Epidemiological and Clinical Insights into the Enterovirus D68 Upsurge in Europe 2021–2022 and Emergence of Novel B3-Derived Lineages, ENPEN Multicentre Study-Reference-Cited by-同舟云学术

Epidemiological and Clinical Insights into the Enterovirus D68 Upsurge in Europe 2021–2022 and Emergence of Novel B3-Derived Lineages, ENPEN Multicentre Study

Published:2024-03-28 Issue: Volume: Page:
ISSN:0022-1899
Container-title:The Journal of Infectious Diseases
language:en
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Author:

Simoes Margarida Pires¹²^ORCID,Hodcroft Emma B³⁴⁵^ORCID,Simmonds Peter⁶^ORCID,Albert Jan⁷⁸^ORCID,Alidjinou Enagnon K⁹,Ambert-Balay Katia¹⁰^ORCID,Andrés Cristina¹¹¹²^ORCID,Antón Andrés¹¹¹²^ORCID,Auvray Christelle¹⁰^ORCID,Bailly Jean-Luc¹³^ORCID,Baldanti Fausto¹⁴¹⁵^ORCID,Bastings Capser¹⁶,Beard Stuart¹⁷,Berengua Carla¹⁸,Berginc Natasa¹⁹,Bloemen Mandy²⁰,Blomqvist Soile²¹,Bosma Froukje²²,Böttcher Sindy²³^ORCID,Bubba Laura²⁴,Buderus Stafan²⁵,Cabrerizo Maria²⁶,Calvo Cristina²⁷^ORCID,Celma Cristina¹⁷,Ceriotti Ferruccio²⁸^ORCID,Clark Gemma²⁹^ORCID,Costa Inës³⁰^ORCID,Coste-Burel Marianne³¹,Couderé Karen³²,Cremer Jeroen¹,del Cuerpo Casas Margarita¹⁸,Daehne Theo³³,de Beer Jessica²²,de Ceano-Vivas Maria²⁷,De Gascun Cillian³⁴,de Rougemont Alexis¹⁰,Dean Jonathan³⁴,Dembinski Jennifer L³⁵,Diedrich Sabine²³,Diez-Domingo Javier³⁶³⁷,Dillner Lena³⁸,Dorenberg Dagny H³⁵,Ducancelle Alexandra³⁹,Dudman Susanne⁴⁰⁴¹,Dyrdak Robert⁷⁸,Eis-Huebinger Anna-Maria⁴²,Falces-Romero Iker¹²^ORCID,Farkas Agnes⁴³,Feeney Susan⁴⁴,Fernandez-Garcia Maria D²⁶,Flipse Jacky⁴⁵,Franck Kristina T⁴⁶,Galli Cristina⁴⁷,Garrigue Isabelle⁴⁸,Geeraedts Felix²²,Georgieva Irina⁴⁹,Giardina Federica¹⁵,Guiomar Raquel³⁰^ORCID,Hauzenberger Elenor³⁸,Heikens Esther⁵⁰,Henquell Cécille¹³⁵¹,Hober Didier⁹,Hönemann Mario⁵²,Howson-Wells Hannah²⁹,Hruškar Željka⁵³,Ikonen Niina²¹,Imbert Berthemarie³¹,Jansz Arjan R¹⁶,Jeannoël Marion⁵⁴,Jiřincová Helena⁵⁵,Josset Laurence⁵⁴,Keeren Kathrin⁵⁶,Kramer-Lindhout Naomie⁵⁷,Krokstad Sidsel⁵⁸,Lazrek Mouna⁹,Le Guillou-Guillemette Hélène³⁹,Lefeuvre Caroline³⁹,Lind Andreas⁴⁰,Lunar Maja M⁵⁹,Maier Melanie⁵²,Marque-Juillet Stéphanie⁶⁰,McClure C Patrick⁶¹,McKenna James⁴⁴,Meijer Adam¹^ORCID,Menasalvas Ruiz Ana⁶²,Mengual-Chuliá Beatriz³⁶³⁷,Midgley Sofie⁴⁶,Mirand Audrey¹³⁵¹,Molenkamp Richard⁶³,Montes Milagrosa⁶⁴,Moreno-Docón Antonio⁶⁵,Morley Ursula³⁴,Murk Jean-Luc³²,Navascués-Ortega Ana⁶⁶,Nijhuis Roel⁶⁷^ORCID,Nikolaeva-Glomb Lubomira⁴⁹,Nordbø Svein A⁶⁸,Numanovic Sanela³⁵,Oggioni Massimo⁶⁹,Oñate Vergara Eider⁶⁴,Pacaud Jordi⁴⁸,Pacreau Marie L⁶⁰,Panning Marcus³³,Pariani Elena⁴⁷,Pekova Lili⁷⁰,Pellegrinelli Laura⁴⁷,Petrovec Miroslav⁷¹,Pietsch Corinna⁵²,Pilorge Léa⁷²,Piñeiro Luis⁶⁴,Piralla Antonio¹⁴,Poljak Mario⁵⁹,Prochazka Birgit⁷³,Rabella Nuria¹⁸,Rahamat-Langendoen Janette C⁶³,Rainetova Petra⁵⁵,Reynders Marijke⁷⁴^ORCID,Riezebos-Brilman Annelies²²,Roorda Lieuwe⁷⁵,Savolainen-Kopra Carita²¹,Schuffenecker Isabelle⁵⁴,Smeets Leo C⁷⁶,Stoyanova Asya⁴⁹,Stefic Karl⁷⁷^ORCID,Swanink Caroline⁴⁵,Tabain Irena⁵³,Tjhie Jeroen¹⁶³²,Thouault Luc⁷²,Tumiotto Camille⁴⁸,Uceda Renteria Sara²⁸^ORCID,Uršič Tina⁷¹,Vallet Sophie⁷²,Van Ranst Marc²⁰,Van Wunnik Peter⁷⁶,Verweij Jaco J³²,Vila Jorgina⁷⁸,Wintermans Bas⁵⁷,Wollants Elke²⁰,Wolthers Katja C⁷⁹,Xavier López-Labrador F³⁶³⁷^ORCID,Fischer Thea Kolsen⁸⁰⁸¹^ORCID,Harvala Heli⁸²⁸³,Benschop Kimberley S M¹^ORCID

