domingo, 19 de febrero de 2012

Cereales integrales salud inglés

Journal of Cereal Science 46 (2007) 220–229

Cereal complex carbohydrates and their contribution to human health

David Topping

Food Futures and Preventative Health National Research Flagships, CSIRO Human Nutrition, Kintore Avenue, Adelaide, SA 5000, Australia

Received 25 January 2007; received in revised form 10 May 2007; accepted 13 June 2007


Population studies have shown that whole grain consumption is associated with diminished risk of serious, diet-related diseases, which

are major problems in wealthy industrialised economies and are emerging in developing countries with greater affluence. These

conditions include coronary heart disease, certain cancers (especially of the large bowel), inflammatory bowel disease and disordered

laxation. Carbohydrates are important contributors to the health benefits of whole grains. Insoluble non-starch polysaccharides (NSP,

major components of dietary fibre) are effective laxatives. Soluble NSP (especially mixed-link
b-glucans) lower plasma cholesterol and so

can reduce heart disease risk but the effect is inconsistent. Processing seems to be an important contributor to this variability and other

grain components may be involved. However, starch not digested in the small intestine (resistant starch, RS) appears to be as important

as NSP to large bowel function. Dietary analysis suggests that some populations (e.g. native Africans) at low risk of diet-related disease

through consumption of unrefined cereals may actually have relatively low fibre intakes. While NSP are effective faecal bulking agents,

they are fermented to a very variable extent by the large bowel microflora. In contrast, RS seems to act largely through the short chain

fatty acids (SCFA) produced by these bacteria. One SCFA (butyrate) appears to be particularly effective in promoting large bowel

function and RS fermentation appears to favour butyrate production. Animal studies show that dietary RS lowers diet-induced

colonocyte genetic damage and chemically-induced large bowel cancer which correlates with increased butyrate. These effects could

contribute to a lower risk of cancer and ulcerative colitis in the long term. Cereal grain oligosaccharide (OS) may also function as

prebiotics and increase the levels of beneficial bacteria in the large bowel. Understanding the relationships between NSP, RS and OS and

large bowel health will be facilitated by the advent of new molecular technologies to identify the bacterial species involved. The potential

for improvements in public health is considerable.

2007 Elsevier Ltd. All rights reserved.

Starch; Oligosaccharides; Non-starch polysaccharides; Cereals; Human health; Resistant starch

1. Introduction

Cereal-based foods have been staples for humans for

millennia. Cereal grains contain the macronutrients (protein,

fat and carbohydrate) required by humans for growth

and maintenance. They also supply important minerals,

vitamins and other micronutrients essential for optimal

health. However, it is becoming apparent that cereals in

general have the potential for health enhancement beyond

the simple provision of these nutrients and that their

consumption can lower the risk of significant diet-related

diseases quite substantially. This is an important attribute

given the social and personal impact of these conditions.

Morbidity and mortality from non-infectious diseases are

significant problems in affluent, developed economies and

include cardiovascular disease (CVD), Type 2 diabetes and

colo-rectal cancer (
Jemal et al., 2005). Diet and lifestyle are

modifiable risk factors for these conditions and prevention

is an accepted strategy for lowering their socio-economic

impact. Risk of these illnesses is exacerbated by obesity

and there is evidence that they are emerging as serious

issues in developing countries through greater affluence


0733-5210/$ - see front matter
r 2007 Elsevier Ltd. All rights reserved.


CHD, coronary heart disease; CD, Crohn’s disease; CVD, cardiovascular disease; FOS, fructo-oligosaccharides; GO, galactooligosaccharides;

GR, glycaemic response; IBD, inflammatory bowel disease; LAB, lactic acid bacteria; LDL, low-density lipoprotein; NSP, non-starch

polysaccharides; OS, oligosaccharides; RS, resistant starch; SCFA, short chain fatty acids; TDF, total dietary fibre; UC, ulcerative colitis

Tel: +618 8303 8930; fax: +618 8303 8899.

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resulting from industrialisation (
Mascie-Taylor and Karim,


