Cryptic sperm defects may be the cause for total fertilization failure in oocyte donor cycles

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1 Reproductive BioMedicine Online (2012) 24, ARTICLE Cryptic sperm defects may be the cause for total fertilization failure in oocyte donor cycles Maria Goudakou a, *, Alexandra Kalogeraki c, Ioannis Matalliotakis c, Yannis Panagiotidis a, Giuseppe Gullo d, Yannis Prapas a,b a Iakentro, Fertility Centre, 4, Agiou Vasiliou Str., Z.C , Thessaloniki, Greece; b 4th Department of Obstetrics and Gynaecology, Aristotle University of Thessaloniki, Greece; c University of Crete, School of Medicine, Department of Obstetrics and Gynaecology, Heraklion, Greece; d Azienda Ospedaliera Universitaria Policlinico Paolo Giaccone PalermoScuola di Specializzazione in Ostetricia e Ginecologia, Palermo, Italy * Corresponding author. address: mgoudakou@yahoo.gr (M Goudakou). Maria Goudakou was born in Kavala and graduated in biology from the Aristotle University, Thessaloniki, Greece in She trained in embryology at the Iakentro Advanced Medical Center, where she now works as an embryologist. She has 10 years of clinical experience in a full range of laboratory diagnostic and assisted conception techniques for spermatozoa, oocytes and embryos. She has also obtained a Masters degree in Biology of Reproduction from the Medicine School of the University of Thessalia, Greece. She is currently undertaking her PhD at the Medicine School of the University of Crete, Greece. Her main interests include embryo culture technologies and endometriosis. Abstract In conventional IVF cycles with total fertilization failure, rescue intracytoplasmic sperm injection (ICSI) performed 24 h after insemination has yielded poor results. However, when ICSI is used, total fertilization failure is a rare event. The aim of the present study is to investigate the degree of sperm contribution to fertilization failures using the egg-sharing model in oocyte donor cycles. The study included only the oocyte donor cycles of sibling oocytes with total fertilization failure in at least one of the matched recipients. Oocytes from 49 oocyte donor cycles were equally shared among 98 recipients undergoing conventional IVF. Due to total fertilization failure in half of the recipients, rescue ICSI was carried out. Compared with the conventional IVF only group, the rescue ICSI group had a lower pregnancy rate (30.61% versus 71.43%), clinical pregnancy rate (28.57% versus 67.35%) and ongoing pregnancy rate (28.57% versus 63.27%) (all P < 0.01). Cryptic sperm defects in apparently normal spermatozoa may be the cause of total fertilization failure, indicating the need for simple routine tests to detect them. RBMOnline ª 2011, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. KEYWORDS: egg-sharing model, spermatogenesis, total fertilization failure, rescue ICSI cycles, oocyte donor cycles, conventional IVF cycles Introduction Although reported fertilization rates are rather high after IVF, the scenario of unexpected total fertilization failure is still an unfortunate event (Chen et al., 1995). Total fertilization failure remains an issue in assisted reproduction, despite the retrieval of normally appearing metaphase II (MII) oocytes and use of spermatozoa with normal parameters. Fertilization failure is more likely to occur after conventional IVF (10 25%; Chen et al., 1995) than after intracytoplasmic sperm injection (ICSI) (2 3%; Mahutte and Arici, 2003). Rescue ICSI was first attempted in the /$ - see front matter ª 2011, Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved. doi: /j.rbmo

2 Sperm contribution to unsuccessful fertilization in oocyte donor cycles 149 mid-1990s in order to salvage conventional IVF cycles with total fertilization failure (Sjögren et al., 1995). Fertilization failure could be due to either the oocyte or the spermatozoon. Oocyte maturity cannot be assessed with classical IVF techniques and undiagnosed immature oocytes may account for fertilization failure. The decision to treat a patient with IVF or ICSI is mainly based on evaluation and assessment of semen parameters. Although semen analysis determines sperm count, motility, viability and morphology, other functions such as sperm penetration and fertilization ability are not detected (Overstreet et al., 1980). It has been reported that some cycles with total fertilization failure might have been rescued with delayed reinsemination using the ICSI