Resistant starch as prebiotic: A review - BPS - Wiley

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DOI 10.1002/star.201000099

Starch/Sta¨rke 2011, 63, 406–415

REVIEW

Resistant starch as prebiotic: A review Evange´lica Fuentes-Zaragoza, Elena Sańchez-Zapata, Esther Sendra, Estrella Sayas, Casilda Navarro, Juana Fernańdez-Lo´pez and Jose´ A. Pe´rez-Alvarez IPOA Research Group, Agro-Food Technology Department, Universidad Miguel Hernańdez, Orihuela, Alicante, Spain

The increase in consumers demand for high-quality food products has led to the growth in the use of new technologies and ingredients such as RS. RS occurs basically in all starchy foods and has a long history as food source for humans. RS includes the portion of starch that can resist digestion by human pancreatic amylase in the small intestine and thus, reach the colon. His great nutritional interest is associated with his physiological effects, similar to those of dietary fibre. The regular consumption of certain subclasses of highly fermentable dietary fibre sources result in gut associated immune and microbiota modulation as well as a significant production of SCFAs. Among the different physiological roles of RS, its prebiotic effect is of great interest. RS can be considered prebiotic and it is not absorbed in the intestine. The best approach of prebiotic–probiotic symbiosis is achieved by encapsulation. But other food biocompounds can be encapsulated too using RS.

Received: August 8, 2010 Revised: January 15, 2011 Accepted: January 17, 2011

Keywords: Microencapsulation / Prebiotic / Probiotic / Resistant starch / Symbiosis

1

Introduction

The role of dietary active compounds in human nutrition is one of the most important areas of concern and research in the field of nutritional science. The findings of researchers on this subject have wide-ranging implications for consumers, health-care providers, and nutrition educators as well as food producers, processors, and distributors [1–3]. Currently, marketing ‘healthy’ foods to otherwise healthy people has met with unprecedented success because of the realization that, attention to diet as part of a healthy lifestyle, can considerably reduce the risk of disease and promote health [3]. The early growth of the obesity epidemic in developed countries some 30 years ago was associated with ingestion of high-fat, low-carbohydrate diets. Thus any improvements in health by diet could be interesting both, food industry and health systems.

Correspondence: Dr. Jose´ A. Pe´rez-Alvarez, IPOA Research Group, Agro-Food Technology Department, Universidad Miguel Hernańdez, Crta. a Beniel, Km. 3,2, E-03312 Orihuela, Alicante, Spain. E-mail: [email protected] Fax: þ34-96-674-9677 Abbreviations: FOS, fructooligosaccharides; RDS, rapidly digested starch.

ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Foods can contain a range of chemically distinct carbohydrate substances, which have varied gastrointestinal and metabolic properties. Based on current knowledge of the mechanisms by which dietary carbohydrates exert their influence on physiology and health, dietary carbohydrates have been classified into: (i) ‘available carbohydrates’, which are digested and absorbed in the small intestine providing carbohydrates for metabolism, and (ii) ‘resistant carbohydrates’, which resist digestion in the small intestine or are poorly absorbed/metabolized [4]. Nutritionally, the most prominent resistant carbohydrate is dietary fibre; however, there are numerous other sources of resistant carbohydrates that occur naturally in small amounts or that have been developed as functional ingredients. These include extracted polysaccharides such as gums, oligosaccharides such as fructans, polydextrose, resistant maltodextrins, and RS [4]. The identification of fibre as one of the effectors of healthy gut function inevitably led to the search for other food carbohydrates with like properties.

