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Journal of Assisted Reproduction and Genetics
Published in: Journal of Assisted Reproduction and Genetics 10/2018

01-10-2018 | Commentary

Ovarian manipulation in ART: going beyond physiological standards to provide best clinical outcomes

Authors: Israel Ortega, Juan A. García-Velasco, Antonio Pellicer

Published in: Journal of Assisted Reproduction and Genetics | Issue 10/2018

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Abstract

Current knowledge on ovarian physiology has challenged the traditional concept of folliculogenesis, creating the basis for novel ovarian stimulation protocols in assisted reproduction technology. The purpose of this review was to evaluate the efficacy of novel clinical interventions that could aid clinicians in individualizing their protocols to patients’ characteristics and personal situations. We conducted a literature review of the available evidence on new approaches for ovarian stimulation from both retrospective and prospective studies in the PubMed database. Here, we present some of the most important interventions, including follicle growth in the gonadotropin-independent and dependent stage, manipulation of estradiol production throughout ovarian stimulation, control of mid-cycle gonadotropin surges, and luteal phase support after different stimulation protocols and trigger agents. The latest research on IVF has moved physicians away from the classical physiology, allowing the development of new strategies to decouple organ functions from the female reproductive system and challenging the traditional concept of IVF.
Literature
1.
Abbara A, Jayasena CN, Christopoulos G, Narayanaswamy S, Izzi-Engbeaya C, Nijher GM, et al. Efficacy of Kisspeptin-54 to trigger oocyte maturation in women at high risk of ovarian hyperstimulation syndrome (OHSS) during in vitro fertilization (IVF) therapy. J Clin Endocrinol Metab. 2015;100:3322–31.CrossRefPubMedPubMedCentral
2.
Arslan M, Bocca S, Arslan EO, Duran HE, Stadtmauer L, Oehninger S. Cumulative exposure to high estradiol levels during the follicular phase of IVF cycles negatively affects implantation. J Assist Reprod Genet. 2007;24:111–7.CrossRefPubMedPubMedCentral
3.
Azim AA, Costantini-Ferrando M, Oktay K. Safety of fertility preservation by ovarian stimulation with letrozole and gonadotropins in patients with breast cancer: a prospective controlled study. J Clin Oncol. 2008;26:2630–5.CrossRefPubMed
4.
Badawy A, Sobh MA, Ahdy M, Abdelhafez MS. Bone marrow mesenchymal stem cell repair of cyclophosphamide-induced ovarian insufficiency in a mouse model. Int J Womens Health. 2017;9:441–7.CrossRefPubMedPubMedCentral
5.
Baerwald AR, Adams GP, Pierson RA. A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril. 2003;80:116–22.CrossRefPubMed
6.
Bar-Hava I, Mizrachi Y, Karfunkel-Doron D, Omer Y, Sheena L, Carmon N, et al. Intranasal gonadotropin-releasing hormone agonist (GnRHa) for luteal-phase support following GnRHa triggering, a novel approach to avoid ovarian hyperstimulation syndrome in high responders. Fertil Steril. 2016;106:330–3.CrossRefPubMed
7.
Bedoschi GM, de Albuquerque FO, Ferriani RA, Navarro PA. Ovarian stimulation during the luteal phase for fertility preservation of cancer patients: case reports and review of the literature. J Assist Reprod Genet. 2010;27:491–4.CrossRefPubMedPubMedCentral
8.
Bosch E, Labarta E, Crespo J, Simon C, Remohi J, Pellicer A. Impact of luteinizing hormone administration on gonadotropin-releasing hormone antagonist cycles: an age-adjusted analysis. Fertil Steril. 2011;95:1031–6.CrossRefPubMed
9.
Cakmak H, Katz A, Cedars MI, Rosen MP. Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril. 2013;100:1673–80.CrossRefPubMed
10.
Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril. 2011;96:277–85.CrossRefPubMed
11.
Cobo A, Meseguer M, Remohi J, Pellicer A. Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod. 2010;25:2239–46.CrossRefPubMed
12.
