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Journal of Nutrition and Metabolism
Volume 2016, Article ID 6462120, 13 pages
http://dx.doi.org/10.1155/2016/6462120
Research Article

Omega-3 Fatty Acids: Possible Neuroprotective Mechanisms in the Model of Global Ischemia in Rats

1Faculty of Medicine, Estácio of Juazeiro do Norte (FMJ), Rua Tenente Raimundo Rocha 515, 63040-360 Juazeiro do Norte, CE, Brazil
2Federal University of Ceará (UFC), Rua Coronel Nunes de Melo 1127, 60430-270 Fortaleza, CE, Brazil
3Federal University of São Paulo (UNIFESP), Rua Pedro de Toledo 669, 04039-032 São Paulo, SP, Brazil

Received 17 December 2015; Revised 1 April 2016; Accepted 4 April 2016

Academic Editor: Duo Li

Copyright © 2016 Maria Elizabeth Pereira Nobre et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Durukan and T. Tatlisumak, “Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia,” Pharmacology Biochemistry and Behavior, vol. 87, no. 1, pp. 179–197, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Braeuninger and C. Kleinschnitz, “Rodent models of focal cerebral ischemia: procedural pitfalls and translational problems,” Experimental & Translational Stroke Medicine, vol. 1, pp. 1–11, 2009. View at Google Scholar
  3. M. Bacigaluppi, G. Comi, and D. M. Hermann, “Animal models of ischemic stroke. part two: modeling cerebral ischemia,” The Open Neurology Journal, vol. 4, pp. 34–38, 2010. View at Google Scholar
  4. Y. Huang and J. O. McNamara, “Ischemic stroke: ‘Acidotoxicity’ is a perpetrator,” Cell, vol. 118, no. 6, pp. 665–666, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Mergenthaler, U. Dirnagl, and A. Meisel, “Pathophysiology of stroke: lessons from animal models,” Metabolic Brain Disease, vol. 19, no. 3-4, pp. 151–167, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. T. G. Phan, P. M. Wright, R. Markus, D. W. Howells, S. M. Davis, and G. A. Donnan, “Salvaging the ischaemic penumbra: more than just reperfusion?” Clinical and Experimental Pharmacology and Physiology, vol. 29, no. 1-2, pp. 1–10, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. W. Zhang, P. Li, X. Hu, F. Zhang, J. Chen, and Y. Gao, “Omega-3 polyunsaturated fatty acids in the brain: metabolism and neuroprotection,” Frontiers in Bioscience, vol. 16, no. 7, pp. 2653–2670, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. W. Phillis and M. H. O'Regan, “Characterization of modes of release of amino acids in the ischemic/reperfused rat cerebral cortex,” Neurochemistry International, vol. 43, no. 4-5, pp. 461–467, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Chalon, S. Delion-Vancassel, C. Belzung et al., “Dietary fish oil affects monoaminergic neurotransmission and behavior in rats,” Journal of Nutrition, vol. 128, no. 12, pp. 2512–2519, 1998. View at Google Scholar · View at Scopus
  10. S. Chalon, “Omega-3 fatty acids and monoamine neurotransmission,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 75, no. 4-5, pp. 259–269, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. C. J. S. Price, E. A. Warburton, and D. K. Menon, “Human cellular inflammation in the pathology of acute cerebral ischaemia,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 74, no. 11, pp. 1476–1484, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Jin, G. Yang, and G. Li, “Inflammatory mechanisms in ischemic stroke: role of inflammatory cells,” Journal of Leukocyte Biology, vol. 87, no. 5, pp. 779–789, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. P. C. Calder, “Dietary modification of inflammation with lipids,” Proceedings of the Nutrition Society, vol. 61, no. 3, pp. 345–358, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. A. P. Simopoulos, “Omega-3 fatty acids in inflammation and autoimmune diseases,” Journal of the American College of Nutrition, vol. 21, no. 6, pp. 495–505, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. P. C. Calder, “Omega-3 fatty acids and inflammatory processes,” Nutrients, vol. 2, no. 3, pp. 355–374, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. P. C. Calder, “Fatty acids and inflammation: the cutting edge between food and pharma,” European Journal of Pharmacology, vol. 668, no. 1, pp. S50–S58, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. M. E. P. Nobre, A. O. Correia, M. B. Borges et al., “Eicosapentaenoic acid and docosahexaenoic acid exert anti-inflammatory and antinociceptive effects in rodents at low doses,” Nutrition Research, vol. 34, pp. 251–263, 2013. View at Google Scholar
