The use of androgens or androgen-modulating agents in poor responders undergoing in vitro fertilization: A systematic review and meta-analysis

Human Reproduction Update

Volumn 18, Issue 2, 2012, Pages 127-145

  Bosdou, J K ^a   Venetis, C A ^a   Kolibianakis, E M ^a   Toulis, K A ^a   Goulis, D G ^a   Zepiridis, L ^a   Tarlatzis, B C ^a  

^a ARISTOTLE UNIVERSITY MEDICAL SCHOOL   (Greece)

Author keywords

Androgens; Aromatase inhibitors; Poor response; Recombinant human chorionic gonadotrophin; Recombinant luteinizing hormone

Indexed keywords

ANDROGEN; FOLLITROPIN; GONADORELIN AGONIST; GONADORELIN ANTAGONIST; LETROZOLE; PRASTERONE; RECOMBINANT CHORIONIC GONADOTROPIN; RECOMBINANT LUTEINIZING HORMONE; TESTOSTERONE;

ARTICLE; ATTRIBUTABLE RISK; BIRTH RATE; DATA BASE; EMBASE; FERTILIZATION IN VITRO; HUMAN; LIVE BIRTH; MEDLINE; META ANALYSIS; PREGNANCY OUTCOME; PREGNANCY RATE; PREMEDICATION; PRIORITY JOURNAL; PROBABILITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); TREATMENT OUTCOME; TREATMENT RESPONSE;

EID: 84857537209     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmr051     Document Type: Article

References (56)

