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Healthcare-associated multispecies outbreaks of OXA-48–positive carbapenemase-producing Enterobacteriaceae in a Singapore tertiary-care hospital

Published online by Cambridge University Press:  14 March 2022

Indumathi Venkatachalam Open the ORCID record for Indumathi Venkatachalam [Opens in a new window] ,
Molly Kue Bien How ,
Karrie Kwan Ki Ko ,
Nurdyana Binte Abdul Rahman ,
Edwin Philip Conceicao ,
May Kyawt Aung ,
Myat Oo Aung ,
Yong Yang ,
Kwee Yuen Tan  and
Jean Xiang Ying Sim
...Show all authors
Indumathi Venkatachalam*
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore Department of Infectious Diseases, Singapore General Hospital, Singapore
Molly Kue Bien How
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
Karrie Kwan Ki Ko
Affiliation:
Department of Microbiology, Singapore General Hospital, Singapore Department of Molecular Pathology, Singapore General Hospital, Singapore
Nurdyana Binte Abdul Rahman
Affiliation:
Department of Molecular Pathology, Singapore General Hospital, Singapore
Edwin Philip Conceicao
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
May Kyawt Aung
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
Myat Oo Aung
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
Yong Yang
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
Kwee Yuen Tan
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
Jean Xiang Ying Sim
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore Department of Infectious Diseases, Singapore General Hospital, Singapore
Lai Chee Lee
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
Moi Lin Ling
Affiliation:
Department of Infection Prevention and Epidemiology, Singapore General Hospital, Singapore
*
Author for correspondence: Dr Indumathi Venkatachalam, E-mail: indumathi.venkatachalam@singhealth.com.sg
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Abstract

Objective:

To describe OXA-48–like carbapenem-producing Enterobacteriaceae (CPE) outbreaks at Singapore General Hospital between 2018 and 2020 and to determine the risk associated with OXA-48 carriage in the 2020 outbreak.

Design:

Outbreak report and case–control study.

Setting:

Singapore General Hospital (SGH) is a tertiary-care academic medical center in Singapore with 1,750 beds.

Methods:

Active surveillance for CPE is conducted for selected high-risk patient cohorts through molecular testing on rectal swabs or stool samples. Patients with CPE are isolated or placed in cohorts under contact precautions. During outbreak investigations, rectal swabs are repeated for culture. For the 2020 outbreak, a retrospective case–control study was conducted in which controls were inpatients who tested negative for OXA-48 and were selected at a 1:3 case-to-control ratio.

Results:

Hospital wide, the median number of patients with healthcare-associated OXA-48 was 2 per month. In the 3-year period between 2018 and 2020, 3 OXA-48 outbreaks were investigated and managed, involving 4 patients with Klebsiella pneumoniae in 2018, 55 patients with K. pneumoniae or Escherichia coli in 2019, and 49 patients with multispecies Enterobacterales in 2020. During the 2020 outbreak, independent risk factors for OXA-48 carriage on multivariate analysis (49 patients and 147 controls) were diarrhea within the preceding 2 weeks (OR, 3.3; 95% CI, 1.1–10.7; P = .039), contact with an OXA-48–carrying patient (OR, 8.7; 95% CI, 1.9–39.3; P = .005), and exposure to carbapenems (OR, 17.2; 95% CI, 2.2–136; P = .007) or penicillin (OR, 16.6; 95% CI, 3.8–71.0; P < .001).

Conclusions:

Multispecies OXA-48 outbreaks in our institution are likely related to a favorable ecological condition and selective pressure exerted by antimicrobial use. The integration of molecular surveillance epidemiology of the healthcare environment is important in understanding the risk of healthcare–associated infection to patients.

Type
Original Article
Information
Infection Control & Hospital Epidemiology , Volume 44 , Issue 1 , January 2023 , pp. 8 - 16
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Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

