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Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread

Nature Microbiology volume 4, pages 1919–1929 (2019)Cite this article

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Abstract

Public health interventions to control the current epidemic of carbapenem-resistant Klebsiella pneumoniae rely on a comprehensive understanding of its emergence and spread over a wide range of geographical scales. We analysed the genome sequences and epidemiological data of >1,700 K. pneumoniae samples isolated from patients in 244 hospitals in 32 countries during the European Survey of Carbapenemase-Producing Enterobacteriaceae. We demonstrate that carbapenemase acquisition is the main cause of carbapenem resistance and that it occurred across diverse phylogenetic backgrounds. However, 477 of 682 (69.9%) carbapenemase-positive isolates are concentrated in four clonal lineages, sequence types 11, 15, 101, 258/512 and their derivatives. Combined analysis of the genetic and geographic distances between isolates with different β-lactam resistance determinants suggests that the propensity of K. pneumoniae to spread in hospital environments correlates with the degree of resistance and that carbapenemase-positive isolates have the highest transmissibility. Indeed, we found that over half of the hospitals that contributed carbapenemase-positive isolates probably experienced within-hospital transmission, and interhospital spread is far more frequent within, rather than between, countries. Finally, we propose a value of 21 for the number of single nucleotide polymorphisms that optimizes the discrimination of hospital clusters and detail the international spread of the successful epidemic lineage, ST258/512.

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Fig. 1: Geographical distribution of carbapenem resistance mechanisms among isolates submitted during the EuSCAPE survey.
Fig. 2: Carbapenemase-positive isolates are concentrated in major clonal lineages of K. pneumoniae.
Fig. 3: Carbapenemase-positive isolates show strong geographical clustering.
Fig. 4: Determination of a SNP cut-off to aid outbreak investigations of ST258/512.
Fig. 5: International spread of the epidemic ST258/512 clone.

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Data availability

All raw and assembled Illumina sequence data are available from the European Nucleotide Archive under the study accession no. PRJEB10018/ERP011196. Individual accession numbers for raw sequence data and de novo assemblies are also available in Supplementary Table 4. Phylogenetic analysis of the 1,717 K. pneumoniae isolates (EuSCAPE only) and the ST258/512 isolates (EuSCAPE and public data) together with all metadata and links to raw sequence data are available at the project URLs https://microreact.org/project/EuSCAPE_Kp and https://microreact.org/project/EuSCAPE_ST258 within Microreact (ref. 51). Phylogenetic analyses and the metadata of the isolates are also available separately for each of the contributing countries in Microreact (see Supplementary Table 7 for project URLs).

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Acknowledgements

We thank the Pathogen Informatics Group and Core Sequencing Facility at the Wellcome Sanger Institute for their contributions to the study. We also thank F. Bosma and M. Zigterman from the Medical Microbiology and Infection Prevention Department of the University Medical Center Groningen for their support in assembling the isolate collection. This work was funded by The Centre for Genomic Pathogen Surveillance, Wellcome Genome Campus, Wellcome (grant nos. 098051 and 099202) and the NIHR Global Health Research Unit on Genomic Surveillance of Antimicrobial Resistance (NIHR 16/136/111). The EuSCAPE project was funded by ECDC through a specific framework contract (ECDC/2012/055) following an open call for tender (OJ/25/04/2012-PROC/2012/036). This work was carried out on behalf of the ESCMID Study Group for Epidemiological Markers (ESGEM); the full list of members is provided in the Supplementary Information.

Author information

Author notes

  1. These authors contributed equally: David M. Aanensen, Hajo Grundmann.

  2. A list of members appears in the Supplementary Note.

Authors and Affiliations

  1. Centre for Genomic Pathogen Surveillance, Wellcome Genome Campus, Cambridge, UK

    Sophia David, Silvia Argimon, Khalil Abudahab, Richard Goater & David M. Aanensen

  2. Institute for Infection Prevention and Hospital Epidemiology, Faculty of Medicine, University of Freiburg, Freiburg, Germany

    Sandra Reuter & Hajo Grundmann

  3. Pathogen Genomics, Wellcome Sanger Institute, Cambridge, UK

    Simon R. Harris & Theresa Feltwell

  4. Department of Medical Microbiology and Infection Prevention, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    Corinna Glasner & Hajo Grundmann

  5. Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy

    Tommaso Giani & Gian Maria Rossolini

  6. Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy

    Giulia Errico

  7. Natural Sciences, University of Bath, Bath, UK

    Marianne Aspbury

  8. Pathogen Informatics, Wellcome Sanger Institute, Cambridge, UK

    Sara Sjunnebo

  9. Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath, UK

    Edward J. Feil

  10. Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Florence, Italy

    Gian Maria Rossolini

  11. Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Medicine, University of Oxford, Oxford, UK

    David M. Aanensen

  12. University Hospital Center Mother Theresa, Tirana, Albania

    Andi Koraqi & Denada Lacej

  13. Elisabethinen Hospital Linz, Linz, Austria

    Petra Apfalter & Rainer Hartl

  14. CHU Dinant-Godinne, UCL Namur, Namur, Belgium

    Youri Glupczynski & Te-Din Huang

  15. Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

    Tanya Strateva

  16. Alexandrovska University Hospital, Sofia, Bulgaria

    Yuliya Marteva-Proevska

  17. University Hospital for Infectious Diseases, Zagreb, Croatia

    Arjana Tambic Andrasevic & Iva Butic

  18. Nicosia General Hospital, Nicosia, Cyprus

    Despo Pieridou-Bagatzouni & Panagiota Maikanti-Charalampous

  19. Faculty of Medicine in Plzen, Charles University in Prague, Plzen, Czech Republic

    Jaroslav Hrabak

  20. National Institute of Public Health, Prague, Czech Republic

    Helena Zemlickova

  21. Statens Serum Institut, Copenhagen, Denmark

    Anette Hammerum & Lotte Jakobsen

  22. East Tallinn Central Hospital, Tallinn, Estonia

    Marina Ivanova & Anastasia Pavelkovich

  23. National Institute for Health and Welfare, Turku, Finland

    Jari Jalava & Monica Österblad

  24. Bicêtre Hospital, Le Kremlin-Bicêtre, France

    Laurent Dortet

  25. Institut de Veille Sanitaire, Saint-Maurice, France

    Sophie Vaux

  26. Universitätsmedizin Göttingen, Göttingen, Germany

    Martin Kaase

  27. Ruhr-University Bochum, Bochum, Germany

    Sören G. Gatermann

  28. National School of Public Health, Athens, Greece

    Alkiviadis Vatopoulos & Kyriaki Tryfinopoulou

  29. National Center for Epidemiology, Budapest, Hungary

    Ákos Tóth & Laura Jánvári

  30. Galway University Hospitals, Galway, Ireland

    Teck Wee Boo & Elaine McGrath

  31. Ministry of Health, Tel Aviv, Israel

    Yehuda Carmeli & Amos Adler

  32. Istituto Superiore di Sanità, Rome, Italy

    Annalisa Pantosti & Monica Monaco

  33. National Institute of Public Health of Kosovo, Prishtina, Kosovo

    Lul Raka & Arsim Kurti

  34. Pauls Stradins Clinical University Hospital, Riga, Latvia

    Arta Balode & Mara Saule

  35. National Public Health Surveillance Laboratory, Vilnius, Lithuania

    Jolanta Miciuleviciene & Aiste Mierauskaite

  36. Laboratoire National De Sante, Düdelingen, Luxembourg

    Monique Perrin-Weniger & Paul Reichert

  37. Mater Dei Hospital, Msida, Malta

    Nina Nestorova & Sonia Debattista

  38. Institute of Public Health, Podgorica, Montenegro

    Gordana Mijovic & Milena Lopicic

  39. University Hospital of North Norway, Tromsø, Norway

    Ørjan Samuelsen & Bjørg Haldorsen

  40. Narodowy Instytut Lekow, Warsaw, Poland

    Dorota Zabicka

  41. National Medicines Institute, Warsaw, Poland

    Elzbieta Literacka

  42. National Institute of Health Dr. Ricardo Jorge, Lisbon, Portugal

    Manuela Caniça & Vera Manageiro

  43. Medical Faculty, Institute of Microbiology and Parasitology, Skopje, Republic of Macedonia

    Ana Kaftandzieva & Elena Trajkovska-Dokic

  44. Cantacuzino National Research Institute, Bucharest, Romania

    Maria Damian & Brandusa Lixandru

  45. Institute for Public Health of Vojvodina, Novi Sad, Serbia

    Zora Jelesic

  46. Institute for Pulmonary Diseases of Vojvodina, Sremska Kamenica, Serbia

    Anika Trudic

  47. Public Health Authority of the Slovak Republic, Bratislava, Slovakia

    Milan Niks

  48. Faculty of Medicine, P. J. Šafárik University, Kosice, Slovakia

    Eva Schreterova

  49. Institute of Microbiology and Immunology, Ljubljana, Slovenia

    Mateja Pirs & Tjasa Cerar

  50. Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, Spain

    Jesús Oteo & Belén Aracil

  51. Karolinska Institutet, Stockholm, Sweden

