Assessment of fat content influence over greek yogurt protossymbiotic culture
João Victor Ferreira Campos
1
, Alex Vieira de Oliveira
2
, Mariana Oliveira Silva
3
, Gabriela Leite Ribeiro Amaral Gonzalez
4
, Sabrina
Coimbra Viera Silva
5
, Jéssica Rodrigues Assis de Oliveira
6
, Leonardo Borges Acurcio
7
*
DOI: https://doi.org/10.35699/2447-6218.2021.35899
Abstract
Greek yogurts have high concentrations of proteins and fats, which results in constant increase in their consumption in the
Brazilian market. A product with higher nutritional contents allows it to have greater added value, which generates an
increase in interest on the part of Brazilian dairy industries. This work aimed to evaluate the influence of the high
concentration of lipids and the presence of flavorings over lactic acid bacteria (LAB) count from Greek yogurts of different
brands. Results obtained showed the variation of titratable acidity and LAB count of samples used. Sample T1 showed lower
microbial growth (1x10³ CFU/g) and higher total fat content (6.7%) compared to the others. There was variation between brands
regarding BAL count (p<0.05), showing variation between the different dairy products from different brands sampled.
Regarding presence or absence of flavoring, there was no difference (p>0.05) between the products sampled. Implementation
of a specific legislation for the product would culminate in the standardization and, possibly, improvement in the global quality
of Greek yogurts sold in the country.
Keywords:
Fat. Fermented milk. Lactic acid bacteria.
Avaliação da influência do teor de gordura sobre a cultura protossimbiótica de
iogurte grego
Resumo
Iogurtes grego apresentam concentrações elevadas de proteínas e gorduras o que resulta em um aumento constante de seu
consumo no mercado brasileiro. Um produto com maiores teores nutricionais permite que este tenha maior valor agregado, o
que gera um aumento de interesse por parte dos laticínios brasileiros. Assim, este trabalho objetivou avaliar a influência da
concentração mais alta de lipídeos e a presença de corantes e aromatizantes sob a contagem de bactérias ácido láticas (BAL)
utilizando marcas distintas de iogurte grego. Os resultados obtidos mostraram a va- riação de acidez titulável e crescimento de
BAL das amostras utilizadas. A amostra T1 apresentou menor crescimento microbiano (1x103 UFC/g) e maior teor de gordura
total (6,7%) em comparação às demais. Observou-se variação entre as marcas no que diz respeito à contagem de BAL
(p<0,05), mostrando variação entre os produtos dos distintos laticínios amostrados. No que diz respeito à presença ou não de
corantes e aromatizantes, não se observou diferença
1Centro Universitário de Formiga (UNIFOR-MG) - Formiga, Minas Gerais, Brasil.
https://orcid.org/0000-0003-0902-0000
2Universidade Estadual de Minas Gerais (UEMG) - Cláudio, Minas Gerais, Brasil.
https://orcid.org/0000-0001-5903-5468
3Universidade Federal de Minas Gerais (UFMG) - Belo Horizonte, Minas Gerais, Brasil.
https://orcid.org/0000-0002-0537-1666
4Centro Universitário de Formiga (UNIFOR-MG) - Formiga, Minas Gerais, Brasil.
https://orcid.org/0000-0002-7511-3793
5Centro Universitário de Formiga (UNIFOR-MG) - Formiga, Minas Gerais, Brasil.
https://orcid.org/0000-0002-3181-3237
6Centro Universitário de Formiga (UNIFOR-MG) - Formiga, Minas Gerais, Brasil.
https://orcid.org/0000-0002-2949-8813
7Centro Universitário de Formiga (UNIFOR-MG) - Formiga, Minas Gerais, Brasil.
https://orcid.org/0000-0002-2981-5479
* Corresponding author: leoacurcio@uniformg.edu.br.
Recebido para publicação em 01 de Setembro de 2021. Aceito para publicação 26 de Dezembro de 2021.
e-ISSN: 2447-6218 /
ISSN: 2447-6218. Atribuição CC BY.
2
Acurcio, L. B. et al.
(p>0,05) entre os produtos amostrados. A implementação de uma legislação própria para o produto culminaria na
padronização e, possivelmente, melhora na qualidade global de iogurtes gregos comercializados no país.
Palavras-chave:
Bactérias ácido láticas. Gordura. Leite fermentado.
