Link between gut microbiota and health outcomes in inulin -treated obese patients: Lessons from the Food4Gut multicenter randomized placebo-controlled trial.

Hiel, Sophie; Gianfrancesco, Marco; Rodriguez, Julie; Portheault, Daphnée; Leyrolle, Quentin; Bindels, Laure B.; Gomes da Silveira Cauduro, Carolina; Mulders, Maria D. G. H.; Zamariola, Giorgia; Azzi, Anne-Sophie; Kalala, Gaetan; Pachikian, Barbara D.; Amadieu, Camille; Neyrinck, Audrey M.; Loumaye, Audrey; Cani, Patrice D.; Lanthier, Nicolas; Trefois, Pierre; Klein, Olivier; Luminet, Olivier; Bindelle, Jérôme; Paquot, Nicolas; Cnop, Miriam; Thissen, Jean-Paul; Delzenne, Nathalie M.

doi:10.1016/j.clnu.2020.04.005

Article (Scientific journals)

Link between gut microbiota and health outcomes in inulin -treated obese patients: Lessons from the Food4Gut multicenter randomized placebo-controlled trial.

Hiel, Sophie; Gianfrancesco, Marco; Rodriguez, Julie et al.

2020 • In Clinical nutrition (Edinburgh, Scotland)

Peer reviewed

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https://hdl.handle.net/2268/250070

DOI
10.1016/j.clnu.2020.04.005

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32340903

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Keywords :

Inulin; Metformin; Microbiota; Obesity; Prebiotics

Abstract :

[en] BACKGROUND: The gut microbiota is altered in obesity and is strongly influenced by nutrients and xenobiotics. We have tested the impact of native inulin as prebiotic present in vegetables and added as a supplement on gut microbiota-related outcomes in obese patients. Metformin treatment was analyzed as a potential modulator of the response. METHODS: A randomized, single-blinded, multicentric, placebo-controlled trial was conducted in 150 obese patients who received 16 g/d native inulin versus maltodextrin, coupled to dietary advice to consume inulin-rich versus -poor vegetables for 3 months, respectively, in addition to dietary caloric restriction. Anthropometry, diagnostic imaging (abdominal CT-scan, fibroscan), food-behavior questionnaires, serum biology and fecal microbiome (primary outcome; 16S rDNA sequencing) were analyzed before and after the intervention. RESULTS: Both placebo and prebiotic interventions lowered energy intake, BMI, systolic blood pressure, and serum γ-GT. The prebiotic induced greater weight loss and additionally decreased diastolic blood pressure, AST and insulinemia. Metformin treatment compromised most of the gut microbiota changes and metabolic improvements linked to prebiotic intervention. The prebiotic modulated specific bacteria, associated with the improvement of anthropometry (i.e. a decrease in Desulfovibrio and Clostridium sensu stricto). A large increase in Bifidobacterium appears as a signature of inulin intake rather than a driver of prebiotic-linked biological outcomes. CONCLUSIONS: Inulin-enriched diet is able to promote weight loss in obese patients, the treatment efficiency being related to gut microbiota characteristics. This treatment is more efficacious in patients who did not receive metformin as anti-diabetic drugs prior the intervention, supporting that both drug treatment and microbiota might be taken into account in personalized nutrition interventions. Registered under ClinicalTrials.gov Identifier no NCT03852069.

Disciplines :

Human health sciences: Multidisciplinary, general & others

Author, co-author :

Hiel, Sophie ^✱

Gianfrancesco, Marco ^✱; Université de Liège - ULiège > GIGA > Laboratoire d'Immunométabolisme et Nutrition

Rodriguez, Julie ^✱

Portheault, Daphnée

Leyrolle, Quentin

Bindels, Laure B.

Gomes da Silveira Cauduro, Carolina

Mulders, Maria D. G. H.

Zamariola, Giorgia

Azzi, Anne-Sophie

More authors (15 more)

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Link between gut microbiota and health outcomes in inulin -treated obese patients: Lessons from the Food4Gut multicenter randomized placebo-controlled trial.