Much of the impetus for the interest in cereals and health

(i.e. disease prevention) has come from human population

studies comparing the consumption of whole grain

products with refined cereal foods. In the former, most

(or all) of the pericarp-seed coat, aleurone and germ (and

their fibre, micronutrients, fat and protein) are retained

while they have been removed by milling and processing in

refined foods, leaving the starchy endosperm. Population

studies have shown that whole grain foods have a

considerable advantage over refined products in the

prevention and management of diet-related diseases. Large

prospective studies have shown that consumption of whole

grain products is associated with lowered risk of CVD and

diabetes (
Jacobs and Gallaher, 2004). Greater intake of

whole grain foods is associated also with lesser obesity

Koh-Banerjee et al., 2004; Liu et al., 2003). The protective

value of whole grains and some of their components (such

as antioxidants) will be discussed elsewhere in this issue of

the journal. However, it should be noted that attempts to

identify the factor(s) in whole grain component which

mediate their health benefits have been unsuccessful. Two

hypotheses have been proposed to account for this

conundrum (
Jacobs and Gallaher, 2004; Topping et al.,

). The first is that the whole grains contain a complete

portfolio of bioactive components which provide comprehensive

protection for the major diseases which have been

identified in population studies (
Jacobs and Gallaher,

). This is the ‘‘whole grain package’’ model. The

alternative is that whole grains possess a general characteristic

(and not specific components) which offers

comprehensive protection and it has been suggested that

a lower small intestinal digestibility of whole grain foods

could be responsible (
Topping et al., 2007). This would

translate to less metabolisable energy, lower glycaemic

response (GR) and more resistant starch (RS). The two

hypotheses are not mutually exclusive and were framed to

account for the fact that while the effects of whole grain

components (e.g. fibre) on biomarkers of disease risk (e.g.

plasma cholesterol) have been shown, the whole seems to

be greater than the sum of the parts. It is not clear if either

hypothesis is correct but it is known that many of the

health-promoting components of intact cereal grains are

lost on refining. However, it must be remembered that

some processing is essential for palatability, safety and

adequate nutrient bioavailability. Wheat bran provides a

ready example of this latter point. It contains both the

pericarp-seed coat and the aleurone layer. Of these two, the

latter is a rich source of nutrients including vitamins such

as folate. However, most of this folate is not bioavailable in

unprocessed bran and only when the aleurone layer is

isolated and disrupted does it become so (
Fenech et al.,

). The application of advanced technology to enhance

the value of a cereal by-product is an example of the

opportunities to maximise the health potential of grains.

This paper is directed at reviewing the relationships

between cereal grain components and human health, to

identify those which mediate important health effects and

the opportunities available to optimise them.

2. Grain carbohydrates and human health

It is abundantly clear that identifiable grain components

have specific effects which improve health and lower

disease risk. The prime focus of this paper will be on

cereal carbohydrates—especially polysaccharides—as they

are an emerging area of research and development in which

considerable effort is being expended on manipulating their

levels and composition in grains to optimise the human

health potential of processed foods. Of course, it must be

recognised that this overview is general in nature and

cannot go in very great depth into individual cereals save

those which are staples.

Dietary carbohydrates can be divided very simply into

two major groups solely on the basis of their susceptibility

to digestion by human small intestinal enzymes. Humans

possess a suite of small intestinal digestive enzymes but

only one (
a-amylase) that can attack a complex carbohydrate.

This enzyme can hydrolyse only one significant

dietary polysaccharide—starch. This specificity depends on

the presence of
a-1,4 glucosidic links in the target

polysaccharide. All of the other major complex carbohydrates

(oligosaccharides (OS) and non-starch polysaccharides

(NSP)) seem to resist human small intestinal enzymic

digestion completely. Indeed, this property became the

basis of the definition of dietary fibre as ‘‘plant structural

and exudative components not digested by human digestive

enzymes’’ (
Spiller, 1993). This resistance is by virtue of a

lack of the appropriate linkages and/or the presence of

non-glucose monomers in the target oligomer or polymer.

NSP are the principal components of dietary fibre and the

lack of small intestinal digestibility explains their principal

physiological properties. However, NSP can be subdivided

further on the basis of their aqueous solubility into soluble

and insoluble NSP. It must be emphasised that this

solubility may be demonstrated under conditions which

do not occur in the human small intestine (
Topping, 1991).

