Skip to main content Accessibility help
×
×
Home

Dietary galacto-oligosaccharides and calcium: effects on energy intake, fat-pad weight and satiety-related, gastrointestinal hormones in rats

  • Joost Overduin (a1), Margriet H. C. Schoterman (a2), Wim Calame (a2) (a3), Arjan J. Schonewille (a1) and Sandra J. M. Ten Bruggencate (a1)...

Abstract

Galacto-oligosaccharides (GOS) are carbohydrates that are fermented by colonic microbiota. The present study examined effects of a 3-week dietary enrichment with 6 % (w/w) GOS on parameters of energy balance in forty-three male Wistar rats. GOS was tested with two doses of calcium phosphate (30 and 100 mmol/kg), known to differently affect colonic fermentation. After 17 d, isoenergetic test meals were presented and plasma responses of ghrelin, glucagon-like peptide-1 (GLP-1) and peptide YY (PYY) were measured. On day 21 (study termination) epididymal fat pads and caecum were weighed. Additionally, gastrointestinal mucosal samples and proximal colonic contents were analysed for gene expression (ghrelin, proglucagon and PYY) and fermentation metabolites (SCFA and lactate), respectively. GOS reduced energy intake most prominently during the first week, without provoking compensatory overeating later on (average intake reduction: 14 %). The GOS-fed rats showed increased caecal and reduced fat-pad weight and increased gene expression of the satiety-related peptides, PYY (1·7-fold) and proglucagon (3·5-fold). Pre-meal baseline and post-meal plasma levels of PYY, but not of ghrelin or GLP-1, were higher in GOS-fed rats than in control rats. Ca enrichment resulted in higher energy intake (average 4·5 %). GOS diets increased lactic acid levels and slightly reduced butyric acid in proximal colonic contents. Ca abolished the GOS-related elevation of lactic acid, while increasing propionic acid levels, but did not inhibit GOS-related effects on energy intake, fat-pad weight or gene expression. These results indicate that dietary GOS stimulate a number of physiological mechanisms that can reduce energy intake, regardless of the calcium phosphate content of the diet.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Dietary galacto-oligosaccharides and calcium: effects on energy intake, fat-pad weight and satiety-related, gastrointestinal hormones in rats
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Dietary galacto-oligosaccharides and calcium: effects on energy intake, fat-pad weight and satiety-related, gastrointestinal hormones in rats
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Dietary galacto-oligosaccharides and calcium: effects on energy intake, fat-pad weight and satiety-related, gastrointestinal hormones in rats
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Dr J. Overduin, fax +31 318 650 400, E-mail: joost.overduin@nizo.com