Cohen I, Figer A, Tepper R, Shapira J, Altaras MM, Yigael D, et al. Ovarian overstimulation and cystic formation in premenopausal tamoxifen exposure: comparison between tamoxifen-treated and nontreated breast cancer patients. Gynecol Oncol. 1999;72:202–7.CrossRefPubMed
13.
Damewood MD, Shen W, Zacur HA, Schlaff WD, Rock JA, Wallach EE. Disappearance of exogenously administered human chorionic gonadotropin. Fertil Steril. 1989;52:398–400.CrossRefPubMed
14.
De Mello Bianchi,PH, Serafini P, Monteiro da Rocha A, Assad Hassun P, Alves da Motta EL, Sampaio Baruselli P, Chada Baracat E, Follicular waves in the human ovary: a new physiological paradigm for novel ovarian stimulation protocolsReprod.Sci., 2010, 17, 12, 1067-1076I
15.
Devine K, Richter KS, Widra EA, McKeeby JL. Vitrified blastocyst transfer cycles with the use of only vaginal progesterone replacement with endometrin have inferior ongoing pregnancy rates: results from the planned interim analysis of a three-arm randomized controlled noninferiority trial. Fertil Steril. 2018;109:266–75.CrossRefPubMed
16.
Diamond MP, Tarlatzis BC, DeCherney AH. Recruitment of multiple follicular development for in vitro fertilization in the presence of a viable intrauterine pregnancy. Obstet Gynecol. 1987;70:498–9.PubMed
17.
Diedrich K, Diedrich C, Santos E, Bauer O, Zoll C, al-Hasani S, et al. Suppression of endogenous LH increase in ovarian stimulation with the GnRH antagonist cetrorelix. Geburtshilfe Frauenheilkd. 1994;54:237–40.CrossRefPubMed
18.
Diedrich K, van der Ven H, Al-Hasani S, Krebs D. Ovarian stimulation for in-vitro fertilization. Hum Reprod. 1988;3:39–44.CrossRefPubMed
19.
Doblinger J, Cometti B, Trevisan S, Griesinger G. Subcutaneous progesterone is effective and safe for luteal phase support in IVF: an individual patient data meta-analysis of the phase III trials. PLoS One. 2016;11:e0151388.CrossRefPubMedPubMedCentral
20.
Driancourt MA. Regulation of ovarian follicular dynamics in farm animals. Implications for manipulation of reproduction. Theriogenology. 2001;55:1211–39.CrossRefPubMed
21.
Eguizabal C, Montserrat N, Vassena R, Barragan M, Garreta E, Garcia-Quevedo L, et al. Complete meiosis from human induced pluripotent stem cells. Stem Cells. 2011;29:1186–95.CrossRefPubMed
22.
Fabris AM, Cruz M, Legidos V, Iglesias C, Munoz M, Garcia-Velasco JA. Dual Triggering With Gonadotropin-Releasing Hormone Agonist and Standard Dose Human Chorionic Gonadotropin in Patients With a High Immature Oocyte Rate Reprod.Sci., 2017, 24, 8, 1221–1225
23.
24.
Garzo VG, Dorrington JH. Aromatase activity in human granulosa cells during follicular development and the modulation by follicle-stimulating hormone and insulin. Am J Obstet Gynecol. 1984;148:657–62.CrossRefPubMed
25.
Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev. 1996;17:121–55.CrossRefPubMed
26.
Griffin D, Benadiva C, Kummer N, Budinetz T, Nulsen J, Engmann L. Dual trigger of oocyte maturation with gonadotropin-releasing hormone agonist and low-dose human chorionic gonadotropin to optimize live birth rates in high responders. Fertil Steril. 2012;97:1316–20.CrossRefPubMed
27.
28.
Hsueh AJ, Kawamura K, Cheng Y, Fauser BC. Intraovarian control of early folliculogenesis. Endocr Rev. 2015;36:1–24.CrossRefPubMed
29.
Humaidan P, Engmann L, Benadiva C. Luteal phase supplementation after gonadotropin-releasing hormone agonist trigger in fresh embryo transfer: the American versus European approaches. Fertil Steril. 2015;103:879–85.CrossRefPubMed
30.
31.
