Fish oil as effective supplement preventing inflammatory and histopathological alterations in adjuvant-induced arthritis in rats
DOI:
https://doi.org/10.33448/rsd-v10i4.14046Keywords:
Fish oil; Freund’s complete adjuvant; Antiinflammatory effect; Cytokines.Abstract
In this study was investigated the effect of treatment with a fish oil preparation (FOP) on inflammatory and histopathological parameters in a rat model of adjuvant-induced arthritis (AIA). Paw edema, the severity of secondary lesions, the number of synovial leukocytes, and serum nitric oxide and cytokines concentrations were evaluated. Histological changes in cartilage and bone of the femorotibial articulation in the paws were analyzed by hematoxylin/eosin and sirius red-hematoxylin staining. Oral treatment with the FOP (75, 150, and 300 mg/kg) that was initiated on the day of arthritis induction (day zero) and maintained for 21 days inhibited inflammatory signals and prevented morphological changes in cartilage and bone of the femorotibial articulation of the paws. These effects could be at least partially attributable to inhibitory and modulatory actions of the FOP on the production and release of nitric oxide and cytokines that participate in the pathophysiology of AIA.
References
Ames, F. Q, Sato, F., Castro, L. V., Arruda, L. L. M., Rocha, B. A., Cuman, R. K. N., Baesso, M. L, & Bersani-Amado, C. A. (2017). Evidence of anti-inflammatory effect and percutaneous penetration of a topically applied fish oil preparation: a photoacoustic spectroscopy study. Journal of Biomedical Optics, 22(5), 055003.
Ames, F. Q., Bracht, L., Sato, F., Castro-Hoshino, L. V., Rocha, B. A., Oliveira, L. A., Lima, E. P., Cuman, R. K. N., Baesso, M. L., & Bersani-Amado, C. A. (2020). Fish oil preparation inhibits leukocyte recruitment and bands that characterize inflamed tissue in a model of phenol-induced skin inflammation: percutaneous penetration of a topically applied preparation demonstrated by photoacoustic spectroscopy. Natural Product Research, 34(16), 2341-2345.
Arruda, L. L. M., Ames, F. Q., Morais, D. R., Grespan, R., Gil, A. P. M., Silva, M. A. R. C. P., Visentainer, J. V., Cuman, R. K. N., & Bersani-Amado, C. A. (2017). A single administration of fish oil inhibits the acute inflammatory response in rats. Asian Pacific Journal of Tropical Medicine, 10(8), 765-772.
Assier, E., Boissier, M. C. J. M., & Dayer, J. M.(2010). Interleukin-6: from identification of the cytokine to development of targeted treatments. Joint Bone Spine, 77(6), 532-536.
Boissier, M., Semerano, L., Challal. S., Saidenberg-Kermanac’h, N., & Falgarone, G. (2012). Rheumatoid arthritis: from autoimmunity to synovitis and joint destruction. Journal of Autoimmunity, 39(3), 222-228.
Bouwens, M., Rest, O. V. D., Dellschaft, N., Bromhaar, M. G., Groot, L. C. P. G. M., Geleijnse, J. M., Müller, M., & Afman, L. A. (2009). Fish-oil supplementation induces antiinflammatory gene expression. American Journal of Clinical Nutrition, 90(2), 415-424.
Calder, P. C. (2006). Long-chain polyunsaturated fatty acids and inflammation. Scandinavian Journal of Food and Nutrition, 50, 54-61.
Calder, P. C. (2010). Omega-3 fatty acids and inflammatory processes. Nutrients, 2(3), 355-374.
Calder, P. C. (2014). Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance. Biochimica et Biophysica Acta, 851, 469-484.
Cascão, R., Rosário, H., Souto-Carneiro, M., & Fonseca, J. (2010). Neutrophils in rheumatoid arthritis: More than simple final effectors. Autoimmunity Reviews, 2010; 9(8), 531-535.
Dayer, J. M., & Choy, E. (2010). Therapeutic targets in rheumatoid arthritis: the interleukin-6 receptor. Rheumatology (Oxford). 49, 15–24.
DeCaterina, R., & Madonna, R. M. M. (2004). Effects of omega-3 fatty acids on cytokines and adhesion molecules. Current Atherosclerosis Reports, 6, 485-491.
