Abstract
The adverse effects of ambient temperature on human health are receiving increasing attention, yet evidence of its impact on intracerebral hemorrhage (ICH) onset is limited. Here, the relationship between ambient temperature and ICH was evaluated. A time-stratified case-crossover analysis was performed based on 4051 ICH patients admitted to five stroke units in Tianjin between January 2014 and December 2020. Conditional logistic regression was applied to evaluate the associations between the daily mean temperature (Tm) or daily temperature range (DTR) and ICH onset. We found a negative association between Tm and ICH onset (OR = 0.977, 95% CI 0.968–0.987) but not between DTR and ICH onset. In stratified analyses, men and individuals aged ≥ 60 years were more susceptible to low-ambient temperature effects; corresponding adjusted ORs were 0.970 (95% CI 0.956–0.983) and 0.969 (95% CI 0.957–0.982), respectively. Tm significantly affected patients with deep ICH (OR = 0.976, 95% CI 0.965–0.988), but had no effect on lobar ICH. There was also seasonal heterogeneity in the effect of Tm on ICH onset, with Tm being negatively associated with ICH onset only in the warm season (OR = 0.961, 95% CI 0.941–0.982). Results suggest that the low-ambient temperature might trigger ICH onset, especially for the male and elderly population, providing important health guidance to prevent cold exposure–induced ICH.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
Burkart KG, Brauer M, Aravkin AY, Godwin WW, Hay SI, He J, Iannucci VC, Larson SL, Lim SS, Liu J, Murray CJL, Zheng P, Zhou M, Stanaway JD (2021) Estimating the cause-specific relative risks of non-optimal temperature on daily mortality: a two-part modelling approach applied to the Global Burden of Disease Study. Lancet (london, England) 398:685–697. https://doi.org/10.1016/s0140-6736(21)01700-1
Cai J, Meng X, Wang C, Chen R, Zhou J, Xu X, Ha S, Zhao Z, Kan H (2016) The cold effects on circulatory inflammation, thrombosis and vasoconstriction in type 2 diabetic patients. Sci Total Environ 568:271–277. https://doi.org/10.1016/j.scitotenv.2016.06.030
Chen R, Yin P, Wang L, Liu C, Niu Y, Wang W, Jiang Y, Liu Y, Liu J, Qi J, You J, Kan H, Zhou M (2018) Association between ambient temperature and mortality risk and burden: time series study in 272 main Chinese cities. BMJ (Clinical research ed) 363:k4306. https://doi.org/10.1136/bmj.k4306
Costello A, Abbas M, Allen A, Ball S, Bell S, Bellamy R, Friel S, Groce N, Johnson A, Kett M, Lee M, Levy C, Maslin M, McCoy D, McGuire B, Montgomery H, Napier D, Pagel C, Patel J, de Oliveira JA et al (2009) Managing the health effects of climate change: Lancet and University College London Institute for Global Health Commission. Lancet (london, England) 373:1693–1733. https://doi.org/10.1016/s0140-6736(09)60935-1
Costello A, Romanello M, Hartinger S, Gordon-Strachan G, Huq S, Gong P, Kjellstrom T, Ekins P, Montgomery H (2023) Climate change threatens our health and survival within decades. Lancet (london, England) 401:85–87. https://doi.org/10.1016/s0140-6736(22)02353-4
Garg RK, Ouyang B, Pandya V, Garcia-Cano R, Da Silva I, Hall D, John S, Bleck TP, Berkelhammer M (2019) The Influence of Weather on the Incidence of Primary Spontaneous Intracerebral Hemorrhage. J Stroke Cerebrovasc Dis 28:405–411. https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.10.011
GBD (2019) Diseases and Injuries Collaborators (2020) Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet (london, England) 396:1204–1222. https://doi.org/10.1016/s0140-6736(20)30925-9
Guo P, Zheng M, Wang Y, Feng W, Wu J, Deng C, Luo G, Wang L, Pan B, Liu H (2017) Effects of ambient temperature on stroke hospital admissions: Results from a time-series analysis of 104,432 strokes in Guangzhou, China. Sci Total Environ 580:307–315. https://doi.org/10.1016/j.scitotenv.2016.11.093
He F, Wei J, Dong Y, Liu C, Zhao K, Peng W, Lu Z, Zhang B, Xue F, Guo X, Jia X (2022) Associations of ambient temperature with mortality for ischemic and hemorrhagic stroke and the modification effects of greenness in Shandong Province, China. Sci Total Environ 851:158046. https://doi.org/10.1016/j.scitotenv.2022.158046
Jäkel L, De Kort AM, Klijn CJM, Schreuder F, Verbeek MM (2022) Prevalence of cerebral amyloid angiopathy: A systematic review and meta-analysis. Alzheimer’s Dementia 18:10–28. https://doi.org/10.1002/alz.12366
