{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T15:21:24Z","timestamp":1788967284394,"version":"build-2803163510"},"reference-count":35,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,6,16]],"date-time":"2023-06-16T00:00:00Z","timestamp":1686873600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>Mumps is a viral infection mainly characterized by inflammation of the parotid glands. Despite of vaccination programs, infections among fully vaccinated populations were reported. The World Health Organization (WHO) recommends molecular surveillance of mumps based on sequencing of the small hydrophobic (SH) gene. The use of hypervariable non-coding regions (NCR) as additional molecular markers was proposed in multiple studies. Circulation of mumps virus (MuV) genotypes and variants in different European countries were described in the literature. From 2010 to 2020, mumps outbreaks caused by genotype G were described. However, this issue has not been analyzed from a wider geographical perspective. In the present study, sequence data from MuV detected in Spain and in The Netherlands during a period of 5\u2009 years (2015- March 2020) were analyzed to gain insights in the spatiotemporal spread of MuV at a larger geographical scale than in previous local studies.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>A total of 1,121 SH and 262 NCR between the Matrix and Fusion protein genes (MF-NCR) sequences from both countries were included in this study. Analysis of SH revealed 106 different haplotypes (set of identical sequences).<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Of them, seven showing extensive circulation were considered variants. All seven were detected in both countries in coincident temporal periods. A single MF-NCR haplotype was detected in 156 sequences (59.3% of total), and was shared by five of the seven SH variants, as well as three minor MF-NCR haplotypes. All SH variants and MF-NCR haplotypes shared by both countries were detected first in Spain.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>Our results suggest a transmission way from south to north Europe. The higher incidence rate of mumps in Spain in spite of similar immunization coverage in both countries, could be associated with higher risk of MuV exportation. In conclusion, the present study provided novel insights into the circulation of MuV variants and haplotypes beyond the borders of single countries. In fact, the use of MF-NCR molecular tool allowed to reveal MuV transmission flows between The Netherlands and Spain. Similar studies including other (European) countries are needed to provide a broader view of the data presented in this study.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2023.1207500","type":"journal-article","created":{"date-parts":[[2023,6,16]],"date-time":"2023-06-16T05:03:31Z","timestamp":1686891811000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Comparison of circulation patterns of mumps virus in the Netherlands and Spain (2015\u20132020)"],"prefix":"10.3389","volume":"14","author":[{"given":"Ana M.","family":"Gavil\u00e1n","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda","family":"van de Nes-Reijnen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Castellanos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tom","family":"Woudenberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noem\u00ed","family":"L\u00f3pez-Perea","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josefa","family":"Masa-Calles","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan E.","family":"Echevarr\u00eda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aurora","family":"Fern\u00e1ndez-Garc\u00eda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rogier","family":"Bodewes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,6,16]]},"reference":[{"key":"ref2","doi-asserted-by":"publisher","first-page":"e0233143","DOI":"10.1371\/journal.pone.0233143","article-title":"Molecular epidemiology of mumps viruses in the Netherlands, 2017\u20132019","volume":"15","author":"Bodewes","year":"2020","journal-title":"PLoS One"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"4393","DOI":"10.1016\/j.vaccine.2014.06.069","article-title":"Mumps increase in Flanders, Belgium, 2012\u20132013: results from temporary mandatory notification and a cohort study among university students","volume":"32","author":"Braeye","year":"2014","journal-title":"Vaccine"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"2932","DOI":"10.1016\/j.vaccine.2010.02.020","article-title":"Mumps outbreak in a highly vaccinated student population, the Netherlands, 2004","volume":"28","author":"Brockhoff","year":"2010","journal-title":"Vaccine"},{"key":"ref500","year":"2023"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"9271","DOI":"10.1016\/j.vaccine.2011.09.072","article-title":"Assessment of serological evidence for mumps virus infection in vaccinated children","volume":"29","author":"Dittrich","year":"2011","journal-title":"Vaccine"},{"key":"ref501","doi-asserted-by":"publisher","first-page":"1245","DOI":"10.1128\/JCM.02386-09","article-title":"Circulation of mumps virus genotypes in Spain from 1996 to 2007","volume":"48","author":"Echevarr\u00eda","year":"2010","journal-title":"J. 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Dis."},{"key":"ref603","doi-asserted-by":"publisher","first-page":"17","DOI":"10.2807\/1560-7917.ES.2018.23.15.17-00349","article-title":"Genomic non-coding regions reveal hidden patterns of mumps virus circulation in Spain, 2005 to 2015","volume":"23","author":"Gavil\u00e1n","year":"2018","journal-title":"Eurosurveillance"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"4676","DOI":"10.1016\/j.vaccine.2012.04.083","article-title":"Mumps outbreak among vaccinated university students associated with a large party, the Netherlands, 2010","volume":"30","author":"Greenland","year":"2012","journal-title":"Vaccine"},{"key":"ref604","article-title":"BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95\/98\/NT","volume":"41","author":"Hall","year":"1999","journal-title":"Nucleic Acids Symp. Ser."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"518","DOI":"10.5281\/zenodo.854445","article-title":"UFBoot2: improving the ultrafast bootstrap approximation","volume":"35","author":"Hoang","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref11","year":""},{"key":"ref12","doi-asserted-by":"publisher","DOI":"10.2807\/1560-7917.ES.2017.22.35.30605","article-title":"Ongoing mumps outbreak in Israel, January to August 2017","volume":"22","author":"Indenbaum","year":"2017","journal-title":"Eur. Secur."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1002\/rmv.1819","article-title":"Genomic diversity of mumps virus and global distribution of the 12 genotypes","volume":"25","author":"Jin","year":"2015","journal-title":"Rev. Med. 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Spain, 1998\u20132014","volume":"35","author":"L\u00f3pez-Perea","year":"2017","journal-title":"Vaccine"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1002\/jmv.25324","article-title":"Mumps outbreak investigation in Jaisalmer, Rajasthan, India, June\u2013September 2016","volume":"91","author":"Moghe","year":"2019","journal-title":"J. Med. Virol."},{"key":"ref16","volume-title":"The National Immunisation Programme in the Netherland","year":"2022"},{"key":"ref17","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0139815","article-title":"A mumps outbreak in vojvodina, Serbia, in 2012 underlines the need for additional vaccination opportunities for young adults","volume":"10","author":"Nedeljkovi\u0107","year":"2015","journal-title":"PLoS One"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1727","DOI":"10.1016\/s0264-410x(00)00392-3","article-title":"Mumps virus neutralizing antibodies do not protect against reinfection with a heterologous mumps virus genotype","volume":"19","author":"N\u00f6 Jd","year":"2001","journal-title":"Vaccine"},{"key":"ref19","doi-asserted-by":"publisher","DOI":"10.3947\/ic.2015.47.1.1","article-title":"Resurgence of mumps in Korea","volume":"47","author":"Park","year":"2015","journal-title":"Infect. Chemother."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1093\/oxfordjournals.aje.a117631","article-title":"Observations on a mumps epidemic in a \u201cvirgin\u201d population","volume":"142","author":"Philip","year":"1995","journal-title":"Am. J. Epidemiol."},{"key":"ref608","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1016\/j.jcv.2011.09.007","article-title":"Mumps virus diagnosis and genotyping using a novel single RT-PCR","volume":"52","author":"Royuela","year":"2011","journal-title":"J. Clin. Virol."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1002\/path.4445","article-title":"Molecular biology, pathogenesis and pathology of mumps virus","volume":"235","author":"Rubin","year":"2015","journal-title":"J. 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