DOI 10.

1007/s11094-020-02139-5
Pharmaceutical Chemistry Journal, Vol. 53, No. 12, March, 2020 (Russian Original Vol. 53, No. 12, December, 2019)

THE RELATIONSHIP OF FREE RADICAL SCAVENGING

AND TOTAL PHENOLIC AND FLAVONOID
CONTENTS OF Garcinia lasoar PAM

Healthy Kainama,1 Sri Fatmawati,1 Mardi Santoso,1

Pamella Mercy Papilaya,2 and Taslim Ersam1,*

Original article submitted September 22, 2019.

The radical scavenging assays of 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical and 2,2¢-azino-bis-3-ethyl-

benzothiazoline-6-sulphonic (ABTS) acid for various extracts and fractions of Garcinia lasoar Pam stem bark
had been examined. The methanol extract showed high total phenolic (272.98 mg GAE (gallic acid equiva-
lent)/100 g) and total flavonoid (223.16 mg QE (quercetin equivalent)/100 g) contents with potential antioxi-
dant activity (DPPH: 0.72 mg/mL; ABTS: 0.24 mg/mL). The ethyl acetate fraction of methanol extract has
higher activity than the dichloromethane fraction with IC50 values of 1.90 and 0.90 mg/mL in DPPH and
ABTS assays, respectively. The Pearson correlation coefficients were calculated in order to identify the rela-
tionship between antioxidant activity and the total phenolic and total flavonoid contents. The antioxidant ac-
tivity showed high positive relationship in both assays (r = 0.762, p < 0.05). The highest positive correlation
between total flavonoid content and ABTS radical scavenging activity for methanol extract and then ethyl ace-
tate had correlation between total flavonoid content. These results suggest that G. lasoar stem bark extracts
can be used as a natural source of antioxidants.
Keywords: Indonesian tradisional medicines, Pearson correlation, DPPH, ABTS.

1. INTRODUCTION tive natural compounds, e.g., xanthones, terpenoids, benzop-

henones, flavonoids. and depsidones [5 – 18]. Indonesia was
Oxidative stress is a negative effect caused by free radi- reported to have 77 species of Garcinia family. Some of
cals in the organism, which can cause various diseases such these species are consumable and have been cultivated, such
as arteriosclerosis, diabetes, tumors, heart disease and aging as G. atroviridis, G. dulcis, G. mangostana, G. Nigrolineata,
[1, 2]. However, healthy humans can detoxify or eliminate and G. parviflora, while others grow wild in the forests and
these free radicals by antioxidant enzymes such as super- are only used as logging [19]. Maluku Islands is known to be
oxide dismutase, catalase, and peroxide, and also by food de- rich in herbs, spices, and endemic plants. Maluku is geo-
rived antioxidants [3]. Natural sources of antioxidant such as graphically located in the Wallacea region, which is unique
vegetables, fruits and medicinal plants which are relatively
and has large potential for growing extensive flora, in both
cheaper and have fewer side effects are interesting objects
primary and secondary forests. The genus Garcinia in
for the investigation of new antioxidants such as flavonoids,
Maluku has been reported to include 17 species, four of
stilbenes, xanthones and coumarins [4, 5]. At present, plants
which are endemic [20].
of the Guttiferae family (Clusiaceae) including Garcinia
The plant of G. lasoar, which is locally known as
hombroniana, G. mangostana, G. brasiliensis, G. lateriflora
“manggustan utang”, is growing up in primary forests. The
var. javanica, G. Combogia. G.virgate, G. speciosa, G.
celebica G. ferrea, G. bentami, G. subelliptica, G. cylindro- local people in Maluku, especially on Ambon island, have
carpa are well-nown sources of a variety of biologically ac- used this plant as treatment for tuberculosis, malaria, diabe-
tes and for increasing immunity. To the best of the authors¢
1
Laboratory of Natural Products and Synthetic Chemistry, Department of knowledge, no phytochemical investigations of this plant has
Chemistry, Institut Teknologi Sepuluh Nopember, Surabaya 60111, Indo-
been reported so far. It is also necessary to perform addi-
nesia.
2
Laboratory of Biology Pattimura University, Indonesia. tional research related to the activities of G. lasoar as a folk
*
e-mail: [email protected] medicine.

