Meat Science 188 (2022) 108799

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Characterization of ginger starch-based edible films incorporated with

coconut shell liquid smoke by ultrasound treatment and application for
ground beef
Yovita Rahmasari , Gökçe Polat Yemiş *
Department of Food Engineering, Faculty of Engineering, Sakarya University, Esentepe Campus, Serdivan 54187, Sakarya, Turkey

A R T I C L E I N F O A B S T R A C T

Keywords: The aim of the present study was to investigate the structural and physicochemical properties of ultrasound-
Ultrasound treatment treated ginger starch-based edible films incorporated with coconut shell liquid smoke (CSLS), and determine
Coconut shell liquid smoke the inhibitory effect of the films against Escherichia coli O157:H7 in ground beef during the storage at 4 ◦ C.
Ginger starch edible film
Ultrasound-treated CSLS-ginger starch films presented a better mechanical, barrier, thermal, and antibacterial
E. coli O157:H7 inactivation
Ground beef
properties. The antibacterial effect of CSLS against E. coli, S. aureus, E. coli O157:H7, Listeria monocytogenes,
Salmonella Enteritidis, and B. cereus increased significantly with ultrasound treatment. The CSLS-films showed
antibacterial activity against E. coli O157:H7 without negatively affecting the sensory attributes of ground beef.
The films containing 15% CSLS reduced E. coli O157:H7 populations by 1.33 log cfu/g in ground beef during the
12-day-storage. The CSLS-starch films effectively inhibited lipid oxidation in the ground beef samples during the
refrigerated storage. These results indicated that ultrasound-treated CSLS-ginger starch film has the application
potential as a novel antimicrobial active packaging for proteinous foods.

1. Introduction
The development of alternatives materials for biodegradable pack­
aging has been recently the subject of many research to meet the
increasing consumer demands and prevent environmental pollution
caused by packaging wastes (Bertotto et al., 2022; Moshood, Nawanir, &
Mahmud, 2021). Edible films and coatings produced from various bio­
polymers have gained great interest since they provide a good barrier
against oxidative and physical stress in biodegradable packaging ma­
terials (Mohamed, El-Sakhawy, & El Sakhawy, 2020). Starch, as an
abundant, inexpensive, and biodegradable edible material that has a
good film-forming ability, is considered one of the most promising al­
ternatives. Being transparent/translucent, odorless, tasteless, colorless,
and having low O2 permeability under low-to-moderate-relative hu­
midity conditions are major attributes of starch based edible films (Su,
Wang, & Wang, 2022). However, starch based edible films have some
limitations, consisting of high-water permeability and poor mechanical
properties. To overcome these drawbacks, several chemical, physical,
and enzymatic methods have been applied to enhance the properties of
starch films (Cheng et al., 2021). Today, the most important commercial
sources of starch are maize, rice, potatoes, tapioca and peas (Zhang,
Rempel, & Liu, 2014). Ginger (Zingiber officinale) is another potential
source of starch, which is grown for medicinal purposes in tropical and
subtropical regions such as China, Indonesia, Nigeria, and mostly India.
Ginger is often processed for its rich oleoresin and essential oil content.
As a result, a significant amount (by weight) of ginger waste is generated
in the herbal medicine and beverage industry. Industrial ginger wastes
have been regarded as biomass for starch production due to their high
starch content (40–59% dry weight) (Gao, Ozel, Dugmore, Sulaeman, &
Matharu, 2021).
Incorporating with different bioactive agents into biodegradable
packing films is a popular strategy for inhibiting of pathogenic and
spoilage microorganisms in food (Chawla, Sivaumar, & Kaur, 2021).
Nanoemulsions are as a new delivery system for encapsulating and
releasing bioactive compounds from edible films into food products
(Ansarian, Aminzare, Azar, Mehrasbi, & Bimakr, 2022; Das, Vishakha,
Banerjee, Mondal, & Ganguli, 2020; Shen et al., 2021). Ultrasound has
been considered an efficient and eco-friendly non-thermal processing
technology for nanoemulsification and starch modification (Cui & Zhu,
2021; Ghazy, Fouad, Saleh, Kholif, & Morsy, 2021; Rahaman et al.,
2021). Previous studies reported that ultrasound could be effective
treatment for improving edible film properties. The reduction in particle

* Corresponding author.
E-mail address: gokceyemis@sakarya.edu.tr (G.P. Yemiş).

