{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T14:09:07Z","timestamp":1790258947293,"version":"4.1.0"},"reference-count":53,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2024,6,24]],"date-time":"2024-06-24T00:00:00Z","timestamp":1719187200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institute of Public Health NIH\u2014National Research Institute","award":["2BWBW\/2021"],"award-info":[{"award-number":["2BWBW\/2021"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>After the first phase of the COVID-19 pandemic in Europe, a new highly pathogenic variant of echovirus 11 (E11) was detected. The aim of this study was to analyze the genetic diversity of Polish E11 environmental and clinical strains circulating between 2017 and 2023 as well as compare them with E11 strains isolated from severe neonatal sepsis cases reported in Europe between 2022 and 2023. Additionally, the study explores the effectiveness of environmental monitoring in tracking the spread of new variants. For this purpose, the complete sequences of the VP1 capsid protein gene were determined for 266 E11 strains isolated in Poland from 2017 to 2023, and phylogenetic analysis was performed. In the years 2017\u20132023, a significant increase in the detection of E11 strains was observed in both environmental and clinical samples in Poland. The Polish E11 strains represented three different genotypes, C3, D5 and E, and were characterized by a high diversity. In Poland, the intensive circulation of the new variant E11, responsible for severe neonatal infections with a high mortality in Europe, was detected in the years 2022\u20132023. This investigation demonstrates the important role of environmental surveillance in the tracking of enteroviruses circulation, especially in settings with limited clinical surveillance.<\/jats:p>","DOI":"10.3390\/v16071011","type":"journal-article","created":{"date-parts":[[2024,6,24]],"date-time":"2024-06-24T13:06:40Z","timestamp":1719234400000},"page":"1011","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Intensified Circulation of Echovirus 11 after the COVID-19 Pandemic in Poland: Detection of a Highly Pathogenic Virus Variant"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3702-1297","authenticated-orcid":false,"given":"Beata","family":"Gad","sequence":"first","affiliation":[{"name":"Department of Virology, National Institute of Public Health NIH\u2014National Research Institute, Chocimska 24, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paulina","family":"K\u0142osiewicz","sequence":"additional","affiliation":[{"name":"Department of Virology, National Institute of Public Health NIH\u2014National Research Institute, Chocimska 24, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kinga","family":"Oleksiak","sequence":"additional","affiliation":[{"name":"Department of Virology, National Institute of Public Health NIH\u2014National Research Institute, Chocimska 24, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arleta","family":"Krzysztoszek","sequence":"additional","affiliation":[{"name":"Department of Virology, National Institute of Public Health NIH\u2014National Research Institute, Chocimska 24, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0309-6987","authenticated-orcid":false,"given":"Kacper","family":"Toczy\u0142owski","sequence":"additional","affiliation":[{"name":"Department of Pediatric Infectious Diseases, Medical University of Bialystok, Waszyngtona 17, 15-274 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8391-4793","authenticated-orcid":false,"given":"Artur","family":"Sulik","sequence":"additional","affiliation":[{"name":"Department of Pediatric Infectious Diseases, Medical University of Bialystok, Waszyngtona 17, 15-274 Bialystok, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tobiasz","family":"Wieczorek","sequence":"additional","affiliation":[{"name":"Faculty of Civil Engineering and Geodesy, Military University of Technology, Gen. S. Kaliskiego 2, 00-908 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8770-5131","authenticated-orcid":false,"given":"Magdalena","family":"Wieczorek","sequence":"additional","affiliation":[{"name":"Department of Virology, National Institute of Public Health NIH\u2014National Research Institute, Chocimska 24, 00-791 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,24]]},"reference":[{"key":"ref_1","first-page":"1","article-title":"Centers for Disease Control and Prevention. Enterovirus surveillance-United States, 1970\u20132005","volume":"55","author":"Khetsuriani","year":"2006","journal-title":"MMWR Surveill. Summ."