The potential of resistant starch as a prebiotic

Abstract

Abstract Resistant starch is defined as the total amount of starch and the products of starch degradation that resists digestion in the small intestine. Starches that were able to resist the digestion will 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 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 and its association with other food component. One of the current interests on resistant starch is their potential to be used as a prebiotic, which is a non-digestible food ingredient that benefits the host by stimulating the growth or activity of one or a limited number of beneficial 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. Realizing this, novel carbohydrates such as resistant starch from various starch sources can contribute to the advancement of the prebiotic industry.

Full text

http://informahealthcare.com/bty
ISSN: 0738-8551 (print), 1549-7801 (electronic)
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
Department of Crop Science, Faculty of Agricultural and Food Sciences, Universiti Putra Malaysia Bintulu Campus, Jalan Nyabau, Bintulu,
Sarawak, Malaysia
Abstract
Resistant starch is defined as the total amount of starch and the products of starch degradation
that resists digestion in the small intestine. Starches that were able to resist the digestion will
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
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
and its association with other food component. One of the current interests on resistant starch
is their potential to be used as a prebiotic, which is a non-digestible food ingredient that
benefits the host by stimulating the growth or activity of one or a limited number of beneficial
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.
Realizing this, novel carbohydrates such as resistant starch from various starch sources can
contribute to the advancement of the prebiotic industry.
Keywords
Functional food, gut microbiota,
oligosaccharide, prebiotic, resistant starch
History
Received 12 June 2014
Revised 6 November 2014
Accepted 6 November 2014
Published online 13 January 2015
Introduction
This review focuses on the potential of resistant starch (RS) as
a functional prebiotic. Prebiotic is defined as a non-digestible
food ingredient that benefit the host by selectively stimulating
the growth or activity of one or limited numbers of bacteria
in the colon, that can improved the host health (Roberfroid
et al., 2010). Meanwhile, RS is defined as the sum of starch
and the product of starch digestion that resists digestion in the
small intestine of a normal human being (Englyst et al., 1992).
Comparing both the definitions, one might realize the
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-
oligosaccharide and galacto-oligosaccharide. All three have
been approved as nutraceutical ingredients due to the
available data. The most prebiotic in demand currently is
the isomalto-oligosaccharide, which is imported from Japan
at a total of 69 000 tons/year (Nakakuki, 2003). The USA
prebiotic market is expected to reach a revenue of $198
million in 2014 (Charalampopoulus & Rastall, 2009).
Resistant starch, with its ability to resist human digestion,
has continued to receive attention, especially on the ferment-
ability properties in the colon and stimulation of bacterial
activities that could affect colon health. Studies on the effects
of RS on the glycemia index, insulin responses, anti-cancer
properties and satiety has been continuously progressing,
proving its role as a functional food. Some RS that have been
commercialized include: Hi-MaizeÕ, a type of RS extracted
from high amylose maize starch produced through natural
breeding program over the past 30 years; NoveloseÕ,a
retrograded high amylose maize starch and Fibersym, a
chemically modified wheat starch. As of last year, Hi-MaizeÕ
and FibersymÕhave obtained approval from Health Canada to
be listed and used as dietary fiber.
Prebiotics
Prebiotics are commonly conceived as carbohydrates of
relatively short chain length (2–10), but some polysaccharides
have also demonstrated prebiotic properties, i.e. inulin. The
most common candidate of prebiotic is the dietary carbohy-
drate, where non-digestible oligosaccharides are currently of
interest due to their selective metabolism. In the USA and
Europe, most marketed prebiotics are inulin-based fructose
oligomers (FOS) or galacto-oligosaccharide (GOS) compo-
nents, which have been granted the prebiotic status of and
their health effects have been extensively studied (Macfarlane
et al., 2008; Panesar et al., 2013). A study on prebiotic
stimulation on Bifidobacterium has compared the effective-
ness of both FOS and GOS in an in vitro setting. Both are
proven to be able to stimulate growth of bifidobacteria, but
GOS are found to be a more preferable substrate for a wider
Address for correspondence: Shahrul R. Sarbini, Department of
Crop Science, Faculty of Agricultural and Food Sciences, Universiti
Putra Malaysia Bintulu Campus, Jalan Nyabau, 97008 Bintulu, Sarawak,
Malaysia. Tel: +60 86855225. Fax: +60 86855415. E-mail:
s.r.sarbini@gmail.com
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
For personal use only.