Jiang Y, Hu J, Peng L, Li H, Ji JS, Fang W, Yan H, Chen J, Wang W, Xiang D, Su X, Yu B, Wang Y, Xu Y, Wang L, Li C, Chen Y, Zhao D, Kan H, Ge J et al (2022) Non-optimum temperature increases risk and burden of acute myocardial infarction onset: A nationwide case-crossover study at hourly level in 324 Chinese cities. EClinicalMedicine 50:101501. https://doi.org/10.1016/j.eclinm.2022.101501
Kephart JL, Sánchez BN, Moore J, Schinasi LH, Bakhtsiyarava M, Ju Y, Gouveia N, Caiaffa WT, Dronova I, Arunachalam S, Diez Roux AV, Rodríguez DA (2022) City-level impact of extreme temperatures and mortality in Latin America. Nat Med 28:1700–1705. https://doi.org/10.1038/s41591-022-01872-6
Koh H (2016) Communicating the Health Effects of Climate Change. JAMA 315:239–240. https://doi.org/10.1001/jama.2015.18271
Li H, Yue P, Su Y, Li C (2019) Plasma levels of matrix metalloproteinase-9: A possible marker for cold-induced stroke risk in hypertensive rats. Neurosci Lett 709:134399. https://doi.org/10.1016/j.neulet.2019.134399
Lim YH, Hong YC, Kim H (2012) Effects of diurnal temperature range on cardiovascular and respiratory hospital admissions in Korea. Sci Total Environ 417–418:55–60. https://doi.org/10.1016/j.scitotenv.2011.12.048
Lim YH, So R, Lee C, Hong YC, Park M, Kim L, Yoon HJ (2018) Ambient temperature and hospital admissions for acute kidney injury: A time-series analysis. Sci Total Environ 616–617:1134–1138. https://doi.org/10.1016/j.scitotenv.2017.10.207
Luo Y, Li H, Huang F, Van Halm-Lutterodt N, Qin X, Wang A, Guo J, Tao L, Li X, Liu M, Zheng D, Chen S, Zhang F, Yang X, Tan P, Wang W, Xie X, Guo X (2018) The cold effect of ambient temperature on ischemic and hemorrhagic stroke hospital admissions: A large database study in Beijing, China between years 2013 and 2014-Utilizing a distributed lag non-linear analysis. Environ Pollut (Barking, Essex 1987)(232):90–96. https://doi.org/10.1016/j.envpol.2017.09.021
Ma P, Zhou J, Wang S, Li T, Fan X, Fan J, Xie J (2018) Differences of hemorrhagic and ischemic strokes in age spectra and responses to climatic thermal conditions. Sci Total Environ 644:1573–1579. https://doi.org/10.1016/j.scitotenv.2018.07.080
Mowry FE, Peaden SC, Stern JE, Biancardi VC (2021) TLR4 and AT1R mediate blood-brain barrier disruption, neuroinflammation, and autonomic dysfunction in spontaneously hypertensive rats. Pharmacol Res 174:105877. https://doi.org/10.1016/j.phrs.2021.105877
Mukai T, Hosomi N, Tsunematsu M, Sueda Y, Shimoe Y, Ohshita T, Torii T, Aoki S, Nezu T, Maruyama H, Kakehashi M, Matsumoto M (2017) Various meteorological conditions exhibit both immediate and delayed influences on the risk of stroke events: The HEWS-stroke study. PloS one 12:e0178223. https://doi.org/10.1371/journal.pone.0178223
Pinho J, Costa AS, Araújo JM, Amorim JM, Ferreira C (2019) Intracerebral hemorrhage outcome: A comprehensive update. J Neurol Sci 398:54–66. https://doi.org/10.1016/j.jns.2019.01.013
Polcaro-Pichet S, Kosatsky T, Potter BJ, Bilodeau-Bertrand M, Auger N (2019) Effects of cold temperature and snowfall on stroke mortality: A case-crossover analysis. Environ Int 126:89–95. https://doi.org/10.1016/j.envint.2019.02.031
Ponjoan A, Blanch J, Alves-Cabratosa L, MartíLluch R, Comas-Cufí M, Parramon D, García-Gil MM, Ramos R, Petersen I (2021) Extreme diurnal temperature range and cardiovascular emergency hospitalisations in a Mediterranean region. Occup Environ Med 78:62–68. https://doi.org/10.1136/oemed-2019-106245
Rakers F, Schiffner R, Rupprecht S, Brandstädt A, Witte OW, Walther M, Schlattmann P, Schwab M (2016) Rapid weather changes are associated with increased ischemic stroke risk: a case-crossover study. Eur J Epidemiol 31:137–146. https://doi.org/10.1007/s10654-015-0060-3
Saeki K, Obayashi K, Tone N, Kurumatani N (2015) Daytime cold exposure and salt intake based on nocturnal urinary sodium excretion: A cross-sectional analysis of the HEIJO-KYO study. Physiol Behav 152:300–306. https://doi.org/10.1016/j.physbeh.2015.10.015
