doi: 10.1111/j.1471-0307.2012.00880.

ORIGINAL
RESEARCH

Cream cheese as a symbiotic food carrier using

Bidobacterium animalis Bb-12 and Lactobacillus
acidophilus La-5 and inulin
LARISSA L ALVES,1* NEILA S P S RICHARDS,1 PAULA MATTANNA,1
DIEGO F ANDRADE,1 ADRIANO P S REZER,1 LIANA I G MILANI,1
A D R I A N O G C R U Z 2 and J O S A F F A R I A 2
1

Departamento de Tecnologia e Cincia dos Alimentos- Av. Roraima, Universidade Federal de Santa Maria (UFSM),
Santa Maria, RS Brasil, and 2Faculdade de Engenharia de Alimentos, Universidade Estadual de Campinas
(UNICAMP), Campinas, SP Brasil

The stability of cream cheeses as a symbiotic food carrier, through supplementation with different
concentrations of probiotic bacteria Bidobacterium animalis Bb-12 and Lactobacillus acidophilus
La-5 and the prebiotic ingredient inulin was investigated. Physicochemical parameters, pH values,
total solids, fat and protein levels and the viable counts of the starter lactic culture Streptococcus
thermophilus and probiotic cultures, were carried out at 1, 15, 30 and 45 days of refrigerated storage (8 0.5 C). Different physicochemical characteristics were observed in all formulations.
S. thermophilus showed good viability in all the trials (6.669.38 log cfu/g), whereas B. animalis
remained above 6 log cfu/g in all the trials during the period evaluated. However, L. acidophilus
showed an accentuated decline, registering values of 3.1 log cfu/g at the end of the period studied.
The results suggested that cream cheese was an adequate food matrix for supplementation with
probiotic bacteria, in particular B. animalis, and the prebiotic ingredient, showing potential as a
symbiotic food.
Keywords Cream cheese, Probiotic bacteria, Inulin, Stability.

INTRODUCTION

*Author for
correspondence. E-mail:
larissafarm@yahoo.com.
br
2012 Society of
Dairy Technology

Dairy products show the most adequate matrix

for supplementation with probiotic cultures and
prebiotic ingredients due to their positive reputation in the mind of the consumers (Granato
et al. 2010). Although fermented milks and
yoghurts represent the most highly studied food
matrixes and are highly accepted by the consumers (Cruz et al. 2011, 2012a,b; Marafon
et al. 2011; Akalin et al. 2012), cheeses show
some technological advantages with respect to
their supplementation with probiotic cultures
and prebiotic ingredients. In comparison with
fermented milks, their cohesive structure, higher
pH and fat content make cheeses capable of
offering additional protection to the probiotic
bacteria during its passage through the gastrointestinal tract (Cruz et al. 2009), as this microbial
group present lower resistance to acid conditions
and need a more effective protection.

Indeed, several researches concerning the

development of probiotic cheeses can be found
in the literature. It has been reported that the
development of fresh Minas-type cheese (Souza
and Saad 2009; Fritzen-Freire et al. 2010;
Gomes et al. 2011), fresh Argentine cheese
(Vinderola et al. 2000), Pategrs cheese (Perotti
et al. 2009), whey cheese (Madureira et al.
2011a,b), Cheddar cheese (Ong and Shah 2009;
Wang et al. 2010; Scheller et al. 2011), Ras
cheese (Abd El-Salam et al. 2011), Turkish
sheeps milk cheese (Albenzio et al. 2010), Fior
di Latte cheese (Minervini et al. 2012), Iranian
ultraltered Feta cheese (Karimi et al. 2012b),
Akami cheese (Ayyash et al. 2012) Iranian
white cheese (Zomorodi et al.2011; Mirzaei
et al. 2012) and Panela cheese (Escobar et al.
2012) all with showing satisfactory results
towards the probiotic bacteria viability along the
commercial shelf life. The addition of prebiotics,
especially inulin, such as imitation cheese (Miri

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Vol 66, No 1 February 2013

et al. 2011) and fresh Portuguese cheese (Rodrigues et al.

