Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-15T01:30:14.747Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of dietary fish oil on selected inflammatory markers in pigs

Published online by Cambridge University Press:  18 January 2018

T. Komprda ,
P. Ondráčková ,
M. Vícenová ,
V. Rozíková ,
N. Procházková ,
L. Levá  and
M. Faldyna
T. Komprda*
Affiliation:
Department of Food Technology, Mendel University in Brno, Zemědělská 1, 613 00 Brno, Czech Republic
P. Ondráčková
Affiliation:
Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic
M. Vícenová
Affiliation:
Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic
V. Rozíková
Affiliation:
Department of Food Technology, Mendel University in Brno, Zemědělská 1, 613 00 Brno, Czech Republic
N. Procházková
Affiliation:
Department of Food Technology, Mendel University in Brno, Zemědělská 1, 613 00 Brno, Czech Republic
L. Levá
Affiliation:
Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic
M. Faldyna
Affiliation:
Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic
*
†E-mail: [email protected]
Get access

Abstract

The present study tested a hypothesis that dietary fish oil (eicosapentaenoic acid+docosahexaenoic acid) in a commonly achievable dose ameliorates a systemic inflammation in pigs. Two groups of pigs of 16 animals each were fed a diet with either 2.5% of fish oil (F) or a control diet with 2.5% of palm oil (P). After 70 days of fattening, eight F and eight P pigs were challenged (F+; P+) i.v. by lipopolysaccharide. After 3 h, all pigs were sacrificed and blood, liver and visceral adipose tissue (VAT) samples were taken. No significant effect (P>0.05) of dietary oil on the feed intake and daily weight gain was found out. Less neutrophils (16.8% v. 28.8%; P<0.05) were found in the F+-leukocytes of the peripheral blood; F+ pigs had lower (P<0.05) percentage of the swine leukocyte antigen-D-related CD163+ (SLA-DR+ CD163+) macrophages in the VAT (15.4% v. 21.8%) and lower expression of the SLA-DR-CD163+ surface molecules of the VAT macrophages. No difference (P>0.05) between F+ and P+ pigs in the peroxisome proliferator-activated receptor γ, GPR120, Adipor1 and Adipor2 (adiponectin receptor) gene expression, respectively, was established; plasma adiponectin was the same (21.1 ng/ml) in F+ and P+ pigs. In comparison with the P+ pigs, increased expression of the lipopolysaccharide-binding protein (LBP) gene and intercellular adhesion molecule 1 (ICAM1) gene was found out in the liver of the F+ pigs; expression of the tumor necrosis factor α (TNFα) gene was higher in the liver but lower in the VAT of the F+ pigs (P<0.05). The F+ pigs had higher (P<0.05) plasma concentration of both anti-inflammatory cytokine interleukin-4 (0.46 v. 0.04 ng/ml) and pro-inflammatory TNF-α (13.41 v. 7.72 ng/ml). It was concluded that dietary fish oil at the tested amount had a negligible effect on expression of the evaluated receptor genes and plasma adiponectin, and had an ambiguous effect on expression of cytokine genes and plasma cytokine levels.