Affiliation:

1. Centre for Infectious Disease Control, Dutch National Public Health Institute , Bilthoven , The Netherlands

2. European Program for Public Health Microbiology Training, European Centre for Disease Prevention and Control , Stockholm , Sweden

3. Geneva Center of Emerging Viral Diseases, Geneva University Hospital and University of Geneva , Geneva , Switzerland

4. Swiss Institute of Bioinformatics , Lausanne , Switzerland

5. Institute of Social and Preventive Medicine, University of Bern , Bern , Switzerland

6. Nuffield Department for Medicine, University of Oxford , Oxford , United Kingdom

7. Department of Clinical Microbiology, Karolinska University Hospital , Stockholm , Sweden

8. Department of Microbiology, Tumor, and Cell Biology, Karolinska Institutet , Stockholm , Sweden

9. Laboratoire de Virologie ULR, Univ Lille, Centre Hospitalier Universitaire de Lille , Lille , France

10. National Reference Centre for Gastroenteritis Viruses, Laboratory of Virology-Serology, University Hospital of Dijon Bourgogne , Dijon , France

11. Respiratory Viruses Unit, Microbiology Department, Vall d’Hebron Hospital Universitari, Vall d’Hebron Institut of Research, Vall d‘Hebron Barcelona Hospital Campus , Barcelona , Spain

12. Microbiology Department, Hospital Unviersitario La Paz, Centro de Investigación Biomédica en Red de Enfermedades Infecciosas, Instituto de Salud Carlos III , Madrid , Spain

13. Labaratoire Microorganismes: Génome Environnement-Epidemiology and Physiopathology of Enterovirus Diseases LMGE-EPIE Team, Université Clermont Auvergne , CNRS, Clermont-Ferrand , France

14. Microbiology and Virology Department, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Policlinico San Matteo , Pavia , Italy

15. Department of Clinical Surgical Diagnostic and Pediatric Sciences, Università Degli Studi di Pavia , Pavia , Italy

16. Laboratory for Medical Microbiology , Eurofins-PAMM, Veldhoven , The Netherlands

17. Enteric Virus Unit, UK Health Security Agency , London , United Kingdom

18. Microbiology Department, Hospital Universitari de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona , Barcelona , Spain

19. National Laboratory of Health, Environment, and Food, Laboratory for Public Health Virology , Ljubljana , Slovenia

20. Clinical and Epidemiological Virology, Rega Institute, Katholieke Universiteit Leuven , Leuven , Belgium

21. Department of Health Security, Expert Microbiology Unit, Finnish Institute for Health and Welfare , Helsinki , Finland

