Impact of Omega-3 Fatty Acids on the Gut Microbiota
Abstract
:1. Introduction
2. Omega-3 Influence on Human Gut Microbiota: State of the Art
3. Gut Microbiota; Inflammation; and Omega-3
4. Gut Microbiota, Behavioral Disorders, and Omega-3
5. Conclusions
Conflicts of Interest
References
- Qin, J.; Li, R.; Raes, J.; Arumugam, M.; Burgdorf, K.S.; Manichanh, C.; Nielsen, T.; Pons, N.; Levenez, F.; Yamada, T.; et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464, 59–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486, 207–214. [Google Scholar] [Green Version]
- Power, S.E.; O’Toole, P.W.; Stanton, C.; Ross, R.P.; Fitzgerald, G.F. Intestinal microbiota, diet and health. Br. J. Nutr. 2014, 111, 387–402. [Google Scholar] [CrossRef] [PubMed]
- Flint, H.J.; Scott, K.P.; Duncan, S.H.; Louis, P.; Forano, E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012, 3, 289–306. [Google Scholar] [CrossRef] [PubMed]
- Flint, H.J.; Duncan, S.H.; Louis, P. The impact of nutrition on intestinal bacterial communities. Curr. Opin. Microbiol. 2017, 38, 59–65. [Google Scholar] [CrossRef] [PubMed]
- Bagga, D.; Wang, L.; Farias-Eisner, R.; Glaspy, J.A.; Reddy, S.T. Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proc. Natl. Acad. Sci. USA 2003, 100, 1751–1756. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, Y.; Tatsuno, I. Omega-3 polyunsaturated fatty acids for cardiovascular diseases: Present, past and future. Expert Rev. Clin. Pharmacol. 2017, 10, 865–873. [Google Scholar] [CrossRef] [PubMed]
- Miles, E.A.; Calder, P.C. Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. Br. J. Nutr. 2012, 107 (Suppl. S2), S171–S184. [Google Scholar] [CrossRef] [PubMed]
- Calder, P.C. Fatty acids and immune function: Relevance to inflammatory bowel diseases. Int. Rev. Immunol. 2009, 28, 506–534. [Google Scholar] [CrossRef] [PubMed]
- Arnold, L.E.; Young, A.S.; Belury, M.A.; Cole, R.M.; Gracious, B.; Seidenfeld, A.M.; Wolfson, H.; Fristad, M.A. Omega-3 fatty acids plasma levels before and after supplementation: Correlation with mood and clinical outcomes in the omega-3 and therapy studies. J. Child Adolesc. Psychopharmacol. 2017, 27, 223–233. [Google Scholar] [CrossRef] [PubMed]
- Merendino, N.; Costantini, L.; Manzi, L.; Molinari, R.; D’Eliseo, D.; Velotti, F. Dietary omega ω-3 polyunsaturated fatty acid DHA: A potential adjuvant in the treatment of cancer. Biomed. Res. Int. 2013, 310186. [Google Scholar] [CrossRef]
- Rajkumar, H.; Mahmood, N.; Kumar, M.; Varikuti, S.R.; Challa, H.R.; Myakala, S.P. Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: A randomized, controlled trial. Mediat. Inflamm. 2014, 2014, 348959. [Google Scholar] [CrossRef]
- 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.; et al. A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut 2017. [Google Scholar] [CrossRef] [PubMed]
- Louis, P.; Flint, H.J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 2017, 19, 29–41. [Google Scholar] [CrossRef] [PubMed]
- Sun, M.; Wu, W.; Liu, Z.; Cong, Y. Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J. Gastroenterol. 2017, 52, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Pu, S.; Khazanehei, H.; Jones, P.J.; Khafipour, E. Interactions between obesity status and dietary intake of monounsaturated and polyunsaturated oils on human gut microbiome profiles in the canol oil multicentre intervention trial (COMIT). Front. Microbiol. 2016, 7, 1612. [Google Scholar] [CrossRef] [PubMed]
- Yokota, A.; Fukiya, S.; Islam, K.B.; Ooka, T.; Ogura, Y.; Hayashi, T. Is bile acid a determination of the gut microbiota on a high-fat diet? Gut Microbes 2012, 3, 455–459. [Google Scholar] [CrossRef] [PubMed]
- Balfego, M.; Canivell, S.; Hanzu, F.A.; Sala-Vila, A.; Martinez-Medina, M.; Murillo, S.; Mur, T.; Ruano, E.G.; Linares, F.; Porras, N.; et al. Effects of sardine-enriched diet on metabolic control, inflammation and gut microbiota in drug-naive patients with type 2 diabetes: A pilot randomized trial. Lipids Health Dis. 2016, 15, 78. [Google Scholar] [CrossRef] [PubMed]
- Noriega, B.S.; Sanchez-Gonzalez, M.A.; Salyakina, D.; Coffman, J. Understanding the Impact of Omega-3 Rich Diet on the Gut Microbiota. Case Rep. Med. 2016, 2016, 3089303. [Google Scholar] [CrossRef] [PubMed]
