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Combination of polydextrose and lactitol affects microbial ecosystem and immune responses in rat gastrointestinal tract

Published online by Cambridge University Press:  09 March 2007

Seppo Peuranen ,
Kirsti Tiihonen ,
Juha Apajalahti ,
Anu Kettunen ,
Markku Saarinen  and
Nina Rautonen
Seppo Peuranen*
Affiliation:
Danisco Innovation, Enteromix Research, Sokeritehtaantie 20, FIN-02460 Kantvik, Finland
Kirsti Tiihonen
Affiliation:
Danisco Innovation, Enteromix Research, Sokeritehtaantie 20, FIN-02460 Kantvik, Finland
Juha Apajalahti
Affiliation:
Danisco Innovation, Enteromix Research, Sokeritehtaantie 20, FIN-02460 Kantvik, Finland
Anu Kettunen
Affiliation:
Danisco Innovation, Enteromix Research, Sokeritehtaantie 20, FIN-02460 Kantvik, Finland
Markku Saarinen
Affiliation:
Danisco Innovation, Enteromix Research, Sokeritehtaantie 20, FIN-02460 Kantvik, Finland
Nina Rautonen
Affiliation:
Danisco Innovation, Enteromix Research, Sokeritehtaantie 20, FIN-02460 Kantvik, Finland
*
*Corresponding author: Dr Seppo Peuranen, fax +358 9 298 2203, email [email protected]
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Abstract

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The effects of various dietary fibres on gut health have been studied extensively but their combined effects are scarcely documented. In the present study the effects of 2 % (w/w) polydextrose (PDX), 2 % (w/w) disaccharide lactitol, or 2 % (w/w) PDX+2 % (w/w) lactitol on gut microflora, microbial metabolism and gut immune responses were investigated in rats. Both PDX and lactitol alone had an effect on many of the studied parameters, but their combination had stronger than additive effects in some parameters. The PDX+lactitol combination altered the microbial community structure as seen by a culture-independent method, percentage guanine+cytosine (%G+C) profiling, increasing the areas of %G+C 35–39 (P<0·0001) and %G+C 45–49 (P=0·0002), and decreasing %G+C 65–74 (P<0·0003). These changes were also reflected in the microbial metabolism so that the production of biogenic amines and branched volatile fatty acids was significantly reduced, by 12 (P=0·03) and 50 % (P=0·002), respectively, indicating a shift from putrefactive towards saccharolytic metabolism. PDX increased the secretion of IgA in the caecum (P=0·007). Secretion of IgA increased even more, almost ten-fold, with the combination of PDX+lactitol (P<0·0001) when compared with the control group. Lactitol increased the production of butyrate by caecal microbes by two- to three-fold when compared with the PDX or control group (P<0·0001). Butyrate is a preferred energy source for mucosal cells; thus a boost in the availability of energy for immune cells may have still added to the synergistic effects of PDX and lactitol on immune cells. It is noteworthy that improvement in the IgA secretion occurred without signs of mucosal inflammation.

Keywords

PolydextroseLactitolMicrobial metabolismImmunoglobulin A
Type
Research Article
Information
British Journal of Nutrition , Volume 91 , Issue 6 , June 2004 , pp. 905 - 914
Copyright
Copyright © The Nutrition Society 2004

