• 1.

    Sahu SS, Dash S, Sonia T, Muthukumaravel S, Sankari T, Gunasekaran K, Jambulingam P, 2018. Entomological investigation of Japanese encephalitis outbreak in Malkangiri district of Odisha state, India. Mem Inst Oswaldo Cruz 113: e170499.

    • Search Google Scholar
    • Export Citation
  • 2.

    Liu B, Gao X, Ma J, Jiao Z, Xiao J, Wang H, 2018. Influence of host and environmental factors on the distribution of the Japanese encephalitis vector Culex tritaeniorhynchus in China. Int J Environ Res Public Health 15: 1848.

    • Search Google Scholar
    • Export Citation
  • 3.

    Ichiro K, Ken-ichi S, Akira K, Yasuaki H, Tomohiko T, 2013. The effect of precipitation on the transmission of Japanese encephalitis (JE) virus in nature: a complex effect on antibody-positive rate to JE virus in sentinel pigs. Int J Environ Res Public Health 10: 18311844.

    • Search Google Scholar
    • Export Citation
  • 4.

    Impoinvil DE, Solomon T, Schluter WW, Rayamajhi A, Bichha RP, Shakya G, Caminade C, Baylis M, 2011. The spatial heterogeneity between Japanese encephalitis incidence distribution and environmental variables in Nepal. PLoS One 6: e22192.

    • Search Google Scholar
    • Export Citation
  • 5.

    Kakoti G, Dutta P, Das BR, Borah J, Mahanta J, 2013. Clinical profile and outcome of Japanese encephalitis in children admitted with acute encephalitis syndrome. Biomed Res Int 2013: e152656.

    • Search Google Scholar
    • Export Citation
  • 6.

    Lannes N, Summerfield A, Filgueira L, 2017. Regulation of inflammation in Japanese encephalitis. J Neuroinflammation 14: 158.

  • 7.

    Kumar K, Arshad SS, Selvarajah GT, Abu J, Toung OP, Abba Y, Yasmin AR, Bande F, Sharma R, Ong BL, 2018. Japanese encephalitis in Malaysia: an overview and timeline. Acta Trop 185: 219229.

    • Search Google Scholar
    • Export Citation
  • 8.

    Duan LL, Shang J, Zhang WM, Ju J, 2019. Analysis of epidemic situation of legal infectious diseases in mainland China in 2010–2017 [in Chinese]. Mod Prev Med 46: 25012506.

    • Search Google Scholar
    • Export Citation
  • 9.

    Baig S, Fox KK, Jee Y, O’Connor P, Hombach J, Wang SA, Hyde T, Fischer M, Hills SL, 2013. Japanese encephalitis surveillance and immunization – Asia and the western Pacific, 2012. MMWR Morb Mortal Wkly Rep 62: 658662.

    • Search Google Scholar
    • Export Citation
  • 10.

    Liang G-D, Huanyu W, 2015. Epidemiology of Japanese encephalitis: past, present, and future prospects. Ther Clin Risk Manag 11: 435448.

  • 11.

    Tao Z, Liu G, Wang M, Wang H, Lin X, Song L, Wang S, Wang H, Liu X, Cui N, 2013. Molecular epidemiology of Japanese encephalitis virus in mosquitoes during an outbreak in China, 2013. Sci Rep 4: 4908.

    • Search Google Scholar
    • Export Citation
  • 12.

    Huanyu W, Yixing L, Xiaofeng L, Guodong L, 2009. Japanese encephalitis in mainland China. Jpn J Infect Dis 62: 331336.

  • 13.

    Zhao X, Cao M, Feng HH, Fan H, Chen F, Feng Z, Li X, Zhou XH, 2014. Japanese encephalitis risk and contextual risk factors in southwest China: a Bayesian hierarchical spatial and spatiotemporal analysis. Int J Environ Res Public Health 11: 42014217.

    • Search Google Scholar
    • Export Citation
  • 14.

