 did not demonstrate the benefits of triclosan-coated sutures. However, the authors, despite good randomization methods, did not exclude baseline imbalances that could have interfered with the primary outcome of the study.

Many meta-analyses have demonstrated that triclosan-coated sutures are effective,99–110 but in some meta-analyses, the effect size differs substantially among subgroups.109 It has been proven that triclosan-coated sutures are more effective in studies using polyglactin 910 sutures than in those using polydioxanone.109 These findings can explain the results of the study by Diener et al,97 as they investigated polydioxanone. A possible reason for the variation in effect between suture types may be found in the features of sutures. Polydioxanone is a monofilament suture and bacterial adherence to polydioxanone may be lower than that to a braided suture such as polyglactin 910.111 Therefore, a polyglactin 910 suture may have more potential to be colonized than a monofilament suture, and thereby may benefit more from an active antibacterial suture. Moreover, polydioxanone is generally used to close the fascia, whereas polyglactin 910 is used to close the subcutaneous tissue. The majority of SSIs are described as superficial and in the study by Diener et al.,97 the most detected SSIs were superficial. It indicates that the majority of described SSIs in this study occurred in a different anatomical layer from that for which the intervention was performed.109

Antimicrobial sutures should be used for the closure of all incisional wound layers throughout the whole incision, mitigating the risk of wound contamination and the occurrence of SSIs. Polydioxanone sutures should be used for closing the fascial layer. Triclosan-coated polyglactin sutures should be used for closing the subcutaneous layer.

The role of triclosan-coated sutures in reducing the incidence of SSIs compared with uncoated sutures has been demonstrated by 12 meta-analyses.99–110

Two recent and large systematic reviews found triclosan-coated sutures significantly reduced the incidence of SSIs.109,110 The first meta-analysis, published in 2017 by de Jonge et al,109 included 21 randomized control trials and involved 6,462 patients. SSIs were reduced significantly by the use of triclosan-coated sutures compared with a comparable uncoated variant (a relative risk reduction of 15% for the use of triclosan-coated sutures).

The second meta-analysis, published in 2019 by Ahmed et al,110 included 25 randomized control trials and involved 11,957 patients. The meta-analysis demonstrated that triclosan-coated sutures significantly reduced the risk of SSIs at 30 days after the surgical procedure, both in clean and contaminated surgery.

Finally, a systematic review and meta-analysis investigating the efficacy of triclosan-coated sutures for preventing SSIs in the specific field of digestive surgery was published in 2018.106 In the 10 randomized control trials, the incidence rates of SSIs were 8.9% using coated sutures and 12.1% using noncoated sutures.

The use of triclosan-coated sutures is now suggested to reduce the risk of SSIs by WHO,12 CDC,13 the American College of Surgeons and Surgical Infection Society,14 NICE,15 and the World Society of Emergency Surgery.112

Statement 11

On an individual level, every surgeon should have the necessary knowledge, skills, and abilities to implement effective IPC practices. However, surgeons with special interest and knowledge in surgical infections should be incorporated into the infection control team and recognized as “champions” (Very low quality of evidence, strong recommendation).

Surgeons are at the forefront in preventing infections across the surgical pathway. They are responsible for many of the processes of healthcare that impact the risk of SSIs and play an important role in their prevention. In hospitals, cultural, contextual, and behavioral determinants influence clinical practice.113 Improving behavior in IPC remains a challenge. A range of factors such as diagnostic uncertainty, fear of clinical failure, time pressure, or organizational contexts can complicate the surgeons’ approach toward infections. However, changing behavior is challenging.

Surgeons should have the necessary knowledge, skills, and abilities to implement effective infection prevention and management practices. Nonetheless, increasing knowledge alone may not be sufficient and may not be effective in changing practice.114

Identifying a local opinion leader to serve as a champion may be important because the “champion” may integrate best clinical practices and drive colleagues in changing behaviors, working on a day-to-day basis, and promoting a culture in which IPC is of high importance.23 Surgeons with satisfactory knowledge of surgical infections may provide feedback to the prescribers, integrate the best practices among surgeons and implement change within their own sphere of influence by interacting directly with the infection control committee. Such a champion model has been previously applied to surgical safety implementations in general, such as surgical checklists, and plays a key role in successful quality improvement at the hospital level.115

Conclusions

The following recommendations proposed in this document aim to disseminate best practices among Italian surgeons and summarize the ACOI recommendations on the prevention of SSIs.