https://doi.org/10.1016/j.meatsci.2022.108799
Received 27 October 2021; Received in revised form 27 February 2022; Accepted 7 March 2022
Available online 11 March 2022
0309-1740/© 2022 Elsevier Ltd. All rights reserved.
Y. Rahmasari and G.P. Yemiş
size of emulsions by ultrasound treatment enhances the accessibility of
bioactive agents and can improve the mechanical, water barrier, struc­
tural, and thermal attributes of starch films (Abral et al., 2019; Cheng,
Chen, Liu, Ye, & Ke, 2010; Garcia-Hernandez, Vernon-Carter, & Alvarez-
Ramirez, 2017; Liu et al., 2021; Liu, Wang, Kang, Cui, & Yu, 2018;
Vasco, Campanone, & Gamboa-Santos, 2022; Wang et al., 2020; Wu,
Zhou, Liang, Zhoung, & Xie, 2021). Cheng et al. (2010) examined the
ultrasound effect on physical and mechanical properties of a maize
starch film. Ultrasound treated starch films showed a more cohesive
structure, and had better transparency and tensile strength than that of
without ultrasound treatment. Similarly, Wu et al. (2021) reported that
ultrasonication led to a more compact structure, which might contribute
to the improvement of the mechanical and water barrier properties of
the starch-acetic acid films.
E. coli O157: H7 has been known as a major worldwide food-borne
pathogen which resulted in life-threatening conditions such as hemo­
lytic uremic syndrome (HUS) and thrombotic thrombocytopenic pur­
pura (TTP) (Salaheen et al. 2019). The hospitalization and death rates of
E. coli O157:H7 are higher than other primer pathogen including Sal­
monella or Campylobacter. It is well known that he main source of E. coli
O157:H7 is cattle and the outbreaks of E. coli O157:H7 have been related
to the with undercooked ground beef (Rani, Ravindran, Surapaneni,
Mantri, & Ball, 2021). Many preventive techniques have been developed
and performed to improve the microbial safety of ground beef which is
an important food for human nutrition. Increasing the stability of meat
and meat products by smoking has been adopted since ancient times. In
addition to increasing product durability, smoking has also many ben­
efits such as developing a new taste, odor, color, preventing oxidation,
and obtaining new products. Today, instead of traditional smoking,
which is applied by direct contact of meat products with wood smoke,
liquid smoking has been commonly used in all over the world and has
many advantages such as minimizing the air pollution problem and
being free of polycyclic aromatic hydrocarbons (Holley & Patel, 2005;
Lingbeck et al., 2014). Liquid smoking is frequently applied in the
preservation of protein-based foods such as meat, fish, and cheese, due
to its pleasant flavor and inhibitory effects on food-borne pathogens
(Nithin et al., 2020; Xin, Dell, Udugama, Young, & Baroutian, 2021).
The coconut (Cocos nucifera L.) is an important crop in many countries
like Indonesia, Philippines, India, Brazil, Thailand. Indonesia has the
largest coconut cultivation area in the world. The coconut (C. nucifera L.)
has a great economic importance, due to its large-scale production in
Indonesia (Alouw & Wulandari, 2020). Coconut shell is an agricultural
byproduct generated by the processing of coconut flesh. Cellulose,
hemicellulose and lignin are the primary fractions in coconut shell.
Lignin fraction account for 27% of coconut shell is a good phenolic
source for the production of liquid smoke (Bledzki, Mamun, & Volk,
2010). Coconut shell liquid smoke (CSLS) is industrially obtained from
coconut shell by the pyrolysis and condensation. Phenols, carbonyls, and
organic acids in CSLS are bioactive components of which play a role as
antimicrobial, antioxidant, flavoring and coloring (Kailaku, Syakir,
Mulyawanti, & Syah, 2017; Saloko, Darmadji, Setiaji, & Pranoto, 2014;
Zuraida, Sukarno, & Budijanto, 2011).
Liquid smoke has been considered as an alternative additive for
edible films due to its antimicrobial, antioxidant, coloring, and flavoring
properties. There is a very limited number of studies on the use of liquid
smoke in edible film formulations, although numerous studies on the
direct use of liquid smoke in foods were reported in the literature. Soazo,
Pérez, Piccirilli, Delorenzi, and Verdini (2016) investigated the thick­
ness, transparency, color, antibacterial and mechanical properties of
whey protein concentrate (WPC) based edible films with the addition of
liquid smoke. In subsequent work by the same authors was reported that
the physicochemical characteristics of WPC-based edible films incor­
porated with 10% w/w of liquid smoke were better preserved at 8 ◦ C
(Piccirilli, Soazo, Pérez, Delorenzi, & Verdini, 2019). Similarly, Wang,
Li, Zhang, and Ni (2016) examined the efficacy of liquid smoke on the
mechanical and water barrier properties of gelatin films. To date, there
2
Meat Science 188 (2022) 108799
has not been any study of the application of liquid smoke based edible
films on food and food products. Therefore, the aims of the present study
were (i) to investigate the structural and physicochemical properties of
ultrasound treated ginger starch-based edible films containing different
concentrations of CSLS, and (ii) to determine the inhibitory effect of
CSLS-ginger starch nano-emulsion films against E. coli O157:H7 in
ground beef during storage at 4 ◦ C.
2. Materials and methods
2.1. Materials
Coconut shell liquid smoke (CSLS, Grade 1) and ginger starch were
supplied from Prima Rosandries (Jember, Indonesia) and UKM R-Rovit
(Batu, Indonesia), respectively. The active compounds in CSLS are
phenol (32.61%), 2-methoxyphenol (guaiacol) (5.26%), furfural
(4.38%), 2-methylphenol (1.44%), 2-methoxy-4-methylphenol (0.81%),
and acetic acid (9.53%) which were determined by GC–MS. Glycerol and
Tween 80 were obtained from Sigma-Aldrich (St. Louis, USA). Ground
beef was bought from local butcher shops and kept at 4 ◦ C. The beef
sample was divided into three parts for chemical, microbiological, and
sensory analysis. The ground beef sample used for microbiological
analysis was sterilized by 10 kGy of gamma irradiation at the Turkish
Atomic Energy Authority (Ankara, Turkey), and then stored at − 18 ◦ C.
The sterility of the ground beef samples was tested throughout the
experiment, and there was no detectable contamination of beef samples
over the storage period.
2.2. Preparation of film-forming nanoemulsions
Ginger starch (5% w/v) was dispersed in a double-distilled water and
gelatinized at 90 ◦ C for 30 min. Coarse emulsions were prepared by
mixing the coconut shell liquid smoke at different concentrations (0%,
5%, 10% or 15% v/v) with the ginger starch suspension, glycerol (1.5%
v/v), and Tween 80 (1% v/v). The mixtures were homogenized at
18,000 rpm for 2 min (T25 digital Ultra-Turrax, IKA, Germany). Then,
the coarse emulsions were subjected to ultrasonication using an ultra­
sonic processor (VCX 750, Sonics & Materials, Inc., USA) for 5 min at
80% power amplitudes with a 13-mm-diameter titanium probe. The
minimum inhibition concentration (MIC) and minimum bactericidal
concentration (MBC) values of CSLS for the tested bacteria were pre­
determined in the range from 1 to 3% to 5–10%, respectively (data not
shown). These data were used to determine the concentration of CSLS-
incorporated ginger starch film formulation.
2.3. Particle size of the film-forming solution
The particle size of film forming nanoemulsions were determined by
dynamic light scattering (DLS) with a Zetasizer NanoZS laser diffrac­
tometer (Malvern Instruments Ltd., Worcestershire, UK).
2.4. Film preparation
Emulsions and nanoemulsions were degassed using a bath-type
