Food Research International 43 (2010) 1–7

Contents lists available at ScienceDirect

Food Research International

journal homepage: www.elsevier.com/locate/foodres

Review

Importance of food in probiotic efficacy

R.D.C.S. Ranadheera a,*, S.K. Baines b, M.C. Adams a
a
School of Environmental and Life Sciences, University of Newcastle, NSW 2308, Australia
b
School of Health Sciences, University of Newcastle, NSW 2308, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Foods are carriers for the delivery of probiotics to the human body. In addition, foods help to buffer the
Received 2 June 2009 probiotic through the gastrointestinal tract, regulate their colonization and contain other functional
Accepted 7 September 2009 ingredients, such as bioactive components, which may interact with probiotics to alter their functionality
and efficacy. The growth and survival of probiotics during gastric transit is affected by the physico-chem-
ical properties of food carriers. Gastric acid, juices and bile tolerance, adherence to gastrointestinal
Keywords: epithelium and the acid production of probiotics are also affected by the food ingredients used in probi-
Probiotics
otic delivery. Same probiotic strains could vary in functional and technological properties in the presence
Food
Efficacy
of different food ingredients. Prebiotic food ingredients encourage the growth of probiotic bacteria. The
Growth and viability appropriate combination of prebiotics and probiotics manifest higher potential for a synergistic effect.
Originally, probiotic delivery was consistently associated with foods, particularly dairy foods. But nowa-
days, there is an increasing trend toward using probiotics in different food systems despite its original
sources and even as nutraceuticals, such as in capsules. This changing trend in delivering probiotics
may lead to a reduction in functional efficacy due to the exclusion of the potential synergistic effect of
the food. Thus, selection of suitable food systems to deliver probiotics is a vital factor that should be
considered in developing functional probiotic foods. This review focuses on information related to the
effect of processed food products on functional efficacy of probiotics.
Ó 2009 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2. Beneficial health effects and therapeutic value of probiotics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. Food carriers for probiotics and effect on efficacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3.1. Yogurt as a probiotic carrier food and effect on efficacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Ice cream and frozen products as probiotic carrier food and effect on efficacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.3. Cheese and chocolate products as probiotic carrier foods and effect on efficacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.4. Beverages, cereals and vegetable products and their effect on probiotic efficacy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

1. Introduction
Probiotics are the live microbial feed supplements that benefi-
cially affect the host animal by improving its intestinal microbial
balance (Fuller, 1989). The whole concept of probiotics is not
* Corresponding author. Address: School of Environmental and Life Sciences,
University of Newcastle, Callaghan, NSW 2308, Australia. Tel.: +61 02 49217742;
fax: +61 02 49215492.
E-mail address: senaka.ranadheera@newcastle.edu.au (R.D.C.S. Ranadheera).
new, and in fact they have been consumed by human beings in
the form of fermented foods, for thousands of years (Cross, Steven-
son, & Gill, 2001; Kopp-Hoolihan, 2001). Their health benefit has
also been long known, with Hippocrates and other scientists in
the early ages being reported that fermented milk could cure some
disorders of the digestive system. Even Biblical scriptures men-
tioned the use of probiotics in treating body ailments (Lourens-
Hattingh & Viljoen, 2001). It was in 1907 that the Russian scientist
Elie Metchnikoff first proposed the concept of probiotics as it is
known today. He observed that consumption of large amounts of

0963-9969/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2009.09.009
2 R.D.C.S. Ranadheera et al. / Food Research International 43 (2010) 1–7

