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Can multidrug-resistant organisms become resistant to ultraviolet (UV) light following serial exposures? Characterization of post-UV genomic changes using whole-genome sequencing

Published online by Cambridge University Press:  22 March 2021

Hosoon Choi
Affiliation:
Department of Research, Central Texas Veterans Health Care System, Temple, Texas
Piyali Chatterjee
Affiliation:
Department of Research, Central Texas Veterans Health Care System, Temple, Texas
Munok Hwang
Affiliation:
Department of Research, Central Texas Veterans Health Care System, Temple, Texas
Eileen M. Stock
Affiliation:
Office of Research and Development, US Department of Veterans’ Affairs, Perry Point, Maryland
Janell S. Lukey
Affiliation:
Department of Pathology & Laboratory Medicine, Central Texas Veterans Health Care System, Temple, Texas
John E. Zeber
Affiliation:
Department of Research, Central Texas Veterans Health Care System, Temple, Texas University of Massachusetts Amherst School of Public Health & Health Sciences, Amherst, Massachusetts
Chetan Jinadatha*
Affiliation:
Department of Medicine, Central Texas Veterans Health Care System, Temple, Texas
*
Author for correspondence: Chetan Jinadatha, E-mail: [email protected]

Abstract

Objectives:

No-touch disinfection systems like xenon- or mercury-based ultraviolet (UV) are now commonly being used for hospital room disinfection. However, serial exposure to UV light can potentially lead to the development of bacterial resistance. We sought to determine whether UV resistance develops due to serial exposure to UV light using 3 epidemiologically important multidrug-resistant microbial strains.

Methods:

Methicillin-resistant Staphylococcus aureus (MRSA), carbapenemase–producing Klebsiella pneumoniae (KPC) and metallo-β-lactamase–producing Klebsiella pneumoniae (MBL) were serially exposed to 25 growth-irradiation cycles of UV produced by a xenon-based UV (Xe-UV) lamp for 5 minutes or a mercury-based UV (Hg-UV) lamp for 10 minutes. After each UV exposure cycle, the surviving colony-forming units (CFUs) were measured and compared with the initial inoculum of each cycle for each strain, respectively.

Results:

In each cycle, ˜1–10 million of MRSA, KPC, and MBL were used to test the effect of UV irradiation. Postexposure colony counts remained low (3–100 colonies) throughout the 25 serial exposures to both xenon- and mercury-based UV. The log-kill rate after each exposure showed no changes following UV disinfection by Xe-UV. The MRSA log-kill rate increased after repeated exposure to Hg-UV unlike KPC and MBL K. pneumoniae, which did not change. Whole-genome sequencing (WGS) analyses performed on these 3 strains demonstrated no significant genetic changes after multiple UV irradiation cycles.

Conclusions:

Exposure of multidrug-resistant bacteria to UV produced from 2 different UV sources did not engender UV resistance after 25 serial exposures, as demonstrated by WGS analysis; thus, UV disinfection is unlikely to generate UV-resistant hospital flora.

