Author’s Accepted Manuscript

The potential applications of probiotics on dairy

and non-dairy foods focusing on viability during
storage

Amal Bakr Shori

www.elsevier.com/locate/bab

PII: S1878-8181(15)00130-9
DOI: http://dx.doi.org/10.1016/j.bcab.2015.09.010
Reference: BCAB309
To appear in: Biocatalysis and Agricultural Biotechnology
Received date: 24 April 2015
Revised date: 20 July 2015
Accepted date: 21 September 2015
Cite this article as: Amal Bakr Shori, The potential applications of probiotics on
dairy and non-dairy foods focusing on viability during storage, Biocatalysis and
Agricultural Biotechnology, http://dx.doi.org/10.1016/j.bcab.2015.09.010
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The potential applications of probiotics on dairy and non-dairy foods focusing on
viability during storage

Shori, Amal Bakr

King Abdulaziz University, Faculty of Science, Department of Biological Sciences,

Jeddah 21589, Saudi Arabia

Abstract

Probiotic foods products are a fast growing area of functional food, as found to be
strongly accepted by the consumers. The application of probiotics in dairy products is
already common. However, the food industry is seeking to produce different varieties
of probiotic foods other than dairy products with potential health benefits. The
success of new probiotic foods depend on the ability of probiotics to provide
sufficient numbers of viable cells that beneficially modify the gut microflora of the
host. It is highly desirable that the viable counts of probiotics in the final product to be
at least 106–107 cfu ml-1 to offering health benefits to the consumers Therefore, the
objective of this study is to review the applications of selected probiotics in dairy and
non- dairy foods and their viability during the storage.

Keywords: Probiotics, dairy products, non-dairy products, probiotics viability.

1
1. Introduction

Foods are not only to satisfy hunger and to deliver essential nutrients but also to
prevent the development of nutrition-related diseases and to improve physical and
mental well-being of consumers (Stanton et al., 2005; Arihara, 2006). This leads to
the development of novel food for special health use that named functional food.
Probiotic foods are the fastest growing area of functional food development. Probiotic
cultures are successfully applied in different types of food matrices. A number of food
products including dairy products (Vinderola et al., 2002; Buriti et al., 2005a, 2005b;
Sheehan et al., 2007), meats products (Klingberg et al., 2005; Sidira et al., 2014b;
Rubio et al., 2014), beverages products (Buriti et al., 2007; Espírito Santo et al., 2012;
Vinderola et al., 2002), cereals products (Kedia et al., 2007; Rozada-Sanchez et al.,
2008), vegetables and fruits products (Tsen et al., 2004; Kim et al., 2010; Blaiotta et
al., 2012; Sarvan et al., 2013) and bread products (Palacios et al., 2006) have been
utilized as delivery vehicles for probiotics. In general, the selection strain of lactic
acid bacteria is important to ensure health benefits of probiotic foods. A number of
health benefits associated with probiotic food products include treatment of diarrhea
(Reid et al., 2003), alleviation of symptoms of lactose intolerance (De Vrese et al.,
2001), reduction of blood cholesterol (Jackson et al., 2002), anti-carcinogenic
properties (Wollowski et al., 2001; Rafter, 2003) and improvement in immunity (Reid
et al., 2003; Broussard et al., 2004). Many factors may affect the viability of probiotic
bacteria in foods including the probiotic strains used, pH, the presence of hydrogen
peroxide and dissolved oxygen, the concentration of metabolites such as lactic and
acetic acids, the medium buffering capacity, storage temperature, the nature of the
added ingredients and food matrices (Donkor et al., 2006; Pereira et al., 2011;
Fonteles et al., 2011; Costa, et al., 2013). Viability and metabolic activity of the
bacteria are important features of probiotics inclusion in food during manufacture thus
the choice of appropriate probiotic strains will be essential. Probiotic foods must
maintain survival of the probiotic strain at suitable levels ranging from 106 to 107 cfu
ml-1 at the time of consumption (Madureira et al., 2011) to offering health benefits to
the consumers. Therefore, the object of this study is to review the applications of
selected probiotics in dairy foods (yogurt and cheese) and non- dairy foods (desserts,
cereals, fruits, vegetables and meats products) and their viability during storage.

2
2. Dairy probiotics products

Dairy products are established as healthy natural products (Ramchandran and Shah,
2009). Regular consumption of certain dairy products has beneficial effects in the
prevention of disease (Bozanic et al., 2001). Lactic acid bacteria (LAB) and their
metabolites play a key role in enhancing microbiological quality and shelf life of
fermented dairy products (Lourens-Hattingh and Viljoen, 2001; Leroy and De Vuyst,
2004). LAB has an essential role in most fermented foods for their ability to produce
various antimicrobial compounds promoting probiotic properties (Temmerman et al.,
2002). A number of dairy food products including yogurt (Kailasapathy and Rybka,
1997) and cheese (Stanton, 2001) have been utilized as delivery vehicles for probiotic
to consumer.

2.1 Yogurt

Yogurt is fermented milk obtained by lactic acid bacteria fermentation of milk and is
a popular product throughout the world. Probiotics mainly Lactobacillus acidophilus
and Bifidobacterium spp. are added to improve the fermentation process for
production probiotic yogurt (Donkor et al., 2006). The key problems associated with
incorporating probiotic bacteria into milk during fermentation are slow growth in milk
and low survival rate during storage (El-Dieb et al. 2012). One of the strategies
applied to improve the growth of probiotic bacteria is the addition of prebiotic
substances with proper selection of starter cultures (El-Dieb et al. 2012; Oliveira et al.
2012). In order to provide functional properties and increase the growth and viability
of probiotic bacteria in yogurt many other supplements with active components have
been studied such as plant extracts, milk proteins, inulin and lactulose as prebiotic
substances (Table 1).

