Published online before print March 15, 2007, doi: 10.1161/STROKEAHA.106.473116
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(Stroke. 2007;38:1447.)
© 2007 American Heart Association, Inc.
Original Contributions |
Adaptation to Social Adversity Is Associated With Stroke Incidence
Evidence From the EPIC-Norfolk Prospective Cohort Study
From the Strangeways Research Laboratory and University of Cambridge Department of Public Health and Primary Care (P.G.S., N.W.J.W., R.L.L.), Worts Causeway, Cambridge, UK; the Medical Research Council Epidemiology Unit (N.J.W.), Elsie Widdowson Laboratories, Cambridge, UK; the Medical Research Council Dunn Human Nutrition Unit (S.A.B.), Cambridge, UK; and the Clinical Gerontology Unit (K.-T.K.), University of Cambridge School of Clinical Medicine, Addenbrooke’s Hospital, Cambridge, UK.
Correspondence to Paul Surtees, Strangeways Research Laboratory, Worts Causeway, Cambridge, CB1 8RN, UK. E-mail paul.surtees{at}srl.cam.ac.uk
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Abstract |
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Background and Purpose— Laboratory-based studies have suggested that individual differences in cardiovascular reactivity and stress adaptive capacity are associated with stroke incidence. We test the hypothesis that sense of coherence (SOC), a marker of social stress adaptive capacity, is associated with incident stroke in a population-based prospective cohort study.
Methods— A total of 20 629 participants, aged 41 to 80 years, in the UK European Prospective Investigation into Cancer (EPIC)-Norfolk study, who had not previously experienced a stroke, completed assessments that included SOC and details of their experience of life events during adulthood. An index of adaptation was constructed from responses to questions concerning over 80 000 adverse life events.
Results— During 145 000 person-years of follow-up (mean 7.1 years), 452 participants experienced either a fatal or nonfatal stroke event. A strong (as opposed to a weak) SOC was associated with a reduced rate of stroke incidence (rate ratio 0.76; 95% CI, 0.60 to 0.96) after adjustment for age, sex, pre-existing myocardial infarction, diabetes, hypertension treatment, family history of stroke, cigarette smoking, systolic blood pressure, obesity, social class, education, hostility and depression. No sex difference in this association was observed. Measures of social adversity occurrence and impact were not associated with stroke incidence, whereas faster reported adaptation to adverse event exposure was associated with a reduced rate of stroke incidence (rate ratio 0.89; 95% CI, 0.81 to 0.98; per standard deviation change in adaptation score, adjusted for age and sex).
Conclusions— Stress adaptive capacity is a potentially important candidate risk factor for stroke.
Key Words: epidemiology • follow-up studies • stress • stroke
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Introduction |
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There have been rapid improvements in the treatment of acute stroke and in the prevention and care of recurrent stroke,1 but there remains a growing global burden of stroke with diverse international stroke epidemiology.2,3 The traditional vascular risk factors for stroke outcomes have been shown to be similar to those for heart disease, a demonstration, for example, that hypertension is associated with increased risk of stroke4 and that blood pressure–lowering is effective in the reduction of stroke risk.5 However, only half of cardiovascular disease risk has been explained by conventional risk factors.6 Though recognized as important, and highly prevalent, limited emphasis has been given to the identification and study of psychosocial risk factors for stroke.7
Exposure to stress has been implicated in the development of hypertension,8 atherosclerosis,9,10 and in coronary heart disease outcomes11 and is a potentially important risk factor for stroke. This is strengthened by evidence concerning stroke incidence after extremely stressful circumstances; for example, stroke rates were shown to increase by 90% after the Hanshin–Awaji earthquake in the southern part of Hyogo Prefecture in Japan, in comparison with the same observation period during the previous year.12 Evidence suggesting that social stress experienced more commonly across a lifetime may be an independent risk factor for stroke has included studies of specific (or combinations of) life events such as divorce or death of spouse,13 or involuntary job loss,14 and studies based on measures of perceived stress.15,16 In addition, a case-control study has reported significantly more severely threatening life events to have been experienced during the year before stroke than among controls.17 Other work has investigated the hypothesis that stroke risk is related to excessive cardiovascular reactivity as revealed by laboratory stress tests. Increased systolic blood pressure reactivity to the anticipation of bicycle exercise was associated in healthy men with a 72% elevated stroke risk relative to those less reactive to the stress test.18 Evidence from a follow-up study of hypertensive men has also suggested that variation in the capacity to adapt to (laboratory-based) stressful situations was associated with a significantly increased incidence of stroke.19
A theoretical construct, sense of coherence (SOC), founded on the observations of Holocaust survivors has been hypothesized as a flexible and adaptive dispositional orientation enabling successful coping with adverse experience.20 Based on data collected from participants in the Norfolk (UK) European Prospective Investigation into Cancer (EPIC-Norfolk) study,21 we have previously demonstrated that a strong SOC is associated with reduced rates of all-cause and cardiovascular mortality22 and that SOC is a marker of an individual’s social stress adaptive capacity, such that those with a strong SOC report faster adaptation to adverse event experience.23 We now test the hypothesis that SOC will be associated with (fatal and nonfatal) stroke incidence: specifically, that a strong SOC will be associated with reduced stroke risk. In addition, we evaluate the association between stroke incidence and measures of social adversity exposure, including adaptation.
