Ultrasonics Sonochemistry 16 (2009) 57–62

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

Simultaneous extraction of phenolic compounds of citrus peel extracts:

Effect of ultrasound
Ya-Qin Ma, Jian-Chu Chen, Dong-Hong Liu, Xing-Qian Ye *
Department of Food Science and Nutrition, Zhejiang University, Hangzhou 310029, China

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

Article history: Ultrasound-assisted extraction (UAE) has been widely applied in the extraction of a variety of biologically
Received 19 February 2008 active compounds including phenolic compounds. However, there is an insufficiency of information on
Received in revised form 25 March 2008 simultaneous extraction of these compounds in this area. In the present study, seven phenolic com-
Accepted 25 April 2008
pounds of two families including cinnamic acids (caffeic, p-coumaric, ferulic, sinapic acid), and benzoic
Available online 7 May 2008
acids (protocatechuic, p-hydroxybenzoic, vanillic acid) from citrus (Citrus unshiu Marc) peels were eval-
uated by UAE. The effects of ultrasonic variables including extraction time, temperature, and ultrasonic
Keywords:
power on the yields of seven phenolic acids was investigated. Results showed that the yields of phenolic
Extraction
Ultrasound
compounds increased with both ultrasonic time and temperature increased, whereas the opposite
Phenolic compounds occurred with increasing time at higher temperature to some certain. In the case of 40 °C, the decrease
Citrus peel in the yields of some phenolic compounds was observed with increased time, whereas those of other
compounds did not significantly declined. Ultrasonic power has a positive effect on the yields of phenolic
acids under study. Among all ultrasound variables, temperature is the most sensitive on stability of phe-
nolic compounds. Moreover, when phenolic compounds from citrus peel extracts were subjected to ultra-
sound process, the benzoic acids were more stable than the cinnamic acids. Meanwhile, the optimal
ultrasound condition was different one compound from another. These were partly attributed to both
the differently chemical structures of phenolic acids and the combination effects of ultrasonic variables.
Ó 2008 Published by Elsevier B.V.

1. Introduction cosmetics, and polymer industry. The ability of a number of meth-

Phenolic acids are widely present in plants. Fruits and vegeta-
bles are the major sources of phenolic acids in human diet [1].
The food and agricultural products processing industries produce
substantial quantities of phenolics-rich by-products, which have
gained much attention due to their antioxidant behavior and ben-
eficial health properties in chronic and degenerative diseases [2].
Citrus industry produces large quantities of by-products such as
peels and seed residues, which may account for up to 50% of the
total fruit weight [3]. Citrus by-products, if utilized fully could be
major sources of phenolic compounds. The peels, in particular,
are an abundant source of natural flavonoids, and contain higher
amount of phenolics compared to the edible portions [4–7]. Gorin-
stein et al. [8] reported that the contents of total phenolics in peels
of lemons, oranges, and grapefruit were 15% higher than those in
the peeled fruits.
Nowadays, renewed interest in the use of plant materials as a
source of naturally bioactive compound has grown. Phenolic
compounds produced by isolation of citrus fruit are promising
chemicals due to their increasing demand in food processing,
* Corresponding author. Tel./fax: +86 571 86971165.
E-mail address: psu@zju.edu.cn (X.-Q. Ye).
ods to extract phenolics compounds from citrus peels have been
evaluated, such as c-irradiation assisted extraction [9], solvent
extraction [10], enzyme-assisted extraction [11], and heat treat-
ment [12,13]. However, these extraction methods have drawbacks
to some degree. For example, c-irradiation assisted extraction still
is unknown to safety; solvent extraction have low efficiency and
consuming time; heat treatment results in pyrolysis, and enzyme
in enzyme-assisted extraction is easy to denature. Furthermore,
phenolic compounds are very sensitive to light, heat and oxygen.
Therefore, it is necessary to build efficient extraction method and
keep the stability of phenolic compounds.
UAE has attracted more and more attention due to its higher
extraction efficiency with shorter extraction time compared to tra-
ditional methods, such as maceration extraction and soxhlet
extraction. It uses sound waves at frequencies above the range
audible to humans (=20 kHz) to disrupt the plant cell wall thereby
enhancing solvent penetration into the plant material and facilitat-
ing the release of extracts [14]. In recent years, there have been
several reports on the application of UAE in the isolation of various
biologically active compounds from plant materials. For example,
release of hemicellulose from buckwheat hulls [15], extraction of
sensitive aroma compound from garlic [16], isolation of oil from ol-
ives [17], and UAE of phenolic compounds from coconut (Cocos

1350-4177/$ - see front matter Ó 2008 Published by Elsevier B.V.

doi:10.1016/j.ultsonch.2008.04.012
58 Y.-Q. Ma et al. / Ultrasonics Sonochemistry 16 (2009) 57–62
nucifera) shell powder [18]. Application of ultrasonic extraction of
bioactive principles from plants has also been reviewed [19].
Although determining the yields of phenolic compounds from
citrus phenolic have been widely described in many published pa-
pers [10–12,20], ultrasonic extraction of seven phenolic com-
pounds simultaneously from citrus peel, which was called as
simultaneously extraction in here, was not reported. In the present
paper, a comparison of the yields of phenolic compounds from UAE
at 60 kHz and maceration extraction was performed. The effect of
simultaneous UAE on the yield of seven phenolic compounds from
citrus peel was evaluated. High-performance liquid chromatogra-
phy (HPLC) coupled with photodiode array detection (PDA) was
developed in this study for measuring the yields of phenolic com-
pounds after ultrasonic treatment.
2. Materials and methods
2.1. Materials and reagents
The citrus (Citrus unshiu Marc) peels were purchased from a cit-
rus processing plant in Ningbo City, Zhejiang, China, in October
2006. The peels were dried in an oven with air circulation at
40 °C, and then they were finely ground in a laboratory grinder.
The dry plant material was then packed in paper bag and stored
at 20 °C for usage.
Standards of caffeic, p-coumaric, ferulic, sinapic, protocatechuic,
p-hydroxybenzoic, vanillic acids were purchased from Sigma (St.
Louis, MO). Methanol (HPLC grade), glacial acetic acid (HPLC grade)
and redistilled water were filtrated through a 0.45 lm membrane
before use. The chemical structures are shown in Fig. 1. All other
chemical reagents used in experiments were of analytical grade.
2.2. Apparatus
2.2.1. Ultrasonic device
The ultrasonic cleaning baths was produced by Guangzhou So-
noc Ultrasonic Electronic Equipment Co. Ltd., China. It has a fre-
quency of 60 kHz, and volume of ultrasonic bath is 1500 mL. The
Schematic diagram of the ultrasonic apparatus is described in pre-
vious paper [21]. Briefly speaking, ultrasonic equipment has an
a volume of 10 mL. The methanol solution was filtered through a
CH3O HO
COOH
COOH
HO HO
ferulic acid caffeic acid
CH3O
COOH
HO
HO OCH3
p-coumaric acid sinapic acid
b COOH
COOH
OH
OH
OH
protocatechuic acid p-hydroxybenzoic acid vanillic acid
Fig. 1. Chemical structures of cinnamic (a) and benzoic (b) acids.
electric current meter to measure output power consumed, a tem-
perature controller and a digital timer. In addition, a rotary gear
was designed, on which the beakers are placed, and the beaker ro-
tated when the rotary gear was drove by Motor.
2.2.2. High-performance liquid chromatography (HPLC) system
A Waters 2695–2996 system (Waters Corp., Milford, MA
equipped with 515 pump and a photodiode array (PDA) detector
was employed. The C-18 column used was reversed phase column
(250  4.6 mm, ID 5 lm, Agilent Technologies, USA).
2.3. Extraction methods
2.3.1. Maceration extraction
Powders of 2 g citrus peels and 40 mL of 80% methanol were put
into a 600 mL flask, which was placed on the rotary gear of ultra-
sonic cleaning baths and extracted by rotating flask at 40 °C for
1, and 8 h. This was performed as a control for comparison with
UAE. All samples were prepared and analyzed in triplicate.
2.3.2. Ultrasound-assisted extraction
Powder of 2 g ground peels was loaded into a 600 mL flask
(8 cm diameter  14.5 cm height), 40 mL 80% methanol was added.
UAE was performed at 3.2 W, at 15, 30, and 40 °C for 10, 20, 30, 40,
50, and 60 min. The effect of different levels of ultrasonic power
was determined by extracting at 3.2, 8, 30 and 56 W at 15 °C for
20 min. Materials in all experiments were carried out by rotating
flask, it has been described in previous paper [21]. After ultra-
sound, extracts were cooled to room temperature (15 °C) before
analysis of phenolic compounds. All samples were prepared and
analyzed in triplicate.
2.3.3. Phenolic compounds extraction
Phenolic compounds were isolated from extracts according to
previously described methods [22,23] with certain modifications.
A 10 mL aliquot of the filtrate was evaporated using a rotary vac-
uum evaporator at 35 °C until approximately 1 mL of filtrate re-
mained. The residue was hydrolyzed with 10 mL of 4 M NaOH for
