Stroke Incidence, Recurrence, and Case-Fatality in Relation to Socioeconomic Position
A Population-Based Study of Middle-Aged Swedish Men and Women
Background and Purpose— Low socioeconomic status is associated with increased incidence of stroke. This study investigated stroke incidence, recurrence, and case-fatality after stroke among middle-aged Swedish men and women and whether this association differs by gender or stroke subtype.
Methods— A total of 69 625 (49% men) citizens, aged 40 to 65 years, living in the city of Malmö in 1990 were studied in relation to total annual income and occupation class, ie, 2 indicators of socioeconomic status. Incidence of first-ever stroke, stroke recurrence, and case-fatality (death within 28 days or 1 year after stroke) were studied over 10 years of follow-up.
Results— During the follow-up, a total of 1648 subjects developed a first-ever stroke of whom 275 also experienced a recurrent stroke. By using Cox regression model with covariate adjustments, the incidence of stroke was significantly increased (relative risk: 1.75, 95% CI:1.36 to 2.25) in women who were in the lowest quartile of income compared with the women being in the highest quartile. Corresponding relative risk in men was 1.29 (1.06 to 1.58). Both in men and women, income was significantly associated with ischemic, but not hemorrhagic, subtypes of stroke. Similar relationships were observed between occupation level and incidence of stroke. In addition, low income was associated with higher 28-day and 1-year fatality rates in men (relative risk: 3.13, 1.35 to 7.24 and 2.17, 1.18 to 4.00, respectively), but not in women. In contrast, recurrence of stroke was inversely associated with income only in women.
Conclusions— Incidence of stroke, stroke recurrence, and case-fatality increased with decreasing socioeconomic status; however, this relationship differed by gender and subtype of events.
There is an increasing trend in current years to explore the association between the risk of stroke and socioeconomic status (SES).1–4 It has been documented by the majority of studies that there is an inverse association between stroke incidence/mortality and socioeconomic status,1–4 ie, lower SES is associated with a higher risk of stroke.
However, not much is known about stroke recurrence and socioeconomic position.5 It is unclear whether the effects of SES on the risk of stroke differs between men and women4,6,7 or whether this association varies by subtype of events.8,9
The aim of this study was to explore the incidence of first-ever stroke, recurrent stroke, and case-fatality rates in relation to SES as measured by total annual income and occupation class, and whether the relationship differs by gender or by subtype of events. The study was conducted in a large urban population of middle-aged Swedish men and women.
Information about all men and women who were 40 to 65 years and living in the city of Malmö in 1990 was retrieved from the Population Census Data10 from 1990 (34 031 men and 35 594 women). This population was followed from November 1, 1990, until January 31, 2001, by record linkage with national population registers11 and the stroke register in Malmö (STROMA).12
The Lund University Ethics Committee approved the study.
STROMA was established in 1989.12 Malmö residents, who have had a stroke, whether hospitalized or nonhospitalized, have been registered in STROMA. A specialized nurse from the Stroke Register systematically searched for and validated the patients with stroke symptoms at the University Hospital of Malmö, which is the only hospital with inpatient care facilities in this city. Primary care and nursing homes work in collaboration with the University Hospital. Patients who present at those healthcare facilities with symptoms of stroke are routinely referred to the hospital for further examination and captured through systematic search of medical records. The research nurse together with a senior physician obtained complete case ascertainment by going through medical records and in most cases also through a patient interview. The ascertainment of cases and validity of STROMA has been shown to be high.13
Stroke was defined as rapid developing clinical signs of local or global loss of cerebral function that lasted for >24 hours or led to death within 24 hours. Subtypes of stroke were coded according to the International Classification of Diseases, 9th Revision. The events were classified as cerebral infarction (ischemic; International Classification of Diseases 434), intracerebral hemorrhage (International Classification of Diseases 431), and subarachnoid hemorrhage (International Classification of Diseases 430). By definition, patients with transient ischemic attacks were excluded. The diagnosis of stroke or subtype classification was verified by CT scan, autopsy, or lumbar puncture. Stroke was classified as unspecified event (International Classification of Diseases 436) if no CT or autopsy was performed.
A recurrent stroke was defined as if more than one stroke event occurred during follow-up. Case-fatality was defined as death within 28 days after onset of stroke or death within 1 year. The data were ascertained by verifying with the National Register of Cause of Death.11
Each individual was followed from November 1, 1990, until first-ever stoke event, death, or January 31, 2000, whichever came first. Case-fatality and stroke recurrence were followed until December 31, 2001, in subjects with a first-ever stroke. Individuals who moved from the city were censored at the date of emigration.
