Skip to main content

Advertisement

SpringerLink
Log in

Predicting the outbreak of hand, foot, and mouth disease in Nanjing, China: a time-series model based on weather variability

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

Hand, foot, and mouth disease (HFMD) is a significant public health issue in China and an accurate prediction of epidemic can improve the effectiveness of HFMD control. This study aims to develop a weather-based forecasting model for HFMD using the information on climatic variables and HFMD surveillance in Nanjing, China. Daily data on HFMD cases and meteorological variables between 2010 and 2015 were acquired from the Nanjing Center for Disease Control and Prevention, and China Meteorological Data Sharing Service System, respectively. A multivariate seasonal autoregressive integrated moving average (SARIMA) model was developed and validated by dividing HFMD infection data into two datasets: the data from 2010 to 2013 were used to construct a model and those from 2014 to 2015 were used to validate it. Moreover, we used weekly prediction for the data between 1 January 2014 and 31 December 2015 and leave-1-week-out prediction was used to validate the performance of model prediction. SARIMA (2,0,0)52 associated with the average temperature at lag of 1 week appeared to be the best model (R 2 = 0.936, BIC = 8.465), which also showed non-significant autocorrelations in the residuals of the model. In the validation of the constructed model, the predicted values matched the observed values reasonably well between 2014 and 2015. There was a high agreement rate between the predicted values and the observed values (sensitivity 80%, specificity 96.63%). This study suggests that the SARIMA model with average temperature could be used as an important tool for early detection and prediction of HFMD outbreaks in Nanjing, China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bertrand I, Schijven JF, Sanchez G, Wyn-Jones P, Ottoson J, Morin T et al (2012) The impact of temperature on the inactivation of enteric viruses in food and water: a review. J Appl Microbiol 112(6):1059–1074

    Article  CAS  Google Scholar 

  • Blomqvist S, Klemola P, Kaijalainen S, Paananen A, Simonen ML, Vuorinen T et al (2010) Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. J Clin Virol 48(1):49–54

    Article  CAS  Google Scholar 

  • Box G, Jenkins G (1970) Time-series analysis: forecasting and control. Holden-Day, San Francisco

    Google Scholar 

  • Chan KP, Goh KT, Chong CY, Teo ES, Lau G, Ling AE (2003) Epidemic hand, foot and mouth disease caused by human enterovirus 71, Singapore. Emerg Infect Dis 9(1):78–85

    Article  Google Scholar 

  • Chan LG, Parashar UD, Lye MS, Ong FG, Zaki SR, Alexander JP et al (2000) Deaths of children during an outbreak of hand, foot, and mouth disease in Sarawak, Malaysia: clinical and pathological characteristics of the disease. For the outbreak study group. Clin Infect Dis 31(3):678–683

    Article  CAS  Google Scholar 

  • Chen B, Sumi A, Toyoda S, Hu Q, Zhou D, Mise K et al (2015a) Time series analysis of reported cases of hand, foot, and mouth disease from 2010 to 2013 in Wuhan, China. BMC Infect Dis 15:495

    Article  Google Scholar 

  • Chen C, Lin H, Li X, Lang L, Xiao X, Ding P et al (2014) Short-term effects of meteorological factors on children hand, foot and mouth disease in Guangzhou, China. Int J Biometeorol 58(7):1605–1614

    Article  Google Scholar 

  • Chen Z, Sun H, Yan Y, Wang Y, Zhu C, Zhou W et al (2015b) Epidemiological profiles of hand, foot, and mouth disease, including meteorological factors, in Suzhou, China. Arch Virol 160(1):315–321

    Article  CAS  Google Scholar 

  • Cheng J, Zhu R, Xu Z, Wu J, Wang X, Li K et al (2016) Impact of temperature variation between adjacent days on childhood hand, foot and mouth disease during April and July in urban and rural Hefei, China. Int J Biometeorol 60(6):883–890

    Article  Google Scholar 

  • Chua KB, Kasri AR (2011) Hand foot and mouth disease due to enterovirus 71 in Malaysia. Virol Sin 26(4):221–228

    Article  Google Scholar 

  • De W, Changwen K, Wei L, Monagin C, Jin Y, Cong M et al (2011) A large outbreak of hand, foot, and mouth disease caused by EV71 and CAV16 in Guangdong, China, 2009. Arch Virol 156(6):945–953

    Article  CAS  Google Scholar 

  • Deng T, Huang Y, Yu S, Gu J, Huang C, Xiao G et al (2013) Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong province, China. PLoS One 8(2):e56943

    Article  CAS  Google Scholar 

  • Feng H, Duan G, Zhang R, Zhang W (2014) Time series analysis of hand-foot-mouth disease hospitalization in Zhengzhou: establishment of forecasting models using climate variables as predictors. PLoS One 9(1):e87916

    Article  Google Scholar 

  • Guo C, Yang J, Guo Y, Ou QQ, Shen SQ, Ou CQ et al (2016) Short-term effects of meteorological factors on pediatric hand, foot, and mouth disease in Guangdong, China: a multi-city time-series analysis. BMC Infect Dis 16(1):524

