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Abstract

In 2016–2019, hospital A’s haematology ward experienced an outbreak of OXA-48-producing ST-22 strains, with toilets identified as source of transmission. Between 2020 and 2022, 28 strains of OXA-48-producing ST-22 were isolated on other wards. This study aimed to determine whether all OXA-48-producing ST-22 strains belonged to the same clone and to investigate the persistence of this clone using whole genome sequencing. OXA-48-producing ST-22 strains collected from patients (n = 33) and from the hospital environment (n = 20) of seven wards were sequenced using Illumina technology and clonal relationships were determined using single nucleotide polymorphism (SNP). Phylogenetic analyses were performed on 53 strains from hospital A and on 240 epidemiologically unrelated carbapenem-resistant ST-22 isolated from elsewhere in France. SNP analysis suggested long-lasting persistence of the same clone for more than 6 years. Phylogenetic analysis showed that 52 of 53 strains isolated in hospital A belonged to the same cluster and were different from the 240 epidemiologically unrelated ST-22. Our data suggest that this clone can persist in hospital environments for years, representing a risk for hospital-acquired infections and outbreaks. Reservoir management is essential to prevent further transmission.

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/content/10.2807/1560-7917.ES.2024.29.49.2400262
2024-12-05
2025-01-08
/content/10.2807/1560-7917.ES.2024.29.49.2400262
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References

  1. European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious Diseases. Stockholm: ECDC. [Accessed: 31 Jul 2024]. Available from: https://atlas.ecdc.europa.eu/public/index.aspx
  2. Falcone M, Tiseo G, Carbonara S, Marino A, Di Caprio G, Carretta A, et al. Mortality Attributable to Bloodstream Infections Caused by Different Carbapenem-Resistant Gram-Negative Bacilli: Results From a Nationwide Study in Italy (ALARICO Network). Clin Infect Dis. 2023;76(12):2059-69.  https://doi.org/10.1093/cid/ciad100  PMID: 36801828 
  3. Willems RPJ, van Dijk K, Vehreschild MJGT, Biehl LM, Ket JCF, Remmelzwaal S, et al. Incidence of infection with multidrug-resistant Gram-negative bacteria and vancomycin-resistant enterococci in carriers: a systematic review and meta-regression analysis. Lancet Infect Dis. 2023;23(6):719-31.  https://doi.org/10.1016/S1473-3099(22)00811-8  PMID: 36731484 
  4. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629-55.  https://doi.org/10.1016/S0140-6736(21)02724-0  PMID: 35065702 
  5. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2018;0(0). PMID: 30409683 
  6. Kim Y, Ko S, Yeon YE, Kim H, Oh C-S, Ahn JK, et al. Genomic and Phenotypic Characterization of a Lytic Bacteriophage CF1 Infecting the Multi-drug Resistant Bacterium Citrobacter freundii. Biotechnol Bioprocess Eng. 2020;25(3):384-93.  https://doi.org/10.1007/s12257-019-0505-8 
  7. Nada T, Baba H, Kawamura K, Ohkura T, Torii K, Ohta M. A small outbreak of third generation cephem-resistant Citrobacter freundii infection on a surgical ward. Jpn J Infect Dis. 2004;57(4):181-2. PMID: 15329453 
  8. Biez L, Bonnin RA, Emeraud C, Birer A, Jousset AB, Naas T, et al. Nationwide molecular epidemiology of carbapenemase-producing Citrobacter spp. in France in 2019 and 2020. MSphere. 2023;8(6):e0036623.  https://doi.org/10.1128/msphere.00366-23  PMID: 37815363 
  9. Jabeen I, Islam S, Hassan AKMI, Tasnim Z, Shuvo SR. A brief insight into Citrobacter species - a growing threat to public health. Front Antibiot. 2023;2:1276982.  https://doi.org/10.3389/frabi.2023.1276982 
  10. Smismans A, Ho E, Daniels D, Ombelet S, Mellaerts B, Obbels D, et al. New environmental reservoir of CPE in hospitals. Lancet Infect Dis. 2019;19(6):580-1.  https://doi.org/10.1016/S1473-3099(19)30230-0  PMID: 31122775 
