Incidence of Stroke and Stroke Subtypes in Malmö, Sweden, 1990–2000
Marked Differences Between Groups Defined by Birth Country
Background and Purpose— The proportion of immigrants has increased in Sweden markedly during the last decades, as in many other Western countries. Incidence of stroke has increased during this period. However, it is primarily unknown whether incidence of stroke and stroke subtypes in Sweden is related to country of birth.
Methods— Incidence of first-ever stroke was followed during 10 years in a cohort consisting of all 40- to 89-year-old inhabitants in the city of Malmö, Sweden (n=118 134). Immigrants from 12 different countries were compared with native-born Swedes.
Results— Adjusted for age, sex, marital status, and socioeconomic indicators, the incidence of stroke (all subtypes) was significantly higher among immigrants from former Yugoslavia (relative risk [RR], 1.31; 95% CI, 1.1 to 1.6) and Hungary (RR, 1.33; CI, 1.02 to 1.7). A significantly increased incidence of intracerebral hemorrhage was observed in immigrants from Peoples Republic of China or Vietnam (RR, 4.2; CI, 1.7 to 10.4) and the former Soviet Union (RR, 2.7; CI, 1.01 to 7.3). Immigrants from Finland had a significantly higher incidence of subarachnoid hemorrhage (RR, 2.8; CI, 1.1 to 6.8). A significantly lower incidence of stroke was observed in the group from Romania (RR, 0.14; CI, 0.04 to 0.6). Immigrants from Denmark, Norway, Germany, Chile, Czechoslovakia, and Poland had approximately the same risk as citizens born in Sweden.
Conclusions— In this urban population from Sweden, there are substantial differences in stroke incidence and stroke subtypes between immigrants from different countries. To what extent this could be accounted for by exposure to biological risk factors remains to be explored.
In Sweden, ≈30 000 individuals experience a stroke event every year.1 Stroke is a leading cause of disability, particularly in the elderly. Although the knowledge about stroke prevention and the possibilities to treat individuals with high blood pressure have improved during the last decades, incidence of stroke is not declining in Sweden.2,3
In the city of Malmö, in the south of Sweden, ≈700 men and women have a first stroke every year. There are substantial socioeconomic differences between the residential areas in the city. Areas with a high incidence of stroke are characterized by inferior socioeconomic circumstances and a large proportion of immigrants.4 The age-adjusted incidence of stroke has increased in Malmö during the last years,2 and the number of immigrants has increased dramatically. Studies from the United States, the United Kingdom, and other countries5–17 have shown differences in stroke mortality between ethnic groups that can be explained only partially by higher prevalence of hypertension and other established risk factors.5,6 However, studies of incidence of stroke are sparse,6,7 and we have not identified any previous study comparing incidence of stroke and stroke subtypes in immigrants from different countries. The purpose of the present study from the Stroke Register of Malmö (STROMA) was to study the incidence of stroke and stroke subtypes in relation to country of birth.
In November 1990, the population of Malmö included 118 134 citizens (52 877 men and 65 257 women) between 40 and 89 years of age. This population was followed from November 1, 1990, until December 31, 2000, by data linkage with national population registers and the STROMA.2,4,18 The Lund University ethics committee approved the study.
The STROMA was established in 1989.18 A specialized nurse from the stroke register systematically searched for and registered patients with stroke who lived in the city. The research nurse, with a senior physician, validated the diagnosis by reviewing medical records. Criteria for stroke was rapidly developing clinical signs of local or global loss of cerebral function lasting for >24 hours or leading to death before then, with no apparent cause other than cerebral ischemia or hemorrhage. Stroke was classified as subarachnoid hemorrhage (International Classification of Diseases, Ninth Revision [ICD-9] code 430), intracerebral hemorrhage (ICD 431), cerebral infarction (ICD 434), and undetermined stroke (ICD 436). Criteria for stroke classified as subarachnoid hemorrhage, intracerebral hemorrhage, and cerebral infarction were verification of the clinical picture at computed tomography, lumbar puncture, or necropsy.
The National Swedish Census investigation is a total register of the Swedish population November 1, 1990, and includes information on country of birth, marital status, rented and self-owned homes, and annual income.19 This database consists of information from a mailed questionnaire and data from other population registers. The response rate of the questionnaire was 97.5%. Information about deaths during the follow-up and migration during the follow-up was retrieved from the Swedish population register and the Swedish cause of death register.
Information about country of birth was available for 99.96% of the population (51 missing). This analysis was limited to immigrants from countries with total follow-up times of ≈2500 person years or more. To allow comparisons with immigrants from the Far East, 2 comparatively large immigrant groups (Peoples Republic of China, 923 person years; Vietnam, 1451 person years) were collapsed into 1 group in this analysis. The countries in this analysis include 96.8% of all 40- to 89-year-old citizens in Malmö.
