Prebiotics Reduce Body Fat and Alter Intestinal Microbiota in Children Who Are Overweight or With Obesity

Gastroenterology

Volumn 153, Issue 3, 2017, Pages 711-722

  Nicolucci, Alissa C ^a   Hume, Megan P ^a   Martínez, Inés ^b   Mayengbam, Shyamchand ^a   Walter, Jens ^b   Reimer, Raylene A ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Adiposity; BMI; Inulin type Fructans; Pediatric Obesity

Indexed keywords

BILE ACID; C REACTIVE PROTEIN; CHENODEOXYCHOLIC ACID; CHOLIC ACID; DEOXYCHOLIC ACID; FRUCTOSE OLIGOSACCHARIDE; GLUCOSE; HIGH DENSITY LIPOPROTEIN; HYODEOXYCHOLIC ACID; INSULIN; INTERLEUKIN 6; INULIN; LIPOPOLYSACCHARIDE; LITHOCHOLIC ACID; LOW DENSITY LIPOPROTEIN; MALTODEXTRIN; OLIGOFRUCTOSE ENRICHED INULIN; PLACEBO; PREBIOTIC AGENT; RNA 16S; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID; OLIGOSACCHARIDE;

ANTHROPOMETRIC PARAMETERS; ARTICLE; BACTEROIDES VULGATUS; BIFIDOBACTERIUM; BLOATING; BLOOD SAMPLING; BODY COMPOSITION; BODY FAT; BODY HEIGHT; BODY MASS; BODY WEIGHT; CHILD; CHILDHOOD OBESITY; CLINICAL ARTICLE; CLINICAL ASSESSMENT; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DUAL ENERGY X RAY ABSORPTIOMETRY; FECES ANALYSIS; FEMALE; FLATULENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INFLAMMATION; INTESTINE FLORA; MALE; OUTCOME ASSESSMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL; SEQUENCE ANALYSIS; WAIST CIRCUMFERENCE; BACTEROIDES; BLOOD; CHEMISTRY; DRUG EFFECTS; FECES; ISOLATION AND PURIFICATION; MICROBIOLOGY; OBESITY; OVERWEIGHT; PEDIATRIC OBESITY;

ADIPOSITY; BACTEROIDES; BIFIDOBACTERIUM; BILE ACIDS AND SALTS; BODY HEIGHT; BODY WEIGHT; CHILD; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INTERLEUKIN-6; INULIN; MALE; OLIGOSACCHARIDES; OVERWEIGHT; PEDIATRIC OBESITY; PREBIOTICS; TRIGLYCERIDES; WAIST CIRCUMFERENCE;

EID: 85025595568     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2017.05.055     Document Type: Article

References (58)

