{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T10:06:14Z","timestamp":1789553174895,"version":"build-2803163510"},"reference-count":39,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T00:00:00Z","timestamp":1789516800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T00:00:00Z","timestamp":1789516800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["JPwm0125001"],"award-info":[{"award-number":["JPwm0125001"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["20fk0108119h0001"],"award-info":[{"award-number":["20fk0108119h0001"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["JP24fk0108661"],"award-info":[{"award-number":["JP24fk0108661"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Microbiology and Immunology"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>The mechanisms underlying seasonal patterns in influenza epidemics have long been an enigma. Our laboratory study revealed that ambient ozone significantly inactivates airborne influenza viruses synergistically with higher relative humidity and temperature. This led us to hypothesize that natural seasonal fluctuations in these ambient factors enhance or mitigate the influenza\u2010transmission risk by altering the efficiency of airborne virus inactivation, thereby contributing to the continuation or subsiding of influenza epidemics. To test the hypothesis, we examined datasets covering 5 years of annual environmental ozone concentrations, relative humidity, and temperature, and reported influenza case numbers in two cities in Japan, Sendai and Naha, which exhibit typical temperate and subtropical climate patterns, respectively; based on the findings of our previous study and actual ambient environmental data, we estimated the influenza airborne\u2010transmission risk in these cities and compared it with observed epidemics. In both cities, the persistence of winter epidemics was strongly associated with low ozone concentration (&lt;\u200935 ppb), and their subsiding in spring was associated with increases in ozone (\u2267\u200935 ppb) and relative humidity (\u2267\u200950%), even at lower temperature (&lt;\u200920\u00b0C). The summer outbreak in Naha was not suppressed solely under high temperatures (25\u00b0C\u201330\u00b0C) and relative humidity (\u2267\u200970%), but was associated with a subsequent increase in ozone (\u2267\u200935 ppb). A similar phenomenon was recognized during the 2009 influenza pandemic. These results were consistent with our hypothesis: influenza epidemic patterns corresponded with the influenza transmission risk estimated from the synergistic inactivation patterns of airborne viruses by ambient ozone, relative humidity, and temperature.<\/jats:p>","DOI":"10.1111\/1348-0421.70089","type":"journal-article","created":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T09:33:29Z","timestamp":1789551209000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Synergistic Effect of Ambient Ozone, Relative Humidity, and Temperature on Epidemic Patterns of Influenza: A Hypothesis and Its Verification"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5681-7971","authenticated-orcid":false,"given":"Hidekazu","family":"Nishimura","sequence":"first","affiliation":[{"name":"Virus Research Center, Clinical Research Division, Sendai Medical Center National Hospital Organization Sendai Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Soichiro","family":"Sakata","sequence":"additional","affiliation":[{"name":"Mediair Japan Inc. Yokohama Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4963-1028","authenticated-orcid":false,"given":"Julian W.","family":"Tang","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology University Hospitals of Leicester NHS Trust Leicester UK"},{"name":"Respiratory Sciences University of Leicester Leicester UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Suguru","family":"Ohmiya","sequence":"additional","affiliation":[{"name":"Virus Research Center, Clinical Research Division, Sendai Medical Center National Hospital Organization Sendai Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masanori","family":"Katsumi","sequence":"additional","affiliation":[{"name":"Virus Research Center, Clinical Research Division, Sendai Medical Center National Hospital Organization Sendai Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takahiro","family":"Yokoyama","sequence":"additional","affiliation":[{"name":"Niterra Co. Ltd. Aichi Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,16]]},"reference":[{"key":"e_1_2_11_2_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0103560"},{"key":"e_1_2_11_3_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1716561115"},{"key":"e_1_2_11_4_1","unstructured":"WHO \u201cGlobal Technical Consultation Report on Proposed Terminology for Pathogens That Transmit Through the Air \u201d2024.https:\/\/www.who.int\/publications\/m\/item\/global-technical-consultation-report-on-proposed-terminology-for-pathogens-that-transmit-through-the-air."