{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T11:38:14Z","timestamp":1789040294530,"version":"build-2803163510"},"reference-count":45,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2021,3,25]],"date-time":"2021-03-25T00:00:00Z","timestamp":1616630400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Key Research and Development Program of China","award":["2017FY101202"],"award-info":[{"award-number":["2017FY101202"]}]}],"content-domain":{"domain":["www.plosntds.org"],"crossmark-restriction":false},"short-container-title":["PLoS Negl Trop Dis"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Background<\/jats:title>\n<jats:p>Hemorrhagic fever with renal syndrome (HFRS), a rodent-borne disease, is a severe public health threat. Previous studies have discovered the influence of meteorological factors on HFRS incidence, while few studies have concentrated on the stratified analysis of delayed effects and interaction effects of meteorological factors on HFRS.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Objective<\/jats:title>\n<jats:p>Huludao City is a representative area in north China that suffers from HFRS with primary transmission by <jats:italic>Rattus norvegicus<\/jats:italic>. This study aimed to evaluate the climate factors of lag, interaction, and stratified effects of meteorological factors on HFRS incidence in Huludao City.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Methods<\/jats:title>\n<jats:p>Our researchers collected meteorological data and epidemiological data of HFRS cases in Huludao City during 2007\u20132018. First, a distributed lag nonlinear model (DLNM) for a maximum lag of 16 weeks was developed to assess the respective lag effect of temperature, precipitation, and humidity on HFRS incidence. We then constructed a generalized additive model (GAM) to explore the interaction effect between temperature and the other two meteorological factors on HFRS incidence and the stratified effect of meteorological factors.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Results<\/jats:title>\n<jats:p>During the study period, 2751 cases of HFRS were reported in Huludao City. The incidence of HFRS showed a seasonal trend and peak times from February to May. Using the median WAT, median WTP, and median WARH as the reference, the results of DLNM showed that extremely high temperature (97.5<jats:sup>th<\/jats:sup> percentile of WAT) had significant associations with HFRS at lag week 15 (RR = 1.68, 95% CI: 1.04\u20132.74) and lag week 16 (RR = 2.80, 95% CI: 1.31\u20135.95). Under the extremely low temperature (2.5<jats:sup>th<\/jats:sup> percentile of WAT), the RRs of HFRS infection were significant at lag week 5 (RR = 1.28, 95% CI: 1.01\u20131.67) and lag 6 weeks (RR = 1.24, 95% CI: 1.01\u20131.57). The RRs of relative humidity were statistically significant at lag week 10 (RR = 1.19, 95% CI: 1.00\u20131.43) and lag week 11 (RR = 1.24, 95% CI: 1.02\u20131.50) under extremely high relative humidity (97.5<jats:sup>th<\/jats:sup> percentile of WARH); however, no statistically significance was observed under extremely low relative humidity (2.5<jats:sup>th<\/jats:sup> percentile of WARH). The RRs were significantly high when WAT was -10 degrees Celsius (RR = 1.34, 95% CI: 1.02\u20131.76), -9 degrees Celsius (1.37, 95% CI: 1.04\u20131.79), and -8 degrees Celsius (RR = 1.34, 95% CI: 1.03\u20131.75) at lag week 5 and more than 23 degrees Celsius after 15 weeks. Interaction and stratified analyses showed that the risk of HFRS infection reached its highest when both temperature and precipitation were at a high level.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec005\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>Our study indicates that meteorological factors, including temperature and humidity, have delayed effects on the occurrence of HFRS in the study area, and the effect of temperature can be modified by humidity and precipitation. Public health professionals should pay more attention to HFRS control when the weather conditions of high temperature with more substantial precipitation and 15 weeks after the temperature is higher than 23 degrees Celsius.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pntd.0009217","type":"journal-article","created":{"date-parts":[[2021,3,25]],"date-time":"2021-03-25T14:46:33Z","timestamp":1616683593000},"page":"e0009217","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":28,"title":["Effects and interaction of meteorological factors on hemorrhagic fever with renal syndrome incidence in Huludao City, northeastern China, 2007\u20132018"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2268-7715","authenticated-orcid":true,"given":"Wanwan","family":"Sun","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaobo","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8128-9904","authenticated-orcid":true,"given":"Wen","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiyuan","family":"Mao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jimin","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liang","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,3,25]]},"reference":[{"issue":"8","key":"pntd.0009217.ref001","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.3201\/eid1608.090470","article-title":"Hantavirus Infections in Humans and Animals, China","volume":"16","author":"YZ Zhang","year":"2010","journal-title":"Emerging Infectious Diseases"},{"issue":"6","key":"pntd.0009217.ref002","first-page":"466","article-title":"The epidemic characteristic and preventive measures of hemorrhagic fever with renal syndromes in China. 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Hantaviruses, a global disease problem","volume":"3","author":"BH Schmaljohn","year":"1997","journal-title":"Emerg Infect Dis"},{"issue":"6","key":"pntd.0009217.ref004","first-page":"451","article-title":"Study on the Factors Influenced Epidemic of Hemorrhagic Fever with Renal Syndrome","volume":"14","author":"CW Luo","year":"2003","journal-title":"Chinese Journal of Vector Biology & Control"},{"issue":"2","key":"pntd.0009217.ref005","doi-asserted-by":"crossref","first-page":"420","DOI":"10.4269\/ajtmh.15-0486","article-title":"Effects of Humidity Variation on the Hantavirus Infection and Hemorrhagic Fever with Renal Syndrome Occurrence in Subtropical China","volume":"94","author":"H Xiao","year":"2016","journal-title":"Am J Trop Med Hyg"},{"issue":"8","key":"pntd.0009217.ref006","doi-asserted-by":"crossref","first-page":"632","DOI":"10.3109\/00365548.2011.566279","article-title":"Comparison of Hantaan and Seoul viral infections among patients with hemorrhagic fever with renal syndrome (HFRS) in Heilongjiang, China","volume":"43","author":"X Zhang","year":"2011","journal-title":"Scand J Infect Dis"},{"issue":"1","key":"pntd.0009217.ref007","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1093\/ije\/31.1.189","article-title":"Climatic, reservoir and occupational variables and the transmission of haemorrhagic fever with renal syndrome in China","volume":"31","author":"P Bi","year":"2002","journal-title":"Int J Epidemiol"},{"issue":"1","key":"pntd.0009217.ref008","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pntd.0002615","article-title":"Animal reservoir, natural and socioeconomic variations and the transmission of hemorrhagic fever with renal syndrome in Chenzhou, China, 2006\u20132010","volume":"8","author":"H Xiao","year":"2014","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009217.ref009","doi-asserted-by":"crossref","first-page":"36081","DOI":"10.1038\/srep36081","article-title":"Prevalence of hemorrhagic fever with renal syndrome in Qingdao City, China, 2010\u20132014","volume":"6","author":"F Jiang","year":"2016","journal-title":"Sci Rep."},{"issue":"1","key":"pntd.0009217.ref010","doi-asserted-by":"crossref","first-page":"87","DOI":"10.3201\/eid0501.990110","article-title":"Climatic and environmental patterns associated with hantavirus pulmonary syndrome, Four Corners region, United States","volume":"5","author":"DM Engelthaler","year":"1999","journal-title":"Emerg Infect Dis"},{"issue":"331","key":"pntd.0009217.ref011","first-page":"1","article-title":"Temporal trend and climate factors of hemorrhagic fever with renal syndrome epidemic in Shenyang City, China","volume":"11","author":"X Liu","year":"2011","journal-title":"BMC Infect Dis"},{"issue":"10","key":"pntd.0009217.ref012","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.1016\/j.scitotenv.2011.02.005","article-title":"Does temperature enhance acute mortality effects of ambient particle pollution in Tianjin City, China","volume":"409","author":"G Li","year":"2011","journal-title":"Sci Total Environ"},{"issue":"6","key":"pntd.0009217.ref013","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1007\/s00484-013-0688-1","article-title":"Meteorological factors are associated with hemorrhagic fever with renal syndrome in Jiaonan County, China, 2006\u20132011","volume":"58","author":"H Lin","year":"2014","journal-title":"Int J Biometeorol"},{"issue":"4","key":"pntd.0009217.ref014","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1017\/S0950268812001434","article-title":"Association of hemorrhagic fever with renal syndrome and weather factors in Junan County, China: a case-crossover study","volume":"141","author":"J Liu","year":"2013","journal-title":"Epidemiol Infect"},{"key":"pntd.0009217.ref015","unstructured":"Zhang C, Fu X, Zhang Y, et al. Epidemiological and time series analysis of haemorrhagic fever with renal syndrome from 2004 to 2017 in Shandong Province, China[J]. entific Reports."},{"issue":"6","key":"pntd.0009217.ref016","doi-asserted-by":"crossref","first-page":"e0006604","DOI":"10.1371\/journal.pntd.0006604","article-title":"Meteorological factors and risk of hemorrhagic fever with renal syndrome in Guangzhou, southern China, 2006\u20132015[J].","volume":"12","author":"W Yuehong","year":"2018","journal-title":"Plos Neglected Tropical Diseases"},{"key":"pntd.0009217.ref017","article-title":"Spatial heterogeneity of hemorrhagic fever with renal syndrome is driven by environmental factors and rodent community composition.[J]","author":"Xiao Hong","year":"2018","journal-title":"Plos Neglected Tropical Diseases"},{"issue":"8","key":"pntd.0009217.ref018","doi-asserted-by":"crossref","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":"A. Gasparrini","year":"2011","journal-title":"Journal of Statistical Software"},{"key":"pntd.0009217.ref019","unstructured":"Simon Wood. mgcv: Mixed GAM Computation Vehicle with Automatic Smoothness Estimation[J]. 2018."},{"issue":"13","key":"pntd.0009217.ref020","doi-asserted-by":"crossref","first-page":"1671","DOI":"10.1017\/S095026881800184X","article-title":"Using a distributed lag non-linear model to identify impact of temperature variables on hemorrhagic fever with renal syndrome in Shandong Province","volume":"146","author":"Q Xu","year":"2018","journal-title":"Epidemiol Infect"},{"key":"pntd.0009217.ref021","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1186\/1471-2334-9-109","article-title":"Investigating the effects of climatic variables and reservoir on the incidence of hemorrhagic fever with renal syndrome in Huludao City, China: a 17-year data analysis based on structure equation model","volume":"9","author":"P Guan","year":"2009","journal-title":"BMC Infect Dis"},{"issue":"18","key":"pntd.0009217.ref022","first-page":"1660","article-title":"The Impacts of Climatic Factors and Vegetation on Hemorrhagic Fever with Renal Syndrome Transmission in China: A Study of 109 Counties[J]","volume":"16","author":"Junyu He","year":"2019","journal-title":"Int J Environ Res Public Health"},{"issue":"11","key":"pntd.0009217.ref023","first-page":"e104","article-title":"Meteorological factors affect the epidemiology of hemorrhagic fever with renal syndrome via altering the breeding and hantavirus-carrying states of rodents and mites: a 9 years\u2019 longitudinal study [J]","volume":"6","author":"F Jiang","year":"2017","journal-title":"Emerging Microbes & Infections"},{"issue":"8","key":"pntd.0009217.ref024","doi-asserted-by":"crossref","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.[J]","volume":"73","author":"J Hardestam","year":"2007","journal-title":"Applied & Environmental Microbiology"},{"issue":"8","key":"pntd.0009217.ref025","doi-asserted-by":"crossref","first-page":"2127","DOI":"10.1099\/vir.0.81643-0","article-title":"Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment[J]","volume":"87","author":"E. R. Kallio","year":"2006","journal-title":"Journal of General Virology"},{"key":"pntd.0009217.ref026","first-page":"360","volume-title":"Generalized Additive Models: An Introduction With R","author":"N. Simon","year":"2006"},{"issue":"3","key":"pntd.0009217.ref027","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1093\/aje\/kwf062","article-title":"On the use of generalized additive models in time-series studies of air pollution and health[J]","volume":"156","author":"F Dominici","year":"2002","journal-title":"American Journal of Epidemiology"},{"issue":"7","key":"pntd.0009217.ref028","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1289\/ehp.0901504","article-title":"Climate variability and hemorrhagic fever with renal syndrome transmission in Northeastern China","volume":"118","author":"WY Zhang","year":"2010","journal-title":"Environ Health Perspect"},{"issue":"9","key":"pntd.0009217.ref029","doi-asserted-by":"crossref","first-page":"e14640","DOI":"10.1097\/MD.0000000000014640","article-title":"Effects of climate factors on hemorrhagic fever with renal syndrome in Changchun, 2013 to 2017","volume":"98","author":"Q Zhao","year":"2019","journal-title":"Medicine (Baltimore)"},{"issue":"1","key":"pntd.0009217.ref030","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1186\/s12879-017-2506-6","article-title":"The influence of climatic factors on the development of hemorrhagic fever with renal syndrome and leptospirosis during the peak season in