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Starch/Stärke 55 (2003) 539–545 DOI 10.1002/star.200300221 539

David L. Toppinga, Resistant Starch and Health – Himalaya 292, a Novel

Matthew K. Morellb,
Roger A. Kinga, Barley Cultivar to Deliver Benefits to Consumers
Zhongyi Lib,
Dietary and lifestyle change is a recognised strategy for the management and preven-
Anthony R. Birda,
tion of socio-economically important non-infectious diseases. Dietary fibre is com-
Manny Noakesa
posed largely of non-starch polysaccharides (NSP), and greater consumption of NSP-
rich foods relieves simple constipation very effectively. Starch (as resistant starch, RS)
a is also receiving attention for its potential role in promoting colonic function. Resistant
CSIRO Health Sciences
and Nutrition, starch is that fraction of starch which escapes human small intestinal digestion and en-
Kintore Avenue, ters the large bowel where (together with a variable fraction of NSP) it is fermented by
Adelaide 5000, Australia the resident microflora. The resulting short chain fatty acids (SCFA) are taken up by the
b CSIRO Plant Industry, large bowel and metabolised. SCFA mediate many of the health benefits ascribed to
Black Mountain, NSP and RS. Starch consumption is low in affluent westernised countries, despite rec-
Canberra 2600, Australia ommendations by health agencies. In Australia, foods enriched in RS as a high amy-
lose maize starch have gained consumer acceptance. However, scope remains for ad-
ditional products and ingredients and a company, Ascentia Pty Ltd, has been estab-
lished to develop a novel barley cultivar (Hordeum vulgare var. himalaya 292) for this
purpose. This cultivar has a specific gene alteration leading to a loss of starch syn-
thetase lla activity resulting in a grain which is low in starch but disproportionately high-
er in amylose and also NSP. Animal and human studies have shown that Himalaya 292
is high in RS relative to existing products and has a low glycaemic index and the culti-
var offers promise as a vehicle to deliver health benefits to consumers.

Keywords: Cereals; Fibre; Health; Resistant starch; Barley

1 Introduction dose-response relationship between its intake and stool

In westernised, affluent societies the major causes of dis-
ability and premature death are chronic, non-infectious
diseases. These have replaced transmissible infectious
illnesses as the most socio-economically important chal-
lenges to public health. Dietary and lifestyle change are
accepted as important contributors to the prevention and
management of coronary heart disease (CHD), diabetes,
mass [2]. Indeed, it has been reported that plastic “bran
flakes” are very effective and act through this bulking
mechanism [3]. Insoluble NSP may also protect against
diverticular disease in the long term with very significant
reductions in symptoms with greater consumption [4]. In
Australia these benefits have translated progressively
over the past 20 years to higher fibre intakes at the gen-

obesity, certain cancers (e.g. of the colon and rectum)
and problems of laxation such as constipation and diver-
ticular disease, and complex carbohydrates, especially
non-starch polysaccharides (NSP, major components of
dietary fibre) have well-documented roles in their man-
agement and in risk reduction. Foods and concentrates,
especially those high in insoluble NSP, are excellent laxa-
tives and can be used to relieve constipation, even in the
very elderly [1]. Non-starch polysaccharides are indi-
gestible by human digestive enzymes and pass into the
large bowel. This helps to explain the effectiveness of
products such as wheat bran, which appear to act me-
chanically through greater faecal bulking with an excellent
Correspondence: David L. Topping, CSIRO Health Sciences
and Nutrition, PO Box 10041, Adelaide BC 5000, Austra-
lia. Phone: +61-8-8303-8930, Fax: +61-8-8303-8899, e-mail:
david.topping@csiro.au.
Review
eral population level [5]. This change has been achieved
through consumption of processed foods rather than sup-
plements.
The generally high level of acceptance of fibre-enriched
foods for their laxating effects is quite easy to understand,
given that symptom relief equates well with long-term pro-
tection against diverticular disease. However, there is one
area in which NSP have yet to show the expected bene-
fits, namely colo-rectal cancer. This is a significant prob-
lem in westernised countries and is highly lifestyle-relat-
ed, with only a small proportion being due to inheritance
[6]. Nevertheless, population [7] and intervention [8] stud-
ies have not yet shown the anticipated risk reduction with
greater fibre consumption. Part of the problem may be
methodological (e.g. inadequate numbers) as the EPIC
(European Prospective Investigation of Cancer) project is
showing a significant protective effect of fibre intake in co-
lo-rectal cancer [9]. This study is examining the relation-

