Carbapenemase-producing Enterobacterales and vancomycin-resistant Enterococcus faecium carriage in patients who have traveled in foreign countries: A single center 5-year prospective study

Published:February 11, 2022DOI:


      • Patients who travelled abroad without hospitalization.
      • Prevention measures for cross-transmission.
      • Survey of patients at high risk of CPE/VRE carriage.


      Numerous patients carrying carbapenemase-producing Enterobacterales (CPE) and/or vancomycin-resistant Enterococcus faecium (VRE) in France have previously travelled abroad. The risk of spreading CPE/VRE by patients who have stayed abroad without hospitalization is underexplored. This prompted us to screen and isolate all patients who travelled abroad in the previous 12 months upon admission to our hospital. Our aim was to evaluate the efficiency of this CPE/VRE-related risk policy.


      From 2014 to 2018, patients who had travelled abroad in the previous year before their admission underwent microbiological screening and were pre-emptively isolated. Contact precautions were verified and CPE/VRE cross-transmission events investigated.


      Among 1,780 screened patients, 59 (3.3%) were colonized with CPE and/or VRE, of whom 17 (29.3%) were not hospitalized abroad. Nine generated 18 readmissions. No episodes of CPE/VRE cross-transmission were related to patients with a stay abroad without hospitalization, whereas 2 patients hospitalized abroad generated one episode each, despite implementation of contact precautions reaching values from 73.6% to 87.5%.


      Throughout 17 admissions and 18 readmissions, patients who stayed abroad without hospitalization represented a true risk of spreading CPE/VRE, without generating cross-transmission.


      Our strategy of CPE/VRE-related risk policy is successful.

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        • Schwaber MJ
        • Klarfeld-Lidji S
        • Navon-Venezia S
        • Schwartz D
        • Leavitt A
        • Carmeli Y.
        Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality.
        Antimicrob Agents Chemother. 2008; 52: 1028-1033
        • Zarkotou O
        • Pournaras S
        • Tselioti P
        • et al.
        Predictors of mortality in patients with bloodstream infections caused by KPC-producing Klebsiella pneumoniae and impact of appropriate antimicrobial treatment.
        Clin Microbiol Infect. 2011; 17: 1798-1803
        • Song X
        • Srinivasan A
        • Plaut D
        • Perl TM.
        Effect of nosocomial vancomycin-resistant enterococcal bacteremia on mortality, length of stay, and costs.
        Infect Control Hosp Epidemiol. 2003; 24: 251-256
        • Brolund A
        • Lagerqvist N
        • Byfors S
        • et al.
        Worsening epidemiological situation of carbapenemase-producing Enterobacteriaceae in Europe, assessment by national experts from 37 countries, July 2018.
        Euro Surveill. 2019; 241900123
        • Pfaller MA
        • Cormican M
        • Flamm RK
        • Mendes RE
        • Jones RN.
        Temporal and geographic variation in antimicrobial susceptibility and resistance patterns of enterococci: results from the SENTRY antimicrobial surveillance program, 1997-2016.
        Open Forum Infect Dis. 2019; 6: S54-S62
        • Gambarotto K
        • Ploy MC
        • Turlure P
        • et al.
        Prevalence of vancomycin-resistant enterococci in fecal samples from hospitalized patients and nonhospitalized controls in a cattle-rearing area of France.
        J Clin Microbiol. 2000; 38: 620-624
        • Tran DM
        • Larsson M
        • Olson L
        • et al.
        High prevalence of colonisation with carbapenem-resistant Enterobacteriaceae among patients admitted to Vietnamese hospitals: risk factors and burden of disease.
        J Infect. 2019; 79: 115-122
      1. Anonymous. Summary of the latest data on antibiotic resistance in the European Union. EARS-Net surveillance data 2017. Accessed October 1, 2020.

      2. Anonymous. Maîtrise de la diffusion des BMR importées en France par des patients rapatriés ou ayant des antécédents d'hospitalisation à l’étranger. CsSP, Haut Conseil de la Santé Publique. 2010. Accessed October 1, 2020.