2.1.1 Probiotics viability of yogurt in the presence of fruits

It is important to emphasise that the addition of fruit juices or pulps might be

deleterious to the viability of some species and strains of probiotics in food products,
particularly as a result of acidity and the presence of antimicrobial compounds
(Vinderola et al., 2002). Several studies have demonstrated the effect of plant
compounds on the growth and metabolism of probiotics in yogurt (Lahtinen et al.,

3
2007; Possemiers et al., 2010; Ranadheera et al., 2012). Previous study detected that
yogurt enriched with flavouring agents such as strawberry, vanilla, peach and banana
essences did not affect the growth of the probiotic bacteria (Table 1) in the optimum
concentrations commonly used in dairy industry (Vinderola et al., 2002). Similarly,
the presence of mango and guava pulps and their natural essences did not affect the
growth of probiotic and starter bacteria in yogurt (Bedani et al., 2014). Another study
conducted by Ranadheera et al. (2012) found that the viability of probiotic (Table 1)
decreased in stirred fruit yogurt made from goat’s milk through 4 weeks of storage.
However, the viability of both B. animalis Bb-12 and Propionibacterium jensenii 702
is still higher (~107 cfu g-1 and ~108 cfu g-1 respectively) than L. acidophilus La-5 (>
105 cfu g-1) by the end of 4 weeks storage. On the other hand, Kailasapathy et al.
(2008) reported a significant increase of L. acidophilus counts (>107 cfu g-1) in stirred
fruit yogurt during 5 weeks of storage. The difference in L. acidophilus counts could
occur because the starter culture used which consists only of S. thermophilus without
any L. delbrueckii subsp. bulgaricus. Since the latter have reported to produce
hydrogen peroxide in yogurt that cause a limitation of L. acidophilus growth (Dave
and Shah, 1997). Espírito Santo et al. (2010) Found a complex relationship between
probiotic strains and açai pulp in yogurt related to high level of polyunsaturated fatty
acids and conjugated linoleic acid in açai pulp which enhanced the survival of L.
acidophilus L10 (7.6 log cfu g-1) and B. lactis Bl04 (9.4 log cfu g-1) in yogurt during
28 days of storage at 4°C. High nutritional value in dates (carbohydrates, salts,
minerals, dietary fiber, vitamins, fatty acids, amino acids and protein) reported to
increase the viability of B. bifidum (7.10 log cfu g-1) in biogarde yogurt enriched with
2% of date syrup (dibs) compared to plain yogurt (6.81 log cfu g-1) during 10 days of
storage (El-Nagga and Abd El–Tawab, 2012).
2.1.2 Probiotics Viability of yogurt in the presence of milk proteins

Milk proteins are cheaper and readily available additive that used to increase the
growth and viability of probiotics during milk fermentation (Bozanic et al., 2001;
Martìn-Diana et al., 2003; Marafon et al., 2011). Martìn-Diana et al. (2003) reported
that fermented goat milk supplemented with 3% and 5% of whey protein concentrate
(WPC) significantly (p<0.05) increased the population of S. thermophilus ST-20Y by
almost 2 folds higher (9.9±1.7 x108 cfu g-1 and 11.2±4.0 x108 cfu g-1 respectively)

4
than control (5.2±2.9 x108 cfu g-1; 0% WPC). In addition, the viability of
Bifidobacterium Bb-12 was significantly enhanced by WPC after fermentation and
even after 21 days refrigerated storage whereas L. acidophilus LA-5 did not influence
by WPC (Martìn-Diana et al., 2003). On the other hand Marafon et al. (2011) reported
no significant differences in the viability of S. thermophilus and B. animalis subsp.
Lactis B94 LAFTI in the presence of milk proteins such as skimmed milk powder,
WPC and sodium caseinate. The differences could be related to bacterial species and
strain. Michael et al. (2010) found that yogurt supplemented with 0.014% and 0.028%
L-cysteine (Cys) maintained higher viability of L. bulgaricus (>6 log cfu g-1) than non
Cys-supplemented yogurt during 50 days of storage.

2.1.3 Probiotics viability of yogurt in the presence of cereals

Cereals contain carbohydrates, proteins, minerals and vitamins that may provide
micronutrients for probiotics and yogurt starter cultures growth. Soy-based products
showed ability to stimulate S. thermophilus growth because of soy oligosaccharides
that can metabolised by this bacteria (Farnworth et al., 2007; Donkor et al., 2007;
Bedani et al., 2014). Zarea et al. (2012) reported that cereal ingredients such as soy
and lentil flours increased the lactobacilli fraction in the yogurt. Likewise, Agil et al.
(2013) demonstrated that green lentils improved the counts of probiotic bacteria in
yogurt after fermentation and maintained high viability over a period of 28 days. The
effect of buckwheat flour and oat bran as prebiotics on the production of probiotic
fiber-enriched fermented milk has been investigated by Coman et al. (2013).
Buckwheat flour and oat bran supplemented fermented milk found to increase the
acidifying ability of the lactobacilli (Table 1) during storage. Coda et al. (2012) used
two selected strains of L. plantarum (6E and M6) to manufacture vegetable yogurt-
like beverages (VYLB). Five VYLB were manufactured including rice (RYLB), rice
and soy (RSYLB), rice and barley (RBYLB), rice and emmer (REYLB) and rice and
oat (ROYLB) yogurt-like beverages. Both selected strains inoculated at 7 log cfu g-1
showed high viability of cell densities (8 log cfu g-1) with pH lower than 4 in all
VYLB during 30 days of storage.

