BMJ 2002;324:1247-1251 ( 25 May )

Papers

    Psychological stress and cardiovascular disease: empirical demonstration of bias in a prospective observational study of Scottish men
    Commentary: Psychosocial factors and health---strengthening the evidence base

Psychological stress and cardiovascular disease: empirical demonstration of bias in a prospective observational study of Scottish men

John Macleod, clinical research fellow a, George Davey Smith, professor of clinical epidemiology b, Pauline Heslop, research assistant b, Chris Metcalfe, research assistant b, Douglas Carroll, professor of applied psychology c, Carole Hart, research fellow d. 

a Department of Primary Care and General Practice, University of Birmingham, Birmingham B15 2TT, b Department of Social Medicine, University of Bristol, Canynge Hall, Bristol BS8 2PR, c School of Sport and Exercise Science, University of Birmingham, Birmingham B15 2TT, d Department of Public Health, University of Glasgow, Glasgow G12 8RZ

Correspondence to: J Macleod j.a.macleod{at}bham.ac.uk


    Abstract
Top
Abstract
Introduction
Methods
Results
Discussion
References

Objectives: To examine the association between self perceived psychological stress and cardiovascular disease in a population where stress was not associated with social disadvantage.
Design: Prospective observational study with follow up of 21 years and repeat screening of half the cohort 5 years from baseline. Measures included perceived psychological stress, coronary risk factors, self reported angina, and ischaemia detected by electrocardiography.
Setting: 27 workplaces in Scotland.
Participants: 5606 men (mean age 48 years) at first screening and 2623 men at second screening with complete data on all measures
Main outcome measures: Prevalence of angina and ischaemia at baseline, odds ratio for incident angina and ischaemia at second screening, rate ratios for cause specific hospital admission, and hazard ratios for cause specific mortality.
Results: Both prevalence and incidence of angina increased with increasing perceived stress (fully adjusted odds ratio for incident angina, high versus low stress 2.66, 95% confidence interval 1.61 to 4.41; P for trend <0.001). Prevalence and incidence of ischaemia showed weak trends in the opposite direction. High stress was associated with a higher rate of admissions to hospital generally and for admissions related to cardiovascular disease and psychiatric disorders (fully adjusted rate ratios for any general hospital admission 1.13, 1.01 to 1.27, cardiovascular disease 1.20, 1.00 to 1.45, and psychiatric disorders 2.34, 1.41 to 3.91). High stress was not associated with increased admission for coronary heart disease (1.00, 0.76-1.32) and showed an inverse relation with all cause mortality, mortality from cardiovascular disease, and mortality from coronary heart disease, that was attenuated by adjustment for occupational class (fully adjusted hazard ratio for all cause mortality 0.94, 0.81 to 1.11, cardiovascular mortality 0.91, 0.78 to 1.06, and mortality from coronary heart disease 0.98, 0.75 to 1.27).
Conclusions: The relation between higher stress, angina, and some categories of hospital admissions probably resulted from the tendency of participants reporting higher stress to also report more symptoms. The lack of a corresponding relation with objective indices of heart disease suggests that these symptoms did not reflect physical disease. The data suggest that associations between psychosocial measures and disease outcomes reported from some other studies may be spurious.

What is already known on this topic
Higher psychological stress has predicted coronary heart disease in several observational studies

Exposure to stress and heart disease outcomes were often based on self report so that a general tendency to negative perceptions may have generated a spurious association between higher perceived stress and heart disease symptoms

What this study adds
Perceived stress was strongly related to subjective symptoms of heart disease, including those leading to hospital admission

However, stress showed a weakly inverse relation to all objective indices of heart disease: socially advantaged men perceived themselves to be most stressed, and the "protective" effect of stress was probably attributable to residual confounding

Suggestions that psychological stress is an important determinant of heart disease may be premature




    Introduction
Top
Abstract
Introduction
Methods
Results
Discussion
References

Psychosocial factors---for example, psychological stress, are widely believed to be important determinants of heart disease.1-3 Exposures to such factors may influence health directly through neuroendocrine mechanisms or indirectly through their association with unhealthy behaviour. 4 5