2

Resistant starch

RS includes the portion of starch that can resist digestion by human pancreatic amylase in the small intestine and thus, reach the colon [5]. The general behaviour of RS is physiologically similar to that of soluble, fermentable fibre, www.starch-journal.com

Starch/Sta¨rke 2011, 63, 406–415 like guar gum. The most common results include increased fecal bulk and lower colonic pH [6] and improvements in glycaemic control, bowel health, and cardiovascular disease risk factors [7], so it has shown to behave more like compounds traditionally referred to as dietary fibre. RS is the fraction of starch which is not hydrolyzed to D-glucose in the small intestine within 120 min of being consumed, but which is fermented in the colon. Many studies have shown that RS is a linear molecule of a-1,4-D-glucan, essentially derived from the retrograded AM fraction, and has a relatively low MW (1.2 105 Da). RS is an extremely broad and diverse range of materials and a number of different types exist. At present, these are mostly defined according to physical and chemical characteristics [8, 9]. A number of factors may cause starch to be resistant to digestion, including the size of the starch-containing fragments (such as coarsely ground grains), the structure and conformation of intact starch granules, and the formation of retrograded crystallites as a result of processing and chemical modification. RS is found in many common foods, including grains, cereals, vegetables (especially potatoes), legumes, seeds, and some nuts [10].

2.1 Types of resistant starch RS has been classified into five general subtypes named RS1–RS5, which are described below: Type 1 includes physically inaccessible starch that is locked within cell walls and food matrixes, thus preventing amylolysis. Milling and chewing can make these starches more accessible and less resistant. RS1 is heat stable in most normal cooking operations, which enables its use as an ingredient in a wide variety of conventional foods. Type 2 is composed of native starch granules from certain plants containing uncooked starch or starch that was gelatinized poorly and hydrolyzed slowly by R-amylases (e.g., high-AM corn starches) [5, 11–13]. RS2 describes native starch granules that are protected from digestion by the conformation or structure of the starch granule. This compact structure limits the accessibility of digestive enzymes (has low bioaccesibility), various amylases, and accounts for the resistant nature of RS2 such as, ungelatinized starch. In the diet, raw starch is consumed in foods like banana [14]. A particular type of RS2 is unique as it retains its structure and resistance even during the processing and preparation of many foods; this RS2 is called high-AM maize starch [15]. Type 3 refers to retrograded or crystalline nongranular starch formed after cooking, like the starch found in cooked and cooled potatoes, bread crusts, cornflakes, and retrograded high AM maize starch. RS3 refers to non-granular starch-derived materials that resist digestion [5, 12, 15]. RS3 is of particular interest, because of its thermal stability. ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

407 This allows it to be stable in most normal cooking operations, and enables its use as an ingredient in a wide variety of conventional foods [9]. During food processing, in most cases in which heat and moisture are involved, RS1 and RS2 can be destroyed, but RS3 can be formed [16]. Storey et al., classified a soluble polysaccharide called ‘retrograded resistant maltodextrins’ as type 3 RS. They are derived from starch that is processed to purposefully rearrange or hydrolyze starch molecules, and subsequent retrogradation, to render them soluble and resistant to digestion. This process results in the formation of indigestible crystallites that have a molecular similarity to type 3 RS but with a smaller degree of polymerization as well as a lower MW [17], converting a portion of the normal alpha1,4-glucose linkages to random 1,2-, 1,3-, and 1,4-alpha or beta linkages [18]. Type 4 includes chemically modified or re-polymerized starches (e.g., chain linkage altered dextrins, ethers, or esters) used by food manufacturers to alter the functional characteristics of the starch [5, 12, 13], and include starches which have been etherized, esterified, or crossbonded with chemicals in such a manner as to decrease their digestibility [19]. RS4 can be produced by chemical modifications, such as conversion, substitution, or crosslinking, which can prevent its digestion by blocking enzyme access and forming atypical linkages [14, 20]. Type 5 RS is an AM-lipid complexed starch [21], which is formed from high AM starches that require higher temperatures for gelatinization and are more susceptible to retrograde [22]. In general, the structure and amount of starch-lipid in foods depend on their botanical sources [23]. Also, Frohberg and Quanz [24] defined as RS5 a polysaccharide that consists of water-insoluble linear polyalpha-1,4-glucan that is not susceptible to degradation by alpha-amylases. They also found that the poly-alpha1,4-D-glucans promote the formation of short-chain fatty acids (SCFA), particularly butyrate, in the colon and are thus suitable for use as nutritional supplements for the prevention of colorectal diseases.