1. Balasch J, Fabregues F, Penarrubia J, Carmona F, Casamitjana R, Creus M, Manau D, Casals G, Vanrell JA. Pretreatment with transdermal testosterone may improve ovarian response to gonadotrophins in poor-responder IVF patients with normal basal concentrations of FSH. Hum Reprod 2006; 7:1884-1893.
2. Barrenetxea G, Agirregoikoa JA, Jimenez MR, de Larruzea AL, 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;3:546-553.
3. Ben-Rafael Z, Bider D, Dan U, Zolti M, Levran D, Mashiach S. Combined gonadotropin releasing hormone agonist/human menopausal gonadotropin therapy (GnRH-a/hMG) in normal, high, and poor responders to hMG. J In Vitro Fert Embryo Transf 1991;1:33-36.
4. Berkkanoglu M, Isikoglu M, Aydin D, Ozgur K. Clinical effects of ovulation induction with recombinant follicle-stimulating hormone supplemented with recombinant luteinizing hormone or low-dose recombinant human chorionic gonadotropin in the midfollicular phase in microdose cycles in poor responders. Fertil Steril 2007;3:665-669.
5. Biljan MM, Hemmings R, Brassard N. The outcome of 150 babies following the treatment with letrozole or letrozole and gonadotropins. Fertil Steril 2005; 84(Suppl. 1):S95-S95.
6. Brahman LE. Confidence intervals assess both clinical significance and statistical significance. Ann Int Med 1991;6:515.
7. Casson PR, Lindsay MS, Pisarska MD, Carson SA, Buster JE. Dehydroepiandrosterone supplementation augments ovarian stimulation in poor responders: a case series. Hum Reprod 2000;10:2129-2132.
8. Demirol A, Gurgan T, Girgin B. Supplementation of rec LH for poor responder patients in ART. Hum Reprod 2005;20(Suppl. 1):i74.
9. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 3:177-188.
10. Durnerin CI, Erb K, Fleming R, Hillier H, Hillier SG, Howles CM, Hugues JN, Lass A, Lyall H, Rasmussen P et al. Effects of recombinant LH treatment on folliculogenesis and responsiveness to FSH stimulation. Hum Reprod 2008;2:421-426.
11. Fabregues F, Penarrubia J, Creus M, Manau D, Casals G, Carmona F, Balasch J. Transdermal testosterone may improve ovarian response to gonadotrophins in low-responder IVF patients: a randomized, clinical trial. Hum Reprod 2009; 2:349-359.
12. Fernández Ramírez MJ, Monzó A, García-Gimeno T, Rubio JM, Montañana V, Duque C, Herrero G, Romeu DA. Role of LH administration during the follicullar phase in women with risk of low response in ovarian stimulation with FSH and cetrorelix for IVF. Rev Iberoamer Fertil 2006;5:281-290.
13. 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;6:1521-1526.
14. Ferraretti AP, La Marca A, Fauser BC, Tarlatzis B, Nargund G, Gianaroli L. ESHRE consensus on the definition of 'poor response' to ovarian stimulation for in vitro fertilization: the Bologna criteria. Hum Reprod 2011;26:1616-1624.
15. Ferrari B, Barusi L, Coppola F. Clinical and endocrine effects of ovulation induction with FSH and hCG supplementation in low responders in the midfollicular phase. A pilot study. J Reprod Med 2002;2:137-143.
16. Filicori M, Cognigni GE, Tabarelli C, Pocognoli P, Taraborrelli S, Spettoli D, Ciampaglia W. Stimulation and growth of antral ovarian follicles by selective LH activity administration in women. J Clin Endocrinol Metab 2002;3:1156-1161.
17. Filicori M, Cognigni GE, Gamberini E, Parmegiani L, Troilo E, Roset B. Efficacy of low-dose human chorionic gonadotropin alone to complete controlled ovarian stimulation. Fertil Steril 2005;2:394-401.
18. Frattarelli JL, Peterson EH. Effect of androgen levels on in vitro fertilization cycles. Fertil Steril 2004;6:1713-1714.
19. Futterweit W, Deligdisch L. Histopathological effects of exogenously administered testosterone in 19 female to male transsexuals. J Clin Endocrinol Metab 1986; 1:16-21.
20. Goswami SK, Das T, Chattopadhyay R, Sawhney V, Kumar J, Chaudhury K, Chakravarty BN, Kabir SN. A randomized single-blind controlled trial of letrozole as a low-cost IVF protocol in women with poor ovarian response: a preliminary report. Hum Reprod 2004;9:2031-2035.
21. Harbord RM, Egger M, Sterne JA. A modified test for small-study effects in meta-analyses of controlled trials with binary endpoints. Stat Med 2006; 20:3443-3457.
22. Harlow CR, Hillier SG, Hodges JK. Androgen modulation of follicle-stimulating hormone-induced granulosa cell steroidogenesis in the primate ovary. Endocrinology 1986;3:1403-1405.
23. Hedges LV, Olkin I. Statistical Methods for Meta-Analysis. New York USA: Academic Press, 1985.
24. Hillier SG, De Zwart FA. Evidence that granulosa cell aromatase induction/activation by follicle-stimulating hormone is an androgen receptor-regulated process in-vitro. Endocrinology 1981;4:1303-1305.
25. Hillier SG, Whitelaw PF, Smyth CD. Follicular oestrogen synthesis: the 'two-cell, two-gonadotrophin' model revisited. Mol Cell Endocrinol 1994;1-2:51-54.
26. Hillier SG, Tetsuka M, Fraser HM. Location and developmental regulation of androgen receptor in primate ovary. Hum Reprod 1997;1:107-111.
27. Hugues JN, Durnerin IC. Impact of androgens on fertility - physiological, clinical and therapeutic aspects. Reprod Biomed Online 2005;5:570-580.
28. Humaidan P, Bungum L, Bungum M, Andersen CY. Ovarian response and pregnancy outcome related to mid-follicular LH levels in women undergoing assisted reproduction with GnRH agonist down-regulation and recombinant FSH stimulation. Hum Reprod 2002;8:2016-2021.
