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The Early Luteal Phase Administration of Estrogen and Progesterone Does European Journal of Endocrinology (2006) 155 355–363 ISSN 0804-4643 CLINICAL STUDY The early luteal phase administration of estrogen and progesterone does not induce premature luteolysis in normo-ovulatory women Nicole G M Beckers1, Peter Platteau4, Marinus J Eijkemans2, Nicholas S Macklon5, Frank H de Jong3, Paul Devroey4 and Bart C J M Fauser5 1Division of Reproductive Medicine, Department of Obstetrics and Gynecology, 2Department of Public Health and 3Department of Medicine, Erasmus MC University Medical Center, Dr Molewaterplein 40, 3015 GD Rotterdam, The Netherlands, 4Center for Reproductive Medicine, Dutch-Speaking Brussels Free University Brussels, Laarbeeklaan 101, 1090, Brussels, Belgium and 5Department of Reproductive Medicine and Gynecology, University Medical Center, Hiedelberglaan 100, 3584 CX, Utrecht, The Netherlands (Correspondence should be addressed to N G M Beckers; Email: [email protected]) Abstract Objective: The luteal phase after ovarian hyperstimulation for in vitro fertilization (IVF) is insufficient. Therefore, luteal phase supplementation is routinely applied in IVF. It may be postulated that premature luteolysis after ovarian hyperstimulation is due to supraphysiological steroid levels in the early luteal phase. In the present study, high doses of steroids are administered after the LH surge in normo-ovulatory volunteers in order to investigate whether this intervention gives rise to endocrine changes and a shortening of the luteal phase. Design: Randomized controlled trial. Methods: Forty non-smoking, normal weight women, between 18 and 37 years of age, with a regular menstrual cycle (24–35 days), received either high dosages of estradiol (E2), progesterone (P), E2CPor no medication. Blood sampling was performed every other day from the day of the LH surge until LHC 14. Duration of the luteal phase and endocrine profiles were the main study outcomes. Results: Early luteal phase steroid concentrations achieved by exogenous administration were comparable with levels observed following ovarian hyperstimulation for IVF. No difference in the luteal phase length was observed comparing all groups. However, a significant decrease in LH levels could be observed 6 days after the mid-cycle LH surge (P!0.001) in women receiving P,resulting in accelerated decrease of inhibin A production by the corpus luteum (PZ0.001). Conclusion: The present intervention of high-dose steroid administration shortly after the LH surge failed to induce a premature luteolysis regularly in cyclic women. It seems that the induced transient suppression in LH allowed for a timely recovery of corpus luteum function. Other additional factors may be held responsible for the distinct reduction in luteal phase length observed after ovarian hyperstimulation for IVF. European Journal of Endocrinology 155 355–363 Introduction (P) and the periodic secretion of pituitary LH for corpus luteum support and demise (7, 8). Indeed, under During normo-ovulatory cycles, the corpus luteum normal conditions, luteolysis can be induced by the remains dependent on support by the pituitary luteal phase administration of either GnRH agonist (9) gonadotropins throughout the luteal phase (1–3). or antagonist (10). Slowing down of the gonadotropin releasing hormone Since the early days of in vitro fertilization (IVF), it has (GnRH) pulse generator along with diminished luteiniz- been described that the luteal phase of stimulated cycles ing hormone (LH) pulse amplitude, is responsible for the is abnormal. In fact, it was already stated in the first demise of the corpus luteum both in the monkey and the extended report on IVF by Edwards et al. (11) that ‘the human (1, 4). Luteolysis can only be prevented by rising luteal phase of virtually all patients was shortened doses of LH (5) or by human chorionic gonadotropin considerably after treatment with gonadotropins’ and it (hCG) (either exogenously administered or produced by was suggested that high-follicular phase E2 levels caused the placenta in the case of pregnancy) (6). Under by ovarian hyperstimulation might be involved. Initial normal conditions, a tight balance is operative between studies in 1983 also confirmed the occurrence of an negative-feedback activity of estradiol (E2), progesterone abnormal lutealphase in IVF cycleswith the characteristic q 2006 Society of the European Journal of Endocrinology DOI: 10.1530/eje.1.02199 Online version via www.eje-online.org Downloaded from Bioscientifica.com at 09/27/2021 05:34:42AM via free access 356 N G M Beckers and others EUROPEAN JOURNAL OF ENDOCRINOLOGY (2006) 155 features of elevated P-levels along with a significantly luteolysis due to massive negative feedback resulting in reduced luteal phase length (12). greatly