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The association of extreme temperatures and the incidence of tuberculosis in Japan

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Abstract

Seasonal variation in the incidence of tuberculosis (TB) has been widely assumed. However, few studies have investigated the association between extreme temperatures and the incidence of TB. We collected data on cases of TB and mean temperature in Fukuoka, Japan for 2008–2012 and used time-series analyses to assess the possible relationship of extreme temperatures with TB incident cases, adjusting for seasonal and interannual variation. Our analysis revealed that the occurrence of extreme heat temperature events resulted in a significant increase in the number of TB cases (relative risk (RR) 1.20, 95 % confidence interval (CI) 1.01–1.43). We also found that the occurrence of extreme cold temperature events resulted in a significant increase in the number of TB cases (RR 1.23, 95 % CI 1.05–1.45). Sex and age did not modify the effect of either heat or cold extremes. Our study provides quantitative evidence that the number of TB cases increased significantly with extreme heat and cold temperatures. The results may help public health officials predict extreme temperature-related TB incidence and prepare for the implementation of preventive public health interventions.

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Abbreviations

CI:

Confidence interval

RR:

Relative risk

TB:

Tuberculosis

References

  • Akhtar S, Mohammad HG (2008) Seasonality in pulmonary tuberculosis among migrant workers entering Kuwait. BMC Infect Dis 8:3

    Article  Google Scholar 

  • Anderson BG, Bell ML (2009) Weather-related mortality: how heat, cold, and heat waves affect mortality in the United States. Epidemiology 20:205–213

    Article  Google Scholar 

  • Armstrong B (2006) Models for the relationship between ambient temperature and daily mortality. Epidemiology 17:624–631

    Article  Google Scholar 

  • Astrom DO, Forsberg B, Edvinsson S, Rocklov J (2013) Acute fatal effects of short-lasting extreme temperatures in Stockholm, Sweden: evidence across a century of change. Epidemiology 24:820–829

    Article  Google Scholar 

  • Atun RA, Samyshkin YA, Drobniewski F, Kuznetsov SI, Fedorin IM, Coker RJ (2005) Seasonal variation and hospital utilization for tuberculosis in Russia: hospitals as social care institutions. Eur J Public Health 15:350–354

    Article  CAS  Google Scholar 

  • Bassil KL, Cole DC (2010) Effectiveness of public health interventions in reducing morbidity and mortality during heat episodes: a structured review. Int J Environ Res Public Health 7:991–1001

    Article  Google Scholar 

  • Belay M, Bjune G, Ameni G, Abebe F (2012) Diagnostic and treatment delay among tuberculosis patients in Afar egion, Ethiopia: a cross-sectional study. BMC Public Health 12:369

    Article  Google Scholar 

  • Borgdorff MW, Sebek M, Geskus RB, Kremer K, Kalisvaart N, van Soolingen D (2011) The incubation period distribution of tuberculosis estimated with a molecular epidemiological approach. Int J Epidemiol 40:964–970

    Article  Google Scholar 

  • Brumback B, Burge HA, Neas LM, Ryan LM, Schwartz JD, Stark PC (2000) Transitional regression models, with application to environmental time series. J Am Stat Assoc 95:16–27

    Article  Google Scholar 

  • Cegielski JP, McMurray DN (2004) The relationship between malnutrition and tuberculosis: evidence from studies in humans and experimental animals. Int J Tuberc Lung Dis 8:286–298

    CAS  Google Scholar 

  • Douglas AS, Strachan DP, Maxwell JD (1996) Seasonality of tuberculosis: the reverse of other respiratory diseases in the UK. Thorax 51:944–946

    Article  CAS  Google Scholar 

  • Fares A (2011) Seasonality of tuberculosis. J Glob Infect Dis 3:46–55

    Article  Google Scholar 

  • Fukuoka Prefectural Government. Fukuoka Prefecture Migration Survey. http://www.pref.fukuoka.lg.jp/dataweb/search-1-1619.html Accessed 31 Jul 2014

  • Fukuoka Prefectural Government. Fukuoka Prefecture Tuberculosis Report 2013. http://www.pref.fukuoka.lg.jp/contents/tbc-2013.html Accessed 31 Jul 2014

  • Gasparrini A, Armstrong B, Kenward MG (2010) Distributed lag non-linear models. Stat Med 29:2224–2234

    Article  CAS  Google Scholar 

  • Janmeja AK, Mohapatra PR (2005) Seasonality of tuberculosis. Int J Tuberc Lung Dis 9:704–705

    Google Scholar 

  • Korthals Altes H, Kremer K, Erkens C, van Soolingen D, Wallinga J (2012) Tuberculosis seasonality in the Netherlands differs between natives and non-natives: a role for vitamin D deficiency? Int J Tuberc Lung Dis 16:639–644

    CAS  Google Scholar 

  • Lawn SD, Zumla AI (2011) Tuberculosis. Lancet 378:57–72

    Article  Google Scholar 

  • Leung CC, Yew WW, Chan TY, Tam CM, Chan CY, Chan CK et al (2005) Seasonal pattern of tuberculosis in Hong Kong. Int J Epidemiol 34:924–930

    Article  Google Scholar 

  • Liao CM, Hsieh NH, Huang TL, Cheng YH, Lin YJ, Chio CP et al (2012) Assessing trends and predictors of tuberculosis in Taiwan. BMC Public Health 12:29

    Article  Google Scholar 

  • Lillebaek T, Dirksen A, Baess I, Strunge B, Thomsen VO, Andersen AB (2002) Molecular evidence of endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J Infect Dis 185:401–404

