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RESEARCH ARTICLE

Effect of docosahexanoic acid on quality of frozen–thawed bull semen in BioXcell extender

Asmatullah Kaka A B , Wahid Haron A , Rosnina Yusoff A E , Nurhusien Yimer A , A. M. Khumran A , Kazhal Sarsaifi A , Atique Ahmed Behan C B , Ubedullah Kaka A B , Akeel Ahmed Memon B and Mahdi Ebrahimi D
+ Author Affiliations
- Author Affiliations

A Department of Veterinary Clinical Studies, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400, UPM, Serdang, Selangor Darul Ehsan, Malaysia.

B Sindh Agriculture University, Tandojam, Hyderabad, Sindh, 70060, Pakistan.

C Department of Animal Science, Faculty of Agriculture, Universiti Putra Malaysia, 43400, UPM, Serdang, Selangor Darul Ehsan, Malaysia.

D Department of Veterinary Preclinical Sciences, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400, UPM, Serdang, Selangor Darul Ehsan, Malaysia.

E Corresponding author. Email: rosninanuris@upm.edu.my

Reproduction, Fertility and Development 29(3) 490-495 https://doi.org/10.1071/RD15089

Abstract

This study was conducted to investigate the effect of docosahexanoic acid (DHA) supplementation in BioXcell extender on the quality of frozen–thawed bull semen. Twenty-four ejaculates were collected from three bulls (eight from each bull). Ejaculates with motility ≥70% and normal morphology ≥80% were extended into BioXcell extender to which 0 (control), 3, 5, 10 or 15 ng mL–1 DHA was added. The supplemented semen samples were incubated at 37°C for 15 min for DHA uptake by spermatozoa. Later, samples were cooled for 2 h at 5°C and packaged into 0.25-mL straws, frozen in liquid nitrogen for 24 h and subsequently thawed for evaluation. Results are presented as percentages ± s.e.m. Supplementation with DHA at 3 ng mL–1 significantly improved sperm functional parameters including sperm motility, normal morphology, viability, acrosome integrity and membrane integrity when compared with other supplemented groups and the control. Lipid peroxidation increased as the incorporation of DHA supplementation increased. In conclusion, 3 ng mL–1 concentration of DHA resulted in superior quality of frozen–thawed bull spermatozoa and is suggested as the optimum level of DHA to be added into BioXcell extender.

Additional keywords: cryopreservation, DHA, sperm motility.


References

Ahluwalia, B., and Holman, R. (1969). Fatty-acid composition of lipids of bull, boar, rabbit and human semen. J. Reprod. Fertil. 18, 431–437.
Fatty-acid composition of lipids of bull, boar, rabbit and human semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXhtVChsbY%3D&md5=db91aefd44584a7e77f712ff4540374cCAS | 5788216PubMed |

Aksoy, Y., Aksoy, H., Altinkaynak, K., Aydin, H. R., and Ozkan, A. (2006). Sperm fatty-acid composition in subfertile men. Prostaglandins Leukot. Essent. Fatty Acids 75, 75–79.
Sperm fatty-acid composition in subfertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xosl2isrc%3D&md5=abc98c91b7c3e0fdc5f3f4ff73ed17d1CAS | 16893631PubMed |

Amann, R. P., and Graham, J. K. (2005). Spermatozoal function. In ‘Equine Reproduction’. 6th edn. (Eds A. O. McKinnon and J. L. Voss.) pp. 715–745. (Blackwell: Ames, IA, USA.)

Argov-Argaman, N., Mahgrefthe, K., Zeron, Y., and Roth, Z. (2013). Variation in lipid profiles within semen compartment – the bovine model of aging. Theriogenology 80, 712–721.
Variation in lipid profiles within semen compartment – the bovine model of aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKrsb%2FM&md5=e26c9c763ae269dd6ee7d23aec8c9134CAS | 23830232PubMed |

Brenner, R. R. (1984). Effect of unsaturated acids on membrane structure and enzyme kinetics. Prog. Lipid Res. 23, 69–96.
Effect of unsaturated acids on membrane structure and enzyme kinetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXitVKq&md5=3d0557e2683545e5dcaf34e9fd5d963cCAS | 6093147PubMed |

