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Microwave and ultrasound-assisted extraction of bioactive compounds from

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DOI: 10.1016/j.ultsonch.2023.106677

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 Ultrasonics Sonochemistry 101 (2023) 106677

Contents lists available at ScienceDirect

Ultrasonics Sonochemistry
journal homepage: www.elsevier.com/locate/ultson

Microwave and ultrasound-assisted extraction of bioactive compounds from

Papaya: A sustainable green process
Rahul Biswas 1, Animesh Sarkar *, Mahabub Alam 2, Mukta Roy , M.M. Mahdi Hasan
Department of Food Engineering and Tea Technology, Shahjalal University of Science and Technology, Sylhet 3114, Bangladesh

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

Keywords: The demand for sustainable and eco-friendly extraction methods for bioactive compounds from natural sources
Green process has increased significantly in recent years. In this study, we investigated the effectiveness of the microwave
Bioactive compounds pretreated ultrasound-assisted extraction (MPUAE) process for the extraction of antioxidants (TPC, DPPH, and
Extraction
FRAP) from papaya pulp and peel. The optimized variables for the MPUAE process were determined using the
Microwave
Ultrasound
Box-Behnken design tool of response surface methodology. Our results showed that the optimized variables for
pulp and peel were 675.76 and 669.70 W microwave power, 150 s of irradiation time, 30 ◦ C ultrasound tem­
perature, and 19.70 and 16.46 min of ultrasonic extraction time, respectively. Moreover, the MPUAE process was
found to be more energy-efficient and environmentally friendly compared to the conventional ultrasound-
associated extraction (UAE) technique. The MPUAE process emitted less CO2 to the environment and had a
shorter extraction time, resulting in a more sustainable and cost-effective extraction process. Our study suggests
that the MPUAE process has the potential to be a promising and eco-friendly alternative for the industrial
extraction of bioactive compounds from papaya and other natural sources.

1. Introduction
Natural products have been widely recognized as an important
source of bioactive compounds with a variety of biological activities,
including antioxidant, anti-inflammatory, and antimicrobial properties
[1]. The use of these compounds has been increasing in various fields,
such as the food and pharmaceutical industries [2]. The extraction of
bioactive compounds from natural sources is a crucial step in their
production and application. However, the traditional methods used for
extraction, such as maceration, Soxhlet extraction, and steam distilla­
tion, have several limitations, including long extraction times, low yield,
and the use of toxic organic solvents, which pose environmental and
health risks [3]. Recently, there has been a growing interest in devel­
oping sustainable and eco-friendly methods for the extraction of
bioactive compounds from natural sources. One such method is the use
of ultrasound-assisted extraction (UAE), which has been demonstrated
to be an effective and eco-friendly technique for the extraction of
bioactive compounds. Ultrasound enhances mass transfer, improving
the movement of solvents in and out of plant materials. UAE utilizes
high-frequency sound waves to disrupt the cell wall structure and
enhance the penetration of the solvent into the plant tissue, resulting in
higher yields of bioactive compounds in a shorter period of time [4].
However, the energy consumption of UAE can be high, which is a sig­
nificant challenge for industrial-scale applications.
To overcome this challenge, the combination of microwave pre­
treatment and ultrasound-assisted extraction (MPUAE) has been pro­
posed as a promising alternative method for the extraction of bioactive
compounds. The microwave pretreatment enhances the permeability of
the plant cell wall and facilitates the release of bioactive compounds
during subsequent ultrasound-assisted extraction [5]. The combination
of microwave and ultrasound energy also allows for a shorter extraction
time, which is beneficial for reducing the energy consumption and
improving the cost-effectiveness of the extraction process [6].
Carica Papaya fruits are widely cultivated in the tropical and sub­
tropical areas of the world and are well known for their high nutritional
value and high concentrations of antioxidants and phytochemical
compounds such as polyphenols, carotenoids, and ascorbic acid [7,8]).
Carotenoids, vitamins, minerals, saponins, flavonoids, alkaloids ascorbic

* Corresponding author.
E-mail addresses: rahul35@student.sust.edu (R. Biswas), animesh-fet@sust.edu (A. Sarkar), mahabub-fet@sust.edu (M. Alam), muktaroy-fet@sust.edu (M. Roy),
mahdi29@student.sust.edu (M.M. Mahdi Hasan).
1
ORCID: 0000-0002-2023-1936
2
ORCID: 0000-0003-1890-879X

