(Stroke. 1997;28:45-52.)
© 1997 American Heart Association, Inc.
Articles |
A 15.5-Year Follow-up Study of Stroke in a Japanese Provincial City
The Shibata Study
the Department of Epidemiology, Medical Research Institute, Tokyo Medical and Dental University (T.N., T.Y., H.T.); the Division of Adult Health Science, National Institute of Health and Nutrition, Tokyo (N.Y., M.Y.); and the Department of Public Health, Osaka City University, Medical School (C.D.) (Japan).
Correspondence to Takeo Nakayama, Department of Epidemiology, Medical Research Institute, Tokyo Medical and Dental University, 2-3-10, Kanda-Surugadai, Chiyoda-Ku, Tokyo, 101 Japan. E-mail takeo.epi@mri.tmd.ac.jp.
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Abstract |
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Background and Purpose Change toward Western lifestyles, particularly during the high economic growth period (approximately 1960 to 1975), dynamically altered stroke frequency and the distribution of risk factors in the Japanese. We reexamined their association after this environmental change by a cohort study.
Methods The cohort (2302 subjects) comprised residents aged 40 years or older of the Akadani-Ijimino district in Shibata City, Niigata Prefecture, Japan, who were followed up from 1977 for 15.5 years.
Results Crude incidence rates per 1000 person-years for all strokes were 5.22 for men and 4.36 for women (3.02 and 2.18 for cerebral infarction, 0.65 and 1.06 for intracerebral hemorrhage, and 0.41 and 0.34 for subarachnoid hemorrhage, respectively). Multivariate analyses performed with the Cox proportional hazard model revealed these risk factors to be independently significant: for cerebral infarction in men, age, blood pressure, atrial fibrillation, albuminuria, funduscopic abnormality, and current smoking; for cerebral infarction in women, age, atrial fibrillation, and history of ischemic heart disease; for intracerebral hemorrhage in men, age and funduscopic abnormality; for intracerebral hemorrhage in women, age, blood pressure, and light physical activity; for all strokes in men, age, blood pressure, atrial fibrillation, albuminuria, funduscopic abnormality, current smoking, and heavy physical activity; and for all strokes in women, age, atrial fibrillation, and light physical activity.
Conclusions Most traditional risk factors, including blood pressure and its related organ diseases, were confirmed, but serum total cholesterol had almost no effect. Physical activity had both negative and positive effects on stroke risk. In these findings, however, some differences related to sex were also observed.
Key Words: cigarette smoking • epidemiology • risk factors
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Introduction |
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Although internationally stroke has shown a tendency to decrease,1 it is still the third leading cause of death and an important cause of hospital admission and long-term disability in most industrialized countries.2 The social burden attributable to stroke remains significant in these countries, and effective preventive measures are highly desirable.
In the 1960s stroke was the leading cause of death in Japan, and epidemiological studies were launched to investigate risk factors. These studies identified hypertension and its related organ diseases as strong determinants for stroke,3 4 5 6 7 8 9 which substantially contributed to promote nationwide preventive action.10 Studies in the United States and some European countries reported that the principal pathological determinant was atherosclerosis, which might be influenced by hypercholesterolemia as well as by hypertension,11 but hypertension appeared to be almost the sole cause of stroke in Japan from the 1960s through the 1980s.
During these three decades, both stroke mortality and incidence decreased dramatically in Japan, particularly during the so-called high economic growth period (approximately 1960 to 1975). Remarkable changes in lifestyle, mainly in terms of diet and working patterns, toward Western styles during this period also affected the distribution of risk factors (ie, blood pressure levels decreased and serum total cholesterol levels increased12 ) and possibly their association with subsequent stroke.13 14
To examine the recent state of stroke risk factors in Japan, we established the Shibata Study, in which since 1977 we followed a cohort composed of rural free-living residents. We discuss some results of this prospective study in the present report.
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Subjects and Methods |
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Study District
The city of Shibata covers an area of 434 km2 and is located in the northern part of Niigata Prefecture. It includes a commercial residential area in the center surrounded by an agricultural area. The study district, Akadani-Ijimino, is within the agricultural area.
