Quality Enhancement of Aceh Swamp Buffalo (Bubalus bubalis) Frozen Semen by Supplementing β-Carotene
Abstract
Sperms are vulnerable to oxidative stress due to the high proportion of polyunsaturated fatty acids within their membranes. This condition could decrease sperms quality during preservation. β-carotene is among antioxidants able to neutralize reactive oxygen species, natural by-products of oxygen metabolism in sperms. This study was done to investigate the capability and protective effect of this antioxidant on motility, viability, acrosomal integrity, and plasma membrane integrity of frozen-thawed sperms of Aceh swamp buffalo. The study was conducted using completely randomized design with four treatments and five replications. Fresh semen was diluted in egg-yolk tris-based extenders with the addition of antioxidant of 0% (w/v) (control, P0), 0.625% (w/v) (P1), 1.25% (w/v) (P2), and 2.5% (w/v) (P3) prior to freezing. Variables of sperms quality examined were motility, viability, acrosomal integrity, and plasma membrane integrity of semen after dilution, equilibration, and thawing. Semen having the best post-thawing quality after β-carotene treatment was used for artificial insemination (AI) for accessing its pregnancy rate. The results showed that the addition of 0.625% (w/v) β-carotene (P1) resulted in the highest motility, viability, acrosomal integrity, and plasma membrane integrity. Pregnancy rate of buffalo inseminated with semen treated with 0.625% β-carotene (P1) was 50%. In conclusion, administration of 0.625% β-carotene was able to maintain and could protect motility, viability, acrosomal integrity, and plasma membrane integrity of frozen sperms of Aceh swamp buffalo that are good for artificial insemination.
References
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Ansari, M.S., B. A. Rakha, N. Ullah, S. M. H. Andrabi, & S. Akhter. 2011. Glutathione addition of cooled buffalo (Bubalus bubalis) bull semen. Pakistan J. Zool. 43(Suppl. 1):49-55.
Asadpour, R. M. M. Pourseif, & G. Moghadam. 2012. Effect of vitamin B12 addition to extenders on some physicochemical parameters of semen in crossbred rams. African. J. Biotechnol. 54:11741-11745.
Bansal, A.K., & G. S. Bilaspuri. 2011. Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 2011: 1-7.
https://doi.org/10.4061/2011/686137
Batista, M., T. Nino, D. Alamo, N. Castro, M. Santana, F. Gonzalez, F. Cabrera, & A. Gracia. 2009. Successful artificial insemination using semen frozen and stored by an ultrafreezer in the Majorera goat breed. Theriogenology 71:1307-1315.
https://doi.org/10.1016/j.theriogenology.2008.12.024
BPS (Central Statistical Board) of Indonesia. 2016. https://www.bps.go.id/linkTableDinamis/view. Accessed on August 20th, 2017
Bucak, M.N., P. B. Tuncer, S. Sariözkan, N. Baspinar, M. Taspinar, K. Coyan, A. Bilqili, P. P. Alkalin, S. Büyükleblebici, S. Aydos, S. Ilgaz, A. Sunguroğlu, & D. Oztuna. 2010a. Effects of antioxidants on post-thawed bovine sperm and oxidative stress parameters: antioxidants protect DNA integrity against cryodamage. Cryobiology. 61(Suppl. 3):248-53. https://doi.org/10.1016/j.cryobiol.2010.09.001
Bucak, M.N., S. Sariözkan, & P. B. Tuncer. 2010b. The effect of antioxidants on post-thawed Angora goat (Capra hircus ancryrensis) sperm parameters, lipid peroxidation and antioxidant activities. Small Rumin Res. 89(Suppl.1):24-30.
