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Sperm DNA fragmentation measured by sperm chromatin dispersion impacts morphokinetic parameters, fertilization rate and blastocyst quality in ICSI treatments

Published online by Cambridge University Press:  26 May 2021

Shikai Wang Open the ORCID record for Shikai Wang [Opens in a new window] ,
Weihong Tan ,
Yueyue Huang ,
Xianbao Mao ,
Zhengda Li ,
Xiaohui Zhang ,
Pingpin Wei  and
Lintao Xue
Shikai Wang
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Weihong Tan
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Yueyue Huang
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Xianbao Mao
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Zhengda Li
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Xiaohui Zhang
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Pingpin Wei
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
Lintao Xue*
Affiliation:
Centre of Reproductive Medicine and Genetic, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China
*
Author for correspondence: Lintao Xue. Department of Reproductive Medicine and Genetics Centre, People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning, Guangxi, China, Taoyuan Road 6 Nanning530021, China. Tel: +86 771 2186483. E-mail: [email protected]
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Summary

To determine the effects of sperm DNA fragmentation (SDF) on embryo morphokinetic parameters, cleavage patterns and embryo quality, this retrospective study analyzed 151 intracytoplasmic sperm injection (ICSI) cycles (1152 embryos collected) between November 2016 and June 2019. SDF was assessed using sperm chromatin dispersion. The cycles were divided into two groups based on the SDF rate: SDF < 15% (n = 114) and SDF ≥ 15% (n = 37). The embryo morphokinetic parameters, cleavage patterns, and embryo quality were compared between the two groups. The morphokinetic parameters tPNf, t2, t3, t4, t5, t6, and t8 were achieved significantly earlier in the SDF < 15% group compared with in the SDF ≥ 15% group. The fertilization and 2PN rates seemed to be significantly higher in the SDF < 15% group compared with in the SDF ≥ 15% group, while the abnormal cleavage rates were similar. However, a significantly higher rate of chaotic cleavage (CC) was observed in the SDF ≥ 15% group. The D3 high-quality embryo and available embryo rates were similar between the two groups. The blastocyst formation, high-quality blastocyst, and available blastocyst rates in the SDF < 15% group were significantly higher than those in the SDF ≥ 15% group. With an increase in SDF level, the chemical pregnancy, clinical pregnancy and implantation rates tended to decrease, while the miscarriage rate increased. This study demonstrated that SDF ≥ 15% reduces the fertilization rate of ICSI cycles and affects certain morphokinetic parameters. A higher SDF level can also induce a higher rate of CC, with subsequent decreases in the blastocyst formation rate and blastocyst quality.

Keywords

Cleavage patternEmbryo qualityICSIMorphokinetic parametersSperm DNA fragmentation
Type
Research Article
Information
Zygote , Volume 30 , Issue 1 , February 2022 , pp. 72 - 79
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Agarwal, A and Allamaneni, SS (2005). Sperm DNA damage assessment: a test whose time has come. Fertil Steril 84, 850–3.CrossRefGoogle ScholarPubMed
Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology (2011). The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod 26, 1270–83.CrossRefGoogle Scholar
Anifandis, G, Bounartzi, T, Messini, CI, Dafopoulos, K, Markandona, R, Sotiriou, S, Tzavella, A and Messinis, IE (2015). Sperm DNA fragmentation measured by Halosperm does not impact on embryo quality and ongoing pregnancy rates in IVF/ICSI treatments. Andrologia 47, 295–302.CrossRefGoogle Scholar
