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Article history: Nowadays, important features for the development of new food products include their convenience,
Received 31 July 2014 taste, and ability to promote beneficial effects to human health. This study aimed to develop a potentially
Received in revised form synbiotic dairy-based tomato spread and to evaluate the viability of the microorganisms employed, as
22 November 2014
well as the sensory acceptability of the product throughout its storage for 28 days. Three different trials
Accepted 12 December 2014
Available online 19 December 2014
were studied, all containing the prebiotic inulin and the starter culture Streptococcus thermophilus ST-M6:
T1 (control); T2 with the probiotic strains Lactobacillus acidophilus NCFM and Bifidobacterium animalis
subsp. lactis Bb-12, and T3 with Bb-12 and the bacteriocinogenic and potentially probiotic strain
Keywords:
Probiotic
Lactobacillus sakei subsp. sakei 2a. The product was stored at 4 C and analysed after 1, 7, 14, 21, and 28
Inulin days of storage. For all trials, the pH decreased throughout storage, the viability of all strains was high
Lactobacillus (7.9 log cfu/g), and sensory evaluation with consumers showed mean scores above 7 during the storage
Bifidobacterium period evaluated (up to 21 days), which demonstrates the product has potential as a functional food.
Dairy-based spread © 2014 Elsevier Ltd. All rights reserved.
1. Introduction the harsh conditions found in the GIT, helping to maintain high cell
viability rates (Cruz, Buriti, Souza, Faria, & Saad, 2009). Tomato
The recent trend in the development of new food products is (Lycopersicon esculentum) is an interesting natural ingredient to be
their convenience, taste, and human health promoting function- added to a dairy-based product. It contains different antioxidants,
ality. A functional synbiotic product combines probiotic and pre- including lycopene, b-carotene, and vitamin C. Lycopene has been
biotic ingredients, which may improve the gastrointestinal tract shown to be useful to prevent different types of cancer by reducing
(GIT) function. Probiotics are defined as live microorganisms, which the side effects of free radicals and unstable molecules, which could
when administered in adequate amounts confer a health benefit on damage the body's healthy cells (Lugasi, Ho va
ri, Biro
, Brandt, &
the host (FAO/WHO, 2001). Prebiotics are selectively fermented Helyes, 2004).
ingredients that promote specific changes in the composition and/ Some probiotic and non-probiotic lactic acid bacteria (LAB)
or activity of the GIT microbiota and confer benefits to the host strains are able to produce antimicrobial compounds, known as
(Gibson, Probert, Van Loo, Rastall, & Roberfroid, 2004). bacteriocins (Nishie, Nagao, & Sonomoto, 2012). Bacteriocins are
Lactobacillus acidophilus NCFM and Bifidobacterium animalis ribosomally synthesized antimicrobial peptides and a promising
subsp. lactis Bb-12 are commercial probiotic cultures used in a va- technological alternative for preventing the growth of spoilage and
riety of food products and dietetic supplements. Dairy products are pathogenic microorganisms in foods, a process called bio-
considered good vehicles for probiotics delivery and, among them preservation (Snyder & Worobo, 2014). Lactobacillus sakei subsp.
cheese is the most appropriate product, due to its buffering ability. sakei 2a is an aerotolerant LAB isolated from a Brazilian fresh
In general, cheeses show higher pH when compared to fermented sausage (De Martinis & Franco, 1998) and there is only one study
milks and, therefore, are able to protect the microorganisms against available in the scientific literature about its application in a dairy
product (Villarreal et al., 2013). Lb. sakei subsp. sakei 2a is able to
produce bacteriocins (Carvalho et al., 2010) and its probiotic po-
* Corresponding author. Tel.: þ55 11 3091 2378; fax: þ55 11 3815 6386. tential was shown in gnotobiotic mice challenged with the food-
E-mail address: susaad@usp.br (S.M.I. Saad). borne pathogen Listeria monocytogenes (Bambirra et al., 2007).
http://dx.doi.org/10.1016/j.lwt.2014.12.030
0023-6438/© 2014 Elsevier Ltd. All rights reserved.
