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Abstract

INTRODUCTION

Enterovirus D68 (EV-D68) is a re-emerging pathogen that can cause acute respiratory illness in children and difficult to predict outbreaks.

AIM

To anticipate outbreaks in children, we investigated if wastewater surveillance could timely detect circulation of EV-D68 and its respective subclades in Niigata City, Japan.

METHODS

During January−December 2024, wastewater samples were collected once a week for EV-D68 RNA concentration determination. Numbers of children (≤ 15 years old) admitted with wheezing to six hospitals with paediatric beds in Niigata City were monitored; in a subset of children, nasopharyngeal swabs were tested for EV-D68 during September−December. Nucleotide sequences of EV-D68 derived from patient and wastewater samples were phylogenetically analysed.

RESULTS

During January−December 2024, EV-D68 RNA was found in 39 (41.9%) of 93 wastewater samples. The first EV-D68 detection occurred in week 27, with RNA concentrations rising in subsequent samples. From week 32, numbers of children hospitalised with wheezing increased, peaking in week 37. Up to week 52, 195 children with wheezing were admitted to the six hospitals. The wastewater EV-D68 RNA concentrations positively correlated with paediatric hospitalisations for wheezing (ρ = 0.54, p < 0.001). In weeks 37–52, 16 (10 girls/6 boys; median age: 4.8 years; interquartile range: 3.1–7.5) of 31 hospitalised children tested for EV-D68 were positive. Strains affecting them were of subclade B3 only, while strains in wastewater belonged to subclades D1 and B3.

CONCLUSIONS

Wastewater surveillance timely detected an increase in EV-D68 activity, revealing the circulation of subclades undetected among patients. It thus can potentially support EV-D68 outbreak prediction and response and could possibly be extended to other pathogens.

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This work is licensed under a Creative Commons Attribution 4.0 International License.
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2026-05-21
2026-06-10
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References

