CADTH Health Technology Review

Antibiotic Solutions for Surgical Irrigation

Rapid Review

Authors: Nazia Darvesh, Robyn Butcher

Key Messages

• During surgery, wounds can be washed out, or irrigated, using antibiotic, antiseptic, or saline solutions to prevent infections; the evidence in this report found over 20 different antibiotic solutions used across trials.

• Most studies showed that antibiotic irrigation solutions were better or no different compared to using antiseptic, saline, or no irrigation; however, a small number of studies indicated otherwise. One study reported in a systematic review showed fewer infections and complications for antiseptic compared to a triple antibiotic solution, while another study included in the same systematic review found a higher percentage of implant loss when a triple antibiotic solution was compared to antiseptic; data were poorly reported in these studies.

• Bacitracin-specific evidence was found in 2 studies; 1 study reported in 1 systematic review showed a higher percentage of infection when bacitracin irrigation was compared to cefazolin and saline irrigation; however, this was not statistically significant. Another study showed no differences in infections requiring surgical intervention or in hospitalization when bacitracin irrigation was compared to no irrigation.

• One guideline recommends that wound irrigation and intracavity lavage should not be conducted during surgery, and that applying antibiotics before wound closure should only be done as part of a research trial.

• Due to the mixed findings across studies, high-quality research is needed to clarify the role of antibiotic irrigation during surgery. Because guideline recommendations about wound irrigation, specifically, are based on research published before 2008, updated guidelines to include research from more current studies are needed to reflect current practice.

Context and Policy Issues

A surgical site infection (SSI) is an infection localized to the site where a surgery was performed.¹ SSIs occur after surgery and can involve skin, tissues, organs, or implanted material below the skin.¹ According to the Canadian Patient Safety Institute, 26,000 to 65,000 patients are affected by SSIs per year.² Several practices may be undertaken to prevent SSIs, and these can take place before (preoperative), during (intraoperative), and after (post-operative) surgery.³ One method to manage wounds from surgeries is intraoperative irrigation with a fluid to remove loose material and decrease bacterial load.⁴ A similar technique called intracavity lavage also reduces the risk of SSI when body cavities are exposed during surgery.⁵ Saline, antiseptic, and antibiotic fluid solutions have been used to perform irrigation during surgery.⁴ However, there are several concerns about using irrigation, including whether fluid can wash away important inflammatory cells needed for healing.⁶ In addition, there are questions about the potential of antibiotics to prevent normal healing, damage tissue, or contribute to antimicrobial resistance with overuse.⁶ Further to these concerns, Health Canada conducted a safety review that showed that the antibiotic bacitracin may increase the risk of hypersensitivity, nephrotoxicity, allergic contact dermatitis, or anaphylaxis.⁷ The guidance from Health Canada is that bacitracin is not indicated as an irrigation solution for prophylaxis during surgical procedures because patients may experience nephrotoxicity and anaphylactic reactions.⁷

Given the uncertainty around using antibiotic solutions for surgical irrigation, a review to determine the clinical effectiveness of antibiotic solutions for irrigation during surgery is necessary. In 2021, CADTH compiled a reference list of relevant publications identified from a literature search.⁸ The current report is an upgrade to that CADTH reference list.⁸ The objectives of this rapid review are to summarize the evidence regarding the clinical effectiveness of antibiotic solutions used for irrigation in any surgery, and to determine evidence-based guidelines regarding the use of antibiotic irrigation solutions to prevent surgical infections.

Research Questions

1. What is the clinical effectiveness of antibiotic solutions used in surgical irrigation?

2. What are the evidence-based guidelines regarding the use of antibiotic solutions for surgical irrigation to prevent infection?

Methods

Literature Search Methods

This report makes use of a literature search developed for a previous CADTH report.⁸ For the previous report, a limited literature search was conducted by an information specialist on key resources, including MEDLINE, Embase, the Cochrane Library, the websites of Canadian and major international health technology agencies, as well as a focused internet search. The search strategy comprised both controlled vocabulary, such as the National Library of Medicine’s MeSH (Medical Subject Headings), and keywords. The main search concepts were antibiotic irrigation and surgery. Search filters were applied to limit retrieval to health technology assessments, systematic reviews (SRs), meta-analyses (MAs), or network meta-analyses (NMAs), randomized controlled trials (RCTs) or controlled clinical trials, or guidelines. Comments, newspaper articles, editorials, and letters were excluded. Where possible, retrieval was limited to the human population. The search was also limited to English-language documents published between January 1, 2011, and September 30, 2021.

Selection Criteria and Methods

One reviewer screened citations and selected studies. In the first level of screening, titles and abstracts were reviewed and potentially relevant articles were retrieved and assessed for inclusion. The final selection of full-text articles was based on the inclusion criteria presented in Table 1.

Exclusion Criteria

Articles were excluded if they did not meet the selection criteria outlined in Table 1, or if they were duplicate publications. Where the intervention included antiseptic, antifungal, steroid, or hormone, the study was excluded. Non-solution versions of the intervention (e.g., oral, powder, drops, ointment, cream, foam) or interventions where items were impregnated with antibiotics were excluded. Only interventions that took place during the intraoperative phase were included or summarized. Comparisons between 2 antibiotics were excluded. SRs in which all relevant studies were captured in other more recent or more comprehensive SRs were excluded. Primary studies retrieved by the search were excluded if they were captured in 1 or more included SRs.

Critical Appraisal of Individual Studies

The included publications were critically appraised by 1 reviewer using the following tools as a guide: A MeaSurement Tool to Assess systematic Reviews 2⁹ for SRs, the “questionnaire to assess the relevance and credibility of a network meta-analysis”^10,11 for NMAs, the Downs and Black checklist¹² for RCTs, and the Appraisal of Guidelines for Research and Evaluation II instrument¹³ for guidelines. Summary scores were not calculated for the included studies; rather, the strengths and limitations of each included publication were described narratively.

Summary of Evidence

Quantity of Research Available

A total of 310 citations were identified in the literature search. Following screening of titles and abstracts, 260 citations were excluded and 50 potentially relevant reports from the electronic search were retrieved for full-text review. Seven potentially relevant publications were retrieved from the grey literature search for full-text review. Of these potentially relevant articles, 44 publications were excluded for various reasons, and 13 publications met the inclusion criteria and were included in this report. These comprised 5 SRs,^6,14-17 7 RCTs,^18-24 and 1 evidence-based guideline reported in 2 publications.^25,26 Appendix 1 presents the PRISMA²⁷ flow chart of the study selection.

