Abstract
Enterovirus D68 (EV-D68) is a respiratory virus that primarily affects children and has been associated with sporadic outbreaks of respiratory illness worldwide. In the present study, temporal spreading and molecular evolution of EV-D68 clades (A1, A2, B, B1, B2, B3, and C) were evaluated. Bayesian coalescent analysis was performed to study viral evolution. Data from 976 whole-genome sequences (WGSs) collected between 1977 and 2022 were evaluated. For A1, the most recent common ancestor was dated to 2005-04-17 in the USA; for A2 it was 2003-12-23 in China; for B, it was 2003-07-06 in China; for B1, it was 2010-03-21 in Vietnam; for B2, it was 2006-11-25 in Vietnam; for B3, it was 2011-01-15 in China; and for C, it was 2000-06-27 in the USA. The molecular origin of EV-D68 was in Canada in 1995, and later it was disseminated in France in 1997, the USA in 1999, Asia in 2008, the Netherlands in 2009, New Zealand in 2010, Mexico in 2014, Kenya in 2015, Sweden in 2016, Switzerland in 2018, Spain in 2018, Belgium in 2018, Australia in 2018, and Denmark in 2019. In 2022, this virus circulated in the USA. In conclusion, EV-D68 originated in Canada in the 1990s and spread to Europe, Asia, Oceania, Latin America, and Africa.
Data availability
Data sharing is not applicable to this article, as no new data were created or analyzed in this study.
Bibliography
Tapparel C, Siegrist F, Petty TJ, Kaiser L (2013) Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 14:282–293. https://doi.org/10.1016/j.meegid.2012.10.016
Jubelt B, Lipton HL (2014) Enterovirus/picornavirus infections. Handb Clin Neurol 123:379–416. https://doi.org/10.1016/B978-0-444-53488-0.00018-3
de Crom SC, Rossen JW, van Furth AM, Obihara CC (2016) Enterovirus and parechovirus infection in children: a brief overview. Eur J Pediatr 175(8):1023–1029. https://doi.org/10.1007/s00431-016-2725-7
Pham NTK, Thongprachum A, Trinh QD, Okitsu S, Komine-Aizawa S, Shimizu H, Hayakawa S, Ushijima H (2018) Detection and genetic characterization of enterovirus strains circulating among children with acute gastroenteritis in Japan during 2014–2016. Infect Genet Evol 61:16–19. https://doi.org/10.1016/j.meegid.2018.03.009
CDC, Centers for Disease Control and Prevention, Non-Polio Enteroviruses (2020) Available: https://www.cdc.gov/non-polio-enterovirus/index.html; Access: June 2023
Elrick MJ, Pekosz A, Duggal P (2021) Enterovirus D68 molecular and cellular biology and pathogenesis. J Biol Chem 296:100317. https://doi.org/10.1016/j.jbc.2021.100317
Sooksawasdi Na Ayudhya S, Laksono BM, van Riel D (2021) The pathogenesis and virulence of enterovirus-D68 infection. Virulence 12(1):2060–2072. https://doi.org/10.1080/21505594.2021.1960106
Andrés C, Vila J, Creus-Costa A, Piñana M, González-Sánchez A, Esperalba J, Codina MG, Castillo C, Martín MC, Fuentes F, Rubio S, García-Comuñas K, Vásquez- Mercado R, Saubi N, Rodrigo C, Pumarola T, Antón A (2022) Enterovirus D68 in Hospitalized Children, Barcelona, Spain, 2014–2021. Emerg Infect Dis 28(7):1327–1331. https://doi.org/10.3201/eid2807.220264
Fischer TK, Simmonds P, Harvala H (2022) The importance of enterovirus surveillance in a post-polio world. Lancet Infect Dis 22(1):e35–e40. https://doi.org/10.1016/S1473-3099(20)30852-5
Sun J, Hu XY, Yu XF (2019) Current Understanding of Human Enterovirus D68. Viruses 11(6):490. https://doi.org/10.3390/v11060490
Hu Y, Musharrafieh R, Zheng M, Wang J (2020) Enterovirus D68 Antivirals: Past, Present, and Future. ACS Infect Dis 6(7):1572–1586. https://doi.org/10.1021/acsinfecdis.0c00120
