Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe

Kimberley S. M. Benschop; Eeva K. Broberg; Emma Hodcroft; Dennis Schmitz; Jan Albert; Anda Baicus; Jean-Luc Bailly; Gudrun Baldvinsdottir; Natasa Berginc; Soile Blomqvist; Sindy Böttcher; Mia Brytting; Erika Bujaki; Maria Cabrerizo; Cristina Celma; Ondrej Cinek; Eric C. J. Claas; Jeroen Cremer; Jonathan Dean; Jennifer L. Dembinski; Iryna Demchyshyna; Sabine Diedrich; Susanne Dudman; Jake Dunning; Robert Dyrdak; Mary Emmanouil; Agnes Farkas; Cillian de Gascun; Guillaume Fournier; Irina Georgieva; Ruben Gonzalez-Sanz; Jolanda van Hooydonk-Elving; Anne J. Jääskeläinen; Ruta Jancauskaite; Kathrin Keeren; Thea K. Fischer; Sidsel Krokstad; Lubomira Nikolaeva-Glomb; Ludmila Novakova; Sofie E. Midgley; Audrey Mirand; Richard Molenkamp; Ursula Morley; Joël Mossong; Svajune Muralyte; Jean-Luc Murk; Trung Nguyen; Svein A. Nordbø; Riikka Österback; Suzan Pas; Laura Pellegrinelli; Vassiliki Pogka; Birgit Prochazka; Petra Rainetova; Marc van Ranst; Lieuwe Roorda; Isabelle Schuffenecker; Rob Schuurman; Asya Stoyanova; Kate Templeton; Jaco J. Verweij; Androniki Voulgari-Kokota; Tytti Vuorinen; Elke Wollants; Katja C. Wolthers; Katherina Zakikhany; Richard Neher; Heli Harvala; Peter Simmonds

doi:10.3201/eid2706.203096

Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe

Kimberley S. M. Benschop^*
, Eeva K. Broberg
, Emma Hodcroft
, Dennis Schmitz
, Jan Albert
, Anda Baicus
, Jean-Luc Bailly
, Gudrun Baldvinsdottir
, Natasa Berginc
, Soile Blomqvist
, Sindy Böttcher
, Mia Brytting
, Erika Bujaki
, Maria Cabrerizo
, Cristina Celma
, Ondrej Cinek
, Eric C. J. Claas
, Jeroen Cremer
, Jonathan Dean
, Jennifer L. Dembinski

Iryna Demchyshyna, Sabine Diedrich, Susanne Dudman, Jake Dunning, Robert Dyrdak, Mary Emmanouil, Agnes Farkas, Cillian de Gascun, Guillaume Fournier, Irina Georgieva, Ruben Gonzalez-Sanz, Jolanda van Hooydonk-Elving, Anne J. Jääskeläinen, Ruta Jancauskaite, Kathrin Keeren, Thea K. Fischer, Sidsel Krokstad, Lubomira Nikolaeva-Glomb, Ludmila Novakova, Sofie E. Midgley, Audrey Mirand, Richard Molenkamp, Ursula Morley, Joël Mossong, Svajune Muralyte, Jean-Luc Murk, Trung Nguyen, Svein A. Nordbø, Riikka Österback, Suzan Pas, Laura Pellegrinelli, Vassiliki Pogka, Birgit Prochazka, Petra Rainetova, Marc van Ranst, Lieuwe Roorda, Isabelle Schuffenecker, Rob Schuurman, Asya Stoyanova, Kate Templeton, Jaco J. Verweij, Androniki Voulgari-Kokota, Tytti Vuorinen, Elke Wollants, Katja C. Wolthers, Katherina Zakikhany, Richard Neher, Heli Harvala, Peter Simmonds

^*Corresponding author for this work

National Institute of Public Health and the Environment
European Centre for Disease Prevention and Control
University of Basel
Karolinska Institutet
Cantacuzino, Bucharest, Romania
CHU de Clermont-Ferrand
Landspitali University Hospital
National laboratory of Health, Environment and Food, Ljubljana, Slovenia
National Institute for Health and Welfare
Robert Koch-Institut
Public Health Agency of Sweden
National Public Health Center, Budapest, Hungary
Instituto de Salud Carlos III
UK Health Security Agency
Charles University
Leiden University Medical Center
University College Dublin
World Health Organization
Zaporizhia Medical Academy of Post-Gradate Education Ministry of Health of Ukraine
University of Oslo
Institut Pasteur Helleniqe
Laboratoire National de Santé
National Center of Infectious and Parasitic Diseases Bulgaria
Microvida, Breda, the Netherlands
University of Helsinki
National Public Health Surveillance Laboratory, Vilnius, Lithuania
University of Copenhagen
Norwegian University of Science and Technology
Czech National Institute of Public Health
WHO Regional Office for Europe
Erasmus MC
ETZ Elisabeth
University of Turku
University of Milan
Austrian Agency for Health and Food Safety GmbH
KU Leuven
Department of Internal Medicine and Infectious Diseases, Maasstad Ziekenhuis, Rotterdam, Netherlands
Hospices civils de Lyon
University Medical Center Utrecht
National Health Services Scotland, Edinburgh, Scotland, UK
Amsterdam UMC - University of Amsterdam
University College London
National Health Service, Colindale
University of Oxford

