Skip to main content
Top
Published in: Malaria Journal 1/2017

Open Access 01-12-2017 | Research

Describing interaction effect between lagged rainfalls on malaria: an epidemiological study in south–west China

Authors: Yunyun Wu, Zhijiao Qiao, Nan Wang, Hongjie Yu, Zijian Feng, Xiaosong Li, Xing Zhao

Published in: Malaria Journal | Issue 1/2017

Login to get access

Abstract

Background

When discussing the relationship between meteorological factors and malaria, previous studies mainly focus on the interaction between different climatic factors, while the possible interaction within one particular climatic predictor at different lag periods has been largely neglected. In this study, this issue was investigated by exploring the interaction of lagged rainfalls and its impact on malaria epidemics, which is a typical example of those meteorological variables.

Methods

The weekly data of malaria cases and three climatic variables of 30 counties in southwest China from 2004 to 2009 were analysed with the varying coefficient-distributed lag non-linear model. The correlation patterns of the 6th, 9th and 12th week lags would vary over different rainfall levels at the 4th-week lag.

Results

The non-linear patterns for rainfall at different rainfall levels are distinct from each other. In the low rainfall level at the 4th week lag, the increasing rainfall may promote the transmission of malaria. However, for the high rainfall level at the 4th week lag, evidence shows that the excessive rainfall decreases the risk of malaria.

Conclusion

This study reports for the first time that the interaction effect between lagged rainfalls on malaria exists, and highlights the importance of integrating the interaction between lagged predictors in relevant studies, which could help to better understand and predict malaria transmission.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO. World malaria report 2011. Geneva: World Health Organization; 2015. WHO. World malaria report 2011. Geneva: World Health Organization; 2015.
2.
go back to reference Zhou G, Minakawa N, Githeko AK, Yan G. Association between climate variability and malaria epidemics in the East African highlands. Proc Natl Acad Sci USA. 2004;101:2375–80.CrossRefPubMedPubMedCentral Zhou G, Minakawa N, Githeko AK, Yan G. Association between climate variability and malaria epidemics in the East African highlands. Proc Natl Acad Sci USA. 2004;101:2375–80.CrossRefPubMedPubMedCentral
3.
go back to reference Xiao D, Long Y, Wang S, Fang L, Xu D, Wang G, et al. Spatiotemporal distribution of malaria and the association between its epidemic and climate factors in Hainan, China. Malar J. 2010;9:185.CrossRefPubMedPubMedCentral Xiao D, Long Y, Wang S, Fang L, Xu D, Wang G, et al. Spatiotemporal distribution of malaria and the association between its epidemic and climate factors in Hainan, China. Malar J. 2010;9:185.CrossRefPubMedPubMedCentral
4.
go back to reference Parham PE, Michael E. Modeling the effects of weather and climate change on malaria transmission. Environ Health Perspect. 2010;118:620–6.CrossRefPubMed Parham PE, Michael E. Modeling the effects of weather and climate change on malaria transmission. Environ Health Perspect. 2010;118:620–6.CrossRefPubMed
5.
go back to reference Mordecai EA, Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T, de Moor E, et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett. 2013;16:22–30.CrossRefPubMed Mordecai EA, Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T, de Moor E, et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett. 2013;16:22–30.CrossRefPubMed
6.
go back to reference Teklehaimanot HD, Schwartz J, Teklehaimanot A, Lipsitch M. Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia II. Weather-based prediction systems perform comparably to early detection systems in identifying times for interventions. Malar J. 2004;3:44.CrossRefPubMedPubMedCentral Teklehaimanot HD, Schwartz J, Teklehaimanot A, Lipsitch M. Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia II. Weather-based prediction systems perform comparably to early detection systems in identifying times for interventions. Malar J. 2004;3:44.CrossRefPubMedPubMedCentral
7.
go back to reference Schwartz J. The distributed lag between air pollution and daily deaths. Epidemiology. 2000;11:320–6.CrossRefPubMed Schwartz J. The distributed lag between air pollution and daily deaths. Epidemiology. 2000;11:320–6.CrossRefPubMed
8.
go back to reference Kilian AH, Langi P, Talisuna A, Kabagambe G. Rainfall pattern, El Nino and malaria in Uganda. Trans R Soc Trop Med Hyg. 1999;93:22–3.CrossRefPubMed Kilian AH, Langi P, Talisuna A, Kabagambe G. Rainfall pattern, El Nino and malaria in Uganda. Trans R Soc Trop Med Hyg. 1999;93:22–3.CrossRefPubMed
9.
go back to reference Abeku TA, De Vlas SJ, Borsboom GJ, Tadege A, Gebreyesus Y, Gebreyohannes H, et al. Effects of meteorological factors on epidemic malaria in Ethiopia: a statistical modelling approach based on theoretical reasoning. Parasitology. 2004;128:585–93.CrossRefPubMed Abeku TA, De Vlas SJ, Borsboom GJ, Tadege A, Gebreyesus Y, Gebreyohannes H, et al. Effects of meteorological factors on epidemic malaria in Ethiopia: a statistical modelling approach based on theoretical reasoning. Parasitology. 2004;128:585–93.CrossRefPubMed
10.
go back to reference Ceccato P, Ghebremeskel T, Jaiteh M, Graves PM, Levy M, Ghebreselassie S, et al. Malaria stratification, climate, and epidemic early warning in Eritrea. Am J Trop Med Hyg. 2007;77:61–8.PubMed Ceccato P, Ghebremeskel T, Jaiteh M, Graves PM, Levy M, Ghebreselassie S, et al. Malaria stratification, climate, and epidemic early warning in Eritrea. Am J Trop Med Hyg. 2007;77:61–8.PubMed
11.
go back to reference Midekisa A, Senay G, Henebry GM, Semuniguse P, Wimberly MC. Remote sensing-based time series models for malaria early warning in the highlands of Ethiopia. Malar J. 2012;11:165.CrossRefPubMedPubMedCentral Midekisa A, Senay G, Henebry GM, Semuniguse P, Wimberly MC. Remote sensing-based time series models for malaria early warning in the highlands of Ethiopia. Malar J. 2012;11:165.CrossRefPubMedPubMedCentral
12.
