{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T14:18:36Z","timestamp":1772201916177,"version":"3.50.1"},"reference-count":42,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2019,4,5]],"date-time":"2019-04-05T00:00:00Z","timestamp":1554422400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2016YFA0600104"],"award-info":[{"award-number":["2016YFA0600104"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81673234"],"award-info":[{"award-number":["81673234"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004826","name":"Beijing Natural Science Foundation","doi-asserted-by":"publisher","award":["JQ18025"],"award-info":[{"award-number":["JQ18025"]}],"id":[{"id":"10.13039\/501100004826","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Young Elite Scientist Sponsorship Program by CAST (YESS)","award":["2018QNRC001"],"award-info":[{"award-number":["2018QNRC001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>The 2009 pandemic influenza virus caused the majority of the influenza A virus infections in China in 2009. It arrived in several Chinese cities from imported cases and then spread as people travelled domestically by all means of transportation, among which road traffic was the most commonly used for daily commuting. Spatial variation in socioeconomic status not only accelerates migration across regions but also partly induces the differences in epidemic processes and in responses to epidemics across regions. However, the roles of both road travel and socioeconomic factors have not received the attention they deserve. Here, we constructed a national highway network for and between 333 cities in mainland China and extracted epidemiological variables and socioeconomic factors for each city. We calculated classic centrality measures for each city in the network and proposed two new measures (SumRatio and Multicenter Distance). We evaluated the correlation between the centrality measures and epidemiological features and conducted a spatial autoregression to quantify the impacts of road network and socioeconomic factors during the outbreak. The results showed that epidemics had more significant relationships with both our new measures than the classic ones. Higher population density, higher per person income, larger SumRatio and Multicenter Distance, more hospitals and college students, and lower per person GDP were associated with higher cumulative incidence. Higher population density and number of slaughtered pigs were found to advance epidemic arrival time. Higher population density, more colleges and slaughtered pigs, and lower Multicenter Distance were associated with longer epidemic duration. In conclusion, road transport and socioeconomic status had significant impacts and should be considered for the prevention and control of future pandemics.<\/jats:p>","DOI":"10.3390\/ijerph16071223","type":"journal-article","created":{"date-parts":[[2019,4,5]],"date-time":"2019-04-05T11:36:01Z","timestamp":1554464161000},"page":"1223","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Impacts of Road Traffic Network and Socioeconomic Factors on the Diffusion of 2009 Pandemic Influenza A (H1N1) in Mainland China"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1920-5829","authenticated-orcid":false,"given":"Bo","family":"Xu","sequence":"first","affiliation":[{"name":"Ministry of Education Key Laboratory for Earth System Modeling, Department of Earth System Science, Tsinghua University, Beijing 100084, China"},{"name":"Joint Center for Global Change Studies, Beijing 100875, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Huaiyu","family":"Tian","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing 100875, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Clive Eric","family":"Sabel","sequence":"additional","affiliation":[{"name":"Department of Environmental Science, Aarhus University, 4000 Roskilde, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bing","family":"Xu","sequence":"additional","affiliation":[{"name":"Ministry of Education Key Laboratory for Earth System Modeling, Department of Earth System Science, Tsinghua University, Beijing 100084, China"},{"name":"Joint Center for Global Change Studies, Beijing 100875, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,4,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2613","DOI":"10.1007\/s11434-011-4598-5","article-title":"Influenza A (H1N1) transmission by road traffic between cities and towns","volume":"56","author":"Xiao","year":"2011","journal-title":"Chin. Sci. Bull."