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Ultrasonics Sonochemistry 34 (2017) 821–830

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

Green ultrasound-assisted extraction of carotenoids from pomegranate


wastes using vegetable oils
Athanasia M. Goula ⇑, Maria Ververi, Anna Adamopoulou, Kyriakos Kaderides
Department of Food Science and Technology, School of Agriculture, Forestry and Natural Environment, Aristotle University, 541 24 Thessaloniki, Greece

a r t i c l e i n f o a b s t r a c t

Article history: The objective of this work was to develop a new process for pomegranate peels application in food indus-
Received 4 April 2016 tries based on ultrasound-assisted extraction of carotenoids using different vegetable oils as solvents. In
Received in revised form 12 July 2016 this way, an oil enriched with antioxidants is produced. Sunflower oil and soy oil were used as alternative
Accepted 26 July 2016
solvents and the effects of various parameters on extraction yield were studied. Extraction temperature,
Available online 27 July 2016
solid/oil ratio, amplitude level, and extraction time were the factors investigated with respect to
extraction yield. Comparative studies between ultrasound-assisted and conventional solvent extraction
Keywords:
were carried out in terms of processing procedure and total carotenoids content. The efficient extraction
Carotenoids
Green extraction
period for achieving maximum yield of pomegranate peel carotenoids was about 30 min. The optimum
Green solvent operating conditions were found to be: extraction temperature, 51.5 °C; peels/solvent ratio, 0.10;
Pomegranate peel amplitude level, 58.8%; solvent, sunflower oil. A second-order kinetic model was successfully developed
Ultrasound extraction for describing the mechanism of ultrasound extraction under different processing parameters.
Ó 2016 Elsevier B.V. All rights reserved.

1. Introduction by-products could be a source of natural antioxidants [47,81]. Kim


et al. [37] introduced the peels of pomegranate as a rich source of
Carotenoids are natural pigments that are present mostly in all antioxidants, especially phenolic compounds and carotenoids. Sev-
plants, algae, some bacteria, and fungi. Generally, it is believed that eral studies have been published in the past to extract phenolics
carotenoids pigments are responsible for the color in fruits and from pomegranate peels with various extraction methods, such as
flowers, which plays an important role in attracting animals to normal stirring, microwave-assisted extraction, pressurized liquid
act as pollinators and seed dispersion vehicles [32]. More than extraction, and ultrasounds [19,80,86,51,52,75,78,34]. However, in
650 carotenoids have been described and isolated from natural literature, to the best of our knowledge, no studies have been
sources, however, only about 60 are regularly present in the presented on the extraction of carotenoids from pomegranate peels.
human diet, and about 20 carotenoids were reported to be in Traditionally, conventional methods have been used to recover
human plasma and tissues [23]. It was found that the consumption nutritionally valuable compounds from plant food matrices. How-
of carotenoids-rich foods, such as fruits and vegetables, decreases ever, nowadays, the need for obtaining greener, sustainable, and
the risk of developing certain types of cancer [26] and other degen- viable processes has led both food industries and food scientists
erative and chronic diseases [20]. to develop new processes in full correspondence with the green
Pomegranate (Punica granatum L.) has been well documented for extraction concept. Compared to the conventional methods, such
its potential health benefits such as its high antioxidant, as Soxhlet extraction, high-energy techniques are gaining a consid-
anti-mutagenic, anti-hypertension, anti-inflammatory, and anti- erable interest in the field of extraction of bioactive compounds,
atherosclerotic activity against osteoarthritis, prostate cancer, heart due to the fast extraction rate, the high extraction yield, the mini-
disease, and HIV-1 [12]. Since the juice yield of pomegranates is less mum detrimental effect on the extracted compounds, the enhance-
half of the fruit weight, very large amounts of by-product wastes, ment of the extraction of thermosensitive nutritional components,
such as peels, are formed every year. Pomegranate by-product the lower processing temperatures, and the use of ‘‘recognized as
wastes have been traditionally valorised as animal feed. Recently, safe” organic solvents.
a number of studies have proposed that some fruit or vegetable One promising alternative to traditional methods for carote-
noids extraction is the use of edible oils as solvents, which offer
attractive advantages, due to the oil solubility of carotenoids
⇑ Corresponding author. [65,31,42,41]. Anderson [6] developed a process for extraction of
E-mail address: athgou@agro.auth.gr (A.M. Goula).