Introduction
Greek yogurt is one of the several products
available classified as fermented milk. With that said,
according to Brazilian legislation, fermented milk is defined
as a product without the addition of other food substances,
obtained by coagulation and reduction of milk, or
reconstituted milk, pH; added or not by other dairy
products, by lactic fermentation through action of cultures
of specific microorganisms. The same legis- lation defines
yogurt as a product whose fermentation occurs with
protossymbiotic cultures of Streptococcus thermophilus and
Lactobacillus delbrueckii that can be accompanied, in a
complementary way, by other lactic
acid bacteria (Brasil,
2007). However, there is no specific
standard that determines
the composition and quality of Greek yogurt.
(which will suffer the action of proteases and consequent
release of free amino acids) and lipids, the latter being used
only by a small class of microorganisms. In addi- tion,
vitamins and minerals (such as sodium, potassium, calcium
and magnesium) are essential for enzymatic reactions
(Pinto et al., 2019).
Pinto et al. (2019) also report that the presence of
essential oils (such as clove and cinnamon eugenol), of
fruits containing organic acids and essential oils, in addition
to milk substances (such as immunoglobulins, lactoferrins
and lysozymes) may have a delaying and/ or inhibitory
effect on the multiplication of microbiota present in yogurt.
Thus, this work aims to evaluate, at different fat
levels, the growth of lactic acid bacteria (protosymbiotic
culture) in Greek yogurts with different flavors, strawberry
and
traditional.
Bacteria Lactobacillus delbrueckii and Streptococcus
thermophilus are extremely important for the microbial
fermentation of milk to occur, as they are capable of
producing lactic acid. As a result of the production of this
acid, there is a reduction in the pH and coagulation of milk
proteins, determining technological aspects of
yogurt. The
sensory characteristics are due to the junction
of volatile
compounds, namely acids, ketones, alcohols,
esters,
hydrocarbons and aldehydes acquired throughout
the
fermentation process (Dan et al., 2017; Nagaoka, 2019).
Material and methods
In the present study, three different brands of
traditional and strawberry flavored Greek yogurt were used,
totaling six samples, within the expiration date, purchased
from the same supermarket located in the municipality of
Formiga, Minas Gerais. The experiment was carried out at
the Microbiology Laboratory of the Centro Universitário de
Formiga – UNIFOR-MG.
The inclusion of components and techniques,
such
as the addition of powdered milk and/or desorption technique -
which consists of removing whey by centrifu-
gation or cloth
bags - result in an increase in the volume of solids, with
emphasis on proteins and fats, delivering
to Greek yogurt its
known characteristics of firm texture,
full-bodied appearance
and differentiated palatability (Varnam et al., 1995).
The lactic acid bacteria (LAB) count was quan-
tified following the method described by the Internatio- nal
Dairy Federation (IDF, 1988), where Lactobacillus
delbrueckii is a thermophilic microorganism that forms
lenticular colonies of 1mm to 3mm in diameter in De Man,
Rogosa and Sharpe (MRS) medium and Streptococcus
thermophiles, which is a thermophilic microorganism that
forms lenticular colonies with a diameter of 1mm to
2mm.
Decimal serial dilutions of Greek yogurt samples in sterile
saline (0.9% NaCl) were performed. Subsequently, 1ml of each
of the selected dilutions of each sample were
added to sterile
Petri dishes, being overlaid with 20ml of
MRS agar melting
medium, with subsequent incubation,
after solidification of
the medium, at 37ºC for 48 hours, thus executing the pour
plate technique. Results were expressed in colony forming
units - CFU/g.
Addition of cream is one of the techniques for
increasing solids in Greek yogurt, however, studies carried out
by Ramos et al. (2009) concluded that the addition of cream
resulted in lower values in physical characteristics
such as:
reduction of stickiness, firmness and adhesive- ness. This
fact can be explained by interaction of the fat present in
cream with other yogurt components. On the other hand, not
adding cream makes the food matrix,
particularly the protein
fraction, more rigid; which is also
not very desirable.
To determine the titratable acidity, 10ml of yogurt
was
transferred to an Erlenmeyer flask, added with five drops of
1% phenolphthalein solution and titrated with
Microbial multiplication can be directly influenced
according to the availability of water, energy/nitrogen
sources such as sugars/carbohydrates, complex proteins
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Assessment of fat content influence over greek yogurt protossymbiotic culture
N/9 sodium hydroxide solution (alkaline solution known
as
Dornic solution) (Farias et al., 2016).
Results and discussion
The total fat content (g/100g) of each Greek
yogurt sample is described in Tab. 1, from values infor- med
on the packaging of each product. According to Normative
Instruction No. 46, from livestock and agri-
cultural
department (MAPA), whole yogurts must contain
a minimum
of 3.0% of fat content (Brasil, 2007), thus, all samples are
within the parameters recommended by Brazilian legislation.