2011) has been equally reported. Finally, the benets of
ingesting probiotic cheese have been published too (Burns
et al. 2012; Lollo et al., 2012) as well as the sensory
aspects of probiotic cheese (Karami et al. 2012c).
Cream cheese is a soft, fresh cheese with a ne, smooth
consistency and slightly butter avour due to the production
of diacetyl. It is obtained by the coagulation of cream or a
mixture of milk and cream by acidication with the use of a
starter culture, and is ready for consumption soon after processing (Phadungath 2005). Its intrinsic characteristics allow
for its adaptation to a large number of combinations and
occasions, according to the consistency and culinary habits
of each country, and it is most consumed in sandwiches as
an accompaniment to salads and as the main ingredient of
cheesecake in the United States (Sanchez et al. 1996).
Researches covering cream cheeses processing are related
to technological modications such as the addition of
enzymes (Miri et al. 2011), addition of extracts (JunqueiraGonalves et al. 2011), its microstructure (Laverse et al.
2011) and also the rheological and sensory characteristics
(Brighenti et al. 2008). Few studies relate its potential as a
functional food, especially as a food matrix carrier for probiotic bacteria and prebiotic ingredients, characterising it as
a symbiotic food. Recently, it was reported that fresh cream
cheese added with inulin and Lactobacillus paracasei presented good stability during 21 days refrigerated storage
(Buriti et al. 2007). However, there is a need to evaluate
increased shelf life and other probiotic strains.
In this context, this research aimed to evaluate the adequacy
of cream cheese as a food matrix for supplementation with probiotic bacteria (Lactobacillus acidophilus and Bidobacterium
animalis Bb 12) and a prebiotic ingredient (inulin), evaluating
its potential as a symbiotic food. In this context, viable bacteria
counts as well as physicalchemical parameters were evaluated
during 1, 15, 30 and 45 days refrigerated storage.
MATERIAL AND METHODS

Cream cheese processing

Twelve cream cheese trials were carried out (T1T12),
adapting the procedure described by Alves et al. (2009).
Fifty litres of pasteurised milk (UNI-UFSM, Santa Maria,
RS, Brazil) was standardised to 8% w/w fat with pasteurised
dairy cream (50% w/w fat content) (UNI-UFSM). Following
this, the starter culture was added (2% w/v, 7 log cfu/g of
Streptococcus thermophilus TH-4; Chr. Hansen, Valinhos,
Brasil) and 0.25% (v/v) of commercial liquid rennet
(Ha-La; Chr. Hansen, Valinhos, So Paulo, Brazil) added.
Fermentation was carried out in a 50 L stainless steel cheese
vat for approximately 18 h at 25 C. On reaching a pH
value of 4.60, the coagulum was cut into cubes to aid
release the whey. After washing the curd with water (25%
w/v, approximately 6 L), it was placed in plastic cheese
64

moulds with cotton whey-removers, and placed in the refrigerator for about 15 h.
After completing whey removal, the curd mass was
divided into appropriated portions, representing the 12 trials
(Table 1). The remaining ingredients were then mixed
together: salt (1% w/w, Salsul; Libraga, Brando & Cia
LTDA, Santa Maria, RS, Brasil); mixed herbs (0.2% w/w,
dehydrated parsley, chervil, tarragon, chives and oregano),
potassium sorbate (0.1% w/w; Sigma Aldrich, Germany),
nisin (0.005 w/w%; Chr. Hansen, So Paulo, Brasil), in
equal concentrations for all the trials. Inulin (Raftline; Orafti, Oreye, Belgium, DP >23) and freeze-dried cultures of
L. acidophilus La-5 and B. animalis Bb-12 (Chr. Hansen)
were then added in the amounts shown in Table 1. The
resulting cream cheeses were lled into plastic containers,
each containing 150 g, and stored under refrigeration at 4
C for 45 days of storage.

Experimental design and statistical analysis

A Central Compound Rotational Design (Box et al. 1978)
was used with the trials numbered from 1 to 12 (T1 to T12,
T9, T10 and T11) being repetitions of the central point, to
check the repeatability of the design, and T12 was the control, containing no probiotic or prebiotic. Although the use
of this type of design naturally leads to the use of response
surface methodology (RSM) (Cruz et al. 2010; Ibarra et al.
2012), in this study the design was only used as a scientic
basis. The concentrations of the prebiotic ingredient (inulin)
and probiotics (L. acidophilus and B. animalis) were chosen
taking into consideration both the preliminary tests.

Table 1 Experimental design and levels of factors in coded and real

values
Coded variable

Real variable

Trials

X1*

X2**

X1*

X2**

T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11
T12***

-1
-1
1
1
1.414
-1.414
0
0
0
0
0

-1
1
-1
1
0
0
1.414
-1.414
0
0
0

0.7
0.7
1.3
1.3
1.5
0.5
1.0
1.0
1.0
1.0
1.0

0.5
1.5
0.5
1.5
1.0
1.0
1.7
0.3
1.0
1.0
1.0

*X1 = probiotic bacteria concentration (Bidobacterium animalis

Bb-12 e Lactobacillus acidophilus La-5); Expressed in g/Kg cheese.
**X2 = prebiotic concentration (inulin); Expressed in g*100/g
cheese. ***T12 = control trial, without supplementation of prebiotic
ingredient and probiotic bacteria.

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Analytical procedures
The physicochemical and microbiological analyses were carried out at 1, 15, 30 and 45 refrigerated storage days. The
processing was repeated twice, being the analyses were performed in triplicate.
The pH values of the cheese samples were determined
using a digital pHmeter (Digimed DM-20; SPLabor, Presidente Prudente, Brasil) by direct insertion of the electrode
into the sample. Total solids were determined by drying
under vacuum (Micronal, So Paulo, Brazil) at 105 C for
24 h. Protein was estimated by measuring the cheese
nitrogen content by the Kjeldahl method and multiplying it
by a conversion factor (6.38). Fat was determined using the
Gerber Method. All the analytical procedures followed the
appropriate standard methods (Association of Ofcial
Analytical Chemistry (AOAC) 2005).
For the microbiological analyses, a total of 25 g of cheese
was transferred into a stomacher containing 225 mL of
sterile 0.1% w/v peptone water (Oxoid, So Paulo, Brazil).
Further dilutions were made from this original dilution and
the quantication of microbial counts was carried out using
the pour plate technique. Streptococcus thermophilus was
enumerated in M17 Agar (Fluka Biochemika, SigmaAldrich Chemie, Steinheim, Sua, Switzerland), aerobic
incubation for 37 C during 48 h, B. animalis was enumerated using deMan, Rogosa e Sharpe Agar (MRS) agar
(Himedia Laboratories, Mumbai, India) supplemented with
glucose, lithium chloride and cysteine (Christian Hansen
1999), and L. acidophilus was enumerated using MRS agar
(Himedia Laboratories) supplemented with maltose (International Dairy Federation 1999). These culture media have
been reported (Oberg et al. 2011; Karimi et al. 2012a) in
previous studies covering probiotic cheese development and
stability.
Statistical analysis
A repeated measure design was used where probiotic cream
cheese formulation was the treatment between subjects, and
repeated measure was carried out at seven different day
points. Analysis of variance for repeated measures was
performed using the XLSTAT for Windows 2012 version
2012.4 (Adinsoft, Paris, France). The Tukey method was
used to determine the signicance differences of mean values
at an a = 0.05 over all comparisons (Shrestha et al. 2011).
RESULTS AND DISCUSSION

pH values and proximate composition

Table 2 shows the values for pH of the cream cheeses during refrigerated storage, varying from 4.60 (treatments T1
and T2) to 4.464.63 (T4 and T5, P < 0.05) throughout the
shelf life of the probiotic cheeses, presenting differences
with respect to the control cream cheese; in addition, an
effect of the storage time was also noted (P < 0.05). This
2012 Society of Dairy Technology