Baseline Examination
All residents aged 40 years or older (1182 men and 1469 women) were included in the study population, and a baseline examination was conducted in July 1977. The details of the methods were previously described.15
The examination included a questionnaire (demographic characteristics, personal and family medical history, smoking, alcohol consumption, and use of antihypertensive medication); measurements of height, weight, and blood pressure; ECG; funduscopic photograph; blood examination; urinalysis; and a dietary habit and physical activity survey. Rose's questionnaire16 for detecting the presence of IHD was also used. BMI was calculated as (weight in kilograms)/(height in meters)2. Trained nurses measured casual blood pressure at rest using a Riva-Rocci sphygmomanometer according to World Health Organization standard procedure.
The ECG at rest was recorded in 12 leads with the use of an ECG with computer-assisted analytical programs (Nihon Koden, Fukuda ME, Fukuda Denshi), and the findings were coded according to the Minnesota code. The right eye was photographed with a nonmydriatic fundus camera (Canon) for funduscopic examination; the Scheie and Keith-Wagner classifications were determined by discussion among three physicians, including an ophthalmologist. Serum total cholesterol was measured on nonfasting venous blood with an auto analyzer. Standardization was achieved by participation in the Lipid Standardization Program of the US Centers for Disease Control and Prevention through the Osaka Prefectural Center for Adult Disease, Japan (presently, the Osaka Medical Center for Cancer and Cardiovascular Diseases).17 Hematocrit was measured by the capillary method. Levels of urinary albumin and glucose were determined with the use of Uristix (Ames, Miles-Sankyo) with samples taken approximately 2 hours after a meal. To evaluate usual physical activity, we developed a simplified estimation method of energy expenditure.18 This method was validated by comparison with a traditional time and motion study in estimating energy expenditure (correlation coefficient, .64; P<.01). In the present analyses, the physical activity index derived from estimated energy expenditure was used to represent the physical activity of each person. The cutoff level of physical activity index suggested by the National Committee of Recommended Dietary Allowance for the Japanese, Ministry of Health and Welfare,19 was adopted for the present analysis. On the basis of this classification, physical activity levels were divided into three levels: heavy, moderate, and light.
Follow-up
The observational cohort had no past history of stroke and was followed up for 15.5 years from July 1977 through December 1992. To identify possible cases of stroke incidence, follow-up examinations were conducted annually during the observational period. A surveillance and registration system was incorporated with the local administration and the regional medical association. Under this system, appropriate information was obtained from primary care physicians in the area, death certificates, reports from public health nurses and public emergency services, records of hospitals, and social insurance. Three of the hospitals were equipped with CT scanners, and their findings since 1980 were available; few cases were autopsied because of prevailing customs in this area. The degree of migration of members of the cohort was determined by periodic review of the resident registration cards, but end points could not be confirmed if subjects moved away from the city. Details of these methods were described elsewhere.20
Definition of Stroke
Stroke was defined as the occurrence of rapidly developing clinical signs of focal or global disturbances of cerebral function that lasted more than 24 hours or resulted in death for which there was no apparent cause other than a vascular accident. According to the standard clinical criteria,21 stroke cases were classified into the following subtypes: ICH, CI, SAH, and undetermined type. If the clinical diagnosis conflicted with CT findings, the subtype was determined by the latter.
ICH
ICH was characterized by rapid evolution of focal neurological signs, rapid progression to coma, signs of meningeal irritation, elevated blood pressure, and headache. Blood-stained cerebrospinal fluid, a high-density area on CT, and distortion of the usual vessel patterns indicating a hematoma on the angiogram were also evidence of ICH.
CI
CI was characterized by slow, gradual development of focal neurological signs lasting more than 24 hours, relative preservation of consciousness, and elevated blood pressure. This category included cerebral embolus with a sudden onset of focal neurological symptoms and evidence of emboli. The absence of blood in the cerebrospinal fluid, a low-density area on CT a few days after onset, and stenotic or occlusive lesions of the intracranial and extracranial arteries on the angiogram also supported this diagnosis.
