Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-14T23:23:49.973Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of polyunsaturated fatty acids on human colonic bacterial metabolism: an in vitro and in vivo study*

Published online by Cambridge University Press:  09 March 2007

Lorna Thompson  and
Robin C. Spiller
Lorna Thompson
Affiliation:
Department of Therapeutics, University Hospital, Queen's Medical Centre, Nottingham NG7 2UH
Robin C. Spiller
Affiliation:
Department of Therapeutics, University Hospital, Queen's Medical Centre, Nottingham NG7 2UH
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Dietary polyunsaturated fatty acids (PUFA) reduce colonic proliferation and exert a mild laxative effect. We have studied the effect of the highly unsaturatede icosapentaenoic acid ethyl ester (EPA-EE) on the growth and metabolism of colonic bacteria in vitro, and in vivo. For the in vitro study, growth was assessed by viable counts. Bacteroides thetaiotaomicron was significantly inhibited in anaerobic media containing EPA-EE at concentrations > 7 g/I. Escherichia coli was apparently resistant even at 100 g/I. For the in vivo study, ten healthy volunteers ingested 18 g EPA-EE/d for 7 d. Stool frequency, 24 h stool weight and whole-gut transit time were assessed together with breath H2 and 14CO2 excretion following oral ingestion of 15 g lactitol labelled with 0·18 MBq [14C]lactitol. The area under the breath-H2-time curve was significantly reduced by EPA-EE, from a control value of 690·3 (SE 94·2) ppm.h to 449·5 (SE 91·7) ppm.h. Percentage dose of 14CO2 excreted, total stool weight and whole-gut transit time were unaltered, being respectively 24 (SE 2)%, 281 (SE 66) g and 45 (SE 4) h with EPA-EE v. control values of 27 (SE 1)%, 300 (SE 89) g and 42 (SE 5) h. It is concluded that dietary supplementation with EPA-EE reduces breath H2 excretion without apparently impairing overall colonic carbohydrate fermentation. The observed reduction may reflect utilization of H2 to hydrogenate the five double bonds of EPA-EE.

Keywords

Polyunsaturated fatty acidsColonic bacteriaEicosapentaenoic acid
Type
PUFA and colonic bacterial metabolism
Information
British Journal of Nutrition , Volume 74 , Issue 5 , November 1995 , pp. 733 - 741
Copyright
Copyright © The Nutrition Society 1995

