Characterization of the Onset of Menopause in the Rhesus Macaque1

Gilardi, Kirsten; Shideler, S. E.; Valverde, Celia R.; Roberts, Jeffrey A.; Lasley, Bill L.

doi:10.1095/biolreprod57.2.335

Cited by 168 publications

(144 citation statements)

References 13 publications

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“…Evidence reported to date supports the idea that macaques go through physical changes associated with reproductive senescence, reminiscent of changes observed during human menopause. Studies involving ovarian, hormonal, and pituitary function of aging rhesus macaques (Hodgen et al 1977, Gilardi et al 1997, Gore et al 2004, Nichols et al 2005, Schramm et al 2002 have consistently shown biological changes mirroring those known to occur in women and support the macaque as an adequate model of human menopause. In Japanese macaques, a decrease in ovarian control of gonadotropin levels has been reported in monkeys approximately at age 18 (Nozaki et al 1995).…”

Section: Ttd (Years)mentioning

confidence: 85%

“…An increase in gonadotropin releasing hormone concentrations, associated with a reduction of estrogen at menopause, has also been reported in aged rhesus monkeys (Gore et al 2004). Aging rhesus monkeys experience irregular menstrual cycles and long follicular phases due to delayed ovulation (Gilardi et al 1997). Moreover, Schramm et al (2002) found that as monkeys age, serum follicle stimulating hormone (FSH) levels increase, peak estradiol levels during hyperstimulation decrease and oocyte retrieval numbers are lower when compared with younger animals, which is consistent with what is commonly seen in older women.…”

Section: Introductionmentioning

confidence: 84%

“…The fact that birth intervals tend to increase with advancing age may be a reflection of irregular ovulation patterns in older monkeys (Nozaki et al 1995, Gilardi et al 1997, as well as the increased strain on older mothers raising infants. In a study of the population on Cayo Santiago, older females were much less likely to produce an infant if they had given birth the previous season (Campell & Gerald 2004).…”

Section: Ttd (Years)mentioning

confidence: 99%

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Age as a determinant of reproductive success among captive female rhesus macaques (Macaca mulatta)

Gagliardi¹,

Liukkonen²,

Phillippi-Falkenstein³

et al. 2007

Reproduction

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A retrospective analysis was performed on fertility outcomes among a colony of captive Indian rhesus monkeys. The analysis covered over 30 years and was based on 1443 females with a total of 11 453 pregnancies. Various determinants of fertility were assessed including birth rates, pregnancy loss, infant survival, interbirth intervals, and interval from last birth to death. Binary variables were analyzed with generalized linear models with random intercepts, while linear mixed models were used for analysis of continuous variables. Age of the dam was a significant factor in determining whether a pregnancy resulted in a birth and whether an infant survived the first 30 days with primiparous or older mothers being less likely to produce an infant surviving to that age. In contrast, sex proved to be the only significant factor in determining whether an infant lived to 1 year, with females being more likely to survive. The interval between births proved to be affected primarily by dam age, while the late death of an infant depressed the likelihood of an extended time interval between her last birth and her death. Overall, these results demonstrate that maternal age contributes significantly to a decline in fertility and older females can live relatively long periods following birth of their last infant.

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Section: Ttd (Years)mentioning

confidence: 85%

Section: Introductionmentioning

confidence: 84%

Section: Ttd (Years)mentioning

confidence: 99%

See 1 more Smart Citation

Age as a determinant of reproductive success among captive female rhesus macaques (Macaca mulatta)

Gagliardi¹,

Liukkonen²,

Phillippi-Falkenstein³

et al. 2007

Reproduction

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“…Despite the absence of seasonality in terms of food availability, individuals were still exposed to seasonal changes in day length and temperature, both important factors driving seasonal breeding and reproductive hormone secretion (Wingfield 1984). A negative correlation between fertility and age has been observed for a number of primate species including hanuman langurs (Presbytis entellus, Borries et al 1991), rhesus macaques (Macaca mulatta, Gilardi et al 1997;Shideler et al 2001) and olive baboons (Papio anubis, Strum and Western 1982). Although the average age of our captive female group was 3.6 ± 1.3 years (range: 2-5), thus at the chronological age of peak reproductive potential, the biological age of the ovaries could be at an advanced stage, influencing ovarian endocrine activity.…”

