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Can sperm quality influence embryo development and its ploidy? Analysis of 811 blastocysts obtained from different sperm sources

Published online by Cambridge University Press:  09 June 2022

Romualdo Polese*
Affiliation:
Centro Fecondazione Assistita. Napoli, Campania, Italy
Filomena Scarselli
Affiliation:
European Hospital, Centre for Reproductive Medicine. Rome, Italy
Brian Dale
Affiliation:
Centro Fecondazione Assistita. Napoli, Campania, Italy
Maria Giulia Minasi
Affiliation:
European Hospital, Centre for Reproductive Medicine. Rome, Italy
Ermanno Greco
Affiliation:
European Hospital, Centre for Reproductive Medicine. Rome, Italy
*
Author for correspondence: Romualdo Polese. Centro Fecondazione Assistita. Napoli, Campania, Italy. E-mail: [email protected]

Summary

The aim of our study was to evaluate the correlation between sperm quality and ploidy status of the derived blastocysts. We performed a retrospective analysis on a restricted pool of patients enrolling only those who had no female factors. Male patients with genetic factors affecting spermatogenesis were also excluded. We chose a maternal age ≤38 years to decrease the female factor, therefore the male factor was the main component of sterility. We divided the patients in four groups based on semen quality and comparing fertilization, pregnancy and euploidy rates above all. In total, 201 intracytoplasmic sperm injection (ICSI) cycles were enrolled in the study. Cycles were divided into four groups, according to semen source: normal semen, oligoasthenoteratozoospermia (OAT), cryptospermia or non-obstructive azoospermia (NOA). An extremely statistically lower fertilization rate was found in NOA patients. Unexpectedly, no differences were detected in blastocyst formation, euploidy, aneuploidy and mosaicism rates among the four groups. Interestingly, we also found a higher abortion rate comparing NOA to normal semen with an odds ratio of 4.67. In our study no statistically significant differences among the analyzed groups were found, showing little or no effect at all using spermatozoa from different semen sources or quality. This may be linked to the oocyte competence of fixing sperm DNA damage and it could be hypothesized that only sperm with a good rate of DNA integrity are able to fertilize the oocyte, explaining why poor quality semen is reflected in a low fertilization rate without effect on ploidy.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Aitken, R. J., Gordon, E., Harkiss, D., Twigg, J. P., Milne, P., Jennings, Z. and Irvine, D. S. (1998). Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biology of Reproduction, 59(5), 10371046. doi: 10.1095/biolreprod59.5.1037 CrossRefGoogle ScholarPubMed
Aitken, R. J., De Iuliis, G. N., Finnie, J. M., Hedges, A. and McLachlan, R. I. (2010). Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: Development of diagnostic criteria. Human Reproduction, 25(10), 24152426. doi: 10.1093/humrep/deq214 CrossRefGoogle Scholar
Benchaib, M., Lornage, J., Mazoyer, C., Lejeune, H., Salle, B. and François Guerin, J. (2007). Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertility and Sterility, 87(1), 93100. doi: 10.1016/j.fertnstert.2006.05.057 CrossRefGoogle ScholarPubMed
Borini, A., Tarozzi, N., Bizzaro, D., Bonu, M. A. FAVA, Fava, L., Flamigni, C. and Coticchio, G., et al. (2006). Sperm DNA fragmentation: Paternal effect on early post-implantation embryo development in ART. Human Reproduction, 21(11), 28762881. doi: 10.1093/humrep/del251 CrossRefGoogle ScholarPubMed
Bungum, M., Humaidan, P., Spano, M., Jepson, K., Bungum, L. and Giwercman, A. (2004). The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Human Reproduction, 19(6), 14011408. doi: 10.1093/humrep/deh280 CrossRefGoogle ScholarPubMed