Information on marital status, country of birth, housing conditions, and total annual income (in 1990) was designed in the questionnaire of the National Census.10 The National Swedish Census investigation is a total register of the Swedish population in November 1, 1990.10 This database consists of information from a mailed questionnaire and data from other population registers. The response rate of the questionnaire was 97.5%. Marital status was categorized as those who were married and those who were not (ie, unmarried, divorced, or widowed). Housing conditions were grouped into self-owned home (house or apartment) or rented apartment. Country of birth was classified as those born in Sweden or in other countries.
For each individual, the total annual income and occupation class were used to measure the SES. Information about total annual income (in Swedish Crowns) was available for all subjects and categorized into gender-specific quartiles in the analysis. Occupational status, assessed by answers to questions concerning job titles and work tasks, formed the basis for classification into socioeconomic index groups according to methods used by the National Bureau of Statistics Sweden.14 This classification system takes into account the educational background needed to qualify for a particular job. In this study, the different socioeconomic index categories were high-level nonmanual workers, medium-level nonmanual workers, low-level nonmanual workers, skilled manual workers, unskilled manual workers. Enterprisers and farmers (ie, professionals with and without employees) were categorized as self-employed and subjects who were early retied, unemployed, and so on, as others.15 Information on occupation was available in 53 549 subjects (76.9%).
Gender-specific baseline characteristics are presented by mean values or as proportions. Cox regression model was used to assess the associations between SES and stroke incidence, subtype, recurrence, and case-fatality. Due to difficulties in ranking subjects classified as self-employed or “others” in relation to other socioeconomic index groups, no formal trend analysis of occupational status in relation to different outcome was performed. Initial models were adjusted for age. Then, the variables of marital status, country of birth, and housing conditions were added in the model. Although the interaction between income and housing conditions was close, the housing conditions were still considered a confounding factor because it may be the case (particularly in women) that someone may have a low income but their whole economic conditions were not poor because of better income of their spouses.
All comparisons were 2-sided and a 5% level of significance was used. The statistical analyses were conducted by the computer software SPSS (14.0).
Baseline characteristics for men and women, respectively, are presented in Table 1. Men had higher annual income and occupational levels than women.
Incidence of Stroke in Relation to Socioeconomic Status
During a mean follow-up of 8.9±2.7 years (621 143 person-years), 1029 men and 619 women developed a first-ever stroke. The age (years) at onset of stroke was 62.6±6.8 in men and 62.8±7.3 in women.
In both men and women, the incidence of stroke increased with decreasing annual income (Table 2). In men, the age-adjusted relative risk (RR) in those who were in the lowest quartile of income was significantly higher than those in the highest quartile (RR:1.37, 95% CI: 1.14 to 1.64). Compared with men with high-level nonmanual occupations, the RR increase for men categorized as “others” (ie, early retired or unemployed) was 1.62 (95% CI: 1.16 to 2.28). These relationships remained after further adjustments for age, marital status, housing conditions, and country of birth. In women, the relationship between SES and incidence of stroke were even stronger (Table 2).
Subtype of Stroke in Relation to Socioeconomic Status
Among those who experienced a first-ever stroke (n=1648), 1301 (79%) were classified as ischemic infarction, 205 (12.4%) as cerebral hemorrhage, and 92 (5.6%) as subarachnoid hemorrhage. The remaining 50 cases (3.0%) were unspecified. Because of the limited number of stroke events with subarachnoid or unspecified origin, the analyses were only performed in ischemic and intracerebral hemorrhagic subtypes.
In both genders, the adjusted risk of ischemic subtype was significantly and inversely associated with annual income (Table 3). This relationship was, although based on fewer events, even stronger in women. No significant associations were observed between hemorrhagic subtype and SES. Men whose occupation was classified as “skilled manual workers” or as “others” had a significant increased risk for hemorrhagic subtype (RR :2.31, 95% CI: 1.01 to 5.43 and 2.89, 1.02 to 8.81, respectively).
Case-Fatality in Relation to Socioeconomic Status
Among stroke cases, 112 (6.8%) died within 28 days after the event and 195 (11.8%) died within 1 year. Case-fatality had remarkable relations with annual income but not with occupation class (data not shown). Among men, there was a significant increasing risk for 28-day fatality with decreasing income (probability value for trend=0.01; Table 4). However, this inverse association was not found in women. A similar result was revealed when 1-year fatality was examined (Table 4).
Recurrent Events in Relation to Socioeconomic Status
The stroke recurrence rate was 16.7% (183 men and 92 women) at the end of follow-up. In women, the risk of recurrent stroke, after adjustment of covariates, increased significantly in line with a decreased annual income (probability value for trend=0.02; Table 5). For men, no apparent relation was found.
