Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T12:46:55.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of sperm preparation methods to improve the recovery of mature spermatozoa in sub-fertile males

Published online by Cambridge University Press:  08 July 2022

Chiara Fasano ,
Giuseppe D’Andolfi ,
Loredana Di Matteo ,
Claudia Forte ,
Brian Dale Open the ORCID record for Brian Dale [Opens in a new window]  and
Elisabetta Tosti Open the ORCID record for Elisabetta Tosti [Opens in a new window]
Chiara Fasano
Affiliation:
Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy
Giuseppe D’Andolfi
Affiliation:
Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy
Loredana Di Matteo
Affiliation:
Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy
Claudia Forte
Affiliation:
Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy
Brian Dale
Affiliation:
Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy
Elisabetta Tosti*
Affiliation:
Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy
*
Author for correspondence: Elisabetta Tosti. Centro Fecondazione Assistita (CFA), Via Tasso 480, 80123 Naples, Italy. Tel: +39 081641689. E-mail: elisabettatosti@yahoo.it
Get access Rights & Permissions [Opens in a new window]

Summary

The integrity of chromatin in the spermatozoon is essential for reproductive outcome. The aim of this study was to evaluate the most effective and cost-effective method to reduce the percentage of spermatozoa with defects in chromatin decondensation for use in assisted reproductive technologies (ART) procedures. Sperm samples from 15 sub-fertile males were examined at CFA Naples to determine the sperm decondensation index (SDI), using the aniline blue test, before and after preparation, comparing density gradients with two different swim-up approaches. All three techniques led to a reduction in decondensed spermatozoa with no statistical difference (P > 0.05) between the control and the treated sperm. In contrast, we found a highly significant decrease in SDI (P < 0.01) after the two swim-up methods in all the samples, confirming the efficacy of these methods in lowering the percentage of chromatin compaction damage. There was no statistical difference between the two swim-up methods, however swim-up from the pellet led to improved count, motility and the percentage of normal condensed spermatozoa. We suggest that swim-up from the pellet be used in ART on sub-fertile males, both to reduce cell stress by multiple centrifugation and improve the recovery rate of mature spermatozoa.

Keywords

Chromatin condensationGradientSperm preparationSpermatozoaSwim-up
Type
Research Article
Information
Zygote , Volume 30 , Issue 5 , October 2022 , pp. 664 - 673
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adiga, S. K.C. and Kumar, P. (2001). Influence of swim-up method on the recovery of spermatozoa from different types of semen samples. Journal of Assisted Reproduction and Genetics, 18(3), 160–164. doi: 10.1023/a:1009464121194 CrossRefGoogle ScholarPubMed
Agarwal, A. and Said, T. M. (2003). Role of sperm chromatin abnormalities and DNA damage in male infertility. Human Reproduction Update, 9(4), 331–345. doi: 10.1093/humupd/dmg027 CrossRefGoogle ScholarPubMed
Aitken, R. J. (2017). Reactive oxygen species as mediators of sperm capacitation and pathological damage. Molecular Reproduction and Development, 84(10), 1039–1052. doi: 10.1002/mrd.22871 CrossRefGoogle ScholarPubMed
Aitken, R. J. and Clarkson, J. S. (1988). Significance of reactive oxygen species and antioxidants in defining the efficacy of sperm preparation techniques. Journal of Andrology, 9(6), 367–376. doi: 10.1002/j.1939-4640.1988.tb01067.x CrossRefGoogle ScholarPubMed
Aitken, R. J., Buckingham, D., West, K., Wu, F. C., Zikopoulos, K. and Richardson, D. W. (1992). Differential contribution of leucocytes and spermatozoa to the generation of reactive oxygen species in the ejaculates of oligozoospermic patients and fertile donors. Reproduction, 94(2), 451–462. doi: 10.1530/jrf.0.0940451 CrossRefGoogle Scholar
