Endometrial advancement after triggering with recombinant or urinary HCG: a randomized controlled pilot study

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1 Reproductive BioMedicine Online (2010) 21, ARTICLE Endometrial advancement after triggering with recombinant or urinary HCG: a randomized controlled pilot study EG Papanikolaou a,b, *, C Bourgain a, H Fatemi a, W Verpoest a, NP Polyzos c, A De Brabanter a, E Kolibianakis b, B Tarlatzis b, P Devroey a, H Tournaye a a Centre for Reproductive Medicine, Universitair Ziekenhuis Brussel, Vrije Universiteit Brussel, 101 Laarbeeklaan, 1090 Brussels, Belgium; b Assisted Reproduction Unit, 1st Ob Gyn Department, Aristotle University of Thessaloniki, Greece; c Panhellenic Association for Continual Medical Research (PACMeR), Section of Obstetrics and Gynaecology, Athens, Greece * Corresponding author. addresses: papanikolaou@irg.gr, drvagpapanikolaou@yahoo.gr (EG Papanikolaou). Vaggelis Papanikolaou obtained his MD degree (1994) and specialisation in Obstetrics and Gynecology (2002) from the Medical School of Ioannina, University of Ioannina, Greece, and was awarded a PhD degree there in 2004 with a thesis entitled Premature ovarian failure and endothelial dysfunction. The same year he obtained the degree of Master in Medical and Pharmaceutical Research from the Dutch-Speaking Free University of Brussels (VUB) where he has been a research fellow in the Centre of Reproductive Medicine at the University Hospital since Dr Papanikolaou s current research interests include ovarian hyperstimulation syndrome, reproductive endocrinology and endometrial receptivity. Abstract More than 3 days luteal endometrial advancement in IVF has been related with no pregnancies. This study assessed the effect of recombinant and urinary human chorionic gonadotrophin (rechcg and uhcg) when administered for final oocyte maturation on the advancement of endometrial histology. Thirty patients were randomized to receive either 250 lg rechcg or 10,000 IU uhcg in an antagonist/recombinant FSH protocol. Endometrial biopsy was performed on the day of oocyte retrieval. All specimens were evaluated according to Noyes criteria by one pathologist blinded to the allocation treatment groups. Single blastocyst transfer was performed. Overall, 13 patients in rechcg group and 14 patients in uhcg group underwent endometrial biopsy. The mean days of histological endometrial advancement were comparable between the two groups: 2.03 versus 2.17 days, respectively. Nevertheless more patients (69%, 9/13) had less than 3 days advanced endometrium in the rechcg arm as compared with 43% (6/14) patients in the uhcg group (OR 3.00, 95% CI ). The delivery rate per patient was higher, although not significantly, in the rechcg group (38.5% versus 28.6%). Both rechcg and uhcg preparations induce advancement of endometrial maturation. Whether a subtle difference in endometrial maturation affects the reproductive outcome remains to be proven. RBMOnline ª 2010, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. KEYWORDS: antagonists, endometrium, histology, receptivity, recombinant HCG /$ - see front matter ª 2010, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. doi: /j.rbmo

2 Endometrial advancement after HCG triggering 51 Introduction During natural cycles, endometrium maturation from proliferative to secretory results in the opening of the implantation window around day 19 and for 5 days. This period is the only period when a blastocyst can implant in the receptive endometrium. Chorionic gonadotrophin, as the major trophoblast-derived signal, not only rescues the corpus luteum but also modulates the uterine environment in preparation for implantation (Cameo et al., 2004). Whereas in natural cycles, initially LH and later chorionic gonadotrophin prepares the endometrium to receive the blastocyst and get implanted, in IVF cycles during multifollicular ovarian stimulation, chorionic gonadotrophin preparation is administered much earlier to induce final oocyte maturation. When endometrium biopsies were performed on the day of oocyte retrieval, histological advancement has been observed (Kolibianakis et al., 2002) compared with the endometrium maturation on the day of ovulation in natural