Stergiou GS, Palatini P, Modesti PA, Asayama K, Asmar R, Bilo G, de la Sierra A, Dolan E, Head G, Kario K, Kollias A, Manios E, Mihailidou AS, Myers M, Niiranen T, Ohkubo T, Protogerou A, Wang J, O’Brien E, Parati G (2020) Seasonal variation in blood pressure: Evidence, consensus and recommendations for clinical practice. Consensus statement by the European Society of Hypertension Working Group on Blood Pressure Monitoring and Cardiovascular Variability. J Hypertens 38:1235–1243. https://doi.org/10.1097/hjh.0000000000002341
Su YY, Li HM, Yan ZX, Li MC, Wei JP, Zheng WX, Liu SQ, Deng YT, Xie HF, Li CG (2019) Renin-angiotensin system activation and imbalance of matrix metalloproteinase-9/tissue inhibitor of matrix metalloproteinase-1 in cold-induced stroke. Life Sci 231:116563. https://doi.org/10.1016/j.lfs.2019.116563
Tamasauskiene L, Rastenyte D, Radisauskas R, Tamosiunas A, Tamasauskas D, Vaiciulis V, Kranciukaite-Butylkiniene D, Milinaviciene E (2017) Relationship of meteorological factors and acute stroke events in Kaunas (Lithuania) in 2000–2010. Environ Sci Pollut Res Int 24:9286–9293. https://doi.org/10.1007/s11356-017-8590-8
Tochihara Y, Yamashita K, Fujii K, Kaji Y, Wakabayashi H, Kitahara H (2021) Thermoregulatory and cardiovascular responses in the elderly towards a broad range of gradual air temperature changes. J Thermal Biol 99:103007. https://doi.org/10.1016/j.jtherbio.2021.103007
Walsh KB, Woo D, Sekar P, Osborne J, Moomaw CJ, Langefeld CD, Adeoye O (2016) Untreated Hypertension: A Powerful Risk Factor for Lobar and Nonlobar Intracerebral Hemorrhage in Whites, Blacks, and Hispanics. Circulation 134:1444–1452. https://doi.org/10.1161/circulationaha.116.024073
Wang Q, Gao C, Liu H, Li W, Zhao Y, Xu G, Yan C, Lin H, Lang L (2017a) Hypertension modifies the short-term effects of temperature on morbidity of hemorrhagic stroke. Sci Total Environ 598:198–203. https://doi.org/10.1016/j.scitotenv.2017.04.159
Wang S, Li M, Hua Z, Ye C, Jiang S, Wang Z, Song Z, Yu Y (2017b) Outdoor temperature and temperature maintenance associated with blood pressure in 438,811 Chinese adults. Blood Press 26:246–254. https://doi.org/10.1080/08037051.2017.1297676
Wang P, Luo S, Cheng S, Li Y, Song W (2021) Optimal Antihypertensive Medication Adherence Reduces the Effect of Ambient Temperature on Intracerebral Hemorrhage Occurrence: A Case-Crossover Study. Patient Prefer Adherence 15:2489–2496. https://doi.org/10.2147/ppa.S341259
Yang L, Li L, Lewington S, Guo Y, Sherliker P, Bian Z, Collins R, Peto R, Liu Y, Yang R, Zhang Y, Li G, Liu S, Chen Z (2015) Outdoor temperature, blood pressure, and cardiovascular disease mortality among 23 000 individuals with diagnosed cardiovascular diseases from China. Eur Heart J 36:1178–1185. https://doi.org/10.1093/eurheartj/ehv023
Yang J, Zhou M, Li M, Yin P, Wang B, Pilot E, Liu Y, van der Hoek W, van Asten L, Krafft T, Liu Q (2018) Diurnal temperature range in relation to death from stroke in China. Environ Res 164:669–675. https://doi.org/10.1016/j.envres.2018.03.036
Zhang X, Zhang S, Wang C, Wang B, Guo P (2014) Effects of moderate strength cold air exposure on blood pressure and biochemical indicators among cardiovascular and cerebrovascular patients. Int J Environ Res Public Health 11:2472–2487. https://doi.org/10.3390/ijerph110302472
Funding
This work was supported by Tianjin Municipal Science and Technology Bureau Project (No. 21JCZDJC01230); Tianjin Key Medical Discipline (Specialty) Construction Project (No. TJYXZDXK-065B); and Tianjin Center for Health and Meteorology Multidisciplinary Innovation.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Data collection, data cleaning, and statistical analysis were performed by Peilin Liu, Zhuangzhuang Chen, and Xiaoshuang Xia. The first draft of the manuscript was written by Peilin Liu, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
This study was approved by the Ethics Committee of the Second Hospital of Tianjin Medical University (No.KY2020K142).
Consent to participate
Not applicable.
Consent to publish
All authors consent to publish this article in Environmental Science and Pollution Research.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, P., Chen, Z., Xia, X. et al. Potential role of ambient temperature as a trigger for intracerebral hemorrhage: a time-stratified case-crossover study in Tianjin, China. Environ Sci Pollut Res 30, 80988–80995 (2023). https://doi.org/10.1007/s11356-023-27942-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-27942-x