References

Abrahamse, SL, Pool-Zobel, BL & Rechkemmer, G (1999) Potential of short chain fatty acids to modulate the induction of DNA damage and changes in the intracellular calcium concentration by oxidative stress in isolated rat distal colon cells. Carcinogenesis 20, 629–634.CrossRefGoogle ScholarPubMed
Apajalahti, JHA, Sarkilahti, LK, Maki, BR, Heikkinen, JP, Nurminen, PH & Holben, WE (1998) Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol 64, 4084–4088.CrossRefGoogle ScholarPubMed
Apajalahti, JHA, Kettunen, A, Bedford, MR & Holben, WE (2001) Percent G+C profiling accurately reveals diet-related differences in the gastrointestinal microbial community of broiler chickens. Appl Environ Microbiol 67, 5656–5667.Google Scholar
Apajalahti, JHA, Kettunen, H, Kettunen, A, Holben, WE, Nurminen, PH, Rautonen, N & Mutanen, M (2002) Culture-independent microbial community analysis reveals that inulin in the diet primarily affects previously unknown bacteria in the mouse caecum. Appl Environ Microbiol 68, 4986–4995.Google Scholar
Cheng, BO, Trimble, RP, Illman, RJ, Stone, BA & Topping, DL (1987) Comparative effects of dietary wheat bran and its morphological components (aleurone and pericarp-seed coat) on volatile fatty acid concentrations in the rat. Br J Nutr 57, 69–76.Google Scholar
Coffman, RL, Lebman, DA & Schrader, B (1989) Transforming growth factor β specifically enhances IgA production by lipopolysaccharide-stimulated murine B lymphocytes. J Exp Med 170, 1039–1044.Google Scholar
Craig, SA, Holden, JF & Khaled, MY (2001) Determination of polydextrose in foods by ion chromatography: collaborative study. J AOAC Int 84, 472–478.Google Scholar
Cummings, JH & Macfarlane, GT (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70, 443–459.CrossRefGoogle ScholarPubMed
Cummings, JH, Pomare, EW, Branch, WJ, Naylor, CP & Macfarlane, GT (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 1221–1227.Google Scholar
Delzenne, NM, Kok, N, Deloyer, P & Dandrifosse, G (2000) Dietary fructans modulate polyamine concentrations in the cecum of rats. J Nutr 130, 2456–2460.Google ScholarPubMed
Dirks, P & Freeman, HJ (1987) Effects of differing purified cellulose, pectin and hemicellulose fiber diets on mucosal morphology in the rat small and large intestine. Clin Invest Med 10, 32–38.Google ScholarPubMed
Djouzi, Z, Andrieux, C, Pelenc, V, Somarriba, S, Popot, F, Paul, F, Monsan, P & Szylit, O (1995) Degradation and fermentation of alpha-gluco-oligosaccharides by bacterial strains from human colon: in vitro and in vivo studies in gnotobiotic rats. J Appl Bacteriol 79, 117–127.Google Scholar
Endo, K, Kumemura, M, Nakamura, K, Fujisawa, T, Suzuki, K, Benno, Y & Mitsuoka, T (1991) Effect of high cholesterol diet and polydextrose supplementation on the microflora, bacterial enzyme activity, putrefactive products, volatile fatty acid (VFA) profile, weight, and pH of the feces in healthy volunteers. Bifidobact Microflora 10, 53–64.CrossRefGoogle Scholar
Galluser, M, Czernichow, B, Dreyfus, H, Gosse, F, Guerold, B, Kachelhoffer, J, Doffoel, M & Raul, F (1993) Comparison of different lipid substrates on intestinal adaptation in the rat. Gut 34, 1069–1074.CrossRefGoogle ScholarPubMed
Gamet, L, Daviaud, D, Denis-Pouxviel, C, Remesy, C & Murat, JC (1992) Effects of short-chain fatty acids on growth and differentiation of the human colon-cancer cell line HT29. Int J Cancer 52, 286–289.CrossRefGoogle ScholarPubMed
Gionchetti, P, Campieri, M, Belluzzi, A et al. (1992) Interleukin 1 beta (IL-1 beta) release from fresh and cultured colonic mucosa in patients with ulcerative colitis (UC). Agents Actions (Special Conference Issue) 35, C50–C52.CrossRefGoogle Scholar
Goodlad, JS & Mathers, JC (1990) Large bowel fermentation in rats given diets containing raw peas (Pisum sativum). Br J Nutr 64, 569–587.CrossRefGoogle ScholarPubMed
Govers, MJAP, Gannon, NJ, Dunshea, FR, Gibson, PR & Muir, JG (1999) Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs. Gut 45, 840–847.CrossRefGoogle Scholar
