Luteal phase support with human chorionic gonadotropin in assisted reproductive technology

References

• Sherman BM, Korenman SG. Hormonal characteristics of the human menstrual cycle throughout reproductive life. J. Clin. Invest. 55(4), 699–706 (1975).
   PubMed Web of Science ®Google Scholar
• Fatemi HM, Popovic-Todorovic B, Papanikolaou E, Donoso P, Devroey P. An update of luteal phase support in stimulated IVF cycles. Hum. Reprod. Update 13(6), 581–590 (2007).
   PubMed Web of Science ®Google Scholar
• Devoto L, Fuentes A, Kohen P et al. The human corpus luteum: life cycle and function in natural cycles. Fertil. Steril. 92(3), 1067–1079 (2009).
   PubMed Web of Science ®Google Scholar
• Fritz MA, McLachlan RI, Cohen NL, Dahl KD, Bremner WJ, Soules MR. Onset and characteristics of the midcycle surge in bioactive and immunoactive luteinizing hormone secretion in normal women: influence of physiological variations in periovulatory ovarian steroid hormone secretion. J. Clin. Endocrinol. Metab. 75(2), 489–493 (1992).
   PubMed Web of Science ®Google Scholar
• Devoto L, Kohen P, Muñoz A, Strauss JF 3rd. Human corpus luteum physiology and the luteal-phase dysfunction associated with ovarian stimulation. Reprod. Biomed. Online 18(Suppl. 2), 19–24 (2009).
   PubMed Web of Science ®Google Scholar
• Messinis IE, Messini CI, Dafopoulos K. Luteal-phase endocrinology. Reprod. Biomed. Online 19(Suppl. 4), 4314 (2009).
   PubMedGoogle Scholar
• Jones GS. Luteal phase defect: a review of pathophysiology. Curr. Opin. Obstet. Gynecol. 3(5), 641–648 (1991).
   PubMed Web of Science ®Google Scholar
• Jordan J, Craig K, Clifton DK, Soules MR. Luteal phase defect: the sensitivity and specificity of diagnostic methods in common clinical use. Fertil. Steril. 62(1), 54–62 (1994).
   PubMed Web of Science ®Google Scholar
• Hazzard TM, Christenson LK, Stouffer RL. Changes in expression of vascular endothelial growth factor and angiopoietin-1 and -2 in the macaque corpus luteum during the menstrual cycle. Mol. Hum. Reprod. 6(11), 993–998 (2000).
   PubMed Web of Science ®Google Scholar
• Fraser HM, Wilson H, Wulff C, Rudge JS, Wiegand SJ. Administration of vascular endothelial growth factor Trap during the ‘post-angiogenic’ period of the luteal phase causes rapid functional luteolysis and selective endothelial cell death in the marmoset. Reproduction 132(4), 589–600 (2006).
   PubMed Web of Science ®Google Scholar
• Duncan WC, Gay E, Maybin JA. The effect of human chorionic gonadotrophin on the expression of progesterone receptors in human luteal cells in vivo and in vitro. Reproduction 130(1), 83–93 (2005).
   PubMed Web of Science ®Google Scholar
• Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N. Engl. J. Med. 340(23), 1796–1799 (1999).
   PubMed Web of Science ®Google Scholar
• Huhtaniemi IT, Catt KJ. Differential binding affinities of rat testis luteinizing hormone (LH) receptors for human chorionic gonadotropin, human LH, and ovine LH. Endocrinology 108(5), 1931–1938 (1981).
   PubMed Web of Science ®Google Scholar
• Pal R, Singh O. Absence of corpus luteum rescue by chorionic gonadotropin in women immunized with a contraceptive vaccine. Fertil. Steril. 76(2), 332–336 (2001).
   PubMed Web of Science ®Google Scholar
• Kohen P, Castro O, Palomino A et al. The steroidogenic response and corpus luteum expression of the steroidogenic acute regulatory protein after human chorionic gonadotropin administration at different times in the human luteal phase. J. Clin. Endocrinol. Metab. 88(7), 3421–3430 (2003).
