Mean air temperature as a risk factor for stroke mortality in São Paulo, Brazil

  • Priscilla V. Ikefuti
  • Ligia V. Barrozo
  • Alfésio L. F. Braga
Original Paper

Abstract

In Brazil, chronic diseases account for the largest percentage of all deaths among men and women. Among the cardiovascular diseases, stroke is the leading cause of death, accounting for 10% of all deaths. We evaluated associations between stroke and mean air temperature using recorded mortality data and meteorological station data from 2002 to 2011. A time series analysis was applied to 55,633 mortality cases. Ischemic and hemorrhagic strokes (IS and HS, respectively) were divided to test different impact on which subgroup. Poisson regression with distributed lag non-linear model was used and adjusted for seasonality, pollutants, humidity, and days of the week. HS mortality was associated with low mean temperatures for men relative risk (RR) = 2.43 (95% CI, 1.12–5.28) and women RR = 1.39 (95% CI, 1.03–1.86). RR of IS mortality was not significant using a 21-day lag window. Analyzing the lag response separately, we observed that the effect of temperature is acute in stroke mortality (higher risk among lags 0–5). However, for IS, higher mean temperatures were significant for this subtype with more than 15-day lag. Our findings showed that mean air temperature is associated with stroke mortality in the city of São Paulo for men and women and IS and HS may have different triggers. Further studies are needed to evaluate physiologic differences between these two subtypes of stroke.

Keywords

Stroke Mean temperature Time series DLNM São Paulo 

Notes

Funding information

This work was supported by Foundation for Research Support of the State of São Paulo - FAPESP (Proc. 2012 / 15085-9). The sponsor did not have any role in the design, data collection or analyses of the study, and did not influence the interpretation of the results.

Compliance with ethical standards

Competing interests

The authors declare they have no competing interests.

References

  1. {WHO} {\textbar} {The} top 10 causes of death, 2015.. WHOGoogle Scholar
  2. Abe T, Ohde S, Ishimatsu S, Ogata H, Hasegawa T, Nakamura T, Tokuda Y (2008) Effects of meteorological factors on the onset of subarachnoid hemorrhage: a time-series analysis. J Clin Neurosci 15:1005–1010.  https://doi.org/10.1016/j.jocn.2007.07.081 CrossRefGoogle Scholar
  3. Armstrong B (2006) Models for the relationship between ambient temperature and daily mortality. Source Epidemiol 17:624–631.  https://doi.org/10.1097/01.ede.0000239732.50999.8f CrossRefGoogle Scholar
  4. Bando DH, Brunoni AR, Fernandes TG, Benseñor IM, Lotufo PA (2012) Taxas de suicídio e tendências em São Paulo, Brasil, de acordo com gênero, faixa etária e aspectos demográficos. Rev Bras Psiquiatr 34:286–293.  https://doi.org/10.1016/j.rbp.2012.02.001 CrossRefGoogle Scholar
  5. Berginer VM, Goldsmith J, Batz U, Vardi H, Shapiro Y (1989) Clustering of strokes in association with meteorologic factors in the Negev Desert of Israel: 1981–1983. Stroke 20:65–69.  https://doi.org/10.1161/01.STR.20.1.65 CrossRefGoogle Scholar
  6. Braga, A.L.F., Pereira, L.A.A., Procópio, M., André, P.A. De, Saldiva, P.H.D.N., 2007. Association between air pollution and respiratory and cardiovascular diseases in Itabira, Minas Gerais State, Brazil. Cad. Saude Publica 23, S570–S578. doi: https://doi.org/10.1590/S0102-311X2007001600017
  7. Braga ALF, Zanobetti A, Schwartz J (2002) The effect of weather on respiratory and cardiovascular deaths in 12 U.S. cities. Environ Health Perspect 110:859–863.  https://doi.org/10.1289/ehp.02110859 CrossRefGoogle Scholar
  8. Capon A, Demeurisse G, Zheng L (1992) Seasonal variation of cerebral hemorrhage in 236 consecutive cases in Brussels. Stroke 23:24–27.  https://doi.org/10.1161/01.STR.23.1.24 CrossRefGoogle Scholar
  9. Coelho FMS, Santos BFCD, Cendoroglo Neto M, Lisboa LF, Cypriano AS, Lopes TO, De Miranda MJ, Avila AMH, Alonso JB, Pinto HS (2010) Temperature variation in the 24 hours before the initial symptoms of stroke. Arq Neuropsiquiatr 68:242–245.  https://doi.org/10.1590/S0004-282X2010000200017 CrossRefGoogle Scholar
  10. Cordonnier C, Sprigg N, Sandset EC, Pavlovic A, Sunnerhagen KS, Caso V, Christensen H (2017) Stroke in women—from evidence to inequalities. Nat Rev Neurol 13:521–532.  https://doi.org/10.1038/nrneurol.2017.95 CrossRefGoogle Scholar
  11. Cowperthwaite MC, Burnett MG (2011) An analysis of admissions from 155 United States hospitals to determine the influence of weather on stroke incidence. J Clin Neurosci 18:618–623.  https://doi.org/10.1016/j.jocn.2010.08.035 CrossRefGoogle Scholar
  12. Ebi KL, Exuzides KA, Lau E, Kelsh M, Barnston A (2004) Weather changes associated with hospitalizations for cardiovascular diseases and stroke in California, 1983–1998. Int J Biometeorol 49:48–58.  https://doi.org/10.1007/s00484-004-0207-5 CrossRefGoogle Scholar
  13. Field TS, Zhu H, Tarrant M, Mitchell RJ, Hill MD (2004) Relationship between supra-annual trends in influenza rates and stroke occurrence. Neuroepidemiology 23:228–235.  https://doi.org/10.1159/000079948 CrossRefGoogle Scholar
  14. Galimanis A, Mono M-L, Arnold M, Nedeltchev K, Mattle HP (2009) Lifestyle and stroke risk: a review. Curr Opin Neurol 22:60–68.  https://doi.org/10.1097/WCO.0b013e32831fda0e CrossRefGoogle Scholar
  15. Gasparrini A (2011) Statistical methods in studies on temperature-health associations 175Google Scholar
  16. Gasparrini A, Armstrong B (2013) Reducing and meta-analysing estimates from distributed lag non-linear models. BMC Med Res Methodol 13(1).  https://doi.org/10.1186/1471-2288-13-1
  17. Goggins WB, Woo J, Ho S, Chan EYY, Chau PH (2012) Weather, season, and daily stroke admissions in Hong Kong. Int J Biometeorol 56:865–872.  https://doi.org/10.1007/s00484-011-0491-9 CrossRefGoogle Scholar
  18. Hu Z, Liebens J, Rao KR (2008) Linking stroke mortality with air pollution, income, and greenness in northwest Florida: an ecological geographical study. Int J Health Geogr 7:20.  https://doi.org/10.1186/1476-072X-7-20 CrossRefGoogle Scholar
  19. Hu Z, Rao KR (2009) Particulate air pollution and chronic ischemic heart disease in the eastern United States: a county level ecological study using satellite aerosol data. Environ Health 8:26.  https://doi.org/10.1186/1476-069X-8-26 CrossRefGoogle Scholar
  20. Inagawa T, Takechi A, Yahara K, Saito J, Moritake K, Kobayashi S, Fujii Y, Sugimura C (2000) Primary intracerebral and aneurysmal subarachnoid hemorrhage in Izumo City, Japan. Part I: incidence and seasonal and diurnal variations. J Neurosurg 93:958–966.  https://doi.org/10.3171/jns.2000.93.6.0958 CrossRefGoogle Scholar
