Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs

The present study evaluated the alterations of the oxidative stress markers in adult dogs fed with high levels of PUFA from the mixture of soybean oil enriched with docosahexaenoic acid (DHA) and supplemented with a natural algae-based antioxidant (AOX). Twelve healthy adult (2 years old) Beagle dog...

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Autores:
E. Pacheco, Gabriel F.
C. Bortolin, Rafael
R. Chaves, Paloma
F. Moreira, José C
M. Kessler, Alexandre
Trevizan, Luciano
Tipo de recurso:
Article of journal
Fecha de publicación:
2018
Institución:
Corporación Universidad de la Costa
Repositorio:
REDICUC - Repositorio CUC
Idioma:
eng
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oai:repositorio.cuc.edu.co:11323/3296
Acceso en línea:
https://hdl.handle.net/11323/3296
https://repositorio.cuc.edu.co/
Palabra clave:
Algal meal
Canines
Free radicals
Lipid oxidation
Oxidative stress
Harina de algas
Caninos Radicales
libres
Oxidación de lípidos
Estrés oxidativo
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openAccess
License
Attribution-NonCommercial-ShareAlike 4.0 International
id RCUC2_489c3a34f7d970b50d9d42376c025212
oai_identifier_str oai:repositorio.cuc.edu.co:11323/3296
network_acronym_str RCUC2
network_name_str REDICUC - Repositorio CUC
repository_id_str
dc.title.spa.fl_str_mv Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
dc.title.translated.spa.fl_str_mv Efectos del consumo de ácidos grasos poliinsaturados en el estado oxidativo de los perros adultos
title Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
spellingShingle Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
Algal meal
Canines
Free radicals
Lipid oxidation
Oxidative stress
Harina de algas
Caninos Radicales
libres
Oxidación de lípidos
Estrés oxidativo
title_short Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
title_full Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
title_fullStr Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
title_full_unstemmed Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
title_sort Effects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogs
dc.creator.fl_str_mv E. Pacheco, Gabriel F.
C. Bortolin, Rafael
R. Chaves, Paloma
F. Moreira, José C
M. Kessler, Alexandre
Trevizan, Luciano
dc.contributor.author.spa.fl_str_mv E. Pacheco, Gabriel F.
C. Bortolin, Rafael
R. Chaves, Paloma
F. Moreira, José C
M. Kessler, Alexandre
Trevizan, Luciano
dc.subject.spa.fl_str_mv Algal meal
Canines
Free radicals
Lipid oxidation
Oxidative stress
Harina de algas
Caninos Radicales
libres
Oxidación de lípidos
Estrés oxidativo
topic Algal meal
Canines
Free radicals
Lipid oxidation
Oxidative stress
Harina de algas
Caninos Radicales
libres
Oxidación de lípidos
Estrés oxidativo
description The present study evaluated the alterations of the oxidative stress markers in adult dogs fed with high levels of PUFA from the mixture of soybean oil enriched with docosahexaenoic acid (DHA) and supplemented with a natural algae-based antioxidant (AOX). Twelve healthy adult (2 years old) Beagle dogs (6 males and 6 females, 11.20 ± 1.92 kg BW), were distributed in 2 completely randomized blocks design and fed with 4 experimental diets coated with 2 lipid sources: saturated (13% bovine tallow) or unsaturated (13% soybean oil enriched with DHA), supplemented or not with 500 mg of AOX for 4 wk, intercalated with a 4 wk adaptation period. Blood samples were collected on days 0, 15, and 30 of each block. Glutathione peroxidase (GSH-Px), superoxide dismutase (SOD), sulfhydryl group (SH), protein carbonylation, thiobarbituric