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Basics in clinical nutrition: Fibre and short chain fatty acids
e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism 4 (2009) e69–e71
Contents lists available at ScienceDirect
e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism journal homepage: http://intl.elsevierhealth.com/journals/espen
Educational Paper
Basics in clinical nutrition: Fibre and short chain fatty acids Remy F. Meier University Hospital, Liestal, Switzerland
a r t i c l e i n f o Article history: Received 1 July 2008 Accepted 7 July 2008 Keywords: fibre short chain fatty acids
1. Learning objectives – To identify the different physiological and chemical properties of fibre. – To explain the different effects of fibre in the gastrointestinal tract. – To identify the role of short chain fatty acids in the gastrointestinal tract.
2. Introduction Dietary fibre may be classified into polysaccharides, lignin and oligosaccharides [e.g. inulin, fructans (FOS), galactans (GOS)], which are not digested by the enzymes of the small intestine and are primarily associated with plant cell walls or plant cells. These plant components have also been defined functionally as structural polysaccharides, structural non-polysaccharides and non-structural polysaccharides (Table 1). Fibre is necessary to maintain the normal functioning of the gastrointestinal tract (Table 2). Sources of fibre vary considerably in chemical structure, in physiological properties and the composition of the fibre-containing matrix in foods. The response within the gastrointestinal tract is dependent on the physiological and chemical properties of the fibre and on the location within the gut. The physiological properties of fibres such as water holding capacity, solubility, viscosity, binding or absorption properties and fermentability may influence these physiological responses by affecting the process of digestion and absorption. Other
E-mail address: [email protected] (Editorial Office).
physiological responses associated with dietary fibre include: reduction of plasma cholesterol and triglyceride levels, reduction of the glycaemic response to carbohydrate-containing meals and a decreased nutrient availability. Fibre is not digested or absorbed in the small intestine. The main site of action of fibre is in the colon, where the more soluble fibre is fermented and the less soluble acts as a bulking agent increasing stool output and frequency. Colonic transit time is reduced by an increase in stool water and by the accumulation of undigested material. Some authors suggest that fibre also protects against cancer, reducing exposure of the colonic mucosa to carcinogens by dilution and transit time reduction. This results in a reduction in diminished exposure of the mucosa to toxins and secondary bile acids. Certain types of soluble fibre (e.g. inulin, FOS, GOS) have a prebiotic function with a strong stimulatory effect on the growth of beneficial bifidobacteria and lactobacilli in the gut and, thereby, increase the body’s natural resistance to invading pathogens. Through fermentation in the large intestine, prebiotic carbohydrates yield SCFAs, stimulate the growth of many bacterial species in addition to the selective effects of bifidobacteria and lactobacilli. It was shown that these effects could prevent episodes of diarrhoea. Unfortunately the available data are controversial. The proximal colon acts mainly as a fermentation and absorption chamber whereas the distal colon is a storage organ, but it has also an absorption role. The anaerobic microbial fermentation of fermentable carbohydrates results in production of short chain fatty acids (SCFA), mainly acetate, propionate and butyrate (Table 3) and of gases hydrogen, methane, etc. SCFAs are rapidly absorbed providing up to 5% of total body energy needs and enhancing salt and water absorption. SCFAs are the main mucosal energy source in the colon, stimulating mucosal cell proliferation, mucus production and mucosal blood flow. Besides being the major source of respiratory fuel for colonic mucosal cells, they are the main source of
1751-4991/$ - see front matter Ó 2008 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.eclnm.2008.07.008
e70
R.F. Meier / e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism 4 (2009) e69–e71
Table 1 Classification of dietary fibre. Solubility
Fermentability (%)
Source
Structural polysaccharides Cellulose Hemicellulose A Hemicellulose B
No Good Bad
Structural non-polysaccharides Lignin
No
5
Mature vegetables, wheat, fruits with edible seed
Non-structural polysaccharides Pectins Gums Mucilages