Antonouli, S, Papatheodorou, A, Panagiotidis, Y, Petousis, S, Prapas, N, Nottola, SA, Palmerini, MG, Macchiarelli, G and Prapas, Y (2019). The impact of sperm DNA fragmentation on ICSI outcome in cases of donated oocytes. Arch Gynecol Obstet 300, 207–15.CrossRefGoogle ScholarPubMed
Athayde, WK, Chen, AA, Conaghan, J, Ivani, K, Gvakharia, M, Behr, B, Suraj, V, Tan, L and Shen, S (2014). Atypical embryo phenotypes identified by time-lapse microscopy: high prevalence and association with embryo development. Fertil Steril 101, 1637–48.CrossRefGoogle Scholar
Benchaib, M, Lornage, J, Mazoyer, C, Lejeune, H, Salle, B and Francois, GJ (2007). Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril 87, 93–100.CrossRefGoogle ScholarPubMed
Borges, EJ, Zanetti, BF, Setti, AS, Braga, D, Provenza, RR and Iaconelli, AJ (2019). Sperm DNA fragmentation is correlated with poor embryo development, lower implantation rate, and higher miscarriage rate in reproductive cycles of non-male factor infertility. Fertil Steril 112, 483–90.CrossRefGoogle ScholarPubMed
Borini, A, Tarozzi, N, Bizzaro, D, Bonu, MA, Fava, L, Flamigni, C and Coticchio, G (2006). Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Hum Reprod 21, 2876–81.CrossRefGoogle ScholarPubMed
Boushaba, S and Belaaloui, G (2015). Sperm DNA fragmentation and standard semen parameters in algerian infertile male partners. World J Mens Health 33, 1–7.CrossRefGoogle ScholarPubMed
Bronet, F, Martinez, E, Gaytan, M, Linan, A, Cernuda, D, Ariza, M, Nogales, M, Pacheco, A, San, CM and Garcia-Velasco, JA (2012). Sperm DNA fragmentation index does not correlate with the sperm or embryo aneuploidy rate in recurrent miscarriage or implantation failure patients. Hum Reprod 27, 1922–9.CrossRefGoogle ScholarPubMed
Chatzimeletiou, K, Rutherford, AJ, Griffin, DK and Handyside, AH (2007). Is the sperm centrosome to blame for the complex polyploid chromosome patterns observed in cleavage stage embryos from an OAT patient? Zygote 15, 81–90.CrossRefGoogle ScholarPubMed
Chia, SE, Tay, SK and Lim, ST (1998). What constitutes a normal seminal analysis? Semen parameters of 243 fertile men. Hum Reprod 13, 3394–8.CrossRefGoogle ScholarPubMed
Chohan, KR, Griffin, JT, Lafromboise, M, De Jonge, CJ and Carrell, DT (2006). Comparison of chromatin assays for DNA fragmentation evaluation in human sperm. J Androl 27, 53–9.CrossRefGoogle ScholarPubMed
Ciray, HN, Campbell, A, Agerholm, IE, Aguilar, J, Chamayou, S, Esbert, M and Sayed, S (2014). Proposed guidelines on the nomenclature and annotation of dynamic human embryo monitoring by a time-lapse user group. Hum Reprod 29, 2650–60.CrossRefGoogle ScholarPubMed
Dar, S, Grover, SA, Moskovtsev, SI, Swanson, S, Baratz, A and Librach, CL (2013). In vitro fertilization-intracytoplasmic sperm injection outcome in patients with a markedly high DNA fragmentation index (>50%). Fertil Steril 100, 75–80.CrossRefGoogle Scholar
Enciso, M, Pieczenik, G, Cohen, J and Wells, D (2012). Development of a novel synthetic oligopeptide for the detection of DNA damage in human spermatozoa. Hum Reprod 27, 2254–66.CrossRefGoogle ScholarPubMed
Esbert, M, Pacheco, A, Vidal, F, Florensa, M, Riqueros, M, Ballesteros, A, Garrido, N and Calderon, G (2011). Impact of sperm DNA fragmentation on the outcome of IVF with own or donated oocytes. Reprod Biomed Online 23, 704–10.CrossRefGoogle ScholarPubMed
Evenson, DP, Larson, KL and Jost, LK (2002). Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 23, 25–43.CrossRefGoogle ScholarPubMed
Fei, Q, Huang, H, Jin, J and Huang, X (2014). Diagnostic value of sperm DNA fragmentation for male infertility. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 31, 60–4. [in Chinese]Google ScholarPubMed
Fernandez, JL, Muriel, L, Goyanes, V, Segrelles, E, Gosalvez, J, Enciso, M, LaFromboise, M and Dejonge, C (2005). Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertil Steril 84, 833–42.CrossRefGoogle ScholarPubMed
Galliano, D, Bellver, J, Diaz-Garcia, C, Simon, C and Pellicer, A (2015). ART and uterine pathology: how relevant is the maternal side for implantation? Hum Reprod Update 21, 13–38.CrossRefGoogle ScholarPubMed
