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Journal of Food Processing and Preservation / Volume 45, Issue 11 / e15939
ORIGINAL ARTICLE
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Physicochemical properties and tenderness analysis of bovine meat

using proteolytic enzymes extracted from pineapple (Ananas comosus)
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and jackfruit (Artocarpus heterophyllus) by-products
Aizi Nor Mazila Ramli , Hazrulrizawati Abd Hamid, Farah Hanani Zulki"i, Normaiza Zamri,
Prakash Bhuyar, Nor Hasmaliana Abdul Manas
First published: 09 September 2021
https://doi.org/10.1111/jfpp.15939
Citations: 1
Abstract
Present research investigation aimed to explore the pineapple and jackfruit byproducts, the core and the seed, respectively, as a meat tenderizer. The e#ects of
beef samples treated with bromelain and Artocarpus heterophyllus protease in
four di#erent concentrations (0, 1%, 2%, 3% and 4%) and combination (4%
bromelain and 4% A. heterophyllus protease) were studied. The physicochemical
treated beef samples showed a 13.30 ± 0.30 decrease in the water holding
capacity (WHC), pH 5.47 ± 0.03, moisture content 63.86 ± 0.16 and cooking yield
75.78 ± 0.16 with the increased addition of crude enzyme extract (p < .05). The
cooking loss increased signi$cantly with the concentration of extracted proteolytic
enzymes (p < .05). Microstructural analysis of the treated beef samples
demonstrated the degradation of muscle $bers and the generation of numerous
gaps or space. The sensory evaluation analysis also revealed the acceptance of
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the treated beef sample compared to the untreated sample. The results showed
that the bromelain and A. heterophyllus protease extract from by-products could
be used as an e#ective natural meat tenderizer. The core and seed as (pineapple
and jackfruit) waste by-product could e#ectively improve the tenderization of
tough muscle in beef without disturbing quality parameters, signi$cantly
contributing to the agricultural processing industry.
Practical applications
Pineapple and jackfruit are popular fruits in south-east Asian countries. Pineapple
and jackfruit are good for preserving meats and for helping to $ght bacterial
spoilage. Some plant-based and food-derived ingredients are more e#ective than
others when maintaining the freshness of a product as long as the meat is not
harmed. Proteolytic enzymes boost the fragmentation of myo$brils in meat and
aid in the degradation of the intramuscular connective tissue structure.
Combining pineapple and jackfruit by-products can be a most e#ective tenderizer
for the meat as an actual preservative without impeding the natural quality or
freshness.
1 INTRODUCTION
Meat, which is animal "esh or tissue eaten as food, is considered an essential
product in some countries with high consumption rates (Guerrero et al., 2013).
Besides being an essential source of dietary protein, meat provides other biological
values such as vitamins, minerals, and other bioactive compounds. In addition, it also
supplies fatty acids, including saturated fatty acids (SFA), unsaturated fatty acids
(USFA), omega-3, cholesterol, triacylglycerol and phospholipids (Hathwar
et al., 2012). Meat tenderness is long known as the highest quality feature for the
acceptability of fresh consumer meat (Mennecke et al., 2007). The tenderness of
meat has a signi$cant impact on customer satisfaction and, as a result, enhances
consecutive purchases (Grunert et al., 2004). The quality of meat can be contributed
by several properties, including tenderness, color quality, water-holding capacity,
cooking losses, and texture. Other critical factors that can in"uence meat value are
eating quality, tenderness, "avor, and juiciness (Istrati et al., 2012). A previous study
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reported that tenderness is the most determinant of palatability characteristics
among consumers (Shackelford et al., 2001). Thus, to improve customer satisfaction
and increase the market potential for meat products, the industry needs to supply
high-quality meat with consistent tenderness. However, the inconsistency in beef
tenderness continues to be a challenge faced by the industry due to the di#erent
tenderness properties among bovine muscles from various anatomical locations and
the dissimilarities in the structural components which can in"uence tenderness (Von
Seggern et al., 2005).