Korea: an ecologic study","volume":"17","author":"YP Joshi","year":"2017","journal-title":"BMC Infect Dis"},{"issue":"5","key":"pntd.0009217.ref031","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.4269\/ajtmh.18-0544","article-title":"Environmental Determinants of Hemorrhagic Fever with Renal Syndrome in High-Risk Counties in China: A Time Series Analysis (2002\u20132012)","volume":"99","author":"J He","year":"2018","journal-title":"Am J Trop Med Hyg"},{"issue":"13","key":"pntd.0009217.ref032","doi-asserted-by":"crossref","first-page":"1671","DOI":"10.1017\/S095026881800184X","article-title":"Using a distributed lag non-linear model to identify impact of temperature variables on hemorrhagic fever with renal syndrome in Shandong Province","volume":"146","author":"Q Xu","year":"2018","journal-title":"Epidemiol Infect"},{"issue":"6","key":"pntd.0009217.ref033","doi-asserted-by":"crossref","first-page":"e0006604","DOI":"10.1371\/journal.pntd.0006604","article-title":"Meteorological factors and risk of hemorrhagic fever with renal syndrome in Guangzhou, southern China, 2006\u20132015","volume":"12","author":"Y Wei","year":"2018","journal-title":"PLoS Negl Trop Dis"},{"issue":"1","key":"pntd.0009217.ref034","doi-asserted-by":"crossref","first-page":"14644","DOI":"10.1038\/s41598-019-50878-7","article-title":"Epidemiological and time series analysis of hemorrhagic fever with renal syndrome from 2004 to 2017 in Shandong Province, China","volume":"9","author":"C Zhang","year":"2019","journal-title":"Sci Rep."},{"key":"pntd.0009217.ref035","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1016\/j.scitotenv.2018.04.407","article-title":"Impact of meteorological factors on hemorrhagic fever with renal syndrome in 19 cities in China, 2005\u20132014","volume":"636","author":"J Xiang","year":"2018","journal-title":"Sci Total Environ"},{"issue":"30","key":"pntd.0009217.ref036","doi-asserted-by":"crossref","first-page":"8041","DOI":"10.1073\/pnas.1701777114","article-title":"Interannual cycles of Hantaan virus outbreaks at the human-animal interface in Central China are controlled by temperature and rainfall","volume":"114","author":"H Tian","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"key":"pntd.0009217.ref037","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1111\/j.1749-6632.2010.05452.x","article-title":"Ecology of hantavirus in a changing world","volume":"1195","author":"MD Dearing","year":"2010","journal-title":"Ann N Y Acad Sci"},{"issue":"5576","key":"pntd.0009217.ref038","doi-asserted-by":"crossref","first-page":"2158","DOI":"10.1126\/science.1063699","article-title":"Climate warming and disease risks for terrestrial and marine biota","volume":"296","author":"CD Harvell","year":"2002","journal-title":"Science"},{"key":"pntd.0009217.ref039","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1186\/1471-2458-7-207","article-title":"Analysis of the geographic distribution of HFRS in Liaoning Province between 2000 and 2005","volume":"7","author":"H Lin","year":"2007","journal-title":"BMC Public Health"},{"issue":"4","key":"pntd.0009217.ref040","doi-asserted-by":"crossref","first-page":"e61536","DOI":"10.1371\/journal.pone.0061536","article-title":"Investigating the effects of food available and climatic variables on the animal host density of hemorrhagic fever with renal syndrome in changsha, china","volume":"8","author":"H Xiao","year":"2013","journal-title":"PLoS One."},{"issue":"6","key":"pntd.0009217.ref041","doi-asserted-by":"crossref","first-page":"e2260","DOI":"10.1371\/journal.pntd.0002260","article-title":"Atmospheric moisture variability and transmission of hemorrhagic fever with renal syndrome in Changsha City, Mainland China, 1991\u20132010","volume":"7","author":"H Xiao","year":"2013","journal-title":"PLoS Negl Trop Dis"},{"key":"pntd.0009217.ref042","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.ijid.2015.02.010","article-title":"Transmission of Hemorrhagic Fever with Renal Syndrome in China and the Role of Climate Factors: A Review","volume":"33","author":"A Hansen","year":"2015","journal-title":"Int J Infect Dis"},{"issue":"9","key":"pntd.0009217.ref043","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.3201\/eid1309.061481","article-title":"Landscape Elements and Hantaan Virus\u2013related Hemorrhagic Fever with Renal Syndrome, People\u2019s Republic of China[J]","volume":"13","author":"Y Lei","year":"2007","journal-title":"Emerging Infectious Diseases"},{"issue":"6","key":"pntd.0009217.ref044","first-page":"731","article-title":"Spatial Change of Dry and Wet Climate Boundary in China in the Recent 50 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