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Department of Analytical Chemistry, Nutrition and Food Science, Faculty of Pharmacy, University of Santiago de Compostela, 15782 Santiago de Compostela, Spain
GAIKER Technological Centre, 48170 Zamudio, Spain
c
Novel Materials and Nanotechnology Group, IATA, CSIC, 46980 Paterna, Spain
d
Department of Chemical Engineering, Industrial Engineering School, University of Vigo, 36310 Vigo, Spain
b
a r t i c l e
i n f o
Article history:
Received 9 January 2014
Accepted 3 June 2014
Available online xxxx
Editor Proof Receive Date 14 July 2014
Keywords:
Active packaging lms
Bioactive compounds
Antimicrobial activity
Antioxidant activity
Functionalized nanoclays
a b s t r a c t
The aim of this study was to develop and evaluate the effectiveness of active packaging lms produced with a
natural extract obtained from a residual stream generated during the PVPP cleaning process in the brewing
industry after a process of elimination of excess of haze active polyphenols present in beer. The thermal stability
of the active phenolic compounds was rst established at 100 C and 200 C and then incorporated into ethylene
vinyl acetate (EVA) and low-density polyethylene (LDPE) lms by extrusion. Migration, antimicrobial activity
and lipid oxidation tests showed that EVA lm was the most suitable for incorporating the natural extract. Finally,
EVA lm was spiked with 3% and 6% (w/w) of the natural extract or functionalized nanoclays (0.6%, 1.2% and
1.8%). Functionalized nanoclays were prepared by combining untreated montmorillonite and 20% of natural extract. The lms spiked with the highest concentrations of extract or functionalized nanoclays provided the best
results by retarding both the oxidation of beef samples by around 60% and S. aureus growth. The active lms developed in the present study show promise for use in the food industry.
Industrial relevance: The new active packaging lms developed in this study with a natural extract obtained from
a brewery waste and functionalized nanoclays (prepared with natural extract) showed the capacity to enhance
the oxidative stability of beef during refrigeration with respect to control lms. The use of functionalized
nanoclays improves the effectiveness of the active packaging and minimizes the amount of natural extract
required. The use of these active packaging lms containing bioactive compounds with both antioxidant and
antimicrobial properties could extend the shelf life of minimally processed meat products and should therefore
be of great interest in the food industry.
2014 Elsevier Ltd. All rights reserved.
1. Introduction
Spoilage of fresh beef is mainly characterized by microbial activity
and by the oxidation of lipids and pigments (Sun & Holley, 2012).
Lipid oxidation, which is one of the main causes of deterioration of
meat quality during refrigerated storage, reduces the stability and
acceptability of food and is often a decisive factor in determining the
shelf-life of food (Gray, Gomaa, & Buckley, 1996). Reducing the oxidation process is an important challenge to food producers and, indeed,
everyone involved in the entire food chain from the farm to the fork.
The shelf-life of fresh meat can be extended by using antioxidants,
antimicrobials and appropriate packaging materials (Zhou, Xu, & Liu,
2010). One of the aims of food packaging is to protect the product
from harmful environmental factors by acting as an inert barrier
(Vermeiren, Devlieghere, van Beest, de Kruijf, & Debevere, 1999). Active
packaging is currently one of the most dynamic technologies used to
Corresponding author at: Industrial Engineering School, University of Vigo Campus
Universitario. As Lagoas- Marcosende E36310 Vigo, Spain.
E-mail address: jmcruz@uvigo.es (J.M. Cruz).
preserve the quality, safety and sensory properties of food. The active
packaging interacts positively with product and environment to improve/preserve the quality of food longer than conventional packaging
(Kerry, O'Grady, & Hogan, 2006). Some types of active packaging allow
the controlled release of bioactive substances (antimicrobials or antioxidants that have previously been added to the package), thus avoiding the
direct addition of the active agents to the food product (Lee, 2010). Most
studies in this eld have concerned active packaging developed with
antimicrobial agents, which can be directly incorporated into packaging
lms and have been extensively studied for use with meat products
(Coma, 2008; Zhou et al., 2010).
Growing concern about the potential health hazards caused by
synthetic additives has led to renewed interest in the use of naturally
occurring antioxidants/antimicrobials (Shahidi & Zhong, 2010). Waste
products from fruit and vegetable processing provide a practical and
economic source of potent antioxidants/antimicrobials that could
replace synthetic preservatives (Balasundram, Sundram, & Samman,
2006; Moure et al., 2001).
Many research studies in recent years have focused on developing
active packaging containing natural antioxidants. Thus, some authors
http://dx.doi.org/10.1016/j.ifset.2014.06.002
1466-8564/ 2014 Elsevier Ltd. All rights reserved.
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
IP
A0 A16
100
A0
where,
A0
A16
2.4. Nanocomposites
The montmorillonite used in this study is a food contact compliant
commercial organomodied clay with substances with afnity to polymeric matrix (Nanobioter AE21) supplied as a powder. No further
details of clay modication were disclosed by the manufacturer. Functionalized montmorillonites, were prepared by combining untreated
nanoclays provided by Nanobiomatters S.L. (Paterna, Spain) and 20%
of PVPP-WS extract, so that the content of PVPP-WS extract used to
produce the lms minimized consumption of natural extract.
The antimicrobial activity of the active lms was assessed by the ASTM
E 2149-01 standard test method for determining the Antimicrobial Activity
of Immobilized Antimicrobial Agents Under Dynamic Contact conditions
(E2149-01, 2002). The test was carried out to evaluate (quantitatively)
the antimicrobial effectiveness of the active lms spiked with natural
extract against selected spoilage microorganisms. Initially, LDPE and
EVA lms spiked with PVPP-WS extract (active additive) were analyzed
against Staphylococcus aureus CECT 239, Escherichia coli ATCC 8739,
Salmonella spp. CECT 443, Listeria monocytogenes CECT 935; E. coli O157:
H7 (non-toxigenic) CECT 4972, and the total aerobic mesophilic biota
isolated from minced meat. LDPE and EVA lms without additives were
tested as controls. The EVA lms (control and spiked with 3% and 6%
PVPP-WS extract) were then tested against microorganisms that were
most susceptible to the natural extract (S. aureus CECT 239 and E. coli
ATCC 8739). EVA NANO lms (control and spiked with 6% and 9% functionalized nanoclays) were also evaluated against S. aureus CECT 239.
2.8. Evaluation of antioxidant effectiveness of the lms with food samples
2.8.1. Beef samples
Freshly cut beef, of 1-cm thickness, was purchased in a local retail
store. The meat was divided in small pieces of 6 1 g and a small
amount of sodium azide (approx. 1 mg) was added to the surface of
the meat, to prevent microbial spoilage during storage.
2.8.2. Evaluation of antioxidant effectiveness of the active packaging lms
Samples of meat were packaged in individual bags prepared with all
lm formulations (see Section 2.5). In the rst test, the following were
evaluated: control LDPE and LDPE spiked with 3% of PVPP-WS extract
(LDPEC, LDPEA1, respectively); control EVA and EVA spiked with 3% and
6% of PVPP-WS extract (EVAC, EVA3% and EVA6%, respectively); and EVA
lm spiked with 3% of the functionalized nanoclays (EVA NANO0.6%).
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
The packaged beef samples were stored at 4 C for 14 days. Analysis for
2-thiobarbituric acid reactive substances (TBARS test) was carried out
after 3, 6, 9 and 14 days of storage.
In a second assay, EVA lms spiked with 6% and 9% of the functionalized nanoclays (EVA NANO1.2% and EVA NANO1.8%, respectively)
were tested against the control lm (EVA NANOC). Beef samples were
removed after 3, 6, 9 and 13 days for TBARS determination.
2.8.3. Lipid oxidation analysisTBARS
Lipid oxidation of beef meat was determined by the TBARS test, according to the extraction procedure described by Witte, Krause, and
Bailey (1970), with slight modications. Five grams of beef, to which
BHT was added (0.2 mg ml1), were extracted with 45.5 ml of extraction solution containing 10% trichloroacetic acid (TCA) in 0.02 M orthophosphoric acid to a nal volume of 50.0 ml. The samples were mixed
in an Ultra-Turrax homogenizer (IKA T25 digital ULTRA-TURRAX,
Ika-Werke, Staufen, Germany) at a speed of 16,000 rpm for 30 s and
then ltered through 0.45-m nylon membrane lters. Five milliliters
of extracted solution and 5 ml of TBA solution (0.02 M) were placed in
a test tube with a screw cap, homogenized by vortex (MS2 Mini
Vortex Shaker IKA, Ika-Werke, Staufen, Germany), and then incubated
in an oven at 100 C for 40 min. Finally, the samples were cooled at room
temperature, and the absorbance was measured by spectrophotometer
(Uvikon XL, Bio-Tek Instruments, Milan, Italy) at 530 nm against a blank
containing 5 ml of TCA solution and 5 ml of TBA reagent.
The concentration of malondialdehyde (MDA) was calculated from
the calibration curve obtained using 1,1,3,3-tetraethoxypropane (TEP)
(a precursor of MDA), as standard, in a concentration range between 0
and 5 mg L1. Results were expressed as milligrams of malondialdehyde
per kilogram of sample (MDA mg kg1 of beef).
2.9. Statistical analysis
Data were analyzed by analysis of variance (ANOVA), and signicant
differences were assessed by the Duncan's multiple range test (at
p b 0.05), by using the IBM SPSS Statistics 20.0.0 statistical software
package. Data are presented as means standard deviations.
3. Results and discussion
3.1. Thermal stability and antioxidant activity of natural extract
The thermal stability of the natural extract was tested to assess
whether the antioxidant compounds underwent thermal degradation
Fig. 1. Thermal stability of the natural extract exposed at temperatures of 100 C and 200 C for 120 min. Evaluation of the total phenolic contents (TPC) determined by FolinDenis method
(left axis) (represented by bars) and the percentage of non-volatile fraction (NVF) determined gravimetrically (right axis) throughout the exposure time (represented by straight lines).
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
Table 1
Antioxidant activity, determined by the DPPH method, of the natural extract exposed to
different temperatures. Results are expressed as EC50 (g L1).
EC50 (g L1)
Time (min)
100 C
200 C
0.355b 0.018
0.254bcd 0.022
0.335bc 0.017
0.299bcd 0.004
0.245bcd 0.010
0.215cd 0.006
0.199d 0.008
0.316 0.006
0.344b 0.018
0.316b 0.070
0.304b 0.016
0.292b 0.017
0.371b 0.049
0.307b 0.011
0.259bcd 0.056
2.497a 0.192
0
5
10
15
30
60
120
BHA
BHT
In the second part of the study, overall migration tests were carried
out with food simulants (meat products) to determine the total amount
of non-volatile substances that migrate into foodstuff by single side contact at 20 C (i.e. simulating realistic storage conditions under refrigeration). In this assay, the EVA lms samples spiked with the highest
concentrations of PVPP-WS extract (EVA6%) and functionalized
nanoclays (EVA NANO1.8%) were evaluated (Table 2b). The EVA active
lms tested comply with the limits established by current legislation
with respect to the overall migration values, which are all lower than
10 mg dm2 (Commission Regulation (EU) No. 10/2011). The overall
migration was higher when the active lms were in contact with 95%
ethanol and isooctane (fat simulants) than when in contact with
distilled water. When in contact with 95% ethanol, migration from
EVA active lms containing i) natural extract at the highest concentration tested (EVA6%) and ii) functionalized nanoclays (EVA NANO1.8%)
was twice as high as from the control lm (EVAC) with signicant differences in statistical terms (p b 0.05%). The overall migration from EVA
NANO1.8% was lower because the total concentration in PVPP-WS extract is lower and probably also because the natural extract that when
being functionalized in the nanoclay has more difculty to migrate
since the nanoclays controlled the release process of active compounds
(Sanchez-Garcia, Lopez-Rubio, & Lagaron, 2010; Silvestre et al., 2011).
Furthermore, the migration of the natural extract from the active lm
EVA6% was not complete during the assay. No signicant differences in
statistical terms (p b 0.05%) were found between different lms when
the lms were in contact with isooctane.
Table 2
(a) Overall migration data in 95% ethanol (v/v) and isooctane for LDPE and EVA lms (total immersion). (b) Overall migration from EVA active lms in water, 95% ethanol (v/v) and
isooctane (single face contact).
(a)
Packaging sample
Packaging material
Natural extract
(%PVPP-WS)
Food simulant
Time (days)
Temperature (C)
LDPEC
LDPE3%
LDPEC
LDPE3%
EVAC
EVA3%
EVAC
EVA3%
LDPE
LDPE
LDPE
LDPE
EVA
EVA
EVA
EVA
0
3
0
3
0
3
0
3
95% ethanol
95% ethanol
Isooctane
Isooctane
95% ethanol
95% ethanol
Isooctane
Isooctane
10
10
2
2
10
10
2
2
40
40
20
20
40
40
20
20
0.8c
1.9c
4.6c
3.0c
4.5c
12.6b
22.1a
25.5a
0.3
0.1
0.4
0.5
0.2
0.7
0.7
0.4
(b)
Packaging sample
Packaging material
Natural extract
(%PVPP-WS)
PVPP-WS
Nanoclays (%)
Food simulant
Time (days)
Temperature (C)
EVAC
EVA6%
EVA NANO1.8%
EVAC
EVA6%
EVA NANO1.8%
EVAC
EVA6%
EVA NANO1.8%
EVA
EVA
EVA
EVA
EVA
EVA
EVA
EVA
EVA
Distilled water
Distilled water
Distilled water
95% ethanol
95% ethanol
95% ethanol
Isooctane
Isooctane
Isooctane
10
10
10
10
10
10
1
1
1
20
20
20
20
20
20
20
20
20
0.10c
0.87c
0.07c
2.27ab
5.30a
4.23ab
4.20ab
5.07a
4.07ab
0.10
0.51
0.06
1.02
0.62
0.38
0.35
1.01
0.61
Values are means of three determinations. Different letters indicate signicant differences (p b 0.05).
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
Table 3
Antimicrobial activity of the different active lms, spiked with PVPP-WS extract or functionalized nanoclays, against Escherichia coli ATCC 8739 and Staphylococcus aureus CECT 239, during
storage for 6 days.
Film sample
EVAC
E. coli
S. aureus
EVA3%
E. coli
S. aureus
EVA6%
E. coli
S. aureus
EVA NANOC
S. aureus
EVA NANO0.6%
S. aureus
EVA NANO1.2%
S. aureus
EVA NANO1.8%
S. aureus
0h
24 h
48 h
6 days
24 h
48 h
6 days
4.56A 0.00
4.41a 0.00
4.54A 0.00
4.38b 0.05
4.52A 0.00
4.41a 0.02
4.50A 0.01
4.42a 0.01
4.56A 0.00
4.41a 0.00
4.52A 0.02
4.28c 0.02
4.55A 0.01
3.79b 0.02
4.57A 0.01
1.69c 0.05
66.00
99.00
4.56A 0.00
4.41a 0.00
4.51A 0.01
2.30f 0.02
1.30f 0.03
b1
1.30d 0.05
99.16
99.85
99.94
99.85
4.41a 0.00
4.52a 0.01
3.45c 0.01
3.15b 0.01
4.41a 0.00
4.14d 0.00
3.37d 0.04
b1
90.96
99.94
4.41a 0.00
3.78e 0.02
2.39e 0.01
1.30d 0.00
53.49
98.10
99.84
53.49
98.84
99.84
4.41
0.00
3.78
0.01
1.30 0.00
1.30
0.00
Mean values (log CFU ml 1 ) standard deviation. Within each column, different capital superscript letters, for E. coli, and, lower case superscript letters for S. aureus,
indicate signicant differences (p b 0.05). Within each row, the different symbols (, , and ) indicate signicant differences (p b 0.05).
EVA again proved to be the most effective polymer in the active packaging. EVA lms (control and spiked with 3% and 6% PVPP-WS extract)
were tested against microorganisms that are most susceptible to the natural extract (S. aureus CECT 239 and E. coli ATCC 8739) (Table 3). The EVA
lm spiked with the lower concentration of extract (EVA3%) was active
against S. auerus after 48 h of contact. EVA6% was effective against both
microorganisms tested during long incubation times for E. coli and
throughout the entire incubation time for S. aureus. All EVA NANO active
lms showed antimicrobial activity against S. aureus during incubation.
Inclusion of the functionalized nanoclays improved the effectiveness of
the active packaging lm, even though they contained lower amounts
of natural extract.
Several authors have reported that phenolic compounds contribute
to the antimicrobial activity. The PVPP-WS natural extract used to develop the active lms contains large amounts of such bioactive compounds.
According to the ndings of Puupponen-Pimi et al. (2001), ferulic and
caffeic acids are probably the main compounds responsible for the antimicrobial effect of the PVPP-WS natural extract used to develop the
active lms tested in this study. However, other compounds such as
avonoids present in the PVPP-WS extract may also be responsible for
the antimicrobial activity. Compounds such as catechins, apigenin,
Table 4
TBARs values (mg MDA kg1 of sample) obtained in beef samples packed with: (a) different active lms spiked with PVPP-WS extract or with the lowest concentration of functionalized
nanoclays and stored at 4 C for 14 days; (b) different active lms spiked with higher concentrations of functionalized nanoclays and stored at 4 C for 13 days.
