Crump JA, Mintz ED , 2010. Global trends in typhoid and paratyphoid fever. Clin Infect Dis 50: 241–246.
Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ , 2002. Typhoid fever. N Engl J Med 347: 1770–1782.
Popoff MY, Bockemühl J, Gheesling LL , 2004. Supplement 2002 (no. 46) to the Kauffmann-White scheme. Res Microbiol 155: 568–570.
Vollaard AM, Ali S, van Asten HA, Widjaja S, Visser LG, Surjadi C, van Dissel JT , 2004. Risk factors for typhoid and paratyphoid fever in Jakarta, Indonesia. JAMA 291: 2607–2615.
Stanaway JD, Reiner RC, Blacker BF, Goldberg EM, Khalil IA, Troeger CE, Andrews JR, Bhutta ZA , 2019. The global burden of typhoid and paratyphoid fevers: a systematic analysis for the global burden of disease study 2017. Lancet Infect Dis 19: 369–381.
Vos T, Barber RM, Bell B, Bertozzi-Villa A, Biryukov S, Bolliger I, Charlson F, Davis A , 2015. Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990–2013: a systematic analysis for the global burden of disease study 2013. Lancet 386: 743–800.
Cao Y, Han YY, Liu FF, Liao QH, Li J, Diao BW, Fan FX, Kan B, Yan MY , 2018. Epidemiological characteristics and molecular typing of typhoid and paratyphoid in China, 2009–2013 [in Chinese]. Chin J Epidemiol 39: 337–341.
DCFPH , 2014. National Notifiable Infectious Disease Database [in Chinese]. Available at: http://www.phsciencedata.cn/Share/ky_sjml.jsp. Accessed September 2020.
Zhao Q et al.2018. Modeling the present and future incidence of pediatric hand, foot, and mouth disease associated with ambient temperature in mainland China. Environ Health Perspect 126: 047010.
Shuman EK , 2011. Global climate change and infectious diseases. Int J Occup Environ Med 2: 11–19.
IPCC , 2018. Special Report on Global Warming of 1.5°C. Cambridge, United Kingdom: Cambridge University Press.
Waits A, Emelyanova A, Oksanen A, Abass K, Rautio A , 2018. Human infectious diseases and the changing climate in the Arctic. Environ Int 121: 703–713.
Zhang Y, Bi P, Hiller JE , 2007. Climate change and disability-adjusted life years. J Environ Health 70: 32–36.
Patz JA, Engelberg D, Last J , 2000. The effects of changing weather on public health. Annu Rev Public Health 21: 271–307.
Rakotomanana F, Ratovonjato J, Randremanana RV, Randrianasolo L, Raherinjafy R, Rudant JP, Richard V , 2010. Geographical and environmental approaches to urban malaria in Antananarivo (Madagascar). BMC Infect Dis 10: 173.
Sheffield PE, Landrigan PJ , 2011. Global climate change and children’s health: threats and strategies for prevention. Environ Health Perspect 119: 291–298.
Saad NJ, Lynch VD, Antillón M, Yang C, Crump JA, Pitzer VE , 2018. Seasonal dynamics of typhoid and paratyphoid fever. Sci Rep 8: 6870.
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.
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. Sci Rep 9: 20310.
Wang H, Di B, Zhang T, Lu Y, Chen C, Wang D, Li T, Zhang Z, Yang Z , 2019. Association of meteorological factors with infectious diarrhea incidence in Guangzhou, southern China: a time-series study (2006–2017). Sci Total Environ 672: 7–15.
D’Souza RM, Becker NG, Hall G, Moodie KB , 2004. Does ambient temperature affect foodborne disease? Epidemiology 15: 86–92.
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.
Ali M, Kim DR, Yunus M, Emch M , 2013. Time series analysis of cholera in Matlab, Bangladesh, during 1988–2001. J Health Popul Nutr 31: 11–19.
Moors E, Singh T, Siderius C, Balakrishnan S, Mishra A , 2013. Climate change and waterborne diarrhoea in northern India: impacts and adaptation strategies. Sci Total Environ 468–469: S139–S151.
Baker S et al.2011. Combined high-resolution genotyping and geospatial analysis reveals modes of endemic urban typhoid fever transmission. Open Biol 1: 110008.
Karkey A et al.2016. The ecological dynamics of fecal contamination and Salmonella typhi and Salmonella Paratyphi A in municipal Kathmandu drinking water. PLoS Negl Trop Dis 10: e0004346.
Feasey NA et al.2015. Modelling the contributions of malaria, HIV, malnutrition and rainfall to the decline in paediatric invasive non-typhoidal Salmonella disease in Malawi. PLoS Negl Trop Dis 9: e0003979.
