Skip to main content
SpringerLink
Log in

Impact of temperature variation between adjacent days on childhood hand, foot and mouth disease during April and July in urban and rural Hefei, China

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

Abstract

Previous studies have found that both high temperature and low temperature increase the risk of childhood hand, foot and mouth disease (HFMD). However, little is known about whether temperature variation between neighboring days has any effects on childhood HFMD. A Poisson generalized linear regression model, combined with a distributed lag non-linear model, was applied to examine the relationship between temperature change and childhood HFMD in Hefei, China, from 1st January 2010 to 31st December 2012. Temperature change was defined as the difference of current day’s mean temperature and previous day’s mean temperature. Late spring and early summer (April–July) were chosen as the main study period due to it having the highest childhood HFMD incidence. There was a statistical association between temperature change between neighboring days and childhood HFMD. The effects of temperature change on childhood HFMD increased below a temperature change of 0 °C (temperature drop). The temperature change has the greatest adverse effect on childhood HFMD at 7 days lag, with 4 % (95 % confidence interval 2–7 %) increase per 3 °C drop of temperature. Male children and urban children appeared to be more vulnerable to the effects of temperature change. Temperature change between adjacent days might be an alternative temperature indictor for exploring the temperature–HFMD relationship.

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

Similar content being viewed by others

References

  • Ang LW, Koh BK, Chan KP, Chua LT, James L, Goh KT (2009) Epidemiology and control of hand, foot and mouth disease in Singapore, 2001–2007. Ann Acad Med Singap 38(2):106–112

    Google Scholar 

  • Ballester F, Corella D, Perez-Hoyos S, Saez M, Hervas A (1997) Mortality as a function of temperature. A study in Valencia, Spain, 1991–1993. Int J Epidemiol 26(3):551–561

    Article  CAS  Google Scholar 

  • Biswas T (2012) Enterovirus 71 causes hand, foot and mouth disease outbreak in Cambodia. Natl Med J India 25(5):316

    Google Scholar 

  • Carder M, McNamee R, Beverland I, Elton R, Cohen GR, Boyd J, Agius RM (2005) The lagged effect of cold temperature and wind chill on cardiorespiratory mortality in Scotland. Occup Environ Med 62(10):702–710

    Article  CAS  Google Scholar 

  • Cardosa MJ, Perera D, Brown BA, Cheon D, Chan HM, Chan KP, Cho H, McMinn P (2003) 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 9(4):461–468

    Article  Google Scholar 

  • Chen C, Lin H, Li X, Lang L, Xiao X, Ding P, He P, Zhang Y, Wang M, Liu Q (2014) Short-term effects of meteorological factors on children hand, foot and mouth disease inGuangzhou, China. Int J Biometeorol 58(7):1605–1614

    Article  Google Scholar 

  • Chen KT, Chang HL, Wang ST, Cheng YT, Yang JY (2007) Epidemiologic features of hand-foot-mouth disease and herpangina caused by enterovirus 71 in Taiwan, 1998–2005. Pediatrics 120(2):e244–e252

    Article  Google Scholar 

  • Chinese Center for Disease Control and Prevention (China CDC). The report of legal infectious disease. http://www.chinacdc.cn/tjsj/fdcrbbg/. Accessed December 7 2013

  • 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 

  • Elwood PC, Beswick A, O’Brien JR, Renaud S, Fifield R, Limb ES, Bainton D (1993) Temperature and risk factors for ischaemic heart disease in the Caerphilly prospective study. Br Heart J 70(6):520–523

    Article  CAS  Google Scholar 

  • Epstein PR (2005) Climate change and human health. N Engl J Med 353(14):1433–1436

    Article  CAS  Google Scholar 

  • Fujimoto T, Chikahira M, Yoshida S, Ebira H, Hasegawa A, Totsuka A, Nishio O (2002) 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 46(9):621–627

