Abstract
Varicella is a rising public health issue. Several studies have tried to quantify the relationships between meteorological factors and varicella incidence but with inconsistent results. We aim to investigate the impact of temperature and relative humidity on varicella, and to further explore the effect modification of these relationships. In this study, the data of varicella and meteorological factors from 2011 to 2019 in 21 cities of Guangdong Province, China were collected. Distributed lag nonlinear models (DLNM) were constructed to explore the relationship between meteorological factors (temperature and relative humidity) and varicella in each city, controlling in school terms, holidays, seasonality, long-term trends, and day of week. Multivariate meta-analysis was applied to pool the city-specific estimations. And the meta-regression was used to explore the effect modification for the spatial heterogeneity of city-specific meteorological factors and social factors (such as disposable income per capita, vaccination coverage, and so on) on varicella. The results indicated that the relationship between temperature and varicella in 21 cities appeared nonlinear with an inverted S-shaped. The relative risk peaked at 20.8 ℃ (RR = 1.42, 95% CI: 1.22, 1.65). The relative humidity-varicella relationship was approximately L-shaped, with a peaking risk at 69.5% relative humidity (RR = 1.25, 95% CI: 1.04, 1.50). The spatial heterogeneity of temperature-varicella relationships may be caused by income or varicella vaccination coverage. And varicella vaccination coverage may contribute to the spatial heterogeneity of the relative humidity-varicella relationship. The findings can help us deepen the understanding of the meteorological factors-varicella association and provide evidence for develo** prevention strategy for varicella epidemic.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-22711-8/MediaObjects/11356_2022_22711_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-22711-8/MediaObjects/11356_2022_22711_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-22711-8/MediaObjects/11356_2022_22711_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-22711-8/MediaObjects/11356_2022_22711_Fig4_HTML.png)
Similar content being viewed by others
Data availability
The data of daily meteorological variables from 2011 to 2019 can be accessed from the China Meteorological Data Sharing Service System (http://www.cma.gov.cn/), and city-specific socio-economic characteristics for 21 cities in Guangdong can be accessed from the official website of Guangdong Provincial Bureau of Statistics (http://stats.gd.gov.cn/gdtjnj/). The data of detailed surveillance generated during and/or analyzed during the current study are not publicly available due to the data management requirements but are available from the corresponding author on reasonable request.
References
Arat A, Burström B, Östberg V, Hjern A (2019) Social inequities in vaccination coverage among infants and pre-school children in Europe and Australia - a systematic review. BMC Public Health 19:290
Ayoade F, Kumar S (2021) Varicella Zoster, StatPearls. StatPearls Publishing LLC, Treasure Island FL
Bakker KM, Eisenberg MC, Woods R, Martinez ME (2021) Exploring the Seasonal Drivers of Varicella Zoster Virus Transmission and Reactivation. Am J Epidemiol 190:1814–1820
Bo Z, Ma Y, Chang Z, Zhang T, Liu F, Zhao X, Long L, Yi X, **ao 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
Chan DYW, Edmunds WJ, Chan HL, Chan V, Lam YCK, Thomas SL, van Hoek AJ, Flasche S (2018) The changing epidemiology of varicella and herpes zoster in Hong Kong before universal varicella vaccination in 2014. Epidemiol Infect 146:723–734
Chan JY, Lin HL, Tian LW (2014) Meteorological factors and El Nino Southern Oscillation are associated with paediatric varicella infections in Hong Kong, 2004–2010. Epidemiol Infect 142:1384–1392
Chen B, Sumi A, Wang L, Zhou W, Kobayashi N (2017) Role of meteorological conditions in reported chickenpox cases in Wuhan and Hong Kong, China. BMC Infect Dis 17:538
Critselis E, Nastos PT, Theodoridou K, Theodoridou M, Tsolia MN, Hadjichristodoulou C, Papaevangelou V (2012) Time trends in pediatric hospitalizations for varicella infection are associated with climatic changes: a 22-year retrospective study in a tertiary Greek referral center. PLoS One 7:e52016
Daulagala S, Noordeen F, Fara MMF, Rathnayake C, Gunawardana K (2017) Exposure rate of VZV among women attending antenatal care clinic in Sri Lanka - a cross sectional study. BMC Infect Dis 17:625
