Prebiotic dietary fibre intervention improves fecal markers related to inflammation in obese patients: results from the Food4Gut randomized placebo-controlled trial.
Neyrinck, Audrey M; Rodriguez, Julie; Zhang, Zhengxiaoet al.
2021 • In European Journal of Nutrition, 60 (6), p. 3159-3170
Gut microbiota; Microbial metabolites; Obesity; Prebiotic; Dietary Fiber; Prebiotics; RNA, Ribosomal, 16S; Inulin; Feces; Humans; Inflammation; Retrospective Studies; Medicine (miscellaneous); Nutrition and Dietetics
Abstract :
[en] ("[en] PURPOSE: Inulin-type fructans (ITF) are prebiotic dietary fibre (DF) that may confer beneficial health effects, by interacting with the gut microbiota. We have tested the hypothesis that a dietary intervention promoting inulin intake versus placebo influences fecal microbial-derived metabolites and markers related to gut integrity and inflammation in obese patients.
METHODS: Microbiota (16S rRNA sequencing), long- and short-chain fatty acids (LCFA, SCFA), bile acids, zonulin, and calprotectin were analyzed in fecal samples obtained from obese patients included in a randomized, placebo-controlled trial. Participants received either 16 g/d native inulin (prebiotic n = 12) versus maltodextrin (placebo n = 12), coupled to dietary advice to consume inulin-rich versus inulin-poor vegetables for 3 months, in addition to dietary caloric restriction.
RESULTS: Both placebo and prebiotic interventions lowered energy and protein intake. A substantial increase in Bifidobacterium was detected after ITF treatment (q = 0.049) supporting our recent data obtained in a larger cohort. Interestingly, fecal calprotectin, a marker of gut inflammation, was reduced upon ITF treatment. Both prebiotic and placebo interventions increased the ratio of tauro-conjugated/free bile acids in feces. Prebiotic treatment did not significantly modify fecal SCFA content but it increased fecal rumenic acid, a conjugated linoleic acid (cis-9, trans-11 CLA) with immunomodulatory properties, that correlated notably to the expansion of Bifidobacterium (p = 0.031; r = 0.052).
CONCLUSIONS: Our study demonstrates that ITF-prebiotic intake during 3 months decreases a fecal marker of intestinal inflammation in obese patients. Our data point to a potential contribution of microbial lipid-derived metabolites in gastro-intestinal dysfunction related to obesity. CLINICALTRIALS.
GOV IDENTIFIER: NCT03852069 (February 22, 2019 retrospectively, registered).","[en] ","")
Disciplines :
Endocrinology, metabolism & nutrition
Author, co-author :
Neyrinck, Audrey M ; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium
Rodriguez, Julie ; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium
Zhang, Zhengxiao ; Department of Medicine, University of Alberta, Edmonton, Canada
Seethaler, Benjamin ; Institute of Nutritional Medicine, University of Hohenheim, Hohenheim, Germany
Sánchez, Cándido Robles; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium
Roumain, Martin ; Bioanalysis and Pharmacology of Bioactive Lipids Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, Brussels, Belgium
Hiel, Sophie; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium
Bindels, Laure B ; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium
Cani, Patrice D ; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium ; WELBIO- Walloon Excellence in Life Sciences and Biotechnology, UCLouvain, Université catholique de Louvain, Brussels, Belgium
Paquot, Nicolas ; Centre Hospitalier Universitaire de Liège - CHU > > Service de diabétologie, nutrition, maladies métaboliques
Cnop, Miriam; ULB Center for Diabetes Research, Université Libre de Bruxelles, Brussels, Belgium ; Division of Endocrinology, Erasmus Hospital, Université Libre de Bruxelles, Brussels, Belgium
Nazare, Julie-Anne ; Rhône-Alpes Research Center for Human Nutrition, Université-Lyon, CarMeN Laboratory, Hospices Civils de Lyon, Lyon, France
Laville, Martine ; Rhône-Alpes Research Center for Human Nutrition, Université-Lyon, CarMeN Laboratory, Hospices Civils de Lyon, Lyon, France
Muccioli, Giulio G ; Bioanalysis and Pharmacology of Bioactive Lipids Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, Brussels, Belgium
Bischoff, Stephan C ; Institute of Nutritional Medicine, University of Hohenheim, Hohenheim, Germany
Walter, Jens ; Department of Medicine, University of Alberta, Edmonton, Canada ; Department of Medicine, and School of Microbiology, APC Microbiome Ireland, University College Cork, Cork, Ireland
Thissen, Jean-Paul; Pole of Endocrinology, Diabetes and Nutrition, Institut de Recherche Expérimentale et Clinique, UCLouvain, Université catholique de Louvain, Brussels, Belgium
Delzenne, Nathalie M ; Metabolism and Nutrition Research Group, Louvain Drug Research Institute, UCLouvain, Université catholique de Louvain, avenue E. Mounier box B1.73.11, B-1200, Brussels, Belgium. nathalie.delzenne@uclouvain.be
Prebiotic dietary fibre intervention improves fecal markers related to inflammation in obese patients: results from the Food4Gut randomized placebo-controlled trial.
