Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-22T09:23:13.907Z Has data issue: false hasContentIssue false

What are the effects of vitamin C on sperm functional properties during direct swim-up procedure?

Published online by Cambridge University Press:  05 March 2019

Georges Raad*
Affiliation:
Azoury IVF Clinic, Mount Lebanon Hospital, Camille Chamoun Bvd, Beirut, Lebanon
Joyce Mansour
Affiliation:
Institut National de Pathologie (INP), Baabda, Lebanon
Rim Ibrahim
Affiliation:
Azoury IVF Clinic, Mount Lebanon Hospital, Camille Chamoun Bvd, Beirut, Lebanon
Jessica Azoury
Affiliation:
Azoury IVF Clinic, Mount Lebanon Hospital, Camille Chamoun Bvd, Beirut, Lebanon
Joan Azoury
Affiliation:
OB-GYN Department, Inova Fairfax Hospital, Falls Church, Virginia, USA
Youmna Mourad
Affiliation:
Al-Hadi Laboratory and Medical Center, Beirut, Lebanon
Chadi Fakih
Affiliation:
Al-Hadi Laboratory and Medical Center, Beirut, Lebanon
Joseph Azoury
Affiliation:
Azoury IVF Clinic, Mount Lebanon Hospital, Camille Chamoun Bvd, Beirut, Lebanon
*
*Address for correspondence: Georges Raad. Azoury IVF clinic, Mount Lebanon Hospital, Camille Chamoun Bvd, Beirut, Lebanon. Tel: +961 71 666306. E-mail: georges.raad@live.com

Summary

Direct swim-up procedure is widely used to separate the motile competent spermatozoa from the antioxidant-rich semen. Subsequently, spermatozoa become more vulnerable to reactive oxygen species (ROS) due to their cytological characteristics. The effect of vitamin C, a highly concentrated antioxidant in the semen, on direct swim-up-enriched sperm population is not fully investigated. Therefore, the aim of the present study was to assess the effect of vitamin C on sperm functional properties during direct swim-up procedure. Semen samples were collected from 22 participants. Each semen sample was divided into several aliquots. The first portion was overlaid with sperm medium without ascorbic acid (0 µM AA). The second and third fractions were overlaid with sperm medium supplemented with 300 µM and 600 µM AA; respectively. After 1 h of incubation, basic sperm parameters, intracellular ROS levels, acrosome reaction, chromatin integrity, and glucose uptake were assessed. Swim-up without AA significantly increased the percentage of ROS(+) spermatozoa compared with the raw semen (P<0.01). Interestingly, swim-up with 300 µM AA did not increase the percentage of ROS(+) sperm compared with the raw semen. In parallel, the percentage of sperm with altered chromatin integrity was significantly lower in the 300 µM AA group compared with that in the raw semen (P<0.05). These findings suggest that supplementation of vitamin C to sperm medium could be beneficial for direct swim-up-derived spermatozoa.