- Menni, C.; Zierer, J.; Pallister, T.; Jackson, M.A.; Long, T.; Mohney, R.P.; Steves, C.J.; Spector, T.D.; Valdes, A.M. Omega-3 fatty acids correlate with gut microbiome diversity and production of N-carbamylglutamate in middle aged and elderly women. Sci. Rep. 2017, 7, 11079. [Google Scholar] [CrossRef] [PubMed]
- Santoru, M.L.; Piras, C.; Murgia, A.; Palmas, V.; Camboni, T.; Liggi, S.; Ibba, I.; Lai, M.A.; Orru, S.; Loizedda, A.L.; et al. Cross sectional evaluation of the gut-microbiome metabolome axis in an Italian cohort of IBD patients. Sci. Rep. 2017, 7, 9523. [Google Scholar] [CrossRef] [PubMed]
- Collado, M.C.; Rautava, S.; Aakko, J.; Isolauri, E.; Salminen, S. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci. Rep. 2016, 6, 23129. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, S.; Nielsen, D.S.; Lauritzen, L.; Jakobsen, M.; Michaelsen, K.F. Impact of diet on the intestinal microbiota in 10-month-old infants. J. Pediatr. Gastroenterol. Nutr. 2007, 44, 613–618. [Google Scholar] [CrossRef] [PubMed]
- Andersen, A.D.; Molbak, L.; Michaelsen, K.F.; Lauritzen, L. Molecular fingerprints of the human fecal microbiota from 9 to 18 months old and the effect of fish oil supplementation. J. Pediatr. Gastroenterol. Nutr. 2011, 53, 303–309. [Google Scholar] [CrossRef] [PubMed]
- Younge, N.; Yang, Q.; Seed, P.C. Enteral High Fat-Polyunsaturated Fatty Acid Blend Alters the Pathogen Composition of the Intestinal Microbiome in Premature Infants with an Enterostomy. J. Pediatr. 2017, 181, 93–101.e6. [Google Scholar] [CrossRef] [PubMed]
- Chu, D.M.; Antony, K.M.; Ma, J.; Prince, A.L.; Showalter, L.; Moller, M.; Aagaard, K.M. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med. 2016, 8, 77. [Google Scholar] [CrossRef] [PubMed]
- Honda, K.; Littman, D.R. The microbiota in adaptive immune homeostasis and disease. Nature 2016, 535, 75–84. [Google Scholar] [CrossRef] [PubMed]
- Sanz, Y.; De Palma, G. Gut microbiota and probiotics in modulation of epithelium and gut-associated lymphoid tissue function. Int. Rev. Immunol. 2009, 28, 397–413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Round, J.L.; Mazmanian, S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9, 313–323. [Google Scholar] [CrossRef] [PubMed]
- Rivollier, A.; He, J.; Kole, A.; Valatas, V.; Kelsall, B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from anti-inflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 2012, 209, 139–155. [Google Scholar] [CrossRef] [PubMed]
- Ohnmacht, C.; Park, J.H.; Cording, S.; Wing, J.B.; Atarashi, K.; Obata, Y.; Gaboriau-Routhiau, V.; Marques, R.; Dulauroy, S.; Fedoseeva, M.; et al. The microbiota regulates type 2 immunity through RORγt(+) T cells. Science 2015, 349, 989–993. [Google Scholar] [CrossRef] [PubMed]
- Ghoshal, S.; Witta, J.; Zhong, J.; de Villiers, W.; Eckhardt, E. Chylomicrons promote intestinal absorption of lipopolysaccharides. J. Lipid Res. 2009, 50, 90–97. [Google Scholar] [CrossRef] [PubMed]
- Komaroff, A.L. The Microbiome and Risk for Obesity and Diabetes. JAMA 2017, 317, 355–356. [Google Scholar] [CrossRef] [PubMed]
- Bruzzese, E.; Callegari, M.L.; Raia, V.; Viscovo, S.; Scotto, R.; Ferrari, S.; Morelli, L.; Buccigrossi, V.; Lo Vecchio, A.; Ruberto, E.; et al. Disrupted intestinal microbiota and intestinal inflammation in children with cystic fibrosis and its restoration with Lactobacillus GG: A randomised clinical trial. PLoS ONE 2014, 9, e87796. [Google Scholar] [CrossRef] [PubMed]
- Berer, K.; Mues, M.; Koutrolos, M.; Rasbi, Z.A.; Boziki, M.; Johner, C.; Wekerle, H.; Krishnamoorthy, G. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011, 479, 538–541. [Google Scholar] [CrossRef] [PubMed]
- Britton, R.A.; Irwin, R.; Quach, D.; Schaefer, L.; Zhang, J.; Lee, T.; Parameswaran, N.; McCabe, L.R. Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J. Cell. Physiol. 2014, 229, 1822–1830. [Google Scholar] [CrossRef] [PubMed]
- Vieira, A.T.; Macia, L.; Galvao, I.; Martins, F.S.; Canesso, M.C.; Amaral, F.A.; Garcia, C.C.; Maslowski, K.M.; de Leon, E.; Shim, D.; et al. A Role for Gut Microbiota and the Metabolite-Sensing Receptor GPR43 in a Murine Model of Gout. Arthritis Rheumatol. 2015, 67, 1646–1656. [Google Scholar] [CrossRef] [PubMed]
