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Published in: BMC Infectious Diseases 1/2015

Open Access 01-12-2015 | Research article

Spatio-temporal analysis of the relationship between climate and hand, foot, and mouth disease in Shandong province, China, 2008–2012

Authors: Yunxia Liu, Xianjun Wang, Chunkun Pang, Zhongshang Yuan, Hongkai Li, Fuzhong Xue

Published in: BMC Infectious Diseases | Issue 1/2015

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Abstract

Background

Hand, foot, and mouth disease (HFMD) is the most common communicable disease in China. Shandong Province is one of the most seriously affected areas. The distribution of HFMD had spatial heterogeneity and seasonal characteristic in this setting. The aim of this study was to explore the associations between climate and HFMD by a Bayesian approach from spatio-temporal interactions perspective.

Methods

The HFMD data of Shandong Province during 2008–2012 were derived from the China National Disease Surveillance Reporting and Management System. And six climatic indicators were obtained from the Meteorological Bureau of Shandong Province. The global spatial autocorrelation statistic (Moran’s I) was used to detect the spatial autocorrelation of HFMD cases in each year. The optimal one among four Bayesian models was further adopted to estimate the relative risk of the occurrence of HFMD via Markov chain Monte Carlo.

Results

The annual average incidence rate of HFMD was 104.40 per 100,000 in Shandong Province. Positive spatial autocorrelation appeared at county level (Moran’s I ≥0.30, P < 0.001). The best fitting Spatio-temporal interactive model showed that annual average temperature, annual average pressure, annual average relative humidity, annual average wind speed and annual sunshine hours were significantly positive related to the occurrence of HFMD. The estimated relative risk of 36, 87, 91, 79, 65 out of 140 counties for 2008–2012 respectively were significantly more than 1.

