Skip to main content
Top
Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Spatio-temporal clustering analysis and its determinants of hand, foot and mouth disease in Hunan, China, 2009–2015

Authors: Xinrui Wu, Shixiong Hu, Abuaku Benjamin Kwaku, Qi Li, Kaiwei Luo, Ying Zhou, Hongzhuan Tan

Published in: BMC Infectious Diseases | Issue 1/2017

Login to get access

Abstract

Background

Hand, foot and mouth disease (HFMD) is one of the highest reported infectious diseases with several outbreaks across the world. This study aimed at describing epidemiological characteristics, investigating spatio-temporal clustering changes, and identifying determinant factors in different clustering areas of HFMD.

Methods

Descriptive statistics was used to evaluate the epidemic characteristics of HFMD from 2009 to 2015. Spatial autocorrelation and spatio-temporal cluster analysis were used to explore the spatial temporal patterns. An autologistic regression model was employed to explore determinants of HFMD clustering.

Results

The incidence rates of HFMD ranged from 54.31/10 million to 318.06/10 million between 2009 and 2015 in Hunan. Cases were mainly prevalent in children aged 5 years and even younger, with an average male-to-female sex ratio of 1.66, and two epidemic periods in each year. Clustering areas gathered in the northern regions in 2009 and in the central regions from 2010 to 2012. They moved to central-southern regions in 2013 and 2014 and central-western regions in 2015. The significant risk factors of HFMD clusters were rainfall (OR = 2.187), temperature (OR = 4.329) and humidity (OR = 2.070). The protect factor was wind speed (OR = 0.258).

