Download as pdf or txt
Download as pdf or txt
You are on page 1of 6

Food Chemistry 197 (2016) 597–602

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Nutrient composition and antioxidant activity of gonads of sea urchin


Stomopneustes variolaris
Ayyagari Archana ⇑, K. Ramesh Babu
Department of Marine Living Resources, Andhra University, Visakhapatnam, India

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

Article history: The study investigated, for the first time, proximate nutritional composition and antioxidant activity of
Received 18 May 2014 gonads from the sea urchin, Stomopneustes variolaris, inhabiting the coastal area of Visakhapatnam
Received in revised form 13 October 2015 (India). Moisture, ash, proteins, lipids and carbohydrate content were 77.53% ± 0.80, 3.76% ± 0.25,
Accepted 1 November 2015
12.10% ± 0.41, 4.98% ± 0.36 and 1.63% ± 0.18, respectively, based on dry weight. The gonads were rich
Available online 2 November 2015
in essential amino acids (ca. 32.1% of total amino acids) with the most predominant being phenylalanine,
lysine and valine. The essential to non-essential amino acid ratio was 0.5. Polyunsaturated fatty acids
Chemical compounds studied in the article:
(PUFA) constituted 22.01% ± 2.2 of total fatty acids. The x6:x3 ratio was 0.94. Total phenol content of
Hydrochloric acid (PubChem CID: 313)
Trisodium citrate (PubChem CID: 6224)
the gonad was 9.90 ± 0.01 mg GAE/g and the IC50 of the extract, using the 1,1-diphenyl-2-
Methanol (PubChem CID: 887) picrylhydrazyl (DPPH) assay, was 57.81 lg/ml.
Perchloric acid (PubChem CID: 24247) Ó 2015 Elsevier Ltd. All rights reserved.
Boric acid (PubChem CID: 7628)
Sodium hydroxide (PubChem CID: 14798)
O-phthalaldehyde (PubChem CID: 4807)
Sodium hypochlorite (PubChem CID:
23665760)
Sodium chloride (PubChem CID: 5234)
Boron trifluoride (PubChem CID: 6356)
Petroleum ether (PubChem CID: 5794)
Folin–Ciocalteu’s reagent (PubChem CID:
516996)
Gallic acid (PubChem CID: 370)
1,1-Diphenyl-2-picrylhydrazyl (DPPH) assay
(PubChem CID: 74358)
Ascorbic acid (PubChem CID 54670067)

Keywords:
Sea urchin
Gonads
Proximate composition
Antioxidant
Stomopneustes variolaris

1. Introduction for foreign exchange earnings by way of exports. As such, many


new species of sea urchins have been explored for edibility. Though
Sea urchin gonads (roe or uni) have gained importance because palatability and non-toxicity are of primary concern for edibility,
of their economic, nutritional and health potential. Gonads of sea biochemical profile of the roe influences the acceptability of sea
urchin species, such as Loxechinus albus, Paracentrotus lividus, urchin as a food (Lawrence, 2001).
Strongylocentrotus droebacheinsis, Anthocidaris crassipina, are con- Nutritionally sea urchin gonads are a rich source of lipids,
sumed as sea food in certain parts of the world. Edible sea urchins carbohydrates and proteins. These influence organoleptic proper-
or parts thereof have a good international market with potential ties, such as colour, texture, firmness and flavour, which affects
gonad quality (Siikavuopio, Dale, & Carlehog, 2007). Gonads are
⇑ Corresponding author at: Department of Marine Living Resources, Andhra prized for their yellow orange colour, bitter-sweet flavour, and
University, Visakhapatnam 530 002, Andhra Pradesh, India. distinctive aroma (Gracia, Lopez-Hernandez, Gonzalez-Castro,
E-mail address: archana.ayyagari@yahoo.com (A. Archana). Rodriguez De Quiros, & Simal-Loranzo, 2000; Shpigel, Mc Bride,

http://dx.doi.org/10.1016/j.foodchem.2015.11.003
0308-8146/Ó 2015 Elsevier Ltd. All rights reserved.
598 A. Archana, K.R. Babu / Food Chemistry 197 (2016) 597–602