http://dx.doi.org/10.1016/j.ultsonch.2016.07.022
1350-4177/Ó 2016 Elsevier B.V. All rights reserved.
822 A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830

carotenoids from shrimp processing wastes wherein soybean oil 2. Materials and methods
was added to the wastes, mixed, heated and the oil fraction recov-
ered by centrifugation. Chen and Meyers [17] applied enzymatic 2.1. Materials
hydrolysis of homogenized crawfish wastes with protease and sub-
sequent extraction with soy oil for recovery of carotenoids. Acid Pomegranate peels as a by-product of fruit juice industry were
ensilaging of crawfish wastes was found to stabilize the astaxan- provided from a local producer (Rodi Hellas, Greece). The peels
thin in the wastes and also increase the recovery of astaxanthin were dried at 40 °C for 48 h and kept at 30 °C until use. The peels
in soy oil [18]. Carotenoids in homogenized crawfish waste were were ground in a laboratory mill (Type A10, Janke and Kunkel, IKA
recovered by acidifying and heating with soybean oil to recover Labortechnik, Germany) immediately prior to extraction. The par-
pigment-enriched oil [49]. Omara-Alwala et al. [50] reported that ticle size distribution of the milled peels is presented in Fig. 1.
the use of propionic acid enhances the recovery of astaxanthin
from crawfish wastes by 35% during vegetable oil extraction. Cod
liver oil also has been used to extract pigments from processing 2.2. Process for pomegranate peels utilization
discards of snow crab and shrimp wastes [67]. A method based
on silica gel column chromatography has been developed for the Fig. 2 presents the proposed integrated process for pomegra-
concentration of carotenoids in Krill oil [30]. Sachindra and Mahen- nate peels application in food industries. This process is based on
drakar [65] studied the extractability of shrimp wastes carotenoids the ultrasound-assisted extraction of carotenoids using a vegetable
in different vegetable oils (sunflower oil, groundnut oil, gingelly oil, oil as an alternative solvent. In this way, an oil enriched with
mustard oil, soy oil, coconut oil, and rice bran oil) and optimized antioxidants is produced. Fig. 2 also presents the conventional
the conditions for oil extraction, such as oil to waste ratio, time, method for producing a carotenoids enriched oil, which is based
and heating temperature. Vasapollo et al. [77], Sun and Temelli on the classic extraction using an organic solvent. In both methods,
[72], and Krichnavaruk et al. [39] investigated the potential of several pretreatment procedures (washing, drying, grinding) are
using different vegetable oils as co-solvents with continuous addi- employed, whereas the conventional method consists of several
tion into SC-CO2 for the extraction of carotenoids from carrots, additional operation steps, such as solvent evaporation and recy-
tomatoes, and H. pluvialis. Handayani et al. [29] extracted astaxan- cling and molecular distillation or vacuum drying to eliminate
thin from giant tiger (Panaeus monodon) shrimp waste using palm residual traces of undesirable solvents according to the regulations
oil. Li et al. [42] developed a method for ultrasound-assisted in force. These additional steps would result in high input cost,
extraction of carotenoids from fresh carrots, in which sunflower energy consumption, and generation of hazardous solvent waste.
oil was applied as a substitute to organic solvents. Parjikolaei
et al. [53] introduced sunflower oil and methyl ester of sunflower 2.3. Ultrasound extraction using vegetable oils
oil as two green solvents for extracting astaxanthin from shrimp
processing waste. Ultrasonication can be applied in two ways: directly to the sam-
Extraction using edible oils can fulfill almost all the principles ple or indirectly through the walls of the sample container using a
as defined by Chemat et al. [16] to be considered as a green process water bath. In the direct method, the ultrasonic probe is immersed
e.g. applying environmentally friendly solvents, reducing the into the solution and provides an ultrasonic power that is at least
energy consumption, and producing the non-denatured extract up to 100 times greater than that supplied by the bath, with
without contaminants. Further, the oil plays a barrier role against sonication time usually 5 min or less. In this work, a 130 W of max-
oxygen and consequently retards the oxidation time and degrada- imum nominal output power, 20 kHz of frequency VCX-130 Sonics
tion rate of the carotenoids extract [59]. However, the high oil and Materials (Danbury, CT, USA) sonicator equipped with a Ti-Al-
viscosity is a major problem, which results in low diffusivity and V sonoprobe (13 mm) was used for ultrasound-assisted extraction
consequently low extraction yield even at high temperatures. In in pulsed mode. The pulse duration and pulse interval refer to ‘‘on’’
recent years, ultrasound-assisted extraction (UAE) of compounds time and ‘‘off’’ time of the sonicator. The amplitude control of the
with antioxidant activities has been widely applied to alleviate this processor allowed the ultrasonic vibrations at the probe to be set
problem [2,42]. at any desired level in the 10–100% range of the nominal power.
Extraction enhancement by ultrasound has been attributed to
the propagation of ultrasound pressure waves and resulting cavita-
tion forces, where bubbles can explosively collapse and generate
localized pressure causing plant tissue rupture and improving the
release of intracellular substances into the solvent [38]. In recent
years, several studies have compared the effects of UAE and
conventional solvent extraction on carotenoids recovery from dif-
ferent plant food materials and their by-products, such as tomato
[44,45,24], tomato wastes [40], carrot [4,42], corn [83], grapefruit
[82], auyama, cabbage, and lettuce wastes [5]. However, no
information on the ultrasound-assisted extraction of carotenoids
from pomegranate peels is available in the literature.
The objective of this work is to investigate the extractability of
pomegranate peels carotenoids using ultrasounds and different
vegetable oils as alternative solvents. In this way, a new process
for pomegranate peels application in food industries was devel-
oped based on an innovative, fast, and green method for producing
an oil naturally enriched with antioxidants, recovering carotenoids
from pomegranate wastes. Comparative studies between
ultrasound-assisted and conventional solvent extraction were car-
ried out in terms of processing procedure and total carotenoids
content. Fig. 1. Particle size distribution of milled pomegranate peels.
A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830 823

