Prebiotics in foods

Dimitris Charalampopoulos and Robert A Rastall

A wealth of information has been gathered over the past 15
years on prebiotics through experimental, animal and human
studies, with the aim to understand the mechanism of actions
and elucidate their benecial health effects to the human host.
Signicant amount of evidence exists for their ability to increase
the bioavailability of minerals and stimulate the immune
system, although there is less clear evidence so far for their
prophylactic or therapeutic role in gastrointestinal infections.
Moreover, the effect of the food delivery vehicle on the efcacy
of prebiotics is an area that has been hardly investigated.
Besides their benecial effects, prebiotics inuence the textural
and organoleptic properties of the food products, such as dairy
and baked products. To do this however, they need to be stable
during food processing, in particular under conditions of high
temperature and low pH.
Address
Department of Food and Nutritional Sciences, The University of Reading,
PO Box 226, Whiteknights, Reading, RG6 6AP, UK
Corresponding author: Charalampopoulos, Dimitris
(d.charalampopoulos@reading.ac.uk)
Current Opinion in Biotechnology 2012, 23:187191
This review comes from a themed issue on
Food biotechnology
Edited by Gabriella Gazzani and Michael Grusak
Available online 12th January 2012
0958-1669/$ see front matter
# 2012 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.copbio.2011.12.028
Introduction
The concept of prebiotics was introduced in 1995 by
Gibson and Roberfoid as an alternative approach to the
modulation of the gut microbiota [1]. A more recent
denition of the term is a selectively fermented ingre-
dient that allows specic changes, both in the compo-
sition and/or activity in the gastrointestinal microbiota
that confers benets upon host wellbeing and health [2].
Any dietary ingredient that can reach the colon has the
potential of being a prebiotic. However, in order to full
the criteria, it should be able to resist the digestion
process, which involves gastric acids, intestinal brush
border and pancreatic enzymes, and gastrointestinal
absorption, and be selectively fermented by specic
genera of colon bacteria [3]. These are primarily bido-
bacteria and lactobacilli, as there is evidence that intes-
tinal lactobacilli and bidobacteria can potentially exert
health-promoting effects to the host, and as a result they
are the usual targets when considering the application of
prebiotics for the modulation of the gut microbiota.
Taking into account the evidence from in vivo studies,
the established prebiotics are inulin, fructo-oligosacchar-
ides (FOS), produced either by hydrolysis of inulin or by
enzymatic synthesis from sucrose, and galacto-oligosac-
charides (GOS), whereas emerging prebiotics include
isomalto-oligosaccharides (IMO), xylo-oligosaccharides
(XOS), resistant starch and soybean oligosaccharides
(SOS). Regarding the latter category, although there is
a moderate amount of data from in vitro and animal
studies suggesting a prebiotic effect in some cases, cur-
rently, there are no published clinical data from human
studies [3,4

,5,6

]. In terms of their production, prebio-

tics are obtained either by extraction from plants, for
example, inulin (extracted from chicory), by enzymatic
hydrolysis of plant polysaccharides, for example, XOS
(produced by enzymatic hydrolysis of xylans from cereal
grains), and by transgalactosylation reactions catalysed by
an enzyme, using either a mono-saccharide or a di-sac-
charide as the substrate, for example, GOS (produced
from lactose using b-galactosidase as the biocatalyst)
[7,8]. Prebiotics can be formulated either as a powder
or syrup and marketed as supplements or incorporated
into food products, most commonly yogurts and breads.
Prebiotics have been associated with a variety of health
benets including an increase in the bioavailability of
minerals, particularly calcium [4

], modulation of the
immune system [3,9], prevention of the incidence or
improvement in the severity and duration of gastrointes-
tinal infections, such as travellers diarrhea, acute diarrhea
and antibiotic-associated diarrhea [3], modication of
inammatory conditions, such as irritable bowel syn-
drome (IBS), ulcerative colitis and inammatory bowel
disease (IBD) [1012], regulation of metabolic disorders
related to obesity [13

,14,15] and reduction of risk of

cancer [16]. It must be noted that the evidence for the
above benets varies signicantly. Signicant amount of
evidence exists for their ability to increase the bioavail-
ability of minerals and stimulate the immune system,
although there is less clear evidence for their prophylactic
or therapeutic role in gastrointestinal infections. The
mechanism through which prebiotics affect the host is
to a large extent through an indirect effect on the host,
and is based on the selective stimulation of specic
intestinal bacteria. This results in the modulation of
the gastrointestinal microbiota and can lead to protection
against harmful microorganisms, to the strengthening of
the barrier function of the epithelia, and to immune
stimulation, although a possible direct immune effect
Available online at www.sciencedirect.com
www.sciencedirect.com Current Opinion in Biotechnology 2012, 23:187191
by prebiotics has also been suggested [3,4