Very good Very good Good
100 100 100
Apples, citrus fruits Oats, legumes, guar, barley Legumes
Oligosaccharides Inulin Fructooligosaccharides (FOS) Galactooligosaccharides (GOS)
Good Good Good
100 100 100
Chicory, onion, artichoke, asparagus, banana
acetyl-coenzyme A for lipid synthesis and cell membrane assembly, necessary for maintaining the integrity of the mucosal cells. Several studies have found that butyrate stimulates crypt proliferation in biopsy samples taken from the normal human caecum. The mechanism by which SCFAs influence cell proliferation is not known. One possible factor may be their effect on mucosal blood flow. Butyrate acts also as a true anti-inflammatory substrate; it inactivates the action of intracellular transcription factors such as NF-kB and hence prevents the synthesis and release of inflammatory mediators (e.g. TNF). In addition butyrate abolishes the lipopolysacharide induced expression of cytokines by peripheral blood mononuclear cells. In summary butyrate is a true dietary factor regulating the inflammatory process from the intestinal lumen. Acetate passes the liver and can be recovered in the peripheral blood. It has been shown that in autoperfused dog colon segments, acetate increases colonic blood flow and oxygen uptake. In addition, SCFA supplemented TPN accelerates mucosal healing in chemically induced colitis and in colonic anastomoses. Trophic effects of SCFAs are also seen in the small bowel where they protect against villous atrophy even when given as part of parenteral nutrition. The integrity of the mucosa can be compromised in shock, sepsis, burn patients and after major surgery. In the first 1–2 days SCFA production is maintained by fermentation of mucin, dead bacteria, sloughed epithelial cells, some glycoproteins and polypeptides. After this initial period, diminished mucosal nutrition can lead to atrophy of the villous architecture, intestinal inflammation and finally to starvation colitis. Rayes et al. examined the ability of
Table 2 Effect of fibre in the gastrointestinal tract. Small bowel Reduction of plasma cholesterol and triglyceride levels Reduced glycaemic response to carbohydrate-containing meals Decreased nutrient availability Decrease of Fe, Ca and Mg resorption Large bowel Reduction in colonic transit time Increase in stool output and frequency Increase in stool water Dilution of colonic content Reduction in availability of toxins, bile acids Increase in colonic fermentation Increase in colonic short chain fatty acids (SCFA) Stimulation of bifidobacteria growth (prebiotic effect) Increase of flatulence
50 70 30
Whole-wheat flour, bran, vegetables Bran, whole grains Bran, whole grains
fibre and the probiotic Lactobacillus plantarum with enteral nutrition to reduce septic complications in 95 patients having liver transplantations. The patients were randomized to a standard formula plus selective bowel decontamination (SBD), fibre-containing formula plus living L. plantarum, or fibre-containing formula plus heat-killed L. plantarum. Receiving living lactobacilli plus fibre reduced bacterial infections significantly (13%) compared to SBD (48%). Diarrhoea is seen as a complication of prolonged starvation and is a common complication of tube-fed patients, especially in the intensive care population. The lack of luminal SCFAs diminishes colonic mucosal integrity. It also allows net colonic and probably ileal secretion of salt and water in response to nasogastric feeding, an effect which is immediately reversed by introduction of SCFAs into the caecum with stimulation of salt and water absorption in the ascending colon. A study in postoperative and critically ill patients, using a diet with partially hydrolyzed guar gum (which is fully fermentable) showed a reduction in the incidence of diarrhoea. These data were recently confirmed in elderly patients fed enterally. A fibre (galactomannas) was added to a semidigested formula. The administration of this soluble fibre significantly decreased the frequency of daily bowel movements and the water content of faeces. As an effect of fermentation, the faecal pH decreased, and the amount of SCFAs in the stools increased 4 weeks after the administration of fibre. 3. Summary Regular fibre intake is essential for the general health and a normal bowel function. Diets containing fermentable fibre as a source of SCFAs play a fundamental role in maintaining gut mucosal function by avoiding epithelial atrophy and possibly bacterial and toxin translocation from the gut lumen into the circulation and also may reduce the incidence of systemic infections and diarrhoea in tube-fed patients.
Table 3 Effects of short chain fatty acids. Main colonic mucosal energy source Stimulation of sodium chloride and water absorption Stimulation of mucosal cell proliferation and differentiation Stimulation of mucosal blood flow Stimulation of mucus production Decrease in colonic pH Maintain mucosal integrity
R.F. Meier / e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism 4 (2009) e69–e71
Conflict of interest There is no conflict of interest. Further reading 1. Cummings JH, Macfarlane GT. Gastrointestinal effects of prebiotics. Br J Nutr 2002;87(Suppl. 2):S145. 2. Homann HH, Kemen M, Fuessenich C, Senkal M, Zumtobel V. Reduction in diarrhoea incidence by soluble fibre in patients receiving total or supplemental enteral nutrition. JPEN 1994;18:486. 3. Kritchevsky D. Dietary fiber. Annu Rev Nutr 1988;8:301.
e71
4. Nakao M, Ogura Y, Satake S, et al. Usefulness of soluble dietary fiber for the treatment of diarrhea during enteral nutrition in elderly patients. Nutrition 2002;18:35. 5. Ramakrishna BS, Roediger WEW. Bacterial short chain fatty acids: their role in gastrointestinal disease. Dig Dis 1990;8:337. 6. Rayes N, Seehofer D, Hansen S, et al. Early enteral supply of lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation 2002;74:123. 7. Ruppin H, Bar-Meir S, Soergel KH, et al. Absorption of short-chain fatty acids by the colon. Gastroenterology 1980;78:1500. 8. Saavedra JM, Tschernia A. Human studies with probiotics and prebiotics: clinical implications. Br J Nutr 2002;87(Suppl. 2):S241. 9. Scheppach W, Bartram P, Richter A, Richter F, Liepold H, Dusel G, et al. Effect of short-chain fatty acids on the human colonic mucosa in vitro. JPEN 1992;16:43.
Contents lists available at ScienceDirect
e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism journal homepage: http://intl.elsevierhealth.com/journals/espen
Educational Paper
Basics in clinical nutrition: Fibre and short chain fatty acids Remy F. Meier University Hospital, Liestal, Switzerland
a r t i c l e i n f o Article history: Received 1 July 2008 Accepted 7 July 2008 Keywords: fibre short chain fatty acids
1. Learning objectives – To identify the different physiological and chemical properties of fibre. – To explain the different effects of fibre in the gastrointestinal tract. – To identify the role of short chain fatty acids in the gastrointestinal tract.
2. Introduction Dietary fibre may be classified into polysaccharides, lignin and oligosaccharides [e.g. inulin, fructans (FOS), galactans (GOS)], which are not digested by the enzymes of the small intestine and are primarily associated with plant cell walls or plant cells. These plant components have also been defined functionally as structural polysaccharides, structural non-polysaccharides and non-structural polysaccharides (Table 1). Fibre is necessary to maintain the normal functioning of the gastrointestinal tract (Table 2). Sources of fibre vary considerably in chemical structure, in physiological properties and the composition of the fibre-containing matrix in foods. The response within the gastrointestinal tract is dependent on the physiological and chemical properties of the fibre and on the location within the gut. The physiological properties of fibres such as water holding capacity, solubility, viscosity, binding or absorption properties and fermentability may influence these physiological responses by affecting the process of digestion and absorption. Other
E-mail address: [email protected] (Editorial Office).
physiological responses associated with dietary fibre include: reduction of plasma cholesterol and triglyceride levels, reduction of the glycaemic response to carbohydrate-containing meals and a decreased nutrient availability. Fibre is not digested or absorbed in the small intestine. The main site of action of fibre is in the colon, where the more soluble fibre is fermented and the less soluble acts as a bulking agent increasing stool output and frequency. Colonic transit time is reduced by an increase in stool water and by the accumulation of undigested material. Some authors suggest that fibre also protects against cancer, reducing exposure of the colonic mucosa to carcinogens by dilution and transit time reduction. This results in a reduction in diminished exposure of the mucosa to toxins and secondary bile acids. Certain types of soluble fibre (e.g. inulin, FOS, GOS) have a prebiotic function with a strong stimulatory effect on the growth of beneficial bifidobacteria and lactobacilli in the gut and, thereby, increase the body’s natural resistance to invading pathogens. Through fermentation in the large intestine, prebiotic carbohydrates yield SCFAs, stimulate the growth of many bacterial species in addition to the selective effects of bifidobacteria and lactobacilli. It was shown that these effects could prevent episodes of diarrhoea. Unfortunately the available data are controversial. The proximal colon acts mainly as a fermentation and absorption chamber whereas the distal colon is a storage organ, but it has also an absorption role. The anaerobic microbial fermentation of fermentable carbohydrates results in production of short chain fatty acids (SCFA), mainly acetate, propionate and butyrate (Table 3) and of gases hydrogen, methane, etc. SCFAs are rapidly absorbed providing up to 5% of total body energy needs and enhancing salt and water absorption. SCFAs are the main mucosal energy source in the colon, stimulating mucosal cell proliferation, mucus production and mucosal blood flow. Besides being the major source of respiratory fuel for colonic mucosal cells, they are the main source of
1751-4991/$ - see front matter Ó 2008 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.eclnm.2008.07.008
e70
R.F. Meier / e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism 4 (2009) e69–e71
Table 1 Classification of dietary fibre. Solubility
Fermentability (%)
Source
Structural polysaccharides Cellulose Hemicellulose A Hemicellulose B
No Good Bad
Structural non-polysaccharides Lignin
No
5
Mature vegetables, wheat, fruits with edible seed
Non-structural polysaccharides Pectins Gums Mucilages
Very good Very good Good
100 100 100
Apples, citrus fruits Oats, legumes, guar, barley Legumes
Oligosaccharides Inulin Fructooligosaccharides (FOS) Galactooligosaccharides (GOS)
Good Good Good
100 100 100
Chicory, onion, artichoke, asparagus, banana
acetyl-coenzyme A for lipid synthesis and cell membrane assembly, necessary for maintaining the integrity of the mucosal cells. Several studies have found that butyrate stimulates crypt proliferation in biopsy samples taken from the normal human caecum. The mechanism by which SCFAs influence cell proliferation is not known. One possible factor may be their effect on mucosal blood flow. Butyrate acts also as a true anti-inflammatory substrate; it inactivates the action of intracellular transcription factors such as NF-kB and hence prevents the synthesis and release of inflammatory mediators (e.g. TNF). In addition butyrate abolishes the lipopolysacharide induced expression of cytokines by peripheral blood mononuclear cells. In summary butyrate is a true dietary factor regulating the inflammatory process from the intestinal lumen. Acetate passes the liver and can be recovered in the peripheral blood. It has been shown that in autoperfused dog colon segments, acetate increases colonic blood flow and oxygen uptake. In addition, SCFA supplemented TPN accelerates mucosal healing in chemically induced colitis and in colonic anastomoses. Trophic effects of SCFAs are also seen in the small bowel where they protect against villous atrophy even when given as part of parenteral nutrition. The integrity of the mucosa can be compromised in shock, sepsis, burn patients and after major surgery. In the first 1–2 days SCFA production is maintained by fermentation of mucin, dead bacteria, sloughed epithelial cells, some glycoproteins and polypeptides. After this initial period, diminished mucosal nutrition can lead to atrophy of the villous architecture, intestinal inflammation and finally to starvation colitis. Rayes et al. examined the ability of
Table 2 Effect of fibre in the gastrointestinal tract. Small bowel Reduction of plasma cholesterol and triglyceride levels Reduced glycaemic response to carbohydrate-containing meals Decreased nutrient availability Decrease of Fe, Ca and Mg resorption Large bowel Reduction in colonic transit time Increase in stool output and frequency Increase in stool water Dilution of colonic content Reduction in availability of toxins, bile acids Increase in colonic fermentation Increase in colonic short chain fatty acids (SCFA) Stimulation of bifidobacteria growth (prebiotic effect) Increase of flatulence
50 70 30
Whole-wheat flour, bran, vegetables Bran, whole grains Bran, whole grains
fibre and the probiotic Lactobacillus plantarum with enteral nutrition to reduce septic complications in 95 patients having liver transplantations. The patients were randomized to a standard formula plus selective bowel decontamination (SBD), fibre-containing formula plus living L. plantarum, or fibre-containing formula plus heat-killed L. plantarum. Receiving living lactobacilli plus fibre reduced bacterial infections significantly (13%) compared to SBD (48%). Diarrhoea is seen as a complication of prolonged starvation and is a common complication of tube-fed patients, especially in the intensive care population. The lack of luminal SCFAs diminishes colonic mucosal integrity. It also allows net colonic and probably ileal secretion of salt and water in response to nasogastric feeding, an effect which is immediately reversed by introduction of SCFAs into the caecum with stimulation of salt and water absorption in the ascending colon. A study in postoperative and critically ill patients, using a diet with partially hydrolyzed guar gum (which is fully fermentable) showed a reduction in the incidence of diarrhoea. These data were recently confirmed in elderly patients fed enterally. A fibre (galactomannas) was added to a semidigested formula. The administration of this soluble fibre significantly decreased the frequency of daily bowel movements and the water content of faeces. As an effect of fermentation, the faecal pH decreased, and the amount of SCFAs in the stools increased 4 weeks after the administration of fibre. 3. Summary Regular fibre intake is essential for the general health and a normal bowel function. Diets containing fermentable fibre as a source of SCFAs play a fundamental role in maintaining gut mucosal function by avoiding epithelial atrophy and possibly bacterial and toxin translocation from the gut lumen into the circulation and also may reduce the incidence of systemic infections and diarrhoea in tube-fed patients.
Table 3 Effects of short chain fatty acids. Main colonic mucosal energy source Stimulation of sodium chloride and water absorption Stimulation of mucosal cell proliferation and differentiation Stimulation of mucosal blood flow Stimulation of mucus production Decrease in colonic pH Maintain mucosal integrity
R.F. Meier / e-SPEN, the European e-Journal of Clinical Nutrition and Metabolism 4 (2009) e69–e71
Conflict of interest There is no conflict of interest. Further reading 1. Cummings JH, Macfarlane GT. Gastrointestinal effects of prebiotics. Br J Nutr 2002;87(Suppl. 2):S145. 2. Homann HH, Kemen M, Fuessenich C, Senkal M, Zumtobel V. Reduction in diarrhoea incidence by soluble fibre in patients receiving total or supplemental enteral nutrition. JPEN 1994;18:486. 3. Kritchevsky D. Dietary fiber. Annu Rev Nutr 1988;8:301.
e71
4. Nakao M, Ogura Y, Satake S, et al. Usefulness of soluble dietary fiber for the treatment of diarrhea during enteral nutrition in elderly patients. Nutrition 2002;18:35. 5. Ramakrishna BS, Roediger WEW. Bacterial short chain fatty acids: their role in gastrointestinal disease. Dig Dis 1990;8:337. 6. Rayes N, Seehofer D, Hansen S, et al. Early enteral supply of lactobacillus and fiber versus selective bowel decontamination: a controlled trial in liver transplant recipients. Transplantation 2002;74:123. 7. Ruppin H, Bar-Meir S, Soergel KH, et al. Absorption of short-chain fatty acids by the colon. Gastroenterology 1980;78:1500. 8. Saavedra JM, Tschernia A. Human studies with probiotics and prebiotics: clinical implications. Br J Nutr 2002;87(Suppl. 2):S241. 9. Scheppach W, Bartram P, Richter A, Richter F, Liepold H, Dusel G, et al. Effect of short-chain fatty acids on the human colonic mucosa in vitro. JPEN 1992;16:43.