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
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
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 (RS
1
)
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 (RS
2
) comprises specially
structured granules that prevent digestive enzymes from
hydrolyzing them (Nugent, 2005), for example potatoes and
corns. The RS
1
and RS
2
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 (RS
3
) 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 RS
2
and RS
3
of different sources and origin
such as Hi-MaizeÕand NoveloseÕ, respectively, have been
successfully marketed in the European market. Hi MaizeÕis
one of the richest natural sources of RS (Ingredion, 2014).
The RS Class 4 (RS
4
) comprises starch that has been
modified with chemicals thus increasing their resistance. One
of the most popular marketed RS
4
is the FibersymÕflour. The
RS
4
which are chemically modified, have to comply with
strict regulations that limit the amount of chemicals allowed
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
2S. A. Zaman & S. R. Sarbini Crit Rev Biotechnol, Early Online: 1–7
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
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 RS
2
were colonized by
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 (RS
3
)
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 (RS
2
; 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
Figure 1. Proposed health benefit of a
prebiotic ingredient.
DOI: 10.3109/07388551.2014.993590 The potential of resistant starch as a prebiotic 3
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
For personal use only.

(Anderson & Woodend, 2003; Bodinham et al., 2010). A study
using FibersymÕon 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
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
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 RS
2
and RS
3
, 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 RS
3
and RS
4
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
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 RS
3
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 (Leszczyn
˜ski, 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
4S. A. Zaman & S. R. Sarbini Crit Rev Biotechnol, Early Online: 1–7
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
For personal use only.

Table 1. Methodology to test the potential of resistant starch as a prebiotic.
Criteria In vitro test In vivo test
Resistance towards gastric acidity,
hydrolysis by mammalian enzymes
and gastrointestinal absorption
Pre-treatment of the starch substrate with
various acids and enzymes that mimic the
gastrointestinal condition.
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.
Able to be fermented and utilize by
gut microbiota
Fermentation of carbohydrates by batch or
continuous model with fecal bacteria.
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.
Selectively stimulate activity and/or
growth of one or limited number of
gut microbiota
Same as above, with further analysis
includes the enumeration of bacteria,
e.g. fluorescent in situ hybridization and
culture dependant methodology.
Same as above, with further analysis includes
the enumeration of bacteria, e.g. fluorescent in
situ hybridization and culture dependant
methodology.
Figure 2. The process of resistant starch to be
qualified as a prebiotic.
DOI: 10.3109/07388551.2014.993590 The potential of resistant starch as a prebiotic 5
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
For personal use only.

