Abstract
Malaria is a climate-sensitive infectious disease. Many ecological studies have investigated the independent impacts of ambient temperature on malaria. However, the optimal temperature measures of malaria and its interaction with other meteorological factors on malaria transmission are less understood. This study aims to investigate the effect of ambient temperature and its interactions with relative humidity and rainfall on malaria in Suzhou, a temperate climate city in Anhui Province, China. Weekly malaria and meteorological data from 2005 to 2012 were obtained for Suzhou. A distributed lag nonlinear model was conducted to quantify the effect of different temperature measures on malaria. The best measure was defined as that with the minimum quasi-Akaike information criterion. GeoDetector and Poisson regression models were employed to quantify the interactions of temperature, relative humidity, and rainfall on malaria transmission. A total of 13,382 malaria cases were notified in Suzhou from 2005 to 2012. Each 5 °C rise in average temperature over 10 °C resulted in a 22% (95% CI: 17%, 28%) increase in malaria cases at lag of 4 weeks. In terms of cumulative effects from lag 1 to 8 weeks, each 5 °C increase over 10 °C caused a 175% growth in malaria cases (95% CI: 139%, 216%). Average temperature achieved the best performance in terms of model fitting, followed by minimum temperature, most frequent temperature, and maximum temperature. Temperature had an interactive effect on malaria with relative humidity and rainfall. High temperature together with high relative humidity and high rainfall could accelerate the transmission of malaria. Meteorological factors may affect malaria transmission interactively. The research findings could be helpful in the development of weather-based malaria early warning system, especially in the context of climate change for the prevention of possible malaria resurgence.
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References
Andersson T, Alfredsson L, Källberg H, Zdravkovic S, Ahlbom A (2005) Calculating measures of biological interaction. Eur J Epidemiol 20:575–579
Bai L, Morton LC, Liu Q (2013) Climate change and mosquito-borne diseases in China: a review. Glob Health 9:10
Barnett AG, Tong S, Clements ACA (2010) What measure of temperature is the best predictor of mortality? Environ Res 110:604–611
Breitner S, Wolf K, Devlin RB, Diaz-Sanchez D, Peters A, Schneider A (2014) Short-term effects of air temperature on mortality and effect modification by air pollution in three cities of Bavaria, Germany: a time-series analysis. Sci Total Environ 485-486:49–61
Cao F, Ge Y, Wang JF (2013) Optimal discretization for geographical detectors-based risk assessment. GISci Remote Sens 50:78–92
Chua TH (2012) Modelling the effect of temperature change on the extrinsic incubation period and reproductive number of Plasmodium falciparum in Malaysia. Trop Biomed 29:121–128
DCFPH (Data Center for Public Health in China) (2019) National Notifiable Infectious Disease Database. http://www.phsciencedata.cn/Share/. Accessed 20 March 2019 (in Chinese)
Ding DJ, Zhang XH, Zhao YJ (1991) Influence of temperature on the generational distribution of An. sinensis and its effective seasons for malaria transmission in China. Chin J Eco 10:54–59 (in Chinese)
Du Z, Lawrence WR, Zhang WJ, Zhang DM, Yu SC, Hao YT (2019) Interactions between climate factors and air pollution on daily HFMD cases: a time series study in Guangdong, China. Sci Total Environ 656:1358–1364
Fan CN, Liu FF, Zhao X, Ma Y, Yang F, Chang ZR, Xiao X (2020) An alternative comprehensive index to quantify the interactive effect of temperature and relative humidity on hand, foot and mouth disease: a two-stage time series study including 143 cities in mainland China. Sci Total Environ 740:140106
Feachem RGA, Chen I, Akbari O, Bertozzi-Villa A, Bhatt S, Binka F, Boni MF, Buckee C, Dieleman J, Dondorp A, Eapen A, Sekhri Feachem N, Filler S, Gething P, Gosling R, Haakenstad A, Harvard K, Hatefi A, Jamison D, Jones KE, Karema C, Kamwi RN, Lal A, Larson E, Lees M, Lobo NF, Micah AE, Moonen B, Newby G, Ning X, Pate M, Quiñones M, Roh M, Rolfe B, Shanks D, Singh B, Staley K, Tulloch J, Wegbreit J, Woo HJ, Mpanju-Shumbusho W (2019) Malaria eradication within a generation: ambitious, achievable, and necessary. Lancet 394:1056–1112
Feng J, Xia ZG (2014) Analysis of trends in cases of malaria reported from 2004 to July 2013 in the People’s Republic of China. J Pathogen Biol 9:442–446 (in Chinese)