Statement 1

As many HAIs may be preventable, each surgical department should have in place and implement measures aimed at reducing the risk of HAIs including SSIs, before, during, and after surgery. Multidisciplinary educational projects should be implemented aiming to increase knowledge and raise awareness and accountability (Moderate quality of evidence, strong recommendation).

Statement 2

Facility-based surveillance of HAIs, including SSIs, surveillance should be performed to guide interventions with timely feedback of results to surgeons. Every surgical unit should know the effectiveness of the adopted prevention strategies (Low quality of evidence, strong recommendation).

Statement 3

An approved local protocol of surgical antibiotic prophylaxis (SAP) according to the local microbiological epidemiology should be in place in each surgical unit. Its appropriate application should be periodically verified (Low quality of evidence, strong recommendation).

Statement 4

Due to their demonstrated efficacy, optimizing patients’ physiologic function by enhanced recovery after surgery (ERAS) protocols and limiting perioperative blood transfusions by patient blood management (PBM) protocols should be implemented to improve the patient’s response to infections (Low quality of evidence, strong recommendation).

Statement 5

Hand hygiene is the cornerstone of IPC. When optimally performed, hand hygiene reduces HAIs and the spread of antimicrobial resistance. Correct hand hygiene should always be performed during the surgical pathway. Its appropriateness and the consumption of alcohol-based hand rub used by surgeons should be monitored periodically (Moderate quality of evidence, strong recommendation).

Statement 6

Appropriate intravenous SAP (one-shot) should be administered within 120 minutes considering the half-life of the antibiotic. Additional intraoperative doses should be administered for procedures exceeding two half-lives of the antibiotic or with associated significant blood loss (more than 1.5 L). The duration of SAP should not exceed 24 hours. Any antibiotic administration 24 hours after the intervention has to be defined as therapy. (Moderate quality of evidence, strong recommendation).

At the moment, the expert panel has no recommendations on the use of oral antibiotic prophylaxis (No recommendations).

Statement 7

Hair should not be removed from the surgical site unless it interferes with the operation. If hair removal is necessary, it should be made by a clipper. Razors for hair removal should not be used because they increase the risk of SSIs (Moderate quality of evidence, strong recommendation).

Statement 8

Alcohol-based solutions of chlorhexidine for surgical site skin preparation should be used in patients undergoing surgical procedures. Alcohol-based solutions of povidone-iodine may be used as an alternative to alcohol-based solutions of chlorhexidine. If the surgical site is next to a mucous membrane, aqueous solutions should be used (Moderate quality of evidence, strong recommendation).

Statement 9

Perioperative patient’s clinical condition, including maintaining normal body temperature (normothermia), should be optimized and monitored (Moderate quality of evidence, strong recommendation).

Statement 10

Where available, triclosan-coated sutures should be used to prevent SSIs (Moderate quality of evidence, strong recommendation).

Statement 11

On an individual level, every surgeon should have the necessary knowledge, skills, and abilities to implement effective IPC practices. However, surgeons with special interest and knowledge in surgical infections should be incorporated into the infection control team and recognized as “champions” (Very low quality of evidence, strong recommendation).