5
2.1.4 Probiotics viability of yogurt in the presence of inulin and lactulose

Inulin has shown to apply a protective action on lactic acid bacteria by interesting
their viability and activity during fermentation and storage (Donkor et al., 2007). This
observation was confirmed by Oliveira et al. (2011b) who found that inulin (40 mg/g)
stimulated the growth of B. lactis in fermented skim milk which increased
dramatically (p<0.05) from 7.5 to 9.1 log cfu ml-1 during 7 days storage at 4 °C. In
addition, the presence of inulin in fermented skim milk with probiotic cocktails of L.
rhamnosus, L. bulgaricus and B. lactis improved the counts of these strains compared
to the absence during two weeks storage. Furthermore, inulin enhanced biomass
growth of both S. thermophilus and L. rhamnosus during milk fermentation and
increased the levels of metabolic end-products such as lactic acid (26.1%), acetic acid
(33.5%) and ethanol (241%; Oliveira et al., 2011b).

Lactulose is a synthetic disaccharide obtained by isomerization of lactose that

already present in milk and whey in almost 4.5% as an average (Zokaee et al., 2002).
It can be considered as a prebiotic because its ability to stimulate healthy intestinal
microflora. Oliveira et al. (2011a) reported that lactulose has important effect on B.
lactis in fermented milk associated with high growth (7.41 log cfu ml-1 to 10.3 log cfu
ml-1) during fermentation. In addition, lactulose maintained high viability of B. lactis
even after 35 days of storage. This observation is in agreement with Ozer et al. (2005)
who demonstrated the potential of lactulose as a prebiotic due to fast hydrolysis to
galactose and fructose.

2.2 Cheese

Cheese is one of the best carriers for probiotics. Probiotic bacteria can be included
into cheese during manufacture in two ways either as a starter (depended on the
ability to produce adequate lactic acid in milk) or as adjunct to the starter culture
which is more favourable option to incorporate probiotic with the starter bacteria
during cheese making. A few approaches have been applied to improve the survival of
probiotic in cheeses one of them is the use of different combination of starter and
probiotic (Ong and Shah, 2008). The development of probiotic cheeses can be very
strain dependent as many of the probiotic strains showed poor performance in the
cheese environment. Strain selection plays a key role in successful development of
6
probiotic cheese. In addition, processing conditions, cooking procedure, the aerobic
environment, temperatures of ripening and storage are affecting the viability of
probiotic bacteria a well as the concentration of these bacteria in the final product
(Ong and Shah, 2008). Several studies have reported the applications of probiotic
bacteria in Minas fresh cheese, Turkish cheese and Cheddar cheese (Table 2).

2.2.1 Viability of probiotics in Minas cheese

Minas cheese is a traditional Brazilian fresh cheese which the pH above 5.0. It has
high water activity and low salt content besides content no preservatives. Thus, it
offers a good option for growth and survival of probiotic strains in order to improve
the health benefits and quality of the final product. Buriti et al. (2005a) indicated
possible interaction between L. paracasei and Lactococcus spp. associated with a
good performance of L. paracasei (7.50 - 8.15 log cfu g-1) in Minas fresh cheese
during 2 weeks of refrigerated storage. Another study found that, the inculcation of L.
acidophilus La-5 alone or with co-culture (mesophilic type O lactic culture) in Minas
fresh cheese during production showed high viability of L. acidophilus La-5 (above
106 cfu g-1) during 21 days of storage (Buriti et al., 2005b). Both L. acidophilus La-5
and B. animalis Bb-12 added to Minas fresh cheese during manufacture showed level
of viable cell counts of 106 cfu g-1 during 21 days of storage (Buriti et al., 2007). The
production of Minas fresh cheese inoculated with the probiotic strain of L.
acidophilus La-5 with S. thermophilus increased the viability of L. acidophilus to
reach 107 cfu g-1 during 2 weeks of storage (Souza and Saad, 2009). The viability of
lactobacilli (Table 2) and B. animalis subsp. lactis (Bl) in co-culture with S.
thermophilus (St) were examined in Minas frescal cheese whey (Almeida et al.,
2008). Based on the results, B1 showed the highest counts (~ 8.43 log cfu g-1) when
combined with St whereas Lr showed the lowest counts (~5.59 log cfu g-1). The viable
cell counts of La and Lb in Minas frescal cheese whey were 6.72 log cfu g-1 and 7.26
log cfu g-1 respectively. This indicated that B1 and Lb had the highest interaction with
St in Minas frescal cheese whey (Almeida et al., 2008). Fritzen-Freire et al. (2010)
reported that the viability of Bifidobacterium (Bb-12) in Minas Frescal cheese does
not influence by the presence of lactic acid. They observed no significant difference in
the cell counts of Bb-12 in samples produced with addition of Bb-12 only and
samples prepared through direct acidification with lactic acid and addition of Bb-12.
7
2.2.2 Viability of probiotics in Turkish cheese

Several types of Turkish cheeses have found strongly suitable for the delivery of
probiotics to consumers (Hayaloglu et al., 2004; Öner et al., 2006; Kil‎iç et al., 2009).
The survival of L. acidophilus in Turkish white cheese during 90 days of storage was
studied by Kasımoğlu et al. (2004). The viable cell counts of L. acidophilus reached
to the highest level (1010 cfu g-1) on day 7 of storage before reduced significantly to
107 cfu g-1 by the end of storage. Yet, this Turkish white cheese still maintained the
recommended level of probiotic in cheeses ≥ 107 cfu g-1 overall storage period (Hoier
et al., 1999). Kil‎iç et al. (2009) investigated the survival of the probiotic strains during
production of Turkish Beyaz cheese. Turkish Beyaz cheeses were produced in three
batches: the first batch with the test probiotic culture mix (P) including L. fermentum
(AB5-18 and AK4-120) and L. plantarum (AB16-65 and AC18-82), second batch
with a commercial starter culture mix (C) including Lactoccocus lactis subsp.
Cremoris and Lactococcus lactis subsp. lactis and the third batch with equal parts of
the commercial starter culture mix and test probiotic culture mix (CP). The results
indicate that the viability of LAB in C cheese were 108 cfu g-1 up to 30 days.
However, the number of lactobacilli and lactococci in P and CP cheeses remained at a
constant level of 108 cfu g-1 for 3 months.

