Prebiotic dietary fibre intervention improves fecal markers related to inflammation in obese patients: results from the Food4Gut randomized placebo-controlled trial.
Gut microbiota
Microbial metabolites
Obesity
Prebiotic
Journal
European journal of nutrition
ISSN: 1436-6215
Titre abrégé: Eur J Nutr
Pays: Germany
ID NLM: 100888704
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
14
10
2020
accepted:
08
01
2021
pubmed:
6
2
2021
medline:
13
8
2021
entrez:
5
2
2021
Statut:
ppublish
Résumé
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. 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. 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). 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. NCT03852069 (February 22, 2019 retrospectively, registered).
Identifiants
pubmed: 33544206
doi: 10.1007/s00394-021-02484-5
pii: 10.1007/s00394-021-02484-5
pmc: PMC8354918
doi:
Substances chimiques
Dietary Fiber
0
Prebiotics
0
RNA, Ribosomal, 16S
0
Inulin
9005-80-5
Banques de données
ClinicalTrials.gov
['NCT03852069']
Types de publication
Journal Article
Randomized Controlled Trial
Langues
eng
Sous-ensembles de citation
IM
Pagination
3159-3170Subventions
Organisme : Service Publique de Wallonie-Économie, Emploi, Recherche
ID : 1610365 and 1318148
Informations de copyright
© 2021. The Author(s).
Références
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. https://doi.org/10.1007/s13679-019-00352-2
doi: 10.1007/s13679-019-00352-2
pubmed: 31175629
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. https://doi.org/10.1016/j.cell.2016.05.041
doi: 10.1016/j.cell.2016.05.041
pubmed: 27259147
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. https://doi.org/10.1038/s41575-019-0157-3
doi: 10.1038/s41575-019-0157-3
pubmed: 31123355
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. https://doi.org/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. https://doi.org/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. https://doi.org/10.1007/s11154-020-09572-7
doi: 10.1007/s11154-020-09572-7
pubmed: 32691288
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. https://doi.org/10.1053/j.gastro.2017.01.055
doi: 10.1053/j.gastro.2017.01.055
pubmed: 28214524
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. https://doi.org/10.1177/0004563212473450
doi: 10.1177/0004563212473450
pubmed: 23771134
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. https://doi.org/10.1002/mnfr.201500014
doi: 10.1002/mnfr.201500014
pubmed: 25820326
pmcid: 4523425
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
pubmed: 10428978
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. https://doi.org/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. https://doi.org/10.1097/01.mco.0000247465.34037.05
doi: 10.1097/01.mco.0000247465.34037.05
pubmed: 17053429
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. https://doi.org/10.1038/nrgastro.2017.75
doi: 10.1038/nrgastro.2017.75
pubmed: 28611480
Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125(6):1401–1412. https://doi.org/10.1093/jn/125.6.1401
doi: 10.1093/jn/125.6.1401
pubmed: 7782892
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. https://doi.org/10.1016/j.clnu.2019.03.002
doi: 10.1016/j.clnu.2019.03.002
pubmed: 30904186
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. https://doi.org/10.1186/1475-2859-10-S1-S10
doi: 10.1186/1475-2859-10-S1-S10
pubmed: 21995448
pmcid: 3231917
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. https://doi.org/10.1038/nrendo.2011.126
doi: 10.1038/nrendo.2011.126
pubmed: 21826100
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. https://doi.org/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. https://doi.org/10.1007/s13679-020-00379-w
doi: 10.1007/s13679-020-00379-w
pubmed: 32632847
Cerdo T, Garcia-Santos JA (2019) The role of probiotics and prebiotics in the prevention and treatment of obesity. Nutrients 11:3. https://doi.org/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. https://doi.org/10.1016/j.clnu.2020.04.005
doi: 10.1016/j.clnu.2020.04.005
pubmed: 33023763
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. https://doi.org/10.1111/nbu.12416
doi: 10.1111/nbu.12416
pubmed: 32194343
pmcid: 7074038
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. https://doi.org/10.1016/j.parkreldis.2018.02.022
doi: 10.1016/j.parkreldis.2018.02.022
pubmed: 29454662
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. https://doi.org/10.12688/f1000research.20510.1
doi: 10.12688/f1000research.20510.1
pubmed: 32051759
pmcid: 6996528
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. https://doi.org/10.1080/00365529950172835
doi: 10.1080/00365529950172835
pubmed: 10048733
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. https://doi.org/10.1080/09637486.2017.1412404
doi: 10.1080/09637486.2017.1412404
pubmed: 29252035
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. https://doi.org/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. https://doi.org/10.1080/19490976.2020.1810530
doi: 10.1080/19490976.2020.1810530
pubmed: 32893709
pmcid: 7524357
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. https://doi.org/10.1038/s41587-019-0209-9
doi: 10.1038/s41587-019-0209-9
pubmed: 31341288
pmcid: 7015180
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. https://doi.org/10.3945/ajcn.2009.27465
doi: 10.3945/ajcn.2009.27465
pubmed: 19386741
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. https://doi.org/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. https://doi.org/10.1371/journal.pone.0216528
doi: 10.1371/journal.pone.0216528
pubmed: 31067253
pmcid: 6505945
Kaakoush NO (2015) Insights into the role of erysipelotrichaceae in the human host. Front Cell Infect Microbiol 5:84. https://doi.org/10.3389/fcimb.2015.00084
doi: 10.3389/fcimb.2015.00084
pubmed: 26636046
pmcid: 4653637
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. https://doi.org/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. https://doi.org/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. https://doi.org/10.1017/S0007114512002723
doi: 10.1017/S0007114512002723
pubmed: 23200109
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. https://doi.org/10.1016/j.clnu.2014.06.001
doi: 10.1016/j.clnu.2014.06.001
pubmed: 24969566
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. https://doi.org/10.1017/S0954422415000037
doi: 10.1017/S0954422415000037
pubmed: 26156216
pmcid: 4501371
Ridlon JM, Kang DJ, Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47(2):241–259. https://doi.org/10.1194/jlr.R500013-JLR200
doi: 10.1194/jlr.R500013-JLR200
pubmed: 16299351
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. https://doi.org/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. https://doi.org/10.1016/j.jchromb.2012.05.015
doi: 10.1016/j.jchromb.2012.05.015
pubmed: 22664055
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. https://doi.org/10.1007/s11745-014-3881-z
doi: 10.1007/s11745-014-3881-z
pubmed: 24473752
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. https://doi.org/10.1021/acs.jafc.9b05744
doi: 10.1021/acs.jafc.9b05744
pubmed: 31690068
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. https://doi.org/10.1099/mic.0.022921-0
doi: 10.1099/mic.0.022921-0
pubmed: 19118369
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. https://doi.org/10.1016/j.jnutbio.2013.08.006
doi: 10.1016/j.jnutbio.2013.08.006
pubmed: 24231103