Marital Status and Socioeconomic Circumstances
For each individual, the total income in 1990 was categorized into 6 categories: 0 to 49 000; 50 000 to 99 000, 100 000 to 149 000, 150 000 to 199 000, 200 000 to 249 000, and ≥250 000 Swedish kronor per year. Because annual income may not fully reflect the socioeconomic differences among people who have retired from work, the results were also adjusted for rented versus self-owned homes. Of the study population, 55.6% owned their house or apartment, and 40.6% rented their apartment firsthand or secondhand. Four percent with missing data were coded in a separate category. The subjects were categorized into those who were married and those who were not.
Each individual was followed from November 1, 1990, until the first stroke event, death, or December 31, 2000. Individuals who moved from the city were censored at the date of migration.
The expected number of strokes in the immigrants groups was calculated by standardization for age (5-year bands) and sex using the indirect method. The Cox proportional hazards model was used to compare incidence rates with adjustments for age, sex, marital status, and socioeconomic indicators.
Characteristics of Immigrants From Specific Countries
The mean age, proportion of men, proportion with Swedish citizenship, and socioeconomic characteristic of immigrants from different counties are presented in Table 1.
Stroke Incidence in Immigrants From Specific Countries
The stroke risk showed substantial differences between immigrants from different Eastern European countries. Immigrants from former Yugoslavia and Hungary showed significantly higher incidence. Although not significantly, immigrants from the former Soviet Union also had higher risk. In contrast, no increased risk was observed among immigrants from former Czechoslovakia or in the large group of immigrants from Poland. Romanian immigrants had a significantly lower risk. Immigrants from Denmark, Norway, Germany, Chile, and Finland had approximately the same risk as citizens born in Sweden (Table 2).
The relationship between country of birth and incidence of stroke was analyzed separately in men and women and in individuals aged 40 to 64 years and 65 to 89 years (ie, the lower and upper half of the 50 years age range; Table 3). The higher risk in Yugoslavian and Hungarian immigrants and the reduced risk in Romanian immigrants were consistent in men and women. The higher risk in immigrants from China and Vietnam was observed mainly in women.
Subtypes of Stroke
There was a large proportion with intracerebral hemorrhage (ICD-9 code 431) among immigrants from the People’s Republic of China and Vietnam. Of the 18 strokes in this group, 5 were intracerebral hemorrhages. The increased risk of intracerebral hemorrhage in this group was significant (relative risk [RR], 4.2; CI, 1.7 to 10.4) after adjustments for age, sex, marital status, income, and home ownership. After adjustments for potential confounders, an increased risk of intracerebral hemorrhage was also observed in immigrants from the former Soviet Union (RR, 2.7; CI, 1.01 to 7.3).
Immigrants from Finland had a significantly higher incidence of subarachnoid hemorrhage (RR, 2.8; CI, 1.1 to 6.8). Of the 49 strokes in this group, 5 were subarachnoid hemorrhages.
Ischemic strokes (ICD-9 codes 434 or 436) were significantly more common in the groups from former Yugoslavia and Hungary (RR, 1.34; CI, 1.11 to 1.62 and RR, 1.33; CI, 1.01 to 1.77, respectively, adjusted for confounders).
In an additional analysis, subjects were followed until death, first stroke event, migration from the city of Malmö, or to the beginning of the first year they were without income according to assessment of taxes. The results for all stroke cases and for stroke subtypes were essentially unchanged when subjects without income were censored (data not shown).
Studies from various countries have reported differences in stroke mortality between immigrants and the native-born population.5,8,9,11,12,14 Differences in coronary heart disease morbidity have been reported between immigrant groups in Sweden.20 However, studies on incidence of stroke and stroke subtypes are rare. The present study showed marked differences in stroke incidence and stroke subtypes by country of birth. Incidence of all strokes and ischemic strokes was significantly higher among immigrants from Hungary and former Yugoslavia, and incidence of intracerebral hemorrhage was increased among immigrants from the Soviet Union and China or Vietnam. The Finnish group had a significantly higher incidence of subarachnoid hemorrhage. Immigrants from Romania had a significantly lower stroke incidence. These differences remained significant after adjustments for age, sex, marital status, and socioeconomic indicators.
According to official statistics, there are substantial differences in stroke mortality between countries and regions.21,22 Studies on stroke incidence have often shown smaller differences between countries compared with the stroke mortality.23 Although the comparability of stroke mortality statistics has been questioned often, Eastern European countries generally have high rates of stroke mortality.21,22 A high incidence of intracerebral hemorrhage has been reported in East Asia,24 and multinational comparisons of subarachnoid hemorrhage have shown a high incidence in Finland.25 In this study, the increased stroke incidence among immigrants from former Yugoslavia, Hungary, China/Vietnam, and the former Soviet Union, and the high incidence of subarachnoid hemorrhage in the group from Finland, are in accordance with these observations. This suggests that the increased incidence in these immigrant groups reflects influences from their original countries.
