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Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Different responses of weather factors on hand, foot and mouth disease in three different climate areas of Gansu, China

Authors: Faxiang Gou, Xinfeng Liu, Jian He, Dongpeng Liu, Yao Cheng, Haixia Liu, Xiaoting Yang, Kongfu Wei, Yunhe Zheng, Xiaojuan Jiang, Lei Meng, Wenbiao Hu

Published in: BMC Infectious Diseases | Issue 1/2018

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Abstract

Background

To determine the linear and non-linear interacting relationships between weather factors and hand, foot and mouth disease (HFMD) in children in Gansu, China, and gain further traction as an early warning signal based on weather variability for HFMD transmission.

Method

Weekly HFMD cases aged less than 15 and meteorological information from 2010 to 2014 in Jiuquan, Lanzhou and Tianshu, Gansu, China were collected. Generalized linear regression models (GLM) with Poisson link and classification and regression trees (CART) were employed to determine the combined and interactive relationship of weather factors and HFMD in both linear and non-linear ways.

Results

GLM suggested an increase in weekly HFMD of 5.9% [95% confidence interval (CI): 5.4%, 6.5%] in Tianshui, 2.8% [2.5%, 3.1%] in Lanzhou and 1.8% [1.4%, 2.2%] in Jiuquan in association with a 1 °C increase in average temperature, respectively. And 1% increase of relative humidity could increase weekly HFMD of 2.47% [2.23%, 2.71%] in Lanzhou and 1.11% [0.72%, 1.51%] in Tianshui. CART revealed that average temperature and relative humidity were the first two important determinants, and their threshold values for average temperature deceased from 20 °C of Jiuquan to 16 °C in Tianshui; and for relative humidity, threshold values increased from 38% of Jiuquan to 65% of Tianshui.

