application of cereals and cereal components in functional foods: a review

11
Application of cereals and cereal components in functional foods: a review D. Charalampopoulos, R. Wang, S.S. Pandiella * , C. Webb Department of Chemical Engineering, Satake Centre for Grain Process Engineering, UMIST, Manchester M60 1QD, UK Received 15 March 2002; received in revised form 23 April 2002; accepted 25 April 2002 Abstract The food industry is directing new product development towards the area of functional foods and functional food ingredients due to consumers’ demand for healthier foods. In this respect, probiotic dairy foods containing human-derived Lactobacillus and Bifidobacterium species and prebiotic food formulations containing ingredients that cannot be digested by the human host in the upper gastrointestinal tract and can selectively stimulate the growth of one or a limited number of colonic bacteria have been recently introduced into the market. The aim of these products is to affect beneficially the gut microbial composition and activities. Cereals offer another alternative for the production of functional foods. The multiple beneficial effects of cereals can be exploited in different ways leading to the design of novel cereal foods or cereal ingredients that can target specific populations. Cereals can be used as fermentable substrates for the growth of probiotic microorganisms. The main parameters that have to be considered are the composition and processing of the cereal grains, the substrate formulation, the growth capability and productivity of the starter culture, the stability of the probiotic strain during storage, the organoleptic properties and the nutritional value of the final product. Additionally, cereals can be used as sources of nondigestible carbohydrates that besides promoting several beneficial physiological effects can also selectively stimulate the growth of lactobacilli and bifidobacteria present in the colon and act as prebiotics. Cereals contain water-soluble fibre, such as h-glucan and arabinoxylan, oilgosaccharides, such as galacto- and fructo-oligosaccharides and resistant starch, which have been suggested to fulfil the prebiotic concept. Separation of specific fractions of fibre from different cereal varieties or cereal by-products, according to the knowledge of fibre distribution in cereal grains, could be achieved through processing technologies, such as milling, sieving, and debranning or pearling. Finally, cereal constituents, such as starch, can be used as encapsulation materials for probiotics in order to improve their stability during storage and enhance their viability during their passage through the adverse conditions of the gastrointestinal tract. It could be concluded that functional foods based on cereals is a challenging perspective, however, the development of new technologies of cereal processing that enhance their health potential and the acceptability of the food product are of primary importance. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Cereals; Probiotic; Prebiotic; Fermentation; Lactic acid bacteria; Bifidobacteria 1. Introduction The interest in developing functional foods is thriv- ing, driven largely by the market potential for foods that can improve the health and well-being of consumers. The concept of functional foods includes foods or food 0168-1605/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII:S0168-1605(02)00187-3 * Corresponding author. Tel.: +44-161-200-4429; fax: +44-161- 200-4399. E-mail address: [email protected] (S.S. Pandiella). www.elsevier.com/locate/ijfoodmicro International Journal of Food Microbiology 79 (2002) 131 – 141

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Page 1: Application of cereals and cereal components in functional foods: a review

Application of cereals and cereal components in

functional foods: a review

D. Charalampopoulos, R. Wang, S.S. Pandiella *, C. Webb

Department of Chemical Engineering, Satake Centre for Grain Process Engineering, UMIST, Manchester M60 1QD, UK

Received 15 March 2002; received in revised form 23 April 2002; accepted 25 April 2002

Abstract

The food industry is directing new product development towards the area of functional foods and functional food ingredients

due to consumers’ demand for healthier foods. In this respect, probiotic dairy foods containing human-derived Lactobacillus and

Bifidobacterium species and prebiotic food formulations containing ingredients that cannot be digested by the human host in the

upper gastrointestinal tract and can selectively stimulate the growth of one or a limited number of colonic bacteria have been

recently introduced into the market. The aim of these products is to affect beneficially the gut microbial composition and activities.

Cereals offer another alternative for the production of functional foods. The multiple beneficial effects of cereals can be exploited

in different ways leading to the design of novel cereal foods or cereal ingredients that can target specific populations. Cereals can

be used as fermentable substrates for the growth of probiotic microorganisms. The main parameters that have to be considered are

the composition and processing of the cereal grains, the substrate formulation, the growth capability and productivity of the starter

culture, the stability of the probiotic strain during storage, the organoleptic properties and the nutritional value of the final product.

