Article

Evaluation of bioactive compounds of black mulberry

juice after thermal, microwave, ultrasonic processing,
and storage at different temperatures

Bo Jiang1,2, Nitin Mantri3, Ya Hu4, Jiayin Lu5, Wu Jiang4 and

Hongfei Lu1,4

Abstract
The effect of different sterilization methods (thermal, microwave, and ultrasonic processing) on the main
bioactive compounds and antioxidant activity of black mulberry juice during selected storage time (8 days)
and temperatures (5, 15, and 25  C) was investigated. The antioxidant activity of thermal-treated juice
depleted with storage time, whilst both ultrasound- and microwave-treated juices showed transient increase
in antioxidant activity during the first 2 days that later decreased with storage time. Lower temperature storage
preserved more bioactive compounds and antioxidant activity, especially in ultrasound sterilized samples.
The activation energy values were 15.99, 13.07, and 12.81 kJ/mol for ultrasonic, microwave, and thermal
pasteurization processes, respectively. In general, ultrasound-sterilized samples showed higher total phen-
olics, anthocyanin, and antioxidant activity compared to the microwave- and thermal-processed juice during
the storage time especially at lower temperatures.

Keywords
Black mulberry juice, anthocyanin content, antioxidant activity, thermal, ultrasound, storage
Date received: 23 November 2012; accepted: 5 May 2014

INTRODUCTION and easily susceptible to degradation through a

Recently, fruit juice obtained from mulberry (Morus
species) is increasingly being promoted and consumed
because of the reported nutritional and health benefits
(Hojjatpanah et al., 2011). It is a rich source of bio-
active compounds including phenolic substances like
flavonols and anthocyanins with high antioxidant activ-
ity (Isabelle et al., 2008). Anthocyanins are the most
important phenolic compounds present in berry fruits
that are of special significance because of their contri-
bution to total antioxidant activity of the fruit
(Hassimotto and Genovese 2007). The major anthocya-
nins identified in mulberries are cyanidine-3-glucoside
and cyanidine-3-rutinoside (Hojjatpanah et al., 2011;
Suh et al., 2003). These anthocyanins are unstable
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DOI: 10.1177/1082013214539153
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number of factors such as light, pH, oxygen, enzymes,
ascorbic acid, and temperature during storage and
especially heat processing (Hojjatpanah et al., 2011;
Kennedy et al., 2001). The stability of anthocyanins
found in foods decreases during processing and stor-
age as temperature rises (Cavalcanti et al., 2011).
Anthocyanins show great susceptibility toward pH
1
College of Life Science, Zhejiang Sci-Tech University, Hangzhou,
China
2
College of Biology and Food Engineering, Changshu Institute of
Technology, Changshu, China
3
Health Innovations Research Institute, School of Applied
Sciences, RMIT University, Melbourne, Australia
4
College of Chemistry and Life Science, Zhejiang Normal
University, Jinhua, China
5
Division of General Studies, University of Illinois at Urbana-
Champaign, Champaign, IL, USA
Corresponding author:
Hongfei Lu, College of Life Science, Zhejiang Sci-Tech University,
Hangzhou, 310018, China.
Email: luhongfei63@yahoo.com.cn