SAH
SAH was characterized by sudden onset of severe headache with only a relatively momentary disturbance of consciousness, signs of meningeal irritation, absence of focal neurological signs, and subhyaloid hemorrhage. The presence of blood in the cerebrospinal fluid, a high-density area on CT, and ruptured aneurysm and arteriovenous malformation on the angiogram were also indications.
Stroke of Undetermined Type
This category was characterized by a history of onset and residual deficit sufficiently well documented to ensure a high probability that stroke has occurred but incomplete clinical data to further subcategorize the type of stroke.
Statistical Analyses
RRs for CI, nonembolic CI (CI cases minus cases with atrial fibrillation at the baseline survey), ICH, and all strokes were obtained for both sexes in two ways: age-adjusted and multivariate analyses with stepwise procedures (the level of significance for a variable to be entered and to stay in the model was set at .10 for tolerant consideration in selecting predictive factors). These analyses were conducted with the Cox proportional hazards model. SAH was not analyzed because of low incidence. Because SBP and DBP are strongly correlated, MBP (MBP=1/3 SBP+2/3 DBP) was adopted as an independent variable in multivariate analysis. Variables were dichotomized: ECG abnormality (high R and/or ST-T change), funduscopic abnormality (Keith-Wagner II or higher), albuminuria (+ or higher), glycosuria (± or higher), alcohol consumption (cutoff point: two drinks per day), and current smoking (cutoff point: 20 cigarettes per day). For physical activity, three levels were described by two dummy variables, with a moderate level as the standard (RR=1.00).
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Results |
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Observational Cohort and Stroke Incidence
From the eligible population, 998 men (response rate, 84%) and 1360 women (93%) were initially examined. When we exclude those with a previous history of stroke, 961 men and 1341 women were followed up for stroke from July 1977 through December 1992. Nonparticipants in the baseline survey were 183 men and 109 women, of whom 28 men and 29 women were hospitalized or being treated at clinics. The number of bedridden patients cared for at home was 14 for both men and women. During the 15.5-year observation, 316 men and 313 women died, and an additional 47 men and 87 women were lost because they moved. Table 1
shows stroke incidence. The crude incidence rates per 1000 person-years for all strokes were 5.22 for men and 4.36 for women. Similarly, rates for CI were 3.02 (men) and 2.18 (women); for ICH, 0.65 (men) and 1.06 (women); and for SAH, 0.41 (men) and 0.34 (women). CT scans were performed in 46% of the identified cases. According to stroke subtype, CT findings were available for 43 of 76 CI cases (cortical artery regions, 25; penetrating artery regions, 16; others, 2); 8 of 19 ICH cases (cortex, 1; thalamus or putamen, 5; cerebellum or brain stem, 2); and 7 of 12 SAH cases. Seven cases that showed no specific findings on CT scan were classified as undetermined type.
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Risk Analyses
RRs and 95% CLs according to stroke subtypes are shown in Table 2 (CI), Table 3 (ICH), and Table 4 (all strokes). The level of significance was P<.05 for age-adjusted analysis and P<.10 for multivariate analysis.
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Age was a common risk factor for each type of stroke. For CI in men, SBP, DBP, MBP, atrial fibrillation, and albuminuria were significant in age-adjusted analysis. In multivariate analysis, MBP, atrial fibrillation, albuminuria, funduscopic abnormality, and current smoking appeared to be independent risk factors. For CI in women, atrial fibrillation and IHD history were significant in age-adjusted analysis, and this finding was also confirmed in multivariate analysis. For ICH in men, only age was significant in univariate analysis, and funduscopic abnormality as well as age appeared to be an independent risk factor in multivariate analysis. For ICH in women, DBP and MBP were significant in age-adjusted analysis. In multivariate analysis, MBP and light physical activity were confirmed as independent risk factors. For all strokes in men, SBP, DBP, MBP, hematocrit, atrial fibrillation, and albuminuria were significant in age-adjusted analysis. In multivariate analysis, MBP, atrial fibrillation, albuminuria, funduscopic abnormality, current smoking, and heavy physical activity appeared to be independent risk factors. For all strokes in women, DBP, MBP, atrial fibrillation, and light physical activity were significant in age-adjusted analysis. In multivariate analysis, atrial fibrillation and light physical activity were confirmed as independent risk factors.