where d is the thickness of the spectrophotometer cell (1 cm) and C


is the content of carotenoids in mg/kg oil.

2.6. Oil quality

To examine the effect of ultrasound on oil quality, the untreated


sunflower oil and the oil treated with ultrasound at the optimum
conditions were analyzed for acid value [8], peroxide value (PV)
[9], and conjugated dienes [10].
In order to estimate the stability of carotenoids during
ultrasound-assisted extraction, identification of the carotenoids in
the extract was carried out by means of high-performance liquid
chromatography (HPLC) as described by Mendes et al. [48]. A Supel-
cosilTM LC-18 column (Supelco Inc., Bellefonte, PA) was used to sepa-
rate individual carotenoids at ambient temperature (25 °C). Samples
(50 lL) were dissolved in methanol/dichloromethane (1:1, v/v) and
the mobile phase, methanol with 10% (v/v) acetonitrile, was
delivered at a flow rate of 1 mL/min under isocratic conditions. Peak
Fig. 2. Production of vegetable oil enriched with carotenoids using: (a) conven- assignment was performed by comparing the retention times and
tional organic solvent extraction, (b) ultrasound–assisted extraction with a line spectral properties obtained from photodiode array detection
vegetable oil as an alternative solvent.
with a-carotene, b-carotene and lutein standards.
In addition, the DPPH radical (1,1-diphenyl-2-picrylhydrazyl)
Sunflower oil and soy oil were used as alternative solvents. A scavenging activity of the extracts was measured according to
sample of powdered pomegranate peels was mixed with 200 mL sol- the method described by Blois [11].
vent to produce different peels/solvent ratios. During the extraction
process, the sample container was held in a thermostat-controlled
2.7. Kinetic model
water bath. The extracts were collected at 10, 20, 30, 40, 50, and
60 min and filtered through glass microfiber paper to remove partic-
The solid-liquid extraction process can be considered as the
ulate residues before carotenoids analysis. reverse of an adsorption operation, therefore the second-order
The extraction temperature (T), the peels/solvent ratio (S/L), and
law was applied to experimentally evaluate the extraction rate
the amplitude level (A) were varied between 20 and 60 °C, 1/10 [61]. The general second-order model can be written as [52]:
and 3/10 (g/mL), and 20 and 60%, respectively. A central composite
design was applied to determine the effects of the above parame- dC t
ters on extraction yield. The effects were studied at five experi- ¼ k  ðC e  C t Þ2 ð2Þ
dt
mental levels a, 1, 0, +1, and +a, where a = 2n/4 and n is the
number of variables. where k is the second-order extraction rate constant (L/g min), Ce is
Extraction yield, Y, was defined as the percent ratio of the total the equilibrium concentration of carotenoids in the liquid extract
weight of carotenoids extracted to the dry peels sample weight. (g/L) (extraction capacity), and Ct is the carotenoids concentration
(g/L) in the liquid extract at a given extraction time t.
2.4. Conventional solvent extraction The integrated rate law for a second-order extraction under the
boundary conditions t = 0 to t and Ct = 0 to Ct, can be written as an
A traditional solvent extraction was applied based on the Eq. (3) or a linearized equation (4) [60]:
method optimized by Sachindra et al. [64] and used by Parjikolaei
et al. [53]. Five grams of peels sample was weighed and repeatedly k  t  C 2e
extracted using 25 mL of mixed hexane and isopropanol (Hex: IPA, Ct ¼ ð3Þ
1 þ k  t  Ce
60:40 v/v) until no further pigment was extracted by the solvent
(four times). In order to separate the phases and remove traces
t 1 t
of IPA in each step, the extract was washed with an equal amount ¼ þ ð4Þ
(100 mL in total) of 0.1% NaCl solution. The supernatant was C t k  C 2e C e
collected and evaporated under vacuum at 35 °C using a rotary
evaporator R-210 (Rotovapor R114, Waterbath B480, Büchi, Flawil, The initial extraction rate, h (g/L min), when t approaches 0, can be
Switzerland). The resulting carotenoids concentrate was re- defined as:
dissolved in 4 mL of acetone before carotenoids analysis. All exper-
iments were performed in dim light. h ¼ k  C 2e ð5Þ

