Environmental Science and Pollution Research

, Volume 26, Issue 18, pp 17974–17985 | Cite as

Impact of PM10 and meteorological factors on the incidence of hand, foot, and mouth disease in female children in Ningbo, China: a spatiotemporal and time-series study

  • Ruixue Huang
  • Huacheng Ning
  • Tianfeng He
  • Guolin Bian
  • Jianan HuEmail author
  • Guozhang XuEmail author
Environmental Pollution and Energy Management


Hand, foot, and mouth disease (HFMD) is a viral illness that is considered a critical public health challenge worldwide. Previous studies have demonstrated that meteorological parameters are significantly related to the incidence of HFMD in children; however, few studies have focused only on female children. This study quantified the associations of HFMD incidence with meteorological parameters and PM10 (particulate matter with an aerodynamic diameter of 10 μm) among female children. Data were collected on daily HFMD cases, meteorological variables, and PM10 levels in Ningbo, China, from January 2012 to December 2016. Data were assessed using a distributed lag nonlinear model (DLNM) with Poisson distribution. A total of 59,809 female children aged 0−15 years with HFMD were enrolled. The results showed that highest relative risk (RR) of HFMD for temperature was 3 °C and the lag effect was 3 days. The highest RR for PM10 was 80 mg/m3 and the lag effect was 5 days. Spatial analysis showed that female HFMD incidence was mainly concentrated in the suburban of Ningbo city indicating that female children in this area should be more paid attention on avoiding this disease outbreak. Our findings suggest that HFMD prevention strategies should focus more attention on local meteorological parameters.


Hand, foot, and mouth disease Female children Spatiotemporal study Incidence 


Authors’ contributions

H RX, B GL, and H TF conceived and designed the experiments; H RX, B GL, and H TF performed the experiments; H TF and HC N analyzed the data; H RX, HC N, H JA, and X GZ drafted the paper. All authors contributed to the interpretation of the analysis, reviewing the manuscript.


This study was supported by the Graduate students’ independent exploration of innovative projects, Central South University (2018zzts849), Health and Medical Science and Technology Scheme of Zhejiang Province (2014KYA202), the Science and Technology Scheme of Ningbo (2014C50027), the Science and Technology Scheme of Health and Family Planning Commission of Hunan Province (BZ2016085), supported by and the Innovation Team of Science and Technology Bureau of Ningbo (2012B82018), the Social Development Research Program of Ningbo (2014C50025), Science and Technology Innovation, Science Popularization Guidance Project of Hunan Province (2016ZK3002).

Compliance with ethical standards

Ethics approval and consent to participate

This study has been approved by the Institutional Review Board of the Ningbo Center for Disease Control. Data analyses were de-identified (number 201601).

Consent for publication

Not applicable.

Conflict of interest

The authors declare that they have no conflicts of interest.


