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Colonization of carbapenem-resistant Klebsiella pneumoniae in a sink-drain model biofilm system

Published online by Cambridge University Press:  25 November 2020

Maria Burgos-Garay ,
Christine Ganim ,
Tom J.B. de Man ,
Terri Davy ,
Amy J. Mathers ,
Shireen Kotay ,
Jonathan Daniels ,
K. Allison Perry ,
Erin Breaker  and
Rodney M. Donlan Open the ORCID record for Rodney M. Donlan [Opens in a new window]
Maria Burgos-Garay
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Christine Ganim
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Tom J.B. de Man
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Terri Davy
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Amy J. Mathers
Affiliation:
Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
Shireen Kotay
Affiliation:
Division of Infectious Diseases and International Health, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia
Jonathan Daniels
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
K. Allison Perry
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Rodney M. Donlan*
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
*
Author for correspondence: Rodney M. Donlan, E-mail: rld8@cdc.gov.
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Abstract

Background:

Sink drains in healthcare facilities may provide an environment for antimicrobial-resistant microorganisms, including carbapenemase-producing Klebsiella pneumoniae (CPKP).

Methods:

We investigated the colonization of a biofilm consortia by CPKP in a model system simulating a sink-drain P-trap. Centers for Disease Control (CDC) biofilm reactors (CBRs) were inoculated with microbial consortia originally recovered from 2 P-traps collected from separate patient rooms (designated rooms A and B) in a hospital. Biofilms were grown on stainless steel (SS) or polyvinyl chloride (PVC) coupons in autoclaved municipal drinking water (ATW) for 7 or 28 days.

Results:

Microbial communities in model systems (designated CBR-A or CBR-B) were less diverse than communities in respective P-traps A and B, and they were primarily composed of β and γ Proteobacteria, as determined using 16S rRNA community analysis. Following biofilm development CBRs were inoculated with either K. pneumoniae ST45 (ie, strain CAV1016) or K. pneumoniae ST258 KPC+ (ie, strain 258), and samples were collected over 21 days. Under most conditions tested (CBR-A: SS, 7-day biofilm; CBR-A: PVC, 28-day biofilm; CBR-B: SS, 7-day and 28-day biofilm; CBR-B: PVC, 28-day biofilm) significantly higher numbers of CAV1016 were observed compared to 258. CAV1016 showed no significant difference in quantity or persistence based on biofilm age (7 days vs 28 days) or substratum type (SS vs PVC). However, counts of 258 were significantly higher on 28-day biofilms and on SS.

Conclusions:

These results suggest that CPKP persistence in P-trap biofilms may be strain specific or may be related to the type of P-trap material or age of the biofilm.

Type
Original Article
Information
Infection Control & Hospital Epidemiology , Volume 42 , Issue 6 , June 2021 , pp. 722 - 730
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Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

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Footnotes

a

Authors of equal contribution.

PREVIOUS PRESENTATION: Portions of this study were presented as poster no. 2532 at the American Society for Microbiology 2017 ASM Microbe Meeting on June 4, 2017, in New Orleans, Louisiana.

