Resistant starch in food: a review - Wiley Online Library

Review Received: 14 March 2014

Revised: 16 October 2014

Accepted article published: 21 October 2014

Published online in Wiley Online Library: 21 November 2014

(wileyonlinelibrary.com) DOI 10.1002/jsfa.6966

Resistant starch in food: a review Pinky Raigond,* Rajarathnam Ezekiel and Baswaraj Raigond Abstract The nutritional property of starch is related to its rate and extent of digestion and absorption in the small intestine. For nutritional purposes, starch is classified as rapidly available, slowly available and resistant starch (RS). The exact underlying mechanism of relative resistance of starch granules is complicated because those factors are often interconnected. The content of RS in food is highly influenced by food preparation manner and processing techniques. Physical or chemical treatments also alter the level of RS in a food. Commercial preparations of RS are now available and can be added to foods as an ingredient for lowering the calorific value and improving textural and organoleptic characteristics along with increasing the amount of dietary fiber. RS has assumed great importance owing to its unique functional properties and health benefits. The beneficial effects of RS include glycemic control and control of fasting plasma triglyceride and cholesterol levels and absorption of minerals. This review attempts to analyze the information published, especially in the recent past, on classification, structure, properties, applications and health benefits of RS. © 2014 Society of Chemical Industry Keywords: resistant starch; classification; properties; applications; health benefits

INTRODUCTION Starch is the most abundant storage polysaccharide in plants and is the major component of diet. Digestibility of starch improves during cooking, but not all of the starch present in a food is digestible. A part of starch present in the diet escapes digestion and absorption in the small intestine and is fermented in the large intestine of humans, with the production of short-chain fatty acids (SCFA). This is termed ‘resistant starch’.1 Resistant starch (RS) is a form of dietary fiber and is naturally present in many starchy foods. Digestibility of starch is influenced by many factors such as temperature during cooking and storage and interaction of starch with proteins, lipids and other carbohydrates. Most of the starch is consumed in gelatinized form, which can be readily digested. Reduced digestibility of RS is influenced by many internal and external factors such as behavior and nature of food, botanical origin of starch, food processing and physiology.2 Properties of starch depend on its two major components, amylose and amylopectin, and how these molecules are organized within the granule.3 Generally, food-processing techniques influence the physiological fate and behavior of dietary carbohydrates. The American Association of Cereal Chemists and the Food Nutrition Board of the Institute of Medicine of the National Academies have defined RS as a type of dietary fiber. RS is not rapidly digested like ordinary starch, and this property is of great biological importance. Based on its origin and physical characteristics, RS is further categorized into five different types. Reviews on RS have appeared in the past, but there is continuous accumulation of newer information as RS continues to attract the attention of researchers. Therefore it has become necessary to update the available information on RS, and this review attempts to analyze the information published, especially in the recent past, on classification, structure, properties, applications and health benefits of RS.

the form of granules in cereal or legume seed endosperm, tubers (potato and sweet potato), unripe fruits (banana and mango) and many other plant reserve organs. It is present in diverse shapes such as round, oval, lenticular and angular, with the shape depending mainly on the botanical source. It can vary among plant species as well as cultivars of the same species.4 The size of starch granules generally ranges between 1 and 100 μm. Starches are natural polymers occurring in all plant organs and are one of the main forms of dietary carbohydrates. Starch occurs as granules wherein carbohydrates are stored in an insoluble and tightly packed manner.5 A number of monosaccharide or sugar (glucose) molecules are linked together with 𝛼-1,4 and 𝛼-1,6 linkages to form starch granules.6 Starch is made up of amylose and amylopectin. Amylose has a degree of polymerization up to 6000, while amylopectin is highly branched and has a degree of polymerization up to 2 × 106 . X-ray diffraction studies reveal that starch is present in two crystalline structures, namely ‘A’ and ‘B’ types. These two forms vary in their proportion of amylopectin. A-type starches are found in cereals, while B-type starches are found in tubers and amylose-rich starches. A third type, namely ‘C’ type, appears to be a mixture of A and B forms and is found in legumes.7 Although starch granules are insoluble in cold water, they form a paste when gelatinized at higher temperature (>40 ∘ C) in excess water. This starch paste is a mixture of dissolved carbohydrate substances and amylose and low-polymerized chains of amylopectin. Starch substances bind a considerable amount of water on cooling. Changes in starch gels stored at 0 ∘ C for a long period of time are termed ‘aging’. A reduction in paste viscosity indicates the phenomenon of ‘syneresis’. The gradual winding-up of straight chains

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STARCH

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Starch is a major storage carbohydrate and is the second most abundant polysaccharide next to cellulose. Starch is present in J Sci Food Agric 2015; 95: 1968–1978

Correspondence to: Pinky Raigond, Division of Crop Physiology, Biochemistry and Postharvest Technology, Central Potato Research Institute, Shimla, India. [email protected] Division of Crop Physiology, Biochemistry and Postharvest Technology, Central Potato Research Institute, Shimla, India

