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Since the beginning of the war in Ukraine in February 2022, Ukrainians have been seeking shelter in other European countries.


We aimed to investigate the prevalence and the molecular epidemiology of multidrug-resistant Gram-negative (MDRGN) bacteria and meticillin-resistant (MRSA) in Ukrainian patients at admittance to the University Hospital Frankfurt, Germany.


We performed screening and observational analysis of all patients from March until June 2022. Genomes of MDRGN isolates were analysed for antimicrobial resistance, virulence genes and phylogenetic relatedness.


We included 103 patients (median age: 39 ± 23.7 years), 57 of whom were female (55.3%; 95% confidence interval (CI): 45.2–5.1). Patients were most frequently admitted to the Department of Paediatrics (29/103; 28.2%; 95% CI: 19.7–37.9). We found 34 MDRGN isolates in 17 of 103 patients (16.5%; 95% CI: 9.9–25.1). Ten patients carried 21 carbapenem-resistant (CR) bacteria, five of them more than one CR isolate. Four of six patients with war-related injuries carried eight CR isolates. In six of 10 patients, CR isolates caused infections. Genomic characterisation revealed that the CR isolates harboured at least one carbapenemase gene, being the most frequent (n = 10). Core genome and plasmid analysis revealed no epidemiological connection between most of these isolates. Hypervirulence marker genes were found in five of six CR isolates. No MRSA was found.


Hospitals should consider infection control strategies to cover the elevated prevalence of MDRGN bacteria in Ukrainian patients with war-related injuries and/or hospital pre-treatment and to prevent the spread of hypervirulent CR isolates.