  18. L. Prut and C. Belzung, “The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review,” European Journal of Pharmacology, vol. 463, no. 1–3, pp. 3–33, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. R. G. M. Morris, “Spatial localization does not require the presence of local cues,” Learning and Motivation, vol. 12, no. 2, pp. 239–260, 1981. View at Publisher · View at Google Scholar · View at Scopus
  20. C. V. Vorhees and M. T. Williams, “Morris water maze: procedures for assessing spatial and related forms of learning and memory,” Nature Protocols, vol. 1, no. 2, pp. 848–858, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. J. B. Bederson, L. H. Pitts, S. M. Germano, M. C. Nishimura, R. L. Davis, and H. M. Bartkowski, “Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats,” Stroke, vol. 17, no. 6, pp. 1304–1308, 1986. View at Publisher · View at Google Scholar · View at Scopus
  22. F. Block, “Global ischemia and behavioural deficits,” Progress in Neurobiology, vol. 58, no. 3, pp. 279–295, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Hodges, A. Nelson, D. Virley, T. R. Kershaw, and J. D. Sinden, “Cognitive deficits induced by global cerebral ischaemia: prospects for transplant therapy,” Pharmacology Biochemistry and Behavior, vol. 56, no. 4, pp. 763–780, 1997. View at Publisher · View at Google Scholar · View at Scopus
  24. W. A. Pulsinelli, J. B. Brierley, and F. Plum, “Temporal profile of neuronal damage in a model of transient forebrain ischemia,” Annals of Neurology, vol. 11, no. 5, pp. 491–498, 1982. View at Publisher · View at Google Scholar · View at Scopus
  25. M. A. Atlasi, H. Naderian, M. Noureddini, E. Fakharian, and A. Azami, “The morphology of rat hippocampus CA1 neurons following modified two and four vessel global ischemia models,” Archives of Trauma Research, vol. 2, no. 3, pp. 124–128, 2013. View at Publisher · View at Google Scholar
  26. I. Fedorova and N. Salem Jr., “Omega-3 fatty acids and rodent behavior,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 75, no. 4-5, pp. 271–289, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Takeuchi, M. Iwanaga, and E. Harada, “Possible regulatory mechanism of DHA-induced anti-stress reaction in rats,” Brain Research, vol. 964, no. 1, pp. 136–143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Harauma and T. Moriguchi, “Dietary n-3 fatty acid deficiency in mice enhances anxiety induced by chronic mild stress,” Lipids, vol. 46, no. 5, pp. 409–416, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Vinot, M. Jouin, A. Lhomme-Duchadeuil et al., “Omega-3 fatty acids from fish oil lower anxiety, improve cognitive functions and reduce spontaneous locomotor activity in a non-human primate,” PLoS ONE, vol. 6, no. 6, Article ID e20491, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Plamondon and M.-C. Roberge, “Dietary PUFA supplements reduce memory deficits but not CA1 ischemic injury in rats,” Physiology and Behavior, vol. 95, no. 3, pp. 492–500, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. H.-M. Su, “Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance,” Journal of Nutritional Biochemistry, vol. 21, no. 5, pp. 364–373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Hashimoto, S. Hossain, Y. Tanabe et al., “The protective effect of dietary eicosapentaenoic acid against impairment of spatial cognition learning ability in rats infused with amyloid β140,” Journal of Nutritional Biochemistry, vol. 20, no. 12, pp. 965–973, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S. C. Heinrichs, “Dietary ω3 fatty acid supplementation for optimizing neuronal structure and function,” Molecular Nutrition and Food Research, vol. 54, no. 4, pp. 447–456, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. J. S. Fernandes, M. A. Mori, R. Ekuni, R. M. W. Oliveira, and H. Milani, “Long-term