  1. AbuBakar S, Chee HY, al-Kobaisi MF, Xiaoshan J, Bing Chua K, Kit Lam S (1999) Identification of enterovirus 71 isolates from an outbreak of hand, foot and mouth disease (HFMD) with fatal cases of encephalomyelitis in Malaysia. Virus Res 61(1):1–9CrossRefGoogle Scholar
  2. Aswathyraj S, Arunkumar G, Alidjinou EK, Hober D (2016) Hand, foot and mouth disease (HFMD): emerging epidemiology and the need for a vaccine strategy. Med Microbiol Immunol 205:397–407CrossRefGoogle Scholar
  3. Ban J, Xu D, He MZ, Sun Q, Chen C, Wang W, Zhu P, Li T (2017) The effect of high temperature on cause-specific mortality: a multi-county analysis in China. Environ Int 106:19–26CrossRefGoogle Scholar
  4. Bo YC, Song C, Wang JF, Li XW (2014) 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 14:358CrossRefGoogle Scholar
  5. Chen, G.P., et al. (2015) Epidemiological characteristics and influential factors of hand, foot and mouth disease (HFMD) reinfection in children in Anhui province. Epidemiol Infect 1–8Google Scholar
  6. Clark CM, Silverberg NB, Weinberg JM (2015) What is your diagnosis? Onychomadesis following hand-foot-and-mouth disease. Cutis 95(6):312 319-20 Google Scholar
  7. Du Z et al (2016) The threshold effects of meteorological factors on hand, foot, and mouth disease (HFMD) in China, 2011. Sci Rep 6:36351CrossRefGoogle Scholar
  8. Dwibedi B, Kar BR, Kar SK (2010) Hand, foot and mouth disease (HFMD): a newly emerging infection in Orissa, India. Natl Med J India 23(5):313Google Scholar
  9. Fujimoto T, Konagaya M, Enomoto M, Tsuboi K, Hashimoto K, Taniguchi K, Kodama T, Okabe N (2010) Novel high-speed real-time PCR method (hyper-PCR): results from its application to adenovirus diagnosis. Jpn J Infect Dis 63(1):31–35Google Scholar
  10. Gasparrini A (2011) Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 43(8):1–20CrossRefGoogle Scholar
  11. Gordian ME, Choudhury AH (2003) PM10 and asthma medication in schoolchildren. Arch Environ Health 58(1):42–47CrossRefGoogle Scholar
  12. Gui J, Liu Z, Zhang T, Hua Q, Jiang Z, Chen B, Gu H, Lv H, Dong C (2015) Epidemiological characteristics and spatial-temporal clusters of hand, foot, and mouth disease in Zhejiang Province, China, 2008-2012. PLoS One 10(9):e0139109CrossRefGoogle Scholar
  13. Guo Y, Barnett AG, Pan X, Yu W, Tong S (2011) The impact of temperature on mortality in Tianjin, China: a case-crossover design with a distributed lag nonlinear model. Environ Health Perspect 119(12):1719–1725CrossRefGoogle Scholar
  14. Hii YL, Rocklov J, Ng N (2011) Short term effects of weather on hand, foot and mouth disease. PLoS One 6(2):e16796CrossRefGoogle Scholar
  15. Howard CT, Vu PD (2015) You’re the flight surgeon: hand, foot, and mouth disease. Aerosp Med Hum Perform 86(5):497–500CrossRefGoogle Scholar
  16. Hu M, Li Z, Wang J, Jia L, Liao Y, Lai S, Guo Y, Zhao D, Yang W (2012) Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS One 7(6):e38978CrossRefGoogle Scholar
  17. Huang JX, Wang JF, Li ZJ, Wang Y, Lai SJ, Yang WZ (2015) Visualized exploratory spatiotemporal analysis of hand-foot-mouth disease in southern China. PLoS One 10(11):e0143411CrossRefGoogle Scholar
  18. Huang R, Bian G, He T, Chen L, Xu G (2016) Effects of meteorological parameters and PM10 on the incidence of hand, foot, and mouth disease in children in China. Int J Environ Res Public Health 13(5).
  19. Huang J, Liao Q, Ooi MH, Cowling BJ, Chang Z, Wu P, Liu F, Li Y, Luo L, Yu S, Yu H, Wei S (2018) Epidemiology of recurrent hand, foot and mouth disease, China, 2008–2015. Emerg Infect Dis 24(3).
  20. Jiang FC et al (2016) Meteorological factors affect the hand, foot, and mouth disease epidemic in Qingdao, China, 2007-2014. Epidemiol Infect 144(11):2354–2362CrossRefGoogle Scholar
  21. Kim JH, Lim DH, Kim JK, Jeong SJ, Son BK (2005) Effects of particulate matter (PM10) on the pulmonary function of middle-school children. J Korean Med Sci 20(1):42–45CrossRefGoogle Scholar
  22. Kim BI, Ki H, Park S, Cho E, Chun BC (2016) Effect of climatic factors on hand, foot, and mouth disease in South Korea, 2010-2013. PLoS One 11(6):e0157500CrossRefGoogle Scholar
  23. Liao Y, Ouyang R, Wang J, Xu B (2015) A study of spatiotemporal delay in hand, foot and mouth disease in response to weather variations based on SVD: a case study in Shandong Province, China. BMC Public Health 15:71CrossRefGoogle Scholar
  24. Liao J, Qin Z, Zuo Z, Yu S, Zhang J (2016) 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 563-564:152–159CrossRefGoogle Scholar
  25. Liu Y, Wang X, Pang C, Yuan Z, Li H, Xue F (2015) Spatio-temporal analysis of the relationship between climate and hand, foot, and mouth disease in Shandong province, China, 2008-2012. BMC Infect Dis 15:146CrossRefGoogle Scholar
  26. Nassef C, Ziemer C, Morrell DS (2015) Hand-foot-and-mouth disease: a new look at a classic viral rash. Curr Opin Pediatr 27(4):486–491CrossRefGoogle Scholar
  27. Ni H, Yi B, Yin J, Fang T, He T, du Y, Wang J, Zhang H, Xie L, Ding Y, Gu W, Zhang S, Han Y, Dong H, Su T, Xu G, Cao G (2012) Epidemiological and etiological characteristics of hand, foot, and mouth disease in Ningbo, China, 2008-2011. J Clin Virol 54(4):342–348CrossRefGoogle Scholar
  28. 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 410-411:119–125CrossRefGoogle Scholar
  29. Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T (2010) Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 9(11):1097–1105CrossRefGoogle Scholar
  30. Phung D, Guo Y, Thai P, Rutherford S, Wang X, Nguyen M, Do CM, Nguyen NH, Alam N, Chu C (2016) The effects of high temperature on cardiovascular admissions in the most populous tropical city in Vietnam. Environ Pollut 208(Pt A):33–39CrossRefGoogle Scholar
  31. Reyes-Zarate E et al (2016) Atmospheric particulate matter (PM10) exposure-induced cell cycle arrest and apoptosis evasion through STAT3 activation via PKCzeta and Src kinases in lung cells. Environ Pollut 214:646–656CrossRefGoogle Scholar
  32. Shi RX, Wang JF, Xu CD, Lai SJ, Yang WZ (2014) Spatiotemporal pattern of hand-foot-mouth disease in China: an analysis of empirical orthogonal functions. Public Health 128(4):367–375CrossRefGoogle Scholar
  33. Smith KR, Veranth JM, Kodavanti UP, Aust AE, Pinkerton KE (2006) Acute pulmonary and systemic effects of inhaled coal fly ash in rats: comparison to ambient environmental particles. Toxicol Sci 93(2):390–399CrossRefGoogle Scholar
  34. Smith MR, Davis RL, Phillips PA, Shvilkina T, Kaur K, Tabolt HK, Krause M, Galdi V (2017) Geographical information system evaluation and trends of nonaccidental trauma at a level I trauma center, pilot study. Ann Surg 265(2):418–423CrossRefGoogle Scholar
  35. Souza LS, Nascimento LF (2016) Air pollutants and hospital admission due to pneumonia in children: a time series analysis. Rev Assoc Med Bras 62:151–156CrossRefGoogle Scholar
  36. Wang J et al (2010) Geographical detectors-based health risk assessment and its application in the neural tube defects study of the Heshun Region, China. Int J Geogr Inf Sci 24(1):107–127CrossRefGoogle Scholar
  37. Wang JF, 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 10:25CrossRefGoogle Scholar
  38. Wang JF, Xu CD, Tong SL, Chen HY, Yang WZ (2013) Spatial dynamic patterns of hand-foot-mouth disease in the People’s Republic of China. Geospat Health 7(2):381–390CrossRefGoogle Scholar
  39. Wang C, Cao K, Zhang Y, Fang L, Li X, Xu Q, Huang F, Tao L, Guo J, Gao Q, Guo X (2016a) Different effects of meteorological factors on hand, foot and mouth disease in various climates: a spatial panel data model analysis. BMC Infect Dis 16(1):233CrossRefGoogle Scholar
  40. Wang J, Zhang T, Fu B (2016b) A measure of spatial stratified heterogeneity. Ecol Indic 67:250–256CrossRefGoogle Scholar
