Differential effects of dietary whey, casein and soya on colonic DNA damage and large bowel SCFA in rats fed diets low and high in resistant starch

British Journal of Nutrition

Volumn 97, Issue 3, 2007, Pages 535-543

  Toden, Shusuke ^a,b   Bird, Anthony R ^a   Topping, David L ^a   Conlon, Michael A ^a  

^a CSIRO   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Casein; Colonic genotoxicity; Resistant starch; Soya protein; Whey protein

Indexed keywords

ACETIC ACID; AMYLOSE; BUTYRIC ACID; CASEIN; DNA; PROPIONIC ACID; STARCH; VEGETABLE PROTEIN; MILK PROTEIN; SOYBEAN PROTEIN; UNCLASSIFIED DRUG; VOLATILE FATTY ACID; WHEY PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; COLON MUCOSA; COMET ASSAY; CONTROLLED STUDY; CORRELATION ANALYSIS; DAIRY PRODUCT; DIETARY INTAKE; DNA DAMAGE; FECES ANALYSIS; MALE; NONHUMAN; PROTEIN INTAKE; RAT; SOYBEAN; STOMACH MUCUS; THICKNESS; WHEY; ANIMAL; CARBOHYDRATE DIET; CECUM; CHEMISTRY; COLON; DRINKING; DRUG EFFECT; EATING; FECES; HISTOLOGY; INTESTINE MUCOSA; METABOLISM; ORGAN SIZE; SPRAGUE DAWLEY RAT; URINE; WEIGHT GAIN;

ANIMALIA; RATTUS;

ANIMALS; CASEINS; CECUM; COLON; DIETARY CARBOHYDRATES; DIETARY PROTEINS; DNA DAMAGE; DRINKING; EATING; FATTY ACIDS, VOLATILE; FECES; INTESTINAL MUCOSA; MALE; MILK PROTEINS; ORGAN SIZE; RATS; RATS, SPRAGUE-DAWLEY; SOYBEAN PROTEINS; STARCH; URINE; WEIGHT GAIN;

EID: 34047257837     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114507336817     Document Type: Article

References (66)