procedure (rescue ICSI) (Boldt et al., 1987). In most of these cycles, reinsemination of the unfertilized oocytes was performed approximately 20 h after the initial insemination with reported fertilization rates as low as 16% or as high as 70% (Ben-Rafael et al., 1986; Boldt et al., 1987; Trounson and Webb, 1984) and pregnancy rates from 6.9% to 20.71% (Bussen et al., 1997; Morton et al., 1997; Yuzpe et al., 2000). In order to study the degree of contribution by the oocyte and spermatozoa to total fertilization failure, this prospective study used the egg-sharing model in oocyte donor cycles. Materials and methods Patient population Data from oocyte donors with total fertilization failure and their corresponding recipients participating in the oocyte donor programme at IAKENTRO IVF Centre, Thessaloniki, Greece between January 2005 and December 2007 were prospectively analysed. All women were donors of known fertility and donated their oocytes anonymously and altruistically and had donated their oocytes in the past. Most of the donors (36/49) had previously successful pregnancies, had completed their families and all of them had conceived naturally. Some of the donors (13/49) didn t have their own children, because they were very young and didn t want to have children at that time. Additionally, inclusion criteria were age 32 years old, body mass index <30 kg/m 2, regular menstrual cycles of days, two normal ovaries based on transvaginal scan findings, no endometriosis and no gynaecological or medical disorders. All donors had blood samples taken for karyotype analysis and screening for previous viral infection (hepatitis B (HbsAg) and C, human immunodeficiency virus, cytomegalovirus and syphilis (rapid plasma reagin)). A total of 51 out of 1814 (2.8%) IVF oocyte donor cycles, for which at least one of their matched receivers presented total fertilization failure, were included in the study. In 49 cycles the egg-sharing model was applied while in two cycles a unique recipient was used. The 49 oocyte donor cycles for which the oocytes were equally shared among 98 recipients were prospectively analysed. Due to total fertilization failure in half of the recipients, rescue ICSI was carried out; the corresponding recipients had conventional IVF. None of the studied cycles had total fertilization failure in both of their recipients. Total fertilization failure in IVF cases without ICSI as a percentage of all cycles performed in the study centre for the same period was in the 2 3% range. Donor stimulation Ovarian stimulation was carried out with the administration of recombinant FSH (Puregon, 250 IU; Organon, Oss, The Netherlands) per day starting on day 2 of the menstrual cycle and a gonadotrophin-releasing hormone antagonist (Orgalutran 0.25 mg; Organon) administered from stimulation day 6 (Prapas et al., 1995). Cycle monitoring and oocyte retrieval have been previously described in detail (Prapas et al., 2009). Recipients A total of 98 recipients were included in the study. All recipients were nulliparous, <50 years of age and were either menopausal or poor responders (less than four oocytes in two previous IVF cycles). All recipients and their partners underwent blood screening similar to the donors (Prapas et al., 2009). A hysterosalpingography was also performed for all recipients. Endometrial preparations of the recipient, donor-recipient synchronization, embryo transfer and luteal-phase support have all been previously described in detail (Prapas et al., 2009). Semen preparation, insemination and embryo culturing Semen samples from the partners were considered normal as regards sperm concentration, motility and morphology according to WHO criteria (World Health Organization, 1992) and Kruger s strict morphology criteria (Kruger et al., 1986). All semen samples were processed through 80% and 40% columns (Sperm Filter; Cryos, Denmark), centrifuged for 20 min at 300 g, followed by a wash in Earle s balanced salt solution with 5% human serum albumin (Irvine Scientific, Santa Anna, California) and 0.5% gentamicin solution (Sigma Aldrich, Germany) and centrifuged for 20 min at 300 g. At the final pellet the swim-up method was performed by adding 0.5 ml of incubated human tubal fluid (Quinn s Advantage Protein Plus; SAGE, Trumbull, USA) and left at 37 C, 6% CO 2 in air, humidified atmosphere for 1 h. A final preparation of 100,000 spermatozoa per oocyte was used to inseminate the oocytes in one well of human tubal fluid 2 4 h after retrieval. Fertilization was checked h later. After being carefully cleaned to remove any remaining cumulus and corona cells, oocytes were checked for the presence of pronuclei (PN), cytoplasmic contraction and the second polar-body extrusion. If none of these features were shown, oocytes were considered as not fertilized and underwent rescue ICSI. Rescue ICSI and embryo scoring All MII oocytes that failed to fertilize underwent rescue ICSI. Motile spermatozoa from the original insemination were used for the rescue ICSI procedure. Following ICSI the