Publication date :
September 2021
Journal title :
European Journal of Nutrition
ISSN :
1436-6207
eISSN :
1436-6215
Publisher :
Springer Science and Business Media Deutschland GmbH, Germany
Service Publique de Wallonie-Économie, Emploi, Recherche
Funding text :
We are grateful to the study participants for their participation in the study. We thank Coralie Frenay for dietetic analysis. We thank Véronique Allaeys for the excellent technical assistance. We thank the UCLouvain’s platform “Support en méthodologie et calcul statistique” and more specifically Céline Bugli for their advice concerning statistical analyses. We thank Céline Druart and Florence Mailleux for their precious help and implication for the LCFA analysis. CRS is a beneficiary of a postdoctoral fellowship program from Fundación Alfonso Martin Escudero. NMD is a recipient of grants from the Fonds de la Recherche Scientifique (FRS-FNRS, convention PINT-MULTI R.8013.19 (NEURON, call 2019) and convention PDR T.0068.19) and from UCLouvain (Action de Recherche Concertée ARC18-23/092). PDC is supported by the Fonds Baillet Latour (Grant for Medical Research 2015), the Fonds de la Recherche Scientifique (FNRS, FRFS-WELBIO: WELBIO-CR-2019C-02R, and EOS program no.30770923).We are grateful to the study participants for their participation in the study. We thank Coralie Frenay for dietetic analysis. We thank Véronique Allaeys for the excellent technical assistance. We thank the UCLouvain’s platform “Support en méthodologie et calcul statistique” and more specifically Céline Bugli for their advice concerning statistical analyses. We thank Céline Druart and Florence Mailleux for their precious help and implication for the LCFA analysis. CRS is a beneficiary of a postdoctoral fellowship program from Fundación Alfonso Martin Escudero. NMD is a recipient of grants from the Fonds de la Recherche Scientifique (FRS-FNRS, convention PINT-MULTI R.8013.19 (NEURON, call 2019) and convention PDR T.0068.19) and from UCLouvain (Action de Recherche Concertée ARC18-23/092). PDC is supported by the Fonds Baillet Latour (Grant for Medical Research 2015), the Fonds de la Recherche Scientifique (FNRS, FRFS-WELBIO: WELBIO-CR-2019C-02R, and EOS program no.30770923).This study was supported by the Service Public de Wallonie (SPW-EER, convention FiberTAG 1610365 and convention FOOD4GUT 1318148, Belgium).
Vallianou N, Stratigou T, Christodoulatos GS, Dalamaga M (2019) Understanding the role of the gut microbiome and microbial metabolites in obesity and obesity-associated metabolic disorders: current evidence and perspectives. Curr Obes Rep 8(3):317–332. 10.1007/s13679-019-00352-2 DOI: 10.1007/s13679-019-00352-2
Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F (2016) From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165(6):1332–1345. 10.1016/j.cell.2016.05.041 DOI: 10.1016/j.cell.2016.05.041
Dalile B, Van Oudenhove L, Vervliet B, Verbeke K (2019) The role of short-chain fatty acids in microbiota-gut-brain communication. Nat Rev Gastroenterol Hepatol 16(8):461–478. 10.1038/s41575-019-0157-3 DOI: 10.1038/s41575-019-0157-3
Delzenne NM, Cani PD (2011) Interaction between obesity and the gut microbiota: relevance in nutrition. AnnuRevNutr 31:15–31
Delzenne NM, Neyrinck AM, Cani PD (2011) Modulation of the gut microbiota by nutrients with prebiotic properties: consequences for host health in the context of obesity and metabolic syndrome. Microb Cell Fact 10:10. 10.1186/1475-2859-10-s1-s10 DOI: 10.1186/1475-2859-10-s1-s10
Delzenne NM, Cani PD, Everard A, Neyrinck AM, Bindels LB (2015) Gut microorganisms as promising targets for the management of type 2 diabetes. Diabetol Clin Ex Diabetes Meta 58(10):2206–2217. 10.1007/s00125-015-3712-7 DOI: 10.1007/s00125-015-3712-7
