Abstract
During the past 15 years, our aging colony of rhesus monkeys, consisting of animals from 20 to 37 years of age, had an annual average population of 88.2 live monkeys and, of this population, an annual average of 13.9 monkeys died spontaneously or were terminated due to severe illness. From 1980 to 1994, a total of 175 autopsies of rhesus macaques, from 20 to 37 years of age, were performed. By cumulative autopsy data, the incidence of age-related pathology in various organs was surveyed. Major geriatric diseases such as coronary sclerosis, emphysema, degenerative joint disorders, cancer, and cerebral amyloid plaque began to develop in 10 to 40% of macaques after 20 years and the incidence significantly increased after 26 years of age. Approximately 12% of aged macaques from 20 to 30 years of age died annually due to such geriatric diseases with severe complications. The average survival rate indicated that half the population at 20 years of age died by 25 years and 73% died by 30 years of age. Less than 10% of macaques survived over 30 years. Using these aged macaques as well as other juvenile to adult monkeys in our Center, clinical opththalmological and reproductive endocrinological studies, and magnetic resonance imaging (MRI) of the brain were conducted to define bioaging markers of captive rhesus monkeys. Cataracts began to develop in 20% of rhesus monkeys at 20 to 22 years of age and the rate significantly increased after 26 years of age. Menopause occurred at 26 to 27 years of age. Multiple cerebral infarctions and iron deposits in the globus pallidus and substantia nigra were detected by MRI in the aged brains. These geriatric disorders in captive aged macaques appear to be natural aging outcomes, since the simple lifestyle of these captive animals offers minimal exposure to environmental factors. Our data will offer useful paradigms for preventive or experimental studies on age-related diseases.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Angelini, L., Nardocci, N., Rumi, V., Zorzi, C., Strada, L., and Savoiardo, M.: Hallervorden-Spatz disease: Clinical and MRI study of 11 cases diagnosed in life. J. Neurol., 239: 417–425, 1992.
Beniashvili, DS.: An overview of the world literature on spontaneous tumors in nonhuman primates. J. Med. Primatol., 18: 423–437, 1989.
Bowden, D.M., and Jones, M.L.: Aging research in nonhuman primates, in Aging in Nonhuman Primates, edited by Bowden, D.M., New York, Van Nostrand Reinhold Co., 1979, pp. 1–13.
Brock, D.B., Guralnik, J.M., and Brody, J.A.: Demography and epidemiology of aging in the United States, in Handbook of the Biology of Aging, edited by Schneider, E.L., and Rowe, J.W., third edition, San Diego, Academic Press, Inc., 1990, pp. 3–23.
Brody, J.A., Brock, D.B., and Williams, T.F.: Trends in the health of the elderly population, in Annual Review of Public Health, Vol. 8, 1987, pp. 211–234.
Bronson, R.T., and Schoene, E.C.: Spontaneous pallidonigral accumulation of iron pigment and spheroid-like structures in macaque monkeys. J. Neuropathol. Exp. Neurol., 39: 181–196, 1980.
Cancer Facts & Figures — 1996, American Cancer Society, Inc., Atlanta, GA.
Clapp, N.K., and Storer, J.B.: Death rates with age from all causes and from colonic carcinoma in wild-caught and colony-born cotton-top tamarins. Chapter 15 in A Primate Model for the Study of Colitis and Colonic Carcinoma, edited by Clapp, N.K., CRC Press, Boca Raton, 1993, pp. 221–230.
Clarkson, T.B., Weingand, K.W., Kaplan, J.R., and Adams, M.R.: Mechanisms of atherogenesis. Circulation, 76(Suppl. I): I20–I28, 1987.
Collins, K., Uno, H., and Dierschke, D.J.: Ovarian follicle populations in peri-and post-menopausal rhesus monkeys. Fed. Proc., 42: 316, 1983.
Cork, L.C., Masters, C., Beyreuther, K., and Price, D.L.: Development of senile plaques. Relationships of neuronal abnormalities and amyloid deposits. Am. J. Pathol., 137: 1383–1392, 1990.
Cork, L.C., and Walker, L.C.: Age-related lesions, nervous system. In Nonhuman PrimatesII, edited by Jones, T.C., Mohr, U., and Hunt, R.D., New York, Springer-Verlag, pp. 173–183.
Cutler, R.G.: Evolution of longevity in primates. J. Human Evolution, 5: 169–202, 1976.
Cutler, R.G.: Evolutionary biology of senescence, in The Biology of Aging, edited by Behnke, J.A., Finch, C.E., and Moment, G.B., New York, Plenum Press, 1978, pp. 311–360.
Davidson, J., Ross, R.K., Paganini-Hill, A., Hammond, C.D., Siiteri, P.K., and Judd, H.L.: Total and free estrogen and androgens in postmenopausal women with hip fractures. J. Clin. Endocrinol. Metab., 54: 115–120, 1982.
DeRousseau, C.J.: Aging in the musculoskeletal system of rhesus monkeys: II. Degenerative joint disease. Amer. J. Phys. Anthrop., 67: 1771–1784, 1985.
DeRousseau, C.J., Bito, L.Z., and Kaufman, P.L.: Age-dependent impairments of the rhesus monkey visual and musculoskeletal systems and apparent biohavioral consequences, in The Cayo Santiago Macaques: History, Behavior and Biology, edited by Rawlins, R.G., and Kessler, M.J., Albany, SUNY Press, 1986, pp. 233–251.
Engle, E.T., and Stout, A.P.: Spontaneous primary carcinoma of the prostate in a monkey (Macaca mulatta). Am. J. Cancer, 39: 334–337, 1940.
Finch, C.E.: Longevity, senescence, and the genome. Chicago, The University of Chicago Press, 1990, p. 163.
Giddens, E.W., and Dillingham, L.A.: Primary tumors of the lung in nonhuman primates. Veterinary Pathol., 8: 467–471, 1971.
Gliatto, J.M., and Bronson, R.T.: Spontaneous pallidonigral spheroids and iron pigment accumulation, macaques, in Nonhuman Primates II, edited by Jones, T.C., Mohr, U., and Hunt, R.D., New York, Springer-Verlag, 1993, pp. 183–187.
Heaney, R.P., Recker, R.R., and Saville, P.D.: Menopausal changes in calcium balance performance. Nutrition Rev., 41: 86–89, 1983.
Hodgen, G.D., Goodman, A.L., O’Connor, A., and Johnson, D.K.: Menopause in rhesus monkeys: Model for study of disorders in the human climacteric. Am. J. Obstet. Gynecol., 127: 581–584, 1977.
Iwata, T.: Studies on senile changes in the brains in monkeys (Macaca fuscata). I. On senile plaque. Acta Sch. Med. Univ. Gifu, 34: 540–550, 1986.
Kaufman, P.L., and Bito, L.Z.: The occurrence of senile cataracts, ocular hypertension and glaucoma in rhesus monkeys. Exp. Eye Res., 34: 287–291, 1982.
Kaufman, P.L., Bito, L.Z., and DeRousseau, C.J.: The development of presbyopia in primates. Trans. Ophthal. Soc. U.K., 102: 323–326, 1983.
King, N.W., Johnson, L.D., and Sehgal, P.K.: The prevalence of idiopathic colitis in the New England Regional Primate Research Center cotton-top tamarin (Saguinus Oedipus) colony, Chapter 5 in A Primate Model for the Study of Colitis and Colonic Carcinoma, edited by Clapp, N.K., CRC Press, Boca Raton, 1993, pp. 101–112.
Lapin, B.A.: Use of nonhuman primates in cancer research. J. Med. Primatol., 11: 327–341, 1982.
Lapin, B.A., Krilova, R.I., Cherkovich, G.M., and Asanov, N.S.: Observations from Sukhumi, Chapter 2 in Aging in Nonhuman Primates, edited by Bowden, D.M., New York, Van Nostrand Reinhold Co., 1979, pp. 14–37.
McClure, H.M.: Neoplastic diseases in nonhuman primates: Literature review and observations in an autopsy series of 2,176 animals, in The Comparative Pathology of Zoo Animals, edited by Montal, R.J., and Migaki, G., Washington, D.C., Smithsonian Institution Press. 1980, pp. 549–565.
Morgan, P.M., Hutz, R.J., Kraus, E.M., Cormie, J.A., Dierschke, D.J., and Bavister, B.D.: Evaluation of ultrasonography for monitoring follicular growth in rhesus monkeys. Theriogenol., 27: 769–779, 1987.
Nozaki, M., Mitsunaga, F., and Shimizu, K.: Reproductive senescence in female Japanese monkeys (Macaca fuscata): Age-and season-related changes in hypothalamic-pituitary-ovarian functions and fecundity rates. Biol. Reprod., 52: 1250–1257, 1995.
Porter-Grenn, L., Silbergleit, R., and Mehta, B.A.: Hallervorden-Spatz disease with bilateral involvement of globus pallidus and substantia nigra: MR demonstration. J. Computer Assisted Tomography, 17: 961–963, 1993.
Price, D.L., Cork, L.C., Struble, R.G., Kitt, C.A., Price, D.L. Jr., Lehmann, J., and Hedreen, J.C.: Neuropathological, neurochemical and behavioral studies of the aging nonhuman primate. Chapter 7 in Behavior and Pathology of Aging in Rhesus Monkeys, New York, Alan R. Liss, 1985, pp. 113–135.
Schoene, W.C., Bronson, R.T., Dooling, E.C., Richardson, E.P.: Spontaneous pallido-nigral spheroid pigmentary degeneration in monkeys: An analog of human Hallervorden-spatz disease. J. Neuropathol. Exp. Neurol., 36: 628, 1977.
Struble, R.G., Price, D.L. Jr., Cork, L.C., and Price, D.L.: Senile plaques in cortex of aged normal monkeys. Brain Res., 361: 267–275, 1985.
Timiras, P.S., and Sentenac, J.: Aging of the female reproductive system, Chapter 7 in Hormones and Aging, edited by Timiras, P.S., Quay, W.D., and Vernadakis, A., Boca Raton, CRC Press, 1995, pp. 121–134.
Trussart, V., Leboucq, N., Carlander, B., Billiard, M., and Castan, P.: Hallervorden-Spatz syndrome and MRI: The “tiger’s eye.” One Case. J. Neuroradiol., 20: 70–75, 1993.
Uno, H., Alsum, P.B., Dong, S., Richardson, R., Zimbric, M., Thieme, C.S., and Houser, W.D.: Cerebral amyloid angiopathy and plaques and visceral amyloidosis of aged macaques. Neurobiol. Aging, 17: 275–281, 1996.
Uno, H., Houser, W.D., and Holden, J.E.: Magnetic resonance images of the cerebral infarction of an aged rhesus macaque: Comparison between T1 and T2 images and neuropathology. Neurosci. Abst., 16(2) 1160, 1990.
Uno, H., Kao, Y., Baker, E., Shelton, S., and Holden, J.: MRI study of multiple infarctions and iron deposits in the globus pallidus in aged rhesus monkeys. Neurosci. Abst., 20-I: 180, 1994.
Uno, H., and Poff, B.: Coronary arterial ectasia, a predominant type of coronary sclerosis in aged captive rhesus monkeys (Macaca mulatta). Am. J. Path., 111: 315–322, 1983.
Uno, H., and Walker, L.C.: The age of biosenescence and the incidence of cerebral b-amyloidosis in aged captive rhesus monkeys. Ann. N.Y. Acad. Sci., 695: 232–235, 1993.
Van Wagenen, G., and Simpson, M.E.: Embryology of the ovary and testis. Homo sapiens and Macaca mulatta. New Haven, Yale Univ. Press, 1965.
Walker, L.C., Masters, C., Beyreuther, K., and Price, D.L.: Amyloid in the brains of aged squirrel monkeys. Acta Neuropathol., 80: 381–387, 1990.
Walker, M.L.: Menopause in female rhesus monkeys. Am. J. Primatol., 35: 59–71, 1995.
Weindruch, R., Kemnitz, J.W., and Uno, H.: Interspecies variations in physiologic and antipathologic outcomes of dietary restriction, in Dietary Restriction: Implications for the Design and Interpretation of Toxicity and Carcinogenicity Studies, edited by Hart, R.W., Neumann, D.A., and Robertson, R.T., Washington, D.C., ILSI Press, 1995, pp. 351–364.
Winston, L.A., Dierschke, D.J., and Robinson, J.A.: Gonadotropins rise before estrogen declines in rhesus monkeys prior to menopause. Endocrine Soc. Absts., 1987, No. 873.
Wisniewski, H.M., Ghetti, B., and Terry, R.D.: Neuritic (senile) plaques and filamentous changes in aged rhesus monkeys. JNEN, 32: 566–584, 1973.
Wissler, R.W., and Vesselinovitch, D.: Differences between human and animal atherosclerosis, in Atherosclerosis III, edited by Schettler, G., and Weigel, A., New York, Springer, 1973, pp. 319–325.
Author information
Authors and Affiliations
About this article
Cite this article
Uno, H. Age-related pathology and biosenescent markers in captive rhesus macaques. AGE 20, 1–13 (1997). https://doi.org/10.1007/s11357-997-0001-5
Issue Date:
DOI: https://doi.org/10.1007/s11357-997-0001-5