https://doi.org/10.1016/j.smallrumres.2009.11.015
Cruz, L. C. 2007. Trends in buffalo production in Asia. Italian J. Anim. Sci. 6(Suppl. 2): 9-24. https://doi.org/10.4081/ijas.2007.s2.9
Eriani, K.,M. Ihdina, R. Rosnizar, D. Dasrul, S. Suhartono, & M. Rizal. 2017a. Cryopreservation of Aceh swamp buffalo (Bubalus bubalis) semen with combination of glyserol and lactose. Biosaintifika. 9(Suppl 3):409-416. https://doi.org/10.15294/biosaintifika.v9i3.11426
Eriani, K.,N. Sari, M. Ihdina, & Rosnizar. 2017b. The effect of equilibration time on semen freezing of local swamp buffalo (Bubalus bubalis) with combination extender of lactose and glycerol. Nus Biosci. 9(Suppl 1):77-82. https://doi.org/10.13057/nusbiosci/n090113
Eveson, D. P. 2016. The Sperm Chromatin Structure Assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Anim. Reprod. Sci. 169:56-75. https://doi.org/10.1016/j.anireprosci.2016.01.017
Fang, Y.I., R. Zhonga, L. Chenb, C. Feng, H. Suna, & D. Zhoua. 2015. Effects of astaxanthin supplementation on the sperm quality and antioxidant capacity of ram semen during liquid storage. Small. Rumin. Res.130:178-182
https://doi.org/10.1016/j.smallrumres.2015.05.016
Gunawan, I., D. N. Laksmi, & D. I. Trilaksana. 2012. The effectiveness of the addition of b-carotene and glutathione in diluent materials to sperm motility and viability at cryopreservation semen cattle. Indonesia. Med. Vet. 1(Suppl. 3):385.
Holt, W. V. 2000. Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology. 53:4758.
https://doi.org/10.1016/S0093-691X(99)00239-3
Judi, T. L. Yusuf, B. Purwantara, D. Sajuthi, M. Agil, J. Manangsang, R. Sudarwati, Y. T. Hastuti, B. Huaso, A. Widianti, & S. Prastitic. 2012. Successful intracervical insemination and characteristics of anoa (Bubalus sp.) parturation behavior in captivity. J. Med. Pet. 32(Suppl. 2):73-79. https://doi.org/10.5398/medpet.2012.35.2.73
Kasimanickam, R., V. Kasimanickam, K. D. Pelzer, & J. J. Dascanio. 2007. Effect of breed and sperm concentration on the changes in structural, functional and motility parameters of ramlamb spermatozoa during storage at 4oC. Anim Reprod Sci. 101:60 -73. https://doi.org/10.1016/j.anireprosci.2006.09.001
Krakowski, L., J. Obara, A. Wachocka, T. Piech, P. Bartoszek, K. Kostro, & M. R. Tatara. 2013. Assessment of extent of apoptosis and DNA defragmentation in chilled semen of stallions during the breeding season. Reprod. Domest. Anim. 48:826-832.
https://doi.org/10.1111/rda.12170
Kumaresan, A., M. R. Ansari, & G. Abhishek. 2005. Modulation of post-thaw sperm functions with oviductal proteins in buffaloes. Anim. Reprod. Sci. 90:73-84.
https://doi.org/10.1016/j.anireprosci.2005.01.009
Layek, S. S., T. K. Mohanty, A. Kumaresan, & J. E. Parks. 2016. Cryopreservation of bull semen: evolution from egg yolk based to soybean based extenders. Anim. Reprod. Sci. 172:1-9. https://doi.org/10.1016/j.anireprosci.2016.04.013
Marti, J. I., E. Marti, J. A. Cebrian-Perez, & T. Muino Blanco. 2003. Survival rate and antioxidant enzyme activity of ram spermatozoa after dilution with different extenders or selection by a dextran swim-up procedure. Theriogenology. 60:1025-1037.
https://doi.org/10.1016/S0093-691X(03)00105-5
Memon, A.A., H. Wahid, Y. Rosnina, Y. M. Goh, M. Ebrahimi, F. M. Nadia, & G. Audrey. 2011. Effect of butylated hydoxytoluene on cryopreservation of boer goat semen in tris egg yolk extender. Anim. Reprod. Sci. 129:44-49.
https://doi.org/10.1016/j.anireprosci.2011.10.004
Memon, A. A., H. Wahid, Y. Rosnina, Y. M. Goh, M. Ebrahimi, & F. M. Nadia. 2012. Effect of antioxidants on post thaw microscopic, oxidative stress parameter and fertility of boer goat spermatozoa in tris egg yolk glycerol extender. Anim. Reprod. Sci. 136:55-60. https://doi.org/10.1016/j.anireprosci.2012.10.020
Morrell, J. M., T. Nongbua, S. Veleanu, I. L. Verde, K. Lundstedt-Enkel, A. Edman, & A. Johannisson. 2017. Sperm quality variables as indicators of bull fertility may be breed dependent. Anim. Reprod. Sci. 185:42-52.