sonicator to remove the air bubbles. The degassed suspensions (15
mL) were poured into plastic Petri dishes (9-cm-diameter) and dried for
48 h at 25 ◦ C. The dried films were stored in an environmental chamber
(25 ◦ C temperature and 50% relative humidity (RH)) for 48 h before
analysis. Ginger starch films were also made without the addition of
CSLS (ginger starch 5% w/v, glycerol 1.5% v/v, and Tween 80 1% v/v)
and considered as the control.
2.5. Characterization of nanoemulsion-edible films
2.5.1. Film thickness
The thickness values of films were determined using a digital
Y. Rahmasari and G.P. Yemiş
micrometer with an accuracy of ±0.001 mm at ten random points of the
film surface and the mean value was presented.
2.5.2. Color and opacity
The color values of films were measured using a colorimeter (PCE-
CSM 7, PCE Instruments, UK). The film opacity was determined using a
UV–visible spectrophotometer (Shimadzu, UV-1240, Kyoto, Japan) at
600 nm. The opacity of film was obtained by the following equation:
(Sun et al., 2017).
Opacity = A600 /x
A600 = absorbance value at 600 nm, x = film thickness (mm)
2.5.3. Water vapor permeability (WVP)
WVP of the films was determined using the method by Xu et al.
(2018), with some modifications. The films were sealed on plastic cups
(internal diameter: 2.5 cm, external diameter 3.0 cm, depth:10 cm),
containing 20 mL distilled water, and the samples were placed in a
controlled chamber (at 25 ◦ C and 50% RH). The cups were weighed at 2-
h-interval for 12 h using an analytical balance (±0.0001 g). The linear
regressions of the results were performed and the slope was calculated.
The WVP was determined as follows.
WVP = (WVTR x T)/ΔP
WVTR = Water vapor transmission rate (g mm/kPa h m2) was defined as
the slope divided by the film area (m2), T = film thickness (mm), ΔP =
vapor pressure difference across the film (1.585 kPa at 25 ◦ C).
2.5.4. Mechanical properties
The evaluation of tensile strength (TS) and elongation at break (EB)
were carried out using a Texture Analyzer (TA. XT plus - Stable Micro
Systems, Surrey, UK) according to the ASTM standard method D882
(ASTM, 2007). The film strips were cut into rectangular shapes (7 cm ×
2 cm) and placed in a texture analyzer with 5 kg loaded cell. The initial
grip separation and crosshead speed values were set to 50 mm and 2
mm.s− 1, respectively. The stress-strain data determined by the software
were utilized to estimating TS and EB.
2.5.5. DSC
Thermal properties of CSLS films were carried out by a differential
scanning calorimeter (Q-10, TA Instruments, Waters, US). The films
were placed in hermetically sealed aluminum pans and gradually heated
from 25 to 200 ◦ C with a heating rate of 10 ◦ C/min.
2.5.6. FT-IR spectra analysis
The film samples were invstigated using a Fourier transform infrared
(FTIR) spectrometer (Thermo Scientific Nicolet i50, USA). The absor­
bance spectra of the films were recorded in the wavelength range of
4,00− 4,000 cm− 1 with a spectral resolution of 4 cm− 1.
2.5.7. Microstructure
Film morphology was examined by field emission scanning electron
microscopy (FESEM, Quanta 450 FEG, FEI, USA) at 1000 magnification
and accelerating voltage of 5 kV.
2.5.8. Antibacterial activity
2.5.8.1. Bacterial culture. The test bacteria, E. coli, S. aureus, E. coli
O157:H7, Listeria monocytogenes, Salmonella Enteritidis, and B. cereus
were kindly provided by Dr. A. Kadir Halkman (Ankara University,
Department of Food Engineering, Turkey). All bacterial cultures were
stored at − 18 ◦ C in Tryptic Soy Broth with 20% glycerol and cultivated
in Tryptic Soy Broth (TSB, Merck, Germany) at 37 ◦ C for 24 h.
2.5.8.2. Antibacterial efficiency of the edible film solution. The agar well
3
Meat Science 188 (2022) 108799
diffusion method was used to determine the antibacterial activity of
edible film solution. Antibacterial efficiency analysis was carried out
using the agar well diffusion method (Polat Yemiş & Candoğan, 2017).
The adjusted bacterial culture (~105) was inoculated into Tryptic Soy
Agar (TSA, Merck, Germany) and poured aseptically into a sterile Petri
dish. Wells (diameter 9 mm) were punched using a sterile cork borer into
the agar, and the various concentrations of ginger starch-based CSLS
film-forming solutions (100 μL) were transferred into each well. The
dishes were incubated at 37 ◦ C for 24 h. The inhibition zones were
measured in millimeters.
2.6. Application of films on ground beef meat
Ten-gram-portions of ground beef were weighed and shaped into
beef patties. Films were applied to the top and bottom surfaces of the
patties, placed separately in sterile low-density polyethylene bags, and
sealed. A total of 120 samples (five treatments x three replicates x two
samples/replicates x four days) were prepared on different days for
TBARS analyses. A total of 120 samples (five treatments x three repli­
cates x eight panelists) were prepared on different days for the sensory
evaluation. Each treatment was stored at 4 ◦ C for 12 days and sampled at
days of 0, 4, 8, and 12 for the analyses (Emiroğlu, Polat Yemiş, Kodal
Coşkun, & Candoğan, 2010). The application groups consisted of (1) the
control samples (C) (2) the samples coated with ginger starch films
without the incorporation of CSLS (CF), and (3) the samples coated with
ginger starch films with the incorporation of 5, 10, or 15% CSLS (LSF1,
LSF2 or LSF3, respectively).
2.6.1. Antibacterial activity against inoculated E. coli O157:H7
Irritated ground beef was weighed (10 ± 0.1 g portions) aseptically
and formed into beef patties. E. coli O157:H7 culture was grown in TSB
supplemented with 5 g/L yeast extract (TSBYE) for 24 h at 37 ◦ C. Each
sample was inoculated with 500 μL aliquots of the E. coli O157:H7
culture to obtain a final concentration of approximately 4 log cfu/g.
Films were applied to the top and bottom surfaces of the beef patties as
described previously. A total of 105 samples (five treatments x three
replicates x seven days) were prepared on different days. Each treatment
was stored at 4 ◦ C for 12 days and sampled at 2-day-intervals. The
sample was homogenized with sterile 0.1% (w/v) peptone water using a
stomacher (BagMixer®, Interscience, France) for 1 min. Appropriate
serial diluted samples were spread on TSA plates and incubated at 37 ◦ C
for 48 h. The microbial counts were expressed as log cfu/g samples.
2.6.2. Thiobarbituric acid reactive substances (TBARS)
TBARS values were determined using the spectrophotometric
method described by Mielnik, Olsen, Vogt, Adeline, and Skrede (2006).
The absorbance was measured by using a spectrophotometer (Shimadzu,
UV-1240, Kyoto, Japan) at 532 nm. The results were expressed as mg
malonaldehyde/kg meat (mg MDA/kg meat).
2.6.3. Sensory evaluation
The sensory properties of cooked ground beef patties were examined
after 2 days of storage with the contribution of eight semi-trained pan­
elists in meat product evaluation at Department of Food Engineering,
Sakarya University. The sensory evaluation was performed in three in­
dependent sessions, and same panelists were used the sensory sessions.
Panelists were trained to assess the sensory characteristics of the sam­
ples in three training sessions prior to sensory evaluations. The sample
groups were individually cooked on non-sticking pans. The panelists
rated each sample for color, odor, flavor, and general acceptability,
using a 9-point hedonic scale ranged from dislike extremely to like
extremely. Beef samples receiving overall scores higher than 5 were
considered acceptable.
Y. Rahmasari and G.P. Yemiş Meat Science 188 (2022) 108799