Several strategies have been implemented to improve meat tenderness, thus making
it more palatable. Conventional methods such as modi$ed online carcass suspension
method (Aalhus et al., 2000), prerigor skeletal separations (Shanks et al., 2002),
pressure treatments (Palka, 1999), electrical stimulation (Claus et al., 2001), blade
tenderization (Pietrasik et al., 2010) and chilling improvement (Janz et al., 2004) have
been used to improve the meat tenderization. There have also been attempts to
tenderize meat by calcium chloride injection chemically (DeYonge-Freeman
et al., 2000), phosphates, salts (Pietrasik et al., 2010) as well as enzymes treatment
(Ashie et al., 2002; Gerelt et al., 2000). Each of these strategies has been shown to
have varying degrees of activity against a di#erent type of meat. Meat tenderization
by proteolytic enzymes originating from plants, bacterial, and fungal sources are
gaining popularity. However, plant proteolytic enzymes, such as papain, bromelain,
and $cin, are superior to bacterial-derived enzymes, which are primarily due to
microbial enzymes’ safety problems, including pathogenicity or other unfavorable
e#ects (Bhuyar, Rahim, Maniam, et al., 2020; Naveena et al., 2006).
The fruit waste accumulates over the year; using it to make essential compounds
helps to reduce the total amount of waste produced. Fruit waste is produced in
signi$cant numbers as a result of agricultural operations. Pineapple, jackfruit, citrus,
banana, apple, and pear residues leftover from industrial processing are examples of
such litter (Bhuyar, Maniam, et al., 2021; Ramli, Badrulzaman, et al., 2021; Ramli, Binti
Muhammad Sukri, et al., 2021; Ramli et al., 2020). Bananas, apples, and pears
produce around 107.1, 75.5, and 24.0 million tons per year, respectively, and 25%–
40% of this mass is wasted after processing. Fruit waste is used as cow feed, but it is
not a high-value feedstock due to its low protein content; thus, much of it is in
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land$lls or the ocean. These disposal methods may generate environmental issues
because fruit waste is high in sugars, antioxidants, and other nutrients. The fruits
also contain many enzymes that can be used for food preservation and meat
tenderizer (Bhuyar, Rahim, Sundararaju, Ramaraj, et al., 2020; Choi et al., 2015; Gupta
et al., 2019).
Proteolytic enzymes were reported to increase the fragmentation of myo$brils in
meat and aid in the degradation of the intramuscular connective tissue structure.
Bromelain is found naturally in di#erent parts of the pineapple plant, including fruit,
core, stem, pulp, peels and leaves (Ramli et al., 2017). Bromelain is a proteolytic
enzyme from the pineapple plant, Ananas comosus, that had been used traditionally
to tenderize meat, including beef (Ketnawa & Rawdkuen, 2011), mutton (Bille &
Taapopi, 2008), chicken (Koide et al., 2010) and pork (Ieowsakulrat et al., 2011).
Bromelain, which is categorized in the sulfhydryl proteolytic enzymes group, works
on myo$brillar proteins by hydrolyzing the structure of myosin and actin $laments.
Furthermore, United States federal agencies recognize bromelain together with
papain, $cin, as generally recognized as safe (GRAS) to improve meat tenderness
(Sullivan & Calkins, 2010). Jackfruit, Artocarpus heterophyllus, is latex and seasonal
fruit-producing tree which belongs to the family of Moraceae and genus Artocarpus
Lam. Though it was originally from India, this tree grows wild in East Asia’s tropical
areas, including Malaysia. As far as we are concerned, lack of prior research studies
on the analysis of proteolytic enzymes produced from di#erent part of the Jackfruit.
In addition, the tenderization e#ect of the proteolytic enzyme from jackfruit and its
combination with bromelain also least explored. Currently, higher demand in fruitprocessed-items leads to the escalation of production processes which consequently
resulted into huge generation of agricultural waste. This is generally owing to the
selection and removal of fruit components unsuitable for human consumption.
Typically, agricultural wastes are easily exposed to microbial spoilage thus limiting
further exploitation. Therefore, the aim of this study is to explore the added value of
the pineapple and jackfruit byproducts; the core and the seed, respectively, to be
used as a meat tenderizer.
2 MATERIALS AND METHODS
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2.1 Sample preparation
2.1.1 Bromelain extracts preparation from pineapple core
The pineapple (A. comosus) samples used throughout this research were obtained
from the local variants around Pahang, Malaysia: Josepine, Sarawak, MD2, Philippine
and Morris. Initially, 100 g of the pineapple core was cut into small pieces and were
weighed using the analytical balance, followed by crushing in a food processor
containing 500 ml of 0.05 M of phosphate bu#er (pH 7.5). The extract was $ltered
through a double-layered muslin cloth to remove the solid parts. The $ltrate was
then collected and centrifuged at 10,000×g at 4℃ for 20 min to remove the
remaining residue. The crude supernatant of bromelain was collected and stored at
−20℃ until further use.