For nonembolic CI, similar factors (atrial fibrillation was excluded from explanatory variables) were detected in both men and women, and therefore data are not shown in the table.
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Discussion |
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Blood Pressure Levels and Related Factors
Although there were some differences related to sex, elevated blood pressure was positively correlated with each type of stroke. The "modernization" of Japanese lifestyles plus successful propagation of community-based hypertension control and improvement of antihypertensive medication were closely related to the major downward shift in the average level of blood pressure and in stroke incidence between the 1960s and the 1980s.12 14 22 23 With decreasing trends for both blood pressure level and stroke incidence, the strength of association between initial blood pressure level and subsequent stroke risk may be weaker than that observed previously. One point that has not been adequately examined in previous studies is the effect of antihypertensive medication. Wolf et al24 attempted to adjust for the treatment effect by including medication status in the analysis as a dummy variable. Furthermore, D'Agostino et al25 modified this method by using an interaction variable between SBP and medication status. This interaction variable, NEWHRXSBP, is expressed as HRX*(SBP-110)*(200-SBP), on the assumption that treatment effect can be expected when SBP is between 110 and 200 mm Hg (HRX=1 if on medication and 0 if not). If SBP <110 or SBP >200, NEWHRXSBP=0. We attempted these two approaches in the present analysis to examine this point. Twenty-three percent of the initial subjects used antihypertensive medications. Multivariate analysis for all strokes including sex, age, MBP, and use of antihypertensive medication (dummy variable) showed no significant effect of treatment (P=.70). Another analysis in which we used the interaction variable mentioned above showed the same result (P=.82). On the basis of these studies, it would appear valid to adopt current blood pressure level regardless of treatment in the present study.
Stability of individual blood pressure levels during the follow-up period must also be considered. We compared the initial level with that of the follow-up survey conducted in 1982, 5 years later (the response rate of the initial sample was 60%; n=1375). The correlation coefficients of SBP, DBP, and MBP were .63, .57, and .62, respectively; the stability of blood pressure levels appeared to be fair.
While overweight is a related factor for hypertension,26 its independent role for stroke risk is somewhat controversial. Our previous study in Taisho, Japan, in which the population was as agricultural as the population in the present study, showed that relatively lean people had a higher risk for ICH.9 Heavy physical activity, especially among middle-aged men, might have resulted in such leanness. In addition, as the result of inadequate balance in the traditional diet characterized by extremely high amounts of salt and carbohydrates and low amounts of fat and animal protein, leanness in this population was often accompanied by hypertension and low serum cholesterol.3 4 9 14 23 In the present study a slightly positive association of BMI with the incidence of each type of stroke was observed, but none were statistically significant. This implies that the etiology of stroke and risk factors among the Japanese have been changing during these decades.
Atrial fibrillation has been identified as a risk factor for CI, particularly for cerebral embolism.27 We confirmed this relationship in this study. Atrial fibrillation was detected in 31 subjects at the baseline examination, of whom 4 had a history of stroke and 1 of IHD. Most of the 26 subjects used antihypertensive medications, and only 1 person was diagnosed as having valvular heart disease. The relationship of atrial fibrillation to CI in Western populations is apparently different from that in Japan. The Framingham Study showed that IHD played an etiologic role in atrial fibrillation,28 whereas in our population, as reported by Kitamura et al,29 atrial fibrillation in most people may be the result of chronic exposure to moderate hypertension.