2.2.3 Viability of probiotics in Cheddar cheese

Cheddar cheese is a good alternative for delivery of probiotics gut and consequently
has been subjected to numerous studies in recent years (Brearty et al., 2001; Ong and
Shah, 2009; Fortin et al., 2011; Amine et al., 2014). Brearty et al. (2001) reported that
B. lactis Bb-12 can survive in high level of cheddar cheese (≥108 cfu g-1) compared to
B. longum BB536 (105 cfu g-1) during six months of ripening. However, the increase
of B. lactis Bb-12 was associated with 40% increase in moisture level which
considered slightly above the legal limit permitted for Cheddar cheese (Brearty et al.,
2001). Another study found that, B. longum 15708 showed slow growths in salted
cheddar cheese which lost about 13% of their viable cells in whey during manufacture
and 3 log cfu g-1 of viability have been decreased after 3 days of storage (Fortin et al.,
2011). Thus, the authors suggested using microencapsulation technique to improve
bacterial survival during the process and storage. Indeed, Amine et al. (2014)

8
evaluated the effect of microencapsulation (ME) in alginate beads on the viability of
B. longum 15708 in cheddar cheese during storage. Two ME methods were used,
droplet extrusion method (ADE) and emulsion method with two polymers, native
alginate (NA) and palmitoylated alginate (PA). Based on the results cheese prepared
with emulsified PA and NA beads showed higher viability of B. longum with only 2
log cfu g-1 reduction compared to 3 and 4 log cfu g-1 reduction for ADE formulation
and free cells respectively after 21 days of storage (Amine et al., 2014). The authors
associated that with the protection effect of the lipid content in alginate and/or
residual oil from the emulsion process toward probiotic bacteria. Moreover, despite B.
longum encapsulated in the PA emulsion showed the highest viability (<106 cfu g-1)
over 21 days of storage, it still below the minimum level (≥ 6 log10 cfu g-1)
recommended for a probiotic products to exert health benefits (Lourens-Hattingh and
Viljoen, 2001). Previous studies found that probiotic adjuncts (Table 2) remained at
the level of 8 log cfu g-1 - 9 log cfu g-1 in cheddar cheeses made with mixture of
starter culture lactococci during 24 weeks of storage at 4°C (Ong et al., 2006; Ong
and Shah, 2009). An elevated ripening temperature to 8 °C did not affect the viability
of probiotics however reduced significantly (p<0.05) the viability of starter lactococci
in cheese batches inoculated with B. animalis B94, L. casei L26 or L. acidophilus
(Ong and Shah, 2009). Similar study was conducted by Phillips et al. (2006) to
determine the viability of probiotics (Table 2) in cheddar cheese during maturation
over 32 weeks. All the three strains of Bifidobacterium showed amount of viable cells
about 4×107 cfu g-1, 1.4×108 cfu g-1 and 5×108 cfu g-1 for B94, Bb12 and DR10
respectively during 32 weeks. However, the two L. acidophilus strains tested
displayed a different trend of survival in cheddar cheese as compared to
Bifidobacterium strains. Although the viability of L. acidophilus strains increased and
reached a maximum population (107 cfu g-1) during 12 weeks however the viable cell
numbers of these strains declined around 4.9×103 cfu g-1 and 3.6×103 cfu g-1 for L10
and La5 respectively during 32 weeks (Phillips et al. 2006). Lactobacillus strains
showed survival patterns comparable to that in Bifidobacterium spp. with viability
ranged between 107 cfu g-1 (for Lc1 and L26) and 108 cfu g-1 (for DR20) during 32
weeks of ripening.

9
3. Non- dairy probiotic products

Probiotics dairy products were shown to be very promising features for a functional
food, since they exhibited excellent conditions for maintaining the viability of
probiotic bacteria (Buriti et al., 2007; Souza and Saad, 2009; El-Dieb et al. 2012).
However, since the increasing number of people with problems of allergic to milk
proteins, high cholesterol levels and lactose intolerance who cannot consume dairy
products besides the increase desire for vegetarian substitutes (Farnworth et al., 2007),
dairy free products can be used as an alternative for delivery of probiotics. Several
non-dairy products such as dessert products, cereals products, fruits and vegetables
products and meat products have successfully used as carriers for the delivery of
probiotics to the human (Table 3).
3.1 Viability of probiotics in desserts products