https://doi.org/10.1016/j.anireprosci.2017.08.001
Oshima, S. F., H. Ojima, Y. Sakamoto, Ishiguro, & J. Terao. 1993. Inhibitory effect of -carotene and asthaxanthin on phorosensitizied oxidation of phospolipid bilayers. Nur. Sci. Vitaminol. 39(Suppl. 3):607-615. https://doi.org/10.3177/jnsv.39.607
Pryor, W. A., W. Stahl, & C. L. Roch. 2000. β-Carotene: from biochemistry to clinical trials. Nutr. Rev.58:39-53. https://doi.org/10.1111/j.1753-4887.2000.tb07810.x
Rizal, M. 2005. Effectivity various concentrations of β-carotene on the quality of frozen Garut sheep semen. Anim. Prod. 7(Suppl. 1):6-13
Sariözkan, S., M. N. Bucak, P. B. Tuncer, S. Buyukleblebici, & F. Canturk. 2014. Influence of various antioxidants added to TCM-199 on post-thaw bovine sperm parameters, DNA integrity and fertilizing ability. Cryobiology. 68:129-133.
https://doi.org/10.1016/j.cryobiol.2014.01.007
Sariözkan, S., P. B. Tuncer, M. N. Bucak, & P. A. Ulutas. 2009. Influence of various antioxidants on microscopic-oxidative stress indicators and fertilizing ability of frozen-thawed bull semen. ACTA VET. BRNO. 78:463-469.
https://doi.org/10.2754/avb200978030463
Sarsaifi, K., H. Y. Rosnina, O. M. Ariff, H. A. Wahid, H. Hani, N. Yimer, S. W. Naing, & M. O. Abas. 2013. Effects of semen collection methods on the quality of pre and post thawed Bali cattle (Bos javanicus) spermatozoa. Reprod. Domest. Anim. 44(Suppl. 6):1006-1012. https://doi.org/10.1111/rda.12206
Siahaan, E. A., D. N. D. I.Laksmi, & W. Bebas. 2012. Efectivity of addition of various concentration β-carotene on motility and viability of Bali cattle spermatozoa post thawing. Indonesia.Med.Vet.1(Suppl 2):239-251.
Sianturi, R. G., B. Purwantara, I. Supriatna, Amrozi, & P. Situmorang. 2012. Optimasi inseminasi buatan pada kerbau lumpur (Bubalus bubalis) melalui teknis sinkronisasi estrus dan ovulasi. JITV. 17(Suppl 2):92-99.
Simmons, L. W. 2011. Effects of vitamins E and beta-carotene on sperm competitiveness. Ecology Letters. 14:891-895.
https://doi.org/10.1111/j.1461-0248.2011.01653.x
Singh, J., A. S. Nanda, & G. P. Adams. 2000. The reproductive pattern efficiency of female. Anim. Reprod. Sci. 60(Suppl. 61):593-604. https://doi.org/10.1016/S0378-4320(00)00109-3
Syarifuddin, A., N. D. I. L. Desak, & B. Wayan. 2012. Effectiveness of the addition of various β-carotene concentrations to motility and viability of Bali cattle spermatozoa post thawing. Indonesia. Med. Vet. 1(Suppl. 2):173-185.
Ting-xi, H. U., Z. H. U. Hua-bin, S. U. N. Wei-jun, H. A. O Hai-sheng, Z. H. A. O. Xue-ming, D. U. Wei-hua, & W. A. N. G. Zong-li. 2016. Sperm pretreatment with glutathione improves IVF embryos development through increasing the viability and antioxidative capacity of sex-sorted and unsorted bull semen. Integrative Agriculture. 15(Suppl. 10):2326-2335. https://doi.org/10.1016/S2095-3119(16)61402-8
Toker, M. B., S. Alcay, E. Gokce, & B. Ustuner. 2017. Cryopreservation of ram semen with antioxidant supplemented soybean lecithin-based extenders and impacts on incubation resilience. Cryobiology. 72:205-209. https://doi.org/10.1016/j.cryobiol.2016.05.001
Uysal, O., M. N. Bucak, I. Yavas, & O. Varish. 2007. Effect of various antioxidantson the quality of frozen-thawed bull semen. J. Anim. Vet. Adv. 6(Suppl. 12):1362-1366
Wanapat, M., & V. Chanthakhoun. 2015. Buffalo production for emerging market as a potential animal protein source for global population. Buffalo Bull. 34(Suppl. 2): 164-180.