1. Arora, T., Backhed, F., The gut microbiota and metabolic disease: Current understanding and future perspectives. J Intern Med 280 (2016), 339–349.
2. Cani, P.D., Bibiloni, R., Knauf, C., et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet–induced obesity and diabetes in mice. Diabetes 57 (2008), 1470–1481.
3. Cani, P.D., Amar, J., Iglesias, M.A., et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 (2007), 1761–1772.
4. Spruss, A., Kanuri, G., Stahl, C., et al. Metformin protects against the development of fructose-induced steatosis in mice: role of the intestinal barrier function. Lab Investig 92 (2012), 1020–1032.
5. Duboc, H., Rainteau, D., Rajca, S., et al. Increase in fecal primary bile acids and dysbiosis in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil 24 (2012), 513–520.
6. Gibson, G.R., Scott, K.P., Rastall, R.A., et al. Dietary prebiotics: current status and new definition. Food Sci Technol Bull Funct Foods 7 (2010), 1–19.
7. Bindels, L.B., Delzenne, N.M., Cani, P.D., et al. Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol 12 (2015), 303–310.
8. 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 (2009), 1751–1759.
9. Dewulf, E.M., Cani, P.D., Claus, S.P., et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62 (2013), 1112–1121.
10. Salazar, N., Dewulf, E.M., Neyrinck, A.M., et al. Inulin-type fructans modulate intestinal Bifidobacterium species populations and decrease fecal short-chain fatty acids in obese women. Clin Nutr 34 (2015), 501–507.
11. Weiss, R., Caprio, S., The metabolic consequences of childhood obesity. Best Pract Res Clin Endocrinol Metab 19 (2005), 405–419.
12. Abrams, S.A., Griffin, I.J., Hawthorne, K.M., et al. A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr 82 (2005), 471–476.
13. Abrams, S.A., Griffin, I.J., Hawthorne, K.M., et al. Effect of prebiotic supplementation and calcium intake on body mass index. J Pediatr 151 (2007), 293–298.
14. Savoye, M., Shaw, M., Dziura, J., et al. Effects of a weight management program on body composition and metabolic parameters in overweight children. JAMA 297 (2007), 2697–2704.
15. Arnberg, K., Larnkjær, A., Michaelsen, K.F., et al. Central adiposity and protein intake are associated with arterial stiffness in overweight children. J Nutr 142 (2012), 878–885.
16. USDA/ARS Children's Nutrition Research Center. Pediatric body composition reference charts. Available at: https://www.bcm.edu/bodycomplab/Flashapps/AllDXArefsChartpage.html.
17. Godin, G., Shephard, R.J., Godin leisure-time exercise questionnaire. Med Sci Sports Exerc 29 (1997), S36–S38.
18. The Oxford Centre for Diabetes Endocrinology and Metabolism. HOMA calculator. Available at: https://www.dtu.ox.ac.uk/homacalculator/.
19. Kakiyama, G., Muto, A., Takei, H., et al. A simple and accurate HPLC method for fecal bile acid profile in healthy and cirrhotic subjects: validation by GC-MS and LC-MS. J Lipid Res 55 (2014), 978–990.
20. Bomhof, M.R., Saha, D.C., Reid, D.T., et al. Combined effects of oligofructose and Bifidobacterium animalis on gut microbiota and glycemia in obese rats. Obesity 22 (2014), 763–771.
21. Collins, K.H., Paul, H.A., Reimer, R.A., et al. Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: Studies in a rat model. Osteoarthr Cartil 23 (2015), 1989–1998.
22. Bomhof, M.R., Paul, H.A., Geuking, M.B., et al. Improvement in adiposity with oligofructose is modified by antibiotics in obese rats. FASEB J, 30, 2016 fj-201600151R.
23. Krumbeck, J.A., Maldonado-Gomez, M.X., Martínez, I., et al. In vivo selection to identify bacterial strains with enhanced ecological performance in synbiotic applications. Appl Environ Microbiol 81 (2015), 2455–2465.
24. R Core Team. R: a language and environment for statistical computing. R Found Stat Comput 2015: Vienna, Austria.
25. Bates, D., Mächler, M., Bolker, B., et al. fitting linear mixed-effects models using lme4. J Stat Softw 67 (2015), 1–48.
26. Oksanen J, Blanchet FG, Kindt R, et al. Vegan: community ecology package. R package version 2.3-2. 2015.
27. Strimmer, K., fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24 (2008), 1461–1462.
28. Manios, Y., Moschonis, G., Kourlaba, G., et al. Prevalence and independent predictors of insulin resistance in children from Crete, Greece: the Children Study. Diabet Med 25 (2008), 65–72.
29. Liber, A., Szajewska, H., Effect of oligofructose supplementation on body weight in overweight and obese children: a randomised, double-blind, placebo-controlled trial. Br J Nutr 112 (2014), 2068–2074.
30. Malina, R., Normal weight gain in growing children. Heal Weight J 13 (1999), 13–14.