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/S1473-3099(19)30566-3","article-title":"Enterovirus study collaborators. Circulation of non-polio enteroviruses in 24 EU and EEA countries between 2015 and 2017: A retrospective surveillance study","volume":"20","author":"Bubba","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Wang, J., Meng, M., Xu, H., Wang, T., Liu, Y., Yan, H., Liu, P., Qin, D., and Yang, Q. (2021). Analysis of enterovirus genotypes in the cerebrospinal fluid of children associated with aseptic meningitis in Liaocheng, China, from 2018 to 2019. BMC Infect. Dis., 21.","DOI":"10.1186\/s12879-021-06112-9"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"7679","DOI":"10.1128\/AEM.02058-13","article-title":"Prevalence of nonpolio enteroviruses in the sewage of Guangzhou city, China, from 2009 to 2012","volume":"79","author":"Zheng","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Huang, S., Zhang, Y., Zhang, W., Chen, M., Li, C., Guo, X., Zhu, S., Zeng, H., Fang, L., and Ke, B. (2023). Prevalence of Non-Polio Enteroviruses in the Sewage of Guangzhou City, China, from 2013 to 2021. Microbiol. Spectr., 11.","DOI":"10.1128\/spectrum.03632-22"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1007\/s12560-015-9195-3","article-title":"Environmental Surveillance of Non-polio Enteroviruses in Poland, 2011","volume":"7","author":"Wieczorek","year":"2015","journal-title":"Food Environ. Virol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1038\/s41390-023-02930-6","article-title":"Laboratory diagnosis of CNS infections in children due to emerging and re-emerging neurotropic viruses","volume":"95","author":"Liu","year":"2024","journal-title":"Pediatr. Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1002\/jmv.24933","article-title":"Non-polio Enterovirus detection with acute flaccid paralysis: A systematic review","volume":"90","author":"Suresh","year":"2018","journal-title":"J. Med. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2343","DOI":"10.1007\/s00705-015-2496-x","article-title":"Molecular characterization of a new human echovirus 11 isolate associated with severe hand, foot and mouth disease in Yunnan, China, in 2010","volume":"160","author":"Su","year":"2015","journal-title":"Arch. Virol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/s705-002-8307-2","article-title":"Phylogenetic and serological characterization of echovirus 11 and echovirus 19 strains causing uveitis","volume":"147","author":"Lukashev","year":"2002","journal-title":"Arch. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1097\/00000441-196012000-00009","article-title":"Acute gastroenteritis associated with ECHO virus, Type 11","volume":"240","author":"Klein","year":"1960","journal-title":"Am. J. Med. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2575","DOI":"10.1007\/s007050070009","article-title":"Nucleotide sequences and mutations of the 5\u2032-nontranslated region (5\u2032NTR) of natural isolates of an epidemic echovirus 11\u2032 (prime)","volume":"145","author":"Mezey","year":"2000","journal-title":"Arch. Virol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Wang, C., Yang, R., Yang, F., Han, Y., Ren, Y., Xiong, X., Wang, X., Bi, Y., Li, L., and Qiu, Y. (2022). Echovirus 11 infection induces pyroptotic cell death by facilitating NLRP3 inflammasome activation. PLoS Pathog., 18.","DOI":"10.1371\/journal.ppat.1010787"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Zhang, M., Wang, H., Tang, J., He, Y., Xiong, T., Li, W., Qu, Y., and Mu, D. (2021). Clinical characteristics of severe neonatal enterovirus infection: A systematic review. BMC Pediatr., 21.","DOI":"10.1186\/s12887-021-02599-y"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.jcv.2013.11.003","article-title":"A case of congenital Echovirus 11 infection acquired early in pregnancy","volume":"59","author":"Tassin","year":"2014","journal-title":"J. Clin. Virol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1097\/01.inf.0000148931.05186.99","article-title":"Vertical transmission of human echovirus 11 at the time of Bornholm disease in late pregnancy","volume":"24","author":"Tang","year":"2005","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1016\/j.jmii.2023.05.004","article-title":"Serostatus of echovirus 11, coxsackievirus B3 and enterovirus D68 in cord blood: The implication of severe newborn enterovirus infection","volume":"56","author":"Hu","year":"2023","journal-title":"J. Microbiol. Immunol. Infect."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Laassri, M., Zagorodnyaya, T., Hassin-Baer, S., Handsher, R., Sofer, D., Weil, M., Karagiannis, K., Simonyan, V., Chumakov, K., and Shulman, L. (2018). Evolution of echovirus 11 in a chronically infected immunodeficient patient. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1006943"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.pedneo.2019.09.012","article-title":"Investigation and successful control of an echovirus 11 outbreak in neonatal intensive care units","volume":"61","author":"Ho","year":"2020","journal-title":"Pediatr. Neonatol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1186\/s12985-022-01821-2","article-title":"Detection of recombinant breakpoint in the genome of human enterovirus E11 strain associated with a fatal nosocomial outbreak","volume":"19","author":"Rueca","year":"2022","journal-title":"Virol. J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1017\/S0950268801005404","article-title":"An outbreak of echovirus 11 in a children\u2019s home","volume":"126","author":"Somekh","year":"2001","journal-title":"Epidemiol. Infect."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1007\/s11262-012-0719-8","article-title":"Evaluating the prevalence and molecular epidemiology of echovirus 11 isolated from sewage in Shandong Province, China in 2010","volume":"44","author":"Yang","year":"2012","journal-title":"Virus Genes"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Bubba, L., Benschop, K.S.M., Blomqvist, S., Duizer, E., Martin, J., Shaw, A.G., Bailly, J.L., Rasmussen, L.D., Baicus, A., and Fischer, T.K. (2023). Wastewater Surveillance in Europe for Non-Polio Enteroviruses and Beyond. Microorganisms, 11.","DOI":"10.3390\/microorganisms11102496"},{"key":"ref_24","unstructured":"World Health Organization (2023, July 07). Disease Outbreak News. Enterovirus-Echovirus 11 Infection in the European Region. Available online: https:\/\/www.who.int\/emergencies\/disease-outbreak-news\/item\/2023-DON474."},{"key":"ref_25","unstructured":"European Centre for Disease Prevention and Control (2023, July 19). Epidemiological Update, Epidemiological Update: Echovirus 11 Infections in Neonates. Available online: https:\/\/www.ecdc.europa.eu\/en\/news-events\/epidemiological-update-echovirus-11-infections-neonates."},{"key":"ref_26","unstructured":"European Centre for Disease Control and Prevention (2023, June 16). Communicable Disease Threat Report, Weekly Bulletin. Available online: https:\/\/www.ecdc.europa.eu\/sites\/default\/files\/documents\/communicable-disease-threats-report-16-jun-2023.pdf."},{"key":"ref_27","unstructured":"World Health Organization (2023, May 31). Disease Outbreak News. Enterovirus Infection\u2014France 31 May 2023. Available online: https:\/\/www.who.int\/emergencies\/disease-outbreak-news\/item\/2023-DON469."},{"key":"ref_28","unstructured":"European Centre for Disease Control (ECDC) (2023, June 15). Echovirus 11 in Newly Born Twins: Case in Italy Shows Close Genetic Relation to Strains Found in France among Neonates. Available online: https:\/\/www.eurekalert.org\/news-releases\/992726."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2300253","DOI":"10.2807\/1560-7917.ES.2023.28.22.2300253","article-title":"Severe and fatal neonatal infections linked to a new variant of echovirus 11, France, July 2022 to April 2023","volume":"28","author":"Grapin","year":"2023","journal-title":"Eurosurveillance"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2300289","DOI":"10.2807\/1560-7917.ES.2023.28.24.2300289","article-title":"Fulminant echovirus 11 hepatitis in male non-identical twins in northern Italy, April 2023","volume":"28","author":"Piralla","year":"2023","journal-title":"Eurosurveillance"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"10583","DOI":"10.1038\/s41598-019-46870-w","article-title":"Multiple genotypes of Echovirus 11 circulated in mainland China between 1994 and 2017","volume":"9","author":"Li","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0168-1702(02)00291-5","article-title":"Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East","volume":"91","author":"Oberste","year":"2003","journal-title":"Virus Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5608","DOI":"10.1128\/AEM.02764-07","article-title":"Isolation of sabin-like polioviruses from wastewater in a country using inactivated polio vaccine","volume":"74","author":"Zurbriggen","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_34","unstructured":"WHO Expanded Programme on Immunization & World Health Organization Division of Communicable Diseases (2022, June 03). World Health Organization Manual for the Virological Investigation of Poliomyelitis. Available online: https:\/\/apps.who.int\/iris\/handle\/10665\/62186."