References

1. Cassini A, Högberg LD, Plachouras D, et al.; Burden of AMR Collaborative Group. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2019;19:56–66.
2. Ministero della Salute. Piano nazionale di contrasto all’antibiotico resistenza (PNCAR) 2017-2020. 2017. Available at: http://www.salute.gov.it/imgs/C_17_pubblicazioni_2660_allegato.pdf. Accessed 21 April 2022.
3. European Centre for Disease Prevention and Control. ECDC country visit to Italy to discuss antimicrobial resistance issues. 2017. Available at: https://ecdc.europa.eu/en/publications-data/ecdc-country-visit-italy-discuss-antimicrobial-resistance-issues. Accessed 21 April 2022.
4. Organization for Economic Co-operation and Development. Antimicrobial resistance - policy insights. 2016. Available at: https://www.oecd.org/health/health-systems/AMR-Policy-Insights-November2016.pdf. Accessed 21 April 2022.
5. Istituto Superiore di Sanità. AR-ISS. Sistema nazionale di sorveglianza sentinella dell’antibiotico-resistenza. 2021.Available at: https://www.epicentro.iss.it/antibiotico-resistenza/ar-iss/RIS-1_2021.pdf. Accessed 21 April 2022.
6. Dipartimento Scienze della Salute Pubblica e Pediatriche, Università di Torino Studio di prevalenza italiano sulle infezioni correlate all’assistenza e sull’uso di antibiotici negli ospedali per acuti - protocollo ECDC. Available at: https://www.salute.gov.it/imgs/C_17_pubblicazioni_2791_allegato.pdf. Accessed 21 April 2022.
7. Badia JM, Casey AL, Petrosillo N, Hudson PM, Mitchell SA, Crosby C. Impact of surgical site infection on healthcare costs and patient outcomes: a systematic review in six European countries. J Hosp Infect. 2017;96:1–15.
8. Allegranzi B, Zayed B, Bischoff P, et al.; WHO Guidelines Development Group. New WHO recommendations on intraoperative and postoperative measures for surgical site infection prevention: an evidence-based global perspective. Lancet Infect Dis. 2016;16:e288–e303.
9. Allegranzi B, Bischoff P, de Jonge S, et al.; WHO Guidelines Development Group. New WHO recommendations on preoperative measures for surgical site infection prevention: an evidence-based global perspective. Lancet Infect Dis. 2016;16:e276–e287.
10. World Health Organization. Global guidelines for the prevention of surgical site infection, 2nd ed. 2018. Available at: https://apps.who.int/iris/bitstream/handle/10665/277399/9789241550475-eng.pdf?sequence=1&isAllowed=y. Accessed 21 April 2022.
11. Berríos-Torres SI, Umscheid CA, Bratzler DW, et al.; Healthcare Infection Control Practices Advisory Committee. Centers for Disease Control and Prevention guideline for the prevention of surgical site infection, 2017. JAMA Surg. 2017;152:784–791.
12. Ban KA, Minei JP, Laronga C, et al. American College of Surgeons and Surgical Infection Society: surgical site infection guidelines, 2016 update. J Am Coll Surg. 2017;224:59–74.
13. National Institute for Health and Care Excellence. Surgical site infections: prevention and treatment. NICE guideline [NG125]. Available at: https://www.nice.org.uk/guidance/ng125. Accessed 21 April 2022.
14. Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG. CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections. Infect Control Hosp Epidemiol. 1992;13:606–608.
15. European Centre for Disease Prevention and Control. Surveillance of surgical site infections and prevention indicators in European hospitals. HAI-Net SSI protocol, version 2.2. 2017. Available at: https://www.ecdc.europa.eu/sites/default/files/documents/HAI-Net-SSI-protocol-v2.2.pdf. Accessed 21 April 2022.
16. Guyatt GH, Oxman AD, Vist GE, et al.; GRADE Working Group. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924–926.
17. Brozek JL, Akl EA, Jaeschke R, et al.; GRADE Working Group. Grading quality of evidence and strength of recommendations in clinical practice guidelines: part 2 of 3. The GRADE approach to grading quality of evidence about diagnostic tests and strategies. Allergy. 2009;64:1109–1116.
18. Schreiber PW, Sax H, Wolfensberger A, Clack L, Kuster SP; Swissnoso. The preventable proportion of healthcare-associated infections 2005-2016: systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2018;39:1277–1295.
