Abstract
Although a number of epidemiological studies have examined the effects of non-optimal temperatures on mortality in Europe, evidence about the mortality risks associated with exposures to hot and cold temperatures in Bulgaria is scarce. This study provides evidence about mortality attributable to non-optimal temperatures in adults aged 65 and over in Sofia, Bulgaria, between 2000 and 2017. We quantified the relationship between the daily mean temperature and mortality in the total elderly adult population aged 65 and over, among males and females aged 65 and over, as well as individuals aged 65–84 and 85 years or older. We used a distributed lag non-linear model with a 25-day lag to fully capture the effects of both cold and hot temperatures and calculated the fractions of mortality attributable to mild and extreme hot and cold temperatures. Cold temperatures had a greater impact on mortality than hot temperatures during the studied period. Most of the temperature-attributable mortality was due to moderate cold, followed by moderate heat, extreme cold, and extreme heat. The total mortality attributable to non-optimal temperatures was greater among females compared to males and among individuals aged 85 and over compared to those aged 65 to 84. The findings of this study can serve as a foundation for future research and policy development aimed at characterizing and reducing the risks from temperature exposures among vulnerable populations in the country, climate adaptation planning and improved public health preparedness, and response to non-optimal temperatures.
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Data availability
The data used in this study are available from the corresponding author on reasonable request.
References
Aboubakri O, Khanjani N, Jahani Y, Bakhtiari B (2019 May 1) Attributable risk of mortality associated with heat and heat waves: a time-series study in Kerman, Iran during 2005–2017. J Therm Biol 82:76–82
Achebak H, Devolder D, Ballester J (2019 Jul 1) Trends in temperature-related age-specific and sex-specific mortality from cardiovascular diseases in Spain: a national time-series analysis. The Lancet Planetary Health 3(7):e297–e306
Anderson BG, Bell ML. Weather-related mortality: how heat, cold, and heat waves affect mortality in the United States. Epidemiology (Cambridge, Mass.). 2009 Mar;20(2):205
Andérson GS, Ward R, Mekjavić IB (1995 Mar 1) Gender differences in physiological reactions to thermal stress. Eur J Appl Physiol Occup Physiol 71(2–3):95–101
Armstrong B, Sera F, Vicedo-Cabrera AM, Abrutzky R, Åström DO, Bell ML, Chen BY, de Sousa Zanotti Stagliorio Coelho M, Correa PM, Dang TN, Diaz MH. The role of humidity in associations of high temperature with mortality: a multicountry, multicity study. Environmental health perspectives. 2019 Sep 25;127(9):097007
Åström DO, Ebi KL, Vicedo-Cabrera AM, Gasparrini A (2018) Investigating changes in mortality attributable to heat and cold in Stockholm, Sweden. Int J Biometeorol 62(9):1777–1780
Åström DO, Veber T, Martinsone Ž, Kaļužnaja D, Indermitte E, Oudin A, Orru H (2019 Aug) Mortality related to cold temperatures in two capitals of the Baltics: Tallinn and Riga. Medicina. 55(8):429
Atsumi A, Ueda K, Irie F, Sairenchi T, Iimura K, Watanabe H, Iso H, Ota H, Aonuma K (2013) Relationship between cold temperature and cardiovascular mortality, with assessment of effect modification by individual characteristics. Circ J 77(7):1854–1861
Bai L, Woodward A, Liu Q (2014 Jul 1) Temperature and mortality on the roof of the world: a time-series analysis in three Tibetan counties, China. Sci Total Environ 485:41–48
Balmain BN, Sabapathy S, Louis M, Morris NR (2018) Aging and thermoregulatory control: the clinical implications of exercising under heat stress in older individuals. Biomed Res Int 2018:1–12