References

Andersson, H., Isaksson, B. & Sjogren, B. (1974) Fat-reduced diet in the symptomatic treatment of small bowel disease. Gut 15, 351–359.CrossRefGoogle ScholarPubMed
Anti, M., Marra, G., Armelao, F., Bartoli, G. M., Ficarelli, R., Percesepe, A., De Vitis, I., Maria, G., Sofo, L., Rapaccini, G. L., Gentiloni, N., Piccioni, E. & Miggiano, G. (1992) Effect of n-3 fatty acids on rectal mucosal cell proliferation in subjects at risk for colon cancer. Gastroenterology 103, 883–891.CrossRefGoogle ScholarPubMed
Bond, J. H., Currier, B. E., Buchwald, H. & Levitt, M. D. (1980) Colonic conservation of malabsorbed carbohydrate. Gastroenterology 78, 444–447.CrossRefGoogle ScholarPubMed
Chen, I. S., Hotta, S., Ikeda, I., Cassidy, M. M., Sheppard, A. J. & Vahouny, G. V. (1987) Digestion, absorption and effects on cholesterol absorption of menhaden oil, fish oil concentrate and corn oil by rats. Journal of Nutrition 117, 1676–1680.CrossRefGoogle ScholarPubMed
Chernenko, G. A., Barrowman, J. A., Kean, K. T., Herzberg, G. R. & Keough, K. M. W. (1989) Intestinal absorption and lymphatic transport of fish oil (MaxEPA) in the rat. Biochimica et Biophysica Acta 1004, 95–102.CrossRefGoogle ScholarPubMed
Christl, S. U., Gibson, G. R. & Cummings, J. H. (1992a) Role of dietary sulphate in the regulation of methanogenesis in the human large intestine. Gut 33, 1234–1238.CrossRefGoogle ScholarPubMed
Christl, S. U., Murgatroyd, P. R., Gibson, G. R. & Cummings, J. H. (1992b) Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology 102, 1269–1277.CrossRefGoogle ScholarPubMed
Czerkawski, J. W., Blaxter, K. L. & Wainman, F. W. (1966) The metabolism of oleic, linoleic and linolenic acids by sheep with reference to their effects on methane production. British Journal of Nutrition 20, 349–361.CrossRefGoogle Scholar
Edwards, C. A., Duerden, B. I. & Read, N. W. (1986) Effect of clindamycin on the ability of a continuous culture of colonic bacteria to ferment carbohydrate. Gut 27, 411–417.CrossRefGoogle ScholarPubMed
El Boustani, S., Colette, C, Monnier, L., Descomps, B., Crastes, de, Paulet, A. & Mendy, F. (1987) Enteral absorption of eicosapentaenoic acid in different chemical forms. Lipids 22, 711–714.CrossRefGoogle ScholarPubMed
Galbraith, H. & Miller, T. B. (1973) Effect of long chain fatty acids on bacterial respiration and amino acid uptake. Journal of Applied Bacteriology 36, 659–675.CrossRefGoogle ScholarPubMed
Govers, M. J. A. P. & van der Meer, R. (1992) Effects of dietary calcium and phosphate on the intestinal interactions between calcium, phosphate, fatty acids, and bile acids. Gut 34, 365–370.CrossRefGoogle Scholar
Grimble, G. K., Patil, D. H. & Silk, D. B. A. (1988) Assimilation of lactitol, an ‘unabsorbed’ disaccharide in the normal human colon. Gut 29, 1666–1671.CrossRefGoogle ScholarPubMed
Hawthorne, A. B., Filipowicz, B. L., Edwards, T. J. & Hawkey, C. J. (1990) High dose eicosapentaenoic acid ethyl ester: effects on lipids and neutrophil leukotriene production in normal volunteers.British Journal of Clinical Pharmacology 30, 187–194.CrossRefGoogle ScholarPubMed
Hendrickse, C, Young, D., Thompson, H., Keighley, M. R. B. & Neoptolemos, J. P. (1993) N-3 fats reduce experimental colorectal tumorigenesis including perianastomotic tumours. Gut 34, S46.Google Scholar
Kaihara, S. & Wagner, H. N. (1968) Measurement of intestinal fat absorption with carbon 14-labelled tracers., Journal of Laboratory and Clinical Medicine 71, 400–411.Google Scholar
Lapre, J. A., de Vries, H. T. & van der Meer, R. (1993) Cytotoxicity of fecal water is dependent on the type of dietary fat and is reduced by supplemental calcium phosphate in rats. Journal of Nutrition 123, 578–585.CrossRefGoogle ScholarPubMed
Maczulak, A. E., Dehority, B. A. & Palmquist, D. L. (1981) Effects of long chain fatty acids on growth of rumen bacteria. Applied and Environmental Mirobiology 42, 856–862.CrossRefGoogle ScholarPubMed
Metz, G., Gassull, M. A., Leeds, A. R., Blendis, L. M. & Jenkins, D. J. A. (1976) A simple method of measuring breath hydrogen in carbohydrate malabsorption by end-expiratory sampling. Clinical Science and Molecular edicine 50, 237–240.CrossRefGoogle ScholarPubMed
Miller, T. L. & Wolin, M. J. (1979) Fermentations by saccharolytic intestinal bacteria. American Journal of Clinical Nutrition 32, 164–172.CrossRefGoogle ScholarPubMed
Nelson, G. J. & Ackman, R. G. (1988) Absorption and transport of fat in mammals with emphasis on n-3 polyunsaturated fatty acids. Lipids 23, 1005–1014.CrossRefGoogle ScholarPubMed
Nicholson, M. L., Neoptolemos, J. P., Clayton, H. A. & Heggarty, A. M. (1988) Diet and colorectal cancer. International Clinical Nutrition Reviews 8, 180–197.Google Scholar
Noble, R. C, Moore, J. H. & Harfoot, C. G. (1974) Observations on the pattern on biohydrogenation of esterified and unesterified linoleic acid in the rumen. British Journal of Nutrition 31, 99–108.CrossRefGoogle ScholarPubMed
Oliver, M. F. (1989) Cigarette smoking, polyunsaturated fats, linoleic acid, and coronary heart disease. Lancet 1, 1241–1242.CrossRefGoogle ScholarPubMed
Rao, S. S. C, Edwards, C. A., Austen, C. J., Bruce, C. & Read, N. W. (1988) Impaired colonic fermentation of carbohydrate after ampicillin. Gastroenterology 94, 928–932.CrossRefGoogle ScholarPubMed
Reddy, B. S. & Sugie, S. (1988) Effect of different levels of omega-3 and omega-6 fatty acids on azoxymethane-induced colon carcinogenesis in F344 rats. Cancer Research 48, 6642–6647.Google ScholarPubMed
Rooney, P. S. (1994) Measurement, significance and dietary manipulation of rectal mucosal proliferation in individuals at increased risk of colorectal cancer. DM Thesis, University of Nottingham.CrossRefGoogle Scholar
Siegel, S. & Castellan, N. J. (1988) Nonparametrie Statistics, 2nd ed. New York: McGraw-Hill Book Company.Google Scholar
Spiller, R. C, Brown, M. L. & Phillips, S. F. (1986) Decreased fluid tolerance, accelerated transit and abnormal motility of the human colon induced by oleic acid. Gastroenterology 91, 100–107.CrossRefGoogle ScholarPubMed
Strocchi, A., Furne, J. K., Ellis, C. J. & Levitt, M. D. (1991) Competition for hydrogen by human faecal bacteria: evidence for the predominance of methane producing bacteria. Gut 32, 1498–1501.CrossRefGoogle ScholarPubMed
Thompson, L., Cockayne, A. & Spiller, R. C. (1992). Inhibitory effect of ω-3 linolenic acid on the growth of Helicobacter pylori. Irish Journal of Medical Science 161, Suppl. 10, 30.Google Scholar
Thompson, L., Edwards, R. E., Greenwood, D. & Spiller, R. C. (1990) Inhibitory effect of long chain fatty acids (LCFAs) on colonic bacteria. Gut 32A, 1167.Google Scholar
Treon, S. P., Fox, E. S. & Broitman, S. A. (1989) Marine oils in the modulation of colonic flora and pH: considerations for colon cancer. Microbiological Ecology in Health and Disease 2, 115–122.CrossRefGoogle Scholar
Ulbricht, T. L. V. & Southgate, D. A. T. (1991) Coronary heart disease: seven dietary factors. Lancet 338, 985–991.CrossRefGoogle ScholarPubMed
Wood, D. A., Reimersma, R. A., Butler, S., Thomson, M., Macintyre, C, Elton, R. A. & Oliver, M. F. (1987) Linoleic and eicosapentaenoic acids in adipose tissue and platelets and risk of coronary heart disease. Lancet 1, 177–182.CrossRefGoogle ScholarPubMed