Galacto-oligosaccharides and colorectal cancer: Feeding our intestinal probiome

Journal of Functional Foods

Volumn 12, Issue , 2015, Pages 92-108

  Bruno Barcena, Jose M ^a   Azcarate Peril, M Andrea ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Colorectal cancer; Galacto oligosaccharides; Microbiome; Prebiotics; Probiome

Indexed keywords

EID: 84920746888     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2014.10.029     Document Type: Review

References (170)

1. Aguilera M., Rakotoarivonina H., Brutus A., Giardina T., Simon G., Fons M. Aga1, the first alpha-galactosidase from the human bacteria Ruminococcus gnavus E1, efficiently transcribed in gut conditions. Research in Microbiology 2012, 163(1):14-21.
2. Andersen J.M., Barrangou R., Abou Hachem M., Lahtinen S., Goh Y.J., Svensson B., Klaenhammer T.R. Transcriptional and functional analysis of galactooligosaccharide uptake by lacS in Lactobacillus acidophilus. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(43):17785-17790.
3. Atuma C., Strugala V., Allen A., Holm L. The adherent gastrointestinal mucus gel layer: Thickness and physical state in vivo. American Journal of Physiology. Gastrointestinal and Liver Physiology 2001, 280(5):G922-G929.
4. Austin G.L., Adair L.S., Galanko J.A., Martin C.F., Satia J.A., Sandler R.S. A diet high in fruits and low in meats reduces the risk of colorectal adenomas. The Journal of Nutrition 2007, 137(4):999-1004.
5. Azcarate-Peril M.A., Altermann E., Goh Y.J., Tallon R., Sanozky-Dawes R.B., Pfeiler E.A., O'Flaherty S., Buck B.L., Dobson A., Duong T., Miller M.J., Barrangou R., Klaenhammer T.R. Analysis of the genome sequence of Lactobacillus gasseri ATCC 33323 reveals the molecular basis of an autochthonous intestinal organism. Applied and Environmental Microbiology 2008, 74(15):4610-4625.
6. Azcarate-Peril M.A., Sikes M., Bruno-Barcena J.M. The intestinal microbiota, gastrointestinal environment and colorectal cancer: A putative role for probiotics in prevention of colorectal cancer?. American Journal of Physiology. Gastrointestinal and Liver Physiology 2011, 301(3):G401-G424.
7. Basson M.D., Sgambati S.A. Effects of short-chain fatty acids on human rectosigmoid mucosal colonocyte brush-border enzymes. Metabolism: Clinical and Experimental 1998, 47(2):133-134.
8. Bassonga E., Forest V., Pierre F., Bornet F., Perrin P., Meflah K., Menanteau J. Cytokine mRNA expression in mouse colon: IL-15 mRNA is overexpressed and is highly sensitive to a fibre-like dietary component (short-chain fructo-oligosaccharides) in an Apc gene manner. Cytokine 2001, 14(4):243-246.
9. Bayerdorffer E., Mannes G.A., Ochsenkuhn T., Dirschedl P., Wiebecke B., Paumgartner G. Unconjugated secondary bile acids in the serum of patients with colorectal adenomas. Gut 1995, 36(2):268-273.
10. Begley M., Hill C., Gahan C.G. Bile salt hydrolase activity in probiotics. Applied and Environmental Microbiology 2006, 72(3):1729-1738.
11. Belenguer A., Duncan S.H., Calder A.G., Holtrop G., Louis P., Lobley G.E., Flint H.J. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Applied and Environmental Microbiology 2006, 72(5):3593-3599.
12. Berg E.L., Fu C.J., Porter J.H., Kerley M.S. Fructooligosaccharide supplementation in the yearling horse: Effects on fecal pH, microbial content, and volatile fatty acid concentrations. Journal of Animal Science 2005, 83(7):1549-1553.
13. Bouhnik Y., Attar A., Joly F.A., Riottot M., Dyard F., Flourie B. Lactulose ingestion increases faecal bifidobacterial counts: A randomised double-blind study in healthy humans. European Journal of Clinical Nutrition 2004, 58(3):462-466.
14. Bouhnik Y., Flourie B., Riottot M., Bisetti N., Gailing M.F., Guibert A., Bornet F., Rambaud J.C. Effects of fructo-oligosaccharides ingestion on fecal bifidobacteria and selected metabolic indexes of colon carcinogenesis in healthy humans. Nutrition and Cancer 1996, 26(1):21-29.
15. 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. Nutrition Journal 2006, 5:8-13.
16. Bouhnik Y., Vahedi K., Achour L., Attar A., Salfati J., Pochart P., Marteau P., Flourie B., Bornet F., Rambaud J.C. Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. The Journal of Nutrition 1999, 129(1):113-116.
17. Boutron-Rualt M.C., Marteau P., Lavergne-Slove A., Myara A., Gerhardt M.F., Franchisseur C., Bornet F., Group E.S. Effects of a 3-mo consumption of short-chain fructo-oligosaccharides on parameters of colorectal carcinogenesis in patients with or without small or large colorectal adenomas. Nutrition and Cancer 2005, 53(2):160-168.
