Biological versus chronological ovarian age: Implications for assisted reproductive technology

Reproductive Biology and Endocrinology

Volumn 7, Issue , 2009, Pages 101-

  Alviggi, Carlo ^a   Humaidan, Peter ^b   Howles, Colin M ^c   Tredway, Donald ^d   Hillier, Stephen G ^e  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b SKIVE REGIONAL HOSPITAL   (Denmark)

^c MERCK SERONO S A   (Switzerland)

^d EMD SERONO INC   (United States)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; GONADORELIN AGONIST; GONADORELIN ANTAGONIST; GONADORELIN DERIVATIVE; GROWTH HORMONE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LUTEINIZING HORMONE; MUELLERIAN INHIBITING FACTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RECOMBINANT LUTEINIZING HORMONE; SOMATOMEDIN C;

AGING; CHROMOSOME ABERRATION; CLINICAL TRIAL; DRUG DOSE INCREASE; ENDOMETRIOSIS; ENVIRONMENTAL FACTOR; FEMALE INFERTILITY; FEMALE SUBFERTILITY; FERTILIZATION IN VITRO; GRANULOSA CELL; HUMAN; INFERTILITY THERAPY; MATERNAL AGE; MENOPAUSE; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OOCYTE RETRIEVAL; OVARIAN RESERVE; OVARY FOLLICLE DEVELOPMENT; OVARY INSUFFICIENCY; OVULATION INDUCTION; PREGNANCY OUTCOME; PREGNANCY RATE; PROGNOSIS; REPRODUCTIVE SUCCESS; REVIEW; THECA CELL; TREATMENT OUTCOME;

AGING; CELL AGING; FEMALE; HUMANS; MATERNAL AGE; MODELS, BIOLOGICAL; OOGENESIS; OVARY; PREGNANCY; REPRODUCTIVE TECHNIQUES, ASSISTED; TIME FACTORS;

EID: 70449516637     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-7-101     Document Type: Review

References (144)

1. Balasch J. Investigation of the infertile couple: investigation of the infertile couple in the era of assisted reproductive technology: a time for reappraisal. Hum Reprod 2000, 15:2251-2257.
2. Leridon H. Can assisted reproduction technology compensate for the natural decline in fertility with age? A model assessment. Hum Reprod 2004, 19:1548-1553.
3. te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update 2002, 8:141-154.
4. Steptoe PC, Edwards RG. Birth after the reimplantation of a human embryo. Lancet 1978, 2:366.
5. Steptoe PC, Edwards RG, Walters DE. Observations on 767 clinical pregnancies and 500 births after human in-vitro fertilization. Hum Reprod 1986, 1:89-94.
6. Menken J, Trussell J, Larsen U. Age and infertility. Science 1986, 233:1389-1394.
7. ESHRE Capri Workshop Group Fertility and ageing. Hum Reprod Update 2005, 11:261-276.
8. Menken J, Larsen U. Fertility rates and aging. Aging, Reproduction and the Climacteric 1986, 147-166. New York: Plenum Press, Mastronianni L, Paulsen A.
9. A long term analysis of the HFEA Register data 1991-2006. , http://www.hfea.gov.uk/en/1540.html
10. Howles CM, Kim CH, Elder K. Treatment strategies in assisted reproduction for women of advanced maternal age. Int Surg 2006, 91:S37-S54.
11. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000, 21:200-214.
12. Lobo RA. Early ovarian ageing: a hypothesis. What is early ovarian ageing?. Hum Reprod 2003, 18:1762-1764.
13. Perez GI, Robles R, Knudson CM, Flaws JA, Korsmeyer SJ, Tilly JL. Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet 1999, 21:200-203.
14. Hillier SG. Current concepts of the roles of follicle stimulating hormone and luteinizing hormone in folliculogenesis. Hum Reprod 1994, 9:188-191.
15. Hillier SG, Whitelaw PF, Smyth CD. Follicular oestrogen synthesis: the 'two-cell, two-gonadotrophin' model revisited. Mol Cell Endocrinol 1994, 100:51-54.