    Christian Giske

  52. Public Health Agency of Sweden, Stockholm, Sweden

    Karin Sjöström

  53. Hacettepe University, Ankara, Turkey

    Deniz Gür & Asli Cakar

  54. Reference Microbiology Services, Public Health England, London, UK

    Neil Woodford & Katie Hopkins

  55. Sydvestjysk Hospital, Esbjerg, Denmark

    Camilla Wiuff

  56. Scottish Microbiology Reference Laboratories, Glasgow, UK

    Derek J. Brown

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Consortia

the EuSCAPE Working Group

  • Andi Koraqi
  • , Denada Lacej
  • , Petra Apfalter
  • , Rainer Hartl
  • , Youri Glupczynski
  • , Te-Din Huang
  • , Tanya Strateva
  • , Yuliya Marteva-Proevska
  • , Arjana Tambic Andrasevic
  • , Iva Butic
  • , Despo Pieridou-Bagatzouni
  • , Panagiota Maikanti-Charalampous
  • , Jaroslav Hrabak
  • , Helena Zemlickova
  • , Anette Hammerum
  • , Lotte Jakobsen
  • , Marina Ivanova
  • , Anastasia Pavelkovich
  • , Jari Jalava
  • , Monica Österblad
  • , Laurent Dortet
  • , Sophie Vaux
  • , Martin Kaase
  • , Sören G. Gatermann
  • , Alkiviadis Vatopoulos
  • , Kyriaki Tryfinopoulou
  • , Ákos Tóth
  • , Laura Jánvári
  • , Teck Wee Boo
  • , Elaine McGrath
  • , Yehuda Carmeli
  • , Amos Adler
  • , Annalisa Pantosti
  • , Monica Monaco
  • , Lul Raka
  • , Arsim Kurti
  • , Arta Balode
  • , Mara Saule
  • , Jolanta Miciuleviciene
  • , Aiste Mierauskaite
  • , Monique Perrin-Weniger
  • , Paul Reichert
  • , Nina Nestorova
  • , Sonia Debattista
  • , Gordana Mijovic
  • , Milena Lopicic
  • , Ørjan Samuelsen
  • , Bjørg Haldorsen
  • , Dorota Zabicka
  • , Elzbieta Literacka
  • , Manuela Caniça
  • , Vera Manageiro
  • , Ana Kaftandzieva
  • , Elena Trajkovska-Dokic
  • , Maria Damian
  • , Brandusa Lixandru
  • , Zora Jelesic
  • , Anika Trudic
  • , Milan Niks
  • , Eva Schreterova
  • , Mateja Pirs
  • , Tjasa Cerar
  • , Jesús Oteo
  • , Belén Aracil
  • , Christian Giske
  • , Karin Sjöström
  • , Deniz Gür
  • , Asli Cakar
  • , Neil Woodford
  • , Katie Hopkins
  • , Camilla Wiuff
  •  & Derek J. Brown

the ESGEM Study Group

Contributions

H.G. and D.M.A. conceived the study. The EuSCAPE Working Group collected the bacterial isolates and epidemiological data and performed preliminary laboratory analyses. The ESGEM facilitated the training and capacity building for the collection of bacterial isolates and preliminary analyses. S.D., S.R., S.R.H., C.G., T.F., S.A., K.A., R.G., T.G., G.E., M.A., S.S., E.J.F., G.M.R., H.G. and D.M.A. performed the data analysis. S.D., S.R., E.J.F., G.M.R., H.G. and D.M.A. wrote the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to David M. Aanensen or Hajo Grundmann.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–3, Supplementary Table 1, Supplementary Table 5, Supplementary Table 7 and Supplementary Note.

Reporting Summary

Supplementary Table 2

Detailed QC results for all sequenced isolates submitted as K. pneumoniae.

Supplementary Table 3

Identification of best-matching taxa to the individual assembly contigs of all sequenced isolates using Mash.

Supplementary Table 4

Epidemiological and genotyping data for 1,717 K. pneumoniae isolates that passed sequencing QC filters.

Supplementary Table 6

Epidemiological and genotyping data and publication sources of 651 isolates used in the ST258/512 phylogenetic analysis.

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David, S., Reuter, S., Harris, S.R. et al. Epidemic of carbapenem-resistant Klebsiella pneumoniae in Europe is driven by nosocomial spread. Nat Microbiol 4, 1919–1929 (2019). https://doi.org/10.1038/s41564-019-0492-8

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