18. Brownlee I.A., Havler M.E., Dettmar P.W., Allen A., Pearson J.P. Colonic mucus: Secretion and turnover in relation to dietary fibre intake. The Proceedings of the Nutrition Society 2003, 62(1):245-249.
19. Buecher B., Thouminot C., Menanteau J., Bonnet C., Jarry A., Heymann M.F., Cherbut C., Galmiche J.P., Blottiere H.M. Fructooligosaccharide associated with celecoxib reduces the number of aberrant crypt foci in the colon of rats. Reproduction, Nutrition, Development 2003, 43(4):347-356.
20. Campbell A.K., Waud J.P., Matthews S.B. The molecular basis of lactose intolerance. Science Progress 2005, 88(Pt. 3):157-202.
21. Campbell J.M., Fahey G.C., Wolf B.W. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats. The Journal of Nutrition 1997, 127(1):130-136.
22. Challa A., Rao D.R., Chawan C.B., Shackelford L. Bifidobacterium longum and lactulose suppress azoxymethane-induced colonic aberrant crypt foci in rats. Carcinogenesis 1997, 18(3):517-521.
23. Colditz G.A., Samplin-Salgado M., Ryan C.T., Dart H., Fisher L., Tokuda A., Rockhill B. Harvard report on cancer prevention, volume 5: Fulfilling the potential for cancer prevention: Policy approaches. Cancer Causes & Control: CCC 2002, 13(3):199-212.
24. Corpet D.E., Pierre F. Point: From animal models to prevention of colon cancer. Systematic review of chemoprevention in min mice and choice of the model system. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2003, 12(5):391-400.
25. Cummings J.H. Short chain fatty acids in the human colon. Gut 1981, 22(9):763-779.
26. Cummings J.H., Bingham S.A., Heaton K.W., Eastwood M.A. Fecal weight, colon cancer risk, and dietary intake of nonstarch polysaccharides (dietary fiber). Gastroenterology 1992, 103(6):1783-1789.
27. Dagher S.F., Azcarate-Peril M.A., Bruno-Barcena J.M. Heterologous expression of a bioactive beta-hexosyltransferase, an enzyme producer of prebiotics, from Sporobolomyces singularis. Applied and Environmental Microbiology 2013, 79(4):1241-1249.
28. Davis L.M., Martinez I., Walter J., Goin C., Hutkins R.W. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS ONE 2011, 6(9). e25200.
29. De Souza Oliveira R.P., Rodrigues Florence A.C., Perego P., De Oliveira M.N., Converti A. Use of lactulose as prebiotic and its influence on the growth, acidification profile and viable counts of different probiotics in fermented skim milk. International Journal of Food Microbiology 2011, 145(1):22-27.
30. Djouzi Z., Andrieux C. Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. The British Journal of Nutrition 1997, 78(2):313-324.
31. Duffaud G.D., McCutchen C.M., Leduc P., Parker K.N., Kelly R.M. Purification and characterization of extremely thermostable beta-mannanase, beta-mannosidase, and alpha-galactosidase from the hyperthermophilic eubacterium Thermotoga neapolitana 5068. Applied and Environmental Microbiology 1997, 63(1):169-177.
32. Duncan S.H., Louis P., Flint H.J. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Applied and Environmental Microbiology 2004, 70(10):5810-5817.
33. Falony G., Vlachou A., Verbrugghe K., De Vuyst L. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Applied and Environmental Microbiology 2006, 72(12):7835-7841.
34. Fanaro S., Boehm G., Garssen J., Knol J., Mosca F., Stahl B., Vigi V. Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: A review. Acta Paediatrica 2007, 94(s449):22-26.
35. Floch M.H. Soluble dietary fiber and short-chain fatty acids: An advance in understanding the human bacterial flora. The American Journal of Gastroenterology 1990, 85(10):1313-1314.
36. Forest V., Pierre F., Bassonga E., Meflah K., Menanteau J. Large intestine intraepithelial lymphocytes from Apc+/+ and Apc+/Min mice and their modulation by indigestible carbohydrates: The IL-15/IL-15R alpha complex and CD4+ CD25+ T cells are the main targets. Cancer Immunology, Immunotherapy: CII 2005, 54(1):78-86.
37. Fujita K., Oura F., Nagamine N., Katayama T., Hiratake J., Sakata K., Kumagai H., Yamamoto K. Identification and molecular cloning of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-alpha-N-acetylgalactosaminidase from Bifidobacterium longum. The Journal of Biological Chemistry 2005, 280(45):37415-37422.
38. Garvie E.I. Bacterial lactate dehydrogenases. Microbiological Reviews 1980, 44(1):106-139.
39. Gibson G.R., Probert H.M., Loo J.V., Rastall R.A., Roberfroid M.B. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics. Nutrition Research Reviews 2004, 17(2):259-275.
40. Gibson G.R., Roberfroid M.B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. The Journal of Nutrition 1995, 125(6):1401-1412.
41. Gibson G.R., Scott K.P., Rastall R.A., Tuohy K., Hotchkiss A.T. Dietary prebiotics: Current status and new definition. IFIS 2010, 7(1):1-19.
42. Goldin B., Gorbach S.L. Alterations in fecal microflora enzymes related to diet, age, lactobacillus supplements, and dimethylhydrazine. Cancer 1977, 40(Suppl. 5):2421-2426.