2.7. Statistical analysis
The obtained data were analyzed using the ANOVA and Duncan's
multiple range tests, and the level of confidence was determined 95% (P
< 0.05). The SPSS 20.0 Statistics Software (SPSS, Chicago, IL, USA) was
utilized for the statistical analyses. The obtained sensory analysis data
were analyzed using the non-parametric Kruskal–Wallis test. The model
used for statistical analyses of the treatments, storage time, the in­
teractions, and panelists were considered to be as fixed terms, and the
replication of the experiments and sessions as the random terms. The
measurements were performed in triplicate or more. The data were
presented as mean ± standard error.
3. Results and discussions
3.1. Characterization of edible films
3.1.1. The particle size of film-forming solutions
The particle size of the film solution can be affected by the me­
chanical and barrier properties of the film. The mean particle size values
of ginger starch-based CSLS emulsions is given in Table 1. The film so­
lutions showed small particle sizes in the range of 218.43 nm to 242.40
nm with no significant differences in the films with and without CSLS
treatment (P > 0.05). Similar particle size results after sonication have
been reported by Gul, Saricaoglu, Besir, Atalar, and Yazici (2018), and
Chu et al. (2020).
3.1.2. Color and opacity
Table 1 shows the color properties (L*, a*, b*) and opacity of ginger
starch films incorporated with CSLS after ultrasound treatment. A slight
decrease in the lightness parameter (L*) of films was observed, when
CSLS with concentration of 5%, 10% and 15% was added into the film
solutions (P < 0.05). The incorporation of liquid smoke resulted in
increased yellowness and redness in ginger starch films compared to
films without CSLS, as indicated by higher a* and b* values (Table 1).
The incorporation of 10% and 15% concentrations of CSLS to the films
increased both a* and b* values. The characteristic colorless property of
ginger starch-based films changed to light yellow through the addition
of CSLS in increasing concentrations in the edible film formulation (P <
0.05). This finding was in agreement with those in previous studies
reporting that the addition of liquid smoke influenced the color prop­
erties of films depending upon the concentration (Soazo et al., 2016;
Wang et al., 2016). The transparency of film is a significant factor in
food packaging applications, and affects consumer perception. Opacity
values increased when CSLS was added into film formulation, and this
behavior was observed in all evaluated CSLS concentrations (P < 0.05).
The opacity results were similar to those in previous studies reporting an
increase in film opacity with the addition of liquid smoke (Soazo et al.,
2016; Wang et al., 2016). However, in the present study, all films were
still transparent despite the increase in opacity values (Fig. 1). Our
findings could be attributed to the super-mixing effect of ultrasonic
treatment, which provides the homogeneity of starch gel after ultra­
sonication. Previous studies reported that ultrasonic treatment had a
great effect on the structure of gelatinized starch granules. This effect of
ultrasonication was ascribed to the microjets and shock waves produced
by acoustic cavitation, which resulted in of dents and pores at the sur­
face of starch, and increase in solubility and transmittance (Garcia-
Hernandez et al., 2017; Wu et al., 2021).
3.1.3. Mechanical properties
The thickness, tensile strength (TS), and elongation at break (EB)
values of ginger starch films containing CSLS are given in Table 2. Film
thickness ranged from 0.1730 ± 0.0021 to 0.1716 ± 0.0062 mm, and
the addition of CSLS resulted in no significant changes in film thickness
(P > 0.05). The results were consistent with those reported in previous
studies demonstrating that incorporation of liquid smoke at various
concentrations did not significantly affect the thickness of edible films
(Soazo et al., 2016; Wang et al., 2016). The mechanical properties of the
film are very important in maintaining the integrity of a packaged
product. According to the mechanical testing results, both TS and EB
significantly increased compared with the control film (P < 0.05). Films
without CSLS showed a TS value of 14.28 ± 0,71 MPa, and the addition
of CSLS significantly enhanced TS, which yielded 15.81 ± 0,62 MPa for
the films with 10% CSLS (P < 0.05). Also, EB values of films increased
from 27. 5 ± 4.14% to 38.95 ± 4.62% for the films with 15% CSLS. TS
and EB values of ginger starch-CSLS films increased with the increase in
CSLS content, however, no statistically significant differences were
observed among films incorporated with concentration of 5%, 10% and
15% CSLS (P > 0.05). This improvement can be related to the function of
the reactive compounds like carbonyls and phenols in CSLS. This result
was in agreement with those in previous studies reporting that the
addition of liquid smoke enhanced the TS of films, depending on the
concentration of liquid smoke (Soazo, Perez, Piccirilli, Delorenzi &
Verdini, 2016; Wang et al., 2016). It has been also reported in the
literature that phenolic compounds can form intermolecular in­
teractions, and hydrogen bonds with starch and gelatin resulted in
improved mechanical properties of the films (Najwa, Guerrero, De La
Caba, & Hanani, 2020). Morever, Liu et al. (2021) reported that the
ultrasonic treatment provides a significant increase in the TS of the film,
indicating that the ultrasonication contributed to a more compact
structure between film components by the changes of the film matrix. It
has been declared that the strong mechanical force by shock waves
during ultrasonication provided a conversion of starch granules to small
fragments and then an effective interaction at molecular level among the
film components. This conversion formed by ultrasonication could yield
a polymer film with higher tensile strength. (Asrofi, Abral, Putra,