International Breast Cancer Study Group, Colleoni M, Gelber S, Goldhirsch A, Aebi S, Castiglione-Gertsch M, et al. Tamoxifen after adjuvant chemotherapy for premenopausal women with lymph node-positive breast cancer: international breast cancer study group trial 13-93. J Clin Oncol. 2006;24:1332–41.CrossRef
32.
Kasum M, Kurdija K, Oreskovic S, Cehic E, Pavicic-Baldani D, Skrgatic L. Combined ovulation triggering with GnRH agonist and hCG in IVF patients. Gynecol Endocrinol. 2016;32:861–5.CrossRefPubMed
33.
Kawamura K, Cheng Y, Sun YP, Zhai J, Diaz-Garcia C, Simon C, et al. Ovary transplantation: to activate or not to activate. Hum Reprod. 2015;30:2457–60.CrossRefPubMed
34.
Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A. 2013;110:17474–9.CrossRefPubMedPubMedCentral
35.
Koering MJ. Comparative morphology of the primate ovary. Contrib Primatol. 1974;3:38–81.PubMed
36.
Kol S. Luteolysis induced by a gonadotropin-releasing hormone agonist is the key to prevention of ovarian hyperstimulation syndrome. Fertil Steril. 2004;81:1–5.CrossRefPubMed
37.
Kol S, Homburg R, Alsbjerg B, Humaidan P. The gonadotropin-releasing hormone antagonist protocol--the protocol of choice for the polycystic ovary syndrome patient undergoing controlled ovarian stimulation. Acta Obstet Gynecol Scand. 2012;91:643–7.CrossRefPubMed
38.
Kol S, Humaidan P, Itskovitz-Eldor J. GnRH agonist ovulation trigger and hCG-based, progesterone-free luteal support: a proof of concept study. Hum Reprod. 2011;26:2874–7.CrossRefPubMed
39.
Kolibianakis EM, Schultze-Mosgau A, Schroer A, van Steirteghem A, Devroey P, Diedrich K, et al. A lower ongoing pregnancy rate can be expected when GnRH agonist is used for triggering final oocyte maturation instead of HCG in patients undergoing IVF with GnRH antagonists. Hum Reprod. 2005;20:2887–92.CrossRefPubMed
40.
Kuang Y, Chen Q, Fu Y, Wang Y, Hong Q, Lyu Q, et al. Medroxyprogesterone acetate is an effective oral alternative for preventing premature luteinizing hormone surges in women undergoing controlled ovarian hyperstimulation for in vitro fertilization. Fertil Steril. 2015;104:62–70.e3.CrossRefPubMed
41.
Kuang Y, Chen Q, Hong Q, Lyu Q, Ai A, Fu Y, et al. Double stimulations during the follicular and luteal phases of poor responders in IVF/ICSI programmes (Shanghai protocol). Reprod BioMed Online. 2014a;29:684–91.CrossRefPubMed
42.
Kuang Y, Hong Q, Chen Q, Lyu Q, Ai A, Fu Y, et al. Luteal-phase ovarian stimulation is feasible for producing competent oocytes in women undergoing in vitro fertilization/intracytoplasmic sperm injection treatment, with optimal pregnancy outcomes in frozen-thawed embryo transfer cycles. Fertil Steril. 2014b;101:105–11.CrossRefPubMed
43.
Kuwayama M. Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology. 2007;67:73–80.CrossRefPubMed
44.
Lamb JD, Shen S, McCulloch C, Jalalian L, Cedars MI, Rosen MP. Follicle-stimulating hormone administered at the time of human chorionic gonadotropin trigger improves oocyte developmental competence in in vitro fertilization cycles: a randomized, double-blind, placebo-controlled trial. Fertil Steril. 2011;95:1655–60.CrossRefPubMed
45.
Lin MH, Wu FS, Lee RK, Li SH, Lin SY, Hwu YM. Dual trigger with combination of gonadotropin-releasing hormone agonist and human chorionic gonadotropin significantly improves the live-birth rate for normal responders in GnRH-antagonist cycles. Fertil Steril. 2013;100:1296–302.CrossRefPubMed
46.
Madrigrano A, Westphal L, Wapnir I. Egg retrieval with cryopreservation does not delay breast cancer treatment. Am J Surg. 2007;194:477–81.CrossRefPubMed
47.
