Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflavone soy diet

Human Reproduction

Volumn 25, Issue 12, 2010, Pages 3083-3094

  Kaplan, J R ^a   Chen, H ^a   Appt, S E ^a   Lees, C J ^a   Franke, A A ^b   Berga, S L ^c   Wilson, M E ^d   Manuck, S B ^e   Clarkson, T B ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HAWAII CANCER CENTER   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d EMORY UNIVERSITY   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

diet; functional hypothalamic anovulatory syndrome; reproduction; stress

Indexed keywords

ESTRADIOL; HYDROCORTISONE; ISOFLAVONE; PROGESTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; BODY WEIGHT; CONTROLLED STUDY; DIETARY INTAKE; EXPERIMENTAL MONKEY; FEMALE; MENSTRUAL CYCLE; MENTAL STRESS; NONHUMAN; OSTEOPENIA; OUTCOME ASSESSMENT; OVARY DISEASE; OVARY FUNCTION; PREMENOPAUSE; SOCIAL STATUS;

ANIMALIA; MACACA FASCICULARIS;

EID: 78649515673     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deq288     Document Type: Article

References (83)

1. Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr et al. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 2003; 43:67-82.
2. Adams MR, Kaplan JR, Koritnik DR. Psychosocial influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiol Behav 1985;35:935-940.
3. Adlercreutz H, Mazur W. Phyto-oestrogens and Western diseases. Ann Med 1997;29:95-120.
4. Bachrach LK. Acquisition of optimal bone mass in childhood and adolescence. Trends Endocrinol Metab 2001;12:2228.
5. Bairey-Merz CN, Johnson BD, Sharaf BL, Bittner V, Berga SL, Braunstein GD, Hodgson KT, Matthews KA, Pepine CJ, Ries SE et al. Hypoestrogenemia of hypothalamic origin and coronary artery disease in premenopausal women: a report from the NHLBI-sponsored WISE study. J Am Coll Cardiol 2003;41:413-419.
6. Beaglehole R. International trends in coronary heart disease mortality, morbidity, and risk factors. Epidemiol Rev 1990;12:11-15.
7. Berga SL. Functional hypothalamic chronic anovulation. In: Adashi EY, Rock JA, Rosenwaks Z (eds). Reproductive Endocrinology, Surgery, and Technology, Vol 1. Philadelphia: Lippencott Raven, 1996,1061-1075.
8. Berga SL, Yen SSC. Reproductive failure due to central nervous system-hypothalamic-pituitary dysfunction. In: Strauss JF, Barbieri RL (eds). Reproductive Endocrinology. Physiology, Pathophysiology, and Clinical Management, 5th edn. Philadelphia: Elsevier Saunders, 2004, 537-632.
9. Berga SL, Mortola JF, Girton L, Suh B, Laughlin G, Pham P, Yen SS. Neuroendocrine aberrations in women with functional hypothalamic amenorrhea. J Clin Endocrinol Metab 1989;68:301-308.
10. Berga SL, Marcus MD, Loucks TL, Hlastala S, Ringham R, Krohn MA. Recovery of ovarian activity of women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil Steril 2003;80:976-981.
11. Bernstein IS. Dominance: the baby and the bathwater. Behav Brain Sci 1981;4:419-457.
12. Breen KM, Karsch FJ. New insights regarding glucocorticoids, stress and gonadotropins suppression. Front Neuroendocrinol 2006;27:233-245.
13. Cameron JL. Stress and behaviorally induced reproductive dysfunction in primates. Semin Reprod Endocrinol 1997;15:37-45.
14. Cassidy A, Bingham S, Setchell KDR. Biological effects of a diet of soy protein rich in isoflavones on the menstrual cycle of premenopausal women. Am J Clin Nutr 1994;60:333-340.
15. Chrousos GP, Torpy DJ, Gold PW. Interactions between the hypothalamic-pituitary-adrenal axis and the female reproductive system: clinical implications. Ann Intern Med 1998;129:229-240.
16. Cline JM, Wood CE. Estrogen/isoflavone interactions in cynomolgus macaques (Macaca fascicularis). Am J Primatol 2009;71:722-731.
17. Conover WJ, Iman RL. Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 1981;35:124-129.
