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Extreme weather events and dengue outbreaks in Guangzhou, China: a time-series quasi-binomial distributed lag non-linear model

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Abstract

Dengue transmission is climate-sensitive and permissive conditions regularly cause large outbreaks in Asia-Pacific area. As climate change progresses, extreme weather events such as heatwaves and unusually high rainfall are predicted more intense and frequent, but their impacts on dengue outbreaks remain unclear so far. This paper aimed to investigate the relationship between extreme weather events (i.e., heatwaves, extremely high rainfall and extremely high humidity) and dengue outbreaks in China. We obtained daily number of locally acquired dengue cases and weather factors for Guangzhou, China, for the period 2006–2015. The definition of dengue outbreaks was based on daily number of locally acquired cases above the threshold (i.e., mean + 2SD of daily distribution of dengue cases during peaking period). Heatwave was defined as ≥2 days with temperature ≥ 95th percentile, and extreme rainfall and humidity defined as daily values ≥95th percentile during 2006–2015. A generalized additive model was used to examine the associations between extreme weather events and dengue outbreaks. Results showed that all three extreme weather events were associated with increased risk of dengue outbreaks, with a risk increase of 115–251% around 6 weeks after heatwaves, 173–258% around 6–13 weeks after extremely high rainfall, and 572–587% around 6–13 weeks after extremely high humidity. Each extreme weather event also had good capacity in predicting dengue outbreaks, with the model’s sensitivity, specificity, accuracy, and area under the receiver operating characteristics curve all exceeding 86%. This study found that heatwaves, extremely high rainfall, and extremely high humidity could act as potential drivers of dengue outbreaks.

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References

  • Anyamba A, Small JL, Britch SC, Tucker CJ, Pak EW, Reynolds CA, Crutchfield J, Linthicum KJ (2014) Recent weather extremes and impacts on agricultural production and vector-borne disease outbreak patterns. PLoS One 9(3):e92538

    Article  Google Scholar 

  • Badurdeen S, Valladares DB, Farrar J, Gozzer E, Kroeger A, Kuswara N, Ranzinger SR, Tinh HT, Leite P, Mahendradhata Y, Skewes R, Verrall A, European Union WHOsIsg (2013) Sharing experiences: towards an evidence based model of dengue surveillance and outbreak response in Latin America and Asia. BMC Public Health 13:607

    Article  Google Scholar 

  • Banu S, Hu W, Guo Y, Hurst C, Tong S (2014) Projecting the impact of climate change on dengue transmission in Dhaka, Bangladesh. Environ Int 63:137–142

    Article  Google Scholar 

  • Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI (2013) The global distribution and burden of dengue. Nature 496(7446):504–507

    Article  CAS  Google Scholar 

  • Brady OJ, Smith DL, Scott TW, Hay SI (2015) Dengue disease outbreak definitions are implicitly variable. Epidemics 11:92–102

    Article  Google Scholar 

  • Chaves LF, Scott TW, Morrison AC, Takada T (2014) Hot temperatures can force delayed mosquito outbreaks via sequential changes in Aedes aegypti demographic parameters in autocorrelated environments. Acta Trop 129:15–24

    Article  Google Scholar 

  • Cheng J, Wu J, Xu Z, Zhu R, Wang X, Li K, Wen L, Yang H, Su H (2014) Associations between extreme precipitation and childhood hand, foot and mouth disease in urban and rural areas in Hefei, China. Sci Total Environ 497-498:484–490

    Article  CAS  Google Scholar 

  • Cheng Q, Jing Q, Spear RC, Marshall JM, Yang Z, Gong P (2017) The interplay of climate, intervention and imported cases as determinants of the 2014 dengue outbreak in Guangzhou. PLoS Negl Trop Dis 11(6):e0005701

    Article  Google Scholar 

  • Cheng J, Zhang Y, Zhang W, Xu Z, Bambrick H, Hu W, Tong S (2018) Assessment of heat- and cold-related emergency department visits in cities of China and Australia: Population vulnerability and attributable burden. Environ Res 166:610–619

    Article  CAS  Google Scholar 

  • Cheng J, Xu Z, Bambrick H, Prescott V, Wang N, Zhang Y, Su H, Tong S, Hu W (2019) Cardiorespiratory effects of heatwaves: A systematic review and meta-analysis of global epidemiological evidence. Environ Res 177:108610

    Article  CAS  Google Scholar 

  • Cheng J, Bambrick H, Yakob L, Devine G, Frentiu FD, Toan DTT, Thai PQ, Xu Z, Hu W (2020) Heatwaves and dengue outbreaks in Hanoi, Vietnam: New evidence on early warning. PLoS Negl Trop Dis 14(1):e0007997