Conclusions

The HFMD incidence from 2009 to 2015 in Hunan showed a new spatiotemporal clustering tendency, with the shifting trend of clustering areas toward south and west. Meteorological factors showed a strong association with HFMD clustering, which may assist in predicting future spatial-temporal clusters.
Appendix
Available only for authorised users
Literature
1.
go back to reference Hosoya M, Kawasaki Y, Sato M, Honzumi K, Kato A, Hiroshima T, Ishiko H, Suzuki H. Genetic diversity of enterovirus 71 associated with hand, foot and mouth disease epidemics in Japan from 1983 to 2003. Pediatr Infect Dis J. 2006;25(8):691–4.CrossRefPubMed Hosoya M, Kawasaki Y, Sato M, Honzumi K, Kato A, Hiroshima T, Ishiko H, Suzuki H. Genetic diversity of enterovirus 71 associated with hand, foot and mouth disease epidemics in Japan from 1983 to 2003. Pediatr Infect Dis J. 2006;25(8):691–4.CrossRefPubMed
2.
go back to reference Weng KF, Chen LL, Huang PN, Shih SR. Neural pathogenesis of enterovirus 71 infection. Microbes and infection / Institut Pasteur. 2010;12(7):505–10.CrossRef Weng KF, Chen LL, Huang PN, Shih SR. Neural pathogenesis of enterovirus 71 infection. Microbes and infection / Institut Pasteur. 2010;12(7):505–10.CrossRef
3.
go back to reference Deng T, Huang Y, Yu S, Gu J, Huang C, Xiao G, Hao Y. Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong Province. China PloS one. 2013;8(2):e56943. Deng T, Huang Y, Yu S, Gu J, Huang C, Xiao G, Hao Y. Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong Province. China PloS one. 2013;8(2):e56943.
4.
go back to reference Hu M, Li Z, Wang J, Jia L, Liao Y, Lai S, Guo Y, Zhao D, Yang W. Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS One. 2012;7(6):e38978.CrossRefPubMedPubMedCentral Hu M, Li Z, Wang J, Jia L, Liao Y, Lai S, Guo Y, Zhao D, Yang W. Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS One. 2012;7(6):e38978.CrossRefPubMedPubMedCentral
5.
go back to reference Chumakov M, Voroshilova M, Shindarov L, Lavrova I, Gracheva L, Koroleva G, Vasilenko S, Brodvarova I, Nikolova M, Gyurova S, et al. Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol. 1979;60(3–4):329–40.CrossRefPubMed Chumakov M, Voroshilova M, Shindarov L, Lavrova I, Gracheva L, Koroleva G, Vasilenko S, Brodvarova I, Nikolova M, Gyurova S, et al. Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol. 1979;60(3–4):329–40.CrossRefPubMed
6.
go back to reference Ishimaru Y, Nakano S, Yamaoka K, Takami S. Outbreaks of hand, foot, and mouth disease by enterovirus 71. High incidence of complication disorders of central nervous system. Arch Dis Child. 1980;55(8):583–8.CrossRefPubMedPubMedCentral Ishimaru Y, Nakano S, Yamaoka K, Takami S. Outbreaks of hand, foot, and mouth disease by enterovirus 71. High incidence of complication disorders of central nervous system. Arch Dis Child. 1980;55(8):583–8.CrossRefPubMedPubMedCentral
7.
go back to reference McMinn P, Stratov I, Nagarajan L, Davis S. Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2001;32(2):236–42.CrossRef McMinn P, Stratov I, Nagarajan L, Davis S. Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2001;32(2):236–42.CrossRef
8.
go back to reference Nguyen NT, Pham HV, Hoang CQ, Nguyen TM, Nguyen LT, Phan HC, Phan LT, Vu LN, Tran Minh NN. Epidemiological and clinical characteristics of children who died from hand, foot and mouth disease in Vietnam, 2011. BMC Infect Dis. 2014;14:341.CrossRefPubMedPubMedCentral Nguyen NT, Pham HV, Hoang CQ, Nguyen TM, Nguyen LT, Phan HC, Phan LT, Vu LN, Tran Minh NN. Epidemiological and clinical characteristics of children who died from hand, foot and mouth disease in Vietnam, 2011. BMC Infect Dis. 2014;14:341.CrossRefPubMedPubMedCentral
9.
go back to reference Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A, 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, Mao N, Xu S, Zhu S, Cui A, 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
10.
go back to reference Xing W, Liao Q, Viboud C, Zhang J, Sun J, Wu JT, Chang Z, Liu F, Fang VJ, Zheng Y, et al. Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis. 2014;14(4):308–18.CrossRefPubMedPubMedCentral Xing W, Liao Q, Viboud C, Zhang J, Sun J, Wu JT, Chang Z, Liu F, Fang VJ, Zheng Y, et al. Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis. 2014;14(4):308–18.CrossRefPubMedPubMedCentral
11.