- Hildebrandt, M.A.; Hoffmann, C.; Sherrill-Mix, S.A.; Keilbaugh, S.A.; Hamady, M.; Chen, Y.Y.; Knight, R.; Ahima, R.S.; Bushman, F.; Wu, G.D. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 2009, 137, 1716–1724. [Google Scholar] [CrossRef] [PubMed]
- Graham, C.; Mullen, A.; Whelan, K. Obesity and the gastrointestinal microbiota: A review of associations and mechanisms. Nutr. Rev. 2015, 73, 376–385. [Google Scholar] [CrossRef] [PubMed]
- Zhang, C.; Zhang, M.; Wang, S.; Han, R.; Cao, Y.; Hua, W.; Mao, Y.; Zhang, X.; Pang, X.; Wei, C.; et al. Interaction between gut microbiota, host genetics and diet relevant to development of metabolic syndrome in mice. ISME J. 2010, 4, 232–241. [Google Scholar] [CrossRef] [PubMed]
- Devkota, S.; Wang, Y.; Musch, M.W.; Leone, V.; Fehlner-Peach, H.; Nadimpalli, A.; Antonopoulos, D.A.; Jabri, B.; Chang, E.B. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature 2012, 487, 104–108. [Google Scholar] [CrossRef] [PubMed]
- Moreira, A.P.; Texeira, T.F.; Ferreira, A.B.; Peluzio Mdo, C.; Alfenas Rde, C. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br. J. Nutr. 2012, 108, 801–809. [Google Scholar] [CrossRef] [PubMed]
- Ji, Y.; Sakata, Y.; Tso, P. Nutrient-induced inflammation in the intestine. Curr. Opin. Clin. Nutr. Metab. Care 2011, 14, 315–321. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Delzenne, N.M. The gut microbiome as therapeutic target. Pharmacol. Ther. 2011, 130, 202–212. [Google Scholar] [CrossRef] [PubMed]
- Laugerette, F.; Vors, C.; Geloen, A.; Chauvin, M.A.; Soulage, C.; Lambert-Porcheron, S.; Peretti, N.; Alligier, M.; Burcelin, R.; Laville, M.; et al. Emulsified lipids increase endotoxemia: Possible role in early postprandial low-grade inflammation. J. Nutr. Biochem. 2011, 22, 53–59. [Google Scholar] [CrossRef] [PubMed]
- Krajmalnik-Brown, R.; Ilhan, Z.E.; Kang, D.W.; DiBaise, J.K. Effects of gut microbes on nutrient absorption and energy regulation. Nutr. Clin. Pract. 2012, 27, 201–214. [Google Scholar] [CrossRef] [PubMed]
- Wu, H.; Tremaroli, V.; Backhed, F. Linking Microbiota to Human Diseases: A Systems Biology Perspective. Trends Endocrinol. Metab. 2015, 26, 758–770. [Google Scholar] [CrossRef] [PubMed]
- Patterson, E.; O’Doherty, R.M.; Murphy, E.F.; Wall, R.; O’Sullivan, O.; Nilaweera, K.; Fitzgerald, G.F.; Cotter, P.D.; Ross, R.P.; Stanton, C. Impact of dietary fatty acids on metabolic activity and host intestinal microbiota composition in C57BL/6J mice. Br. J. Nutr. 2014, 111, 1905–1917. [Google Scholar] [CrossRef] [PubMed]
- Candido, F.G.; Valente, F.X.; Grzeskowiak, L.M.; Moreira, A.P.B.; Rocha, D.M.U.P.; Alfenas, R.C.G. Impact of dietary fat on gut microbiota and low-grade systemic inflammation: Mechanism and clinical implication in obesity. Int. J. Food Sci. Nutr. 2017, 4, 1–19. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Pan, L.; Lu, J.; Li, N.; Li, J. N-3 PUFAs attenuate ischemia/reperfusion induced intestinal barrier injury by activating I-FABP-PPARγ pathway. Clin. Nutr. 2012, 31, 951–957. [Google Scholar] [CrossRef] [PubMed]
- Desbois, A.P.; Smith, V.J. Antibacterial free fatty acids: Activities, mechanisms of action and biotechnological potential. Appl. Microbiol. Biotechnol. 2010, 85, 1629–1642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kaliannan, K.; Wang, B.; Li, X.Y.; Kim, K.J.; Kang, J.X. A host-microbiome interaction mediates the opposing effects of omega-6 and omega-3 fatty acids on metabolic endotoxemia. Sci. Rep. 2015, 5, 11276. [Google Scholar] [CrossRef] [PubMed]
- Cani, P.D.; Neyrinck, A.M.; Fava, F.; Knauf, C.; Burcelin, R.G.; Tuohy, K.M.; Gibson, G.R.; Delzenne, N.M. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007, 50, 2374–2383. [Google Scholar] [CrossRef] [PubMed]
- Lam, Y.Y.; Ha, C.W.; Campbell, C.R.; Mitchell, A.J.; Dinudom, A.; Oscarsson, J.; Cook, D.I.; Hunt, N.H.; Caterson, I.D.; Holmes, A.J.; et al. Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS ONE 2012, 7, e34233. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.; Hougen, H.; Vollmer, A.C.; Hiebert, S.M. Gut bacteria profiles of Mus musculus at the phylum and family levels are influenced by saturation of dietary fatty acids. Anaerobe 2012, 18, 331–337. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.N.; Zhu, J.; Pan, W.S.; Shen, S.R.; Shan, W.G.; Das, U.N. Effects of fish oil with a high content of n-3 polyunsaturated fatty acids on mouse gut microbiota. Arch. Med. Res. 2014, 45, 195–202. [Google Scholar] [CrossRef] [PubMed]
