STRESS, HEALTH, AND DISEASE

Allostasis and Allostatic Load

An important new attempt to understand the relationships between environmental and behavioral challenges and stressors, the physiological responses to these events, and disease uses the terms allostasis and allostatic load. Allostasis is the maintenance of overall stability (homeostasis) through the constant adjustment and balancing of various components in the process of adapting to challenge. Sterling and Eyer (1988) first used the term to describe cardiovascular system adjustments in response to rest and activity states. Later, the idea was generalized to other physiologic mediators, such as adrenal cortisol and the catecholamines. Allostatic load is the wear and tear the body experiences as a result of repeated allostatic response (McEwen, 1998; McEwen and Stellar, 1993).

Allostasis and allostatic load operate in all systems of the body and focus attention on the protective, as well as the damaging, property of the primary mediators of the stress response: cortisol and the catecholamines. The major aspects are summarized in Figure 2-1. First, the brain integrates and coordinates behavioral and physiologic responses (hormonal and autonomic) to challenge. Some challenges can be perceived as stressful; others are related to circadian rhythms and to coordination of the functions of sleep and waking with the environment. Second, individual differences in the capacity to cope with challenges are based on multilevel relationships between genetic, developmental, and experiential influences. Third, intrinsic to the autonomic, neuroendocrine, and behavioral responses to challenge is the capacity to adapt (allostasis); indeed, neuroendocrine responses, such as the release of cortisol, are by nature protective and acute. Problems arise only when they persist, so efficient initiation and cessation of these responses is vital. Negative effects result when allostatic responses to challenge or stress occur inappropriately or are terminated inefficiently. Fourth, allostasis has a price that is related to the degree of inefficiency in the response and to the number of challenges and stressors a person experiences. Allostatic load is more than chronic stress. It can also reflect a genetically or developmentally induced failure to cope efficiently with the daily challenges related to the sleep/waking cycle and other experiences. And it also includes contributions of lifestyle factors, such as diet, alcohol and tobacco use, physical activity, and sleep, through their influences on the production of stress hormones.

FIGURE 2-1

The Stress Response and Development of Allostatic Load. Individuals experience objective psychological and environmental conditions that are conducive to stress, referred to as stressors. The perception of stress is influenced by social, psychological, (more...)

Protective and Damaging Effects of Stress Mediators

A behavioral response to challenge or stress can be protective or damaging. The risk of harm or disease can be increased by such patterns of behavior as hostility or aggression, and it can be reduced by cooperation and conciliation. Cigarette-smoking, excessive alcohol consumption, high fat consumption, and exposure to physical hazards increase the risk, as does insufficient physical activity. The link of allostasis and allostatic load can be applied to various behavioral responses: Such behaviors as smoking, high alcohol consumption, and consumption of high-fat foods all have some perceived adaptive effects in the short-term but damaging effects if they persist. Behavior can attenuate some of the damaging effects of physiologic responses. For example, even a brief period of exercise can enhance glucose uptake by reducing the insulin resistance of muscle tissue (Perseghin et al.,1996).

The mediators of protective and damaging effects of allostatic responses are mainly adrenal steroids and catecholamines. Other hormones—such as dehydroepiandrosterone, prolactin, growth hormones, and the cytokines—also mediate adaptive or maladaptive effects, but their consequences are often specific to an organ or a system. Once the mediators are released, they produce their effects by acting on cellular receptors. The effects can be classified as primary effects; secondary outcomes, which are risk factors for disease; and tertiary outcomes, which are diseases themselves (McEwen and Seeman, 1999). The actions of the mediators adrenal glucocorticoids and catecholamines are shown in Figure 2-2. These substances act via receptors that trigger changes throughout the target cell (including changes in gene expression) that have long-lasting consequences for cell function. It is important to consider the short- and long-term consequences of hormone release for cell function. There are many examples of beneficial and adverse effects of the mediators of allostatic responses. These factors are introduced here and discussed in more detail later.

FIGURE 2-2

Allostasis in the Autonomic Nervous System and HPA Axis. Allostatic systems respond to stress (upper panel) by initiating the adaptive response, sustaining it until the stress ceases, and then shutting it off (recovery). Allostatic responses are initiated (more...)

In the central nervous system, catecholamines and adrenal steroids promote the storage and retrieval of memories of events, pleasant and unpleasant, associated with arousal. However, adrenal steroids acting with excitatory amino acid neurotransmitters are associated with cognitive dysfunction involving various mechanisms that promote atrophy and, in some extreme cases, the death of neurons, particularly in the hippocampal region.

In the cardiovascular system, autonomic responses, in part because of catecholamines, promote allostasis (adaptation) by adjusting heart rate and blood pressure according to the changing demands of sleeping, waking, and physical exertion. Damaging allostatic load occurs as a result of a failure to terminate blood pressure surges efficiently. This accelerates atherosclerosis and synergizes with metabolic hormones to accelerate non-insulin-dependent diabetes.

The immune system is particularly responsive to the mediators of allostatic response. Adrenal steroids and catecholamines promote the movement of immune cells to organs or tissues where they are needed to resist infection or other challenge, thereby enhancing the effectiveness of immune responses. But adrenal steroids also can increase allostatic load and suppress immune system response when they are secreted chronically or when their release from the adrenal cortex is not terminated properly.

Allostatic load is associated with at least four patterns of long-term harm to the body. The first is a perception of excessive stress. This can take the form of repeated events of various types that cause recurring increases in the release of stress mediators. For example, the amount and frequency of economic hardship are good predictors of decline in physical and mental functioning and even death (Lynch et al., 1997b). The second pattern involves a failure to adapt to recurrence of the same stressor. This leads to overexposure to stress mediators because of the failure to dampen response to a repeated event. Most people, for example, adapt to repeated public-speaking challenges, but some continue to show elevated cortisol concentrations, which indicate a failure to adapt (Kirschbaum et al., 1995). The third pattern entails the failure to terminate the hormonal stress response or the lack of appearance of the normal trough in the daily cortisol release pattern. Examples are increased blood pressure caused by work-related stress (Gerin and Pickering, 1995), increased evening cortisol and hyperglycemia caused by sleep deprivation (Van Cauter et al., 1997), and the chronically elevated cortisol that often accompanies depressive illness (Michelson et al., 1996). The fourth pattern involves inadequate release of hormones, thus allowing other systems, such as inflammatory cytokines, to become overactive. In the Lewis rats, for example, inadequate release of cortisol is associated with increased susceptibility to inflammatory and autoimmune disturbances (Sternberg, 1997; Sternberg et al., 1996).

THE BRAIN AS INTERPRETER, REGULATOR, AND TARGET

The brain is influenced by experiences, including stress, and it is a target of allostatic load, or long-term wear and tear. Since the IOM (1982) report, advances in basic neuroscience and the development of imaging technology have combined to enhance our understanding of how different regions of the brain control behavior. They reveal the plasticity and vulnerability of the brain to effects of life experiences. Advances in the neurobiology of learning and memory have provided important insights into the dynamic nature of brain function throughout life and from the level of the gene to the level of nerve-cell structure and function. Studies of the interplay between brain development and early experience have emphasized their importance in establishing patterns of brain function that persist through life. This section discusses advances in neurobiology that are particularly relevant to the brain as an interpreter of life events, as a regulator of the stress response and daily biological rhythms, and as a target of the protective and the damaging functions of stress mediators. Developmental issues are discussed later in the chapter.

IMMUNE SYSTEM FUNCTION IN HEALTH AND DISEASE

The rebirth of integrative physiology in the context of the growing pool of information about genes and gene regulation has led to the development of new interdisciplinary fields of study, such as neuroendocrine immunology and psychoneuroimmunology—the latter includes psychology and an eclectic mix of other disciplines. At the same time, the more traditional field of immunology has advanced with growing knowledge about the messengers of the immune system, the cytokines and chemokines. Those advances underline the importance of explaining how the immune system functions in the living body, as opposed to examining only its theoretical workings. The immune system is highly integrated with other physiologic systems. It is sensitive to virtually every hormone in the body, and sympathetic, parasympathetic, and sensory nerves innervate the organs of the immune system. These organs also produce hormones that affect cells in the rest of the body. The remarkable capacity to distinguish “self” from “nonself” to protect the body from infectious and malignant challenges is a hallmark of the immune system that has been studied in great detail at the cellular and molecular levels over the past 50 years.

Much progress has been made recently in explaining how the body responds to environmental challenges through immunologic pathways. Research has led to development of the notion of a “danger” hypothesis in which tissue damage (and perhaps a threat to the very survival of the organism) is a signal that activates inflammatory and immune responses (Fuchs and Matzinger, 1996). The response of the immune system to environmental challenge represents a coordinated pattern of gene expression that results in rapid and sustained production of activated cells, secretory products, and effector mechanisms that persist until the challenge is eliminated.

Like many other bodily and behavioral responses to challenge, immune system responses are initially beneficial, but when they are sustained, they can damage healthy host tissue or augment damage produced by pathogens. That potential threat is reduced by the high level of regulation of the immune system and its close integration with the autonomic and endocrine systems. Bidirectional interaction of common chemical messengers and cellular receptors connects the immune system with the nervous system and the endocrine system. In this interactive communication between systems, sensory stimuli to the central nervous system that activates the HPA axis result in the peripheral release of adrenal steroids and catecholamines, both of which can have immunoregulatory effects. Similarly, a challenge that induces an inflammatory response causes the release of cytokines that stimulate the peripheral and central nervous systems (Figure 2-3). This provides an important link through which the neuroendocrine response modulates the development of an inflammatory response at the site of challenge. That is especially important in the lungs, heart, brain, and kidneys, where there are limits to the magnitude an inflammatory response can reach without causing loss of critical function (Hermann et al., 1995).

FIGURE 2-3

Neuroendocrine Regulation of Immunity. Tissue damage, infection, and malignancy are hypothesized to generate a danger signal. This signal is transduced at the cellular and molecular levels leading to activation, trafficking and expression of effector (more...)

The movement of immune cells to organs and tissues where they are needed to fight infection or other challenge is highly regulated at multiple levels, including interactions among neural, endocrine, and immune systems (Fauci, 1975; Hermann et al., 1995). Steroid hormones and catecholamines released from the adrenals promote the movement of immune cells. These steroid hormones and catecholamines are immuno-suppressive when they are secreted chronically or when their release is not terminated properly—in which case they can actually increase susceptibility to infection and malignancy (Dobbs et al., 1993; Hermann et al., 1993). A deficiency of circulating glucocorticoids and catecholamines, however, allows other immune mediators, such as cytokines, to overreact and thereby increase the risk of autoimmune and inflammatory disorders (Sternberg et al., 1992, 1989; Wilder, 1995).

ADDITIONAL FACTORS INFLUENCE LONG-TERM EFFECTS OF STRESS

CARDIOVASCULAR HEALTH AND DISEASE

Cardiovascular health and disease provide an example of the interactions of behavioral, psychologic, and social factors. This discussion of CHD will be used to point out the biological effects of stress and the psychosocial influences that exist. Despite progress in elucidating the role of genetics in human disease, it is clear that no single cause of CHD can be identified and that these conditions develop as a result of complex interactions among multiple factors.

One example of the effects of disparate factors on the incidence of cardiovascular disease is provided by a recent analysis of changing mortality patterns in Russia (Notzon et al., 1998). Over a 4-year period after the breakup of the former Soviet Union, mean life expectancy declined by 5 years. Most of the decline could be attributed to increased mortality in men aged 25 to 64 because of accidents and cardiovascular disease. Factors implicated in the dramatic change in death rates included economic instability, chronic stress, depression, and the increased use of alcohol and tobacco.

DEVELOPMENTAL TRAJECTORIES

Development is important in the biological and behavioral processes that preserve health or lead to human disease throughout life. Cumulative experience, adaptive plasticity, physical and social exchange with surrounding environments, and genetic predisposition interact to influence development. The unique physiology of each person, partly encoded in the genome and partly determined by prior physical exposures and social experiences, generates the individual behaviors that influence morbidity and mortality.

Although developmental status is a continuing factor in health outcomes over life, it has heightened salience for immediate and long-term health responses during infancy, early childhood, and adolescence. These periods are characterized by extremely rapid biological and psychosocial change. The resolution of the developmental challenges faced at these times determine set points for homeostatic systems, as well as for adopting crucial health-related attitudes and behaviors. These outcomes, in turn, determine trajectories for subsequent biobehavioral functioning that can have long-term effects on health. Therefore, the periods of infancy, early childhood, and adolescence are highlighted here.

Early childhood, infancy, and even prenatal experiences appear to have long-term consequences for health because they influence the biological mechanisms that underlie stress reactivity. There are sociocultural consequences of these experiences as well (NRC, 2000). A secure attachment with a parenting person provides a protective modulator of the environmental influences on an infant. The mother/child attachment is affected by the infant's temperament, which is characterized by reactions to stimuli, the tone of the emotional expression (positive or negative), activity level, and sociability. There is increasing evidence that temperament has a biological base (Boyce et al., 1992), including a genetic component that is heavily influenced by experience (van der Boom, 1994). The minority of infants who have difficult temperaments can experience attachment problems and high levels of stress, with consequences for their stress responses as adults. Unresponsive, insensitive, or abusive parenting also can lead to atypical emotional development. Research with infants of depressed mothers, for example, has shown that diminished parental responsiveness is associated with changes in infant emotional regulation and the balance of left vs. right frontal cortical activation (Dawson et al., 1997). A disproportionate number of severely deprived infants raised in Romanian orphanages exhibited abnormalities in cognitive, emotional, and linguistic development (Fisher et al., 1997). They also showed retarded growth and higher rates of infectious diseases (Albers et al., 1997; Hostetter et al, 1991).

Stress in young children can influence future health. Although currently limited to retrospective analyses, studies of physical and sexual abuse in childhood suggest variable but elevated risk for later depression, somatization, excessive rates of health care use, homelessness, and other indicators of behavioral maladaptation (Cheatsy et al., 1998; Herman et al., 1997; Salmon and Calderbank, 1996; Styron and Janoff-Bulman, 1997). A recent prospective controlled study (Heim et al., 2000) found that, during a relatively mild stress task involving public speaking and mental arithmetic, those with a history of sexual abuse showed significantly elevated concentrations of adrenocorticotropic hormone. This was most pronounced in participants who exhibited symptoms of major depression at the time of testing. The results provide support for increased stress vulnerability and altered HPA axis function in adults who were abused as children (Heim et al., 2000). Elevated prolactin response to serotonin challenge has been found among abused children (Kaufman et al., 1998; Pine et al., 1997), suggesting that the experience could be associated with dysregulation of serotonergic neurotransmission. Activation of specific neuroendocrine systems, such as the HPA axis, also has been found in conditions of normative, acute stress, such as that which accompanies the transition to primary school (Boyce et al., 1995), and prolonged extreme neglect and sensory deprivation, such as adverse rearing in a Romanian orphanage (Gunnar, 1998). Furthermore, chronic stressors in early childhood could impair the emergence of higher cognitive processes such as memory (Nelson and Carver, 1998). The potential for “recovery” from prolonged, severe early adverse experiences through later enrichment is still unknown. All are important areas for research.

Behavioral factors, such as physical activity and diet, are significant in setting health trajectories in children. Nearly half of American children are not regularly physically active, and physical activity declines dramatically among older children (U.S. Department of Health and Human Services, 1996). In the United States, children currently are 20–30% less active than is recommended by the World Health Organization (Salbe et al., 1997). Childhood activity is associated with relative weight, parental obesity, and the proportion of time spent outdoors (Klesges et al., 1990). These statistics are important because the prevalence of overweight children between the ages of 6 and 11 in the National Health and Nutrition Examination Study increased from 5% to 22% between 1976–1980 and 1988–1991 (Troiano et al., 1995). In the Bogalusa Heart Study, the prevalence of overweight 5- to 24-year-olds doubled between 1973 and 1994 (Freedman et al., 1997). Evidence is growing that obesity in childhood has psychosocial consequences and portends greater risk of disease in adulthood (for reviews, see Dietz, 1998; Must and Strauss, 1999).

Adolescence provides another important period for promoting healthy behaviors. Many of the behaviors associated with adult morbidities and even mortality, such as cigarette smoking, alcohol and drug abuse, unsafe sexual practices, and violent or aggressive responses to stress often begin in adolescence. But because adolescents, in general, are curious about and interested in their bodies, that time of life also provides opportunities to promote good health and to involve young people in decision making about themselves. Effective early intervention can prevent the onset of health-compromising behaviors and can work to prevent their becoming less firmly established as life-long patterns (Millstein et al., 1993).

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