2.5. Carotenoids analysis


2.8. Statistical analysis
Three grams of oil were accurately weighed and dissolved in
cyclohexane up to a final volume of 10 mL. Carotenoids content The data were analyzed using the statistical software MINITAB
was calculated from the absorption value, A, of the oil solution at (Release 13.32). Regression analysis was used to fit a full second
470 nm and the specific coefficient for lutein, Eo = 2000, using the order polynomial, reduced second order polynomials, and linear
Eq. (1) [36]: models to the data of the response variable. F values for all reduced
and linear models with an R2 > 0.70 were calculated to determine if
A  106 the models could be used in place of full second order polynomials
C¼ ð1Þ
2000  100  d to predict the response of a variable to the independent variables.
824 A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830

3. Results and discussion improved extraction performance, whereas the reduction in the
particles size by ultrasound disintegration will increase the num-
3.1. Extraction yield ber of cells directly exposed to extraction by solvent and ultrasonic
cavitation [79].
In overall, the highest concentrations obtained depending on In all experiments, the extraction yield (Y) was time dependent
the applied extraction solvent were 0.6134 and 0.6715 mg carote- and increased with extended ultrasonic times, especially from 10
noids/100 g of dry peels using sunflower oil and soy oil, respec- to 30 min, but slowly from 30 to 60 min (Fig. 4). Thus, the efficient
tively (Fig. 3). During an extraction process, a low solvent extraction period for achieving maximum yield of pomegranate
viscosity is usually associated with an improved solvent migration peel carotenoids was about 30 min. This can be attributed to the
through the matrix to increase extraction efficiency [55]. Fasina fact that extraction presents two stages; the first stage, which is
and Colley [25] and Diamante and Lan [21] reported viscosity characterized by a rapid rate, involves the penetration of the
values of 0.0234–0.0250 and 0.0232 Pa s (at 38 °C) for sunflower solvent into the cellular structure followed by the dissolution of
oil and soy oil, respectively. Thus, the higher extraction yield soluble constituents in the solvent, whereas the second one
obtained for soy oil may be attributed to its lower viscosity. How- involves the external diffusion of soluble constituents through
ever, the effect of solvent type on extraction yield was not statisti- the porous structure of the residual solids and its transfer from
cally significant (p P 0.05). A similar trend was reported by the solution in contact with the particles to the bulk of the solution
Sachindra and Mahendrakar [65], who studied the extractability [28]. A similar trend was reported by Zhang et al. [84], Pan et al.
of shrimp wastes carotenoids in different vegetable oils. Highest [52], Li et al. [42], Kaderides et al. [34], and Kalamara et al. [35],
carotenoids yield of 26.3 lg/g waste was obtained by extraction who extracted oil from flaxseeds, antioxidants from dry pomegra-
with sunflower oil. However, the extraction yield of carotenoids nate marc, carotenoids from carrots, phenolic compounds from
in soy oil, coconut oil, and rice bran oil was similar to that in pomegranate peels, and oil from pomegranate seeds, respectively.
sunflower oil. They attributed this observation to the fact that ultrasonic wave
Extracting four times with a fresh mixture of Hex:IPA extracted could disrupt the cell walls, so larger contact area between solvent
nearly all the carotenoids present in the waste material. Based on and material was created and more oil appeared on the surface.
this, extracting once with the green solvents and using ultrasound However, this effect would be increasingly weak on the inner cell
successfully extracted about 85.7 and 93.8% of the total carote- walls as the distance is increased. Thus, the ultrasonic waves affect
noids present in the waste material. As carotenoids are degraded the mass transfer rate mainly in the solvent penetration stage. In
to some extent during extraction, reducing the extraction time is addition, as the pomegranate peel cell walls ruptured, impurities
important both from a process time and a yield point of view. such as insoluble substances are suspended in the extract, lower-
Improved extraction yields may be explained in terms of a) oil- ing the solvent permeability into cell structures [46,76]. Further-
soluble property of carotenoids and b) cavitational effects caused more, target components also re-adsorb into the ruptured tissue
by the application of high-intensity ultrasound. As large amplitude particles, due to their relatively large specific surface areas, lower-
ultrasound waves travel through a mass medium, they cause com- ing yields of peel phenolics [22]. Ahmad-Qasem et al. [3] reported
pression and shearing of solvent molecules resulting in localized that, during phenolic extraction from olive leaves, the ultrasound
changes in density and elastic modulus. As a consequence, the application led to an immediate leaching of polyphenols into the
initially sinusoidal compression and shear waves will at a finite solvent; thus, 84% of total phenolics content was extracted during
distance from the ultrasonic transducer be distorted into shock the first 5 min of ultrasound treatment. Therefore, ultrasound
waves. The abrupt decrease in pressure at the edge of the saw effects accelerated the solubilization of accessible antioxidant
tooth shaped ultrasonic wave in the negative pressure cycle gener- compounds (washing effect) and contributed to the extraction of
ates small bubbles. These bubbles collapse in the positive pressure the non-accessible compounds. A review of the literature also
cycle and produce turbulent flow conditions associated with high brings opposite results to light, thus, Jerman et al. [33] determined
pressures and temperatures [58,43]. In addition, ultrasound facili- that the extraction efficiency of polyphenols from olive fruit was
tates swelling and hydration and causes enlargement of the pores low for the first 4 min of ultrasound application, indicating that
in the cell wall [79]. Diffusion through the plant cell walls, disrup- longer times were needed for wall disruption. This mild effect
tion, and washing out of the cell contents were also attributed to

