Industrial Crops and Products 83 (2016) 255267

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Industrial Crops and Products

journal homepage: www.elsevier.com/locate/indcrop

Phytochemical content and antioxidant activity of different fruit parts

juices of three gs (Ficus carica L.) varieties grown in Tunisia
Arij Harzallah , Amira Mnari Bhouri, Zahra Amri, Hala Soltana, Mohamed Hammami
Biochemistry Laboratory, Research Laboratory LR12ES05: Lab-NAFS NutritionFunctional Food & Vascular Health, Faculty of MedicineUniversity of
Monastir, Tunisia

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

Article history: Fig is an important source of bioactive compounds and has been a typical component in the health-
Received 2 October 2015 promoting Mediterranean diet for many centuries.
Received in revised form This study was conducted to evaluate differences between phytochemical composition and antioxidant
15 December 2015
properties of juices of peel, pulp and total fruit of gs from three different varieties grown in Tunisia
Accepted 16 December 2015
Mediterranean coast and corresponding to three different colors (green, purple and black) as well as the
Available online 22 January 2016
effect of maturation stage on the amounts of phytochemical composition including total phenols content
(TPC), total avonoids content (TFC), total ortho-diphenols content (TOPC), total tannins content total
Keywords:
Ficus carica L.
(TTC) and total anthocyanins content (TAC).
Fig juice Antioxidant potential was assessed by two assays: 1,1-diphenyl-2-picrylhydrazyl (DPPH) scaveng-
Phytochemical content ing capacity and reducing power (RP) and showed that different g juices extracts exhibited the same
Antioxidant activity antioxidant capacity in both systems tested and at different concentrations.
Fruit color Black peel juice acted as the greatest antioxidant by having the highest DPPH and RP activities followed
by the juice of black g total fruit. The antioxidant capacities observed were attributed to higher total
phenolic, avonoid and anthocyanin contents according to the chemometric results.
Comparison of phytochemical composition of g fruits during the development stage revealed a sig-
nicant increase of TPC, TFC, TOPC, TTC and TAC in the ripe fruits of the three tested varieties.
This is the rst study comparing the phytochemical composition and antioxidant potential of juices of
Ficus carica L. peels, pulps and total fruits.
2015 Elsevier B.V. All rights reserved.

1. Introduction
The g tree (Ficus carica L.) was evidently originated in the Mid-
dle East (Mars, 2001). Most of the worlds g production occurs in
the Mediterranean countries (Sadder and Ateyyeh, 2006), where
diets are characterized by abundant intake of g fruit (Solomon
et al., 2006). Tunisia is one of the most important consumers of
gs. F. carica L. is present all over Tunisia in various environmental
conditions. The tree grows well and produces tasteful and avour-
ing fruits enhanced by warm and shiny conditions during ripening
(Trad et al., 2012).
Abbreviations: TPC, total polyphenols content; TFC, total avonoids content;
TTC, total tannins content; TOPC, total O-diphenols content; TAC, total anthocyanins
content; (DPPH) scavenging capacity, 1,1-diphenyl-2-picrylhydrazyl scavenging
capacity assay; RP, reducing power assay; PCA, principal component analysis.
Corresponding author.
E-mail address: harzallaharij@yahoo.fr (A. Harzallah).
Figs were analysed for total polyphenols, total avonoids and
exhibited high anti-oxidant capacity (Solomon et al., 2006). It is a
very nourishing food and used in industrial products. It is rich in
vitamins, mineral elements, water, and fats. It is one of the highest
plant sources of calcium and ber (Joseph and Raj, 2011). They are
rich in easily digestible natural sugars, and contain rich amounts
of anthocyanins and avonoids that contribute to gs coloration
(Solomon et al., 2006) and to signaling pathways regulation that
guide cellular metabolism. Humans have eaten the fruits of this tree
from the earliest times, and utilized it and its by-products (leaves,
latex, bark, and roots) in various disorders such as gastrointestinal
respiratory, inammatory, cardiovascular disorders, ulcerative dis-
eases, cancers (Canal et al., 2000; Joseph and Raj, 2011), as laxative,
antispasmodic remedies (Guarrera, 2005), antiviral, an tibacterial,
hypoglycaemic, and anthelmintic effects (Jeong et al., 2005; Joseph
and Raj, 2011).
In another hand, gs can be eaten dried, fresh, as a jam or also as a
juice. Figs are often peeled; the pulp is eaten and the peel discarded

http://dx.doi.org/10.1016/j.indcrop.2015.12.043
0926-6690/ 2015 Elsevier B.V. All rights reserved.
256 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 1. Color appearance of the three g varieties examined in this study.

(Veberic et al., 2008), however, in different countries like Tunisia,
consumers prefer to eat the whole fresh fruit.
Most of the previous scientic studies have been focused mainly
on dried gs (Vinson et al., 2005; Vallejo et al., 2012), on fresh gs
to determine their total phenolic prole and antioxidant capacity
(Veberic et al., 2008; Vallejo et al., 2012), and also on g leafs to
describe their antimicrobial activity (Jeong et al., 2009; Lee and
Cha, 2010; Ahmad, 2013) or anti-HSV effect (Joseph and Raj, 2011),
neglecting the other edible parts. However, there is few data com-
paring the phytochemical content changes occurring in the g fruit
during ripening (Veberic et al., 2008; Crisosto et al., 2010), as well
as, in spite of the few researches describing the distribution of
the phenols content between gs pulp and peel (Solomon et al.,
2006; Del Caro and Piga, 2008), no data described neither the whole
phytochemical composition in the g fruit including total phenols
content (TPC), total avonoids content (TFC), total ortho-diphenols
content (TOPC), total tannins content total (TTC) and total antho-
cyanins content (TAC), nor the antioxidant potential of juices of
different g fruit parts.
Thus, to improve the knowledge on g compositions and to val-
orise it as a functional food, the aim of this study is rstly to evaluate
the entire phytochemical composition as well as the antioxidant
capacities of juices of different ripe g fruit parts including peel,
pulp and total fruit of the most abundant varieties in Tunisia cor-
responding to three different colors: black, purple and green; and
secondly, to evaluate the inuence of the variety and the crop tim-
ing on the phytochemical composition level of fresh ripe g fruit.
For every variety, three repetitions were carried out (n = 3); each
repetition included 10 fruits sampled from three trees.
An agricultural technician performed identication of fruit vari-
eties. Fruits were placed in a 4 C refrigerated box and transported
within 3 h to the Herbarium of the Laboratory of Biochemistry, Fac-
ulty of Medicine of Monastir, Tunisia. There, fruits were washed
with water, wiped completely dry and stored at 20 C until prepar-
ing samples the next day.
2.2. Sample preparation
To prepare whole g juice, 10 ripe gs (2nd crop) from each
variety were mixed. An equal portion of ripe gs from each variety
was peeled manually with a knife, paying attention not to include
the fruit pulp. Peel and pulp were mixed separately too. A blender
(Moulinex, France) was used to obtain peel juice, pulp juice and
whole fruit juice. In the blender, the three compartments were
juiced. The juice was centrifuged at 3.000 rpm for 10 min; the super-
natant was kept and ltered through a lter. The ltered juices were
stored at 20 C until preparing methanolic extracts the following
day. Different g juices samples are shown in Fig. 2.
To evaluate the effect of ripening stage on the phytochemical
content of gs, 10 ripe and 10 partially ripe gs from each variety
were homogenized and used.