Conclusions

There were obvious spatio-temporal heterogeneity of HFMD in Shandong Province, and the climatic indicators were associated with the epidemic of HFMD. Bayesian approach should be recommended to capture the spatial-temporal pattern of HFMD.
Literature
1.
go back to reference Gopalkrishna V, Patil PR, Patil GP, Chitambar SD. Circulation of multiple enterovirus serotypes causing hand, foot and mouth disease in India. J Med Microbiol. 2012;61:420–5.CrossRefPubMed Gopalkrishna V, Patil PR, Patil GP, Chitambar SD. Circulation of multiple enterovirus serotypes causing hand, foot and mouth disease in India. J Med Microbiol. 2012;61:420–5.CrossRefPubMed
2.
go back to reference Zeng M, Li YF, Wang XH, Lu GP, Shen HG, Yu H, et al. Epidemiology of hand, foot, and mouth disease in children in Shanghai 2007–2010. Epidemiol Infect. 2012;140:1122–30.CrossRefPubMed Zeng M, Li YF, Wang XH, Lu GP, Shen HG, Yu H, et al. Epidemiology of hand, foot, and mouth disease in children in Shanghai 2007–2010. Epidemiol Infect. 2012;140:1122–30.CrossRefPubMed
3.
go back to reference Fan X, Jiang J, Liu Y, Huang X, Wang P, Liu L, et al. Detection of human enterovirus 71 and Coxsackievirus A16 in an outbreak of hand, foot, and mouth disease in Henan Province, China in 2009. Virus Genes. 2013;46:1–9.CrossRefPubMed Fan X, Jiang J, Liu Y, Huang X, Wang P, Liu L, et al. Detection of human enterovirus 71 and Coxsackievirus A16 in an outbreak of hand, foot, and mouth disease in Henan Province, China in 2009. Virus Genes. 2013;46:1–9.CrossRefPubMed
4.
go back to reference Cardosa MJ, Perera D, Brown BA, Cheon D, Chan HM, Chan KP, et al. Molecular epidemiology of human enterovirus 71 strains and recent outbreaks in the Asia-Pacific region: comparative analysis of the VP1 and VP4 genes. Emerg Infect Dis. 2003;9:461–8.CrossRefPubMed Cardosa MJ, Perera D, Brown BA, Cheon D, Chan HM, Chan KP, et al. Molecular epidemiology of human enterovirus 71 strains and recent outbreaks in the Asia-Pacific region: comparative analysis of the VP1 and VP4 genes. Emerg Infect Dis. 2003;9:461–8.CrossRefPubMed
5.
go back to reference Tu PV, Thao NT, Perera D, Huu TK, Tien NT, Thuong TC, et al. Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerg Infect Dis. 2007;13:1733–41.CrossRefPubMedPubMedCentral Tu PV, Thao NT, Perera D, Huu TK, Tien NT, Thuong TC, et al. Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerg Infect Dis. 2007;13:1733–41.CrossRefPubMedPubMedCentral
6.
go back to reference Fujimoto T, Chikahira M, Yoshida S, Ebira H, Hasegawa A, Totsuka A, et al. Outbreak of central nervous system disease associated with hand, foot, and mouth disease in Japan during the summer of 2000: detection and molecular epidemiology of enterovirus 71. Microbiol Immunol. 2002;46:621–7.CrossRefPubMed Fujimoto T, Chikahira M, Yoshida S, Ebira H, Hasegawa A, Totsuka A, et al. Outbreak of central nervous system disease associated with hand, foot, and mouth disease in Japan during the summer of 2000: detection and molecular epidemiology of enterovirus 71. Microbiol Immunol. 2002;46:621–7.CrossRefPubMed
7.
go back to reference Wang Y, Feng Z, Yang Y, Self S, Gao Y, Longini IM, et al. Hand, foot and mouth disease in china: patterns of spread and transmissibility during 2008–2009. Epidemiology. 2011;22:781–92.CrossRefPubMedPubMedCentral Wang Y, Feng Z, Yang Y, Self S, Gao Y, Longini IM, et al. Hand, foot and mouth disease in china: patterns of spread and transmissibility during 2008–2009. Epidemiology. 2011;22:781–92.CrossRefPubMedPubMedCentral
8.
go back to reference Wu Y, Yeo A, Phoon MC, Tan EL, Poh CL, Quak SH, et al. The largest outbreak of hand; foot and mouth disease in Singapore in 2008: the role of enterovirus 71 and coxsackievirus A strains. Int J Infect Dis. 2010;14:e1076–81.CrossRefPubMed Wu Y, Yeo A, Phoon MC, Tan EL, Poh CL, Quak SH, et al. The largest outbreak of hand; foot and mouth disease in Singapore in 2008: the role of enterovirus 71 and coxsackievirus A strains. Int J Infect Dis. 2010;14:e1076–81.CrossRefPubMed
