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(Stroke. 1996;27:1774-1779.)
© 1996 American Heart Association, Inc.

Articles

Seasonal Variation in the Occurrence of Stroke in a Finnish Adult Population

The FINMONICA Stroke Register

Dimitrije Jakovljevic, MD; Veikko Salomaa, MD, PhD; Juhani Sivenius, MD, PhD; Markku Tamminen, MSc; Cinzia Sarti, MD, PhD; Kalervo Salmi, MD; Esko Kaarsalo, MD, PhD; Vihtori Narva, MD, PhD; Pirjo Immonen-Raiha, MD, PhD; Jorma Torppa, MSc Jaakko Tuomilehto, MD, PhD

the Department of Epidemiology and Health Promotion, National Public Health Institute, Helsinki (D.J., V.S., M.T., C.S., J. Torppa, J. Tuomilehto); University Hospital, Kuopio (J.S.); Central Hospital of North Karelia, Joensuu (K.S.); District Hospital, Loimaa (E.K.); and City Hospital, Turku (V.N., P.I.-R.), Finland.

Correspondence to Dimitrije Jakovljevic, MD, Department of Epidemiology and Health Promotion, National Public Health Institute, Mannerheimintie 166, FIN-00300 Helsinki, Finland. E-mail djakovlj@ktl.fi.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Seasonal influence on the incidence of and mortality from cerebrovascular disease has been reported during the last three decades, but generally with some discrepancy in results, particularly regarding stroke subtypes. The aim of this study was to examine seasonal variation in the incidence, mortality, and case-fatality rate of stroke in data from the FINMONICA population-based stroke register.

Methods During 1982 to 1992, 15 449 stroke events were registered in the monitored populations aged 25 to 99 years in three geographic areas of Finland: the provinces of Kuopio and North Karelia in eastern Finland and the Turku/Loimaa area in southwestern Finland. We analyzed the seasonal and monthly incidence, mortality, and case-fatality rate of stroke and subtypes of stroke by pooling the data for the three areas and stratifying by sex and age.

Results The rate of occurrence of ischemic stroke events was 12% (95% confidence interval [CI], 5% to 20%) greater in men and 11% (95% CI, 4% to 19%) greater in women in winter than in summer. For intracerebral hemorrhage, we observed a 28% (95% CI, 3% to 58%) greater rate of occurrence in men and a 33% (95% CI, 6% to 66%) greater rate of occurrence in women in winter than in summer. The occurrence of subarachnoid hemorrhage did not vary significantly by season. The greater incidence of ischemic strokes in winter was particularly prominent among men aged 25 to 64 years and less prominent in elderly men and in women. The 28-day case-fatality rate of ischemic stroke showed significant seasonal variation only in women (P=.001), with the lowest rate in summer.

Conclusions There is a significantly greater incidence of ischemic strokes and intracerebral hemorrhages during winter in Finland. Further research that also takes meteorologic and sociodemographic factors into account is warranted, since it may help to determine new ways to prevent strokes.

Key Words: cerebral ischemia • Finland • intracerebral hemorrhage • registries • stroke onset

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Seasonal variation in morbidity and mortality from cerebrovascular disease has been of interest in several studies from different countries and climate zones, but discrepant findings have made the conclusions unclear.^{1 2 3 4 5 6 7 8} This inconsistency may in part be due to the fact that the numbers of patients have been small and most of the studies have not had sufficient power to analyze the subtypes of strokes. Alternatively, larger studies have often been based on routine mortality statistics or hospital admission registers, in which the diagnoses are not standardized and time of onset of symptoms is not accurately determined. To our knowledge, none of the previous studies has examined the case-fatality rate of stroke by season.