1151
0091-150X/20/5312-1151 © 2020 Springer Science+Business Media, LLC
1152 Healthy Kainama et al.

In this work, we have examined the antioxidant activity assay was carried out according to the method of Hidayati, et
of G. lasoar stem bark in various extracts by using DPPH and al. [22]. Trolox was used as a positive control.
ABTS assays. The total phenolic content (TPC) and total
2.5. Phytochemical Analysis
flavonoid content (TFC) of the extract were also determined.
This paper provides a basic information on this Garcinia spe- Determination of TPC and TFC. Total phenolic and
cies that can be used as a natural antioxidant. flavonoid contents were determined by Folin-Ciocalteu and
aluminium chloride colometric methods, respectively
2. MATERIALS AND METHODS [23, 24], followed by quantification on the basis of standard
curve in terms of gallic acid (GAE) and quercetin (QE)
2.1. Plant Material equivalent, respectively.
The stem bark of G. lasoar was collected from Hattu For- 2.6. Statistical Analysis
est on Ambon island, Indonesia. This plant was identified
Determination of total phenolic and flavonoid contents
and a voucher specimen (No. 51) was deposited at Biology
and antioxidants activity by ABTS and DPPH assay was
Laboratory of the Biology Departement, Pattimura Univer-
conducted in triplicate. The value for each sample was calcu-
sity, Indonesia.
lated as Mean ± SD. Correlation coefficients were calculated
2.2. Chemicals and Reagents using SPSS v22. Differences at p < 0.05 were concidered to
be significant.
Petroleum ether, n-hexane, dichloromethane, ethyl ace-
tate, methanol, ethanol, sodium carbonate, trolox (6-hydro-
xy-2,5,7,8-tetramethylchromane-2-carboxylic acid), ABTS 3. RESULTS AND DISCUSSION
(2,2¢-azino-bis-3-ethylbenzothiazoline-6-sulphanic acid) di-
3.1. Free Radical Scavenging Activity of G. lasoar Extracts
ammonium salt, DPPH (1,1-diphenyl-2-picrylhydrazyl), and
and Fractions in DPPH and ABTS Assays
DMSO, gallic acid, Folin – Ciocalteau (FC) reagent, and
quercetin, all chemicals used for the analysis were of analyti- In the present study, aqueous infusion and three different
cal grade. solvents were chosen to extract compounds of different po-
larities. Petroleum ether, n-hexane and dichloromethane
2.3. Preparation of Extracts and Fractions
were used to obtain nonpolar fractions. The remaining crude
The stem bark of G. lasoar was dried at room tempera- extract was then treated with ethyl acetate for extracting
ture and reduced to coarse powder using a disk mill SMJMA, semipolar fractions and polar fractions were extracted by us-
FFC-15, Shandong Jimo. Each dried stem bark powder ing methanol and ethanol. The aqueous extract was obtained
(100 g) was mixed separately with 500 mL etanol 70%, ethyl by traditional empirical methods of green chemistry.
acetate, dichloromethane and n-hexane. The solvent was The antioxidant activity of seven extracts of G. lasoar
evaporated under reduced pressure (Rotavapor R-210, Buchi, stem bark and two fractions of methanol extract as tested us-
Switzerland) to obtain a solid mass extract of ethanol (EE; ing ABTS and DPPH assays is shown in Fig. 1. Concentra-
12.8% w/w), ethyl acetate (EAE; 13.3% w/w), dichloro- tions of sample required to scavenge 50% of DPPH and
methane (DE; 3.8% w/w), and n-hexane (n-HE; 2.5 % w/w). ABTS radicals (IC50) are listed in Table 1. In tests at the
Aliquots (20 g) of solid powder were extracted with 250 mL ABTS concentration of 99.0 mg/mL, ME showed the maxi-
petroleum ether (PEE) in soxhlet extractor for 72 h at 55oC. mum inhibition (96.97 ± 1.39%; IC50 3.59 mg/mL) while
The extract was filtered off and evaporated to yield extract
PEE produced the lowest inhibition (20.42 ± 1.20%) with
(4.5% w/w). The aqueous extract (AE; 20.2 % w/w) was ob-
IC50 value of >100 mg/mL. The results for ABTS showed
tained by infusion in hot water, prepared just before use. The
air-dried stem bark of G. lasoar (3.0 kg) was also extracted trolox (IC50 value of 0.88 mg/mL) to exhibit lower activity of
radical scavenging as compared to ME. The ME, AE and EE
with methanol (ME) (3 ´ 7 L) by maceration at room tem-
extracts have higher activity of DPPH radical scavenging
perature for three days. The extract was concentrated in
vacuo to yield 30.0 g of brown crude extract, and then sepa- than trolox.
The ME extract was the strongest inhibitor
rated by vacuum liquid chromatography (VLC) on silica gel
(300 g) with increasing solvent polarity to get n-hexane, di- (98.58 ± 1.49%; IC50 = 0.24 mg/mL), while PEE was the
chloromethane (DF), ethyl acetate (EAF) and methanol frac- weakest one (14.80 ± 1.28%; IC50 100) in DPPH concentra-
tions. EAF (46.66% w/w) and DF (23.33% w/w) fractions tion of 319.45 mg/mL in the radical scavenging activity test.
was further subjected to DPPH and ABTS assays. In the same concentration, fractions from ME, EAF have
higher activity than that of DF with IC50 value of 0.90 and
2.4. DPPH and ABTS Free Radical Scavenging Assay
1.20 mg/mL in DPPH and ABTS assay, respectively.
The DPPH radical scavenging activity was tested by Trolox used as positive control showed higher activities
method of Fitriana, et al. [21]. The ABTS radical scavenging against DPPH (IC50 value of 2.16 mg/mL) than all extracts
The Relationship of Free Radical Scavenging 1153

Fig. 1. Free radical scavenging effect of G. lasoar stem bark extracts, fractions and trolox. Concentration 99.0 mg/mL for ABTS and
319.45 mg/mL for DPPH. Data show Mean ± SD (n = 3) for each experiment performed in triplicate; p < 0.001 as compared to the control.

and fractions. The result for ABTS showed trolox (IC50value (77.54 ± 1.61 mg GAE/100 g) (Fig. 2A). Extracts of
of 4.11 mg/mL) to have lower activity of radical scavenging nonpolar solvents (PEE, n-HE, DE) were not detected.
than ME. Flavonoids are a group of polyphenolic compounds,
which exhibit several biological effects such as anti-inflam-
3.2. Total Phenolic and Flavonoid Content
matory, anti-hepatotoxic, anti-ulcer, anti-allergic, anti-viral
The extraction of bioactive compounds from plant mate- and anti-cancer [33]. They are capable of effectively scav-
rials is the first step toward potential utilization of enging reactive O2 species because of their phenolic
phytochemical extracts, in the preparation of functional food, hydroxyl groups, so they are potent antioxidants [34]. Their
dietary supplements or nutraceuticals, cosmetics and phar- effects on human nutrition and health are also consider-
maceutical products. The extraction yield of phenolics as able.The total flavonoid content in different of G. lasoar stem
well as their antioxidant efficacy not only depend upon plant bark extracts was determined by aluminum chloride method.
part/type, genetic make up of species, agroclimatic condi- This compound forms stable acid complexes with the car-
tions, harverst time, post-harverst processing, and it is bonyl group at C-4 and hydroxyls at C-3 in flavonols and
strongly affected by the chemical nature of extraction media C-5 in both flavonols and flavones. Besides, it form labile
employed [25, 26].
Successful prediction of botanical compounds isolated
from plant material much depends on the type of solvent se-
lected for the extraction [27]. In previous studies, polar and TABLE 1. IC50 of G. lasoar Stem Bark Extracts and Fractions
nonpolar solvents such as methanol, ethanol, acetone, Antioxidant activity
propanol, ethyl acetate and water have been commonly used Sample
DPPH ABTS
for the extraction of phenolic compounds [28 – 30]. The re-
covery of phenolics from plant materials is influenced by the Extract
solubility of these phenolic compounds in the solvent used ME 0.72 0.24
for the extraction process. Importance of solvent variation AE 0.79 0.67
for accumulation of total phenolic and flavonoid contents as
EE 0.84 0.56
antioxidants has been recognized.
EAE 1.20 0.94
The phenolic contents among the different varieties of G.
lasoar stem bark were expressed in quercetin equivalent us- DE >100 >100
ing the standard curve equation y = 0.00384x + 0.101, R2= n-HE >100 >100
0.976. ME gave the highest amount of phenolic compounds PEE >100 >100
(272.98 ± 0.61 mg GAE/100 g extract). This result suggests Fraction
that the nature of these polyphenols is polar [31, 32]. Total EAF 1.05 0.90
phenolic content of EE was higher than that of AE with
DF 1.25 1.20
270.16 ± 1.61 and 212.63 ± 1.05 mg GAE/100 g extract, re-
Trolox (positive control) 0.88 0.47
spectively. The lowest values were obtained in the EA extract
1154 Healthy Kainama et al.