https://doi.org/10.1016/j.ultsonch.2023.106677
Received 7 May 2023; Received in revised form 31 October 2023; Accepted 1 November 2023
Available online 3 November 2023
1350-4177/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
R. Biswas et al.
Fig. 1. Schematic outline of research design.
acids, and phenols are abundant in papaya, indicating a high antioxidant
activity that is beneficial to human health [9]. A huge quantity of wastes
and byproducts are produced; papaya peel waste accounted for around
12 % of the fruit weight, and postharvest losses of 40–60 % are observed
[10]. Papaya peel is used for a variety of uses in the food and medicine
industries, including cosmetics, due to its high content of phytochemi­
cals, bioactive compounds, vitamins, minerals, and antioxidant activity
[11]. Therefore, the extraction of bioactive compounds from papaya
pulp and peel using sustainable and eco-friendly methods is of consid­
erable interest.
While previous studies have reported the extraction of phenolic
compounds from various sources, including papaya leaves, the specific
conditions of microwave power, irradiation time, ultrasound extraction
time, and temperature have not been optimized. These variables play a
crucial role in bioactive extraction [12]. The diverse composition and
bioactive compounds in natural sources make developing a universally
optimal extraction process challenging [13]. Furthermore, the type and
quantity of polyphenols may vary based on plant species and extraction
conditions. Consequently, the ideal extraction process is expected to
differ depending on the fruit and its edible and non-edible components.
To address these knowledge gaps, our study introduces a systematic
framework for optimizing bioactive compound extraction, focusing on
microwave-dried papaya pulp and peel using the MPUAE technique.
This method leverages the benefits of both microwave and ultrasound,
enhancing the permeability of plant cell walls and promoting more
sustainable extraction. This innovative extraction method offers a new
dimension to bioactive compound extraction in papaya. However,
despite the advantages of the MPUAE approach, there are considerable
concerns about whether microwave irradiation and ultrasound indi­
vidually would degrade the quality of the extracted bioactive. As a
result, a novel method known as MPUAE was developed in this study,
which uses a combination of microwave energy as pretreatment and
ultrasonic waves for extraction. To extend the scope of our investigation,
we also assessed the environmental consequences of the optimized
MPUAE process, encompassing electrical consumption and CO2 emis­
sions. This eco-conscious approach adds a layer of novelty to our study,
contributing to a broader understanding of the environmental implica­
tions of innovative extraction methods. The objectives of this study were
2
Ultrasonics Sonochemistry 101 (2023) 106677
to optimize the extraction of bioactive compounds from papaya pulp and
peel using a combination of microwave power, irradiation time, ultra­
sonic temperature, and time through response surface methodology and
to compare the process yield and environmental consequences of the
optimized process (MPUAE) with the ultrasound-associated extraction
(UAE) technique. Understanding the fundamentals of this method is
crucial for its practical application in extracting bioactives from a range
of plant sources, fruits, and vegetables.
2. Materials and methods
2.1. Sample collection and preparation for extracts
Fresh mature green unripe Carica papaya L. was collected from Sylhet
local market with uniform size for quantitative measurement experi­
ment. After accumulating, samples were rinsed with clean water to
remove dirt. The seeds were removed and separated into the pulp and
peel of papaya fruits. The pulp was cut into small pieces of slices. After
that, the pulp and peel of the papaya were dried in a microwave oven
(Model- MC28H5025VK/D2) at 300 W until gaining equilibrium mois­
ture conditions. Based on a prior study, the exploratory experiment was
recommended [14]. Then the dried parts were powdered by a
laboratory-type hammer mill and passed through a sieve of 1 mm in size.
All the samples were immediately preserved inside air-tight polythene
bags. The microwave-dried pulp and peel powder from unripe papaya
were extracted using 60 % concentrated ethanol, according to pre­
liminary research and initial analysis [15]. The study design is depicted
in Fig. 1 as a schematic outline.
2.2. Microwave pretreated ultrasound-assisted extraction (MPUAE)
process
For each extraction, 200 mg of sample (dry powder) was mixed with
25 mL of ethanol solution (60 %, v/v). For the extraction, a Box-Behnken
design was utilized, with A representing the microwave power (W), B
representing the microwave irradiation time (s), C representing the ul­
trasound temperature (oC), and D representing the ultrasound extraction
time (min) as independent variables. At first, the samples were vortexed
R. Biswas et al.
to ensure that the samples and solvents are correctly mixed before
extraction. After that, the samples were pretreated by a microwave oven
(Model- MC28H5025VK/D2) with different microwave power and
irradiation time. The container was covered with parafilm and cooling
the sample’s container to prevent solvent evaporation during the mi­
crowave process. Then, the ultrasound was performed by ultrasonic
water bath (Model- VGT – 1860QT) with different ultrasound temper­
atures and extraction times. To avoid evaporation losses during
extraction, the samples were maintained as airtight as feasible. After­
ward, the samples were centrifuged (Gyrozen-Benchtop centrifuge,
Model- 416G) at 1130 g for 5 min. The specimens were filtered with
Whatman filter paper at the end of each removal. After that, the filtrates’
total phenolic content (TPC), DPPH radical scavenging activity, and
ferric-reducing antioxidant power (FRAP) were determined.
2.3. Evaluation of total phenolic content (TPC)
The modified method of Almusallam et al. [16] was used to calculate
the total phenolic content. Briefly, 0.5 mL of the ethanolic extract was
placed in a 10-mL flask. The extracts were then treated with 0.5 mL 1 M
Folin-Ciocalteu reagent. Then, the volume was increased to 10 mL using
double-distilled water after adding 1.0 mL of Na2CO3 (7.5 % w/v) re­
agent. Subsequently, the mixture was kept at 25 ◦ C for 1 h, the absor­
bance of the supernatant was measured against a reagent blank using a
UV Spectrophotometer (PG Instruments Ltd, Model- T60U) at a wave­
length of 725 nm. The calibration curve (y = 4.802x; R2 = 0.998) for
gallic acid was determined by comparing absorbance to corresponding
standard gallic acid solutions, with the water blank adjusted to zero (0).
The results were presented in mg gallic acid equivalent per 100 g dry
matter (mg GAE/100 g DM).
2.4. DPPH radical scavenging activity
For the DPPH radical scavenging assay, Zzaman et al. [17] method
was used. Firstly, 1.0 mL ethanolic extracts were vortexed with 4 mL,
0.06 mM DPPH solution in a tube. The tubes were then left in the dark
for 30 min at room temperature without being handled. The absorbance
of the mixtures was then measured using a UV Spectrophotometer (PG
Instruments Ltd, Model- T60U) at a wavelength of 517 nm. A DPPH
solution was used as a control but without the aliquot. Finally, the
following Eq. (1) was used to calculate the scavenging activity.
DPPH radical scavenging (%) =
Absorbancecontrol − Absorbancesample
× 100
Absorbancecontrol
(1)
2.5. Determination of ferric-reducing power (FRAP)
The modified method of Hossain and Hossain [12] was used to
calculate the FRAP. Briefly, 0.3 mL of extracted samples were vortexed
with 0.85 mL of phosphate buffer (pH 6.6; 0.2 M) and 0.85 mL of po­
tassium ferricyanide (1 % w/v). After 20 min of incubation at 50 ◦ C,
0.85 mL of trichloroacetic acid (10 % w/v) was added and vortexed
thoroughly. Finally, 2.85 mL distilled water and 0.57 mL FeCl3 (1 % w/
v) were added, and the mixture was maintained at 25 ◦ C for 30 min. A
UV Spectrophotometer (PG Instruments Ltd, Model- T60U) was used to
detect absorbance at a wavelength of 700 nm after the second incuba­
tion. In the meantime, a blank was made using distilled water instead of
the extract. The standard ascorbic acid was made by diluting the stock
solution in water serially. Fitting the absorbance versus its matching
standard ascorbic solutions, with the water blank set to zero (0), got the
standard curve (y = 2.915x; R2 = 0.998). The results were expressed as
mg of ascorbic acid equivalent antioxidant capacity per 100 g dry matter
(mg AAE/100 g DM).
3
Ultrasonics Sonochemistry 101 (2023) 106677
2.6. Statistical analysis and experimental design for optimization
The experiments were designed, and the statistical data was analyzed
(ANOVA) using Minitab (version 20.4.0.0). The relevance of Tukey’s
test of significance between means was demonstrated. The BBD was used
by RSM to optimize the experimental extraction procedure. Initially, the
four most important factors were chosen: microwave power, microwave
irradiation time, ultrasound temperature, and extraction time. The main
influential independent variables were determined as 300–900 W mi­
crowave power (A), 30–150 s microwave irradiation time (B), 30–60 ◦ C
ultrasound temperature (C), and 10–30 min ultrasound extraction time
(D) after trial studies. Every variable was encoded with three possible
values based on trial experiments and previous studies: high (+1), me­
dium (0), and low (-1). The most important three dependent variables
(multiple responses) TPC, DPPH, and FRAP extraction yield were chosen
in the experimental design.
Multiple regressions using the least-square approach were employed
to analyze the data, and the BBD was used to fit the experimental model
with the typical second-order quadratic equation Eq. (2):
∑
n ∑
n ∑
n
yr = α0 + αi xi + αii x2i + αij xi xj (2)
i=1 i=1 i∕
=j=1
where, yr denotes the measured response variables and xi and xj denote
the independent variable levels. α0 are a constant (predicted response at
the center) and the linear, quadratic, and two-factor interactive co­
efficients of the model are αi , aii , and αij , respectively. The total error
criteria were used in all statistical significance tests, with a confidence
level of 95 %.
2.7. Ultrasound-assisted extraction (UAE) process
Bioactive compound extraction was also performed using the UAE
process, based on the MPUAE procedure’s optimal conditions, in a
comparison investigation. After optimization of the MPUAE process
condition, the samples were extracted from both UAE and MPUAE.
Triplicate extractions were carried out.
2.8. Effect of process on the environment
Electrical consumption and CO2 emission of the applicable proced­
ures were also assessed in the current study regarding the environmental
effect. As a result, electrical consumption (EC) was computed as the
electrical power for a certain period, as follows in Eq. (3) [18]:
P×t
EC = (3)
1000
When 1 kWh of coal or fuel is burned, 0.8 kg of CO2 is emitted into the
environment [18]. As a result, CO2 emissions may be computed using
the following Eq. (4):
ECO2 = EC × 0.8 (4)
where, EC = electrical consumption (kWh); P = electrical power (W); t
= process time (h); andECO2 = CO2 emission (kg).
3. Results and discussion
3.1. Fitting of regression model and statistical analysis
The RSM linear models were applied to associate with the BBD of
bioactive compound extraction to determine the best process yield
conditions for microwave-dried papaya pulp and peel against various
trials. Bioactive componds (assessed by TPC, DPPH radical scavenging
activity, and FRAP attributes) were extracted based on several inde­
pendent factors found in early studies, including microwave power (W),
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Table 1
BBD matrix and multiple responses for process yield of microwave-dried pulp and peel of papaya against different runs using the MPUAE method.
Run Independent variables Pulp Peel
Coded level Uncoded level