43. Goldin B.R., Gorbach S.L. The relationship between diet and rat fecal bacterial enzymes implicated in colon cancer. Journal of the National Cancer Institute 1976, 57(2):371-375.
44. Gopalakrishnan A., Clinthorne J.F., Rondini E.A., McCaskey S.J., Gurzell E.A., Langohr I.M., Gardner E.M., Fenton J.I. Supplementation with galacto-oligosaccharides increases the percentage of NK cells and reduces colitis severity in Smad3-deficient mice. The Journal of Nutrition 2012, 142(7):1336-1342.
45. Gourineni V.P., Verghese M., Boateng J., Shackelford L., Bhat N.K., Walker L.T. Combinational effects of prebiotics and soybean against azoxymethane-induced colon cancer in vivo. Journal of Nutrition and Metabolism 2011, 2011. 868197.
46. Hansson G.C. Role of mucus layers in gut infection and inflammation. Current Opinion in Microbiology 2012, 15(1):57-62.
47. Henrissat B., Bairoch A. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. The Biochemical Journal 1993, 293(Pt. 3):781-788.
48. Henrissat B., Bairoch A. Updating the sequence-based classification of glycosyl hydrolases. The Biochemical Journal 1996, 316(Pt. 2):695-696.
49. Hernandez-Hernandez O., Muthaiyan A., Moreno F.J., Montilla A., Sanz M.L., Ricke S.C. Effect of prebiotic carbohydrates on the growth and tolerance of Lactobacillus. Food Microbiology 2012, 30(2):355-361.
50. Hofmanova J., Strakova N., Vaculova A.H., Tylichova Z., Safarikova B., Skender B., Kozubik A. Interaction of dietary fatty acids with tumour necrosis factor family cytokines during colon inflammation and cancer. Mediators of Inflammation 2014, 2014. 848632.
51. Holscher H.D., Faust K.L., Czerkies L.A., Litov R., Ziegler E.E., Lessin H., Hatch T., Sun S., Tappenden K.A. Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. JPEN. Journal of Parenteral and Enteral Nutrition 2012, 36(Suppl. 1):95S-105S.
52. Holt S.M., Teresi J.M., Cote G.L. Influence of alternansucrase-derived oligosaccharides and other carbohydrates on alpha-galactosidase and alpha-glucosidase activity in Bifidobacterium adolescentis. Letters in Applied Microbiology 2008, 46(1):73-79.
53. Hosono A., Ozawa A., Kato R., Ohnishi Y., Nakanishi Y., Kimura T., Nakamura R. Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer's patch cells. Bioscience, Biotechnology, and Biochemistry 2003, 67(4):758-764.
54. Howard M.D., Gordon D.T., Pace L.W., Garleb K.A., Kerley M.S. Effects of dietary supplementation with fructooligosaccharides on colonic microbiota populations and epithelial cell proliferation in neonatal pigs. Journal of Pediatric Gastroenterology and Nutrition 1995, 21(3):297-303.
55. Hsu C.K., Liao J.W., Chung Y.C., Hsieh C.P., Chan Y.C. Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. The Journal of Nutrition 2004, 134(6):1523-1528.
56. Hylemon P.B., Harder J. Biotransformation of monoterpenes, bile acids, and other isoprenoids in anaerobic ecosystems. FEMS Microbiology Reviews 1998, 22(5):475-488.
57. Illanes A. Whey upgrading by enzyme biocatalysis. Electronic Journal of Biotechnology 2011, 14(6).
58. Iqbal S., Nguyen T.H., Nguyen H.A., Maischberger T., Kittl R., Haltrich D. Characterization of a heterodimeric GH2 beta-galactosidase from Lactobacillus sakei Lb790 and formation of prebiotic galacto-oligosaccharides. Journal of Agricultural and Food Chemistry 2011, 59(8):3803-3811.
59. Iqbal S., Nguyen T.H., Nguyen T.T., Maischberger T., Haltrich D. beta-Galactosidase from Lactobacillus plantarum WCFS1: Biochemical characterization and formation of prebiotic galacto-oligosaccharides. Carbohydrate Research 2010, 345(10):1408-1416.
60. Johnson I.T., Lund E.K. Review article: Nutrition, obesity and colorectal cancer. Alimentary Pharmacology and Therapeutics 2007, 26(2):161-181.
61. Kanakupt K., Vester Boler B.M., Dunsford B.R., Fahey G.C. Effects of short-chain fructooligosaccharides and galactooligosaccharides, individually and in combination, on nutrient digestibility, fecal fermentative metabolite concentrations, and large bowel microbial ecology of healthy adults cats. Journal of Animal Science 2011, 89(5):1376-1384.
62. Kanehisa M., Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research 2000, 28(1):27-30.
63. Kaplan H., Hutkins R.W. Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria. Applied and Environmental Microbiology 2000, 66(6):2682-2684.
64. Kasbauer C.W., Paper D.H., Franz G. Sulfated beta-(1→4)-galacto-oligosaccharides and their effect on angiogenesis. Carbohydrate Research 2001, 330(3):427-430.