},{"issue":"6","key":"e_1_2_11_5_1","first-page":"S783","article-title":"Aerosol Transmission of Influenza A Virus: A Review of New Studies","volume":"6","author":"Tellier R.","year":"2009","journal-title":"Journal of the Royal Society Interface S6"},{"key":"e_1_2_11_6_1","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-024-70615-z","article-title":"Minimal Influenza Virus Transmission From Touching Contaminated Face Masks: A Laboratory Study","volume":"14","author":"Fan Y.","year":"2024","journal-title":"Scientific Reports"},{"key":"e_1_2_11_7_1","doi-asserted-by":"publisher","DOI":"10.1111\/1348-0421.13226"},{"key":"e_1_2_11_8_1","doi-asserted-by":"publisher","DOI":"10.1289\/ehp.1002383"},{"key":"e_1_2_11_9_1","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.01680-06"},{"key":"e_1_2_11_10_1","doi-asserted-by":"publisher","DOI":"10.1111\/1348-0421.13204"},{"key":"e_1_2_11_11_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12889-016-3503-1"},{"key":"e_1_2_11_12_1","doi-asserted-by":"publisher","DOI":"10.3390\/v11030207"},{"key":"e_1_2_11_13_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0167712"},{"key":"e_1_2_11_14_1","doi-asserted-by":"publisher","DOI":"10.1111\/irv.12682"},{"key":"e_1_2_11_15_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.02426-18"},{"key":"e_1_2_11_16_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12889-025-24182-1"},{"key":"e_1_2_11_17_1","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jis467"},{"key":"e_1_2_11_18_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0030151"},{"key":"e_1_2_11_19_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0022172400039176"},{"key":"e_1_2_11_20_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01317930"},{"key":"e_1_2_11_21_1","doi-asserted-by":"publisher","DOI":"10.1183\/13993003.00369-2018"},{"key":"e_1_2_11_22_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11356-022-22814-2"},{"key":"e_1_2_11_23_1","doi-asserted-by":"publisher","DOI":"10.1289\/EHP12145"},{"key":"e_1_2_11_24_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-025-95085-9"},{"key":"e_1_2_11_25_1","doi-asserted-by":"crossref","first-page":"3338","DOI":"10.1186\/s12889-025-24755-0","article-title":"Association Between Short\u2010Term Exposure to Ambient Ozone Concentration and Influenza Incidence in Kawasaki City, Japan: A Time\u2010Stratified Case\u2010Crossover Analysis","volume":"25","author":"Wagatsuma K.","year":"2025","journal-title":"BMC Public Health"},{"key":"e_1_2_11_26_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-024-48199-z"},{"key":"e_1_2_11_27_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12879-023-08769-w"},{"key":"e_1_2_11_28_1","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s10874-005-1172-z","article-title":"Seasonal and Diurnal Ozone Variations","volume":"50","author":"Schneider N.","year":"2005","journal-title":"Journal of Atmospheric Chemistry"},{"key":"e_1_2_11_29_1","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.4209\/aaqr.2012.03.0055","article-title":"Analysis of Diurnal and Seasonal Behavior of Surface Ozone and Its Precursors (NOx) at a Semi\u2010Arid Rural Site in Southern India","volume":"12","author":"Reddy B. S. K.","year":"2012","journal-title":"Aerosol and Air Quality Research"},{"key":"e_1_2_11_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.eti.2022.102809"},{"key":"e_1_2_11_31_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1750-2659.2007.00024.x"},{"key":"e_1_2_11_32_1","article-title":"The Ministry of the Environment and Government of Japan","author":"Soramame\u2010kun","year":"2019","journal-title":"Atmospheric Environmental Regional Observation System (AEROS)"},{"key":"e_1_2_11_33_1","first-page":"297","article-title":"\u00dcber Einige Meteorologische Begriffe","volume":"6","author":"Tetens O.","year":"1930","journal-title":"Zeitschrift Fuer Geophysik"},{"key":"e_1_2_11_34_1","first-page":"11","volume-title":"Water Vapor and its Specification,\u201d Principles of Environmental Physics: Plants, Animals, and the Atmosphere","author":"Monteith J. L.","year":"2013"},{"key":"e_1_2_11_35_1","article-title":"Sentinel\u2010Reporting Diseases (Weekly), Number of Cases Per Sentinel by Week, Prefecture, and Sex","author":"NIID, JIHS","journal-title":"Infectious Diseases Surveillance, Annual Reports"},{"key":"e_1_2_11_36_1","unstructured":"The National Institute for Environmental Studies Japan. \u201cThe Environment Observatory Air Pollution Monitoring Data File; Data From the Tsutsujigaoka Monitoring Station in Sendai City Miyagi Prefecture Japan\u201dhttps:\/\/tenbou.nies.go.jp\/download\/."},{"key":"e_1_2_11_37_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0054445"},{"key":"e_1_2_11_38_1","doi-asserted-by":"publisher","DOI":"10.1111\/ina.12052"},{"key":"e_1_2_11_39_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00484-015-1019-5"},{"issue":"1","key":"e_1_2_11_40_1","first-page":"118","article-title":"Indoor Pollutant Gas Concentration and the Effect on Image Stability","volume":"67","author":"Kanazawa Y.","year":"2004","journal-title":"Journal of The Society of Photographic Science and Technology of Japan"}],"container-title":["Microbiology and Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/1348-0421.70089","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/1348-0421.70089","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/1348-0421.70089","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,16]],"date-time":"2026-09-16T09:33:34Z","timestamp":1789551214000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/1348-0421.70089"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,16]]},"references-count":39,"alternative-id":["10.1111\/1348-0421.70089"],"URL":"https:\/\/doi.org\/10.1111\/1348-0421.70089","archive":["Portico"],"relation":{},"ISSN":["0385-5600","1348-0421"],"issn-type":[{"value":"0385-5600","type":"print"},{"value":"1348-0421","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,16]]},"assertion":[{"value":"2026-03-05","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-08-25","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-16","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"1348-0421.70089"}}