- Caesar, R.; Tremaroli, V.; Kovatcheva-Datchary, P.; Cani, P.D.; Bäckhed, F. Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab. 2015, 22, 658–668. [Google Scholar] [CrossRef] [PubMed]
- David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mujico, J.R.; Baccan, G.C.; Gheorghe, A.; Díaz, L.E.; Marcos, A. Changes in gut microbiota due to supplemented fatty acids in diet-induced obese mice. Br. J. Nutr. 2013, 110, 711–720. [Google Scholar] [CrossRef] [PubMed]
- Myles, I.A.; Pincus, N.B.; Fontecilla, N.M.; Datta, S.K. Effects of parental omega-3 fatty acid intake on offspring microbiome and immunity. PLoS ONE 2014, 9, e87181. [Google Scholar] [CrossRef] [PubMed]
- Kankaanpaa, P.E.; Salminen, S.J.; Isolauri, E.; Lee, Y.K. The influence of polyunsaturated fatty acids on probiotic growth and adhesion. FEMS Microbiol. Lett. 2001, 194, 149–153. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, S.; DeCoffe, D.; Brown, K.; Rajendiran, E.; Estaki, M.; Dai, C.; Yip, A.; Gibson, D.L. Fish oil attenuates omega-6 polyunsaturated fatty acid-induced dysbiosis and infectious colitis but impairs LPS dephosphorylation activity causing sepsis. PLoS ONE 2013, 8, e55468. [Google Scholar] [CrossRef] [PubMed]
- Fasano, A.; Not, T.; Wang, W.; Uzzau, S.; Berti, I.; Tommasini, A.; Goldblum, S.E. Zonulin, a newly discovered modulator of intestinal permeability, and its expression in coeliac disease. Lancet 2000, 355, 1518–1519. [Google Scholar] [CrossRef]
- Liu, J.J.; Galfalvy, H.C.; Cooper, T.B.; Oquendo, M.A.; Grunebaum, M.F.; Mann, J.J.; Sublette, M.E. Omega-3 polyunsaturated fatty acid (PUFA) status in major depressive disorder with comorbid anxiety disorders. J. Clin. Psychiatry 2013, 74, 732–738. [Google Scholar] [CrossRef] [PubMed]
- Tripathi, A.; Lammers, K.M.; Goldblum, S.; Shea-Donohue, T.; Netzel-Arnett, S.; Buzza, M.S.; Antalis, T.M.; Vogel, S.N.; Zhao, A.; Yang, S.; et al. Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc. Natl. Acad. Sci. USA 2009, 106, 16799–16804. [Google Scholar] [CrossRef] [PubMed]
- Zak-Golab, A.; Kocelak, P.; Aptekorz, M.; Zientara, M.; Juszczyk, L.; Martirosian, G.; Chudek, J.; Olszanecka-Glinianowicz, M. Gut microbiota, microinflammation, metabolic profile, and zonulin concentration in obese and normal weight subjects. Int. J. Endocrinol. 2013, 2013, 674106. [Google Scholar] [CrossRef] [PubMed]
- Moreno-Navarrete, J.M.; Sabater, M.; Ortega, F.; Ricart, W.; Fernandez-Real, J.M. Circulating zonulin, a marker of intestinal permeability, is increased in association with obesity-associated insulin resistance. PLoS ONE 2012, 7, e37160. [Google Scholar] [CrossRef] [PubMed]
- Jayashree, B.; Bibin, Y.S.; Prabhu, D.; Shanthirani, C.S.; Gokulakrishnan, K.; Lakshmi, B.S.; Mohan, V.; Balasubramanyam, M. Increased circulatory levels of lipopolysaccharide (LPS) and zonulin signify novel biomarkers of proinflammation in patients with type 2 diabetes. Mol. Cell. Biochem. 2014, 388, 203–210. [Google Scholar] [CrossRef] [PubMed]
- Mokkala, K.; Roytio, H.; Munukka, E.; Pietila, S.; Ekblad, U.; Ronnemaa, T.; Eerola, E.; Laiho, A.; Laitinen, K. Gut Microbiota Richness and Composition and Dietary Intake of Overweight Pregnant Women Are Related to Serum Zonulin Concentration, a Marker for Intestinal Permeability. J. Nutr. 2016, 146, 1694–1700. [Google Scholar] [CrossRef] [PubMed]
- Kerr, C.A.; Grice, D.M.; Tran, C.D.; Bauer, D.C.; Li, D.; Hendry, P.; Hannan, G.N. Early life events influence whole-of-life metabolic health via gut microflora and gut permeability. Crit. Rev. Microbiol. 2015, 41, 326–340. [Google Scholar] [CrossRef] [PubMed]
- Persborn, M.; Soderholm, J.D. Commentary: The effects of probiotics on barrier function and mucosal pouch microbiota during maintenance treatment for severe pouchitis in patients with ulcerative colitis—Authors’ reply. Aliment. Pharmacol. Ther. 2013, 38, 1406–1407. [Google Scholar] [CrossRef] [PubMed]