fermented milk products containing lactobacilli prolonged life and
gave the first scientific explanation for the beneficial effects of lac-
tic acid bacteria present in fermented milk (Rasic, 2003). Today it is
accepted that daily intake of these probiotics contributes to
improving and maintaining well balanced intestinal flora, and pre-
vents gastrointestinal disorders (Lavermicocca, 2006).
Various species of genera Lactobacillus and Bifidobacterium
mainly and some other species of micro-organisms have been used
as probiotics over the years (Boyle & Tang, 2006). Different strains
of Lactobacillus acidophilus, Lactobacillus casei, Lactobacillus crispatus,
Lactobacillus delbrueckii subsp. Bulgaricus, Lactobacillus fermentum,
Lactobacillus gasseri, Lactobacillus johnsonii, Lactobacillus paracasei,
Lactobacillus plantarum, Lactobacillus reuteri, Lactobacillus rhamnous,
Lactobacillus helveticus, Lactobacillus lactis, Bifidobacterium bifidum,
Bifidobacterium breve, Bifidobacterium infantis, Bifidobacterium lon-
gum, Bifidobacterium lactis, Bifidobacterium adolescentis, Bifidobacte-
rium essensis, Bifidobacterium laterosporus and other species like
Escherichia coli Nissle, Saccharomyces boulardii, Streptococcus ther-
mophilus, Enterococcus francium, Propionibacterium, Pediococcus
and Leuconostoc could be considered as the main microbial species
that have been used as probiotics (Senok, Ismaeel, & Botta, 2005;
Shah, 2007). There are however, concerns regarding the safety of
probiotics other than Lactobacillus and Bifidobacterium, since some
of these genera contain many pathogenic species, particularly
Enterococcus. Streptococcus salivarius subsp. thermophilus and Lacto-
bacillus delbrueckii subsp. bulgaricus have been traditionally used in
yoghurt production. Since these micro-organisms are not expected
to survive and grow in the host’s intestinal tract, they are not cate-
gorized as probiotics by most scientists and are considered as yo-
gurt cultures (Senok et al., 2005). Regardless of the diversity of
these micro-organisms, the main probiotic preparations currently
available on the market belong to a group of bacteria designated
as lactic acid bacteria (e.g. Lactobacilli, Streptococci and Bifidobacte-
ria), which are important normal constituents of the human gastro-
intestinal microflora and produce lactic acid as a major metabolic
product (Penner, Fedorak, & Madsen, 2005; Reddy, Altaf, Naveena,
Venkateshwar, & Kumar, 2007). These probiotics used in foods have
previously been primarily added as part of the fermentation pro-
cess, however increasingly they are added as supplements. Further
there is also an increasing trend in using probiotics as nutraceuti-
cals, being available in various forms such as in capsules. This
changing trend in probiotic delivery may lead to reduced functional
efficacy due to exclusion of the potential synergistic effect of the
food.
Food substrate/diet is considered as one of the major factors in
regulating colonization of micro-organisms in gastrointestinal
tract. Food helps to buffer the bacteria through the stomach and
may contain other functional ingredients that could interact with
probiotics to alter their functionality. Colonic foods, which encour-
age the growth of favourable bacteria, are referred to as prebiotics.
Oligosaccharides such as lactulose, galactooligosaccharides, inulin,
fructooligosaccharides, and other food carbohydrates are some of
the well known examples of prebiotics. There is an obvious poten-
tial for a synergetic effect when combining probiotics and prebiot-
ics appropriately, because prebiotics promote the growth and
activities of probiotics (Table 1). By increasing the amount of pre-
biotics in the diet, it is possible to increase and maintain healthy
bacterial gut flora in the host (Gibson, Rastall, & Fuller, 2003;
Sanders, 1998). Ingredients in certain food products may naturally
contain prebiotics which help to improve the functional efficacy of
probiotics. Many other foods such as dairy and meat products,
cereals, beverages and infant formulates can be fortified with pre-
biotics during manufacturing process to increase probiotic efficacy
(Gibson, Probert, Rastall, & Roberfroid, 2004). In addition a number
of other suitable food components including non-specific sub-
strates, plants and their extracts, metabolites of micro-organisms
and polyunsaturated fatty acids may also be important in probiotic
efficacy (Bomba et al., 2006). Physico-chemical properties of food
carriers used for probiotic delivery, such as buffering capacity
and pH, are significant factors that influence survival of the probi-
otic and hence potential probiotic effects during gastric transit.
Food formulations with appropriate pH ranges and high buffering
capacity would increase the pH of the gastric tract and thereby en-
hance the stability of probiotics (Kailasapathy & Chin, 2000). Since
combinations of probiotics with synergistically acting components
and properties such as pH from the food seems to be one of the
best ways of improving probiotic efficacy, careful selection of the
food matrix is an important factor that should be considered in
developing probiotic products. In this context, this paper reviews
the current literature related to effects of different food carries
on probiotic efficacy with the aim of identifying food substrate as
one of the most important factors in probiotic efficacy.
2. Beneficial health effects and therapeutic value of probiotics
There are several evidences supporting potential clinical appli-
cations of probiotics in the prevention and treatment of diseases of
the gastrointestinal, respiratory and urogenital tracts (Gardiner
et al., 2002). Probiotics may provide a number of potential health
benefits mainly through maintaining good balance and composi-
tion of intestinal flora, helping to increase the body’s ability to re-
sist the invasion of pathogens and maintain the host’s well being
(D’Aimmo, Modesto, & Biavati, 2007). Maintenance of normal
intestinal gut microflora, protection against gastrointestinal patho-
gens (Lourens-Hattingh & Viljoen, 2001), enhancement of the im-
mune system, reduction of lactose intolerance (Gilliland, 1990;
Kim & Gilliland, 1983), reduction of serum cholesterol level and
blood pressure (Rasic, 2003), anti-carcinogenic activity (Gilliland,
1990; Ouwehand, Kirjavainen, Shortt, & Salminen, 1999; Rasic,
2003), improved utilization of nutrients and improved nutritional
value of food (Lourens-Hattingh et al., 2001) are some of these
identified benefits. Therefore, probiotics have been widely used
in therapeutic applications including prevention of urogenital dis-
eases (candidal vaginitis), alleviation of constipation, protection
against traveller’s diarrhoea, prevention of infantile diarrhoea,
reduction of antibody-induced diarrhoea, control of inflammatory
bowel diseases and irritable bowel syndrome (Brigidi, Vitali, Swen-
nen, Bazzocchi, & Matteuzzi, 2001; Nobaek, Johansson, Molin,
Ahrne, & Jeppsson, 2000; Saarela, Lahteenmaki, Crittenden, Salmi-
nen, & Mattila-Sandholm, 2002; Venturi et al., 1999), reduction of
hypercholesterolemia, protection against colon and bladder cancer,
prevention of osteoporosis and prevention of food allergy and ato-
pic diseases (Lourens-Hattingh et al., 2001). Although some of
these benefits are yet to be thoroughly proven, these potential ben-
efits may result from the growth and action of the probiotic during
the manufacturing of cultured foods, while some may result from
the growth and action of certain species of probiotics in the intes-
tinal tract following ingestion of foods containing them (Lourens-
Hattingh et al., 2001; Rasic, 2003).
3. Food carriers for probiotics and effect on efficacy
Fat content, concentration and type of proteins, sugars and pH
of the product are some factors that could affect probiotic growth
and survival in food. Therefore, product formulation can be manip-
ulated to aid their efficacy. Food, particularly dairy products are
considered as an ideal vehicle for delivering probiotic bacteria to
the human gastrointestinal tract (Ross, Fitzgerald, Collins, & Stan-
ton, 2002). At present probiotic bacteria are mainly incorporated
into dairy products such as cheese, yogurt, ice cream and other
dairy desserts. Limitations of dairy products such as the presence
 R.D.C.S. Ranadheera et al. / Food Research International 43 (2010) 1–7 3

Table 1
Beneficial effects of prebiotics on probiotic bacteria in foods.

Food Prebiotics Probiotics Effect Reference

Yogurt Hi-maize/resistant L. acidophilus "Growth and viability Donkor et al. (2007)
starch L. casei
Inulin L. acidophilus "Growth and viability Hekmat, Soltani, and Reid (2009)
L.casei Aryana and McGrew (2007)
L. rhamnosus Donkor et al. (2007)
L. reuteri Capela et al. (2006)
Bifidobaceterium
Fructooligosaccharides L. acidophilus "Viability and fatty (Akalin, Tokusoglu, Gonc and Aycan
acid production (2007)
L.casei Akalin, Fenderya, and Akbulut (2004)
L. rhamnosus Capela et al. (2006)
Bifidobaceterium
B. animalis
B. longum

Fermented milk Polydextose L. acidophilus "Growth, viability and fatty acid Oliveira et al. (2009)
L. rhamnosus production
B. animalis subsp. lactis
Oligofructose L. acidophilus "Growth, viability and fatty acid Oliveira et al. (2009)
L. rhamnosus production
B. animalis subsp. lactis

Ice cream Inulin L. acidophilus "Viability AkIn et al. (2007)