19. Umscheid CA, Mitchell MD, Doshi JA, Agarwal R, Williams K, Brennan PJ. Estimating the proportion of healthcare-associated infections that are reasonably preventable and the related mortality and costs. Infect Control Hosp Epidemiol. 2011;32:101–114.
20. Zingg W, Holmes A, Dettenkofer M, et al.; systematic review and evidence-based guidance on organization of hospital infection control programmes (SIGHT) study group. Hospital organisation, management, and structure for prevention of health-care-associated infection: a systematic review and expert consensus. Lancet Infect Dis. 2015;15:212–224.
21. World Health Organization. Implementation manual to support the prevention of surgical site infections at the facility level: turning recommendations into practice. 2018. Available at: https://www.who.int/publications/i/item/WHO-HIS-SDS-2018-18. Accessed 21 April 2022.
22. World Health Organization. Improving infection prevention and control at the health facility. Interim practical manual supporting implementation of the WHO Guidelines on Core Components of Infection Prevention and Control Programmes 2018. 2018. Available at: https://www.who.int/publications/i/item/WHO-HIS-SDS-2018-10. Accessed 21 April 2022.
23. Sartelli M, Labricciosa FM, Coccolini F, et al. It is time to define an organizational model for the prevention and management of infections along the surgical pathway: a worldwide cross-sectional survey. World J Emerg Surg. 2022;17:17.
24. Ling ML, Apisarnthanarak A, Abbas A, et al. APSIC guidelines for the prevention of surgical site infections. Antimicrob Resist Infect Control. 2019;8:174.
25. Gastmeier P, Schwab F, Sohr D, Behnke M, Geffers C. Reproducibility of the surveillance effect to decrease nosocomial infection rates. Infect Control Hosp Epidemiol. 2009;30:993–999.
26. Condon RE, Schulte WJ, Malangoni MA, Anderson-Teschendorf MJ. Effectiveness of a surgical wound surveillance program. Arch Surg. 1983;118:303–307.
27. Haley RW, Culver DH, White JW, et al. The efficacy of infection surveillance and control programs in preventing nosocomial infections in US hospitals. Am J Epidemiol. 1985;121:182–205.
28. Jamtvedt G, Young JM, Kristoffersen DT, O’Brien MA, Oxman AD. Audit and feedback: effects on professional practice and health care outcomes. Cochrane Database Syst Rev. 2006:CD000259.
29. Marchi M, Pan A, Gagliotti C, et al.; Sorveglianza Nazionale Infezioni in Chirurgia (SNICh) Study Group. The Italian national surgical site infection surveillance programme and its positive impact, 2009 to 2011. Euro Surveill. 2014;19:20815.
30. European Centre for Disease Prevention and Control. Healthcare-associated infections: surgical site infections. Annual Epidemiological Report for 2017. 2019. Available at: https://www.ecdc.europa.eu/sites/default/files/documents/AER_for_2017-SSI.pdf. Accessed 21 April 2022.
31. Ansari F, Erntell M, Goossens H, Davey P. The European Surveillance of Antimicrobial Consumption (ESAC) point-prevalence survey of antibacterial use in 20 European hospitals in 2006. Clin Infect Dis. 2009;49:1496–1504.
32. Robert J, Péan Y, Varon E, et al.; Société de pathologie infectieuse de langue française (SPILF); Observatoire national de l’épidémiologie de la résistance bactérienne aux antibiotiques (ONERBA); Surveillance de la prescription des antibiotiques (SPA) Group. Point prevalence survey of antibiotic use in French hospitals in 2009. J Antimicrob Chemother. 2012;67:1020–1026.
33. Slimings C, Riley TV. Antibiotics and hospital-acquired Clostridium difficile infection: update of systematic review and meta-analysis. J Antimicrob Chemother. 2014;69:881–891.
34. Owens RC Jr, Donskey CJ, Gaynes RP, Loo VG, Muto CA. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin Infect Dis. 2008;46(suppl 1):S19–S31.
35. Bratzler DW, Dellinger EP, Olsen KM, et al.; American Society of Health-System Pharmacists; Infectious Disease Society of America; Surgical Infection Society; Society for Healthcare Epidemiology of America. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm. 2013;70:195–283.