© 2003 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.starch-journal.de


540 Topping et al.
ship between dietary intakes and disease risk in a large
population across a range of European countries with
widely differing dietary habits. While this approach
promises to give new insights into the role of dietary fibre
in colo-rectal cancer, the current uncertainty about the
role of NSP in this condition has led to a general reap-
praisal of human polysaccharide digestion and metab-
olism, especially of starch. This is reflected in the continu-
ing development of the concept of resistant starch (RS)
which, in addition to protection against large bowel can-
cer, may have wider implications for human gut function
and health such as improved mineral bioavailability [10,
11].
2 Historical Aspects of the Relative
Importance of Dietary Fibre, NSP and RS
For a perspective on the current state of knowledge of
NSP and RS it is helpful to consider the early epidemi-
ological work of Burkitt and colleagues [12]. These work-
ers noted that native East Africans were free of non-infec-
tious diseases which affected Europeans living in the
same environment. The Africans consumed a diet high in
unrefined cereal products and it was concluded that their
diet was relatively high in fibre. It was hypothesised that it
was a deficiency of fibre intake that was responsible for
the prevalence of the “diseases of affluence” in the Euro-
peans. Since then, intense human and animal investiga-
tion has shown the benefits of plant fibre consumption for
health, despite the problematic issue of colo-rectal can-
cer. This particular anomaly is central to an understanding
of the mechanisms whereby carbohydrates (and diet in
general) can affect disease risk. Firstly, it seems that one
of the key differences between native African diets and
those of Europeans is that the former are relatively low in
energy (as fat) and animal products [13]. Energy intake
per se appears to be a risk factor for a number of condi-
tions, including colo-rectal cancer [14] and its importance
may have been overlooked. More germane to this discus-
sion are the advances in analytical technology which
have led to a re-examination of the diets of Africans. Cur-
rently, fibre is understood to be composed largely of NSP
with only a small contribution from other components
such as lignin. This contrasts with the more traditional
perception of fibre and fibre-rich foods as being essential-
ly “woody” [15]. Again, the issue is partly methodological
as the analytical procedures used when Birkett et al. were
making their observations were those used to analyse the
fibre content of forage for ruminants. The cereal diets of
the Africans correlate well with crude fibre methods, but
that of the whites appears to have been underestimated.
The animal feeds referred to above are high in insoluble
NSP (e.g. cellulose) and the methods underestimate im-
portant constituents such as pectins quite substantially
© 2003 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
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Starch/Stärke 55 (2003) 539–545
[14]. With the application of more advanced technologies
it has emerged that the African diet (and the diet of other
low-risk groups) may actually be lower in fibre (or NSP)
relative to that of high risk populations [14]. The former al-
so appear to consume relatively high levels of starch
compared with societies such as Australia and the USA.
Indeed, statistical analysis of dietary intakes across pop-
ulations shows non-significant relationships between fibre
(as NSP) and risk but strong negative correlations be-
tween starch consumption and colo-rectal cancer risk [7].
It is thought that the RS component of dietary starch con-
fers this apparent protection and also may promote other
aspects of large bowel function.
3 Ileal Carbohydrate Digestibility and RS
Fibre polysaccharides are resistant to intrinsic human
oral, gastric and small intestinal enzymes so that, within
the limits of analytical precision, there seems to be quan-
titative entry of ingested NSP into the large bowel. In large
part, this explains the faecal bulking action of fibre-rich
products. In contrast, starch is the only polysaccharide of
natural origin which can be hydrolysed to its monomer
(glucose) by human upper intestinal amylases and asso-
ciated enzymes. Negligible quantities of starch appear in
the faeces of normal humans which is the probable rea-
son for the view that ileal starch digestibility is 100% [14].
Complete small intestinal digestion is certainly possible
for gelatinised starches where intermolecular forces are
disrupted allowing access of hydrolytic enzymes to the
amylose and amylopectin. However, there is indirect evi-
dence of long-standing that ileal starch digestibility is less
than complete [16]. With time, more information has ac-
crued that a substantial fraction of starch escapes from
the small intestine into the large bowel. This fraction is
termed resistant starch (RS), a name which derives from
in vitro studies which showed resistance of starch to en-
zymatic hydrolysis [17]. Gradually, RS has come to em-
brace all starch (and products of starch digestion) which
escapes into the large bowel of healthy humans [18].
Resistant starch has been classified into four types – RS1,
physically inaccessible; RS2, granular; RS3, retrograded;
and, RS4, chemically modified [19] (Tab. 1). This classifi-
cation is useful but very limited as these are not the only
determinants of RS. Ileal starch digestibility is affected by