2.1.2 Proteolytic extracts preparation from ripe and unripe jackfruit
The fruit sample of A. heterophyllus that was used in this research was “nangka
madu”. The fruits were obtained from the local jackfruit orchard located around
Pahang, Malaysia. Both ripe and unripe jackfruit samples (seed, skin, inner part) were
used in this research study. Each part was cut into small pieces. A total of 100.0 g was
weighed for each part by using an electronic balance. The extraction method was the
same for each part of the jackfruits. The sample was crushed in a food processor
containing 500 ml of 0.05 M of phosphate bu#er (pH 7.5). The mixture was then
$ltered by using a double-layered muslin cloth, and the solid parts were removed.
Filtration was carried out to discard the $brous materials, and the $ltrate containing
protein was collected. Next, the $ltrate was centrifuged at 10,000×g at 4℃ for
20 min. The supernatant was collected and stored at −20℃ until further use.
2.2 Proteolytic analysis of di#erent pineapple variants and
jackfruit samples
The incubation temperature in this enzyme assay was 37℃. 5 ml of casein solution
(0.65% [wt/vol]) was added to the test tubes, followed by incubation at 37℃ for
5 min. A total volume of 1 ml of bromelain solution was added to the test tube and
incubated for 10 min. After that, 5 ml TCA (110 mM) solution was added to the
mixture reaction, including control. The tubes were incubated for 30 min and
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subjected to centrifugation at 6,000×g for 5 min. The supernatant was transferred
into new tubes, and 5 ml Na2CO3 (500 mM) was added, followed by 1 ml Folin &
Ciocalteu’s Phenol Reagent. After centrifugation at 6,000×g for 5 min, the absorbance
value of the supernatant was obtained at 660 nm. This enzymatic assay was obtained
in triplicate. The proteolytic activity can be determined in terms of Units/ml activity,
indicating the amount of tyrosine in micromole equivalents released from casein per
minute (Bhuyar, 2017; Bhuyar, Rahim, Sundararaju, Maniam, et al., 2020).
2.3 Marination of meat samples by bromelain extract
Fresh boneless meat was purchased from a local store and cut into cubes of the
same size and weight before being treated with bromelain solutions of varying
concentrations (1%, 2%, 3%, and 4%). The meat sample obtained was identi$ed as
beef meat from cattle (Tulang Lembu). The meat samples were labeled as a control
(untreated meat: 0%) and bromelain treated samples at di#erent concentrations. All
the experimental analysis of treated beef cubes was done in triplicates.
2.4 Physicochemical properties determination
2.4.1 Water-Holding Capacity (WHC)
Water-holding capacity (WHC) determination was conducted using a method
described by Wardlaw et al. (1973). Beef cubes (6 g) were prepared using di#erent
bromelain and A. heterophyllus protease (1%, 2%, 3%, and 4%). Untreated beef cube
was used as a control. All the beef samples were mixed with 10 ml of 0.6 M sodium
chloride (NaCl) solution in a centrifuge tube and stirred with a glass rod for 1 min.
The tubes were then incubated at 4℃ for 15 min and stirred again for 1 min,
followed by centrifugation at 10,000×g at 4℃ for 15 min. After centrifugation, the
volume of the supernatant was measured, and the water-holding capacity of the
treated and untreated beef was calculated using the formula:
2.4.2 Measurement of pH
Beef cubes were weighed (2 g) accurately and treated with di#erent bromelain and A.
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heterophyllus protease solution (1%, 2%, 3%, and 4%) in test tubes. A test tube
without bromelain served as a control. The samples were incubated for 10 min at
room temperature and homogenized by grinding and then crushing mechanically
using a mortar and pestle. The pH of the samples was measured by a pH meter. The
pH meter was initially calibrated with pH 7 and pH 4 bu#ers before being used in pH
determination (Bhuyar, Sundararaju, et al., 2021).
2.4.3 Moisture content
For determination of the moisture content, 5 g of beef cubes (treated with 1%, 2%,
3% and 4% of bromelain and A. heterophyllus protease solution) and control samples
(untreated) were suspended in 10 ml of 0.6 M sodium chloride (NaCl) solution for
30 min. The weight of the samples was measured using an analytical balance. The
beef cubes were then placed on an aluminum foil and heated (100℃) for 20 min
using a hot plate. The weight of the beef cubes (treated and untreated) after
removing moisture was determined. Percentage of moisture content in the meat
samples were calculated as the following:
2.4.4 Cooking yield
The beef cubes were weighed accurately (5 g). The samples were cooked for 1 min at
100℃ and then cooled at room temperature. The cooked sample was reweighed
using an analytical balance. The cooking yield was calculated by the di#erence in raw
and cooked weights as follows: (Brugiapaglia & Destefanis, 2012):
2.4.5 Cooking loss
The beef cubes were prepared and weighed accurately just before cooking (5 g).
