{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T13:49:59Z","timestamp":1787320199514,"version":"build-2736575974"},"reference-count":47,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,12,16]],"date-time":"2025-12-16T00:00:00Z","timestamp":1765843200000},"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. Public Health"],"abstract":"<jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Hemorrhagic Fever with Renal Syndrome (HFRS) is a naturally occurring zoonotic disease significantly influenced by meteorological factors, with rodents serving as the primary reservoir. It imposes a substantial global disease burden. This study aims to investigate the non-linear and interactive effects of meteorological factors on HFRS, as well as the exposure-lag-response patterns on the Jiaodong Peninsula in China.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Method<\/jats:title>\n                    <jats:p>Daily meteorological data for the Jiaodong Peninsula from 2020 to 2024 were collected from the China Meteorological Data Sharing Service System. Daily incidence data for HFRS cases were collected from the China Disease Prevention and Control Information System. A generalized additive model with quasi-Poisson regression was conducted to examine the non-linear relationships and interactive effects between meteorological factors and HFRS. A distributed lag non-linear model was constructed to investigate the exposure-lag effects of meteorological factors on HFRS. Model analysis was conducted using R 4.5.1 software, and visualization was performed using ArcGIS 10.7 software.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Result<\/jats:title>\n                    <jats:p>From 2020 to 2024, a cumulative total of 1,121 cases of HFRS were reported in China\u2019s Jiaodong Peninsula. Among these, Qingdao reported 594 cases, Yantai reported 438 cases, and Weihai reported 89 cases. HFRS exhibits a distinct seasonal pattern, with the peak incidence occurring annually from October to December. Spearman correlation analysis and random forest regression analysis were employed to screen the original meteorological factors. Ultimately, weekly average air pressure was excluded, while weekly average temperature, weekly average wind speed, weekly average humidity, and weekly average precipitation were incorporated into subsequent modeling. The results indicate that all four meteorological factors influence the occurrence of HFRS, exhibiting a pronounced non-linear relationship. Interaction analysis indicates that within an appropriate temperature range, increases in precipitation, relative humidity, and wind speed within certain thresholds can synergistically heighten the risk of HFRS incidence. Using the median meteorological factor as the baseline, the risk of HFRS significantly increased after a 13-week lag (RR\u202f=\u202f1.185, 95% CI: 1.016\u20131.381) during periods of extremely high temperature (the 95th percentile of WAT, 27\u202f\u00b0C). Under extremely low temperature (the 5th percentile of WAT, \u22121\u202f\u00b0C), the risk of HFRS significantly increased after a 15-week lag period (RR\u202f=\u202f1.189, 95% CI: 1.014\u20131.394). Under extremely high humidity (the 95th percentile of WAH, 88%), the risk of HFRS significantly increased after a 14-week lag period (RR\u202f=\u202f1.262, 95% CI: 1.023\u20131.557). However, no statistically significant effect was observed at extremely low humidity (the 5th percentile of WAH, 50%).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>The prevalence of HFRS on China\u2019s Jiaodong Peninsula exhibits a significant non-linear association with meteorological factors, accompanied by pronounced interaction effects and complex exposure lag effects. The findings of this study provide quantitative evidence for regional precision-based early warning and tiered prevention and control measures. Public health authorities should formulate disease prevention and control strategies based on these results to reduce the burden of HFRS.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fpubh.2025.1743845","type":"journal-article","created":{"date-parts":[[2025,12,16]],"date-time":"2025-12-16T06:27:25Z","timestamp":1765866445000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["Meteorological drivers of hemorrhagic fever with renal syndrome in China\u2019s Jiaodong Peninsula: an ecological time-series study from 2020 to 2024"],"prefix":"10.3389","volume":"13","author":[{"given":"Xiaofang","family":"Guo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruixiao","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xueying","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanxin","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lianlong","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ti","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qing","family":"Duan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renpeng","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zengqiang","family":"Kou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,12,16]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"200","DOI":"10.16250\/j.32.1374.2021163","article-title":"Epidemic