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Food Science and Technology International 0(0)
being more stable in acidic media at low pH values than
in alkaline solutions with high pH values (Brouillard,
1982; Cavalcanti et al., 2011).
Sterilization is an essential process to improve the
shelf-life and safety of mulberry juice. Conventional
thermal processing of fruit juice remains the most
widely adopted technology for shelf-life extension and
preservation of fruit juice. However, it often leads to
detrimental changes in the sensory qualities of the juice
(Odriozola-Serrano et al., 2008). Ultrasound processing
is a promising non-thermal processing technology and
a potential alternative or supplement to traditional
thermal pasteurization (Tiwari et al., 2009c). The use
of sonication to provide fresh high-quality, microbio-
logically safe, and high-nutritional-value fruit juices
continue to be an area of research as shown in recent
studies conducted on orange juice (Valero et al., 2007),
strawberry juice (Tiwari et al., 2008), and blackberry
juice (Tiwari et al., 2009a). Microwave pasteurization
offers similar benefits to conventional methods, but
with an improved product quality and reduced time
of exposure to energy (Cañumir et al., 2002). Several
studies have successfully been conducted on the micro-
wave pasteurization of fruit juices, as it preserves the
natural organoleptic characteristics of the juice and
reduces the time of exposure to energy, with the subse-
quently lower risk of losing essential thermolabile nutri-
ents (Igual et al., 2010).
Evaluating the influence of different sterilization
methods on the bioactive compounds of mulberry
juice during storage is essential for determining the
best conditions for preserving the bioactive properties
of the juice. In addition, no information is available on
the degradation kinetics of anthocyanins during the
storage of ultrasound- and microwave-processed mul-
berry juice to predict the quality changes that occur
during storage. Hence, the main objective of this
study was to investigate the effect of different steriliza-
tion methods including thermal, microwave, and ultra-
sound sterilization on the quality attributes of black
mulberry juice as well as the anthocyanin degradation
kinetics of these differently processed mulberry juices
during storage.
MATERIALS AND METHODS
Sample preparation
Black mulberry fruits (Morus nigra L) were purchased
from a local fruit market in Jinghua (Zhejiang, China).
Black mulberries were selected on the basis of a similar
degree of ripeness and apparent fruit quality. The fruits
were squeezed using a domestic juice extractor
and immediately filtered using four layers of cheese
cloth to remove the pulp before different sterilization
treatments.
2
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Experimental design
All fresh juice filtrated was randomly divided into three
groups (three individuals per group) among which one
group was treated by thermal sterilization, and others
were treated with microwave and ultrasonic processing,
respectively. The total phenols, anthocyanin content,
and 2,20 -diphenyl-1-picrylhydrazyl (DPPH) radical
scavenging activity of black mulberry juice before
and after three different pasteurization processes were
measured to evaluate the effect of different methods of
sterilization on the quality of mulberry juice.
Treatments
A 650 -W high-intensity ultrasonic processor (Ningo
Scientz biotechnology Co. Ltd., Ningbo, China) with a
6-mm titanium probe whose immersion depth was
25 mm in a 100 mL test tube was used for juice sonic-
ation. The juice samples were sonicated for 30 min and
processed at a constant frequency of 20 kHz (Bhat et al.,
2011). In the case of ultrasonic-treated juice, samples of
50 mL were placed in a 100 mL jacketed vessel through
which water at 20  1  C was circulated at a flow rate of
0.5 L/min. The microwave process was performed in a
microwave oven (Galanz WD900ASL23-5 S, 23 L,
900 W). Each time, 50 mL of the juice was treated by
microwave for 30 s (Igual et al., 2010). For thermal pas-
teurization, 50 mL of the juice was heated in glass tubes
in a thermostatic water bath operating at 90  C for 30 s.
After the different sterilization processes these black
mulberry juices were rapidly cooled in an ice bath and
were poured separately into sterile test tubes; then these
samples of every sterilization treatment were stored in
incubators at 5, 15, and 25  C, respectively in the dark
for 8 days. Samples were randomly taken and analyzed
for each index every day during storage. All analyzed
samplings were carried out in triplicate.
Chemicals and reagents
Trolox and DPPH free radical were of analytical grade
and purchased from Sigma-Aldrich (St. Louis,
MO, USA). Gallic acid and Folin–Ciocalteu reagent
(purity 99%), were purchased from Shanghai
Sangon Biological Engineering Technology & Services
Co., Ltd. (Shanghai, China).
Total phenols content determination
The total phenols content was determined by using
Folin–Ciocalteu reagent method, as described by our
previous study (Lu et al., 2012). Total phenols assay
was conducted by mixing 0.5 mL of black mulberry
juice sample, 8.25 mL of deionized water, 0.5 mL
of Folin–-Ciocalteu reagent, and 0.75 mL of 20%