treatment with fish oil prevents memory impairments but not hippocampal damage in rats subjected to transient, global cerebral ischemia,” Nutrition Research, vol. 28, no. 11, pp. 798–808, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Okabe, T. Nakamura, T. Toyoshima, O. Miyamoto, F. Lu, and T. Itano, “Eicosapentaenoic acid prevents memory impairment after ischemia by inhibiting inflammatory response and oxidative damage,” Journal of Stroke and Cerebrovascular Diseases, vol. 20, no. 3, pp. 188–195, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. N. F. A. Sopian, M. Ajat, N. I. Shafie et al., “Does short-term dietary omega-3 fatty acid supplementation influence brain hippocampus gene expression of zinc transporter-3?” International Journal of Molecular Sciences, vol. 16, no. 7, pp. 15800–15810, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. L. G. Puskás, K. Kitajka, C. Nyakas, G. Barcelo-Coblijn, and T. Farkas, “Short-term administration of omega 3 fatty acids from fish oil results in increased transthyretin transcription in old rat hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 4, pp. 1580–1585, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. W. Zhang, X. Hu, W. Yang, Y. Gao, and J. Chen, “Omega-3 polyunsaturated fatty acid supplementation confers long-term neuroprotection against neonatal hypoxic-ischemic brain injury through anti-inflammatory actions,” Stroke, vol. 41, no. 10, pp. 2341–2347, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Tang, Z.-J. Li, J. Xu et al., “Short term effects of different omega-3 fatty acid formulation on lipid metabolism in mice fed high or low fat diet,” Lipids in Health and Disease, vol. 11, article 70, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Ajami, S. Eghtesadi, R. Habibey et al., “Effect of short- and long-term treatment with Omega-3 fatty acids on scopolamine-induced amnésia,” Iranian Journal of Pharmaceutical Research, vol. 11, no. 2, pp. 533–540, 2012. View at Google Scholar · View at Scopus
  41. S. K. Raatz, J. B. Redmon, N. Wimmergren, J. V. Donadio, and D. M. Bibus, “Enhanced absorption of n-3 fatty acids from emulsified compared with encapsulated fish oil,” Journal of the American Dietetic Association, vol. 109, no. 6, pp. 1076–1081, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Yurko-Mauro, D. McCarthy, D. Rom et al., “Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline,” Alzheimer's and Dementia, vol. 6, no. 6, pp. 456–464, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. S. C. Gerhardt and C. A. Boast, “Motor activity changes following cerebral ischemia in gerbils are correlated with the degree of neuronal degeneration in hippocampus,” Behavioral Neuroscience, vol. 102, no. 2, pp. 301–303, 1988. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Karasawa, H. Araki, and S. Otomo, “Changes in locomotor activity and passive avoidance task performance induced by cerebral ischemia in mongolian gerbils,” Stroke, vol. 25, no. 3, pp. 645–650, 1994. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Milot and H. Plamondon, “Ischemia-induced hyperactivity: effects of dim versus bright illumination on open-field exploration and habituation following global ischemia in rats,” Behavioural Brain Research, vol. 192, no. 2, pp. 166–172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. M. R. Milot and H. Plamondon, “Time-dependent effects of global cerebral ischemia on anxiety, locomotion, and habituation in rats,” Behavioural Brain Research, vol. 200, no. 1, pp. 173–180, 2009. View at Publisher · View at Google Scholar
