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DOI: 10.1111/jfpe.12880
ORIGINAL ARTICLE
1
Department of Biotechnology Engineering,
Kulliyyah of Engineering, International Islamic Abstract
University of Malaysia, Kuala Lumpur, Penaeus monodon is a species of shrimp with astaxanthin content that prevents various diseases
Malaysia
and enhances immune system. High-pressure processing (HPP) is capable of achieving higher
2
International Institute for Halal Research and
extraction astaxanthin yield within short processing time. The aim of this research was to opti-
Training (INHART), International Islamic
University of Malaysia, Kuala Lumpur, mize the extraction condition of astaxanthin from P. monodon using HPP using response surface
Malaysia methodology (RSM). The investigation was carried out using variables: pressure (150–250 MPa),
3
Herbarium Unit, Department of Landscape holding time (10–20 min), and amount of acetone-methanol mixture, 7:3, vol/vol (3–7 ml). The
Architecture, Kulliyyah of Architecture and optimum condition was achieved at the pressure of 238.54 MPa, 16.29 min of holding time,
Environmental Design, International Islamic
University of Malaysia, Kuala Lumpur,
and 6.59 ml of solvent mixture. The optimum yield of astaxanthin was 95.17 μg/gdw. The R2
Malaysia value was 0.9836 and the adjusted-R2 value was 0.9688. These values indicate that the applica-
Correspondence tion of RSM to optimize the yield of astaxanthin with HPP has a significant impact in enhancing
Irwandi Jaswir, Department of Biotechnology the yield of astaxanthin.
Engineering, Kulliyyah of Engineering,
International Islamic University of Malaysia,
Jalan Gombak, Kuala Lumpur, Malaysia.
Email: irwandi@iium.edu.my
Funding information
Ministry of Higher Education, Malaysia, Grant/
Award Number: MIRGS13-01-001-0002;
International Islamic University Malaysia;
Ministry of Higher Education
damage and color changes, as well as higher stability of substrates meat were separated from the samples and then stored directly in a
(Gamlath & Wakeling, 2011; Kaur & Rao, 2017). freezer for 2 days at −21 C. Next, the samples were dried using a
HPP system consists of four important components. These freeze dryer (Tokyo Rikakikai Co., Japan) for 3 days, crushed using a
include a pressure vessel, a pressurization fluid, an intensifier, and a blender to form a powder, and stored in a freezer at −21 C for
pump (Ferstl & Ferstl, 2013). The machine needs to be handled with further treatment.
caution as the sensors are crucial and sensitive components. It will be
maintained at the present pressure by controlling a valve (Niu, Zhao, &
2.2 | Extraction of astaxanthin using HPP
Tian, 2014). The principle of HPP is twofolds: Pascal’s and isobaric
The extraction procedure was relevant to the previous work (Othman,
principles. Pascal’s principle is based on the application of a static fluid
2009) and modified using the HPP method (Du et al., 2013). The HPP
of external power in a sealed container, resulting in the transmission
of an equal pressure change to all parts of the fluid. The isobaric prin- equipment (Toyokoatsu Co., Ltd., Japan) has capability up to 400 MPa
ciple states that there is no size or shape effect of pressure on a liquid with one liter volume container. The conditions (Table 1) were set up
medium in a closed environment since the applied pressure is identical with holding time (10–20 min), pressure (150–250 MPa), and amount
from all directions (Huang, Hsu, Yang, & Wang, 2014). In addition, of acetone-methanol mixture (3–7 ml). The equipment works under
HPP method depends on various operating variables to obtain the room temperature with manual set up. In this experiment, all samples
optimum condition (Theodore, 2011). were run in triplicate at room temperature throughout the experimen-
Factors, responses, and levels are three important terms in the tal design (Table 2) and well packaged using plastic bag. One gram of
optimization of design. Factors are independent variables, responses the sample was added into a plastic bag with a mixture of acetone and
are dependent variables, and levels involve the factor variables methanol (7:3, vol/vol). The headspaces in the plastic bag were
selected (Myers, Montgomery, & Anderson-Cook, 2009). In the removed before it sealed and then it loaded into the container. The
current study, three independent variables were considered to equipment was required to be pumped manually until the pressure
increase the effects of dissolving astaxanthin: pressure, holding time, reached 90 MPa, hence, the pressure raised up automatically and run
and amount of solvents. These variables are the factors used to based on the setting. The extracted then centrifuged at 10,000 × g
increase the yield of astaxanthin (Du et al., 2013). for 10 min. Its supernatant was added with an equal volume of
The optimized condition is designed using design of experiment distilled water and hexane (1:1, vol/vol). After the upper layer was
(DOE) in order to obtain the optimum condition and yield (Anthony, collected and dried under oxygen-free nitrogen, it was immediately
2008). Quantitative data of response surface method is used to solve stored in a freezer at −80 C for further analysis.