   PubMed Web of Science ®Google Scholar
• Sugino N, Okuda K. Species-related differences in the mechanism of apoptosis during structural luteolysis. J. Reprod. Dev. 53(5), 977–986 (2007).
   PubMed Web of Science ®Google Scholar
• Shi QJ, Lei ZM, Rao CV, Lin J. Novel role of human chorionic gonadotropin in differentiation of human cytotrophoblasts. Endocrinology 132(3), 1387–1395 (1993).
   PubMed Web of Science ®Google Scholar
• Reshef E, Lei ZM, Rao CV, Pridham DD, Chegini N, Luborsky JL. The presence of gonadotropin receptors in nonpregnant human uterus, human placenta, fetal membranes, and decidua. J. Clin. Endocrinol. Metab. 70(2), 421–430 (1990).
   PubMed Web of Science ®Google Scholar
• Licht P, Russu V, Wildt L. On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial microenvironment: implications for differentiation and implantation. Semin. Reprod. Med. 19(1), 37–47 (2001).
   PubMed Web of Science ®Google Scholar
• Licht P, Fluhr H, Neuwinger J, Wallwiener D, Wildt L. Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol. Cell. Endocrinol. 269(1–2), 85–92 (2007).
   PubMed Web of Science ®Google Scholar
• Rogers PA, Milne BJ, Trounson AO. A model to show human uterine receptivity and embryo viability following ovarian stimulation for in vitro fertilization. J. In Vitro Fert. Embryo Transf. 3(2), 93–98 (1986).
   PubMedGoogle Scholar
• Balasch J, Jové I, Márquez M, Vanrell JA. Hormonal and histological evaluation of the luteal phase after combined GnRH-agonist/gonadotrophin treatment for superovulation and luteal phase support in in-vitro fertilization. Hum. Reprod. 6(7), 914–917 (1991).
   PubMed Web of Science ®Google Scholar
• Bourgain C, Ubaldi F, Tavaniotou A, Smitz J, Van Steirteghem AC, Devroey P. Endometrial hormone receptors and proliferation index in the periovulatory phase of stimulated embryo transfer cycles in comparison with natural cycles and relation to clinical pregnancy outcome. Fertil. Steril. 78(2), 237–244 (2002).
   PubMed Web of Science ®Google Scholar
• Papanikolaou EG, Bourgain C, Fatemi H et al. Endometrial advancement after triggering with recombinant or urinary HCG: a randomized controlled pilot study. Reprod. Biomed. Online 21(1), 50–55 (2010).
   PubMed Web of Science ®Google Scholar
• Strowitzki T, Germeyer A, Popovici R, von Wolff M. The human endometrium as a fertility-determining factor. Hum. Reprod. Update 12(5), 617–630 (2006).
   PubMed Web of Science ®Google Scholar
• Gambino LS, Wreford NG, Bertram JF, Dockery P, Lederman F, Rogers PA. Angiogenesis occurs by vessel elongation in proliferative phase human endometrium. Hum. Reprod. 17(5), 1199–1206 (2002).
   PubMed Web of Science ®Google Scholar
• Tavaniotou A, Smitz J, Bourgain C, Devroey P. Ovulation induction disrupts luteal phase function. Ann. NY Acad. Sci. 943, 55–63 (2001).
   PubMed Web of Science ®Google Scholar
• Hutchinson-Williams KA, Lunenfeld B, Diamond MP, Lavy G, Boyers SP, DeCherney AH. Human chorionic gonadotropin, estradiol, and progesterone profiles in conception and nonconception cycles in an in vitro fertilization program. Fertil. Steril. 52(3), 441–445 (1989).
   PubMed Web of Science ®Google Scholar
• DeCherney AH, Tarlatzis BC, Laufer N. Follicular development: lessons learned from human in vitro fertilization. Am. J. Obstet. Gynecol. 153(8), 911–923 (1985).