    Article  Google Scholar 

  • Hii YL, Rocklov J, Ng N (2011) Short term effects of weather on hand, foot and mouth disease. PLoS One 6(2):e16796

    Article  CAS  Google Scholar 

  • Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF et al (1999) An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N Engl J Med 341(3):929–935

    Article  CAS  Google Scholar 

  • Huang Y, Deng T, Yu S, Gu J, Huang C, Xiao G et al (2013) 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 13:134

    Article  Google Scholar 

  • Jiang M, Wei D, WL O, Li KX, Luo DZ, Li YQ et al (2012) Autopsy findings in children with hand, foot, and mouth disease. N Engl J Med 367(1):91–92

    Article  CAS  Google Scholar 

  • Li T, Yang Z, Di B, Wang M (2014) Hand foot and mouth disease and weather factors in Guangzhou, southern China. Epidemiol Infect 142(8):1741–1750

    Article  CAS  Google Scholar 

  • Lin H, Zou H, Wang Q, Liu C, Lang L, Hou X et al (2013) Short-term effect of EI Nino-Southern Oscillation on pediatric hand, foot and mouth disease in Shenzhen, China. PLoS One 8(7):e65585

    Article  CAS  Google Scholar 

  • Liu L, Luan RS, Yin F, Zhu XP, Lu Q (2016) Predicting the incidence of hand, foot and mouth disease in Sichuan province, China using the ARIMA model. Epidemiol Infect 144(1):144–151

    Article  CAS  Google Scholar 

  • Liu MY, Liu W, Luo J, Liu Y, Zhu Y, Berman H et al (2011) Characterization of an outbreak of hand, foot, and mouth disease in Nanchang, China in 2010. PLoS One 6(9):e25287

    Article  CAS  Google Scholar 

  • Liu W, Ji H, Shan J, Bao J, Sun Y, Li J et al (2015a) Spatiotemporal dynamics of hand-foot-mouth disease and its relationship with meteorological factors in Jiangsu province, China. PLoS One 10(6):e0131311

    Article  Google Scholar 

  • Liu Y, Wang X, Pang C, Yuan Z, Li H, Xue F (2015b) Spatio-temporal analysis of the relationship between climate and hand, foot, and mouth disease in Shandong province, China, 2008-2012. BMC Infect Dis 15:146

    Article  Google Scholar 

  • Luz PM, Mendes BV, Codeco CT, Struchiner CJ, Galvani AP (2008) Time series analysis of dengue incidence in Rio de Janeiro, Brazil. Am J Trop Med Hyg 79(6):933–939

    Google Scholar 

  • Ma E, Lam T, Wong C, Chuang SK (2010) Is hand, foot and mouth disease associated with meteorological parameters? Epidemiol Infect 138(12):1779–1788

    Article  CAS  Google Scholar 

  • Maes M, De Meyer F (2000) Relationships of climatic data to immune and hematologic variables in normal human. Neuro Endocrinol Lett 21(2):127–136

    Google Scholar 

  • Midekisa A, Senay G, Henebry GM, Semuniguse P, Wimberly MC (2012) Remote sensing-based time series models for malaria early warning in the highlands of Ethiopia. Malar J 11:165

    Article  Google Scholar 

  • Onozuka D, Hashizume M (2011) The influence of temperature and humidity on the incidence of hand, foot, and mouth disease in Japan. Sci Total Environ 410–411:119–125

    Article  Google Scholar 

  • Puenpa J, Theamboonlers A, Korkong S, Linsuwanon P, Thongmee C, Chatproedprai S et al (2011) Molecular characterization and complete genome analysis of human enterovirus 71 and coxsackievirus A16 from children with hand, foot and mouth disease in Thailand during 2008-2011. Arch Virol 156(11):2007–2013

    Article  CAS  Google Scholar 

  • Rajtar B, Majek M, Polanski L, Polz-Dacewicz M (2008) Enteroviruses in water environment-a potential threat to public health. Ann Agric Environ Med 15(2):199–203

    Google Scholar 

  • Qian H, Huo D, Wang X, Jia L, Li X, Li J et al (2016) Detecting spatial-temporal cluster of hand foot and mouth disease in Beijing, China, 2009-2014. BMC Infect Dis 16(1):206

    Article  Google Scholar 

  • Ren H, Li J, Yuan ZA, JY H, Yu Y, YH L (2013) The development of a combined mathematical model to forecast the incidence of hepatitis E in Shanghai, China. BMC Infect Dis 13:421

    Article  Google Scholar 

  • Shi Y, Liu X, Kok SY, Rajarethinam J, Liang S, Yap G et al (2016) Three-month real-time dengue forecast models: an early warning system for outbreak alerts and policy decision support in Singapore. Environ Health Perspect 124(9):1369–1375

    Google Scholar 

  • Styra D, Usovaite A, Damauskaite J, Juozulynas A (2009) Leaps in cardiovascular diseases after a decrease of hard cosmic ray flux and atmospheric pressure in Vilnius city in 2004-2007. Int J Biometeorol 53(6):471–477

    Article  CAS  Google Scholar 

  • Tu PV, Thao NT, Perera D, Huu TK, Tien NT, Thuong TC et al (2007) Epidemiologic and virologic investigation of hand, foot, and mouth disease, southern Vietnam, 2005. Emerg Infect Dis 13(11):1733–1741

    Article  CAS  Google Scholar 

  • Wang JF, Guo YS, Christakos G, Yang WZ, Liao YL, Li ZJ et al (2011) Hand foot and mouth disease: spatiotemporal transmission and climate. Int J Health Geogr 10:25

    Article  Google Scholar 

  • Wang P, Goggins WB, Chan EY (2016) Hand, foot and mouth disease in Hong Kong: a time-series analysis on its relationship with weather. PLoS One 11(8):e0161006

    Article  Google Scholar 

  • Wei J, Hansen A, Liu Q, Sun Y, Weinstein P, Bi P (2015) The effect of meteorological variables on the transmission of hand, foot and mouth disease in four major cities of Shanxi province, China: a time series data analysis (2009-2013). PLoS Negl Trop Dis 9(3):e0003572

    Article  Google Scholar 

  • Wong SS, Yip CC, Lau SK, Yuen KY (2010) Human enterovirus 71 and hand, foot and mouth disease. Epidemiol Infect 138(8):1071–1089

    Article  CAS  Google Scholar 

  • Wu Y, Yeo A, Phoon MC, Tan EL, Poh CL, Quak SH et al (2010) 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 14(12):e1076–e1081

    Article  Google Scholar 

  • Xiao X, Gasparrini A, Huang J, Liao Q, Liu F, Yin F et al (2017) The exposure-response relationship between temperature and childhood hand, foot and mouth disease: a multicity study from mainland China. Environ Int 100:102–109

    Article  Google Scholar 

  • Xie YH, Chongsuvivatwong V, Tang Z, McNeil EB, Tan Y (2014) Spatio-temporal clustering of hand, foot, and mouth disease at the county level in Guangxi, China. PLoS One 9(2):e88065

    Article  Google Scholar 

  • Xing W, Liao Q, Viboud C, Zhang J, Sun J, JT W et al (2014) Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis 14(4):308–318

    Article  Google Scholar 

  • Xu J, Zhao D, Su H, Xie M, Cheng J, Wang X et al (2016) Impact of temperature variability on childhood hand, foot and mouth disease in Huainan, China. Public Health 134:86–94

    Article  CAS  Google Scholar 

  • Yin F, Zhang T, Liu L, Lv Q, Li X (2016) The association between ambient temperature and childhood hand, foot, and mouth disease in Chengdu, China: a distributed lag non-linear analysis. Sci Rep 6:27305

    Article  CAS  Google Scholar 

  • Yu Y, Li J, Zhou L, Chen XD (2015) Association of meteorological factors with incidence of hand, foot and mouth disease in Nanjing city from 2010 to 2013 [in Chinese]. J Environ Occup Med 32:1132–1135

    Google Scholar 

  • Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y et al (2010) An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in Fuyang city of China. Virol J 7:94

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions and Jiangsu Government Scholarship for Overseas Studies.

Author information

Authors and Affiliations

  1. Department of Social Medicine and Health Education, School of Public Health, Nanjing Medical University, Nanjing, 211166, China

    Sijun Liu, Jianming Wang & Zhuchao Wu

  2. Department of Epidemiology, School of Public Health, Nanjing Medical University, Nanjing, 211166, China

    Sijun Liu, Jiaping Chen, Jianming Wang, Fei Xu & Hongbing Shen

  3. School of Public Health and Social Work, Queensland University of Technology, Kelvin Grove, Brisbane, Queensland, 4059, Australia

    Sijun Liu, Zhiwei Xu, Wenbiao Hu & Shilu Tong

  4. Department of Infectious Diseases, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing Medical University, Nanjing, 210008, China

    Weihua Wu

  5. Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, 4059, Australia

    Zhiwei Xu, Wenbiao Hu & Shilu Tong

  6. Department of Non-communicable Disease Prevention, Nanjing Municipal Center for Disease Control and Prevention, Nanjing, 210003, China

    Fei Xu

Authors
  1. Sijun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiaping Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhuchao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weihua Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhiwei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wenbiao Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shilu Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hongbing Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wenbiao Hu or Fei Xu.

Ethics declarations

This study was approved by the Ethical Committee of Nanjing Medical University.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Table S1

(DOCX 263 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Chen, J., Wang, J. et al. Predicting the outbreak of hand, foot, and mouth disease in Nanjing, China: a time-series model based on weather variability. Int J Biometeorol 62, 565–574 (2018). https://doi.org/10.1007/s00484-017-1465-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-017-1465-3

Keywords

Search

Navigation