Castellano, C. A., Audet, I., Bailey, J., Laforest, J. P., and Matte, J. (2010). Dietary omega-3 fatty acids (fish oils) have limited effects on boar semen stored at 17°C or cryopreserved. Theriogenology 74, 1482–1490.
Dietary omega-3 fatty acids (fish oils) have limited effects on boar semen stored at 17°C or cryopreserved.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Cls7%2FL&md5=73cc69c36f219e1a05a97921df1d4992CAS | 20708242PubMed |

Chakrabarty, J., Banerjee, D., Pal, D., De, J., Ghosh, A., and Majumder, G. C. (2007). Shedding off specific lipid constituents from sperm cell membrane during cryopreservation. Cryobiology 54, 27–35.
Shedding off specific lipid constituents from sperm cell membrane during cryopreservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Kit7Y%3D&md5=a91ab686568d732173e0f46210d5829fCAS | 17227673PubMed |

Chanapiwat, P., Kaeoket, K., and Tummaruk, P. (2009). Effects of DHA-enriched hen egg yolk and L-cysteine supplementation on quality of cryopreserved boar semen. Asian J. Androl. 11, 600–608.
Effects of DHA-enriched hen egg yolk and L-cysteine supplementation on quality of cryopreserved boar semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2jtbzJ&md5=0d1058aaefd99124af96cc944f85987aCAS | 19633681PubMed |

Chanapiwat, P., Kaeoket, K., and Tummaruk, P. (2012). Improvement of the frozen boar semen quality by docosahexanoic acid (DHA) and L-cysteine supplementation. Afr. J. Biotechnol. 11, 3697–3703.
| 1:CAS:528:DC%2BC38XjvFajsr4%3D&md5=eff8037e88024027ab6d91558ef6db3bCAS |

Comhaire, F. H., and Mahmoud, A. (2003). The role of food supplements in the treatment of the infertile man. Reprod. Biomed. Online. 7, 385–391.
The role of food supplements in the treatment of the infertile man.Crossref | GoogleScholarGoogle Scholar | 14656398PubMed |

Conquer, J. A., Martin, J. B., Tummon, I., Watson, L., and Tekpetey, F. (2000). Effect of DHA supplementation on DHA status and sperm motility in as then ozoospermic males. Lipids 35, 149–154.
Effect of DHA supplementation on DHA status and sperm motility in as then ozoospermic males.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Krurc%3D&md5=728d2870940cb82e3d4092012c9fff63CAS | 10757545PubMed |

de Graaf, S. P., Peake, K., Maxwell, W. M. C., O’Brien, J. K., and Evans, G. (2007). Influence of supplementing diet with oleic and linoleic acid on the freezing ability and sex-sorting parameters of ram semen Livest. Sci. 110, 166–173.
Influence of supplementing diet with oleic and linoleic acid on the freezing ability and sex-sorting parameters of ram semenCrossref | GoogleScholarGoogle Scholar |

Drokin, S. I., Vaisberg, T. N., Kopeika, E. F., Miteva, K. D., and Pironecheva, G. L. (1999). Effect of cryopreservation on lipids and some physiological features of spermatozoa from rams pastured in highlands and in valleys. Cytobios. 100, 27–36.
| 1:CAS:528:DC%2BD3cXjvF2nug%3D%3D&md5=7a0b450711a0d694ea26667b02097fd0CAS | 10643642PubMed |

Evans, G., and Maxwell, W. M. C. (1987). Handling and examining semen. In ‘Salamon’s Artificial Insemination of Sheep and Goats’. (Ed. W. M. C. Maxwell.) pp. 93–106. (Butterworths: Sydney.)

