Abstract. Introduction. Materials and methods. Patients and methods

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1 RBMOnline - Vol 8. No Reproductive BioMedicine Online; on web 20 January 2004 Article Cumulative live birth rates after transfer of cryopreserved ICSI embryos Dr Osmangaoglu is Belgian with Turkish roots. He obtained his MD qualification in 1988 at the Gazi University of Ankara, Turkey, becoming a board certified specialist in nuclear medicine in 1994 (Gent University of Belgium) and a board certified specialist in gynaecology, obstetrics and fertility in 2000 (Free University of Brussels). Currently he is a PhD student at the Centre for Reproductive Medicine of the Free University of Brussels. His thesis is entitled Life-Table Analysis of Cumulative Delivery Rates After Intracytoplasmic Sperm Injection. At present he is working at the fertility centre of the Jan Palfijn General Hospital in Gent, Belgium. Dr Kaan Osmanagaoglu Kaan Osmanagaoglu 1, Efstratios Kolibianakis, Herman Tournaye, Michel Camus, Andre Van Steirteghem, Paul Devroey Centre for Reproductive Medicine, Dutch-speaking Brussels Free University, Laarbeeklaan 101, B 1090 Brussels, Belgium 1 Correspondence: Tel: Fax: ; osmanagaoglu@hotmail.com Abstract A cohort follow-up study was designed to assess the efficacy of an intracytoplasmic sperm injection cryopreservation programme through analysis of cumulative live birth rates in successive frozen thawed cycles in a tertiary referral centre. There were 2013 patients and they underwent 2680 frozen thawed embryo transfer cycles. The follow-up period was between 1992 and Only frozen thawed embryo transfer cycles up to the fourth trial were included. Crude cumulative live birth rates were calculated in five age subgroups, i.e. <30, 30 34, 35 37, and 40 years old and in surgically or non-surgically retrieved sperm subgroups. Expected cumulative live birth rates were calculated only for the total number of patients. Outcome measure was a live birth occurring after 25 weeks of gestation. Overall, the expected cumulative live birth rate was as high as 26.7% after four cycles while the crude cumulative delivery rate was 10.5%. Multiple cryopreserved embryo transfer cycles increase the chance of a couple to achieve a live birth. Keywords: cumulative pregnancy rates, cryopreserved embryos, ICSI, life-table analysis, live birth 344 Introduction The occurrence of multiple pregnancies and ovarian hyperstimulation syndrome after assisted reproductive techniques remains a source of considerable concern. Cryopreservation and embryo transfer at a later stage reduces the chance of multiple pregnancies by allowing the transfer of only one or two embryos. In addition, it has been used as an alternative treatment in patients at high risk of ovarian hyperstimulation. However, cryopreservation results in the accumulation of an increasing number of cryopreserved embryos from fresh cycles. It has been reported that there is no significant difference in either pregnancy rates or miscarriage rates between cryopreserved IVF and intracytoplasmic sperm injection (ICSI) embryos (Al-Hasani et al., 1996; Kowalik et al., 1998). When considering the safety of cryopreservation of embryos, no difference appears to exist in the incidence of major malformation in children born after IVF and ICSI from either a fresh or a frozen thawed embryo transfer cycle (Aytoz et al., 1999). However, no data exist currently in the literature on the value of performing multiple frozen thawed embryo transfers following ICSI treatment. The purpose of this study was to assess the efficacy of an ICSI cryopreservation programme by analysing expected cumulative delivery rates in frozen thawed cycles. Materials and methods Patients and methods The patient population was observed between 1992 and June Patient age was calculated on the first day of the menstrual cycle in which the first ICSI treatment was carried out. Following ICSI, 2013 couples underwent 2680 frozen thawed embryo transfer (FRET) cycles in which at least one embryo was transferred. The indications for ICSI were longstanding male infertility or fertilization failure after conventional

2 IVF. The main outcome measure was live birth after 25 weeks of gestation. Embryo donation cycles were not included in the study. A long-term desensitization protocol using the gonadotrophinreleasing hormone agonist buserelin combined with human menopausal gonadotrophin was used for ovarian stimulation. Human chorionic gonadotrophin (HCG), 10,000 IU, was used to induce ovulation, which was followed by vaginal oocyte retrieval 36 h later. All the details of ICSI procedures have been extensively described elsewhere (Van Steirteghem et al., 1996). Embryos were frozen at the multicellular stage on day 2 or 3 until December 1998 and at the blastocyst stage on day 5 or 6 since January Selection of embryos for freezing (Van den Abbeel et al., 2000), freezing procedures (Van der Elst et al., 1995, 1997), thawing strategies (Van den Abbeel et al., 2000) and transfer of frozen thawed embryos (Van der Elst et al., 1995, 1997) have been described in detail elsewhere. Except for some minor changes, the cryobiology procedures used in this study were fundamentally similar. The embryo transfer policy used in this study has been described in detail previously (Van der Elst et al., 1995, 1997; Adonakis et al., 1997). However, in patients over 40 years of age, more than three embryos were transferred into the uterine cavity (Grimbizis et al., 