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Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study

  • Caroline E. Childs (a1) (a2), Henna Röytiö (a3) (a4), Esa Alhoniemi (a5), Agnes A. Fekete (a1), Sofia D. Forssten (a3), Natasa Hudjec (a1), Ying Ni Lim (a1), Cara J. Steger (a1), Parveen Yaqoob (a1), Kieran M. Tuohy (a1) (a6), Robert A. Rastall (a1), Arthur C. Ouwehand (a3) and Glenn R. Gibson (a1)...

Abstract

Prebiotics, probiotics and synbiotics are dietary ingredients with the potential to influence health and mucosal and systemic immune function by altering the composition of the gut microbiota. In the present study, a candidate prebiotic (xylo-oligosaccharide, XOS, 8 g/d), probiotic (Bifidobacterium animalis subsp. lactis Bi-07, 109 colony-forming units (CFU)/d) or synbiotic (8 g XOS+109 CFU Bi-07/d) was given to healthy adults (25–65 years) for 21 d. The aim was to identify the effect of the supplements on bowel habits, self-reported mood, composition of the gut microbiota, blood lipid concentrations and immune function. XOS supplementation increased mean bowel movements per d (P= 0·009), but did not alter the symptoms of bloating, abdominal pain or flatulence or the incidence of any reported adverse events compared with maltodextrin supplementation. XOS supplementation significantly increased participant-reported vitality (P= 0·003) and happiness (P= 0·034). Lowest reported use of analgesics was observed during the XOS+Bi-07 supplementation period (P= 0·004). XOS supplementation significantly increased faecal bifidobacterial counts (P= 0·008) and fasting plasma HDL concentrations (P= 0·005). Bi-07 supplementation significantly increased faecal B. lactis content (P= 0·007), lowered lipopolysaccharide-stimulated IL-4 secretion in whole-blood cultures (P= 0·035) and salivary IgA content (P= 0·040) and increased IL-6 secretion (P= 0·009). XOS supplementation resulted in lower expression of CD16/56 on natural killer T cells (P= 0·027) and lower IL-10 secretion (P= 0·049), while XOS and Bi-07 supplementation reduced the expression of CD19 on B cells (XOS × Bi-07, P= 0·009). The present study demonstrates that XOS induce bifidogenesis, improve aspects of the plasma lipid profile and modulate the markers of immune function in healthy adults. The provision of XOS+Bi-07 as a synbiotic may confer further benefits due to the discrete effects of Bi-07 on the gut microbiota and markers of immune function.

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      Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study
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      Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study
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      Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study
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Corresponding author

* Corresponding author: Dr C. E. Childs, fax +44 2381 204221, email c.e.childs@soton.ac.uk

References

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1 Gibson, GR, Scott, KP, Rastall, RA, et al. (2010) Dietary prebiotics: current status and new definition. Food Sci Technol Bull Funct Foods 7, 119.
2 Imaizumi, K, Nakatsu, Y, Sato, M, et al. (1991) Effects of xylooligosaccharides on blood-glucose, serum and liver lipids and cecum short-chain fatty-acids in diabetic rats. Agr Biol Chem Tokyo 55, 199205.
3 Koga, K & Fujikawa, S (1993) Xylooligosaccharides. In Oligosaccharides: Production, Properties and Applications, Japanese Technology Reviews, 1st ed., pp. 130143 [Nakakuki, T, editor]. Philadelphia, PA: Gordon and Breach Science Publishers.
4 Jaskari, J, Kontula, P, Siitonen, A, et al. (1998) Oat beta-glucan and xylan hydrolysates as selective substrates for Bifidobacterium and Lactobacillus strains. Appl Microbiol Biotechnol 49, 175181.
5 Kontula, P, von Wright, A & Mattila-Sandholm, T (1998) Oat bran beta-gluco- and xylo-oligosaccharides as fermentative substrates for lactic acid bacteria. Int J Food Microbiol 45, 163169.
6 Yong, X, Hua, J, Quiang, Y, et al. (2001) The ability of XOS to promote the proliferation of Bifidobacterium adolescentis . Food Sci 22, 1517.
7 Crittenden, R, Karppinen, S, Ojanen, S, et al. (2002) In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J Sci Food Agr 82, 781789.
8 Palframan, RJ, Gibson, GR & Rastall, RA (2003) Carbohydrate preferences of Bifidobacterium species isolated from the human gut. Curr Issues Intest Microbiol 4, 7175.
9 Makelainen, H, Saarinen, M, Stowell, J, et al. (2010) Xylo-oligosaccharides and lactitol promote the growth of Bifidobacterium lactis and Lactobacillus species in pure cultures. Benef Microbes 1, 139148.
10 Rycroft, CE, Jones, MR, Gibson, GR, et al. (2001) A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J Appl Microbiol 91, 878887.
11 Zampa, A, Silvi, S, Fabiani, R, et al. (2004) Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10, 1926.
12 Makelainen, H, Forssten, S, Saarinen, M, et al. (2010) Xylo-oligosaccharides enhance the growth of bifidobacteria and Bifidobacterium lactis in a simulated colon model. Benef Microbes 1, 8191.
13 Campbell, JM, Fahey, GC Jr & Wolf, BW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. J Nutr 127, 130136.
14 Hsu, CK, Liao, JW, Chung, YC, et al. (2004) Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. J Nutr 134, 15231528.
15 Santos, A, San Mauro, M & Diaz, DM (2006) Prebiotics and their long-term influence on the microbial populations of the mouse bowel. Food Microbiol 23, 498503.
16 Nakakuki, T (2003) Development of functional oligosaccharides in Japan. Trends Glycosci Glyctechnol 15, 5764.
17 Okazaki, M, Fujikawa, S & Matsumoto, M (1990) Effect of xylooligosaccharide on the growth of bifidobacteria. Bifidobact Microflora 9, 7786.
18 Lecerf, JM, Depeint, F, Clerc, E, et al. (2012) 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, 18471858.
19 Iino, T, Nishijima, Y, Sawada, S, et al. (1997) Improvement of constipation by a small amount of XOS ingestion in adult women. J Jap Assoc Dietary Fiber Res 1, 1924.
20 Tateyama, I, Hashii, K, Johno, I, et al. (2005) Effect of xylooligosaccharide intake on severe constipation in pregnant women. J Nutr Sci Vitaminol (Tokyo) 51, 445448.
21 Gibson, GR, Probert, HM, Loo, JV, et al. (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17, 259275.
22 Roberfroid, M (2007) Prebiotics: the concept revisited. J Nutr 137, 830S837S.
23 Roberfroid, M, Gibson, GR, Hoyles, L, et al. (2010) Prebiotic effects: metabolic and health benefits. Br J Nutr 104, S1S63.
24 Ebersbach, T, Jorgensen, JB, Heegaard, PM, et al. (2010) Certain dietary carbohydrates promote Listeria infection in a guinea pig model, while others prevent it. Int J Food Microbiol 140, 218224.
25 Ebersbach, T, Andersen, JB, Bergstrom, A, et al. (2012) Xylo-oligosaccharides inhibit pathogen adhesion to enterocytes in vitro . Res Microbiol 163, 2227.
26 Lomax, AR & Calder, PC (2009) Probiotics, immune function, infection and inflammation: a review of the evidence from studies conducted in humans. Curr Pharm Des 15, 14281518.
