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Transmission pathways of multidrug-resistant organisms in the hospital setting: a scoping review

Published online by Cambridge University Press:  06 March 2019

Natalia Blanco
Affiliation:
Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, Maryland
Lyndsay M. O’Hara
Affiliation:
Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, Maryland
Anthony D. Harris*
Affiliation:
Department of Epidemiology and Public Health, University of Maryland School of Medicine, Baltimore, Maryland
*
Author for correspondence: Anthony D. Harris, Email: [email protected]

Abstract

Background:

Prevalence of multidrug-resistant microorganisms (MDROs) continues to increase, while infection control gaps in healthcare settings facilitate their transmission between patients. In this setting, 5 distinct yet interlinked pathways are responsible for transmission. The complete transmission process is still not well understood. Designing and conducting a single research study capable of investigating all 5 complex and multifaceted pathways of hospital transmission would be costly and logistically burdensome. Therefore, this scoping review aims to synthesize the highest-quality published literature describing each of the 5 individual potential transmission pathways of MDROs in the healthcare setting and their overall contribution to patient-to-patient transmission.

Methods:

In 3 databases, we performed 2 separate systematic searches for original research published during the last decade. The first search focused on MDRO transmission via the HCW or the environment to identify publications studying 5 specific transmission pathways: (1) patient to HCW, (2) patient to environment, (3) HCW to patient, (4) environment to patient, and (5) environment to HCW. The second search focused on overall patient-to-patient transmission regardless of the transmission pathway. Both searches were limited to transmission of methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus, multidrug-resistant A. baumannii, and carbapenem-resistant Enterobacteriaceae. After abstract screening of 5,026 manuscripts, researchers independently reviewed and rated the remaining papers using objective predefined criteria to identify the highest quality and most influential manuscripts.

Results:

High-quality manuscripts were identified for all 5 routes of transmission. Findings from these studies were consistent for all pathways; however, results describing the routes from the environment/HCW to a noncolonized patient were more limited and variable. Additionally, most research focused on MRSA, instead of other MDROs. The second search yielded 10 manuscripts (8 cohort studies) that demonstrated the overall contribution of patient-to-patient transmission in hospitals regardless of the transmission route. For MRSA, the reported cross-transmission was as high as 40%.

Conclusions:

This scoping review brings together evidence supporting all 5 possible transmission pathways and illustrates the complex nature of patient-to-patient transmission of MDROs in hospitals. Our findings also confirm that transmission of MDROs in hospitals occurs frequently, suggesting that ongoing efforts are necessary to strengthen infection prevention and control to prevent the spread of MDROs.

Type
Review
Copyright
© 2019 by The Society for Healthcare Epidemiology of America. All rights reserved. 

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References

Blanco, N, Perencevich, E, Li, SS, et al. Effect of meteorological factors and geographic location on methicillin-resistant staphylococcus aureus and vancomycin-resistant Enterococci colonization in the US. PLoS One 2017;12:e0178254.CrossRefGoogle ScholarPubMed
Corbella, X, Pujol, M, Ayats, J, et al. Relevance of digestive tract colonization in the epidemiology of nosocomial infections due to multiresistant Acinetobacter baumannii. Clin Infect Dis 1996;23:329334.CrossRefGoogle ScholarPubMed
Bratu, S, Landman, D, Haag, R, et al. Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: a new threat to our antibiotic armamentarium. Arch Intern Med 2005;165:14301435.CrossRefGoogle ScholarPubMed
Harris, AD, Pineles, L, Belton, B, et al. Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial. JAMA 2013;310:15711580.Google ScholarPubMed
Causes of antimicrobial (drug) resistance. National Institutes of Allergy and Infectious Diseases website. https://www.niaid.nih.gov/research/antimicrobial-resistance-causes. Published December 21, 2011. Accessed September 21, 2018.Google Scholar
Visalachy, S, Palraj, KK, Kopula, SS, Sekar, U. Carriage of multidrug resistant bacteria on frequently contacted surfaces and hands of health care workers. J Clin Diagn Res 2016;10:DC18DC20.Google ScholarPubMed
Eveillard, M, Martin, Y, Hidri, N, Boussougant, Y, Joly-Guillou, ML. Carriage of methicillin-resistant Staphylococcus aureus among hospital employees: prevalence, duration, and transmission to households. Infect Control Hosp Epidemiol 2004;25:114120.CrossRefGoogle ScholarPubMed
Morgan, DJ, Rogawski, E, Thom, KA, et al. Transfer of multidrug-resistant bacteria to healthcare workers’ gloves and gowns after patient contact increases with environmental contamination. Crit Care Med 2012;40:10451051.CrossRefGoogle ScholarPubMed
Morgan, DJ, Liang, SY, Smith, CL, et al. Frequent multidrug-resistant Acinetobacter baumannii contamination of gloves, gowns, and hands of healthcare workers. Infect Control Hosp Epidemiol 2010;31:716721.CrossRefGoogle ScholarPubMed
Duckro, AN, Blom, DW, Lyle, EA, Weinstein, RA, Hayden, MK. Transfer of vancomycin-resistant Enterococci via health care worker hands. Arch Intern Med 2005;165:302307.CrossRefGoogle ScholarPubMed
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;34:517520.CrossRefGoogle ScholarPubMed
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;39:711715.CrossRefGoogle ScholarPubMed
Mitchell, A, Spencer, M, Edmiston, C Jr. Role of healthcare apparel and other healthcare textiles in the transmission of pathogens: a review of the literature. J Hosp Infect 2015;90:285292.CrossRefGoogle ScholarPubMed
Pham, MT, Rajić, A, Greig, JD, Sargeant, JM, Papadopoulos, A, McEwen, SA. A scoping review of scoping reviews: advancing the approach and enhancing the consistency. Res Synth Methods 2014;5:371385.CrossRefGoogle ScholarPubMed
Colquhoun, HL, Levac, D, O’Brien, KK, et al. Scoping reviews: time for clarity in definition, methods, and reporting. J Clin Epidemiol 2014;67:12911294.CrossRefGoogle ScholarPubMed
Hayden, MK, Blom, DW, Lyle, EA, Moore, CG, Weinstein, RA. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant Enterococcus or the colonized patients’ environment. Infect Control Hosp Epidemiol 2008;29:149154.CrossRefGoogle ScholarPubMed
Schweizer, M, Ward, M, Cobb, S, et al. The epidemiology of methicillin-resistant Staphylococcus aureus on a burn trauma unit. Infect Control Hosp Epidemiol 2012;33:11181125.CrossRefGoogle ScholarPubMed
Yakupogullari, Y, Otlu, B, Ersoy, Y, et al. Is airborne transmission of Acinetobacter baumannii possible: a prospective molecular epidemiologic study in a tertiary care hospital. Am J Infect Control 2016;44:15951599.CrossRefGoogle Scholar
Wilson, AP, Hayman, S, Whitehouse, T, et al. Importance of the environment for patient acquisition of methicillin-resistant staphylococcus aureus in the intensive care unit: a baseline study. Crit Care Med 2007;35:22752279.CrossRefGoogle ScholarPubMed
Ben-David, D, Mermel, LA, Parenteau, S. Methicillin-resistant Staphylococcus aureus transmission: the possible importance of unrecognized health care worker carriage. Am J Infect Control 2008;36:9397.CrossRefGoogle ScholarPubMed
Loftus, RW, Koff, MD, Brown, JR, et al. The epidemiology of Staphylococcus aureus transmission in the anesthesia work area. Anesth Analg 2015;120:807818.CrossRefGoogle ScholarPubMed
Creamer, E, Shore, AC, Rossney, AS, et al. Transmission of endemic ST22-MRSA-IV on four acute hospital wards investigated using a combination of spa, dru and pulsed-field gel electrophoresis typing. Eur J Clin Microbiol Infect Dis 2012;31:31513161.CrossRefGoogle ScholarPubMed
Barbolla, RE, Centron, D, Maimone, S, et al. Molecular epidemiology of Acinetobacter baumannii spread in an adult intensive care unit under an endemic setting. Am J Infect Control 2008;36:444452.CrossRefGoogle Scholar
Danzmann, L, Gastmeier, P, Schwab, F, Vonberg, RP. Health care workers causing large nosocomial outbreaks: a systematic review. BMC Infect Dis 2013;13:98.CrossRefGoogle ScholarPubMed
Moore, C, Dhaliwal, J, Tong, A, et al. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) acquisition in roommate contacts of patients colonized or infected with MRSA in an acute-care hospital. Infect Control Hosp Epidemiol 2008;29:600606.CrossRefGoogle ScholarPubMed
Bloemendaal, AL, Fluit, AC, Jansen, WM, et al. Acquisition and cross-transmission of Staphylococcus aureus in European intensive care units. Infect Control Hosp Epidemiol 2009;30:117124.CrossRefGoogle ScholarPubMed
Johnson, JK, Smith, G, Lee, MS, et al. The role of patient-to-patient transmission in the acquisition of imipenem-resistant pseudomonas aeruginosa colonization in the intensive care unit. J Infect Dis 2009;200:900905.CrossRefGoogle ScholarPubMed
Khandavilli, S, Wilson, P, Cookson, B, Cepeda, J, Bellingan, G, Brown, J. Utility of spa typing for investigating the local epidemiology of MRSA on a UK intensive care ward. J Hosp Infect 2009;71:2935.CrossRefGoogle ScholarPubMed
El-Ageery, SM, Abo-Shadi, MA, Elgendy, AM, Alghaithy, AA, Kandeel, AY. The role of health care workers and environment on transmission of methicillin–resistant Staphylococcus aureus among patients in a medical intensive care unit in a Saudi hospital. J Pure Appl Microbiol 2011;5:18.Google Scholar
Irfan, S, Turton, JF, Mehraj, J, et al. Molecular and epidemiological characterisation of clinical isolates of carbapenem-resistant Acinetobacter baumannii from public and private sector intensive care units in Karachi, Pakistan. J Hosp Infect 2011;78:143148.CrossRefGoogle ScholarPubMed
Price, JR, Golubchik, T, Cole, K, et al. Whole-genome sequencing shows that patient-to-patient transmission rarely accounts for acquisition of Staphylococcus aureus in an intensive care unit. Clin Infect Dis 2014;58:609618.CrossRefGoogle Scholar
Long, SW, Beres, SB, Olsen, RJ, Musser, JM. Absence of patient-to-patient intrahospital transmission of Staphylococcus aureus as determined by whole-genome sequencing. MBio 2014;5:e0169214.CrossRefGoogle ScholarPubMed
Amissah, NA, Chlebowicz, MA, Ablordey, A, et al. Molecular characterization of staphylococcus aureus isolates transmitted between patients with Buruli ulcer. PLoS Negl Trop Dis 2015;9:e0004049.CrossRefGoogle ScholarPubMed
Moore, G, Cookson, B, Gordon, NC, et al. Whole-genome sequencing in hierarchy with pulsed-field gel electrophoresis: the utility of this approach to establish possible sources of MRSA cross-transmission. J Hosp Infect 2015;90:3845.CrossRefGoogle ScholarPubMed
Huang, SS, Datta, R, Platt, R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 2006;166:19451951.CrossRefGoogle ScholarPubMed
Mitchell, B, Digney, W, Ferguson, J. Prior room occupancy increases risk of methicillin-resistant Staphylococcus aureus acquisition. Healthc Infect 2014;19:135140.CrossRefGoogle Scholar
Barnes, SL, Morgan, DJ, Harris, AD, Carling, PC, Thom, KA. Preventing the transmission of multidrug-resistant organisms: modeling the relative importance of hand hygiene and environmental cleaning interventions. Infect Control Hosp Epidemiol 2014;35:11561162.CrossRefGoogle ScholarPubMed
Alhmidi, H, John, A, Mana, TC, et al. Evaluation of viral surrogate markers for study of pathogen dissemination during simulations of patient care. Open Forum Infect Dis 2017;4:ofx128.CrossRefGoogle ScholarPubMed
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;54:31433148.CrossRefGoogle ScholarPubMed
Huang, SS, Platt, R. Risk of methicillin-resistant Staphylococcus aureus infection after previous infection or colonization. Clin Infect Dis 2003;36:281285.CrossRefGoogle ScholarPubMed