Superoxide Dismutase (SOD) Activity in Cryopreserved Semen of Itik Pinas-Khaki (Anas platyrhynchos L.)
Abstract
Cryopreservation induces oxidative stress on sperm due to an increase in the number of reactive oxygen species (ROS), thereby resulting in decreased sperm quality. ROS's destructive potential is normally counteracted in sperm by their innate antioxidant system consisting of enzymes, which include superoxide dismutase (SOD). This study aimed to assess the quality of semen from Itik Pinas-Khaki (IP-Khaki) drakes that were cryopreserved with either 4.5% DMSO or 7.0% glycerol as cryoprotectant through evaluation of total sperm motility (%) and determination of SOD activity (U/mL). Here, semen samples were collected from 12 sexually mature IP-Khaki drakes, an improved egg-type breed of Philippine mallard duck, and processed using modified reported cryopreservation procedure for ducks. Results showed that post-thawing total sperm motility averages of 12.04±5.61% using 4.5% DMSO and 13.99±5.28% using 7.0% glycerol were comparable. Moreover, similar SOD activity levels of 0.39±0.18 U/mL with 4.5% DMSO and 0.33±0.21 U/mL with 7.0% glycerol in 2.00 x 108 IP- Khaki sperm cells were also observed. The observed very low intracellular SOD activity indicates severe damage to sperm cells due to cryopreservation, which resulted in a comparably low total sperm motility with either of the cryoprotectants. Thus, the cryopreservation protocol used is not the optimum for IP- Khaki semen based on the observed considerable decline in sperm motility and very low SOD activity after cryopreservation.
References
Abouelezz, F. M., M.A. Sayed, & J. Santiago-Moreno. 2017. Fertility disturbances of dimethylacetamide and glycerol in rooster sperm diluents: Discrimination among effects produced pre and post freezing-thawing process. Anim. Reprod. Sci. 184:228-234. https://doi.org/10.1016/j.anireprosci.2017.07.021
Aitken, R.J. 2020. Impact of oxidative stress on male and female germ cells: implications for fertility. Reprod. 159: R189-R201. https://doi.org/10.1530/REP-19-0452
Aramli, M., M. Kalbassi, R. Nazari, & S. Aramli. 2013. Effects of short-term storage on the motility, oxidative stress, and ATP content of Persian sturgeon (Acipenser persicus) sperm. Anim. Reprod. Sci. 143:112-117. https://doi.org/10.1016/j.anireprosci.2013.10.010
Atifah, Y., Y. Sistina, & D.M. Saleh. 2018. Morphology of local duck (Anas platyrhyncos) spermatozoa post preservation in different medium combined in egg yolk cryoprotectant. BioLink. 4:121-129. https://doi.org/10.31289/biolink.v4i2.970
Aya, R.A. 2018. Genetic improvement of Itik Pinas to be continued in new R&D facility. http://www.pcaarrd.dost.gov.ph/home/portal/index.PhP/quick-information-dispatch/3217-genetic-improvement-of-itik-pinas-to-be-continued-in-new-r-d-facility
Bansal, A. K. & G. S. Bilaspuri. 2011. Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 11:1-7. https://doi.org/10.4061/2011/686137
Blanch, E., C. Tomás, L. Casares, E.A. Gómez, S. Sansano, & I. Giménez. 2014. Development of methods for cryopreservation of rooster sperm from the endangered breed “Gallina Valenciana de Chulilla” using low glycerol concentrations. Theriogenology. 81: 1174-1180. https://doi.org/10.1016/j.theriogenology.2014.01.019
Blanco, J. M., G. Gee, D.E. Wildt, & A.M. Donoghue. 2011. Comparative cryopreservation of avian spermatozoa: Benefits of non-permeating osmoprotectants and ATP on turkey and crane sperm cryosurvival. Anim. Reprod. Sci. 123:242-248. https://doi.org/10.1016/j.anireprosci.2010.12.005
Blanco, J. M., G. Gee, D.E. Wildt, & A.M. Donoghue. 2012. Comparative cryopreservation of avian spermatozoa: Effects of freezing and thawing rates on turkey and sandhill crane sperm cryosurvival. Anim. Reprod. Sci. 131:1-8. https://doi.org/10.1016/j.anireprosci.2012.02.001
Bootwalla, S.M. & R.D. Miles. 1992. Development of diluents for domestic fowl semen. Poult. Sci. J. 48:121–128. https://doi.org/10.1079/WPS19920012
Borziak, K., A. Fernandez, T. Karr, T. Pizzari, & S. Dorus. 2016. The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication. Sci. Rep. 6:35864. https://doi.org/10.1038/srep35864
Burrows, W.H. & J.P. Quinn. 1935. A method of obtaining spermatozoa from the domestic fowl. Poult. Sci. J. 14: 251-253. https://doi.org/10.3382/ps.0140251
Capitan, S.S. & O.A. Palad. 1999. Manual for Artificial Breeding of Farm Animals. College of Agriculture Publications Program, Los Baños.
Chen Y. C., H.C. Liu, L.Y. Wei, J.F. Huang, C.C. Lin, E. Blesbois, & M.C. Chen. 2016. Sperm quality parameters and reproductive efficiency in muscovy duck (Cairina moschata). J. Poult. Sci. 53:223-232. https://doi.org/10.2141/jpsa.0150162
Churchil, R., P. Praveena, & D. Sharma. 2014. Semen quality parameters, their inter-relationship and post-washing sperm attributes of Rhode Island Red roosters. Vet. World. 7:1117-1122. https://doi.org/10.1016/j.theriogenology.2017.05.016
Comizzoli, P. 2015. Biobanking efforts and new advances in male fertility preservation for rare and endangered species. Asian J. Androl. 17:640-645. https://doi.org/10.4103/1008-682X.153849
Cyriac, S., L. Joseph, P.A. Peethambaran, K. Narayanankutty, & K. Karthiayini. 2013. Semen quality characteristics of White Pekin, Kuttanad (Anas platyrhynchos domesticus) and Muscovy (Cairina moschata momelanotus) drakes. Indian J. Anim. Sci. 83: 595-599.
Di Iorio, M., G. Rusco, R. Iampietro, M.A. Colonna, L. Zaniboni, S. Cerolini, & N. Iaffaldano. 2020. Finding an effective freezing protocol for Turkey semen: Benefits of ficoll as non-permeant cryoprotectant and 1:4 as dilution rate. Animals (Basel). 10:421. https://doi.org/10.3390/ani10030421
Elliot, G.D., S. Wang, & B.J. Fuller. 2017. Cryoprotectants: A review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures. Cryobiology. 76: 74-91. https://doi.org/10.1016/j.cryobiol.2017.04.004
Esguerra, J.M., J.H. Quimio, G.A. Dichoso, C.L. Junsay, V.A. Magpantay, & P.P. Sangel. 2020. Coconut water with either tomato juice or garlic extract as extender components for Paraoakan native chicken semen at different storage temperatures. Philipp J. Sci. 149: 121-131.
Evangelista-Vargas, S. & A. Santiani. 2017. Detection of intracellular reactive oxygen species (superoxide anion and hydrogen peroxide) and lipid peroxidation during cryopreservation of alpaca spermatozoa. Reprod. Domest. Anim. 52:819-824. https://doi.org/10.1111/rda.12984
Gerzilov, V. 2010. Influence of various cryoprotectants on the sperm mobility of Muscovy semen before and after cryopreservation. J. Agri. Sci. 2:57-60.
Gerzilov, V., P. Rashev, A. Bochukov, & P. Bonchev. 2011. Effect of semen extenders on sperm motion of in vitro stored Muscovy drake spermatozoa. Biotech. Anim. Husbandry 27: 733-740. https://doi.org/10.2298/BAH1103733G
Han, X.F., Z.Y. Niu, F.Z. Liu, & C.S. Yang. 2005. Effect of diluents, cryoprotectants, equilibrium time and thawing temperature on cryopreservation of duck semen. Intern. J. Poult. Sci. 4: 197-201. https://doi.org/10.3923/ijps.2005.197.201
Hu, J., W. Tian, X. Zhao, L. Zan, H. Wang, Q. Li, & Y. Xin. 2010. The cryoprotective effects of ascorbic acid supplementation on bovine semen quality. Anim. Reprod. 121: 272-77. https://doi.org/10.1016/j.anireprosci.2010.04.180
Huang, X., P. Zhuang, L. Zhang, F. Zhao, J. Liu, G. Feng, & T. Zhang. 2014a. Effects of cryopreservation on motility characteristics and enzyme activity of sperm in a Chinese fish, Nibea albiflora. Cryo-Letters 35:267-276.
Huang, X., P. Zhuang, L. Zhang, F. Zhao, J. Liu, G. Feng, & T. Zhang. 2014b. Effect of cryopreservation on the enzyme activity of Russian sturgeon (Acipenser gueldenstaedtii Brandt & Ratzeburg, 1833) semen. J. Appl. Ichthyol. 30:1585-1589. https://doi.org/10.1111/jai.12608
Ighodaro, O.M. & O.A. Akinloye. 2018. First line defense antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX); Their fundamental role in the entire antioxidant defense grid. Alexandria J. Med. 54:287-293. https://doi.org/10.1016/j.ajme.2017.09.001
Kadirve, G., S. Kumar, S.K. Gosh, & P. Perumal. 2014. Activity of antioxidative enzymes in fresh and frozen thawed buffalo (Bubalus bubalis) spermatozoa in relation to lipid peroxidation and semen quality. Asian Pac. J. Reprod. 3: 210-217. https://doi.org/10.1016/S2305-0500(14)60028-2
Kasai, K. & A. Izumo. 2001. Efficiency of artificial vagina method in semen collection from Osaka Drakes. J. App. Poult. Res. 10:206-210. https://doi.org/10.1093/japr/10.3.206
Khaeruddin, K., M. Kurniawan, & S. Soman. 2019. Cryopreservation of Kampung rooster semen using egg yolk diluent from four types of poultry with different concentrations. J. Ked. Hewan. 13: 60-65. https://doi.org/10.21157/1021157/j.ked.hewan.vl3i3.14892
Khan, R.U. 2011. Antioxidants and poultry semen quality. World Poult. Sci. J. 67:297-308. https://doi.org/10.1017/S0043933911000316
Kim, S., Y. Lee, & Y. Kim. 2011. Changes in sperm membrane and ROS following cryopreservation of liquid boar semen stored at 15˚C. Anim Reprod Sci. 124:118-124. https://doi.org/10.1016/j.anireprosci.2011.01.014
Lasso, J.L., E.E. Noiles, J.G. Alvarez, & B.T. Storey. 1994. Mechanism of superoxide dismutase loss from human sperm cells during cryopreservation. J. Androl. 15: 255-265. https://doi.org/10.1002/j.1939-4640.1994.tb00444.x
Lone, S. A., J.K. Prasad, S.K. Ghosh, G.K. Das, B. Balamurugan, & M.R. Verma. 2018. Study on correlation of sperm quality parameters with antioxidant and oxidant status of buffalo bull semen during various stages of cryopreservation. Andrologia. 50(4). https://doi.org/10.1111/and.12970
Long, J.A. 2006. Avian semen cryopreservation: what are the biological challenges? Poult. Sci. J. 85:232-236. https://doi.org/10.1093/ps/85.2.232
Long, J.A, D.C. Bongalhardo, J. Pelaéz, S. Saxena, P. Settar, N.P. O’Sullivan, & J.E. Fulton. 2010. Rooster semen cryopreservation: Effect of pedigree line and male age on postthaw sperm function. Poult. Sci. 89: 966-973. https://doi.org/10.3382/ps.2009-00227
Majhi, R. K., A. Kumar, M. Yadav, P. Kumar, A. Maity, S. C. Giri, & C. Goswami. 2016. Light and electron microscopic study of mature spermatozoa from White Pekin duck (Anas platyrhynchos): An ultrastructural and molecular analysis. Andrology. 4:232-244. https://doi.org/10.1111/andr.12130
Malik, A., A.W. Haron, R. Yusoff, M. Nesa, M. Bukar, & A. Kasim. 2013. Evaluation of the ejaculate quality of the red jungle fowl, domestic chicken, and bantam chicken in Malaysia. Turk. J. Vet. Anim. Sci. 37: 564–568. https://doi.org/10.3906/vet-1107-26
Marti, E., J.I. Marti, T. Muiño-Blanco, & A. Cebrián-Pérez. 2008. Effect of cryopreservation process on the activity and immunolocalization of antioxidant enzymes in ram spermatozoa. J. Androl. 29: 459-467. https://doi.org/10.2164/jandrol.107.003459
Mphaphathi, M. L., D. Luseba, B. Sutherland, & T.L. Nedambale. 2012. Comparison of slow freezing and vitrification methods for Venda cockerel’s spermatozoa. Open J. Anim. Sci. 2:204-210. https://doi.org/10.4236/ojas.2012.23028
Mohanty, T.K., S.A. Lone, A. Kumaresan, A. Bhakat, R. Kumar, R.K. Baithalu, R. Sinha, A.R. Paray, H.P. Yadav, S.K. Sahu, & A.K. Mohanty. 2018. Sperm dosage and site of insemination in relation to fertility in bovines. Asian Pac. J. Reprod. 7:1-5. https://doi.org/10.4103/2305-0500.220977
Mossa, R.K. 2006. Characterization of Iraqi local drake ejaculate and effect of frequency of collection in sperm quality. Bas. J. Vet. Res. 5 :146-152. https://doi.org/10.33762/bvetr.2006.59047
Nahak, A.K., S.C. Giri, D.N. Mohanty, P.C. Mishra, & S.K. Dash. 2015. Effect of frequency of collection on seminal characteristics of White Pekin duck. Asian Pac. J. 4:70-73. https://doi.org/10.1016/S2305-0500(14)60062-2
Nor-Ashikin M. N. & R. B. Abdullah. 2011. Comparison between tris-citric acid yolk, yolk albumin citrate and skimmed milk extenders on sperm motility, livability and mass movement in frozen-thawed goat sperm. Biomed. Res. 22(3).
Orzołek, A., P. Wysocki, J. Strzezek, & W. Kordan. 2013. Superoxide dismutase (SOD) in boar spermatozoa: Purification, biochemical properties and changes in activity during semen storage (16 °C) in different extenders. Reprod. Biol. 13:34-40. https://doi.org/10.1016/j.repbio.2013.01.176
Partyka, A, E. Łukaszewicz, & W. Niżański. 2012a. Effect of cryopreservation on sperm parameters, lipid peroxidation and antioxidant enzymes activity in fowl semen. Theriogenology. 77: 1497-1504. https://doi.org/10.1016/j.theriogenology.2011.11.006
Partyka, A, E. Łukaszewicz, & W. Niżański. 2012b. Lipid peroxidation and antioxidant enzymes activity in avian semen. Anim. Reprod. 134:184–190. https://doi.org/10.1016/j.anireprosci.2012.07.007
Partyka, A., W. Niżański, J. Bajzert, E. Łukaszewicz, & M. Ochota. 2013. The effect of cysteine and superoxide dismutase on the quality of post-thawed chicken sperm. Cryobiology 67: 132-136. https://doi.org/10.1016/j.cryobiol.2013.06.002
Parungao, A.R. 2016. Itik Pinas to boost the balut industry through increased duck egg production. http://www.pcaarrd.dost.gov.ph/home/portal/index.PhP/quick-information-dispatch/2751-itik-pinas-to-boost-the-balut-industry-through-increased-duck-egg-production?platform=hootsuite
Parungao, A.R. 2017. ITIK PINAS: Development, promotion and utilization in building rural enterprises. http://www.pcaarrd.dost.gov.ph/home/portal/index.PhP/quick-information-dispatch/2970-itik-pinas-development-promotion-and-utilization-in-building-rural-enterprises
Pelaéz, J., D.C. Bongalhardo, & J.A. Long. 2011. Characterizing the glycocalyx of poultry spermatozoa: III. Semen cryopreservation methods alter the carbohydrate component of rooster sperm membrae glycoconjugates. Poult. Sci. 90: 435-443. https://doi.org/10.3382/ps.2010-00998
Perumal, P. 2014. Effect of superoxide dismutase on semen parameters and antioxidant enzyme activities of liquid stored (5°C) mithun (Bos frontalis). Semen. J. Anim. 2014:1-9. https://doi.org/10.1155/2014/821954
Pinca, A., H. Bautista, C. Adiova, & P. Sangel. 2019. Comparative expression analysis of small intestine nutrient transporters sodium/glucose cotransporter 1 (SGLT1) and peptide transporter 1 (PepT1) between Itik Pinas (Anas platyrhynchos L.) and commercial layer chicken (Gallus gallus domesticus). Philipp J. Sci. 148:433-439.
Rakha, B.A., M.S. Ansari, S. Akhter S, I. Hussain, & E. Blesbois. 2016. Cryopreservation of Indian red jungle fowl (Gallus gallus murghi) semen. Anim. Reprod. 174:45–55. https://doi.org/10.1016/j.anireprosci.2016.09.004
Rakha, B.A., M.S. Ansari, S. Akhter, & E. Blesbois. 2018. Cryoprotective effect of glycerol concentrations on Indian Red Jungle Fowl (Gallus gallus murghi) spermatozoa. Avian Biol. Res. 11:80–88. https://doi.org/10.3184/175815618X15180876264262
Saint Jalme, M., R. Lecoq, F. Seigneurin, E. Blesbois, & E. Plouzeau. 2003. Cryopreservation of semen from endangered pheasants: The first step towards a cryobank for endangered avian species. Theriogenology 59:875-888. https://doi.org/10.1016/S0093-691X(02)01153-6
Slowinska, M., E. Liszewska, S. Judycka, M. Konopka, & A. Ciereszko. 2018. Mitochondrial membrane potential and reactive oxygen species in liquid stored and cryopreserved turkey (Melagris galopavo) spermatozoa. Poult. Sci. 97: 3709-3717. https://doi.org/10.3382/ps/pey209
Strzeżek, R, M. Koziorowska-Gilun, & M. Stawiszyńska. 2012. Cryopreservation of canine semen: the effect of two extender variants on the quality and antioxidant properties of spermatozoa. Pol. J. Vet. Sci. 15: 721-726. https://doi.org/10.2478/v10181-012-0109-0
Surai, P.F. & Wishart G.J. 1996. Poultry artificial insemination technology in the countries of the former USSR. World Poult. Sci. J. 52:27-43. https://doi.org/10.1079/WPS19960003
Surai, P.F., E. Blesbois, I. Grasseau, T. Chalah, J.-P. Brillard, G.J. Wishart, S. Cerolini, & N.H.C. Sparks. 1998. Fatty acid composition, glutathione peroxidase and superoxide dismutase activity and total antioxidant activity of avian semen. Comp. Biochem. Phys. A. 120-527-533. https://doi.org/10.1016/S0305-0491(98)10039-1
Surai, P. F., J. P. Brillard, B.K. Speake, E. Blesbois, F. Seigneurin, & N.H. Sparks. 2000. Phospholipid fatty acid composition, vitamin E content and susceptibility to lipid peroxidation of duck spermatozoa. Theriogenology 53:1025-1039. https://doi.org/10.1016/S0093-691X(00)00249-1
Surai, P.F. 2016. Antioxidant systems in poultry biology: superoxide dismutase. J. Anim. Res. 1: 1-17. https://doi.org/10.21767/2572-5459.100008
Surai, P. F., I.I. Kochish, V.I. Fisinin, & M.T. Kidd. 2019. Antioxidant defence systems and oxidative stress in poultry biology: an update. Antioxidants (Basel). 8: 235. https://doi.org/10.3390/antiox8070235
Svoradová, A., L. Kuželova, J. Vašíček, A. Baláži, & E. Hanusová. 2018. In vitro effect of various cryoprotectants on the semen quality of endangered Oravka chicken. Zygote 26: 33-39. https://doi.org/10.1017/S0967199417000685
Tatone, C., G. Di Emidio, M. Vento, R. Ciriminna, & P.G. Artini. 2010. Cryopreservation and oxidative stress in reproductive cells. Gynecol. Endocrinol. 26:563-567. https://doi.org/10.3109/09513591003686395
Telnoni, S.P., R. Iis Arifiantini, T.L. Yusuf, & S. Darwati. 2017. SK Kedu semen cryopreservation in beltsville poultry semen extender and lactated ringer’s-egg yolk extender using dimethyl sulfoxie. Asian J. Poult. Sci. 11: 14-19. https://doi.org/10.3923/ajpsaj.2017.14.19
Thelie, A., A. Bailliard, F. Seigneurin, T. Zerjal, M. Biochard, & E. Blesbois. 2019. Chicken semen cryopreservation and use for the restoration of rare genetic resources. Poult. Sci. 98:446-455. https://doi.org/10.3382/ps/pey360
Van Voorst, A. & F.R. Leenstra. 1995. Effect of dialysis before storage or cryopreservation on fertilizing ability of fowl semen. Poult. Sci. J. 74: 141-146. https://doi.org/10.3382/ps.0740141
Wang, X., X. Shi, Y. Liu, D. Yu, S. Guan, Q. Liu, & J. Li. 2016. Effects of chilled storage and cryopreservation on sperm characteristics, antioxidant enzyme activities, and lipid peroxidation in Pacific cod Gadus microcephalus. Chin. J. Oceanol. Limn. 34:763–771. https://doi.org/10.1007/s00343-016-5088-z
Wang, Y., R. Branicky, A. Noë, & S. Hekimi. 2018. Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. J. Cell. Biol. 217:1915-1928. https://doi.org/10.1083/jcb.201708007
Zakošek Pipan, M., J. Mrkun, M. Kosec, A. Nemec Svete, & P. Zrimšek. 2014. Superoxide dismutase: a predicting factor for boar semen characteristics for short-term preservation. Hindawi 2014:1-7. https://doi.org/10.1155/2014/105280
Zaniboni L., C. Cassinelli, M.G. Mangiagalli, T.M. Gliozzi, & S. Cerolini. 2014. Pellet cryopreservation for chicken semen: effects of sperm working concentration, cryoprotectant concentration and equilibration time during in vitro processing. Theriogenology 82:251-8. https://doi.org/10.1016/j.theriogenology.2014.04.007
Zawadzka J., E. Łukaszewicz, & A. Kowalczyk. 2015. Comparative semen analysis of two Polish duck strains from a conservation programme. Europ. Poult. Sci. 79.
Aitken, R.J. 2020. Impact of oxidative stress on male and female germ cells: implications for fertility. Reprod. 159: R189-R201. https://doi.org/10.1530/REP-19-0452
Aramli, M., M. Kalbassi, R. Nazari, & S. Aramli. 2013. Effects of short-term storage on the motility, oxidative stress, and ATP content of Persian sturgeon (Acipenser persicus) sperm. Anim. Reprod. Sci. 143:112-117. https://doi.org/10.1016/j.anireprosci.2013.10.010
Atifah, Y., Y. Sistina, & D.M. Saleh. 2018. Morphology of local duck (Anas platyrhyncos) spermatozoa post preservation in different medium combined in egg yolk cryoprotectant. BioLink. 4:121-129. https://doi.org/10.31289/biolink.v4i2.970
Aya, R.A. 2018. Genetic improvement of Itik Pinas to be continued in new R&D facility. http://www.pcaarrd.dost.gov.ph/home/portal/index.PhP/quick-information-dispatch/3217-genetic-improvement-of-itik-pinas-to-be-continued-in-new-r-d-facility
Bansal, A. K. & G. S. Bilaspuri. 2011. Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 11:1-7. https://doi.org/10.4061/2011/686137
Blanch, E., C. Tomás, L. Casares, E.A. Gómez, S. Sansano, & I. Giménez. 2014. Development of methods for cryopreservation of rooster sperm from the endangered breed “Gallina Valenciana de Chulilla” using low glycerol concentrations. Theriogenology. 81: 1174-1180. https://doi.org/10.1016/j.theriogenology.2014.01.019
Blanco, J. M., G. Gee, D.E. Wildt, & A.M. Donoghue. 2011. Comparative cryopreservation of avian spermatozoa: Benefits of non-permeating osmoprotectants and ATP on turkey and crane sperm cryosurvival. Anim. Reprod. Sci. 123:242-248. https://doi.org/10.1016/j.anireprosci.2010.12.005
Blanco, J. M., G. Gee, D.E. Wildt, & A.M. Donoghue. 2012. Comparative cryopreservation of avian spermatozoa: Effects of freezing and thawing rates on turkey and sandhill crane sperm cryosurvival. Anim. Reprod. Sci. 131:1-8. https://doi.org/10.1016/j.anireprosci.2012.02.001
Bootwalla, S.M. & R.D. Miles. 1992. Development of diluents for domestic fowl semen. Poult. Sci. J. 48:121–128. https://doi.org/10.1079/WPS19920012
Borziak, K., A. Fernandez, T. Karr, T. Pizzari, & S. Dorus. 2016. The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication. Sci. Rep. 6:35864. https://doi.org/10.1038/srep35864
Burrows, W.H. & J.P. Quinn. 1935. A method of obtaining spermatozoa from the domestic fowl. Poult. Sci. J. 14: 251-253. https://doi.org/10.3382/ps.0140251
Capitan, S.S. & O.A. Palad. 1999. Manual for Artificial Breeding of Farm Animals. College of Agriculture Publications Program, Los Baños.
Chen Y. C., H.C. Liu, L.Y. Wei, J.F. Huang, C.C. Lin, E. Blesbois, & M.C. Chen. 2016. Sperm quality parameters and reproductive efficiency in muscovy duck (Cairina moschata). J. Poult. Sci. 53:223-232. https://doi.org/10.2141/jpsa.0150162
Churchil, R., P. Praveena, & D. Sharma. 2014. Semen quality parameters, their inter-relationship and post-washing sperm attributes of Rhode Island Red roosters. Vet. World. 7:1117-1122. https://doi.org/10.1016/j.theriogenology.2017.05.016
Comizzoli, P. 2015. Biobanking efforts and new advances in male fertility preservation for rare and endangered species. Asian J. Androl. 17:640-645. https://doi.org/10.4103/1008-682X.153849
Cyriac, S., L. Joseph, P.A. Peethambaran, K. Narayanankutty, & K. Karthiayini. 2013. Semen quality characteristics of White Pekin, Kuttanad (Anas platyrhynchos domesticus) and Muscovy (Cairina moschata momelanotus) drakes. Indian J. Anim. Sci. 83: 595-599.
Di Iorio, M., G. Rusco, R. Iampietro, M.A. Colonna, L. Zaniboni, S. Cerolini, & N. Iaffaldano. 2020. Finding an effective freezing protocol for Turkey semen: Benefits of ficoll as non-permeant cryoprotectant and 1:4 as dilution rate. Animals (Basel). 10:421. https://doi.org/10.3390/ani10030421
Elliot, G.D., S. Wang, & B.J. Fuller. 2017. Cryoprotectants: A review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures. Cryobiology. 76: 74-91. https://doi.org/10.1016/j.cryobiol.2017.04.004
Esguerra, J.M., J.H. Quimio, G.A. Dichoso, C.L. Junsay, V.A. Magpantay, & P.P. Sangel. 2020. Coconut water with either tomato juice or garlic extract as extender components for Paraoakan native chicken semen at different storage temperatures. Philipp J. Sci. 149: 121-131.
Evangelista-Vargas, S. & A. Santiani. 2017. Detection of intracellular reactive oxygen species (superoxide anion and hydrogen peroxide) and lipid peroxidation during cryopreservation of alpaca spermatozoa. Reprod. Domest. Anim. 52:819-824. https://doi.org/10.1111/rda.12984
Gerzilov, V. 2010. Influence of various cryoprotectants on the sperm mobility of Muscovy semen before and after cryopreservation. J. Agri. Sci. 2:57-60.
Gerzilov, V., P. Rashev, A. Bochukov, & P. Bonchev. 2011. Effect of semen extenders on sperm motion of in vitro stored Muscovy drake spermatozoa. Biotech. Anim. Husbandry 27: 733-740. https://doi.org/10.2298/BAH1103733G
Han, X.F., Z.Y. Niu, F.Z. Liu, & C.S. Yang. 2005. Effect of diluents, cryoprotectants, equilibrium time and thawing temperature on cryopreservation of duck semen. Intern. J. Poult. Sci. 4: 197-201. https://doi.org/10.3923/ijps.2005.197.201
Hu, J., W. Tian, X. Zhao, L. Zan, H. Wang, Q. Li, & Y. Xin. 2010. The cryoprotective effects of ascorbic acid supplementation on bovine semen quality. Anim. Reprod. 121: 272-77. https://doi.org/10.1016/j.anireprosci.2010.04.180
Huang, X., P. Zhuang, L. Zhang, F. Zhao, J. Liu, G. Feng, & T. Zhang. 2014a. Effects of cryopreservation on motility characteristics and enzyme activity of sperm in a Chinese fish, Nibea albiflora. Cryo-Letters 35:267-276.
Huang, X., P. Zhuang, L. Zhang, F. Zhao, J. Liu, G. Feng, & T. Zhang. 2014b. Effect of cryopreservation on the enzyme activity of Russian sturgeon (Acipenser gueldenstaedtii Brandt & Ratzeburg, 1833) semen. J. Appl. Ichthyol. 30:1585-1589. https://doi.org/10.1111/jai.12608
Ighodaro, O.M. & O.A. Akinloye. 2018. First line defense antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX); Their fundamental role in the entire antioxidant defense grid. Alexandria J. Med. 54:287-293. https://doi.org/10.1016/j.ajme.2017.09.001
Kadirve, G., S. Kumar, S.K. Gosh, & P. Perumal. 2014. Activity of antioxidative enzymes in fresh and frozen thawed buffalo (Bubalus bubalis) spermatozoa in relation to lipid peroxidation and semen quality. Asian Pac. J. Reprod. 3: 210-217. https://doi.org/10.1016/S2305-0500(14)60028-2
Kasai, K. & A. Izumo. 2001. Efficiency of artificial vagina method in semen collection from Osaka Drakes. J. App. Poult. Res. 10:206-210. https://doi.org/10.1093/japr/10.3.206
Khaeruddin, K., M. Kurniawan, & S. Soman. 2019. Cryopreservation of Kampung rooster semen using egg yolk diluent from four types of poultry with different concentrations. J. Ked. Hewan. 13: 60-65. https://doi.org/10.21157/1021157/j.ked.hewan.vl3i3.14892
Khan, R.U. 2011. Antioxidants and poultry semen quality. World Poult. Sci. J. 67:297-308. https://doi.org/10.1017/S0043933911000316
Kim, S., Y. Lee, & Y. Kim. 2011. Changes in sperm membrane and ROS following cryopreservation of liquid boar semen stored at 15˚C. Anim Reprod Sci. 124:118-124. https://doi.org/10.1016/j.anireprosci.2011.01.014
Lasso, J.L., E.E. Noiles, J.G. Alvarez, & B.T. Storey. 1994. Mechanism of superoxide dismutase loss from human sperm cells during cryopreservation. J. Androl. 15: 255-265. https://doi.org/10.1002/j.1939-4640.1994.tb00444.x
Lone, S. A., J.K. Prasad, S.K. Ghosh, G.K. Das, B. Balamurugan, & M.R. Verma. 2018. Study on correlation of sperm quality parameters with antioxidant and oxidant status of buffalo bull semen during various stages of cryopreservation. Andrologia. 50(4). https://doi.org/10.1111/and.12970
Long, J.A. 2006. Avian semen cryopreservation: what are the biological challenges? Poult. Sci. J. 85:232-236. https://doi.org/10.1093/ps/85.2.232
Long, J.A, D.C. Bongalhardo, J. Pelaéz, S. Saxena, P. Settar, N.P. O’Sullivan, & J.E. Fulton. 2010. Rooster semen cryopreservation: Effect of pedigree line and male age on postthaw sperm function. Poult. Sci. 89: 966-973. https://doi.org/10.3382/ps.2009-00227
Majhi, R. K., A. Kumar, M. Yadav, P. Kumar, A. Maity, S. C. Giri, & C. Goswami. 2016. Light and electron microscopic study of mature spermatozoa from White Pekin duck (Anas platyrhynchos): An ultrastructural and molecular analysis. Andrology. 4:232-244. https://doi.org/10.1111/andr.12130
Malik, A., A.W. Haron, R. Yusoff, M. Nesa, M. Bukar, & A. Kasim. 2013. Evaluation of the ejaculate quality of the red jungle fowl, domestic chicken, and bantam chicken in Malaysia. Turk. J. Vet. Anim. Sci. 37: 564–568. https://doi.org/10.3906/vet-1107-26
Marti, E., J.I. Marti, T. Muiño-Blanco, & A. Cebrián-Pérez. 2008. Effect of cryopreservation process on the activity and immunolocalization of antioxidant enzymes in ram spermatozoa. J. Androl. 29: 459-467. https://doi.org/10.2164/jandrol.107.003459
Mphaphathi, M. L., D. Luseba, B. Sutherland, & T.L. Nedambale. 2012. Comparison of slow freezing and vitrification methods for Venda cockerel’s spermatozoa. Open J. Anim. Sci. 2:204-210. https://doi.org/10.4236/ojas.2012.23028
Mohanty, T.K., S.A. Lone, A. Kumaresan, A. Bhakat, R. Kumar, R.K. Baithalu, R. Sinha, A.R. Paray, H.P. Yadav, S.K. Sahu, & A.K. Mohanty. 2018. Sperm dosage and site of insemination in relation to fertility in bovines. Asian Pac. J. Reprod. 7:1-5. https://doi.org/10.4103/2305-0500.220977
Mossa, R.K. 2006. Characterization of Iraqi local drake ejaculate and effect of frequency of collection in sperm quality. Bas. J. Vet. Res. 5 :146-152. https://doi.org/10.33762/bvetr.2006.59047
Nahak, A.K., S.C. Giri, D.N. Mohanty, P.C. Mishra, & S.K. Dash. 2015. Effect of frequency of collection on seminal characteristics of White Pekin duck. Asian Pac. J. 4:70-73. https://doi.org/10.1016/S2305-0500(14)60062-2
Nor-Ashikin M. N. & R. B. Abdullah. 2011. Comparison between tris-citric acid yolk, yolk albumin citrate and skimmed milk extenders on sperm motility, livability and mass movement in frozen-thawed goat sperm. Biomed. Res. 22(3).
Orzołek, A., P. Wysocki, J. Strzezek, & W. Kordan. 2013. Superoxide dismutase (SOD) in boar spermatozoa: Purification, biochemical properties and changes in activity during semen storage (16 °C) in different extenders. Reprod. Biol. 13:34-40. https://doi.org/10.1016/j.repbio.2013.01.176
Partyka, A, E. Łukaszewicz, & W. Niżański. 2012a. Effect of cryopreservation on sperm parameters, lipid peroxidation and antioxidant enzymes activity in fowl semen. Theriogenology. 77: 1497-1504. https://doi.org/10.1016/j.theriogenology.2011.11.006
Partyka, A, E. Łukaszewicz, & W. Niżański. 2012b. Lipid peroxidation and antioxidant enzymes activity in avian semen. Anim. Reprod. 134:184–190. https://doi.org/10.1016/j.anireprosci.2012.07.007
Partyka, A., W. Niżański, J. Bajzert, E. Łukaszewicz, & M. Ochota. 2013. The effect of cysteine and superoxide dismutase on the quality of post-thawed chicken sperm. Cryobiology 67: 132-136. https://doi.org/10.1016/j.cryobiol.2013.06.002
Parungao, A.R. 2016. Itik Pinas to boost the balut industry through increased duck egg production. http://www.pcaarrd.dost.gov.ph/home/portal/index.PhP/quick-information-dispatch/2751-itik-pinas-to-boost-the-balut-industry-through-increased-duck-egg-production?platform=hootsuite
Parungao, A.R. 2017. ITIK PINAS: Development, promotion and utilization in building rural enterprises. http://www.pcaarrd.dost.gov.ph/home/portal/index.PhP/quick-information-dispatch/2970-itik-pinas-development-promotion-and-utilization-in-building-rural-enterprises
Pelaéz, J., D.C. Bongalhardo, & J.A. Long. 2011. Characterizing the glycocalyx of poultry spermatozoa: III. Semen cryopreservation methods alter the carbohydrate component of rooster sperm membrae glycoconjugates. Poult. Sci. 90: 435-443. https://doi.org/10.3382/ps.2010-00998
Perumal, P. 2014. Effect of superoxide dismutase on semen parameters and antioxidant enzyme activities of liquid stored (5°C) mithun (Bos frontalis). Semen. J. Anim. 2014:1-9. https://doi.org/10.1155/2014/821954
Pinca, A., H. Bautista, C. Adiova, & P. Sangel. 2019. Comparative expression analysis of small intestine nutrient transporters sodium/glucose cotransporter 1 (SGLT1) and peptide transporter 1 (PepT1) between Itik Pinas (Anas platyrhynchos L.) and commercial layer chicken (Gallus gallus domesticus). Philipp J. Sci. 148:433-439.
Rakha, B.A., M.S. Ansari, S. Akhter S, I. Hussain, & E. Blesbois. 2016. Cryopreservation of Indian red jungle fowl (Gallus gallus murghi) semen. Anim. Reprod. 174:45–55. https://doi.org/10.1016/j.anireprosci.2016.09.004
Rakha, B.A., M.S. Ansari, S. Akhter, & E. Blesbois. 2018. Cryoprotective effect of glycerol concentrations on Indian Red Jungle Fowl (Gallus gallus murghi) spermatozoa. Avian Biol. Res. 11:80–88. https://doi.org/10.3184/175815618X15180876264262
Saint Jalme, M., R. Lecoq, F. Seigneurin, E. Blesbois, & E. Plouzeau. 2003. Cryopreservation of semen from endangered pheasants: The first step towards a cryobank for endangered avian species. Theriogenology 59:875-888. https://doi.org/10.1016/S0093-691X(02)01153-6
Slowinska, M., E. Liszewska, S. Judycka, M. Konopka, & A. Ciereszko. 2018. Mitochondrial membrane potential and reactive oxygen species in liquid stored and cryopreserved turkey (Melagris galopavo) spermatozoa. Poult. Sci. 97: 3709-3717. https://doi.org/10.3382/ps/pey209
Strzeżek, R, M. Koziorowska-Gilun, & M. Stawiszyńska. 2012. Cryopreservation of canine semen: the effect of two extender variants on the quality and antioxidant properties of spermatozoa. Pol. J. Vet. Sci. 15: 721-726. https://doi.org/10.2478/v10181-012-0109-0
Surai, P.F. & Wishart G.J. 1996. Poultry artificial insemination technology in the countries of the former USSR. World Poult. Sci. J. 52:27-43. https://doi.org/10.1079/WPS19960003
Surai, P.F., E. Blesbois, I. Grasseau, T. Chalah, J.-P. Brillard, G.J. Wishart, S. Cerolini, & N.H.C. Sparks. 1998. Fatty acid composition, glutathione peroxidase and superoxide dismutase activity and total antioxidant activity of avian semen. Comp. Biochem. Phys. A. 120-527-533. https://doi.org/10.1016/S0305-0491(98)10039-1
Surai, P. F., J. P. Brillard, B.K. Speake, E. Blesbois, F. Seigneurin, & N.H. Sparks. 2000. Phospholipid fatty acid composition, vitamin E content and susceptibility to lipid peroxidation of duck spermatozoa. Theriogenology 53:1025-1039. https://doi.org/10.1016/S0093-691X(00)00249-1
Surai, P.F. 2016. Antioxidant systems in poultry biology: superoxide dismutase. J. Anim. Res. 1: 1-17. https://doi.org/10.21767/2572-5459.100008
Surai, P. F., I.I. Kochish, V.I. Fisinin, & M.T. Kidd. 2019. Antioxidant defence systems and oxidative stress in poultry biology: an update. Antioxidants (Basel). 8: 235. https://doi.org/10.3390/antiox8070235
Svoradová, A., L. Kuželova, J. Vašíček, A. Baláži, & E. Hanusová. 2018. In vitro effect of various cryoprotectants on the semen quality of endangered Oravka chicken. Zygote 26: 33-39. https://doi.org/10.1017/S0967199417000685
Tatone, C., G. Di Emidio, M. Vento, R. Ciriminna, & P.G. Artini. 2010. Cryopreservation and oxidative stress in reproductive cells. Gynecol. Endocrinol. 26:563-567. https://doi.org/10.3109/09513591003686395
Telnoni, S.P., R. Iis Arifiantini, T.L. Yusuf, & S. Darwati. 2017. SK Kedu semen cryopreservation in beltsville poultry semen extender and lactated ringer’s-egg yolk extender using dimethyl sulfoxie. Asian J. Poult. Sci. 11: 14-19. https://doi.org/10.3923/ajpsaj.2017.14.19
Thelie, A., A. Bailliard, F. Seigneurin, T. Zerjal, M. Biochard, & E. Blesbois. 2019. Chicken semen cryopreservation and use for the restoration of rare genetic resources. Poult. Sci. 98:446-455. https://doi.org/10.3382/ps/pey360
Van Voorst, A. & F.R. Leenstra. 1995. Effect of dialysis before storage or cryopreservation on fertilizing ability of fowl semen. Poult. Sci. J. 74: 141-146. https://doi.org/10.3382/ps.0740141
Wang, X., X. Shi, Y. Liu, D. Yu, S. Guan, Q. Liu, & J. Li. 2016. Effects of chilled storage and cryopreservation on sperm characteristics, antioxidant enzyme activities, and lipid peroxidation in Pacific cod Gadus microcephalus. Chin. J. Oceanol. Limn. 34:763–771. https://doi.org/10.1007/s00343-016-5088-z
Wang, Y., R. Branicky, A. Noë, & S. Hekimi. 2018. Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. J. Cell. Biol. 217:1915-1928. https://doi.org/10.1083/jcb.201708007
Zakošek Pipan, M., J. Mrkun, M. Kosec, A. Nemec Svete, & P. Zrimšek. 2014. Superoxide dismutase: a predicting factor for boar semen characteristics for short-term preservation. Hindawi 2014:1-7. https://doi.org/10.1155/2014/105280
Zaniboni L., C. Cassinelli, M.G. Mangiagalli, T.M. Gliozzi, & S. Cerolini. 2014. Pellet cryopreservation for chicken semen: effects of sperm working concentration, cryoprotectant concentration and equilibration time during in vitro processing. Theriogenology 82:251-8. https://doi.org/10.1016/j.theriogenology.2014.04.007
Zawadzka J., E. Łukaszewicz, & A. Kowalczyk. 2015. Comparative semen analysis of two Polish duck strains from a conservation programme. Europ. Poult. Sci. 79.
Authors
AncueloA. E., LandichoM. M., DichosoG. A., & SangelP. (2021). Superoxide Dismutase (SOD) Activity in Cryopreserved Semen of Itik Pinas-Khaki (Anas platyrhynchos L.). Tropical Animal Science Journal, 44(2), 138-145. https://doi.org/10.5398/tasj.2021.44.2.138
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Authors submitting manuscripts should understand and agree that copyright of manuscripts of the article shall be assigned/transferred to Tropical Animal Science Journal. The statement to release the copyright to Tropical Animal Science Journal is stated in Form A. This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License (CC BY-SA) where Authors and Readers can copy and redistribute the material in any medium or format, as well as remix, transform, and build upon the material for any purpose, but they must give appropriate credit (cite to the article or content), provide a link to the license, and indicate if changes were made. If you remix, transform, or build upon the material, you must distribute your contributions under the same license as the original.
Article Details