  47. T. G. Ohk, K.-Y. Yoo, S. M. Park et al., “Neuronal damage using fluoro-jade B histofluorescence and gliosis in the striatum after various durations of transient cerebral ischemia in gerbils,” Neurochemical Research, vol. 37, no. 4, pp. 826–834, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. R. E. Hartman, J. M. Lee, G. J. Zipfel, and D. F. Wozniak, “Characterizing learning deficits and hippocampal neuron loss following transient global cerebral ischemia in rats,” Brain Research, vol. 1043, no. 1-2, pp. 48–56, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Von Euler, O. Bendel, T. Bueters, J. Sandin, and G. Von Euler, “Profound but transient deficits in learning and memory after global ischemia using a novel water maze test,” Behavioural Brain Research, vol. 166, no. 2, pp. 204–210, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. K. D. Langdon, S. Granter-Button, and D. Corbett, “Persistent behavioral impairments and neuroinflammation following global ischemia in the rat,” European Journal of Neuroscience, vol. 28, no. 11, pp. 2310–2318, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Bueters, M. von Euler, O. Bendel, and G. von Euler, “Degeneration of newly formed CA1 neurons following global ischemia in the rat,” Experimental Neurology, vol. 209, no. 1, pp. 114–124, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Luo, H. Ren, J.-B. Wan et al., “Enriched endogenous omega-3 fatty acids in mice protect against global ischemia injury,” Journal of Lipid Research, vol. 55, no. 7, pp. 1288–1297, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. W. Cao, A. Drumheller, M. Zaharia, G. Lafond, J.-R. Brunette, and F. B. Jolicoeur, “Effects of experimentally induced ischemia on dopamine metabolism in rabbit retina,” Investigative Ophthalmology & Visual Science, vol. 34, no. 11, pp. 3140–3146, 1993. View at Google Scholar · View at Scopus
  54. W. A. Pulsinelli and T. E. Duffy, “Regional energy balance in rat brain after transient forebrain ischemia,” Journal of Neurochemistry, vol. 40, no. 5, pp. 1500–1503, 1983. View at Publisher · View at Google Scholar · View at Scopus
  55. L. A. Phebus and J. A. Clemens, “Effects of transient, global, cerebral ischemia on striatal extracellular dopamine, serotonin and their metabolites,” Life Sciences, vol. 44, no. 19, pp. 1335–1342, 1989. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Y.-T. Globus, “Role of dopamine in ischemic neuronal damage,” Stroke, vol. 20, no. 6, pp. 827–828, 1989. View at Google Scholar · View at Scopus
  57. T. Kawano, K. Tsutsumi, H. Miyake, and K. Mori, “Striatal dopamine in acute cerebral ischemia of stroke-resistant rats,” Stroke, vol. 19, no. 12, pp. 1540–1543, 1988. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Slivka, T. S. Brannan, J. Weinberger, P. J. Knott, and G. Cohen, “Increase in extracellular dopamine in the striatum during cerebral ischemia: a study utilizing cerebral microdialysis,” Journal of Neurochemistry, vol. 50, no. 6, pp. 1714–1718, 1988. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Kuruvilla, R. Cherian, D. R. Theodore, and J. Abraham, “Temporal profile of tissue levels of dopamine and its metabolites, HVA and DOPAC following focal cerebral ischaemia in anaesthetized primates,” Clinical and Experimental Pharmacology and Physiology, vol. 13, no. 7, pp. 519–524, 1986. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Ogura, M. Shibuya, Y. Suzuki, M. Kanamori, and I. Ikegaki, “Changes in striatal dopamine metabolism measured by in vivo voltammetry during transient brain ischemia in rats,” Stroke, vol. 20, no. 6, pp. 783–787, 1989. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Brannan, J. Weinberger, P. Knott et al., “Direct evidence of acute, massive striatal dopamine release in gerbils with unilateral strokes,” Stroke, vol. 18, no. 1, pp. 108–110, 1987. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Weinberger, J. Nieves-Rosa, and G. Cohen, “Nerve terminal damage in cerebral ischemia: protective effect of alpha-methyl-para-tyrosine,” Stroke, vol. 16, no. 5, pp. 864–870, 1985. View at Publisher · View at Google Scholar · View at Scopus
  63. J. A. Clemens and L. A. Phebus, “Dopamine depletion protects striatal neurons from ischemia-induced cell death,” Life Sciences, vol. 42, no. 6, pp. 707–713, 1988. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Zimmer, S. Delion-Vancassel, G. Durand et al., “Modification of dopamine neurotransmission in the nucleus accumbens of rats deficient in n-3 polyunsaturated fatty acids,” Journal of Lipid Research, vol. 41, no. 1, pp. 32–40, 2000. View at Google Scholar · View at Scopus
  65. L. C. Schmued and K. J. Hopkins, “Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration,” Brain Research, vol. 874, no. 2, pp. 123–130, 2000. View at Publisher · View at Google Scholar · View at Scopus
