Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Polyunsaturated Fatty Acids in Male Ruminant Reproduction - A Review

  • Tran, Len Van (Southern Agricuture College) ;
  • Malla, Bilal Ahmad (Division of Dairy Cattle Nutrition, National Dairy Research Institute) ;
  • Kumar, Sachin (Division of Dairy Cattle Nutrition, National Dairy Research Institute) ;
  • Tyagi, Amrish Kumar (Division of Dairy Cattle Nutrition, National Dairy Research Institute)
  • Received : 2015.12.15
  • Accepted : 2016.02.29
  • Published : 2017.05.01
Download PDF
⟨ Previous Next ⟩

Abstract

Fatty acids such as n-3 and n-6 polyunsaturated fatty acids (PUFA) are critical nutrients, used to improve male reproductive performance through modification of fatty acid profile and maintenance of sperm membrane integrity, especially under cold shock or cryopreservation condition. Also, PUFA provide the precursors for prostaglandin synthesis and can modulate the expression patterns of many key enzymes involved in both prostaglandin and steroid metabolism. Many studies carried out on diets supplemented with PUFA have demonstrated their capability to sustain sperm motility, viability and fertility during chilling and freezing as well as improving testis development and spermatogenesis in a variety of livestock species. In addition to the type and quantity of dietary fatty acids, ways of addition of PUFA to diet or semen extender is very crucial as it has different effects on semen quality in male ruminants. Limitation of PUFA added to ruminant ration is due to biohydrogenation by rumen microorganisms, which causes conversion of unsaturated fatty acids to saturated fatty acids, leading to loss of PUFA quantity. Thus, many strategies for protecting PUFA from biohydrogenation in rumen have been developed over the years. This paper reviews four aspects of PUFA in light of previous research including rumen metabolism, biological roles, influence on reproduction, and strategies to use in male ruminants.

Keywords

References

  1. Santos JE, Bilby TR, Thatcher WW, Staples CR, Silvestre FT. Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod Domest Anim 2008;43:23-30. https://doi.org/10.1111/j.1439-0531.2008.01139.x
  2. Thatcher WW, Staples RC. Using fats and fatty acids to enhance reproductive performance. Proceedings of the 5th Mid-Atlantic Nutrition Conference. Timonium, MD: University of Maryland; 2007. p. 116-29.
  3. Poulos A, White IG. The phospholipid composition of human spermatozoa and seminal plasma. J Reprod Fertil 1973;35:265-72. https://doi.org/10.1530/jrf.0.0350265
  4. Poulos A, Darin Bennett A, White IG. The phospholipid bound fatty acids and aldehydes of mammalian spermatozoa. Comp Biochem Physiol B 1973;46:541-9. https://doi.org/10.1016/0305-0491(73)90094-1
  5. Jain YC, Anand SR. Fatty acids and fatty aldehydes of buffalo seminal plasma and sperm lipid. J Reprod Fertil 1976;47:261-7. https://doi.org/10.1530/jrf.0.0470261
  6. Kelso KA, Redpath A, Noble RC, Speake BK. Lipid and antioxidant changes in spermatozoa and seminal plasma throughout the reproductive period of bulls. J Reprod Fertil 1997;109:1-6. https://doi.org/10.1530/jrf.0.1090001
  7. Wathes DC, Abayasekara DRE, Aitken RJ. Polyunsaturated fatty acids in male and female reproduction. Biol Reprod 2007;77:190-201.
  8. Wassall SR, Stillwell W. Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes. Biochim Biophys Acta 2009;1788:24-32. https://doi.org/10.1016/j.bbamem.2008.10.011
  9. Stubbs CD, Smith AD. The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 1984;779:89-137. https://doi.org/10.1016/0304-4157(84)90005-4
  10. Hammerstedt RH, Graham JK, Nolan JP. Cryopreservation of mammalian sperm: what we ask them to survive. J Androl 1990;11:73-88.