Table 2 pH values of symbiotic cream cheeses during the refrigerated storage

Days

T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11
T12

X1*

X2**

15

30

45

0.7
0.7
1.3
1.3
1.5
0.5
1.0
1.0
1.0
1.0
1.0

0.5
1.5
0.5
1.5
1.0
1.0
1.7
0.3
1.0
1.0
1.0

4.60a
4.60b
4.58b
4.58c
4.59b
4.56b
4.49b
4.51b
4.48c
4.50b
4.47c
4.52c

4.62a
4.63a
4.55b
4.63a
4.62a
4.60a
4.50b
4.54ab
4.49c
4.58c
4.48c
4.58d

4.61a
4.61ab
4.53a
4.61b
4.58c
4.61a
4.52b
4.52ab
4.54b
4.52b
4.51b
4.54b

4.54bc
4.49c
4.49c
4.46d
4.47d
4.48c
4.58a
4.57a
4.61a
4.60a
4.60a
4.60a

*Analysis performed in duplicate. Different lowercase letters in the

same row in indicate presence of statistical difference (P < 0.05)
among the treatments (cream cheeses) along the storage days,
according with the Tukey Test. X1 = probiotic bacteria concentration (g/kg); **X2 = prebiotic ingredient concentration (g*100/g). T1,
T2,., T12 = see Table 1.

suggests the occurrence of metabolic activity of the probiotic cultures in the products during this refrigerated storage.
Similar results were reported found in Pategras cheese supplemented with six different probiotic cultures (Bergamini
et al. 2010).
Table 3 shows the results obtained in the proximate analyses of the cream cheeses. Most of the cheeses could be classied as semifat cheeses, presenting fat content ranged from
21.01 to 26.69% and total solid contents ranged from 60.54 to
66.49% w/w respectively. As expected, the formulations containing the highest inulin contents (T2, T4 and T7) showed
the lowest moisture contents (P < 0.05), as the prebiotic contributed to the total solids contents. Similar results were
reported by Akalin et al. (2007) and Guggisberg et al. (2009)
in yoghurts supplemented with inulin. In addition, there was
no variation in fat content in the formulations of cream cheese
(P < 0.05) being reported; however, different ndings in the
protein content among the cream cheese trials (P < 0.05).
These differences could be related to some minor problems occurred during the cheese processing. Although
efforts were made to standardise cheese manufacturing, the
possibility of a small variation during the cutting of the curd
and the whey drainage cannot be completely excluded.

Viability of the starter and probiotic cultures during

storage
Overall, it was observed an effect of storage time at all
viable number of starter culture (P < 0.05). Streptococcus
thermophilus counts ranged from 6.66 to 9.38 log cfu/g
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Vol 66, No 1 February 2013

Table 3 Centesimal composition of symbiotic cream cheeses

X1*
T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11
T12

0.7
0.7
1.3
1.3
1.5
0.5
1.0
1.0
1.0
1.0
1.0

X2**
0.5
1.5
0.5
1.5
1.0
1.0
1.7
0.3
1.0
1.0
1.0

Total solids
a

65.55
60.54b
66.56a
60.86b
65.58a
65.06a
60.84b
66.11a
61.03b
61.07b
61.14b
66.49a

Fat

Protein
a

22.24
25.16a
21.01a
26.69a
26.50a
21.74a
26.40a
21.27a
25.72a
26.02a
26.27a
21.11a

7.38cd
7.05e
7.32cde
7.15de
7.37cd
7.10de
7.51bc
7.81a
7.33cde
7.50bc
7.25cde
7.74ab

*Analysis performed in duplicate; values expressed in g*100/g.

Different lowercase letters in the same row in indicate presence of
statistical difference (P < 0.05) among the treatments (cream
cheeses) along the storage days, according with the Tukey Test.
X1 = probiotic bacteria concentration (g/kg); **X2 = prebiotic ingredient concentration (g*100/g). T1, T2,., T12 = see Table 1.

