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Chronic stress, allostatic load, and aging in nonhuman primates

Published online by Cambridge University Press:  21 October 2011

Dario Maestripieri  and
Christy L. Hoffman
Dario Maestripieri*
Affiliation:
University of Chicago
Christy L. Hoffman
Affiliation:
University of Chicago
*
Address correspondence and reprint requests to: Dario Maestripieri, University of Chicago, 5730 South Woodlawn Avenue, Chicago, IL 60637; E-mail: dario@uchicago.edu.
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Abstract

Allostatic load is the “wear and tear” of the body resulting from the repeated activation of compensatory physiological mechanisms in response to chronic stress. Allostatic load can significantly affect the aging process and result in reduced longevity, accelerated aging, and impaired health. Although low socioeconomic status is associated with high allostatic load during aging, the effects of status-related psychosocial stress on allostatic load are often confounded by lifestyle variables. Chronic psychosocial stress associated with low dominance rank in nonhuman primates represents an excellent animal model with which to investigate allostatic load and aging in humans. Research conducted with free-ranging rhesus monkeys suggests that female reproduction can also be a source of stress and allostatic load. Female reproduction is associated with increased risk of mortality and hyperactivation of the hypothalamic–pituitary–adrenal axis. Reproduction is especially stressful and costly for aging females of low rank. Although many indicators of body condition and neuroendocrine and immune function are influenced by aging, there are marked and stable individual differences among aging females in body condition, plasma cortisol responses to stress, and cytokine responses to stress. These differences are consistent with the hypothesis that there are strong differences in chronic stress among individuals, and that allostatic load resulting from chronic stress affects health during aging. Comparisons between captive and free-ranging rhesus monkey populations may allow us to understand how differences in environmental stress and allostatic load affect rates of aging, and how these in turn translate into differences in longevity and health.

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Articles
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Development and Psychopathology , Volume 23 , Issue 4: Allostatic Load: Part 2 , November 2011 , pp. 1187 - 1195
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Copyright © Cambridge University Press 2011

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References

Abbott, D. H., Keverne, E. B., Bercovitch, F. B., Shively, C. A., Mendoza, S. P., Saltzman, W., et al. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior, 43, 67–82.CrossRefGoogle ScholarPubMed
Austad, S. N. (1993). Retarded senescence in an insular population of Virginia opossums. Journal of Zoology, 229, 695–708.Google Scholar
Austad, S. N. (1996). The uses of intraspecific variation in aging research. Experimental Gerontology, 31, 453–463.Google Scholar
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 16–25.Google Scholar
Clark, M. S., Bond, M. J., & Hecker, J. R. (2007). Environmental stress, psychological stress and allostatic load. Psychological Health Medicine, 12, 18–25.CrossRefGoogle ScholarPubMed
Coe, C. L. (1993). Psychosocial factors and immunity in nonhuman primates: A review. Psychosomatic Medicine, 55, 298–308.Google Scholar
Coe, C. L. (2004). Biological and social predictors of immune senescence in the aged primate. Mechanisms of Ageing and Development, 125, 95–98.CrossRefGoogle ScholarPubMed
Coe, C. L., & Ershler, W. B. (2001). Intrinsic and environmental influences on immune senescence in the aged monkey. Physiology & Behavior, 73, 379–384.CrossRefGoogle ScholarPubMed
Coe, C. L., & Laudenslager, M. L. (2007). Psychosocial influences on immunity, including effects on immune maturation and senescence. Brain, Behavior, and Immunity, 21, 1000–1008.Google Scholar