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"11401","DOI":"10.1038\/srep11401","article-title":"Integrated travel network model for studying epidemics: Interplay between journeys and epidemic","volume":"5","author":"Ruan","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1098\/rsif.2010.0142","article-title":"Modelling the influence of human behaviour on the spread of infectious diseases: A review","volume":"7","author":"Funk","year":"2010","journal-title":"J. R. Soc. Interface"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"016111","DOI":"10.1103\/PhysRevE.79.016111","article-title":"Impact of travel patterns on epidemic dynamics in heterogeneous spatial metapopulation networks","volume":"79","author":"Ni","year":"2009","journal-title":"Phys. Rev. E Stat. Nonlinear Soft Matter Phys."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.actatropica.2018.03.026","article-title":"Spatiotemporal responses of dengue fever transmission to the road network in an urban area","volume":"183","author":"Li","year":"2018","journal-title":"Acta Trop."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"A Bozick, B., and Real, L.A. (2015). The Role of Human Transportation Networks in Mediating the Genetic Structure of Seasonal Influenza in the United States. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1004898"},{"key":"ref_7","unstructured":"National Bureau of Statistics of China (2010). China Statistical Yearbook 2009."},{"key":"ref_8","first-page":"120","article-title":"Travel choice characteristics of transportation corridor of Europe-Asia","volume":"5","author":"Peng","year":"2005","journal-title":"J. Traffic Transp. Eng."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1177\/0037549715581637","article-title":"Evaluation of containment and mitigation strategies for an influenza A pandemic in China","volume":"91","author":"Weng","year":"2015","journal-title":"Simulation"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1093\/aje\/kwr411","article-title":"Distribution and risk factors of 2009 pandemic influenza A (H1N1) in mainland China","volume":"175","author":"Fang","year":"2012","journal-title":"Am. J. Epidemiol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Fang, L.Q., de Vlas, S.J., Liang, S., Looman, C.W., Gong, P., Xu, B., Yan, L., Yang, H., Richardus, J.H., and Cao, W.C. (2008). Environmental factors contributing to the spread of H5N1 avian influenza in mainland China. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002268"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.compenvurbsys.2014.12.002","article-title":"Simulating city-level airborne infectious diseases","volume":"51","author":"Mei","year":"2015","journal-title":"Comput. Environ. Urban Syst."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1111\/j.1365-3156.2008.02189.x","article-title":"Geographical spread of SARS in mainland China","volume":"14","author":"Fang","year":"2009","journal-title":"Trop. Med. Int. Health"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Teurlai, M., Huy, R., Cazelles, B., Duboz, R., Baehr, C., and Vong, S. (2012). Can human movements explain heterogeneous propagation of dengue fever in Cambodia?. PLoS Negl. Trop. Dis., 6.","DOI":"10.1371\/journal.pntd.0001957"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"4168","DOI":"10.1007\/s11434-010-4225-x","article-title":"Risk analysis for the highly pathogenic avian influenza in Mainland China using meta-modeling","volume":"55","author":"Cao","year":"2010","journal-title":"Chin. Sci. Bull."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e800","DOI":"10.1016\/j.ijid.2010.03.014","article-title":"Risk factors of poultry outbreaks and human cases of H5N1 avian influenza virus infection in West Java Province, Indonesia","volume":"14","author":"Yupiana","year":"2010","journal-title":"Int. J. Infect. Dis."},{"key":"ref_17","first-page":"320","article-title":"Metapopulation model using commuting flow for national spread of the 2009 H1N1 influenza virus in the Republic of Korea","volume":"454","author":"Lee","year":"2018","journal-title":"J. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4707","DOI":"10.1073\/pnas.1712767115","article-title":"Urbanization prolongs hantavirus epidemics in cities","volume":"115","author":"Tian","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"13839","DOI":"10.1073\/pnas.1612838113","article-title":"Disparities in influenza mortality and transmission related to sociodemographic factors within Chicago in the pandemic of 1918","volume":"113","author":"Grantz","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Wang, L., Wang, J., Xu, C., and Liu, T. (2016). Modelling input-output flows of severe acute respiratory syndrome in mainland China. BMC Public Health, 16.","DOI":"10.1186\/s12889-016-2867-6"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1126\/science.aat6030","article-title":"Urbanization and humidity shape the intensity of influenza epidemics in U.S. cities","volume":"362","author":"Dalziel","year":"2018","journal-title":"Science"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1007\/s11434-013-0084-6","article-title":"Urban structure and the risk of influenza A(H1N1) outbreaks in municipal districts","volume":"59","author":"Xiao","year":"2014","journal-title":"Sci. Bull."