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.jcv.2008.11.015","article-title":"Direct identification of human enterovirus serotypes in cerebrospinal fluid by amplification and sequencing of the VP1 region","volume":"44","author":"Leitch","year":"2009","journal-title":"J. Clin. Virol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1111\/2041-210X.12410","article-title":"PopART: Full Feature Software for Haplotype Network Construction","volume":"6","author":"Leigh","year":"2015","journal-title":"Methods Evol. Ecol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"105381","DOI":"10.1016\/j.jcv.2023.105381","article-title":"Disruption of seasonal enterovirus and parechovirus detections in the CSF and plasma of children during the COVID-19 pandemic","volume":"160","author":"Lee","year":"2023","journal-title":"J. Clin. Virol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"105617","DOI":"10.1016\/j.jcv.2023.105617","article-title":"Changes in enterovirus epidemiology after easing of lockdown measures","volume":"169","author":"Forero","year":"2023","journal-title":"J. Clin. Virol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.bsheal.2023.05.003","article-title":"Analysis of the distribution characteristics of enterovirus types based on environmental surveillance from 2013 to 2021 in Fujian Province, China","volume":"5","author":"Yang","year":"2023","journal-title":"Biosaf. Health"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"7181","DOI":"10.1128\/AEM.69.12.7181-7187.2003","article-title":"Assessment of an enterovirus sewage surveillance system by comparison of clinical isolates with sewage isolates from milwaukee, wisconsin, collected August 1994 to December 2002","volume":"69","author":"Sedmak","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Ivanova, O.E., Yarmolskaya, M.S., Eremeeva, T.P., Babkina, G.M., Baykova, O.Y., Akhmadishina, L.V., Krasota, A.Y., Kozlovskaya, L.I., and Lukashev, A.N. (2019). Environmental Surveillance for Poliovirus and Other Enteroviruses: Long-Term Experience in Moscow, Russian Federation, 2004\u20132017. Viruses, 11.","DOI":"10.3390\/v11050424"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1186\/s12985-018-1075-7","article-title":"Assessment of enteroviruses from sewage water and clinical samples during eradication phase of polio in North India","volume":"15","author":"Tiwari","year":"2018","journal-title":"Virol. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1007\/s12560-018-9350-8","article-title":"Poliovirus and Other Enteroviruses from Environmental Surveillance in Italy, 2009\u20132015","volume":"10","author":"Delogu","year":"2018","journal-title":"Food Environ. Virol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e01604-19","DOI":"10.1128\/AEM.01604-19","article-title":"Environmental Surveillance Can Dynamically Track Ecological Changes in Enteroviruses","volume":"85","author":"Ozawa","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Kitakawa, K., Kitamura, K., and Yoshida, H. (2023). Monitoring Enteroviruses and SARS-CoV-2 in Wastewater Using the Polio Environmental Surveillance System in Japan. Appl. Environ. Microbiol., 89.","DOI":"10.1128\/aem.01853-22"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"170519","DOI":"10.1016\/j.scitotenv.2024.170519","article-title":"Detection of Echovirus 11 lineage 1 in wastewater samples in Sicily","volume":"918","author":"Giammanco","year":"2024","journal-title":"Sci. Total Environ."},{"key":"ref_48","first-page":"157","article-title":"Characterisation of an echovirus type 11\u2032 (prime) epidemic strain causing haemorrhagic syndrome in newborn babies in Hungary","volume":"42","author":"Uj","year":"1998","journal-title":"Acta Virol."},{"key":"ref_49","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_50","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1097\/00006454-198501000-00009","article-title":"Maternal and neonatal neutralizing antibody titers to selected enteroviruses","volume":"4","author":"Hammond","year":"1985","journal-title":"Pediatr. Infect. Dis."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.meegid.2014.12.033","article-title":"Molecular epidemiology of echoviruses 11 and 30 in Russia: Different properties of genotypes within an enterovirus serotype","volume":"30","author":"Yarmolskaya","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"ofy250","DOI":"10.1093\/ofid\/ofy250","article-title":"Environmental Surveillance Reveals Complex Enterovirus Circulation Patterns in Human Populations","volume":"5","author":"Majumdar","year":"2018","journal-title":"Open Forum Infect. Dis."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1128\/JCM.01801-16","article-title":"Universal PCR Primers Are Critical for Direct Sequencing-Based Enterovirus Genotyping","volume":"55","author":"Liu","year":"2016","journal-title":"J. Clin. Microbiol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/7\/1011\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:03:40Z","timestamp":1760108620000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/7\/1011"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,24]]},"references-count":53,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2024,7]]}},"alternative-id":["v16071011"],"URL":"https:\/\/doi.org\/10.3390\/v16071011","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,24]]}}}