4 h at room temperature, and then acidified to pH 2 with 4 M
HCl. The solution acidified was extracted three times with 25 mL
of diethyl ether/ethyl acetate (1:1, v/v). The clear organic phase
was combined and concentrated to dryness in a rotary vacuum
evaporator at 35 °C, and 80% methanol was added to make a final
0.45 lm microporous membrane and used for the identification
and quantification of the bound phenolic compounds. All extracts
were made in triplicates.
2.4. Chromatographic conditions
COOH
The HPLC chromatographic conditions were as follows: Column
temperature was maintained at 40 °C and the injection volume for
all samples was 10 lL. Elution was performed isocratically with the
mobile phase consisting of 4% (v/v) acetic acid in water: 100%
methanol (80:20, v/v) at a solvent flow rate of 1 mL/min. The col-
umn was washed with 100% methanol and equilibrated to initial
COOH
conditions for 15 min before each injection [24]. UV visible spec-
tral measurements were made over the range of 210–400 nm.
Chromatograms were recorded at 320 nm for cinnamic acids (caf-
feic, p-coumaric, ferulic, sinapic), and at 260 nm for benzoic acids
(protocatechuic, p-hydroxybenzoic, vanillic acid). Identification of
OH phenolic acids was based on retention times and UV–visible spec-
OCH3 tra in comparison with standards. Quantification of phenolic com-
pounds was achieved by the absorbance recorded in the
chromatograms relative to external standards. The concentration
of extracts was calculated from peak area according to calibration
 Y.-Q. Ma et al. / Ultrasonics Sonochemistry 16 (2009) 57–62
curves. The amount of each phenolic acid was expressed as micro-
gram per gram of dry weight (lg/g DW).
2.5. Statistical analysis
All samples were prepared and analyzed in triplicate. The re-
sults were compared by analysis of variance (ANOVA) using SPSS
for Windows (version 15.0.0 [6 September 2006, SPSS Inc.]). The
significant differences among the treatments were determined at
P < 0.05 levels using Duncan’s multiple range tests.
3. Results and discussion
3.1. Comparison of phenolic compounds extracted from citrus peel by
maceration extraction and ultrasound-assisted extraction
Table 1 shows that phenolic compounds extracted from citrus
peel by maceration extraction (ME) and UAE. There was an in-
crease in the yield of phenolic compounds with increasing macer-
ation time. After maceration treatment at 40 °C from 1 to 8 h, the
yields of caffeic, ferulic, vanillic acids increased from 12.46 to
31.72, 189.99 to 763.54, 19.23 to 29.99 lg/g of DW, respectively.
The yields of extracts, after UAE at 15 °C for 1 h (Table 1), were sig-
nificantly higher than those by maceration treatment at 40 °C for
8 h. The results showed that UAE gave higher extraction efficien-
cies at lower temperature compared to maceration method. How-
ever, the extraction yields of phenolic acids by UAE at 40 °C for 1 h
were lower than those by UAE at 15 °C for 1 h, indicating that UAE
at higher temperature resulted in reduction in the yields of the
phenolics. Likewise, in agreement with the previous finding [18],
this also showed that that UAE at low temperature enhanced the
yields of extracts.
3.2. The effect ultrasonic time and temperature on phenolic
compounds from citrus peel
The effects of ultrasonic time and temperature on the yields of
phenolic compounds from citrus peels are summarized in Fig. 2
(cinnamic acids) and Fig. 3 (benzoic acids). The yields of cinnamic
acids were generally higher than those of benzoic acids, and among
all phenolic acids, the yield of ferulic acid was highest. Similarly, it
has been reported that the contents of ferulic acid in Satsuma man-
darin (C. unshiu Marc.) peel extracts by hot water is highest [20].
For all detected phenolic acids under study, their yields de-
pended dramatically on extraction time and temperature. At rela-
tively lower temperature (15 and 30 °C), the yields of phenolic
acids increased with increased extraction time. For example, after
UAE at 15 °C for 40 min, the yields of caffeic, p-coumaric, ferulic,
p-hydroxy-benzoic acid increased from 15.4 to 103.7, 36.4 to
171.3, 452.3 to 1672.3, 18.3 to 42.0 lg/g of DW, respectively. In
agreement with our results, Sueli and Pinto [18] reported that
extraction time significantly affected the yields of phenolic com-
pounds from coconut shell powder. Likewise, the yield of phenolic
Table 1
