{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T19:44:58Z","timestamp":1790624698883,"version":"4.1.0"},"reference-count":44,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2021,5,11]],"date-time":"2021-05-11T00:00:00Z","timestamp":1620691200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Enteroviruses are associated with various diseases accompanied by rare but severe complications. In recent years, outbreaks of enterovirus D68 and enterovirus A71 associated with severe respiratory infections and neurological complications have been reported worldwide. Since information on molecular epidemiology in respiratory samples is still limited, the genetic diversity of enteroviruses was retrospectively analysed over a 4-year period (2013\u20132016) in respiratory samples from paediatric patients. Partial viral major capsid protein gene (VP1) sequences were determined for genotyping. Enteroviruses were detected in 255 (6.1%) of 4187 specimens. Phylogenetic analyses of 233 (91.4%) strains revealed 25 different genotypes distributed to Enterovirus A (39.1%), Enterovirus B (34.3%), and Enterovirus D (26.6%). The most frequently detected genotypes were enterovirus D68 (26.6%), coxsackievirus A6 (15.9%), and enterovirus A71 (7.3%). Enterovirus D68 detections were associated with lower respiratory tract infections and increased oxygen demand. Meningitis\/encephalitis and other neurological symptoms were related to enterovirus A71, while coxsackievirus A6 was associated with upper respiratory diseases. Prematurity turned out as a potential risk factor for increased oxygen demand during enterovirus infections. The detailed analysis of epidemiological and clinical data contributes to the non-polio enterovirus surveillance in Europe and showed high and rapidly changing genetic diversity of circulating enteroviruses, including different enterovirus D68 variants.<\/jats:p>","DOI":"10.3390\/v13050882","type":"journal-article","created":{"date-parts":[[2021,5,11]],"date-time":"2021-05-11T22:53:40Z","timestamp":1620773620000},"page":"882","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Enteroviruses in Respiratory Samples from Paediatric Patients of a Tertiary Care Hospital in Germany"],"prefix":"10.3390","volume":"13","author":[{"given":"Susanne","family":"Baertl","sequence":"first","affiliation":[{"name":"Institute of Medical Microbiology and Virology, Leipzig University Hospital, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6029-3368","authenticated-orcid":false,"given":"Corinna","family":"Pietsch","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Virology, Leipzig University Hospital, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie","family":"Maier","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Virology, Leipzig University Hospital, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"H\u00f6nemann","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Virology, Leipzig University Hospital, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra","family":"Bergs","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Virology, Leipzig University Hospital, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5129-0875","authenticated-orcid":false,"given":"Uwe G.","family":"Liebert","sequence":"additional","affiliation":[{"name":"Institute of Medical Microbiology and Virology, Leipzig University Hospital, 04103 Leipzig, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Kaslow, R.A., Stanberry, L.R., and Le Duc, J.W. (2014). Enteroviruses and Parechoviruses: Echoviruses, Coxsackieviruses, and Others. Viral Infections of Humans, Springer US.","DOI":"10.1007\/978-1-4899-7448-8"},{"key":"ref_2","unstructured":"(2019, December 19). Picornavirus Home. Available online: https:\/\/www.picornaviridae.com."},{"key":"ref_3","first-page":"839","article-title":"Enteroviruses","volume":"Volume 1","author":"Knipe","year":"2006","journal-title":"Fields Virology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2698","DOI":"10.1128\/JCM.00542-06","article-title":"Sensitive, Seminested PCR Amplification of VP1 Sequences for Direct Identification of All Enterovirus Serotypes from Original Clinical Specimens","volume":"44","author":"Nix","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.jcv.2018.01.008","article-title":"Recommendations for enterovirus diagnostics and characterisation within and beyond Europe","volume":"101","author":"Harvala","year":"2018","journal-title":"J. Clin. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Royston, L., and Tapparel, C. (2016). Rhinoviruses and Respiratory Enteroviruses: Not as Simple as ABC. Viruses, 8.","DOI":"10.3390\/v8010016"},{"key":"ref_7","first-page":"1023","article-title":"Enterovirus and parechovirus infection in children: A brief overview","volume":"175","author":"Rossen","year":"2016","journal-title":"Eur. J. Nucl. Med. Mol. Imaging"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1016\/j.meegid.2012.10.016","article-title":"Picornavirus and enterovirus diversity with associated human diseases","volume":"14","author":"Tapparel","year":"2013","journal-title":"Infect. Genet. Evol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"719","DOI":"10.3201\/eid1505.081286","article-title":"New Respiratory Enterovirus and Recombinant Rhinoviruses among Circulating Picornaviruses","volume":"15","author":"Tapparel","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.jcv.2018.11.004","article-title":"Surveillance of enteroviruses from paediatric patients attended at a tertiary hospital in Catalonia from 2014 to 2017","volume":"110","author":"Vila","year":"2019","journal-title":"J. Clin. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1177\/0009922818809483","article-title":"The Resource Burden of Infections with Rhinovirus\/Enterovirus, Influenza, and Respiratory Syncytial Virus in Children","volume":"58","author":"Fine","year":"2018","journal-title":"Clin. Pediatr."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1016\/S1473-3099(10)70194-8","article-title":"Virology, epidemiology, pathogenesis, and control of enterovirus","volume":"10","author":"Solomon","year":"2010","journal-title":"Lancet Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e64","DOI":"10.1016\/S1473-3099(15)00543-5","article-title":"Global emergence of enterovirus D68: A systematic review","volume":"16","author":"Midgley","year":"2016","journal-title":"Lancet Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"352","DOI":"10.1016\/j.cmi.2017.02.010","article-title":"The importance of enterovirus surveillance in a Post-polio world","volume":"23","author":"Midgley","year":"2017","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"20935","DOI":"10.2807\/1560-7917.ES2014.19.42.20935","article-title":"Continued seasonal circulation of enterovirus D68 in the Netherlands, 2011","volume":"19","author":"Meijer","year":"2014","journal-title":"Eurosurveillance"},{"key":"ref_16","unstructured":"(2018, April 23). Rapid Risk Assessment\u2014Enterovirus Detections Associated with Severe Neurological Symptoms in Children and Adults in European Countries, 8 August 2016. Available online: https:\/\/www.ecdc.europa.eu\/sites\/portal\/files\/media\/en\/publications\/Publications\/01-08-2016-RRA-Enterovirus%2071-Spain,%20France,%20Netherlands.pdf."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1097\/INF.0000000000002289","article-title":"Enterovirus D68 Causing Acute Respiratory Infection: Clinical Characteristics and Differences with Acute Respiratory Infections Associated With Enterovirus Non-D","volume":"38","author":"Montes","year":"2019","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3007","DOI":"10.1002\/jmv.25765","article-title":"Genotyping of enteroviruses and human parechoviruses highlights their diversity in Northwest Ethiopia","volume":"92","author":"Gelaw","year":"2020","journal-title":"J. Med. Virol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.jcv.2011.03.006","article-title":"An automated genotyping tool for enteroviruses and noroviruses","volume":"51","author":"Kroneman","year":"2011","journal-title":"J. Clin. Virol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1002\/jmv.24658","article-title":"Molecular epidemiology of enterovirus and parechovirus infections according to patient age over a 4-year period in Spain","volume":"89","author":"Cabrerizo","year":"2017","journal-title":"J. Med. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jcv.2014.11.011","article-title":"The emergence of enterovirus D68 in a Dutch University Medical Center and the necessity for routinely screening for respiratory viruses","volume":"62","author":"Poelman","year":"2015","journal-title":"J. Clin. Virol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jcv.2015.07.296","article-title":"European surveillance for enterovirus D68 during the emerging North-American outbreak in 2014","volume":"71","author":"Poelman","year":"2015","journal-title":"J. Clin. Virol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1438","DOI":"10.1080\/22221751.2019.1668243","article-title":"Enterovirus D68-associated respiratory and neurological illness in Spain, 2014","volume":"8","author":"Taravillo","year":"2019","journal-title":"Emerg. Microbes Infect."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.jcv.2018.01.005","article-title":"Enterovirus-D68 (EV-D68) in pediatric patients with respiratory infection: The circulation of a new B3 clade in Italy","volume":"99\u2013100","author":"Piralla","year":"2018","journal-title":"J. Clin. Virol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"140","DOI":"10.3201\/eid2301.161313","article-title":"Upsurge of Enterovirus D68, the Netherlands","volume":"23","author":"Knoester","year":"2017","journal-title":"Emerg. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"30403","DOI":"10.2807\/1560-7917.ES.2016.21.46.30403","article-title":"Outbreak of enterovirus D68 of the new B3 lineage in Stockholm, Sweden, August to September","volume":"21","author":"Dyrdak","year":"2016","journal-title":"Eurosurveillance"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1700711","DOI":"10.2807\/1560-7917.ES.2018.23.37.1700711","article-title":"Molecular diversity and biennial circulation of enterovirus D68: A systematic screening study in Lyon, France, 2010 to 2016","volume":"23","author":"Kramer","year":"2018","journal-title":"Eurosurveillance"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1590","DOI":"10.1002\/jmv.23821","article-title":"Phylogenetic characterization of enterovirus 68 strains in patients with respiratory syndromes in Italy","volume":"86","author":"Piralla","year":"2013","journal-title":"J. Med. Virol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Benschop, K.S.M., Rahamat-Langendoen, J.C., Van Der Avoort, H.G.A.M., Claas, E.C.J., Pas, S.D., Schuurman, R., Verweij, J.J., Wolthers, K.C., Niesters, H.G.M., and Koopmans, M.P.G. (2016). VIRO-TypeNed, systematic molecular surveillance of enteroviruses in the Netherlands between 2010 and 2014. Eurosurveillance, 21.","DOI":"10.2807\/1560-7917.ES.2016.21.39.30352"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.jcv.2016.01.014","article-title":"Prospective assessment of clinical symptoms associated with enterovirus and parechovirus genotypes in a multicenter study in Dutch children","volume":"77","author":"Rossen","year":"2016","journal-title":"J. Clin. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Antona, D., Kossorotoff, M., Schuffenecker, I., Mirand, A., Leruez-Ville, M., Bassi, C., Aubart, M., Moulin, F., L\u00e9vy-Bruhl, D., and Henquell, C. (2016). Severe paediatric conditions linked with EV-A71 and EV-D68, France, May to October. Eurosurveillance, 21.","DOI":"10.2807\/1560-7917.ES.2016.21.46.30402"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"B\u00f6ttcher, S., Prifert, C., Wei\u00dfbrich, B., Adams, O., Aldabbagh, S., Eis-H\u00fcbinger, A.M., and Diedrich, S. (2016). Detection of enterovirus D68 in patients hospitalised in three tertiary university hospitals in Germany, 2013 to 2014. Eurosurveillance, 21.","DOI":"10.2807\/1560-7917.ES.2016.21.19.30227"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1097\/01.inf.0000237798.07462.32","article-title":"Neonatal Enterovirus Infections Reported to the National Enterovirus Surveillance System in the United States, 1983\u20132003","volume":"25","author":"Khetsuriani","year":"2006","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"30047","DOI":"10.2807\/1560-7917.ES.2015.20.43.30047","article-title":"Systematic community- and hospital-based surveillance for enterovirus-D68 in three Canadian provinces, August to December","volume":"20","author":"Skowronski","year":"2015","journal-title":"Eurosurveillance"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"837","DOI":"10.3201\/eid2105.141900","article-title":"Low-level Circulation of Enterovirus D68\u2013Associated Acute Respiratory Infections, Germany","volume":"21","author":"Reiche","year":"2015","journal-title":"Emerg. Infect. Dis."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Hixon, A.M., Yu, G., Leser, J.S., Yagi, S., Clarke, P., Chiu, C.Y., and Tyler, K.L. (2017). A mouse model of paralytic myelitis caused by enterovirus D. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006199"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"17-00310","DOI":"10.2807\/1560-7917.ES.2018.23.3.17-00310","article-title":"The association between acute flaccid myelitis (AFM) and Enterovirus D68 (EV-D68)\u2014What is the evidence for causation?","volume":"23","author":"Dyda","year":"2018","journal-title":"Eurosurveillance"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1662","DOI":"10.1016\/S0140-6736(14)62457-0","article-title":"A cluster of acute flaccid paralysis and cranial nerve dysfunction temporally associated with an outbreak of enterovirus D68 in children in Colorado, USA","volume":"385","author":"Messacar","year":"2015","journal-title":"Lancet"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/irv.12300","article-title":"High frequency of enterovirus D68 in children hospitalised with respiratory illness in Norway, autumn 2014","volume":"9","author":"Bragstad","year":"2014","journal-title":"Influ. Other Respir. Viruses"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1136\/jech-2014-203836","article-title":"Enterovirus 71 related severe hand, foot and mouth disease outbreaks in South-East Asia: Current situation and ongoing challenges","volume":"68","author":"Sabanathan","year":"2014","journal-title":"J. Epidemiol. Community Heal."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2826","DOI":"10.1128\/JCM.00507-09","article-title":"Epidemiology of Enterovirus 71 in The Netherlands, 1963 to 2008","volume":"47","author":"Koopmans","year":"2009","journal-title":"J. Clin. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1056\/NEJMoa1304923","article-title":"Efficacy, Safety, and Immunogenicity of an Enterovirus 71 Vaccine in China","volume":"370","author":"Zhu","year":"2014","journal-title":"N. Engl. J. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2677","DOI":"10.3389\/fmicb.2018.02677","article-title":"Enterovirus D68\u2014The New Polio?","volume":"9","author":"Cassidy","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"16-00807","DOI":"10.2807\/1560-7917.ES.2017.22.45.16-00807","article-title":"Surveillance and laboratory detection for non-polio enteroviruses in the European Union\/European Economic Area","volume":"22","author":"Harvala","year":"2017","journal-title":"Eurosurveillance"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/5\/882\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:59:17Z","timestamp":1760162357000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/5\/882"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,11]]},"references-count":44,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["v13050882"],"URL":"https:\/\/doi.org\/10.3390\/v13050882","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,11]]}}}