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Resistant starch in food

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in starch paste is a process termed ‘retrogradation’. This process occurs at a higher rate in starch pastes stored at lower temperature. The retrograded starch is considered semi-crystalline in nature, as both crystalline and amorphous patterns are present. Crystalline structures formed by the double helices of amylopectin have lower thermostability owing to their branching and short chains. Heating at temperatures above 120 and 60 ∘ C helps in the rehydration of products of amylose and amylopectin retrogradation, respectively. Amylolytic enzymes can easily hydrolyze the gelatinized starch.8 In general, digestible starches are broken down/hydrolyzed by the enzymes 𝛼-amylase, glucoamylase and sucrose-isoamylase in the small intestine. It has been shown that B-type starches are resistant to enzymatic digestion, while A-type starches are slowly digestible.9,10 The supramolecular structure, i.e. packing of crystallites inside starch granules, the ratio of amylose and amylopectin, the fine structure of amylose and the surface characteristics of starch granules are the major internal factors that affect the digestibility of raw starch.11 The semi-crystalline structure of starch is formed owing to the concentric layers of amorphous and crystalline regions radiating from the hilum, and amylopectin is responsible for the semi-crystalline region.12

CLASSIFICATION OF STARCH The classification of dietary carbohydrates is based on their chemical and physiological properties.13 Based on the action of enzymes and the rate and extent of digestion, starches can be classified into three kinds, namely rapidly digestible starch (RDS),14 slowly digestible starch (SDS)14 and resistant starch (RS).15 These three types of starch differ in the time taken for digestion in the small intestine. Rapidly digestible starch The major proportion of dietary starch is rapidly digested. High levels of RDS are found in starchy foods cooked by moist heat (bread and potatoes). RDS is defined as a ‘type of starch which is rapidly (within 20 min) converted to glucose molecules by enzymatic digestion’.14 If RDS is present in high proportions in food, it will rapidly release glucose into the blood and thereby elevate blood glucose and insulin response, which is detrimental to health.16 RDS is significantly correlated with glycemic index, based on in vivo postprandial glycemic response.17 – 19

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Resistant starch The resistance of starch is influenced by the ratio of amylose and amylopectin. Amylose is slowly digested, whereas digestion of amylopectin is fast after retrogradation. Starch is hydrolyzed in the gastrointestinal tract by the activity of amylolytic enzymes, and the product of hydrolysis, i.e. glucose, is digested and absorbed in the small intestine. This type of hydrolysis and digestion occurs only when the starch present in food is gelatinized during cooking and the cooked food is consumed immediately after preparation. The term ‘resistant starch’ was coined by Englyst et al.15 to describe a small fraction of starch that resists hydrolysis by 𝛼-amylase and pullulanase treatment in vitro. When compared with RDS and SDS, RS is not hydrolyzed to glucose in the small intestine within 120 min of being consumed but is fermented in the colon. RS is a linear molecule of 𝛼-1,4-d-glucan and is mainly derived from retrograded amylose. The rate and extent of digestion are affected by a large number of factors, all of which are interlinked, which complicates understanding of the resistant nature of starch granules. Generally, the RS content of granular starch is positively correlated with the amylose level of the starch. However, there are some exceptions such as pea starch in which the amylose content is medium but the RS content is high.33 – 35 A strong correlation between the amylose and RS contents of maize starch has been reported by Morita et al.36 Because of the unique functional and nutritional properties of amylose, efforts have been made to develop crops containing high-amylose starch.37 High-amylose potato, barley and wheat have been developed.38 – 41 Several in vitro and in vivo methods are available to measure RS content accurately. Relationship between RDS, SDS and RS Three starch fractions, i.e. RDS, SDS and RS, are measured during enzymatic hydrolysis. In most processed foods, RDS is inversely proportional to SDS and RS, i.e. if the amount of RDS is higher, the amount of SDS and RS is lower. Therefore, when making SDS, the first important step is to reduce the amount of RDS. Usually, SDS and RS coexist in processed foods and are structurally close in terms of retrogradation.42 To make SDS from RDS, several physical, chemical and physiological methods are available.43 Table 1 summarizes the classification of starch.14

CLASSIFICATION AND STRUCTURE OF RS Depending on its nature, RS is classified into five subtypes, namely RS1, RS2, RS3, RS4 and RS5. Earlier classification of RS included the three types RS1, RS2 and RS3, while types RS4 and RS5 were included in subsequent years.14,44 – 47 RS1 RS1 is a type of RS that is physically inaccessible to digestion, possibly owing to its entrapment within whole or partly milled grains or seeds and the presence of intact cell walls in grains, seeds or tubers. In such cases the starch becomes inaccessible to amylolytic and digestive enzymes, and degradation of cell wall components is not possible in the gastrointestinal tract owing to the lack of cell wall-degrading enzymes.8 This type of starch passes the small intestine as such. It can be completely digested in the small intestine only if it is properly milled. Being heat-stable, it does not break down during normal cooking.


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Slowly digestible starch As the name indicates, SDS is the proportion of starch that takes a long time for digestion but is completely digested in the small intestine. SDS is defined as a ‘type of starch which is converted to glucose after 120 min of enzymatic digestion’.14 SDS is basically a physically inaccessible amorphous starch. The in vitro Englyst test has revealed that mostly raw cereal starches are rich in SDS, while the slow and prolonged postprandial glucose release profile was confirmed by human testing of normal corn starch (A type).20 Gelatinization of starches during heat–moisture food processing/cooking decreases the slow digestion property of native cereal starches.21 For the production of SDS in a patented process, partially debranched amylopectin was retrograded after isoamylase treatment.22,23 According to investigators, it is possible to prepare SDS by modifying the molecular structure of starch molecules, including 1-octenyl succinic anhydride (OSA)-modified starch, cross-linked starch and enzymatically modified starch with 𝛼-1,6 linkages.24 – 26 SDS and low-glycemic food confer similar

health benefits. Foods rich in SDS are beneficial27 – 29 and delay the occurrence of metabolic syndrome, diabetes and cardiovascular diseases.30 – 32