16. Faddy MJ, Gosden RG. A model conforming the decline in follicle numbers to the age of menopause in women. Hum Reprod 1996, 11:1484-1486.
17. Eppig JJ, Chesnel F, Hirao Y, O'Brien MJ, Pendola FL, Watanabe S, Wigglesworth K. Oocyte control of granulosa cell development: how and why. Hum Reprod 1997, 12:127-132.
18. Hirshfield AN. Comparison of granulosa cell proliferation in small follicles of hypophysectomized, prepubertal, and mature rats. Biol Reprod 1985, 32:979-987.
19. Klein NA, Soules MR. Endocrine changes of the perimenopause. Clin Obstet Gynecol 1998, 41:912-920.
20. Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, Grunfeld L. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 1991, 337:1375-1377.
21. te Velde ER, Scheffer GJ, Dorland M, Broekmans FJ, Fauser BC. Developmental and endocrine aspects of normal ovarian aging. Mol Cell Endocrinol 1998, 145:67-73.
22. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod 1992, 7:1342-1346.
23. Gosden RG, Faddy MJ. Ovarian aging, follicular depletion, and steroidogenesis. Exp Gerontol 1994, 29:265-274.
24. Nikolaou D, Templeton A. Early ovarian ageing: a hypothesis. Detection and clinical relevance. Hum Reprod 2003, 18:1137-1139.
25. Gougeon A, Ecochard R, Thalabard JC. 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.
26. Gregory SJ, Kaiser UB. Regulation of gonadotropins by inhibin and activin. Semin Reprod Med 2004, 22:253-267.
27. Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002, 124:601-609.
28. Beemsterboer SN, Homburg R, Gorter NA, Schats R, Hompes PG, Lambalk CB. The paradox of declining fertility but increasing twinning rates with advancing maternal age. Hum Reprod 2006, 21:1531-1532.
29. Faddy MJ, Gosden RG, Edwards RG. Ovarian follicle dynamics in mice: a comparative study of three inbred strains and an F1 hybrid. J Endocrinol 1983, 96:23-33.
30. den Tonkelaar I, te Velde ER, Looman CW. Menstrual cycle length preceding menopause in relation to age at menopause. Maturitas 1998, 29:115-123.
31. Farhi J, Homburg R, Ferber A, Orvieto R, Ben RZ. Non-response to ovarian stimulation in normogonadotrophic, normogonadal women: a clinical sign of impending onset of ovarian failure pre-empting the rise in basal follicle stimulating hormone levels. Hum Reprod 1997, 12:241-243.
32. de Boer EJ, den Tonkelaar I, te Velde ER, Burger CW, Klip H, van Leeuwen FE. A low number of retrieved oocytes at in vitro fertilization treatment is predictive of early menopause. Fertil Steril 2002, 77:978-985.
33. Nikolaou D, Lavery S, Turner C, Margara R, Trew G. Is there a link between an extremely poor response to ovarian hyperstimulation and early ovarian failure?. Hum Reprod 2002, 17:1106-1111.
34. Lawson R, El-Toukhy T, Kassab A, Taylor A, Braude P, Parsons J, Seed P. Poor response to ovulation induction is a stronger predictor of early menopause than elevated basal FSH: a life table analysis. Hum Reprod 2003, 18:527-533.
35. Treloar AE. Menstrual cyclicity and the pre-menopause. Maturitas 1981, 3:249-264.
36. van Noord PA, Dubas JS, Dorland M, Boersma H, te Velde E. Age at natural menopause in a population-based screening cohort: the role of menarche, fecundity, and lifestyle factors. Fertil Steril 1997, 68:95-102.
37. Santoro N, Brown JR, Adel T, Skurnick JH. Characterization of reproductive hormonal dynamics in the perimenopause. J Clin Endocrinol Metab 1996, 81:1495-1501.
38. Soules MR, Sherman S, Parrott E, Rebar R, Santoro N, Utian W, Woods N. Executive summary: Stages of Reproductive Aging Workshop (STRAW). Fertil Steril 2001, 76:874-878.
39. Freeman EW, Sammel MD, Gracia CR, Kapoor S, Lin H, Liu L, Nelson DB. Follicular phase hormone levels and menstrual bleeding status in the approach to menopause. Fertil Steril 2005, 83:383-392.