Publication date :

2020

Journal title :

Clinical nutrition (Edinburgh, Scotland)

ISSN :

0261-5614

eISSN :

1532-1983

Peer reviewed :

Peer reviewed

Additional URL :

https://doi.org/10.1016/j.clnu.2020.04.005

Commentary :

Available on ORBi :

since 11 August 2020

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Bibliography

Anon, Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med 377 (2017), 13–27 Available at: http://www.nejm.org/doi/10.1056/NEJMoa1614362.
Zmora, N., Suez, J., Elinav, E., You are what you eat: diet, health and the gut microbiota. Nat Rev Gastroenterol Hepatol 16:1 (2019), 35–56.
Forouhi, N.G., Unwin, N., Global diet and health: old questions, fresh evidence, and new horizons. Lancet 393:10184 (2019), 1916–1918.
Gibson, G.R., Hutkins, R., Sanders, M.E., Prescott, S.L., Reimer, R.A., Salminen, S.J., et al. 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 (2017), 491–502.
Delzenne, N.M., Neyrinck, A.M., Cani, P.D., Gut microbiota and metabolic disorders: how prebiotic can work?. Br J Nutr 109:Suppl 2 (2013), S81–S85.
Kalala, G., Kambashi, B., Everaert, N., Beckers, Y., Richel, A., Pachikian, B., et al. Characterization of fructans and dietary fibre profiles in raw and steamed vegetables. Int J Food Sci Nutr 69:6 (2018), 682–689.
Hiel, S., Bindels, L.B., Pachikian, B.D., Kalala, G., Broers, V., Zamariola, G., et al. Effects of a diet based on inulin-rich vegetables on gut health and nutritional behavior in healthy humans. Am J Clin Nutr 109:6 (2019), 1683–1695.
Rodriguez, J., Hiel, S., Delzenne, N.M., Metformin: old friend, new ways of action-implication of the gut microbiome?. Curr Opin Clin Nutr Metab Care 21:4 (2018), 294–301.
Potgens, S.A., Brossel, H., Sboarina, M., Catry, E., Cani, P.D., Neyrinck, A.M., et al. Klebsiella oxytoca expands in cancer cachexia and acts as a gut pathobiont contributing to intestinal dysfunction. Sci Rep, 8(1), 2018, 12321.
Sun, S.S., Chumlea, W.C., Heymsfield, S.B., Lukaski, H.C., Schoeller, D., Friedl, K., et al. Development of bioelectrical impedance analysis prediction equations for body composition with the use of a multicomponent model for use in epidemiologic surveys. Am J Clin Nutr 77:2 (2003), 331–340.
Mintz, L.B., O'Halloran, M.S., Mulholland, A.M., Schneider, P.A., Questionnaire for eating disorder Diagnoses: reliability and validity of operationalizing DSM-IV criteria into a self-report format. J Counsel Psychol 44 (1997), 63–79.
Bailly, N., Maitre, I., Amanda, M., Herve, C., Alaphilippe, D., The Dutch Eating Behaviour Questionnaire (DEBQ). Assessment of eating behaviour in an aging French population. Appetite 59:3 (2012), 853–858.
Olivares, M., Neyrinck, A.M., Potgens, S.A., Beaumont, M., Salazar, N., Cani, P.D., et al. The DPP-4 inhibitor vildagliptin impacts the gut microbiota and prevents disruption of intestinal homeostasis induced by a Western diet in mice. Diabetologia 61:8 (2018), 1838–1848.
European Food Safety Authority, Scientific opinion on dietary reference values for carbohydrates and dietary fibre. EFSA J, 8, 2010, 1462.
Dewulf, E.M., Cani, P.D., Claus, S.P., Fuentes, S., Puylaert, P.G., Neyrinck, A.M., et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62:8 (2013), 1112–1121.
Pol, K., de Graaf, C., Meyer, D., Mars, M., The efficacy of daily snack replacement with oligofructose-enriched granola bars in overweight and obese adults: a 12-week randomised controlled trial. Br J Nutr 119:9 (2018), 1076–1086.
de Luis, D.A., de la Fuente, B., Izaola, O., Aller, R., Gutierrez, S., Morillo, M., Double blind randomized clinical trial controlled by placebo with a fos enriched cookie on saciety and cardiovascular risk factors in obese patients. Nutr Hosp 28:1 (2013), 78–85.
Daud, N.M., Ismail, N.A., Thomas, E.L., Fitzpatrick, J.A., Bell, J.D., Swann, J.R., et al. The impact of oligofructose on stimulation of gut hormones, appetite regulation and adiposity. Obesity 22:6 (2014), 1430–1438.
Parnell, J.A., Reimer, R.A., 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 (2009), 1751–1759.
Tuschl, R.J., From dietary restraint to binge eating: some theoretical considerations. Appetite 14:2 (1990), 105–109.
Vilar-Gomez, E., Martinez-Perez, Y., Calzadilla-Bertot, L., Torres-Gonzalez, A., Gra-Oramas, B., Gonzalez-Fabian, L., et al. Weight loss through lifestyle modification significantly reduces features of nonalcoholic steatohepatitis. Gastroenterology 149:2 (2015), 367–378 e5; quiz e14-5.
