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Strategies to prevent central line-associated bloodstream infections in acute-care hospitals: 2022 Update

Published online by Cambridge University Press:  19 April 2022

Niccolò Buetti
Affiliation:
Infection Control Programme, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland University of Paris, Paris, France
Jonas Marschall
Affiliation:
Department of Infectious Diseases, Bern University Hospital and University of Bern, Bern, Switzerland Division of Infectious Diseases, Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, United States
Marci Drees
Affiliation:
ChristianaCare, Wilmington, Delaware, United States Sidney Kimmel Medical College at Thomas Jefferson University, Philadelphia, Pennsylvania, United States
Mohamad G. Fakih
Affiliation:
Ascension Healthcare and Wayne State University School of Medicine, Detroit, Michigan, United States
Lynn Hadaway
Affiliation:
Lynn Hadaway Associates, Milner, Georgia, United States
Lisa L. Maragakis
Affiliation:
Johns Hopkins University School of Medicine, Baltimore, Maryland, United States
Elizabeth Monsees
Affiliation:
Children’s Mercy Hospital, Kansas City, Missouri, United States University of Missouri–Kansas City School of Medicine, Kansas City, Missouri, United States,
Shannon Novosad
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia, United States
Naomi P. O’Grady
Affiliation:
National Institutes of Health, Bethesda, Maryland, United States
Mark E. Rupp
Affiliation:
University of Nebraska Medical Center, Omaha, Nebraska, United States
Joshua Wolf
Affiliation:
Department of Infectious Diseases, St. Jude Children’s Research Hospital, Memphis, Tennessee, United States Department of Pediatrics, University of Tennessee Health Science Center, Memphis, Tennessee, United States
Deborah Yokoe
Affiliation:
University of California–San Francisco, San Francisco, California, United States
Leonard A. Mermel*
Affiliation:
Warren Alpert Medical School of Brown University, Providence, Rhode Island, United States Rhode Island Hospital, Providence, Rhode Island, United States
*
Author for correspondence: Dr. Leonard A. Mermel, E-mail: lmermel@lifespan.org
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Abstract

Type
SHEA/IDSA/APIC Practice Recommendation
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

Purpose

Previously published guidelines provide comprehensive recommendations for detecting and preventing healthcare-associated infections (HAIs). The intent of this document is to highlight practical recommendations in a concise format designed to assist acute-care hospitals in implementing and prioritizing their central line-associated bloodstream infection (CLABSI) prevention efforts. This document updates the Strategies to Prevent Central Line-Associated Bloodstream Infections in Acute-Care Hospitals published in 2014. Reference Marschall, Mermel and Fakih1 This expert guidance document is sponsored by the Society for Healthcare Epidemiology of America (SHEA). It is the product of a collaborative effort led by SHEA, the Infectious Diseases Society of America (IDSA), the Association for Professionals in Infection Control and Epidemiology (APIC), the American Hospital Association (AHA), and The Joint Commission, with major contributions from representatives of a number of organizations and societies with content expertise.

Summary of major changes

This section lists major changes from the Strategies to Prevent Central Line-Associated Bloodstream Infections in Acute-Care Hospitals: 2014 Update, Reference Marschall, Mermel and Fakih1 including recommendations that have been added, removed, or altered. Recommendations are categorized as essential practices that should be adopted by all acute-care hospitals (in 2014 these were “basic practices,” renamed to highlight their importance as foundational for hospitals’ HAI prevention programs) or additional approaches that can be considered for use in locations and/or populations within hospitals when CLABSIs are not controlled after implementation of essential practices (in 2014 these were “special approaches”). See Table 1 for a complete summary of the recommendations contained in this document.

Table 1. Summary of Recommendations to Prevent CLABSI

Note. CLABSI, central line-associated bloodstream infection; CVC, central venous catheter; HCP, healthcare personnel; ICU, intensive care unit.

Essential practices

  • The subclavian vein is considered the preferable site for central venous catheter (CVC) insertion in the intensive care setting to reduce infectious complications. Previously, the primary recommendation was to avoid the femoral vein for access. Although this remains valid, it has been replaced by a positively formulated recommendation regarding the subclavian site.

  • The recommendation to use ultrasound guidance for catheter insertion is backed by better evidence than was available previously; however, the procedure itself may jeopardize the strict observation of sterile technique.

  • The use of chlorhexidine-containing dressings is now considered an “essential practice”; in the past, it was listed under special approaches that should only be employed if CLABSI rates remain high despite the implementation of basic practices.

  • Routine replacement of administration sets not used for blood, blood products, or lipid formulations can be performed at intervals of up to 7 days. Previously, this interval was no longer than 4 days.

Additional approaches

  • Antimicrobial ointment for the catheter site, which is geared toward the population of hemodialysis patients, has been moved to “additional practices” given the focus on a specific population.

  • Despite currently being supported by high-level evidence, antiseptic-containing caps remain an “additional practice” because they are not considered superior to the manual disinfection, an essential practice.

  • The importance of infusion teams has been highlighted by listing it under “additional practices” (previously considered unresolved).

  • Sutureless securement of catheters was not discussed in the previous version of this section.

Intended use

This document was developed following the process outlined in the Handbook for SHEA-Sponsored Guidelines and Expert Guidance Documents. 2 No guideline or expert guidance document can anticipate all clinical situations, and this document is not meant to be a substitute for individual clinical judgment by qualified professionals.

This document is based on a synthesis of evidence, theoretical rationale, current practices, practical considerations, writing-group consensus, and consideration of potential harm, where applicable. A summary list of recommendations is provided along with their relevant rationales (see Table 1).

Methods

SHEA recruited 3 subject-matter experts in the prevention of CLABSI to lead the panel of members representing the Compendium partnering organizations: SHEA, the Infectious Diseases Society of America (IDSA), the Association for Professionals in Infection Control and Epidemiology (APIC), the American Hospital Association (AHA), and The Joint Commission, as well as representation by the Centers for Disease Control and Prevention (CDC).

SHEA utilized a consultant medical librarian, who worked with each panel to develop a comprehensive search strategy for PubMed and Embase (January 2012–July 2019; updated to August 2021). Articles’ abstracts were reviewed by panel members in a double-blind fashion using the abstract management software, Covidence (Melbourne, Australia), and subsequently reviewed as full text. The Compendium Lead Authors group voted to update the literature findings, and the librarian reran the search to update it to August 2021. Panel members reviewed the abstracts of these articles via Covidence and incorporated relevant references.

Recommendations resulting from this literature review process were classified based on the quality of evidence and the balance between desirable and potential for undesirable effects of various interventions (see Table 2). Panel members met via video conference to discuss literature findings; recommendations; quality of evidence for these recommendations; and classification as essential practices, additional approaches, or unresolved issues. Panel members reviewed and approved the document and its recommendations.

Table 2. Quality of Evidence a

a Based on the CDC Healthcare Infection Control Practices Advisory Committee (HICPAC) “Update to the Centers for Disease Control and Prevention and the Healthcare Infection Control Practices Advisory Committee Recommendations Categorization Scheme for Infection Control and Prevention Guideline Recommendations” (October 2019), the Grades of Recommendation, Assessment, Development, and Evaluation (GRADE), Reference Guyatt, Oxman and Vist265 and the Canadian Task Force on Preventive Health Care. 266

The Compendium Expert Panel, made up of members with broad healthcare epidemiology and infection prevention expertise, reviewed the draft manuscript after consensus had been reached by writing panel members.

Following review and approval by the Expert Panel, the 5 partnering organizations, stakeholder organizations, and the CDC reviewed the document. Prior to dissemination, the guidance document was reviewed and approved by the SHEA Guidelines Committee, the IDSA Standards and Practice Guidelines Committee, and the Boards of SHEA, IDSA, APIC, AHA, and The Joint Commission.

All panel members complied with SHEA and IDSA policies on conflict-of-interest disclosure.

Section 1: Rationale and statements of concern

Burden of outcomes associated with hospital-acquired CLABSI

  1. 1. Increased length of hospital stay Reference Digiovine, Chenoweth, Watts and Higgins3Reference Leistner, Hirsemann, Bloch, Gastmeier and Geffers6

  2. 2. Increased cost. The adjusted variable costs for patients with CLABSI were $32,000 (2010 US dollars) higher on average than for patients without CLABSI Reference Stevens, Geiger, Concannon, Nelson, Brown and Dumyati7

  3. 3. Increased morbidity and mortality Reference Ziegler, Pellegrini and Safdar8

Risk factors for CLABSI

  1. 1. Patients at risk for CLABSI in acute-care facilities are those with a CVC in place:

    1. a. Intensive care unit (ICU) population: The risk of CLABSI in ICU patients is high. Reasons for this include the frequent insertion of multiple catheters Reference Dube, Jacob and Zheng9,Reference Mermel10 ; the use of specific types of catheters that are almost exclusively inserted in ICU patients and associated with substantial risk (eg, pulmonary artery catheters with catheter introducers); and the fact that catheters are frequently placed in emergency circumstances, repeatedly accessed each day, and often needed for extended periods. Reference Maki, Kluger and Crnich11,12

    2. b. Non-ICU population: Although the primary focus of attention over the last 20 years has been the ICU setting, most CLABSIs occur in hospital units outside the ICU or in outpatients. Reference Marschall, Leone, Jones, Nihill, Fraser and Warren13Reference Rhee, Heung, Chen and Chenoweth17

  2. 2. Infection prevention and control efforts should include other vulnerable populations such as patients receiving hemodialysis through catheters, Reference Nguyen, Shugart and Lines18 intraoperative patients, Reference Loftus, Brown and Koff19 and oncology patients. Reference Zakhour, Chaftari and Raad20

  3. 3. In addition to CVCs, short-term peripheral catheters, Reference Mermel21 peripherally inserted central venous catheters (PICCs), midline catheters, and peripheral arterial catheters also carry a risk of infection. Reference O’Horo, Maki, Krupp and Safdar22

  4. 4. Independent risk factors for CLABSI (in at least 2 published studies) Reference Almuneef, Memish, Balkhy, Hijazi, Cunningham and Francis23Reference Timsit, Mimoz and Mourvillier45

    1. a. Prolonged hospitalization before catheterization

    2. b. Prolonged duration of catheterization

    3. c. Heavy microbial colonization at insertion site

    4. d. Heavy microbial colonization of the catheter hub

    5. e. Multilumen catheters

    6. f. Concurrent catheters

    7. g. Neutropenia

    8. h. Body mass index (BMI) >40

    9. i. Prematurity (ie, early gestational age)

    10. j. Reduced nurse-to-patient ratio in the ICU

    11. k. Parenteral nutrition

    12. l. Substandard catheter care (eg, excessive manipulation of the catheter)

    13. m. Transfusion of blood products (in children)

Section 2: Background on detection of CLABSI

Surveillance methods and definitions for CLABSI

  1. 1. Use consistent surveillance methods and definitions to allow comparison to benchmark data.

  2. 2. Refer to the National Healthcare Safety Network (NHSN) Patient Safety Component Manual for information on the appropriate surveillance methodology, including information about blood specimen collection and surveillance definitions of CLABSIs. The relevant chapter of the manual is “Chapter 4: Bloodstream Infection Event (Central Line-Associated Bloodstream Infection and Non-Central Line-Associated Bloodstream Infection).” 46

    1. a. Recent data suggest that interrater reliability using NHSN definitions is lower than expected. Reference Grooth, Timsit and Mermel47Reference Mayer, Greene, Howell, Ying, Rubin and Trick50 This may also affect the reliability of public reporting.

    2. b. The NHSN surveillance definition for CLABSI is different than the clinical definition for catheter-related bloodstream infection (CRBSI). The latter is subject to various factors (eg, laboratory capabilities, catheter removal, and submitting the catheter tip for culture). Reference Mermel, Allon and Bouza51 The evidence presented here includes studies that used either CLABSI or CRBSI as an outcome measure and the lesser accuracy of CLABSI may impact the validity of the evidence.