Mai Q, Hu X, Yang G, Luo Y, Huang K, Yuan Y, et al. Effect of letrozole on moderate and severe early-onset ovarian hyperstimulation syndrome in high-risk women: a prospective randomized trial. Am J Obstet Gynecol. 2017;216:42.e1–42.e10.CrossRef
48.
Martinez F, Clua E, Devesa M, Rodriguez I, Arroyo G, Gonzalez C, et al. Comparison of starting ovarian stimulation on day 2 versus day 15 of the menstrual cycle in the same oocyte donor and pregnancy rates among the corresponding recipients of vitrified oocytes. Fertil Steril. 2014;102:1307–11.CrossRefPubMed
49.
Martins WP, Ferriani RA, Navarro PA, Nastri CO. GnRH agonist during luteal phase in women undergoing assisted reproductive techniques: systematic review and meta-analysis of randomized controlled trials. Ultrasound Obstet Gynecol. 2016;47:144–51.CrossRefPubMed
50.
Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun. 2004;320:383–8.CrossRefPubMed
51.
Medrano JV, Martinez-Arroyo AM, Miguez JM, Moreno I, Martinez S, Quinonero A, et al. Human somatic cells subjected to genetic induction with six germ line-related factors display meiotic germ cell-like features. Sci Rep. 2016;6:24956.CrossRefPubMedPubMedCentral
52.
Meirow D, Raanani H, Maman E, Paluch-Shimon S, Shapira M, Cohen Y, et al. Tamoxifen co-administration during controlled ovarian hyperstimulation for in vitro fertilization in breast cancer patients increases the safety of fertility-preservation treatment strategies. Fertil Steril. 2014;102:488–495.e3.CrossRefPubMed
53.
Nakano R, Mizuno T, Kotsuji F, Katayama K, Wshio M, Tojo S. “Triggering” of ovulation after infusion of synthetic luteinizing hormone releasing factor (LRF). Acta Obstet Gynecol Scand. 1973;52:269–72.CrossRefPubMed
54.
Novella-Maestre E, Herraiz S, Rodriguez-Iglesias B, Diaz-Garcia C, Pellicer A. Short-term PTEN inhibition improves in vitro activation of primordial follicles, preserves follicular viability, and restores AMH levels in cryopreserved ovarian tissue from cancer patients. PLoS One. 2015;10:e0127786.CrossRefPubMedPubMedCentral
55.
Oktay K, Hourvitz A, Sahin G, Oktem O, Safro B, Cil A, et al. Letrozole reduces estrogen and gonadotropin exposure in women with breast cancer undergoing ovarian stimulation before chemotherapy. J Clin Endocrinol Metab. 2006;91:3885–90.CrossRefPubMed
56.
Olivennes F, Cunha-Filho JS, Fanchin R, Bouchard P, Frydman R. The use of GnRH antagonists in ovarian stimulation. Hum Reprod Update. 2002;8:279–90.CrossRefPubMed
57.
Patterson M, Murphy KG, Thompson EL, Patel S, Ghatei MA, Bloom SR. Administration of kisspeptin-54 into discrete regions of the hypothalamus potently increases plasma luteinising hormone and testosterone in male adult rats. J Neuroendocrinol. 2006;18:349–54.CrossRefPubMed
58.
Pellicer A, Simon C, Miro F, Castellvi RM, Ruiz A, Ruiz M, et al. Ovarian response and outcome of in-vitro fertilization in patients treated with gonadotrophin-releasing hormone analogues in different phases of the menstrual cycle. Hum Reprod. 1989;4:285–9.CrossRefPubMed
59.
Phillips A, Hahn DW, Klimek S, McGuire JL. A comparison of the potencies and activities of progestogens used in contraceptives. Contraception. 1987;36:181–92.CrossRefPubMed
60.
Pirard C, Donnez J, Loumaye E. GnRH agonist as novel luteal support: results of a randomized, parallel group, feasibility study using intranasal administration of buserelin. Hum Reprod. 2005;20:1798–804.CrossRefPubMed
61.
Practice Committees of American Society for Reproductive Medicine. Society for assisted reproductive technology. Mature oocyte cryopreservation: a guideline. Fertil Steril. 2013;99:37–43.CrossRef
62.