- Egshatyan, L.; Kashtanova, D.; Popenko, A.; Tkacheva, O.; Tyakht, A.; Alexeev, D.; Karamnova, N.; Kostryukova, E.; Babenko, V.; Vakhitova, M.; et al. Gut microbiota and diet in patients with different glucose tolerance. Endocr. Connect. 2016, 5, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Zhang, Q.; Wang, M.; Zhao, S.; Xu, G.; Li, J. n-3 polyunsaturated fatty acids prevent disruption of epithelial barrier function induced by proinflammatory cytokines. Mol. Immunol. 2008, 45, 1356–1365. [Google Scholar] [CrossRef] [PubMed]
- Mani, V.; Hollis, J.H.; Gabler, N.K. Dietary oil composition differentially modulates intestinal endotoxin transport and postprandial endotoxemia. Nutr. Metab. 2013, 10, 6. [Google Scholar] [CrossRef] [PubMed]
- Nishikawa, J.; Kudo, T.; Sakata, S.; Benno, Y.; Sugiyama, T. Diversity of mucosa-associated microbiota in active and inactive ulcerative colitis. Scand. J. Gastroenterol. 2009, 44, 180–186. [Google Scholar] [CrossRef] [PubMed]
- Mondot, S.; Kang, S.; Furet, J.P.; Aguirre de Carcer, D.; McSweeney, C.; Morrison, M.; Marteau, P.; Dore, J.; Leclerc, M. Highlighting new phylogenetic specificities of Crohn’s disease microbiota. Inflamm. Bowel Dis. 2011, 17, 185–192. [Google Scholar] [CrossRef] [PubMed]
- Willing, B.P.; Dicksved, J.; Halfvarson, J.; Andersson, A.F.; Lucio, M.; Zheng, Z.; Jarnerot, G.; Tysk, C.; Jansson, J.K.; Engstrand, L. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 2010, 139, 1844–1854.e1. [Google Scholar] [CrossRef] [PubMed]
- Joossens, M.; Huys, G.; Cnockaert, M.; De Preter, V.; Verbeke, K.; Rutgeerts, P.; Vandamme, P.; Vermeire, S. Dysbiosis of the faecal microbiota in patients with Crohn’s disease and their unaffected relatives. Gut 2011, 60, 631–637. [Google Scholar] [CrossRef] [PubMed]
- David, R.-C.; Patricia, R.-M.; Margolles, A.; Gueimonde, M.; de Los Reyes-Gavilan, C.G.; Salazar, N. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 2016, 7, 185. [Google Scholar] [CrossRef]
- Silverberg, M.S.; Satsangi, J.; Ahmad, T.; Arnott, I.D.; Bernstein, C.N.; Brant, S.R.; Caprilli, R.; Colombel, J.F.; Gasche, C.; Geboes, K.; et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: Report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can. J. Gastroenterol. 2005, 19 (Suppl. A), 5A–36A. [Google Scholar] [CrossRef] [PubMed]
- Zheng, P.; Zeng, B.; Zhou, C.; Liu, M.; Fang, Z.; Xu, X.; Zeng, L.; Chen, J.; Fan, S.; Du, X.; et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol. Psychiatry 2016, 21, 786–796. [Google Scholar] [CrossRef] [PubMed]
- Desbonnet, L.; Clarke, G.; Shanahan, F.; Dinan, T.G.; Cryan, J. Microbiota is essential for social development in the mouse. Mol. Psychiatry 2014, 19, 146–148. [Google Scholar] [CrossRef] [PubMed]
- Leonard, B.; Maes, M. Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci. Biobehav. Rev. 2012, 36, 764–785. [Google Scholar] [CrossRef] [PubMed]
- O’Brien, S.M.; Scott, L.V.; Dinan, T.G. Cytokines: Abnormalities in major depression and implications for pharmacological treatment. Hum. Psychopharmacol. 2004, 19, 397–403. [Google Scholar] [CrossRef] [PubMed]
- Sampson, T.; Mazmanian, S.K. Control of Brain Development, Function, and Behavior by the Microbiome. Cell Host Microbe 2015, 17, 565–576. [Google Scholar] [CrossRef] [PubMed]
- Cryan, J.F.; Dinan, T.G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012, 13, 701–712. [Google Scholar] [CrossRef] [PubMed]
- Naseribafrouei, A.; Hestad, K.; Avershina, E.; Sekelja, M.; Linlokken, A.; Wilson, R.; Rudi, K. Correlation between the human fecal microbiota and depression. Neurogastroenterol. Motil. 2014, 26, 1155–1162. [Google Scholar] [CrossRef] [PubMed]
- Jiang, H.; Ling, Z.; Zhang, Y.; Mao, H.; Ma, Z.; Yin, Y.; Wang, W.; Tang, W.; Tan, Z.; Shi, J.; et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 2015, 48, 186–194. [Google Scholar] [CrossRef] [PubMed]
- Mulder, K.A.; King, D.J.; Innis, S.M. Omega-3 Fatty Acid Deficiency in Infants before Birth Identified Using a Randomized Trial of Maternal DHA Supplementation in Pregnancy. PLoS ONE 2014, 9, e83764. [Google Scholar] [CrossRef] [PubMed]
- Chalon, S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot. Essent. Fat. Acids 2006, 75, 259–269. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.F.; Su, H.M. Exposure to a maternal n-3 fatty acid-deficient diet during brain development provokes excessive hypothalamic-pituitary-adrenal axis responses to stress and behavioral indices of depression and anxiety in male rat offspring later in life. J. Nutr. Biochem. 2013, 24, 70–80. [Google Scholar] [CrossRef] [PubMed]