Marciano, Ron, & Ben-Amotz, 2005). Some gonads are a source of 2.3. Amino acid analysis
vitamins, minerals and other micronutrients although the diet of
the sea urchin can influence biochemical composition of the 2.3.1. Chemicals used
gonads (Chen et al., 2010). This can be exploited in aquaculture Hydrochloric acid, trisodium citrate, methanol, perchloric acid,
to improve the final product through artificial feed. boric acid, sodium hydroxide were purchased from Merck
From the health point of view, gonads are a rich source of (Mumbai, India); O-phthalaldehyde and sodium hypochlorite from
polyunsaturated fatty acids (PUFA) (Dincer & Cakli, 2007). These Sigma–Aldrich Chemical Co. (Mumbai, India).
have a profound influence on cardiovascular morbidity and mortal- Amino acid composition of the sea urchin gonads was estimated
ity (Siriwardhana, Kalupahana, & Moustaid-Moussa, 2012). They using the procedure adopted by Ishida, Fujita, and Arai (1981).
also have preventive effect on hypertension, inflammation, 150 mg of tissue was added to 10 ml of 6 mol l-2 HCl in a Pyrex
arrhythmias and cancer (Fetterman & Zdanowich, 2009). The main tube. The tube was heat sealed after filling it up with pure nitrogen
PUFA found in gonads are long chain x-3 fatty acids, in particular gas. Hydrolysis of the mixture was carried out in a hot air oven at
eicosapentaenoic acid (EPA, C20:5 (n3)) and docosahexaenoic 110 °C for 24 h. Then, the contents were filtered and flash evapo-
acid (DHA, C22:6 (n3)). The antioxidant activity of the gonads rated to remove traces of HCl. This process was repeated for 2–3
also has bearing on the health through scavenging of reactive times with distilled water. The residue was made up to 10 ml with
oxygen species (ROS, e.g. superoxide and hydroxyl radicals) and 0.05 mol l-1 HCl before being passed through a 0.45 lm membrane
oxidants, such as, singlet oxygen and hydrogen peroxide, gener- filter (Merck Millipore, Bangalore, India), and 20 ll injected on to
ated by endogenous or exogenous factors that are injurious to the HPLC column (Shimadzu-LC10AS). The column (Shim-pack
the cells of the body (Brewer, 2011; Mamelona & Peltetier, 2010). Amino-ISC-07/S 1504Na) was 19 cm long with a 5 cm diameter,
Besides antioxidants from animal origin, plant antioxidants, and packed with a strong acidic cation exchange resin i.e., styrene
including polyphenolic compounds, are also found in sea urchin divinyl copolymer with sulphonic group. The mobile phase consists
gonads, consumption of which is associated with anti- of two buffers; buffer A (trisodium citrate 32.7 g, methanol 140 ml,
inflammatory, anti-atherosclerotic and anti-carcinogenic activities perchloric acid 16.6 ml, pH3.2) and buffer B (trisodium citrate
(Mamelona & Peltetier, 2010; Soobrattee et al., 2005). 117.6 g, boric acid 24.8 g, 4 mol l-1 NaOH 45 ml, pH10). The oven
Antioxidants are typically used in the food industry for prevent- temperature was maintained at 60 °C. Amino acids were eluted
ing rancidity of foodstuffs. The commonly used synthetic antioxi- from the column using stepwise elution, i.e., acidic amino acid first
dants such as butylated hydroxyl anisole (BHA) and butylated followed by neutral and basic amino acids. Amino acid analysis
hydroxyl toluene (BHT), though potent, have been found to be used the non-switching flow method where sodium hypochlorite
toxic and carcinogenic (Li et al., 2007). Marine organisms offer a is added continuously as an oxidizing agent during elution to con-
safe and effective alternative to these. Accordingly, screening for vert secondary amines to primary amines. Post-column derivatisa-
antioxidant activity from marine organisms has increased (Ashraf tion was achieved with O-phthalaldehyde, and the fluorescence
Jazayeri, 2012). (excitation 350 nm and fluorescence 450 nm) end products
In the present study Stomopneustes variolaris, an abundant sea detected. An amino acid standard (Sigma–Aldrich, MO, USA) was
urchin species on the Visakhapatnam coast was screened for bio- also run from which amino acid concentrations were determined.
chemical profile and antioxidant activity. The results will enhance Data are expressed as mean percentage of total amino acids
not only our understanding of the nutritional aspects of S. variolaris obtained from triplicate determinations.
but also provides essential data for further scientific research.
2.4. Fatty acid analysis