Process variables
Run Holding time (min) Pressure (MPa) Amount of solvents (ml) Astaxanthin (μg/gdw) (experiment) Astaxanthin (μg/gdw) (predicted)
1 20.00 150.00 3.00 23.52 1.14 26.88
2 15.00 200.00 5.00 72.15 1.07 74.93
3 6.59 200.00 5.00 37.92 1.42 32.22
4 15.00 284.09 5.00 55.06 0.70 53.28
5 15.00 115.91 5.00 32.85 1.12 27.54
6 15.00 200.00 5.00 75.58 0.88 74.93
7 15.00 200.00 8.36 58.39 0.81 55.40
8 15.00 200.00 5.00 77.25 1.04 74.93
9 15.00 200.00 5.00 70.63 0.79 74.93
10 10.00 150.00 3.00 12.56 0.48 16.17
11 15.00 200.00 5.00 75.86 0.94 74.93
12 23.41 200.00 5.00 42.56 0.95 41.18
13 10.00 250.00 7.00 64.56 1.26 66.21
14 20.00 250.00 7.00 64.76 1.65 66.16
15 10.00 150.00 3.00 9.98 0.78 13.67
16 20.00 250.00 7.00 31.74 0.52 33.06
17 20.00 200.00 3.00 18.56 0.77 18.86
18 15.00 200.00 1.64 10.12 0.78 6.02
19 15.00 200.00 5.00 76.89 0.85 74.93
20 10.00 150.00 7.00 22.89 1.02 27.59
Table 1 lists the values of independent variables of optimization each other. This value indicates that the variables contributed positively
investigated in the extraction of astaxanthin. CCD was used for to the response (Cohen, Cohen, West, & Aiken, 2013).
optimization using RSM in Design Expert software v.7.0.0.
end capped. The solvents used as the mobile phases were acetonitrile FIGURE 2 Normal probability plot of residuals
and distilled water at the ratio of 9:1 (vol/vol) (mobile phase A) and ethyl
response (Khuri & Mukhopadhyay, 2010). The range was chosen based
acetate (mobile phase B). The gradient elution used was 60–40% sol-
on the optimum point of a previous study (Du et al., 2013). Holding
vent A–B (0–20 min), 40–60% solvent A–B (20–25 min), 0–100% sol-
time was investigated because HPP is functioning to shorten the pro-
vent A–B (25–25.1 min), 100–0% solvent A–B (25.1–35 min), and
cessing time while organic solvents may lead to environmental pollu-
100–0% solvent B (35–35.1 min) at a flow rate of 1.0 ml/min. The col-
tion (Du et al., 2013; Muntean et al., 2016). Pressure is an important
umn temperature was 20 C. The detection range was set at
parameter in HPP since it helps to open the pore of cells and therefore
350–550 nm with the volume injection of 10 μl. The quantitative analy-
solvents to enter the cells of shrimp carapace, hence it helps hasten
sis of astaxanthin yield was calculated using Microsoft Excel by referring
the biochemical reaction involving solvents (Uhm & Yoon, 2011). How-
to the linear regression of the astaxanthin standard curve prepared with
ever, a temperature is not selected as a variable in the optimization
correlation coefficient of 0.98 and in the range of 0.5–2.5 μg/ml.
study because astaxanthin is susceptible to oxidation when stimulated
by heat. The nutritional value also will be reduced due to the thermola-
bile characteristic (Handayani, Indraswati, & Ismadji, 2008). Hence,
3 | RESULTS AND DISCUSSION
HPP is the most relevant method to be used in order to extract astax-
anthin since it is a nonthermal processing technology (Armenta &
3.1 | Optimization of astaxanthin yield by RSM Guerrero-Legarreta, 2009; Barbosa-Cánovas & Juliano, 2008).
The significance of the interaction of three variables (holding time, The normal probability plot of residuals is shown in Figure 2. It is
pressure, and amount of solvents) and two levels can be represented clear that most residuals are on the straight line shown in the figure.
by the model in the optimization using RSM. RSM is able to control The SD of studentized residuals was estimated to measure the studen-
the variables of the optimum setting in order to obtain maximum tized residuals, which are the quotient resulting from the division of a
Source Sum of squares Degrees of freedom (df ) Mean square F value Prob > F
Model 11,664.31 9 1,296.03 66.55 <0.0001 Significant
A 96.98 1 96.98 4.98 0.0497 *
B 799.66 1 799.66 41.06 <0.0001 **
C 2,943.89 1 2,943.89 151.16 <0.0001 **
AB 15.21 1 15.21 0.78 0.3976
AC 13.76 1 13.76 0.71 0.4203
BC 845.22 1 845.22 43.40 <0.0001 **
A2 2,633.03 1 2,633.03 135.19 <0.0001 **
B2 2,146.19 1 2,146.19 110.20 <0.0001 **
C2 3,521.94 1 3,521.94 180.84 <0.0001 **
Residual 194.76 10 19.48
Lack of fit 158.28 5 31.66 4.34 0.0666 Not significant
Pure error 36.48 5 7.30
Cor. Total 11,859.07 19
*Significant.