0.6
A = 40%, T = 40oC, S/L = 0.2 g/mL
Y (mg carotenoids/100 g dry peels)

0.5
Sunflower oil
0.4 Soy oil
A = 28%, T = 52oC, S/L = 0.14 g/mL
0.3

0.2

0.1

0
0 10 20 30 40 50 60
t (min)

Fig. 4. Extraction yield (Y) of carotenoids from pomegranate peels as a function of


Fig. 3. Box plot showing the effect of solvent (vegetable oil) type on extraction time (t) for some experiments (continuous lines and closed symbols for sunflower
yield (Y). oil; dotted lines and open symbols for soy oil).
A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830 825

could be linked to the level of ultrasonic power applied, since these Table 1
authors carried out the experiments in an ultrasonic bath, which Regression analysis of central composite design.

actually supplies lower ultrasonic intensities than probe systems Sunflower oil Soy oil
like the one used in the current study. Variable Coefficient p-Value Coefficient p-Value
As shown in Fig. 5 and Table 1, the effect of temperature on the
Constant 1.5841 0.001 0.5005 0.150
carotenoids content extracted by vegetable oils was significant. A 0.04085 0.001 0.008812 0.286
Increasing extraction temperature from 20 to 40 °C, extraction T 0.02011 0.011 0.018857 0.022
yield increased, whereas an opposite trend was observed when T S/L 6.348 0.005 1.688 0.299
increased from 40 to 60 °C. The first effect may be attributed to A*A 0.0003254 0.002 0.0000863 0.242
T*T 0.0002885 0.005 0.0001316 0.076
the fact that an increase in temperature increases solubility and
S/L * S/L 10.089 0.014 0.951 0.747
diffusion coefficients of the compounds to be extracted and A*T 0.0001004 0.494 0.0000362 0.717
decreases the viscosity of the solvent, thus facilitating its passage A * S/L 0.08172 0.006 0.01211 0.544
through the solid substrate mass. However, at temperatures higher T * S/L 0.00119 0.968 0.04397 0.029
than 40 °C, the tendency of impurities dissolution will also increase
and some thermal labile constituents will decompose [22]. Chemat
et al. [13], who compared conventional and ultrasound-assisted which increased the contact surface area between solid and liquid
extraction of carvone and limonene from caraway seeds, reported surfaces and caused greater penetration of the solvent into the peel
that the activation energies for the ultrasound procedure are much matrix. At high amplitude levels, cavitational bubble collapse is
lower compared with those obtained by the control procedure, more violent [74]. According to Zhang et al. [84], since the temper-
which explains the enhancement of extraction in ultrasound ature and pressure were very high inside the bubbles and the col-
experiments at low temperatures. Comparing the effect of temper- lapse of bubbles occurred over a very short time, a violent shock
ature on the carotenoids content in soy oil with that in sunflower wave and a high-speed jet were generated, which could enhance
oil, the lower effect observed may be associated with the lower the penetration of the solvent into the cell tissues and accelerate
influence of temperature on the viscosity of soy oil compared to the intracellular product release into the solvent by disrupting
that of sunflower oil. Fasina and Colley [25] and Diamante and L. the cell walls. However, for amplitude levels above 40%, the
M [21]. reported activation energy values of 23.40–24.64 and increase in A led to a decrease in yield, possibly due to degradation
21.58–22.95 kJ/mol for sunflower oil and soy oil, respectively. of the plant material.
The extraction yield improved with increased amplitude level As far as the ratio of peel/solvent (S/L) is concerned, the extrac-
(A) up to values around 40% (Fig. 5). This effect may be due to tion yield increased with decreasing the ratio up to values around
the improved cavitation and mechanical effect of ultrasound, 0.2, a trend that is consistent with the mass transfer principles.
Higher solvent/solid ratio resulted in larger concentration gradient
during the diffusion from the solid into the solution and, thus, in
higher carotenoids concentration in the extract. Zhang et al. [84]
and Qu et al. [60] also reported this effect of solvent/sample ratio
on the extraction yield of chlorogenic acid from Eucommia
ulmodies, oil from flaxseed, and antioxidants from pomegranate