1998). For the purposes of this analysis, thawed embryos transferred could have been cryopreserved after different fresh cycles. Thirty-seven per cent of the FRET were performed in natural cycles and 63% were performed in clomiphene citrate cycles. Luteal-phase supplementation with micronized progesterone (600 mg per day) was administered intravaginally in three separate doses with or without the addition of HCG. Pregnancy and child follow-up was carried out in the context of a prospective follow-up programme for ICSI (Bonduelle et al., 2002). Statistical analysis Cumulative delivery rates are shown up until the fourth trial. Further analysis included calculation of crude cumulative delivery rates in five age subgroups, (<30, 30 34, 35 37, and 40 years) and in patients whose spermatozoa were retrieved surgically or non-surgically. However, life-table analysis was confined to the overall group in order to avoid overestimation of the cumulative delivery rates analysing small groups of patients. Cumulative delivery rates were calculated by life-table analysis using the Kaplan Meier product limit procedure (Kaplan and Meier, 1958). The Kaplan Meier method was developed to calculate the estimated survival rates of cancer patients in different therapy models, and thus provides only expected delivery or pregnancy rates. Cumulative delivery rates were expressed as cumulative percentage probabilities with 95% confidence interval (95% CI). Furthermore, differences between groups were assessed by the log-rank test or Mann Whitney U- test (SPSS version 10.0; SPSS Inc., Chicago, IL, USA). A P- value of 0.05 was assumed to indicate significance. Values are expressed as mean ± SD. Results From 1991 to 2001, 11,082 ICSI oocyte collection cycles were performed, resulting in 9963 fresh embryo transfer procedures (90%; 9963/11082). Embryo freezing of at least one embryo was done in 4587 cycles (ICSI cycle cryopreservation rate: 46%; 4587/9963). A total of 68,302 2-pronuclei-stage embryos were obtained. Following in-vitro culture, 25,804 embryos were transferred fresh (fresh embryo transfer rate: 38%; 25,804/68,302) and 19,952 embryos were frozen (embryo cryopreservation rate: 29%; 19,952/68,302). Study population The mean age of the patients was 31.3 ± 4.4 years. The mean interval between repeated fresh treatment cycles was 5.5 ± 1.2 months. The live birth rate per frozen thawed embryo transfer cycle was 8.25% overall. In the overall population, expected cumulative deliveries reached 26.7% after four cycles, while the crude cumulative delivery rate was 10.5% (Table 1). There was no significant difference in the crude delivery rate achieved by either non-surgically or surgically retrieved sperm groups (8.6 versus 5% respectively) The crude cumulative delivery rate in patients younger than 30 years old increased until the third FRET cycle, after which it reached a plateau at 13.5%. In contrast, the cumulative delivery rate in patients older than 40 years levelled off at the second FRET cycle, at 6.9%. The difference between the two age groups is not statistically significant (log rank test: P = 0.259). Delivery rates per cycle and cumulative rates according to age group (<30, 30 34, 35 37, and 40 years) are presented in Table 2. Drop-out rate (patients who were not able to proceed to a further frozen thawed embryo transfer cycle) was 68% after the first frozen thawed embryo transfer in women less than 40 years old and 79% in patients older than 40 years (Table 2). Deliveries in both corresponding fresh and cryopreservation cycles were observed in 2.4% of patients after the first cycle. Delivery rates for fresh and cryopreserved embryo transfer cycles are given in Table 3. There were 38 (34 twins and four triplets) multiple pregnancies. Six extra-uterine pregnancies were detected beside the deliveries. Discussion This study has shown that, overall, the expected cumulative delivery rate following four frozen thawed embryo transfers may reach 26.7%, while the crude cumulative delivery rate is 10.5%. Moreover, a delivery rate of 8.3% per FRET cycle can be obtained following a fresh transfer. The calculation of cumulative delivery rates after frozen thawed embryo transfer may be biased by a variety of factors. In this study, cumulative delivery rates after frozen thawed embryo transfer cycles were calculated irrespective of whether embryos transferred were obtained from different ICSI cycles. 345

3 Table 1. Cumulative live birth rates according to sperm origin with frozen thawed embryos. All ages, surgical, non-surgical spermatozoa No. of patients No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) Expected cumulative live birth rates (%) % confidence interval All ages, non-surgical spermatozoa No. of patients No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) All ages, surgical spermatozoa No. of patients No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rate (%) Table 2. Cumulative live birth rates according to age groups with frozen thawed embryos. No. of patients (age <30 years) No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) No. of patients (age 30 to <35 years) No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) No. of patients (age 35 to <38 years) No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) No. of patients (age 38 to <40 years) No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) No. of patients (age 40 years) No. of live births No. of non-pregnant and discontinued Crude cumulative live birth rates (%) P = (log rank).

4 Table 3. Deliveries in corresponding fresh and cryopreservation cycles a. Deliveries after 339/ /466 27/134 7/42 fresh cycles (%) (16.8) (16.3) (20.1) (16.6) Deliveries after 166/ /466 6/134 4/42 cryopreservation (8.3) (7.5) (4.5) (9.5) cycles (%) Deliveries occurring 4/166 5/35 1/6 0 in both fresh and (2.4) (14.2) (16.7) cryopreservation cycles (%) a In the first fresh stimulation cycle there were 2013 patients, 339 of them became pregnant and the remaining embryos were frozen. All of these 2013 patients came back to use their frozen embryos and 166 patients became pregnant after transfer of frozen thawed embryos. Only four of 166 (2.4%) patients after a transfer of frozen thawed embryos had also been pregnant in their previous fresh embryo transfer cycles. This ignores the effect of increasing maternal age between ICSI cycles, but this is probably negligible, as the median interval between consecutive ICSI cycles is only 5.3 months. The stage at which embryos should be cryopreserved remains a matter of debate, as improved survival rates have been reported at the multi-cellular embryo stage (Kattera et al., 1999) and the 1-cell stage (Hoover et al., 1997), while the efficacy of blastocyst cryopreservation is still not clear. On the other hand, less favourable results were reported when mixed embryos were transferred in comparison to transfer with further-cleaved embryos only (Van den Abbeel et al., 2000). The current study could not consider the above factors in its analysis, due to the restrictions imposed by the size of the population analysed. Life-table analyses have been used to estimate the success rates in assisted reproduction techniques. In life-table analysis, it is assumed that those who continue and those who quit have the same probability of reaching the defined event (i.e. a clinical pregnancy or a delivery). Life-table analysis may overestimate live birth rate, but it should be noted that the benefit of frozen thawed embryo transfers has not been completely evaluated in the current analysis. This is due to the fact that there are still frozen-embryos in the cryo-bank and these embryos may be assumed to have the same pregnancy rate potential (Jones et al., 1997). The calculation of expected delivery rates for frozen thawed embryos is performed by assuming that there are enough embryos to be frozen after the ICSI cycle for every individual. As a consequence, the results presented here should be interpreted with caution, since the calculated expected rates cannot provide valid conclusions for individuals, but only for the overall pool of frozen thawed embryos. Only 2.4% of the pregnant patient group delivered after transferring fresh as well as after transferring frozen thawed embryos from the same stimulation cycle. This stresses the added value of cryopreserved embryos and discredits the idea that women achieving a successful pregnancy from an earlier fresh embryo transfer cycle have a higher chance of success from later frozen thawed embryo transfer cycles. Up to now, no data have been available regarding cumulative delivery rates exclusively from cryopreserved embryo transfers after IVF or ICSI. This is the first study to analyse such a large population of patients undergoing at least one frozen thawed cycle following ICSI embryo transfer and for whom complete pregnancy follow-up was recorded. This study shows that by performing at least four FRET cycles, one out of four patients would be expected to achieve a live birth (as assessed by using the life-table analysis). Overall live birth rate in ICSI cycles was 17%, while FRET cycles conferred an additional 8% live birth rate per cycle. Thus the combined delivery rate per cycle reached 25%. However, this calculation method might be misleading, as not every patient will have enough embryos for cryopreservation and subsequent embryo transfer, while patients for whom embryos can be frozen are probably a priori in a better prognosis category. The cumulative delivery rate reached a plateau after the third FRET attempt, as opposed to that achieved after ICSI cycles, which continues to increase until the sixth attempt (Osmanagaoglu et al., 1999, 2002). This is probably due to the fact that a patient undergoing a third FRET attempt is likely to have