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Job Strain and Anger Expression Predict Early Morning Elevations in Salivary Cortisol

From the Department of Psychology (A.S., M.C., J.G.), St. George’s Hospital Medical School, University of London, London, United Kingdom; and Department of Physiological Psychology (C.K.), University of Trier, Trier, Germany.

Address reprint requests to: Dr. Andrew Steptoe, Department of Psychology, St. George’s Hospital Medical School, Cranmer Terrace, London SW17 0RE, United Kingdom.

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

 
OBJECTIVE: The objectives of this study were to test the hypothesis that high job demands and low job control (job strain) are associated with elevated free cortisol levels early in the working day and with reduced variability across the day and to evaluate the contribution of anger expression to this pattern.

METHODS: One hundred five school teachers (41 men and 64 women) classified 12 months earlier as high (N = 48) or low (N = 57) in job strain according to the demand/control model sampled saliva at 2-hour intervals from 8:00 to 8:30 hours to 22:00 to 22:30 hours on a working day. Anger expression was assessed with the Speilberger State-Trait Anger Expression Inventory, and negative affect was also measured.

RESULTS: Free cortisol was significantly elevated at 8:00 to 8:30 hours in the high job strain group but not at later times of the day or evening. After adjustment for age and negative affect, cortisol was an average of 21.7% higher early in the working day in the high job strain group. This effect was significantly greater in high job strain teachers, who also reported high anger-out. The cortisol decline from morning to evening was greater in the high than low job strain individuals. Independently of job strain, women had a higher cortisol concentration at 8:00 to 8:30 hours than men, whereas cortisol concentration was greater in men than women in the middle of the working day between 12:00 and 16:30 hours.

CONCLUSIONS: Job strain is associated with elevated free cortisol concentrations early in the working day but not with reduced cortisol variability. The interaction with outward anger expression suggests that individual characteristics modulate the impact of chronic work stress on the hypothalamic-pituitary-adrenocortical system.

Key Words: jobstrain • cortisol • anger • work stress • teaching

Abbreviations: HPA = hypothalamic-pituitary-adrenocortical.

	INTRODUCTION

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Work stress has emerged as a major psychosocial influence on physical and mental health over recent decades (1). The demand/control model has proved valuable in understanding the work characteristics associated with coronary heart disease risk (2), hypertension (3), mental health (4), quality of life (5), and other outcomes (6). This model proposes that people working in highly demanding jobs who also have low control and limited opportunities to use skills will experience high job strain. The HPA axis is one of the principal pathways activated as part of the physiological stress response (7, 8). It is puzzling, therefore, that clear links between cortisol and work stress have not been established. This study used serial sampling over the working day to determine whether salivary cortisol was predicted by measures of job strain taken 1 year earlier in men and women working in a single occupation.

Several approaches to the investigation of cortisol and work stress have been taken. Cross-sectional studies with a single saliva or blood sample have generally not shown consistent associations with different aspects of work stress (9, 10), and in two studies, cortisol was lower in individuals reporting high job strain (11, 12). No significant differences between cortisol concentrations in urine excreted on working and nonworking days have been reported in several investigations (13–16), and a similar result has been obtained for plasma adrenocorticotrophic hormone (17). However, associations between work characteristics and cortisol have been observed in some studies (18, 19). In a study of air traffic controllers, urinary cortisol concentration was correlated with objective workload and perceived work difficulty (20). Another investigation of air traffic controllers found that salivary cortisol increased over work sessions, and responses were again related to workload (21). Luecken et al. (22) found that cortisol excretion during the working day in a sample of working women was not related to demands, control, or strain at work but was greater among those reporting high strain at home due to domestic responsibilities. More recently, Schulz et al. (23) compared cortisol responses to awakening in students reporting high and low chronic work overload. Repeated samples of saliva taken over the first hour after waking up on 3 consecutive days showed that chronically work-stressed students had significantly larger increases than those reporting low work stress.

This raises the possibility that the inconclusive effects observed in previous studies have arisen with cortisol assessed later in the day. However, it has also been proposed that the diurnal rhythm of cortisol output is disturbed with chronic stress and that maintenance of neuroendocrine activation after termination of stressful stimulation may characterize chronic allostatic load, leading to a "flat" circadian rhythm (8, 24, 25). We therefore obtained measures of salivary cortisol throughout the working day and evening and assessed differences between day and evening as well as early morning levels. We hypothesized that job strain would be associated with elevated cortisol early in the morning together with heightened cortisol later in the day. Such a pattern might lead to reduced variability in cortisol output over the working day.

An additional aim of this study was to investigate possible interactions between job strain and anger expression. Hostility and cynical distrust have been associated with increased risk of coronary heart disease and the progression of carotid atherosclerosis (26–28). The inhibition of anger expression has also been related to atheroma (29). Several experimental studies have linked anger expression and hostility with cardiovascular reactivity (30), and Suarez et al. (31) demonstrated heightened cortisol responses in hostile individuals who were harassed during behavioral task performance. Elevated cortisol excretion during the day has been found in cynically hostile students (32), although Van Eck et al. (33) showed no association between salivary cortisol sampled over the day and trait anger. In this study, we used the Speilberger State-Trait Anger Expression Inventory (34) to assess anger-in and anger-out. Anger-out scores on this measure are related to other indices of antagonistic hostility (35). A prospective design was used, with measures of job strain and anger expression obtained 1 year before cortisol monitoring. As a precaution against dysphoric mood influencing self-reported observations, negative affect was assessed and included as a covariate in analyses.

	METHODS

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Participants
Data were collected at the 12-month follow-up phase of a study of job strain and cardiovascular risk, details of which have been published previously (36). Participants in the original sample were 162 junior and high school teachers, selected on the basis of scores on a work stress measure (37) as having high (28 men and 52 women) or low (32 men and 50 women) job strain scores. Eighty-five (52.5%) were classroom teachers, and 77 (47.5%) had additional administrative roles. One hundred thirty-seven teachers took part in the 12-month phase (84.6%), which consisted of ambulatory blood pressure monitoring and a psychiatric interview (to be reported elsewhere) in addition to cortisol measurements. Of the 25 who did not participate at 12 months, 10 had left teaching or retired, 7 were seriously ill or pregnant, 1 experienced equipment failure, and 7 did not respond to our invitation. Comparisons between the 137 participants and 25 who dropped out of the study revealed no significant differences in gender, job strain scores, age, grade of employment, or scores on negative affect or anger expression. An additional 15 of the 137 individuals refused to sample saliva during the working day, mainly because they envisaged that data collection might be embarrassing or inconvenient at school. Statistical comparisons of these individuals with the remainder again identified no differences on demographic or psychological variables.

Measures
Job strain was assessed with a 10-item measure adapted from Karasek and Theorell (37). Three items indexed job demands (eg, "The pace of work in my job is very intense"), three items concerned perceived job control (eg, "I have freedom to decide what I do in my job"), and four related to skill utilization (eg, "My job involves me in learning new things"). Each item was rated on a four-point scale ranging from "strongly disagree" to "strongly agree." Scores for each dimension were scaled to range from 0 to a maximum of 10. An index of job strain was derived, where job strain = job demands/(job control + skill utilization). A job strain of 10 indicates a perfect balance between demands and control, with higher scores reflecting high demand coupled with low control and skill utilization.

Negative affect was assessed using the Positive and Negative Affects Schedule (38). Participants were asked about their general feelings or emotions over the past few weeks. Ten items contributed to the Negative Affect scale (including distressed and nervous), each of which was rated on a five-point scale from "very slightly or not at all" to "extremely." Ratings were summed to produce a total negative affect score ranging from a minimum of 10 to a maximum of 50.

Anger expression was assessed with the anger-in and anger-out items from the anger expression scales (34). Each consisted of eight items rated on a four-point scale describing ways people react when they are angry (eg, "I keep things in" for anger-in and "I make sarcastic remarks to others" for anger-out). Total scores for each scale could range from 4 to 32, with higher scores indicating greater anger-in or anger-out.

Procedure
Saliva sampling was conducted on a working day at schools. Participants were asked to take eight saliva samples at 2-hour intervals, and a 30-minute time window was allowed for each sample. Participants were asked to not consume any caffeine, citrus drinks, or food for at least 60 minutes before the saliva sample was taken. The schedule sampling sequence was therefore 8:00 to 8:30, 10:00 to 10:30, 12:00 to 12:30, 14:00 to 14:30, 16:00 to 16:30, 18:00 to 18:30, 20:00 to 20:30, and 22:00 to 22:30 hours. The first sample of the day was always obtained at schools after explanation of the procedure by the investigators. Saliva samples were collected in Salivettes (Sarstedt, Leicester, UK), which were stored at -30°C until analysis. After defrosting, samples were spun at 3000 rpm for 5 minutes, and 100 µl of supernatant was used for duplicate analysis involving a time-resolved immunoassay with fluorescence detection (39).

Analysis
Some participants went to bed before the last scheduled sample, so samples 7 and 8 (20:00–20:30 and 22:00–22:30 hours) were combined. Complete data for seven sampling points were available for 105 participants, and assays were incomplete for the other 17 participants. This was due predominantly to participants failing to take one or more samples, although in a few cases there was insufficient saliva for analysis. The data analyses are therefore based on a final sample of 105 participants. Comparisons were made on demographic and psychological variables between the 105 participants with complete data and those with missing data, but no differences emerged on any variable.

The profile of cortisol across the working day and evening was analyzed using repeated-measures analysis of variance with job strain (high or low) and gender as between-subject factors and time as a within-subject factor. The Greenhouse-Geisser correction of degrees of freedom was applied where appropriate. In separate analyses, anger-in and anger-out were introduced as between-subject factors. Subsequent analyses of individual sample times were conducted with analysis of covariance, including age and negative affect as covariates. Cortisol decline from morning to evening was measured by calculating changes between levels obtained at 8:00 to 8:30 and 20:00 to 22:30 hours. These were also analyzed with repeated-measures analysis of variance and covariance.

	RESULTS

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The characteristics of the sample are summarized in Table 1. The high and low job strain groups did not differ in gender distribution, age, occupational grade, or proportion of cigarette smokers. There were significant differences between groups in job strain (F(1,103) = 237.2, p < .0001) and in its components job demands, job control, and skill utilization (F(1,103) = 49.3, 140.5, and 27.9, respectively; p < .0001). The high job strain group reported greater demands, lower control, and less skill utilization than the low job strain group. Negative affect was significantly higher among high job strain individuals (F(1,103) = 23.0, p < .0001), and anger-in scores were also greater (F(1,103) = 8.88, p < .005). There were no differences in anger-out ratings between groups.

Repeated-measures analysis of cortisol samples across the day revealed a main effect of time (F(6,606) = 140.7, p < .001) together with significant job strain by time and gender by time interactions (F(6,606) = 3.19 and 6.32 respectively; p < .005). The three-way interaction of job strain, gender, and time was not significant. Figure 1 illustrates the job strain by time interaction. It is apparent that cortisol concentration was high early in the day, declined rapidly across the morning, showed a small postprandial increase in the early afternoon, followed by progressive reductions through the afternoon and evening. This pattern is typical of cortisol output over the day. High job strain subjects had higher cortisol levels on the first sample of the day with no differences at later times. Post hoc analysis of each sample with job strain and gender as between-subject factors and age and negative affect as covariates confirmed the significant job strain effect on the 8:00 to 8:30 sample (F(1,99) = 5.85, p < .025).

View larger version (13K): [in this window] [in a new window]   Fig. 1. Mean concentration of saliva free cortisol in high and low job strain groups across the day and evening.

View larger version (14K): [in this window] [in a new window]   Fig. 2. Mean concentration of saliva free cortisol in men and women across the day and evening.

Cortisol Decline From Morning to Evening
The analysis of cortisol decline from morning to evening showed a main effect of job strain (F(1,101) = 7.53, p < .01) but no gender differences. The mean cortisol decline adjusted for age and negative affect is illustrated in Figure 3, where it is evident that the decrease was substantially greater in the high than low job strain participants. Similar analyses were also conducted by dividing the sample into low and high groups on the basis of the three components of job strain. Although the cortisol decline from morning to evening tended to be greater in individuals reporting high job demands, low job control, and low skill utilization, the difference was significant only in the analysis of job control (F(1,101) = 4.01, p < .05). Control therefore seemed to be the most important component of job strain with respect to cortisol variation across the day.

View larger version (23K): [in this window] [in a new window]   Fig. 3. Mean decline in cortisol concentration between 8:00 and 8:30 hours and 20:00 and 22:30 hours, adjusted for age and negative affect, in participants divided on the basis of job strain, job demands, job control, and skill utilization.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION ACKNOWLEDGMENTS REFERENCES

The first cortisol sample of the day in this study was obtained between 8:00 and 8:30 hours before the commencement of school work. It can therefore be assumed that the job strain effects reflect anticipatory psychobiological responses, or the influence of early morning activities before formal work. Although samples were all collected under standardized conditions at schools soon after the teachers arrived for work, we did not find out about the time participants woke up. Cortisol concentration increases quite markedly in the first 30 to 45 minutes after awakening and then begins to decline. However, this response seems to be independent of sleep duration and time of awakening (40), so the length of time spent in bed or asleep the previous night is unlikely to account for the early morning differences.

We also hypothesized that teachers experiencing high job strain would have heightened cortisol later in the day and a consequent reduction in cortisol variability as indexed by morning-evening differences. The temporal profile of cortisol showed the expected reduction across the day, punctuated by a small increase after lunch as recently described by Gibson et al. (41). However, the prediction concerning cortisol variability was not confirmed. Instead, the decline in cortisol between morning and evening was actually greater in the high than low job strain groups (Figure 3). We found no evidence that chronically stressed high job strain teachers exhibited reduced variability or a flat circadian variation. This result suggests that HPA feedback regulation of cortisol output was unimpaired in the high job strain individuals, in contrast to the patterns reported with aging (24) and abdominal obesity (25).

One explanation for this finding is suggested by the recent observation of diminished cortisol responses to awakening in a group of school teachers considered to be burnt out according to their scores on the Maslach Burnout Inventory (42). It was also found that teachers with high levels of burnout showed increased suppression of cortisol after a low-dose dexamethasone challenge on the previous night. Different self-report measures were used in this study and the one by Pruessner et al. (42), so the comparability of the groups is not clear. We might, however, speculate that early morning cortisol levels show a biphasic pattern. Increases occur with chronic stress, as observed in the present investigation, while individuals struggle to meet their goals and performance demands. But once the person reaches a state of burnout, cortisol output is disrupted and falls below control levels. Hyposecretion of cortisol has been reported in other groups experiencing very severe prolonged stress (7, 43).

The elevation in cortisol recorded in the working day in high job strain teachers was present only among those who also had high anger-out scores. As can be seen in Table 2, the cortisol concentration at 8:00 to 8:30 hours was an average of 18.3% greater in the high than low anger-out members of the high job strain group. To our knowledge, this pattern has not previously been reported. Associations between ambulatory blood pressure and high scores on the Cook-Medley Hostility Scale have been described by a number of investigators (44, 45), and anger-out has been correlated with HPA responsiveness (46). It should be noted that anger-out was not directly associated with job strain (Table 1) and so is not elevated as part of the broader dysphoria observed in individuals reporting high job strain (47). In view of the role of outward expression of anger in hypertension (48) and other cardiovascular disorders, our results suggest that individual characteristics modulate the impact of chronic work stress on HPA activation.

An interesting gender difference was observed: Cortisol was higher in female than male school teachers early in the day, whereas levels were greater in men during the central working hours of the day (Figure 2). Pruessner et al. (40) also described a larger early morning increase in women than men. This may be a consequence of the additional domestic responsibilities of women before the working day, although the response was unrelated to the presence of children at home. The elevated level of cortisol during the central part of the day in men may reflect the pattern of heightened HPA responsivity to acute challenge described in the experimental literature (49, 50). The work situation may resemble the achievement-orientated tasks used in experimental studies, eliciting greater activation in men than women. We found no evidence of sustained cortisol activation in the evening among women, even when comparisons were made between women who had no children and those with childcare and domestic responsibilities (data not shown). Sustained activation of the sympathoadrenal axis through the evening has been described in women with managerial responsibilities (51), but the evidence relating parental status to neuroendocrine and cardiovascular function in the day and evening is mixed (16, 22, 52, 53).

The limitations of this study should be recognized. The investigation was performed with subjects from a single occupation rather than comparing job strain and other work characteristics across occupational groups. Because school teachers have broadly similar responsibilities, this means that the differences in job demands, control, and skill utilization reported by the high and low job strain groups are more a reflection of individual perceptions of the work situation than in studies where persons from different occupations are included. The reason for taking this approach is that professions or occupations differing in job strain may also vary in social status, physical activity, and other factors that might influence neuroendocrine function independently of work stress. However, the pattern of results may not be generalizable to other populations. We did not obtain data about awakening time and early morning activities, and these may have influenced the pattern of results. Nevertheless, the results of this study indicate that work stress may be associated with elevated cortisol levels, provided that information about variations across the day is collected. This study provides additional evidence of the potentially adverse impact of high job demands and low job control on human physiology.

	ACKNOWLEDGMENTS

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This research was supported by the Medical Research Council of the United Kingdom.

Received for publication June 2, 1999.

Revision received July 26, 1999.

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