Rombauts L, Suikkari AM, MacLachlan V, Trounson AO, Healy DL. Recruitment of follicles by recombinant human follicle-stimulating hormone commencing in the luteal phase of the ovarian cycle. Fertil Steril. 1998;69:665–9.CrossRefPubMed
63.
Schally AV, Arimura A, Kastin AJ, Matsuo H, Baba Y, Redding TW, et al. Gonadotropin-releasing hormone: one polypeptide regulates secretion of luteinizing and follicle-stimulating hormones. Science. 1971;173:1036–8.CrossRefPubMed
64.
Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614–27.CrossRefPubMed
65.
Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A. 2005;102:2129–34.CrossRefPubMedPubMedCentral
66.
Shapiro BS, Andersen CY. Major drawbacks and additional benefits of agonist trigger--not ovarian hyperstimulation syndrome related. Fertil Steril. 2015;103:874–8.CrossRefPubMed
67.
Shepard MK, Balmaceda JP, Leija CG. Relationship of weight to successful induction of ovulation with clomiphene citrate. Fertil Steril. 1979;32:641–5.CrossRefPubMed
68.
Singh A, Bhandari S, Agrawal P, Gupta N, Munaganuru N. Use of clomiphene-based stimulation protocol in oocyte donors: a comparative study. J Hum Reprod Sci. 2016;9:159–63.CrossRefPubMedPubMedCentral
69.
Sirois J, Fortune JE. Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biol Reprod. 1988;39:308–17.CrossRefPubMed
70.
Sitruk-Ware R, Nath A, Mishell DR Jr. Contraception technology: past, present and future. Contraception. 2013;87:319–30.CrossRefPubMed
71.
Smitz J, Devroey P, Braeckmans P, Camus M, Khan I, Staessen C, et al. Management of failed cycles in an IVF/GIFT programme with the combination of a GnRH analogue and HMG. Hum Reprod. 1987;2:309–14.CrossRefPubMed
72.
Sonmezer M, Oktay K. Fertility preservation in young women undergoing breast cancer therapy. Oncologist. 2006;11:422–34.CrossRefPubMed
73.
Sonmezer M, Turkcuoglu I, Coskun U, Oktay K. Random-start controlled ovarian hyperstimulation for emergency fertility preservation in letrozole cycles. Fertil Steril. 2011;95:2125.e9–11.CrossRef
74.
Strickland S, Beers WH. Studies on the role of plasminogen activator in ovulation. In vitro response of granulosa cells to gonadotropins, cyclic nucleotides, and prostaglandins. J Biol Chem. 1976;251:5694–702.PubMed
75.
Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod. 2015;30:608–15.CrossRefPubMed
76.
Tan SL, Kingsland C, Campbell S, Mills C, Bradfield J, Alexander N, et al. The long protocol of administration of gonadotropin-releasing hormone agonist is superior to the short protocol for ovarian stimulation for in vitro fertilization. Fertil Steril. 1992;57:810–4.CrossRefPubMed
77.
Teramoto S, Kato O. Minimal ovarian stimulation with clomiphene citrate: a large-scale retrospective study. Reprod BioMed Online. 2007;15:134–48.CrossRefPubMed
78.
Tesarik J, Hazout A, Mendoza-Tesarik R, Mendoza N, Mendoza C. Beneficial effect of luteal-phase GnRH agonist administration on embryo implantation after ICSI in both GnRH agonist- and antagonist-treated ovarian stimulation cycles. Hum Reprod. 2006;21:2572–9.CrossRefPubMed
79.
Toftager M, Bogstad J, Bryndorf T, Lossl K, Roskaer J, Holland T, et al. Risk of severe ovarian hyperstimulation syndrome in GnRH antagonist versus GnRH agonist protocol: RCT including 1050 first IVF/ICSI cycles. Hum Reprod. 2016;31:1253–64.CrossRefPubMed
80.
Trounson AO, Leeton JF, Wood C, Webb J, Wood J. Pregnancies in humans by fertilization in vitro and embryo transfer in the controlled ovulatory cycle. Science. 1981;212:681–2.CrossRefPubMed
81.