    Masuoka P, Klein TA, Kim HC, Claborn DM, Achee N, Andre R, Chamberlin J, Small J, Anyamba A, Dongkyu L, 2010. Modeling the distribution of Culex tritaeniorhynchus to predict Japanese encephalitis distribution in the Republic of Korea. Geospat Health 5: 4557.

    • Search Google Scholar
    • Export Citation
  • 15.

    Wang L 2014. The role of environmental factors in the spatial distribution of Japanese encephalitis in Mainland China. Environ Int 73: 19.

    • Search Google Scholar
    • Export Citation
  • 16.

    Li X, Gao X, Ren Z, Cao Y, Wang J, Liang G, 2014. A spatial and temporal analysis of Japanese encephalitis in Mainland China, 1963–1975: a period without Japanese encephalitis vaccination. PLoS One 9: e99183.

    • Search Google Scholar
    • Export Citation
  • 17.

    Chowdhury FR, Ibrahim QSU, Bari MS, Alam MMJ, Dunachie SJ, Rodriguez-Morales AJ, Patwary MI, 2018. The association between temperature, rainfall and humidity with common climate-sensitive infectious diseases in Bangladesh. PLoS One 13: e0199579.

    • Search Google Scholar
    • Export Citation
  • 18.

    Yang H, Luo P, Wang J, Mou C, Mo L, Wang Z, Fu Y, Lin H, Yang Y, Bhatta LD, 2015. Ecosystem evapotranspiration as a response to climate and vegetation coverage changes in Northwest Yunnan, China. PLoS One 10: e0134795.

    • Search Google Scholar
    • Export Citation
  • 19.

    Zhang F, Liu Z, Zhang C, Jiang B, 2016. Short-term effects of floods on Japanese encephalitis in Nanchong, China, 2007–2012: a time-stratified case-crossover study. Sci Total Environ 563–564: 11051110.

    • Search Google Scholar
    • Export Citation
  • 20.

    Zhang FF, 2017. Short-Term Impacts of Floods and Meteorological Factors on Japanese Encephalitis in Sichuan Province, China, 2005–2012 in Chinese. Jinan, People’s Republic of China: Shandong University.

    • Search Google Scholar
    • Export Citation
  • 21.

    Figueiras A, Roca-Pardinas J, Cadarso-Suarez C, 2005. A bootstrap method to avoid the effect of concurvity in generalised additive models in time series studies of air pollution. J Epidemiol Community Health 59: 881884.

    • Search Google Scholar
    • Export Citation
  • 22.

    Beaumont DC, 1981. Regression diagnostics—identifying influential data and sources of collinearity. J Oper Res Soc 32: 157158.

  • 23.

    Gasparrini A, Armstrong B, Kenward MG, 2010. Distributed lag non-linear models. Stat Med 29: 22242234.

  • 24.

    Li R, Lin H, Liang Y, Zhang T, Luo C, Jiang Z, Xu Q, Xue F, Liu Y, Li X, 2016. The short-term association between meteorological factors and mumps in Jining, China. Sci Total Environ 568: 10691075.

    • Search Google Scholar
    • Export Citation
  • 25.

    Bai Y 2014. Regional impact of climate on Japanese encephalitis in areas located near the three gorges dam. PLoS One 9: e84326.

  • 26.

    Krishnan B, Antonio G, Shakoor H, Liam S, Ben A, 2013. Time series regression studies in environmental epidemiology. Int J Epidemiol 42: 11871195.

  • 27.

    Solomon T, Dung NM, Kneen R, Gainsborough M, Vaughn DW, Khanh VT, 2015. Japanese encephalitis. J Neurol Sci 357: e463.

  • 28.

    Zhang MX, Wang N, Du CL, Li XS, 2017. Application of the distributed lag non-linear model in relation between epidemic encephalitis B and meteorological factors [in Chinese]. Mod Prev Med 44: 17451749 ; 1769.

    • Search Google Scholar
    • Export Citation
  • 29.

    Gasparrini A, 2011. Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 43: 120.

  • 30.