2. Material and methods 2.4.1. Chemicals used


Sodium hydroxide, methanol, sodium chloride, boron trifluo-
2.1. Sample collection and preparation ride, petroleum ether (Merck, Mumbai, India).
Fatty acid analysis was performed using the method of
Sea urchins (n = 30) with a diameter greater than 65 mm were Metcalfe, Schimitz, and Peika (1966). Samples (0.2 g) were trans-
collected with the help of SCUBA divers from the intertidal region methylated in 6 ml 0.5 mol l-1 methanolic NaOH, and refluxed
along Visakhapatnam coast (India, 17°450 N, 83°210 300 E) during their under nitrogen for 10 min. BF3 solution (5 ml) was added and the
maturation period. All the sea urchins collected were transported mixture boiled. Saturated NaCl solution (6 ml) was added and
to the laboratory in sea water. The test diameter was measured phase separation carried with petroleum ether. The upper organic
using vernier callipers to nearest 0.01 mm. Then, the shells layer was evaporated under vacuum. Fatty acids methyl esters
were opened and gonads removed. The gonads were pooled for (FAME) were detected using gas chromatography (Thermoquest
biochemical analysis. Trace GC, Milan, Italy) equipped with a capillary column (Supel
co, Sigma–Aldrich, Germany) (30 m long and 0.54 mm diameter)
and a flame ionization detector. The carrier gas was nitrogen and
2.2. Determination of proximate composition and calculation of the flow rate was 0.8 ml/min. The temperature was programmed
energetic values from 170 °C to 250 °C with an increment of 1 °C/min up to
250 °C. Injector and detector temperatures were set at 260 °C and
The moisture and ash content of the sea urchin gonads were 275 °C, respectively. The FAME were identified by comparison with
determined using standard methods (AOAC, 1998a, 1998b). Crude retention times for authentic standards (Supel co 37 component
protein content was estimated using the Kjeldahl method (AOAC, FAME mix, Sigma–Aldrich, Germany). Individual fatty acids are
1998c). Carbohydrates were determined using the Anthrone– expressed as a percentage of total fatty acids.
sulphuric acid method (Kohler, 1952), and total lipids were
analysed using the method of Bligh and Dyer (1959). Energy was 2.5. Antioxidant activity
calculated from the energy values of all the constituents, and
expressed as kcal/100 g on dry weight basis. The conversion factors 2.5.1. Chemicals used
were 5.65, 9.5 and 3.90 for protein, lipid and carbohydrate, respec- Folin–Ciocalteu’s reagent, gallic acid, 1,1-diphenyl-2-
tively (Mol, Baygar, Varlik, & Tosun, 2008). picrylhydrazyl (DPPH), ascorbic acid was purchased from
A. Archana, K.R. Babu / Food Chemistry 197 (2016) 597–602 599