B. lactis

Cheese and cheese-based Oligofructose L. acidophilus "Growth, viability, sensory Cardarelli, Saad, Gibson, and Vulevic
products and fatty acid production (2007)
B. animalis subsp. lactis Cardarelli et al. (2008)
Inulin L. acidophilus "Growth, viability, sensory Cardarelli et al. (2007)
B. animalis subsp. lactis and fatty acid production Cardarelli et al. (2008)
Carboxy methyl P. freudenreichii subsp. "Growth Buriti et al. (2005)
cellulose shermanii

of allergens and the requirement for cold storage facilities, as well
as an increasing demand for new foods and tastes have initiated a
trend in non-dairy probiotic product development (Lavermicocca,
2006). Further it is important to develop probiotic products with
food and beverages that are part of day to day normal diet to main-
tain minimum therapeutic level easily. Higher levels of viable mi-
cro-organisms (1  107 cfu/g) are recommended in probiotic
foods for better efficacy in regulating beneficial effects (Gardiner
et al., 2002; Vinderola & Reinheimer, 2000). Better growth and sur-
vivability during food manufacturing and storage as well as in gas-
trointestinal tract, protection against acid, bile and gastrointestinal
enzymes, adhesion to intestinal epithelium, antimicrobial proper-
ties and antibiotic resistance could be considered as factors that
might be important in maintaining probiotic efficacy. However,
viability of probiotic is arguably the most important factor since
it could affect all the other parameters.
3.1. Yogurt as a probiotic carrier food and effect on efficacy
Yogurt and fermented milks are considered as the main vehicle
for probiotic delivery. Usually yogurt is prepared by allowing milk
to ferment by specific pure cultures of lactic acid bacteria (S. ther-
mophilus and L. bulgaricus cultures) (Lourens-Hattingh & Viljoen,
2001). Increasingly yogurts have been prepared with probiotic mi-
cro-organisms with varying viability over a range of shelf lives.
Different yogurts have demonstrated different viability levels of
probiotics over shelf lives. In 2000 Birollo, Reinheimer and Vinde-
rola observed that in whole set-yogurt the level of streptococci de-
creased approximately 1 log cycle at 6 °C in 60 days shelf life.
While they remained viable and even reproduce in skimmed set-
yogurt under the same conditions. When whole set-yogurts are
produced together with a concentrated product of heated milk
and sugar, their viability decreased 1.5 log cycles. Higher milk fat
content further demonstrated inhibitory effects for probiotic cul-
tures, particularly B. bifidum BBI in yogurts (Vinderola, Bailo, &
Reinheimer, 2000). Plain-yogurts demonstrated significant ability
in retaining a higher level of L. acidophilus over the shelf life com-
pared to yogurts containing mixed berry or passion fruits. How-
ever, interestingly, yogurts containing mango or strawberry
contained higher level of L. acidophilus than the plain-yogurts dem-
onstrating the effect of different properties of various fruit mix-
tures such as pH on the viability of probiotics in yogurt. This
study further showed that the correlation between post storage
pH in yogurts and the viability of probiotics is affected by the pres-
ence of fruit pulp (Kailasapathy, Harmstorf, & Phillips, 2008). Sur-
vival of L. acidophilus is affected by the low pH of the
environment (Shah, Lankaputhra, Britz, & Kyle, 1995). Therefore,
fruit mixtures or any other added ingredients that contribute to a
lowering of pH in yogurt may contribute in reducing the vivability
of L. acidophilus. Different nutrient compositions such as vitamin
levels of fruit juice may also have an influence on viability. Fortifi-
cation with ascorbic acid was reported to improve viability of L.
acidophilus in yogurts although this was not to have any effect on
bifidobacteria (Dave & Shah, 1997b). Oxygen scavenging effect of
ascorbic acid is one of the possible reasons that may help to im-
prove the viability of probiotics. Yogurt starter culture bacteria
are also identified as oxygen scavengers. These cultures were
demonstrated to finish the food fermentation within 5–10 h and
utilized most of the oxygen in milk (Dave & Shah, 1997b). There-
fore, incubation time of the product also affects the viability of
probiotics in yogurt. In the case of longer incubation period, added
oxygen scavengers may not cause an advantage in improving
4 R.D.C.S. Ranadheera et al. / Food Research International 43 (2010) 1–7
viability. In addition to incubation period, incubation temperature
and storage time of yogurts appeared to be affected on the cell via-
bility (AkIn, AkIn, & KirmacI, 2007). On the other hand stirred-yo-
gurts might result low viability levels compared to plain-yogurts if
the probiotic strain is less tolerant to oxygen, because oxygen is
incorporated into yogurts while stirring fruit pulp into yogurt base.
Kailasapathy et al. (2008) reported rapid loss of viability of Bifido-
bacterium animalis subsp. lactis with increasing percentage of fruit
pulp added into yogurt base. Acidity of stirred fruit yogurt could be
increased with the addition of more fruit pulp into yogurt base
resulting in rapid viability losses. Therefore, addition of substances
such as whey protein into yogurt may enhance the viability of
some probiotics due to maintaining the buffering capacity of
yogurt.
Higher viability of L. acidophilus was demonstrated in response
to added cysteine at 250 and 500 mg L1 in yogurt during manu-
facture and storage while viability of bifidobacteria was adversely
affected by the same levels in different starter cultures. In the same
study, bifidobacteria demonstrated better viability in a concentra-
tion of 50 mg L1 of cysteine. Greater drops in pH, observed in
yogurts with higher cysteine concentrations, may result in adverse
effect on bifidobacteria, while the availability of amino nitrogen
from cysteine caused positive effect on growth of both probiotic
species, but in different concentrations. Different culture combina-
tions used in these experiments may also have an affect on the
different viability levels due to antagonistic or symbiotic relation-
ships (Dave & Shah, 1997a, 1997c). Furthermore, addition of cys-
teine greatly improved the growth and viability of L. acidophilus,
Lactobacillus paracasei subsp. casei and also B. bifidum in goat milk
yogurts during fermentation and storage (Güler-AkIn & AkIn,
2007). Addition of ‘‘Hi-maize” or amylase maize starch (a natural
dietary fiber/resistant starch) and inulin has demonstrated signifi-
cant improvement on growth, viability and organic acid production
of L. acidophilus and L. casei in set-yogurts. Interestingly, in the
presence of inulin, both cultures showed better retention of viabil-
ity compared to Hi-maize. However, proteolytic activity of these
cultures significantly improved in the presence of Hi-maize in
comparison to that in the presence of inulin or without any supple-
mentation (Donkor, Nilmini, Stolic, Vasiljevic, & Shah, 2007). This
demonstrates some prebiotics are a much better medium com-
pared to other prebiotics and their influence on different functional
properties of probiotics. Furthermore, prebiotics can selectively
stimulate the growth and activity of probiotics (Gibson et al.,
2004). Positive effects of adding Hi-maize, inulin and fructooligo-
saccharides on viability of L. acidophilus, L. casei, Lactobacillus
rhamnosus and Bifidobacterium spp. were also observed by Capela,
Hay, and Shah (2006) in yogurts. These authors reported fructool-
igosaccharides as the most effective prebiotic in helping to retain
the viability of probiotics. All these prebiotics could improve met-
abolic activities of probiotics and resulting in higher functional
efficacy. Different viability levels of L. casei have also been reported
from commercial yogurts with various physical and chemical com-
positions (Ravula & Shah, 1998b). Thus, it is clear that viability and
some functional properties of probiotic bacteria in yogurt are
related to the characteristics of the carrier food product including
its chemical composition. However, functional efficacy of these
probiotics is not only governed by the chemical composition of
the carrier medium but also by the several other factors that
should be further investigated.
3.2. Ice cream and frozen products as probiotic carrier food and effect
on efficacy
Ice cream and frozen dairy deserts demonstrated great potential
for use as vehicles for probiotic cultures. Ice cream is considered
favourably as a probiotic carriers due to the lower storage temper-
ature and less risk of temperature abuse during frozen storage
which leads to higher viability of probiotics at the time of con-
sumption (Cruz, Antunes, Sousa, Faria, & Saad, 2009) .
Ice cream made from different levels of fat and added sugar
have shown different survival rates of probiotic strain L. johnsonii
La 1 at 30 days of storage at 28 °C. These authors also observed
different survival rates of the same bacteria to bile resistant tests
in vitro. A 0.4% concentration of bile caused a 50% reduction of
the initial cell counts of fresh cells and a 30% reduction of fro-
zen–thawed cells. For higher bile concentrations, survival rates sta-
bilized at around 30% and 15% for fresh and frozen–thawed cells,
respectively (Alamprese, Foschino, Rossi, Pompei, & Savani,
2002). Lactic streptococci/lactic starter cultures also demonstrated
different percentage of viability, acid development and proteinase
activity under different frozen storage temperatures in skim milk
medium (Cowman & Speck, 1965). Therefore, when a probiotic
strain is used to produce frozen food product their efficacy in the
small intestine may vary from non frozen food product fortified
with the same strain. Probiotics incorporated into frozen food
products have further demonstrated better viability during shelf
life (Heenan, Adams, Hosken, & Fleet, 2004; Kebary, 1996). A slight
increase in cell concentration of bifidobacteria, during frozen soy
dessert manufacture was reported by Heenan et al. (2004). This
could happen possibly due to bacterial chain disruption by
mechanical churning during freezing. They also observed a de-
crease in the viability of some probiotic species during manufac-
ture and freezing as reported by others (Alamprese et al., 2002;
Ravula & Shah, 1998a). Better survivability of probiotics in frozen
products could be due to the lower temperature that they are held
at and subjected to less temperature abuse. However, damage to
cells caused by freezing and thawing, mechanical stresses of mix-
ing and incorporation of oxygen into the mixture during manufac-
turing may result lower viability and thereby exert a negative
effect on functional efficacy of probiotics in frozen products after
ingestion. Added inulin also demonstrated significantly higher via-
bility of L. acidophilus and B. lactis in ice cream due to prebiotic ef-
fect. It is also found that viability of these probiotics may vary
depending on the sugar levels of ice cream (AkIn et al., 2007).
3.3. Cheese and chocolate products as probiotic carrier foods and effect
on efficacy
Cheese is a versatile food product, appealing to many palates
and is suitable for all age groups and provides a valuable alterna-
tive to yogurt and fermented milk as a vehicle in probiotic delivery.
Consumption of cheese has increased in many countries during
past decade (da Cruz, Buriti, de Souza, Faria, & Sadd, 2009), provid-
ing additional advantage of use of cheese products in probiotic
delivery. Furthermore, aerated dairy deserts such as chocolate
mousse have also shown a great market potential and potential
as probiotic delivering agents (Aragon-Alegro, Alegro, Cardarelli,
Chiu, & Sadd, 2007).
Production of petit-suisse cheese with oligofructose and/or inu-
lin was reported to be excellent in terms of viability of both L. aci-
dophilus and B. animalis subsp. lactis while addition of eucalyptus
honey reduced the viability level of L. acidophilus and B. animalis
subsp. lactis in the same cheese. The low oligosaccharides content
of honey may lead to poor growth and this could explain in part the
poor viability reported. Interestingly cheese produced with oligo-
fructose and inulin demonstrated better consumer acceptability
indicating advantages of selected prebiotics not only in probiotic
growth viability and stability, but also in improving sensory qual-
ities (Cardarelli, Buriti, Castro, & Saad, 2008). Viability of L. paraca-
sei subsp. paracasei LBC 82 in Minas fresh cheese manufactured
through direct acidification with lactic acid increased from 6.61
up to 8.22 log cfu/g during 21 days of storage at 5 °C (Buriti, da
 R.D.C.S. Ranadheera et al. / Food Research International 43 (2010) 1–7
Rocha, Assis, & Saad, 2005), whereas, viability of the same strain in
chocolate mousse increased slightly from 7.36 up to 7.66 log cfu/g
under the same storage conditions during 21 days (Aragon-Alegro
et al., 2007), demonstrating influences of different types of food
product on probiotic growth and viability. Therefore, choosing a
suitable food system is important in delivering certain species or
strains of probiotics. Although inulin helps to improve the growth
and viability of various probiotic species in a number of different
products (Capela, Hay, & Shah, 2006; Cardarelli et al., 2008), addi-
tion of inulin did not influence the viability of L. paracasei subsp.
paracasei in chocolate mousse.
Cheddar cheese ripening temperature significantly affected only
the viability of starter lactococci and some other physico-chemical
properties of the final product when combined with certain bifido-
bacteria and Lactobacillus strains. This may be due to combination
of low pH, high NaCl and lack of fermentable carbohydrates (Ong &
Shah, 2009) which might have some negative effect on the viability
of probiotic bifidobacteria and lactobacilli strains if cheese were
further ripened. Although not significant, in combination with
few other probiotics, Propionibacterium freudenreichii subsp. sher-
manii has shown better growth in the presence of canola oil and
a mixture of carboxy methyl cellulose and xanthan gums in
cheese-based French onion dips. A minimal or no antagonistic ef-
fect might be a possible reason for these results. Addition of acetic
acid has shown a negative effect on L. acidophilus survivability
compared to lactic acid or citric acid while B. animalis performed
better in acetic acid than other two acids in the same product. This
might be due to more resistance of B. animalis to acetic acid com-
pared to other bacteria since acetic acid is one of their metabolites.
On average P. freudenreichii subsp. shermanii and L. paracasei subsp.
paracasei survived better than L. acidophilus and B. animalis in the
presence of organic acids during storage. Furthermore, all these
strains have demonstrated different viability levels at different
pH levels created by above acids. Since these acids are naturally
occurring and most commonly used organic acids in the food
industry to enhance safety and organoleptic properties, combina-
tion of suitable strains, and type and level of acids should be con-
sidered in developing functional probiotic foods to have maximum
efficacy. Viability of all the bacteria was greater in dips with NaH-
CO3 compared to L-cysteine and without any of these food addi-
tives, possibly due to buffering capacity of NaHCO3 in reducing
acid effect (Tharmaraj & Shah, 2004).
3.4. Beverages, cereals and vegetable products and their effect on
probiotic efficacy
Although most of the current probiotic foods are mainly dairy
based, there is a growing interest in the development of non-dairy
probiotic products due to problems such as lactose intolerance in
many people and the unfavourable cholesterol content of fer-
mented dairy products. In addition there is an increasing demand
for vegetarian probiotic products (Heenan et al., 2004). This has
led to development of probiotic products from various food metrics
including fruits (Lavermicocca, 2006), vegetables (Yoon, Woodams,
& Hang, 2006), legumes (Heenan et al., 2004) and cereal products
(Helland, Wicklund, & Narvhus, 2004).
According to Oliveira, Sodini, Remeuf, and Corrieu (2001) differ-
ent milk supplementation such as sweet whey, casein hydrolysate
and milk proteins had effects on microbiological stability of fer-
mented drinking milk containing probiotic L. acidophilus and L.
rhamnosus with or without S. thermophilus. Addition of whey pro-
tein concentrate has further been reported to significantly influ-
ence the viability of Bifidobacterium BB-12 in the fermented
goats’ milk during refrigerated storage (Martin-Diana, Janer, Pe-
laez, & Requena, 2003). Incorporation of micronutrients into the
milk, such as peptides and amino acids, with these ingredients,
5
may be useful in reducing fermentation time and thereby delay
acidification. Commercially available different fermented drinking
milks also have shown various viability levels of L. casei (Ravula &
Shah, 1998b). Addition of soygerm powder has shown certain po-
sitive effects on producing fermented milk with L. reuteri, because
soygerm powder may release important bioactive isoflavones dur-
ing fermentation that could protect L. reuteri from bile salt toxicity
in the small intestine (De Boever, Wouters, & Verstraete, 2001).
Addition of soy protein to fermented soymilk has been reported
to lower the probiotic inhibition activity of bile due to their poten-
tial ability in binding and aggregating bile salts (Shimakava,
Matsubara, Yuki, Ikeda, & Ishikawa, 2003; Sugano et al., 1990).
When L. acidophilus, L. gasseri, Propionibacterium jensenii 702 and
B. lactis are grown in cow’s milk and goat’s milk, their growth as
well as in vitro cytokine production appeared to be influenced by
the type of milk that they were grown (Ranadheera, Ho, Luo, &
Adams, 2007). This might be caused due to different levels of
growth stimulation by different media. P. jensenii 702 is a potential
probiotic bacteria isolated from raw cow’s milk (Huang, Kotula, &
Adams, 2003), therefore, its metabolic activities in cow’s milk
might be much better than in goat’s milk or any other medium
and may result in better growth, survival and stability when incor-
porated into cow’s milk.
Microencapsulated B. lactis in traditional African fermented bev-
erages has shown significantly higher survival rates in the presence
of stimulated gastric juice and considerable higher viability over the
shelf life compared to free cells (McMaster, Kokott, Reid, & Abratt,
2005). Microencapsulation was also found to improve the viability
of probiotics in freeze-dried yogurt after 6 months of storage at 4
and 21 °C (Capela et al., 2006). This is because microencapsulation
helps to reduce cell injury and cell loss by retaining cells within
the encapsulating materials (Ravula & Shah, 2003). After 2 months
of refrigerated storage viability of L. gasseri was reported to be re-
duced by 0.5 log cfu/g in spray dried milk powder and 1 log cfu/g
in spray dried kudzu powder, a starch derived from roots of Pueraria
lobata which has traditionally been used as a food ingredient in East
Asia. Probiotic survivability in the presence of simulated small
intestinal juice was also varied depending on the carrier material
(Ho, Adams, & Le, 2007). Different cryoprotectants used in freeze
drying further altered probiotic stability in food products due to
inhibition of intracellular or extracellular ice formation by binding
to the water (Capela et al., 2006; Ravula & Shah, 2003). Sucrose pro-
tected B. animalis subsp. lactis exhibited significantly higher sur-
vival rate than reconstituted skim milk protected cells in fruit
juice. However, the same probiotic has shown better stability in
low fat milk during 2 weeks of refrigerated storage compared to or-
ange, grape or passion fruit juices. Furthermore, their acid and bile
tolerance were also much better in milk than in fruit juice. This may
be due to additional protective effect of milk beside its buffering
capacity (Saarela, Virkajarvi, Alakomi, Sigvart-Mattila, & Matto,
2006). Thirteen different strains of dairy propionibacteria demon-
strated significantly higher capacity of in vitro upper gastrointesti-
nal transit tolerance in the presences of soy milk and commercial
liquid breakfast mixture. Increase of pH of reaction mix after addi-