Immediately after cooking, the samples were cooled and weighed. According to
Sultana et al. (2009), the cooking loss was calculated as the following equation:
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2.4.6 Textural properties
The beef sample texture was analyzed using an electronic universal testing machine
(VEW-20, Victor) with a 10 mm/min crosshead speed. Three rectangular samples of
bromelain treated and untreated bromelain raw beef with dimensions of 20 × 20 ×
25 mm (width × length × height) were prepared. The room conditions were
controlled at 25℃ and 34% humidity. The load-displacement values were reordered
for further analysis.
2.4.7 Microstructure property using a scanning electron microscope
(SEM)
In the present study, the samples’ microstructures were observed using a Scanning
Electron Microscopy (SEM) (FEI QUANTA 450) at an accelerating voltage of 15 kV.
Cross-sections of all samples were $xed with 2.5% (vol/vol) glutaraldehyde in a 0.2 M
phosphate bu#er (pH 7.2) for 2 hr. After that, the samples were dehydrated with
increasing alcohol concentrations (20%, 40%, 60%, 80%, and 100%) for 10 min each.
The samples were air-dried by keeping the samples in a fume hood. Lastly, the
samples were sputter-coated with a thin layer of platinum in double 30 s consecutive
cycles at 45 mA to reduce charging and produce conductive surfaces (BALTEC SCD
005 Sputter Coater—BALTEC).
2.4.8 Sensory evaluation
The sensory evaluation was carried out based on a 5-point hedonic scale method, as
proposed by (O’Sullivan, 2016). A survey was conducted among Universiti Malaysia
Pahang (UMP) students and sta#. Totally 10 participants were chosen randomly. The
survey was performed in an isolated room to minimize external factors such as
noise, which might a#ect the sensory evaluation. The survey was carried out to check
the tenderness and toughness of the meat after being treated with the best enzyme
extracts. The meat samples were marinated with the enzyme extracts for 30 min and
then cooked for 8 min. The ten participants were given two di#erent samples of
meat (treated and untreated meat samples). A form of the survey was given to each
of them, and they had to evaluate these meat samples regarding appearance, taste,
texture, aroma and acceptance, with $ve taste scales, starting from score 1 indicate
like signi$cantly to score 5, which indicate dislike highly. At the end of the sensory
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evaluation, the panelists need to choose which meat samples were better between
the two provided.
2.4.9 Statistical analysis
The resulting data were statistically analyzed using the SPSS analysis of variance
(SPSS version 12.0 for Windows, SPSS Inc., Chicago, IL, USA). Duncan’s multiple range
test was used to analyze the di#erence between means. The signi$cance for all
comparisons was determined at the p < .05 level. Experiments were conducted in
triplicate.
3 RESULTS AND DISCUSSION
3.1 Bromelain analysis from di#erent variants of A. comosus
A di#erent A. comosus: Josepine, Sarawak, MD2, Philippine and Morris were collected
from di#erent places in Malaysia. Each variant is di#erent: skin color, size and shape,
and the amount and size of spines. These di#erences could contribute to the
dissimilarity in the amount of protein content for each sample. Josepine’s skin is
much darker than other varieties, almost black with more prominent and lesser
spines. Its body size is smaller than other variants of pineapple. MD2 has bright
yellow skin and smaller and lesser spines, and it has the most robust smell among
the other varieties. This type of pineapple also produces smaller fruit sizes. Sarawak
variety has the most signi$cant size with brighter orange skin color and more spines.
Morris’s size is considered signi$cant, but it is usually much smaller than Sarawak,
usually known as Queen Pineapple (Yuris & Siow, 2014). Morris variant usually
produces yellowish-brown fruit with more prominent spines. Philippine’s body
contains greenish-yellow skin, which is smoother than others and in moderate size.
Extracting crude bromelain from the core part is more di&cult than the "esh part
due to the husk content in the core that is higher than the "esh part with lower
moisture content. All $ve varieties of A. comosus have a core diameter range from 1.5
to 2.3 cm. Sarawak species has the biggest core diameter, while Josephine and Morris
have the smallest comparatively. Determination of enzyme activity is essential for
$nding out the actual proteolytic activity and any application purpose. The activity of
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an enzyme can be assayed either by substrate utilization method or product
formation method. A protease activity assay was done to determine bromelain
activity from di#erent varieties of A. comosus (Figure 1a). From the enzymatic
analysis, MD2 gave the highest activity of bromelain, which is 0.5486 units/ml
followed by Josepine (0.5008 units/ml), Philippine (0.3813 units/ml), Morris (0.3015
units/ml), and Sarawak (0.2940 units/ml).
