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Dehydroepiandrosterone-sulfate (DHEA-S), sex, and age in zoo-housed western lowland gorillas (Gorilla gorilla gorilla)

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Abstract

Among humans, dehydroepiandrosterone-sulfate (DHEA-S) declines with age and is hypothesized to be involved in somatic maintenance and healthy aging. Men have significantly higher DHEA-S than women, contradicting longer lifespans in the latter. Declines of DHEA-S with age also are observed in chimpanzees. In both chimpanzees and bonobos, males and females show no differences in DHEA-S production. Based on human and chimpanzee data, gorillas were predicted to show declining DHEA-S with age. Similar to chimpanzees and bonobos, it also was predicted DHEA-S would not be significantly different between males and females. DHEA-S was assayed from serum banked during physical examinations of gorillas housed at three North American zoos (n = 63). Gorillas ranged from 6 to 52 years of age. Differences between males and females were examined using t tests. Linear regression was used to determine the relationship of DHEA-S with age. There was no significant difference in DHEA-S between males and females. Additionally, there was no significant relationship between DHEA-S and age. As predicted, there were no sex-based differences in DHEA-S in gorillas, which is similar to chimpanzees and bonobos but different from modern humans. Unlike chimpanzees and humans, there was no significant relationship between DHEA-S and age in gorillas. The absence of a relationship between age and DHEA-S may be due to the lack of gorillas under age 6 years in this sample as declines in chimpanzees occur prior to age 5 years, more rapid growth and development among gorillas compared with other African hominoids, or a unique pattern of DHEA-S production.

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References

  • Barrett-Connor E, Goodman-Gruen D (1995) The epidemiology of DHEAS and cardiovascular disease. Ann N Y Acad Sci 774:259–270

    Article  CAS  PubMed  Google Scholar 

  • Barrett-Connor E, Khaw K-T, Yen SSC (1986) A prospective study of dehydroepiandrosterone sulfate, mortality, and cardiovascular disease. N Engl J Med 315:1519–1524

    Article  CAS  PubMed  Google Scholar 

  • Bastianetto S, Ramassamy C, Poirier J, Quirion R (1999) Dehydroepiandrosterone (DHEA) protects hippocampal cells from oxidative stress-induced damage. Mol Brain Res 66:35–41

    Article  CAS  PubMed  Google Scholar 

  • Behringer V, Hohmann G, Stevens JMG, Weltring A, Deschner T (2012) Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels. J Endocrinol 214:55–65

    Article  CAS  PubMed  Google Scholar 

  • Beishuizen A, Thijs LG, Vermes I (2002) Decreased levels of dehydroepiandrosterone sulphate in severe critical illness: a sign of exhausted adrenal reserve? Crit Care 6:434–438

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernstein RM, Sterner KN, Wildman DE (2012) Adrenal androgen production in catarrhine primates and the evolution of adrenarche. Am J Phys Anthropol 147:389–400

    Article  PubMed  PubMed Central  Google Scholar 

  • Bird CE, Cook SJ, Dressel DE, Clark AF (1980) Plasma C19-Δ5-steroid levels during normal human pregnancy. Clin Biochem 13:126–128

    Article  CAS  PubMed  Google Scholar 

  • Blevins JK, Coxworth JE, Herndon JG, Hawkes K (2013) Brief communication: adrenal androgens and aging: female chimpanzees (Pan troglodytes) compared with women. Am J Phys Anthropol 151:643–648

    Article  PubMed  PubMed Central  Google Scholar 

  • Buford TW, Willoughby DS (2008) Impact of DHEA(S) and cortisol on immune function in aging: a brief review. Appl Physiol Nutr Metab 33:429–433

    Article  CAS  PubMed  Google Scholar 

  • Butcher SK, Killampalli V, Lascelles D, Wang K, Alpar EK, Lord JM (2005) Raised cortisol:DHEAS ratios in the elderly after injury: potential impact upon neutrophil function and immunity. Aging Cell 4:319–324

    Article  CAS  PubMed  Google Scholar 

  • Conley AJ, Pattison JC, Bird IM (2004) Variations in adrenal androgen production among (nonhuman) primates. Sem Reprod Med 22:311–326

