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Department of Chemical and Process Engineering, University of Genoa, Via Opera Pia, 15, 16145 Genoa, Italy
Department of Biochemical and Pharmaceutical Technology, So Paulo University, Av. Prof. Lineu Prestes, 580, Bl 16, 05508-900, So Paulo, Brazil
a r t i c l e
i n f o
Article history:
Received 18 July 2012
Accepted 8 September 2012
Keywords:
Yoghurt
Passion fruit ber
Probiotics
Rheology
Microstructure
Sensory
a b s t r a c t
Beyond demonstrated benecial health attributes, passion fruit rinds are a by-product of the fruit pulp industry, rich in total dietary ber, particularly pectin. The aim of this study was to evaluate the inuence of the
addition of passion fruit ber on the whey formation, rheological parameters, microstructure and sensorial
characteristics of probiotic yoghurts. Skim milk bases enriched with 1% of passion fruit ber or not were
heat treated and inoculated with Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus,
and divided into four groups according to the probiotic strain added Lactobacillus acidophilus strains L10
and NCFM and Bidobacterium animalis subsp. lactis strains Bl04 and B94. Fermentations were performed
until the pH reached 4.5. Rheological characteristics of yoghurts were determined by a rotational rheometer
in two cycles of shear rate ranging from 0 to 15 s1 in both upward and downward curves. Sensorial analysis
of passion fruit ber yoghurts, either without any probiotic or co-fermented by L. acidophilus L10 or
B. animalis subsp. lactis Bl04, was evaluated against a control yoghurt without ber. Photomicrographs of
freeze-dried yoghurts were made by eld-emission scanning electron microscope (SEM). Thixotropy of
enriched yoghurts was higher than that of their respective controls in the two cycles of shear rate. Apparent
viscosity was signicantly higher in ber yoghurts co-fermented by the lactobacilli than in their controls at
the end of cold storage. Photomicrographs demonstrated that in passion fruit ber yoghurts the casein gel
was more compact and overlaid the ber, while laments of exopolysaccharides were more frequent in
control yoghurts. Appearance, odor and color of the passion fruit ber yoghurts received scores as good,
and the intensity of the passion fruit avor was considered weak by the sensory assessors. Results indicate
that the passion fruit ber is an almost neutral ingredient for the design of new high value-added yoghurt.
2012 Published by Elsevier Ltd.
1. Introduction
During milk fermentation in yoghurt manufacture, the pH decreases
as the lactic acid is produced by the starter culture Streptococcus
thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. Casein
begins to aggregate at pH 4.7, isoelectric point, forming a fragile gel
net. At the end of fermentation, the gel of the set-type yoghurt is usually
broken to produce stirred yoghurt and the subsequent operations of
mixing, pumping and packaging impact in its structure, decreasing the
apparent viscosity. However, during thawing to approximately 20 C
and cold storage at 45 C, the stirred yoghurt recovers partially its
structure and viscosity, thus behaving as a pseudoplastic material
(Damin, Minowa, Alcantara, & Oliveira, 2008; Marafon, Sumi,
Alcantara, Tamime, & de Oliveira, 2011; Marafon et al., 2011; Sodini,
Remeuf, Haddad, & Corrieu, 2004; Tamime & Robinson, 2007).
Rheological and organoleptic properties, texture characteristics
and microstructure of yoghurt depend on many factors such as milk
Corresponding author. Tel.: +55 1130913690; fax: +55 1138156386.
E-mail address: monolive@usp.br (M.N. Oliveira).
0963-9969/$ see front matter 2012 Published by Elsevier Ltd.
http://dx.doi.org/10.1016/j.foodres.2012.09.012
225
Table 1
Experimental design to study the rheology, spontaneous whey separation, microstructure and sensorial characteristics of probiotic yoghurts enriched with passion fruit
ber.