Gao HW, Wang LP, Liang S, Liu YX, Tong SL, Wang JJ, Li YP, Wang XF, Yang H, Ma JQ, Fang LQ, Cao WC (2012) Change in rainfall drives malaria re-emergence in Anhui Province, China. PLoS One 7:e43686
Gasparrini A (2010) Distributed lag non-linear models. Stat Med 29:2224–2234
Gasparrini A (2011) Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 43:1–20
Gunda R, Chimbari MJ, Shamu S, Sartorius B, Mukaratirwa S (2017) Malaria incidence trends and their association with climatic variables in rural Gwanda, Zimbabwe, 2005-2015. Malar J 16:393
Guo C, Yang L, Ou CQ, Li L, Zhuang Y, Yang J, Zhou YX, Qian J, Chen PY, Liu QY (2015) Malaria incidence from 2005-2013 and its associations with meteorological factors in Guangdong, China. Malar J 14:116
Hajat S, Armstrong B, Baccini M, Biggeri A, Bisanti L, Russo A, Paldy A, Menne B, Kosatsky T (2006) Impact of high temperatures on mortality: is there an added heat wave effect? Epidemiology 17:632–638
Hundessa S, Williams G, Li S, Guo J, Zhang W, Guo Y (2017) The weekly associations between climatic factors and Plasmodium vivax and Plasmodium falciparum malaria in China, 2005-2014. Trans R Soc Trop Med Hyg 111:211–219
Josling GA, Llinas M (2015) Sexual development in Plasmodium parasites: knowing when it’s time to commit. Nat Rev Microbiol 13:573–587
Kim YM, Park JW, Cheong HK (2012) Estimated effect of climatic variables on the transmission of Plasmodium vivax malaria in the Republic of Korea. Environ Health Perspect 120:1314–1319
Kristan M, Abeku TA, Beard J, Okia M, Rapuoda B, Sang J, Cox J (2008) Variations in entomological indices in relation to weather patterns and malaria incidence in East African highlands: implications for epidemic prevention and control. Malar J 7:231
le Sueur D, Sharp BL (1991) Temperature-dependent variation in Anopheles merus larval head capsule width and adult wing length: implications for anopheline taxonomy. Med Vet Entomol 5:55–62
Li T, Yang Z, Wang M (2013) Temperature, relative humidity and sunshine may be the effective predictors for occurrence of malaria in Guangzhou, southern China, 2006-2012. Parasit Vectors 6:155
Liu Z, Zhang F, Zhang Y, Li J, Liu X, Ding G, Zhang C, Liu Q, Jiang B (2018) Association between floods and infectious diarrhea and their effect modifiers in Hunan province, China: a two-stage model. Sci Total Environ 626:630–637
Luo Y, Zhang YH, Pei FQ, Liu T, Zeng WL, Xiao JP et al (2012) Time-series analysis on the malaria morbidity affected by meteorological factors in Guangdong province. Chin J Prev Med 46:892–897 (in Chinese)
Lyons CL, Coetzee M, Terblanche JS, Chown SL (2014) Desiccation tolerance as a function of age, sex, humidity and temperature in adults of the African malaria vectors Anopheles arabiensis and Anopheles funestus. J Exp Biol 217:3823–3833
Mordecai EA, Caldwell JM, Grossman MK, Lippi CA, Johnson LR, Neira M, Rohr JR, Ryan SJ, Savage V, Shocket MS, Sippy R, Stewart Ibarra AM, Thomas MB, Villena O (2019) Thermal biology of mosquito-borne disease. Ecol Lett 22:1690–1708
Mukhtar AYA, Munyakazi JB, Ouifki R (2019) Assessing the role of climate factors on malaria transmission dynamics in South Sudan. Math Biosci 310:13–23
Nath DC, Mwchahary DD (2012) Association between climatic variables and malaria incidence: a study in Kokrajhar district of Assam, India. Global J Health Sci 5:90–106
Nathaniel S, Jane FG (2001) On judging the significance of differences by examining the overlap between confidence intervals. Am Stat 55:182–186
NHC (National Health Commission of the People’s Republic of China) (2010) Notice on the issuance of China’s Action plan to malaria elimination (2010-2020). http://www.nhc.gov.cn/zwgk/wtwj/201304/15a4cc7a40b0452191fe409590ca99d8.shtml. Accessed 20 March 2019 (in Chinese)
Pan RB, Wang X, Yi WZ, Wei QN, Su H (2020) Interactions between climate factors and air quality index for improved childhood asthma self-management. Sci Total Environ 723:137804
Peng RD, Dominici F, Louis TA (2006) Model choice in time series studies of air pollution and mortality. J R Stat Soc Ser A 169:179–203
Ren Z, Wang D, Hwang J, Bennett A, Sturrock HJ, Ma A et al (2015) Spatial-temporal variation and primary ecological drivers of Anopheles sinensis human biting rates in malaria epidemic-prone regions of China. PLoS One 10:e0116932
Roberts S (2004) Interactions between particulate air pollution and temperature in air pollution mortality time series studies. Environ Res 96:328–337
Simon N (2006) Generalized additive models: an introduction with R. Chapman & Hall/CRC, Boca Raton, pp 360–361
Song Y, Ge Y, Wang J, Ren Z, Liao Y, Peng J (2016) Spatial distribution estimation of malaria in northern China and its scenarios in 2020, 2030, 2040 and 2050. Malar J 15:345