References

Hide All
1Taskforce, IO (2010) The Global Epidemic. http://www.iaso.org/iotf/obesity/obesitytheglobalepidemic/ (accessed accessed December 2011).
2Slavin, J & Green, H (2007) Dietary fiber and satiety. Nutr Bull 32, Suppl. 1, 3242.
3Nauta, A, Bakker-Zierikzee, A & Schoterman, M (2010) Galacto-oligosaccharides. In Handbook of Prebiotics and Probiotics Ingredients: Health Benefits and Food Applications, pp. 7594 [Cho, S and Finocchiaro, E, editors]. Boca Raton: CRC Press.
4Boehm, G & Stahl, B (2007) Oligosaccharides from milk. J Nutr 137, 847S849S.
5Williams, CM & Jackson, KG (2002) Inulin and oligofructose: effects on lipid metabolism from human studies. Br J Nutr 87, Suppl. 2, S261S264.
6Keenan, MJ, Zhou, J, McCutcheon, KL, et al. (2006) Effects of resistant starch, a non-digestible fermentable fiber, on reducing body fat. Obesity (Silver Spring) 14, 15231534.
7Cani, PD, Dewever, C & Delzenne, NM (2004) Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Br J Nutr 92, 521526.
8Tolhurst, G, Heffron, H, Lam, YS, et al. (2012) Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 61, 364371.
9Cani, PD, Neyrinck, AM, Maton, N, et al. (2005) Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like peptide-1. Obes Res 13, 10001007.
10Delzenne, NM, Cani, PD, Daubioul, C, et al. (2005) Impact of inulin and oligofructose on gastrointestinal peptides. Br J Nutr 93, Suppl. 1, S157S161.
11Gee, JM & Johnson, IT (2005) Dietary lactitol fermentation increases circulating peptide YY and glucagon-like peptide-1 in rats and humans. Nutrition 21, 10361043.
12Cummings, DE & Overduin, J (2007) Gastrointestinal regulation of food intake. J Clin Invest 117, 1323.
13Ten Bruggencate, SJ, Bovee-Oudenhoven, IM, Lettink-Wissink, ML, et al. (2004) Dietary fructo-oligosaccharides and inulin decrease resistance of rats to salmonella: protective role of calcium. Gut 53, 530535.
14Remesy, C, Levrat, MA, Gamet, L, et al. (1993) Cecal fermentations in rats fed oligosaccharides (inulin) are modulated by dietary calcium level. Am J Physiol 264, G855G862.
15Louis, P, Scott, KP, Duncan, SH, et al. (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102, 11971208.
16Schepens, MA, Ten Bruggencate, SJ, Schonewille, AJ, et al. (2012) The protective effect of supplemental calcium on colonic permeability depends on a calcium phosphate-induced increase in luminal buffering capacity. Br J Nutr 107, 950956.
17Zemel, MB (2004) Role of calcium and dairy products in energy partitioning and weight management. Am J Clin Nutr 79, 907S912S.
18Ross, AC, Manson, JE, Abrams, SA, et al. (2011) The 2011 Dietary Reference Intakes for Calcium and Vitamin D: what dietetics practitioners need to know. J Am Diet Assoc 111, 524527.
19Gao, X, Wilde, PE, Lichtenstein, AH, et al. (2006) Meeting adequate intake for dietary calcium without dairy foods in adolescents aged 9 to 18 years (National Health and Nutrition Examination Survey 2001–2002). J Am Diet Assoc 106, 17591765.
20Reeves, PG, Nielsen, FH, Fahey, GC, et al. (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 19391951.
21Ten Bruggencate, SJ, Bovee-Oudenhoven, IM, Lettink-Wissink, ML, et al. (2005) Dietary fructooligosaccharides increase intestinal permeability in rats. J Nutr 135, 837842.
22Coussement, PA (1999) Inulin and oligofructose: safe intakes and legal status. J Nutr 129, 1412S1417S.
23Park, Y, Yetley, E & Calco, M (1997) Calcium intake levels in the United States: issues and considerations. In Food, Nutrition and Agriculture, pp. 34–41 [JL Albert, JR Ciaffi-Cannizzo, A Lupier, et al., editors]. Rome: FAO Food and Nutrition Division.
24Mangano, KM, Walsh, SJ, Insogna, KL, et al. (2011) Calcium intake in the United States from dietary and supplemental sources across adult age groups: new estimates from the National Health and Nutrition Examination Survey 2003–2006. J Am Diet Assoc 111, 687695.
25Jackson, KA & Savaiano, DA (2001) Lactose maldigestion, calcium intake and osteoporosis in African-, Asian-, and Hispanic-Americans. J Am Coll Nutr 20, 198S207S.
26Garrow, J & James, W (1993) Human Nutrition and Dietetics, 9th ed.Edinburgh: Churchill Livingstone.
27Cummings, JH, Roberfroid, MB, Andersson, H, et al. (1997) A new look at dietary carbohydrate: chemistry, physiology and health. Paris Carbohydrate Group. Eur J Clin Nutr 51, 417423.
28Macfarlane, GT, Steed, H & Macfarlane, S (2008) Bacterial metabolism and health-related effects of galacto-oligosaccharides and other prebiotics. J Appl Microbiol 104, 305344.
29Sako, T, Matsumoto, K & Tanaka, R (1999) Recent progress on research and applications of non-digestible galacto-oligosaccharides. Int Dairy J 9, 6980.
30Anini, Y, Fu-Cheng, X, Cuber, JC, et al. (1999) Comparison of the postprandial release of peptide YY and proglucagon-derived peptides in the rat. Pflugers Arch 438, 299306.
31Lim, G & Brubaker, P (2006) Glucagon-like peptide 1 secretion by the L-cell: the view from within. Diabetes 55, 870877.
32Remie, R, Van Dongen, JJ, Rensema, JW, et al. (1990) General techniques. In Manual of Microsurgery on the Laboratory Rat, pp. 81156 [Remie, R, van Dongen, JJ, Rensema, JW and van Wunnik, GHJ, editors]. Amsterdam: Elsevier.