Daulagala S, Noordeen F (2018) Epidemiology and factors influencing varicella infections in tropical countries including Sri Lanka. Virusdisease 29:277–284
Dong P, Wang M, Liu Y (2020) Epidemiological characteristics of varicella in China, 2016–2019. Chinese J Vaccin Immunization 26:403–406
Fang J, Song J, Wu R, **e Y, Xu X, Zeng Y, Zhu Y, Wang T, Yuan N, Xu H, Song X, Zhang Q, Xu B, Huang W (2021) Association between ambient temperature and childhood respiratory hospital visits in Bei**g, China: a time-series study (2013–2017). Environ Sci Pollut Res Int 28:29445–29454
Gao Y, Niu Y, Sun W, Liu K, Liu X, Zhao N, Yue Y, Wu H, Meng F, Wang J, Wang X, Liu Q (2020) Climate factors driven typhus group rickettsiosis incidence dynamics in **shuangbanna Dai autonomous prefecture of Yunnan province in China, 2005–2017. Environ Health : a Glob Access Sci Source 19:3
Gasparrini A, Armstrong B, Kenward MG (2010) Distributed lag non-linear models. Stat Med 29:2224–2234
Gasparrini A (2011) Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 43:1–20
Gasparrini A, Armstrong B, Kenward MG (2012) Multivariate meta-analysis for non-linear and other multi-parameter associations. Stat Med 31:3821–3839
Gasparrini A, Armstrong B (2013) Reducing and meta-analysing estimates from distributed lag non-linear models. BMC Med Res Methodol 13:1
Guangdong Bureau of Statistics (2021) Guangdong Statistical Yearbook 2021. Guangdong Bureau of Statistics
Halloran SK, Wexler AS, Ristenpart WD (2012) A comprehensive breath plume model for disease transmission via expiratory aerosols. PLoS One 7:e37088–e37088
Lam HCY, Chan JCN, Luk AOY, Chan EYY, Goggins WB (2018) Short-term association between ambient temperature and acute myocardial infarction hospitalizations for diabetes mellitus patients: A time series study. PLoS Med 15:e1002612
Li XK, Gao XL, Li Y, Xu H, Fan CL (2019) Seroepidemiology of varicella among the healthy population aged 1–19 years in Harbin, China. Chin J Contemp Pediatr 21:203–207
Lin Z, Meng X, Chen R, Huang G, Ma X, Chen J, Huang M, Gui Y, Chu C, Liu F, Kan H (2017) Ambient air pollution, temperature and kawasaki disease in Shanghai, China. Chemosphere 186:817–822
Liyanage NP, Fernando S, Malavige GN, Mallikahewa R, Sivayogan S, Jiffry MT, Vitarana T (2007) Seroprevalence of varicella zoster virus infections in Colombo district, Sri Lanka. Indian J Med Sci 61:128–134
Lu JY, Zhang ZB, He Q, Ma XW, Yang ZC (2020) Association between climatic factors and varicella incidence in Guangzhou, Southern China, 2006–2018. Sci Total Environ 728:138777
Luo C, Ma Y, Liu Y, Lv Q, Yin F (2020) The burden of childhood hand-foot-mouth disease morbidity attributable to relative humidity: a multicity study in the Sichuan Basin, China. Sci Rep 10:19394
Ma W, Wang L, Lin H, Liu T, Zhang Y, Rutherford S, Luo Y, Zeng W, Wang X, Gu X, Chu C, **ao J, Zhou M (2015) The temperature-mortality relationship in China: An analysis from 66 Chinese communities. Environ Res 137:72–77
Marziano V, Poletti P, Béraud G, Boëlle PY, Merler S, Colizza V (2018) Modeling the impact of changes in day-care contact patterns on the dynamics of varicella transmission in France between 1991 and 2015. PLoS Comput Biol 14:e1006334
Neiderud CJ (2015) How urbanization affects the epidemiology of emerging infectious diseases. Infect Ecol Epidemiol 5:27060
Ni L, Zheng X, Huang Y (2018) Modelling and predicting the long-term impact of varicella vaccine immunization Modern. Prev Med 45:449–453
Pan J, Wang Y, Cao L, Wang Y, Zhao Q, Tang S, Gong W, Guo L, Liu Z, Wen Z, Zheng B, Wang W (2021) Impact of immunization programs on 11 childhood vaccine-preventable diseases in China: 1950–2018. Innovation 2:100113
Santermans E, Goeyvaerts N, Melegaro A, Edmunds WJ, Faes C, Aerts M, Beutels P, Hens N (2015) The social contact hypothesis under the assumption of endemic equilibrium: Elucidating the transmission potential of VZV in Europe. Epidemics 11:14–23
Sumi A (2018) Role of temperature in reported chickenpox cases in northern European countries: Denmark and Finland. BMC research notes 11:377
Sun Y, Wang Z, Zhang Y, Sundell J (2011) In China, students in crowded dormitories with a low ventilation rate have more common colds: evidence for airborne transmission. PLoS One 6:e27140
Tang X, Geater A, McNeil E, Deng Q, Dong A, Zhong G (2017) Spatial, temporal and spatio-temporal clusters of measles incidence at the county level in Guangxi, China during 2004–2014: flexibly shaped scan statistics. BMC Infect Dis 17:243
