Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T03:39:28.215Z Has data issue: false hasContentIssue false
  • English
  • Français

Household carriage and acquisition of extended-spectrum β-lactamase–producing Enterobacteriaceae: A systematic review

Published online by Cambridge University Press:  11 December 2019

Romain Martischang Open the ORCID record for Romain Martischang [Opens in a new window] ,
Maria E. Riccio ,
Mohamed Abbas ,
Andrew J. Stewardson ,
Jan A. J. W. Kluytmans  and
Stephan Harbarth
Romain Martischang
Affiliation:
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Maria E. Riccio
Affiliation:
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Mohamed Abbas
Affiliation:
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Andrew J. Stewardson
Affiliation:
Department of Infectious Diseases, Monash University and Alfred Health, Melbourne, Australia
Jan A. J. W. Kluytmans
Affiliation:
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, the Netherlands
Stephan Harbarth*
Affiliation:
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
*
Author for correspondence: Stephan Harbarth, Hôpitaux Universitaires de Genève, Service Prévention et Contrôle de l'Infection, CH-1211 Genève 14. E-mail: stephan.harbarth@hcuge.ch
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

The epidemiology of ESBL-producing Enterobacteriaceae (ESBL-PE) has been extensively studied in hospitals, but data on community transmission are scarce. We investigated ESBL-PE cocarriage and acquisition in households using a systematic literature review.

Methods:

We conducted a systematic literature search to retrieve cross-sectional or cohort studies published between 1990 and 2018 evaluating cocarriage proportions and/or acquisition rates of ESBL-PE among household members, without language restriction. We excluded studies focusing on animal-to-human transmission or conducted in nonhousehold settings. The main outcomes were ESBL-PE cocarriage proportions and acquisition rates, stratified according to phenotypic or genotypic assessment of strain relatedness. Cocarriage proportions of clonally related ESBL-PE were transformed using the double-arcsine method and were pooled using a random-effects model. Potential biases were assessed manually.

Results:

We included 13 studies. Among 863 household members of ESBL-PE positive index cases, prevalence of ESBL-PE cocarriage ranged from 8% to 37%. Overall, 12% (95% confidence interval [CI], 8%–16%) of subjects had a clonally related strain. Those proportions were higher for Klebsiella pneumoniae (20%–25%) than for Escherichia coli (10%–20%). Acquisition rates of clonally related ESBL-PE among 180 initially ESBL-PE–free household members of a previously identified carrier ranged between 1.56 and 2.03 events per 1,000 person weeks of follow-up. We identified multiple sources of bias and high heterogeneity (I2, 70%) between studies.

Conclusions:

ESBL-PE household cocarriage is frequent, suggesting intrafamilial acquisition. Further research is needed to evaluate the risk and control of ESBL-PE household transmission.

Type
Original Article
Information
Infection Control & Hospital Epidemiology , Volume 41 , Issue 3 , March 2020 , pp. 286 - 294
Copyright
© 2019 by The Society for Healthcare Epidemiology of America. All rights reserved.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

PREVIOUS PRESENTATION: These results were presented in part as a poster at the Fifth International Conference on Prevention and Infection Control on September 13, 2019, in Geneva, Switzerland.

References

Karanika, S, Karantanos, T, Arvanitis, M, et al.Fecal colonization with extended-spectrum beta-lactamase–producing Enterobacteriaceae and risk factors among healthy individuals: a systematic review and meta-analysis. Clin Infect Dis 2016;63:310–318.CrossRefGoogle Scholar
Stewardson, AJ, Allignol, A, Beyersmann, J, et al.The health and economic burden of bloodstream infections caused by antimicrobial-susceptible and non-susceptible Enterobacteriaceae and Staphylococcus aureus in European hospitals, 2010 and 2011: a multicentre retrospective cohort study. Euro Surveill 2016;21(33). doi: 10.2807/1560-7917.ES.2016.21.33.30319.CrossRefGoogle ScholarPubMed
Johnson, JR, Thuras, P, Johnston, BD, et al.The pandemic H30 subclone of Escherichia coli sequence type 131 is associated with persistent infections and adverse outcomes independent from its multidrug resistance and associations with compromised hosts. Clin Infect Dis 2016;62:1529–1536.CrossRefGoogle ScholarPubMed
Stewardson, AJ, Vervoort, J, Adriaenssens, N, et al.Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae: a multinational prospective cohort study. Clin Microbiol Infect 2018;24:972–979.CrossRefGoogle ScholarPubMed
Rodríguez-Baño, J, Navarro, MD, Romero, L, et al.Epidemiology and clinical features of infections caused by extended-spectrum beta-lactamase–producing Escherichia coli in nonhospitalized patients. J Clin Microbiol 2004;42:1089–1094.CrossRefGoogle ScholarPubMed
Calbo, E, Romaní, V, Xercavins, M, et al.Risk factors for community-onset urinary tract infections due to Escherichia coli harbouring extended-spectrum beta-lactamases. J Antimicrob Chemother 2006;57:780–783.CrossRefGoogle ScholarPubMed
Aldeyab, MA, Harbarth, S, Vernaz, N, et al.The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase–producing bacteria in primary and secondary healthcare settings. Br J Clin Pharmacol 2012;74:171–179.CrossRefGoogle ScholarPubMed
Tham, J, Odenholt, I, Walder, M, et al.Risk factors for infections with extended-spectrum beta-lactamase–producing Escherichia coli in a county of Southern Sweden. Infect Drug Resist 2013;6:93–97.CrossRefGoogle Scholar
Ruppé, E, Andremont, A, Armand-Lefèvre, L.Digestive tract colonization by multidrug-resistant Enterobacteriaceae in travellers: an update. Travel Med Infect Dis 2018;21:28–35.CrossRefGoogle ScholarPubMed
van den Bunt, G, Liakopoulos, A, Mevius, DJ, et al.ESBL/AmpC-producing Enterobacteriaceae in households with children of preschool age: prevalence, risk factors and cocarriage. J Antimicrob Chemother 2017;72:589–595.CrossRefGoogle Scholar
Hijazi, SM, Fawzi, MA, Ali, FM, et al.Prevalence and characterization of extended-spectrum beta-lactamases producing Enterobacteriaceae in healthy children and associated risk factors. Ann Clin Microbiol Antimicrob 2016;15:3.CrossRefGoogle ScholarPubMed
Otter, JA, Natale, A, Batra, R, et al.Individual- and community-level risk factors for ESBL Enterobacteriaceae colonization identified by universal admission screening in London. Clin Microbiol Infect 2019;25:1259–1265.CrossRefGoogle Scholar
Samore, MH, Tonnerre, C, Hannah, EL, et al.Impact of outpatient antibiotic use on carriage of ampicillin-resistant Escherichia coli. Antimicrob Agents Chemother 2011;55:1135–1141.CrossRefGoogle ScholarPubMed
Moher, D, Liberati, A, Tetzlaff, J, et al.Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097.CrossRefGoogle ScholarPubMed
Viechtbauer, W. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software website. http://www.jstatsoft.org/v36/i03/. Published 2010. Accessed February 21, 2019.CrossRefGoogle Scholar
Guido Schwarzer. meta: An R package for meta-analysis. R News website. https://cran.r-project.org/doc/Rnews/Rnews_2007-3.pdf. Published 2007. Accessed February 21, 2019.Google Scholar
Barendregt, JJ, Doi, SA, Lee, YY, et al.Meta-analysis of prevalence. J Epidemiol Commun Health 2013;67:974–978.CrossRefGoogle Scholar
Adler, A, Baraniak, A, Izdebski, R, et al.A multinational study of colonization with extended spectrum β-lactamase–producing Enterobacteriaceae in healthcare personnel and family members of carrier patients hospitalized in rehabilitation centres. Clin Microbiol Infect 2014;20:O516–O523.CrossRefGoogle ScholarPubMed
Rodríguez-Baño, J, López-Cerero, L, Navarro, MD, et al.Faecal carriage of extended-spectrum beta-lactamase–producing Escherichia coli: prevalence, risk factors and molecular epidemiology. J Antimicrob Chemother 2008;62:1142–1149.CrossRefGoogle ScholarPubMed
Strenger, V, Feierl, G, Resch, B, et al.Fecal carriage and intrafamilial spread of extended-spectrum β-lactamase–producing Enterobacteriaceae following colonization at the neonatal ICU. Pediatr Crit Care Med 2013;14:157–163.CrossRefGoogle ScholarPubMed
Lo, W-U, Ho, P-L, Chow, K-H, et al.Fecal carriage of CTXM type extended-spectrum beta-lactamase–producing organisms by children and their household contacts. J Infect 2010;60:286–292.CrossRefGoogle ScholarPubMed
Liakopoulos, A, van den Bunt, G, Geurts, Y, et al.High prevalence of intra-familial co-colonization by extended-spectrum cephalosporin-resistant Enterobacteriaceae in preschool children and their parents in Dutch households. Front Microbiol 2018;9:293.CrossRefGoogle ScholarPubMed
Valverde, A, Grill, F, Coque, TM, et al.High rate of intestinal colonization with extended-spectrum beta-lactamase–producing organisms in household contacts of infected community patients. J Clin Microbiol 2008;46:2796–2799.CrossRefGoogle ScholarPubMed
Arcilla, MS, van Hattem, JM, Haverkate, MR, et al.Import and spread of extended-spectrum β-lactamase–producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis 2017;17:78–85.CrossRefGoogle ScholarPubMed
Kurz, MSE, Bayingana, C, Ndoli, JM, et al.Intense pre-admission carriage and further acquisition of ESBL-producing Enterobacteriaceae among patients and their caregivers in a tertiary hospital in Rwanda. Trop Med Int Health 2017;22:210–220.CrossRefGoogle Scholar
Tandé, D, Boisramé-Gastrin, S, Münck, MR, et al.Intrafamilial transmission of extended-spectrum beta-lactamase–producing Escherichia coli and Salmonella enterica Babelsberg among the families of internationally adopted children. J Antimicrob Chemother 2010;65:859–865.CrossRefGoogle ScholarPubMed
Löhr, IH, Rettedal, S, Natås, OB, et al.Long-term faecal carriage in infants and intrahousehold transmission of CTX-M-15–producing Klebsiella pneumoniae following a nosocomial outbreak. J Antimicrob Chemother 2013;68:1043–1048.CrossRefGoogle Scholar
Haverkate, MR, Platteel, TN, Fluit, AC, et al.Quantifying within-household transmission of extended-spectrum beta-lactamase–producing bacteria. Clin Microbiol Infect 2017;23:46.e1–46.e7.CrossRefGoogle ScholarPubMed
Hilty, M, Betsch, BY, Bögli-Stuber, K, et al.Transmission dynamics of extended-spectrum β-lactamase–producing Enterobacteriaceae in the tertiary care hospital and the household setting. Clin Infect Dis 2012;55:967–975.CrossRefGoogle ScholarPubMed
Bevan, ER, Jones, AM, Hawkey, PM.Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother 2017;72:2145–2155.CrossRefGoogle ScholarPubMed
van Duijkeren, E, Wielders, CCH, Dierikx, CM, et al.Long-term carriage of extended-spectrum beta-lactamase–producing Escherichia coli and Klebsiella pneumoniae in the general population in The Netherlands. Clin Infect Dis 2018;66:1368–1376.CrossRefGoogle ScholarPubMed
Kronenberg, A, Hilty, M, Endimiani, A, et al.Temporal trends of extended-spectrum cephalosporin-resistant Escherichia coli and Klebsiella pneumoniae isolates in in- and outpatients in Switzerland, 2004 to 2011. Euro Surveill 2013;18(21). pii: 20484.Google ScholarPubMed
Castillo García, FJ, Seral García, C, Pardos De la Gandara, M, et al.Prevalence of fecal carriage of ESBL-producing Enterobacteriaceae in hospitalized and ambulatory patients during two nonoutbreak periods. Eur J Clin Microbiol Infect Dis 2007;26:77–78.CrossRefGoogle Scholar
Galas, M, Decousser, J-W, Breton, N, et al.Nationwide study of the prevalence, characteristics, and molecular epidemiology of extended-spectrum β-lactamase–producing Enterobacteriaceae in France. Antimicrob Agents Chemother 2008;52:786–789.CrossRefGoogle ScholarPubMed
Ulstad, CR, Solheim, M, Berg, S, et al.Carriage of ESBL/AmpC-producing or ciprofloxacin nonsusceptible Escherichia coli and Klebsiella spp in healthy people in Norway. Antimicrob Resist Infect Control 2016;5:57. doi: 10.1186/s13756-016-0156-x.CrossRefGoogle ScholarPubMed
Johnson, JR, Davis, G, Clabots, C, et al.Household clustering of Escherichia coli sequence type 131 clinical and fecal isolates according to whole genome sequence analysis. Open Forum Infect Dis 2016;3:ofw129.CrossRefGoogle ScholarPubMed
Zingg, W, Huttner, B, Ginet, C, et al. Period vs point prevalence—what is the difference? In: Program and abstracts of the 2nd International Conference on Prevention and Infection Control (ICPIC 2013); June 25–28, 2013; Geneva, Switzerland. Abstract 222.CrossRefGoogle Scholar
Ruppé, E, Olearo, F, Pires, D, et al.Clonal or not clonal? Investigating hospital outbreaks of KPC-producing Klebsiella pneumoniae with whole-genome sequencing. Clin Microbiol Infect 2017;23:470–475.CrossRefGoogle ScholarPubMed
Gurieva, T, Dautzenberg, MJD, Gniadkowski, M, et al.The transmissibility of antibiotic-resistant Enterobacteriaceae in intensive care units. Clin Infect Dis 2018;66:489–493.CrossRefGoogle ScholarPubMed
Schaufler, K, Semmler, T, Wieler, LH, et al.Genomic and functional analysis of emerging virulent and multidrug-resistant Escherichia coli lineage sequence type 648. Antimicrob Agents Chemother 2019;63(6). pii: e00243-19. doi: 10.1128/AAC.00243-19.CrossRefGoogle ScholarPubMed
Supplementary material: File

Martischang et al. supplementary material

Martischang et al. supplementary material

Download Martischang et al. supplementary material(File)
File 149.9 KB