Delzenne NM, Rodriguez J, Olivares M, Neyrinck AM (2020) Microbiome response to diet: focus on obesity and related diseases. Rev Endocr Metab Disord. 10.1007/s11154-020-09572-7 DOI: 10.1007/s11154-020-09572-7
Chavez-Talavera O, Tailleux A, Lefebvre P, Staels B (2017) Bile acid control of metabolism and inflammation in obesity, Type 2 diabetes, dyslipidemia, and nonalcoholic fatty liver disease. Gastroenterology 152(7):1679–1694. 10.1053/j.gastro.2017.01.055 DOI: 10.1053/j.gastro.2017.01.055
Vincent RP, Omar S, Ghozlan S, Taylor DR, Cross G, Sherwood RA, Fandriks L, Olbers T, Werling M, Alaghband-Zadeh J, le Roux CW (2013) Higher circulating bile acid concentrations in obese patients with type 2 diabetes. Ann Clin Biochem 50(Pt 4):360–364. 10.1177/0004563212473450 DOI: 10.1177/0004563212473450
Druart C, Bindels LB, Schmaltz R, Neyrinck AM, Cani PD, Walter J, Ramer-Tait AE, Delzenne NM (2015) Ability of the gut microbiota to produce PUFA-derived bacterial metabolites: proof of concept in germ-free versus conventionalized mice. Mol Nutr Food Res 59(8):1603–1613. 10.1002/mnfr.201500014 DOI: 10.1002/mnfr.201500014
Moya-Camarena SY, Vanden Heuvel JP, Blanchard SG, Leesnitzer LA, Belury MA (1999) Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARalpha. J Lipid Res 40(8):1426–1433 DOI: 10.1016/S0022-2275(20)33384-8
den Hartigh LJ (2019) Conjugated linoleic acid effects on cancer, obesity, and atherosclerosis: a review of pre-clinical and human trials with current perspectives. Nutrients 11:2. 10.3390/nu11020370 DOI: 10.3390/nu11020370
Toomey S, McMonagle J, Roche HM (2006) Conjugated linoleic acid: a functional nutrient in the different pathophysiological components of the metabolic syndrome? Curr Opin Clin Nutr Metab Care 9(6):740–747. 10.1097/01.mco.0000247465.34037.05 DOI: 10.1097/01.mco.0000247465.34037.05
Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, Verbeke K, Reid G (2017) Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14(8):491–502. 10.1038/nrgastro.2017.75 DOI: 10.1038/nrgastro.2017.75
Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125(6):1401–1412. 10.1093/jn/125.6.1401 DOI: 10.1093/jn/125.6.1401
Delzenne NM, Olivares M, Neyrinck AM, Beaumont M, Kjolbaek L, Larsen TM, Benitez-Paez A, Romani-Perez M, Garcia-Campayo V, Bosscher D, Sanz Y, van der Kamp JW (2020) Nutritional interest of dietary fiber and prebiotics in obesity: lessons from the MyNewGut consortium. Clin Nutr 39(2):414–424. 10.1016/j.clnu.2019.03.002 DOI: 10.1016/j.clnu.2019.03.002
Delzenne NM, Neyrinck AM, Cani PD (2011) Modulation of the gut microbiota by nutrients with prebiotic properties: consequences for host health in the context of obesity and metabolic syndrome. Microb Cell Fact 10(Suppl 1):S10. 10.1186/1475-2859-10-S1-S10 DOI: 10.1186/1475-2859-10-S1-S10
Delzenne NM, Neyrinck AM, Backhed F, Cani PD (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7(11):639–646. 10.1038/nrendo.2011.126 DOI: 10.1038/nrendo.2011.126
Green M, Arora K, Prakash S (2020) Microbial medicine: prebiotic and probiotic functional foods to target obesity and metabolic syndrome. Int J Mol Sci 21:8. 10.3390/ijms21082890 DOI: 10.3390/ijms21082890
Vallianou N, Stratigou T, Christodoulatos GS, Tsigalou C, Dalamaga M (2020) Probiotics, prebiotics, synbiotics, postbiotics, and obesity: current evidence, controversies, and perspectives. Curr Obes Rep. 10.1007/s13679-020-00379-w DOI: 10.1007/s13679-020-00379-w
Cerdo T, Garcia-Santos JA (2019) The role of probiotics and prebiotics in the prevention and treatment of obesity. Nutrients 11:3. 10.3390/nu11030635 DOI: 10.3390/nu11030635