Sigma–Aldrich (Mumbai, India). All other solvents used were of the present study, the total protein content of S. variolaris gonads
analytical grade. (12.10% ± 0.41) was similar to that of P. lividus (12.03% ± 1.26)
(Dincer & Cakli, 2007), but higher than S. droebacheinsis
2.5.2. Determination of total phenol content (7.4% ± 0.2) (Liyana-Pathirana, Shahidi, & Whittick, 2002a;
Total phenol content of the gonads was measured using the Montero-Torreiro & Garcia-Martinez, 2003) and other echinoid
Folin–Ciocalteu method as described by Singleton and Rossi species reported by Chen et al. (2010). This variation in the protein
(1965). The gonad extract (gonads soaked in methanol, 200 ll) content might explain in part differences in organoleptic proper-
was added to 1 ml of 1:10 diluted Folin–Ciocalteu reagent and ties of the various species (Chen et al., 2010).
incubated at room temperature for 5 min. Saturated sodium car- Lipids were a significant component (Table 1) with values
bonate (800 ll) was added to the mixture and mixed gently. After greater than other sea urchins, such as P. lividus (3.05% ± 0.5)
incubation at room temperature (120 min), the absorbance was (Mol et al., 2008) and S. droebacheinsis (4.7%) (Liyana-Pathirana
measured at 765 nm using a UV–VIS spectrophotometer (Perkin et al., 2002a). These results indicated that lipid is an important
Elmer Lamda, USA). Gallic acid (0–100 lg/ml) was used to create storage nutrient for the development and maturity of sea urchin
calibration curve for determination of equivalent values. Total phe- gonads (Gonzalez-Duran, Castell, Robinson, & Blair, 2008). The car-
nolic content was expressed as gallic acid equivalent GAE/g of the bohydrate content of S. variolaris gonads was very low
sample. All determinations were done in triplicates. (1.63% ± 0.18). Low content of carbohydrates was also reported in
P. lividus (Dincer & Cakli, 2007). The low carbohydrate content
2.5.3. Determination of DPPH radical scavenging activity might be related to the stage of development (Chen et al., 2010).
The DPPH radical scavenging activity assay, as described by Total energy levels of S. variolaris gonad, on dry weight basis
Chan, Lim, and Omar (2007) was adopted with slight modification. (122.04 ± 2.03 kcal/100 g) was higher than that reported in other
0.1 mM of DPPH was prepared in 96% methanol. This solution sea urchin P. lividus (107.81 ± 4.98 kcal/100 g) (Mol et al., 2008).
(1 ml) was added to the extract (3 ml) at different concentrations In sea urchins, biochemical composition varies with season, food
(20–100 lg/ml). The mixture was shaken vigorously and left to availability and quality, temperature, and reproductive cycle
stand in the dark for 30 min. The absorbance of the resulting solu- (Cook, Hughes, Orr, Kelly, & Black, 2007; Dincer & Cakli, 2007).
tion was measured spectrophotometrically at 517 nm. Ascorbic
acid was used as the standard. The percentage scavenging activity 3.2. Amino acid composition
of DPPH was then calculated using the equation: DPPH scavenging
activity = 100  (Ac  As)/Ac where, Ac is the absorbance of the The amino acid composition is shown in Table 2. In general, the
control and As is the absorbance of the sample. Antioxidant activ- amino acid composition is important in two aspects, namely nutri-
ities of the extracts were expressed as IC50, calculated from the tion and flavour (Dincer & Cakli, 2007). Not only are they building
graph plotting scavenging activity against sample concentration. blocks for proteins but also, in the free form, have a major role in
IC50 is the concentration of the sample required to scavenge half taste and sensory aspects of numerous foods (Osako et al., 2006).
the DPPH free radical. All the determinations were performed in Glycine and alanine contribute to sweetness, while valine is bitter,
triplicate. and glutamine contributes to umami (Komata, 1964). In the pre-
sent study, it was observed that tyrosine and glutamic acid were
2.6. Statistical analysis the most abundant amino acids. The amino acid composition of
S. variolaris gonads was similar to that reported earlier for other
All the data are expressed as mean ± standard deviation (SD) urchin species (Dincer & Cakli, 2007; Gracia et al., 2000;
(n = 3) calculated using MS-Excel.

Table 2
3. Results and discussion Amino acid composition of sea urchin S. variolaris gonads.

Amino acids % composition in gonadsa


3.1. Proximate composition and energetic values
Essential amino acids
Histidine 2.3 ± 0.16
The proximate composition and energy values for sea urchin
Isoleucine 3.3 ± 0.16
S. variolaris gonads compared with P. lividus are presented in Leucine 4.0 ± 0.33
Table 1. In the present study, protein was the main constituent; Lysine 5.5 ± 0.08
lipid content was relatively abundant but carbohydrates levels Methionine 0.6 ± 0.20
were low. The moisture content of S. variolaris gonads Phenylalanine 6.9 ± 0.25
Threonine 4.4 ± 0.16
(77.53% ± 0.80) was similar to that observed in other species
Valine 5.1 ± 0.30
(Dincer & Cakli, 2007; Gracia et al., 2000). The ash content Total (EAA)b 32.1
(3.76% ± 0.25) of the gonad was higher than those reported for P.
Nonessential amino acids
lividus (2.25% ± 0.24) (Dincer & Cakli, 2007), indicating a high min- Arginine 9.3 ± 0.08
eral content. Proteins are the main reserves of S. variolaris gonad. In Aspartic acid 11.2 ± 0.40
Serine 5.6 ± 0.16
Glutamic acid 14.4 ± 0.16
Table 1 Proline 0.6 ± 0.16
Biochemical composition and energy values of sea urchins S. variolaris and P. lividus Glycine 2.8 ± 0.33
gonads (dry weight basis). Alanine 4.6 ± 0.41
Cysteine 0.0
Composition of gonads S. variolaris P. lividus Tyrosine 19.7 ± 0.70
Moisture (%) 77.53 ± 0.80 79.65 ± 0.65 Total (NEAA)c 67.2
Proteins (%) 12.10 ± 0.41 12.03 ± 1.26 EAA/NEAA 0.5
Lipids (%) 4.98 ± 0.30 3.05 ± 0.5 a
Data is expressed as mean % of total amino acids obtained from triplicate
Ash (%) 3.76 ± 0.25 2.25 ± 0.24
determinations.
Carbohydrates (%) 1.63 ± 0.18 3.02 ± 0.12 b
EAA, essential amino acids
Energy (kcal/100 g) 122.04 ± 2.03 107.81 ± 4.98 c
NEAA, nonessential amino acids.
600 A. Archana, K.R. Babu / Food Chemistry 197 (2016) 597–602