  11. Robinson JJ, Ashworth CJ, Rooke JA, Mitchell LM, McEvoy TG. Nutrition and fertility in ruminant livestock. Anim Feed Sci Technol 2006;126:259-76. https://doi.org/10.1016/j.anifeedsci.2005.08.006
  12. Rooke JA, Shao CC, Speake BK. Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen. Reproduction 2001;121:315-22. https://doi.org/10.1530/rep.0.1210315
  13. Moallem U, Neta N, Zeron Y, Zachut M, Roth Z. Dietary a-linolenic acid from flaxseed oil or eicosapentaenoic and docosahexaenoic acids from fish oil differentially alter fatty acid composition and characteristics of fresh and frozen-thawed bull semen. Theriogenology 2015;83:1110-20. https://doi.org/10.1016/j.theriogenology.2014.12.008
  14. Khoshvaght A, Towhidi A, Zare-shahneh A, et al. Dietary n-3 PUFA improve fresh and post-thaw semen quality in Holstein bulls via alteration of sperm fatty acid composition. Theriogenology 2016;85:807-12. https://doi.org/10.1016/j.theriogenology.2015.10.023
  15. Adibromadi M, Najafi MH, Zeinoaldini S, Ganjkhanlou M, Yousefi AR. Effect of dietary soybean oil and fish oil supplementation on blood metabolites and testis development of male growing kids. Egypt J Sheep Goat Sci 2012;7:19-25. https://doi.org/10.12816/0005004
  16. Samadian F, Towhidi A, Rezayazdi K, Bahreini M. Effects of dietary n-3 fatty acids on characteristics and lipid composition of ovine sperm. Animal 2010;4:2017-22. https://doi.org/10.1017/S1751731110001308
  17. Jafaroghli M, Abdi-Benemar H, Zamiri MJ, Khalili B, Farshad A, Shadparvar AA. 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. Anim Reprod Sci 2014;147:17-24. https://doi.org/10.1016/j.anireprosci.2014.03.013
  18. Kiernan, M, Fahey AG, Fair S. The effect of the in vitro supplementation of exogenous long-chain fatty acids on bovine sperm cell function. Reprod Fertil Dev 2013;25:947-54. https://doi.org/10.1071/RD12204
  19. Towhidi A, Parks JE. Effect of n-3 fatty acids and ${\alpha}$-tocopherol on post-thaw parameters and fatty acid composition of bovine sperm. J Assist Reprod Genet 2012;29:1051-6. https://doi.org/10.1007/s10815-012-9834-7
  20. Abavisani A, Arshami J, Naserian AA, Kandelousi MAS, Azizzadeh M. Quality of bovine chilled or frozen-thawed semen after addition of omega-3 fatty acids supplementation to extender. Int J Fertil Steril 2013;7:161-8.
  21. Swain JE, Miller Jr RR. A postcryogenic comparison of membrane fatty acids of elephant spermatozoa. Zoo Biol 2000;19:461-73. https://doi.org/10.1002/1098-2361(2000)19:5<461::AID-ZOO13>3.0.CO;2-X
  22. Waterhouse KE, Hofmo PO, Tverdal A, Miller Jr RR. Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 2006;131:887-94. https://doi.org/10.1530/rep.1.01049
  23. White IG. Lipids and calcium uptake of sperm in relation to cold shock and preservation: A review. Reprod Fertil Dev 1993;5:639-58. https://doi.org/10.1071/RD9930639
  24. Neuringer M, Anderson GJ, Connor WE. The essentiality of n-3 fatty acids for the development and function of the retina and brain. Ann Rev Nutr 1988;8:517-41. https://doi.org/10.1146/annurev.nu.08.070188.002505
  25. Castellini C, Lattaioli P, Dal bosco A, Minelli A, Mugnai C. Oxidative Status and semen characteristics of rabbit buck as affected by dietary Vitamin E, C and n-3 fatty acids. Reprod Nutr Dev 2003;43:91-103. https://doi.org/10.1051/rnd:2003008
  26. Harfoot CG. Lipid metabolism in the rumen. Prog Lipid Res 1978;17:21-54. https://doi.org/10.1016/0079-6832(78)90004-6
  27. Palmquist DL, Jenkins TC. Fat in lactation rations: Review. J. Dairy Sci 1980;63:l-14.
  28. Davis CL. Fats in animal feeds. Sycamore, IL: Barnaby Inc.; 1990.
  29. Harfoot CG, Hazlewood GP. Lipid metabolism in the rumen. In: Hobson PN, editor. The rumen microbial ecosystem. NY, USA: Elsevier Appl. Sci. Publ. Co., Inc.; 1988. p. 285.
  30. Henderson C. The effects of fatty acids on pure cultures of rumen bacteria. J Agric Sci 1973;81:107-12. https://doi.org/10.1017/S0021859600058378
  31. Garton GA, Lough AK, Vioque E. Glyceride hydrolysis and glycerol fermentation by sheep rumen contents. J Gen Microbiol 1961;25:215-25. https://doi.org/10.1099/00221287-25-2-215
  32. Beam TM, Jenkins TC, Moate PJ, Kohn RA, Palmquist DL. Effects of amount and source of fat on the rates of lipolysis and biohydrogenation of fatty acids in ruminal contents. J Dairy Sci 2000;83:2564-73. https://doi.org/10.3168/jds.S0022-0302(00)75149-6
  33. Van Nevel CJ, Demeyer DI. Lipolysis and biohydrogenation of soybean oil in the rumen in vitro: Inhibition by antimicrobials. J Dairy Sci 1995;78:2797-806. https://doi.org/10.3168/jds.S0022-0302(95)76910-7
  34. Demeyer D, Doreau M. Targets and procedures for altering ruminant meat and milk lipids. Proc Nutr Soc 1999;58:593-607. https://doi.org/10.1017/S0029665199000786
  35. Harfoot CG, Hazlewood GP. Lipid metabolism in the rumen. In: Hobson PN, Stewart CS, editors. The rumen microbial ecosystem. London, UK: Chapman & Hall; 1997. p. 382-426.
  36. Harfoot CG, Noble RC, Moore JH. Factors influencing the extent of biohydrogenation of linoleic acid by rumen microorganisms in vitro. J Sci Food Agric 1973;24:961-70. https://doi.org/10.1002/jsfa.2740240814
  37. Doreau M, Ferlay A. Digestion and utilisation of fatty acids by ruminants. Anim Feed Sci Technol 1994;45:379-96. https://doi.org/10.1016/0377-8401(94)90039-6
  38. Noble RC. Lipid metabolism in the chick embryo: Some recent ideas. J Exp Zool 1987;1:65-73.
  39. Christie WWW. Gas chromatography; a practical guide. 1st edn, Ayr, Scotland: The Oily Press; 1989.
  40. Yeagle P. The lipids of cell membranes. In: The membranes of cells. London, UK: Academic Press; 1987. p. 22-39.
  41. Jones R, Mann T. Damage to ram spermatozoa by peroxidation of endogenous phospholipids. J Reprod Fertil 1977;50:261-8. https://doi.org/10.1530/jrf.0.0500261
  42. Alvarez JG, Storey BT. Spontaneous lipid peroxidation in rabbit epididymal spermatozoa: its effect on sperm motility. Biol Reprod 1982;27:1102-08. https://doi.org/10.1095/biolreprod27.5.1102
  43. McDonald P, Edwards RA, Greenhalgh JFD. Animal Nutrition. 4th edn. London, UK: Longman Ltd.; 1988. 34-45.
  44. Alberts B, Bray D, Lewis J, et al. The molecular organisation of cells: The plasma membrane; the lipid bilayer. In: Molecular biology of the cell. New York: Garland Publishing Incorporated; 1983. p. 256-64.
  45. Komarek RJ, Pickett BW, Gibson EW, Lanz RN. Composition of lipids in stallion semen. J Reprod Fertil 1965;10:337-42. https://doi.org/10.1530/jrf.0.0100337
  46. Scott TW. Lipid metabolism of spermatozoa. J Reprod Fertil 1973;18:65-76.
  47. Poulos A, Brown-Woodman PDC, White IG, Cox RI. Changes in phospholipids of ram spermatozoa during migration through the epididymis and possible origin of prostaglandin $F2{\alpha}$ in testicular and epididymal fluid. Biochim Biophys Acta 1975;388:12-8. https://doi.org/10.1016/0005-2760(75)90057-0
  48. Rana APS, Majumder GC, Misra S, Ghosh A. Lipid changes of goat sperm plasma membrane during epididymal maturation. Biochim Biophys Acta 1991;1061:185-96. https://doi.org/10.1016/0005-2736(91)90284-F
  49. Lenzi A, Picardo M, Gandini L, Dondero F. Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum Reprod 1996;2:246-56. https://doi.org/10.1093/humupd/2.3.246
  50. Scott TW, Dawson RM. Metabolism of phospholipids by spermatozoa and seminal plasma. Biochem J 1968;108:457-75. https://doi.org/10.1042/bj1080457
  51. Hartree EF, Mann T. Phospholipids in ram semen: metabolism of plasmalogen and fatty acids. Biochem J 1961;80:464-76. https://doi.org/10.1042/bj0800464
  52. Lardy HA, Phillips PH. The interrelation of oxidative and glycolytic processes as sources of energy for bull spermatozoa. Am J Physiol 1994;133:602-9.
  53. Dolatpanah MB, Towhidi A, Farshad A, Rashidi A, Rezayazdi A. Effects of dietary fish oil on semen quality of goats. Asian-Australas J Anim Sci 2008;21:29-34. https://doi.org/10.5713/ajas.2008.70035
  54. Cross NL. Decrease in order of human sperm lipids during capacitation. Biol Reprod 2003;69:529-34. https://doi.org/10.1095/biolreprod.102.013052
  55. Kadirvel G, Kumar S, Kumaresan A, Kathiravan P. Capacitation status of fresh and frozen-thawed buffalo spermatozoa in relation to cholesterol level, membrane fluidity and intracellular calcium. Anim Reprod Sci 2009;116:244-53. https://doi.org/10.1016/j.anireprosci.2009.02.003
  56. Manna PR, Dyson MT, Stocco DM. Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Mol Hum Reprod 2009;15:321-33. https://doi.org/10.1093/molehr/gap025
  57. Georgiadi A, Kersten S. Mechanisms of gene regulation by fatty acids. Adv Nutr 2012;3:127-34. https://doi.org/10.3945/an.111.001602
  58. Watanabe K. Prostaglandin F synthase. Prostaglandins Other Lipid Mediat 2002;401-07.
  59. Lands WE. Biochemistry and physiology of n-3 fatty acids. FASEB J 1992;6:2530-6. https://doi.org/10.1096/fasebj.6.8.1592205
  60. Mekonnen G, Boland M, Gordon I. The effect of prostaglandin on semen production and libido in the ram. Ir Vet J 1989;42:56-9.