process and influencing factors of hemorrhagic fever with renal syndrome: a review","volume":"34","author":"Wang","year":"2021","journal-title":"Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"e0009673","DOI":"10.1371\/journal.pntd.0009673","article-title":"The changing epidemiology of hemorrhagic fever with renal syndrome in southeastern China during 1963-2020: a retrospective analysis of surveillance data","volume":"15","author":"Zhang","year":"2021","journal-title":"PLoS Negl Trop Dis"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"e6","DOI":"10.1111\/1469-0691.12291","article-title":"Hantavirus infections","volume":"21","author":"Av\u0161i\u010d-\u017dupanc","year":"2019","journal-title":"Clin Microbiol Infect"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"2553784","DOI":"10.1080\/21505594.2025.2553784","article-title":"Pathogenicity and virulence of rodent-borne Orthohantaviruses","volume":"16","author":"Taylor","year":"2025","journal-title":"Virulence"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1186\/s12879-022-07301-w","article-title":"Comparison of 19 major infectious diseases during COVID-19 epidemic and previous years in Zhejiang, implications for prevention measures","volume":"22","author":"Li","year":"2022","journal-title":"BMC Infect Dis"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fcimb.2016.00001","article-title":"Hemorrhagic fever with renal syndrome: pathogenesis and clinical picture","volume":"6","author":"Jiang","year":"2016","journal-title":"Front Cell Infect Microbiol"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3947\/ic.2021.0148","article-title":"Hemorrhagic fever with renal syndrome: literature review, epidemiology, clinical picture and pathogenesis","volume":"54","author":"Tariq","year":"2022","journal-title":"Infect Chemother"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"S864","DOI":"10.1093\/clinids\/11.Supplement_4.S864","article-title":"Hemorrhagic fever with renal syndrome in Korea","volume":"11","author":"Lee","year":"1989","journal-title":"Rev Infect Dis"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"e371","DOI":"10.1016\/s1473-3099(23)00128-7","article-title":"Hantavirus in humans: a review of clinical aspects and management","volume":"23","author":"Vial","year":"2023","journal-title":"Lancet Infect Dis"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"10.3390\/v15020561","DOI":"10.3390\/v15020561","article-title":"Hemorrhagic fever with renal syndrome in Asia: history, pathogenesis, diagnosis, treatment, and prevention","volume":"15","author":"Sehgal","year":"2023","journal-title":"Viruses"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"2771","DOI":"10.3389\/fmicb.2018.02771","article-title":"Genetic diversity and the spatio-temporal analyses of hantaviruses in Shandong Province, China","volume":"9","author":"Zuo","year":"2018","journal-title":"Front Microbiol"},{"key":"ref12","first-page":"472","article-title":"Epidemiological progresses of hemorrhagic fever with renal syndrome in China","volume":"112","author":"Song","year":"1999","journal-title":"Chin Med J"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"410","DOI":"10.1007\/s40506-020-00236-3","article-title":"Hantavirus infections-treatment and prevention","volume":"12","author":"Dheerasekara","year":"2020","journal-title":"Curr Treat Options Infect Dis"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.5365\/wpsar.2011.2.2.007","article-title":"Epidemiologic characteristics of haemorrhagic fever with renal syndrome in mainland China from 2006 to 2010","volume":"3","author":"Huang","year":"2012","journal-title":"Western Pac Surveill Response J"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"3723","DOI":"10.1111\/gcb.16708","article-title":"Tracing the future of epidemics: coincident niche distribution of host animals and disease incidence revealed climate-correlated risk shifts of main zoonotic diseases in China","volume":"29","author":"Cao","year":"2023","journal-title":"Glob Chang Biol"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1186\/s40249-024-01272-7","article-title":"Risk of hemorrhagic fever with renal syndrome associated with meteorological factors in diverse epidemic regions: a nationwide longitudinal study in China","volume":"14","author":"Chang","year":"2025","journal-title":"Infect Dis Poverty"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"e789","DOI":"10.1371\/journal.pntd.0000789","article-title":"Spatiotemporal trends and climatic factors of hemorrhagic fever with renal syndrome epidemic in Shandong Province, China","volume":"4","author":"Fang","year":"2010","journal-title":"PLoS Negl Trop Dis"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"e52221","DOI":"10.2196\/52221","article-title":"Epidemic characteristics and meteorological risk factors of Hemorrhagic fever with renal syndrome in 151 cities in China from 2015 to 2021: retrospective analysis","volume":"10","author":"Luo","year":"2024","journal-title":"JMIR Public Health Surveill"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"100895","DOI":"10.1016\/j.onehlt.2024.100895","article-title":"Asymmetric association between meteorological factors and human infections with hemorrhagic fever with renal syndrome: a 16-year ecological trend study in Shaanxi, China","volume":"19","author":"Xue","year":"2024","journal-title":"One Health"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"3781","DOI":"10.1002\/sim.2073","article-title":"Using generalized additive models to reduce residual confounding","volume":"23","author":"Benedetti","year":"2004","journal-title":"Stat Med"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1484","DOI":"10.1186\/s12889-022-13890-7","article-title":"Long-term air pollution levels modify the relationships between short-term exposure to meteorological factors, air pollution and the incidence of hand, foot and mouth disease in children: a DLNM-based multicity time series study in Sichuan Province, China","volume":"22","author":"Luo","year":"2022","journal-title":"BMC Public Health"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"2224","DOI":"10.1002\/sim.3940","article-title":"Distributed lag non-linear models","volume":"29","author":"Gasparrini","year":"2010","journal-title":"Stat Med"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"180214","DOI":"10.1038\/sdata.2018.214","article-title":"Present and future K\u00f6ppen-Geiger climate classification maps at 1-km resolution","volume":"5","author":"Beck","year":"2018","journal-title":"Sci Data"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1007\/s40484-017-0121-6","article-title":"Variable importance-weighted random forests","volume":"5","author":"Liu","year":"2017","journal-title":"Quant Biol"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"e0009776","DOI":"10.1371\/journal.pntd.0009776","article-title":"The association between tropical cyclones and dengue fever in the Pearl River Delta, China during 2013-2018: a time-stratified case-crossover study","volume":"15","author":"Li","year":"2021","journal-title":"PLoS Negl Trop Dis"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"418","DOI":"10.3760\/cma.j.cn112338-20240813-00499","article-title":"Study of prediction of hemorrhagic fever with renal syndrome incidence in Hebei Province based on generalized additive model","volume":"46","author":"Yue","year":"2025","journal-title":"Zhonghua Liu Xing Bing Xue Za Zhi"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"e0147054","DOI":"10.1371\/journal.pone.0147054","article-title":"Short-term effects of climatic variables on hand, foot, and mouth disease in mainland China, 2008-2013: a multilevel spatial Poisson regression model accounting for overdispersion","volume":"11","author":"Liao","year":"2016","journal-title":"PLoS One"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1199","DOI":"10.1093\/ije\/dyaa286","article-title":"A systematic review on lagged associations in climate-health studies","volume":"50","author":"Wang","year":"2021","journal-title":"Int J Epidemiol"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.4269\/ajtmh.12-0473","article-title":"Association between hemorrhagic fever with renal syndrome epidemic and climate factors in Heilongjiang Province, China","volume":"89","author":"Li","year":"2013","journal-title":"Am J Trop Med Hyg"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v043.i08","article-title":"Distributed lag linear and non-linear models in R: the package dlnm","volume":"43","author":"Gasparrini","year":"2011","journal-title":"J Stat Softw"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"e0009217","DOI":"10.1371\/journal.pntd.0009217","article-title":"Effects and interaction of meteorological factors on hemorrhagic fever with renal syndrome incidence in Huludao City, northeastern China, 2007-2018","volume":"15","author":"Sun","year":"2021","journal-title":"PLoS Negl Trop Dis"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"e0010806","DOI":"10.1371\/journal.pntd.0010806","article-title":"Time series analyses based on the joint lagged effect analysis of pollution and meteorological factors of hemorrhagic fever with renal syndrome and the construction of prediction model","volume":"17","author":"Chen","year":"2023","journal-title":"PLoS Negl Trop Dis"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"e0012151","DOI":"10.1371\/journal.pntd.0012151","article-title":"Using empirical dynamic modeling to identify the impact of meteorological factors on hemorrhagic fever with renal syndrome in Weifang, northeastern China, from 2011 to 2020","volume":"18","author":"Zheng","year":"2024","journal-title":"PLoS Negl Trop Dis"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"137564","DOI":"10.1016\/j.scitotenv.2020.137564","article-title":"Interactions and marginal effects of meteorological factors on haemorrhagic fever with renal syndrome in different climate zones: evidence from 254 cities of China","volume":"721","author":"Cao","year":"2020","journal-title":"Sci Total Environ"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"20037","DOI":"10.1038\/s41598-022-23945-9","article-title":"Meteorological change and hemorrhagic fever with renal syndrome epidemic in China, 2004-2018","volume":"12","author":"Luo","year":"2022","journal-title":"Sci Rep"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"e0007688","DOI":"10.1371\/journal.pntd.0007688","article-title":"Distribution of geographical scale, data aggregation unit and period in the correlation analysis between temperature and incidence of HFRS in mainland China: a systematic review of 27 ecological studies","volume":"13","author":"Bai","year":"2019","journal-title":"PLoS Negl Trop Dis"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"305","DOI":"10.24272\/j.issn.2095-8137.2019.045","article-title":"Effect of temperature on antioxidant defense and innate immunity in Brandt's voles","volume":"40","author":"Xu","year":"2019","journal-title":"Zool Res"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"e0008786","DOI":"10.1371\/journal.pntd.0008786","article-title":"Hantavirus pulmonary syndrome outbreaks associated with climate variability in northwestern Argentina, 1997-2017","volume":"14","author":"Ferro","year":"2020","journal-title":"PLoS Negl Trop Dis"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"e0006901","DOI":"10.1371\/journal.pntd.0006901","article-title":"The ecological dynamics of hantavirus diseases: from environmental variability to disease prevention largely based on data from China","volume":"13","author":"Tian","year":"2019","journal-title":"PLoS Negl Trop Dis"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"e3344","DOI":"10.1371\/journal.pntd.0003344","article-title":"Spatiotemporal transmission dynamics of hemorrhagic fever with renal syndrome in China, 2005-2012","volume":"8","author":"Zhang","year":"2014","journal-title":"PLoS Negl Trop Dis"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1021\/acs.estlett.2c00243","article-title":"Humidity reduces rapid and distant airborne dispersal of viable viral particles in classroom settings","volume":"9","author":"Skanata","year":"2022","journal-title":"Environ Sci Technol Lett"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"e2429682","DOI":"10.1001\/jamanetworkopen.2024.29682","article-title":"The 2016 severe floods and incidence of Hemorrhagic fever with renal syndrome in the Yangtze River basin","volume":"7","author":"Ji","year":"2024","journal-title":"JAMA Netw Open"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"2547","DOI":"10.1128\/aem.02869-06","article-title":"Ex vivo stability of the rodent-borne Hantaan virus in comparison to that of arthropod-borne members of the Bunyaviridae family","volume":"73","author":"Hardestam","year":"2007","journal-title":"Appl Environ Microbiol"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"1012","DOI":"10.3967\/bes2022.130","article-title":"Spatial heterogeneity and influencing factors of HFRS epidemics in rural and urban areas: a study in Guanzhong plain of Shaanxi Province, China","volume":"35","author":"Zhu","year":"2022","journal-title":"Biomed Environ Sci"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2023\/5572334","article-title":"Assessing the relationship between climate variables and Hemorrhagic fever with renal syndrome transmission in eastern China: a multi-cities time series study","volume":"2023","author":"Wang","year":"2023","journal-title":"Transbound Emerg Dis"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"458","DOI":"10.4103\/ijph.ijph_926_22","article-title":"The impact of COVID-19 pandemic on influenza surveillance: a systematic review and meta-analysis","volume":"66","author":"Sabeena","year":"2022","journal-title":"Indian J Public Health"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1186\/s12967-024-04855-y","article-title":"Evaluating the long-term impact of COVID-19-associated public health interventions on zoonotic and vector-borne diseases in China: an interrupted time series analysis","volume":"22","author":"Wang","year":"2024","journal-title":"J Transl Med"}],"container-title":["Frontiers in Public Health"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpubh.2025.1743845\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,16]],"date-time":"2025-12-16T06:27:35Z","timestamp":1765866455000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpubh.2025.1743845\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,12,16]]},"references-count":47,"alternative-id":["10.3389\/fpubh.2025.1743845"],"URL":"https:\/\/doi.org\/10.3389\/fpubh.2025.1743845","relation":{},"ISSN":["2296-2565"],"issn-type":[{"value":"2296-2565","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,12,16]]},"article-number":"1743845"}}