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
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.
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.
References
Allsopp P, Possemiers S, Campbell D, et al. (2013). An exploratory study
into the putative prebiotic activity of fructans isolated from Agave
angustifolia and the associated anticancer activity. Anaerobe, 22,
38–44.
Anderson GH, Woodend D. (2003). Consumption of sugars and the
regulation of short term satiety and food intake. Am J Clin Nutr, 78,
8435–95.
Belobrajdic DP, King RA, Christophersen CT, Bird AR. (2012). Dietary
resistant starch dose-dependently reduces adiposity in obesity-prone
and obesity resistant male rats. Nutr Metab, 9, 93–7.
Ben XM, Li J, Fend ZT, et al. (2008). Low level of galacto-
oligosaccharide in infant formula stimulates growth of intestinal
Bifidobacteria and Lactobacilli. World J Gastroenterol, 14, 6564–8.
Bindels LB, Porporato P, Dewulf EM, et al. (2012). Gut microbiota
derived propionate reduces cancer cell proliferation in the liver. Br J
Cancer, 107, 1337–44.
Birkett A, Muir J, Phillips J, et al. (1996). Resistant starch lowers fecal
concentrations of ammonia and phenols in human. Am J Clin Nutr,
137, 830–7.
Bodinham CL, Frost GS, Robertson MD. (2010). Acute ingestion of
resistant starch reduces food intake in healthy adults. Br J Nutr, 103,
917–22.
Bodinham CL, Smith L, Wright J, et al. (2012). Dietary fibre improves
first-phase insulin secretion in overweight individuals. PLoS One, 7,
e40834.
Brussow H. (2013). Microbiota and healthy ageing: observational and
nutritional intervention studies. Microb Biotechnol, 6, 326–34.
Cani PD, Holst JJ, Drucker DJ, et al. (2007). GLUT2 and the incretin
receptors involved in glucose induced incretin secretion. Mol Cell
Endocrinol, 278, 18–23.
Case SE, Capitani T, Whaley JK, et al. (1998). Physical properties and
gelation behaviour of a low amylopectin maize starch and other high
amylose maize starches. J Cereal Sci, 27, 301–14.
Charalampopoulus D, Rastall RA. (2009). Prebiotics and probiotics
science and technology. New York: Springer.
Charalampopoulus D, Wang R, Pandiella SS, Webb C. (2002).
Application of cereals and cereal components in functional foods: a
review. Int J Food Microbiol, 79, 131–41.
Charrier JA, Martin RJ, Mccutcheon KL, et al. (2013). High fat diet
partially attenuates fermentation responses in rats fed resistant starch
starch from high amylose maize. Obesity (Silver Spring), 21, 2350–5.
Clark MJ, Robien K, Slavin JL. (2012). Effect of prebiotics on
biomarkers of colorectal cancer in human: a systematic review. Nutr
Rev, 70, 436–43.
Clausen MR, Mortensen PB. (1997). Lactulose, disaccharides and
colonic flora. Drugs, 53, 930–42.
Dewulf EM, Cani PD, Neyrinck AM, et al. (2011). Inulin-type fructans
with prebiotic properties counteract GPR43 overexpression and
PPARy-related adipogenesis in the white adipose tissue of high fat
diet fed mice. J Nutr Biochem, 22, 712–22.
Eerlingen RC, Jacobs H, Delcour JA. (1994). Enzyme resistant starch. V.
Effect of retrogradation of waxy maize starch on enzyme suscepti-
bility. Cereal Chem, 71, 351–5.
Enggum BO, Juliano BO, Perez CM, Acedo EF. (1993). The resistant
starch, undigestible energy and undigestible protein contents of raw
and cooked milled rice. J Cereal Sci, 18, 159–70.
Englyst HN, Kingman SM, Cummings JH. (1992). Classification and
measurement of nutritionally important starch fractions. Eur J Clin
Nutr, 46, 33–55.
Escarpa A, Gonzalez MC, Morales MD, Saura-Calixto F. (1997). An
approach to the influence of nutrients and other food constituents on
resistant starch formation. Food Chem, 60, 527–32.
Everard A, Lazarevic V, Gaia N, et al. (2014). Microbiome of prebiotic-
treated mice reveals novel targets involved in host response during
obesity. ISME J, 8, 2116–30.
Gibson GR, Probert HM, Loo JV, et al. (2004). Dietary modulation of the
human colonic microbiota: updating the concept of prebiotics. Nutr
Res Rev, 17, 259–75.
Gibson GR, Roberfroid MB. (1995). Dietary modulation of the human
colonic microbiota: introducing the concept of prebiotics. J Nutr, 125,
1401–12.
Haralampu SG. (2000). Resistant starch: a review of the physical
properties and biological impact of RS 3. Carbohydr Polym, 41,
285–92.
Hollis J, Hutchison C, Hsu W. (2014). Effect of resistant starch on
subjective appetite and food intake in healthy adults. FASEB J, 28,
1–7.
Ingredion. (2014). Hi-Maize resistant starch-fibre, carbohydrate and
more. Singapore: Food Innovation.
Jane J. (2006). Current understanding on starch granule structures.
J Appl Glycosci, 53, 205–13.
Jane JL, Robyt JF. (1984). Structure studies of amylose-V complexes and
retrograded amylose by action of alpha amylases and a new method
for preparing amylodextrins. Carbohydr Res, 132, 105–18.
Jiang H, Campbell M, Blanco M, Jane JI. (2010). Characterization of
maize amylose extender (ae) mutant starches. Part II: structures and
properties of starch residues remaining after enzymatic hydrolysis at
boiling water temperature. Carbohydr Polym, 80, 1–12.
Johnston K, Thomas E, Bell J, et al. (2010). Resistant starch improves
insulin sensitivity in metabolic syndrome. Diabetic Med, 27, 391–7.
Kalmokoff M, Zwicker B, O’hara M, et al. (2013). Temporal change in
the gut community of rats fed with high amylose corn starch is driven
by endogenous urea rather than strictly on carbohydrate availability.
J Appl Microbiol, 11, 1516–28.
Kohyama K, Nishikari K. (1991). Effect of soluble sugars on gelatin-
ization and retrogradation of sweet potato starch. J Agric Food Chem,
39, 1406–10.
6S. A. Zaman & S. R. Sarbini Crit Rev Biotechnol, Early Online: 1–7
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
For personal use only.