  61. Shankar U, Benjamin BR, Agarwal SK. Effect of prostaglandin $F2{\alpha}$ ($PGF2{\alpha}$) on reaction time and semen characteristics of buffalo bulls. Ind J Anim Sci 1984;54:38-40.
  62. Titiroongruang J, Hirunpattarawong P, Sophonpattana P, Singlor J, Tummaruk P. Effects of prostaglandin $F2{\alpha}$ on serum testosterone and semen output in Holstein Friesian bulls in tropical climate. Thai J Vet Med Suppl 2011;41:159-60.
  63. Olfati A, Moghaddam GH, Daghigh Kia H, Karami Shabankareh H. Effects of prostaglandin $F2{\alpha}$ treatment on semen characteristics of crossbred rams in the non-breeding season. J Cell Anim Biol 2013;7:16-20. https://doi.org/10.5897/JCAB2013.0204
  64. Gustafsson BK, Graham EF, Crabo BG, Pavelko MK, Wagner WC. Pre-freeze supplementation of ram semen with PGE1 and PGF2 alpha: Effects on sperm vitality in vitro and on sperm transport in the ewe. In: Proceedings of the 10th Annual Meeting Society Study Reproduction; 1997. Abstract # 10.
  65. Ojeda S, Negro-Vilar A, McCann SM. Role of prostaglandins in the control of pituitary hormone secretion. Prog Clin Biol Res 1981;74:229-47.
  66. Jump DB, Clarke SD. Regulation of gene expression by dietary fat. Ann Rev Nutr 1999;19:63-90. https://doi.org/10.1146/annurev.nutr.19.1.63
  67. Saksena S, Hunt DM, Lau IF. Effects of prostaglandin $F2{\alpha}$ on sperm count, sperm motility and fertilizing capacity in the male rabbit. Int J androl 1999;1:639-48.
  68. Free MJ, Jaffe RA, Morford DE. Sperm transport through the rete testis in anesthetized rats: Role of the testicular capsule and effect of gonadotropins and prostaglandins. Biol Reprod 1980;22:1073-8. https://doi.org/10.1093/biolreprod/22.5.1073
  69. Surai PF, Noble RC, Sparks NH, Speake BK. Effect of long-term supplementation with arachidonic or docosahexaenoic acids on sperm production in the broiler chicken. J Reprod Fertil 2000;120:257-64.
  70. Esmaeili V, Shahverdi AH, Alizadeh AR, Alipour H, Chehrazi M. Saturated, omega-6 and omega-3 dietary fatty acid effects on the characteristics of fresh, frozen-thawed semen and blood parameters in rams. Andrologia 2014;46:42-9. https://doi.org/10.1111/and.12040
  71. Orth JM. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 1982;203:485-92. https://doi.org/10.1002/ar.1092030408
  72. Almiron I, Chemes H. Spermatogenic onset. II. FSH modulates mitotic activity of germ and Sertoli cells in immature rats. Int J Androl 1988;11:235-46. https://doi.org/10.1111/j.1365-2605.1988.tb00998.x
  73. Huhtaniemi IT, Warren DW, Catt KJ. Functional maturation of rat testis Leydig cells. Ann NY Acad Sci 1984;438:283-303. https://doi.org/10.1111/j.1749-6632.1984.tb38293.x
  74. Chandolia RK, Honaramooz A, Bartlewski PM, Beard AP, Rawlings NC. Effects of treatment with LH releasing hormone before the early increase in LH secretion on endocrine and reproductive development in bull calves. J Reprod Fertil 1997;111:41-50. https://doi.org/10.1530/jrf.0.1110041
  75. Bagu ET, Madgwick S, Duggavathia R, et al. Effects of treatment with LH or FSH from 4 to 8 weeks of age on the attainment of puberty in bull calves. Theriogenology 2004;62:861-73. https://doi.org/10.1016/j.theriogenology.2003.12.021
  76. Hoeflich A, Reichenbach HD, Schwartz J, et al. Insulin-like growth factors and IGF-binding proteins in bovine seminal plasma. Domest Anim Endocrinol 1999;17:39-51. https://doi.org/10.1016/S0739-7240(99)00023-5
  77. Selvaraju S, Reddy IJ, Nandi S, Rao SB, Ravindra JP. Influence of IGF-I on buffalo (Bubalus bubalis) spermatozoa motility, membrane integrity, lipid peroxidation and fructose uptake in vitro. Anim Reprod Sci 2009;113:60-70. https://doi.org/10.1016/j.anireprosci.2008.08.011
  78. Fair S, Doyle DN, Diskin MG, Hennessy AA, Kenny DA. The effect of dietary n-3 polyunsaturated fatty acids supplementation of rams on semen quality and subsequent quality of liquid stored semen. Theriogenology 2014;81:210-9. https://doi.org/10.1016/j.theriogenology.2013.09.002
  79. Robinson RS, Pushpakumara PG, Cheng Z, et al. Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 2002;124:119-31. https://doi.org/10.1530/rep.0.1240119
  80. Stratikopoulos E, Szabolcs M, Dragatsis I, Klinakis A, Efstratiadis A. The hormonal action of IGF1 in postnatal mouse growth. Proc Natl Acad Sci 2008;105:19378-83. https://doi.org/10.1073/pnas.0809223105
  81. Griffeth RJ, Bianda V, Nef S. The emerging role of insulin-like growth factors in testis development and function. Basic Clin Androl 2014;24:12. https://doi.org/10.1186/2051-4190-24-12
