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The link between carbohydrate intake and health is becoming increasingly important for consumers, particularly in the areas of glycemic index (GI) and extended energy-releasing starches. From a physiological point of view, slowly digestible starch (SDS) delivers a slow and sustained release of blood glucose along with the benefits resulting from low glycemic and insulinemic response. SDS has been implicated in several health problems, including diabetes, obesity, and cardiovascular diseases (metabolic syndromes). It may also have commercial potential as a novel functional ingredient in a variety of fields, such as nutrition, medicine, and agriculture. The present review assesses this form of digestion by analyzing methods to prepare and evaluate SDS, factors affecting its transformation, its health benefits, and its applications.
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Slowly Digestible Starch—A Review
Ming Miaoab, Bo Jiangab, Steve W. Cuiab, Tao Zhangab & Zhengyu Jinab
a State Key Laboratory of Food Science & TechnologyJiangnan University, Wuxi, Jiangsu
Province, P.R. China
b Synergetic Innovation Center of Food Safety and NutritionJiangnan University, Wuxi,
Jiangsu Province, P.R. China
Accepted author version posted online: 23 Oct 2013.
To cite this article: Ming Miao, Bo Jiang, Steve W. Cui, Tao Zhang & Zhengyu Jin (2015) Slowly Digestible Starch—A Review,
Critical Reviews in Food Science and Nutrition, 55:12, 1642-1657, DOI: 10.1080/10408398.2012.704434
To link to this article: http://dx.doi.org/10.1080/10408398.2012.704434
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Critical Reviews in Food Science and Nutrition, 55:1642–1657 (2015)
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ISSN: 1040-8398 / 1549-7852 online
DOI: 10.1080/10408398.2012.704434
Slowly Digestible Starch—A Review
MING MIAO,1,2 BO JIANG,1,2 STEVE W. CUI,1,2 TAO ZHANG,1,2 and ZHENGYU
JIN1,2
1State Key Laboratory of Food Science & Technology, Jiangnan University, Wuxi, Jiangsu Province, P.R. China
2Synergetic Innovation Center of Food Safety and Nutrition, Jiangnan University, Wuxi, Jiangsu Province, P.R. China
The link between carbohydrate intake and health is becoming increasingly important for consumers, particularly in the
areas of glycemic index (GI) and extended energy-releasing starches. From a physiological point of view, slowly digestible
starch (SDS) delivers a slow and sustained release of blood glucose along with the benefits resulting from low glycemic and
insulinemic response. SDS has been implicated in several health problems, including diabetes, obesity, and cardiovascular
diseases (metabolic syndromes). It may also have commercial potential as a novel functional ingredient in a variety of fields,
such as nutrition, medicine, and agriculture. The present review assesses this form of digestion by analyzing methods to
prepare and evaluate SDS, and factors affecting its transformation, its health benefits, and its applications.
Keywords Slowly digestible starch, structure, digestibility, glycemic response, health claim
INTRODUCTION
In human nutrition, starch plays a major role in supplying
metabolic energy, which enables the body to perform a multi-
tude of functions. Based on the rate and extent of digestibil-
ity, starches have been classified into rapidly digestible starch
(RDS), slowly digestible starch (SDS), and resistant starch (RS)
(Englyst et al., 1992; Englyst and Englyst, 2005). Starch can
be quantified into different fractions using the in vitro Englyst
assay: the starch fraction digested within 20 minutes of incuba-
tion is classified as RDS, the starch fraction digested between
20 and 120 minutes corresponds to SDS, and the remaining
fraction that is not further digested is RS (Fig. 1a). RDS induces
a fast increase in blood glucose and insulin levels, which can
induce a series of health complications, such as diabetes and
cardiovascular diseases. SDS is slowly digested throughout the
small intestine, resulting in a slow and prolonged release of glu-
cose into the blood stream, coupled to a low glycemic response.
This starch type may be helpful in controlling and preventing
hyperglycemia-related diseases. Moreover, RS is the starch por-
tion that cannot be digested in the small intestine, but instead
is fermented in the colon as dietary fiber, which may prevent
disease and lead to better colonic health (Fig. 1b) (Englyst et al.,
1992; Bjrck et al., 2000; Ells et al., 2005; Aston, 2006).
Obesity and diabetes have become major public health con-
cerns worldwide, with the number of cases increasing expo-
Address correspondence to Ming Miao, State Key Laboratory of Food Sci-
ence and Technology, Jiangnan University, 1800 Lihu Avenue, Wuxi, Jiangsu
Province 214122, P.R. China. E-mail: miaoming@jiangnan.edu.cn
nentially in recent years (FAO/WHO, 2002). The multifactorial
etiology of this worldwide epidemic, and the idea that diet may
contribute to it, is now well recognized. New developments in
food and nutritional science have led to the conclusion that
slowing down the rate of digestion of glucose from ingested
carbohydrate sources helps to blunt glycemia, reduces insulin
requirements, and causes satiety (FAO/WHO, 1997). The food
industry has been developing a new, slowly digestible carbo-
hydrate (SDC) (Thorburn et al., 1987; Bjrck and Asp, 1994;
Wrsch, 1994; Wolf et al., 2003). Some examples of commer-
cially available products include isomaltulose, trehalose, oligo-
alternan, pullulans, sucromalt, as well as other slowly digestible
syrups. All of these products claim to have a slow and extended
postprandial level of glucose after intake, although they differ
in molecular structure, functional properties, and potential ap-
plication in conjunction with SDS (Wrsch, 1994; Asp, 1995;
Heymann et al., 1995; Scheppach et al., 2001; Sparti et al.,
2002; Wolf et al., 2003). The present review focuses on SDS as
an SDC and analyzes its digestibility, preparation, physiological
effects, and potential application.
DIGESTION OF SDS
Starch digestion and absorption consists of essentially three
phases: the intraluminal phase, the brush border phase, and the
glucose absorption phase. Starch is ingested, then enzymati-
cally hydrolyzed, and finally absorbed as glucose for energy
metabolism within the upper gastrointestinal tract.
1642
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SLOWLY DIGESTIBLE STARCH 1643
Figure 1 Classification of the bioavailability of nutritional starch fractions.
(a) In vitro digestion using the Englyst assay, and (b) in vivo glycemic response
to RDS, SDS, and RS.
Unlike most starch components, molecules of SDS are
not disrupted in the oral cavity by salivary α-amylase, in the
stomach lining by gastric acid, or through the vigorous grinding
action resulting from gastric motility. The process of digestion
is initiated after acidic chyme moves into the small intestine
through gastric emptying, and most digestion of SDS occurs
in the duodenum. SDS is hydrolyzed by enzymes secreted
from the pancreas and is converted into small linear oligomers
and α-limit dextrins. These amylolytic degradation products
from SDS, made up predominantly of disaccharides (maltose),
diffuse from the lumen into the brush border membrane, where
the final digestion to glucose occurs through the action of the
mucosal enzyme complexes containing sucrase-isomaltase (SI)
and maltase-glucoamylase (MGAM) (Heymann et al., 1995;
Breitmeier et al., 1997). Quezada-Calvillo et al. reported
that MGAM and SI account for more than 85% of starch
α-glucogenesis, while α-amylase serves only as an amplifier of
mucosal starch digestion. MGAM has a higher α-glucogenic
activity than SI, but it is inhibited by mealtime concentrations
of luminal maltodextrins (Quezada-Calvillo et al., 2007a;
Quezada-Calvillo et al., 2007b). In this way, MGAM regulates
the total rate of starch α-glucogenesis. Compared to the N-
terminal subunit of MGAM, the C-terminal subunit of MGAM
has greater catalytic efficiency due to its higher affinity for
glucan substrates and larger number of binding configurations
at the active site (Quezada-Calvillo et al., 2008). Ao et al.
have also shown that hydrolysis by pancreatic α-amylase is
not required in order for the N-terminal subunit of MGAM
to degrade native starch granules in the human small intestine
(Ao et al., 2007a). In summary, SDS is degraded primarily by
recombinant human enzymes: α-glucosidases, including small
intestinal MGAM; SI; and pancreatic α-amylase.
ANALYTICAL METHODS FOR SDS DIGESTION
In order to monitor the rate and extent of starch digestion
or the intestinal absorption of starch-derived glucose, several
available methods are available, and they vary in their degree of
invasiveness and accuracy.
In vitro Approaches
Measuring Nutritional Starch Fractions
The method most widely used to quantify nutritionally im-
portant starch fractions was developed by Englyst et al. (1992),
and it involves stimulation of the human digestion system. In
this procedure, the various types of starch constituents are de-
termined by controlled enzymatic hydrolysis with pancreatic
amylase and amyloglucosidase at 37C and the released glu-
cose is measured using glucose oxidase. SDS is calculated by
subtracting the amount of glucose hydrolyzed after 120 minutes
from the amount of glucose hydrolyzed after 20 minutes. This
technique yields values for rapidly available glucose (RAG) and
slowly available glucose (SAG), thereby providing a description
of the rate of glucose release from the food being tested (Englyst
et al., 1996).
A novel method from The Netherlands Organization for Ap-
plied Science Research (TNO) made two major improvements
to the Englyst test: a mixture of microbial enzymes and anal-
ysis of the amount of glucose released at specific time points.
One study comparing various pure carbohydrates to different
kinds of carbohydrate-containing food products showed that
the GI values obtained with the TNO method correspond well
with results obtained from human studies (Sanders et al., 2007).
Guraya et al. reported that the digestibility of SDS can be deter-
mined by measuring the rate of starch hydrolysis due to porcine
α-amylase (Guraya et al., 2001a, 2001b). The hydrolysate (mal-
tose) can be measured using the colorimetric dinitrosalicylic
acid (DNS) method. In this approach, SDS is calculated as fol-
lows: SDS% =(BA)/C×100, where Ais the mg of maltose
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1644 M. MIAO ET AL.
produced upon digestion of starch after one hour has passed; B
is the maximum mg of maltose produced after a certain time,
with no further increase in maltose observed; and Cis the to-
tal starch expressed in mg of maltose. Other investigators have
attempted to improve the Guraya procedure and confirmed the
maximum mg of maltose produced after 10 hours (Shin et al.,
2004). Few comparisons have been performed using the same
samples. However, only the method of Englyst has been vali-
dated using in vivo data and there are some drawbacks to this
authoritative method. These include its troublesome demand for
a wide variety of substrates, its lengthy procedure and poor re-
producibility when the technician is not extensively trained, its
requirement for specific equipment, and the fact that some of
the enzymes needed are not commercially available.
Measuring Viscosity
Various researchers have shown that changes in starch vis-
cosity affect its digestibility. The controlled stress rheometers, a
commercially available concentric cylinder viscometer, provide
a sensitive indicator of the extent of dissolution of starch gran-
ules and of their subsequent enzymatic hydrolysis (Dickinson
et al., 1982). Gee and Johnson have shown that viscosity de-
clines over the course of a simulated digestion and that relative
viscosity values can predict to what extent intact foods raise the
viscosity of partially digested gut contents (Gee and Johnson,
1985). The viscosity is inversely related to the digestibility of
the partial α-amylase–treated maize starch, which can function
as SDS and RS consistent with its low GI (Han et al., 2006). Ac-
cording to the studies of Han and Hamaker as well as the work of
Benmoussa et al., the extent of breakdown of swollen granules
and the viscosity after gelatinized starch granule structure de-
pends on how much amylopectin fine structure have disrupted
(Han and Hamaker, 2001; Benmoussa et al., 2007). In those
studies, breakdown viscosity was found to correlate negatively
with SDS based on Rapid Visco Analyser (RVA) profiles. In-
deed, RVA method may serve as a tool for screening the slow
digestion properties of different starches. Zhang et al. reported
that a viscosity-based screening method based on RVA profiles
can be used to assess the properties of SDS obtained from ge-
netic mutants of maize (Zhang et al., 2008).
Other Methods for Measuring Digestion Rate
Granfeldt et al. introduced a method for measuring the rate
of in vitro starch digestion in products that is based on a pe-
culiar “as eaten” (chewing/dialysis test) structure, which shows
promise for predicting the metabolic behavior of starchy foods
(Granfeldt et al., 1992). In this method, the test starch substrate
is chewed under standardized conditions, and then incubated
with the proteolytic enzyme pepsin. Subsequently, the mixture
is transferred to dialysis tubing and incubated with pancreatic α-
amylase for three hours. Aliquots of the dialysate are collected at
different times, and the degree of hydrolysis is calculated as the
proportion of potentially available starch degraded to maltose.
The hydrolysis index (HI) is calculated as the area under the hy-
drolysis curve (0–180 minutes) with the product as a percentage
of the corresponding area with white wheat bread, chewed by
the same person (Granfeldt et al., 1992; Åkerberg et al., 1998).
Starch hydrolysis kinetic curves follow a first-order equation
C=C(1ekt), where Cis the quantity of ingested starch di-
gested at time t,Cis the potentially digestible starch fraction
(less than 100), kis the fractional starch digestion rate, and tis
the chosen time. Weurding et al. stated that the kof SDS among
feedstuffs, during a study of starch digestive behavior in the
small intestines of broiler chickens, was less than 1 h1in an in
vitro test (Weurding et al., 2001a, 2001b). Wen et al. published
a method for measuring total carbohydrate digestion rate (Wen
et al., 1996). It involves homogenizing the starch samples with
water, transferring them to a dialysis bag, and incubating with
salivary α-amylase for various times. Maltose concentration is
determined using a standard curve of maltose content versus ab-
sorbance (the Somogyi–Nelson method), and the carbohydrate
digestion rate is determined as: rate (mg/g1/h1)=x/[w·(1m)·t],
where xis the carbohydrate amount in the diluted dialysate by
reference to the standard curve, wis the weight of sample, m
is the moisture of the starch, and tis the reaction time. These
methods have been used to provide the in vitro values for some
starchy foods, but not for SDS, which may need to be confirmed
in the future.
In vivo Approaches
Glycemic Index (GI)
The concept of GI was introduced by Jenkins et al. in an
attempt to classify carbohydrate-based foods according to the
postprandial glucose responses that they elicit (Jenkins et al.,
1981). The GI is defined as the incremental area under the
blood sugar response curve (the change in blood glucose level
two hours after a meal) of 50 g available carbohydrate portion of
a test food expressed as percentage of the response to the same
amount of carbohydrate from a standard food (either white bread
or glucose) ingested by the same subject (Wolever et al., 1991;
FAO/WHO, 1997). The related term of glycemic load (GL) has
been proposed to take into account differences in carbohydrate
content among foods, meals, or diets (Salmern et al., 1997a;
Salmern et al., 1997b). GL is calculated by multiplying the GI
of a food by the amount of total dietary carbohydrate per serv-
ing and it therefore serves as an indicator of the ability of the
carbohydrate to raise blood glucose levels or global dietary in-
sulin demand. A food-based “GI,” the relative glycemic potency
(RGP), has recently been proposed to overcome the limitations
of GI and is defined as the theoretical glycemic response to
50 g of a food, expressed as a percentage of the response to
50 g of glucose (Monro, 2002). In addition, the glycemic glu-
cose equivalent (GGE), defined as the weight of glucose with
the same glycemic impact as a given weight of food, has been
proposed as a practical measure of relative glycemic impact
(Monro, 2002; Liu et al., 2003).
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SLOWLY DIGESTIBLE STARCH 1645
Given the glycemic response to SDS, which shows a de-
layed appearance of the blood glucose peak and a prolonged,
moderate elevation of glucose after the peak, the extended
glycemic index (EGI) has been proposed to measure the slow
digestion of starchy foods in vivo on an extended time scale (He
et al., 2008). In addition, the equation introduced by Granfeldt
and Go˜
ni et al. has been used to predict the GI from the HI: GI =
0.862 ×(HI) +8.198 and GI =0.549 ×(HI) +39.71, respec-
tively (Granfeldt et al., 1994; Goi et al., 1997). HI and GI corre-
late significantly in cereal and legume products (Granfeldt et al.,
1992). Data from the hydrolysis of novel starch products in vitro
are useful in predicting glycemic responses in vivo (Seal et al.,
2003). Englyst et al. demonstrated that the relationship between
RAG and glycemic response is significantly positive, and that
RAG accounts for 70% of the remaining variance in glycemic
response (Englyst et al., 1999, 2003). However, the combina-
tion of SAG and fat accounts for 73.1% of the variance in GI,
with SAG as the dominant variable. Using a plain sweet biscuit,
Garsetti et al. observed a similar relationship between starch di-
gestibility in vitro and responses in vivo (Garsetti et al., 2005).
Insulin Index (II)
Insulin secretion is largely assumed to be proportional to
postprandial plasma glucose responses. Cumulative changes in
insulin responses for food are quantified as the incremental area
under the 120 minutes response curve; the incremental area is
calculated using the trapezoidal rule, with fasting concentrations
taken as the baseline and truncated at zero (Holt et al., 1997).
The insulin index (II) has been suggested as a concept for dietary
management of people with diabetes. The calculated equation of
II is similar to the equation developed by Jenkins for calculating
GI values. Using the in vitro method, Granfeldt et al. showed
a significant correlation between HI and II (Granfeldt et al.,
1992). In cereal products, the combination of RAG and protein
contribute equally to account for 45.0% of the variance in II
(Englyst et al., 2003).
FACTORS INFLUENCING THE FORMATION OF SDS
Starch Structure
Starch is a semicrystalline material synthesized as roughly
spherical granules in plant tissues. These granules consist of
alternating concentric layers of ordered and dense crystalline
and less-ordered amorphous regions (lamellas) extending from
the hilum to the surface of the granules. The crystalline re-
gions are formed from the short-branch chains of amylopectin
molecules arranged in clusters; these crystalline regions are in-
terspersed with amorphous regions that constitute branching
points of amylopectin and amylose. The sub-chains of the amy-
lopectin molecules can be classified into three types according
to their length and branching points (Fig. 2). The shortest A
chains, for which the degree of polymerization (DP)is615,
have no branching points as “outer” chains. The B chains are
branched by A chains or other B chains (e.g. B1, B2, and B3,
depending on their respective length and the number of clusters
they span). There is only one C chain per amylopectin molecule,
which is identifiable because it contains a single reducing ter-
minal. Within this structure, the branch-points are located in the
region of low molecular order, and the linear chains lie within
the region of high molecular order. These linear chains can then
form double helices to make up the crystal structure. On the
basis of wide-angle X-ray diffraction scattering studies, native
starch is classified into A, B, C, and V types (Fig. 3). The A
type is characteristic of most starches of cereal origin, while the
B type is typically found in potatoes, other root starches, amy-
lomaize starches, and retrograded starch. The C type, which is a
combination of the A and B types, is commonly found in smooth
pea and various bean starches. The V type can be found only in
amylose helical complex starches after starch gelatinization and
the formation of complexes with lipids or related compounds.
Using the Englyst method, Zhang et al. showed that native
cereal starch is an ideal SDS, since its structure causes them to
be digested slowly (Zhang et al., 2006a, 2006b). They found that
the semicrystalline A-type structure of native cereal starches, in-
cluding the distribution and perfect crystalline regions in both
crystalline and amorphous lamellae explains this slow diges-
tion. The high proportion of SDS in cereal starches was also
found to correlate with a higher fraction of short A chains with
DP 5–10. The mechanism of slow digestion of native cereal
starch involves digestion from inside out and layer-by-layer:
enzymatic digestion begins at the surface pores and interior
channels, and then side-by-side digestion gradually enlarges the
channel by simultaneously digesting crystalline and amorphous
regions. Native starch is digested more slowly than processed
(gelatinized) starch; the latter has lost its crystalline structure,
allowing greater accessibility to enzymes without the obstruc-
tions caused by α-glucan associations, such as double helices
(especially in crystallites), or by amylose-lipid complexes in
cereal starches (Tester et al., 2002). Hamaker et al. and Zhang
et al. reported that dispersed, amylopectin fine structures with
high branching density, either long or short internal chains as
well as shortened terminal nonreducing ends, lead to slow diges-
tion, which is the chemical entity that is responsible for a slow
digestion property because of the inherent molecular structure
of amylopectin (Hamaker et al., 2007; Zhang et al., 2008). In an
in vivo study by Seal et al. (2003), the plasma glucose response
after consuming raw maize starch is slow and sustained, which
is a characteristic of a typical glycemic response curve of SDS.
The structure of SDS may consist of imperfect crystallites and
amylopectin with a high branching density and pattern, and this
is most likely the cause of the slow digestion.
Heat and Moisture
Heat and water content are important factors in the formation
of SDS. When native starches are heated in excess water,
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1646 M. MIAO ET AL.
Figure 2 Schematic models of the subchains within an amylopectin molecule as proposed by (a) French (1972), (b) Hizukuri (1986), and (c) Robin et al. (1974)
(Reproduced with permission). ø, reducing end; CL, chain length; A chain, outer chain; B1, B2, and B3 chains, inner chains; C chain, backbone chain; 1, crystalline
region or high molecular order; and 2, amorphous region or low molecular order.
the granules undergo a characteristic structural reorganization
(gelatinization). The extent of gelatinization depends on the
water content, temperature, time, and degree of shear during
the process. As previously described, native starch (especially
Figure 3 X-ray diffraction diagram of different starches (Zobel, 1988)
(Reproduced with permission).
A-type) is an ideal SDS, and the slow digestibility of starch
changes in cooked or processed starchy food. Incomplete gela-
tinization can be achieved by lowering the heating temperature,
decreasing the water content, or shortening the processing time
of the starch. In this way, some of the nutritional and low-GI
benefits of SDS may be retained. Chung et al. reported that when
partially gelatinized waxy rice starch pastes, containing 5%
starch on a dry weight basis, are heated at different temperatures
(60, 65, or 70C for 5 minutes), they show different digestion
rates after retrogradation (Chung et al., 2006). The amounts
of SDS and RS positively correlate with the relative melting
enthalpy of the partially gelatinized starch samples. In cereal
products, such as barley porridges, parboiled rice, biscuits, and
pasta, the degree of gelatinization or limited-swelling starch,
which is determined mainly by the moisture level, cooking
time, and temperature, influences the formation of SDS and
moderates glycemic response (Wolever et al., 1986a, 1986b;
Holm et al., 1992; Granfeldt et al., 1994; Garsetti et al., 2005).
Heat-moisture as one of the hydrothermal treatments usually
refers to the incubation of starch granules at low moisture levels
(<35% w/w) for a certain period of time at a temperature above
the glass transition temperature, but below the gelatinization
temperature. At the same time, annealing is performed in excess
water or at an intermediate water content (40% w/w) (Jacobs
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SLOWLY DIGESTIBLE STARCH 1647
and Delcour, 1998; Tester and Debon, 2000). Heat–moisture
treatment does not destroy granule structure, but it alters
the crystalline packing of starch; for example, the B type of
potato starch can be converted to the A or C type, whereas the
annealing processes modify the binding forces between the
crystallites and the amorphous matrix (Stute, 1992). Therefore,
hydrothermal treatment can be used as a method to form SDS.
Anderson et al. adjusted nonwaxy and waxy rice starches
to 20% moisture (wet basis), heated them to their melting
temperature (Tm) in a differential scanning calorimeter, and
held them there for 60 minutes (Anderson et al., 2002). They
found that the starches were digested more slowly than unheated
samples. Moreover, microwave heating produces only minimal
changes in digestibility, even though it causes a re-association
of amylopectin branch chains (Anderson and Guraya, 2006).
Severijnen et al. used these principles to study the production
of a sterilized liquid product with a low GI (Severijnen et al.,
2007). When the modified high amylose starch is heated above
120C for—four to five minutes, the SDS proportion increases
and reaches a maximum, where it remains for at least several
months when stored at 4C. According to a patent of Woortman
and Steeneken (2004), high SDS content can be achieved when
producing a gellable starch product by heating starch with an
amylose content below 50% to at least 170C under mildly
acidic conditions, and then rapidly cooling it.
Interactions of Starch with Other Components
Interactions of starch with different components present in
the food system are known to influence the formation of SDS
or SDS-state food; the latter refers to the form of food in which
starch is slowly digested. The two most important forms of
starch interaction with other constituents involve formation
of starch–protein interactions and starch–lipid complexes.
Starch–protein interaction in the protein matrix is thought to
reduce the rate of α-amylolysis in cereal and legume products
(Wrsch et al., 1986; Jenkins et al., 1987; Colonna et al., 1990;
Biliaderis, 1991). According to Colonna et al. (1990) and Gran-
feldt and Bj¨
orck (1991), a viscoelastic and dense gluten network
surrounds the starch granules in pasta products and reduces the
access of amylases to the starch, and it also restricts the swelling
and leaching of starch during boiling. In cooked sorghum por-
ridge, encapsulation of starch in sheet-like and web-like protein
structures reduces the access of degrading enzymes to the starch.
This explains the lower starch digestibility and slower kinetics
of digestion (Bugusu, 2003). The interaction between starch
and protein also limits the availability of the starch in white
bread made from regular flour, while gluten-free bread elicits a
higher glycemic and insulinemic response (Jenkins et al., 1987).
In a study by Holm et al. (Holm et al., 1983), amylose in
starch molecules forms complexes with lysolecithin, and these
complexes are degraded slowly and are completely absorbed in
the gastrointestinal tract of rats within 120 minutes. As a result,
they produce lower plasma glucose and liver glycogen than
does free amylose. Murray et al. evaluated apparent digestibility
in ileal-cannulated dogs that were fed enteral diets containing
a debranched amylopectin-lipid complex (V-complex) or RS
(Murray et al., 1998). They found that the ileal and total tract
digestibilities of carbohydrate for the control, V-complex, and
RS diets were 89, 76, and 43%, respectively, which indicates
that consuming a diet containing V-complex diet lowers the
carbohydrate digestibility and, subsequently, the serum glucose
and insulin responses.
In addition to interactions with protein and lipid, starch may
also interact with soluble fibers (guar gum, psyllium, β-glucans,
or pectin), antinutrients (enzyme inhibitors, tannins, phytates,
saponins, or lectins), sugars, and organic acids (Biliaderis, 1991;
Bjrck et al., 2000; Pi-Sunyer, 2002). Brennan et al. reported
that the rate of starch hydrolysis slows significantly when the
starch granules and surrounding bread matrix are coated with
a layer of galactomannan mucilage, which acts as a physical
barrier to amylase–starch interactions and subsequent release of
hydrolyzed products (Brennan et al., 1996). In addition to its
effect on digesta viscosity, guar gum may significantly reduce
the rise in postprandial glycemic response that results from the
reduction in the rate of gastric emptying. Starch blockers (α-
amylase inhibitors) may inhibit in vitro α-amylase activity or
may bind to starch substrate, indicating that these substances
have the potential to interfere with starch digestion in vivo and
thereby modulate the glycemic effect of SDS (Giri and Kachole,
1998; Obiro et al., 2008).
Processing Conditions
Processing techniques may affect both postprocessing/
cooking processes and storage conditions (retrogradation), in-
fluencing SDS formation in food, i.e. the formation of SDS-state
foods. This fact is of great importance for the food industry,
since it offers the possibility of increasing the SDS content of
processed food and foodstuffs, such as the use of whole grains in
bread or paste, wherein the cellular layers surrounding the starch
granules are intact and present an organized food form to phys-
ical hindrance of enzyme accessibility. Autoclaving, baking,
pressure-cooking, flaking, and parboiling, among other meth-
ods, are known to influence starch digestibility and the yield of
SDS (Brand et al., 1985; Holm et al., 1985; Casiraghi et al.,
1993; Kingman and Englyst, 1994). Holm et al. demonstrated
that starch in flaked whole-grain wheat is less available than that
in boiled, popped, and steam-cooked wheat in an in vitro assay
using pepsin and pancreatic α-amylase (Holm et al., 1985).
This starch elicited lower plasma glucose and plasma insulin in
vivo. In a study of Casiraghi et al. (1993), both parboiled and
quick-cooking parboiled rice are digested more slowly with a
lower GI than polished rice, which has a starch availability for
α-amylase similar to that of white bread. Autoclaving of red kid-
ney beans was shown to increase the metabolic response (blood
glucose and insulin levels) compared to boiling at atmospheric
pressure, and this result may be due in part to the thermal or
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1648 M. MIAO ET AL.
mechanical alteration of the botanical structure of the seeds and
also to the release of physically inaccessible starch as a result
of the mechanical disruption of cell walls (Tovar et al., 1992;
Tovar et al., 1992). Granfeldt et al. reported that thick rolled
oats cause lower metabolic responses than reference bread or
thin flakes (Granfeldt et al., 2000). Boiling and pressure- cook-
ing significantly decrease the levels of SDS in three varieties
of rice (Doongara, Inga, and Japonica) and the amylose con-
tent affects starch digestibility, which has been attributed to the
process of retrogradation (Sagum and Arcot, 2000).
According to Guraya et al. (2001a), when 10% nonwaxy and
waxy starch suspensions are debranched with pullulanase, fol-
lowed by heating, cooling to allow crystallization or gelling, and
then stirred, the digestibility decreases after cooling, because of
the prevention or slowing of the formation of crystalline struc-
tures or double helices. Freezing of debranched, cooled waxy
and nonwaxy starch does not affect this decrease in digestibility.
During pullulanase debranching and retrogradation treatment of
the cooked waxy maize starch suspensions, short-term retrogra-
dation occurs as a result of the gelation and crystallization of the
amylose fraction, leading to maximum SDS formation; in con-
trast, long-term retrogradation due to the amylopectin fraction
occurs during storage of starch gels (Miao et al., 2009). Chung
et al. showed that the retrogradation changes the enzymatic di-
gestion behavior of the waxy rice starch samples, leading to
significant changes during the initial stages of digestion (Chung
et al., 2006).
PREPARATION OF SDS
For starchy products with high SDS, structural modification
of starch molecules (double helical structures and crystallites)
can be achieved using physical, enzymatic, chemical, genetic,
or multiple methods.
Physical Modification
Physical treatments for preparation of SDS include hy-
drothermal treatment, recrystallization, polymer-entrapment,
and extrusion. Shin et al. reported that when granular sweet
potato starch with 50% moisture content is heated to 55C, the
amount of heat-stable SDS relative to that of raw starch in-
creases by 200% (Shin et al., 2005). Hydrothermal treatment of
granular sweet potato starch alters its structure from Cbtype to
A-type as a result of the starch crystallites melting and subse-
quent recrystallization. This structure change reduces the rela-
tive crystallinity and converts a fraction of amorphous amylose
into the crystalline form, thereby increasing enzyme suscepti-
bility. According to Guraya et al. (2001b), the maximum SDS
(44%) is produced using higher enzyme concentration, shorter
debranching time, and rapid cooling and storage at 1C. This
process favors the nucleation step of crystallization and the for-
mation of SDS, while higher temperature favors the propagation
and maturation of crystals, resulting in RS formation. Shin et al.
observed a similar result in the storage of waxy sorghum starch
that had been debranched with isoamylase (Shin et al., 2004).
The SDS contained optimum product at a level of 27% after
isoamylase treatment for eight hours and storage at 1Cfor
three days. The resulting SDS fraction may consist primarily of
amorphous regions and a small portion of imperfect crystallites.
Miao et al. showed that controlled retrogradation with partially
debranched waxy maize starch can be used to make SDS, which
occurs upon the formation of imperfect, low-density B-type
crystallites (Miao et al., 2009). Debranching treatment of waxy
starches forms a great number of short chains available for chain
re-alignment and cross-linking, and it favors the formation of
double helices that aggregate into ordered crystalline structures
via hydrogen bonding and/or hydrophobic interactions during
cooling, leading to the formation of more SDS. Similarly, SDS
can be obtained through storage of cooked-debranched starch,
and subjecting the starch samples to additional hydrothermal
treatment increases the amount of boiling-stable SDS (Jiang
et al., 2008). Recent studies have shown that retrogradation
correlates with the SDS content of mutant maize; this maize
has a higher proportion of long amylopectin chains and linear
branched chains of amylopectin with DP 9–30. This type of
amylopectin molecule probably acts as an anchor point to slow
the digestion of branched-chain fractions with DP >30, which
as physical entities are the primary constituent of the slowly
digestible portion of the starch (Zhang et al., 2008). Abrahamse
et al. developed a sterilized food product containing a high level
of SDS by melting amylose and then rapidly cooling before
storing or drying it (Abrahamse et al., 2008).
Using entrapment or encapsulation of the starch in the struc-
tured protein network of noodles to reduce digestibility, Venkat-
achalam and Hamaker showed that biopolymer-entrapped starch
microspheres can be used as novel SDC ingredients that lead
to a moderate and extended glycemic response (Venkatachalam
and Hamaker, 2006). Starch-encapsulated spheres with a max-
imum SDS concentration of 44% were prepared by dropping
a homogeneous mixture of 1% (w/w) sodium alginate and 5 g
of starch into a 2% (w/v) CaCl2solution. This technology was
patented by Hamaker et al. (2007), who used it to create starch
entrapped in biopolymer matrix compositions, which provides
boiling-stable, SDS that can serve as a source of fermentable di-
etary fiber with health benefits. Factors such as biopolymer type
and concentration, as well as microsphere size and starch type,
have been manipulated to obtain defined amounts of SDS rang-
ing from 23 to 50%. An SDS product can be generated by using
partially gelatinized or partially plasticized materials to form a
low-swelling network linking mixed crystallites consisting of
short-chain amylose (DP <300) and basic starch. This network
can be formed through cooking or mixing processes, especially
extrusion (Innereber and Mueller, 2005). In addition, according
to the patent of Winowiski et al. (2005), SDS can be gener-
ated in feed by adding a reducing carbohydrate to comminuted
cereal grain, heating the mixture, then drying. In other words,
physical modifications of the starch structure that affect enzyme
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SLOWLY DIGESTIBLE STARCH 1649
binding and the rate of digestion can be used to modulate starch
digestibility and form SDS.
Enzymatic Modification
Controlled enzymatic treatment of starch with pullulanase,
isoamylase, α-amylase, β-amylase, or transglucosidase is an
alternative approach to changing the chain-length of starch
supramolecular structure in order to achieve appropriate
digestibility and glycemic response. According to a disclosed
patent of Shi et al. (2003), a SDS can be prepared by de-
branching amylose-containing starches using pullulanase or
isoamylase. In the case of waxy starches, higher concentrations
of debranching enzyme and shorter debranching time are more
suitable for debranching starch to form SDS (Guraya et al.,
2001b). According to Han et al. (2006), a low GI maize starch
with some branched structure can be developed by partial
α-amylase treatment and retrogradation, since slow digestibility
was retained after cooking. Short chains of amylopectin and
noncrystalline amylose are rapidly digested, while DPn121
chains show the greatest resistance to digestion, followed by
DPn46 chains. A similar trend was reported in the formation
of SDS from native and commercial starches by controlling the
hydrolysis of gelatinized starch with α-amylase (Hamaker and
Han, 2006). Recently, van der Maarel et al. filed a patent for
“novel slowly digestible storage carbohydrate,” which is pro-
duced by treating a native root or tuber starch, comprising more
than 90% amylopectin, with a branching enzyme derived from
a microorganism with a branching degree of at least 8.5–9%
(van der Maarel et al., 2008). Daniel and Marie-Helene showed
that soluble, highly branched glucose polymers containing a
larger proportion of α-1,6 glucoside linkages, produced using a
branching enzyme, are an SDS-state food that can regulate di-
gestion (Daniel and Marie-Helene, 2005). Ao et al. reported that
both the increase in branch density and the crystalline structure
of starch enhance its slow digestibility through the partial short-
ening of amylopectin A and B1 chains (exterior chains), as well
as linear chains of amylose, through the action of β-amylase
and maltogenic α-amylase (Ao et al., 2007b). This correlates
closely with an increase in the number of α-1, 6 linkages and a
decrease in the number of α-1, 4 linkages. The enzyme-treated
starch contains B- and V-type crystalline structures, which
increase the resistance of the starch to digestion. These studies
suggest that enzymatic debranching of the exterior chain length
of amylopectin in order to change its molecular structure can
form starch with higher proportions of SDS.
Chemical Modification
In many processes, starch is modified by chemical methods to
improve functionality and create commercially valuable, starch-
based products. The most common chemical modification pro-
cesses are acid treatment, cross-linking, oxidation, and substi-
tution, including esterification and etherification. Some studies
have focused on such treatments in SDS production. In the patent
of Ian et al. (2006), a chemically modified starch is achieved us-
ing propylene oxidation, acetylation, octenyl succinic anhydride
(OSA) modification, phosphorylation, dextrinization, or combi-
nations of such treatments to yield less than 25% blood glucose
at 20 minutes and 30–70% at 120 minutes after ingestion, in-
dicating controlled glucose release over an extended period of
time and more constant glucose levels. Wolf et al. reported an ef-
fect of chemical modification on the rate and extent of digestion
of common starch (27% amylose), waxy and dull waxy starch
(0% amylose), and a high-amylose variety (50% amylose) (Wolf
et al., 1999). The extent of starch digestion was significantly re-
duced using dextrinization, etherification, and oxidation, except
for cross-linking, whereas the rate of starch digestion was not
markedly affected by any chemical modifications. These chemi-
cal modifications generated RS rather than SDS, and increasing
the degree of modification decreased the extent of digestion.
According to Shin et al. (2007), the optimal condition for using
citric acid treatment to produce rice starch enriched in heat-
stable SDS (54.1%) is to add 2.62 mmol of citric acid to 20 g of
starch, which is then incubated at 128.4C for 13.8 hours. Ester-
ification with OSA has been shown to be the most potent method
of modifying waxy starch to form SDS, followed by combined
modifications (crosslinking-hydroxypropylation or acetylation)
and crosslinking (Han and BeMiller, 2007). Based on the results
of Wolf et al. (2001), OSA-modified starch shows markedly low
glycemic response during human trials, consistent with the ex-
tended glucose release profile of SDS. Dry heating (130C) of
OSA-starch increases the SDS content and decreases the RS
content, which consistent with the results of acid-treated rice
starch cooking reported by Shin et al. (2007). He et al. also
showed that a higher level of SDS (42.8%) was produced by
subjecting OSA-starch to heat-moisture treatment (10% mois-
ture, 120C for four hours) than by treating OSA-starch (28.3%)
with the Englyst method (He et al., 2008). The modified starch
products with attached OSA molecules may act as uncompeti-
tive inhibitors to reduce the enzyme activity and thereby cause
slow digestion. As these studies show, chemical modifications
can be used to prepare SDS, but clinical and toxicological trials
need to be performed in order to evaluate the safety and efficacy
of SDS consumption.
Genetic Modification
Genetic modification of starch biosynthesis involves devel-
oping a strategy to generate new cultivars with desired func-
tionality through extensive breeding and characterization of the
resulting varieties. Genetically controlled factors that affect the
type of starch produced include starch structure, starch content,
interacting cell components, and starch granule architecture.
Waxy starches may be more suitable for making SDS, since
their fine amylopectin structure–the distribution of branches
and chain length–is more critical for SDS formation (Guraya
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1650 M. MIAO ET AL.
et al., 2001b). Moallic et al. developed a novel SDS (long-chain
amylopectin starch) from maize by overexpressing a particular
enzyme involved in starch biosynthesis (Moallic et al., 2006).
This starch, with high granule crystallinity, has few short chains
and more intermediate and long chains. Zhang et al. also showed
that genetic mutants containing amylopectin starch molecules
with either a higher proportion of short chains with DP <13,
particularly A chains with DP 5–9, or a higher proportion of long
chains with DP 13, particularly intermediate to long B chains
with DP >30, contain a greater proportion of SDS than wild
type (Zhang et al., 2008). According to a study by Benmoussa
et al. (2007), formation of SDS positively correlates with the
presence of both long and intermediate/short chains, respec-
tively, while it negatively correlates with the lowest proportion
of extremely short chains. They also found that starch granules
channels can regulate starch digestibility, since starch granules
with channels are digested from the interior outward, and more
extensive channelization gives the enzymes more access to sub-
strate (Benmoussa et al., 2006). Therefore, genetic engineering
has the potential to produce ideal starch with a high SDS content.
BENEFICIAL PHYSIOLOGICAL EFFECTS OF SDS
Many studies have suggested that choosing carbohydrates
withalowGI(GI55) has beneficial effects on various
aspects of physiology and metabolic disorders involved in
chronic nontransmissible disease. As described above from
Fig. 1, low-GI diets yield a more stable diurnal profile,
reducing postprandial hyperglycemia and hyperinsulinemia,
as well as attenuating late postprandial rebound in circulating,
nonesterified fatty acids (NEFA), all of which are factors that
exacerbate these metabolic syndromes (Table 1). Lower glucose
and insulin levels are associated with improved risk profiles,
including insulin sensitivity, β-cell function, high-density
lipoprotein cholesterol, oxidative status, prothrombotic factors,
and endothelial function (FAO/WHO, 1997; Bjrck et al., 2000;
FAO/WHO, 2002; Aston, 2006).
A moderate postprandial glycemic and insulinemic response
due to SDS implies that SDS-rich foods may provide wide
health benefits by reducing common chronic diseases related to
diet, such as diabetes and pre-diabetes, cardiovascular diseases,
and obesity (metabolic syndromes). SDS-rich foods may exert
these effects by reducing the stress on regulatory systems related
to glucose homeostasis (Sievenpiper et al., 2002). According to
Seal et al. (2003), the plasma glucose concentration and serum
insulin concentration in both healthy adults and diet-controlled
type 2 diabetic subjects rose faster, and showed a maximum
glucose change approximately 1.8 times greater, when rapidly
hydrolyzed starch was digested than when slowly hydrolyzed
starch was digested. As reported by Ells et al. (2005), SDS con-
sumption leads to a low and sustained glycemic and insulinemic
response as well as low NEFA, which can decrease cholesterol.
Such a response can contribute to the prevention and treatment
of diabetes and the complications of this metabolic syndrome.
There was a reduction in plasma triacylglycerols, phospholipids
levels, and epididymal adipocyte volume as well as a tendency
toward lower plasma insulin levels after consumption of low-GI
starchy food compared to an isoenergetic isoglucidic high-GI
diet for five weeks (Lerer-Metzger et al., 1996). High-GI starch
is thought to increase fatty acid synthase activity and lipoge-
nesis by reducing the amount of hepatic phosphoenolpyruvate
carboxykinase mRNA, and this starch may have undesirable
long-term metabolic effects (Kabir et al., 1998). Mixed
meals containing SDC induce low-glycemic and insulinemic
responses, and they also reduce the postprandial accumulation
of both hepatically and intestinally-derived, triacylglycerol-rich
lipoproteins (apolipoprotein B-100 and B-48) in obese subjects
with insulin resistance (Harbis et al., 2004). Rapidly and SDC
differ considerably in the stimulation of incretin hormonal
secretion. SDS induces the late and prolonged glucagon-like
peptide-1 (GLP-1) and glucose-dependent insulinotropic
polypeptide (GIP) response from—three to five hours after
ingestion, which may indicate that SDS modulates glucose
homeostasis and regulation of energy storage in the late
postprandial phase (Wachters-Hagedoorn et al., 2006).
SDS and Diabetes Mellitus (DM)
Postprandial hyperglycemia leads to insulin resistance and
eventual pancreatic β-cell failure, which result in noninsulin-
dependent diabetes mellitus (NIDDM), which comprises 90%
of diabetes cases. Therefore, reducing meal-associated hyper-
glycemia is one goal in the prevention of DM. Pharmaceutical
approaches have shown that reducing the rate of carbohydrate di-
gestion attenuates the postprandial glucose response. A glucosi-
dase inhibitor (Acarbose) and Phaseolus vulgaris α-amylase
inhibitor (Phase 2 R) are effective at reducing postprandial hy-
perglycemia; they act by reducing starch bioavailability and
colonic fermentation (Celleno et al., 2007; Wachters-Hagedoorn
et al., 2007; Obiro et al., 2008). Because of the poor nutritional
Tab l e 1 Physiological effects of low-GI foods
Physiological benefits Implications for Health
Improved metabolic modulation Diabetes mellitus
Improved glucose tolerance Cardiovascular disease
Prevention of hypoglycemia and
hyperglycemia
Glycogen storage disease
Improved postprandial glycemic and
insulinemic response
Dyslipidemia
Reduced blood lipid level Cancer
Reduced cariogenic potential Inflammation
Reduced glycosylation of body protein Athletic performance
Prolonged satiety Cognitive function
Prolonged physical performance during
endurance exercise
Weight management
Delayed aging Dental care
Source: Truswell, 1992; Bjrck et al., 2000; Bjrck and Asp, 1994; Ludwig, 2002;
Jenkins et al., 2002; Pi-Sunyer, 2002; Augustin et al., 2002; Sievenpiper et al.,
2002; and Bell and Sears, 2003.
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SLOWLY DIGESTIBLE STARCH 1651
view of nutritionist, this method should be restricted, whereas
the use of SDS is preferred (Jenkins et al., 1988). Kaufman
et al. reported that raw (uncooked) cornstarch as an SDS source
as part of an evening snack may diminish the nighttime and
morning hypoglycemia associated with insulin-dependent dia-
betes mellitus (IDDM), without causing hyperglycemia (Kauf-
man et al., 1995). This method of ingesting a complex carbo-
hydrate to regulate and stabilize the blood glucose level has
been patented (Kaufman, 1995). Two other patents have ap-
peared that use native cornstarch by itself to prepare medical
foods for improving impaired glucose tolerance and preventing
hypoglycemia-induced diabetes (Axelsen and Smith, 2001; Qi
and Tester, 2005). Clinical studies have shown that a low-GI diet
results in a modest improvement in long-term glycemic control
in normolipidemic, well-controlled individuals or overweight
patients with NIDDM (Brand et al., 1991; Wolever et al., 1992).
In randomized controlled trials, a low-GI food proved more
beneficial in the management of diabetes than a conventional or
high-GI food, through reduction of HbA1c or fructosamine lev-
els (Brand-Miller et al., 2003). Consumption of low-GI, starchy
foods decreases the glucose and insulin responses throughout the
day and improves glucose utilization, lipid profile, and capacity
for fibrinolysis, suggesting therapeutic potential for the treat-
ment of diabetes (Jrvi et al., 1999; Rizkalla et al., 2004). SDS
can reduce meal-associated hyperglycemia, and hence it should
be recommended for the prevention and management of DM.
SDS and Cardiovascular Disease (CVD)
High carbohydrate consumption is associated with increased
serum triglycerides and low HDL-cholesterol levels, both of
which are hallmarks of the metabolic syndromes and an in-
creased risk for certain cardiovascular diseases (Leeds, 2002).
High-carbohydrate and high-GI diets are linked to a risk of
coronary heart disease in women during a large prospective
study (Liu et al., 2000). Cross-sectional studies showed that
low-GI diets are associated with a high concentration of HDL-
cholesterol, especially in women (Frost et al., 1999). In addition,
in a well-controlled study involving type 2 diabetic patients,
several parameters were found to be significantly lower after a
low-GI diet than after a high-GI diet: the fasting plasma total,
the activity of serum cholesterol, LDL cholesterol, free fatty
acids, apolipoprotein B, and plasminogen activator inhibitor 1
(Wolever et al., 1992; Rizkalla et al., 2004). Bouch´
eetal.re-
ported that five weeks of a low-GI diet improves some plasma
lipid parameters, decreases total fat mass, and tends to increase
lean body mass without altering body weight; these changes
are accompanied by a decrease in the expression of some genes
implicated in lipid metabolism (Bouch et al., 2002). In this way,
such a diet may help healthy, slightly overweight subjects and it
may play a role in the prevention of metabolic diseases and their
cardiovascular complications. In conclusion, SDS can have an
impact on postprandial blood glucose, insulin levels, and the re-
sulting metabolic syndromes, such as CVD and coronary heart
disease (CHD).
SDS and Glycogen Storage Disease (GSD)
GSD is any one of several hereditary metabolic disorders
that result from enzyme defects. It affects glycogen synthesis
or degradation in muscles, liver, and other cell types. Type I
GSD is associated with the absence or deficiency of glucose-6-
phosphatase, which results in hypoglycemia during fasting. Un-
cooked native maize starch has been administered overnight to
patients as a continuous dietary source of glucose, an approach
that has proven effective as an oral therapy for preventing night-
time hypoglycemic episodes (Chen et al., 1984; Wolfsdorf and
Crigler, 1997). Qi and Tester reported that a therapeutic food
composition comprising a waxy and/or hydrothermally treated
starch may be used to treat or prevent hypoglycemia in pa-
tients susceptible to hypoglycemic episodes, such as patients
with GSD, type 1 diabetes, or liver disease (Qi and Tester,
2005). Giving GSD patients cornstarch processed by controlled
heat-moisture treatment induces euglycemia that lasts longer
and leads to metabolic control that is better in the short term,
compared to uncooked cornstarch (Bhattacharya et al., 2007). In
these cases, SDS can be a significant aid in the treatment of GSD.
SDS and Weight or Obesity Control
Obesity is becoming more prevalent and is associated with
an increase in mortality and morbidity due to DM, hypertension,
CVD, stroke, and cancer. In theory, low-GI foods may benefit
body weight management by promoting satiety and fat oxidation
at the expense of carbohydrate oxidation (Brand-Miller et al.,
2002; Ludwig, 2002; Bell and Sears, 2003; McMillan-Price and
Brand-Miller, 2006), which would support the hypothesis of
nutritional benefits from SDS consumption. Epidemiologic and
clinical intervention studies show that a low-GI diet increases
satiety to a greater extent and reduces plasma insulin responses
more than a high-GI diet (Ludwig, 2002; Warren et al., 2003;
Wolever, 2003). Consumption of overall high-GI starch favors
adipogenesis more than does low-GI starch, leading to a greater
risk of obesity, since digestion and absorption of low-GI starch
may be slower than that of high GI starch. Slower digestion
leads to reduced lipogenesis in adipose and liver tissues, whereas
the apparent digestibility of low-GI starch is similar to that of
normal cornstarch (Bauer et al., 2006). A diet high in rapidly
absorbed carbohydrates leads to an increase in the total body
and hepatic fat deposition, hyperinsulinemia, and an elevation
in the concentration of plasma triacylglycerol. In this way, con-
sumption of a low-GI diet decreases the risk of nonalcoholic
fatty liver disease (NAFLD) in humans (Scribner et al., 2007).
The oxidation pattern of unavailable and SDC helps to modulate
feelings of hunger, and the high-unavailable carbohydrate diet
suppresses feelings of hunger to a greater extent than does the
low-unavailable carbohydrate diet during the postprandial peri-
ods (Sparti et al., 2002). Thus, low-GI meals appear to improve
access to stored metabolic fuels and promote satiety (Ludwig
et al., 1999; Ball et al., 2003; Livesey, 2005). Ad libitum studies
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1652 M. MIAO ET AL.
in overweight or obese adults and children show that low-GL
diets correlate with marked weight benefits, loss of adiposity,
and reduced food intake (Livesey, 2005). Long-term random-
ized controlled trials showed that a low-GI diet can be used
to prevent and treat obesity in children (Spieth et al., 2000).
Therefore, these studies identify SDS as a major component of
strategies to prevent obesity.
SDS and Physical Exercise
To avoid hypoglycemia, central fatigue, and exhaustion as-
sociated with endurance sports activities, such as marathons,
oral glucose may need to be taken before prolonged vigor-
ous exercise in order to increase endurance. Consumption of
a low-GI and carbohydrate-rich food may attenuate the insulin-
mediated metabolic disturbances associated with carbohydrate
intake prior to exercise, facilitating the maintenance of carbohy-
drate availability (Burke et al., 1998). Therefore, SDS may be
beneficial in products used by athletes to enhance performance
by providing an increased, more consistent source of systemic
energy via extended glucose release (Shi et al., 2003; Hamaker
and Han, 2006).
SDS and Cognitive Performance
Brain processes that provide accurate perception and memory
of environmental events enable organisms to function success-
fully depending on the enough glucose from food. A number of
studies performed in adults have shown that missing breakfast
may impair performance in tasks that test reaction time, spa-
tial memory, and immediate word recall (Benton and Parker,
1998). Lang et al. invented a breakfast cereal product (biscuit
or cracker) containing more than 12% (w/w) SDS with the goal
of improving cognitive performance in people, particularly in
children and adolescents, specifically with regard to memory
retention, attention, concentration, vigilance, and mental well-
being (Lang et al., 2003). Glucose regulation has been associ-
ated with cognitive performance in elderly subjects with normal
glucose tolerance, and dietary carbohydrates result in enhanced
cognition in subjects with poor memories or β-cell function
independently of plasma glucose (Kaplan et al., 2000). A re-
cent study involving low-GI breakfasts containing SAG rather
than RAG showed improvement in cognitive performance later
in the morning (Benton et al., 2003). A literature review that
focused on physiological effects of starches concluded that ad-
ministration of glucose may influence both memory and mood,
particularly when intense metabolic demands are placed on the
brain (Benton, 2002).
SDS and Other Health Implications
The digestion of alginate-entrapped starch microspheres as
an SDS source in the alimentary canal generates short-chain
fatty acids, such as acetic, propionic, and n-butyric acid, which
help to prevent colon cancer and produce less energy (Hamaker
et al., 2007; Rose et al., 2007). Low pH in human dental plaque
caused by bacterial fermentation of sugars into acids induces
dental cariogenesis. The pH has been shown to decrease the
least after ingestion of whole-grain foods containing consider-
able amounts of SDS (Truswell, 1992; Bjrck and Asp, 1994).
Raw cornstarch can also be used to maintain normoglycemia
in children with nesidioblastosis (Boneh et al., 1988). Intake
of low-GI diets for 10 weeks reduces LDL cholesterol, which
is beneficial for preventing ischemic heart disease (Sloth et al.,
2004). Consumption of low-GI carbohydrates during pregnancy
not only reduces the risk of gestational DM in healthy pregnant
women, but improves the long-term outcomes of infants (Moses
et al., 2006).
APPLICATIONS OF SDS
SDS, as a new functional component or ingredient in novel
product development, can be widely used in edible solid or liq-
uid processed food products, nutritional supplements, and drug
preparations (tablet, emulsion, and suspension). The amount of
SDS added is selected in order to achieve the desired functional
properties, digestibility, and glucose release rate, or some desir-
able balance of these parameters. SDS can be used in the form of
a powder as an ingredient in a variety of edible products to mod-
ulate the rapid glucose release that is typical of many processed
starchy foods, such as cakes, bread, cookies, pastries, pasta,
pizza, cereals, chips, fries, candy, muesli, dressings, fillings, ic-
ing, sauces, syrups, soups, gravies, puddings, custards, cheese,
yogurts, creams, beverages, dietary supplements, diabetic prod-
ucts, sports drinks, nutritional bars, energy bars, as well as food
for children and babies (Shi et al., 2003; Innereber and Mueller,
2005; Hamaker and Han, 2006; Jiang et al., 2008; van der Maarel
et al., 2008). A new slow-digesting rice starch (Ricemic) has
been developed at the USDA ARS Southern Regional Research
Center, and used to maintain a stable blood-sugar level in diabet-
ics, to provide athletes with a steady energy supply to maintain
endurance, and to replace fat in nonfrozen dairy products (Ben-
nett, 1997; Lee, 1997). To date, starch-based cereal foods and
whole-kernel foods have been developed with both a low GI and
a high SDS load, for example the EDP R(“energy delivered pro-
gressively”) range of plain biscuits developed by experts from
Danone Vitapole. These products are currently marketed in sev-
eral European countries (Belgium, The Netherlands, France,
Spain, Italy, Czech Republic, and Slovakia), as well as in China,
Malaysia, and Russia. Jolly-Zarrouk et al. reported an extended
energy beverage containing much SDS (1.5–15 times) prepared
by hydrothermal treatment (20–35% moisture, 100–110Cfor
20–60 minutes), such as Milo Rbeverage, Nesquick Rbever-
age, Migros Rdrink, or orange juice from Nestl´
e (Jolly-Zarrouk
et al., 2005). Numerous reports describe how to produce SDS,
while studies regarding the mechanism and molecular structural
basis of slow digestion are fewer. In addition, most of the re-
ported SDS materials show low thermal stability when used in
food processing. The current challenge for the food industry is
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SLOWLY DIGESTIBLE STARCH 1653
to develop new technologies to make tailor-made carbohydrate
foods with low GI and appropriate amounts of heat-stable SDS.
Diabetic snack bars are available that are formulated with
uncooked cornstarch either to prevent hypoglycemia or to
reduce postprandial hyperglycemia: Extend Bar (Clinical
Products, Ltd.), Nite Bite Timed-Release Glucose Bar (ICN
Pharmaceuticals, Inc.), Gluc-O-Bar (APIC, USA, Inc.), Ensure
Glucerna (Rose Products Division, Abbott Laboratories), and
Choice DM (Mead Johnson Nutritionals) (Rafkin-Mervis
and Marks, 2001). In addition, given the characteristics of
enzymatic digestion in the upper gastrointestinal tract, SDS
is used as a novel, starch-based biodegradable carrier that
may prove useful in oral drug delivery systems specifically
targeting the small intestine (Jiang et al., 2008). For example,
SDS may be able to serve as a biomacromolecule film-former
for pharmaceutical/nutraceutical coatings to allow complete
release in the small intestine.
In addition to its applications in food and medicine, SDS
can also be used as feedstuff material. Based on a patent of
Winowiski et al. (2005), feed for ruminants that is rich in SDS
may reduce the rate of digestion by rumen microbes, thereby
reducing the effect that rapid consumption of fermentable grains
can have on rumen pH and fiber digestion. This may provide
a more even flow of fermentable starch to support microbial
metabolism, and it may increase the proportion of starch from
cereal grain consumption that ultimately arrives in the small
intestine. Compared to consumption of RDS, consumption of
SDS results in improved protein and energy utilization in broiler
chickens, such as superior feed conversion in amino acid level
(van der Aar, 2003; Weurding et al., 2003)
CONCLUSIONS
Accumulating epidemiological data indicate that a diet char-
acterized by low-GI foods has beneficial metabolic effects and
the potential to reduce insulin resistance and improve certain
metabolic conditions. Consuming a much wider range of low-
GI foods is necessary to achieve a well-balanced, low-GI diet.
However, there are few commercially available low-GI products
in the market, which severely fails to meet the growing needs
of people with diabetes, obesity, and related disorders. SDS as
a novel functional component in products delivers a slow and
prolonged release of glucose when digested, resulting in a lower
GI. It not only helps to fill the existing scarcity of low-GI foods
available, but it also maintains glucose homeostasis and prevents
metabolic syndromes. Although SDS is potentially beneficial to
health, the slow digestion and structural properties of starch need
to be further elucidated in order to increase the SDS content in
processed food.
ACKNOWLEDGMENTS
The authors acknowledge the excellent assistance of Ms.
Meriem Bensmira and Mr. Obiro Wokadala during the drafting
of this manuscript.
FUNDING
The authors are also grateful for the support of the
Program of National Natural Science Foundation of China
(31000764, 31230057, 20976073), the Science & Technology
Pillar Program of Jiangsu Province (BE2012613, BY2012049,
BE2014703), and the Research Program of State Key Labo-
ratory of Food Science & Technology of Jiangnan University
(SKLF-TS-201117).
ABBREVIATIONS
CHD coronary heart disease
CVD cardiovascular disease
DM diabetes mellitus
DNS dinitrosalicylic acid
DP degree of polymerization
EGI extended glycemic index
HI hydrolysis index
GCE glycemic glucose equivalent
GI glycemic index
GIP glucose-dependent insulinotropic polypeptide
GL glycemic load
GLP-1 glucagon-like peptide-1
GSD glycogen storage disease
IDDM insulin-dependent diabetes mellitus (type 1
diabetes)
II insulin index
MGAM maltase-glucoamylase
NEFA nonesterified fatty acids
NIDDM noninsulin-dependent diabetes mellitus (type 2
diabetes)
OSA octenyl succinic anhydride
RAG rapidly available glucose
RDS rapidly digestible starch
RGP relative glycemic potency
RS resistant starch
RVA Rapid Visco Analyser
SAG slowly available glucose
SDC slowly digestible carbohydrate
SDS slowly digestible starch
SI sucrase-isomaltase
TNO The Netherlands Organization for Applied Science
Research
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... Many reviews have shown the positive health benefits of the SDS and RS. [10,14,15] The metabolism of SDS in the small intestine results in a small peak of postprandial blood glucose, which is beneficial for hormonal and metabolic balance, with ultimate improvement in physical and mental performance, satiety control, and diabetes management. [16] On the other hand, RS goes to the large intestine, serving as a substrate for probiotic bacteria, resulting in a fermentation process associated with positive health outcomes. ...
... [16] On the other hand, RS goes to the large intestine, serving as a substrate for probiotic bacteria, resulting in a fermentation process associated with positive health outcomes. [14,15] RS has been associated with reducing the risk of colon cancer and contributing to appetite control. [17] Despite the importance of starch digestibility on the nutritional characteristics of foods and the current health benefits of RS and SDS, their content is not presented in food composition tables (FCT). ...
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Starch is an important dietary carbohydrate in the human diet and is greatly associated with human health. The health effects of starch are classically evaluated by postprandial glycemic response. However, glycemic response is the test result of blood glucose level and sometimes fails to perfectly describe the health effects exerted by starch. Therefore, other factors, besides glycemic response, merit consideration. Herein, we endeavor to provide some insights into the description of health effects exerted by starch. For this purpose, we summarize advances in recent studies to support the crucial roles of glucose kinetics, insulin response, and gut hormones release. A moderate postprandial insulin response and an enhanced release of several specific gut hormones are critical characteristics of a healthier starch, such as those slowly digested till the distal ileum. It is also hoped that further studies can develop feasible methods to produce tailor-made starches with individualized health effects.
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Objective: To examine prospectively the relationship between glycemic diets, low fiber intake, and risk of non-insulin-dependent diabetes mellitus. Design: Cohort study. Setting: In 1986, a total of 65173 US women 40 to 65 years of age and free from diagnosed cardiovascular disease, cancer, and diabetes completed a detailed dietary questionnaire from which we calculated usual intake of total and specific sources of dietary fiber, dietary glycemic index, and glycemic load. Main outcome measure: Non-insulin-dependent diabetes mellitus. Results: During 6 years of follow-up, 915 incident cases of diabetes were documented. The dietary glycemic index was positively associated with risk of diabetes after adjustment for age, body mass index, smoking, physical activity, family history of diabetes, alcohol and cereal fiber intake, and total energy intake. Comparing the highest with the lowest quintile, the relative risk (RR) of diabetes was 1.37 (95% confidence interval [CI], 1.09-1.71, P trend=.005). The glycemic load (an indicator of a global dietary insulin demand) was also positively associated with diabetes (RR= 1.47; 95% CI, 1.16-1.86, P trend=.003). Cereal fiber intake was inversely associated with risk of diabetes when comparing the extreme quintiles (RR=0.72, 95% CI, 0.58-0.90, P trend=.001). The combination of a high glycemic load and a low cereal fiber intake further increased the risk of diabetes (RR=2.50, 95% CI, 1.14-5.51) when compared with a low glycemic load and high cereal fiber intake. Conclusions: Our results support the hypothesis that diets with a high glycemic load and a low cereal fiber content increase risk of diabetes in women. Further, they suggest that grains should be consumed in a minimally refined form to reduce the incidence of diabetes.
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It has been suggested that foods with a high glycemic index are detrimental to health and that healthy people should be told to avoid these foods. This paper takes the position that not enough valid scientific data are available to launch a public health campaign to disseminate such a recommendation. This paper explores the glycemic index and its validity and discusses the effect of postprandial glucose and insulin responses on food intake, obesity, type 1 diabetes, and cardiovascular disease. Presented herein are the reasons why it is premature to recommend that the general population avoid foods with a high glycemic index.
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