},{"key":"ref_23","unstructured":"(2013). MATLAB and Statistics Toolbox, R2013a, The MathWorks, Inc."},{"key":"ref_24","unstructured":"(2011). ArcGIS Desktop, Release 10, Environmental Systems Research Institute."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1145\/367766.368168","article-title":"Algorithm 97: Shortest path","volume":"5","author":"Floyd","year":"1962","journal-title":"Commun. ACM"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.socnet.2010.03.006","article-title":"Node centrality in weighted networks: Generalizing degree and shortest paths","volume":"32","author":"Opsahl","year":"2010","journal-title":"Soc. Netw."},{"key":"ref_27","first-page":"1","article-title":"The igraph software package for complex network research","volume":"1695","year":"2006","journal-title":"InterJournal Complex Syst."},{"key":"ref_28","unstructured":"R Core Team (2016). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Michishita, R., Bing, X., and Yamada, I. (2008, January 28\u201329). Time-series network analysis of civil aviation in Japan, 1985-2005. Proceedings of the Geoinformatics 2008 and Joint Conference on GIS and Built Environment: The Built Environment and its Dynamics, Guangzhou, China.","DOI":"10.1117\/12.812857"},{"key":"ref_30","first-page":"97","article-title":"A study on destination choice behavior of Chinese urban residents","volume":"52","author":"Bihu","year":"1997","journal-title":"Acta Geogr. Sin."},{"key":"ref_31","first-page":"1","article-title":"Spatial relation and layers division of Chinese urban system based on gravity model","volume":"27","author":"Chaolin","year":"2008","journal-title":"Geogr. Res."},{"key":"ref_32","unstructured":"Zhang, Y. (2011). Spreading of Influenza A (H1N1) in Mainland China: Modeling and Analysis. [Master\u2019s Thesis, Beijing Normal University]."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1111\/j.1467-9787.2008.00573.x","article-title":"Spatial econometric modeling of origin-destination flows","volume":"48","author":"Lesage","year":"2010","journal-title":"J. Reg. Sci."},{"key":"ref_34","first-page":"780","article-title":"Epidemiological characteristics of confirmed cases of pandemic influenza A(H1N1) 2009 in mainland China, 2009-2010","volume":"26","author":"Sun","year":"2011","journal-title":"Dis. Surveill."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.jinf.2011.03.011","article-title":"The clustering and transmission dynamics of pandemic influenza A (H1N1) 2009 cases in Hong Kong","volume":"63","author":"Lee","year":"2011","journal-title":"J. Infect."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"S783","DOI":"10.1098\/rsif.2009.0302.focus","article-title":"Aerosol transmission of influenza A virus: A review of new studies","volume":"6","author":"Tellier","year":"2009","journal-title":"J. R. Soc. Interface"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"758","DOI":"10.3201\/eid1805.110356","article-title":"Transmission dynamics, border entry screening, and school holidays during the 2009 influenza A (H1N1) pandemic, China","volume":"18","author":"Yu","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Holmes, E.C., and Grenfell, B.T. (2009). Discovering the phylodynamics of RNA viruses. PLoS Comput. Biol., 5.","DOI":"10.1371\/journal.pcbi.1000505"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"7588","DOI":"10.1073\/pnas.0611071104","article-title":"The effect of public health measures on the 1918 influenza pandemic in U.S. cities","volume":"104","author":"Bootsma","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1016\/S1473-3099(09)70176-8","article-title":"Closure of schools during an influenza pandemic","volume":"9","author":"Cauchemez","year":"2009","journal-title":"Lancet Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Cai, J., Xu, B., Chan, K.K.Y., Zhang, X., Zhang, B., Chen, Z., and Xu, B. (2019). Roles of Different Transport Modes in the Spatial Spread of the 2009 Influenza A(H1N1) Pandemic in Mainland China. Int. J. Environ. Res. Public Health, 16.","DOI":"10.3390\/ijerph16020222"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Garske, T., Yu, H., Peng, Z., Ye, M., Zhou, H., Cheng, X., Wu, J., and Ferguson, N. (2011). Travel patterns in China. PLoS ONE, 6.","DOI":"10.1371\/annotation\/e4781265-2e4f-45a9-85b7-1930e0a16171"}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/16\/7\/1223\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:43:12Z","timestamp":1760186592000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/16\/7\/1223"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,4,5]]},"references-count":42,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2019,4]]}},"alternative-id":["ijerph16071223"],"URL":"https:\/\/doi.org\/10.3390\/ijerph16071223","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,4,5]]}}}