3 150 M Goudakou et al. injected oocytes were placed in 30 ll Quinn s Advantage Protein Plus and cultured in a tri-gas incubator (5% CO 2, 5% O 2 and 90% NO 2 ) for approximately 18 h. Then fertilized zygotes were carefully checked for the number and regular size of PN and normal presence of nucleoli within the pronucleus (Scott, 2001, 2002, 2003; Scott and Smith, 1998). The embryos were then graded on a scale of 1 to 4 (Cummins et al., 1986). Grade-1 embryos were excellent with symmetrical blastomeres and no obvious fragmentation. Grade-2 embryos had blastomeres with <10% fragmentation of the cytoplasmic mass. Grade-3 embryos had 10 50% of their cytoplasm fragmented and grade-4 embryos had >50% cytoplasmic fragmentation. Embryo transfer, cryopreservation and outcome At most, three good-quality embryos were transferred on day 3 after oocyte retrieval under ultrasound guidance (Prapas et al., 1995). In cases of rescue ICSI, transfer of 2 4-cell embryos was carried out because of the delayed fertilization. Supranumerary embryos were cultured and cryopreserved if they reached the blastocyst stage. A pregnancy test was performed 15 days after embryo transfer, and, if positive, an ultrasound scan was scheduled 2 weeks later. Clinical pregnancy was defined as the presence of a gestational sac in the ultrasound scan at 7 weeks of gestation. Statistical analysis Data were analysed with Statistica 8 (StatSoft, OK, USA). Independent samples t-test was used for the comparison of mean values of quantitative variables and chi-squared test was used to compare qualitative variables. Normality was evaluated by the use of Kolmogorov Smirnov test. All tests were two-sided. A P-value <0.05 was considered as statistically significant. Results Data were prospectively collected for 49 egg-sharing cycles at the Iakentro s oocyte donor programme from January 2005 to December All these cycles had at least one of their matched recipients presenting total fertilization failure. Additionally, during the study period we did not have any egg-sharing cycle with total fertilization failure in both matched receivers. A total of 98 recipients received oocytes from 49 donors. Mean age of recipients was ± 4.60 years in the rescue ICSI group and ± 5.70 years in the conventional IVF group, and mean age of their male partners was ± 5.47 years and ± 5.70 years, respectively (Table 1). The number of donated oocytes was similar between the two groups. Sperm parameters with regards sperm concentration, motility and morphology were also similar between the two groups (Table 2). In two out of 49 rescue ICSI cycles, no embryo transfer took place due to poor embryo quality (Table 1). Mean number of embryos transferred (2.34 ± 0.77 versus 2.36 ± 0.73), embryonic score of transferred embryos (1.46 ± 2.22 versus 1.53 ± 0.70) and mean endometrial thickness (10.96 ± 1.54 versus ± 1.39) on the day of embryo transfer were similar between the two groups (Table 1). Table 1 Cycle characteristics of the rescue intracytoplasmic sperm injection (ICSI) and conventional IVF groups. Characteristic Rescue ICSI (n = 49) Conventional IVF (n = 49) Recipient age (years) ± ± 5.70 Male age (years) ± ± 5.70 Donated oocytes 7.36 ± ± 2.46 Endometrial thickness (mm) ± ± 1.39 Metaphase II Fertilization rate 183/347 (52.7) 157/230 (68.3) No transfer cycles 2 0 Embryos transferred 2.34 ± ± 0.73 Embryonic score 1.46 ± ± 0.70 Values are mean ± SD, n or n/total (%). There were no statistically significant differences between the two groups. Table 2 Sperm parameters of the rescue intracytoplasmic sperm injection (ICSI) and conventional IVF groups. Sperm parameter Rescue ICSI (n = 49) Conventional IVF (n = 49) Concentration ( 10 6 /ml) ± ± Total motility (%) ± ± Progressive motility (%) ± ± WHO normal morphology (%) ± ± Values are mean ± SD. There were no statistically significant differences between the two groups.