A B C D A B C D TPC (GAE mg/ DPPH FRAP (AAE mg/ TPC (GAE mg/ DPPH FRAP (AAE mg/
100 g DM) (%) 100 g DM) 100 g DM) (%) 100 g DM)

1 − 1 − 1 0 0 300 30 45 20 411.26 74.09 1946.83 491.95 74.73 2602.92

2 1 − 1 0 0 900 30 45 20 515.38 75.16 1822.47 653.33 75.80 2607.20
3 − 1 1 0 0 300 150 45 20 512.78 78.80 1565.18 551.82 79.87 2367.07
4 1 1 0 0 900 150 45 20 541.41 80.51 2118.35 640.32 82.23 2688.68
5 0 0 − 1 − 1 600 90 30 10 596.07 74.73 1955.40 689.77 76.02 2705.83
6 0 0 1 − 1 600 90 60 10 603.88 74.30 1869.64 596.07 75.16 2568.61
7 0 0 − 1 1 600 90 30 30 575.25 77.52 1766.72 588.26 78.59 2534.31
8 0 0 1 1 600 90 60 30 533.60 78.80 1406.52 570.04 80.09 2199.83
9 − 1 0 0 − 1 300 90 45 10 476.33 68.97 1938.25 510.17 68.70 2534.31
10 1 0 0 − 1 900 90 45 10 510.17 66.84 1732.42 671.55 70.03 2590.05
11 − 1 0 0 1 300 90 45 30 484.14 78.16 1209.26 512.78 78.80 2092.62
12 1 0 0 1 900 90 45 30 489.35 76.87 1728.13 502.36 77.94 2388.51
13 0 − 1 − 1 0 600 30 30 20 517.98 78.37 2195.54 640.32 79.87 2945.97
14 0 1 − 1 0 600 150 30 20 663.74 82.01 2204.12 845.95 84.15 3023.16
15 0 − 1 1 0 600 30 60 20 554.42 75.80 1998.28 655.94 77.73 2688.68
16 0 1 1 0 600 150 60 20 637.72 81.80 2036.88 741.83 82.66 2993.14
17 − 1 0 − 1 0 300 90 30 20 507.57 80.30 1565.18 512.78 80.94 2319.90
18 1 0 − 1 0 900 90 30 20 554.42 77.09 1963.98 596.07 78.37 2585.76
19 − 1 0 1 0 300 90 60 20 502.36 76.87 1475.13 549.22 77.52 2174.10
20 1 0 1 0 900 90 60 20 528.39 79.23 1895.37 541.41 80.73 2251.29
21 0 − 1 0 − 1 600 30 45 10 525.79 66.58 1796.74 674.16 69.23 2855.92
22 0 1 0 − 1 600 150 45 10 570.04 76.39 2118.35 778.27 76.13 2920.24
23 0 − 1 0 1 600 30 45 30 536.20 77.52 1766.72 603.88 81.80 2731.56
24 0 1 0 1 600 150 45 30 567.44 78.80 1505.15 718.41 79.87 2508.58
25 0 0 0 0 600 90 45 20 640.32 78.37 1552.32 744.43 79.66 2555.75
26 0 0 0 0 600 90 45 20 627.30 77.09 1436.54 705.39 77.73 2598.63
27 0 0 0 0 600 90 45 20 622.10 76.66 1539.45 736.63 79.66 2654.37