   PubMed Web of Science ®Google Scholar
• Hayden C. GnRH analogues: applications in assisted reproductive techniques. Eur. J. Endocrinol. 159(Suppl. 1), S17–S25 (2008).
   PubMed Web of Science ®Google Scholar
• Fauser BC, Devroey P. Reproductive biology and IVF: ovarian stimulation and luteal phase consequences. Trends Endocrinol. Metab. 14(5), 236–242 (2003).
   PubMed Web of Science ®Google Scholar
• Penzias AS. Luteal phase support. Fertil. Steril. 77(2), 318–323 (2002).
   PubMed Web of Science ®Google Scholar
• Pabuccu R, Akar ME. Luteal phase support in assisted reproductive technology. Curr. Opin. Obstet. Gynecol. 17(3), 277–281 (2005).
   PubMed Web of Science ®Google Scholar
• Hutchinson-Williams KA, DeCherney AH, Lavy G, Diamond MP, Naftolin F, Lunenfeld B. Luteal rescue in in vitro fertilization-embryo transfer. Fertil. Steril. 53(3), 495–501 (1990).
   PubMed Web of Science ®Google Scholar
• Nader S, Berkowitz AS, Ochs D, Held B, Winkel CA. Luteal-phase support in stimulated cycles in an in vitro fertilization/embryo transfer program: progesterone versus human chorionic gonadotropin. J. In Vitro Fert. Embryo Transf. 5(2), 81–84 (1988).
   PubMedGoogle Scholar
• Buvat J, Marcolin G, Guittard C, Herbaut JC, Louvet AL, Dehaene JL. Luteal support after luteinizing hormone-releasing hormone agonist for in vitro fertilization: superiority of human chorionic gonadotropin over oral progesterone. Fertil. Steril. 53(3), 490–494 (1990).
   PubMed Web of Science ®Google Scholar
• Mahadevan MM, Leader A, Taylor PK. Effect of low-dose human chorionic gonadotropin on corpus luteum function after embryo transfer. J. In Vitro.Fert. Embryo. Transf. 2(4), 190–194 (1985).
   PubMedGoogle Scholar
• Balasch J, Creus M, Fábregues F et al. Hormonal profiles in successful and unsuccessful implantation in IVF-ET after combined GnRH agonist/gonadotropin treatment for superovulation and hCG luteal support. Gynecol. Endocrinol. 9(1), 51–58 (1995).
   PubMed Web of Science ®Google Scholar
• Smith EM, Anthony FW, Gadd SC, Masson GM. Trial of support treatment with human chorionic gonadotrophin in the luteal phase after treatment with buserelin and human menopausal gonadotrophin in women taking part in an in vitro fertilisation programme. BMJ 298(6686), 1483–1486 (1989).
   PubMedGoogle Scholar
• Belaisch-Allart J, De Mouzon J, Lapousterle C, Mayer M. The effect of HCG supplementation after combined GnRH agonist/HMG treatment in an IVF programme. Hum. Reprod. 5(2), 163–166 (1990).
   PubMed Web of Science ®Google Scholar
• Soliman S, Daya S, Collins J, Hughes EG. The role of luteal phase support in infertility treatment: a meta-analysis of randomized trials. Fertil. Steril. 61(6), 1068–1076 (1994).
   PubMed Web of Science ®Google Scholar
• Pritts EA, Atwood AK. Luteal phase support in infertility treatment: a meta-analysis of the randomized trials. Hum. Reprod. 17(9), 2287–2299 (2002).
   PubMed Web of Science ®Google Scholar
• van der Linden M, Buckingham K, Farquhar C, Kremer JA, Metwally M. Luteal phase support for assisted reproduction cycles. Cochrane Database Syst. Rev. 10, CD009154 (2011).