GraphPad Prism 6.0 program (GraphPad Softwa-
re,
San Diego, California, USA) was used to perform all
statistical analyses. Unpaired t test (or One-Way ANOVA)
and
Turkey’s post-test were used with significance of 5% (p<0.05)
to compare the means of samples of different brands and
flavors.
Values of total fat of each sample were obtained in
their respective packages.
Table 1 – Total fat content of each sample containing 100g
Sample
Commercial
presentation
Fat content (%)
Brand 1
Brand 1
Brand 2
Brand 2
Brand 3
Brand 3
Traditional (T1)
Strawberry (S1)
Traditional (T2)
Strawberry (S2)
Traditional (T3)
Strawberry (S3)
6,7
6,1
4,7
4,6
5
4,2
Estimates indicate that the per capita consump- tion
of yogurt in Brazil presented an increase of 100% compared
to 20 years ago (Barros et al., 2020) which
highlights the
need for a specific legislation for Greek yo- gurts, since the
lack of standardization of its composition
appears to have
great influence on the final product.
It is possible to observe that the T1 sample has the
highest fat content (6.7%) and obtained the lowest BAL
growth in MRS medium (1x103 CFU/g).
Ferreira (2005) states that for an effective growth
of a
dairy culture, the type and quality of the substrate used is of
paramount importance, since fatty solids, in addition to
minerals, will probably influence in culture growth.
Amaral et al. (2016) evaluated physicochemical
compositions of different brands of Greek yogurt and
obtained values that also confirm the influence of com-
position variation between brands regarding titratable
acidity, fat matter and other analyzed parameters.
Studies led by Martinovic et al. (2016) obtained
results regarding the reduction in the count of Lactoba-
cillus sp. and Propionibacterium sp. in semi-hard cheeses
when compared in terms of fat content, where the cheese
with
10% fat content had a reduction of only 1-2 Log10 of CFU/g
while the cheese with 28% of fat content had a
Log
10
reduction
of 2- 3 CFU/g. This fact can be explained
by the fact that low
fat cheese has more water activity (Aw) and, thus, presents
more favorable conditions for microbial growth.
Li et al. (2020) obtained results where different fat
contents in cheeses fermented by Lactobacillus rhamnosus
B10, Streptococcus thermophilus B8, Weissella confused
B14 and Lactobacillus helveticus B6 influenced physical,
chemical and biological parameters. Results found by
Ferreira et al. (2021) were similar regarding the activity of fat
content when performed with yogurts, confirming fat
influence over microbial growth in different dairy matrixes.
Results obtained for titratable acidity (g of lactic
acid/100g of product) are shown in Fig. 2. Following Nor-
mative Instruction No. 46 for fermented milks classified as
yogurt, the recommended titratable acidity standard must be
between 0.6 to 1.5g of ac. lactic/100g (Brasil, 2007). With
that said, it is possible to conclude that two samples are
outside the standard defined by Brazilian legislation.
Total count of lactic acid bacteria present in each
product is shown in Fig. 1. It was possible to observe that
all
samples do not meet the microbiological standard defined
by Normative Instruction No. 46, where it is recommended
that the total count of lactic acid bacteria (CFU/g) should be
at least 1x107 CFU/g (Log10=7) for fermented milks
classified as yogurts (Brasil, 2007).
Based on Fig. 2, it is noteworthy that samples S2
and T3 presented higher values of lactic acid, 1.56
Cad. Ciênc. Agrá., v. 13, p. 01–06, DOI: https://doi.org/10.35699/2447-6218.2021.35899
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Acurcio, L. B. et al.
and 1.66 respectively; values that are out of what is
recommended by legislation.
(lactic acid production) of starter cultures (Nascimento et al.,
2016; Gengatharan et al., 2017). Lima (2011) shows
that
product storage temperature directly influences microbial
multiplication along with metabolic reactions, such as
acidification.
Prolonged storage can generate less stability in
Greek yogurt, mainly in terms of acidity. This statement is
explained due to the continuous fermentation process
Figure 1 – Mean total lactic acid bacteria count (Log10 CFU/g + SD) in MRS agar of Greek yogurts of different brands and
flavors
Caption: SD=standard deviation, T=traditional flavor, M=strawberry flavor. Different numbers indicate different brands. The dashed line shows the minimum
total growth pattern of BAL (7 Log10 CFU/g) defined by legislation.
Studies carried out by Reis et al. (2011) con-
cluded that high concentrations of non-fat solids result in
higher levels of casein, an acidic milk protein, which
consequently generates an increase in the spent amount of
sodium hydroxide (NaOH N/9) during the titration process,
causing the increase in titratable acidity.
