Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2021 Apr 20;41(2):211–218. doi: 10.1007/s11596-021-2338-x

The Short-term Effects of Temperature on Infectious Diarrhea among Children under 5 Years Old in Jiangsu, China: A Time-series Study (2015–2019)

Nan-nan Huang 1,#, Hao Zheng 2,#, Bin Li 1, Gao-qiang Fei 1, Zhen Ding 2, Jia-jia Wang 3, Xiao-bo Li 1,✉
PMCID: PMC8056199  PMID: 33877537

Summary

The association between meteorological factors and infectious diarrhea has been widely studied in many countries. However, investigation among children under 5 years old in Jiangsu, China remains quite limited. Data including infectious diarrhea cases among children under five years old and daily meteorological indexes in Jiangsu, China from 2015 to 2019 were collected. The lag-effects up to 21 days of daily maximum temperature (Tmax) on infectious diarrhea were explored using a quasi-Poisson regression with a distributed lag non-linear model (DLNM) approach. The cases number of infectious diarrhea was significantly associated with seasonal variation of meteorological factors, and the burden of disease mainly occurred among children aged 0–2 years old. Moreover, when the reference value was set at 16.7°C, Tmax had a significant lag-effect on cases of infectious diarrhea among children under 5 years old in Jiangsu Province, which was increased remarkably in cold weather with the highest risk at 8°C. The results of DLNM analysis implicated that the lag-effect of Tmax varied among the 13 cities in Jiangsu and had significant differences in 8 cities. The highest risk of Tmax was presented at 5 lag days in Huaian with a maximum RR of 1.18 (95% CI: 1.09, 1.29). Suzhou which had the highest number of diarrhea cases (15830 cases), had a maximum RR of 1.04 (95% CI:1.03, 1.05) on lag 15 days. Tmax is a considerable indicator to predict the epidemic of infectious diarrhea among 13 cities in Jiangsu, which reminds us that in cold seasons, more preventive strategies and measures should be done to prevent infectious diarrhea.

Electronic supplementary material

The online version of this article (10.1007/s11596-021-2338-x) contains supplementary material, which is available to authorized users.

Key words: infectious diarrhea, incidence, meteorological factors, maximum temperature (Tmax), lag-effect

Electronic supplementary material

11596_2021_2338_MOESM1_ESM.pdf (25.8MB, pdf)

Supplementary material, approximately 25.7 MB.

Footnotes

Conflict of Interest Statement

The authors declare that there is no conflict of interest with any financial organization or corporation or individual that can inappropriately influence this work.

Both authors contributed equally to this study.

Contributor Information

Nan-nan Huang, Email: 220193573@seu.edu.cn.

Hao Zheng, Email: zhenghao@jscd.cn.

Xiao-bo Li, Email: 101011116@seu.edu.cn.