(a)
Film sample
LDPEC
LDPE3%
EVAC
EVA3%
EVA6%
EVA NANO0.6%
3
A
0.399
0.399A
0.399A
0.399A
0.399A
0.399A
0.046
0.046
0.046
0.046
0.046
0.046
6
aB
6.61
4.22dB
5.02cB
2.63fB
3.28eB
5.79bB
0.149
0.464
0.149
0.507
1.02
0.785
9
aC
8.06
8.98aC
8.09aC
3.86bB
3.28bB
8.85aC
0.838
1.20
1.26
0.089
0.820
0.570
14
aD
15.6
15.2bD
14.3cD
8.46dC
5.86eC
11.8fD
1.06
0.072
0.905
0.876
0.038
0.564
18.3aE
14.9bcD
16.6abE
12.9cD
5.43dC
13.1cE
0.640
0.110
1.01
1.02
0.704
0.625
(b)
Film sample
EVA NANOC
EVA NANO1.2%
EVA NANO1.8%
13
0.274A 0.025
0.274A 0.025
0.274A 0.025
0.550aA 0.271
0.544aA 0.000
0.673aA 0.375
3.69aB 0.821
1.55bB 0.456
1.34bB 0.035
6.92aC 0.253
4.69bC 1.03
1.87cC 0.115
9.17aD 0.534
8.36bD 0.873
7.06cD 0.121
Different lower case superscript letters (within the same time) and capital superscript letters (within the same row) denote statistically signicant differences in the mean
values (n = 3) at p b 0.05.
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
(A)
20
18
mg MDA Kg-1 of beef
16
14
12
10
8
6
4
2
0
12
15
Time (days)
LDPE C
LDPE 3%
EVA C
EVA 3%
(B)
20
18
mg MDA Kg-1 of beef
16
14
12
10
8
6
4
2
0
12
15
Time (days)
EVA C
EVA 3%
EVA 6%
(C)
12
10
8
6
4
2
0
10
12
14
Time (days)
EVA NANO C
Fig. 2. Lipid oxidation of beef packed with active lms determined by measuring the TBARS during storage at 4 C. Evaluation of antioxidant effectiveness of the following: (A) LDPE and
EVA lms controls and LDPE and EVA lms spiked with the same concentration of natural extract; (B) EVA lm control, EVA lms spiked with different concentrations of natural extract
and EVA lms spiked with the lowest concentration of functionalized nanoclays; (C) EVA lm control and EVA lms spiked with different concentrations of functionalized nanoclays.
Please cite this article as: Barbosa-Pereira, L., et al., Development of new active packaging lms containing bioactive nanocomposites, Innovative
Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002
L. Barbosa-Pereira et al. / Innovative Food Science and Emerging Technologies xxx (2014) xxxxxx
4. Conclusions
The natural extract obtained from a residual waste exhibited a high
degree of thermal stability, conserving the antioxidant properties and
the percentage of total phenolic content that makes it suitable for the
development of active lms by extrusion. Antioxidant active lms
were successfully developed by extrusion. Migration, antimicrobial
activity and lipid oxidation tests showed that EVA lm was the most
suitable for incorporating the natural extract. The EVA lms spiked
with the natural extract protected the food sample (beef) better than
the control lm, by retarding lipid oxidation and microbial growth of
spoilage microorganisms with a reduction of the number of bacteria
(S. aureus) above 90% at 24 h for EVA6% and at 48 h for EVA NANO
lms up to 99% of reduction at day 6 for all EVA active lms. The EVA
active lms comply with the limits established by current legislation
with respect to the overall migration values. The use of functionalized
nanoclays (prepared with the natural extract) improved the effectiveness of the active packaging and minimized the amount of natural
extract required.
The active lms produced in the study could be used to develop
active packaging for use in the food industry to extend the shelf-life of
meat products. Furthermore, the additive used is a natural product
obtained from an agro-industrial residual source and is therefore likely
to be more acceptable to consumers than similar products based on
synthetic antioxidants.
Acknowledgments
This study was nancially supported by the Consorcios Estratgicos
Nacionales en Investigacin Tcnica (CENIT) of Ministerio de Ciencia y
Inovacin (CENIT-2007-2016-FUTURAL). The authors are grateful
to the Mahou-San Miguel Group and FUTURAL project (Ingenio
ProgramCDTI).
The authors express their sincere thanks to Ms. Patricia Blanco Carro,
Ms. Cristina Casal Romero and Mr. Gonzalo Hermelo Vidal for their
excellent technical assistance.
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Food Science and Emerging Technologies (2014), http://dx.doi.org/10.1016/j.ifset.2014.06.002