FIGURE 1
Open in !gure viewer
 PowerPoint
(a) Protease activity assay to determine the activity of bromelain from di#erent varieties of Ananas comosus.
(b) Protease activity assay to determine the proteolytic activity from di#erent parts of Artocarpus heterophyllus
fruit
3.2 A. heterophyllus protease analysis from di#erent parts
Di#erent parts of ripe and unripe A. heterophyllus, including seed, skin and inner part,
were used in the proteolytic analysis. Ripe A. heterophyllus produced pleasant smells
compared to unripe A. heterophyllus. The cotyledon of ripe A. heterophyllus seed was
enclosed by a thin brown spermoderm; meanwhile, the cotyledon of unripe seed was
enclosed by white spermoderm. In addition, the colour of the ripe skin was much
brighter (bright yellow skin) than unripe skin. The inner part of ripe A. heterophyllus
has appeared in dark yellowish colour. It is edible, and people also consumed ripe
inner parts due to its sweet taste. However, the unripe inner part has appeared in
white, and it is tasteless. Each part of both ripe and unripe A. heterophyllus contained
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a certain amount of protease. Thus, a protease activity assay was carried out to
determine the proteolytic activity for each di#erent component of the A.
heterophyllus fruit.
Figure 1b shows that ripe seed exhibited the highest proteolytic activity, 0.2955
units/mL, followed by ripe inner, which is 0.2369 units/ml. The enzymatic activity for
unripe skin is 0.1547 units/ml, followed by mature skin with its enzymatic activity of
0.1401 units/ml. Unripe inner and unripe seed shows the lowest protease activity,
0.1188 and 0.0997 units/ml, respectively. Generally, all the ripe parts of A.
heterophyllus exhibits higher proteolytic activity compared to the unripe parts. To the
best of our knowledge, no studies were reported on the proteolytic analysis of
di#erent parts of ripe and unripe jackfruit, A. heterophyllus. Usually, the fruit is
consumed due to its delectability; however, the seed is often discarded. Thus, it was
interesting to see the potential of the A. heterophyllus by-products as a meat
tenderizer.
3.3 Physicochemical properties determination of meat
3.3.1 Assessment of WHC, pH and moisture content
Zayas (1997) determined that water holding capacity (WHC) is the food’s ability to
hold existing water and the added water during the forces, pressing, centrifugation,
or heating processes. In addition, WHC also has been categorized under the physical
property and a food structure ability to avoid water losses from its three-dimensional
structure (Wallingford & Labuza, 1983). The determination of WHC in meat is
essential since several physical properties, including color, texture and $rmness, are
partially reliant on the WHC (Ketnawa & Rawdkuen, 2011). In this experiment, a
signi$cant reduction of WHC is observed in all treated meat samples, signi$cantly
when the concentration of bromelain and A. heterophyllus protease extracts
increased, as presented in Table 1 (p < .05). The highest WHC value was found in the
untreated sample (control). The highest and the lowest WHC values of treated
samples obtained were from the beef cube samples treated with 1% and 4% of both
bromelain and A. heterophyllus protease, respectively (Table 1). The lowest WHC
values were observed in the beef sample treated with a combination of 4%
bromelain and A. heterophyllus protease compared with others. The treated beef
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sample with 1% bromelain showed the highest WHC value. Compared to the
untreated sample, reducing the WHC value in treated samples can be possibly due to
proteolytic enzyme action on the myo$brillar proteins, thus leading to protein
denaturation. Generally, in the muscle structure, water is entrapped in the intra- and
extra- myo$brillar spaces of cells (Hu#-Lonergan & Lonergan, 2005). The increase or
decrease in WHC may a#ect vice versa. The decrease in water holding capacity
a#ects loss of pro$t for the meat seller, and the increased cooking loss a#ecting the
customers to get less meat in their pan. Bromelain is suggested to hydrolyze these
myo$brillar proteins in the muscle into simpler components that in"uence the
changes in the cell’s intracellular architecture, consequently a#ecting the ability of
muscle cells to retain water.
