Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 12, 2011, Pages 6501-6510

  Weaver, Connie M ^a   Martin, Berdine R ^a   Nakatsu, Cindy H ^a   Armstrong, Arthur P ^a   Clavijo, Andrea ^a   McCabe, Linda D ^b   McCabe, George P ^b   Duignan, Sinead ^a   Schoterman, Margriet H C ^c   Van Den Heuvel, Ellen G H M ^c  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c FRIESLANDCAMPINA   (Netherlands)

Author keywords

bone mineral density; galactooligosaccharide (GOS); mineral absorption; nondigestible oligosaccharides

Indexed keywords

16S RRNA GENE; BACTERIAL COMMUNITY STRUCTURE; BIFIDOBACTERIA; BONE MINERAL DENSITY; BREAKING STRENGTH; CALCIUM ABSORPTION; DISTAL FEMURS; DOSE RESPONSE; DOSE-DEPENDENT MANNER; FECAL DNA; FINGERPRINT PATTERN; GALACTO-OLIGOSACCHARIDES; GALACTOOLIGOSACCHARIDE (GOS); MICROBIOTAS; MINERAL ABSORPTION; NONDIGESTIBLE OLIGOSACCHARIDES; PCR-DGGE; PREBIOTICS; QUANTITATIVE PCR; REGRESSION MODELING; SPRAGUE-DAWLEY RATS; TREATMENT GROUP;

ABSORPTION; BACTERIA; CALCIUM; GENES; MAGNESIUM; OLIGOSACCHARIDES; POLYMERASE CHAIN REACTION; RATS; RNA; SILICATE MINERALS;

BONE;

CALCIUM; MAGNESIUM; MINERAL; OLIGOSACCHARIDE; PREBIOTIC AGENT;

ABSORPTION; ANIMAL; ANIMAL MODEL; ARTICLE; BIFIDOBACTERIUM; BONE; BONE DENSITY; BONE DEVELOPMENT; FERMENTATION; GENETICS; HUMAN; INTESTINE; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; RANDOMIZATION; RAT; SPRAGUE DAWLEY RAT;

ABSORPTION; ANIMALS; BIFIDOBACTERIUM; BONE AND BONES; BONE DENSITY; BONE DEVELOPMENT; CALCIUM; FERMENTATION; HUMANS; INTESTINES; MAGNESIUM; MALE; MINERALS; MODELS, ANIMAL; OLIGOSACCHARIDES; PREBIOTICS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

BACTERIA (MICROORGANISMS); RATTUS;

EID: 79959256073     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf2009777     Document Type: Article

References (40)