40. Hall Moran V, Leathard HL, Coley J. Urinary hormone levels during the natural menstrual cycle: the effect of age. J Endocrinol 2001, 170:157-164.
41. Piltonen T, Koivunen R, Ruokonen A, Tapanainen JS. Ovarian age-related responsiveness to human chorionic gonadotropin. J Clin Endocrinol Metab 2003, 88:3327-3332.
42. Ferrell RJ, O'Connor KA, Holman DJ, Brindle E, Miller RC, Rodriguez G, Simon JA, Mansfield PK, Wood JW, Weinstein M. Monitoring reproductive aging in a 5-year prospective study: aggregate and individual changes in luteinizing hormone and follicle-stimulating hormone with age. Menopause 2007, 14:29-37.
43. Akande VA, Fleming CF, Hunt LP, Keay SD, Jenkins JM. Biological versus chronological ageing of oocytes, distinguishable by raised FSH levels in relation to the success of IVF treatment. Hum Reprod 2002, 17:2003-2008.
44. Santoro N. Mechanisms of premature ovarian failure. Ann Endocrinol (Paris) 2003, 64:87-92.
45. De Leener A, Montanelli L, Van Durme J, Chae H, Smits G, Vassart G, Costagliola S. Presence and absence of follicle-stimulating hormone receptor mutations provide some insights into spontaneous ovarian hyperstimulation syndrome physiopathology. J Clin Endocrinol Metab 2006, 91:555-562.
46. Danilovich N, Javeshghani D, Xing W, Sairam MR. Endocrine alterations and signaling changes associated with declining ovarian function and advanced biological aging in follicle-stimulating hormone receptor haploinsufficient mice. Biol Reprod 2002, 67:370-378.
47. Danilovich N, Sairam MR. Haploinsufficiency of the follicle-stimulating hormone receptor accelerates oocyte loss inducing early reproductive senescence and biological aging in mice. Biol Reprod 2002, 67:361-369.
48. May-Panloup P, Chretien MF, Jacques C, Vasseur C, Malthiery Y, Reynier P. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod 2005, 20:593-597.
49. Munne S, Alikani M, Tomkin G, Grifo J, Cohen J. Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil Steril 1995, 64:382-391.
50. Munne S, Chen S, Fischer J, Colls P, Zheng X, Stevens J, Escudero T, Oter M, Schoolcraft B, Simpson JL, Cohen J. Preimplantation genetic diagnosis reduces pregnancy loss in women aged 35 years and older with a history of recurrent miscarriages. Fertil Steril 2005, 84:331-335.
51. Wilding M, De Placido G, De Matteo L, Marino M, Alviggi C, Dale B. Chaotic mosaicism in human preimplantation embryos is correlated with a low mitochondrial membrane potential. Fertil Steril 2003, 79:340-346.
52. Greb RR, Grieshaber K, Gromoll J, Sonntag B, Nieschlag E, Kiesel L, Simoni M. A common single nucleotide polymorphism in exon 10 of the human follicle stimulating hormone receptor is a major determinant of length and hormonal dynamics of the menstrual cycle. J Clin Endocrinol Metab 2005, 90:4866-4872.
53. Perez Mayorga M, Gromoll J, Behre HM, Gassner C, Nieschlag E, Simoni M. Ovarian response to follicle-stimulating hormone (FSH) stimulation depends on the FSH receptor genotype. J Clin Endocrinol Metab 2000, 85:3365-3369.
54. Haavisto AM, Pettersson K, Bergendahl M, Virkamaki A, Huhtaniemi I. Occurrence and biological properties of a common genetic variant of luteinizing hormone. J Clin Endocrinol Metab 1995, 80:1257-1263.
55. Alviggi C, Clarizia R, Pettersson K, Mollo A, Humaidan P, Strina I, Coppola M, Ranieri A, D'Uva M, De Placido G. Suboptimal response to GnRHa long protocol is associated with a common LH polymorphism. Reprod Biomed Online 2009, 18:9-14.