2.2 Sources of resistant starch RS occurs basically in all starchy foods but not in a fixed quantity. In addition to the structure of the starch as laid down during biosynthesis, methods used to prepare process and store foods, either domestically or industrially also determine the proportion of the starch that escapes digestion [25]. Table 1 provides a summary of the RS content of some basic and processed foods. Starch is found in a wide variety of plant tissues, including leaves, tubers, fruits, and seeds. RS may be found in both unprocessed and processed foods. As shown in Table 1, cereal grains and legumes are an important natural source of RS. www.starch-journal.com

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Starch/Sta¨rke 2011, 63, 406–415

E. Fuentes-Zaragoza et al.

Table 1. Approximate total dietary fibre, starch and resistant starch of some food sources (g/100 g as eaten). Source Legumes Red kidney beans Lentils Black-eyed peas Cereal grains Barley Corn White rice Wheat Oats Flours Corn Wheat Rice Potato Grain-based food products Spaghetti Rolled oats Cereal products Crisp bread White bread ‘Granary’ bread Extruded oat cereal Puffed wheat cereal Oat porridge Cooked spaghetti Cooked rice Potato products Boiled potatoes Chips Mashed potatoes

Total starch

Total dietary fibre

Resistant starch

42.6 53.3 53.9

36.8 33.1 32.8

24.6 25.4 17.7

55.2 77.9 95.1 50.8 43.4

17.0 19.6 1.5 17.0 37.7

18.2 25.2 14.1 13.6 7.2

84.3 68.8 86.9 81.0

2.8 12.1 5.1 2.1

11.0 1.7 1.6 1.7

73.0 56.0

5.6 10.0

3.3 8.5

67.4 46.7 44.1 57.2 67.0 9.0 n/a n/a

n/a n/a n/a n/a n/a n/a n/a n/a

1.4 1.9 6.0 0.2 1.2 0.3 2.9 3.7

n/a 29.5 n/a

n/a n/a n/a

2.0 4.8 2.4

Adapted from [7]; n/a: not available. In fruits, starch is an energetic reserve and its concentration decreases with ripeness; banana and mango are examples of this behaviour, since in their green or immature state, RS constitutes the largest fraction (70–80% in mango and 40–50% in banana), and simple carbohydrates (glucose, fructose, sucrose, etc.) are very scarce [26, 27]. Kumari et al. [28] reported that processing treatments and storage result in an increase in RS content of ready-toeat foods. Processed foods invariably undergo storage at moderate or low temperatures before consumption. Storage of foods is also a contributing factor to the changes in the available starch content of the product. The quantity of RS formed during processing/storage depends on the severity of the processing conditions like temperature, pH, moisture, number of heating/cooking cycles adopted, condition of storage, etc. In addition, many of the processing treatments such as freezing, autoclaving, etc., are also known to have significant impact on the fermentation of RS. ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

3

Resistant starch as functional ingredient

Starch-based food products have diverse nutritional properties, which are influenced by the origin of the starch, its composition, processing method used, and process conditions applied. Increasing health awareness and growing demand for functional foods by consumers are driving the food industry internationally to look at ways to produce innovative food products with health benefits [29]. Considerable scientific research has confirmed the beneficial role of the dietary fibre in the reduction of several chronic diseases. So consumer awareness about the healthy role of dietary fibre intake has raised, gaining popularity fibre-enriched cereal based products [30]. The development of slowly digestible carbohydrates has increased considerably in recent years, due to interest in low GI foods and to control obesity and diabetes and, subsequently, to reduce the risk of cardiovascular disease [29]. www.starch-journal.com