1. Cashman, K. D.; Flynn, A. Optimal nutrition: calcium, magnesium and phosphorus Proc. Nutr. Soc. 1999, 58, 477-487 (Pubitemid 29398135)
2. Scholz-Ahrens, K.; Ade, P.; Marten, B.; Weber, P.; Timm, W.; Açil, Y.; Glüer, C. C.; Schrezenmeir, J. Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure J. Nutr. 2007, 137, 838S-846S (Pubitemid 46397527)
3. Roberfoid, M. B. Prebiotics and probiotics: are they functional foods? Am. J. Clin. Nutr. 2000, 71, 1682S-1687S
4. Macfarlane, S.; Macfarlane, G.; Cummings, J. Review article: prebiotics in the gastrointestinal tract Aliment. Pharmacol. Ther. 2006, 24, 701-714
5. Sherman, P. M.; Cabana, M.; Gibson, G. R.; Koletzko, B. V.; Neu, J.; Veereman-Wauters, G.; Ziegler, E. E.; Walker, W. A. Potential Roles and Clinical Utility of Prebiotics in Newborns, Infants, and Children: Proceedings from a Global Prebiotic Summit Meeting, New York City, June 27-28, 2008. J. Pediatr. 2009, 155, S61-S70
6. Vernazza, C.; Gibson, G.; Rastall, R. Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium J. Appl. Microbiol. 2006, 100, 846-853
7. Bongers, A.; van den Heuvel, E. G. H. M. Prebiotics and the bioavailability of minerals and trace elements Food Rev. Int. 2003, 19 (4) 397-422 (Pubitemid 37459262)
8. Chonan, O; Watanuki, M. Effect of galactooligosaccharides on calcium absorption in rats J. Nutr. Sci. Vitaminol. 1995, 41, 95-104
9. Perez-Conesa, D.; Lopez, G.; Ros, G. Effects of probiotic, prebiotic and synbiotic follow-up infant formulas on large intestine morphology and bone mineralisation in rats J. Sci. Food Agric. 2007, 87, 1059-1068 (Pubitemid 46657850)
10. Chonan, O.; Takahashi, R.; Watanuki, M. Role of activity of gastrointestinal microflora in absorption of calcium and magnesium in rats fed b1-4 linked galactooligosaccharides Biosci., Biotechnol., Biochem. 2001, 65 (8) 1872-1875 (Pubitemid 33617798)
11. Bouhnik, Y.; Flourié, B.; DAgay-Abensour, L.; Pochart, P.; Gramet, G.; Durand, M.; Rambaud, J. C. Administration of transgalactooligosaccharides increases fecal bifidobacteria and modifies colonic fermentation metabolism in healthy humans J. Nutr. 1997, 127, 444-448 (Pubitemid 27119998)
12. Bouhnik, Y.; Raskine, L.; Simoneau, G.; Vicaut, E.; Neut, C.; Flourie, B.; Brouns, F.; Bornet, F. R. The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study Am. J. Clin. Nutr. 2004, 80, 1658-1664 (Pubitemid 41103868)
13. Fanaro, S.; Marten, B.; Bagna, R.; Vigi, V.; Fabris, C.; Peña-Quintana.; Argüelles, F.; Scholz-Ahrens, K. E.; Sawatzki, G.; Zelenka, R.; Schrezenmeir, J.; de Vrese, M.; Bertino, E. Galactooligosaccharides are bifidogenic and safe at weaning: a double-blind randomized multicenter study J. Pediatr. Gastroenterol. Nutr. 2009, 48, 82-88
14. Ben, X. M.; Li, J.; Feng, Z. T.; Shi, S. Y.; Lu, Y. D.; Chen, R. Low level of galactooligosaccharide in infant formula stimulates growth of intestinal bifidobacteria and lactobaccili World J. Gastroenterol. 2008, 14, 6564-6568
15. Kripke, S.; Fox, A.; Berman, J.; Settle, R.; Rombeau, J. Stimulation of intestinal mucosal growth with intracolonic infusion of short-chain fatty acids J. Parenter. Enteral. Nutr. 1989, 13, 109-116 (Pubitemid 19096619)
16. Frankel, W.; Zhang, W.; Singh, A.; Klurfeld, D.; Don, S.; Sakata, T.; Modlin, I.; Rombeau, J. L. Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon Gastroenterology 1994, 106, 375-380 (Pubitemid 24041214)
17. Scheppach, W.; Bartram, P.; Richter, A.; Richter, F.; Liepold, H.; Dusel, G.; Hofstetter, G.; Rüthlein, J.; Kasper, H. Effect of short-chain fatty acids on the human colonic mucosa in vitro J. Parenter. Enteral. Nutr. 1992, 16, 43-48
18. Raschka, L.; Daniel, H. Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats Bone 2005, 37, 728-735 (Pubitemid 41476396)
19. Chonan, O.; Watanuki, M. The effect of 6′-galactooligosaccharides on bone mineralization of rats adapted to different levels of dietary calcium Int. J. Vitam. Nutr. Res. 1996, 66, 244-249 (Pubitemid 26369563)
20. Perez-Conesa, D.; Lopez, G.; Abella, P.; Ros, G. Bioavailability of calcium, magnesium and phosphorus in rats fed probiotic, prebiotic and synbiotic powder follow-up infant formulas and their effect on physiological and nutritional parameters J. Sci. Food Agric. 2006, 86, 2327-2336 (Pubitemid 44690153)