56. Takahashi K, Ozaki T, Okada M, Kurioka H, Kanasaki H, Miyazaki K. Increased prevalence of luteinizing hormone beta-subunit variant in patients with premature ovarian failure. Fertil Steril 1999, 71:96-101.
57. Takahashi K, Kurioka H, Ozaki T, Kanasaki H, Kohsaka M, Miyazaki K, Karino K. Increased prevalence of luteinizing hormone beta-subunit variant in Japanese infertility patients. Hum Reprod 1998, 13:3338-3344.
58. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL, Lan ZJ, Cooney AJ, Huhtaniemi I, Liu K. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008, 319:611-613.
59. Zofkova I, Hill M, Zajickova K. Association of C/T polymorphism in the LRP5 gene with circulating follicle stimulating hormone in Caucasian postmenopausal women. Physiol Res 2007, 56:735-739.
60. Islam MN, Islam MM. Biological and behavioural determinants of fertility in Bangladesh: 1975-1989. Asia Pac Popul J 1993, 8:3-18.
61. Rahman MM, Islam MN, Islam MM. Users of traditional methods of contraception in Bangladesh: 1981-91. J Biosoc Sci 1996, 28:257-264.
62. Hossain MB. Barkat-e-Khuda Fertility decline in Bangladesh: toward an understanding of major causes. Health Transit Rev 1996, 6(Suppl):155-167.
63. Baird DD, Tylavsky FA, Anderson JJB. Do vegetarians have earlier menopause?. Am J Epidemiol 1998, 1:907-908.
64. Freour T, Masson D, Mirallie S, Jean M, Bach K, Dejoie T, Barriere P. Active smoking compromises IVF outcome and affects ovarian reserve. Reprod Biomed Online 2008, 16:96-102.
65. Soares SR, Melo MA. Cigarette smoking and reproductive function. Curr Opin Obstet Gynecol 2008, 20:281-291.
66. Matikainen T, Perez GI, Jurisicova A, Pru JK, Schlezinger JJ, Ryu HY, Laine J, Sakai T, Korsmeyer SJ, Casper RF, Sherr DH, Tilly JL. Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals. Nat Genet 2001, 28:355-360.
67. Meirow D, Nugent D. The effects of radiotherapy and chemotherapy on female reproduction. Hum Reprod Update 2001, 7:535-543.
68. Donnez J, Martinez-Madrid B, Jadoul P, Van Langendonckt A, Demylle D, Dolmans MM. Ovarian tissue cryopreservation and transplantation: a review. Hum Reprod Update 2006, 12:519-535.
69. Himelstein-Braw R, Peters H, Faber M. Morphological study of the ovaries of leukaemic children. Br J Cancer 1978, 38:82-87.
70. Chapman RM, Sutcliffe SB, Malpas JS. Cytotoxic-induced ovarian failure in women with Hodgkin's disease. I. Hormone function. JAMA 1979, 242:1877-1881.
71. Marcello MF, Nuciforo G, Romeo R, Di Dino G, Russo I, Russo A, Palumbo G, Schiliro G. Structural and ultrastructural study of the ovary in childhood leukemia after successful treatment. Cancer 1990, 66:2099-2104.
72. Familiari G, Caggiati A, Nottola SA, Ermini M, Di Benedetto MR, Motta PM. Ultrastructure of human ovarian primordial follicles after combination chemotherapy for Hodgkin's disease. Hum Reprod 1993, 8:2080-2087.
73. Practice Committee of the American Society for Reproductive Medicine Endometriosis and infertility. Fertil Steril 2006, 86:S156-S160.
74. Speroff L, Fritz MA. Clinical Gynecologic Endocrinology and Infertility 2004, Lippincott Williams & Wilkins.
75. Jacobson TZ, Barlow DH, Koninckx PR, Olive D, Farquhar C. Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev 2002, CD001398.
76. Somigliana E, Vercellini P, Vigano P, Ragni G, Crosignani PG. Should endometriomas be treated before IVF-ICSI cycles?. Hum Reprod Update 2006, 12:57-64.
77. Garcia-Velasco JA, Somigliana E. Management of endometriomas in women requiring IVF: to touch or not to touch. Hum Reprod 2009, 24:496-501.