Starch/Sta¨rke 2011, 63, 406–415 There is considerable interest in the nutritional implications of RS in foods, since its physiological effects are similar to those attributed to dietary fibre [31], such as increased laxation, reduced risk of get digestive tract cancers [32], lowering postprandial glucose response [33, 34], and lowering blood lipid levels [35, 36]. RS also shows promising physiological impact in the prevention of gall stone formation [37]. RS has a long history of safe consumption by humans and is a natural component of some foods. Intakes vary but are generally low, particularly in Western diets. Similar to soluble fibre, a minimum intake of RS (5–6 g) appears to be needed in order for beneficial reductions in insulin response to be observed. Estimates of daily intake of RS range from 3 to 6 g/day (averaging 4.1 g/day) in Europe and Australia with similar but inconsistent data for the US [38]. As diets become more and more ‘processed’ – with fewer raw fruit and vegetables – the consumption of RS is reduced. Therefore, incorporating RS into processed foods is increasingly important [39–42]. As a food ingredient, RS has a lower calorific (8 kJ/g) value compared with fully digestible starch (15 kJ/g) [43], therefore it can be a substitutive of digestible carbohydrates, lowering the energy content of the final formulation. Some RS products are also measured as total dietary fibre (TDF) in standard assays, potentially allowing high-fibre claims. In addition, RS can be either water

409 soluble (e.g., Fibersol 2; resistant maltodextrins) or insoluble. These differences can have a profound impact on potential food applications and quality [10]. RS can be fermented by human gut microbiota, providing a source of carbon and energy for the 400–500 bacteria species present in this anaerobic environment and thus potentially altering the composition of the microbiota and its metabolic activities. The fermentation of carbohydrates by anaerobic bacteria yields SCFA, primarily composed of acetic, propionic, and butyric acids, which can lower the lumen pH, creating an environment less prone to the formation of cancerous tumours [5]. Table 2 shows some results of the production of SCFA of some different sources of RS. RS consumption has also been related to reduced postprandial glycemic and insulinemic responses, which may have beneficial implications in the management of diabetes, and is associated with a decrease in the levels of cholesterol and triglycerides. Other effects of RS consumption are increased excretion frequency and fecal bulk, prevention of constipation and hemorrhoids, decreased production of toxic and mutagenic compounds, lower colonic pH, and ammonia levels. Considering that nowadays several diseases result from inadequate feeding, and that some may be related to insufficient fibre intake, it is reasonable to assume that an increased consumption of indigestible components would be important.

Table 2. Molar proportion of the three main SCFAs produced from RS sources, compared with other types of fibre, after 24 h of fermentation (mol%). Fermentation conditions

Source

Acetate

Propionate

Butyrate

Ref.

RS Starch Oat bran Wheat bran Cellulose Guar gum Ispaghula Pectin

41 50 57 57 61 59 56 75

21 22 21 15 20 26 26 14

38 29 23 19 19 11 10 9

[8] [8] [8] [8] [8] [8] [8] [8]

Amylopectin Xilan Inulin Pectin RS Hylon VIIa) (3 g/L) RS Hylon VIIa) (6 g/L) RS Hylon VIIa) (12 g/L) Novelose 240 Cristalean ACT-RS31

35 18 20 64 6 5 5 53 66 62

11 11 5 12 4 5 7 16 12 12

54 70 75 26 4 6 9 30 20 24

[71] [71] [71] [71] [72] [72] [72] [73] [73] [73]

In vivo

In vitro

a) Hylon VII ¼ High-amylose maize starch. ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

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In this context, RS sources could be preferentially included in the diet, since they do not cause pronounced organoleptic alterations as do traditional fibre sources (brans) [44, 45].