Section 3: Background on prevention of CLABSI

Summary of existing guidelines and recommendations

  1. 1. Several governmental, public health, and professional organizations have published evidence-based guidelines and/or implementation aids regarding the prevention of CLABSI including the following:

    1. a. Healthcare Infection Control Practices Advisory Committee (HICPAC), Centers for Disease Control and Prevention (CDC) Reference O’Grady, Alexander and Dellinger52,Reference O’Grady, Alexander and Burns53

    2. b. Institute for Healthcare Improvement (IHI) Reference Masse, Elkalioubie and Blazejewski54

    3. c. Agency for Healthcare Research and Quality, Making Health Care Safer Reference Saint55

    4. d. American Pediatric Surgical Association, Outcomes and Clinical Trials Committee Reference Huang, Chen and Abdullah56

    5. e. The Joint Commission 57

    6. f. APIC, Implementation Guide to Preventing Central Line-Associated Bloodstream Infections Reference Barnes, Olmsted and Monsees58

    7. g. Infusion Nurses Society, Infusion Nursing Standards of Practice Reference Gorski, Hadaway and Hagle59

  2. 2. The recommendations in this document focus on CVCs unless noted otherwise. These recommendations:

    1. a. Are not stratified based on the type of catheter (eg, tunneled, implanted, cuffed, non-cuffed catheter, dialysis catheter).

    2. b. May not be applicable in their entirety for prevention of bloodstream infections with other intravascular devices.

Infrastructure requirements

Facilities undertaking CLABSI interventions should have the following elements in place:

  1. 1. An adequately staffed infection prevention and control program responsible for identifying patients who meet the surveillance definition for CLABSI.

  2. 2. Infection prevention staff and, preferably, information technology support to collect and calculate catheter days as a denominator when computing rates of CLABSI and patient days to allow calculation of CVC utilization. Catheter days from information systems should be validated against a manual method, with a margin of error no greater than ±5%. 60Reference Woeltje, McMullen, Butler, Goris and Doherty62

  3. 3. Resources to provide appropriate education and training.

  4. 4. Adequate laboratory support for timely processing of specimens and reporting of results, as specified by the supervisor of the surveillance program.

Section 4: Recommended strategies to prevent CLABSI

Recommendations are categorized as either (1) essential practices that should be adopted by all acute-care hospitals or (2) additional approaches that can be considered in locations and/or populations within hospitals when CLABSIs are not controlled by use of essential practices. Essential practices include recommendations in which the potential to affect CLABSI risk clearly outweighs the potential for undesirable effects. Additional approaches include recommendations in which the intervention is likely to reduce CLABSI risk but there is concern about the risks for undesirable outcomes, recommendations for which the quality of evidence is low, recommendations in which cost-to-benefit ratio may be high, or recommendations in which evidence supports the impact of the intervention in select settings (eg, during outbreaks) or for select patient populations. Hospitals can prioritize their efforts by initially focusing on implementation of the prevention strategies listed as essential practices. If CLABSI surveillance or other risk assessments suggest ongoing opportunities for improvement, hospitals should consider adopting some or all of the prevention approaches listed as additional approaches. These can be implemented in specific locations or patient populations or can be implemented hospital-wide, depending on outcome data, risk assessment, and/or local requirements. Each infection prevention recommendation is given a quality of evidence grade (see Table 2).

Essential practices for preventing CLABSI recommended for all acute-care hospitals

Some of the following measures have been combined into a “prevention bundle” that focuses on catheter insertion. Reference Pronovost, Watson, Goeschel, Hyzy and Berenholtz63,64 Numerous studies have documented that use of such bundles is effective, sustainable, and cost-effective in both adults and children. Reference Pronovost, Watson, Goeschel, Hyzy and Berenholtz63,Reference Kim, Holtom and Vigen65Reference Ista, van der Hoven and Kornelisse68 Bundles are most likely to be successful if implemented in a previously established patient safety culture and their success depends on adherence to individual measures. Reference Richter and McAlearney69 However, data suggests that not all components of bundles may be necessary to achieve an effect on CLABSI rates. Reference Furuya, Dick, Perencevich, Pogorzelska, Goldmann and Stone70 After catheter insertion, maintenance bundles have been proposed to ensure optimal catheter care. Reference Guerin, Wagner, Rains and Bessesen71 More data are needed to determine which components of the maintenance bundle are essential in reducing risk. Reference Miller, Niedner and Huskins72,Reference O’Neil, Ball and Wood73

Before insertion

  1. 1. Provide easy access to an evidence-based list of indications for CVC use to minimize unnecessary CVC placement (Quality of Evidence: LOW)

  2. 2. Require education and competency assessment of healthcare personnel (HCP) involved in insertion, care, and maintenance of CVCs about CLABSI prevention (Quality of Evidence: MODERATE) Reference Sherertz, Ely and Westbrook74Reference Warren, Zack and Mayfield78

    1. a. Include the indications for catheter use, appropriate insertion and maintenance, the risk of CLABSI, and general infection prevention strategies.

    2. b. Ensure that all HCP involved in catheter insertion and maintenance complete an educational program on essential practices to prevent CLABSI before performing these duties. Reference Lobo, Levin and Oliveira79,Reference Cherry, Brown, Neal and Ben Shaw80 Periodic retraining with a competency assessment may be of benefit. 81

    3. c. Periodically assess HCP knowledge of and adherence to preventive measures.

    4. d. Require all HCP who insert a CVC to undergo a credentialing process (as established by the individual healthcare institution) to ensure their competency before independently inserting a CVC and aseptic technique for accessing and maintaining the CVC thereafter.

    5. e. Re-educate when an institution changes components of the infusion system that requires a change in practice (eg, when an institution’s change of the needleless connector requires a change in nursing practice).

    6. f. Use simulation training for proper catheter insertion and maintenance if available. Reference Barsuk, Cohen and Potts82Reference Ma, Brindle, Ronksley, Lorenzetti, Sauve and Ghali85

  3. 3. Bathe ICU patients >2 months of age with a chlorhexidine preparation on a daily basis (Quality of Evidence: HIGH) Reference Bleasdale, Trick, Gonzalez, Lyles, Hayden and Weinstein86Reference Afonso, Blot and Blot90

    1. a. In long-term acute-care hospitals (LTACHs), daily chlorhexidine bathing may also be considered as a preventive measure. Reference Munoz-Price, Hota, Stemer and Weinstein91

    2. b. The role of chlorhexidine bathing in non-ICU patients remains unclear. Reference Medina, Serratt, Pelter and Brancamp92,Reference Huang, Septimus and Kleinman93 One cluster-randomized study found a significant reduction in device-associated bacteremia with CHG bathing in this patient population Reference Huang, Septimus and Kleinman93 ; however, some of these patients also received methicillin-resistant Staphylococcus aureus (MRSA) decolonization, making it difficult to draw firm conclusions regarding CHG bathing alone. Several studies have suggested benefit among adult hematology-oncology patients; however, a similar reduction was not observed for pediatric patients with similar conditions. Reference Tien, Sheng and Shieh94,Reference Zerr, Milstone and Dvorak95 Accordingly, potential benefits and risks, such as increases in resistance and cost, need to be carefully considered.