    Zhang S, Hu W, Qi X, Zhuang G, 2018. How socio-environmental factors are associated with Japanese encephalitis in Shaanxi, China-A Bayesian spatial analysis. Int J Environ Res Public Health 15: 608.

    • Search Google Scholar
    • Export Citation
  • 31.

    Borah J, Dutta P, Khan SA, Mahanta J, 2013. Association of weather and anthropogenic factors for transmission of Japanese encephalitis in an endemic area of India. Ecohealth 10: 129136.

    • Search Google Scholar
    • Export Citation
  • 32.

    Lin CL, Chang HL, Lin CY, Chen KT, 2017. Seasonal patterns of Japanese encephalitis and associated meteorological factors in Taiwan. Int J Environ Res Public Health 14: 1317.

    • Search Google Scholar
    • Export Citation
  • 33.

    Gu PQ, Min JG, Gu ZQ, Huang PX, Song HL, 2003. The relationship between the first appearance in spring and seasonal distribution of Culex tritaeniorhynchus and the meteorological conditions in Shanghai. Acta Entomol Sin 46: 325332.

    • Search Google Scholar
    • Export Citation
  • 34.

    Chai C, Wang Q, Cao S, Zhao Q, Wen Y, Huang X, Wen X, Yan Q, Ma X, Wu R, 2018. Serological and molecular epidemiology of Japanese encephalitis virus infections in swine herds in China, 2006–2012. J Vet Sci 19: 151155.

    • Search Google Scholar
    • Export Citation
  • 35.

    Bi P, Zhang Y, Parton KA, 2007. Weather variables and Japanese encephalitis in the metropolitan area of Jinan city, China. J Infect 55: 551556.

    • Search Google Scholar
    • Export Citation
  • 36.

    Krzyzewska A, Wereski S, Dobek M, 2020. Summer UTCI variability in Poland in the twenty-first century. Int J Biometeorol (Epub ahead of print). doi: 10.1007/s00484-020-01965-2.

    • Search Google Scholar
    • Export Citation
  • 37.

    Mansfield KL, Hernandez-Triana LM, Banyard AC, Fooks AR, Johnson N, 2017. Japanese encephalitis virus infection, diagnosis and control in domestic animals. Vet Microbiol 201: 8592.

    • Search Google Scholar
    • Export Citation
  • 38.

    Oya A, Kurane I, 2007. Japanese encephalitis for a reference to international travelers. J Trav Med 14: 259268.

  • 39.

    Ciota A, Kramer LD, 2013. Vector-virus interactions and transmission dynamics of West Nile virus. Virus 5: 30213047.

  • 40.

    Bashar K, Rahman MS, Nodi IJ, Howlader AJ, 2016. Species composition and habitat characterization of mosquito (Diptera: Culicidae) larvae in semi-urban areas of Dhaka, Bangladesh. Pathog Glob Health 110: 4861.

    • Search Google Scholar
    • Export Citation
  • 41.

    Miller RH, Masuoka P, Klein TA, Kim HC, Somer T, Grieco J, 2012. Ecological niche modeling to estimate the distribution of Japanese encephalitis virus in Asia. PLoS Negl Trop Dis 6: 119121.

    • Search Google Scholar
    • Export Citation
  • 42.

    Mordecai EA 2019. Thermal biology of mosquito-borne disease. Ecol Lett 22: 16901708.

  • 43.

    Xu Y, Ramanathan V, Victor DG, 2018. Global warming will happen faster than we think. Nature 564: 3032.

  • 44.

    Rossati A, 2017. Global warming and its health impact. Int J Occup Environ Med 8: 720.

  • 45.

    Li SC, Xue H, Su Y, Sun H, Zhao FH, 2010. Survey of underreporting of notifiable communicable diseases and network direct reporting quality in Ganzhou district in Zhangye, Gansu province [in Chinese]. Dis Surveill 25: 816819.

    • Search Google Scholar
    • Export Citation
  • 46.

