iBet uBet web content aggregator. Adding the entire web to your favor.
iBet uBet web content aggregator. Adding the entire web to your favor.



Link to original content: https://doi.org/10.1007/BF02087431
Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation | Digestive Diseases and Sciences Skip to main content

Advertisement

Springer Nature Link
Log in

Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation

  • Original Articles
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Resistant starch is by definition that part of starch that escapes digestion in the small bowel. Cecal fermentation of resistant starch into short-chain fatty acids will result subsequently in a decrease in pH. Thus, resistant starch may have the same effect on colonic luminal contents and mucosa as some fiber components. We studied the effects of adding 45 g native amylomaize (Hylon-VII) to a standardized diet in 14 healthy volunteers on fermentation and colonic mucosal proliferation. Hylon-VII is a high amylose maize starch, containing 62% resistant starch. During amylomaize consumption, breath hydrogen excretion rose 85% and fecal short chain fatty acid output increased 35% (P<0.01). Excretion of primary bile acids increased and the soluble deoxycholic acid concentration decreased by 50% (P=0.002). Subsequently, cytotoxicity of the aqueous phase of feces—as measured on a colon cancer cell line—decreased (P=0.007). Colonic mucosal proliferation in rectal biopsies (proliferating cell nuclear antigen immunostaining) decreased from 6.7 to 5.4% (P=0.05). We speculate that resistant starch consumption decreases colonic mucosal proliferation as a result of the decreased formation of cytotoxic secondary bile acids, which is possibly mediated through acidification of the large bowel by production of short-chain fatty acids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kashtan H, Stern HS, Jenkins DJ, Jenkins AL, Thompson LU, Hay K, Marcon N, Minkin S, Bruce WR: Colonic fermentation and markers of colorectal-cancer risk. Am J Clin Nutr 55:723–728, 1992

    Google Scholar 

  2. Clausen MR, Bonnen H, Mortensen PB: Colonic fermentation of dietary fibre to short chain fatty acids in patients with adenomatous polyps and colonic cancer. Gut 32:923–928, 1991

    Google Scholar 

  3. Weaver GA, Krause JA, Miller TL, Wolin MJ: Short chain fatty acid distributions of enema samples from a sigmoidoscopy population: An association of high acetate and low butyrate ratios with adenomatous polyps and colon cancer. Gut 29:1539–1543, 1988

    Google Scholar 

  4. Dexter DL, Lev R, McKendall GR, Mitchell P, Calabres P: Sodium butyrate-induced alteration of growth properties and glycogen levels in cultured human colon carcinoma cells. Histochem J 16:137–149, 1984

    Google Scholar 

  5. Friedman E, Lightdale C, Winawer S: Effects of psyllium fiber and short-chain organic acids derived from fiber breakdown on colonic epithelial cells from high-risk patients. Cancer Lett 43:121–124, 1988

    Google Scholar 

  6. MacDonald IA, Singh G, Mahony DE, Meier CE: Effect of pH on bile salt degradation by mixed fecal cultures. Steroids 32:245–256, 1978

    Google Scholar 

  7. Nagengast FM, Hectors MP, Buys WA, van Tongeren JH: Inhibition of secondary bile acid formation in the large intestine by lactulose in healthy subjects of two different age groups. Eur J Clin Invest 18:56–61, 1988

    Google Scholar 

  8. Rafter JJ, Eng VW, Furrer R, Medline A, Bruce WR: Effects of calcium and pH on the mucosal damage produced by deoxycholic acid in the rat colon. Gut 27:1320–1329, 1986

    Google Scholar 

  9. Lapre JA, van der Meer R: Diet-induced increase of colonic bile acids stimulates lytic activity of fecal water and proliferation of colonic cells. Carcinogenesis 13:41–44, 1992

    Google Scholar 

  10. Deschner EE, Long FC, Hakissan M, Herrman SL: Differential susceptibility of AKR, C57BL/6J, and CF1 mice to 1,2-dimethylhydrazine-induced colonic tumor formation predicted by proliferative characteristics of colonic epithelial cells. J Natl Cancer Inst 70:279–282, 1983

    Google Scholar 

  11. Lipkin M, Enker WE, Winawer SJ: Tritiated-thymidine labeling of rectal epithelial cells in “non-prep” biopsies of individuals at increased risk for colonic neoplasia. Cancer Lett 37:153–161, 1987