    3. c. The safety and efficacy of routine use of chlorhexidine bathing in infants <2 months of postnatal age remains unclear. Reference Milstone, Bamford, Aucott, Tang, White and Bearer96 Although life-threatening skin injuries from CHG have been reported in very young or very preterm infants, they typically occur in infants with a birthweight <1,000 g who are <7 days postnatal age, and they appear rare in older infants. Reference Kieran, O’Sullivan, Miletin, Twomey, Knowles and O’Donnell97Reference Chandonnet, Toole and Young99

    4. d. Widespread use of chlorhexidine may be associated with decreased chlorhexidine susceptibility, although the clinical relevance of this finding is not well defined. Reference Kampf100

At insertion

  1. 1. In ICU and non-ICU settings, a facility should have a process in place, such as a checklist, to ensure adherence to infection prevention practices at the time of CVC insertion (Quality of Evidence: MODERATE) Reference Wichmann and Belmar Campos101

    1. a. Ensure and document adherence to aseptic technique

      1. i. Checklists have been suggested to ensure optimal insertion practices. If used, the documentation should be done by someone other than the inserter.

      2. ii. Observation of CVC insertion should be done by a nurse, physician, or other HCP who has received appropriate education (see above) to ensure that aseptic technique is maintained.

      3. iii. HCP should be empowered to stop the procedure if breaches in aseptic technique are observed.

  2. 2. Perform hand hygiene prior to catheter insertion or manipulation (Quality of Evidence: MODERATE) Reference Elgohari, Wilson, Saei, Sheridan and Lamagni102Reference van der Kooi, Sax and Pittet107

    1. a. Use an alcohol-based waterless product or soap and water.

      1. i. Use of gloves does not obviate hand hygiene.

  3. 3. The subclavian site is preferred to reduce infectious complications when the catheter is placed in the ICU setting (Quality of Evidence: HIGH) Reference Parienti, Mongardon and Megarbane33,Reference Merrer, De Jonghe and Golliot37,Reference Arvaniti, Lathyris, Blot, Apostolidou-Kiouti, Koulenti and Haidich108Reference Timsit, Bouadma and Mimoz110

    1. a. In the non-ICU setting, the risk of infection between the different sites remains unclear. Importantly, in emergent settings, ensuring life-saving vascular access in the fastest possible way may determine the choice of access site.

    2. b. In children and infants, femoral vein catheterization may be considered if upper body sites are contraindicated. Reference Ullman, Bernstein and Brown111 Tunneled femoral vein catheters, with an exit site outside the diaper area in the mid-thigh, may be safer and provide additional risk reduction. Reference Chau, Hernandez, Pimpalwar, Ashton and Kukreja112,Reference Gaballah, Krishnamurthy and Berman113

    3. c. Controversy exists regarding infectious and noninfectious complications associated with different short-term CVC access sites. Reference Parienti, Mongardon and Megarbane33 The risk and benefit of different insertion sites must be considered on an individual basis with regard to infectious and noninfectious complications. Reference Parienti, Mongardon and Megarbane33 Among others, this applies to patients currently receiving or likely to require hemodialysis in whom the subclavian site is avoided due to risk of stenosis.

    4. d. Do not use peripherally inserted central venous catheters (PICCs) as a strategy to reduce the risk of CLABSI. Risk of infection with PICCs in hospitalized patients approaches that of other CVCs. Reference Chopra, O’Horo, Rogers, Maki and Safdar114 However, the majority of CLABSIs due to PICCs occur in non-ICU settings. Reference Ajenjo, Morley and Russo115

    5. e. Midline catheters are increasingly being used as an alternative to CVCs for short-term vascular access, with some observational studies suggesting lower bloodstream infection risk associated with midline catheters versus PICCs Reference Swaminathan, Flanders, Horowitz, Zhang, O’Malley and Chopra116 and versus CVCs, Reference Mushtaq, Navalkele and Kaur117 respectively. Randomized controlled trials comparing the risk of bloodstream infections and other complications associated with these devices are needed.

  4. 4. Use an all-inclusive catheter cart or kit (Quality of Evidence: MODERATE) Reference Berenholtz, Pronovost and Lipsett118

    1. a. A catheter cart or kit that contains all necessary components for aseptic catheter insertion should be available and easily accessible in all units where CVCs are inserted.

  5. 5. Use ultrasound guidance for catheter insertion (Quality of Evidence: HIGH) Reference Karakitsos, Labropoulos and De Groot119,Reference Brass, Hellmich, Kolodziej, Schick and Smith120

    1. a. Ultrasound-guided internal jugular and femoral vein catheterization reduces the risk of noninfectious complications associated with CVC placement Reference Hind, Calvert and McWilliams121 but the use of ultrasound may lead to a breach in aseptic technique. Reference Buetti, Mimoz and Mermel122

    2. b. It is unclear whether ultrasound-guided subclavian vein insertion reduces risk of infectious complications.

  6. 6. Use maximum sterile barrier precautions during CVC insertion (Quality of Evidence: MODERATE) Reference Mermel, McCormick, Springman and Maki123Reference Lee, Jung and Choi128

    1. a. Use maximum sterile barrier precautions:

      1. i. A mask, cap, sterile gown, and sterile gloves are to be worn by all HCP involved in the catheter insertion procedure.

      2. ii. The patient is to be covered with a large (“full-body”) sterile drape during catheter insertion.

    2. b. These measures should also be followed when exchanging a catheter over a guidewire.

    3. c. A prospective, randomized study in surgical patients showed no additional benefit for maximum sterile barrier precautions Reference Ishikawa, Kiyama and Haga126 ; nevertheless, most available evidence suggests risk reduction with this intervention.

  7. 7. Use an alcoholic chlorhexidine antiseptic for skin preparation (Quality of Evidence: HIGH) Reference Mimoz, Lucet and Kerforne42,Reference Garland, Buck and Maloney129Reference Masuyama, Yasuda, Sanui and Lefor134

    1. a. Before catheter insertion, apply an alcoholic chlorhexidine solution containing at least 2% chlorhexidine gluconate to the insertion site.