Lehmann U, Robin F. (2007). Slowly digestible starch – its structure and
health implication: a review. Trends Food Sci Technol, 18, 346–55.
Leszczyn
˜ski WA. (2004). Resistant starch – classification, structure,
production. Polish J Food Nutr Sci, 13, 37–50.
Li L, Jiang H, Campbell M, et al. (2008). Characterization of maize
amylose-extender mutant starches. Part I: relationship between
resistant starch contents and molecular structures. Carbohydr Polym,
74, 396–404.
Liu Z, Lin X, Huang G, et al. (2014). Prebiotic effects of almonds and
almond skins on intestinal microbiota in healthy adult humans.
Anaerobe, 26, 1–6.
Luoto R, Ruuskanen O, Waris M, et al. (2014). Prebiotic and probiotic
supplementation prevents rhinovirus infections in preterm infants: a
randomized, placebo-controlled trial. J Allergy Clin Immunol, 133,
403–13.
Macfarlane GT, Steed H, Macfarlane S. (2008). Bacterial metabolism
and health-related effects of galacto-oligosaccharides and other
prebiotics. J Appl Microbiol, 104, 305–44.
Maki KC, Pelkman CL, Finocchiaro ET, et al. (2012). Resistant starch
from high amylose maize increases insulin sensitivity in overweight
and obese man. J Nutr, 142, 717–23.
Matthuis AJ, Vandenheuvel EG, Schotermann MH, Venema K. (2012).
Galacto-oligosaccharides have prebiotic activity in a dynamic in vitro
colon model using a (13) C-labelling technique. J Nutr, 142, 1205–12.
Morrison WR. (1981). Starch lipids: a reappraisal. Starke, 33, 408–10.
Morrison WR. (1995). Starch lipids and how they relate to starch granule
structure and functionality. Cereal Foods World, 40, 437–38, 440–1,
443–6.
Morrison WR. (2000). Starch lipids, starch granule structure and
properties. R Sci Chem, 212, 261–70.
Morrison WR, Tester RF, Snape CE, et al. (1993). Swelling and
gelatinization of cereal starches. Some effects of lipid-complexed
amylose and free amylose in waxy and normal barley starches. Cereal
Chem, 70, 385–91.
Munjal U, Scharlau D, Glei M. (2012). Gut fermentation products of
inulin-type fructans modulate the expression of xenobiotic-matabolis-
ing enzymes in human colonic tumour cells. Anticancer Res, 32,
5379–86.
Nakakuki T. (2003). Development of functional oligosaccharides in
Japan. Trends Glycosci Glycotechnol, 15, 57–64.
Nakayama T, Oishi K. (2013). Influence of coffee (Coffea arabica) and
the galacto-oligosaccharide consumption of intestinal microbiota and
the host responses. FEMS Microbiol Lett, 343, 161–8.
Nayak B, De J, Berrios J, Tang J. (2014). Impact of food processing on
the glycemic index (GI) of potato products. Food Res Int, 56, 35–46.
Nugent AP. (2005). Health properties of resistant starch. Nutr Bull, 30,
27–54.
Panesar PS, Kumari S, Panesar R. (2013). Biotechnological approaches
for the production of prebiotics and their potential applications. Crit
Rev Biotechnol, 33, 345–64.
Phillips J. (1995). Effect of resistant starch on fecal bulk and
fermentation dependent events in humans. Am J Clin Nutr, 62,
121–30.
Polesi LF, Sarmento S, Franco CM. (2011). Production and physico-
chemical properties of resistant starch from hydrolysed wrinkled pea
starch. Int J Food Sci Technol, 46, 2257–64.
Roberfroid M, Hoyles L, Mccartney AL, et al. (2010). Prebiotic concept:
definition, metabolic and health benefits. Br J Nutr, 104, 1–63.
Robertson MD, Currie JM, Morgan LM, et al. (2003). Prior short term