Conclusion

Average temperature was the primary weather factor in three areas, more sensitive in southeast Tianshui, compared with northwest Jiuquan; Relative humidity’s effect on HFMD showed a non-linear interacting relationship with average temperature.
Literature
1.
go back to reference Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol. 2010;9(11):1097–105.CrossRefPubMed Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T. Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol. 2010;9(11):1097–105.CrossRefPubMed
2.
go back to reference Seiff A. Cambodia unravels cause of mystery illness. Lancet (London, England). 2012;380(9838):206.CrossRef Seiff A. Cambodia unravels cause of mystery illness. Lancet (London, England). 2012;380(9838):206.CrossRef
3.
go back to reference Ma E, Chan KC, Cheng P, Wong C, Chuang SK. The enterovirus 71 epidemic in 2008—public health implications for Hong Kong. Int J Infect Dis. 2010;14(9):775–80.CrossRef Ma E, Chan KC, Cheng P, Wong C, Chuang SK. The enterovirus 71 epidemic in 2008—public health implications for Hong Kong. Int J Infect Dis. 2010;14(9):775–80.CrossRef
4.
go back to reference Tu PV, Thao NT, Perera D, Huu TK, Tien NT, Thuong TC, How OM, Cardosa MJ, Mcminn PC. Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerg Infect Dis. 2007;13(11):1733–41.CrossRefPubMedPubMedCentral Tu PV, Thao NT, Perera D, Huu TK, Tien NT, Thuong TC, How OM, Cardosa MJ, Mcminn PC. Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerg Infect Dis. 2007;13(11):1733–41.CrossRefPubMedPubMedCentral
5.
go back to reference Chan KP, Goh KT, Chong CY, Teo ES, Lau G, Ling AE. Epidemic hand, foot and mouth disease caused by human Enterovirus 71, Singapore. Emerg Infect Dis. 2003;9(1):78–85.CrossRefPubMedPubMedCentral Chan KP, Goh KT, Chong CY, Teo ES, Lau G, Ling AE. Epidemic hand, foot and mouth disease caused by human Enterovirus 71, Singapore. Emerg Infect Dis. 2003;9(1):78–85.CrossRefPubMedPubMedCentral
6.
go back to reference Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shih SR. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N Engl J Med. 1999;341(13):929–35.CrossRefPubMed Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shih SR. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N Engl J Med. 1999;341(13):929–35.CrossRefPubMed
7.
go back to reference Jee YM, Cheon DS, Kim K, Cho JH, Chung YS, Lee J, Lee SH, Park KS, Lee JH, Kim EC. Genetic analysis of the VP1 region of human enterovirus 71 strains isolated in Korea during 2000. Arch Virol. 2003;148(9):1735–46.CrossRefPubMed Jee YM, Cheon DS, Kim K, Cho JH, Chung YS, Lee J, Lee SH, Park KS, Lee JH, Kim EC. Genetic analysis of the VP1 region of human enterovirus 71 strains isolated in Korea during 2000. Arch Virol. 2003;148(9):1735–46.CrossRefPubMed
8.
go back to reference Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, Ji F, Wang XJ, Gao YJ, Chen L. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J Clin Virol. 2009;44(4):262–7.CrossRefPubMed Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, Ji F, Wang XJ, Gao YJ, Chen L. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J Clin Virol. 2009;44(4):262–7.CrossRefPubMed
9.
go back to reference Yan Z, Zhen Z, Yang W, Ren J, Tan X, Yu W, Mao N, Xu S, Zhu S, Cui A. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J. 2010;7(8):94.PubMedPubMedCentral Yan Z, Zhen Z, Yang W, Ren J, Tan X, Yu W, Mao N, Xu S, Zhu S, Cui A. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J. 2010;7(8):94.PubMedPubMedCentral
10.
go back to reference Sun S, Jiang L, Liang Z, Mao Q, Su W, Zhang H, Li X, Jin J, Xu L, Zhao D. Evaluation of monovalent and bivalent vaccines against lethal enterovirus 71 and Coxsackievirus A16 infection in newborn mice. Human Vaccin Immunother. 2014;10(10):2885–95.CrossRef Sun S, Jiang L, Liang Z, Mao Q, Su W, Zhang H, Li X, Jin J, Xu L, Zhao D. Evaluation of monovalent and bivalent vaccines against lethal enterovirus 71 and Coxsackievirus A16 infection in newborn mice. Human Vaccin Immunother. 2014;10(10):2885–95.CrossRef
12.
go back to reference Wu H, Wang H, Wang Q, Xin Q, Lin H. The effect of meteorological factors on adolescent hand, foot, and mouth disease and associated effect modifiers. Glob Health Action. 2014;7:24664.CrossRefPubMed Wu H, Wang H, Wang Q, Xin Q, Lin H. The effect of meteorological factors on adolescent hand, foot, and mouth disease and associated effect modifiers. Glob Health Action. 2014;7:24664.CrossRefPubMed
13.
go back to reference Chen C, Lin H, Li X, Lang L, Xiao X, Ding P, He P, Zhang Y, Wang M, Liu Q. Short-term effects of meteorological factors on children hand, foot and mouth disease in Guangzhou, China. Int J Biometeorol. 2014;58(7):1605–14.CrossRefPubMed Chen C, Lin H, Li X, Lang L, Xiao X, Ding P, He P, Zhang Y, Wang M, Liu Q. Short-term effects of meteorological factors on children hand, foot and mouth disease in Guangzhou, China. Int J Biometeorol. 2014;58(7):1605–14.CrossRefPubMed
14.
go back to reference Zhao D, Wang L, Cheng J, Xu J, Xu Z, Xie M, Yang H, Li K, Wen L, Wang X, et al. Impact of weather factors on hand, foot and mouth disease, and its role in short-term incidence trend forecast in Huainan City, Anhui Province. Int J Biometeorol. 2016;61(3):1-9. Zhao D, Wang L, Cheng J, Xu J, Xu Z, Xie M, Yang H, Li K, Wen L, Wang X, et al. Impact of weather factors on hand, foot and mouth disease, and its role in short-term incidence trend forecast in Huainan City, Anhui Province. Int J Biometeorol. 2016;61(3):1-9.
15.
go back to reference Lee CC, Tang JH, Hwang JS, Shigematsu M, Chan TC. Effect of meteorological and geographical factors on the epidemics of hand, foot, and mouth disease in island-type territory, East Asia. Biomed Res Int. 2015;2015:805039.PubMedPubMedCentral Lee CC, Tang JH, Hwang JS, Shigematsu M, Chan TC. Effect of meteorological and geographical factors on the epidemics of hand, foot, and mouth disease in island-type territory, East Asia. Biomed Res Int. 2015;2015:805039.PubMedPubMedCentral
16.
go back to reference Gardner ES. Forecasting: methods and applications (Second Edition), Makridakis, S., Wheelwright, S. C. and McGee, V. E., New York: Wiley, 1983. Price: $47.85/$20.15 (cloth), $34.15/E14.35 (paper). Pages: 923. J Forecasting. 1984;3(4):457–60.CrossRef Gardner ES. Forecasting: methods and applications (Second Edition), Makridakis, S., Wheelwright, S. C. and McGee, V. E., New York: Wiley, 1983. Price: $47.85/$20.15 (cloth), $34.15/E14.35 (paper). Pages: 923. J Forecasting. 1984;3(4):457–60.CrossRef
17.
go back to reference Bartholomew D, Box GEP, Jenkins GM. Time series analysis: forecasting and control. In: Holden-day series in time series analysis, revised Ed, San Francisco: Holden-day, vol. 1976; 1976. p. 199–201. Bartholomew D, Box GEP, Jenkins GM. Time series analysis: forecasting and control. In: Holden-day series in time series analysis, revised Ed, San Francisco: Holden-day, vol. 1976; 1976. p. 199–201.
18.
go back to reference Huang X, Clements ACA, Williams G, Milinovich G, Hu W. A threshold analysis of dengue transmission in terms of weather variables and imported dengue cases in Australia. Emerg Microbes Infect. 2013;2(12):e87.CrossRefPubMedPubMedCentral Huang X, Clements ACA, Williams G, Milinovich G, Hu W. A threshold analysis of dengue transmission in terms of weather variables and imported dengue cases in Australia. Emerg Microbes Infect. 2013;2(12):e87.CrossRefPubMedPubMedCentral
19.
go back to reference Nelder JA, Wedderburn RWM. Generalized linear models. J R Stat Soc Ser A (General). 1972;135(3):370–84.CrossRef Nelder JA, Wedderburn RWM. Generalized linear models. J R Stat Soc Ser A (General). 1972;135(3):370–84.CrossRef
20.
go back to reference Team RC: R: a language and environment for statistical computing: R Foundation for stastical computing. 2017. Team RC: R: a language and environment for statistical computing: R Foundation for stastical computing. 2017.
21.
go back to reference Liu W, Ji H, Shan J, Bao J, Sun Y, Li J, Bao C, Tang F, Yang K, Bergquist R, et al. Spatiotemporal dynamics of hand-foot-mouth disease and its relationship with meteorological factors in Jiangsu Province, China. PLoS One. 2015;10(6):e0131311.CrossRefPubMedPubMedCentral Liu W, Ji H, Shan J, Bao J, Sun Y, Li J, Bao C, Tang F, Yang K, Bergquist R, et al. Spatiotemporal dynamics of hand-foot-mouth disease and its relationship with meteorological factors in Jiangsu Province, China. PLoS One. 2015;10(6):e0131311.CrossRefPubMedPubMedCentral
22.
go back to reference Gui J, Liu Z, Zhang T, Hua Q, Jiang Z, Chen B, Gu H, Lv H, Dong C. Epidemiological characteristics and spatial-temporal clusters of hand, foot, and mouth disease in Zhejiang Province, China, 2008-2012. PLoS One. 2015;10(9):e0139109.CrossRefPubMedPubMedCentral Gui J, Liu Z, Zhang T, Hua Q, Jiang Z, Chen B, Gu H, Lv H, Dong C. Epidemiological characteristics and spatial-temporal clusters of hand, foot, and mouth disease in Zhejiang Province, China, 2008-2012. PLoS One. 2015;10(9):e0139109.CrossRefPubMedPubMedCentral
23.
go back to reference Liu Y, Wang X, Pang C, Yuan Z, Li H, Xue F. Spatio-temporal analysis of the relationship between climate and hand, foot, and mouth disease in Shandong province, China, 2008-2012. BMC Infect Dis. 2015;15:146.CrossRefPubMedPubMedCentral Liu Y, Wang X, Pang C, Yuan Z, Li H, Xue F. Spatio-temporal analysis of the relationship between climate and hand, foot, and mouth disease in Shandong province, China, 2008-2012. BMC Infect Dis. 2015;15:146.CrossRefPubMedPubMedCentral
24.
go back to reference Chen Z, Sun H, Yan Y, Wang Y, Zhu C, Zhou W, Huang L, Wang M, Mize M, Tian J, et al. Epidemiological profiles of hand, foot, and mouth disease, including meteorological factors, in Suzhou, China. Arch Virol. 2015;160(1):315–21.CrossRefPubMed Chen Z, Sun H, Yan Y, Wang Y, Zhu C, Zhou W, Huang L, Wang M, Mize M, Tian J, et al. Epidemiological profiles of hand, foot, and mouth disease, including meteorological factors, in Suzhou, China. Arch Virol. 2015;160(1):315–21.CrossRefPubMed
25.
go back to reference Huang X, Wei H, Wu S, Du Y, Liu L, Su J, Xu Y, Wang H, Li X, Wang Y, et al. Epidemiological and etiological characteristics of hand, foot, and mouth disease in Henan, China, 2008–2013. Sci Rep. 2015;5:8904.CrossRefPubMedPubMedCentral Huang X, Wei H, Wu S, Du Y, Liu L, Su J, Xu Y, Wang H, Li X, Wang Y, et al. Epidemiological and etiological characteristics of hand, foot, and mouth disease in Henan, China, 2008–2013. Sci Rep. 2015;5:8904.CrossRefPubMedPubMedCentral
26.
go back to reference Song Y, Wang F, Wang B, Tao S, Zhang H, Liu S, Ramirez O, Zeng Q. Time series analyses of hand, foot and mouth disease integrating weather variables. PLoS One. 2015;10(3):e0117296.CrossRefPubMedPubMedCentral Song Y, Wang F, Wang B, Tao S, Zhang H, Liu S, Ramirez O, Zeng Q. Time series analyses of hand, foot and mouth disease integrating weather variables. PLoS One. 2015;10(3):e0117296.CrossRefPubMedPubMedCentral
27.
go back to reference Chen KT, Chang HL, Wang ST, Cheng YT, Yang JY. Epidemiologic features of hand-foot-mouth disease and herpangina caused by enterovirus 71 in Taiwan, 1998-2005. Pediatrics. 2007;120(2):e244–52.CrossRefPubMed Chen KT, Chang HL, Wang ST, Cheng YT, Yang JY. Epidemiologic features of hand-foot-mouth disease and herpangina caused by enterovirus 71 in Taiwan, 1998-2005. Pediatrics. 2007;120(2):e244–52.CrossRefPubMed
28.
go back to reference Ma E, Lam T, Chan KC, Wong C, Chuang SK. Changing epidemiology of hand, foot, and mouth disease in Hong Kong, 2001-2009. Jpn J Infect Dis. 2010;63(6):422–6.PubMed Ma E, Lam T, Chan KC, Wong C, Chuang SK. Changing epidemiology of hand, foot, and mouth disease in Hong Kong, 2001-2009. Jpn J Infect Dis. 2010;63(6):422–6.PubMed
29.
go back to reference Onozuka D, Hashizume M. The influence of temperature and humidity on the incidence of hand, foot, and mouth disease in Japan. Sci Total Environ. 2011;410-411:119–25.CrossRefPubMed Onozuka D, Hashizume M. The influence of temperature and humidity on the incidence of hand, foot, and mouth disease in Japan. Sci Total Environ. 2011;410-411:119–25.CrossRefPubMed
30.
go back to reference Liu L, Luan RS, Yin F, Zhu XP, Lu Q. Predicting the incidence of hand, foot and mouth disease in Sichuan province, China using the ARIMA model. Epidemiol Infect. 2016;144(1):144–51.CrossRefPubMed Liu L, Luan RS, Yin F, Zhu XP, Lu Q. Predicting the incidence of hand, foot and mouth disease in Sichuan province, China using the ARIMA model. Epidemiol Infect. 2016;144(1):144–51.CrossRefPubMed
31.
go back to reference Kim HJ, Hyeon JY, Hwang S, Lee YP, Lee SW, Yoo JS, Kang B, Ahn JB, Jeong YS, Lee JW. Epidemiology and virologic investigation of human enterovirus 71 infection in the Republic of Korea from 2007 to 2012: a nationwide cross-sectional study. BMC Infect Dis. 2016;16(1):425.CrossRefPubMedPubMedCentral Kim HJ, Hyeon JY, Hwang S, Lee YP, Lee SW, Yoo JS, Kang B, Ahn JB, Jeong YS, Lee JW. Epidemiology and virologic investigation of human enterovirus 71 infection in the Republic of Korea from 2007 to 2012: a nationwide cross-sectional study. BMC Infect Dis. 2016;16(1):425.CrossRefPubMedPubMedCentral
32.
go back to reference Akiyoshi K, Suga T, Mori A. Enteroviruses in patients experiencing multiple episodes of hand, foot, and mouth disease in the same season in Kobe, Japan, 2011. Jpn J Infect Dis. 2012;65(5):459–61.CrossRefPubMed Akiyoshi K, Suga T, Mori A. Enteroviruses in patients experiencing multiple episodes of hand, foot, and mouth disease in the same season in Kobe, Japan, 2011. Jpn J Infect Dis. 2012;65(5):459–61.CrossRefPubMed
33.
go back to reference Wang Y, Feng Z, Yang Y, Self S, Gao Y, Longini IM, Wakefield J, Zhang J, Wang L, Chen X, et al. Hand, foot, and mouth disease in China: patterns of spread and transmissibility. Epidemiology (Cambridge, Mass). 2011;22(6):781–92.CrossRef Wang Y, Feng Z, Yang Y, Self S, Gao Y, Longini IM, Wakefield J, Zhang J, Wang L, Chen X, et al. Hand, foot, and mouth disease in China: patterns of spread and transmissibility. Epidemiology (Cambridge, Mass). 2011;22(6):781–92.CrossRef
34.
go back to reference Wang P, Goggins WB, Chan EYY. Hand, foot and mouth disease in Hong Kong: a time-series analysis on its relationship with weather. PLoS One. 2016;11(8):e0161006.CrossRefPubMedPubMedCentral Wang P, Goggins WB, Chan EYY. Hand, foot and mouth disease in Hong Kong: a time-series analysis on its relationship with weather. PLoS One. 2016;11(8):e0161006.CrossRefPubMedPubMedCentral
35.
go back to reference Li T, Yang Z, Liu X, Kang Y, Wang M. Hand-foot-and-mouth disease epidemiological status and relatinship with meteorological variables in Guangzhou, southern China, 2008-2012. Rev Inst Med Trop Sao Paulo. 2014;56(6):533–9.CrossRefPubMedPubMedCentral Li T, Yang Z, Liu X, Kang Y, Wang M. Hand-foot-and-mouth disease epidemiological status and relatinship with meteorological variables in Guangzhou, southern China, 2008-2012. Rev Inst Med Trop Sao Paulo. 2014;56(6):533–9.CrossRefPubMedPubMedCentral
36.
go back to reference Liao J, Yu S, Yang F, Yang M, Hu Y, Zhang J. Short-term effects of climatic variables on hand, foot, and mouth disease in mainland China, 2008-2013: a multilevel spatial Poisson regression model accounting for overdispersion. PLoS One. 2016;11(1):e0147054.CrossRefPubMedPubMedCentral Liao J, Yu S, Yang F, Yang M, Hu Y, Zhang J. Short-term effects of climatic variables on hand, foot, and mouth disease in mainland China, 2008-2013: a multilevel spatial Poisson regression model accounting for overdispersion. PLoS One. 2016;11(1):e0147054.CrossRefPubMedPubMedCentral
37.
go back to reference Zhang Z, Xie X, Chen X, Li Y, Lu Y, Mei S, Liao Y, Lin H. Short-term effects of meteorological factors on hand, foot and mouth disease among children in Shenzhen, China: non-linearity, threshold and interaction. Sci Total Environ. 2016;539:576–82.CrossRefPubMed Zhang Z, Xie X, Chen X, Li Y, Lu Y, Mei S, Liao Y, Lin H. Short-term effects of meteorological factors on hand, foot and mouth disease among children in Shenzhen, China: non-linearity, threshold and interaction. Sci Total Environ. 2016;539:576–82.CrossRefPubMed
Metadata
Title
Different responses of weather factors on hand, foot and mouth disease in three different climate areas of Gansu, China
Authors
Faxiang Gou
Xinfeng Liu
Jian He
Dongpeng Liu
Yao Cheng
Haixia Liu
Xiaoting Yang
Kongfu Wei
Yunhe Zheng
Xiaojuan Jiang
Lei Meng
Wenbiao Hu
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2860-4

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