27 Ringel-Kulka, T, Palsson, OS, Maier, D, et al. (2011) Probiotic bacteria Lactobacillus acidophilus NCFM and Bifidobacterium lactis Bi-07 versus placebo for the symptoms of bloating in patients with functional bowel disorders: a double-blind study. J Clin Gastroenterol 45, 518525.
28 Leyer, GJ, Li, S, Mubasher, ME, et al. (2009) Probiotic effects on cold and influenza-like symptom incidence and duration in children. Pediatrics 124, e172e179.
29 Rastall, RA & Maitin, V (2002) Prebiotics and synbiotics: towards the next generation. Curr Opin Biotechnol 13, 490496.
30 Erdfelder, E, Faul, F & Buchner, A (1996) GPOWER: a general power analysis program. Behav Res Methods Instrum Comput 28, 111.
31 Gill, HS, Rutherfurd, KJ, Cross, ML, et al. (2001) Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 74, 833839.
32 Roessler, A, Friedrich, U, Vogelsang, H, et al. (2008) The immune system in healthy adults and patients with atopic dermatitis seems to be affected differently by a probiotic intervention. Clin Exp Allergy 38, 93102.
33 Seidel, C, Boehm, V, Vogelsang, H, et al. (2007) Influence of prebiotics and antioxidants in bread on the immune system, antioxidative status and antioxidative capacity in male smokers and non-smokers. Br J Nutr 97, 349356.
34 Roller, M, Clune, Y, Collins, K, et al. (2007) Consumption of prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis has minor effects on selected immune parameters in polypectomised and colon cancer patients. Br J Nutr 97, 676684.
35 Kang, M, Ragan, BG & Park, JH (2008) Issues in outcomes research: an overview of randomization techniques for clinical trials. J Athl Train 43, 215221.
36 Costabile, A, Kolida, S, Klinder, A, et al. (2010) 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, 10071017.
37 Ventura, M, Reniero, R & Zink, R (2001) Specific identification and targeted characterization of Bifidobacterium lactis from different environmental isolates by a combined multiplex-PCR approach. Appl Environ Microbiol 67, 27602765.
38 Apajalahti, JH, Kettunen, H, Kettunen, A, et al. (2002) Culture-independent microbial community analysis reveals that inulin in the diet primarily affects previously unknown bacteria in the mouse cecum. Appl Environ Microbiol 68, 49864995.
39 Richardson, AJ, Calder, AG, Stewart, CS, et al. (1989) Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas-chromatography. Lett Appl Microbiol 9, 58.
40 Costabile, A, Fava, F, Roytio, H, et al. (2012) Impact of polydextrose on the faecal microbiota: a double-blind, crossover, placebo-controlled feeding study in healthy human subjects. Br J Nutr 108, 471481.
41 Hothorn, T, Bretz, F & Westfall, P (2008) Simultaneous inference in general parametric models. Biom J 50, 346363.
42 Shepherd, J (2005) Raising HDL-cholesterol and lowering CHD risk: does intervention work? Eur Heart J 7, F15F22.
43 Gordon, DJ, Probstfield, JL, Garrison, RJ, et al. (1989) High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies. Circulation 79, 815.
44 Delzenne, NM & Williams, CM (2002) Prebiotics and lipid metabolism. Curr Opin Lipidol 13, 6167.
45 Ooi, L-G & Liong, M-T (2010) Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. In J Mol Sci 11, 24992522.
46 Lomax, AR & Calder, PC (2009) Prebiotics, Immune function, infection and inflammation: a review of the evidence. Br J Nutr 101, 633658.
47 Bermudez-Brito, M, Plaza-Díaz, J, Muñoz Quezada, S, et al. (2012) Probiotic mechanisms of action. Ann Nutr Metab 61, 160174.
48 Albers, R, Antoine, JM, Bourdet-Sicard, R, et al. (2005) Markers to measure immunomodulation in human nutrition intervention studies. Br J Nutr 94, 452481.

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Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study

  • Caroline E. Childs (a1) (a2), Henna Röytiö (a3) (a4), Esa Alhoniemi (a5), Agnes A. Fekete (a1), Sofia D. Forssten (a3), Natasa Hudjec (a1), Ying Ni Lim (a1), Cara J. Steger (a1), Parveen Yaqoob (a1), Kieran M. Tuohy (a1) (a6), Robert A. Rastall (a1), Arthur C. Ouwehand (a3) and Glenn R. Gibson (a1)...

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