suppressed LH secretion (33, 34). The stimu- GnRH agonist co-treatment has been the standard of lation of multiple dominant follicles during the care in IVF for the prevention of a premature rise in LH follicular phase will subsequently give rise to multiple during ovarian hyperstimulation (13). Typically, GnRH corpora lutea, all involved in luteal phase steroid agonist treatment is initiated in the luteal phase of the synthesis. The present study in volunteers was preceding cycle and continued until the late follicular undertaken to explore further the role of early luteal phase. Delayed pituitary recovery from downregulation phase steroids in the regulation of pituitary LH release during the luteal phase results in lack of support of the and corpus luteum function. These findings may corpus luteum by endogenous LH and therefore in be relevant for the better understanding of luteal advanced luteolysis (14). The corpus luteum can be phase dysfunction following ovarian hyperstimulation rescued under these circumstances by the adminis- for IVF. tration of hCG (15) and this treatment modality became the standard of care for luteal support during the late 1980s (16). Because of the association between hCG and ovarian hyperstimulation syndrome (17), luteal Materials and methods phase hCG support has been largely replaced by luteal phase P supplementation (18, 19). Subjects Attempts to secure pituitary recovery during the luteal This prospective randomized two-center trial was phase by the early follicular phase cessation of GnRH approved by the local ethics review committees of both agonist treatment (20, 21) failed, presumably due to the participating centers (Erasmus MC Rotterdam, The prolonged recovery of LH secretion (22). Because of the Netherlands (EMC) and AZ-VUB Brussels (VUB)). An rapid recovery of pituitary gonadotropin release after information form was sent to responders of advertise- discontinuation of GnRH antagonist (23, 24), it has been ments. Subjects interested in participating underwent widely speculated that the luteal phase supplementation initial screening before enrollment in the study. A signed may not be required following ovarian hyperstimulation written informed consent was obtained from all study in combination with late follicular phase co-administra- participants. Women who completed the study were tion of GnRH antagonist (25). Preliminary observations paid for their participation. Inclusion criteria were: in intrauterine insemination seem to favor this conten- (i) regular menstrual cycle (cycle length between 24 tion (26). However, various studies in IVF applying and 35 days), (ii) normal body weight (body mass index GnRH antagonist co-treatment have now clearly estab- 18–28 kg/m2), (iii) reproductive age (18–37 years), (iv) lished that luteolysis is also initiated prematurely under normal early follicle-stimulating hormone (FSH) level those conditions resulting in a significant reduction in (%10 IU/l), (v) absence of factor V Leiden mutation, (vi) luteal phase length and greatly compromised chances for no use of oral contraceptive or other hormone-related pregnancy (27, 28). More detailed studies could confirm contraceptives in the previous 3 months, (vii) no that early- and mid-luteal phase LH levels remained smoking habit, (viii) no history of epilepsy, diabetes, suppressed following the follicular phase administration gastrointestinal, hepatic, renal, or pulmonary disease, of GnRH antagonist (28, 29). (ix) no use of other investigational drugs within 3 Alternative mechanisms involved in luteal dysfunc- months prior to the study, or hormonal preparations tion following ovarian hyperstimulation in IVF may be within 1 month prior to the study, and finally (x) no use proposed: (i) follicle puncture and the removal of of anti-depressive drugs. cumulus–oocyte complexes including large quantities of surrounding granulosa cells (which form the most important P secreting unit in the subsequent corpus Study protocol luteum). However, initial studies addressing this issue The initial screening comprised of a medical history and failed to consistently show detrimental effects (30). (ii) aphysicalexamination,includingvitalsignsand Short-loop feedback by the late follicular phase bolus vaginal ultrasound examination to exclude abnormal- dose of hCG to induce final oocyte meiotic maturation. ities in both uterus and ovaries. Blood was taken for the Although there were some indications of such an effect assessment of FSH and factor V Leiden mutation (to at the pituitary level suppressing gonadotropin release exclude women with an increased risk for thrombo- (31), this could not be confirmed by subsequent studies embolic processes). After successful screening, the (28, 29). (iii) Luteal phase defects can also be induced by volunteers
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