Cream Cheese as a Symbiotic Food Carrier Using Bifidobacterium

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ORIGINALRE SE ARCH Cream cheese as a symbiotic food carrier using

Bi dobacterium animalis Bb-12 and Lactobacillusacidophilus La-5 and inulin

L ARISSA L AL VE S,1* NE IL A S P S RICHARDS,1 PAUL A MAT T ANNA,1

DIE GO F ANDRADE , 1 ADRIANO P S RE Z E R,1 L IANA I G MIL ANI,1

ADRIANO G CRUZ2 and JOS É A F FA RIA 21 Departamento de Tecnologia e Ciência 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 acidophilusLa-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 Streptococcusthermophilus and probiotic cultures, were carried out at 1, 15, 30 and 45 days of refrigerated stor-age (8 ± 0.5 °C). Different physicochemical characteristics were observed in all formulations.

S. thermophilus showed good viability in all the trials (6.66 – 9.38 log cfu/g), whereas B. animalisremained above 6 log cfu/g in all the trials during the period evaluated. However, L. acidophilusshowed 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 asymbiotic food.

Keywords Cream cheese, Probiotic bacteria, Inulin, Stability.

INTRODUCTION

Dairy products show the most adequate matrixfor supplementation with probiotic cultures andprebiotic ingredients due to their positive reputa-tion in the mind of the consumers (Granatoet al. 2010). Although fermented milks andyoghurts represent the most highly studied foodmatrixes and are highly accepted by the con-sumers (Cruz et al. 2011, 2012a,b; Marafonet al. 2011; Akalin et al. 2012), cheeses showsome technological advantages with respect totheir supplementation with probiotic culturesand prebiotic ingredients. In comparison withfermented milks, their cohesive structure, higher pH and fat content make cheeses capable of offering additional protection to the probioticbacteria during its passage through the gastroin-testinal tract (Cruz et al. 2009), as this microbialgroup present lower resistance to acid conditionsand need a more effective protection.

Indeed, several researches concerning thedevelopment of probiotic cheeses can be foundin the literature. It has been reported that thedevelopment of fresh Minas-type cheese (Souzaand Saad 2009; Fritzen-Freire et al. 2010;Gomes et al. 2011), fresh Argentine cheese(Vinderola et al. 2000), Pategrás cheese (Perottiet 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), Turkishsheep’s milk cheese (Albenzio et al. 2010), Fior di Latte cheese (Minervini et al. 2012), Iranianultraltered Feta cheese (Karimi et al. 2012b),Akami cheese (Ayyash et al. 2012) Iranianwhite cheese (Zomorodi et al.2011; Mirzaeiet al. 2012) and Panela cheese (Escobar et al.2012) all with showing satisfactory resultstowards the probiotic bacteria viability along thecommercial shelf life. The addition of prebiotics,especially inulin, such as imitation cheese (Miri

*Author for correspondence. E-mail:[email protected]

© 2012 Society of Dairy Technology

Vol 66, No 1 February 2013 International Journal of Dairy Technology 63

doi: 10.1111/j.1471-0307.2012.00880.x


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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 (Burnset al. 2012; Lollo et al., 2012) as well as the sensoryaspects of probiotic cheese (Karami et al. 2012c).

Cream cheese is a soft, fresh cheese with a

ne, smoothconsistency and slightly butter avour due to the productionof diacetyl. It is obtained by the coagulation of cream or amixture of milk and cream by acidication with the use of astarter culture, and is ready for consumption soon after pro-cessing (Phadungath 2005). Its intrinsic characteristics allowfor its adaptation to a large number of combinations andoccasions, according to the consistency and culinary habitsof each country, and it is most consumed in sandwiches asan accompaniment to salads and as the main ingredient of cheesecake in the United States (Sanchez et al. 1996).

