Received: 26 December 2020 | Revised: 4 February 2021 | Accepted: 6 February 2021

DOI: 10.1002/fsn3.2186

ORIGINAL RESEARCH

Control of microbial growth and lipid oxidation in beef using a

Lepidium perfoliatum seed mucilage edible coating incorporated
with chicory essential oil

Behrooz Alizadeh Behbahani1 | Fereshteh Falah2 |

Alireza Vasiee2 | Farideh Tabatabaee Yazdi2

1
Department of Food Science and
Technology, Faculty of Animal Science and Abstract
Food Technology, Agricultural Sciences and In this study, chicory essential oil (CEO) was obtained by hydrodistillation-­based ex-
Natural Resources University of Khuzestan,
Mollasani, Iran traction method and it was rich in camphor (31.3%) and phenolic compounds with
2
Department of Food Science and outstanding antioxidant and antimicrobial properties. The CEO was then incorpo-
Technology, Faculty of Agriculture, Ferdowsi
rated into Lepidium perfoliatum seed mucilage (LPSM) based aqueous solution to pre-
University of Mashhad, Mashhad, Iran
pare an active CEO-­loaded LPSM edible coating. The effect of the edible coating was
Correspondence
then investigated on the quality and shelf life of beef slices during 7 days storage at
Farideh Tabatabaee Yazdi, Department
of Food Science and Technology, Faculty 4°C. The results revealed that beef slice coated with CEO-­loaded LPSM edible coat-
of Agriculture, Ferdowsi University of
ing had a significant inhibitory effect on its lipid oxidation and microbial growth. The
Mashhad, Mashhad, Iran.
Email: [email protected] CEO-­LPSM coating also inhibited the weight and texture losses of beef slices dur-
ing display more efficiently compared with the control and CEO-­free LPSM coating.
Besides, the beef slices coated with CEO-­LPSM were the preferred samples in terms
of sensory scores throughout the storage. Thus, using CEO-­rich LPSM edible coating
might inhibit decay and significantly improve the shelf life of fresh beef.

KEYWORDS

chicory essential oil, edible coating, fresh beef, Lepidium perfoliatum mucilage, shelf life

1 | I NTRO D U C TI O N gums of natural origin for the development of novel edible coatings
has been increased.
Meat and meat products, due to their suitable pH, fermentable Lepidium perfoliatum (locally called Qodume shahri) is native to Iran,
carbohydrate, and high contents of nitrogen, moisture, and fat, Iraq, Egypt, Arabia, and Pakistan, and its seed mucilage is widely used
are highly prone to chemical and microbial deteriorations, which in traditional medicine to treat whooping cough, dry cough, and lung
could affect the texture, flavor, color, and nutritional quality of infections and as a demulcent (Koocheki et al., 2013). It has been re-
the related products (Alizadeh Behbahani, Noshad, et al., 2020). ported that the mucilage extracted from L. perfoliatum seeds could be
Currently, hydrocolloid-­based edible coatings are receiving a great used as a stabilizing and thickening agent in food systems for viscosity
deal of research and industrial attention as novel food packag- increment, texture modification, and consistency stabilization purposes
ing systems to ameliorate shelf life and quality of food products, (Hesarinejad et al., 2014). It is also noteworthy that the L. perfoliatum
through preventing chemical, microbial, and physical damages seed mucilage (LPSM) films have good physicochemical, mechani-
(Barzegar et al., 2020). Recently, the demand for polysaccharide cal, and thermal properties and could be applied as a biodegradable

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2021 The Authors. Food Science & Nutrition published by Wiley Periodicals LLC

2458 | 
www.foodscience-nutrition.com Food Sci Nutr. 2021;9:2458–2467.
ALIZADEH BEHBAHANI et al. | 2459

packaging for improving the shelf life of various food products (Seyedi official standard procedures to extract and control the quality of
et al., 2015). Nonetheless, edible coatings based on polysaccharides EOs of medicinal herbs (Taherpour et al., 2017). For the extrac-
have hardly antioxidant and antimicrobial activity themselves; there- tion of CEO, the chicory was dried, powdered, and added to the
fore, food-­grade ingredients (e.g., plant-­based antioxidant and antimi- Clevenger device (containing 50 g powder in 750 ml distilled water).
crobial components) are commonly added to edible coatings to improve The extraction process was performed for 3 hr at 335 power, ac-
their biological and functional properties (Barzegar et al., 2020). cording to a method reported by Heydari et al. (2020), with some
In this context, essential oils (EOs) are frequently used in food changes. The oil (CEO) was then collected, dehydrated, and stored
preservation technologies as natural and are generally recognized at 4°C.
as safe agents, owing to antimicrobial and antioxidant compounds
they carry (Calo et al., 2015; Rehman et al., 2020). For example, it has
been reported that the lemon/thyme EOs-­enriched chitosan coating 2.3 | Gas chromatography-­mass spectroscopy (GC/
maintained higher hardness and color and retarded lipid/protein ox- MS)
idation and microbial growth in grass carp filled during cold storage
(Cai et al., 2018). Similarly, Cai et al. (2015) demonstrated that the A gas chromatograph (GC; Agilent 7890A) coupled to a mass spec-
fresh fish fillets treated with clove, cumin, and spearmint oils main- trometer (MS; Agilent 5975C) was employed for the identification
tained the hardness, delayed protein and nucleotide degradation, re- and quantification of the main chemical compounds of the CEO.
tarded the sensory deterioration, and inhibited the microbial growth Briefly, 0.2 µl of the oil was injected to the DB-­5 capillary column
and the formation of biogenic amines. (30 m × 0.25 mm × 0.25 µm) and the heating rate, ionization energy,
Chicory (Cichorium intybus L.) is a perennial herb and rich in bio- helium gas flow rate was set at 5°C/min, 70 eV, and 1 ml/min, respec-
active compounds for human food fortification purposes. It also has tively. Finally, the retention profiles were obtained and compared
many types of biological properties, such as anticancer, antidiabetic, with those of know samples which were analyzed under the same
anti-­
inflammatory, hepatoprotective, hypolipidemic, antioxidant, conditions (Alizadeh Behbahani & Shahidi, 2019).
and antimicrobial effects (Šaponjac et al., 2021). Moreover, the chic-
ory essential oil (CEO) has remarkable antioxidant and antimicrobial
properties (Gol et al., 2014). Accordingly, CEO could be used as a 2.4 | Total phenolics and flavonoids
potential natural preservative in edible coatings to amend their oxi- content
dation-­and microbial growth-­suppression functions.
To the best of our knowledge, there is no evidence about the role Total phenolic content of the CEO was measured based on the
of the oxidative and microbial stability of meat and meat products method described by Ahmed et al. (2019). Gallic acid (0–­0.5 mg/ml)
wrapped by CEO-­loaded LPSM edible coating. The objective of this was used as a standard to obtain a calibration curve and the total
study was therefore to isolate and characterize the CEO and develop phenolic content of the oil was expressed as mg gallic acid equiva-
a novel CEO-­loaded LPSM edible coating to improve the microbial lent (GAE)/g.
and oxidative stability of beef slices during cold storage. The procedure of Saki et al. (2019) was used to determine the
total flavonoid content of the CEO. Briefly, the absorbance of the
mixture of CEO, NaNO2, AlCl3, NaOH, and distilled water was re-
2 | M ATE R I A L S A N D M E TH O DS corded at 510 nm, and the content of total flavonoids of the CEO was
then expressed as mg quercetin equivalent (QE)/g.
2.1 | Materials

The L. perfoliatum seeds and chicory were purchased from a local mar- 2.5 | Antioxidant activity
ket (Khuzestan, Iran). β-­carotene, Linoleic acid, ABTS (2,2′-­A zino-­bis
(3-­ethylbenzothiazoline-­6-­sulfonic acid) diammonium salt), quercetin, In this study, DPPH-­radical scavenging (DPPH-­RS) activity, ABTS
gallic acid, and DPPH (2,2-­diphenyl-­1-­picrylhydrazyl) were purchased radical scavenging (ABTS-­RS) activity, and β-­carotene-­linoleic acid
from Sigma-­Aldrich Co. Mannitol Salt Agar (MSA), Eosin Methylene bleaching assays were used to determine the antioxidant activity of
Blue (EMB), Mueller Hinton Broth (MHB), Mueller Hinton Agar (MHA), the oil, according to the method described by Barzegar et al. (2020).
Sabouraud Dextrose Broth (SDB), Sabouraud Dextrose Agar (SDA), To determine the DPPH-­RS activity, the CEO (50 μl) or control
and Plate Count Agar (PCA) were obtained from Merck Co. (50 50 μl) was mixed with 0.12 mM ethanolic DPPH solution (5 ml).
The resulting solution was stored at 25°C for 30 min, and its ab-
sorbance (A) was read at 517 nm. The DPPH-­RS activity was then
2.2 | CEO extraction measured as below:

The CEO extraction was performed according to the hydrodistil- Acontrol − ACEO
DPPH − RS activity ( % ) = × 100.
lation method, which is known as one of the famous, routine, and Acontrol
2460 | ALIZADEH BEHBAHANI et al.

For the ABTS-­RS activity, ABTS solution and K 2S2O8 were ini- beef slice was used as control. The samples were designated as
tially mixed together to generate ABTS radical cation solution. After control, LPSM + 0%CEO, LPSM + 0.5%CEO, LPSM + 1%CEO, and
that, the CEO (0.1 ml) or control (0.1 ml) was mixed with the ABTS LPSM + 1.5%CEO.
radical solution (3.9 ml) and its absorbance was recorded at 734 nm.
The ABTS-­RS activity was then measured as follows:
2.9 | Microbial analysis
A − ACEO
ABTS − RS activity ( % ) = control × 100.
Acontrol To determine the microbial load changes of beef slices during display,
the slices were firstly mixed and homogenized with 0.1% peptone
The following equation was used to measure the inhibitory ef- water in a Stomacher. The slurry was then added to the test tubes
fect of the CEO against β-­carotene-­linoleate solution bleaching: containing 0.1% peptone water to prepare subsequent dilutions (10–­
1
to 10–­6), which were further inoculated into the plates contain-
AS(120) − AC(120) ing culture medium. The following tests were then performed to
Inhibitory effect ( % ) = × 100,
AC(0) − AC(120) evaluate the microbial growth during storage (Alizadeh Behbahani,
Noshad, et al., 2020):
where, AS(120) is the absorbance of the solution at 490 nm after 120 min
incubation, AC(0) is the absorbance of control at the time zero, and AC(0) ● Total viable count (TVC) bacterial count in PCA (48 hr incu-
is the absorbance of control at the after 120 min reaction. bation at 37°C)
● Psychrotrophic count (PTC) in PCA (10 days incubation at 7°C)
● Staphylococcus aureus count in MSA (24 hr incubation at 37°C)
2.6 | Antimicrobial activity ● Escherichia coli count in EMB (24 hr incubation at 37°C)
● Fungi count in SDA (72 hr incubation at 27°C).
The method of Noshad et al. (2018) was used to evaluate the anti-
bacterial effect of the CEO against some pathogenic gram-­positive
bacteria (Staphylococcus aureus, Listeria innocua, and Bacillus cereus) 2.10 | Physicochemical analysis
and gram-­
negative bacteria (Escherichia coli, Pseudomonas aerugi-
nosa, and Salmonella typhi), through disk diffusion agar (DDA), well 2.10.1 | Lipid oxidation
diffusion agar (WDA), and minimum inhibitory/bactericidal concen-
tration (MIC/MBC) methods. The peroxide value (PV; meq O2/kg) and thiobarbituric acid (TBA;
mg MDA/kg) value of beef slices were measured according to the
methods of Bazargani-­Gilani et al. (2015).
2.7 | Mucilage extraction

The L. perfoliatum seed mucilage (LPSM) was extracted according 2.10.2 | Moisture content
to the method of Koocheki et al. (2013). The seeds were dispersed
in deionized water (1:30 ratio), and the extraction process was per- The beef slices were dried at 105°C for 3 hr, and the moisture con-
formed for 90 min at pH 8 and 48°C. The slurry was oven-­dried tent was then determined (AOAC, 1995).
(45°C), milled, sieved, and stored at 4°C.

2.10.3 | pH measurement
2.8 | Beef slices coating
The beef samples (10 g) were mixed with deionized water (90 ml) and
The edible coatings were prepared by mixing LPSM (2 g) and homogenized (30 s, 13,000 rpm, 25°C). The pH value of the slurry
Tween-­8 0 (1 ml) in distilled water (the volume was made up to was then determined by a pH-­meter (Barzegar et al., 2020).
100 ml). The CEO (0, 0.5, 1, and 1.5% v/v) was then added. The
beef slices were immersed in the CEO-­LPSM solution for 60 s
and then air-­dried for 10 min. The essential oil concentrations 2.10.4 | Hardness
and coating treatments were selected according to the prelimi-
nary experiments for the beef slices to assure (a) adherence and A cylindrical probe was used to compress the beef slices (30% of
steadiness of the LPSM coating, (b) antimicrobial and antioxidant the sample thickness) at a constant pretest speed, test speed, and
activity of the essential oil, and (c) acceptable sensory properties post-­test speed of 3, 1, and 3 mm/s, respectively, by a Stable Micro
(masking the strong flavor or odor of the essential oil). The coated System Texture Analyzer (TA, XT2i). The highest force (N) was re-
beef slices were then stored at 4°C for 7 days. The noncoated ported as the hardness of the beef slices.
ALIZADEH BEHBAHANI et al. | 2461

2.10.5 | Sensory evaluation phenolic compounds have the potential to possess antioxidant and
antimicrobial activities and improve the shelf life of food products.
The odor, color, texture, and overall acceptance of the coated and Antioxidant capacity is occurred by various mechanisms, which
control beef slices were evaluated by 25-­well trained panelists via a indicates utilizing a method based on one mechanism may not
nine-­point hedonic scale test. The sensory scores ranked from best demonstrate the true antioxidant activity (Karadag et al., 2009). Thus,
(9 = like extremely) to worst (1 = dislike extremely). several antioxidant tests, such as DPPH-­and ABTS radical scaveng-
ing activity and β-­carotene-­linoleic acid model system, were used
to measure the antioxidant effect of the CEO. The oil had a DPPH-­
2.10.6 | Statistical analysis radical scavenging effect of 72.95 ± 0.53%, and this remarkably high
antioxidant capacity indicates that the CEO has hydrogen/electron
Data were analyzed by Minitab software (version 16) via one-­way ability to reduce DPPH free radicals to nonreactive molecules. The
ANOVA. The Tukey test, at confidence level of 95% (p < .05), was oil was also able to scavenge ABTS radicals by 64.59 ± 0.4%, prob-
applied to determine the differences between the data means. It ably through hydrogen atom and electron transfer mechanisms. It
is also necessary to note that the experiments were done at three was also observed that the CEO had a moderate inhibitory effect
replications. against β-­carotene discoloration (54.5 ± 0.47%) likely via neutralizing
linoleate free radicals. The antioxidant activity of chicory extracts
and EOs has been reported in the literature (Gol et al., 2014; Khalaf
3 | R E S U LT S A N D D I S CU S S I O N et al., 2018; Sahan et al., 2017). This positive biological activity of

3.1 | CEO characterization

Plant EOs are rich in bioactive compounds with versatile biological

functions. In this study, CEO was subjected to GC/MS apparatus to
identify and quantify its main chemical constituents. The oil was
rich in camphor (31.3%), cymene (18.2%), γ-­terpinene (8.45%), and
β-­pinene (7.85%). Other compounds, such as pinene (4.9%), eucalyp-
tol (3.3%), camphene (3.1%), and carvacrol (2.7%), were also found
in the CEO at lower concentrations. In accordance with our study,
it was reported that the major components of the CEO are cam-
phor (20.74%), cymene (15.06%), γ-­terpinene (13.24%), and cumi-
nal (10.79%) (Gol et al., 2014). Similarly, it was found that camphor
(21.4%–­26%) is the main compound of the CEO (Farhoudi, 2017).
However, the variation found in the concentration and type of the
major constituents is due to the fact that the composition of vola-
tile organic compounds is greatly dependent on the genetic factors,
harvest time, growing location, storage conditions, nutrients, light,
water, and extraction methods (Šaponjac et al., 2021).
The CEO also contained considerable levels of phenolic and
flavonoid compounds (73.45 ± 0.7 mg GAE/g and 67.62 ± 0.58 mg F I G U R E 1 Antimicrobial effect of chicory essential oil (CEO)
QE/g, respectively). The content of total phenolic and flavonoid against some pathogenic and spoilage bacterial species
compounds is indeed dependent on the chicory culture, harvest
time, other environmental factors, and extraction method/solvent. TA B L E 1 The minimum inhibitory concentration (MIC) and
Accordingly, the cultivated and wild chicory roots have significantly minimum bactericidal concentration (MBC) of the chicory essential
different total phenolic contents of 35.1 and 22.4 mg GAE/100 g, oil (CEO) on some pathogenic microorganisms
respectively (Spina et al., 2008). Likewise, it seems that chicory MBC
leaves have noticeably higher total phenolic contents in comparison Microorganism MIC (mg/ml) (mg/ml)
with other parts of the plant (Heimler et al., 2009). The total flavo- Pseudomonas aeruginosa 100 400
noid content of 112.38 mg QE/100 g has been also found in chicory
Escherichia coli 200 400
leaves (Khalaf et al., 2018). Indeed, chicory plant is a rich source of
Salmonella typhi 400 >400
phenolic compounds, such as gallic acid, syringic acid, catechin, caf-
Listeria innocua 100 200
feic acid, vanillic acid, protocatechic acid, ferulic acid, chlorogenic
Staphylococcus aureus 25 100
acid, naringin, hesperidin, neohesperidin, myricetin, kaempferol,
Bacillus cereus 100 200
quercetin, rutin hydrate, and resveratrol (Sahan et al., 2017). These
2462 | ALIZADEH BEHBAHANI et al.

the CEO is mainly due to the redox properties of its phenolic com- disks surface to the medium determines its antibacterial effect in
pounds, thereby acting as hydrogen/electron donors, singlet oxygen the DDA technique (Alizadeh Behbahani & Imani Fooladi, 2018a;
quenchers, and metal ions chelation (Indrianingsih et al., 2015). Barzegar et al., 2020). It could be also noteworthy that low levels
As can be seen from Figure 1 and Table 1, the CEO showed of CEO were generally enough to possess growth-­suppression or
considerable antibacterial effect against all tested microorganisms. killing effect against gram-­positive microorganisms, in comparison
The gram-­positive bacteria (S. aureus, B. cereus, and L. innocua) were with the gram-­negative ones (Table 1). The higher susceptibility of
more susceptible to the oil compared with the gram-­negative ones the gram-­positive bacterial species to the oil is greatly due to the
(S. typhi, E. coli, and P. aeruginosa) as confirmed by the higher inhibi- presence of a thin and single mucopeptide layer in their cell mem-
tion zones in the DDA (14.8 mm vs. 11.6 mm) and WDA (16.1 mm vs. brane, whereas, the outer cell membrane of the gram-­negative ones
12.66 mm) tests. Moreover, it can be observed that the inhibition is covered and protected by a complex lipopolysaccharide layer
zones in the WDA antimicrobial assay (14.38 mm) were generally which could function as a barrier toward diffusion of hydrophobic
higher compared with those in the DDA test (13.2 mm). This might antimicrobial agents across the cell (Alizadeh Behbahani, Falah,
be due to the direct interaction between the oil and the microor- et al., 2020; Alizadeh Behbahani et al., 2019; Alizadeh Behbahani,
ganism in the WDA method; while, the diffusion of CEO from the Noshad, et al., 2020; Noshad et al., 2021; Yeganegi et al. 2018).

F I G U R E 2 Changes in total viable count (a), psychrotrophic count (b), Escherichia coli count (c), Staphylococcus aureus count (d), and fungi
count (e) of the beef slices stored at 4°C for 7 days
ALIZADEH BEHBAHANI et al. | 2463

F I G U R E 3 Changes in pH value of the coated and noncoated F I G U R E 5 Changes in moisture content of the coated and
beef slices stored at 4°C for 7 days noncoated beef slices stored at 4°C for 7 days

F I G U R E 4 Changes in hardness value of the coated and

noncoated beef slices stored at 4°C for 7 days

These results are supported by the findings of Majd et al. (2009) and
Khalaf et al. (2018).

3.2 | Application of CEO-­loaded LPSM edible

coating on beef slices

The CEO with considerable antimicrobial and antioxidant properties

was therefore used as a natural preservative to develop novel active
edible coatings (i.e., CEO-­loaded LPSM coating) to ameliorate quality F I G U R E 6 Changes in peroxide value (a) and thiobarbituric acid
and shelf life of beef slices. value (b) of the coated and noncoated beef slices stored at 4°C for
Figure 2 indicates the changes in TVC, PTC, E. coli, S. aureus, 7 days
and fungi counts of the control and coated beef slices during cold
storage. The samples experienced a significant increase in TVC as a are predicted for the control, LPSM + 0%CEO, LPSM + 0.5%CEO,
function of storage period (Figure 2a), and the coated samples had LPSM + 1%CEO, and LPSM + 1.5%CEO coated samples, respec-
significantly lower TVC than the noncoated one. Indeed, the TVC of tively. This might be likely due to the antimicrobial effect of the CEO
the beef slices increased up to 5.24-­, 4.23-­, 4.16-­, 3.22-­, and 3.15-­ and oxygen barrier function of the CEO-­rich edible coatings, in ac-
fold in control, LPSM + 0%CEO, LPSM + 0.5%CEO, LPSM + 1%CEO, cordance with other studies (Alizadeh Behbahani et al., 2017).
and LPSM + 1.5%CEO coated samples, respectively, by the end of Similar trends were observed for the PTC, E. coli, S. aureus, and
storage time. It is also worth to note that a TVC of 7 log CFU/g is the fungi counts in the control and coated samples (Figure 2b–­e). Despite
maximum permitted TVC level for fresh beef (Alizadeh Behbahani, the fact that all the beef slices experienced a significant increase
Noshad, et al., 2020). In this context, the beef slices exceeded the (p < .05) in the microbial growth over time, the coated samples had
permitted level on day 3 (control) and day 5 (LPSM + 0%CEO and significantly lower microbial counts compared with the noncoated
LPSM + 0.5%CEO), while the LPSM + 1%CEO and LPSM + 1.5%CEO one. And this effect was more pronounced in the samples wrapped
coated beef samples never reached this limit level during refrigeration by LPSM + 1.5%CEO. The positive effect of the CEO-­loaded LPSM
storage. Accordingly, the microbial shelf lives of 2, 4, 4, 7, and 7 days edible coating on the beef preservation could be mainly ascribed
2464 | ALIZADEH BEHBAHANI et al.

to (a) the antimicrobial activity of the oil and (b) the oxygen barrier microbial growth-­suppression and meat enzymes activity-­inhibitory
characteristics of the edible coating. The growth of aerobic mi- effects of the CEO and edible coating, thereby preventing meat
croorganism, such as fungi and psychrotrophic bacteria, which are protein degradation and subsequent pH increase and texture loss
the main cause of meat spoilage during cold storage under aerobic (Mohan et al., 2012; Omidi-­Mirzaei et al., 2020).
conditions, is therefore inhibited remarkably (Alizadeh Behbahani & The edible coating was also able to efficiently inhibit weight
Imani Fooladi, 2018a, 2018b). These results are in accordance with loss of the beef slices over time (Figure 5). Despite the fact that
those of Kiarsi et al. (2020), who reported that EOs-­loaded seed all the samples underwent a significant decrease in moisture con-
mucilage-­
based edible coatings could significantly suppress the tent (i.e., higher weight loss) during cold storage, the beef slices
growth of microorganisms (i.e., TVC, PTC, E. coli, S. aureus, and fungi) coated by the CEO-­enriched LPSM maintained moisture content
during cold storage. compared with the noncoated sample. At the end of refrigeration
Accordingly, the beef slices coated by the CEO-­rich LPSM had period, the control sample underwent a significant weight loss of
the lowest changes in pH value (Figure 3) and hardness (Figure 4) about 23.23%, whereas the samples coated by LPSM + 0%CEO,
throughout the storage time. Although all the samples experienced LPSM + 0.5%CEO, LPSM + 1%CEO, and LPSM + 1.5%CEO had
an increase in pH value as a function of storage time, the CEO and lower weight losses of 10.89%, 9.24%, 7.18%, and 7.35%, respec-
edible coatings had no significant effects on the pH value of the tively. The less weight loss by CEO-­loaded LPSM edible coating
samples (p > .05). However, the higher CEO concentration in the could be attributed to the water barrier properties of the coating
LPSM edible coating, the lower were the pH increment (p > .05) and (Ruan et al., 2019). In line with our study, little exudates were ob-
hardness loss (p < .05). The samples coated by CEO-­loaded LPSM served in meat samples coated by bioactive-­loaded edible coat-
had significantly higher hardness value compared with the con- ing and the meat protected against water losses during storage
trol sample, at the 7th day of storage. This could probably due to (Alexandre et al., 2020).

FIGURE 7 Changes in odor (a), color (b), texture (c), and overall acceptance (d) of the coated and noncoated beef slices stored at 4°C for
7 days
ALIZADEH BEHBAHANI et al. | 2465

It is also necessary to point out that lipid oxidation is consid- odor conferred on the beef by the CEO could also have influenced
ered as one of the main factors of quality deterioration in beef. its consumer acceptance.
The PV and TBA value were then measured as lipid oxidation indi-
ces (Figure 6). As can be observed in Figure 6a, the PV increased
significantly during refrigeration storage. The uncoated beef sam- 4 | CO N C LU S I O N S
ple experienced the highest PV increase during storage (6.69-­fold).
While the PV of the coated samples increased remarkably slowly, The chicory essential oil showed a large number of bioactive com-
and the LPSM + 0%CEO, LPSM + 0.5%CEO, LPSM + 1%CEO, and pounds with superb antioxidant and antimicrobial properties. The
LPSM + 1.5%CEO showed approximately 5.85-­, 5.95-­, 5.71-­, and incorporation of chicory essential oil into the L. perfoliatum seed
4.31-­fold PV increase as the storage time rose from 1 to 7 days. It mucilage-­based edible coating reduced the beef lipid oxidation and
is noteworthy that the permitted PV limit for meat is 7 meq O2/ microbial growth more efficiently compared with the oil-­free coat-
kg (Alizadeh Behbahani, Noshad, et al., 2020). Accordingly, the un- ing. The bioactive-­
loaded edible coating also decreased weight
coated beef sample exceeded the permitted limit on the 7th day and and texture losses during display and improved beef acceptability.
its shelf life is therefore predicted to be 5 days under cold storage Therefore, edible coatings rich in natural compounds with superb
conditions; while, the beef samples coated by LPSM + 1%CEO and antimicrobial and antioxidant effects could be used in animal meat
LPSM + 1.5%CEO had lower PVs than the limited value, and the products to ameliorate their shelf life.
shelf life of these coated meat samples is greater than 7 days.
Before storage (day 1), the TBA levels were similar in the beef AC K N OW L E D G M E N T
slices from uncoated and CEO-­
loaded LPSM coated treatments The authors would like to express their sincere gratitude to the Vice-­
and lowest from treatments containing higher CEO concentra- chancellor for Research and Technology of Ferdowsi University of
tions (p > .05) (Figure 6b). As expected, the TBA values increased Mashhad for supporting this study as the project No. 52734.
significantly during storage (p < .05), mainly in the noncoated sam-
ple, which presented the highest value of 1.64 MDA/kg at the end C O N FL I C T O F I N T E R E S T
of storage period, greater than the TBA limit for acceptability in The authors have declared no conflict of interest.
meat (i.e., 1 MDA/kg) (Alizadeh Behbahani & Imani Fooladi, 2018a,
2018b). However, the addition of CEO into LPSM edible coating E T H I C A L A P P R OVA L
decreased the TBA progression more efficiently, and all the CEO-­ This article does not contain any studies with human or animal
loaded LPSM coated beef slices had lower TBA levels than the ac- subjects.
ceptable limit. This study showed that the use of CEO-­rich edible
coating was effective in delaying the oxidation of beef during 7 days ORCID
of refrigeration display, probably due to the antioxidant activity of Behrooz Alizadeh Behbahani https://orcid.
the oil and the ability of the edible coating to minimize the contact org/0000-0002-1447-5088
with oxygen and light (Alizadeh Behbahani & Imani Fooladi, 2018a, Fereshteh Falah https://orcid.org/0000-0001-8991-8755
2018b; Barzegar et al., 2020). Alireza Vasiee https://orcid.org/0000-0002-4395-8695
Oxidation and microbial growth in foods are also associated with Farideh Tabatabaee Yazdi https://orcid.
consumer rejection. As shown in Figure 7, all sensory properties of org/0000-0002-0387-8690
beef samples (odor, color, texture, and overall acceptance), whether
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How to cite this article: Alizadeh Behbahani B, Falah F, Vasiee
physical and moisture barrier properties of Lepidium perfoliatum seed
A, Tabatabaee Yazdi F. Control of microbial growth and lipid
gum biodegradable film with stearic and palmitic acids. International
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