undergone more than five assisted reproduction attempts (fresh and frozen in total), which puts her in an adverse prognosis group. In conclusion, this analysis demonstrates the advantage of multiple frozen thawed embryo transfers. Overall, the expected cumulative live birth rate rose to 26.7% after four cycles while the crude cumulative live birth rate was 10.5%. At least an 8.3% live birth rate can be obtained from cryopreservation in addition to those occurring from a fresh cycle. It appears that the increasing pressure by authorities on fertility centres to reduce multiple pregnancies by limiting the numbers of embryos transferred will lead to more embryos being available for cryopreservation in the near future, which will result in consecutive frozen thawed embryo transfers. This analysis provides an important basis for counselling 347

5 patients about their chances of achieving a delivery after consecutive frozen thawed embryo transfers. Acknowledgements The authors wish to thank the clinical, scientific, nursing, and technical staff of the Centre for Reproductive Medicine especially the nurses and technicians involved in the follow-up project. Ms Julie Deconinck of the Language Education Centre at our University corrected the manuscript. This work was supported by grants from the Fund for Scientific Research- Flanders. References Adonakis G, Camus M, Joris H et al The role of the number of replaced embryos on intracytoplasmic sperm injection outcome in women over the age of 40. Human Reproduction 11, Al-Hasani S, Ludwig M, Gagsteiger F et al Comparison of cryopreservation of supernumerary pronuclear human oocytes obtained after intracytoplasmic sperm injection (ICSI) and after conventional in-vitro fertilization. Human Reproduction 11, Aytoz A, Van den Abbeel E, Bonduelle M et al Obstetric outcome of pregnancies after the transfer of cryopreserved embryos and fresh embryos obtained by conventional in-vitro fertilization and intracytoplasmic injection. Human Reproduction 14, Bonduelle M, Liebaers I, Deketelaere V et al Neonatal data on a cohort of 2889 infants born after ICSI ( ) and of 2995 infants born after IVF ( ). Human Reproduction 17, Grimbizis G, Vandervorst M, Camus M et al Intracytoplasmic sperm injection, results in women older than 39, according to age and the number of oocytes replaced in selective or non-selective transfers. Human Reproduction 13, Hoover L, Baker A, Check J et al Clinical outcome of cryopreserved human pronuckea stage embryos resulting from intracytoplasmic injection. Fertility and Sterility 67, Jones HW, Out H, Hoomans E et al Cryopreservation: the practicalities of evaluation. Human Reproduction 12, Kaplan EL, Meier P 1958 Nonparametric estimation from incomplete observations. Journal of the American Statistical Association 53, Kattera S, Shrivastav P, Craft I 1999 Comparison of pregnancy outcome of pronuclear and multicellular-stage frozen thawed embryo transfers. Journal of Assisted Reproduction 16, Kowalik A, Palermo GD, Barmat L et al Comparison of clinical outcome after cryopreservation of embryos obtained from intracytoplasmic sperm injection and in-vitro fertilization. Human Reproduction 13, Osmanagaoglu K, Tournaye H, Camus M et al Cumulative delivery rates after ICSI: a five-year follow-up of 498 patients. Human Reproduction 14, Osmanagaoglu K, Tournaye H, Kolibianakis E et al Cumulative delivery rates after intracytoplasmic sperm injection in women older than 37 years. Human Reproduction 17, Van den Abbeel E, Camus M, Joris H et al Embryo freezing after intracytoplasmic injection. Molecular and Cellular Endocrinology 169, Van der Elst J, Camus M, Van den Abbeel E et al Prospective randomized study on the cryopreservation of human embryos with dimethylsulfoxide or 1,2 propanediol protocols. Fertility and Sterility 63, Van der Elst J, Van den Abbeel E, Vitrier S et al Selective transfer of cryopreserved human embryos with further cleavage after thawing increases delivery and implantation rates. Human Reproduction 12, Van Steirteghem A, Nagy P, Joris H et al The development of intracytoplasmic injection. Human Reproduction 11 (suppl. 1), Received 6 November 2003; refereed 26 November 2003; accepted 18 December

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