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

Abstract

In 2018, an upsurge in echovirus 30 (E30) infections was reported in Europe. We conducted a large-scale epidemiologic and evolutionary study of 1,329 E30 strains collected in 22 countries in Europe during 2016-2018. Most E30 cases affected persons 0-4 years of age (29%) and 25-34 years of age (27%). Sequences were divided into 6 genetic clades (G1-G6). Most (53%) sequences belonged to G1, followed by G6 (23%), G2 (17%), G4 (4%), G3 (0.3%), and G5 (0.2%). Each clade encompassed unique individual recombinant forms; G1 and G4 displayed >2 unique recombinant forms. Rapid turnover of new clades and recombinant forms occurred over time. Clades G1 and G6 dominated in 2018, suggesting the E30 upsurge was caused by emergence of 2 distinct clades circulating in Europe. Investigation into the mechanisms behind the rapid turnover of E30 is crucial for clarifying the epidemiology and evolution of these enterovirus infections.

Original language	English
Pages (from-to)	1616-1626
Number of pages	11
Journal	Emerging infectious diseases
Volume	27
Issue number	6
DOIs	https://doi.org/10.3201/eid2706.203096
Publication status	Published - 1 Jun 2021

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SDG 3 Good Health and Well-being

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10.3201/eid2706.203096

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Benschop, K. S. M., Broberg, E. K., Hodcroft, E., Schmitz, D., Albert, J., Baicus, A., Bailly, J.-L., Baldvinsdottir, G., Berginc, N., Blomqvist, S., Böttcher, S., Brytting, M., Bujaki, E., Cabrerizo, M., Celma, C., Cinek, O., Claas, E. C. J., Cremer, J., Dean, J., ... Simmonds, P. (2021). Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe. Emerging infectious diseases, 27(6), 1616-1626. https://doi.org/10.3201/eid2706.203096

@article{244e0203570a4880aa13458187230910,

title = "Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe",

abstract = "In 2018, an upsurge in echovirus 30 (E30) infections was reported in Europe. We conducted a large-scale epidemiologic and evolutionary study of 1,329 E30 strains collected in 22 countries in Europe during 2016-2018. Most E30 cases affected persons 0-4 years of age (29\%) and 25-34 years of age (27\%). Sequences were divided into 6 genetic clades (G1-G6). Most (53\%) sequences belonged to G1, followed by G6 (23\%), G2 (17\%), G4 (4\%), G3 (0.3\%), and G5 (0.2\%). Each clade encompassed unique individual recombinant forms; G1 and G4 displayed >2 unique recombinant forms. Rapid turnover of new clades and recombinant forms occurred over time. Clades G1 and G6 dominated in 2018, suggesting the E30 upsurge was caused by emergence of 2 distinct clades circulating in Europe. Investigation into the mechanisms behind the rapid turnover of E30 is crucial for clarifying the epidemiology and evolution of these enterovirus infections.",

author = "Benschop, \{Kimberley S. M.\} and Broberg, \{Eeva K.\} and Emma Hodcroft and Dennis Schmitz and Jan Albert and Anda Baicus and Jean-Luc Bailly and Gudrun Baldvinsdottir and Natasa Berginc and Soile Blomqvist and Sindy B{\"o}ttcher and Mia Brytting and Erika Bujaki and Maria Cabrerizo and Cristina Celma and Ondrej Cinek and Claas, \{Eric C. J.\} and Jeroen Cremer and Jonathan Dean and Dembinski, \{Jennifer L.\} and Iryna Demchyshyna and Sabine Diedrich and Susanne Dudman and Jake Dunning and Robert Dyrdak and Mary Emmanouil and Agnes Farkas and \{de Gascun\}, Cillian and Guillaume Fournier and Irina Georgieva and Ruben Gonzalez-Sanz and \{van Hooydonk-Elving\}, Jolanda and J{\"a}{\"a}skel{\"a}inen, \{Anne J.\} and Ruta Jancauskaite and Kathrin Keeren and Fischer, \{Thea K.\} and Sidsel Krokstad and Lubomira Nikolaeva-Glomb and Ludmila Novakova and Midgley, \{Sofie E.\} and Audrey Mirand and Richard Molenkamp and Ursula Morley and Jo{\"e}l Mossong and Svajune Muralyte and Jean-Luc Murk and Trung Nguyen and Nordb{\o}, \{Svein A.\} and Riikka {\"O}sterback and Suzan Pas and Laura Pellegrinelli and Vassiliki Pogka and Birgit Prochazka and Petra Rainetova and \{van Ranst\}, Marc and Lieuwe Roorda and Isabelle Schuffenecker and Rob Schuurman and Asya Stoyanova and Kate Templeton and Verweij, \{Jaco J.\} and Androniki Voulgari-Kokota and Tytti Vuorinen and Elke Wollants and Wolthers, \{Katja C.\} and Katherina Zakikhany and Richard Neher and Heli Harvala and Peter Simmonds",