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  1. Bilefsky D, Pérez-Peña R, Nagourney E. The roots of the Ukraine war: how the crisis developed. New York: The New York Times; 12 Oct 2022. Available from: https://www.nytimes.com/article/russia-ukraine-nato-europe.html
  2. Flüchtlinge aus der Ukraine. [Refugees from Ukraine]. Berlin: Mediendienst Integration. [Accessed: 26 Oct 2022]. German. Available from: https://mediendienst-integration.de/migration/flucht-asyl/ukrainische-fluechtlinge.html
  3. Gesamtzahl der offiziell gezählten Kriegsflüchtlinge aus der Ukraine in Deutschland bis August 2022. [Total number of officially counted war refugees from Ukraine in Germany until August 2022]. Hamburg: Statista GmbH. [Accessed: 5 Sep 2022]. German. Available from: https://de.statista.com/statistik/daten/studie/1294820/umfrage/kriegsfluechtlinge-aus-der-ukraine-in-deutschland
  4. Murthy RS, Lakshminarayana R. Mental health consequences of war: a brief review of research findings. World Psychiatry. 2006;5(1):25-30. PMID: 16757987 
  5. McFarlane AC. The impact of war on mental health: lest we forget. World Psychiatry. 2015;14(3):351-3.  https://doi.org/10.1002/wps.20253  PMID: 26407792 
  6. Murphy RA, Ronat JB, Fakhri RM, Herard P, Blackwell N, Abgrall S, et al. Multidrug-resistant chronic osteomyelitis complicating war injury in Iraqi civilians. J Trauma. 2011;71(1):252-4.  https://doi.org/10.1097/TA.0b013e31821b8622  PMID: 21818032 
  7. Murray CK, Obremskey WT, Hsu JR, Andersen RC, Calhoun JH, Clasper JC, et al. Prevention of infections associated with combat-related extremity injuries. J Trauma. 2011;71(2) Suppl 2;S235-57.  https://doi.org/10.1097/TA.0b013e318227ac5f  PMID: 21814090 
  8. Mandavilli A. Public health catastrophe looms in Ukraine, experts warn.New York: The New York Times; 26 Mar 2022. Available from: https://www.nytimes.com/2022/03/26/health/ukraine-health-tb-hiv.html
  9. WHO Regional Office for Europe (WHO/Europe)/European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance surveillance in Europe 2022–2020 data. Copenhagen: WHO/Europe; 2022. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/ECDC-WHO-AMR-report.pdf
  10. Higgins PG, Hagen RM, Podbielski A, Frickmann H, Warnke P. Molecular epidemiology of carbapenem-resistant Acinetobacter baumannii Isolated from war-injured Patients from the Eastern Ukraine. Antibiotics (Basel). 2020;9(9):579.  https://doi.org/10.3390/antibiotics9090579  PMID: 32899463 
  11. Davis KA, Moran KA, McAllister CK, Gray PJ. Multidrug-resistant Acinetobacter extremity infections in soldiers. Emerg Infect Dis. 2005;11(8):1218-24.  https://doi.org/10.3201/1108.050103  PMID: 16102310 
  12. Ahmad OB, Boschi-Pinto C, Lopez AD, Murray CJL, Lozano R, Inoue M. Age standardization of rates: A new WHO standard. Geneva: World Health Organization; 2001. Available from: https://cdn.who.int/media/docs/default-source/gho-documents/global-health-estimates/gpe_discussion_paper_series_paper31_2001_age_standardization_rates.pdf
  13. Bundesministerium der Justiz (BMJ). Gesetz zur Verhütung und Bekämpfung von Infektionskrankheiten beim Menschen. [Law on the prevention and control of infectious diseases in humans]. Berlin: BMJ. [Accessed: 20 May 2022]. German. Available from: https://www.gesetze-im-internet.de/ifsg
  14. Reinheimer C, Kempf VA, Göttig S, Hogardt M, Wichelhaus TA, O’Rourke F, et al. Multidrug-resistant organisms detected in refugee patients admitted to a University Hospital, Germany June‒December 2015. Euro Surveill. 2016;21(2):30110.  https://doi.org/10.2807/1560-7917.ES.2016.21.2.30110  PMID: 26794850 
  15. Reinheimer C, Kempf VA, Jozsa K, Wichelhaus TA, Hogardt M, O’Rourke F, et al. Prevalence of multidrug-resistant organisms in refugee patients, medical tourists and domestic patients admitted to a German university hospital. BMC Infect Dis. 2017;17(1):17.  https://doi.org/10.1186/s12879-016-2105-y  PMID: 28056820 
  16. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters, version 12.0. Växjö: EUCAST; 2022. Available from: http://www.eucast.org/clinical_breakpoints
  17. Doyle D, Peirano G, Lascols C, Lloyd T, Church DL, Pitout JD. Laboratory detection of Enterobacteriaceae that produce carbapenemases. J Clin Microbiol. 2012;50(12):3877-80.  https://doi.org/10.1128/JCM.02117-12  PMID: 22993175 
  18. Göttig S, Gruber TM, Stecher B, Wichelhaus TA, Kempf VA. In vivo horizontal gene transfer of the carbapenemase OXA-48 during a nosocomial outbreak. Clin Infect Dis. 2015;60(12):1808-15.  https://doi.org/10.1093/cid/civ191  PMID: 25759432 
  19. Villinger D, Schultze TG, Musyoki VM, Inwani I, Aluvaala J, Okutoyi L, et al. Genomic transmission analysis of multidrug-resistant Gram-negative bacteria within a newborn unit of a Kenyan tertiary hospital: A four-month prospective colonization study. Front Cell Infect Microbiol. 2022;12:892126.  https://doi.org/10.3389/fcimb.2022.892126  PMID: 36093198 
  20. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691-3.  https://doi.org/10.1093/bioinformatics/btv421  PMID: 26198102 
  21. Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017;45(D1):D566-73.  https://doi.org/10.1093/nar/gkw1004  PMID: 27789705 
  22. Pitout JDD, Peirano G, Chen L, DeVinney R, Matsumura Y. Escherichia coli ST1193: following in the footsteps of E. coli ST131. Antimicrob Agents Chemother. 2022;66(7):e0051122.  https://doi.org/10.1128/aac.00511-22  PMID: 35658504 
  23. Peirano G, Chen L, Nobrega D, Finn TJ, Kreiswirth BN, DeVinney R, et al. Genomic epidemiology of global carbapenemase-producing Escherichia coli, 2015-2017. Emerg Infect Dis. 2022;28(5):924-31.  https://doi.org/10.3201/eid2805.212535  PMID: 35451367 
  24. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M, Røder BL, et al. Escherichia coli sequence type 410 is causing new international high-risk clones. MSphere. 2018;3(4):e00337-18.  https://doi.org/10.1128/mSphere.00337-18  PMID: 30021879 
  25. Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev. 2019;32(3):e00001-00019.  https://doi.org/10.1128/CMR.00001-19  PMID: 31092506 
  26. Di Pilato V, Henrici De Angelis L, Aiezza N, Baccani I, Niccolai C, Parisio EM, et al. Resistome and virulome accretion in an NDM-1-producing ST147 sublineage of Klebsiella pneumoniae associated with an outbreak in Tuscany, Italy: a genotypic and phenotypic characterisation. Lancet Microbe. 2022;3(3):e224-34.  https://doi.org/10.1016/S2666-5247(21)00268-8  PMID: 35544076 
  27. Falcone M, Tiseo G, Arcari G, Leonildi A, Giordano C, Tempini S, et al. Spread of hypervirulent multidrug-resistant ST147 Klebsiella pneumoniae in patients with severe COVID-19: an observational study from Italy, 2020-21. J Antimicrob Chemother. 2022;77(4):1140-5.  https://doi.org/10.1093/jac/dkab495  PMID: 35040981 
  28. Becker K, Podbielski A, Sunderkötter C, Berner R, Eckmann C, von Eiff C, et al. MiQ 06a/b: Infektionen der Haut und der subkutanen Weichgewebe - Teil I und II. [Infections of the skin and subcutaneous soft tissues - parts I and II]. In: Podbielski A, Herrmann M, Kniehl H, Rüssmann MH (Hrsg.). Mikrobiologisch-infektiologische Qualitätsstandards (MiQ). [Microbiological-infectious quality standards]. München, Jena: Elsevier/Urban and Fischer; 2013.
  29. Brennan C, DeLappe N, Cormican M, Tuohy A, Tobin A, Moran L, et al. A geographic cluster of healthcare-associated carbapenemase-producing hypervirulent Klebsiella pneumoniae sequence type 23. Eur J Clin Microbiol Infect Dis. 2022.  https://doi.org/10.1007/s10096-022-04535-z  PMID: 36454389 
  30. Hygienemaßnahmen bei Infektionen oder Besiedlung mit multiresistenten gramnegativen Stäbchen. Empfehlung der Kommission für Kranken-haushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut (RKI). [Hygiene measures for infection or colonization with multidrug-resistant gram-negative bacilli. Commission recommendation for hospital hygiene and infection prevention KRINKO at the Robert Koch Institute RKI]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2012;55(10):1311-54. German.  https://doi.org/10.1007/s00103-012-1549-5  PMID: 23011096 

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