Additionally, cereals can be used as sources of nondigestible carbohydrates that besides promoting several beneficial physiological

effects can also selectively stimulate the growth of lactobacilli and bifidobacteria present in the colon and act as prebiotics. Cereals

contain water-soluble fibre, such ash-glucan and arabinoxylan, oilgosaccharides, such as galacto- and fructo-oligosaccharides andresistant starch, which have been suggested to fulfil the prebiotic concept. Separation of specific fractions of fibre from different

cereal varieties or cereal by-products, according to the knowledge of fibre distribution in cereal grains, could be achieved through

processing technologies, such as milling, sieving, and debranning or pearling. Finally, cereal constituents, such as starch, can be

used as encapsulation materials for probiotics in order to improve their stability during storage and enhance their viability during

their passage through the adverse conditions of the gastrointestinal tract. It could be concluded that functional foods based on

cereals is a challenging perspective, however, the development of new technologies of cereal processing that enhance their health

potential and the acceptability of the food product are of primary importance.

D 2002 Elsevier Science B.V. All rights reserved.

Keywords: Cereals; Probiotic; Prebiotic; Fermentation; Lactic acid bacteria; Bifidobacteria

1. Introduction

The interest in developing functional foods is thriv-

ing, driven largely by themarket potential for foods that

can improve the health and well-being of consumers.

The concept of functional foods includes foods or food

0168-1605/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved.

PII: S0168 -1605 (02 )00187 -3

* Corresponding author. Tel.: +44-161-200-4429; fax: +44-161-

200-4399.

E-mail address: [email protected] (S.S. Pandiella).

www.elsevier.com/locate/ijfoodmicro

International Journal of Food Microbiology 79 (2002) 131–141

Page 2: Application of cereals and cereal components in functional foods: a review

ingredients that exert a beneficial effect on host health

and/or reduce the risk of chronic disease beyond basic

nutritional functions (Huggett and Schliter, 1996).

Successful types of functional products that have been

designed to reduce high blood pressure, cholesterol

blood sugar, and osteoporosis have been introduced

into the market (Sanders, 1998). Recently, the func-

tional food research has moved progressively towards

the development of dietary supplementation, introduc-

ing the concept of probiotics and prebiotics, which may

affect gut microbial composition and activities (Ziemer

and Gibson, 1998).

Probiotic foods are defined as those that contain

a single or mixed culture of microorganisms that

affect beneficially the consumer’s health by improv-

ing their intestinal microbial balance (Fuller, 1989).

There is significant scientific evidence, based

mainly on in vitro studies and on clinical trials

using animals, suggesting the potentially beneficial

effects of probiotic microorganisms. These include:

metabolism of lactose, control of gastrointestinal

infections, suppression of cancer, reduction of

serum cholesterol, and immune stimulation (Gilli-

land, 1990; Salminen et al., 1998; Fooks et al.,

1999). The necessity for epidemiological studies on

healthy human populations to support the specific

health promoting claims of a probiotic strain is

generally highlighted (Sanders, 1998; Shortt, 1999;

Saarela et al., 2000). Common microorganisms used

in probiotic preparations are predominantly Lacto-

bacillus species, such as Lactobacillus acidophilus,

L. casei, L. reuteri, L. rhamnosus, L. johnsonii, and

L. plantarum and Bifidobacterium species, such as

Bifidobacterium longum, B. breve, B. lactis (Shortt,

1999). The incorporation of probiotic strains in

traditional food products has been established in

the dairy industry, leading to the production of

novel types of fermented milks and cheeses (Gomes

and Malcata, 1999).

A prebiotic is a food ingredient that is not

hydrolysed by the human digestive enzymes in

the upper gastrointestinal tract and beneficially

affects the host by selectively stimulating the

growth and/or activity of one or a limited number

of bacteria in the colon that can improve host

health (Gibson and Roberfroid, 1995). Fibre is a

general term of different types of carbohydrates

derived from plant cell walls that are not hydro-

lysed by human digestive enzymes. Specific forms

of dietary fibre are readily fermentable by specific

colonic bacteria, such as bifidobacteria and lactoba-

cilli species, increasing their cell population with

the concomitant production of short-chain fatty

acids (SCFA). These acids, especially butyrate,

acetate, and propionate, provide metabolic energy

for the host and acidification of the bowel (Sghir et

al., 1998). Several clinical studies have also sug-

gested that dietary fibre could promote beneficial

physiological effects including laxation and blood

cholesterol attenuation (Spiller, 1994), as well as

blood glucose attenuation (Bijlani, 1985). It may

also prevent cancer (McCann et al., 2001), diabetes

(Wang et al., 2001), heart disease (Fernandez,

2001), and obesity (Iwata and Ishiwatari, 2001).

However, epidemiological results have to be treated

with great precaution due to the complexity of the

possible mechanisms involved.

