Fung-Chang Sung1,2,3, Hei-Tung Yip2, Cheng-Li Lin2, Jiann-Shing Jeng4, Jiunn-Tay Lee5, Yu Sun6, Cheng-Yu Wei7,8, Po-Yen Yeh9, Kuang-Hsi Chang10,11,12, Shang-Yu Chien13, Kai-Cheng Hsu This email address is being protected from spambots. You need JavaScript enabled to view it.13,14,15,16, TSR team# 

1 Department of Health Services Administration, China Medical University College of Public Health, Taichung 406, Taiwan
2 Management Office for Health Data, China Medical University Hospital, Taichung 404, Taiwan
3 Department of Food Nutrition and Health Biotechnology, Asia University, Taichung 413, Taiwan
4 Stroke Center and Department of Neurology, National Taiwan University Hospital, Taipei 101, Taiwan
5 Department of Neurology, Tri-Service General Hospital, National Defense Medical Center, Taipei 114, Taiwan
6 Department of Neurology, En Chu Kong Hospital, New Taipei City 237, Taiwan
7 Department of Neurology, Chang Bing Show Chwan Memorial Hospital, Changhua County 505, Taiwan
8 Department of Exercise and Health Promotion, College of Kinesiology and Health, Chinese Culture University, Taipei 111, Taiwan
9 Department of Neurology, St. Martin de Porres Hospital, Chiayi 600, Taiwan
10 Department of Medical Research, Tungs' Taichung Metroharbor Hospital, Taichung, Taiwan
11 Center for General Education, China Medical University, Taichung, Taiwan
12 General Education Center, Jen-Teh Junior College of Medicine, Nursing and Management, Miaoli, Taiwan
13 Artificial Intelligence Center, China Medical University Hospital, Taichung 404, Taiwan
14 Department of Neurology, China Medical University Hospital, Taichung 404, Taiwan
15 School of Medicine, China Medical University, Taichung, Taiwan
16 Neuroscience and Brain Disease Center, China Medical University, Taichung, Taiwan
# Taiwan Stroke Registry team can be found in the Supplementary Material


Received: June 6, 2023
Revised: August 17, 2023
Accepted: August 24, 2023

 Copyright The Author(s). This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are cited.


Download Citation: ||https://doi.org/10.4209/aaqr.230131  


Cite this article:

Sung, F.C., Yip, H.T., Lin, C.L., Jeng, J.S., Lee, J.T., Sun, Y., Wei, C.Y., Yeh, P.Y., Chang, K.H., Chien, S.Y., Hsu, K.C., TSR Team (2023). Risk of Stroke Associated with Temperature and PM2.5: Taiwan Stroke Registry-based Study. Aerosol Air Qual. Res. 23, 230131. https://doi.org/10.4209/aaqr.230131


HIGHLIGHTS

  • We evaluated stroke risks associated with temperature and PM2.5 levels in Taiwan.
  • Incident ischemic and hemorrhagic strokes were the highest in February and January.
  • The stroke incidence is steadily declining as the weather gets warmer.
  • PM2.5 pollution has little effect on the risk of stroke.
 

ABSTRACT


This study aimed to assess seasonal stroke risks related to temperature and PM2.5 in Taiwan. Using data of the Taiwan Stroke Registry and air pollution monitored in 2006–2017, the researchers estimated daily average ischemic and hemorrhagic strokes according to temperature and PM2.5 levels, evaluating stroke risks by categorizing PM2.5 levels in each temperature zone. The results revealed a higher incidence of ischemic strokes in February and a higher incidence of hemorrhagic strokes in January, both decreased to the lowest in July. The study found that incident strokes increased with the PM2.5 level in each temperature zone except for the 30+°C stratum. The highest incidence of ischemic strokes appeared at PM2.5 greater than 37.0 µg m–3 during 20–24°C, whereas the highest incidence of hemorrhagic strokes appeared at PM2.5 greater than 37.0 µg m–3 at less than 15°C. No adjusted RRs of strokes were significantly associated with PM2.5 in all temperature zones after controlling for sex, age, BMI, smoking and drinking. We conclude that stroke incidence decreases as the weather gets warmer, whereas PM2.5 pollution may have little effect on stroke incidence. It is essential to keep warm during cold days.