   PubMed Web of Science ®Google Scholar
• Cohlen BJ. Should luteal support be introduced in ovarian stimulation/IUI programmes? An evidence-based review. Reprod. Biomed. Online. 19(Suppl. 4), 32–38 (2009).
   Google Scholar
• Erdem A, Erdem M, Atmaca S, Guler I. Impact of luteal phase support on pregnancy rates in intrauterine insemination cycles: a prospective randomized study. Fertil. Steril. 91(6), 2508–2513 (2009).
   PubMed Web of Science ®Google Scholar
• Montville CP, Khabbaz M, Aubuchon M, Williams DB, Thomas MA. Luteal support with intravaginal progesterone increases clinical pregnancy rates in women with polycystic ovary syndrome using letrozole for ovulation induction. Fertil. Steril. 94(2), 678–683 (2010).
   PubMed Web of Science ®Google Scholar
• Kyrou D, Fatemi HM, Tournaye H, Devroey P. Luteal phase support in normo-ovulatory women stimulated with clomiphene citrate for intrauterine insemination: need or habit? Hum. Reprod. 25(10), 2501–2506 (2010).
   PubMed Web of Science ®Google Scholar
• Keenan JA, Moghissi KS. Luteal phase support with hCG does not improve fecundity rate in human menopausal gonadotropin-stimulated cycles. Obstet. Gynecol. 79(6), 983–987 (1992).
   PubMed Web of Science ®Google Scholar
• Papanikolaou EG, Humaidan P, Polyzos N et al. New algorithm for OHSS prevention. Reprod. Biol. Endocrinol. 9, 147 (2011).
   PubMed Web of Science ®Google Scholar
• Tay PY, Lenton EA. The optimum time for exogenous human chorionic gonadotropin to rescue the corpus luteum. J. Assist. Reprod. Genet. 16(9), 495–499 (1999).
   PubMed Web of Science ®Google Scholar
• Stovall DW, Van Voorhis BJ, Sparks AE, Adams LM, Syrop CH. Selective early elimination of luteal support in assisted reproduction cycles using a gonadotropin-releasing hormone agonist during ovarian stimulation. Fertil. Steril. 70(6), 1056–1062 (1998).
   PubMed Web of Science ®Google Scholar
• Tesarik J, Hazout A, Mendoza C. Luteinizing hormone affects uterine receptivity independently of ovarian function. Reprod. Biomed. Online 7(1), 59–64 (2003).
   PubMedGoogle Scholar
• Youssef MA, Van der Veen F, Al-Inany HG et al. Gonadotropin-releasing hormone agonist versus HCG for oocyte triggering in antagonist assisted reproductive technology cycles. Cochrane Database Syst. Rev. 1, CD008046 (2011).
   Google Scholar
• Kol S, Humaidan P. GnRH agonist triggering: recent developments. Reprod. Biomed. Online 26(3), 226–230 (2013).
   PubMed Web of Science ®Google Scholar
• Humaidan P, Ejdrup Bredkjaer H, Westergaard LG, Yding Andersen C. 1,500 IU human chorionic gonadotropin administered at oocyte retrieval rescues the luteal phase when gonadotropin-releasing hormone agonist is used for ovulation induction: a prospective, randomized, controlled study. Fertil. Steril. 93(3), 847–854 (2010).
   PubMed Web of Science ®Google Scholar
• 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. 26(10), 2874–2877 (2011).
   PubMed Web of Science ®Google Scholar
• Radesic B, Tremellen K. Oocyte maturation employing a GnRH agonist in combination with low-dose hCG luteal rescue minimizes the severity of ovarian hyperstimulation syndrome while maintaining excellent pregnancy rates. Hum. Reprod. 26(12), 3437–3442 (2011).
   PubMed Web of Science ®Google Scholar
• Mansour R, Tawab N, Kamal O et al. Intrauterine injection of human chorionic gonadotropin before embryo transfer significantly improves the implantation and pregnancy rates in in vitro fertilization/intracytoplasmic sperm injection: a prospective randomized study. Fertil. Steril. 96(6), 1370–1374.e1 (2011).