4

Prebiotic effects of resistant starch

4.1 Prebiotic definition The definition of ‘prebiotics’ as a novel concept in nutrition has been proposed in 1995, by semantic analogy with the term ‘probiotics’. Even if slightly different definitions are proposed and discussed by several international instances, prebiotics always refer to the fact that food ingredients or nutrients escape the digestion in the upper part of the digestive tract, are selectively fermented by bacteria, thereby changing the composition and/or activity of the gastrointestinal microbiota. An important point of the definition is that it must confer benefits upon host health [46, 47]. Prebiotics are utilized to promote the survival of probiotics. Prebiotics are nondigestible carbohydrates that are not absorbed in the intestine, such as RS [48]. RS is not absorbed in the small intestine; it provides the colonic microbiota with a fermentable carbohydrate substrate. It has been suggested that RS promotes a higher proportion of butyric acid than other indigestible carbohydrates. Butyrate constitutes a major energy substrate for the colonocytes and is associated with benefits in relation to colonic health [49, 50]. They travel to the colon where they promote the growth of specific advantageous microbiota (probiotics) by supplying food/energy, while simultaneously influencing the microbiota’s gene expression [51]. RS is currently attracting widespread interest for its potential health benefits leading to growing demand for robust, cost-effective RS assays for industrial, regulatory, and research use. Unlike other dietary fibre components, RS is neither intrinsically indigestible nor a fixed entity and is determined by an individual´s upper gut digestive capacity as well as food processing and storage conditions so any analysis needs to accommodate physiological factors such as transit time [52]. The possible applications of RS such as prebiotic constituents in functional food formulations could be summarized [53]:

(i) as fermentable substrates for growth of probiotic microbiota, especially lactobacilli and bifidobacteria, (ii) as dietary fibre promoting several beneficial physiological effects, (iii) as encapsulation materials for probiotic in order to enhance their stability. ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Starch/Sta¨rke 2011, 63, 406–415

4.2 Synergistic effects of RS Short chain fructooligosaccharides (FOS) and RS may act synergistically (by combining, and thus increasing, their prebiotic effects) [54], the administration of the combination of FOS and RS induced changes in the intestinal microbiota, by increasing lactobacilli and bifidobacteria in caecum and colonic contents. Several types of prebiotic fibres can be distinguished considering their rate of fermentability. Such role depends on the carbohydrate chain length as it has been demonstrated in vitro in a fermentation system, showing that FOS are rapidly fermented whereas long chain prebiotic, like inulin, are steadily fermented. These observations have been confirmed in vivo once the different prebiotics reach the large intestine: FOS are rapidly fermented, whereas RS is slowly degraded. In consequence, the particular kinetics would determine the region of the intestine where the effects will be clearer. Thus, FOS would be more active in the first parts of the large bowel whereas RS would reach the distal part of the colon. In fact, Le Blay et al. [55] have reported that administration of FOS or raw potato starch induces different changes in bacterial populations and metabolites in the caecum, proximal, and distal colon, as well as in faeces. As compared with RS FOS doubled the pool of caecal fermentation products, like lactate, while the situation was just the opposite distally. These observations confirm that each prebiotic shows particular properties, which should be considered before their application for intestinal diseases; thus, rapidly fermentable prebiotics are particularly useful in those affecting the proximal part of the large intestine, while slowly fermentable prebiotics should be chosen for more distal intestinal conditions. Moreover, an association with different prebiotics with complementary kinetics should be considered when a health-promoting effect throughout the entire colon is required. So, functional foods based on the combination of two different dietary fibres, with different rate of fermentability along the large intestine, may result in a synergistic effect, and thus, in a more evident prebiotic effect that may confer a greater health benefit to the host [56]. Also, RS and inulin combination showed synergistic effects on intestinal calcium and magnesium absorption and balance in rats. The fermentation of these substrates in the large bowel to SCFA is the main reason for this increase in mineral absorption [56].