]. Although a
better understanding of the mechanisms of action has
been achieved over the past 15 years, the difculty still
remaining in prebiotic research is to demonstrate that the
exerted health benet is directly associated with the
selective changes in the microbiota. The aim of this
review is to discuss the potential role of prebiotics in
gastrointestinal infections and highlight the key techno-
logical issues for the incorporation of prebiotics into
commonly consumed food products, in particular dairy
products, fruit juices and baked goods.
Prebiotics and gastrointestinal infections
Taking a closer look at the area of gastrointestinal infec-
tions, over the past 15 years there has been an increased
interest in evaluating the potential of prebiotics to prevent
or decrease the severity and duration of acute diarrhea,
travellers associated diarrhea or antibiotic-associated diar-
rhea. The fact that prebiotics act mainly in the large
intestine presents a limitation for their application as
preventative agents against travellers diarrhea; hence
the fact that only two published human trials could be
found on this subject. In the rst study [17], in which 244
healthy subjects took part, it was shown that consumption
of FOS (administered in dried form in sachets) did not
signicantly decrease the number of episodes of diarrhea,
although it gave a signicantly better sense of well-being
during the holiday. The authors of the study concluded
that prebiotics, owing to their mechanism of action, are
probably not sufcient to prevent travellers diarrhea, as
although they can improve colonisation resistance in the
large intestine and thus protect the host from bacterial
infections, they cannot do the same in the small intestine,
where many of the bacterial infections occur; however,
besides this the authors did identify some issues with the
design of the study, which might have affected the results.
On the basis of the above discussion, the authors recom-
mended the use of synbiotics (probiotics and prebiotics at
the same formulation) based on the fact that probiotic
bacteria usually target the small intestine through their
ability to adhere to mucosal surfaces, where they can
displace, compete or exclude invading pathogenic species
[17]. On the contrary, in a more recent study, in which 159
healthy subjects took part, it was shown that consumption
of GOS (administered in dried form in sachets) had a
signicant positive effect in the incidence and duration
of the diarrhea episodes, as well as the overall quality of life
assessment [18]. According to the authors of that study, the
reason for the effectiveness of GOS was probably associ-
ated with the fact that GOS can interact directly with the
host epithelium, thus preventing theadhesion and invasion
of gastrointestinal pathogens [19

].
In respect to antibiotic-associated diarrhea, linked to
Clostridium difcile infections, little amount of research
on the application of prebiotics has been carried out, as in
the case of the travellers diarrhea. A study with patients
of the age of 65 and above consuming FOS (administered
in dried form in sachets) while taking broad-spectrum
antibiotics for 7 days, followed by another 7 days of the
same treatment, reported no signicant effects on diar-
rhea incidence and C. difcile infection [20]. By contrast,
continued consumption of higher amounts of FOS than
the previous study, for 30 days after the cessation of C.
difcile associated diarrhea reduced signicantly the
relapse rate [21]. The above studies highlight the import-
ance of the dose and the mode of delivery on the impact
that prebiotics have.
In respect to acute gastrointestinal infections, the poten-
tial use of prebiotics has been studied in experimental
and animal studies for their ability to protect against a
variety of potential pathogenic bacteria, such as Salmo-
nella enterica serovar Typhimurium (S. Typhimurium),
Listeria monocytogenes and Escherichia coli, with the former
receiving most attention, as Salmonella infections occur
worldwide and can be severe systemic infections [22].
The results from several animal studies point towards a
benecial effect of prebiotics on S. Typhimurium infec-
tions, although there are some studies showing the oppo-
site effect. For example, FOS and inulin protected mice
from S. Typhimurium and reduced their mortality [23],
and furthermore administration of a mixture of GOS and
bidobacteria increased the resistance of mice to S.
Typhimurium infection [24]. In another study, adminis-
tration of GOS to mice immediately prior the S. Typhi-
murium challenge reduced signicantly the colonisation
in the liver and spleen of the mice, and the pathology
associated with the clinical signs of S. Typhimurium
infection in mice [19