        • Ergani-Ozcan A
        • Naas T
        • Baysan BO
        • et al.
        Nosocomial outbreak of vancomycin-resistant Enterococcus faecium in a paediatric unit at a Turkish university hospital.
        J Antimicrob Chemother. 2008; 61: 1033-1039
        • Lerner A
        • Adler A
        • Abu-Hanna J
        • Cohen Percia S
        • Kazma Matalon M
        • Carmeli Y
        Spread of KPC-producing carbapenem-resistant Enterobacteriaceae: the importance of super-spreaders and rectal KPC concentration.
        Clin Microbiol Infect. 2015; 21 (470.e1-7)
      3. Anonymous. Circulaire N°DGS/RI/DGOS/PF/2010/413 du 6 décembre 2010 relative à la mise en œuvre de mesure de contrôles des cas importés d'entérobactéries productrices de carbapénèmases (EPC). Ministère du Travail, de l'Emploi et de la Santé. Accessed October 1, 2020.

      4. Anonymous. Prévention de la transmission croisée des Bactéries Hautement Résistantes aux antibiotiques émergentes (BHRe). Haut Conseil de la Santé Publique. 2013. Accessed October 1, 2020.

      5. Anonymous. InVS. Episodes impliquant des entérobactéries productrices de carbapénèmases en France: Situation épidémiologique du 1er avril 2013. Accessed September 1, 2020.

      6. Anonymous. Facility Guidance for Control of Carbapenem-resistant Enterobacteriaceae (CRE). Accessed December 1, 2020.

        • Magiorakos A.P.
        • Burns K.
        • Rodríguez Baño J.
        • et al.
        Infection prevention and control measures and tools for the prevention of entry of carbapenem-resistant Enterobacteriaceae into healthcare settings: guidance from the European Centre for Disease Prevention and Control.
        Antimicrob Resist Infect Control. 2017; 6: 113
      7. Anonymous. Actualisation des recommandations relatives à la maîtrise de la diffusion des bactéries hautement résistantes aux antibiotiques émergentes (BHRe). Haut Conseil de la Santé Publique. 2019. Accessed October 1, 2020.

        • Jolivet S
        • Vaillant L
        • Poncin T
        • et al.
        Prevalence of carriage of extended-spectrum β-lactamase-producing enterobacteria and associated factors in a French hospital.
        Clin Microbiol Infect. 2018; 24: 1311-1314
        • Fournier S
        • Desenfant L
        • Monteil C
        • Nion-Huang M
        • Richard C
        • Jarlier V
        • The Ap-Hp Outbreaks Control Group
        Efficiency of different control measures for preventing carbapenemase-producing enterobacteria and glycopeptide-resistant Enterococcus faecium outbreaks: a 6-year prospective study in a French multihospital institution, January 2010 to December 2015.
        Euro Surveill. 2018; 23
        • Dortet L
        • Poirel L
        • Nordmann P.
        Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria.
        Biomed Res Int. 2014; (2014:249856)
        • Dortet L
        • Cuzon G
        • Ponties V
        • Nordmann P.
        Trends in carbapenemase-producing Enterobacteriaceae, France, 2012 to 2014.
        Euro Surveill. 2017; 22: 30461
      8. Siegel JD, Rhinehart E, Jackson M, Chiarello L, Healthcare Infection Control Practices Advisory Committee. Guideline for isolation precautions: preventing transmission of infectious agents in healthcare settings. Accessed September 1, 2020.

        • Weber DJ
        • Sickbert-Bennett EE
        • Brown VM
        • et al.
        Compliance with isolation precautions at a university hospital.
        Infect Control Hosp Epidemiol. 2007; 28: 358-361
        • Chitnis AS
        • Caruthers PS
        • Rao AK
        • et al.
        Outbreak of carbapenem-resistant enterobacteriaceae at a long-term acute care hospital: sustained reductions in transmission through active surveillance and targeted interventions.
        Infect Control Hosp Epidemiol. 2012; 33: 984-992
        • Birgand G
        • Leroy C
        • Nerome S
        • et al.
        Costs associated with implementation of a strict policy for controlling spread of highly resistant microorganisms in France.
        BMJ Open. 2016; 6e009029
        • Mairi A
        • Pantel A
        • Ousalem F
        • Sotto A
        • Touati A
        • Lavigne JP.
        OXA-48-producing Enterobacterales in different ecological niches in Algeria: clonal expansion, plasmid characteristics and virulence traits.
        J Antimicrob Chemother. 2019; 74: 1848-1855
        • Kluytmans-van den Bergh MF
        • Verhulst C
        • Willemsen LE
        • Verkade E
        • Bonten MJ
        • Kluytmans JA.
        Rectal carriage of extended-spectrum-Beta-Lactamase-Producing enterobacteriaceae in hospitalized patients: selective preenrichment increases yield of screening.
        J Clin Microbiol. 2015; 53: 2709-2712