9.
go back to reference Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, et al. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong. China J Clin Virol. 2009;44:262–7.CrossRefPubMed Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, et al. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong. China J Clin Virol. 2009;44:262–7.CrossRefPubMed
10.
go back to reference Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, et al. 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;7:94.CrossRefPubMedPubMedCentral Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, et al. 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;7:94.CrossRefPubMedPubMedCentral
11.
go back to reference Yan XF, Gao S, Xia JF, Ye R, Yu H, Long JE. Epidemic characteristics of hand, foot, and mouth disease in Shanghai from 2009 to 2010: Enterovirus 71 subgenotype C4 as the primary causative agent and a high incidence of mixed infections with coxsackievirus A16. Scand J Infect Dis. 2012;44:297–305.CrossRefPubMed Yan XF, Gao S, Xia JF, Ye R, Yu H, Long JE. Epidemic characteristics of hand, foot, and mouth disease in Shanghai from 2009 to 2010: Enterovirus 71 subgenotype C4 as the primary causative agent and a high incidence of mixed infections with coxsackievirus A16. Scand J Infect Dis. 2012;44:297–305.CrossRefPubMed
12.
go back to reference Liu MY, Liu W, Luo J, Liu Y, Zhu Y, Berman H, et al. Characterization of an outbreak of hand, foot, and mouth disease in Nanchang, China in 2010. PLoS One. 2011;6:e25287.CrossRefPubMedPubMedCentral Liu MY, Liu W, Luo J, Liu Y, Zhu Y, Berman H, et al. Characterization of an outbreak of hand, foot, and mouth disease in Nanchang, China in 2010. PLoS One. 2011;6:e25287.CrossRefPubMedPubMedCentral
13.
go back to reference Xu WB, Tan XJ. Hand, foot, and mouth disease: new challenge for the prevention and control of children infectious diseases in China. Disease Surveillance. 2009;24:649–51. Xu WB, Tan XJ. Hand, foot, and mouth disease: new challenge for the prevention and control of children infectious diseases in China. Disease Surveillance. 2009;24:649–51.
14.
go back to reference Ren M, Zhang K. The temporal and spatial distribution of hand-foot-mouth disease in China from May 2008 to 2010. Chin J Health Educ. 2011;27:568–70. Ren M, Zhang K. The temporal and spatial distribution of hand-foot-mouth disease in China from May 2008 to 2010. Chin J Health Educ. 2011;27:568–70.
15.
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
16.
go back to reference Ang LW, Koh BK, Chan KP, Chua LT, James L, Goh KT. Epidemiology and control of hand, foot and mouth disease in Singapore. Ann Acad Med Singapore. 2009;38:106–12.PubMed Ang LW, Koh BK, Chan KP, Chua LT, James L, Goh KT. Epidemiology and control of hand, foot and mouth disease in Singapore. Ann Acad Med Singapore. 2009;38:106–12.PubMed
17.
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;63:422–6.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;63:422–6.PubMed
18.
go back to reference Feng H, Duan G, Zhang R, Zhang W. Time series analysis of hand-foot-mouth disease hospitalization in Zhengzhou: establishment of forecasting models using climate variables as predictors. PLoS One. 2014;9:e87916.CrossRefPubMedPubMedCentral Feng H, Duan G, Zhang R, Zhang W. Time series analysis of hand-foot-mouth disease hospitalization in Zhengzhou: establishment of forecasting models using climate variables as predictors. PLoS One. 2014;9:e87916.CrossRefPubMedPubMedCentral
19.
