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Seasonal modeling of hand, foot, and mouth disease as a function of meteorological variations in Chongqing, China

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Abstract

Hand, foot, and mouth disease (HFMD) is an enterovirus-induced infectious disease, mainly affecting children under 5 years old. Outbreaks of HFMD in recent years indicate the disease interacts with both the weather and season. This study aimed to investigate the seasonal association between HFMD and weather variation in Chongqing, China. Generalized additive models and distributed lag non-linear models based on a maximum lag of 14 days, with negative binomial distribution assumed to account for overdispersion, were constructed to model the association between reporting HFMD cases from 2009 to 2014 and daily mean temperature, relative humidity, total rainfall and sun duration, adjusting for trend, season, and day of the week. The year-round temperature and relative humidity, rainfall in summer, and sun duration in winter were all significantly associated with HFMD. An inverted-U relationship was found between mean temperature and HFMD above 19 °C in summer, with a maximum morbidity at 27 °C, while the risk increased linearly with the temperature in winter. A hockey-stick association was found for relative humidity in summer with increasing risks over 60%. Heavy rainfall, relative to no rain, was found to be associated with reduced HFMD risk in summer and 2 h of sunshine could decrease the risk by 21% in winter. The present study showed meteorological variables were differentially associated with HFMD incidence in two seasons. Short-term weather variation surveillance and forecasting could be employed as an early indicator for potential HFMD outbreaks.

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References

  • Alsop J, Flewett TH, Foster JR (1960) “Hand-foot-and-mouth disease” in Birmingham in 1959. Br Med J 2:1708–1711

    Article  CAS  Google Scholar 

  • Blomqvist S, Klemola P, Kaijalainen S, Paananen A, Simonen ML, Vuorinen T, Roivainen M (2010) 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 48:49–54. doi:10.1016/j.jcv.2010.02.002

    Article  CAS  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:e244–e252. doi:10.1542/peds.2006-3331

    Article  Google Scholar 

  • Chongqing Meteorological Bureau (2015) Climate of Chongqing. http://www.cqmb.gov.cn/ecms/qixiangfuwu/qhzk/2015-05-06/10739.html. Accessed 10 Jun 2016

  • Chua KB, Kasri AR (2011) Hand foot and mouth disease due to enterovirus 71 in Malaysia. Virol Sin 26:221–228. doi:10.1007/s12250-011-3195-8

    Article  Google Scholar 

  • Deng T, Huang Y, Yu S, Gu J, Huang C, Xiao G, Hao Y (2013) Spatial-temporal clusters and risk factors of hand, foot, and mouth disease at the district level in Guangdong Province, China. PLoS One 8:e56943. doi:10.1371/journal.pone.0056943

    Article  CAS  Google Scholar 

  • Ding Z et al (2015) Impact of diurnal temperature range on mortality in a high plateau area in Southwest China: a time series analysis. Sci Total Environ 526:358–365. doi:10.1016/j.scitotenv.2015.05.012

    Article  CAS  Google Scholar 

  • Duff MF (1968) Hand-foot-and-mouth syndrome in humans: coxackie A10 infections in New Zealand. Br Med J 2:661–664

    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:e87916. doi:10.1371/journal.pone.0087916

    Article  Google Scholar 

  • Gasparrini A (2011) Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 43:1–20

    Article  Google Scholar 

  • Grassly NC, Fraser C (2006) Seasonal infectious disease epidemiology. Proc Biol Sci 273:2541–2550. doi:10.1098/rspb.2006.3604

    Article  Google Scholar 

  • Guo B, Naish S, Hu W, Tong S (2015) The potential impact of climate change and ultraviolet radiation on vaccine-preventable infectious diseases and immunization service delivery system. Expert Rev Vaccines 14:561–577. doi:10.1586/14760584.2014.990387

    Article  CAS  Google Scholar 

  • He YQ et al (2013) Emergence, circulation, and spatiotemporal phylogenetic analysis of coxsackievirus a6- and coxsackievirus a10-associated hand, foot, and mouth disease infections from 2008 to 2012 in Shenzhen, China. J Clin Microbiol 51:3560–3566. doi:10.1128/JCM.01231-13

    Article  Google Scholar 

  • Hii YL, Rocklov J, Ng N (2011) Short term effects of weather on hand, foot and mouth disease. PLoS One 6:e16796. doi:10.1371/journal.pone.0016796

    Article  CAS  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. doi:10.1186/1471-2334-13-134

    Article  Google Scholar 

  • Kung YH et al (2010) Introduction of a strong temperature-sensitive phenotype into enterovirus 71 by altering an amino acid of virus 3D polymerase. Virology 396:1–9. doi:10.1016/j.virol.2009.10.017

    Article  CAS  Google Scholar 

  • Lai FF, Yan Q, Ge SX, Tang X, Chen RJ, Xu HM (2015) Epidemiologic and etiologic characteristics of hand, foot, and mouth disease in Chongqing, China between 2010 and 2013. J Med Virol. doi:10.1002/jmv.24349

    Google Scholar 

  • Lai FF, Yan Q, Ge SX, Tang X, Chen RJ, Xu HM (2016) Epidemiologic and etiologic characteristics of hand, foot, and mouth disease in Chongqing, China between 2010 and 2013. J Med Virol 88:408–416. doi:10.1002/jmv.24349

    Article  Google Scholar 

  • Lee SJ, Si J, Yun HS, Ko G (2015) Effect of temperature and relative humidity on the survival of foodborne viruses during food storage. Appl Environ Microbiol 81:2075–2081. doi:10.1128/AEM.04093-14

    Article  CAS  Google Scholar 

  • Lin H, Zou H, Wang Q, Liu C, Lang L, Hou X, Li Z (2013) Short-term effect of El Niño-Southern Oscillation on pediatric hand, foot and mouth disease in Shenzhen, China. PLoS One 8:e65585. doi:10.1371/journal.pone.0065585

    Article  CAS  Google Scholar 

  • Ma E, Lam T, Wong C, Chuang SK (2010) Is hand, foot and mouth disease associated with meteorological parameters? Epidemiol Infect 138:1779–1788. doi:10.1017/s0950268810002256

    Article  CAS  Google Scholar 

  • Minhaz Ud-Dean SM (2010) Structural explanation for the effect of humidity on persistence of airborne virus: seasonality of influenza. J Theor Biol 264:822–829. doi:10.1016/j.jtbi.2010.03.013

    Article  CAS  Google Scholar 

  • Nguyen NT et al (2014) Epidemiological and clinical characteristics of children who died from hand, foot and mouth disease in Vietnam, 2011. BMC Infect Dis 14:341. doi:10.1186/1471-2334-14-341

    Article  Google Scholar 

  • Norval M (2001) Effects of solar radiation on the human immune system. J Photochem Photobiol B 63:28–40

    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. doi:10.1016/j.scitotenv.2011.09.055

    Article  CAS  Google Scholar 

  • Sagripanti JL, Lytle CD (2007) Inactivation of influenza virus by solar radiation. Photochem Photobiol 83:1278–1282. doi:10.1111/j.1751-1097.2007.00177.x

    Article  CAS  Google Scholar 

  • Salo RJ, Cliver DO (1976) Effect of acid pH, salts, and temperature on the infectivity and physical integrity of enteroviruses. Arch Virol 52:269–282

    Article  CAS  Google Scholar 

  • Sasidharan CK, Sugathan P, Agarwal R, Khare S, Lal S, Jayaram Paniker CK (2005) Hand-foot-and-mouth disease in Calicut. Indian J Pediatr 72:17–21

    Article  CAS  Google Scholar 

  • Sattar SA, Dimock KD, Ansari SA, Springthorpe VS (1988) Spread of acute hemorrhagic conjunctivitis due to enterovirus-70: effect of air temperature and relative humidity on virus survival on fomites. J Med Virol 25:289–296