Table 1 CF LSF1 LSF2 LSF3

Particle size, color and opacity values of ginger starch films.
Film Particle size L* a* b* Opacity
samples (nm)

CF 242.40 ± 90.60 ± 1.49 ± 5.47 ± 1.20 ±

2.97a 0.04a 0.01b 0.04b 0.02b
LSF1 222.77 ± 90.30 ± 1.50 ± 5.65 ± 1.34 ±
18.97a 0.05b 0.02b 0.10b 0.13ab
LSF2 234.93 ± 90.28 ± 1.57 ± 6.08 ± 1.47 ±
7.21a 0.06b 0.03a 0.09a 0.05a
LSF3 218.43 ± 90.20 ± 1.61 ± 6.10 ± 1.50 ±
17.7a 0.08b 0.02a 0.06a 0.06a

Results are represented as mean ± standard error. Mean values in each column
with different lower case letter superscripts are significantly different (P < 0.05).
CF: ultrasound treated ginger starch film without CSLS. LSF1, LSF2, LSF3: ul­
trasound treated ginger starch film incorporated with 5, 10, and 15% CSLS,
respectively.
Fig. 1. Physical appearances of the films. CF: ultrasound treated ginger starch
film without CSLS. LSF1, LSF2, LSF3: ultrasound treated ginger starch film
incorporated with 5, 10, and 15% CSLS, respectively.

4
Y. Rahmasari and G.P. Yemiş Meat Science 188 (2022) 108799

Table 2 by ultrasonication. They have shown that the disappearance of the

Thickness. mechanical and barrier properties of ginger starch films. ghosts in the starch film solutions treated by ultrasound caused in a more
Film Thickness Tensile Elongation at WVP (g.mm/ homogeneous matrix.
samples (mm) strenght (Mpa) break (%) m2h.kPa)

CF 0.1730 ± 14.28 ± 0.32b 27.55 ± 1.85b 1.54 ± 0.06a 3.1.5. Water vapor permeability (WVP)
0.0009a The WVP of the ginger starch nano-emulsion films incorporated with
LSF1 0.1720 ± 15.35 ± 0.37a 33.34 ± 2.23a 1.38 ± different concentrations of CSLS was examined at 25 ◦ C. It is known
0.0006a 0.05ab from literature that the starch films have poor moisture barrier prop­
LSF2 0.1716 ± 15.81 ± 0.28a 35.92 ± 1.34a 1.35 ± 0.08b
0.0028a
erties due to their hydrophilic characteristics. Our results showed that
LSF3 0.1724 ± 15.74 ± 0.40a 38.95 ± 2.07a 1.33 ± 0.02b the WVP value for the ginger starch film was 1.54 ± 0.10 g.mm/m2h.
0.0022a kPa, and significantly reduced with the incorporation of CSLS (Table 2).
Results are represented as mean ± standard error. Mean values in each column
But, no statistically significant differences were observed among ginger
with different lower case letter superscripts are significantly different (P < 0.05). starch films produced by adding different concentration of CSLS (P >
CF: ultrasound treated ginger starch film without CSLS. LSF1, LSF2, LSF3: ul­ 0.05). The decreased WVP values in ginger starch-CSLS films could be
trasound treated ginger starch film incorporated with 5, 10, and 15% CSLS, related to the intermolecular interactions between ginger starch and
respectively. CSLS. Wang et al. (2016) also reported that the WVP values of gelatin-LS
films decreased by increasing the content of LS. The addition of LS
Sapuan, & Kim, 2018; Liu et al., 2018). contributed to improving the moisture resistance of the gelatin films.
Several studies have reported that the incorporation of phenolic extract
3.1.4. Microstructure reduced the WVP value of polysaccharide films (Cruz-Gálvez et al.,
The micrographs of the surfaces and cross-sections of the films are 2018; Dhumal, Ahmed, Bandara, & Sarkar, 2019; Mei et al., 2020; Saberi
presented in Fig. 2. The films showed homogeneous structures without et al., 2017). Furthermore, it has been indicated that having less micro-
any large cracks, wholes, or phase separations. These results revealed sized porosities of the polymer films produced by ultrasonic treatment
that CSLS was successfully integrated into the starch-glycerol matrix. It limits the diffusion ability of the water molecule into porous space.
has been reported that ultrasound treatment could disintegrate the (Asrofi et al., 2018; Gul et al., 2018; Vasco et al., 2022).
starch agglomerations, and resulted in the formation of starch matrix
with fewer micro-pores and cracks (Garcia-Hernandez et al., 2017; Wu 3.1.6. Thermal properties
et al., 2021). Wang et al. (2016) reported that gelatin-liquid smoke films The DSC thermograms of ginger starch films incorporated with
exhibited a smooth and homogenous surface, and the addition of liquid different levels of CSLS content are shown in Fig. 3. The films exhibited
smoke had no effect on the film morphology. However, in the same endothermic peaks around 42.7 ◦ C and 183.1 ◦ C. The melting temper­
study, a cross-section of the films demonstrated a slightly coarser ature (Tm) of ginger starch films containing CSLS increased with the
structure in comparison to untreated films. The effect of ultrasonic increase in CSLS content. As seen in Fig. 3, Tm values of ginger starch
treatment on the structure of starch films has been recently reported by films containing 0%, 5%, 10%, and 15% CSLS were 101.6 ◦ C, 104.2 ◦ C,
Liu et al. (2021). The authors noticed that the film surface became more 107.9 ◦ C, and 112.5 ◦ C, respectively (P < 0.05). These results indicated
homogeneous and showed a uniform texture after ultrasonic treatment that strong interactions between CSLS and film components increased
compared to that of the untreated sample. Similarly, Abral et al. (2019) the thermal stability of ginger starch films, and an increased amount of
conducted a study on improving the properties of the sago starch films thermal energy is required to decompose interactions among film

CF LSF1 LSF2 LSF3

(a)

CF LSF1 LSF2 LSF3

(b)

Fig. 2. FESEM micrographs of the cross-section (a) and surface (b) of ginger starch films. CF: ultrasound treated ginger starch film without CSLS. LSF1, LSF2, LSF3:
ultrasound treated ginger starch film incorporated with 5, 10, and 15% CSLS, respectively.