4 Sperm contribution to unsuccessful fertilization in oocyte donor cycles 151 Table 3 groups. Outcome Outcomes of the rescue intracytoplasmic sperm injection (ICSI) and conventional IVF Rescue ICSI (n = 49) Conventional IVF (n = 49) P-value Pregnancy rate 15 (30.61) 35 (71.43) <0.01 Clinical 14 (28.57) 33 (67.35) <0.01 Biochemical 1 (6.67) 2 (5.71) NS Ongoing 14 (28.57) 31 (63.27) <0.01 Miscarriage rate 0 2 (4.08) NS Live births 14 (1 triplets, 4 twins) Values are n (%). NS = not statistically significant. Compared with the conventional IVF only group, the rescue ICSI group had a lower pregnancy rate (30.61% versus 71.43%), clinical pregnancy rate (28.57% versus 67.35%) and ongoing pregnancy rate (28.57% versus 63.27%) (all P < 0.01; Table 3). Two women in the conventional IVF group underwent miscarriage. Discussion This prospective study has shown that undiagnosed cryptic sperm defects may be the main reason accounting for total fertilization failure in IVF oocyte donor cycles and that rescue ICSI is an acceptable alternative solution to save the otherwise lost cycles. It has been reported that the inability of the spermatozoa to penetrate the oocyte could be due to either gamete (Morton et al., 1997). The inability of spermatozoa to bind and penetrate (15 56%; Asch et al., 1995; Rawe et al., 2000), as well as maternal chromosomal defects (10 30%; Asch et al., 1995; Selva et al., 1991), have been proposed as pre-sperm penetration problems. Sperm defects, disturbances in spermatozoon oocyte interaction and oocyte abnormalities have all been proposed as possible causes of total fertilization failure after IVF (Bedford and Kim, 1993). Chen and Kattera (2003) have questioned whether in IVF cycles with total fertilization failure the rescued oocytes were in the MII stage or immature, since oocyte maturity is not always obvious with the classical IVF techniques. The present study has shown that oocyte maturity might not have been the cause of total fertilization failure since none of the studied oocyte donor cycles had total fertilization failure in both recipients who had received oocytes from the same donor that were randomly and equally shared among the two recipients. Additionally, analysing the oocyte donor data retrospectively from 2001 to 2004 confirmed that there were no cases with total fertilization failure in both recipients sharing oocytes from the same donor in the previous years (data not shown). Rescue ICSI was first attempted in the 1990s as a back up for IVF cases with total fertilization failure or poor fertilization rates to increase the number of available embryos (Ben-Rafael et al., 1986). Lundin et al. (1996) were the first to report pregnancies by ICSI of unfertilized oocytes after IVF. Pregnancy rates as low as 6.9% or as high as 48% (Bussen et al., 1997; Chen and Kattera, 2003; Morton et al., 1997; Yuzpe et al., 2000) were reported for the rescue ICSI cases. Chen and Kattera (2003) reported higher pregnancy rates (48%) when rescue ICSI was performed 6 h post insemination, compared with rescue ICSI 22 h post insemination (5%). They postulated that differences in pregnancy rates may be due to the ageing of oocytes in culture, which results in increased cytogenetic abnormalities and fewer normal embryos. In the current study, although pregnancy and implantation rates were significantly lower for the rescue ICSI group compared with the conventional IVF group, the ongoing pregnancy rate of 28.5% could be considered a rather acceptable alternative solution to otherwise lost cycles. Failures of unknown origin in which the spermatozoa appear to be normal may be rather problematic (Sakkas et al., 2004). Simple tests that assess sperm binding to the zona may be diagnostically useful and prevent a number of fertilization failures. In the current study, although pregnancy rates in the rescue ICSI group were lower than in the conventional IVF group, oocyte fertilization rates after rescue ICSI indicates that the intrinsic fertilizing capacity of the spermatozoa is intact in many cases of total fertilization failure. In addition, the oocyte donor model used in this study means that the developmental defects of the oocyte that could prevent penetration through the inner part of the zona pellucida are mostly likely to be absent. As such, a cryptic inability of apparently normal spermatozoa to bind to receptors at the zona surface or to intrude into the zona may exist and be the possible cause of failure of fertilization. In conclusion, cryptic sperm defects in apparently normal spermatozoa may be the cause of total fertilization failure in oocyte donor cycles, indicating the need for simple routine tests to detect them. References Asch, R., Simerly, C., Ord, T., et al., The stages at which human fertilization arrests: microtubule and chromosome configurations in inseminated oocytes which failed to complete fertilization and development in humans. Hum. Reprod. 