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Materials and Methods |
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Participants and Measures
Residents of Norfolk (UK) were recruited during 1993 to 1997 into the EPIC-Norfolk study using general practice age-sex registers.21 Baseline assessment included details of physician diagnosed diabetes, heart attack or stroke, together with an assessment of current and lifetime smoking behavior, hypertension treatment, family history of stroke, and education. Social class was classified according to the registrar general’s occupation-based classification scheme. A subsequent health check attendance included assessment of systolic blood pressure (mm Hg), based on the mean of 2 readings taken by trained nurses (after each study participant had been seated for 5 minutes), using an Accutorr sphygmomanometer (Datascope Medical Company Ltd). Height was measured (with shoes removed) to the nearest 0.1 cm using a free-standing stadiometer, and weight was measured (wearing light clothing) to the nearest 100 g using digital scales (Salter). Body mass index (BMI) was determined according to the Quetelet Index (weight in kilograms divided by height in meters squared). The study was approved by the Norwich District Health Authority Ethics Committee, and all participants gave signed informed consent. (See reference 21 for further details of study design and participant assessments.)
During 1996 to 2000 a total of 20 921 (of 28 582 eligible EPIC-Norfolk) participants completed the Health and Life Experiences Questionnaire (HLEQ), an assessment of social and psychological circumstances. The HLEQ included a 3-item SOC scale24 designed to assess each of the component constructs (comprehensibility, manageability and meaningfulness) by single questions: namely, ‘Do you usually feel that the things that happen to you in your daily life are hard to understand?’ (comprehensibility), ‘Do you usually see a solution to problems and difficulties that other people find hopeless?’ (manageability), and ‘Do you usually feel that your daily life is a source of personal satisfaction?’ (meaningfulness). Response choice was yes, usually (scored 0); yes, sometimes (scored 1); and no (scored 2). After reverse scoring for comprehensibility, all items were summed to provide a total SOC scale score within the range 0 to 6 with a lower score representing a stronger SOC.
The HLEQ included assessment of a set of specific adverse events experienced in adulthood. For each life event reported in adulthood, year of occurrence, event impact (through response to the question ‘How much did this upset you at the time?’) and event adaptation (through response to the question ‘Do you feel that you have got over this now?’) were assessed. Based on responses to these questions in the HLEQ sample (n=20 921), indices of event impact (I-Impact) and adaptation (I-Adapt) were constructed. These were designed to take account of variations in ratings of impact by event type, and variations in adaptation by event type and according to the number of years since each event was reported to have occurred. I-Impact was based on responses from 109 153 reported events, and I-Adapt on responses from 80 386 events. I-Impact and I-Adapt scores were standardized to have mean 0 and standard deviation 1. A positive I-Impact score represents a higher impact of adverse events experienced than the sample mean, and a positive I-Adapt score represents slower adaptation to the adverse effects of the adverse events experienced than the sample mean. (See reference 25 for full details of these assessments and of the derivation of these indices.)