microwave irradiation duration (s), ultrasound temperature (oC), and
ultrasound extraction time (min). According to the applicable variables
for the yield of bioactives employing the MPUAE process, the numerous
extraction conditions are depicted in Table 1 as obtained results. In
terms of TPC, DPPH radical scavenging activity, and FRAP, peel out­
performed pulp whereas peel ranged from 491.95 to 845.95 GAE mg/
100 g DM, 70.03 to 84.15 %, and 2092.62 to 3023.16 AAE mg/100 g DM
comapared to pulp ranged from 411.26 to 663.74 GAE mg/100 g DM,
66.58 to 82.01 %, and 1209.26 to 2204.12 AAE mg/100 g DM,
respectively. ANOVA was employed to evaluate every variable’s impact
and the viability of the quadratic model.
interaction of all factors.
The R-sq(adj) values in Table 2, which were observed to be 85.11 %
for pulp and 81.69 % for peel, imply that the models’ parameters are
quite capable of describing variance in the dependent variable, the TPC
extraction response. The following Eq. 5a-5b is an explanation of the
regression model utilized to calculate the expected value of TPC for pulp
and peel respectively. The model offered substantial practical impor­
tance since the coefficients of determination (R-sq) for pulp and peel
exhibited considerable variations between actual and predicted values
of 8.02 % and 9.86 %, respectively.

( / )
TPC_Pulp GAE mg 100 g DM = − 412 + 1.581A + 3.810B + 6.07C + 22.66D − 0.001099A2 − 0.00940B2 − 0.0275C2 −
2 (5a)
0.4457D − 0.001048A*B − 0.00116A*C − 0.00239A*D − 0.0174B*C − 0.0054B*D − 0.0824C*D

TPC_Peel (GAE mg/100 g DM) = − 794 + 2.616A + 1.94B + 18.96C + 21.3D − 0.001565A2 + 0.00470B2 − 0.1851C2
(5b)
− 0.556D2 − 0.00101A*B − 0.00506A*C − 0.01432A*D − 0.0333B*C + 0.0043B*D + 0.126C*D

The results from Table 2 revealed fitting model coefficients and
statistical analysis, accompanied by the lack of fit and pure error for
each response, indicating that the full quadratic model along with linear
terms of independent variables strongly (P < 0.05) influenced the TPC
extraction for both pulp and peel, while the linear impact of ultrasound
temperature (C) was insignificant (P > 0.05) for both and ultrasound
time (D) for pulp. Moreover, the quadratic terms for all parameters
except ultrasound temperature (C2) for pulp and irradiation time (B2) for
peel had a significant (P < 0.05) effect on polyphenol extraction.
However, each response was not considerably (P > 0.05) affected by the
The variance analysis for second-order quadratic regression models was
carried out on the DPPH antioxidant activity for pulp and peel response,
where Table 2 expressed the model’s adaptability, coefficients, and
impacts of the predictor variables. According to the analysis, both pulp
and peel were significantly (P < 0.05) impacted by the full quadratic
model as well as linear terms of independent variables. However, the
linear influence of microwave power (A) and ultrasonic temperature (C)
was not significant (P > 0.05). Furthermore, the quadratic terms of ul­
trasound time (D2) were also significantly (P < 0.05) impacted, but
other factors were not. Besides, the interaction of irradiation time to

4
 R. Biswas et al.
Table 2
ANOVA for response and regression model coefficient for bioactive extraction process yield.
Model parameter DF VIF TPC (GAE mg/100 g DM) DPPH radical scavenging activity (%) FRAP (AAE mg/100 g DM)

Pulp Peel Pulp Peel Pulp Peel

Coefficient F-Value P-Value Coefficient F-Value P-Value Coefficient F-Value P-Value Coefficient F-Value P-Value Coefficient F-Value P-Value Coefficient F-Value P-Value