Daubioul, C.A., Horsmans, Y., Lambert, P., Danse, E., Delzenne, N.M., Effects of oligofructose on glucose and lipid metabolism in patients with nonalcoholic steatohepatitis: results of a pilot study. Eur J Clin Nutr 59:5 (2005), 723–726.
Farhangi, M.A., Javid, A.Z., Dehghan, P., The effect of enriched chicory inulin on liver enzymes, calcium homeostasis and hematological parameters in patients with type 2 diabetes mellitus: a randomized placebo-controlled trial. Prim Care Diabetes 10:4 (2016), 265–271.
Chambers, E.S., Byrne, C.S., Morrison, D.J., Murphy, K.G., Preston, T., Tedford, C., et al. Dietary supplementation with inulin-propionate ester or inulin improves insulin sensitivity in adults with overweight and obesity with distinct effects on the gut microbiota, plasma metabolome and systemic inflammatory responses: a randomised cross-over trial. Gut 68:8 (2019), 1430–1438.
Cani, P.D., Neyrinck, A.M., Maton, N., Delzenne, N.M., Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like Peptide-1. Obes Res 13:6 (2005), 1000–1007.
de la Cuesta-Zuluaga, J., Mueller, N.T., Corrales-Agudelo, V., Velasquez-Mejia, E.P., Carmona, J.A., Abad, J.M., et al. Metformin is associated with higher relative abundance of mucin-degrading Akkermansia muciniphila and several short-chain fatty acid-producing microbiota in the gut. Diabetes Care 40:1 (2017), 54–62.
Wu, H., Esteve, E., Tremaroli, V., Khan, M.T., Caesar, R., Manneras-Holm, L., et al. Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med 23:7 (2017), 850–858.
Le Bastard, Q., Chapelet, G., Javaudin, F., Lepelletier, D., Batard, E., Montassier, E., The effects of inulin on gut microbial composition: a systematic review of evidence from human studies. Eur J Clin Microbiol Infect Dis 39:3 (2020), 403–413.
Nicolucci, A.C., Hume, M.P., Martinez, I., Mayengbam, S., Walter, J., Reimer, R.A., Prebiotics reduce body fat and alter intestinal microbiota in children who are overweight or with obesity. Gastroenterology 153:3 (2017), 711–722.
Reimer, R.A., Willis, H.J., Tunnicliffe, J.M., Park, H., Madsen, K.L., Soto-Vaca, A., Inulin-type fructans and whey protein both modulate appetite but only fructans alter gut microbiota in adults with overweight/obesity: a randomized controlled trial. Mol Nutr Food Res, 61(11), 2017.
Yan, H., Potu, R., Lu, H., Vezzoni de Almeida, V., Stewart, T., Ragland, D., et al. Dietary fat content and fiber type modulate hind gut microbial community and metabolic markers in the pig. PloS One, 8(4), 2013, e59581.
Garcia-Mantrana, I., Selma-Royo, M., Alcantara, C., Collado, M.C., Shifts on gut microbiota associated to mediterranean diet adherence and specific dietary intakes on general adult population. Front Microbiol, 9, 2018, 890.
Costabile, A., Kolida, S., Klinder, A., Gietl, E., Bauerlein, M., Frohberg, C., et al. A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr 104:7 (2010), 1007–1017.
Slavin, J., Feirtag, J., Chicory inulin does not increase stool weight or speed up intestinal transit time in healthy male subjects. Food Funct 2:1 (2011), 72–77.
Ramnani, P., Costabile, A., Bustillo, A.G., Gibson, G.R., A randomised, double- blind, cross-over study investigating the prebiotic effect of agave fructans in healthy human subjects. J Nutr Sci, 4, 2015, e10.
Vandeputte, D., Falony, G., Vieira-Silva, S., Wang, J., Sailer, M., Theis, S., et al. Prebiotic inulin-type fructans induce specific changes in the human gut microbiota. Gut 66:11 (2017), 1968–1974.
Falony, G., Vlachou, A., Verbrugghe, K., De Vuyst, L., Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 72:12 (2006), 7835–7841.
Holscher, H.D., Bauer, L.L., Gourineni, V., Pelkman, C.L., Fahey, G.C. Jr., Swanson, K.S., Agave inulin supplementation affects the fecal microbiota of healthy adults participating in a randomized, double-blind, placebo-controlled, crossover trial. J Nutr 145:9 (2015), 2025–2032.
Yun, Y., Kim, H.N., Kim, S.E., Heo, S.G., Chang, Y., Ryu, S., et al. Comparative analysis of gut microbiota associated with body mass index in a large Korean cohort. BMC Microbiol, 17(1), 2017, 151.
Zeng, Q., Li, D., He, Y., Li, Y., Yang, Z., Zhao, X., et al. Discrepant gut microbiota markers for the classification of obesity-related metabolic abnormalities. Sci Rep, 9(1), 2019, 13424.