Comparison of phenolic compounds (lg/g DW) extracted from dried Satsuma mandarin (Citrus unshiu Marc) peels with maceration extraction at 40 °C for 1, 8 h and ultrasound-
assisted extraction at 40 and 15 °C for 1 h
Extraction Extraction Caffeic p-Coumaric
method time
MEA 1h (40 °C) 12.5 ± 2.6dB 23.0 ± 1.7d
8h (40 °C) 31.7 ± 1.5c 63.2 ± 1.9c
UAE 1h (40 °C) 50.9 ± 0.5b 97.9 ± 1.2b
1h (15 °C) 97.5 ± 0.7a 177.3 ± 1.4a
A
ME = maceration extraction.
B
Mean ± SD of three replicated samples. Means in each column with different letters are significantly different (P < 0.05).
59
compounds increased also with extraction temperature increased.
For example, after UAE from 15 to 30 °C for 20 min, the yield of caf-
feic acid increased from 36.9 to 86.7 lg/g DW, 80.0 to 165.3 lg/g
DW in p-coumaric acid, 951.8 to 2283.3 lg/g DW in ferulic acid,
27.0 to 43.4 lg/g DW in p-hydroxy-benzoic acid, respectively. This
is consistent with previous findings, Herrera and Luque de Castro
[25] and Pinelo et al. [26] reported that the yields of phenolic com-
pounds from milled berries and grape pomace depended signifi-
cantly on extraction temperature and time. On the other hand,
higher temperatures beyond 50 °C induced the instability of phe-
nolic compounds [25]. In the investigation, when extraction tem-
perature up to 40 °C, the yields of phenolic acids decreased with
increased extraction time. For example, when ultrasonic extraction
was performed at 40 °C for 20 min, the yields of caffeic, p-couma-
ric, ferulic, p-hydroxy-benzoic acid decreased significantly from
99.3 to 57.3, 168.9 to 136.6, 2224.5 to 1242.152, 47.2 to 30.5 lg/
g of DW, respectively. This indicated high temperature may have
resulted in degradation of some phenolic acids. As has been re-
ported before [25], the degradation (close 100%) of phenolic com-
pounds from strawberries occurred by ultrasound. However, the
yields of sinapic, vanillic acid did not declined significantly with in-
creased extraction time at 40 °C. One of the possible reasons for
this phenomenon is that the stability of these compounds suffering
from high temperature was different. This may be partly ascribed
to the differences of their chemical structures.
Phenolic compounds contain two subgroups, i.e., the hydroxy-
benzoic and hydroxycinnamic acids [27]. And there are two types
of substituents in their aromatic rings, such as hydroxylic-type
and methoxylic-type substituents. It was found the higher stability
of phenolic compounds corresponding to the greater the number of
hydroxylic-type substituents and the smaller the number of meth-
oxylic-type substituents in their aromatic rings, and vice versa. In
the cases of stable phenolic compounds at higher temperature un-
der study, the sinapic acid contains two methoxylic-type substitu-
ents, and one for vanillic acid. Despite of caffeic acid having one
methoxylic-type substituents, it remained with suffering signifi-
cantly degradation at 40 °C for 20 min. In the cases of unstable
phenolic acids, caffeic, ferulic, p-coumaric, protocatechuic, and p-
hydroxy-benzoic acid contain only hydroxylic-type substituents
in their aromatic rings. Evaluation for the stability of simultaneous
extraction of phenolic compounds from plant materials by UAE has
not been fully reported. As an example, a stability study of phenolic
compounds using microwave-assisted extraction (MAE) showed
that a greater number of hydroxyl-type substituents are more eas-
ily degraded [28]. Although there was a similar trend to the effect
of the stability of phenolic acids by UAE and MAE, differences in
two cases were still significant. For example, both p-coumaric
and p-hydroxy-benzoic acids suffered significantly degradation
by ultrasound at 40 °C for 20 min, and have no suffered any degra-
dation by microwave at 175 °C. In addition, extraction efficiency at
higher temperature decreases, because there is a higher concentra-
tion of solvent molecules in the cavitational bubble which dampen
the collapse, and then decrease the forces that act on the surface of
Ferulic Sinapic Protocatechuic p-Hydroxy-benzoic Vanillic
189.0 ± 1.4d 40.4 ± 6.0c 17.6 ± 0.1b 15.0 ± 0.2d 19.2 ± 0.2c
763.5 ± 19.8c 132.39 ± 0.3b 20.7 ± 1.0a 23.5 ± 0.8c 30.0 ± 0.6b
1187.6 ± 5.3b 218.2 ± 2.2a 15.0 ± 1.6b 31.2±0.1b 40.1 ± 1.8a
2226.8 ± 27.1a 219.8 ± 8.5a 19.4 ± 1.4a 45.6 ± 0.7a 41.5 ± 1.6a
60 Y.-Q. Ma et al. / Ultrasonics Sonochemistry 16 (2009) 57–62

