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Trends in Food Science & Technology 14 (2003) 507518

Review

Grain legumes a boon to human nutrition


R.N. Tharanathan* and S. Mahadevamma
Department of Biochemistry & Nutrition, Central Food Technological Research Institute, Mysore-570 013, India (tel: +91-821-514876; fax: +91-821-517233; e-mail: tharanathan@ yahoo.co.uk)

Introduction
Legume grains occupy an important place in human nutrition, especially in the pattern of low-income groups of people in developing countries. The term legume is commonly used in India; where it is classied into three categories, namely grains, peas, and beans (Swaminathan, 1974). Legumes are prepared for consumption in many ways, such as whole legumes called grains or dehusked and split legumes, known as dhals. Next to Bengal gram dhal, red gram (pigeon pea, Cajanus cajan), a native of South-east Asia, is the most widely consumed legume, especially in South India, where it is used mainly in the preparation of rasam, sambar and other savory dishes. Several reports claim that inclusion of legumes in the daily diet has many benecial physiological eects in controlling and preventing various metabolic diseases such as diabetes mellitus, coronary heart disease and colon cancer. Currently, the role of legumes as therapeutic agents in the diets of persons suering from metabolic disorders is gaining interest (Shehata, Darwish, Nahr, & Razek, 1988; Simpson et al., 1981). The consensus of recent opinion on healthy eating habits favors an increase in the proportion of legume-based polymeric plant carbohydrates including starch in the diet. Legumes belong to a group that elicits the lowest blood glucose response. Legumes are considered as poor mans meat. They are generally good sources of slow release carbohydrates (viz. dietary bre) and are rich in proteins ( $ 1825%). Soya bean is unique in containing about 3543% proteins. Legumes are the cheapest sources of supplementary proteins in Indian diets (Swaminathan, 1974). They are also good sources of minerals and vitamins. It has been reported that germinated legumes are rich in vitamin C and in some there is an increase in the riboavin as well as niacin contents upon germination (Swaminathan, 1988). The activity of many enzymes such as amylase, protease, phytase and lipase will increase during germination. Processed legumes such as pued Bengal gram contains proteins of fairly high biological value and is a good supplement to the diets of children. There are many varieties of legumes such as red gram (pigeon pea, Cajanus cajan), black gram (Vigna mungo L.), broad bean (Vicia faba L.), Bengal gram (chickpea, Cicer arietinum L.), cowpea (Vigna unguiculata L.), eld bean

Grain legumes occupy an important place in human nutrition, especially in the dietary pattern of low-income groups of people in developing countries. Legumes, considered as poor mans meat, are generally good sources of slow release carbohydrates and are rich in proteins. Legumes are normally consumed after processing, which not only improves palatability of foods but also increases the bioavailability of nutrients, by inactivating trypsin and growth inhibitors and haemagglutinins. Starch, the major biopolymeric constituent of legumes, upon processing gets partially modied into resistant starch (RS). The latter, a man made functional dietary bre, is a unique ingredient that can yield high quality foods, in addition to its signicance on faecal bulk and butyrate production, which are the putative markers of colonic health of humans. The slow and reduced digestibility of legume starch has been attributed to its amylose, which is considerably branched and is of high molecular weight. Dietary bre, which is a heterogeneous mixture of several types of polysaccharides, is rich in legumes, especially in their husk fractions and contributes to benecial therapeutic health eects. # 2003 Elsevier Ltd. All rights reserved.

* Corresponding author.
0924-2244/$ - see front matter # 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tifs.2003.07.002

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(Dolichos lablab), green gram (Phaseolus aureus Roxb), horse gram (Dolichos biorus), etc. which are commonly used in India, especially by the weaker section of the population.

Processing of legumes
Legumes are common components of diets all over the world. They are used in a variety of food preparations either as such or in combination with cereals, because cereal proteins are generally decient in some essential amino acids. The use of legumes assumes signicance as a cheap and concentrated source of proteins, due to the high cost of proteins of animal origin and their inaccessibility by the poorer section of the population. Legumes are generally consumed after processing into various products like milling into dhal, pung or roasting into snack foods, grinding into our for dierent food preparations (Kurien, 1981), or as germinated grains. Many of the legumes contain toxic factors such as protease inhibitors, haemagglutinins and growth inhibitors, which are either partially or completely eliminated by dierent methods of processing, e.g., autoclaving. Heat processing in general, improves the nutritive value of legume proteins, by inactivating trypsin and growth inhibitors and haemagglutinins (Swaminathan, 1974). Traditional methods of processing and cooking legumes have been evolved to give acceptable, appetizing and nutritious products. Processing of legumes increases the digestibility and enhances the aroma, sensory qualities and nutritional attributes. Processing not only improves palatability of foods but also increases the bioavailability of nutrients. Dehulling of legume seeds (into dhal) and splitting the cotyledons are often carried out for better product prole and acceptability. Dehulling reduces cooking time and it shows a negligible eect on the total protein content and amino acid composition. Dehulling also removes tannins that lower protein digestibility (Bressani & Elfas, 1980). Soaking is a preliminary step common to almost all methods of preparing legumes, prior to cooking. Soaking helps in the removal of seed coat to shorten the cooking time. The process of germination is an ancient and popular practice in many parts of the world, particularly in Asia. Germinated legumes are often added to diets to increase their acceptability and nutrient contents. Germination involves the breakdown of seed reserves owing to increased enzyme activity. Upon germination, the content of vitamins also increases considerably (Vijayaraghavan, 1981). Heat treatment of all kinds inactivates antinutritional enzymes and improves avor and overall acceptability of the foods prepared. Roasting, parching, toasting and frying are some of the dry heat processing methods used