36. Dettenkofer M, Forster DH, Ebner W, Gastmeier P, Rüden H, Daschner FD. The practice of perioperative antibiotic prophylaxis in eight German hospitals. Infection. 2002;30:164–167.
37. Napolitano F, Izzo MT, Di Giuseppe G, Angelillo IF; Collaborative Working Group. Evaluation of the appropriate perioperative antibiotic prophylaxis in Italy. PLoS One. 2013;8:e79532.
38. Charani E, Tarrant C, Moorthy K, Sevdalis N, Brennan L, Holmes AH. Understanding antibiotic decision making in surgery- a qualitative analysis. Clin Microbiol Infect. 2017;23:752–760.
39. Jayasuriya-Illesinghe V, Guruge S, Gamage B, Espin S. Interprofessional work in operating rooms: a qualitative study from Sri Lanka. BMC Surg. 2016;16:61.
40. Branch-Elliman W, O’Brien W, Strymish J, Itani K, Wyatt C, Gupta K. Association of duration and type of surgical prophylaxis with antimicrobial-associated adverse events. JAMA Surg. 2019;154:590–598.
41. Piano Nazionale Linee Guida. PNLG 5. Antibioticoprofilassi perioperatoria nell’adulto. Linea Guida. 2003. Available at: https://www.ccm-network.it/documenti_Ccm/prg_area1/Inf_Oss/LG_naz/Pnlg_Antibioticoprofilassi_Adulto.pdf. Accessed 21 April 2022.
42. Ahmed NJ, Almalki ZS, Alfaifi AA, et al. Implementing an antimicrobial stewardship programme to improve adherence to a perioperative prophylaxis guideline. Healthcare (Basel). 2022;10:464.
43. Kilan R, Moran D, Eid I, et al. Improving antibiotic prophylaxis in gastrointestinal surgery patients: a quality improvement project. Ann Med Surg (Lond). 2017;20:6–12.
44. Manniën J, van Kasteren ME, Nagelkerke NJ, et al. Effect of optimized antibiotic prophylaxis on the incidence of surgical site infection. Infect Control Hosp Epidemiol. 2006;27:1340–1346.
45. van Kasteren ME, Kullberg BJ, de Boer AS, Mintjes-de Groot J, Gyssens IC. Adherence to local hospital guidelines for surgical antimicrobial prophylaxis: a multicentre audit in Dutch hospitals. J Antimicrob Chemother. 2003;51:1389–1396.
46. Segala FV, Murri R, Taddei E, et al. Antibiotic appropriateness and adherence to local guidelines in perioperative prophylaxis: results from an antimicrobial stewardship intervention. Antimicrob Resist Infect Control. 2020;9:164.
47. Brindle M, Nelson G, Lobo DN, Ljungqvist O, Gustafsson UO. Recommendations from the ERAS® Society for standards for the development of enhanced recovery after surgery guidelines. BJS Open. 2020;4:157–163.
48. Ficari F, Borghi F, Catarci M, et al. Enhanced recovery pathways in colorectal surgery: a consensus paper by the Associazione Chirurghi Ospedalieri Italiani (ACOI) and the PeriOperative Italian Society (POIS). G Chir. 2019;40(4 suppl):1–40.
49. World Health Organization. The Urgent Need to Implement Patient Blood Management: Policy Brief©. World Health Organization2021. ISBN 978-92-4-003574-4 (electronic version).
50. Hofmann A, Spahn DR, Holtorf AP; PBM Implementation Group. Making patient blood management the new norm(al) as experienced by implementors in diverse countries. BMC Health Serv Res. 2021;21:634.
51. Weber WP, Zwahlen M, Reck S, et al. The association of preoperative anemia and perioperative allogeneic blood transfusion with the risk of surgical site infection. Transfusion. 2009;49:1964–1970.
52. Talbot TR, D’Agata EM, Brinsko V, Lee B, Speroff T, Schaffner W. Perioperative blood transfusion is predictive of poststernotomy surgical site infection: marker for morbidity or true immunosuppressant? Clin Infect Dis. 2004;38:1378–1382.
53. Biondo S, Kreisler E, Fraccalvieri D, Basany EE, Codina-Cazador A, Ortiz H. Risk factors for surgical site infection after elective resection for rectal cancer. a multivariate analysis on 2131 patients. Colorectal Dis. 2012;14:e95–e102.
54. Tang R, Chen HH, Wang YL, et al. Risk factors for surgical site infection after elective resection of the colon and rectum: a single-center prospective study of 2,809 consecutive patients. Ann Surg. 2001;234:181–189.
55. Leahy MF, Hofmann A, Towler S, et al. Improved outcomes and reduced costs associated with a health-system-wide patient blood management program: a retrospective observational study in four major adult tertiary-care hospitals. Transfusion. 2017;57:1347–1358.