Additional references of potential interest are provided in Appendix 6.

Summary of Study Characteristics

Study Design

The 5 included SRs^6,14-17 were published between 2018 and 2021 and they had broader inclusion criteria than the scope of this review. An SR by Baker et al.¹⁴ looked at irrigation during implant-based breast surgery using various irrigation solutions of antibiotics and/or antiseptics. The search dates for the SR¹⁴ were unclear, and included 4 retrospective cohort studies that reported interventions and comparators of interest to the current review. An SR by Saeg et al.¹⁷ included any study about wound irrigation published from January 2000 to March 2020, which comprised 1 MA, 2 SRs, and 2 retrospective cohort studies with interventions and comparators relevant to the current review. An SR about antimicrobial irrigation by Leas¹⁵ included literature published from 2017 to 2021, and had 1 study that was relevant to the current review. It should be noted that the primary study was also included in the SR by Saeg et al.;¹⁷ however, the relevant aspects for this report were described in more detail in the Leas publication.¹⁵ An SR with NMA by Thom et al.⁶ included literature published up to February 1, 2017, covering any surgery, and had 20 RCTs relevant to the current review. An SR with MA by López-Cano et al.¹⁶ included literature published up to January 31, 2017, covering any surgery, and had 10 RCTs relevant to the current review. There was some overlap in the primary studies that were included in the SRs; therefore, the narrative summaries and pooled estimates from the SRs may contain some data from the same RCTs. This overlap is presented in Appendix 5, Table 17. Across all 5 SRs^6,14-17 in the current report, population sizes ranged from 14 patients to 8,892 patients, all studies reported on infections, and follow-up time ranged from 8 days to 1 year.

Seven RCTs^18-24 published between 2018 and 2021 were included. One study by Krahn et al.¹⁹ was a cluster randomized crossover trial. All studies included some form of blinding. Six studies were conducted at 1 centre^18,20-24 and 1 study was conducted across 28 centres in Canada and the Netherlands.¹⁹ In 6 RCTs, patients were randomized,^18-21,23,24 and in 1 RCT, mastectomy pockets were randomized.²² Across the 7 RCTs,^18-24 population sizes ranged from 40 to 19,603 and follow-up time ranged from 1 week to 606 days.

One guideline published in 2019²⁶ by the National Institute for Health and Care Excellence (NICE) on prevention and treatment of SSIs is included in the current review. This guideline was an update to a 2008 guideline.²⁵ In this report, both the 2019²⁶ and 2008²⁵ publications are referenced for completeness of reporting. The recommendations for wound irrigation and intracavity lavage were based on the 2008 guideline,²⁵ and the recommendations for antiseptics and antibiotics before wound closure were based on the 2019 guideline.²⁶ Although the NICE guidelines do not provide recommendations specifically for antibiotics, they provide recommendations for wound irrigation, intracavity lavage, and general antiseptic and antibiotic application before wound closure.

Both the 2008 and 2019 versions of the guideline were developed by searching in 6 or more databases and scanning reference lists. The 2008 guideline assessed quality using 8 hierarchical levels with informal and formal consensus steps, while the 2019 guideline used Risk of Bias in Systematic Reviews, the Cochrane risk of bias tool, Risk Of Bias In Non-randomised Studies – of Interventions, and Grading of Recommendations Assessment, Development and Evaluation, depending on study design with a committee discussion of the evidence.

Country of Origin

Three SRs^14,15,17 were from the US, 1 SR⁶ was from England, and 1 SR was from Spain.¹⁶ Among the included RCTs, 3 were from the US,^20,22,24 1 from Egypt,¹⁸ 1 from Iran,²¹ 1 from Nigeria,²³ and 1 was a study conducted across multiple centres in Canada and the Netherlands.¹⁹ The included guideline is for those working in the UK or using services of the National Health Service in England, Wales, and Northern Ireland.²⁵

Patient Population

Three SRs included relevant studies of patients undergoing breast surgery,^14,15,17 1 SR included relevant studies of patients undergoing surgeries with primary site closures,⁶ and 1 SR included relevant studies of patients undergoing various procedures such as abdominal, trauma, biliary tract, colorectal, hernia, breast, soft tissue, or cardiovascular surgeries.¹⁶ One SR⁶ reported that studies had patients of varying age groups, mostly adults, and that some studies such as those with Caesarean sections enrolled only women. Other SRs did not specify age, gender, or sex of included populations.

Across RCTs, included populations were patients undergoing breast reconstruction,²² open appendectomy,¹⁸ laparoscopic colectomy,²¹ neurosurgical procedures,²³ benign gynecologic surgery,²⁴ nonemergent open pancreatoduodenectomy,²⁰ or cardiac implantable electronic device procedures.¹⁹ The mean age ranged from 27.9 to 72.0 years across the RCTs. Two RCTs included only female patients,^22,24 2 RCTs did not specify gender,^20,21 1 RCT had a greater proportion of patients who were female,¹⁸ 1 RCT had a greater proportion of patients who were male.²³ One RCT¹⁹ reported 33.9% patients who were female and did not specify gender for the remaining population. Recognizing that gender and sex are different, gendered terms used in this report reflect the reporting in the included studies, and it is unclear how these terms were defined and measured.

For the included guideline,^25,26 the target population is children, young people, and adults undergoing surgery involving a skin cut. The intended users of the guideline are people having surgeries and their carers, health care professionals, and commissioners and providers.

Interventions and Comparators

Relevant interventions across studies varied and included irrigation and lavage with single or multiple antibiotics solutions such as ampicillin, bacitracin, cefamandole, cefazolin, cefotaxime, cefotetan, cefoxin, cefoxitin, cefuroxime, cephaloridine, cephalothin, cephapirin, cephradine, chloramphenicol, gentamicin with clindamycin, gentamicin, kanamycin with cephalothin, kanamycin, moxalactam, neosporin, polymyxin B, triple antibiotic solution (TAS), taurolin, or tetracycline. All studies that reported TAS as an intervention were included in this report because TAS used in Canada commonly includes a mixture of bacitracin, cefazolin, and gentamicin, which are applicable to the current review. Relevant comparators across studies included saline irrigation and lavage, chlorhexidine gluconate irrigation, or no irrigation. One SR with MA¹⁶ included studies that compared antibiotic irrigation to placebo, where the placebo arm comprised patients who did not have prophylactic topical antibiotic agents, other antibiotics, or antiseptic. In this report, the results for this study are reported in the results for antibiotic irrigation compared to no irrigation.

