Abstract
Hand, foot, and mouth disease (HFMD) poses a great disease burden in China. However, there are few studies on the relationship between temperature variability (TV) and HFMD. Moreover, whether air pollutions have modified effects on this relationship is still unknown. Therefore, this study aims to explore the modified effects of air pollutants on TV-HFMD association in Zibo City, China. Daily data of HFMD cases, meteorological factors, and air pollutants from 2015 to 2019 were collected for Zibo City. TV was estimated by calculating standard deviation of minimum and maximum temperatures over the exposure days. We used generalized additive model to estimate the association between TV and HFMD. The modified effects of air pollutants were assessed by comparing the estimated TV-HFMD associations between different air stratums. We found that TV increased the risk of HFMD. The effect was strongest at TV03 (4 days of exposure), when the incidence of HFMD increased by 3.6% [95% CI: 1.3–5.9%] for every 1℃ increases in TV. Males, children aged 0–4 years, were more sensitive to TV. We found that sulfur dioxide (SO2) enhanced TV’s effects on all considered exposure days, while ozone (O3) reduced TV’s effects on some exposure days in whole concerned population. However, we did not detect significant effect modification by particulate matter less than 10 microns in aerodynamic diameter (PM10). These findings are of significance in developing policies and public health practices to reduce the risks of HFMD by integrating changes in temperatures and air pollutants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
References
Alahmad B, Khraishah H, Shakarchi AF et al (2020) Cardiovascular mortality and exposure to heat in an inherently hot region: implications for climate change. Circulation 141:1271–1273. https://doi.org/10.1161/CIRCULATIONAHA.119.044860
Carder M, McNamee R, Beverland I et al (2005) The lagged effect of cold temperature and wind chill on cardiorespiratory mortality in Scotland. Occup Environ Med 62:702–710. https://doi.org/10.1136/oem.2004.016394
CDC (2021)The Data-center of China Public Health Science. http://www.phsciencedata.cn/Share/en/index.jsp. Accessed 6 Jan 2021
Cheng J, Zhu R, Xu Z et al (2016) 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. https://doi.org/10.1007/s00484-015-1082-y
Cheng Q, Bai L, Zhang Y et al (2018) Ambient temperature, humidity and hand, foot, and mouth disease: a systematic review and meta-analysis. Sci Total Environ 625:828–836. https://doi.org/10.1016/j.scitotenv.2018.01.006
Coates SJ, Davis MDP, Andersen LK (2019) Temperature and humidity affect the incidence of hand, foot, and mouth disease: a systematic review of the literature – a report from the International Society of Dermatology Climate Change Committee. Int J Dermatol 58:388–399. https://doi.org/10.1111/ijd.14188
Cohen AJ, Brauer M, Burnett R et al (2017) Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: an analysis of data from the Global Burden of Diseases Study 2015. Lancet 389:1907–1918. https://doi.org/10.1016/S0140-6736(17)30505-6
Cox B, Levent F (2018) Hand, foot, and mouth disease. JAMA 320:2492. https://doi.org/10.1001/jama.2018.17288
Du Z, Lawrence WR, Zhang W 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. https://doi.org/10.1016/j.scitotenv.2018.11.391
Fan C, Liu F, Zhao X et al (2020) An alternative comprehensive index to quantify the interactive effect of temperature and relative humidity on hand, foot and mouth disease: a two-stage time series study including 143 cities in mainland China. Sci Total Environ 740:140106. https://doi.org/10.1016/j.scitotenv.2020.140106
Fu X, Wan Z, Li Y et al (2020) National epidemiology and evolutionary history of four hand, foot and mouth disease-related enteroviruses in China from 2008 to 2016. Virol Sin 35:21–33. https://doi.org/10.1007/s12250-019-00169-2
Gonzalez G, Carr MJ, Kobayashi M et al (2019) Enterovirus-associated hand-foot and mouth disease and neurological complications in japan and the rest of the world. Int J Mol Sci 20:5201. https://doi.org/10.3390/ijms20205201
Guo Y, Gasparrini A, Armstrong BG et al (2016) Temperature variability and mortality: a multi-country study. Environ Health Perspect 124:1554–1559. https://doi.org/10.1289/EHP149
He X, Dong S, Li L et al (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 Negl Trop Dis 14:e0008085. https://doi.org/10.1371/journal.pntd.0008085
Hiatt RA, Beyeler N (2020) Cancer and climate change. Lancet Oncol 21:e519–e527. https://doi.org/10.1016/S1470-2045(20)30448-4
Huang R, Ning H, He T 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. https://doi.org/10.1007/s11356-018-2619-5
Jiang M, Wei D, Ou W-L et al (2012) Autopsy findings in children with hand, foot, and mouth disease. N Engl J Med 367:91–92. https://doi.org/10.1056/nejmc1110981
Koh WM, Badaruddin H, La H et al (2018) Severity and burden of hand, foot and mouth disease in Asia: a modelling study. BMJ Glob Heal 3:e000442. https://doi.org/10.1136/bmjgh-2017-000442
Li Y, Zhang J, Zhang X (2014) Modeling and preventive measures of hand, foot and mouth disease (HFMD) in China. Int J Environ Res Public Health 11:3108–3117. https://doi.org/10.3390/ijerph110303108