Ubaldi FM, Capalbo A, Vaiarelli A, Cimadomo D, Colamaria S, Alviggi C, et al. Follicular versus luteal phase ovarian stimulation during the same menstrual cycle (DuoStim) in a reduced ovarian reserve population results in a similar euploid blastocyst formation rate: new insight in ovarian reserve exploitation. Fertil Steril. 2016;105:1488–1495.e1.CrossRefPubMed
82.
Villasante A, Pacheco A, Ruiz A, Pellicer A, Garcia-Velasco JA. Vascular endothelial cadherin regulates vascular permeability: implications for ovarian hyperstimulation syndrome. J Clin Endocrinol Metab. 2007;92:314–21.CrossRefPubMed
83.
von Wolff M, Capp E, Jauckus J, Strowitzki T, Germeyer A. FertiPROTEKT study group. Timing of ovarian stimulation in patients prior to gonadotoxic therapy: an analysis of 684 stimulations. Eur J Obstet Gynecol Reprod Biol. 2016;199:146–9.CrossRef
84.
von Wolff M, Thaler CJ, Frambach T, Zeeb C, Lawrenz B, Popovici RM, et al. Ovarian stimulation to cryopreserve fertilized oocytes in cancer patients can be started in the luteal phase. Fertil Steril. 2009;92:1360–5.CrossRef
85.
Wang Y, Chen Q, Wang N, Chen H, Lyu Q, Kuang Y. Controlled ovarian stimulation using medroxyprogesterone acetate and hMG in patients with polycystic ovary syndrome treated for IVF: a double-blind randomized crossover clinical trial. Medicine (Baltimore). 2016;95:e2939.CrossRef
86.
Wu Z, Li R, Ma Y, Deng B, Zhang X, Meng Y, et al. Effect of HCG-day serum progesterone and oestradiol concentrations on pregnancy outcomes in GnRH agonist cycles. Reprod BioMed Online. 2012;24:511–20.CrossRefPubMed
87.
Xu B, Li Y. Flexible ovarian stimulation in a poor responder: a case report and literature review. Reprod BioMed Online. 2013;26:378–83.CrossRefPubMed
88.
Yen SS, Llerena O, Little B, Pearson OH. Disappearance rates of endogenous luteinizing hormone and chorionic gonadotropin in man. J Clin Endocrinol Metab. 1968;28:1763–7.CrossRefPubMed
89.
Zalmon I, Carvalho G, Ferreira CA. Induction of ovulation with a new drug: clomiphene citrate. Hospital (Rio J). 1965;67:1249–54.
90.
91.
Zelinski-Wooten MB, Hutchison JS, Hess DL, Wolf DP, Stouffer RL. A bolus of recombinant human follicle stimulating hormone at midcycle induces periovulatory events following multiple follicular development in macaques. Hum Reprod. 1998;13:554–60.CrossRefPubMed
92.
Zelinski-Wooten MB, Hutchison JS, Hess DL, Wolf DP, Stouffer RL. Follicle stimulating hormone alone supports follicle growth and oocyte development in gonadotrophin-releasing hormone antagonist-treated monkeys. Hum Reprod. 1995;10:1658–66.CrossRefPubMed
93.
Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients. J Clin Endocrinol Metab. 2016;101:4405–12.CrossRefPubMedPubMedCentral
94.
Zhu X, Ye H, Fu Y. The Utrogestan and hMG protocol in patients with polycystic ovarian syndrome undergoing controlled ovarian hyperstimulation during IVF/ICSI treatments. Medicine (Baltimore). 2016;95:e4193.CrossRef
95.
Zhu X, Zhang X, Fu Y. Utrogestan as an effective oral alternative for preventing premature luteinizing hormone surges in women undergoing controlled ovarian hyperstimulation for in vitro fertilization. Medicine (Baltimore). 2015;94:e909.CrossRef
96.
Zorn JR, Boyer P, Guichard A. Never on a Sunday: programming for IVF-ET and GIFT. Lancet. 1987;1:385–6.CrossRefPubMed
Metadata
Title
Ovarian manipulation in ART: going beyond physiological standards to provide best clinical outcomes
Authors
Israel Ortega
Juan A. García-Velasco
Antonio Pellicer
Publication date
01-10-2018
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 10/2018
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-018-1258-6

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