Current understanding of ovarian aging

Springer Science and Business Media LLC - Tập 55 - Trang 659-669 - 2012
Qian Li1, XiaoDan Geng1, Wei Zheng1, Jie Tang1, Bo Xu1, QingHua Shi1
1Hefei National Laboratory for Physical Sciences at Microscale and School of Life Sciences, University of Science and Technology of China, Hefei, China

Tóm tắt

The reproductive system of human female exhibits a much faster rate of aging than other body systems. Ovarian aging is thought to be dominated by a gradual decreasing numbers of follicles, coinciding with diminished quality of oocytes. Menopause is the final step in the process of ovarian aging. This review focuses on the mechanisms underlying the ovarian aging involving a poor complement of follicles at birth and a high rate of attrition each month, as well as the alternated endocrine factors. We also discuss the possible causative factors that contribute to ovarian aging, e.g., genetic factors, accumulation of irreparable damage of microenvironment, pathological effect and other factors. The appropriate and reliable methods to assess ovarian aging, such as quantification of follicles, endocrine measurement and genetic testing have also been discussed. Increased knowledge of the ovarian aging mechanisms may improve the prevention of premature ovarian failure.

Tài liệu tham khảo

Templeton A, Morris J K, Parslow W. Factors that affect outcome of in vitro fertilisation treatment. Lancet, 1996, 348: 1402–1406 Baird D T, Collins J, Egozcue J, et al. Fertility and ageing. Hum Reprod Update, 2005, 11: 261–276 Broekmans F J, Knauff E A, te Velde E R, et al. Female reproductive ageing: Current knowledge and future trends. Trends Endocrinol Metab, 2007, 18: 58–65 Djahanbakhch O, Ezzati M, Zosmer A. Reproductive ageing in women. J Pathol, 2007, 211: 219–231 Hansen K R, Knowlton N S, Thyer A C, et al. A new model of reproductive aging: The decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod, 2008, 23: 699–708 McGee E A, Hsueh A J. Initial and cyclic recruitment of ovarian follicles. Endocr Rev, 2000, 21: 200–214 Hirshfield A N. Development of follicles in the mammalian ovary. Int Rev Cytol, 1991, 124: 43–101 Markstrom E, Svensson E, Shao R, et al. Survival factors regulating ovarian apoptosis — dependence on follicle differentiation. Reproduction, 2002, 123: 23–30 te Velde E R, Pearson P L. The variability of female reproductive ageing. Hum Reprod Update, 2002, 8: 141–154 Block E. A quantitative morphological investigation of the follicular system in newborn female infants. Acta anatomica, 1953, 17: 201–206 Alviggi C, Humaidan P, Howles C M, et al. Biological versus chronological ovarian age: Implications for assisted reproductive technology. Reprod Biol Endocrinol, 2009, 7: 101 te Velde E R, Scheffer G J, Dorland M, et al. Developmental and endocrine aspects of normal ovarian aging. Mol Cell Endocrinol, 1998, 145: 67–73 Faddy M J, Gosden R G, Gougeon A, et al. Accelerated disappearance of ovarian follicles in mid-life: Implications for forecasting menopause. Hum Reprod, 1992, 7: 1342–1346 Klein N A, Soules M R. Endocrine changes of the perimenopause. Clin Obstet Gynecol, 1998, 41: 912–920 Navot D, Bergh P A, Williams M A, et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet, 1991, 337: 1375–1377 Faddy M J, Gosden R G. A mathematical model of follicle dynamics in the human ovary. Hum Reprod, 1995, 10: 770–775 Faddy M J. Follicle dynamics during ovarian ageing. Mol Cell Endocrinol, 2000, 163: 43–48 Nikolaou D, Templeton A. Early ovarian ageing: A hypothesis. Detection and clinical relevance. Hum Reprod, 2003, 18: 1137–1139 de Bruin J P, Dorland M, Spek E R, et al. Age-related changes in the ultrastructure of the resting follicle pool in human ovaries. Biol Reprod, 2004, 70: 419–424 Treloar A E. Menstrual cyclicity and the pre-menopause. Maturitas, 1981, 3: 249–264 Battaglia D E, Goodwin P, Klein N A, et al. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod, 1996, 11: 2217–2222 Kuliev A, Cieslak J, Verlinsky Y. Frequency and distribution of chromosome abnormalities in human oocytes. Cytogenet Genome Res, 2005, 111: 193–198 Hunt P A, Hassold T J. Human female meiosis: What makes a good egg go bad? Trends Genet, 2008, 24: 86–93 Pellestor F, Anahory T, Hamamah S. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet Genome Res, 2005, 111: 206–212 Warburton D. Biological aging and the etiology of aneuploidy. Cytogenet Genome Res, 2005, 111: 266–272 Menken J, Trussell J, Larsen U. Age and infertility. Science, 1986, 233: 1389–1394 Howles C M, Kim C H, Elder K. Treatment strategies in assisted reproduction for women of advanced maternal age. Int Surgery, 2006, 91: S37–54 Gougeon A, Ecochard R, Thalabard J C. Age-related changes of the population of human ovarian follicles: Increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol Reprod, 1994, 50: 653–663 van Zonneveld P, Scheffer G J, Broekmans F J M, et al. Do cycle disturbances explain the age-related decline of female fertility? Cycle characteristics of women aged over 40 years compared with a reference population of young women. Hum Reprod, 2003, 18: 495–501 Santoro N, Isaac B, Neal-Perry G, et al. Impaired folliculogenesis and ovulation in older reproductive aged women. J Clin Endocrinol Metab, 2003, 88: 5502–5509 Treloar A E, Boynton R E, Behn B G, et al. Variation of the human menstrual cycle through reproductive life. Int J Fertil, 1967, 12: 77–126 Yamoto M, Minami S, Nakano R, et al. Immunohistochemical localization of inhibin/activin subunits in human ovarian follicles during the menstrual cycle. J Clin Endocrinol Metab, 1992, 74: 989–993 Schwall R H, Mason A J, Wilcox J N, et al. Localization of inhibin/activin subunit mrnas within the primate ovary. Mol Endocrinol, 1990, 4: 75–79 Roberts V J, Barth S, el-Roeiy A, et al. Expression of inhibin/activin subunits and follistatin messenger ribonucleic acids and proteins in ovarian follicles and the corpus luteum during the human menstrual cycle. J Clin Endocrinol Metab, 1993, 77: 1402–1410 Klein N A, Illingworth P J, Groome N P, et al. Decreased inhibin B secretion is associated with the monotropic FSH rise in older, ovulatory women: A study of serum and follicular fluid levels of dimeric inhibin a and b in spontaneous menstrual cycles. J Clin Endocr Metab, 1996, 81: 2742–2745 Klein N A, Houmard B S, Hansen K R, et al. Age-related analysis of inhibin a, inhibin B, and activin a relative to the intercycle monotropic follicle-stimulating hormone rise in normal ovulatory women. J Clin Endocrinol Metab, 2004, 89: 2977–2981 Danforth D R, Arbogast L K, Mroueh J, et al. Dimeric inhibin: A direct marker of ovarian aging. Fertil Steril, 1998, 70: 119–123 Hurwitz J M, Santoro N. Inhibins, activins, and follistatin in the aging female and male. Semin Reprod Med, 2004, 22: 209–217 Santoro N, Adel T, Skurnick J H. Decreased inhibin tone and increased activin a secretion characterize reproductive aging in women. Fertil Steril, 1999, 71: 658–662 Reame N E, Wyman T L, Phillips D J, et al. Net increase in stimulatory input resulting from a decrease in inhibin B and an increase in activin a may contribute in part to the rise in follicular phase follicle-stimulating hormone of aging cycling women. J Clin Endocrinol Metab, 1998, 83: 3302–3307 Randolph J F Jr., Sowers M, Bondarenko I V, et al. Change in