Acquisition of Antibiotic-Resistant Gram-negative Bacteria in the Benefits of Universal Glove and Gown (BUGG) Cluster Randomized Trial

Anthony D Harris, Daniel J Morgan, Lisa Pineles, Larry Magder, Lyndsay M O'Hara, J Kristie Johnson, Anthony D Harris, Daniel J Morgan, Lisa Pineles, Larry Magder, Lyndsay M O'Hara, J Kristie Johnson

Abstract

Background: The Benefits of Universal Glove and Gown (BUGG) cluster randomized trial found varying effects on methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus and no increase in adverse events. The aim of this study was to assess whether the intervention decreases the acquisition of antibiotic-resistant gram-negative bacteria.

Methods: This was a secondary analysis of a randomized trial in 20 hospital intensive care units. The intervention consisted of healthcare workers wearing gloves and gowns when entering any patient room compared to standard care. The primary composite outcome was acquisition of any antibiotic-resistant gram-negative bacteria based on surveillance cultures.

Results: A total of 40 492 admission and discharge perianal swabs from 20 246 individual patient admissions were included in the primary outcome. For the primary outcome of acquisition of any antibiotic-resistant gram-negative bacteria, the intervention had a rate ratio (RR) of 0.90 (95% confidence interval [CI], .71-1.12; P = .34). Effects on the secondary outcomes of individual bacteria acquisition were as follows: carbapenem-resistant Enterobacteriaceae (RR, 0.86 [95% CI, .60-1.24; P = .43), carbapenem-resistant Acinetobacter (RR, 0.81 [95% CI, .52-1.27; P = .36), carbapenem-resistant Pseudomonas (RR, 0.88 [95% CI, .55-1.42]; P = .62), and extended-spectrum β-lactamase-producing bacteria (RR, 0.94 [95% CI, .71-1.24]; P = .67).

Conclusions: Universal glove and gown use in the intensive care unit was associated with a non-statistically significant decrease in acquisition of antibiotic-resistant gram-negative bacteria. Individual hospitals should consider the intervention based on the importance of these organisms at their hospital, effect sizes, CIs, and cost of instituting the intervention.

Clinical trials registration: NCT01318213.

Keywords: antibiotic resistance; barrier precautions; contact precautions.

© The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America.

Figures

Figure 1.
Figure 1.
Rate differences (per 1000 person-days) and 95% confidence intervals for the impact of universal glove and gown use, by organism. The rate difference provides a measure of the public health impact of the intervention and describes the number of cases that could be prevented. Abbreviations: ESBL, extended-spectrum β-lactamase.
Figure 2.
Figure 2.
Admission positivity rate per organism, by month. Abbreviations: CRE, carbapenemase-resistant Enterobacteriaceae; ESBL, extended-spectrum β-lactamase.