Fair, S., Doyle, D. N., Diskin, M. G., Hennessy, A. A., and Kenny, D. A. (2014). The effect of dietary n-3 polyunsaturated fatty acid supplementation of rams on semen quality and subsequent quality of liquid-stored semen. Theriogenology 81, 210–219.
The effect of dietary n-3 polyunsaturated fatty acid supplementation of rams on semen quality and subsequent quality of liquid-stored semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOgt7fO&md5=15fbba1ffb5cdf2f35a74cd94f080914CAS | 24100164PubMed |

Farooqui, A. A., Horrocks, L. A., and Farooqui, T. (2000). Glycerophospholipids in brain: their metabolism, incorporation into membranes, functions and involvement in neurological disorders. Chem. Phys. Lipids 106, 1–29.
Glycerophospholipids in brain: their metabolism, incorporation into membranes, functions and involvement in neurological disorders.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlKku7s%3D&md5=a433014c06286c3855324bbe2df74100CAS | 10878232PubMed |

Folch, J., Lees, M., and Sloane Stanely, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=dade5b0e3aa4eac492435d8d35f9c13aCAS | 13428781PubMed |

Gholami, H., Chamani, M., Towhidi, A., and Fazeli, M. H. (2010). Effect of feeding a docosahexanoic acid-enriched nutriceutical on the quality of fresh and frozen–thawed semen in Holstein bulls. Theriogenology 74, 1548–1558.
Effect of feeding a docosahexanoic acid-enriched nutriceutical on the quality of fresh and frozen–thawed semen in Holstein bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKhsLnF&md5=d56f8a90f124e5e616a8d0bd85222de0CAS | 20708237PubMed |

Herlick, K. (1990). ‘Official Methods of Analysis’. (Association of Official Analytical Chemists: Arlington, TX, USA.)

Kaeoket, K., Sang-urai, P., Thamniyom, P., Chanapiwat, P., and Techakumphu, M. (2010). Effect of docosahexanoic acid on quality of cryopreserved boar semen in different breeds. Reprod. Domest. Anim. 45, 458–463.
Effect of docosahexanoic acid on quality of cryopreserved boar semen in different breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvFGrtbg%3D&md5=abeec08db0d50f8e5059fcb186309f3bCAS | 19090818PubMed |

Kaka, A., Wahid, H., Rosnina, Y., Yimer, N., Khumran, A. M., Sarsaifi, K., Behan, A. A., Kaka, U., and Ebrahimi, M. (2015a). Linolenic acid supplementation in BioXcell extender can improve the quality of post-cooling and frozen–thawed bovine spermatozoa. Anim. Reprod. Sci. 153, 1–7.
Linolenic acid supplementation in BioXcell extender can improve the quality of post-cooling and frozen–thawed bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVWqtbk%3D&md5=8bbf96fc38a09c4019307cf272985d06CAS | 25544152PubMed |

Kaka, A., Wahid, H., Rosnina, Y., Yimer, N., Khumran, A. M., Behan, A. A., and Ebrahimi, M. (2015b). Alpha-linolenic acid supplementation in Tris extender can improve frozen–thawed bull semen quality. Reprod. Domest. Anim. 50, 29–33.
Alpha-linolenic acid supplementation in Tris extender can improve frozen–thawed bull semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVWktro%3D&md5=ce799b18b7eed61b87305e89070f6378CAS | 25366298PubMed |

Kelso, K. A., Redpath, A., Noble, R. C., and Speake, B. K. (1997). Lipid and antioxidant changes in spermatozoa and seminal plasma throughout the reproductive period of bulls. J. Reprod. Fertil. 109, 1–6.
Lipid and antioxidant changes in spermatozoa and seminal plasma throughout the reproductive period of bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gnt70%3D&md5=a310bed615a7fd4ae38519b0c8554e75CAS | 9068407PubMed |

Kiernan, M., Fahy, A. G., and Fair, S. (2013). Effect of in vitro supplementation of exogenous long-chain fatty acids on bovine sperm cell function. Reprod. Fertil. Dev. 25, 947–954.
Effect of in vitro supplementation of exogenous long-chain fatty acids on bovine sperm cell function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSrtrzI&md5=359f35c1877fced22b9a738f64e089a8CAS | 23036717PubMed |

Koppers, A. J., Garg, M. L., and Aitken, R. J. (2010). Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic. Biol. Med. 48, 112–119.
Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFyku7rI&md5=8655cab667d4ccd68450b7aba1e97451CAS | 19837155PubMed |

Lenzi, A., Gandini, L., Picardo, M., Tramer, F., Sandri, G., and Panfili, E. (2000). Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible scavenger therapies. Front. Biosci. 5, E1–E15.
| 1:CAS:528:DC%2BD3cXht1Shtbs%3D&md5=032666e621e5e88d42009c91db17876aCAS | 10702376PubMed |

Martínez-Soto, J. C., Landeras, J., and Gadea, J. (2013). Spermatozoa and seminal plasma fatty acids as predictors of cryopreservation success. Andrology 1, 365–375.
Spermatozoa and seminal plasma fatty acids as predictors of cryopreservation success.Crossref | GoogleScholarGoogle Scholar | 23596043PubMed |

Memon, A. A., Wahid, H., Rosnina, Y., Goh, Y. M., Ebrahimi, M., Nadia, F. M., and Audrey, G. (2011). Effect of butylated hydroxytoluene on cryopreservation of Boer goat semen in Tris egg-yolk extender. Anim. Reprod. Sci. 129, 44–49.
Effect of butylated hydroxytoluene on cryopreservation of Boer goat semen in Tris egg-yolk extender.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOgu7%2FI&md5=e300b25420ac1d6c1afe01340014a2dcCAS | 22024366PubMed |

Mercier, Y., Gatellier, P., Viau, M., Remignon, H., and Renerre, M. (1998). Effect of dietary fat and vitamin E on colour stability and on lipid and protein oxidation in turkey meat during storage. Meat Sci. 48, 301–318.
Effect of dietary fat and vitamin E on colour stability and on lipid and protein oxidation in turkey meat during storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvVOrtw%3D%3D&md5=bba10f288322a2422ad46486976ecb64CAS | 22063078PubMed |

Nasiri, A. H., Towhidi, A., and Zeinoaldini, S. (2012). Combined effect of DHA and α-tocopherol supplementation during semen cryopreservation on sperm characteristics and fatty-acid composition. J. Andrologia 44, 550–555.
Combined effect of DHA and α-tocopherol supplementation during semen cryopreservation on sperm characteristics and fatty-acid composition.Crossref | GoogleScholarGoogle Scholar |

O’Connell, M., McClure, N., and Lewis, S. E. (2002). The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum. Reprod. 17, 704–709.
The effects of cryopreservation on sperm morphology, motility and mitochondrial function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387jsVymsQ%3D%3D&md5=f86631f8d7e90e7d7d78b79680b750c5CAS | 11870124PubMed |

Penny, P. C., Maldjian, A., and Noble, R. C. (2000). An enhancement of boar fertility and reproductive performance. In ‘Proceedings of the 14th International Congress of Animal Reproduction, Stockholm, Sweden’. (Eds M. Forsberg, T. Greve, H. Gustaffson, T. Katila, H. Kindahl and E. Ropstad.) p. 109. (ICAR: Stockholm.)

Revell, S. G., and Mrode, R. A. (1994). An osmotic resistance test for bovine semen. Anim. Reprod. Sci. 36, 77–86.
An osmotic resistance test for bovine semen.Crossref | GoogleScholarGoogle Scholar |

Robinson, J. J., Ashworth, C. J., Rooke, J. A., Mitchell, L. M., and McEvoy, T. G. (2006). Nutrition and fertility in ruminant livestock. Anim. Feed Sci. Technol. 126, 259–276.
Nutrition and fertility in ruminant livestock.Crossref | GoogleScholarGoogle Scholar |

Rooke, J. A., Shao, C.-C., and Speake, B. K. (2001). Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen. Reproduction 121, 315–322.
Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslSisbc%3D&md5=232daa4f054249b8442add0f1d0b6916CAS | 11226056PubMed |

Safarinejad, M. R., Hosseini, S. Y., Dadkhah, F., and Asgari, M. A. (2010). Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin. Nutr. 29, 100–105.
Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1antLc%3D&md5=efb8626fc4712dc74afd6ba861124856CAS | 19666200PubMed |