    Liu ZT, Li QF, Wang RH, Huang T, Yu JX, 2011. Underreporting of notifiable communicable diseases in medical institutions in Yunnan province [in Chinese]. Dis Surveill 26: 565567.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Nonlinear and Threshold Effect of Meteorological Factors on Japanese Encephalitis Transmission in Southwestern China

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  • 1 Department of Personnel, Qilu Hospital of Shandong University, Jinan, People’s Republic of China;
  • 2 Department of Epidemiology, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, People’s Republic of China;
  • 3 Cheeloo College of Medicine, Shandong University Climate Change and Health Center, Jinan, People’s Republic of China;
  • 4 School of Public Health, The University of Adelaide, Adelaide, Australia;
  • 5 School of Public Health, China Studies Centre, The University of Sydney, Sydney, Australia;
  • 6 School of Public Health, Fujian Medical University, Fuzhou, People’s Republic of China;
  • 7 National Meteorological Center, China Meteorological Administration, Beijing, People’s Republic of China

ABSTRACT

Although previous studies have reported that meteorological factors might affect the risk of Japanese encephalitis (JE), the relationship between meteorological factors and JE remains unclear. This study aimed to evaluate the relationship between meteorological factors and JE and identify the threshold temperature. Daily meteorological data and JE surveillance data in Dazhou, Sichuan, were collected for the study period from 2005 to 2012 (restricting to May–October because of the seasonal distribution of JE). A distributed lag nonlinear model was used to analyze the lagged and cumulative effect of daily average temperature and daily rainfall on JE transmission. A total of 622 JE cases were reported over the study period. We found JE was positively associated with daily average temperature and daily rainfall with a 25-day lag and 30-day lag, respectively. The threshold value of the daily average temperature is 20°C. Each 5°C increase over the threshold would lead to a 13% (95% CI: 1–17.3%) increase in JE. Using 0 mm as the reference, a daily rainfall of 100 mm would lead to a 132% (95% CI: 73–311%) increase in the risk of JE. Japanese encephalitis is climate-sensitive; meteorological factors should be taken into account for the future prevention and control measure making, especially in a warm and rainy weather condition.

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Author Notes

Address correspondence to Baofa Jiang, Department of Epidemiology, School of Public Health, Cheeloo College of Medicine, Shandong University, No. 44 Wenhuaxi Rd., Jinan 250012, People’s Republic of China. E-mail: bjiang@sdu.edu.cn

Disclosure: An ethics exemption from the Ethics Review Committee of Public health Shandong University (20120501) was obtained. All the patient records involved were anonymized and de-identified before receiving.

Financial support: This study was supported by the Special Foundation of Basic Science and Technology Resources Survey of Ministry of Science and Technology (Grant No. 2017FY101202) and the National Basic Research Program of China (973 Program) (Grant No. 2012CB955502).

Authors’ addresses: Zhidong Liu, Department of Personnel, Qilu Hospital of Shandong University, Jinan, People’s Republic of China, E-mail: liuzhidong3105@163.com. Yiwen Zhang, Qi Gao, Shuzi Wang, and Baofa Jiang, Department of Epidemiology, School of Public Health, Shandong University, Jinan, People’s Republic of China, and Cheeloo College of Medicine, Shandong University Climate Change and Health Center, Jinan, People’s Republic of China, E-mails: zhangyiwen@mail.sdu.edu.cn, gqi6835@126.com, wangshuzi830@163.com, and bjiang@sdu.edu.cn. Michael Xiaoliang Tong and Peng Bi, School of Public Health, The University of Adelaide, Adelaide, Australia, E-mails: michael.tong@adelaide.edu.au and peng.bi@adelaide.edu.au. Ying Zhang, School of Public Health, China Studies Centre, The University of Sydney, Sydney, Australia, E-mail: ying.zhang@sydney.edu.au. Jianjun Xiang, School of Public Health, Fujian Medical University, Fuzhou, People’s Republic of China, and The University of Adelaide, Adelaide, Australia, E-mail: jianjun.xiang@adelaide.edu.au. Shuyue Sun, National Meteorological Center, China Meteorological Administration, Beijing, People’s Republic of China, E-mail: sunshy@cma.gov.cn.

These authors contributed equally to this work.

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