Skip to main content
PMC home page
Gut logoLink to Gut
. 1999 Dec;45(6):840–847. doi: 10.1136/gut.45.6.840

Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs

M Govers 1, N Gannon 1, F Dunshea 1, P Gibson 1, J Muir 1
PMCID: PMC1727739  PMID: 10562582

Abstract

BACKGROUND—Recent studies suggest that resistant starch (effective in producing butyrate and lowering possibly toxic ammonia) is rapidly fermented in the proximal colon; the distal colon especially would, however, benefit from these properties of resistant starch.
AIMS—To determine whether wheat bran (a rich source of insoluble non-starch polysaccharides), known to hasten gastrointestinal transit, could carry resistant starch through to the distal colon and thus shift its site of fermentation.
METHODS—Twenty four pigs were fed four human type diets: a control diet, or control diet supplemented with resistant starch, wheat bran, or both. Intestinal contents and faeces were collected after two weeks.
RESULTS—Without wheat bran, resistant starch was rapidly fermented in the caecum and proximal colon. Supplementation with wheat bran inhibited the caecal fermentation of resistant starch, resulting in an almost twofold increase (from 12.9 (2.5) to 20.5 (2.1) g/day, p<0.05) in resistant starch being fermented between the proximal colon and faeces. This resulted in higher butyrate (133%, p<0.05) and lower ammonia (81%, p<0.05) concentrations in the distal colonic regions.
CONCLUSIONS—Wheat bran can shift the fermentation of resistant starch further distally, thereby improving the luminal conditions in the distal colonic regions where tumours most commonly occur. Therefore, the combined consumption of resistant starch and insoluble non-starch polysaccharides may contribute to the dietary modulation of colon cancer risk.


Keywords: resistant starch; non-starch polysaccharides; colonic fermentation; butyrate; ammonia; colon cancer risk

Full Text

The Full Text of this article is available as a PDF (143.4 KB).

Figure 1  .

Figure 1  

Open in a new tab

Effects of diets supplemented with resistant starch (RS) and/or non-starch polysaccharide (NSP) on daily amounts of (A) starch and (B) NSP in intestinal contents and faeces. *Significantly different from control group (one way ANOVA, p<0.05). †Significant positive interaction between RS and NSP (two way ANOVA, p<0.05).

Figure 2  .

Figure 2  

Open in a new tab

Effects of diets supplemented with resistant starch (RS) and/or non-starch polysaccharide (NSP) on pH of intestinal contents and faeces. *Significantly different from control group (one way ANOVA, p<0.05).

Figure 3  .

Figure 3  

Open in a new tab

Effects of diets supplemented with resistant starch (RS) and/or non-starch polysaccharide (NSP) on concentrations of (A) total short chain fatty acids (SCFA) and (B) butyrate, and on daily amounts of (C) total SCFA and (D) butyrate in intestinal contents and faeces. *Significantly different from control group (one way ANOVA, p<0.05). †Significant positive interaction between RS and NSP (two way ANOVA, p<0.05).

Figure 4  .

Figure 4  

Open in a new tab

Effects of diets supplemented with resistant starch (RS) and/or non-starch polysaccharide (NSP) on concentrations of ammonia in intestinal contents and faeces. *Significantly different from control group (one way ANOVA, p<0.05). †Significant positive interaction between RS and NSP (two way ANOVA, p<0.05).

Figure 5  .