Gyires, K (1994) Some of the factors that may mediate or modify the gastrointestinal mucosal damage induced by non-steroidal anti-inflammatory drugs. Agents Actions 41, 73–79.Google Scholar
Hara, H, Suzuki, T & Aoyama, Y (2000) Ingestion of the soluble dietary fibre, polydextrose, increases calcium absorption and bone mineralization in normal and total-gastrectomized rats. Br J Nutr 84, 655–661.CrossRefGoogle ScholarPubMed
Holben, WE, Sarkilahti, LK, Williams, P, Saarinen, M & Apajalahti, JHA (2002) Phylogenetic analysis of intestinal microflora indicates a novel Mycoplasma phylotype in farmed and wild salmon. Microb Ecol 44, 175–185.CrossRefGoogle ScholarPubMed
Jie, Z, Bang-Yao, L, Ming-Jie, X, Hai-Wei, L, Zu-Kang, Z, Ting-Song, W & Craig, SA (2000) Studies on the effects of polydextrose intake on physiologic functions in Chinese people. Am J Clin Nutr 72, 1503–1509.CrossRefGoogle ScholarPubMed
Kaila, M, Isolauri, E, Soppi, E, Virtanen, E, Laine, S & Arvilommi, H (1992) Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res 32, 141–144.CrossRefGoogle ScholarPubMed
Keenan, KP, Sharpnack, DD, Collins, H, Formal, SB & O'Brien, AD (1986) Morphologic evaluation of the effects of Shiga toxin and E coli Shiga-like toxin on the rabbit intestine. Am J Pathol 125, 69–80.Google Scholar
Kelsall, B & Strober, W (1999) Gut-associated lymphoid tissue. Antigen handling and T-lymphocyte responses. In Mucosal Immunology, pp. 293–313 [Pearay, L, Mestecky, J, Lamm, ME, Strober, W, Bienenstock, J and McGhee, JR, editors]. New York: Academic Press.Google Scholar
Larkin, HA & Hannan, J (1984) Intestinal absorption and structure in iron deficient piglets. Res Vet Sci 36, 199–204.Google Scholar
Lee, A & Storey, DM (1999) Comparative gastrointestinal tolerance of sucrose, lactitol, or D-tagatose in chocolate. Regul Toxicol Pharmacol 29, S78–S82.CrossRefGoogle ScholarPubMed
Letterio, JJ & Roberts, AB (1998) Regulation of immune responses by TGF-beta. Annu Rev Immunol 16, 137–161.CrossRefGoogle ScholarPubMed
Levin, B (1992) Ulcerative colitis and colon cancer: biology and surveillance. J Cell Biochem 16, Suppl.47–50.CrossRefGoogle Scholar
Livesey, G, Johnson, IT, Gee, JM, Smith, T, Lee, WE, Hillan, KA, Meyer, J & Turner, SC (1993) ‘Determination’ of sugar alcohol and polydextrose absorption in humans by the breath hydrogen (H 2 ) technique: the stoichiometry of hydrogen production and the interaction between carbohydrates assessed in vivo and in vitro. Eur J Clin Nutr 47, 419–430.Google Scholar
McDonald, DE, Pethick, DW, Mullan, DP & Hampson, DJ (2001) Increasing viscosity of the intestinal contents alters small intestinal structure and intestinal growth, and stimulates proliferation of enterotoxigenic Escherichia coli in newly-weaned pigs. Br J Nutr 86, 487–498.Google Scholar
Macfarlane, GT, Cummings, JH & Allison, C (1986) Protein degradation by human intestinal bacteria. J Gen Microbiol 132, 1647–1656.Google ScholarPubMed
McGee, DW, Vitkus, SJ & Lee, P (1996) The effect of cytokine stimulation on IL-1 receptor mRNA expression by intestinal epithelial cells. Cell Immunol 168, 276–280.CrossRefGoogle ScholarPubMed
Masini, A, Efrati, C, Merli, M, Attili, AF, Amodio, P, Ceccanti, M & Riggio, O (1999) Effect of lactitol on blood ammonia response to oral glutamine challenge in cirrhotic patients: evidence for an effect of nonabsorbable disaccharides on small intestine ammonia generation. Am J Gastroenterol 94, 3323–3327.CrossRefGoogle ScholarPubMed
Mitsuoka, T (1996) Intestinal flora and human health. Asia Pacific J Clin Nutr 1, 2–9.Google Scholar
Natah, SS, Hussien, KR, Tuominen, JA & Koivisto, VA (1997) Metabolic response to lactitol and xylitol in healthy men. Am J Clin Nutr 65, 947–950.Google Scholar
Noack, J, Kleessen, B, Proll, J, Dongowski, G & Blaut, M (1998) Dietary guar gum and pectin stimulate intestinal microbial polyamine synthesis in rats. J Nutr 128, 1385–1391.Google Scholar
Oku, T, Fujii, Y & Okamatsu, H (1991) Polydextrose as dietary fiber: hydrolysis by digestive enzymes and its effects on gastrointestinal transit time in rats. J Clin Biochem Nutr 11, 31–40.Google Scholar