tion of these foods, is one of the factors that contributed to the
improvement of the viability of tested dairy strains. These results
further suggested that low-acid tolerant strains need not be ex-
cluded from probiotic applications, because they can be delivered
to the intestine in high numbers, as part of a buffered food or encap-
sulated delivery system in order to achieve maximum efficacy
(Huang & Adams, 2004). Significantly lower viable counts of L. aci-
dophilus, L. rhamnosus GG and B. animalis Bb 12 were obtained dur-
ing fermentation and storage of water based cereal puddings
compared to milk-based cereal puddings, indicating different
growth and stability of these probiotics depend on the type of foods
in which they were fortified. The pH levels of the products
6 R.D.C.S. Ranadheera et al. / Food Research International 43 (2010) 1–7
depended on the strain used and whether the products were based
on milk or water. Water based puddings obtained significantly low-
er pH levels and faster reduction in pH during storage which could
adversely affect probiotic growth and viability (Helland et al., 2004).
Malt, wheat and barley extracts have a positive influence in increas-
ing bile tolerance of L. acidophilus, L. reuteri and L. plantarum. How-
ever, addition of malt demonstrated a greater positive influence
while barley and wheat extracts demonstrated similar levels of
influence in retaining viability (Michida et al., 2006; Patel, Pandiella,
Wang, & Webb, 2004). Immobilization of L. plantarum within malt
and barley fiber seems to play a major role on the gastrointestinal
tolerance (Michida et al., 2006). Furthermore, malt medium has
demonstrated better support for the growth of L. acidophilus, L. fer-
mentum, L. reuteri and L. plantarum than wheat or barley mediums
due to its favourable chemical composition and availability of con-
siderable amount of maltose, sucrose, glucose, fructose and free
amino nitrogen (Charalampopoulos, Pandiella, & Webb, 2002).
Thus, composition of cereals and individual components appeared
to play a major role in these beneficial protective effects. Higher sur-
vival rates of L. paracasei, L. plantarum and some other probiotics in
table olives and artichokes have been reported during storage as
well as in vitro and in vivo gastrointestinal conditions. These sur-
vival rates are quite comparable or even higher than those of
milk-based probiotic products. This high viability is caused by the
micro-architecture of these vegetables, where roughness might
protect the probiotic in an acid environment, presence of prebiotic
substances and positively influence the survival due to the release
of nutrients from vegetables (Lavermicocca, 2006; Lavermicocca
et al., 2005; Valerio et al. 2006). Therefore, not only chemical
composition of foods but their physical structures are important
in probiotic efficacy that they are bearing.
More intensive lactic acid production was reported in carrot
juice fermented with brewer’s yeast autolysate and L. acidophilus
compared to beetroot juice because of the high content of minerals
influencing lactic acid fermentation in the carrot juice. However,
the increase of the number of L. acidophilus was higher in the beet-
root juice (Rakin, Vukasinovic, Siler-Marinkovic, & Maksimovic,
2007). L. plantarum, L. delbrueckii and L. casei grew well and
reached nearly similar cell concentrations in cabbage juice after
48 h of fermentation at 30 °C. However, only L. plantarum and L.
delbrueckii have shown satisfactory viability rates in fermented
cabbage juice up to 4 weeks of cold storage while L. casei lost cell
viability completely after 2 weeks under same conditions (Yoon
et al., 2006). That may be due to negative impact of chemical con-
stituents of cabbage on L. casei viability and functionality.
4. Conclusions
When considered together the above mentioned evidences rein-
force the fact that food can influence growth, viability and survival,
acid and bile tolerance, and different functionality of probiotics that
determine their efficacy in gastrointestinal tract. Thus, careful inves-
tigation of the interaction of different probiotics and food compo-
nents should be considered in developing functional probiotic
foods. More research is needed to determine the effect of food
substrate on adhesion to intestinal epithelium, antimicrobial
properties, antibiotic resistance and other metabolic activities of
probiotics.
References
Akalin, A. S., Fenderya, S., & Akbulut, N. (2004). Viability and activity of
bifidobacteria in yoghurt containing fructooligosaccharide during refrigerated
storage. International Journal of Food Science and Technology, 39, 613–621.
Akalin, A. S., Tokusoglu, O., Gonc, S., & Aycan, S. (2007). Occurrence of conjugated
linoleic acid in probiotic yoghurts supplemented with fructooligosaccharide.
International Dairy Journal, 17, 1089–1095.
AkIn, M. B., AkIn, M. S., & KirmacI, Z. (2007). Effects of inulin and sugar levels on the
viability of yogurt and probiotic bacteria and the physical and sensory
characteristics in probiotic ice-cream. Food Chemistry, 104(1), 93–99.
Alamprese, C., Foschino, R., Rossi, M., Pompei, C., & Savani, L. (2002). Survival of
Lactobacillus johnsonii La 1 and influence of its addition in retail-manufactured
ice cream produced with different sugar and fat concentrations. International
Dairy Journal, 12(2–3), 201–208.
Aragon-Alegro, L. C., Alegro, J. H. A., Cardarelli, H. R., Chiu, M. C., & Sadd, S. M. I.
(2007). Potentially probiotic and synbiotic chocolate mousse. LWT-Food Science
and Technology, 40(4), 669–675.
Aryana, K. J., & McGrew, P. (2007). Quality attributes of yogurt with Lactobacillus
casei and various prebiotics. LWT-Food Science and Technology, 40, 1808–
1814.
Birollo, G. A., Reinheimer, J. A., & Vinderola, C. G. (2000). Viability of lactic acid
microflora in different types of yoghurt. Food Research International, 33(9),
799–805.
Bomba, A., Jonecova, Z., Koscova, J., Nemcova, R., Gancarcikova, S., Mudronova, D.,
et al. (2006). The improvement of probiotics efficacy by synergistically acting
components of natural origin: A review. Biologia, 61(6), 729–734.
Boyle, R. J., & Tang, M. L. (2006). The role of probiotics in the management of allergic
disease. Clinical & Experimental Allergy, 36(5), 568–576.
Brigidi, P., Vitali, B., Swennen, E., Bazzocchi, G., & Matteuzzi, D. (2001). Effects of
probiotic administration upon the composition and enzymatic activity of
human fecal microbiota in patients with irritable bowel syndrome or functional
diarrhea. Research in Microbiology, 152(8), 735–741.
Buriti, F. C. A., da Rocha, J. S., Assis, E. G., & Saad, S. M. I. (2005). Probiotic potential of
Minas fresh cheese prepared with the addition of Lactobacillus paracasei.
Lebensmittel-Wissenschaft und-Technologie, 38(2), 173–180.
