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Fiber: Physiological and Functional Effects
FIBER
Contents Physiological and Functional Effects Resistant Starch and Oligosaccharides
Physiological and Functional Effects IT Johnson, Institute of Food Research, Norwich, UK r 2013 Elsevier Ltd. All rights reserved.
Glossary Glycemic Pertaining to sugar or glucose in the blood. Glycemic index A quantitative ranking of the bloodglucose response to a carbohydrate food, compared to a reference food such as pure glucose.
Introduction It has long been recognized that both animal foodstuffs and human foods contain poorly digestible components that do not contribute to nutrition in the classical sense of providing essential substances or metabolic energy. With the development of scientific approaches to animal husbandry in the 19th century, the term ‘crude fiber’ was coined to describe the material that remained after rigorous nonenzymatic hydrolysis of feeds. During the 20th century, various strands of thought concerning the virtues of ‘whole’ foods, derived from plant components that had undergone only minimal processing, began to converge, leading eventually to the dietary fiber hypothesis. Put simply, this states that the nondigestible components of plant cell walls are essential for the maintenance of human health. In the early 1970s the physician and epidemiologist Hugh Trowell recognized that the crude fiber figures available at the time for foods had little physiological significance and were of no practical value in the context of human diets. He was amongst the first to use the term dietary fiber to describe the ‘remnants of plant cell walls resistant to hydrolysis (digestion) by the alimentary enzymes of man.’ This definition was later refined and given the more quantitative form: The sum of lignin and the plant polysaccharides that are not digested by the endogenous secretions of the mammalian digestive tract. This definition paved the way for the development of analytical methods that could be used to define the fiber content of human foods. The use of enzymic hydrolysis to determine the ‘unavailable carbohydrate’ content of foods, originally developed by McCance and Lawrence, was refined by Southgate, and his technique was used for the 4th edition of the UK standard food tables, The Composition of Foods published in
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Prebiotic A fermentable but non-digestible food component favoring the growth of beneficial bacteria in the human microbiota.
1978. Broadly, all techniques for analysis of fiber are based on enzymic removal of the digestible elements in food, followed by either gravimetric analysis (i.e., by weight) of the residue as used in the Association of Analytical Chemists (AOAC) method, which results in the retention of some undigested starch, or chemical analysis using gas–liquid chromatography (‘Englyst’ method), which enables a more precise separation of starch from the structural polysaccharides of the cell wall. In the latter case, the cell wall components are defined as ‘nonstarch polysaccharides’ (NSPs). Whatever analytical approach is used, both ‘dietary fiber’ and nonstarch polysaccharides are shorthand terms for large and complex mixtures of polysaccharides. The components of such mixtures vary widely among foods and they often share few properties other than resistance to digestion in the small intestine. A summary of the main types of plant cell polysaccharides contained in the general definition of dietary fiber is given in Table 1.
Table 1
Major components of dietary fiber
Food source
Polysaccharides and related substances
Fruits and vegetables
Cellulose, xyloglucans, arabinogalactans, pectic substances, glycoproteins Cellulose, arabinoxylans, glucoarabinoxylans, b-D-glucans, lignin, and phenolic esters Cellulose, xyloglucans, galactomannans, pectic substances Gums (guar gum, gum arabic), alginates, carrageenan, modified cellulose gums (methyl cellulose, carboxymethyl cellulose)
Cereals Legume seeds Manufactured products
Encyclopedia of Human Nutrition, Volume 2
http://dx.doi.org/10.1016/B978-0-12-375083-9.00105-7
Fiber: Physiological and Functional Effects
In recent years this problem has been made more complex in some ways because of the explosion of interest in functional foods for gastrointestinal health. These often contain high levels of novel oligosaccharides, which are beta-linked saccharide polymers consisting of between three and nine monomers, or larger synthetic or purified carbohydrate polymers that behave as dietary fiber in the gut lumen. Fructose oligosaccharides, which are nondigestible in the small intestine but highly fermentable by the bacteria of the large bowel, are often added to foods as prebiotic substrates to modify the colonic microflora. Such materials may not fit the original definition of dietary fiber, but it is unrealistic in practice to exclude them from the modern concept of fiber. The need to accommodate recent developments is reflected in the 2009 definition of dietary fiber, recommended for international use by the Commission on Nutrition and Foods for Special Dietary Uses, of the Codex Alimentarius Commission, stating that: ‘‘Dietary fiber means carbohydrate polymers with ten or more monomeric units, which are not hydrolyzed by endogenous enzymes in the small intestine of human beings’’. This definition includes a footnote leaving the inclusion of oligosaccharides with between three and nine oligomeric units to the discretion of national governments, and so paves the way for very broad definitions of fiber that embrace commercial prebiotic products. The widely used definition of fiber recommended by the Institute of Medicine of the National Academy of Sciences of the USA, makes a distinction between ‘dietary fiber’, which consists of nondigestible carbohydrates and lignin that are intrinsic and intact in plants, and what is called ‘functional fiber’, consisting of isolated, nondigestible carbohydrate components that have beneficial physiological effects in humans. Oligosaccharides, whether from natural or synthetic sources, are excluded from the first category but are included in the second. Total dietary fiber (TDF) is defined as the sum of Dietary and Functional fiber. In practice, however, no analytical technique can distinguish between dietary fiber and functional fiber when they occur as a mixture in food products. The European Food Safety Authority (EFSA) has recommended a simpler definition of dietary fiber as ‘‘all carbohydrates occurring in foods that are nondigestible in the human small intestine’’. The presence in the lumen of large undigested cell wall fragments, finely dispersed particulates, or soluble polysaccharides can alter physiological processes throughout the gut. The effects of different fiber components depend on their varied physical and chemical properties during digestion, and also on their susceptibility to degradation by bacterial enzymes in the colon. The complex nature of the various substances covered by the general definition of dietary fiber means that a single analytical value for the fiber content of a food is a poor guide to its physiological effects. This article will review the main mechanisms of action of resistant polysaccharides in the alimentary tract and their implications for human health.
Sources and Types of Dietary Fiber The main sources of dietary fiber in most Western diets are well characterized, and high-quality data are available for both food
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Table 2 A Comparison of values for nonstarch polysaccharides and dietary fiber Food source
Nonstarch polysaccharides (Englyst method)
Total dietary fiber (AOAC method)
White bread Brown bread Wholemeal bread Green vegetables Potatoes Fresh fruit Nuts
2.1 3.5 5.0 2.7 1.9 1.4 6.6
2.9 5.0 7.0 3.3 2.4 1.9 8.8
composition and dietary intakes. This is not always true for diets in developing countries, however, and this problem bedevils attempts to investigate the importance of fiber by making international comparisons of diet and disease. Another problem is that different analytical approaches give statistically significant differences for the dietary fiber content of foods. Moreover single analytical values for fiber alone do not reflect the physical and chemical properties of the different polysaccharide components. A comparison of values for NSP, and total TDF values obtained by the AOAC method, is given in Table 2. In the UK approximately 47% of dietary fiber is obtained from cereal products, including bread and breakfast cereals. The level of cell wall polysaccharides in a product made from flour depends on the extraction rate, which is the proportion of the original grain present in the flour after milling. Thus a ‘white’ flour with an extraction rate of 70% usually contains approximately 3% NSP, whereas a ‘wholemeal’ flour with an extraction rate of 100% contains approximately 10% NSP. Although the terms ‘soluble’ and ‘insoluble’ fiber describe the behavior of different classes of nonstarch polysaccharides under experimental conditions in vitro, they do give some insight into the behavior of different components of dietary fiber during digestion, and thus partially overcome the problem of the lack of correspondence between the total analytical value for fiber and the physical properties of the measured polysaccharides. By adopting the Englyst technique for the separation and chemical analysis of nonstarch polysaccharides it is possible to specify both the soluble and insoluble fiber content of foods. Some representative values for soluble and insoluble fiber in cereal foods are given in Table 3, and those for fruits and vegetables, which provide a further 45% of the fiber in UK diets, are given in Table 4.
Fiber in the Digestive Tract The primary function of the alimentary tract is to break down the complex organic macromolecules of which other organisms are composed into smaller molecules, which can then be selectively absorbed into the circulation by specialized mucosal epithelial cells. Food is conveyed progressively through the alimentary tract, stored at intervals, and broken down mechanically as required, by a tightly controlled system of rhythmic muscular contractions. The digestive enzymes are released into the lumen at the appropriate stages to facilitate
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Fiber: Physiological and Functional Effects
Table 3 Soluble and insoluble nonstarch polysaccharides in some cereal products and nuts Food source
Nonstarch polysaccharides (g per 100 g fresh weight)
Sliced white bread Sliced brown bread Wholemeal bread Spaghetti Rye biscuits Cornflakes Crunchy oat cereal Walnuts Hazelnuts Peanuts Brazil nuts
Total NSP
Soluble NSP
Insoluble NSP
1.5 3.6 4.8 1.2 11.7 0.9 6.0 3.5 6.5 6.2 4.3
0.9 1.1 1.6 0.6 3.9 0.4 3.3 1.5 2.5 1.9 1.3
0.6 2.5 3.2 0.6 7.8 0.5 2.7 2.0 4.0 4.3 3.0
Table 4 Soluble and insoluble nonstarch polysaccharides in some vegetables and fruits Food source
Apples (Cox) Oranges Plums Bananas Potatoes Sprouts Peas (frozen) Carrots Courgettes Runner beans Baked beans Tomato Lettuce Onion Celery
Nonstarch polysaccharides (g per 100 g fresh weight)
determinant of food texture, and they exert an indirect effect on the degree of mechanical breakdown of plant foods before swallowing. Hard foods tend to be chewed more thoroughly than soft ones, and hence the presence of dietary fiber in unrefined foods may begin to regulate digestion at a very early stage.
The Stomach The first delay in the transit of food through the digestive tract occurs in the stomach, where large food fragments are further degraded by rigorous muscular activity in the presence of hydrochloric acid and proteolytic enzymes. The need to disrupt and disperse intractable food particles and cell walls appears to delay the digestive process significantly. For example, the absorption of sugar from whole apples is significantly slower than from apple juice. Similarly, the rate at which the starch is digested and absorbed from cubes of cooked potato has been shown to be much slower when they are swallowed whole than when they are chewed normally. Thus, simple mechanical factors can limit the rate at which glucose from carbohydrate foods enters the circulation.
Total NSP
Soluble NSP
Insoluble NSP
The Small Intestine
1.7 2.1 1.8 1.1 1.1 4.8 5.2 2.5 1.2 2.3 3.5 1.1 1.2 1.7 1.3
0.7 1.4 1.2 0.7 0.6 2.5 1.6 1.4 0.6 0.9 2.1 0.4 0.6 0.9 0.6
1.0 0.7 0.6 0.4 0.5 2.3 3.6 1.1 0.6 1.4 1.4 0.7 0.6 0.8 0.7
The small intestine is the main site of nutrient absorption, and it is in fact the largest of the digestive organs in terms of surface area. The semi-liquid products of gastric digestion are released periodically into the duodenum, and then propelled downstream by peristaltic movements, at approximately 1 cm per minute. The hydrolysis of proteins, triglycerides, and starch continues within the duodenum and upper jejunum, under the influence of pancreatic enzymes. The final stages of hydrolysis of dietary macromolecules occur under the influence of extracellular enzymes at the mucosal surface. The released products are absorbed into the circulation, along with water and electrolytes, via the specialized epithelial cells of the intestinal villi. Muscular activity in the small intestinal wall, together with rhythmic contractions of the villi, ensures that the partially digested chyme is well stirred. In adults, the first fermentable residues from a meal containing complex carbohydrates enter the colon approximately 4.5 h after ingestion. When a solution containing indigestible sugar is swallowed without food it reaches the colon approximately 1.5 h earlier than when the same material is added to a solid meal containing dietary fiber. The presence of solid food residues slows transit, probably by delaying gastric emptying and perhaps also by increasing the viscosity of the chyme so that it tends to resist the peristaltic flow. Soluble polysaccharides such as guar gum, pectin, and b-glucan from oats increase mouth to cecum transit time still further. In creating the dietary fiber hypothesis, Trowell’s principal interest was its role in the prevention of metabolic disorders. In particular, he believed that dietary fiber was a major factor in the prevention of diabetes mellitus, which, he argued, was probably unknown in Western Europe before the introduction of mechanized flour milling. In earlier times the nearuniversal consumption of unrefined carbohydrate foods
Source: Data modified from Englyst HN, Bingham SA, Runswick SS, Collinson E, and Cummings JH (1989) Dietary fiber (non-starch polysaccharides) in fruit vegetables and nuts. Journal of Human Nutrition and Dietetics 1: 247–286, with permission from Wiley.
the decomposition of carbohydrates, proteins, and complex lipids. By definition, the polysaccharides that comprise dietary fiber are not digested by endogenous enzymes, though they are often fermented to a greater or lesser degree by bacterial enzymes in the large intestine.
The Mouth and Pharynx The earliest stages of digestion begin in the mouth, where food particles are reduced in size, lubricated with saliva, and prepared for swallowing. The saliva also contains the digestive enzyme salivary amylase, which begins the hydrolysis of starch molecules. Cell wall polysaccharides are an important
Fiber: Physiological and Functional Effects
would have ensured that intact indigestible cell wall polysaccharides were present throughout the upper alimentary tract during digestion. This, according to Trowell and others, favored slow absorption of glucose, which in turn placed less strain on the ability of the pancreas to maintain glucose homeostasis. There is no doubt that Type 2 diabetes has become more common in Western countries as prosperity, and an excess of energy consumption over expenditure, has grown. It is not established that rapid absorption of glucose due to consumption of refined starches is a primary cause of diabetes, but the control of glucose assimilation is certainly a key factor in its management. Cell wall polysaccharides influence the digestion and absorption of carbohydrates in a variety of ways, and are a major determinant of the ‘glycemic index’, which is defined as the incremental area under the blood–glucose response curve after consumption of a standardized sample, expressed as a percentage of the response to an equivalent amount of carbohydrate consumed as glucose. This is essentially a quantitative expression of the rate of change and quantity of glucose appearing in the bloodstream after ingestion of a carbohydrate-rich food. To calculate the index, healthy volunteers are given a test meal of the experimental food containing a standardized quantity of carbohydrate, after an overnight fast. Blood samples are taken at intervals for biochemical analysis, and the change in concentration of glucose in the blood is measured and plotted over a period of time. The ratio of the area under the blood–glucose curve in response to the test meal to that produced by an equal quantity of a standard reference food is then calculated and expressed as a percentage. Individual human subjects do vary significantly in their glycemic response to food, but when glucose is used as the standard, most complex starchy foods have glycemic indices lower than 100%, and this has been shown to be a consistent property of the foods, rather than reflection of human variation. The GI values of foods have been used successfully to design diets for the management of Type 2 diabetes. The physical resistance of plant cell walls during their passage through the gut varies considerably from one food to another. Cell walls that remain intact in the small intestine will impede the access of pancreatic amylase to starch. This is particularly true of the cells of legume seeds, which have been shown to retain much of their integrity during digestion. Legume-based foods such as lentils and chilli beans have glycemic indices that are amongst the lowest of all complex carbohydrate foods. Even when enzymes and their substrates do come into contact, the presence of cell wall polysaccharides may slow the diffusion of hydrolytic products through the partially digested matrix in the gut lumen. These effects of dietary fiber on carbohydrate metabolism emphasize once more that physiological effects cannot be predicted from simple analytical values for total fiber, because they are consequences of cellular structure, rather than the absolute quantity of cell wall polysaccharides within the food. Many studies on postprandial glycemia have been conducted using isolated fiber supplements added to glucose testmeals or to low-fiber sources of starch. They demonstrate that, contrary to Trowell’s original hypothesis, wheat bran and other insoluble cell wall materials have little effect on human glucose metabolism. However, certain soluble
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polysaccharides, such as guar gum, pectin, and oat b-glucan, which form viscous solutions in the stomach and small intestine, do slow the absorption of glucose. Highly viscous food components may delay gastric emptying and inhibit the dispersion of the digesta along the small intestine, but the primary mechanism of action appears to be suppression of convective stirring in the fluid layer adjacent to the mucosal surface. The rapid uptake of monosaccharides by the epithelial cells tends to reduce the concentration of glucose in this boundary layer, so that absorption from the gut lumen becomes rate-limited by the relatively slow process of diffusion. The overall effect is to delay the assimilation of glucose and hence suppress the glycemic response to glucose or starchy foods in both healthy volunteers and in people with diabetes. A similar mechanism probably inhibits the reabsorption of cholesterol and bile salts in the distal ileum and this may account for the ability of some viscous types of soluble dietary fiber such as guar gum and b-glucan to reduce plasma cholesterol levels in humans. In one meta-analysis of randomized, controlled intervention trials it was shown that the soluble polysaccharides most commonly used in human intervention studies all modified plasma cholesterol levels to a similar though modest extent, which, in the case of oat b-glucans, amounted to a reduction of approximately 0.13 mmol l 1 (5.0 mg dl 1) cholesterol for every 3 g of soluble fiber consumed per day. The glycemic response to carbohydrate ingestion is the major determinant of insulin secretion, and glucose uptake also regulates the release of glucagon-like peptide 1 (GLP-1) and gastric inhibitory peptide (GIP), which are known as incretins. These are hormones that act to amplify the release of insulin by the pancreatic beta cell and to reduce secretion of glucagon by pancreatic alpha cells. The presence of dietary fiber in foods modulates this system. For example, the addition of viscous oat b-glucan to a test-beverage has been shown to suppress the absorption of glucose and to inhibit the release of insulin, GLP-1 and the peptide hormones cholecystokinin and PYY in humans. The importance of the viscosity of the polysaccharide is shown by the fact that these effects are abolished by hydrolysis of the b-glucan to smaller less viscous polymers. The potential significance of such endocrine effects lies in the regulatory role of PYY and other gut peptides in relation to intestinal motility and to appetite. However more research is needed to clarify their true physiological importance. One of the main reasons for developing analytical methods to distinguish between soluble and insoluble components of dietary fiber is to provide a means of assessing the capacity of fiber-rich foods to influence carbohydrate and lipid metabolism. There is evidence that diets that provide 30–50% of their fiber in the form of soluble polysaccharides lead to lower cholesterol levels and better glycemic control than diets that contain mostly insoluble fiber. Several officially recognized sets of guidelines for patients with obesity, impaired glucose metabolism and its complications (metabolic syndrome) now recommend a high intake of carbohydrate foods that are rich in soluble fiber. Some of the effects of cell wall polysaccharides in the small intestine involve specific chemical interactions with other food components. For example, there has been considerable
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Fiber: Physiological and Functional Effects
interest over a number of years in the possibility that the polysaccharides and complex phenolic components of cell walls contain polar groups that could interact with and bind ionized mineral species in the gastrointestinal contents, thereby reducing their availability for absorption. Intraluminal binding of heavy metals, toxins, and carcinogens might be a valuable protective mechanism, but binding of micronutrients could seriously compromise nutritional status. Interactions of this type can be shown to occur in vitro, and studies with animals and human ileostomists suggest that charged polysaccharides such as pectin can displace cations into the colon under experimental conditions. However, there is little objective evidence that dietary fiber per se has much of an adverse effect on mineral metabolism in humans. Indeed, highly fermentable polysaccharides and fructose oligosaccharides have recently been shown to promote the absorption of calcium and magnesium in both animal and human studies. The mechanism for the effect is not entirely clear, but it is probably a consequence of fermentation acidifying the luminal contents of the colon and enhancing carrier-mediated transport of minerals across the colonic mucosa. In unprocessed legume seeds, oats, and other cereals phytate (myo-inositol hexaphosphate) is often present in close association with cell wall polysaccharides. Unlike the polysaccharides themselves, phytate does exert a potent binding effect on minerals, and has been shown to significantly reduce the availability of magnesium, zinc, and calcium for absorption in humans. Phytate levels in foods can be reduced by the activity of endogenous phytase, by hydrolysis with exogenous enzymes, or by fermentation. Dephytinized products may therefore be of benefit to individuals at risk of suboptimal mineral status. However, there are indications from animal and in vitro studies that phytate is an anticarcinogen that may contribute to the protective effects of complex fiber-rich foods. The overall significance of phytate in the diet therefore requires further assessment in human trials.
The Large Intestine Microorganisms occur throughout the alimentary tract but in healthy individuals their numbers and diversity are maintained within strict limits by the combined effects of intraluminal conditions, rapid transit, and host immunity. The colon and rectum, however, are adapted to facilitate bacterial colonization, and the typical adult human colonic microflora has been estimated to contain approximately 400 different bacterial species. The largest single groups present are Gramnegative anaerobes of the genus Bacteroides, and Gram-positive organisms including bifidobacteria, eubacteria, lactobacilli, and clostridia. A large proportion of the species present cannot be cultured in vitro and are very poorly characterized, although this problem is being solved rapidly by the emergence of new and relatively inexpensive techniques for sequencing bacterial genomes. Most of the bacteria of the human colon utilize carbohydrate as a source of energy, although not all can degrade polysaccharides directly. It has been estimated that somewhere between 20 and 80 g of carbohydrates enter the human colon every day, about half of which is undigested
starch. Approximately 30 g of bacteria are produced for every 100 g of carbohydrate fermented. Apart from dietary fiber, there are three major sources of unabsorbed carbohydrate for the colonic microflora. Perhaps the most important is resistant starch, which can be classified as physically inaccessible starch contained within unprocessed cell walls (RS1), resistant starch granules found in certain raw foods (RS2), retrograded amylose polymers found in foods such as potatoes and legumes that have been cooked and cooled (RS3), and chemically modified starches in manufactured foods (RS4). Nondigestible sugars, sugar alcohols, and oligosaccharides such as fructooligosaccharides and galactooligosaccharides occur only sparingly in most plant foods, but, as mentioned earlier, they are now much more common in human diets because of their use as prebiotics to selectively manipulate the numbers of bifidobacteria and other supposedly beneficial species in the human colon. Endogenous substrates including mucus are also important for the colonic microflora. The beneficial effects of dietary fiber on the alimentary tract were emphasized by another of the founders of the dietary fiber hypothesis, Denis Burkitt, who based his arguments largely on the concept of fecal bulk, developed as a result of field observations in rural Africa, where cancer and other chronic bowel diseases were rare. His hypothesis was that populations consuming the traditional rural diets, rich in vegetables and cereal foods, produced bulkier, more frequent stools than persons eating the refined diets typical of industrialized societies. Chronic constipation was thought to cause straining of abdominal muscles during passage of stool, leading to prolonged high pressures within the colonic lumen and the lower abdomen. This in turn was thought to increase the risk of various diseases of muscular degeneration including varicose veins, hemorrhoids, hiatus hernia, and colonic diverticulas. Colorectal neoplasia was also thought to result from infrequent defecation, because it caused prolonged exposure of the colonic epithelial cells to mutagenic chemicals, which could initiate cancer. Epidemiological evidence continues to support a protective role of fiber against colorectal cancer, but the origins of intestinal neoplasia are now known to be far more complex than Burkitt was able to envisage. Whatever the relationship to disease, it is certainly true that the consumption of dietary fiber is one major determinant of both fecal bulk and the frequency of defecation (bowel habit). However, the magnitude of the effect depends on the type of fiber consumed. Soluble cell wall polysaccharides such as pectin are readily fermented by the microflora, whereas lignified tissues such as wheat bran tend to remain at least partially intact in the feces. Both classes of dietary fiber can contribute to fecal bulk but by different mechanisms. The increment in stool mass caused by wheat bran depends to some extent on particle size, but in healthy Western populations it has been shown that for every 1 g of wheat bran consumed per day, the output of stool is increased by between 3 and 5 g. Other sources of dietary fiber also favor water retention. For example, isphagula, a mucilaginous material derived from Psyllium, is used pharmaceutically as a bulk laxative. Soluble polysaccharides such as guar and oat b-glucan are readily fermented by anaerobic bacteria, but solubility is no guarantee of fermentability, as is illustrated by modified
Fiber: Physiological and Functional Effects
cellulose gums such as methylcellulose, which is highly resistant to degradation in the human gut. Fermentation reduces the mass and water-holding capacity of soluble polysaccharides considerably, but the bacterial cells derived from them do make some contribution to total fecal output. Thus, although all forms of dietary fiber are mild laxatives, the single analytical measurement of total fiber content again provides no simple predictive measure of physiological effect. Although fermentation of fiber tends to reduce its effectiveness as a source of fecal bulk, it has other very important benefits. The absorption and metabolism of the short-chain fatty acids acetate, propionate, and butyrate derived from carbohydrate fermentation provides the route for the recovery of energy from undigested polysaccharides. Butyrate functions as the preferred source of energy for the colonic mucosal cells, whereas propionate and acetate are absorbed and metabolized systemically. Butyrate is of particular interest because of its ability to modify the expression of genes by acting as an inhibitor of histone deacetylase (HDAC) in a variety of cell types, including the epithelial cells of the colon. In in vitro models, butyrate causes differentiation of tumor cells, suppresses cell division, and induces programmed cell death (apoptosis). In principle, these effects might serve to suppress the development of cancer, but the true role of butyrate as a regulator of epithelial integrity in the human colon remains to be established. The other major breakdown products of carbohydrate fermentation are hydrogen, methane, and carbon dioxide, which together comprise flatus gas. Excess gas production can cause distension and pain in some individuals, especially if they attempt to increase their fiber consumption too abruptly. In most cases, however, extreme flatus is probably caused more by fermentation of oligosaccharides such as stachyose and verbascose, which are found principally in legume seeds, rather than the cell wall polysaccharides themselves.
Conclusion Several decades of research have confirmed that cell wall polysaccharides modify physiological mechanisms throughout the alimentary tract. Delayed absorption of glucose and lipids in the small intestine makes an important contribution to metabolic control in Type 2 diabetes, and certain types of hypercholesterolemia, respectively. Any loss of carbohydrates in the colon will lead to increased fermentative activity, and through this pathway, most of the unabsorbed energy will be recovered as short-chain fatty acids. Unfermented cell wall polysaccharides and increased bacterial mass contribute to
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fecal bulk. All these established physiological effects, coupled with the possibility of using oligosaccharides as prebiotics to modify the colonic microflora, have greatly stimulated interest in nondigestible carbohydrates amongst food manufacturers and consumers in the past few years. There is little to suggest that conventional sources of fiber compromise micronutrient metabolism in otherwise healthy individuals, but the possibility of this and other adverse effects needs to be considered, as the use of novel polysaccharides as sources or analogs of dietary fiber, both for conventional products and for functional foods, continues to expand.
See also: Cancer: Epidemiology and Associations Between Diet and Cancer. Carbohydrates: Requirements and Dietary Importance. Diabetes Mellitus: Dietary Management. Dietary Fiber: Physiological Effects and Health Outcomes; Role in Nutritional Management of Disease. Glycemic Index. Colon: Structure, Function, and Disorders
Further Reading Bordonaro M, Lazarova DL, and Sartorelli AC (2008) Butyrate and Wnt signaling: A possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7: 1178–1183. Burkitt DP and Trowell HC (eds.) (1975) Refined Carbohydrate Foods: Some Implications of Dietary Fibre. London: Academic Press. Food and Nutrition Board, Institute of Medicine of the National Academies. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: The National Academies Press. www.nap.edu Johnson IT and Southgate DAT (1994) Dietary Fibre and Related Substances. London: Chapman Hall. Kushi LH, Meyer KA, and Jacobs DR Jr (1999) Cereals legumes and chronic disease risk reduction: Evidence from epidemiologic studies. American Journal of Clinical Nutrition 70: 451S–458S. McCleary BV and Prosky L (2001) Advanced Dietary Fibre Technology. Oxford: Blackwell Science. Rideout TC, Harding SV, Jones PJ, and Fan MZ (2008) Guar gum and similar soluble fibers in the regulation of cholesterol metabolism: current understandings and future research priorities. Vascular Health Risk Management 4: 1023–1033. Scholz-Ahrens KE and Schrezenmeir J (2002) Inulin, oligofructose and mineral metabolism – experimental data and mechanism. British Journal of Nutrition 87(supplement 2): S179–S186. Southgate DAT (1992) Determination of Food Carbohydrates, 2nd edn. London: Elsevier Applied Science Publishers. Weickert MO and Pfeiffer AF (2008) Metabolic effects of dietary fiber consumption and prevention of diabetes. Journal of Nutrition 138: 439–442. World Cancer Research Fund (2007) Food Nutrition, Physical activity and the prevention of cancer: a global perspective. (Cancers of colon and rectum and foods containing dietary fibre, Chapter 7.9) Washington, DC: AICR.
Contents Physiological and Functional Effects Resistant Starch and Oligosaccharides
Physiological and Functional Effects IT Johnson, Institute of Food Research, Norwich, UK r 2013 Elsevier Ltd. All rights reserved.
Glossary Glycemic Pertaining to sugar or glucose in the blood. Glycemic index A quantitative ranking of the bloodglucose response to a carbohydrate food, compared to a reference food such as pure glucose.
Introduction It has long been recognized that both animal foodstuffs and human foods contain poorly digestible components that do not contribute to nutrition in the classical sense of providing essential substances or metabolic energy. With the development of scientific approaches to animal husbandry in the 19th century, the term ‘crude fiber’ was coined to describe the material that remained after rigorous nonenzymatic hydrolysis of feeds. During the 20th century, various strands of thought concerning the virtues of ‘whole’ foods, derived from plant components that had undergone only minimal processing, began to converge, leading eventually to the dietary fiber hypothesis. Put simply, this states that the nondigestible components of plant cell walls are essential for the maintenance of human health. In the early 1970s the physician and epidemiologist Hugh Trowell recognized that the crude fiber figures available at the time for foods had little physiological significance and were of no practical value in the context of human diets. He was amongst the first to use the term dietary fiber to describe the ‘remnants of plant cell walls resistant to hydrolysis (digestion) by the alimentary enzymes of man.’ This definition was later refined and given the more quantitative form: The sum of lignin and the plant polysaccharides that are not digested by the endogenous secretions of the mammalian digestive tract. This definition paved the way for the development of analytical methods that could be used to define the fiber content of human foods. The use of enzymic hydrolysis to determine the ‘unavailable carbohydrate’ content of foods, originally developed by McCance and Lawrence, was refined by Southgate, and his technique was used for the 4th edition of the UK standard food tables, The Composition of Foods published in
240
Prebiotic A fermentable but non-digestible food component favoring the growth of beneficial bacteria in the human microbiota.
1978. Broadly, all techniques for analysis of fiber are based on enzymic removal of the digestible elements in food, followed by either gravimetric analysis (i.e., by weight) of the residue as used in the Association of Analytical Chemists (AOAC) method, which results in the retention of some undigested starch, or chemical analysis using gas–liquid chromatography (‘Englyst’ method), which enables a more precise separation of starch from the structural polysaccharides of the cell wall. In the latter case, the cell wall components are defined as ‘nonstarch polysaccharides’ (NSPs). Whatever analytical approach is used, both ‘dietary fiber’ and nonstarch polysaccharides are shorthand terms for large and complex mixtures of polysaccharides. The components of such mixtures vary widely among foods and they often share few properties other than resistance to digestion in the small intestine. A summary of the main types of plant cell polysaccharides contained in the general definition of dietary fiber is given in Table 1.
Table 1
Major components of dietary fiber
Food source
Polysaccharides and related substances
Fruits and vegetables
Cellulose, xyloglucans, arabinogalactans, pectic substances, glycoproteins Cellulose, arabinoxylans, glucoarabinoxylans, b-D-glucans, lignin, and phenolic esters Cellulose, xyloglucans, galactomannans, pectic substances Gums (guar gum, gum arabic), alginates, carrageenan, modified cellulose gums (methyl cellulose, carboxymethyl cellulose)
Cereals Legume seeds Manufactured products
Encyclopedia of Human Nutrition, Volume 2
http://dx.doi.org/10.1016/B978-0-12-375083-9.00105-7
Fiber: Physiological and Functional Effects
In recent years this problem has been made more complex in some ways because of the explosion of interest in functional foods for gastrointestinal health. These often contain high levels of novel oligosaccharides, which are beta-linked saccharide polymers consisting of between three and nine monomers, or larger synthetic or purified carbohydrate polymers that behave as dietary fiber in the gut lumen. Fructose oligosaccharides, which are nondigestible in the small intestine but highly fermentable by the bacteria of the large bowel, are often added to foods as prebiotic substrates to modify the colonic microflora. Such materials may not fit the original definition of dietary fiber, but it is unrealistic in practice to exclude them from the modern concept of fiber. The need to accommodate recent developments is reflected in the 2009 definition of dietary fiber, recommended for international use by the Commission on Nutrition and Foods for Special Dietary Uses, of the Codex Alimentarius Commission, stating that: ‘‘Dietary fiber means carbohydrate polymers with ten or more monomeric units, which are not hydrolyzed by endogenous enzymes in the small intestine of human beings’’. This definition includes a footnote leaving the inclusion of oligosaccharides with between three and nine oligomeric units to the discretion of national governments, and so paves the way for very broad definitions of fiber that embrace commercial prebiotic products. The widely used definition of fiber recommended by the Institute of Medicine of the National Academy of Sciences of the USA, makes a distinction between ‘dietary fiber’, which consists of nondigestible carbohydrates and lignin that are intrinsic and intact in plants, and what is called ‘functional fiber’, consisting of isolated, nondigestible carbohydrate components that have beneficial physiological effects in humans. Oligosaccharides, whether from natural or synthetic sources, are excluded from the first category but are included in the second. Total dietary fiber (TDF) is defined as the sum of Dietary and Functional fiber. In practice, however, no analytical technique can distinguish between dietary fiber and functional fiber when they occur as a mixture in food products. The European Food Safety Authority (EFSA) has recommended a simpler definition of dietary fiber as ‘‘all carbohydrates occurring in foods that are nondigestible in the human small intestine’’. The presence in the lumen of large undigested cell wall fragments, finely dispersed particulates, or soluble polysaccharides can alter physiological processes throughout the gut. The effects of different fiber components depend on their varied physical and chemical properties during digestion, and also on their susceptibility to degradation by bacterial enzymes in the colon. The complex nature of the various substances covered by the general definition of dietary fiber means that a single analytical value for the fiber content of a food is a poor guide to its physiological effects. This article will review the main mechanisms of action of resistant polysaccharides in the alimentary tract and their implications for human health.
Sources and Types of Dietary Fiber The main sources of dietary fiber in most Western diets are well characterized, and high-quality data are available for both food
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Table 2 A Comparison of values for nonstarch polysaccharides and dietary fiber Food source
Nonstarch polysaccharides (Englyst method)
Total dietary fiber (AOAC method)
White bread Brown bread Wholemeal bread Green vegetables Potatoes Fresh fruit Nuts
2.1 3.5 5.0 2.7 1.9 1.4 6.6
2.9 5.0 7.0 3.3 2.4 1.9 8.8
composition and dietary intakes. This is not always true for diets in developing countries, however, and this problem bedevils attempts to investigate the importance of fiber by making international comparisons of diet and disease. Another problem is that different analytical approaches give statistically significant differences for the dietary fiber content of foods. Moreover single analytical values for fiber alone do not reflect the physical and chemical properties of the different polysaccharide components. A comparison of values for NSP, and total TDF values obtained by the AOAC method, is given in Table 2. In the UK approximately 47% of dietary fiber is obtained from cereal products, including bread and breakfast cereals. The level of cell wall polysaccharides in a product made from flour depends on the extraction rate, which is the proportion of the original grain present in the flour after milling. Thus a ‘white’ flour with an extraction rate of 70% usually contains approximately 3% NSP, whereas a ‘wholemeal’ flour with an extraction rate of 100% contains approximately 10% NSP. Although the terms ‘soluble’ and ‘insoluble’ fiber describe the behavior of different classes of nonstarch polysaccharides under experimental conditions in vitro, they do give some insight into the behavior of different components of dietary fiber during digestion, and thus partially overcome the problem of the lack of correspondence between the total analytical value for fiber and the physical properties of the measured polysaccharides. By adopting the Englyst technique for the separation and chemical analysis of nonstarch polysaccharides it is possible to specify both the soluble and insoluble fiber content of foods. Some representative values for soluble and insoluble fiber in cereal foods are given in Table 3, and those for fruits and vegetables, which provide a further 45% of the fiber in UK diets, are given in Table 4.
Fiber in the Digestive Tract The primary function of the alimentary tract is to break down the complex organic macromolecules of which other organisms are composed into smaller molecules, which can then be selectively absorbed into the circulation by specialized mucosal epithelial cells. Food is conveyed progressively through the alimentary tract, stored at intervals, and broken down mechanically as required, by a tightly controlled system of rhythmic muscular contractions. The digestive enzymes are released into the lumen at the appropriate stages to facilitate
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Fiber: Physiological and Functional Effects
Table 3 Soluble and insoluble nonstarch polysaccharides in some cereal products and nuts Food source
Nonstarch polysaccharides (g per 100 g fresh weight)
Sliced white bread Sliced brown bread Wholemeal bread Spaghetti Rye biscuits Cornflakes Crunchy oat cereal Walnuts Hazelnuts Peanuts Brazil nuts
Total NSP
Soluble NSP
Insoluble NSP
1.5 3.6 4.8 1.2 11.7 0.9 6.0 3.5 6.5 6.2 4.3
0.9 1.1 1.6 0.6 3.9 0.4 3.3 1.5 2.5 1.9 1.3
0.6 2.5 3.2 0.6 7.8 0.5 2.7 2.0 4.0 4.3 3.0
Table 4 Soluble and insoluble nonstarch polysaccharides in some vegetables and fruits Food source
Apples (Cox) Oranges Plums Bananas Potatoes Sprouts Peas (frozen) Carrots Courgettes Runner beans Baked beans Tomato Lettuce Onion Celery
Nonstarch polysaccharides (g per 100 g fresh weight)
determinant of food texture, and they exert an indirect effect on the degree of mechanical breakdown of plant foods before swallowing. Hard foods tend to be chewed more thoroughly than soft ones, and hence the presence of dietary fiber in unrefined foods may begin to regulate digestion at a very early stage.
The Stomach The first delay in the transit of food through the digestive tract occurs in the stomach, where large food fragments are further degraded by rigorous muscular activity in the presence of hydrochloric acid and proteolytic enzymes. The need to disrupt and disperse intractable food particles and cell walls appears to delay the digestive process significantly. For example, the absorption of sugar from whole apples is significantly slower than from apple juice. Similarly, the rate at which the starch is digested and absorbed from cubes of cooked potato has been shown to be much slower when they are swallowed whole than when they are chewed normally. Thus, simple mechanical factors can limit the rate at which glucose from carbohydrate foods enters the circulation.
Total NSP
Soluble NSP
Insoluble NSP
The Small Intestine
1.7 2.1 1.8 1.1 1.1 4.8 5.2 2.5 1.2 2.3 3.5 1.1 1.2 1.7 1.3
0.7 1.4 1.2 0.7 0.6 2.5 1.6 1.4 0.6 0.9 2.1 0.4 0.6 0.9 0.6
1.0 0.7 0.6 0.4 0.5 2.3 3.6 1.1 0.6 1.4 1.4 0.7 0.6 0.8 0.7
The small intestine is the main site of nutrient absorption, and it is in fact the largest of the digestive organs in terms of surface area. The semi-liquid products of gastric digestion are released periodically into the duodenum, and then propelled downstream by peristaltic movements, at approximately 1 cm per minute. The hydrolysis of proteins, triglycerides, and starch continues within the duodenum and upper jejunum, under the influence of pancreatic enzymes. The final stages of hydrolysis of dietary macromolecules occur under the influence of extracellular enzymes at the mucosal surface. The released products are absorbed into the circulation, along with water and electrolytes, via the specialized epithelial cells of the intestinal villi. Muscular activity in the small intestinal wall, together with rhythmic contractions of the villi, ensures that the partially digested chyme is well stirred. In adults, the first fermentable residues from a meal containing complex carbohydrates enter the colon approximately 4.5 h after ingestion. When a solution containing indigestible sugar is swallowed without food it reaches the colon approximately 1.5 h earlier than when the same material is added to a solid meal containing dietary fiber. The presence of solid food residues slows transit, probably by delaying gastric emptying and perhaps also by increasing the viscosity of the chyme so that it tends to resist the peristaltic flow. Soluble polysaccharides such as guar gum, pectin, and b-glucan from oats increase mouth to cecum transit time still further. In creating the dietary fiber hypothesis, Trowell’s principal interest was its role in the prevention of metabolic disorders. In particular, he believed that dietary fiber was a major factor in the prevention of diabetes mellitus, which, he argued, was probably unknown in Western Europe before the introduction of mechanized flour milling. In earlier times the nearuniversal consumption of unrefined carbohydrate foods
Source: Data modified from Englyst HN, Bingham SA, Runswick SS, Collinson E, and Cummings JH (1989) Dietary fiber (non-starch polysaccharides) in fruit vegetables and nuts. Journal of Human Nutrition and Dietetics 1: 247–286, with permission from Wiley.
the decomposition of carbohydrates, proteins, and complex lipids. By definition, the polysaccharides that comprise dietary fiber are not digested by endogenous enzymes, though they are often fermented to a greater or lesser degree by bacterial enzymes in the large intestine.
The Mouth and Pharynx The earliest stages of digestion begin in the mouth, where food particles are reduced in size, lubricated with saliva, and prepared for swallowing. The saliva also contains the digestive enzyme salivary amylase, which begins the hydrolysis of starch molecules. Cell wall polysaccharides are an important
Fiber: Physiological and Functional Effects
would have ensured that intact indigestible cell wall polysaccharides were present throughout the upper alimentary tract during digestion. This, according to Trowell and others, favored slow absorption of glucose, which in turn placed less strain on the ability of the pancreas to maintain glucose homeostasis. There is no doubt that Type 2 diabetes has become more common in Western countries as prosperity, and an excess of energy consumption over expenditure, has grown. It is not established that rapid absorption of glucose due to consumption of refined starches is a primary cause of diabetes, but the control of glucose assimilation is certainly a key factor in its management. Cell wall polysaccharides influence the digestion and absorption of carbohydrates in a variety of ways, and are a major determinant of the ‘glycemic index’, which is defined as the incremental area under the blood–glucose response curve after consumption of a standardized sample, expressed as a percentage of the response to an equivalent amount of carbohydrate consumed as glucose. This is essentially a quantitative expression of the rate of change and quantity of glucose appearing in the bloodstream after ingestion of a carbohydrate-rich food. To calculate the index, healthy volunteers are given a test meal of the experimental food containing a standardized quantity of carbohydrate, after an overnight fast. Blood samples are taken at intervals for biochemical analysis, and the change in concentration of glucose in the blood is measured and plotted over a period of time. The ratio of the area under the blood–glucose curve in response to the test meal to that produced by an equal quantity of a standard reference food is then calculated and expressed as a percentage. Individual human subjects do vary significantly in their glycemic response to food, but when glucose is used as the standard, most complex starchy foods have glycemic indices lower than 100%, and this has been shown to be a consistent property of the foods, rather than reflection of human variation. The GI values of foods have been used successfully to design diets for the management of Type 2 diabetes. The physical resistance of plant cell walls during their passage through the gut varies considerably from one food to another. Cell walls that remain intact in the small intestine will impede the access of pancreatic amylase to starch. This is particularly true of the cells of legume seeds, which have been shown to retain much of their integrity during digestion. Legume-based foods such as lentils and chilli beans have glycemic indices that are amongst the lowest of all complex carbohydrate foods. Even when enzymes and their substrates do come into contact, the presence of cell wall polysaccharides may slow the diffusion of hydrolytic products through the partially digested matrix in the gut lumen. These effects of dietary fiber on carbohydrate metabolism emphasize once more that physiological effects cannot be predicted from simple analytical values for total fiber, because they are consequences of cellular structure, rather than the absolute quantity of cell wall polysaccharides within the food. Many studies on postprandial glycemia have been conducted using isolated fiber supplements added to glucose testmeals or to low-fiber sources of starch. They demonstrate that, contrary to Trowell’s original hypothesis, wheat bran and other insoluble cell wall materials have little effect on human glucose metabolism. However, certain soluble
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polysaccharides, such as guar gum, pectin, and oat b-glucan, which form viscous solutions in the stomach and small intestine, do slow the absorption of glucose. Highly viscous food components may delay gastric emptying and inhibit the dispersion of the digesta along the small intestine, but the primary mechanism of action appears to be suppression of convective stirring in the fluid layer adjacent to the mucosal surface. The rapid uptake of monosaccharides by the epithelial cells tends to reduce the concentration of glucose in this boundary layer, so that absorption from the gut lumen becomes rate-limited by the relatively slow process of diffusion. The overall effect is to delay the assimilation of glucose and hence suppress the glycemic response to glucose or starchy foods in both healthy volunteers and in people with diabetes. A similar mechanism probably inhibits the reabsorption of cholesterol and bile salts in the distal ileum and this may account for the ability of some viscous types of soluble dietary fiber such as guar gum and b-glucan to reduce plasma cholesterol levels in humans. In one meta-analysis of randomized, controlled intervention trials it was shown that the soluble polysaccharides most commonly used in human intervention studies all modified plasma cholesterol levels to a similar though modest extent, which, in the case of oat b-glucans, amounted to a reduction of approximately 0.13 mmol l 1 (5.0 mg dl 1) cholesterol for every 3 g of soluble fiber consumed per day. The glycemic response to carbohydrate ingestion is the major determinant of insulin secretion, and glucose uptake also regulates the release of glucagon-like peptide 1 (GLP-1) and gastric inhibitory peptide (GIP), which are known as incretins. These are hormones that act to amplify the release of insulin by the pancreatic beta cell and to reduce secretion of glucagon by pancreatic alpha cells. The presence of dietary fiber in foods modulates this system. For example, the addition of viscous oat b-glucan to a test-beverage has been shown to suppress the absorption of glucose and to inhibit the release of insulin, GLP-1 and the peptide hormones cholecystokinin and PYY in humans. The importance of the viscosity of the polysaccharide is shown by the fact that these effects are abolished by hydrolysis of the b-glucan to smaller less viscous polymers. The potential significance of such endocrine effects lies in the regulatory role of PYY and other gut peptides in relation to intestinal motility and to appetite. However more research is needed to clarify their true physiological importance. One of the main reasons for developing analytical methods to distinguish between soluble and insoluble components of dietary fiber is to provide a means of assessing the capacity of fiber-rich foods to influence carbohydrate and lipid metabolism. There is evidence that diets that provide 30–50% of their fiber in the form of soluble polysaccharides lead to lower cholesterol levels and better glycemic control than diets that contain mostly insoluble fiber. Several officially recognized sets of guidelines for patients with obesity, impaired glucose metabolism and its complications (metabolic syndrome) now recommend a high intake of carbohydrate foods that are rich in soluble fiber. Some of the effects of cell wall polysaccharides in the small intestine involve specific chemical interactions with other food components. For example, there has been considerable
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Fiber: Physiological and Functional Effects
interest over a number of years in the possibility that the polysaccharides and complex phenolic components of cell walls contain polar groups that could interact with and bind ionized mineral species in the gastrointestinal contents, thereby reducing their availability for absorption. Intraluminal binding of heavy metals, toxins, and carcinogens might be a valuable protective mechanism, but binding of micronutrients could seriously compromise nutritional status. Interactions of this type can be shown to occur in vitro, and studies with animals and human ileostomists suggest that charged polysaccharides such as pectin can displace cations into the colon under experimental conditions. However, there is little objective evidence that dietary fiber per se has much of an adverse effect on mineral metabolism in humans. Indeed, highly fermentable polysaccharides and fructose oligosaccharides have recently been shown to promote the absorption of calcium and magnesium in both animal and human studies. The mechanism for the effect is not entirely clear, but it is probably a consequence of fermentation acidifying the luminal contents of the colon and enhancing carrier-mediated transport of minerals across the colonic mucosa. In unprocessed legume seeds, oats, and other cereals phytate (myo-inositol hexaphosphate) is often present in close association with cell wall polysaccharides. Unlike the polysaccharides themselves, phytate does exert a potent binding effect on minerals, and has been shown to significantly reduce the availability of magnesium, zinc, and calcium for absorption in humans. Phytate levels in foods can be reduced by the activity of endogenous phytase, by hydrolysis with exogenous enzymes, or by fermentation. Dephytinized products may therefore be of benefit to individuals at risk of suboptimal mineral status. However, there are indications from animal and in vitro studies that phytate is an anticarcinogen that may contribute to the protective effects of complex fiber-rich foods. The overall significance of phytate in the diet therefore requires further assessment in human trials.
The Large Intestine Microorganisms occur throughout the alimentary tract but in healthy individuals their numbers and diversity are maintained within strict limits by the combined effects of intraluminal conditions, rapid transit, and host immunity. The colon and rectum, however, are adapted to facilitate bacterial colonization, and the typical adult human colonic microflora has been estimated to contain approximately 400 different bacterial species. The largest single groups present are Gramnegative anaerobes of the genus Bacteroides, and Gram-positive organisms including bifidobacteria, eubacteria, lactobacilli, and clostridia. A large proportion of the species present cannot be cultured in vitro and are very poorly characterized, although this problem is being solved rapidly by the emergence of new and relatively inexpensive techniques for sequencing bacterial genomes. Most of the bacteria of the human colon utilize carbohydrate as a source of energy, although not all can degrade polysaccharides directly. It has been estimated that somewhere between 20 and 80 g of carbohydrates enter the human colon every day, about half of which is undigested
starch. Approximately 30 g of bacteria are produced for every 100 g of carbohydrate fermented. Apart from dietary fiber, there are three major sources of unabsorbed carbohydrate for the colonic microflora. Perhaps the most important is resistant starch, which can be classified as physically inaccessible starch contained within unprocessed cell walls (RS1), resistant starch granules found in certain raw foods (RS2), retrograded amylose polymers found in foods such as potatoes and legumes that have been cooked and cooled (RS3), and chemically modified starches in manufactured foods (RS4). Nondigestible sugars, sugar alcohols, and oligosaccharides such as fructooligosaccharides and galactooligosaccharides occur only sparingly in most plant foods, but, as mentioned earlier, they are now much more common in human diets because of their use as prebiotics to selectively manipulate the numbers of bifidobacteria and other supposedly beneficial species in the human colon. Endogenous substrates including mucus are also important for the colonic microflora. The beneficial effects of dietary fiber on the alimentary tract were emphasized by another of the founders of the dietary fiber hypothesis, Denis Burkitt, who based his arguments largely on the concept of fecal bulk, developed as a result of field observations in rural Africa, where cancer and other chronic bowel diseases were rare. His hypothesis was that populations consuming the traditional rural diets, rich in vegetables and cereal foods, produced bulkier, more frequent stools than persons eating the refined diets typical of industrialized societies. Chronic constipation was thought to cause straining of abdominal muscles during passage of stool, leading to prolonged high pressures within the colonic lumen and the lower abdomen. This in turn was thought to increase the risk of various diseases of muscular degeneration including varicose veins, hemorrhoids, hiatus hernia, and colonic diverticulas. Colorectal neoplasia was also thought to result from infrequent defecation, because it caused prolonged exposure of the colonic epithelial cells to mutagenic chemicals, which could initiate cancer. Epidemiological evidence continues to support a protective role of fiber against colorectal cancer, but the origins of intestinal neoplasia are now known to be far more complex than Burkitt was able to envisage. Whatever the relationship to disease, it is certainly true that the consumption of dietary fiber is one major determinant of both fecal bulk and the frequency of defecation (bowel habit). However, the magnitude of the effect depends on the type of fiber consumed. Soluble cell wall polysaccharides such as pectin are readily fermented by the microflora, whereas lignified tissues such as wheat bran tend to remain at least partially intact in the feces. Both classes of dietary fiber can contribute to fecal bulk but by different mechanisms. The increment in stool mass caused by wheat bran depends to some extent on particle size, but in healthy Western populations it has been shown that for every 1 g of wheat bran consumed per day, the output of stool is increased by between 3 and 5 g. Other sources of dietary fiber also favor water retention. For example, isphagula, a mucilaginous material derived from Psyllium, is used pharmaceutically as a bulk laxative. Soluble polysaccharides such as guar and oat b-glucan are readily fermented by anaerobic bacteria, but solubility is no guarantee of fermentability, as is illustrated by modified
Fiber: Physiological and Functional Effects
cellulose gums such as methylcellulose, which is highly resistant to degradation in the human gut. Fermentation reduces the mass and water-holding capacity of soluble polysaccharides considerably, but the bacterial cells derived from them do make some contribution to total fecal output. Thus, although all forms of dietary fiber are mild laxatives, the single analytical measurement of total fiber content again provides no simple predictive measure of physiological effect. Although fermentation of fiber tends to reduce its effectiveness as a source of fecal bulk, it has other very important benefits. The absorption and metabolism of the short-chain fatty acids acetate, propionate, and butyrate derived from carbohydrate fermentation provides the route for the recovery of energy from undigested polysaccharides. Butyrate functions as the preferred source of energy for the colonic mucosal cells, whereas propionate and acetate are absorbed and metabolized systemically. Butyrate is of particular interest because of its ability to modify the expression of genes by acting as an inhibitor of histone deacetylase (HDAC) in a variety of cell types, including the epithelial cells of the colon. In in vitro models, butyrate causes differentiation of tumor cells, suppresses cell division, and induces programmed cell death (apoptosis). In principle, these effects might serve to suppress the development of cancer, but the true role of butyrate as a regulator of epithelial integrity in the human colon remains to be established. The other major breakdown products of carbohydrate fermentation are hydrogen, methane, and carbon dioxide, which together comprise flatus gas. Excess gas production can cause distension and pain in some individuals, especially if they attempt to increase their fiber consumption too abruptly. In most cases, however, extreme flatus is probably caused more by fermentation of oligosaccharides such as stachyose and verbascose, which are found principally in legume seeds, rather than the cell wall polysaccharides themselves.
Conclusion Several decades of research have confirmed that cell wall polysaccharides modify physiological mechanisms throughout the alimentary tract. Delayed absorption of glucose and lipids in the small intestine makes an important contribution to metabolic control in Type 2 diabetes, and certain types of hypercholesterolemia, respectively. Any loss of carbohydrates in the colon will lead to increased fermentative activity, and through this pathway, most of the unabsorbed energy will be recovered as short-chain fatty acids. Unfermented cell wall polysaccharides and increased bacterial mass contribute to
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fecal bulk. All these established physiological effects, coupled with the possibility of using oligosaccharides as prebiotics to modify the colonic microflora, have greatly stimulated interest in nondigestible carbohydrates amongst food manufacturers and consumers in the past few years. There is little to suggest that conventional sources of fiber compromise micronutrient metabolism in otherwise healthy individuals, but the possibility of this and other adverse effects needs to be considered, as the use of novel polysaccharides as sources or analogs of dietary fiber, both for conventional products and for functional foods, continues to expand.
See also: Cancer: Epidemiology and Associations Between Diet and Cancer. Carbohydrates: Requirements and Dietary Importance. Diabetes Mellitus: Dietary Management. Dietary Fiber: Physiological Effects and Health Outcomes; Role in Nutritional Management of Disease. Glycemic Index. Colon: Structure, Function, and Disorders
Further Reading Bordonaro M, Lazarova DL, and Sartorelli AC (2008) Butyrate and Wnt signaling: A possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7: 1178–1183. Burkitt DP and Trowell HC (eds.) (1975) Refined Carbohydrate Foods: Some Implications of Dietary Fibre. London: Academic Press. Food and Nutrition Board, Institute of Medicine of the National Academies. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: The National Academies Press. www.nap.edu Johnson IT and Southgate DAT (1994) Dietary Fibre and Related Substances. London: Chapman Hall. Kushi LH, Meyer KA, and Jacobs DR Jr (1999) Cereals legumes and chronic disease risk reduction: Evidence from epidemiologic studies. American Journal of Clinical Nutrition 70: 451S–458S. McCleary BV and Prosky L (2001) Advanced Dietary Fibre Technology. Oxford: Blackwell Science. Rideout TC, Harding SV, Jones PJ, and Fan MZ (2008) Guar gum and similar soluble fibers in the regulation of cholesterol metabolism: current understandings and future research priorities. Vascular Health Risk Management 4: 1023–1033. Scholz-Ahrens KE and Schrezenmeir J (2002) Inulin, oligofructose and mineral metabolism – experimental data and mechanism. British Journal of Nutrition 87(supplement 2): S179–S186. Southgate DAT (1992) Determination of Food Carbohydrates, 2nd edn. London: Elsevier Applied Science Publishers. Weickert MO and Pfeiffer AF (2008) Metabolic effects of dietary fiber consumption and prevention of diabetes. Journal of Nutrition 138: 439–442. World Cancer Research Fund (2007) Food Nutrition, Physical activity and the prevention of cancer: a global perspective. (Cancers of colon and rectum and foods containing dietary fibre, Chapter 7.9) Washington, DC: AICR.