Mamelona & Peltetier, 2010; Mol et al., 2008). As with other nutri- (n9) and C16:1 (n7) were also found in S. variolaris gonads.
ents, amino acid composition varies with diet and gonadal lifestage Among PUFA, C20:5 (n3), eicosapentaenoic acid (EPA) and
(Liyana-Pathirana et al., 2002a). The percentage of essential amino C20:4 (n6), arachidonic acids were present in higher proportion;
acids in S. variolaris was 32.1%, which is similar to Strongylocentro- similar results were observed elsewhere (Arafa, Chouaibi, Sadok, &
tus nudus (Weiding, Ping, Limei, Zunchun, & Jiabo, 2009). The El Abed, 2012; Liyana-Pathirana et al., 2002b; Mol et al., 2008).
essential (EAA) to non essential amino acid (NEAA) ratio was 0.5 Omega-3, PUFA such as C20:5 (n3), eicosapentaenoic acid (EPA)
in this study, which is comparable with P. lividus (0.58 ± 0.01) and C22:6 (n3), docosahexaenoic acid (DHA), are important in
(Mol et al., 2008). Usually in marine foods, EAA:NEAA greater than human nutrition and results showed they were found in consider-
0.5 indicate a useful source of dietary proteins (Mamelona & able quantities in S. variolaris gonads. Similar observation was
Peltetier, 2010). made by Liyana-Pathirana et al. (2002b) in S. droebacheinsis. It
has also been reported that a high proportion of EPA reflects the
presence of algal material in the diet of sea urchin (Arafa et al.,
3.3. Fatty acid composition 2012). Indeed, algae may be the main sources of fatty acids
(Cook, Bell, Black, & Kelly, 2000). As with the other nutrients, qual-
The fatty acid composition S. variolaris gonads is shown in the ity of the diet, temperature variations and reproductive stage also
Table 3. Fatty acid composition is important as it influences flavour affect the fatty acid composition (Arafa et al., 2012). The ratio of
and storage characteristics. Saturated fatty acids (SFA) were the omega-6 fatty acids to omega-3 fatty acids is significant nutrition-
most dominant group (61.13% ± 1.0) compared with monounsatu- ally; in the present study, the ratio was 0.94. Excess intake of x-6
rated fatty acids (MUFA) (16.91% ± 0.8) and polyunsaturated fatty fatty acids in human diet, compared with x-3 fatty acids, leads to
acid (PUFA) (22.01% ± 2.2). Among saturated fatty acids, C14:0 formation of eicosanoids, specifically prostaglandins, thrombox-
and C16:0 were dominant. Similar observations were made in anes, hydroxyl fatty acid and lipoxin. These metabolic products
S. droebacheinsis (Liyana-Pathirana, Shahidi, Whittick, & Hooper, contribute to the formation of thrombus and inflammatory disor-
2002b) and in P. lividus (Mol et al., 2008). In 1970, Fujino, ders. Diets rich in x-3 fatty acids protect against cardiovascular
Negishi, and Umatani also reported that these fatty acids were diseases, especially acute complications of coronary heart disease
predominant in the sea urchin A. crassipina, Strongylocentrotus (Simopoulos, 1991).
pulcherrimus, Strongylocentrotus franciscanus, S. intermedius and
Echinus esculentus. Among the MUFA, C20:1 (n9) was predomi-
3.4. Antioxidant activity
nant in S. varolaris (Table 3). Earlier studies reported that C20:1
(n9) was higher than other MUFAs in sea urchin species; the con-
3.4.1. Total phenol content
tent is influenced by de novo synthesis rather than diet (Liyana-
Phenols are a class of low molecular weight secondary metabo-
Pathirana et al., 2002b; Takagi, Eaton, & Ackman, 1980). C18:1
lites. The total phenolic content of a methanolic extract of sea
urchin gonads was obtained on the basis of a standard curve of gal-
Table 3 lic acid (Fig. 1) as 9.9 mg GAE/g. Phenolic compounds are consid-
Fatty acid composition of sea urchin S. variolaris gonads. ered important as bioactive dietary compounds with putative
Fatty acids % composition in gonads* health benefits. They are able to terminate free radicals and chelate
metal ions, which are capable of catalyzing formation of ROS and
C12:0 0.44 ± 0.1
C14:0 25.8 ± 0.2
promoting lipid peroxidation (Mamelona & Peltetier, 2010).
C15:0 1.52 ± 0.0
C16:0 20.7 ± 0.0 3.4.2. DPPH radical scavenging activity
C17:0 0.65 ± 0.1
C18:0 5.68 ± 0.0
In this study, the antioxidant capacity of a methanolic extract of
C20:0 5.86 ± 0.2 S. variolaris gonads was evaluated using the DPPH radical scaveng-
C22:0 0.21 ± 0.1 ing assay. DPPH radical scavenging activity assesses the capacity of
C23:0 0.27 ± 0.3 an extract to donate hydrogen or scavenge free radicals, such as
R SFAa 61.13 ± 1.0
superoxide and hydroxyl radicals. When the DPPH radical is scav-
C14:1 0.12 ± 0.0
C16:1 (n7) 1.51 ± 0.0 enged, the reaction mixture changes from purple to yellow with
C17:1 0.12 ± 0.3 decreasing of absorbance at 517 nm. Figs. 2 and 3 show the per-
C18:1 (n9) 5.07 ± 0.4 centage inhibition activity for the methanolic extract and ascorbic
C20:1 (n9) 9.29 ± 0.1 acid, respectively, at various concentrations ranging from 20 lg/ml
C22:1 (n9) 0.66 ± 0.0
to 100 lg/ml. The DPPH radical scavenging activities of the extract
C24:1 0.14 ± 0.0
R MUFAb 16.91 ± 0.8 increased gradually in a dose dependent manner. At a concentra-
C18:3 (n3) 0.92 ± 0.0 tion of 100 lg/ml, the methanolic extract and ascorbic acid
C20:3 (n3) 0.37 ± 0.1
C20:5 (n3) 8.67 ± 0.1
C22:6 (n3) 1.06 ± 0.2
R x3 11.02 ± 0.4
C18:2 (n6) 1.92 ± 0.3
C18:3 (n6) 0.48 ± 0.4
C20:3 (n6) 0.29 ± 0.0
C20:4 (n6) 7.64 ± 0.1
R x6 10.33 ± 0.8
C22:1 (n9) 0.66 ± 0.0
R PUFAc 22.01 ± 2.2
x6:x3 0.94
*
Data is expressed as mean % of total fatty acids obtained from triplicate
determination.
a
SFA saturated fatty acids.
b
MUFA mono unsaturated fatty acids.
c
PUFA poly unsaturated fatty acids. Fig. 1. Calibration curve for gallic acid.
A. Archana, K.R. Babu / Food Chemistry 197 (2016) 597–602 601