      1. i. The antiseptic solution must be allowed to dry before making the skin puncture.

      2. ii. Alcoholic chlorhexidine for skin antisepsis to prevent CLABSI in NICU patients should be used when the benefits are judged to outweigh potential risk.

After insertion

  1. 1. Ensure appropriate nurse-to-patient ratio and limit use of float nurses in ICUs (Quality of Evidence: HIGH) Reference Fridkin, Pear, Williamson, Galgiani and Jarvis34,Reference Cimiotti, Haas, Saiman and Larson35

    1. a. Observational studies suggest that an adequate nurse-to-patient ratio must be maintained in ICUs where nurses are managing patients with CVCs and that the number of float nurses working in the ICU environment should be minimized.

  2. 2. Use chlorhexidine-containing dressings for CVCs in patients over 2 months of age (Quality of Evidence: HIGH) Reference Timsit, Mimoz and Mourvillier45,Reference Garland, Alex and Mueller135Reference Puig-Asensio, Marra, Childs, Kukla, Perencevich and Schweizer142

    1. a. It is unclear whether there is additional benefit with use of a chlorhexidine-containing dressing if daily chlorhexidine bathing is already established and vice-versa.

    2. b. For long-term catheters (eg, hemodialysis catheters) in well-healed access sites, it is unclear whether use of a chlorhexidine dressing reduces risk of infectious complications. Reference Camins, Richmond and Dyer140,Reference Righetti, Palmieri and Bracchi143,Reference Apata, Hanfelt, Bailey and Niyyar144

    3. c. For children under 2 months of age, use of chlorhexidine dressings remains unclear, particularly in very preterm or low birthweight infants. Reference Neri, Ravaioli, Faldella, Capretti, Arcuri and Patrizi98

  3. 3. For nontunneled CVCs in adults and children, change transparent dressings and perform site care with a chlorhexidine-based antiseptic at least every 7 days or immediately if the dressing is soiled, loose, or damp. Change gauze dressings every 2 days or earlier if the dressing is soiled, loose, or damp. (Quality of Evidence: MODERATE) Reference Maki, Stolz, Wheeler and Mermel145Reference Gavin, Webster, Chan and Rickard148

    1. a. Less frequent, clinically indicated dressing changes may be used for NICU patients or others at high risk of serious complications from catheter dislodgement. Reference Short149

    2. b. If there is excessive bleeding or drainage from the catheter exit site, use gauze dressings instead of transparent dressings until drainage resolves.

  4. 4. Disinfect catheter hubs, needleless connectors, and injection ports before accessing the catheter (Quality of Evidence: MODERATE) Reference Salzman, Isenberg and Rubin150Reference Soothill, Bravery, Ho, Macqueen, Collins and Lock154

    1. a. Before accessing catheter hubs, needleless connectors, or injection ports, vigorously apply mechanical friction with an alcoholic chlorhexidine preparation, or 70% alcohol. Alcoholic chlorhexidine may have additional residual activity compared to alcohol for this purpose and is therefore preferred. Reference Hong, Morrow, Sandora and Priebe155

    2. b. Apply mechanical friction for a minimum of 5 seconds to reduce contamination. Reference Rupp, Yu and Huerta156,Reference Simmons, Bryson and Porter157 It is unclear whether this duration of disinfection can be generalized to needleless connectors not tested in these studies.

    3. c. Monitor compliance with hub-connector-port disinfection because approximately half of such catheter components are colonized under conditions of standard practice. Reference Casey, Worthington, Lambert, Quinn, Faroqui and Elliott152,Reference Rupp, Yu and Huerta156,Reference Hankins, Majorant and Rupp158

  5. 5. Remove nonessential catheters (Quality of Evidence: MODERATE)

    1. a. Assess the need for continued intravascular access on a daily basis during multidisciplinary rounds. Remove catheters not required for patient care. Decreasing CVC utilization reduces CRBSI risk. Reference van der Kooi, Sax and Pittet159 However, reducing CVC utilization may result in increased use of other intravascular catheters with corresponding infection risk.

    2. b. Audits to determine whether CVCs are routinely removed after their intended use may be helpful. Reference Rotz and Sopirala160,Reference Cload, Day and Ilan161 Both simple and multifaceted interventions are effective at reducing unnecessary CVC use. Reference Seguin, Laviolle, Isslame, Coue and Malledant162,Reference Faruqi, Medefindt, Dutta, Philip, Tompkins and Carey163

  6. 6. Routine replacement of administration sets not used for blood, blood products, or lipid formulations can be performed at intervals up to 7 days (Quality of Evidence: HIGH) Reference Rickard, Marsh and Larsen164

    1. a. The optimal replacement of intermittently used administration sets is unresolved.

  7. 7. Perform surveillance for CLABSI in ICU and non-ICU settings (Quality of Evidence: HIGH) Reference Marschall, Leone, Jones, Nihill, Fraser and Warren13,Reference Gastmeier, Geffers and Brandt165,Reference Zingg, Sax and Inan166

    1. a. Measure unit-specific incidence of CLABSI (eg, CLABSI per 1,000 catheter days) and report the data on a regular basis to the units, physician and nursing leadership, and hospital administrators overseeing the units.

    2. b. Compare CLABSI incidence to historical data for individual units and to national rates (ie, NHSN). Reference Sunkesula, Kundrapu, Knighton, Cadnum and Donskey167

    3. c. Audit surveillance as necessary to minimize variation in interobserver reliability. Reference Niedner48,Reference Lin, Hota and Khan168

Additional approaches for preventing CLABSI

Several additional approaches are currently available for use. Perform a CLABSI risk assessment before considering implementation of any of these approaches, taking potential adverse events and costs into consideration. Although it is reasonable to evaluate the utility of technology-based interventions when CLABSI rates are above the institutional- or unit-based threshold, this is also an opportunity to review practices and consider behavioral changes that may be instituted to reduce CLABSI risk. These additional approaches are recommended for use in locations and/or populations within the hospital with unacceptably high CLABSI rates despite implementation of the essential CLABSI prevention strategies listed above. These measures may not be indicated if institutional goals have been consistently achieved.

