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Ram semen deterioration by short-term exposure to high altitude is prevented by improvement of antioxidant status

  • E. Cofré (a1), O. A. Peralta (a1), A. Raggi (a2) (a3), M. De los Reyes (a1), F. Sales (a4), A. González-Bulnes (a5) (a6) and V. H. Parraguez (a1) (a2) (a3)...


Ovine reproduction efficiency in herds at high altitude (ha) is lower than that at low altitude (la). In ewes, ha effects are due to hypoxia and oxidative stress. Our aim was to establish the effect of antioxidant vitamin supplementation on semen traits and antioxidant status of rams exposed to short or long time ha. A total of 32 rams native to la (~500 m) were used, 16 were kept at la and the other 16 were brought to ha (~3600 m), where they were placed in the same flock as the ha native rams (n=16). Half of the animals in each group were supplemented daily with vitamins C 600 mg and E 450 IU per os, during the entire experimental period, starting the 4th day after animal’s arrival at ha (day 0). At days 0, 30 and 60 of treatment, blood and semen samples were collected for evaluation of antioxidant status and semen standard characteristics. Data were compared within each experimental time by analysis of variance using a general linear model. Elevated concentrations of oxidative stress biomarkers were present in blood from animals maintained at ha. Ejaculates from ha exposed rams showed decreased sperm concentration, progressive motility and viability, in addition to decreased antioxidant status in seminal fluid. A total of 30 days of oral supplementation with vitamins C and E prevented some ha negative effects on semen characteristics, mainly in recently ha exposed rams. It is concluded that exposure of rams to ha negatively affects semen quality, where oxidative stress plays a predominant role. These effects are mainly prevented by oral supplementation of vitamins C and E, which constitutes a simple and cheap alternative to improve semen quality of rams when they are moved to ha.


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Agarwal, A and Allamaneni, SSR 2011. Free radicals and male reproduction. Journal of Indian Medical Association 109, 184187.
Agarwal, A and Sekhon, LH 2010. The role of antioxidant therapy in the treatment of male infertility. Human Fertility 13, 217225.
Aitken, RJ and Koppers, AJ 2011. Apoptosis and DNA damage in human spermatozoa. Asian Journal of Andrology 13, 642.
Bansal, AK and Bilaspuri, GS 2011. Impacts of oxidative stress and antioxidants on semen functions. Veterinary Medicine International 2011,
Barnholt, KE, Hoffman, AR, Rock, PB, Muza, SR, Fulco, CS, Braun, B, Holloway, L, Mazzeo, RS, Cymerman, A and Friedlander, AL 2006. Endocrine responses to acute and chronic high-altitude exposure (4,300 meters): modulating effects of caloric restriction. American Journal of Physiology Endocrinology and Metabolism 290, E1078E1088.
Basu, M, Pal, K, Prasad, R, Malhotra, AS, Rao, KS and Sawhney, RC 1997. Pituitary, gonadal and adrenal hormones after prolonged residence at extreme altitude in man. International Journal of Andrology 20, 153158.
Benedetti, S, Tagliamonte, MC, Catalani, S, Primiterra, M, Canestrari, F, De Stefanu, S, Palini, S and Bulleti, C 2012. Differences in blood and semen oxidative status in fertile and infertile men, and their relationship with sperm quality. Reproductive Biomedicine Online 25, 300306.
Benso, A, Broglio, F, Aimaretti, G, Lucatello, B, Lanfranco, F, Ghigo, E and Grottoli, S 2007. Endocrine and metabolic responses to extreme altitude and physical exercise in climbers. European Journal of Endocrinolgy 157, 733740.
Cofré, E, Peralta, O, Urquieta, B, Raggi, A, Benavides, N and Parraguez, VH 2016. Improvement of antioxidant status and semen quality by oral supplementation with vitamins C and E in rams. Revista Científica FCV-LUZ 26, 156163.
Donayre, J, Guerra-García, R, Moncloa, F and Sobrevilla, LA 1968. Endocrine studies at high altitude. Journal of Reproduction and Fertility 16, 5558.
Dosek, A, Ohno, H, Acs, Z, Taylor, AW and Radak, Z 2007. High altitude and oxidative stress. Respiration Physiology and Neurobiology 158, 128131.
Emmanverdi, M, Zhandi, M, Zareshahneh, A, Sharafi, M and Akabar-Sharif, A 2013. Optimization of ram semen cryopreservation using a chemically defined soybean lecithin-based extender. Reproduction in Domestic Animals 48, 899904.
Farías, JG, Bustos-Obregón, E, Tapia, PJ, Gutiérrez, E, Zepeda, A, Juantok, C, Cruz, G, Soto, G, Benites, J and Reyes, JG 2008. Time course of endocrine changes in the hypophysis-gonad axis induced by hypobaric hypoxia in male rats. Journal of Reproduction and Development 54, 1821.
Gonzales, G 2013. Serum testosterone levels and excessive erythrocytosis during the process of adaptation to high altitudes. Asian Journal of Andrology 15, 368374.
Gonzales, GF 2007. Peruvian contributions to the study on human reproduction at high altitude: From the chronicles of the Spanish conquest to the present. Respiration Physiology and Neurobiology 158, 172179.
Hess, RA and de Franca, LR 2008. Spermatogenesis and cycle of the seminiferous epithelium. In Advances in experimental medicine and biology, volume 636: Molecular mechanisms in spermatogenesis, (ed. CY Cheng), p 274. Landes Bioscience and Springer Science+Business Media, LLC, TX, USA.
Huddleston, B, Ataman, E, de Salvo, P, Zanetti, M, Bloise, M, Bel, J, Franceschini, G and Fèd´Ostiani, L 2003. Towards a GIS-based analysis of mountain environments and populations. In Environment and natural resources. Working paper no. 10. Food and Agriculture Organization of the United Nations, Rome, Italy. 26pp.
Jafaroghli, M, Abdi-Benemar, H, Zamiri, MJ, Khalili, B, Farshad, A and Shadparvar, AA 2014. Effects of dietary n-3 fatty acids and vitamin C on semen characteristics, lipid composition of sperm and blood metabolites in fat-tailed Moghani rams. Animal Reproduction Science 147, 1724.
Kasimanickam, R, Pelzer, KD, Kasimanickam, V, Swecker, WS and Tatcher, CD 2006. Association of classical semen parameters, sperm DNA fragmentation index, lipid peroxidation and antioxidant enzymatic activity of semen in ram-lambs. Theriogenology 65, 14071421.
Khosrowbeygi, A, Nosratollah, MS and Deldar, Y 2004. Correlation between sperm quality parameters and seminal plasma antioxidants status. Iranian Journal of Reproductive Medicine 2, 5864.
Majid, A, Qureshi, MS and Khan, RU 2014. In vivo adverse effects of alpha-tocopherol on the semen quality of male bucks. Journal of Animal Physiology and Animal Nutrition 99, 841846.
Marrocco, I, Altieri, F and Peluso, I 2017. Measurement and clinical significance of biomarkers of oxidative stress in humans. Oxidative Medicine and Cellular Longevity 2017,
Matthews, N, Bester, N and Schwalbach, LMJ 2003. A Comparison of ram semen collected by artificial vagina and electroejaculation. South African Journal of Animal Science 4, 2830.
Monge, C, San Martín, M, Atkins, J and Castañón, J 1945. Aclimatación del Ganado ovino en las grandes Alturas. Anales de la Facultad de Medicina 28, 1531.
NRC 2006. Nutrient requirements of small ruminants. National Academic Press, Washington, DC, USA.
Okumura, A, Fuse, H, Kawauchi, Y and Akashi, T 2003. Changes in male reproductive function after high altitude mountaineering. High Altitude Medicine and Biology 4, 349353.
Parraguez, VH, Díaz, F, Cofre, E, Urquieta, B, De Los Reyes, M, Astiz, S and González-Bulnes, A 2014. Fertility of a high-altitude sheep-model is compromised by deficiencies in both preovulatory follicle development and plasma LH availability. Reproduction in Domestic Animals 49, 977984.
Parraguez, VH, Atlagich, M, Araneda, O, García, C, Muñoz, A, De los Reyes, M and Urquieta, B 2011. Effects of antioxidant vitamins on newborn and placental traits in gestations at high altitude: comparative study in high and low altitude native sheep. Reproduction Fertility and Development 23, 285296.
Parraguez, VH, Atlagich, M, Behn, C, Bruzzone, ME and Raggi, LA 2006. Fertility in ewes at high altitude: comparison between animals with long- and short-time residence at high altitude and the effect of antioxidant vitamins. Reproduction in Domestic Animals 41, 372.
Parraguez, VH, Urquieta, B, Pérez, L, Castellaro, G, De Los Reyes, M, Torres-Rovira, L, Aguado-Martínez, A, Astiz, S and González-Bulnes, A 2013. Fertility in a high-altitude environment is compromised by luteal dysfunction: the relative roles of hypoxia and oxidative stress. Reproductive Biology and Endocrinology 11, 24.
Rekkas, C, Kokolis, N, Belibasaki, S, Tsantarliotou, M and Smokovitis, A 2000. Effect of a-tocopherol on plasma testosterone and plasminogen activator activity or inhibition in ram spermatozoa. Theriogenology 53, 751760.
Sharpe, RM 1994. Regulation of the spermatogenesis. In The physiology of reproduction, 2nd edition (ed. E Knobil and JD Neill), pp. 13431363. Raven Press Ltd, New York, NY.
Sinha, S, Singh, SN, Saha, M, Kain, TC and Tyagi, AK 2010. Antioxidant and oxidative stress responses of sojourners at high altitude in different climatic temperatures. International Journal of Biometeorology 54, 8592.
Walczak–Jedrzejowska, R, Wolski, JC and Slowikowska-Hilczer, J 2013. The role of oxidative stress and antioxidants in male fertility. Central European Journal of Urology 66, 6067.
Yue, D, Yan, L, Luo, H, Xu, X and Jin, X 2010. Effect of vitamin E supplementation on semen quality and the testicular cell membranal and mitochondrial antioxidant abilities in Aohanfine-wool sheep. Animal Reproduction Science 118, 217222.


Ram semen deterioration by short-term exposure to high altitude is prevented by improvement of antioxidant status

  • E. Cofré (a1), O. A. Peralta (a1), A. Raggi (a2) (a3), M. De los Reyes (a1), F. Sales (a4), A. González-Bulnes (a5) (a6) and V. H. Parraguez (a1) (a2) (a3)...


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