Yoghurt
Probiotic
Fiber
Control
Control
Control
Control
Passion
Passion
Passion
Passion
+
+
+
+
fruit
fruit
fruit
fruit
ber
ber
ber
ber
226
0 n
where is the shear stress, K the consistency index and n the Power
Law index that describes the ow behavior of the uid as shearthinning/pseudoplastic (n b 1) or shear-thickening/dilatant (n > 1)
(Fischer, Pollard, Erni, Marti, & Padar, 2009). A recent study of our
group demonstrated that major alterations in the texture prole of
PFF yoghurts occur during the rst two weeks of cold storage. Thus,
the rheological characterization of the yoghurts was focused at days
1, 7 and 14.
2.7. Microstructural analyses
Three cups of each yoghurt type were freeze-dried in a lyophilizer
(L4KR 118, BOC Edwards, So Paulo, Brazil) after 1 day of storage at
4 C, as described by Damin, Alcntara, Nunes, and Oliveira (2009).
Afterwards, the samples were stuck on stubs with double-face tape
and coated with 15 nm of a goldpalladium layer applied by a
cathodic coater, E 5100 (Polaron, Hertfordshire, West Sussex, UK).
Six elds of each sample were observed in a eld-emission scanning
electron microscope (SEM) (JSM-7401-F, JEOL, Akishima, Japan), operating at a voltage of 5.0 kV, and photomicrographs were registered
under magnications from 1000 to 10,000. Images were analyzed
using the software Image Pro Plus v.4.5.1 (Media Cybernetics, Silver
Spring, MD, USA) as JPG les, and to three images at 10,000 of magnication of each sample were applied the highest contrast to highlight the pores in the casein network, while the areas of the pores
were marked and measured through a CINAG system of planimetry
(Centro de Informtica na Agricultura, Faculdade de Cincias
Agronmicas, UNESP, Botucatu, Brazil) according to Brito and
Deschamps (2001), and expressed as area of porosity100 1 of area
of yoghurt's gel.
2.8. Sensorial analysis
For the sensorial analysis, were chosen passion fruit ber yoghurts
co-fermented by L. acidophilus L10 and B. animalis subsp. lactis Bl04,
which showed the highest apparent viscosities (app) compared to
their respective controls. Natural control yoghurt and PFF yoghurt
without probiotic were used to evaluate the inuence of PFF and probiotic strain, respectively, on the sensorial perception. In each session,
four samples packed in white cups and identied with random
three-digit codes were served to the untrained assessors (170) in a
227
Table 2
Spontaneous whey separation in yoghurts during 2 weeks of cold storage and their porosity in freeze-dried samples.
Probiotic
Treatment
Day 1
Lactobacillus acidophilus NCFM
L. acidophilus L10
Bidobacterium animalis subsp. lactis Bl04
B. animalis subsp. lactis B94
L. acidophilus NCFM
L. acidophilus L10
B. animalis subsp. lactis Bl04
B. animalis subsp. lactis B94
Control
Control
Control
Control
Passion
Passion
Passion
Passion
Day 7
e
fruit
fruit
fruit
fruit
ber
ber
ber
ber
5.1
4.6
4.2
4.6
0.8
0.0
0.0
0.4
5.0 (0.0)
4.2 (0.15)c
4.2 (0.15)c
4.6 (0.15)d
0.4 (0.1)b
0.0 (0.0)a
0.0 (0.0)a
0.4 (0.1)b
Day 14
e
(0.2)
(0.15)d
(0.15)c
(0.15)d
(0.1)b
(0.0)a
(0.0)a
(0.1)b
5.1
4.6
4.2
4.6
0.8
0.0
0.0
0.4
(0.1)f
(0.15)e
(0.15)d
(0.15)e
(0.1)c
(0.1)a
(0.1)a
(0.1)b
30.5
33.6
30.9
31.2
24.7
22.3
22.1
23.6
(2.8)d
(3.1)ef
(2.7)d
(3.0)de
(1.5)bc
(1.2)a
(1.2)a
(1.4)ab
*Means (N = 32) (standard deviation) with different superscript letters in the same column differ signicantly (P b 0.05).
**Determined on day 1; N = 24.
In the second cycle, the structure recovery ranged from 3.4 to 7.7%
and from 0.5 to 3.3% in PFF and control yoghurts, respectively, being
generally higher in yoghurts supplemented with PFF (Fig. 1).