22. Laboratory for Medical Microbiology and Public Health , Hengelo , The Netherlands

23. National Reference Laboratory for Poliomyelitis and Enteroviruses, Robert Koch Institute , Berlin , Germany

24. European Non-Polio Enterovirus Network

25. GFO Kliniken Bonn, Betriebsstätte St Marien , Bonn , Germany

26. Enterovirus and Viral Gastroenteritis Lab, National Centre for Microbiology, Instituto de Salud Carlos III and the Spanish Research Networks Consortium of Epidemiology and Public Health , Madrid , Spain

27. Pediatric and Infectious Diseases Department, Hospital Universtiario La Paz, Fundación IdiPaz, Centro de Investigación Biomédica en Red de Enfermedades Infecciosas, Instituto de Salud Carlos III , Madrid , Spain

28. Virology Unit, Fondazione Istituto di Ricovero e Cura a Carattere Scientifico Ca’ Granda Ospedale Maggiore Policlinico , Milan , Italy

29. Clinical Microbiology, Nottingham University Hospitals National Health Service Trust , Nottingham , United Kingdom

30. National Reference Laboratory for Influenza and Other Respiratory Viruses, National Institute of Health Dr Ricardo Jorge , Lisbon , Portugal

31. Virology Department, Centre Hospitalier Universitaire Hôtel Dieu, University Hospital , Nantes , France

32. Microvida, Laboratory of Medical Microbiology and Immunology, Elisabeth Tweesteden Hospital , Tilburg , The Netherlands

33. Institute of Virology, Medical Center University of Freiburg, Faculty of Medicine, University of Freiburg , Freiburg , Germany

34. National Virus Reference Laboratory, University College Dublin , Dublin , Ireland

35. Department of Virology, Norwegian Institute of Public Health , Oslo , Norway

36. Center for Public Health Research (Foundation for the Promotion of Health and Biomedical Research in the Valencian Community), Generalitat Valenciana , Valencia , Spain

37. Spanish Research Networks Consortium of Epidemiology and Public Health, Instituto de Salud Carlos III , Madrid Spain

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

39. Laboratoire de Virologie, Département de Biologie des Agents Infectieux, Centre Hospitalier Universitaire Angers , Angers , France

40. Department of Microbiology, Oslo University Hospital , Oslo , Norway

41. Insititute of Clinical Medicine, University of Oslo , Oslo , Norway

42. Insitute of Virology, Medical Faculty, University Bonn , Bonn , Germany

43. National Public Health Center , Budapest , Hungary

44. Regional Virus Laboratory, Belfast Health and Social Care Trust, Royal Victoria Hospital , Belfast , United Kingdom

45. Laboratory for Medical Microbiology and Immunology, Rijnstate , Velp , The Netherlands

46. Danish World Health Organization National Reference Laboratory for Poliovirus, Statens Serum Institut , Copenhagen , Denmark

47. Department of Biomedical Sciences for Health, University of Milan , Milan , Italy

48. Virology Department, University Hospital of Bordeaux , Bordeaux , France

49. National Reference Laboratory for Enteroviruses, National Center of Infectious and Parasitic Diseases , Sofia , Bulgaria

50. Department of Medical Microbiology, St Jansdal Hospital , Harderwijk , The Netherlands

51. National Reference Centre for Enteroviruses and Parechoviruses-Associated Laboratory, Centre Hospitalier Universitaire Clermont-Ferrand , Clermont-Ferrand , France

52. Institute of Medical Microbiology and Virology, University of Leipzig , Leipzig , Germany

53. Department of Virology, Croatian Institute of Public Health , Zagreb , Croatia

54. National Reference Center for Enteroviruses and Parechoviruses, Institut des Agents Infectieux, Hospices Civils de Lyon , Lyon , France

55. National Reference Laboratory for Enteroviruses, National Institute of Public Health , Prague , Czech Republic

56. Commission for Polio Eradication in Germany, Robert Koch Institute , Berlin , Germany

57. Laboratory Medical Microbiology and Immunology, Admiraal de Ruijter Hospital , Goes , The Netherlands

58. Department of Medical Microbiology, St Olavs Hospital, Trondheim University Hospital , Trondheim , Norway

59. Institute of Microbiology and Immunology, Faculty of Medicine, University of Ljubljana , Ljubljana , Slovenia

60. Service de Biologie, Centre Hospitalier de Versailles Le Chesnay , France

61. Wolfson Centre for Global Virus Research, School of Life Sciences, University of Nottingham , Nottingham , United Kingdom