Much of the evidence supporting this hypothesis comes from studies relating self reported psychosocial measures, such as perceived stress, to self reported health outcomes. Individuals with a general tendency towards negative perceptions of different aspects of life may over-report both psychosocial adversity and symptoms of disease, leading to a spurious association between adverse psychosocial exposure and health.6

Reeder stress inventory

The Reeder stress inventory consists of four statements:

In general I am usually tense or nervous

There is a great amount of nervous strain connected with my daily activities

At the end of the day I am completely exhausted mentally and physically

My daily activities are extremely trying and stressful

Participants indicate the extent to which each statement applies to them. A scoring system was employed to derive a summary score ranging from 1 (low perceived stress) to 8 (high perceived stress).

Studies using more objective outcomes have largely been conducted in populations where psychosocial adversity was associated with general social disadvantage. Therefore it is impossible to discount the possibility that the apparent "effects" of psychosocial exposure are due to residual confounding by other correlates of relative deprivation.7

An association between stress and social disadvantage is not inevitable, as the social distribution of perceived stress seems to vary with place and historical period.8 We explored the relation between self perceived stress and several indices of cardiovascular health within a workplace derived population of men in whom reported stress was not greater among the socially disadvantaged.9 By comparing the association between stress and a series of health outcomes dependent on self report to a different degree, we were able to assess the influence of reporting tendency.


    Methods
Top
Abstract
Introduction
Methods
Results
Discussion
References

Our investigation is based on a cohort of men recruited from 27 workplaces in Scotland between 1970 and 1973. Measurements at recruitment included cardiovascular risk factors, "Rose" angina, and six lead resting electrocardiography.10 Perceived stress was measured with the Reeder stress inventory (box), a four item questionnaire instrument widely used during the 1960s and 1970s. 9 11-14

The same workplaces were revisited in 1977, a mean of 5 years and 2 months from first screening. Around 50% of participants were rescreened using the methods as in the initial screening. Our study is based on 5606 men at first screening and 2623 at second screening with complete data on all measures. Full descriptions of the methods and procedures have been published elsewhere. 9 15

Men who died over the 21 years of follow up were identified through flagging at the NHS Central Registry in Edinburgh, which provides death certificates coded according to the ICD-9 (international classification of diseases, 9th revision). Deaths from cardiovascular disease were those covered by codes 390-459; coronary heart disease was covered by codes 410-414.

Data on hospital admissions for the same period were provided through linkage to the Scottish Morbidity Register. This has data on all admissions to Scottish hospitals, coded according to the contemporaneous revision of the international classification of diseases.16

Stress scores (1-8) were categorised as high (6-8), medium (4 and 5), or low (1-3). We calculated the distribution of coronary risk factors and the prevalence of angina and ischaemia at first screening associated with each category. We standardised all estimates for age and occupational class. We defined "incident" angina or ischaemia as angina or ischaemia at second screening in a participant without angina or ischaemia at first screening.


    Results
Top
Abstract
Introduction
Methods
Results
Discussion
References

Perceived stress showed a graded association with occupational class from a mean stress score of 4.4 in social class I to a mean stress score of 2.8 in social class V (P for trend <0.001). Table 1 shows the distribution of cardiovascular risk factors and prevalence of angina and ischaemia by perceived stress at first screening. Higher stress is associated with an adverse pattern of behavioural risk factors but shows no clear relation with physiological risk factors. A substantial trend of higher prevalence of angina with higher stress is apparent. Conversely, there is a weak, inverse association of prevalent ischaemia with baseline stress.


                              
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Table 1.  Relations between perceived stress, coronary risk factors, and prevalence of angina and ischaemia at first screening. Values are numbers (percentages) unless stated otherwise


                              
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Table 2.  Odds ratio (95% confidence intervals) for incident angina and ischaemia at second screening by reported stress category at first screening (low stress as baseline, mean follow up period 5 years 2 months)

Table 2 shows an age adjusted odds ratio for development of incident angina of 2.32 in participants with high stress compared with those with low stress. Further adjustment for social class and cardiovascular risk factors strengthened this relation. A dose-response association between stress and incident angina was seen. There was, however, an apparent weakly inverse relation between high stress and incident ischaemia.