go back to reference Thomson MC, Doblas-Reyes FJ, Mason SJ, Hagedorn R, Connor SJ, Phindela T, et al. Malaria early warnings based on seasonal climate forecasts from multi-model ensembles. Nature. 2006;439:576–9.CrossRefPubMed Thomson MC, Doblas-Reyes FJ, Mason SJ, Hagedorn R, Connor SJ, Phindela T, et al. Malaria early warnings based on seasonal climate forecasts from multi-model ensembles. Nature. 2006;439:576–9.CrossRefPubMed
13.
14.
go back to reference Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M. Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA. 2006;103:5829–34.CrossRefPubMedPubMedCentral Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M. Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA. 2006;103:5829–34.CrossRefPubMedPubMedCentral
16.
go back to reference Zhou SS, Huang F, Wang JJ, Zhang SS, Su YP, Tang LH. Geographical, meteorological and vectorial factors related to malaria re-emergence in Huang–Huai River of central China. Malar J. 2010;9:337.CrossRefPubMedPubMedCentral Zhou SS, Huang F, Wang JJ, Zhang SS, Su YP, Tang LH. Geographical, meteorological and vectorial factors related to malaria re-emergence in Huang–Huai River of central China. Malar J. 2010;9:337.CrossRefPubMedPubMedCentral
17.
go back to reference Gasparrini A. Modeling exposure-lag-response associations with distributed lag non-linear models. Stat Med. 2014;33:881–99.CrossRefPubMed Gasparrini A. Modeling exposure-lag-response associations with distributed lag non-linear models. Stat Med. 2014;33:881–99.CrossRefPubMed
18.
go back to reference Heaton MJ, Peng RD. Extending distributed lag models to higher degrees. Biostatistics. 2014;15:398–412.CrossRefPubMed Heaton MJ, Peng RD. Extending distributed lag models to higher degrees. Biostatistics. 2014;15:398–412.CrossRefPubMed
19.
go back to reference Hui FM, Xu B, Chen ZW, Cheng X, Liang L, Huang HB, et al. Spatio-temporal distribution of malaria in Yunnan Province, China. Am J Trop Med Hyg. 2009;81:503–9.PubMed Hui FM, Xu B, Chen ZW, Cheng X, Liang L, Huang HB, et al. Spatio-temporal distribution of malaria in Yunnan Province, China. Am J Trop Med Hyg. 2009;81:503–9.PubMed
20.
go back to reference Ma ZF, Liu J, Yang SQ. Climate change in southwest China during 1961–2010: impacts and adaptation. Adv Clim Change Res. 2013;4:223–9.CrossRef Ma ZF, Liu J, Yang SQ. Climate change in southwest China during 1961–2010: impacts and adaptation. Adv Clim Change Res. 2013;4:223–9.CrossRef
21.
go back to reference Zhao X, Chen F, Feng Z, Li X, Zhou XH. 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. 2014;13:57.CrossRefPubMedPubMedCentral Zhao X, Chen F, Feng Z, Li X, Zhou XH. 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. 2014;13:57.CrossRefPubMedPubMedCentral
23.
go back to reference Wang L, Wang Y, Jin S, Wu Z, Chin DP, Koplan JP, et al. Emergence and control of infectious diseases in China. Lancet. 2008;372:1598–605.CrossRefPubMed Wang L, Wang Y, Jin S, Wu Z, Chin DP, Koplan JP, et al. Emergence and control of infectious diseases in China. Lancet. 2008;372:1598–605.CrossRefPubMed
24.
go back to reference Teklehaimanot HD, Lipsitch M, Teklehaimanot A, Schwartz J. Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia. I. Patterns of lagged weather effects reflect biological mechanisms. Malar J. 2004;3:41.CrossRefPubMedPubMedCentral Teklehaimanot HD, Lipsitch M, Teklehaimanot A, Schwartz J. Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia. I. Patterns of lagged weather effects reflect biological mechanisms. Malar J. 2004;3:41.CrossRefPubMedPubMedCentral
25.
go back to reference Craig MH, Kleinschmidt I, Le Sueur D, Sharp BL. Exploring 30 years of malaria case data in KwaZulu-Natal, South Africa: part II. The impact of non-climatic factors. Trop Med Int Health. 2004;9:1258–66.CrossRefPubMed Craig MH, Kleinschmidt I, Le Sueur D, Sharp BL. Exploring 30 years of malaria case data in KwaZulu-Natal, South Africa: part II. The impact of non-climatic factors. Trop Med Int Health. 2004;9:1258–66.CrossRefPubMed
26.
go back to reference Dell AI, Pawar S, Savage VM. Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci USA. 2011;108:10591–6.CrossRefPubMedPubMedCentral Dell AI, Pawar S, Savage VM. Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci USA. 2011;108:10591–6.CrossRefPubMedPubMedCentral
27.
go back to reference Hastie T, Tibshirani R. Varying-coefficient models. J R Stat Soc B. 1996;55:757–96. Hastie T, Tibshirani R. Varying-coefficient models. J R Stat Soc B. 1996;55:757–96.
28.
29.
go back to reference Bates D, Maechler M, Bolker B, Walker S. Lme4: linear mixed-effects models using Eigen and S4. R Package Version. 2013;1:1–5. Bates D, Maechler M, Bolker B, Walker S. Lme4: linear mixed-effects models using Eigen and S4. R Package Version. 2013;1:1–5.
30.