62. Pediatric Infectious Diseases Unit, Hospital Universitario Virgen de la Arrixaca , Murcia , Spain

63. Department of Viroscience, Erasmus Medical Center , Rotterdam , The Netherlands

64. Microbiology Department, Donostia University Hospital and Biogipuzkoa Health Research Institute , San Sebastián , Spain

65. Microbiology Department, Hospital Clínico Universitario Virgen de la Arrixaca, Instituto Murciano De Investigación Biosanitaria Arrixaca, Murcia University , Murcia , Spain

66. Microbiology Department, Complejo Hospitalario de Navarra , Navarra , Spain

67. Department of Medical Microbiology and Immunology, Meander Medical Center , Amersfoort , The Netherlands

68. Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology , Trondheim , Norway

69. Microbiology and Virology Unit, Department of Diagnostic Services, Azienda Socio Sanitaria Territoriale della Brianza , Vimercate , Italy

70. Clinic of Infectious Diseases, University Hospital Prof Dr Stoyan Kirkovich AD , Stara Zagora , Bulgaria

71. Institute of Microbiology and Immunology, Laboratory for the Diagnosis of Viral Infections, Faculty of Medicine, University of Ljubljana , Ljubljana , Slovenia

72. Unité de Virologie, Département de Bactériologie-Virologie-Parasitologie-Mycologie-Hygiène, Pôle de Biologie-Pathologie, Centre Hospitalier Régional et Universitaire de Brest , Brest Cedex , France

73. Austrian Agency for Health and Food Safety, National Reference Laboratory for Poliomyelitis , Vienna , Austria

74. Laboratory Medicine, Molecular Microbiology, AZ St Jan Brugge-Oostende AV , Bruges , Belgium

75. Department of Medical Microbiology, Maasstad Hospital , Rotterdam , The Netherlands

76. Department of Medical Microbiology, Reinier Haga Medical Diagnostic Center , Delft , The Netherlands

77. Laboratoire de Virologie INSERM U1259, Centre Hospitalier Régional, Universitaire de Tours , Tours , France

78. Paediatric Hospital Medicine, Department of Paediatrics, Hospital Universitari Vall d'Hebron , Barcelona , Spain

79. Department of Medical Microbiology, OrganoVIR Labs, Amsterdam University Medical Centers , Amsterdam , The Netherlands

80. Department of Clinical Research, Nordsjællands Hospital , Hilleroed , Denmark

81. Department of Public Health, University of Copenhagen , Copenhagen , Denmark

82. Nuffield Division of Clinical Laboratory Sciences, Radcliffe Department of Medicine , Oxford , United Kingdom

83. National Health Service Blood and Transplant, Microbiology Services , Colindale , United Kingdom

Abstract

Abstract Enterovirus D68 (EV-D68) infections are associated with severe respiratory disease and acute flaccid myelitis (AFM). The European Non-Polio Enterovirus Network (ENPEN) aimed to investigate the epidemiological and genetic characteristics of EV-D68 infections and its clinical impact during the fall-winter season of 2021–2022. From 19 European countries, 58 institutes reported 10 481 (6.8%) EV-positive samples of which 1004 (9.6%) were identified as EV-D68 (including 852 respiratory samples). Clinical data were reported for 969 cases; 78.9% of infections were reported in children (0–5 years); and 37.9% of cases were hospitalized. Acute respiratory distress was commonly noted (93.1%) followed by fever (49.4%). Neurological problems were observed in 6.4% of cases including 6 diagnosed with AFM. Phylodynamic/Nextstrain and phylogenetic analyses based on 694 sequences showed the emergence of 2 novel B3-derived lineages, with no regional clustering. In conclusion, we describe a large-scale European EV-D68 upsurge with severe clinical impact and the emergence of B3-derived lineages.

Funder

Austrian Ministry of Health

Czechia Ministry of Health

Foundation for Influenza Epidemiology

Santé Publique France

European Union

Ministry of Health

Welfare and Sport, The Netherlands

National Health Insurance

National Surveillance Program

Slovenian Research Agency

UK Clinical Virology Network