Aitken, R. J., Jones, K. T. and Robertson, S. A. (2012). Reactive oxygen species and sperm function—In sickness and in health. Journal of Andrology, 33(6), 1096–1106. doi: 10.2164/jandrol.112.016535 CrossRefGoogle ScholarPubMed
Amaral, A., Lourenço, B., Marques, M. and Ramalho-Santos, J. (2013). Mitochondria functionality and sperm quality. Reproduction, 146(5), R163–R174. doi: 10.1530/REP-13-0178 CrossRefGoogle ScholarPubMed
Babakhanzadeh, E., Nazari, M., Ghasemifar, S. and Khodadadian, A. (2020). Some of the factors involved in male infertility: A prospective review. International Journal of General Medicine, 13, 29–41. doi: 10.2147/IJGM.S241099 CrossRefGoogle ScholarPubMed
Baldini, D., Baldini, A., Silvestris, E., Vizziello, G., Ferri, D. and Vizziello, D. (2020). A fast and safe technique for sperm preparation in ICSI treatments within a randomized controlled trial (RCT). Reproductive Biology and Endocrinology: RB&E, 18(1), 88. doi: 10.1186/s12958-020-00642-8 CrossRefGoogle Scholar
Balhorn, R., Cosman, M., Thornton, K., Krishnan, V., Corzett, M., Bench, G., Kramer, C., Hud, N., Allen, M. and Prieto, M. (1999). Protamine mediated condensation of DNA in mammalian sperm. In Gagnon, C. (Ed.), The male gamete: From basic science to clinical applications (pp. 55–70). Cache River Press.Google Scholar
Boissonneault, G. (2002). Chromatin remodeling during spermiogenesis: A possible role for the transition proteins in DNA strand break repair. FEBS Letters, 514(2–3), 111–114. doi: 10.1016/s0014-5793(02)02380-3 CrossRefGoogle ScholarPubMed
Booze, M., Brannian, J., Von Wald, T., Hansen, K. and Evenson, D. (2019). High DNA stability in the SCSA is associated with poor embryo development and live birth outcome. In American Association of bioanalysts conference (pp. 16–18).Google Scholar
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), 174–179. doi: 10.1093/humrep/del326 CrossRefGoogle ScholarPubMed
Caron, C., Govin, J., Rousseaux, S. and Khochbin, S. (2005). How to pack the genome for a safe trip. In Jeanteur, P. (Ed.), Epigenetics and chromatin, 38 (pp. 65–89). Springer-Verlag.CrossRefGoogle Scholar
Coughlan, C., Clarke, H., Cutting, R., Saxton, J., Waite, S., Ledger, W., Li, T. and Pacey, A. A. (2015). Sperm DNA fragmentation, recurrent implantation failure and recurrent miscarriage. Asian Journal of Andrology, 17(4), 681–685. doi: 10.4103/1008-682X.144946 Google ScholarPubMed
Couture, V., Delisle, S., Mercier, A. and Pennings, G. (2021). The other face of advanced paternal age: A scoping review of its terminological, social, public health, psychological, ethical and regulatory aspects. Human Reproduction Update, 27(2), 305–323. doi: 10.1093/humupd/dmaa046 CrossRefGoogle ScholarPubMed
Curry, M. and Watson, P. (1995). Sperm-structure and function. In Grudzinskas, J. G. & Yovich, J. L. (Eds.), Gametes: The spermatozoon (pp. 45–69). Cambridge University Press.Google Scholar
Dai, X., Wang, Y., Cao, F., Yu, C., Gao, T., Xia, X., Wu, J. and Chen, L. (2020). Sperm enrichment from poor semen samples by double density gradient centrifugation in combination with swim-up for IVF cycles. Scientific Reports, 10(1), 2286. doi: 10.1038/s41598-020-59347-y CrossRefGoogle ScholarPubMed
Dale, B., Wilding, M., Coppola, G. and Tosti, E. (2010). How do spermatozoa activate oocytes? Reproductive Biomedicine Online, 21(1), 1–3. doi: 10.1016/j.rbmo.2010.02.015 CrossRefGoogle ScholarPubMed
Daumler, D., Chan, P., Lo, K. C., Takefman, J. and Zelkowitz, P. (2016). Men’s knowledge of their own fertility: A population-based survey examining the awareness of factors that are associated with male infertility. Human Reproduction, 31(12), 2781–2790. doi: 10.1093/humrep/dew265 CrossRefGoogle ScholarPubMed
Edwards, R. G., Bavister, B. D. and Steptoe, P. C. (1969). Early stages of fertilization in vitro of human oocytes matured in vitro . Nature, 221(5181), 632–635. doi: 10.1038/221632a0 CrossRefGoogle ScholarPubMed
