The effects of a long-term psychosocial stress on reproductive indicators in the baboon

American Journal of Physical Anthropology

Volumn 145, Issue 4, 2011, Pages 629-638

  O'Connor, Kathleen A ^a   Brindle, Eleanor ^a   Shofer, Jane ^a   Trumble, Benjamin C ^a   Aranda, Jennifer D ^a   Rice, Karen ^b   Tatar, Marc ^c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

cortisol; FSH; ovarian steroids; reproductive ecology; tumescence

Indexed keywords

ESTROGEN; ESTRONE; FOLLITROPIN; HYDROCORTISONE; PREGNANEDIOL; PREGNANEDIOL 3 GLUCURONIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOVULATION; ARTICLE; BABOON; CONTROLLED STUDY; FEMALE; HORMONE DETERMINATION; HORMONE URINE LEVEL; HYDROCORTISONE URINE LEVEL; HYPOTHALAMUS FUNCTION; LONG TERM EXPOSURE; LUTEAL PHASE; MENSTRUAL CYCLE; MENSTRUATION; MENTAL STRESS; NONHUMAN; OVULATION; REPRODUCTIVE FITNESS; SOCIAL ADAPTATION; SOCIAL ISOLATION; URINALYSIS;

ANIMALS; AREA UNDER CURVE; BIOLOGICAL MARKERS; ESTRONE; FEMALE; FOLLICLE STIMULATING HORMONE; HYDROCORTISONE; MENSTRUAL CYCLE; OVULATION; PAPIO; PREGNANEDIOL; REPRODUCTION; STRESS, PSYCHOLOGICAL;

EID: 79960181126     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21538     Document Type: Article

References (65)

1. Baird DD, Weinberg CR, Zhou H, Kamel F, McConnaughey DR, Kesner JS, Wilcox AJ,. 1999. Preimplantation urinary hormone profiles and the probability of conception in healthy women. Fertil Steril 71: 40-49. (Pubitemid 29042341)
2. Bercovitch FB, and, Goy RW,. 1990. The socioendocrinology of reproductive development and reproductive success in macaques. In:, Ziegler TE, Bercovitch FB, editors. Socioendocrinology of primate reproduction. New York: Wiley-Liss. p 59-93.
3. Berkman LF, Syme SL,. 1979. Social networks, host resistance, and mortality: a nine-year follow-up study of Alameda County residents. Am J Epidemiol 109: 186-204. (Pubitemid 10201150)
4. Bethea CL, Pau FK, Fox S, Hess DL, Berga SL, Cameron JL,. 2005. Sensitivity to stress-induced reproductive dysfunction linked to activity of the serotonin system. Fertil Steril 83: 148-155. (Pubitemid 40094794)
5. Brindle E, Miller RC, Shofer JB, Klein NA, Soules MR, O'Connor KA,. 2006. Urinary beta-luteinizing hormone and beta-follicle stimulating hormone immunoenzymometric assays for population research. Clin Biochem 39: 1071-1079. (Pubitemid 44737478)
6. Cameron JL,. 1997. Stress and behaviorally induced reproductive dysfunction in primates. Semin Reprod Endocrinol 15: 37-45. (Pubitemid 27113781)
7. Caperton L, Eddy C, Leland MM, Carey KD, McCarrey JR,. 2006. Alteration of the menstrual cycle in baboons placed on tethering devices and moved to individual housing-a stress model for a follicular phase defect. J Med Primatol 35: 341-345.
8. Chrousos GP, Gold PW,. 1998. A healthy body in a healthy mind-and vice versa-the damaging power of "uncontrollable" stress. J Clin Endocrinol Metab 83: 1842-1845. (Pubitemid 28496303)
9. Dobson H, Smith RF,. 2000. What is stress, and how does it affect reproduction? Anim Reprod Sci 60-61: 743-752. (Pubitemid 30397837)
10. Edozien LC,. 2006. Mind over matter: psychological factors and the menstrual cycle. Curr Opin Obstet Gynecol 18: 452-456. (Pubitemid 43964775)
11. Ellison PT,. 1990. Human ovarian function and reproductive ecology: new hypotheses. Am Anthropol 92: 933-952.
12. Ellison PT,. 1994. Salivary steroids and natural variation in human ovarian function. Ann NY Acad Sci 709: 287-298. (Pubitemid 24123349)
13. Ellison PT,. 2003. Energetics and reproductive effort. Am J Hum Biol 15: 342-351. (Pubitemid 36546296)
14. Ellison PT, Lipson SF, Jasienska G, Ellison PL,. 2007. Moderate anxiety, whether acute or chronic, is not associated with ovarian suppression in healthy, well-nourished. Western women. Am J Phys Anthropol 134: 513-519. (Pubitemid 350155986)
15. Ferin M,. 1999. Clinical review 105: stress and the reproductive cycle. J Clin Endocrinol Metab 84: 1768-1774. (Pubitemid 30646986)
16. Ferin M,. 2006. Stress and the reproductive system. In:, Neill JD, editor. Knobil and Neill's physiology of reproduction. Amsterdam: Elsevier. p 2627-2695.
17. Gard PR,. 1998. Human endocrinology. London; Bristol, PA: Taylor & Francis.
18. Gesquiere LR, Wango EO, Alberts SC, Altmann J,. 2007. Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 51: 114-125. (Pubitemid 44838637)
19. Gillmann J,. 1940. The effect of multiple injections of progesterone on the turgescent perineum of the baboon (Papio porcarius). Endocrinology 26: 1072-1077.
20. Hayashi KT, Moberg GP,. 1990. Influence of the hypothalamic-pituitary- adrenal axis on the menstrual cycle and the pituitary responsiveness to estradiol in the female rhesus monkey (Macaca mulatta). Biol Reprod 42: 260-265. (Pubitemid 20107249)
21. Hendrick AG, and, Dukelow RW,. 1995. Reproductive biology. In:, Bennett BT, Abee CR, Hendrickson R, editors. Nonhuman primates in biomedical research: biology and management. San Diego: Academic Press. p 147-191.
22. Kaplan JR, Manuck SB,. 2004. Ovarian dysfunction, stress, and disease: a primate continuum. ILAR J 45: 89-115.
23. Laudenslager ML, Rasmussen KL, Berman CM, Lilly AA, Shelton SE, Kalin NH, Suomi SJ,. 1999. A preliminary description of responses of free-ranging rhesus monkeys to brief capture experiences: behavior, endocrine, immune, and health relationships. Brain Behav Immun 13: 124-137. (Pubitemid 29419579)
24. Li H, Nakajima ST, Chen J, Todd HE, Overstreet JW, Lasley B,. 2001. Differences in hormonal characteristics of conceptive versus nonconceptive menstrual cycles. Fertil Steril 75: 549-553. (Pubitemid 32175671)
25. Lipson SF, Ellison PT,. 1996. Comparison of salivary steroid profiles in naturally occurring conception and non-conception cycles. Hum Reprod 11: 2090-2096. (Pubitemid 26391993)
26. Maestripieri D, Hoffman CL, Fulks R, Gerald MS,. 2008. Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Horm Behav 53: 170-176. (Pubitemid 350309375)
27. Miller RC, Brindle E, Holman DJ, Shofer JB, Klein NA, Soules MR, O'Connor KA,. 2004. Comparison of specific gravity and creatinine methods for normalizing urinary reproductive hormone concentrations. Clin Chem 50: 924-932. (Pubitemid 38543672)
28. Morrow CJ, Kolver ES, Verkerk GA, Matthews LR,. 2000. Urinary corticosteroids: an indicator of stress in dairy cattle. Proc New Zeal Soc Anim Prod 60: 218-221.
29. Munro C, Stabenfeldt GH,. 1985. Development of a cortisol enzyme-immunoassay in plasma. Clin Chem 31: 956.
30. Nepomnaschy PA, Welch K, McConnell D, Strassmann BI, England BG,. 2004. Stress and female reproductive function: a study of daily variations in cortisol, gonadotrophins, and gonadal steroids in a rural Mayan population. Am J Hum Biol 16: 523-532. (Pubitemid 39199846)
31. Nepomnaschy PA, Welch KB, McConnell DS, Low BS, Strassmann BI, England BG,. 2006. Cortisol levels and very early pregnancy loss in humans. Proc Natl Acad Sci USA 103: 3938-3942. (Pubitemid 43376659)
32. Norman RL, McGlone J, Smith CJ,. 1994. Restraint inhibits luteinizing hormone secretion in the follicular phase of the menstrual cycle in rhesus macaques. Biol Reprod 50: 16-26. (Pubitemid 24006003)
33. O'Connor KA, Brindle E, Holman DJ, Klein NA, Soules MR, Campbell KL, Kohen F, Munro CJ, Shofer JB, Lasley BL, etal. 2003. Urinary estrone conjugate and pregnanediol-3-glucuronide enzymeimmunoassays for population research. Clin Chem 49: 1139-1148. (Pubitemid 36751101)
34. O'Connor KA, Brindle E, Miller RC, Shofer JB, Ferrell RJ, Klein NA, Soules MR, Holman DJ, Mansfield PK, Wood JW,. 2006. Ovulation detection methods for urinary hormones: precision, daily and intermittent sampling, and a combined hierarchical method. Hum Reprod 21: 1442-1452. (Pubitemid 44445020)
35. Pinheiro JC, and, Bates DM,. 2000. Mixed-effects models in S and S-PLUS. New York: Springer.
36. Rodbard D,. 1974. Statistical quality control and routine data processing for radioimmunoassays and immunoradiometric assays. Clin Chem 20: 1255-1270.
37. Rowell T,. 1970. Baboon menstrual cycles affected by social environment. J Reprod Fertil 21: 133-141.
38. Shaikh AA, Celaya CL, Gomez I, Shaikh SA,. 1982. Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates 23: 444-452.
39. Shivapathasundram G, Kwik M, Chapman M,. 2010. Luteal phase defect: part of the infertility zeitgeist or relic from the past? Hum Fertil (Camb) 14: 60-63.
40. Silk JB,. 1987. Social behavior in evolutionary perspective. In:, Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 318-329.
41. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL,. 2009. The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc Biol Sci 276: 3099-3104.
42. Sopelak VM, Lynch A, Williams RF, Hodgen GD,. 1983. Maintenance of ovulatory menstrual cycles in chronically cannulated monkeys: a vest and mobile tether assembly. Biol Reprod 28: 703-706. (Pubitemid 13104998)
43. Sterck EHM, Watts DP, van Schaik CP,. 1997. The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41: 291-309. (Pubitemid 27523423)
44. Stevens VC, Sparks SJ, Powell JE,. 1970. Levels of estrogens, progestogens and luteinizing hormone during the menstrual cycle of the baboon. Endocrinology 87: 658-666.
45. Stewart DR, Overstreet JW, Nakajima ST, Lasley BL,. 1993. Enhanced ovarian steroid secretion before implantation in early human pregnancy. J Clin Endocrinol Metab 76: 1470-1476. (Pubitemid 23164363)
46. Team RD,. 2007. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
47. Thompson ME, Wrangham RW,. 2008. Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park. Uganda. Am J Phys Anthropol 135: 171-181.
48. Tilbrook AJ, Turner AI, Clarke IJ,. 2002. Stress and reproduction: central mechanisms and sex differences in non-rodent species. Stress 5: 83-100. (Pubitemid 34532747)
49. Todd HE, Shideler SE, Laughlin LS, Overstreet JW, Pohl CR, Byrd W, Lasley BL,. 1999. Application of an enzyme immunoassay for urinary follicle-stimulating hormone to describe the effects of an acute stressor at different stages of the menstrual cycle in female laboratory macaques. Am J Primatol 48: 135-151. (Pubitemid 29216056)
50. Tsigos C, Chrousos GP,. 2002. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53: 865-871. (Pubitemid 35282615)
51. Uchino B,. 2006. Social support and health: a review of physiological processes potentially underlying links to disease outcomes. Behav Med 29: 377-387. (Pubitemid 44134207)
52. Van Vugt DA, Piercy J, Farley AE, Reid RL, Rivest S,. 1997. Luteinizing hormone secretion and corticotropin-releasing factor gene expression in the paraventricular nucleus of rhesus monkeys following cortisol synthesis inhibition. Endocrinology 138: 2249-2258. (Pubitemid 27215222)
53. Venners SA, Liu X, Perry MJ, Korrick SA, Li Z, Yang F, Yang J, Lasley BL, Xu X, Wang X,. 2006. Urinary estrogen and progesterone metabolite concentrations in menstrual cycles of fertile women with non-conception, early pregnancy loss or clinical pregnancy. Hum Reprod 21: 2272-2280. (Pubitemid 44530600)
54. Vitzthum VJ, Spielvogel H, Thornburg J, West B., 2006. A prospective study of early pregnancy loss in humans. Fertil Steril 86: 373-379. (Pubitemid 44118956)
55. Vitzthum VJ, Spielvogel H, Thornburg J, West B,. 2006. A prospective study of early pregnancy loss in humans. Fertil and Steril 86(2): 373-379. (Pubitemid 44118956)
56. Wasser SK,. 1996. Reproductive control in wild baboons measured by fecal steroids. Biol Reprod 55: 393-399. (Pubitemid 26301151)
57. Wasser SK, Barash DP,. 1983. Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q Rev Biol 58: 513-538.
58. Watson SL, Shively CA, Kaplan JR, Line SW,. 1998. Effects of chronic social separation on cardiovascular disease risk factors in female cynomolgus monkeys. Atherosclerosis 137: 259-266. (Pubitemid 28215872)
59. Williams NI, Berga SL, Cameron JL,. 2007. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am J Physiol Endocrinol Metab 293: E270-E276. (Pubitemid 47105941)
60. Xiao E, Xia-Zhang L, Barth A, Zhu J,. 1998. Stress and the menstrual cycle: relevance of cycle quality in the short-and long-term response to a 5-day endotoxin challenge during the follicular phase in the rhesus monkey. J Clin Endocrinol Metab 83: 2454-2460. (Pubitemid 28503047)
61. Xiao E, Xia-Zhang L, Ferin M,. 1999. Stress and the menstual cycle: short-and long-term response to a five-day endotoxin challenge during the luteal phase in the rhesus monkey. J Clin Endocrinol Metab 84: 623-626. (Pubitemid 29075695)
62. Xiao E, Xia-Zhang L, Ferin M,. 2002. 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 87: 2232-2237. (Pubitemid 34521514)
63. Xiao E, Xia-Zhang L, Thornell D, Ferin M,. 1996. Interleukin-1 stimulates luteinizing hormone release during the midfollicular phase in the rhesus monkey: a novel way in which stress may influence the menstrual cycle. J Clin Endocrinol Metab 81: 2136-2141. (Pubitemid 26175938)
64. Xiao E, Xia-Zhang L, Vulliemoz N, Rivier J, Ferin M,. 2007. Astressin B, a corticotropin-releasing hormone receptor antagonist, accelerates the return to normal luteal function after an inflammatory-like stress challenge in the rhesus monkey. Endocrinology 148: 841-848. (Pubitemid 46143184)
65. Zuckerman S, Parkes AS,. 1939. Observations on the secondary sexual characters in monkeys. J Endocrinol 1: 430-439.