1. Anderson D, Hambly RJ, Yu TW, Thomasoni F & Shuker DE (1999) The effect of potassium diazoacetate on human peripheral lymphocytes, human adenocarcinoma Colon caco-2 cells, and rat primary colon cells in the comet assay. Teratog Carcinog Mutagen 19, 137-146.
2. Annison G, Illman RJ & Topping DL (2003) Acetylated, propionylated or butyrylated starches raise large bowel short-chain fatty acids preferentially when fed to rats. J Nutr 133, 3523-3528.
3. Asano T & McLeod RS (2002) Dietary fibre for the prevention of colorectal adenomas and carcinomas. The Cochrane Database of Systematic Reviews 2002 CD003430.
4. Badger TM, Ronis MJ, Simmen RC & Simmen FA (2005) Soy protein isolate and protection against cancer. J Am Coll Nutr 24, 146S-149S.
5. Bauer-Marinovic M, Florian S, Muller-Schmehl K, Glatt H & Jacobasch G (2006) Dietary resistant starch type 3 prevents tumor induction by 1,2-dimethylhydrazine and alters proliferation, apoptosis and dedifferentiation in rat colon. Carcinogenesis 27, 1849-1859.
6. Belobrajdic DP, McIntosh GH & Owens JA (2003) Whey proteins protect more than red meat against azoxymethane induced ACF in Wistar rats. Cancer Lett 198, 43-51.
7. Bingham SA, Day NE, Luben R, et al. (2003) Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): An observational study. Lancet 361, 1496-1501.
8. Bird AR, Flory C, Davies DA, Usher S & Topping DL (2004) A novel barley cultivar (Himalaya 292) with a specific gene mutation in starch synthase IIa raises large bowel starch and short-chain fatty acids in rats, J Nutr 134, 831-835.
9. Bounous G (2000) Whey protein concentrate (WPC) and glutathione modulation in cancer treatment. Anticancer Res 20, 4785-4792.
10. Cassidy A, Bingham SA & Cummings JH (1994) Starch intake and colorectal cancer risk: An international comparison. Br J Cancer 69, 937-942.
11. Chao A, Thun MJ, Connell CJ, McCullough ML, Jacobs EJ, Flanders WD, Rodriguez C, Sinha R & Calle EE (2005) Meat consumption and risk of colorectal cancer. JAMA 293, 172-182.
12. Chen R, Rabinovitch PS, Crispin DA, Emond MJ, Bronner MP & Brentnall TA (2005) The initiation of colon cancer in a chronic inflammatory setting. Carcinogenesis 26, 1513-1519.
13. Clausen MR & Mortensen PB (1995) Kinetic studies on colonocyte metabolism of short chain fatty acids and glucose in ulcerative colitis. Gut 37, 684-689.
14. Cross AJ & Sinha R (2004) Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ Mol Mutagen 44, 44-55.
15. Cummings JH & Macfarlane GT (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70 443-459.
16. 14C threonine labelled mucin substrate. Gut 37, 58-62.
17. Emenaker NJ & Basson MD (2001) Short chain fatty acids differentially modulate cellular phenotype and c-myc protein levels in primary human nonmalignant and malignant colonocytes. Dig Dis Sci 46, 96-105.
18. Englyst H, Wiggins HS & Cummings JH (1982) Determination of the non-starch polysaccharides in plant foods by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst 107, 307-318.
19. Giovannucci E & Willett WC (1994) Dietary factors and risk of colon cancer. Ann Med 26, 443-452.
20. Govers MJ, Lapre JA, De Vries HT & Van der Meer R (1993) Dietary soybean protein compared with casein damages colonic epithelium and stimulates colonic epithelial proliferation in rats. J Nutr 123, 1709-1713.
21. Hakkak R, Korourian S, Ronis MJ, Johnston JM & Badger TM (2001a) Dietary whey protein protects against azoxymethane-induced colon tumors in male rats. Cancer Epidemiol Biomarkers Prev 10, 555-558.
22. Hakkak R, Korourian S, Ronis MJ, Johnston JM & Badger TM (2001b) Soy protein isolate consumption protects against azoxymethane-induced colon tumors in male rats. Cancer Lett 166, 27-32.
23. Helma C & Uhl M (2000) A public domain image-analysis program for the single-cell gel-electrophoresis (comet) assay. Mutat Res 466 9-15.
24. Jowett SL, Seal CJ, Pearce MS, Phillips E, Gregory W, Barton JR & Welfare MR (2004) Influence of dietary factors on the clinical course of ulcerative colitis: A prospective cohort study. Gut 53, 1479-1484.