21. Van den Heuvel, E. G.; Schoterman, M. H.; Muijs, T. Transgalactooligosaccharides stimulate calcium absorption in postmenopausal women J. Nutr. 2000, 130, 2938-2942 (Pubitemid 32005321)
22. De Slegte, J. Determination of trans-galactooligosaccharides in selected food products by ion-exchange chromatography: collaborative study J. AOAC Int. 2002, 85 (2) 417-423 (Pubitemid 135691712)
23. Weaver, C. M.; Janle, E.; Martin, B.; Browne, S.; Guiden, H.; Lachcik, P.; Lee, W.-H. Dairy versus calcium carbonate in promoting peak bone mass and bone maintenance during subsequent calcium deficiency J. Bone Miner. Res. 2009, 24, 1411-1419
24. Koo, J.; Weaver, C.; Neylan, M. Solubility of calcium salts and carrageenan used in infant formulas did not influence calcium absorption in rats J. Pediatr. Gastroenterol. Nutr. 1993, 17, 298-302 (Pubitemid 23314064)
25. Ariefdjohan, M. W.; Savaiano, D. A.; Nakatsu, C. H. Optimization of DNA extraction kits for PCR-DGGE analysis of human intestinal microbial communities from fecal specimens Nutr. J. 2010, 9, 23
26. Lane, D. J. 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics; Stackebrandt, E.; Goodfellow, M., Eds.; Wiley: New York, 1991; pp 115-175.
27. Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA Appl. Environ. Microbiol. 1993, 59, 695-700 (Pubitemid 23072343)
28. Satokari, R. M.; Vaughan, E. E.; Akkermans, A. D. L.; Saarela, M.; de Vos, W. M. Bifidobacterial diversity in human feces detected by genus-specific PCR and denaturing gradient gel electrophoresis Appl. Environ. Microbiol. 2001, 67, 504-513 (Pubitemid 32121335)
29. Nakatsu, C. H.; Marsh, T. L. Analysis of microbial communities with denaturing gradient gel electrophoresis and terminal restriction fragment length polymorphism. In Methods for General and Molecular Bacteriology, 3 rd ed.; Reddy, C. A., Ed.; 2007; pp 909-923.
30. Zafar, T.; Weaver, C.; Zhao, Y.; Martin, B.; Wastney, M. Nondigestible oligosaccharides increase calcium absorption and suppress bone resorption in ovariectomized rats J. Nutr. 2004, 134, 399-402 (Pubitemid 38141823)
31. Chonan, O.; Matsumoto, K.; Watanuki, M. Effect of galactooligosaccharides on calcium absorption and preventing bone loss in ovariectomized rats Biosci., Biotechnol., Biochem. 1995, 59, 236-239
32. Brommage, R.; Binacua, C.; Antille, S.; Carrie, A.-L. Intestinal calcium absorption in rats is stimulated by dietary lactose and other resistant sugars J. Nutr. 1993, 123, 2186-2194 (Pubitemid 24020745)
33. Yanahira, S.; Morita, M.; Aoe, S.; Sucguri, T.; Takada, Y.; Miura, S.; Nakajima, I. Effects of lactitol-oligosaccharides on calcium and magnesium absorption in rats J. Nutr. Sci. Vitaminol. 1997, 43, 123-132 (Pubitemid 127779983)
34. Heaney, R. P. Role of dietary sodium in osteoporosis J. Am. Coll. Nutr. 2006, 25 (3) 271S-276S (Pubitemid 46931006)
35. Weaver, C. M.; Martin, B. R.; Story, J. A.; Hutchinson, I.; Sanders, L. Novel fibers increase bone calcium content and strength beyond efficiency of large intestine fermentation J. Agric. Food Chem. 2010, 58, 8952-8957
36. Moro, G.; Minoli, I.; Mosca, M.; Fanaro, S.; Jelinek, J.; Stahl, B.; Boehm, G. Dosage-related bifidogenic effects of galacto- and fructooligosaccharides in formula-fed term infants J. Pediatr. Gastroenterol. Nutr. 2002, 34, 291-295 (Pubitemid 34437523)
37. Sato, T.; Matsumoto, K.; Okumura, T.; Yokoi, W.; Naito, E.; Yoshida, Y.; Nomoto, K.; Ito, M.; Sawada, H. Isolation of lactate-utilizing butyrate-producing bacteria from human feces and in vivo administration of Anaerostipes caccae strain L2 and galactooligosaccharides in a rat model FEMS Microbiol. Ecol. 2008, 66, 528-536
38. Reagan-Shaw, S.; Nikal, M.; Ahmad, N. Dose translation from animal to human studies revisited FASEB J. 2007, 22, 342-346
39. Institute of Medicine of the National Academy of Science. Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients); National Academy Press: Washington DC, 2002; Vol. 936.
40. Kranz, S.; Mitchell, D. C.; Siega-Riz, A. M.; Smiciklas-Wright, H. Dietary fiber intake by American preschoolers is associated with more nutrient-dense diets J. Am. Diet. Assoc. 2005, 105, 221-225 (Pubitemid 40164686)