Dessert foods have shown a great market potential. As a consumer interest in lighter
and healthier dessert products (Aragon-Alegro et al., 2007), probiotic bacterial strains
are successfully used in the production of dessert foods (Heenan et al., 2004;
Possemiers et al., 2010). Chocolate mousse is shown to be an effective vehicle for the
incorporation of L. paracasei subsp. paracasei LBC 82 (Aragon-Alegro et al., 2007).
The neutral pH values of probiotic chocolate mousse (pH 6.3 - 5.7) represent an
appropriate condition for L. paracasei survival during 28 days of storage at 4°C. The
authors concluded that the good stability of viable counts of L. paracasei (above 7 log
cfu g-1) in chocolate mousse during the entire storage period may have beneficial
effects on the consumer’s health. Moreover, the addition of prebiotic ingredient such
as inulin does not affect the viability of L. paracasei during the storage (Aragon-
Alegro et al., 2007). Previous study has demonstrated potential protective effect of
chocolate as a suitable product for oral delivery of microencapsulated mixture of
probiotics (Table 3) with high survival rate in acidic conditions (Possemiers et al.,
2010). The incorporation of probiotic microorganisms (Table 3) into a non-fermented
vegetarian frozen soy dessert was studied by Heenan et al. (2004). This study
indicated that the freezing and churning process had significant effect on the viability
of L. rhamnosus 100-C and S. boulardii 74012. However, all Lactobacillus and
Bifidobacterium species showed initial populations of 107–108 cfu g-1 in frozen soy
dessert (pH 7.0) whereas the yeast S. boulardii 74012 showed viability around 106 cfu
10
g-1 (Heenan et al., 2004). All probiotics species retain sufficient viability of 107 cfu g-1
after 28 weeks of storage at -20°C except S. boulardii 74012 that decreased
significantly below 106 cfu g-1. A wider surface area of the yeast cell than bacterial
cell and the lack of ‘cell shielding’ (Bozoglu et al., 1987) may cause the decrease in
viability of S. boulardii 74012. Heenan et al. (2004) found that the presence of S.
boulardii in frozen soy dessert generated unfavourable flavours for the consumers.
Fermented acerola (Malpighia emarginata) ice cream has demonstrated a good carrier
of probiotic bacteria, since B. longum and B. lactis remained viable (above 106 cfu g-
1
) over 14 days of storage (Favaro-Trindade et al., 2006). Another study indicated
that, B. lactis and L. paracasei inoculated as single or combined cultures in the
coconut flan remained above 107 cfu g-1 during 28 days storage at 5°C (Correa et al.,
2008). Previously, it has innovated new probiotic product based on liquid maple sap
or its concentrate (Khalf et al., 2010). This product is potentially useful as vehicle for
the delivery of viable B. lactis Bb12 and L. rhamnosus GG, because both probiotic
strains have high viable cell counts (7 log10 cfu g-1) during 28 days of storage at 4°C
(Khalf et al., 2010).

3.2 Viability of probiotics in cereals-based products

Cereal grains are rich sources of protein, carbohydrates, vitamins, minerals and fiber
(Chavan and Kadam, 1989). It also consists of non-digestible carbohydrates that have
beneficial physiologic effects in humans such as stimulation the growth of
Lactobacilli and Bifidobacteria present in the colon (Andersson et al., 2001). Many
studies have demonstrated that cereals are good substrates for probiotic bacteria
growth (Mårtenson et al., 2002; Angelov et al., 2006; Trachoo et al., 2006; Kedia et
al., 2007). Mantzouridou et al. (2013) Concluded that salad dressing emulsion based
on different level of oat flour (1.0, 3.0, and 5.0 g/ 100g) can significantly ensure
viability of L. paracasei subsp. paracasei DC412 ranging between 2.0 x 107 cfu g-1
and 5.6 x 107 cfu g-1 during 7 weeks storage at 4°C and maintain pH values (3.58 -
3.69) close to that recommended for the commercial salad dressing products
(Mantzouridou et al., 2013). However, despite salad dressing emulsion based on
inulin at level of 1.0, 3.0, and 5.0 g/ 100g showed higher viability of L. paracasei
DC412 (4.7 x 108 cfu g-1 - 7.7 x 108 cfu g-1) during 7 weeks storage, it has showed
lower pH values (3.05-3.08) than that recommended for the commercial salad

11
dressing products (Mantzouridou et al., 2013). Zubaidah et al. (2012) have reported
that both L. casei and L. plantarum B2 can grow effectively in fermented rice bran
with viable cell counts of 1.07x109 cfu g-1 and 1.25x109 cfu g-1 respectively after 12
hours fermentation. Another study demonstrated that barley, wheat and malt extracts
supported well the growth of L. plantarum and its survival in the fermented product
during refrigerated storage (Charalampopoulos and Pandiella, 2010). The viable cell
counts in all fresh cereals extracts (pH 2.9-3.4) ranging between 9.5 and 10.3 log cfu
g-1 after 24 hours fermentation. Higher sugar and lactic acid concentrations in malt
extract supported significantly (p<0.05) better L. plantarum growth than wheat and
barley extracts (Charalampopoulos and Pandiella, 2010). Furthermore, higher residual
sugar present in fermented malt extracts resulted in the best survival of L. plantarum
compared to barley and wheat extracts over 70 days of storage at 4°C. Similarly,
Kedia et al. (2007) investigated the production of a new cereal-based probiotic food.
The author indicated that fresh L. reuteri isolated from human intestine can grow well
in 5% malt suspension. The viable cell counts of L. reuteri at the end of fermentation
(12 hours) increased from log 6.35 cfu g-1 to log 8.41 cfu g-1 and caused a decrease in
broth pH, which dropped from 5.0 to 3.5 (Kedia et al., 2007). Helland et al. (2004)
reported that maize porridge prepared using maize flour and barley malt is a suitable
product for the delivery of probiotics (Table 3) which exhibit high viability of these
probiotics (7.2–8.2 log cfu g-1; pH below 4.0) after fermentation for 12 hours at 37 °C.
Earlier study found that the addition of inulin (3 g/100 ml) and/or okara flour (5 g/100
ml) in fermented soymilk product produced from soymilk fermented with ABT-4
culture (Table 3) did not influence the viability of L. acidophilus and B. animalis
during 28 days of storage (Bedani et al., 2013). The pH of all fermented soymilk
products was similar and significantly did not affect the viability of L. acidophilus and
B. animalis that remained above 8 log cfu g-1 in all fermented soymilk products
during 28 days of storage.
3.3 Viability of probiotics in fruits and vegetables based products

Fermented foods of plant origin have been increasingly considered as vehicle for
probiotic bacteria delivery (Gupta and Abu-Ghannam, 2012). The high level of
beneficial nutrients in fruits and vegetables such as antioxidants, vitamins, dietary
fibres and minerals could make them ideal substrates for probiotics growing (Soccol