  1. Grizer CS, Messacar K, Mattapallil JJ. Enterovirus-D68 - a reemerging non-polio enterovirus that causes severe respiratory and neurological disease in children. Front Virol. 2024;4:1378129.  https://doi.org/10.3389/fviro.2024.1378129  PMID: 39246649 
  2. Holm-Hansen CC, Midgley SE, Fischer TK. Global emergence of enterovirus D68: a systematic review. Lancet Infect Dis. 2016;16(5):e64-75.  https://doi.org/10.1016/S1473-3099(15)00543-5  PMID: 26929196 
  3. Simoes MP, Hodcroft EB, Simmonds P, Albert J, Alidjinou EK, Ambert-Balay K, et al. Epidemiological and clinical insights into the enterovirus D68 upsurge in Europe 2021–2022 and the emergence of novel B3-derived lineages, ENPEN multicentre study. J Infect Dis. 2024;230(4):jiae154.  https://doi.org/10.1093/infdis/jiae154  PMID: 38547499 
  4. Cao RG, Mejias A, Leber AL, Wang H. Clinical and molecular characteristics of the 2022 Enterovirus-D68 outbreak among hospitalized children, Ohio, USA. J Clin Virol. 2023;169:105618.  https://doi.org/10.1016/j.jcv.2023.105618  PMID: 37977074 
  5. Ikuse T, Aizawa Y, Yamanaka T, Habuka R, Watanabe K, Otsuka T, et al. Outbreak of enterovirus D68 among children in Japan-worldwide circulation of enterovirus D68 clade B3 in 2018. Pediatr Infect Dis J. 2021;40(1):6-10.  https://doi.org/10.1097/INF.0000000000002889  PMID: 32947598 
  6. Ikuse T, Aizawa Y, Kachikawa R, Kamata K, Osada H, Win SMK, et al. Detection of enterovirus D68 among children with severe acute respiratory infection in Myanmar. J Microbiol Immunol Infect. 2024;57(2):238-45.  https://doi.org/10.1016/j.jmii.2024.01.001  PMID: 38233293 
  7. Jallow M, Mendy M, Barry M, Diagne M, Sagne S, Tall F, et al. Real-time Enterovirus D68 outbreak detection through hospital surveillance of severe acute respiratory infection, Senegal, 2023. Emerg Infect Dis. 2024;30(8):1687-91.  https://doi.org/10.3201/eid3008.240410  PMID: 39043450 
  8. Fall A, Ndiaye N, Messacar K, Kebe O, Jallow MM, Harouna H, et al. Enterovirus D68 subclade B3 in children with acute flaccid paralysis in West Africa, 2016. Emerg Infect Dis. 2020;26(9):2227-30.  https://doi.org/10.3201/eid2609.200312  PMID: 32818390 
  9. Bal A, Sabatier M, Wirth T, Coste-Burel M, Lazrek M, Stefic K, et al. Emergence of enterovirus D68 clade D1, France, August to November 2018. Euro Surveill. 2019;24(3):1800446.  https://doi.org/10.2807/1560-7917.ES.2019.24.3.1800699  PMID: 30670143 
  10. Korematsu S, Nagashima K, Sato Y, Nagao M, Hasegawa S, Nakamura H, et al. "Spike" in acute asthma exacerbations during enterovirus D68 epidemic in Japan: A nation-wide survey. Allergol Int. 2018;67(1):55-60.  https://doi.org/10.1016/j.alit.2017.04.003  PMID: 28455155 
  11. Chong PF, Kira R, Mori H, Okumura A, Torisu H, Yasumoto S, et al. , Acute Flaccid Myelitis Collaborative Study Investigators. Clinical features of acute flaccid myelitis temporally associated with an enterovirus D68 outbreak: results of a nationwide survey of acute flaccid paralysis in Japan, August-December 2015. Clin Infect Dis. 2018;66(5):653-64.  https://doi.org/10.1093/cid/cix860  PMID: 29028962 
  12. Parkins MD, Lee BE, Acosta N, Bautista M, Hubert CRJ, Hrudey SE, et al. Wastewater-based surveillance as a tool for public health action: SARS-CoV-2 and beyond. Clin Microbiol Rev. 2024;37(1):e0010322.  https://doi.org/10.1128/cmr.00103-22  PMID: 38095438 
  13. Ando H, Murakami M, Ahmed W, Iwamoto R, Okabe S, Kitajima M. Wastewater-based prediction of COVID-19 cases using a highly sensitive SARS-CoV-2 RNA detection method combined with mathematical modeling. Environ Int. 2023;173:107743.  https://doi.org/10.1016/j.envint.2023.107743  PMID: 36867995 
  14. Niigata City. The central part sewage-treatment plant. [cited 2025 Jan 28]. https://www.city.niigata.lg.jp/kurashi/jyogesuido/gesui/gesuishisetsu/shori/chubu.html
  15. Niigataken-Gesuidou-Kousha. Niigata Wastewater Treatment Plant. [cited 2025 Jan 28]. http://www.niigata-gesuikou.or.jp/information
  16. Ikuse T, Aizawa Y, Takihara H, Okuda S, Watanabe K, Saitoh A. Development of novel PCR assays for improved detection of enterovirus D68. J Clin Microbiol. 2021;59(11):e01151-21.  https://doi.org/10.1128/JCM.01151-21  PMID: 34432489 
  17. Kitajima M, Haramoto E, Phanuwan C, Katayama H, Furumai H. Molecular detection and genotyping of human noroviruses in influent and effluent water at a wastewater treatment plant in Japan. J Appl Microbiol. 2012;112(3):605-13.  https://doi.org/10.1111/j.1365-2672.2012.05231.x  PMID: 22221550 
  18. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725-9.  https://doi.org/10.1093/molbev/mst197  PMID: 24132122 
  19. Niigata City. The latest population data. [Accessed 28 Jan 2025]. https://www.city.niigata.lg.jp/shisei/gaiyo/profile/00_01jinkou/index.html
  20. The R Foundation. The R Project for Statistical Computing. Vienna, Austria. [Accessed: 14 Jul 2024]. Available from: https://www.r-project.org.