a 150 a 30
15 ºC 30 ºC 40 ºC

Yield of PR (ug/g DW)

120 24
Yield of CA (ug/g DW)

18
90

12
60
6
30
0
10 20 30 40 50 60
0 Time (min)
10 20 30 40 50 60
Time (min)
b 60

b 300

Yield of PH (ug/g DW)

48

250
36
Yield of SI (ug/g DW)

200
24
150
12
100
0
50 10 20 30 50 40 60
Time (min)
0
10 20 30 50 40 60 c 50
Time (min)

40
Yield of VA (ug/g DW)

c 250

30
200
Yield of PC (ug/g DW)

20
150
10
100
0
10 20 30 40 50 60
50 Time (min)

Fig. 3. Effect of ultrasonic time and temperature on the yields of benzoic acids from
0 Satsuma mandarin (Citrus unshiu Marc) peels by ultrasound-assisted extraction
10 20 30 40 50 60
using 60 kHz at 8 W. (a) PR = protocatechuic acid; (b) PH = p-hydroxy-benzoic acid;
Time (min) and (c) VA = vanillic acid.

d 3000

the peel [29]. Therefore, temperature was a sensitive ultrasonic

2400
Yield of FE (ug/g DW)

variable for extraction phenolics from citrus peel. We suggested

that extraction temperature in extracting citrus phenolic com-
1800 pounds by ultrasound should not exceed 40 °C.
As already discussed, a significant reduction in yields of ex-
1200 tracted phenolic compounds at higher temperature may be proba-
bly attributed to thermodegradation. However, it is also the
600 potential that polymerization reactions occurred due to the combi-
nation of various phenols by themselves, having an effect on the
analytical quantification [26]. Other works showed that polymeri-
0
10 20 30 40 50 60 zation in phenols happened widely [30,6]. Thus, whether decrease
Time (min) in the amount of citrus peel phenols by UAE was due to the degra-
dation or polymerization process. To clear the point, further works
Fig. 2. Effect of ultrasonic time and temperature on the yields of cinnamic acids
is under study.
from Satsuma mandarin (Citrus unshiu Marc) peels by ultrasound-assisted extrac-
tion using 60 kHz at 8 W. (a) CA = caffeic acid; (b) SI = sinapic acid; (c) PC = p-cou- For each phenolic acid under study, the optimal conditions to
maric acid; and (d) FE = ferulic acid. give the highest yields of phenolic acids by UAE varied from one
 Y.-Q. Ma et al. / Ultrasonics Sonochemistry 16 (2009) 57–62 61

