Effects of Humidity Variation on the Hantavirus Infection and Hemorrhagic Fever with Renal Syndrome Occurrence in Subtropical China

Hong Xiao College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Ru Huang College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Li-Dong Gao College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Cun-Rui Huang College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Xiao-Ling Lin College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Na Li College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Hai-Ning Liu College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Shi-Lu Tong College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Huai-Yu Tian College of Resources and Environment Science, Hunan Normal University, Changsha, China; Hunan Provincial Center for Disease Control and Prevention, Changsha, China; School of Public Health, Sun Yat-Sen University, Guangzhou, China; Weizikeng Center for Disease Control and Prevention, Beijing, China; School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia; State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China

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Infection rates of rodents have a significant influence on the transmission of hemorrhagic fever with renal syndrome (HFRS). In this study, four cities and two counties with high HFRS incidence in eastern Hunan Province in China were studied, and surveillance data of rodents, as well as HFRS cases and related environmental variables from 2007 to 2010, were collected. Results indicate that the distribution and infection rates of rodents are closely associated with environmental conditions. Hantavirus infections in rodents were positively correlated with temperature vegetation dryness index and negatively correlated with elevation. The predictive risk maps based on multivariate regression model revealed that the annual variation of infection risks is small, whereas monthly variation is large and corresponded well to the seasonal variation of human HFRS incidence. The identification of risk factors and risk prediction provides decision support for rodent surveillance and the prevention and control of HFRS.

Author Notes

* Address correspondence to Hong Xiao, College of Resources and Environment Science, Hunan Normal University, 36 Lushan Road, Changsha 410081, China, E-mail: xiaohong.hnnu@gmail.com or Huai-Yu Tian, State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, 19 Xinjiekou Outer Street, Beijing 100875, China, E-mail: tianhuaiyu@gmail.com
† These authors contributed equally to this work.

Financial support: This work was supported by the Key Discipline Construction Project in Hunan Province (2008001), National Natural Science Foundation (40971038), Scientific Research Fund of the Hunan Provincial Education Department (11K037), Hunan Provincial Natural Science Foundation of China (11JJ3119), Science and Technology Planning Project of Hunan Province of China (2010SK3007), and Key Subject Construction Project of Hunan Normal University (geographic information systems).

Authors' addresses: Hong Xiao, Ru Huang, Xiao-Ling Lin, and Hai-Ning Liu, College of Resources and Environment Science, Hunan Normal University, Changsha, China, E-mails: xiaohong.hnnu@gmail.com, huangru@qq.com, linxiaoling@qq.com, and liuhaining@qq.com. Li-Dong Gao, Hunan Provincial Center for Disease Control and Prevention, Changsha, China, E-mail: gldcdc@qq.com. Cun-Rui Huang, School of Public Health, Sun Yat-Sen University, Guangzhou, China, E-mail: huangcunrui@hotmail.com. Na Li, Weizikeng Center for Disease Control and Prevention, Beijing, China, E-mail: gw_lina@126.com. Shi-Lu Tong, School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia, E-mail: s.tong@qut.edu.au. Huai-Yu Tian, State Key Laboratory of Remote Sensing Science, College of Global Change and Earth System Science, Beijing Normal University, Beijing, China, E-mail: tianhuaiyu@gmail.com.

  • 1.