In the rst cycle of shear rate, the apparent viscosity (app) varied
from 41.5 to 62.7 Pas in control yoghurts and from 44.3 to 91.6 Pas
in PFF yoghurts during the storage period (Fig. 2). All PFF yoghurts increased signicantly their app; however, in general this pattern was
not followed by the control yoghurts (Fig. 2), indicating that the
structure of PFF yoghurts was possibly stabilized by positive interactions between pectins from the fruit and exopolysaccharides produced by the bacteria. On the other hand, in the second cycle of
shear rate, PFF and control yoghurts showed practically the same
mean values of app, which varied from 8.1 to 16.3 Pas in control yoghurts and from 10.2 to 18.4 Pas in PFF yoghurts, respectively
(Fig. 2). The second cycle of shear rate reduced signicantly app in
all yoghurts. However, since PFF yoghurts presented the highest
app in the rst cycle, it is evident, especially after 14 days of cold
storage, that they suffered greater damage in their structure than
the controls, probably because the bers acted as knives, breaking
the proteinprotein interactions during tests, which also reduced
the thixotropy in the second cycle (Figs. 1, 2 and 3).
The decrease in K values (Table 3), combined to the partial structure recovery between the two cycles of shear rate (Fig. 1), indicates
that both control and PFF yoghurts presented shear rate-thinning and
thixotropic properties, which are typical of yoghurts (McCann et al.,
2011; Rawson & Marshall, 1997; Staffolo et al., 2004). Moreover, different rheological behaviors of control and PFF yoghurts may have
been the result of positive interaction of pectin present in PFF with
both protein and exopolysaccharides, hence helping the yoghurts to
partially recover their structure (thixotropy) during the decrease of
shear rate. According to Lucey (2002) and Everett and McLeod
(2005), pectins have demonstrated to interact with the positive
charges on the surface of casein micelles, promoting strengthening
Table 3
Flow behavior of control and passion fruit ber yoghurts predicted by the Power Law model during two weeks of cold storage.
Probiotic
Treatment
Day 1
Control
Control
Control
Control
Passion
Passion
Passion
Passion
fruit
fruit
fruit
fruit
ber
ber
ber
ber
Day 7
Day 14
K1
(Pa s1)
n1
2
(Pa s1)
n2
K1
(Pa s1)
n1
12.15lm
8.10hi
11.49k
0.15bcd
0.30e
0.13bcd
5.01cd
3.52a
4.20ab
0.43fgh
0.56j
0.49ghij
12.40lm
10.75k
11.51klm
9.21j
15.80p
13.83mno
19.02tw
13.16mn
0.20cde
0.08ab
0.17cd
0.09abc
0.08ab
3.88a
4.48bc
4.11ab
4.70bc
3.78a
0.51hij
0.50hij
0.55j
0.49ghij
0.52ij
11.31kl
18.98rst
18.11rs
20.64st
16.47pq
2
(Pa s1)
2
(Pa s1)
n2
K1
(Pa s1)
n1
0.10abcd 5.25cdef
0.17cd
4.85bc
0.24de
5.34e
0.39efg
0.46ghi
0.38defg
14.02no
11.21kl
12.92lmn
0.09abc 5.68efg
0.14bcd 4.87bc
0.11abcd 5.90cd
0.37ef
0.43fgh
0.38defg
0.15bcd
0.09abc
0.08ab
0.07a
0.09abc
0.41fg
0.43fgh
0.48ghi
0.44gh
0.51hij
12.91lmn
23.39x
18.33rs
21.15t
17.87r
0.08ab
0.06a
0.09abc
0.07a
0.08ab
0.36ef
0.43fgh
0.46ghi
0.39efg
0.45ghi
5.21cde
5.83fg
4.86bc
5.58efg
4.96bcd
5.52ef
5.57ef
5.30cde
6.15fg
5.03cde
n2
Means (N = 40) with different superscript letters in the same column differ signicantly (P b 0.05). Abbreviations: K1 and K2 are the consistency index of upward curves of the rst
and the second cycles, respectively; n1 and n2 are the Power Law index that indicates the ow behavior in upward curves of the rst and the second cycle, respectively.