]. However, in a set of studies

published by another research group, a reduced resistance
to Salmonella infection was observed in mice fed diets
containing FOS and XOS. Interestingly, this was despite
the fact that a signicant bidogenic effect was observed
(i.e. increase in bidobacteria concentration). The
authors argued that the difference between their study
and the Searle et al. study [19

] could be attributed to the

manner of prebiotic delivery, as in their study the pre-
biotics were continuously ingested, rather than given just
before the S. Typhimirium challenge [22,25]. Further
work in the area of prebiotics and gastrointestinal infec-
tions should aim to elucidate the mechanisms through
which prebiotics participate in the hosts defence against
the different types of infections. More human studies are
also needed with prebiotics and travellers diarrhea and
antibiotic-associated diarrhea to assess their prophylactic
or therapeutic potential. Finally, the effect of the delivery
vehicle and in particular the type of the food matrix used
should be investigated, as it could potentially inuence
the activity of the prebiotics.
Incorporation of prebiotics in foods
In order for prebiotics to be incorporated into food pro-
ducts they should not affect negatively the organoleptic
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Current Opinion in Biotechnology 2012, 23:187191 www.sciencedirect.com
properties of the product and be stable during food
processing. The latter includes mainly processes invol-
ving high temperatures, low pH, or a combination of the
two, and conditions favouring Maillard reactions. These
take place between reducing sugars and amino acids at
high temperatures and result in the production of both
high and low molecular weight compounds; besides
affecting the organoleptic properties of the foods, this
can potentially reduce the prebiotic activity of the carbo-
hydrate, if the prebiotic compound is a reducing sugar
[26]. There is a considerable amount of information on
the stability of prebiotics, in particular, GOS, FOS and
inulin, mainly from experiments using model systems and
to a lesser extent with real foods.
GOS are in general very stable to acidic conditions and
high temperatures and for this reason they can be poten-
tially added to a variety of acid or heated foods, such as
yogurts, fermented milks, buttermilk, pasteurised fruit
juices and bakery products [6

,8], although their main

commercial application is in infant formulas, in which
they are present at around 6.07.2 g/l, together with 0.6
0.8 g/l FOS [27]. Playne and Crittenden [28] reported that
GOS were stable in water-based solutions during heating
at 100 8C and pH 3 for 10 min; at pH 2, only 5% of the
GOS was degraded. At 37 8C and pH 2 they were stable
during storage for several months. A high GOS stability in
various fruit juices, with pH ranging from 2.7 to 4.1, at a
range of pasteurisation conditions (8895 8C for a varying
number of minutes) was also demonstrated; in most cases,
more than 99% of GOS survived pasteurisation [29].
According to several authors, the likely reason for the
high stability of GOS is the presence of b-linkages, which
are very stable to hydrolysis, although other factors, such
as the sugar residues present, the ring form and the
anomeric conguration can play a role too [7,29].
Inulin and FOS have been suggested to be less stable
than other oligosaccharides at conditions of low pH and
high temperatures, especially the combination of the two.
In very acidic conditions, the b(2-1) bonds between the
fructose units can be partially hydrolysed [30]. More
specically, it has been reported that the heating of a
FOS solution pH 3.5 at 145 8Cfor only 10 s resulted in the
hydrolysis of approximately 10% of FOS [7], whereas
exposure of a FOS solution to high temperatures
(85 8C for 30 min), relevant to pasteurisation processing,
resulted in a signicant reduction in its prebiotic activity
score [26]. Similarly, moderate to high levels of degra-
dation were found in another pasteurisation study; at
temperatures between 60 8C and 70 8C, and pH 2.0
and 2.5, FOS degradation ranged from 10% to 30%
[31]. Moreover, in a study investigating the log-term
stability of FOS, it was shown that at pH 2, 63% and
38% of FOS were hydrolysed after 56 days of storage at
37 8C and 18 weeks of storage at 4 8C, respectively [32].
In another study, using fruit juices as the food matrix, it
was concluded that FOS are susceptible to hydrolysis
during pasteurisation, and could even degrade by over
80%, depending on the conditions [29]. The lower
stability of FOS at acidic pH, especially at high tempera-
tures (>70 8C), could be explained by the fact that the
fragility of the fructose-fructose and fructose-glucose C
Oosidic bonds involved in the glycosidic linkages in FOS
increases as the temperature increases [31,33]. Finally, in
an interesting study investigating non thermal processing,
it was shown that FOS incorporated into apple purees,
were stable for over 30 days at 4 8C following high
hydrostatic pressure (HHP) treatment; this opens up
the possibility of incorporating prebiotics into HHP trea-
ted foods. Suggested further work in the topic includes
the evaluation of the stability of established prebiotics in
real food systems rather than model solutions, as there is a
lack of data on this and the scarce existing data suggest
that the food matrix can inuence prebiotic stability. A
lack of data exists also as regards emerging prebiotics.
Another important technological aspect of prebiotics is
their effect on the physicochemical and organoleptic
properties of the food product. Among the established
prebiotics, inulin is used extensively in the food industry
as a fat replacer or texture modier. It has moderate
solubility in water (10% soluble at room temperature),
which is convenient for its incorporation into liquid food
systems, has a neutral taste and is slightly sweet (less than
10% compared to sucrose) [34]. Owing to the above
properties, it is used primarily in low fat dairy products,
including fermented milks, yogurts, dairy desserts,
cheeses and ice cream, as a fat replacer [3537,38

],
and in baked products as a texture modier, often in
combination with dietary bers [3941]. The use of inulin
as a fat replacer is particularly suitable as it might con-
tribute to improved mouthfeel [38]. The reason for this is
inulins gelling properties; at high concentration (>25%
in water for native inulin and >15% for long-chain inulin)
it forms upon shearing a gel, owing to a network of
crystalline particles [42]. More specically, after thorough
mixing with water, a white, creamy gel is formed; this
provides a short and spreadable texture and smooth fatty
mouthfeel, and can be used to completely replace fat into
foods [34]. The physicochemical properties of inulin
depend considerably on its degree of polymerisation;
the longer the chains (degree of polymerisation
DP > 10) the stronger the gel, leading to improved body
and mouthfeel [7,34,43,44]; this is owing to the fact that
the longer chains have a lower solubility, and thus will
crystallise more quickly [38

].
FOS on the other contrary are much more soluble than
inulin (up to 85% soluble at room temperature). They are
fairly sweet (3035% compared to sucrose) and have
similar technological properties to sucrose and glucose
syrups; as a result, they are frequently used as sugar
replacements [30]. They have been already applied in
Prebiotics Charalampopoulos and Rastall 189
www.sciencedirect.com Current Opinion in Biotechnology 2012, 23:187191
a variety of dairy products, as they are the ideal ingredients
to give bulk with fewer calories and increase the functional
value without compromising on the taste and mouthfeel of
the products [34]. They are also used in baked goods and
breads to replace sugar andto retain moisture in theproduct
[45,46]. In respect to GOS, there are few commercial
examples of GOS-containing food products, and very little
information on the impact of GOS on the physicochemical
properties of the food carrier. They are however, as other
oligosaccharides, very soluble in water, mildly sweet (30
35%compared to sucrose) and can be used to improve the
textural properties of dairy products, such as yogurts [6

].
They are also suitable ingredients for use in bread and
baked products, owing to their high moisture retaining
capacity [8], as well as in fruit juices owing to their high
acid stability. As a nal note, the importance of carrying out
research on the impact of both the established and emer-
ging prebiotics on the textural, rheological, sensory and
nutritional properties of food products, especially non-dairy
products, must be highlighted.
Conclusion
Based on the research in the eld of prebiotics, carried out
bynumerous experimental, animal and human studies over
the past 15 years, a number of health benets have been
attributed to prebiotics, with varying levels of evidence
supporting each one. In terms of the role of prebiotics in
gastrointestinal infections, further work is needed to elu-
cidate the mechanisms through which prebiotics partici-
pate in the hosts defence against the different types of
infections, and in particular travellers diarrhea, acute
diarrhea and antibiotic-associated diarrhea. Moreover,
the effect of the delivery vehicle and in particular the type
of the food matrix used should be investigated, as it could
potentially inuence the activity of prebiotics; most of the
studies so far have been carriedout using dried forms of the
prebiotic compounds. In order to incorporate successfully
prebiotics into food products their inuence on the textural
and organoleptic properties of the product is very import-
ant. Although there is a lot of information on the physico-
chemical attributes of inulin, and to a lesser extent of FOS,
there is very little information on GOS and the emerging
prebiotics, such as XOS. In terms of stability, prebiotics are
overall stable under not extreme conditions of high
temperature and low pH, and can therefore be applied
in a variety of acidic products, such as yogurts, pasteurised
fruit juices, as well as baked products, without been
signicantly degraded.
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