Samadian, F., Towhidi, A., Rezayazdi, K., and Bahreini, M. (2010). Effects of dietary n-3 fatty acids on characteristics and lipid composition of ovine spermatozoa. Animal 4, 2017–2022.
Effects of dietary n-3 fatty acids on characteristics and lipid composition of ovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGjsr%2FE&md5=85f54c875436709813d66cbea24ad201CAS | 22445376PubMed |

Sanocka, D., and Kurpisz, M. (2004). Reactive oxygen species and sperm cells. Reprod. Biol. Endocrinol. 2, 12.
Reactive oxygen species and sperm cells.Crossref | GoogleScholarGoogle Scholar | 15038829PubMed |

Sarsaifi, K., Rosnina, H. Y., Ariff, O. M., Wahid, H. A., Hani, H., Yimer, N., Naing, S. W., and Abas, M. O. (2013). Effect of semen collection methods on the quality of pre-and post-thawed Bali cattle (Bos javanicus) spermatozoa. Reprod. Domest. Anim. 48, 1006–1012.
Effect of semen collection methods on the quality of pre-and post-thawed Bali cattle (Bos javanicus) spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sjmsF2lsA%3D%3D&md5=28960c936b0b98a2e7b4c5d59c2cab23CAS | 23808560PubMed |

Schiller, J., Arnhold, J., Glander, H. J., and Arnold, K. (2000). Lipid analysis of human spermatozoa and seminal plasma by MALDI-TOF mass spectrometry and NMR spectroscopy – effects of freezing and thawing. Chem. Phys. Lipids 106, 145–156.
Lipid analysis of human spermatozoa and seminal plasma by MALDI-TOF mass spectrometry and NMR spectroscopy – effects of freezing and thawing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1KnsLs%3D&md5=8adc8aace82c4d4934abebb041561850CAS | 10930566PubMed |

Vishwanath, R., and Shannon, P. (2000). Storage of bovine semen in liquid and frozen state. Anim. Reprod. Sci. 62, 23–53.
Storage of bovine semen in liquid and frozen state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Kgsbs%3D&md5=d71d7ce45d851472553215f8cf941e18CAS | 10924819PubMed |

Yildiz, C., Kaya, A., Aksoy, M., and Tekeli, T. (2000). Influence of sugar supplementation of the extender on motility, viability and acrosomal integrity of dog spermatozoa during freezing. Theriogenology 54, 579–585.
Influence of sugar supplementation of the extender on motility, viability and acrosomal integrity of dog spermatozoa during freezing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3crht1Kgsw%3D%3D&md5=5080b7960a255ddb25178fc229aa99bfCAS | 11071132PubMed |

Yimer, N., Noraisyah, A. H., Rosnina, Y., Wahid, H., Sarsaifi, K., and Hafizal, A. M. (2014). Comparison of cryopreservative effect of different levels of omega-3 egg yolk in citrate extender on the quality of goat spermatozoa. Pak. Vet. J. 34, 347–350.

Yoshida, M. (2000). Conservation of spermatozoa: current status and new trends. Anim. Reprod. Sci. 60–61, 349–355.
Conservation of spermatozoa: current status and new trends.Crossref | GoogleScholarGoogle Scholar | 10844206PubMed |

Yousef, M. I., Abdallah, G. A., and Kcalamel, K. I. (2003). Effect of ascorbic acid and vitamin E supplementation on semen quality and biochemical parameters of male rabbits. Anim. Reprod. Sci. 76, 99–111.
Effect of ascorbic acid and vitamin E supplementation on semen quality and biochemical parameters of male rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1aqsw%3D%3D&md5=433cc1ba21f6913765f43f2f1ca9cce0CAS | 12559724PubMed |

Zalata, A. A., Christophe, A. B., Depuydt, C. E., Schoonjans, F., and Comhaire, F. H. (1998). The fatty-acid composition of phospholipids of spermatozoa from infertile patients. Mol. Hum. Reprod. 4, 111–118.
The fatty-acid composition of phospholipids of spermatozoa from infertile patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlamurY%3D&md5=897a0872fc5997af476792ade62cdcbcCAS | 9542967PubMed |