Toi CS, Dwyer DE (2010) Prevalence of varicella-zoster virus genotypes in Australia characterized by high-resolution melt analysis and ORF22 gene analyses. J Med Microbiol 59:935–940
Ueshiba R, Abe K, Kingetsu M, Ito M (2013) Suggestion to school pharmacists to utilize absolute humidity parameter for maintaining air-conditioning. Yakugaku Zasshi : Journal of the Pharmaceutical Society of Japan 133:479–483
Wang JY, Li S, Ma HP, Dong JY, Wang YH, Zhang W, Zhang XY, Li P, Li SY (2018) Research on the relationship between the daily mean temperature and the daily cases of varicella during 2008–2016 in Lanzhou, China. Chin J Prev Med 52:842–848
Wang L, Hu W, Soares Magalhaes RJ, Bi P, Ding F, Sun H, Li S, Yin W, Wei L, Liu Q, Haque U, Sun Y, Huang L, Tong S, Clements AC, Zhang W, Li C (2014) The role of environmental factors in the spatial distribution of Japanese encephalitis in mainland China. Environ Int 73:1–9
WHO (2014) Varicella and herpes zoster vaccines: WHO position paper, June 2014. Wkly Epidemiol Rec 89:265–287
WHO (2016) Varicella and herpes zoster vaccines: WHO position paper, June 2014–Recommendations. Vaccine 34:198–199
Wu H, Wang H, Wang Q, **n Q, Lin H (2014) The effect of meteorological factors on adolescent hand, foot, and mouth disease and associated effect modifiers. Glob Health Action 7:24664
Wu J, Cheng J, Xu Z, Zhao K, Zhao D, **e 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 35:1086–1091
**ao X, Gasparrini A, Huang J, Liao Q, Liu F, Yin F, Yu H, Li X (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
Yang F, Ma Y, Liu F, Zhao X, Fan C, Hu Y, Hu K, Chang Z, **ao X (2020) Short-term effects of rainfall on childhood hand, foot and mouth disease and related spatial heterogeneity: evidence from 143 cities in mainland China. BMC Public Health 20:1528
Yang Y, Geng X, Liu X, Wang W, Zhang J (2016) Association between the incidence of varicella and meteorological conditions in **an, Eastern China, 2012–2014. BMC Infect Dis 16:179
Yu G, Yang R, Wei Y, Yu D, Zhai W, Cai J, Long B, Chen S, Tang J, Zhong G, Qin J (2018) Spatial, temporal, and spatiotemporal analysis of mumps in Guangxi Province, China, 2005–2016. BMC Infect Dis 18:360
Zhang Y, Liu QY, Luan RS, Liu XB, Zhou GC, Jiang JY, Li HS, Li ZF (2012) Spatial-temporal analysis of malaria and the effect of environmental factors on its incidence in Yongcheng, China, 2006–2010. BMC Public Health 12:544
Zhu Q, Wang X, Su W, Cui Y, Liang J, Wu C, Shao X-p, Zheng H-z (2016) Effectiveness of varicella vaccine based on several varicella outbreaks in Guangdong Province. South China J Prev Med 42:129–133
Acknowledgements
We are grateful for all people who diagnosed and submitted the varicella cases to the National Notifiable Infectious Disease Surveillance System. We thank the staffs at the hospitals, local health departments, and county-, district-, and prefecture-level Centers for Disease Control and Prevention for their valuable assistance in data collection.
Funding
This work was primarily supported by the National Key Research and Development Program of China (2018YFA0606200), Guangdong Medical Science and Technology Research Foundation (B2020105), the Key-Area Research and Development Program of Guangdong Province (2019B111103001), and the Science and Technology Program of Guangzhou (202102080554).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Conceived and designed the experiments: Limei Sun, Jianpeng **ao. Analyzed the data: Yihan Li, Jianpeng **ao. Contributed reagents/materials/analysis tools: Yihan Li, Jialing Li, Zhihua Zhu, Weilin Zeng, Qi Zhu, Zuhua Rong, Jianxiong Hu, **ng Li, Guanhao He, Jianguo Zhao, Lihua Yin, Yi Quan, Qian Zhang, Manman Li, Li Zhang, Yan Zhou, Tao Liu, Wenjun Ma, Siqing Zeng, Qing Chen, Limei Sun, Jianpeng **ao. Wrote the paper: Yihan Li, Jianpeng **ao, Weilin Zeng. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
The study was approved by the ethics committee of Guangdong Provincial Center for Disease Control and Prevention (No. W96-027E-201925).
Consent to participate
Not applicable.
Consent for publication
The authors have provided consent to publish this work.
Conflict of interest
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
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, Y., Li, J., Zhu, Z. et al. Exposure–response relationship between temperature, relative humidity, and varicella: a multicity study in South China. Environ Sci Pollut Res 30, 7594–7604 (2023). https://doi.org/10.1007/s11356-022-22711-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-22711-8