  21. Pariani E, Piralla A, Pellegrinelli L, Giardina F, Porrello VN, Romano G, et al. , Respiratory viruses pandemic preparedness group Lombardy. Enhanced laboratory surveillance of respiratory infection disclosed the rapid rise of enterovirus D68 cases, northern Italy, August to September 2024. Euro Surveill. 2024;29(41):2400645.  https://doi.org/10.2807/1560-7917.ES.2024.29.41.2400645  PMID: 39392006 
  22. Messacar K, Matzinger S, Berg K, Weisbeck K, Butler M, Pysnack N, et al. Multimodal surveillance model for enterovirus D68 respiratory disease and acute flaccid myelitis among children in Colorado, USA, 2022. Emerg Infect Dis. 2024;30(3):423-31.  https://doi.org/10.3201/eid3003.231223  PMID: 38407198 
  23. Boehm AB, Wadford DA, Hughes B, Duong D, Chen A, Padilla T, et al. Trends of enterovirus D68 concentrations in wastewater, California, USA, February 2021–April 2023. Emerg Infect Dis. 2023;29(11):2362-5.  https://doi.org/10.3201/eid2911.231080  PMID: 37877593 
  24. Tedcastle A, Wilton T, Pegg E, Klapsa D, Bujaki E, Mate R, et al. Detection of enterovirus D68 in wastewater samples from the UK between July and November 2021. Viruses. 2022;14(1):143.  https://doi.org/10.3390/v14010143  PMID: 35062346 
  25. Rector A, Bloemen M, Thijssen M, Delang L, Raymenants J, Thibaut J, et al. Monitoring of SARS-CoV-2 concentration and circulation of variants of concern in wastewater of Leuven, Belgium. J Med Virol. 2023;95(2):e28587.  https://doi.org/10.1002/jmv.28587  PMID: 36799251 
  26. Bisseux M, Colombet J, Mirand A, Roque-Afonso AM, Abravanel F, Izopet J, et al. Monitoring human enteric viruses in wastewater and relevance to infections encountered in the clinical setting: a one-year experiment in central France, 2014 to 2015. Euro Surveill. 2018;23(7):1700237.  https://doi.org/10.2807/1560-7917.ES.2018.23.7.17-00237  PMID: 29471623 
  27. Weil M, Mandelboim M, Mendelson E, Manor Y, Shulman L, Ram D, et al. Human enterovirus D68 in clinical and sewage samples in Israel. J Clin Virol. 2017;86:52-5.  https://doi.org/10.1016/j.jcv.2016.11.013  PMID: 27930928 
  28. Erster O, Bar-Or I, Levy V, Shatzman-Steuerman R, Sofer D, Weiss L, et al. Monitoring of enterovirus D68 outbreak in Israel by a parallel clinical and wastewater based surveillance. Viruses. 2022;14(5):1010.  https://doi.org/10.3390/v14051010  PMID: 35632752 
  29. Howson-Wells HC, Tsoleridis T, Zainuddin I, Tarr AW, Irving WL, Ball JK, et al. Enterovirus D68 epidemic, UK, 2018, was caused by subclades B3 and D1, predominantly in children and adults, respectively, with both subclades exhibiting extensive genetic diversity. Microb Genom. 2022;8(5):mgen000813.  https://doi.org/10.1099/mgen.0.000825  PMID: 35532121 
  30. Andrés C, Vila J, Creus-Costa A, Piñana M, González-Sánchez A, Esperalba J, et al. Enterovirus D68 in hospitalized children, Barcelona, Spain, 2014-2021. Emerg Infect Dis. 2022;28(7):1327-31.  https://doi.org/10.3201/eid2807.220264  PMID: 35731133 
  31. Lau SK, Yip CC, Zhao PS, Chow WN, To KK, Wu AK, et al. Enterovirus D68 infections associated with severe respiratory illness in elderly patients and emergence of a novel clade in Hong Kong. Sci Rep. 2016;6(1):25147.  https://doi.org/10.1038/srep25147  PMID: 27121085 
  32. Duval M, Mirand A, Lesens O, Bay JO, Caillaud D, Gallot D, et al. Retrospective study of the upsurge of enterovirus D68 clade D1 among adults (2014-2018). Viruses. 2021;13(8):1607.  https://doi.org/10.3390/v13081607  PMID: 34452471 
Prospective use of wastewater surveillance for early detection of enterovirus D68 in community outbreaks among children, Niigata City, Japan, 2024
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Jun+Tachikawa&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tachikawa Jun</a>, <a href="/search?value1=Yuta+Aizawa&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Aizawa Yuta</a>, <a href="/search?value1=Rie+Habuka&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Habuka Rie</a>, <a href="/search?value1=Kotaro+Tsushima&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tsushima Kotaro</a>, <a href="/search?value1=Nur+Irma+Safitri&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Safitri Nur Irma</a>, <a href="/search?value1=Tatsuki+Ikuse&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ikuse Tatsuki</a>, <a href="/search?value1=Masaaki+Kitajima&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kitajima Masaaki</a>, <a href="/search?value1=Akihiko+Saitoh&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Saitoh Akihiko</a></span>. Prospective use of wastewater surveillance for early detection of enterovirus D68 in community outbreaks among children, Niigata City, Japan, 2024. <a href="/content/ecdc">Euro Surveill.</a> 2026;31(20):pii=2500779. <a href="https://doi.org/10.2807/1560-7917.ES.2026.31.20.2500779" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2026.31.20.2500779</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 09 Oct 2025;&nbsp;&nbsp; <span class="generated">Accepted</span>: 19 Jan 2026 </span> </p>
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