TABLE 1. Physicochemical properties of beef samples treated with bromelain and
Artocarpus heterophyllus protease extract at di#erent concentrations
Sample
pH
WHC (%)
Properties
Cooking
moisture (%)
yield
Cooking loss
A. comosus
Bromelain
0%
6.01 ± 0.04
36.7 ± 0.06
71.17 ± 0.01
96.18 ± 0.06
3.82 ± 0.06
1%
5.32 ± 0.12
26.95 ± 0.01
71.02 ± 0.06
90.88 ± 0.18
9.12 ± 0.18
2%
5.22 ± 0.02
21.19 ± 0.01
69.46 ± 0.07
82.50 ± 0.16
17.5 ± 0.16
3%
5.12 ± 0.05
21.07 ± 0.01
66.57 ± 0.01
79.86 ± 0.04
20.13 ± 0.04
4%
4.83 ± 0.08
20.95 ± 0.01
65.98 ± 0.01
76.35 ± 0.09
23.65 ± 0.09
1%
5.97 ± 0.02
23.30 ± 0.06
70.32 ± 0.04
92.26 ± 0.19
7.74 ± 0.19
2%
5.96 ± 0.02
20.00 ± 0.00
67.97 ± 0.12
90.88 ± 0.11
9.12 ± 0.11
A. heterophyllus
protease
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3%
5.91 ± 0.04
16.72 ± 0.12
66.78 ± 0.11
89.28 ± 0.13
10.72 ± 0.13
4%
5.85 ± 0.06
16.70 ± 0.06
64.24 ± 0.11
88.28 ± 0.07
11.72 ± 0.07
Combination
5.47 ± 0.03
13.30 ± 0.30
63.86 ± 0.16
75.78 ± 0.16
24.22 ± 0.14
4% A. comosus
bromelain and
In addition, the $nal pH value also plays an essential role in the WHC of meat. The
reduction in WHC in all treated samples might be due to a lower pH value (Ketnawa &
Rawdkuen, 2011). In this study, a signi$cant reduction in pH was observed in all
bromelains, and A. heterophyllus protease treated samples compared to the
untreated sample (Table 1). The pH was found to be decreased signi$cantly with the
increasing concentration of bromelain and A. heterophyllus protease. The decrease in
pH of the treated sample with 1%–4% of each bromelain and A. heterophyllus
protease ranges are between 5.32 to 4.83 and 5.97 to 5.85, respectively, while the
beef sample treated with the combination of 4% bromelain and A. heterophyllus
protease gave the pH value of 5.47. The lowest pH was found in the sample treated
with 4% bromelain (pH4.83), while the highest was found in the untreated beef
sample (pH6.01). Gradual increase in bromelain and A. heterophyllus protease
concentration results in a pH decrease, making the treated meat sample more acidic.
Previously, the WHC was found to increase markedly with decreasing ultimate pH,
reducing the electrostatic repulsion between the $laments (den Hertog-Meischke
et al. (1997)). This phenomenon causes the water movement from the myo$lament
space into the extracellular space, thus leading to myo$brillar shrinkage. Therefore,
the rate of the pH decrease is an essential determinant of WHC (Hu#-Lonergan &
Lonergan, 2005). Other than WHC, the pH value in the meat product is also highly
important because it has a signi$cant in"uence on other quality and physicochemical
properties, including tenderness and juiciness (Goli et al., 2007).
It was found that the moisture content of the treated samples of beef with extracted
bromelain from the core part decreased considerably compared to the untreated
sample, as shown in Table 1 (p < .05). The beef sample treated with the combination
of 4% bromelain and A. heterophyllus protease gave the lowest moisture content of
63.86%, followed by 64.24% and 65.98% when treated with 4% bromelain and 4% A.
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heterophyllus protease, respectively. The control beef sample contains the highest
moisture content of 71.17%. A comparable $nding was reported by Sultana
et al. (2009), which reported a signi$cant decrease in the moisture content of treated
beef from 75.8% to 68.77%. Nadzirah and his coworkers (2016) also reported a
similar $nding of reduced moisture content in bromelain treated beef compared to
the control. Huang et al. (2011) reported that the water content in meat is primarily
located within the structure and cells of muscles. Thus, the degradation of
myo$brillar protein muscle by the action of bromelain triggered the muscle structure
destruction, leading to the decrease in the percentage of moisture content in treated
beef samples.
3.3.2 Cooking yield and cooking loss
All the cooking yields of the treated samples were signi$cantly low compared to the
untreated sample (p < .05). As shown in Table 1, it was found that with the increase
of bromelain and A. heterophyllus protease concentration in the samples, the cooking
yield decreased. For bromelain treated sample analysis, the sample treated with 1%
bromelain shows the highest cooking yield percentage of 90.88%, followed by the
samples treated with 3%, 2%, and 1% bromelain the percentage value of 82.50%,
79.86% and 76.35%, respectively. A similar trend was observed for the beef sample
treated with A. heterophyllus protease, where 1% enzyme extract treatment gave the
highest cooking yield (92.26%), followed by 2% (90.88%), 3% (89.28%), and 4%
(88.28%) enzyme concentration. However, the lowest cooking yield for all treated
samples was observed in a beef sample treated with the combination of 4%
bromelain and 4% A. heterophyllus protease (75.78%), while the most considerable
value of cooking yield was exhibited in an untreated beef sample that served as a
control (96.18%). This result implies that thermal treatment removes more water
from the treated beef samples than the untreated sample. It is suggested that the
protein hydrolysis e#ect is more potent in the sample treated with a higher
concentration of bromelain. Compared to the untreated sample, the reduced
cooking yield in the treated sample may be caused by the degradation of
sarcoplasmic and myo$brillar proteins in the muscle meat. Ketnawa and Rawdkuen
(2011) studied the e#ects of bromelain extract from pineapple peels on beef, chicken
and squid, and it was found that all marinated meat samples with bromelain extract
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showed a reduction in cooking yield.
On the other hand, the percentage of cooking loss was inversely proportional to
cooking yield (p < .05). The cooking loss for treated beef was increased signi$cantly
from 9.12% to 23.65% and 7.74% to 11.72% after treatment with 1% to 4% bromelain
and 4% A. heterophyllus protease, represented in Table 1. The lowest percentage of
cooking loss was detected in untreated beef samples (3.82%), while the highest
percentage was observed in the beef sample treated with the combination of 4%
bromelain and 4% A. heterophyllus protease (24.22%). This $nding was in agreement
with Nadzirah et al. (2016), which found that bromelain produced from pineapple
crowns increases beef’s cooking loss value which is also supported by Klinhom
et al. (2011), which reported an increase of untreated beef from 36.55% to 42.90%
after the beef was treated with 0.05 M citric acid followed by the cooking process at
70℃. Temperature rise during the cooking process resulted in the denaturation of
myo$brillar proteins, especially the actomyosin complex part, leading to the
shrinkage of the muscle $ber. This condition causes water loss from tissue because
the myo$brils weaken the ability to hold water (Murphy & Marks, 2000; del Pulgar
et al., 2012). Furthermore, the beef with proteolytic enzymes is suggested to cause
the denaturation of myo$brillar proteins in muscle, which results in structural
changes, thus causing the cooking loss of meat to increase. The resulting data was
obtained from the physicochemical properties (pH, WHC, moisture content, cooking
yield and cooking loss) of beef samples treated with di#erent bromelain, A.
heterophyllus protease, and combination of both extracts textural and microstructure
properties were performed, followed by sensory evaluation.
3.3.3 Textural properties
The beef sample treated with both extracts (4% bromelain and 4% A. heterophyllus
protease) and the untreated beef sample were then selected for textural properties
analysis. Figure 2 shows the textural properties such as compress strength and
elongation at the break of treated and untreated samples. The mechanical
properties, such as the data of load and elongation, are summarized in Table 2.
Compared with the bromelain untreated samples, the load and elongation at break
are reduced from 101.04 to 46.5 kN and 9.35 to 8.95 mm, respectively. The high force
load stress observed in untreated bromelain samples speci$es the toughness of the
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meat, where more connective tissues are presented. When the applied stress
increases, the dislocation of intramuscular connective tissue also increased, as
observed in the sample chemically treated by bromelain enzyme due to the reduced
amounts of connective detective tissue before the action of proteolytic enzymes on
myo$brillar proteins (Kumar et al., 2011; Manohar et al., 2016). This $nding agrees
with Ketnawa and Rawdkuen (2011), which con$rmed a signi$cant reduction in
roughness values of treated samples with the increased bromelain concentration
from 3% to 20% (wt/wt).
FIGURE 2
Open in !gure viewer
 PowerPoint
The textural properties of treated and untreated beef samples
TABLE 2. Sensory score of combination of bromelain and Artocarpus heterophyllus
protease tenderizer on the sensory attributes of beef sample based on a hedonic
scale
Sample
Appearance
Taste
Texture
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Aroma
Acceptance
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Control
1.97 ± 0.556
2.03 ± 0.765
1.87 ± 0.730
2.10 ± 0.803
1.77 ± 0.774
Treated
1.80 ± 0.551
1.87 ± 1.252
1.53 ± 0.860
1.73 ± 0.944
1.50 ± 0.572
3.3.4 Microstructure properties
Scanning electron micrograph (SEM) of the treated beef combined with 4% bromelain
and 4% A. heterophyllus protease and untreated beef (control) provided additional
physical evidence for the structure organization changes of the meat before and
after treatment. Figure 3(a) shows the microstructure of the untreated beef samples
where all the muscle $bers had a well-organized structure and were closely bound to
each other. Whereas Figure 3(b) depicts the muscle $bers in the di#erent bundles of
the treated sample are broken, not well attached and has a loss of interaction.
