Abstract
Infectious diarrhea (ID) is an intestinal infectious disease including cholera, typhoid and paratyphoid fever, bacterial and amebic dysentery, and other infectious diarrhea. There are many studies that have explored the relationship between ambient temperature and the spread of infectious diarrhea, but the results are inconsistent. It is necessary to systematically evaluate the impact of temperature on the incidence of ID. This study was based on the PRISMA statement to report this systematic review. We conducted literature searches from CNKI, VIP databases, CBM, PubMed, Web of Science, Cochrane Library, and other databases. The number registered in PROSPERO is CRD42021225472. After searching a total of 4915 articles in the database and references, 27 studies were included. The number of people involved exceeded 7.07 million. The overall result demonstrated when the temperature rises, the risk of infectious diarrhea increases significantly (RRcumulative=1.42, 95%CI: 1.07–1.88, RRsingle-day=1.08, 95%CI: 1.03–1.14). Subgroup analysis found the effect of temperature on the bacillary dysentery group (RRcumulative=1.85, 95%CI: 1.48–2.30) and unclassified diarrhea groups (RRcumulative=1.18, 95%CI: 0.59–2.34). The result of the single-day effect subgroup analysis was similar to the result of the cumulative effect. And the sensitivity analysis proved that the results were robust. This systematic review and meta-analysis support that temperature will increase the risk of ID, which is helpful for ID prediction and early warning in the future.
Similar content being viewed by others
References
Asadgol Z, Badirzadeh A, Niazi S, Mokhayeri Y, Kermani M, Mohammadi H, Gholami M (2020) How climate change can affect cholera incidence and prevalence? A systematic review. Environ Sci Pollut Res 27:1–21
Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101
Black R, Lanata C (1995) Epidemiology of diarrheal diseases in developing countries. In: Infections of the gastrointestinal tract. Raven Press, New York
Borenstein M, Hedges LV, Higgins JP, Rothstein H (2010) A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods 1:97–111
Campbell-Lendrum D, Manga L, Bagayoko M, Sommerfeld J (2015) Climate change and vector-borne diseases: what are the implications for public health research and policy? Philoso Transac Royal Soc B Biolog Sci 370:20130552
Carlton EJ, Woster AP, DeWitt P, Goldstein RS, Levy K (2016) A systematic review and meta-analysis of ambient temperature and diarrhoeal diseases. Int J Epidemiol 45:117–130
Checkley W, Epstein LD, Gilman RH, Figueroa D, Cama RI, Patz JA, Black RE (2000) Effects of EI Niño and ambient temperature on hospital admissions for diarrhoeal diseases in Peruvian children. Lancet 355:442–450
Cheng J et al (2017) Impacts of ambient temperature on the burden of bacillary dysentery in urban and rural Hefei, China. Epidemiol Infect 145:1567–1576. https://doi.org/10.1017/s0950268817000280
D’Souza RM, Hall G, Becker NG (2008) Climatic factors associated with hospitalizations for rotavirus diarrhoea in children under 5 years of age. Epidemiol Infect 136:56–64. https://doi.org/10.1017/s0950268807008229
Deeks JJ, Higgins JP, Altman DG, Groupa CSM (2019) Analysing data and undertaking meta-analyses. In: Cochrane handbook for systematic reviews of interventions, pp 241–284
DerSimonian R, Laird NJ (1986) Meta-anal Clin Trials 7:177–188
Dewan AM, Corner R, Hashizume M, Ongee ET (2013) Typhoid Fever and Its Association with Environmental Factors in the Dhaka Metropolitan Area of Bangladesh: A Spatial and Time-Series Approach. PLoS Negl Trop Dis 7:e1998. https://doi.org/10.1371/journal.pntd.0001998