EPIC-Norfolk HLEQ participants completed a revised form of the Personality Deviance Scales that included an 8-item hostility scale.26 Individual items were scored (in the range 1 to 4) and summed to give a scale range from 8 to 32, where a low scale score indicates increased hostility. In addition, the HLEQ included a structured self-assessment approach to psychiatric symptoms embodying Diagnostic and Statistical Manual of Mental Disorders (DSM-IV)27 criteria for major depressive disorder. As appropriate, study participants provided estimates of episode onset and offset timings. Current major depressive disorder was defined as any episode that was either current at the time of HLEQ completion or ended within 1 year of questionnaire assessment.28
All deaths among EPIC-Norfolk participants to March 31, 2005, were recorded through linkage with data from the UK Office for National Statistics. Data on all hospital admissions to March 31, 2005, throughout England and Wales were obtained for EPIC-Norfolk participants through linkage with the National Health Services health district database. Stroke mortality and morbidity was classified according to the International Classification of Diseases, Ninth Revision (ICD 9) as codes 430 to 438 (hemorrhagic stroke 430 to 432; cerebral infarction 433 to 435; stroke unspecified or other 436 to 438) or according to ICD 10 as codes I60 to I69 (hemorrhagic stroke I60 to I62; ischemic stroke I63, I65 and I66; stroke unspecified or other I64 and I67 to I69). Attending physicians assigned diagnostic codes for stroke events resulting in hospital admission.
Statistical Analysis
Mean (and standard deviation) SOC scale scores are presented for men and for women according to age, pre-existing myocardial infarction (MI), hypertension treatment, family history of stroke, pre-existing diabetes, cigarette smoking, systolic blood pressure, obesity (BMI 
30), social class, education, hostility and depression, with differences tested through analysis of variance. The association between SOC and incident stroke end points was investigated using Poisson regression taking account of duration of follow-up. SOC was coded as strong; scale score 0 or 1, and weak; score 2 to 6, consistent with previous analysis of these data.22 Results are presented as rate ratios (95% CI) for a strong versus a weak SOC for men and women both separately and combined, and for fatal and nonfatal stroke end points both separately and combined. The potential attenuation of this association with increased follow-up was investigated through inclusion of a time-dependent covariate representing each successive year of follow-up, and more specifically through inclusion of a linear interaction term between SOC and time. The dose-response association according to increasingly strong SOC was investigated for SOC scale scores 0 (strongest SOC), 1, and 2 versus SOC scale scores 3 to 6 (weakest SOC) as the reference catgory (with these categories combined because of smaller cell sizes) and tested through inclusion as a continuous measure in the Poisson regression model (a 1 degree of freedom test of trend). Associations are adjusted firstly for age (in 5-year bands) and sex, subsequently for pre-existing MI, pre-existing diabetes, hypertension treatment, family history of stroke, cigarette smoking, systolic blood pressure (included as a continuous variable), obesity, social class and education, and finally for hostility and depression (in addition to all the above). Adjustment for all risk factors resulted in a reduced sample size of 16 935 for analysis. Differences in measures of social adversity, defined by the number of either moderately or extremely upsetting life events (excluding participants’ own illness) experienced within the past 5 years, impact (I-Impact) and adaptation (I-Adapt) and SOC were tested through analysis of variance. The associations between these social adversity measures and (fatal and nonfatal) stroke end points were investigated using Poisson regression. For ease of comparison of effect sizes, results are presented as rate ratios per standard deviation decrease in each variable, adjusted firstly for age and sex, and subsequently for risk factors (as above).
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Results |
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After the exclusion of participants who reported a previous stroke (n=260), of those where pre-existing stroke was unknown (n=14), and of those who were admitted to hospital with a stroke between EPIC baseline and HLEQ completion (n=18), a sample of 20 629 (of 20 921) HLEQ participants was available for analysis. A total of 452 (2.2% of these 20 629) participants had at least one incident fatal or nonfatal stroke during a mean of 7.0 (and a total of 144 802) person-years of follow-up; an incidence rate of 3.1 per 100 000 person-years. Of these, 78 were hemorrhagic stroke, 188 were ischemic stroke, and the remaining 186 were undetermined. There were 223 stroke end points among 8939 men (3.6 per 100 000 person-years), and 229 among 11 690 women (2.8 per 100 000 person-years). The age range of the sample was from 41 to 80 years. In men and women combined, there were 131 fatal stroke end points and 417 hospital admissions, with 96 participants being admitted to hospital before subsequent death.