note = "Funding Information: The study was supported by the Ministry of Health, Welfare and Sport, the Netherlands as part of the EV surveillance program of the National Institute for Public Health and the Environment; the European Union Horizon 2020 research and innovation program (COMPARE grant no. 643476 from Aristotle University of Thessaloniki, Greece); the Wellcome Trust (grant no. ISSF204826/ Z/16/Z); the Belgian National Reference Center for Enteroviruses from the RIZIV/INAMI (National Institute for Health and Disability Insurance); and the HONOURs Horizon 2020 Marie Sklodowska-Curie Training Network (grant no. 721367). Publisher Copyright: {\textcopyright} 2021 Centers for Disease Control and Prevention (CDC). All rights reserved.",

year = "2021",

month = jun,

day = "1",

doi = "10.3201/eid2706.203096",

language = "English",

volume = "27",

pages = "1616--1626",

journal = "Emerging infectious diseases",

issn = "1080-6040",

publisher = "Centers for Disease Control and Prevention (CDC)",

number = "6",

}

Benschop, KSM, Broberg, EK, Hodcroft, E, Schmitz, D, Albert, J, Baicus, A, Bailly, J-L, Baldvinsdottir, G, Berginc, N, Blomqvist, S, Böttcher, S, Brytting, M, Bujaki, E, Cabrerizo, M, Celma, C, Cinek, O, Claas, ECJ, Cremer, J, Dean, J, Dembinski, JL, Demchyshyna, I, Diedrich, S, Dudman, S, Dunning, J, Dyrdak, R, Emmanouil, M, Farkas, A, de Gascun, C, Fournier, G, Georgieva, I, Gonzalez-Sanz, R, van Hooydonk-Elving, J, Jääskeläinen, AJ, Jancauskaite, R, Keeren, K, Fischer, TK, Krokstad, S, Nikolaeva-Glomb, L, Novakova, L, Midgley, SE, Mirand, A, Molenkamp, R, Morley, U, Mossong, J, Muralyte, S, Murk, J-L, Nguyen, T, Nordbø, SA, Österback, R, Pas, S, Pellegrinelli, L, Pogka, V, Prochazka, B, Rainetova, P, van Ranst, M, Roorda, L, Schuffenecker, I, Schuurman, R, Stoyanova, A, Templeton, K, Verweij, JJ, Voulgari-Kokota, A, Vuorinen, T, Wollants, E, Wolthers, KC, Zakikhany, K, Neher, R, Harvala, H & Simmonds, P 2021, 'Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe', Emerging infectious diseases, vol. 27, no. 6, pp. 1616-1626. https://doi.org/10.3201/eid2706.203096

TY - JOUR

T1 - Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe

AU - Benschop, Kimberley S. M.

AU - Broberg, Eeva K.

AU - Hodcroft, Emma

AU - Schmitz, Dennis

AU - Albert, Jan

AU - Baicus, Anda

AU - Bailly, Jean-Luc

AU - Baldvinsdottir, Gudrun

AU - Berginc, Natasa

AU - Blomqvist, Soile

AU - Böttcher, Sindy

AU - Brytting, Mia

AU - Bujaki, Erika

AU - Cabrerizo, Maria

AU - Celma, Cristina

AU - Cinek, Ondrej

AU - Claas, Eric C. J.

AU - Cremer, Jeroen

AU - Dean, Jonathan

AU - Dembinski, Jennifer L.

AU - Demchyshyna, Iryna

AU - Diedrich, Sabine

AU - Dudman, Susanne

AU - Dunning, Jake

AU - Dyrdak, Robert

AU - Emmanouil, Mary

AU - Farkas, Agnes

AU - de Gascun, Cillian

AU - Fournier, Guillaume

AU - Georgieva, Irina

AU - Gonzalez-Sanz, Ruben

AU - van Hooydonk-Elving, Jolanda

AU - Jääskeläinen, Anne J.

