ARTICLE IN PRESS

LWT 41 (2008) 1067–1072

www.elsevier.com/locate/lwt

Antioxidant activity of three edible seaweeds from

two areas in South East Asia
Y.L. Chewa, Y.Y. Lima,!, M. Omara, K.S. Khoob
a
School of Arts and Sciences, Monash University Malaysia, Bandar Sunway, 46150 Petaling Jaya, Selangor, Malaysia
b
Department of Biosciences and Chemistry, Faculty of Engineering and Science, Tunku Abdul Rahman University, Jalan Genting Kelang,
53300, Setapak, Kuala Lumpur, Malaysia
Received 21 November 2006; received in revised form 7 June 2007; accepted 21 June 2007

Abstract

Total phenolic content (TPC) and antioxidant activity (AOA) of 50% aqueous methanol extracts of the marine algae, Padina
antillarum, Caulerpa racemosa and Kappaphycus alvarezzi were studied. TPC was measured using Folin–Ciocalteu method while 1, 1-
diphenyl-2-picrylhydrazyl (DPPH) radical scavenging, ferric reducing antioxidant power (FRAP), ferrous ion chelating (FIC) assay and
beta carotene bleaching (BCB) assay were used to study their AOA. P. antillarum was found to have the highest TPC, 24307208 mg
gallic acid equivalents (GAE) per 100 g dried sample and ascorbic acid equivalent antioxidant capacity (AEAC), 1140785 mg AA/100 g.
C. racemosa and K. alvarezzi displayed lower TPC and AEAC. C. racemosa had 144722 mg GAE/100 g dried sample of TPC and
14.372.0 mg AA/100 g of AEAC, while K. alvarezzi had 115735 mg/100 g dried sample of TPC and 37.8716.8 mg AA/100 g of AEAC.
In addition, P. antillarum displayed the highest reducing power, 15.772.6 mg GAE/g and highest chelating ability. C. racemosa and K.
alvarezzi exhibited lower reducing power, 0.73770.423 mg GAE/g and 0.56170.269 mg GAE/g, and lower chelating ability. However,
the AOA of these three seaweeds as assessed by BCB assay were equally high.
r 2007 Swiss Society of Food Science and Technology. Published by Elsevier Ltd. All rights reserved.

Keywords: Padina antillarum; Caulerpa racemosa; Kappaphycus alvarezzi; Brown seaweeds; Green seaweeds; Red seaweeds; Antioxidants; Antioxidative
activity

1. Introduction Stadtman, 1992; Wiseman & Halliwell, 1996). The negative

Reactive oxygen species (ROS) is generated in living
organisms during metabolism (Aruoma & Cuppette, 1997;
Cavas & Yurdakoc, 2005). It is produced in the forms of
superoxide anion (O! d
2 ), hydroxyl radical ( OH), hydrogen
peroxide (H2O2) and nitric oxide (NO). Excessive amounts
of ROS may be harmful because they can initiate
biomolecular oxidations which lead to cell injury and
death, and create oxidative stress which results in
numerous diseases and disorders such as cancer, stroke,
mycocardial infarction, diabetes, septic and haemorrhagic
shock, Alzhemer’s and Parkinsons diseases. In addition,
oxidative stress may cause inadvertent enzyme activation
and oxidative damage to cellular systems (Ames, 1983;
!Corresponding author. Tel.: +60 3 55146103; fax: +60 3 55146099.
E-mail address: Lim.Yau.Yan@artsci.monash.edu.my (Y.Y. Lim).
effects of oxidative stress may be mitigated by antioxidants
(Larson, 1995; Pryor, 1991).
Marine algae extracts have been demonstrated to have
strong antioxidant properties (Kuda, Tsunekawaa, Goto,
& Araki, 2005; Yuan & Walsh, 2006), protective effects
against liver injury caused by carbon tetrachloride (Wong,
Ooi, & Ang, 2000), antiproliferative activity towards HeLa
cells (Yuan et al., 2006), antimicrobial activity (Valdebe-
nito, Bittner, Sammes, Silva, & Watson, 1982) and antiviral
properties (Chatterji, Dhargalkar, Sreekumar, Parames-
waran, Rodrigues, & Kotnala, 2004).
Padina antillarum (previously known as Padina tetra-
stromatica) is a brown algae which proliferates in tropical
waters. It is used as seasoning in dried flake form and as
table salt replacement for high blood pressure patients
(Novaczek & Athy, 2001). There are studies which showed
that it contains alginic acid, a major polysaccharide which