Keywords: Stroke, PM2.5, Temperature, Taiwan stroke registry


1 INTRODUCTION


Seasonality of infectious diseases and respiratory disorders is a common phenomenon well recognized and discussed in studies (Dowell et al., 2003; Dowell and Ho, 2004; Fisman, 2007; Azziz Baumgartner et al., 2012; Nguyen et al., 2016; Moriyama et al., 2020; Chen et al., 2022a). The occurrences of these diseases are climate dependent and may vary among areas, relating to meteorological condition changes, particularly the temperature and precipitations. The yearly influenza epidemic may appear more frequent in tropical areas than in temperate areas, although mainly fortifying in colder periods (Azziz Baumgartner et al., 2012). There are also strong seasonal patterns of childhood acute bronchitis and bronchiolitis associated with the respiratory syncytial virus (RSV) infection (Zhang et al., 2015; Lopes et al., 2020; Chen et al., 2022a). The infection increases in winter and spring in temperate areas, and in rainy season in tropical areas. Host social activity and contact frequency may change with season relating to the spread of infectious agents (Chen and Cheng, 2020; Chen et al., 2022a). However, air pollution also has been considered as a risk factor associated with respiratory infection (Leung et al., 2021; Rittweger et al., 2022).

The seasonality of health and/or the air pollution role on diseases have spanned the globe researchers from infectious diseases to non-infectious diseases, even for asthma and chronic obstructive pulmonary disease (Wang et al., 2018). Studies on the occurrences and deaths of chronic diseases also appear seasonality characteristics, particularly for cardiovascular diseases (CVD) (Boulay et al., 1999; Nguyen et al., 2016; Chen et al., 2018; Levin et al., 2018). An earlier study in France found that both occurrence of and death from chronic heart failure shared a similar seasonal pattern, higher in the cold months than in hot months (Boulay et al., 1999). Both mortality and hospitalization reach the peak in January for the elderly reaching 85 years and older. Using the 7-year vital statistical data to analyze hospitalization records of the New York elderly, Nguyen et al. (2016) found that the CVD deaths peaked during influenza seasons. The mortality was associated with the emergency visits for influenza-like illness. With a warm climate in Sao Paulo, Brazil, population have 30% and 16% higher risks of hospitalizations for heart failure and acute myocardial infarction, respectively, in the minor winter than in summer (Levin et al., 2018). On the other hand, in the tropical area of Qatar, the stroke risk is associated with solar radiations in hot summer (Salam et al., 2019).

Studies have also investigated the potential risks of developing CVD and stroke associated with exposure to air pollutants, including PM2.5. A study in China has found that the risk of out-of-hospital cardiac arrest (OHCA) increased with PM2.5 exposure, particularly for those with a stroke history (Xia et al., 2017). A recent Japanese study reported that the risk of OHCA had a positive association with PM2.5, but a negative association with NO2 (Zhao et al., 2020). Another Japanese study analyzed the multicenter registry data of 6885 ischemic stroke suggesting that a short-term exposure to PM and PM2.5 for one day might associate with the stroke risk (Matsuo et al., 2016). Whereas, an earlier Canadian study analyzing registry data of 9202 patients with acute ischemic stroke in Ontario failed to support the risk overall (O’Donnell et al., 2011). These studies emphasized the impacts of pollution with inconsistent findings, without considering whether the climate condition has a role in association with these disorders. A recent study, using ambulance services records in Taiwan to evaluate the OHCA risk, found that both ambient PMs and climate condition play significant role (Wang et al., 2020). Study on stroke risk considering roles of both climate and air pollution is needed.

The Taiwan Stroke Registry (TSR) is among the large stroke registry programs established in the world (Hsieh et al., 2010). We therefore took the advantage to design a study using the TSR data to evaluate the roles of ambient temperature and PM2.5 on risks of ischemic strokes and hemorrhagic strokes.


2 METHODS


 
2.1 Data Source and Study Population

After receiving the Institutional Review Board approval from each of 59 participating medical centers and community hospitals in Taiwan, the TSR program sponsored by the Department of Health was established to start stroke registry activities in 2006 (Hsieh et al., 2010). Each participating institute assigned personnel to be trained to collect the information of patients with stroke from hospitalization to discharge and enter the records linking to the data bank of TSR program with informed consents. Subsequent information on patient health status post discharge including death was collected at the 1st, 3rd, 6th, and 12th months follow-up. This study used records of stroke patients of whom had been collected from 2006 to 2017, with the approval of the Institutional Review Board of China Medical University Hospital Research Ethics Committee (CMUH102-REC1-086(CR-9)).

The air pollution and meteorological data was obtained from the website of the Environmental Protection Administration (EPA) of Taiwan, https://taqm.epa.gov.tw/taqm/en/ default.aspx. The EPA has established 76 air quality monitoring stations, mostly in urban areas and one station in each of rural counties, since 1993, to monitor hourly ambient air pollutants, temperature and humidity. However, the hourly PM2.5 was not routinely monitored until 2006. We, therefore, used the hourly data of ambient temperature and PM2.5 levels collected from these monitoring stations during the years of 2006–2017 for this study.


2.2 Data Analysis

From the registry database, we first identified patients with the diagnosis of ischemic stroke and hemorrhagic stroke from 2006 to 2017. For this study, we conducted data analysis by adapting statistical methods previously used in studying the childhood acute bronchitis and bronchiolitis risk associated with ambient temperature and PM2.5 (Chen et al., 2022a). In order to illustrate the seasonal fluctuations of stroke events, we calculated the average daily cases of ischemic and hemorrhagic strokes separately from January to December for the period of 2006-2017 by the monthly average temperature and PM2.5. We then estimated the daily stroke cases by sex, age (18–49, 50–64, 65–74, and 75+ years), body mass index (BMI) (< 20, 20–24 and 25+ kg m2), smoking and drinking status, previous history of stroke (no, yes), modified Rankin Scale (mRS) (scale measuring degree of disability after stroke: 0–1, 2–3, and 4–5), temperature zone (< 15, 15–19, 20–24, 25–29, and 30+°C), and approximate quartile PM2.5 levels (< 15, 15–23.6, 23.7–36.9, and 37.0+ µg m–3) based on temperatures at < 15°C. Poisson regression was used to calculate crude relative risk (cRR) and adjusted relative risk (aRR) of stroke and the related 95% confidence interval (CI) associated with these factors for ischemic and hemorrhagic strokes separately. Multivariable analysis was used to calculate the aRR after controlling for sex, age, BMI, smoking and drinking. The ischemic stroke to the hemorrhagic stroke cRR and aRR were also estimated for each stratum of these variables. We conducted the analyses without an offset.

We further calculated and illustrated daily incident stroke cases by the average PM2.5 level in each temperature zone for ischemic and hemorrhagic strokes separately. With the daily stroke incidence cases at < 15°C and PM2.5 < 15.0 µg m–3 as the reference, the univariable Poisson regression was applied to estimate the cRR of stroke by PM2.5 stratum in each temperature zone. We computed aRR using the multivariable Poisson regression model after controlling for sex, age, BMI, smoking and drinking.

 
3 RESULTS AND DISCUSSION


 
3.1 Daily Stroke Incidence by Temperature and PM2.5

Fig. 1 presents distributions of the average daily incidence cases of stroke by the monthly average temperature and PM2.5. The stroke incidence cases were higher in cold months and lower in the hot months, showing an inverse relationship with temperature, but a positive relationship with PM2.5. The highest daily ischemic stroke incidence appeared in February when it was 18.0°C with 33.3 µg m–3 of PM2.5, and the lowest in July when it was 29.7°C with 16.7 µg m–3 of PM2.5 (20.6 versus 17.7 cases). The highest daily hemorrhagic stroke incidence appeared in January when it was 16.5°C with 32.5 µg m–3 of PM2.5 and the lowest in July when it was 29.5°C with 15.2 µg m3 of PM2.5 (9.45 versus 6.55 cases).

 Fig. 1. Daily average stroke cases associated monthly average temperature and PM2.5 from 2006 to 2017 in Taiwan Stroke Registry.Fig. 1. Daily average stroke cases associated monthly average temperature and PM2.5 from 2006 to 2017 in Taiwan Stroke Registry.

 
3.2 Daily Stroke Incidence Compared between Ischemic Stroke and Hemorrhagic Stroke by Covariates

Among 115950 stroke cases identified from TSR for the period of 2006-2017 consisted of 70% ischemic strokes and 30% hemorrhagic cases, with more men than women (61 versus 39%) (Table 1). The incidence increased with age, BMI and mRS, and higher in nonsmokers and nondrinkers, and those without previous stroke history. The ischemic incidence decreased with increasing temperature (from 20.4 cases at < 15°C to 17.4 cases at 30+°C), while increased with increasing PM2.5 (from 15.5 cases at < 15.0 µg m–3 to 22.1 cases at 37.0+ µg m–3). The hemorrhagic incidence appeared similar trends associated with the ambient conditions, but with lower incident cases. Table 2 shows the ischemic stroke to hemorrhagic stroke RRs by stratified covariates. Most of cRRs were significantly higher than 1.0 except young patients and patients with mRS of 0–1.

 Table 1. Average daily cases and relative risks of ischemic stroke and hemorrhagic stroke estimated by sex, age, BMI, smoking, drinking, stroke history, mRS, and daily average temperature and PM2.5.


Table 2. Daily average stroke cases and ischemic stroke to hemorrhagic stroke relative risk.


3.3 Daily Stroke Incidence by PM2.5 Level in Each Temperature Stratum

Fig. 2(a) shows that the daily ischemic stroke incidence increased with the PM2.5 level, in each temperature zone, to the highest at 37.0+ µg m–3 with 22.0–22.6 stroke cases/day, excepting when the incidence dropped to 14.7 cases/day at 30+°C with 37.0+ µg m–3 PM2.5. Compared to the condition of < 15°C and < 15.0 µg m–3 PM2.5, the cRR of stroke at the condition of < 15°C and 37.0+ µg m–3 PM2.5 was 1.20 (95% CI, 1.04–1.38). The corresponding aRR became 1.07 (95% CI, 0.93–1.24) after controlling for sex, age, BMI, smoking and drinking (Fig. 2(b)). In all temperature zones, none of the aRR of ischemic stroke was significantly associated with PM2.5 after controlling for covariates.

Fig. 2(a). Average daily ischemic stroke cases and crude relative risk (RR) by PM2.5 level in each temperature stratum.Fig. 2(a). Average daily ischemic stroke cases and crude relative risk (RR) by PM2.5 level in each temperature stratum.

Fig. 2(b). Average daily ischemic stroke cases by PM2.5 level in each temperature stratum and adjusted relative risk (RR) after controlling for sex, age, BMI, smoking, and drinking.Fig. 2(b). Average daily ischemic stroke cases by PM2.5 level in each temperature stratum and adjusted relative risk (RR) after controlling for sex, age, BMI, smoking, and drinking.

Fig. 3(a) shows that the average daily incident hemorrhagic stroke cases in each temperature stratum also tended to increase with PM2.5 level, and decreased with temperature to the lowest of 6.25 cases/day at the condition of 30+°C with 37.0+ µg m–3 PM2.5, with a cRR of 0.64 (95% CI, 0.42–0.98). The aRR in each stratum was not significant, comparing to the condition at of < 15°C and PM2.5 < 15.0 µg m–3 (Fig. 3(b)).

Fig. 3(a). Average daily hemorrhagic stroke cases and crude relative risk (RR) by PM2.5 level in each temperature stratum.Fig. 3(a). Average daily hemorrhagic stroke cases and crude relative risk (RR) by PM2.5 level in each temperature stratum.

 Fig. 3(b). Average daily hemorrhagic stroke cases by PM2.5 level in each temperature stratum and adjusted relative risk (RR) after controlling for sex, age, BMI, smoking and drinking.Fig. 3(b). Average daily hemorrhagic stroke cases by PM2.5 level in each temperature stratum and adjusted relative risk (RR) after controlling for sex, age, BMI, smoking and drinking.

 
3.4 Discussion

Both air pollution and climate condition have been considered as risk factors for stroke. Among the air pollutants, particular matters haves been considered as the major component linking to stroke, contributing 30% of the global stroke burden, particularly for the low-income population with household air pollution from solid fuels (Feigin et al., 2016). This type of household air pollution is now not a burden in Taiwan, in where traffic contributed most of air pollution. On the other hand, studies have reported the stroke risk during stressful weather conditions could be associated with extreme climate conditions, higher in extreme cold and hot events (Argaud et al., 2007; Chen et al., 2018; Epstein and Yanovich, 2019; Wang et al., 2020; Qi et al., 2021). It is well known stroke is a significant threat in the extreme cold during winter. A study in China found that the risk of death from ischemic stroke was near 2.7-fold higher at the freezing temperature below 0°C, compared to the optimum temperature of near 22–24°C (Chen et al., 2018). It is also well known, the severe heat reaching to 40°C and over in Europe in 2003 had caused 14,800 heat-related deaths in France (Argaud et al., 2007).

Taiwan is an island located on the west of the Pacific Ocean. With the ocean and atmosphere effects, the average annual temperatures of subtropical climate range from 8–33°C in urban areas (Lin et al., 2020; Wang et al., 2020). Population in Taiwan are not likely to expose to the environment with temperature falling below freezing point or heat wave reaching to 40°C and over. The winter temperature of the 5th percentile (< 15°C) is considered as extreme cold spell and the summer temperature of 99 percentile is considered as extreme heat reaching to > 30°C in Taiwan (Wang et al., 2020). The air pollution level in Taiwan has been declining in the past decades with the PM2.5 level reduced from 30.4 µg m–3 in 2006 to 18.8 µg m–3 in 2017 (Cheng et al., 2018). With this type of moderate ambient environment, our study did reveal that the daily stroke events among the TSR patients appeared an inverse relation with the monthly temperature, but positively associated with the monthly PM2.5 level. In general, the relationship between these ambient conditions and stroke risks were alike for both ischemic strokes and hemorrhagic strokes.

The inversed temperature correlation is also familiar in the correlations between respiratory infections and temperature, such as for the childhood acute bronchitis and bronchiolitis of viral infection (Chen et al., 2022a). The monthly pattern of the viral infection also appears a higher incidence in cold months than in hot months, mostly alike the pattern of incident stroke cases in the present study. Children spending more time indoors in cold months may increase close contacts and increase the spread of infectious pathogen among children. Whereas, the increased stroke incidence in cold months in Taiwan is mainly associated with the ambient low temperature.

A recent study used the insurance claims data of Taiwan from 2010 to 2015 to evaluate the stroke risk for residents associated with the time-varying exposure to PM2.5 level (Chen et al., 2022b). Results showed that the long-term exposure to PM2.5 was associated with a moderate risk for 12,942 stroke cases with an aHR of 1.03 (1.01–1.05) after controlling for age, sex, income and urbanization level, or 1.03 (1.00–1.07) after controlling for temperature. Information on BMI and smoking was unavailable in the insurance claims data for further use as controlling variables in the data analysis model.

Our study evaluated the daily stroke risk by the PM2.5 level in five temperature zones, considering not only the interaction between the two ambient factors, but also the association with covariates of lifestyles. We found that the incidence tended to decrease with the increasing temperature, while the cRRs of stroke mostly increased with the PM2.5 level in each temperature zone of less than 30°C. The stroke risk associating with PM2.5 is likely not existing when the ambient temperature reaches 30°C and over, indicating a reduced risk. It is important to note that the increasing trend of aRR of stroke associating with PM2.5 level became insignificant after controlling sex, age, BMI, smoking, and drinking. The covariate of BMI has been reported as a modifiable factor in a systematic analysis for the Global Burden of Disease Study 2019 (Feigin et al., 2021). However, it is interest to note that non-smokers are at a higher risk of both ischemic and hemorrhagic strokes, and non-drinkers are at a higher risk of ischemic strokes. Our further data analyzed showed that the mean age of non-smokers were 9 years older than the current smokers (69.5 versus 60.6 years), indicating the older non-smokers were prone to stroke for other risk factor.

