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Short-term effects of meteorological factors on children hand, foot and mouth disease in Guangzhou, China

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Abstract

Hand, foot and mouth disease (HFMD) is a contagious viral illness that commonly affects infants and children. The underlying risk factors have not yet been systematically examined. This study analyzed the short-term effects of meteorological factors on children HFMD in Guangzhou, China. Daily count of HFMD among children younger than 15 years and meteorological variables from 2009 to 2011 were collected to construct the time series. A generalized additive model was applied to estimate the effects of meteorological factors on HFMD occurrence, after adjusting for long-term trend, seasonal trend, day of week, and public holidays. A negative association between temperature and children HFMD occurrence was observed at lag days 1–3, with the relative risk (RR) for a 1 °C increase on lag day 2 being 0.983 (95 % confidence intervals (CI) 0.977 to 0.989); positive effect was found for temperature at lag days 5–9, with the highest effect at lag day 6 (RR = 1.014, 95 % CI 1.006 to 1.023). Higher humidity was associated with increased HFMD at lag days 3–10, with the highest effect at lag day 8 (RR = 1.009 for 1 % increase in relative humidity, 95 % CI 1.007 to 1.010). And we also observed significant positive effect for rainfall at lag days 4 and 8 (RR = 1.001, 95 % CI 1.000 to 1.002) for 1-mm increase. Subgroup analyses showed that the positive effects of temperature were more pronounced among younger children. This study suggests that meteorological factors might be important predictors of children HFMD occurrence in Guangzhou.

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References

  • Abad FX, Pinto RM, Bosch A (1994) Survival of enteric viruses on environmental fomites. Appl Environ Microbiol 60(10):3704–3710

    CAS  Google Scholar 

  • Bell ML, Peng RD, Dominici F, Samet JM (2009) Emergency hospital admissions for cardiovascular diseases and ambient levels of carbon monoxide. Circulation 120(11):949–955

    Article  CAS  Google Scholar 

  • Bendig JW, Fleming DM (1996) Epidemiological, virological, and clinical features of an epidemic of hand, foot, and mouth disease in England and Wales. Commun Dis Rep CDR Rev 6(6):R81–R86

    CAS  Google Scholar 

  • Blomqvist S, Klemola P, Kaijalainen S, Paananen A, Simonen M-L, Vuorinen T, Roivainen M (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 

  • Chang LY, King CC, Hsu KH, Ning HC, Tsao KC, Li CC, Huang YC, Shih SR, Chiou ST, Chen PY (2002) Risk factors of enterovirus 71 infection and associated hand, foot, and mouth disease/herpangina in children during an epidemic in Taiwan. Pediatrics 109(6):e88–e88

    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 

  • Fletcher L, Noakes C, Beggs C, Sleigh P (2004) The importance of bioaerosols in hospital infections and the potential for control using germicidal ultraviolet irradiation. Proceedings of the First Seminar on Applied Aerobiology. Murcia, Spain, May

    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, Wang JR, Shih SR (1999) An epidemic of enterovirus 71 infection in Taiwan. New England Journal of Medicine 341(13):929–935

    Article  CAS  Google Scholar 

  • Hong Y-C, Lee J-T, Kim H, Kwon H-J (2002) Air pollution: a new risk factor in ischemic stroke mortality. Stroke 33(9):2165–2169

    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. The Pediatric infectious disease journal 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(1):134

    Article  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 

  • Jiang M, Wei D, Ou WL, Li KX, Luo DZ, Li YQ, Chen E, Nong GM (2012) Autopsy findings in children with hand, foot, and mouth disease. New England Journal of Medicine 367(1):91–92

    Article  CAS  Google Scholar 

  • Jin Y, Zhang J, Sun JL, Chang ZR (2012) Epidemiology of hand, foot and mouth disease in mainland of China, 2011. Disease Surveillance 27(9):676–679

    Google Scholar 

  • Kan H, Jia J, Chen B (2003) Acute stroke mortality and air pollution: new evidence from Shanghai, China. J Occup Health 45(5):321–323

    Article  Google Scholar 

  • Kan H, London SJ, Chen G, Zhang Y, Song G, Zhao N, Jiang L, Chen B (2007) Differentiating the effects of fine and coarse particles on daily mortality in Shanghai, China. Environ Int 33(3):376–384

    Article  Google Scholar 

  • Li W, Yi L, Su J, Lu J, Zeng H, Guan D, Ma C, Zhang W, Xiao H, Li H, Zhang Y, Lin J, Ke C (2013) Seroepidemiology of human enterovirus71 and coxsackievirusA16 among children in Guangdong province, China. BMC Infect Dis 13(1):322

    Article  Google Scholar 

  • Lin H, Yang L, Liu Q, Wang T, Hossain SR, Ho SC, Tian L (2012) Time series analysis of Japanese encephalitis and weather in Linyi City, China. Int J Public Health 57(2):289–296

    Article  Google Scholar 

  • Lin H, Zhang Z, Lu L, Li X and Liu Q (2013a). Meteorological factors are associated with hemorrhagic fever with renal syndrome in Jiaonan County, China, 2006–2011. International Journal of Biometeorology: 1–7.