0023-6438/$34.00 r 2007 Swiss Society of Food Science and Technology. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.lwt.2007.06.013
 ARTICLE IN PRESS
1068 Y.L. Chew et al. / LWT 41 (2008) 1067–1072
shows high anticoagulant (Prasada Rao, Sastrey, & Venkata
Rao, 1984) and antiviral properties (Chatterji et al., 2004).
Caulerpa racemosa is a green algae which mainly grows
in tropical regions, although some varieties may be found
in subtropical regions (Prud’homme van Reine & Trono,
2001). In South East Asian countries, it is usually served
raw as salad or eaten cooked. In addition, it is used as
animal feed and in folk medicine to reduce blood pressure
and to treat rheumatism (Novaczek, 2001; Prud’homme
van Reine & Trono, 2001).
Kappaphycus alvarezzi, formerly termed as Eucheuma
cottonii (Rönnbäck, Bryceson, & Kautsky, 2002; Bryceson,
2002), is a red algae which is cultivated in many tropical
countries. It is a popular species for aquaculture, being
farmed at places with strong wave action such as on the
reef edge (Prud’homme van Reine & Trono, 2001). Its main
product of commercial importance is carrageenan.
As these three species of seaweeds are used by humans as
food and in view of the potential benefits listed above, it is
therefore of great interest to study and determine the total
phenolic content (TPC) and antioxidant activities (AOA)
of these three seaweeds.
2. Materials and methods
2.1. Samples
P. antillarum and C. racemosa were collected from a coral
reef in Teluk Kumang, Port Dickson, Malaysia, in the period
October–December, 2005 and January–April, 2006 respec-
tively. K. alvarezzi was obtained from the sea off Kampot,
Cambodia, where it was cultured during the period
October–December, 2005. They were put on ice upon
delivery to the laboratory. The samples were rinsed with
distilled water to remove salt and debris and then freeze-
dried. The samples were stored at !20 1C until further use.
2.2. Chemicals and reagents
Sodium carbonate, potassium dihydrogen phosphate and
iron (III) chloride-6-hydrate were purchased from Fisher
Chemicals, while trichloroacetic acid, methanol and iron (II)
sulfate-7-hydrate from HmbG Chemicals. 1, 1-diphenyl-2-
picrylhydrazyl (DPPH) and b-carotene were purchased from
Sigma Aldrich; quercetin and ferrozine iron reagent were
purchased from ACROS Organics. Folin-Ciocalteu’s phenol
reagent and Tween 40 were purchased from Fluka
Biochemika, di-potassium hydrogen phosphate trihydrate
from Merck, potassium ferricyanide from APS Ajax
Finechem and linoleic acid from Calbiochem.
2.3. Preparation of sample extract
One gram of freeze-dried sample was crushed in liquid
nitrogen and extracted using 50 ml of 50% v/v methanol. It
was shaken continuously on an orbital shaker for 1 h. The
extract was then filtered with filter paper and was stored at
!20 1C for further analysis.
2.4. Total phenolic content (TPC)
The TPC of the extracts in 50% methanol was measured
using Folin Ciocalteu method as described by Kahkonen
et al. (1999). Folin Ciocalteu’s phenol reagent (1.5 ml)
and 7.5% w/v Na2CO3 (1.2 ml) were added to sample
extract (0.3 ml) and the reaction mixture was incubated in
the dark for 30 min. The absorbance of the reaction
mixture was then measured at 765 nm. TPC was expressed
in terms of mg gallic acid equivalents (GAE)/100 g dried
samples. The calibration equation for gallic acid was y ¼
0:0111x20:0148 (R2 ¼ 0:9998).
2.5. Antioxidant activities (AOA)
2.5.1. 1, 1-diphenyl-2-picrylhydrazyl (DPPH) radical
scavenging
The DPPH free-radical scavenging assay was carried out
in triplicate, based on the method used by Leong and Shui
(2002) and Miliauskas, Venskutonis, and Van Beek, (2004).
Two milliliters of 0.15 mM DPPH were added to the
different dilutions of the extract (amounting to 1 ml) and
the reaction mixture was incubated for 30 min after which
its absorbance was measured at 517 nm. DPPH was
expressed in terms of ascorbic acid equivalent antioxidant
capacity (AEAC) which was calculated based on its
concentration of extract required to reduce DPPH radicals
by 50% (IC50), as follows:
AEAC ðmg AA=100 gÞ ¼ IC50 ðascorbateÞ=IC50 ðsampleÞ % 100; 000
IC50(ascorbate) was (3.8270.04) % 10!3 mg/ml.
2.5.2. Ferric- reducing antioxidant power (FRAP)
The FRAP assay was determined, following the method
of Chu, Chang, and Hsu (2000) with modifications. A
0.1 M potassium phosphate buffer (pH 6.6) (2.5 ml) and
1% w/v potassium ferricyanide (2.5 ml) were mixed with
1 ml of extracts of varying dilutions. The reaction mixture
was incubated at 50 1C for 20 min, after which 10% w/v
trichloroacetic acid (2.5 ml) was added. 2.5 ml of water and
0.5 ml of 0.1% w/v FeCl3 were then added to 2.5 ml of the
reaction mixture. The solution was incubated at ambient
temperature for 30 min for colour development. The
absorbance was then measured at 700 nm. The FRAP
value was expressed in mg GAE/g.
2.5.3. Ferrous ion chelating (FIC) assay
The FIC assay was based on Singh and Rajini (2004).
Equal volumes of 0.1 mM FeSO4, extracts of various
dilutions (concentration range of 1.0–7.0 mg/ml) and
0.25 mM ferrozine were mixed. The reaction mixtures (in
triplicates) were incubated for 10 min and the absorbance
was measured at 562 nm. The result was expressed in
percentage of chelating ability (% chelating ability), using
 ARTICLE IN PRESS
Y.L. Chew et al. / LWT 41 (2008) 1067–1072 1069

the following equation: Antioxidant activity ð%AOAÞ

Chelating ability ð%Þ ¼ ½ðAcontrol ! Asample Þ=Acontrol ' % 100: ¼ ½ðDRcontrol ! DRsample Þ=DRcontrol ' % 100:

3. Results and discussion

2.5.4. Beta carotene bleaching (BCB) assay
BCB assay reported by Kumazawa et al. (2002) was
adapted. Quercetin was used as a positive control.
Three milliliters of b-carotene (5 mg/50 ml chloroform)
was added to 40 mg of linoleic acid and 400 mg of Tween
40. The chloroform in mixture was evaporated and 100 ml
of oxygenated ultra-pure water was added into the dried
mixture. The b-carotene/linoleic acid emulsion was then
mixed well, and the initial absorbance of the emulsion was
measured at 470 and 700 nm. Three milliliters aliquots of
the emulsion were added to 10–100 ml of the extracts, which
were incubated at 50 1C and the reaction mixtures were
measured again at 470 and 700 nm at the end of 60 min.
The absorbance at 700 nm (due to haze) was subtracted
from the absorbance at 470 nm.
AOA was expressed in percentage of AOA, calculated as
follows:
Degradation rate ðDRÞ of b!carotene
¼ ln ðAinitial =Asample Þ=60:
Table 1
Extraction efficiencies of various dilutions of methanol in water on P.
antillarum, C. racemosa and K. alvarezzi samples
Species TPC (mg GAE/100 g dried samples)a
100% methanol 50% methanol
P. antillarum 1240798 24307208
C. racemosa 96.574.7 144722
K. alvarezzi 28.471.1 115735
a
Results are means7SD (n ¼ 3).
3.1. Selection of extraction solvents
In order to select the best solvent for extraction of the
three species of seaweeds, three different percentages of
methanol (20%, 50% and 100% v/v) were used for
extraction. 50% methanol was found to give the highest
extraction efficiency for all the three species, as was
indicated by the TPC (Table 1), while 100% methanol
had the lowest extraction efficiency. 50% methanol was
thus used for subsequent AOA assays. The average
extraction efficiency of 50% methanol was determined by
multiple extraction experiment and was found to range
from 78% to 89% in the first extraction depending on the
type of seaweeds (Table 2).
3.2. Total phenolic content (TPC)
Using the Folin Ciocalteu method, P. antillarum was
found to have the highest TPC while K. alvarezzi had the
lowest. The polyphenols of seaweeds such as phlorotannins
(Burtin, 2003), which are bi-polar in nature, and mostly
found in brown seaweeds (Targett & Arnold, 1998), such as
in P. antillarum, function as antioxidative components due
to the presence of multiple phenolic groups. These phenolic
compounds could assist the algae to overcome oxidative
stress as well as play a putative adaptive role in defense
against grazers, such as marine herbivores (Altena &
20% methanol Steinberg, 1992) due to their plasticity characteristics. The
presence of antioxidative phlorotanins in P. antillarum
20407148 could cause it to have higher TPC compared to the other
11473
10274
two species.
On the other hand, both K. alvarezzi and C. racemosa
had fairly low TPC (Table 3). According to Fayaz et al.

Table 2
Extraction efficiencies of P. antillarum, C. racemosa and K. alvarezzi

Species Extraction Average TPC (mg GAE/ Average extraction

100 g dried sample) efficiencies (%)

P. antillarum 1st 2201733 85.771.8

2nd 262735 10.171.2
3rd 113718 4.2270.61

C. racemosa 1st 12578 77.571.3

2nd 31.572.3 17.571.0
3rd 12.370.5 5.0970.60
K. alvarezzi 1st 10671 88.871.7
2nd 16.171.3 10.271.1
3rd 5.5070.76 0.9670.69

Note: The average of TPC and extraction efficiencies are based on triplicates from a single batch. Results are expressed as means7SD (n ¼ 3).
 ARTICLE IN PRESS
1070 Y.L. Chew et al. / LWT 41 (2008) 1067–1072
Table 3
TPC and AOA values of P. antillarum, C. racemosa and K. alvarezzi samples extracted with 50% methanol
Species TPC (mg GAE/100 g Antioxidant activity (AOA)
dried samples)
DPPH
IC50(mg/ml)
P. antillarum 24307208 0.33770.025
C .racemosa 144722 14.372.0
K. alvarezzi 115735 11.875.7
Results are expressed as means7SD (n ¼ 3).
(2005), K. alvarezzi contains ascorbic acid and polyphenols,
which are hydrophilic. Novaczek (2001) reported that
C. racemosa is rich in folic acid, ascorbic acid, vitamin A,
and B1 (thiamine).
3.3. Antioxidant activity (AOA)
3.3.1. 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical
scavenging
DPPH is a compound that possesses a nitrogen free
radical and is readily destroyed by a free radical scavenger.
This assay was used to test the ability of the antioxidative
compounds functioning as proton radical scavengers or
hydrogen donors (Singh & Rajini, 2004).
A correlation was found between the TPC and IC50.
When the TPC level was high, the IC50 was low and results
in high level of AEAC. This is due to the high amount of
polyphenolic constituents present in the seaweed, which
were capable of functioning as free radical scavengers.
However, this assay was not specific to any particular
antioxidants. The TPC of P. antillarum was highest among
the three seaweeds, and it had lowest IC50 and highest
AEAC. Both C. racemosa and K. alvarezzi had approxi-
mately the same TPC. The radical scavenging activity of
C. racemosa could be due to the presence of folic acid,
thiamine and ascorbic acid (Novaczek, 2001).
3.3.2. Ferric reducing antioxidant power (FRAP)
In FRAP, the AOA was determined based on the ability
of the antioxidant components in the samples to reduce
ferric (III) to ferrous (II) in a redox-linked colourimetric
reaction (Li et al., 2006) that involves single electron
transfer.
Table 2 shows that P. antillarum had the highest ability
for reducing Fe3+. The reducing ability of C. racemosa and
K. alvarezzi was considerably lower as was the TPC.
3.3.3. Ferrous ion chelating (FIC) assay
The binding of the antioxidant components to metal ions
was evaluated using the FIC assay. An extract with higher
binding ability would prevent or inhibit reaction such as a
Fenton’s type reaction, which generates reactive hydroxyl
radicals.
FRAP (mg GAE/g)
AEAC(mg AA/100 g)
114078.5 15.772.6
27.673.9 0.73770.423
37.8716.8 0.56170.269
Fig. 1. Ferrous ion chelating ability (FIC) of P. antillarum (1), C.
racemosa (2) and K. alvarezzi (3) samples. Data are expressed as
means7SD (n ¼ 3).
Fig. 1 shows that the chelating ability of all the three
species of seaweeds increased with concentration. Brown
seaweed, P. antillarum had the highest chelating ability.
However, its chelating ability started to level off when the
concentration increased from 1 to 2.3 mg/ml. According to
Toth and Pavia (2000), the phlorotanins which are usually
present in brown seaweeds are strong chelators of heavy
metals, which are believed to be responsible for the
chelating ability of P. antillarum. K. alvarezzi also had
the same trend as P. antillarum, but its chelating ability at
the same concentrations was lower.
3.3.4. Beta carotene bleaching (BCB) assay
In the BCB assay, the oxidation of linoleic acid generates
peroxyl free radicals due to the abstraction of hydrogen
atom from diallylic methylene groups of linoleic acid
(Kumaran & Joel karunakaran, 2006). The free radical
then will oxidize the highly unsaturated b-carotene.
Consequently, the orange coloured chromophore of
b-carotene would be degraded and the result could be
monitored spectrophotometrically. However, the presence
of antioxidant constituents could neutralize the linoleate-
free radical and hence prevent the bleaching of b-carotene.
Most studies showed there was no correlation between
TPC and BCB (Amarowicz, Wanasundara, Wanasundara, &
Shahidi, 1993; Othman, Ismail, Abdul Ghani, & Adenan,
 ARTICLE IN PRESS
Y.L. Chew et al. / LWT 41 (2008) 1067–1072 1071

100
90

Antioxidant Activity (percent)

80
70
60
50
40
30
20
10
0
0.001 0.005 0.01 0.200 1.00 2.00 0.200 1.00 2.00 0.200 1.00 2.00
Quercetin P. antillarum C. racemosa K. alvarezzi
Mass (mg)

Fig. 2. Antioxidant activity of P. antillarum, C. racemosa and K. alvarezzi samples as determined by beta-carotene bleaching (BCB) assay. Data are
expressed as means7SD (n ¼ 3).

70 The TPC and the AOA of P. antillarum, C. racemosa and

K. alvarezzi could be due to both the hydrophilic and
Antioxidant Activity (percent)

60
50
40
30
20
10
0 could cause food spoilage.
0 0.5
Mass (mg)
Fig. 3. Antioxidant activity of three batches of P. antillarum as
determined by BCB assay. Values are the means7SD of three determina-
tions.
2006; Sun & Ho, 2005; Tsuda, Makino, Kato, Osawa, &
Kawakishi, 1993) although a positive correlation has been
reported (Velioglu, Mazza, Gao, & Oomah, 1998). This is
due to the different types of antioxidants that are assayed by
the two methods. TPC gives an indication of the levels of
both lipophilic and hydrophilic compounds. BCB in
contrast, only gives an indication of the levels of lipohilic
compounds. Fig. 2 shows that all three seaweeds have similar
BCB antioxidant activity in spite of very large differences in
TPC. This implies the presence of approximately similar
amounts of lipophilic antioxidants in all three species. For
100 ml of solution, 0.2–2 mg of seaweed extracts gave as high
AOA values as 0.001–0.01 mg of quercetin standard.
It is noted that there is a significant variation in
antioxidant activity between the batches of seaweeds
sampled. An example is shown in Fig. 3 for P. antillarum.
4. Conclusion
Fifty percent methanolic extract showed highest extrac-
tion efficiency. P. antillarum showed significantly higher
TPC, AEAC and FRAP than K. alvarezzi and C. racemosa.
1 1.5
hydrophobic antioxidants. Chelating ability of P. antillar-
um performed better than the two other seaweeds, but the
AOA as measured by BCB assay of the three seaweeds
were comparable.
The high TPC of P. antillarum could be utilized as a
source of antioxidants for the food industry, while the
lipophilic antioxidants in the seaweeds could be employed
as food preservatives, preventing lipid peroxidation which
2
Acknowledgement
This study was supported by Monash University
Malaysia research grant AS-6-05. The authors wish to
thank Mr. Lim Lian Tho of Star Enterprise for supplying
and delivering fresh K. alvarezzi from the aquaculture
facilities in Kampot, Cambodia.
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