Edwards, R. G., Steptoe, P. C. and Purdy, J. M. (1980). Establishing full-term human pregnancies using cleaving embryos grown in vitro . British Journal of Obstetrics and Gynaecology, 87(9), 737–756. doi: 10.1111/j.1471-0528.1980.tb04610.x CrossRefGoogle ScholarPubMed
Erel, C. T., Senturk, L. M., Irez, T., Ercan, L., Elter, K., Colgar, U. and Ertungealp, E. (2000). Sperm-preparation techniques for men with normal and abnormal semen analysis. A comparison. Journal of Reproductive Medicine, 45(11), 917–922.Google ScholarPubMed
Esterhuizen, A. D., Franken, D. R., Lourens, J. G. H., Van Zyl, C., Müller, I. I. and Van Rooyen, L. H. (2000). Chromatin packaging as an indicator of human sperm dysfunction. Journal of Assisted Reproduction and Genetics, 17(9), 508–514. doi: 10.1023/a:1009493824953 CrossRefGoogle ScholarPubMed
Esterhuizen, A. D., Franken, D. R., Becker, P. J., Lourens, J. G. H., Müller, I. I. and van Rooyen, L. H. (2002). Defective sperm decondensation: A cause for fertilization failure. Andrologia, 34(1), 1–7. doi: 10.1046/j.0303-4569.2001.00423.x CrossRefGoogle ScholarPubMed
Evenson, D. and Jost, L. (2000). Sperm chromatin structure assay is useful for fertility assessment. Methods in Cell Science, 22(2–3), 169–189. doi: 10.1023/a:1009844109023 CrossRefGoogle ScholarPubMed
Evenson, D. P. and Wixon, R. (2006). Clinical aspects of sperm DNA fragmentation detection and male infertility. Theriogenology, 65(5), 979–991. doi: 10.1016/j.theriogenology.2005.09.011 CrossRefGoogle ScholarPubMed
Evenson, D. P., Witkin, S. S., de Harven, E. and Bendich, A. (1978). Ultrastructure of partially decondensed human spermatozoal chromatin. Journal of Ultrastructure Research, 63(2), 178–187. doi: 10.1016/s0022-5320(78)80073-2 CrossRefGoogle ScholarPubMed
Evenson, D. P., Jost, L. K., Marshall, D., Zinaman, M. J., Clegg, E., Purvis, K., de Angelis, P. and Claussen, O. P. (1999). Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Human Reproduction, 14(4), 1039–1049. doi: 10.1093/humrep/14.4.1039 CrossRefGoogle ScholarPubMed
Evenson, D. P., Larson, K. L. and Jost, L. K. (2002). Sperm chromatin structure assay: Its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. Journal of Andrology, 23(1), 25–43. doi: 10.1002/j.1939-4640.2002.tb02599.x CrossRefGoogle ScholarPubMed
Gallo, A., Boni, R. and Tosti, E. (2020). Gamete quality in a multistressor environment. Environment International, 138, 105627. doi: 10.1016/j.envint.2020.105627 CrossRefGoogle Scholar
Galotto, C., Cambiasso, M. Y., Julianelli, V. L., Valzacchi, G. J. R., Rolando, R. N., Rodriguez, M. L., Calvo, L., Calvo, J. C. and Romanato, M. (2019). Human sperm decondensation in vitro is related to cleavage rate and embryo quality in IVF. Journal of Assisted Reproduction and Genetics, 36(11), 2345–2355. doi: 10.1007/s10815-019-01590-y CrossRefGoogle ScholarPubMed
Gandini, L., Lombardo, F., Paoli, D., Caruso, F., Eleuteri, P., Leter, G., Ciriminna, R., Culasso, F., Dondero, F., Lenzi, A. and Spanó, M. (2004). Full-term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Human Reproduction, 19(6), 1409–1417. doi: 10.1093/humrep/deh233 CrossRefGoogle ScholarPubMed
Gellert-Mortimer, S. T., Clarke, G. N., Baker, H. W. G., Hyne, R. V. and Johnston, W. I. H. (1988). Evaluation of Nycodenz**Nyegaard and Co., Oslo, Norway. and Percoll††Pharmacia. Fertility and Sterility. Uppsala, 49(2), 335–341. doi: 10.1016/s0015-0282(16)59725-8 CrossRefGoogle Scholar
Ghaleno, L. R., Valojerdi, M. R., Janzamin, E., Chehrazi, M., Sharbatoghli, M. and Yazdi, R. S. (2014). Evaluation of conventional semen parameters, intracellular reactive oxygen species, DNA fragmentation and dysfunction of mitochondrial membrane potential after semen preparation techniques: A flow cytometric study. Archives of Gynecology and Obstetrics, 289(1), 173–180. doi: 10.1007/s00404-013-2946-1 CrossRefGoogle ScholarPubMed
Gill, K., Jakubik-Uljasz, J., Rosiak-Gill, A., Grabowska, M., Matuszewski, M. and Piasecka, M. (2020). Male aging as a causative factor of detrimental changes in human conventional semen parameters and sperm DNA integrity. Aging Male, 23(5), 1321–1332. doi: 10.1080/13685538.2020.1765330 CrossRefGoogle ScholarPubMed