25. Kleessen B, Stoof G, Proll J, Schmiedl D, Noack J & Blaut M (1997) Feeding resistant starch affects fecal and cecal microflora and short-chain fatty acids in rats. J Anim Sci 75, 2453-2462.
26. Larsson SC, Rafter J, Holmberg L, Bergkvist L & Wolk A (2005) Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: The Swedish Mammography Cohort. Int J Cancer 113, 829-834.
27. Le Leu RK, Hu Y & Young GP (2002) Effects of resistant starch and nonstarch polysaccharides on colonic luminal environment and genotoxin-induced apoptosis in the rat. Carcinogenesis 23, 713-719.
28. Lee SO, Simons AL, Murphy PA & Hendrich S (2005) Soyasaponins lowered plasma cholesterol and increased fecal bile acids in female golden syrian hamsters. Exp Biol Med (Maywood) 230, 472-478.
29. Lin Y, Meijer GW, Vermeer MA & Trautwein EA (2004) Soy protein enhances the cholesterol-lowering effect of plant sterol esters in cholesterol-fed hamsters. J Nutr 134, 143-148.
30. Lupton JR (1995) Butyrate and colonic cytokinetics: Differences between in vitro and in vivo studies. Eur J Cancer Prev 4 373-378.
31. McBurney MI, Thompson LU, Cuff DJ & Jenkins DJ (1988) Comparison of ileal effluents, dietary fibers, and whole foods in predicting the physiological importance of colonic fermentation. Am J Gastroenterol 83, 536-540.
32. McIntosh GH & Le Leu RK (2001) The influence of dietary proteins on colon cancer risk. Nutr Res 21, 1053-1066.
33. McIntosh GH, Regester GO, Le Leu RK, Royle PJ & Smithers GW (1995) Dairy proteins protect against dimethylhydrazine-induced intestinal cancers in rats. J Nutr 125, 809-816.
34. Moreau NM, Martin LJ, Toquet CS, Laboisse CL, Nguyen PG, Siliart BS, Dumon HJ & Champ MM (2003) Restoration of the integrity of rat caeco-colonic mucosa by resistant starch, but not by fructo-oligosaccharides, in dextran sulfate sodium-induced experimental colitis. Br J Nutr 90, 75-85.
35. Morita T, Kasaoka S, Hase K & Kiriyama S (1999) Psyllium shifts the fermentation site of high-amylose cornstarch toward the distal colon and increases fecal butyrate concentration in rats. J Nutr 129, 2081-2087.
36. Morita T, Kasaoka S, Ohhashi A, Ikai M, Numasaki Y & Kiriyama S (1998) Resistant proteins alter cecal short-chain fatty acid profiles in rats fed high amylose cornstarch. J Nutr 128, 1156-1164.
37. Morita T, Tanabe H, Takahashi K & Sugiyama K (2004) Ingestion of resistant starch protects endotoxin influx from the intestinal tract and reduces D-galactosamine-induced liver injury in rats. J Gastroenterol Hepatol 19, 303-313.
38. Muir JG, Yeow EG, Keogh J, Pizzey C, Bird AR, Sharpe K, O'Dea K & Macrae FA (2004) Combining wheat bran with resistant starch has more beneficial effects on fecal indexes than does wheat bran alone. Am J Clin Nutr 79, 1020-1028.
39. Narisawa T, Magadia NE, Weisbuger JH & Wynder EL (1974) Promoting effect of bile acids on colon carcinogenesis after intrarectal instillation of N-methyl-N′-nitro-N-nitrosoguanidine in rats. J Natl Cancer Inst 53, 1093-1097.
40. National Health and Medical Research Council (2004) Australian code of practice for the care and use of animals for scientific purposes, 7th ed. (http://www.nhmc.gov.au/publications/synopses/ea16syn.htm).
41. Norat T, Bingham S, Ferrari P, et al. (2005) Meat, fish, and colorectal cancer risk: The European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst 97, 906-916.
42. Norat T, Lukanova A, Ferrari P & Riboli E (2002) Meat consumption and colorectal cancer risk: An estimate of attributable and preventable fractions. IARC Sci Publ 156, 223-225.
43. Patten GS, Abeywardena MY, McMurchie EJ & Jahangiri A (2002) Dietary fish oil increases acetylcholine- and eicosanoid-induced contractility of isolated rat ileum. J Nutr 132, 2506-2513.
44. Potter JD, Slattery ML, Bostick RM & Gapstur SM (1993) Colon cancer: A review of the epidemiology. Epidemiol Rev 15, 499-545.