acid reactive substances (TBARS), and total reactive antioxidant potential (TRAP) were evaluated in the serum, while GSH-Px, SOD, glutathione S-transferase (GST), catalase (CAT), SH, and TBARS were measured in erythrocytes. There was no significant difference in most of the oxidative markers evaluated. In contrast, GST activity in erythrocytes was greater in the animals that consumed the diets coated with bovine tallow compared to dogs that consumed diets coated with soybean oil enriched with DHA (P < 0.05). Serum from dogs fed on diets supplemented with AOX presented greater TRAP values (P < 0.05). These data demonstrate that the concentrations of unsaturated fatty acids used in the diets for dogs were not sufficient to cause large changes in the oxidative status. It was not possible to evaluate the efficiency of the natural antioxidant in maintaining the oxidative balance of the animals as it appears that the oxidative status of the dogs was not challenged by the unsaturated diets. Our findings also suggest that dogs, as descendants from carrion carnivores, may have some natural protection against oxidation
publishDate 2018
dc.date.issued.none.fl_str_mv 2018-07-30
dc.date.accessioned.none.fl_str_mv 2019-05-10T16:31:27Z
dc.date.available.none.fl_str_mv 2019-05-10T16:31:27Z
dc.type.spa.fl_str_mv Artículo de revista
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dc.type.coar.spa.fl_str_mv http://purl.org/coar/resource_type/c_6501
dc.type.content.spa.fl_str_mv Text
dc.type.driver.spa.fl_str_mv info:eu-repo/semantics/article
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dc.type.version.spa.fl_str_mv info:eu-repo/semantics/acceptedVersion
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dc.identifier.issn.spa.fl_str_mv 0021-8812
dc.identifier.uri.spa.fl_str_mv https://hdl.handle.net/11323/3296
dc.identifier.instname.spa.fl_str_mv Corporación Universidad de la Costa
dc.identifier.reponame.spa.fl_str_mv REDICUC - Repositorio CUC
dc.identifier.repourl.spa.fl_str_mv https://repositorio.cuc.edu.co/
identifier_str_mv 0021-8812
Corporación Universidad de la Costa
REDICUC - Repositorio CUC
url https://hdl.handle.net/11323/3296
https://repositorio.cuc.edu.co/
dc.language.iso.none.fl_str_mv eng
language eng
dc.relation.references.spa.fl_str_mv Aebi, H. 1984. Catalase in vitro. Methods Enzymol. 105:121–126. doi.org/10.1016/S0076- 6879(84)05016-3. Aliya, S., P. Reddanna, and K. Thyagaraju. 2003. Does glutathione S-transferase Pi (GST-Pi) a marker protein for cancer? Mol. Cell Biochem. 253:319–327. doi.org/10.1023/A:1026036521852. Calder, P. C. 2012. Mechanisms of action of (n-3) fatty acids. J. Nutr. 592S–599S. doi.org/10.3945/jn.111.155259. Case, L. P., L. Daristotle, M. G. Hayek, and M. F. Raasch. 2011. Canine and feline nutrition: A resource for companion animal professional. 3rd ed., Mosby Elsevier, Missouri. Delles, R. M., Y. L. Xiong, A. D. True, T. Ao, and K. A. Dawson. 2014. Dietary antioxidant supplementation enhances lipid and protein oxidative stability of chicken broiler meat through promotion of antioxidant enzymes activity. Poult. Sci. 93:1561–1570. doi.org/10.3382/ps.2013- 03682. Draper, H. H., and M. Hadley. 1990. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 186:421–431. doi.org/10.1016/0076-6879(90)86135-I. Dresch, M. T., S. B. Rossato, V. D. Kappel, R. Biegelmeyer, M. L. M. Hoff, and P. Mayorga. 2009. Optimization and validation of an alternative method to evaluated total reactive antioxidant potential. Anal. Biochem. 385:107–114. doi.org/10.1016/j.ab.2008.10.036. Ellman, G. L. 1959. Tissue sulfhydryl group. Arch. Biochem. Biophys. 