Benmarhnia T, Deguen S, Kaufman JS, Smargiassi A (2015 Nov 1) Vulnerability to heat-related mortality. Epidemiology. 26(6):781–793
Bittel J, Henane R (1975 Sep 1) Comparison of thermal exchanges in men and women under neutral and hot conditions. J Physiol 250(3):475–489
Bunker A, Wildenhain J, Vandenbergh A, Henschke N, Rocklöv J, Hajat S, Sauerborn R (2016 Apr 1) Effects of air temperature on climate-sensitive mortality and morbidity outcomes in the elderly; a systematic review and meta-analysis of epidemiological evidence. EBioMedicine. 6:258–268
Curriero FC, Heiner KS, Samet JM, Zeger SL, Strug L, Patz JA (2002 Jan 1) Temperature and mortality in 11 cities of the eastern United States. Am J Epidemiol 155(1):80–87
Davídkovová H, Plavcová E, Kynčl J, Kyselý J (2014 Dec 1) Impacts of hot and cold spells differ for acute and chronic ischaemic heart diseases. BMC Public Health 14(1):480
Dufour A, Candas V (2007 May 1) Ageing and thermal responses during passive heat exposure: sweating and sensory aspects. Eur J Appl Physiol 100(1):19–26
Falk B, Bar-Or O, Smolander J, Frost G (1994 Jan 1) Response to rest and exercise in the cold: effects of age and aerobic fitness. J Appl Physiol 76(1):72–78
Fouillet A, Rey G, Laurent F, Pavillon G, Bellec S, Guihenneuc-Jouyaux C, Clavel J, Jougla E, Hémon D (2006) Excess mortality related to the August 2003 heat wave in France. Int Arch Occup Environ Health 80(1):16–24
Gagnon D, Crandall CG, Kenny GP (2013 Feb 1) Sex differences in postsynaptic sweating and cutaneous vasodilation. J Appl Physiol 114(3):394–401
Gagnon D, Kenny GP (2012 Dec 1) Does sex have an independent effect on thermoeffector responses during exercise in the heat? J Physiol 590(23):5963–5973
Gagnon D, Kenny GP (2011 Dec 15) Sex modulates whole-body sudomotor thermosensitivity during exercise. J Physiol 589(24):6205–6217
Gasparrini A (2020) Distributed lag linear and non-linear models: the R the package DLNM. https://cran.rproject.org/web/packages/dlnm/vignettes/dlnmOverview.pdf. Accessed 28 May 2020
Gasparrini A, Guo Y, Hashizume M, Lavigne E, Zanobetti A, Schwartz J, Tobias A, Tong S, Rocklöv J, Forsberg B, Leone M (2015 Jul 25) Mortality risk attributable to high and low ambient temperature: a multicountry observational study. Lancet 386(9991):369–375
Gasparrini A, Leone M (2014 Dec 1) Attributable risk from distributed lag models. BMC Med Res Methodol 14(1):55
Goggins WB, Chan EY, Yang C, Chong M (2013 Dec) Associations between mortality and meteorological and pollutant variables during the cool season in two Asian cities with sub-tropical climates: Hong Kong and Taipei. Environ Health 12(1):59
Graczyk D, Kundzewicz ZW, Choryński A, Førland EJ, Pińskwar I, Szwed M (2019 May 1) Heat-related mortality during hot summers in Polish cities. Theor Appl Climatol 136(3–4):1259–1273
Graham TE (1988 Oct) Thermal, metabolic, and cardiovascular changes in men and women during cold stress. Med Sci Sports Exerc 20(5 Suppl):S185–S192
Hajat S, Kosatky T (2010 Sep 1) Heat-related mortality: a review and exploration of heterogeneity. J Epidemiol Community Health 64(9):753–760
Hajat S, Kovats RS, Lachowycz K (2007 Feb 1) Heat-related and cold-related deaths in England and Wales: who is at risk? Occup Environ Med 64(2):93–100
Hoegh-Guldberg, O, Jacob D, Taylor M, Bindi M, Brown S, Camilloni U, Diedhiou A, Djalante R, Ebi KL, Engelbrecht F, Guiot J, Hijioka Y, Mehrotra S, Payne A, Seneviratne S I, Thomas A, Warren R, and Zhou G, 2018: Impacts of 1.5°C global warming on natural and human systems. In: Global warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty [Masson-Delmotte, V., P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P.R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J.B.R. Matthews, Y. Chen, X. Zhou, M.I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield (eds.)]
