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

Microbiome

Volumn 6, Issue 1, 2018, Pages

  Krumbeck, Janina A ^a   Rasmussen, Heather E ^b   Hutkins, Robert W ^a   Clarke, Jennifer ^a   Shawron, Krista ^b   Keshavarzian, Ali ^b   Walter, Jens ^a,c,d  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d Department of Biological Sciences ^*  (Canada)

Author keywords

Allochthonous; Autochthonous; Bifidobacteria; Bifidobacterium; Galactooligosaccharide; Gut barrier function; Obesity; Prebiotic; Probiotic; Synbiotic

Indexed keywords

ENDOTOXIN; GALACTOSE OLIGOSACCHARIDE; LACTULOSE; LIPOPOLYSACCHARIDE BINDING PROTEIN; PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT; RNA 16S; SUCRALOSE; SYNBIOTIC AGENT; OLIGOSACCHARIDE; SUCROSE; TRICHLOROSUCROSE;

ABDOMINAL DISCOMFORT; ABDOMINAL PAIN; ACTINOBACTERIA; ADOLESCENT; ADULT; ANTHROPOMETRY; ARTICLE; BACTERIUM IDENTIFICATION; BIFIDOBACTERIUM ADOLESCENTIS; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM PSEUDOCATENULATUM; CLINICAL FEATURE; COLONY FORMING UNIT; CONTROLLED STUDY; DEMOGRAPHY; DIETARY INTAKE; DNA ISOLATION; DOUBLE BLIND PROCEDURE; ENDOTOXEMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES ANALYSIS; FECES MICROFLORA; FEMALE; FLATULENCE; GASTROINTESTINAL SYMPTOM; GENE SEQUENCE; HUMAN; INTESTINE MUCOSA PERMEABILITY; LACTOSE INTOLERANCE; LIMIT OF DETECTION; MALE; OBESITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REAL TIME POLYMERASE CHAIN REACTION; STRUCTURED QUESTIONNAIRE; URINALYSIS; ANALOGS AND DERIVATIVES; BIFIDOBACTERIUM; DRUG EFFECT; GENETICS; INTESTINE; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; MIDDLE AGED; PHYSIOLOGY; TIGHT JUNCTION; YOUNG ADULT;

ADULT; BIFIDOBACTERIUM; DOUBLE-BLIND METHOD; ENDOTOXEMIA; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINES; MALE; MIDDLE AGED; OBESITY; OLIGOSACCHARIDES; PREBIOTICS; PROBIOTICS; RNA, RIBOSOMAL, 16S; SUCROSE; SYNBIOTICS; TIGHT JUNCTIONS; YOUNG ADULT;

EID: 85049211175     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/s40168-018-0494-4     Document Type: Article

References (100)

1. Joyce SA, Gahan CGM. The gut microbiota and the metabolic health of the host. Curr Opin Gastroenterol. 2014;30:120-7.
2. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148:1258-70.
3. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012;9:577-89.
4. Marchesi JR, Adams DH, Fava F, Hermes GDA, Hirschfield GM, et al. The gut microbiota and host health: a new clinical frontier. Gut. 2015;65:330-9.
5. Sommer F, Bäckhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol. 2013;11:227-38.
6. Cani PD, Everard A. Talking microbes: when gut bacteria interact with diet and host organs. Mol Nutr Food Res. 2016;60:58-66.
7. Tran CD, Grice DM, Wade B, Kerr CA, Bauer DC, et al. Gut permeability, its interaction with gut microflora and effects on metabolic health are mediated by the lymphatics system, liver and bile acid. Future Microbiol. 2015;10:1339-53.
8. Farhadi A, Banan A, Fields J, Keshavarzian A. Intestinal barrier: an interface between health and disease. J Gastroenterol Hepatol. 2003;18:479-97.
9. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500:541-6.
10. Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105:141-50.
11. Zeyda M, Stulnig TM. Obesity, inflammation, and insulin resistance-a mini-review. Gerontology. 2009;55:379-86.
12. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761-72.
13. Neves AL, Coelho J, Couto L, Leite-Moreira A, Roncon-Albuquerque R. Metabolic endotoxemia: a molecular link between obesity and cardiovascular risk. J Mol Endocrinol. 2013;51:R51-64.
14. Cani PD. Interactions between gut microbes and host cells control gut barrier and metabolism. Int J Obes Suppl. 2016;6:S28-31.
15. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, et al. Changes in gut microbiota control metabolic diet-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470-81.
16. Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes. 2012;3:279-88.
17. Akbari P, Braber S, Alizadeh A, Verheijden K, Schoterman M, et al. Galacto-oligosaccharides protect the intestinal barrier by maintaining the tight junction network and modulating the inflammatory responses after a challenge with the mycotoxin deoxynivalenol in human Caco-2 cell monolayers and B6C3F1 mice. J Nutr. 2015;145:1604-13.
18. Akbari P, Fink-Gremmels J, Willems RHAM, Difilippo E, Schols HA, et al. Characterizing microbiota-independent effects of oligosaccharides on intestinal epithelial cells: insight into the role of structure and size: structure-activity relationships of non-digestible oligosaccharides. Eur J Nutr. 2017;56:1919-30.
19. Alizadeh A, Akbari P, Difilippo E, Schols HA, Ulfman LH, et al. The piglet as a model for studying dietary components in infant diets: effects of galacto-oligosaccharides on intestinal functions. Br J Nutr. 2015;115:605-18.
20. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001;121:580-91.
21. Hsieh C-Y, Osaka T, Moriyama E, Date Y, Kikuchi J, et al. Strengthening of the intestinal epithelial tight junction by Bifidobacterium bifidum. Physiol Rep. 2015;3:e12327.
22. Guo S, Gillingham T, Guo Y, Meng D, Zhu W, Walker WA, et al. Secretions of Bifidobacterium infantis and Lactobacillus acidophilus protect intestinal epithelial barrier function. J Pediatr Gastroenterol Nutr. 2017;64:404-12.
23. Anderson RC, Cookson AL, McNabb WC, Kelly WJ, Roy N. Lactobacillus plantarum DSM 2648 is a potential probiotic that enhances intestinal barrier function. FEMS Microbiol Lett. 2010;309:184-92.
24. Mujagic Z, De Vos P, Boekschoten MV, Govers C, Pieters HJH, De Wit NJ, et al. The effects of Lactobacillus plantarum on small intestinal barrier function and mucosal gene transcription; a randomized double-blind placebo controlled trial. Sci Rep. 2017;4:40128.
25. Ren C, Dokter-Fokkens J, Figueroa Lozano S, Zhang Q, Haan BJ, et al. Lactic acid bacteria may impact intestinal barrier function by modulating goblet cells. Mol Nutr Food Res. 2018;62:1700572.
26. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007;50:2374-83.
27. Cani PD, Delzenne NM. Interplay between obesity and associated metabolic disorders: new insights into the gut microbiota. Curr Opin Pharmacol. 2009;9:737-43.
28. Mills DA. Probiotic nomenclature matters redux: confusion on Bifidobacterium longum subsp. infantis taxonomy persists. Curr Med Res Opin. 2017;33:2097.
29. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, et al. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol. 2008;295:G1025-34.
30. Bergmann KR, Liu SXL, Tian R, Kushnir A, Turner JR, et al. Bifidobacteria stabilize claudins at tight junctions and prevent intestinal barrier dysfunction in mouse necrotizing enterocolitis. Am J Pathol. 2013;182:1596-606.
31. Griffiths EA, Duffy LC, Schanbacher FL, Qiao H, Dryja D, et al. In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in balb/c mice. Dig Dis Sci. 2004;49:579-89.
32. Wang Z, Xiao G, Yao Y, Guo S, Lu K, et al. The role of bifidobacteria in gut barrier function after thermal injury in rats. J Trauma-Injury Infect Crit Care. 2006;61:650-7.
33. Chen J, Wang RR-L, Li X-F, Wang RR-L. Bifidobacterium adolescentis supplementation ameliorates visceral fat accumulation and insulin sensitivity in an experimental model of the metabolic syndrome. Br J Nutr. 2012;107:1429-34.
34. Reichold A, Brenner SA, Spruss A, Förster-Fromme K, Bergheim I, et al. Bifidobacterium adolescentis protects from the development of nonalcoholic steatohepatitis in a mouse model. J Nutr Biochem. 2014;25:118-25.
35. Martínez I, Wallace G, Zhang C, Legge R, Benson AK, et al. Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol. 2009;75:4175-84.
36. Fanaro S, Marten B, Bagna R, Vigi V, Fabris C, et al. Galacto-oligosaccharides are bifidogenic and safe at weaning: a double-blind randomized multicenter study. J Pediatr Gastroenterol Nutr. 2009;48:82-8.
37. Sierra C, Bernal M-J, Blasco J, Martinez R, Dalmau J, et al. Prebiotic effect during the first year of life in healthy infants fed formula containing GOS as the only prebiotic: a multicentre, randomised, double-blind and placebo-controlled trial. Eur J Nutr. 2015;54:89-99.
38. Haarman M, Knol J. Quantitative real-time PCR analysis of fecal Lactobacillus species in infants receiving a prebiotic infant formula. Appl Environ Microbiol. 2006;72:2359-65.
39. Davis LMG, Martínez I, Walter J, Hutkins R. A dose dependent impact of prebiotic galactooligosaccharides on the intestinal microbiota of healthy adults. Int J Food Microbiol. 2010;144:285-92.
40. Walton GE, van den Heuvel EGHM, Kosters MHW, Rastall RA, Tuohy KM, et al. A randomised crossover study investigating the effects of galacto-oligosaccharides on the faecal microbiota in men and women over 50 years of age. Br J Nutr. 2012;107:1466-75.
41. Vulevic J, Juric A, Tzortzis G, Gibson GR. A mixture of trans-galactooligosaccharides reduces markers of metabolic syndrome and modulates the fecal microbiota and immune function of overweight adults. J Nutr. 2013:324-31.
42. Bouhnik Y, Raskine L, Simoneau G, Paineau D, Bornet F. The capacity of short-chain fructo-oligosaccharides to stimulate faecal bifidobacteria: a dose-response relationship study in healthy humans. Nutr J. 2006;5:8.
43. Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, et al. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr. 2008;101:541-50.
44. Clarke ST, Brooks SP, Inglis GD, Yanke LJ, Green J, Petronella N., Ramdath DD, Bercik P, Green-Johnson JM, Kalmokoff M. Impact of β2-1 fructan on faecal community change: results from a placebo-controlled, randomised, double-blinded, cross-over study in healthy adults. Br J Nutr. 2017;118:441-53.
45. Davis L, Martínez I, Walter J, Goin C, Hutkins RW. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS One. 2011;6:e25200.
46. Martínez I, Kim J, Duffy PR, Schlegel VL, Walter J. Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS One. 2010;5:e15046.
47. Ringel-Kulka T, Cheng J, Ringel Y, Salojärvi J, Carroll I, et al. Intestinal microbiota in healthy U.S. young children and adults-a high throughput microarray analysis. PLoS One. 2013;8:e64315.
48. Agans R, Rigsbee L, Kenche H, Michail S, Khamis HJ, et al. Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol. 2011;77:404-12.
49. Salonen A, Lahti L, Salojärvi J, Holtrop G, Korpela K, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014;8:2218-30.
50. Venkataraman A, Sieber JR, Schmidt AW, Waldron C, Theis KR, et al. Variable responses of human microbiomes to dietary supplementation with resistant starch. Microbiome. 2016;4:33.
51. Kolida S, Gibson GR. Synbiotics in health and disease. Annu Rev Food Sci Technol. 2011;2:373-93.
52. Mallon CA, Van Elsas JD, Salles JF. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol. 2015;23:719-29.
53. Walter J, Maldonado-Gómez MX, Martínez I. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes. Curr Opin Biotechnol. 2017;49:129-39.
54. Freitas MB, Moreira EAM, de Lima Oliveira D, Tomio C, Rosa JS, Moreno YMF, et al. Effect of synbiotic supplementation in children and adolescents with cystic fibrosis: a randomized controlled clinical trial. Eur J Clin Nutr.2018;72:736-43.