consumption of resistant starch enhances postprandial insulin sensi-
tivity in healthy subjects. Diabetologia, 46, 659–65.
Sajilata MG, Singhal RS, Kulkarni PR. (2006). Resistant starch –
a review. Comp Rev Food Sci Food Saf, 5, 1–17.
Salminen S, Bouley C, Boutron-Ruault MC, et al. (1998). Functional
food science and gastrointestinal physiology and function. Br J Nutr,
80, 147–71.
Sarawong C, Schoenlechner R, Sekiguchi K, et al. (2014). Effect of
extrusion cooking on the physicochemical properties, resistant starch,
phenolic content and antioxidant capacities of green banana flour.
Food Chem, 143, 33–9.
Sarbini SR, Kolida S, Deaville ER, et al. (2014). Potential of novel
dextran oligosaccharides as prebiotics for obesity management
through in vitro experimentation. Br J Nutr, 112, 1303–14.
Sarbini SR, Kolida S, Gibson GR, Rastall RA. (2013). In vitro
fermentation of commercial a-gluco-oligosaccharide by faecal micro-
biota from lean and obese human subjects. Br J Nutr, 109, 1980–9.
Sarbini SR, Rastall RA. (2011). Prebiotics: metabolism, structure and
function. Funct Food Rev, 3, 93–106.
Scholz-Ahrens KE, Ade P, Marten B, et al. (2007). Prebiotics, probiotics,
and synbiotics affect mineral absorption, bone mineral content, and
bone structure. J Nutr, 137, 838S–46S.
Scott KP, Martin JC, Duncan SH, Flint HJ. (2014). Prebiotic stimulation
of human colonic butyrate-producing bacteria and bifidobacteria,
in vitro. FEMS Microbiol Ecol, 87, 30–40.
Shen R-L, Zhang W-L, Dong J-L, et al. (2014). Sorghum resistant starch
reduces adiposity in high-fat diet-induced overweight and obese rats
via mechanisms involving adipokines and intestinal flora. Food Agric
Immunol, 1–11.
Shi YC, Capitani T, Trzasko P, Jeffcoat R. (1998). Molecular structure of
a low amylopectin starch and other high amylose maize starch.
J Cereal Sci, 27, 289–99.
Sievert D, Pomeranz Y. (1989). Enzyme resistant starch.
I. Charcterization and evaluation by enzymatic, thermoanalytical
and microscopic method. Cereal Chem, 66, 342–7.
Silva CS, Bome JJGCVD, Gerrits WJJ, et al. (2012). Effects of dietary
fibers with different physiochemical properties on feeding motivation
in an adult female pigs. Physiol Behav, 107, 218–30.
Singh J, Dartois A, Kaur L. (2010). Starch digestibility in food matrix: a
review. Trends Food Sci Technol, 21, 168–80.
Slavin J. (2004). Whole grains and human health. Nutr Res Rev, 17,
99–110.
Tachon S, Zhou J, Keenan M, et al. (2013). The intestinal microbiota in
aged mice is modulated by dietary resistant starch and correlated with
improvements in host responses. FEMS Microb Ecol, 83, 299–309.
Tester RF, Qi X, Karkalas J. (2006). Hydrolysis of native starches with
amylases. Anim Feed Sci Technol, 130, 39–54.
Toden S. (2006). Resistant starch prevents colonic DNA damage induced
by high dietary cooked red meat or casein in rats. Cancer Biol Ther, 5,
267–72.
Zhu C-L, Zhao X-H. (2013). In vitro fermentation of a retrograded maize
starch by healthy adult fecal extract and impacts of exogenous
microorganisms on three acids production. Starke, 65, 330–7.
DOI: 10.3109/07388551.2014.993590 The potential of resistant starch as a prebiotic 7
Critical Reviews in Biotechnology Downloaded from informahealthcare.com by 175.140.56.62 on 01/13/15
For personal use only.