Completed SOC scale scores were available for 20 303 (98.4%) of 20 629 participants. Women reported a weaker SOC than men (mean (SD) 1.68 (1.14) for men, and 1.96 (1.15) for women, P<0.0001). Table 1 shows that, in this cohort, SOC was significantly associated with age (such that participants aged between 60 and 69 years had the lowest SOC scores, representing strongest SOC), hypertension treatment (such that participants who had been receiving treatment at baseline had weaker SOC), cigarette smoking status (such that current smokers had weaker SOC than former or never smokers), social class (such that those in lower social classes had weaker SOC), education (such that those who were educated to a lower level had weaker SOC), hostility (such that participants who were more hostile had weaker SOC) and depression (such that those with current depression had weaker SOC) in both men and women, and with obesity in women but not in men (such that obese women had weaker SOC than nonobese women). SOC was not associated either with pre-existing MI, family history of stroke, diabetes or with systolic blood pressure. Participants with a strong SOC reported fewer life events in the past 5 years than those with a weak SOC (mean 0.82 and 0.99 events for those with a strong and a weak SOC, respectively, P<0.0001). In addition, participants with a strong SOC reported that they were less upset and adapted faster to the adverse effects of life events than those with a weak SOC (mean I-Impact –0.14 and 0.10 and mean I-Adapt –0.21 and 0.15 for those with a strong and a weak SOC, respectively, both P<0.0001).
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Of 8509 participants who reported a strong SOC, 149 had an incident fatal or nonfatal stroke in 60 198 person-years of follow-up (2.5 per 100 000 person-years). Of the 11 794 participants who reported a weak SOC, 280 had a stroke end point in 82 408 person-years (3.4 per 100 000 person-years). Figure 1 shows a Kaplan–Meier survival plot and reveals that participants with a strong SOC had a reduced rate of (fatal and nonfatal) stroke incidence over follow-up. Table 2 shows the association between SOC and stroke, by sex, for fatal and nonfatal stroke end points separately, and with progressive adjustments. After adjustment for age, sex, cigarette smoking, systolic blood pressure, pre-existing MI, diabetes, hypertension treatment, family history of stroke, obesity, social class and education, a strong (as opposed to a weak) SOC was associated with a 26% reduced rate of incident (fatal and nonfatal) stroke (P=0.008). With further adjustment for hostility and major depressive disorder history, this association was slightly attenuated, though remained significant (P=0.02). This association was consistent for men and for women (though not significant in women, the rate ratios for men and for women were similar, and sex differences were not significant, P=0.95), and was broadly consistent for fatal as well as for nonfatal stroke end points. There was no evidence that the association between SOC and stroke incidence attenuated with increasing duration of follow-up (P=0.64 for test of linear interaction with time, adjusted for age and sex).
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Figure 2 shows the association between SOC and (fatal and nonfatal) stroke incidence according to incremental changes in SOC score and gives some support to a dose-response relation, such that increasingly strong SOC was associated with increasingly lower rates of stroke (P=0.02). Participants in the lowest (score 0, representing strongest SOC) versus the highest (score 3 to 6) category of SOC had a 42% reduced rate of (fatal and nonfatal) stroke incidence (rate ratio 0.58; 95% CI, 0.36 to 0.93; after adjustment for all risk factors above).
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Table 3 shows the association between the social adversity measures and (fatal and nonfatal) stroke. Neither the number of recently experienced upsetting life events or the index of impact (I-Impact) were associated with stroke incidence. However, the index of adaptation (I-Adapt) was associated with stroke incidence such that a one standard deviation decrease in adaptation score (representing faster adaptation) was associated with an 11% decreased rate of incident stroke (P=0.02), after adjusting for age and sex. The magnitude of this association was attenuated slightly with further adjustment for pre-existing MI, hypertension treatment, family history of stroke, cigarette smoking, systolic blood pressure, pre-existing diabetes, obesity, social class, education, hostility and depression. Participants who reported faster adaptation to the adverse effects of life event experience than the sample mean (=0) had an 
20% reduced rate of stroke incidence than those who reported slower adaptation (age-sex adjusted rate ratio=0.81; 95% CI, 0.67 to 0.99).
