Spatiotemporal Distribution of Hand, Foot, and Mouth Disease and the Influence of Air Pollutants and Socioeconomic Factors on Incidence in Fujian, China
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Area
2.2. Data Collection
2.3. Statistical Analysis
2.3.1. Spatial Autocorrelation Analysis
2.3.2. Generalized Additive Model (GAM)
3. Results
3.1. Epidemiological Trends of HFMD in Fujian in 2014–2023
3.2. Spatial Clustering of HFMD
3.3. Effects of Environmental and Socioeconomic Determinants on HFMD Risk
4. Discussion
Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Brouwer, L.; Moreni, G.; Wolthers, K.C.; Pajkrt, D. Worldwide prevalence and genotype distribution of enteroviruses. Viruses 2021, 13, 434. [Google Scholar] [CrossRef] [PubMed]
- Zhu, P.; Ji, W.; Li, D.; Li, Z.; Chen, Y.; Dai, B.; Han, S.; Chen, S.; Jin, Y.; Duan, G. Current status of hand-foot-and-mouth disease. J. Biomed. Sci. 2023, 30, 15. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, G.; Carr, M.J.; Kobayashi, M.; Hanaoka, N.; Fujimoto, T. Enterovirus-associated hand-foot and mouth disease and neurological complications in Japan and the rest of the world. Int. J. Mol. Sci. 2019, 20, 5201. [Google Scholar] [CrossRef] [PubMed]
- Puenpa, J.; Wanlapakorn, N.; Vongpunsawad, S.; Poovorawan, Y. The history of enterovirus A71 outbreaks and molecular epidemiology in the Asia-Pacific region. J. Biomed. Sci. 2019, 26, 75. [Google Scholar] [CrossRef]
- Sabanathan, S.; Tan le, V.; Thwaites, L.; Wills, B.; Qui, P.T.; Van Doorn, H.R. Enterovirus 71 related severe hand, foot and mouth disease outbreaks in South-East Asia: Current situation and ongoing challenges. J. Epidemiol. Community Health 2014, 68, 500–502. [Google Scholar] [CrossRef]
- Han, Y.; Ji, H.; Shen, W.; Duan, C.; Cui, T.; Chen, L.; Hang, H.; Zhang, Z.; Sun, H.; Zhang, X.; et al. Disease burden in patients with severe hand, foot, and mouth disease in Jiangsu Province: A cross-sectional study. Hum. Vaccin. Immunother. 2022, 18, 2049168. [Google Scholar] [CrossRef]
- Pallansch, M.; Roos, R. Enterovirus: Polioviruses, Coxsackieviruses, Echoviruses and Newer Enteroviruses. In Virology, 4th ed.; Knipe, D., Howley, P., Griffin, D., Eds.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; pp. 839–893. [Google Scholar]
- Wang, X.; Wei, H.X.; Jia, L.; Huo, D.; Wang, H.Q.; Wang, Q.Y. Study on the economic burden of hand, foot and mouth disease in China. Chin. J. Epidemiol. 2020, 41, 273–279. (In Chinese) [Google Scholar]
- Available online: https://www.who.int/zh/news/item/04-04-2022-billions-of-people-still-breathe-unhealthy-air-new-who-data (accessed on 25 February 2025).
- Global Health Data Exchange. Global Burden of Disease Study 2021 (GBD 2021); Institute for Health Metrics and Evaluation: Seattle, WA, USA, 2021. [Google Scholar]
- State of Global Air. State of Global Air (SoGA) 2024; Institute for Health Metrics and Evaluation: Seattle, WA, USA, 2024. [Google Scholar]
- Peng, H.; Chen, Z.; Cai, L.; Liao, J.; Zheng, K.; Li, S.; Ren, X.; Duan, X.; Tang, X.; Wang, X.; et al. Relationship between meteorological factors, air pollutants and hand, foot and mouth disease from 2014 to 2020. BMC Public Health 2022, 22, 998. [Google Scholar] [CrossRef]
- Zhong, R.; Wu, Y.; Cai, Y.; Wang, R.; Zheng, J.; Lin, D.; Wu, H.; Li, Y. Forecasting hand, foot, and mouth disease in Shenzhen based on daily level clinical data and multiple environmental factors. Biosci. Trends 2018, 12, 450–455. [Google Scholar] [CrossRef]
- Yu, G.; Li, Y.; Cai, J.; Yu, D.; Tang, J.; Zhai, W.; Wei, Y.; Chen, S.; Chen, Q.; Qin, J. Short-term effects of meteorological factors and air pollution on childhood hand-foot-mouth disease in Guilin, China. Sci. Total Environ. 2019, 646, 460–470. [Google Scholar] [CrossRef]
- Huang, R.; Bian, G.; He, T.; Chen, L.; Xu, G. 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 2016, 13, 481. [Google Scholar] [CrossRef] [PubMed]
- Huang, R.; Ning, H.; He, T.; Bian, G.; Hu, J.; Xu, G. 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. Int. 2019, 26, 17974–17985. [Google Scholar] [CrossRef] [PubMed]
- Phung, D.; Nguyen, H.X.; Nguyen, H.L.T.; Do, C.M.; Tran, Q.D.; Chu, C. Spatiotemporal variation of hand-foot-mouth disease in relation to socioecological factors: A multiple-province analysis in Vietnam. Sci. Total Environ. 2018, 610–611, 983–991. [Google Scholar] [CrossRef]
- Jiang, X.; Ma, Y.; Lv, Q.; Liu, Y.; Zhang, T.; Yin, F.; Shui, T. Influence of social and meteorological factors on hand, foot, and mouth disease in Sichuan Province. BMC Public Health 2023, 23, 849. [Google Scholar] [CrossRef]
- Hu, M.; Li, Z.; Wang, J.; Jia, L.; Liao, Y.; Lai, S.; Guo, Y.; Zhao, D.; Yang, W.; Colizza, V. Determinants of the incidence of hand, foot and mouth disease in China using geographically weighted regression models. PLoS ONE 2012, 7, e38978. [Google Scholar] [CrossRef]
- Li, C.H.; Mao, J.J.; Wu, Y.J.; Zhang, B.; Zhuang, X.; Qin, G.; Liu, H.M. Combined impacts of environmental and socioeconomic covariates on HFMD risk in China: A spatiotemporal heterogeneous perspective. PLoS Negl. Trop. Dis. 2023, 17, e0011286. [Google Scholar] [CrossRef]
- Gou, F.; Liu, X.; Ren, X.; Liu, D.; Liu, H.; Wei, K.; Yang, X.; Cheng, Y.; Zheng, Y.; Jiang, X.; et al. Socio-ecological factors and hand, foot and mouth disease in dry climate regions: A Bayesian spatial approach in Gansu, China. Int. J. Biometeorol. 2017, 61, 137–147. [Google Scholar] [CrossRef]
- Pearson, D.; Basu, R.; Wu, X.M.; Ebisu, K. Temperature and hand, foot and mouth disease in California: An exploratory analysis of emergency department visits by season, 2005–2013. Environ. Res. 2020, 185, 109461, Erratum in Environ. Res. 2023, 220, 115206. [Google Scholar] [CrossRef]
- Hong, J.; Liu, F.; Qi, H.; Tu, W.; Ward, M.P.; Ren, M.; Zhao, Z.; Su, Q.; Huang, J.; Chen, X.; et al. Changing epidemiology of hand, foot, and mouth disease in China, 2013-2019: A population-based study. Lancet Reg. Health West Pac. 2022, 20, 100370. [Google Scholar] [CrossRef]
- Cliff, A.D.; Ord, K. Spatial autocorrelation: A review of existing and new measures with applications. Econ. Geogr. 1970, 46 (Suppl. S1), 269–292. [Google Scholar] [CrossRef]
- Hastie, T.J.; Tibshirani, R.J. Generalized Additive Models. In Lifetime Data Analysis; Chapman and Hall: London, UK, 1990. [Google Scholar]
- Wang, Y.T.; Peng, W.J.; Su, H.L.; Wang, W. Spatial-temporal characteristics and influencing factors of hand, foot and mouth disease in China, 2011–2018. Chin. J. Epidemiol. 2021, 43, 1562–1567. [Google Scholar]
- Rui, J.; Luo, K.; Chen, Q.; Zhang, D.; Zhao, Q.; Zhang, Y.; Zhai, X.; Zhao, Z.; Zhang, S.; Liao, Y.; et al. Early warning of hand, foot, and mouth disease transmission: A modeling study in mainland, China. PLoS Negl. Trop. Dis. 2021, 15, e0009233. [Google Scholar] [CrossRef]
- Kimmis, B.D.; Downing, C.; Tyring, S. Hand-foot-and-mouth disease caused by coxsackievirus A6 on the rise. Cutis 2018, 102, 353–356. [Google Scholar]
- Bian, L.; Gao, F.; Mao, Q.; Sun, S.; Wu, X.; Liu, S.; Yang, X.; Liang, Z. Hand, foot, and mouth disease associated with coxsackievirus A10: More serious than it seems. Expert. Rev. Anti Infect. Ther. 2019, 17, 233–242. [Google Scholar] [CrossRef]
- Messacar, K.; Abzug, M.J.; Dominguez, S.R. 2014 outbreak of enterovirus D68 in North America. J. Med. Virol. 2016, 88, 739–745. [Google Scholar] [CrossRef]
- Messacar, K.; Abzug, M.J.; Dominguez, S.R. The changing epidemiology of acute flaccid paralysis warrants a paradigm shift in surveillance. J. Med. Virol. 2018, 90, 1–2. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. Vital Signs: Acute Flaccid Myelitis. 2020. Available online: https://www.cdc.gov/vitalsigns/afm2020/index.html (accessed on 25 December 2024).