Table 3 shows a higher rate of hospital admission with higher stress. This was most strongly apparent in relation to psychiatric disorders. Higher stress also strongly predicted admissions related to hypertension, varicose veins, and ill defined cardiovascular conditions. Patients admitted with angina showed a weak positive association with stress. Those admitted for acute myocardial infarction showed a weak inverse association with stress. Adjustment for social position and risk factors made little difference to most of these estimates.


                              
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Table 3.  Rate ratios (95% confidence intervals) for hospital admissions over 21 years from first screening by level of perceived stress at first screening

Table 4 shows a moderate inverse relation between stress and mortality from all causes, cardiovascular disease, and coronary heart disease. Adjustment for occupational class substantially attenuated this association, with further adjustment for risk factors having little influence.


                              
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Table 4.  Hazard ratios (95% confidence intervals) for mortality over 21 years from first screening by level of perceived stress at first screening




    Discussion
Top
Abstract
Introduction
Methods
Results
Discussion
References

A strong and substantial relation exists between self reported stress and self reported symptoms of coronary heart disease. A relation of similar strength and magnitude is seen between stress and admission to hospital for psychiatric disorders. A weaker and less substantial relation is apparent between stress and admissions to a general hospital, including those broadly classified as related to cardiovascular disease. No relation is apparent between stress and hospital admission for coronary heart disease. Higher stress is weakly associated with lower risk of ischaemia as detected by electrocardiography, admission to hospital for myocardial infarction, and mortality.

A proportion of individuals with coronary heart disease may never be treated in hospital and may have a normal resting electrocardiogram. However it seems unlikely that genuine coronary heart disease would not be associated with an increased risk of mortality in a middle aged male population followed up for over 20 years. The alternative, and more likely, explanation is that our "positive" findings were an artefact of reporting bias. Individuals who perceived and reported their lives as most stressful also tended to perceive and report more symptoms attributable to cardiovascular disease, leading to an association between heightened stress and angina. These individuals were also more likely to attend a health facility and to report their symptoms to a doctor. The mainstay of diagnosis is a history of symptoms.17 Self reported symptoms are also an important influence on decisions about hospital admission, particularly in situations where the condition is one where admission would normally be considered discretionary rather than mandatory. This is the most likely explanation for the positive association between stress and many categories of hospital admissions.

In our study, heightened stress showed typical associations with unhealthy behaviour. The expected relation between stress and admissions for psychiatric disorders and experience in other studies increases our confidence in the validity of our measure of stress. 9 11-13 However, we emphasise that our results are presented to show the way in which reporting bias and confounding can generate non-causal associations between psychosocial measures and health outcomes. These points do not depend on the validity or comprehensiveness of our stress measure. Given the predictable associations observed between conventional risk factors and a range of disease end points we have no suspicion that our results reflected an unusual study population. Furthermore, we do not believe that the issues we have highlighted have any less relevance to studies incorporating more recent or more elaborate measures of perceived stress or other self reported psychosocial constructs.

Given the plausibility of an effect of psychosocial adversity on physical health and the current popularity of psychosocial explanations for patterns of health in developed countries, it is important to clarify these issues. Spurious associations between exposures and outcomes are to be expected when both are substantially subjective. Adjustment for a measure of reporting tendency is unlikely to abolish this effect because reporting tendency is impossible to measure precisely.18 Relations with objective outcomes are more suggestive of important effects. However unless they are shown in populations where heightened exposure is not associated with social disadvantage, residual confounding is impossible to discount. Experimental studies could resolve this issue and indicate the potential, if any, for interventions targeting psychosocial exposure to improve population health.

    Acknowledgments

We thank Victor Hawthorne, Charles Gillis, David Hole, and Pauline MacKinnon whose work provided us with the data required for this analysis.

    Footnotes

Contributors: see bmj.com

Funding: This work was supported by a grant within phase two of the health variations research programme of the Economic and Social Research Council. Preliminary analyses on this dataset were undertaken by JM while he was supported by a clinical epidemiology training fellowship from the Wellcome Trust.