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References

Evans, BA, Amyes, SGB. OXA b-lactamases. Clin Microbiol Rev 2014;27:241–263.CrossRefGoogle Scholar
Poirel, L, Heritier, C, Tolun, V, Nordmann, P. Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae . Antimicrob. Agents Chemother 2004;48:15–22.CrossRefGoogle ScholarPubMed
Pitout, JDD, Peirano, G, Kock, MM, Strydom, KA, Matsumura, Y. The global ascendency of OXA-48–type carbapenemases. Clin Microbiol Rev 2020;33(1):e00102–19.Google Scholar
Potron, A, Nordmann, P, Rondinaud, E, Jaureguy, F, Poirel, L. A mosaic transposon encoding OXA-48 and CTX-M-15: towards pan-resistance. J Antimicrob Chemother 2013;68:476–477.CrossRefGoogle ScholarPubMed
Sah, R, Khadka, S, Shrestha, GS, et al. Detection of pan drug resistance OXA-48–producing Providencia in an ICU patient for the first time in Nepal. Antimicrob Resist Infect Control 2019;8:155 CrossRefGoogle Scholar
Kanamori, H, Weber, DJ, Gergen, MF, DiBiase, LM, Sickbert-Bennett, EE, Rutala, WA. Epidemiologic characteristics of healthcare-associated outbreaks and lessons learned from multiple outbreak investigations with a focus on the usefulness of routine molecular analysis. Am J Infect Control 2018;46:893–898.CrossRefGoogle Scholar
Robustillo-Rodela, A, Perez-Blanco, V, Ruiz, MAE, Carrascoso, GR, Iglesias, JCF, Martin, DA. Successful control of 2 simultaneous outbreaks of OXA-48 carbapenemase-producing Enterobacteriaceae and multidrug-resistant Acinetobacter baumannii in an intensive care unit. Am J Infect Control 2017;45:1356–1362.CrossRefGoogle Scholar
Marimuthu, K, Venkatachalam, I, Khong, WX, et al. Clinical and molecular epidemiology of carbapenem-resistant Enterobacteriaceae among adult inpatients in Singapore. Clin Infect Dis 2017;64 suppl 2:S68–S75.CrossRefGoogle Scholar
Koh, TH, Babini, GS, Woodford, N, Sng, LH, Hall, LM, Livermore, DM. Carbapenem- hydrolysing IMP-1 β-lactamase in Klebsiella pneumoniae from Singapore. Lancet 1999;353:2162.CrossRefGoogle ScholarPubMed
Teo, J, Ngan, G, Balm, M, Jureen, R, Krishnan, P, Lin, R. Molecular characterization of NDM-1 producing Enterobacteriaceae isolates in Singapore hospitals. Western Pac Surveill Response J 2012;3:19–24.CrossRefGoogle ScholarPubMed
Venkatachalam, I, Teo, J, Balm, MN, Fisher, DA, Jureen, R, Lin, RT. Klebsiella pneumoniae carbapenemase-producing enterobacteria in hospital, Singapore. Emerg Infect Dis 2012;18:1381–1383.CrossRefGoogle ScholarPubMed
Balm, MN, Ngan, G, Jureen, R, Lin, RT, Teo, JW. OXA-181–producing Klebsiella pneumoniae establishing in Singapore. BMC Infect Dis 2013;13:58.CrossRefGoogle ScholarPubMed
de Man, TJB, Yaffee, AQ, Zhu, W, et al. Multispecies outbreak of verona integron-encoded metallo-ß-lactamase–producing multidrug-resistant bacteria driven by a promiscuous incompatibility group A/C2 plasmid. Clin Infect Dis 2021;72:414–420.CrossRefGoogle ScholarPubMed
Gupta, N, Limbago, BM, Patel, JB, Kallen, AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis 2011;53:60–67.CrossRefGoogle ScholarPubMed
Nordmann, P, Gniadkowski, M, Giske, CG, et al. Identification and screening of carbapenemase-producing Enterobacteriaceae . Clin Microbiol Infect 2012;18:432–438.CrossRefGoogle ScholarPubMed
Wee, LEI, Conceicao, EP, Tan, JY, et al. Unintended consequences of infection prevention and control measures during COVID-19 pandemic. Am J Infect Control 2021;49:469–477.CrossRefGoogle ScholarPubMed
Potron, A, Kalpoe, J, Poirel, L, Nordmann, P. European dissemination of a single OXA-48-producing Klebsiella pneumoniae clone. Clin Microbiol Infect 2011;17:E24–E26.CrossRefGoogle ScholarPubMed
Voulgari, E, Zarkotou, O, Ranellou, K, et al. Outbreak of OXA-48 carbapenemase-producing Klebsiella pneumoniae in Greece involving an ST11 clone. J Antimicrob Chemother 2013;68:84–88.CrossRefGoogle ScholarPubMed