go back to reference Zou XN, Zhang XZ, Wang B, Qiu YT. Etiologic and epidemiologic analysis of hand, foot, and mouth disease in Guangzhou city: a review of 4,753 cases. Braz J Infect Dis. 2012;16:457–65.CrossRefPubMed Zou XN, Zhang XZ, Wang B, Qiu YT. Etiologic and epidemiologic analysis of hand, foot, and mouth disease in Guangzhou city: a review of 4,753 cases. Braz J Infect Dis. 2012;16:457–65.CrossRefPubMed
20.
go back to reference Huang Y, Deng T, Yu S, Gu J, Huang C, Xiao G, et al. Effect of meteorological variables on the incidence of hand, foot, and mouth disease in children: a time-series analysis in Guangzhou. China BMC Infect Dis. 2013;13:134.CrossRefPubMed Huang Y, Deng T, Yu S, Gu J, Huang C, Xiao G, et al. Effect of meteorological variables on the incidence of hand, foot, and mouth disease in children: a time-series analysis in Guangzhou. China BMC Infect Dis. 2013;13:134.CrossRefPubMed
22.
go back to reference Zhuang D, Hu W, Ren H, Ai W, Xu X. The influences of temperature on spatiotemporal trends of hand-foot-and-mouth disease in mainland China. Int J Environ Health Res. 2014;24:1–10.CrossRefPubMed Zhuang D, Hu W, Ren H, Ai W, Xu X. The influences of temperature on spatiotemporal trends of hand-foot-and-mouth disease in mainland China. Int J Environ Health Res. 2014;24:1–10.CrossRefPubMed
23.
go back to reference Deng T, Huang Y, Yu S, Gu J, Huang C, Xiao G, et al. Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong Province. China PLoS One. 2013;8:e56943.CrossRefPubMed Deng T, Huang Y, Yu S, Gu J, Huang C, Xiao G, et al. Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong Province. China PLoS One. 2013;8:e56943.CrossRefPubMed
24.
go back to reference Zheng S, Cao CX, Cheng JQ, Wu YS, Xie X, Xu M. Epidemiological features of hand-foot-and-mouth disease in Shenzhen, China from 2008 to 2010. Epidemiol Infect. 2014;142:1751–62.CrossRefPubMed Zheng S, Cao CX, Cheng JQ, Wu YS, Xie X, Xu M. Epidemiological features of hand-foot-and-mouth disease in Shenzhen, China from 2008 to 2010. Epidemiol Infect. 2014;142:1751–62.CrossRefPubMed
25.
go back to reference Bo YC, Song C, Wang JF, Li XW. Using an autologistic regression model to identify spatial risk factors and spatial risk patterns of hand, foot and mouth disease (HFMD) in Mainland China. BMC Public Health. 2014;14:358.CrossRefPubMedPubMedCentral Bo YC, Song C, Wang JF, Li XW. Using an autologistic regression model to identify spatial risk factors and spatial risk patterns of hand, foot and mouth disease (HFMD) in Mainland China. BMC Public Health. 2014;14:358.CrossRefPubMedPubMedCentral
26.
go back to reference Huang J, Wang J, Bo Y, Xu C, Hu M, Huang D. Identification of health risks of hand, foot and mouth disease in china using the geographical detector technique. Int J Environ Res Public Health. 2014;11:3407–23.CrossRefPubMedPubMedCentral Huang J, Wang J, Bo Y, Xu C, Hu M, Huang D. Identification of health risks of hand, foot and mouth disease in china using the geographical detector technique. Int J Environ Res Public Health. 2014;11:3407–23.CrossRefPubMedPubMedCentral
27.
go back to reference Liu Y, Wang X, Liu Y, Sun D, Ding S, Zhang B, et al. Detecting Spatial-temporal clusters of HFMD from 2007 to 2011 in Shandong province. China PLoS One. 2013;8:e63447.CrossRefPubMed Liu Y, Wang X, Liu Y, Sun D, Ding S, Zhang B, et al. Detecting Spatial-temporal clusters of HFMD from 2007 to 2011 in Shandong province. China PLoS One. 2013;8:e63447.CrossRefPubMed
28.
go back to reference Samphutthanon R, Tripathi NK, Ninsawat S, Duboz R. Spatio-temporal distribution and hotspots of Hand, Foot and Mouth Disease (HFMD) in Northern Thailand. Int J Environ Res Public Health. 2013;11:312–36.CrossRefPubMedPubMedCentral Samphutthanon R, Tripathi NK, Ninsawat S, Duboz R. Spatio-temporal distribution and hotspots of Hand, Foot and Mouth Disease (HFMD) in Northern Thailand. Int J Environ Res Public Health. 2013;11:312–36.CrossRefPubMedPubMedCentral
29.
go back to reference Xie YH, Chongsuvivatwong V, Tang Z, McNeil EB, Tan Y. Spatio-temporal clustering of hand, foot, and mouth disease at the county level in Guangxi. China PLoS One. 2014;9:e88065.CrossRefPubMed Xie YH, Chongsuvivatwong V, Tang Z, McNeil EB, Tan Y. Spatio-temporal clustering of hand, foot, and mouth disease at the county level in Guangxi. China PLoS One. 2014;9:e88065.CrossRefPubMed
30.
go back to reference Zhang W, Li C, Ji G, Shi J, Ma Y, Zhang S. The application of flexible spatial scan statistic in spatial aggregation of HFMD. Chin J Health Stat. 2012;29:507–13. Zhang W, Li C, Ji G, Shi J, Ma Y, Zhang S. The application of flexible spatial scan statistic in spatial aggregation of HFMD. Chin J Health Stat. 2012;29:507–13.
31.
go back to reference Yu L, Zhou L, Tan L, Jiang H, Zhang F, Tian L, et al. Application of multiple seasonal ARIMA model in forecasting incidence of HFMD in Wuhan. China Int J Infect Dis. 2014;21:271.CrossRef Yu L, Zhou L, Tan L, Jiang H, Zhang F, Tian L, et al. Application of multiple seasonal ARIMA model in forecasting incidence of HFMD in Wuhan. China Int J Infect Dis. 2014;21:271.CrossRef
32.
go back to reference Hossain MM, Lawson AB. Space-time Bayesian small area disease risk models: development and evaluation with a focus on cluster detection. Environ Ecol Stat. 2010;17:73–95.CrossRefPubMedPubMedCentral Hossain MM, Lawson AB. Space-time Bayesian small area disease risk models: development and evaluation with a focus on cluster detection. Environ Ecol Stat. 2010;17:73–95.CrossRefPubMedPubMedCentral
33.
go back to reference Lunn DJ, Whittaker JC, Best N. A Bayesian toolkit for genetic association studies. Genet Epidemiol. 2006;30:231–47.CrossRefPubMed Lunn DJ, Whittaker JC, Best N. A Bayesian toolkit for genetic association studies. Genet Epidemiol. 2006;30:231–47.CrossRefPubMed
34.
go back to reference Gelman A, Pardoe I. Bayesian measures of explained variance and pooling in multilevel (hierarchical) models. Technometrics. 2006;48:241–51.CrossRef Gelman A, Pardoe I. Bayesian measures of explained variance and pooling in multilevel (hierarchical) models. Technometrics. 2006;48:241–51.CrossRef
35.
go back to reference Pan L, He X, Luo Y, Gao Q, Wu L, Li X, et al. Exploration of tuberculosis evolution characteristics and ecological factors based on the bayes temporal-spatial theory. Chin J Health Stat. 2013;30:658–60. 64. Pan L, He X, Luo Y, Gao Q, Wu L, Li X, et al. Exploration of tuberculosis evolution characteristics and ecological factors based on the bayes temporal-spatial theory. Chin J Health Stat. 2013;30:658–60. 64.
36.
go back to reference Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2014. Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2014.
37.
go back to reference Chinese Ministry of Health. Hand, foot and mouth disease control and prevention guide, 2009. Clin Educ Gen Pract. 2010;8:125–27. 33. Chinese Ministry of Health. Hand, foot and mouth disease control and prevention guide, 2009. Clin Educ Gen Pract. 2010;8:125–27. 33.
38.
go back to reference Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2009. Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2009.
39.
go back to reference Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2010. Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2010.
40.
go back to reference Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2011. Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2011.
41.
go back to reference Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2012. Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2012.
42.
go back to reference Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2013. Liu XH. Shandong statistical yearbook. Beijing: China Statistics Press; 2013.
43.
go back to reference Pfeiffer D, Robinson T, Stevenson M, Stevens K, Rogers D, Clements A. Spatial analysis in epidemiology. New York: Oxford University Press; 2008.CrossRef Pfeiffer D, Robinson T, Stevenson M, Stevens K, Rogers D, Clements A. Spatial analysis in epidemiology. New York: Oxford University Press; 2008.CrossRef
44.
go back to reference Souza WV, Carvalho MS, Albuquerque Mde F, Barcellos CC, Ximenes RA. Tuberculosis in intra-urban settings: a Bayesian approach. Trop Med Int Health. 2007;12:323–30.CrossRefPubMed Souza WV, Carvalho MS, Albuquerque Mde F, Barcellos CC, Ximenes RA. Tuberculosis in intra-urban settings: a Bayesian approach. Trop Med Int Health. 2007;12:323–30.CrossRefPubMed
45.
go back to reference Liu WD, Wu Y, Liang Q, Hu JL, Dai QG, Li Y, et al. Epidemiological characteristics and temporal-spatial clustering analysis on hand-foot-mouth disease in Jiangsu province, 2009–2011. Zhonghua Liu Xing Bing Xue Za Zhi. 2012;33:813–7.PubMed Liu WD, Wu Y, Liang Q, Hu JL, Dai QG, Li Y, et al. Epidemiological characteristics and temporal-spatial clustering analysis on hand-foot-mouth disease in Jiangsu province, 2009–2011. Zhonghua Liu Xing Bing Xue Za Zhi. 2012;33:813–7.PubMed
46.
go back to reference Hu M, Li Z, Wang J, Jia L, Liao Y, Lai S, et al. Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS One. 2012;7:e38978.CrossRefPubMedPubMedCentral Hu M, Li Z, Wang J, Jia L, Liao Y, Lai S, et al. Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS One. 2012;7:e38978.CrossRefPubMedPubMedCentral
47.
go back to reference Rodríguez-Prieto V, Martínez-López B, Barasona JÁ, Acevedo P, Romero B, Rofriguez-Campos S, et al. A Bayesian approach to study the risk variables for tuberculosis occurrence in domestic and wild ungulates in South Central Spain. BMC Vet Res. 2012;8:148.CrossRefPubMedPubMedCentral Rodríguez-Prieto V, Martínez-López B, Barasona JÁ, Acevedo P, Romero B, Rofriguez-Campos S, et al. A Bayesian approach to study the risk variables for tuberculosis occurrence in domestic and wild ungulates in South Central Spain. BMC Vet Res. 2012;8:148.CrossRefPubMedPubMedCentral
49.
go back to reference Odoi A, Martin SW, Michel P, Middleton D, Holt J, Wilson J. Investigation of clusters of giardiasis using GIS and a spatial scan statistic. Int J Health Geogr. 2004;3:11.CrossRefPubMedPubMedCentral Odoi A, Martin SW, Michel P, Middleton D, Holt J, Wilson J. Investigation of clusters of giardiasis using GIS and a spatial scan statistic. Int J Health Geogr. 2004;3:11.CrossRefPubMedPubMedCentral
50.
go back to reference Johnson GD. Small area mapping of prostate cancer incidence in New York State (USA) using fully Bayesian hierarchical modelling. Int J Health Geogr. 2004;3:29.CrossRefPubMedPubMedCentral Johnson GD. Small area mapping of prostate cancer incidence in New York State (USA) using fully Bayesian hierarchical modelling. Int J Health Geogr. 2004;3:29.CrossRefPubMedPubMedCentral
51.
go back to reference Tango T. A test for spatial disease clustering adjusted for multiple testing. Stat Med. 2000;19:191–204.CrossRefPubMed Tango T. A test for spatial disease clustering adjusted for multiple testing. Stat Med. 2000;19:191–204.CrossRefPubMed
52.
go back to reference Morgenstern H. Ecologic studies in epidemiology: concepts, principles, and methods. Annu Rev Public Health. 1995;16:61–81.CrossRefPubMed Morgenstern H. Ecologic studies in epidemiology: concepts, principles, and methods. Annu Rev Public Health. 1995;16:61–81.CrossRefPubMed
Metadata
Title
Spatio-temporal analysis of the relationship between climate and hand, foot, and mouth disease in Shandong province, China, 2008–2012
Authors
Yunxia Liu
Xianjun Wang
Chunkun Pang
Zhongshang Yuan
Hongkai Li
Fuzhong Xue
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2015
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-015-0901-4

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