{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,15]],"date-time":"2026-07-15T23:24:20Z","timestamp":1784157860778,"version":"3.55.0"},"update-to":[{"DOI":"10.1371\/journal.pntd.0010806","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,8,3]],"date-time":"2023-08-03T00:00:00Z","timestamp":1691020800000}}],"reference-count":47,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2023,7,24]],"date-time":"2023-07-24T00:00:00Z","timestamp":1690156800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"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) is a rodent-related zoonotic disease induced by hantavirus. Previous studies have identified the influence of meteorological factors on the onset of HFRS, but few studies have focused on the stratified analysis of the lagged effects and interactions of pollution and meteorological factors on HFRS.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>We collected meteorological, contaminant and epidemiological data on cases of HFRS in Shenyang from 2005\u20132019. A seasonal autoregressive integrated moving average (SARIMA) model was used to predict the incidence of HFRS and compared with Holt-Winters three-parameter exponential smoothing model. A distributed lag nonlinear model (DLNM) with a maximum lag period of 16 days was applied to assess the lag, stratification and extreme effects of pollution and meteorological factors on HFRS cases, followed by a generalized additive model (GAM) to explore the interaction of SO<jats:sub>2<\/jats:sub> and two other meteorological factors on HFRS cases.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>The SARIMA monthly model has better fit and forecasting power than its own quarterly model and the Holt-Winters model, with an optimal model of (1,1,0) (2,1,0)<jats:sub>12<\/jats:sub>. Overall, environmental factors including humidity, wind speed and SO<jats:sub>2<\/jats:sub> were correlated with the onset of HFRS and there was a non-linear exposure-lag-response association. Extremely high SO<jats:sub>2<\/jats:sub> increased the risk of HFRS incidence, with the maximum RR values: 2.583 (95%CI:1.145,5.827). Extremely low windy and low SO<jats:sub>2<\/jats:sub> played a significant protective role on HFRS infection, with the minimum RR values: 0.487 (95%CI:0.260,0.912) and 0.577 (95%CI:0.370,0.898), respectively. Interaction indicated that the risk of HFRS infection reached its highest when increasing daily SO<jats:sub>2<\/jats:sub> and decreasing humidity.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>The SARIMA model may help to enhance the forecast of monthly HFRS incidence based on a long-range dataset. Our study had shown that environmental factors such as humidity and SO<jats:sub>2<\/jats:sub> have a delayed effect on the occurrence of HFRS and that the effect of humidity can be influenced by SO<jats:sub>2<\/jats:sub> and wind speed. Public health professionals should take greater care in controlling HFRS in low humidity, low windy conditions and 2\u20133 days after SO<jats:sub>2<\/jats:sub> levels above 200 \u03bcg\/m<jats:sup>3<\/jats:sup>.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pntd.0010806","type":"journal-article","created":{"date-parts":[[2023,7,24]],"date-time":"2023-07-24T17:25:37Z","timestamp":1690219537000},"page":"e0010806","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":20,"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"],"prefix":"10.1371","volume":"17","author":[{"given":"Ye","family":"Chen","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weiming","family":"Hou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9353-2246","authenticated-orcid":true,"given":"Jing","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,7,24]]},"reference":[{"key":"pntd.0010806.ref001","doi-asserted-by":"crossref","first-page":"e6","DOI":"10.1111\/1469-0691.12291","article-title":"Hantavirus infections","volume":"21S","author":"T Avsic-Zupanc","year":"2019","journal-title":"Clin Microbiol Infect"},{"issue":"3","key":"pntd.0010806.ref002","first-page":"544","article-title":"New cases of suspected HFRS (Hantavirus infection) in south-eastern Poland","volume":"20","author":"AK Gut","year":"2013","journal-title":"Ann Agric Environ Med"},{"issue":"3","key":"pntd.0010806.ref003","doi-asserted-by":"crossref","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\u20132018","volume":"15","author":"W Sun","year":"2021","journal-title":"PLoS Negl Trop Dis"},{"issue":"8","key":"pntd.0010806.ref004","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.3201\/eid1608.090470","article-title":"Hantavirus Infections in Humans and Animals, China","volume":"16","author":"Y-Z Zhang","year":"2010","journal-title":"Emerging Infectious Diseases"},{"issue":"10","key":"pntd.0010806.ref005","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/S1473-3099(03)00774-6","article-title":"Hantavirus Infections in Europe","volume":"3","author":"O Vapalahti","year":"2003","journal-title":"The Lancet Infectious Diseases"},{"issue":"2","key":"pntd.0010806.ref006","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1586\/14787210.7.2.205","article-title":"Hantavirus infections in Europe: from virus carriers to a major public-health problem","volume":"7","author":"P Heyman","year":"2009","journal-title":"Expert Review of Anti-infective Therapy"},{"issue":"2","key":"pntd.0010806.ref007","doi-asserted-by":"crossref","first-page":"95","DOI":"10.3201\/eid0302.970202","article-title":"Hantaviruses: a global disease problem","volume":"3","author":"C Schmaljohn","year":"1997","journal-title":"Emerg Infect Dis"},{"issue":"6","key":"pntd.0010806.ref008","doi-asserted-by":"crossref","first-page":"e0006554","DOI":"10.1371\/journal.pntd.0006554","article-title":"Spatiotemporal variation of the association between climate dynamics and HFRS outbreaks in Eastern China during 2005\u20132016 and its geographic determinants","volume":"12","author":"J He","year":"2018","journal-title":"PLoS Negl Trop Dis"},{"issue":"11","key":"pntd.0010806.ref009","first-page":"857","article-title":"Epidemiologic surveillance on the hemorrhagic fever with renal syndrome in China","volume":"106","author":"HX Chen","year":"1993","journal-title":"Chin Med J"},{"key":"pntd.0010806.ref010","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1186\/1471-2334-11-218","article-title":"Forecasting incidence of hemorrhagic fever with renal syndrome in China using ARIMA model","volume":"11","author":"Q Liu","year":"2011","journal-title":"BMC Infect Dis"},{"issue":"7883","key":"pntd.0010806.ref011","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1038\/s41586-021-04043-8","article-title":"Disease variant prediction with deep generative models of evolutionary data","volume":"599","author":"J Frazer","year":"2021","journal-title":"Nature"},{"issue":"1","key":"pntd.0010806.ref012","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1186\/s12889-021-10383-x","article-title":"Forecasting the incidence of mumps in Chongqing based on a SARIMA model","volume":"21","author":"H Qiu","year":"2021","journal-title":"BMC Public Health"},{"issue":"1","key":"pntd.0010806.ref013","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1186\/s12874-020-01130-8","article-title":"SARFIMA model prediction for infectious diseases: application to hemorrhagic fever with renal syndrome and comparing with SARIMA","volume":"20","author":"C Qi","year":"2020","journal-title":"BMC Med Res Methodol"},{"issue":"2","key":"pntd.0010806.ref014","doi-asserted-by":"crossref","first-page":"e1006770","DOI":"10.1371\/journal.ppat.1006770","article-title":"Influenza interaction with cocirculating pathogens and its impact on surveillance, pathogenesis, and epidemic profile: A key role for mathematical modelling","volume":"14","author":"L Opatowski","year":"2018","journal-title":"PLoS Pathog"},{"issue":"1","key":"pntd.0010806.ref015","doi-asserted-by":"crossref","first-page":"e28269","DOI":"10.1002\/jmv.28269","article-title":"Spatial-temporal dynamics and time series prediction of HFRS in mainland China: A long-term retrospective study","volume":"95","author":"J He","year":"2023","journal-title":"J Med Virol"},{"issue":"2","key":"pntd.0010806.ref016","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":"The American Society of Tropical Medicine and Hygiene"},{"issue":"1","key":"pntd.0010806.ref017","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.virusres.2008.06.012","article-title":"Genetic analysis of hantaviruses carried by reed voles Microtus fortis in China","volume":"137","author":"Y Zou","year":"2008","journal-title":"Virus Res"},{"issue":"8","key":"pntd.0010806.ref018","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.0010806.ref019","doi-asserted-by":"crossref","first-page":"e1006198","DOI":"10.1371\/journal.ppat.1006198","article-title":"Anthropogenically driven environmental changes shift the ecological dynamics of hemorrhagic fever with renal syndrome","volume":"13","author":"H Tian","year":"2017","journal-title":"PLoS PathogPubMed Central PMCID"},{"key":"pntd.0010806.ref020","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1186\/1471-2334-11-331","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":"7","key":"pntd.0010806.ref021","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":"6","key":"pntd.0010806.ref022","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1111\/zph.12175","article-title":"Climate Variability and the Occurrence of Human Puumala Hantavirus Infections in Europe: A Systematic Review","volume":"62","author":"J Roda Gracia","year":"2015","journal-title":"Zoonoses Public Health"},{"issue":"1","key":"pntd.0010806.ref023","doi-asserted-by":"crossref","first-page":"20037","DOI":"10.1038\/s41598-022-23945-9","article-title":"Meteorological change and hemorrhagic fever with renal syndrome epidemic in China, 2004\u20132018","volume":"12","author":"Y Luo","year":"2022","journal-title":"Sci Rep"},{"issue":"2","key":"pntd.0010806.ref024","first-page":"160339","article-title":"Dual seasonal pattern for hemorrhagic fever with renal syndrome and its potential determinants in China","volume":"859","author":"CL Lv","year":"2023","journal-title":"Sci Total Environ"},{"key":"pntd.0010806.ref025","article-title":"Analysis on epidemiological characteristics of scarlet fever,Shenyang city,2013\u20132017","author":"MY Dai","year":"2018","journal-title":"Preventive Medicine Tribune"},{"issue":"11","key":"pntd.0010806.ref026","doi-asserted-by":"crossref","first-page":"e3344","DOI":"10.1371\/journal.pntd.0003344","article-title":"Spatiotemporal transmission dynamics of hemorrhagic fever with renal syndrome in China, 2005\u20132012","volume":"8","author":"WY Zhang","year":"2014","journal-title":"PLoS Negl Trop Dis"},{"issue":"23","key":"pntd.0010806.ref027","doi-asserted-by":"crossref","first-page":"23603","DOI":"10.1007\/s11356-019-05565-5","article-title":"Short-term exposure to ambient air pollution and daily atherosclerotic heart disease mortality in a cool climate","volume":"26","author":"G Liu","year":"2019","journal-title":"Environ Sci Pollut Res Int"},{"issue":"5","key":"pntd.0010806.ref028","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1016\/j.jiph.2018.04.009","article-title":"Forecasting the incidence of tuberculosis in China using the seasonal auto-regressive integrated moving average (SARIMA) model","volume":"11","author":"Q Mao","year":"2018","journal-title":"J Infect Public Health"},{"issue":"7","key":"pntd.0010806.ref029","doi-asserted-by":"crossref","first-page":"e0219889","DOI":"10.1371\/journal.pone.0219889","article-title":"Spring onion seed demand forecasting using a hybrid Holt-Winters and support vector machine model","volume":"14","author":"Y Zhu","year":"2019","journal-title":"PLoS One"},{"key":"pntd.0010806.ref030","author":"E Harrison","year":"2012","journal-title":"Arima Fit to Nigerian Unemployment Data"},{"issue":"18","key":"pntd.0010806.ref031","doi-asserted-by":"crossref","first-page":"11299","DOI":"10.1039\/C6CP08437K","article-title":"Application of machine\/statistical learning, artificial intelligence and statistical experimental design for the modeling and optimization of methylene blue and Cd(ii) removal from a binary aqueous solution by natural walnut carbon","volume":"19","author":"H Mazaheri","year":"2017","journal-title":"Phys Chem Chem Phys"},{"key":"pntd.0010806.ref032","doi-asserted-by":"crossref","first-page":"871768","DOI":"10.3389\/fnut.2022.871768","article-title":"Interaction Analysis Based on Shapley Values and Extreme Gradient Boosting: A Realistic Simulation and Application to a Large Epidemiological Prospective Study","volume":"9","author":"N Orsini","year":"2022","journal-title":"Front Nutr"},{"issue":"1","key":"pntd.0010806.ref033","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1890\/0012-9658(2007)88[243:BTFEMA]2.0.CO;2","article-title":"Boosted trees for ecological modeling and prediction","volume":"88","author":"G. De\u2019ath","year":"2007","journal-title":"Ecology"},{"key":"pntd.0010806.ref034","doi-asserted-by":"crossref","first-page":"121769","DOI":"10.1016\/j.jhazmat.2019.121769","article-title":"Bio-inspired, high, and fast adsorption of tetracycline from aqueous media using Fe(3)O(4)-g-CN@PEI-\u03b2-CD nanocomposite: Modeling by response surface methodology (RSM), boosted regression tree (BRT), and general regression neural network","volume":"388","author":"M Foroughi","year":"2020","journal-title":"J Hazard