References

Lowe, C, Willey, B, O’Shaughnessy, A, et al. Outbreak of extended-spectrum beta-lactamase-producing Klebsiella oxytoca infections associated with contaminated handwashing sinks. Emerg Infect Dis 2012;18:1242–1247.CrossRefGoogle ScholarPubMed
Chapuis, A, Amoureux, L, Bador, J, et al. Outbreak of extended-spectrum beta-lactamase–producing Enterobacter cloacae with high MICs of quaternary ammonium compounds in a hematology ward associated with contaminated sinks. Front Microbiol 2016;7:1070.CrossRefGoogle Scholar
Lalancette, C, Charron, D, Laferriere, C, et al. Hospital drains as reservoirs of Pseudomonas aeruginosa: multiple-locus variable-number of tandem repeats analysis genotypes recovered from faucets, sink surfaces and patients. Pathogens 2017;6. doi: 3390/pathogens6030036.CrossRefGoogle Scholar
De Geyter, D, Blommaert, L, Verbraeken, N, et al. The sink as a potential source of transmission of carbapenemase-producing Enterobacteriaceae in the intensive care unit. Antimicrob Resist Infect Control 2017;6:24.CrossRefGoogle ScholarPubMed
Starlander, G, Melhus, A. Minor outbreak of extended-spectrum beta-lactamase–producing Klebsiella pneumoniae in an intensive care unit due to a contaminated sink. J Hosp Infect 2012;82:122–124.CrossRefGoogle Scholar
Leitner, E, Zarfel, G, Luxner, J, et al. Contaminated handwashing sinks as the source of a clonal outbreak of KPC-2–producing Klebsiella oxytoca on a hematology ward. Antimicrob Agents Chemother 2015;59:714–716.CrossRefGoogle ScholarPubMed
Palmore, TN, Henderson, DK. Managing transmission of carbapenem-resistant Enterobacteriaceae in healthcare settings: a view from the trenches. Clin Infect Dis 2013;57:1593–1599.CrossRefGoogle ScholarPubMed
Gupta, N, Limbago, B, Patel, JB, Kallen, AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis 2011;53:60–67.CrossRefGoogle ScholarPubMed
Centers for Disease Control and Prevention. Antibiotic Resistance Threats in the United States, 2019. Atlanta, GA: CDC; 2019.Google Scholar
Santiago, AJ, Burgos-Garay, ML, Kartforosh, L, Mazher, M, Donlan, RM. Bacteriophage treatment of carbapenemase-producing Klebsiella pneumoniae in a multispecies biofilm: a potential for biocontrol strategy for healthcare facilities. AIMS Microbiol 2020;6:43–63.CrossRefGoogle Scholar
Abbott, S. Klebsiella, Enterobacter, Citrobacter, Serratia, Plesiomonas, and Other Enterobacteraceae. In: Versalovic J, Carroll KC, Funke G, Jorgensen JH, Landry ML, Warnock DW, eds. Manual of Clinical Microbiology Vol. 1, Tenth edition. Washington, DC: ASM Press; 2011: 639–657.Google Scholar
Camper, AK, McFeters, GA, Characklis, WG, Jones, WL. Growth kinetics of coliform bacteria under conditions relevant to drinking water distribution systems. Appl Environ Microbiol 1991;57:2233–2239.CrossRefGoogle ScholarPubMed
Morin, P, Camper, A, Jones, W, Gatel, D, Goldman, JC. Colonization and disinfection of biofilms hosting coliform-colonized carbon fines. Appl Environ Microbiol 1996;62:4428–4432.CrossRefGoogle ScholarPubMed
Mathers, AJ, Cox, HL, Bonatti, H, et al. Fatal cross infection by carbapenem-resistant Klebsiella in two liver transplant recipients. Transpl Infect Dis 2009;11:257–265.CrossRefGoogle ScholarPubMed
Marsh, JW, Krauland, MG, Nelson, JS, et al. Genomic epidemiology of an endoscope-associated outbreak of Klebsiella pneumoniae carbapenemase (KPC)-producing K. pneumoniae . PLoS ONE 2015. doi: 10.1371/journal.pone.0144310.CrossRefGoogle Scholar
Pierce, VM, Simner, PJ, Lonsway, DR, et al. Modified carbapenem inactivation method for phenotypic detection of carbapenemase production among Enterobacteriaceae. J Clin Microbiol 2017;55:2321–2333.CrossRefGoogle ScholarPubMed
Franco, LC, Tanner, W, Ganim, C, Davy, T, Edwards, J, Donlan, R. A microbiological survey of handwashing sinks in the hospital built environment reveals differences in patient room and healthcare personnel sinks. Scientific Rept 2020;10. doi: 10.1038/s41598-020-65052-7.CrossRefGoogle Scholar