  41. Wu X, Sun Y, Lin C, Jia L, Wu Q, Li X, Wang Q (2014) A case-control study to identify environmental risk factors for hand, foot, and mouth disease outbreaks in Beijing. Jpn J Infect Dis 67(2):95–99CrossRefGoogle Scholar
  42. Wu J, Cheng J, Xu Z, Zhao K, Zhao D, Xie M, Yang H, Wen L, Li K, Su H (2016) Nonlinear and interactive effects of temperature and humidity on childhood hand, foot and mouth disease in Hefei, China. Pediatr Infect Dis J 35(10):1086–1091CrossRefGoogle Scholar
  43. Wu X et al (2017) Spatio-temporal clustering analysis and its determinants of hand, foot and mouth disease in Hunan, China, 2009–2015. BMC Infect Dis 17(1):645CrossRefGoogle Scholar
  44. Xu CD, Xiao GX (2017) Spatiotemporal risk mapping of hand, foot and mouth disease and its association with meteorological variables in children under 5 years. Epidemiol Infect 145(14):2912–2920CrossRefGoogle Scholar
  45. 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):e0126171CrossRefGoogle Scholar
  46. Xu J, Zhao D, Su H, Xie M, Cheng J, Wang X, Li K, Yang H, Wen L, Wang B (2016) Impact of temperature variability on childhood hand, foot and mouth disease in Huainan, China. Public Health 134:86–94CrossRefGoogle Scholar
  47. Yang H, Wu J, Cheng J, Wang X, Wen L, Li K, Su H (2017) Is high relative humidity associated with childhood hand, foot, and mouth disease in rural and urban areas? Public Health 142:201–207CrossRefGoogle Scholar
  48. Ye Q, Fu JF, Mao JH, Shen HQ, Chen XJ, Shao WX, Shang SQ, Wu YF (2016) Haze is an important medium for the spread of rotavirus. Environ Pollut 216:324–331CrossRefGoogle Scholar
  49. 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 6:27305CrossRefGoogle Scholar
  50. Zha J, Ma Z (2015) Epidemiological and genetic analysis concerning the coxsackievirus A6 related endemic outbreak of hand-foot-mouth disease in Taizhou, China, during 2013. J Med Virol 87(12):2000–2008CrossRefGoogle Scholar
  51. Zhang Y, Zhu Z, Yang W, Ren J, Tan X, Wang Y, Mao N, Xu S, Zhu S, Cui A, Zhang Y, Yan D, Li Q, Dong X, Zhang J, Zhao Y, Wan J, Feng Z, Sun J, Wang S, Li D, Xu W (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 7:94CrossRefGoogle Scholar
  52. Zhang W, du Z, Zhang D, Yu S, Hao Y (2016) Boosted regression tree model-based assessment of the impacts of meteorological drivers of hand, foot and mouth disease in Guangdong, China. Sci Total Environ 553:366–371CrossRefGoogle Scholar
  53. Zhang D et al (2017) Enterovirus 71 neutralizing antibodies Seroepidemiological research among children in Guangzhou, China between 2014 and 2015: a cross-sectional study. Int J Environ Res Public Health 14(3)Google Scholar
  54. Zhou L et al (2015) Clinical feature of severe hand, foot and mouth disease with acute pulmonary edema in pediatric patients. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue 27(7):563–567Google Scholar
  55. Zhu FC, Liang ZL, Meng FY, Zeng Y, Mao QY, Chu K, Song XF, Yao X, Li JX, Ji H, Zhang YJ, Li L, Pan HX, Xu K, Dai WM, Zhang WW, Deng F, Wang H, Wang JZ (2012) Retrospective study of the incidence of HFMD and seroepidemiology of antibodies against EV71 and CoxA16 in prenatal women and their infants. PLoS One 7(5):e37206CrossRefGoogle Scholar
  56. Zhu L, Yuan Z, Wang X, Li J, Wang L, Liu Y, Xue F, Liu Y (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(8):8691–8704CrossRefGoogle Scholar
  57. Zhu L, Wang X, Guo Y, Xu J, Xue F, Liu Y (2016) Assessment of temperature effect on childhood hand, foot and mouth disease incidence (0-5years) and associated effect modifiers: a 17 cities study in Shandong Province, China, 2007-2012. Sci Total Environ 551-552:452–459CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Occupational and Environmental Health, Xiangya School of Public HealthCentral South UniversityChangshaChina
  2. 2.Ningbo Municipal Center for Disease Control and PreventionNingboChina

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