    Google Scholar 

  12. Terpstra OT, van-Blankenstein M, Dees J, Eilers GA: Abnormal pattern of cell proliferation in the entire colonic mucosa of patients with colon adenoma or cancer. Gastroenterology 92:704–708, 1987

    Google Scholar 

  13. Cohen BI, Raicht RF, Deschner EE, et al: Effect of cholic acid feeding onN-methyl-N-nitrosourea-induced colon tumors and cell kinetics in rats. J Natl Cancer Inst 64:573–578, 1980

    Google Scholar 

  14. Weisburger JH, Reddy BS, Barnes WS, Wynder EL: Bile acids, but not neutral sterols, are tumor promoters in the colon in man and in rodents. Environ Health Perspect 50:101–107, 1983

    Google Scholar 

  15. Hill MJ: Bile acids and colorectal cancer: Hypothesis. Eur J Cancer Prev 1(suppl 2):69–72, 1991

    Google Scholar 

  16. Steimetz KA, Potter JD: Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Control 2:325–357, 1991

    Google Scholar 

  17. Vargas PA, Alberts DS, Ritenbauch C, Atwood JR, Sampliner R, Earnest D, Clark LC, Emerson SS: Dietary fiber and colon cancer prevention. Cancer Bull 43:549–561, 1991

    Google Scholar 

  18. Willett WC, Stampfer MJ, Colditz GA, Rosner BA, Speizer FE: Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N Engl J Med 323:1664–1672, 1990

    Google Scholar 

  19. Giovannucci E, Stampfer MJ, Colditz G, Rimm EB, Willett WC: Relationship of diet to risk of colorectal adenoma in men. J Natl Cancer Inst 84:91–98, 1992

    Google Scholar 

  20. Alberts DS, Einspahr J, Rees-McGee S, Ramanujam P, Buller MK, Clark L, Ritenbaugh C, Atwood J, Pethigal P, Earnest D, et al: Effects of dietary wheat bran fiber on rectal epithelial cell proliferation in patients with resection for colorectal cancers. J Natl Cancer Inst 82:1280–1285, 1990

    Google Scholar 

  21. McIntyre A, Young GP, Taranto T, Gibson PR, Ward PB: Different fibers have different regional effects on luminal contents of rat colon. Gastroenterology 101:1274–1281, 1991

    Google Scholar 

  22. van Munster IP, Nagengast FM: The influence of dietary fibre on bile acid metabolism. Eur J Cancer Prev 1(suppl 2):35–44, 1991

    Google Scholar 

  23. Reddy BS, Engle A, Simi B, Goldman M: Effect of dietary fiber on colonic bacterial enzymes and bile acids in relation to colon cancer. Gastroenterology 102:1475–1482, 1992

    Google Scholar 

  24. Trock B, Lanza E, Greenwald P: Dietary fiber, vegetables, and colon cancer: Critical review and meta-analysis of the epidemiological evidence. J Natl Cancer Inst 83:650–661, 1990

    Google Scholar 

  25. Cummings JH, Englyst HN: Fermentation in the human large intestine and the available substrates. Am J Clin Nutr 45:1243–1255, 1987

    Google Scholar 

  26. Chapman RW, Sillery JK, Graham MM, Saunders DR: Absorption of starch by healthy ileostomates: Effect of transit time and of carbohydrate load. Am J Clin Nutr 41:1244–1248, 1985

    Google Scholar 

  27. Englyst HN, Cummings JH: Digestion of the polysaccharides of some cereal foods in the human small intestine. Am J Clin Nutr 42:778–787, 1985

    Google Scholar 

  28. Thornton JR, Dryden A, Kelleher J, Losowsky MS: Super-efficient starch absorption. A risk factor for colonic neoplasia? Dig Dis Sci 32:1088–1091, 1987

    Google Scholar 

  29. Nordgaard I, Rumessen JJ, Damgaard Nielsen A, Gudmand-Hoyer E: Absorption of wheat starch in patients resected for left-sided colonic cancer. Scand J Gastroenterol 27:632–634, 1992

    Google Scholar 

  30. Englyst HN, Kingman SM, Cummings JH: Classification and measurement of nutritionally important starch fractions. Eur J Clin Nutr 46 (suppl 2):S33-S50, 1992

    Google Scholar 

  31. Tangerman A, van Schaik A, Meuwese-Arends MT, van Tongeren JHM: Quantitative determination of C2–C8 volatile fatty acids in human serum by vacuum distillation and gas chromatography. Clin Chim Acta 133:341–348, 1983

    Google Scholar 

  32. Tangerman A, van Schaik A, van der Hoek EW: Analysis of conjugated and unconjugated bile acids in serum and jejunal fluid of normal subjects. Clin Chim Acta 159:123–132, 1986

    Google Scholar 

  33. van Faassen A, Nagengast FM, Hectors MPC, Van den Broek WJM, Huijbregts AWM, van der Werf SDJ, van Berge Henegouwen GP, van Tongeren JHM: Determination of individual human faecal bile acids by gas-liquid chromatography after enzymatic deconjugation and simultaneous solvolysis and methylation using dimethoxypropane. Clin Chim Acta 152:231–239, 1985

    Google Scholar 

  34. Bjork I, Nyman M, Pedersen B, Siljestrom M, Asp N-G, Eggum BO: Formation of enzyme resistant starch during autoclaving of wheat starch: Studiesin vitro andin vivo. J Cereal Sci 6:159–172, 1987

    Google Scholar 

  35. van Munster IP, Tangerman A, de Haan AJF, Nagengast FM: A new method for the determination of cytotoxicity of bile acids and the aqueous phase of stool; the effect of calcium. Eur J Clin Invest 23:773–777, 1993

    Google Scholar 

  36. Park JG, Kramer BS, Steinberg SM, Carmichael J, Collins JM, Minna JD, Gazdar AF: Chemosensitivity testing of human colorectal carcinoma cell lines using a tetrazolium-based colorimetric assay. Cancer Res 47:5875–5879, 1987

    Google Scholar 

  37. Hansen MB, Nielsen SE, Berg K: Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Methods 119:203–210, 1989

    Google Scholar 

  38. Mosman T: Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63, 1983

    Google Scholar 

  39. Florent C, Flourie B, Leblond A, Rautureau M, Bernier JJ, Rambaud JC: Influence of chronic lactulose ingestion on the colonic metabolism of lactulose in man (anin vivo study). J Clin Invest 75:608–613, 1985

    Google Scholar 

  40. Perman JA, Modler S, Olson C: Role of pH in production of hydrogen from carbohydrates by colonic bacterial flora. J Clin Invest 67:643–650, 1981

    Google Scholar 

  41. Peters SG, Pomare EW, Fisher CA: Portal and peripheral blood short chain fatty acid concentrations after caecal lactulose installation at surgery. Gut 33:1249–1252, 1992

    Google Scholar 

  42. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT: Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28:1221–1227, 1987

    Google Scholar 

  43. Flourie B, Florent C, Jouany JP: Colonic metabolism of wheat starch in healthy humans. Effects of fecal outputs and clinical symptoms. Gastroenterology 90:111–119, 1986

    Google Scholar 

  44. Gum JR, Kam WK, Byrd JC, Hicks JW, Sleisenger MH, Kim YS: Effects of sodium butyrate on human colonic adenocarcinoma cells. Induction of placental-like alkaline phosphatase. J Biol Chem 262:1092–1097, 1987

    Google Scholar 

  45. Scheppach W, Sommer H, Kirchner T, Paganelli GM, Bartram P, Christl S, Richter F, Dusel G, Kasper H: Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103:51–56, 1992

    Google Scholar 

  46. Caderni G, Bianchini F, Dolara P, Kriebel D: Starchy foods and colon proliferation in mice. Nutr Cancer 15:33–40, 1991

    Google Scholar 

  47. Scheppach W, Fabian C, Ahrens F, Spengler M, Kasper H: Effect of starch malabsorption on colonic function and metabolism in humans. Gastroenterology 95:1549–1555, 1988

    Google Scholar 

  48. Weaver GA, Krause JA, Miller TL, Wolin MJ: 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 55:70–77, 1992

    Google Scholar 

  49. Flourie B, Florent C, Etanchaud F, Evard D, Franchisseur C, Rambaud JC: Starch absorption by healthy man evaluated by lactulose hydrogen breath test. Am J Clin Nutr 47:61–66, 1988

    Google Scholar 

  50. Fallingborg J, Christensen LA, Ingeman-Nielsen M, Jacobseb BA, Abildgaard K, Rasmussen HH: pH-profile and regional transit times of the normal gut by a radiotelemetry device. Aliment Pharmacol Ther 3:605–613, 1989

    Google Scholar 

  51. Hofmann AF, Cravetto C, Molino G, Belforte G, Bona B: Simulation of the metabolism and enterohepatic circulation of endogeneous deoxycholic acid in humans using a physiologic pharmacokinetic model for bile acid metabolism. Gastroenterology 93:693–709, 1987

    Google Scholar 

  52. Okhuysen-Young C, Kellog TF: The effect of cecectomy on fecal bile acid and neutral steroid excretion of the rat. Comp Biochem Physiol (B) 70B:345–347, 1981

    Google Scholar 

  53. Yahiro K, Setoguchi T, Katsuki T: Effect of cecum and appendix on 7α-dehydroxylation and 7β-epimerisation of chenodeoxycholic acid in the rabbit. J Lipid Res 21:215–222, 1980

    Google Scholar 

  54. Fini A, Roda A: Chemical properties of bile acids. IV. Acidity constants of glycine-conjugated bile acids. J Lipid Res 28:755–759, 1987

    Google Scholar 

  55. Geltner-Allinger U, Johansson GK, Gustafsson J, Rafter JJ: Shift from a mixed to a lactovegetarian diet: Influence on acidic lipids in fecal water—a potential risk factor for colon cancer. Am J Clin Nutr 50:992–996, 1989

    Google Scholar 

  56. van Berge Henegouwen GP, van der Werf SD, Ruben AT: Effect of long term lactulose ingestion on secondary bile salt metabolism in man: Potential protective effect of lactulose in colonic carcinogenesis. Gut 28:675–680, 1987

    Google Scholar 

  57. Thornton JR, Heaton KW: Do colonic bacteria contribute to cholesterol gall-stone formation? Effects of lactulose on bile. Br Med J 282:1018–1020, 1981

    Google Scholar 

  58. Andrieux C, Gadelle D, Leprince C, Sacquet E: Effects of some poorly digestible carbohydrates on bile acid bacterial transformations in the rat. Br J Nutr 62:103–119, 1989

    Google Scholar 

  59. Bartram HP, Scheppach W, Heid C, Fabian C, Kasper H: Effect of starch malabsorption on fecal bile acids and neutral sterols in humans: Possible implications for colonic carcinogenesis. Cancer Res 51:4238–4242, 1991

    Google Scholar 

  60. Macfarlane GT, Cummings JH: The colonic flora, fermentation, and large bowel digestive function.In The Large Intestine: Physiology, Pathophysiology, and Disease. SF Phillips, JH Pemberton, RG Shorter (eds). New York, Raven Press, 1991, p 51

    Google Scholar 

  61. Heitman DW, Ord VA, Hunter KE, Cameron IL: Effect of dietary cellulose on cell proliferation and progression of 1,2-dimethylhydrazine-induced colon carcinogenesis in rats. Cancer Res 49:5581–5585, 1989

    Google Scholar 

  62. Jacobs LR, Lupton JR: Relationship between colonic luminal pH, cell proliferation, and colon carcinogenesis in 1,2-dimethylhydrazine treated rats fed high fiber diets. Cancer Res 46:1727–1734, 1986

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. From the Department of Internal Medicine, Groot Ziekengasthuis,'s-Hertogenbosch, The Netherlands

    Ivo P. van Munster MD, Albert Tangerman PhD & Fokko M. Nagengast MD, PhD

  2. Department of Medicine, Division of Gastroenterology, University Hospital Nijmegen, P.O. Box 9101, 6500 HB, Nijmegen, The Netherlands

    Ivo P. van Munster MD, Albert Tangerman PhD & Fokko M. Nagengast MD, PhD

Authors
  1. Ivo P. van Munster MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Albert Tangerman PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fokko M. Nagengast MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This study was financially supported by the Dutch Cancer Foundation, grant 89-04.

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Munster, I.P., Tangerman, A. & Nagengast, F.M. Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Digest Dis Sci 39, 834–842 (1994). https://doi.org/10.1007/BF02087431

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02087431

Key words

Search

Navigation