References

AOAC (1998a). Official method 980.46. Moisture in meat. Meat and meat products.
Chapter 39. Soderberg, D. L. Chapter ed. In Patrica Cunniff (Ed.), Official methods
of analysis of AOAC international, 16th ed, 4th Rev. Vol. II., Gaithersbury,
Maryland, USA..
AOAC (1998b) Official method 938.08. Ash of seafood, fish and other marine
products. Chapter 35 Chapter ed. Hungerford, J.M. In Patrica Cunniff (Ed.),
Official methods of analysis of AOAC International, Sixteenth Edt. 4th Rev. Vol II.,
Gaithersbury, Maryland, USA.
AOAC (1998c). Official method 928.08. Nitrogen in meat. Kjeldahl method. Meat
and meat products. Chapter 39. Soderberg, D. L. Chapter ed. In P. Cunniff (Ed.),
Official methods of analysis of AOAC international, 16th ed, 4th Rev. Vol. II.,
Gaithersbury, Maryland, USA.
Ashraf Jazayeri (2012). The importance of antioxidants with the marine origin in
Fig. 2. DPPH radical scavenging activity of methanolic extract of gonads of inhibit free radicals. Life Science Journal, 9(2), 1128–1132.
S. variolaris. Bligh, E. G., & Dyer, W. J. (1959). A rapid method for total lipid extraction and
purification. Canadian Journal of Biochemistry and Physiology, 37, 911–917.
Brewer, M. S. (2011). Natural antioxidants, sources, compounds, mechanism of
action and potential application. Comprehensive Review in Food Science and Food
Safety, 10(4), 221–247.
Chan, E. W. C., Lim, Y. Y., & Omar, M. (2007). Antioxidant and antibacterial activity of
leaves of Etlingera species (Zingiberaceae) in Peninsular Malaysia. Food
Chemistry, 104(4), 1586–1593.
Chen, G. Q., Xiang, W. Z., Lau, C. C., et al. (2010). A comparative analysis of lipid and
carotenoid composition of the Gonads of Anthocidaris crassispina, Diadema
setosum and Salmacis sphaeroides. Food Chemistry, 120(4), 973–977.
Cook, E. J., Bell, M. V., Black, K. D., & Kelly, M. S. (2000). Fatty acid composition of
gonadal materials and diets of the sea urchin Psammechinus miliaris: Trophic
and nutritional implications. Journal of Experimental Marine Biology and Ecology,
255, 261–274.
Cook, E. J., Hughes, A. D., Orr, H., Kelly, M. S., & Black, K. D. (2007). Influence of
dietary protein on essential fatty acids in the gonadal tissue of the sea urchins
Psammechinus miliaris and Paracentrotus lividus (Echinodermata). Aquaculture,
273(4), 586–594.
Fig. 3. DPPH radical scavenging activity of ascorbic acid.
Dincer, T., & Cakli, S. (2007). Chemical composition and biometrical measurements
of the Turkish Sea urchin (Paracentrotus lividus, Lamarck, 1816). Critical Reviews
in Food Science and Nutrition, 47(1), 21–26.
generates 89.57% and 79.64% inhibition, respectively, with IC50 val- Fetterman, J. W., Jr., & Zdanowich, M. M. (2009). Therapeutic potential of n3
ues 57.81 lg/ml and 33.64 lg/ml, respectively (Figs. 2 and 3). The polyunsaturated fatty acids in disease. American Journal of Health System
Pharmacy, 66(13), 1169–1179.
lower the IC50 value, the greater the antioxidant value of the Fujino, Y., Negishi, T., & Umatani, K. (1970). Studies on lipids in the sea urchin egg.
extract. Part I. On the chemical changes of lipids during curing with salt. Nippon
In addition to fish and crustaceans, sea urchins are a good Shokuhin Kogyo Gakkaishi, 17, 343–349.
Gonzalez-Duran, E., Castell, J. D., Robinson, S. M. C., & Blair, T. J. (2008). Effects of
sources of antioxidants (Ashraf Jazayeri, 2012). The antioxidant dietary lipids on the fatty acid composition and lipid metabolism of the green
potential of gonads from S. droebacheinsis (Mamelona & Peltetier, sea urchin Strongylocentrotus droebachiensis. Aquaculture, 276, 120–129.
2010) and S. nudus (Zhou et al., 2012) have been reported Gracia, C., Lopez-Hernandez, J., Gonzalez-Castro, M. J., Rodriguez De Quiros, A., &
Simal-Loranzo, M. J. (2000). Protein, amino acid and fatty acid content in raw
