Abstract
The influence of weather and air pollution factors on hand, foot, and mouth disease (HFMD) has received widespread attention. However, most of the existing studies came from lightly polluted areas and the results were inconsistent. There was a lack of relevant evidence of heavily polluted areas. This study aims to quantify the relationship between weather factors and air pollution with HFMD in heavily polluted areas. We collected the daily number of hand, foot, and mouth disease in Shijiazhuang, China from 2014 to 2018, as well as meteorological and air pollutant data over the same period. The generalized linear model combined with the distributed lag model was used to study the effect of meteorological factors and air pollutants on the daily cases of HFMD and its hysteresis effect. We found that the dose-response relationship between temperature, PM2.5, and the risk of hand-foot-mouth disease was non-linear. Both low temperature and high temperature increased the risk of hand-foot-mouth disease. The cumulative effect of high temperature reached the maximum at 0–10 lag days, and the cumulative effect of low temperature reached the maximum at 0–3 lag days. The concentration of PM2.5 between 76 and 200 μg/m3 has a certain risk of the onset of hand, foot, and mouth disease, but the extreme PM2.5 concentration has a certain protective effect. In addition, low humidity, low wind speed, and low-O3 can increase the risk of HFMD. Risks of humidity and low concentration of O3 increased as lag days extended. In conclusion, our study found that climate factors and air pollutants exert varying degrees of impact on HFMD. Our research provided the scientific basis for establishing an early warning system so that medical staff and parents can take corresponding measures to prevent HFMD.
Similar content being viewed by others
Data availability
Our data are not public. The data come from Shijiazhuang CDC, please contact the corresponding unit if necessary. The data can be accessed from the Shijiazhuang CDC and Department of Hebei Environmental Protection with permission via direct request.
Abbreviations
- HFMD:
-
hand foot mouth disease
- DLNM:
-
distributed lag nonlinear model
- CI:
-
confidence interval
- RR:
-
relative risk
- NO2 :
-
nitrogen dioxide
- PM2.5 :
-
particulate matter with aerodynamic diameter of ≤2.5 μm
- PM10 :
-
particulate matter with aerodynamic diameter of ≤10 μm
- SO2 :
-
sulfur dioxide
- O3 :
-
ozone
References
Abad FX, Pintó RM, Bosch A (1994) Survival of enteric viruses on environmental fomites. Appl Environ Microbiol 60:3704–3710
Akey DH, Walton TE (1985)Liquid-phase study of ozone inactivation of Venezuelan equine encephalomyelitis virus. Appl Environ Microbiol 50:882–886
Ang LW et al (2009) Epidemiology and control of hand, foot and mouth disease in Singapore, 2001-2007. Ann Acad Med Singapore 38:106–112
Beamish LA, Osornio-Vargas AR, Wine E (2011) Air pollution: an environmental factor contributing to intestinal disease. Journal of Crohn's and Colitis. 5:279–286
Bélanger M, Gray-Donald K, O'loughlin J, Paradis G, Hanley J (2009) Influence of weather conditions and season on physical activity in adolescents. Ann Epidemiol 19:180–186
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:R81–R86
Bo Z, Ma Y, Chang Z, Zhang T, Liu F, Zhao X, Long L, Yi X, Xiao X, Li Z (2020) The spatial heterogeneity of the associations between relative humidity and pediatric hand, foot and mouth disease: evidence from a nation-wide multicity study from mainland China. Sci Total Environ 707:136103
Cai Y, Jiang L, Shi Y (2012) Survey on enterovirus 71 survival ability on different surfaces under different climate. Chin J Infect Dis:398–401 (in Chinese)
Chang HL et al (2012) The association between enterovirus 71 infections and meteorological parameters in Taiwan. PLoS ONE. 7:e46845
