Emergence of Escherichia coli ST131 carrying carbapenemase genes, European Union/European Economic Area, August 2012 to May 2024

doi:10.2807/1560-7917.ES.2024.29.47.2400727

. 2024 Nov;29(47):2400727.

doi: 10.2807/1560-7917.ES.2024.29.47.2400727.

Emergence of Escherichia coli ST131 carrying carbapenemase genes, European Union/European Economic Area, August 2012 to May 2024

Anke Kohlenberg¹, Olov Svartström¹, Petra Apfalter², Rainer Hartl², Pierre Bogaerts³, Te-Din Huang³, Katerina Chudejova⁴, Lucia Malisova^{5

6}, Jessica Eisfeld⁷, Mirco Sandfort⁸, Anette M Hammerum⁹, Louise Roer⁹, Kati Räisänen¹⁰, Laurent Dortet^{11

12}, Rémy A Bonnin^{11

12}, Ákos Tóth¹³, Kinga Tóth¹³, Christina Clarke¹⁴, Martin Cormican¹⁵, Algirdas Griškevičius¹⁶, Kirstin Khonyongwa¹⁷, Marie Meo¹⁷, Baiba Niedre-Otomere¹⁸, Reinis Vangravs¹⁸, Antoni Pa Hendrickx¹⁹, Daan W Notermans¹⁹, Ørjan Samuelsen²⁰, Manuela Caniça²¹, Vera Manageiro²¹, Vilhelm Müller²², Barbro Mäkitalo²², Urška Kramar²³, Mateja Pirs²⁴, Daniel Palm¹, Dominique L Monnet¹, Erik Alm¹, Marius Linkevicius¹

Affiliations

¹ European Centre for Disease Prevention and Control, Stockholm, Sweden.
² Austrian National Reference Centre for Antimicrobial Resistance, Ordensklinikum Linz Elisabethinen, Linz, Austria.
³ National Reference Centre for Antimicrobic-Resistant Gram-Negative Bacilli, Laboratory of Microbiology, CHU UCL Namur, Yvoir, Belgium.
⁴ Department of Microbiology, Faculty of Medicine, University Hospital in Pilsen, Charles University, Pilsen, Czechia.
⁵ National Reference Laboratory for Antibiotics, National Institute of Public Health, Prague, Czechia.
⁶ Department of Microbiology, 3rd Faculty of Medicine, Charles University, University Hospital Kralovske Vinohrady and National Institute of Public Health, Prague, Czechia.
⁷ German National Reference Centre for Multidrug-resistant Gram-negative Bacteria, Department of Medical Microbiology, Ruhr-University Bochum, Bochum, Germany.
⁸ Department of Infectious Disease Epidemiology, Robert Koch Institute, Berlin, Germany.
⁹ National Reference Laboratory for Antimicrobial Resistance, Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark.
¹⁰ Finnish Institute for Health and Welfare, Helsinki, Finland.
¹¹ Associated French National Reference Centre for Antibiotic Resistance: Carbapenemase-Producing Enterobacteriaceae, Le Kremlin-Bicêtre, France.
¹² Team "Resist" UMR1184 "Immunology of Viral, Auto-Immune, Hematological and Bacterial diseases (IMVA-HB)", INSERM, Université Paris-Saclay, CEA, IHU Prometheus Faculty of Medicine, Le Kremlin-Bicêtre, France.
¹³ National Centre for Public Health and Pharmacy, Budapest, Hungary.
¹⁴ Galway Reference Laboratory Service, Galway University Hospital, Galway, Ireland.
¹⁵ School of Medicine, University of Galway, Galway, Ireland.
¹⁶ National Public Health Surveillance Laboratory, Vilnius, Lithuania.
¹⁷ Service Bactériologie-Mycologie-Antibiorésistance-Hygiène Hospitalière, Département de Microbiologie, Laboratoire National de Santé, Dudelange, Luxembourg.
¹⁸ National Microbiology Reference Laboratory of Latvia, Laboratory "Latvian Centre of Infectious Diseases", Laboratory Service, Riga East University Hospital, Riga, Latvia.
¹⁹ Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.
²⁰ Norwegian National Advisory Unit on Detection of Antimicrobial Resistance, Department of Microbiology and Infection Control, University Hospital of North Norway, Tromsø, Norway.
²¹ National Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr Ricardo Jorge, Lisbon, Portugal.
²² Public Health Agency of Sweden, Solna, Sweden.
²³ National Laboratory of Health, Environment and Food, Centre for Medical Microbiology, Maribor, Slovenia.
²⁴ Institute of Microbiology and Immunology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia.