    Luo CW, Chen HX, 2003. Study on the factors influenced epidemic of hemorrhagic fever with renal syndrome [in Chinese]. Chin J Vector Bio Control 14: 451–454.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Van Loock F, Thomas I, Clement J, Ghoos S, Colson P, 1999. A case-control study after a hantavirus infection outbreak in the south of Belgium: who is at risk? Clin Infect Dis 28: 834–839.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Hjelle B, Glass GE, 2000. Outbreak of hantavirus infection in the Four Corners region of the United States in the wake of the 1997–1998 El Nino-southern oscillation. J Infect Dis 181: 1569–1573.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Glass GE, Shields T, Cai B, Yates TL, Parmenter R, 2007. Persistently highest risk areas for hantavirus pulmonary syndrome: potential sites for refugia. Ecol Appl 17: 129–139.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Viel JF, Lefebvre A, Marianneau P, Joly D, Giraudoux P, Upegui E, Tordo N, Hoen B, 2011. Environmental risk factors for haemorrhagic fever with renal syndrome in a French new epidemic area. Epidemiol Infect 139: 867–874.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Kallio ER, Begon M, Henttonen H, Koskela E, Mappes T, Vaheri A, Vapalahti O, 2009. Cyclic hantavirus epidemics in humans—predicted by rodent host dynamics. Epidemics 1: 101–107.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Tian HY, Yu PB, Luis AD, Bi P, Cazelles B, Huang SQ, Ma CF, Zhou S, Wei J, Li S, Lu XL, Qu JH, Jong JH, Tong SL, Wang JJ, Grenfell B, Xu B, 2015. Changes in rodent abundance and weather conditions potentially drive hemorrhagic fever with renal syndrome outbreaks in Xi'an, China, 2005–2012. PLoS Negl Trop Dis 9: e0003530.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Padula P, Figueroa R, Navarrete M, Pizarro E, Cadiz R, Bellomo C, Jofre C, Zaror L, Rodriguez E, Murua R, 2004. Transmission study of Andes hantavirus infection in wild sigmodontine rodents. J Virol 78: 11972–11979.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Douglass RJ, Wilson T, Semmens WJ, Zanto SN, Bond CW, Van Horn RC, Mills JN, 2001. Longitudinal studies of Sin Nombre virus in deer mouse-dominated ecosystems of Montana. Am J Trop Med Hyg 65: 33–41.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Kausrud KL, Mysterud A, Steen H, Vik JO, Østbye E, Cazelles B, Framstad E, Eikeset AM, Mysterud I, Solhøy T, 2008. Linking climate change to lemming cycles. Nature 456: 93–97.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Luis AD, Douglass RJ, Mills JN, Bjørnstad ON, 2010. The effect of seasonality, density and climate on the population dynamics of Montana deer mice, important reservoir hosts for Sin Nombre hantavirus. J Anim Ecol 79: 462–470.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Zhang WY, Fang LQ, Jiang JF, Hui FM, Glass GE, Yan L, Xu YF, Zhao WJ, Yang H, Liu W, 2009. Predicting the risk of hantavirus infection in Beijing, People's Republic of China. Am J Trop Med Hyg 80: 678–683.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Wei L, Qian Q, Wang ZQ, Glass GE, Song SX, Zhang WY, Li XJ, Yang H, Wang XJ, Fang LQ, Cao WC, 2011. Using geographic information system-based ecologic niche models to forecast the risk of hantavirus infection in Shandong Province, China. Am J Trop Med Hyg 84: 497–503.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Yan L, Fang LQ, Huang HG, Zhang LQ, Feng D, Zhao WJ, Zhang WY, Li XW, Cao WC, 2007. Landscape elements and Hantaan virus-related hemorrhagic fever with renal syndrome, People's Republic of China. Emerg Infect Dis 13: 1301–1306.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Zhang WY, Guo WD, Fang LQ, Li CP, Bi P, Glass GE, Jiang JF, Sun SH, Qian Q, Liu W, 2010. Climate variability and hemorrhagic fever with renal syndrome transmission in northeastern China. Environ Health Perspect 118: 915–920.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Liu YZ, Peng JP, Long QZ, 2000. Analysis on surveillance results of hemorrhagic fever with renal syndrome in Hunan Province from 1994 to 1998 [in Chinese]. Pract Prev Med 7: 345–346.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Ma GH, Gao LD, Yang YQ, Xiao H, Tian HY, 2015. Spatial and temporal statistical modeling of hand, foot, and mouth disease and its characteristics in China: a review. Infect Dis Transl Med 1: 23–29.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Liu FQ, Gao LD, Dai DF, Zhang H, Zeng K, Guo SH, 2008. Analysis on surveillance results of hemorrhagic fever with renal syndrome in 2007 in Hunan Province [in Chinese]. Chin J Nat Med 10: 199–202.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Hardestam J, Simon M, Hedlund K, Vaheri A, Klingström J, Lundkvist Å, 2007. Ex vivo stability of the rodent-borne Hantaan virus in comparison to that of arthropod-borne members of the Bunyaviridae family. Appl Environ Microbiol 73: 2547–2551.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Ma CF, Yu PB, Nawaz MHM, Zuo SQ, Jin TZ, Li YL, Li LIJS, Xu HX Jr, 2012. Hantaviruses in rodents and humans, Xi'an, PR China. J Gen Virol 93: 2227–2236.