2. Cereal-based functional products

The development of nondairy probiotic products is

a challenge to the food industry in its effort to utilise

the abundant natural resources by producing high

quality functional products. In this respect, probi-

otic-containing baby foods or confectionery formula-

tions have been developed by adding the strains as

additives (Saarela et al., 2000). In recent years, cereals

have also been investigated regarding their potential

use in developing functional foods. Cereals are grown

over 73% of the total world harvested area and

contribute over 60% of the world food production

providing dietary fibre, proteins, energy, minerals, and

vitamins required for human health. The possible

applications of cereals or cereal constituents in func-

tional food formulations could be summarised:

� as fermentable substrates for growth of probiotic

microorganisms, especially lactobacilli and bifido-

bacteria� as dietary fibre promoting several beneficial

physiological effects� as prebiotics due to their content of specific

nondigestible carbohydrates� as encapsulation materials for probiotic in order to

enhance their stability.

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141132

Page 3: Application of cereals and cereal components in functional foods: a review

3. Cereals as substrates for probiotics

Lactic acid fermentation of cereals is a long-estab-

lished processing method and is being used in Asia

and Africa for the production of foods in various

forms such as beverages, gruels, and porridge.

Although differences exist between regions, the prep-

aration procedure could be generalised. Cereal grains,

mainly maize, sorghum, or millet grains, are soaked in

clean water for 0.5–2 days. Soaking softens the grains

and makes them easier to crash or wet-mill into slurry,

from which hulls, bran particles, and germs can be

removed by sieving procedures. During the slurring or

doughing stage, which lasts for 1–3 days, mixed

fermentations including lactic acid fermentation take

place. During the fermentation, the pH decreases with

a simultaneous increase in acidity, as lactic and other

organic acids accumulate due to microbial activity.

InWestern countries, cereals, like wheat and rye, are

used for sourdough production, which is traditionally

prepared by adding a prefermented sourdough of good

quality to the dough. These starter cultures can be

characterised as ‘mixed-strain cultures’ and are con-

tinuously propagated and distributed in small propor-

tions in bakeries. The population of lactobacilli in fully

fermented sourdoughs is more than 109 cfu g� 1, while

the lactic acid bacteria (LAB)/yeast ratio is generally

100:1 (Salovaara, 1998).

The good growth of LAB in cereals suggests that

the incorporation of a human-derived probiotic strain

in a cereal substrate under controlled conditions

would produce a fermented food with defined and

consistent characteristics, and possibly health-promot-

ing properties combining the probiotic and prebiotic

concept. However, in designing such a novel fermen-

tation food process, several technological aspects have

to be considered such as the composition and process-

ing of the cereal grains, the growth capability and

productivity of the starter culture, the stability of the

probiotic during storage, the organoleptic properties,

and the nutritional value of the final product.

3.1. Effect of cereal composition on growth of

probiotics

Probiotic products are usually standardised based on

the presumption that culture viability is a reasonable

measure of probiotic activity, thus the ability of the

strain to attain high cell population is of primary

importance. A concentration of approximately 107 cells

ml� 1 at the time of consumption is considered func-

tional (Gomes and Malcata, 1999; Shortt, 1999). High

cell growth rates and acidification rates would also re-

sult in reduction of fermentation times and enhance the

viability of the specific strain by preventing growth of

undesirable microorganisms present in the rawmaterial

(Marklinder and Lonner, 1992), which would lead to

the formation of off-flavours (Svensson, 1999). There-

fore, the adaptability of the probiotic in the substrate is a

very important criterion in the selection procedure of a

suitable strain (Oberman and Libudzisz, 1998).

Lactobacilli and bifidobacteria have complex nutri-

tional requirements such as carbohydrates, amino

acids, peptides, fatty esters, salts, nucleic acid deriva-

tives, and vitamins, which vary a lot from species to

species (Severson, 1998). The principal carbohydrate

constituents of cereal grains are starch, water-soluble or

-insoluble components of dietary fibre, and several free

sugars, such as glucose, glycerol, stachyose, xylose,

fructose, maltose, sucrose, and arabinose. The contents

of these components depend on the variety (Becker and

Hanners, 1991), the processing, and the amount of

water addition. Table 1 presents the composition of

different varieties of cereals compared to that of milk.

Cereals have higher content of some of the essential

vitamins than milk, higher content of dietary fibre, and

increased amount of minerals, especially phosphorus,

but lower amount of fermentable carbohydrates, usu-

ally less than 1% in wheat dough.