PMID: 39574387
PMCID: PMC11583312
DOI: 10.2807/1560-7917.ES.2024.29.47.2400727

Emergence of Escherichia coli ST131 carrying carbapenemase genes, European Union/European Economic Area, August 2012 to May 2024

Anke Kohlenberg et al. Euro Surveill. 2024 Nov.

. 2024 Nov;29(47):2400727.

doi: 10.2807/1560-7917.ES.2024.29.47.2400727.

Authors

Affiliations

¹ European Centre for Disease Prevention and Control, Stockholm, Sweden.
² Austrian National Reference Centre for Antimicrobial Resistance, Ordensklinikum Linz Elisabethinen, Linz, Austria.
³ National Reference Centre for Antimicrobic-Resistant Gram-Negative Bacilli, Laboratory of Microbiology, CHU UCL Namur, Yvoir, Belgium.
⁴ Department of Microbiology, Faculty of Medicine, University Hospital in Pilsen, Charles University, Pilsen, Czechia.
⁵ National Reference Laboratory for Antibiotics, National Institute of Public Health, Prague, Czechia.
⁶ Department of Microbiology, 3rd Faculty of Medicine, Charles University, University Hospital Kralovske Vinohrady and National Institute of Public Health, Prague, Czechia.
⁷ German National Reference Centre for Multidrug-resistant Gram-negative Bacteria, Department of Medical Microbiology, Ruhr-University Bochum, Bochum, Germany.
⁸ Department of Infectious Disease Epidemiology, Robert Koch Institute, Berlin, Germany.
⁹ National Reference Laboratory for Antimicrobial Resistance, Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark.
¹⁰ Finnish Institute for Health and Welfare, Helsinki, Finland.
¹¹ Associated French National Reference Centre for Antibiotic Resistance: Carbapenemase-Producing Enterobacteriaceae, Le Kremlin-Bicêtre, France.
¹² Team "Resist" UMR1184 "Immunology of Viral, Auto-Immune, Hematological and Bacterial diseases (IMVA-HB)", INSERM, Université Paris-Saclay, CEA, IHU Prometheus Faculty of Medicine, Le Kremlin-Bicêtre, France.
¹³ National Centre for Public Health and Pharmacy, Budapest, Hungary.
¹⁴ Galway Reference Laboratory Service, Galway University Hospital, Galway, Ireland.
¹⁵ School of Medicine, University of Galway, Galway, Ireland.
¹⁶ National Public Health Surveillance Laboratory, Vilnius, Lithuania.
¹⁷ Service Bactériologie-Mycologie-Antibiorésistance-Hygiène Hospitalière, Département de Microbiologie, Laboratoire National de Santé, Dudelange, Luxembourg.
¹⁸ National Microbiology Reference Laboratory of Latvia, Laboratory "Latvian Centre of Infectious Diseases", Laboratory Service, Riga East University Hospital, Riga, Latvia.
¹⁹ Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.
²⁰ Norwegian National Advisory Unit on Detection of Antimicrobial Resistance, Department of Microbiology and Infection Control, University Hospital of North Norway, Tromsø, Norway.
²¹ National Reference Laboratory of Antibiotic Resistances and Healthcare Associated Infections, Department of Infectious Diseases, National Institute of Health Dr Ricardo Jorge, Lisbon, Portugal.
²² Public Health Agency of Sweden, Solna, Sweden.
²³ National Laboratory of Health, Environment and Food, Centre for Medical Microbiology, Maribor, Slovenia.
²⁴ Institute of Microbiology and Immunology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia.

PMID: 39574387
PMCID: PMC11583312
DOI: 10.2807/1560-7917.ES.2024.29.47.2400727

Abstract

Analysis of 594 isolates of Escherichia coli sequence type (ST)131 and its single locus variants carrying carbapenemase genes from 17 European Union/European Economic Area countries revealed acquisition of 18 carbapenemase variants, mainly in ST131 clades A and C. Most frequent were bla _OXA-244 (n = 230) and bla _OXA-48 (n = 224), detected in 14 and 12 countries, respectively. Isolates carrying bla _OXA-244 have increased rapidly since 2021. The increasing detection of carbapenemase genes in the E. coli high-risk lineage ST131 is a public health concern.

Keywords: Carbapenem-resistant Enterobacterales; Escherichia coli; antibiotics; antimicrobial resistance; carbapenemase; cross-border spread; surveillance; whole genome sequencing.

PubMed Disclaimer

Conflict of interest statement

Conflict of interest: None declared.