   PubMed Web of Science ®Google Scholar
• Yovich JL, Stanger JD, Yovich JM, Tuvik AI. Assessment and hormonal treatment of the luteal phase of in vitro fertilization cycles. Aust. N. Z. J. Obstet. Gynaecol. 24(2), 125–130 (1984).
   PubMed Web of Science ®Google Scholar
• Smitz J, Devroey P, Camus M et al. The luteal phase and early pregnancy after combined GnRH-agonist/HMG treatment for superovulation in IVF or GIFT. Hum. Reprod. 3(5), 585–590 (1988).
   PubMed Web of Science ®Google Scholar
• Van Steirteghem AC, Smitz J, Camus M et al. The luteal phase after in-vitro fertilization and related procedures. Hum. Reprod. 3(2), 161–164 (1988).
   PubMed Web of Science ®Google Scholar
• Kupferminc MJ, Lessing JB, Amit A, Yovel I, David MP, Peyser MR. A prospective randomized trial of human chorionic gonadotrophin or dydrogesterone support following in-vitro fertilization and embryo transfer. Hum. Reprod. 5(3), 271–273 (1990).
   PubMed Web of Science ®Google Scholar
• Albert JL, Pfeifer M. Luteal phase hormone levels after in vitro fertilization and embryo transfer (IVF-ET): A prospective randomized trial of human chorionic gonadotropin (HCG) vs intramuscular (IM) progesterone (P) for luteal phase support following stimulation with gonadotropin-releasing hormone agonist (GnRH-a) and human menopausal gonadotropins (HMG). Fertil. Steril. 56, S18 (1991).
   Google Scholar
• Claman P, Domingo M, Leader A. Luteal phase support in in-vitro fertilization using gonadotrophin releasing hormone analogue before ovarian stimulation: a prospective randomized study of human chorionic gonadotrophin versus intramuscular progesterone. Hum. Reprod. 7(4), 487–489 (1992).
   PubMed Web of Science ®Google Scholar
• Golan A, Herman A, Soffer Y, Bukovsky I, Caspi E, Ron-El R. Human chorionic gonadotrophin is a better luteal support than progesterone in ultrashort gonadotrophin-releasing hormone agonist/menotrophin in-vitro fertilization cycles. Hum. Reprod. 8(9), 1372–1375 (1993).
   PubMed Web of Science ®Google Scholar
• Araujo E Jr, Bernardini L, Frederick JL, Asch RH, Balmaceda JP. Prospective randomized comparison of human chorionic gonadotropin versus intramuscular progesterone for luteal-phase support in assisted reproduction. J. Assist. Reprod. Genet. 11(2), 74–78 (1994).
   PubMed Web of Science ®Google Scholar
• Herman A, Raziel A, Strassburger D, Soffer Y, Bukovsky I, Ron-El R. The benefits of mid-luteal addition of human chorionic gonadotrophin in in-vitro fertilization using a down-regulation protocol and luteal support with progesterone. Hum. Reprod. 11(7), 1552–1557 (1996).
   PubMed Web of Science ®Google Scholar
• Mochtar MH, Hogerzeil HV, Mol BW. Progesterone alone versus progesterone combined with HCG as luteal support in GnRHa/HMG induced IVF cycles: a randomized clinical trial. Hum. Reprod. 11(8), 1602–1605 (1996).
   PubMed Web of Science ®Google Scholar
• Artini PG, Volpe A, Angioni S, Galassi MC, Battaglia C, Genazzani AR. A comparative, randomized study of three different progesterone support of the luteal phase following IVF/ET program. J. Endocrinol. Invest. 18(1), 51–56 (1995).
   PubMed Web of Science ®Google Scholar
• Martinez F, Coroleu B, Parera N et al. Human chorionic gonadotropin and intravaginal natural progesterone are equally effective for luteal phase support in IVF. Gynecol. Endocrinol. 14(5), 316–320 (2000).
   PubMed Web of Science ®Google Scholar
• Ludwig M, Finas A, Katalinic A et al. Prospective, randomized study to evaluate the success rates using hCG, vaginal progesterone or a combination of both for luteal phase support. Acta Obstet. Gynecol. Scand. 80(6), 574–582 (2001).
   PubMed Web of Science ®Google Scholar
• Ugur M, Yenicesu O, Ozcan S, Keles G, Gokmen O. A prospective randomized study comparing hCG, vaginal micronized progesterone and a combination regimen for luteal phase support in an in-vitro fertilization programme. Fertil. Steril. 76(3), S118 (2001).
   Google Scholar
• Vimpeli T, Tinkanen H, Huhtala H, Rönnberg L, Kujansuu E. Salivary and serum progesterone concentrations during two luteal support regimens used in in vitro fertilization treatment. Fertil. Steril. 76(4), 847–848 (2001).
   PubMed Web of Science ®Google Scholar
• Fujimoto A, Osuga Y, Fujiwara T et al. Human chorionic gonadotropin combined with progesterone for luteal support improves pregnancy rate in patients with low late-midluteal estradiol levels in IVF cycles. J. Assist. Reprod. Genet. 19(12), 550–554 (2002).
   PubMed Web of Science ®Google Scholar
• Lam PM, Cheung MC, Cheung LP, Lok HI, Haines CJ. Effects of early luteal-phase vaginal progesterone supplementation on the outcome of in vitro fertilization and embryo transfer. Gynecol. Endocrin. 24(12), 674–680 (2008).
   PubMed Web of Science ®Google Scholar
• Ghanem ME, Sadek EE, Elboghdady LA et al. The effect of luteal phase support protocol on cycle outcome and luteal phase hormone profile in long agonist protocol intracytoplasmic sperm injection cycles: a randomized clinical trial. Fertil. Steril. 92(2), 486–493 (2009).
   PubMed Web of Science ®Google Scholar
• Var T, Tonguc EA, Doganay M, Gulerman C, Gungor T, Mollamahmutoglu L. A comparison of the effects of three different luteal phase support protocols on in vitro fertilization outcomes: a randomized clinical trial. Fertil. Steril. 95(3), 985–989 (2011).
   PubMed Web of Science ®Google Scholar
• Mahadevan MM, Leader A, Taylor PJ. Effects of low-dose human chorionic gonadotropin on corpus luteum function after embryo transfer. J. In Vitro Fert. Embryo Transf. 2(4), 190–194 (1985).
   PubMedGoogle Scholar
• Baber RJ, Kuan R, Porter RN, Saunders DM. Early pregnancy support in an in vitro fertilization program: does human chorionic gonadotropin reduce the miscarriage rate? Asia. Oceania. J. Obstet. Gynaecol. 14(4), 453–455 (1988).
   PubMedGoogle Scholar
• Buvat J, Marcolin G, Herbaut JC, Dehaene JL, Verbecq P, Fourlinnie JC. A randomized trial of human chorionic gonadotropin support following in vitro fertilization and embryo transfer. Fertil. Steril. 49(3), 458–461 (1988).
   PubMed Web of Science ®Google Scholar
• Herman A, Ron-El R, Golan A, Raziel A, Soffer Y, Caspi E. Pregnancy rate and ovarian hyperstimulation after luteal human chorionic gonadotropin in in vitro fertilization stimulated with gonadotropin-releasing hormone analog and menotropins. Fertil. Steril. 53(1), 92–96 (1990).
   PubMed Web of Science ®Google Scholar
• Beckers NG, Laven JS, Eijkemans MJ, Fauser BC. Follicular and luteal phase characteristics following early cessation of gonadotrophin-releasing hormone agonist during ovarian stimulation for in-vitro fertilization. Hum. Reprod. 15(1), 43–49 (2000).
   PubMed Web of Science ®Google Scholar