228
35
35
opq
pq
mno
25
no
mn
no
nop
mno
mn
lm
jkl
20
hij
hij
hi
hi
ij
ijk
ij
ghi
15
gh
30
opq
nop
10
pq
30
25
20
15
10
d1
d7
d14
cde
cd
ab
0
def
cde
ab
ab
cde
cde
cd
ab
cd
bc
ab
bc
ab
de
bc
bc
ab
ab
ab
ab
d1
d7
d14
Fig. 1. Thixotropy of control and passion fruit ber yoghurts. Means (N = 40) with different letters are signicantly different (P b 0.05). Abbreviations: NCFM and L10: yoghurts
co-fermented by Lactobacillus acidophilus NCFM and L10, respectively; Bl04 and B94: yoghurts co-fermented by Bidobacterium animalis subsp. lactis Bl04 and B94, respectively.
d1, d7 and d14: samples taken after 1, 7 and 14 days of cold storage after fermentation. Control Passion fruit ber.
Fig. 2. Apparent viscosity (app) at = 2 s1 of control and passion fruit ber yoghurts in the two cycles of upwarddownward curves of shear rate. Means (N = 40) with different
letters are signicantly different (P b 0.05). Abbreviations: NCFM and L10: yoghurts co-fermented by Lactobacillus acidophilus NCFM and L10, respectively; Bl04 and B94: yoghurts
co-fermented by Bidobacterium animalis subsp. lactis Bl04 and B94, respectively. d1, d7 and d14: samples taken after 1, 7 and 14 days of cold storage after fermentation. Control
Passion fruit ber.
229
the area of pores (Table 2) point out that PFF yoghurts had higher density
of the casein network than their respective controls (Pb 0.05), consistent
with a lower number of pores and a higher number of cross-links between strands (Fig. 3a compared to Fig. 3b). In control yoghurts, but
not in PFF yoghurts, exopolysaccharides formed several laments and
covered some areas of the protein gel (Fig. 3b). Also this observation
can be explained by the presence of pectin in PFF, which may have
interacted with proteins and bacterial exopolysaccharides forming a
more compact structure with greater apparent viscosity and ability to entrap the whey phase (Fig. 2, Table 2). The passion fruit ber presented a
needle-shaped blade and was clearly observed in the micrographs
nesting the casein gel and, sometimes, the yoghurt bacteria (Fig. 3c).
3.4. Sensorial characteristics
Results of hedonic tests summarized in Table 4 emphasize that the
four types of yoghurt assayed had no signicant differences among
them (P > 0.05) in the scores of appearance and color, which varied
from 6.6 to 7.0 (like moderately), in spite of the evident light yellowish color of PFF yoghurts.
However, natural yoghurts had higher scores (P b 0.05) for texture
than the PFF ones, which were scored as having a sandy or graininess
mouth feeling by some of the assessors, even though the particle size
of bers was less than 17.7 m. This result can be ascribed not only to
the amount or size of PFF in yoghurts but also to the shape of bers,
which had edges like stones (Fig. 3c) capable of sensitizing the
mouth more than if they had spherical and smooth shape. PFF yoghurts with or without probiotic bacteria received higher mean
scores for odor (neither like nor dislike) than the natural ones (dislike
moderately) (Table 4). Nonetheless, the passion fruit avor was more
intense (P b 0.05) in PFF yoghurts co-fermented by L. acidophilus L10
(3.2) and B. animalis subsp. lactis Bl04 (mean score = 3.3) than in
PFF yoghurt without probiotics (mean score = 2.1). In a previous
study of our group, the pH and total titratable acidity of PFF yoghurts
were not signicantly different from their respective controls
(Esprito-Santo et al., 2012b). Thus, the enhancement of the passion
fruit avor observed in PFF yoghurts co-fermented by L. acidophilus
and B. animalis subsp. lactis is unlikely due to the post-acidication
during storage. Therefore, these probiotic bacteria may have produced or transformed compounds that reinforce the avor of the
Passiora edulis peels which is due, mainly, to esters, 3-methylthiohexan-1-ol, 2-methyl-4-propyl-1, 3-oxathione enantiomers and
edulans I and II (Dhawan, Dhawan, & Sharma, 2004). However, considering only the probiotic yoghurts, the strain of probiotic bacteria
had no signicant effect on odor and passion fruit avor perceived
by the panelists. Similarly, Sendra et al. (2008) observed that probiotic bacteria used in yoghurts supplemented with citrus ber had no inuence on those parameters.