65. Kuntz S., Kunz C., Rudloff S. Oligosaccharides from human milk induce growth arrest via G2/M by influencing growth-related cell cycle genes in intestinal epithelial cells. British Journal of Nutrition 2009, 101(9):1306-1315.
66. Kuntz S., Rudloff S., Kunz C. Oligosaccharides from human milk influence growth-related characteristics of intestinally transformed and non-transformed intestinal cells. British Journal of Nutrition 2008, 99(3):462-471.
67. Kunz C., Rudloff S., Baier W., Klein N., Strobel S. Oligosaccharides in human milk: Structural, functional, and metabolic aspects. Annual Review of Nutrition 2000, 20:699-722.
68. Le Blay G., Michel C., Blottiere H.M., Cherbut C. Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. The Journal of Nutrition 1999, 129(12):2231-2235.
69. Leforestier G., Blais A., Blachier F., Marsset-Baglieri A., Davila-Gay A.M., Perrin E., Tome D. Effects of galacto-oligosaccharide ingestion on the mucosa-associated mucins and sucrase activity in the small intestine of mice. European Journal of Nutrition 2009, 48(8):457-464.
70. Leonel A.J., Alvarez-Leite J.I. Butyrate: Implications for intestinal function. Current Opinion in Clinical Nutrition and Metabolic Care 2012, 15(5):474-479.
71. Lewis S.J., Heaton K.W. The metabolic consequences of slow colonic transit. The American Journal of Gastroenterology 1999, 94(8):2010-2016.
72. Li M., Bauer L.L., Chen X., Wang M., Kuhlenschmidt T.B., Kuhlenschmidt M.S., Fahey G.C., Donovan S.M. Microbial composition and in vitro fermentation patterns of human milk oligosaccharides and prebiotics differ between formula-fed and sow-reared piglets. The Journal of Nutrition 2012, 142(4):681-689.
73. LoCascio R.G., Desai P., Sela D.A., Weimer B., Mills D.A. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Applied and Environmental Microbiology 2010, 76(22):7373-7381.
74. Lomax A.R., Calder P.C. Prebiotics, immune function, infection and inflammation: A review of the evidence. The British Journal of Nutrition 2009, 101(5):633-658.
75. London D.R., Cuatrecasas P., Birge S.J., Segal S. Metabolism of lactose by intestinal mucosa from normal and lactase-deficient subjects. British Medical Journal 1967, 1(5539):524-526.
76. Maathuis A.J., van den Heuvel E.G., Schoterman M.H., Venema K. Galacto-oligosaccharides have prebiotic activity in a dynamic in vitro colon model using a C-labeling technique. The Journal of Nutrition 2012, 142(7):1205-1212.
77. Macfarlane G.T., Macfarlane S. Fermentation in the human large intestine: Its physiologic consequences and the potential contribution of prebiotics. Journal of Clinical Gastroenterology 2011, 45(Suppl.):S120-S127.
78. Maischberger T., Leitner E., Nitisinprasert S., Juajun O., Yamabhai M., Nguyen T.H., Haltrich D. Beta-galactosidase from Lactobacillus pentosus: Purification, characterization and formation of galacto-oligosaccharides. Biotechnology Journal 2010, 5(8):838-847.
79. Marshall J.R. Prevention of colorectal cancer: Diet, chemoprevention, and lifestyle. Gastroenterology Clinics of North America 2008, 37(1):73-82.
80. Martinez-Villaluenga C., Cardelle-Cobas A., Corzo N., Olano A. Study of galactooligosaccharide composition in commercial fermented milks. Journal of Food Composition and Analysis 2008, 21:540-544.
81. Matthews B.W. The structure of E. coli beta-galactosidase. Comptes Rendus Biologies 2005, 328(6):549-556.
82. McCance R.A., Lawrence R.D. The carbohydrate content of foods. Medical research council special report series 1929, H. M. Stationary Office, London.
83. McCleary B.V. Dietary fibre analysis. The Proceedings of the Nutrition Society 2003, 62(1):3-9.
84. McGarr S.E., Ridlon J.M., Hylemon P.B. Diet, anaerobic bacterial metabolism, and colon cancer: A review of the literature. Journal of Clinical Gastroenterology 2005, 39(2):98-109.
85. McIntyre A., Gibson P.R., Young G.P. Butyrate production from dietary fibre and protection against large bowel cancer in a rat model. Gut 1993, 34(3):386-391.
86. Mei G.Y., Carey C.M., Tosh S., Kostrzynska M. Utilization of different types of dietary fibres by potential probiotics. Canadian Journal of Microbiology 2011, 57(10):857-865.
87. Meslin J.C., Andrieux C., Sakata T., Beaumatin P., Bensaada M., Popot F., Szylit O., Durand M. Effects of galacto-oligosaccharide and bacterial status on mucin distribution in mucosa and on large intestine fermentation in rats. The British Journal of Nutrition 1993, 69(3):903-912.
88. Messina M.J. Legumes and soybeans: Overview of their nutritional profiles and health effects. The American Journal of Clinical Nutrition 1999, 70(Suppl. 3):439S-450S.
89. Midtvedt A.C., Midtvedt T. Production of short chain fatty acids by the intestinal microflora during the first 2 years of human life. Journal of Pediatric Gastroenterology and Nutrition 1992, 15(4):395-403.