C.D. Staliano et al. / LWT - Food Science and Technology 62 (2015) 682e688 683
Therefore, this study aimed to develop a particularly innovative cheese; salt; olive oil; commercial sucrose; stabilisers guar gum,
synbiotic dairy-based tomato spread and to evaluate the viability of xantan gum, carrageenan gum, prebiotic fibre inulin, and the whey
the microorganisms employed, as well as the sensory acceptability obtained during cheese production. After the mixture step, a
of the product throughout its refrigerated storage for up to 28 days. smooth salmon cream was formed. Samples containing approxi-
mately 40 g of the food product were packaged in individual plastic
2. Material and methods pots for food products (68 mm diameter, 32 mm high, 55 mL total
volume, Tries Aditivos Pl ~o Paulo, Brazil). The plastic pots
asticos, Sa
2.1. Experimental design and microbial cultures were sealed with aluminium covers, and stored at 4 ± 1 C for up to
28 days. Table 2 shows the dairy-based spread overall formulation.
Experimental design was randomized and consisted of three
combinations (trials) (Table 1). Every trial was manufactured as 2.3. Determination of pH
three repetitions (triplicates) and samples from the food product
were obtained at 1, 7, 14, 21, and 28 days of storage for further The pH values of the dairy-based tomato spreads were deter-
analysis. mined for triplicate samples with a Thermo Orion Three Stars pH
The strains Streptococcus thermophilus ST-M6, B. animalis subsp. metre (Thermofisher Scientific, Waltham, MA, USA) equipped with
lactis Bb-12 (Christian Hansen, Hoersholm, Denmark), and Lb. aci- a penetration electrode model 2AO4 (Analyser, Sa ~o Paulo, Brazil)
dophilus NCFM (Danisco, Dange , France) used in the present study after 1, 7, 14, 21, and 28 days of storage at 4 ± 1 C and also during
consisted of freeze-dried commercial cultures powders for direct the steps of the quark cheese preparation.
vat inoculation (DVS) and were added at 0.01 g/100 mL, 0.03 g/
100 mL, and 0.05 g/100 mL, respectively. Lb. sakei subsp. sakei 2a
2.4. Microbiological analysis
was kept in De Man Rogosa Sharpe (MRS) broth (Oxoid, Basing-
stoke, UK) added of glycerol (20 mL/100 mL) and stored at e 80 C.
Microbial counts of Lb. acidophilus NCFM, B. animalis subsp. lactis
The microorganism was grown in MRS broth at 30 C for 24 h, re-
Bb-12, Lb. sakei subsp. sakei 2a, and St. thermophilus were con-
cultivated (inoculum of 4 mL/100 mL) at 30 C for approximately
ducted throughout the food product storage (after 1, 7, 14, 21, and
16 h, centrifuged (5000 g for 10 min) and finally washed twice
28 days) for all trials. For the microbiological analysis, portions of
(NaCl 0.9 g/100 mL) to obtain the pellet. This washed pellet was
25 g of the food product were transferred to aseptic bags (Nasco,
inoculated directly in the 18 L of milk employed for the cheese
Whirl-Pak®, USA), added of 225 mL of 0.1 g/100 mL peptone (Oxoid)
production.
