Abstract
Purpose
Salmonella is one of the main causes of gastroenteritis, and its incidence may be affected by meteorological variables. This is the first study about the effect of climatic factors on salmonella incidence in Kermanshah, Iran.
Methods
Data about salmonellosis cases in Kermanshah were inquired from Center for Communicable Disease Control, at the Ministry of Health and Medical Education of Iran, for the 2008 to 2018 time-frame. Meteorological variables including maximum, minimum and mean of temperature and humidity, sunshine hours and rainfall were inquired for the same time frame. Negative binomial generalized linear models (GLM) were used to assess the effect of meteorological variables on the weekly incidence of salmonellosis.
Results
During the years under study, 569 confirmed cases were registered in Kermanshah province. Study results showed a 3 % increase in salmonellosis incidence, after 1 % increase in minimum humidity in the week before (incidence rate ratio (IRR): 1.03; 95 % confidence interval (CI):1.02–1.05) and also a 4 % increase in incidence for 1 °C increase in mean temperature in the same week (IRR: 1.04; 95 % CI:1.02–1.06).
Conclusions
Increase in minimum humidity and mean temperature may have a role in increasing the incidence of salmonellosis in Iran.
Similar content being viewed by others
Code availability
STATA software version 16.
References
World Health Organization (WHO). 2020. https://www.who.int/foodsafety/areas_work/foodborne-diseases/salmonella/en/. Accessed 20 Feb 2018.
Ryan K, Ray C. Sherris Medical Microbiology. 4th edition. McGraw Hill. 2004; 362–8.
CDC. Centers for Disease Control and Prevention. 2019. https://www.cdc.gov/salmonella/general/prevention.html. Accessed 8 Feb 2019.
Awofisayo-Okuyelu A, McCarthy N, Mgbakor I, Hall I. Incubation period of typhoidal salmonellosis: a systematic review and meta-analysis of outbreaks and experimental studies occurring over the last century. BMC Infect Dis. 2018;18(1):483.
Ghoddusi A, Nayeri Fasaei B, Zahraei Salehi T, Akbarein H. Serotype Distribution and Antimicrobial Resistance of Salmonella Isolates in Human, Chicken, and Cattle in Iran. Arch Razi Inst. 2019;74(3):259–66.
World Health Organization (WHO). 2020. https://www.who.int/health-topics/typhoid#tab=tab_1. Accessed 20 Apr 2020.
Cheng LH, Crim SM, Cole CR, Shane AL, Henao OL, Mahon BEJJotPIDS. Epidemiology of infant salmonellosis in the United States, 1996–2008: a foodborne diseases active surveillance network study. J Pediatr Infect Dis Soc. 2013;2(3):232–9.
Zhang Y, Bi P, Hiller JJ. Climate variations and salmonellosis transmission in Adelaide, South Australia: a comparison between regression models. Int J Biometeorol. 2008;52(3):179–87.
Bentham G, Langford IHJIjob. Environmental temperatures and the incidence of food poisoning in England and Wales. Int J Biometeorol. 2001;45(1):22–6.
Grjibovski A, Kosbayeva AJEJPH. Climate variations and Salmonella infection in Astana, Kazakhstan: a time-series analysis. Euro J Public Health. 2012;22:162.
Aik J, Heywood AE, Newall AT, Ng L-C, Kirk MD, Turner RJSoTTE. Climate variability and salmonellosis in Singapore–A time series analysis. Sci Total Environ. 2018;639:1261–7.
Lake I, Gillespie I, Bentham G, Nichols G, Lane C, Adak G, et al. A re-evaluation of the impact of temperature and climate change on foodborne illness. Epidemiol Infect. 2009;137(11):1538–47.
Wang P, Goggins WB, Chan EYJEi. Associations of Salmonella hospitalizations with ambient temperature, humidity and rainfall in Hong Kong. Environ Int. 2018;120:223–30.
Zhang Y, Bi P, Hiller JEJSotTE. Climate variations and Salmonella infection in Australian subtropical and tropical regions. Sci Total Environ. 2010;408(3):524–30.
Stephen DM, Barnett AGJBo. Effect of temperature and precipitation on salmonellosis cases in South-East Queensland, Australia: an observational study. BMJ Open. 2016;6(2):e010204.
Jiang C, Shaw KS, Upperman CR, Blythe D, Mitchell C, Murtugudde R, et al. Climate change, extreme events and increased risk of salmonellosis in Maryland, USA: Evidence for coastal vulnerability. Environ Int. 2015;83:58–62.
Ehrampoush MH, Soltandallal MM, Dehghani Tafti AA, Yaseri M, Aminharati F. Surveillance of foodborne illnesses in association with ecological conditions in Yazd province, Iran. J Disaster Emerg Res. 2020;1(1):5–13.
Bradley MJ, Kutz SJ, Jenkins E, O’hara TMJI, Jo CH. The potential impact of climate change on infectious diseases of Arctic fauna. Int J Circumpolar Health. 2005;64(5):468–77. https://doi.org/10.3402/ijch.v64i5.18028.
Fleury M, Charron DF, Holt JD, Allen OB, Maarouf AR. A time series analysis of the relationship of ambient temperature and common bacterial enteric infections in two Canadian provinces. Int J Biometeorol. 2006;50(6):385–91.