previously. The gonads contain carotenoids and polyhydroxy and canned sea urchin (Paracentrotus lividus) harvested in Glacia (NW Spain).
napthoquinone pigment, echinochrome-A, which possess potent Journal of the Science of Food and Agriculture, 80, 1189–1192.
antioxidant activity (Popov & Krivoshapko, 2013). Hence, the Ishida, Y., Fujita, T., & Arai, K. (1981). New detection and separation method for
amino acid by high performance liquid chromatography. Journal of
gonads of S. variolaris are new potential resources for natural Chromatography, 204, 143–148.
antioxidants. Kohler, L. H. (1952). Differentiation of carbohydrates by Anthrone reaction rate and
colour intensity. Analytical Chemistry, 24, 157–1579.
Komata, Y. (1964). Study on the extractives of ‘‘uni” IV. Taste of each component in
4. Conclusion the extractives. Nippon Suisan Gakkaishi, 30, 749–756.
Lawrence, J. M. (2001). Edible sea urchins: Biology and ecology. Boston, USA: Elsevier.
The gonads of S. variolaris have high protein and lipid contents. Li, H. B., Cheng, K. W., Wong, C. C., Fan, K. W., Chen, F., & Jiang, Y. (2007). Evaluation
of antioxidant capacity and total phenolic content of different fractions of
They are also a good source of PUFA and essential amino acids. The selected microalgae. Food Chemistry, 102, 771–776.
biochemical profile is comparable with other commercially edible Liyana-Pathirana, C., Shahidi, F., & Whittick, A. (2002a). Comparison of nutrient
species of sea urchins exploited in various parts of the world. composition of gonads and coelomic fluid of green sea urchin Strongylocentrotus
droebachiensis. Journal of Shellfish Research, 21, 861–870.
Besides their nutritional value, these sea urchin gonads possess Liyana-Pathirana, C. F., Shahidi, F., Whittick, A., & Hooper, R. (2002b). Lipid and lipid
potent antioxidant activity. Thus, they may be an alternative soluble components of gonads of sea urchin S. droebachiensis. Journal of Food
source for natural antioxidants in the international market if fur- Lipids, 9, 105–126.
Mamelona, J., & Peltetier, E. (2010). Producing high antioxidant activity from
ther development strategies are employed to improve quality.
Echinoderm by products by using Pressured Liquid Extraction. Biotechnology, 9,
523–528.
Acknowledgements Metcalfe, L. D., Schimitz, A. A., & Peika (1966). Rapid preparation of fatty acid esters
from lipids for gas chromatographic analysis. Analytical Chemistry, 38(3),
514–515.
The corresponding author acknowledges the Department of Mol, S., Baygar, T., Varlik, C., & Tosun, S. Y. (2008). Seasonal variations in yield, fatty
Science and Technology, Government of India for providing the acids, amino acids and proximate composition of sea urchin Paracentrotus
financial support to carry out the research work. The authors thank lividus roe. Journal of Food and Drug Analysis, 16(2), 68–74.
Montero-Torreiro, M. F., & Garcia-Martinez, P. (2003). Seasonal changes in the
the Head, Department of Marine Living Resources, Andhra biochemical composition of body components of the sea urchin, Paracentrotus
University for providing the necessary facilities. They also heartily livid, in Lorbe (Galicia, north-western Spain). Journal of the Marine Biological
thank all the reviewers for their valuable suggestions on the paper. Association of the United Kingdom, 83(3), 575–581.
Osako, K., Kiriyama, T., Ruttanapornvareesakul, Y., Kuwahara, K., Okamoto, A., &
The authors declare that there is no conflict of interests regard- Nagano, N. (2006). Free amino acid composition of the gonad of the wild and
ing the publication of this paper. cultured sea urchins Anthocidaris crassispina. Aquaculture Science, 54, 301–304.
602 A. Archana, K.R. Babu / Food Chemistry 197 (2016) 597–602

Popov, A. M., & Krivoshapko, O. N. (2013). Protective effects of polar lipids and Soobrattee, M. A. et al. (2005). Phenolics as potential antioxidant therapeutic
redox-active compounds from marine organisms at modelling of agents: Mechanism and actions. Mutation Research, 57(1–2), 200–213.
hyperlipidemia and diabetes. Journal of Biomedical Science and Engineering, 6, Soumaya Arafa Moncef Chouaibi Saloua Sadok & Amor El Abed (2012). The
543–550. influence of season on the gonad index and biochemical composition of the sea
Shpigel, M., Mc Bride, S. C., Marciano, S., Ron, S., & Ben-Amotz, A. (2005). Improving urchin Paracentrotus lividus from the golf of Tunis. The Scientific World Journal,
gonad colour and somatic index in the European sea urchin Paracentrotus 1–8. Article id. 815935.
lividus. Aquaculture, 245(1–4), 101–109. Takagi, T., Eaton, C. A., & Ackman, R. G. (1980). Distribution of any acids in lipids of
Siikavuopio, S. I., Dale, T., & Carlehog, M. (2007). Sensory quality of gonads from the the common Atlantic sea urchin Strongylocentrotus droebachiensis. Canadian
green sea urchin Strongylocentrotus droebachiensis fed different diets. Journal of Journal of Fisheries and Aquatic Sciences, 37, 195–202.
Shellfish Research, 26(2), 637–643. Weiding, Xu, Ping, He, Limei, Wang, Zunchun, Zhou, & Jiabo, Han (2009). The amino
Simopoulos, A. P. (1991). Evolutionary aspects of the dietary omega 6:omega3 fatty acid compositions of gonads in sea urchin Strongylocentrotus nudus. Journal of
acid ratio: medical implications. In A. P. Simopolous, F. De Meester (Eds.), A Dalian Fisheries University, 6, 583–586.
balanced omega-6/omega3 fatty acid ratio, cholesterol and coronary heart disease, Zhou, D., Qin, L., Zhu, B., Li, D., Yang, J., Dong, X., & Murata, Y. (2012). Optimisation
World Review of Nutrition and Dietetics, pp. 1–22. of hydrolysis of purple sea urchin (Strongylocentrotus nudus) gonad by
Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with response surface methodology and evaluation of in vitro antioxidant activity
phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology of the hydrolysate. Journal of the Science of Food and Agriculture, 92(8),
and Viticulture, 16, 144–153. 1694–1701.
Siriwardhana, N., Kalupahana, N. S., & Moustaid-Moussa, N. (2012). Advances in Food
and Nutrition Research, 65, 211–222.

You might also like