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Synergistic effects of length of stay and prior MDRO carriage on the colonization and co-colonization of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and carbapenemase-producing Enterobacterales across healthcare settings

Published online by Cambridge University Press:  30 March 2022

Htet Lin Htun Open the ORCID record for Htet Lin Htun [Opens in a new window] ,
Pei-Yun Hon ,
Rei Tan ,
Brenda Ang Open the ORCID record for Brenda Ang [Opens in a new window]  and
Angela Chow Open the ORCID record for Angela Chow [Opens in a new window]
Htet Lin Htun
Affiliation:
Department of Clinical Epidemiology, Office of Clinical Epidemiology, Analytics and Knowledge (OCEAN), Tan Tock Seng Hospital, Singapore
Pei-Yun Hon
Affiliation:
Department of Clinical Epidemiology, Office of Clinical Epidemiology, Analytics and Knowledge (OCEAN), Tan Tock Seng Hospital, Singapore
Rei Tan
Affiliation:
Yong Loo Lin School of Medicine, National University of Singapore, Singapore
Brenda Ang
Affiliation:
Yong Loo Lin School of Medicine, National University of Singapore, Singapore Department of Infectious Diseases, Tan Tock Seng Hospital, Singapore Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore
Angela Chow*
Affiliation:
Department of Clinical Epidemiology, Office of Clinical Epidemiology, Analytics and Knowledge (OCEAN), Tan Tock Seng Hospital, Singapore Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore Saw Swee Hock School of Public Health, National University of Singapore, Singapore
*
Author for correspondence: Angela Chow, E-mail: angela_chow@ttsh.com.sg
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Abstract

Objective:

To characterize the epidemiology of methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), and carbapenemase-producing Enterobacterales (CPE) co-colonization and to compare risk factors between healthcare facility types.

Design, setting, and participants:

We conducted a 3-year cross-sectional study among patients admitted to an acute-care hospital (ACH) and its 6 closely affiliated intermediate- and long-term care facilities (ILTCFs) in Singapore in June and July of 2014–2016.

Methods:

Specimens were concurrently collected from nares, axillae, and groins for MRSA detection, and from rectum or stool for VRE and CPE detection. Co-colonization was defined as having >1 positive culture of MRSA/VRE/CPE. Multinomial logistic regression was performed to determine predictors of co-colonization.

Results:

Of 5,456 patients recruited, 176 (3.2%) were co-colonized, with higher prevalence among patients in ITCFs (53 of 1,255, 4.2%) and the ACH (120 of 3,044, 3.9%) than LTCFs (3 of 1,157, 0.3%). MRSA/VRE was the most common type of co-colonization (162 of 5,456, 3.0%). Independent risk factors for co-colonization included male sex (odds ratio [OR], 1.96; 95% confidence interval [CI], 1.37–2.80), prior antibiotic therapy of 1–3 days (OR, 10.39; 95% CI, 2.08–51.96), 4–7 days (OR, 4.89; 95% CI, 1.01–23.68), >7 days (OR, 11.72; 95% CI, 2.81–48.85), and having an open wound (OR, 2.34; 95% CI, 1.66–3.29). Additionally, we detected the synergistic interaction of length of stay >14 days and prior multidrug-resistant organism (MDRO) carriage on co-colonization. Having an emergency surgery was a significant predictor of co-colonization in ACH patients, and we detected a dose–response association between duration of antibiotic therapy and co-colonization in ILTCF patients.

Conclusions:

We observed common and differential risk factors for MDRO co-colonization across healthcare settings. This study has identified at-risk groups that merit intensive interventions, particularly patients with prior MDRO carriage and longer length of stay.

Type
Original Article
Information
Infection Control & Hospital Epidemiology , Volume 44 , Issue 1 , January 2023 , pp. 31 - 39
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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