  82. Lejeune H, Chuzel F, Thomas T, et al. Paracrine regulation of Leydig cells. Ann Endocrinol (Paris) 1996;57:55-63.
  83. Henricks DM, Kouba AJ, Lackey BR, Boone WR, Gray SL. Identification of insulin-like growth factor I in bovine seminal plasma and its receptor on spermatozoa: influence on sperm motility. Biol Reprod 1998;59:330-7. https://doi.org/10.1095/biolreprod59.2.330
  84. Watson PE. Recent developments and concepts in the cryopreservation of spermatozoa and the assessment of their post-thawing function. Reprod Fertil Dev 1995;7:871-91. https://doi.org/10.1071/RD9950871
  85. Mandal R, Badyakar D, Chakrabarty J. Role of membrane lipid fatty acids in sperm cryopreservation. Adv Androl 2014;Article ID 190542.
  86. Kandelousi MAS, Arshami J, Naserian AA, Abavisan A. The effects of addition of omega-3, 6, 9 fatty acids on the quality of bovine chilled and frozen-thawed sperm. Open Vet J 2013;3:47-52.
  87. Kaka A, Wahid H, Rosnina N, et al. Alpha-linolenic acid supplementation in tris extender can improve frozen-thawed bull semen quality. Anim Reprod Sci 2015;153:1-7. https://doi.org/10.1016/j.anireprosci.2014.12.001
  88. Nasiri AH, Towhidi A, Zeinoaldini S. Combined effect of DHA and ${\alpha}$-tocopherol supplementation during bull semen cryopreservation on sperm characteristics and fatty acid composition. Andrologia 2012;44:550-5. https://doi.org/10.1111/j.1439-0272.2011.01225.x
  89. Towhidi A, Zeinoaldini S, Ardebili R, Davachi ND, Nasiri AH. Combined n-3 fatty acids and ${\alpha}$-tocopherol supplementation improved the ovine sperm cryosurvival. Iran J Biotechnol 2013;11:238-43. https://doi.org/10.5812/ijb.14469
  90. Aitken RJ, Harkiss D, Buckingham DW. Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol Reprod Dev 1993;35:302-15. https://doi.org/10.1002/mrd.1080350313
  91. Kothari S, Thompson A, Agarwal A, du Plessis SS. Free radicals: Their beneficial and detrimental effects on sperm function. Indian J Exp Biol 2010;48:425-35.
  92. Castellano CA, Audet I, Bailey JL, Laforest JP, Matte JJ. Dietary omega-3 fatty acids (fish oils) have limited effects on boar semen stored at $17^{\circ}C$ or cryopreserved. Theriogenology 2010;74:1482-90. https://doi.org/10.1016/j.theriogenology.2010.06.020
  93. Strzezek J, Lapkiewicz S, Lecewicz M. A note on antioxidant capacity of boar seminal plasma. Anim Sci Pep Rep 1999;17:181-8.
  94. Maldjian A, Pizzi F, Gliozzi T, et al. Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology 2005;63:411-21. https://doi.org/10.1016/j.theriogenology.2004.09.021
  95. Gulliver CE, Friend MA, King BJ, Clayton ET. The role of omega-3 polyunsaturated fatty acids in reproduction of sheep and cattle. Anim Reprod Sci 2012;131:9-22. https://doi.org/10.1016/j.anireprosci.2012.02.002
  96. De Graaf SP, Peake K, Maxwell WMC, O'Brien JK, Evans G. Influence of supplementing diet with oleic and linoleic acid on the freezing ability and sex-sorting parameters of ram semen. Livest Sci 2007;110:166-73. https://doi.org/10.1016/j.livsci.2006.11.001
  97. Alizadeh AR, Esmaeili V, Shahverdi A, Rashidi L. Dietary fish oil can change sperm parameters and fatty acid profiles of ram sperm during oil consumption period and after removal of oil source. Cell J 2014;16:289-98.
  98. Adeel M, Ijaz A, Aleem M, et al. Improvement of liquid and frozen-thawed semen quality of Nili-Ravi buffalo bulls (Bubalus bubalis) through supplementation of fat. Theriogenology 2009;71:1220-5. https://doi.org/10.1016/j.theriogenology.2009.01.008
  99. Gholami H, Chamani M, Towhidi A, Fazeli MH. Effect of feeding a docosahexaenoic acid-enriched nutriceutical on the quality of fresh and frozen-thawed semen in Holstein bulls. Theriogenology 2010;74:1548-58. https://doi.org/10.1016/j.theriogenology.2010.06.025
  100. Khan MIR, Ijaz A. Assessing undiluted, diluted and frozen-thawed Nili-Ravi buffalo bull sperm by using standard semen assays. Ital J Anim Sci 2007;6:784-7. https://doi.org/10.4081/ijas.2007.s2.784
  101. Milovanov VK, Golubj VS. Effect of special nutrition of rams on the lipid content of spermatozoa and on fertility results after insemination. Zhivotnovodstvo 1973;11:78-80.
  102. Calisici O. Investigation of antioxidative capacity in bovine seminal plasma-effects of omega-3 fatty acid. Hanover: Bibliothek der Tierarztlichen Hochschule hanover 2010;37-8.
  103. Lyberg AM, Fasoli E, Adlercreutz P. Monitoring the oxidation of docosahexaenoic acid in lipids. Lipids 2005;40:969-79. https://doi.org/10.1007/s11745-005-1458-1
  104. Gholami H, Chamani M, Towhidi A, Fazeli MH. Improvement of semen quality in holstein bulls during heat stress by dietary supplementation of omega-3 fatty acids. Int. J Fertil Steril 2011;4:160-7.
  105. Strzezek J, Fraser L, Kuklinska M, Dziekonska A. Effects of dietary supplementation with polyunsaturated fatty acids and antioxidants on biochemical characteristics of boar semen. Reprod Biol 2004;4:271-87.
  106. Aitken RJ. Reactive oxygen species and human sperm function. In: Bacetti B, editor. Comparative spermatology 20 years after. NY, USA: Raven Press; 1991. p. 787-92.
  107. Jahanian E, Nanaei HA, Kor NM. Influence of oxidative stress on sperm quality in animal. Int J Bio Sci 2014;4:10-6.
  108. De Lamirande E, Tsai C, Harakat A, Gagnon C. Involvement of reactive oxygen species in human sperm arcosome reaction induced by A23187, Iysophosphatidylcholine, and biological Fluid ultrafilttates. J Androl 1998;19:585-94.
  109. Goncalves FS, Barretto LSS, Arruda RP, Perri SHV, Mingoti GZ. Effect of antioxidants during bovine in vitro fertilization procedures on spermatozoa and embryo development. Reprod Domest Anim 2010;45:129-35. https://doi.org/10.1111/j.1439-0531.2008.01272.x
  110. Balercia G, Moretti S, Vignini A, et al. Role of nitric oxide concentrations on human sperm motility. J Androl 2004;25:245-9. https://doi.org/10.1002/j.1939-4640.2004.tb02784.x
  111. Donnelly ET, Lewis SE, Thompson W, Chakravarthy U. Sperm nitric oxide and motility: The effects of nitric oxide synthase stimulation and inhibition. Mol Hum Reprod 1997;3:755-62. https://doi.org/10.1093/molehr/3.9.755
  112. Kwon WS, Oh SA, Kim YJ, et al. Proteomic approaches for profiling negative fertility markers in inferior boar spermatozoa. Sci Rep 2015;5:13821. https://doi.org/10.1038/srep13821
  113. Kwon WS, Rahman MS, Ryu DY, Park YJ, Pang MG. Increased male fertility using fertility-related biomarkers. Sci Rep 2015;5:15654. https://doi.org/10.1038/srep15654
  114. Tavilani H, Goodarzi MT, Doosti M, et al. Relationship between seminal antioxidant enzymes and the phospholipid and fatty acid composition of spermatozoa. Reprod Biomed Online 2008;16:649-56. https://doi.org/10.1016/S1472-6483(10)60478-6
  115. Park YJ, Kwon WS, Oh SA, Pang MG. Fertility-related proteomic profiling bull spermatozoa separated by percoll. J Proteome Res 2012;11:4162-8. https://doi.org/10.1021/pr300248s
  116. Cocco T, Di Paola M, Papa S, Lorusso M. Chemical modification of the bovine mitochondrial bc1 complex reveals critical acidic residues involved in the proton pumping activity. Biochemistry 1998;37:2037-43. https://doi.org/10.1021/bi9724164
  117. Shibanuma M, Inoue A, Ushida K, et al. Importance of mitochondrial dysfunction in oxidative stress response: A comparative study of gene expression profiles. Free Radic Res 2011;45:672-880. https://doi.org/10.3109/10715762.2011.564169
  118. Aguilera-Aguirre, Bacsi LA, Saavedra-Molina A, et al. Mitochondrial dysfunction increases allergic airway inflammation. J Immunol 2009;183:5379-87. https://doi.org/10.4049/jimmunol.0900228
  119. Manjunath P, Therien I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 2002;53:109-19. https://doi.org/10.1016/S0165-0378(01)00098-5
  120. Doreau M, Chilliard Y. Digestion and metabolism of dietary fat in farm animals. Br J Nutr 1997;78:S15-S35. https://doi.org/10.1079/BJN19970132
  121. NRC (National Research Council). Nutrient requirements of dairy cattle. 7th edn. Washington, DC: National Academy of Sciences; 2001.
  122. Syadati SA, Aghsaghali AM, Fathi H, Davuodi J. Importance essential fatty acids (n-6 and n-3) in animal nutrition: I: Ruminant. Ann Biol Res 2012;3:1161-76.
  123. Ashes JR, Siebert BD, Gulati SK, Cuthbertson AZ, Scott TW. Incorporation of n-3 fatty acids of fish oil into tissue and serum lipids of ruminants. Lipids 1992;27:629-31. https://doi.org/10.1007/BF02536122
  124. Ashes JR, Gulati SK, Cook LJ, Scott TW, Donnelly JB. Assessing the biological effectiveness of protected lipid supplements for ruminants. J Am Oil Chem Soc 1979;56:552-7. https://doi.org/10.1007/BF02660231
  125. Putnam D, Garrett J, Kung L. Evaluation key to use of rumen-stable encapsulates. Feedstuffs 2003;75:10-2.
  126. Fotouhi N, Jenkins TC. Resistance of fatty acyl amides to degradation and hydrogenation by ruminal microorganisms. J Dairy Sci 1992;75:1527-32. https://doi.org/10.3168/jds.S0022-0302(92)77909-0
  127. Jenkins TC, Palmquist DL. Effect of fatty acids or calcium soaps on rumen and total nutrient digestibility of dairy rations. J Dairy Sci 1984;67:978-86. https://doi.org/10.3168/jds.S0022-0302(84)81396-X
  128. Sukhija PS, Palmquist DL. Dissociation of calcium soaps of longchain fatty-acids in rumen fluid. J Dairy Sci 1990;73:1784-7. https://doi.org/10.3168/jds.S0022-0302(90)78858-3
  129. Naik PK, Saijpaul S, Rani N. Evaluation of rumen protected fat prepared by fusion method. Anim Nutr Feed Technol 2007;7:95-101.
  130. Simopoulos AP. Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr 1991;54:438-63. https://doi.org/10.1093/ajcn/54.3.438
  131. Am-in N, Kirkwood RN, Techakumphu M, Tantasuparuk W. Lipid profiles of sperm and seminal plasma from boars having normal or low sperm motility. Theriogenology 2011;75:897-903. https://doi.org/10.1016/j.theriogenology.2010.10.032
  132. Liu Q, Zhou YF, Duan RJ, Wei HK, Jiang SW, Peng J. Effects of dietary n-6:n-3 fatty acid ratio and vitamin E on semen quality, fatty acid composition and antioxidant status in boars. Anim Reprod Sci 2015;162:11-9. https://doi.org/10.1016/j.anireprosci.2015.08.012
  133. Yan L, Bai X, Fang Z, et al. Effect of different dietary omega-3/omega-6 fatty acid ratios on reproduction in male rats. Lipids Heath Dis 2013;12:33. https://doi.org/10.1186/1476-511X-12-33
  134. Hazim J, Al-Daraji HA, Al-Mashadani WK, et al. Effect of n-3 and n-6 fatty acid supplemented diets on semen quality in Japanese quail (Coturnix coturnix japonica). Int J Poult Sci 2010;9:656-63. https://doi.org/10.3923/ijps.2010.656.663
  135. Grady ST, Cavinder CA, Brinsko SP, et al. Dietary supplementation of two varying sources of n-3 fatty acids and subsequent effects on fresh, cooled, and frozen seminal characteristics of stallions. Prof Anim Sci 2009;25:768-73.
  136. Al-Daraji HJ, Al-Mashadani HA, Al-Hayani WK, Al-Hassani AS, Mirza HA. Effect of n-3 and n-6 fatty acid supplemented diets on semen quality in Japanese quail (Coturnix coturnix japonica). Int J Poult Sci 2010;9:656-63. https://doi.org/10.3923/ijps.2010.656.663
  137. Woods VB, Fearon AM. Dietary sources of unsaturated fatty acids for animals and their transfer into meat, milk and eggs: A review. Livest Sci 2009;126:1-20. https://doi.org/10.1016/j.livsci.2009.07.002

Cited by

  1. Influence of omega-3 incorporation in sperm preservation medium on physical and kinematic properties of chilled and cryopreserved ram spermatozoa pp.09366768, 2018, https://doi.org/10.1111/rda.13289
  2. Effects of PUFAs on animal reproduction: male and female performances and endocrine mechanisms vol.17, pp.4, 2018, https://doi.org/10.1007/s11101-018-9559-z
  3. Effects of adding egg yolks of different avian species to Tris glycerol extender on the post-thawing quality of buck semen vol.195, pp.None, 2017, https://doi.org/10.1016/j.anireprosci.2018.06.016
  4. Sustainable Valorization of Halophytes from the Mediterranean Area: A Comprehensive Evaluation of Their Fatty Acid Profile and Implications for Human and Animal Nutrition vol.11, pp.8, 2017, https://doi.org/10.3390/su11082197
  5. Ram Semen Cryopreservation Using Egg Yolk or Egg Yolk-free Extenders: Preliminary Results vol.50, pp.2, 2017, https://doi.org/10.2478/sab-2019-0014
  6. Effect of Supplementation with Trimethylglycine (Betaine) and/or Vitamins on Semen Quality, Fertility, Antioxidant Status, DNA Repair and Welfare of Roosters Exposed to Chronic Heat Stress vol.9, pp.8, 2017, https://doi.org/10.3390/ani9080547
  7. Increased quality of in natura and cryopreserved semen of water buffaloes supplemented with saturated and unsaturated fatty acids from the palm oil industry vol.17, pp.4, 2017, https://doi.org/10.1590/1984-3143-ar2020-0522
  8. The effect of feed restriction on the fat profile of Santa Inês lamb meat vol.42, pp.None, 2017, https://doi.org/10.4025/actascianimsci.v42i1.48229
  9. Relevance of Fatty Acids to Sperm Maturation and Quality vol.2020, pp.None, 2020, https://doi.org/10.1155/2020/7038124
  10. Across‐breed validation study confirms and identifies new loci associated with sexual precocity in Brahman and Nellore cattle vol.137, pp.2, 2017, https://doi.org/10.1111/jbg.12429
  11. Effect of Soy Lecithin Supplementation in Beef Cows before Calving on Colostrum Composition and Serum Total Protein and Immunoglobulin G Concentrations in Calves vol.10, pp.5, 2017, https://doi.org/10.3390/ani10050765
  12. Gallic acid and omega‐3 fatty acids mitigate epididymal and testicular toxicity in manganese‐treated rats vol.52, pp.7, 2020, https://doi.org/10.1111/and.13630
  13. Effects of astaxanthin supplementation on the freezability, lipid peroxidation, antioxidant enzyme activities and post-thawing fertility of ram semen vol.192, pp.None, 2017, https://doi.org/10.1016/j.smallrumres.2020.106213
  14. Lipidomic markers of sperm cryotolerance in cattle vol.10, pp.1, 2017, https://doi.org/10.1038/s41598-020-77089-9
  15. Assessment of the toxicity effects of nicotine on sperm and IVF and the potential protective role of silymarin-an experimental study in mice vol.25, pp.1, 2017, https://doi.org/10.1186/s43043-020-00025-4
  16. Enhancement impact of Moringa oleifera leaves extract-base extender on cryopreservation and fertilization of Barki ram sperms: comparative study with vitamin E and selenium combination vol.20, pp.1, 2017, https://doi.org/10.1080/1828051x.2021.1953411
  17. Stimulation of follicle growth and development during estrus in Ettawa Grade does fed a flushing supplement of different polyunsaturated fatty acids vol.14, pp.1, 2021, https://doi.org/10.14202/vetworld.2021.11-22
  18. Role of Long Chain Fatty Acids in Developmental Programming in Ruminants vol.11, pp.3, 2021, https://doi.org/10.3390/ani11030762
  19. Effects of the Inclusion of Different Levels of Dietary Sunflower Hulls on the Colostrum Compositions of Ewes vol.11, pp.3, 2017, https://doi.org/10.3390/ani11030777
  20. Exogenous Factors Affecting the Functional Integrity of Male Reproduction vol.11, pp.3, 2021, https://doi.org/10.3390/life11030213
  21. Role of Antioxidants in Cooled Liquid Storage of Mammal Spermatozoa vol.10, pp.7, 2017, https://doi.org/10.3390/antiox10071096
  22. Role of peroxisome proliferator-activated receptor gamma (PPARγ) in the regulation of fatty acid metabolism related gene expressions in testis of men with impaired spermatogenesis vol.21, pp.4, 2021, https://doi.org/10.1016/j.repbio.2021.100543
  23. Flaxseed Oil as a Source of Omega n-3 Fatty Acids to Improve Semen Quality from Livestock Animals: A Review vol.11, pp.12, 2017, https://doi.org/10.3390/ani11123395