12
et al., 2010; Peres et al., 2012). Several studies have reported the spontaneous
fermentation in both Spanish and Italian table olives by L. plantarum, L.
paraplantarum L. pentosus and L. casei (Hurtado et al., 2008; Panagou et al., 2008;
Randazzo et al., 2010; Abriouel et al., 2012; Tofalo et al., 2012). This process is
strongly influenced by many factors such as variation of indigenous microbiota, the
acidity, the competitive activity of yeast population, the variety of contaminating
microorganisms from fermentation vessels, external temperature and salt
concentration (Panagou et al., 2003; Bevilacqua et al., 2009; Hurtado et al., 2009;
Abriouel et al., 2012). In addition, the viability of indigenous LAB in naturally
fermented olives is influenced by polyphenols content in olives fruits and LAB ability
to degrade oleuropein (Hurtado et al., 2012). LAB capability to colonize the surface
of green olives during fermentation discovered promising perspectives for using table
olives as carrier of probiotic bacteria (Sisto and Lavermicocca, 2012). Recently, a
clinical isolation of L. paracasei IMPC2.1 from human gastrointestinal tract has been
used as a probiotic culture during fermentation of green and ripe olives with highly
significant results (Lavermicocca et al., 2005; De Bellis et al., 2010; Sisto and
Lavermicocca, 2012). Fermentation of table olives with probiotic bacteria may
provide high added value to the final product with probiotic potential. Current study
found that, L. pentosus B281 and L. plantarum B282 (isolated from industrially
fermented table olives) inoculated either as single or combined cultures had capacity
to establish a vigorous lactic fermentation of green olives despite the initial salt level
in the brines (Blana et al., 2014). In addition, L. pentosus B281 was shown to be more
viable and remained at levels exceeding 6.0 log units over 120 day regardless of the
salt levels employed during fermentation. However, L. plantarum B282 was slightly
affected by the 10% salt brines and remained at levels below 6.0 log units at the end
of the process. Furthermore, higher recover percentage (93.3%) of L. pentosus B281
in 10% brines than 81.2% of L. plantarum B282 in 8% salt brines indicating that L.
pentosus B281 is particularly well adapted to higher salt concentrations (Blana et al.,
2014). Similarly, Randazzo et al. (2014) demonstrated that both L. plantarum and L.
paracasei was well adapted in the brine salt (6%) during the fermentation of Giarraffa
and Grossa di Spagna table olives. The viable cell counts of these probiotics reached
to high level (7 log cfu ml-1) after 2 weeks fermentation and maintained their viability
over 120 days (Randazzo et al., 2014).
13
 Chestnut purees verified to be the suitable media for probiotic growth. Six
probiotic strains (Table 3) demonstrating to be well adapted to the environment with
high cell counts of 109 cfu ml-1 for L. rhamnosus VT1 and RBT397 and 108 cfu ml-1
for other strains in the final product after fermentation for 24 hours (Blaiotta et al.,
2012). All the six strains seemed to have significant potential for survival in chestnut
puree (8 log cfu ml-1; pH 2.5 - 3) during 40 days of storage at 4 °C (Blaiotta et al.,
2012). Therefore, probiotic chestnut puree would be suitable candidates for increase
functional products availability being above the minimum value (6 log10 cfu ml-1)
recommended for a probiotic to exert its health benefits (Lourens-Hattingh and
Viljoen, 2001). Another study conducted by Kim et al. (2010) reported that fermented
pear puree by Leuconostoc mesenteroides showed high viable cell counts (109 cfu ml-
1
) for 2 weeks storage. Microencapsulated L. acidophilus inoculated in banana puree
during fermentation resulting in desirable viable cell counts of 108 cfu ml-1 in the final
product (Tsen et al., 2004).

A novel fermented cabbage product (sauerkraut) has produced using probiotic

strain of L. paracasei LMG P22043 (Sarvan et al., 2013). It was shown that blanched
white cabbage without nutrient supplementation supported L. paracasei LMG P22043
growth reaching counts of 8 log cfu ml-1 after 71 hours of fermentation in 4% brine at
25°C. The viability of probiotic remained steady in fermented cabbage (pH 4.1-3.6)
during 30 days refrigerated vacuum-packed storage at 4°C (Sarvan et al., 2013).
3.4 Viability of probiotics in meats products
The commercial application of probiotic bacteria in meat products is not yet common.
Food industry is seeking to improve the quality characteristics of meat products and
extend the shelf life through maintain high level of viable cell counts of probiotic
bacteria (Sidira et al., 2014b). When probiotic strains are selected, attributes important
for their ability to compete with endogenous LAB found in meat besides good growth
and survival during fermentation and storage must be considered (Benito et al., 2007;
Rebucci et al., 2007; Kołożyn-Krajewska and Dolatowski, 2012). Thus the select of
appropriate probiotic strains will be important. One obvious industrial option is to use
bacteria familiar to the meat environment that have probiotic properties and beneficial
health effects. Several factors such as high content of curing salt, low pH, low water
activity and heat treatment may affect the activity of probiotics in fermented meat

14
products. However, numbers of studies have proved the suitability of selected
probiotic bacteria to use as probiotic cultures in fermented sausages (Arihara, 2006;
Ammor and Mayo, 2007; Rebucci et al., 2007). This is because of well adapted to the
environment during sausage fermentation associated with fast growth rate and
acidification. Erkkilä et al. (2001a and b) reported that some probiotics (Table 3) were
suitable for use as starter cultures in more acidic North European dry sausages. The
viable counts of these probiotics at the end of the processing period ranged between
8.0 and 9.0 log cfu g-1. P. pentosaceus E-90390 was the fastest growing strain
whereas L. plantarum E-98098 and L. rhamnosus LC-705 were the slowest.
Klingberg et al. (2005) identified three potential probiotic strains (Table 3) as
dominant non-starter LAB from fermented meat products. The three strains were
successfully applied as starter cultures for the production of Scandinavian-type
fermented sausages with high cell numbers ranging between 7.0 and 8.0 log cfu g-1 in
the final product. Previous study found that the viable counts of L. plantarum 299V
inoculated in fermented sausages increased from 105 cfu g-1 to 108 cfu g-1 at the end of
processing and this value remained constant even during storage at 1°C for one month
(Rubio et al. 2013). Immobilized cells technology with probiotic bacteria has shown
significantly higher survival rates than free cells during food manufacture and storage
(Kourkoutas et al., 2005, 2006). The application of cell immobilization could
potentially benefit the meat industry by maintain high cell viability, which is an
important requirement in the manufacture of probiotic foods. Sidira et al. (2014b)
investigated the immobilized L. casei ATCC 393 on wheat as probiotic starter culture
in dry fermented sausages. Immobilized L. casei ATCC 393 was detected after 71
days of ripening at above the minimum level of probiotics (≥6 log cfu g-1) for
providing the health benefits. Moreover, despite dry fermented sausages are usually
consumed uncooked, mild heat treatment application (70-72 °C for 8-10 min) found
to have no effect on the probiotic cell counts of sausages produced with immobilized
cells (Sidira et al., 2014a). Another study showed that the viable cell counts of
alginate-microencapsulated L. reuteri in dry fermented sausages reduced by only ≤
0.5 log units compared to 2.6 log units of unencapsulated L. reuteri cells samples after
drying at 13 °C and 75% relative humidity (RH) for 25 days (Muthukumarasamy and
Holley, 2006). Rubio et al. (2014) concluded that probiotic strains (Table 3) isolated
from infant faeces represent promising candidates for probiotic meat starter cultures
15
suitable to grow, survive and dominate the endogenous LAB in a fermented sausage
environment. Previously, it has reported that traditional Spanish non fermented dry
cured sausage (Longaniza de Pascua) can be a good vehicle for probiotic bacteria, as
it showed excellent survival of the probiotic species especially in the presence of 1%
orange fibre (Sayas-Barberá et al., 2012).
4. Conclusion

The utilisation of dairy and non-dairy foods as probiotics carrier is representing

potential advantages and valuable alternatives for the food industry. Since several
probiotic bacteria observed impressive viability in dairy and non-dairy foods, it is a
great potential for using the milk, meat, fruits, vegetables and cereals as substrate or
as active ingredients (prebiotic) during manufacture of probiotic foods. In order to
improve the survival rates of probiotic microorganisms during foods production,
microencapsulation considered to be a promising process. Encapsulation materials are
recognized as safe ingredients and can be used in food applications. Therefore, there
is a widespread interest in the improvement of the physical and mechanical stability
of the polymers use in probiotics encapsulation, to ensure high population of
probiotics not only in food during storage but also after gastrointestinal digestion.

Conflict of Interest

The authors declare that there is no conflict of interest.

16
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Tables:

Table 1. Applications of probiotics in different types of yogurt

Probiotics
Lactobacillus acidophilus,
Lactobacillus casei, Lactobacillus
paracasei, Lactobacillus rhamnosus,
and bifidobacteria
L. acidophilus La-5 and
Bifidobacterium animalis Bb-12
L. acidophilus La-5, B. animalis Bb-12
and Propionibacterium jensenii 702
L. acidophilus
L. acidophilus L10 and B. lactis Bl04
B. bifidum
Streptococcus thermophilus ST-20Y, L.
acidophilus LA-5, and
Bifidobacterium BB-12
S. thermophilus, L. delbrueckii subsp.
Bulgaricus and B. animalis subsp.
Lactis
L. bulgaricus and S. thermophilus
L. rhamnosus and L. acidophilus
L. acidophilus and B. lactis
L. rhamnosus IMC 501 and L.
paracasei IMC 502
L. plantarum (6E and M6)
S. thermophilus, L. acidophilus, L.
rhamnosus, L. bulgaricus and B. lactis
L. acidophilus, L. rhamnosus, L.
bulgaricus, B. lactis and S.
thermophilus
B. bifidum Bb-02 and L. acidophilus
La-5
Yogurt type References
Yogurt with flavouring agents such as (Vinderola et al., 2002)
strawberry, vanilla, peach, and banana
essences
Soy yogurt enriched with mango and (Bedani et al., 2014)
guava pulps
stirred fruit yogurts (Ranadheera et al., 2012)
stirred fruit yogurts (Kailasapathy et al., 2008)
Açai pulp yogurt (Espírito Santo et al., 2010)
Dates yogurt (El-Nagga and Abd El–Tawab, 2012)
Yogurt enriched with whey protein (Martìn-Diana et al., 2003)
concentrate (WPC)
Yogurt enriched with skimmed milk (Marafon et al., 2011)
powder, WPC and sodium caseinate
Yogurt enriched with L-cysteine (Cys) (Michael et al., 2010)
Yogurt enriched with pea protein, (Zarea et al., 2012)
chickpea flour, lentil flour, pea fibre,
soy protein concentrate and soy flour
Yogurt enriched with green lentils (Agil et al., 2013)
Yogurt enriched with buckwheat flour (Coman et al., 2013)
and oat bran
Yogurt-like beverages enriched with (Coda et al., 2012)
rice, rice and soy, rice and barley, rice
and emmer and rice and oat
Yogurt enriched with inulin (Oliveira et al., 2011a)
Yogurt enriched with Lactulose (Oliveira et al., 2011b)
Yogurt enriched with Lactulose (Ozer et al., 2005)

Table 2. Applications of probiotics in cheese.