Figure 5  

Open in a new tab

Relation between total short chain fatty acid (SCFA) concentration and pH in intestinal and faecal samples. Ileum to middle colon: r=−0.84, n=96, p<0.001; distal colon and faeces: r=+0.10, n=38, NS. Individual sections: ileum: r=−0.52, p<0.001; caecum: r=−0.60, p<0.001; proximal colon: r=−0.72, p<0.001; middle colon: r=−0.40, p<0.001; distal colon: r=−0.05, NS; faeces: r=+0.28, NS (Pearson's correlation).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Birkett A., Muir J., Phillips J., Jones G., O'Dea K. Resistant starch lowers fecal concentrations of ammonia and phenols in humans. Am J Clin Nutr. 1996 May;63(5):766–772. doi: 10.1093/ajcn/63.5.766. [DOI] [PubMed] [Google Scholar]
  2. Cassidy A., Bingham S. A., Cummings J. H. Starch intake and colorectal cancer risk: an international comparison. Br J Cancer. 1994 May;69(5):937–942. doi: 10.1038/bjc.1994.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clinton S. K., Bostwick D. G., Olson L. M., Mangian H. J., Visek W. J. Effects of ammonium acetate and sodium cholate on N-methyl-N'-nitro-N-nitrosoguanidine-induced colon carcinogenesis of rats. Cancer Res. 1988 Jun 1;48(11):3035–3039. [PubMed] [Google Scholar]
  4. Cummings J. H., Beatty E. R., Kingman S. M., Bingham S. A., Englyst H. N. Digestion and physiological properties of resistant starch in the human large bowel. Br J Nutr. 1996 May;75(5):733–747. doi: 10.1079/bjn19960177. [DOI] [PubMed] [Google Scholar]
  5. Englyst H. N., Cummings J. H. Improved method for measurement of dietary fiber as non-starch polysaccharides in plant foods. J Assoc Off Anal Chem. 1988 Jul-Aug;71(4):808–814. [PubMed] [Google Scholar]
  6. Englyst H. N., Kingman S. M., Cummings J. H. Classification and measurement of nutritionally important starch fractions. Eur J Clin Nutr. 1992 Oct;46 (Suppl 2):S33–S50. [PubMed] [Google Scholar]
  7. Goodlad J. S., Mathers J. C. Digestion by pigs of non-starch polysaccharides in wheat and raw peas (Pisum sativum) fed in mixed diets. Br J Nutr. 1991 Mar;65(2):259–270. doi: 10.1079/bjn19910085. [DOI] [PubMed] [Google Scholar]
  8. Goodlad J. S., Mathers J. C. Large bowel fermentation in rats given diets containing raw peas (Pisum sativum). Br J Nutr. 1990 Sep;64(2):569–587. doi: 10.1079/bjn19900057. [DOI] [PubMed] [Google Scholar]
  9. Graham H., Aman P. The pig as a model in dietary fibre digestion studies. Scand J Gastroenterol Suppl. 1987;129:55–61. doi: 10.3109/00365528709095851. [DOI] [PubMed] [Google Scholar]
  10. Heijnen M. L., Beynen A. C. Consumption of retrograded (RS3) but not uncooked (RS2) resistant starch shifts nitrogen excretion from urine to feces in cannulated piglets. J Nutr. 1997 Sep;127(9):1828–1832. doi: 10.1093/jn/127.9.1828. [DOI] [PubMed] [Google Scholar]
  11. Key F. B., Mathers J. C. Digestive adaptations of rats given white bread and cooked haricot beans (Phaseolus vulgaris): large-bowel fermentation and digestion of complex carbohydrates. Br J Nutr. 1995 Sep;74(3):393–406. doi: 10.1079/bjn19950143. [DOI] [PubMed] [Google Scholar]
  12. Key F. B., Mathers J. C. Gastrointestinal responses of rats fed on white and wholemeal breads: complex carbohydrate digestibility and the influence of dietary fat content. Br J Nutr. 1993 Mar;69(2):481–495. doi: 10.1079/bjn19930049. [DOI] [PubMed] [Google Scholar]
  13. Kritchevsky D. Epidemiology of fibre, resistant starch and colorectal cancer. Eur J Cancer Prev. 1995 Oct;4(5):345–352. doi: 10.1097/00008469-199510000-00003. [DOI] [PubMed] [Google Scholar]
  14. Lin H. C., Visek W. J. Colon mucosal cell damage by ammonia in rats. J Nutr. 1991 Jun;121(6):887–893. doi: 10.1093/jn/121.6.887. [DOI] [PubMed] [Google Scholar]
  15. Lin H. C., Visek W. J. Large intestinal pH and ammonia in rats: dietary fat and protein interactions. J Nutr. 1991 Jun;121(6):832–843. doi: 10.1093/jn/121.6.832. [DOI] [PubMed] [Google Scholar]
  16. Marsono Y., Illman R. J., Clarke J. M., Trimble R. P., Topping D. L. Plasma lipids and large bowel volatile fatty acids in pigs fed on white rice, brown rice and rice bran. Br J Nutr. 1993 Sep;70(2):503–513. doi: 10.1079/bjn19930144. [DOI] [PubMed] [Google Scholar]
  17. 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 Mar;34(3):386–391. doi: 10.1136/gut.34.3.386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McIntyre A., Young G. P., Taranto T., Gibson P. R., Ward P. B. Different fibers have different regional effects on luminal contents of rat colon. Gastroenterology. 1991 Nov;101(5):1274–1281. doi: 10.1016/0016-5085(91)90077-x. [DOI] [PubMed] [Google Scholar]