marc, respectively. However, in the case of sunflower oil, where
the effect of S/L is significant (Table 1), with further decrease in
solid-to-liquid ratio, a decrease in carotenoids content was
observed. A similar observation was reported by Prasad et al.
[57] and Kaderides et al. [34], who found the maximum extraction
yield of total phenolics from Mangifera pajang and pomegranate
peels at a solid/solvent ratio of about 0.03. Sachindra and Mahen-
drakar [65] found a marginal decrease in carotenoids extraction
yield by further increasing the solvent (oil)/solids ratio from 2 to
3 and hence there is no additional advantage of increasing the ratio
above 2. Regarding soy oil as a solvent, no statistically significant
effect of peels/solvent ratio was observed (Table 1).
Using the central composite design, the effect of the examined
variables on extraction yield was analyzed. The variables
evidencing statistically significant effects were screened via
Student’s t-test for ANOVA (Table 1). According to the ANOVA
analysis of the optimization study, temperature, peels/solvent
ratio, and amplitude level influence significantly the extraction
yield using sunflower oil (p < 0.05) (Table 1). These parameters also
showed a significant quadratic effect. Regarding soy oil as a
solvent, the extraction temperature, with a probability value of
0.022, was determined to be the only significant factor. The desir-
ability profile for optimum carotenoids yield indicates that the
maximum desirability level of 1.0 (on a scale of 0–1) can be
achieved with a temperature of 51.5 °C, an amplitude level of
58.8%, a peels/solvent ratio of 0.10 g/mL, and sunflower oil as
solvent (Fig. 6). Under these optimized conditions, the predicted
value for extraction yield was 0.3291 mg carotenoids/100 g of dry
Fig. 5. Main effects of amplitude level (A, %), extraction temperature (T, °C),
peels/solvent ratio (S/L, g/mL) on extraction yield (Y, mg carotenoids/100 g dry peels, whereas the observed experimental value was found
peels) for the two vegetable oils. 0.3255 mg carotenoids/100 g of dry peels.
826 A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830

a carotenoids enriched oil is based on the classic extraction using


an organic solvent. This conventional method consists of several
additional operation steps, such as solvent evaporation and recy-
cling and molecular distillation or vacuum drying to eliminate
residual traces of undesirable solvents according to the regulations
in force. These additional steps result in high input cost, energy
consumption, and generation of hazardous solvent waste. Gener-
ally, reducing the number of steps in a process chain leads to a
reduction in costs and better use of energy.
According to Kaderides et al. [34], while conventional extraction
procedures are often time and/or energy consuming, ultrasound-
assisted extraction provides numerous advantages from an indus-
trial perspective. Ultrasound as a food processing technology has
shown large commercial large scale application, with high returns
on capital investment. Improvements in product efficiency, process
enhancement, and low maintenance cost are achievable on a com-
Fig. 6. Optimization of green ultrasound-assisted extraction of carotenoids from mercial scale. Also, depending on the application, the required
pomegranate peels. energy is comparable to those of other operation units currently
utilized in the industry [56].
In addition, vegetable oils as substitutes to organic solvents,
The process proposed in this work was based on the ultrasound- besides being biodegradable and non-toxic, do not emit VOCs
assisted extraction of carotenoids using a vegetable oil as an alter- (volatile organic compounds) and they have technical perfor-
native solvent. In this way, an oil enriched with antioxidants was mances comparable with those of petrochemical solvents. One sig-
produced. On the contrary, the conventional method for producing nificant advantage of using vegetable oils is that there is no need

Fig. 7. Effect of amplitude level (A, %), extraction temperature (T, °C), and peels/solvent ratio (S/L, g/mL) on kinetic parameters of extraction using sunflower oil.
A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830 827