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Bmj 315:629–634
Fang J, Song J, Wu R, Xie 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 Beijing, China: a time-series study (2013–2017). Environ Sci Pollut Res 28:29445–29454. https://doi.org/10.1007/s11356-021-12817-w
Gao Y, Chen Y, Shi P, Zhang Q, Qian C, Xiao Y, Feng W, Shen Y, Shi C (2020) The effect of ambient temperature on infectious diarrhea and diarrhea-like illness in Wuxi, China. Disast Med Public Health Prep:1–7. https://doi.org/10.1017/dmp.2020.340
Hao Y, Liao W, Ma W, Zhang J, Zhang N, Zhong S, Wang Z, Yang L, Huang C (2019) Effects of ambient temperature on bacillary dysentery: a multi-city analysis in Anhui Province, China. Sci Total Environ 671:1206–1213. https://doi.org/10.1016/j.scitotenv.2019.03.443
Hashizume M, Armstrong B, Wagatsuma Y, Faruque AS, Hayashi T, Sack DA (2008) Rotavirus infections and climate variability in Dhaka, Bangladesh: a time-series analysis. Epidemiol Infect 136:1281–1289. https://doi.org/10.1017/s0950268807009776
Hu W, Li Y, Ma W (2019) Short-term impact of temperature on infectious diarrhea in southeast coastal area of China, 2005-2013. Chin J Prev Med 53:103–106
Ip S et al (2009) Predictors of clinical outcomes following fundoplication for gastroesophageal reflux disease remain insufficiently defined: a systematic review. Am J Gastroenterol 104:752–758
Jagai JS, Sarkar R, Castronovo D, Kattula D, McEntee J, Ward H, Kang G, Naumova EN (2012) Seasonality of rotavirus in South Asia: a meta-analysis approach assessing associations with temperature, precipitation, and vegetation index. PLoS One 7:e38168. https://doi.org/10.1371/journal.pone.0038168
James SL et al (2018) Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392:1789–1858
Jelinski DE, Wu J (1996) The modifiable areal unit problem and implications for landscape ecology. Landsc Ecol 11:129–140
Kosek M, Bern C, Guerrant RL (2003) The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81:197–204
Kotloff KL et al (1999) Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ 77:651
Kovats R, Edwards S, Hajat S, Armstrong B, Ebi K, Menne B (2004) The effect of temperature on food poisoning: a time-series analysis of salmonellosis in ten European countries. Epidemiol Infect 132:443–453
Leddin D, Macrae F (2020) Climate change: implications for gastrointestinal health and disease. J Clin Gastroenterol 54:393–397. https://doi.org/10.1097/mcg.0000000000001336
Levy K, Hubbard AE, Eisenberg JN (2009) Seasonality of rotavirus disease in the tropics: a systematic review and meta-analysis. Int J Epidemiol 38:1487–1496. https://doi.org/10.1093/ije/dyn260
Li K, Zhao K, Shi L, Wen L, Yang H, Cheng J, Wang X, Su H (2016) Daily temperature change in relation to the risk of childhood bacillary dysentery among different age groups and sexes in a temperate city in China. Public Health 131:20–26. https://doi.org/10.1016/j.puhe.2015.10.011
Li S, Wang Y, Dong J (2019) Association between incidence of other infectious diarrhea and meteorological factors in Jiayuguan. Chin J PHM 35:157–159
Li T, Yang Z, Wang M (2014) Temperature and atmospheric pressure may be considered as predictors for the occurrence of bacillary dysentery in Guangzhou, Southern China. Rev Soc Bras Med Trop 47:382–384. https://doi.org/10.1590/0037-8682-0144-2013
Li Z, Wang L, Sun W, Hou X, Yang H, Sun L, Xu S, Sun Q, Zhang J, Song H, Lin H (2013) Identifying high-risk areas of bacillary dysentery and associated meteorological factors in Wuhan, China. Sci Rep 3:3239. https://doi.org/10.1038/srep03239