estradiol and follicle-stimulating hormone across the early menopausal transition: Effects of ethnicity and age. J Clin Endocrinol Metab, 2004, 89: 1555–1561 Santoro N. The menopausal transition. Am J Med, 2005, 118: 8–13 Burger H G, Hale G E, Robertson D M, et al. A review of hormonal changes during the menopausal transition: Focus on findings from the melbourne women’s midlife health project. Hum Reprod Update, 2007, 13: 559–565 Beemsterboer S N, Homburg R, Gorter N A, et al. The paradox of declining fertility but increasing twinning rates with advancing maternal age. Hum Reprod, 2006, 21: 1531–1532 Gleicher N, Weghofer A, Barad D H. Defining ovarian reserve to better understand ovarian aging. Reprod Biol Endocrinol, 2011, 9: 23 Ferrell R J, Sowers M. Longitudinal, epidemiologic studies of female reproductive aging. Ann N Y Acad Sci, 2010, 1204: 188–197 Younis J S. Ovarian aging: Latest thoughts on assessment and management. Curr Opin Obstet Gynecol, 2011, 23: 427–434 Murabito J M, Yang Q, Fox C, et al. Heritability of age at natural menopause in the framingham heart study. J Clin Endocrinol Metab, 2005, 90: 3427–3430 Torgerson D J, Thomas R E, Reid D M. Mothers and daughters menopausal ages: Is there a link? Eur J Obstet Gynecol Reprod Biol, 1997, 74: 63–66 van Asselt K M, Kok H S, Pearson P L, et al. Heritability of menopausal age in mothers and daughters. Fertil Steril, 2004, 82: 1348–1351 Wicks J, Treloar S A, Martin N G. Using identity-by-de scent information in affected sib pairs to increase the efficiency of genetic association studies. Twin Res, 2004, 7: 211–216 Jagarlamudi K, Reddy P, Adhikari D, et al. Genetically modified mouse models for premature ovarian failure (POF). Mol Cell Endocrinol, 2010, 315: 1–10 Altshuler D, Brooks L D, Chakravarti A, et al. A haplotype map of the human genome. Nature, 2005, 437: 1299–1320 Lakhal B, Laissue P, Braham R, et al. Bmp15 and premature ovarian failure: Causal mutations, variants, polymorphisms? Clin Endocrinol, 2010, 72: 425–426 Willer C J, Scott L J, Bonnycastle L L, et al. Tag snp selection for finnish individuals based on the ceph utah hapmap database. Genet Epidemiol, 2006, 30: 180–190 Hamatani T, Falco G, Carter M G, et al. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet, 2004, 13: 2263–2278 Welt C K, Smith P C, Taylor A E. Evidence of early ovarian aging in fragile X premutation carriers. J Clin Endocr Metab, 2004, 89: 4569–4574 Hsu S Y, Hsueh A J W. Tissue-specific Bcl-2 protein partners in apoptosis: An ovarian paradigm. Physiol Rev, 2000, 80: 593–614 Petros A M, Olejniczak E T, Fesik S W. Structural biology of the Bcl-2 family of proteins. Bba-Mol Cell Res, 2004, 1644: 83–94 He C Y, Kraft P, Chen C, et al. Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nat Genet, 2009, 41: 724–728 Stolk L, Zhai G, van Meurs J B J, et al. Loci at chromosomes 13, 19 and 20 influence age at natural menopause. Nat Genet, 2009, 41: 645–647 Pellestor F, Anahory T, Hamamah S. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet Genome Res, 2005, 111: 206–212 Pellestor F, Andreo B, Anahory T, et al. The occurrence of aneuploidy in human: Lessons from the cytogenetic studies of human oocytes. European J Med Genet, 2006, 49: 103–116 Colbere-Garapin F, Duncan G, Pavio N, et al. An approach to understanding the mechanisms of poliovirus persistence in infected cells of neural or non-neural origin. Clin Diagn Virol, 1998, 9: 107–113 Battaglia D E, Goodwin P, Klein N A, et al. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod, 1996, 11: 2217–2222 Ghosh S, Bhaumik P, Ghosh P, et al. Chromosome 21 non-disjunction and down syndrome birth in an indian cohort: Analysis of incidence and aetiology from family linkage data. Genet Res, 2010, 92: 189–197 Hassold T, Abruzzo M, Adkins K, et al. Human aneuploidy: Incidence, origin, and etiology. Environ Mol Mutag, 1996, 28: 167–175 Macdonald M, Hassold T, Harvey J, et al. The origin of 47,XXY and 47,XXX aneuploidy-heterogeneous mechanisms and role of aberrant recombination. Hum Mol Genet, 1994, 3: 1365–1371 Angell R R. Predivision in human oocytes at meiosis-I — a mechanism for trisomy formation in man. Hum Genet, 1991, 86: 383–387 Petersen M B. Origin and mechanisms of nondisjunction in human autosomal trisomies. Cytogenet Cell Genet, 1999, 85: 21–21 Watanabe Y, Nurse P. Cohesin rec8 is required for reductional chromosome segregation at meiosis. Nature, 1999, 400: 461–464 Trifunovic A, Wredenberg A, Falkenberg M, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature, 2004, 429: 417–423 Seifer D B, DeJesus V, Hubbard K. Mitochondrial deletions in luteinized granulosa cells as a function of age in women undergoing in vitro fertilization. Fertil Steril, 2002, 78: 1046–1048 Tatone C, Carbone M C, Falone S, et al. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod, 2006, 12: 655–660 Perez G I, Jurisicova A, Matikainen T, et al. A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J, 2005, 19: 860–862 Perez G I, Tilly J L. Cumulus cells are required for the increased apoptotic potential in oocytes of aged mice. Hum Reprod, 1997, 12: 2781–2783 Gaulden M E. Maternal age effect: The enigma of down syndrome and other trisomic conditions. Mutat Res, 1992, 296: 69–88 Gordo A C, Rodrigues P, Kurokawa M, et al. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod, 2002, 66: 1828–1837 Eichenlaub-Ritter U, Vogt E, Yin H, et al. Spindles, mitochondria and redox potential in ageing oocytes. Reprod Biomed Online, 2004, 8: 45–58 Klein J, Sauer M V. Assessing fertility in women of advanced reproductive age. Am J Obstet Gynecol, 2001, 185: 758–770 Blasco M A, Gasser S M, Lingner J. Telomeres and telomerase. Genes Dev, 1999, 13: 2353–2359 Greider C W. Telomeres, telomerase and senescence. Bioessays, 1990, 12: 363–369 Harley C B, Futcher A B, Greider C W. Telomeres shorten during aging of human fibroblasts. Nature, 1990, 345: 458–460 Vonzglinicki T, Saretzki G, Docke W, et al. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts-a model for senescence. Exp Cell Res, 1995, 220: 186–193 Collins K. Structure and function of telomerase. Curr Opin Cell Biol, 1996, 8: 374–380 Harrington L A, Greider C W. Telomerase primer specificity and chromosome healing. Nature, 1991, 353: 451–454 Yu G L, Blackburn E H. Developmentally programmed healing of chromosomes by telomerase in tetrahymena. Cell, 1991, 67: 823–832 Keefe D L, Marquard K, Liu L. The telomere theory of reproductive senescence in women. Curr Opin Obstet Gyn, 2006, 18: 280–285 Kinugawa C, Murakami T, Okamura K, et al. Telomerase activity in normal ovaries and premature ovarian failure. Tohoku J Exp Med, 2000, 190: 231–238 Hanna C W, Bretherick K L, Gair J L, et al. Telomere length and reproductive aging. Hum Reprod, 2009, 24: 1206–1211 Butts S, Riethman H, Ratcliffe S, et al. Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab, 2009, 94: 4835–4843 Moore G E. Biochemical and cellular mechanisms of aging and degenerative disease: Excessive, poor-quality caloric intake may deplete essential nutrients and interfere with cellular processes to produce degenerative damage. Med Hypotheses, 2008, 70: 768–775 Yin D, Chen K. The essential mechanisms of aging: Irreparable damage accumulation of biochemical side-reactions. Exp Gerontol, 2005, 40: 455–465 Sohal R S. Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med, 2002, 33: 37–44 Agarwal A, Aponte-Mellado A, Premkumar B J, et al. The effects of oxidative stress on female reproduction: A review. Reprod Biol Endocrinol, 2012, 10: 49 Sahin E, Depinho R A. Axis of ageing: Telomeres, p53 and mitochondria. Nat Rev Mol Cell Biol, 2012, 13: 397–404 Miquel J, Economos A C, Fleming J, et al. Mitochondrial role in cell aging. Exp Gerontol, 1980, 15: 575–591 Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: Implications for cell death. Ann Rev Pharmacol Toxicol, 2007, 47: 143–183 Vercesi A E, Kowaltowski A J, Oliveira H C, et al. Mitochondrial Ca2+ transport, permeability transition and oxidative stress in cell death: Implications in cardiotoxicity, neurodegeneration and dyslipidemias. Front Biosci, 2006, 11: 2554–2564 Tatone C, Amicarelli F, Carbone M C, et al. Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update, 2008, 14: 131–142 Wiener-Megnazi Z, Vardi L, Lissak A, et al. Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization. Fertil Steril, 2004, 82: 1171–1176 Tarin J J. Aetiology of age-associated aneuploidy: A mechanism based on the ‘free radical theory of ageing’. Hum Reprod, 1995, 10: 1563–1565 Tarin J J. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod, 1996, 2: 717–724 Tamura H, Takasaki A, Miwa I, et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res, 2008, 44: 280–287 Liu L, Keefe D L. Cytoplasm mediates both development and oxidation-induced apoptotic cell death in mouse zygotes. Biol Reprod, 2000, 62: 1828–1834 Liu L, Trimarchi J R, Keefe D L. Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol Reprod, 2000, 62: 1745–1753 Lass A, Skull J, McVeigh E, et al. Measurement of ovarian volume by transvaginal sonography before ovulation induction with human menopausal gonadotrophin for in-vitro fertilization can predict poor response. Hum Reprod, 1997, 12: 294–297 Van Blerkom J. The influence of intrinsic and extrinsic factors on the developmental potential and chromosomal normality of the human oocyte. J Soc Gynecol Investig, 1996, 3: 3–11 Tarin J J, Perez-Albala S, Cano A. Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse. Mol Reprod Dev, 2002, 61: 385–397 Zhang X, Wu X Q, Lu S, et al. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res, 2006, 16: 841–850 Carbone M C, Tatone C, Delle Monache S, et al. Antioxidant enzymatic defences in human follicular fluid: Characterization and age-dependent changes. Mol Hum Reprod, 2003, 9: 639–643 Gonzalez-Parraga P, Hernandez J A, Arguelles J C. Role of antioxidant enzymatic defences against oxidative stress H2O2 and the acquisition of oxidative tolerance in candida albicans. Yeast, 2003, 20: 1161–1169 Yim M B, Yim H S, Lee C, et al. Protein glycation: Creation of catalytic sites for free radical generation. Ann N Y Acad Sci, 2001, 928: 48–53 Schmidt A M, Yan S D, Yan S F, et al. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta, 2000, 1498: 99–111 Mullarkey C J, Edelstein D, Brownlee M. Free radical generation by early glycation products: A mechanism for accelerated atherogenesis in diabetes. Biochem Biophys Res Commun, 1990, 173: 932–939 Sakurai T, Tsuchiya S. Superoxide production from nonenzymatically glycated protein. FEBS Lett, 1988, 236: 406–410 Wen Y, Skidmore J C, Porter-Turner M M, et al. Relationship of glycation, antioxidant status and oxidative stress to vascular endothelial damage in diabetes. Diabetes Obes Metab, 2002, 4: 305–308 Soldatos G, Cooper M E. Advanced glycation end products and vascular structure and function. Curr Hypertens Rep, 2006, 8: 472–478 Frye E B, Degenhardt T P, Thorpe S R, et al. Role of the maillard reaction in aging of tissue proteins. Advanced glycation end