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Infection Control & Hospital Epidemiology


patients usingWGS(n=4), PFGE (n=4), multiple-locus variable- number tandem repeat analysis (MLVA; n = 1), and multilocus sequence typing (MLST; n = 1). The overall impact of patient-to-patient transmission reported


by these studies varied. For MRSA, the most studied MDRO included in our review, the overall impact of cross-transmission was highly variable (0–44%).


Discussion


Although it would be logistically burdensome to follow the whole transmission process ofMDROfrom colonized or infected patients to other susceptible patients in real-life healthcare settings, we have illustrated that existing high-quality studies demonstrate each of the 5 components of the complete transmission pathway. Nevertheless, the published and eligible evidence demonstrat-


ing transmission of MDRO from contaminated patients to the environment or to theHCWis more available and consistent than the evidence demonstrating the transmission in the contrary direc- tion (from environment to patient orHCWto patient). However, if we had loosen our eligibility criteria (ie, removing the molecular technique requirement), additional evidence supporting the trans- mission route from the environment to a subsequent patient could have been identified. Prior room occupancy studies have demon- strated that admission to a room previously occupied by an MRSA-positive patient or a VRE-positive patient significantly increases the odds of the newly admitted patient to acquire these MDROs.35,36 Studying these 2 transmission routes in real-life healthcare settings is indeed even more complicated and burden- some than studying the rest of the potential transmission routes. Nevertheless, more research directly focused on the importance and impact of these 2 specific routes of transmission would greatly inform infection prevention efforts in the acute-care setting. Furthermore, most manuscripts we identified through this scoping review focused on MRSA. More studies are needed on the trans- mission pathways of other MDROs, particularly recently emergent ones such as CRE. Additionally, the intercorrelation between transmission routes complicated our ability to measure the individual contributions from each vector of transmission (ie,HCWor healthcare environ- ment). Likewise, the tendency of infection prevention and control efforts to bundle multiple interventions (eg, environmental clean- ing plus contact precautions) restricted our ability to separate their effectiveness to prevent patient-to-patient MDRO transmission in hospitals. We need to incorporate new methods in our epidemio- logical toolkit such as mathematical modeling or benign surrogate markers to segregate these effects and identify interactions between them. For example, Barnes et al37 developed an agent-based model of patient-to-patient transmission to better understand the relative importance of hand hygiene and environmental clean- ing. Likewise, Donskey et al38 explored the use of cauliflower mosaic virus DNA as a surrogate marker for study pathogen dis- semination, which exemplifies how multiple unique markers can be introduced and followed. New tools such as these could allow us to better inform infection control measures and bundles to focus our efforts only on those measures that are highly effective. However, for these tools to be useful, these models must use parameters and data from high-quality field research based in real-life healthcare settings. Finally, this scoping review emphasizes the meaningful


impact of MDRO patient-to-patient transmission in healthcare settings. For MRSA, the most studied microorganism included


455


in our review, patient-to-patient transmission was observed as much as 44% of the time. Moreover, a large study across multi- ple ICUs in the United States demonstrated that on average, 21 VRE or MRSA new acquisitions per 1,000 patient days occurred.4 Furthermore, our review is limited only to acute-care settings. Post-acute care and long-term settings may potentially present even higher rates of MDRO transmission. These high levels of transmission are concerning; ~20% of patients who acquire anMDROgo on to develop an infection with this organ- ism post acquisition.27,39,40 Efforts to minimize MDRO acquis- ition events are critical and should be prioritized. It is essential to furtherstrengtheninfectionpreventionand controleffortsin healthcare settings to assure that all patients receive the highest possible quality of care.


Author ORCIDs. Natalia Blanco, 0000-0002-3157-1119


Financial support. This study was supported by the National Institutes of Health (NIH grant no. K24AI079040 to A. D. Harris) and by the Banting Postdoctoral Fellowship Program administered by the Government of Canada (L. O’Hara).


Conflict of interest. All authors report no conflicts of interest relevant to this article.


References


1. 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.


2. 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;23:329–334.


3. 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;165:1430–1435.


4. 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;310:1571–1580.


5. 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.


6. 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:DC18–DC20.


7. 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;25:114–120.


8. 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: 1045–1051.


9. 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;31:716–721.


10. Duckro AN, Blom DW, Lyle EA, Weinstein RA, Hayden MK. Transfer of vancomycin-resistant Enterococci via health care worker hands. Arch Intern Med 2005;165:302–307.


11. Munoz-Price LS, Namias N, Cleary T, et al. Acinetobacter baumannii: asso- ciation between environmental contamination of patient rooms and occu- pant status. Infect Control Hosp Epidemiol 2013;34:517–520.


12. 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;39:711–715.


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