- Wang, C.; Li, X.; Zhang, Y.; Xu, Q.; Huang, F.; Cao, K.; Tao, L.; Guo, J.; Gao, Q.; Wang, W.; et al. Spatiotemporal cluster patterns of hand, foot, and mouth disease at the county level in mainland China, 2008–2012. PLoS ONE 2016, 11, e0147532. [Google Scholar] [CrossRef]
- Stanaway, J.D. Insights from Disease Ecology: Focus on Hand, Foot and Mouth Disease in China. Ph.D Thesis, University of Washington, Seattle, WA, USA, 2013. [Google Scholar]
- Lin, H.; Zou, H.; Wang, Q.; Liu, C.; Lang, L.; Hou, X.; Li, Z. Short-term effect of El Nino-Southern Oscillation on pediatrichand, foot and mouth disease in Shenzhen, China. PLoS ONE 2013, 8, e65585. [Google Scholar]
- Bo, Y.C.; Song, C.; Wang, J.F.; Li, X.W. 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 2014, 14, 358. [Google Scholar] [CrossRef]
- Chen, J.J.; Shen, H.F.; Li, T.W.; Peng, X.; Cheng, H.; Ma, C. Temporal and spatial features of the correlation between PM2.5 and O3 concentrations in China. Int. J. Environ. Res. Public Health 2019, 16, 4824. [Google Scholar] [CrossRef]
- Wang, Y.; Zhao, H.; Ou, R.; Zhu, H.; Gan, L.; Zeng, Z.; Yuan, R.; Yu, H.; Ye, M. Epidemiological and clinical characteristics of severe hand-foot-and-mouth disease (HFMD) among children: A 6-year population-based study. BMC Public Health 2020, 20, 801. [Google Scholar] [CrossRef] [PubMed]
Year | Moran’s I | Z-Score | p-Value |
---|---|---|---|
2014 | 0.16 | 2.34 | 0.02 |
2015 | 0.21 | 3.10 | 0.00 * |
2016 | 0.17 | 2.51 | 0.01 |
2017 | 0.17 | 2.57 | 0.01 |
2018 | 0.20 | 2.92 | 0.00 * |
2019 | 0.36 | 5.24 | 0.00 * |
2020 | 0.37 | 5.36 | 0.00 * |
2021 | 0.21 | 3.09 | 0.00 * |
2022 | 0.34 | 4.95 | 0.00 * |
2023 | 0.25 | 3.41 | 0.00 * |
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Zhan, M.; Cai, S.; Xie, Z.; Zheng, S.; Huang, Z.; Ou, J.; Wu, S. Spatiotemporal Distribution of Hand, Foot, and Mouth Disease and the Influence of Air Pollutants and Socioeconomic Factors on Incidence in Fujian, China. Trop. Med. Infect. Dis. 2025, 10, 188. https://doi.org/10.3390/tropicalmed10070188
Zhan M, Cai S, Xie Z, Zheng S, Huang Z, Ou J, Wu S. Spatiotemporal Distribution of Hand, Foot, and Mouth Disease and the Influence of Air Pollutants and Socioeconomic Factors on Incidence in Fujian, China. Tropical Medicine and Infectious Disease. 2025; 10(7):188. https://doi.org/10.3390/tropicalmed10070188
Chicago/Turabian StyleZhan, Meirong, Shaojian Cai, Zhonghang Xie, Senshuang Zheng, Zhengqiang Huang, Jianming Ou, and Shenggen Wu. 2025. "Spatiotemporal Distribution of Hand, Foot, and Mouth Disease and the Influence of Air Pollutants and Socioeconomic Factors on Incidence in Fujian, China" Tropical Medicine and Infectious Disease 10, no. 7: 188. https://doi.org/10.3390/tropicalmed10070188
APA StyleZhan, M., Cai, S., Xie, Z., Zheng, S., Huang, Z., Ou, J., & Wu, S. (2025). Spatiotemporal Distribution of Hand, Foot, and Mouth Disease and the Influence of Air Pollutants and Socioeconomic Factors on Incidence in Fujian, China. Tropical Medicine and Infectious Disease, 10(7), 188. https://doi.org/10.3390/tropicalmed10070188