Constant 629.9 0.000 728.8 0.000 77.373 0.000 79.015 0.000 1509.4 0.000 2602.9 0.000
Model 14 11.62 0.000 9.29 0.000 11.07 0.000 10.56 0.000 12.31 0.000 9.09 0.000
Linear 4 10.48 0.001 9.68 0.001 22.76 0.000 21.04 0.000 16.02 0.000 10.19 0.001
A 1 1.00 20.39 9.70 0.009 39.7 11.49 0.005 − 0.123 0.08 0.785 0.378 0.71 0.417 130.1 20.84 0.001 85.0 7.67 0.017
B 1 1.00 36.01 30.24 0.000 46.4 15.71 0.002 2.567 33.88 0.000 2.145 22.77 0.000 1.8 0.00 0.951 5.7 0.03 0.855
C 1 1.00 − 4.56 0.48 0.500 − 18.2 2.42 0.146 − 0.268 0.37 0.555 − 0.339 0.57 0.465 − 80.8 8.04 0.015 − 103.3 11.30 0.006
D 1 1.00 − 8.03 1.50 0.244 − 35.4 9.11 0.011 3.321 56.72 0.000 3.485 60.12 0.000 − 169.0 35.20 0.000 − 143.3 21.76 0.001
Square 4 28.54 0.000 20.42 0.000 12.94 0.000 12.73 0.000 18.06 0.000 19.60 0.000
A2 1 1.25 − 98.91 101.42 0.000 − 140.9 64.32 0.000 − 1.055 2.54 0.137 − 1.589 5.55 0.036 49.5 1.34 0.269 − 229.4 24.79 0.000
B2 1 1.25 11.87 0.005 16.9 0.93 0.354 0.563 0.72 0.411 0.712 1.11 0.312 313.8 53.90 0.000 236.9 26.44 0.000
5

–33.84
C2 1 1.25 − 6.18 0.40 0.541 − 41.6 5.62 0.035 1.937 8.58 0.013 1.680 6.21 0.028 221.0 26.75 0.000 − 5.9 0.02 0.900
D2 1 1.25 − 44.57 20.60 0.001 − 55.6 10.03 0.008 − 3.232 23.87 0.000 − 3.253 23.28 0.000 28.6 0.45 0.516 − 50.9 1.22 0.291
2-Way Interaction 6 1.09 0.421 1.60 0.229 2.02 0.141 2.12 0.126 5.99 0.004 1.35 0.309
A*B 1 1.00 − 18.9 2.77 0.122 − 18.2 0.81 0.387 0.161 0.04 0.837 0.321 0.17 0.687 169.4 11.78 0.005 79.3 2.22 0.162
A*C 1 1.00 − 5.2 0.21 0.654 –22.8 1.26 0.283 1.392 3.32 0.093 1.445 3.45 0.088 5.4 0.01 0.915 − 47.2 0.79 0.393
A*D 1 1.00 − 7.2 0.40 0.540 − 42.9 4.48 0.056 0.209 0.08 0.789 − 0.546 0.49 0.497 181.2 13.48 0.003 60.0 1.27 0.281
B*C 1 1.00 − 15.6 1.90 0.194 − 29.9 2.18 0.166 0.589 0.59 0.456 0.161 0.04 0.840 7.5 0.02 0.882 56.8 1.14 0.307
B*D 1 1.00 − 3.3 0.08 0.779 2.6 0.02 0.900 − 2.132 7.80 0.016 − 2.206 8.03 0.015 − 145.8 8.73 0.012 − 71.8 1.82 0.202
C*D 1 1.00 − 12.4 1.19 0.297 18.9 0.87 0.371 0.428 0.31 0.585 0.589 0.57 0.464 − 68.6 1.93 0.190 − 49.3 0.86 0.372
Error 12
Lack-of-Fit 10 6.81 0.135 4.43 0.198 3.32 0.253 2.15 0.359 2.70 0.300 5.36 0.167
Pure Error 2
Total 26
R-sq 93.13 % 91.55 % 92.81 % 92.49 % 93.49 % 91.38 %
R-sq(adj) 85.11 % 81.69 % 84.42 % 83.74 % 85.89 % 81.33 %