cycles (Papanikolaou et al., 2005). Furthermore, when this advancement exceeds 3 days, the probability of pregnancy becomes zero (Kolibianakis et al., 2002). Endometrial advancement has been mainly considered the result of the exposure to the endometrium of supraphysiological steroid hormones throughout IVF treatment (Devroey et al., 2004). Since, chorionic gonadotrophin/lh receptors are present on the endometrium (Licht et al., 2003; Rao, 2001; Srisuparp et al., 2001), chorionic gonadotrophin preparations may directly affect the endometrium. Ovulation triggering with 10,000 IU urinary-derived human chorionic gonadotrophin (uhcg) preparation is the current practice and a key-step in IVF treatment for final oocyte maturation. Recently, however, recombinant human chorionic gonadotrophin (rechcg) has been introduced in IVF cycles. rechcg administered at a dose of 250 lg is equivalent to approximately 6700 IU of uhcg and, due to the DNA technology used, the recombinant regimen has higher purity and interbatch consistency. Thus, taking into account the different technology and the decreased bioequivalent dose of the recombinant regimen, it was postulated that the administration of rechcg might exert a reduced, if any, effect on the advanced maturation observed on endometria under ovarian stimulation for IVF compared with traditional treatment with uhcg. The aim of the current prospective randomized pilot study was to evaluate whether there is any difference on the endometrial maturation, when 250 lg recombinant HCG is administered for final oocyte maturation instead of the standard regime of 10,000 IU of urinary HCG. them for eligibility. The randomization list was not open to the treating physicians. All the specimens were evaluated by one pathologist blinded to the allocation treatment groups. Inclusion criteria were: (i) age less than 36 years; (ii) elective single embryo transfer on day 5; and (iii) signed informed consent for endometrium biopsy. Exclusion criteria were: (i) known intrauterine pathology; (ii) testicular spermatozoa; (iii) endometriosis stage III and IV; and (iv) polycystic ovary syndrome. The study was approved by the ethical committee of the University Hospital at the Vrije Universiteit Brussel as a proof of concept (EC ref 2005/70). All patients signed an informed consent. The patients were randomized to receive either 250 lg rechcg (Ovitrelle; Merck-Serono, Geneva, Switzerland) or 10,000 IU uhcg (Pregnyl; NV Schering-Plough, Organon, Oss, The Netherlands) for ovulation triggering (Figure 1). Ovarian stimulation was achieved with a fixed dose of IU of recombinant FSH (Gonal-F; Merck-Serono) starting at day 2 of the cycle with co-administration of gonadotrophin-releasing hormone antagonist, 0.25 mg cetrorelix (Cetrotide, Merck-Serono) commenced on day 6 of the stimulation. Stimulation could only initiate if progesterone was lower than 1.5 ng/ml and oestradiol lower than 80 pg/ml. Ovulation-triggering medication was administered when at least three follicles of 17 mm were present. All patients underwent elective single blastocyst transfer. Luteal support offered as 600 mg micronized progesterone vaginally administered from the day after oocyte retrieval (therefore endometrium histology was not affected). Clinical pregnancy was defined as cardiac activity present at 7 weeks of gestation. Delivery rate was also recorded. Endometrial biopsy and histological assessment Endometrium biopsies were performed with a Pipelle de Cornier under local anaesthesia on the day of oocyte retrieval. All endometrial specimens were fixed immediately in neutral buffered formalin 10% solution and were sent for histopathological examination. Endometrial advancement Materials and methods Patient population and ovarian stimulation Between July 2005 and January 2007, 30 patients were recruited to participate in this randomized controlled trial. Patients were randomized at the outpatient clinic after consenting to start IVF treatment. Allocation concealment was ensured by a research nurse. The research nurse used a computer-generated list, which was kept private, and she undertook randomization of the subjects after controlling Figure 1 Study design. rechcg = recombinant HCG; uhc- G = urinary HCG.