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Discussion |
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A strong sense of coherence was associated with a 25% reduced rate of stroke incidence after adjusting for prexisting MI, diabetes, hypertension treatment, family history of stroke, cigarette smoking, systolic blood pressure, obesity, social class, education, hostility and depression. This association was consistent by sex, was observed for both fatal and nonfatal stroke end points, did not attenuate with increasing length of follow-up, and followed a dose-response relationship, such that participants who reported the strongest SOC had a 40% reduced rate of stroke incidence relative to those who reported the weakest SOC. Importantly, given previous evidence of association between depression,29,30 and anger/hostility31 with increased stroke risk, our findings underpin SOC as defining a distinctive psychosocial concept that is not simply a proxy for measures of emotionality.32 An index of adaptation, constructed from details of over 80 000 life events experienced throughout adulthood, was associated with stroke incidence, such that participants who reported that their adaptation to the adverse effects of life events was faster than the sample average had a 20% reduced rate of stroke. Measures of social adversity occurrence or of its impact were not associated with stroke incidence.
Whereas the strengths of this study include the prospective ascertainment of stroke end points in over 140 000 person-years of follow-up, and the availability of baseline data that allowed adjustment for a wide range of (well and less well-documented) cerebrovascular risk factors, including specific chronic disease history, we are unable to exclude confounding with other conditions known to be associated with stroke risk. For example, silent brain infarcts and white matter lesions have been reported to be associated with increased stroke risk among elderly people, including in general population studies.33 In addition, the study design relied on a single assessment of SOC, operationalized by Antonovsky initially as a 29-item questionnaire,20 based here on a simplified 3-item measure. The original developers of the scale have reported satisfactory short-term test-retest reliability and validity for the 3-item measure,24 and its brevity will facilitate its future use within other large-scale prospective studies. Such studies should give careful consideration to questionnaire design to avoid the introduction of method variation bias.
Although we are unaware of any other published studies with which to directly compare our findings, other research potentially relevant to their interpretation concerns evidence that exaggerated cardiovascular reactivity to psychological stress is associated, after comprehensive adjustment, with carotid atherosclerosis,9 hypertension,8 coronary calcification,10 silent cerebrovascular disease,34 and (in a population-based study of men) stroke risk.18 These, and allied studies, used a diverse range of potentially stressful challenges, including exercise tolerance tests, video games, public speaking, memory, and Stroop Color-Word tests, to differentiate individual differences in stress reactivity. Of particular significance is further work demonstrating an association between chronic failure to master the conflict created through the serial Stroop Color-Word tests with significantly increased stroke incidence (in hypertensive men).19 Results from these studies follow from measures of individual difference established through laboratory-based stressful challenge tests. Our results may be interpreted as both complementing and aiding translation of this work into epidemiological settings.
Summary
Evidence is accumulating to support the salutogenic perspective introduced by Antonovsky, represented by SOC, as the capacity to tune available resources flexibly and proactively to meet the demands of specific circumstances.35,36 Evidence suggests, for example, that these personal characteristics, where strong, are associated with improved health biomarkers37 and the adoption of less risky lifestyle behavior.38 We have previously demonstrated SOC to be a marker of an individual’s social stress adaptive capacity23 and that a strong SOC is associated with reduced rates of all-cause and cardiovascular mortality.22 Our results, that both SOC and stress adaptive capacity (indexed through actual adverse event exposure) are associated with incident stroke, are consistent with previous findings concerning cardiovascular reactivity to psychological stress. Collectively, these results signal the potential of stress adaptive capacity as a candidate risk factor for stroke, and underpin the potential importance of a paradigm of flexibility39 for aiding understanding of the role of psychosocial factors for cardiac and now cerebrovascular health.
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Acknowledgments |
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We thank the participants and general practitioners who took part in this study and the staff associated with the research program.
Sources of Funding
EPIC-Norfolk is supported by programme grants from the Medical Research Council UK (G9502233, G0300128) and Cancer Research UK (C865/A2883) with additional support from the European Union, Stroke Association, British Heart Foundation, Department of Health, Food Standards Agency and the Wellcome Trust.
Disclosures
None.
Received September 18, 2006; revision received November 20, 2006; accepted December 11, 2006.
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