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

Sandra Witteveen; Jörg B. Hans; Radosław Izdebski; Henrik Hasman; Ørjan Samuelsen; Laurent Dortet; Yvonne Pfeifer; Niall Delappe; Jesús Oteo-Iglesias; Dorota Żabicka; Martin Cormican; Mirco Sandfort; Felix Reichert; Anna K. Pöntinen; Martin A. Fischer; Nelianne Verkaik; María Pérez-Vazquez; Niels Pfennigwerth; Anette M. Hammerum; Søren Hallstrøm; Marta Biedrzycka; Kati Räisänen; Cornelia Ch Wielders; Paweł Urbanowicz; Angela de Haan; Karin Westmo; Fabian Landman; Han Gj van der Heide; Simon Lansu; Romy D. Zwittink; Daan W. Notermans; Aneta Guzek; Viacheslav Kondratiuk; Aidyn Salmanov; Sebastian Haller; Marius Linkevicius; Sören Gatermann; Anke Kohlenberg; Marek Gniadkowski; Guido Werner; Antoni Pa Hendrickx

doi:10.2807/1560-7917.ES.2024.29.23.2300616

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

Sandra Witteveen
, Jörg B. Hans
, Radosław Izdebski
, Henrik Hasman
, Ørjan Samuelsen
, Laurent Dortet
, Yvonne Pfeifer
, Niall Delappe
, Jesús Oteo-Iglesias
, Dorota Żabicka
, Martin Cormican
, Mirco Sandfort
, Felix Reichert
, Anna K. Pöntinen
, Martin A. Fischer
, Nelianne Verkaik
, María Pérez-Vazquez
, Niels Pfennigwerth
, Anette M. Hammerum
, Søren Hallstrøm

Marta Biedrzycka, Kati Räisänen, Cornelia Ch Wielders, Paweł Urbanowicz, Angela de Haan, Karin Westmo, Fabian Landman, Han Gj van der Heide, Simon Lansu, Romy D. Zwittink, Daan W. Notermans, Aneta Guzek, Viacheslav Kondratiuk, Aidyn Salmanov, Sebastian Haller, Marius Linkevicius, Sören Gatermann, Anke Kohlenberg, Marek Gniadkowski, Guido Werner, Antoni Pa Hendrickx^*

^*Corresponding author for this work

Medical Microbiology & Infectious Diseases

National Institute of Public Health and the Environment
Robert Koch-Institut
Ruhr University Bochum
National Medicines Institute, Warsaw
Statens Serum Institut
University of Tromsø – The Arctic University of Norway
University Hospital of North Norway
Immunology of Viral Infections and Autoimmune Diseases
University of Galway
Centro Nacional de Microbiologia
University of Oslo
National Institute for Health and Welfare
Public Health Agency of Sweden
Wojskowy Instytut Medyczny
National Pirogov Memorial Medical University, Vinnytsya
Shupyk National Healthcare University of Ukraine
European Centre for Disease Prevention and Control

Research output: Contribution to journal › Article › Academic › peer-review

24 Citations (Scopus)

30 Downloads (Pure)

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 blaNDM-1-carrying-P. stuartii isolates underwent antimicrobial susceptibility testing (AST). Transferability to Escherichia coli of a blaNDM-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 blaNDM-1-carrying-P. stuartii and the third blaNDM-5-carrying-P. stuartii. The blaNDM-1 clusters (PstCluster-001, n = 22 isolates; PstCluster-002, n = 8 isolates) comprised strains from seven and four countries, respectively. The blaNDM-5 cluster (PstCluster-003) included 13 isolates from six countries. PstCluster-001 and PstCluster-002 isolates carried an MDR plasmid harbouring blaNDM-1,blaOXA-10, blaCMY-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.

Original language	English
Article number	pii=2300616
Number of pages	13
Journal	Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin
Volume	9
Issue number	23
DOIs	https://doi.org/10.2807/1560-7917.ES.2024.29.23.2300616
Publication status	Published - 6 Jun 2024

Bibliographical note

Publisher Copyright:
© 2024 European Centre for Disease Prevention and Control (ECDC). All rights reserved.

