Dissemination of extensively drug-resistant NDM-producing Providencia stuartii in Europe linked to patients transferred from Ukraine, March 2022 to March 2023

Author:

Witteveen Sandra1ORCID,Hans Jörg B23ORCID,Izdebski Radosław4ORCID,Hasman Henrik5ORCID,Samuelsen Ørjan67ORCID,Dortet Laurent8ORCID,Pfeifer Yvonne9,Delappe Niall10,Oteo-Iglesias Jesús11ORCID,Żabicka Dorota12ORCID,Cormican Martin10ORCID,Sandfort Mirco2ORCID,Reichert Felix2ORCID,Pöntinen Anna K137ORCID,Fischer Martin A9ORCID,Verkaik Nelianne14ORCID,Pérez-Vazquez María11ORCID,Pfennigwerth Niels3ORCID,Hammerum Anette M5ORCID,Hallstrøm Søren5ORCID,Biedrzycka Marta4ORCID,Räisänen Kati15ORCID,Wielders Cornelia CH1ORCID,Urbanowicz Paweł4ORCID,de Haan Angela1,Westmo Karin16,Landman Fabian1,van der Heide Han GJ1,Lansu Simon1ORCID,Zwittink Romy D1ORCID,Notermans Daan W1ORCID,Guzek Aneta17ORCID,Kondratiuk Viacheslav18ORCID,Salmanov Aidyn19ORCID,Haller Sebastian2ORCID,Linkevicius Marius20ORCID,Gatermann Sören3,Kohlenberg Anke20,Gniadkowski Marek4ORCID,Werner Guido9ORCID,Hendrickx Antoni PA1ORCID

Affiliation:

1. Centre for Infectious Disease Control (CIb), National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands

2. Department for Infectious Disease Epidemiology, Robert Koch Institute, Berlin, Germany

3. German National Reference Centre for Multidrug-Resistant Gram-Negative Bacteria, Department of Medical Microbiology, Ruhr-University Bochum, Bochum, Germany

4. Departement of Molecular Microbiology, National Medicines Institute, Warsaw, Poland

5. National Reference Laboratory for Antimicrobial Resistance, Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark

6. Department of Pharmacy, Faculty of Health Sciences, UiT The Arctic University of Norway, Tromsø, Norway

7. Norwegian National Advisory Unit on Detection of Antimicrobial Resistance, Department of Microbiology and Infection Control, University Hospital of North Norway, Tromsø, Norway

8. French National Reference Center for Antimicrobial Resistance, INSERM UMR 1184, Paris-Saclay University, Bicêtre Hospital, Assistance Publique des Hôpitaux de Paris, Paris, France

9. Division of Nosocomial Pathogens and Antibiotic Resistances, Department of Infectious Diseases, Robert Koch Institute, Wernigerode Branch, Wernigerode, Germany

10. University of Galway, Galway, Ireland

11. Reference and Research Laboratory on Antibiotic Resistance of the National Center for Microbiology and CIBERINFEC, Instituto de Salud Carlos III, Madrid, Spain

12. Departement of Epidemiology and Clinical Microbiology, National Medicines Institute, Warsaw, Poland

13. Department of Biostatistics, Faculty of Medicine, University of Oslo, Oslo, Norway

14. Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, the Netherlands

15. Department of Health Security, Finnish Institute for Health and Welfare, Helsinki, Finland

16. Department of Microbiology, Public Health Agency of Sweden, Solna, Sweden

17. Department of Laboratory Diagnostics, Section of Microbiology, Military Institute of Medicine - National Research Institute, Warsaw, Poland

18. National Pirogov Memorial University, Vinnytsia, Ukraine

19. Shupyk National Healthcare University of Ukraine, Kyiv, Ukraine

20. European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden

Abstract

Background The war in Ukraine led to migration of Ukrainian people. Early 2022, several European national surveillance systems detected multidrug-resistant (MDR) bacteria related to Ukrainian patients. Aim To investigate the genomic epidemiology of New Delhi metallo-β-lactamase (NDM)-producing Providencia stuartii from Ukrainian patients among European countries. Methods Whole-genome sequencing of 66 isolates sampled in 2022–2023 in 10 European countries enabled whole-genome multilocus sequence typing (wgMLST), identification of resistance genes, replicons, and plasmid reconstructions. Five bla NDM-1-carrying-P. stuartii isolates underwent antimicrobial susceptibility testing (AST). Transferability to Escherichia coli of a bla NDM-1-carrying plasmid from a patient strain was assessed. Epidemiological characteristics of patients with NDM-producing P. stuartii were gathered by questionnaire. Results wgMLST of the 66 isolates revealed two genetic clusters unrelated to Ukraine and three linked to Ukrainian patients. Of these three, two comprised bla NDM-1-carrying-P. stuartii and the third bla NDM-5-carrying-P. stuartii. The bla NDM-1 clusters (PstCluster-001, n = 22 isolates; PstCluster-002, n = 8 isolates) comprised strains from seven and four countries, respectively. The bla NDM-5 cluster (PstCluster-003) included 13 isolates from six countries. PstCluster-001 and PstCluster-002 isolates carried an MDR plasmid harbouring bla NDM-1, bla OXA-10, bla CMY-16, rmtC and armA, which was transferrable in vitro and, for some Ukrainian patients, shared by other Enterobacterales. AST revealed PstCluster-001 isolates to be extensively drug-resistant (XDR), but susceptible to cefiderocol and aztreonam–avibactam. Patients with data on age (n = 41) were 19–74 years old; of 49 with information on sex, 38 were male. Conclusion XDR P. stuartii were introduced into European countries, requiring increased awareness and precautions when treating patients from conflict-affected areas.

Publisher

European Centre for Disease Control and Prevention (ECDC)

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