  11. Räisänen K, Sarvikivi E, Arifulla D, Pietikäinen R, Forsblom-Helander B, Tarkka E, et al. Three clusters of carbapenemase-producing Citrobacter freundii in Finland, 2016-20. J Antimicrob Chemother. 2021;76(10):2697-701.  https://doi.org/10.1093/jac/dkab209  PMID: 34164687 
  12. Lee AS, Dolan L, Jenkins F, Crawford B, van Hal SJ. Active surveillance of carbapenemase-producing Enterobacterales using genomic sequencing for hospital-based infection control interventions. Infect Control Hosp Epidemiol. 2023;1-7. PMID: 37702063 
  13. Kizny Gordon AE, Mathers AJ, Cheong EYL, Gottlieb T, Kotay S, Walker AS, et al. The Hospital Water Environment as a Reservoir for Carbapenem-Resistant Organisms Causing Hospital-Acquired Infections-A Systematic Review of the Literature. Clin Infect Dis. 2017;64(10):1435-44.  https://doi.org/10.1093/cid/cix132  PMID: 28200000 
  14. Hamerlinck H, Aerssens A, Boelens J, Dehaene A, McMahon M, Messiaen A-S, et al. Sanitary installations and wastewater plumbing as reservoir for the long-term circulation and transmission of carbapenemase producing Citrobacter freundii clones in a hospital setting. Antimicrob Resist Infect Control. 2023;12(1):58.  https://doi.org/10.1186/s13756-023-01261-9  PMID: 37337245 
  15. Nurjadi D, Scherrer M, Frank U, Mutters NT, Heininger A, Späth I, et al. Genomic Investigation and Successful Containment of an Intermittent Common Source Outbreak of OXA-48-Producing Enterobacter cloacae Related to Hospital Shower Drains. Microbiol Spectr. 2021;9(3):e0138021.  https://doi.org/10.1128/Spectrum.01380-21  PMID: 34817232 
  16. Jolivet S, Couturier J, Vuillemin X, Gouot C, Nesa D, Adam M, et al. Outbreak of OXA-48-producing Enterobacterales in a haematological ward associated with an uncommon environmental reservoir, France, 2016 to 2019. Euro Surveill. 2021;26(21):2000118.  https://doi.org/10.2807/1560-7917.ES.2021.26.21.2000118  PMID: 34047273 
  17. Haut Conseil de la Santé Publique. Prévention de la transmission croisée des Bactéries Hautement Résistantes aux antibiotiques émergentes (BHRe). [Prevention of cross-transmission of “Emerging Highly Antibiotic-Resistant Bacteria” (EHRB)]. Paris: Haut Conseil de la Santé Publique; 2013. French. Available from: http://www.hcsp.fr/explore.cgi/avisrapportsdomaine?clefr=372
  18. Haut Conseil de la Santé Publique. Actualisation des recommandations relatives aux BHRe. [Updated recommendations for controlling the spread of emerging highly antibiotic-resistant bacteria]. Paris: Haut Conseil de la Santé Publique; 2019. French. Available from: https://www.hcsp.fr/explore.cgi/avisrapportsdomaine?clefr=758
  19. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124.  https://doi.org/10.12688/wellcomeopenres.14826.1  PMID: 30345391 
  20. Emeraud C, Mahamat A, Jousset AB, Bernabeu S, Goncalves T, Pommier C, et al. Emergence and rapid dissemination of highly resistant NDM-14-producing Klebsiella pneumoniae ST147, France, 2022. Euro Surveill. 2023;28(42):2300095.  https://doi.org/10.2807/1560-7917.ES.2023.28.42.2300095  PMID: 37855905 
  21. Gomez-Simmonds A, Annavajhala MK, Wang Z, Macesic N, Hu Y, Giddins MJ, et al. Genomic and Geographic Context for the Evolution of High-Risk Carbapenem-Resistant Enterobacter cloacae Complex Clones ST171 and ST78. MBio. 2018;9(3):e00542-18.  https://doi.org/10.1128/mBio.00542-18  PMID: 29844109 
  22. Neidhöfer C, Sib E, Neuenhoff M, Schwengers O, Dummin T, Buechler C, et al. Hospital sanitary facilities on wards with high antibiotic exposure play an important role in maintaining a reservoir of resistant pathogens, even over many years. Antimicrob Resist Infect Control. 2023;12(1):33.  https://doi.org/10.1186/s13756-023-01236-w  PMID: 37061726 
  23. Kotay S, Chai W, Guilford W, Barry K, Mathers AJ. Spread from the Sink to the Patient: In Situ Study Using Green Fluorescent Protein (GFP)-Expressing Escherichia coli To Model Bacterial Dispersion from Hand-Washing Sink-Trap Reservoirs. Appl Environ Microbiol. 2017;83(8):e03327-16.  https://doi.org/10.1128/AEM.03327-16  PMID: 28235877 