Fig. 8. Effect of amplitude level (A, %), extraction temperature (T, °C), and peels/solvent ratio (S/L, g/mL) on kinetic parameters of extraction using soy oil.

for subsequent separation of oil and carotenoids since the pig- difference between the two oils. The acid value (0.13 and 0.12 mg
mented oil can find use as carotenoids source in different products, KOH/g oil for the treated and the untreated oil, respectively) and
such as aquaculture feeds [39]. According to Spinelli and Mahnken the percentage of conjugated dienes (0.064 and 0.066% for the trea-
[69], in aquaculture feed preparations, vegetable oil or fish oil is ted and the untreated oil, respectively) were about the same and
commonly used as a source of energy. The use of pigmented oil only a slight increase in peroxide value was observed. PV increased
in feeds thus serves the dual purpose of pigment carrier as well a from 5.68 meq O2/kg oil for the untreated oil to 6.22 meq O2/kg oil
source of lipid energy. Sowmya and Sachindra [68] extracted measured immediately after sonication of sunflower oil. However,
carotenoids using vegetable oils and found that the enriched oil the Codex Alimentarius standard for the quality of oils states a
has a protective effect against ammonia-induced stress in common maximum acid value of 4.0 mg KOH/g oil and a maximum peroxide
carp (Cyprinus carpio) and prevents lipid peroxidation in the tissues value of 15 meq O2/kg oil, thus, the treated oil is below the limit
exposed to ammonia. Sachindra and Mahendrakar [66] used despite the increase in PV value observed after the ultrasound-
carotenoids pigmented oil as a colorant in fish sausage and assisted extraction.
reported that addition of carotenoids enhanced the sensory color, In addition, the chromatograms correspond to carotenoids
flavor, and overall quality score of sausage, whereas the added extracted by ultrasound at the optimum conditions and organic
carotenoids were stable during processing. solvent showed that there was no carotenoids degradation in son-
However, the flavor and composition of some edible oils may be icated sunflower oil. b-carotene was the main carotenoid detected
deteriorated by ultrasound treatment [14,54]. According to Chemat in pomegranate peels extracts obtained by both ultrasound and
et al. [15], the ultrasonic oxidation of edible oils is probably conventional techniques, made up 93% of the total carotenoids
attributed to cavitation that influences structural and functional content, while the other carotenoids identified, such as a-
components up to the point of lipid oxidation and deterioration. carotene and lutein, were only present in small amounts. A similar
Metals such as copper, which occur naturally in edible oils, in observation was reported by Sun et al. [73] and Li et al. [42], who
combination with ultrasound cavitation, were also suspected as found that the ultrasonic degradation of b-carotene is typically
possibly responsible for the formation of oxyradical species. A slow in comparison with that of more volatile aromatics that dif-
comparison of untreated sunflower oil and oil treated with ultra- fuse more readily into the cavitation bubble in an aqueous system.
sounds at the optimum conditions showed that there was no major As far as the antioxidant activity is concerned, carotenoids
828 A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830

Table 2
Best model predictions for the kinetic parameters (Ce, h, k) in relation to the processing factors, amplitude level (A), extraction temperature (T), peels/solvent ratio (S/L).

Parameter Model R2
Sunflower oil
Ce 2:53 þ 0:0792  A þ 0:0448  T þ 4:35  S=L  0:000618  A2  0:000544  T 2  0:131  A  S=L 0.918
h 0:338 þ 0:0106  A þ 0:00597  T þ 0:580  S=L  0:000082  A2  0:000073  T 2  0:0174  A  S=L 0.892
k (105) 61:1 þ 2:0  A þ 1:1  T þ 98:4  S=L  3:3  A  S=L þ 0:3  T  S=L 0.938
Soy oil
Ce 1:03 þ 0:0354  T þ 6:60  S=L  0:000251  T 2  10:5  S=L2  0:0713  T  S=L 0.902
h 0:0562 þ 0:00102  A þ 0:00269  T þ 0:111  S=L  0:000011  A2  0:000017  T 2  0:00588  T  S=L 0.876
k (105) 6:3 þ 0:2  A þ 0:4  T  0:1  A2  0:1  T 2  0:6  T  S=L 0.956