Na2CO3. After 40 min of reaction in a water bath at
40  C, the absorbance of the reaction mixture was mea-
sured at 755 nm using a spectrophotometer. Results
were expressed as milligrams gallic acid equivalents
(GAE) per 100 mL of juice.
DPPH radical scavenging activity determination
The DPPH free radical scavenging activity was evalu-
ated according to the method described by Zheng et al.
(2010). Briefly, 0.1 mL mulberry juice sample was mixed
with 10 mL of 0.03 g/L DPPH (2,2-diphenyl-1-picrylhy-
drazyl) ethanol solution at room temperature. The
diluted solution (0.1 mL) with 10 mL distilled water
was used as control. The absorbance was measured at
517 nm after 30 min of reaction in the dark. Scavenging ations among the data obtained. Statistical analyses
activity was measured in triplicate samples. The percent-were carried out using the statistical analysis systems
age of DPPH radical scavenging activity of each plant
extract was calculated using the following equation
 
A0  ðA1  As Þ
Scavenging activity ð%Þ ¼  100
A0
ð1Þ of anthocyanins in various processed mulberry juices
where A0 is the absorbance of the control solution (con-
taining only DPPH), A1 is the absorbance of the DPPH
solution containing plant extract, and As is the absorb-
ance of the sample extract solution without DPPH.
The value was measured in triplicate samples.
Anthocyanins content determination
Total anthocyanins content of each sample was mea-
sured using the modified pH differential method
described by Zheng and Lu (2011), using two buffer
systems: potassium chloride 0.025 M at pH 1.0 and
sodium acetate 0.4 M at pH 4.5. Briefly, 1 mL of
sample was transferred to a 10 mL volumetric flask
and made up with each buffer. The absorbance of
each equilibrated solution was then measured at 510
and 700 nm, using a UV–Vis spectrophotometer.
Quartz cuvettes of 1-cm path length were used, and
all measurements were carried out at room temperature
(25  C). Absorbance readings were made against dis-
tilled water as a blank. The total anthocyanins content
was calculated on the basis of cyanidin-3-glucoside
(Alasalvar et al., 2005) with a molecular weight
of 445.2 g/mol and an extinction coefficient of
29,600 L/mol cm (Giusti and Wrolstad, 2001), as
AC ¼ ½ðA510  A700 ÞPH 1:0  ðA510  A700 ÞPH 4:5 
MWDF1000="L
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Jiang et al.
where MW is the molecular weight of cyanidin-3-gluco-
side, DF is the dilution factor, L is the path length in
cm, and " is the molar extinction coefficient for cyani-
din-3-glucoside. Results were expressed as milligram
cyanidin-3-glucoside equivalents (CGE) per 100 mL
of juice.
Statistical analysis
The data of total phenolic compounds, anthocyanin,
and antioxidant activity were expressed as
mean  standard deviation (SD) from three steriliza-
tion treatments (each treatment with three samples)
and each sample with three replications. Pearson’s
correlation coefficient was used to calculate correl-
(SAS, version 9.0) software package and Excel stat-
istical tools (Microsoft software). The data were
graphically plotted by using OriginLab (OriginPro,
version 8.0).
Experimental data were fitted to a first-order kinetic
model (equations (2) and (3)) to describe the evolution
during storage. This kinetic type was expressed by the
following equations
C ¼ C0 expðktÞ ð3Þ
T1=2 ¼  ln 0:5=k ð4Þ
where C and C0 are anthocyanins content at time t
and zero (day), respectively and k is the first-order
rate constant, while T1/2 is the half-life and t is the
storage time.
Temperature-dependence of anthocyanin degrad-
ation rate constant was determined by the Arrhenius
equation
k ¼ A expðEa =RTÞ ð5Þ
where A is the frequency factor (per day), Ea is the
activation energy (kJ/mol), R is the universal gas con-
stant (8.314 J/mol/K), and T is the absolute tempera-
ture (in Kelvin, K).
In addition, temperature quotients (Q10) were calcu-
lated from the following equations
Q10 ¼ kðT þ 10Þ=kðTÞ ð6Þ
where k(T þ 10) is the rate constant at (T þ 10) and
ð2Þ k(T) is the rate constant at T.
3
Food Science and Technology International 0(0)