  24. Kotay SM, Parikh HI, Barry K, Gweon HS, Guilford W, Carroll J, et al. Nutrients influence the dynamics of Klebsiella pneumoniae carbapenemase producing enterobacterales in transplanted hospital sinks. Water Res. 2020;176:115707.  https://doi.org/10.1016/j.watres.2020.115707  PMID: 32224328 
  25. Heireman L, Hamerlinck H, Vandendriessche S, Boelens J, Coorevits L, De Brabandere E, et al. Toilet drain water as a potential source of hospital room-to-room transmission of carbapenemase-producing Klebsiella pneumoniae. J Hosp Infect. 2020;106(2):232-9.  https://doi.org/10.1016/j.jhin.2020.07.017  PMID: 32707194 
  26. Boutin S, Scherrer M, Späth I, Kocer K, Heeg K, Nurjadi D. Cross-contamination of carbapenem-resistant Gram-negative bacteria between patients and hospital environment in the first year of a newly built surgical ward. J Hosp Infect. 2023. PMID: 38081456 
  27. Kotay SM, Donlan RM, Ganim C, Barry K, Christensen BE, Mathers AJ. Droplet- Rather than Aerosol-Mediated Dispersion Is the Primary Mechanism of Bacterial Transmission from Contaminated Hand-Washing Sink Traps. Appl Environ Microbiol. 2019;85(2):e01997-18.  https://doi.org/10.1128/AEM.01997-18  PMID: 30367005 
  28. Regev-Yochay G, Margalit I, Smollan G, Rapaport R, Tal I, Hanage WP, et al. Sink-traps are a major source for carbapenemase-producing Enterobacteriaceae transmission. Infect Control Hosp Epidemiol. 2023;1-8. PMID: 38149351 
  29. Lemarié C, Legeay C, Mahieu R, Moal F, Ramont C, Kouatchet A, et al. Long-term contamination of sink drains by carbapenemase-producing Enterobacterales in three intensive care units: characteristics and transmission to patients. J Hosp Infect. 2021;112:16-20.  https://doi.org/10.1016/j.jhin.2021.02.016  PMID: 33636255 
  30. Kearney A, Boyle MA, Curley GF, Humphreys H. Preventing infections caused by carbapenemase-producing bacteria in the intensive care unit - Think about the sink. J Crit Care. 2021;66:52-9.  https://doi.org/10.1016/j.jcrc.2021.07.023  PMID: 34438134 
  31. Fucini G-B, Geffers C, Schwab F, Behnke M, Sunder W, Moellmann J, et al. Sinks in patient rooms in ICUs are associated with higher rates of hospital-acquired infection: a retrospective analysis of 552 ICUs. J Hosp Infect. 2023;139:99-105.  https://doi.org/10.1016/j.jhin.2023.05.018  PMID: 37308060 
Persistence of OXA-48-producing ST-22 Citrobacter freundii in patients and the hospital environment, Paris, France, 2016 to 2022
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Sarah+Jolivet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jolivet Sarah</a>, <a href="/search?value1=Jeanne+Couturier&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Couturier Jeanne</a>, <a href="/search?value1=Killian+Le+Neindre&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Le Neindre Killian</a>, <a href="/search?value1=Muriel+Ehmig&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ehmig Muriel</a>, <a href="/search?value1=Laurent+Dortet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dortet Laurent</a>, <a href="/search?value1=C%C3%A9cile+Emeraud&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Emeraud Cécile</a>, <a href="/search?value1=Fr%C3%A9d%C3%A9ric+Barbut&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Barbut Frédéric</a></span>. Persistence of OXA-48-producing ST-22 Citrobacter freundii in patients and the hospital environment, Paris, France, 2016 to 2022. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(49):pii=2400262. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.49.2400262" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.49.2400262</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 29 Apr 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 15 Aug 2024 </span> </p>
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