Giwercman, A., Lindstedt, L., Larsson, M., Bungum, M., Spano, M., Levine, R. J. and Rylander, L. (2010). Sperm chromatin structure assay as an independent predictor of fertility in vivo: A case–control study. International Journal of Andrology, 33(1), e221–e227. doi: 10.1111/j.1365-2605.2009.00995.x CrossRefGoogle ScholarPubMed
Gorus, F. K. and Pipeleers, D. G. (1981). A rapid method for the fractionation of human spermatozoa according to their progressive motility. Fertility and Sterility, 35(6), 662–665. doi: 10.1016/s0015-0282(16)45561-5 CrossRefGoogle ScholarPubMed
Haddad, M., Stewart, J., Xie, P., Cheung, S., Trout, A., Keating, D., Parrella, A., Lawrence, S., Rosenwaks, Z. and Palermo, G. D. (2021). Thoughts on the popularity of ICSI. Journal of Assisted Reproduction and Genetics, 38(1), 101–123. doi: 10.1007/s10815-020-01987-0 CrossRefGoogle ScholarPubMed
Hammadeh, M. E., Stieber, M., Haidl, G. and Schmidt, W. (1998). Association between sperm cell chromatin condensation, morphology based on strict criteria, and fertilization, cleavage and pregnancy rates in an IVF program. Andrologia, 30(1), 29–35. doi: 10.1111/j.1439-0272.1998.tb01379.x CrossRefGoogle Scholar
Hao, S. L., Ni, F. D. and Yang, W. X. (2019). The dynamics and regulation of chromatin remodeling during spermiogenesis. Gene, 706, 201–210. doi: 10.1016/j.gene.2019.05.027 CrossRefGoogle ScholarPubMed
Henkel, R. (2012). Sperm preparation: State-of-the-art—Physiological aspects and application of advanced sperm preparation methods. Asian Journal of Andrology, 14(2), 260–269. doi: 10.1038/aja.2011.133 CrossRefGoogle ScholarPubMed
Henkel, R. R. and Schill, W. B. (2003). Sperm preparation for ART. Reproductive Biology and Endocrinology: RB&E, 1, 108. doi: 10.1186/1477-7827-1-108 CrossRefGoogle ScholarPubMed
Henkel, R. R., Franken, D. R., Lombard, C. J. and Schill, W. B. (1994). Selective capacity of glass-wool filtration for the separation of human spermatozoa with condensed chromatin: A possible therapeutic modality for male-factor cases? Journal of Assisted Reproduction and Genetics, 11(8), 395–400. doi: 10.1007/BF02211725 CrossRefGoogle ScholarPubMed
Ihara, M., Meyer-Ficca, M. L., Leu, N. A., Rao, S., Li, F., Gregory, B. D., Zalenskaya, I. A., Schultz, R. M. and Meyer, R. G. (2014). Paternal poly (ADP-ribose) metabolism modulates retention of inheritable sperm histones and early embryonic gene expression. PLOS Genetics, 10(5), e1004317. doi: 10.1371/journal.pgen.1004317 CrossRefGoogle ScholarPubMed
Irez, T., Sahmay, S., Ocal, P., Goymen, A., Senol, H., Erol, N., Kaleli, S. and Guralp, O. (2015). Investigation of the association between the outcomes of sperm chromatin condensation and decondensation tests, and assisted reproduction techniques. Andrologia, 47(4), 438–447. doi: 10.1111/and.12286 CrossRefGoogle ScholarPubMed
Irez, T., Dayioglu, N., Alagöz, M., Karatas, S. and Güralp, O. (2018). The use of aniline blue chromatin condensation test on prediction of pregnancy in mild male factor and unexplained male infertility. Andrologia, 50(10), e13111. doi: 10.1111/and.13111 CrossRefGoogle ScholarPubMed
Iwasaki, A. and Gagnon, C. (1992). Formation of reactive oxygen species in spermatozoa of infertile patients. Fertility and Sterility, 57(2), 409–416. doi: 10.1016/s0015-0282(16)54855-9 CrossRefGoogle ScholarPubMed
Jerre, E., Bungum, M., Evenson, D. and Giwercman, A. (2019). Sperm chromatin structure assay high DNA stainability sperm as a marker of early miscarriage after intracytoplasmic sperm injection. Fertility and Sterility, 112(1), 46–53.e2. doi: 10.1016/j.fertnstert.2019.03.013 CrossRefGoogle ScholarPubMed
Karydis, S., Asimakopoulos, B., Papadopoulos, N., Vakalopoulos, I., Al-Hasani, S. and Nikolettos, N. (2005). ICSI outcome is not associated with the incidence of spermatozoa with abnormal chromatin condensation. In Vivo, 19(5), 921–925.Google Scholar
Kazerooni, T., Asadi, N., Jadid, L., Kazerooni, M., Ghanadi, A., Ghaffarpasand, F., Kazerooni, Y. and Zolghadr, J. (2009). Evaluation of sperm’s chromatin quality with acridine orange test, chromomycin A3 and aniline blue staining in couples with unexplained recurrent abortion. Journal of Assisted Reproduction and Genetics, 26(11–12), 591–596. doi: 10.1007/s10815-009-9361-3 CrossRefGoogle ScholarPubMed
Kim, H. S., Kang, M. J., Kim, S. A., Oh, S. K., Kim, H., Ku, S. Y., Kim, S. H., Moon, S. Y. and Choi, Y. M. (2013). The utility of sperm DNA damage assay using toluidine blue and aniline blue staining in routine semen analysis. Clinical and Experimental Reproductive Medicine, 40(1), 23–28. doi: 10.5653/cerm.2013.40.1.23 CrossRefGoogle ScholarPubMed
Krüger, T. F., Acosta, A. A., Simmons, K. F., Swanson, R. J., Matta, J. F., Veeck, L. L., Morshedi, M. and Brugo, S. (1987). New method of evaluating sperm morphology with predictive value for human in vitro fertilization. Urology, 30(3), 248–251. doi: 10.1016/0090-4295(87)90246-9 CrossRefGoogle ScholarPubMed
Kutchy, N. A., Menezes, E. S. B., Ugur, M. R., Ul Husna, A., ElDebaky, H., Evans, H. C., Beaty, E., Santos, F. C., Tan, W., Wills, R. W., Topper, E., Kaya, A., Moura, A. A. and Memili, E. (2019). Sperm cellular and nuclear dynamics associated with bull fertility. Animal Reproduction Science, 211, 106203. doi: 10.1016/j.anireprosci.2019.106203 CrossRefGoogle ScholarPubMed
Lefièvre, L., Bedu-Addo, K., Conner, S. J., Machado-Oliveira, G. S. M., Chen, Y., Kirkman-Brown, J. C., Afnan, M. A., Publicover, S. J., Ford, W. C. L. and Barratt, C. L. R. (2007). Counting sperm does not add up any more: Time for a new equation? Reproduction, 133(4), 675–684. doi: 10.1530/REP-06-0332 CrossRefGoogle Scholar
Lewis, S. E. M. and Aitken, R. J. (2005). DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell and Tissue Research, 322(1), 33–41. doi: 10.1007/s00441-005-1097-5 CrossRefGoogle ScholarPubMed
Lewis, S. E. M., Agbaje, I. and Alvarez, J. (2008). Sperm DNA tests as useful adjuncts to semen analysis. Systems Biology in Reproductive Medicine, 54(3), 111–125. doi: 10.1080/19396360801957739 CrossRefGoogle ScholarPubMed
Li, Z., Zhou, Y., Liu, R., Lin, H., Liu, W., Xiao, W. and Lin, Q. (2012). Effects of semen processing on the generation of reactive oxygen species and mitochondrial membrane potential of human spermatozoa. Andrologia, 44(3), 157–163. doi: 10.1111/j.1439-0272.2010.01123.x 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), 352–359. doi: 10.1016/j.fertnstert.2007.06.018 CrossRefGoogle Scholar
Manicardi, G. C., Bianchi, P. G., Pantano, S., Azzoni, P., Bizzaro, D., Bianchi, U. and Sakkas, D. (1995). Presence of endogenous nicks in DNA of ejaculated human spermatozoa and its relationship to chromomycin A3 accessibility. Biology of Reproduction, 52(4), 864–867. doi: 10.1095/biolreprod52.4.864 CrossRefGoogle ScholarPubMed
Matsuura, R., Takeuchi, T. and Yoshida, A. (2010). Preparation and incubation conditions affect the DNA integrity of ejaculated human spermatozoa. Asian Journal of Andrology, 12(5), 753–759. doi: 10.1038/aja.2010.46 CrossRefGoogle ScholarPubMed
Meitei, H. Y., Uppangala, S., Sharan, K., Chandraguthi, S. G., Radhakrishnan, A., Kalthur, G., Schlatt, S. and Adiga, S. K. (2021). A simple, centrifugation-free, sperm-sorting device eliminates the risks of centrifugation in the swim-up method while maintaining functional competence and DNA integrity of selected spermatozoa. Reproductive Sciences, 28(1), 134–143. doi: 10.1007/s43032-020-00269-5 CrossRefGoogle ScholarPubMed
Ménézo, Y. (2021). Evaluation of the human sperm nucleus: Ambiguity and risk of confusion with chromomycin staining. Zygote, 29(4), 257–259. doi: 10.1017/S0967199420000672 CrossRefGoogle ScholarPubMed
Ménézo, Y. J., Hazout, A., Panteix, G., Robert, F., Rollet, J., Cohen-Bacrie, P., Chapuis, F., Clément, P. and Benkhalifa, M. (2007). Antioxidants to reduce sperm DNA fragmentation: An unexpected adverse effect. Reproductive Biomedicine Online, 14(4), 418–421. doi: 10.1016/s1472-6483(10)60887-5 CrossRefGoogle Scholar
Ménézo, Y., Dale, B. and Cohen, M. (2010). DNA damage and repair in human oocytes and embryos: A review. Zygote, 18(4), 357–365. doi: 10.1017/S0967199410000286 CrossRefGoogle ScholarPubMed
Mohamed, E. E. and Mohamed, M. A. (2012). Effect of sperm chromatin condensation on the outcome of intrauterine insemination in patients with male factor infertility. Journal of Reproductive Medicine, 57(9–10), 421–426.Google ScholarPubMed
Mortimer, D. (1991). Sperm preparation techniques and iatrogenic failures of in-vitro fertilization. Human Reproduction, 6(2), 173–176. doi: 10.1093/oxfordjournals.humrep.a137300 CrossRefGoogle ScholarPubMed
Muratori, M., Maggi, M., Spinelli, S., Filimberti, E., Forti, G. and Baldi, E. (2003). Spontaneous DNA fragmentation in swim-up selected human spermatozoa during long term incubation. Journal of Andrology, 24(2), 253–262. doi: 10.1002/j.1939-4640.2003.tb02670.x CrossRefGoogle ScholarPubMed
Muratori, M., Tamburrino, L., Marchiani, S., Cambi, M., Olivito, B., Azzari, C., Forti, G. and Baldi, E. (2015). Investigation on the origin of sperm DNA fragmentation: Role of apoptosis, immaturity and oxidative stress. Molecular Medicine, 21, 109–122. doi: 10.2119/molmed.2014.00158 CrossRefGoogle ScholarPubMed
Oseguera-López, I., Ruiz-Díaz, S., Ramos-Ibeas, P. and Pérez-Cerezales, S. (2019). Novel techniques of sperm selection for improving IVF and ICSI outcomes. Frontiers in Cell and Developmental Biology, 7, 298. doi: 10.3389/fcell.2019.00298 CrossRefGoogle ScholarPubMed
Palermo, G. D., O’Neill, C. L., Chow, S., Cheung, S., Parrella, A., Pereira, N. and Rosenwaks, Z. (2017). Intracytoplasmic sperm injection: State of the art in humans. Reproduction, 154(6), F93–F110. doi: 10.1530/REP-17-0374 CrossRefGoogle ScholarPubMed
Poccia, D. (1986). Remodeling of nucleoproteins during gametogenesis, fertilization, and early development. International Review of Cytology, 105, 1–65. doi: 10.1016/s0074-7696(08)61061-x CrossRefGoogle Scholar
Rahman, M. B., Schellander, K., Luceño, N. L. and Van Soom, A. (2018). Heat stress responses in spermatozoa: Mechanisms and consequences for cattle fertility. Theriogenology, 113, 102–112. doi: 10.1016/j.theriogenology.2018.02.012 CrossRefGoogle ScholarPubMed
Rathke, C., Baarends, W. M., Awe, S. and Renkawitz-Pohl, R. (2014). Chromatin dynamics during spermiogenesis. Biochimica et Biophysica Acta, 1839(3), 155–168. doi: 10.1016/j.bbagrm.2013.08.004 CrossRefGoogle ScholarPubMed
Rex, A. S., Aagaard, J. and Fedder, J. (2017). DNA fragmentation in spermatozoa: A historical review. Andrology, 5(4), 622–630. doi: 10.1111/andr.12381 CrossRefGoogle ScholarPubMed
Romero-Aguirregomezcorta, J., Laguna-Barraza, R., Fernández-González, R., Štiavnická, M., Ward, F., Cloherty, J., McAuliffe, D., Larsen, P. B., Grabrucker, A. M., Gutiérrez-Adán, A., Newport, D. and Fair, S. (2021). Sperm selection by rheotaxis improves sperm quality and early embryo development. Reproduction, 161(3), 343–352. doi: 10.1530/REP-20-0364 CrossRefGoogle ScholarPubMed
Sabeti, P. Pourmasumi, S., Rahiminia, T., Akyash, F. and Talebi, A. R. (2016). Etiologies of sperm oxidative stress. International Journal of Reproductive Biomedicine, 14, 231–240.Google ScholarPubMed
Sakkas, D., Manicardi, G. C., Tomlinson, M., Mandrioli, M., Bizzaro, D., Bianchi, P. G. and Bianchi, U. (2000). The use of two density gradient centrifugation techniques and the swim-up method to separate spermatozoa with chromatin and nuclear DNA anomalies. Human Reproduction, 15(5), 1112–1116. doi: 10.1093/humrep/15.5.1112 CrossRefGoogle ScholarPubMed
Sakkas, D., Urner, F., Bianchi, P. G., Bizzaro, D., Wagner, I., Jaquenoud, N., Manicardi, G. and Campana, A. (1996). Sperm chromatin anomalies can influence decondensation after intracytoplasmic sperm injection. Human Reproduction, 11(4), 837–843. doi: 10.1093/oxfordjournals.humrep.a019263 CrossRefGoogle ScholarPubMed
Sakkas, D., Urner, F., Bizzaro, D., Manicardi, G., Bianchi, P. G., Shoukir, Y. and Campana, A. (1998). Sperm nuclear DNA damage and altered chromatin structure: Effect on fertilization and embryo development. Human Reproduction, 13 Suppl. 4, 11–19. doi: 10.1093/humrep/13.suppl_4.11 CrossRefGoogle ScholarPubMed
Sánchez, R., Villagrán, E., Risopatrón, J. and Célis, R. (1994). Evaluation of nuclear maturity in human spermatozoa obtained by sperm-preparation methods. Andrologia, 26(3), 173–176. doi: 10.1111/j.1439-0272.1994.tb00784.x CrossRefGoogle ScholarPubMed
Saylan, A. and Erimsah, S. (2019). High quality human sperm selection for IVF: A study on sperm chromatin condensation. Acta histochemica, 121(7), 798–803. doi: 10.1016/j.acthis.2019.07.006 CrossRefGoogle Scholar
Sellami, A., Chakroun, N., Ben Zarrouk, S., Sellami, H., Kebaili, S., Rebai, T. and Keskes, L. (2013). Assessment of chromatin maturity in human spermatozoa: Useful aniline blue assay for routine diagnosis of male infertility. Advances in Urology, 2013, 578631. doi: 10.1155/2013/578631 CrossRefGoogle ScholarPubMed
Setti, A. S., Braga, D. P. A. F., Provenza, R. R., Iaconelli, A. and Borges, E. (2021). Oocyte ability to repair sperm DNA fragmentation: The impact of maternal age on intracytoplasmic sperm injection outcomes. Fertility and Sterility, 116(1), 123–129. doi: 10.1016/j.fertnstert.2020.10.045 CrossRefGoogle ScholarPubMed
Shamsi, M. B., Imam, S. N. and Dada, R. (2011). Sperm DNA integrity assays: Diagnostic and prognostic challenges and implications in management of infertility. Journal of Assisted Reproduction and Genetics, 28(11), 1073–1085. doi: 10.1007/s10815-011-9631-8 CrossRefGoogle ScholarPubMed
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), 2402–2412. doi: 10.1093/humrep/deu228 CrossRefGoogle ScholarPubMed
Simon, L., Emery, B. and Carrell, D. T. (2019). Sperm DNA fragmentation: consequences for reproduction. Advances in Experimental Medicine and Biology, 1166, 87–105. doi: 10.1007/978-3-030-21664-1_6 CrossRefGoogle ScholarPubMed
Soygur, B., Celik, S., Celik-Ozenci, C. and Sati, L. (2018). Effect of erythrocyte-sperm separation medium on nuclear, acrosomal, and membrane maturity parameters in human sperm. Journal of Assisted Reproduction and Genetics, 35(3), 491–501. doi: 10.1007/s10815-017-1085-1 CrossRefGoogle ScholarPubMed
Sreenivasa, G., Kavitha, P., Vineeth, V. S., Channappa, S. K. and Malini, S. S. N. (2012). Evaluation of in vitro sperm nuclear chromatin decondensation among different subgroups of infertile males in Mysore, India. Journal of Research in Medical Sciences: the Official Journal of Isfahan University of Medical Sciences, 17(5), 456–460.Google ScholarPubMed
Starosta, A., Gordon, C. E. and Hornstein, M. D. (2020). Predictive factors for intrauterine insemination outcomes: A review. Fertility Research and Practice, 6(1), 23. doi: 10.1186/s40738-020-00092-1 CrossRefGoogle ScholarPubMed
Takeshima, T., Yumura, Y., Kuroda, S., Kawahara, T., Uemura, H. and Iwasaki, A. (2017). Effect of density gradient centrifugation on reactive oxygen species in human semen. Systems Biology in Reproductive Medicine, 63(3), 192–198. doi: 10.1080/19396368.2017.1294214 CrossRefGoogle ScholarPubMed
Talebi, A. R., Vahidi, S., Aflatoonian, A., Ghasemi, N., Ghasemzadeh, J., Firoozabadi, R. D. and Moein, M. R. (2012). Cytochemical evaluation of sperm chromatin and DNA integrity in couples with unexplained recurrent spontaneous abortions. Andrologia, 44 Suppl. 1, 462–470. doi: 10.1111/j.1439-0272.2011.01206.x CrossRefGoogle ScholarPubMed
Tomlinson, M. J., Amissah-Arthur, J. B., Thompson, K. A., Kasraie, J. L. and Bentick, B. (1996). Prognostic indicators for intrauterine insemination (IUI): Statistical model for IUI success. Human Reproduction, 11(9), 1892–1896. doi: 10.1093/oxfordjournals.humrep.a019513 CrossRefGoogle ScholarPubMed
Torabi, F., Binduraihem, A. and Miller, D. (2017). Sedimentation properties in density gradients correspond with levels of sperm DNA fragmentation, chromatin compaction and binding affinity to hyaluronic acid. Reproductive Biomedicine Online, 34(3), 298–311. doi: 10.1016/j.rbmo.2016.11.011 CrossRefGoogle ScholarPubMed
Tosti, E. and Fortunato, A. (2012). Is sperm chromatin packaging relevant for IVF success? Journal of Fertilization, 01(2). doi: 10.4172/2165-7491.1000e107 Google Scholar
Tosti, E. and Ménézo, Y. (2016). Gamete activation: Basic knowledge and clinical applications. Human Reproduction Update, 22(4), 420–439. doi: 10.1093/humupd/dmw014 CrossRefGoogle ScholarPubMed
Twigg, J., Fulton, N., Gomez, E., Irvine, D. S. and Aitken, R. J. (1998a). Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: Lipid peroxidation, DNA fragmentation and effectiveness of antioxidants. Human Reproduction, 13(6), 1429–1436. doi: 10.1093/humrep/13.6.1429 CrossRefGoogle ScholarPubMed
Twigg, J., Irvine, D. S., Houston, P., Fulton, N., Michael, L. and Aitken, R. J. (1998b). Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: Protective significance of seminal plasma. Molecular Human Reproduction, 4(5), 439–445. doi: 10.1093/molehr/4.5.439 CrossRefGoogle ScholarPubMed
Vaughan, D. A. and Sakkas, D. (2019). Sperm selection methods in the 21st century. Biology of Reproduction, 101(6), 1076–1082. doi: 10.1093/biolre/ioz032 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), 1289–1295. doi: 10.1016/j.fertnstert.2003.09.063 CrossRefGoogle ScholarPubMed
Volpes, A., Sammartano, F., Rizzari, S., Gullo, S., Marino, A. and Allegra, A. (2016). The pellet swim-up is the best technique for sperm preparation during in vitro fertilization procedures. Journal of Assisted Reproduction and Genetics, 33(6), 765–770. doi: 10.1007/s10815-016-0696-2 CrossRefGoogle ScholarPubMed
Ward, W. S. (2010). Function of sperm chromatin structural elements in fertilization and development. Molecular Human Reproduction, 16(1), 30–36. doi: 10.1093/molehr/gap080 CrossRefGoogle ScholarPubMed
Ward, W. S. and Coffey, D. S. (1991). DNA packaging and organization in mammalian spermatozoa: Comparison with somatic cells. Biology of Reproduction, 44(4), 569–574. doi: 10.1095/biolreprod44.4.569 CrossRefGoogle ScholarPubMed
Wilding, M. and Dale, B. (1997). Sperm factor: What is it and what does it do? Molecular Human Reproduction, 3(3), 269–273. doi: 10.1093/molehr/3.3.269 CrossRefGoogle Scholar
World Health Organization. (2010). WHO Laboratory manual for the examination and processing of human semen.Google Scholar
Zalata, A., Hafez, T. and Comhaire, F. (1995). Evaluation of the role of reactive oxygen species in male infertility. Human Reproduction, 10(6), 1444–1451. doi: 10.1093/humrep/10.6.1444 CrossRefGoogle ScholarPubMed
Zhang, Z., Zhu, L. L., Jiang, H. S., Chen, H., Chen, Y. and Dai, Y. T. (2016). Predictors of pregnancy outcome for infertile couples attending IVF and ICSI programmes. Andrologia, 48(9), 874–881. doi: 10.1111/and.12525 CrossRefGoogle ScholarPubMed
Zhao, Y., Vlahos, N., Wyncott, D., Petrella, C., Garcia, J., Zacur, H. and Wallach, E. E. (2004). Impact of semen characteristics on the success of intrauterine insemination. Journal of Assisted Reproduction and Genetics, 21, 143–148. doi: 10.1023/b:jarg.0000031246.76666.f6 CrossRefGoogle ScholarPubMed
Zheng, W. W., Song, G., Wang, Q. L., Liu, S. W., Zhu, X. L., Deng, S. M., Zhong, A., Tan, Y. M. and Tan, Y. (2018). Sperm DNA damage has a negative effect on early embryonic development following in vitro fertilization. Asian Journal of Andrology, 20(1), 75–79. doi: 10.4103/aja.aja_19_17 CrossRefGoogle Scholar
Zini, A. (2011). Are sperm chromatin and DNA defects relevant in the clinic? Systems Biology in Reproductive Medicine, 57(1–2), 78–85. doi: 10.3109/19396368.2010.515704 CrossRefGoogle ScholarPubMed
Zini, A., Finelli, A., Phang, D. and Jarvi, K. (2000). Influence of semen processing technique on human sperm DNA integrity. Urology, 56(6), 1081–1084. doi: 10.1016/s0090-4295(00)00770-6 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), 2663–2668. doi: 10.1093/humrep/den321 CrossRefGoogle ScholarPubMed
Zorn, B., Vidmar, G. and Meden-Vrtovec, H. (2003). Seminal reactive oxygen species as predictors of fertilization, embryo quality and pregnancy rates after conventional in vitro fertilization and intracytoplasmic sperm injection. International Journal of Andrology, 26(5), 279–285. doi: 10.1046/j.1365-2605.2003.00424.x CrossRefGoogle ScholarPubMed