extracted by ultrasound at the optimum conditions and organic ultrasound power, while the mass transfer coefficient for diffusion
solvent showed about the same antioxidant activity (13.69 and decreased with increasing ultrasound power.
14.08% inhibition for the ultrasound and the conventional method, The highest Ce, k, and h values were obtained at peels/solvent
respectively). Similar results were reported by Roidaki [62], who ratio values around 0.2. The kinetic parameters increase with the
concluded that UAE was proven to be effective for leaves extraction increase of the solid to liquid ratio up to a certain limit of the tested
for Leikora variety, concerning the antioxidant activity measured range. However, further increases in solid to liquid ratio did not
by DPPH and ABTS. translate into significant improvement in the yield. This observa-
tion can be explained by the fact that the system has become sat-
3.2. Ultrasound kinetics urated as the solute has entirely dissolved in the fluid. A similar
trend was reported by Prasad et al. [57], Anwar et al. [7], Stam-
For all the factors studied, the plots of t/Ct versus t resulted in atopoulos et al. [71], and Kaderides et al. [34] during extraction
linear functions, in agreement with the second order leaching of phenolic compounds from Melastoma malabathricum fruit, olive
model expressed by Eq. (4). The slopes and intercepts allowed leaves, and peels of Mangifera pajang and pomegranate.
the determination of extraction capacities (Ce) and extraction rate Qu et al. [60] fitted the relationships between kinetic parame-
constants (k) from Eq. (4) and of initial extraction rates (h) from Eq. ters and processing factors (particle size, water/sample ratio, and
(5). Figs. 7 and 8 present the achieved values of Ce, k, and h. temperature) by linear, power or second-order polynomial func-
The kinetic parameters of carotenoids extraction were tions. However, they developed a different model for each factor.
enhanced with temperature increase and extraction at 40–50 °C In this work, multiple regression analysis was used to develop
had highest efficiencies. The values of kinetic parameters declined equations predicting the effect of all extraction factors simultane-
when the temperature was higher than 50 °C. According to Spigno ously (Table 2). Substituting equations presented in Table 2 into
et al. [70], an increase in temperature favors extraction due to the Eq. (4), a kinetic model for predicting carotenoids extraction from
enhancement of both solute solubility and diffusion coefficient, but pomegranate peels can be obtained.
beyond a certain temperature level, carotenoids can be denatured. Even though the empirical models in Table 2 cannot account for
This fact has already been reported in the literature, where there is the phenomena governing extraction processes, they could be used
a controversy surrounding the influence of temperature in antiox- to determine the effects of temperature, solids/solvent ratio, and
idants extraction processes. Thus, Jerman et al. [33] reported an amplitude level on the carotenoids extraction capacity during the
increase in extraction efficiency at temperatures of up to 45 °C extraction process. According to Goula [28], mechanistic models
for olive fruit phenolic compounds. The same trend was observed provide more from a basic understanding of a given system, a
by Zhang et al. [85] in the temperature range of 15–45 °C, where greater basis for extrapolation and a representation of a response
high temperatures reduced the extraction yield. González- function that is more precise than one attained empirically. In
Centeno et al. [27] reported that temperature has a positive effect the food industry, on the other hand, if it is desired to optimize a
only when it is not too high, as most of the bioactive compounds given unit process, the process of developing an empirical model
are susceptible to degradation at higher temperatures, reducing would most likely be more economically feasible. Such models
the observed extraction rate. However, Zhang et al. [86] found that may be more limiting than mechanistic models. However, for the
extraction yields rose as the temperature increased from 60 to purposes of the manufacturer, the main concern is narrowing the
80 °C, while Rostagno et al. [63] found that phenolics underwent range of processing variables to produce the best product possible.
an important degradation at temperatures of over 60 °C. Therefore, Thus, the empirical models in Table 2 should provide the guidance
it seems that the temperature influence may be product- for optimizing the extraction process decreasing the operating cost
dependent, it being necessary to determine the proper extraction and time.
temperature for a specific commodity.
As it can be seen in Figs. 7 and 8, the kinetic parameters 4. Conclusions
increased with increased amplitude level up to values around
40%, due to the improved cavitation and mechanical effect of ultra- An integrated approach for utilization of pomegranate peels is
sound. Similar results were also found for extraction of antioxi- suggested based on the ultrasound-assisted extraction of carote-
dants from pomegranate peels and seeds [52,28,34]. However, for noids using different vegetable oils as solvents. In this way, an oil
amplitude levels above 40%, the increase in A led to a small enriched with antioxidants is produced. On the contrary, the con-
decrease in kinetic parameters. A similar trend was reported by ventional method for producing a carotenoids enriched oil is based
Abdullah and Koc [1], who mentioned that the coefficients of equi- on the classic extraction using organic solvents. The proposed
librium concentration for the diffusion stage were higher than the method meets the terms of green process definition, since reduces
washing stage, which indicates that ultrasound power had a energy consumption and solvent amount, allows the use of renew-
greater effect during the diffusion stage than the washing stage. able natural products, and ensures a safe and high-quality extract/
The mass transfer coefficient for washing increased with increasing product. In addition, there is no need for subsequent separation of
A.M. Goula et al. / Ultrasonics Sonochemistry 34 (2017) 821–830 829

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