    Article  CAS  Google Scholar 

  • Enomoto M, Adachi H, Fukami A, Furuki K, Satoh A, Otsuka M, Kumagae S, Nanjo Y, Shigetoh Y, Imaizumi T (2008) Serum dehydroepiandrosterone sulfate levels predict longevity in men: 27-year follow-up study in a community-based cohort (Tanushimaru study). J Am Geriatr Soc 56:994–998

    Article  PubMed  Google Scholar 

  • Everly GS, Lating JM (2013) The anatomy and physiology of the human stress response. A clinical guide to the treatment of the human stress response, 3rd edn. Springer, New York, pp 17–51

    Chapter  Google Scholar 

  • Giordano R, Di Vito L, Lanfranco F, Broglio F, Benso A, Gianotti L, Grottoli S, Ghigao E, Arvat E (2001) Elderly subjects show severe impairment of dehydroepiandrosterone sulphate and reduced sensitivity of cortisol and aldosterone response to the stimulary effect of ACTH1-24. Clin Endocrinol 55:259–265

    Article  CAS  Google Scholar 

  • Goldman N, Glei DA, Seplaki C, Liu IW, Weinstein M (2005) Perceived stress and physiological dysregulation in older adults. Stress 8:95–105

    Article  CAS  PubMed  Google Scholar 

  • Gordon CM, Glowacki J, LeBoff MS (1999) DHEA and the skeleton (through the ages). Endocrine 11:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hagey LR, Czekala NM (2003) Comparative urinary androstanes in the great apes. Gen Comp Endocrinol 130:64–69

    Article  CAS  PubMed  Google Scholar 

  • Harcourt AH, Stewart KJ (2007) Gorilla society: conflict, compromise, and cooperation between the sexes. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Harder JD (2012) Reproduction and hormones. In: Silvy NJ (ed) The wildlife techniques manual. John Hopkins University Press, Baltimore, pp 502–525

    Google Scholar 

  • Labrie F, Bélanger A, Cusan L, Gomez J-L, Candas B (1997) Marked decline in serum concentrations of adrenal C19 sex steroid precursors and conjugated androgen metabolites during aging. J Clin Endocrinol Metab 82:2396–2402

    Article  CAS  PubMed  Google Scholar 

  • Longcope C (1996) Dehydroepiandrosterone metabolism. J Endocrinol 150:S125–S127

    CAS  PubMed  Google Scholar 

  • Marik PE (2009) Endocrinology of the stress response during critical illness. In: Ronco C, Bellomo R, Kellum JA (eds) Critical care nephrology, 2nd edn. Elsevier, Philadelphia, pp 711–716

    Google Scholar 

  • Mazat L, Lafont S, Berr C, Debuire B, Tessier J-F, Dartigues J-F, Baulieu E-E (2001) Prospective measurements of dehydroepiandrosterone sulfate in a cohort of elderly subjects: relationship to gender, subjective health, smoking habits, and 10-year mortality. Proc Natl Acad Sci USA 98:8145–8150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEwen BS (2004) Protective and damaging effects of the mediators of stress and adaptation: allostasis and allostatic load. In: Schulkin J (ed) Allostatis, homeostasis, and the costs of physiological adaptation. Cambridge University Press, Cambridge, pp 65–98

    Chapter  Google Scholar 

  • Muehlenbein MP, Campbell BC, Murchison MA, Phillippi KM (2002) Morphological and hormonal parameters in two species of macaques: impact of seasonal breeding. Am J Phys Anthropol 117:218–227

    Article  PubMed  Google Scholar 

  • Nelson RJ (2011) An introduction to behavioral endocrinology. Sinauer Associates, Sunderland

    Google Scholar 

  • Nieschlag E, Walk T, Schindler AE (1974) Dehydroepiandrosterone (DHA) and DHA-sulfate during pregnancy in maternal blood. Horm Metab Res 6:170–171

    Article  CAS  PubMed  Google Scholar 

  • Orentreich N, Brind JL, Rizer RL, Vogelman JH (1984) Age changes and sex differences in serum dehydroepiandrosterone sulfate concentrations throughout adulthood. J Clin Endocrinol Metab 59:551–555