Participants of the sensory panel were familiarized in eating
fruit-avored yoghurt (97.6%), but not to consume natural yoghurt.
These data are in agreement with Ribeiro et al. (2010), who reported
that the Brazilian yoghurt market is dominated by fruit-avored yoghurt (about 95% of the market), and the colorful and sweet yoghurts
are those preferred by the consumers. Therefore, some sensory properties of the natural yoghurt, such as appearance, color, smell and
eps
fb
Table 4
Scores of the sensory evaluation of passion fruit ber yoghurts.
Yoghurt type
Control natural skim yoghurt
PFF yoghurt
PFF yoghurt co-fermented by Lactobacillus acidophilus L10
PFF yoghurt co-fermented by Bidobacterium animalis subsp. lactis Bl04
Appearance
7.03
6.83
6.84
6.74
(1.51)
(1.44)a
(1.45)a
(1.33)a
Color
6.95
6.68
6.67
6.68
Texture
a
(1.59)
(1.39)a
(1.41)a
(1.35)a
7.11
5.52
5.72
5.66
Odor
b
(1.98)
(1.91)a
(1.94)a
(1.74)a
2.27
5.35
5.67
5.62
(1.04)
(1.46)b
(1.65)b
(1.56)b
Mean (N = 170) (standard deviation). Values with different superscript letters in the same column are signicantly different (P b 0.05).
1.25
2.41
3.17
3.29
(0.82) a
(1.83)b
(2.02)c
(2.39)c
230
even the intensity of passion fruit avor may have been underestimated or confused by the assessors, not accustomed to its
characteristics.
Fernndez-Garca and McGregor (1997) reported that the supplementation of yoghurt with oat ber reduced the score for texture, but
the authors refereed to the healthy benets of the new product to
justify its use. Tuorila and Cardello (2002) observed that consumers
are, indeed, more prone to accept off-avors and some unpleasant
characteristics depending on the functional claim of the food product.
Notes attributed to avor, for all enriched yoghurts, revealed a weak
or very weak passion fruit avor, and a minimum, but signicant, inuence on texture, which are important features for the development
of new functional foods, as well as broader possibilities in the formulation of avors.
4. Conclusions
Enriching probiotic yoghurt with passion fruit ber or PFF offered
a scaffold that strengthened the yoghurt's structure, and increases apparent viscosity during storage. In contrast, these bers also act as
cutting blades during shearing, breaking the casein cross-links and
dropping down the apparent viscosity of yoghurts.
The two cycles at low shear rate were effective to discriminate the
rheological behavior of control and enriched PFF yoghurts, minimizing the destructive effect of the analysis during rheological tests in
a rotational rheometer.
SEM micrographs showed that in PFF yoghurts the casein gel overlaid the ber and sometimes was nestled in it, but laments of
exopolysaccharides were more evident in control yoghurts.
The attributes of appearance, odor and color of PFF yoghurts were
considered neutral or good, and the intensity of the passion fruit avor was deemed weak by the sensory assessors.
Results indicate that PFF, when added at a dose of 1 g100 mL 1,
is an almost neutral ingredient and a promising avenue in designing
of new high value-added probiotic yoghurts.
Acknowledgments
The authors wish to thank DuPont Brasil Ltda (Cotia, So Paulo,
Brazil) and Globalfood (So Paulo, Brazil) for providing the cultures,
De Marchi for the donation of passion fruit by-product, Dr. C. Bona
from the Botany Department of Federal University of Paran, Brazil,
for the help with the pore's area analysis, and nally for FAPESP,
CNPq and CAPES for the nancial support.
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