    Article  CAS  Google Scholar 

  • Song Y et al (2015) Time series analyses of hand, foot and mouth disease integrating weather variables. PLoS One 10:e0117296. doi:10.1371/journal.pone.0117296

    Article  Google Scholar 

  • Wang Y et al (2011) Hand, foot, and mouth disease in China: patterns of spread and transmissibility. Epidemiology (Cambridge, Mass) 22:781–792. doi:10.1097/EDE.0b013e318231d67a

    Article  CAS  Google Scholar 

  • Wang J, Cao Z, Zeng DD, Wang Q, Wang X, Qian H (2014) Epidemiological analysis, detection, and comparison of space-time patterns of Beijing hand-foot-mouth disease (2008–2012). PLoS One 9:e92745. doi:10.1371/journal.pone.0092745

    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:e0003572. doi:10.1371/journal.pntd.0003572

    Article  Google Scholar 

  • Wong SS, Yip CC, Lau SK, Yuen KY (2010) Human enterovirus 71 and hand, foot and mouth disease. Epidemiol Infect 138:1071–1089. doi:10.1017/S0950268809991555

    Article  CAS  Google Scholar 

  • Wood S (2006) Generalized additive models: an introduction with R, 1st edn. Chapman and Hall/CRC, Boca Raton

    Google Scholar 

  • World Health Organization Western Pacific Region (2011) A guide to clinical management and public health response for hand, foot and mouth disease (HFMD)

  • Wu H, Wang H, Wang Q, Xin Q, Lin H (2014a) The effect of meteorological factors on adolescent hand, foot, and mouth disease and associated effect modifiers. Glob Health Action 7:24664. doi:10.3402/gha.v7.24664

    Article  Google Scholar 

  • Wu X, Sun Y, Lin C, Jia L, Wu Q, Li X, Wang Q (2014b) A case-control study to identify environmental risk factors for hand, foot, and mouth disease outbreaks in Beijing. Jpn J Infect Dis 67:95–99

    Article  Google Scholar 

  • Xing W et al (2014) Hand, foot, and mouth disease in China, 2008–12: an epidemiological study. Lancet Infect Dis 14:308–318. doi:10.1016/S1473-3099(13)70342-6

    Article  Google Scholar 

  • Zhang 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. doi:10.1186/1743-422X-7-94

    Article  Google Scholar 

  • Zhang T, Du J, Xue Y, Su H, Yang F, Jin Q (2013) Epidemics and frequent recombination within species in outbreaks of human enterovirus B-associated hand, foot and mouth disease in Shandong China in 2010 and 2011. PLoS One 8:e67157. doi:10.1371/journal.pone.0067157

    Article  CAS  Google Scholar 

  • Zhu L et al (2015) The impact of ambient temperature on childhood HFMD incidence in inland and coastal area: a two-city study in Shandong Province, China. Int J Environ Res Public Health 12:8691–8704. doi:10.3390/ijerph120808691

    Article  CAS  Google Scholar 

  • Zou XN, Zhang XZ, Wang B, Qiu YT (2012) Etiologic and epidemiologic analysis of hand, foot, and mouth disease in Guangzhou city: a review of 4,753 cases. Braz J Infect Dis 16:457–465. doi:10.1016/j.bjid.2012.08.001

    Article  Google Scholar 

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Acknowledgements

We thank the Chongqing Center for Disease Control and Prevention for the provision of disease data and the China Meteorological Administration for the provision of weather data.

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Correspondence to William B. Goggins.

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This study involves human participants but is not a survey or observation of human behavior. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required. This study complies with the current laws in China.

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The authors declare that they have no conflict of interest.

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Wang, P., Zhao, H., You, F. et al. Seasonal modeling of hand, foot, and mouth disease as a function of meteorological variations in Chongqing, China. Int J Biometeorol 61, 1411–1419 (2017). https://doi.org/10.1007/s00484-017-1318-0

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  • DOI: https://doi.org/10.1007/s00484-017-1318-0

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