90. Minekus M., Smeets-Peeters M., Bernalier A., Marol-Bonnin S., Havenaar R., Marteau P., Alric M., Fonty G., Huis in't Veld J.H. A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products. Applied Microbiology and Biotechnology 1999, 53(1):108-114.
91. Molis C., Flourie B., Ouarne F., Gailing M.F., Lartigue S., Guibert A., Bornet F., Galmiche J.P. Digestion, excretion, and energy value of fructooligosaccharides in healthy humans. The American Journal of Clinical Nutrition 1996, 64(3):324-328.
92. Morishita Y., Oowada T., Ozaki A., Mizutani T. Galactooligosaccharide in combination with Bifidobacterium and Bacteroides affects the population of Clostridium perfringens in the intestine of gnotobiotic mice. Nutrition Research 2002, 22:1333-1341.
93. 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. Journal of Pediatric Gastroenterology and Nutrition 2002, 34(3):291-295.
94. Moser A.R., Pitot H.C., Dove W.F. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990, 247(4940):322-324.
95. Mudd D.G., McKelvey S.T., Norwood W., Elmore D.T., Roy A.D. Faecal bile acid concentration of patients with carcinoma or increased risk of carcinoma in the large bowel. Gut 1980, 21(7):587-590.
96. Mussatto S.I., Mancilha I.M. Non-digestible oligosaccharides: A review. Carbohydrate Polymers 2007, 68:587-597.
97. Nagendra R., Vishwanatha S., Rao S.V., Ravish S.R. Effect of feeding infant formula containing lactulose on intestinal flora in the infant. Indian Journal of Pediatrics 1992, 59(6):763-766.
98. Nakamura J., Kubota Y., Miyaoka M., Saitoh T., Mizuno F., Benno Y. Comparison of four microbial enzymes in Clostridia and Bacteroides isolated from human feces. Microbiology and Immunology 2002, 46(7):487-490.
99. Newmark H.L., Lupton J.R. Determinants and consequences of colonic luminal pH: Implications for colon cancer. Nutrition and Cancer 1990, 14(3-4):161-173.
100. Nguyen T.H., Splechtna B., Krasteva S., Kneifel W., Kulbe K.D., Divne C., Haltrich D. Characterization and molecular cloning of a heterodimeric beta-galactosidase from the probiotic strain Lactobacillus acidophilus R22. FEMS Microbiology Letters 2007, 269(1):136-144.
101. Nguyen T.H., Splechtna B., Steinbock M., Kneifel W., Lettner H.P., Kulbe K.D., Haltrich D. Purification and characterization of two novel beta-galactosidases from Lactobacillus reuteri. Journal of Agricultural and Food Chemistry 2006, 54(14):4989-4998.
102. Nguyen T.T., Nguyen H.A., Arreola S.L., Mlynek G., Djinovic-Carugo K., Mathiesen G., Nguyen T.H., Haltrich D. Homodimeric beta-galactosidase from Lactobacillus delbrueckii subsp. bulgaricus DSM 20081: Expression in Lactobacillus plantarum and biochemical characterization. Journal of Agricultural and Food Chemistry 2012, 60(7):1713-1721.
103. Nilsson K.G.I. Enzymatic synthesis of oligosaccharides. Trends in Biotechnology 1988, 6:256-264.
104. Nishimoto M., Kitaoka M. Identification of N-acetylhexosamine 1-kinase in the complete lacto-N-biose I/galacto-N-biose metabolic pathway in Bifidobacterium longum. Applied and Environmental Microbiology 2007, 73(20):6444-6449.
105. Ohtsuka K., Tsuji K., Nakagawa Y., Ueda H., Ozawa O., Uchida T., Ichikawa T. Utilization and metabolism of [U-14C]4' galactosyllactose (O-beta-D-galactopyranosyl-(1--4)-O-beta-D-galactopyranosyl-(1--4)- D-glucopyranose) in rats. Journal of Nutritional Science and Vitaminology 1991, 37(2):173-184.
106. Okazaki N., Jue X.X., Miyake H., Kuroda M., Shimamoto T., Tsuchiya T. A melibiose transporter and an operon containing its gene in Enterobacter cloacae. Journal of Bacteriology 1997, 179(13):4443-4445.
107. Ozer D., Akin S., Ozer B. Effect of inulin and lactulose on survival of Lactobacillus acidophilus LA-5 and Bifidobacterium bifidum BB-02 on Acidophilus-Bifidus yoghurt. Food Science and Technology International 2005, 11:19-24.
108. Pan X.D., Chen F.Q., Wu T.X., Tang H.G., Zhao Z.Y. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. Journal of Zhejiang University. Science. B 2009, 10(4):258-263.
109. Panesar P.S., Kumari S. Lactulose: Production, purification and potential applications. Biotechnology Advances 2011, 29(6):940-948.
110. Paturi G., Butts C.A., Stoklosinski H., Ansell J. Effects of early dietary intervention with a fermentable fibre on colonic microbiota activity and mucin gene expression in newly weaned rats. Journal of Functional Foods 2012, 4(2):520-530.
111. Pierre F., Perrin P., Champ M., Bornet F., Meflah K., Menanteau J. Short-chain fructo-oligosaccharides reduce the occurrence of colon tumors and develop gut-associated lymphoid tissue in Min mice. Cancer Research 1997, 57(2):225-228.
112. Priebe M.G., Vonk R.J., Sun X., He T., Harmsen H.J., Welling G.W. The physiology of colonic metabolism. Possibilities for interventions with pre- and probiotics. European Journal of Nutrition 2002, 41(Suppl. 1):I2-I10.
113. Rackis J.J., Honig D.H., Sessa D.J., Steggerda F.R. Flavor and flatulence factors in soybean protein products. Journal of Agricultural and Food Chemistry 1970, 18(6):977-982.
114. Randi G., Edefonti V., Ferraroni M., La Vecchia C., Decarli A. Dietary patterns and the risk of colorectal cancer and adenomas. Nutrition Reviews 2010, 68(7):389-408.
115. Reddy B.S., Hamid R., Rao C.V. Effect of dietary oligofructose and inulin on colonic preneoplastic aberrant crypt foci inhibition. Carcinogenesis 1997, 18(7):1371-1374.
116. Reddy B.S., Sharma C., Simi B., Engle A., Laakso K., Puska P., Korpela R. Metabolic epidemiology of colon cancer: Effect of dietary fiber on fecal mutagens and bile acids in healthy subjects. Cancer Research 1987, 47(2):644-648.
117. Reddy B.S., Watanabe K., Weisburger J.H., Wynder E.L. Promoting effect of bile acids in colon carcinogenesis in germ-free and conventional F344 rats. Cancer Research 1977, 37(9):3238-3242.
118. Reddy B.S., Wynder E.L. Metabolic epidemiology of colon cancer. Fecal bile acids and neutral sterols in colon cancer patients and patients with adenomatous polyps. Cancer 1977, 39(6):2533-2539.
119. Roberfroid M.B., Bornet F., Bouley C., Cummings J.H. Colonic microflora: Nutrition and health. Summary and conclusions of an International Life Sciences Institute (ILSI) [Europe] workshop held in Barcelona, Spain. Nutrition Reviews 1995, 53(5):127-130.
120. Roncucci L., Di Donato P., Carati L., Ferrari A., Perini M., Bertoni G., Bedogni G., Paris B., Svanoni F., Girola M., Ponz de Leon M. Antioxidant vitamins or lactulose for the prevention of the recurrence of colorectal adenomas. Colorectal Cancer Study Group of the University of Modena and the Health Care District 16. Diseases of the Colon and Rectum 1993, 36(3):227-234.
121. Rooney P.S., Hunt L.M., Clarke P.A., Gifford K.A., Hardcastle J.D., Armitage N.C. Wheat fibre, lactulose and rectal mucosal proliferation in individuals with a family history of colorectal cancer. The British Journal of Surgery 1994, 81(12):1792-1794.
122. Rossi M., Corradini C., Amaretti A., Nicolini M., Pompei A., Zanoni S., Matteuzzi D. Fermentation of fructooligosaccharides and inulin by bifidobacteria: A comparative study of pure and fecal cultures. Applied and Environmental Microbiology 2005, 71(10):6150-6158.
123. Rowland I. The influence of the gut microflora on food toxicity. The Proceedings of the Nutrition Society 1981, 40(1):67-74.
124. Rowland I.R., Bearne C.A., Fischer R., Pool-Zobel B.L. The effect of lactulose on DNA damage induced by DMH in the colon of human flora-associated rats. Nutrition and Cancer 1996, 26(1):37-47.
125. Rowland I.R., Tanaka R. The effects of transgalactosylated oligosaccharides on gut flora metabolism in rats associated with a human faecal microflora. The Journal of Applied Bacteriology 1993, 74(6):667-674.
126. Salminen S., Salminen E. Lactulose, lactic acid bacteria, intestinal microecology and mucosal protection. Scandinavian Journal of Gastroenterology. Supplement 1997, 222:45-48.
127. Salvini F., Riva E., Salvatici E., Boehm G., Jelinek J., Banderali G., Giovannini M. A specific prebiotic mixture added to starting infant formula has long-lasting bifidogenic effects. The Journal of Nutrition 2011, 141(7):1335-1339.
128. Samelson S.L., Nelson R.L., Nyhus L.M. Protective role of faecal pH in experimental colon carcinogenesis. Journal of the Royal Society of Medicine 1985, 78(3):230-233.
129. Sangwan V., Tomar S.K., Singh R.R., Singh A.K., Ali B. Galactooligosaccharides: Novel components of designer foods. Journal of Food Science 2011, 76(4):R103-R111.
130. Sarmiento-Rubiano L.A., Zuniga M., Perez-Martinez G., Yebra M.J. Dietary supplementation with sorbitol results in selective enrichment of lactobacilli in rat intestine. Research in Microbiology 2007, 158(8-9):694-701.
131. 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 galacto-oligosaccharides in a rat model. FEMS Microbiology Ecology 2008, 66(3):528-536.
132. Scalabrin D.M., Mitmesser S.H., Welling G.W., Harris C.L., Marunycz J.D., Walker D.C., Bos N.A., Tolkko S., Salminen S., Vanderhoof J.A. New prebiotic blend of polydextrose and galacto-oligosaccharides has a bifidogenic effect in young infants. Journal of Pediatric Gastroenterology and Nutrition 2012, 54(3):343-352.
133. Scharlau D., Borowicki A., Habermann N., Hofmann T., Klenow S., Miene C., Munjal U., Stein K., Glei M. Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutation Research 2009, 682(1):39-53.
134. Schuster-Wolff-Buhring R., Fischer L., Hinrichs J. Production and physiological action of the disaccharide lactulose. International Dairy Journal 2010, 20:731-741.
135. Searle L.E.J., Cooley W.A., Jones G., Nunez A., Crudgington B., Weyer U., Dugdale A.H., Tzortzis G., Collins J.W., Woodward M.J., La Ragione R.M. Purified galactooligosaccharide, derived from a mixture produced by the enzymic activity of Bifidobacterium bifidum, reduces Salmonella enterica serovar Typhimurium adhesion and invasion in vitro and in vivo. Journal of Medical Microbiology 2010, 59(12):1428-1439.
136. Searle L.E.J., Jones G., Tzortzis G., Woodward M., Rastall R.A., Gibson G.R., La Ragione R.M. Low molecular weight fractions of BiMuno® exert immunostimulatory properties in murine macrophages. Journal of Functional Foods 2012, 4(4):941-953.
137. Seki N., Hamano H., Iiyama Y., Asano Y., Kokubo S., Yamauchi K., Tamura Y., Uenishi K., Kudou H. Effect of lactulose on calcium and magnesium absorption: A study using stable isotopes in adult men. Journal of Nutritional Science and Vitaminology 2007, 53(1):5-12.
138. Shafe A.C., Lee S., Dalrymple J.S., Whorwell P.J. The LUCK study: Laxative usage in patients with GP-diagnosed constipation in the UK, within the general population and in pregnancy. An epidemiological study using the General Practice Research Database (GPRD). Therapeutic Advances in Gastroenterology 2011, 4(6):343-363.
139. Shen Q., Tuohy K.M., Gibson G.R., Ward R.E. In vitro measurement of the impact of human milk oligosaccharides on the faecal microbiota of weaned formula-fed infants compared to a mixture of prebiotic fructooligosaccharides and galactooligosaccharides. Letters in Applied Microbiology 2011, 52(4):337-343.
140. Shimamoto T., Xu X.J., Okazaki N., Kawakami H., Tsuchiya T. A cryptic melibiose transporter gene possessing a frameshift from Citrobacter freundii. Journal of Biochemistry 2001, 129(4):607-613.
141. Shoaf K., Mulvey G.L., Armstrong G.D., Hutkins R.W. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infection and Immunity 2006, 74(12):6920-6928.
142. Silvestroni A., Connes C., Sesma F., De Giori G.S., Piard J.C. Characterization of the melA locus for alpha-galactosidase in Lactobacillus plantarum. Applied and Environmental Microbiology 2002, 68(11):5464-5471.
143. Suarez F.L., Springfield J., Furne J.K., Lohrmann T.T., Kerr P.S., Levitt M.D. Gas production in human ingesting a soybean flour derived from beans naturally low in oligosaccharides. The American Journal of Clinical Nutrition 1999, 69(1):135-139.
144. Suzuki H., Li S.C., Li Y.T. Alpha-galactosidase from Mortierella vinacea. Crystallization and properties. The Journal of Biological Chemistry 1970, 245(4):781-786.
145. Swennen K., Courtin C.M., Delcour J.A. Non-digestible oligosaccharides with prebiotic properties. Critical Reviews in Food Science and Nutrition 2006, 46(6):459-471.
146. Tabbers M.M., Boluyt N., Berger M.Y., Benninga M.A. Clinical practice: Diagnosis and treatment of functional constipation. European Journal of Pediatrics 2011, 170(8):955-963.
147. Takemura N., Ozawa K., Kimura N., Watanabe J., Sonoyama K. Inulin-type fructans stimulated the growth of exogenously administered Lactobacillus plantarum No. 14 in the mouse gastrointestinal tract. Bioscience, Biotechnology, and Biochemistry 2010, 74(2):375-381.
148. Talbot G., Sygusch J. Purification and characterization of thermostable beta-mannanase and alpha-galactosidase from Bacillus stearothermophilus. Applied and Environmental Microbiology 1990, 56(11):3505-3510.
149. Tamura Y., Mizota T., Shimamura S., Tomita M. Lactulose and its application to the food and pharmaceutical industries. Bulletin of the International Dairy Federation 1993, 289:43-53.
150. Tong J.L., Ran Z.H., Shen J., Fan G.Q., Xiao S.D. Association between fecal bile acids and colorectal cancer: A meta-analysis of observational studies. Yonsei Medical Journal 2008, 49(5):792-803.
151. Torres D.P.M., Goncalves M.P., Teixeira J.A., Rodrigues L.R. Galacto-oligosaccharides: Production, properties, applications, and significance as prebiotics. Comprehensive Reviews in Food Science and Food Safety 2010, 9(5):438-454.