Song YZ, Wang JF, Ge Y, Xu CD (2020) An optimal parameters-based geographical detector model enhances geographic characteristics of explanatory variables for spatial heterogeneity analysis: cases with different types of spatial data. GISci Remote Sens 57:593–610
Teklehaimanot HD, Lipsitch M, Teklehaimanot A, Schwartz J (2004) Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia I. Patterns of lagged weather effects reflect biological mechanisms. Malar J 3:41
Wang JF, Hu Y (2012) Environmental health risk detection with GeogDetector. Environ Model Softw 33:114–115
Wang JF, Li XH, Christakos G, Liao YL, Zhang T, Gu X, Zheng XY (2010) Geographical detectors-based health risk assessment and its application in the neural tube defects study of the Heshun region, China. Int J Geogr Inf Sci 24:107–127
Wang JF, Zhang TL, Fu BJ (2016) A measure of spatial stratified heterogeneity. Ecol Indic 67:250–256
Wardrop NA, Barnett AG, Atkinson JA, Clements AC (2013) Plasmodium vivax malaria incidence over time and its association with temperature and rainfall in four counties of Yunnan Province, China. Malar J 12:452
WHO (World Health Organization) (2015) World Malaria Report 2015. https://www.who.int/malaria/publications/world-malaria-report-2015/en/. Accessed 18 June 2019
WHO (World Health Organization) (2018) World Malaria Report 2018. https://www.who.int/malaria/publications/world-malaria-report-2018/en/. Accessed 18 June 2019
WHO (World Health Organization) (2019a) World Malaria Report 2019. https://www.who.int/malaria/publications/world-malaria-report-2019/en/. Accessed 3 October 2020
WHO (World Health Organization) (2019b) From 30 million to zero: China creates a malaria-free future. https://www.who.int/malaria/news/2019/china-from-30-million-to-zero/en/. Accessed 18 June 2019
Wu Y, Qiao Z, Wang N, Yu H, Feng Z, Li X, Zhao X (2017) Describing interaction effect between lagged rainfalls on malaria: an epidemiological study in south-west China. Malar J 16:53
Xiang J, Hansen A, Liu Q, Tong MX, Liu X, Sun Y et al (2018) Association between malaria incidence and meteorological factors: a multi-location study in China, 2005-2012. Epidemiol Infect 146:89–99
Yang GJ, Gao Q, Zhou SS, Malone JB, McCarroll JC, Tanner M et al (2010) Mapping and predicting malaria transmission in the People’s Republic of China, using integrated biology-driven and statistical models. Geospat Health 5:11–22
Yin Q, Wang JF, Ren ZP, Li J, Guo YM (2019) Mapping the increased minimum mortality temperatures in the context of global climate change. Nat Commun 10:4640
Zacarias OP, Andersson M (2011) Spatial and temporal patterns of malaria incidence in Mozambique. Malar J 10:189
Zhao X, Chen F, Feng Z, Li X, Zhou XH (2014a) The temporal lagged association between meteorological factors and malaria in 30 counties in south-west China: a multilevel distributed lag non-linear analysis. Malar J 13:57
Zhao X, Chen F, Feng Z, Li X, Zhou XH (2014b) Characterizing the effect of temperature fluctuation on the incidence of malaria: an epidemiological study in south-west China using the varying coefficient distributed lag non-linear model. Malar J 13:192
Zhou G, Minakawa N, Githeko AK, Yan G (2004) Association between climate variability and malaria epidemics in the East African highlands. Proc Natl Acad Sci U S A 101:2375–2380
Acknowledgments
We are thankful for Chinese Center for Disease Control and Prevention and National Meteorological Information Center of China for providing the data for the study.
Funding
This work 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)
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All authors contributed to the study conception and design. Data analysis and writing of the first draft of the manuscript were performed by LZD and WSZ. LQY, SSY, XJJ, and TM provided assistance for data acquisition, data analysis, and statistical analysis. BP, JBF, and ZY participated in the coordination of the study and reviewed the manuscript. GQ and ZYW carried out literature searching and manuscript editing. All authors commented on previous versions of the manuscript and approved the final manuscript.
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Liu, Z., Wang, S., Zhang, Y. et al. Effect of temperature and its interactions with relative humidity and rainfall on malaria in a temperate city Suzhou, China. Environ Sci Pollut Res 28, 16830–16842 (2021). https://doi.org/10.1007/s11356-020-12138-4
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DOI: https://doi.org/10.1007/s11356-020-12138-4