Hadfield J, Megill C, Bell SM et al (2018) Nextstrain: real-time tracking of pathogen evolution. Kelso J, ed. Bioinformatics. ;34(23):4121–4123. https://doi.org/10.1093/bioinformatics/bty407
Kumar G, Ertel A, Feldman G, Kupper J, Fortina P (2020) iSeqQC: a tool for expression-based quality control in RNA sequencing. BMC Bioinformatics 21(1):56. https://doi.org/10.1186/s12859-020-3399-8
Sagulenko P, Puller V, Neher RA, TreeTime (2018) Maximum-likelihood phylodynamic analysis. Virus Evol 4(1). https://doi.org/10.1093/ve/vex042
Robert E, Kass, Adrian E Raftery. Bayes Factors, J Am Stat Assoc. 90:430, 773–795, https://doi.org/10.1080/01621459.1995.10476572
Fall A, Kenmoe S, Ebogo-Belobo JT, Mbaga DS, Bowo-Ngandji A, Foe-Essomba JR, Tchatchouang S, Amougou Atsama M, Yéngué JF, Kenfack-Momo R, Feudjio AF, Nka AD, Mbongue Mikangue CA, Taya-Fokou JB, Magoudjou-Pekam JN, Noura EA, Zemnou-Tepap C, Meta-Djomsi D, Maïdadi-Foudi M, Kame-Ngasse GI, Nyebe I, Djukouo LG, Kengne Gounmadje L, Tchami Ngongang D, Oyono MG, Demeni Emoh CP, Tazokong HR, Mahamat G, Kengne-Ndé C, Sadeuh-Mba SA, Dia N, La Rosa G, Ndip L, Njouom R (2022a) Global prevalence and case fatality rate of Enterovirus D68 infections, a systematic review and meta-analysis. PLoS Negl Trop Dis 16(2):e0010073. https://doi.org/10.1371/journal.pntd.0010073
Ikuse T, Aizawa Y, Yamanaka T, Habuka R, Watanabe K, Otsuka T, Saitoh A (2021) Outbreak of Enterovirus D68 Among Children in Japan-Worldwide Circulation of Enterovirus D68 Clade B3 in 2018. Pediatr Infect Dis J 40(1):6–10. https://doi.org/10.1097/INF.0000000000002889
Pellegrinelli L, Giardina F, Lunghi G, Uceda Renteria SC, Greco L, Fratini A, Galli C, Piralla A, Binda S, Pariani E, Baldanti F (2018) Emergence of divergente enterovirus (EV) D68 sub-clade D1 strains, northern Italy, September to October 2018. Euro Surveill 24(7):1900090. https://doi.org/10.2807/1560-7917.ES.2018.24.7.1900090
Liu Y, Gong C, Luo M, Zhang T, Li M, Shen L, Zhang H, Huang F (2021) Seroepidemiology of enterovirus D68 in a healthy population in Beijing, China, between 2012 and 2017: A retrospective study. J Med Virol 93(6):3524–3531. https://doi.org/10.1002/jmv.26132
Park SW, Pons-Salort M, Messacar K, Cook C, Meyers L, Farrar J, Grenfell BT (2021) Epidemiological dynamics of enterovirus D68 in the United States and implications for acute flaccid myelitis. Sci Transl Med 13(584):eabd2400. https://doi.org/10.1126/scitranslmed.abd2400
Shah MM, Perez A, Lively JY, Avadhanula V, Boom JA, Chappell J, Englund JA, Fregoe W, Halasa NB, Harrison CJ, Hickey RW, Klein EJ, McNeal MM, Michaels MG, Moffatt ME, Otten C, Sahni LC, Schlaudecker E, Schuster JE, Selvarangan R, Staat MA, Stewart LS, Weinberg GA, Williams JV, Ng TFF, Routh JA, Gerber SI, McMorrow ML, Rha B, Midgley CM (2021) Enterovirus D68-Associated Acute Respiratory Illness New Vaccine Surveillance Network, United States, July-November 2018–2020. MMWR Morb Mortal Wkly Rep 70(47):1623–1628. https://doi.org/10.15585/mmwr.mm7047a1
Chan YF, Sam IC, Nayan E, Tan XH, Yogarajah T (2022) Seroepidemiology of enterovirus D68 infection in Kuala Lumpur, Malaysia between 2013 and 2015. J Med Virol 94(6):2607–2612. https://doi.org/10.1002/jmv.27381
Hodcroft EB, Dyrdak R, Andrés C, Egli A, Reist J, García Martínez de Artola D, Alcoba-Flórez J, Niesters HGM, Antón A, Poelman R, Reynders M, Wollants E, Neher RA, Albert J (2022) Evolution, geographic spreading, and demographic distribution of Enterovirus D68. PLoS Pathog 18(5):e1010515. https://doi.org/10.1371/journal.ppat.1010515
Larsson SB, Vracar D, Karlsson M, Ringlander J, Norder H (2022) Epidemiology and clinical manifestations of different enterovirus and rhinovirus types show that EV-D68 may still have an impact on severity of respiratory infections. J Med Virol 94(8):3829–3839. https://doi.org/10.1002/jmv.27767
Fall A, Gallagher N, Morris CP, Norton JM, Pekosz A, Klein E, Mostafa HH (2022b) Circulation of Enterovirus D68 during Period of Increased Influenza-Like Illness, Maryland, USA, 2021. Emerg Infect Dis 28(7):1525–1527. https://doi.org/10.3201/eid2807.212603
Benschop KS, Albert J, Anton A, Andrés C, Aranzamendi M, Armannsdóttir B, Bailly JL, Baldanti F, Baldvinsdóttir GE, Beard S, Berginc N, Böttcher S, Blomqvist S, Bubba L, Calvo C, Cabrerizo M, Cavallero A, Celma C, Ceriotti F, Costa I, Cottrell S, Del Cuerpo M, Dean J, Dembinski JL, Diedrich S, Diez-Domingo J, Dorenberg D, Duizer E, Dyrdak R, Fanti D, Farkas A, Feeney S, Flipse J, De Gascun C, Galli C, Georgieva I, Gifford L, Guiomar R, Hönemann M, Ikonen N, Jeannoël M, Josset L, Keeren K, López-Labrador FX, Maier M, McKenna J, Meijer A, Mengual-Chuliá B, Midgley SE, Mirand A, Montes M, Moore C, Morley U, Murk JL, Nikolaeva-Glomb L, Numanovic S, Oggioni M, Palminha P, Pariani E, Pellegrinelli L, Piralla A, Pietsch C, Piñeiro L, Rabella N, Rainetova P, Uceda Renteria SC, Romero MP, Reynders M, Roorda L, Savolainen-Kopra C, Schuffenecker I, Soynova A, Swanink CM, Ursic T, Verweij JJ, Vila J, Vuorinen T, Simmonds P, Fischer TK, Harvala H (2021) Re-emergence of enterovirus D68 in Europe after easing the COVID-19 lockdown, September 2021. Euro Surveill 26(45):2100998. https://doi.org/10.2807/1560-7917.ES.2021.26.45.2100998
Ebada MA, Fayed N, Alkanj S, Allah AW, Enterovirus (2021) D-68 Molecular Virology, Epidemiology, and Treatment: an Update and Way Forward. Infect Disord Drug Targets 21(3):320–327. https://doi.org/10.2174/1871526520666200715101230
Fang Y, Chen Q, Wang H, Wang L, Rong H, Liao Q, Dong C (2021) The role of conformational epitopes in the evolutionary divergence of enterovirus D68 clades: A bioinformatics-based study. Infect Genet Evol 93:104992. https://doi.org/10.1016/j.meegid.2021.104992
Tan Y, Hassan F, Schuster JE, Simenauer A, Selvarangan R, Halpin RA, Lin X, Fedorova N, Stockwell TB, Lam TT, Chappell JD, Hartert TV, Holmes EC, Das SR (2015) Molecular Evolution and Intraclade Recombination of Enterovirus D68 during the 2014 Outbreak in the United States. J Virol 90(4):1997–2007. https://doi.org/10.1128/JVI.02418-15
Gong YN, Yang SL, Shih SR, Huang YC, Chang PY, Huang CG, Kao KC, Hu HC, Liu YC, Tsao KC (2016) Molecular evolution and the global reemergence of enterovirus D68 by genome-wide analysis. Med (Baltim) 95(31):e4416. https://doi.org/10.1097/MD.0000000000004416
Wollants E, Beller L, Beuselinck K, Bloemen M, Lagrou K, Reynders M, Van Ranst M (2019) A decade of enterovirus genetic diversity in Belgium. J Clin Virol 121:104205. https://doi.org/10.1016/j.jcv.2019.104205
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares no conflicts of interest.
Additional information
Communicated by Akbar Dastjerdi
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material
Rights and permissions
About this article
Cite this article
Wolf, J. Insights into the molecular evolution of enterovirus D68. Arch Virol 168, 268 (2023). https://doi.org/10.1007/s00705-023-05894-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00705-023-05894-4