**Highly significant.
IRNA ET AL. 5 of 8
TABLE 4 Analysis of the model fitting for astaxanthin yield These values indicate that the variables (holding time, pressure, and
Elements Values Elements Values amount of solvents) contributed positively to the response.
SD 4.41 R-squared 0.9836
Mean 46.69 Adj R-squared 0.9688 3.3 | Graphical analysis for yield optimization
C. V. % 9.45 Pred R-squared 0.8941
RSM plays a key role for dependent variables to identify a maximum
PRESS 1,256.33 Adeq precision 22.082
response of the optimum values from independent variables. It shows
residual. Referring to Figure 2, the residuals were studentized and the contours of constant response of two-dimensional (2D) and three-
values were greater than +2 and less than −2. It shows that the resid- dimensional (3D) graphs with the axis system being a specific pair of
uals followed a normal distribution and the majority of the data points the two design variables, while the other design variables remain con-
are distributed along the fitted line, which are fairly close with reason- stant. The interactions between holding time and pressure, as well as
able outliers (Anuar, Mohd Adnan, Saat, Aziz, & Mat Taha, 2013). between holding time and amount of solvents, were insignificant
according to the value of Prob > F. Therefore, the contour plot and 3D
3.2 | Analysis of variance surface shown involved the interaction between pressure and amount
of solvents because these variables have significant Prob > F values.
Analysis of variance (ANOVA) provides a means to examine the effect
The model equation of effects is drawn using a 2D contour plot
of qualitative factors on qualitative results. ANOVA was evaluated
and a 3D response surface plot (Figures 3–5) to illustrate the indepen-
using a quadratic model (Table 3). The F value of this study was 66.55.
dent variables and interactive effects of each independent variable
This implies that the model is a significantly useful model. The distri-
(Dejaegher, Durand, & Heyden, 2010). The significance or
bution of the independent variables of probability for N samples was
estimated using the p value (Prob > F). Table 3 shows that A, B, C, BC,
A2, B2, and C2 are significant model terms. The model terms are not
significant if the values are greater than 0.1. From the findings, hold-
ing time (A), pressure (B), and amount of solvents (C) influenced the
extraction of astaxanthin because the values of Prob > F are less than
0.05. Factor A had a significant influence on the response because its
Prob > F was close to 0.05, while B and C had highly significant effects
on the response because the Prob > F was <0.0001 (Mudge, Baker,
Edge, & Houlahan, 2012).
The estimation of the variables according to the application of
RSM, both response and tested variables in coded units according to
an empirical relationship, is represented through the following regres-
sion equation:
TABLE 5 Validation of developed quadratic model with the optimum constituents (mean SE)
Yield
Run Holding time (min) Pressure (MPa) Amount of solvent (ml) Experiment μg/gdw Predicted μg/gdw % error
1 17.25 233.76 6.02 80.23 83.63 0.54 4.24
2 16.29 238.54 6.59 80.94 84.17 0.36 3.99
3 17.05 240.68 6.32 79.48 83.35 0.77 4.87
Hence, the highest astaxanthin yield was observed approximately (pressure, holding time, and amount of solvents) indicates that the appli-
82 μg/g when the pressure was fixed to approximately 225 MPa and cation of RSM could optimize the yield of astaxanthin. Moreover, HPP
the amount of solvents was increased to 6 ml. The exerted pressure is has proven its potential as an alternative astaxanthin extraction method
limited in order to avoid excessive levels that have been shown to cause that can be conducted in shorter time and with good properties.
oxidation and affect food quality (Shankar, 2014).
CONFLIC T OF INT E RE ST
3.4 | Model validation
The authors confirmed that there are no known conflicts of interest
In order to assess model accuracy, the criterion for numerical solution
associated with this publication.
was evaluated by running optimized solutions with the highest
desirability (Table 5). The predicted values were compared with exper-
imental values and the percentage of errors was calculated. The result ACKNOWLEDGMENTS
of the three confirmation experiments was presented in Table 5. The authors would like to thank for the Ministry of Higher Education
The percentage of error varied from 3.99 to 4.87%. Table 5 shows
(MOHE) and International Islamic University Malaysia (IIUM) for the
that the optimum condition of the model based on the validation is
Research Grant MIRGS13-01-001-0002.
the second run with a yield of astaxanthin at 84.17 μg/g and error of
3.99%. This condition then was carried out using HPLC then qualita- ORCID
tively analyzed based on the retention time (13 min) with astaxanthin
Cicy Irna https://orcid.org/0000-0003-0586-8258
standard chromatogram. In addition, the quantitative analysis
(Figure 6) resulted at 95.17 0.63 μg/gdw for the yield of astax-
anthin with a pressure of 238.54 MPa, holding time of 16.29 min, and RE FE RE NC ES
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