10, Bedford, J.M., Kim, H.H., Sperm/egg binding patterns and oocyte cytology in retrospective analysis of fertilization failure in vivo. Hum. Reprod. 8, Ben-Rafael, Z., Kopf, G.S., Blasco, L., et al., Fertilization and cleavage after reinsemination of human oocytes in vitro. Fertil. Steril. 45, Boldt, J., Howe, A.M., Butler, W.J., et al., The value of oocyte reinsemination in human in vitro fertilization. Fertil. Steril. 48,

5 152 M Goudakou et al. Bussen, S., Mulfinger, L., Sütterlin, M., et al., Dizygotic twin pregnancy after intracytoplasmic sperm injection of 1 day old unfertilized oocytes. Hum. Reprod. 12, Chen, C., Kattera, S., Rescue ICSI of oocytes that failed to extrude the second polar body 6 h post-insemination in conventional IVF. Hum. Reprod. 18, Chen, H.L., Copperman, A.B., Grunfeld, L., et al., Failed fertilization in vitro: second day micromanipulation of oocytes versus reinsemination. Fertil. Steril. 63, Cummins, J.M., Breen, T.M., Harrison, K.L., et al., A formula for scoring human embryo growth rates in in-vitro fertilization: its value in predicting pregnancy and in comparison with visual estimates of embryo quality. J. IVF. Embryo. Transf. 3, Kruger, T.F., Menkveld, R., Stander, F.S., et al., Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil. Steril. 46, Lundin, K., Sjögren, A., Hamberger, L., Reinsemination of one-day-old oocytes by use of intracytoplasmic sperm injection. Fertil. Steril. 66, Mahutte, N.G., Arici, A., Failed fertilization: is it predictable? Curr. Opin. Obstet. Gynecol. Rev. 15, Morton, P.C., Yoder, C.S., Tucker, M.J., et al., Reinsemination by intracytoplasmic sperm injection of 1-day-old oocytes after complete conventional fertilization failure. Fertil. Steril. 68, Overstreet, J.W., Yanagimachi, R., Katz, D.F., et al., Penetration of human spermatozoa into the human zona pellucida and the zona-free hamster egg: a study of fertile donors and infertile patients. Fertil. Steril. 33, Prapas, N., Tavaniotou, A., Panagiotidis, Y., et al., GnRH antagonists and endometrial receptivity in oocyte recipients: a prospective randomized trial. Reprod. Biomed. Online 18, Prapas, Y., Prapas, N., Hatziparasidou, A., et al., The echoguide embryo transfer maximizes the IVF results. Acta Eur. Fertil. 26, Rawe, V.Y., Olmedo, S.B., Nodar, F.N., et al., Cytoskeletal organization defects and abortive activation in human oocytes after IVF and ICSI failure. Mol. Hum. Reprod. 6, Sakkas, D., D Arcy, Y., Percival, G., Sinclair, L., Afnan, M., Sharif, K., Use of the egg-share model to investigate the paternal influence on fertilization and embryo development after in vitro fertilization and intracytoplasmic sperm injection. Fertil. Steril. 82, Scott, L., The biological basis of non invasive strategies for selection of human oocytes and embryos. Hum. Reprod. Update 9, Scott, L., Morphological correlates of oocyte and embryo competence identification. Hum. Fertil. 5, Scott, L., Analysis of fertilization. In: Gardner, D.K., Weissman, A., Howles, C.M., Shoham, Z. (Eds.), Textbook of Assisted Reproductive Techniques: Laboratory and Clinical Perspectives. Taylor & Francis. Scott, L.A., Smith, S., The successful use of pronuclear embryo transfers the day following oocyte retrieval. Hum. Reprod. 13, Selva, J., Martin-Pont, B., Hugues, J.N., et al., Cytogenetic study of human oocytes uncleaved after in-vitro fertilization. Hum. Reprod. 6, Sjögren, A., Lundin, K., Hamberger, L., Intracytoplasmic sperm injection of 1 day old oocytes after fertilization failure. Hum. Reprod. 10, Trounson, A., Webb, J., Fertilization of human oocytes following reinsemination in vitro. Fertil. Steril. 41, Yuzpe, A.A., Liu, Z., Fluker, M.R., Rescue intracytoplasmic sperm injection (ICSI)-salvaging in vitro fertilization (IVF) cycles after total or near-total fertilization failure. Fertil. Steril. 73, World Health Organization, WHO Laboratory Manual for the Examination of Human Semen and Sperm Cervical Mucus Interaction, third ed. Cambridge University Press, Cambridge, pp. 44. Declaration: The authors report no financial or commercial conflicts of interest. Received 10 February 2011; refereed 13 October 2011; accepted 18 October 2011.

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