However, there were great differences between immigrants from different countries in Eastern Europe. No increased incidence was observed in Czechoslovakian immigrants or in the large Polish group. Although the stroke mortality in Eastern Europe generally is much higher than in Sweden,21,22 it also has been reported that the stroke incidence in Poland is similar to countries from Western Europe.26 The differences between the immigrant groups could partially reflect the circumstances in the original countries. However, another possible explanation is that the circumstances and reasons for moving to Sweden have been different. For example, Yugoslavian immigrants that arrived during the 1960s and 1970s were often recruited as workers, whereas Czechoslovakian and Polish immigrants often were highly educated refugees who arrived during the 1980s. Stroke incidence was also comparatively low in the Chilean group. This suggests that immigrants from these countries are selected groups of more healthy individuals.
Quite unexpectedly, Romanian immigrants had a significantly lower risk. Only 2 incidents of stroke occurred during 3500 person years compared with the expected 14, and both were hemorrhagic. Studies of immigrant groups (eg, all-cause mortality in Turkish people living in Germany27 or stroke mortality in immigrants to the United States)14 have sometimes shown paradoxically lower mortality rates among immigrants compared with the native-born population and the population in the original country. The reasons for the lower mortality rates are controversial, and several explanations have been proposed (eg, highly selected groups of immigrants and the difference in the speed by which risk factors and protective factors change after migration).14,27 It has also been suggested that this could be explained by foreign-born people who remigrate without reporting this to the authorities, which could exaggerate the population at risk and cause low risk estimates for the immigrants.28 A study from Sweden Statistics estimated that ≈25 000 to 50 000 foreign-born individuals who officially live in Sweden have left the country.29 One question is whether “denominator bias” could have reduced the risk of stroke for the immigrants in this study. According to the Population and Housing Census, all subjects in this study lived in Malmö in 1990, and information on birth country was available for the entire population. Those who moved from the city of Malmö during the follow-up were censored at the time of migration. The results were essentially the same when individuals who were without income were censored. Therefore, we believe that remigration was a minor problem in this study. Whether the low incidence in the Romanian group could be explained by a highly selected group who emigrated from this country or whether there are other explanations remains to be explored.
There are substantial socioeconomic differences between residential areas in the city. Areas with a high incidence of stroke are characterized by inferior socioeconomic circumstances and a large proportion of immigrants.4 It has been reported that incidence of stroke in Malmö increased between 1989 and 1998, with annual rates of 3.1% and 2.9% for men and women, respectively.2 One question is whether this could be explained by the increasing proportion of immigrants. When all non-Nordic immigrants were compared with native-born Swedes, the age- and sex-adjusted RR was 1.10 (95% CI, 1.01 to 1.21). Immigrants from the Nordic countries had no increased risk. Although the number of immigrants has increased in the city, it is unlikely that this fully explains the increasing incidence of stroke.
Complete case retrieval and validation of cases, as well as reliable information about the population at risk, are important prerequisites for valid studies of stroke incidence. The STROMA has systematically and actively searched for patients with symptoms of stroke since 1989. The same experienced research nurse validated all cases. The primary care is organized by the community and works in collaboration with the university hospital, which is the only hospital for somatic care in the city. Patients with suspected stroke in primary care are referred routinely to the hospital for further examination. Very few stroke patients are treated as outpatients in Sweden,30,31 and the proportion of nonhospitalized patients is similar in this study compared with other Swedish studies. We have no reason to believe that biased case retrieval or validation of cases has confounded the results.
The large number of individuals and events, the careful procedures for case ascertainment, and the complete and reliable data about the background population are considerable study strengths. The main limitation of the study is that no information on cardiovascular risk factors (eg, smoking and hypertension) was available. However, to collect these data from an unselected urban population is impossible for practical reasons. Hypertension is generally considered to be the most important risk factor for stroke in the general population. Several studies from the city have shown that prevalence of cardiovascular risk factors is associated with the socioeconomic circumstances.4 Adjustments for marital status, income, and home ownership probably picked up much of the differences in traditional risk factors. However, it is possible that the increased risk in some immigrant groups is partially explained by a less favorable risk factor profile. Another limitation is that we do not know how long the subjects had been living in Sweden before 1990, when the study started. However, it is noteworthy that the proportion with Swedish citizenship was high in several groups with high incidence of stroke (ie, the groups from Hungary, former Yugoslavia, China or Vietnam, and the former Soviet Union).
The incidence of stroke and stroke subtypes varies widely between immigrants from different countries in this urban population. The differences in stroke incidence observed in this study only partially reflect the pattern of the stroke mortality reported from these countries. To what extent this could be accounted for by exposure to biological cardiovascular risk factors remains to be explored.
The study was supported by grants from the Swedish Council for Working Life and Social Research, the Swedish Stroke Foundation, the Syskonen Svensson Foundation, and the Segerfalk Foundation.
- Received January 21, 2004.
- Revision received March 26, 2004.
- Accepted May 17, 2004.
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