    Article  CAS  Google Scholar 

  • Lin YJ, Liao CM (2014) Seasonal dynamics of tuberculosis epidemics and implications for multidrug-resistant infection risk assessment. Epidemiol Infect 142:358–370

    Article  Google Scholar 

  • Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJL (2006) Global burden of disease and risk factors. World Bank, Washington

    Book  Google Scholar 

  • Luquero FJ, Sanchez-Padilla E, Simon-Soria F, Eiros JM, Golub JE (2008) Trend and seasonality of tuberculosis in Spain, 1996–2004. Int J Tuberc Lung Dis 12:221–224

    CAS  Google Scholar 

  • McCullagh P, Nelder J (1989) Generalized linear models. Chapman and Hall, London

    Book  Google Scholar 

  • Ministry of Health, Labour and Welfare (2013) Act on prevention of infectious diseases and medical care for patients suffering infectious diseases. http://www.mhlw.go.jp/bunya/kenkou/kekkaku-kansenshou11/01.html Accessed 1 April 2014

  • Ministry of Justice. Report on Internal Migration in Japan. http://www.moj.go.jp/housei/toukei/toukei_ichiran_nyukan.html Accessed 31 Jul 2014

  • Naranbat N, Nymadawa P, Schopfer K, Rieder HL (2009) Seasonality of tuberculosis in an Eastern-Asian country with an extreme continental climate. Eur Respir J 34:921–925

    Article  CAS  Google Scholar 

  • Parrinello CM, Crossa A, Harris TG (2012) Seasonality of tuberculosis in New York City, 1990–2007. Int J Tuberc Lung Dis 16:32–37

    Article  CAS  Google Scholar 

  • Rios M, Garcia JM, Sanchez JA, Perez D (2000) A statistical analysis of the seasonality in pulmonary tuberculosis. Eur J Epidemiol 16:483–488

    Article  CAS  Google Scholar 

  • Sita-Lumsden A, Lapthorn G, Swaminathan R, Milburn HJ (2007) Reactivation of tuberculosis and vitamin D deficiency: the contribution of diet and exposure to sunlight. Thorax 62:1003–1007

    Article  CAS  Google Scholar 

  • Soetens LC, Boshuizen HC, Korthals Altes H (2013) Contribution of seasonality in transmission of Mycobacterium tuberculosis to seasonality in tuberculosis disease: a simulation study. Am J Epidemiol 178:1281–1288

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tattevin P, Che D, Fraisse P, Gatey C, Guichard C, Antoine D et al (2012) Factors associated with patient and health care system delay in the diagnosis of tuberculosis in France. Int J Tuberc Lung Dis 16:510–515

    Article  CAS  Google Scholar 

  • Thorpe LE, Frieden TR, Laserson KF, Wells C, Khatri GR (2004) Seasonality of tuberculosis in India: is it real and what does it tell us? Lancet 364:1613–1614

    Article  Google Scholar 

  • Vynnycky E, Fine PE (2000) Lifetime risks, incubation period, and serial interval of tuberculosis. Am J Epidemiol 152:247–263

    Article  CAS  Google Scholar 

  • Wilkinson RJ, Llewelyn M, Toossi Z, Patel P, Pasvol G, Lalvani A et al (2000) Influence of vitamin D deficiency and vitamin D receptor polymorphisms on tuberculosis among Gujarati Asians in west London: a case–control study. Lancet 355:618–621

    Article  CAS  Google Scholar 

  • Willis MD, Winston CA, Heilig CM, Cain KP, Walter ND, Mac Kenzie WR (2012) Seasonality of tuberculosis in the United States, 1993–2008. Clin Infect Dis 54:1553–1560

    Article  Google Scholar 

  • World Health Organization (WHO) (2013) Global tuberculosis report 2013. http://www.who.int/tb/publications/global_report/en/index.html Accessed 1 April 2014

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Acknowledgments

We thank the Fukuoka Prefectural Government, Department of Public Health and Medical Affairs, Division of Public Health for their painstaking efforts in infectious disease surveillance in Fukuoka, Japan.

Financial disclosure

The study was supported by grants from the Ministry of Health, Labour and Welfare, Japan, and budgets for research of the Department of Public Health and Medical Affairs, Fukuoka Prefectural Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author contributions

DO has made substantial contributions to conception and design, analyzed data, and wrote the manuscript. AH was involved in drafting the manuscript and critically revising it for important intellectual content.

Conflict of interest

The authors have declared that no competing interests exist.

Ethics approval

The study was approved by the ethics committee at Fukuoka Prefectural Government. The requirement for written informed consent was waived. Patient records and other patient information were anonymized and de-identified prior to analysis.

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Corresponding author

Correspondence to Daisuke Onozuka.

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Figure S1

Diagnostics of models: (a) plots of model residuals, (b) predicted and observed time-series plots, and (c) partial autocorrelation function of the residuals. (GIF 85 kb)

(TIFF 1631 kb)

Figure S2

Crude relationship between the relative risk (RR) of TB (scaled to the mean weekly number of TB cases) and temperature (shown as a 3 df natural cubic spline): (a) over lag periods of 0 to 3 weeks, and (b) over lag periods of 0 to 5 weeks. The center line in the graph shows the estimated spline curve. (GIF 52 kb)

(TIFF 1444 kb)

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Onozuka, D., Hagihara, A. The association of extreme temperatures and the incidence of tuberculosis in Japan. Int J Biometeorol 59, 1107–1114 (2015). https://doi.org/10.1007/s00484-014-0924-3

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  • DOI: https://doi.org/10.1007/s00484-014-0924-3

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