56. Grant MC, Yang D, Wu CL, Makary MA, Wick EC. Impact of enhanced recovery after surgery and fast track surgery pathways on healthcare-associated infections: results from a systematic review and meta-analysis. Ann Surg. 2017;265:68–79.
57. Gandaglia G, Ghani KR, Sood A, et al. Effect of minimally invasive surgery on the risk for surgical site infections: results from the National Surgical Quality Improvement Program (NSQIP) Database. JAMA Surg. 2014;149:1039–1044.
58. Romy S, Eisenring MC, Bettschart V, Petignat C, Francioli P, Troillet N. Laparoscope use and surgical site infections in digestive surgery. Ann Surg. 2008;247:627–632.
59. Zhuang CL, Ye XZ, Zhang XD, Chen BC, Yu Z. Enhanced recovery after surgery programs versus traditional care for colorectal surgery: a meta-analysis of randomized controlled trials. Dis Colon Rectum. 2013;56:667–678.
60. Soomro FH, Razzaq A, Qaisar R, Ansar M, Kazmi T. Enhanced recovery after surgery: are benefits demonstrated in international studies replicable in Pakistan? Cureus. 2021;13:e19624.
61. Gronnier C, Grass F, Petignat C, et al. Influence of enhanced recovery pathway on surgical site infection after colonic surgery. Gastroenterol Res Pract. 2017;2017:9015854.
62. World Health Organization. Surgical Site Infection Prevention Guidelines Web Appendix 10 Summary of a systematic review on surgical hand preparation. 2018. Available at: https://cdn.who.int/media/docs/default-source/integrated-health-services-(ihs)/ssi/evidence/appendix10.pdf?sfvrsn=1fac04b_2. Accessed 21 April 2022.
63. Tanner J, Dumville JC, Norman G, Fortnam M. Surgical hand antisepsis to reduce surgical site infection. Cochrane Database Syst Rev. 2016;1:CD004288.
64. World Health Organization Guidelines on Hand Hygiene in Health Care: First Global Patient Safety Challenge Clean Care Is Safer Care. World Health Organization2009. 1, Hand hygiene as a performance indicator. Available at: https://www.ncbi.nlm.nih.gov/books/NBK144028/. Accessed 21 April 2022.
65. Ierano C, Thursky K, Peel T, Rajkhowa A, Marshall C, Ayton D. Influences on surgical antimicrobial prophylaxis decision making by surgical craft groups, anaesthetists, pharmacists and nurses in public and private hospitals. PLoS One. 2019;14:e0225011.
66. A global declaration on appropriate use of antimicrobial agents across the surgical pathway. Surg Infect (Larchmt). 2017;18:846–853.
67. de Jonge SW, Gans SL, Atema JJ, Solomkin JS, Dellinger PE, Boermeester MA. Timing of preoperative antibiotic prophylaxis in 54,552 patients and the risk of surgical site infection: a systematic review and meta-analysis. Medicine (Baltimore). 2017;96:e6903.
68. Weber WP, Mujagic E, Zwahlen M, et al. Timing of surgical antimicrobial prophylaxis: a phase 3 randomised controlled trial. Lancet Infect Dis. 2017;17:605–614.
69. de Jonge SW, Boldingh QJJ, Koch AH, et al. Timing of preoperative antibiotic prophylaxis and surgical site infection: TAPAS, an observational cohort study. Ann Surg. 2021;274:e308–e314.
70. Wolfhagen N, Boldingh QJJ, de Lange M, Boermeester MA, de Jonge SW. Intraoperative redosing of surgical antibiotic prophylaxis in addition to preoperative prophylaxis versus single-dose prophylaxis for the prevention of surgical site infection: a meta-analysis and GRADE recommendation. Ann Surg. 2022;275:1050–1057.
71. Sartelli M, Coccolini F, Carrieri A, Labricciosa FM, Cicuttin E, Catena F. The “Torment” of surgical antibiotic prophylaxis among surgeons. Antibiotics (Basel). 2021;10:1357.
72. Scarborough JE, Mantyh CR, Sun Z, Migaly J. Combined mechanical and oral antibiotic bowel preparation reduces incisional surgical site infection and anastomotic leak rates after elective colorectal resection: an analysis of colectomy-targeted ACS NSQIP. Ann Surg. 2015;262:331–337.
73. Ljungqvist O, Scott M, Fearon KC. Enhanced recovery after surgery: a review. JAMA Surg. 2017;152:292–298.
74. McSorley ST, Steele CW, McMahon AJ. Meta-analysis of oral antibiotics, in combination with preoperative intravenous antibiotics and mechanical bowel preparation the day before surgery, compared with intravenous antibiotics and mechanical bowel preparation alone to reduce surgical-site infections in elective colorectal surgery. BJS Open. 2018;2:185–194.
