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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Virol.</journal-id>
<journal-title>Frontiers in Virology</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Virol.</abbrev-journal-title>
<issn pub-type="epub">2673-818X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fviro.2024.1515652</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Virology</subject>
<subj-group>
<subject>Editorial</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Editorial: Enterovirus surveillance in Europe and beyond</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Benschop</surname>
<given-names>Kimberley S. M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1265449"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Johannesen</surname>
<given-names>Caroline Klint</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/2406200"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Midgley</surname>
<given-names>Sofie E.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1076071"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Harvala</surname>
<given-names>Heli</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup>&#x2020;</sup>
</xref>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Fischer</surname>
<given-names>Thea K.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/503990"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Centre for Infectious Disease Research, Diagnostics and Laboratory Surveillance (IDS), Centre for Infectious Disease Control (CIb), Institute for Public Health and the Environment (RIVM)</institution>, <addr-line>Bilthoven</addr-line>, <country>Netherlands</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Clinical Research, Nordsj&#xe6;llands Hospital</institution>, <addr-line>Hiller&#xf8;d</addr-line>, <country>Denmark</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Virus &amp; Microbiological Special Diagnostics, Statens Serum Institut</institution>, <addr-line>Copenhagen</addr-line>, <country>Denmark</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>The Danish WHO National Reference Laboratory for Poliovirus, Virus &amp; Microbiological Special Diagnostics, Statens Serum Institut</institution>, <addr-line>Copenhagen</addr-line>, <country>Denmark</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>Microbiology Services, National Health Service (NHS) Blood and Transplant</institution>, <addr-line>London</addr-line>, <country>United Kingdom</country>
</aff>
<aff id="aff6">
<sup>6</sup>
<institution>Division of Infection and Immunity, University College London</institution>, <addr-line>London</addr-line>, <country>United Kingdom</country>
</aff>
<aff id="aff7">
<sup>7</sup>
<institution>Department of Public Health, University of Copenhagen</institution>, <addr-line>Copenhagen</addr-line>, <country>Denmark</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited and Reviewed by: Javier Buesa, University of Valencia, Spain</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Kimberley S. M. Benschop, <email xlink:href="mailto:kim.benschop@rivm.nl">kim.benschop@rivm.nl</email>
</p>
</fn>
<fn fn-type="other" id="fn003">
<p>&#x2020;ORCID: Nadia Sabbah, <uri xlink:href="https://orcid.org/0000-0001-9154-4190">orcid.org/0000-0001-9154-4190</uri>
</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>20</day>
<month>11</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>4</volume>
<elocation-id>1515652</elocation-id>
<history>
<date date-type="received">
<day>23</day>
<month>10</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>30</day>
<month>10</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Benschop, Johannesen, Midgley, Harvala and Fischer</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Benschop, Johannesen, Midgley, Harvala and Fischer</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<related-article id="RA1" related-article-type="commentary-article" xlink:href="https://www.frontiersin.org/research-topics/56177" ext-link-type="uri">Editorial on the Research Topic <article-title>Enterovirus surveillance in Europe and beyond</article-title>
</related-article>
<kwd-group>
<kwd>enterovirus</kwd>
<kwd>circulation patterns</kwd>
<kwd>surveillance</kwd>
<kwd>CNS infection</kwd>
<kwd>seasonal difference</kwd>
</kwd-group>
<counts>
<fig-count count="0"/>
<table-count count="0"/>
<equation-count count="0"/>
<ref-count count="7"/>
<page-count count="3"/>
<word-count count="918"/>
</counts>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-in-acceptance</meta-name>
<meta-value>Viral Disease Investigation</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<p>Enteroviruses (EV) are ubiquitous. Most infections are mild. However severe and even fatal infections occur, in particular among young children. This Research Topic on &#x201c;<italic>Enterovirus Surveillance in Europe and Beyond</italic>&#x201d; entails five research articles on EV circulation in Europe over a prolonged period including the COVID-19 pandemic years of 2020-2021. The studies describe both the epidemiological and clinical characteristics of EV infections, where two studies specifically focus on EV-D68 circulation (<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1335752">Ur&#x161;i&#x10d; et&#xa0;al.</ext-link>, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1358963">Landaas et&#xa0;al.</ext-link>) and a fatal infection of EV-A71 (<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1381001">Nieminem et&#xa0;al.</ext-link>).</p>
<p>Increased circulation of EVs is often seen in the summer and autumn months, though the dominant EV type varies between years. The emergence of EV-D68 and its increased detection among patients with respiratory infection and acute flaccid myelitis has been noted since 2010 (<xref ref-type="bibr" rid="B1">1</xref>, <xref ref-type="bibr" rid="B2">2</xref>). For almost a decade, circulation of EV-D68 was limited to a  biennial seasonal pattern from late summer to early winter (<xref ref-type="bibr" rid="B1">1</xref>, <xref ref-type="bibr" rid="B3">3</xref>) but since 2020, this seasonal pattern has been observed every year (<xref ref-type="bibr" rid="B4">4</xref>).</p>
<p>However, while these patterns may reflect an overall picture of EV circulation dynamics, country and regional based differences need to be accounted for as well, and in particular, the dominating types per region/country and even per reporting institute seem to vary.</p>