    Article  Google Scholar 

  • Davis RE, McGregor GR, Enfield KB (2016) Humidity: A review and primer on atmospheric moisture and human health. Environ Res 144(Pt A):106–116

    Article  CAS  Google Scholar 

  • Gasparrini A, Guo Y, Hashizume M, Lavigne E, Zanobetti A, Schwartz J, Tobias A, Tong S, Rocklov J, Forsberg B, Leone M, De Sario M, Bell ML, Guo YL, Wu CF, Kan H, Yi SM, de Sousa Zanotti Stagliorio Coelho M, Saldiva PH, Honda Y, Kim H, Armstrong B (2015) Mortality risk attributable to high and low ambient temperature: a multicountry observational study. Lancet 386(9991):369–375

    Article  Google Scholar 

  • Guo C, Zhou Z, Wen Z, Liu Y, Zeng C, Xiao D, Ou M, Han Y, Huang S, Liu D, Ye X, Zou X, Wu J, Wang H, Zeng EY, Jing C, Yang G (2017) Global Epidemiology of Dengue Outbreaks in 1990-2015: A Systematic Review and Meta-Analysis. Front Cell Infect Microbiol 7:317

    Article  Google Scholar 

  • Guo P, Zhang Q, Chen Y, Xiao J, He J, Zhang Y, Wang L, Liu T, Ma W (2019) An ensemble forecast model of dengue in Guangzhou, China using climate and social media surveillance data. Sci Total Environ 647:752–762

    Article  CAS  Google Scholar 

  • IPCC (Intergovernmental Panel on Climate Change). Climate Change 2014: Synthesis Report. https://archive.ipcc.ch/pdf/assessment-report/ar5/syr/AR5_SYR_FINAL_All_Topics.pdf. Accessed 18 Jan 2020

  • Jia P, Liang L, Tan X, Chen J, Chen X (2019) Potential effects of heat waves on the population dynamics of the dengue mosquito Aedes albopictus. PLoS Negl Trop Dis 13(7):e0007528

    Article  Google Scholar 

  • Kucharski AJ, Kama M, Watson CH, Aubry M, Funk S, Henderson AD, Brady OJ, Vanhomwegen J, Manuguerra JC, Lau CL, Edmunds WJ, Aaskov J, Nilles EJ, Cao-Lormeau VM, Hue S, Hibberd ML (2018) Using paired serology and surveillance data to quantify dengue transmission and control during a large outbreak in Fiji. Elife 7:e34848

    Article  Google Scholar 

  • Legros M, Lloyd AL, Huang Y, Gould F (2009) Density-dependent intraspecific competition in the larval stage of Aedes aegypti (Diptera: Culicidae): revisiting the current paradigm. J Med Entomol 46(3):409–419

    Article  Google Scholar 

  • Li C, Lu Y, Liu J, Wu X (2018) Climate change and dengue fever transmission in China: Evidences and challenges. Sci Total Environ 622-623:493–501

    Article  CAS  Google Scholar 

  • Li R, Xu L, Bjornstad ON, Liu K, Song T, Chen A, Xu B, Liu Q, Stenseth NC (2019) Climate-driven variation in mosquito density predicts the spatiotemporal dynamics of dengue. Proc Natl Acad Sci U S A 116(9):3624–3629

    Article  CAS  Google Scholar 

  • Lowe R, Gasparrini A, Van Meerbeeck CJ, Lippi CA, Mahon R, Trotman AR, Rollock L, Hinds AQJ, Ryan SJ, Stewart-Ibarra AM (2018) Nonlinear and delayed impacts of climate on dengue risk in Barbados: A modelling study. PLoS Med 15(7):e1002613

    Article  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305(5686):994–997

    Article  CAS  Google Scholar 

  • Mordecai EA, Cohen JM, Evans MV, Gudapati P, Johnson LR, Lippi CA, Miazgowicz K, Murdock CC, Rohr JR, Ryan SJ, Savage V, Shocket MS, Stewart Ibarra A, Thomas MB, Weikel DP (2017) Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PLoS Negl Trop Dis 11(4):e0005568

    Article  Google Scholar 

  • Morin CW, Comrie AC, Ernst K (2013) Climate and dengue transmission: evidence and implications. Environ Health Perspect 121(11-12):1264–1272

    Article  Google Scholar 

  • Oidtman RJ, Lai S, Huang Z, Yang J, Siraj AS, Reiner RC Jr, Tatem AJ, Perkins TA, Yu H (2019) Inter-annual variation in seasonal dengue epidemics driven by multiple interacting factors in Guangzhou, China. Nat Commun 10(1):1148

    Article  CAS  Google Scholar 

  • Paz S (2006) The West Nile Virus outbreak in Israel (2000) from a new perspective: the regional impact of climate change. Int J Environ Health Res 16(1):1–13