  • 21.

    Ministry of Health, 1998. Handbook of Epidemic Hemorrhagic Fever Prevention and Control. Beijing, China: China People's Health Publishing House.

  • 22.

    Sandholt I, Rasmussen K, Andersen J, 2002. A simple interpretation of the surface temperature/vegetation index space for assessment of surface moisture status. Remote Sens Environ 79: 213–224.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Bi P, Tong SL, Donald K, Parton K, Ni JF, 2002. Climatic, reservoir and occupational variables and the transmission of haemorrhagic fever with renal syndrome in China. Int J Epidemiol 31: 189–193.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Yan L, Huang HG, Zhang WY, Wang JB, Ren YH, Fang LQ, Huang XX, Cao WC, Yan SY, Wang SW, 2009. The relationship between hemorrhagic fever with renal syndrome cases and time series of NDVI in Dayangshu District. J Remote Sens 13: 873–878.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Huete A, Didan K, Miura T, Rodriguez EP, Gao X, Ferreira LG, 2002. Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sens Environ 83: 195–213.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Ernest SK, Brown JH, Parmenter RR, 2000. Rodents, plants, and precipitation: spatial and temporal dynamics of consumers and resources. Oikos 88: 470–482.

  • 27.

    Previtali MA, Lima M, Meserve PL, Kelt DA, Gutiérrez JR, 2009. Population dynamics of two sympatric rodents in a variable environment: rainfall, resource availability, and predation. Ecology 90: 1996–2006.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Xiao H, Tian HY, Zhang XX, Zhao J, Zhu PJ, Liu RC, Chen TM, Dai XY, Lin XL, 2011. The warning model and influence of climatic changes on hemorrhagic fever with renal syndrome in Changsha city [in Chinese]. Chin J Prev Med 45: 881–885.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Engelthaler DM, Mosley DG, Cheek JE, Levy CE, Komatsu KK, Ettestad P, Davis T, Tanda DT, Miller L, Frampton JW, 1999. Climatic and environmental patterns associated with hantavirus pulmonary syndrome, Four Corners region, United States. Emerg Infect Dis 5: 87–94.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Brown JH, Ernest SKM, 2002. Rain and rodents: complex dynamics of desert consumers. Bioscience 52: 979–987.

  • 31.

    Luo CW, Liu QY, 2007. The epidemic factors analysis of natural focus diseases and their countermeasures [in Chinese]. Chin J Vector Bio Control 18: 293–297.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Xiao H, Lin X, Gao L, Huang C, Tian H, Li N, Qin J, Zhu P, Chen B, Zhang X, 2013. Ecology and geography of hemorrhagic fever with renal syndrome in Changsha, China. BMC Infect Dis 13: 305.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Zhang GP, Liu JY, Zhang ZX, 2003. Spatial-temporal changes of cropland in China for the past 10 years based on remote sensing. Acta Geogr Sin 58: 323–332.

  • 34.

    Zhang MW, Wang Y, Li B, Chen AG, 2003. The rodent pest control of the social economical natural complex ecosystem [in Chinese]. Acta Theriologica Sinica 23: 250–258.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Dai DF, Zhang H, Liu YZ, Liu FQ, Li FC, Gao LD, Wu ZG, Li W, 2007. Monitoring study on hemorrhagic fever with renal syndrome (HFRS) in Hunan Province [in Chinese]. Dis Surveill 22: 78–82.

    • PubMed
    • Search Google Scholar
    • Export Citation
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