  1. 1. Use antiseptic- or antimicrobial-impregnated CVCs (Quality of Evidence: HIGH in adult patients Reference Raad, Darouiche and Dupuis38,Reference Hanna, Benjamin and Chatzinikolaou39,Reference Wang, Tong and Liu169Reference Novikov, Lam, Mermel, Casey, Elliott and Nightingale171 and MODERATE in pediatric patients Reference Gilbert, Mok and Dwan172,Reference Lai and Yue173 )

    1. a. The risk of CLABSI is reduced with some currently marketed antiseptic-impregnated (eg, chlorhexidine-silver sulfadiazine) catheters and antimicrobial-impregnated (eg, minocycline-rifampin) catheters. Use such catheters under the following conditions:

      1. i. Hospital units or patient populations have a CLABSI rate above institutional goals despite compliance with essential CLABSI prevention practices. Some evidence suggests that use of antimicrobial CVCs, along with other preventive technologies, may have no additional benefit in patient care units that have already established a low incidence of catheter infections. Reference Cherry-Bukowiec, Denchev and Dickinson174,Reference Ullman, Paterson and Schults175

      2. ii. Patients have limited venous access and a history of recurrent CLABSI.

      3. iii. Patients are at heightened risk of severe sequelae from a CLABSI (eg, patients with recently implanted intravascular devices such as a prosthetic heart valve or aortic graft).

    2. b. Monitor patients for adverse effects such as anaphylaxis. Reference Guleri, Kumar, Morgan, Hartley and Roberts176

    3. c. Many studies investigating antimicrobial-impregnated catheters were performed before infection preventive bundles were routine. Whether such catheters have an impact on CLABSI in such settings remains unknown.

  2. 2. Use antimicrobial lock therapy for long-term CVCs (Quality of Evidence: HIGH)Reference Carratala, Niubo and Fernandez-Sevilla177Reference Sheng, Zhang and Li184

    1. a. Antibiotic and antiseptic locks are created by filling the lumen of the catheter with a supratherapeutic concentration of an antibiotic solution and leaving the solution in place until the catheter hub is re-accessed. Such an approach can reduce the risk of CLABSI. The optimal antimicrobial agent or combination of agents, their concentration, and duration of lock therapy are matters of ongoing research. Due to concerns regarding the potential for the emergence of resistance in exposed organisms, use antimicrobial locks as a preventative strategy for the following:

      1. i. Patients with long-term hemodialysis catheters who have a history of recurrent CLABSI. Reference Arechabala, Catoni and Claro185

      2. ii. Prophylaxis for patients with limited venous access and a history of recurrent CLABSI.

      3. iii. Patients who are at heightened risk of severe sequelae from a CLABSI (eg, patients with recently implanted intravascular devices such as a prosthetic heart valve or aortic graft).

    2. b. To minimize systemic toxicity, aspirate rather than flush the antimicrobial lock solution after the dwell time has elapsed. Reference Opilla, Kirby and Edmond186Reference Heng, Abdelkader and Diaconita189 The potential of adverse effects associated with ethanol locks should be carefully considered before use. Reference Mermel and Alang190,Reference Wolf, Connell and Allison191

  3. 3. Use recombinant tissue plasminogen activating factor (rt-PA) once weekly after hemodialysis in patients undergoing hemodialysis through a CVC (Quality of Evidence: HIGH) Reference Hemmelgarn, Moist and Lok192

  4. 4. Utilize infusion or vascular access teams for reducing CLABSI rates (Quality of Evidence: LOW) Reference Miller, Goetz, Squier and Muder193,Reference Taylor, Massaro and Williams194

    1. a. Studies have shown that an infusion/vascular access team responsible for insertion and maintenance of peripheral intravenous catheters reduces the risk of bloodstream infections Reference Soifer, Borzak, Edlin and Weinstein195 ; however, few studies have been performed regarding the impact of intravenous therapy teams on CLABSI rates. Reference Carr, Higgins, Cooke, Mihala and Rickard196

  5. 5. Use antimicrobial ointments for hemodialysis catheter insertion sites (Quality of Evidence: HIGH) Reference Levin, Mason, Jindal, Fong and Goldstein197Reference James, Conley, Tonelli, Manns, MacRae and Hemmelgarn201

    1. a. Apply polysporin “triple” (where available) or povidone-iodine ointment to hemodialysis catheter insertion if compatible with the catheter material.

    2. b. Ingredients in ointments may interact with the chemical composition of some catheters. Thus, ensure the selected ointment will not interact with the catheter material before any such product is applied to the catheter insertion/exit site. For example, ointments containing glycol should not be applied to insertion/exit sites of polyurethane catheters.

    3. c. Mupirocin ointment should not be applied to the catheter insertion site due to the risks of facilitating mupirocin resistance and the potential damage to polyurethane catheters.

  6. 6. Use an antiseptic-containing hub/connector cap/port protector to cover connectors (Quality of Evidence: MODERATE) Reference Oto, Imanaka, Konno, Nakataki and Nishimura202Reference Flynn, Larsen, Keogh, Ullman and Rickard208

    1. a. The utility of routinely disinfecting hub connectors and ports when using antiseptic-containing hub/connector cap/port protectors is unknown.

Approaches that should not be considered a routine part of CLABSI prevention

  1. 1. Do not use antimicrobial prophylaxis for short-term or tunneled catheter insertion or while catheters are in situ (Quality of Evidence: HIGH) Reference McKee, Dunsmuir, Whitby and Garden209Reference van de Wetering, van Woensel and Lawrie213

    1. a. Systemic antimicrobial prophylaxis is not recommended.

  2. 2. Do not routinely replace CVCs or arterial catheters (Quality of Evidence: HIGH) Reference Cook, Randolph and Kernerman214

    1. a. Routine catheter replacement is not recommended.

Unresolved issues

  1. 1. Routine use of needleless connectors as a CLABSI prevention strategy before an assessment of risks, benefits, and education regarding proper use Reference Maragakis, Bradley and Song215Reference Jarvis, Murphy and Hall219

    1. a. Multiple devices are currently available but the optimal design for preventing infections is unresolved. The original purpose of needleless connectors was to prevent needlestick injuries during intermittent use. No data are available regarding their use with continuous infusions. Needle-free connectors with 3-way stopcocks may increase the risk of catheter infections. Reference Rosenthal220

      1. i. Use of silver-coated catheter connectors may be associated with reduced intraluminal contamination in ex vivo catheters and CLABSI. Reference Casey, Karpanen, Nightingale, Cook and Elliott221,Reference Jacob, Chernetsky Tejedor and Dent Reyes222 Clinical evidence is limited regarding the risk reduction with their routine use or use of other antimicrobial catheter connectors.