  66. H. D. Cardoso, P. P. Passos, C. J. Lagranha et al., “Differential vulnerability of Substantia nigra and Corpus striatum to oxidative insult induced by reduced dietary levels of essential fatty acids,” Frontiers in Human Neuroscience, vol. 6, article 249, 2012. View at Publisher · View at Google Scholar
  67. J.-C. Delpech, C. Madore, C. Joffre et al., “Transgenic increase in n-3/n-6 fatty acid ratio protects against cognitive deficits induced by an immune challenge through decrease of neuroinflammation,” Neuropsychopharmacology, vol. 40, no. 3, pp. 525–536, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. R. De Caterina, M. I. Cybulsky, S. K. Clinton, M. A. Gimbrone Jr., and P. Libby, “The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 14, no. 11, pp. 1829–1836, 1994. View at Publisher · View at Google Scholar · View at Scopus
  69. T. A. Babcock, W. S. Helton, D. Hong, and N. J. Espat, “Omega-3 fatty acid lipid emulsion reduces LPS-stimulated macrophage TNF-α production,” Surgical Infections, vol. 3, no. 2, pp. 145–149, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. T. E. Novak, T. A. Babcock, D. H. Jho, W. S. Helton, and N. J. Espat, “NF-κB inhibition by ω-3 fatty acids modulates LPS-stimulated macrophage TNF-α-transcription,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 284, no. 1, pp. L84–L89, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. A. A. Nielsen, L. G. M. Jørgensen, J. N. Nielsen et al., “Omega-3 fatty acids inhibit an increase of proinflammatory cytokines in patients with active Crohn's disease compared with omega-6 fatty acids,” Alimentary Pharmacology and Therapeutics, vol. 22, no. 11-12, pp. 1121–1128, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. I. H. Skuladottir, D. H. Petursdottir, and I. Hardardottir, “The effects of omega-3 polyunsaturated fatty acids on TNF-α and IL-10 secretion by murine peritoneal cells in vitro,” Lipids, vol. 42, no. 8, pp. 699–706, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. J. X. Kang and K. H. Weylandt, “Modulation of inflammatory cytokines by omega-3 fatty acids,” Sub-Cellular Biochemistry, vol. 49, pp. 133–143, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. P. C. Calder, “Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology?” British Journal of Clinical Pharmacology, vol. 75, no. 3, pp. 645–662, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. J. H. Garman, S. Mulroney, M. Manigrasso, E. Flynn, and C. Maric, “Omega-3 fatty acid rich diet prevents diabetic renal disease,” American Journal of Physiology—Renal Physiology, vol. 296, no. 2, pp. F306–F316, 2009. View at Publisher · View at Google Scholar
  76. A. Razzak, C. Aldrich, T. A. Babcock, A. Saied, and N. J. Espat, “Attenuation of iNOS in an LPS-stimulated macrophage model by omega-3 fatty acids is independent of COX-2 derived PGE2,” Journal of Surgical Research, vol. 145, no. 2, pp. 244–250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Suschek, O. Schnorr, and V. Kolb-Bachofen, “The role of iNOS in chronic inflammatory processes in vivo: Is it damage-promoting, protective, or active at all?” Current Molecular Medicine, vol. 4, no. 7, pp. 763–775, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. Kobayashi, “The regulatory role of nitric oxide in proinflammatory cytokine expression during the induction and resolution of inflammation,” Journal of Leukocyte Biology, vol. 88, no. 6, pp. 1157–1162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. V. Ramirez-Ramirez, M. A. Macias-Islas, G. G. Ortiz et al., “Efficacy of fish oil on serum of TNF α, IL-1 β, and IL-6 oxidative stress markers in multiple sclerosis treated with interferon beta-1b,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 709493, 8 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. N. Blondeau, R. H. Lipsky, M. Bourourou, M. W. Duncan, P. B. Gorelick, and A. M. Marini, “Alpha-linolenic acid: an omega-3 fatty acid with neuroprotective properties—Ready for use in the stroke clinic?” BioMed Research International, vol. 2015, Article ID 519830, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus