Increased quality of in natura and cryopreserved semen of water buffaloes supplemented with saturated and unsaturated fatty acids from the palm oil industry
Lílian Kátia Ximenes Silva; José de Brito Lourenço Júnior; Aluizio Otavio Almeida da Silva; José Silva de Sousa; André Guimarães Maciel e Silva; Adriana Novaes dos Reis; Moysés dos Santos Miranda; Simone do Socorro Damasceno Santos; Otávio Mitio Ohashi; Lucieta Guerreiro Martorano; Geraldo Narciso da Rocha Filho; Cristian Faturi; Eziquiel de Morais; Érica Karine Lourenço Mares; Alexandre Rossetto Garcia
Abstract
Keywords
References
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Z (Berl). 2013;22(6):711-28.
Andrabi SMH. Factors affecting the quality of cryopreserved buffalo (
Argov N, Sklan D, Zeron Y, Roth Z. Association between seasonal changes in fatty-acid composition, expression of VLDL receptor and bovine sperm quality. Theriogenology. 2007;67(4):878-85.
Barth AD, Brito LF, Kastelic JP. The effect of nutrition on sexual development of bulls. Theriogenology. 2008;70(3):485-94.
Berchielli TT, Messana JD, Canesin RC. Produção de metano entérico em pastagens tropicais. Rev Bras Saúde Prod Anim. 2012;13(4):954-68.
Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):911-7.
Blom E. The ultrastructure of some characteristic sperm defects and a proposal for a new classification of the bull spermiogram. Nord Vet Med. 1973;25(7):383-91. PMid:4768226.
Bongalhardo DC, Leeson S, Buhr MM. Dietary lipids differentially affect membranes from different areas of rooster sperm. Poult Sci. 2009;88(5):1060-9.
Calder PC. Mechanisms of action of (n-3) fatty acids. J Nutr. 2012;142(3):592S-9S.
Castro LS, Hamilton TR, Mendes CM, Nichi M, Barnabe VH, Visintin JA, Assumpção ME. Sperm cryodamage occurs after rapid freezing phase: flow cytometry approach and antioxidant enzymes activity at different stages of cryopreservation. J Anim Sci Biotechnol. 2016;5:7-17.
Celeghini EC, de Arruda RP, de Andrade AF, Nascimento J, Raphael CF, Rodrigues PH. Effects that bovine sperm cryopreservation using two different extenders has on sperm membranes and chromatin. Anim Reprod Sci. 2008;104(2-4):119-31.
Celeghini ECC, de Arruda RP, de Andrade AFC, Nascimento J, Raphael CF. Practical techniques for bovine sperm simultaneous fluorimetric assessment of plasma, acrosomal and mitochondrial membranes. Reprod Domest Anim. 2007;42(5):479-88.
Celeghini ECC, Nascimento J, Raphael CF, Andrade AFC, Arruda RP. Simultaneous assessment of plasmatic, acrosomal, and mitochondrial membranes in ram sperm by fluorescent probes. Arq Bras Med Vet Zoot. 2010;62:536-43.
Cerolini S, Zaniboni L, Maldjian A, Gliozzi T. Effect of docosahexaenoic acid and α-tocopherol enrichment in chicken sperm on semen quality, sperm lipid composition and susceptibility to peroxidation. Theriogenology. 2006;66(4):877-86.
Colégio Brasileiro de Reprodução Animal – CBRA. (2013). Manual para exame andrológico e avaliação de sêmen animal. 3. ed. Belo Horizonte: CBRA. 104 p.
Costa QPB, Wechsler FS, Costa DPB, Polizel A No, Roça RO, Brito TP. Desempenho e características da carcaça de bovinos alimentados com dietas com caroço de algodão. Arq Bras Med Vet Zootec. 2011;63(3):729-35.
Durairajanayagam D, Singh D, Agarwal A, Henkel R. Causes and consequences of sperm mitochondrial dysfunction. Andrologia. 2020;8:e13666.
