Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics

Abstract Background One way to improve both the ecological performance and functionality of probiotic bacteria is by combining them with a prebiotic in the form of a synbiotic. However, the degree to which such synbiotic formulations improve probiotic strain functionality in humans has not been test...

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Main Authors: Janina A. Krumbeck, Heather E. Rasmussen, Robert W. Hutkins, Jennifer Clarke, Krista Shawron, Ali Keshavarzian, Jens Walter
Format: Article
Language:English
Published: BMC 2018-06-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-018-0494-4
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author Janina A. Krumbeck
Heather E. Rasmussen
Robert W. Hutkins
Jennifer Clarke
Krista Shawron
Ali Keshavarzian
Jens Walter
author_facet Janina A. Krumbeck
Heather E. Rasmussen
Robert W. Hutkins
Jennifer Clarke
Krista Shawron
Ali Keshavarzian
Jens Walter
author_sort Janina A. Krumbeck
collection DOAJ
description Abstract Background One way to improve both the ecological performance and functionality of probiotic bacteria is by combining them with a prebiotic in the form of a synbiotic. However, the degree to which such synbiotic formulations improve probiotic strain functionality in humans has not been tested systematically. Our goal was to use a randomized, double-blind, placebo-controlled, parallel-arm clinical trial in obese humans to compare the ecological and physiological impact of the prebiotic galactooligosaccharides (GOS) and the probiotic strains Bifidobacterium adolescentis IVS-1 (autochthonous and selected via in vivo selection) and Bifidobacterium lactis BB-12 (commercial probiotic allochthonous to the human gut) when used on their own or as synbiotic combinations. After 3 weeks of consumption, strain-specific quantitative real-time PCR and 16S rRNA gene sequencing were performed on fecal samples to assess changes in the microbiota. Intestinal permeability was determined by measuring sugar recovery in urine by GC after consumption of a sugar mixture. Serum-based endotoxin exposure was also assessed. Results IVS-1 reached significantly higher cell numbers in fecal samples than BB-12 (P < 0.01) and, remarkably, its administration induced an increase in total bifidobacteria that was comparable to that of GOS. Although GOS showed a clear bifidogenic effect on the resident gut microbiota, both probiotic strains showed only a non-significant trend of higher fecal cell numbers when administered with GOS. Post-aspirin sucralose:lactulose ratios were reduced in groups IVS-1 (P = 0.050), IVS-1 + GOS (P = 0.022), and GOS (P = 0.010), while sucralose excretion was reduced with BB-12 (P = 0.002) and GOS (P = 0.020), indicating improvements in colonic permeability but no synergistic effects. No changes in markers of endotoxemia were observed. Conclusion This study demonstrated that “autochthony” of the probiotic strain has a larger effect on ecological performance than the provision of a prebiotic substrate, likely due to competitive interactions with members of the resident microbiota. Although the synbiotic combinations tested in this study did not demonstrate functional synergism, our findings clearly showed that the pro- and prebiotic components by themselves improved markers of colonic permeability, providing a rational for their use in pathologies with an underlying leakiness of the gut.
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spelling doaj.art-29ff2d4a3fd7420a9822ed5fc0f3b9cd2022-12-21T22:39:47ZengBMCMicrobiome2049-26182018-06-016111610.1186/s40168-018-0494-4Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbioticsJanina A. Krumbeck0Heather E. Rasmussen1Robert W. Hutkins2Jennifer Clarke3Krista Shawron4Ali Keshavarzian5Jens Walter6Department of Food Science and Technology, 258 Food Innovation Center Lincoln, University of Nebraska-LincolnDepartment of Clinical Nutrition, Rush University Medical CenterDepartment of Food Science and Technology, 258 Food Innovation Center Lincoln, University of Nebraska-LincolnDepartment of Food Science and Technology, 258 Food Innovation Center Lincoln, University of Nebraska-LincolnDivision of Digestive Diseases and Nutrition, Department of Internal Medicine, Rush University Medical CenterDivision of Digestive Diseases and Nutrition, Department of Internal Medicine, Rush University Medical CenterDepartment of Food Science and Technology, 258 Food Innovation Center Lincoln, University of Nebraska-LincolnAbstract Background One way to improve both the ecological performance and functionality of probiotic bacteria is by combining them with a prebiotic in the form of a synbiotic. However, the degree to which such synbiotic formulations improve probiotic strain functionality in humans has not been tested systematically. Our goal was to use a randomized, double-blind, placebo-controlled, parallel-arm clinical trial in obese humans to compare the ecological and physiological impact of the prebiotic galactooligosaccharides (GOS) and the probiotic strains Bifidobacterium adolescentis IVS-1 (autochthonous and selected via in vivo selection) and Bifidobacterium lactis BB-12 (commercial probiotic allochthonous to the human gut) when used on their own or as synbiotic combinations. After 3 weeks of consumption, strain-specific quantitative real-time PCR and 16S rRNA gene sequencing were performed on fecal samples to assess changes in the microbiota. Intestinal permeability was determined by measuring sugar recovery in urine by GC after consumption of a sugar mixture. Serum-based endotoxin exposure was also assessed. Results IVS-1 reached significantly higher cell numbers in fecal samples than BB-12 (P < 0.01) and, remarkably, its administration induced an increase in total bifidobacteria that was comparable to that of GOS. Although GOS showed a clear bifidogenic effect on the resident gut microbiota, both probiotic strains showed only a non-significant trend of higher fecal cell numbers when administered with GOS. Post-aspirin sucralose:lactulose ratios were reduced in groups IVS-1 (P = 0.050), IVS-1 + GOS (P = 0.022), and GOS (P = 0.010), while sucralose excretion was reduced with BB-12 (P = 0.002) and GOS (P = 0.020), indicating improvements in colonic permeability but no synergistic effects. No changes in markers of endotoxemia were observed. Conclusion This study demonstrated that “autochthony” of the probiotic strain has a larger effect on ecological performance than the provision of a prebiotic substrate, likely due to competitive interactions with members of the resident microbiota. Although the synbiotic combinations tested in this study did not demonstrate functional synergism, our findings clearly showed that the pro- and prebiotic components by themselves improved markers of colonic permeability, providing a rational for their use in pathologies with an underlying leakiness of the gut.http://link.springer.com/article/10.1186/s40168-018-0494-4SynbioticProbioticPrebioticObesityGut barrier functionAutochthonous
spellingShingle Janina A. Krumbeck
Heather E. Rasmussen
Robert W. Hutkins
Jennifer Clarke
Krista Shawron
Ali Keshavarzian
Jens Walter
Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
Microbiome
Synbiotic
Probiotic
Prebiotic
Obesity
Gut barrier function
Autochthonous
title Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
title_full Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
title_fullStr Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
title_full_unstemmed Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
title_short Probiotic Bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
title_sort probiotic bifidobacterium strains and galactooligosaccharides improve intestinal barrier function in obese adults but show no synergism when used together as synbiotics
topic Synbiotic
Probiotic
Prebiotic
Obesity
Gut barrier function
Autochthonous
url http://link.springer.com/article/10.1186/s40168-018-0494-4
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