Gardner, DK, Lane, M, Stevens, J, Schlenker, T and Schoolcraft, WB (2000). Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril 73, 1155–8.CrossRefGoogle ScholarPubMed
Gat, I, Tang, K, Quach, K, Kuznyetsov, V, Antes, R, Filice, M, Zohni, K and Librach, C (2017). Sperm DNA fragmentation index does not correlate with blastocyst aneuploidy or morphological grading. PLoS One 12, e179002.CrossRefGoogle ScholarPubMed
Gryshchenko, MG, Pravdyuk, AI and Parashchyuk, VY (2014). Analysis of factors influencing morphokinetic characteristics of embryos in ART cycles. Gynecol Endocrinol 30(Suppl 1), 6–8.CrossRefGoogle ScholarPubMed
Kalatova, B, Jesenska, R, Hlinka, D and Dudas, M (2015). Tripolar mitosis in human cells and embryos: occurrence, pathophysiology and medical implications. Acta Histochem 117, 111–25.CrossRefGoogle ScholarPubMed
Kamath, MS, Mascarenhas, M, Kirubakaran, R, Nair, R and Kulkarni, A (2018). Use of embryo culture supernatant to improve clinical outcomes in assisted reproductive technology: a systematic review and meta-analysis. Hum Fertil (Camb) 21, 90–7.CrossRefGoogle ScholarPubMed
Kazdar, N, Brugnon, F, Bouche, C, Jouve, G, Veau, S, Drapier, H, Rousseau, C, Pimentel, C, Viard, P, Belaud-Rotureau, MA and Ravel, C (2017). Comparison of human embryomorphokinetic parameters in sequential or global culture media. Ann Biol Clin (Paris) 75, 403–10.Google ScholarPubMed
Liu, Y, Chapple, V, Roberts, P and Matson, P (2014). Prevalence, consequence, and significance of reverse cleavage by human embryos viewed with the use of the Embryoscope time-lapse video system. Fertil Steril 102, 1295–300.CrossRefGoogle ScholarPubMed
Liu, Y, Chapple, V, Feenan, K, Roberts, P and Matson, P (2016). Time-lapse deselection model for human day 3 in vitro fertilization embryos: the combination of qualitative and quantitative measures of embryo growth. Fertil Steril 105, 656–62.CrossRefGoogle ScholarPubMed
Liu, Y, Feenan, K, Chapple, V and Matson, P (2019). Assessing efficacy of day 3 embryo time-lapse algorithms retrospectively: impacts of dataset type and confounding factors. Hum Fertil (Camb) 22, 182–90.CrossRefGoogle ScholarPubMed
Lundberg, T, Hambiliki, F, Sondèn, F, Akerlund, E and Bungum, M (2014). Evaluation of sperm DNA integrity and its effect on embryo development using time-lapse microscopy. Fertil Steril 102, e312.CrossRefGoogle Scholar
Ma, NZ, Chen, L, Hu, LL, Dai, W, Bu, ZQ and Sun, YP (2018). The influence of male age on treatment outcomes and neonatal birthweight following assisted reproduction technology involving intracytoplasmic sperm injection (ICSI) cycles. Andrologia 50, e12826.CrossRefGoogle ScholarPubMed
Maettner, R, Sterzik, K, Isachenko, V, Strehler, E, Rahimi, G, Alabart, JL, Sanchez, R, Mallmann, P and Isachenko, E (2014). Quality of human spermatozoa: relationship between high-magnification sperm morphology and DNA integrity. Andrologia 46, 547–55.CrossRefGoogle ScholarPubMed
Martin, JH, John, AR, Bromfield, EG and Brett, N (2018). DNA damage and repair in the female germline: contributions to ART. Hum Reprod Update 25, 180–201.CrossRefGoogle Scholar
Milewski, R, Kuc, P, Kuczynska, A, Stankiewicz, B, Lukaszuk, K and Kuczynski, W (2015). A predictive model for blastocyst formation based on morphokinetic parameters in time-lapse monitoring of embryo development. J Assist Reprod Genet 32, 571–9.CrossRefGoogle ScholarPubMed
Montag, M, Liebenthron, J and Koster, M (2011). Which morphological scoring system is relevant in human embryo development? Placenta 32(Suppl 3), S252–6.CrossRefGoogle ScholarPubMed
Moon, SY, Kim, SH, Jung, BJ, Jee, BC, Suh, CS and Lee, JY (2000). Influence of female age on pregnancy outcome in in vitro fertilization and embryo transfer patients undergoing intracytoplasmic sperm injection. J Obstet Gynaecol Res 26, 49–54.CrossRefGoogle ScholarPubMed