5
Y. Rahmasari and G.P. Yemiş Meat Science 188 (2022) 108799

0.1
Temperature (°C)
0
0 50 100 150 200
-0.1

Heat flow (W/g)

-0.2

-0.3

-0.4

-0.5

Exo Up CF LSF1 LSF2 LSF3

Fig. 3. DSC thermograms of ginger starch films. CF: ultrasound treated ginger starch film without CSLS. LSF1, LSF2, LSF3: ultrasound treated ginger starch film
incorporated with 5, 10, and 15% CSLS, respectively.

components. This behavior was consistent with that observed by Wang
et al. (2016), who reported that the incorporation of liquid smoke
improved slightly the thermostability of gelatin films. A similar trend
was observed for starch films produced by blueberry pomace (Luchese,
Garrido, Spada, Tessaro, & De La Caba, 2018) and cocoa nibs extract
(Kim, Baek, Go, & Song, 2018). Previous studies reported that the dis­
tribution of melting temperature of ginger starch was found to be in the
range of 84.7–86.2 ◦ C (Sukhija, Singh, & Riar, 2016; Li et al., 2020).
However, in the current study, the melting temperature of ultrasound
treated the ginger starch film without CSLS was determined to be
101.6 ◦ C. Similarly, Abral et al. (2019) also reported that the melting
temperature of sago starch films treated by ultrasonication was higher
than that of films untreated by ultrasonication.
3.1.7. FTIR spectra analysis
FTIR spectroscopy was performed to characterize the intermolecular
interaction between film matrix and CSLS. The FTIR spectra of ginger
starch-based films incorporated with different concentrations of CSLS is
exhibited in Fig. 4. FTIR spectra of all ginger starch-based films
demonstrated a similar pattern. The intense broad peak at 3281 cm− 1
was related to the stretching vibration frequency of the hydroxyl groups
(O–H). The peaks at 2927 and 2890 cm− 1 showed the presence of
asymmetric and symmetric stretching of the C–H band for the glucose
unit. The absorption band in 1646 cm− 1, attributed to the free O–H
band stretching, was associated with the residual bound water in the
films due to the hygroscopic nature of starch (Mei et al., 2020). The
signal arriving at 996 cm− 1 was characteristic of the C-O-C stretching
and indicates the presence of α-1,4 glycosidic linkages. A similar

CF

LSF3

LSF2

LSF1

Fig. 4. FTIR spectra of the ginger starch films. CF: ultrasound treated ginger starch film without CSLS. LSF1, LSF2, LSF3: ultrasound treated ginger starch film
incorporated with 5, 10, and 15% CSLS, respectively.

6
Y. Rahmasari and G.P. Yemiş Meat Science 188 (2022) 108799

observation has been reported by Li et al. (2020), and Gao et al. (2021).
The FTIR absorbance bands of ginger starch films exhibited similar
infrared absorption characteristics. It was not observed new absorption
peaks or absorption peak shift. FTIR results showed that the addition of
CSLS did not change the chemical structure of ginger starch films and no
new types of bonds were created during film formation.
3.1.8. Antimicrobial properties
The antibacterial activity of ultrasound-treated and untreated ginger
starch film-forming solutions containing various concentrations of CSLS
against test bacteria is presented in Table 3. All the ginger starch film-
forming solutions without CSLS showed no activity against the tested
bacteria. Similarly, ultrasound-untreated films incorporated with 5%
CSLS (LSF1) had no antibacterial activity against the tested bacteria.
Moreover, increasing the concentration of CSLS in film-forming solu­
tions resulted in significantly higher antibacterial activity (P < 0.05).
This result was consistent with those in previous studies (Kailaku et al.,
2017; Saloko et al., 2014; Zuraida et al., 2011). CSLS contains phenolic
compounds including 2-methoxyphenols (guaiacol), phenol, 4-ethyl-2-
methoxyphenol (EMP), syringol, carbonyls, and organic acids, which
they play a major role in antibacterial activity (Surboyo, Arundina,
Rahayu, Mansur, & Bramantoro, 2019). Antibacterial action mecha­
nisms of phenolic compounds in liquid smoke are based on disrupting
the cell wall, increasing cell membrane permeability, and subsequently
causing leakage of intracellular components. Carbonyls inhibit bacterial
growth by penetrating the cell wall and inactivating membrane-bound
enzymes (Lingbeck et al., 2014). As shown in Table 3, the antibacte­
rial effect significantly enhanced with US treatment (P < 0.05). Cavi­
tation, which is the primary effect of ultrasonication, cause particle size
reduction of film-forming components, and so increase the surface area.
Therefore, the antibacterial activity of CSLS on the tested bacteria
improved after US treatment. These results were in agreement with
smoke may be linked to its source material, chemical composition, and
extraction methods.
3.2. Application of films on ground beef meat
3.2.1. Antibacterial activity against E. coli O157:H7 inoculated in ground-
beef patties
The results of the E. coli O157:H7 growth inhibition in film-coated
and uncoated ground beef samples during the refrigerated storage
period are shown in Fig. 5. The initial population of E. coli O157:H7
(4.27 ± 0.05 log cfu/g) did not significantly change over the 12-day
refrigerated storage in both uncoated and film-coated control samples
(P > 0.05). E. coli O157:H7 counts significantly decreased in the samples
coated with CSLS-incorporated edible films during the whole storage
time (P < 0.05). The antibacterial effect of ginger starch films incor­
porated with CSLS on E. coli O157:H7 was detected, depending on the
concentration of CSLS. Bacterial reduction level in the films containing
CSLS was found to be between 0.28 and 0.65 log cfu/g, depending on the
CSLS concentration at the end of day 2. Moreover, a reduction of 0.40,
0.80, and 1.11 log cfu/g was observed for ground beef samples coated
with 5%, 10%, and 15% CSLS added films respectively after a storage
period of six days. A reduction of 0.44, 0.95, and 1.33 log cfu/g were
determined in the ginger starch films containing 5%, 10%, and 15%
CSLS, respectively, compared to the control group during the 12-day-
storage. The antibacterial effects of liquid smoke on E. coli O157:H7 in
a meat model system were investigated by Estrada-Munoz, Boyle, and
Marsden (1998). Liquid smoke-treated beef patties demonstrated a
5
E. coli O157:H7 (log cfu/g)