31. Hume, M.P., Nicolucci, A.C., Reimer, R.A., Prebiotic supplementation improves appetite control in children with overweight and obesity: a randomized controlled trial. Am J Clin Nutr 105 (2017), 790–799.
32. Despres, J.-P., Lemieux, I., Abdominal obesity and metabolic syndrome. Nature 444 (2006), 881–887.
33. Bastard, J.-P., Jardel, C., Bruckert, E., et al. Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. J Clin Endocrinol Metab 85 (2000), 3338–3342.
34. Ford, E.S., Galuska, D.A., Gillespie, C., et al. C-reactive protein and body mass index in children: findings from the Third National Health and Nutrition Examination Survey, 1988-1994. J Pediatr 138 (2001), 486–492.
35. Lecerf, J.-M., Dépeint, F., Clerc, E., et al. Xylo-oligosaccharide (XOS) in combination with inulin modulates both the intestinal environment and immune status in healthy subjects, while XOS alone only shows prebiotic properties. Br J Nutr 108 (2012), 1847–1858.
36. Varma, M.C., Kusminski, C.M., Azharian, S., et al. Metabolic endotoxaemia in childhood obesity. BMC Obes, 3, 2016, 3.
37. Weiss, R., Dziura, J., Burgert, T.S., et al. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350 (2004), 2362–2374.
38. Dehghan, P., Pourghassem Gargari, B., Asghari Jafar-abadi, M., Oligofructose-enriched inulin improves some inflammatory markers and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized controlled clinical trial. Nutrition 30 (2014), 418–423.
39. Dehghan, P., Pourghassem Gargari, B., Asghari Jafar-Abadi, M., et al. Inulin controls inflammation and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized-controlled clinical trial. Int J Food Sci Nutr 65 (2014), 117–123.
40. Parnell, J.A., Klancic, T., Reimer, R.A., Oligofructose decreases serum lipopolysaccharide and plasminogen activator inhibitor-1 in adults with overweight/obesity. Obesity 25 (2017), 510–513.
41. Wahlstrom, A., Sayin, S.I., Marschall, H.U., et al. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab 24 (2016), 41–50.
42. Yu, H., Ni, Y., Bao, Y., et al. Chenodeoxycholic acid as a potential prognostic marker for roux-en-y gastric bypass in Chinese obese patients. J Clin Endocrinol Metab 100 (2015), 4222–4230.
43. Ridlon, J., Kang, D., Hylemon, P., et al. Bile acids and the gut microbiome. Curr Opin Gastroenterol 30 (2014), 332–338.
44. Gibson, G.R., Roberfroid, M.B., Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 126 (1995), 1401–1412.
45. Di Gioia, D., Aloisio, I., Mazzola, G., et al. Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl Microbiol Biotechnol 98 (2013), 563–577.
46. Kalliomäki, M., Collado, M.C., Salminen, S., et al. Early differences in fecal microbiota composition in children may predict overweight. Am J Cinical Nutr 87 (2008), 534–538.
47. Schwiertz, A., Taras, D., Schäfer, K., et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18 (2009), 190–195.
48. Bouhnik, Y., Vahedi, K., Achour, L., et al. Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. J Nutr 129 (1999), 113–116.
49. Finegold, S.M., Song, Y., Liu, C., et al. Clostridium clostridioforme: a mixture of three clinically important species. Eur J Clin Microbiol Infect Dis 24 (2005), 319–324.
50. Karlsson, F.H., Tremaroli, V., Nookaew, I., et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498 (2013), 99–103.
51. Qin, J., Li, Y., Cai, Z., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
52. Sokol, H., Pigneur, B., Watterlot, L., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 105 (2008), 16731–16736.
53. Balamurugan, R., George, G., Kabeerdoss, J., et al. Quantitative differences in intestinal Faecalibacterium prausnitzii in obese Indian children. Br J Nutr 103 (2010), 335–338.
54. Riva, A., Borgo, F., Lassandro, C., et al. Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Environ Microbiol 19 (2017), 95–105.
55. Ramirez-Farias, C., Slezak, K., Fuller, Z., et al. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 101 (2009), 541–550.
56. Moens, F., Weckx, S., Vuyst L De. Bifidobacterial inulin-type fructan degradation capacity determines cross-feeding interactions between bifidobacteria and Faecalibacterium prausnitzii. Int J Food Microbiol 231 (2016), 76–85.
57. Hippe, B., Remely, M., Aumueller, E., et al. Faecalibacterium prausnitzii phylotypes in type two diabetic, obese, and lean control subjects. Benef Microbes 7 (2016), 511–517.
58. Payne, A.N., Chassard, C., Zimmermann, M., et al. The metabolic activity of gut microbiota in obese children is increased compared with normal-weight children and exhibits more exhaustive substrate utilization. Nutr Diabetes, 1, 2011, e12.