Albuminuria and funduscopic and ECG abnormalities are recognized as "target organ disease" induced by hypertension.26 Albuminuria, which was a significant risk factor in men in the present study, was found in 155 subjects at the baseline survey. Cases detected in this study may be due to hypertension or arteriosclerotic renal dysfunction because only 19 of those with albuminuria had chronic nephritis or nephrosis. Funduscopic abnormality (hypertensive and/or arteriolosclerotic changes) is regarded as a strong risk factor for stroke in Japan.30 Although we reported a nonsignificant association between funduscopic abnormality and subsequent stroke in our previous preliminary article (6.5-year follow-up),15 we confirmed significant relationships between funduscopic abnormality and both CI and ICH in men in this 15.5-year follow-up, possibly because of the accumulation of a statistically sufficient number of events. However, we failed to find the significant relationship between ECG abnormality and stroke occurrence that had been observed in the preliminary report.15 Unlike our funduscopic abnormality findings, ECG abnormalities cannot be clearly explained. As presently defined, ECG abnormality may be a rather short-term predictor for stroke in this population because its significance was observed in the shorter observational period. Its RR for all strokes was 1.41 (95% CL, 0.99 to 2.01) in sex- and age-adjusted analysis, which was attenuated when MBP was included in the model. Thus, ECG abnormality in this study did not predict subsequent stroke independent of casual blood pressure.
The relationship of alcohol consumption to hypertension has been established,26 and that to stroke, particularly ICH, was also observed in several Japanese reports.9 31 32 However, in the present study we confirmed this tendency by only limited analysis, ie, CI and all strokes in men in age-adjusted analyses. We found almost no relationship for ICH, which may be due to an insufficient number of events in men for this analysis (n=8).
Atherogenic Risk Factors
We observed almost no relationship between serum total cholesterol and each type of stroke in the present study. The relationship between hypercholesterolemia and stroke is controversial at present.2 33 A recent meta-analysis that included 45 prospective cohort studies showed almost no relationship between serum total cholesterol and subsequent stroke (all strokes combined only).34 This discordance may be due to the difference in the population, in which the dominant subtype of stroke is different.35 In some American or European populations in which long exposure to high levels of serum total cholesterol exists and the predominant subtype of stroke is CI, particularly infarction in cortical artery regions (cortical CI), a positive relationship may be observed.36 37 In the Multiple Risk Factor Intervention Trial, a positive relationship was found when analysis was limited to nonhemorrhagic strokes.38 In Japan, some studies showed a lower percentage of cortical infarction than those in Western populations.39 40 CI in the present study was of mixed subtypes, as demonstrated by CT findings. The effect of serum total cholesterol could not be detected when the analysis was performed for overall CI or for all strokes. With the change in dietary patterns, particularly the increase in fat intake, the mean level of serum total cholesterol among the Japanese adults continues to increase, although this level is still much lower than those of other Western populations.41 42 43 The mean serum total cholesterol level of Shibata residents was low compared with concurrent national averages (Shibata residents versus national samples, aged 40 years or older: 174 mg/dL versus 190 mg/dL).12 The strongly rural characteristic of the study population may have mitigated the speed of lifestyle changes compared with the national average.
The relationship of hypocholesterolemia to stroke risk, particularly ICH, has recently interested many investigators.44 45 Although some Japanese epidemiologists including us have described this relationship,4 5 9 23 it is no longer a clear finding. This may primarily be due to the substantial rise in mean serum total cholesterol levels and the fact that the prevalence of severe hypocholesterolemia, which has been associated with ICH, has decreased.23 41
Smoking has been an established risk factor for stroke in Western populations.46 However, most Japanese investigators have failed to find a significant positive relationship. We identified current smoking (
20 cigarettes per day) as a risk factor for all strokes among men, particularly CI. Smoking may have been recognized as a predictor of CI in the present study because among stroke cases, the relative frequency of cortical CI, which may have a stronger association with smoking, tended to increase through the observational period. Among CI cases in which CT findings were available, cortical CIs were more frequent than infarctions in penetrating artery regions (penetrating CIs, which are closely related to lacunar infarction). These observations are not conclusive because we lacked CT findings in almost 40% of CI cases and observation of the frequency of CI subtypes was limited to only one specified period, but nevertheless the findings tend to support the aforementioned hypothesis. Although smoking and hypercholesterolemia are regarded as atherogenic factors, the effect of current smoking is more detectable in extracranial arteries.47 This may partially explain the discrepancy in the findings of a positive relationship between current smoking and CI and the absence of a relationship between hypercholesterolemia and CI.
History of IHD has been shown to increase stroke risk in some Western populations.36 48 49 50 Although no Japanese studies have observed this association, we found a significant relationship with CI in women in the present study. A common atherogenic background in these cases is implied when IHD preceded stroke occurrence.