Olson, AD, Ayass, M & Chensue, S (1993) Tumor necrosis factor and IL-1 beta expression in pediatric patients with inflammatory bowel disease. J Pediatr Gastroenterol Nutr 16, 241–246.Google ScholarPubMed
Patil, DH, Grimble, GK & Silk, DBA (1987) Lactitol, a new hydrogenated lactose derivative: intestinal absorption and laxative threshold in normal human subjects. Br J Nutr 57, 195–199.Google Scholar
Pfizer (1978) Pfizer Inc. Polydextrose Food Additive Petition, FDA petition 9A3441. New York: Pfizer Inc.Google Scholar
Piva, A, Panciroli, A, Meola, E & Formigoni, A (1996) Lactitol enhances short-chain fatty acid and gas production by swine cecal microflora to a greater extent when fermenting low rather than high fiber diets. J Nutr 126, 280–289.Google Scholar
Piva, A, Prandini, A, Fiorentini, L, Morlacchini, M, Galvano, F & Luchansky, JB (2002) Tributyrin and lactitol synergistically enhanced the trophic status of the intestinal mucosa and reduced histamine levels in the gut of nursery pigs. J Anim Sci 80, 670–680.Google Scholar
Prosky, L (2000) When is dietary fiber considered a functional food? Biofactors 12, 289–297.Google Scholar
Remesy, C & Demigne, C (1976) Partition and absorption of volatile fatty acids in the alimentary canal of the rat. Ann Vet Res 3, 39–55.Google Scholar
Roche, JK, Martins, CA, Cosme, R, Fayer, R & Guerrant, RL (2000) Transforming growth factor beta1 ameliorates intestinal epithelial barrier disruption by Cryptosporidium parvum in vitro in the absence of mucosal T lymphocytes. Infect Immun 68, 5635–5644.CrossRefGoogle ScholarPubMed
Saarinen, MT (2002) Determination of biogenic amines as dansyl derivatives in intestinal digesta and feces by reversed phase HPLC. Chromatographia 55, 297–300.CrossRefGoogle Scholar
Sagher, FA, Dodge, JA, Johnston, CF, Shaw, C, Buchanan, KD & Carr, KE (1991) Rat small-intestinal morphology and tissue regulatory peptides: effects of high dietary fat. Br J Nutr 65, 21–28.Google Scholar
Schley, PD & Field, CJ (2002) The immune-enhancing effects of dietary fibres and prebiotics. Br J Nutr 87, Suppl. 2, S221–S230.Google Scholar
Schroeder, CP & Maurer, HR (2002) Tributyrin-induced differentiation promotes apoptosis of LS 174T colon cancer cells in vitro. Int J Oncol 20, 195–200.Google Scholar
Seiler, N, Atanassov, CL & Raul, F (1998) Polyamine metabolism as target for cancer chemoprevention (review). Int J Oncol 13, 993–1006.Google Scholar
Smith, EA & Macfarlane, GT (1997) Dissimilatory amino acid metabolism in human colonic bacteria. Anaerobe 3, 327–337.Google Scholar
Smith, JG, Youkoyama, WH & German, JB (1998) Butyric acid from the diet: actions at the level of gene expression. Crit Rev Food Sci 38, 259–297.CrossRefGoogle ScholarPubMed
Smith, KM, Eaton, AD, Finlayson, LM & Garside, P (2000) Oral tolerance. Am J Respir Crit Care Med 162, S175–S178.Google Scholar
Solomons, NW & Rosenthal, A (1985) Intestinal metabolism of a random-bonded polyglucose bulking agent in humans: in vitro and in vivo studies of hydrogen evolution. J Lab Clin Med 105, 585–592.Google ScholarPubMed
Soontornchai, S, Sirichakwal, P, Puwastien, P, Tontisirin, K, Kruger, D & Grossklaus, R (2003) Lactitol tolerance in healthy Thai adults. Eur J Nutr 38, 218–226.CrossRefGoogle Scholar
Southon, S, Livesey, G, Gee, JM & Johnson, IT (1985) Intestinal cellular proliferation and protein synthesis in zinc-deficient rats. Br J Nutr 53, 595–603.Google Scholar
Topping, DL, Illman, RJ & Trimble, RP (1985) Volatile fatty acid concentrations in rats fed diets containing gum arabic and cellulose separately and as a mixture. Nutr Rep Int 4, 809–814.Google Scholar
Watanabe, M, Ozaki, T, Hirata, Y, Yamamoto, O, Niida, H, Ueda, F, Yoshikuni, Y & Kimura, K (1995) Mechanism for lowering blood ammonia levels by lactitol. Jpn J Pharmacol 67, 369–374.CrossRefGoogle ScholarPubMed
Yoshioka, M, Shimomura, Y & Suzuki, M (1994) Dietary polydextrose affects the large intestine in rats. J Nutr 124, 539–547.CrossRefGoogle ScholarPubMed