- Robertson, R.C.; Oriach, C.S.; Murphy, K.; Moloney, G.M.; Cryan, J.F.; Dinan, T.G.; Ross, R.P.; Stanton, C. Omega-3 polyunsaturated fatty acids critically regulate behaviour and gut microbiota development in adolescence and adulthood. Brain Behav. Immun. 2017, 59, 21–37. [Google Scholar] [CrossRef] [PubMed]
- Jory, J. Abnormal fatty acids in Canadian children with autism. Nutrition 2016, 32, 474–477. [Google Scholar] [CrossRef] [PubMed]
- Al-Farsi, Y.M.; Waly, M.I.; Deth, R.C.; Al-Sharbati, M.M.; Al-Shafaee, M.; Al-Farsi, O.; Al-Khaduri, M.M.; Al-Adawi, S.; Hodgson, N.W.; Gupta, I.; et al. Impact of nutrition on serum levels of docosahexaenoic acid among Omani children with autism. Nutrition 2013, 29, 1142–1146. [Google Scholar] [CrossRef] [PubMed]
- Lin, P.Y.; Huang, S.Y.; Su, K.P. A meta-analytic review of polyunsaturated fatty acid compositions in patients with depression. Biol. Psychiatry 2010, 68, 140–147. [Google Scholar] [CrossRef] [PubMed]
- Grosso, G.; Pajak, A.; Marventano, S.; Castellano, S.; Galvano, F.; Bucolo, C.; Drago, F.; Caraci, F. Omega-3 fatty acids and depression: Scientific evidence and biological mechanisms. Oxid. Med. Cell. Longev. 2014, 2014, 313570. [Google Scholar] [CrossRef] [PubMed]
- Jacka, F.N.; Pasco, J.A.; Williams, L.J.; Meyer, B.J.; Digger, R.; Berk, M. Dietary intake of fish and PUFA, and clinical depressive and anxiety disorders in women. Br. J. Nutr. 2013, 109, 2059–2066. [Google Scholar] [CrossRef] [PubMed]
- Amminger, G.P.; Berger, G.E.; Schafer, M.R.; Klier, C.; Friedrich, M.H.; Feucht, M. Omega-3 fatty acids supplementation in children with autism: A double-blind randomized, placebo-controlled pilot study. Biol. Psychiatry 2007, 61, 551–553. [Google Scholar] [CrossRef] [PubMed]
- Pusceddu, M.M.; El Aidy, S.; Crispie, F.; O’Sullivan, O.; Cotter, P.; Stanton, C.; Kelly, P.; Cryan, J.F.; Dinan, T.G. N-3 Polyunsaturated Fatty Acids (PUFAs) Reverse the Impact of Early-Life Stress on the Gut Microbiota. PLoS ONE 2015, 10, e0139721. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ganesh, B.P.; Klopfleisch, R.; Loh, G.; Blaut, M. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLoS ONE 2013, 8, e74963. [Google Scholar] [CrossRef] [PubMed]
- Frank, D.N.; St Amand, A.L.; Feldman, R.A.; Boedeker, E.C.; Harpaz, N.; Pace, N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007, 104, 13780–13785. [Google Scholar] [CrossRef] [PubMed]
- Campbell, E.L.; MacManus, C.F.; Kominsky, D.J.; Keely, S.; Glover, L.E.; Bowers, B.E.; Scully, M.; Bruyninckx, W.J.; Colgan, S.P. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. Proc. Natl. Acad. Sci. USA 2010, 107, 14298–14303. [Google Scholar] [CrossRef] [PubMed]
- Davis, D.J.; Hecht, P.M.; Jasarevic, E.; Beversdorf, D.Q.; Will, M.J.; Fritsche, K.; Gillespie, C.H. Sex-specific effects of docosahexaenoic acid (DHA) on the microbiome and behavior of socially-isolated mice. Brain Behav. Immun. 2017, 59, 38–48. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Christophersen, C.T.; Sorich, M.J.; Gerber, J.P.; Angley, M.T.; Conlon, M.A. Increased abundance of Sutterella spp. and Ruminococcus torques in feces of children with autism spectrum disorder. Mol. Autism 2013, 4, 42. [Google Scholar] [CrossRef] [PubMed]
Human Studies | Studied Population | Diets | Method | Main Outcomes |
---|---|---|---|---|
Rajkumar et al. (2014) [12] | 60 overweight healthy people | Commercial prebiotic, named VSL#3, vs. VSL#3 + 180 mg EPA and 120 mg of DHA for 6 weeks | Colony counting on anaerobic or aerobic selective media | No difference between groups. |
Watson et al. (2017) [13] | 20 middle-aged healthy individuals | 4 g of mixed DHA/EPA supplement (as capsules and functional drink) for 8 weeks | Sequencing by NGS (Illumina) of 16S rRNA gene, V4 region | No difference for Firmicutes/Bacteroidetes phyla ratio. Increases in the Clostridiaceae, Sutterellaceae, and Akkermansiaceae families in both experimental groups. Increased abundance of Bifidobacterium, Oscillospira, associated with a reduction of Coprococcus and Faecalibacterium genera in both experimental groups. Increased abundance of Lachnospira and Roseburia genera only in functional drink group. |