Lin YC, Wu SC (2006) Effects of ozone exposure on inactivation of intra- and extracellular enterovirus 71. Antiviral Res 70:147–153. https://doi.org/10.1016/j.antiviral.2005.12.007
Lin YC, Juan HC, Cheng YC (2007) Ozone exposure in the culture medium inhibits enterovirus 71 virus replication and modulates cytokine production in rhabdomyosarcoma cells. Antiviral Res 76:241–251. https://doi.org/10.1016/j.antiviral.2007.07.004
Luo K, Li R, Wang Z et al (2017) Effect modification of the association between temperature variability and daily cardiovascular mortality by air pollutants in three Chinese cities. Environ Pollut 230:989–999. https://doi.org/10.1016/j.envpol.2017.07.045
Medlock JM, Leach SA (2015) Effect of climate change on vector-borne disease risk in the UK. Lancet Infect Dis 15:721–730. https://doi.org/10.1016/S1473-3099(15)70091-5
Messacar K, Spence-Davizon E, Osborne C et al (2020) Clinical characteristics of enterovirus A71 neurological disease during an outbreak in children in Colorado, USA, in 2018: an observational cohort study. Lancet Infect Dis 20:230–239. https://doi.org/10.1016/S1473-3099(19)30632-2
Owino CO, Chu JJH (2019) Recent advances on the role of host factors during non-poliovirus enteroviral infections. J Biomed Sci 26:47. https://doi.org/10.1186/s12929-019-0540-y
Pearson D, Basu R, Wu X (May), Ebisu K (2020) Temperature and hand, foot and mouth disease in California: an exploratory analysis of emergency department visits by season, 2005–2013. Environ Res 185:109461. https://doi.org/10.1016/j.envres.2020.109461
Rocklöv J, Dubrow R (2020) Climate change: an enduring challenge for vector-borne disease prevention and control. Nat Immunol 21:479–483. https://doi.org/10.1038/s41590-020-0648-y
Salas RN, Malina D, Solomon CG (2019) Prioritizing health in a changing climate. N Engl J Med 381:773–774. https://doi.org/10.1056/nejme1909957
Schmidt CW (2018) More cases of hand, foot, and mouth disease in China: a consequence of climate change? Environ Health Perspect 126:094002. https://doi.org/10.1289/EHP3778
Semenza JC (2020) Cascading risks of waterborne diseases from climate change. Nat Immunol 21:484–487. https://doi.org/10.1038/s41590-020-0631-7
Shao P, Wu X, Li H et al (2017) Clinical significance of inflammatory cytokine and chemokine expression in hand, foot and mouth disease. Mol Med Rep 15:2859–2866. https://doi.org/10.3892/mmr.2017.6324
Tan YW, Chu JJH (2020) Protecting the most vulnerable from hand, foot, and mouth disease. Lancet Infect Dis 3099:30452–30457. https://doi.org/10.1016/S1473-3099(20)30452-7
Watts N, Adger WN, Ayeb-Karlsson S et al (2017) The Lancet Countdown: tracking progress on health and climate change. Lancet 389:1151–1164. https://doi.org/10.1016/S0140-6736(16)32124-9
Wei Q, Wu J, Zhang Y 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. https://doi.org/10.1016/j.scitotenv.2018.11.481
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. https://doi.org/10.1016/j.tox.2016.08.018
Xu J, Zhao D, Su H et al (2016) Impact of temperature variability on childhood hand, foot and mouth disease in Huainan, China. Public Health 134:86–94. https://doi.org/10.1016/j.puhe.2015.10.029
Yin F, Ma Y, Zhao X et al (2017) The association between diurnal temperature range and childhood hand, foot, and mouth disease: a distributed lag non-linear analysis. Epidemiol Infect 145:3264–3273. https://doi.org/10.1017/S0950268817002321
Yu G, Li Y, Cai J et al (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. https://doi.org/10.1016/j.scitotenv.2018.07.329
Zeka A, Zanobetti A, Schwartz J (2006) Individual-level modifiers of the effects of particulate matter on daily mortality. Am J Epidemiol 163:849–859. https://doi.org/10.1093/aje/kwj116
Zhu L, Yuan Z, Wang X 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. https://doi.org/10.3390/ijerph120808691
Funding
This work was supported by the National Key Research and Development Program of China (grant numbers: 2019YFC1200500, 2019YFC1200502); General Administration of Customs, P.R. China [grant number: 2019HK125]; and National Natural Science Foundation of China [grant number: 81673238]. The funding agencies had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.
Author information
Authors and Affiliations
Contributions
CYL: Conceptualization, formal analysis, validation, writing, and editing. YCZ: Formal analysis and validation. KLS: Formal analysis and validation. YJ: Formal analysis and validation. TXL: Formal analysis and validation. CH: Formal analysis and validation. QDF: Formal analysis and validation. CLC: Formal analysis and validation. LYH: Formal analysis and validation. YL: Formal analysis and validation. YZ: Supervision, writing (review), and editing. XJL: Conceptualization, validation, funding acquisition, supervision, writing (review), and editing. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
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
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, C., Zhu, Y., She, K. et al. Modified effects of air pollutants on the relationship between temperature variability and hand, foot, and mouth disease in Zibo City, China. Environ Sci Pollut Res 29, 44573–44581 (2022). https://doi.org/10.1007/s11356-022-18817-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-18817-8