82:70–77. doi.org/10.1016/0003-9861(59)90090-6. FEDIAF, Federação Europeia das Indústrias de Pet Food. 2016. Nutritional Guidelines. Bruxelles. 1– 100. Ferreira, C. S., R. S. Vasconcellos, R. S. Pedreira, F. L. Silva, F. C. Sá, F. S. A. Kroll, A. P. J. Maria, K. S. Venturini, and A. C. Carciofi. 2014. Alterations to oxidative stress markers in dogs after a shortterm stress during transport. J. Nutr. Sci. 3(27):1–5. doi.org/10.1017/jns.2014.47. Goto, S., M. Kawakatsu, S. Izumi, Y. Urata, K. Kageyama, Y. Ihara, T. Koji, and T. Kondo. 2009. Glutathione S-transferase pi localizes in mitochondria and protects against oxidative stress. Free Radic. Biol. Med. 46:1392–1403. doi.org/10.1016/j.freeradbiomed.2009.02.025. Hadley, K. B., J. E. Bauer, and N. W. Milgram. 2017. The oil-rich alga Schizochytrium sp. as a dietary source of docosahexaenoic acid improves shape discrimination learning associated with visual processing in a canine model of senescence. Prostaglandins Leukot. Essent. Fatty Acids. 118:10– 18. doi.org/10.1016/j.plefa.2017.01.011. Hall, J. A. 1996. Potential adverse effects a long-term consumption of (n-3) fatty acids. Compend. Contin. Educ. Pract. Vet. 18(8):879–895. Hall, J. A., R. A. Picton, M. M. Skinner, D. E. Jewell, and R. C. Wander. 2006. The (n-3) fatty acid dose, independent of the (n-6) to (n-3) fatty acid ratio, affects the plasma fatty acid profile of normal dogs. J. Nutr. 136:2338–2344. doi.org/10.1093/jn/136.9.2338. Hall, J. A., K. A. Tooley, J. L. Gradin, D. E. Jewell, and R. C. Wander. 2003. Effects of dietary n-6 and n3 fatty acids and vitamin E on the immune response of healthy geriatric dogs. Am. J. Vet. Res. 64:762–772. doi.org/10.2460/ajvr.2003.64.762. Hall, J. A., R. M. Chinn, W. R. Vorachek, M. E. Gorman, J. L. Greitl, D. K. Joshi, and D. E. Jewell. 2011. Influence of dietary antioxidants and fatty acids on neutrophil mediated bacterial killing and gene expression in healthy Beagles. Vet. Immunol Immunophatol. 139:271–228. doi.org/10.1016/j.vetimm.2010.10.020. Kil, D. Y., B. M. V. Boler, C. J. Apanavicius, L. B. Schook, and K. S. Swanson. 2010. Age and diet affect gene expression profiles in canine liver tissue. PLoS One. 5(10): e13319:1–12. doi.org/10.1371/journal.pone.0013319. LeBlanc, C. J., J. E. Bauer, G. Hosgood, and G. E. Mauldin. 2005. Effect of dietary fish oil and vitamin E supplementation on hematologic and serum biochemical analytes and oxidative status in young dogs. Vet. Ther. 6:325–340. Lenox, C. E., and J. E. Bauer. 2013. Potential adverse effects of omega-3 fatty acids in dogs and cats. J. Vet. Intern. Med. 27:217–226. doi.org/10.1111/jvim.12033. Levine, R. J., D. Garland, C. N. Oliver, A. Amici, I. Climent, A. G. Lenz, B. W. Ahn, S. Shaltiel, and E. R. Stadtman. 1990. Determination of carbonyl content in oxidatively modified protein. Methods Enzymol. 186:464–478. doi.org/10.1016/0076-6879(90)86141-H. Lissi, F., C. Pascual, and M. D. Del Castillo. 1992. Luminol luminescence induced by 2,2’-Azo-bis(2- amidinopropane) thermolysis. Free Radic. Res. Commun. 17:299–311. doi.org/10.3109/10715769209079523. Marx, F. R., L. Trevizan, F. M. O. B. Saad, K. G. Lisenko, J. S. Reis, and A. M. Kessler. 2017. Endogenous fat loss and true total tract digestibility of poultry fat in adult dogs. J. Anim. Sci. 95:2928–2935. doi.org/10.2527/jas.2017.1393. Misra, H. P, and I. Fridovich. 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Biol. Chem. 247:3170–3175. Mueller, R. S., K. V. Fieseler, M. J. Fettman, S. Zabel, R. A. W. Rosychuk, G. K. Ogilvie, and T. L. Greenwalt. 2004. Effect of omega-3 fatty acids on canine atopic dermatitis. J. Small Anim. Pract. 45:293–297. doi.org/10.1111/j.1748-5827.2004.tb00238.x. Mueller, R. S., M. J. Fettman, K, Richardson, R. A. Hansen, A. Miller, J. Magowitz, and G. K. Ogilvie. 2005. Plasma and skinconcentrations of polyunsaturated fatty acids before and after supplementation with n-3 fatty acids in dogs with atopic dermatitis. Am. J. Vet. Res. 66:868–873. doi.org/10.2460/ajvr.2005.66.868. NRC. 2006. Nutrient requirement of dogs and cats. Natl. Acad. Press., Washington, DC. Ogilvie, G. K., M. J. Fettman, C. H. Mallinckrodt, J. A. Walton, R. A. Hansen, D. J. Davenport, K. L. Gross, K. L. Richardson, Q. Rogers, and M. S. Hand. 2000. Effect of fish oil, arginine, and doxorubicin chemotherapy on remission and survival time for dogs with lymphoma: a doubleblind, randomized placebo-controlled study. Cancer, 88:1916–1928. doi.org/10.1002/(SICI)1097- 0142(20000415)88:8<1916:: AID-CNCR22>3.0.CO;2-F. Ogoshi, R. C. S., M. G. Zangeronimo, J. S. Reis, R. V. Souza, T. M. Gonçalves, K. G. Lisenko, I. O. Alves, K. W. Silva, J. França, and F. M. O. B. Saad. 2016. Equilíbrio acidobásico, parâmetros urinários e sanguíneos de gatos induzidos ao estresse e suplementados com compostos antioxidantes. (In Portuguese) Arq. Bras. Mad. Vet. Zootec. 68(5):1121–1128. doi.org/10.1590/1678-4162-7966. Salas, A., F. Subirada, M. Pérez-Enciso, F. Blanch, I. Jeusette, V. Romano, and C. Torre. 2008. Plant polyphenol intake alters gene expression in canine leukocytes. J. Nutrigenet. Nutrigenomics. 2:43–52. doi.org/10.1159/000200018. Waldron, M. K. M. K. Hannah, and J. E. Bauer. 2012. Plasma Phospholipid Fatty Acid and Ex Vivo Neutrophil Responses are Differentially Altered in Dogs Fed Fish- and Linseed-Oil Containing Diets at the Same n-6:n-3 Fatty Acid Ratio. Lipids. 47:425–434. doi.org/10.1007/s11745-012-3652-7. Wander, R. C., J. A. Hall, J. L. Gradin, S. H. Du, and. D. E. Jewell. 1997. The ratio of dietary (n-6) to (n3) fatty acids influences immune system function, eicosanoid metabolism, lipid peroxidation and vitamin E status in aged dogs. J. Nutr. 127:1198–1205. doi.org/10.1093/jn/127.6.1198. Wendel, A. 1981. Glutathione peroxidase. Methods Enzymol. 77:325–333.
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spelling E. Pacheco, Gabriel F.C. Bortolin, RafaelR. Chaves, PalomaF. Moreira, José CM. Kessler, AlexandreTrevizan, Luciano2019-05-10T16:31:27Z2019-05-10T16:31:27Z2018-07-300021-8812https://hdl.handle.net/11323/3296Corporación Universidad de la CostaREDICUC - Repositorio CUChttps://repositorio.cuc.edu.co/The present study evaluated the alterations of the oxidative stress markers in adult dogs fed with high levels of PUFA from the mixture of soybean oil enriched with docosahexaenoic acid (DHA) and supplemented with a natural algae-based antioxidant (AOX). Twelve healthy adult (2 years old) Beagle dogs (6 males and 6 females, 11.20 ± 1.92 kg BW), were distributed in 2 completely randomized blocks design and fed with 4 experimental diets coated with 2 lipid sources: saturated (13% bovine tallow) or unsaturated (13% soybean oil enriched with DHA), supplemented or not with 500 mg of AOX for 4 wk, intercalated with a 4 wk adaptation period. Blood samples were collected on days 0, 15, and 30 of each block. Glutathione peroxidase (GSH-Px), superoxide dismutase (SOD), sulfhydryl group (SH), protein carbonylation, thiobarbituric acid reactive substances (TBARS), and total reactive antioxidant potential (TRAP) were evaluated in the serum, while GSH-Px, SOD, glutathione S-transferase (GST), catalase (CAT), SH, and TBARS were measured in erythrocytes. There was no significant difference