As shown in other population-based studies,1–4 incidence of stroke and case-fatality rates increased with decreasing SES, being the highest among individuals with low annual income or with manual work conditions, but also among those being early retired or unemployed. However, the effects of SES on stroke differed by gender. The 28-day and 1-year case-fatality rates, respectively, increased linearly with a decreasing annual income in men. Such an association was not observed among women. On the other hand, the association between SES and incidence of stroke seemed to be somewhat stronger in women as compared with men. Little is known about stroke recurrence in relation to SES. The present study showed a significant relationship between income and stroke recurrence in women but not in men.
Few previous studies have reported gender differences regarding the impact of SES on stroke and the results are inconsistent.4,6,7 The results by Lisabeth et al6 are in accordance with our findings. In that study, a significant strong association between ischemic stroke and neighborhood SES score was found in women but not in men.6 However, a comparable gender-specific effect of socioeconomic index on the incidence of stroke was reported in a study from northern Sweden.7 In addition to that, a Finnish study reported strong relationships between income and 28-day case-fatality rates after ischemic stroke among men, but the association was less striking in women.16
The conflicting results may be attributable to several circumstances. Differences in study design may be one explanation such as sample size, age restriction, definition of SES, statistical approaches, and so on. Today, it is still debated whether there is a gender-related socioeconomic index on stroke.17 Although there are no convincing explanations so far, it should be noticed that the gender differences are present in terms of clinical presentation, management, and outcome among patients with stroke.18,19 Presence of ischemic heart diseases and diabetes, conditions both related to SES,20 are more commonly found among male than female patients with stroke.18,19 The high comorbidity rates associated with male patients with stroke may be one of the explanations for the strong association between short- and long-term case-fatality and SES. In addition, the findings from a large European study of hospital admissions for acute stroke indicate that the diagnostic procedures, including brain imaging, Doppler examination, echocardiogram and angiography, and aggressive therapy (eg, carotid endarterectomy) are less frequently performed in female than male patients.18 It is unknown, however, whether such gender-specific differences exist in Sweden with its equalized structure of health care. Gender differences in personal characteristics and behaviors may also be related to attitudes to access to medical care system, awareness about the disease, or to differences in compliance of medical intervention and modification of unhealthy lifestyle.
To our knowledge, only few studies have explored the effects of SES on subtypes of stroke.3,4,8,9 Our results, in line with previous reports,3,4 demonstrated that the inverse association between stroke and SES was mainly observed for ischemic subtype. In a Finnish study, it was reported that the age-standardized incidence and mortality of intracerebral hemorrhage was inversely related to income levels.8 Similar results have been documented from the United States in which educational attainments were measured.9 In the present study, no association was found between income and hemorrhagic stroke. However, men with skilled manual jobs or unemployed/retired had a higher risk of hemorrhagic subtype. The nonsignificant finding, particularly in women, may be explained by limited power due to low number of events.
The strength of this study lies in a large population-based setting with the ascertainment of all cases within a population defined by age and geographic region. A large number of stroke events were followed for a long period of time. The STROMA register has systematically and actively searched for patients with symptoms of stroke since 1989 in the city of Malmö.12 All cases were validated by the same experienced research nurse. There is no reason to consider that biased case retrieval or validation of cases has confounded the results.
Some limitations are worth noting. The main limitation of the study is that no information was available to investigate the causal factors, which may contribute to stroke inequality by SES, eg, behavioral factors or health-related problems.21,22 It is generally noticed that stroke subjects with low SES have higher blood pressure, body mass index, and higher prevalence of smoking, and so on. Adjustments for those factors would probably attenuate the observed association. However, a previous study from the Malmö Prevention Project has shown that SES is associated with stroke even after extensive adjustments of other risk factors.23 The information on SES was collected only in the questionnaire in 1990. It is likely that the annual income in some individuals changed during the years of follow-up, especially among those who were earlier retied. In addition, lacking information on the prevalence of transient ischemic attack or subtype of ischemic stroke was another limitation of this study.
In this population-based study on middle-aged Swedish men and women, the risks of incident stroke, recurrence of stroke, and case-fatality increased with decreasing SES, being the highest among individuals with low annual income. However, the effects of SES on stroke differed by gender. The incidence of first-ever stroke, particularly ischemic subtype, and recurrent stroke increased with decreasing SES more strongly among women, whereas case-fatality showed a significant inverse association with SES among men only. Those findings may suggest that SES is a good proxy to identify the individuals at higher risk of stroke. Clinical preventive focus targeting those disadvantaged populations, hence, may reduce the high burden of stroke in the population.
Sources of Funding
This study was supported by grants from the Swedish Research Council (521-2007 to 1919), the Swedish Heart-Lung Foundation (20060924), and funds from the Lund University, Malmö University Hospitals and the Region Skåne.
- Received October 19, 2007.
- Revision received January 11, 2008.
- Accepted January 18, 2008.
Kuper H, Adami HO, Theorell T, Weiderpass E. The socioeconomic gradient in the incidence of stroke. Stroke. 2007; 38: 27–33.