Wang, X., R. K. Sharma, S. C. Sikka, A. J. Thomas Jr, T. Falcone, & A. Agarwal. 2003. Oxsidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients eith male factor infertility. Fertil. Steril. 80:531-535
https://doi.org/10.1016/S0015-0282(03)00756-8
Yeste, M., E. Estrada, E. Pinart, S. Bonet, J. Miro, & J. E. Rodriguez-Gil. 2014. The improving effect of reduced glutathione on boar sperm cryotolerance is related with the intrinsic ejaculate freezability. Cryobiology. 68:251-261.
https://doi.org/10.1016/j.cryobiol.2014.02.004
Yulnawati, Y., H. Maheshwari, M. Rizal, & A. Boediono. 2013. The success rate of artificial insemination using post-thawed spotted buffaloes epididymal sperm. J. Met. Pet. 36(Suppl. 2):101-105. https://doi.org/10.5398/medpet.2013.36.2.101
Ansari, M.S., B. A. Rakha, N. Ullah, S. M. H. Andrabi, & S. Akhter. 2011. Glutathione addition of cooled buffalo (Bubalus bubalis) bull semen. Pakistan J. Zool. 43(Suppl. 1):49-55.
Asadpour, R. M. M. Pourseif, & G. Moghadam. 2012. Effect of vitamin B12 addition to extenders on some physicochemical parameters of semen in crossbred rams. African. J. Biotechnol. 54:11741-11745.
Bansal, A.K., & G. S. Bilaspuri. 2011. Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 2011: 1-7.
https://doi.org/10.4061/2011/686137
Batista, M., T. Nino, D. Alamo, N. Castro, M. Santana, F. Gonzalez, F. Cabrera, & A. Gracia. 2009. Successful artificial insemination using semen frozen and stored by an ultrafreezer in the Majorera goat breed. Theriogenology 71:1307-1315.
https://doi.org/10.1016/j.theriogenology.2008.12.024
BPS (Central Statistical Board) of Indonesia. 2016. https://www.bps.go.id/linkTableDinamis/view. Accessed on August 20th, 2017
Bucak, M.N., P. B. Tuncer, S. Sariözkan, N. Baspinar, M. Taspinar, K. Coyan, A. Bilqili, P. P. Alkalin, S. Büyükleblebici, S. Aydos, S. Ilgaz, A. Sunguroğlu, & D. Oztuna. 2010a. Effects of antioxidants on post-thawed bovine sperm and oxidative stress parameters: antioxidants protect DNA integrity against cryodamage. Cryobiology. 61(Suppl. 3):248-53. https://doi.org/10.1016/j.cryobiol.2010.09.001
Bucak, M.N., S. Sariözkan, & P. B. Tuncer. 2010b. The effect of antioxidants on post-thawed Angora goat (Capra hircus ancryrensis) sperm parameters, lipid peroxidation and antioxidant activities. Small Rumin Res. 89(Suppl.1):24-30.
https://doi.org/10.1016/j.smallrumres.2009.11.015
Cruz, L. C. 2007. Trends in buffalo production in Asia. Italian J. Anim. Sci. 6(Suppl. 2): 9-24. https://doi.org/10.4081/ijas.2007.s2.9
Eriani, K.,M. Ihdina, R. Rosnizar, D. Dasrul, S. Suhartono, & M. Rizal. 2017a. Cryopreservation of Aceh swamp buffalo (Bubalus bubalis) semen with combination of glyserol and lactose. Biosaintifika. 9(Suppl 3):409-416. https://doi.org/10.15294/biosaintifika.v9i3.11426
Eriani, K.,N. Sari, M. Ihdina, & Rosnizar. 2017b. The effect of equilibration time on semen freezing of local swamp buffalo (Bubalus bubalis) with combination extender of lactose and glycerol. Nus Biosci. 9(Suppl 1):77-82. https://doi.org/10.13057/nusbiosci/n090113
Eveson, D. P. 2016. The Sperm Chromatin Structure Assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Anim. Reprod. Sci. 169:56-75. https://doi.org/10.1016/j.anireprosci.2016.01.017
Fang, Y.I., R. Zhonga, L. Chenb, C. Feng, H. Suna, & D. Zhoua. 2015. Effects of astaxanthin supplementation on the sperm quality and antioxidant capacity of ram semen during liquid storage. Small. Rumin. Res.130:178-182
https://doi.org/10.1016/j.smallrumres.2015.05.016
Gunawan, I., D. N. Laksmi, & D. I. Trilaksana. 2012. The effectiveness of the addition of b-carotene and glutathione in diluent materials to sperm motility and viability at cryopreservation semen cattle. Indonesia. Med. Vet. 1(Suppl. 3):385.
Holt, W. V. 2000. Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology. 53:4758.
https://doi.org/10.1016/S0093-691X(99)00239-3
Judi, T. L. Yusuf, B. Purwantara, D. Sajuthi, M. Agil, J. Manangsang, R. Sudarwati, Y. T. Hastuti, B. Huaso, A. Widianti, & S. Prastitic. 2012. Successful intracervical insemination and characteristics of anoa (Bubalus sp.) parturation behavior in captivity. J. Med. Pet. 32(Suppl. 2):73-79. https://doi.org/10.5398/medpet.2012.35.2.73
Kasimanickam, R., V. Kasimanickam, K. D. Pelzer, & J. J. Dascanio. 2007. Effect of breed and sperm concentration on the changes in structural, functional and motility parameters of ramlamb spermatozoa during storage at 4oC. Anim Reprod Sci. 101:60 -73. https://doi.org/10.1016/j.anireprosci.2006.09.001
Krakowski, L., J. Obara, A. Wachocka, T. Piech, P. Bartoszek, K. Kostro, & M. R. Tatara. 2013. Assessment of extent of apoptosis and DNA defragmentation in chilled semen of stallions during the breeding season. Reprod. Domest. Anim. 48:826-832.
https://doi.org/10.1111/rda.12170
Kumaresan, A., M. R. Ansari, & G. Abhishek. 2005. Modulation of post-thaw sperm functions with oviductal proteins in buffaloes. Anim. Reprod. Sci. 90:73-84.
https://doi.org/10.1016/j.anireprosci.2005.01.009
Layek, S. S., T. K. Mohanty, A. Kumaresan, & J. E. Parks. 2016. Cryopreservation of bull semen: evolution from egg yolk based to soybean based extenders. Anim. Reprod. Sci. 172:1-9. https://doi.org/10.1016/j.anireprosci.2016.04.013
Marti, J. I., E. Marti, J. A. Cebrian-Perez, & T. Muino Blanco. 2003. Survival rate and antioxidant enzyme activity of ram spermatozoa after dilution with different extenders or selection by a dextran swim-up procedure. Theriogenology. 60:1025-1037.
https://doi.org/10.1016/S0093-691X(03)00105-5
Memon, A.A., H. Wahid, Y. Rosnina, Y. M. Goh, M. Ebrahimi, F. M. Nadia, & G. Audrey. 2011. Effect of butylated hydoxytoluene on cryopreservation of boer goat semen in tris egg yolk extender. Anim. Reprod. Sci. 129:44-49.
https://doi.org/10.1016/j.anireprosci.2011.10.004
Memon, A. A., H. Wahid, Y. Rosnina, Y. M. Goh, M. Ebrahimi, & F. M. Nadia. 2012. Effect of antioxidants on post thaw microscopic, oxidative stress parameter and fertility of boer goat spermatozoa in tris egg yolk glycerol extender. Anim. Reprod. Sci. 136:55-60. https://doi.org/10.1016/j.anireprosci.2012.10.020
Morrell, J. M., T. Nongbua, S. Veleanu, I. L. Verde, K. Lundstedt-Enkel, A. Edman, & A. Johannisson. 2017. Sperm quality variables as indicators of bull fertility may be breed dependent. Anim. Reprod. Sci. 185:42-52.
https://doi.org/10.1016/j.anireprosci.2017.08.001
Oshima, S. F., H. Ojima, Y. Sakamoto, Ishiguro, & J. Terao. 1993. Inhibitory effect of -carotene and asthaxanthin on phorosensitizied oxidation of phospolipid bilayers. Nur. Sci. Vitaminol. 39(Suppl. 3):607-615. https://doi.org/10.3177/jnsv.39.607
Pryor, W. A., W. Stahl, & C. L. Roch. 2000. β-Carotene: from biochemistry to clinical trials. Nutr. Rev.58:39-53. https://doi.org/10.1111/j.1753-4887.2000.tb07810.x
Rizal, M. 2005. Effectivity various concentrations of β-carotene on the quality of frozen Garut sheep semen. Anim. Prod. 7(Suppl. 1):6-13
Sariözkan, S., M. N. Bucak, P. B. Tuncer, S. Buyukleblebici, & F. Canturk. 2014. Influence of various antioxidants added to TCM-199 on post-thaw bovine sperm parameters, DNA integrity and fertilizing ability. Cryobiology. 68:129-133.
https://doi.org/10.1016/j.cryobiol.2014.01.007
Sariözkan, S., P. B. Tuncer, M. N. Bucak, & P. A. Ulutas. 2009. Influence of various antioxidants on microscopic-oxidative stress indicators and fertilizing ability of frozen-thawed bull semen. ACTA VET. BRNO. 78:463-469.
https://doi.org/10.2754/avb200978030463
Sarsaifi, K., H. Y. Rosnina, O. M. Ariff, H. A. Wahid, H. Hani, N. Yimer, S. W. Naing, & M. O. Abas. 2013. Effects of semen collection methods on the quality of pre and post thawed Bali cattle (Bos javanicus) spermatozoa. Reprod. Domest. Anim. 44(Suppl. 6):1006-1012. https://doi.org/10.1111/rda.12206
Siahaan, E. A., D. N. D. I.Laksmi, & W. Bebas. 2012. Efectivity of addition of various concentration β-carotene on motility and viability of Bali cattle spermatozoa post thawing. Indonesia.Med.Vet.1(Suppl 2):239-251.
Sianturi, R. G., B. Purwantara, I. Supriatna, Amrozi, & P. Situmorang. 2012. Optimasi inseminasi buatan pada kerbau lumpur (Bubalus bubalis) melalui teknis sinkronisasi estrus dan ovulasi. JITV. 17(Suppl 2):92-99.
Simmons, L. W. 2011. Effects of vitamins E and beta-carotene on sperm competitiveness. Ecology Letters. 14:891-895.
https://doi.org/10.1111/j.1461-0248.2011.01653.x
Singh, J., A. S. Nanda, & G. P. Adams. 2000. The reproductive pattern efficiency of female. Anim. Reprod. Sci. 60(Suppl. 61):593-604. https://doi.org/10.1016/S0378-4320(00)00109-3
Syarifuddin, A., N. D. I. L. Desak, & B. Wayan. 2012. Effectiveness of the addition of various β-carotene concentrations to motility and viability of Bali cattle spermatozoa post thawing. Indonesia. Med. Vet. 1(Suppl. 2):173-185.
Ting-xi, H. U., Z. H. U. Hua-bin, S. U. N. Wei-jun, H. A. O Hai-sheng, Z. H. A. O. Xue-ming, D. U. Wei-hua, & W. A. N. G. Zong-li. 2016. Sperm pretreatment with glutathione improves IVF embryos development through increasing the viability and antioxidative capacity of sex-sorted and unsorted bull semen. Integrative Agriculture. 15(Suppl. 10):2326-2335. https://doi.org/10.1016/S2095-3119(16)61402-8
Toker, M. B., S. Alcay, E. Gokce, & B. Ustuner. 2017. Cryopreservation of ram semen with antioxidant supplemented soybean lecithin-based extenders and impacts on incubation resilience. Cryobiology. 72:205-209. https://doi.org/10.1016/j.cryobiol.2016.05.001
Uysal, O., M. N. Bucak, I. Yavas, & O. Varish. 2007. Effect of various antioxidantson the quality of frozen-thawed bull semen. J. Anim. Vet. Adv. 6(Suppl. 12):1362-1366
Wanapat, M., & V. Chanthakhoun. 2015. Buffalo production for emerging market as a potential animal protein source for global population. Buffalo Bull. 34(Suppl. 2): 164-180.
Wang, X., R. K. Sharma, S. C. Sikka, A. J. Thomas Jr, T. Falcone, & A. Agarwal. 2003. Oxsidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients eith male factor infertility. Fertil. Steril. 80:531-535
https://doi.org/10.1016/S0015-0282(03)00756-8
Yeste, M., E. Estrada, E. Pinart, S. Bonet, J. Miro, & J. E. Rodriguez-Gil. 2014. The improving effect of reduced glutathione on boar sperm cryotolerance is related with the intrinsic ejaculate freezability. Cryobiology. 68:251-261.
https://doi.org/10.1016/j.cryobiol.2014.02.004
Yulnawati, Y., H. Maheshwari, M. Rizal, & A. Boediono. 2013. The success rate of artificial insemination using post-thawed spotted buffaloes epididymal sperm. J. Met. Pet. 36(Suppl. 2):101-105. https://doi.org/10.5398/medpet.2013.36.2.101
Authors
ErianiK., AzharA., IhdinaM., RosadiB., RizalM., & BoedionoA. (2018). Quality Enhancement of Aceh Swamp Buffalo (Bubalus bubalis) Frozen Semen by Supplementing β-Carotene. Tropical Animal Science Journal, 41(1), 1-7. https://doi.org/10.5398/tasj.2018.41.1.1
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