    Article  CAS  Google Scholar 

  • Qi L, Gao Y, Yang J, Ding XB, Xiong Y, Su K, Liu T, Li Q, Tang WG, Liu QY (2020) The burden of influenza and pneumonia mortality attributable to absolute humidity among elderly people in Chongqing, China, 2012-2018. Sci Total Environ 716:136682

    Article  CAS  Google Scholar 

  • Sang S, Gu S, Bi P, Yang W, Yang Z, Xu L, Yang J, Liu X, Jiang T, Wu H, Chu C, Liu Q (2015) Predicting unprecedented dengue outbreak using imported cases and climatic factors in Guangzhou, 2014. PLoS Negl Trop Dis 9(5):e0003808

    Article  CAS  Google Scholar 

  • Semenza JC, Menne B (2009) Climate change and infectious diseases in Europe. Lancet Infect Dis 9(6):365–375

    Article  Google Scholar 

  • Sharmin S, Glass K, Viennet E, Harley D (2015) Interaction of Mean Temperature and Daily Fluctuation Influences Dengue Incidence in Dhaka, Bangladesh. PLoS Negl Trop Dis 9(7):e0003901

    Article  CAS  Google Scholar 

  • Shen JC, Luo L, Li L, Jing QL, Ou CQ, Yang ZC, Chen XG (2015) The Impacts of Mosquito Density and Meteorological Factors on Dengue Fever Epidemics in Guangzhou, China, 2006-2014: a Time-series Analysis. Biomed Environ Sci 28(5):321–329

    Google Scholar 

  • Shepard DS, Undurraga EA, Halasa YA, Stanaway JD (2016) The global economic burden of dengue: a systematic analysis. Lancet Infect Dis 16(8):935–941

    Article  Google Scholar 

  • Stahl HC, Butenschoen VM, Tran HT, Gozzer E, Skewes R, Mahendradhata Y, Runge-Ranzinger S, Kroeger A, Farlow A (2013) Cost of dengue outbreaks: literature review and country case studies. BMC Public Health 13:1048

    Article  Google Scholar 

  • Sun Y, Zhang X, Zwiers FW, Song L, Wan H, Hu T, Yin H, Ren G (2014) Rapid increase in the risk of extreme summer heat in Eastern China. Nat Clim Chang 4:1082–1085

    Article  Google Scholar 

  • Tong S, Wang XY, FitzGerald G, McRae D, Neville G, Tippett V, Aitken P, Verrall K (2014) Development of health risk-based metrics for defining a heatwave: a time series study in Brisbane, Australia. BMC Public Health 14:435

    Article  Google Scholar 

  • Tong S, FitzGerald G, Wang XY, Aitken P, Tippett V, Chen D, Wang X, Guo Y (2015) Exploration of the health risk-based definition for heatwave: A multi-city study. Environ Res 142:696–702

    Article  CAS  Google Scholar 

  • Tran BX, Thu Vu G, Hoang Nguyen L, Tuan Le Nguyen A, Thanh Tran T, Thanh Nguyen B, Phuong Thi Thai T, Latkin CA, Ho CSH, Ho RCM (2018) Cost-of-Illness and the Health-Related Quality of Life of Patients in the Dengue Fever Outbreak in Hanoi in 2017. Int J Environ Res Public Health 15(6)

  • Wang WH, Lin CY, Chang K, Urbina AN, Assavalapsakul W, Thitithanyanont A, Lu PL, Chen YH, Wang SF (2019) A clinical and epidemiological survey of the largest dengue outbreak in Southern Taiwan in 2015. Int J Infect Dis 88:88–99

    Article  CAS  Google Scholar 

  • Watts N, Amann M, Arnell N, Ayeb-Karlsson S, Belesova K, Berry H, Bouley T, Boykoff M, Byass P, Cai W, Campbell-Lendrum D, Chambers J, Daly M, Dasandi N, Davies M, Depoux A, Dominguez-Salas P, Drummond P, Ebi KL, Ekins P, Montoya LF, Fischer H, Georgeson L, Grace D, Graham H, Hamilton I, Hartinger S, Hess J, Kelman I, Kiesewetter G, Kjellstrom T, Kniveton D, Lemke B, Liang L, Lott M, Lowe R, Sewe MO, Martinez-Urtaza J, Maslin M, McAllister L, Mikhaylov SJ, Milner J, Moradi-Lakeh M, Morrissey K, Murray K, Nilsson M, Neville T, Oreszczyn T, Owfi F, Pearman O, Pencheon D, Pye S, Rabbaniha M, Robinson E, Rocklov J, Saxer O, Schutte S, Semenza JC, Shumake-Guillemot J, Steinbach R, Tabatabaei M, Tomei J, Trinanes J, Wheeler N, Wilkinson P, Gong P, Montgomery H, Costello A (2018) The 2018 report of the Lancet Countdown on health and climate change: shaping the health of nations for centuries to come. Lancet 392(10163):2479–2514