18. Craig WJ, Mangels AR. Position of the American Dietetic Association: vegetarian diets; American Dietetic Association. J Am Diet Assoc 2009; 109:1266-1282.
19. Dall TM, Fulgoni VL 3rd, Zhang Y, Reimers KJ, Packard PT, Astwood JD. Potential health benefits and medical cost savings from calorie, sodium, and saturated fat reductions in the American diet. Am J Health Promot 2009;23:412-422.
20. De Souza MJ, Van Heest J, Demers LM, Lasley BL. Luteal phase deficiency in recreational runners: Evidence for a hypometabolic state. J Clin Endocrinol Metab 2003;88:337-346.
21. Dittus WPJ. The social regulation of population density and age-sex distribution in the toque monkey. Behaviour 1977;63:281-322.
22. Dittus WPJ. The social regulation of primate populations: a synthesis. In: Lindburg DG (ed). The Macaques: Studies in Ecology, Behavior and Evolution, New York: Nostrand Reinhold Co., 1980,263-283.
23. Drew FL. Epidemiology: the epidemiology of secondary amenorrhea. J Chron Dis 1961;14:396-407.
24. Duncan AM, Merz BE, Xu X, Nagel TC, Phipps WR, Kurzer MS. Soy isoflavones exert modest hormonal effects in premenopausal women. J Clin Endocrinol Metab 1998;84:192-197.
25. Ferin M. Clinical Review 105: stress and the reproductive cycle. J Clin Endocrinol Metab 1999;84:1768-1774.
26. Franke AA, Custer LJ, Wilkens LR, Le Marchand LL, Nomura AM, Goodman MT, Kolonel LN. Liquid chromatographic-photodiode array mass spectrometric analysis of dietary phytoestrogens from human urine and blood. J Chromatogr B Analyt Technol Biomed Life Sci 2002; 777:45-59.
27. Gallagher JC. Effect of early menopause on bone mineral density and fractures. Menopause 2007;14(3 Pt 2):567-571.
28. Ginsburg KA. Luteal phase defect: etiology, diagnosis, and management. Endocrinol Metab Clin N Am 1992;21:85-104.
29. Hanke H, Hanke S, Ickrath O, Lange K, Bruck B, Mück AO, Seeger H, Zwirner M, Voisard R, Haasis R et al. Estradiol concentrations in premenopausal women with coronary heart disease. Coron Artery Dis 1997;8:511-515.
30. Harcourt AH. Dominance and fertility among female primates. Zool Soc Lond 1987;213:471-487.
31. Hooper L, Ryder JJ, Kurzer MS, Lampe JW, Messina MJ, Phipps WR, Cassidy A. Effects of soy protein and isoflavones on circulating hormone concentrations in pre- and post-menopausal women: a systematic review and meta-analysis. Hum Reprod Update 2009; 15:423-440.
32. Jakes RW, Alexander L, Duffy SW, Leong J, Chen LH, Lee WH. Dietary intake of soybean protein and menstrual cycle length in pre-menopausal Singapore Chinese women. Public Health Nutr 2001; 4:191-196.
33. Jayo MJ, Rankin SE, Weaver DS, Carlson CS, Clarkson TB. Accuracy and precision of lumbar bone mineral content by dual-energy X-ray absorptiometry in live female monkeys. Calcif Tissue Int 1991; 49:438-440.
34. Jones GES. Some newer aspects of the management of infertility. J Am Med Assoc 1949;141:1123-1129.
35. Kaplan JR, Manuck SB. Status, stress, and atherosclerosis: the role of environment and individual behavior. Ann N Y Acad Sci 1998; 896:145-161.
36. Kaplan JR, Manuck SB. Ovarian dysfunction, stress, and disease: a primate continuum. ILAR J 2004;45:89-115.
37. Kaplan JR, Manuck SB. Ovarian dysfunction and the premenopausal origins of coronary heart disease. Menopause 2008;15:768-776.
38. Kaplan JR, Adams MR, Koritnik DR, Rose JC, Manuck SB. Adrenal responsiveness and social status in intact and ovariectomized Macaca fascicularis. Am J Primatol 1986;11:181-193.
39. Kaplan JR, Adams MR, Anthony MS, Morgan TM, Manuck SB, Clarkson TB. Dominant social status and contraceptive hormone treatment inhibit atherogenesis in premenopausal monkeys. Arterioscler Thromb Vasc Biol 1995;15:2094-2100.
40. Kaplan JR, Chen H, Manuck SB. The relationship between social status and atherosclerosis in male and female monkeys as revealed by meta-analysis. Am J Primatol 2009;71:732-741.
41. Kaplan JR, Manuck SB, Anthony MS, Clarkson TB. Premenopausal social status and hormone exposure predict postmenopausal atherosclerosis in female monkeys. Obstet Gynecol 2002a;99:381-388.
42. Kaplan JR, Manuck SB, Fontenot MB, Mann JJ. Central nervous system monoamine correlates of social dominance in cynomolgus monkeys (Macaca fascicularis). Neuropsychopharmacology 2002b; 26:431-443.
43. Knobil E. The neuroendocrine control of ovulation. Hum Reprod 1988; 3:469-472.
44. Kurzer MS. Hormonal effects of soy in premenopausal women and men. J Nutr 2002;132:570S-573S.
45. Lawson EA, Donoho D, Miller KK, Misra M, Meenaghan E, Lydecker J, Wexler T, Herzog DB, Klibanksi A. Hypercortisolemia is associated with severity of bone loss and depression in hypothalamic amenorrhea and anorexia nervosa. J Clin Endocrinol Metab 2009; 94:4710-4716.
46. Lees CJ, Register TC, Turner CH, Wang T, Stancill M, Jerome CP. Effects of raloxifene on bone density, biomarkers, and histomorphometric and biomechanical measures in ovariectomized cynomolgus monkeys. Menopause 2002;9:320-328.
47. Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003;88:297-311.
48. Lu L-JW, Anderson KE, Grady JJ, Nagamani M. Effects of Soya consumption for one month on steroid hormones in premenopausal women: implications for breast cancer risk reduction. Cancer Epidemiol Biomarkers Prev 1996;5:63-70.
49. Maskarinec G, Franke AA, Williams AE, Hebshi S, Oshiro C, Murphy S, Stanczyk FZ. Effects of a 2-year randomized soy intervention on sex hormone levels in premenopausal women. Cancer Epidemiol Biomarkers Prev 2004;13(11 Pt1):1739-1744.
50. Merz CN, Johnson BD, Berga S, Braunstein G, Reis SE, Bittner V; WISE Study Group. Past oral contraceptive use and angiographic coronary artery disease in postmenopausal women: data from the National Heart, Lung, and Blood Institute-sponsored Women's Ischemia Syndrome Evaluation. Fertil Steril 2006;85:1425-1431.
51. Michopoulos V, Berga SL, Kaplan JR, Wilson ME. Social subordination and polymorphisms in the gene encoding the serotonin transporter enhance estradiol inhibition of luteinizing hormone secretion in female rhesus monkeys. Biol Reprod 2009;81:1154-1163.
52. Miksicek RJ. Interaction of naturally occurring nonsteroidal estrogens with expressed recombinant human estrogen receptor. J Steroid Biochem Mol Biol 1994;49:153-160.
53. Misra M, Klibanski A. Anorexia nervosa and osteoporosis. Rev Endocr Metab Disord 2006;7:91-99.
54. Nagata C, Kabuto M, Kurisu Y, Shimizu H. Decreased serum estradiol concentration associated with high dietary intake of soy products in premenopausal Japanese women. Nutr Cancer 1997;29:228-233.
55. Newton TL, Philhower CL. Socioemotional correlates of self-reported menstrual cycle irregularity in premenopausal women. Psychosom Med 2003;65:1065-1069.
56. Parkin DM, Muir CS, Whelan SL, Gao YT, Ferlay J, Powell J (eds) Cancer Incidence in Five Continents, Vol VI, IARC Scientific Publication no. 120. Lyon: International Agency for Research on Cancer, 1992,145-173.
57. Pazol K, Kaplan JR, Abbott D, Appt SE, Wilson ME. Practical measurement of total and bioavailable estradiol in female macaques. Clin Chim Acta 2004;340:117-126.
58. Reifenstein EC Jr Psychogenic or 'hypothalamic' amenorrhea. Med Clin North Am 1946;30:110-1114.
59. Ripley HS, Papanicolaou GN. The menstrual cycle with vaginal smear studies in schizophrenia, depression, and elation. Am J Psychiatry 1942; 98:567-574.
60. Rocca WA, Grossardt BR, Andrade de M, Malkasian GD, Melton LJ. Survival patterns after oophorectomy in premenopausal women: a population-based cohort study. Lancet Oncol 2006;7:821-828.
61. Rocca WA, Bower JH, Maraganore DM, Ahlskog JE, Grossardt BR, de Andrade M, Melton LJ. Increased risk of cognitive impairment or dementia in women who underwent oophorectomy before menopause. Neurology 2007;69:1074-1073.
62. Sade DS. An ethogram for Rhesus monkeys. I. Antithetical contrasts in posture and movement. Am J Phys Anthropol 1973;38:534-542.
63. Sade DS, Cushing K, Cushing P, Dunaif J, Figueroa A, Kaplan JR, Lauer C, Rhodes D, Schneider J. Population dynamics in relation to social structure on Cayo Santiago. Yearbook Phys Anthropol 1976;20:253-262.
64. Shively CA, Clarkson TB. Social status and coronary artery atherosclerosis in female monkeys. Arterioscler Thromb 1994;14:721-726.
65. Silk JB. Practice random acts of aggression and senseless acts of intimidation: the logic of status contests in social groups. Evol Anthropol 2002;11:221-225.
66. Snell-Bergeon JK, Dabelea D, Ogden LG, Hokanson JE, Kinney GL, Ehrlich J, Rewers M. Reproductive history and hormonal birth control use are associated with coronary calcium progression in women with type 1 diabetes mellitus. J Clin Endocrinol Metab 2008;93:2142-2148.
67. Sowers M, Crutchfield M, Bandekar R, Randolph JF, Shapiro B, Schork MA, Jannausch M. Bone mineral density and its change in pre-and perimenopausal white women: the Michigan Bone Health Study. J Bone Miner Res 1998;13:1134-1140.
68. Speroff L. Gonads are the heart of the matter. Menopause 2007; 14:342-344.
69. Stute P, Wood CE, Kaplan JR, Cline JM. Cyclic changes in the mammary gland of cynomolgus macaques. Fertil Steril 2004;82(Suppl 3): 1160-1170.
70. Ursin G, Bernstein L, Pike MC. Breast cancer. In: Doll R, Fraumeni JF, Muir CS (eds). Trends in Cancer Incidence and Mortality, vol 19/20. Plainview, NY: Cold Spring Harbor Laboratory Press, 1994, 241-264.
71. Vitolins MZ, Anthony MS, Burke GL. Phytoestrogens and Health, 1st edn, Champaign, IL: AOCS Press, 2002, 260.
72. Walker SE, Register TC, Appt SE, Adams M, Clarkson TB, Chen H, Isom S, Franke AA, Kaplan JR. Plasma lipid-dependent and -independent effects of dietary soy protein and social status on atherogenesis in premenopausal monkeys: implications for postmenopausal atherosclerosis burden. Menopause 2008;15:950-957.
73. Wang TT, Sathyamoorthy N, Phang JM. Molecular effects of genistein on estrogen receptor mediated pathways. Carcinogenesis 1996;17:271-275.
74. Wilks JW, Hodgen GD, Ross GT. Luteal phase defects in the rhesus monkey: The significance of serum FSH:LH ratios. J Clin Endocrinol Metab 1976;43:1261-1267.
75. Williams RF, Hodgen GD. The reproductive cycle in female macaques. Am J Primatol 1982;3(Suppl 1):181-192.
76. Williams NI, Berga SL, Cameron JL. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am J Physiol Endocrinol Metab 2007;293:E270-E276.
77. Wilson ME. Premature elevation in serum insulin-like growth factor-I advances first ovulation in rhesus monkeys. J Endocrinol 1998; 158:247-257.
78. Wilson ME, Pazol K, Legendre A, Fisher J, Chikazawa K. Gonadal steroid modulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis is influenced by social status in female rhesus monkeys. Endocrine 2005; 26:89-97.
79. Wood CE, Kaplan JR, Stute P, Cline JM. Effects of soy on the mammary glands of premenopausal female monkeys. Fertil Steril 2006;85(Suppl 1):1179-1186.
80. Wu AH, Stanczyk FZ, Hendrich S, Murphy PA, Zhang C, Wan P, Pike MC. Effects of soy foods on ovarian function in premenopausal women. Br J Cancer 2000;82:1879-1886.
81. Xiao E, Xia-Zhang L, Ferin M. Inadequate luteal function is the initial clinical cyclic defect in a 12-day stress model that includes a psychogenic component in the rhesus monkey. J Clin Endocrinol Metab 2002;87:2232-2237.
82. Zuckerman S. The menstrual cycle of the primates. I. General nature and homology. Proc Zool Soc Lond 1930;100:691-754.
83. Zuckerman S, Parks MA. The menstrual cycle of primates. V. The cycle of the baboon. Proc Zool Soc Lond 1932;102:138-191.