El-Sayyad, S. M., Ali, M. A., Kandil, L. S., Ragab, G. M., & Abdelhamid Ibrahim, S. S. (2021). Metformin and omega-3 fish oil elicit anti-inflammatory effects via modulation of some dysregulated micro RNAs expression and signaling pathways in experimental induced arthritis. International Immunopharmacology, 2021, 92:107362. doi: 10.1016/j.intimp.2020.107362
Estevão-Silva, C. F., Ames, F. Q., Silva-Comar, F. M. S., Kummer, R., Tronco, R. P., Cuman, R. K. N., & Bersani-Amado, C. A. (2016). Fish oil and adjuvant-induced arthritis: inhibitory effect on leukocyte recruitment. Inflammation, 39(1), 320-326.
Ferrucci, L., Cherubini, A., Bandinelli, S., Bartali, B., Corsi, A., Lauretani, F., Martin, A., Andres-Lacueva, C., Senin, U., & Guralnik, J. M. (2006). Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers. Journal of Clinical Endocrinology & Metabolism, 91(2), 439-446.
Giudetti, A. M., & Cagnazzo, R. (2012). Beneficial effects of n-3 PUFA on chronic airway inflammatory diseases. Prostaglandins Other Lipid Mediators, 99, 57-67.
Hansen, R. A.,. Harris, M. A., Pluhar, E., Motta, T., Brevard, S., Ogilvie, G., Fettman, M. J., & Allen, K. G. D. (2008). Fish oil decreases matrix metalloproteinases in knee synovia of dogs with inflammatory joint disease. Journal of Nutritional Biochemistry, 19(2), 101-108.
He, Z., Kwek, E., & Chen, Z. Y. (2020). Lipids and Arthritis, The Chinese University of Hong Kong, Hong Kong, China Bailey’s Industrial Oil and Fat Products, 7th Edition, edited by Fereidoon Shahidi. Copyright©John Wiley & Sons, Ltd. doi:0.1002/047167849X.bio108
Ierna, M., Kerr, A., Scales, H., Berge, K., & Griinari, M. (2010). Supplementation of diet with krill oil protects against experimental rheumatoid arthritis. BMC Musculoskelet Disorders, 11, 136-146.
LaBranche, T. P., Jesson, M. I., Radi, Z., Storer, C.E., Guzova, J., Bonar, S. L., Thompson, J. M., Happa, F. A., Stewart, Z. S., Zhan, Y., Bollinger, C. S., Bansal, P. N., Wellen, J. W., Wilkie, D. P., Bailey, S. A, Symanowicz, P. T., Hegen, M., Head, R. D., Kishore, N., Mbalaviele, G., & Meyer, D. M. (2012). JAK inhibition with tofacitinib suppresses arthritic joint structural damage through decreased RANKL production. Arthritis & Rheumatology, 64(11), 3531-3542.
Lally, F., Smith, E., Filer, A., Stone, M. A., Shaw, S., Nash, G. B., Buckley, C. D, & Ed Rainger G. (2005). A novel mechanism of neutrophil recruitment in a coculture model of the rheumatoid synovium. Arthritis & Rheumatism, 52(11), 3460-3469.
Leslie, C., Conte, J., Hayes, K., & Cathcart, E. (1988). A fish oil diet reduces the severity of collagen induced arthritis after onset of the disease. Clinical and Experimental Immunology, 1988;73(2), 328-332.
Lima-Garcia, J., Dutra, R., Silva, K., Motta, E., Campos, M., & Calixto, J. B. (2011). The precursor of resolvin D series and aspirin-triggered resolvin D1 display anti-hyperalgesic properties in adjuvant-induced arthritis in rats. British Journal of Pharmacology, 164, 278-293.
Mattos, P., & Andrade, M. (2006). Ácidos graxos n-3 : um link entre eicosanóides, inflamação e imunidade. Mn-Metabólica, 8(3), 135-143. Mcinnes, B., Schett, G. (2011). The pathogenesis of rheumatoid arthritis. New England Journal of Medicine, 365: 2205-2221.
Mcinnes, B., & Schett, G. (2011). The pathogenesis of rheumatoid arthritis. New England Journal of Medicine, 365: 2205-2221.
Miles, E., & Calder, P. C. (2012). Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. British Journal of Nutrition, 107, S171-84.
Mingomataj, E., & Bakiri, A. (2016). Regulator Versus Effector Paradigm: Interleukin-10 as indicator of the switching response. Clinical Reviews in Allergy & Immunology, 50(1), 97-113.
Mori, T, Watts, G., Burke, V., Hilme, E., Puddey, I., & Beilin, L. (2000). Differential effects of eicosapentaenoic acid and docosahexaenoic acid on vascular reactivity of the forearm microcirculation. Circulation, 102, 1264-1269.
