Prevalence, genetic diversity of and factors associated with ESBL-producing Enterobacterales carriage in residents of French nursing homes

doi:10.1016/j.jhin.2019.12.008

Journal of Hospital Infection

Volume 104, Issue 4, April 2020, Pages 469-475

https://doi.org/10.1016/j.jhin.2019.12.008 Get rights and content

Summary

Objective

To determine the prevalence and genotypic characteristics of extended-spectrum β-lactamase-producing Enterobacterales (ESBLE) and carbapenemase-producing Enterobacterales (CPE) in nursing homes (NHs) in a French region. Risk factors associated with their carriage were also investigated.

Methods

A point-prevalence survey was proposed from November 2017 to June 2018 to NHs in the study region. Volunteer residents were screened for ESBLE and CPE carriage. Escherichia coli and Klebsiella pneumoniae isolates were genotyped using multi-locus sequence typing, pulsed-field gel electrophoresis (PFGE) and phylogrouping (for E. coli alone). Collective and individual data were analysed by random-effects logistic regression.

Results

The study was conducted in 18 NHs and included 262 patients. Fifty-two patients (19.8%) carried at least one ESBLE, corresponding to 56 isolates (42 E. coli, 11 K. pneumoniae and three others), while no CPE was detected. The majority (27/42) of ESBL E. coli belonged to phylogroup B2, and ST131 was over-represented in this subset (21/27). PFGE analysis revealed ST131 cross-transmission within NHs. Regarding ESBL K. pneumoniae, nine of 11 isolates belonged to ST663, and PFGE suggested diffusion of the clone in six NHs. Significant individual risk factors for colonization by ESBLE were: use of a shared bathroom, previous antibiotic use and recent history of hospitalization. Significant collective protective factors were proper compliance with glove use and support of the NH by a healthcare facility.

Conclusion

This study shows that NHs in the study region are an important reservoir of ESBLE, whereas no residents were CPE carriers. The control of ESBLE in NHs should focus on antibiotic stewardship and excreta management policies.

Introduction

Antimicrobial resistance is a worldwide problem and is projected to surpass cancer as the leading cause of death by 2050 [1]. Of particular interest, extended-spectrum β-lactamase-producing Enterobacterales (ESBLE) has become a major European public health concern in the last two decades [2]. For instance, the incidence of infections caused by ESBLE has increased dramatically in French hospitals, and Escherichia coli has become the most common species among ESBLE (60%), before Klebsiella pneumoniae (25%) [3]. There is rising concern regarding nursing homes (NHs) which are considered as reservoirs of ESBLE, because the residents frequently require medical care and antimicrobial treatments [4]. In addition, the recent emergence of carbapenemase-producing Enterobacterales (CPE) represents a significant worldwide threat to public health, and some studies from southern Europe have reported significant prevalence of CPE carriage in residents of NHs or long-term care facilities [5,6]. However, the prevalence of ESBLE and CPE carriage among residents of French NHs remains poorly described. In this context, the objective of this study was to assess the prevalence of ESBLE and CPE carriage in residents of NHs of Franche-Comté, a region in eastern France. In addition, the molecular characteristics of these multi-drug-resistant isolates were investigated, as well as collective and individual risk factors associated with their carriage.

Section snippets

Study design, setting and participants

A cross-sectional prevalence survey was performed from November 2017 to June 2018 in NHs in Franche-Comté. A two-stage random sampling method was used. Fifty NHs were selected at random from the 135 NHs eligible to participate in the study. Between 20 and 35 residents, depending on housing capacity, were selected at random from each of these 50 NHs. Residents who were unable to express their agreement to participate were excluded. Individual residents who agreed to participate in the study were

Participation

Of the 50 NHs randomized, 18 (36.0%) agreed to participate in the study. In these NHs, 776 residents met the inclusion criteria. After randomization and recording their agreement to participate, 262 residents, with complete data and samples, were included, representing an average of 14.5 residents per NH (range 3–33). The flow chart of the study is presented in Figure 1. Data collected on NHs and residents are displayed in Table I, Table II, respectively.

Microbiological analysis

Fifty-two of the residents [19.8%, 95%

Discussion

This study shows that NHs in the study region are an important reservoir of ESBLE, with almost 20% carriage amongst residents. This figure is in line with the pooled prevalence of ESBLE reported by Flokas et al. in their systematic review (i.e. 18% in European NHs) despite considerable geographical variability [11]. Huge variability was observed within NHs included in this study, mainly due to intra-NH outbreaks of pandemic clonal group ST131. This survey revealed occult outbreaks of

Acknowledgements

The authors wish to thank all the NHs, healthcare workers and residents for their participation in this study.

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Prevalence, genetic diversity of and factors associated with ESBL-producing Enterobacterales carriage in residents of French nursing homes

Summary

Objective

Methods

Results

Conclusion

Introduction

Section snippets

Study design, setting and participants

Participation

Microbiological analysis

Discussion

Acknowledgements

Lancet Infect Dis

Int J Antimicrob Agents

Int J Antimicrob Agents

J Hosp Infect

Review on antimicrobial resistance. Antimicrobial resistance: tackling a crisis for the health and wealth of nations

National multidrug-resistant bacteria (MDRB) surveillance in France through the RAISIN network: a 9 year experience

J Antimicrob Chemother

Extensive dissemination of extended spectrum beta-lactamase-producing Enterobacteriaceae in a Dutch nursing home

Infect Control Hosp Epidemiol

A single-day point-prevalence study of faecal carriers in long-term care hospitals in Madrid (Spain) depicts a complex clonal and polyclonal dissemination of carbapenemase-producing Enterobacteriaceae

J Antimicrob Chemother

Colonization of long-term care facility residents in three Italian provinces by multidrug-resistant bacteria

Antimicrob Resist Infect Control

Wastewater treatment plants release large amounts of extended-spectrum beta-lactamase-producing Escherichia coli into the environment

Clin Infect Dis

The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups

Environ Microbiol Rep

Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates

J Clin Microbiol