Information concerning the effects of cereal compo-

sition on the growth of probiotic microorganisms is

limited. Marklinder and Lonner (1992) suggested the

potential of fermented oatmeal soup (18.5%) contain-

ing viable LAB as a base for nutritive solution in enteral

feeding. After testing several heterofermentative and

homofermentative probiotic lactobacilli, it was con-

cluded that oats are in general a suitable substrate for

LAB growth, regardless of the differences between

species and strains. Among the strains tested, L. acid-

ophilus exhibited the slowest rates of pH reduction, and

lowest levels of viable cells in the final product, due

probably to its high requirements for several nutrients

(Morishita et al., 1981). The highest viable cell counts,

3� 109 and 1�109 cfu ml� 1, were achieved using L.

plantarum and L. reuteri, respectively. Addition of

malted barley flour, proteases and amino acids

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141 133

Page 4: Application of cereals and cereal components in functional foods: a review

increased the rate of pH-decrease and the total amount

of lactobacilli in the final product (Marklinder and

Lonner, 1994). In a similar study, L. acidophilus was

successfully cultivated in an enzymatically hydrolysed

oat mash reaching 109 cfu ml� 1 (Bekers et al., 2001).

In our study (Charalampopoulos et al., 2002),

human-derived strains of L. reuteri, L. plantarum, L.

acidophilus, and a L. fermentum strain isolated from

cereals were cultured in malt, barley, and wheat

extracts formulated without the addition of any sup-

plements. The growth parameters are presented in

Table 2. The malt medium supported better cell

growth than barley and wheat due to the increased

amounts of maltose, sucrose, glucose, and fructose

(approximately 15 g l � 1 of total fermentable sugars)

and free amino nitrogen (approximately 80 mg l � 1).

It must be emphasised that each strain demonstrated a

specific preference for one or more sugars, which has

been reported for LAB isolated from fermented cereal

products (Gobbetti and Corsetti, 1997). The similar

fermentation patterns observed in wheat and barley

for all the strains tested could be attributed to the low

total fermentable sugar (3–4 g l � 1) and the low free

amino nitrogen concentration (15.3–26.6 mg l � 1). L.

plantarum exhibited the highest cell population owing

to its unique ability to tolerate low pH values by

Table 1

Composition of foods expressed as 100 g of edible portion

Parameter Malt Rice Corn Wheat Sorghum Millet Milk (liquid)

Water (%) 8 12 13.8 12 11 11.8 87.4

Protein (g) 13.1 7.5 8.9 13.3 11 9.9 3.5

Fat (g) 1.9 1.9 3.9 2.0 3.3 2.9 3.5

Carbohydrates (g) 77.4 77.4 72.2 71.0 73.0 72.9 4.9

Fiber (g) 5.7 0.9 2.0 2.3 1.7 3.2 n.d.

Ash (g) 2.4 1.2 1.2 1.7 1.7 2.5 0.7

Ca (mg) 40 32 22 41 28 20 118

P (mg) 330 221 268 372 287 311 93

Fe (mg) 4.0 1.6 2.1 3.3 4.4 68 Trace

K (mg) 400 214 284 370 350 430 144

Thiamin (mg) 0.49 0.34 0.37 0.55 0.38 0.73 0.03

Riboflavin (mg) 0.31 0.05 0.12 0.12 0.15 0.38 0.17

Niacin (mg) 900 1.7 2.2 4.3 3.9 2.3 0.1

Mg (mg) 140 88 147 113 n.d. 162 13

Source: Adapted from Severson (1998).

Table 2

Numerical values of estimated microbial growth parameters in sterile malt, barley, and wheat media

Medium Microorganism lmax (h� 1) X0 (log10cfu ml� 1) Xmax (log10 cfu ml� 1) pH

Malt L. fermentum 0.62F 0.04 6.85F 0.08 9.68F 0.03 3.77F 0.09

L. plantarum 0.41F 0.03 6.90F 0.10 10.11F 0.18 3.40F 0.09

L. reuteri 0.38F 0.02 6.20F 0.07 8.86F 0.06 3.72F 0.09

L. acidophilus 0.19F 0.02 6.89F 0.06 8.10F 0.06 3.73F 0.09

Barley L. fermentum 0.43F 0.05 6.90F 0.11 9.12F 0.05 4.61F 0.09

L. plantarum 0.20F 0.02 6.71F 0.13 9.43F 0.10 3.92F 0.09

L. reuteri 0.13F 0.01 6.14F 0.04 7.28F 0.05 4.88F 0.09

L. acidophilus 0.18F 0.03 7.02F 0.04 7.73F 0.03 3.93F 0.09

Wheat L. fermentum 0.53F 0.05 6.93F 0.09 9.28F 0.04 4.50F 0.09

L. plantarum 0.23F 0.02 7.21F 0.05 9.29F 0.06 3.83F 0.09

L. reuteri 0.13F 0.01 6.22F 0.03 7.20F 0.04 4.40F 0.09

L. acidophilus 0.15F 0.01 7.02F 0.02 7.71F 0.03 3.73F 0.09

lmax =maximum specific growth rate, X0 = initial cell population, X max =maximum cell population at the end of the exponential phase, pH= pH

at the end of the exponential phase.