Nakagawa, S., Arai, Y., Mazda, O., Kishida, T., Takahashi, K., Sakao, K., Saito, M., Honjo, K., Imanishi, J., & Kubo, T. (2010). N-acetylcysteine prevents nitric oxide-induced chondrocyte apoptosis and cartilage degeneration in an experimental model of osteoarthritis. Journal of Orthopaedic Research, 28, 156-163.
Nobre, M. E. P., Correia, A. O., Borges, M. B., Sampaio, T. M. A., Chakraborty, S. A., Gonçalves, D; O., Brito. G; A, Almeida, L. K., Felipe, C. F. B., Lucetti, D. L., Arida, R. M., & Viana, G. S. B. (2013). Eicosapentaenoic acid and docosahexaenoic acid exert anti-inflammatory and antinociceptive effects in rodents at low doses. Nutrition Research, 33(5), 422-433.
Nohe, B., Johannes, T., & Dieterich, H. (2003). Antiinflammatory effects of omega-3 fatty acids vary at different stages of inflammation. American Journal of Physiology-Heart and Circulatory Physiology, 285, 2248-2250.
Pal, R., Chaudhary, M., Tiwari, P., Babu, S., & Pant, K. (2015). Protective role of theophylline and their interaction with nitric oxide (NO) in adjuvant-induced rheumatoid arthritis in rats. International Immunopharmacology, 29(2), 854-862.
Paleolog, E. (2002). Angiogenesis in rheumatoid arthritis. Arthritis Research, 4, 81-90.
Penglis, P., Cleland, L., Demasi, M., Caughey, G., & James, M. (2000). Differential regulation of prostaglandin E 2 and thromboxane A 2 production in human monocytes: implications for the use of cyclooxygenase inhibitors. Journal of Immunology,165(3),1605-1611.
Rabe, B., Chalaris, A., May, U., Waetzig, G., Seegert, D., Williams, A., Jones, S. A., John, S. R., & Scheller, J. (2008). Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood, 111(3), 1021-1029.
Ritter, A. M. V., Hernandes, L., Rocha, B. A, Estevão-Silva, C. F., Wisniewski-Rebecca, E. S., Cezar, J. S., Caparroz-Assef, S. M., Cuman, R. K. N., & Bersani-Amado, C. A. (2017). Anethole reduces inflammation and joint damage in rats with adjuvant-induced arhritis. Inflammation Research, 66, 725-737.
Rosenthale, M. E. (1970). A comparative study of the Lewis and Sprague Dawly rat in adjuvant arthritis. Arch Int Pharmacodyn et Therapie, 188(1), 14-22.
Sakata, S., Hayashi, S., Fujishiro, T., Kawakita, K., Kanzaki, N., Hashimoto, S., Iwasa, K., Chinzei, N., Kihara, S., Haneda, M., Ueha, T., Nishiyama, T., Kuroda, R., & Kurosaka, M. (2015). Oxidative stress-induced apoptosis and matrix loss of chondrocytes is inhibited by eicosapentaenoic acid. Journal of Orthopaedic Research, 33, 359-365.
Smolen, J., & Steiner, G. (2003). Therapeutic strategies for rheumatoid arthritis. Nature Reviews Drug Discover, 2, 473-488.
Simopoulos, A. (2002). Omega-3 Fatty Acids in Inflammation and Autoimmune Diseases. Journal of the American College of Nutrition, 21(6), 495-505.
Volker, D. H., Fitzgerald, P. E. B., & Garg, M. L. (2000). The eicosapentaenoic to ocosdahexaenoic acid ratio of diets affects the pathogenesis of arthritis in Lew/SSN rats. Journal of Nutrition, 130(3), 559-565.
Watson, H., Mitra, S., Croden, F. C., Taylor, M., Wood, H. M., Perry, S. L., Spencer, J. A., Quirke, P., Toogood, G. J., Lawton, C. L, Dye, L., Loadman, P. M., & Hull, M. A. (2018). A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut, 67(11), 1974-1983.
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Copyright (c) 2021 Camila Fernanda Estevão-Silva ; Alessandra Mileni Versuti Ritter; Franciele Queiroz Ames; Bruno Ambrósio da Rocha; Jurandir Fernando Comar ; Edirlene Sara Wisniewski-Rebecca; Silvana Martins Caparroz-Assef; Roberto Kenji Nakamura Cuman; Luzmarina Hernandes; Ciomar Aparecida Bersani-Amado
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