Type
Original Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

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References

Otter, JA, Yezli, S, French, GL. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 2011;32:687699.CrossRefGoogle ScholarPubMed
Dancer, SJ. Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Dis 2008;8:101113.CrossRefGoogle ScholarPubMed
Otter, JA, Yezli, S, Perl, TM, Barbut, F, French, GL. The role of ‘no-touch’ automated room disinfection systems in infection prevention and control. J Hosp Infect 2013;83:113.CrossRefGoogle ScholarPubMed
Gebel, J, Exner, M, French, G, et al. The role of surface disinfection in infection prevention. GMS Hyg Infect Control 2013;8:Doc10.Google Scholar
Stibich, M, Stachowiak, J, Tanner, B, et al. Evaluation of a pulsed-xenon ultraviolet room disinfection device for impact on hospital operations and microbial reduction. Infect Control Hosp Epidemiol 2011;32:286288.CrossRefGoogle ScholarPubMed
Rutala, WA, Gergen, MF, Weber, DJ. Room decontamination with UV radiation. Infect Control Hosp Epidemiol 2010;31:10251029.CrossRefGoogle ScholarPubMed
Havill, NL, Moore, BA, Boyce, JM. Comparison of the microbiological efficacy of hydrogen peroxide vapor and ultraviolet light processes for room decontamination. Infect Control Hosp Epidemiol 2012;33:507512.CrossRefGoogle Scholar
Nerandzic, MM, Cadnum, JL, Pultz, MJ, Donskey, CJ. Evaluation of an automated ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens in hospital rooms. BMC Infect Dis 2010;10:197.CrossRefGoogle ScholarPubMed
Nagaraja, A, Visintainer, P, Haas, JP, Menz, J, Wormser, GP, Montecalvo, MA. Clostridium difficile infections before and during use of ultraviolet disinfection. Am J Infect Control 2015;43:940945.CrossRefGoogle ScholarPubMed
Levin, J, Riley, LS, Parrish, C, English, D, Ahn, S. The effect of portable pulsed-xenon ultraviolet light after terminal cleaning on hospital-associated Clostridium difficile infection in a community hospital. Am J Infect Control 2013;41:746748.CrossRefGoogle Scholar
Miller, R, Simmons, S, Dale, C, Stachowiak, J, Stibich, M. Utilization and impact of a pulsed-xenon ultraviolet room disinfection system and multidisciplinary care team on Clostridium difficile in a long-term acute-care facility. Am J Infect Control 2015;43:13501353.CrossRefGoogle Scholar
Haas, JP, Menz, J, Dusza, S, Montecalvo, MA. Implementation and impact of ultraviolet environmental disinfection in an acute-care setting. Am J Infect Control 2014;42:586590.CrossRefGoogle Scholar
Napolitano, NA, Mahapatra, T, Tang, W. The effectiveness of UV-C radiation for facility-wide environmental disinfection to reduce healthcare-acquired infections. Am J Infect Control 2015;43:13421346.CrossRefGoogle Scholar
Zeber, JE, Pfeiffer, C, Baddley, JW, et al. Effect of pulsed-xenon ultraviolet room disinfection devices on microbial counts for methicillin-resistant Staphylococcus aureus and aerobic bacterial colonies. Am J Infect Control 2018;46:668673.CrossRefGoogle ScholarPubMed
El Haddad, L, Ghantoji, SS, Stibich, M, et al. Evaluation of a pulsed-xenon ultraviolet disinfection system to decrease bacterial contamination in operating rooms. BMC Infect Dis 2017;17:672.CrossRefGoogle ScholarPubMed
Anderson, DJ, Moehring, RW, Weber, DJ, et al. Effectiveness of targeted enhanced terminal room disinfection on hospital-wide acquisition and infection with multidrug-resistant organisms and Clostridium difficile: a secondary analysis of a multicentre cluster randomised controlled trial with crossover design (BETR Disinfection). Lancet Infect Dis 2018;18:845853.CrossRefGoogle Scholar
Anderson, DJ, Gergen, MF, Smathers, E, et al. Decontamination of targeted pathogens from patient rooms using an automated ultraviolet-C–emitting device. Infect Control Hosp Epidemiol 2013;34:466471.CrossRefGoogle ScholarPubMed
Nerandzic, MM, Thota, P, Sankar, CT, et al. Evaluation of a pulsed-xenon ultraviolet disinfection system for reduction of healthcare-associated pathogens in hospital rooms. Infect Control Hosp Epidemiol 2015;36:192197.CrossRefGoogle ScholarPubMed
Alcantara-Diaz, D, Brena-Valle, M, Serment-Guerrero, J. Divergent adaptation of Escherichia coli to cyclic ultraviolet light exposures. Mutagenesis 2004;19:349354.CrossRefGoogle ScholarPubMed
Nakamura, Y, Gojobori, T, Ikemura, T. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res 2000;28:292.CrossRefGoogle ScholarPubMed
Otaki, M, Okuda, A, Tajima, K, Iwasaki, T, Kinoshita, S, Ohgaki, S. Inactivation differences of microorganisms by low pressure UV and pulsed xenon lamps. Water Sci Technol 2003;47:185190.CrossRefGoogle ScholarPubMed
Guo, M, Hu, H, Bolton, JR, El-Din, MG. Comparison of low- and medium-pressure ultraviolet lamps: photoreactivation of Escherichia coli and total coliforms in secondary effluents of municipal wastewater treatment plants. Water Res 2009;43:815821.CrossRefGoogle ScholarPubMed
Kauser, I, Ciesielski, M, Poretsky, RS. Ultraviolet disinfection impacts the microbial community composition and function of treated wastewater effluent and the receiving urban river. Peer J 2019;7:e7455.CrossRefGoogle ScholarPubMed
Portero, LR, Alonso-Reyes, DG, Zannier, F, et al. Photolyases and cryptochromes in UV-resistant bacteria from high-altitude Andean lakes. Photochem Photobiol 2019;95:315330.CrossRefGoogle ScholarPubMed
Zenoff, VF, Heredia, J, Ferrero, M, Sineriz, F, Farias, ME. Diverse UV-B resistance of culturable bacterial community from high-altitude wetland water. Curr Microbiol 2006;52:359362.CrossRefGoogle ScholarPubMed
Dib, J, Motok, J, Zenoff, VF, Ordonez, O, Farias, ME. Occurrence of resistance to antibiotics, UV-B, and arsenic in bacteria isolated from extreme environments in high-altitude (above 4,400 m) Andean wetlands. Curr Microbiol 2008;56:510517.CrossRefGoogle Scholar
Rasuk, MC, Ferrer, GM, Kurth, D, Portero, LR, Farias, ME, Albarracin, VH. UV-resistant actinobacteria from high-altitude Andean lakes: isolation, characterization and antagonistic activities. Photochem Photobiol 2017;93:865880.CrossRefGoogle ScholarPubMed
Shibai, A, Takahashi, Y, Ishizawa, Y, et al. Mutation accumulation under UV radiation in Escherichia coli . Sci Rep 2017;7:14531.CrossRefGoogle ScholarPubMed
Rames, J, Chaloupecky, V, Sojkova, N, Bencko, V. An attempt to demonstrate the increased resistance of selected bacterial strains during repeated exposure to UV radiation at 254 nm. Cent Eur J Public Health 1997;5:3031.Google ScholarPubMed
Shoults, DC, Ashbolt, NJ. Decreased efficacy of UV inactivation of Staphylococcus aureus after multiple exposure and growth cycles. Int J Hyg Environ Health 2019;222:111116.CrossRefGoogle ScholarPubMed
Hall, MD, Holden, MT, Srisomang, P, et al. Improved characterisation of MRSA transmission using within-host bacterial sequence diversity. Elife 2019;8.Google ScholarPubMed
Miro, E, Rossen, JWA, Chlebowicz, MA, et al. Core-/Whole-genome multilocus sequence typing and core genome SNP-based typing of OXA-48-producing Klebsiella pneumoniae clinical isolates from Spain. Front Microbiol 2019;10:2961.CrossRefGoogle ScholarPubMed
Williams, PD, Eichstadt, SL, Kokjohn, TA, Martin, EL. Effects of ultraviolet radiation on the gram-positive marine bacterium Microbacterium maritypicum . Curr Microbiol 2007;55:17.CrossRefGoogle ScholarPubMed
Gehr, R, Wagner, M, Veerasubramanian, P, Payment, P. Disinfection efficiency of peracetic acid, UV and ozone after enhanced primary treatment of municipal wastewater. Water Res 2003;37:45734586.CrossRefGoogle ScholarPubMed