Pu et al. (2016) COMIT study [16] | 25 volunteers with risk of metabolic syndrome | 60 g of five different unsaturated oil blends for 30 days: conventional canola oil (35.17 g oleic acid), DHA-enriched high oleic canola oil (37.95 g oleic acid and 3.48 g DHA), high oleic canola oil (42.88 g oleic acid), a blend of 25:75 corn/safflower oil (41.61 g linolenic acid), and a blend of 60:40 flax/safflower (22.48 g linolenic acid and 19.19 g ALA) | Sequencing by pyrosequencing of 16S rRNA gene, V1–V3 regions | No difference between groups at phylum level. Highest level of Faecalibacterium genus in high oleic canola oil, and lowest in DHA-enriched high oleic canola oil. Conventional canola was correlated with Coprobacillus and Blautia genera, whereas canola/DHA was associated with the family Lachnospiraceae of the phylum Firmicutes. All the canola oils are correlated with Parabacteroidetes, Prevotella, and Turicibacter genera, and with Enterobacteriaceae family versus the PUFA-rich oils (i.e., corn/safflower and flax/safflower) correlated with the genus Isobaculum. |
Balfego et al. (2016) Pilchardus Study [18] | 32 patients diagnosed with type 2 diabetes | Standard diet for diabetes supplemented with 100 g of sardines 5 days a week for 6 months (n = 17) (~3 g of EPA + DHA) | qPCR on target bacterial indicators | Firmicutes/Bacteroidetes phyla ratio decrease, while Prevotella genus increase in the omega-3 group. |
Noriega et al. (2016) [19] | One healthy 45-year-old man | Daily supplementation of 600 mg of omega-3 PUFAs by fish protein diet, for 2 weeks | Sequencing by NGS (Ion Torrent) of 16S rRNA gene, V4 region | Increase of the phylum Firmicutes and a decrease of Bacteroidetes and Actinobacteria phyla. Reduction in Faecalibacterium genus versus an increase in Blautia, Roseburia, Coprococcus, Ruminococcus and Subdoligranulum genera. |
Menni et al. (2017) [20] | Cohort of 876 middle-aged and elderly women | DHA intake of 350 mg/day with a serum concentration of 0.14 mmol/L. (DHA dietary intake determined by Food Frequency Questionnaire) | Sequencing by NGS (Illumina) of 16S rRNA gene, V4 region | This intake is correlated with 21 OTUs belonging to Lachnospiraceae family, 7 OTUs to the Ruminococcaceae family, and 5 to the Bacteroidetes phylum. |
Nielsen et al. (2007) [23] | One hundred and fourteen 9-month-old infants | Cow’s milk or infant formula with or without 5 mL/day of fish oil until the 12th month | Fingerprint profiles generated by PCR-DGGE of 16S rRNA gene, V6-8 and V3 regions | Fish oil in cow’s milk groups has a differential fingerprint profile, and this difference was not found in infant formula groups. |
Andersen et al. (2011) [24] | One hundred and thirty-two 9-month-old infants | Daily supplementation of 5 mL fish oil (1.6 g EPA + DHA) or sunflower oil (3.1 g linolenic acid, omega-6) for 9 months | Fingerprint profiles generated by T-RFLP of 16S rRNA gene, whole gene | Fish oil gave significant changes in microbiota in comparison with sunflower oil, but only among children who had stopped breast-feeding before the study. |
Younge et al. (2017) [25] | 32 premature infants with enterostomy | Usual nutritional therapy and an enteral supplementation of a fish and safflower blend oil for a maximum of 10 weeks | Sequencing by NGS (Illumina) of 16S rRNA gene, V4 region | Lower abundance of some pathogenic bacteria as Streptococcus, Clostridium, Escherichia, Pantoea, Serratia, and Citrobacter genera. |
Studies | Studied Population | Diets | Main Outcomes |
---|---|---|---|
Hildebrandt et al. (2009) [38] | C57BL/6 and β resistin-like molecule β knockout mice | High-fat diet (45% fat) for 21 weeks | High fat diet caused changed in microbiota composition with a decrease in Bacteroidetes phylum and an increase in both Firmicutes and Proteobacteria phyla. |
Zhang et al. (2010) [40] | Apoa-I−/− and wild-type C57BL/6J mice | High-fat diet (34.9% fat) for 25 weeks | Sulphate-reducing, endotoxin-producing bacteria populations were enhanced in all animals fed with the high-fat diet. |
Devkota et al. (2012) [41] | C57BL/6 germ free mice | Milk, lard fat, or PUFAs (38% fat) for 3 weeks | Milk fat promotes expansion of sulfite-reducing bacteria, Bilophila genus of Proteobacteria phylum. PUFAs resulted in a higher abundance of Bacteroidetes phylum and lower abundance of Firmicutes phylum. |