On the other hand, ingredients used in the
composition of Greek yogurt that present chemical cha-
racteristics close to pH neutrality are supposed to be an
interference factor in the total acidity parameter in Greek
yogurts (Bezerra et al., 2019).
Figure 2 – Titratable acidity (g of lactic acid/100g of product + SD) from Greek yogurt of different brands and flavors
Caption: SD=standard deviation, T=traditional flavor, M=strawberry flavor, different numbers indicate different brands. The dashed line shows the titratable
acidity standard defined by legislation.
Total growth of BAL and titratable acidity for
traditional and strawberry flavor samples with compari-
son between brands is shown in Fig. 3 and 4. Difference
(p<0.05) between brands 1 and 3 is shown in both para-
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Assessment of fat content influence over greek yogurt protossymbiotic culture
meters analyzed. Brand 2 showed no difference (p>0.05) with
brand 3 in both parameters, as well as no difference
with brand
1 when comparing total growth of lactic acid bacteria
(CFU/g), however, when comparing titratable acidity
results, there was a difference (p<0.05).
with added lactic acid bacteria Lactobacillus acidophilus
LA-5 and Lactobacillus casei CRL-431 resulted in a count of
108 CFU/g of total lactobacilli in low-fat cheeses while non-fat
and reduced fat cheeses had a fall of up to eight
times in the
total count of lactobacilli. This reinforces our
results, where
milk fat can be related to a reduction in lactic acid bacteria
count in a dairy fermented product.
In Fig. 3 we can see that samples from brand 1
(which have higher fat content) presented lowest total count
of lactic acid bacteria (4x103 CFU/g). Samples 2 and 3, on
the other hand, did not show any difference (P>0.05).
Andrade et al. (2015) found different results for
titratable acidity (p<0.05) using fermented dairy products of
different compositions and brands. Costa et al. (2019)
found
similar results (p<0.05) when using sweeteners of different
compositions in yogurt, when compared to traditional
presentations.
Using whole, reduced-fat, and low-fat cheddar
cheeses, Ganesan et al. (2014) concluded that products
Figure 3 – Mean total lactic acid bacteria count (Log10 CFU/g + SD) in MRS agar of Greek yogurts of each brand
Caption: SD = standard deviation. Different numbers indicate different brands. Different letters represent different results (p<0.05) by the One-way ANOVA test
with Turkey post-test.
Figure 4 – Mean total titratable acidity (g of lactic acid/100g product + SD) for Greek yogurt results of each brand.
Caption: SD = standard deviation. Different numbers indicate different brands. Different letters represent different results (p<0.05) by the One-way ANOVA test
with Turkey post-test.
Fig. 5 and 6 show that, based on the total BAL
count and titratable acidity, respectively, there was no
difference when comparing strawberry and traditional
Greek yogurt flavors (p>0.05).
Cad. Ciênc. Agrá., v. 13, p. 01–06, DOI: https://doi.org/10.35699/2447-6218.2021.35899
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Acurcio, L. B. et al.
Barros et al. (2020) obtained different results from
this work, where the difference in flavors of Greek yogurt
(maize starch and pumpkin jelly) resulted in a significant
influence (p<0.05) in the results of titratable acidity.
acidity and other parameters were compared between
samples containing different formulations of sour flavor
(such as citric) addition and samples that did not contain
flavor.
These studies show that each food matrix may
have a different effect over final quality of fermented dairy
products such as yogurts.
Studies evaluated by Junior et al. (2016) also
obtained different results from this work when titratable
Figure 5 – Mean total lactic acid bacteria count (Log10 CFU/g + SD) in MRS agar of Greek yogurt of each flavor
Caption: SD=standard deviation, T=traditional flavor, M=strawberry flavor. Different letters represent different results (p<0.05) by the Unpaired t test ANOVA
test with Turkey post-test.
Figure 6 – Mean total titratable acidity (g of lactic acid/100g of product + SD) for Greek yogurt results for each flavor
Caption: SD=standard deviation, T=traditional flavor, M=strawberry flavor. Different letters represent different results (p<0.05) by the Unpaired t test NOVA
test with Turkey post-test.
Conclusion
tigate the influence of fat content over protossymbiotic
cultures. With this work it is possible to emphasize the
need
to implement a specific legislation for Greek yogurts,
since
different brands have different compositions and different
results regarding legislation requirements.
The sample with the highest fat content showed
lowest count of lactic acid bacteria in Greek yogurt, which
confirms the suspicion on which the study was based.
Further studies are of paramount importance to inves-
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Assessment of fat content influence over greek yogurt protossymbiotic culture
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