Capela, P., Hay, T. K. C., & Shah, N. P. (2006). Effect of cryoprotectants, prebiotics and
microencapsulation on survival of probiotic organisms in yoghurt and freeze-
dried yoghurt. Food Research International, 39(2), 203–211.
Cardarelli, H. R., Buriti, F. C. A., Castro, I. A., & Saad, S. M. I. (2008). Inulin and
oligofructose improve sensory quality and increase the probiotic viable count in
potentially synbiotic petit-suisse cheese. LWT-Food Science and Technology,
41(6), 1037–1046.
Cardarelli, H. R., Saad, S. M. I., Gibson, G. R., & Vulevic, J. (2007). Functional petit-
suisse cheese: Measure of the prebiotic effect. Anaerobe, 13, 200–207.
Charalampopoulos, D., Pandiella, S. S., & Webb, C. (2002). Growth studies of
potentially probiotic lactic acid bacteria in cereal-based substrates. Journal of
Applied Microbiology, 92(5), 851–859.
Cowman, E. A., & Speck, M. L. (1965). Ultra-low temperature storage of lactic
Streptococci. Journal of Dairy Science, 48(11), 1531–1532.
Cross, M. L., Stevenson, L. M., & Gill, H. S. (2001). Anti-allergy properties of
fermented foods: An important immunoregulatory mechanism of lactic acid
bacteria? International Immunopharmacology, 1(5), 891–901.
Cruz, A. G., Antunes, A. E. C., Sousa, A. L. O. P., Faria, J. A. F., & Saad, S. M. I. (2009).
Ice-cream as a probiotic food carrier. Food Research International, 42(9),
1233–1239.
da Cruz, A. G., Buriti, F. C. A., de Souza, C. H. B., Faria, J. A. F., & Sadd, S. M. I. (2009).
Probiotic cheese: Health benefits, technological and stability aspects. Trends in
Food Science & Technology, 20, 344–354.
D’Aimmo, M. R., Modesto, M., & Biavati, B. (2007). Antibiotic resistance of lactic acid
bacteria and Bifidobacterium spp. Isolated from dairy and pharmaceutical
products. International Journal of Food Microbiology, 115(1), 35–42.
Dave, R. I., & Shah, N. P. (1997a). Effect of cysteine on the viability of yoghurt and
probiotic bacteria in yoghurts made with commercial starter cultures.
International Dairy Journal, 7, 537–545.
Dave, R. I., & Shah, N. P. (1997b). Effectiveness of ascorbic acid as an oxygen
scavenger in improving viability of probiotic bacteria in yoghurts made with
commercial starter cultures. International Dairy Journal, 7(6–7), 435–443.
Dave, R. I., & Shah, N. P. (1997c). Viability of yoghurt and probiotic bacteria in
yoghurts made from commercial starter cultures. International Dairy Journal,
7(1), 31–41.
De Boever, P., Wouters, R., & Verstraete, W. (2001). Combined use of Lactobacillus
reuteri and soygerm powder as food supplement. Letters in Applied Microbiology,
33(6), 420–424.
Donkor, O. N., Nilmini, S. L. I., Stolic, P., Vasiljevic, T., & Shah, N. P. (2007). Survival
and activity of selected probiotic organisms in set-type yoghurt during cold
storage. International Dairy Journal, 17(6), 657–665.
Fuller, R. (1989). Probiotics in man and animals. Journal of Applied Bacteriology,
66(5), 365–378.
Gardiner, G. E., Bouchier, P., O’Sullivan, E., Kelly, J., Kevin Collins, J., Fitzgerald, G.,
et al. (2002). A spray-dried culture for probiotic Cheddar cheese manufacture.
International Dairy Journal, 12(9), 749–756.
Gibson, G. R., Probert, H. M., Rastall, R. A., & Roberfroid, M. B. (2004). Dietary
modulation of the human colonic microbiota: Updating the concept of
prebiotics. Nutrition Research Reviews, 17, 259–275.
Gibson, G. R., Rastall, R. A., & Fuller, R. (2003). The Health Benefits of Probiotics and
Prebiotics. In R. Fuller & G. Perdigon (Eds.), Gut flora, nutrition, immunity and
health (1st ed., pp. 52–76). Oxford: Blackwell Publishing.
Gilliland, S. E. (1990). Health and nutritional benefits from lactic acid bacteria. FEMS
Microbiology Letters, 87(1–2), 175–188.
Güler-AkIn, M. B., & AkIn, M. S. (2007). Effects of cysteine and different incubation
temperatures on the microflora, chemical composition and sensory
characteristics of bio-yogurt made from goat’s milk. Food Chemistry, 100(2),
788–793.
 R.D.C.S. Ranadheera et al. / Food Research International 43 (2010) 1–7
Heenan, C. N., Adams, M. C., Hosken, R. W., & Fleet, G. H. (2004). Survival and
sensory acceptability of probiotic microorganisms in a nonfermented frozen
vegetarian dessert. Lebensmittel-Wissenschaft und-Technologie, 37(4), 461–466.
Hekmat, S., Soltani, H., & Reid, G. (2009). Growth and survival of Lactobacillus reuteri
RC-14 and Lactobacillus rhamnosus GR-1 in yogurt for use as functional food.
Innovative Food Science and Emerging Technologies, 10, 293–296.
Helland, M. H., Wicklund, T., & Narvhus, J. A. (2004). Growth and metabolism of
selected strains of probiotic bacteria in milk- and water-based cereal puddings.
International Dairy Journal, 14(11), 957–965.
Ho, P. H., Adams, M. C., & Le, T. M. (2007). The effect of spray drying on the probiotic
efficacy of a Lactobacillus sp. In Paper presented at the XXX international
congress on microbial ecology and disease (SOMED).
Huang, Y., & Adams, M. C. (2004). In vitro assessment of the upper gastrointestinal
tolerance of potential probiotic dairy propionibacteria. International Journal of
Food Microbiology, 91(3), 253–260.
Huang, Y., Kotula, L., & Adams, M. C. (2003). The in vivo assessment of safety and
gastrointestinal survival of an orally administered novel probiotic,
Propionibacterium jensenii 702, in a male Wister rat model. Food and Chemical
Toxicology, 41(12), 1781–1787.
Kailasapathy, K., & Chin, J. (2000). Survival and therapeutic potential of probiotic
organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp.
Immunology & Cell Biology, 78(1), 80–88.
Kailasapathy, K., Harmstorf, I., & Phillips, M. (2008). Survival of Lactobacillus
acidophilus and Bifidobacterium animalis ssp. Lactis in stirred fruit yogurts. LWT-
Food Science and Technology, 41(7), 1317–1322.
Kebary, K. M. K. (1996). Viability of Bifidobacterium bifidum and its effect on quality
of frozen Zabady. Food Research International, 29(5–6), 431–437.
Kim, H. S., & Gilliland, S. (1983). Lactobacillus acidophilus as a dietary adjunct for
milk to aid lactose digestion in humans. Journal of Dairy Science, 66, 959–966.
Kopp-Hoolihan, L. (2001). Prophylactic and therapeutic uses of probiotics: A review.
Journal of the American Dietetic Association, 101(2), 229–241.
Lavermicocca, P. (2006). Highlights on new food research. Digestive and Liver
Disease, 38(Suppl. 2), S295–S299.
Lavermicocca, P., Valerio, F., Lonigro, S. L., De Angelis, M., Morelli, L., Callegari, M. L.,
et al. (2005). Study of adhesion and survival of Lactobacilli and Bifidobacteria on
table olives with the aim of formulating a new probiotic food. Applied and
Environmental Microbiology, 71(8), 4233–4240.
Lourens-Hattingh, A., & Viljoen, B. C. (2001). Yogurt as probiotic carrier food.
International Dairy Journal, 11(1–2), 1–17.
Martin-Diana, A. B., Janer, C., Pelaez, C., & Requena, T. (2003). Development of a
fermented goat’s milk containing probiotic bacteria. International Dairy Journal,
13(10), 827–833.
McMaster, L. D., Kokott, S. A., Reid, S. J., & Abratt, V. R. (2005). Use of traditional
African fermented beverages as delivery vehicles for Bifidobacterium lactis DSM
10140. International Journal of Food Microbiology, 102(2), 231–237.
Michida, H., Tamalampudi, S., Pandiella, S. S., Webb, C., Fukuda, H., & Kondo, A.
(2006). Effect of cereal extracts and cereal fiber on viability of Lactobacillus
plantarum under gastrointestinal tract conditions. Biochemical Engineering
Journal, 28(1), 73–78.
Nobaek, S., Johansson, M.-. L., Molin, G., Ahrne, S., & Jeppsson, B. (2000). Alteration of
intestinal microflora is associated with reduction in abdominal bloating and
pain in patients with irritable bowel syndrome. The American Journal of
Gastroenterology, 95(5), 1231–1238.
Oliveira, R. P. S., Florence, A. C. R., Silva, R. C., Perego, P., Converti, A., Gioielli, L. A.,
et al. (2009). Effects of different prebiotics on the fermentation kinetics,
probiotic survival and fatty acids profiles in nonfat symbiotic fermented milk.
International Journal of Food Microbiology, 128, 467–472.
Oliveira, M. N., Sodini, I., Remeuf, F., & Corrieu, G. (2001). Effect of milk
supplementation and culture composition on acidification, textural properties
and microbiological stability of fermented milks containing probiotic bacteria.
International Dairy Journal, 11(11–12), 935–942.
Ong, L., & Shah, N. P. (2009). Probiotic Cheddar cheese: Influence of ripening
temperatures on survival of probiotic microorganisms, cheese composition and
organic acid profiles. LWT-Food Science and Technology, 42, 1260–1268.
Ouwehand, A. C., Kirjavainen, P. V., Shortt, C., & Salminen, S. (1999). Probiotics:
Mechanisms and established effects. International Dairy Journal, 9(1), 43–52.
Patel, H. M., Pandiella, S. S., Wang, R. H., & Webb, C. (2004). Influence of malt, wheat,
and barley extracts on the bile tolerance of selected strains of lactobacilli. Food
Microbiology, 21(1), 83–89.
7
Penner, R., Fedorak, R. N., & Madsen, K. L. (2005). Probiotics and nutraceuticals:
Non-medicinal treatments of gastrointestinal diseases. Current Opinion in
Pharmacology, 5(6), 596–603.
Rakin, M., Vukasinovic, M., Siler-Marinkovic, S., & Maksimovic, M. (2007).
Contribution of lactic acid fermentation to improved nutritive quality
vegetable juices enriched with brewer’s yeast autolysate. Food Chemistry,
100(2), 599–602.
Ranadheera, R. D. C. S., Ho, P. H., Luo, J., & Adams, M. C. (2007). Does the food
substrate influence the functionality of probiotics? Asia Pacific Journal of Clinical
Nutrition, 16(Suppl. 3), S81.
Rasic, J. L. (2003). Microflora of the intestine probiotics. In B. Caballero, L. Trugo, & P.
Finglas (Eds.), Encyclopedia of food sciences and nutrition (pp. 3911–3916).
Oxford: Academic Press.
Ravula, R. R., & Shah, N. P. (1998a). Effect of acid casein hydrolysate and cysteine on
the viability of yogurt and probiotic bacteria in fermented frozen dairy desserts.
Australian Journal of Dairy Technology, 53(3), 175–179.
Ravula, R. R., & Shah, N. P. (1998b). Selective enumeration of Lactobacillus casei from
yogurts and fermented milk. Biotechnology Techniques, 12(11), 819–822.
Ravula, R. R., & Shah, N. P. (2003). Microencapsulation of probiotic bacteria and their
survival in frozen fermented dairy desserts. Australian Journal of Dairy
Technology, 55(3), 139–143.
Reddy, G., Altaf, M., Naveena, B. J., Venkateshwar, M., & Kumar, E. V. (2007).
Amylolytic bacterial lactic acid fermentation – A review. Biotechnology
Advances, 26(1), 22–34.
Ross, R. P., Fitzgerald, G. F., Collins, J. K., & Stanton, C. (2002). Cheese delivering
biocultures-probiotic cheese. The Australian Journal of Dairy Technology, 57(2),
71–78.
Saarela, M., Lahteenmaki, L., Crittenden, R., Salminen, S., & Mattila-Sandholm, T.
(2002). Gut bacteria and health foods-the European perspective. International
Journal of Food Microbiology, 78(1–2), 99–117.
Saarela, M., Virkajarvi, I., Alakomi, H.-L., Sigvart-Mattila, P., & Matto, J. (2006).
Stability and functionality of freeze-dried probiotic Bifidobacterium cells during
storage in juice and milk. International Dairy Journal, 16(12), 1477–1482.
Sanders, M. A. (1998). Overview of functional foods: Emphasis on probiotic bacteria.
International Dairy Journal, 8, 341–347.
Senok, A. C., Ismaeel, A. Y., & Botta, G. A. (2005). Probiotics: Facts and myths. Clinical
Microbiology & Infection, 11(12), 958–966.
Shah, N. P. (2007). Functional cultures and health benifits. International Dairy
Journal.
Shah, N. P., Lankaputhra, W. E. V., Britz, M. L., & Kyle, W. S. A. (1995). Survival of
Lactobacillus acidophilus and Bifidobacterium bifidum in Commercial Yoghurt
During Refrigerated Storage. International Dairy Journal, 5, 515–521.
Shimakava, Y., Matsubara, S., Yuki, N., Ikeda, M., & Ishikawa, F. (2003). Evaluation of
Bifidobacterium breve strain Yakult-fermented soymilk as a probiotic food.
International Journal of Food Microbiology, 81(2), 131–136.
Sugano, M., Goto, S., Yamada, Y., Yashida, K., Hashimoto, Y., Matsuo, T., et al. (1990).
Cholesterol-lowering activity of various undigested fractions of soybean protein
in rats. Journal of Nutrition, 120, 977–985.
Tharmaraj, N., & Shah, N. P. (2004). Survival of Lactobacillus acidophilus, Lactobacillus
paracasei subsp. Paracasei, Lactobacillus rhamnosus, Bifidobacterium animalis and
Propionibacterium in cheese-based dips and the suitability of dips as effective
carriers of probiotic bacteria. International Dairy Journal, 14(12), 1055–1066.
Valerio, F., De Bellis, P., Lonigro, S. L., Morelli, L., Visconti, A., & Lavermicocca, P.
(2006). In vitro and in vivo survival and transit tolerance of potentially probiotic
strains carried by artichokes in the gastrointestinal tract. Applied and
Environmental Microbiology, 72, 3042–3045.
Venturi, A., Gionchetti, P., Rizzello, F., Johansson, R., Zucconi, E., Brigidi, P., et al.
(1999). Impact on the composition of the faecal flora by a new probiotic
preparation: preliminary data on maintenance treatment of patients with
ulcerative colitis. Alimentary Pharmacology Therapeutics, 13(8).
Vinderola, C. G., Bailo, N., & Reinheimer, J. A. (2000). Survival of probiotic microflora
in Argentinian yoghurts during refrigerated storage. Food Research International,
33(2), 97–102.
Vinderola, C. G., & Reinheimer, J. A. (2000). Enumeration of Lactobacillus casei in the
presence of L. Acidophilus, bifidobacteria and lactic stater bacteria in fermented
dairy products. International Dairy Journal, 10(4), 271–275.
Yoon, K. Y., Woodams, E. E., & Hang, Y. D. (2006). Production of probiotic cabbage
juice by lactic acid bacteria. Bioresource Technology, 97(12), 1427–1430.