    Article  Google Scholar 

  • WHO (World Health Organization) (n.d.) Dengue and serve dengue. https://www.who.int/en/news-room/fact-sheets/detail/dengue-and-severe-dengue. Accessed 31 Jan 2020

  • Wu X, Lang L, Ma W, Song T, Kang M, He J, Zhang Y, Lu L, Lin H, Ling L (2018) Non-linear effects of mean temperature and relative humidity on dengue incidence in Guangzhou, China. Sci Total Environ 628-629:766–771

    Article  CAS  Google Scholar 

  • Xiang J, Hansen A, Liu Q, Liu X, Tong MX, Sun Y, Cameron S, Hanson-Easey S, Han GS, Williams C, Weinstein P, Bi P (2017) Association between dengue fever incidence and meteorological factors in Guangzhou, China, 2005-2014. Environ Res 153:17–26

    Article  CAS  Google Scholar 

  • Xu L, Stige LC, Chan KS, Zhou J, Yang J, Sang S, Wang M, Yang Z, Yan Z, Jiang T, Lu L, Yue Y, Liu X, Lin H, Xu J, Liu Q, Stenseth NC (2017) Climate variation drives dengue dynamics. Proc Natl Acad Sci U S A 114(1):113–118

    Article  CAS  Google Scholar 

  • Yakob LAL, Bonsall MB (2008) Aedes aegypti control: the concomitant role of competition, space and transgenic technologies. J Appl Ecol 45(4):1258–1265

    Article  Google Scholar 

  • Yan S, Wei L, Duan Y, Li H, Liao Y, Lv Q, Zhu F, Wang Z, Lu W, Yin P, Cheng J, Jiang H (2019) Short-Term Effects of Meteorological Factors and Air Pollutants on Hand, Foot and Mouth Disease among Children in Shenzhen, China, 2009-2017. Int J Environ Res Public Health 16(19)

  • Zeng W, Lao X, Rutherford S, Xu Y, Xu X, Lin H, Liu T, Luo Y, Xiao J, Hu M, Chu C, Ma W (2014) The effect of heat waves on mortality and effect modifiers in four communities of Guangdong Province, China. Sci Total Environ 482-483:214–221

    Article  CAS  Google Scholar 

  • Zhao H, Zhang FC, Zhu Q, Wang J, Hong WX, Zhao LZ, Deng YQ, Qiu S, Zhang Y, Cai WP, Cao WC, Qin CF (2016) Epidemiological and Virological Characterizations of the 2014 Dengue Outbreak in Guangzhou, China. PLoS One 11(6):e0156548

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank China Centre for Disease Control and Prevention and National Meteorological Information Center for providing data set for this study.

Funding

This study was funded by the National Health and Medical Research Council (NHMRC) of Australia (project grant: APP 1138622).

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Authors and Affiliations

  1. School of Public Health and Social Work, Queensland University of Technology, Brisbane, Queensland, 4059, Australia

    Jian Cheng, Hilary Bambrick, Zhiwei Xu & Wenbiao Hu

  2. Department of Epidemiology and Biostatistics & Anhui Province Key Laboratory of Major Autoimmune Disease, School of Public Health, Anhui Medical University, Anhui, China

    Jian Cheng

  3. Centre for Immunology and Infection Control, School of Biomedical Sciences, Queensland University of Technology, Brisbane, Australia

    Francesca D. Frentiu

  4. Mosquito Control Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, Australia

    Gregor Devine

  5. Department of Disease Control, London School of Hygiene and Tropical Medicine, London, UK

    Laith Yakob

  6. School of Public Health, Faculty of Medicine, University of Queensland, Brisbane, Australia

    Zhiwei Xu

  7. Division of Infectious Disease, Key Laboratory of Surveillance and Early Warning of Infectious Disease, Chinese Center for Disease Control and Prevention, Beijing, China

    Zhongjie Li & Weizhong Yang

  8. School of Population Medicine & Public Health, Chinese Academy of Medical Sciences/Peking Union Medical College, Beijing, China

    Weizhong Yang

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  1. Jian Cheng
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Correspondence to Wenbiao Hu.

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Cheng, J., Bambrick, H., Frentiu, F.D. et al. Extreme weather events and dengue outbreaks in Guangzhou, China: a time-series quasi-binomial distributed lag non-linear model. Int J Biometeorol 65, 1033–1042 (2021). https://doi.org/10.1007/s00484-021-02085-1

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