Although several studies report that glucose intolerance is an independent predictor of stroke,2 36 48 51 52 only one Japanese study has reported this thus far.6 We observed no significant relationship between glycosuria, as a marker of glucose intolerance, and each type of stroke. At the baseline survey, 49 subjects were positive for glycosuria. However, the low sensitivity of glycosuria for detecting glucose intolerance is well recognized. Therefore, the use of glycosuria as a predictor of stroke may decrease the true association of glucose intolerance to each type of stroke.
Other Factors
Some studies showed a significant relationship between physical inactivity and stroke occurrence in men.37 53 54 55 56 57 We observed a U-shaped relationship between the physical activity index adopted in this study and incidence of all strokes in an earlier report of a 7.5-year follow-up.58 Although this relationship was previously demonstrated in both sexes combined, analyses for men and women were possible in the present report because a sufficient number of events were obtained. We confirmed a positive relationship between light physical activity and all strokes (particularly ICH) in women and a positive relationship between heavy physical activity and all strokes in men. While the former is similar to the findings of other studies, reports of this relationship in women have been rare.59 Furthermore, the latter relationship observed in men appears to be somewhat novel. Some earlier studies in Japan suggested that nonobese people who engaged in heavy physical labor were at high risk for cardiovascular diseases including stroke.3 9 60 The community examined in this study is noted for its cultivation of rice, and most residents engage in some form of agricultural work. Although mechanization has reduced their amount of hard labor, they still were much more active physically than urban or sedentary populations. In contrast, the present recommendations for physical activity are based on findings from the sedentary populations that have been studied in the United States or Western countries.61 62 In this community, very few people reported exercising regularly or enjoying sports at the baseline survey. Therefore, the physical activity index used in this study represented mostly work-related physical activity, including housekeeping. Because complete exclusion of various biases and confounding factors cannot be confirmed,63 further studies are necessary to determine the relationship between physical activity and stroke risk. However, the potential harmfulness to health of heavy physical activity should be noted.
Although several studies have indicated that a high hematocrit level may be associated with the occurrence of cerebral ischemia,64 only a few population-based studies observed this relationship.6 65 66 In this study hematocrit was associated positively only with the risk for all strokes among men in an age-adjusted analysis. This association could not be confirmed in multivariate analyses.
Limitations
The sample size was rather small, and therefore some factors that are actually predictive of stroke occurrence may not have been found.
Sole dependence on clinical information for half of the stroke subtypes is a major limitation of the present study. While our previous study validated the adequacy of sensitivity and specificity of the clinical diagnosis compared with classification by CT findings, we also recognized that small putaminal or thalamic hemorrhages tended to be misclassified as penetrating CIs.67 Although CT findings were available in only 46% of stroke cases, this may be a result of effective surveillance. Some general practitioners in this community who actively cooperated with this surveillance system operated small hospitals in which CT was not available. This made our incidence registration system reliable, although there was a rather low rate of CT findings.
The relationships between incidence of stroke, predominant stroke subtypes, and distribution of risk factors are neither static in terms of time nor homogeneous in terms of place, race, and sex. The unique background of the examined population should be considered in interpreting and generalizing these findings. Although disentangling the web of causation is difficult, epidemiological studies play a major role in describing the natural history of stroke and providing the basis for prevention.
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Acknowledgments |
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This study was supported by the following grants from the Ministry of Health and Welfare, Japan: Nervous and Mental Disorders (grant 3A-3) from the National Center of Neurology and Psychiatry; Cardiovascular Diseases (grant 3C-2) from the National Cardiovascular Center. Appreciation is extended to the following persons: Drs Torahiko Kon (mayor of Shibata City), Ken-ichi Baba (Niigata Medical Association), Masuro Togashi, Kazuo Kawai, Makoto Kumakura, Shun Mayama, Yatsunori Sobue, and many other collaborators in Shibata City as well as the staffs of our colleagues. Special thanks to Drs Edward K. Fujimoto and Mohammad Mostafa Zaman for English language assistance.
Received July 11, 1996; revision received September 3, 1996; accepted September 3, 1996.
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