Furthermore, the inter$brillar space between muscle $bers is more signi$cant in the
treated sample, which could be due to the degradation of muscle $bers and
connective tissue layers surrounding muscle $bers and the degradation of cell
membranes. The microstructure properties of the treated and untreated samples
showed a strong correlation with the previous results in terms of textural properties
and can become the evidence to improve the meat tenderization process. Similar
microstructure properties have been found in the bu#alo muscle treated with the
ginger extract (Naveena et al., 2004). SEM analysis revealed that the treatment broke
muscle $bers into di#erent bundles and enlarged the bundles’ space. In addition,
there was obvious structure deformation and disruption detected in beef, chicken
and squid samples treated with bromelain extracted from the pineapple peels, which
involve broken tissue $bers, degraded cell membranes, loss of connections between
the sarcolemma as well as the myo$brils and the formation of more gaps (Ketnawa &
Rawdkuen, 2011).
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FIGURE 3
Open in !gure viewer
 PowerPoint
Microstructure of the beef samples at magni$cation of 500× (a) untreated (control) and (b) treated with 4%
bromelain and 4% Artocarpus heterophyllus protease extract
3.3.5 Sensory evaluation
The primary purpose of the sensory evaluation was to give more detailed
information on the acceptability of the formulated meat tenderizer to the consumer.
This method enables the panelists to evaluate the softness, taste and palatability of
the meat. Data on the sensory evaluation of beef containing a combination of 4%
bromelain and 4% A. heterophyllus protease as a tenderizer and untreated beef
(control) are presented in Table 2. From the analysis, most panelists preferred
treated meat samples (a combination of 4% bromelain and 4% A. heterophyllus
protease) compared to the untreated sample. All the attributes’ scores for the
treated sample were higher than the control sample. The texture was the most vital
attribute to consider in this sensory evaluation. A combination of bromelain and A.
heterophyllus protease had a tenderizing e#ect on the beef samples. The treated beef
sample provided the tender meat compared to the untreated sample. The level of
tenderness was excessive, leading to a relatively high taste, aroma, and acceptance
score. Regarding appearance, the presence of a tenderizer makes a slight di#erence
beyond the color contribution. The appearance had a minuscule percentage
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compared to other criteria as the meat was not marinated with anything other than
the combination enzyme extract itself. The score would probably be much better if
the meat were cooked well by adding any seasoning to the meat. Except for color, all
other organoleptic characteristic’s samples were signi$cantly di#erent (p > .05).
4 CONCLUSION
In conclusion, the treatments given in this work were proved to exhibit the e#ective
utilization of extracted bromelain and A. heterophyllus protease from pineapple and
jackfruit waste by-product, respectively, in improving the tenderization tough muscle
in beef without unfavorably disturbing other quality parameters. The results reveled
that physicochemical treated beef samples showed a decrease in the water holding
capacity (WHC), pH, moisture content and cooking yield with the increased addition
of crude enzyme extract. Results suggested that the extracted proteolytic enzymes
from a local variety of A. comosus and A. heterophyllus can be used as a source of
meat tenderizer and become a better alternative to chemical tenderizers. All the
attributes of sensory evaluation scores for the treated sample were higher than the
control sample. In addition, coupled with pineapple and jackfruit processing items,
the core and the seed as a waste by-product could signi$cantly contribute to the
overall return from the investment in the meat and agricultural processing industry.
ACKNOWLEDGEMENTS
The authors gratefully acknowledged Universiti Malaysia Pahang for the $nancial
assistance through the Internal Research Grant No. UIC190301 and RDU182207-1.
CONFLICT OF INTEREST
The author declares that there is no con"ict of interest that could be perceived as
prejudicing the impartiality of the research reported.
AUTHOR CONTRIBUTIONS
Aizi Nor Mazila Ramli: Conceptualization; Funding acquisition; Methodology; Project
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administration; Software; Supervision; Visualization; Writing-original draft; Writingreview & editing. Hazrulrizawati Abd Hamid: Writing-review & editing. Farah
Hanani Zulki"i: Writing-review & editing. Normaiza Zamri: Writing-review & editing.
Prakash Bhuyar: Conceptualization; Formal analysis; Software; Writing-original
draft; Writing-review & editing. Nor Hasmaliana Abdul Manas: Writing-review &
editing.
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