Ultrasonics Sonochemistry 101 (2023) 106677

R. Biswas et al.
ultrasound time (B*D) had a significant (P < 0.05) effect on the
extraction of DPPH antioxidant activity for pulp and peel.
The adequacy of the models is demonstrated by the coefficient of
determination (R-sq) values of DPPH radical scavenging activity in
Table 2, which were 92.81 % and 92.49 % for pulp and peel, respec­
tively. Pulp and peel had adjusted R-sq(adj) values of respectively 84.42
% and 83.74 % along with the difference between R-sq and R-sq(adj)
was 8.39 % and 8.75 %. The DPPH radical scavenging activity of pulp
and peel is predicted employing regression equations, which are pre­
sented in Eq. 6a-6b.
DPPH_Pulp ​ (%) = 78.0 − 0.0025A + 0.0509B − 1.094C + 1.774D
− 0.000012A2 + 0.000156B2 + 0.00861C2 − 0.03232D2
+ 0.000009A*B + 0.000309A*C + 0.000070A*D
+ 0.000654B*C − 0.00355B*D + 0.00286C*D
(6a)
DPPH_Peel ​ (%) = 71.5 + 0.0100A + 0.0549B − 0.982C + 1.913D
− 0.000018A2 + 0.000198B2 + 0.00747C2 − 0.03253D2
+ 0.000018 A*B + 0.000321A*C − 0.000182A*D
+ 0.000178B*C − 0.00368B*D + 0.00393C*D
(6b)
Table 2 demonstrated fitting model coefficients and analysis of variance,
along with model reliability, implying that the full quadratic mod­
el associated with linear terms of independent factors, substantially (P
< 0.05) affected FRAP extraction for both pulp and peel, although
irradiation time (B) had no significant (P > 0.05) linear effect. Corre­
spondingly, the quadratic terms for microwave power (A2) and irradi­
ation time (B2) for peel as well as irradiation time (B2) and ultrasound
temperature (C2) for pulp exhibited a significant (P < 0.05) impact on
FRAP extraction. Moreover, the interaction of microwave power to
irradiation time (A*B), microwave power to ultrasound time (A*D), and
irradiation time to ultrasound time (B*D) had a considerable (P < 0.05)
effect on the extraction of FRAP for pulp.
Since the coefficients of determination (R-sq) for the pulp and peel
indicated 93.49 % and 91.38 %, respectively in Table 2, the model
provided considerable important implications for FRAP extraction. The
adjusted R-sq(adj) values for the pulp and peel were 85.89 % and 81.33
%, respectively, while the variance between actual and predicted values
was 7.60 % and 10.05 %, demonstrating the validity of the model. The
description Eq. 7a-7b of the regression equations used to evaluate the
anticipated value of the FRAP for pulp and peel.
FRAP_Pulp ​ (AAE ​ mg/100g ​ DM) ​ = ​ 5284-2.335A- 16.82B − 86.1C
− 22.1D + 0.000550A 2 of the waves. Consequently, as the ultrasonic amplitude increases, there
+ 0.0872B2 + 0.982C2 + 0.286D2
+ 0.00941A*B + 0.0012A*C
+ 0.0604A*D + 0.0083B*C
− 0.2430B*D − 0.457C*D
(7a)
FRAP_Peel ​ (AAE ​ mg/100g ​ DM) ​ = ​ 2319 + 3.017A- 14.84 B + 2.7C
+ 19.6 D − 0.002549 A2
+ 0.0658 B − 0.026 C2 − 0.509 D2
2 the movement of ions and the rotation of dipoles, and thus energy
+ 0.00441A*B − 0.0105 A*C
+ 0.0200A*D + 0.0631B*C
− 0.1197B*D − 0.329C*D
(7b)
The lack of fit denoted that it was insignificant (P > 0.05) in comparison
6
Ultrasonics Sonochemistry 101 (2023) 106677
to pure errors, which was desirable, and that the models were adequate
for anticipating the TPC, DPPH radical scavenging activity, and FRAP
responses. In addition, Variance Inflation Factor (VIF) range for all
predictor variables was found to be from 1.00 to 1.25 for multiple re­
sponses, indicating a lack of multicollinearity among independent var­
iables. Therefore, all the models demonstrated that they were suitable
and effective for predicting the responses.
3.2. Impact of variables on the bioactive extraction process
The analysis revealed that the TPC extraction yield was positively
correlated with the main effects of microwave power and irradiation
time for pulp and peel, but those interactions among factors had a
negative impact, whereas interactions of irradiation time to ultrasound
extraction time and ultrasound temperature to extraction time along
with quadratic terms of irradiation time had a positive influence for the
peel indicated in Table 2.
According to antioxidant activity, DPPH radical scavenging proper­
ties extraction was positively correlated to the main impacts of irradi­
ation time and ultrasound extraction time for pulp, but other factors
were negatively associated. Similarly, microwave power, irradiation
time, and ultrasound extraction time positively interacted with peel
extraction, but other variables were adversely related shown in Table 2.
Moreover, the quadratic terms of ultrasound temperature and irradia­
tion time were positively linked for the pulp and peel. Furthermore, the
terms of the variable interactions were all positively interrelated, while
the relationship between the time of irradiation and the time of ultra­
sound extraction for the pulp and peel, as well as microwave power to
ultrasound extraction time, was negatively influenced for the peel.
Accordingly, the FRAP extraction attributes were linked positively
with the main effects of microwave power and irradiation time as well as
the quadratic and interaction terms of all variables, whereas the inter­
action between the ultrasound temperature and extraction time along
with the irradiation time and ultrasound extraction time impacted
negatively on the pulp as illustrated in Table 2. Besides, for the peel,
these qualities were positively proportional to the main effects of mi­
crowave power and irradiation time, although other parameters were
negatively influenced. Subsequently, a positive correlation of the
quadratic components of irradiation time as well as the interaction terms
of microwave power to irradiation time, microwave power to extraction
time, and irradiation time to ultrasound temperature were observed.
Ultrasound amplitude can be used to describe the beneficial effects of
ultrasonic power. Owing to the sound wave and liquid droplets formed
by cavitation, the plant’s cell wall seems to collapse when it is exposed to
ultrasound waves. The rarefaction and compression of these waves cause
the liquid to cavitate, and these processes are influenced by the intensity
are more cavities, leading to a greater extraction yield reachable [18]. In
addition, ultrasound waves considerably enhanced the yields of bioac­
tive substances throughout the recovery process and reduced extraction
time [19]. In contrast, high-intensity ultrasonics might break down the
bioactive molecule, which raises concerns about the importance of the
process’s duration [20]. Nevertheless, in comparison to the impact of
microwave power, this effect is less substantial, thus of their exposure,
the yield is essentially unaffected. The conversion of electromagnetic
energy into heat energy occurs without physical touch in microwave
operation. Nonionizing radiation generates molecular motion through
conversion is based on these two processes [21]. The treated material
absorbed energy more rapidly, which decreased heat gradients and se­
lective heating [22]. Moreover, the microwave heating of the water
molecule within the treated biomaterial results in significant stress on
the cell walls, and mechanically collapses the walls. As a result, solvent
absorption into the internal tissues is boosted, thus, it is possible to
attain maximum extraction yields and selection [23].
Based on the study, a proper irradiation period should be selected to
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 2. Response (a) surface and (b) contour plots of total phenolic content (GAE mg/100 g DM) vs four independent variables of papaya pulp.

7
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 3. Response (a) surface and (b) contour plots of total phenolic content (GAE mg/100 g DM) vs four independent variables of papaya peel.

8
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 4. Response (a) surface and (b) contour plots of DPPH antioxidant activity (%) vs four independent variables of papaya pulp.