Probiotics Cheese type References
L. paracasei and Lactococcus spp Minas cheese (Buriti et al., 2005a)
L. acidophilus La-5, Lactococcus lactis subsp. Lactis and Lactococcus lactis Minas cheese (Buriti et al., 2005b)
subsp. Cremoris
L. acidophilus La-5, B. animalis Bb-12 and S. thermophilus Minas cheese (Buriti et al., 2007)
L. acidophilus La-5 and S. thermophilus Minas cheese (Souza and Saad, 2009)
L. delbrueckii subsp. bulgaricus, L. acidophilus, L. rhamnosus, B. animalis Minas frescal (Almeida et al., 2008)
subsp. Lactis and Streptococcus thermophilus cheese whey
Bifidobacterium (Bb-12) Minas Frescal (Fritzen-Freire et al.,
cheese 2010)
L. acidophilus Turkish white (Kasımoğlu et al., 2004)
cheese
L. fermentum, L. plantarum, Lactoccocus lactis subsp. Cremoris and Turkish Beyaz (Kil‎iç et al., 2009)
Lactococcus lactis subsp. lactis cheeses
B. lactis Bb-12 and B. longum BB536 Cheddar cheese (Brearty et al., 2001)
B. longum 15708 Cheddar cheese (Fortin et al., 2011;
Amine et al., 2014)
L. acidophilus 4962, L. cidophilus L10, L. casei 279, L. casei L26, B. longum Cheddar cheese (Ong et al., 2006; Ong
1941, B lactis B94 and Shah, 2009)
B. lactis B94, B. lactis Bb12, Bifidobacterium sp. DR10, L. acidophilus L10 Cheddar cheese (Phillips et al., 2006)
and La5, L. paracasei L26, L. casei Lc1 and L. rhamnosus DR20

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Table 3. Applications of probiotics in non-dairy foods.
Probiotics Food product References
L. paracasei subsp. paracasei LBC 82 Chocolate mousse (Aragon-Alegro et al., 2007)
L. helveticus CNCM I-1722 and B. longum Chocolate (Possemiers et al., 2010)
CNCM I-3470
L. acidophilus MJLA1, L. rhamnosus 100-C, L. Non-fermented (Heenan et al., 2004)
paracasei ssp. paracasei 01, B. lactis BBDB2, B. vegetarian frozen soy
lactis Bb-12 and Saccharomyces boulardii 74012 dessert
B. longum and B. lactis Fermented acerola (Favaro-Trindade et al., 2006)
B. lactis and L. paracasei Coconut flan (Correa et al., 2008)
B. lactis Bb12 and L. rhamnosus GG Liquid maple sap (Khalf et al., 2010)
L. paracasei subsp. paracasei DC412 Salad dressing (Mantzouridou et al., 2013)
L. casei and L. plantarum B2 Fermented rice bran (Zubaidah et al., 2012)
L. plantarum Barley, wheat and malt (Charalampopoulos and Pandiella, 2010)
extracts
L. reuteri Cereal-based probiotic (Kedia et al., 2007)
food
L. reuteri, L. acidophilus (LA5 and 1748) and L. Maize porridge (Helland et al., 2004)
rhamnosus GG
L. acidophilus La-5, B. animalis Bb-12, and S. Fermented soymilk (Bedani et al., 2013)
thermophilus product with inulin and
okara flour
L. paracasei IMPC2.1 Fermentation green (Lavermicocca et al., 2005; De Bellis et al.,
olives 2010; Sisto and Lavermicocca, 2012)
L. plantarum, L. paraplantarum, L. pentosus and Spanish and Italian table (Hurtado et al., 2008; Panagou et al., 2008;
L. casei olives Randazzo et al., 2010; Abriouel et al., 2012;
Tofalo et al., 2012)
L. pentosus B281 and L. plantarum B282 Green olives (Blana et al., 2014)
L. plantarum and L. paracasei Giarraffa and Grossa di (Randazzo et al., 2014)
Spagna table olives
L. rhamnosus VT1, LrhRBM526, lrhRBT739, L. Chestnut purees (Blaiotta et al., 2012)
casei, Lbc491, Lbc496 and L. rhamnosus GG
Leuconostoc mesenteroides Pear puree (Kim et al., 2010)
L. acidophilus Banana puree (Tsen et al., 2004)
L. paracasei LMG P22043 Fermented cabbage (Sarvan et al., 2013)
(sauerkraut)
L. rhamnosus (GG, LC-705 and E-97800), North European dry (Erkkilä et al., 2001a and b)
Pediococcus pentosaceus E-90390 and L. sausages
plantarum E-98098
L. plantarum MF1291 and MF 1298, L. pentosus Scandinavian-type (Klingberg et al., 2005)
MF1300 fermented sausages
L. plantarum 299V Fermented sausages (Rubio et al. 2013)
L. casei ATCC 393 Dry fermented sausages (Sidira et al., 2014 a and b)
L. reuteri Dry fermented sausages (Muthukumarasamy and Holley, 2006)
L. casei/paracasei CTC1677, L. casei/paracasei Fermented sausage (Rubio et al., 2014)
CTC1678 and L. rhamnosus CTC1679
L. brevis, L. plantarum, L. casei, L. paracsei, L. Fermented sausages (Pennacchia et al. , 2004)
pentosus, L. reuteri, L. curvatus, L. sakei and L.
zeae
L. curvatus and L. plantarum Greek dry fermented (Papamanoli et al., 2003)
sausages

Highlights

 Viability of probiotics in fermented dairy products.

 Viability of probiotics in desserts products.

 Viability of probiotics in cereals-based products.

 Viability of probiotics in fruits and vegetables based products.

 Viability of probiotics in meats products.

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