33Delzenne, NM, Cani, PD & Neyrinck, AM (2007) Modulation of glucagon-like peptide 1 and energy metabolism by inulin and oligofructose: experimental data. J Nutr 137, 2547S2551S.
34Foster-Schubert, KE, Overduin, J, Prudom, CE, et al. (2008) Acyl and total ghrelin are suppressed strongly by ingested proteins, weakly by lipids, and biphasically by carbohydrates. J Clin Endocrinol Metab 93, 19711979.
35Deacon, CF (2004) Circulation and degradation of GIP and GLP-1. Horm Metab Res 36, 761765.
36Holst, JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87, 14091439.
37Keire, DA, Whitelegge, JP, Souda, P, et al. (2010) PYY(1-36) is the major form of PYY in rat distal small intestine: quantification using high-resolution mass spectrometry. Regul Pept 165, 151157.
38Tangerman, A & Nagengast, FM (1996) A gas chromatographic analysis of fecal short-chain fatty acids, using the direct injection method. Anal Biochem 236, 18.
39Beck, B, Richy, S & Stricker-Krongrad, A (2003) Ghrelin and body weight regulation in the obese Zucker rat in relation to feeding state and dark/light cycle. Exp Biol Med (Maywood) 228, 11241131.
40Zhou, J, Hegsted, M, McCutcheon, KL, et al. (2006) Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity (Silver Spring) 14, 683689.
41Cani, PD, Joly, E, Horsmans, Y, et al. (2006) Oligofructose promotes satiety in healthy humans: a pilot study. Eur J Clin Nutr 60, 567572.
42Higgins, JA, Higbee, DR, Donahoo, WT, et al. (2004) Resistant starch consumption promotes lipid oxidation. Nutr Metab (Lond) 1, 8.
43Schutz, Y & Jequier, E (2004) Resting energy expenditure, thermic effect of food, and total energy expernditure. In Handbook of Obesity, 2nd ed., pp. 615630 [Bray, GA and Bouchard, C, editors]. New York, NY: Marcel Dekker, Inc.
44Westerterp-Plantenga, MS, Smeets, AJ & Nieuwenhuizen, A (2007) Sustained protein intake for body weight management. Nutr Bull 32, 2231.
45Wang, ZQ, Zuberi, AR, Zhang, XH, et al. (2007) Effects of dietary fibers on weight gain, carbohydrate metabolism, and gastric ghrelin gene expression in mice fed a high-fat diet. Metabolism 56, 16351642.
46Parnell, JA & Reimer, RA (2012) Prebiotic fibres dose-dependently increase satiety hormones and alter Bacteroidetes and Firmicutes in lean and obese JCR:LA-cp rats. Br J Nutr 107, 601613.
47Lapre, JA, De Vries, HT, Koeman, JH, et al. (1993) The antiproliferative effect of dietary calcium on colonic epithelium is mediated by luminal surfactants and dependent on the type of dietary fat. Cancer Res 53, 784789.
48Papakonstantinou, E, Flatt, WP, Huth, PJ, et al. (2003) High dietary calcium reduces body fat content, digestibility of fat, and serum vitamin D in rats. Obes Res 11, 387394.
49Zemel, MB, Shi, H, Greer, B, et al. (2000) Regulation of adiposity by dietary calcium. FASEB J 14, 11321138.
50Cani, PD, Hoste, S, Guiot, Y, et al. (2007) Dietary non-digestible carbohydrates promote L-cell differentiation in the proximal colon of rats. Br J Nutr 98, 3237.
51Theodorakis, MJ, Carlson, O, Michopoulos, S, et al. (2006) Human duodenal enteroendocrine cells: source of both incretin peptides, GLP-1 and GIP. Am J Physiol Endocrinol Metab 290, E550E559.
52Dumoulin, V, Moro, F, Barcelo, A, et al. (1998) Peptide YY, glucagon-like peptide-1, and neurotensin responses to luminal factors in the isolated vascularly perfused rat ileum. Endocrinology 139, 37803786.
53Younes, H, Coudray, C, Bellanger, J, et al. (2001) Effects of two fermentable carbohydrates (inulin and resistant starch) and their combination on calcium and magnesium balance in rats. Br J Nutr 86, 479485.
54Holma, R, Juvonen, P, Asmawi, MZ, et al. (2002) Galacto-oligosaccharides stimulate the growth of bifidobacteria but fail to attenuate inflammation in experimental colitis in rats. Scand J Gastroenterol 37, 10421047.
55Le Blay, G, Michel, C, Blottiere, H, et al. (1999) Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. J Nutr 129, 22312235.
56Cummings, JH (1981) Short chain fatty acids in the human colon. Gut 22, 763779.
57Belenguer, A, Duncan, SH, Holtrop, G, et al. (2007) Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl Environ Microbiol 73, 65266533.
58Bergman, EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 70, 567590.
59Ten Bruggencate, SJ, Bovee-Oudenhoven, IM, Lettink-Wissink, ML, et al. (2003) Dietary fructo-oligosaccharides dose-dependently increase translocation of salmonella in rats. J Nutr 133, 23132318.
60Butler, R, Topping, D, Illman, R, et al. (1990) Effects of starvation-refeeding on volatile fatty acid distribution in the large bowel of the rat. Nutr Res 10, 9198.
61Walton, GE, van den Heuvel, EG, Kosters, MH, et al. (2012) 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 107, 14661475.
62Walker, AW, Ince, J, Duncan, SH, et al. (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5, 220230.
63Ley, RE (2010) Obesity and the human microbiome. Curr Opin Gastroenterol 26, 511.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed