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Article history:
Received 22 January 2016
Received in revised form
25 May 2016
Accepted 28 June 2016
Available online 29 June 2016
The use of edible coatings and lms formulated with bioactive compounds in food products in order to
convey new functionalities or extend shelf-life opens new possibilities as a carrier for functional lactic
acid bacteria. In this work the main objective was to study the stability of probiotic microorganisms, viz.
Bidobacterium animalis Bb-12 and Lactobacillus casei-01, in edible lm formulations based on whey
protein isolate (WPI).
The results demonstrated a loss of bacterial cell viability of ca. 3 log cycles (reaching 106 CFU/g lm)
until 60 d at both 23 and 4 C, noting that the most marked decrease was at 23 C for both strains.
Bidobacterium animalis Bb-12 remained viable for a longer period of time and with less decrease in its
cell numbers (108 CFU/g lm).
Physical properties, namely color, water activity, thickness, youngs modulus, tensile strength, elongation at break and the molecular structure of WPI lms were maintained stable throughout the storage
period at both temperatures tested.
Edible lms incorporated with probiotics can be good carriers for these to be ingested together with
food products.
2016 Elsevier Ltd. All rights reserved.
Keywords:
Edible coatings/lms
Whey protein isolate
Lactic acid bateria
Bidobacterium
Lactobacillus
1. Introduction
Edible coatings and lms are natural polymers used to retain the
appearance and physicochemical properties of foods during storage. When adsorbed on the surface of the food, they may promote
protection against moisture migration or oxidation and control of
microbial growth (Han, 2000; Naushad & Stading, 2007).
Several reviews have demonstrated that edible lms can be
prepared from different structural materials such as lipids
(Hambleton, Debeaufort, Bonnotte, & Voilley, 2009), polynez, Fabra, Talens, & Chiralt, 2013; Jridi et al.,
saccharides (Jime
2014) and proteins (Ramos, Fernandes, Silva, Pintado, & Malcata,
2011; Ramos et al., 2013; Ramos et al., 2012) or by combining two
or several of these compounds. Protein based lms have received
considerable attention because they have advantages over others,
in particular, due to their mechanical properties that are generally
better since proteins have a distinctive structure, which confers a
wider range of functional properties, (Cuq, Gontard, & Guilbert,
1995; Gennadios & Weller, 1990; Wittaya, 2012).
Edible packaging systems mainly deal with maintaining or
* Corresponding author.
E-mail address: mpintado@porto.ucp.pt (M. Pintado).
http://dx.doi.org/10.1016/j.lwt.2016.06.060
0023-6438/ 2016 Elsevier Ltd. All rights reserved.
544
J. Odila Pereira et al. / LWT - Food Science and Technology 73 (2016) 543e550
Table 1
Viable cell numbers (Log CFU/g) of B. animalis Bb-12 and L. casei-01 incorporated in whey protein based lms stored under vacuum for 60 days at 23 1 C and 4 1 C.
23 C
4 C
B. animalis Bb-12
Film-forming solutions
0 days
3 days
5 days
10 days
40 days
60 days
Note:
a, b, c, d, e, f
9.06
8.98
8.81
7.90
7.17
6.66
6.09
0.03
0.01a
0.04b
0.01c
0.01d
0.01e
0.02f
L. casei-01
9.07
8.93
8.53
7.43
6.53
6.40
5.98
0.03
0.04a
0.04b
0.04c
0.05d
0.02e
0.01f
B. animalis Bb-12
9.06
8.94
8.64
8.56
8.41
8.07
7.90
0.03
0.03a
0.03b
0.03c
0.03d
0.04e
0.01f
Means within the same columns, labeled with the same letter, do not statistically differ from each other (p > 0.05).
L. casei-01
9.07
8.93
8.55
8.34
8.75
7.17
6.95
0.03
0.04a
0.03b
0.02c
0.02d
0.03e
0.01f
Table 2
Evolution of thickness (mm) and water activity (Aw) of control and probiotic lms incorporated with B. animalis Bb-12 and L. casei-01 during storage for 60 days at 23 1 C
(a) and 4 1 C (b).
B. animalis Bb-12
Control
Thickness (mm)
a)
0 days
3 days
5 days
10 days
40 days
60 days
b)
0 days
3 days
5 days
10 days
40 days
60 days
Note:
L. casei-01
Thickness (mm)
aw
aw
Thickness (mm)
aw
0.396
0.395
0.400
0.399
0.397
0.397
0.006a
0.003a
0.007a
0.008a
0.008a
0.001a
0.578
0.577
0.575
0.576
0.577
0.576
0.004a
0.003a
0.001a
0.001a
0.001a
0.001a
0.408
0.407
0.408
0.405
0.409
0.408
0.006a
0.001a
0.001a
0.002a
0.001a
0.003a
0.637
0.637
0.638
0.637
0.637
0.637
0.001b
0.001b
0.001b
0.002b
0.001b
0.001b
0.395
0.395
0.396
0.396
0.397
0.395
0.001a
0.001a
0.001a
0.002a
0.007a
0.002a
0.738
0.738
0.737
0.736
0.738
0.737
0.001c
0.002c
0.001c
0.003c
0.001c
0.001c
0.405
0.406
0.404
0.404
0.402
0.403
0.001a
0.001a
0.000a
0.001a
0.000a
0.001a
0.589
0.588
0.590
0.588
0.589
0.589
0.002a
0.002a
0.003a
0.001a
0.001a
0.001a
0.410
0.408
0.410
0.409
0.410
0.410
0.001a
0.000a
0.001a
0.001a
0.002a
0.001a
0.551
0.550
0.550
0.551
0.551
0.549
0.001b
0.001b
0.002b
0.001b
0.001b
0.003b
0.399
0.400
0.400
0.398
0.399
0.397
0.001a
0.002a
0.001a
0.001a
0.000a
0.002a
0.570
0.570
0.571
0.570
0.570
0.570
0.001c
0.002c
0.001c
0.001c
0.001c
0.000c
a, b, c
, Means within the same columns, labeled with the same letter, do not statistically differ from each other (p > 0.05).
DE
Lfilm Lstandard
2
2
afilm astandard
2 1=2
bfilm bstandard
For each condition, four samples were measuredeand, on each
lm disk, four readings were made on each side.
(1)
0.05a
0.05a
0.01a
0.02a
0.02a
0.00a
16.75
16.73
16.75
16.72
16.72
16.71
0.05a
0.06a
0.01a
0.02a
0.02a
0.01a
17.45
17.44
17.46
17.43
17.43
17.42
0.01c
0.01c
0.01c
0.01c
0.01c
0.00c
0.53
0.53
0.53
0.51
0.53
0.53
0.01c
0.01c
0.01c
0.01c
0.01c
0.01c
92.74
92.75
92.75
92.75
92.75
92.75
0.01b
0.15b
0.14b
0.08b
0.05b
0.04b
18.77
18.90
18.92
18.85
18.83
18.88
Note:
a, b, c
, Means within the same columns, labeled with the same letter, do not statistically differ from each other (p > 0.05).
0.04b
0.21b
0.14b
0.08b
0.04b
0.03b
18.97
19.10
19.11
19.05
19.04
19.10
0.02b
0.01b
0.01b
0.01b
0.01b
0.01b
0.61
0.59
0.59
0.59
0.59
0.59
0.06b
0.12b
0.01b
0.01b
0.02b
0.03b
90.93
90.92
90.88
90.93
90.95
90.97
0.00a
0.04a
0.01a
0.00a
0.00a
0.00a
17.00
17.00
16.99
17.00
17.00
17.01
0.01a
0.03a
0.01a
0.01a
0.01a
0.01a
17.39
17.38
17.38
17.39
17.39
17.39
0.00a
0.00a
0.01a
0.01a
0.01a
0.01a
0.75
0.76
0.75
0.76
0.76
0.76
0.02a
0.03a
0.01a
0.02a
0.01a
0.03a
91.78
91.78
91.78
91.78
91.79
91.77
15.28
15.29
15.31
15.30
15.30
15.30
0.94
0.94
0.96
0.94
0.94
0.92
0.16a
0.18a
0.09a
0.11a
0.03a
0.01a
a)
23 C
0 days
3 days
5 days
10 days
40 days
60 days
b)
4 C
0 days
3 days
5 days
10 days
40 days
60 days
91.11
91.33
91.38
91.34
91.34
91.36
0.01a
0.01a
0.00a
0.01a
0.01a
0.00a
19.31
19.35
19.36
19.36
19.39
19.51
0.08a
0.26a
0.06a
0.06a
0.03a
0.02a
19.05
19.04
19.00
19.03
19.04
19.15
0.02a
0.18a
0.09a
0.01a
0.01a
0.01a
93.66
93.63
93.64
93.63
93.62
93.61
0.04b
0.03b
0.02b
0.03b
0.01b
0.01b
0.75
0.76
0.71
0.73
0.73
0.75
0.02b
0.01b
0.01b
0.02b
0.00b
0.00b
16.56
16.60
16.59
16.61
16.61
16.59
0.02b
0.03b
0.01b
0.02b
0.01b
0.01b
15.65
15.69
15.67
15.70
15.70
15.69
0.01b
0.02b
0.02b
0.03b
0.01b
0.00b
93.57
93.58
93.61
93.59
93.57
93.55
0.03b
0.09b
0.01b
0.01b
0.03b
0.02b
0.68
0.66
0.63
0.65
0.66
0.64
0.01c
0.01c
0.01c
0.01c
0.01c
0.01c
16.17
16.17
16.21
16.19
16.18
16.16
0.00b
0.05b
0.01b
0.01b
0.02b
0.01b
DE
b*
a*
L*
L. casei-01
DE
b*
a*
L*
DE
b
B. animalis Bb-12
Film morphology was evaluated by Scanning Electron Microscopy (SEM) using a JSM-5600 Lv microscope (from JEOL, Tokyo,
Japan). The samples were coated with gold/palladium using a
Sputter Coater (Polaron, Bad Schwalbach, Germany). The cold-stage
(20 C) method was used to examine the samples. SEM was
operated at the low vacuum mode, using a spot size of 25e29 and a
potential of 16e23 kV.
Control
0.01b
0.02b
0.01b
0.01b
0.01b
0.01b
J. Odila Pereira et al. / LWT - Food Science and Technology 73 (2016) 543e550
Table 3
Color characteristics of control and probiotic lms incorporated with B. animalis Bb-12 and L. casei-01 during storage for 60 days at 23 1 C (a) and 4 1 C (b), viz. L* (blackewhite), a* (greenered), b* (blueeyellow) and DE
(color difference).
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J. Odila Pereira et al. / LWT - Food Science and Technology 73 (2016) 543e550
547
Table 4
Texture characteristics of control and probiotic lms incorporated with B. animalis Bb-12 and L. casei-01 during storage for 60 days at 23 1 C (a) and 4 1 C (b), viz. Youngs
Modulus (MPa), Tensile Strength (MPa) and Elongation at Break (%).
B. animalis Bb-12
Control
Youngs
modulus
(Mpa)
a)
0 days
3 days
5 days
10 days
40 days
60 days
b)
4 C
0 days
3 days
5 days
10 days
40 days
60 days
Note:
Tensile strength
(Mpa)
Elongation at
break (%)
Youngs
modulus (Mpa)
L. casei-01
Tensile
strength (Mpa)
Elongation at
break (%)
Youngs
modulus
(Mpa)
Tensile strength
(Mpa)
Elongation at
break (%)
0.311
0.312
0.311
0.311
0.311
0.312
0.000a
0.001a
0.001a
0.001a
0.000a
0.001a
0.770
0.767
0.771
0.777
0.769
0.767
0.004a
0.007a
0.003a
0.003a
0.010a
0.010a
65.500
65.500
65.534
65.533
65.521
65.500
1.803a
1.803a
1.859a
1.790a
1.782a
1.803a
0.309
0.309
0.309
0.310
0.313
0.310
0.000a
0.000a
0.000a
0.001a
0.006a
0.000a
0.675
0.676
0.676
0.675
0.679
0.679
0.025b
0.025b
0.025b
0.025b
0.023b
0.025b
64.667
64.671
64.700
64.737
64.677
64.684
0.577a
0.570a
0.608a
0.553a
0.586a
0.547a
0.310
0.310
0.310
0.311
0.312
0.311
0.002a
0.002a
0.002a
0.002a
0.003a
0.003a
0.615
0.615
0.616
0.615
0.610
0.615
0.020c
0.020c
0.020c
0.026c
0.020c
0.023c
65.000
65.018
65.037
65.004
64.968
65.001
3.500a
3.500a
3.505a
3.505a
3.449a
3.499a
0.310
0.312
0.311
0.310
0.311
0.312
0.002a
0.001a
0.001a
0.001a
0.002a
0.001a
0.771
0.770
0.771
0.775
0.771
0.767
0.005a
0.004a
0.003a
0.006a
0.009a
0.012a
65.502
65.510
65.527
65.530
65.525
65.507
1.807a
1.810a
1.850a
1.795a
1.804a
1.806a
0.310
0.310
0.308
0.311
0.310
0.310
0.001a
0.002a
0.000a
0.002a
0.002a
0.000a
0.676
0.677
0.676
0.679
0.679
0.678
0.024b
0.023b
0.025b
0.024b
0.025b
0.025b
64.700
64.685
64.720
64.733
64.635
64.690
0.578a
0.547a
0.609a
0.554a
0.580a
0.548a
0.311 0.000a
0.10 0.002a
0.311 0.003a
0.312 0.002a
0.312 0.003a
0.310 0.000a
0.615
0.612
0.615
0.613
0.610
0.615
0.020c
0.020c
0.020c
0.025c
0.021c
0.022c
65.020
65.018
65.021
65.020
65.027
65.011
3.498a
3.497a
3.500a
3.500a
3.486a
3.489a
a, b, c
, Means within the same columns, labeled with the same letter, do not statistically differ from each other (p > 0.05).
stored at 2 C, whereas for Bidobacterium lactis Bb-12, the optimum storage temperature was 8 C (Mortazavian, Razavi,
Ehsani, & Sohrabvandi, 2007; Mortazavian et al., 2007; Tripathi
& Giri, 2014). Storage temperature of 20 C resulted in signicant reductions in viable counts of this species in the dried
products.
These results suggest that the stability of probiotics increases
with low temperatures. This phenomenon occurs as the microorganisms are kept in a latent state avoiding rearrangements in the
wall material, preventing thus inadequate exposure of microorganisms (Albertini et al., 2010). Temperatures near to 0 C improve
the cell viability rate, because low temperatures reduce chemical
reaction rates that are harmful for microorganisms, such as,
oxidation (Nag, Han, & Singh, 2011).
Moreover, addition of whey protein and glycerol in the lm
solutions which are known as protectants could help in protecting
the viability of probiotic cells (Tripathi & Giri, 2014).
Furthermore, whey protein has signicant positive effects on
the survival of probiotic microorganisms during storage
(Mohammadi, Mortazavian, Khosrokhavar, & da Cruz, 2011) by
providing nutrition for the cells, reducing redox potential of the
medium as well as increasing buffering capacity of the medium that
results in a smaller decrease in pH (Mortazavian et al., 2007;
Soukoulis et al., 2014).
Nevertheless, the viable cell numbers at the end of the storage
period for both temperatures and probiotics tested are still within
the minimum threshold necessary for intended biological function
in the human body, although the storage at 23 C after 10 d would
slightly compromise the current most accepted value of 107 CFU/g
lm (FAO/WHO, 2002).
In similarity to the studies mentioned above, the results of this
study were the most promising to maintain the viability of
probiotics.
Fig. 1. FTIR absorbance spectra of whey protein based lms without microorganism
(control), with B. animalis Bb-12 at 0 days of storage at 23 1 C (a), with B. animalis
Bb-12 at 60 days of storage at 23 1 C (b), with B. animalis Bb-12 at 0 days of
storage at 4 1 C (c) and with B. animalis Bb-12 at 60 days of storage at 4 1 C (d).
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J. Odila Pereira et al. / LWT - Food Science and Technology 73 (2016) 543e550
Fig. 2. Scanning electron microscopy visualization of the surface (a, b and c) and cross-section (d and e) of whey protein based lms without microorganism (a and d) and with B.
animalis Bb-12 or L. casei-01 (b, c and e). Arrows indicate bacterial cells.
J. Odila Pereira et al. / LWT - Food Science and Technology 73 (2016) 543e550
549
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J. Odila Pereira et al. / LWT - Food Science and Technology 73 (2016) 543e550
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