Table 2
Yields of phenolic compounds (lg/g DW) extracted from dried Satsuma mandarin (Citrus unshiu Marc) peels with ultrasound-assisted extraction at 60 kHz and at 15 °C for 20 min

Phenolic acids Ultrasonic power (W)

3.2 8 30 56
Caffeic 36.9 ± 3.2cA 51.13 ± 1.8b 57.01 ± 2.1a 61.45 ± 0.8a
Sinapic 124.0 ± 10.4b 138.2 ± 7.6b 155.6 ± 6.7a 157.9 ± 1.7a
p-Cinnamic 79. 6 ± 2.4c 92.8 ± 3.5b 106.8 ± 1.2a 115.8 ± 13.0a
Ferulic 951.9 ± 41.2d 1126.9 ± 37.6c 1299.5 ± 88.0b 1420.0 ± 96.2a
Protocatechuic 18.8 ± 0.4b 19.2 ± 1.9a 20.6 ± 0.4a 20.8 ± 0.6a
p-Hydroxy-benzoic 37.1 ± 0.1a 27. 6 ± 1.5c 31.8 ± 1.7b 32.3 ± 0.2ab
Vanillic 28.8 ± 0.3b 30.1 ± 1.4ab 32.6 ± 1.1a 34.6 ± 0.2a
A
Mean ± SD of three replicated samples. Means in each low with different letters are significantly different (P < 0.05).

compound to another. According to Figs. 2 and 3, the optimal
extraction condition for caffeic acid is at 30 °C for 40 min, sinapic
acid was at 30 °C for 30 min, vanillic acid is at 40 °C for 20 min.
Generally, the yields of cinnamic acids increased significantly at
30 °C for 40 min. However, the yields of benzoic acids have an in-
creased trend at 40 °C for 10 min. Likewise, it has been reported
that the effect of ultrasonic variables on the extraction of multi-
bioactive compounds from Hypericum perforatum L. varied from
one compound to another [31]. Different physi-chemical proper-
ties of phenolic compounds may be account for different extraction
efficiencies of phenolic acids under the same ultrasonic parame-
ters. We will attempt to do more work in the effect of UAE on sim-
ple phenolic acids in the future.
To sum up, the choice of appropriately extraction temperature
and time were crucial to increase the extraction yields of phenolic
acids. During UAE, a temperature of 40 °C reduced the yield of
some phenolic compounds extracted from peel.
3.3. The effect ultrasonic power on phenolic compounds from citrus
peel
which is particularly favorable for extraction of thermally unstable
components from vegetable materials. In addition, UAE resulted in
the reduction in yield of phenolic compounds with increased
extraction temperature and time, it was probably due to thermal
degradation or polymerization reactions of phenols themselves.
Likewise, the optimal ultrasound condition for each phenolic com-
pound was significantly different. Therefore, simultaneous extrac-
tion of several phenolic compounds by UAE should be considered
the differences of their chemical structures and the combination
effect of ultrasonic variables.
Acknowledgements
The work was financial supported by National Key Technologies
R&D program of China during the 11th Five-Year Plan Period
(2006BAD27B06): Development and industrialization of functional
foods: and by Zhejiang Key R&D Project: extraction, isolation and
purification of bioactive substances from plants (2005C12017).
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The effect of ultrasonic power on the yields of phenolic com-
pounds from citrus peels is shown in Table 2. A positive effect on
the yields of phenolic compounds was observed with increase of
ultrasonic power. When ultrasonic power increased from 3.2 to
30 W, the yields of most phenolic compounds were significantly
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