The maximum specific growth rate was estimated using a logistic-type equation, applied to the data obtained during growth.

Source: Adapted from Charalampopoulos et al. (2002).

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141134

Page 5: Application of cereals and cereal components in functional foods: a review

maintaining a proton (pH) and charge gradient

between the inside and the outside of the cells even

in the presence of high amounts of lactate and protons

(Giraud et al., 1998). L. acidophilus exhibited the

poorest growth probably because of substrate defi-

ciency in specific nutrients, confirming the impor-

tance of substrate composition in conjunction with the

nutritional requirements of the specific strain.

3.2. Survival of probiotics

A key factor in the selection of suitable probiotic

starter is its ability to survive the acidic environment of

the final fermented product (in vitro) and the adverse

conditions of the gastrointestinal tract (in vivo). The

survival of the probiotic bacteria in vitro might be

influenced by the metabolites formed by the starter

such as lactic acid and acetic acid, hydrogen peroxide,

and bacteriocins (Saarela et al., 2000). Although differ-

ences exist between species and specific strains, lacto-

bacilli are generally considered to be intrinsically

resistant (Kashket, 1987), especially at pH values

higher than 3.0 (Hood and Zottola, 1988; Jin et al.,

1998). Of the various probiotic bacteria, L. casei and L.

plantarum appear to have longer shelf lives than L.

acidophilus, L. reuteri, and bifidobacteria in cultured

milk (Lee and Salminen, 1995). Based on the above,

the optimum final pH and the concentrations of lactic

acid and acetic acid in fermented cereal product in

relation to the properties of each specific probiotic

strain have to be investigated in order to maximise

the viability during storage. Besides the intrinsic stabil-

ity of each strain, the inclusion of slow-metabolising

energy sources, such as arginine, fructose, citric acid,

and malic acid, which could be present in cereals, has

been reported to enhance the viability by providing

energy (Lee and Salminen, 1995).

Survival of the probiotic strains during gastric

transit is also influenced by the physicochemical

properties of the food carrier used for delivery. The

buffering capacity and the pH of the carrier medium

are significant factors, since food formulations with

pH ranging from 3.5 to 4.5 and high buffering

capacity would increase the pH of the gastric tract

and thus enhance the stability of the probiotic strain

(Kailasapathy and Chin 2000; Zarate et al., 2000). In

addition, it has been shown that malt, wheat, and

barley extracts exhibited a significant protective effect

on the viability of human-derived L. plantarum and L.

acidophilus strains under acidic conditions mimicking

the stomach, which based on supporting experiments

with dietary constituents could be mainly attributed to

the presence of soluble sugars in the cereal extracts

and to a less extent to the free amino nitrogen content,

depending on the strain. (Charalampopoulos et al.,

data not shown).

3.3. Organoleptic properties

The grains of corn, sorghum, millet, barley, rye,

and oats contain appreciable amount of crude fibre

and lack gluten-like proteins of wheat. The traditional

foods made from these grains usually lack flavour and

aroma (Chavan and Kadam, 1989). Lactic acid fer-

mentation improves the sensorial value, which is very

much dependent on the amounts of lactic acid, acetic

acid and several aromatic volatiles, such as higher

alcohols and aldehydes, ethyl acetate and diacetyl,

produced via the homofermentative or heterofermen-

tative metabolic pathways. Consequently, an appro-

priate selection of the strain is necessary to efficiently

control the distribution of the metabolic end products

(Lonner and Preve-Akesson, 1988; Damiani et al.,

1996; Hansen et al., 1989). Knowledge of the bio-

chemical pathways leading to flavour production can

help in making the right choice of starter. However,

the end product distribution of lactic acid fermenta-

tions depends also on the chemical composition of the

substrate (carbohydrate content, presence of electron

acceptors, nitrogen availability) and the environmen-

tal conditions (pH, temperature, aeorbiosis/anaerobio-

sis), controlling of which would allow specific

fermentations to be channelled towards a more desir-

able product (Hansen and Hansen, 1994).

In general, probiotic products obtained using a

single strain probiotic starter are hardly acceptable to

consumers, lacking sensory appeal due to a rather sour

and acidic taste. For milk-based products, the probiotic

strains are often mixed with Streptococcus thermophi-

lus and L. delbrueckii (Saarela et al., 2000). In this

respect, another alternative in enhancing the aromatic

profile of the final product would be the incorporation

of supporting strains being able to bring out the

preferred flavour. It is important that the supporting

strains grow in the cereal substrate and do not act

antagonistically towards the probiotic strain. In indus-

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141 135

Page 6: Application of cereals and cereal components in functional foods: a review

trial cereal fermentations L. sanfransisco, the most

important sourdough bacteria, is usually mixed with

Sacharomyces exiguus or Candida milleri, improving

the overall organoleptic properties (Gobbetti, 1998).

3.4. Nutritional value

Lactic acid fermentation improves usually the nutri-

tional value and digestibility of cereals. Cereals are

limited in essential amino acids such as threonine,

lysine, and tryptophan, thus making their protein qual-

ity poorer compared with animals and milk (Chavan

and Kadam, 1989). Their protein digestibility is also

lower than that of animals, due partially to the presence

of phytic acid, tannins, and polyphenols which bind to

protein thus making them indigestible (Oyewole,

1997). Lactic acid fermentation of different cereals,

such as maize, sorghum, finger millet, has been found

effectively to reduce the amount of phytic acid, tannins

and improve protein availability (Chavan et al., 1988;

Lorri and Svanberg, 1993). Increased amounts of ribo-

flavin, thiamine, niacin, and lysine due to the action of

LAB in fermented blends of cereals were also reported

(Hamad and Fields, 1979; Sanni et al., 1999). Khetar-

paul and Chauhan (1990) reported improved minerals

availability of pearl millet fermented with pure cultures

of lactobacilli and yeasts.

4. Dietary fibre from cereal grains and their

prebiotic and physiological effects

4.1. Definition

Dietary fibre is the edible part of plants or analo-

gous carbohydrates, which resists the hydrolysis by

alimentary tract enzymes. In addition, fibre is not

totally unavailable either, because a portion of dietary

fibre is metabolised to volatile fatty acids in the

gastrointestinal tract. Dietary fibre can be divided into

two categories according to their water solubility.

Each category provides different therapeutic effects.

Water-soluble fibre consists mainly of nonstarchy

polysaccharides, mainly h-glucan and arabinoxylan.

By forming viscous solution, soluble fibre slows

intestinal transit, delays gastric emptying, and reduces

glucose and sterol absorption by the intestine. Soluble

fibre also decreases serum cholesterol, prostprandial

blood glucose, and insulin contents in human body.

Water-insoluble fibre contains lignin, cellulose, hemi-

celluloses (Bingham, 1987; Marlett, 1990), and non-

starchy polysaccharides such as water-unextractable

arabinoxylan.

Between cereal grains, the content of dietary fibre

varies (Table 3) (Nelson, 2001; Herrera et al., 1998).

In cereal botanical components, the majority of diet-

ary fibres generally occur in decreasing amounts from

the outer pericarp to the endosperm, except arabinox-

ylan, which is also a major component of endosperm

cell wall materials. The procedures for the isolation

and purification of dietary fibre and the techniques

involved in their quantitative and structural analysis

were developed for the isolation of dietary fibre from

conventional milling streams. The combination of the

debranning or pearling technology and the subsequent

simplified milling process might produce processing

streams of more specified botanical components, such

as the outer pericarp, the inner pericarp, the seed coat,

the aleurone cells, the embryo, and the starchy endo-

sperm. Targeting at particular dietary fibres in each of

these streams according to the knowledge of fibre

distribution in cereal grains, these isolation procedures

would be simplified and their products more purified.

4.2. b-Glucan

One of the most important members of the dietary

fibre family is h-glucan. It is unbranched polysac-

charides composed of (1! 4) and (1! 3) linked h-D-glucopyranosyl units in varying proportions. Various

forms of h-glucan have been recognised as having

Table 3

Comparison of total dietary fibre content in cereal grains

Cereals Total dietary fibre (%, db)

Legumes 13.6–28.9

Rye 15.5

Corn 15

Triticale 14.5

Oats 14

Wheat 12

Sorghum 10.7

Barley 10

Finger millet 6.2–7.2

Rice 3.9F 0.2

Source: Compiled from Herrera et al. (1998) and Nelson (2001).

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141136

Page 7: Application of cereals and cereal components in functional foods: a review

important positive therapeutic effects on coronary

heart disease, on the reductions of cholesterol and

glycemic response (Wood, 1993; Beer et al., 1995). In

addition, oat h-glucan has been reported to selectively

support the growth of lactobacilli and bifidobactera in

rat experiments (Ryhanen et al., 1996) and in in vitro

studies (Jaskari et al., 1993). High molecular weight

h-glucans, up to 3 million Da (Wood et al., 1991), are

viscous due to labile cooperative associations. Low

molecular weight h-glucans, as low as 9000 Da

(Gomez et al., 1997), can form soft gels as the chains

are easier to rearrange to maximise linkages. When

exposed to physical forces and chemical or enzymatic

hydrolysis, molecular size of h-glucan reduces to

achieve molecular weights of 0.4–2 million Da in

typical food preparations (Beer et al., 1997). Hydro-

lysates of oat h-glucan have been reported to stim-

ulate the growth of three Bifidobacterium strains and

L. rhamosus GG (Kontula et al., 1998). Among all the

cereal grains, barley and oats contain the highest level

of h-glucan, covering the ranges of 3� 11% and

3� 7% on a dry basis, respectively. It is usually

concentrated in the inner aleurone cell walls and

subaleurone endosperm cell walls of barley (Koksel,

1999), oats (Wood, 1993), and wheat (Wood, 1997).

Considerable amount of h-glucan is also found in the

crease area of wheat (Wood, 1984) and possibly other

grains. Wheat is not recognised as a source of h-glucan because of its much lower content, usually

below 1% on a dry basis. The physical properties of

wheat grain, however, allow the development of

pearling technology to separate the aleurone layer as

potential source of h-glucan. The pearling process

applies friction and abrasion to debran grains for the

improvement of milling performance. Developments

such as the PeriTec process from Satake Engineers

and the Tkac process from Tkac and Timm Enter-

prises provide the opportunity to individually collect

wheat botanical components. The combination of the

pericarp, the seed coat, and the nucellus forms a rich

source of both arabinoxylan and lignin. The bran

section in the crease area and the subaleurone section

might be separated by the subsequent milling process

and mixed into the aleurone section from debranning,

as a source of h-glucan. The successful application of

the pearling technology to other grains would rely on

factors such as proper conditioning of the grains prior

to debranning and special design of the debranner.

4.3. Oligosaccharides

Oligosaccharides, such as lactulose, fructo-oligo-

saccharides, transgalacto-oligosaccharides (Gibson et

al., 1995; Bouhnik et al., 1997) have received

increased attention, especially because they have been

shown to be effective in stimulating the growth of

bifidobacteria and lactobacilli in human large intes-

tine. These oligosaccharides can be isolated from

plant materials or can be synthesised enzymatically

(Crittenden and Playne, 1996). In the food industry,

simple oligasaccarides are used as bifidogenic sub-

stances and some infant products contain them in the

hope that this might provide some of the benefits

attributed to oligosaccharides in human milk (Rivero-

Urgell and Santamaria-Orleans, 2001). At least two

types of oligosaccarides exist in cereal grains. They

are galactosyl derivatives of sucrose, stachyose and

raffinose, and fructosyl derivatives of sucrose, fructo-

oligosaccharides (Henry and Saini, 1989). The exact

distributions of these polymers within cereal grain

have not been fully established. In respect of wheat,

reported values suggest their distributions in all mill-

ing products, including bran (Yamada et al., 1993),

germ (Pomeranz, 1988), and flour (Nakazawa et al.,

2000). Wheat germ is particularly rich in raffinose

family oligosaccharides, 7.2% on a dry basis. Total

sugar content in the aleurone cells have been approxi-

mated as 11.1% (Mizuochi, 1999) on a dry basis,

while the reported values for milling flour fall in the

range of 1.2� 1.6% (Pomeranz, 1988).

Extraction of oligosaccharides from natural resour-

ces has not been fully developed due to the complexity

of these substances and their connections with other

macromolecules, particularly proteins. Oligosacchar-

ide concentrate might be obtained from cereal botanical

constituents by exploring their water solubility. Taking

wheat as example, the water washing process com-

monly applied for gluten separationwould retain water-

soluble oligosaccharides in the starch slurry. After the

removal of starch by centrifugation or vibrating screen,

the residual paste might be centrifuged to obtain a

coloured fibrous substance, starch tailings. Oligosac-

charides can be released from other cell wall compo-

nents by the treatment of cellulase to these tailings.

Separation of oligosaccharides from both wheat germ

residue, usually after oil extraction, and from the

aleurone layer might be developed based on the sol-

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141 137

Page 8: Application of cereals and cereal components in functional foods: a review

ubility of oligosaccharides in 80% ethanol solution

(Henry and Saini, 1989). Purification of these materials

will require the application of cellulose column chro-

matography (Mizuochi, 1999) gel filtration (Palmacci

et al., 2001), high-performance liquid affinity chroma-

tography (Zopf et al., 1989).

Cereal bioprocessing through enzymatic reactions

or through fermentation can also produce a large range

of oligosaccharides with potential prebiotic properties.

The a-amylase present in the cereal grain can hydro-

lyse the gelatinised starch granules, and the extent of

the hydrolysis could be regulated through temperature

control. The different fractions of the oligosaccharides

obtained could then be separated and their functionality

could be tested. Another alternative for the hydrolysis

of the starch would be through fungal fermentation of

the use of solid state fermentation technology. The

processing steps prior to the starch hydrolysis (e.g.,

milling) could also have an effect in the biotransforma-

tion and should be taken into account.

4.4. Resistant starch

Resistant starch has been recognised as a functional

fibre performing an important role in digestive physi-

ology. Similar to oligosaccharides, especially fructo-

oligosaccharides, it escapes digestion and provides

fermentable carbohydrates for colonic bacteria. Resist-

ant starch has also been shown to provide benefits such

as the production of desirable metabolites including

short-chain fatty acids in the colon. In addition to its

therapeutic effects, resistant starch provides better

appearance, texture, and mouthfeel than conventional

fibres (Martinez Flores et al., 1999). Opportunities

exist for the development of ingredients from resistant

starch as prebiotics for decreasing the risk of bowel

diseases. Resistant starch might be classified into four

categories (Yue and Waring, 1998), but the natural

types are frequently destroyed when subjected to mod-

ern food processes. Resistant starch is naturally found

in cereal grains and in heated starch or starch-contain-

ing foods. The manufacture of resistant starch usually

involves partial acid hydrolysis and hydrothermal treat-

ments (Brumovsky and Thompson, 2001), heating,

retrogradation (Schmiedel et al., 2000), extrusion cook-

ing (Gebhardt et al., 2001), chemical modification

(Wolf et al., 1999), and repolymerisation (Yue and

Waring, 1998).

5. Encapsulation of probiotic strains using cereal

fractions

In the last years, several encapsulation techniques

using cereal fractions have been tested in order to

improve the viability of the probiotic strains in func-

tional foods. The possibility of using high amylose

maize (amylomaize) starch granules as a delivery

system for probiotic bacteria has been investigated

by Wang et al. (1999). In this case, Bifidobacterium

strains isolated from a healthy human were used

adhered to amylomaize starch granules. In vitro stud-

ies showed that growth in these conditions led to

enhanced survival of the probiotic strains. Survival in

vivo was also monitored by measuring the faecal level

of Bifidobacterium after oral administration of the

strain to mice. A sixfold better recovery of the strains

was noted for cells grown in amylose-containing

medium compared with the control.

A modified method using calcium alginate for the

microencapsulation of probiotic bacteria in yoghurt

has also been reported in the literature (Sultana et al.,

2000). Incorporation of maize starch (a prebiotic) with

alginate improved the encapsulation of viable bacteria

as compared to when the bacteria were encapsulated

without the starch. The survival of encapsulated

cultures was in all cases higher than with the free

cells. Techniques such as spray drying could be used

to produce small uniformly coated microspheres con-

taining the viable probiotic bacteria (O’Riordan et al.,

2001).

Other encapsulation techniques have been used by

other authors. Jankowski et al. (1997) used capsules

of a liquid starch core with calcium alginate mem-

branes, while Selmer-Olsen et al. (1999) and Shah and

Ravula (2000) used pure Ca-alginate gel beads. Adhi-

kari et al. (2000) used kappa-carrageenan for the

encapsulation of bifidobacteria in yogurt. In all these

cases, the encapsulation technique could be used to

transmit probiotic bacteria via fermented products

provided that the sensory characteristics of the prod-

uct are improved or maintained.

6. Future perspectives

Cereals are generally suitable substrates for the

growth of human-derived probiotic strains. Regardless

D. Charalampopoulos et al. / International Journal of Food Microbiology 79 (2002) 131–141138

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of the relatively big differences in performance

between species and the complexity of cereal sub-

strates, a systematic approach is needed in order to

identify the intrinsic and processing factors that could

enhance the growth and, more importantly, the sur-

vival of the probiotic strain in vitro and in vivo. The

possible improvement of the organoleptic properties

should also be investigated by using supporting cul-

tures that act synergistically on the probiotic strains.

Additionally, the functionality of colonic strains

could be improved by the presence of specific non-

digestible components of the cereal matrix that could

act as prebiotics. The possibility of separating specific

fractions of nondigestible soluble fibre from different

types of cereals or cereal by-products, either through

primary processing technologies, such as pearling and

sieving, or through enzymatic modifications, looks

very promising.

The development of new functional ingredients has

the advantage that food manufacturers can add extra

value to products the consumer is already familiar

with. Developing new foods involves larger market-

ing campaigns and often the consumer needs an

adaptation time to the new product. By either devel-

oping new and innovative products or just reformulat-

ing existing ones, nutritional food ingredients enable

manufacturers to meet and exceed the expectations of

today’s health-conscious consumer. Cereals not only

have the ability to grow and deliver probiotic lactic

acid bacteria to the human gut, but also contain

potentially prebiotic compounds whose functionality

should be explored.

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