45. Reddy BS (2000) The Fourth DeWitt S. Goodman lecture. Novel approaches to the prevention of colon cancer by nutritional manipulation and chemoprevention. Cancer Epidemiol Biomarkers Prev 9, 239-247.
46. Rieger MA, Parlesak A, Pool-Zobel BL, Rechkemmer G & Bode C (1999) A diet high in fat and meat but low in dietary fibre increases the genotoxic potential of 'faecal water'. Carcinogenesis 20, 2311-2316.
47. Ritzhaupt A, Ellis A, Hosie KB & Shirazi-Beechey SP (1998) The characterization of butyrate transport across pig and human colonic luminal membrane. J Physiol 507, (Pt3), 819-830.
48. Rowland IR, Mallett AK & Wise A (1985) The effect of diet on the mammalian gut flora and its metabolic activities. Crit Rev Toxicol 16, 31-103.
49. Schwiertz A, Lehmann U, Jacobasch G & Blaut M (2002) Influence of resistant starch on the SCFA production and cell counts of butyrate-producing Eubacterium spp. in the human intestine. J Appl Microbiol 93, 157-162.
50. Shaoul R, Okada Y, Cutz E & Marcon MA (2004) Colonic expression of MUC2, MUC5AC, and TFF1 in inflammatory bowel disease in children. J Pediatr Gastroenterol Nutr 38, 488-493.
51. Shimotoyodome A, Meguro S, Hase T, Tokimitsu I & Sakata T (2000) Short chain fatty acids but not lactate or succinate stimulate mucus release in the rat colon. Comp Biochem Physiol A Mol Integr Physiol 125 525-531.
52. Silvester KR, Bingham SA, Pollock JR, Cummings JH & O'Neill IK (1997) Effect of meat and resistant starch on fecal excretion of apparent N-nitroso compounds and ammonia from the human large bowel. Nutr Cancer 29, 13-23.
53. Smith EA & Macfarlane GT (1996) Enumeration of human colonic bacteria producing phenolic and indolic compounds: Effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J Appl Bacteriol 81, 288-302.
54. Spector D, Anthony M, Alexander D & Arab L (2003) Soy consumption and colorectal cancer. Nutr Cancer 47, 1-12.
55. Steinmetz KA & Potter JD (1996) Vegetables, fruit, and cancer prevention: A review. J Am Diet Assoc 96, 1027-1039.
56. Toden S, Bird AR, Topping DL & Conlon MA (2005) Resistant starch attenuates colonic DNA damage induced by higher dietary protein in rats. Nutr Cancer 51, 45-51.
57. Toden S, Bird AR, Topping DL & Conlon MA (2006) Resistant starch prevents colonic DNA damage induced by high dietary cooked red meat or casein in rats. Cancer Biol Ther 5, 267-272.
58. Topping DL & Clifton PM (2001) Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81, 1031-1064.
59. Topping DL, Fukushima M & Bird AR (2003) Resistant starch as a prebiotic and synbiotic: State of the art. Proc Nutr Soc 62, 171-176.
60. Topping DL, Gooden JM, Brown IL, Biebrick DA, McGrath L, Trimble RP, Choct M & Illman RJ (1997) A high amylose (amylomaize) starch raises proximal large bowel starch and increases colon length in pigs. J Nutr 127, 615-622.
61. Tsuda H, Sekine K, Ushida Y, Kuhara T, Takasuka N, Iigo M, Han BS & Moore MA (2000) Milk and dairy products in cancer prevention: Focus on bovine lactoferrin. Mutat Res 462, 227-233.
62. Wacker M. Wanek P, Eder E, Hylla S, Gostner A & Scheppach W (2002) Effect of enzyme-resistant starch on formation of 1,N(2)-propanodeoxyguanosine adducts of trans-4-hydroxy-2-nonenal and cell proliferation in the colonic mucosa of healthy volunteers. Cancer Epidemiol Biomarkers Prev 11, 915-920.
63. Willemsen LE, Koetsier MA, van Deventer SJ & van Tol EA (2003) Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut 52, 1442-1447.
64. Williamson SL, Kartheuser A, Coaker J, Kooshkghazi MD, Fodde R, Burn J & Mathers IC (1999) Intestinal tumorigenesis in the Apc1638N mouse treated with aspirin and resistant starch for up to 5 months. Carcinogenesis 20, 805-810.
65. Wu AH, Yang D & Pike MC (2000) A meta-analysis of soyfoods and risk of stomach cancer: The problem of potential confounders. Cancer Epidemiol Biomarkers Prev 9, 1051-1058.
66. Xiao R, Badger TM & Simmen FA (2005) Dietary exposure to soy or whey proteins alters colonic global gene expression profiles during rat colon tumorigenesis. Mol Cancer 4, 1.