in most of the oxidative markers evaluated. In contrast, GST activity in erythrocytes was greater in the animals that consumed the diets coated with bovine tallow compared to dogs that consumed diets coated with soybean oil enriched with DHA (P < 0.05). Serum from dogs fed on diets supplemented with AOX presented greater TRAP values (P < 0.05). These data demonstrate that the concentrations of unsaturated fatty acids used in the diets for dogs were not sufficient to cause large changes in the oxidative status. It was not possible to evaluate the efficiency of the natural antioxidant in maintaining the oxidative balance of the animals as it appears that the oxidative status of the dogs was not challenged by the unsaturated diets. Our findings also suggest that dogs, as descendants from carrion carnivores, may have some natural protection against oxidationEl presente estudio evaluó las alteraciones de los marcadores de estrés oxidativo en perros adultos alimentados con altos niveles de PUFA de la mezcla de aceite de soja enriquecido con ácido docosahexaenoico (DHA) y suplementado con un antioxidante natural basado en algas (AOX). Doce perros Beagle adultos (2 años) sanos (6 machos y 6 hembras, 11.20 ± 1.92 kg BW), se distribuyeron en 2 bloques de diseño completamente al azar y se alimentaron con 4 dietas experimentales cubiertas con 2 fuentes de lípidos: saturadas (13% de sebo bovino). ) o insaturado (13% de aceite de soja enriquecido con DHA), suplementado o no con 500 mg de AOX durante 4 semanas, intercalado con un período de adaptación de 4 semanas. Las muestras de sangre se recolectaron en los días 0, 15 y 30 de cada bloque. La glutatión peroxidasa (GSH-Px), la superóxido dismutasa (SOD), el grupo sulfhidrilo (SH), la carbonilación de proteínas, las sustancias reactivas al ácido tiobarbitúrico (TBARS) y el potencial antioxidante reactivo total (TRAP) se evaluaron en el suero, mientras que GSH-Px, SOD, glutatión S-transferasa (GST), catalasa (CAT), SH y TBARS se midieron en eritrocitos. No hubo diferencia significativa en la mayoría de los marcadores oxidativos evaluados. En contraste, la actividad de GST en los eritrocitos fue mayor en los animales que consumieron las dietas recubiertas con sebo bovino en comparación con los perros que consumieron dietas recubiertas con aceite de soja enriquecido con DHA (P <0.05). El suero de perros alimentados con dietas suplementadas con AOX presentó mayores valores de TRAP (P <0.05). Estos datos demuestran que las concentraciones de ácidos grasos insaturados utilizados en las dietas para perros no fueron suficientes para causar grandes cambios en el estado oxidativo. No fue posible evaluar la eficacia del antioxidante natural para mantener el equilibrio oxidativo de los animales, ya que parece que el estado oxidativo de los perros no fue desafiado por las dietas insaturadas. Nuestros hallazgos también sugieren que los perros, como descendientes de carnívoros de carroña, pueden tener alguna protección natural contra la oxidaciónE. Pacheco, Gabriel F.-b11a5fb0-e08f-4e3f-abc7-077c109bc946-0C. Bortolin, Rafael-57e00f7b-f24c-48a5-99c5-0de7dc19c046-0R. Chaves, Paloma-9d300773-1fc2-4a23-ad39-96871d7a5ea0-0F. Moreira, José C-09ed84e3-ec49-43f8-9eae-bb56092f144e-0M. Kessler, Alexandre-6bd96b66-650a-4fd9-a355-8be41f7a19c3-0Trevizan, Luciano-c9548b82-c54d-45a5-8943-34a3dc5e1d91-0engJournal of Animal ScienceAttribution-NonCommercial-ShareAlike 4.0 Internationalhttp://creativecommons.org/licenses/by-nc-sa/4.0/info:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2Algal mealCaninesFree radicalsLipid oxidationOxidative stressHarina de algasCaninos RadicaleslibresOxidación de lípidosEstrés oxidativoEffects of the consumption of polyunsaturated fatty acids on the oxidative status of adult dogsEfectos del consumo de ácidos grasos poliinsaturados en el estado oxidativo de los perros adultosArtículo de revistahttp://purl.org/coar/resource_type/c_6501http://purl.org/coar/resource_type/c_2df8fbb1Textinfo:eu-repo/semantics/articlehttp://purl.org/redcol/resource_type/ARTinfo:eu-repo/semantics/acceptedVersionAebi, H. 1984. Catalase in vitro. Methods Enzymol. 