Researches covering cream cheeses processing are relatedto technological modications such as the addition of

enzymes (Miri et al. 2011), addition of extracts (Junqueira-Gonçalves 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 afunctional food, especially as a food matrix carrier for pro-biotic bacteria and prebiotic ingredients, characterising it asa symbiotic food. Recently, it was reported that fresh creamcheese added with inulin and Lactobacillus paracasei pre-sented good stability during 21 days refrigerated storage(Buriti et al. 2007). However, there is a need to evaluateincreased 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 pro-biotic bacteria ( Lactobacillus acidophilus and Bi dobacteriumanimalis Bb 12) and a prebiotic ingredient (inulin), evaluatingits potential as a symbiotic food. In this context, viable bacteriacounts as well as physical – chemical parameters were evaluatedduring 1, 15, 30 and 45 days refrigerated storage.

MATERIAL AND METHODS

Cream cheese processing

Twelve cream cheese trials were carried out (T1 – T12),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 pasteuriseddairy cream (50% w/w fat content) (UNI-UFSM). Followingthis, 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, São Paulo, Brazil) added.Fermentation was carried out in a 50 L stainless steel cheesevat for approximately 18 h at 25 °C. On reaching a pHvalue of 4.60, the coagulum was cut into cubes to aidrelease the whey. After washing the curd with water (25%w/v, approximately 6 L), it was placed in plastic cheese

moulds with cotton whey-removers, and placed in the refrig-erator for about 15 h.

After completing whey removal, the curd mass wasdivided into appropriated portions, representing the 12 trials(Table 1). The remaining ingredients were then mixed

together: salt (1% w/w, Salsul

®

; Libraga, Brandão & CiaLTDA, 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, São Paulo, Brasil), inequal concentrations for all the trials. Inulin (Raftline®; Ora-fti, 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. Theresulting 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 analysisA 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, tocheck the repeatability of the design, and T12 was the con-trol, containing no probiotic or prebiotic. Although the useof this type of design naturally leads to the use of responsesurface methodology (RSM) (Cruz et al. 2010; Ibarra et al.2012), in this study the design was only used as a scienticbasis. The concentrations of the prebiotic ingredient (inulin)and probiotics ( L. acidophilus and B. animalis) were chosentaking into consideration both the preliminary tests.

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

Trials

Coded variable Real variable

X 1* X 2** X 1* X 2**

T1 -1 -1 0.7 0.5T2 -1 1 0.7 1.5T3 1 -1 1.3 0.5T4 1 1 1.3 1.5T5 1.414 0 1.5 1.0T6 -1.414 0 0.5 1.0

T7 0 1.414 1.0 1.7T8 0 -1.414 1.0 0.3T9 0 0 1.0 1.0T10 0 0 1.0 1.0T11 0 0 1.0 1.0T12*** – – – –

*X1 = probiotic bacteria concentration ( Bi dobacterium 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 car-ried out at 1, 15, 30 and 45 refrigerated storage days. Theprocessing was repeated twice, being the analyses were per-formed in triplicate.

The pH values of the cheese samples were determinedusing a digital pHmeter (Digimed DM-20; SPLabor, Presi-dente Prudente, Brasil) by direct insertion of the electrodeinto the sample. Total solids were determined by dryingunder vacuum (Micronal, São Paulo, Brazil) at 105 °C for 24 h. Protein was estimated by measuring the cheesenitrogen content by the Kjeldahl method and multiplying it by a conversion factor (6.38). Fat was determined using theGerber Method. All the analytical procedures followed theappropriate standard methods (Association of Of cialAnalytical Chemistry (AOAC) 2005).

For the microbiological analyses, a total of 25 g of cheesewas transferred into a stomacher containing 225 mL of

sterile 0.1% w/v peptone water (Oxoid, São Paulo, Brazil).Further dilutions were made from this original dilution andthe quantication of microbial counts was carried out usingthe pour plate technique. Streptococcus thermophilus wasenumerated in M17 Agar (Fluka Biochemika, Sigma-Aldrich Chemie, Steinheim, Suíça, Switzerland), aerobicincubation for 37 °C during 48 h, B. animalis was enumer-ated using deMan, Rogosa e Sharpe Agar (MRS) agar (Himedia Laboratories, Mumbai, India) supplemented withglucose, lithium chloride and cysteine (Christian Hansen1999), and L. acidophilus was enumerated using MRS agar (Himedia Laboratories) supplemented with maltose (Interna-

tional Dairy Federation 1999). These culture media havebeen reported (Oberg et al. 2011; Karimi et al. 2012a) inprevious studies covering probiotic cheese development andstability.