  19. Miller E. R., Ullrey D. E. The pig as a model for human nutrition. Annu Rev Nutr. 1987;7:361–382. doi: 10.1146/annurev.nu.07.070187.002045. [DOI] [PubMed] [Google Scholar]
  20. Muir J. G., O'Dea K. Validation of an in vitro assay for predicting the amount of starch that escapes digestion in the small intestine of humans. Am J Clin Nutr. 1993 Apr;57(4):540–546. doi: 10.1093/ajcn/57.4.540. [DOI] [PubMed] [Google Scholar]
  21. Newmark H. L., Lupton J. R. Determinants and consequences of colonic luminal pH: implications for colon cancer. Nutr Cancer. 1990;14(3-4):161–173. doi: 10.1080/01635589009514091. [DOI] [PubMed] [Google Scholar]
  22. Noakes M., Clifton P. M., Nestel P. J., Le Leu R., McIntosh G. Effect of high-amylose starch and oat bran on metabolic variables and bowel function in subjects with hypertriglyceridemia. Am J Clin Nutr. 1996 Dec;64(6):944–951. doi: 10.1093/ajcn/64.6.944. [DOI] [PubMed] [Google Scholar]
  23. Payler D. K., Pomare E. W., Heaton K. W., Harvey R. F. The effect of wheat bran on intestinal transit. Gut. 1975 Mar;16(3):209–213. doi: 10.1136/gut.16.3.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Phillips J., Muir J. G., Birkett A., Lu Z. X., Jones G. P., O'Dea K., Young G. P. Effect of resistant starch on fecal bulk and fermentation-dependent events in humans. Am J Clin Nutr. 1995 Jul;62(1):121–130. doi: 10.1093/ajcn/62.1.121. [DOI] [PubMed] [Google Scholar]
  25. Rémésy C., Demigné C. Specific effects of fermentable carbohydrates on blood urea flux and ammonia absorption in the rat cecum. J Nutr. 1989 Apr;119(4):560–565. doi: 10.1093/jn/119.4.560. [DOI] [PubMed] [Google Scholar]
  26. Scheppach W. Effects of short chain fatty acids on gut morphology and function. Gut. 1994 Jan;35(1 Suppl):S35–S38. doi: 10.1136/gut.35.1_suppl.s35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Scott T. A., Boldaji F. Comparison of inert markers [chromic oxide or insoluble ash (Celite)] for determining apparent metabolizable energy of wheat- or barley-based broiler diets with or without enzymes. Poult Sci. 1997 Apr;76(4):594–598. doi: 10.1093/ps/76.4.594. [DOI] [PubMed] [Google Scholar]
  28. Shetty P. S., Kurpad A. V. Increasing starch intake in the human diet increases fecal bulking. Am J Clin Nutr. 1986 Feb;43(2):210–212. doi: 10.1093/ajcn/43.2.210. [DOI] [PubMed] [Google Scholar]
  29. Tomlin J., Read N. W. The effect of resistant starch on colon function in humans. Br J Nutr. 1990 Sep;64(2):589–595. doi: 10.1079/bjn19900058. [DOI] [PubMed] [Google Scholar]
  30. Topping D. L., Gooden J. M., Brown I. L., Biebrick D. A., McGrath L., Trimble R. P., Choct M., Illman R. J. A high amylose (amylomaize) starch raises proximal large bowel starch and increases colon length in pigs. J Nutr. 1997 Apr;127(4):615–622. doi: 10.1093/jn/127.4.615. [DOI] [PubMed] [Google Scholar]
  31. Topping D. L., Illman R. J., Clarke J. M., Trimble R. P., Jackson K. A., Marsono Y. Dietary fat and fiber alter large bowel and portal venous volatile fatty acids and plasma cholesterol but not biliary steroids in pigs. J Nutr. 1993 Jan;123(1):133–143. doi: 10.1093/jn/123.1.133. [DOI] [PubMed] [Google Scholar]
  32. Van Dokkum W., Pikaar N. A., Thissen J. T. Physiological effects of fibre-rich types of bread. 2. Dietary fibre from bread: digestibility by the intestinal microflora and water-holding capacity in the colon of human subjects. Br J Nutr. 1983 Jul;50(1):61–74. doi: 10.1079/bjn19830072. [DOI] [PubMed] [Google Scholar]
  33. Weaver G. A., Krause J. A., Miller T. L., Wolin M. J. Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fiber fermentation; cornstarch fermentation rates correlate negatively with methanogenesis. Am J Clin Nutr. 1992 Jan;55(1):70–77. doi: 10.1093/ajcn/55.1.70. [DOI] [PubMed] [Google Scholar]
  34. Young G. P., McIntyre A., Albert V., Folino M., Muir J. G., Gibson P. R. Wheat bran suppresses potato starch--potentiated colorectal tumorigenesis at the aberrant crypt stage in a rat model. Gastroenterology. 1996 Feb;110(2):508–514. doi: 10.1053/gast.1996.v110.pm8566598. [DOI] [PubMed] [Google Scholar]
  35. van Munster I. P., Tangerman A., Nagengast F. M. Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig Dis Sci. 1994 Apr;39(4):834–842. doi: 10.1007/BF02087431. [DOI] [PubMed] [Google Scholar]

Articles from Gut are provided here courtesy of BMJ Publishing Group

RESOURCES