Lin M, Dong B (2008) Status of epidemiological research of infectious diarrhea. China Trop Med 8:675–677
Liu Y, Wu H, Lao J, Jiang B (2018) Relationship between meteorological factors and incidence of bacillary dysentery:a meta-analysis. J Environ Health 35:487–491
Liu Z, Liu Y, Zhang Y, Lao J, Zhang J, Wang H, Jiang B (2019) Effect of ambient temperature and its effect modifiers on bacillary dysentery in Jinan, China. Sci Total Environ 650:2980–2986. https://doi.org/10.1016/j.scitotenv.2018.10.053
Liu Z, Tong MX, Xiang J, Dear K, Wang C, Ma W, Lu L, Liu Q, Jiang B, Bi P (2020) Daily temperature and bacillary dysentery: estimated effects, attributable risks, and future disease burden in 316 Chinese cities. Environ Health Perspect 128:057008. https://doi.org/10.1289/ehp5779
Luque Fernández MA, Bauernfeind A, Jiménez JD, Gil CL, El Omeiri N, Guibert DH (2009) Influence of temperature and rainfall on the evolution of cholera epidemics in Lusaka, Zambia, 2003-2006: analysis of a time series. Trans R Soc Trop Med Hyg 103:137–143. https://doi.org/10.1016/j.trstmh.2008.07.017
Ma Y, Zhang Y, Cheng B, Feng F, Jiao H, Zhao X, Ma B, Yu Z (2020) A review of the impact of outdoor and indoor environmental factors on human health in China. Environ Sci Pollut Res Int 27:42335–42345. https://doi.org/10.1007/s11356-020-10452-5
Min M, Shi T, Ye P, Wang Y, Yao Z, Tian S, Zhang Y, Liang M, Qu G, Bi P, Duan L, Sun Y (2019) Effect of apparent temperature on daily emergency admissions for mental and behavioral disorders in Yancheng, China: a time-series study. Environ Health 18:98. https://doi.org/10.1186/s12940-019-0543-x
National Health Commission of the People’s Republic of China (2007) Diagnostic criteria for infectious diarrhea. http://www.nhc.gov.cn/wjw/s9491/200704/38817/files/4c71b9f101344f12801c94255383219f.pdf. Accessed May 10 2021
National People’s Congress of the People’s Republic of China (2013) Law of the People’s Republic of China on prevention and control of infectious diseases. http://www.nhc.gov.cn/wjw/s9491/200704/38817/files/4c71b9f101344f12801c94255383219f.pdf. Accessed 15 January 2021
Navaneethan U, Giannella RA (2008) Mechanisms of infectious diarrhea. Nat Clin Pract Gastroenterol Hepatol 5:637–647
Oh EJ, Jeon JS, Kim JK (2021) Effects of climatic factors and particulate matter on Rotavirus A infections in Cheonan, Korea, in 2010–2019. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-021-13852-3
Pitzer VE, Viboud C, Lopman BA, Patel MM, Parashar UD, Grenfell BT (2011) Influence of birth rates and transmission rates on the global seasonality of rotavirus incidence. J R Soc Interface 8:1584–1593
Qiang L, Jianping Y, Tao Y, Liu YM (2013) The relationship between daily incidence of bacillary dysentery and meteorological factors in Chengguan District, Lanzhou City. J Environ Health 30:644–646
Shane AL, Mody RK, Crump JA, Tarr PI, Steiner TS, Kotloff K, Langley JM, Wanke C, Warren CA, Cheng AC, Cantey J, Pickering LK (2017) 2017 Infectious Diseases Society of America clinical practice guidelines for the diagnosis and management of infectious diarrhea. Clin Infect Dis 65:e45–e80
Thindwa D, Chipeta MG, Henrion MYR, Gordon MA (2019) Distinct climate influences on the risk of typhoid compared to invasive non-typhoid Salmonella disease in Blantyre. Malawi Scient Rep 9:20310. https://doi.org/10.1038/s41598-019-56688-1
Trærup SL, Ortiz RA, Markandya A (2011) The costs of climate change: a study of cholera in Tanzania. Int J Environ Res Public Health 8:4386–4405. https://doi.org/10.3390/ijerph8124386