Keywords

polyunsaturated fatty acids n-3neutrophilsadiponectininter-cellular adhesion molecule 1cytokines
Type
Research Article
Information
animal , Volume 12 , Issue 10 , October 2018 , pp. 2098 - 2107
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Chen, Y-J, Chen, C-C, Li, T-K, Wang, P-H, Liu, L-R, Chang, F-Y, Wang, Y-C, Yu, Y-H, Lin, S-P, Mersmann, HJ and Ding, ST 2012. Docosahexaenoic acid suppresses the expression of FoxO and its target genes. Journal of Nutritional Biochemistry 23, 1609–1616.Google Scholar
Cormier, H, Rudkowska, I, Lemieux, S, Couture, P and Vohl, M-C 2016. Expression and sequence variants of inflammatory genes; effects in plasma inflammation biomarkers following a 6-week supplementation with fish oil. International Journal of Molecular Sciences 17, 375.Google Scholar
Cranmer-Byng, MM, Liddle, DM, De Boer, AA, Monk, JM and Robinson, LE 2015. Proinflammatory effects of arachidonic acid in a lipopolysaccharide-induced inflammatory microenvironment in 3T3-L1 adipocytes in vitro. Applied Physiology Nutrition and Metabolism 40, 142–154.Google Scholar
Das, U 2006. Essential fatty acids – a review. Current Pharmaceutical Biotechnology 7, 467–482.Google Scholar
De Boer, AA, Monk, JM and Robinson, LE 2014. Docosahexaenoic acid decreases pro-inflammatory mediators in an in vitro murine adipocyte macrophage co-culture model. PLoS One 9, e85037.Google Scholar
Duan, Y, Li, F, Li, L, Fan, J, Sun, X and Yin, Y 2014. n-6:n-3 PUFA ratio is involved in regulating lipid metabolism and inflammation in pigs. British Journal of Nutrition 111, 445–451.Google Scholar
Feng, ZM, Guo, JP, Kong, XF, Wang, WC, Li, FN, Nyachoti, M and Yin, YL 2012. Molecular cloning and expression profiling of G protein coupled receptor 120 in Landrace pig and different Chinese indigenous pig breeds. Journal of Food Agriculture & Environment 10, 809–814.Google Scholar
Flock, MR, Rogers, CJ, Sandeep Prabhu, K and Kris-Etherton, PM 2013. Immunometabolic role of long-chain omega-3 fatty acids in obesity-induced inflammation. Diabetes/Metabolism Research and Reviews 29, 431–445.Google Scholar
Frikke-Schmidt, H, OʼRourke, RW, Lumeng, CN, Sandoval, DA and Seelej, RJ 2016. Does bariatric surgery improve adipose tissue function? Obesity Reviews 17, 795–809.Google Scholar
Fritsche, K, Irons, R, Pompos, L, Janes, J, Zheng, Y and Brown, C 2005. Omega-3 polyunsaturated fatty acid impairment of early host resistance against Listeria monocytogenes infection is independent of neutrophil infiltration and function. Cellular Immunology 235, 65–71.Google Scholar
Gessner, DK, Gröne, B, Couturier, A, Rosenbaum, S, Hillen, S, Becker, S, Erhardt, G, Reiner, G, Ringseis, R and Eder, K 2015. Dietary fish oil inhibits pro-inflammatory and ER stress signaling pathways in the liver of sows during lactation. PLoS One 10, e0137684.Google Scholar
Guo, J, Liu, Z, Sun, H, Huang, Y, Albrecht, E, Zhao, R and Yang, X 2015. Lipopolysaccharide challenge significantly influences lipid metabolism and proteome of white adipose tissue in growing pigs. Lipids in Health and Disease 14, 68.Google Scholar
Gurzell, EA, Teague, H, Duriancik, D, Clinthorne, J, Harris, M, Shaikh, SR and Fenton, JI 2015. Marine fish oils are not equivalent with respect to B-cell membrane organization and activation. Journal of Nutritional Biochemistry 26, 369–377.Google Scholar
Hall, JCE, Priestley, JV, Perry, VH and Michael-Titus, AT 2012. Docosahexaenoic acid, but not eicosapentaenoic acid, reduces the early inflammatory response following compression spinal cord injury in the rat. Journal of Neurochemistry 121, 738–750.Google Scholar
Helmer, KS, Cui, Y, Chang, L, Dewan, A and Mercer, DW 2003. Effects of ketamine/xylazine on expression of tumor necrosis factor-α, inducible nitric oxide synthase, and cyclo- oxygenase-2 in rat gastric mucosa during endotoxemia. Shock 20, 63–69.Google Scholar
