Abstract
This study determined the effects of antioxidant supplementation and storage time at cool temperatures on the characteristics of epididymal camel spermatozoa. Camel testes were collected at the abattoir after animal slaughtering and kept at 4 °C during transportation and until processing (max 6 h). Spermatozoa were retrieved and diluted with SHOTOR extender, split in aliquots, supplemented with the following antioxidants: 200 μm/mL vitamin E, 1.0 g/L vitamin C, 1 μg/mL selenium nanoparticles, 50 μg/mL zinc nanoparticles, 2 μg/mL sodium selenite, and 100 μg/mL zinc sulfate, and stored at 4 °C for 2, 48, 96, and 144 h. The storage time significantly affected (P < 0.05) the sperms’ motility and livability, the sperms’ membrane integrity, and the percentages of cytoplasmic droplets as well as the percentage of morphologically normal spermatozoa. Epididymal sperm characteristics (progressive motility, livability, membrane integrity, and abnormalities) were significantly improved (P < 0.05) when the spermatozoa were diluted with antioxidants as compared with the control group, and the best additives were identified as nano-selenium, sodium selenite, nano-zinc, and zinc sulfate. In conclusion, adding nano-sized minerals or inorganic trace elements and vitamins maintained the progressive motility, livability, and membrane integrity, and decreased abnormalities and cytoplasmic droplet percentages of epididymal camel spermatozoa stored at 4 °C up to 144 h.
Similar content being viewed by others
References
Abdelkhalek, A., Gabr, S.A., Khalil, W., Shamiah, S., Pan, L., Qin, G., and Farouk, M., 2017. In vitro production of Sudanese camel (Camelus dromedarius) embryos from epididymal spermatozoa and follicular oocytes of slaughtered animals, Polish Journal of Veterinary Sciences, 20, 95-101
Afifi, M., and Abdelazim, A.M., 2015. Ameliorative effect of zinc oxide and silver nanoparticles on antioxidant system in the brain of diabetic rats, Asian Pacific Journal of Tropical Biomedicine, 5, 874-877
Al-Bulushi, S., Manjunatha, B., Bathgate, R., Rickard, J., and de Graaf, S., 2019. Liquid storage of dromedary camel semen in different extenders, Animal Reproduction Science, 207, 95-106
Ali, A., Derar, D.R., Alhassun, T.M., and Almundarij, T.I., 2020. Effect of Zinc, Selenium, and Vitamin E Administration on Semen Quality and Fertility of Male Dromedary Camels with Impotentia Generandi, Biological Trace Element Research, 1-7
Amidi, F., Pazhohan, A., Nashtaei, M.S., Khodarahmian, M., and Nekoonam, S., 2016. The role of antioxidants in sperm freezing: a review, Cell and tissue banking, 17, 745-756
Badr, M., and Abdel-Malak, M.G., 2010. In vitro fertilization and embryo production in dromedary camel using epididymal spermatozoa, Global Veterinaria, 4, 271-276
Bansal, A.K., and Bilaspuri, G.S., 2009. Antioxidant effect of vitamin E on motility, viability and lipid peroxidation of cattle spermatozoa under oxidative stress, Animal Science Papers and Reports, 27, 5-14
Bansal, A.K., and Bilaspuri, G.S., 2011. Impacts of oxidative stress and antioxidants on semen functions, Veterinary Medicine International, 2011, 1-7
Barkhordari, A., Hekmatimoghaddam, S., Jebali, A., Khalili, M.A., Talebi, A., and Noorani, M., 2013. Effect of zinc oxide nanoparticles on viability of human spermatozoa, Iranian Journal of Reproductive Medicine, 11, 767-771
Cholakkal, I.K., Koroth, A., and Sharifi, S.A., 2016. Observations on semen collection and suitability of different modifications of artificial vagina for dromedary camels (Camelus dromedarius), Journal of Camel Practice and Research, 23, 169-174
Dawson, E.B., Harris, W.A., Teter, M.C., and Powell, L.C., 1992. Effect of ascorbic acid supplementation on the sperm quality of smokers, Fertility and Sterility, 58, 1034-1039
Dorostkar, K., Alavi-Shoushtari, S.M., and Mokarizadeh, A., 2012. Effects of in vitro selenium addition to the semen extender on the spermatozoa characteristics before and after freezing in water buffaloes (Bubalus bubalis), Veterinary Research Forum, 3, 263–268
Duncan, B.D., 1955. Multiple range and multiple F-test. Biometrics, 11, 1-42
El-Harairy, M.A., Abd El-Razek, I.M., Abdel-Khalek, A.E., Shamiah, S.M., Zaghloul, H.K., and Khalil, W.A., 2016. Effect of antioxidants on the stored dromedary camel epididymal sperm characteristics, Asian Journal of Animal Sciences, 10, 147-153
Elwishy, A., 1988. Reproduction in the male dromedary (Camelus dromedarius): a review, Animal Reproduction Science, 17, 217-241
Eskiocak, S., Gozen, A.S., Yapar, S.B., Tavas, F., Kilic, A.S., and Eskiocak, M., 2005. Glutathione and free sulphydryl content of seminal plasma in healthy medical students during and after exam stress, Human Reproduction, 20, 2595-2600
Foote, R.H., Brockett, C.C., and Kaproth, M.T., 2002. Motility and fertility of bull sperm in whole milk extender containing antioxidants, Animal Reproduction Science, 71, 13-23
Hafez, E., and Hafez, B., 2001. Reproductive parameters of male dromedary and bactrian camels, Archives of Andrology, 46, 85-98
Handy, R.D., Owen, R., and Valsami-Jones, E., 2008. The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs, Ecotoxicology, 17, 315-325
Jeong, Y.-J., Kim, M.-K., Song, H.-J., Kang, E.-J., Ock, S.-A., Kumar, B.M., Balasubramanian, S., and Rho, G.-J., 2009. Effect of α-tocopherol supplementation during boar semen cryopreservation on sperm characteristics and expression of apoptosis related genes, Cryobiology, 58, 181-189
Kadim, I.T., Mahgoub, O., and Purchas, R.W., 2008. A review of the growth, and of the carcass and meat quality characteristics of the one-humped camel (Camelus dromedaries), Meat Science, 80, 555-569
Khalil, W., El-Harairy, M., Zeidan, A., and Hassan, M., 2019. Impact of selenium nano-particles in semen extender on bull sperm quality after cryopreservation, Theriogenology, 126, 121-127
Khalil, W.A., Abdel-Khalek, A.-K.E., Falchi, L., El-Saidy, B.E., and Yousif, A.I., 2020. Effects of extender and packaging method on morphological and functional characteristics of cryopreserved Ossimi ram semen, Asian Pacific Journal of Reproduction, 9, 148-155
Kilian, I., Lubbe, K., Bartels, P., Friedmann, Y., and Denniston, R.S., 2000. Evaluating epididymal sperm of African wild ruminants: longevity when stored at 4 °C and viability following cryopreservation, Theriogenology, 53, 336
Kotdawala, A.P., Kumar, S., Salian, S.R., Thankachan, P., Govindraj, K., Kumar, P., Kalthur, G., and Adiga, S.K., 2012. Addition of zinc to human ejaculate prior to cryopreservation prevents freeze-thaw-induced DNA damage and preserves sperm function, Journal of Assisted Reproduction and Genetics, 29, 1447-1453
Kumar, N., Verma, R.P., Singh, L.P., Varshney, V.P., and Dass, R.S., 2006. Effect of different levels and sources of zinc supplementation on quantitative and qualitative semen attributes and serum testosterone level in crossbred cattle (Bos indicus x Bos taurus) bulls, Reproduction Nutrition Development, 46, 663-675
Marin-Guzman, J., Mahan, D.C., and Whitmoyer, R., 2000. Effect of dietary selenium and vitamin E on the ultrastructure and ATP concentration of boar spermatozoa, and the efficacy of added sodium selenite in extended semen on sperm motility, Journal of Animal Science, 78, 1544-1550
Menon, A.G., Thundathil, J.C., Wilde, R., Kastelic, J.P., and Barkema, H.W., 2011. Validating the assessment of bull sperm morphology by veterinary practitioners, The Canadian Veterinary Journal, 52, 407-408
Mir, S.S., Lone, F.A., Khan, M.Z., Malik, A.A., Islam, R., and Sofi, K.A., 2012. Effect of cold storage period on the quality of ram cauda epididymal spermatozoa recovered postmortem, Turkish Journal of Veterinary and Animal Sciences, 36, 683-687
Monaco, D., and Lacalandra, G., 2020. Considerations for the development of a dromedary camel (Camelus dromedarius) semen collection centre, Animal Reproduction Science, 212, 1-10
Morton, K., Billah, M., and Skidmore, J., 2013. Effect of sperm diluent and dose on the pregnancy rate in dromedary camels after artificial insemination with fresh and liquid-stored semen, Journal of Camelid Science, 6, 49-62
Moskovtsev, S.I., and Librach, C.L., 2013. Methods of sperm vitality assessment. Spermatogenesis, 2013, Springer, 13-19
Niasari-Naslaji, A., Mosaferi, S., Bahmani, N., Gharahdaghi, A.A., Abarghani, A., Ghanbari, A., and Gerami, A., 2006. Effectiveness of a tris-based extender (SHOTOR diluent) for the preservation of Bactrian camel (Camelus bactrianus) semen, Cryobiology, 53, 12-21
Niki, E., 2014. Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence, Free Radical Biology and Medicine, 66, 3-12
Panahi, F., Niasari-Naslaji, A., Seyedasgari, F., Ararooti, T., Razavi, K., and Moosavi-Movaheddi, A.A., 2017. Supplementation of tris-based extender with plasma egg yolk of six avian species and camel skim milk for chilled preservation of dromedary camel semen, Animal Reproduction Science, 184, 11-19
Prasad, A.S., Bao, B., Beck, F.W.J., Kucuk, O., and Sarkar, F.H., 2004. Antioxidant effect of zinc in humans, Free Radical Biology and Medicine, 37, 1182-1190
Pukazhenthi, B., Pelican, K., Wildt, D., and Howard, J., 1999. Sensitivity of domestic cat (Felis catus) sperm from normospermic versus teratospermic donors to cold-induced acrosomal damage, Biology of Reproduction, 61, 135-141
Saadeldin, I.M., Moulavi, F., Swelum, A.A.-A., Khorshid, S.S., Hamid, H.-F., and Hosseini, S.M., 2020. Vitrification of camel oocytes transiently impacts mitochondrial functions without affecting the developmental potential after intracytoplasmic sperm injection and parthenogenetic activation, Environmental Science and Pollution Research, 27, 44604-44613
Sánchez-Gutiérrez, M., García-Montalvo, E.A., Izquierdo-Vega, J.A., and Del Razo, L.M., 2007. Effect of dietary selenium deficiency on the in vitro fertilizing ability of mice spermatozoa. Proceedings of the VIIIth Conference of the International Society for Trace Element Research in Humans (ISTERH), the IXth Conference of the Nordic Trace Element Society (NTES), and the VIth Conference of the Hellenic Trace Element Society (HTES), 2007, Springer, 41-49
SAS, 2007. Statistical analysis System. Stat-user’s guid. Release 9.1.3. SAS Institute. Cary, NC, USA
Saurabh, S.S., Sharma, P., and Gautam, V., 2018. Effect of ascorbic acid on preservability of spermatozoa of buffalo bull after storage of epididymis at temperature 4 °C and -196 °C, Journal of Entomology and Zoology Studies, 6, 1065-1070
Scholkamy, T., El-Badry, D., and Mahmoud, K.G.M., 2016. Developmental competence of Dromedary camel oocytes fertilized in vitro by frozen-thawed ejaculated and epididymal spermatozoa, Iranian Journal of Veterinary Research, 17, 253-258
Shahin, M.A., Khalil, W.A., Saadeldin, I.M., Swelum, A.A.-A., and El-Harairy, M.A., 2020. Comparison between the effects of adding vitamins, trace elements, and nanoparticles to shotor extender on the cryopreservation of dromedary camel epididymal spermatozoa, Animals, 10, 1-16
Sikka, S.C., 2004. Role of oxidative stress and antioxidants in andrology and assisted reproductive technology, Journal of andrology, 25, 5-18
Skidmore, J., Morton, K., and Billah, M., 2013. Artificial insemination in dromedary camels, Animal Reproduction Science, 136, 178-186
Storey, B.T., 1997. Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa, Molecular Human Reproduction, 3, 203-213
Swelum, A.A., Saadeldin, I.M., Ba-Awadh, H., Alowaimer, A.N. 2018a. Effects ofmelatonin implants on the reproductive performance and endocrine function of camel (Camelus dromedarius) bulls during the non-breeding and subsequent breeding seasons. Theriogenology 119, 18–27.
Swelum, A.A., Saadeldin, I.M., Ba-Awadh, H., Alowaimer, A.N. 2018b. Shortened daily photoperiod during the non-breeding season can improve the reproductive performance of camel bulls (Camelus dromedarius). Animal Reproduction Science 195, 334–344.
Swelum, A.A., Saadeldin, I.M., Ba-Awadh, H., Al-Mutary, M., Alowaimer, A.N. 2019a. Effect of short artificial lighting and low temperature in housing rooms during non-rutting season on reproductive parameters of male dromedary camels. Theriogenology 131, 133–139.
Swelum, A.A., Saadeldin, I.M., Ba-Awadh, H., Al-Mutary, M.G., Moumen, A.F., Alowaimer, A.N., Abdalla, H. 2019b. Efficiency of Commercial Egg Yolk-Free and Egg Yolk-Supplemented Tris-Based Extenders for Dromedary Camel Semen Cryopreservation. Animals 9, 999.
Tatone, C., Di Emidio, G., Vento, M., Ciriminna, R., and Artini, P.G., 2010. Cryopreservation and oxidative stress in reproductive cells, Gynecological Endocrinology, 26, 563-567
Taylor, K., Roberts, P., Sanders, K., and Burton, P., 2009. Effect of antioxidant supplementation of cryopreservation medium on post-thaw integrity of human spermatozoa, Reproductive Biomedicine Online, 18, 184-189
Ursini, F., Heim, S., Kiess, M., Maiorino, M., Roveri, A., Wissing, J., and Flohé, L., 1999. Dual function of the selenoprotein PHGPx during sperm maturation, Science, 285, 1393-1396
Waheed, M.M., Al-Eknah, M.M., and El-Bahr, S.M., 2011. Some biochemical characteristics and preservation of epididymal camel spermatozoa (Camelus dromedarius), Theriogenology, 76, 1126-1133
Waheed, M.M., Meligy, A.M., and Dhalam, S.A., 2018. The relationship between seminal plasma and serum trace elements and semen parameters of dromedary camels (Camelus dromedarius), Reproduction in Domestic Animals, 53, 1367-1374
Wani, N., 2009. In vitro embryo production in camel (Camelus dromedarius) from in vitro matured oocytes fertilized with epididymal spermatozoa stored at 4 °C, Animal Reproduction Science, 111, 69-79
Wani, N.A., and Hong, S., 2018. Intracytoplasmic sperm injection (ICSI) of in vitro matured oocytes with stored epididymal spermatozoa in camel (Camelus dromedarius): Effect of exogenous activation on in vitro embryo development, Theriogenology, 113, 44-49
Zhu, Z., Fan, X., Lv, Y., Zhang, N., Fan, C., Zhang, P., and Zeng, W., 2015. Vitamin E analogue improves rabbit sperm quality during the process of cryopreservation through its antioxidative action, PloS one, 10, 1-16
Funding
The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through research group no. (RG-1438-018).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article belongs to the Topical Collection: Camelids
Guest Editor: Bernard Faye
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shahin, M.A., Khalil, W.A., Saadeldin, I.M. et al. Effects of vitamin C, vitamin E, selenium, zinc, or their nanoparticles on camel epididymal spermatozoa stored at 4 °C. Trop Anim Health Prod 53, 86 (2021). https://doi.org/10.1007/s11250-020-02521-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-020-02521-1