Nevertheless, the terms ‘‘soluble fibre’’ and ‘‘insoluble

fibre’’ have entered into common usage and also serve to

segregate NSP on one of their best documented physiological

effects—lowering of plasma cholesterol, an established

risk factor for CVD (
Clearfield, 2006). Of the other

carbohydrates found in physiologically significant quantities

in some grains, OS are a relatively unknown quantity

in terms of the health benefits of cereals. They contribute to

the dietary fibre content of grains and may have health

benefits. For example, OS extracted from Belgian endive

(chicory) or obtained as dairy by-products have found use

in food manufacture as prebiotics, i.e. agents used to

stimulate the activity and viability of bacteria thought to

promote human health (probiotics) (
Gibson and Roberfroid,



D. Topping / Journal of Cereal Science 46 (2007) 220–229

Starch is the most important polysaccharide in nearly all

seeds (including legumes) grown and used for human

foods. The most notable exception is soy, which does not

contain starch to any significant level. Hitherto, starch has

been regarded largely as a source of energy and of little

additional value. However, it is becoming clear that

controlling small intestinal starch digestibility (both in

terms of its rate and extent) offers very significant

opportunities for health delivery. Slowing starch digestion

leads to a lower glycaemic response (GR) while reducing

total small intestinal amylolysis increases RS. This is an

area of major research and development effort. For

example, CSIRO is investing substantially in generating

cereal grain cultivars (wheat and barley) which are lower in

GI and higher in RS (see
Morell et al., 2003; Regina et al.,

). These cereals are higher in amylose than standard

ones and build on the successful precedent of high amylose

maize starch which has been used to develop high RS foods

Brown, 2004). Amylose is slower to gelatinise and quicker

to retrograde than amylopectin and so gives processed food

products which are higher in RS. It is intended that these

grains will be used to make a wider range of foods with

substantiated health benefits than is feasible with high

amylose maize starches. The availability of advanced

molecular technologies to engineer new cultivars is facilitating

this progress greatly.

3. Dietary fibre and health outcomes

It is essential that any potential health benefits of foods

or food components be substantiated to ensure their

effectiveness and sustain consumer confidence. For dietary

fibre there are two specific instances where the positive

outcomes of greater consumption have been established—

laxation and plasma cholesterol reduction.

3.1. NSP and laxation

Much of the present interest in the health properties of

dietary fibre can be said to have started with the pioneering

work of Burkitt and co-workers in Africa (
Burkitt, 1973).

They noted that native (black) Africans were at much lower

risk of what have become known as the ‘‘diseases of

affluence’’ than Europeans living in the same environment.

The difference was ascribed to the greater consumption of

unrefined foods by the natives. With time, research

emphasis shifted to the apparently greater fibre content

of these foods and the development of the so-called

‘‘roughage’’ model of dietary fibre (
Topping and Illman,

). This model hinges on the resistance of NSP to

human small intestinal digestive enzymes which helps to

explain the well-recognised dose-dependent effects of fibrerich

foods in increasing faecal bulk. This bulking is taken

as the mechanism of action of what is probably the bestdocumented

effect of dietary fibre—promotion of regularity.

The pioneering study of Baghurst and colleagues

showed conclusively that increased fibre (including cereal

fibre) consumption relieved simple constipation in a group

of institutionalised elderly people (
Baghurst et al., 1985)

Table 1). These individuals had a high frequency of

laxative use which was abolished completely in a short time

period by increased consumption of fibre, mainly cereal

foods high in insoluble NSP. Diverticular disease is a

herniation of the large bowel and is associated with chronic

constipation. Analysis of data from a large prospective

study has shown strong, dose-dependent protection against

this condition by dietary fibre (
Aldoori et al., 1998).

These bulking effects of fibre are greatest with cereal

fibre, especially products high in insoluble NSP (such as

wheat bran) (
Topping, 1998). Soluble NSP are generally

less effective in increasing stool mass. A study from

Heaton’s laboratory has shown that the laxative effect of

fibre is substantially through greater faecal mass (and not

any other effect) as consumption of indigestible plastic

‘‘bran’’ flakes promoted laxation and increased stool

output (
Lewis and Heaton, 1997). This important experiment

shows that NSP can relieve an important problem

solely by its physical presence. The actual quantity of fibre

required for the effect is not certain but would seem to be

between 20 and 25 g/person/d. What is clear is that surveys

show that fibre intakes in many developed countries are

generally low but relatively high in some others (e.g.

Australia) (
Baghurst et al., 1996). Clearly, there is an

opportunity to effect a substantial improvement in public

health by increasing fibre intakes. Whether there is scope

for engineering cereal polysaccharides to improve laxation

is to be determined. However, the very low fibre intakes in

many countries (e.g. the US) provide an opportunity for

the food industry to improve public health.

3.2. Soluble NSP and plasma cholesterol

Consumption of whole grains is associated with a

lowered risk of coronary heart disease (CHD) (

and Gallaher, 2004
). CHD is a disease characterised by

infiltration of lipoprotein cholesterol into the major arteries

of the heart. This process (atherosclerosis) leads to a

progressive occlusion of the circulation resulting in

impaired cardiac function and, if unchecked, tissue necrosis

and death. CHD has a number of risk factors (such as age

and gender) which cannot be altered. Modifiable risk

factors include smoking, physical activity and raised

plasma low-density lipoprotein (LDL) cholesterol. LDL


Table 1

Effects of increased fibre consumption on laxative use by institutionalised

elderly people





(laxative) use





Average time to

stop aperient use


Baseline 13.9 1.3 0.9

End 25.4 0 1.4 5.4

: Baghurst et al. (1984).