Section: Discussionmentioning

confidence: 99%

Female reproductive activity and its endocrine correlates in the African lesser bushbaby, Galago moholi

et al. 2015

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Steroid hormones play an important role in female reproductive physiology and behaviour and are often used to monitor important female reproductive events. However, such studies are often attempted on captive populations alone, delivering limited data. One such example is the African lesser bushbaby, Galago moholi, for which contradicting observational data exist between captive and free-ranging populations, while hormonal analyses have only been obtained from a single captive population. To extend and rectify the limited information, we monitored faecal progestagen and oestrogen metabolite levels across various important life history stages of both captive and free-ranging G. moholi. We additionally recorded changes 2 in vaginal state as well as the occurrence of reproductive and aggressive behaviour throughout the study. Data from our captive population revealed an ovarian cycle length of 33.44 ± 0.59 days (mean ± SD), with follicular and luteal phases of 14.2 ± 1.0 and 19.1 ± 1.5 days, respectively, and an average pregnancy length of 128 ± 3.3 days. The initiation of female reproductive activity was closely linked to an oestrus-related increase in faecal oestrogen metabolite levels. Four of the seven captive females monitored in our study conceived during the May mating period, with one additional female fertilised in September, supporting the idea that the September mating period functions as a back-up for female G. moholi. Identified benchmark faecal progestagen metabolite levels (non-pregnant: > 1 µg/g dry weight (DW), pregnant: > 9 µg/g DW) should help researchers to determine pregnancy-status of randomly wild-caught females in even a cross-sectional study set-up.

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“…Reproductive physiology and aging in Rhesus monkeys closely model these processes in women [42]. Rhesus monkeys live about 35 years, reach puberty at 3-5 years old, ovulate one egg each month, and maintain fertility for about 20 years, after which follicle numbers decline, and menopause ensues [43,44]. We tested the hypothesis that DNA damage increases and the DNA repair protein BRCA1 decreases in granulosa cells with advancing age in the Rhesus monkey.…”

Section: Electronic Supplementary Materialsmentioning

confidence: 99%

Increased DNA damage and repair deficiency in granulosa cells are associated with ovarian aging in rhesus monkey

Zhang

Zeng

et al. 2015

J Assist Reprod Genet

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Purpose Ovarian aging is closely tied to the decline in ovarian follicular reserve and oocyte quality. During the prolonged reproductive lifespan of the female, granulosa cells connected with oocytes play critical roles in maintaining follicle reservoir, oocyte growth and follicular development. We tested whether double-strand breaks (DSBs) and repair in granulosa cells within the follicular reservoir are associated with ovarian aging. Methods Ovaries were sectioned and processed for epifluorescence microscopy, confocal microscopy, and immunohistochemistry. DNA damage was revealed by immunstaining of γH2AX foci and telomere damage by γH2AX foci colocalized with telomere associated protein TRF2. DNA repair was indicated by BRCA1 immunofluorescence.Results DSBs in granulosa cells increase and DSB repair ability, characterized by BRCA1 foci, decreases with advancing age. γH2AX foci increase in primordial, primary and secondary follicles with advancing age. Likewise, telomere damage increases with advancing age. In contrast, BRCA1 foci in granulosa cells of primordial, primary and secondary follicles decrease with monkey age. BRCA1 positive foci in the oocyte nuclei also decline with maternal age. Conclusions Increased DSBs and reduced DNA repair in granulosa cells may contribute to ovarian aging. Discovery of therapeutics that targets these pathways might help maintain follicle reserve and postpone ovarian dysfunction with age.

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Characterization of the Onset of Menopause in the Rhesus Macaque1

Cited by 168 publications

References 13 publications

Age as a determinant of reproductive success among captive female rhesus macaques (Macaca mulatta)

Age as a determinant of reproductive success among captive female rhesus macaques (Macaca mulatta)

Female reproductive activity and its endocrine correlates in the African lesser bushbaby, Galago moholi

Increased DNA damage and repair deficiency in granulosa cells are associated with ovarian aging in rhesus monkey

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