Hondula DM, Vanos JK, Gosling SN (2014 Mar 1) The SSC: a decade of climate–health research and future directions. Int J Biometeorol 58(2):109–120
Inoue Y, Shibasaki M (1996 Aug 1) Regional differences in age-related decrements of the cutaneous vascular and sweating responses to passive heating. Eur J Appl Physiol Occup Physiol 74(1–2):78–84
Kaltsatou A, Kenny GP, Flouris AD. The impact of heat waves on mortality among the elderly: a mini systematic review. J Geriatr Med Gerontol 2018: 4:053
Keatinge WR, Donaldson GC, Cordioli E, Martinelli M, Kunst AE, Mackenbach JP, Nayha S, Vuori I (2000 Sep 16) Heat related mortality in warm and cold regions of Europe: observational study. Bmj. 321(7262):670–673
Kenney WL, Armstrong CG (1996 Feb 1) Reflex peripheral vasoconstriction is diminished in older men. J Appl Physiol 80(2):512–515
Kenney WL, Morgan AL, Farquhar WB, Brooks EM, Pierzga JM, Derr JA (1997 Apr 1) Decreased active vasodilator sensitivity in aged skin. Am J Phys Heart Circ Phys 272(4):H1609–H1614
Kenney WL, Munce TA (2003 Dec) Invited review: aging and human temperature regulation. J Appl Physiol 95(6):2598–2603
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006 Jun 1) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15(3):259–263
Lane K, Ito K, Johnson S, Gibson EA, Tang A, Matte T (2018 Apr) Burden and risk factors for cold-related illness and death in New York City. Int J Environ Res Public Health 15(4):632
Li G, Hui T, Qun L (2012) Interaction between inhalable particulate matter and apparent temperature on respiratory emergency room visits of a Hospital in Beijing. J Environ Health 29(6):483–486
Liu C, Yavar Z, Sun Q (2015 Dec 1) Cardiovascular response to thermoregulatory challenges. Am J Phys Heart Circ Phys 309(11):H1793–H1812
Ma W, Chen R, Kan H (2014 Oct 1) Temperature-related mortality in 17 large Chinese cities: how heat and cold affect mortality in China. Environ Res 134:127–133
McMichael AJ, Wilkinson P, Kovats RS, Pattenden S, Hajat S, Armstrong B, Vajanapoom N, Niciu EM, Mahomed H, Kingkeow C, Kosnik M (2008 Oct 1) International study of temperature, heat and urban mortality: the ‘ISOTHURM’project. Int J Epidemiol 37(5):1121–1131
Ministry of Environment and Water (MEW). National climate change adaptation strategy and action plan. 2019. https://www.moew.government.bg/en/climate/international-negotiations-and-adaptation/adaptation/ (Accessed 6 July 2020)
Moghadamnia MT, Ardalan A, Mesdaghinia A, Keshtkar A, Naddafi K, Yekaninejad MS (2017 Aug 4) Ambient temperature and cardiovascular mortality: a systematic review and meta-analysis. PeerJ. 5:e3574
National Institute of Meteorology (2020) http://www.meteo.bg/. Accessed 4 Jul 2020
National Statistical Institute (2020) http://www.nsi.bg/. Accessed 6 Jul 2020
Nawrot TS, Torfs R, Fierens F, de Henauw S, Hoet PH, van Kersschaever G, de Backer G, Nemery B (2007) Stronger associations between daily mortality and fine particulate air pollution in summer than in winter: evidence from a heavily polluted region in western Europe. J Epidemiol Community Health 61:146–149
Ng CF, Boeckmann M, Ueda K, Zeeb H, Nitta H, Watanabe C, Honda Y (2016 Jul 1) Heat-related mortality: effect modification and adaptation in Japan from 1972 to 2010. Glob Environ Chang 39:234–243
Nguyen JL, Schwartz J, Dockery DW (2014 Feb) The relationship between indoor and outdoor temperature, apparent temperature, relative humidity, and absolute humidity. Indoor Air 24(1):103–112
Okazaki K, Kamijo YI, Takeno Y, Okumoto T, Masuki S, Nose H (2002 Nov 1) Effects of exercise training on thermoregulatory responses and blood volume in older men. J Appl Physiol 93(5):1630–1637
Orru H, Åström DO (2017 May 1) Increases in external cause mortality due to high and low temperatures: evidence from northeastern Europe. Int J Biometeorol 61(5):963–966
Pascal M, Wagner V, Corso M, Laaidi K, Ung A, Beaudeau P (2018 Dec 1) Heat and cold related-mortality in 18 French cities. Environ Int 121:189–198
Pattenden S, Nikiforov B, Armstrong BG (2003 Aug 1) Mortality and temperature in Sofia and London. J Epidemiol Community Health 57(8):628–633
Pfeifer K, Oudin Åström D, Martinsone Ž, Kaļužnaja D, Oudin A (2020 Jan) Evaluating mortality response associated with two different Nordic heat warning systems in Riga, Latvia. Int J Environ Res Public Health 17(21):7719