Studies investigating the seasonality of disease risk associated with the ambient condition rarely considered the impact of temperature inversion (Chen et al., 2022a), which is an essential factor affecting the air quality (Yin et al., 2022; Shao et al., 2023). The constrained dispersion during the inversion accumulates PM2.5 near the ground (Yin et al., 2022). There is a strong inverse relationship between temperature and PM2.5 in areas with temperature inversion. In Taiwan, the inversion occurs more often in the cold months and less often in the warm months (Liou and Yan, 2006). This is why a disease with the seasonality characteristics shows a negative relationship with temperature. On the other hand, the disease has a positive relationship with PM2.5, which could be a surrogate relationship. Our study design evaluated the stroke risk by evaluating the role of both temperature and PM2.5 simultaneously.

 
3.5 Strength and Limitations

This study is strengthened for being able to use a large sample allowing to measure daily stroke incident cases and risks by stratified variables. We measured the stroke incidence by four PM2.5 levels within each of the five temperature zones to clarify the impact associated with these ambient conditions. To our knowledge, no previous study has ever used this method to evaluate the stroke risk in association with the interaction between temperature and PM2.5. This type of evaluation is required for studying the meteorological effects on health and well-being for population living in areas with moderate climate, particularly in regions with frequent thermal inversions.

This study has also limitations. The study population consisted of registered cases who had been hospitalized at the major medical centers and regional hospitals for stroke. Patients with severe conditions died prior to care might not be registered in the program. Patients with minor symptoms who had been cared at local general medical practitioners might not be registered in the program as well. We were unable to evaluate whether cases deceased from stroke not being registered in TSR are associated with the impact of extreme meteorological conditions. We are also not clear whether patients with minor symptoms occurred under thermal comfort conditions. Second, the climate and air pollution varied among areas on the island, warmer in the south with higher air pollution from industry emits than in the north. We did not compare the risk variation among areas. Third, the stroke incidence varied by demographic factors including sex, age, BMI, smoking status and mRS. These factors may interact with meteorological conditions, deserving further investigation.

 
4 CONCLUSIONS 


Our data showed that there is an obvious ubiquitous seasonality characteristic in stroke risk in Taiwan, higher in cold months with increased PM2.5 concentrations and lower in warm months with decreased PM2.5 concentrations, the highest in January or February and the lowest in July. The incidence increased with the PM2.5 concentration when it was below 30°C. This relationship is no longer significant after controlling for sex, age, and lifestyles, indicating patient characteristics may modify the stroke risk. Our data may rectify the overemphasis laid on PM2.5 linking to stroke risk.

 
ACKNOWLEDGMENTS


We are grateful to Chair Professor Chung Y. Hsu, MD, PhD for his contribution and wisdom in establishing the TSR program. This study has been supported in part by Taiwan Ministry of Health and Welfare Clinical Trial Center (MOHW110-TDU-B-212-124004), Ministry of Science and Technology (MOST 110-2321-B-039-003; MOST 110-2314-B-039-010-MY2; MOST 111-2321-B-039-005), National Science and Technology Council (NSTC 112-2321-B-039-006- ; NSTC 110-2314-B-039-010-MY2) and China Medical University Hospital (DMR-111-228), Department of Health grants (the Bureau of Health Promotion: DOH95-HP-1102, DOH96-HP-1105, DOH97-HP-2102, DOH98-HP-1102; Clinical Trial and Research Center of Excellence: DOH-TD-B-111-002; DOH99-TD-B-111-003, DOH99-TD-B-111-004), the Ministry of Education (Topnotch Stroke Research Center) and the Dr. Chi-Chin Huang Stroke Foundation. TSR is dedicated to Dr Chi-Chin Huang and family for their generous support to advance the quality of stroke care and prevention in Taiwan. The funders have no role in our study design, data collection and analysis, manuscript preparation, or the decision to publish.

 
ADDITIONAL INFORMATION AND DECLARATIONS


 
Disclaimer

The authors declare have no conflict of interest relevant to this study.


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