go back to reference Zhao X, Chen F, Feng Z, Li X, Zhou XH. 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. 2014;13:192.CrossRefPubMedPubMedCentral Zhao X, Chen F, Feng Z, Li X, Zhou XH. 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. 2014;13:192.CrossRefPubMedPubMedCentral
31.
go back to reference Erhart A, Ngo DT, Phan VK, Ta TT, Van Overmeir C, Speybroeck N, et al. Epidemiology of forest malaria in central Vietnam: a large scale cross-sectional survey. Malar J. 2005;4:58.CrossRefPubMedPubMedCentral Erhart A, Ngo DT, Phan VK, Ta TT, Van Overmeir C, Speybroeck N, et al. Epidemiology of forest malaria in central Vietnam: a large scale cross-sectional survey. Malar J. 2005;4:58.CrossRefPubMedPubMedCentral
32.
go back to reference Luo Y, Zhang YH, Pei FQ, Liu T, Zeng WL, Xiao JP, et al. Time-series analysis on the malaria morbidity affected by meteorological factors in Guangdong province. Chin J Prev Med. 2012;46:892–7. Luo Y, Zhang YH, Pei FQ, Liu T, Zeng WL, Xiao JP, et al. Time-series analysis on the malaria morbidity affected by meteorological factors in Guangdong province. Chin J Prev Med. 2012;46:892–7.
33.
go back to reference Tian L, Bi Y, Ho SC, Liu W, Liang S, Goggins WB, et al. One-year delayed effect of fog on malaria transmission: a time-series analysis in the rain forest area of Mengla County, south–west China. Malar J. 2008;7:110.CrossRefPubMedPubMedCentral Tian L, Bi Y, Ho SC, Liu W, Liang S, Goggins WB, et al. One-year delayed effect of fog on malaria transmission: a time-series analysis in the rain forest area of Mengla County, south–west China. Malar J. 2008;7:110.CrossRefPubMedPubMedCentral
34.
go back to reference le Sueur D, Sharp BL. Temperature-dependent variation in Anopheles merus larval head capsule width and adult wing length: implications for anopheline taxonomy. Med Vet Entomol. 1991;5:55–62.CrossRefPubMed le Sueur D, Sharp BL. Temperature-dependent variation in Anopheles merus larval head capsule width and adult wing length: implications for anopheline taxonomy. Med Vet Entomol. 1991;5:55–62.CrossRefPubMed
35.
go back to reference Huang F, Zhou S, Zhang S, Zhang H, Li W. Meteorological factors-based spatio-temporal mapping and predicting malaria in central China. Am J Trop Med Hyg. 2011;85:560–7.CrossRefPubMedPubMedCentral Huang F, Zhou S, Zhang S, Zhang H, Li W. Meteorological factors-based spatio-temporal mapping and predicting malaria in central China. Am J Trop Med Hyg. 2011;85:560–7.CrossRefPubMedPubMedCentral
36.
go back to reference Huang F, Zhou S, Zhang S, Wang H, Tang L. Temporal correlation analysis between malaria and meteorological factors in Motuo County, Tibet. Malar J. 2011;10:54.CrossRefPubMedPubMedCentral Huang F, Zhou S, Zhang S, Wang H, Tang L. Temporal correlation analysis between malaria and meteorological factors in Motuo County, Tibet. Malar J. 2011;10:54.CrossRefPubMedPubMedCentral
37.
go back to reference Zhang Y, Bi P, Hiller JE. Meteorological variables and malaria in a Chinese temperate city: a twenty-year time-series data analysis. Environ Int. 2010;36:439–45.CrossRefPubMed Zhang Y, Bi P, Hiller JE. Meteorological variables and malaria in a Chinese temperate city: a twenty-year time-series data analysis. Environ Int. 2010;36:439–45.CrossRefPubMed
38.
go back to reference Gelman A. Multilevel (Hierarchical) modeling: what it can and cannot do. Technometrics. 2006;48:432–5.CrossRef Gelman A. Multilevel (Hierarchical) modeling: what it can and cannot do. Technometrics. 2006;48:432–5.CrossRef
39.
go back to reference Bi Y, Hu W, Yang H, Zhou XN, Yu W, Guo Y, et al. Spatial patterns of malaria reported deaths in Yunnan Province, China. Am J Trop Med Hyg. 2013;88:526–35.CrossRefPubMedPubMedCentral Bi Y, Hu W, Yang H, Zhou XN, Yu W, Guo Y, et al. Spatial patterns of malaria reported deaths in Yunnan Province, China. Am J Trop Med Hyg. 2013;88:526–35.CrossRefPubMedPubMedCentral
40.
go back to reference Kigozi R, Zinszer K, Mpimbaza A, Sserwanga A, Kigozi SP, Kamya M. Assessing temporal associations between environmental factors and malaria morbidity at varying transmission settings in Uganda. Malar J. 2016;15:511.CrossRefPubMedPubMedCentral Kigozi R, Zinszer K, Mpimbaza A, Sserwanga A, Kigozi SP, Kamya M. Assessing temporal associations between environmental factors and malaria morbidity at varying transmission settings in Uganda. Malar J. 2016;15:511.CrossRefPubMedPubMedCentral
Metadata
Title
Describing interaction effect between lagged rainfalls on malaria: an epidemiological study in south–west China
Authors
Yunyun Wu
Zhijiao Qiao
Nan Wang
Hongjie Yu
Zijian Feng
Xiaosong Li
Xing Zhao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2017
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-017-1706-2

Other articles of this Issue 1/2017

Malaria Journal 1/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.