55. Panigrahi P, Parida S, Nanda NC, Satpathy R, Pradhan L, et al. A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature. Epub ahead of print 2017. https://doi.org/10.1038/nature23480.
56. Rossi M, Johnson DW, Morrison M, Pascoe EM, Coombes JS, et al. Synbiotics easing renal failure by improving gut microbiology (SYNERGY): a randomized trial. Clin J Am Soc Nephrol. 2016;11:223-31.
57. Ogawa T, Asai Y, Yasuda K, Sakamoto H. Oral immunoadjuvant activity of a new synbiotic Lactobacillus casei subsp casei in conjunction with dextran in BALB/c mice. Nutr Res. 2005;25:295-304.
58. Tanaka R, Takayama H, Morotomi M, Kuroshima T, Ueyama S, et al. Effects of administration of TOS and Bifidobacterium breve 4006 on the human fecal flora. Bifidobact Microflora. 1983;2:17-24.
59. Pietro FA, Luceri C, Dolara P, Giannini A, Biggeri A, et al. Antitumorigenic activity of the prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis on azoxymethane-induced colon carcinogenesis in rats. Carcinogenesis. 2002;23:1953-60.
60. Wang X, Brown IL, Evans AJ, Conway PL. The protective effects of high amylose maize (amylomaize) starch granules on the survival of Bifidobacterium spp. in the mouse intestinal tract. J Appl Microbiol. 1999;87:631-9.
61. Krumbeck JA, Maldonado-Gomez MX, Martínez I, Frese SA, Burkey TE, et al. In vivo selection to identify bacterial strains with enhanced ecological performance in synbiotic applications. Appl Environ Microbiol. 2015;81:2455-65.
62. Krumbeck JA, Walter J, Hutkins RW. Synbiotics for improved human health: recent developments, challenges, and opportunities. Annu Rev Food Sci Technol. 2018;9:451-79.
63. Maldonado-Gómez MX, Martínez I, Bottacini F, O'Callaghan A, Ventura M, et al. Stable engraftment of Bifidobacterium longum AH1206 in the human gastrointestinal tract depends on individualized features of the resident microbiome. Cell Host Microbe. 2016;20:515-26.
64. Bindels LB, Munoz RRS, Gomes-Neto JC, Mutemberezi V, Martínez I, Salazar N, et al. Resistant starch can improve insulin sensitivity independently of the gut microbiota. Microbiome. 2017;5:12.
65. Wu RY, Määttänen P, Napper S, Scruten E, Li B, et al. Non-digestible oligosaccharides directly regulate host kinome to modulate host inflammatory responses without alterations in the gut microbiota. Microbiome. 2017;5:135.
66. Fransen F, Sahasrabudhe NM, Elderman M, Bosveld M, El Aidy S, Hugenholtz F, et al. β2→ 1-fructans modulate the immune system in vivo in a microbiota-dependent and-independent fashion. Front Immunol. 2017;8:154.
67. Pokusaeva K, Fitzgerald GF, Sinderen D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 2011;6:285.
68. Vernazza CL, Gibson GR, Rastall R. Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol. 2006;100:846-53.
69. Thongaram T, Hoeflinger JL, Chow J, Miller MJ. Prebiotic galactooligosaccharide metabolism by probiotic lactobacilli and bifidobacteria. J Agric Food Chem. 2017;65:4184-92.
70. Alander M, Mättö J, Kneifel W, Johansson M, Koegle B, et al. Effect of galacto-oligosaccharide supplementation on human faecal microflora and on survival and persistence of Bifidobacterium lactis Bb-12 in the gastrointestinal tract. Int Dair. 2001;11:817-25.
71. Malinen E, Mättö J, Salmitie M, Alander M, Saarela M, et al. PCR-ELISA II: analysis of Bifidobacterium populations in human faecal samples from a consumption trial with Bifidobacterium lactis Bb-12 and a galacto-oligosaccharide preparation. Syst Appl Microbiol. 2002;25:249-58.
72. Satokari RM, Vaughan EE, Akkermans AD, Saarela M, de Vos WM. Polymerase chain reaction and denaturing gradient gel electrophoresis monitoring of fecal Bifidobacterium populations in a prebiotic and probiotic feeding trial. Syst Appl Microbiol. 2001;231:227-31.
73. Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome. 2017;5:1-18.
74. Taipale T, Pienihäkkinen K, Isolauri E, Larsen C, Brockmann E, et al. Bifidobacterium animalis subsp. lactis BB-12 in reducing the risk of infections in infancy. Br J Nutr. 2010;105:409-16.
75. Shaikh M, Rajan K, Forsyth CB, Voigt RM, Keshavarzian A. Simultaneous gas-chromatographic urinary measurement of sugar probes to assess intestinal permeability: use of time course analysis to optimize its use to assess regional gut permeability. Clin Chim Acta. 2015;10:24-32.
76. Farhadi A, Gundlapalli S, Shaikh M, Frantzides C, Harrell L, et al. Susceptibility to gut leakiness: a possible mechanism for endotoxaemia in non-alcoholic steatohepatitis. Liver Int. 2008;28:1026-33.
77. Hilsden R, Meddings J, Sutherland L. Intestinal permeability changes in response to acetylsalicylic acid in relatives of patients with Crohn's disease. Gastroenterology. 1996;110:1395-403.
78. Ben X-M, Li J, Feng Z-T, Shi S-Y, Lu Y-D, et al. Low level of galacto-oligosaccharide in infant formula stimulates growth of intestinal bifidobacteria and lactobacilli. World J Gastroenterol. 2008;14:6564-8.
79. Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr. 2008;88:1438-46.
80. Chandel D, Perez-Munoz M, Yu F, Boissy R, Satpathy R, et al. Changes in the gut microbiota after early administration of oral synbiotics to young infants in India. J Pediatr Gastroenterol Nutr. 2017;65:218-24.
81. Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, De Vadder F, et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab. 2015;22:971-82.
82. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science (80- ). 2011;334:105-9.
83. Hjorth MF, Roager HM, Larsen TM, Poulsen SK, Licht TR, et al. Pre-treatment microbial Prevotella-to-Bacteroides ratio, determines body fat loss success during a 6-month randomized controlled diet intervention. Int J Obes. 2018;42:580-3.
84. Angelakis E, Lagier J-C. Samples and techniques highlighting the links between obesity and microbiota Microb Pathog Epub ahead of print 2016. https://doi.org/10.1016/j.micpath.2016.01.024.
85. Blekhman R, Goodrich JK, Huang K, Sun Q, Bukowski R, et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 2015;16:191.
86. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Courtney C, et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 2007;39:31-40.
87. Szilagyi A. Redefining lactose as a conditional prebiotic. Can J Gastroenterol. 2004;18:163-7.
88. Parche S, Jacobs D, Arigoni F, Titgemeyer F, Jankovic I. Lactose-over-glucose preference in Bifidobacterium longum NCC2705: glcP, encoding a glucose transporter, is subject to lactose repression. J Bacteriol. 2006;188:1260-5.
89. Azcarate-Peril MA, Ritter AJ, Savaiano D, Monteagudo-Mera A, Anderson C, Magness ST, Klaenhammer TR. Impact of short-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals. PNAS. 2017;114:E367-75.
90. Antoni L, Nuding S, Wehkamp J, Stange EF. Intestinal barrier in inflammatory bowel disease. World J Gastrointerol. 2014;20:1165-79.
91. Scarpellini E, Lupo M, Iegri C, Gasbarrini A, De Santis A, et al. Intestinal permeability in non-alcoholic fatty liver disease: the gut-liver axis. Rev Recent Clin Trials. 2014;9:141-7.
92. Forsyth C, Shannon K, Kordower J, Voigt R, Shaikh M, et al. Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS One. 2011;6:e28032.
93. Zhong Y, Cai D, Cai W, Geng S, Chen L, et al. Protective effect of galactooligosaccharide-supplemented enteral nutrition on intestinal barrier function in rats with severe acute pancreatitis. Clin Nutr. 2009;28:575-80.
94. Martín R, Laval L, Chain F, Miquel S, Natividad J, et al. Bifidobacterium animalis ssp. lactis CNCM-I2494 restores gut barrier permeability in chronically low-grade inflamed mice. Front Microbiol. 2016;7:1-12.
95. Agostini S, Goubern M, Tondereau V, Salvador-Cartier C, Bezirard V, et al. A marketed fermented dairy product containing Bifidobacterium lactis CNCM I-2494 suppresses gut hypersensitivity and colonic barrier disruption induced by acute stress in rats. Neurogastroenterol Motil. 2012;24:376-e172.
96. Schroeder B, Birchenough GM, Stahlman M, Arike L, Johansson ME, et al. Bifidobacteria or fiber protects against diet-induced microbiota-mediated colonic mucus deterioration. Cell Host Microbe. 2018;23:27-40.e7.
97. Morel F, Dai Q, Ni J, Thomas D, Parnet P, et al. α-Galacto-oligosaccharides dose-dependently reduce appetite and decrease inflammation in overweight adults. J Nutr. 2015;145:2052-9.
98. Rodes L, Saha S, Tomaro-Duchesneau C, Prakash S. Microencapsulated Bifidobacterium longum subsp. infantis ATCC 15697 favorably modulates gut microbiota and reduces circulating endotoxins in F344 rats. Biomed Res Int. 2014;602832. https://www.hindawi.com/journals/bmri/2014/602832/abs/.
99. Canfora EE, van der Beek, Christina M Hermes GDA, Gijs GH, Jocken JWE, Holst JJ, et al. Supplementation of diet with galacto-oligosaccharides increases bifidobacteria, but not insulin sensitivity, in obese prediabetic individuals. Gastroenterology. 2017;153:87-97.e3.
100. Carvalho-Wells AL, Helmolz K, Nodet C, Molzer C, Leonard C, et al. Determination of the in vivo prebiotic potential of a maize-based whole grain breakfast cereal: a human feeding study. Br J Nutr. 2010;104:1353-6.