78. Weissman A, Howles CM. Treatment strategies in assisted reproduction for the low responder patient. Textbook of Assisted Reproductive Techniques 2008, Informa Healthcare, Gardener E, Weissman A, Howles CM, Shoham Z, 3.
79. Templeton A, Morris JK, Parslow W. Factors that affect outcome of in-vitro fertilisation treatment. Lancet 1996, 348:1402-1406.
80. van Kooij RJ, Looman CW, Habbema JD, Dorland M, te Velde ER. Age-dependent decrease in embryo implantation rate after in vitro fertilization. Fertil Steril 1996, 66:769-775.
81. Abdalla HI, Burton G, Kirkland A, Johnson MR, Leonard T, Brooks AA, Studd JW. Age, pregnancy and miscarriage: uterine versus ovarian factors. Hum Reprod 1993, 8:1512-1517.
82. de Boer EJ, den Tonkelaar I, te Velde ER, Burger CW, van Leeuwen FE. Increased risk of early menopausal transition and natural menopause after poor response at first IVF treatment. Hum Reprod 2003, 18:1544-1552.
83. Sharif K, Elgendy M, Lashen H, Afnan M. Age and basal follicle stimulating hormone as predictors of in vitro fertilisation outcome. Br J Obstet Gynaecol 1998, 105:107-112.
84. Pruksananonda K, Boonkasemsanti W, Virutamasen P. Basal follicle--stimulating hormone levels on day 3 of previous cycle are predictive of in vitro fertilization outcome. J Med Assoc Thai 1996, 79:365-369.
85. Scott RT, Toner JP, Muasher SJ, Oehninger S, Robinson S, Rosenwaks Z. Follicle-stimulating hormone levels on cycle day 3 are predictive of in vitro fertilization outcome. Fertil Steril 1989, 51:651-654.
86. Abdalla H, Thum MY. An elevated basal FSH reflects a quantitative rather than qualitative decline of the ovarian reserve. Hum Reprod 2004, 19:893-898.
87. Klinkert ER, Broekmans FJ, Looman CW, Habbema JD, te Velde ER. Expected poor responders on the basis of an antral follicle count do not benefit from a higher starting dose of gonadotrophins in IVF treatment: a randomized controlled trial. Hum Reprod 2005, 20:611-615.
88. Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update 2006, 12:685-718.
89. Klinkert ER, Broekmans FJ, Looman CW, Habbema JD, te Velde ER. The antral follicle count is a better marker than basal follicle-stimulating hormone for the selection of older patients with acceptable pregnancy prospects after in vitro fertilization. Fertil Steril 2005, 83:811-814.
90. Nahum R, Shifren JL, Chang Y, Leykin L, Isaacson K, Toth TL. Antral follicle assessment as a tool for predicting outcome in IVF--is it a better predictor than age and FSH?. J Assist Reprod Genet 2001, 18:151-155.
91. Hansen KR, Morris JL, Thyer AC, Soules MR. Reproductive aging and variability in the ovarian antral follicle count: application in the clinical setting. Fertil Steril 2003, 80:577-583.
92. Bancsi LF, Broekmans FJ, Looman CW, Habbema JD, te Velde ER. Impact of repeated antral follicle counts on the prediction of poor ovarian response in women undergoing in vitro fertilization. Fertil Steril 2004, 81:35-41.
93. Lawson R, El-Toukhy T, Kassab A, Taylor A, Braude P, Parsons J, Seed P. Poor response to ovulation induction is a stronger predictor of early menopause than elevated basal FSH: a life table analysis. Hum Reprod 2003, 18:527-533.
94. de Vet A, Laven JS, de Jong FH, Themmen AP, Fauser BC. Antimullerian hormone serum levels: a putative marker for ovarian aging. Fertil Steril 2002, 77:357-362.
95. Fanchin R, Schonauer LM, Righini C, Guibourdenche J, Frydman R, Taieb J. 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.
96. van Rooij I, Broekmans FJ, te Velde ER, Fauser BC, Bancsi LF, de Jong FH, Themmen AP. Serum anti-Mullerian hormone levels: a novel measure of ovarian reserve. Hum Reprod 2002, 17:3065-3071.
97. van Roijen JH, Ooms MP, Weber RF, Brinkmann AO, Grootegoed JA, Vreeburg JT. Comparison of the response of rat testis and accessory sex organs to treatment with testosterone and the synthetic androgen methyltrienolone (R1881). J Androl 1997, 18:51-61.
98. Ficicioglu C, Kutlu T, Baglam E, Bakacak Z. Early follicular antimullerian hormone as an indicator of ovarian reserve. Fertil Steril 2006, 85:592-596.
99. Nelson SM, Yates RW, Fleming R. Serum anti-Mullerian hormone and FSH: prediction of live birth and extremes of response in stimulated cycles--implications for individualization of therapy. Hum Reprod 2007, 22:2414-2421.
100. Sowers MR, Eyvazzadeh AD, McConnell D, Yosef M, Jannausch ML, Zhang D, Harlow S, Randolph JF. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab 2008, 93:3478-3483.
101. Nelson SM, Yates RW, Lyall H, Jamieson M, Traynor I, Gaudoin M, Mitchell P, Ambrose P, Fleming R. Anti-Mullerian hormone-based approach to controlled ovarian stimulation for assisted conception. Hum Reprod 2009, 24:867-875.
102. Fevold HL. Synergism of follicle stimulating and luteinizing hormones in producing estrogen secretion. Endocrinology 1941, 28:33-36.
103. Erickson GF, Wang C, Hsueh AJ. FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature 1979, 279:336-338.
104. Filicori M, Cognigni GE, Pocognoli P, Ciampaglia W, Bernardi S. Current concepts and novel applications of LH activity in ovarian stimulation. Trends Endocrinol Metab 2003, 14:267-273.
105. Shima K, Kitayama S, Nakano R. Gonadotropin binding sites in human ovarian follicles and corpora lutea during the menstrual cycle. Obstet Gynecol 1987, 69:800-806.
106. Huang ZH, Clayton PE, Brady G, Morris ID. Insulin-like growth factor-I gene expression in human granulosa-lutein cells. J Mol Endocrinol 1994, 12:283-291.
107. Zhou J, Bondy C. Anatomy of the human ovarian insulin-like growth factor system. Biol Reprod 1993, 48:467-482.
108. Zeleznik AJ, Hillier SG. The role of gonadotropins in the selection of the preovulatory follicle. Clin Obstet Gynecol 1984, 27:927-940.
109. Fabregues F, Creus M, Penarrubia J, Manau D, Vanrell JA, Balasch J. Effects of recombinant human luteinizing hormone supplementation on ovarian stimulation and the implantation rate in down-regulated women of advanced reproductive age. Fertil Steril 2006, 85:925-931.
110. Kolibianakis EM, Kalogeropoulou L, Griesinger G, Papanikolaou EG, Papadimas J, Bontis J, Tarlatzis BC. Among patients treated with FSH and GnRH analogues for in vitro fertilization, is the addition of recombinant LH associated with the probability of live birth? A systematic review and meta-analysis. Hum Reprod Update 2007, 13:445-452.
111. Barrenetxea G, Agirregoikoa JA, Jimenez MR, Lopez de Larruzea A, Ganzabal T, Carbonero K. Ovarian response and pregnancy outcome in poor-responder women: a randomized controlled trial on the effect of luteinizing hormone supplementation on in vitro fertilization cycles. Fertil Steril 2008, 89:546-553.
112. Humaidan P, Bungum M, Bungum L, Yding Andersen C. Effects of recombinant LH supplementation in women undergoing assisted reproduction with GnRH agonist down-regulation and stimulation with recombinant FSH: an opening study. Reprod Biomed Online 2004, 8:635-643.
113. Marrs R, Meldrum D, Muasher S, Schoolcraft W, Werlin L, Kelly E. Randomized trial to compare the effect of recombinant human FSH (follitropin alfa) with or without recombinant human LH in women undergoing assisted reproduction treatment. Reprod Biomed Online 2004, 8:175-182.
114. Bosch E, Labarta E, Simón C, Remohi J, Pellicer A. The impact of luteinizing hormone supplementation in gonadotropin releasing hormone antagonist cycles. An age adjusted randomized trial. Fertil Steril 2008, 90:S41.