RESULTS AND DISCUSSION by ultrasonic and microwave treatments than by ther-

mal process (Igual et al., 2010; Zheng and Lu, 2011).
Changes in total polyphenol
Furthermore, the possible reason for the observed high-
The content of total phenolics during the 8 days of est values of phenolic compounds in the samples after
storage ranged from 228.9 to 252.0, 231.0 to 253.3, ultrasonic processing might be attributed to the add-
and 237.5 to 258.1 mg per 100 mL for conventional ition of sonochemically generated hydroxyl radicals
thermal-, microwave-, and ultrasound-treated juice, (OH) to the aromatic ring of the phenolic compounds
respectively (Figure 1). Ultrasonic and microwave pro- which has been reported to enhance the antioxidant
cesses could avoid the decrease in the total phenolic activity of the phenolics (Ashokkumar et al., 2008;
content more availably when compared to the thermal Bhat et al., 2011).
pasteurization (Figure 1). This is probably because the Furthermore, in the first 5 days, the total phenolic
polyphenoloxidase, peroxidase, and b-glucosidase in content of all mulberry juices decreased. However,
the juice samples have been inactivated more heavily

(a) 95
(a) 265 90

Anthocyanins (mg/100mL)
Total phenols (mg/100 mL)

260 c 85
255 c 80
250 b
b c 75
b b
245 b 70
b
b b
240 a 65
a a
235 a 60
a
230 a a 55
225 50
0 1 2 3 4 5 6 7 8
0 1 2 3 4 5 6 7 8
(b) 265 (b) 95
Total phenols (mg/100 mL)

90
260
Anthocyanins (mg/100mL)

c 85
255
c 80
250 b b
c 75
245 c b
c
c 70
240 a b b
b b 65
235 a a
a 60
230 a
a a 55
225
50
0 1 2 3 4 5 6 7 8 0 1 2 3 4 5 6 7 8
(c) 265
(c) 95
Total phenols (mg/100 mL)

260 90
Anthocyanins (mg/100mL)

255 b 85
c
250 80
c
245 c b 75
a c
c b
240 b 70
b
235 b a
a a 65
b a
230 60
a a
225 a
55
0 1 2 3 4 5 6 7 8 50
Storage time (days) 0 1 2 3 4 5 6 7 8
Storage time (days)
Figure 1. Effect of thermal (), microwave (), and ultra-
sound (r) sterilizations on total phenols of black mulberry Figure 2. Effect of thermal (), microwave (), and ultra-
juice during storage at (a) 5  C, (b) 15  C, and (c) 25  C sound (r) sterilizations on anthocyanins of black mulberry
(p < 0.05). juice during storage at (a) 5  C, (b) 15  C, and (c) 25  C.

