You are on page 1of 10

406 DOI 10.1002/star.

201000099 Starch/Starke 2011, 63, 406415


Resistant starch as prebiotic: A review

Evangelica Fuentes-Zaragoza, Elena Sanchez-Zapata, Esther Sendra, Estrella Sayas,
Casilda Navarro, Juana Fernandez-Lopez and Jose A. Perez-Alvarez

IPOA Research Group, Agro-Food Technology Department, Universidad Miguel Hernandez, Orihuela, Alicante, Spain

The increase in consumers demand for high-quality food products has led to the growth in the Received: August 8, 2010
use of new technologies and ingredients such as RS. RS occurs basically in all starchy foods Revised: January 15, 2011
and has a long history as food source for humans. RS includes the portion of starch that can Accepted: January 17, 2011
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 prebioticprobiotic symbiosis is achieved by encapsulation.
But other food biocompounds can be encapsulated too using RS.

Microencapsulation / Prebiotic / Probiotic / Resistant starch / Symbiosis

1 Introduction Foods can contain a range of chemically distinct carbo-

hydrate substances, which have varied gastrointestinal
The role of dietary active compounds in human nutrition is and metabolic properties. Based on current knowledge
one of the most important areas of concern and research in of the mechanisms by which dietary carbohydrates exert
the field of nutritional science. The findings of researchers their influence on physiology and health, dietary carbo-
on this subject have wide-ranging implications for consum- hydrates have been classified into: (i) available carbo-
ers, health-care providers, and nutrition educators as well hydrates, which are digested and absorbed in the small
as food producers, processors, and distributors [13]. intestine providing carbohydrates for metabolism, and
Currently, marketing healthy foods to otherwise healthy (ii) resistant carbohydrates, which resist digestion in the
people has met with unprecedented success because of small intestine or are poorly absorbed/metabolized [4].
the realization that, attention to diet as part of a healthy Nutritionally, the most prominent resistant carbohydrate
lifestyle, can considerably reduce the risk of disease and is dietary fibre; however, there are numerous other sources
promote health [3]. The early growth of the obesity epi- of resistant carbohydrates that occur naturally in small
demic in developed countries some 30 years ago was amounts or that have been developed as functional ingre-
associated with ingestion of high-fat, low-carbohydrate dients. These include extracted polysaccharides such as
diets. Thus any improvements in health by diet could be gums, oligosaccharides such as fructans, polydextrose,
interesting both, food industry and health systems. 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.
Correspondence: Dr. Jose A. Perez-Alvarez, IPOA Research
Group, Agro-Food Technology Department, Universidad Miguel
Hernandez, Crta. a Beniel, Km. 3,2, E-03312 Orihuela, Alicante, 2 Resistant starch
E-mail: RS includes the portion of starch that can resist digestion
Fax: 34-96-674-9677
by human pancreatic amylase in the small intestine and
Abbreviations: FOS, fructooligosaccharides; RDS, rapidly thus, reach the colon [5]. The general behaviour of RS is
digested starch. physiologically similar to that of soluble, fermentable fibre,

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

Starch/Starke 2011, 63, 406415 407

like guar gum. The most common results include increased This allows it to be stable in most normal cooking oper-
fecal bulk and lower colonic pH [6] and improvements in ations, and enables its use as an ingredient in a wide
glycaemic control, bowel health, and cardiovascular dis- variety of conventional foods [9]. During food processing,
ease risk factors [7], so it has shown to behave more like in most cases in which heat and moisture are involved, RS1
compounds traditionally referred to as dietary fibre. and RS2 can be destroyed, but RS3 can be formed [16].
RS is the fraction of starch which is not hydrolyzed to Storey et al., classified a soluble polysaccharide called
D-glucose in the small intestine within 120 min of being retrograded resistant maltodextrins as type 3 RS. They
consumed, but which is fermented in the colon. Many are derived from starch that is processed to purposefully
studies have shown that RS is a linear molecule of rearrange or hydrolyze starch molecules, and subsequent
a-1,4-D-glucan, essentially derived from the retrograded retrogradation, to render them soluble and resistant to
AM fraction, and has a relatively low MW (1.2  105 Da). digestion. This process results in the formation of indiges-
RS is an extremely broad and diverse range of materials tible crystallites that have a molecular similarity to type 3
and a number of different types exist. At present, these are RS but with a smaller degree of polymerization as well as a
mostly defined according to physical and chemical charac- lower MW [17], converting a portion of the normal alpha-
teristics [8, 9]. 1,4-glucose linkages to random 1,2-, 1,3-, and 1,4-alpha or
A number of factors may cause starch to be resistant to beta linkages [18].
digestion, including the size of the starch-containing frag- Type 4 includes chemically modified or re-polymerized
ments (such as coarsely ground grains), the structure and starches (e.g., chain linkage altered dextrins, ethers, or
conformation of intact starch granules, and the formation esters) used by food manufacturers to alter the functional
of retrograded crystallites as a result of processing and characteristics of the starch [5, 12, 13], and include
chemical modification. RS is found in many common starches which have been etherized, esterified, or cross-
foods, including grains, cereals, vegetables (especially bonded with chemicals in such a manner as to decrease
potatoes), legumes, seeds, and some nuts [10]. their digestibility [19]. RS4 can be produced by chemical
modifications, such as conversion, substitution, or cross-
2.1 Types of resistant starch linking, which can prevent its digestion by blocking enzyme
access and forming atypical linkages [14, 20].
RS has been classified into five general subtypes named Type 5 RS is an AM-lipid complexed starch [21], which
RS1RS5, which are described below: is formed from high AM starches that require higher tem-
Type 1 includes physically inaccessible starch that is peratures for gelatinization and are more susceptible to
locked within cell walls and food matrixes, thus preventing retrograde [22]. In general, the structure and amount of
amylolysis. Milling and chewing can make these starches starch-lipid in foods depend on their botanical sources [23].
more accessible and less resistant. RS1 is heat stable in Also, Frohberg and Quanz [24] defined as RS5 a poly-
most normal cooking operations, which enables its use as saccharide that consists of water-insoluble linear poly-
an ingredient in a wide variety of conventional foods. alpha-1,4-glucan that is not susceptible to degradation
Type 2 is composed of native starch granules from by alpha-amylases. They also found that the poly-alpha-
certain plants containing uncooked starch or starch that 1,4-D-glucans promote the formation of short-chain fatty
was gelatinized poorly and hydrolyzed slowly by R-amy- acids (SCFA), particularly butyrate, in the colon and are
lases (e.g., high-AM corn starches) [5, 1113]. RS2 thus suitable for use as nutritional supplements for the
describes native starch granules that are protected from prevention of colorectal diseases.
digestion by the conformation or structure of the starch
granule. This compact structure limits the accessibility of 2.2 Sources of resistant starch
digestive enzymes (has low bioaccesibility), various amy-
lases, and accounts for the resistant nature of RS2 such RS occurs basically in all starchy foods but not in a fixed
as, ungelatinized starch. In the diet, raw starch is con- quantity. In addition to the structure of the starch as laid
sumed in foods like banana [14]. A particular type of RS2 is down during biosynthesis, methods used to prepare proc-
unique as it retains its structure and resistance even during ess and store foods, either domestically or industrially also
the processing and preparation of many foods; this RS2 is determine the proportion of the starch that escapes diges-
called high-AM maize starch [15]. tion [25]. Table 1 provides a summary of the RS content of
Type 3 refers to retrograded or crystalline nongranular some basic and processed foods.
starch formed after cooking, like the starch found in cooked Starch is found in a wide variety of plant tissues, includ-
and cooled potatoes, bread crusts, cornflakes, and retro- ing leaves, tubers, fruits, and seeds. RS may be found in
graded high AM maize starch. RS3 refers to non-granular both unprocessed and processed foods. As shown in
starch-derived materials that resist digestion [5, 12, 15]. Table 1, cereal grains and legumes are an important
RS3 is of particular interest, because of its thermal stability. natural source of RS.

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

408 E. Fuentes-Zaragoza et al. Starch/Starke 2011, 63, 406415

Table 1. Approximate total dietary fibre, starch and resistant starch of some food sources (g/100 g as eaten).

Source Total starch Total dietary fibre Resistant starch

Red kidney beans 42.6 36.8 24.6
Lentils 53.3 33.1 25.4
Black-eyed peas 53.9 32.8 17.7
Cereal grains
Barley 55.2 17.0 18.2
Corn 77.9 19.6 25.2
White rice 95.1 1.5 14.1
Wheat 50.8 17.0 13.6
Oats 43.4 37.7 7.2
Corn 84.3 2.8 11.0
Wheat 68.8 12.1 1.7
Rice 86.9 5.1 1.6
Potato 81.0 2.1 1.7
Grain-based food products
Spaghetti 73.0 5.6 3.3
Rolled oats 56.0 10.0 8.5
Cereal products
Crisp bread 67.4 n/a 1.4
White bread 46.7 n/a 1.9
Granary bread 44.1 n/a 6.0
Extruded oat cereal 57.2 n/a 0.2
Puffed wheat cereal 67.0 n/a 1.2
Oat porridge 9.0 n/a 0.3
Cooked spaghetti n/a n/a 2.9
Cooked rice n/a n/a 3.7
Potato products
Boiled potatoes n/a n/a 2.0
Chips 29.5 n/a 4.8
Mashed potatoes n/a n/a 2.4

Adapted from [7]; n/a: not available.

In fruits, starch is an energetic reserve and its concen- 3 Resistant starch as functional ingredient
tration decreases with ripeness; banana and mango are
examples of this behaviour, since in their green or imma- Starch-based food products have diverse nutritional prop-
ture state, RS constitutes the largest fraction (7080% in erties, which are influenced by the origin of the starch, its
mango and 4050% in banana), and simple carbohydrates composition, processing method used, and process con-
(glucose, fructose, sucrose, etc.) are very scarce [26, 27]. ditions applied. Increasing health awareness and growing
Kumari et al. [28] reported that processing treatments demand for functional foods by consumers are driving the
and storage result in an increase in RS content of ready-to- food industry internationally to look at ways to produce
eat foods. Processed foods invariably undergo storage at innovative food products with health benefits [29].
moderate or low temperatures before consumption. Considerable scientific research has confirmed the
Storage of foods is also a contributing factor to the beneficial role of the dietary fibre in the reduction of several
changes in the available starch content of the product. chronic diseases. So consumer awareness about the
The quantity of RS formed during processing/storage healthy role of dietary fibre intake has raised, gaining
depends on the severity of the processing conditions like popularity fibre-enriched cereal based products [30].
temperature, pH, moisture, number of heating/cooking The development of slowly digestible carbohydrates has
cycles adopted, condition of storage, etc. In addition, many increased considerably in recent years, due to interest in
of the processing treatments such as freezing, autoclav- low GI foods and to control obesity and diabetes and,
ing, etc., are also known to have significant impact on the subsequently, to reduce the risk of cardiovascular disease
fermentation of RS. [29].

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

Starch/Starke 2011, 63, 406415 409

There is considerable interest in the nutritional implica- soluble (e.g., Fibersol 2; resistant maltodextrins) or insolu-
tions of RS in foods, since its physiological effects are ble. These differences can have a profound impact on
similar to those attributed to dietary fibre [31], such as potential food applications and quality [10].
increased laxation, reduced risk of get digestive tract can- RS can be fermented by human gut microbiota, provid-
cers [32], lowering postprandial glucose response [33, 34], ing a source of carbon and energy for the 400500 bacteria
and lowering blood lipid levels [35, 36]. RS also shows species present in this anaerobic environment and thus
promising physiological impact in the prevention of gall potentially altering the composition of the microbiota and
stone formation [37]. its metabolic activities. The fermentation of carbohydrates
RS has a long history of safe consumption by humans by anaerobic bacteria yields SCFA, primarily composed of
and is a natural component of some foods. Intakes vary but acetic, propionic, and butyric acids, which can lower the
are generally low, particularly in Western diets. Similar to lumen pH, creating an environment less prone to the
soluble fibre, a minimum intake of RS (56 g) appears to formation of cancerous tumours [5]. Table 2 shows some
be needed in order for beneficial reductions in insulin results of the production of SCFA of some different sources
response to be observed. Estimates of daily intake of of RS.
RS range from 3 to 6 g/day (averaging 4.1 g/day) in RS consumption has also been related to reduced post-
Europe and Australia with similar but inconsistent data prandial glycemic and insulinemic responses, which may
for the US [38]. As diets become more and more proc- have beneficial implications in the management of diabe-
essed with fewer raw fruit and vegetables the con- tes, and is associated with a decrease in the levels of
sumption of RS is reduced. Therefore, incorporating RS cholesterol and triglycerides. Other effects of RS con-
into processed foods is increasingly important [3942]. sumption are increased excretion frequency and fecal
As a food ingredient, RS has a lower calorific (8 kJ/g) bulk, prevention of constipation and hemorrhoids,
value compared with fully digestible starch (15 kJ/g) [43], decreased production of toxic and mutagenic compounds,
therefore it can be a substitutive of digestible carbo- lower colonic pH, and ammonia levels. Considering that
hydrates, lowering the energy content of the final formu- nowadays several diseases result from inadequate feed-
lation. Some RS products are also measured as total ing, and that some may be related to insufficient fibre
dietary fibre (TDF) in standard assays, potentially allowing intake, it is reasonable to assume that an increased con-
high-fibre claims. In addition, RS can be either water sumption 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.

In vivo
RS 41 21 38 [8]
Starch 50 22 29 [8]
Oat bran 57 21 23 [8]
Wheat bran 57 15 19 [8]
Cellulose 61 20 19 [8]
Guar gum 59 26 11 [8]
Ispaghula 56 26 10 [8]
Pectin 75 14 9 [8]
In vitro
Amylopectin 35 11 54 [71]
Xilan 18 11 70 [71]
Inulin 20 5 75 [71]
Pectin 64 12 26 [71]
RS Hylon VIIa) (3 g/L) 6 4 4 [72]
RS Hylon VIIa) (6 g/L) 5 5 6 [72]
RS Hylon VIIa) (12 g/L) 5 7 9 [72]
Novelose 240 53 16 30 [73]
Cristalean 66 12 20 [73]
ACT-RS31 62 12 24 [73]

a) Hylon VII High-amylose maize starch.

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

410 E. Fuentes-Zaragoza et al. Starch/Starke 2011, 63, 406415

In this context, RS sources could be preferentially included 4.2 Synergistic effects of RS

in the diet, since they do not cause pronounced organo-
leptic alterations as do traditional fibre sources (brans) Short chain fructooligosaccharides (FOS) and RS may act
[44, 45]. synergistically (by combining, and thus increasing, their
prebiotic effects) [54], the administration of the combi-
nation of FOS and RS induced changes in the intestinal
4 Prebiotic effects of resistant starch microbiota, by increasing lactobacilli and bifidobacteria in
caecum and colonic contents. Several types of prebiotic
4.1 Prebiotic definition fibres can be distinguished considering their rate of fer-
mentability. Such role depends on the carbohydrate chain
The definition of prebiotics as a novel concept in nutrition length as it has been demonstrated in vitro in a fermenta-
has been proposed in 1995, by semantic analogy with the tion system, showing that FOS are rapidly fermented
term probiotics. Even if slightly different definitions are whereas long chain prebiotic, like inulin, are steadily fer-
proposed and discussed by several international instan- mented. These observations have been confirmed in vivo
ces, prebiotics always refer to the fact that food ingredients once the different prebiotics reach the large intestine: FOS
or nutrients escape the digestion in the upper part of the are rapidly fermented, whereas RS is slowly degraded. In
digestive tract, are selectively fermented by bacteria, consequence, the particular kinetics would determine the
thereby changing the composition and/or activity of the region of the intestine where the effects will be clearer.
gastrointestinal microbiota. An important point of the Thus, FOS would be more active in the first parts of the
definition is that it must confer benefits upon host health large bowel whereas RS would reach the distal part of the
[46, 47]. colon. In fact, Le Blay et al. [55] have reported that admin-
Prebiotics are utilized to promote the survival of pro- istration of FOS or raw potato starch induces different
biotics. Prebiotics are nondigestible carbohydrates that are changes in bacterial populations and metabolites in the
not absorbed in the intestine, such as RS [48]. RS is not caecum, proximal, and distal colon, as well as in faeces. As
absorbed in the small intestine; it provides the colonic compared with RS FOS doubled the pool of caecal fer-
microbiota with a fermentable carbohydrate substrate. It mentation products, like lactate, while the situation was just
has been suggested that RS promotes a higher proportion the opposite distally. These observations confirm that each
of butyric acid than other indigestible carbohydrates. prebiotic shows particular properties, which should be
Butyrate constitutes a major energy substrate for the colo- considered before their application for intestinal diseases;
nocytes and is associated with benefits in relation to thus, rapidly fermentable prebiotics are particularly useful
colonic health [49, 50]. They travel to the colon where in those affecting the proximal part of the large intestine,
they promote the growth of specific advantageous micro- while slowly fermentable prebiotics should be chosen for
biota (probiotics) by supplying food/energy, while simul- more distal intestinal conditions. Moreover, an association
taneously influencing the microbiotas gene expression with different prebiotics with complementary kinetics
[51]. should be considered when a health-promoting effect
RS is currently attracting widespread interest for its throughout the entire colon is required. So, functional foods
potential health benefits leading to growing demand for based on the combination of two different dietary fibres,
robust, cost-effective RS assays for industrial, regulatory, with different rate of fermentability along the large
and research use. Unlike other dietary fibre components, intestine, may result in a synergistic effect, and thus, in
RS is neither intrinsically indigestible nor a fixed entity and a more evident prebiotic effect that may confer a greater
is determined by an individuals upper gut digestive health benefit to the host [56].
capacity as well as food processing and storage conditions Also, RS and inulin combination showed synergistic
so any analysis needs to accommodate physiological fac- effects on intestinal calcium and magnesium absorption
tors such as transit time [52]. and balance in rats. The fermentation of these substrates
The possible applications of RS such as prebiotic con- in the large bowel to SCFA is the main reason for this
stituents in functional food formulations could be summar- increase in mineral absorption [56].
ized [53]:
(i) as fermentable substrates for growth of probiotic 4.3 Probiotic and symbiotic
microbiota, especially lactobacilli and bifido-
bacteria, Functional foods have changed and increased the role of
(ii) as dietary fibre promoting several beneficial phys- food in health. Probiotics are the fastest growing sector of
iological effects, the functional food industry, through their role in increasing
(iii) as encapsulation materials for probiotic in order to the number of beneficial bacteria in the gut. These living
enhance their stability. microorganisms are primarily derived from lactic acid bac-

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

Starch/Starke 2011, 63, 406415 411

teria, comprising multiple strains from the genera the possibility to immobilize lactic acid bacteria without
Lactobacillus and Bifidobacterium. Some foods combine loss of viability and fermentation ability [60]. Starch and
several microorganisms [50]. Beneficial health effects its derivated (RS) are widely used in the encapsulation of
attributed to probiotics are shortening of the duration of various food components, as probiotics. Indeed the use of
rotavirus diarrhea, relief of signs, and symptoms of lactose starch in many encapsulation processes has provided
intolerance, decreasing the risk of allergy in atopic individ- solutions to problems such as thermal stabilization; proc-
uals, cancer prevention, lowering of serum cholesterol ess induced controlled release, and extended shelf-life of
levels, prevention of urogenital infections, and synthesis sensitive compounds [61]. The (micro) encapsulation of
and enhancement of the bioavailability of nutrients. probiotics has received attention from food companies
Probiotic bacteria may compete with pathogens for interested in producing probiotic-containing consumer
nutrients and mucosal adherence, produce antimicrobial products, but faced with the difficulty of maintaining cell
substances, and modulate mucosal immune functions. viability over the shelf-life of the product [59].
The beneficial effects of probiotics are strain-specific, A symbiotic approach is often accomplished by co-
therefore for the definition of which probiotics (as a single encapsulation of RS in the form of high-AM maize starch
strain or a combination) are most effective in specific together with the probiotic microorganisms within the
diseases is needed [48]. microcapsule. Usually, 12% insoluble starch grains are
The breakdown of prebiotic molecules by bacterial added to the probiotichydrocolloid precursor directly
enzymes into SCFA (acetate, butyrate, and propionate) before the encapsulation process, with the aim to further
are crucial for gut integrity and function, modulation of the maintain the viability of probiotics [57, 62].
immune system, calcium and magnesium absorption, and RS had been used to improve encapsulation of viable
maintenance of normal serum cholesterol levels. The end bacteria in yogurt. Sultana et al. [62] reported that the
products of this fermentation are consumed by both these incorporation of Hi-Maize1 starch (commercial RS)
bacteria and intestinal epithelium as fuel. Symbiotic refer improved encapsulation of viable bacteria (Lactobacillus
to nutritional supplements which contain probiotics and acidophilus and Bifidobacterium spp.) in yoghurt, as com-
prebiotics in combination. Since it has been hypothesized pared to when the bacteria were encapsulated without the
that prebiotics ensure the survival of some beneficial bac- starch.
teria, their effects might be additive or symbiotic [48]. Iyer and Kailasapathy [57], selected three different
Prebiotics selectively can stimulate probiotic strains. complementary prebiotics and were separately coencap-
Prebiotics may improve the survival of bacteria crossing sulated with Lactobacillus acidophilus and tested for their
the upper part of the gastrointestinal tract, thereby enhanc- efficacy in yogurt. Addition of Hi-maize1 starch to capsu-
ing their effects in the large bowel [57]. les containing Lactobacillus spp. provided maximum pro-
The best model of prebioticprobiotic symbiosis is the tection to the encapsulated bacteria after 3 h of incubation
encapsulation. Encapsulation is often mentioned as a way at pH 2.0 compared with other two prebiotics, Raftiline1
to protect bacteria against severe environmental factors. and Raftilose1. Viable counts of Lactobacillus spp.
The physical protection of probiotics by microencapsula- increased significantly ( p < 0.05) with Hi-maize concen-
tion is a new approach to improve the probiotic survival. tration of up to 1.0% w/v the viability of bacteria under in
Encapsulation helps to isolate the bacterial cells from the vitro acidic conditions. Addition of Hi-maize (1.0% w/v) to
effects of the hostile environment and gastrointestinal capsules containing Lactobacillus spp. and further coating
tract, thus potentially preventing cell loss [58]. The goal with chitosan significantly increased ( p < 0.05) the sur-
of encapsulation is to create a micro-environment in which vival of encapsulated bacteria under in vitro acidic and bile
the bacteria will survive during processing and storage and salt conditions and also in stored yogurt compared with
be released at appropriate sites (e.g., small intestine) in the alginate encapsulated cells.
digestive tract. The benefits of encapsulation to protect Homayouni et al. [58] have shown that encapsulation
probiotics against low gastric pH have been shown in can significantly increase the survival rate of probiotic
numerous reports and similarly for liquid based products bacteria in ice cream over an extended shelf-life. They
such as dairy products [59]. manufactured two types of symbiotic ice cream containing
Microcapsules consist of a liquid core surrounded by a 1% of RS with free and encapsulated Lactobacillus casei
semipermeable membrane which retains the cells inside, (Lc-01) and Bifidobacterium lactis (Bb-12). The addition of
reduces mass transfer limitation, and minimize phage encapsulated probiotics had no significant effect on the
contamination. For the encapsulation of viable cells, the sensory properties of non-fermented ice cream in which
materials and formulation conditions used should be was used the RS as prebiotic compound and L. casei and
gentle and non-toxic. In this respect, the antibacterial B. lactis survive in high numbers in the encapsulated
properties of chitosan limit its use as a core solution. samples. Encapsulation thus may enhance the shelf-life
However, alginate and starch liquid core capsules offer of probiotic cultures in frozen dairy products.

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

412 E. Fuentes-Zaragoza et al. Starch/Starke 2011, 63, 406415

Probiotic cell concentrates are often required to be result, this type of RS (RS2) is almost completely trans-
stored over longer periods prior to food manufacture formed into RDS upon cooking, but upon cooling, the
and ingestion. Hence, it is often required to dry the pro- content of RS again increases. Because this latter form
biotic microcapsules after production. This is particular of RS must have been regenerated from the almost com-
important for dry foods, such as cereal products or bev- pletely digestible form (RDS) present in the potatoes
erage powder where probiotics are added in dry form. immediately after cooking, it is RS Type III (RS3), or
Nevertheless, the impact of microencapsulation on drying retrograded starch [65].
and storage of dried probiotic microorganisms prior to Shimoni [61] studied a fraction of RS, from high AM
application in food systems is barely investigated, since corn-starch, called RS type III (RS III). RS III is fermented
efforts with respect to increase in survival are mainly by the microbiota in the colon, and it indicates that it may
focused on the application of protective substances. have health benefits such as modifying lipid metabolism
Heidebach et al. [63] studied the viability of probiotic cells and reducing the risk of colon cancer. RS III can be pro-
(Bifidobacterium Bb12 and Lactobacillus F19) with dried duced by heat-induced gelatinization of starch followed by
protein-hydrogels microcapsules during a freeze-drying recrystallization. The amount of RS III produced is affected
step as well as during subsequent storage in the dried by its composition, heat treatment, and recrystallization
state and the influence of RS granules in the protein matrix. conditions. Understanding the relation between RS III poly-
In the case of Bifidobacterium Bb12 no difference in sur- morphism and its resistance is critical for the development
vival was found between free and encapsulated samples of RS with improved prebiotic properties. The crystallite
with and without RS. In the case of Lactobacillus F19, polymorphism and the lamella structure of RS III affect its
survival rates of microencapsulated cells without RS were enzymatic resistance, thus changing its prebiotic activities
significantly higher compared to free cells as well as cells (e.g., its properties as an enzymatic substrate). This hy-
that were encapsulated together with RS corns. pothesis was formulated based on studies that found
correlation between starch crystallinity and its resistance
to enzymatic digestion, and on other studies showing the
5 Health benefits of resistant starch effect of crystallization conditions on RS polymorph type.

Scientific interest upon RS has increased significantly

during the last decades, mostly due to its capacity to 6 Evaluation of the fermentation
produce a large amount of butyrate all along the colon. properties and potential prebiotic activity
Butyrate has been observed to have a range of effects on
cell metabolism, differentiation, and cell growth as well as The prebiotic effect of a substrate can be measured as a
inhibition of a variety of factors that underlie the initiation, selective effect upon growth of major bacterial groups
progression, and growth of colon tumors [64]. commonly found in human gut, in particular a selection
Starch processing can increase its prebiotic properties. for increased numbers of bifidobacteria and lactobacilli in
The digestibility of starch in cooked potatoes changes comparison with undesirable micro-organisms, such as
when the potatoes are cooled after cooking, and these certain clostridia and bacteroides [67]. There are a number
changes may be of considerable nutritional significance. of methods currently in use to determine the prebiotic
When potato is cooled after cooking the starch undergoes properties of a substrate, from pure cultures studies to
profound changes in digestibility: the content of rapidly human trials [54, 6770]. However, a defining character-
digested starch (RDS) decreases; the content of slowly istic of prebiotic is the selective nature of certain groups of
digested starch (SDS), defined as starch digested colonic bacteria seen as beneficial towards human health.
between 20 and 120 min in vitro, increases markedly This can only be determined in studies using mixed
and the proportion of RS increases. The increase in RS microbial culture which mimic the microbial ecology of
means that the loading of non-digested polysaccharide the human intestinal tract. For a rapid comparative evalu-
(dietary fibre) into the colon is greatly increased, making ation, anaerobic batch fermentations inoculated with fae-
the cooled potato a valuable source of dietary fibre which, cal slurries are used. Because they represent the diverse
moreover, is enriched in a type (RS) that has demonstrated gut microbiota, but are completed rapidly with several sets
benefits as a prebiotic [65]. running simultaneously, these anaerobic batch fermenta-
Without heat gelatinization the starch remains in gran- tions present an excellent mode for small-scale screening
ular form, highly resistant to enzymic attack (RS2) [66]. In of novel substrates. Until recently, growth of specific bac-
such a state the potato would have little glycaemic impact teria in such fermentations was measured through colony
but may contribute to prebiotic effects, although its use counting on selective agars. This approach, however, suf-
would be limited to products of low water content in which fers from several drawbacks (time-consuming, labour-
the granular form of the starch would remain intact. As a intensive and non recovery of uncultivable organisms).

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

Starch/Starke 2011, 63, 406415 413

As a result, molecular techniques such as fluorescence in [9] Haralampu, S. G., Resistant starch: A review of the physical
properties and biological impact of RS3. Carbohydr. Polym.
situ hybridization (FISH) have been developed to study 2000, 41, 285292.
microbial communities [70].
[10] Goldring, J. M., Resistant starch: Safe intakes and legal
status. J. AOAC Int. 2004, 87, 733739.
[11] Hernandez, O., Emaldi, U., Tovar, J., In vitro digestibility of
7 Conclusions edible films from various starch sources. Carbohydr. Polym.
2008, 71, 648655.
Functional foods have revolutionized and augmented the [12] Sanz, T., Salvador, A., Baixauli, R., Fiszman, S. M.,
Evaluation of four types of resistant starch in muffins. II.
role of food in health. Probiotics are the fastest growing Effects in texture, colour and consumer response. Eur.
component of the functional food industry, through their Food Res. Technol. 2009, 229, 197204.
role in increasing the number of beneficial bacteria in the [13] Ratnayake, W. S., Jackson, D. S., Thermal behavior of resist-
gut. RS can be fermented by human gut microbiota, and ant starches RS 2, RS 3, and RS 4. J. Food Sci. 2008, 73,
provides the colonic microbiota with a fermentable carbo- 356366.
hydrate substrate. Scientific interest upon RS has [14] Sajilata, M. G., Singhal, R. S., Kulkarni, P. R., Resistant starch
A review. Compr. Rev. Food Sci. Food Saf. 2006, 5, 117.
increased significantly during the last decades, mostly
due to its capacity to produce a large amount of butyrate [15] Wepner, B., Berghofer, E., Miesenberger, E., Tiefenbacher,
K., Citrate starch: Application as resistant starch in different
all along the colon. Short chain FOS and RS may act food systems. Starch/Starke 1999, 51, 354361.
synergistically by combining, and thus increasing, their
[16] Faraj, A., Vasanthan, T., Hoover, R., The effect of extrusion
prebiotic effects. The best model of prebioticprobiotic cooking on resistant starch formation in waxy and regular
symbiosis is the encapsulation. Starch and its derivated barley flours. Food Res. Int. 2004, 37, 517525.
(RS) are widely used in the encapsulation of various food [17] Storey, D., Lee, A., Bornet, F., Brouns, F., Gastrointestinal
components, as probiotics. A symbiotic approach is often responses following acute and medium term intake of retro-
graded resistant maltodextrins, classified as type 3 resistant
accomplished by co-encapsulation of RS in the form of starch. Eur. J. Clin. Nutr. 2007, 61, 12621270.
high-amylose maize starch together with the probiotic
[18] Mermelstein, N. H., Analyzing for resistant starch. Food
microorganisms within the microcapsule. Technol. 2009, 4, 8084.
[19] Nugent, A. P., Health properties of resistant starch. British
The authors have declared no conflict of interest. Nutrition Foundation. Nutr. Bull. 2005, 30, 2754.
[20] Kim, M. J., Choi, S. J., Shin, S. I., Sohn, M. R., et al. Resistant
8 References glutarate starch from adlay: Preparation and properties.
Carbohydr. Polym. 2008, 74, 787796.
[1] Howlett, J. (Ed.), ILSI Europe Concise Monograph Series, [21] Jiang, H., Jane, J. L., Acevedo, D., Green, A., et al. Variations
Walker, R., Brussels 2008. in starch physicochemical properties from a generation-
means analysis study using amylomaize V and VII parents.
[2] Food Quality and Standards Service (AGNS) & Food and
J. Agric. Food Chem. 2010, 58, 56335639.
Agriculture Organization of the United Nations (FAO), Report
On Functional Foods 2007, Available at: [22] Cummings, J. H., Stephen, A. M., Carbohydrate terminology
ag/agn/agns/files/Functional_Foods_Report_Nov2007.pdf. and classification. Eur. J. Clin. Nutr. 2007, 61, 518.
[3] Arvanitoyannis, I. S., Van Houwelingen-Koukaliaroglou, M., [23] Siswoyo, T. R., Morita, N., Thermal properties of partially
Functional foods: A survey of health claims, pros and cons, hydrolyzed starch-glycerophosphatidylcholine complexes
and current legislation. Crit. Rev. Food Sci. Nutr. 2005, 45, with various acyl chains. J. Agric. Food Chem. 2003, 51,
385404. 31623167.
[4] Englyst, K. N., Liu, S., Englyst, H. N., Nutritional character- [24] Frohberg, C., Quanz, M., Use of Linear Poly-Alpha-1,4-
ization and measurement of dietary carbohydrates. Eur. J. Glucans as Resistant Starch, United States Patent
Clin. Nutr. 2007, 61, 1939. Application 20080249297, 2008, Available on line at: http:// 2005040223.
[5] Yao, N., Paez, A. V., White, P. J., Structure and function of
starch and resistant starch from corn with different doses of [25] Rahmana, S., Birda, A., Reginaa, A., Lia, Z., et al. Resistant
mutant amylose-extender and floury-1 alleles. J. Agric. Food starch in cereals: Exploiting genetic engineering and genetic
Chem. 2009, 57, 20402048. variation. J. Cereal Sci. 2007, 46, 251260.
[6] Slavin, J., Stewart, M., Timm, D., Hospattankar, A., [26] Sandhu, K. S., Lim, S. T., Structural characteristics and in
International Association for Cereal Science and vitro digestibility of Mango kernel starches (Mangifera indica
Technology (ICC), 13 July 2009, van der Kamp, J. W., L.). Food Chem. 2008, 107, 9297.
Vienna, Austria 2009, p. 35.
[27] Juarez-Garcia, E., Agama-Acevedo, E., Sayago-Ayerdi, S.
[7] Lunn, J., Buttriss, J. L., 2007, Carbohydrates and dietary G., Rodriguez-Ambriz, S. L., Bello-Perez, L. A., Composition,
fibre. Nutr. Bull. 32, 2164. digestibility and application in breadmaking of banana Flvor.
Plant Foods Hum. Nutr. 2006, 61, 131137.
[8] Sharma, A., Yadav, B. S., Ritika, B. Y., Resistant starch:
Physiological roles and food applications. Food Rev. Int. [28] Kumari, M., Urooj, A., Prasad, N. N., Effect of storage on
2008, 24, 193234. resistant starch and amylose content of cerealpulse based

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

414 E. Fuentes-Zaragoza et al. Starch/Starke 2011, 63, 406415

ready-to-eat commercial products. Food Chem. 2007, 102, [46] Roberfroid, M., Prebiotics: the concept revisited. J. Nutr.
14251430. 2007, 137, (3 Suppl 2): 830S837S.
[29] Htoon, A. K., Uthayakumaran, S., Piyasiri, U., Appelqvist, I., [47] Delzenne, N. M., in: Taylor, J., Poms, R. (Eds.), Prebiotics:
et al. The effect of acid dextrinisation on enzyme-resistant New Trends and Developments. Proceedings of 4th
starch content in extruded maize starch. Food Chem. 2010, International Dietary Fibre Conference, ICC, van der
120, 140149. Kamp, J. W., Vienna, Austria 2009, p. 28.
[30] Rosell, C. M., Santos, E., Impact of fibers on physical charac- [48] Coskun, T., Pro-, pre- and synbiotics. Cocuk Sagligi Hast.
teristics of fresh and staled bake off bread. J. Food Eng. Derg. 2006, 49, 128148.
2010, 98, 273281.
[49] Leeman, A. M., Karlsson, M. E., Eliasson, A. C., Bjorck, I. M.
[31] Tan, H. Z., Li, Z. G., Tan, B., Starch noodles: History, classi- E., Resistant starch formation in temperature treated potato
fication, materials, processing, structure. Food Res. Int. starches varying in amylose/amylopectin ratio. Carbohydr.
2010, 42, 551576. Polym. 2006, 65, 306313.
[32] Liu, R., Xu, G., Effects of resistant starch on colonic preneo- [50] Scourboutakos, M., 1 1 3. Synbiotics: Combining the
plastic aberrant crypt foci in rats. Food Chem. Toxicol. 2008, power of pre- and probiotics. J. Food Sci. Educ. 2010, 9,
46, 26722679. 3637.
[33] Higgins, J. A., Higbee, D. R., Donahoo, W. T., Brown, I. L., [51] Lee, Y. K. Salminen, S. Hoboken, N. J. (Eds.), Handbook of
et al. Resistant starch consumption promotes lipid oxidation. probiotics and prebiotics, 2nd edn. John Wiley & Sons, Inc.,
Nutr. Metab. 2004, 1, 8. United Kingdom 2009.
[34] Shimada, M., Mochizuki, K., Goda, T., Dietary resistant [52] Bird, A. R., Usher, S., May, B., Topping, D. L., Morell, M. K., in:
starch reduces levels of glucose-dependent insulinotropic Cho, S. (Ed.), Proceedings of the 9th Vahouny Fiber
polypeptide mRNA along the jejunumileum in both normal Symposium, Bethesda, MD, USA 2010, p. 25.
and type 2 diabetics rats. Biosci. Biotechnol. Biochem. 2008,
72, 22062209. [53] Charalampopoulos, D., Wang, R., Pandiella, S. S., Webb, C.,
Application of cereals and cereal components in functional
[35] Hashimoto, N., Ito, Y., Han, K. H., Shimada, K., et al. Potato foods: A review. Int. J. Food Microbiol. 2002, 79, 131141.
pulps lowered the serum cholesterol and triglyceride levels in
rats. J. Nutr. Sci. Vitaminol. 2006, 52, 445450. [54] Rodrguez-Cabezas, M. E., Camuesco, D., Arribas, B.,
Garrido-Mesa, N., et al. The combination of fructooligosac-
[36] Martinez-Flores, H. E., Chang, Y. K., Martinez-Bustos, F., charides and resistant starch shows prebiotic additive effects
Sgarbierid, V., Effect of high fiber products on blood lipids in rats. Clin. Nutr. 2010, 29, 832839.
and lipoproteins in hamsters. Nutr. Res. 2004, 24, 8593.
[55] Le Blay, G. M., Michel, C. D., Blottiere, H. M., Cherbut, C. J.,
[37] Patindol, J. A., Guraya, H. S., Champagne, E. T., McClung, Raw potato starch and short-chain fructo-oligosaccharides
A. M., Nutritionally important starch fractions of rice affect the composition and metabolic activity of rat
cultivars grown in Southern United States. J. Food Sci. intestinal microbiota differently depending on the caeco-
2010, 75, 137144. colonic segment involved. J. Appl. Microbiol. 2003, 94,
[38] Kay M. Behall, K.M., Daniel J. Scholfield, D.J., Hallfrisch, 312320.
J.G., Liljeberg-Elmstahl, H.G.M., Consumption of both [56] Younes, H., Coudray, C., Bellanger, J., Demigne, C., et al.
resistant starch and b-glucan improves postprandial plasma Effects of two fermentable carbohydrates (inulin and
glucose and insulin in women. Diabetes Care 2006, 29, 976 resistant starch) and their combination on calcium and
981. magnesium balance in rats. Brit. J. Nutr. 2001, 86, 479485.
[39] Ovando-Martinez, M., Sayago-Ayerdi, S., Agama-Acevedo, [57] Iyer, C., Kailasapathy, K., Effect of co-encapsulation of
E., Goni, I., Bello-Perez, L. A., Unripe banana flour as an probiotics with prebiotics on increasing the viability of
ingredient to increase the undigestible carbohydrates of encapsulated bacteria under in vitro acidic and bile salt
pasta. Food Chem. 2009, 113, 121126. conditions and in yogurt. J. Food Sci. 2005, 70, 1823.
[40] Korus, J., Witczak, M., Ziobro, R., Juszczak, L., The impact of [58] Homayouni, A., Azizi, A., Ehsani, M. R., Yarmand, M. S.,
resistant starch on characteristics of gluten-free dough and Razavi, S. H., Effect of microencapsulation and resistant
bread, Food Hydrocolloids 2009, 23, 988995. starch on the probiotic survival and sensory properties of
[41] Ares, G., Baixauli, R., Sanz, T., Varela, P., Salvador, A., New synbiotic ice cream. Food Chem. 2008, 111, 5055.
functional fibre in milk puddings: Effect on sensory properties [59] Weinbreck, F., Bodnar, I., Marco, M. L., Can encapsulation
and consumers acceptability, LWT - Food Sci. Technol. lengthen the shelf-life of probiotic bacteria in dry products?
2009, 42, 710716.
Int. J. Food Microbiol. 2010, 136, 364367.
[42] Baixauli, R., Sanz, T., Salvador, A., Fiszman, S. M., Muffins [60] Jankowski, T., Zielinska, M., Wysakowska, A., Encapsulation
with resistant starch: Baking performance in relation to the of lactic acid bacteria with alginate/starch capsules.
rheological properties of the batter, J. Cereal Sci. 2008, 47, Biotechnol. Technol. 1997, 11, 3134.
[61] Shimoni, E., in: Garti, N. (Ed.), Starch as an encapsulation
[43] Rochfort, S., Panozzo, J., Phytochemicals for health, the role material to control digestion rate in the delivery of active food
of pulses. J. Agric. Food Chem. 2007, 55, 79817994. components. Delivery and controlled release of bioactives in
[44] Wei, C., Qin, F., Zhu, L., Zhou, W., et al. Microstructure and foods and nutraceuticals. CRC Press, Boca Raton, FL, USA
ultrastructure of high-amylose rice resistant starch granules 2008, DOI: 10.1201/9781439824207.ch11.
modified by antisense RNA inhibition of starch branching
enzyme. J. Agric. Food Chem. 2010, 58, 12241232. [62] Sultana, K., Godward, G., Reynolds, N., Arumugaswamy, R.,
et al. Encapsulation of probiotic bacteria with alginatestarch
[45] Walter, M., Picolli da Silva, L., Casagrande denardin, C., rice and evaluation of survival in simulated gastrointestinal
and resistant starch: Different content depending on chosen conditions and in yoghurt. Int. J. Food Microbiol. 2000,
methodology. J. Food Compos. Anal. 2005, 18, 279285. 62, 4755.

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

Starch/Starke 2011, 63, 406415 415

[63] Heidebach, T., Forst, P., Kulozik, U., Influence of casein- potential of dietary oligosaccharides. FEMS Microbiol. Lett.
based microencapsulation on freeze-drying and storage of 2004, 236, 153159.
probiotic cells. J. Food Eng. 2010, 98, 309316.
[69] Mandalari, G., Nueno Palop, C., Tuohy, K., Gibson, G. R., et
[64] Champ, M., Langkilde, A. M., Brouns, F., Kettlitz, B., Le Bail- al. In vitro evaluation of the prebiotic activity of a pectic
Collet, Y., Advances in dietary fibre characterisation. 2. oligosaccharide-rich extract enzymatically derived from
Consumption, chemistry, physiology and measurement of bergamot peel. Appl. Microbiol. Biotechnol. 2007, 73,
resistant starch; implications for health and food labelling. 11731179.
Nutr. Res. Rev. 2003, 16, 143161.
[70] Parkar, S. G., Redgate, E. L., Wibisono, R., Luo, X., et al. Gut
[65] Mishra, S., Monro, J., Hedderley, D., Effect of processing on health benefits of kiwifruit pectins: Comparison with commer-
slowly digestible and resistant starch. Starch/Starke 2008, cial functional polysaccharides. J. Funct. Food 2010, 2, 210
60, 500507. 218.
[66] Fuentes-Zaragoza, E., Riquelme-Navarrete, M. J., Sanchez- [71] Scott, K. P., Duncan, S. H., Flint, H. J., Dietary fibre and the
Zapata, E., Perez-Alvarez, J. A., Resistant starch as gut microbiota. Br. Nutr. Found. Nutr. Bull. 2008, 33, 201
functional ingredient: A review. Food Res. Int. 2010, 43, 211.
[72] Zhao, X. H., Lin, Y., Resistant starch prepared from high-
[67] Gomez, E., Tuohy, K. M., Gibson, G. R., Klinder, A., amylose maize starch with citric acid hydrolysis and its
Costabile, A., In vitro evaluation of the fermentation proper- simulated fermentation in vitro. Eur. Food Res. Technol.
ties and potential prebiotic activity of Agave fructans. J. Appl. 2009, 228, 10151021.
Microbiol. 2010, 108, 21142121.
[73] Brouns, F., Kettlitz, B., Arrigoni, E., Resistant starch and the
[68] Vulevic, J., Rastall, R. A., Gibson, G. R., Developing a butyrate revolution. Trends Food Sci. Technol. 2002, 13,
quantitative approach for determining the in vitro prebiotic 251261.

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