  21. Keatinge W, Coleshaw S, Cotter F, Mattock M, Murphy M, Chelliah R (1984) Increases in platelet and red cell counts, blood viscosity, and arterial pressure during mild surface cooling: factors in mortality from coronary and cerebral thrombosis in winter. Br Med J 289:1405–1408.  https://doi.org/10.1136/bmj.289.6456.1405 CrossRefGoogle Scholar
  22. Keatinge WR, Donaldson GC, Cordioli E, Martinelli M, Kunst a E, Mackenbach JP, Nayha S, Vuori I (2000) Heat related mortality in warm and cold regions of Europe: observational study. BMJ 321:670–673.  https://doi.org/10.1136/bmj.321.7262.670 CrossRefGoogle Scholar
  23. Khan FA, Engstrom G, Jerntorp I, Pessah-Rasmussen H, Janzon L (2005) Seasonal patterns of incidence and case fatality of stroke in Malmö, Sweden: the STROMA study. Neuroepidemiology 24:26–31.  https://doi.org/10.1159/000081046 CrossRefGoogle Scholar
  24. Lim YH, Kim H, Hong YC (2013) Variation in mortality of ischemic and hemorrhagic strokes in relation to high temperature. Int J Biometeorol 57:145–153.  https://doi.org/10.1007/s00484-012-0542-x CrossRefGoogle Scholar
  25. Mendis S, Puska P, Norrving B, (2011) Global atlas on cardiovascular disease prevention and control. World Heal. Organ. 2–14. doi:NLM classification: WG 120Google Scholar
  26. Morabito M, Crisci A, Vallorani R, Modesti PA, Gensini GF, Orlandini S (2011) Innovative approaches helpful to enhance knowledge on weather-related stroke events over a wide geographical area and a large population. Stroke 42:593–600.  https://doi.org/10.1161/STROKEAHA.110.602037 CrossRefGoogle Scholar
  27. Pan WH, Li LA, Tsai MJ (1995a) Temperature extremes and mortality from coronary heart disease and cerebral infarction in elderly Chinese. Lancet (London, England) 345:353–355.  https://doi.org/10.5555/URI:PII:S0140673695903410 CrossRefGoogle Scholar
  28. Pan WH, Li LA, Tsai MJ (1995b) Temperature extremes and mortality from coronary heart disease and cerebral infarction in elderly Chinese. Lancet (London, England) 345:353–355CrossRefGoogle Scholar
  29. Rothwell PM, Wroe SJ, Slattery J, Warlow CP (1996) Is stroke incidence related to season or temperature? Lancet 347:934–936.  https://doi.org/10.1016/S0140-6736(96)91415-4 CrossRefGoogle Scholar
  30. Rufca et al (2009) Influência das variaçõescircadianas e temperatura no AVEI. Rev Assoc Med Bras 55:60–63CrossRefGoogle Scholar
  31. Rumel D, Riedel LF, Latorre MR, Duncan BB (1993) Infarto do miocárdio e acidente vascular cerebral associados à alta temperatura e monóxido de carbono em àrea metropolitana do sudeste do Brasil. Rev Saude Publica 27:15–22.  https://doi.org/10.1590/S0034-89101993000100003 CrossRefGoogle Scholar
  32. Schellinger PD, Fiebach JB, Hacke W (2003) Imaging-based decision making in thrombolytic therapy for ischemic stroke: present status. Stroke 34:575–582.  https://doi.org/10.1161/01.STR.0000051504.10095.9C CrossRefGoogle Scholar
  33. Turin TC, Kita Y, Murakami Y, Rumana N, Sugihara H, Morita Y, Tomioka N, Okayama A, Nakamura Y, Abbott RD, Ueshima H (2008) Higher stroke incidence in the spring season regardless of conventional risk factors: Takashima Stroke Registry, Japan, 1988–2001. Stroke 39:745–752.  https://doi.org/10.1161/STROKEAHA.107.495929 CrossRefGoogle Scholar
  34. Vodonos A, Novack V, Horev A, Abu Salameh I, Lotan Y, Ifergane G (2017) Do gender and season modify the triggering effect of ambient temperature on ischemic stroke? Women’s Heal Issues 27:245–251.  https://doi.org/10.1016/j.whi.2016.11.002 CrossRefGoogle Scholar
  35. Wang, X.Y., Barnett, A.G., Hu, W., Tong, S., 2009. Temperature variation and emergency hospital admissions for stroke in Brisbane, Australia, 1996–2005. Int J Biometeorol 53, 535–541. doi: https://doi.org/10.1007/s00484-009-0241-4
  36. Zanobetti A, O’Neill MS, Gronlund CJ, Schwartz JD (2012) Summer temperature variability and long-term survival among elderly people with chronic disease. Proc Natl Acad Sci U S A 109:6608–6613.  https://doi.org/10.1073/pnas.1113070109 CrossRefGoogle Scholar
  37. Zhang Y, Li S, Pan X, Tong S, Jaakkola JJ, Gasparrini A, Guo Y, Wang S (2014) The effects of ambient temperature on cerebrovascular mortality: an epidemiologic study in four climatic zones in China. Environ Health 13:24.  https://doi.org/10.1186/1476-069X-13-24 CrossRefGoogle Scholar

Copyright information

© ISB 2018

Authors and Affiliations

  • Priscilla V. Ikefuti
    • 1
  • Ligia V. Barrozo
    • 1
  • Alfésio L. F. Braga
    • 2
    • 3
  1. 1.Department of Geography, School of Philosophy, Literature and Human SciencesUniversity of São PauloSão PauloBrazil
  2. 2.Department of Pathology, School of MedicineUniversity of São PauloSão PauloBrazil
  3. 3.Collective Health Graduate ProgramCatholic University of SantosSantosBrazil

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