Cohen, ML. Changing patterns of infectious disease. Nature 2000;406:762–767.CrossRefGoogle ScholarPubMed
Eliopoulos, GM, Cosgrove, SE, Carmeli, Y. The impact of antimicrobial resistance on health and economic outcomes. Clin Infect Dis 2003;36:1433–1437.CrossRefGoogle Scholar
Friedman, ND, Temkin, E, Carmeli, Y. The negative impact of antibiotic resistance. Clin Microbiol Infect 2016;22:416–422.CrossRefGoogle ScholarPubMed
Chow, A, Htun, HL, Hon, P-Y, et al. Comparative epidemiology and factors associated with major healthcare-associated methicillin-resistant Staphylococcus aureus clones among interconnected acute-, intermediate- and long-term healthcare facilities in Singapore. Clin Microbiol Infect 2021;27:785.e789–785.e716.CrossRefGoogle Scholar
Tan, D, Htun, HL, Koh, J, et al. Comparative epidemiology of vancomycin-resistant enterococci colonization in an acute-care hospital and its affiliated intermediate- and long-term care facilities in Singapore. Antimicrob Agents Chemother 2018;62:e01507–e01518.CrossRefGoogle Scholar
Koh, TH, Hsu, LY, Chiu, LL, Lin, RV. Emergence of epidemic clones of vancomycin-resistant Enterococcus faecium in Singapore. J Hosp Infect 2006;63:234–236.CrossRefGoogle ScholarPubMed
Aung, AH, Kanagasabai, K, Koh, J, et al. Epidemiology and transmission of carbapenemase-producing Enterobacteriaceae in a healthcare network of an acute-care hospital and its affiliated intermediate- and long-term care facilities in Singapore. Antimicrob Agents Chemother 2021;65:e0258420.CrossRefGoogle Scholar
Boswihi, SS, Udo, EE. Methicillin-resistant Staphylococcus aureus: An update on the epidemiology, treatment options, and infection control. Curr Med Res Pract 2018;8:18–24.CrossRefGoogle Scholar
Elstrøm, P, Astrup, E, Hegstad, K, Samuelsen, Ø, Enger, H, Kacelnik, O. The fight to keep resistance at bay, epidemiology of carbapenemase producing organisms (CPOs), vancomycin-resistant enterococci (VRE) and methicillin-resistant Staphylococcus aureus (MRSA) in Norway, 2006–2017. PloS One 2019;14:e0211741.CrossRefGoogle ScholarPubMed
Liu, C, Chambers, HF. Staphylococcus aureus with heterogeneous resistance to vancomycin: epidemiology, clinical significance, and critical assessment of diagnostic methods. Antimicrob Agent Chemother 2003;47:3040–3045.CrossRefGoogle ScholarPubMed
Sng, L-H, Koh, TH, Wang, GCY, Hsu, L-Y, Kapi, M, Hiramatsu, K. Heterogeneous vancomycin-resistant Staphylococcus aureus (hetero-VISA) in Singapore. Int J Antimicrob Agents 2005;25:177–179.CrossRefGoogle ScholarPubMed
Hiramatsu, K, Hanaki, H, Ino, T, Yabuta, K, Oguri, T, Tenover, FC. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 1997;40:135–136.CrossRefGoogle ScholarPubMed
Howden, BP, Johnson, PDR, Ward, PB, Stinear, TP, Davies, JK. Isolates with low-level vancomycin resistance associated with persistent methicillin-resistant Staphylococcus aureus bacteremia. Antimicrob Agents Chemother 2006;50:3039–3047.CrossRefGoogle ScholarPubMed
Weinstein, RA, Fridkin, SK. Vancomycin-intermediate and -resistant Staphylococcus aureus: what the infectious disease specialist needs to know. Clin Infect Dis 2001;32:108–115.CrossRefGoogle Scholar
Noble, WC, Virani, Z, Cree, RG. Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus . FEMS Microbiol Lett 1992;72:195–198.CrossRefGoogle ScholarPubMed
Htun, HL, Hon, PY, Holden, MTG, Ang, B, Chow, A. Chlorhexidine and octenidine use, carriage of qac genes, and reduced antiseptic susceptibility in methicillin-resistant Staphylococcus aureus isolates from a healthcare network. Clin Microbiol Infect 2019;25:1154.e1151–1154.e1157.CrossRefGoogle ScholarPubMed
Hidron, AI, Kourbatova, EV, Halvosa, JS, et al. Risk factors for colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis 2005;41:159–166.CrossRefGoogle Scholar
Young, BE, Lye, DC, Krishnan, P, Chan, SP, Leo, YS. A prospective observational study of the prevalence and risk factors for colonization by antibiotic resistant bacteria in patients at admission to hospital in Singapore. BMC Infect Dis 2014;14:298.CrossRefGoogle ScholarPubMed
Hayakawa, K, Marchaim, D, Bathina, P, et al. Independent risk factors for the co-colonization of vancomycin-resistant Enterococcus faecalis and methicillin-resistant Staphylococcus aureus in the region most endemic for vancomycin-resistant Staphylococcus aureus isolation. Eur J Clin Microbiol Infect Dis 2013;32:815–820.CrossRefGoogle ScholarPubMed