29. 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;6:635-643.
30. Jenkins JM, Davies DW, Devonport H, Anthony FW, Gadd SC, Watson RH, Masson GM. Comparison of 'poor' responders with 'good' responders using a standard buserelin/human menopausal gonadotrophin regime for in-vitro fertilization. Hum Reprod 1991;7:918-921.
31. Kashyap S, Wells G, Davis O, Williams-Pittman MA, Rosenwaks Z. Aromatase inhibitors improve IVF outcomes in poor responders: A randomized controlled pilot study. J Soc Gyn Invest 2005;2:709.
32. Kim CH, Howles CM, Lee HA. The effect of transdermal testosterone gel pretreatment on controlled ovarian stimulation and IVF outcome in low responders. Fertil Steril 2011;2:679-683.
33. Kolibianakis EM, Venetis CA, Diedrich K, Tarlatzis BC, Griesinger G. Addition of growth hormone to gonadotrophins in ovarian stimulation of poor responders treated by in-vitro fertilization: a systematic review and meta-analysis. Hum Reprod Update 2009;6:613-622.
34. Kroboth PD, Salek FS, Pittenger AL, Fabian TJ, Frye RF. DHEA and DHEA-S: a review. J Clin Pharmacol 1999;4:327-348.
35. Kyrou D, Kolibianakis EM, Venetis CA, Papanikolaou EG, Bontis J, Tarlatzis BC.Howto improve the probability of pregnancy in poor responders undergoing in vitro fertilization: a systematic review and meta-analysis. Fertil Steril 2009;3:749-766.
36. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959;4:719-748.
37. Massin N, Cedrin-Durnerin I, Coussieu C, Galey-Fontaine J, Wolf JP, Hugues JN. Effects of transdermal testosterone application on the ovarian response to FSH in poor responders undergoing assisted reproduction technique-a prospective, randomized, double-blind study. Hum Reprod 2006;5:1204-1211.
38. Mitwally MF, Casper RF. Aromatase inhibition improves ovarian response to FSH: a potential option for low responders during ovarian stimulation. Fertil Steril 2001; 4(Supplement 1):S8-S9.
39. Mitwally MF, Casper RF. Aromatase inhibition improves ovarian response to follicle-stimulating hormone in poor responders. Fertil Steril 2002;4:776-780.
40. Mochtar MH, Van der V, Ziech M, van Wely M. Recombinant Luteinizing Hormone (rLH) for controlled ovarian hyperstimulation in assisted reproductive cycles. Cochrane Database Syst Rev (Online) 2007;2:CD005070.
41. O'Brien PC, Shampo MA. Statistical considerations for performing multiple tests in a single experiment. 4. Performing multiple statistical tests on the same data. Mayo Clin Proc 1988;10:1043-1045.
42. Ozmen B, Sonmezer M, Atabekoglu CS, Olmus H. Use of aromatase inhibitors in poor-responder patients receiving GnRH antagonist protocols. Reprod Biomed Online 2009;4:478-485.
43. Polidoropoulos N, Papanikopoulos C, Stefanis P, Tavaniotou M, Argyrou M, Doriza S, Sisi V, Karamalegos C, Moschopoulou M, Karagianni T et al. Addition of exogenous recombinant LH in poor responders protocols: does it really help? Hum Reprod 2007;2007;22(Suppl. 1):i4.
44. 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;3:542-546.
45. Spinder T, Spijkstra JJ, van den Tweel JG, Burger CW, van Kessel H, Hompes PG, Gooren LJ. The effects of long term testosterone administration on pulsatile luteinizing hormone secretion and on ovarian histology in eugonadal female to male transsexual subjects. J Clin Endocrinol Metab 1989;1:151-157.
46. Sunkara SK, Pundir J, Khalaf Y. Effect of androgen supplementation or modulation on ovarian stimulation outcome in poor responders: a meta-analysis. Reprod Biomed Online 2011;6:545-555.
47. Surrey ES, Schoolcraft WB. Evaluating strategies for improving ovarian response of the poor responder undergoing assisted reproductive techniques. Fertil Steril 2000;4:667-676.
48. Tarlatzis BC, Zepiridis L, Grimbizis G, Bontis J. Clinical management of low ovarian response to stimulation for IVF: a systematic review. Hum Reprod Update 2003; 1:61-76.
49. Tulandi T, Martin J, Al-Fadhli R, Kabli N, Forman R, Hitkari J, Librach C, Greenblatt E, Casper RF. Congenital malformations among 911 newborns conceived after infertility treatment with letrozole or clomiphene citrate. Fertil Steril 2006;6:1761-1765.
50. Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest 1998; 12:2622-2629.
51. Vendola K, Zhou J, Wang J, Famuyiwa OA, Bievre M, Bondy CA. Androgens promote oocyte insulin-like growth factor I expression and initiation of follicle development in the primate ovary. Biol Reprod 1999;2:353-357.
52. Venetis CA, Kolibianakis EM, Tarlatzi TB, Tarlatzis BC. Evidence-based management of poor ovarian response. Ann N Y Acad Sci 2010;1205:199-206.
53. Weil SJ, Vendola K, Zhou J, Adesanya OO, Wang J, Okafor J, Bondy CA. Androgen receptor gene expression in the primate ovary: cellular localization, regulation, and functional correlations. J Clin Endocrinol Metab 1998;7:2479-2485.
54. Weil S, Vendola K, Zhou J, Bondy CA. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. J Clin Endocrinol Metab 1999;8:2951-2956.
55. Westergaard LG, Laursen SB, Andersen CY. Increased risk of early pregnancy loss by profound suppression of luteinizing hormone during ovarian stimulation in normogonadotrophic women undergoing assisted reproduction. Hum Reprod 2000;5:1003-1008.
56. Wiser A, Gonen O, Ghetler Y, Shavit T, Berkovitz A, Shulman A. Addition of dehydroepiandrosterone (DHEA) for poor-responder patients before and during IVF treatment improves the pregnancy rate: a randomized prospective study. Hum Reprod 2010;10:2496-2500.