for whole legume seeds, which are eaten as snack foods, e.g., fried ground nuts, roasted chickpeas, etc. Fried dhals are quite common in India, especially in South India. Bengal gram dhal and green gram dhal are deep-fat-fried and with addition of spice+salt mixture, are used as snack items. Fried bean cakes made from fried ground legume paste are widely consumed throughout the world.

Starch
Starch, the major biopolymeric constituent of plants, viz., grains, seeds and tubers, occurs in characteristic granular forms of various shapes and sizes (Tharanathan, 1995). Starch provides the major source of physiological energy in human diet and accordingly it is classied, in general, as available carbohydrate. Starch is also functionally a very important polysaccharide that has attracted the attention of nutritionists and food technologists in particular. Starch has many applications both in food and non-food industries. Apart from its energy contribution, the other important role of starch in most of the processed food systems is to contribute to the texture and as a result, to the organoleptic properties of food. Chemically, starch is composed of two main components, namely amylose (Am) and amylopectin (Ap) and a minor third component known as the intermediate fraction, which is neither Am nor Ap in its primary structure. The properties of these components depend upon the type of starch, its maturity, agro-climatic conditions and the type of cultivars. The characteristics of Am and Ap, mainly their molecular weight (MW), degree of polymerization (DP) and linearity or otherwise aect their capacity to bind iodine and attack by enzymes. Ap is a highly branched molecule consisting of a main chain of (1-4)-linked a-d -glucose with short chains of (1-6)-a-d -glucose-linked branches (Fig. 1). Recent studies suggest that small number of branches do exist in Am molecule (Kennedy, Griths, & Atkins, 1983; Madhusudhan & Tharanathan, 1996). Molecular weight of Am varies between 70 000 and 200 000 Da, whereas that of Ap has a value > 2107 Da, which makes Ap as one of the largest naturally occurring macromolecules (Kennedy et al., 1983). The ratio of Ap to Am varies with the source and cultivars and it is typically 20:80, respectively (Orford, Stephen, Carroll, Miles, & Morris, 1987). The overall architecture of starch depends on the nature of the constituent macromolecules, their association by inter- and intra-molecular hydrogen bonding, and the presence/inuence of other non-carbohydrate components. It is inferred that Am and Ap are distributed throughout the granules and that their degree of mutual association is responsible for the structural heterogeneities (Sivak & Preiss, 1998). When these bonds are strong, numerous and regular, the chains

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Fig. 1. The a-(1,4) and a-(1,6) linkages between the glucosyl units present in Ap (and Am) of starch.

associate as crystalline network, in contrast to the amorphous region, whose associated bond forces are fairly weaker. In Ap, the presence of occasional 1,6bonds is responsible for the alternative amorphous and crystalline zones. Starch is degraded by a variety of enzymes such as aand b-amylases, glucoamylase, pullulanase, etc. to oligodextrins and glucose. The action pattern of starch degrading enzymes is shown in Fig. 2 (Mathewson, 1998). Biotechnologically, starch degradation is an important area of high commercial value in the production of glucose, fructose enriched corn syrups, a multitude of derivatives and chemicals for innumerable applications (Tharanathan, 2002). The digestibility pat-

tern of starch in relation to its physical form and processing is shown in Fig. 3 (Cummings & Englyst, 1995).

Starch digestibility
Food particle size can aect starch digestion by amylases as a result of surface area because smaller particles with larger surface area relative to the volume are digested more rapidly than larger ones (Liljeberg, Granfeldt, & Bjorck, 1992). Examination of starch granules of dierent sizes from cassava and corn has suggested that the smaller the granules (probably with a higher Am content), the greater is the extent of in vitro digestion by dierent amylases (Franco & Ciacco, 1992). Higher levels of Am in starch granules per se do

Fig. 2. Action pattern of starch-degrading enzymes.

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Fig. 3. Digestibility pattern of starch in relation to its physical form and processing.

not appear to aect digestibility (Fujita, Glover, Okuno, & Fuwa, 1989). Starches in processed foods may be either essentially unchanged or partially or wholly gelatinized or partially retrograded. Raw starches are highly resistant to enzymic hydrolysis as compared to gelatinized starches. Gelatinization of starch is shown to enhance the extent of both in vitro and in vivo hydrolysis. Gelatinization is a process wherein starch is heated in the presence of excess water, where it undergoes an orderdisorder phase transition, resulting in irreversible changes like disruption of semi-crystalline structure of starch, as evidenced by a total loss of birefringence, increase in the size of the granules (may not be uniform), increase in the viscosity of starch, etc. (Ring, Gee, Whitham, Orford, & Johnson, 1988). Sometimes, starch granules are surrounded by other plant materials (e.g. cell wall components) that may block access of amylases to the granules (Tovar, Bjork, & Asp, 1992). In some processed foods, protein may encapsulate the starch granules (Tovar, Bjork, & Asp, 1990), which has to be removed before treatment with amylases. Recent ndings indicate that disruption of cell walls is a pre-requisite for ecient starch digestion (Tovar et al., 1990). During some processing conditions, the long a-glucan chains can form inclusion complexes with fatty acids (Holm, Bjork, Ostrowska, Eliasson, & Asp, 1983) that can aect starch digestibility. In vitro susceptibility to porcine a-amylase of amylose lipid complexes is reduced when compared with free amylose (Holm et al., 1983). However, complete digestion of amylose can still be achieved if a-amylase levels are increased. Studies of digestion of the amyloselipid complex in rats showed that although small intestinal breakdown was somewhat retarded, it was nevertheless complete (Holm et al., 1983). During processing of foods, the amylose retrogrades more rapidly than amylopectin, which also aects the digestion of starch. Digestion of starch begins in the mouth, where food is mixed with salivary a-amylase, but the hydrolysis stops in the stomach because of changes in pH and later, it is resumed in the duodenum where pancreatic a-amylase is

secreted. The rate of starch digestion is aected by the physical form of foodits shape, crystallinity of the starch granule, recrystallization and retrogradation characteristics, amyloselipid complexes, native a-amylase inhibitors and also the presence of non-starch polysaccharides (NSP). Recent study by Edwards (1995) has revealed that the digestibility of starch is aected by the associated dietary bre, which causes a decrease in transit time through the small intestine and thereby reduces the time available for starch digestion in the small intestine. Earlier, it was believed that starch was completely digested and absorbed within the small intestine (Englyst, Kingman, & Cummings, 1992), but that was later found incorrect. The factors responsible for the incomplete digestion of starch have been divided into two types.

Intrinsic factors
Starch digestion is slowed down in the small intestine, if the physical form of the food hinders access to pancreatic amylase, especially when the starch granules are being surrounded by other plant materials. If the cell walls are rigid, they inhibit swelling and dispersion of starch as in the case of legumes and also if the granules are very densely packed in food, such as spaghetti. Food particle size also aects starch digestion by amylase. The crystallinity of starch is another factor that aects starch digestibility. The former is of three types, viz., A, B and C based on their characteristic X-ray diraction patterns. The latter dier in their inter-planar spacing and reection intensities. Starch crystallinity is attributed to the ordered arrangements of adjacent double helix Ap branches. Cereal starches are A-type whereas tuber starches tend to show B- and C-types found in legumes, the latter are generally more resistant to digestion.

Extrinsic factors
Eating exposes food to several external inuences that may alter the starch susceptibility to amylases. For example, the extent of chewing determines the physical accessibility of starch contained within rigid structure. Other factors such as transit time, the form of food, the concentration of amylase in the gut, the amount of starch and presence of other food components will also aect the enzymatic hydrolysis of starch. The digestibility of starch can be followed both by in vivo and in vitro studies. In the former, the rate and extent of starch digestion are determined by measurement of breath hydrogen, glycemic index, etc. Recent studies have shown that the dietary starch, unutilized in the (human) small intestine, passes onto the colon where it gets fermented by the microora, producing short chain fatty acids and hydrogen. The latter can be quantitatively measured. Ileostomy and colonoscopy are the methods where puncture of the small and large intestine,

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respectively of animals or human subjects is eected, thus enabling withdrawal of partially digested foods from which the undigested starch content is estimated quantitatively. In the in vitro study, these experiments are conducted in the laboratory with various enzymes under specic conditions such as buer, pH, incubation time and temperature. After hydrolysis, the amount of reducing sugars released or the end products having reducing capacity is taken as an estimate of starch digestion (Tharanathan, Paramahans, & Wankhede, 1980). Usually, a-amylase from Aspergillus niger and amyloglucosidase from a fungal source are used. In vitro digestion of starch has been studied even using the intestinal bacterial ora isolated from animals (rats, pigs) or humans.

Resistant starch
Based on their susceptibility to amylases and consequent digestibility prole, starches have been classied into several types (Table 1, Englyst & Kingman, 1990). The fraction of starch that is not hydrolyzed in the small intestine but later fermented by the colonic microora is designated as resistant starch (RS), in the sense that it resists hydrolysis by the amylolytic enzymes elaborated by the healthy human being (Champ, Martin, Noah, & Gratas, 1999). A minimum chain length of 3040 glucose residues seems to be a requirement for RS formation. Longer Am chains promote whereas the presence of lipids prevents (due to complex formation) RS formation (Eliasson, Finstod, & Ljunger, 1988). The percent Am has been shown to bear a direct correlation with RS yield, the higher the Am content, the higher is the RS formed. In fact, RS is considered as a concept, not as a true structural entity. Its resistance to enzymic hydrolysis is solely attributed to its characteristic features, viz., its Btype crystalline nature or to a strong hydrogen bonded inter-chain association between short (2025 glucose residues) amylose chains. The B-type X-ray pattern of RS is analogous to potato starch and high Am corn starch. The latter has long been known to be resistant to pancreatic amylase digestion (Rudolph, Sueda, & Abbot, 1962). Processed foods consist of mainly RS-3. The non-digestible characteristics of RS may, in part be attributed to strong macromolecular interactions,
Table 1. In vitro nutritional classication of starch Type of starch Rapidly digestible starch Slowly digestible starch Resistant starch 1. Physically inaccessible starch, RS-1 2. Resistant starch granules, RS-2 3. Retrograded starch, RS-3 4. Chemically modied starch, RS-4 Example of occurrence

essentially through extensive hydrogen bonding network, possibly between Am chains and short-branched chains of Ap as well as long chains of Am (Fig. 4, Jeffrey, Kluciner, & Donald, 1999). The length of the exterior chains of Ap limits the length of ApAm double helices that are formed. Such interactions serve as Type 1 junction zones. The possible mode of hydrogen bonding (both intra- and intermolecular) of Am molecules is between the hemiacetal oxygen atom and the adjacent OH-6 of the glucose residue (Fig. 5, Tako & Okinawa, 1996). A little decrease in dynamic modulus upon addition of 4 M urea suggests the involvement of methylene group at C-6 to contribute to the intermolecular association with hydrophobic interaction (through van der Walls forces of attraction, Jerey et al., 1999). The formation of RS upon retrogradation seems to occur also by shrinkage of the Ap molecules leading to the formation of side-by-side intermolecular hydrogen bonding of parallel cluster of chains, as formed in Am molecules. Nevertheless, debranching of Ap has been shown to be eective in generating RS from Ap. In an attempt to construct an in vitro model of RS, amylose gels and lms prepared and stored for 7 days showed high levels of crystallinity (2835%). The ability of the enzyme to diuse into such substrates played a major role in the resistance to hydrolysis. The physical nature and the content of resistant component formed in retrograded Am were dependent up on the processing and storage conditions to which the starchy material was subjected to.

Fig. 4. Possible interactions between short-branched chains of Ap and long chains of Am.

Possible digestion in small intestine Rapid Slow but complete Resistant Resistant Resistant Resistant

Freshly cooked starchy food Most raw cereals Partially milled grains and seeds Raw potato and banana Cooled, cooked potato, bread and corn akes Modication induced

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Fig. 5. Possible mode of intra- and intermolecular hydrogen bonding of Am molecules in aqueous solution. The dotted lines refer to hydrogen bonding.

That the RS is a concept and not a true structural entity is based on the fact that individuals dier in their ability to digest starch, and that there is no absolute structural distinction between RS and digestible starch. In fact, what behaves as RS in one person may not behave as RS in another. Repeated heating and cooling cycles have been shown to increase the content of RS (Mangala, Malleshi, Mahadevamma, & Tharanathan, 1999). By judicious selection of processing conditions the proportion of the material that tests as RS can be altered. There is likely a distribution of enzyme susceptibilities in starch molecule, and processing treatments may be considered to inuence this distribution. RS is not digested in the small intestine (Asp, 1992; Asp & Bjorck, 1992). It enters the large intestine, where it becomes an available substrate for bacterial fermentation (Cummings & Englyst, 1991; Stephen, Haddan, & Phillips, 1983). Microbial fermentation of RS produces several metabolic end-products, viz., short chain fatty acids (SCFA) such as acetic, propionic and butyric acids, carbon dioxide, hydrogen and methane (Cummings & Englyst, 1987; Macfarlene & Cummings, 1991). Some studies indicate that fermentation of RS specically leads to an increase in butyric acid (Phillips et al., 1995; Scheppach, Fabian, Sachs, & Kasper, 1988). These SCFA are of value to human nutrition in recent years. They have many benecial physiological eects of value to colonic health. They are rapidly absorbed by the colonic mucosa and promote water and sodium absorption (Ruppin, Bar-Meir, Sorgel, Wood, & Scmitt, 1989). Their production leads to acidication of the lumen, which in turn, can aect processes including the ionization of SCFA (Gustafsson, 1982; Newman & Lupton, 1980), the balance of bacterial species inhibiting the growth of pathogenic organisms, and enhancing

uid and electrolyte absorption (Macfarlene & Cummings, 1991). RS has drawn broad interest worldwide for both its potential health benets and functional properties. RS, a man-made functional dietary bre, is a unique ingredient that can yield high quality foods. RS has a signicant impact on faecal bulk and butyrate production, the putative markers of colonic health of humans. RS formation takes place depending on several factors like physical structure of starch, food processing conditions such as moisture content, pH and temperature regimen, chewing, intestinal transit time, presence of amylase inhibitors in the food, possible cross linking/ structural modication of starch, proteinstarch/lipid starch interactions, etc. (Cummings, 1981; Englyst et al., 1992). RS is considered to confer benecial eects similar to those of dietary bre (Annison & Topping, 1994, Bjorck, 1996; Rube, 1999). The nature and structure of RS are yet not fully understood, to answer the following questions, e.g., is RS a consequence of starch retrogradation and a simple Am chain association, is RS due to Am helix aggregation, what is the nature and frequency of B-type crystallinity, and can RS be mass produced by all processing methods (extrusion cooking)? The recent consideration is that the new genotypes of corn (Am extender waxy) are shown to be natural sources of RS (Shi & Sieb, 1995). Such being the case, the choice, therefore, is between RS derived from farm vs food industry, and naturally, the solution depends on the functional values and cost compatibilities of RS production on a large scale. Chemically RS is shown to be a linear a 1,4-d glucan in the case of cereals like rice (Mangala et al., 1999), ragi (Mangala & Tharanathan, 1999) and wheat (Mahadevamma & Tharanathan, 2001). It is a low MW fraction essentially derived from retrograded Am. Technically it is possible to increase the content of RS in foods by modifying the processing conditions such as severity of heating and cooling, water content, pH, temperature and time and drying. By suitable processing treatments as high as 40% of RS can be obtained. The benecial functional values of RS are exemplied in many trade and technical publications for use in fat substitution, DF applications, low calorie bulking agent, and slow release carbohydrate for diabetic. The industrial application of RS is mainly in the preparation of moisture-free food products (Yue & Waring, 1998). Bakery products are commonly prepared from cereals, which are rich in bre components. A few bakery products such as bread, muns and breakfast cereals can be prepared using RS as a source of bre (Yue & Waring, 1998). It has been mentioned that the granular resistant starches provide better appearance, texture and mouth feel than do the conventional dietary bre, and RS improves expansion and crispness in certain products (Yue and Waring, 1998). It is also reported

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that bread containing RS as the bre source has superior quality compared to those prepared with traditional bre. Being non-digestible, RS can be used in reduced fat and sugar formulations. As a functional bre, RS is white in colour and its ne particles and bland taste make it possible to formulate a variety of food products that have better consumer appeal and greater palatability than those made solely with traditional bre. Thus, RS not only forties bre but also imparts special characteristics not otherwise attainable in high bre foods.

Legume starch digestibility


Generally, among the starchy foods, legumes are of particular interest because they contain several ingredients that may inuence the starch digestibility. Legumes have been shown to decrease blood glucose responses compared to other cereal based foods (Jenkins et al., 1982; Tovar, Granfeldt, & Bjorck, 1992b) such as whole meal bread, and are of very vital benet in the diets of diabetes and hyperlipidemia patients. Generally, legumes contain 3040% amylose compared to cereals (Madhusudhan & Tharanathan, 1995a). Cooked legumes are prone to retrograde more quickly, thereby lowering the process of digestion. Processed legumes contain signicant amount of RS-3. The digestibility of legume starch is much lower than that of cereal starch (Madhusudhan & Tharanathan, 1995a, 1995b, 1996). The higher content of amylose in legumes, which probably may lead to a higher RS content, may possibly account for their low digestibility. High amylose cereal starch has been shown to be digested at a signicantly lower rate (Borchers, 1961). Also, legumes contain more of proteins than cereals and protein-starch interaction in legumes may equally contribute to their decreased glycemic responses (Geervani & Theophilus, 1981). Additionally, the presence of high amounts of dietary bre and antinutritional factors such as phytates and amylase inhibitors may greatly inuence the rate and extent of legume starch digestibility. As a consequence of poor starch digestibility, legumes promote slow and moderate post-prandial glucose and insulin responses (Jenkins, Wolever, Taylor, Barker, & Fielden, 1980; Jenkins et al., 1982). Legume carbohydrates, known as slow release carbohydrate because of this property, are considered benecial in the management of diabetes and hyperlipidemia. Legume starches contain about 3040% of amylose and processing of legumes may lead to increase in the net RS content which may have important eects on human physiology (Edwards, 1993). Several reports claim that inclusion of legumes in the daily diet has many benecial eects in preventing various metabolic diseases such as diabetes mellitus, coronary heart disease and various types of cancer (Simpson et al., 1981; Soni, George, & Singh, 1982). Current interest in the role of legumes as therapeutic agents in the diets of persons suering from metabolic disorders is growing (Thorne, Thompson, & Jenkins, 1983). In fact, grain legumes are the major sources of RS and in turn DF. Many studies have been carried out during the last two decades to assess the importance of RS and DF components in foods.

Physiological consequences of RS
The diet rich in RS may have important repercussions on human health with some eects similar to those reported for soluble dietary bre (Annison & Topping, 1994; Muire et al., 1993; Stephen, 1991). For example, RS consumption has been related to reduced postprandial glycemic and insulinemic responses, which may have benecial implications in the management of diabetes (Granfeldt, Liljeberg, Drews, Newman, & Bjorck, 1994). In vitro studies with human faeces have shown that fermentation of RS yields relatively high amounts of butyrate as compared with other non-starch polysaccharides (Cummings & Macfarlene, 1991). Andrieux, Pacheco, Bochet, Gallant, and Szylit (1992) have suggested that the relative proportion of SCFA produced may vary on the nature of RS and also possibly on the type of RS (Berggren, Bjorck, Margaret, & Nyman, 1995). In a study on humans, Reader, Johnson, Hollander, and Franz (1997) reported that consumption of RS-3 resulted in reduced serum glucose and insulin levels in comparison to that by other carbohydrates. The study also showed that RS containing food decreased postprandial blood glucose and might play a role in providing improved metabolic control in type II diabetes. RS in enteral formulations may improve gastrointestinal tract health status due to faecal bulking, potential dilution of toxins and a greater production of SCFA. There is evidence that butyrate may reduce the risk of malignant changes in cells (Whitehead, Young, & Bhathal, 1986), whereas population studies have shown that increase in faecal bulking (Cummings, Bingham, Heaton, & Eastwood, 1992) and lower faecal pH (Malhotra, 1982) are associated with decreased incidence of colon cancer. Birkett, Muir, Phillips, Jones, and ODea (1996) have reported that RS has benecial eects on putative markers of colonic health, including increased faecal bulk, lower faecal pH and increased concentration of SCFA (Cassidy, Bingham, & Cummings, 1994). RS has also been suggested for use in prebiotic composition to promote the growth of such benecial microorganisms as bidobacterium (Brown, 1996). Since RS almost entirely passes through the small intestine, it can behave as a substrate for growth of the prebiotic microorganisms.

Dietary bre
Dietary bre (DF) is generally dened as the macromolecules present in the diet that resist digestion by human endogenous enzymes and is essentially composed

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of plant cell wall components such as polysaccharides and lignin. During the last two decades, DF has played an important role in decreasing the risk of many diseases such as diabetes mellitus, cardiovascular diseases, colon cancer, constipation and diverticulosis. The health benets associated with high bre foods are delayed nutrient absorption, increased faecal bulk, lowering of blood lipids, prevention of colon cancer, barrier to digestion, mobility of intestinal contents, increased faecal transit time and fermentability characteristics. The various benecial physiological eects of DF in relation to functions of small and large intestines are given in Tables 2 and 3, respectively (Barbara, 1999). Dietary bre does not constitute a dened chemical group; instead it represents a combination of chemically heterogeneous substances such as cellulose, hemicelluloses, pectins, gums, mucilages, resistant starch, other polysaccharides and lignin, a non-carbohydrate polymer of phenyl propane residues. DF is classied mainly into two types, viz., insoluble DF and soluble DF. The (water) insoluble DF are cellulose, lignin and some hemicelluloses, whereas soluble DF are natural gel-forming bres like pectins, gums, mucilages and some hemicellulosic fractions. Each one of these exerts specic physiological eects (Stephen, 1995).

bre bread and biscuits. The bre incorporation in such foods may cause undesirable changes in the food, particularly their avor, texture and mouth feel, which have been partially overcome by modifying the polysaccharides by chemical, physical and enzymatic treatments (Thompson, 2000). Wheat bran IDF is shown to increase faecal bulk and therefore dilutes its contents, thereby decreasing interactions between the intestinal mucosa and any carcinogenic metabolite present in the faeces (Thebaudin, Lefebvre, Harrington, & Bourgeois, 1997). Also, IDF reduces intestinal transit time, thus reducing contact time for faecal mutagens to interact with the intestinal epithelium. As fermentative substrates, IDF modies the activity of digestive microora and leads to modication or reduction in the production of mutagens. Some bres can adsorb mutagenic agents and are eliminated in the faeces. In spite of all these data, the evidence for a protective carcinogenic eect per se of DF is still inconclusive.

Soluble dietary bre (SDF)


Soluble DF develops signicant viscosity upon dissolution in water, which is benecial during its passage through intestine. High viscosity of SDF can inuence absorption by delaying gastric emptying, impairing mixing in the upper small intestine, changing the absorption site and delaying small bowel transit time. These, in turn, help in modifying post-prandial glucose and lipid levels. SDF can protect against colon cancer through microbial fermentation in the large intestine and alleviate colon carcinogenesis. SDFs are having the potential to lower the levels of total cholesterol and LDL in the serum. Absorption of

Insoluble dietary bre (IDF)


These primarily come from plant cell walls (mature and immature), which consist of a heterogeneous mixture of cellulose and non-cellulosic components to form a complex matrix. A variety of DF fractions are available commercially as supplements for use in dietetic and other functional foods such as bakery products, viz., high

Table 2. DF and small intestinal functionsa Characteristics Dispersibility in water Bulk Viscosity Adsorptionbinding
a

Eects Increases volume, dilution of metabolites formed Increases bulk, alters mixing of contents Slows gastric emptying Increases bile acid excretion

Physiological implications Slower digestion, promotes nutrient absorption with reduction of plasma cholesterol Alters transit time Alters mixing and diusion Reduction in plasma cholesterol

Taken from Barbara (1999).

Table 3. DF and large intestinal functionsa Characteristics Dispersibility in water Bulk Adsorptionbinding Fermentability
a

Eects Provides an aqueous phase for penetration of microbes Increases bulk/volume Increases bile acid concentration Growth of microora, microbial adaptation to polysaccharide structures

Physiological implications Increased polysaccharide breakdown by microora Aids laxation Bile acid excretion increased Increased microbial mass and products of metabolism

Taken from Barbara (1999).

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bile salts by SDF results in changes in cholesterol metabolism, viz., loss of cholesterol, unavailability of bile salts in the intestine for micelle formation, which inhibits lipid and cholesterol absorption, increased faecal bulk dilutes bile acids in the lower intestinal tract, and SCFA produced, especially the propionate has been proposed to inhibit hepatic cholesterol synthesis (Scheppach et al., 1988). In addition to lowering of colonic pH and prevention of diarrhea, the liberated SCFA, especially the propionate and butyrate exhibit specic benets pertaining to many health claims. Propionate enhances colonic muscular contraction in vitro (Yajima, 1985) and also promotes large bowel blood ow through relaxation of the vasculature; whereas butyrate is important for the maintenance of colonic health. Butyrate is considered as the major metabolic fuel for normal colonocytes, its infusion relieves ulcerative colitis (Scheppach et al., 1992), it assists in maintenance of a normal cell phenotype through mechanisms involving repair of damaged DNA and suppression of the growth of transformed cells (Kruh, Defer, & Tichonky, 1994). DF is incorporated into processed foods both for its nutritional (colonic fermentation and adsorption of toxic carcinogenic metabolites) and functional (gelling, thickening) properties. The latter is of food technological value, which is of interest to food manufacturer, in a way that agricultural by-products (husks, bran, etc.) can be suitably processed as food ingredients. Currently, wide ranges of bre-enriched foods (bakery products, snacks, beverages, cereals, etc.) are available in the market to choose from. DF aects mineral bioavailability, especially high bre diet, rich in acidic groups chelates minerals such as Ca, Zn, Fe, etc. Nevertheless, the contribution of phytate in such chelation cannot be discounted. Hydration properties such as water-holding capacity, swelling and solubility of DF are important to determine their optimum usage values in foods. The presence of charged, dissociated uronic acid, sulphate, or phytate groups tends to favor solubilization because of their electric charge, which is dependent on the pH and temperature. Of late, increased intakes of complex carbohydrates and dietary bre have been recommended in the western countries, because their diets are essentially based on rened our, which lacks DF. Diverticular disease is one of the most common disorders of the colon among the elderly in western societies. Diverticular disease is mainly due to lack of DF in the diet (Painter & Birekette, 1975). Adequate amount of bre in the diet, that too insoluble DF may decrease the risk of diverticular disease. Increase in DF and high amylose starch has been shown to decrease blood lipids (Anderson & Akanji, 1993; Behall & Howe, 1993). Dietary high amylose corn-starch, when compared with low amylose corn starch, lowered the blood cholesterol concentration in rats by 3036% (Sacquet, Leprince, & Riottot, 1983)

and altered glycemic responses (Brand, Colagiuri, Crossman, Allen, & Truswell, 1991) and metabolic changes in people prone to atherosclerosis and onset of diabetes. Not only dietary bre escapes digestion but dietary protein may also reach the colon undigested in a western diet containing protein up to 12 g/day (Gibson, Slayden, & Dawson, 1976). The undigested protein that reaches the colon is fermented by microora and produces the end products that include phenol, cresol, indoles, amines and ammonia (Macfarlene & Cummings, 1991). Many of these end products have adverse eects. Ammonia may promote tumorigenesis by stimulating cell proliferation (Lin & Visck, 1991), which favors the growth of malignant cells (Visck, 1978). Phenols, the byproducts of the metabolism of aromatic amino acids are known to promote skin cancer and also have been implicated in bladder and bowel cancer (Bingham, 1988). These harmful by-products of protein metabolism may be neutralized by the fermentation of undigested carbohydrates. In vivo studies (Vince, Mencil, Wager, & Wrong, 1990) both in animals and humans showed that the presence of fermentable carbohydrates lowered faecal ammonia concentration. A high bre diet was also shown to lower urinary phenol and cresol concentrations in humans (Cummings et al., 1979). It has been suggested that the presence of undigested carbohydrates stimulates rapid growth of colonic bacteria, which can act as nitrogen sinks for using remaining protein and protein metabolites for their metabolism and growth (Cummings et al., 1979).

Future strategy
Good health undoubtedly is a universal concern and the desire of every human being. Diet is the only one component of an overall life style that can have an impact on health and well-being. A large body of evidence from epidemiological, in vitro and in vivo as well as clinical trial data indicates that a plant-based diet, which is rich in DF and a variety of phytochemicals, can reduce the risk of chronic diseases, particularly cancer. At a molecular level, convincing scientic explanation for such physiological role of DF is not yet available, and is urgently called for. There is a popular belief that legume-based foods, in particular are less digestible and their consumption leads to atulence and other physiological discomforts (Jaya, Naik, & Venkataraman, 1979). It is known that the digestibility, both in vivo and in vitro of legume starch is lower than that of cereal starches, whether in native or cooked form (Madhusudhan & Tharanathan, 1995a, 1995b). It is also known that the formation of RS is at least partially dependent on the content of amylose in the starch. It is not known whether legume starches, being rich in amylose would lead to a higher RS content upon processing. Also, it is not known

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R.N. Tharanathan, S. Mahadevamma / Trends in Food Science & Technology 14 (2003) 507518 Brand, J. C., Colagiuri, S., Crossman, S., Allen, A., & Truswell, A. S. (1991). Low glycemic index carbohydrate foods improve glucose control in non-insulin dependent diabetes mellitus (NIDDM). Diabetes Care, 14, 95101. Bressani, R., & Elfas, L. G. (1980). Nutritional values of legume crops for humans and animals. In R. J. Summereld, & A. H. Bunting (Eds.), Advances in legume science (pp. 5766). London: FAO. Brown, I. (1996). Complex carbohydrates and resistant starch. Nutr. Rev., 54, 51155119. Cassidy, A., Bingham, S. A., & Cummings, J. H. (1994). Starch intake and colorectal cancer riskan international comparison. Br. J. Cancer, 69, 937942. Champ, M., Martin, L., Noah, L., & Gratas, M. In S. S. Cho, L. Prosky, & M. Drcher (Eds.), In Complex carbohydrates in foods (pp. 169 187). New York: Marcel Dekker. Cummings, J. H. (1981). Short chain fatty acids in the human colon. Gut, 22, 763779. Cummings, J. H., & Englyst, H. N. (1987). Fermentation in the human large intestine and the available substrates. Am. J. Clin. Nutr., 45, 12431255. Cummings, J. H., & Englyst, H. N. (1991). Measurement of starch fermentation in the human large intestine. Can. J. Physiol. Pharmacol., 69, 121129. Cummings, J. H., & Englyst, H. N. (1995). Gastrointestinal eects of food carbohydrates, Am. J. Clin. Nutr., 61, 938 S-945S. Cummings, J. H., & Macfarlene, G. T. (1991). The control and consequences of bacterial fermentation in the human colon. J. Appl. Bacteriol., 70, 443459. Cummings, J. H., Bingham, S., Heaton, K. W., & Eastwood, M. A. (1992). Faecal weight colon cancer risk, and dietary intake of non-starch polysaccharides (dietary bre). Gasteroenterology, 103, 17831789. Cummings, J. H., Hill, M. J., Bone, E. S., & Branch, W. J. (1979). The eect of meat protein and dietary bre on colonic function and metabolism. II. Bacterial metabolites in faeces and urine. Am. J. Clin. Nutr., 32, 20942101. Edwards, C. A. (1993). Interactions between nutrition and intestinal microora. Proc. Nutr. Soc., 52, 375382. Edwards, C.A. (1995). In Kristchevsky, D., & Boneld, C. (Eds.), The physiological eects of dietary bre: dietary bre in health and disease (pp. 5871). St. Paul, MN: Eagan Press. Eliasson, A. C., Finstod, H., & Ljunger, G. (1988). A study of starch lipid interactions for some native and modied maize starches. Staerke, 40, 95100. Englyst, H. N., & Kingman, S. M. (1990). Dietary bre and resistant starch. A nutritional classication of plant polysaccharides. In D. Kristchevsky, C. Boneld, & J. A. Anderson (Eds.), Dietary bre, chemistry, physiology and health eects (pp. 4965). New York: Plenum Press. Englyst, H. N., Kingman, S. M., & Cummings, J. H. (1992). Classication and measurement of nutritionally important starch fractions. Eur. J. Clin. Nutr, 46, 533550. Franco, C. L. M., & Ciacco, D. F. (1992). Factors that aect the enzymatic degradation of natural starch granuleseect of the size of the granules. Staerke, 44, 422426. Fujita, S., Glover, D. V., Okuno, D., & Fuwa, H. (1989). In vitro and in vivo digestion of high amylose type starch granules. Staerke, 41, 221224. Geervani, P., & Theophilus, F. (1981). Studies on digestibility of selected legume carbohydrates and its impact on the pH of the gastrointestinal tract in rats. J. Sci. Food Agric., 32, 7178. Gibson, J. A., Sladen, G. E., & Dawson, A. M. (1976). Protein absorption and ammonia production, the eect of dietary protein and removal of the colon. Br. J. Nutr., 35, 6165. Granfeldt, Y., Liljeberg, H., Drews, A., Newman, R., & Bjorck, I. M. (1994). Glucose and insulin responses to barley products. Inuence of food structure and amylose-amylopectin ratio. Am. J. Clin. Nutr, 59, 10751082.

whether the high protein content of legumes leads to any macromolecular interactions (starchprotein) upon processing, which probably may result in an altered RS levels in processed legumes. Before consumption, the edible raw materials are normally subjected, in the presence or absence of additives, to a very wide variety of processing treatments such as pressure-cooking, deepfat-frying, popping, roasting and extrusion cooking, and all these may aect the starch bioavailability to a considerable extent. Only very scanty information is available on the RS content of processed legumes. Large scale production of RS, having prebiotic and butyrogenic properties, for incorporation into designer foods with specic physiological roles to play is of priority. Processing of legume (and cereal) based foods, which are rich in proteins as well as free and bound barbohydrates, may possibly generate Maillard reaction products, some of them have good antioxidant properties. This is a topic worthy of systematic investigation. Earlier studies from this laboratory have shown the sparcely branched nature of legume amylose fractions with high molecular weights (Madhusudhan & Tharanathan, 1995a, 1995b), which possibly may restrict RS formation upon legume processing. Scientic reasoning, at a molecular level, to all these and many more unknowns is possible only after a detailed experimentation with several grain legumes.

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