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P Raigond, R Ezekiel, B Raigond

Table 1. Classification of starch14 Starch fractions Item

RDS

SDS

Digestion timeline (in vitro)/place Examples

Within 20 min/mouth and small intestine Freshly cooked food

Amount (g per 100 g dry matter) Main physiological property

Boiled hot potato: 65 Rapid source of energy

Native waxy maize starch, millet, legumes Boiled millet: 28 Slow and sustained source of energy and sustained blood glucose

Structure

Mainly amorphous

Amorphous/crystalline

1970

RS2 RS2 comprises native starch granules that are protected from digestion by their conformation or structure, as in raw potatoes and green bananas. Because of their crystalline nature, native and uncooked starch granules are poorly susceptible to hydrolysis.48 The compact structure of RS2 makes it inaccessible to digestive enzymes and amylases. Digestion of RS1 and RS2 is slow and incomplete in the small intestine. The resistant nature of raw potato starch was first observed by Nowotny49 in 1938. He subjected raw starch from numerous plant species to enzymatic hydrolysis and observed the small extent of enzymatic hydrolysis of raw potato starch. Japanese researchers confirmed this result later.50,51 The resistant nature of raw starch is not fully understood and requires further investigation. The resistant nature of fine-grain high-amylose maize starch and coarse-grain potato starch is similar. High-amylose maize starch is a type of RS2 which retains its structure and resistance even during processing and preparation of foods. Potato starch granules are bigger than cereal starch granules, and the size of granules affects the extent of enzyme adsorption on their surface. Kimura and Robyt52 found that there was no relationship between the extent of enzyme adsorption and the degree of hydrolysis. Later, the degree of starch crystallinity was related to the extent of enzymatic hydrolysis. Amylolytic enzymes first degrade the amorphous region. Therefore resistance was attributed to the crystalline region. However, the degree of crystallinity is not always linked to resistance to amylolytic enzymes. Starch containing more amylose is considered to be more resistant to enzymatic hydrolysis. Starches with B-type crystallinity have been found to be more resistant to enzymatic hydrolysis.51,53 In B-type starches, enzymatic damage is only on the surface of granules, whereas starches with A-type crystallinity undergo deep enzymatic hydrolysis. Gallant et al.,54 Ridout et al.55 and Kossmann and Lloyd56 observed that the B-type crystalline structure of potato starch consists of double helices forming large ‘blocklets’ incorporated in ‘hard’ crystalline layers of granules, and these large ‘blocklets’ are responsible for the resistant nature of potato starch. In cereal starch granules the ‘blocklets’ are smaller than those in potato starch granules, so cereal starch is more susceptible to enzymatic hydrolysis. Therefore it can be concluded that starch resistance does not depend on any single factor but on a large number of factors, including size of granules, shape of granule surface, amylose content, starch crystallinity and size of pores in starch granules.8


20–120 min/small intestine

RS (types 1–5) >120 min/not in small intestine, main action in colon Raw potato, staled bread Raw potato starch: 75 Effects on gut health (e.g. prebiotic, fermentation to butyrate with hypothesized anticarcinogenic effects) Dependent on type, mainly crystalline

RS3 Physically modified starches come under this category. RS3 is retrograded starch, mainly retrograded/recrystallized amylose, formed during cooling of gelatinized starch and in cooked foods that are kept at low or room temperature. RS3 is thermally very stable and is formed in moist-heated foods. Being thermally stable, it is an important starch fraction and is also used as an ingredient in a wide variety of conventional foods.48 RS3 has a higher water-holding capacity than granular starch.57 Cooked and cooled potatoes and cornflakes are good examples of RS3. When starch paste/gel is stored at low or room temperature for some time, amylose double helices aggregate and form a highly thermostable B-type crystalline structure. The aggregates can be rehydrated only at temperatures above 150 ∘ C. RS formation is influenced by storage temperature and duration. More RS is formed when starch paste is stored at low temperature for several hours than at high temperatures.58 B-type crystalline RS is obtained during storage at low temperature, whereas storage at boiling temperature results in A-type crystallinity.59 Starch gel contains amorphous and crystalline fractions, with the former being hydrolyzed by amylolytic enzymes and the latter remaining resistant to enzyme activity.60 Interaction of starch with other components also affects its resistance. In starch from many plant species, amylose chains are penetrated by lipids and consequently do not participate in retrogradation, resulting in less production of RS3.61 Like amylose, amylopectin also forms partly crystallized gels. Crystallization of amylopectin proceeds very slowly, and amylopectin crystalline structures are less stable than amylose crystalline structures. They can be rehydrated at 55–70 ∘ C.45 Amylopectin crystalline structures formed during storage of starch paste/gel are also resistant to activity of amylolytic enzymes. The major part of amylose is retrograded and precipitated from solution, but at high temperatures these processes occur only in its fractions.62 Formation of retrograded starch depends on the botanical origin of the starch and the procedure applied for its production. The products of amylose retrogradation prepared by both in vitro and in vivo methods are resistant to amylolytic enzymes. Product preparation from amylopectin retrogradation is a lengthy process and may take from a few days to a few weeks of paste storage at an appropriate temperature. This process becomes efficient with repeated heating and cooling of starch pastes. RS4 RS4 is a group of chemically modified starches with similarity to resistant oligosaccharides and polydextrose.63 Starches that


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have been etherized, esterified or cross-bonded with chemicals to decrease their digestibility come under this category. Depending on its solubility in water and the method of analysis, RS4 is further subdivided into four subcategories.64 Chemical modification can prevent the digestion of RS by blocking enzyme access and forming typical linkages such as 𝛼-1,4 and 𝛼-1,6 linkages, and the main modifications are conversion, substitution and cross-linking.65 The resistance of acetylated and hydroxypropylated starch increases with increasing degree of substitution.66 Hydroxypropyl distarch phosphate and acetylated distarch phosphate are less susceptible to enzymatic hydrolysis than native starches.67 The degree of chemical modification and the level of resistance are directly proportional: the higher the degree of substitution with phosphoric acid, the greater is the resistance of monostarch phosphate. Heating the product of monostarch phosphate with glycine produced starch with higher resistance to enzymatic hydrolysis than monostarch phosphate itself.68 Also, heating of soluble starch saturated with iron(III) and treated with glycine resulted in starch highly resistant to amylolytic enzyme activity. Chemical modification changes the structure and composition of starch granules and hence increases their resistance to amylolytic enzymes. The normal chain arrangement of starch is disturbed by substitution and the starch becomes inaccessible to amylolytic enzymes. RS5 RS5 is a type of RS arising from the formation of amylose–lipid complexes. These complexes can be formed during food processing and can also be prepared under controlled conditions. Amylose–lipid complexes are generally formed from highamylose starches. The structure and formation of RS5 depend on the botanical source. RS5 comprises polysaccharides of waterinsoluble linear poly-𝛼-1,4-glucan and is resistant to degradation by 𝛼-amylase.47 These polysaccharides promote the formation of SCFA, particularly butyrate, which is the most important SCFA. Table 2 summarizes the classification of RS types.14,47,64,69 – 71

PROPERTIES OF RS RS has gained importance because of its functional properties. It has many desirable physicochemical properties, e.g. swelling, viscosity increase, gel formation and water-binding capacity, which make it useful in a variety of foods.72 RS can be used to replace flour on a one-to-one basis without significantly affecting dough

handling or rheology. RS is present naturally and is bland in flavor, with white color and fine particle size. Because of its fine particle size, RS does not affect the texture of food. RS imparts special characteristics along with dietary fiber fortification in high-fiber foods.73 The calorific content of RS is also low (1.6–2.8 kcal g−1 ), so it can be used to complement reduced-fat and reduced-sugar food formulations. Its physical properties, particularly its low water-holding capacity, provide good handling in processing, as well as crispiness, expansion and improved texture in the end-product. RS has a high gelatinization temperature, good extrusion and film-forming qualities and lower water-holding properties than traditional fiber products. It increases the coating crispness of products and the bowl life of breakfast cereals. Because of the above properties, RS has been used successfully in a range of baked and extruded products. RS is especially suitable for grain-based, low-moisture and moderate-moisture food systems.

APPLICATIONS OF RS RS has attracted the attention of nutritionists and food processors because of its potential physiological benefits and unique functional properties. Owing to increasing awareness about healthy and nutritious foods, consumers are now concerned with supplementary health merits derived from regular ingestion of RS along with traditional nutritional aspects of foods.74 Looking into consumer awareness, food manufacturers, researchers and producers are aiming at the production of improved foods with better digestion and health benefits.75 RS is present naturally in a broad range of starchy products, so it can be added as a functional ingredient. RS-fortified foods are becoming popular and consumers are accepting food products enriched with RS in order to increase their dietary fiber intake.76 RS-containing starch ingredients are commonly sold as ‘resistant starch’ at commercial level. A large number of these products are fully digestible and considered as RS suppliers.77 The first ever commercially available product of RS was reported only during the mid-1990s. Nowadays, RS rich-powders are prepared by a number of companies employing technologies such as that developed at Kansas State University using an amylose-rich starch from maize hybrids.78 RS products are of high quality and cannot be replaced by traditional insoluble fibers.79 RS is used in the production of moisture-free food products. Cross-linked starches prepared from maize, tapioca and

Table 2. Classification of types of resistant starch (RS), food sources and factors affecting their resistance to digestion in colon14,47,64,69 – 71 RS type

Description

RS1

Physically protected

RS2

Ungelatinized resistant granules with type B crystallinity, slowly hydrolysed by 𝛼-amylase Retrograded starch

RS3

RS4

RS5

Chemically modified starches due to cross-linking with chemical reagents Amylose–lipid complexes

Resistance minimized by

Whole or partly milled grains and seeds, legumes Raw potatoes, green bananas, some legumes, high-amylose corn

Milling, chewing

Cooked and cooled potatoes, bread, cornflakes, food products with repeated moist heat treatment Foods in which modified starches have been used (e.g. breads, cakes) Foods with high amylose content

Processing conditions

Food processing and cooking

Less susceptible to digestibility in vitro Not susceptible to hydrolysis by 𝛼-amylase


Digestion in small intestine Slow rate; partial degree; totally digested if properly milled Very slow rate; little degree; totally digested when freshly cooked Slow rate; partial degree; reversible digestion; digestibility improved by reheating Result of chemical modification; can resist hydrolysis Can resist digestion

1971

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Food sources


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Table 3. Functional properties and advantages of commercial sources of RS2 and RS364,70,80,83 Natural sources Bland in flavor White in color High gelatinization temperature Fine particle size (which causes less interference with texture) Useful in products for celiacs as bulk laxatives and in products for oral rehydration therapy Allow the formation of low-bulk high-fiber products with improved texture, appearance and mouth-feel (such as better organoleptic qualities) compared with traditional high-fiber products Increase coating crispness of products Increase bowl life of breakfast cereals Functional food ingredients Lower calorific value of foods Lower water-holding properties than traditional fiber products Good extrusion and film-forming qualities

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potato are used for formulations that need pulpy texture, smoothness, flowability, low-pH storage and high-temperature storage.80 To improve the textural properties and health benefits, baked products, pasta products and beverages are fortified with RS. Arimi et al.81 have successfully replaced most or all of the fat in imitation cheese with RS, without adversely affecting meltability or hardness and conferring the well-established benefits of RS as a functional fiber. A large number of products rich in fiber are available on the market, e.g. high-fiber bread and breakfast cereals,82 but other products such as white bread, biscuits and cakes are not fortified with fiber. The availability of process-tolerant RS has now made it possible to prepare foods rich in dietary fiber. RS has been added in the preparation of pasta and beverages, and dried pasta products containing up to 15% RS can be made with little or no effect on dough rheology during extrusion. Pasta prepared with addition of RS was lighter in color, but a firm texture was obtained in the same cooking time as a control that contained no added fiber.69 Resistant starches generally require suspension and add opacity to beverages and may be used in thickened, opaque health drinks where insoluble fiber is desired. Fibers other than RS generally have a strong flavor, coarse texture and poor as well as dry mouth-feel. However, RS imparts a less gritty mouth-feel and masks flavors to a lesser extent. Table 3 summarizes the functional properties and advantages of commercial sources of RS2 and RS3.64,70,80,83 The first commercial RS was introduced as Hi-maize by Starch Australia Ltd. Later, other commercial sources of RS such as Crystalean (RS3), Novelose 240 (RS2), Novelose 260 (RS2), Novelose 330 (RS3), Eurylon (RS2), Amylomaize VII (RS2) and Neo-amylose (RS3) were introduced to increase the dietary fiber content in foods. Crystalean is an RS3 preparation produced by starch retrogradation of high-amylose maize starch ae-VII hybrid. Hylon VII, a natural high-amylose maize starch, was introduced by the National Starch and Chemicals Co. (USA). The above-mentioned RS3 products have been prepared by heating and cooling high-amylose corn starch under controlled moisture and temperature conditions; these processes help in the manufacture of granular forms of concentrated RS containing 47–60% RS. Using maltodextrins as starting material, a natural, highly crystalline RS3 (Actistar Act*-RS3) has also been developed. The taste of Act*-RS3 is very natural owing to the


P Raigond, R Ezekiel, B Raigond raw material and production process used. Fibersym HA is a product of high-amylose corn and is suitable for use in a wide array of lower-net-carbohydrate food products. This product provides more than 70% dietary fiber in food and is used in a wide variety of products such as pizza crusts, breads, tortillas, cookies, muffins, breakfast cereals, snack products and nutritional bars. Fibersym 80ST is a product derived from potatoes and has slightly higher water-holding properties, which can impact finished food product properties such as cookie spread or muffin volume. The RS content is also high in products such as Nutriose FB06 and Fibersol-2, which deliver 85 and 90% fiber content respectively. Commercial preparations of RS4 such as Fibersym 80ST, Fibersym RW, Fibersym HA and Fibersol-2 are available on the market. RS4 is less susceptible to enzymatic hydrolysis and confers health benefits by reducing cholesterol, triglyceride and glucose levels in blood.8 RS preparations reduce the availability of some saccharides in food without affecting the organoleptic properties of food products. The quality of products remains the same after addition of components with artificially increased RS and does not deteriorate during baking; hence the quality of bakery products is not affected. Also, the organoleptic properties of extruded products and confectionery are not affected.84 Table 4 summarizes the commercially manufactured resistant starches commonly used in foods.42,70,85

HEALTH BENEFITS OF RS The international food industry is investigating ways to produce innovative food products with health benefits to fulfill the growing demands of consumers for functional foods due to increasing health awareness. Development of carbohydrate products with low glycemic index is gaining attention owing to their health benefits. Products with low glycemic index can improve the control of obesity and diabetes and subsequently reduce the risk of cardiovascular disease.86 All types of RS are not beneficial to the cholesterol level in blood. The production of SCFA by bacterial fermentation of RS in the large intestine is determined by the composition and properties of RS.87 Slow digestibility of RS leads to the slow release of glucose. RS has physiological benefits of soluble fibers and a positive impact on colonic health by increasing the crypt cell production rate or decreasing colonic epithelial atrophy in comparison with no-fiber diets. Although RS would not normally be used in unheated foods, for physiological studies of the health benefits of RS, raw RS powders were added to beverages and jellies at levels of 24–60 g RS day−1 .88 Nowadays, viewpoints on nutrition have changed. Until recently, consumption of carbohydrate-rich foods was highly recommended. Nutritional value of food is expressed by a tendency to reduce the calorific value of meals, especially in developed countries. Civilizational changes have also contributed to an increased intake of dietary fiber, indispensable for proper functioning of the human organism. RS has gained greater interest because it is a natural food component which is neutral to the organism and adds little calorific value to food. Dietary fibers, including RS, promote beneficial physiological effects, including laxation, blood cholesterol attenuation and blood glucose attenuation. RS: a type of dietary fiber Dietary fiber is usually defined as a food component that resists digestion by human enzymes in the small intestine and passes into the large intestine where it may or may not be fermented by


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Table 4. Commercially manufactured resistant starches commonly used in various foods42,70,85 Brand name of commercial RS

Type

RS/TDF contenta

Hi-maize

RS2

30–60% TDF

Crystalean

RS3

19.2–41% RS

Novelose 240

RS2

47% RS

Novelose 260

RS2

60% RS

Novelose 300

RS3

70% TDF

Fibersym 80ST

RS4

80% TDF

Nutriose FB06 Fibersol-2

– –

85% TDF 90% TDF

Hylon VII Neo-amylose

RS2 RS3

23% TDF 87 or 95% RS

a

Physiological and/or health benefits Prebiotic properties; lowers fecal pH; increases level of SCFA (in particular butyrate, which may reduce cancer risk); increases bowel action with its mild laxative effect; increases bowel-beneficial microflora Prebiotic effect; increases proportion of butyrate; increases cell proliferation in proximal colon (in rats); provides soluble dietary fiber and prebiotic effects; low glycemic index Lowers glycemic response when used as a substitute for flour and other rapidly digested carbohydrates Lowers glycemic response when used as a substitute for flour and other rapidly digested carbohydrates Lowers glycemic response when used as a substitute for flour and other rapidly digested carbohydrates Health benefit potential; prebiotic effect; source of butyrate; supports immune system; reduces glycemic response; low calorific value; easily fermentable; very well tolerated Acts as prebiotic; reduces glycemic and insulin response of healthy individuals as well as type 2 diabetics Acts as prebiotic; reduces glycemic and insulin response of healthy individuals as well as type 2 diabetics Low calorific value Probiotic effect; intestinal regularity and blood sugar regulation Increases level of SCFA Prebiotic; protects against inflammatory intestinal disease; may protect against colorectal cancer; may help control blood glucose levels in diabetics

Manufacturer National Starch and Chemicals Co., USA

Opta Food Ingredients Inc., USA

National Starch and Chemicals Co., USA



Cerestar (a Cargill company)

MGP Ingredients, Inc. (Atchison, KS) and Cargill

MGP Ingredients, Inc. (Atchison, KS) and Cargill

Roquette Freres, France ADM/Matsutani National Starch and Chemicals Co., USA Protos-Biotech. (Celanese Ventures GmbH)

RS, resistant starch; TDF, total dietary fiber.

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Insoluble dietary fiber such as lignin, cellulose and hemicellulose usually has high water-holding capacity, which contributes to increased fecal bulk. The role of dietary fiber in the body is influenced by degree of fermentation, and dietary fiber that is not fermented in the body is excreted in the feces. Dietary fiber confers health benefits and physiological effects, including laxation and/or blood cholesterol attenuation and/or blood glucose attenuation.93 RS promotes probiotic bacteria RS has been found to function as a prebiotic, and interest in its prebiotic potential is increasing. Prebiotics are defined as ‘non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacterial species already resident in the colon and thus attempt to improve host health’.94 There is a symbiotic relationship between prebiotics and probiotics.94 One of the best examples of a prebiotic is fructo-oligosaccharide, but certain other carbohydrates also have potential as prebiotics. RS functions as a prebiotic as well as a symbiotic.95 Some examples of typical prebiotics include inulin, oligofructose and inulin-type fructans.76 RS promotes the growth and activity of probiotic bacteria and can interact with other prebiotic dietary fibers such as 𝛽-glucan



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gut bacteria; examples are oligosaccharides and RS. Another definition of dietary fiber is that it is the part of a plant, present in the form of a chemical substance, which has indigestibility in the small intestine and/or has beneficial digestive and physiological effects and metabolic fate.89 The recent definition of dietary fiber is ‘the edible part of plants or analogous carbohydrates that are resistant to digestion and absorption in the human small intestine with complete or partial fermentation in the large intestine’.90 The main components of dietary fiber are non-starch polysaccharides (NSP), lignin, RS and non-digestible oligosaccharides. NSP include cellulose and hemicellulose (glucans, gums and pectin). The principal components of dietary fiber are NSP and lignin, where lignin is a non-carbohydrate component of plant cell walls. More recently, it has been suggested that non-digestible oligosaccharides such as raffinose, stachyose, oligofructose and inulin also function as dietary fiber. NSP (𝛽-linked polymers) are completely resistant to amylolytic enzymes.91 Consumption of soluble dietary fiber such as 𝛽-glucan and arabinoxylan leads to the formation of viscous solutions and increases the viscosity in the intestine, slowing intestinal transit, which in turn delays gastric emptying and slows glucose and sterol absorption by the intestine. It can also lower serum cholesterol, postprandial blood glucose and insulin levels.92

www.soci.org and hence acts as a prebiotic component.96,97 Probiotics improve human health by acting on the specific colonization of the human (or animal) gastrointestinal tract by one or more bacterial species. The ingestion of RS helps in extending the viability of some probiotic organisms in the colon. As a prebiotic, RS protects some of the ingested organisms on their path to the colon and effectively increases the initial levels of the desirable species once they reach the colon. In the colon, RS may initiate its role as substrate for a portion of the probiotic organisms.94 High-amylose starch (HAS) acts as a prebiotic and is also a source of RS2. The health benefit of HAS is through the promotion of fecal excretion of probiotic organisms. HAS also prevents the development of non-reversible insulin resistance and lowers plasma cholesterol and triglyceride concentrations compared with a diet rich in amylopectin starch in humans.98 RS has a close relationship with colonic health as it affects fecal bulk and SCFA metabolism.69 The role of RS has been investigated in relation to hypocholesterolemic effects and protective effects against colorectal cancer.99 The high fermentation rate of retrograded RS3 and the production of SCFA with a high proportion of butyrate by action of the intestinal microflora are mainly responsible for better colonic health.100 In the case of RS4, enzymes are inaccessible because of chemical modifications such as conversion, substitution and cross-linking and also owing to the formation of typical linkages such as 1 → 2, 1 → 3, 1 → 4 and 1 → 6. Most of the biopolymers are digested and metabolized in the colon by the large number of microorganisms and enzymes present. Bacterial amylases hydrolyze RS to produce glucose, which is further metabolized into organic acids (e.g. lactic acid) and gases (CO2 , H2 and CH4 ).101,102 Among all dietary fibers, only RS during fermentation produces higher butyrate, which is known as the principal nutrient of colonocytes and whose lack would increase the risk of some colonic diseases such as colon cancer. Among SCFA, butyrate has been implicated in improving colonic health and reducing the risk of colorectal cancer. Butyrate provides energy to the epithelial cells and inhibits the malignant transformation of such cells in vitro; this makes easily fermentable RS fractions especially useful in preventing colonic cancer. The site of production of SCFA is dependent on the rate of fermentation in the colon and explains the low risk of flatus after ingestion of significant levels of RS.89 Liu and Xu103 showed that suppression of the formation of colonic aberrant crypt loci was dependent on RS dose only when it was present during the phase of genotoxic carcinogen formation in the middle and distal colon. This shows that RS may retard the development of neoplastic lesions in the colon. RS can be beneficial to adults with colonic lesions. It has the potential to improve human health and lower the risk of many diet-related diseases.75,104

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Hypoglycemic effect of RS Hypoglycemia mainly occurs as a side effect in patients with diabetes mellitus, but it can also occur in other diseases. The rate of digestion is slow in foods rich in RS. The inaccessibility of starch to digestive enzymes (𝛼-amylase, isoamylase and pullulanase) in starchy products is responsible for the nutraceutical potential of starchy products as well as the reduction in postprandial blood glucose and insulin response. Glycemic index (GI) is used to rank products with respect to their influence on postprandial glycemia.3 RS has been reported to play a role in the reduction of glycemic and insulinemic responses to food. In 1998 the FAO recommended increased intake of low-GI foods, with emphasis on diabetics and subjects with impaired glucose tolerance.13 In the case of type II diabetes, RS has assumed great importance owing


P Raigond, R Ezekiel, B Raigond to its slow rate of glucose release as well as the time it takes to metabolize. Higher SDS content in the diet can also help to maintain good health in both diabetic and non-diabetic persons.14,105 The nutritional quality of cereal grains can be improved by reducing the starch digestibility during processing and increasing the SDS and RS content of the product. Whole grains with a higher concentration of dietary fibers may lower the sugar release into blood and are a good example of low-GI foods.106 The outer layer and germ of wheat, barley, rye and oat grains contain many bioactive components such as dietary fibers, antioxidants, phenolic compounds, lignin, vitamins and minerals.107 These bioactive compounds have been linked to reduced risk of cardiovascular disease, cancer, diabetes, obesity and other chronic diseases as well as coronary heart disease.108 Owing to increasing consumer awareness about the relationship between diet and disease, the food industry is now focusing on producing functional foods based on various cereal whole grain flours and other low-GI products. Hypocholesterolemic effects RS particularly affects lipid metabolism. Total lipids, total cholesterol, low-density lipoproteins (LDL), high-density lipoproteins (HDL), very-low-density lipoproteins (VLDL), intermediate-density lipoproteins (IDL), triglycerides and triglyceride-rich lipoproteins have been affected by RS.64 RS diets containing 25% raw potato markedly raised the cecal size and cecal pool of SCFA as well as SCFA absorption in the colon and lowered plasma cholesterol and triglyceride levels in rats. Also, a low concentration of cholesterol in all lipoprotein fractions, especially HDL1, and a reduction in triglyceride concentration in the triglyceride-rich lipoprotein fraction have been observed in rats.69 Cassava starch extruded with 9.9% oat fiber or cassava starch extruded with 9.7% RS confers hypocholesterolemic properties, and these starches can be used in foods to improve cardiovascular health.109 According to Hashimoto et al.,110 RS ingestion may decrease the serum cholesterol level in rats fed a cholesterol-free diet. There are still contradictions regarding the role of RS in altering triglyceride and cholesterol levels. Hence more research is needed to help us better understand the effects of RS on lipid metabolism in humans. Energy and weight management RS provides balanced energy for hours after consumption, because the energy of RS is partially released in the small intestine as glucose and partially released in the large intestine as fermentation by-products (such as acetate). The energy value of RS is very low and has been calculated as approximately 8 kJ g−1 (2 kcal g−1 ), whereas the energy value for completely digestible starch is 15 kJ g−1 (4.2 kcal g−1 ).111 The role of RS in modifying fat oxidation, as a satiety agent and in weight management has been studied by many authors.64,70,112 RS-rich diets may potentially enhance the mobilization and use of fat stores as an indirect result of any reduction in insulin secretion.113 RS-rich foods provide fewer calories along with lower glucose response as compared with digestible glucose-based carbohydrates. By RS consumption, total and regional body fat accumulation is reduced, with lower adipocyte volume. RS is associated with increased lipid oxidation at the expense of carbohydrate oxidation and thus decreased lipid production. The physiological properties mentioned above are important to control weight and reduce obesity.2 Keenan et al.114 reported that using RS in a diet as a bioactive functional food component is a natural, endogenous way to increase gut hormones that are effective in reducing energy intake. This may be an effective natural approach to the treatment of obesity.


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Reduction of gallstone formation Consumption of digestible starch causes greater secretion of insulin, leading to gallstone formation. Insulin is also reported to stimulate cholesterol synthesis.69 Therefore RS consumption helps in reducing the incidence of gallstones. Incidences of gallstones are less frequent in southern India, where whole grains are consumed rather than flour, than in northern India.82 The dietary intake of RS is two- to fourfold lower in the USA, Europe and Australia compared with populations consuming high-starch diets, such as in India and China, which may be reflected in the difference in the number of gallstone cases in the latter countries.69,115 Absorption of minerals RS increases the ileal absorption of a number of minerals in rats and humans. Enhanced absorption of only calcium has been observed in humans, whereas enhanced absorption of calcium, magnesium, zinc, iron and copper has been reported in rats fed RS-rich diets.97 A large increase in calcium and iron absorption was observed when a meal containing 16.4% RS was consumed.116 According to Schulz et al.,117 some RS (RS2 but not RS3) could improve calcium and magnesium absorption by enhancing mineral solubility in the cecum and/or large intestine. However, no effect of RS on the absorption of glucose produced by digestion of the digestible starch fraction has been demonstrated and also no evidence of the influence of RS on amino acids and vitamins has been reported. Raw potato starch is considered to be RS2. Feeding raw potato starch enhances fermentation in the distal parts of the digestive tract. As a result, the absorption of calcium, magnesium, iron, zinc and copper was increased owing to hypertrophy of the cecal wall and cecal acidification.118 Other health benefits of RS RS has been found to reduce inflammatory bowel diseases such as ulcerative colitis and other large bowel problems such as diverticulitis and constipation.64 As RS increases SCFA and butyrate production in vivo, it may prove a useful adjunct to traditional treatments of ulcerative colitis (SCFA enemas in human patients). RS2- and RS3-rich diets fed to rats with chemically induced colitis resulted in normalization of cell functions such as activation of colonic cell proliferation, restoration of apoptotic responses and uptake of SCFA, increased cecal levels of butyrate and improved cecal and distal macroscopic and histological observations.119 However, owing to the beneficial effects of RS on supplementation of fecal bulk, fecal consistency and transit time, for example, consumption of RS may be helpful in improving these conditions. RS has also been reported to affect immune functions through production of pro-inflammatory cytokines and expression of the number of receptors on T- and B-lymphocytes that are required for the initiation of immune responses.120,121

FUTURE TRENDS

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SUMMARY RS has assumed great importance owing to its potential health benefits and functional properties in foods. A reasonably good understanding of RS with respect to its structure and mechanism has been achieved through research on its physical, chemical and physiological aspects. Food consumption studies have shown that RS consumption has declined over the last few decades. This decline could be due to reduced intake of foods containing natural fibers and increased intake of fast foods. To overcome this problem, food scientists have developed a number of RS-enriched products. RS is ideal for use in ready-to-eat cereals, snacks, pasta, noodles, baked goods and fried foods and allows for easy labelling as simply ‘starch conferring additional nutraceutical benefits’. Its content can be increased by modifying processing conditions such as number of heating and cooling cycles, pH, temperature and time and freezing and drying. RS shows improved crispness and expansion in certain products, which have better mouth-feel, color and flavor than products produced with traditional fibers. RS is considered as a type of dietary fiber and shows physiological properties that can reduce the risk of several diseases, including colon cancer and diabetes, and can be very useful in controlling diabetes and obesity. RS-fortified products have found better consumer acceptability because of the unique physicochemical properties of RS and its bland taste.



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RS in food is an active area of research, and the increasing number of research papers that have appeared on this topic in recent years is testimony to the importance of RS. It will continue to interest researchers in the future as well. Several commercial preparations of RS are now available that can be used to increase the fiber content of foods. More research will be needed to produce RS with improved functional properties in terms of texture, solubility and resistance to thermal processes. Health benefits of RS are well

recognized. However, further studies will be needed for developing RS preparations with optional characteristics to claim specific health benefits such as improved bowel health and lowering the glycemic response. With the available information on RS, it is very difficult to suggest a figure for RS consumption for general health benefit, although some figures have been proposed for specific health benefits.85 More research will be needed before recommendations on minimum RS consumption can be made for general health benefit. Modern food-processing practices have led to lower RS consumption. Because of the desirable functional and physiological properties of RS, there is an increasing trend to incorporate commercial preparations of RS in processed foods. In developed countries where processed food daily intake is considerable, RS may constitute a substantial part of dietary fiber intake. RS can be used in diets as a bioactive functional food component to increase gut hormones that are effective in reducing energy intake for the treatment of obesity. RS is considered to be a promising and innovative food ingredient owing to its physiological benefits, and it may form an essential ingredient of innovative foods to be developed in the future as the demands for healthier foods increase. More tailor-made starch derivatives with multiple modifications are likely to be developed in the future.82 The development of insoluble, resistant maltodextrins with a functionality similar to RS has been reported by Buttriss and Stokes.76 More innovations of this type can be expected in the future. Chemically modified starch derivatives, which are non-digestible and can be categorized as RS, are likely to find increasing applications in food formulations.122 Although there are some reservations regarding chemically modified starches, the use of nutritionally harmless chemicals such as citric acid for chemical modification of starches can be helpful in addressing such reservations. Extrusion has been reported to be useful for increasing the RS content of native starches,123 and more extruded products with increased RS content can be expected in the future. The production of RS with resistance to thermal processing will be needed to increase its use in processed food formulations.

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