  2. 2. Surveillance of other types of catheters (eg, peripheral arterial or venous catheters) Reference Maki, Kluger and Crnich11,Reference Mermel21,Reference O’Horo, Maki, Krupp and Safdar22

    1. a. Peripheral arterial catheters, short-term peripheral venous catheters and midline catheters are not included in most surveillance systems although they are associated with risk of bloodstream infection. Future surveillance systems should consider including bloodstream infections associated with these types of catheters.

    2. b. If considering further infection prevention interventions due to concern for an increase in infections, hospitals may want to consider extending their surveillance programs to include all types of catheters used to gauge the size of the problem.

  3. 3. Standard, nonantimicrobial transparent dressings and CLABSI risk

    1. a. A meta-analysis reported an association between CLABSI and transparent dressing use; however, the source studies for the meta-analysis reporting this association were of low quality. Reference Webster, Gillies, O’Riordan, Sherriff and Rickard223

  4. 4. The impact of using chlorhexidine-based products on bacterial resistance to chlorhexidine

    1. a. Widespread use of chlorhexidine-based products (eg, use of chlorhexidine bathing, antisepsis, and dressings) may promote reduced chlorhexidine susceptibility. Reference Batra, Cooper, Whiteley, Patel, Wyncoll and Edgeworth224 However, testing for chlorhexidine susceptibility is not standardized. The clinical impact of reduced chlorhexidine susceptibility is unknown.

  5. 5. Sutureless securement

    1. a. The impact of sutureless securement devices in reducing CLABSI is unknown. Reference Rickard, Edwards and Spooner225,Reference Karpanen, Casey and Whitehouse226

  6. 6. Impact of silver zeolite-impregnated umbilical catheters in preterm infants (applicable in countries where it is approved for use in children) Reference Bertini, Elia, Ceciarini and Dani227

    1. a. One randomized study suggests that antimicrobial-impregnated umbilical catheters appear to be safe and effective in NICU patients. Reference Bertini, Elia, Ceciarini and Dani228

  7. 7. Necessity of mechanical disinfection of a catheter hub, needleless connector, and injection port before accessing the catheter when antiseptic-containing caps are being used.

    1. a. It is unknown whether the application and removal of an antiseptic-containing cap provides the same benefit to reducing risk of CLABSI as manual disinfection. Future research is needed to determine if using such a cap will obviate the need for manual disinfection before accessing a catheter.

Section 5: Performance measures

Internal reporting

These performance measures are intended to support internal hospital quality improvement efforts Reference Bizzarro, Sabo and Noonan229,Reference Sawyer, Weeks and Goeschel230 and do not necessarily address external reporting needs.

The process and outcome measures suggested here are derived from published guidelines, other relevant literature, and the opinion of the authors. Report process and outcome measures to senior hospital leadership, nursing leadership, and clinicians who care for patients at risk for CLABSI.

Process measures (Table 3)

  1. 1. Compliance with CVC insertion guidelines as documented on an insertion checklist

    1. a. Assess compliance with the checklist in all hospital settings where CVCs are inserted (eg, ICUs, ED, OR, radiology, general patient care units) and assign HCP familiar with CVCs to this task.

    2. b. Documenting compliance using the insertion checklist upholds accountability and compliance with the proper procedure steps and identifies gaps to be mitigated. The Institute for Healthcare Improvement (IHI) provides an example of a central catheter checklist. 231

    3. c. Documentation of CVC insertion procedures in compliance with appropriate hand hygiene, use of maximal sterile barrier precautions, and use of chlorhexidine-based cutaneous antisepsis of the insertion site:

      1. i. Numerator: Number of CVC insertions that have documented the use of all 3 interventions (hand hygiene, maximal barrier precautions, and chlorhexidine-based cutaneous antiseptic use) performed at the time of CVC insertion.

      2. ii. Denominator: Number of all CVC insertions.

      3. iii. Multiply by 100 so that the measure is expressed as a percentage.

  2. 2. Compliance with documentation of daily assessment regarding the need for continuing CVC access.

    1. a. Measure the percentage of patients with a CVC where there is documentation of daily assessment:

      1. i. Numerator: Number of patients with a CVC who have documentation of daily assessment.

      2. ii. Denominator: Number of patients with a CVC.

      3. iii. Multiply by 100 so that the measure is expressed as a percentage.

  3. 3. Simulation of catheter maintenance as an alternative to address HCP competency Reference Fakih, Jones and Rey232,Reference Fakih, Jones and Rey233

    1. i. Numerator: Number of HCP properly simulating the aseptic infusion of medications.

    2. ii. Denominator: Number of HCP simulating the aseptic infusion of medications.

    3. iii. Multiply by 100 so that the measure is expressed as a percentage.

  4. 4. Device utilization can be evaluated over time to assess any changes. Utilization may be compared at the hospital and unit level. It provides a surrogate for patient exposure risk. Reference Fakih, Gould and Trautner234 The standardized utilization ratio (SUR) is an NHSN measure that accounts for facility- and location-level factors that may affect device use.

    1. i. SUR: Observed device days divided by predicted device days.

Table 3. CLABSI Prevention Process Measures

Outcome measures (See Table 4)

  1. 1. CLABSI rate: Use NHSN definitions.

    1. a. Numerator: Number of CLABSIs in each unit assessed (using NHSN definitions).

    2. b. Denominator: Total number of catheter days in each unit assessed (using NHSN definitions).

    3. c. Multiply by 1,000 so that the measure is expressed as number of CLABSIs per 1,000 catheter days.

  2. 2. Risk adjustment: Stratify CLABSI rates by type of patient-care unit. Reference Widmer, Nettleman, Flint and Wenzel235Reference Pittet and Wenzel237

    1. a. Report comparisons based on historic data and NHSN data, if available. Reference Sunkesula, Kundrapu, Knighton, Cadnum and Donskey167

    2. b. Use the NHSN device standardized infection ratio (dSIR) to evaluate hospital and unit CLABSI rates.

      1. i. dSIR: Observed CLABSI events divided by predicted CLABSI events based on actual device days.

    3. c. Consider measures that address device risk at the patient population level. A population SIR (pSIR) Reference Fakih, Huang and Bufalino238 accounts for both device SIR and SUR, reflecting both the care of the device, and interventions to reduce utilization.

      1. i. pSIR: Observed CLABSI events divided by predicted CLABSI events based on predicted device days.

Table 4. CLABSI Prevention Outcome Measures

External reporting

Many challenges exist in providing useful information to consumers and other stakeholders and in preventing unintended consequences of public reporting of HAIs. Reference Wong, Rupp and Mermel239,Reference Aswani, Reagan, Jin, Pronovost and Goeschel240 Recommendations for public reporting of HAIs have been provided by the Healthcare Infection Control Practices Advisory Committee (HICPAC), Reference Talbot, Bratzler and Carrico241 the Healthcare-Associated Infection Working Group of the Joint Public Policy Committee, Reference Evans, Kralovic, Simbartl, Jain and Roselle242 and the National Quality Forum. Reference Hamill, Reed and Fogel243

State and federal requirements

  1. 1. Hospitals in states that have mandatory reporting requirements for CLABSI must collect and report the data required by the state.

  2. 2. For information on state and federal requirements, contact your state or local health department.

External quality initiatives

  1. 1. Hospitals that participate in external quality initiatives or state programs must collect and report the data required by the initiative or the program.

  2. 2. Problems with interrater reliability may affect comparisons between different institutions.

Section 6: Implementation of CLABSI prevention strategies

Prevention of CLABSI depends on integrating best practices to reduce the risk of infection and incorporating a culture to support implementation. Hospitals should address technical and socioadaptive components Reference Chopra, Flanders and Saint244 to CLABSI prevention, including formal training of HCP on indications, placement, and maintenance of devices, in addition to regular assessment of competencies. Reference Fakih, Heavens, Ratcliffe and Hendrich245

One example of a widely used model in the United States, known as the Four Es (ie, engage, educate, execute, and evaluate Reference Owings, Graves, Johnson, Gilliam, Gipson and Hakim246 ), involves summarizing evidence, identifying local barriers to implementation, measuring performance, and ensuring that patients receive the infection prevention intervention Reference Pronovost, Berenholtz and Needham247 by addressing knowledge, critical thinking, behavior and psychomotor skills, as well as attitudes and beliefs of all members of the healthcare team involved with the insertion and care of CVCs. Reference Safdar and Abad248,Reference Smith, Kirksey, Becker and Brown249 Facilities may consider utilizing tools to promote high-reliability processes (eg, Lean Six Sigma) and to enhance teamwork (eg, Team STEPPS).

Engage

Historically, efforts have been centered around having a champion to support CLABSI reduction initiatives. Champions are often very effective in initial phases of adoption, but their efforts may not be enough for integration of processes and sustainability. Reference Hendy and Barlow250 It is important to engage both frontline and senior leadership champions in the process and outcome improvement plan, Reference Weaver, Lubomksi, Wilson, Pfoh, Martinez and Dy251 but institutionalizing the work and garnering the support of stakeholder groups facilitates successful, long-lasting results. Reference Fakih, Krein, Edson, Watson, Battles and Saint252

Educate

HCP, patients, and caregivers involved in care of a CVC should be trained in and competent, relative to their role, with the following:

  1. 1. Appropriate indications prior to insertion.

  2. 2. Use of full barrier precautions at the time of insertion.

  3. 3. Daily evaluation of necessity of the device.

Execute

A standardized competency assessment checklist should be used to assess and document competency of each individual performing CVC insertion and procedures related to care and maintenance (eg, dressing changes). Reference Wathen, Kshettry and Krishnaney253Reference Evans and Dodge255 In addition, education of the patient and/or family, as appropriate, is required for all CVC care procedures especially when transfer to an alternative setting (eg, home care, ambulatory setting) is planned. Reference Segreti, Garcia-Houchins and Gorski256,Reference Nailon, Rupp and Lyden257

Evaluate

Evaluation involves both process and outcome measurement. Reference Wheeler, Giaccone and Hutchinson258 Multidisciplinary teams should set clear goals and identify the key factors to be measured. It is important for members of the healthcare team to receive feedback on their performance. Feedback should include periodic (eg, monthly, quarterly) communication (eg, e-mail messages, written reports) of process measurement data via posters, reports, or other forms of communication with graphs showing cumulative compliance with process measures. Reference Marra, Cal and Durao259Reference Assanasen, Edmond and Bearman262 Differences between age groups should also be considered (eg, neonates, pediatrics, and adults). Reference Powers and Wirtschafter260,Reference Miller, Griswold and Harris263,Reference Stevens and Schulman264 Central line data can be used to capture trends over time. The standardized utilization ratio (SUR) provides a method for the hospital’s units to compare themselves to others with similar characteristics. CLABSI events are important to discuss with the different members of the team caring for the patient to have a clear understanding of gaps and ways to mitigate them in the future.

Acknowledgments

We appreciate Sarah Rolli, Bern University Hospital, for her help with document editing and formatting.

Disclaimer

The findings and conclusions in this report are those of the author and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Conflicts of interest

The following disclosures reflect what has been reported to SHEA. To provide thorough transparency, SHEA requires full disclosure of all relationships, regardless of relevancy to the topic. Such relationships as potential conflicts of interest are evaluated in a review process that includes assessment by the SHEA Conflict of Interest Committee and may include the Board of Trustees and Editor of Infection Control and Hospital Epidemiology. The assessment of disclosed relationships for possible conflicts of interest has been based on the relative weight of the financial relationship (ie, monetary amount) and the relevance of the relationship (ie, the degree to which an association might reasonably be interpreted by an independent observer as related to the topic or recommendation of consideration).

N.B. received a Mobility grant from the Swiss National Science Foundation (grant nos. P400PM_183865 and P4P4PM_194449) and a grant from the Bangerter-Rhyner Foundation. J.M. is the recipient of a project grant on surgical site infections from the Swiss National Science Foundation (grant no. 32003B_179500, “Understanding the drivers of surgical site infection: Investigating and modeling the Swissnoso surveillance data”). L.M. served as an advisor/consultant for Marvao Medical Devices. L.H. served as an advisor/consultant for B Braun Medical, BD Medical, Atrion Medical, Nexus Medical, Teleflex. M.E.R. served as an advisor/consultant for 3M, Becton Dickinson, and Cetius, and Teleflex, and received honoraria from Teleflex. All other authors report no conflicts of interest related to this article.

Footnotes

a

Authors of equal contribution.

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