Wang H, di B, Zhang TJ, Lu Y, Chen C, Wang D, Li T, Zhang Z, Yang Z (2019a) Association of meteorological factors with infectious diarrhea incidence in Guangzhou, southern China: a time-series study (2006–2017). Sci Total Environ 672:7–15. https://doi.org/10.1016/j.scitotenv.2019.03.330
Wang H, Liu Z, Lao J, Zhao Z, Jiang B (2019) Lag effect and influencing factors of temperature on other infectious diarrhea in Zhejiang province. Zhonghua Liuxingbingxue Zazhi 40:960–964
Wang H et al (2020) Effect of ambient temperatures on category C notifiable infectious diarrhea in China: an analysis of national surveillance data. Sci Total Environ 759:143557
Wang H, Liu Z, Xiang J, Tong MX, Lao J, Liu Y, Zhang J, Zhao Z, Gao Q, Jiang B, Bi P (2021) Effect of ambient temperatures on category C notifiable infectious diarrhea in China: An analysis of national surveillance data. Sci Total Environ 759:143557. https://doi.org/10.1016/j.scitotenv.2020.143557
Wang J et al (2018) Distributed lag effects on the relationship between daily mean temperature and the incidence of bacillary dysentery in Lanzhou city. Beijing Da Xue Xue Bao 50:861–867
Wang L-X et al (2011) Typhoid and paratyphoid fever in Yunnan province: distributional patterns and the related meteorological factors. Zhonghua Liuxingbingxue Zazhi 32:485–489
Wei Y, Kouse AB, Murphy ER (2017) Transcriptional and posttranscriptional regulation of Shigella shuT in response to host-associated iron availability and temperature. Microbiologyopen 6:e00442
Wu J, Yunus M, Ali M, Escamilla V, Emch M (2018) Influences of heatwave, rainfall, and tree cover on cholera in Bangladesh. Environ Int 120:304–311. https://doi.org/10.1016/j.envint.2018.08.012
Xu C, Xiao G, Wang J, Zhang X, Liang J (2017) Spatiotemporal risk of bacillary dysentery and sensitivity to meteorological factors in Hunan Province, China. Int J Environ Res Public Health 15:47. https://doi.org/10.3390/ijerph15010047
Zhang J (2019) Effect of precipitation and temperature on other infectious diarrhea in Beijing from 2014 to 2016. Shandong University
Zhang X, Gu X, Wang L, Zhou Y, Huang Z, Xu C, Cheng C (2020) Spatiotemporal variations in the incidence of bacillary dysentery and long-term effects associated with meteorological and socioeconomic factors in China from 2013 to 2017. Sci Total Environ 755:142626
Zhang X, Gu X, Wang L, Zhou Y, Huang Z, Xu C, Cheng C (2021) Spatiotemporal variations in the incidence of bacillary dysentery and long-term effects associated with meteorological and socioeconomic factors in China from 2013 to 2017. Sci Total Environ 755:142626. https://doi.org/10.1016/j.scitotenv.2020.142626
Availability of data and materials
Not applicable.
Author information
Authors and Affiliations
Contributions
M.L.: data curation, writing, original draft preparation, software. X.D.: conceptualization, original draft preparation, methodology. Y.W.: data curation and writing—reviewing. Y.S.: supervision, writing—reviewing 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
There is no conflict of interest that exists in this manuscript, and it is approved by all authors.
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 32 kb)
Rights and permissions
About this article
Cite this article
Liang, ., Ding, X., Wu, Y. et al. Temperature and risk of infectious diarrhea: a systematic review and meta-analysis. Environ Sci Pollut Res 28, 68144–68154 (2021). https://doi.org/10.1007/s11356-021-15395-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-15395-z