The specific procedures for surgeries varied across studies. Only antibiotic-related surgical processes are described in this report. In the Nguyen et al. study,²² all patients were given cefazolin intravenously at least 30 minutes before the surgery. The TAS intervention consisted of 50,000 U of bacitracin, 1 g of cefazolin, and 80 mg of gentamicin in 500 mL of normal saline.²² The chlorhexidine gluconate control contained 0.05% chlorhexidine gluconate in sterile water.²² After surgery, all patients were given cefazolin intravenously for 24 hours or until discharge followed by a 14-day treatment of oral sulfamethoxazole and trimethoprim DS 800 mg/160 mg 2 times per day (100 mg doxycycline 2 times per day for patients who had sulfa allergies).²²

In the Emile et al. study,¹⁸ all patients were given 2 g of cefotaxime and 500 mg of metronidazole at anesthesia induction as part of antibiotic prophylaxis. The interventions were either 160 mg of gentamicin in 400 mL of normal saline (0.9% sodium chloride) or normal saline alone applied using a 20 cm syringe to irrigate each layer of the wound before closure.¹⁸ In the control group, layer-by-layer wound closure was performed with polyglactin 2/0 sutures and no irrigation.¹⁸ All patients received 1 g of cefotaxime intravenously within 12 hours of their incisions being closed.¹⁸

In the Negahi et al. study,²¹ the intervention group received lavage with a suction-irrigation machine containing 240 mg of gentamicin and 600 mg of clindamycin dissolved in 500 mL of sterile saline, and the control group received lavage with 500 mL of sterile saline only.

In the Okunlola et al. study,²³ both study groups were given 2 g of parenteral ceftriaxone intravenously when anesthesia commenced and 1 g of ceftriaxone intravenously every 12 hours for 24 hours after surgery. In addition, the intervention group received irrigation with 250 mg/mL of ceftriaxone in normal saline and the control group received plain normal saline irrigation using jet and droplets from a 50 mL syringe.

In the Slopnick et al. study,²⁴ the intervention group received irrigation of a solution containing 200,000 U polymyxin B sulphate and 40 mg neomycin sulphate, while the control group had irrigation with normal saline only. All patients received cefazolin for antibiotic prophylaxis and metronidazole for hysterectomy in patients who were premenopausal unless patients were allergic.²⁴

In the Maatman et al. study,²⁰ the intervention group received irrigation with polymyxin B, 500,000 U in 1 L of normal saline, and the control group received irrigation with 1 L of 0.9% sodium chloride. In both cases, 2 L of each solution was used for irrigation.²⁰ All patients were given 2 g of IV ceftriaxone and 1 g of IV metronidazole within 60 minutes of skin incision.²⁰

In the randomized crossover trial,¹⁹ there were 4 randomly assigned 6-month periods where participating centres used different sequences of incremental or conventional procedures. In the conventional period, a single dose of cefazolin (1 g to 2 g) was given intravenously 60 minutes before skin incision. If patients were allergic to penicillin, vancomycin (1 g to 1.5 g) was given intravenously 120 minutes before skin incision. In addition to the aforementioned procedure with cefazolin or vancomycin, the incremental period applied an intraoperative wound pocket wash using bacitracin 50,000 U diluted in 50 mL of saline before skin closure, and patents were given oral cephalexin (500 mg 4 times per day) or cephadroxil (1,000 mg 2 times per day for 2 days) after the operation. For patients who were allergic to penicillin, clindamycin 150 mg to 300 mg was prescribed 3 times per day. Thus, regarding this report, the relevant comparison in the study¹⁹ was between antibiotic irrigation with bacitracin pocket wash and no irrigation. Authors of the study¹⁹ reported that bacitracin was not available at 1 Canadian site and at all Netherlands sites, so cefazolin or saline pocket wash was administered. Limitations of this procedural change are discussed in the Summary of Critical Appraisal section.

The NICE guideline^25,26 considered all methods before, during, and after surgery to minimize surgery risk. However, the current review focuses only on aspects relating to intraoperative methods for wound irrigation, intracavity lavage, and antibiotic application before wound closure.

Outcomes

Several outcomes were reported across the SRs and RCTs: infection-related outcomes (including SSI, infection requiring surgical intervention, white blood cell count, C-reactive protein [CRP]), capsular contracture (CC), hospital-related outcomes (hospital stay, hospitalization for infection), pain-related outcomes (pain, painkiller needed), patient satisfaction, wound-related outcomes (necrosis, hematoma, seroma, wound dehiscence, wound infection), adverse events and complications (including surgical site occurrence, urine retention or ileus, intra-abdominal abscess, bowel obstruction, intestinal fistula, urinary tract infection (UTI), implant loss, allergic reaction, pancreatic fistula, organ failure, sepsis, delayed gastric emptying, bile leak, venous thromboembolism, cholangitis, myocardial infarction), and death.

Several studies did not provide definitions or had unclear definitions for outcomes. For studies that defined outcomes, 1 SR⁶ and 2 RCTs^18,22 referenced the Centers for Disease Control and Prevention (CDC) definition for SSIs. The CDC definition of an SSI is an infection that happens after surgery in the area of the body (incision, organ, or space) where the surgery occurred.^28,29 In the Nguyen et al. study,²² SSIs were further classified as minor if patients required oral antibiotics; major if patients required IV antibiotics, hospitalization, or incision and washout; or referred to as explantation if patients needed a bilateral explant after developing a persistent non-infectious rash. In the Krahn et al. study,¹⁹ hospitalization for pocket or cardiac implantable electronic device infections was categorized as pocket infection, endocarditis, or bloodstream infection. In the Maatman et al. study, SSIs were defined using another study³⁰ that monitored and reported on SSIs over a 2-year period.

Pain was measured in the Emile et al. study¹⁸ at the 1-week follow-up using the Visual Analogue Scale, which ranged from 0 to 10, with 0 indicating absence of pain at incision site and 10 implying worse severe pain at incision site.