Chen G, Zhang W, Li S, Williams G, Liu C, Morgan GG, Jaakkola JJK, Guo Y (2017) Is short-term exposure to ambient fine particles associated with measles incidence in China?. A multi-city study. Environ Res 156:306–311
Chen J, Lv M, Yao W, Chen R, Lai H, Tong C, Fu W, Zhang W, Wang C (2020) Association between fine particulate matter air pollution and acute aortic dissections: a time-series study in Shanghai, China. Chemosphere. 243:125357
Cheng Y, Kan H (2012) Effect of the interaction between outdoor air pollution and extreme temperature on daily mortality in Shanghai, China. J Epidemiol 22:28–36
Cheng J, Wu J, Xu Z, Zhu R, Wang X, Li K, Wen L, Yang H, Su H (2014) Associations between extreme precipitation and childhood hand, foot and mouth disease in urban and rural areas in Hefei, China. Sci Total Environ 497-498:484–490
Cheng Q, Bai L, Zhang Y, Zhang H, Wang S, Xie M, Zhao D, Su H (2018) Ambient temperature, humidity and hand, foot, and mouth disease: a systematic review and meta-analysis. Sci Total Environ 625:828–836
Chua KB, Kasri AR (2011) Hand foot and mouth disease due to enterovirus 71 in Malaysia. Virol Sin 26:221–228
Cox B, Levent F (2018) Hand, foot, and mouth disease. JAMA. 320:2492
Dong W, Li X’, Yang P, Liao H, Wang X, Wang Q (2016) The effects of weather factors on hand, foot and mouth disease in Beijing. Sci Rep 6:36351
Du Z et al (2019) Interactions between climate factors and air pollution on daily HFMD cases: a time series study in Guangdong, China. Sci Total Environ 656:1358–1364
Fong TT, Lipp EK (2005) Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol Rev. 69:357–371
Gasparrini A (2011) Distributed lag linear and non-linear models in R: the package dlnm., Vol. 43. Foundation for Open Access Statistics, United States, pp 1-20
Gu S, Li D, Lu B, Huang R, Xu G (2020) Associations between ambient air pollution and daily incidence of pediatric hand, foot and mouth disease in Ningbo, 2014-2016: a distributed lag nonlinear model. Epidemiol Infect 148:e46
Halmerbauer G et al (1997) Monitoring of disease activity by measurement of inflammatory markers in atopic dermatitis in childhood. Allergy. 52:765–769
Hammond GW, Raddatz RL, Gelskey DE (1989) Impact of atmospheric dispersion and transport of viral aerosols on the epidemiology of influenza. Rev Infect Dis. 11:494–497
Hao J, Yang Z, Yang W, Huang S, Tian L, Zhu Z, Lu Y, Xiang H, Liu S (2020) Impact of ambient temperature and relative humidity on the incidence of hand-foot-mouth disease in Wuhan, China. Int J Environ Res Public Health 17
He X, Dong S, Li L, Liu X, Wu Y, Zhang Z, Mei S (2020) Using a Bayesian spatiotemporal model to identify the influencing factors and high-risk areas of hand, foot and mouth disease (HFMD) in Shenzhen. PLOS Neglected Tropical Diseases. 14:e0008085
Hu W, Li Y, Han W, Xue L, Zhang W, Ma W, Bi P (2018) Meteorological factors and the incidence of mumps in Fujian Province, China, 2005–2013: Non-linear effects. Sci Total Environ 619-620:1286–1298
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
Huang R et al (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 13:481
Huang R et al (2019) 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. Environ Sci Pollut Res 26:17974–17985
Huang J, Li J, Yin P, Wang L, Pan X, Zhou M, Li G (2021) Ambient nitrogen dioxide and years of life lost from chronic obstructive pulmonary disease in the elderly: a multicity study in China. Chemosphere. 275:130041
Huss-Marp J, Eberlein-Konig B, Breuer K, Mair S, Ansel A, Darsow U, Kramer U, Mayer E, Ring J, Behrendt H (2006) Influence of short-term exposure to airborne Der p 1 and volatile organic compounds on skin barrier function and dermal blood flow in patients with atopic eczema and healthy individuals. Clin Exp Allergy 36:338–345
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:e35108
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. 20:42–45
Kimmis BD, Downing C, Tyring S (2018)Hand-foot-and-mouth disease caused by coxsackievirus A6 on the rise. Cutis. 102:353–356
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. 15:71
Lin Y et al (2007) Ozone exposure in the culture medium inhibits enterovirus 71 virus replication and modulates cytokine production in rhabdomyosarcoma cells. Antiviral Research. 76:241–251
Liu S et al (2015) Comparative epidemiology and virology of fatal and nonfatal cases of hand, foot and mouth disease in mainland China from 2008 to 2014. Rev Med Virol 25:115–128
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
Patel D, Shibata T, Wilson J, Maidin A (2016) Challenges in evaluating PM concentration levels, commuting exposure, and mask efficacy in reducing PM exposure in growing, urban communities in a developing country. Sci Total Environ. 543:416–424
Qi H, Chen Y, Xu D, Su H, Zhan L, Xu Z, Huang Y, He Q, Hu Y, Lynn H, Zhang Z (2018) Impact of meteorological factors on the incidence of childhood hand, foot, and mouth disease (HFMD) analyzed by DLNMs-based time series approach. Infect Dis Poverty 7:7
Qu F, Liu F, Zhang H, Chao L, Guan J, Li R, Yu F, Yan X (2019) The hospitalization attributable burden of acute exacerbations of chronic obstructive pulmonary disease due to ambient air pollution in Shijiazhuang, China. Environ Sci Pollut Res 26:30866–30875
Rajtar B, Majek M, Polański Ł, Polz-Dacewicz M (2008) Enteroviruses in water environment--a potential threat to public health. Ann Agric Environ Med. 15:199–203
Ruan Z, Qian Z(M), Xu Y, Yang Y, Zhang S, Hang J, Howard S, Acharya BK, Jansson DR, Li H, Sun X, Xu X, Lin H (2020) How longer can people live by achieving the daily ambient fine particulate pollution standards in the Pearl River Delta region, China? Chemosphere. 254:126853
Rzeżutka A, Cook N (2004) Survival of human enteric viruses in the environment and food. FEMS Microbiol Rev 28:441–453
Shi W, Sun Q, du P, Tang S, Chen C, Sun Z, Wang J, Li T, Shi X (2020) Modification effects of temperature on the ozone–mortality relationship: a nationwide multicounty study in China. Environ Sci Technol 54:2859–2868
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. 93:390–399
Sumi A et al (2017) Association between meteorological factors and reported cases of hand, foot, and mouth disease from 2000 to 2015 in Japan. Epidemiol Infect 145:2896–2911
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 52:189–197
Tian S, Pan Y, Liu Z, Wen T, Wang Y (2014)Size-resolved aerosol chemical analysis of extreme haze pollution events during early 2013 in urban Beijing, China. J Hazard Mater 279:452–460
Tian L, Liang F, Xu M, Jia L, Pan X, Clements ACA (2018)Spatio-temporal analysis of the relationship between meteorological factors and hand-foot-mouth disease in Beijing, China. BMC Infect Dis 18:158
Ver HJ, Boveng PL (2007)Quasi-Poisson vs. negative binomial regression: how should we model overdispersed count data? Ecology. 88:2766–2772
Wang P, Goggins WB, Chan EYY (2016) Hand, foot and mouth disease in Hong Kong: a time-series analysis on its relationship with weather. PLoS ONE. 11:e0161006
Wang J et al (2018) Epidemiological and serological surveillance of hand-foot-and-mouth disease in Shanghai, China, 2012–2016. Emerg Microb Infect 7:1–12
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 Neglected Tropical Diseases. 9:e0003572
Wei Q et al (2019)Short-term exposure to sulfur dioxide and the risk of childhood hand, foot, and mouth disease during different seasons in Hefei, China. Sci Total Environ 658:116–121
Wigenstam E, Elfsmark L, Bucht A, Jonasson S (2016) Inhaled sulfur dioxide causes pulmonary and systemic inflammation leading to fibrotic respiratory disease in a rat model of chemical-induced lung injury. Toxicology. 368-369:28–36