Type
Research Article
Copyright
© Cambridge University Press 2019 

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

Agarwal, A and Majzoub, A (2017) Free radicals in andrology. In Balercia G, Gandini L, Lenzi A and Lombardo F (eds). Antioxidants in Andrology, Trends in Andrology and Sexual Medicine. Springer International Publishing, Cham, pp. 121.Google Scholar
Agarwal, A and Said, TM (2003) Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update 9, 331345.Google Scholar
Agarwal, A, Makker, K and Sharma, R (2008) Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 59, 211.Google Scholar
Agarwal, A, Durairajanayagam, D and du Plessis, SS (2014) Utility of antioxidants during assisted reproductive techniques: an evidence based review. Reprod Biol Endocrinol 12, 112.Google Scholar
Agarwal, A, Roychoudhury, S, Bjugstad, KB and Cho, C-L (2016) Oxidation–reduction potential of semen: what is its role in the treatment of male infertility? Ther Adv Urol 8, 302318.Google Scholar
Ahmad, G, Agarwal, A, Esteves, SC, Sharma, R, Almasry, M, Al-Gonaim, A, AlHayaza, G, Singh, N, Al Kattan, L, Sannaa, WM and Sabanegh, E (2017) Ascorbic acid reduces redox potential in human spermatozoa subjected to heat-induced oxidative stress. Andrologia 49, doi: 10.1111/and.12773.Google Scholar
Aitken, RJ, Fisher, HM, Fulton, N, Gomez, E, Knox, W, Lewis, B and Irvine, S (1997) Reactive oxygen species generation by human spermatozoa is induced by exogenous NADPH and inhibited by the flavoprotein inhibitors diphenylene iodonium and quinacrine. Mol Reprod Dev 47, 468482.Google Scholar
Aitken, RJ, Finnie, JM, Muscio, L, Whiting, S, Connaughton, HS, Kuczera, L, Rothkirch, TB and De Iuliis, GN (2014) Potential importance of transition metals in the induction of DNA damage by sperm preparation media. Hum Reprod Oxf Engl 29, 21362147.Google Scholar
Ajina, T, Ammar, O, Haouas, Z, Sallem, A, Ezzi, L, Grissa, I, Sakly, W, Jlali, A and Mehdi, M (2017) Assessment of human sperm DNA integrity using two cytochemical tests: acridine orange test and toluidine blue assay. Andrologia 49, doi: 10.1111/and.12765Google Scholar
Akhir, NAM, Chua, LS, Majid, FAA and Sarmidi, MR (2011) Cytotoxicity of aqueous and ethanolic extracts of Ficus deltoidea on human ovarian carcinoma cell line. Br J Med Med Res 1, 397409.Google Scholar
Alves, IP, Cancelli, CHB, Grassi, TLM, Oliveira, PRH, Franciscato, DA, Carreira, JT and de Koivisto, MB (2018) Evaluation of sperm head dimensions and chromatin integrity of epididymal sperm from domestic cats using the toluidine blue technique. Anim Reprod Sci 197, 3339.Google Scholar
Anbari, F, Halvaei, I, Nabi, A, Ghazali, S, Khalili, MA and Johansson, L (2016) The quality of sperm preparation medium affects the motility, viability, and DNA integrity of human spermatozoa. J Hum Reprod Sci 9, 254258.Google Scholar
Angulo, C, Maldonado, R, Pulgar, E, Mancilla, H, Córdova, A, Villarroel, F, Castro, MA and Concha, II (2011) Vitamin C and oxidative stress in the seminiferous epithelium. Biol Res 44, 169180.Google Scholar
Beydola, T, Sharma, RK and Agarwal, A (2014) Sperm preparation and selection techniques. In Rizk BRMB, Aziz N, Agarwal A and Sabanegh E, Jr (eds) Medical and Surgical Management of Male Infertility 1st edn, Chapter 29. Jaypee Brothers Medical Publisers.Google Scholar
Bormann, CL, Alagretti, JR, da Motta, ELA, Serafini, P and Smith, GD (2010) Preparation and selection of sperm for IVF and ICSI. In Carrell, DT and Peterson, CM (eds). Reproductive Endocrinology and Infertility: Integrating Modern Clinical and Laboratory Practice. Springer New York, NY, USA, pp. 579590.Google Scholar
Burruel, V, Klooster, K, Barker, CM, Pera, RR and Meyers, S (2014) Abnormal early cleavage events predict early embryo demise: sperm oxidative stress and early abnormal cleavage. Sci Rep 4, 6598.Google Scholar
Castro D, S L, Assis D, M P, Siqueira, AFP, Hamilton, TRS, Mendes, CM, Losano, JDA, Nichi, M, Visintin, JA and Assumpção, MEOA (2016) Sperm oxidative stress is detrimental to embryo development: a dose-dependent study model and a new and more sensitive oxidative status evaluation. Oxid Med Cell Longev 2016, 8213071.Google Scholar
Chi, HJ, Kim, JH, Ryu, CS, Lee, JY, Park, JS, Chung, DY, Choi, SY, Kim, MH, Chun, EK and Roh, SI (2008) Protective effect of antioxidant supplementation in sperm-preparation medium against oxidative stress in human spermatozoa. Hum Reprod Oxf Engl 23, 10231028.Google Scholar
Dawson, EB, Harris, WA, Rankin, WE, Charpentier, LA and McGanity, WJ (1987) Effect of ascorbic acid on male fertility. Ann N Y Acad Sci 498, 312323.Google Scholar
de Lamirande, E and O’Flaherty, C (2008) Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta 1784, 106115.Google Scholar
Donnelly, ET, McClure, N and Lewis, SE (1999a) Antioxidant supplementation in vitro does not improve human sperm motility. Fertil Steril 72, 484495.Google Scholar
Donnelly, ET, McClure, N and Lewis, SE (1999b) The effect of ascorbate and alpha-tocopherol supplementation in vitro on DNA integrity and hydrogen peroxide-induced DNA damage in human spermatozoa. Mutagenesis 14, 505512.Google Scholar
Ellington, JE, Evenson, DP, Wright, RW, Jones, AE, Schneider, CS, Hiss, GA and Brisbois, RS (1999) Higher-quality human sperm in a sample selectively attach to oviduct (fallopian tube) epithelial cells in vitro . Fertil Steril 71, 924929.Google Scholar
Emiliani, S, Van Den Bergh, M, Vannin, AS, Biramane, J, Verdoodt, M and Englert, Y (2001) Evidence of reduced single-stranded testicular sperm DNA from obstructive azoospermic men after 3 days of in-vitro culture. Hum Reprod Oxf Engl 16, 12001203.Google Scholar
Erenpreiss, J, Bars, J, Lipatnikova, V, Erenpreisa, J and Zalkalns, J (2001) Comparative study of cytochemical tests for sperm chromatin integrity. J Androl 22, 4553.Google Scholar
Esfandiari, N, Sharma, RK, Saleh, RA, Thomas, AJ and Agarwal, A (2003) Utility of the nitroblue tetrazolium reduction test for assessment of reactive oxygen species production by seminal leukocytes and spermatozoa. J Androl 24, 862870.Google Scholar
Esteves, SC, Sharma, RK, Thomas, AJ and Agarwal, A (2000) Effect of swim-up sperm washing and subsequent capacitation on acrosome status and functional membrane integrity of normal sperm. Int J Fertil Womens Med 45, 335341.Google Scholar
Fanaei, H, Khayat, S, Halvaei, I, Ramezani, V, Azizi, Y, Kasaeian, A, Mardaneh, J, Parvizi, MR and Akrami, M (2014) Effects of ascorbic acid on sperm motility, viability, acrosome reaction and DNA integrity in teratozoospermic samples. Iran J Reprod Med 12, 103110.Google Scholar
Fraczek, M, Sanocka, D and Kurpisz, M (2004) Interaction between leucocytes and human spermatozoa influencing reactive oxygen intermediates release. Int J Androl 27, 6975.Google Scholar
Giustarini, D, Dalle-Donne, I, Colombo, R, Milzani, A and Rossi, R (2008) Is ascorbate able to reduce disulfide bridges? A cautionary note. Nitric Oxide Biol Chem 19, 252258.Google Scholar
Gualtieri, R, Barbato, V, Fiorentino, I, Braun, S, Rizos, D, Longobardi, S and Talevi, R (2014) Treatment with zinc, d-aspartate, and coenzyme Q10 protects bull sperm against damage and improves their ability to support embryo development. Theriogenology 82, 592598.Google Scholar
Hughes, CM, Lewis, SE, McKelvey-Martin, VJ and Thompson, W (1998) The effects of antioxidant supplementation during Percoll preparation on human sperm DNA integrity. Hum Reprod Oxf Engl 13, 12401247.Google Scholar
Ji, BT, Shu, XO, Linet, MS, Zheng, W, Wacholder, S, Gao, YT, Ying, DM and Jin, F (1997) Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst 89, 238244.Google Scholar
Kessopoulou, E, Tomlinson, MJ, Barratt, CL, Bolton, AE and Cooke, ID (1992) Origin of reactive oxygen species in human semen: spermatozoa or leucocytes? J Reprod Fertil 94, 463470.Google Scholar
Ko, EY and Sabanegh, ES (2012) The role of over-the-counter supplements for the treatment of male infertility—fact or fiction? J Androl 33, 292308.Google Scholar
Kupka, MS, Ferraretti, AP, de Mouzon, J, Erb, K, D’Hooghe, T, Castilla, JA, Calhaz-Jorge, C, De Geyter, C, Goossens, V, the European IVF-Monitoring Consortium, for the European Society of Human Reproduction and Embryology (2014) Assisted reproductive technology in Europe, 2010: results generated from European registers by ESHRE. Hum Reprod Oxf Engl 29, 20992113.Google Scholar
Lewis, SEM, Sterling, ESL, Young, IS and Thompson, W (1997) Comparison of individual antioxidants of sperm and seminal plasma in fertile and infertile men. Fertil Steril 67, 142147.Google Scholar
Li, Z, Lin, Q, Liu, R, Xiao, W and Liu, W (2010) Protective effects of ascorbate and catalase on human spermatozoa during cryopreservation. J Androl 31, 437444.Google Scholar
Lopes, S, Sun, JG, Jurisicova, A, Meriano, J and Casper, RF (1998) Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 69, 528532.Google Scholar
Marchesi, DE, Biederman, H, Ferrara, S, Hershlag, A and Feng, HL (2010) The effect of semen processing on sperm DNA integrity: comparison of two techniques using the novel toluidine blue assay. Eur J Obstet Gynecol Reprod Biol 151, 176180.Google Scholar
Ménézo, YJR, 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. Reprod Biomed Online 14, 418421.Google Scholar
Menkveld, R (2010) Clinical significance of the low normal sperm morphology value as proposed in the 5th edition of the WHO Laboratory Manual for the Examination and Processing of Human Semen. Asian J Androl 12, 4758.Google Scholar
Meseguer, M, Martínez-Conejero, JA, O’Connor, JE, Pellicer, A, Remohí, J and Garrido, N (2008) The significance of sperm DNA oxidation in embryo development and reproductive outcome in an oocyte donation program: a new model to study a male infertility prognostic factor. Fertil Steril 89, 11911199.Google Scholar
O’Flaherty, C, de Lamirande, E and Gagnon, C (2006) Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Radic Biol Med 41, 528540.Google Scholar
Pereira, R, , R, Barros, A and Sousa, M (2017) Major regulatory mechanisms involved in sperm motility. Asian J Androl 19, 514.Google Scholar
Rengan, AK, Agarwal, A, van der Linde, M and du Plessis, SS (2012) An investigation of excess residual cytoplasm in human spermatozoa and its distinction from the cytoplasmic droplet. Reprod Biol Endocrinol 10, 92.Google Scholar
Robinson, L, Gallos, ID, Conner, SJ, Rajkhowa, M, Miller, D, Lewis, S, Kirkman-Brown, J and Coomarasamy, A (2012) The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum Reprod Oxf Engl 27, 29082917.Google Scholar
Shahar, S, Wiser, A, Ickowicz, D, Lubart, R, Shulman, A and Breitbart, H (2011) Light-mediated activation reveals a key role for protein kinase A and sarcoma protein kinase in the development of sperm hyper-activated motility. Hum Reprod Oxf Engl 26, 22742282.Google Scholar
Sierens, J, Hartley, JA, Campbell, MJ, Leathem, AJC and Woodside, JV (2002) In vitro isoflavone supplementation reduces hydrogen peroxide-induced DNA damage in sperm. Teratog Carcinog Mutagen 22, 227234.Google Scholar
Sunderam, S (2018) Assisted Reproductive Technology Surveillance – United States, 2015. MMWR 67, 128.Google Scholar
Talbot, P and Chacon, RS (1981) A triple-stain technique for evaluating normal acrosome reactions of human sperm. J Exp Zool 215, 201208.Google Scholar
Talevi, R, Barbato, V, Fiorentino, I, Braun, S, Longobardi, S and Gualtieri, R (2013) Protective effects of in vitro treatment with zinc, d-aspartate and coenzyme q10 on human sperm motility, lipid peroxidation and DNA fragmentation. Reprod Biol Endocrinol 11, 81.Google Scholar
Tanaka, A, Nagayoshi, M, Tanaka, I and Kusunoki, H (2012) Human sperm head vacuoles are physiological structures formed during the sperm development and maturation process. Fertil Steril 98, 315320.Google Scholar
Tsarev, I, Bungum, M, Giwercman, A, Erenpreisa, J, Ebessen, T, Ernst, E and Erenpreiss, J (2009) Evaluation of male fertility potential by toluidine blue test for sperm chromatin structure assessment. Hum Reprod Oxf Engl 24, 15691574.Google Scholar
World Health Organization (ed.) (2010) WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn World Health Organization, Geneva.Google Scholar
Yun, JI, Gong, SP, Song, YH and Lee, ST (2013) Effects of combined antioxidant supplementation on human sperm motility and morphology during sperm manipulation in vitro . Fertil Steril 100, 373378.Google Scholar
Zidi-Jrah, I, Hajlaoui, A, Mougou-Zerelli, S, Kammoun, M, Meniaoui, I, Sallem, A, Brahem, S, Fekih, M, Bibi, M, Saad, A and Ibala-Romdhane, S (2016) Relationship between sperm aneuploidy, sperm DNA integrity, chromatin packaging, traditional semen parameters, and recurrent pregnancy loss. Fertil Steril 105, 5864.Google Scholar
Zini, A, San Gabriel, M , and Libman, J (2010) Lycopene supplementation in vitro can protect human sperm deoxyribonucleic acid from oxidative damage. Fertil Steril 94, 10331036.Google Scholar
Supplementary material: File

Raad et al. supplementary material

Tables S1-S2

Download Raad et al. supplementary material(File)
File 14.4 KB