References

    1. Zimlichman E, Henderson D, Tamir O, et al. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA Intern Med 2013; 173:2039–46.
    1. Talbot GH, Bradley J, Edwards JE Jr, Gilbert D, Scheld M, Bartlett JG; Antimicrobial Availability Task Force of the Infectious Diseases Society of America Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America. Clin Infect Dis 2006; 42:657–68.
    1. Klevens RM, Edwards JR, Richards CL Jr, et al. Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep 2007; 122:160–6.
    1. Weiner LM, Webb AK, Limbago B, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2011–2014. Infect Control Hosp Epidemiol 2016; 37:1288–301.
    1. World Health Organization. WHO publishes list of bacteria for which new antibiotics are urgently needed Available at: . Accessed 19 March 2019.
    1. Morgan DJ, Murthy R, Munoz-Price LS, et al. Reconsidering contact precautions for endemic methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococcus (VRE). Infect Control Hosp Epidemiol 36:1163–72.
    1. Rubin MA, Samore MH, Harris AD. The importance of contact precautions for endemic methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci. JAMA 2018; 319:863–4.
    1. Harris AD, Pineles L, Belton B, et al. ; Benefits of Universal Glove and Gown (BUGG) Investigators Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial. JAMA 2013; 310:1571–80.
    1. Centers for Disease Control and Prevention. The biggest antibiotic-resistant threats in the U.S. 2019 Available at: . Accessed 7 August 2019.
    1. Yokoe DS, Anderson DJ, Berenholtz SM, et al. Society for Healthcare Epidemiology of America (SHEA) A compendium of strategies to prevent healthcare-associated infections in acute care hospitals: 2014 updates. Infect Control Hosp Epidemiol 2014; 35:967–77.
    1. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Health Care Infection Control Practices Advisory Committee 2007 guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007; 35:S65–164.
    1. Campbell MK, Piaggio G, Elbourne DR, Altman DG, CONSORT Group Consort 2010 statement: extension to cluster randomised trials. BMJ 2012; 345:e5661.
    1. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Healthcare Infection Control Practices Advisory Committee Management of multidrug-resistant organisms in health care settings, 2006. Am J Infect Control 2007; 35:S165–93.
    1. Morgan DJ, Pineles L, Shardell M, et al. BUGG Study Primary Investigators Effect of chlorhexidine bathing and other infection control practices on the Benefits of Universal Glove and Gown (BUGG) trial: a subgroup analysis. Infect Control Hosp Epidemiol 2015; 36:734–7.
    1. Green HP, Johnson JA, Furuno JP, et al. Impact of freezing on the future utility of archived surveillance culture specimens. Infect Control Hosp Epidemiol 2007; 28:886–8.
    1. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011; 70:119–23.
    1. Centers for Disease Control and Prevention. Multiplex real-time PCR detection of Klebsiella pneumoniae carbapenemase (KPC) and New Delhi metallo-β-lactamase (NDM-1) genes Available at: . Accessed 15 March 2019.
    1. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 26th informational supplement. CLSI document M100-S26. Wayne, PA: CLSI, 2016.
    1. R-GNOSIS. Main findings and results Available at: . Accessed 7 August 2019.
    1. Harris AD, Johnson JK, Pineles L, O’Hara LM, Bonomo RA, Thom KA. Patient-to-patient transmission of Acinetobacter baumannii gastrointestinal colonization in the intensive care unit. Antimicrob Agents Chemother 2019; 63. doi:10.1128/AAC.00392-19.
    1. Munoz-Price LS, Namias N, Cleary T, et al. Acinetobacter baumannii: association between environmental contamination of patient rooms and occupant status. Infect Control Hosp Epidemiol 2013; 34:517–20.
    1. Thom KA, Johnson JK, Lee MS, Harris AD. Environmental contamination because of multidrug-resistant Acinetobacter baumannii surrounding colonized or infected patients. Am J Infect Control 2011; 39:711–5.
    1. Rosa R, Arheart KL, Depascale D, et al. Environmental exposure to carbapenem-resistant Acinetobacter baumannii as a risk factor for patient acquisition of A. baumannii. Infect Control Hosp Epidemiol 2014; 35:430–3.
    1. Wasserstein RL, Lazar NA. The ASA statement on P-values: context, process, and purpose. Am Stat2016; 70: 129.–. Available at: . Accessed 7 August 2019.
    1. Wasserstein RL, Schirm AL, Lazar NA. Moving to a world beyond “p < 0.05.” Am Stat2019. Available at: . Accessed 7 August 2019.
    1. Harrington D, D’Agostino RB Sr, Gatsonis C, et al. New guidelines for statistical reporting in the journal. N Engl J Med 2019; 381:285–6.
    1. Goodman SN, Berlin JA. The use of predicted confidence intervals when planning experiments and the misuse of power when interpreting results. Ann Intern Med 1994; 121:200–6.
    1. Harris AD, Nemoy L, Johnson JA, et al. Co-carriage rates of vancomycin-resistant Enterococcus and extended-spectrum beta-lactamase-producing bacteria among a cohort of intensive care unit patients: implications for an active surveillance program. Infect Control Hosp Epidemiol 2004; 25:105–8.
    1. Harris AD, Furuno JP, Roghmann MC, et al. Targeted surveillance of methicillin-resistant Staphylococcus aureus and its potential use to guide empiric antibiotic therapy. Antimicrob Agents Chemother 2010:3143–8.
    1. Harris AD, Jackson SS, Robinson G, et al. Pseudomonas aeruginosa colonization in the intensive care unit: prevalence, risk factors, and clinical outcomes. Infect Control Hosp Epidemiol 2016; 37:544–8.
    1. Blanco N, Harris AD, Rock C, et al. Risk factors and outcomes associated with multidrug-resistant Acinetobacter baumannii upon intensive care unit admission. Antimicrob Agents Chemother 2017; 62. doi:10.1128/AAC.01631-17.
    1. Borer A, Saidel-Odes L, Eskira S, et al. Risk factors for developing clinical infection with carbapenem-resistant Klebsiella pneumoniae in hospital patients initially only colonized with carbapenem-resistant K pneumoniae. Am J Infect Control 2012; 40:421–5.
    1. Schechner V, Kotlovsky T, Kazma M, et al. Asymptomatic rectal carriage of blaKPC producing carbapenem-resistant Enterobacteriaceae: who is prone to become clinically infected? Clin Microbiol Infect 2013; 19:451–6.
    1. Emmanuel Martinez A, Widmer A, Frei R, et al. ESBL-colonization at ICU admission: impact on subsequent infection, carbapenem-consumption, and outcome. Infect Control Hosp Epidemiol 2019; 40:408–13.
    1. Mauldin PD, Salgado CD, Hansen IS, Durup DT, Bosso JA. Attributable hospital cost and length of stay associated with health care-associated infections caused by antibiotic-resistant gram-negative bacteria. Antimicrob Agents Chemother 2010; 54:109–15.
    1. Nelson RE, Jones M, Liu CF, et al. The impact of healthcare-associated methicillin-resistant Staphylococcus aureus infections on post-discharge healthcare costs and utilization. Infect Control Hosp Epidemiol 2015; 36:534–42.
    1. Derde LPG, Cooper BS, Goossens H, et al. MOSAR WP3 Study Team Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial. Lancet Infect Dis 2014; 14:31–9.
    1. MacFadden DR, McGough SF, Fisman D, Santillana M, Brownstein JS. Antibiotic resistance increases with local temperature. Nat Clim Chang 2018; 8:510–4.
    1. Fisman DN Seasonality of infectious diseases. Annu Rev Public Health 2007; 28:127–43.
    1. Perencevich EN, McGregor JC, Shardell M, et al. Summer peaks in the incidences of gram-negative bacterial infection among hospitalized patients. Infect Control Hosp Epidemiol 2008; 29:1124–31.
    1. Bonten MJM Colonization pressure: a critical parameter in the epidemiology of antibiotic-resistant bacteria. Crit Care 2012; 16:142.
    1. Arvaniti K, Lathyris D, Ruimy R, et al. The importance of colonization pressure in multiresistant Acinetobacter baumannii acquisition in a Greek intensive care unit. Crit Care 2012; 16:R102.
    1. Ajao AO, Harris AD, Roghmann MC, et al. Systematic review of measurement and adjustment for colonization pressure in studies of methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and clostridium difficile acquisition. Infect Control Hosp Epidemiol 2011; 32:481–9.
    1. Feng PJ, Kallen AJ, Ellingson K, Muder R, Jain R, Jernigan JA. Clinical incidence of methicillin-resistant Staphylococcus aureus (MRSA) colonization or infection as a proxy measure for MRSA transmission in acute care hospitals. Infect Control Hosp Epidemiol 2011; 32:20–5.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться