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Crit Rev Biotechnol, Early Online: 1–7

! 2015 Informa Healthcare USA, Inc. DOI: 10.3109/07388551.2014.993590

REVIEW ARTICLE

The potential of resistant starch as a prebiotic

Siti A. Zaman and Shahrul R. Sarbini
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by Flinders University of South Australia on 01/14/15

Department of Crop Science, Faculty of Agricultural and Food Sciences, Universiti Putra Malaysia Bintulu Campus, Jalan Nyabau, Bintulu,
Sarawak, Malaysia

Abstract Keywords
Resistant starch is defined as the total amount of starch and the products of starch degradation Functional food, gut microbiota,
that resists digestion in the small intestine. Starches that were able to resist the digestion will oligosaccharide, prebiotic, resistant starch
arrive at the colon where they will be fermented by the gut microbiota, producing a variety of
products which include short chain fatty acids that can provide a range of physiological History
benefits. There are several factors that could affect the resistant starch content of a
carbohydrate which includes the starch granule morphology, the amylose–amylopectin ratio Received 12 June 2014
and its association with other food component. One of the current interests on resistant starch Revised 6 November 2014
is their potential to be used as a prebiotic, which is a non-digestible food ingredient that Accepted 6 November 2014
benefits the host by stimulating the growth or activity of one or a limited number of beneficial Published online 13 January 2015
bacteria in the colon. A resistant starch must fulfill three criterions to be classified as a prebiotic;
resistance to the upper gastrointestinal environment, fermentation by the intestinal microbiota
and selective stimulation of the growth and/or activity of the beneficial bacteria. The market of
prebiotic is expected to reach USD 198 million in 2014 led by the export of oligosaccharides.
For personal use only.

Realizing this, novel carbohydrates such as resistant starch from various starch sources can
contribute to the advancement of the prebiotic industry.

Introduction activities that could affect colon health. Studies on the effects
of RS on the glycemia index, insulin responses, anti-cancer
This review focuses on the potential of resistant starch (RS) as
properties and satiety has been continuously progressing,
a functional prebiotic. Prebiotic is defined as a non-digestible
proving its role as a functional food. Some RS that have been
food ingredient that benefit the host by selectively stimulating
commercialized include: Hi-MaizeÕ , a type of RS extracted
the growth or activity of one or limited numbers of bacteria
from high amylose maize starch produced through natural
in the colon, that can improved the host health (Roberfroid
breeding program over the past 30 years; NoveloseÕ , a
et al., 2010). Meanwhile, RS is defined as the sum of starch
retrograded high amylose maize starch and Fibersym, a
and the product of starch digestion that resists digestion in the
chemically modified wheat starch. As of last year, Hi-MaizeÕ
small intestine of a normal human being (Englyst et al., 1992).
and FibersymÕ have obtained approval from Health Canada to
Comparing both the definitions, one might realize the
be listed and used as dietary fiber.
similarities, but it is noteworthy to know that not all RS can
fulfill the criteria as a prebiotic.
Most studies on prebiotics were focused on inulin, fructo- Prebiotics
oligosaccharide and galacto-oligosaccharide. All three have
Prebiotics are commonly conceived as carbohydrates of
been approved as nutraceutical ingredients due to the
relatively short chain length (2–10), but some polysaccharides
available data. The most prebiotic in demand currently is
have also demonstrated prebiotic properties, i.e. inulin. The
the isomalto-oligosaccharide, which is imported from Japan
most common candidate of prebiotic is the dietary carbohy-
at a total of 69 000 tons/year (Nakakuki, 2003). The USA drate, where non-digestible oligosaccharides are currently of
prebiotic market is expected to reach a revenue of $198
interest due to their selective metabolism. In the USA and
million in 2014 (Charalampopoulus & Rastall, 2009).
Europe, most marketed prebiotics are inulin-based fructose
Resistant starch, with its ability to resist human digestion,
oligomers (FOS) or galacto-oligosaccharide (GOS) compo-
has continued to receive attention, especially on the ferment-
nents, which have been granted the prebiotic status of and
ability properties in the colon and stimulation of bacterial
their health effects have been extensively studied (Macfarlane
et al., 2008; Panesar et al., 2013). A study on prebiotic
Address for correspondence: Shahrul R. Sarbini, Department of stimulation on Bifidobacterium has compared the effective-
Crop Science, Faculty of Agricultural and Food Sciences, Universiti ness of both FOS and GOS in an in vitro setting. Both are
Putra Malaysia Bintulu Campus, Jalan Nyabau, 97008 Bintulu, Sarawak,
Malaysia. Tel: +60 86855225. Fax: +60 86855415. E-mail: proven to be able to stimulate growth of bifidobacteria, but
s.r.sarbini@gmail.com GOS are found to be a more preferable substrate for a wider
 2 S. A. Zaman & S. R. Sarbini
range of Bifidobacterium spp. (Scott et al., 2014). In addition,
other potential prebiotic candidates such as isomalto-oligo-
saccharides, xylo-oligosaccharides, soybean-oligosacchar-
ides, lactosucrose and polydextrose are still in need of
further studies. The assumption and claims of many carbo-
hydrates as prebiotics without due consideration to its criteria
will generate more confusion to the consumer. A manageable
set of in vitro and in vivo tests are required to fully understand
the digestion and fermentation of the prebiotic. The main
criteria used as a guideline to prebiotic labeling are as follows
(Roberfroid et al., 2010):
(1) Resistance to gastric acidity, hydrolysis by mammalian
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enzymes and gastrointestinal absorption.
(2) Fermented and utilized by the gut microbiota.
(3) Selectively stimulate activity and/or growth of one or
limited number of gut bacteria that contribute to host
health and well being.
Health benefit of prebiotics
Prebiotics will only be functional once it reaches the colon,
where it will be utilized by a specific group of gut microbiota.
The specificity is important, as prebiotic will only be
considered functional when it stimulates only the growth
and activity of the beneficial bacteria, i.e. Bifidobacterium
and Lactobacillus, subsequently producing metabolites such
as the short-chain fatty acids that could later benefit the host
(Sarbini et al., 2014). Figure 1 shows the proposed health
For personal use only.
benefit of a prebiotic ingredient. The recommended daily
intake of a prebiotic is 5–8 g, while exceeding 20 g/day may
cause intestinal discomfort due to gas distension (Clausen &
Mortensen, 1997).
Resistant starch
Naturally occurring RS is often found in cereal grains,
seeds and heated starch and starch-containing foods
(Charalampopoulus et al., 2002). Resistant starches have
been classified into four classes. The RS Class 1 (RS1)
comprises of physically inaccessible starch such as legumes
and seeds. The resistance comes from the compact molecular
structure that limits the accessibility of digestive enzymes
(Haralampu, 2000). The RS Class 2 (RS2) comprises specially
structured granules that prevent digestive enzymes from
hydrolyzing them (Nugent, 2005), for example potatoes and
corns. The RS1 and RS2 are naturally occurring starches that
can easily be destroyed upon processing. Non-naturally
occurring RS2 can be produced through genetic engineering
and strategized breeding. The RS Class 3 (RS3) comprises
retrograded starches produced through gelatinization and
retrogradation process during food processing and manufactur-
ing. They are commonly found in cooked and cooled foods
such as bread. The RS2 and RS3 of different sources and origin
such as Hi-MaizeÕ and NoveloseÕ , respectively, have been
successfully marketed in the European market. Hi MaizeÕ is
one of the richest natural sources of RS (Ingredion, 2014).
The RS Class 4 (RS4) comprises starch that has been
modified with chemicals thus increasing their resistance. One
of the most popular marketed RS4 is the FibersymÕ flour. The
RS4 which are chemically modified, have to comply with
strict regulations that limit the amount of chemicals allowed
Crit Rev Biotechnol, Early Online: 1–7
for consumption. The USA and Japan are the only countries
that authorized chemically modified RS for their food market.
Meanwhile, the European Union has yet to approve the usage
of chemically modified RS for human consumption.
Factors affecting resistant starch content
The factors that influence resistance towards digestion
includes: the physical form of the grains and seeds, the size
and type of the starch granules and the association between
the starch with other dietary components resistance (Slavin,
2004). Food preparation process, such as cooking, can also be
a factor as demonstrated in rice where its resistance had
increased after milling and cooking (Enggum et al., 1993).
Extrusion with high feed moisture and low screw speed has
also been shown to increase RS content in green banana flour
(Sarawong et al., 2014).
Starch granules morphology
The morphology of the starch granule is dependable on their
botanic origin. The smaller the granules means the more
susceptible they are to enzyme digestion (Lehmann & Robin,
2007). This may be attributed to a larger specific surface area
which increases enzyme binding rate (Tester et al., 2006). The
enzyme binding rate is also relatable to the shape of starch
granules. The various shapes of the starch granules from
spherical to polyhedral may influence enzyme binding.
Another factor affecting the RS content is the surface of the
granule. Potato starch and high amylase starches has been
shown to have a smooth surface and very few pits or pores
(Lehmann & Robin, 2007). The pin holes, equatorial grooves
and small nodules often become the entry point of the
amylase enzymes (Singh et al., 2010).
Amylose–amylopectin ratio
It has been demonstrated that higher amylose content of
starches correlates with higher resistance towards enzyme
digestion. This is due to the compact linear structure of
amylose (Sajilata et al., 2006; Sievert & Pomeranz, 1989). In
addition, the presence of hydrogen bond linking the glucose
chain of the starch amylose confers them to more resistance
towards the enzyme activity (Sajilata et al., 2006). The
amylopectin can also contribute to an increase of RS content.
A previous study has shown that RS content of bakery products
proceeds during their storage time due to amylopectin
retrogradation (Eerlingen et al., 1994). The formation of RS
from amylopectin during retrogradation is due to an increase in
molecule entanglement in the gel network and/or an increase of
molecular order by the helix formation of the outer short chains
of amylopectin, in a three-dimensional, partially crystalline
structure (Polesi et al., 2011). Amylopectin debranching has
also been shown to be able to improve RS content, where the
end products of low-molecular weight polymers could promote
the retrogradation process (Polesi et al., 2011).
Interaction of starch with other food components
The most studied association of starch with food components
is the interaction between amylose and lipid. Association of
amylose with lipid increases the starch resistance properties
 DOI: 10.3109/07388551.2014.993590
Figure 1. Proposed health benefit of a
prebiotic ingredient.
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For personal use only.
by reducing the access of the active site of a-amylase to
the amylose chain. Several other studies has also recognized
the amylose–lipid complexes as RS by itself (Sajilata et al.,
2006). However, association of starch with protein, soluble
sugars, calcium and potassium has been shown to reduce the
RS content. The interaction between soluble sugars and starch
molecular chain decreases its crystallinity and subsequently
its resistance (Kohyama & Nishikari, 1991). The association
of starch to calcium and potassium caused a reduction of
hydrogen bonds due to the adsorption of the minerals, thus
decreasing the RS content (Escarpa et al., 1997). On the other
hand, its interaction with insoluble dietary fiber showed the
most minimal effect (Sajilata et al., 2006).
Health benefit of resistant starch
Some studies have demonstrated that RS is capable of
influencing the gut microbiota composition towards those that
are beneficial to the host. A study demonstrated that mice fed
with diets containing high amylose RS2 were colonized by
The potential of resistant starch as a prebiotic 3
higher levels of Bacteroidetes and Bifidobacterium,
Akkermansia and Allobactum species (Tachon et al., 2013).
A recent nutritional intervention study exhibited that RS from
different geographical areas induced a 10-fold increase of the
gut bifidobacteria (Brussow, 2013).
One of the beneficial by products of RS fermentation are
short-chain fatty acids, i.e. acetate, propionate and butyrate.
A recent study demonstrated the fermentation of retrograded
maize starch increases the short chain fatty acids (Zhu &
Zhao, 2013). Another study with high amylose maize (RS3)
feedings in rats, shows an increase in propionate, acetate and
butyrate (Charrier et al., 2013). In addition, an increase of
propionate was demonstrated in rats fed with high amylase
maize starch (RS2; Kalmokoff et al., 2013).
Resistant starch has also been proven to be an excellent
fiber in terms of providing satiety to the consumer. Studies
with RS fed pigs showed RS were among the most satiating
fiber, possibly due to their fermentation properties (Silva
et al., 2012). Several other studies have also showed that the
ingestion of RS may enhance short- and long-term satiety
 4 S. A. Zaman & S. R. Sarbini
(Anderson & Woodend, 2003; Bodinham et al., 2010). A study
using FibersymÕ on healthy adults has also shown that
replacing rapidly digestible starch with RS decreases meal
caloric density (Hollis et al., 2014). Another perspective of RS
application currently being studied is their potential role as an
anti-colorectal cancer agent by altering the composition
or activity of the colorectal microbiota (Clark et al., 2012).
This study demonstrated that the crypt mitotic location, gene
expression and DNA methylation were improved after RS
consumption.
The RS has been shown to have an impact on insulin
response. A study explored the effects of RS on insulin
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excretion with 12 overweight individuals participating in the
randomized, blind, crossover study (Bodinham et al., 2012). In
just 4 weeks, the RS intake significantly increased the first-
phase insulin secretion in individuals at risk of developing
type-2 diabetes. Other studies demonstrated a dampen insulin
response and improvement of insulin sensitivity following
RS consumption (Johnston et al., 2010; Maki et al., 2012;
Robertson et al., 2003).
The RS consumption has been shown to be able to
beneficially increase the stool bulk, giving mild laxative
effects which promote the regularity of bowel movement
(Phillips, 1995). A study of rats that were fed with high
amylose maize exhibited an increase of cecal weight and a
decrease in cecal pH (Charrier et al., 2013). This supports a
previous study that exhibited a decrease of intestinal pH while
For personal use only.
reducing the production of potentially harmful secondary bile
acids, ammonia and phenols (Birkett et al., 1996). In addition,
the consumption of RS may help in preventing the degradation
of the mucous layer within the colon (Toden, 2006). Another
study using Sprague–Dawley model has also shown that RS
could reduce body fat of high-fat diet-induced overweight and
obese rats, and improve lipid metabolism disorders (Shen et al.,
2014).
Resistant starch as prebiotics
It is quite difficult to conclude the suitability of RS to be
regarded as a prebiotic candidate due to the broad diversity of
starches. In general, a type of RS has to fulfill the following
criteria to be fully identified as prebiotic.
Criteria 1: resistance to gastric acidity, hydrolysis by
mammalian enzymes and gastrointestinal absorption
RS resistance is mostly contributed by their structural charac-
teristics. However, due to the diverse physico-chemical
properties of RS, it is hard to establish the standard degree of
resistance required to be fully resist the upper digestion in the
human gastrointestinal tract. The RS2 and RS3, which are
naturally occurring starches, are inaccessible towards enzym-
atic digestion contributed by their complex structure. Both RS
did not undergo any physical or chemical modification but
instead they can be produced through genetic engineering or
selected breeding to further enhance their resistance. The RS3
and RS4 are produced through either physical or chemical
manipulation. The degree of modification affects the degrees
of resistance, and for most modified starches, the RS content
increases with increasing degree of modification (Nayak et al.,
2014). However, the modification itself needs to adhere to
Crit Rev Biotechnol, Early Online: 1–7
strict regulation from a respective governing body for it to be
suitable for consumption. In the US, the Food and Drug
Administration has provided a complete detail of additives and
the concentration allowed in food in the market.
One of the main characteristics that determine the resistance
of starch is the amylose to amylopectin ratio. In starch
structure, the amylose and amylopectin molecules are
organized in semi-crystalline structure of double helices
where the entanglement between the molecules holds the
integrity of starch granules. For example, in RS3 preparation,
the amylose which exists in the linear fraction, can easily
undergoes retrogradation where the resultant retrograded
starch with increased thermal stability contributes to its
resistance (Leszczyñski, 2004). Several other studies have
also demonstrated that, as the ratio of amylose to amylopectin
increases, the enzymatic digestibility of the starch decreases
(Jane, 2006; Li et al., 2008). This is due to the interaction of
amylose molecules with amylopectin which prevents the starch
from swelling thus reducing the accessibility of enzymes to
hydrolyze starch molecules (Case et al., 1998; Jiang et al.,
2010; Shi et al., 1998)
Another starch characteristic that could influence its
digestibility is the lipid content. The presence of lipid in the
starch molecules may retard the starch’s enzymatic hydrolysis
(Jiang et al., 2010). The amylose–lipid complexes which are
resistant to amylase hydrolysis, restricts starch swelling and
reduces the enzymatic hydrolysis of starch granules (Jane &
Robyt, 1984; Morrison, 2000; Morrison et al., 1993). In
addition, the presence of lipid on the surface of starch granules
can contribute to their resistance (Morrison, 1981, 1995).
Criteria 2: able to be fermented and be utilized by gut
microbiota
Starch portion that has successfully resisted the upper digestive
system will eventually reach the colon. For a RS to be qualified
as a prebiotic that contributes to its beneficial effect towards
the host, it must be able to be used as a fermentation substrate
for the existing gut microbiota. Two main types of bacterial
fermentation exists in the gut, i.e. saccharolytic and proteolytic.
The favorable saccharolytic bacteria are responsible for the
breaking down of carbohydrate, whereas the proteolytic
bacteria break down protein molecules. Saccharolytic bacteria
are usually more dominant in the proximal colon whereas
proteolytic bacteria are more abundant in the distal part of the
colon (Salminen et al., 1998). The two types of fermentation
will produce different by products which can be tested to
determine the RS efficacy as prebiotic candidates. Most studies
on prebiotics usually investigate criteria 2 and 3, collectively.
Criteria 3: selectively stimulate activity and/or growth of one
or a limited number of gut bacteria that contribute to host
health and well being
In most cases, the RS might only be able to fulfill Criteria 2,
where the fermentation is not specific towards beneficial
bacteria. The RS may also be fermented by a wide array of
gut microbiota including the pathogens, as typically demon-
strated by the fermentation of dietary fiber (Gibson &
Roberfroid, 1995). Criteria 3 is the most difficult to fulfill
when investigating a putative prebiotic carbohydrate (Gibson
 DOI: 10.3109/07388551.2014.993590
Table 1. Methodology to test the potential of resistant starch as a prebiotic.
Criteria
Resistance towards gastric acidity,
hydrolysis by mammalian enzymes
and gastrointestinal absorption
Able to be fermented and utilize by
gut microbiota
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Selectively stimulate activity and/or
growth of one or limited number of
gut microbiota
Figure 2. The process of resistant starch to be
qualified as a prebiotic.
For personal use only.
The potential of resistant starch as a prebiotic
In vitro test
 Pre-treatment of the starch substrate with
various acids and enzymes that mimic the
gastrointestinal condition.
 Fermentation of carbohydrates by batch or
continuous model with fecal bacteria.
 Same as above, with further analysis
includes the enumeration of bacteria,
e.g. fluorescent in situ hybridization and
culture dependant methodology.
5
In vivo test
 Measuring substrate recovery in feces of rat
 Intubation into the gastrointestinal system of
anesthetized rat.
 Direct recovery of undigested molecules in the
distal ileum following oral administration of
substrate.
 Animal model – Rats are fed with food or
drink fortified with prebiotic for a duration of
time. The animal will then be anesthetized and
killed to recover the colon for further analysis.
 Indirect method – Collection of breath air at
regular time intervals to measure the
concentration of gases, i.e. hydrogen.
 Direct method – Collection of feces to meas-
ure the recovery of test substrate.
 Same as above, with further analysis includes
the enumeration of bacteria, e.g. fluorescent in
situ hybridization and culture dependant
methodology.
 6 S. A. Zaman & S. R. Sarbini
et al., 2004). These require quantitative microbiological
analysis of major colonic bacterial genera for example
bacteroides, bifidobacteria, lactobacilli, clostridia, enterobac-
teria, eubacteria and the total aerobes/anaerobes (Sarbini et al.,
2013). To date, molecular-based microbiological methodolo-
gies have been developed and accepted as a reliable tool. In
addition, the production of organic acids, gas and enzymes
have been used as markers to monitor stimulation of the
bacterial activity (Sarbini & Rastall, 2011). Therefore, it is
important to design studies that can demonstrate specific
potential of RS as a prebiotic. Table 1 shows the methodologies
to test the potential of starch as a prebiotic. One last thing to
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note is that for the RS to be fully proven as a prebiotic, a
strategized human clinical study must be conducted. Figure 2
summarizes the process of RS to be qualified as a prebiotic.
Conclusion
There is no doubt that RS has prebiotic potential as more
recent and upcoming studies are conducted on RS influencing
the gut microbiota. It is essential to understand the factors
affecting the RS content in food. Another important issue that
needs to be addressed is the establishment of standard
procedures to demonstrate prebiotic potential via in vitro and/
or in vivo tests due to the diverse source of RS. With the
expansion of prebiotic market, especially in the US and Japan,
the emergence of RS could facilitate this demand.
For personal use only.
Acknowledgements
We gratefully acknowledge the reviewers for their critical
reading and scientific inputs. We would also like to thank the
library staff at the Faculty of Agricultural and Food Sciences,
Universiti Putra Malaysia for their collaboration in retrieving
the scientific literature.
Declaration of interest
The authors report no declarations of interest. The authors are
responsible for the content and writing of this article.
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