Mater"},{"key":"pntd.0010806.ref035","doi-asserted-by":"crossref","first-page":"143821","DOI":"10.1016\/j.scitotenv.2020.143821","article-title":"Associations between weekly air pollution exposure and congenital heart disease","volume":"757","author":"Q Zhang","year":"2021","journal-title":"Sci Total Environ"},{"issue":"9","key":"pntd.0010806.ref036","article-title":"The Mortality Effect of Apparent Temperature: A Multi-City Study in Asia","volume":"18","author":"R Cao","year":"2021","journal-title":"Int J Environ Res Public Health"},{"key":"pntd.0010806.ref037","doi-asserted-by":"crossref","first-page":"e248","DOI":"10.1017\/S0950268820002344","article-title":"Investigation on risk factors of haemorrhagic fever with renal syndrome (HFRS) in Xuancheng City in Anhui Province, Mainland China","volume":"148","author":"G Wu","year":"2020","journal-title":"Epidemiol Infect"},{"issue":"13","key":"pntd.0010806.ref038","doi-asserted-by":"crossref","first-page":"1680","DOI":"10.1017\/S0950268818002030","article-title":"Spatiotemporal analysis and forecasting model of hemorrhagic fever with renal syndrome in mainland China","volume":"146","author":"L Sun","year":"2018","journal-title":"Epidemiol Infect"},{"issue":"19","key":"pntd.0010806.ref039","doi-asserted-by":"crossref","first-page":"12551","DOI":"10.1007\/s00521-021-05901-2","article-title":"Long-term time-series pollution forecast using statistical and deep learning methods","volume":"33","author":"P Nath","year":"2021","journal-title":"Neural Comput Appl"},{"issue":"9","key":"pntd.0010806.ref040","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"},{"key":"pntd.0010806.ref041","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1016\/j.scitotenv.2015.09.027","article-title":"Short-term effects of meteorological factors on hand, foot and mouth disease among children in Shenzhen, China: Non-linearity, threshold and interaction","volume":"539","author":"Z Zhang","year":"2016","journal-title":"Sci Total Environ"},{"issue":"7","key":"pntd.0010806.ref042","doi-asserted-by":"crossref","first-page":"1580","DOI":"10.1128\/aem.53.7.1580-1583.1987","article-title":"Estimating downwind concentrations of viable airborne microorganisms in dynamic atmospheric conditions","volume":"53","author":"B Lighthart","year":"1987","journal-title":"Appl Environ Microbiol"},{"key":"pntd.0010806.ref043","doi-asserted-by":"crossref","first-page":"e11397","DOI":"10.7717\/peerj.11397","article-title":"Air pollutants and outpatient visits for influenza-like illness in Beijing, China","volume":"9","author":"X Li","year":"2021","journal-title":"PeerJ"},{"key":"pntd.0010806.ref044","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1016\/j.scitotenv.2018.07.329","article-title":"Short-term effects of meteorological factors and air pollution on childhood hand-foot-mouth disease in Guilin, China","volume":"646","author":"G Yu","year":"2019","journal-title":"Sci Total Environ"},{"issue":"14","key":"pntd.0010806.ref045","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1080\/08958370701665434","article-title":"Air pollution and respiratory viral infection","volume":"19","author":"J Ciencewicki","year":"2007","journal-title":"Inhal Toxicol"},{"issue":"5","key":"pntd.0010806.ref046","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.jinf.2008.08.013","article-title":"Inactivation of influenza A viruses in the environment and modes of transmission: a critical review","volume":"57","author":"TP Weber","year":"2008","journal-title":"J Infect"},{"issue":"2","key":"pntd.0010806.ref047","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"}],"updated-by":[{"DOI":"10.1371\/journal.pntd.0010806","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,8,3]],"date-time":"2023-08-03T00:00:00Z","timestamp":1691020800000}}],"container-title":["PLOS Neglected Tropical Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0010806","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,3]],"date-time":"2023-08-03T17:53:10Z","timestamp":1691085190000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pntd.0010806"}},"subtitle":[],"editor":[{"given":"Christopher M.","family":"Barker","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,7,24]]},"references-count":47,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2023,7,24]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pntd.0010806","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pntd.0010806","asserted-by":"object"}]},"ISSN":["1935-2735"],"issn-type":[{"value":"1935-2735","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,24]]}}}