Bungum, M., Humaidan, P., Axmon, A., Spano, M., Bungum, L., Erenpreiss, J. and Giwercman, A. (2007). Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Human Reproduction, 22(1), 174179. doi: 10.1093/humrep/del326 CrossRefGoogle ScholarPubMed
Chabory, E., Damon, C., Lenoir, A., Kauselmann, G., Kern, H., Zevnik, B., Garrel, C., Saez, F., Cadet, R., Henry-Berger, J., Schoor, M., Gottwald, U., Habenicht, U., Drevet, J. R. and Vernet, P. (2009). Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. Journal of Clinical Investigation, 119(7), 20742085. doi: 10.1172/JCI38940 Google ScholarPubMed
Chandra, A., Martinez, G. M., Mosher, W. D., Abma, J. C. and Jones, J. (2005). Fertility, family planning, and reproductive health of U.S. women: Data from the 2002 National Survey of Family Growth. Vital and Health Statistics. Series 23, Data from the National Survey of Family Growth. Dec, 25(25), 1160.Google Scholar
Chatterjee, S. and Gagnon, C. (2001). Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Molecular Reproduction and Development, 59(4), 451458. doi: 10.1002/mrd.1052 CrossRefGoogle ScholarPubMed
Check, J. H., Graziano, V., Cohen, R., Krotec, J. and Check, M. L. (2005). Effect of an abnormal sperm chromatin structural assay (SCSA) on pregnancy outcome following (IVF) with ICSI in previous IVF failures. Archives of Andrology, 51(2), 121124. doi: 10.1080/014850190518125 CrossRefGoogle ScholarPubMed
Coates, A., Hesla, J. S., Hurliman, A., Coate, B., Holmes, E., Matthews, R., Mounts, E. L., Turner, K. J., Thornhill, A. R. and Griffin, D. K. (2015). Use of suboptimal sperm increases the risk of aneuploidy of the sex chromosomes in preimplantation blastocyst embryos. Fertility and Sterility Oct, 104(4), 866872. doi: 10.1016/j.fertnstert.2015.06.033 CrossRefGoogle ScholarPubMed
Collins, J. A., Barnhart, K. T. and Schlegel, P. N. (2008). Do sperm DNA integrity tests predict pregnancy with in vitro fertilization? Fertility and Sterility, 89(4), 823831. doi: 10.1016/j.fertnstert.2007.04.055 CrossRefGoogle ScholarPubMed
Dar, S., Grover, S. A., Moskovtsev, S. I., Swanson, S., Baratz, A. and Librach, C. L. (2013). In vitro fertilization intracytoplasmic sperm injection outcome in patients with a markedly high DNA fragmentation index (>50%). Fertility and Sterility, 100(1), 7580. doi: 10.1016/j.fertnstert.2013.03.011 CrossRefGoogle Scholar
De Iuliis, G. N., Thomson, L. K., Mitchell, L. A., Finnie, J. M., Koppers, A. J., Hedges, A., Nixon, B. and Aitken, R. J. (2009). DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2′-deoxyguanosine a marker of oxidative stress. Biology of Reproduction, 81(3), 517524. doi: 10.1095/biolreprod.109.076836 CrossRefGoogle ScholarPubMed
Franco, G., Scarselli, F., Casciani, V., De Nunzio, C., Dente, D., Leonardo, C., Greco, P. F., Greco, A., Minasi, M. G. and Greco, E. (2016). A novel stepwise micro-TESE approach in non obstructive azoospermia. BMC Urology, 16(1), 20. doi: 10.1186/s12894-016-0138-6 CrossRefGoogle ScholarPubMed
Frydman, N., Prisant, N., Hesters, L., Frydman, R., Tachdjian, G., Cohen-Bacrie, P. and Fanchin, R. (2008). Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertility and Sterility Jan, 89(1), 9297. doi: 10.1016/j.fertnstert.2007.02.022 CrossRefGoogle Scholar
Gandini, L., Lombardo, F., Paoli, D., Caruso, F., Eleuteri, P., Leter, G., Ciriminna, R., Culasso, F., Dondero, F., Lenzi, A. and Spanò, M. (2004). Full-term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Human Reproduction, 19(6), 14091417. doi: 10.1093/humrep/deh233 CrossRefGoogle ScholarPubMed
Giraud, M. N., Motta, C., Boucher, D. and Grizard, G. (2000). Membrane fluidity predicts the outcome of cryopreservation of human spermatozoa. Human Reproduction, 15(10), October 1, 21602164. doi: 10.1093/humrep/15.10.2160 CrossRefGoogle ScholarPubMed
Greco, E., Litwicka, K., Arrivi, C., Varricchio, M. T., Caragia, A., Greco, A., Minasi, M. G. and Fiorentino, F. (2016). The endometrial preparation for frozen–thawed euploid blastocyst transfer: A prospective randomized trial comparing clinical results from natural modified cycle and exogenous hormone stimulation with GnRH agonist. Journal of Assisted Reproduction and Genetics, 33(7), 873884. doi: 10.1007/s10815-016-0736-y CrossRefGoogle ScholarPubMed
Gutiérrez-Mateo, C., Colls, P., Sánchez-García, J., Escudero, T., Prates, R., Ketterson, K., Wells, D. and Munné, S. (2011). Validation of microarray comparative genomic hybridization for comprehensive chromosome analysis of embryos. Fertility and Sterility, 95(3), 953958. doi: 10.1016/j.fertnstert.2010.09.010 CrossRefGoogle ScholarPubMed
Hansen, M., Bower, C., Milne, E., de Klerk, N. and Kurinczuk, J. J. (2005). Assisted reproductive technologies and the risk of birth defects—A systematic review. Human Reproduction, 20(2), 328338. doi: 10.1093/humrep/deh593 CrossRefGoogle ScholarPubMed
Henkel, R., Kierspel, E., Hajimohammad, M., Stalf, T., Hoogendijk, C., Mehnert, C., Menkveld, R., Schill, W. B. and Kruger, T. F. (2003). DNA fragmentation of spermatozoa and assisted reproduction technology. Reproductive Biomedicine Online, 7(4), 477484. doi: 10.1016/s1472–6483(10)61893–7 CrossRefGoogle ScholarPubMed
Holubcová, Z., Blayney, M., Elder, K. and Schuh, M. (2015). Human oocytes. Error-prone chromosome-mediated spindle assembly favors chromosome segregation defects in human oocytes. Science, 348(6239), 11431147. doi: 10.1126/science.aaa9529 CrossRefGoogle ScholarPubMed
Jiang, L. Y., Yang, L. Y., Tong, X. M., Zhu, H. Y., Xue, Y. M., Xu, W. Z., Yang, Y. and Zhang, S. Y. (2015). Intracytoplasmic sperm injection fertilization rate does not depend on the proportion of round headed sperm, small acrosomal sperm, or morphologically normal sperm in patients with partial globozoospermia. Chinese Medical Journal, 128(12), 15901595. doi: 10.4103/0366-6999.158310 CrossRefGoogle ScholarPubMed
Keegan, B. R., Barton, S., Sanchez, X., Berkeley, A. S., Krey, L. C. and Grifo, J. (2007). Isolated teratozoospermia does not affect in vitro fertilization outcome and is not an indication for intracytoplasmic sperm injection. Fertility and Sterility, 88(6), 15831588. doi: 10.1016/j.fertnstert.2007.01.057 CrossRefGoogle Scholar
Kobayashi, H., Sato, A., Otsu, E., Hiura, H., Tomatsu, C., Utsunomiya, T., Sasaki, H., Yaegashi, N. and Arima, T. (2007). Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Human Molecular Genetics, 16(21), 25422551. doi: 10.1093/hmg/ddm187 CrossRefGoogle ScholarPubMed
Küpker, W., al-Hasani, S., Schulze, W., Kühnel, W., Schill, T., Felberbaum, R. and Diedrich, K. (1995). Morphology in intracytoplasmic sperm injection: Preliminary results. Journal of Assisted Reproduction and Genetics Oct, 12(9), 620626. doi: 10.1007/BF02212586 CrossRefGoogle ScholarPubMed
Kuwayama, M. (2007). Highly efficient vitrification for cryopreservation of human oocytes and embryos: The Cryotop method. Theriogenology, 67(1), 7380. doi: 10.1016/j.theriogenology.2006.09.014 CrossRefGoogle ScholarPubMed
Lane, M., McPherson, N. O., Fullston, T., Spillane, M., Sandeman, L., Kang, W. X. and Zander-Fox, D. L. (2014). Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring. PLoS One, 9(7), e100832. doi: 10.1371/journal.pone.0100832 CrossRefGoogle ScholarPubMed
Larson-Cook, K. L., Brannian, J. D., Hansen, K. A., Kasperson, K. M., Aamold, E. T. and Evenson, D. P. (2003). Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertility and Sterility, 80(4), 895902. doi: 10.1016/s0015-0282(03)01116-6 CrossRefGoogle ScholarPubMed
Lin, M. H., Kuo-Kuang Lee, R., Li, S. H., Lu, C. H., Sun, F. J. and Hwu, Y. M. (2008). Sperm chromatin structure assay parameters are not related to fertilization rates, embryo quality, and pregnancy rates in in vitro fertilization and intracytoplasmic sperm injection, but might be related to spontaneous abortion rates. Fertility and Sterility, 90(2), 352359. doi: 10.1016/j.fertnstert.2007.06.018 CrossRefGoogle Scholar
Litwicka, K., Mencacci, C., Arrivi, C., Varricchio, M. T., Caragia, A., Minasi, M. G. and Greco, E. (2018). HCG administration after endogenous LH rise negatively influences pregnancy rate in modified natural cycle for frozen–thawed euploid blastocyst transfer: A pilot study. Journal of Assisted Reproduction and Genetics, 35(3), 449455. doi: 10.1007/s10815-017-1089-x CrossRefGoogle ScholarPubMed
Lopes, S., Sun, J. G., Jurisicova, A., Meriano, J. and Casper, R. F. (1998). Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertility and Sterility, 69(3), 528532. doi: 10.1016/s0015-0282(97)00536-0 CrossRefGoogle ScholarPubMed
Lord, T. and Aitken, R. J. (2015). Fertilization stimulates 8-hydroxy-2′-deoxyguanosine repair and antioxidant activity to prevent mutagenesis in the embryo. Developmental Biology, 406(1), 113. doi: 10.1016/j.ydbio.2015.07.024 CrossRefGoogle ScholarPubMed
Lu, Y. H., Gao, H. J., Li, B. J., Zheng, Y. M., Ye, Y. H., Qian, Y. L., Xu, C. M., Huang, H. F. and Jin, F. (2012). Different sperm sources and parameters can influence intracytoplasmic sperm injection outcomes before embryo implantation. Journal of Zhejiang University. Science. B, 13(1), 110. doi: 10.1631/jzus.B1100216.CrossRefGoogle ScholarPubMed
Ludwig, M. (2005). Risk during pregnancy and birth after assisted reproductive technologies: An integral view of the problem. Seminars in Reproductive Medicine, 23(4), 363370. doi: 10.1055/s-2005-923394 CrossRefGoogle Scholar
Ludwig, A., Katalinic, A., Thyen, U., Sutcliffe, A. G., Diedrich, K. and Ludwig, M. (2009). Neuromotor development and mental health at 5.5 years of age of singletons born at term after intracytoplasmatic sperm injection ICSI: Results of a prospective controlled single-blinded study in Germany. Fertility and Sterility, 91(1), 125132. doi: 10.1016/j.fertnstert.2007.11.030 CrossRefGoogle ScholarPubMed
Lundin, K., Söderlund, B. and Hamberger, L. (1997). The relationship between sperm morphology and rates of fertilization, pregnancy and spontaneous abortion in an in-vitro fertilization/intracytoplasmic sperm injection programme. Human Reproduction, 12(12), 26762681. doi: 10.1093/humrep/12.12.2676 CrossRefGoogle Scholar
MacLennan, M., Crichton, J. H., Playfoot, C. J. and Adams, I. R. (2015). Oocyte development, meiosis and aneuploidy. Seminars in Cell and Developmental Biology, 45, 6876. doi: 10.1016/j.semcdb.2015.10.005 CrossRefGoogle ScholarPubMed
Mazzilli, R., Cimadomo, D., Vaiarelli, A., Capalbo, A., Dovere, L., Alviggi, E., Dusi, L., Foresta, C., Lombardo, F., Lenzi, A., Tournaye, H., Alviggi, C., Rienzi, L. and Ubaldi, F. M. (2017). Effect of the male factor on the clinical outcome of intracytoplasmic sperm injection combined with preimplantation aneuploidy testing: Observational longitudinal cohort study of 1,219 consecutive cycles. Fertility and Sterility, 108(6), 961972.e3. doi: 10.1016/j.fertnstert.2017.08.033 CrossRefGoogle ScholarPubMed
McKenzie, L. J., Kovanci, E., Amato, P., Cisneros, P., Lamb, D. and Carson, S. A. (2004). Pregnancy outcome of in vitro fertilization/intracytoplasmic sperm injection with profound teratospermia. Fertility and Sterility, 82(4), 847849. doi: 10.1016/j.fertnstert.2004.03.054 CrossRefGoogle ScholarPubMed
Minasi, M. G., Colasante, A., Riccio, T., Ruberti, A., Casciani, V., Scarselli, F., Spinella, F., Fiorentino, F., Varricchio, M. T. and Greco, E. (2016). Correlation between aneuploidy, standard morphology evaluation and morphokinetic development in 1730 biopsied blastocysts: A consecutive case series study. Human Reproduction, 31(10), 22452254. doi: 10.1093/humrep/dew183 CrossRefGoogle ScholarPubMed
Munné, S., Márquez, C., Reing, A., Garrisi, J. and Alikani, M. (1998). Chromosome abnormalities in embryos obtained after conventional in vitro fertilization and intracytoplasmic sperm injection. Fertility and Sterility, 69(5), 904908. doi: 10.1016/s0015-0282(98)00039-9 CrossRefGoogle ScholarPubMed
Nagy, Z. P., Liu, J., Joris, H., Verheyen, G., Tournaye, H., Camus, M., Derde, M. C., Devroey, P. and Van Steirteghem, A. C. (1995). The result of intracytoplasmic sperm injection is not related to any of the three basic sperm parameters. Human Reproduction, 10(5), 11231129. doi: 10.1093/oxfordjournals.humrep.a136104 CrossRefGoogle ScholarPubMed
Ozmen, B., Caglar, G. S., Koster, F., Schopper, B., Diedrich, K. and Al-Hasani, S. (2007). Relationship between sperm DNA damage, induced acrosome reaction and viability in ICSI patients. Reproductive Biomedicine Online, 15(2), 208214. doi: 10.1016/s1472-6483(10)60710-9 CrossRefGoogle ScholarPubMed
Rodrigo, L., Rubio, C., Peinado, V., Villamón, R., Al-Asmar, N., Remohí, J., Pellicer, A., Simón, C. and Gil-Salom, M. (2011). Testicular sperm from patients with obstructive and nonobstructive azoospermia: Aneuploidy risk and reproductive prognosis using testicular sperm from fertile donors as control samples. Fertility and Sterility, 95(3), 10051012. doi: 10.1016/j.fertnstert.2010.10.022 CrossRefGoogle ScholarPubMed
Simon, L., Proutski, I., Stevenson, M., Jennings, D., McManus, J., Lutton, D. and Lewis, S. E. (2013). Sperm DNA damage has a negative association with live-birth rates after IVF. Reproductive Biomedicine Online, 26(1), 6878. doi: 10.1016/j.rbmo.2012.09.019 CrossRefGoogle Scholar
Simon, L., Murphy, K., Shamsi, M. B., Liu, L., Emery, B., Aston, K. I., Hotaling, J. and Carrell, D. T. (2014). Paternal influence of sperm DNA integrity on early embryonic development. Human Reproduction, 29(11), 24022412. doi: 10.1093/humrep/deu228 CrossRefGoogle ScholarPubMed
Svalander, P., Jakobsson, A. H., Forsberg, A. S., Bengtsson, A. C. and Wikland, M. (1996). The outcome of intracytoplasmic sperm injection is unrelated to “strict criteria” sperm morphology. Human Reproduction, 11(5), 10191022. doi: 10.1093/oxfordjournals.humrep.a019289 CrossRefGoogle ScholarPubMed
Takahashi, M. (2012). Oxidative stress and redox regulation on in vitro development of mammalian embryos. Journal of Reproduction and Development, 58(1), 19. doi: 10.1262/jrd.11-138n CrossRefGoogle ScholarPubMed
Taşdemir, I., Taşdemir, M., Tavukçuoglu, S., Kahraman, S. and Biberoģlu, K. (1997). Effect of abnormal sperm head morphology on the outcome of intracytoplasmic sperm injection in humans. Human Reproduction, 12(6), 12141217. doi: 10.1093/humrep/12.6.1214 CrossRefGoogle ScholarPubMed
Tsai, C. C., Huang, F. J., Wang, L. J., Lin, Y. J., Kung, F. T., Hsieh, C. H. and Lan, K. C. (2011). Clinical outcomes and development of children born after intracytoplasmic sperm injection (ICSI) using extracted testicular sperm or ejaculated extreme severe oligo-astheno-teratozoospermia sperm: A comparative study. Fertility and Sterility Sep, 96(3), 567571. doi: 10.1016/j.fertnstert.2011.06.080, PubMed: 21880275CrossRefGoogle ScholarPubMed
Tsai, Y.-R., Huang, F.-J., Lin, P.-Y., Kung, F.-T., Lin, Y.-J. and Lan, K.-C. (2015). Clinical outcomes and development of children born to couples with obstructive and nonobstructive azoospermia undergoing testicular sperm extraction-intracytoplasmic sperm injection: A comparative study. Taiwanese Journal of Obstetrics and Gynecology, 54(2), 155159. doi: 10.1016/j.tjog.2014.03.005 CrossRefGoogle ScholarPubMed
Virro, M. R., Larson-Cook, K. L. and Evenson, D. P. (2004). Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertility and Sterility, 81(5), 12891295. doi: 10.1016/j.fertnstert.2003.09.063 CrossRefGoogle ScholarPubMed
Zini, A., Meriano, J., Kader, K., Jarvi, K., Laskin, C. A. and Cadesky, K. (2005). Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Human Reproduction, 20(12), 34763480. doi: 10.1093/humrep/dei266 CrossRefGoogle ScholarPubMed
Zini, A., Boman, J. M., Belzile, E. and Ciampi, A. (2008). Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: Systematic review and meta-analysis. Human Reproduction, 23(12), 26632668. doi: 10.1093/humrep/den321 CrossRefGoogle ScholarPubMed
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