4.3 Probiotic and symbiotic Functional foods have changed and increased the role of food in health. Probiotics are the fastest growing sector of the functional food industry, through their role in increasing the number of beneficial bacteria in the gut. These living microorganisms are primarily derived from lactic acid bacwww.starch-journal.com

Starch/Sta¨rke 2011, 63, 406–415 teria, comprising multiple strains from the genera Lactobacillus and Bifidobacterium. Some foods combine several microorganisms [50]. Beneficial health effects attributed to probiotics are shortening of the duration of rotavirus diarrhea, relief of signs, and symptoms of lactose intolerance, decreasing the risk of allergy in atopic individuals, cancer prevention, lowering of serum cholesterol levels, prevention of urogenital infections, and synthesis and enhancement of the bioavailability of nutrients. Probiotic bacteria may compete with pathogens for nutrients and mucosal adherence, produce antimicrobial substances, and modulate mucosal immune functions. The beneficial effects of probiotics are strain-specific, therefore for the definition of which probiotics (as a single strain or a combination) are most effective in specific diseases is needed [48]. The breakdown of prebiotic molecules by bacterial enzymes into SCFA (acetate, butyrate, and propionate) are crucial for gut integrity and function, modulation of the immune system, calcium and magnesium absorption, and maintenance of normal serum cholesterol levels. The end products of this fermentation are consumed by both these bacteria and intestinal epithelium as fuel. Symbiotic refer to nutritional supplements which contain probiotics and prebiotics in combination. Since it has been hypothesized that prebiotics ensure the survival of some beneficial bacteria, their effects might be additive or symbiotic [48]. Prebiotics selectively can stimulate probiotic strains. Prebiotics may improve the survival of bacteria crossing the upper part of the gastrointestinal tract, thereby enhancing their effects in the large bowel [57]. The best model of prebiotic–probiotic symbiosis is the encapsulation. Encapsulation is often mentioned as a way to protect bacteria against severe environmental factors. The physical protection of probiotics by microencapsulation is a new approach to improve the probiotic survival. Encapsulation helps to isolate the bacterial cells from the effects of the hostile environment and gastrointestinal tract, thus potentially preventing cell loss [58]. The goal of encapsulation is to create a micro-environment in which the bacteria will survive during processing and storage and be released at appropriate sites (e.g., small intestine) in the digestive tract. The benefits of encapsulation to protect probiotics against low gastric pH have been shown in numerous reports and similarly for liquid based products such as dairy products [59]. Microcapsules consist of a liquid core surrounded by a semipermeable membrane which retains the cells inside, reduces mass transfer limitation, and minimize phage contamination. For the encapsulation of viable cells, the materials and formulation conditions used should be gentle and non-toxic. In this respect, the antibacterial properties of chitosan limit its use as a core solution. However, alginate and starch liquid core capsules offer ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

411 the possibility to immobilize lactic acid bacteria without loss of viability and fermentation ability [60]. Starch and its derivated (RS) are widely used in the encapsulation of various food components, as probiotics. Indeed the use of starch in many encapsulation processes has provided solutions to problems such as thermal stabilization; process induced controlled release, and extended shelf-life of sensitive compounds [61]. The (micro) encapsulation of probiotics has received attention from food companies interested in producing probiotic-containing consumer products, but faced with the difficulty of maintaining cell viability over the shelf-life of the product [59]. A symbiotic approach is often accomplished by coencapsulation of RS in the form of high-AM maize starch together with the probiotic microorganisms within the microcapsule. Usually, 1–2% insoluble starch grains are added to the probiotic–hydrocolloid precursor directly before the encapsulation process, with the aim to further maintain the viability of probiotics [57, 62]. RS had been used to improve encapsulation of viable bacteria in yogurt. Sultana et al. [62] reported that the incorporation of Hi-Maize1 starch (commercial RS) improved encapsulation of viable bacteria (Lactobacillus acidophilus and Bifidobacterium spp.) in yoghurt, as compared to when the bacteria were encapsulated without the starch. Iyer and Kailasapathy [57], selected three different complementary prebiotics and were separately coencapsulated with Lactobacillus acidophilus and tested for their efficacy in yogurt. Addition of Hi-maize1 starch to capsules containing Lactobacillus spp. provided maximum protection to the encapsulated bacteria after 3 h of incubation at pH 2.0 compared with other two prebiotics, Raftiline1 and Raftilose1. Viable counts of Lactobacillus spp. increased significantly ( p < 0.05) with Hi-maize concentration of up to 1.0% w/v the viability of bacteria under in vitro acidic conditions. Addition of Hi-maize (1.0% w/v) to capsules containing Lactobacillus spp. and further coating with chitosan significantly increased ( p < 0.05) the survival of encapsulated bacteria under in vitro acidic and bile salt conditions and also in stored yogurt compared with alginate encapsulated cells. Homayouni et al. [58] have shown that encapsulation can significantly increase the survival rate of probiotic bacteria in ice cream over an extended shelf-life. They manufactured two types of symbiotic ice cream containing 1% of RS with free and encapsulated Lactobacillus casei (Lc-01) and Bifidobacterium lactis (Bb-12). The addition of encapsulated probiotics had no significant effect on the sensory properties of non-fermented ice cream in which was used the RS as prebiotic compound and L. casei and B. lactis survive in high numbers in the encapsulated samples. Encapsulation thus may enhance the shelf-life of probiotic cultures in frozen dairy products. www.starch-journal.com

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Probiotic cell concentrates are often required to be stored over longer periods prior to food manufacture and ingestion. Hence, it is often required to dry the probiotic microcapsules after production. This is particular important for dry foods, such as cereal products or beverage powder where probiotics are added in dry form. Nevertheless, the impact of microencapsulation on drying and storage of dried probiotic microorganisms prior to application in food systems is barely investigated, since efforts with respect to increase in survival are mainly focused on the application of protective substances. Heidebach et al. [63] studied the viability of probiotic cells (Bifidobacterium Bb12 and Lactobacillus F19) with dried protein-hydrogels microcapsules during a freeze-drying step as well as during subsequent storage in the dried state and the influence of RS granules in the protein matrix. In the case of Bifidobacterium Bb12 no difference in survival was found between free and encapsulated samples with and without RS. In the case of Lactobacillus F19, survival rates of microencapsulated cells without RS were significantly higher compared to free cells as well as cells that were encapsulated together with RS corns.

5

Health benefits of resistant starch

Scientific interest upon RS has increased significantly during the last decades, mostly due to its capacity to produce a large amount of butyrate all along the colon. Butyrate has been observed to have a range of effects on cell metabolism, differentiation, and cell growth as well as inhibition of a variety of factors that underlie the initiation, progression, and growth of colon tumors [64]. Starch processing can increase its prebiotic properties. The digestibility of starch in cooked potatoes changes when the potatoes are cooled after cooking, and these changes may be of considerable nutritional significance. When potato is cooled after cooking the starch undergoes profound changes in digestibility: the content of rapidly digested starch (RDS) decreases; the content of slowly digested starch (SDS), defined as starch digested between 20 and 120 min in vitro, increases markedly and the proportion of RS increases. The increase in RS means that the loading of non-digested polysaccharide (‘dietary fibre’) into the colon is greatly increased, making the cooled potato a valuable source of dietary fibre which, moreover, is enriched in a type (RS) that has demonstrated benefits as a prebiotic [65]. Without heat gelatinization the starch remains in granular form, highly resistant to enzymic attack (RS2) [66]. In such a state the potato would have little glycaemic impact but may contribute to prebiotic effects, although its use would be limited to products of low water content in which the granular form of the starch would remain intact. As a ß 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Starch/Sta¨rke 2011, 63, 406–415 result, this type of RS (RS2) is almost completely transformed into RDS upon cooking, but upon cooling, the content of RS again increases. Because this latter form of RS must have been regenerated from the almost completely digestible form (RDS) present in the potatoes immediately after cooking, it is RS Type III (RS3), or retrograded starch [65]. Shimoni [61] studied a fraction of RS, from high AM corn-starch, called RS type III (RS III). RS III is fermented by the microbiota in the colon, and it indicates that it may have health benefits such as modifying lipid metabolism and reducing the risk of colon cancer. RS III can be produced by heat-induced gelatinization of starch followed by recrystallization. The amount of RS III produced is affected by its composition, heat treatment, and recrystallization conditions. Understanding the relation between RS III polymorphism and its resistance is critical for the development of RS with improved prebiotic properties. The crystallite polymorphism and the lamella structure of RS III affect its enzymatic resistance, thus changing its prebiotic activities (e.g., its properties as an enzymatic substrate). This hypothesis was formulated based on studies that found correlation between starch crystallinity and its resistance to enzymatic digestion, and on other studies showing the effect of crystallization conditions on RS polymorph type.

6 Evaluation of the fermentation properties and potential prebiotic activity The prebiotic effect of a substrate can be measured as a selective effect upon growth of major bacterial groups commonly found in human gut, in particular a selection for increased numbers of bifidobacteria and lactobacilli in comparison with ‘undesirable’ micro-organisms, such as certain clostridia and bacteroides [67]. There are a number of methods currently in use to determine the prebiotic properties of a substrate, from pure cultures studies to human trials [54, 67–70]. However, a defining characteristic of prebiotic is the selective nature of certain groups of colonic bacteria seen as beneficial towards human health. This can only be determined in studies using mixed microbial culture which mimic the microbial ecology of the human intestinal tract. For a rapid comparative evaluation, anaerobic batch fermentations inoculated with faecal slurries are used. Because they represent the diverse gut microbiota, but are completed rapidly with several sets running simultaneously, these anaerobic batch fermentations present an excellent mode for small-scale screening of novel substrates. Until recently, growth of specific bacteria in such fermentations was measured through colony counting on selective agars. This approach, however, suffers from several drawbacks (time-consuming, labourintensive and non recovery of uncultivable organisms). www.starch-journal.com

Starch/Sta¨rke 2011, 63, 406–415 As a result, molecular techniques such as fluorescence in situ hybridization (FISH) have been developed to study microbial communities [70].

7

Conclusions

413 [9] Haralampu, S. G., Resistant starch: A review of the physical properties and biological impact of RS3. Carbohydr. Polym. 2000, 41, 285–292. [10] Goldring, J. M., Resistant starch: Safe intakes and legal status. J. AOAC Int. 2004, 87, 733–739. [11] Hernańdez, O., Emaldi, U., Tovar, J., In vitro digestibility of edible films from various starch sources. Carbohydr. Polym. 2008, 71, 648–655. [12] Sanz, T., Evaluation Effects in Food Res.

Salvador, A., Baixauli, R., Fiszman, S. M., of four types of resistant starch in muffins. II. texture, colour and consumer response. Eur. Technol. 2009, 229, 197–204.

Functional foods have revolutionized and augmented the role of food in health. Probiotics are the fastest growing component of the functional food industry, through their role in increasing the number of beneficial bacteria in the gut. RS can be fermented by human gut microbiota, and provides the colonic microbiota with a fermentable carbohydrate substrate. Scientific interest upon RS has increased significantly during the last decades, mostly due to its capacity to produce a large amount of butyrate all along the colon. Short chain FOS and RS may act synergistically by combining, and thus increasing, their prebiotic effects. The best model of prebiotic–probiotic symbiosis is the encapsulation. Starch and its derivated (RS) are widely used in the encapsulation of various food components, as probiotics. A symbiotic approach is often accomplished by co-encapsulation of RS in the form of high-amylose maize starch together with the probiotic microorganisms within the microcapsule.

[18] Mermelstein, N. H., Analyzing for resistant starch. Food Technol. 2009, 4, 80–84.

The authors have declared no conflict of interest.

[19] Nugent, A. P., Health properties of resistant starch. British Nutrition Foundation. Nutr. Bull. 2005, 30, 27–54.

8 References

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