AU - Jancauskaite, Ruta

AU - Keeren, Kathrin

AU - Fischer, Thea K.

AU - Krokstad, Sidsel

AU - Nikolaeva-Glomb, Lubomira

AU - Novakova, Ludmila

AU - Midgley, Sofie E.

AU - Mirand, Audrey

AU - Molenkamp, Richard

AU - Morley, Ursula

AU - Mossong, Joël

AU - Muralyte, Svajune

AU - Murk, Jean-Luc

AU - Nguyen, Trung

AU - Nordbø, Svein A.

AU - Österback, Riikka

AU - Pas, Suzan

AU - Pellegrinelli, Laura

AU - Pogka, Vassiliki

AU - Prochazka, Birgit

AU - Rainetova, Petra

AU - van Ranst, Marc

AU - Roorda, Lieuwe

AU - Schuffenecker, Isabelle

AU - Schuurman, Rob

AU - Stoyanova, Asya

AU - Templeton, Kate

AU - Verweij, Jaco J.

AU - Voulgari-Kokota, Androniki

AU - Vuorinen, Tytti

AU - Wollants, Elke

AU - Wolthers, Katja C.

AU - Zakikhany, Katherina

AU - Neher, Richard

AU - Harvala, Heli

AU - Simmonds, Peter

N1 - Funding Information: The study was supported by the Ministry of Health, Welfare and Sport, the Netherlands as part of the EV surveillance program of the National Institute for Public Health and the Environment; the European Union Horizon 2020 research and innovation program (COMPARE grant no. 643476 from Aristotle University of Thessaloniki, Greece); the Wellcome Trust (grant no. ISSF204826/ Z/16/Z); the Belgian National Reference Center for Enteroviruses from the RIZIV/INAMI (National Institute for Health and Disability Insurance); and the HONOURs Horizon 2020 Marie Sklodowska-Curie Training Network (grant no. 721367). Publisher Copyright: © 2021 Centers for Disease Control and Prevention (CDC). All rights reserved.

PY - 2021/6/1

Y1 - 2021/6/1

N2 - In 2018, an upsurge in echovirus 30 (E30) infections was reported in Europe. We conducted a large-scale epidemiologic and evolutionary study of 1,329 E30 strains collected in 22 countries in Europe during 2016-2018. Most E30 cases affected persons 0-4 years of age (29%) and 25-34 years of age (27%). Sequences were divided into 6 genetic clades (G1-G6). Most (53%) sequences belonged to G1, followed by G6 (23%), G2 (17%), G4 (4%), G3 (0.3%), and G5 (0.2%). Each clade encompassed unique individual recombinant forms; G1 and G4 displayed >2 unique recombinant forms. Rapid turnover of new clades and recombinant forms occurred over time. Clades G1 and G6 dominated in 2018, suggesting the E30 upsurge was caused by emergence of 2 distinct clades circulating in Europe. Investigation into the mechanisms behind the rapid turnover of E30 is crucial for clarifying the epidemiology and evolution of these enterovirus infections.

AB - In 2018, an upsurge in echovirus 30 (E30) infections was reported in Europe. We conducted a large-scale epidemiologic and evolutionary study of 1,329 E30 strains collected in 22 countries in Europe during 2016-2018. Most E30 cases affected persons 0-4 years of age (29%) and 25-34 years of age (27%). Sequences were divided into 6 genetic clades (G1-G6). Most (53%) sequences belonged to G1, followed by G6 (23%), G2 (17%), G4 (4%), G3 (0.3%), and G5 (0.2%). Each clade encompassed unique individual recombinant forms; G1 and G4 displayed >2 unique recombinant forms. Rapid turnover of new clades and recombinant forms occurred over time. Clades G1 and G6 dominated in 2018, suggesting the E30 upsurge was caused by emergence of 2 distinct clades circulating in Europe. Investigation into the mechanisms behind the rapid turnover of E30 is crucial for clarifying the epidemiology and evolution of these enterovirus infections.

UR - https://www.scopus.com/pages/publications/85106520894

U2 - 10.3201/eid2706.203096

DO - 10.3201/eid2706.203096

M3 - Article

C2 - 34013874

SN - 1080-6040

VL - 27

SP - 1616

EP - 1626

JO - Emerging infectious diseases

JF - Emerging infectious diseases

IS - 6

ER -

Molecular epidemiology and evolutionary trajectory of emerging echovirus 30, Europe

Abstract

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