75. Menz BD, Charani E, Gordon DL, Leather AJM, Moonesinghe SR, Phillips CJ. Surgical antibiotic prophylaxis in an era of antibiotic resistance: common resistant bacteria and wider considerations for practice. Infect Drug Resist. 2021;14:5235–5252.
76. Tanner J, Melen K. Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev. 2021;8:CD004122.
77. Shi D, Yao Y, Yu W. Comparison of preoperative hair removal methods for the reduction of surgical site infections: a meta-analysis. J Clin Nurs. 2017;26:2907–2914.
78. Maiwald M, Chan ES. Pitfalls in evidence assessment: the case of chlorhexidine and alcohol in skin antisepsis. J Antimicrob Chemother. 2014;69:2017–2021.
79. Jolivet S, Lucet JC. Surgical field and skin preparation. Orthop Traumatol Surg Res. 2019;105(1S):S1–S6.
80. Sistla SC, Prabhu G, Sistla S, Sadasivan J. Minimizing wound contamination in a ‘clean’ surgery: comparison of chlorhexidine-ethanol and povidone-iodine. Chemotherapy. 2010;56:261–267.
81. Rodrigues AL, Simões Mde L. Incidence of surgical site infection with pre-operative skin preparation using 10% polyvidone-iodine and 0.5% chlorhexidine-alcohol. Rev Col Bras Cir. 2013;40:443–448.
82. Srinivas A, Kaman L, Raj P, et al. Comparison of the efficacy of chlorhexidine gluconate versus povidone iodine as preoperative skin preparation for the prevention of surgical site infections in clean-contaminated upper abdominal surgeries. Surg Today. 2015;45:1378–1384.
83. Paocharoen V, Mingmalairak C, Apisarnthanarak A. Comparison of surgical wound infection after preoperative skin preparation with 4% chlohexidine and povidone iodine: a prospective randomized trial. J Med Assoc Thai. 2009;92:898–902.
84. Darouiche RO, Wall MJ Jr, Itani KM, et al. Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. N Engl J Med. 2010;362:18–26.
85. Tuuli MG, Liu J, Stout MJ, et al. A randomized trial comparing skin antiseptic agents at cesarean delivery. N Engl J Med. 2016;374:647–655.
86. Ngai IM, Van Arsdale A, Govindappagari S, et al. Skin preparation for prevention of surgical site infection after cesarean delivery: a randomized controlled trial. Obstet Gynecol. 2015;126:1251–1257.
87. World Health Organization Surgical Site Infection Prevention Guidelines. Web Appendix 8. Summary of a systematic literature review on surgical site preparation. 2018. Available at: https://cdn.who.int/media/docs/default-source/integrated-health-services-(ihs)/ssi/evidence/appendix8.pdf?sfvrsn=eaf9f849_2. Accessed 21 April 2022.
88. Sessler DI. Complications and treatment of mild hypothermia. Anesthesiology. 2001;95:531–543.
89. Anderson DJ, Podgorny K, Berríos-Torres SI, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(suppl 2):S66–S88.
90. Kurz A, Sessler DI, Lenhardt R. Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N Engl J Med. 1996;334:1209–1215.
91. Melling AC, Ali B, Scott EM, Leaper DJ. Effects of preoperative warming on the incidence of wound infection after clean surgery: a randomised controlled trial. Lancet. 2001;358:876–880.
92. Wong PF, Kumar S, Bohra A, Whetter D, Leaper DJ. Randomized clinical trial of perioperative systemic warming in major elective abdominal surgery. Br J Surg. 2007;94:421–426.
93. Madrid E, Urrútia G, Roqué i Figuls M, et al. Active body surface warming systems for preventing complications caused by inadvertent perioperative hypothermia in adults. Cochrane Database Syst Rev. 2016;4:CD009016.
94. Gristina AG, Price JL, Hobgood CD, Webb LX, Costerton JW. Bacterial colonization of percutaneous sutures. Surgery. 1985;98:12–19.
95. Storch ML, Rothenburger SJ, Jacinto G. Experimental efficacy study of coated VICRYL plus antibacterial suture in guinea pigs challenged with Staphylococcus aureus. Surg Infect (Larchmt). 2004;5:281–288.
96. Barbolt TA. Chemistry and safety of triclosan, and its use as an antimicrobial coating on Coated VICRYL* Plus Antibacterial Suture (coated polyglactin 910 suture with triclosan). Surg Infect (Larchmt). 2002;3(suppl 1):S45–S53.