115. De Placido G, Mollo A, Clarizia R, Strina I, Conforti S, Alviggi C. Gonadotropin-releasing hormone (GnRH) antagonist plus recombinant luteinizing hormone vs. a standard GnRH agonist short protocol in patients at risk for poor ovarian response. Fertil Steril 2006, 85:247-250.
116. Mochtar MH, van der Veen F, Ziech M, van Wely M. Recombinant luteinizing hormone (rLH) for controlled ovarian hyperstimulation in assisted reproductive cycles. Cochrane Database Syst Rev 2007, CD005070.
117. Ferraretti AP, Gianaroli L, Magli MC, D'Angelo A, Farfalli V, Montanaro N. Exogenous luteinizing hormone in controlled ovarian hyperstimulation for assisted reproduction techniques. Fertil Steril 2004, 82:1521-1526.
118. De Placido G, Alviggi C, Perino A, Strina I, Lisi F, Fasolino A, De Palo R, Ranieri A, Colacurci N, Mollo A. Recombinant human LH supplementation versus recombinant human FSH (rFSH) step-up protocol during controlled ovarian stimulation in normogonadotrophic women with initial inadequate ovarian response to rFSH. A multicentre, prospective, randomized controlled trial. Hum Reprod 2005, 20:390-396.
119. Lisi F, Rinaldi L, Fishel S, Caserta D, Lisi R, Campbell A. Evaluation of two doses of recombinant luteinizing hormone supplementation in an unselected group of women undergoing follicular stimulation for in vitro fertilization. Fertil Steril 2005, 83:309-315.
120. De Placido G, Mollo A, Alviggi C, Strina I, Varricchio MT, Ranieri A, Colacurci N, Tolino A, Wilding M. Rescue of IVF cycles by HMG in pituitary down-regulated normogonadotrophic young women characterized by a poor initial response to recombinant FSH. Hum Reprod 2001, 16:1875-1879.
121. De Placido G, Alviggi C, Mollo A, Strina I, Ranieri A, Alviggi E, Wilding M, Varricchio MT, Borrelli AL, Conforti S. Effects of recombinant LH (rLH) supplementation during controlled ovarian hyperstimulation (COH) in normogonadotrophic women with an initial inadequate response to recombinant FSH (rFSH) after pituitary downregulation. Clin Endocrinol (Oxf) 2004, 60:637-643.
122. Ruvolo G, Bosco L, Pane A, Morici G, Cittadini E, Roccheri MC. Lower apoptosis rate in human cumulus cells after administration of recombinant luteinizing hormone to women undergoing ovarian stimulation for in vitro fertilization procedures. Fertil Steril 2007, 87:542-546.
123. Abir R, Garor R, Felz C, Nitke S, Krissi H, Fisch B. Growth hormone and its receptor in human ovaries from fetuses and adults. Fertil Steril 2008, 90:1333-1339.
124. Ménézo YJ, el Mouatassim S, Chavrier M, Servy EJ, Nicolet B. Human oocytes and preimplantation embryos express mRNA for growth hormone receptor. Zygote 2003, 11:293-297.
125. Mendoza C, Cremades N, Ruiz-Requena E, Martinez F, Ortega E, Bernabeu S, Tesarik J. Relationship between fertilization results after intracytoplasmic sperm injection, and intrafollicular steroid, pituitary hormone and cytokine concentrations. Hum Reprod 1999, 14:628-635.
126. Izadyar F, Van Tol HT, Hage WG, Bevers MM. Preimplantation bovine embryos express mRNA of growth hormone receptor and respond to growth hormone addition during in vitro development. Mol Reprod Dev 2000, 57:247-255.
127. Kolle S, Stojkovic M, Boie G, Wolf E, Sinowatz F. Growth hormone inhibits apoptosis in in vitro produced bovine embryos. Mol Reprod Dev 2002, 61:180-186.
128. Kucuk T, Kozinoglu H, Kaba A. Growth hormone co-treatment within a GnRH agonist long protocol in patients with poor ovarian response: a prospective, randomized, clinical trial. J Assist Reprod Genet 2008, 25:123-127.