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This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being
SDG 16 Peace, Justice and Strong Institutions

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eurosurv-29-23_4Final published version, 800 KBLicence: CC BY

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Witteveen, S., Hans, J. B., Izdebski, R., Hasman, H., Samuelsen, Ø., Dortet, L., Pfeifer, Y., Delappe, N., Oteo-Iglesias, J., Żabicka, D., Cormican, M., Sandfort, M., Reichert, F., Pöntinen, A. K., Fischer, M. A., Verkaik, N., Pérez-Vazquez, M., Pfennigwerth, N., Hammerum, A. M., ... Hendrickx, A. P. (2024). Dissemination of extensively drug-resistant NDM-producing Providencia stuartii in Europe linked to patients transferred from Ukraine, March 2022 to March 2023. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin, 9(23), Article pii=2300616. https://doi.org/10.2807/1560-7917.ES.2024.29.23.2300616

@article{a17fb6b0c6a844ff96bd486b04ffc1ed,

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

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 blaNDM-1-carrying-P. stuartii isolates underwent antimicrobial susceptibility testing (AST). Transferability to Escherichia coli of a blaNDM-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 blaNDM-1-carrying-P. stuartii and the third blaNDM-5-carrying-P. stuartii. The blaNDM-1 clusters (PstCluster-001, n = 22 isolates; PstCluster-002, n = 8 isolates) comprised strains from seven and four countries, respectively. The blaNDM-5 cluster (PstCluster-003) included 13 isolates from six countries. PstCluster-001 and PstCluster-002 isolates carried an MDR plasmid harbouring blaNDM-1,blaOXA-10, blaCMY-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.",

author = "Sandra Witteveen and Hans, \{J{\"o}rg B.\} and Rados{\l}aw Izdebski and Henrik Hasman and {\O}rjan Samuelsen and Laurent Dortet and Yvonne Pfeifer and Niall Delappe and Jes{\'u}s Oteo-Iglesias and Dorota {\.Z}abicka and Martin Cormican and Mirco Sandfort and Felix Reichert and P{\"o}ntinen, \{Anna K.\} and Fischer, \{Martin A.\} and Nelianne Verkaik and Mar{\'i}a P{\'e}rez-Vazquez and Niels Pfennigwerth and Hammerum, \{Anette M.\} and S{\o}ren Hallstr{\o}m and Marta Biedrzycka and Kati R{\"a}is{\"a}nen and Wielders, \{Cornelia Ch\} and Pawe{\l} Urbanowicz and \{de Haan\}, Angela and Karin Westmo and Fabian Landman and \{van der Heide\}, \{Han Gj\} and Simon Lansu and Zwittink, \{Romy D.\} and Notermans, \{Daan W.\} and Aneta Guzek and Viacheslav Kondratiuk and Aidyn Salmanov and Sebastian Haller and Marius Linkevicius and S{\"o}ren Gatermann and Anke Kohlenberg and Marek Gniadkowski and Guido Werner and Hendrickx, \{Antoni Pa\}",

year = "2024",

month = jun,

day = "6",

doi = "10.2807/1560-7917.ES.2024.29.23.2300616",

language = "English",

volume = "9",

journal = "Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin",

issn = "1560-7917",

publisher = "European Centre for Disease Prevention and Control (ECDC)",

number = "23",

}

Witteveen, S, Hans, JB, Izdebski, R, Hasman, H, Samuelsen, Ø, Dortet, L, Pfeifer, Y, Delappe, N, Oteo-Iglesias, J, Żabicka, D, Cormican, M, Sandfort, M, Reichert, F, Pöntinen, AK, Fischer, MA, Verkaik, N, Pérez-Vazquez, M, Pfennigwerth, N, Hammerum, AM, Hallstrøm, S, Biedrzycka, M, Räisänen, K, Wielders, CC, Urbanowicz, P, de Haan, A, Westmo, K, Landman, F, van der Heide, HG, Lansu, S, Zwittink, RD, Notermans, DW, Guzek, A, Kondratiuk, V, Salmanov, A, Haller, S, Linkevicius, M, Gatermann, S, Kohlenberg, A, Gniadkowski, M, Werner, G & Hendrickx, AP 2024, 'Dissemination of extensively drug-resistant NDM-producing Providencia stuartii in Europe linked to patients transferred from Ukraine, March 2022 to March 2023', Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin, vol. 9, no. 23, pii=2300616. https://doi.org/10.2807/1560-7917.ES.2024.29.23.2300616

Dissemination of extensively drug-resistant NDM-producing Providencia stuartii in Europe linked to patients transferred from Ukraine, March 2022 to March 2023. / Witteveen, Sandra; Hans, Jörg B.; Izdebski, Radosław et al.
In: Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin, Vol. 9, No. 23, pii=2300616, 06.06.2024.

Research output: Contribution to journal › Article › Academic › peer-review

TY - JOUR

T1 - Dissemination of extensively drug-resistant NDM-producing Providencia stuartii in Europe linked to patients transferred from Ukraine, March 2022 to March 2023

AU - Witteveen, Sandra

AU - Hans, Jörg B.

AU - Izdebski, Radosław

AU - Hasman, Henrik

AU - Samuelsen, Ørjan

AU - Dortet, Laurent

AU - Pfeifer, Yvonne

AU - Delappe, Niall

AU - Oteo-Iglesias, Jesús

AU - Żabicka, Dorota

AU - Cormican, Martin

AU - Sandfort, Mirco

AU - Reichert, Felix

AU - Pöntinen, Anna K.

AU - Fischer, Martin A.

AU - Verkaik, Nelianne

AU - Pérez-Vazquez, María

AU - Pfennigwerth, Niels

AU - Hammerum, Anette M.

AU - Hallstrøm, Søren

AU - Biedrzycka, Marta

AU - Räisänen, Kati

AU - Wielders, Cornelia Ch

AU - Urbanowicz, Paweł

AU - de Haan, Angela

AU - Westmo, Karin

AU - Landman, Fabian

AU - van der Heide, Han Gj

AU - Lansu, Simon

AU - Zwittink, Romy D.

AU - Notermans, Daan W.

AU - Guzek, Aneta

AU - Kondratiuk, Viacheslav

AU - Salmanov, Aidyn

AU - Haller, Sebastian

AU - Linkevicius, Marius

AU - Gatermann, Sören

AU - Kohlenberg, Anke

AU - Gniadkowski, Marek

AU - Werner, Guido

AU - Hendrickx, Antoni Pa

PY - 2024/6/6

Y1 - 2024/6/6

N2 - 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 blaNDM-1-carrying-P. stuartii isolates underwent antimicrobial susceptibility testing (AST). Transferability to Escherichia coli of a blaNDM-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 blaNDM-1-carrying-P. stuartii and the third blaNDM-5-carrying-P. stuartii. The blaNDM-1 clusters (PstCluster-001, n = 22 isolates; PstCluster-002, n = 8 isolates) comprised strains from seven and four countries, respectively. The blaNDM-5 cluster (PstCluster-003) included 13 isolates from six countries. PstCluster-001 and PstCluster-002 isolates carried an MDR plasmid harbouring blaNDM-1,blaOXA-10, blaCMY-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.

AB - 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 blaNDM-1-carrying-P. stuartii isolates underwent antimicrobial susceptibility testing (AST). Transferability to Escherichia coli of a blaNDM-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 blaNDM-1-carrying-P. stuartii and the third blaNDM-5-carrying-P. stuartii. The blaNDM-1 clusters (PstCluster-001, n = 22 isolates; PstCluster-002, n = 8 isolates) comprised strains from seven and four countries, respectively. The blaNDM-5 cluster (PstCluster-003) included 13 isolates from six countries. PstCluster-001 and PstCluster-002 isolates carried an MDR plasmid harbouring blaNDM-1,blaOXA-10, blaCMY-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.

UR - https://www.scopus.com/pages/publications/85195438763

U2 - 10.2807/1560-7917.ES.2024.29.23.2300616

DO - 10.2807/1560-7917.ES.2024.29.23.2300616

M3 - Article

C2 - 38847120

AN - SCOPUS:85195438763

SN - 1560-7917

VL - 9

JO - Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin

JF - Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin

IS - 23

M1 - pii=2300616

ER -

Witteveen S, Hans JB, Izdebski R, Hasman H, Samuelsen Ø, Dortet L et al. Dissemination of extensively drug-resistant NDM-producing Providencia stuartii in Europe linked to patients transferred from Ukraine, March 2022 to March 2023. Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin. 2024 Jun 6;9(23):pii=2300616. doi: 10.2807/1560-7917.ES.2024.29.23.2300616

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

Abstract

Bibliographical note

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