those in other recent studies which reported that the conversion of liquid
smoke into nano-form improved antibacterial activity (Ceylan, Unal 4
Sengor, & Yilmaz, 2018; Saloko et al., 2014). In our study, the US-
treated film-forming solution had the highest inhibition zone against
the Gram-positive bacteria among all the tested bacteria. Greater anti­
microbial activity was observed at 15% CSLS against S. aureus followed 3
by B. cereus and L. monocytogenes with inhibition zone diameters 14.67
± 0.58, 14.33 ± 0.58, 14.33 ± 0.58 mm, respectively. These variations
C CF LSF1 LSF2 LSF3

can be due to the differences in bacterial cell wall structures between

Gram-negative and Gram-positive bacteria. Saloko et al. (2014) reported 2
that the nanocapsules of coconut shell liquid smoke showed strong 0 2 4 6 8 10 12
growth inhibition activity against E. coli and P. fluorescens. The different
strains of the same species may vary in susceptibility to liquid smoke
Storage days
(Lingbeck et al., 2014). Whey protein concentrate-based edible film
Fig. 5. Changes in E. coli O 157:H7 counts of ground beef samples during
incorporated with commercial liquid smoke contents of 5%, 10%, and refrigeration storage. C: control samples. CF: samples coated ultrasound treated
15% were effective in inhibiting the growth of L. monocytogenes, ginger starch film without the incorporation of CSLS. LSF1, LSF2, LSF3: samples
whereas failed to prevent the growth of E. coli, Salmonella typhimurium, coated ultrasound treated ginger starch film with the incorporation of 5, 10, or
and S. aureus (Soazo et al., 2016). The antimicrobial activity of liquid 15% CSLS, respectively. Error bars represent standard error.

Table 3
Antibacterial activity of ultrasound treated and untreated ginger starch film-forming solutions containing CSLS.
Film Samples E. coli S. aureus E. coli O157:H7 Listeria monocytogenes B. cereus S. Enteritidis

CF 0.00 ± 0.00d 0.00 ± 0.00e 0.00 ± 0.00d 0.00 ± 0.00d 0.00 ± 0.00e 0.00 ± 0.00d
LSF1 0.00 ± 0.00d 0.00 ± 0.00e 0.00 ± 0.00d 0.00 ± 0.00d 0.00 ± 0.00e 0.00 ± 0.00d
LSF2 10.00 ± 0.00cB 10.83 ± 0.17dA 10.00 ± 0.00cB 10.17 ± 0.17cB 10.50 ± 0.29dAB 10.17 ± 0.17cB
LSF3 11.83 ± 0.17bB 12.00 ± 0.00cB 12.00 ± 0.00bB 12.33 ± 0.33bB 13.00 ± 0.00bA 11.67 ± 0.33bB
US-CF 0.00 ± 0.00d 0.00 ± 0.00e 0.00 ± 0.00d 0.00 ± 0.00d 0.00 ± 0.00e 0.00 ± 0.00d
US-LSF1 10.00 ± 0.00cB 10.33 ± 0.33dB 10.00 ± 0.00cB 10.33 ± 0.33cB 11.17 ± 0.17cA 10.17 ± 0.17cB
US-LSF2 12.00 ± 0.00bB 13.00 ± 0.00bA 12.17 ± 0.17bB 12.33 ± 0.33bB 13.00 ± 0.00bA 11.67 ± 0.33bB
US-LSF3 13.33 ± 0.33aBC 14.67 ± 0.33aA 13.33 ± 0.33aBC 14.33 ± 0.33aAB 14.33 ± 0.33aAB 12.50 ± 0.29aC

The inhibition zone diameters (mm) are given as mean ± standard error.Mean values in each column with different lower case letter superscripts are significantly
different (P < 0.05). Mean values in each row with different lower upper letter superscripts are significantly different (P < 0.05). CF: ginger starch film without CSLS.
LSF1, LSF2, LSF3: ginger starch film forming solution incorporated with 5, 10, and 15% CSLS. US-CF: ultrasound treated ginger starch film without CSLS. US-LSF1, US-
LSF2, US-LSF3: ultrasound treated ginger starch film forming solution incorporated with 5, 10, and 15% CSLS, respectively.