Competing interests: None declared.


    References
Top
Abstract
Introduction
Methods
Results
Discussion
References

1. Davison C, Davey Smith G, Frankel SJ. Lay epidemiology and the prevention paradox: the implications of the coronary candidate for health promotion. Sociol Health Illness 1991; 13: 1-19.
2. Greenwood DC, Muir KR, Packham CJ, Madeley RJ. Coronary heart disease: a review of the role of psychosocial stress and social support. J Pub Health Med 1996; 18: 221-231[Abstract/Free Full Text].
3. Hemingway H, Marmot M. Evidence based cardiology: psychosocial factors in the aetiology and prognosis of coronary heart disease: systematic review of prospective cohort studies BMJ 1999; 318: 1460-1467[Free Full Text].
4. Brunner E. Stress and the biology of inequality. BMJ 1997; 314: 1472-1476[Abstract/Free Full Text].
5. Schachter S, Silverstein B, Kozlowski LT, Herman CP, Liebling B. Effects of stress on cigarette smoking and urinary pH. J Exp Psychol: Gen 1977; 106: 24-30[CrossRef][Web of Science][Medline].
6. Watson D, Clark LA. Negative affectivity: the disposition to experience aversive emotional states. Psychol Bull 1984; 96: 465-490[CrossRef][Web of Science][Medline].
7. Davey Smith G, Harding S. Is control at work the key to socio-economic gradients in mortality? Lancet 1997; 350: 1369-1370[CrossRef][Web of Science][Medline].
8. Wainwright D, Calnan M. Rethinking the work stress "epidemic." Eur J Public Health 2000; 10: 231-234[Free Full Text].
9. Heslop P, Davey Smith G, Carroll D, Macleod J, Hart C. Perceived stress and coronary heart disease risk-factors: the contribution of socio-economic position. Br J Health Psychol 2001; 6: 167-178[CrossRef][Web of Science][Medline].
10. Rose GA, Blackburn H, Gillum RF, Prineas RJ. Cardiovascular survey methods. Geneva: World Health Organization, 1982.
11. Chapman JM, Reeder LG, Massey J, Borun ER, Picken B, Browning GG, et al. Relationships of stress, tranquilizers and plasma cholesterol levels in a sample population under study for coronary heart disease. Am J Epidemiol 1966; 83: 537-547[Free Full Text].
12. Reeder LG, Schrama PGM, Dirken JM. Stress and cardiovascular health: an international cooperative study: I. Soc Sci Med 1973; 7: 573-584.
13. Haynes SG, Levine S, Scotch N, Feinleib M, Kannel WB. The relationship of psychosocial factors to coronary heart disease in the Framingham Study: methods and risk-factors. Am J Epidemiol 1978; 107: 362-383[Abstract/Free Full Text].
14. Reeder LG, Chapman JM, Coulson AH. Socioenvironmental stress, tranquilizers and cardiovascular disease. Proceedings of the Excerpta Medica International Congress Series, 1968; 182: 226-238.
15. Davey Smith G, Hart C, Hole D, MacKinnon P, Gillis C, Watt G, et al. Education and occupational social class: which is the more important indicator of mortality risk? J Epidemiol Community Health 1998; 52: 153-160[Abstract].
16. Kendrick S, Clarke J. The Scottish record linkage system. Health Bull 1993; 51: 72-79.
17. Sackett DL. Clinical diagnosis and the clinical laboratory. Clin Invest Med 1978; 1: 37-43[Web of Science][Medline].
18. Macleod J, Davey Smith G, Heslop P, Metcalfe C, Carroll D. Limitations of attempts to adjust for reporting tendency in observational studies of stress and self-reported coronary heart disease. J Epidemiol Community Health 2002; 56: 76-77[Free Full Text].

(Accepted 29 November 2001)

Commentary: Psychosocial factors and health---strengthening the evidence base

John Lynch. 

jwlynch{at}umich.edu

Reading the paper by Macleod and colleagues I am reminded of growing up in Australia, where my parents impressed upon me the importance of not being a "whinger." In fact, it was common for my grandmother when asked how she was feeling to reply "musn't grumble." Such stoicism even in the face of malaise was thought to be a positive personality disposition.