Pitzer VE, Feasey NA, Msefula C, Mallewa J, Kennedy N, Dube Q, Denis B, Gordon MA, Heyderman RS , 2015. Mathematical modeling to assess the drivers of the recent emergence of typhoid fever in Blantyre, Malawi. Clin Infect Dis 61(Suppl 4): S251–S258.
Wang P, Goggins WB, Chan EYY , 2018. Associations of Salmonella hospitalizations with ambient temperature, humidity and rainfall in Hong Kong. Environ Int 120: 223–230.
Bureau TMS , 2019. Statistical Information Manual of Taizhou in 2019. Available at: http://tjj.zjtz.gov.cn/. Accessed September 20, 2020.
Zhou JX, 2009. Taizhou climate impact assessment in 2008 [in Chinese]. Anhui Agric Sci Bulletin 15: 162–164.
Shi XM, Guo Y, Wang LP, Qi XP, Zhang CX, Guo Q, JQ M , 2007. Analysis on the quality of notifiable infectious diseases reporting at medical health units in China [in Chinese]. Chin J Dis Control Prev 3: 266–269.
Hu YF, Chang Y, W l , 2016. Report of infectious diseases by medical institutions in Taizhou [in Chinese]. Prev Med 28: 1262–1264.
NHC , 2006. The Measures for Administration of Public Health Emergencies and Communicable Disease Monitoring Information Reporting (Ministry of Health Order No. 37) [in Chinese]. Available at: http://www.moh.gov.cn/mohzcfgs/pgz/200901/38689. shtml. Accessed September 2020.
NHC , 2008. Diagnostic Criteria for Typhoid Fever and Paratyphoid Fever (WS 280–2008) [in Chinese]. Available at: http://www.nhfpc.gov.cn/zhuz/s9491/200802/38820.shtml. Accessed September 2020.
Bhan MK, Bahl R, Bhatnagar S , 2005. Typhoid and paratyphoid fever. Lancet 366: 749–762.
Zhang Z , 2016. Introduction to machine learning: k-nearest neighbors. Ann Transl Med 4: 218.
Figueiras A, Roca-Pardiñas J, Cadarso-Suárez C , 2005. A bootstrap method to avoid the effect of concurvity in generalised additive models in time series studies of air pollution. J Epidemiol Community Health 59: 881–884.
Imai C, Hashizume M , 2015. A systematic review of methodology: time series regression analysis for environmental factors and infectious diseases. Trop Med Health 43: 1–9.
Gasparrini A , 2011. Distributed lag linear and non-linear models in R: the package dlnm. J Stat Softw 43: 1–20.
Hu W, Li Y, Han W, Xue L, Zhang W, Ma W, Bi P , 2018. Meteorological factors and the incidence of mumps in Fujian Province, China, 2005–2013: non-linear effects. Sci Total Environ 619–620 : 1286–1298.
Gasparrini A , 2014. Modeling exposure-lag-response associations with distributed lag non-linear models. Stat Med 33: 881–899.
Stolwijk AM, Straatman H, Zielhuis GA , 1999. Studying seasonality by using sine and cosine functions in regression analysis. J Epidemiol Community Health 53: 235–238.
Li LJ, Ren H , 2013. Infectious Disease. Beijing, China: People’s Medical Publishing House.
Wang LX, Li XJ, Fang LQ, Wang DC, Cao WC, Kan B , 2012. Association between the incidence of typhoid and paratyphoid fever and meteorological variables in Guizhou, China. Chin Med J (Engl) 125: 455–460.
Mervyn S, 1977. An asymptotic equivalence of choice of model by cross-validation and Akaike’s criterion. J Roy Statist Soc Ser B 1: 44–47.
Gasparrini A, Leone M , 2014. Attributable risk from distributed lag models. BMC Med Res Methodol 14: 55.
Li M, Lin HJ , 2015. Epidemiological analysis of typhoid and paratyphoid fever in Taizhou city from 2008 to 2013 [in Chinese]. Shanghai J Prev Med 27: 328–329.
Milazzo A, Giles LC, Zhang Y, Koehler AP, Hiller JE, Bi P , 2016. The effect of temperature on different Salmonella serotypes during warm seasons in a Mediterranean climate city, Adelaide, Australia. Epidemiol Infect 144: 1231–1240.
Britton E, Hales S, Venugopal K, Baker MG , 2010. Positive association between ambient temperature and salmonellosis notifications in New Zealand, 1965–2006. Aust N Z J Public Health 34: 126–129.
Huang D, Guan P, Guo J, Wang P, Zhou B , 2008. Investigating the effects of climate variations on bacillary dysentery incidence in northeast China using ridge regression and hierarchical cluster analysis. BMC Infect Dis 8: 130.
Hashizume M, Armstrong B, Hajat S, Wagatsuma Y, Faruque AS, Hayashi T, Sack DA , 2007. Association between climate variability and hospital visits for non-cholera diarrhoea in Bangladesh: effects and vulnerable groups. Int J Epidemiol 36: 1030–1037.
Liu Z, Lao J, Zhang Y, Liu Y, Zhang J, Wang H, Jiang B , 2018. Association between floods and typhoid fever in Yongzhou, China: effects and vulnerable groups. Environ Res 167: 718–724.
Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM , 2015. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev 28: 901–937.
Gu H, Fan W, Liu K, Qin S, Li X, Jiang J, Chen E, Zhou Y, Jiang Q , 2017. Spatio-temporal variations of typhoid and paratyphoid fevers in Zhejiang Province, China from 2005 to 2015. Sci Rep 7: 5780.
Checkley W, Epstein LD, Gilman RH, Figueroa D, Cama RI, Patz JA, Black RE , 2000. Effect of El Nino and ambient temperature on hospital admissions for diarrhoeal diseases in Peruvian children. Lancet 355: 442–450.
Mackey BM, Kerridge AL , 1988. The effect of incubation temperature and inoculum size on growth of salmonellae in minced beef. Int J Food Microbiol 6: 57–65.
Nygren BL, Schilling KA, Blanton EM, Silk BJ, Cole DJ, Mintz ED , 2013. Foodborne outbreaks of shigellosis in the USA, 1998–2008. Epidemiol Infect 141: 233–241.
Kovats RS, Edwards SJ, Hajat S, Armstrong BG, Ebi KL, 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.
Semenza JC, Wilson DJ, Parra J, Bontempo BD, Hart M, Sailor DJ, George LA , 2008. Public perception and behavior change in relationship to hot weather and air pollution. Environ Res 107: 401–411.
Xu Z, Liu Y, Ma Z, Sam Toloo G, Hu W, Tong S , 2014. Assessment of the temperature effect on childhood diarrhea using satellite imagery. Sci Rep 4: 5389.
Kelly-Hope LA, Alonso WJ, Thiem VD, Anh DD, Canh DG, Lee H, Smith DL, Miller MA , 2007. Geographical distribution and risk factors associated with enteric diseases in Vietnam. Am J Trop Med Hyg 76: 706–712.
Kouadio IK, Aljunid S, Kamigaki T, Hammad K, Oshitani H , 2012. Infectious diseases following natural disasters: prevention and control measures. Expert Rev Anti Infect Ther 10: 95–104.
Akullian A et al.2015. Environmental transmission of typhoid fever in an Urban Slum. PLoS Negl Trop Dis 9: e0004212.
Guan P, Huang D, Guo J, Wang P, Zhou B , 2008. Bacillary dysentery and meteorological factors in northeastern China: a historical review based on classification and regression trees. Jpn J Infect Dis 61: 356–360.
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.
Singh RB, Hales S, de Wet N, Raj R, Hearnden M, Weinstein P , 2001. The influence of climate variation and change on diarrheal disease in the Pacific Islands. Environ Health Perspect 109: 155–159.
Yi L et al.2019. The impact of climate variability on infectious disease transmission in China: current knowledge and further directions. Environ Res 173: 255–261.
Gao Q, Liu Z, Xiang J, Tong M, Zhang Y, Wang S, Zhang Y, Lu L, Jiang B, Bi P , 2020. Forecast and early warning of hand, foot, and mouth disease based on meteorological factors: evidence from a multicity study of 11 meteorological geographical divisions in mainland China. Environ Res 192: 110301.
Huang C, Barnett AG, Xu Z, Chu C, Wang X, Turner LR, Tong S , 2013. Managing the health effects of temperature in response to climate change: challenges ahead. Environ Health Perspect 121: 415–419.
Kolstad EW, Johansson KA , 2011. Uncertainties associated with quantifying climate change impacts on human health: a case study for diarrhea. Environ Health Perspect 119: 299–305.
WHO , 2008. Typhoid vaccines: WHO position paper. Wkly Epidemiol Rec 83: 49–59.
Ekdahl K, de Jong B, Andersson Y , 2005. Risk of travel-associated typhoid and paratyphoid fevers in various regions. J Travel Med 12: 197–204.
Christie AB , 1987. Infectious Diseases: Epidemiology and Clinical Practice, 4th edition. Edinburgh, Scotland: Churchill Livingstone.
Shang XP, Wu C, Wu HC , 2015. An investigation on the quality of infectious disease report in the medical institutions in Zhejiang province [in Chinese]. Zhejiang Prev Med 27: 635–637.
The impact of temperature and rainfall on the occurrence of typhoid/paratyphoid fever are not fully understood. This study aimed to characterize the effect of daily ambient temperature and total rainfall on the incidence of typhoid/paratyphoid in a sub-tropical climate city of China and to identify the vulnerable groups for disease prevention. Daily notified typhoid/paratyphoid fever cases and meteorological data for Taizhou from 2005 to 2013 were extracted from the National Notifiable Disease Surveillance System and the Meteorological Data Sharing Service System, respectively. Distributed lag nonlinear model was used to quantify the association between daily mean temperature, total rainfall, and typhoid/paratyphoid fever. Subgroup analyses by gender, age, and occupation were conducted to identify the vulnerable groups. A total of 625 typhoid fever cases and 1,353 paratyphoid fever cases were reported during the study period. An increased risk of typhoid fever was detected with the increase of temperature (Each 2°C rise resulted in 6%, 95% [confidence interval] CI: 2–10% increase in typhoid cases), while the increased risk was associated with the higher temperature for paratyphoid (the highest cumulative risk of temperature was 33.40 [95% CI: 12.23–91.19] at 33°C). After the onset of mild precipitation, the relative risk of typhoid fever increased in a short-lasting and with a 13–26 days delay, and the risk was no significant after the continuous increase of precipitation (the highest cumulative risk of rainfall was 24.96 [95% CI: 4.54–87.21] at 100 mm). Whereas the risk of paratyphoid fever was immediate and long lasting, and increase rapidly with the increase of rainfall (each 100 mm increase was associated with 26% increase in paratyphoid fever cases). Significant temperature-typhoid/paratyphoid fever and rainfall-typhoid/paratyphoid fever associations were found in both genders and those aged 0–4 years old, 15–60 years old, farmers, and children. Characterized with a lagged, nonlinear, and cumulative effect, high temperature and rainfall could increase the risk of typhoid/paratyphoid fever in regions with a subtropical climate. Public health interventions such as early warning and community health education should be taken to prevent the increased risk of typhoid/paratyphoid fever, especially for the vulnerable groups.
These authors contributed equally to this article and share the first authorship.
Disclosure: This study was approved by the Ethical Review Committee of Public Health of Shandong University (approval no. 20120501).
Financial support: This work was supported by the Special Foundation of Basic Science and Technology Resources Survey of Ministry of Science and Technology (Grant No. 2017FY101202) and the National Basic Research Program of China (973 Program) (Grant No. 2012CB955502).
Authors’ addresses: Qi Gao and Baofa Jiang, Department of Epidemiology and Biostatistics, School of Public Health, Shandong University, Jinan, Shandong Province, People’s Republic of China, and Shandong University Climate Change and Health Center, Cheeloo College of Medicine, Jinan, Shandong Province, People’s Republic of China, E-mails: gqi6835@126.com and bjiang@sdu.edu.cn. Zhidong Liu, Department of Personnel, Qilu Hospital of Shandong University, Jinan, Province, People’s Republic of China, E-mail: liuzhidong3105@163.com. Jianjun Xiang, School of Public Health, The University of Adelaide, Adelaide, South Australia, Australia, and School of Public Health, Fujian Medical University, Fuzhou, People’s Republic of China, E-mail: jianjun.xiang@adelaide.edu.au. Ying Zhang, School of Public Health, China Studies Centre, The University of Sydney, New South Wales, Australia, E-mail: ying.zhang@sydney.edu.au. Michael Xiaoliang Tong and Peng Bi, School of Public Health, The University of Adelaide, Adelaide, South Australia, Australia, E-mails: michael.tong@adelaide.edu.au and peng.bi@adelaide.edu.au. Shuzi Wang, Shandong Center for Disease Control and Prevention, Jinan, Shandong Province, People’s Republic of China, E-mail: wangshuzi830@163.com. Yiwen Zhang, Yunnan Center for Disease Control and Prevention, Kunming, Yunnan Province, People’s Republic of China, E-mail: zhangyiwen@mail.sdu.edu.cn. Qiyong Liu, Shandong University Climate Change and Health Center, Cheeloo College of Medicine, Jinan, Shandong Province, People’s Republic of China, and State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People’s Republic of China, E-mail: liuqiyong@icdc.cn.