4
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prolonged storage of the juices at selected temperatures
resulted in increase in the total phenolic content toward
the end of storage period for all juices (Figure 1).
Similar behaviors were observed in grapefruit juice
(Igual et al., 2010), blueberry juices (Barba et al.,
2012), and six dark fruit juices (Piljac-Žegarac et al.,
2009) during storage. This decrease of phenols during
storage can be explained in such a way that some com-
pounds are formedthat react with the unspecific Folin–
Ciocalteu reagent and significantly decrease the phen-
olic content (Escarpa and González, 2001; Vinson
et al., 2001). Some studies found the existence of a
little peroxidase in the juices processed by pasteuriza-
tion treatment, which promote to react with oxidation
and significantly enhance phenolic content (Igual et al.,
2010; Zheng and Lu, 2011). Other possible reason of
increase in the total phenolic content with prolonged
storage is that the formation of novel compounds such
as Maillard reaction products had antioxidant activity
(Manzocco et al., 2001).
Changes in anthocyanins
The initial anthocyanin content expressed as cyaniding-
3-glucoside was 89.61 mg per 100 mL (Figure 2). For all
methods, the degradation rate of black mulberry antho-
cyanins increased with storage time and temperature.
However, anthocyanin loss was greater in thermal
sterilization compared to microwave and ultrasound
sterilized juices during all temperature storage.
Anthocyanin content decreased by 36%, 37%, and
45%, respectively when thermally processed juice was
stored at 5, 15, and 25  C for 8 days. Comparatively,
anthocyanin content of microwave and ultrasound
sterilized juices reduced between 28–38% and 24–
34%, respectively during the same storage period
Table 1. Kinetic parameters for anthocyanins of black mulberry juice treated by different sterilization methods during
storage
Temperature
Treatment (  C) K  102 (days)
Thermal 5 5.25  014
15 5.88  0.19
25 7.75  0.23
Microwave 5 4.06  0.065
15 4.61  0.11
25 6.03  0.12
Ultrasound 5 3.18  0.11
15 3.68  0.089
25 5.07  0.14
Data are the means  SD of three samples, each with three replicates.
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Jiang et al.
(Figure 2). Different studies have demonstrated the
effectiveness of ultrasound in achieving high anthocya-
nin retention (Ashokkumar et al., 2008; Bhat et al.,
2011; Tiwari et al., 2009a,b). Tiwari et al. (2009b) sug-
gested that the level of anthocyanin degradation due to
sonication was relatively low and compares favorably
to thermal processing. They also demonstrated that son-
ication could be employed as a preservation technique
for blackberry (Tiwari et al., 2009a) where anthocyanin
retention is desired.
The kinetic parameters of anthocyanin degradation
during storage at selected temperatures are shown in
Table 1. The degradation of anthocyanins in all pro-
cessed black mulberry juice samples stored at selected
temperatures were fitted to a first-order kinetic model
(Figure 2), confirming the results of previous studies
reporting the same model in other fruit juices during
storage (Alighourchi and Barzegar, 2009; Kirca et al.,
2007; Wang and Xu, 2007). Anthocyanin content was
found to follow first-order degradation with R2 > 0.945.
For all sterilization methods, the degradation rate
increased at higher storage temperatures, which sug-
gested that high temperature accelerated the anthocya-
nin degradation (Kirca et al., 2007). The lowest
degradation rate value of anthocyanins was for ultra-
sound followed by microwave and least for thermal
sterilization. Similar results were observed in grape
and blackberry juices (Tiwari et al. 2009a,b). The pos-
sible reason was that the higher retention in anthocya-
nins may be caused by cavitation, which governs
various physical, chemical, or biological reactions
(Tiwari et al. 2009a).
To determine the effect of storage temperature on
the parameters, the constants obtained from equation
(4) were fitted to an Arrhenius-type equation (Figure 3).
The calculated activation energy values of the samples
Q10
T1/2 (days) Ea (kJ/mol) 5–15  C 15–25  C 5–25  C
13.20  0.36 12.81  0.88 1.12  0.040 1.32  0.049 1.21  0.021
11.79  0.37
8.94  0.26
17.07  0.28 13.07  1.37 1.14  0.028 1.31  0.045 1.22  0.014
15.03  0.35
11.49  0.23
21.79  0.75 15.99  1.52 1.16  0.042 1.38  0.043 1.27  0.024
18.83  0.46
13.69  0.37
5
Food Science and Technology International 0(0)

3.5 (a) 32 c
3.4 30 b c

DPPH Scavenging activity (%)

3.3 b c
28 b
3.2
26 a b c
3.1 a c
a c b
3.0 24
-lnk

b b
2.9 a b
22
2.8 a
20 a
2.7 a a a
2.6 18
2.5 16
2.4 14
3.30 3.35 3.40 3.45 3.50 3.55 3.60 3.65 0 1 2 3 4 5 6 7 8
1/T 103(°K) (b) 32
c
30 b c

DPPH Scavenging activity (%)

Figure 3. The Arrhenius plots for degradation of antho- 28 b
cyanins in black mulberry juice processed by thermal (),
26 b
microwave (), and ultrasound (r) sterilization methods a b b
during storage. 24 c
c
22 a b b
b
varied with the different methods of sterilization 20 a b
a
(Table 1). The values were 12.81 kJ/mol for thermal, 18 a a
13.07 kJ/mol for microwave, and 15.99 kJ/mol for a
a
16
ultrasound sterilization. Higher activation energy
14
implied that the degradation of anthocyanins in ultra- 0 1 2 3 4 5 6 7 8
sonic sterilized samples is more stable to temperature (c) 32
elevations (Vikram et al., 2005). 30 c
DPPH Scavenging activity (%)