water, blended in a Bag Mixer 400 device (Interscience, St. Nom,
France), and then submitted to further ten-fold serial dilutions
2.2. Dairy-based tomato spread production using the same diluent.
St. thermophilus ST-M6 was counted by pour-plating 1 mL of
Quark cheese was produced with 18 L of skimmed pasteurised each dilution in agar M17 (Oxoid) supplemented with 10 g/100 mL
milk (Salute, Descalvado, Brazil; high temperature short time of lactose (Oxoid), followed by aerobic incubation at 37 C for 48 h
[HTST] process), which was heated to 37e38 C and inoculated (Richter & Vedamuthu, 2001). Lb. acidophilus NCFM was enumer-
with the appropriate microbial cultures, according to the experi- ated by pour-plating 1 mL of each dilution in formulated MRS agar,
mental design shown in Table 1 and described above. Next, calcium modified by the replacement of glucose by maltose, followed by
chloride (0.25 g/L) was added in all trials. As soon as the pH reached aerobic incubation at 37 C for 48 h (International Dairy Federation,
values in the range of 6.3e6.5, commercial rennet Ha-la (100% 1995). B. animalis subsp. lactis Bb-12 populations were determined
chymosin identical to the bovine enzyme; Christian Hansen, by pour-plating 1 mL of each dilution in MRS agar (Oxoid)
Valinhos, Brazil; 5 mg/L) was added to the cheese-milk, which was
allowed to set again for approximately 1 h, until a curd was formed
and the pH reached values between 5.6 and 5.8. The gel formed was Table 2
cut into cubes (20 20 20 mm), placed in sterilised cotton Ingredients and formulation of the dairy-based spreads studied.
cheesecloth, and allowed to drain at 15 C for 15 h. After draining, Ingredients Amount (g/100 g)
the cheese-base was placed in sterilised beakers, covered with a
1. Quark cheese 50.00
PVC film and stored at 4 ± 1 C, until the final mixture took place. 2. Tomato pulp 14.00
For the final mixture, an industrial blender (Lucre, Catanduva, 3. Milk cream 13.00
Brazil, 15 L capacity) was employed for mixing the following in- 4. Dried tomato 11.00
5. Inulin 4.00
gredients: quark cheese; pasteurized tomato pulp; dried tomato;
6. Whey 2.60
commercial sterilized milk cream; dried basil; grated parmesan 7. Parmesan cheese 1.51
8. Olive oil 1.50
9. Sugar 1.00
Table 1 10. Salt 0.80
Description of the three different trials (T1, T2, and T3) of the dairy-based tomato 11. Guar gum 0.22
spread studied, according to the microbial cultures employed. 12. Basil 0.15
13. Xantan gum 0.11
Trials St. thermophilus B. animalis subsp. Lb. acidophilus Lb. sakei subsp.
14. Carrageenan gum 0.11
ST-M6a lactis Bb-12b NCFMc sakei 2ad
Total 100.00
T1* þ e e e
2. Pasteurized tomato pulp (5.8 Brix, Pomodoro, Goia ^nia, Brazil); 3.
T2 þ þ þ e
Commercial sterilized milk cream (25% lipids, Nestle , Araçatuba, Brazil);
T3 þ þ e þ
4. Dried tomato (Agro Industrial Itaguaçú, Itaguaçú da Bahia, Brazil); 5.
*
control; þ ¼ addition; - ¼ no addition. Prebiotic inulin (GR, Orafti, Oreye, Belgium); 7. Grated parmesan cheese
a
Streptococcus thermophilus ST-M6 (Christian Hansen, Hoersholm, Denmark). (Faixa Azul, Vigor, S~ ao Paulo, Brazil); 8. Olive oil (Gallo, Mairinque,
b
Bifidobacterium animalis subsp. lactis Bb-12 (Christian Hansen). Brazil); 9. Commercial sucrose (Uni~ ao, Limeira, Brazil); 10. Salt (Cisne,
c
Lactobacillus acidophilus NCFM (Danisco, Dange , France). Cabo Frio, Brazil); 11. Guar gum (Grindsted® 250, Danisco, Cotia, Brazil);
d
Lactobacillus sakei subsp. sakei 2a (Laboratory of Food Microbiology, School of 12. Dried basil (Fuchs, Itupeva, Brazil); 13. Xantan gum (Grindsted® 80,
Pharmaceutical Sciences/University of Sa ~o Paulo, Sa
~o Paulo, Brazil). Danisco), and 14. Carrageenan gum (Grindsted® CY500, Danisco).