Howe, PRC, Buckley, JD, Murphy, KJ, Pettman, T, Milte, C and Coates, AM 2014. Relationship between erythrocyte omega-3 content and obesity is gender dependent. Nutrients 6, 1850–1860.Google Scholar
Khiaosa-ard, R, Chungsiriwat, P, Chommanart, N, Kreuzer, M and Jaturasitha, S 2011. Enrichment with n-3 fatty acid by tuna oil feeding of pigs: changes in composition and properties of bacon and different sausages as affected by the supplementation period. Canadian Journal of Animal Science 91, 87–95.Google Scholar
Komprda, T 2012. Eicosapentaenoic and docosahexaenoic acid as inflammation-modulating and lipid homeostasis influencing nutraceuticals: a review. Journal of Functional Foods 4, 25–38.Google Scholar
Komprda, T, Zorníková, G, Rozíková, V, Borkovcová, M and Przywarová, A 2013. The effect of dietary Salvia hispanica seed on the content of n-3 long-chain polyunsaturated fatty acids in tissues of selected animal species, including edible insects. Journal of Food Composition and Analysis 32, 36–43.Google Scholar
Lai, CH, Yin, JD, Li, DF, Zhao, LD, Qiao, SY and Xing, JJ 2005. Conjugated linoleic acid attenuates the production and gene expression of proinflammatory cytokines in weaned pigs challenged with lipopolysacharide. Journal of Nutrition 135, 239–244.Google Scholar
Liu, YH, Li, XY, Chen, CY, Zhang, HM and Kang, JX 2015. Omega-3 fatty acid intervention supresses lipopolysacharide-induced inflammation and weight loss in mice. Marine Drugs 13, 1026–1036.Google Scholar
Liu, YL, Gong, LM, Li, DF, Feng, ZY, Zhao, LD and Dong, T 2003. Effects of fish oil on lymphocyte proliferation, cytokine production and intracellular signalling in weanling pigs. Archives of Animal Nutrition-Archiv für Tierernährung 57, 151–165.Google Scholar
Liu, YL, Shi, JX, Lu, J, Meng, GQ, Zhu, HI, Hou, YQ, Yin, YL, Zhao, SJ and Ding, BY 2009. Activation of peroxisome proliferator-activated receptor γ potentiates pro-inflammatory cytokine production, and adrenal and somatotropin changes of weaned pigs after Escherichia coli lipopolysaccharide challenge. Innate Immunity 15, 169–178.Google Scholar
Long, Q, Lei, T, Feng, B, Yin, C, Jin, D, Wu, Y, Zhu, X, Chen, X, Gan, L and Yang, Z 2010. Peroxisome proliferator-activated receptor-γ increases adiponectin secretion via transcriptional repression of endoplasmic reticulum chaperone protein ERp44. Endocrinology 151, 3195–3203.Google Scholar
Luci, S, König, B, Giemsa, B, Huber, S, Hause, G, Kluge, H, Stangl, GI and Eder, K 2007. Feeding of a deep-fried fat causes PPARγ activation in the liver of pigs as a non-proliferating species. British Journal of Nutrition 97, 872–882.Google Scholar
Mason, RP, Jacob, RF, Shrivastava, S, Sherratt, SCR and Chattopadhyay, A 2016. Eicosapentaenoic acid reduces membrane fluidity, inhibits cholesterol domain formation, and normalizes bilayer width in atherosclerotic-like model membranes. Biochimica et Biophysica Acta 1858, 3131–3140.Google Scholar
Morel, PCH, Leong, J, Nuijten, WGM, Purchas, RW and Wilkinson, BHP 2013. Effect of lipid type on growth performance, meat quality and the content of long chain n-3 fatty acids in pork meat. Meat Science 95, 151–159.Google Scholar
Oliver, E, McGillicudy, F, Phillips, C, Toomey, S and Roche, HM 2010. The role of inflammation and macrophage accumulation in development of the obesity-induced type 2 diabetes mellitus and the possible therapeutic effects of long-chain n-3 PUFA. Proceedings of the Nutrition Society 69, 232–243.Google Scholar
Ondrackova, P, Leva, L, Kucerova, Z, Vicenova, M, Mensikova, M and Faldyna, M 2013. Distribution of porcine monocytes in different lymphoid tissues and the lungs during experimental Actinobacillus pleuropleumoniae infection and the role of chemokines. Veterinary Research 44, 98.Google Scholar
Orr, JS, Kennedy, AJ and Hasty, AH 2013. Isolation of adipose tissue immune cells. Journal of Visualized Experiments 75, e50707.Google Scholar