Crimmins, E. M., Kim, J. K., & Seeman, T. E. (2009). Poverty and biological risk: The earlier “aging” of the poor. Journal of Gerontology, Series A, 64, 286–292.CrossRefGoogle ScholarPubMed
Elsworth, J. D., Leahy, D. J., Roth, R. H., & Redmond, D. E. (1987). Homovanillic acid concentrations in brain, CSF and plasma as indicators of central dopamine function in primates. Journal of Neural Transmission, 68, 51–62.CrossRefGoogle ScholarPubMed
Epel, E. S. (2009). Psychological and metabolic stress: A recipe for accelerated aging? Hormones: International Journal for Endocrinology and Metabolism, 8, 7–22.Google Scholar
Epel, E. S., Blackburn, E. H., Lin, J., Dhabhar, S., Adler, N. E., Morrow, J. D., et al. (2004). Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences of the United States of America, 101, 17312–17315.Google Scholar
Finkel, T., & Holbrook, N. J. (2000). Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239–247.CrossRefGoogle ScholarPubMed
Ganzel, B. L., Morris, P. A., & Wethington, E. (2010). Allostasis and the human brain: Integrating models of stress from the social and life sciences. Psychological Review, 117, 134–174.CrossRefGoogle ScholarPubMed
Geronimus, A. T., Hicken, M. T., Keene, D., & Bound, J. (2006). “Weathering” and age patterns of allostatic load scores among blacks and whites in the United States. American Journal of Public Health, 96, 826–833.Google Scholar
Geronimus, A. T., Hicken, M. T., Pearson, J. A., Seashols, S. J., Brown, K. L., & Dawson Cruz, T. (2010). Do US black women experience stress-related accelerated biological aging? Human Nature, 21, 19–38.Google Scholar
Gersten, O. (2008). Neuroendocrine biomarkers, social relations, and the cumulative costs of stress in Taiwan. Social Science & Medicine, 66, 507–515.Google Scholar
Glover, D. A. (2006). Allostatic load in women with and without PTSD symptoms. Annals of the New York Academy of Sciences, 1071, 442–453.Google Scholar
Glover, D. A., Garcia-Arcena, E. F., & Mohlman, J. (2008). Peripheral biomarker composite associated with smaller hippocampal volume. NeuroReport, 19, 1313–1320.CrossRefGoogle ScholarPubMed
Goldman-Rakic, P., & Brown, R. M. (1981). Regional changes of monoamines in cerebral cortex and subcortical structures of aging rhesus monkeys. Neuroscience, 6, 177–187.Google Scholar
Gruenewald, T. L., Seeman, T. E., Ryff, C. D., Karlamangla, A. S., & Singer, B. H. (2006). Combinations of biomarkers predictive of later life mortality. Proceedings of the National Academy of Sciences of the United States of America, 103, 14158–14163.CrossRefGoogle ScholarPubMed
Gust, D. A., Gordon, T. P., Hambright, K., & Wilson, M. E. (1993). Relationship between social factors and pituitary-adrenocortical activity in female rhesus monkeys (Macaca mulatta). Hormones and Behavior, 27, 318–331.Google Scholar
Gust, D. A., Wilson, M. E., Stocker, T., Conrad, S., Plotsky, P. M., & Gordon, T. P. (2000). Activity of the hypothalamic–pituitary–adrenal axis is altered by aging and exposure to social stress in female rhesus monkeys. Journal of Clinical Endocrinology and Metabolism, 85, 2556–2563.Google ScholarPubMed
Hof, P. R., & Morrison, J. H. (2004). The aging brain: Morphomolecular senescence of cortical circuits. Trends in Neurosciences, 27, 607–613.CrossRefGoogle ScholarPubMed
Hoffman, C. L., Ayala, J. E., Mas-Rivera, A., & Maestripieri, D. (2010). Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free-ranging female rhesus macaques. American Journal of Primatology, 72, 559–565.Google Scholar
Hoffman, C. L., Higham, J. P., Heistermann, M., Coe, C. L., Prendergast, B. J., & Maestripieri, D. (2011). Immune function and HPA axis activity in free-ranging rhesus macaques. Physiology & Behavior, 104, 507–514.CrossRefGoogle ScholarPubMed
Hoffman, C. L., Higham, J. P., Mas-Rivera, A., Ayala, J. E., & Maestripieri, D. (2010). Terminal investment and senescence in rhesus macaques on Cayo Santiago. Behavioral Ecology, 21, 972–978.CrossRefGoogle ScholarPubMed
Hoffman, C. L., Ruiz-Lambides, A. V., Davila, E., Maldonado, E., Gerald, M. S., & Maestripieri, D. (2008). Sex differences in survival costs of reproduction in a promiscuous primate. Behavioral Ecology and Sociobiology, 62, 1711–1718.CrossRefGoogle Scholar
Holmen, K., & Furukawa, H. (2002). Loneliness, health and social network among elderly people—A follow-up study. Archives of Gerontology and Geriatrics, 35, 261–274.CrossRefGoogle ScholarPubMed
Johnson, R. L., & Kapsalis, E. (1995). Ageing, infecundity, and reproductive senescence in free-ranging female rhesus monkeys. Journal of Reproduction and Fertility, 105, 271–278.Google Scholar
Juster, R. P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience and Biobehavioral Reviews, 35, 2–16.Google Scholar
Kaplan, J. R., Manuck, S. B., Anthony, M. S., & Clarkson, T. B. (2002). Premenopausal social status and hormone exposure predict postmenopausal atherosclerosis in female monkeys. Obstetrics & Gynecology, 99, 381–388.Google ScholarPubMed
Kaufman, D., Smith, E. L. P., Gohil, B. C., Banerji, M. A., Coplan, J. D., Kral, J. G., et al. (2005). Early appearance of the metabolic syndrome in socially reared bonnet macaques. Journal of Clinical Endocrinology and Metabolism, 90, 404–408.Google Scholar
Kessler, M. J., & Rawlins, R. G. (1983). Age- and pregnancy-related changes in serum total cholesterol and trygliceride levels in the Cayo Santiago rhesus macaques. Experimental Gerontology, 18, 1–14.CrossRefGoogle Scholar
Kiecolt-Glaser, J. K., Glaser, R., Williger, D., Stout, J., Messick, G., Sheppard, S., et al. (1985). Psychosocial enhancement of immunocompetence in a geriatric population. Health Psychology, 4, 25–41.CrossRefGoogle Scholar
Kotrschal, A., Ilmonen, P., & Penn, D. J. (2007). Stress impacts telomere dynamics. Biology Letters, 3, 128–130.Google Scholar
Laudenslager, M. L., Rasmussen, K. L., Berman, C. M., Lilly, A. A., Shelton, S. E., Kalin, N. H., et al. (1999). A preliminary description of responses of free-ranging rhesus monkeys to brief capture experiences: Behavior, endocrine, immune, and health relationships. Brain, Behavior, and Immunity, 13, 124–137.CrossRefGoogle ScholarPubMed
Lupien, S. J., de Leon, M. J., de Santi, S., Convit, A., Tarshish, C., Nair, N. P. V., et al. (1998). Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience, 1, 69–73.Google Scholar
Maestripieri, D. (1993a). Maternal anxiety in rhesus macaques (Macaca mulatta). I. Measurement of anxiety and identification of anxiety-eliciting situations. Ethology, 95, 19–31.Google Scholar
Maestripieri, D. (1993b). Maternal anxiety in rhesus macaques (Macaca mulatta). II. Emotional bases of individual differences in mothering style. Ethology, 95, 32–42.Google Scholar
Maestripieri, D. (2007). Macachiavellian intelligence: How rhesus macaques and humans have conquered the world. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Maestripieri, D., Hoffman, C. L., Fulks, R., & Gerald, M. S. (2008). Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Hormones and Behavior, 53, 170–176.Google Scholar
McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87, 873–904.Google Scholar
Miller, R. A., Harper, J. M., Dysko, R. C., Durkee, S. J., & Austad, S. N. (2002). Longer life spans and delayed maturation in wild-derived mice. Experimental Biology & Medicine, 227, 500–508.Google Scholar
Mohr, P. N. C., Li, S.-C., & Heekeren, H. R. (2010). Neuroeconomics and aging: Neuromodulation of economic decision making in old age. Neuroscience & Biobehavioral Reviews, 34, 678–688.Google Scholar
Morrison, J. H. (2003). Aging and mammalian cerebral cortex: Monkeys to humans. Alzheimer Disease & Associated Disorders, 17, S51–S53.CrossRefGoogle ScholarPubMed
Morrison, J. H., & Hof, P. R. (2007). Life and death of neurons in the aging cerebral cortex. Neurobiology of Epilepsy and Aging, 81, 41–52.CrossRefGoogle ScholarPubMed
Parker, K. J., Hoffman, C. L., Hyde, S. A., Cummings, C. S., & Maestripieri, D. (2010). Effects of age on cerebrospinal fluid oxytocin levels in free-living adult female and infant rhesus macaques. Behavioral Neuroscience, 124, 428–433.CrossRefGoogle Scholar
Penn, D. J., & Smith, K. R. (2007). Differential fitness costs of reproduction between the sexes. Proceedings of the National Academy of Sciences of the United States of America, 104, 553–558.CrossRefGoogle ScholarPubMed
Radley, J. J., & Morrison, J. H. (2005). Repeated stress and structural plasticity in the brain. Ageing Research Reviews, 4, 271–287.Google Scholar
Rawlins, R. G., & Kessler, M. J. (1985). Climate and seasonal reproduction in the Cayo Santiago macaques. American Journal of Primatology, 9, 87–99.Google Scholar
Rawlins, R. G., & Kessler, M. J. (Eds.). (1986). The Cayo Santiago macaques: History, behavior, and biology. Albany: SUNY Press.Google Scholar
Roth, G. S., Mattison, J. A., Ottinger, M. A., Chahich, M. E., Lane, M. A., & Ingram, D. K. (2004). Aging in rhesus monkeys: Relevance to human health interventions. Science, 305, 1423–1426.Google Scholar
Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308, 648–652.CrossRefGoogle ScholarPubMed
Sapolsky, R. M., Krey, L., & McEwen, B. S. (1986). The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis. Endocrine Reviews, 7, 284–301.Google Scholar
Sapolsky, R. M., Uno, H., Rebert, C. S., & Finch, C. E. (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. Journal of Neuroscience, 10, 2897–2902.Google Scholar
Schwartz, S. M., Kemnitz, J. W., & Howard, C. F. (1993). Obesity in free-ranging rhesus macaques. International Journal of Obesity and Related Metabolic Disorders, 17, 1–9.Google Scholar
Seeman, T. E. (2000). Health promoting effects of friends and family on health outcomes in older adults. American Journal of Health Promotion, 14, 362–370.CrossRefGoogle ScholarPubMed
Shelton, S. E., Kalin, N. H., Gluck, J. P., Keresztury, M. F., Schneider, V. A., & Lewis, M. H. (1988). Effect of age on cisternal cerebrospinal fluid concentrations of monoamine metabolites in nonhuman primates. Neurochemistry International, 13, 353–357.Google Scholar
Smucny, D. A., Allison, D. B., Ingram, D. K., Roth, G. S., Kemnitz, J. W., Kohama, S. G., et al. (2001). Changes in blood chemistry and hematology variables during aging in captive rhesus macaques (Macaca mulatta). Journal of Medical Primatology, 30, 161–173.Google Scholar
Smucny, D. A., Allison, D. B., Ingram, D. K., Roth, G. S., Kemnitz, J. W., Kohama, S. G., et al. (2004). Update: Changes in blood chemistry and hematology variables during aging in captive rhesus macaques (Macaca mulatta). Journal of Medical Primatology, 33, 48–54.Google Scholar
Tyrka, A. R., Price, L. H., Kao, H. T., Porton, B., Marsella, S. A., & Carpenter, L. L. (2010). Childhood maltreatment and telomere shortening: Preliminary support for an effect of early stress on cellular aging. Biological Psychiatry, 67, 531–534.CrossRefGoogle ScholarPubMed
Uno, H., Tarara, R., Else, J. G., Suleman, M. A., & Sapolsky, R. M. (1989). Hippocampal damage associated with prolonged and fatal stress in primates. Journal of Neuroscience, 9, 1705–1711.CrossRefGoogle ScholarPubMed
Veenema, H. C., Spruijt, B. M., Gispen, W. H., & van Hooff, J. A. R. A. M. (1997). Aging, dominance history, and social behavior in Java-monkeys (Macaca fascicularis). Neurobiology of Aging, 18, 509–515.Google Scholar
Veenema, H. C., van Hooff, J. A. R. A. M., Gispen, W. H., & Spruijt, B. M. (2001). Increased rigidity with age in social behavior of Java-monkeys (Macaca fascicularis). Neurobiology of Aging, 22, 273–281.Google Scholar
Volkow, N. D., Gur, R. C., Wang, G.-J., Fowler, J. S., Moberg, P. J., Ding, Y-S., et al. (1998). Association between decline in brain dopamine activity with age and cognitive and motor impairment in healthy individuals. American Journal of Psychiatry, 155, 344–349.Google Scholar
Von Zglinicki, T. (2002). Oxidative stress shortens telomeres. Trends in Biochemical Sciences, 27, 339–344.Google Scholar
Wright, C. E., & Steptoe, A. (2005). Subjective socioeconomic position, gender and cortisol responses to waking in an elderly population. Psychoneuroendocrinology, 30, 582–590.Google Scholar