97. Diener MK, Knebel P, Kieser M, et al. Effectiveness of triclosan-coated PDS Plus versus uncoated PDS II sutures for prevention of surgical site infection after abdominal wall closure: the randomised controlled PROUD trial. Lancet. 2014;384:142–152.
98. Mattavelli I, Rebora P, Doglietto G, et al. Multi-center randomized controlled trial on the effect of triclosan-coated sutures on surgical site infection after colorectal surgery. Surg Infect (Larchmt). 2015;16:226–235.
99. Apisarnthanarak A, Singh N, Bandong AN, Madriaga G. Triclosan-coated sutures reduce the risk of surgical site infections: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2015;36:169–179.
100. Daoud FC, Edmiston CE Jr, Leaper D. Meta-analysis of prevention of surgical site infections following incision closure with triclosan-coated sutures: robustness to new evidence. Surg Infect (Larchmt). 2014;15:165–181.
101. Edmiston CE Jr, Daoud FC, Leaper D. Is there an evidence-based argument for embracing an antimicrobial (triclosan)-coated suture technology to reduce the risk for surgical-site infections?: A meta-analysis. Surgery. 2013;154:89–100.
102. Guo J, Pan LH, Li YX, et al. Efficacy of triclosan-coated sutures for reducing risk of surgical site infection in adults: a meta-analysis of randomized clinical trials. J Surg Res. 2016;201:105–117.
103. Henriksen NA, Deerenberg EB, Venclauskas L, et al. Triclosan-coated sutures and surgical site infection in abdominal surgery: the TRISTAN review, meta-analysis and trial sequential analysis. Hernia. 2017;21:833–841.
104. Konstantelias AA, Andriakopoulou CS, Mourgela S. Triclosan-coated sutures for the prevention of surgical-site infections: a meta-analysis. Acta Chir Belg. 2017;117:137–148.
105. Leaper DJ, Edmiston CE Jr, Holy CE. Meta-analysis of the potential economic impact following introduction of absorbable antimicrobial sutures. Br J Surg. 2017;104:e134–e144.
106. Uchino M, Mizuguchi T, Ohge H, et al.; SSI Prevention Guideline Committee of the Japan Society for Surgical Infection. The efficacy of antimicrobial-coated sutures for preventing incisional surgical site infections in digestive surgery: a systematic review and meta-analysis. J Gastrointest Surg. 2018;22:1832–1841.
107. Wang ZX, Jiang CP, Cao Y, Ding YT. Systematic review and meta-analysis of triclosan-coated sutures for the prevention of surgical-site infection. Br J Surg. 2013;100:465–473.
108. Wu X, Kubilay NZ, Ren J, et al. Antimicrobial-coated sutures to decrease surgical site infections: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2017;36:19–32.
109. de Jonge SW, Atema JJ, Solomkin JS, Boermeester MA. Meta-analysis and trial sequential analysis of triclosan-coated sutures for the prevention of surgical-site infection. Br J Surg. 2017;104:e118–e133.
110. Ahmed I, Boulton AJ, Rizvi S, et al. The use of triclosan-coated sutures to prevent surgical site infections: a systematic review and meta-analysis of the literature. BMJ Open. 2019;9:e029727.
111. Fowler JR, Perkins TA, Buttaro BA, Truant AL. Bacteria adhere less to barbed monofilament than braided sutures in a contaminated wound model. Clin Orthop Relat Res. 2013;471:665–671.
112. De Simone B, Sartelli M, Coccolini F, et al. Intraoperative surgical site infection control and prevention: a position paper and future addendum to WSES intra-abdominal infections guidelines. World J Emerg Surg. 2020;15:10.
113. Sartelli M, Coccolini F, Abu-Zidan FM, et al. Hey surgeons! It is time to lead and be a champion in preventing and managing surgical infections! World J Emerg Surg. 2020;15:28.
114. Sartelli M, Kluger Y, Ansaloni L, et al. Knowledge, awareness, and attitude towards infection prevention and management among surgeons: identifying the surgeon champion. World J Emerg Surg. 2018;13:37.
115. Raval MV, Bentrem DJ, Eskandari MK, et al. The role of surgical champions in the American College of Surgeons National Surgical Quality Improvement Program–a national survey. J Surg Res. 2011;166:e15–e25.
Keywords:

Antimicrobial resistance; Healthcare-associated infections; Infection prevention and control; Surgical antibiotic prophylaxis; Surgical site infections

Copyright © 2022 The Authors. Published on behalf of the Associazione Chirurghi Ospedalieri Italiani and Wolters Kluwer.