Ejaz R, Ansari MS, Rakha BA, Qadeer S, Husna AU, Akhter S. Evaluation of a-linolenic acid for freezability and in vivo fertility of Nili Ravi (
Ejaz R, Ansari MS, Rakha BA, Ullah N, Husna AU, Iqbal R, Akhter S. Arachidic acid in extender improves post-thaw parameters of cryopreserved Nili-Ravi buffalo bull semen. Reprod Domest Anim. 2014;49(1):122-5.
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(1):42-9.
Fan YY, McMurray DN, Ly LH, Chapkin RS. Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts. J Nutr. 2003;133(6):1913-20.
Flesch FM, Gadella BM. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim Biophys Acta. 2000;1469(3):197-235.
Furland NE, Oresti GM, Antollini SS, Venturino A, Maldonado EN, Aveldano MI. Very long-chain polyunsaturated fatty acids are the major acyl groups of sphingomyelins and ceramides in the head of mammalian spermatozoa. J Biol Chem. 2007;282(25):18151-61.
Garcia AR. Influência de fatores ambientais sobre as características reprodutivas de búfalos do rio (
Gonçalves AA, Garcia AR, Arruda RP, Barioni W Jr, Lourenço JB Jr, Kahwage PR, Silva GR. A suplementação alimentar com ácidos graxos insaturados melhora a qualidade do sêmen criopreservado de búfalos (
Grupo Agropalma. Óleo de palma bruto e ácido graxo de palma. Ficha técnica de produto. Folha 1/1. Limeira: Grupo Agropalma; 2010.
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(1-2):9-22.
Gürler H, Calisici O, Calisici D, Bollwein H. Effects of feeding omega-3-fatty acids on fatty acid composition and quality of bovine sperm and on antioxidative capacity of bovine seminal plasma. Anim Reprod Sci. 2015;160:97-104.
Hammerstedt RH. Maintenance of bioenergetic balance in sperm and prevention of lipid peroxidation: a review of the effect on design of storage preservation systems. Reprod Fertil Dev. 1993;5(6):675-90.
Iqbal M, Aleem M, Ijaz A, Rehman H, Yousaf MS. Assessment of buffalo semen with the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide reduction assay. J Anim Sci. 2010;88(3):922-5.
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(1-2):17-24.
Jain YC, Anand SR. Fatty acids and fatty aldehydes of buffalo seminal plasma and sperm lipid. J Reprod Fertil. 1976;47(2):261-7.
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):1-6.
Khoshniat MT, Towhidi A, Rezayazdi K, Zhandi M, Rostami F, Dadashpour Davachi N, Khalooee F, Kastelic J. Dietary omega-3 fatty acids from linseed oil improve quality of post-thaw but not fresh sperm in Holstein bulls. Cryobiology. 2020;93:102-8.
Khoshvaght A, Towhidi A, Zare-Shahneh A, Noruozi M, Zhandi M, Dadashpour Davachi N, Karimi R. Dietary n-3 PUFAs improve fresh and post-thaw semen quality in Holstein bulls via alteration of sperm fatty acid composition. Theriogenology. 2016;85(5):807-12.
Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, National Centre for the Replacement, Refinement and Reduction of Amimals in Research. Animal research: reporting in vivo experiments--the ARRIVE guidelines. J Cereb Blood Flow Metab. 2011;31(4):991-3.
Kumar D, Kumar P, Singh P, Yadav SP, Sarkar SK, Bharadwaj A, Yadav PS. Characteristics of frozen-thawed semen in predict-ing the fertility of buffalo bulls. Indian J Anim Sci. 2014;84:389-92.
Lee SH, Kim YJ, Ho Kang B, Park CK. Effect of nicotinic acid on the plasma membrane function and polyunsaturated fatty acids composition during cryopreservation in boar sperm. Reprod Domest Anim. 2019;54(9):1251-7.
Lenzi A, Gandini L, Picardo M, Tramer F, Sandri G, Panfili E. Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible scavenger therapies. Front Biosci. 2000;5:E1-15.
Longobardi V, Zullo G, Salzano A, De Canditiis C, Cammarano A, De Luise L, Puzio MV, Neglia G, Gasparrini B. Resveratrol prevents capacitation-like changes and improves in vitro fertilizing capability of buffalo frozen-thawed sperm. Theriogenology. 2017;88:1-8.
Maldjian A, Pizzi F, Gliozzi T, Cerolini S, Penny P, Noble R. Changes in sperm quality and lipid composition during cryopreservation of boar semen. Theriogenology. 2005;63(2):411-21.
Mandal DK, Nagpaul PK, Gupta AK. Motion characteristics of Murrah buffalo bull spermatozoa in various seasons and its relationship with functional integrity of the plasmallema. Theriogenology. 2003;60(2):349-58.
Melville DF, Johnston SD, Miller RR Jr. Flying-fox (
Minervini F, Guastamacchia R, Pizzi F, Dell’Aquila ME, Barile VL. Assessment of different functional parameters of frozen–thawed buffalo spermatozoa by using cytofluorimetric determinations. Reprod Domest Anim. 2013;48(2):317-24.
Mitre R, Cheminade C, Allaume P, Legrand P, Legrand AB. Oral intake of shark liver oil modifies lipid composition and improves motility and velocity of boar sperm. Theriogenology. 2004;62(8):1557-66.
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(7):1110-20.
Monteiro JP, Morais CM, Oliveira PJ, Jurado AS. Mitochondrial membrane lipids in life and death and their molecular modulation by diet: tuning the furnace. Curr Drug Targets. 2014;15(8):797-810.
Monteiro JP, Pereira CV, Silva AM, Maciel E, Baldeiras I, Peixoto F, Domingues MR, Jurado AS, Oliveira PJ. Rapeseed oil-rich diet alters hepatic mitochondrial membrane lipid composition and disrupts bioenergetics. Arch Toxicol. 2013;87(12):2151-63.
Mourvaki E, Cardinali R, Dal Bosco A, Corazzi L, Castellini C. Effects of flaxseed dietary supplementation on sperm quality and on lipid composition of sperm subfractions and prostatic granules in rabbit. Theriogenology. 2010;73(5):629-37.
Nasrallah F, Taieb SH, Sethoum MM, Omar S, Aribia HB, Sanhaji H, Feki M. Altered semen quality is associated with decreased semen docosahexaenoic acid and increased oleic acid levels. Clin Lab. 2020;66(1).
Neill AR, Masters CJ. Incorporation of (U-14C)palmitic acid into the phospholipids of bovine semen. J Reprod Fertil. 1971;24(2):295-7.
Osman C, Voelker DR, Langer T. Making heads or tails of phospholipids in mitochondria. J Cell Biol. 2011;192(1):7-16.
Pegg DE. The history and principles of cryopreservation. Semin Reprod Med. 2002;20(1):5-13.
Perini JAL, Stevanato FB, Sargi SC, Visentainer JEL, Dalalio MMO, Matshushita M, Souza NE, Visentainer JV. Ácidos graxos poli-insaturados n-3 e n-6: metabolismo em mamíferos e resposta imune. Rev Nutr. 2010;23(6):1075-86.
Pustowka C, McNiven MA, Richardson GF, Lall SP. Source of dietary lipid affects sperm plasma membrane integrity and fertility in rainbow trout
Rodrigues AMC, Darnet S, Silva LHM. Fatty acid profiles and tocopherol contents of buriti (
Roqueta-Rivera M, Stroud CK, Haschek WM, Akare SJ, Segre M, Brush RS, Agbaga MP, Anderson RE, Hess RA, Nakamura MT. Docosahexaenoic acid supplementation fully restores fertility and spermatogenesis in male delta-6 desaturase-null mice. J Lipid Res. 2010;51(2):360-7.
Safarinejad MR, Hosseini SY, Dadkhah F, Asgari MA. Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin Nutr. 2010;29(1):100-5.
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(12):2017-22.
Santana PP, da Silva BB, Silva TV, Costa NN, Cordeiro MS, Santos SS, Ohashi OM, Miranda MS. Addition of L-arginine to the fertilization medium enhances subsequent bovine embryo development rates. Theriogenology. 2016;85(6):1132-8.
Santos AX, Kahwage PR, Faturi C, Lourenço JB Jr, Alvarez WFM, Garcia AR. Efecto de la suplementación alimenticia con fuentes lipídicas sobre la ganancia de peso y niveles de testosterona sérica en toros bufalinos. J Vet Androl. 2017;2:52-9.
Santos AX, Kahwage PR, Faturi C, Quinzeiro Neto T, Lourenço JB Jr, Joele MRSP, Garcia AR. Feed supplementation with palm kernel cake-based concentrate increases the quality of water buffalo semen. Anim Reprod. 2014;11:85-95.
Schenkel LC, Bakovic M. Formation and regulation of mitochondrial membranes. Int J Cell Biol. 2014;2014:709828.
Sesso A, Belizário JE, Marques MM, Higuchi ML, Schumacher RI, Colquhoun A, Ito E, Kawakami J. Mitochondrial swelling and incipient outer membrane rupture in preapoptotic and apoptotic cells. Anat Rec (Hoboken). 2012;295(10):1647-59.
Silva AR, Fontenele-Neto JD, Cardoso RCS, Silva LDM, Chiniréa VH, Lopes MD. Description of ultrastructural damages in frozen-thawed canine spermatozoa. Cienc Anim Bras. 2009;10:595-601.
Silva GR, Garcia AR, Faturi C, Lourenço JB Jr, Nahúm BS, Gonçalves AA, Kawhage PR, Silva LHM, Meneses AMC. Adição de óleo de palma na dieta sobre a lipidemia e a qualidade do sêmen de bubalinos (
Silva PF, Gadella BM. Detection of damage in mammalian sperm cells. Theriogenology. 2006;65(5):958-78.
Statistical Analysis System Institute – SAS. Base SAS 9.3. Procedures Guide. Cary, NC: USA: SAS; 2011.
Tran LV, Malla BA, Sharma AN, Kumar S, Tyagi N, Tyagi AK. Effect of omega-3 and omega-6 polyunsaturated fatty acid enriched diet on plasma IGF-1 and testosterone concentration, puberty and semen quality in male buffalo. Anim Reprod Sci. 2016;173:63-72.
Vale WG, Ohashi OM, Ribeiro HFL, Sousa JS. Semen freezing and artificial insemination in the water buffalo in the Amazon valley. Buffalo J. 1991;7:137-44.
Valinote AC, Nogueira JCM Fo, Leme PR, Silva SL, Cunha JA. Fontes de lipídio e monensina sódica na fermentação, cinética e degradabilidade ruminal de bovinos. Pesqui Agropecu Bras. 2006;41(1):117-24.
Van Tran L, Malla BA, Kumar S, Tyagi AK. Polyunsaturated fatty acids in male ruminant reproduction: a review. Asian-Australas J Anim Sci. 2017;30(5):622-37.
Vertika S, Singh KK, Rajender S. Mitochondria, spermatogenesis, and male infertility - an update. Mitochondrion. 2020;54:26-40.
Wathes DC, Abayasekara DRE, Aitken RJ. Polyunsaturated fatty acids in males and female reproduction. Biol Reprod. 2007;77(2):190-201.
Zhu Z, Li R, Feng C, Liu R, Zheng Y, Hoque SAM, Wu D, Lu H, Zhang T, Zeng W. Exogenous oleic acid and palmitic acid improve boar sperm motility via enhancing mitochondrial β-oxidation for ATP generation. Animals (Basel). 2020;10(4):591.
Submitted date:
03/22/2020
Accepted date:
10/14/2020