684 C.D. Staliano et al. / LWT - Food Science and Technology 62 (2015) 682e688
Table 4 8e9 log cfu/mL, and also displayed high acid production,
Viability (mean values shown as log cfu/g ± standard deviation) of St. thermophilus decreasing the pH. Yoon, Woodams, and Hang (2004) studied to-
ST-M6, Lb. acidophilus NCFM, B. animalis subsp. lactis Bb-12, and Lb. sakei subsp. sakei
2a throughout storage (4 ± 1 C) assessed for the different trials of the dairy-based
mato juice fermented with Lb. acidophilus LA39 at 30 C for 72 h and
spreads evaluated (see Table 1 for description of trials T1eT3). then stored at 4 C for four weeks. The authors reported high counts
and a fast growth rate of Lb. acidophilus, achieving 9 log cfu/g and
Microorganism Time Populations of microorganisms (log cfu/g)
(days)
remaining stable, being able to survive under the adverse condi-
Trials tions of low pH and high acidity.
T1 T2 T3 Even though tomato was shown to positively influence the
St. thermophilus 1 9.35 ± 0.05Aa 9.12 ± 0.13Ba 9.17 ± 0.10Ba viability of microorganisms in the current study, different out-
ST-M6 7 9.22 ± 0.07Aab 9.21 ± 0.17Aa 9.26 ± 0.09Aa comes were observed for other vegetable-origin ingredients in
14 9.12 ± 0.07ABab 9.07 ± 0.11Ba 9.20 ± 0.13Aa probiotic products. Espírito Santo, Perego, Converti, and Oliveira
21 9.03 ± 0.18Bab 9.04 ± 0.24Ba 9.26 ± 0.17Aa (2012) added passion fruit peel powder in skim yoghurt supple-
28 8.95 ± 0.36Bb 9.00 ± 0.50Ba 9.24 ± 0.09Aa
Lb. acidophilus 1 e 8.50 ± 0.16ab e
mented with Lb. acidophilus NCFM. The authors observed that the
NCFM 7 e 8.61 ± 0.23a e passion fruit led to an inhibitory effect of the probiotic strain, since
14 e 8.30 ± 0.36ab e populations were significantly reduced throughout 28 days of
21 e 8.16 ± 0.46ab e storage. Also, in a study with milk-based mousses (Buriti, Komatsu,
28 e 7.93 ± 0.93b e
& Saad, 2007b), the addition of passion fruit as concentrated juice
B. animalis subsp. 1 e 8.43 ± 0.19Ba 8.62 ± 0.11Aa
lactis Bb-12 7 e 8.41 ± 0.04Bab 8.60 ± 0.16Aa or pasteurized frozen pulp reduced Lb. acidophilus La-5 viability in
14 e 8.34 ± 0.06Babc 8.56 ± 0.09Aa 4.7 log cycles after 21 days of storage at 4 C. Different results were
21 e 8.25 ± 0.07Bc 8.58 ± 0.06Aa reported for fermented soy products, in which the addition of
28 e 8.26 ± 0.11Bbc 8.54 ± 0.12Aa mango and guava pulps did not affect Lb. acidophilus La-5 and
Lb. sakei subsp. 1 e e 8.18 ± 0.20a
Bifidobacterium Bb-12 viability (Bedani, Vieira, Rossi, & Saad, 2014).
sakei 2a 7 e e 8.17 ± 0.20a
14 e e 8.10 ± 0.14a Lb. acidophilus NCFM and Lb. sakei 2a showed high and stable
21 e e 8.16 ± 0.08a viability in the dairy matrix studied throughout storage of T2 and
28 e e 8.11 ± 0.11a T3, respectively. Both LAB displayed a good interaction with the
A,B
Superscript capital letters, in a line, mean significant differences (P < 0.05) among probiotic strain Bb-12, as observed by the high counts of the
trials for a same day studied. microorganism (around 8 log cfu/g).
a,b,c
Superscript lower case letters, in a column, mean significant differences The pH values determined in T2 were statistically lower
(P < 0.05) among days for the same trial and microorganism evaluated.