    Article  CAS  Google Scholar 

  • Gasparrini A. (2013) Distributed lag non-linear models in R: the package dlnm. http://cran.r-project.org/web/packages/dlnm/vignettes/dlnmOverview.pdf. Accessed December 7 2013

  • Gasparrini A, Armstrong B, Kenward MG (2010) Distributed lag non-linear models. Stat Med 29(21):2224–2234

    Article  CAS  Google Scholar 

  • Guo Y, Barnett AG, Yu W, Pan X, Ye X, Huang C, Tong S (2011) A large change in temperature between neighbouring days increases the risk of mortality. PLoS One 6(2):e16511

    Article  CAS  Google Scholar 

  • Ha J, Kim H (2013) Changes in the association between summer temperature and mortality in Seoul, South Korea. Int J Biometeorol 57(4):535–544

    Article  Google Scholar 

  • Hammond GW, Raddatz RL, Gelskey DE (1989) Impact of atmospheric dispersion and transport of viral aerosols on the epidemiology of influenza. Rev Infect Dis 11(3):494–497

    Article  CAS  Google Scholar 

  • Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, Tsai SF, Wang JR, Shih SR (1999) An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus rEpidemic Working Group. N Engl J Med 341(13):929–935

    Article  CAS  Google Scholar 

  • Hosoya M, Kawasaki Y, Sato M, Honzumi K, Hayashi A, Hiroshima T, Ishiko H, Kato K, Suzuki H (2007) Genetic diversity of coxsackievirus A16 associated with hand, foot, and mouth disease epidemics in Japan from 1983 to 2003. J Clin Microbiol 45(1):112–120

    Article  CAS  Google Scholar 

  • Hosoya M, Kawasaki Y, Sato M, Honzumi K, Kato A, Hiroshima T, Ishiko H, Suzuki H (2006) Genetic diversity of enterovirus 71 associated with hand, foot and mouth disease epidemics in Japan from 1983 to 2003. Pediatr Infect Dis J 25(8):691–694

    Article  Google Scholar 

  • Huang Y, Deng T, Yu S, Gu J, Huang C, Xiao G, Hao Y (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 

  • Kesic MJ, Meyer M, Bauer R, Jaspers I (2012) Exposure to ozone modulates human airway protease/antiprotease balance contributing to increased influenza A infection. PLoS One 7(4):e35108

    Article  CAS  Google Scholar 

  • Ji YB, Guo Y, Guo Q, Zhang CX, Ma JQ (2011) Analysis of notifiable infectious disease surveillance and reporting of medical units in 6 provinces. Mod Preventive Med 38(20):4266–4268

    Google Scholar 

  • Khanh TH, Sabanathan S, Thanh TT, Thoa le PK, Thuong TC, Hang V, Farrar J, Hien TT, Chau N, van Doorn HR (2012) Enterovirus 71-associated hand, foot, and mouth disease, Southern Vietnam, 2011. Emerg Infect Dis 18(12):2002–2005

    Article  Google Scholar 

  • Lin H, Zhang Y, Xu Y, Xu X, Liu T, Luo Y, Xiao J, Wu W, Ma W (2013a) Temperature changes between neighboring days and mortality in summer: a distributed lag non-linear time series analysis. PLoS One 8(6):e66403

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lowen AC, Mubareka S, Steel J, Palese P (2007) Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 3(10):1470–1476

    Article  CAS  Google Scholar 

  • Mercer JB, Osterud B, Tveita T (1999) The effect of short-term cold exposure on risk factors for cardiovascular disease. Thromb Res 95(2):93–104

    Article  CAS  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  CAS  Google Scholar 

  • Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (2007) Climate change 2007: impacts, adaptation and vulnerability: Intergovernmental Panel on Climate Change

  • 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 

  • Ren C, Williams GM, Tong S (2006) Does particulate matter modify the association between temperature and cardiorespiratory diseases? Environ Health Perspect 114(11):1690–1696

    Google Scholar 

  • Roberts S (2004) Interactions between particulate air pollution and temperature in air pollution mortality time series studies. Environ Res 96(3):328–337