9
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 5. Response (a) surface and (b) contour plots of DPPH antioxidant activity (%) vs four independent variables of papaya peel.

obtain adequate extraction since irradiation time is one of the major
variables that affect bioactive extraction yield. This variable has a
favorable influence on the process when associated with time. The
extraction yield was observed to be proportional to the irradiation time
and its quadratic impact, however, the ultrasound extraction time had a
negative influence except for DPPH activity. Nevertheless, the extraction
efficiency is lowered because consistent exposition to microwave radi­
ation causes structural deterioration of the extracted substances [24].
Therefore, a reduced period needs to maximize bioactive compound
extraction in terms of industrial application. Correspondingly, the
MPUAE method revealed the high bioactive extraction efficiency
combining microwave radiation and ultrasound wave leading to a lower

10
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 6. Response (a) surface and (b) contour plots of FRAP antioxidant activity (AAE mg/100 g DM) vs four independent variables of papaya pulp.

11
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 7. Response (a) surface and (b) contour plots of FRAP antioxidant activity (AAE mg/100 g DM) vs four independent variables of papaya peel.

12
R. Biswas et al. Ultrasonics Sonochemistry 101 (2023) 106677

Fig. 8. The optimal condition for bioactive extraction of papaya (a) pulp and (b) peel by MPUAE process.

processing time. The extraction of bioactive substances from various researchers have also noted that raising the extraction temperature en­
biomaterials has been accomplished effectively using ultrasound wave hances extraction, diffusion coefficient, and solute solubility [25,26].
and microwave radiation conjunction [25]. Hence, merging these sys­ Nonetheless, some samples of bioactive can break down above a certain
tems can result in some synergistic benefits, such as a reduction in the temperature [27]. A prior study found that some polyphenols bound to
amount of solvent needed and faster time for extraction, an enhance­ proteins may result in a bioactive depletion in the tissue at a greater
ment in energy efficiency, and a reduced cost [26]. Since both ultra­ temperature [28]. In addition, heat may boost the extraction of anti­
sound and microwave treatments independently degrade bioactive oxidants, and the improved temperature of the extraction releases the
molecules during their long recovery processes, pretreatment of micro­ plant material and breaks the bond between the polyphenols and the
wave irradiation is used in the UAE procedure to minimize the period. proteins or polysaccharides, raising the solubility and enhancing the
Therefore, the MPUAE technique performed 150 s microwave run and diffusion rate [12]. The observable FRAP activities are brought about by
19.70 min and 16.46 min ultrasonic runs for the pulp and peel, the denaturation of TPC [29]. This could be because polymeric phenols
respectively. could bind iron ions at reduced temperatures, enhancing the FRAP and
TPC, DPPH antioxidant properties, and FRAP attribute extraction DPPH intensity [30].
were depicted by plotting three-dimensional response surface plots
(Fig. 2a, Fig. 4a, and Fig. 6a of pulp and Fig. 3a, Fig. 5a, and Fig. 7a of
3.3. Optimization of MPUAE process variables
peel) and the contour plots (Fig. 2b, Fig. 4b, and Fig. 6b of pulp and
Fig. 3b, Fig. 5b, and Fig. 7b of peel) respectively. These plots illustrated
According to the information previously stated, an optimization
the impact of the process variables, whereas response surfaces exhibit
study was conducted to identify the optimum processing conditions for
substantial curvature and contour plots display a color gradient.
recovering from the pulp and peel. Bioactive substances are often
Accordingly, all parameters were influenced significantly regarding
extracted utilizing several factors, yet the combined effects of these
multiple bioactive responses. Following the investigation, the temper­
parameters have not been extensively investigated by these basic ap­
ature has been identified as one of the most crucial variables influencing
proaches. Consequently, multiple response optimizations were
the discharge of polyphenols from the food material, and many other
employed to define the optimized field, which can then assist to select
the most pragmatic proportion among microwave power, irradiation
Table 3 time, ultrasound temperature, and ultrasound extraction time, along
Bioactive extraction of process yields by UAE and MPUAE methods. with promoting bioactive yields and extract possibilities. The intended
Bioactive UAE MPUAE function of process optimization is the simultaneous influence of the
Compounds predictor variables on the three responses. The target was to maximize
Pulp Peel Pulp Peel
TPC, DPPH radical, and FRAP attributes while also considering the
TPC (GAE mg/ 618.63 ± 793.02 ± 633.38 ± 803.43 ± viability of the analysis and predicting the process condition against a
100 g DM) 7.95b 5.42a 6.55b 9.14a
DPPH (%) 77.23 ± 80.37 ± 79.01 ± 82.23 ±
variety of responses for both pulp and peel extraction.
0.89c 0.75b 0.64bc 0.43a The findings of research on the optimization of papaya pulp (Fig. 8a)
FRAP (AAE mg/ 1985.42 ± 2844.48 ± 2129.79 ± 2913.09 ± and peel (Fig. 8b) depicted the following multiple bioactive responses
100 g DM) 23.88d 24.38b 20.27c 27.9a along with the best-fitting prediction processing condition. Therefore,
All Values in the table depict the mean ± standard deviation of three replications the optimum independent variables condition was 675.76 W microwave
- the significant difference (p < 0.05) among samples in the same row with power, 150 s irradiation time, 30 ◦ C ultrasound temperature, and 19.70
distinct superscript characters. min ultrasound extraction time for the maximum simultaneous bioactive

13
R. Biswas et al.
Fig. 9. Energy consumption and environmental effect of ultrasound-assisted extraction (UAE); and microwave pretreated ultrasound-assisted extraction
(MPUAE) process.
extraction of papaya pulp. As well as optimal predictor variable com­
binations were 669.70 W microwave power, 150 s irradiation time,
30 ◦ C ultrasound temperature, and 16.46 min ultrasound extraction time
for the maximum simultaneous bioactive extraction of papaya peel. The
composite desirability of pulp and peel was 0.96 and 0.93, respectively,
indicating the model’s validity. The actual values of bioactive were
relatively near to the anticipated maximum response, which was per­
formed based on optimal conditions. In this condition of pulp, the actual
value of TPC, DPPH, and FRAP were 633.38 ± 6.55 GAE mg/100 g DM,
79.01 ± 0.64 %, and 2129.79 ± 20.27 AAE mg/100 g DM, respectively.
On the other hand, the actual value of TPC, DPPH, and FRAP of peel
were 803.43 ± 9.14 GAE mg/100 g DM, 82.23 ± 0.43 %, and 2913.09
± 27.90 AE mg/100 g DM, respectively. Previous researchers optimized
the antioxidant activity using DPPH and FRAP assays and TPC of Bac­
caurea ramiflora was employed as an analogous protocol [12].
3.4. Comparison between UAE and MPUAE process
The use of MPUAE had a favorable impact on the yield of bioactive
obtained. Extraction was also conducted using the UAE procedure to
assess the potential of the proposed MPUAE strategy. The UAE process
was carried out based on a preliminary experiment; the ultrasound
temperature and time were 45 ◦ C and 40 min for pulp and 35 min for
peel extraction. Correspondingly, the MPUAE technique was used based
on the optimal conditions, which performed better than the UAE
method. As depicted in Table 3, the TPC, DPPH, and FRAP values
recovered by the MPUAE process were 2.38 %, 2.30 %, and 7.27 % for
pulp and 1.31 %, 2.31 %, and 2.41 % for peel, respectively higher.
Because the synergistic impacts of microwave and ultrasound waves on
plant cell walls, which result in a noticeably larger extraction yield of
bioactive, can be used to explain why the MPUAE is more effective [18].
This demonstrates that MPUAE might be a suitable extraction method
for extracting bioactive substances from papaya since it offers the
highest extraction efficiency in the least amount of time. Consequently,
the MPUAE process exhibited a shorter process time than the UAE
technique, which was 19.70 min and 16.46 min, respectively, for the
pulp and peel. Hence, the analysis indicates that MPUAE has enhanced
bioactive compound extraction compared to UAE. Thus, the MPUAE
procedure does not result in any destruction of the compounds and may
be adopted as a sustainable and green process for extraction.
14
Ultrasonics Sonochemistry 101 (2023) 106677
3.5. Effect on energy and environment
The calculation of the required electrical power and CO2 emissions to
the environment for conducting the UAE and MPUAE procedures, using
microwave and ultrasound power levels of 900 W and 450 W, respec­
tively depicted in Fig. 9. The MPUAE procedure revealed lower energy
consumption and CO2 emissions during the process, which were 36.67 %
and 37.50 % for pulp and 38.46 % and 38.10 % for peel, respectively,
when compared to the UAE technique. Consequently, the MPUAE
technique employs much less energy and emits significantly minimal
carbon dioxide gases into the environment as well. It is worth assessing
that process duration directly correlates with energy usage and CO2
emissions. The overall protocol took 40 min for pulp extraction and 35
min for peel extraction using the UAE method with ultrasound power
450 W, whereas MPUAE used a 150 s irradiation pretreatment period
with 900 W level and 19.70 min for pulp16.46 min for peel ultrasound
extraction time. Therefore, the total bioactive substances were observed
to be considerably higher in extraction in MPUAE. The previous study
observed that the single-effect extraction strategy requires more energy
and generates greater greenhouse gas emissions, however, the combined
microwave-ultrasound system extraction method required the reverse
[18]. Thus, it can be said that the established MPUAE was a green
procedure for the bioactive extraction of papaya because a considerable
reduction in extraction time was noticed in this technique.
4. Conclusions
This study highlights the successful optimization of the microwave
pretreated ultrasound-assisted extraction (MPUAE) process for the
extraction of bioactive compounds from papaya pulp and peel using
response surface methodology (RSM) with the Box-Behnken design
(BBD) tool. The results of this study indicate that the MPUAE process is
an effective and environmentally sustainable approach for the extrac­
tion of bioactive compounds from papaya, with shorter extraction time
and observable energy efficiency compared to the traditional
ultrasound-associated extraction (UAE) technique. The acceptability
attributes of all anticipated models were adequate and effectively
employed for bioactive optimization. The findings of this study can
guide future research on the development of innovative and sustainable
techniques for the extraction of antioxidant compounds from plant
materials in industrial applications using a combination of microwave
radiation and ultrasonic waves based on several predictor variables ef­
fects that are optimizable.
R. Biswas et al.
While our study has made significant contributions to the optimi­
zation of bioactive compound extraction from papaya pulp and peel
using Microwave Pretreated Ultrasound-Assisted Extraction (MPUAE), it
is important to recognize certain limitations. As our investigation pri­
marily focused on optimizing the extraction process and evaluating its
environmental impact, we did not conduct a detailed assessment of
potential changes or modifications to bioactive compounds during the
extraction process. Further research is needed to comprehensively un­
derstand the extent to which microwave irradiation and ultrasound may
impact the quality of these compounds. These limitations open avenues
for future investigations, which can build upon our work and provide a
more comprehensive understanding of bioactive compound extraction
using MPUAE.
Funding details
The research work was funded by Shahjalal University of Science and
Technology Research Center (Project ID: AS/2022/1/35).
CRediT authorship contribution statement
Rahul Biswas: Conceptualization, Methodology, Validation, Inves­
tigation, Writing – review & editing, Software, Formal analysis, Writing
– original draft, Visualization, Data curation, Resources. Animesh Sar­
kar: Conceptualization, Methodology, Validation, Writing – review &
editing, Funding acquisition, Software, Writing – original draft, Visual­
ization, Supervision, Project administration, Resources. Mahabub
Alam: Conceptualization, Methodology, Validation, Investigation,
Writing – review & editing, Software, Formal analysis, Writing – original
draft, Visualization, Data curation. Mukta Roy: Methodology, Valida­
tion, Writing – review & editing, Software. M.M. Mahdi Hasan:
Investigation, Writing – review & editing, Formal analysis, Data
curation.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
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