D. Topping / Journal of Cereal Science 46 (2007) 220–229

is the major plasma vehicle for transporting cholesterol to

the tissues and its connection to atherosclerosis is fairly

self-evident. Preventive strategies for CHD include cessation

of smoking, dietary modification, exercise and other

lifestyle changes. Lowering of LDL cholesterol is also an

extremely important line of attack and large scale intervention

studies have shown that drugs which lower plasma

total and LDL cholesterol are effective in reducing CHD

events (
Clearfield, 2006). Chief among these are a group of

agents known collectively as the statins. They appear to act

by inhibiting cholesterol synthesis and their potency has

been recognised in a number of trials which have shown

significant reductions in coronary deaths. Their effectiveness

has accepted to the point where statins are now

available as over the counter (i.e. non-prescription)

medication in pharmacies in the United Kingdom (


While drugs are effective, they are also expensive and

diet is a much cheaper avenue. A portfolio diet approach

has been tested whereby food intake is modified to

accommodate a number of features known to lower

CHD risk and has been shown to have positive impacts

on biomarkers, including LDL cholesterol (
Jenkins et al.,

). The effectiveness of this approach has to be

quantified relative to drugs. Nevertheless it does hold

promise for non-drug control of a serious disease.

The potential of grain components to assist in risk

reduction is fairly self-evident, given the relationship

between whole grain consumption and lowered CHD risk.

However, there has been some confusion both as to the

active agent and the means of protection. It was thought

originally that dietary insoluble fibre was responsible,

acting by lowering plasma cholesterol. The proposition was

based on the observations that plant fibre concentrates and

isolates bound bile acids
in vitro. This binding is similar to

that of a synthetic resin (cholestyramine) which has been

used to lower plasma cholesterol in patients with high LDL

levels (
Okolicsanyi et al., 1986). Bile acids are surfaceactive

steroids synthesised from cholesterol in the liver and

are secreted into the gut (in bile) where they assist in lipid

digestion and absorption. These acids are conserved

through the enterohepatic circulation whereby they are

reabsorbed from the terminal small intestine and returned

to the liver. Interruption of this cycle leads to greater faecal

loss with the deficit leading to increased hepatic cholesterol

catabolism and a fall in plasma LDL concentrations. The

attractive hypothesis that insoluble NSP (or lignin) bound

bile acids has not translated to an effective lowering of

LDL in human or animal trials. Indeed, it has been known

for some considerable time that the effect may be an

artifact of the procedures used to isolate lignin (

and Oakenfull, 1981
). However, it has been established that

cereals high in soluble NSP can lower plasma cholesterol

effectively. At the least, these reductions are of the order of

3–5% and are obtained through the consumption of foods

in quantities which consumers are likely to eat (e.g.

et al., 1990
). The lowering of total and LDL cholesterol has

been demonstrated particularly with oats and to a lesser

extent, barley (
Truswell, 2002). Both cereals contain

soluble NSP
b-linked glucans which are thought to be the

active agents (
Dikeman and Fahey, 2006). Studies in

humans and animals have shown reductions with isolated

glucans supporting this hypothesis. However, it must be

recognised that there are some contradictory data with

glucan enriched fractions (
Keogh et al., 2003). The reasons

for this uncertainty are very important and may reflect

isolation procedures and food production procedures

among other factors. Glucans (and other soluble NSP

such as psyllium) are thought to modulate digestion

through their viscosity in solution (
Dikeman and Fahey,

). The higher viscosity is believed to slow the flow of

digesta which would delay fat absorption and the

reabsorption of bile acids. This viscosity is also thought

also to contribute to the effects of soluble NSP on the

absorption of other nutrients eg glucose. Loss of this key

physico-chemical property on isolation is a distinct


One of the paradoxes in the relationship between cereals

and CHD is the relationship between whole greater whole

grain intake in general and a dose-dependent lowering of

risk. These whole grains include wheat and rye, i.e. grains

not high in soluble NSP. Moreover, wheat fibre in general

and wheat bran in particular does not seem to affect

plasma cholesterol (
Truswell, 2002). Indeed, in some

studies wheat bran has been used as a control fibre

while some animal dietary studies suggest that wheat bran

can actually raise plasma cholesterol relative to baseline

Topping et al., 1993). This may be a result of

processing as Kahlon and colleagues (
Kahlon et al., 2006)

have obtained some very interesting data from animal

studies suggesting that milling and extrusion could modify

the properties of wheat bran so that it lowers plasma

cholesterol. Clearly, this work needs to be repeated in

humans as it offers the opportunity to modify a cheap and

plentiful ingredient favourably. Processing differences may

also account for the fact that oat bran products were

shown to lower plasma cholesterol in trials in Australia

Kestin et al., 1990) but not New Zealand (Truswell, 2002)

despite the fact that the products were supplied by the same


In the only randomised controlled trial of the effects of

dietary fibre, a supplement containing wheat bran did not

prevent re-infarction in men with a prior history of CHD

Burr et al., 1989), although the validity of this trial has

been questioned (
Truswell, 2002). Clearly, there is an

opportunity to modify cereal grains through breeding and

processing to maximise the effect and make it more


While it is abundantly clear that specific grain components

have physiological effects which improve health and

lower disease risk, not all of the benefits can be directly

linked. It is possible that fibre alone does not account for

the protection against CHD afforded by whole grains and

cereal foods. The incomplete small intestinal digestion of


D. Topping / Journal of Cereal Science 46 (2007) 220–229

starch is emerging as a potentially positive factor. We have

proposed that the small intestinal digestibility of whole

grains is limited compared with that of highly refined foods

Topping et al., 2007). This leads to reduced absorption

of glucose in the small intestine and the passage of

more starch into the large bowel. In the case of the large

bowel, RS is fermented by the resident bacteria with

the production of substantial quantities of end products

(short chain fatty acids, SCFA) with specific health

promoting attributes. This proposal is supported by a

body of experimental and population data on humans and


4. Starch and human health

Significant interest in the health promoting potential of

cereal grain food foods began largely with observational

studies of native populations such as those of Burkitt and

colleagues in East Africa. These populations consumed

diets high in unrefined cereals (in this case maize) and were

at much lower risk of the diseases of affluence which

affected Europeans living in the same environment but who

ate highly refined foods. As noted earlier, attention became

directed specifically on the fibre content of these foods

which was assumed to be high relative to that in European

diets. The development of improved methodologies to

measure plant polysaccharides has given much greater

specificity and reliability to their assay. Application of

these techniques to staple African and European foods

showed that although the former did eat unrefined

products, their fibre intakes were actually lower than those

of the high risk Europeans (
Segal, 2002). The paradox

between food consumption and relative risk can be

reconciled by the facts that the African ate considerably

more unrefined starch than the Europeans and that

their cooking and practices were rather different. In

particular, the Africans ate maize porridge, which had

been cooked in water and then cooled and stored for some

time.While cooking increases the digestibility of starch and

other nutrients, the cooling and storage leads to retrogradation

of starch and the formation of RS. Retrogradation

refers to a self-association of starch chains to

form aggregates which resist digestion by

Human studies have confirmed that the stored cooked

maize gruel was high in RS relative to the fresh product

Ahmed et al., 2000).

The importance of controlling the rate of small intestinal

starch digestion to lower the GR is accepted. However, it is

emerging that controlling the extent of starch digestion can

also have a major impact on health outcomes. Indeed, it

appears that slower (and less complete) small intestinal

starch digestion may be more important than fibre itself in

this regard. This is not to discount the benefits of NSP but

to add a further dimension to the health benefits of cereal

polysaccharides. Indeed there is evidence that, for optimal

large bowel health, combinations of RS and NSP may be

optimal (
Muir et al., 2004).

5. RS, lowered small intestinal starch digestibility and

human health

The explanation for the relative lack of recognition of RS

as a health-related food component is probably quite simple.

Firstly, starch has the potential to be hydrolysed completely

to glucose in the small intestine. This, plus the absence of

detectable levels of starch in normal human faeces led to the

natural conclusion that no starch entered the large bowel,

despite long-standing evidence to the contrary. Levitt and

colleagues (
Anderson et al., 1981) showed that breath H2

evolution was increased following consumption of modern

convenience (i.e. highly processed, low fibre) starchy wheat

foods. H
2 is produced in the body of humans and other

mammals principally through intestinal bacterial carbohydrate

fermentation. In omnivores, this fermentation occurs

principally in the large bowel. These data point to an

important difference between RS and NSP. The effects of

the latter are explicable largely (but not exclusively) through

their indigestibility. In contrast, the net intestinal digestibility

of RS is high and their action is substantially via the

products of their fermentation by the large bowel microflora.

The human caecum and colon are home to a

numerically large, taxonomically diverse and metabolically

active, bacterial population. Most of the bacteria in adult

humans are non-pathogenic and ferment unabsorbed dietary

carbohydrates. These organisms resemble those found in

the large bowel of obligate herbivores in metabolic capacity

and end products, i.e. gases (H
2, CO2 and CH4) and short

chain fatty acids (SCFA). As in herbivores, the principal

acids are acetate, propionate and butyrate and, as in those

animals, they make a significant contribution to metabolism

and to the optimal functioning of the viscera.

6. SCFA and health effects of complex carbohydrates

There have been a number of significant developments in

understanding the relationships between cereal components

and human health. One of these is the appreciation

that many of the health benefits of complex carbohydrates

accrue from the SCFA produced in the large bowel

Topping and Clifton, 2001). SCFA have a number of

general effects including the direct acidification of digesta

contents. This lowering of pH leads to the ionisation of

potentially cytotoxic compounds including biogenic amines

and ammonia (
Visek, 1978). Ammonia is a potential

carcinogen and is produced in the large bowel from urea

through the action of urease. Free NH
3 is absorbed from

the lumen into colonocytes whereas NH

is not. A

reduction of one pH unit (which has been observed within

the porcine large bowel with feeding of fermentable

carbohydrate) would lower ammonia absorption by

90%—an effect of considerable potential importance.

Lowering of pH has also been proposed as a mechanism

for preventing the overgrowth of potentially pathogenic

bacteria. However, this effect has been shown
in vitro but

not yet
in vivo.


D. Topping / Journal of Cereal Science 46 (2007) 220–229

SCFA are absorbed on passage of the faecal stream and

less than 10% of those produced appear in excreted faeces.

The absorbed SCFA are metabolised by the viscera and

contribute to their energy needs. While the acids make this

general metabolic contribution, one SCFA in particular has

attracted considerable interest for its potential to promote

large bowel health. This acid is butyrate and there is a

substantial body of literature showing that its role is pivotal.

Butyrate is the preferred metabolic substrate for colonocytes.

Its metabolism is thought to drive the uptake of

cations and water leading to water salvage. There is good

circumstantial evidence that this may be of importance in

controlling bacterial infections as well as in the normal

colon. Incorporation of RS (as high amylose maize starch)

into the oral rehydration solution accelerates recovery and

lowers net water loss in patients with watery diarrhoea

Ramakrishna et al., 2000). Butyrate is also believed to

promote a normal phenotype in colonocytes through the

repair of damaged DNA and induction of programmed cell

death (apoptosis) in transformed cells. These actions are

thought to lower the risk of colo-rectal cancer and have been

shown in cultured transformed cells. SCFA have a number

of other positive effects on large bowel health with butyrate

being the most potent. These actions include modulation of

muscular contraction and relaxation of resistance blood

vessels in the splanchnic bed. This latter effect allows for

greater tissue perfusion and O
2 supply.

7. Cereal carbohydrates and large bowel health

Clearly, there is considerable potential for cereal grains

to promote large bowel health through their complex

carbohydrates, especially RS. There are several areas where

this potential can be applied. However, before examining

those issues, it must be noted that RS has a significant basic

attribute which can impact on human health, i.e. its lower

metabolisable energy. The bacterial digestion of starch is

intrinsically less efficient than that of the human small

intestine. This means that the energy available to the host

as SCFA and any other products is less than 50% of the

glucose absorbed in the small intestine (
Livesey, 1990).

This has obvious implications for the control of obesity,

itself a risk factor for diet-related disease (especially

diabetes) and it may be that the protection against CHD

could be indirect via this mechanism. It should be noted

that soluble NSP may have a role to play in modulating the

RS content of grains. A study in rats showed that a wheat

of low metabolisable energy (measured in chickens) had an

apparently high content of RS. This difference was

ascribed to its marginally higher level of soluble NSP

Choct et al., 1998). This relationship is yet to be examined

in any systematic fashion.

7.1. Colo-rectal cancer

Large bowel cancer is a major internal malignancy in

affluent industrialised countries and, as noted earlier, it is

becoming an important cause of morbidity and mortality

in emerging countries with greater affluence. The early

human population studies indicated a protective role of

complex carbohydrates, especially dietary fibre, in this

disease. Based on these historical observational reports it

was expected that dietary fibre would emerge as a strong

protective agent. This has proved to be rather more elusive

than could have been anticipated. The laboratory data are

supportive of fibre and studies in rodents with experimentally

induced large bowel cancer have shown a protective

role for products high insoluble in NSP such as wheat bran

Zoran et al., 1997). Some prospective population

studies have shown that whole grain consumption was

protective against this malignancy in a dose-dependent

manner (
Larsson et al., 2005). However, the effect is not

consistent and a meta-analysis of such studies failed to

show any reduction in cancer risk with greater fibre intake

Park et al., 2005). Interventions in individuals with a

predisposition to colo-rectal cancer such as adenomatous

polyps have also failed to show any effect of dietary fibre

supplements on polyp recurrence after surgical removal

Schatzkin et al., 2000).

However, our increasing knowledge of plant carbohydrates

and their effects on gut physiology suggests that a

reappraisal may be timely. The original premise for fibre

action was that it was indigestible by human small

intestinal enzymes. However, it is apparent that RS makes

a significant contribution to large bowel fermentation.

There is evidence of a similar degradation of some NSP in

some foods (e.g. in cabbage) but not necessarily those in

cereals (
Stephen and Cummings, 1980). Given the role of

the SCFA produced by this fermentation in large bowel

health, it seems appropriate to factor these considerations

into the relationship between dietary intakes and disease

risk. Human and animal feeding trials have shown a

substantial increase in large bowel and faecal SCFA,

including butyrate, on consumption of RS in a variety of

foods (for a review see
Topping and Clifton, 2001). Indeed,

it is thought that RS fermentation by the large bowel

microflora favours the production of butyrate above other

SCFA. Studies in rodents with chemically induced large

bowel cancer have shown significant protection with the

feeding of RS as high amylose starch (
Le Leu et al., 2005).

Genomic damage is a pre-requisite for carcinogenesis and

we have shown that high levels of dietary protein induce

DNA strand breaks in colonocytes in rats in vivo. This is

reversed by RS in a dose-dependent manner with a close

negative correlation between higher large bowel butyrate

concentrations and the level of damage (
Toden et al., 2007)

Fig. 1). These data are consistent with a meta-analysis of

nutrient intakes which showed that greater consumption of

protein (and fat) were correlated positively with colo-rectal

cancer risk. Starch (and RS) intakes were protective but

NSP had no relationship to risk (
Cassidy et al., 1994). NSP

are the main components of dietary fibre so that this

absence of a protection accords with the prospective

population data. However, there is inconsistency in the


D. Topping / Journal of Cereal Science 46 (2007) 220–229

epidemiological data notably the demonstration of dose

dependent, protection by dietary fibre in a large, multicentre

European prospective study (
Bingham et al., 2003).

This can be reconciled with the other work when one

considers the measures of fibre intake. The total dietary

fibre (TDF) method used to analyse foods to estimate

intake includes not only NSP but also a fraction of RS.

There is no accepted method to determine RS which has

been applied to foods so that the TDF provides the only

measure of its intake, albeit incomplete. It follows that

TDF may be an indirect measure of RS intake and that

this, rather than NSP alone may be a major part of the

protective agency. Of course, there are no data as yet to

support this proposition and prospective and intervention

studies are needed to establish any such benefit.

7.2. Gut microbiology, inflammatory bowel diseases and


The large bowel fermentation of RS and a variable

fraction of NSP alter the landscape of the relationship

between diet and health. Instead of considering carbohydrates

solely in terms of small intestinal digestibility and

physical faecal bulking, the relationship between the

microflora and SCFA and their role in health becomes

much more significant. This may assist in examining the

data in relation to other diseases as well as cancer. For

example, inflammatory bowel diseases (IBD) are a

significant socio-economic cost in developed countries

(e.g. Germany,
Stark et al., 2006). There are two main

variants of IBD-Crohn’s disease (CD) and ulcerative colitis

(UC). UC is generally located in the distal region of the

large bowel whereas CD has a more diffuse distribution

through the large bowel and may occur in the small

intestine. In both cases there are similarities as well as

differences. There is evidence of a breakdown of the

mucosal barrier in both UC and IBD. This leads to

translocation of bacteria which could provoke the inflammatory

response (
Scholmerich, 2006). A recent (relatively

small) prospective study showed that greater dietary

protein intakes were associated with loss of remission in

patients with previously quiescent UC (
Jowett et al., 2005).

The loss of mucosal barrier function which we have noted

in rodents fed higher protein diets is consistent with these

data. The protection afforded by RS is also consistent with

a proposed role of SCFA in protecting against UC. This

amelioration was thought to come from the provision of

butyrate to colonocytes which were otherwise starved of

substrate. The hypothesis is possible for UC as it occurs

predominantly in the distal colon, i.e. where the availability

of SCFA is lower than in the proximal and median large

bowel. It accords with reports that topical SCFA can lead

to repair of UC and potentiate standard anti-inflammatory

treatments (
Vernia et al., 2003). A small study in UC

patients has shown that consumption of a germinated

barley resulted in a similar improvement (
Kanauchi et al.,

). This is a long way from demonstrating a substantial

benefit of RS and the role SCFA in UC (and CD) is still

open to question. Nevertheless, it is apparent that diet has

a role to play in maintenance of large bowel mucosal

integrity and that RS has potential to assist in that regard.

7.3. RS, OS and prebiosis

The considerable attention being given to the prebiotic

concept is relatively new and derives from the long-


Fig. 1. Dose-dependent reduction of colonic genetic damage by resistant starch in rats fed high dietary protein as 25% casein. Damage was measured by

the comet assay in isolated colonocytes and is expressed as the tail moment (comet tail length
% DNA in the tail). Data are presented as the arithmetic

7SEM (n ¼ 8) and values not sharing the same superscript are significantly different (Po0.05).

D. Topping / Journal of Cereal Science 46 (2007) 220–229

standing proposition that the ingestion of specific live

bacterial cultures is beneficial for health. These bacteria are

referred to
probiotics and, for the most part, they belong to

a group referred to as the lactic acid bacteria (LAB). This

name derives from the fact that lactate is their major

fermentation product. Their principal substrates are OS,

especially those derived from milk. The latter include

galacto-oligosaccharides (GOS) but they also use others,

including fructo-oligsacchardies (FOS) which are found in

certain plants such as chicory. LAB find industrial use in

the manufacture of fermented milk products (especially

yoghurt) but they occur normally in the human gastrointestinal

tract. They are present in their highest concentration

and relative numbers in infancy, especially in breast

fed babies (
Harmsen et al., 2000). The fermentative

product profile of breast milk-fed infants differs radically

from that of adults. It includes ethanol and formate as well

lactate but little or no propionate or butyrate. This profile

may be important for the early development of the human

gut in terms of controlling the bacterial population (which

changes substantially on weaning). However, it does point

to a weakness in the case for probiotics as their metabolic

products are found in low levels in adults. While there is

evidence that dietary OS are of benefit in controlling

infantile diarrhoea (
Chen and Walker, 2005), their

potential in adults seems to be less clear. Part of this lack

of clarity reflects the fact that colonisation of the adult gut

after ingestion of live LAB is hard to maintain. This led to

the development of prebiotics which are defined as ‘‘nondigestible

food ingredients that beneficially affect the host

by selectively stimulating the growth and (or) activity of

one or a limited number of bacterial species already

resident in the colon, and, thus, improve host health’’. OS

were the archetypal prebiotics given their importance as

substrates for LAB. However, it is clear that restricting the

definition of the concept to OS alone is inappropriate.

Animal and
in vitro studies have shown that RS (as high

amylose maize starches) can function as prebiotics and

enhance the survival of ingested LAB (
Brown et al., 1998).

However, the effects of RS on the normal microflora are

also beneficial and their consumption stimulates SCFA

production. This translates to direct benefit in situations

such as infectious diarrhoea. The fact remains also that

knowledge of the prebiotic potential of cereal OS (both in

the grain and as isolates) is limited as is their contribution

to human health.

8. Cereal complex carbohydrates and health—conclusions

and future directions

There is strong evidence that cereal polysaccharides have

benefits in the control and prevention of human diseases.

Their capacity to improve health status is established

reasonably well in some areas, for example, soluble NSP

and plasma cholesterol control. However, despite the

extensive research effort that has been expended in this

area, questions remain, especially the issue of whether

other components are involved and if the effect can be

optimised through processing. The impact of the latter is

seldom examined and could be an important factor in

altering the plasma cholesterol lowering properties of

cereals (such as wheat bran) which do not seem to have

any benefit in this regard. In other areas, their benefits are

only just beginning to emerge. This is especially the case for

starch and its digestibility. Until relatively recently,

controlling starch digestion was considered substantially

in terms of the rate of hydrolysis in the small intestine, i.e.

GR. However, manipulating digestibility has much broader

implications, especially as current starchy foods seem to

be very low in RS. This is a major field of research and

development, especially in terms of its relationship to the

health of the large bowel. There is an abundant literature

relating the benefits of NSP (i.e. fibre) for large bowel

function and a similarly large volume of work on GR but

the contribution of starches to large bowel health is only

just beginning to gain support. As noted, there is the

opportunity to use advanced gene technologies to accelerate

the engineer new cereal cultivars to make food

products with substantiated health benefits. One of the

most radical recent developments in the relationship

between dietary carbohydrates and health is the emergence

of the importance of the large bowel microflora in human

health. It is becoming clear that many of the large bowel

actions ascribed to complex carbohydrates are actually due

to the products of their fermentation by the large bowel

microflora. Up to now, the diversity of the large bowel

colonisation and the limited technology available to culture

and identify them has been a significant block to progress.

New molecular technologies offer to free this log-jam.

Understanding the relationships between the metagenome,

carbohydrates, SCFA and health will offer great opportunities

to improve health. This should include obtaining an

understanding of the interactions between cereal OS and

the microflora. Following from this are important questions

on the relevance of the relatively short-term changes

in biomarkers reported in human and animals studies to

prevention of non-infectious disease in the long term. In

many ways, the field is at a very early stage of development

but is evolving rapidly and the promise to improve human

health is substantial indeed. However, this raises the

important question of consumer attitudes and regulation

to these developments. Will consumers accept these new

products and will regulation facilitate their introduction?

There is a further, important ethical issue. Consumer

resistance to genetically modified foods is well known yet it

is not commonly understood that persons with insulindependent

diabetes regularly inject themselves with human

insulin made by microorganisms using gene modification

technology. The new cereal cultivars are aimed at improving

public health in important areas, including diabetes.

This leads to the paradox of diabetics injecting themselves

with insulin while being denied access to foods (made with

similar technology) which will assist them in condition

prevention and management. These new technologies will


D. Topping / Journal of Cereal Science 46 (2007) 220–229

also help to unravel the relationships between gut microflora,

food polysaccharides and health.


The contribution of Tony Bird, Ian Brown, Michael

Conlon, Mike Gidley, Matthew Morell, Shusuke Toden

and Graeme Young to the development of this paper is

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