Paschoal, VA, Vinolo, MAR, Crisma, AR, Magdalon, J and Curi, R 2013. Eicosapentaenoic (EPA) and docosahexaenoic (DHA) acid differentially modulate rat neutrophil function in vitro . Lipids 48, 93–103.Google Scholar
Petursdottir, DH and Hardardottir, I 2007. Dietary fish oil increases the number of splenic macrophages secreting TNF-α and IL-10 but decreases the secretion of these cytokines by splenic T cells from mice. Journal of Nutrition 137, 665–670.Google Scholar
Puglisi, MJ, Hasty, AH and Saraswathi, V 2011. The role of adipose tissue in mediating the beneficial effects of dietary fish oil. Journal of Nutritional Biochemistry 22, 101–108.Google Scholar
Romacho, T, Glosse, P, Richter, I, Elsen, M, Schoemaker, MH, van Tol, EA and Eckel, J 2015. Nutritional ingredients modulate adipokine secretion and inflammation in human primary adipocytes. Nutrients 7, 865–886.Google Scholar
Schmitz, G and Ecker, J 2008. The opposing effects of n-3 and n-6 fatty acids. Progress in Lipid Research 47, 147–155.Google Scholar
Schmittgen, TD and Livak, KJ 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.Google Scholar
Sierra, S, Lara-Villoslada, F, Comalada, M, Olivares, M and Xaus, J 2006. Dietary fish oil n-3 fatty acids increase regulatory cytokine production and exert anti-inflammatory effects in two murine models of inflammation. Lipids 41, 1115–1125.Google Scholar
Siriwardhana, N, Kalupahana, NS, Cekanova, M, LeMieux, M, Greer, B and Moustaid-Moussa, N 2013. Modulation of adipose tissue inflammation by bioactive food compounds. Journal of Nutritional Biochemistry 24, 613–623.Google Scholar
Smit, MN, Patterson, JL, Webel, SK, Spencer, JD, Cameron, AC, Dyck, MK, Dixon, WT and Foxcroft, GR 2013. Responses to n-3 fatty acid (LCPUFA) supplementation of gestating gilts, and lactating and weaned sows. Animal 7, 784–792.Google Scholar
Smits, RJ, Luxford, BG, Mitchell, M and Nottle, MB 2011. Sow litter size is increased in the subsequent parity when lactating sows are fed diets containing n-3 fatty acids from fish oil. Journal of Animal Science 89, 2731–2738.Google Scholar
Sundaram, S, Bukowski, MR, Lie, W-R, Picklo, MJ and Yan, L 2016. High-fat diets containing different amounts of n3 and n6 polyunsaturated fatty acids modulate inflammatory cytokine production in mice. Lipids 51, 571–582.Google Scholar
Tewari, N, Awad, S, Macdonald, IA and Lobo, DN 2015. Obesity-related insulin resistance: implication for the surgical patient. International Journal of Obesity 39, 1575–1588.Google Scholar
Upadhaya, SD, Kim, JC, Mullan, BP, Pluske, JR and Kim, IH 2015. Vitamin E and omega-3 fatty acids independently attenuate plasma concentrations of proinflammatory cytokines and prostaglandin E2 in Escherichia coli lipopolysaccharide-challenged growing-finishing pigs. Journal of Animal Science 93, 2926–2934.Google Scholar
Vaisman, N, Zaruk, Y, Shirazi, I, Kaysar, N and Barak, V 2005. The effect of fish oil supplementation on cytokine production in children. European Cytokine Network 16, 194–198.Google Scholar
Vigerust, NF, Bjørndal, B, Bohov, P, Brattelid, T, Svardal, A and Berge, RK 2013. Krill oil versus fish oil in modulation of inflammation and lipid metabolism in mice transgenic for TNF-α. European Journal of Nutrition 52, 1315–1325.Google Scholar
Yates, CM, Calder, PC and Rainger, GE 2014. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacology & Therapeutics 141, 272–282.Google Scholar
Zhu, H, Liu, Y, Chen, S, Wang, X, Pi, D, Leng, W, Chen, F, Zhang, J and Kang, P 2016. Fish oil enhances intestinal barrier function and inhibits corticotrophin-releasing hormone receptor 1 signalling pathway in weaned pigs after lipopolysaccharide challenge. British Journal of Nutrition 115, 1947–1957.Google Scholar
Supplementary material: File

Komprda et al. supplementary material

Tables S1-S2

Download Komprda et al. supplementary material(File)
File 26.9 KB