Finland is a Nordic country with clear seasonal variation in weather conditions. The winters are usually cold and the summers relatively warm. As a part of the World Health Organization's MONICA project, stroke registers have been functioning in three geographic areas of Finland for 10 years.^{9 10} Altogether, 15 449 consecutive strokes in persons aged 25 to 99 years were registered during the monitoring period according to a standardized protocol and under strict quality control. We have now used the data of the FINMONICA Stroke Register to examine the seasonal variation in incidence, mortality, and case-fatality rate of stroke in Finland.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The registration methods applied in the FINMONICA Stroke Register have been described previously.^{9 10 11 12} In brief, registration was performed in three areas: the provinces of North Karelia and Kuopio in eastern Finland and the Turku/Loimaa area in southwestern Finland. The 10-year monitoring period included the years 1982 to 1991 in North Karelia and 1983 to 1992 in Kuopio and Turku/Loimaa. In all three areas the registration covers all consecutive strokes in the resident population aged 25 to 74 years. In the town of Turku, strokes occurring in persons aged 75 to 99 years were also included during the entire 10-year period. In Kuopio, persons aged 75 to 99 years were included in the registration during 1990 to 1992.

The populations of the FINMONICA areas remained stable during the monitoring period. In 1988, within the group aged 25 to 74 years there were 53 336 men and 53 426 women in North Karelia, 77 114 men and 79 331 women in Kuopio, and 60 126 men and 67 231 women in Turku/Loimaa. In the group aged 75 years, there were 2892 men and 7724 women in Turku and 4283 men and 9695 women in Kuopio.

According to the World Health Organization MONICA protocol, each suspected case of stroke occurring in the monitored populations was checked and evaluated for registration.^{13 14} The stroke register data were cross-checked with the National Death Register for stroke deaths (ICD codes 430 to 438) with the use of a computerized record linkage system on the basis of personal identification numbers unique to every citizen in Finland. Cases found from the National Death Register but not from the stroke register were sent to the local registration teams for evaluation. ICD-8 was used in Finland until the end of 1986 and ICD-9 thereafter.

In the present report, incidence refers to first-ever strokes, ie, those occurring without any evidence of a clinically recognized previous stroke event in the patient's history. The period for one stroke event was 28 days. If symptoms recurred after 28 days from onset, it was considered that a new, recurrent event had occurred. Fatal events were defined as those in which the patient died within 28 days after the beginning of symptoms. Case-fatality rate was defined as the proportion of fatal events of all events. In the analyses by subtype of strokes, strokes were divided into three categories: SAH (ICD 430), ICH (ICD 431), and IS (ICD 432 to 436). The third category combines ischemic strokes of thrombotic and embolic origin. As has been documented earlier,^{9 12} these three categories can be reliably distinguished from each other in the FINMONICA Stroke Register.

Statistical Methods
Data from the 10-year period were pooled for the analyses, and each year was divided into four seasons. Winter included December, January, and February; spring included March, April, and May; summer included June, July, and August; and autumn included September, October, and November. Assuming that the sizes of the monitored populations do not vary by season, we examined the null hypothesis that the strokes were equally distributed across the four seasons using ² tests to compare observed numbers with those expected on the basis of even distribution. Since February is shorter than the other months, the expected numbers were weighted by the number of days in each season, with leap years also taken into account. These analyses were stratified by area, sex, and age. The findings were approximately similar in all three areas, however, and therefore the data from all areas were combined. Of the 15 449 registered stroke events, 219 events with MONICA diagnostic class 9 (insufficient data) were excluded from the final analyses because in these cases the information was insufficient to determine stroke subtype.

Using Poisson regression, we calculated the risk ratios comparing other seasons with summer. The 95% CIs for the risk ratios were obtained in the usual manner: CI=exp (ß±1.96xSEß). Age, sex, and study area were added as covariates in these analyses.

The distribution of strokes was also examined by month with Roger's method,¹⁵ which is sensitive to cyclic trends based on the cosine function. The statistical analyses were performed with SAS.¹⁶

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The included stroke events were almost evenly distributed between men and women (7509 in men and 7721 in women). Of these, 2893 (19%) were registered in North Karelia, 6400 (42%) in Kuopio, and 5937 (39%) in Turku/Loimaa. Their distribution by subtype of stroke was as follows: SAH 1105 (7.3%), ICH 1388 (9.1%), and IS 12 737 (83.6%).

Table 1 shows the distribution of strokes across the four seasons by sex and by subtype of stroke. It demonstrates that all strokes are unevenly distributed throughout the four seasons (P<.0001 in men and P=.003 in women). The highest number of strokes occurs in winter and the lowest in summer, with intermediate values in spring and autumn. Examination of the subtypes of stroke demonstrated that the occurrence of IS and ICH differed by season in both men and women. In contrast, SAH did not show a significant seasonal pattern. The incidence of first-ever IS and ICH followed a seasonal pattern similar to that of total IS and ICH, with the exception of the incidence of IS in women (Table 1). The incidence of SAH did not show a significant seasonal variation.