Qin RX, Xiao C, Zhu Y, Li J, Yang J, Gu S, Xia J, Su B, Liu Q, Woodward A (2017) The interactive effects between high temperature and air pollution on mortality: a time-series analysis in Hefei, China. Sci Total Environ 575:1530–1537
Ren C, Williams GM, Morawska L, Mengersen K, Tong S (2008) Ozone modifies associations between temperature and cardiovascular mortality analysis of the NMMAPS data. Occup Environ Med 65:255–260
Robine JM, Cheung SL, Le Roy S, Van Oyen H et al (2008) Death toll exceeded 70,000 in Europe during the summer of 2003. Comptes Rendus Biologies 331(2):171–178
Rocklöv J, Forsberg B, Ebi K, Bellander T (2014 Dec 1) Susceptibility to mortality related to temperature and heat and cold wave duration in the population of Stockholm County, Sweden. Glob Health Action 7(1):22737
Rodrigues M, Santana P, Rocha A (2019 Apr 15) Effects of extreme temperatures on cerebrovascular mortality in Lisbon: a distributed lag non-linear model. Int J Biometeorol 63(4):549–559
Sagawa S, Shiraki K, Yousef MK, Miki K (1988 Jan 1) Sweating and cardiovascular responses of aged men to heat exposure. J Gerontol 43(1):M1–M8
Semenza JC, Rubin CH, Falter KH, Selanikio JD, Flanders WD, Howe HL, Wilhelm JL (1996) Heat-related deaths during the July 1995 heat wave in Chicago. N Engl J Med 335(2):84–90
Sheridan SC, Kalkstein LS (2004 Dec) Progress in heat watch–warning system technology. Bull Am Meteorol Soc 85(12):1931–1942
Shibasaki M, Okazaki K, Inoue Y (2013 Mar 25) Aging and thermoregulation. The Journal of Physical Fitness and Sports Medicine 2(1):37–47
Smith ET, Sheridan SC (2019 Jan 10) The influence of extreme cold events on mortality in the United States. Sci Total Environ 647:342–351
Son JY, Gouveia N, Bravo MA, De Freitas CU, Bell ML (2016 Jan 1) The impact of temperature on mortality in a subtropical city: effects of cold, heat, and heat waves in São Paulo, Brazil. Int J Biometeorol 60(1):113–121
Son JY, Lee JT, Anderson GB, Bell ML (2011 Sep 7) Vulnerability to temperature-related mortality in Seoul, Korea. Environmental Research Letters 6(3):034027
Son JY, Liu JC, Bell ML (2019 Jul 9) Temperature-related mortality: a systematic review and investigation of effect modifiers. Environ Res Lett 14(7):073004
World Health Organization (WHO) (2019) Action plan to improve public health preparedness and response in the WHO European Region 2018–2023. www.euro.who.int/en/health-topics/health-emergencies/publications/2019/action-plan-to-improve-public-health-preparedness-and-response-in-the-who-european-region-20182023. Accessed 5 Jul 2020
Yang J, Yin P, Zhou M, Ou CQ, Li M, Li J, Liu X, Gao J, Liu Y, Qin R, Xu L (2016 Jul 1) Environ Int 92:232–238
Yanovich R, Ketko I, Charkoudian N (2020 May 1) Sex differences in human thermoregulation: relevance for 2020 and beyond. Physiology. 35(3):177–184
Ye X, Wolff R, Yu W, Vaneckova P, Pan X, Tong S (2012 Jan) Ambient temperature and morbidity: a review of epidemiological evidence. Environ Health Perspect 120(1):19–28
Yu W, Hu W, Mengersen K, Guo Y, Pan X, Connell D, Tong S (2011 Jul 1) Time course of temperature effects on cardiovascular mortality in Brisbane, Australia. Heart 97(13):1089–1093
Zeng J, Zhang X, Yang J, Bao J, Xiang H, Dear K, Liu Q, Lin S, Lawrence WR, Lin A, Huang C (2017 Nov) Humidity may modify the relationship between temperature and cardiovascular mortality in Zhejiang Province, China. Int J Environ Res Public Health 14(11):1383
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The code used in this study can be provided along with the publication or upon request.
Funding
This study was partially funded by the Frontiers of Science Program at Columbia University. In addition, AG and FS were supported by the Medical Research Council-UK (Grant ID: MR/M022625/1), the Natural Environment Research Council UK (Grant ID: NE/R009384/1), and the European Union’s Horizon 2020 Project Exhaustion (Grant ID: 820655).
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Petkova, E.P., Dimitrova, L.K., Sera, F. et al. Mortality attributable to heat and cold among the elderly in Sofia, Bulgaria. Int J Biometeorol 65, 865–872 (2021). https://doi.org/10.1007/s00484-020-02064-y
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DOI: https://doi.org/10.1007/s00484-020-02064-y