129. Ménézo YJ, Nicollet B, Rollet J, Hazout A. Pregnancy and delivery after in vitro maturation of naked ICSI-GV oocytes with GH and transfer of a frozen thawed blastocyst: case report. J Assist Reprod Genet 2006, 23:47-49.
130. Ménézo YJ, Jacquet J, Girard A, Chouteau J, Nicollet B, Servy E. In vitro maturation of human oocytes with growth hormone. Fertil Steril 2003, 80:277.
131. Owen EJ, Shoham Z, Mason BA, Ostergaard H, Jacobs HS. Cotreatment with growth hormone, after pituitary suppression, for ovarian stimulation in in vitro fertilization: a randomized, double-blind, placebo-control trial. Fertil Steril 1991, 56:1104-1110.
132. Shoham Z, Homburg R, Owen EJ, Conway GS, Ostergaard H, Jacobs HS. The role of treatment with growth hormone in infertile patients. Baillieres Clin Obstet Gynaecol 1992, 6:267-281.
133. Adashi EY, Resnick CE, Hurwitz A, Ricciarelli E, Hernandez ER, Roberts CT, Leroith D, Rosenfeld R. Insulin-like growth factors: the ovarian connection. Hum Reprod 1991, 6:1213-1219.
134. Adashi EY, Resnick CE, Hernandez ER, Hurwitz A, Roberts CT, Leroith D, Rosenfeld R. Insulin-like growth factor I as an intraovarian regulator: basic and clinical implications. Ann N Y Acad Sci 1991, 626:161-168.
135. Howles CM, Loumaye E, Germond M, Yates R, Brinsden P, Healy D, Bonaventura LM, Strowitzki T. Does growth hormone-releasing factor assist follicular development in poor responder patients undergoing ovarian stimulation for in-vitro fertilization?. Hum Reprod 1999, 14:1939-1943.
136. Suikkari A, Maclachlan V, Koistinen R, Seppala M, Healy D. Double-blind placebo controlled study: human biosynthetic growth hormone for assisted reproductive technology. Fertil Steril 1996, 65:800-805.
137. Shaker AG, Fleming R, Jamieson ME, Yates RW, Coutts JR. Absence of effect of adjuvant growth hormone therapy on follicular responses to exogenous gonadotropins in women: normal and poor responders. Fertil Steril 1992, 58:919-923.
138. Hughes SM, Huang ZH, Morris ID, Matson PL, Buck P, Lieberman BA. A double-blind cross-over controlled study to evaluate the effect of human biosynthetic growth hormone on ovarian stimulation in previous poor responders to in-vitro fertilization. Hum Reprod 1994, 9:13-18.
139. Dor J, Seidman DS, Amudai E, Bider D, Levran D, Mashiach S. Adjuvant growth hormone therapy in poor responders to in-vitro fertilization: a prospective randomized placebo-controlled double-blind study. Hum Reprod 1995, 10:40-43.
140. Younis JS, Simon A, Koren R, Dorembus D, Schenker JG, Laufer N. The effect of growth hormone supplementation on in vitro fertilization outcome: a prospective randomized placebo-controlled double-blind study. Fertil Steril 1992, 58:575-580.
141. Kotarba D, Kotarba J, Hughes E. Growth hormone for in vitro fertilization. Cochrane Database Syst Rev 2000, CD000099.
142. Tesarik J, Hazout A, Mendoza C. Improvement of delivery and live birth rates after ICSI in women aged >40 years by ovarian co-stimulation with growth hormone. Hum Reprod 2005, 20:2536-2541.
143. Kyrou D, Kolibianakis EM, Venetis CA, Papanikolaou EG, Bontis J, Tarlatzis BC. How to improve the probability of pregnancy in poor responders undergoing in vitro fertilization: a systematic review and meta-analysis. Fertil Steril 2009, 91:749-766.
144. Zhuang GL, Wong SX, Zhou CQ. The effect of co-administration of low dosage growth hormone and gonadotropin for ovarian hyperstimulation in vitro fertilization and embryo transfer. Zhonghua Fu Chan Ke Za Zhi 1994, 29:471-4, 510.