<p>The study by <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1346352">Johannesen et&#xa0;al.</ext-link> on EV infections linked to hospitalizations and outpatient visits in Denmark 2015-2022, shows that while the COVID-19 pandemic led to a drastic decrease in number of cases reported, it has not affected the seasonal patterns (also seen by <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1335752">Ur&#x161;i&#x10d; et&#xa0;al.</ext-link>, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1358963">Landaas et&#xa0;al.</ext-link> and <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2023.1343781">Dudman et&#xa0;al.</ext-link> Central nervous system (CNS) infections were commonly found among neonates in hospitalized settings, while skin infections were more common among outpatients. The age distribution of patients with CNS infection and skin infections remained similar before and after the pandemic, with neonates commonly affected with CNS infections and children aged 1-2 years with skin infections respectively. Of interest is that <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2023.1343781">Dudman et&#xa0;al.</ext-link> who studied EV infections from 2016-2022 noted an increase in detection skin infections with coxsackievirus A6 (CVA6), a virus most often associated with skin infections and in particular atypical hand foot and mouth disease. The dominance of CVA6 continued also after the COVID-19 pandemic.</p>
<p>In a similar study period, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1335752">Ur&#x161;i&#x10d; et&#xa0;al.</ext-link> showed a similar seasonal pattern of EV circulation for 2014 and 2016. In addition, they demonstrated EV-D68 circulation in Slovenia during the biannual years pre COVID-19 pandemic, 2014-2016, and hardly any cases after that. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1358963">Landaas et&#xa0;al.</ext-link> also showed an upsurge of EV-D68 cases in these two years in Norway when studying a period from 2012-2022, with low numbers in 2018, 2019 and 2021.</p>
<p>Of interest is that for 2021, a European wide upsurge of EV-D68 was observed following ease of the COVID-19 pandemic restriction (<xref ref-type="bibr" rid="B4">4</xref>) among 58 institutes in 19 European countries participating in the European Non Polio enterovirus network (ENPEN). Sim&#xf5;es et&#xa0;al. indeed stated that large differences in the proportions of EV-D68&#x2013;positive samples were observed among countries/reporting institutes. While most infections in the 2021 study by Sim&#xf5;es et&#xa0;al. were identified among children &lt;5 years of age, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1358963">Landaas et&#xa0;al.</ext-link> and <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1335752">Ur&#x161;i&#x10d; et&#xa0;al.</ext-link> both showed that the pediatric population of Norway and Slovenia deviated from the European wide upsurge in 2021, with hardly any cases being reported. In contrast, <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1358963">Landaas et&#xa0;al.</ext-link> reports a large EV-D68 outbreak in 2022 in the pediatric Norwegian population, yet only two cases were reported by <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2023.1343781">Dudman et&#xa0;al.</ext-link> in Oslo, Norway, despite screening all age groups. The 2022 EV-D68 upsurge was previously not seen by other countries (Sten et&#xa0;al. manuscript in preparation) and also not seen in Slovenia (<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fviro.2024.1335752">Ur&#x161;i&#x10d; et&#xa0;al.</ext-link>).</p>
<p>The studies in this Research Topic show the differences in the epidemiology of EV infections between countries/institutes. This may reflect the true circulation in these countries although its more likely to reflect the lack of standardized public health surveillance guidelines and/or systems, challenging the comparability among these and other studies (<xref ref-type="bibr" rid="B4">4</xref>&#x2013;<xref ref-type="bibr" rid="B7">7</xref>). These include the lack of a uniform case definition and sampling strategy, and differences in screening and typing methods across institutes. In addition, while the European region has set up uniform legal and ethical regulations concerning data sharing, the implementation and interpretation proves to be limiting uniform data sharing. The varied and in some cases incomplete reporting to larger ENPEN studies may lead to biases in the data. As such to understand and better determine the disease burden of EV infection, we need clear standardization of data collection with comprehensive reporting. Utilizing existing surveillance systems for poliovirus and non-polio enteroviruses, enables synergy between the different surveillance systems (clinical, sewage and AFP surveillance) which is needed for overall enterovirus surveillance as for poliovirus surveillance specifically (Fischer et&#xa0;al., manuscript submitted). The final study in this Research Topic reflects on the identification of a fatal case of EV-A71 in 2019. Despite their effort in enhanced communication, surveillance, and typing the overall number of clinical EV positive cases was low in 2019, yet environmental surveillance showed continued circulation of EVs and the EV-A71 strain.</p>
<p>ENPEN is an interdisciplinary consortium which brings together specialists from clinical, diagnostic and research areas including clinical and molecular virology, epidemiology, public health, neurology, and pediatric infectious diseases across Europe and beyond. The main aim of ENPEN is to ensure harmonized, coordinated and standardized (real-time) data sharing and collaborative research.</p>
</body>
<back>
<sec id="s1" sec-type="author-contributions">
<title>Author contributions</title>
<p>KB: Conceptualization, Writing &#x2013; original draft, Writing &#x2013; review &amp; editing. CJ: Conceptualization, Writing &#x2013; review &amp; editing. SM: Conceptualization, Writing &#x2013; review &amp; editing. HH: Conceptualization, Writing &#x2013; review &amp; editing. TF: Conceptualization, Writing &#x2013; review &amp; editing.</p>
</sec>
<sec id="s2" sec-type="COI-statement">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
<p>The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.</p>
</sec>
<sec id="s3" sec-type="disclaimer">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
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