Adler, A, Solter, E, Masarwa, S, et al. Epidemiological and microbiological characteristics of an outbreak caused by OXA-48–producing Enterobacteriaceae in a neonatal intensive care unit in Jerusalem, Israel. J Clin Microbiol 2013;51:2926–2930.CrossRefGoogle Scholar
Outbreak of carbapenemase-producing (NDM-1 and OXA-48) and colistin-resistant Klebsiella pneumoniae ST307, north-east Germany, 2019. European Centre for Disease Prevention and Control website. https://www.ecdc.europa.eu/en/publications-data/outbreak-Klebsiella-pneumoniae-Germany#:∼:text=Executive%20summary-,Germany%20has%20reported%20an%20outbreak%20of%20carbapenemase%2Dproducing%20(NDM%2D,east%20Germany%20have%20been%20affected. Published October 28, 2019. Accessed February 28, 2022.Google Scholar
Hidalgo, L, de Been, M, Rogers, MRC, et al. Sequence-based epidemiology of an OXA-48 plasmid during a hospital outbreak. Antimicrob Agents Chemother 2019;63(12):e01204–19.CrossRefGoogle ScholarPubMed
Dautzenberg, MJD, Ossewaarde, JM, de Greeff, SC, Troelstra, A, Bonten, MJM. Risk factors for the acquisition of OXA-48–producing Enterobacteriaceae in a hospital outbreak setting: a matched case–control study. J Antimicrob Chemother 2016;71:2273–2279.CrossRefGoogle Scholar
Regev-Yochay, G, Smollan, G, Tal, I, et al. Sink traps as the source of transmission of OXA-48-producing Serratia marcescens in an intensive care unit. Infect Control Hosp Epidemiol 2018;39:1307–1315.CrossRefGoogle Scholar
Bourigault, C, Le Gallou, F, Bodet, N, et al. Duodenoscopy: an amplifier of cross-transmission during a carbapenemase-producing Enterobacteriaceae outbreak in a gastroenterology pathway. J Hosp Infect 2008;99:422–426.CrossRefGoogle Scholar
Ling, ML, Tee, YM, Tan, SG, et al. Risk factors for acquisition of carbapenem-resistant Enterobacteriaceae in an acute tertiary-care hospital in Singapore. Antimicrob Resist Infect Control 2015;4:26.CrossRefGoogle Scholar
Regev-Yochay, G, Smollan, G, Tal, I, et al. Sink traps as the source of transmission of OXA-48–producing Serratia marcescens in an intensive care unit. Infect Control Hosp Epidemiol 2018;39:1307–1315.CrossRefGoogle Scholar
Bourigault, C, Le Gallou, F, Bodet, N, et al. Duodenoscopy: an amplifier of cross-transmission during a carbapenemase-producing Enterobacteriaceae outbreak in a gastroenterology pathway. J Hosp Infect 2018;99:422–426.CrossRefGoogle Scholar
Potron, A, Poirel, L, Nordmann, P. Origin of OXA-181, an emerging carbapenem-hydrolyzing oxacillinase, as a chromosomal gene in Shewanella xiamenensis . Antimicrob Agents Chemother 2011;55:4405–4407.CrossRefGoogle ScholarPubMed
Poirel, L, Naas, T, Nordmann, PP. Diversity, epidemiology, and genetics of class D β-lactamases. Antimicrob Agents Chemother 2010;54:24–38.CrossRefGoogle ScholarPubMed
Bonten, MJ. Colonization pressure: a critical parameter in the epidemiology of antibiotic-resistant bacteria. Crit Care 2012;16:142.CrossRefGoogle ScholarPubMed
D’Agata, EMC. Methodologic issues of case–control studies: a review of established and newly recognized limitations. Infect Control Hosp Epidemiol 2005;26:338–341.CrossRefGoogle ScholarPubMed
Merrer, J, Santoli, F, Appéré de Vecchi C, Tran B, De Jonghe B, Outin H. ‘Colonization pressure’ and risk of acquisition of methicillin-resistant Staphylococcus aureus in a medical intensive care unit. Infect Control Hosp Epidemiol 2000;21:718–723.CrossRefGoogle Scholar
Harris, AD, Johnson, JK, Thom, KA, et al. Risk factors for development of intestinal colonization with imipenem-resistant Pseudomonas aeruginosa in the intensive care unit setting. Infect Control Hosp Epidemiol 2011;32:719–722.CrossRefGoogle ScholarPubMed
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;32:481–489.CrossRefGoogle ScholarPubMed
Harris, AD, Karchmer, TB, Carmeli, Y, Samore, MH. Methodological principles of case-control studies that analyzed risk factors for antibiotic resistance: a systematic review. Clin Infect Dis 2001;32:1055–1061.CrossRefGoogle ScholarPubMed