References

  • 1.Walker CLF, Rudan I, Liu L, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013;381(9875):1405–1416. doi: 10.1016/S0140-6736(13)60222-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Mekonnen GK, Alemu BM, Mulat W, et al. Risk factors for acute childhood diarrhea: A cross-sectional study comparing refugee camps and host communities in Gambella Region, Ethiopia. Travel Med Infect Dis. 2019;31:101385. doi: 10.1016/j.tmaid.2019.02.003. [DOI] [PubMed] [Google Scholar]
  • 3.Gou F, Liu X, He J, et al. Different responses of weather factors on hand, foot and mouth disease in three different climate areas of Gansu, China. BMC Infect Dis. 2018;18(1):15. doi: 10.1186/s12879-017-2860-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Imai C, Armstrong B, Chalabi Z, et al. Time series regression model for infectious disease and weather. Environ Res. 2015;142:319–327. doi: 10.1016/j.envres.2015.06.040. [DOI] [PubMed] [Google Scholar]
  • 5.Stott PA, Stone DA, Allen MR. Human contribution to the European heatwave of 2003. Nature. 2004;432(7017):610–614. doi: 10.1038/nature03089. [DOI] [PubMed] [Google Scholar]
  • 6.Singh RB, Hales S, de Wet N, et al. The influence of climate variation and change on diarrheal disease in the Pacific Islands. Environ Health Perspect. 2001;109(2):155–159. doi: 10.1289/ehp.01109155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Chou WC, Wu JL, Wang YC, et al. Modeling the impact of climate variability on diarrhea-associated diseases in Taiwan (1996–2007) Sci Total Environ. 2010;409(1):43–51. doi: 10.1016/j.scitotenv.2010.09.001. [DOI] [PubMed] [Google Scholar]
  • 8.Van GRD, Van DKJ, Hahne SJM, et al. Determinants of Rotavirus Transmission: A Lag Nonlinear Time Series Analysis. Epidemiology. 2017;28(4):503–513. doi: 10.1097/EDE.0000000000000654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Chou WC, Wu JL, Wang YC, et al. Modeling the impact of climate variability on diarrhea-associated diseases in Taiwan (1996–2007) Sci Total Environ. 2010;409(1):43–51. doi: 10.1016/j.scitotenv.2010.09.001. [DOI] [PubMed] [Google Scholar]
  • 10.Greer AL, Drews SJ, Fisman DN. Why “Winter” Vomiting Disease? Seasonality, Hydrology, and Norovirus Epidemiology in Toronto, Canada. EcoHealth. 2009;6(2):192–199. doi: 10.1007/s10393-009-0247-8. [DOI] [PubMed] [Google Scholar]
  • 11.Singh RB, Hales S, Wet N, et al. The influence of climate variation and change on diarrheal disease in the Pacific Islands. Environmental Health Perspectives. 2001;109(2):155–159. doi: 10.1289/ehp.01109155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Gong L, Hou S, Su B, et al. Short-term effects of moderate and severe floods on infectious diarrheal diseases in Anhui Province, China. Sci Total Environ. 2019;675:420–428. doi: 10.1016/j.scitotenv.2019.04.248. [DOI] [PubMed] [Google Scholar]
  • 13.Xiang J, Bi P, Pisaniello D, et al. Association between high temperature and work-related injuries in Adelaide, South Australia, 2001–2010. Occup Environ Med. 2014;71(4):246–252. doi: 10.1136/oemed-2013-101584. [DOI] [PubMed] [Google Scholar]
  • 14.Guo Y, Punnasiri K, Tong S. Effects of temperature on mortality in Chiang Mai city, Thailand: a time series study. Environ Health. 2012;11:36. doi: 10.1186/1476-069X-11-36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Gasparrini A. Distributed Lag Linear and Non-Linear Models in R: The Package dlnm. J Stat Softw. 2011;43(8):1–20. doi: 10.18637/jss.v043.i08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Wang HT. Lag effect and influencing factors of temperature on other infectious diarrhea in Zhejiang province. Chin J Epidemiol. 2019;40(8):960–964. doi: 10.3760/cma.j.issn.0254-6450.2019.08.016. [DOI] [PubMed] [Google Scholar]
  • 17.Gao J, Lu M, Sun Y, et al. Changes in ambient temperature increase hospital outpatient visits for allergic rhinitis in Xinxiang, China. BMC Public Health. 2021;21(1):600. doi: 10.1186/s12889-021-10671-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Zhu G, Zhu Y, Wang Z, et al. The association between ambient temperature and mortality of the coronavirus disease 2019 (COVID-19) in Wuhan, China: a time-series analysis. BMC Public Health. 2021;21(1):117. doi: 10.1186/s12889-020-10131-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Yi X, Chang Z, Zhao X, et al. The temporal characteristics of the lag-response relationship and related key time points between ambient temperature and hand, foot and mouth disease: A multicity study from mainland China. Sci Total Environ. 2020;749:141679. doi: 10.1016/j.scitotenv.2020.141679. [DOI] [PubMed] [Google Scholar]
  • 20.Girish KCP, Giri S, Chawla-Sarkar M, et al. Epidemiology of rotavirus diarrhea among children less than 5 years hospitalized with acute gastroenteritis prior to rotavirus vaccine introduction in India. Vaccine. 2020;38(51):8154–8160. doi: 10.1016/j.vaccine.2020.10.084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.D’Souza RM, Hall G, Becker NG. Climatic factors associated with hospitalizations for rotavirus diarrhoea in children under 5 years of age. Epidemiol Infect. 2008;136(1):56–64. doi: 10.1017/S0950268807008229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Jagai JS, Sarkar R, Castronovo D, et al. Seasonality of rotavirus in South Asia: a meta-analysis approach assessing associations with temperature, precipitation, and vegetation index. PLoS One. 2012;7(5):e38168. doi: 10.1371/journal.pone.0038168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Olesen B, Neimann J, Bottiger B, et al. Etiology of diarrhea in young children in Denmark: a case-control study. J Clin Microbiol. 2005;43(8):3636–3641. doi: 10.1128/JCM.43.8.3636-3641.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Santika NKA, Efendi F, Rachmawati PD, et al. Determinants of diarrhea among children under two years old in Indonesia. Child Youth Serv Rev, 2020,111
  • 25.Rogawski MET, Platts-Mills JA, Gratz J, et al. Impact of Water Quality, Sanitation, Handwashing, and Nutritional Interventions on Enteric Infections in Rural Zimbabwe: The Sanitation Hygiene Infant Nutrition Efficacy (SHINE) Trial. J Infect Dis. 2020;221(8):1379–1386. doi: 10.1093/infdis/jiz179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Rissman L, Deavenport-Saman A, Corden MH, et al. A pilot project: handwashing educational intervention decreases incidence of respiratory and diarrheal illnesses in a rural Malawi orphanage. Glob Health Promot, 2020:1757975920963889 [DOI] [PubMed]
  • 27.Fang X, Ai J, Liu W, et al. Epidemiology of infectious diarrhoea and the relationship with etiological and meteorological factors in Jiangsu Province, China. Sci Rep. 2019;9(1):19571. doi: 10.1038/s41598-019-56207-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Dong Y, Wang L, Burgner DP, et al. Infectious diseases in children and adolescents in China: analysis of national surveillance data from 2008 to 2017. BMJ. 2020;369:m1043. doi: 10.1136/bmj.m1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Ximenes RA, Southgate B, Smith PG, et al. Migration and urban schistosomiasis. The case of Sao Lourenco da Mata, northeast of Brazil. Rev Inst Med Trop Sao Paulo. 2000;42(4):209–217. doi: 10.1590/S0036-46652000000400006. [DOI] [PubMed] [Google Scholar]
  • 30.Wang H, Di B, Zhang TJ, et al. Association of meteorological factors with infectious diarrhea incidence in Guangzhou, southern China: A time-series study (2006–2017) Sci Total Environ. 2019;672:7–15. doi: 10.1016/j.scitotenv.2019.03.330. [DOI] [PubMed] [Google Scholar]
  • 31.Milazzo A, Giles LC, Zhang Y, et al. The effect of temperature on different Salmonella serotypes during warm seasons in a Mediterranean climate city, Adelaide, Australia. Epidemiol Infect. 2016;144(6):1231–1240. doi: 10.1017/S0950268815002587. [DOI] [PubMed] [Google Scholar]
  • 32.Chai SJ, Gu W, O’Connor KA, et al. Incubation periods of enteric illnesses in foodborne outbreaks, United States, 1998–2013. Epidemiol Infect. 2019;147:e285. doi: 10.1017/S0950268819001651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Hughes SL, Morbey RA, Elliot AJ, et al. Monitoring telehealth vomiting calls as a potential public health early warning system for seasonal norovirus activity in Ontario, Canada. Epidemiol Infect. 2019;147:e112. doi: 10.1017/S0950268818003357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Levy K, Woster AP, Goldstein RS, et al. Untangling the Impacts of Climate Change on Waterborne Diseases: a Systematic Review of Relationships between Diarrheal Diseases and Temperature, Rainfall, Flooding, and Drought. Environ Sci Technol. 2016;50(10):4905–4922. doi: 10.1021/acs.est.5b06186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Zhang F, Liu Z, Gao L, et al. Short-term impacts of floods on enteric infectious disease in Qingdao, China, 2005–2011. Epidemiol Infect. 2016;144(15):3278–3287. doi: 10.1017/S0950268816001084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Makaya JM, Kaplon J, Fremy C, et al. Norovirus and rotavirus survival in urine collected from a public ecological sanitation system in Ouagadougou, Burkina Faso. Food Environ Virol. 2015;7(1):41–48. doi: 10.1007/s12560-014-9172-2. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

11596_2021_2338_MOESM1_ESM.pdf (25.8MB, pdf)

Supplementary material, approximately 25.7 MB.

Articles from Current Medical Science are provided here courtesy of Nature Publishing Group

RESOURCES