Kaliannan et al. (2015) [52] | C57BL/6 wild type, fat-1 mice | Diet high in omega-6 PUFAs (10% corn oil) or omega-3 PUFAs (5% corn oil, 5% fish oil) for 8 months | High tissue omega-6/omega-3 PUFAs ratio can increase the proportions of LPS-producing and/or pro-inflammatory bacteria, low n-6/n-3 PUFAs ratio can increase LPS-suppressing and/or anti-inflammatory bacteria. |
Liu et al. (2012) [55] | Wild-type mice | Saturated fatty acids, omega-6 PUFAs, or omega-3 PUFAs diet for 14 weeks | Omega-6 PUFAs and the omega-3 PUFAs diet reduced the proportion of Bacteroidetes phylum. |
Yu et al. (2014) [56] | Imprinting Control Region mice | Natural saline group, high-dose fish oil group (10 mg/kg), and low dose fish oil group (5 mg/kg) for 2 weeks | Fish oil treatment resulted in a decrease in Firmicutes phylum. |
Caesar et al. (2015) [57] | C57Bl/6 Wild-type germ free mice | High fat diet (45%) for fish oil or lard | Fish-oil diet increases levels of Lactobacillus genera and Akkermansia muciniphila species, lard diet increases levels of Bilophila genus of Proteobacteria phylum. |
Mujico et al. (2013) [59] | Imprinting Control Region mice | Control diet (4% fat), high fat diet (43.3% fat, saturated 16.1%, MUFAs 12.7%, PUFAs 5.5%) for 19 weeks | PUFAs increases Firmicutes phylum. |
Ghosh et al. (2013) [62] | C57BL/6 mice | Corn oil diet or corn oil + fish oil diet for 5 weeks | Omega-6 PUFAs enriched the microbiota with Enterobacteriaceae family, omega-3 PUFA enriched microbiota with Lactobacillus and Bifidobacteria genera of Firmicutes phylum. |
Mokkala et al. (2016) [69] | Pregnant women | Diet with high intake of omega-3 PUFAs | Pregnant women with high intake of omega-3 PUFAs have shown higher abundance of F. prausnitzii species of Firmicutes phylum and a lower abundance of Bacteroides genera of Bacteroidetes phylum. |
Studies | Studied Population | Diets | Main Outcomes |
---|---|---|---|
Robertson et al. (2017) [92] | C57BL/6J mice | Control standard chow or omega-3 PUFA supplemented diet contained 1 g EPA + DHA/100 g diet (O3+), or omega-3 PUFA deficient diet (O3−) | O3+ diet leads to an increase of the abundance of Bifidobacterium and Lactobacillus genera; enhances cognition and dampens HPA axis activity. |
Pusceddu et al. (2015) [99] | Maternally separated female rats | Saline water or EPA/DHA 0.4 g/kg/day (low dose) or EPA/DHA 1 g/kg/day (high dose) | Long-term administration of high dose of EPA/DHA leads to restoration of the normal Firmicutes/Bacteroidetes phyla ratio; increases level of the butyrate-producing bacteria Butyrivibrio genus; increases the levels of several members of anti-inflammatory Actinobacteria phylum (such as Aerococcus genus); decreases the abundance of pro-inflammatory Proteobacteria phylum (such as Undibacterium genus); and decreases other pro-inflammatory bacteria genera including Akkermansia and Flexibacter. |
Davis et al. (2016) [103] | Socially isolated C57BL/6J mice | Control diet (modified AIN-93G diet composed by soybean, soy, and corn oils) or modified AIN-93G diet with the addition of 0.1% by weight DHA or modified AIN-93G diet with the addition of 1% by weight DHA | Addition of DHA leads to sex-specific compositional shifts within the Firmicutes phylum, more accentuated in male than in female, with an increase of Allobaculum genus (SCFAs-producing bacteria) and a decrease of Ruminococcus genus (involved in tryptophan metabolism). |
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Costantini, L.; Molinari, R.; Farinon, B.; Merendino, N. Impact of Omega-3 Fatty Acids on the Gut Microbiota. Int. J. Mol. Sci. 2017, 18, 2645. https://doi.org/10.3390/ijms18122645
Costantini L, Molinari R, Farinon B, Merendino N. Impact of Omega-3 Fatty Acids on the Gut Microbiota. International Journal of Molecular Sciences. 2017; 18(12):2645. https://doi.org/10.3390/ijms18122645
Chicago/Turabian StyleCostantini, Lara, Romina Molinari, Barbara Farinon, and Nicolò Merendino. 2017. "Impact of Omega-3 Fatty Acids on the Gut Microbiota" International Journal of Molecular Sciences 18, no. 12: 2645. https://doi.org/10.3390/ijms18122645