go back to reference Huang Y, Deng T, Yu S, Gu J, Huang C, Xiao G, Hao Y. Effect of meteorological variables on the incidence of hand, foot, and mouth disease in children: a time-series analysis in Guangzhou. China BMC infectious diseases. 2013;13:134.CrossRefPubMed Huang Y, Deng T, Yu S, Gu J, Huang C, Xiao G, Hao Y. Effect of meteorological variables on the incidence of hand, foot, and mouth disease in children: a time-series analysis in Guangzhou. China BMC infectious diseases. 2013;13:134.CrossRefPubMed
12.
go back to reference Li T, Yang Z, Di B, Wang M. Hand-foot-and-mouth disease and weather factors in Guangzhou, southern China. Epidemiol Infect. 2014;142(8):1741–50.CrossRefPubMed Li T, Yang Z, Di B, Wang M. Hand-foot-and-mouth disease and weather factors in Guangzhou, southern China. Epidemiol Infect. 2014;142(8):1741–50.CrossRefPubMed
13.
go back to reference Huang JX, Wang JF, Li ZJ, Wang Y, Lai SJ, Yang WZ. Visualized exploratory spatiotemporal analysis of hand-foot-mouth disease in southern China. PLoS One. 2015;10(11):e0143411.CrossRefPubMedPubMedCentral Huang JX, Wang JF, Li ZJ, Wang Y, Lai SJ, Yang WZ. Visualized exploratory spatiotemporal analysis of hand-foot-mouth disease in southern China. PLoS One. 2015;10(11):e0143411.CrossRefPubMedPubMedCentral
14.
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(1):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(1):312–36.CrossRefPubMedPubMedCentral
15.
go back to reference Wang J, Cao Z, Zeng DD, Wang Q, Wang X, Qian H. Epidemiological analysis, detection, and comparison of space-time patterns of Beijing hand-foot-mouth disease (2008-2012). PLoS One. 2014;9(3):e92745.CrossRefPubMedPubMedCentral Wang J, Cao Z, Zeng DD, Wang Q, Wang X, Qian H. Epidemiological analysis, detection, and comparison of space-time patterns of Beijing hand-foot-mouth disease (2008-2012). PLoS One. 2014;9(3):e92745.CrossRefPubMedPubMedCentral
16.
go back to reference Dolan C, O'Halloran A, Bradley DG, Croke DT, Evans A, O'Brien JK, Dicker P, Shields DC. Genetic stratification of pathogen-response-related and other variants within a homogeneous Caucasian Irish population. European journal of human genetics : EJHG. 2005;13(7):798–806.CrossRefPubMed Dolan C, O'Halloran A, Bradley DG, Croke DT, Evans A, O'Brien JK, Dicker P, Shields DC. Genetic stratification of pathogen-response-related and other variants within a homogeneous Caucasian Irish population. European journal of human genetics : EJHG. 2005;13(7):798–806.CrossRefPubMed
17.
go back to reference Flahaut B, Mouchart M, San Martin E, Thomas I. The local spatial autocorrelation and the kernel method for identifying black zones. A comparative approach. Accid Anal Prev. 2003;35(6):991–1004.CrossRefPubMed Flahaut B, Mouchart M, San Martin E, Thomas I. The local spatial autocorrelation and the kernel method for identifying black zones. A comparative approach. Accid Anal Prev. 2003;35(6):991–1004.CrossRefPubMed
18.
go back to reference Mattsson BJ, Zipkin EF, Gardner B, Blank PJ, Sauer JR, Royle JA. Explaining local-scale species distributions: relative contributions of spatial autocorrelation and landscape heterogeneity for an avian assemblage. PLoS One. 2013;8(2):e55097.CrossRefPubMedPubMedCentral Mattsson BJ, Zipkin EF, Gardner B, Blank PJ, Sauer JR, Royle JA. Explaining local-scale species distributions: relative contributions of spatial autocorrelation and landscape heterogeneity for an avian assemblage. PLoS One. 2013;8(2):e55097.CrossRefPubMedPubMedCentral
19.
go back to reference Viladomat J, Mazumder R, McInturff A, McCauley DJ, Hastie T. Assessing the significance of global and local correlations under spatial autocorrelation: a nonparametric approach. Biometrics. 2014;70(2):409–18.CrossRefPubMedPubMedCentral Viladomat J, Mazumder R, McInturff A, McCauley DJ, Hastie T. Assessing the significance of global and local correlations under spatial autocorrelation: a nonparametric approach. Biometrics. 2014;70(2):409–18.CrossRefPubMedPubMedCentral
20.
go back to reference Waldhor T. The spatial autocorrelation coefficient Moran's I under heteroscedasticity. Stat Med. 1996;15(7–9):887–92.CrossRefPubMed Waldhor T. The spatial autocorrelation coefficient Moran's I under heteroscedasticity. Stat Med. 1996;15(7–9):887–92.CrossRefPubMed
22.
go back to reference Anselin L. Local indicators of spatial association-LISA. Geogr Anal. 1995;27:93–115.CrossRef Anselin L. Local indicators of spatial association-LISA. Geogr Anal. 1995;27:93–115.CrossRef
23.
go back to reference Gu H, Zhang W, Xu H, Li P, Wu L, Guo P, Hao Y, Lu J, Zhang D: [predicating risk area of human infection with avian influenza a (H7N9) virus by using early warning model in China]. Zhonghua liu xing bing xue za zhi =Zhonghua liuxingbingxue zazhi 2015, 36(5):470–475. Gu H, Zhang W, Xu H, Li P, Wu L, Guo P, Hao Y, Lu J, Zhang D: [predicating risk area of human infection with avian influenza a (H7N9) virus by using early warning model in China]. Zhonghua liu xing bing xue za zhi =Zhonghua liuxingbingxue zazhi 2015, 36(5):470–475.
24.
go back to reference Kulldorff M, Huang L, Pickle L, Duczmal L. An elliptic spatial scan statistic. Stat Med. 2006;25(22):3929–43.CrossRefPubMed Kulldorff M, Huang L, Pickle L, Duczmal L. An elliptic spatial scan statistic. Stat Med. 2006;25(22):3929–43.CrossRefPubMed
25.
go back to reference Kulldorff M, Feuer EJ, Miller BA, Freedman LS. Breast cancer clusters in the northeast United States: a geographic analysis. Am J Epidemiol. 1997;146(2):161–70.CrossRefPubMed Kulldorff M, Feuer EJ, Miller BA, Freedman LS. Breast cancer clusters in the northeast United States: a geographic analysis. Am J Epidemiol. 1997;146(2):161–70.CrossRefPubMed
26.
go back to reference Kleinman KP, Abrams AM, Kulldorff M, Platt R. A model-adjusted space-time scan statistic with an application to syndromic surveillance. Epidemiol Infect. 2005;133(3):409–19.CrossRefPubMedPubMedCentral Kleinman KP, Abrams AM, Kulldorff M, Platt R. A model-adjusted space-time scan statistic with an application to syndromic surveillance. Epidemiol Infect. 2005;133(3):409–19.CrossRefPubMedPubMedCentral
27.
go back to reference Kulldorff M, Heffernan R, Hartman J, Assuncao R, Mostashari F. A space-time permutation scan statistic for disease outbreak detection. PLoS Med. 2005;2(3):e59.CrossRefPubMedPubMedCentral Kulldorff M, Heffernan R, Hartman J, Assuncao R, Mostashari F. A space-time permutation scan statistic for disease outbreak detection. PLoS Med. 2005;2(3):e59.CrossRefPubMedPubMedCentral
28.
go back to reference Anselin LS. I; Kho, Y: GeoDa: A introduction to spatial data analysis. Geogr Anal. 2006;38:5–22.CrossRef Anselin LS. I; Kho, Y: GeoDa: A introduction to spatial data analysis. Geogr Anal. 2006;38:5–22.CrossRef
29.
go back to reference Besag J. Spatial interaction and the statistical analysis of lattice systems. J R Stat Soc Ser B Methodol. 1974;36(2):192–236. Besag J. Spatial interaction and the statistical analysis of lattice systems. J R Stat Soc Ser B Methodol. 1974;36(2):192–236.
30.
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. 2011;22(6):781–92.CrossRefPubMedPubMedCentral 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. 2011;22(6):781–92.CrossRefPubMedPubMedCentral
31.
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
32.
go back to reference Zhuang ZC, Kou ZQ, Bai YJ, Cong X, Wang LH, Li C, Zhao L, Yu XJ, Wang ZY, Wen HL. Epidemiological research on hand, foot, and mouth disease in mainland China. Viruses. 2015;7(12):6400–11.CrossRefPubMedPubMedCentral Zhuang ZC, Kou ZQ, Bai YJ, Cong X, Wang LH, Li C, Zhao L, Yu XJ, Wang ZY, Wen HL. Epidemiological research on hand, foot, and mouth disease in mainland China. Viruses. 2015;7(12):6400–11.CrossRefPubMedPubMedCentral
33.
go back to reference Liu Y, Wang X, Liu Y, Sun D, Ding S, Zhang B, Du Z, Xue F. Detecting spatial-temporal clusters of HFMD from 2007 to 2011 in Shandong Province. China. PloS one. 2013;8(5):e63447.CrossRefPubMed Liu Y, Wang X, Liu Y, Sun D, Ding S, Zhang B, Du Z, Xue F. Detecting spatial-temporal clusters of HFMD from 2007 to 2011 in Shandong Province. China. PloS one. 2013;8(5):e63447.CrossRefPubMed
34.
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. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases. 2010;14(9):e775–80.CrossRef Ma E, Chan KC, Cheng P, Wong C, Chuang SK. The enterovirus 71 epidemic in 2008--public health implications for Hong Kong. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases. 2010;14(9):e775–80.CrossRef
35.
go back to reference Liu W, Wu S, Xiong Y, Li T, Wen Z, Yan M, Qin K, Liu Y, Wu J. Co-circulation and genomic recombination of coxsackievirus A16 and enterovirus 71 during a large outbreak of hand, foot, and mouth disease in Central China. PLoS One. 2014;9(4):e96051.CrossRefPubMedPubMedCentral Liu W, Wu S, Xiong Y, Li T, Wen Z, Yan M, Qin K, Liu Y, Wu J. Co-circulation and genomic recombination of coxsackievirus A16 and enterovirus 71 during a large outbreak of hand, foot, and mouth disease in Central China. PLoS One. 2014;9(4):e96051.CrossRefPubMedPubMedCentral
36.
go back to reference Tian H, Zhang Y, Sun Q, Zhu S, Li X, Pan Z, Xu W, Xu B. Prevalence of multiple enteroviruses associated with hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China: outbreaks of coxsackieviruses a10 and b3. PLoS One. 2014;9(1):e84233.CrossRefPubMedPubMedCentral Tian H, Zhang Y, Sun Q, Zhu S, Li X, Pan Z, Xu W, Xu B. Prevalence of multiple enteroviruses associated with hand, foot, and mouth disease in Shijiazhuang City, Hebei province, China: outbreaks of coxsackieviruses a10 and b3. PLoS One. 2014;9(1):e84233.CrossRefPubMedPubMedCentral
37.
go back to reference Blomqvist S, Klemola P, Kaijalainen S, Paananen A, Simonen ML, Vuorinen T, Roivainen M. Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology. 2010;48(1):49–54.CrossRef Blomqvist S, Klemola P, Kaijalainen S, Paananen A, Simonen ML, Vuorinen T, Roivainen M. Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology. 2010;48(1):49–54.CrossRef
38.
go back to reference Li JL, Yuan J, Yang F, Wu ZQ, Hu YF, Xue Y, Zhou BP, Jin Q. Epidemic characteristics of hand, foot, and mouth disease in southern China, 2013: coxsackievirus A6 has emerged as the predominant causative agent. The Journal of infection. 2014;69(3):299–303.CrossRefPubMed Li JL, Yuan J, Yang F, Wu ZQ, Hu YF, Xue Y, Zhou BP, Jin Q. Epidemic characteristics of hand, foot, and mouth disease in southern China, 2013: coxsackievirus A6 has emerged as the predominant causative agent. The Journal of infection. 2014;69(3):299–303.CrossRefPubMed
39.
go back to reference Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, Bailly JL, Peigue-Lafeuille H. Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: a large citywide, prospective observational study. Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 2012;18(5):E110–8.CrossRef Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, Bailly JL, Peigue-Lafeuille H. Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: a large citywide, prospective observational study. Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 2012;18(5):E110–8.CrossRef
40.
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. Annals of the Academy of Medicine, Singapore 2009. 2001-2007;38(2):106–12. Ang LW, Koh BK, Chan KP, Chua LT, James L, Goh KT. Epidemiology and control of hand, foot and mouth disease in Singapore. Annals of the Academy of Medicine, Singapore 2009. 2001-2007;38(2):106–12.
41.
go back to reference Hsu CH, Lu CY, Shao PL, Lee PI, Kao CL, Chung MY, Chang LY, Huang LM. Epidemiologic and clinical features of non-polio enteroviral infections in northern Taiwan in. Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi 2011. 2008;44(4):265–73.CrossRef Hsu CH, Lu CY, Shao PL, Lee PI, Kao CL, Chung MY, Chang LY, Huang LM. Epidemiologic and clinical features of non-polio enteroviral infections in northern Taiwan in. Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi 2011. 2008;44(4):265–73.CrossRef
42.
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
43.
go back to reference Liao J, Qin Z, Zuo Z, Yu S, Zhang J. Spatial-temporal mapping of hand foot and mouth disease and the long-term effects associated with climate and socio-economic variables in Sichuan Province, China from 2009 to 2013. Sci Total Environ. 2016;563-564:152–9.CrossRefPubMed Liao J, Qin Z, Zuo Z, Yu S, Zhang J. Spatial-temporal mapping of hand foot and mouth disease and the long-term effects associated with climate and socio-economic variables in Sichuan Province, China from 2009 to 2013. Sci Total Environ. 2016;563-564:152–9.CrossRefPubMed
44.
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. 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.
Metadata
Title
Spatio-temporal clustering analysis and its determinants of hand, foot and mouth disease in Hunan, China, 2009–2015
Authors
Xinrui Wu
Shixiong Hu
Abuaku Benjamin Kwaku
Qi Li
Kaiwei Luo
Ying Zhou
Hongzhuan Tan
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2742-9

Other articles of this Issue 1/2017

BMC Infectious Diseases 1/2017 Go to the issue