Hiel S, Gianfrancesco MA, Rodriguez J, Portheault D, Leyrolle Q, Bindels LB, da Silveira G, Cauduro C, Mulders M, Zamariola G, Azzi AS, Kalala G, Pachikian BD, Amadieu C, Neyrinck AM, Loumaye A, Cani PD, Lanthier N, Trefois P, Klein O, Luminet O, Bindelle J, Paquot N, Cnop M, Thissen JP, Delzenne NM (2020) Link between gut microbiota and health outcomes in inulin-treated obese patients: Lessons from the Food4Gut multicenter randomized placebo-controlled trial. Clin Nutr. 10.1016/j.clnu.2020.04.005 DOI: 10.1016/j.clnu.2020.04.005
Neyrinck AM, Rodriguez J, Vinoy S, Maquet V, Walter J, Bischoff SC, Laville M, Delzenne NM (2020) The FiberTAG project: tagging dietary fibre intake by measuring biomarkers related to the gut microbiota and their interest for health. Nutr Bull 45(1):59–65. 10.1111/nbu.12416 DOI: 10.1111/nbu.12416
Schwiertz A, Spiegel J, Dillmann U, Grundmann D, Burmann J, Fassbender K, Schafer KH, Unger MM (2018) Fecal markers of intestinal inflammation and intestinal permeability are elevated in Parkinson’s disease. Parkinsonism Relat Disord 50:104–107. 10.1016/j.parkreldis.2018.02.022 DOI: 10.1016/j.parkreldis.2018.02.022
Fasano A (2020) All disease begins in the (leaky) gut: role of zonulin-mediated gut permeability in the pathogenesis of some chronic inflammatory diseases. F1000Res. 10.12688/f1000research.20510.1 DOI: 10.12688/f1000research.20510.1
Roseth AG, Schmidt PN, Fagerhol MK (1999) Correlation between faecal excretion of indium-111-labelled granulocytes and calprotectin, a granulocyte marker protein, in patients with inflammatory bowel disease. Scand J Gastroenterol 34(1):50–54. 10.1080/00365529950172835 DOI: 10.1080/00365529950172835
Kalala G, Kambashi B, Everaert N, Beckers Y, Richel A, Pachikian B, Neyrinck AM, Delzenne NM, Bindelle J (2018) Characterization of fructans and dietary fibre profiles in raw and steamed vegetables. Int J Food Sci Nutr 69(6):682–689. 10.1080/09637486.2017.1412404 DOI: 10.1080/09637486.2017.1412404
Neyrinck AM, Nazare JA, Rodriguez J, Jottard R, Dib S, Sothier M, Berghe LVD, Alligier M, Alexiou H, Maquet V, Vinoy S, Bischoff SC, Walter J, Laville M, Delzenne NM (2020) Development of a repertoire and a food frequency questionnaire for estimating dietary fiber intake considering prebiotics: input from the FiberTAG project. Nutrients 12:9. 10.3390/nu12092824 DOI: 10.3390/nu12092824
Rodriguez J, Neyrinck AM, Zhang Z, Seethaler B, Nazare JA, Robles Sanchez C, Roumain M, Muccioli GG, Bindels LB, Cani PD, Maquet V, Laville M, Bischoff SC, Walter J, Delzenne NM (2020) Metabolite profiling reveals the interaction of chitin-glucan with the gut microbiota. Gut Microbes 12(1):1810530. 10.1080/19490976.2020.1810530 DOI: 10.1080/19490976.2020.1810530
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodriguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vazquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37(8):852–857. 10.1038/s41587-019-0209-9 DOI: 10.1038/s41587-019-0209-9
Benjamini YHY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc 57:289–300
Parnell JA, Reimer RA (2009) Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr 89(6):1751–1759. 10.3945/ajcn.2009.27465 DOI: 10.3945/ajcn.2009.27465
Verdam FJ, Fuentes S, de Jonge C, Zoetendal EG, Erbil R, Greve JW, Buurman WA, de Vos WM, Rensen SS (2013) Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity (Silver Spring) 21(12):E607-615. 10.1002/oby.20466 DOI: 10.1002/oby.20466
Murray KA, Hoad CL, Garratt J, Kaviani M, Marciani L, Smith JK, Siegmund B, Gowland PA, Humes DJ, Spiller RC (2019) A pilot study of visceral fat and its association with adipokines, stool calprotectin and symptoms in patients with diverticulosis. PLoS ONE 14(5):e0216528. 10.1371/journal.pone.0216528 DOI: 10.1371/journal.pone.0216528