Patient satisfaction with the outcome of the surgery was measured in the Emile et al. study¹⁸ at the 6-week follow-up as unsatisfied, partly satisfied, or completely satisfied indicating causes of dissatisfaction, if applicable.

Surgical site occurrence was measured in the Emile et al. study¹⁸ and included SSI, necrosis, cellulitis, serous or purulent drainage, chronic and/or non-healing wound, seroma, hematoma, wound dehiscence, or fistula at the surgical site.

UTI was measured in the Slopnick et al. study²⁴ at 6 weeks post-surgery. This study adapted the CDC’s definition of a symptomatic UTI: “(1) at least one sign or symptom accompanied by positive urine culture with ≥105 colony‐forming units/mL, (2) symptomatic UTI with clinician decision to treat as reported by the patient, or (3) at least one sign or symptom with positive urine dipstick.”²⁴

Post-operative pancreatic fistula was defined using the definition from the International Study Group on Pancreatic Fistula with a fluid drain output at 3 or more days after surgery and amylase greater than 3 times the upper limit of laboratory normal. Clinically relevant post-operative pancreatic fistula were those graded as B or C as defined by the International Study Group on Pancreatic Fistula.

The 2008 version²⁵ of the NICE guideline considered wound infection rates and SSI, and the 2019 version²⁶ of the guideline considered SSI, mortality, hospital stay, post-operative antibiotic use, adverse events, and complications.

Additional details regarding the characteristics of the included publications are provided in Appendix 2, Table 2, Table 3, and Table 4.

Summary of Critical Appraisal

Systematic Reviews

All 5 SRs^6,14-17 described the interventions and outcomes of interest clearly, 4 SRs^6,14-16 described the specific study populations of interest, and 3 SRs^6,15,16 stated comparator groups of interest. All SRs^6,14-17 included literature from at least 2 databases, which is a strength; however, only 3 SRs^6,16,17 supplemented searches with reference list scanning, and 1 SR with NMA⁶ consulted clinical trial registries and reference lists of other relevant SRs. No SRs reported searching grey literature, which limits the breadth of literature found in these SRs. Only 2 SRs^15,16 established protocols before review conduct; it is unclear, for the remaining SRs,^6,14,17 whether outcomes of interest were established before review conduct.

In 3 SRs,^14,16,17 screening and data extraction were conducted by at least 2 reviewers. In 1 SR,⁶ 2 reviewers screened articles and appraised risk of bias; however, it is unclear whether data extraction was also conducted in duplicate. In 1 SR,¹⁵ it is unclear whether study selection and extraction was conducted in duplicate. In SRs where screening and data extraction were not completed in duplicate, is unclear if there was any bias in the study selected or potential errors in the data extracted and reported from these publications.

The level of detail provided about each included study varied across SRs and no SRs provided sufficient detail on all study characteristics. In 4 SRs,^6,15-17 authors described interventions, comparators, outcomes, and study designs in detail, which is a strength, but patient populations were not described in sufficient detail. One SR¹⁴ did not provide further details on populations, interventions, comparators, and outcomes. Insufficient detail on any study characteristics may limit how the results from these SRs can be applied to other contexts. Three SRs^6,15,16 used an appropriate method to assess risk of bias. One SR¹⁴ did not report assessing risk of bias. Another SR¹⁷ used a method to assess bias but it did not consider study design, confounding, unconcealed allocation, outcome measurement, or reporting bias, and bias was not accounted for when reporting results. For these latter 2 SRs,^14,17 since the risk of bias assessment was not sufficiently completed, the interpretation of results may be limited because the quality of the evidence is unknown. In addition, for 3 SRs,^6,14,17 it is unclear how the reported conflicts of interest or funding may have affected the reporting of the results.

Heterogeneity across studies was considered and described in 4 SRs,^6,14,16,17 which is a strength. In the 1 SR¹⁵ that did not discuss heterogeneity, the impact of potential heterogeneity on the results is unknown. Strengths of the 2 SRs^6,16 that conducted quantitative analyses include that both studies applied appropriate methods for combination of results while taking heterogeneity and risk of bias of individual studies into account. Further, the strengths of the SR with NMA⁶ are that both direct and indirect comparisons were included, inconsistency was assessed, results from individual studies were provided, treatment effect estimates with measures of uncertainty and a rank probability plot with uncertainty were provided, heterogeneity was explored through additional analyses by important patient or publication characteristics. The limitations of the SR with NMA⁶ are that the results are likely biased due to unexplained high heterogeneity and the low quality of individual studies. This limits the conclusions that can be drawn from this SR with NMA.⁶

Randomized Controlled Trials

All 7 RCTs^18-24 sufficiently described their objectives, interventions, and main outcomes, and 4 RCTs^18,20,22,24 clearly described patient characteristics, which is a strength. Further, randomization occurred in all 7 RCTs^18-24 to balance intervention and control groups as much as possible so that effects could be attributed to the intervention; however, in the Nguyen et al. study,²² it remains unclear whether the investigators used appropriate allocation techniques to prevent selection bias. In the randomized crossover trial,¹⁹ since bacitracin was unavailable at 1 Canadian site and all Netherlands sites, a cefazolin or saline pocket wash was administered instead; the results may have been biased because the intervention and comparator groups did not match across study groups. All SRs^18-24 included blinding of study personnel. Three RCTs^19,21,22 had no blinding or unclear blinding of patients; however, because the intervention took place during surgery, it is unlikely that patients would discover what infection prevention protocol they received.

Five RCTs^18,21-24 occurred at single centres and patients were likely from the same population; however, these patients may not be generalizable to other populations beyond these clinical settings. One RCT²⁰ did not clarify if it took place at a single centre or multiple centres.

Five RCTs^18-20,22,23 described main findings and 5 SRs^18-20,22,24 described covariates in sufficient detail. Two RCTs^21,24 did not report complete details, which may limit understanding of the results. Further, 4 RCTs^20-23 did not report clearly on controlling for potential confounders so it is unclear if the results may be biased. It is unclear if statistical tests could adequately answer the research question in 6 RCTs.^18,20-24 In 2 RCTs,^22,23 authors noted that their studies had small sample sizes; these studies may not have been sufficiently powered to detect any effects. In 1 RCT,²¹ a power calculation was not provided so the power is unclear, and in another RCT,²⁴ the study sample was smaller than what the power calculation required. In 1 RCT,¹⁸ the study had sufficient power, but the data were analyzed using a per-protocol approach that did not reflect the randomization assignment and may have biased results. In 1 RCT,²⁴ some covariates were not adjusted for, and in another RCT,²⁰ the low infection rate could not be explained.

Four RCTs^18-20,24 had minimal to no loss to follow-up. In 1 RCT,¹⁹ there was higher noncompliance in the intervention group, which was mainly attributed to administration of oral antibiotics before surgery. In addition, 2 RCTs^21,23 had unclear follow-up and 1 RCT²² had early termination. Within each study, these differences between groups may have biased the results. Loss to follow-up may have affected results if reasons for dropout were related to the intervention.

Guideline

This section considers research included in both the 2008²⁵ and 2019²⁶ versions of the NICE guideline. The overall objectives, health questions, and populations were described in sufficient detail. The guideline described the target population and included important stakeholders in guideline development. Sufficient methods were used to search for evidence, describe evidence selection, appraise the quality of the evidence, considered benefits and harms in formulating recommendations, ensure the guideline was reviewed, and implement a process for updating the guideline. For the 2019 version²⁶ of the guideline, the methods for formulating the recommendations were not described in sufficient detail, and the link between recommendations and supporting evidence was unclear. Key recommendations were clearly visible and auditing criteria were posted. However, the recommendations are to not conduct wound irrigation in general; there are no detailed recommendations about specific antibiotics or preparations to avoid, clear advice on alternative options, or barriers and facilitators to implementing the guidance. Although competing interests of the guideline development group members were recorded, it is unclear how any funding affected formation of the guideline as funding was not reported in the publication.

Additional details regarding the strengths and limitations of included publications are provided in Appendix 3, Table 5, Table 6, and Table 7.

Summary of Findings

Appendix 4 presents the main study findings by outcome in Table 8, Table 9, Table 10, Table 11, Table 12, Table 13, Table 14, Table 15, and Table 16.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Infection

Two SRs^6,14 and 1 RCT²² reported results comparing antibiotic solution to antiseptic solution. In 1 SR with NMA,⁶ results showed that antibiotic irrigation was not statistically superior to antiseptic irrigation. The other SR¹⁴ had relevant data from 2 retrospective cohort studies; 1 demonstrated a statistically significant reduction in risk of infection in the chlorhexidine gluconate (CHG) group compared to the TAS group, while the other study did not report analyses comparing TAS and CHG. One RCT²² included in the current review found that SSI did not differ statistically between TAS and CHG groups, even when results were broken down by infection type (minor, major, explantation).

Four SRs^6,14,15,17 and 4 RCTs^18,20,21,23 reported results comparing antibiotic solution to saline with mixed findings. Two SRs showed that infections were reduced in a cefuroxime and gentamicin group compared to a saline group,¹⁵ a cephalothin group compared to a saline group,¹⁵ and an antibiotic group compared to a normal saline group,¹⁷ based on MA and NMA results. However, 1 SR with MA¹⁶ showed that based on 3 RCTs and 753 patients, beta-lactam antibiotic irrigation solutions were not effective in reducing SSIs compared to no antibiotic solution irrigation. In addition, 1 SR and 3 RCTs showed no statistically significant differences in infection for bacitracin compared to saline,¹⁴ cefazolin compared to saline,¹⁴ gentamicin-saline compared to saline,¹⁸ ceftriaxone compared to saline,²³ and polymyxin B compared to saline.²⁰ One RCT²¹ reported that CRP levels after 12 hours were better in a gentamicin-clindamycin lavage group compared to normal saline lavage group; no further details were provided.

Two RCTs^18,19 compared antibiotic irrigation to no irrigation. One RCT¹⁸ demonstrated a statistically significant lower value of SSIs for a gentamicin-saline group compared to a no irrigation group; however, post hoc analyses showed no statistically significant difference. In a randomized crossover trial,¹⁹ there was no statistically significant difference in infections requiring surgical intervention between bacitracin and no irrigation.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Capsular Contracture

One SR¹⁴ reported results from a retrospective cohort study that found no difference in CC between the TAS and CHG groups.

Three SRs^14,15,17 had mixed results on the effect of antibiotic solution irrigation on CC when compared to saline solution. Two SRs found no differences in CC between a TAS group compared to a saline group in a retrospective cohort study,¹⁴ between a cefuroxime and gentamicin group compared to a saline group,¹⁵ or a cephalothin group compared to a saline group. In 1 SR¹⁷ that included 2 SRs and 2 RCTs, there were mixed findings; 1 retrospective cohort study found a statistically significant reduction in CC in a TAS groups compared to a normal saline group, 1 included MA reported reduced CC with antibiotic irrigation compared to normal saline irrigation, no differences in CC between TAS and normal saline from another retrospective cohort study, and no differences in CC between antibiotic irrigation and normal saline from another included SR.

No studies examined the effectiveness of antibiotic irrigation compared to no irrigation on CC.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Hospital-Related Outcomes

No studies examined the effectiveness of antibiotic irrigation compared to antiseptic irrigation on hospital-related outcomes (e.g., hospital stay, hospitalization). Three RCTs^18,20,21 reported results for the effect of antibiotic irrigation compared to saline irrigation on hospital stay. One RCT²¹ showed that hospital stay in days was lower for the gentamicin-clindamycin lavage group compared to the normal saline lavage group and this was statistically significant. The other 2 RCTs showed no statistically significant differences in hospital stay for a gentamicin-saline group compared to a saline group,¹⁸ and a polymyxin B group compared to saline group.²⁰

Two RCTs comparing gentamicin-saline to no irrigation^18,19 found no statistically significant differences between the 2 regarding hospital stay or hospitalization for infection after surgical procedures.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Pain-Related Outcomes

One RCT¹⁸ showed no difference in pain visual analogue scores between a gentamicin-saline group and a saline group. Another RCT²¹ showed statistically significant differences in mean pain score between gentamicin-clindamycin lavage and normal saline lavage groups at both 3 hours and 24 hours after surgery, and the amount of acetaminophen needed after 24 hours was significantly lower in the gentamicin-clindamycin lavage group. However, no statistically significant differences were seen for the amount of acetaminophen needed after 3 hours of surgery or pethidine needed after 24 hours of surgery.

One RCT¹⁸ showed that pain visual analogue scores were similar between a gentamicin-saline group and a no irrigation group.

No studies examined the effectiveness of antibiotic irrigation compared to antiseptic irrigation on pain-related outcomes.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Patient Satisfaction

One RCT¹⁸ found that a significantly higher percentage of patients in gentamicin-saline and saline groups were completely or partly satisfied with the outcome of their procedures compared to no irrigation; this was statistically significant.

No studies examined the effectiveness of antibiotic irrigation compared to antiseptic irrigation on patient satisfaction.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Wound-Related Outcomes

Results from 3 SRTs^18,21,22 showed no differences in necrosis, hematoma, seroma, and wound infection across study groups.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Adverse Events and Complications

One SR¹⁴ reported that in 1 retrospective cohort study, patients who received irrigation with CHG showed a greater reduction in complications compared to those who had TAS irrigation; this was statistically significant. Another retrospective cohort study in the same SR¹⁴ showed a lower percentage of implant loss in the CHG group compared to the TAS group; however, the level of statistical significance in the difference was not reported. One RCT²² showed that no patients in TAS or CHG groups had any allergic reactions.

Three RCTs^18,20,24 that compared antibiotic to saline irrigation found no statistically significant differences in adverse events or complications between the groups. One RCT¹⁸ showed no differences in surgical site occurrences, or urine retention or ileus between gentamicin-saline and saline groups. Another RCT²⁴ showed no difference in treatment required for UTI between neosporin compared to saline groups, even when limiting results by UTI timing or those needing vaginal prolapse repair. This study²⁴ also reported finding no association between antibiotic irrigation and new urinary frequency or urgency after surgery, and there were no adverse events related to antibiotic irrigation. Another RCT²⁰ found no difference in post-operative pancreatic fistula or clinically relevant post-operative pancreatic fistula between polymyxin B and saline groups. Other complications that showed no statistically significant differences between groups were organ failure, sepsis, delayed gastric emptying, bile leaks, UTIs, venous thromboembolism, cholangitis, or myocardial infarction.

In the RCT¹⁸ that compared gentamicin-saline to no irrigation, surgical site occurrences were significantly lower for gentamicin-saline compared to no irrigation and there were no differences in urine retention or ileus between groups.

A randomized crossover trial¹⁹ showed that adverse events were rare in both bacitracin and no irrigation groups.

Clinical Effectiveness of Antibiotic Irrigation Solutions on Mortality

One RCT²² comparing TAS to CHG indicated that overall, there were 2 patient deaths out of a study population of 88 patients. One RCT²³ comparing ceftriaxone to saline showed that 30-day mortality was 10.6% overall and was not associated with SSI; a breakdown by study groups was not provided. Another RCT²⁰ showed that both 30-day and 90-day mortality were not significantly different for polymyxin groups compared to saline groups.

No studies examined the effectiveness of antibiotic irrigation compared to no irrigation on mortality.

Guidelines Regarding the Use of Antibiotic Solutions for Surgical Irrigation to Prevent Infection

The NICE guideline^25,26 does not recommend wound irrigation to reduce the risk of SSI based on evidence from well-conducted MAs, SRs of RCTs, or RCTs with a low risk of bias. The NICE guideline^25,26 does not recommend intracavity lavage to reduce the risk of SSI based on mixed evidence from well-conducted MAs, SRs of RCTs, or RCTs with a low risk of bias; and 3 trials with high risk of bias. The NICE guideline²⁶ recommends application of antibiotic to the would before closure only when conducting clinical trials, based on 1 low-quality RCT and moderate quality RCT.

Limitations

Limitations to the body of evidence include high heterogeneity, low generalizability, and a lack of guidelines with more recent evidence. Included SRs^6,14-17 noted the high heterogeneity across studies, which varied by surgery type, specific antibiotics used for irrigation, comparator groups, and outcomes measured. Patients undergoing surgery varied greatly and procedures included breast implant surgeries, neurologic procedures, cardiac device operations, gynecological surgeries, and appendectomies, among others. Two SRs^6,16 were conducted on any surgery. The antibiotics studied also varied across studies and comprised over 20 different agents that were used alone or in combinations of 2 or 3 antibiotics in a solution. Comparator groups included antiseptic, saline solution, or no irrigation. Outcomes across studies also varied and were grouped into 8 categories in the current report.

The evidence is also limited by low generalizability. Of the 7 RCTs^18-24 included in this report, 1¹⁹ enrolled patients within Canada and from the Netherlands, whereas the others did not include patients from Canada. Six RCTs^18,20-24 were conducted at single centres; it is unclear whether their results are applicable to populations beyond surgical patients presenting to specific departments in these institutions. Therefore, overall, the generalizability of the findings in the Canadian context is unclear. In addition, it is unclear whether findings in the current report may be replicated for surgeries other than those mentioned in the included evidence.

The current report found 1 evidence-based guideline,^25,26 which included recommendations about wound irrigation and intracavity lavage based on a 2008 version²⁵ of the guideline, and recommendations about antibiotic use before wound closure based on a 2019 version²⁶ of the guideline. For the wound irrigation guideline based on evidence up to 2008, it is unclear whether there are newer studies published in 2008 and later that may change the conclusions. Given that Health Canada recommendations for bacitracin changed in December 2020,⁷ new guidelines may be required to reflect current practice.

Conclusions and Implications for Decision- or Policy-Making

A rapid review was conducted to examine the effectiveness of antibiotic solutions for surgical irrigation, and to summarize recommendations for using antibiotic irrigation to prevent surgical infection. The review is an upgrade of a 2021 CADTH report⁸ that provided a reference list of relevant studies on the topic identified from the literature. The rapid review identified 5 SRs^6,14-17 (1 with MA and 1 with NMA), 7 RCTs,^18-24 and 1 guideline reported in 2 publications,^25,26 published between 2018 and 2021. The current report includes more studies than the CADTH 2021 reference list report⁸ because it evaluated full-text articles to determine relevancy of studies that may have had unclear information from only titles and abstracts. Over 20 different solutions of antibiotics were reported in included studies as interventions, and comparators included antiseptic, saline, or no irrigation.

For studies comparing antibiotic solution to antiseptic solution, no significant effects were found in higher-level evidence (SR⁶ or RCT²²) on infection, while 1 retrospective study included in 1 SR¹⁴ found a significant effect of antibiotic compared to antiseptic solution on infection. One retrospective study included in an SR¹⁴ showed a significant effect of antibiotic irrigation on complications. Across all the included studies, there were no significant effects of antibiotic solution over antiseptic solution on CC or wound-related outcomes, and mixed effects for hospital-related outcomes, pain, and painkiller use.

For studies comparing antibiotic solution to saline, 3^6,15,17 out of 4 SRs showed significant effects on infection, while 3^18,20,23 out of 4 RCTs showed no effects on infection. One RCT²¹ showed that CRP levels were better in the gentamicin-clindamycin lavage group compared to the normal saline lavage group. One RCT¹⁸ found that patients in the antibiotic group were more satisfied with the outcome of their surgery. Across all studies, there were no significant effects or mixed effects of antibiotic solution over saline on CC, hospital stay, pain, and wound-related outcomes. Findings on mortality were unclear due to poor reporting.

For studies comparing antibiotic solution to no irrigation, 1 RCT¹⁸ found higher patient satisfaction when comparing antibiotic to no irrigation. There were mixed effects for antibiotic irrigation on infection, adverse events, and complications, and no effects found for hospital stay, pain, and wound-related outcomes.

The included guideline^25,26 recommended that wound irrigation and intracavity lavage should not be used to reduce SSIs, and that antibiotics should only be applied before closure as part of clinical research trials.

Most studies included in the current review indicated that antibiotic solutions for irrigation were better or no different compared to antiseptic, saline, or no irrigation on various outcomes; however, 1 retrospective study included in 1 poorly reported SR¹⁴ found a significant reduction in infections and complications in a CHG group compared to a TAS group while another retrospective study included in the same SR¹⁴ found a higher percentage of implant loss in the TAS group compared to the CHG group, although no data on statistical significance was reported.

Regarding bacitracin-specific evidence, 1 retrospective cohort study included in 1 poorly reported SR¹⁴ showed a higher percentage of infection in a bacitracin irrigation group when comparing it to cefazolin and saline irrigation groups; however, this was not statistically significant. One randomized crossover trial¹⁹ showed no statistically significant differences between bacitracin irrigation and no irrigation on infections requiring surgical intervention or hospitalization for infections from cardiac rhythm device implants.

The findings of the current review suggest that the literature is mixed regarding any potential benefits or harms of antibiotic solutions for surgical wound irrigation. There was high heterogeneity across studies and most RCTs were either not powered sufficiently to detect any effects or had potential selection bias. No high-quality SRs were found, and several had methodological weaknesses such as search strategies that were not comprehensive, lack of reporting on duplicate screening and extraction, and insufficient reporting of the details of each included study. Future high-quality SRs and RCTs can be conducted to target some of the limitations of the current review, and new primary research where evidence gaps currently exist can be added to the literature (e.g., the effectiveness of antibiotic irrigation compared to no irrigation on CC in breast surgery, antibiotic irrigation compared to antiseptic irrigation on hospital-related outcomes). Because the 1 included guideline^25,26 includes recommendations from 2008 for wound irrigation specifically, an updated guideline with more recent literature that reflects current practice for this type of intervention may be helpful for practitioners.

Because of the mixed findings from the literature, contraindication of bacitracin in recent Health Canada guidance,⁷ and NICE guidelines^25,26 that do not recommend wound irrigation, decision-makers may also consider the resources needed to perform wound irrigation or stop using this process altogether. For example, clinicians may consider whether current non-irrigation infection prevention protocols that take place before, during, and after surgery (e.g., preoperative hand decontamination, post-operative wound cleansing with saline) may be sufficient until updated guidelines with more recent research becomes available.

References

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2.Canadian surgical site infection prevention audit month. Recap report. Ottawa (ON): Canadian Patient Safety Institute; 2016: https://www.patientsafetyinstitute.ca/en/toolsResources/Documents/SSI%20Audit%202016_Recap%20Report%20EN.pdf. Accessed 2022 Jan 12.

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5.Norman G, Atkinson RA, Smith TA, et al. Intracavity lavage and wound irrigation for prevention of surgical site infection. Cochrane Database Syst Rev. 2017;10(10):CD012234. PubMed

6.Thom H, Norman G, Welton NJ, Crosbie EJ, Blazeby J, Dumville JC. Intra-cavity lavage and wound irrigation for prevention of surgical site infection: systematic review and network meta-analysis. Surg Infect (Larchmt). 2021;22(2):144-167. PubMed

7.Bacitracin for injection (50,000 IU per vial) and the risk of nephrotoxicity and anaphylactic reactions. Ottawa (ON): Government of Canada; 2020: https://recalls-rappels.canada.ca/en/alert-recall/bacitracin-injection-50000-iu-vial-and-risk-nephrotoxicity-and-anaphylactic-reactions. Accessed 2022 Jan 12.

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9.Shea BJ, Reeves BC, Wells G, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ. 2017;358:j4008. PubMed

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11.Jansen JP, Trikalinos T, Cappelleri JC, et al. Supplementary material to: Indirect treatment comparison/network meta-analysis study questionnaire to assess relevance and credibility to inform health care decision making: an ISPOR-AMCP-NPC Good Practice Task Force report. Value Health. 2014;17(2):157-173. PubMed

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13.Agree Next Steps Consortium. The AGREE II Instrument. [Hamilton, ON]: AGREE Enterprise; 2017: https://www.agreetrust.org/wp-content/uploads/2017/12/AGREE-II-Users-Manual-and-23-item-Instrument-2009-Update-2017.pdf. Accessed 2021 Dec 8.

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15.Leas B, Talati N. Effectiveness of intra-operative antimicrobial irrigation to prevent surgical site infection in clean surgeries. An evidence review from Penn Medicine’s Center for Evidence-based Practice. Philadelphia (PA): University of Pennsylvania; 2021.

16.López-Cano M, Kraft M, Curell A, et al. Use of topical antibiotics before primary incision closure to prevent surgical site infection: a meta-analysis. Surg Infect (Larchmt). 2019;20(4):261-270. PubMed

17.Saeg F, Schoenbrunner AR, Janis JE. Evidence-based wound irrigation: separating fact from fiction. Plast Reconstr Surg. 2021;148(4):601e-614e. PubMed

18.Emile SH, Elfallal AH, Abdel-Razik MA, El-Said M, Elshobaky A. A randomized controlled trial on irrigation of open appendectomy wound with gentamicin- saline solution versus saline solution for prevention of surgical site infection. Int J Surg. 2020;81:140-146. PubMed

19.Krahn AD, Longtin Y, Philippon F, et al. Prevention of arrhythmia device infection trial: the PADIT trial. J Am Coll Cardiol. 2018;72(24):3098-3109. PubMed

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21.Negahi A, Arminfar A, Vaseghi H, Moradi M, Alemrajabi M. Evaluating the effect of gentamicin-clindamycin lavage on post-operational pain and infection through laparoscopic colectomy surgery. J Coloproctol. 2020 Jan-Mar;40(1):008-011.

22.Nguyen L, Afshari A, Green J, et al. Post-mastectomy surgical pocket irrigation with triple antibiotic solution vs chlorhexidine gluconate: a randomized controlled trial assessing surgical site infections in immediate tissue expander breast reconstruction. Aesthet Surg J. 2021;41(11):NP1521-NP1528. PubMed

23.Okunlola AI, Adeolu AA, Malomo AO, Okunlola CK, Shokunbi MT. Intra-operative wound irrigation with ceftriaxone does not reduce surgical site infection in clean neurosurgical procedures. Br J Neurosurg. 2020:1-4. Online ahead of print. PubMed

24.Slopnick EA, Welles Henderson J, Chapman G, et al. Cystoscopy with antibiotic irrigation during pelvic reconstruction and minimally invasive gynecologic surgery: a double-blind randomized controlled trial. Neurourol Urodyn. 2020;39(8):2386-2393. PubMed

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Appendix 1: Selection of Included Studies

Note that this appendix has not been copy-edited.

Figure 1: Selection of Included Studies

Appendix 2: Characteristics of Included Publications

Note that this appendix has not been copy-edited.

Table 2: Characteristics of Included Systematic Reviews and Network Meta-Analysis

BRC = Biomedical Research Centre; CC = capsular contracture; CHG = chlorhexidine gluconate; MA = meta-analysis; NHS = National Health Service; NIHR = National Institute for Health Research; NMA = network meta-analysis; NRS = nonrandomized study; NR = not reported; RCT = randomized controlled trial; SR = systematic review; SSI = surgical site infection; TAS = triple antibiotic solution

Appendix 3: Critical Appraisal of Included Publications

Note that this appendix has not been copy-edited.

Table 5: Strengths and Limitations of Systematic Reviews and Network Meta-Analyses Using AMSTAR 2⁹ and the ISPOR Questionnaire^10,11

AMSTAR 2 = A MeaSurement Tool to Assess systematic Reviews 2; ISPOR = International Society for Pharmacoeconomics and Outcomes Research; MA = meta-analysis; NMA = network meta-analysis; NRS = nonrandomized study; RCT = randomized controlled trial

Table 6: Strengths and Limitations of Clinical Studies Using the Downs and Black Checklist¹²

Table 7: Strengths and Limitations of Guideline Using AGREE II¹³

AGREE II = Appraisal of Guidelines for Research and Evaluation II

Appendix 4: Main Study Findings and Authors’ Conclusions

Note that this appendix has not been copy-edited.

Table 8: Summary of Findings for Infection-related Outcomes

CHG = chlorhexidine gluconate; CI = confidence interval; CrI = credible interval; CRP = C-reactive protein; MA = meta-analysis; OR = odds ratio; RCT = randomized controlled trial; RR = relative risk; SR = systematic review; SSI = surgical site infection; TAS = triple antibiotic solution; WBC = white blood cells

Table 9: Summary of Findings for Capsular Contracture

CC = capsular contracture; CHG = chlorhexidine gluconate; CI = confidence interval; MA = meta-analysis; RR = relative risk; SR = systematic review; TAS = triple antibiotic solution

Table 10: Summary of Findings for Hospital-Related Outcomes

CI = confidence interval; OR = odds ratio; RCT = randomized controlled trial; SD = standard deviation

Table 11: Summary of Findings for Pain-Related Outcomes

RCT = randomized controlled trial; SD = standard deviation

Table 12: Summary of Findings for Patient Satisfaction

RCT = randomized controlled trial

Table 13: Summary of Findings for Wound-Related Outcomes

CHG = chlorhexidine gluconate; RCT = randomized controlled trial; SSI = surgical site infection; TAS = triple antibiotic solution

Table 14: Summary of Findings for Adverse Events and Complications

CHG = chlorhexidine gluconate; CI = confidence interval; OR = odds ratio; POPF = post-operative pancreatic fistula; RCT = randomized controlled trial; SR = systematic review; SSI = surgical site infection; TAS = triple antibiotic solution; UTI = urinary tract infection

Table 15: Summary of Findings for Mortality

RCT = randomized controlled trial; SSI = surgical site infection

Appendix 5: Overlap Between Included Systematic Reviews

Table 17: Overlap in Relevant Primary Studies Between Included Systematic Reviews

Note: This table has not been copy-edited.

Appendix 6: References of Potential Interest

Previous CADTH Reports

CADTH. 2021; https://www.cadth.ca/antibiotic-solutions-surgical-irrigation.

Review Articles

31.Awad AN, Heiman AJ, Patel A. Implants and breast pocket irrigation: outcomes of antibiotic, antiseptic, and saline irrigation. Aesthet. 2021;09:09.

32.Mann M, Wright CH, Jella T, et al. Cranial surgical site infection interventions and prevention bundles: a systematic review of the literature. World Neurosurg. 2021;148:206-219.e4. PubMed

33.Pop-Vicas AE, Abad C, Baubie K, Osman F, Heise C, Safdar N. Colorectal bundles for surgical site infection prevention: a systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2020;41(7):805-812. PubMed

34.Lynch JM, Sebai ME, Rodriguez-Unda NA, Seal S, Rosson GD, Manahan MA. Breast pocket irrigation with antibiotic solution at implant insertion: a systematic review and meta-analysis. Aesthetic Plast Surg. 2018;42(5):1179-1186. PubMed

35.Nelson RL, Iqbal NM, Kravets A, et al. Topical antimicrobial prophylaxis in colorectal surgery for the prevention of surgical wound infection: a systematic review and meta-analysis. Tech Coloproctol. 2018;22(8):573-587. PubMed

36.Yao R, Tan T, Tee JW, Street J. Prophylaxis of surgical site infection in adult spine surgery: a systematic review. J Clin Neurosci. 2018;52:5-25. PubMed