Temperature quotient (Q10) values were also calcu- 28 b b

lated for the temperature ranges of 5–15, 15–25, and b
26
5–25  C (Table 1). According to these values, the least b
24 a
effect of temperature rise on anthocyanin degradation b b
was observed in thermal sterilized juice, followed by 22
c
a c
microwave and ultrasound sterilized samples, respect- 20 b c
a b
ively indicating that degradation of anthocyanin in 18 b a
ultrasonic processing needed higher energy. 16 a a
a a
14
0 1 2 3 4 5 6 7 8
Changes in antioxidant activity Storage time (days)

As shown in Figure 4, the antioxidant activity of ther-

mal-treated juice depleted with storage time, whereas
both ultrasound- and microwave-treated juices
showed increase in antioxidant activity during the first
2 days of storage. Moreover, at the end of the storage,
all the sterilized juices exhibited a significant decrease in
antioxidants varying from 30% to 42% for thermally
treated juice, 30% to 40% for microwave-treated
juice, and 23% to 35% for ultrasound-sterilized juice.
Increase in antioxidant activity during the first few days
of storage has been previously reported for dark fruit
juices (Piljac-Žegarac et al., 2009) and during the first
few hours of incubation of apple juice (Van der Sluis
et al., 2005) at elevated temperature. According to
Pinelo et al. (2004), the increase in the activity may be
explained by the strong tendency of polyphenols to
undergo polymerization reactions, whereby the result-
ing oligomers possess larger areas available for charge
Figure 4. Effect of thermal (), microwave (), and ultra-
sound (r) sterilizations on antioxidant activity of black
mulberry juice during storage at (a) 5  C, (b) 15  C, and
(c) 25  C (p < 0.05).
delocalization. When the degree of polymerization
exceeds a critical value, the increased molecular com-
plexity and steric hindrance reduce the availability of
hydroxyl groups in the reaction with the DPPH rad-
icals. This causes a resultant decrease in the antiradical
capacity. This may explain the observed decrease in
antioxidant activity of our mulberry juices, which
decreased after the initial transient increase.
The antioxidant capacity is related to the amount
and composition of bioactive compounds present in
food (Odriozola-Serrano et al., 2008). In this study,
for all sterilization methods used, the DPPH values

6
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correlated well with anthocyanin levels (R2 ¼ 0.794–
0.816). This demonstrates that anthocyanin is one of
the main antioxidant compounds in black mulberry
juice. However, there was no significant correlation
between the total phenolic content and antioxidant
activity of thermal processing (R2 ¼ 0.581), microwave
(R2 ¼ 0.509), and ultrasound (R2 ¼ 0.279) sterilized
juices. These Endings are in agreement with those of
other researchers who observed no significant correl-
ation between total phenolic content and radical
scavenging activity in currant, pomegranate, cherry,
and a few berry species. (Amakura et al., 2000;
Piljac-Žegarac et al., 2009).
CONCLUSIONS
This study investigated the effect of thermal, micro-
wave, and ultrasound sterilization methods on the
phytochemical content of black mulberry juice when
stored at different temperatures. The higher stability
of nutritional quality of black mulberry juice was
achieved at the lowest temperature. Anthocyanin deg-
radation of all sterilized juices followed the first-order
reaction kinetics. Variation of degradation rate con-
stants with temperature obeyed the Arrhenius relation-
ship. In the black mulberry juice anthocyanins, total
phenolics, and antioxidant activity degraded more
quickly with increasing temperature during storage.
For all storage temperatures, ultrasound sterilized
juice was found to have higher retention of total phen-
olics, anthocyanins, and antioxidant activity compared
to microwave and thermally processed juice. This work
demonstrates that ultrasonic processing should be a
preferred method for sterilizing mulberry juice products
where retention of nutritional quality is desired upon
storage.
AUTHOR CONTRIBUTIONS
Jiang B, Mantri N, and Hu Y contributed equally to this
work.
FUNDING
This work was supported by Zhejiang Provincial University
Top Key Discipline of Biology, Science and Technology Key
Project of Jiangsu Province (BE2012416), Six Key Talents
Program of Jiangsu (2011NY032), and Science and
Technology Project of Changshu City (CN201302).
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