    Article  CAS  Google Scholar 

  • Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH (2010) Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 10(11):778–790

    Article  Google Scholar 

  • The Ministry of Health of the People’s Republic of China (MHC) (2010) Guide for the preparedness and control measures of hand, foot, and mouth disease in China. Int J Respir (2010 version) (in Chinese); 1473–75

  • Urashima M, Shindo N, Okabe N (2003) Seasonal models of herpangina and hand-foot-mouth disease to simulate annual fluctuations in urban warming in Tokyo. Jpn J Infect Dis 56(2):48–53

    Google Scholar 

  • Wang Y, Feng Z, Yang Y, Self S, Gao Y, Longini IM, Wakefield J, Zhang J, Wang L, Chen X, Yao L, Stanaway JD, Wang Z, Yang W (2011) Hand, foot, and mouth disease in China: patterns of spread and transmissibility. Epidemiology 22(6):781–792

    Article  CAS  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 

  • WPRO/WHO (2009) Hand, foot and mouth disease a rising menace in Asia. World Health Organization

  • Wu H, Wang H, Wang Q, Xin Q, Lin H (2014) The effect of meteorological factors on adolescent hand, foot, and mouth disease and associated effect modifiers. Glob Health Action 7:24664

    Google Scholar 

  • Xu M, Yu W, Tong S, Jia L, Liang F, Pan X (2015) Non-linear association between exposure to ambient temperature and children’s hand-foot-and-mouth disease in Beijing, China. PLoS One 10(5):e0126171

    Article  Google Scholar 

  • Xu Z, Etzel RA, Su H, Huang C, Guo Y, Tong S (2012) Impact of ambient temperature on children’s health: a systematic review. Environ Res 117:120–131

    Article  CAS  Google Scholar 

  • Xu Z, Hu W, Williams G, Clements AC, Kan H, Tong S (2013a) Air pollution, temperature and pediatric influenza in Brisbane, Australia. Environ Int 59:384–388

    Article  CAS  Google Scholar 

  • Xu Z, Shen H, Wang Z, Altmeyer R, Xia A, Mao S, Zhen Y, Li W, Zhao Y, Su H, Zhan L, Wang X, Pan H, Hu J, Zeng M (2013b) The population-based health effect of hand, foot and mouth disease in children in Shanghai, Pediatr Infect Dis J doi:10.1097/INF.0000000000000136

Download references

Acknowledgments

The authors thank the Hefei Bureau of Meteorology and Hefei Center for Disease Control and Prevention for providing the data. This work was funded by Anhui Natural Science Fund (no. 1408085MH159).

Author information

Authors and Affiliations

  1. Department of Epidemiology and Health Statistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, Anhui, 230032, China

    Jian Cheng, Xu Wang, Kesheng Li, Liying Wen, Huihui Yang & Hong Su

  2. Department of Child and Maternal Health Care, School of Public Health, Anhui Medical University, Hefei, Anhui, 230032, China

    Rui Zhu

  3. School of Public Health and Social Work, Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvin Grove, Brisbane, QLD, 4509, Australia

    Zhiwei Xu

  4. Hefei Center for Disease Control and Prevention of Anhui province, Hefei, Anhui, 230061, China

    Jinju Wu

Authors
  1. Jian Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rui Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhiwei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinju Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kesheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Liying Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huihui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hong Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong Su.

Ethics declarations

Ethical approval was obtained from the Ethics Committee of Anhui Medical University prior to the data collection.

Conflict of interest

The authors declare that they have no competing interests.

Electronic Supplementary Material

Supplementary Fig. 1

(JPEG 74 kb)

Supplementary Fig. 2

(JPEG 132 kb)

Supplementary Fig. 3

(JPEG 132 kb)

Supplementary Fig. 4

(JPEG 94 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, J., Zhu, R., Xu, Z. et al. 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, 883–890 (2016). https://doi.org/10.1007/s00484-015-1082-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-015-1082-y

Keywords

Search

Navigation