Environmental sources of psychologic stress
Although blood pressure tends to rise with age, this is not an invariable phenomenon, and many societies have been described in which it remains low throughout life. The change with age appears to be determined culturally rather than genetically. A good example of this phenomenon is provided by a 30-yr observational study of Italian nuns living in a secluded order, reported by Timio. The nuns were compared with a control group both at entry and after 30 yr. blood pressures were the same at entry, but by the end of the study were approx 30 mmHg higher in the control subjects than in the nuns. The differences could not be explained by changes in body weight, by diet, or by childbearing. Fimio concluded that the differences were owing to the monastic and relatively stress-free environment in which the nuns were living.
The effects of social interactions on blood pressure have also been studied in experimental animals. Figure 6-3, taken from a study by Hallback, shows that in spontaneously hypertensive rats being reared in social isolation results in a lower blood pressure than when rats are reared in colonies.
In normotensive control rats, however, this environmental difference is without effect.
A similar series of observations has been made in people who migrate from a stable traditional society to a Westernized one. Studies of the nomadic Samburo in Kenya and of the bushmen of the Kalahari have shown no increase in blood pressure with age. Bushmen who abandon their traditional lifestyle, however, and become farm laborers, or even prisoners, have blood pressures 15 mmHg higher than the nomads. And Samburo warriors who joined the Kenyan army also showed an increase in blood pressure. Numerous other studies could be quoted confirming the effects of acculturation from structured traditional societies to contemporary Western life, but the problem with nearly all of them is that it is difficult to know exactly what factors were responsible for the rise in blood pressure. While stress may be one of them, there are also major dietary changes.
One of the most important of these studies is the Kenyan Luo migration study, in which 355 subjects who migrated from rural villages to Nairobi were followed prospectively for 2 yr after they migrated, and were matched with a control group that stayed in the villages. Even as soon as 1 mo after migrating, the distribution curve of blood pressure had shifted to the right in the migrants. There were also significant increases in body weight, heart rate, and urinary sodium:potassium ratio. Over the 2-yr follow-up period, the differences in blood pressure persisted, whereas those of body weight and heart rate did not. The authors suggested that the two factors responsible for the early increase in blood pressure were sodium retention and increased sympathetic nervous system (sympathetic nervous system) activity occurring in response to the stress of migrating. Urine catecholamines tend to be higher in Westernized Samoans than in those living a traditional village life.
Defense-Defeat Model
The defense reaction is a very fundamental response to challenges in the natural environment and consists of a generalized autonomic arousal, with an increase in blood pressure and cardiac output, and increased blood flow to the skeletal muscles. Many years ago Brod et al., observed this reaction and found that these changes resemble those seen in young patients with borderline hypertension. It has been proposed by Neel that “diseases of civilization” such as diabetes may occur as a result of natural selection, and that traits that confer red a survival advantage in primitive societies may be detrimental in modern society. Julius et al. have extended this concept to include hypertension, and propose that a permanent hemodynamic pattern of the defense reaction would lead to hypertension and insulin resistance.
On the basis of an extensive series of studies of mice housed in colonies designed to promote social interaction and conflict, Henry et al. proposed that two psychophysiologic patterns, which they referred to as the defense and defeat reactions, might determine which individuals become hypertensive and which do not. Their mice were housed in population cages consisting of boxes connected by narrow tubing, wide enough to accommodate only one mouse at a time. This promotes the development of a social hierarchy, in which the dominant animals develop higher blood pressures than the subordinates. Subsequent work showed that the highest blood pressures (160 mmHg) were seen in subdominants attempting to achieve control; the blood pressures in stable unchallenged dominants was 145 mmHg, and in the subordinates 125 mmHg. Similar results have been reported by Fokkema in rats, in which the subdominant individuals again had the highest blood pressures.
The subdominant animals are conceived as showing a chronic defense (fight or flight) reaction, characterized by activation of the sympathetic nervous system, whereas the subordinates exhibit the defeat reaction, in which there is activation of the pituitary-adrenal cortical axis.
Not surprisingly, comparable studies in humans are sparse. A situation analogous to the social interaction of mice in population cages was reported by D’Atri and Ostfeld, who studied men confined to prison. The systolic blood pressure (systolic blood pressure) of men who had lived for several months in a dormitory was 131 mmHg, whereas in men living in single-occupancy cells it was only 115 mmHg. Furthermore, transfer from a cell to a dormitory caused blood pressure to increase, and vice versa. These changes could not be attributed to diet, because all the prisonersate the same food.
Demand-Control and Effort-Distress Models
The subdominant individuals in the social hierarchy of the Defense-Defeat model may be perceived as attempting to achieve control. Two models that originated in Sweden, and that closely resemble each other, have some similarity to the model of Henry et al.. The first is the Job Strain model of Karasek and Theorell, which was specifically designed to assess occupational stress. It has two orthogonal components: psychologic demands, and decision latitude, which is equivalent to control. The most stressful (or “high-strain”) jobs are those that are perceived to combine high demands and low decision latitude. This model has been used mainly for studying the effects of job strain on the development of coronary heart disease, but, in my laboratory, we have shown that it may also be relevant in the development of hypertension. In the Cornell Worksite Study (originally a case-control study of men employed in a variety of jobs), we found that hypertensive individuals (the cases) were approximately three times as likely to be employed in high-strain jobs as the normotensive controls. Exposure to job strain was also associated with an increased left ventricular mass, which would be consistent with the effects of a sustained elevation in blood pressure. Subjects in high-strain jobs also had higher ambulatory blood pressure. Interestingly, this elevation in blood pressure was seen not only during working hours but also while at home and during sleep. An important aspect of the results is that neither of the two components of job strain — demands and perceived control — were individually associated with any changes in blood pressure; only the interaction of high demands and low control had an effect.
Two other interactive effects that were observed in our study are worth noting. The first was with alcohol intake. The highest blood pressures were observed in subjects who were in high-strain jobs and drank regularly. However, alcohol intake had no discernible effect on blood pressure in subjects with low-strain jobs. In the present context, alcohol intake may be regarded as another environmental pressor agent, whose intake is perhaps related to personality. The second interactive effect was with age. The effects of job strain on blood pressure were much greater in older than in younger subjects. This finding could have at least two explanations: first, the effects are cumulative over many years, and, second, the physiological susceptibility of the older subjects might be greater. In a 3-yr follow-up of 195 men in the Cornell Worksite Study, we found that the cross-sectional relationships between job strain and blood pressure were virtually identical 3 yr apart, although nearly half of the men had changed their job strain status. In addition, men who remained in high-strain jobs over the 3 yr had blood pressures at work and at home that were on average 11/7 mmHg higher than those in men in non-high-strain jobs at both times, and men who changed from a high-strain to a non-high-strain job showed a decrease of 5/3 mmHg. There was a small but insignificant increase in men who went from a non-high-strain to a high-strain job. These results strongly support the idea that the previously observed association between job strain and blood pressure is causal.
These findings have received some support from other studies. Theorell et al. studied 161 men with borderline hypertension with ambulatory monitoring and found that job strain (expressed by the ratio between psychologic demands and control) was significantly related to diastolic pressure during work and at night. Van Egeren studied 11 subjects with high-strain jobs and 26 with low-strain jobs, and found higher blood pressures in both groups during work and while at home in the former. There was a less clearcut tendency for sleep blood pressures to be higher as well. A third study, by Light et al., performed in 129 healthy young men and women found that job strain was associated with higher work blood pressures in men, but not in women.
A closely related model is the effort-distress model of Frankenhaueser. This also has two orthogonal components, which are termed effort and distress. Effort corresponds to demands in the job strain model, and distress to control. Effort is conceived as arousing the sympathetic nervous system, and distress the adrenocortical system. A typical example of this type of approach is provided by a study conducted by Lundberg and Frankenhaueser in which normal subjects performed two tasks. The first was a monotonous vigilance task that was perceived to induce effort and distress, and the second was a more enjoyable self-paced reaction-time talk, which required effort but without distress. During the vigilance task, urinary excretion of both epinephrine and cortisol increased, whereas during the reaction-time task only epinephrine increased. This model has not yet been related to sustained hypertension, but it is relevant because epinephrine and cortisol are both potential pressor hormones.
Models of Socioecologic Stress
The studies of the effects of acculturation, which I have briefly reviewed, suggest that there is something about modern society that tends to elevate blood pressure. Waldron et al. pooled data from 84 different societies and concluded that higher blood pressures were associated with increasing emphasis on a market economy, increased economy competition, and decreased family ties. These associations appeared to be independent of salt intake, and in men, of obesity.
In another series of studies, Dressier and colleagues have developed the concept of “lifestyle incongruity,” which is defined as the extent to which a high status style of life exceeds an individual’s occupational class. Its evaluation is relatively objective and is based on a match between occupation and income, on the one hand, and possession of material goods, on the other. Lifestyle incongruity has been found to be related to blood pressure not only in developing countries but also in African Americans in the United States.
A somewhat similar approach has been used by James et al., who developed the concept of John Henryism to investigate the effects of socioecologic stress in African Americans. An individual who scores high on the John Henryism scale is one who believes that he can control environmental stressors through a combination of hard work and determination. In their first study, James et al. found that men who scored below the sample median on education but above the median on John Henryism had higher blood pressures than men who scored above the median on both measures. In a subsequent study, they found that men who had achieved a relatively high level of job success and scored high on John Henryism had higher diastolic pressures than men with similar levels of job success and low John Henryism. Another psychosocial factor that contributed to higher blood pressures in the more successful men was the perception that being African American had hindered their chances of success.
The effects of socioecologic stress on blood pressure in African Americans have also been documented in a study by Harburg et al.. They performed a population survey of blood pressure in different neighborhoods of Detroit, which were defined as either high stress or low stress according to the socioeconomic status of the inhabitants (defined by variables such as income, home ownership, and education) and instability variables (e.g., crime rate and marital instability). The highest blood pressures were seen in African-American males under the age of 40 living in high-stress neighborhoods; African-American and Caucasian males living in low-stress neighborhoods had similar blood pressures. More recent research conducted in U.S. cities has provided further evidence for a “neighborhood” effect on blood pressure (people living in poorer neighborhoods have higher blood pressure, which is related to psychosocial factors independently of the traditional environmental influences.
Role of Genetic Factors and Race
As mentioned, hypertension evolves through an interaction of individual and environmental factors. Such individual factors are likely to be at least in part genetic. Thus, the mice in Henry et al.’s studies were of a certain strain, and experiments in other strains have not been found to replicate the hypertension. A good example of the role of genetic factors is provided by a study conducted by Henry et al. in different strains of rats, using a design similar to the studies conducted previously in mice, in which social interaction raised blood pressure. When subjected to the same protocol, there was no effect on blood pressure in Wistar-Kyoto hyperactive rats, a modest increase in Sprague-Dawley rats, and a much more marked increase in Long-Evans rats.
Another animal model of stress-induced hypertension is the borderline hypertensive rat, which is a cross between the spontaneously hypertensive rat and the normotensive Wistar-Kyoto rat. When reared in a benign environment, the borderline hypertensive rat remains normotensive, but if subjected to continued environmental stress or a high-salt diet, it becomes hypertensive.
In the United States, African Americans bear a greater burden of cardiovascular disease than Caucasians, and the prevalence of hypertension is approximately double. This difference, however, is much greater in the United States than in other countries. Several studies have documented that hypertension was traditionally relatively rare in Africa, with the exception of the big cities. It is also clearly established in longitudinal studies conducted mostly in Africa (described above) that moving from village to city life is associated with an increase in blood pressure, which suggests that environmental factors are predominantly responsible. A major unresolved issue is whether the higher prevalence of hypertension seen in African Americans in the United States compared with Caucasians is genetic or environmental. So far, attempts to identify genes or physiologic processes that distinguish “African-American hypertension” from “Caucasian hypertension” have proved disappointing. Several studies have found that African Americans with darker skin have higher blood pressures than those with light skin, which could be explained by either genetic or cultural factors. Although there have been reports of racial differences in physiologic regulatory processes such as sodium sensitivity, the renin-angiotensin system, and kallikrein, there is no evidence that these differences, which are usually subtle, are causally related to the differing prevalence of hypertension.
Considerable attention is currently being paid to identifying racial differences in genes that contribute to the development of hypertension, or that increase the susceptibility to environmental factors. An example is the angiotensinogen gene, in which a mutant allele has been reported to be related to blood pressure in Caucasians, and which has been found to occur much more frequently in African Americans in the United States and Nigeria. It cannot, however, be assumed that this explains the higher prevalence of hypertension in African Americans, because within African Americans there is no correlation between the presence of the mutant allele and blood pressure. It is possible that there are gene-environment interactions that predispose African Americans to the pressor effects of environmental stimuli, but these are difficult to demonstrate in human studies, because they require evaluation of the expression of a genotype in different environments. The problem is compounded by the fact that hypertension is almost certainly polygenic, so that the presence or absence of a particular allele is unlikely to account for more than a small effect on blood pressure.
Presently, the higher prevalence of hypertension in African Americans in the United States can best be explained by environmental factors. The prevalence of hypertension is inversely proportional to educational status, particularly in African Americans. A proportion of the racial differential can be explained by obesity (particularly in African-American women) and mineral intake, but potentially stronger and also less well-defined factors are psychosocial stress and racism. The low prevalence of hypertension in rural Africa has already been referred to, and there are populations in which an African-American-Caucasian blood pressure difference is absent or very small. One example is Cuba, and another is factory workers in England. In both populations it was concluded that the similarities of social class between the ethnic groups might account for the similarity in blood pressures. In the United States, there is such a strong association between race and socioeconomic status that it is quite difficult to separate the two.
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