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Temperature and risk of infectious diarrhea: a systematic review and meta-analysis

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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.

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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

    Article  CAS  Google Scholar 

  • Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  CAS  Google Scholar 

  • Black R, Lanata C (1995) Epidemiology of diarrheal diseases in developing countries. In: Infections of the gastrointestinal tract. Raven Press, New York

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • DerSimonian R, Laird NJ (1986) Meta-anal Clin Trials 7:177–188

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Bmj 315:629–634

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jelinski DE, Wu J (1996) The modifiable areal unit problem and implications for landscape ecology. Landsc Ecol 11:129–140

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lin M, Dong B (2008) Status of epidemiological research of infectious diarrhea. China Trop Med 8:675–677

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zhang J (2019) Effect of precipitation and temperature on other infectious diarrhea in Beijing from 2014 to 2016. Shandong University

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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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.

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Correspondence to Yehuan Sun.

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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

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