a range of physiological influences which vary greatly be-
tween individuals (for a review see [14]). For example,
gender is a major variable with starch digestibility being
affected greatly by the menstrual cycle in females [20].
Similarly, food particle size is important with larger par-
ticles allowing less access of digestive enzymes to the
substrate and also having a faster oro-ileocaecal transit
time. Put simply, people who chew their food sparingly
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Starch/Stärke 55 (2003) 539–545 Resistant Starch and Health – Himalaya 292, a Novel Barley Cultivar
Tab. 1. Resistant starch types.
Resistant starch type Description
RS1 starch physically trapped within the
matrix of the food
RS2 native granular starch
RS3 retrograded or crystalline starch
RS4 chemically modified starch
are likely to experience more RS in that food than individ-
uals who do not. This is an important fundamental differ-
ence between NSP and RS. The former are defined in
terms of chemical structure but RS is measured as a
physiological outcome. Clearly, an analytical procedure
for RS needs to accommodate the full range of influences
on starch digestibility and currently there appears to be no
physiologically validated in vitro measurement. This defi-
ciency limits knowledge generation greatly [14].
4 Large Bowel Carbohydrate Fermen-
tation, SCFA and Colonic Function
Dietary digestion does not cease when food enters the
large bowel. However, the key difference between this
viscus and the small intestine is that the breakdown is ef-
fected not by human, but by bacterial enzymes. The large
bowel of humans and other omnivores such as the rat, pig
and dog is home to a large and complex bacterial ecosys-
tem. In adult humans, potential pathogens are present but
species which metabolise undigested dietary compo-
nents and endogenous secretions predominate [21]. This
complex bacterial system is understood very poorly, es-
pecially the population dynamics of the major species.
Largely this is because of the limitations of current classi-
cal technology for bacterial species identification and
enumeration which are labour intensive and time-con-
suming. It is hoped that the advent of new, molecular
technologies will facilitate the advance of knowledge in
this important area. However, there is substantial infor-
mation about the major end-products of bacterial fermen-
tation and their interactions with the host. For the bacte-
ria, carbohydrate fermentation provides energy which (to-
gether with a supply of nitrogen and other essential nutri-
ents) enables bacterial growth and proliferation. In adults,
the net reaction of the microflora has as its major prod-
ucts, some heat, inert gases (CO2, CH4 and H2) and short
chain fatty acids (SCFA) (see below) [14].
carbohydrates + H2O → acetate + propionate + butyrate
+ CO2 + CH4 + H+ + heat + more bacteria
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541
Examples
whole and partially milled cereal grains, seeds
and legumes
raw potato, green bananas, high-amylose starch-
es (e.g. Hi-maize™, Novelose 240TM)
bread, cooled cooked potatoes, Novelose 330™
etherised, esterified or cross-linked starches (e.g.
starch acetate)
In both ruminant herbivores and omnivores (including
adult humans) the principal SCFA are acetate, propionate
and butyrate. While they are end products for bacteria, for
the host they are useful metabolically and are absorbed
from the large bowel lumen and used by the viscera. This
uptake is efficient, with only 5-10% of the total SCFA pro-
duced appearing in faeces. In addition to modulating
colonic muscular activity and stimulating colonic blood
flow, SCFA appear to lower the risk of pathogen over-
growth [22]. They also enhance the absorption of fluid
and electrolytes – effects which have been used practi-
cally to control cholera-induced diarrhoea in affected chil-
dren [23]. Interestingly, it appears possible that RS con-
sumption may increase Ca2+ absorption from the large
bowel, a change of some potential significance for net
mineral bioavailability [11]. Of the principal SCFA, acetate
appears not to have any specific actions in the large bow-
el. That acetate which is absorbed is transported to the
liver via the hepatic portal vein where a significant fraction
is extracted for oxidative metabolism [24]. However, bu-
tyrate is thought to be pivotal for human colonic function.
It is a preferred metabolic substrate for isolated colono-
cytes and appears to promote growth of normal colono-
cytes and the maintenance of a normal phenotype in vivo.
In cancer cell lines (including those from tissues outside
the large bowel) butyrate promotes apoptosis (pro-
grammed cell death) in vitro. All of this evidence suggests
that butyrate may play a controlling role in colo-rectal can-
cer but such a link remains to be established in humans.
It should be noted that propionate shares many of the
physiological attributes of butyrate albeit at rather higher
concentrations [14].
One of the important features of SCFA production and ab-
sorption is their anatomical distribution along the large
bowel [14]. In essence, this organ is a tube with undigest-
ed food entering from the terminal ileum through a one
way valve (the ileo-caecal valve) and passing along to the
rectum. Bacterial inoculation occurs in the caecum and
fermentation predominates in that viscus and the proxi-
mal colon. Production slows on passage of the faecal
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542 Topping et al. Starch/Stärke 55 (2003) 539–545

Fig. 1. An overview of the relationship between transit of food through the human gastrointestinal
tract and the digestion of nutrients in the small intestine and fermentation in the caecum and colon.
Foods are rendered digestible (comminuted) by processing (milling, cooking) and by mastication in
the mouth. Digestion is also enhanced by wetting and maceration in the stomach. In the small intes-
tine, digestion occurs through the action of intrinsic enzymes, and nutrients are absorbed. Food com-
ponents and endogenous secretions not absorbed in that viscus (e.g. resistant starch, NSP) pass
through the ileocaecal valve and are fermented. Fermentation is high in the proximal large bowel as
is SCFA production. Absorption of SCFA and of water and minerals is high in this viscus. On passage
of the faecal stream, fermentation declines through substrate depletion, and SCFA concentrations
fall. The distal large colon and rectum are the regions of the large bowel with the most limited supply
of SCFA and are the sites of most pathology. Bacteria and unfermented components of low fer-
mentability are voided in the faeces.

stream through substrate depletion (Fig. 1). Reflecting
this gradient, SCFA levels are high in the proximal large
bowel and low in the distal colon and rectum as they are
absorbed and metabolised. This profile is of considerable
significance as much organic large bowel disease (e.g.
cancer) appears to be located more distally and is thought
to reflect limited SCFA supply [25].
5 Foods, RS and SCFA
Interest in the contribution of SCFA to large bowel func-
tion has stimulated research into the relationships be-
tween RS and other fermentable carbohydrates and
health. One of the key investigative outcomes is the dif-
ferentiation between NSP and RS in their mechanism of
action. Although the former can be degraded by the mi-
croflora, and some (e.g. gum arabic, pectin) have high
fermentability, most resist fermentation to a greater or
lesser degree and some insoluble NSP (e.g. cellulose)
are excreted almost completely [14]. This explains the rel-
ative efficiency of insoluble NSP sources as faecal bulk-
ing and laxating agents. In contrast, the fermentability of
RS is generally very high which makes them relatively
poor laxatives. Thus, effects of RS are mediated through
their metabolic products rather than their physical pres-
ence so that SCFA become one of the key biomarkers for
RS action.
There seems to be a good case for an improvement in
bowel health and function with greater RS consumption.
However, the lack of a suitable analytical method means
that, unlike dietary fibre (or NSP), there is no target figure
set for daily intake. Quite reasonably, it is inferred that RS
intakes in westernised countries are inadequate (because
starch intakes are low) and public health efforts are under
way to increase total starch consumption. Of itself, this
will increase RS intake but there is some evidence that
the foods consumed in these westernised countries may
differ from those in low risk societies. For example, stale
cooked maize porridge is a staple dish for native South
Africans. This product is very likely to be high in retro-
graded starch (RS3). Indeed, it has been shown that its
consumption leads to much higher levels of colonic
SCFA, including butyrate compared with fresh maize
starch [26]. The latter increase is, potentially, a very im-
portant one in view of the putative role of butyrate in nor-
mal colonic function. Some in vitro studies suggest that
RS fermentation by faecal bacteria leads preferentially to
butyrate production [27]. This may not be universally true
as the faecal microflora of some humans seem incapable
of metabolising certain forms of RS [28].

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Starch/Stärke 55 (2003) 539–545 Resistant Starch and Health – Himalaya 292, a Novel Barley Cultivar
As a generalisation it appears to be the case that con-
sumption of high RS foods leads to greater SCFA produc-
tion. Much of the work on which this conclusion is based
has been carried out in animals for the simple reason that
only faecal measures are available routinely in humans
and these are not good indicators of total SCFA availabil-
ity in the colon. While the rat has been used extensively
for dietary studies, the data are limited due to the sub-
stantial differences in gastrointestinal physiology between
rodents and humans [14]. The pig is a better model for hu-
man large bowel physiology and studies in this species
have shown higher large bowel SCFA with consumption
of certain foods. At equivalent levels of dietary fibre, foods
such as navy beans and whole brown rice give much
greater large bowel SCFA than other foods (e.g. wheat
bran, rice bran) fed at equivalent levels of dietary fibre or
NSP (Tab. 2) [11, 29, 30]. The disparity has been ascribed
to RS and is sufficient to make very substantial increases
in the net “fibre” content of those foods. Indeed, RS is now
recognised as a component of dietary fibre in foods in
Australia.
Tab. 2. Comparison of the effects of high fibre diets low
(wheat bran) and high (navy beans) in resistant starch on
total colonic short chain fatty acid pools in pigs.
Dietary Fibre Total SCFA % increase
treatment intake pool in SCFA
[g/d] [mmol] pool
Low fibre control 14.1 14.1
Wheat bran 42.1 32.2 128
Navy beans 44.6 60.0 326
6 Crops, Foods, Food Modification and RS
RS occurs in relative abundance in a narrow range of
crops and foods including unripened banana, cooked and
cooled potato or rice, pulses, whole grain (brown) rice etc.
Therefore the identification of diverse sources of RS that
can be incorporated into diets at the population level is an
important area for research and development. At the crop
plant level three of the four types of RS can potentially be
increased directly or indirectly through a range of mech-
anisms. For example, it may be possible to make starch
more physically inaccessible (i.e. to increase RS1) by
breeding grain cultivars that maximise this characteristic
through changes to grain structure. Resistant starch gran-
ules (RS2) are found in plants such as legumes and ba-
nanas where an unknown mechanism results in resis-
tance to digestion in the small intestine. High amylose
starches that resist digestion occur in specific genotypes
in a range of crops and are best characterised in amylose
extender maize [17, 31]. While starches containing amy-
lose can have the levels of resistant starch increased by
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543
processing techniques such as thermal cycling, high amy-
lose starches are likely to yield the highest levels of RS3
by this process and by retrogradation because of the en-
hanced ability of the amylose in such starches to form ret-
rogradation-derived complexes. Genetic strategies for re-
ducing branching enzyme activity have been targeted for
the development of high amylose crops, through either
mutation breeding or through GMO technologies.
There seems to be little information on the RS content of
convenience foods but these are likely to be low in RS,
because nutritional trials with high RS foods at modest
levels of dietary inclusion raise faecal SCFA excretion
substantially relative to the same foods without added RS
[31]. Increased consumption of starchy foods raises RS
intake by default. However, there seems to be good rea-
son to anticipate consumer resistance to the significant
dietary changes required to increase RS substantially, at
least in the short term. One strategy which has been
adopted in Australia is the fortification of existing conve-
nience foods with RS in the form of a high amylose starch.
High amylose starches are slower to gelatinise than con-
ventional starches and quicker to retrograde. Thus, these
starches, as are and the foods into which they are incor-
porated, are higher in RS through the presence of RS2
and also, after processing and cooling, retrograded starch
(RS3). The range of commercial foods containing this
starch includes breads, other bakery products and break-
fast cereals. Consumption of the starch alone (i.e. as the
ingredient used in food processing) by pigs raises large
bowel and faecal SCFA, consistent with greater fermenta-
tion [32]. Nutritional trials have established that consump-
tion of the enriched bakery products by volunteers leads
to a mild enhancement of laxation and a substantial in-
crease in faecal total SCFA and butyrate excretion [31]. In
studies in pigs, the same starch has been shown to func-
tion as a prebiotic with substantial increases in faecal
numbers of a probiotic bacterium compared with a con-
ventional (low amylose) maize starch [33].
7 Himalaya 292 – a Novel Barley Cultivar
It must be recognised that the potential range of products
which can be enriched with high amylose starch could be
rather restricted. This presents a major opportunity for
product innovation by the food industry through food pro-
cessing and through plant breeding.
One avenue which is being investigated by CSIRO in as-
sociation with Ascentia Pty Ltd is based on a novel hull-
less barley cultivar, Himalaya 292 (Hordeum vulgare, var.
himalaya 292) [34]. This variant was a product of a chem-
ical mutagenesis program and has a single nucleotide
change in the gene encoding starch synthetase IIa (EC
2.4.1.21). As expected, this loss of enzyme activity leads
www.starch-journal.de

544 Topping et al.
Tab. 3. Selected nutritional components of Barleyplus™.
g/100g
Himalaya 292 Standard barley
Total fibre 25 14
β-Glucan 10 5 of the grains and their food products.
Simple sugars 6 2
Lipids 8 2
Total starch 27 55
% Amylose 71 25
to a shrunken grain with a lower total starch content. How-
ever, the unexpected finding from this work was that the
relative proportion of amylose in the endosperm is much
higher (~70% of total starch) than in the parent strain, re-
flecting the block in amylopectin synthesis. Surprisingly,
this specific loss of enzyme activity also leads to other
beneficial compositional changes including a higher con-
tent of total and soluble non-starch polysaccharides
(NSP) (Tab. 3). These changes could increase the resis-
tant starch (RS) content of the grain. Studies in rats with
heat-stabilised flour have confirmed greater excretion of
starch into the large bowel of rats, consistent with more
RS [Bird, Flory, Davies, Usher, Topping, unpublished
work]. Other studies have shown higher large bowel
SCFA in pigs and also a lower glycaemic index in human
volunteers consuming foods containing the processed
grain (Fig. 2). Further exploration of this novel cultivar is
Fig. 2. Response of mixed venous blood glucose concen-
tration following consumption by humans of a breakfast
cereal made from Himalaya 292 barley, a standard hull-
less barley breakfast cereal, or a glucose drink, each con-
taining 50 g carbohydrate.
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Starch/Stärke 55 (2003) 539–545
underway, but it appears to be capable of being
processed into a range of convenience foods relatively
easily. The research and development program incorpo-
rates breeding into elite varieties and a comprehensive
evaluation of the compositional and nutritional attributes
8 Conclusion
The case for increasing RS consumption in populations at
risk remains to be proved definitively for colo-rectal can-
cer. Nevertheless, the benefits of RS for other important
aspects of large bowel health, such as improved mineral
uptake appear to be well-justified. Meeting the needs of
consumers and improving public health through the pro-
duction of modified foods needs the active collaboration
of science and industry. Himalaya 292 is an example of
this partnership and is a developing collaboration be-
tween plant geneticists, agronomists, food technologists
and health scientists. Shortly, we hope that this alliance
will include food industry so that the potential social and
economic benefits of the novel grain can be realised.
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(Received: April 9, 2003)
(Accepted: September 16, 2003)
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