View this table: [in this window] [in a new window]   Table 1. Strokes by Subtype and Season* in Men and Women Aged 25 Years During the 10-Year Period of the FINMONICA Stroke Register

The occurrence of fatal IS also followed a clear seasonal pattern in women (P<.0001) with a trough in summer and a peak in winter, but among men the pattern was nonsignificant (P=.60) (Table 1). For fatal ICH, the lowest number of strokes was observed in summer consistently in both sexes, but differences were not significant. For fatal SAH, the differences between the seasons were nonsignificant. The 28-day case-fatality rate for all strokes varied significantly by season in women (P<.001) but not in men (P=.99) (Table 1). This was due to a prominent seasonal difference in the case-fatality rate of IS in women (P=.001).

Fig 1 presents risk ratios and 95% CIs for the occurrence of different types of strokes when the other seasons are compared with summer. For SAH, the risk ratios were close to 1 in both sexes. The highest risk ratios were observed for ICH, with values between 1.36 and 1.28 in men and between 1.41 and 1.27 in women. Among men, all other seasons showed significantly higher risk of IS than summer. Among women, only winter showed significantly higher risk of IS than summer. These risk ratios were not substantially altered when age and study area were included as covariates.

View larger version (32K): [in this window] [in a new window]   Figure 1. Risk ratios (RR) and 95% CIs for the occurrence of SAH (ICD 430), ICH (ICD 431), IS (ICD 432 to 436), and all stroke events (ICD 430 to 436) in winter, spring, and autumn compared with summer in men and women aged 25 years in the FINMONICA Stroke Register.

The mean number of strokes per day is depicted by month and by subtype of stroke in Fig. 2. Roger's test demonstrated significant cyclic trends for ICH (P=.005) and for IS (P=.003) but not for SAH (P=.20). Table 2 presents the monthly occurrence of incident and fatal ICHs and ISs during the 10-year period according to age group and sex. The incidence of first IS showed a strong seasonal variation in men aged <65 years (P=.005) but not in older men or in women. Fatal IS showed a strong seasonal pattern in women aged 65 years but not in younger women or in men. The incidence of ICH showed a clear seasonal variation in men aged 65 years (P=.007), and the variation in the occurrence of fatal ICH approached statistical significance in both men and women aged 65 years (P=.08 for both sexes).

View larger version (18K): [in this window] [in a new window]   Figure 2. Mean number of strokes per day by month and by subtype of stroke in men and women aged 25 years in the FINMONICA Stroke Register. P=.005 for ICH, P=.20 for SAH, and P=.003 for IS (Roger's test for cyclic trends).

View this table: [in this window] [in a new window]   Table 2. Number of Incident and Fatal Cases of ICH and IS by Age Group and Month in Men and Women Aged 25 Years During the 10-Year Period of the FINMONICA Stroke Register

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The present study demonstrated a clear seasonal variation in the occurrence of all stroke events in both sexes. In winter, the overall risk of stroke was 13% higher among men and 14% higher among women than in summer. This difference was mainly due to IS, which is by far the most common type of stroke. However, there was also a seasonal difference in the occurrence of ICH. In fact, the point estimates of the risk ratios for ICH were higher than those of IS. Our results are consistent with findings from other studies.^{5 6 17} For example, in a population-based study from Japan, Shinkawa et al⁷ found significant seasonality in the incidence of all strokes, ICH, and cerebral infarctions. In a community-based stroke register study from Italy,¹⁸ cerebral infarctions were more frequent during winter and primary ICH during autumn. Some studies have obtained different results for ICH.² Most of the studies in this field have been performed in countries with cold or temperate climates, but in a study from Israel the average daily incidence of stroke was approximately twice as great on hot days as on relatively cold days.¹⁹ This suggests that exposure to extreme temperatures, whether cold or hot, may increase the risk of stroke.