3 52 EG Papanikolaou et al. was assessed prospectively using Noyes criteria (Noyes et al., 1950). For assessment of endometrial maturation, the day of oocyte retrieval was defined the day of ovulation (luteal-phase day 0). All the specimens were evaluated by one pathologist blinded to the allocation treatment groups as well as the hormonal data and the stimulation outcome. Embryology data Sperm preparation, IVF and intracytoplasmic sperm injection procedures, and embryo culture were carried out as described elsewhere (Papanikolaou et al., 2006). In brief, embryo quality was assessed daily until the moment of transfer. The embryo quality on day 5 was assessed according to the formation and degree of expansion of the blastocele, the development of the inner cell mass and the development of the trophectoderm. The combined score ranged from 1 to 4, with each embryo received a score of 1 (top quality), 2 (good quality), 3 (fair quality) or 4 (poor quality). Embryos with a score of 4 were not transferred. Supernumerary embryos were frozen on day 5. Outcomes The primary outcomes were the mean advancement of endometrial maturation in days in each group and the effect of both regimens on the number of patients with more than 2 (3 or 4) days endometrial advancement. Secondary outcomes were the clinical pregnancy rate (defined as the presence of intrauterine sac with an embryonic pole demonstrating cardiac activity) and the relation between pregnancy achievement and endometrium advancement. Statistical analysis Statistical analysis was performed using the Statistical Package for Social Sciences version 15 (SPSS, USA). Non-parametric statistics were used due to the small sample size. Fisher s exact test was used to analyse nominal variables in the form of frequency tables. Mann Whitney U-test was used for non-normally distributed metric variables. All tests were two tailed with a confidence level of 95% (P = 0.05). Values are expressed as mean ± SEM. Group sample sizes of 12 patients in each group achieve 81% power to detect a difference of 1 day of advancement between the null hypothesis that both groups mean endometrial advancement is 2 days and the alternative hypothesis that the mean of uhcg group is 3 days with known group standard deviations of 1.00 and 0.70 and with a significance level (alpha) of 0.05 using a two-sided two-sample t-test. Results Fourteen out of 15 patients in the uhcg group and 13 out of 15 patients in the rechcg group underwent biopsy and had samples analysed (Figure 1). Patient demographics and stimulation characteristics are presented in Table 1. There were no statistically significant differences between the two groups with regards to age, days of stimulation, total dose of recombinant FSH administered, number of oocytes retrieved and number of fertilized ova (2PN embryos). Single blastocyst transfer was performed in each patient and the mean quality of transferred embryos was similar among the two groups. Similarly the oestradiol and progesterone values on the day of ovulation triggering were comparable in both groups. However, statistically significant higher HCG concentrations were present on the day of oocyte retrieval in the uhcg group (P = 0.001). One patient in each group did not undergo embryo transfer as no blastocysts were available on day 5. The mean endometrial advancement in the uhcg group was 2.17 ± 0.2 days, as compared with 2.03 ± 0.3 days in the rechcg group. The detailed histology dating and diagnosis is presented in Table 2. Although there was no statistical Table 1 Parameter Patient demographics and stimulation characteristics. uhcg group (n = 14) rechcg group (n = 13) Age (years) ± ± 0.6 Days of stimulation 10.6 ± ± 0.9 Total recombinant FSH dose (IU) 2075 ± ± 187 Oestradiol on trigger day (pg/ml) 1809 ± ± 326 Progesterone on trigger day (ng/ml) 1.09 ± ± 0.1 Oestradiol at oocyte retrieval (pg/ml) 1027 ± ± 115 Progesterone at oocyte retrieval (ng/ml) 11.4 ± ± 1.8 HCG at oocyte retrieval (miu/ml) ± 27 a ± 12 b Cumulus oocyte complexes retrieved 12.8 ± ± 1.3 2PN embryos (2 pronuclear zygotes) 6.8 ± ± 0.9 No. of day-5 embryos transferred 1 1 Mean quality of transferred blastocyst 1.2 ± ± 0.1 Embryos cryopreserved 2.9 ± ± 0.6 Endometrial advancement (days) 2.17 ± ± 0.3 Values are mean ± SEM unless otherwise stated. rechcg = recombinant human chorionic gonadotrophin; uhcg = urinary human chorionic a,b P =

4 Endometrial advancement after HCG triggering 53 Table 2 Results of endometrial advancement with urinary or recombinant human chorionic Endometrial dating in luteal phase a uhcg group (n = 14) rechcg group (n = 13) OR (95% CI) Proliferative 1 1 Day 2 LF (2 days advancement) 5 8 Day 3 LF (3 days advancement) 5 3 Day 4 LF (4 days advancement) 1 0 Polyp 1 1 Endometritis 1 0 Patients with less than 3 days advancement (%) 6/14 (42.9) 9/13 (69.2) 3.00 ( ) Values are number unless otherwise stated. LF = luteal phase; rechcg = recombinant human chorionic gonadotrophin; uhcg = urinary human chorionic a Histological dating according to Noyes criteria. difference regarding the mean endometrial advancement between groups, more patients 69% (9/13) had advanced their endometrium less than 3 days in the rechcg group compared with 43% (6/14) patients in the uhcg group (OR 3.00, 95% CI ). Similarly the above-observed non-significant difference in the endometrial advancement was reflected in the clinical pregnancy rate since 38.5% (5/13) of the patients in the rechcg group managed to achieve a clinical pregnancy compared with 28.6% (4/14) in the uhcg group (Table 3). Figure 2 illustrates the endometrial histology according to the achievement of clinical pregnancy or not in on the whole population. It is interesting to see that less patients became pregnant with 3 or even 2 days of advanced endometrial maturation and the one patient who experienced 4 days advancement did not achieve a pregnancy. Discussion Embryo and endometrium quality are pivotal to successful human embryo implantation and development. Accumulating literature indicates, however, that early luteal-phase endometrium is histologically advanced and concerns have been raised on the negative impact of this advancement on the implantation process (Bourgain and Devroey, 2007). The current prospective randomized controlled trial found no difference in the mean endometrial histology advancement in the early luteal phase of IVF patients undergoing ovulation triggering either with rechcg or uhcg. Nonetheless, there was a higher number of patients with less than 3 days advancement in the rechcg group. Despite the fact that this difference was not statistically significant, this 26% discrepancy in the percentage of patients with less than 3 days advancement of the endometrium may be actually reflected in the 10% higher pregnancy rate achieved with rechcg. This may be attributed to the fact that when endometrial advancement exceeds 3 days, the probability of pregnancy becomes zero (Kolibianakis et al., 2002; Ubaldi et al., 1997). This trial confirms earlier findings that, with the exception of one patient in each group, the rest of the patients had advanced endometria on the day of oocyte retrieval regardless the type of chorionic gonadotrophin used for ovulation triggering (Table 2). The study was not powered to detect differences in the overall clinical pregnancy rate among recombinant and urinary HCG. However, a non-significant difference was observed in the number of patients with less than 3 days advancement in the endometrial histology and this observation merits further research. A proper look at the hormones concentrations (Table 1) shows that the HCG concentrations at the day of oocyte retrieval significantly differ among the two regimens, being significantly higher in the uhcg group. Consequently, this higher concentration of HCG after uhcg triggering might have been responsible for the higher incidence of 3 or more days advancement observed in the uhcg group. This lower Table 3 Pregnancy outcomes after treatment with urinary or recombinant human chorionic Outcome uhcg group (n = 14) rechcg group (n = 13) OR (95% CI) Positive HCG rate per patient 35.7 (5/14) 38.5 (5/13) 1.12 ( ) Clinical pregnancy rate per patient 28.6 (4/14) 38.5 (5/13) 1.56 ( ) Delivery rate per embryo transfer 30.8 (4/13) 41.7 (5/12) 1.60 ( ) Values are percentage (number/total) unless otherwise stated. One patient in each group did not undergo embryo transfer. There were no statistically significant differences between the two groups. rechcg = recombinant human chorionic gonadotrophin; uhcg = urinary human chorionic

5 54 EG Papanikolaou et al. Figure 2 Endometrial advancement according to pregnancy achievement in both groups. HCG concentration in the recombinant arm is reasonable as the 250 lg of rechcg are equivalent to 6700 IU of uhcg. Therefore, it can be argued that if the comparison was attempted with 6700 IU of urinary HCG the difference in endometrial maturation might have disappeared. Although recent approaches of the endometrium are focusing on factors emerging in the implantation window either retrieved from animal or in-vitro studies, clinically applicable receptivity markers have not been emerged. On the contrary, endometrial histology, despite limitations due to interpretation and inter-observer variability (Papanikolaou et al., 2006), when it presents extremely deviant morphology (more than 3 days advancement on the day of ovum retrieval) it has been correlated with a deleterious effect on reproductive outcome (Papanikolaou et al., 2005). Indeed, the only patient in the uhcg group who presented 4 days advanced endometrium did not get pregnant. Furthermore, a more detailed evaluation of Figure 2 shows that more patients with 3 or even 2 days advancement did not manage to achieve a pregnancy. A limitation of this study is the limited number of patients included. The small sample size might have been responsible for not reaching statistical significance in the analysis despite the 26% difference regarding less than 3 days advancement of the endometrium maturation between the compared arms (OR 3.00). Possibly a larger sample size would have been able to detect statistically significant differences. Nonetheless, this has to be validated by future and larger randomized trials. Of course, attempting to draw conclusions from endometrium studies regarding implications on the probability of pregnancy would not be reliable and such an extrapolation of the results requires appropriate study design. By transferring a single embryo (as in this study), and especially a highly developed blastocyst, eliminates bias introduced by multiple embryos to be transferred and specifically of different quality. Although the delivery rate in this study is not equal between the two groups, larger sample sizes are needed to reach significance. Another important observation is that although an endometrium biopsy was performed in the luteal phase 5 days before the embryo replacement, excellent birth rates were observed, in all aspects comparable with previous published birth rates following single blastocyst transfer in IVF cycles with similar population demographics (Papanikolaou et al., 2006). The above justifies and encourages continuation of taking endometrium biopsies in fresh embryo-transfer stimulated cycles as being the major method of exploring the endometrial role in implantation. Moreover, several studies exploring the possibility that endometrial injury modulates the expression of specific genes that may increase uterine receptivity (Kalma et al., 2008) and pregnancy rates (Zhou et al., 2008) provide further evidence to pursue research into endometrial biopsy/histology. In conclusion, the present study shows that the mean endometrium histology is advanced when both regimens for ovulation triggering uhcg or rechcg are used. Nonetheless, 3 or more days advancement of the endometrium is more likely to happen in patients treated with urinary rather than rechcg. This might be attributed in the difference bioequivalence of the two medications used. Whether this observation may result in significant different pregnancy rates remains unclear. Larger studies, adequately powered to assess pregnancy rates are needed in order to confirm whether the non-statistically significant difference found in this study can reach significance. If this is the case, then the dogma of 10,000 IU of uhcg should be reconsidered and lower doses to be investigated for ovulation triggering in IVF. Acknowledgements All the medications were kindly offered by Merck Serono. References Bourgain, C., Devroey, P., Histologic and functional aspects of the endometrium in the implantatory phase. Gynecol. Obstet. Invest. 64, Cameo, P., Srisuparp, S., Strakova, Z., et al., Chorionic gonadotropin and uterine dialogue in the primate. Reprod. Biol. Endocrinol. 2, 50.

6 Endometrial advancement after HCG triggering 55 Devroey, P., Bourgain, C., Macklon, N.S., et al., Reproductive biology and IVF: ovarian stimulation and endometrial receptivity. Trends Endocrinol. Metab. 15, Kalma, Y., Granot, I., Gnainsky, Y., et al., Endometrial biopsy-induced gene modulation: first evidence for the expression of bladder-transmembranal uroplakin Ib in human endometrium. Fertil. Steril. (Epub ahead of print). Kolibianakis, E., Bourgain, C., Albano, C., et al., Effect of ovarian stimulation with recombinant follicle-stimulating hormone, gonadotropin releasing hormone antagonists, and human chorionic gonadotropin on endometrial maturation on the day of oocyte pick-up. Fertil. Steril. 78, Licht, P., von, W.M., Berkholz, A., et al., Evidence for cycledependent expression of full-length human chorionic gonadotropin/luteinizing hormone receptor mrna in human endometrium and decidua. Fertil. Steril. 79 (Suppl. 1), Noyes, R.W., Hertig, A.J., Rock, J., Dating the endometrial biopsy. Fertil. Steril. 1, Papanikolaou, E.G., Bourgain, C., Kolibianakis, E., et al., Steroid receptor expression in late follicular phase endometrium in GnRH antagonist IVF cycles is already altered, indicating initiation of early luteal phase transformation in the absence of secretory changes. Hum. Reprod. 20, Papanikolaou, E.G., Camus, M., Kolibianakis, E.M., et al., In vitro fertilization with single blastocyst-stage versus single cleavage-stage embryos. N. Engl. J. Med. 354, Rao, C.V., Multiple novel roles of luteinizing hormone. Fertil. Steril. 76, Srisuparp, S., Strakova, Z., Fazleabas, A.T., The role of chorionic gonadotropin (CG) in blastocyst implantation. Arch. Med. Res. 32, Ubaldi, F., Bourgain, C., Tournaye, H., et al., Endometrial evaluation by aspiration biopsy on the day of oocyte retrieval in the embryo transfer cycles in patients with serum progesterone rise during the follicular phase. Fertil. Steril. 67, Zhou, L., Li, R., Wang, R., Huang, H.X., et al., Local injury to the endometrium in controlled ovarian hyperstimulation cycles improves implantation rates. Fertil. Steril. 89, Declaration: The authors report no financial or commercial conflicts of interest. Received 25 September 2009; refereed 2 November 2009; accepted 8 February 2010.

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