Wolfe CDA, Rudd AG, Howard R, Coshall C, Stewart J, Lawrence E, Hajat C, Hillen T. Incidence and case fatality rates of stroke subtypes in a multiethnic population: the South London Stroke Register. J Neurol Neurosurg Psychiatry. 2002; 72: 211–216.
Avendano M, Kunst AE, Huisman M, Lenthe FV, Bopp M, Regidor E, Glickman M, Costa G, Spadea T, Deboosere P, Borrell C, Valkonen T, Gisser R, Borgan JK, Gadeyne S, Mackenbach JP. Educational level and stroke mortality: a comparison of 10 European populations during the 1990s. Stroke. 2004; 35: 432–437.
Boden-Albala B, Litwak E, Elkind MS, Rundek T, Sacco RL. Social isolation and outcomes post stroke. Neurology. 2005; 64: 1888–1892.
Lisabeth LD, Diez Roux AV, Escobar JD, Smith MA, Morgenstern LB. Neighborhood environment and risk of ischemic stroke. Am J Epidemiol. 2007; 165: 279–287.
Peltonen M, Rosen M, Lundberg V, Asplund K. Social patterning of myocardial infarction and stroke in Sweden: incidence and survival. Am J Epidemiol. 2000; 151: 283–292.
Jakovljevic D, Sarti C, Sivenius J, Torppa J, Mahoen M, Immonen-Raha P, Kaarsalo E, Alhainen K, Tuomilehto J, Puska P, Salomaa V. Socioeconomic differences in the incidence, mortality and prognosis of intracerebral hemorrhage in Finnish adult population. Neuroepidemiology. 2001; 20: 85–90.
Qureshi AI, Suri MFK. Sasd M. Hopkin N. Educational attainment and risk of stroke and myocardial infarction. Med Sci Monit. 2003; 9: 466–473.
Population and Housing Census 1990. Stockholm and Örebro: Statistics Sweden; 1992.
The National Register of Cause of Death. Stockholm, Sweden: Centre for Epidemiology, The National Board of Health and Welfare; 2002.
Jerntorp P, Berglund G. Stroke registry in Malmö. Stroke. 1992; 23: 357–361.
Ali Khan F. Epidemiology of stoke in an urban population—aspects of time, place and person. PhD Thesis. Malmö, Sweden: Department of Clinical Sciences, Lund University; 2005.
Swedish National Bureau of Statistics. Swedish Socio-Economic Classification. Stockholm, Sweden: The Bureau; 1982. Reports of Statistical Coordination, No 4 [in Swedish].
Jakovljević D, Sarti C, Sivenius J, Torppa J, Mähönen M, Immonen-Räihä P, Kaarsalo E, Alhainen K, Kuulasmaa K, Tuomilehto J, Puska P, Salomaa V. Socioeconomic status and ischemic stroke: the FINMONICA Stroke Register. Stroke. 2001; 32: 1492–1498.
Pilote L, Dasgupta K, Guru V, Humphries KH, McGrath J, Norris C, Rabi D, Tremblay J, Alamian A, Barnett T, Cox J, Ghali WA, Grace S, Hamet P, Ho T, Kirkland S, Lambert M, Libersan D, O'Loughlin J, Paradis G, Petrovich M, Tagalakis V. A comprehensive view of sex-specific issues related to cardiovascular disease. Can Med Assoc J. 2007; 176: S1–S44.
Di Carlo A, Lamassa M, Baldereschi M, Pracucci G, Basile AM, Wolfe CD, Giroud M, Rudd A, Ghetti A, Inzitari D. Sex differences in the clinical presentation, resource use, and 3-month outcome of acute stroke in Europe. Stroke. 2003; 34: 1114–1119.
Holroyd-Leduc JM, Kapral MK, Austin PC, Tu JV. Sex differences and similarities in the management and outcome of stroke patients. Stroke. 2000; 31: 1833–1837.
Kaplan GA, Keil JE. Socioeconomic factors and cardiovascular disease: a review of the literature. Circulation. 1993; 88: 1973–1998.
Kurth T, Berger K. The socioeconomic stroke puzzle. Stroke. 2007; 38: 4–5.
Lynch JW, Kaplan GA, Cohen RD, Tuomilehto J, Salonen JT. Do cardiovascular risk factors explain the relation between socioeconomic status, risk of all-cause mortality, cardiovascular mortality, and acute myocardial infarction? Am J Epidemiol. 1996; 144: 934–942.
Engström G, Hedblad B, Rosvall M, Janzon L, Lindgärde F. Occupation, marital status, and low-grade inflammation: mutual confounding or independent cardiovascular risk factors? Arterioscler Thromb Vasc Biol. 2006; 26: 643–648.