Jiang C, Shaw KS, Upperman CR, Blythe D, Mitchell C, Murtugudde R, et al. Climate change, extreme events and increased risk of salmonellosis in Maryland, USA: Evidence for coastal vulnerability. Environ Int. 2015;83:58–62.
Lal A, Hales S, French N, Baker MGJPO. Seasonality in human zoonotic enteric diseases: a systematic review. PLoS One. 2012;7(4):e31883.
Kovats R, Edwards S, Hajat S, Armstrong B, Ebi K, Menne BJE, et al. The effect of temperature on food poisoning: a time-series analysis of salmonellosis in ten European countries. Epidemiol Infect. 2004;132(3):443–53.
Gast RK, Porter RE Jr. Salmonella infections. Diseases of poultry. 2020. p. 717–53.
Rajabi A, Shabanlou S. Climate index changes in future by using SDSM in Kermanshah, Iran. J Environ Res Dev. 2012;7(1):37–44.
tabatabai MZM, Ahmadnia H, Ghotbi M, Rahimi F. In: M M, editor. Principle of prevention and surviellane of disease. Tehran: Department of Communicable Disease at the Ministry of Health and Medical Education of Iran; 2007. p. 185–9.
Salmerón R, García C, García J. Variance inflation factor and condition number in multiple linear regression. J Stat Comput Simul. 2018;88(12):2365–84.
Hilbe J. Negative binomial overdispersion. Negative Binomial Regression. New York: Cambridge University Press; 2011. pp. 180–5.
Vuong QH. Likelihood ratio tests for model selection and non-nested hypotheses. Econometrica. 1989:307–33.
Hilbe JM. Negative binomial regression. 2nd ed. Cambridge: Cambridge University Press; 2011.
Dewan AM, Corner R, Hashizume M, Ongee ETJPntd. 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. 2013;7(1):e1998.
Grjibovski A, Kosbayeva A, Menne BJE, Infection. The effect of ambient air temperature and precipitation on monthly counts of salmonellosis in four regions of Kazakhstan, Central Asia, in 2000–2010. Epidemiol Infect. 2014;142(3):608–15.
Micallef SA, Goldstein RER, George A, Kleinfelter L, Boyer MS, McLaughlin CR, et al. Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on mid-Atlantic tomato farms. Environ Res. 2012;114:31–9.
Lublin A, Sela SJPs. The impact of temperature during the storage of table eggs on the viability of Salmonella enterica serovars Enteritidis and Virchow in the eggs. Poult Sci. 2008;87(11):2208–14.
Allen RL, Warren BR, Archer DL, Schneider KR, Sargent SAJH. Survival of Salmonella spp on the surfaces of fresh tomatoes selected packing line materials. Horttechnology. 2005;15(4):831–6.
Smadi H, Sargeant JM, Shannon HS, Raina PJ. Growth and inactivation of Salmonella at low refrigerated storage temperatures and thermal inactivation on raw chicken meat and laboratory media: mixed effect meta-analysis. J Epidemiol Glob Health. 2012;2(4):165–79.
Heyndrickx M, Vandekerchove D, Herman L, Rollier I, Grijspeerdt K, De Zutter LJE, et al. Routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiol Infect. 2002;129(2):253–65.
Adak G, Long S, O’brien SJG. Trends in indigenous foodborne disease and deaths, England and Wales: 1992 to 2000. Gut. 2002;51(6):832–41.
Wang P, Goggins WB, Chan EY. Associations of Salmonella hospitalizations with ambient temperature, humidity and rainfall in Hong Kong. Environ Int. 2018;120:223–30.
Kinsella K, Prendergast D, McCann M, Blair I, McDowell D, Sheridan J. The survival of Salmonella enterica serovar Typhimurium DT104 and total viable counts on beef surfaces at different relative humidities and temperatures. J Appl Microbiol. 2009;106(1):171–80.
Iturriaga MH, Tamplin ML, Escartin EF. Colonization of tomatoes by Salmonella Montevideo is affected by relative humidity and storage temperature. J Food Prot. 2007;70(1):30–4.
Bi P, Cameron AS, Zhang Y, Parton KAJJoI. Weather and notified Campylobacter infections in temperate and sub-tropical regions of Australia: an ecological study. J Infect. 2008;57(4):317–23.
Liu Z, Lao J, Zhang Y, Liu Y, Zhang J, Wang H, et al. Association between floods and typhoid fever in Yongzhou, China: Effects and vulnerable groups. Environ Res. 2018;167:718–24.
Funding
This study was supported by Grant No.97–429, from Kerman University of Medical Sciences, Kerman, Iran.
Author information
Authors and Affiliations
Contributions
NK suggested the topic, was the main supervisor, and helped in writing and editing the final manuscript. SN acquired the data, cleaned the data, analyzed the data and prepared the initial draft. BB provided scientific advice and edited the final article. YJ supervised data analysis, provided statistical consultation and edited the final manuscript. HD helped in inquiring meteorological data, cleaning the data, and writing the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethics approval
The study proposal was approved by the Ethics Committee of Kerman University of Medical Science. Ethics Code: IR.KMU.REC.1397.231.
Consent to participate
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nili, S., Khanjani, N., Bakhtiari, B. et al. The effect of meteorological variables on salmonellosis incidence in Kermanshah, West of Iran: a generalized linear model with negative binomial approach. J Environ Health Sci Engineer 19, 1171–1177 (2021). https://doi.org/10.1007/s40201-021-00684-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40201-021-00684-z