In an ingenious use of data collected in the early 1970s, Macleod and colleagues utilised baseline and follow up self reported and clinical data, combined with subsequent hospital admissions and mortality to show that men who reported themselves as feeling more tense, nervous, and exhausted by the stress of daily activities were more likely to have angina (derived from self report) and to be admitted to hospital for certain conditions (influenced by self reports to the attending physician). However, higher stress was not associated with hospital admissions, for which there were more objective criteria, such as myocardial infarction. Nor was stress associated with mortality. The authors concluded that their results showed a reporting bias---that is, people who viewed their lives as more stressful were also more likely to report more symptoms attributable to cardiovascular disease.

This study will evoke a range of responses. Some may point out that the stress measure used here is rather old fashioned and so the results are not widely applicable. Contemporary psychosocial research investigates constructs like hostility, hopelessness, and depression, which are defined more precisely than stress, measured using more refined instruments, and have been linked to objective outcomes. 1 2 Others will argue that this is a good example of how the effects of psychosocial exposures on health may have been oversold. The nature of the effects of self reported stress found here are reasonably typical of the evidence generated from studies linking job stress and self reported outcomes like angina, and this paper may aid in greater understanding of such links.3

This study represents a cogent empirical example of how reporting bias can generate associations between self reported exposures and outcomes. This does not necessarily mean that all such associations are spurious, but it does illustrate the potential for reporting bias. Furthermore, Macleod and colleagues argued that when a psychosocial exposure is not linked to social disadvantage, associations between self reported psychosocial stress and self reported outcomes may be the result of reporting bias. When the psychosocial exposure is patterned by socioeconomic disadvantage associations may be---depending on the outcome---the result of reporting bias or residual confounding by unmeasured socioeconomic factors from across the life course.4 These points are well defined challenges for those of us trying to gain greater understanding of the role of psychosocial exposures. Investigators now have more reason than ever to address reporting bias and residual confounding in investigating the health effects of psychosocial exposures. They imply that the most convincing evidence for a causal role of psychosocial exposures will come from studies that have objective and self reported outcomes and have measured all the relevant covariates including other psychosocial factors and socioeconomic factors from all stages of the life course.5 I think that for many extant studies that will be tough to achieve. But as I have an aversion to whingeing perhaps it's just better to get on and try to ensure that future studies of the health effects of psychosocial exposures can address these challenges. Macleod and colleagues' results should not be seen as a threat to the study of psychosocial exposures and health. On the contrary, they help to strengthen the discipline.

    Footnotes

Competing interests: None declared.

The full version of this article appears on bmj.com


    References

1. Everson SA, Goldberg DE, Kaplan GA, Cohen RD, Pukkala E, Tuomilento J, et al. Hopelessness and risk of mortality and incidence of myocardial infarction and cancer. Psychosom Med 1996; 58: 113-121[Abstract/Free Full Text].]
2. Iribarren C, Sidney S, Bild DE, Liu K, Markovitz JW, Roseman JM, et al. Association of hostility with coronary artery calcification in young adults---the CARDIA study. JAMA 2000; 283: 2546-2551[Abstract/Free Full Text].
3. Bosma H, Marmot MG, Hemingway H, Nicholson AC, Brunner E, Stansfeld SA. Low job control and risk of coronary heart disease in Whitehall II (prospective cohort) study BMJ 1997; 314: 558-565[Abstract/Free Full Text].
4. J Macleod J, Davey Smith G, Heslop P, Metcalfe C, Carroll D, Hart C. Are the effects of psychosocial exposures attributable to confounding? Evidence from a prospective observational study on psychological stress and mortality. J Epidemiol Community Health 2001; 5: 878-884.
5. Harper S, Lynch JW, Everson SA, Hsu W-L, Raghunathan T, Kaplan GA. Lifecourse socioeconomic position and depression, cynical hostility and hopelessness in adulthood. Int J Epidemiol 2002. (In press.)

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Rapid Responses:

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Rose questionnaire is not what it seems
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bmj.com, 24 May 2002 [Full text]
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