product-dependent increase in imidazolium cross-links in human lens proteins. J Biol Chem, 1998, 273: 18714–18719 Kim J, Kim O S, Kim C S, et al. Accumulation of argpyrimidine, a methylglyoxal-derived advanced glycation end product, increases apoptosis of lens epithelial cells both in vitro and in vivo. Exp Mol Med, 2012, 44: 167–175 Mizutani K, Ikeda K, Tsuda K, et al. Inhibitor for advanced glycation end products formation attenuates hypertension and oxidative damage in genetic hypertensive rats. J Hypertens, 2002, 20: 1607–1614 Dixit H, Rao L K, Padmalatha V V, et al. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet, 2006, 119: 408–415 Laissue P, Christin-Maitre S, Touraine P, et al. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol, 2006, 154: 739–744 Schmidt D, Ovitt C E, Anlag K, et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development, 2004, 131: 933–942 Van Blerkom J, Antczak M, Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: Association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum Reprod, 1997, 12: 1047–1055 Modlich U, Kaup F J, Augustin H G. Cyclic angiogenesis and blood vessel regression in the ovary: Blood vessel regression during luteolysis involves endothelial cell detachment and vessel occlusion. Lab Invest, 1996, 74: 771–780 Redmer D A, Reynolds L P. Angiogenesis in the ovary. Rev Reprod, 1996, 1: 182–192 Huey S, Abuhamad A, Barroso G, et al. Perifollicular blood flow doppler indices, but not follicular po2, pco2, or ph, predict oocyte developmental competence in in vitro fertilization. Fertil Steril, 1999, 72: 707–712 Bhal P S, Pugh N D, Gregory L, et al. Perifollicular vascularity as a potential variable affecting outcome in stimulated intrauterine insemination treatment cycles: A study using transvaginal power doppler. Hum Reprod, 2001, 16: 1682–1689 Borini A, Maccolini A, Tallarini A, et al. Perifollicular vascularity and its relationship with oocyte maturity and IVF outcome. Ann N Y Acad Sci, 2001, 943: 64–67 Amicarelli F, Ragnelli A M, Aimola P, et al. Age-dependent ultrastructural alterations and biochemical response of rat skeletal muscle after hypoxic or hyperoxic treatments. Biochim Biophys Acta, 1999, 1453: 105–114 Vessey M P, Villard-Mackintosh L, Painter R. Epidemiology of endometriosis in women attending family planning clinics. BMJ, 1993, 306: 182–184 Allaire C. Endometriosis and infertility: A review. J Reprod Med, 2006, 51: 164–168 Jacobson T Z, Duffy J M, Barlow D, et al. Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev, 2010, CD001398 Islam M N, Islam M M. Biological and behavioural determinants of fertility in bangladesh: 1975–1989. Asia Pac Popul J, 1993, 8: 3–18 McKinlay S M, Brambilla D J, Posner J G. The normal menopause transition. Maturitas, 2008, 61: 4–16 Jensen T K, Henriksen T B, Hjollund N H, et al. Adult and prenatal exposures to tobacco smoke as risk indicators of fertility among 430 danish couples. Am J Epidemiol, 1998, 148: 992–997 Sharara F I, Scott R T Jr., Seifer D B. The detection of diminished ovarian reserve in infertile women. Am J Obstet Gynecol, 1998, 179: 804–812 Goldin A, Beckman J A, Schmidt A M, et al. Advanced glycation end products: Sparking the development of diabetic vascular injury. Circulation, 2006, 114: 597–605 Richardson S J, Nelson J F. Follicular depletion during the menopausal transition. Ann N Y Acad Sci, 1990, 592: 13–20; discussion 44–51 Lass A, Silye R, Abrams D C, et al. Follicular density in ovarian biopsy of infertile women: A novel method to assess ovarian reserve. Hum Reprod, 1997, 12: 1028–1031 Lambalk C B, de Koning C H, Flett A, et al. Assessment of ovarian reserve. Ovarian biopsy is not a valid method for the prediction of ovarian reserve. Hum Reprod, 2004, 19: 1055–1059 Hendriks D J, Kwee J, Mol B W J, et al. Ultrasonography as a tool for the prediction of outcome in ivf patients: A comparative meta-analysis of ovarian volume and antral follicle count. Fertil Steril, 2007, 87: 764–775 van Rooij I A J, Tonkelaar I, Broekmans F J M, et al. Anti-mullerian hormone is a promising predictor for the occurrence of the menopausal transition. Menopause, 2004, 11: 601 Broekmans F J, de Ziegler D, Howles C M, et al. The antral follicle count: Practical recommendations for better standardization. Fertil Steril, 2010, 94: 1044–1051 Younis J S, Haddad S, Matilsky M, et al. Undetectable basal ovarian stromal blood flow in infertile women is related to low ovarian reserve. Gynecol Endocrinol, 2007, 23: 284–289 Robertson D M. Anti-müllerian hormone as a marker of ovarian reserve: An update. Women’s Health, 2008, 4: 137–141 Sowers M F R, Eyvazzadeh A D, McConnell D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab, 2008, 93: 3478–3483 Sharov A A, Falco G, Piao Y, et al. Effects of aging and calorie restriction on the global gene expression profiles of mouse testis and ovary. BMC Biol, 2008, 6: 24 Welt C K, Smith Z A, Pauler D K, et al. Differential regulation of inhibin a and inhibin B by luteinizing hormone, follicle-stimulating hormone, and stage of follicle development. J Clin Endocr Metab, 2001, 86: 2531–2537 Catteau-Jonard S, Pigny P, Reyss A C, et al. Changes in serum anti-müllerian hormone level during low-dose recombinant follicular-stimulating hormone therapy for anovulation in polycystic ovary syndrome. J Clin Endocr Metab, 2007, 92: 4138–4143 Fanchin R, Schonauer L M, Righini C, et al. Serum anti-mullerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod, 2003, 18: 323–327 Ficicioglu C, Kutlu T, Baglam E, et al. Early follicular antimullerian hormone as an indicator of ovarian reserve. Fertil Steril, 2006, 85: 592–596 Visser J A, de Jong F H, Laven J S E, et al. Anti-müllerian hormone: A new marker for ovarian function. Reproduction, 2006, 131: 1–9 de Vet A, Laven J S E, de Jong F H, et al. Antimüllerian hormone serum levels: A putative marker for ovarian aging. Fertil Steril, 2002, 77: 357–362 Hagstad A, Johansson S, Wilhelmsson C, et al. Gynaecology of middle-aged women — menstrual and reproductive histories. Maturitas, 1985, 7: 99–113 van Rooij I A J, Broekmans F J M, Scheffer G J, et al. Serum antimüllerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: A longitudinal study. Fertil Steril, 2005, 83: 979–987 Fanchin R, Taieb J, Lozano D H M, et al. High reproducibility of serum anti-müllerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod, 2005, 20: 923–927 La Marca A, Sighinolfi G, Radi D, et al. Anti-müllerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update, 2010, 16: 113–130 Sowers M R, Eyvazzadeh A D, McConnell D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab, 2008, 93: 3478–3483 Groome N P, Illingworth P J, O’Brien M, et al. Detection of dimeric inhibin throughout the human menstrual cycle by two-site enzyme immunoassay. Clin Endocrinol (Oxf), 1994, 40: 717–723 Groome N P, Illingworth P J, O’Brien M, et al. Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab, 1996, 81: 1401–1405 Hall J E, Welt C K, Cramer D W. Inhibin A and inhibin B reflect ovarian function in assisted reproduction but are less useful at predicting outcome. Hum Reprod, 1999, 14: 409–415 Hartge P. Genetics of reproductive lifespan. Nat Genet, 2009, 41: 637–638 Kok H S, van Asselt K M, van der Schouw Y T, et al. Genetic studies to identify genes underlying menopausal age. Hum Reprod Update, 2005, 11: 483–493