105:121–126. doi.org/10.1016/S0076- 6879(84)05016-3. Aliya, S., P. Reddanna, and K. Thyagaraju. 2003. Does glutathione S-transferase Pi (GST-Pi) a marker protein for cancer? Mol. Cell Biochem. 253:319–327. doi.org/10.1023/A:1026036521852. Calder, P. C. 2012. Mechanisms of action of (n-3) fatty acids. J. Nutr. 592S–599S. doi.org/10.3945/jn.111.155259. Case, L. P., L. Daristotle, M. G. Hayek, and M. F. Raasch. 2011. Canine and feline nutrition: A resource for companion animal professional. 3rd ed., Mosby Elsevier, Missouri. Delles, R. M., Y. L. Xiong, A. D. True, T. Ao, and K. A. Dawson. 2014. Dietary antioxidant supplementation enhances lipid and protein oxidative stability of chicken broiler meat through promotion of antioxidant enzymes activity. Poult. Sci. 93:1561–1570. doi.org/10.3382/ps.2013- 03682. Draper, H. H., and M. Hadley. 1990. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 186:421–431. doi.org/10.1016/0076-6879(90)86135-I. Dresch, M. T., S. B. Rossato, V. D. Kappel, R. Biegelmeyer, M. L. M. Hoff, and P. Mayorga. 2009. Optimization and validation of an alternative method to evaluated total reactive antioxidant potential. Anal. Biochem. 385:107–114. doi.org/10.1016/j.ab.2008.10.036. Ellman, G. L. 1959. Tissue sulfhydryl group. Arch. Biochem. Biophys. 82:70–77. doi.org/10.1016/0003-9861(59)90090-6. FEDIAF, Federação Europeia das Indústrias de Pet Food. 2016. Nutritional Guidelines. Bruxelles. 1– 100. Ferreira, C. S., R. S. Vasconcellos, R. S. Pedreira, F. L. Silva, F. C. Sá, F. S. A. Kroll, A. P. J. Maria, K. S. Venturini, and A. C. Carciofi. 2014. Alterations to oxidative stress markers in dogs after a shortterm stress during transport. J. Nutr. Sci. 3(27):1–5. doi.org/10.1017/jns.2014.47. Goto, S., M. Kawakatsu, S. Izumi, Y. Urata, K. Kageyama, Y. Ihara, T. Koji, and T. Kondo. 2009. Glutathione S-transferase pi localizes in mitochondria and protects against oxidative stress. Free Radic. Biol. Med. 46:1392–1403. doi.org/10.1016/j.freeradbiomed.2009.02.025. Hadley, K. B., J. E. Bauer, and N. W. Milgram. 2017. The oil-rich alga Schizochytrium sp. as a dietary source of docosahexaenoic acid improves shape discrimination learning associated with visual processing in a canine model of senescence. Prostaglandins Leukot. Essent. Fatty Acids. 118:10– 18. doi.org/10.1016/j.plefa.2017.01.011. Hall, J. A. 1996. Potential adverse effects a long-term consumption of (n-3) fatty acids. Compend. Contin. Educ. Pract. Vet. 18(8):879–895. Hall, J. A., R. A. Picton, M. M. Skinner, D. E. Jewell, and R. C. Wander. 2006. The (n-3) fatty acid dose, independent of the (n-6) to (n-3) fatty acid ratio, affects the plasma fatty acid profile of normal dogs. J. Nutr. 136:2338–2344. doi.org/10.1093/jn/136.9.2338. Hall, J. A., K. A. Tooley, J. L. Gradin, D. E. Jewell, and R. C. Wander. 2003. Effects of dietary n-6 and n3 fatty acids and vitamin E on the immune response of healthy geriatric dogs. Am. J. Vet. Res. 64:762–772. doi.org/10.2460/ajvr.2003.64.762. Hall, J. A., R. M. Chinn, W. R. Vorachek, M. E. 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