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. 67:95–99
Xiao X, Gasparrini A, Huang J, Liao QH, Liu FF, Yin F, Yu HJ, Li XS (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
Xing W, Liao Q, Viboud C, Zhang J, Sun J, Wu JT, Chang Z, Liu F, Fang VJ, Zheng Y, Cowling BJ, Varma JK, Farrar JJ, Leung GM, Yu H (2014) Hand, foot, and mouth disease in China, 2008-12: an epidemiological study. Lancet Infect Dis. 14:308–318
Xu M, Su L, Cao L, Zhong H, Dong N, Dong Z, Xu J (2015) Genotypes of the enterovirus causing hand, foot and mouth disease in Shanghai, China, 2012-2013. PLoS ONE. 10:e0138514
Yang Z, Zhang Q, Cowling BJ, Lau EHY (2017) Estimating the incubation period of hand, foot and mouth disease for children in different age groups. Sci Rep 7
Yang S, Ma YL, Duan FK, He KB, Wang LT, Wei Z, Zhu LD, Ma T, Li H, Ye SQ (2018a) Characteristics and formation of typical winter haze in Handan, one of the most polluted cities in China. Sci Total Environ 613-614:1367–1375
Yang Y, You E, Wu J, Zhang W, Jin J, Zhou M, Jiang C, Huang F (2018b) Effects of relative humidity on childhood hand, foot, and mouth disease reinfection in Hefei, China. Sci Total Environ 630:820–826
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. 216:324–331
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
Yu G, Li Y, Cai J, Yu D, Tang J, Zhai W, Wei Y, Chen S, Chen Q, Qin J (2019)Short-term effects of meteorological factors and air pollution on childhood hand-foot-mouth disease in Guilin, China. Sci Total Environ 646:460–470
Zhang K (2018) Time Series Analysis of PM2.5 Impacts on years of life lost in Chengdu cardiovascular disease patients by DLNM. Chinese Center for Disease Control and Prevention
Zhang Q, Crooks R (2012) Toward an environmentally sustainable future: country environmental analysis of the People's Republic of China. © Asian Development Bank
Zhang Y, Tan XJ, Wang HY, Yan DM, Zhu SL, Wang DY, Ji F, Wang XJ, Gao YJ, Chen L, An HQ, Li DX, Wang SW, Xu AQ, Wang ZJ, Xu WB (2009) An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J Clin Virol 44:262–267
Zhang Q, Sun S, Sui X, Ding L, Yang M, Li C, Zhang C, Zhang X, Hao J, Xu Y, Lin S, Ding R, Cao J (2021) Associations between weekly air pollution exposure and congenital heart disease. Sci Total Environ 757:143821
Zhao S, Yu Y, Yin D, He J, Liu N, Qu J, Xiao J (2016) Annual and diurnal variations of gaseous and particulate pollutants in 31 provincial capital cities based on in situ air quality monitoring data from China National Environmental Monitoring Center. Environ Int 86:92–106
Zhuang ZC, Kou ZQ, Bai YJ, Cong X, Wang LH, Li C, Zhao L, Yu XJ, Wang ZY, Wen HL (2015) Epidemiological research on hand, foot, and mouth disease in Mainland China. Viruses. 7:6400–6411
Author information
Authors and Affiliations
Contributions
Xiaolin Zhang, Weiheng Guo, and Shiyong Zhang designed the study; Jianning Cai, Shiyong Zhang, and Wenjuan Wang collected the data; Shiyong Zhang and Ning Ma checked the data; Ran Liu and Jianning Cai collated the data; Ran Liu, Lina Yan, and Wei Guo analyzed data; Ran Liu drafted the original manuscript; Weiheng Guo and Xiaolin Zhang helped revise the manuscript.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
This study has been approved by the ethics committee of the Shijiazhuang Center for Disease Control (202006). The data of this study do not involve any personal information. Private information has been erased before research.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 178 kb)
Rights and permissions
About this article
Cite this article
Liu, ., Cai, J., Guo, W. et al. Effects of temperature and PM2.5 on the incidence of hand, foot, and mouth in a heavily polluted area, Shijiazhuang, China. Environ Sci Pollut Res 29, 11801–11814 (2022). https://doi.org/10.1007/s11356-021-16397-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16397-7