  • Lin HL, Wang HC, Wu W, Lang LL, Wang QZ, Tian LW (2013b) The effects of smoke-free legislation on acute myocardial infarction: a systematic review and meta-analysis. BMC Public Health 13(1):529

    Article  Google Scholar 

  • Lin HL, Zou H, Nie J, Liu CX, Li ZJ (2013c) Short term effects of El Nino-Southern Oscillation on hand, foot, and mouth disease in Shenzhen, China. PLoS One 8(7):e65585

    Article  CAS  Google Scholar 

  • Liu C, Liu Q, Lin H, Xin B, Nie J (2013) Spatial analysis of dengue fever in Guangdong Province, China, 2001–2006. Asia Pac J Public Health. doi:10.1177/1010539512472356

    Google Scholar 

  • Lu L, Lin HL, Tian LW, Yang WZ, Sun JM, Liu QY (2009) Time series analysis of dengue fever and weather in Guangzhou, China. BMC Public Health 9:395

    Article  CAS  Google Scholar 

  • Ma E, Lam T, Chan KC, Wong C, Chuang SK (2010a) Changing epidemiology of hand, foot, and mouth disease in Hong Kong, 2001–2009. Jpn J Infect Dis 63(6):422–426

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mao LX, Wu B, Bao WX, Han FA, Xu L, Ge QJ, Yang J, Yuan ZH, Miao CH, Huang XX, Zhang C, Xu H (2010) Epidemiology of hand, foot, and mouth disease and genotype characterization of Enterovirus 71 in Jiangsu, China. J Clin Virol 49(2):100–104

    Article  Google Scholar 

  • Morris R, Sanson R, Stern M, Stevenson M, Wilesmith J (2002) Decision-support tools for foot and mouth disease control. Rev sci tech Off int Epiz 21(3):557–564

    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. Science of the Total Environment 410–411:119–125

    Article  Google Scholar 

  • Ooi E-E, Phoon M-C, Ishak B, Chan S-H (2002) Seroepidemiology of human enterovirus 71, Singapore. Emerg Infect Dis 8(9):995–997

    Article  Google Scholar 

  • Peng RD, Dominici F, Louis TA (2006) Model choice in time series studies of air pollution and mortality. J R Stat Soc A Stat Soc 169(2):179–203

    Article  Google Scholar 

  • Peng RD, Bell ML, Geyh AS, McDermott A, Zeger SL, Samet JM, Dominici F (2009) Emergency admissions for cardiovascular and respiratory diseases and the chemical composition of fine particle air pollution. Environ Health Perspect 117(6):957–963

    Article  CAS  Google Scholar 

  • Suminski RR, Poston WC, Market P, Hyder M, Sara PA (2008) Meteorological conditions are associated with physical activities performed in open-air settings. Int J Biometeorol 52(3):189–197

    Article  Google Scholar 

  • Tian LW, Bi Y, Ho SC, Liu W, Liang S, Goggins WB, Chan EY, Zhou S, Sung JJ (2008) One-year delayed effect of fog on malaria transmission: a time-series analysis in the rain forest area of Mengla County, south-west China. Malar J 7:110

    Article  Google Scholar 

  • 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 

  • Villeneuve PJ, Burnett RT, Shi Y, Krewski D, Goldberg MS, Hertzman C, Chen Y, Brook J (2003) A time-series study of air pollution, socioeconomic status, and mortality in Vancouver, Canada. J Expo Anal Environ Epidemiol 13(6):427–435

    Article  CAS  Google Scholar 

  • Wang J, Guo YS, Christakos G, Yang WZ, Liao YL, Li ZJ, Li XZ, Lai SJ, Chen HY (2011) Hand, foot and mouth disease: spatiotemporal transmission and climate. Int J Health Geogr 10(1):25

    Article  Google Scholar 

  • Wong S, Yip C, Lau S, Yuen K (2010) Human enterovirus 71 and hand, foot and mouth disease. Epidemiol Infect 138(8):1071–1089

    Article  CAS  Google Scholar 

  • Wood SN (2006). Generalized additive models: an introduction with R, CRC.

  • Wu Y, Yeo A, Phoon M, Tan E, Poh C, Quak S, Chow VTK (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 

  • Zeka A, Zanobetti A, Schwartz J (2006) Individual-level modifiers of the effects of particulate matter on daily mortality. Am J Epidemiol 163(9):849–859

    Article  Google Scholar 

  • Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, Ji F, Wang XJ, Gao YJ, Chen L (2009) An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J Clin Virol 44(4):262–267

    Article  Google Scholar 

  • Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A (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(1):94

    Article  Google Scholar 

  • Zhao P, Yang S, Yu R (2010) Long-term changes in rainfall over eastern China and large-scale atmospheric circulation associated with recent global warming. J Climate 23(6):1544–1562

    Article  Google Scholar 

  • Zhu Z, Zhu S, Guo X, Wang J, Wang D, Yan D, Tan X, Tang L, Zhu H, Yang Z (2010) Retrospective seroepidemiology indicated that human enterovirus 71 and coxsackievirus A16 circulated wildly in central and southern China before large-scale outbreaks from 2008. Virol J 7(1):300–305

    Article  Google Scholar 

Download references

Acknowledgments

This study was funded by National Major Research Program of China (no. 2012CB955500). We thank the anonymous reviewers for numerous helpful comments.

Conflicts of interest

The authors have no conflicts of interest to declare.

Ethics statement

Data were collected as part of government-mandated health surveillance and analyzed anonymously so ethical approval was not needed.

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Correspondence to Ming Wang or Qiyong Liu.

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Chun Chen, Hualiang Lin, and Xiaoquan Li contributed to this work equally.

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Chen, C., Lin, H., Li, X. et al. Short-term effects of meteorological factors on children hand, foot and mouth disease in Guangzhou, China. Int J Biometeorol 58, 1605–1614 (2014). https://doi.org/10.1007/s00484-013-0764-6

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