Reyes, K, Malik, R, Moore, C, et al. Evaluation of risk factors for coinfection or cocolonization with vancomycin-resistant Enterococcus and methicillin-resistant Staphylococcus aureus . J Clin Microbiol 2010;48:628–630.CrossRefGoogle ScholarPubMed
Warren, DK, Nitin, A, Hill, C, Fraser, VJ, Kollef, MH. Occurrence of cocolonization or coinfection with vancomycin-resistant enterococci and methicillin-resistant Staphylococcus aureus in a medical intensive care unit. Infect Control Hosp Epidemiol 2015;25:99–104.CrossRefGoogle Scholar
Heinze, K, Kabeto, M, Martin, ET, Cassone, M, Hicks, L, Mody, L. Predictors of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci cocolonization among nursing facility patients. Am J Infect Control 2019;47:415–420.CrossRefGoogle ScholarPubMed
Flannery, EL, Wang, L, Zöllner, S, Foxman, B, Mobley, HLT, Mody, L. Wounds, functional disability, and indwelling devices are associated with cocolonization by methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci in southeast Michigan. Clin Infect Dis 2011;53:1215–1222.CrossRefGoogle ScholarPubMed
Furuno, J, Perencevich, E, Johnson, J, et al. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci cocolonization. Emerg Infect Dis J 2005;11:1539.CrossRefGoogle ScholarPubMed
McKinley, L, Becerra, B, Moriarty, H, et al. Vancomycin-resistant Enterococcus cocolonization rates with methicillin-resistant Staphylococcus aureus and Clostridium difficile in critically ill veterans. Am J Infect Control 2016;44:1047–1049.CrossRefGoogle ScholarPubMed
Rabinowitz, RP, Kufera, JA, Makley, MJ. A hidden reservoir of methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus in patients newly admitted to an acute rehabilitation hospital. PM R 2012;4:18–22.CrossRefGoogle Scholar
Meyer, E, Ziegler, R, Mattner, F, Schwab, F, Gastmeier, P, Martin, M. Increase of patients cocolonized or coinfected with methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus faecium or extended-spectrum β-lactamase–producing Enterobacteriaceae. Infection 2011;39:501–506.CrossRefGoogle ScholarPubMed
Wang, Y, Oppong, TB, Liang, X, Duan, G, Yang, H. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci cocolonization in patients: a meta-analysis. Am J Infect Control 2020;48:925–932.CrossRefGoogle ScholarPubMed
Flemming, H-C, Wingender, J. The biofilm matrix. Nat Revs Microbiol 2010;8:623–633.CrossRefGoogle ScholarPubMed
Percival, SL. Importance of biofilm formation in surgical infection. Br J Surg 2017;104:e85–e94.CrossRefGoogle ScholarPubMed
Wang, J, Foxman, B, Mody, L, Snitkin, ES. Network of microbial and antibiotic interactions drive colonization and infection with multidrug-resistant organisms. Proc Nat Acad Sci 2017;114:10467–10472.CrossRefGoogle ScholarPubMed
Sigurdardottir, B, Berg, JV, Hu, J, et al. Descriptive epidemiology and case–control study of patients colonized with vancomycin-resistant Enterococcus and methicillin-resistant Staphylococcus aureus . Infect Control Hosp Epidemiol 2016;27:913–919.CrossRefGoogle Scholar
Yoon, YK, Lee, MJ, Ju, Y, et al. Determining the clinical significance of co-colonization of vancomycin-resistant enterococci and methicillin-resistant Staphylococcus aureus in the intestinal tracts of patients in intensive care units: a case-control study. Ann Clin Microbiol Antimicrob 2019;18:28.CrossRefGoogle ScholarPubMed
Graffunder, EM, Venezia, RA. Risk factors associated with nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection including previous use of antimicrobials. J Antimicrob Chemother 2002;49:999–1005.CrossRefGoogle ScholarPubMed
Callejo-Torre, F, Eiros Bouza, JM, Olaechea Astigarraga, P, et al. Risk factors for methicillin-resistant Staphylococcus aureus colonisation or infection in intensive care units and their reliability for predicting MRSA on ICU admission. Infezioni medicina 2016;24:201–209.Google ScholarPubMed
Kibbler, CC, Quick, A, O’Neill, AM. The effect of increased bed numbers on MRSA transmission in acute medical wards. J Hosp Infect 1998;39:213–219.CrossRefGoogle ScholarPubMed
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