152. Tzortzis G., Jay A.J., Baillon M.L., Gibson G.R., Rastall R.A. Synthesis of alpha-galactooligosaccharides with alpha-galactosidase from Lactobacillus reuteri of canine origin. Applied Microbiology and Biotechnology 2003, 63(3):286-292.
153. U.S.Food and Drug Administration Complementary and Alternative Medicine Products and their Regulation by the Food and Drug Administration. Guidance for Industry http://www.fda.gov/RegulatoryInformation/Guidances/ucm144657.htm?utm_source=fdaSearch%26utm_medium=website%26utm_term=prebiotics%26utm_content=10.
154. van Berge Henegouwen G.P., van der Werf S.D., Ruben A.T. Effect of long term lactulose ingestion on secondary bile salt metabolism in man: Potential protective effect of lactulose in colonic carcinogenesis. Gut 1987, 28(6):675-680.
155. van Dokkum W., Wezendonk B., Srikumar T.S., van den Heuvel E.G. Effect of nondigestible oligosaccharides on large-bowel functions, blood lipid concentrations and glucose absorption in young healthy male subjects. European Journal of Clinical Nutrition 1999, 53(1):1-7.
156. Vaisman N., Press J., Leibovitz E., Boehm G., Barak V. Short-term effect of prebiotics administration on stool characteristics and serum cytokines dynamics in very young children with acute diarrhea. Nutrients 2010, 2(7):683-692.
157. Van den Heuvel E.G., Mujis T., Van Dokkum W., Schaafsma G. Lactulose stimulates calcium absorption in postmenopausal women. Journal of Bone and Mineral Research 1999, 14(7):1211-1216.
158. Van der Meulen R., Adriany T., Verbrugghe K., De Vuyst L. Kinetic analysis of bifidobacterial metabolism reveals a minor role for succinic acid in the regeneration of NAD+ through its growth-associated production. Applied and Environmental Microbiology 2006, 72(8):5204-5210.
159. Vanhoutte T., De Preter V., De Brandt E., Verbeke K., Swings J., Huys G. Molecular monitoring of the fecal microbiota of healthy human subjects during administration of lactulose and Saccharomyces boulardii. Applied and Environmental Microbiology 2006, 72(9):5990-5997.
160. Vos A.P., M'Rabet L., Stahl B., Boehm G., Garssen J. Immune-modulatory effects and potential working mechanisms of orally applied nondigestible carbohydrates. Critical Reviews in Immunology 2007, 27(2):97-140.
161. Vulevic J., Drakoularakou A., Yaqoob P., Tzortzis G., Gibson G.R. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. The American Journal of Clinical Nutrition 2008, 88(5):1438-1446.
162. Wada J., Ando T., Kiyohara M., Ashida H., Kitaoka M., Yamaguchi M., Kumagai H., Katayama T., Yamamoto K. Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Applied and Environmental Microbiology 2008, 74(13):3996-4004.
163. Wijnands M.V., Appel M.J., Hollanders V.M., Woutersen R.A. A comparison of the effects of dietary cellulose and fermentable galacto-oligosaccharide, in a rat model of colorectal carcinogenesis: Fermentable fibre confers greater protection than non-fermentable fibre in both high and low fat backgrounds. Carcinogenesis 1999, 20(4):651-656.
164. Wijnands M.V., Schoterman H.C., Bruijntjes J.B., Hollanders V.M., Woutersen R.A. Effect of dietary galacto-oligosaccharides on azoxymethane-induced aberrant crypt foci and colorectal cancer in Fischer 344 rats. Carcinogenesis 2001, 22(1):127-132.
165. Wong J.M., de Souza R., Kendall C.W., Emam A., Jenkins D.J. Colonic health: Fermentation and short chain fatty acids. Journal of Clinical Gastroenterology 2006, 40(3):235-243.
166. Yoshida E., Sakurama H., Kiyohara M., Nakajima M., Kitaoka M., Ashida H., Hirose J., Katayama T., Yamamoto K., Kumagai H. Bifidobacterium longum subsp. infantis uses two different beta-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 2012, 22(3):361-368.
167. Zenhom M., Hyder A., de Vrese M., Heller K.J., Roeder T., Schrezenmeir J. Prebiotic oligosaccharides reduce proinflammatory cytokines in intestinal Caco-2 cells via activation of PPARgamma and peptidoglycan recognition protein 3. The Journal of Nutrition 2011, 141(5):971-977.
168. Zhang X., Vrijenhoek J.E., Bonten M.J., Willems R.J., van Schaik W. A genetic element present on megaplasmids allows Enterococcus faecium to use raffinose as carbon source. Environmental Microbiology 2011, 13(2):518-528.
169. Zhao H., Lu L., Xiao M., Wang Q., Lu Y., Liu C., Wang P., Kumagai H., Yamamoto K. Cloning and characterization of a novel alpha-galactosidase from Bifidobacterium breve 203 capable of synthesizing Gal-alpha-1,4 linkage. FEMS Microbiology Letters 2008, 285(2):278-283.
170. Zhong Y., Cai D., Cai W., Geng S., Chen L., Han T. Protective effect of galactooligosaccharide-supplemented enteral nutrition on intestinal barrier function in rats with severe acute pancreatitis. Clinical Nutrition (Edinburgh, Scotland) 2009, 28(5):575-580.