Osman, A, Alsomait, H, Seshadri, S, El-Toukhy, T and Khalaf, Y (2015). The effect of sperm DNA fragmentation on live birth rate after IVF or ICSI: a systematic review and meta-analysis. Reprod Biomed Online 30, 120–7.CrossRefGoogle ScholarPubMed
Sakkas, D and Alvarez, JG (2010). Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 93, 1027–36.CrossRefGoogle Scholar
Sathananthan, AH (1998). Paternal centrosomal dynamics in early human development and infertility. J Assist Reprod Genet 15, 129–39.CrossRefGoogle ScholarPubMed
Scarselli, F, Casciani, V, Cursio, E, Muzzi, S, Colasante, A, Gatti, S, Greco, MC, Greco, P, Minasi, MG and Greco, E (2018). Influence of human sperm origin, testicular or ejaculated, on embryo morphokinetic development. Andrologia 50, e13061.CrossRefGoogle ScholarPubMed
Scully, R, Panday, A, Elango, R and Willis, NA (2019). DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat Rev Mol Cell Biol 20, 698–714.CrossRefGoogle ScholarPubMed
Simon, L, Lutton, D, McManus, J and Lewis, SE (2011). Sperm DNA damage measured by the alkaline Comet assay as an independent predictor of male infertility and in vitro fertilization success. Fertil Steril 95, 652–7.CrossRefGoogle ScholarPubMed
Siristatidis, CS, Sertedaki, E and Vaidakis, D (2017). Metabolomics for improving pregnancy outcomes in women undergoing assisted reproductive technologies. Cochrane Database Syst Rev 5, CD11872.CrossRefGoogle Scholar
Stevenson, VA, Kramer, J, Kuhn, J and Theurkauf, WE (2001). Centrosomes and the Scrambled protein coordinate microtubule-independent actin reorganization. Nat Cell Biol 3, 68–75.CrossRefGoogle ScholarPubMed
Storr, A, Venetis, CA, Cooke, S, Susetio, D, Kilani, S and Ledger, W (2015). Morphokinetic parameters using time-lapse technology and day 5 embryo quality: a prospective cohort study. J Assist Reprod Genet 32, 1151–60.CrossRefGoogle ScholarPubMed
Sun, TC, Zhang, Y, Li, HT, Liu, XM, Yi, DX, Tian, L and Liu, YX (2018). Sperm DNA fragmentation index, as measured by sperm chromatin dispersion, might not predict assisted reproductive outcome. Taiwan J Obstet Gynecol 57, 493–8.CrossRefGoogle Scholar
Swiatecka, J, Bielawski, T, Anchim, T, Lesniewska, M, Milewski, R and Wolczynski, S (2014). Oocyte zona pellucida and meiotic spindle birefringence as a biomarker of pregnancy rate outcome in IVF–ICSI treatment. Ginekol Pol 85, 264–71.CrossRefGoogle ScholarPubMed
Tandara, M, Bajic, A, Tandara, L, Bilic-Zulle, L, Sunj, M, Kozina, V, Goluza, T and Jukic, M (2014). Sperm DNA integrity testing: big halo is a good predictor of embryo quality and pregnancy after conventional IVF. Andrology 2, 678–86.CrossRefGoogle ScholarPubMed
Ugajin, T, Terada, Y, Hasegawa, H, Nabeshima, H, Suzuki, K and Yaegashi, N (2010). The shape of the sperm midpiece in intracytoplasmic morphologically selected sperm injection relates sperm centrosomal function. J Assist Reprod Genet 27, 75–81.CrossRefGoogle ScholarPubMed
VerMilyea, MD, Ivani, K, Gvakharia, M, Boostanfar, R, Baker, VL and Conaghan, J (2014). Correlation between computer-automated time-lapse analysis results and implantation success in patients of different age groups: a blinded, multi-center study. Fertil Steril 102, e129.CrossRefGoogle Scholar
Wdowiak, A, Bakalczuk, S and Bakalczuk, G (2015). The effect of sperm DNA fragmentation on the dynamics of the embryonic development in intracytoplasmatic sperm injection. Reprod Biol 15, 94–100.CrossRefGoogle ScholarPubMed
World Health Organization (2010). WHO Laboratory Manual for the Examination and Processing for Human Semen, 5th edn. Switzerland: WHO Press, pp. 223–5.Google Scholar
Xue, LT, Wang, RX, He, B, Mo, WY, Huang, L, Wang, SK, Mao, XB, Cheng, JP, Huang, YY and Liu, RZ (2016). Effect of sperm DNA fragmentation on clinical outcomes for Chinese couples undergoing in vitro fertilization or intracytoplasmic sperm injection. J Int Med Res 44, 1283–91.CrossRefGoogle ScholarPubMed
Zini, A, Meriano, J, Kader, K, Jarvi, K, Laskin, CA and Cadesky, K (2005). Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Hum Reprod 20, 3476–80.CrossRefGoogle ScholarPubMed