7
Y. Rahmasari and G.P. Yemiş Meat Science 188 (2022) 108799

significant reduction (2.3 log cfu/g) after 3 days of cold storage Table 4
compared to that of the control group. In another study, the addition of TBARS changes of coated and uncoated ground beef samples during 12 days
0.5% liquid smoke reduced the bacterial populations by 1 log cfu/cm2 in storage at 4 ◦ C (mg malonaldehyde/kg).
treated beef samples compared to those in untreated samples (Dima­ Samples Storage time (days)
kopoulou-Papazoglou & Katsanidis, 2017). Xin et al. (2021) also 0 4 8 12
observed that the use of 15% liquid smoke inhibited the microbial
C 0.68 ± 0.02aC 2.69 ± 0.05aB 3.44 ± 0.10aA 3.83 ± 0.34aA
growth in mussel meat with no significant changes in the color and
CF 0.68 ± 0.02aC 1.89 ± 0.09bB 2.02 ± 0.05bB 2.73 ± 0.35bA
textural properties. LSF1 0.68 ± 0.02aBC 0.66 ± 0.02cC 0.72 ± 0.02cB 0.81 ± 0.01cA
LSF2 0.68 ± 0.02aA 0.66 ± 0.01cA 0.71 ± 0.03cA 0.72 ± 0.05cA
3.2.2. Oxidative stability of ground beef patties LSF3 0.68 ± 0.02aA 0.68 ± 0.01cA 0.73 ± 0.01cA 0.73 ± 0.03cA
The lipid oxidation of ground beef samples was evaluated utilizing Results are represented as mean ± standard error. Mean values in each column
the TBARS analysis (Table 4). The highest TBARS value (3.83 ± 0.5 mg with different lower case letter superscripts are significantly different (P < 0.05).
MDA/ kg sample) was observed in uncoated samples (the control Mean values in each row with different lower upper letter superscripts are
group). The TBARS values of film control samples also increased 2.73 ± significantly different (P < 0.05). C: control samples. CF: samples coated ultra­
0.61 mg MDA/kg meat on day 12, however, the values were lower than sound treated ginger starch film without the incorporation of CSLS. LSF1, LSF2,
those of the control throughout the whole storage (P < 0.05). Starch- LSF3: samples coated ultrasound treated ginger starch film with the incorpora­
based edible films have good oxygen barriers. Therefore, the use of tion of 5, 10, or 15% CSLS, respectively.
the control film may have provided physical protection against oxygen.
The TBARS value of coated beef samples was significantly lower than
Table 5
those of uncoated beef samples during storage (P < 0.05). The ground
The effect of CSLS-ginger starch films coating on the sensory properties of the
beef samples coated with 5%, 10%, or 15% CSLS-added films were ground beef samples.
significantly lower than those in the control and the film control sam­
Samples Appearance Odor Color Flavor Overall
ples. The obtained results showed that CSLS was effective on lipid
acceptability
oxidation during storage. The antioxidant properties of CSLS were
C 7.71 ± 7.00 ± 7.52 ± 7.05 ± 7.24 ± 0.05a
associated with its high content of phenolic compounds, carbonyls, and
0.08a 0.08a 0.21a 0.05a
organic acids (Surboyo et al., 2019). Similar results have been reported CF 7.67 ± 6.90 ± 7.67 ± 7.05 ± 7.19 ± 0.19a
that the liquid smoke significantly inhibited lipid oxidation in the beef 0.05a 0.17a 0.13a 0.21a
samples during the storage (Dimakopoulou-Papazoglou & Katsanidis, LSF1 7.62 ± 7.10 ± 7.52 ± 6.95 ± 7.14 ± 0.22a
2017). Estrada-Munoz et al. (1998) also found that the liquid smoke 0.10a 0.39a 0.10a 0.29a
LSF2 7.62 ± 6.86 ± 7.81 ± 6.71 ± 7.00 ± 0.08a
treated precooked beef patties had lower TBARS values at all sampling
0.21a 0.22a 0.17a 0.22a
days and exhibited antioxidative properties. LSF3 7.43 ± 6.76 ± 7.62 ± 6.57 ± 6.86 ± 0.16a
0.22a 0.10a 0.05a 0.22a
3.2.3. Sensory evaluation
Results are represented as mean ± standard error. Mean values in each column
The effect of CSLS-ginger starch films coating on the sensory prop­ with different lower case letter superscripts are significantly different (P < 0.05).
erties of the beef patties is presented in Table 5. The panelists were able C: control samples. CF: samples coated ultrasound treated ginger starch film
to distinguish between the control and the treatment groups based on without the incorporation of CSLS. LSF1, LSF2, LSF3: samples coated ultrasound
the taste, odor, and general acceptability of the cooked ground beef. The treated ginger starch film with the incorporation of 5, 10, or 15% CSLS,
general acceptability scores for samples coated with 5%, 10%, or 15% respectively.
CSLS-added films were lower than those in the control (7.24), however,
no significant differences were found in the general acceptability be­ bacteria significantly enhanced with ultrasound treatment. The same
tween the control group and film-coated groups (P > 0.05). The overall inhibitory effect against E. coli O157:H7 was observed when the CSLS-
acceptability and flavor scores decreased depending on the increase in ginger starch film applied on ground beef, and the concentration was
CSLS concentration in the ginger starch film. However, ground beef a significant factor in inhibiting E. coli O157:H7. In addition, CSLS
samples coated with a ginger starch edible film containing CSLS were effectively inhibited lipid oxidation of the ground beef samples during
considered to be acceptable at all concentrations used in the present the storage period. Sensory evaluations indicated that ginger starch
study. Sensory evaluations indicated that ginger starch films containing films containing different concentration of CSLS can be used without
CSLS at 5, 10, or 15% concentrations can be used with no negative ef­ negatively affecting the sensory attributes of ground beef. Thus,
fects on the sensory qualities of the meat product. Similar results have ultrasound-treated CSLS-ginger starch films appeared to be promising
been reported by Pilevar et al. (2017) who observed the addition of for active antimicrobial packaging applications of meat products.
liquid smoke to minced beef had no adverse effects on the overall
acceptance values. Morey, Bratcher, Singh, and Mckee (2012) have re­
Declaration of Competing Interest
ported that formulation of frankfurters containing liquid smoke at 2.5, 5,
and 10% concentrations did not affect the texture, flavor, and general
The authors have no known competing financial interests or personal
scores of the frankfurters.
relationships to declare that might have appeared to influence the work
reported in this paper.
4. Conclusions
Acknowledgments
In the present study, a novel edible ginger starch-based film incor­
porated with CSLS was developed by ultrasonication. Ultrasound treated
This study was produced from Miss. Rahmasari's MSc thesis and
CSLS-ginger starch films presented a better mechanical, barrier, ther­
funded by Scientific Research Project Unit of Sakarya University (Grant
mal, and antibacterial properties compare to control film. The WVP
No: 2019-7-24-45).
values of ginger starch-CSLS films gradually decreased with the increase
of CSLS content. The films showed a compact and uniform structure with
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