(Table 4) in the probiotic cream cheeses, presenting variable

behaviour. In some treatments (T1T6), a reduction in the
viable count was observed, whereas in others (T7T11) the
reduction was minimal or nonexistent, not differing from
the control (T12). The viability of this micro-organism is
associated with the different ability to liberate acids into the
medium due to lactose degradation as a part of their metabolism, producing galactose which can be available for the
growth of the probiotic cultures, contributing positively to
the maintenance of their viability.
Bidobacterium animalis count (Table 5) maintained levels above 6 log cfu/g for all the trials up to 45 days of
refrigerated storage, guaranteeing the amount considered
minimum to obtain the positive effect for the consumer
(Uysal et al. 2003; Boylston et al. 2004). After 45 days of
refrigerated storage, the viability of B. animalis varied from
6.04 (T3) to 6.93 log cfu/g. This result is of interest, as the
values were obtained using a minimal concentration of the
probiotic culture and prebiotic ingredient, to the contrary of
other studies (Magarios et al. 2007; Ekinci et al. 2008),
and suggests a protective effect of the food matrix in the
case of cream cheese in relation to the various extrinsic factors that affect the product, such as the oxygen that permeates the package, as mentioned by other authors (Cruz et al.
2007). Previous researches have indicated the presence of
excess acid and low pH values as decisive factors in the
viability of probiotics, especially of Bidobacterium (Dave
and Shah 1997; Shah 2000; Kailasapathy 2006). In this
study, the maintenance of the pH value above this value
may have contributed to the elevated survival rate of the
B. animalis.
66

Table 4 Viable Streptococcus thermophilus count of symbiotic

cream cheeses during the refrigerated storage
Days

T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11
T12

X1*

X2**

15

30

45

0.7
0.7
1.3
1.3
1.5
0.5
1.0
1.0
1.0
1.0
1.0

0.5
1.5
0.5
1.5
1.0
1.0
1.7
0.3
1.0
1.0
1.0

8.22a
8.20
8.04a
8.53
8.58
8.64
9.38
9.10c
9.05
9.09
9.17
9.25

7.95b
8.04b
7.93b
7.83b
7.96b
7.87b
9.07c
9.17b
9.11
9.13
9.25
9.17b

7.47c
7.72c
7.54c
7.59c
7.59c
7.72c
9.10c
9.10c
9.07
9.02b
8.95b
8.98c

7.17d
7.13d
7.08d
7.00d
6.90d
6.66d
9.23b
9.24
8.80b
8.91c
8.93b
9.28abc

*Microbiological analysis is expressed in log cfu/g of cheese. Analysis performed in duplicate. Different lowercase letters in the same
row in indicate presence of statistical difference (P < 0.05) among
the treatments (cream cheeses) along the storage days, according
with the Tukey Test. X1 = probiotic bacteria concentration (g/kg);
**X2 = prebiotic ingredient concentration (g*100/g). T1, T2,.,
T12 = see Table 1.

Table 5 Viable Bidobacterium animalis count of symbiotic cream

cheeses during the refrigerated storage
Days

T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11

X1*

X2**

15

30

45

0.7
0.7
1.3
1.3
1.5
0.5
1.0
1.0
1.0
1.0
1.0

0.5
1.5
0.5
1.5
1.0
1.0
1.7
0.3
1.0
1.0
1.0

7.74
7.76
7.60
7.54
7.70
7.52
7.02
7.08
7.03
7.22
7.50

7.27b
7.19b
7.45b
7.01b
7.34b
7.16b
6.47b
6.47c
6.46d
7.18
7.57ab

6.44c
6.59c
6.52c
6.48c
6.73c
6.49c
6.90
6.87b
6.85b
6.83b
6.86ab

6.49c
6.48c
6.04d
6.19c
6.51c
6.12d
6.93
6.88b
6.67c
6.84b
6.75b

*Microbiological analysis is expressed in log cfu/g of cheese. Analysis performed in duplicate. Different lowercase letters in the same
row in indicate presence of statistical difference (P < 0.05) among
the treatments (cream cheeses) along the storage days, according
with the Tukey Test. X1 = probiotic bacteria concentration (g/kg);
**X2 = prebiotic ingredient concentration (g*100/g). T1, T2,.,
T12 = see Table 1.

Lactobacillus acidophilus showed a sharp fall in viability

during the period 211 studied (Table 6), reaching values
between 3.10 and 5.4 log cfu/g along 45 days refrigerated
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Table 6 Viable Lactobacillus acidophilus count of symbiotic cream

cheeses along the refrigerated storage
Days

T1
T2
T3
T4
T5
T6
T7
T8
T9
T10
T11

X1*

X2**

15

30

45

0.7
0.7
1.3
1.3
1.5
0.5
1.0
1.0
1.0
1.0
1.0

0.5
1.5
0.5
1.5
1.0
1.0
1.7
0.3
1.0
1.0
1.0

8.00
8.20
7.89
7.85
7.93
7.87
6.84
6.73
6.86
6.67
6.97

7.18b
7.15b
7.31b
7.05b
7.54b
7.44b
4.52b
5.09b
5.18b
5.14b
5.06b

6.26c
6.23c
6.50c
6.47c
6.57c
6.54c
4.42b
5.09b
4.16c
4.16c
4.12c

4.56d
5.40d
4.05d
4.12d
4.03d
3.97d
3.20c
3.26c
3.26d
3.10d
3.20d

*Microbiological analysis is expressed in log cfu/g of cheese. Analysis performed in duplicate. Different lowercase letters in the same
row in indicate presence of statistical difference (P < 0.05) among
the treatments (cream cheeses) along the storage days, according
with the Tukey Test. X1 = probiotic bacteria concentration (g/kg);
**X2 = prebiotic ingredient concentration (g*100/g). T1, T2,.,
T12 = see Table 1.

in the intestinal tract by the probiotic bacteria, modulating

the composition of the intestinal ora of the consumer in a
positive way. In this context, spite of the limitations of this
study, as it was not performed the determination of inulin
by the appropriated analytical methodology, our results
present interesting and relevant.
Oliveira and Jurkiewicz (2009) only observed an effect of
adding inulin concentrations varying from 0.44% to 3% to
fermented milk on the counts of B. animalis Bb-12 after
64 days of storage, and found no effect of the prebiotic on
L. acidophilus La-5. Overall, the ndings suggest that cream
cheese has a potential to be used as a food matrix for carrying probiotic bacteria and prebiotic ingredients, characterising it as a functional food. Bidobacterium animalis counts
above 6 log cfu/g were observed in all the treatments, in
agreement with the recommendations made in various studies (Shah 2000). With respect to inulin, if the recommended
portions (30 g) of some formulations of cream cheese were
consumed twice a day, this would result in a daily consumption of 3 g of inulin, characterising such cheeses as
prebiotic foods with respect to the Brazilian regulatory legislation (Brasil 2008).
CONCLUSION

storage. Among the possible reasons, we hypothesised the

negative interaction between this probiotic culture and the
lactic cultures added (Joseph et al. 1998; Vinderola et al.
2002) as well. This hypothesis should be taken into consideration when comparing the S. thermophilus and L. acidophilus counts, where the trials containing larger numbers
of viable cells in the starter culture (T7, T8, T9, T10 and
T11) showed lower probiotic counts during the analytical
period. However, it is possible that this interaction is dependent on the strain and the food matrix used as the vehicle
for supplementation, as a recent study found no negative
effects of the starter culture on the viability of L. acidophilus in yoghurt and Pategras cheese (Bergamini et al. 2010;
Ng et al. 2011). Additional studies are required to better
understand this problem.
Absence of effect of the different concentrations of inulin
on the viability of the probiotics was observed, contrary to
the results of various other studies (Akalin et al. 2007;
Cardarelli et al. 2008; Oliveira et al. 2009), reinforcing the
need for prior compatibility between the probiotics and prebiotics in the food matrix, to provide a positive interaction.
This can be observed in trials T7 and T8, in which the
same concentration of probiotics presented similar behaviour on the viable population of B. animalis (Table 4) and
L. acidophilus (Table 5) throughout the 45 days of storage,
despite the concentrations of inulin being different
(T7 = 1.7% w/w and T8 = 0.3 w/w%). This can be considered as an advantage, as the inulin will only be degraded
2012 Society of Dairy Technology

Our ndings suggest the potential of cream cheese as an

adequate food matrix for supplementation with probiotic
bacteria and prebiotic ingredient during 45 days of refrigerated storage, conrming its potential as a symbiotic food.
However, it seems that this nding is strain dependent, as
only B. animalis presented good survival along the refrigerated storage towards L. acidophilus, which presented
opposite behaviour.
Further studies should investigate the supplementation and
of other probiotic strains as well as other prebiotic ingredients. In addition, descriptive tests aimed to identify relevant
sensory descriptors for the optimisation of the formulation
should be also performed.
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