Figures

**Figure 1**
Number of *Escherichia coli* ST131 isolates, including its single locus variants^a, carrying carbapenemase genes, by year, EU/EEA, 2012–2023^b (n = 535)

**Figure 2**
Phylogenetic tree of *Escherichia coli* ST131 isolates, including its single locus variants included in the genomic relatedness analysis, EU/EEA and outside, 2005–2024 (n = 691)

See this image and copyright information in PMC

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References

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1. Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565-91. 10.1128/CMR.00116-14 - DOI - PMC - PubMed
1. Welker S, Boutin S, Miethke T, Heeg K, Nurjadi D. Emergence of carbapenem-resistant ST131 Escherichia coli carrying bla OXA-244 in Germany, 2019 to 2020. Euro Surveill. 2020;25(46):2001815. 10.2807/1560-7917.ES.2020.25.46.2001815 - DOI - PMC - PubMed
1. Piazza A, Corbella M, Mattioni Marchetti V, Merla C, Mileto I, Kuka A, et al. Clinical isolates of ST131 blaOXA-244-positive Escherichia coli, Italy, December 2022 to July 2023. Euro Surveill. 2024;29(8):2400073. 10.2807/1560-7917.ES.2024.29.8.2400073 - DOI - PMC - PubMed
1. Patiño-Navarrete R, Rosinski-Chupin I, Cabanel N, Zongo PD, Héry M, Oueslati S, et al. Specificities and Commonalities of Carbapenemase-Producing Escherichia coli Isolated in France from 2012 to 2015. mSystems. 2022;7(1):e0116921. 10.1128/msystems.01169-21 - DOI - PMC - PubMed

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[1] 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. 10.1016/S0140-6736(21)02724-0 - DOI - PMC - PubMed

[2] 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. 10.1016/S0140-6736(21)02724-0 - DOI - PMC - PubMed

[3] Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565-91. 10.1128/CMR.00116-14 - DOI - PMC - PubMed

[4] Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565-91. 10.1128/CMR.00116-14 - DOI - PMC - PubMed

[5] Welker S, Boutin S, Miethke T, Heeg K, Nurjadi D. Emergence of carbapenem-resistant ST131 Escherichia coli carrying bla OXA-244 in Germany, 2019 to 2020. Euro Surveill. 2020;25(46):2001815. 10.2807/1560-7917.ES.2020.25.46.2001815 - DOI - PMC - PubMed

[6] Welker S, Boutin S, Miethke T, Heeg K, Nurjadi D. Emergence of carbapenem-resistant ST131 Escherichia coli carrying bla OXA-244 in Germany, 2019 to 2020. Euro Surveill. 2020;25(46):2001815. 10.2807/1560-7917.ES.2020.25.46.2001815 - DOI - PMC - PubMed

[7] Piazza A, Corbella M, Mattioni Marchetti V, Merla C, Mileto I, Kuka A, et al. Clinical isolates of ST131 blaOXA-244-positive Escherichia coli, Italy, December 2022 to July 2023. Euro Surveill. 2024;29(8):2400073. 10.2807/1560-7917.ES.2024.29.8.2400073 - DOI - PMC - PubMed

[8] Piazza A, Corbella M, Mattioni Marchetti V, Merla C, Mileto I, Kuka A, et al. Clinical isolates of ST131 blaOXA-244-positive Escherichia coli, Italy, December 2022 to July 2023. Euro Surveill. 2024;29(8):2400073. 10.2807/1560-7917.ES.2024.29.8.2400073 - DOI - PMC - PubMed

[9] Patiño-Navarrete R, Rosinski-Chupin I, Cabanel N, Zongo PD, Héry M, Oueslati S, et al. Specificities and Commonalities of Carbapenemase-Producing Escherichia coli Isolated in France from 2012 to 2015. mSystems. 2022;7(1):e0116921. 10.1128/msystems.01169-21 - DOI - PMC - PubMed

[10] Patiño-Navarrete R, Rosinski-Chupin I, Cabanel N, Zongo PD, Héry M, Oueslati S, et al. Specificities and Commonalities of Carbapenemase-Producing Escherichia coli Isolated in France from 2012 to 2015. mSystems. 2022;7(1):e0116921. 10.1128/msystems.01169-21 - DOI - PMC - PubMed

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Emergence of Escherichia coli ST131 carrying carbapenemase genes, European Union/European Economic Area, August 2012 to May 2024

Affiliations

Emergence of Escherichia coli ST131 carrying carbapenemase genes, European Union/European Economic Area, August 2012 to May 2024

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