Kaakoush NO (2015) Insights into the role of erysipelotrichaceae in the human host. Front Cell Infect Microbiol 5:84. 10.3389/fcimb.2015.00084 DOI: 10.3389/fcimb.2015.00084
Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, Hardt PD (2010) Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18(1):190–195. 10.1038/oby.2009.167 DOI: 10.1038/oby.2009.167
Fava F, Gitau R, Griffin BA, Gibson GR, Tuohy KM, Lovegrove JA (2013) The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome “at-risk” population. Int J Obes (Lond) 37(2):216–223. 10.1038/ijo.2012.33 DOI: 10.1038/ijo.2012.33
Teixeira TF, Grzeskowiak L, Franceschini SC, Bressan J, Ferreira CL, Peluzio MC (2013) Higher level of faecal SCFA in women correlates with metabolic syndrome risk factors. Br J Nutr 109(5):914–919. 10.1017/S0007114512002723 DOI: 10.1017/S0007114512002723
Salazar N, Dewulf EM, Neyrinck AM, Bindels LB, Cani PD, Mahillon J, de Vos WM, Thissen JP, Gueimonde M, de Los Reyes-Gavilan CG, Delzenne NM (2015) Inulin-type fructans modulate intestinal Bifidobacterium species populations and decrease fecal short-chain fatty acids in obese women. Clin Nutr 34(3):501–507. 10.1016/j.clnu.2014.06.001 DOI: 10.1016/j.clnu.2014.06.001
Verbeke KA, Boobis AR, Chiodini A, Edwards CA, Franck A, Kleerebezem M, Nauta A, Raes J, van Tol EA, Tuohy KM (2015) Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr Res Rev 28(1):42–66. 10.1017/S0954422415000037 DOI: 10.1017/S0954422415000037
Ridlon JM, Kang DJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47(2):241–259. 10.1194/jlr.R500013-JLR200 DOI: 10.1194/jlr.R500013-JLR200
Zeng H, Umar S, Rust B, Lazarova D, Bordonaro M (2019) Secondary bile acids and short chain fatty acids in the colon: a focus on colonic microbiome, cell proliferation, inflammation, and cancer. Int J Mol Sci 20:5. 10.3390/ijms20051214 DOI: 10.3390/ijms20051214
Humbert L, Maubert MA, Wolf C, Duboc H, Mahe M, Farabos D, Seksik P, Mallet JM, Trugnan G, Masliah J, Rainteau D (2012) Bile acid profiling in human biological samples: comparison of extraction procedures and application to normal and cholestatic patients. J Chromatogr B Analyt Technol Biomed Life Sci 899:135–145. 10.1016/j.jchromb.2012.05.015 DOI: 10.1016/j.jchromb.2012.05.015
Druart C, Dewulf EM, Cani PD, Neyrinck AM, Thissen JP, Delzenne NM (2014) Gut microbial metabolites of polyunsaturated fatty acids correlate with specific fecal bacteria and serum markers of metabolic syndrome in obese women. Lipids 49(4):397–402. 10.1007/s11745-014-3881-z DOI: 10.1007/s11745-014-3881-z
Chen Y, Yang B, Ross RP, Jin Y, Stanton C, Zhao J, Zhang H, Chen W (2019) Orally administered CLA Ameliorates DSS-induced colitis in mice via intestinal barrier improvement, oxidative stress reduction, and inflammatory cytokine and gut microbiota modulation. J Agric Food Chem 67(48):13282–13298. 10.1021/acs.jafc.9b05744 DOI: 10.1021/acs.jafc.9b05744
McIntosh FM, Shingfield KJ, Devillard E, Russell WR, Wallace RJ (2009) Mechanism of conjugated linoleic acid and vaccenic acid formation in human faecal suspensions and pure cultures of intestinal bacteria. Microbiology 155(Pt 1):285–294. 10.1099/mic.0.022921-0 DOI: 10.1099/mic.0.022921-0
Penedo LA, Nunes JC, Gama MA, Leite PE, Quirico-Santos TF, Torres AG (2013) Intake of butter naturally enriched with cis9, trans11 conjugated linoleic acid reduces systemic inflammatory mediators in healthy young adults. J Nutr Biochem 24(12):2144–2151. 10.1016/j.jnutbio.2013.08.006 DOI: 10.1016/j.jnutbio.2013.08.006