a
Fig. 2. Total phenolic (A) and flavonoid (B) contents of G. lasoar stem bark extracts; gallic acid equivalents//100 g of stem bark extract;
b
quercetin equivalents//100 g of stem bark extract; values represent Mean ± SD of experiments performed in triplicate; level of significance,
p < 0.001.

acid complexes with hydroxyls in the ortho position in A or DPPH scavenging activity (r = 0.756, p < 0.001) was ob-
B rings of flavonoids [35]. The flavonoid contents in differ- served for AE, followed by EE (r = 0.655, p < 0.001). The
ent varieties of G. lasoar stem bark were expressed in gallic EAE extract showed positive correlation between total
acic equivalent using the standard curve equation flavonoid and DPPH scavenging activity (r = 0.024, p .001).
y = 0.009x + 0.0161, R2 = 0.983. The flavonoid content in Negative correlation between total flavonoid content and
solvents of different polarity was as follow: DPPH scavenging activity was given by ME (r = –0.854).
ME > EE > AE > EAE (Fig. 2B). Extracts of the nonpolar The highest and positive correlation between total flavonoid
solvents (PEE, n-HE, DE) were not detected. content and DPPH scavenging activity (r = 0.756, p < 0.001)
was observed for AE, followed by EE (r = 0.655, p < 0.001).
3.3. Relationship between TPC, TFC and Antioxidant
The high and positive correlation between total phenolic
Activity
content and ABTS scavenging activity (r = 0.943, p < 0.001)
The highest and positive correlation between total phe- was observed for DF. Negative correlation between total
nolic content and ABTS scavenging activity (r = 0.977, phenolic content and ABTS scavenging activity was given
p < 0.001) is observed for EE (Table 2). There was moderate by EAF (r = –0.843). The high and positive correlation be-
correlation between total phenolic content and ABTS scav- tween total flavonoid content and ABTS scavenging activity
enging (r = 0.444, p < 0.001) for ME, followed by AE (r = 0.943, p < 0.001) was observed for EAF. Negative corre-
(r = 0.312, p < 0.001). Negative correlation between total lation between total flavonoid and ABTS scavenging activity
phenolic content and ABTS scavenging activity was given was given by DF (r = –0.874). The positive correlation be-
by EAE (r = –0.908). The highest and positive correlation tween total phenolic content and DPPH scavenging activity
between total flavonoid content and ABTS scavenging activ- (r = 0.294, p < 0.001) was observed for EAF. Negative corre-
ity (r = 0.998, p < 0.001) was observed for ME, followed by lation between total phenolic content and DPPH scavenging
AE (r = 0.865, p < 0.001). There was positive correlation be- activity was given by DF (r = –0.843). Negative correlation
tween total flavonoid content and ABTS scavenging between total flavonoid and DPPH scavenging activity was
(r = 0.524, p < 0.001) for EAE. Negative correlation be- given by EAF (r = –0.673) followed by DF (r = –0.368).
tween total flavonoid content and ABTS scavenging activity The ME extract had high positive correlation between to-
was given by EE (r = –0.908). tal flavonoid and ABTS scavenging activities. There was
The highest and positive correlation between total phe- negative corrrelation between total flavonoid content and
nolic content and DPPH scavenging activity (r = 0.862, DPPH scavenging activities for ME. Furthermore, positive
p < 0.001) was observed for EAE. There was positive corre- correlation between total phenolic and both of DPPH and
lation between total phenolic and DPPH scavenging ABTS scavenging activities. These data indicate that higher
(r = 0.023, p < 0.001) for ME. Negative correlation between total flavonoid in ME would give higher ABTS scavenging
total phenolic content and DPPH scavenging activity was activity.
given by EE (r = –0.481) and AE (r = –0.149). The highest The EE extract had high positive correlation of total phe-
and positive correlation between total flavonoid content and nolic content – ABTS and total flavonoid content – DPPH
The Relationship of Free Radical Scavenging 1155

scavenging activities. It can be concluded that ABTS and negative correlations between total flavonoid and ABTS and
DPPH scavenging activities of EE extracts can be predicted DPPH scavenging activities. This shows that total flavonoid
indirectly by using total phenolic and total flavonoid con- content in DF lower contributed to ABTS and DPPH scav-
tents, while the total flavonoid content in AE extract had pos- enging activities. It was predicted that flavonoid in DF has
itive high correlation with both of ABTS and DPPH scav- no –OH in ortho C3¢,4¢; –OH in C3, oxo function in C4, dou-
enging activities. Besides that, AE had positive correlation ble bond at C2 and C3, which would influence the scaveng-
between total phenolic content and ABTS scavenging activ- ing activity.
ity. It was demostrated for both ABTS and DPPH scavenging In general, total phenolic and flavonoid contributed in
activities that AE extract can be assessed indirectly by using antioxidant activity which is function as chain breakers, free
its total phenolic and flavonoid contents. radical scavengers and electron donors. It is assumed that as
The EAE extract had high positive correlation between
concentration of phenolic or the degree of hydroxylation of
total phenolic content and DPPH scavenging activities.
the phenolic compounds increases DPPH, also increase radi-
There was negative correlation between total phenolic con-
cal scavenging activity and antioxidant activity [36]. In this
tent of EEA extract and ABTS scavenging activities. The
research, flavonoid is related with antioxidant activity, but
EAE extract had positive correlation total flavonoid content
the different showed that ME had negative correlation be-
with ABTS and DPPH scavenging activities. It can be con-
tween total flavonoid and DPPH. The present study showed
cluded that DPPH and ABTS scavenging activities of EEA
extract are contributed by its total phenolic and flavonoid ME have high radical scavenging activities. The best results
contents. is supported by previous reports that some of phenolic com-
The EAF fraction had high positive correlation between pounds beside flavonoid like xanthones, benzophenones,
total flavonoid and ABTS scavenging activities. It can be coumarins, stilbenes, and depsidones would give higher anti-
concluded that ABTS scavenging activities of EAF can be oxidant activities [37 – 42]. The other side, this can be ex-
predicted indirectly by using total flavonoid contents. While plained by the fact that not only phenolic compounds but
the total phenolic in DF had positive high correlation with of also some other compounds may also have DPPH free radi-
ABTS and positive moderate correlation between DPPH cal [43]. Previous studies have also indicated some of
scavenging activities. It was demostrated that both of ABTS triterpenoid compounds have antioxidant activity such as
and DPPH scavenging activities of DF can be estimated indi- dysoxyhaine A-D, chilianthin A-C, myriceric B and
rectly by using its total phenolic contents. There were high uncarinic acid E [44, 45].

TABLE 2. Pearson Correlation Coefficients (r) for TPC, TFC of G. lasoar Stem Bark Extracts and Fractions in DPPH and ABTS Radical Scav-
enging.
TPC TFC DPPH AlE ABTS AlE DPPH AlF ABTS AlF
** **
ABTS AE 0.312 0.865
ABTS ME 0.444** 0.998**
ABTS EE 0.977** 0.481**
ABTS EAE –0.908** 0.524**
**
ABTS AlE –0.345 0.459** 0.762*
DPPH AE –0.149** 0.756**
**
DPPH ME 0.023 –0.854**
DPPH EE –0.190** 0,655**
**
DPPH EAE 0.862 0.024**
DPPHAlE 0.347** 0.490** 0.762*
** **
ABTS EAF –0.843 0.874
**
ABTS DF 0.943 –0.874**
**
ABTS AlF –0.053 –0.061** 0.901*
DPPH EAF 0.294** –0.673**
DPPH DF –0.563** –0.368**
**
DPPH AlF 0.008 –0.001** 0.901*

Correlation significant at * p < 0.05 and ** p < 0.001; abbreviations: AlE = all extracts, AlF = all fractions.
1156 Healthy Kainama et al.

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