    Article  CAS  PubMed  Google Scholar 

  • Parker CR Jr, Slayden SM, Azziz R, Crabbe SL, Hines GA, Boots LR, Bae S (2000) Effects of aging on adrenal function in the human: responsiveness and sensitivity of adrenal androgens and cortisol to adrenocorticotropin in premenopausal and postmenopausal women. J Clin Endocrinol Metab 85:48–54

    CAS  PubMed  Google Scholar 

  • Poršová-Dutoit I, Šulcová J, Stárka L (2000) Do DHEA/DHEAS play a protective role in coronary heart disease? Physiol Res 49:S43–S56

    PubMed  Google Scholar 

  • Rivarola MA, Forest MG, Migeon CJ (1968) Testosterone, androstenedione and dehydroepiandrosterone in plasma during pregnancy and at delivery: concentration and protein binding. J Clin Endocrinol Metab 28:34–40

    Article  CAS  PubMed  Google Scholar 

  • Schaefer SA, Steklis HD (2014) Personality and subjective well-being in captive male western lowland gorillas living in bachelor groups. Am J Primatol 76:879–889

    Article  PubMed  Google Scholar 

  • Seaward BL (2006) Managing stress: principles and strategies for health and well being. Jones and Bartlett, Boston

    Google Scholar 

  • Seeman TE, Singer BH, Rowe JW, Horwitz RI, McEwen BS (1997) Price of adaptation—allostatic load and its health consequences. Arch Intern Med 157:2259–2268

    Article  CAS  PubMed  Google Scholar 

  • Seraphin SB, Whitten PL, Reynolds V (2008) The influence of age on fecal steroid hormone levels in male Budongo Forest chimpanzees (Pan troglodytes schweinfurthii). Am J Primatol 70:661–669

    Article  CAS  PubMed  Google Scholar 

  • Singer BH, Ryff CD, Seeman TE (2004) Operationalizing allostatic load. In: Schulkin J (ed) Allostatis, homeostasis, and the costs of physiological adaptation. Cambridge University Press, Cambridge, pp 113–149

    Chapter  Google Scholar 

  • Šulcová J, Hill M, Hampl R, Stárka L (1997) Age and sex related differences in serum levels of unconjugated dehydroepiandrosterone and its sulphate in normal subjects. J Endocrinol 154:57–62

    Article  PubMed  Google Scholar 

  • Svec F, Lopez SA (1989) Antiglucocorticoid actions of dehydroepiandrosterone and low concentrations in Alzheimer’s disease. Lancet 334:1335–1336

    Article  Google Scholar 

  • Tagawa N, Hidaka Y, Takano T, Shimaoka Y, Kobayashi Y, Amino N (2004) Serum concentrations of dehydroepiandrosterone and dehydroepiandrosterone sulfate and their relation to cytokine production during and after normal pregnancy. Clin Chim Acta 340:187–193

    Article  CAS  PubMed  Google Scholar 

  • Watts DP (2012) The apes: taxonomy, biogeography, life histories, and behavioral ecology. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp 113–142

    Google Scholar 

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Acknowledgements

This research would not have been possible without the assistance of veterinarians and staff at the Columbus Zoo and Aquarium. I would like to express my gratitude to Douglas E. Crews, the associate editor, and two anonymous reviewers for their helpful suggestions and advice.

Funding

Funding for this research was provided by The Ohio State University Department of Anthropology and the Columbus Zoo and Aquarium.

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  1. Department of Anthropology, The Ohio State University, 4034 Smith Laboratory, 174 West 18th Avenue, Columbus, OH, 43210, USA

    Ashley N. Edes

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  1. Ashley N. Edes
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Correspondence to Ashley N. Edes.

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I declare no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Edes, A.N. Dehydroepiandrosterone-sulfate (DHEA-S), sex, and age in zoo-housed western lowland gorillas (Gorilla gorilla gorilla). Primates 58, 385–392 (2017). https://doi.org/10.1007/s10329-017-0602-2

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  • DOI: https://doi.org/10.1007/s10329-017-0602-2

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