Goeres, DM, Loetterle, LR, Hamilton, MA, Murga, R, Kirby, DW, Donlan, RM. Statistical assessment of a laboratory method for growing biofilms. Microbiol 2005;151:757–762.CrossRefGoogle ScholarPubMed
Armbruster, CR, Forster, TS, Donlan, RM, O’Connell, HA, Shams, AM, Williams, MM. A biofilm model developed to investigate survival and disinfection of Mycobacterium mucogenicum in potable water. Biofouling 2012;28:1129–1139.CrossRefGoogle ScholarPubMed
Lax, S, Smith, D, Sangwan, N, et al. Bacterial colonization and succession in a newly opened hospital. Sci Transl Med 2017;9. doi: 10.1126/scitranslmed.aah6500.CrossRefGoogle Scholar
Parada, AE, Needham, DM, Fuhrman, JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 2016;18:1403–1414.CrossRefGoogle ScholarPubMed
Walters, W, Hyde, ER, Berg-Lyons, D, et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 2015;1.CrossRefGoogle Scholar
Zhang, J, Kobert, K, Flouri, T, Stamatakis, A. PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 2014;30:614–620.CrossRefGoogle ScholarPubMed
Fast-X Tool Kit. Hannon Lab website. http://hannonlab.cshl.edu/fastx_toolkit/. Accessed October 29, 2020/Google Scholar
Rognes, T, Flouri, T, Nichols, B, Quince, C, Mahe, F. VSEARCH: a versatile open source tool for metagenomics. Peer J 2016;4:e2584.CrossRefGoogle ScholarPubMed
Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335–336.CrossRefGoogle ScholarPubMed
Rideout, JR, He, Y, Navas-Molina, JA, et al. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. Peer J 2014;21:2:e545.CrossRefGoogle Scholar
Kopylova, E, Noe, L, Touzet, H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 2012;28:3211–3217.CrossRefGoogle ScholarPubMed
Sumaclust. GitHub website. http://metabarcoding.org/sumatra/. Accessed October 29, 2020.Google Scholar
DeSantis, TZ, Hugenholtz, P, Larsen, N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006;72:5069–5072.CrossRefGoogle ScholarPubMed
Lozupone, C, Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005;71:8228–8235.CrossRefGoogle ScholarPubMed
Feazel, LM, Baumgartner, LK, Peterson, KL, Frank, DN, Harris, JK, Pace, NR. Opportunistic pathogens enriched in showerhead biofilms. Proc Nat Acad Sci 2009;106:16393–16399.CrossRefGoogle ScholarPubMed
Buse, HY, Lu, J, Lu, X, Mou, X, Ashbolt, NJ. Microbial diversities (16S and 18S rRNA gene pyrosequencing) and environmental pathogens within drinking water biofilms grown on the common premise plumbing materials unplasticized polyvinylchloride and copper. FEMS Microbiol Ecol 2014;88:280–295.CrossRefGoogle Scholar
McBain, AJ, Bartolo, RG, Catrenich, CE, Charbonneau, D, Ledder, RG, Rickard, AH, Symmons, SA, Gilbert, P. Microbial characterization of biofilms in domestic drains and the establishment of stable biofilm microcosms. Appl Environ Microbiol 2003;69:177–185.CrossRefGoogle ScholarPubMed
Henne, K, Kahlisch, L, Brettar, I, Hofle, MG. Analysis of structure and composition of bacterial core communities in mature drinking water biofilms and bulk water of a citywide network in Germany. Appl Environ Microbiol 2012;78:3530–3538.CrossRefGoogle ScholarPubMed
Szabo, JG, Rice, EW, Bishop, PL. Persistence of Klebsiella pneumoniae on simulated biofilm in a model drinking water system. Environ Sci Technol 2006;40:4996–5002.CrossRefGoogle Scholar
Byrd, JJ, Xu, H-S, Colwell, RR. Viable but nonculturable bacteria in drinking water. Appl Environ Microbiol 1991;57:875–878.CrossRefGoogle ScholarPubMed
Banning, N, Toze, S, Mee, BJ. Persistance of biofilm-associated Escherichia coli and Pseudomonae aeruginosa in groundwater and treated effluent in a laboratory model system. Microbiol 2003;149:47–55.CrossRefGoogle Scholar
Juhna, T, Birzniece, D, Larsson, S, et al. Detection of Escherichia coli in biofilms from pipe samples and coupons in drinking water distribution networks. Appl Environ Microbiol 2007;73:7456–7464.CrossRefGoogle ScholarPubMed
Sibille, I, Sime-Ngando, T, Mathieu, L, Block, JC. Protozoan bacterivory and Escherichia coli survival in drinking water distribution systems.Google Scholar