Interestingly, a recent report from the Oxfordshire Community Stroke Project⁸ did not find a seasonal variation in the incidence of IS in the United Kingdom, although there was a nonsignificant trend toward higher mortality in winter. The authors concluded that the reported winter excess in the mortality from IS could be due to a higher case-fatality rate caused by the complications of stroke, such as pneumonia, which show seasonal variation. However, our study was much larger than the British study and shows clearly that, at least in Finnish conditions, the incidence of IS also has significant seasonal variation in men aged <65 years. The higher case-fatality rate of IS during seasons other than summer observed in our study in women aged 65 years may, however, be due to complications of stroke, as was hypothesized by British investigators. Our findings for ICH are consistent with those of the British study, although the seasonal variation did not reach statistical significance in Oxfordshire, presumably because of the small number of ICH events.

We did not find a significant association between season and the occurrence of SAH, which is in accordance with findings from Japan⁷ and Portugal.¹⁷ Some other researchers⁵ have reported significant association, however, and it should be noted that in our study the occurrence of SAH also tended to be higher during the winter months than during the other months. At least in part, these controversies may be due to the small numbers of patients in these studies and to the relative rarity of SAH. Our study was larger than most other studies that have examined the seasonal variability of SAH. However, we had only 50% power to detect a significant difference at a level of P<.05 between the seasons with highest and lowest occurrence of SAH (eg, between winter and autumn in men). Therefore, seasonal variation in the occurrence of SAH cannot be excluded on the basis of our data.

In the present study, the seasonal differences in the occurrence of IS were most prominent among men aged 25 to 64 years, with the older men and women showing smaller and nonsignificant differences. Previous literature has reported that the seasonal differences in mortality from cerebral and myocardial infarction are greater in older than in younger age groups.^{20 21} Our finding is, however, in agreement with the results of Shinkawa et al⁷ from Japan, who also found a more prominent seasonal variation in younger than in older persons. It is likely that younger men are outdoors more and thus are more exposed to cold weather²² and respiratory infections.²³ In Finnish conditions, effective insulation of houses and adequate heating may protect older persons, since the indoor temperatures do not vary substantially by season in Finland.^{24 25}

The biological reasons for the higher occurrence of strokes during winter are not known, but several possible mechanisms may be suggested. From basic physiology it is known that exposure to cold causes peripheral vasoconstriction and increase in blood pressure.^{26 27} Furthermore, total cholesterol and triglycerides tend to be higher in winter than in summer.²⁸ Perhaps most importantly, plasma fibrinogen concentration and viscosity show considerable seasonal variations, at least in elderly persons,^{29 30} and there is evidence that fibrinogen is a significant predictor of stroke.³¹ Seasonal variations in other factors such as air pollution, exposure to sunlight, incidence of influenza, and diet have been also suggested to play a role, but variation in temperature has been considered the most likely reason.³²

A limitation of our study was that the oldest age group (75 to 99 years) was registered during the entire study period only in the town of Turku and only since 1990 in the province of Kuopio. Therefore, the oldest age group represents only the populations of these areas. Since Turku is a coastal town with smaller seasonal variations in temperature than Kuopio, we analyzed the highest age group separately for Turku and for the province of Kuopio, but the results did not differ substantially from those presented in this report. In any case, the present results can be generalized to the elderly population of Finland as a whole only with great caution.

In conclusion, we noted a significantly higher incidence of IS and ICH in winter than in summer in the FINMONICA areas. The higher incidence of IS was particularly prominent in young and middle-aged men. Further research that takes into account meteorologic factors, such as daily temperature, humidity, and barometric pressure, as well as certain sociodemographic and behavioral factors may help to explain the observed seasonal differences and to determine ways to prevent excess strokes in winter.

	Selected Abbreviations and Acronyms

 

CI = confidence interval ICD (ICD-8, ICD-9) = International Classification of Diseases (8th or 9th Revision) ICH = intracerebral hemorrhage IS = ischemic stroke MONICA = Monitoring Trends and Determinants in Cardiovascular Disease SAH = subarachnoid hemorrhage

	Acknowledgments

 
The FINMONICA Stroke Register was supported by the Academy of Finland.

	Footnotes

 
Deceased.

Received April 15, 1996; revision received June 24, 1996; accepted June 27, 1996.

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