Statistical analysis

A repeated measure design was used where probiotic creamcheese formulation was the treatment between subjects, andrepeated measure was carried out at seven different daypoints. Analysis of variance for repeated measures wasperformed using the XLSTAT for Windows 2012 version2012.4 (Adinsoft, Paris, France). The Tukey method wasused to determine the signicance differences of mean valuesat 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 dur-ing refrigerated storage, varying from 4.60 (treatments T1and T2) to 4.46 – 4.63 (T4 and T5, P < 0.05) throughout theshelf life of the probiotic cheeses, presenting differenceswith respect to the control cream cheese; in addition, aneffect of the storage time was also noted (P < 0.05). This

suggests the occurrence of metabolic activity of the probiot-ic cultures in the products during this refrigerated storage.Similar results were reported found in Pategras cheese sup-plemented with six different probiotic cultures (Bergaminiet al. 2010).

Table 3 shows the results obtained in the proximate analy-ses of the cream cheeses. Most of the cheeses could be classi-ed as semifat cheeses, presenting fat content ranged from21.01 to 26.69% and total solid contents ranged from 60.54 to66.49% w/w respectively. As expected, the formulations con-taining the highest inulin contents (T2, T4 and T7) showedthe lowest moisture contents (P < 0.05), as the prebiotic con-tributed to the total solids contents. Similar results werereported by Akalin et al. (2007) and Guggisberg et al. (2009)in yoghurts supplemented with inulin. In addition, there wasno variation in fat content in the formulations of cream cheese(P < 0.05) being reported; however, different ndings in theprotein content among the cream cheese trials (P < 0.05).

These differences could be related to some minor prob-lems occurred during the cheese processing. Althoughefforts were made to standardise cheese manufacturing, thepossibility of a small variation during the cutting of the curdand 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 allviable number of starter culture (P < 0.05). Streptococcusthermophilus counts ranged from 6.66 to 9.38 log cfu/g

Table 2 pH values of symbiotic cream cheeses during the refriger-ated storage

X 1* X 2**

Days

1 15 30 45

T1 0.7 0.5 4.60a 4.62a 4.61a 4.54bc

T2 0.7 1.5 4.60b 4.63a 4.61ab 4.49c

T3 1.3 0.5 4.58b 4.55b 4.53a 4.49c

T4 1.3 1.5 4.58c 4.63a 4.61b 4.46d

T5 1.5 1.0 4.59b 4.62a 4.58c 4.47d

T6 0.5 1.0 4.56b 4.60a 4.61a 4.48c

T7 1.0 1.7 4.49b 4.50b 4.52b 4.58a

T8 1.0 0.3 4.51b 4.54ab 4.52ab 4.57a

T9 1.0 1.0 4.48c 4.49c 4.54b 4.61a

T10 1.0 1.0 4.50b 4.58c 4.52b 4.60a

T11 1.0 1.0 4.47c 4.48c 4.51b 4.60a

T12 – – 4.52c 4.58d 4.54b 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 concentra-

tion (g/kg); **X2 = prebiotic ingredient concentration (g*100/g). T1,

T2,…., T12 = see Table 1.

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(Table 4) in the probiotic cream cheeses, presenting variablebehaviour. In some treatments (T1 – T6), a reduction in theviable count was observed, whereas in others (T7 – T11) thereduction was minimal or nonexistent, not differing fromthe control (T12). The viability of this micro-organism isassociated with the different ability to liberate acids into themedium due to lactose degradation as a part of their metab-

olism, producing galactose which can be available for thegrowth of the probiotic cultures, contributing positively tothe maintenance of their viability.

Bi dobacterium animalis count (Table 5) maintained lev-els above 6 log cfu/g for all the trials up to 45 days of refrigerated storage, guaranteeing the amount consideredminimum 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 from6.04 (T3) to 6.93 log cfu/g. This result is of interest, as thevalues were obtained using a minimal concentration of theprobiotic culture and prebiotic ingredient, to the contrary of other studies (Magariños et al. 2007; Ekinci et al. 2008),and suggests a protective effect of the food matrix in thecase of cream cheese in relation to the various extrinsic fac-tors that affect the product, such as the oxygen that perme-ates 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 theviability of probiotics, especially of Bi dobacterium (Daveand Shah 1997; Shah 2000; Kailasapathy 2006). In thisstudy, the maintenance of the pH value above this valuemay have contributed to the elevated survival rate of the

B. animalis.

Lactobacillus acidophilus showed a sharp fall in viabilityduring the period 211 studied (Table 6), reaching valuesbetween 3.10 and 5.4 log cfu/g along 45 days refrigerated

Table 3 Centesimal composition of symbiotic cream cheeses

X 1* X 2** Total solids Fat Protein

T1 0.7 0.5 65.55a 22.24a 7.38cd

T2 0.7 1.5 60.54b 25.16a 7.05e

T3 1.3 0.5 66.56a

21.01a

7.32cde

T4 1.3 1.5 60.86b 26.69a 7.15de

T5 1.5 1.0 65.58a 26.50a 7.37cd

T6 0.5 1.0 65.06a 21.74a 7.10de

T7 1.0 1.7 60.84b 26.40a 7.51bc

T8 1.0 0.3 66.11a 21.27a 7.81a

T9 1.0 1.0 61.03b 25.72a 7.33cde

T10 1.0 1.0 61.07b 26.02a 7.50bc

T11 1.0 1.0 61.14b 26.27a 7.25cde

T12 – – 66.49a 21.11a 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


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storage. Among the possible reasons, we hypothesised thenegative interaction between this probiotic culture and thelactic cultures added (Joseph et al. 1998; Vinderola et al.2002) as well. This hypothesis should be taken into consid-

eration when comparing the S. thermophilus and L. aci-dophilus counts, where the trials containing larger numbersof viable cells in the starter culture (T7, T8, T9, T10 andT11) showed lower probiotic counts during the analyticalperiod. However, it is possible that this interaction is depen-dent on the strain and the food matrix used as the vehiclefor supplementation, as a recent study found no negativeeffects of the starter culture on the viability of L. acidophi-lus 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 inulinon the viability of the probiotics was observed, contrary tothe results of various other studies (Akalin et al. 2007;Cardarelli et al. 2008; Oliveira et al. 2009), reinforcing theneed for prior compatibility between the probiotics and pre-biotics in the food matrix, to provide a positive interaction.This can be observed in trials T7 and T8, in which thesame concentration of probiotics presented similar behav-iour 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 consid-ered as an advantage, as the inulin will only be degraded

in the intestinal tract by the probiotic bacteria, modulatingthe composition of the intestinal ora of the consumer in apositive way. In this context, spite of the limitations of thisstudy, as it was not performed the determination of inulinby 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% tofermented 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 creamcheese has a potential to be used as a food matrix for carry-ing probiotic bacteria and prebiotic ingredients, characteris-ing it as a functional food. Bi dobacterium animalis countsabove 6 log cfu/g were observed in all the treatments, inagreement with the recommendations made in various stud-ies (Shah 2000). With respect to inulin, if the recommendedportions (30 g) of some formulations of cream cheese were

consumed twice a day, this would result in a daily con-sumption of 3 g of inulin, characterising such cheeses asprebiotic foods with respect to the Brazilian regulatory leg-islation (Brasil 2008).

CONCLUSION

Our ndings suggest the potential of cream cheese as anadequate food matrix for supplementation with probioticbacteria and prebiotic ingredient during 45 days of refriger-ated 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 refriger-ated storage towards L. acidophilus, which presentedopposite behaviour.

Further studies should investigate the supplementation andof other probiotic strains as well as other prebiotic ingredi-ents. In addition, descriptive tests aimed to identify relevant sensory descriptors for the optimisation of the formulationshould be also performed.

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Table 6 Viable Lactobacillus acidophilus count of symbiotic creamcheeses along the refrigerated storage

X 1* X 2**

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T1 0.7 0.5 8.00 ª 7.18b 6.26c 4.56d

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with the Tukey Test. X1 = probiotic bacteria concentration (g/kg);

**X2 = prebiotic ingredient concentration (g*100/g). T1, T2,….,

T12 = see Table 1.




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Cream Cheese as a Symbiotic Food Carrier Using Bifidobacterium

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