(P < 0.05) than those assessed for T3 and T1 (Table 3), probably due
to the higher ability of NCFM to degrade lactose present in milk into
lactic acid. In reality, Lb. sakei strains are frequently used as starter
life (ANVISA, 2008). It is worthy to mention that, for similar types of cultures in fermented meat products, including sausages, due to
spread, Brazilian standards recommend a daily serving portion of their ability to quickly ferment carbohydrates (Champomier-
10 g (ANVISA, 2003). Therefore, the tomato-based dairy spread was Verge s, Chaillou, Cornet, & Zagorec, 2001). Lb. sakei 2a is a poten-
shown to be a good vehicle for the delivery of LAB and Bb-12. tially probiotic strain that was originally isolated from a meat
St. thermophilus easily adapted to the dairy product, since it is a product with very different intrinsic characteristics. However, we
homofermentative LAB commonly used as starter culture in yo- can clearly infer that the microorganism showed a good adaptation
ghurts (together with Lb. delbrueckii subsp. bulgaricus) and fer- to the dairy food matrix tested. Likely, the promising results ob-
mented milk (Saad, Komatsu, Granato, Branco, & Buriti, 2011). The tained from this study suggest that the microorganism could also
addition of St. thermophilus ST-M6 was an interesting approach, be applied as a starter culture in fermented dairy products. Even
since it remained viable during the product storage and it is
required for milk acidification to promote coagulation through the
action of chymosin on the k-casein steric stabilizing layer of the
casein micellae, which is needed to obtain cheese (Cruz et al.,
2009).
There are many studies using St. thermophilus as a starter culture
and supplemented with probiotics. Among them, Buriti, Cardarelli,
and Saad (2007) used St. thermophilus in co-culture with Lb. para-
casei to produce potentially probiotic and synbiotic fresh cream
cheeses. The authors reported St. thermophilus populations above
9.5 log cfu/g for both kinds of cheeses during storage for up to 21
days. In another study, St. thermophilus and Lb. acidophilus NCFM
were added in co-culture in yoghurt stored during 28 days at 4 C,
and the authors observed an adequate probiotic viability
(0.5 log cfu/g reduction) (Ng, Yeung, & Tong, 2011).
As shown by our data, it is important to stress out that the as-
sociation of milk and tomato in the dairy-based spread was bene-
ficial for an adequate adaptation and high viability rates of Lb.
acidophilus NCFM. Similarly, some studies have also demonstrated a
positive adaptation of Lactobacillus spp., particularly Lb. acidophilus,
to the dairy matrix of food products with tomato. Babu, Mital, and
Grag (1992) evaluated the addition of tomato juice in skimmed
Fig. 1. Sensory scores attributed by female ( ) and male ( ) consumers for the
milk inoculated with different strains of L. acidophilus. After incu- different trials of the dairy-based tomato spreads stored for 7, 14, and 21 days at
bation at 37 C for 16e18 h, the authors observed that the micro- 4 ± 1 C. Bars mean the average values given by each gender displaying two units of
organism was able to grow, exhibiting final populations of standard deviation (see Table 1 for description of trials T1eT3).
686 C.D. Staliano et al. / LWT - Food Science and Technology 62 (2015) 682e688
though Lb sakei 2a is believed to produce bacteriocins in the food determined during the dairy product storage period, as observed by
matrix tested, which apparently did not affect the high viability of Oliveira, Perego, Oliveira, and Converti (2011). The authors
ST-M6 and Bb-12 throughout storage, a more detailed inquiry is demonstrated that the supplementation of inulin in skimmed milk
currently being undertaken in our laboratory to verify this fermented with a cocktail containing Lb. acidophilus, Lb. rhamnosus,
possibility. Lb. bulgaricus, Bifidobacterium lactis, and St. thermophilus led to
Several studies evaluated the use of Lactobacillus in co-culture significantly lower (17e48%) generation times compared to those
with Bifidobacterium in food systems. Pereira, Souza, Behrens, and obtained in pure skim milk. The authors attributed these results to
Saad (2010) added Lb. acidophilus La-5 and B. animalis subsp. lac- a positive prebiotic effect, which improved the probiotic strains
tis BL04 to petit-suisse cheese formulations and observed pop- growth rates.
ulations above, respectively, 7 log cfu/g and 8 log cfu/g, throughout
28 days of refrigerated storage. As demonstrated in the present 3.3. Sensory evaluation of the dairy-based tomato spreads during
study, Bb-12 viability was also high (Table 4) in T2 and T3. storage
Even though all the products in this study included the prebiotic
fibre inulin in their formulation, it is possible that the compound In the present study, an affective sensory test was included to
contributed for the high viability of the microbial populations determine if consumers liked or not (and at what intensity) the
A 45.0%
40.0%
35.0%
30.0%
Frequency
25.0%
20.0%
15.0%
10.0%
5.0%
0.0%
1 2 3 4 5 6 7 8 9
Scores
B 45.0%
40.0%
35.0%
30.0%
Frequency
25.0%
20.0%
15.0%
10.0%
5.0%
0.0%
1 2 3 4 5 6 7 8 9
Scores
C 45.0%
40.0%
35.0%
30.0%
Frequency
25.0%
20.0%
15.0%
10.0%
5.0%
0.0%
1 2 3 4 5 6 7 8 9
Fig. 2. Frequency (expressed as percentage) of scores (ranging from 1 to 9) attributed by consumers for the different trials ( ) of the dairy-based tomato spreads stored
for 7 (A), 14 (B), and 21 (C) days at 4 ± 1 C (see Table 1 for description of trials T1eT3).
C.D. Staliano et al. / LWT - Food Science and Technology 62 (2015) 682e688 687
innovative food product developed. According to Cruz, Cadena, (present in the dried tomato and in tomato pulp added as in-
Farias, and Bolini (2011), this is considered a chief assessment in gredients) was technologically feasible and exhibited high viability
order to determine the potential for commercialization of new food results for the beneficial microorganisms Lb. acidophilus NCFM and
products supplemented with pro- and/or prebiotics, which is the Bb-12 during the entire period of storage tested. Additionally, Lb.
case of our potentially synbiotic dairy-based tomato spread. sakei subsp. sakei 2a, a bacteriocinogenic and potentially probiotic
Fig. 1 summarizes the results obtained for the sensory accept- strain, showed high counts throughout the product storage and
ability test conducted for T1, T2, and T3. The mean overall scores could, therefore, be adequately incorporated into the product dairy
were given by different genders of consumers, of which 55.26% matrix. Sensory evaluation revealed mean scores higher than 7
were women and 44.74% men. There was not a significant differ- (liked regularly) for all trials, which demonstrated the product was
ence (P > 0.05) among the scores given by the consumers for any well accepted by consumers. Moreover, future researches should be
product during the different periods evaluated for the three trials. done in order to investigate the synbiotic potential of the product
The mean scores attributed for the samples ranged from 6.04 through in vitro tests and clinical trials.
(minimum value given by a male consumer for T1 on day 14) to 8.30
(maximum rate given by a male consumer for T2 on day 14). Also, Acknowledgements
there was not a remarkable difference between the minimum and
the maximum average scores judged by the consumers, which is a The authors thank “Fundaç~ ao de Amparo a Pesquisa do Estado
positive outcome and demonstrates that the sensory characteristics de Sa~o Paulo” (FAPESP) (Projects # 2009/13347-3, 2009/52600-6,
of the dairy-based tomato spread were satisfactory. The mean and 2010/52267-2) and “Coordenaça ~o de Aperfeiçoamento de
scores for all samples were higher among the female consumers in Pessoal de Nível Superior” (CAPES) for financial support and fel-
seven out of nine sections, in comparison with those given by the lowships. The authors also thank Danisco, Orafti, and Salute com-
male consumers; however, no significant difference (P > 0.05) was panies for the donation of some material sources, and Prof.
observed among them. The mean scores were at least 7 (liked Bernadette D. G. M. Franco for providing the Lb. sakei subsp. sakei 2a
regularly) considering all trials, with a high frequency of scores 7, 8, strain.
and 9 (Fig. 2), which demonstrates that the innovative product was
well accepted by consumers since the product global impression References
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