2. Materials and methods

2.1. Plant material

Fresh g fruits (F. carica L.) were manually picked from a same
farm in Bekalta, (coastal town, governorate of MonastirCentral
East part of Tunisia) in 2 different ripening stages: partially ripe
at the beginning of July 2013 (1st crop) and at ripening time at
the last of August 2013 (2nd crop). Specimens were chosen from
three varieties corresponding to three different colors as following
(Figs. 1 and 2):

Kohli variety is a dark type, black in color with dark red pulp. Fruit
are sweet and juicy.
Hamri variety is a dark type, purple in color with light red pulp.
Fruit are sweet and juicy. Fig. 2. Appearance of different fruit parts juices of the three g varieties examined
in this study.
Bidhi variety is a light type, green in color with dark red pulp.
A1: Bidhi pulp, A2: Bidhi total fruit, A3: Bidhi peel, B1: Hamri pulp, B2: Hamri total
Fruit are sweet and juicy. fruit, B3: Hamri peel, C1: Kohli pulp, C2: Kohli total fruit, C3: Kohli peel.
 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 257

Fig. 3. Bar graphics comparing total polyphenols content (TPC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars
with different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

Fig. 4. Bar graphics comparing total avonoids content (TFC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars with
different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

2.3. Methanolic extracts preparation
Each sample (5 g) was homogenized in 5 ml of methanol until
uniform consistency, using an Ultra-Turrax homogenizer (IKA, T25,
digital). The homogenates were centrifuged at 3000 rpm for 13 min.
The supernatants were recovered, ltered using 0.45 m lter and
stored at 20 C until further analysis within a maximum period of
one week.
2.4. Determination of total phenols content (TPC)
The method of Montedoro et al. (1992) with slight modications
was used to determine total phenolic content. Each extract (0.1 ml)
was combined with water 1:4 (v/v) and 2.5 ml FolinCiocalteus
phenol reagent (1/10) and incubated for one minute at room tem-
perature, followed by the addition of 2 ml of sodium carbonate
(7.5%). The mixture was well shaking and standing for 6 h. The
absorbance of the solutions was measured at 765 nm using a spec-
trophotometer (Lambda 25, UV/vis Spectrometer). Values of TPC
were estimated by comparing the absorbance of each sample with
a standard response curve employing six different Gallic acid stan-
dard solutions, in the same conditions reported for the methanolic
extract. Results are expressed as milli gram gallic acid equivalents
per gram of fresh weight (mg GAE/g FW). Samples of each extraction
were analysed in triplicate.
2.5. Determination of total avonoids content (TFC)
Total avonoid content was quantied using the colorimetric
method with aluminum chloride according to (Marinova et al.,
2005; Lenucci et al., 2006; Bakar et al., 2009). Extract (1 ml) was
mixed with 4 ml of distilled water in a test tube followed by addi-
tion of 0.3 ml of 5% sodium nitrate solution and allowed to react for
5 min. Then 0.3 ml of 10% aluminum chloride solution was added.
After 6 min, 2 ml of 1 M sodium hydroxide was added. The mix-
ture was diluted with distilled water up to 10 ml and then mixed
well using a vortex. The absorbance was immediately recorded at
510 nm.
The absorbance was measured immediately at 510 nm using a
spectrophotometer and the avonoid content was expressed as mg
of Catechin equivalents per gram of fresh weight (mg CE/g FW). All
the tests were carried out in triplicate.
2.6. Determination of total O-diphenols content (TOPC)
Total ortho-diphenol content was determined using the method
described by Bahorun et al. (1996). Test sample (100 l) was mixed
with 1 ml of HCl (0.5N), 1 ml of (NaNo2 + Na2 MoO4 2H2 O) solution
and 1 ml of NaOH (1 M). The mixture was stirred and kept for half
an hour at room temperature in the dark. The absorbance was
measured at 500 nm against the blank. Different concentrations
of hydroxytyrosol solution were used for calibration. Results were
expressed as milli gram of hydroxytyrosol equivalents per gram of
fresh weight (mg hydroxytyrosol/g FW).
2.7. Determination of total tannins content (TTC)
Total tannins content were determined spectrophotometrically
according to Broadhurst and Jones (1978). A 0.5 ml of aqueous
extract, contained in a test tube covered with aluminum foil, was
258 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 5. Bar graphics comparing total ortho-diphenols content (TOC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars
with different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

Fig. 6. Bar graphics comparing total tannins content (TTC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars with
different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

mixed with 3 ml of 4% vanillinmethanol solution and then with
1.5 ml of hydrochloric acid. The mixture was allowed to stand for
15 min at 20 C in the dark. The absorbance of the mixture was
measured at 500 nm.
A different concentration of tannic acid aqueous solution
(30 mg/l) was used for calibration. The nal results were expressed
as milli gram tannic acid equivalents per gram of fresh weight (mg
TAE/g FW).
2.8. Determination of total anthocyanins content (TAC)
Total anthocyanin content was quantied according to
Padmavati et al. (1997) and Chung et al. (2005).
Anthocyanins were extracted from 0.5 g of fresh weight with
20 ml methanol/water: concentrated HCl (80/20/1). Samples were
put on a shaker in the dark at room temperature for 24 h;
absorbance (A) was measured spectrophotometrically with the fol-
lowing equation:
A = A530 (0.24 A657) , (Gould et al., 2000) where A530 is
the absorbance at 530 nm and A657 is the absorbance at 657 nm.
Total anthocyanin content was calculated as mg Cyanidin-3-
glucoside equivalents per 100 g of fresh weight by the following
equation:
TAC = AMWVDF100
100
, (Giusti and Wrolstad, 2001) where
A = absorbance, MW = molecular weight (449.2 g/mol),
DF = dilution factor, and = molar absorbance coefcient
(26,900 L/mol/cm). All measurements were done in triplicate.
2.9. DPPH free radical scavenging activity
The hydrogen atom or electron-donation ability of the F. car-
ica extracts was determined using 1,1-diphenyl-2-picrylhydrazyl
(DPPH) free radical as a reagent according to the method of Braca
et al. (2001) with minor modication. Briey, 3 ml of solution of
DPPH radical in methanol was mixed with 1 ml of g juice extract
at different concentrations (220 mg/ml).
The mixture was shaken vigorously and incubated for 30 min in
the dark at room temperature before measuring the absorbance.
The scavenging capacity was determined spectrophotometri-
cally by monitoring the decrease in absorbance at 517 nm against
a blank using a spectrophotometer (Bio-Rad SmartSpec Plus). The
percent DPPH scavenging effect was calculated using the following
equation:
Acontrol Asample
DPPH scavenging effect(%) = 100
Acontrol
where Acontrol is the absorbance of the control reaction containing
all reagents except the tested compound. Asample is the absorbance
of the test compound.
The results were reported as EC50 value, the effective concen-
tration of antioxidant agent (extract) providing inhibition 50% of
the initial DPPH radical concentration. EC50 was calculated from
the graph-plotting inhibition percentage against extract concentra-
tion. The lowest EC50 value indicates the strongest ability of sample
to act as an antioxidant. Ascorbic acid was used as an antioxidant
standard. Tests were carried out in triplicate.
 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267
2.10. Reducing power assay
The reducing power of methanolic extracts of g juices was
determined by the method of Oyaizu (1986). Substances, which
have reduction potential, react with potassium ferricyanide (Fe3+)
to form potassium ferrocyanide (Fe2+), which then reacts with fer-
ric chloride to form ferric ferrous complex that has an absorption
maximum at 700 nm according to the following equation:
Antioxidant
Potassium ferricyanidine + Ferric chloridePotassium
ferrocyanide + Ferrous chloride
Different concentrations (220 mg/ml) of g juice extract
(2.5 ml) were mixed with sodium phosphate buffer (2.5 ml, 0.2 M,
pH 6.6) and potassium ferricyanide [K3 Fe (CN)6] (2.5 ml, 1%). The
mixture was incubated at 50 C for 20 min. After cooling, 2.5 ml of
trichloroacetic acid (10%) were added to the mixture, which was
then centrifuged at 3000 rpm for 10 min. The upper layer of solu-
tion (2.5 ml) was mixed with distilled water (2.5 ml) and a freshly
prepared ferric chloride solution (0.5 ml, 0.1%). The absorbance was
measured at 700 nm in a spectrophotometer. Increased absorbance
of the reaction mixture indicates increase in reducing capability.
The percentage increase in reducing power was calculated using
the following equation:
A test A blank
Increasing in reducing power(%) = 100
A blank
where A test is absorbance of test solution; A blank is absorbance of
blank. Control was prepared in similar manner excluding samples
without adding standard or test compound. Ascorbic acid was used
as standard at the same concentrations of the samples. Reducing
power was measured by varying the concentration of the extract
and the contact time.
2.11. Statistical analyses
For all the experiments three samples of each g juice were ana-
lysed and all assays was carried out in triplicate. Data analyses were
performed using SPSS software version 22, Duncan multiple range
test at p < 0.05 probability level. Principal component analysis (PCA)
was carried out using XLSTAT (2014) for Windows (Addinsoft, New
York, USA).
3. Results and discussion
3.1. Phytochemical composition in (peel, pulp, total fruit) g
juices of different varieties
The phytochemical composition dened by the total polyphe-
nol (TPC), total avonoid (TFC), total ortho-diphenol (TOPC), total
tannin (TTC) and total anthocyanin (TAC) contents of peel, pulp
and total fruit juices from three ripe gs (2nd crop) varieties was
estimated.
The total phenolic content (TPC) of juices extracts is shown in
Fig. 3. For the black g, peel juice showed a high TPC, followed by
total fruit and pulp. Values varied between 50.57 GAE/g FW and
74.16 mg GAE/g FW. Concerning purple g, the amount of TPC was
higher and near in all juices, especially for peel and total fruit juices
(61.47 mg GAE/g FW and 63.11 mg GAE/g FW.). This may suggest
that peel is responsible of the higher content of fruit TPC. How-
ever, for Bidhi variety (green g), amount of TPC was the lowest
and close in the three juices (p > 0.05) comparing to other varieties.
Similar data were reported by Faleh et al. (2012) who found that
green varieties of dry g have higher phenolic content than red
ones, but discorded with those founded by Solomon et al. (2006)
259
who reported that total phenolic content of Kadota pulp (green
variety) was signicantly higher compared with peel. Among vari-
eties, dark fruits (black and purple gs) showed higher polyphenols
content than the light ones (green g). Differences observed were
statistically signicant (p < 0.05).
Flavonoids are important for human health because of their
high pharmacological activities as radical scavengers (Bakar et al.,
2009). The total avonoid content (TFC) is mentioned in Fig. 4 are
expressed in terms of (mg CE/g FW). Peel of Kohli variety showed
the highest concentration of avonoids (12.75 mg CE/g FW). Mean-
while, in Hamri variety avonoids were concentrated in total fruits
(11.30 mg CE/g FW). However, in Bidhi variety, avonoids exhib-
ited the lowest concentration compared to the other varieties with
similar amounts in different juices parts.
Statistically signicant differences in ortho-diphenol content
(TOPC) were found between dark and light varieties (p < 0.05)
(Fig. 5). TOPC in the peels ranged from 8.81 mg hydroxytyrosol/g
FW for Kohli variety to 1.45 mg hydroxytyrosol/g FW for Bidhi vari-
ety; in the total fruits from 6.97 mg hydroxytyrosol/g FW for Kohli
variety to 1.74 mg hydroxytyrosol/g FW for Bidhi variety and in
the pulps from 3.92 mg hydroxytyrosol/g FW for Kohli to 2.44 mg
hydroxytyrosol/g FW for Bidhi variety. Total ortho-diphenol con-
tent were concentrated differently according to variety: for Kohli
in peel, for Hamri in total fruit and in pulp for Bidhi variety.
Total tannin content (TTC) was found being usually more abun-
dant in Bidhi variety (75.98 mg TAE/g FW in peel, 65.87 mg TAE/g
FW in pulp and 60.35 mg TAE/g FW in total fruit) than in Kohli and
Hamri ones (Fig. 6). All differences observed between varieties for
all samples studied were statistically signicant. For Kohli and Bidhi
varieties, TTC were concentrated in peel. However in Hamri variety,
they were abundant in the total fruit.
Total anthocyanin content (TAC) was ranged from 429.80 mg
cyanidin-3-glucoside/100 g FW (total fruit) to 162 mg cyanidin-
3-glucoside/100 g FW (pulp) for Hamri and from 344.89 mg
cyanidin-3-glucoside/100 g FW (pulp) to 144.62 mg cyanidin-3-
glucoside/100 g FW (peel) for Bidhi (Fig. 7). Among varieties,
our results showed that Hamri and Bidhi varieties had the low-
est anthocyanin content (p < 0.05). Peel and total fruit of Kohli
variety hold both the higher total anthocyanin content with respec-
tively 3330.84 mg cyanidin-3-glucoside/100 g FW and 1972.47 mg
cyanidin-3-glucoside/100 g FW. Our results are similar to those of
Piga et al. (2005) who indicated that anthocyanins are found mainly
in the peel, except for certain types of red fruit, in which they also
occur in the pulp (cherries and strawberries). A signicant differ-
ence (p < 0.05) between pulp juice and the other parts juices was
observed only for Kohli variety.
In summary, dark gs in particular, Kohli g (black variety) had
a signicantly higher content of four phytochemical classes: TPC,
TFC, TOPC and TAC, compared with the green one; with peel being
the major contributing part. TPC, TFC, TOPC and TAC contents were
signicantly different among the three vegetal materials, follow-
ing the order peel > total fruit > pulp for black g and the order total
fruit > peel> pulp for purple g. Our results are also consistent with
those of Caliskan and Polat (2011) who reported that some purple
and black g fruits, from Turkey, contained 2.5-fold higher TPC and
15-fold higher TAC than the green and yellow ones. Same observa-
tion was shown with Italian g fruits (Del Caro and Piga, 2008) and
Turkish g fruits (Solomon et al., 2006) where black gs were men-
tioned to have higher amounts of polyphenols and anthocyanins
than the green ones and those amounts were concentrated in the
g peel. The signicant difference between peel and pulp content
has also been previously found in other consumed fruits, such as
nectarines, peaches and plums (Toms-Barbern et al., 2001) and
was mainly related in the anthocyanin content. Anthocyanins are
pigments they impart a pink, red, blue, or purple color in the epi-
dermal tissues of owers and fruit. In human diet, they are found
260 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267
Fig. 7. Bar graphics comparing total anthocyanins content (TAC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars
with different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.
in some cereals, leafy, root vegetables and mostly in fruits (Mazza
and Miniati, 1993).
It was proposed that cyanidin was the sole anthocyani-
din skeleton in g fruits (Solomon et al., 2006). Puech et al.
(1975) suggested the presence of three anthocyanins in dark
g fruits, namely, cyanidin-3-rhamnoglucoside, cyanidin 3,5-
diglucoside, and pelargonidin 3-rhamnoglucoside, with cyanidin-
3-rhamnoglucoside being the predominant pigment in ripe peels.
Recently, (Del Caro and Piga, 2008) reported that cyanidin 3-O-
rutinoside was present in both peel and pulp of black g, whereas,
cyanidin 3-O-glucoside was dominated in the peel of black g only.
Different expression of genes controlling the anthocyanin pathway
may result in differences in fruit color, with the highest expres-
sion associated with the dark varieties. Furthermore, (Oliveira
et al., 2009) reported the high amount in g peel of the avonoid
quercetin 3-O-rutinoside compared to g pulps and leaves.
Data indicate that chemical composition is dependent on the
fruit part and the variety, thus extracts of darker varieties namely
peel, showed higher contents of phytochemicals compared to
lighter colored extracts.
3.2. Antioxidant activity in (peel, pulp and total fruit) juices of
different g varieties
The antioxidant capacity was evaluated using two commonly
used colorimetric methods namely, 1,1-diphenyl-2-picrylhydrazyl
(DPPH) free radical scavenging activity and reducing power (RP)
assay.
3.2.1. DPPH radical scavenging activity
The 1,1-diphenyl-2-picrylhydrazyl DPPH is usually used as a
reagent to evaluate free radical scavenging activity of antioxidants
(Oyaizu, 1986). In the DPPH assay, the antioxidants were able to
reduce the stable radical DPPH to the yellow colored diphenyl-
picrylhydrazine. Radical scavengers decolorize the colored DPPH ,
so the loss of absorbance at 517 nm reects radical scavenging
activity.
This study attempted to compare the DPPH free radical (DPPH )
scavenging activity of different juices of g fruit parts tested (Fig. 8).
The scavenging effect was compared to ascorbic acid such as a
standard. The free radical scavenging activity is expressed as per-
centage of DPPH inhibition and by the antioxidant concentration
required for a 50% of radical reduction (EC50), so that a lower
value of EC50 indicated a higher antioxidant activity and vice versa
(Table 1).
Table 1
EC50 values obtained in DPPH antioxidant assay of different fruit parts juices of three
g varieties with three different phenotypes.
Phenotypes Peel (mg/ml) Pulp (mg/ml) Total fruit (mg/ml)
Black 4.52 0.71a 15.45 0.98d 8.63 0.15c
Purple 9.71 0.83c 12.99 0.74d 7.04 0.15b
Green 26.7 1.92e 10.59 0.74c 14.6 0.62d
Values are expressed as mean SD (n = 3) of triplicate measurement. Means with
different letters are signicantly different (p < 0.05).
There was a dose-dependent relationship in DPPH scavenging
activity of all three parts (peel, pulp, total fruit) juices of three g
varieties within the range of concentrations from 2 to 20 mg/ml.
All samples were proven having antioxidant activities with signi-
cant differences (p < 0.05) between all juices extracts. The peel juice
extract of black g with a mean value of 4.55 mg/ml for EC50 was
almost near to EC50 of ascorbic acid (2.21 mg/ml) (Fig. 8a, Table 1).
The total fruit juice extract EC50 of purple variety (mean value
6.96 mg/ml) was lower than those of peel (mean value 9.73 mg/ml)
and pulp (mean value 12.98 mg/ml). The juice extract of the pur-
ple total fruit was found to act as a stronger secondary antioxidant
(Fig. 8b, Table 1). The peel juice extract of green g present the low-
est DPPH scavenging activity (Fig. 8c) and the highest EC50 value
(Table 1) so that the weakest antioxidant capacity (1214 times
less active than ascorbic acid). Antioxidant activity against DPPH
was correlated with the concentration, chemical structure, poly-
merization, and degree of antioxidants (Kumaran and Karunakaran,
2007; Oszmianski et al., 2007).
3.2.2. Reducing power assay
The reducing capacity of a compound may serve as a signicant
indicator of its potential antioxidant activity. In this assay, the yel-
low color of the test solution changes to various shades of green and
blue depending on the reducing power of each compound (Chung
et al., 2002).
As shown from Fig. 9, g juices of different parts had effec-
tive and powerful reducing power when compared to the standard
ascorbic acid. At 20 mg/ml, peel and total fruit juices extracts of
Kohli g, as well as total fruit and peel juices extracts of Hamri g
demonstrated the highest and the nearest absorbance to those of
ascorbic acid at the same concentration. Absorbance values were
ranged from 3.36 (Kohli peel) to 2.33 (Kohli total fruit) versus 4.17
for the ascorbic acid. Differences observed between peel, pulp and
total fruit of each variety were statistically signicant (p < 0.05)
started from 15 mg/ml. The reducing properties in foods are asso-
ciated with reductones (Duh, 1998; Jayaprakasha et al., 2001). The
 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267
phenolic compounds present in g juices may act in a similar
fashion as reductones by donating electrons and quenching free
radicals.
To conclude, it was found that at the same higher concentration,
the extracts cited previously had always the powerful antioxidant
activities, measured either by reducing power test or by DPPH test,
probably because the phenolic compounds in gs react similarly
within two methods. Toms-Barbern et al. (2001) suggested the
fact that the varied radical scavenging activity of extracts depended
on the amount of total phenolic in each fraction. The antioxidant
capacity is highly correlated with the presence of anthocyanins too
(Shiow and Lin, 2000). The relative contributions of anthocyanins to
the overall antioxidant capacities were estimated in previous study
to 28 and 36% in dark g fruit (Solomon et al., 2006).
Peel of green g, and the pulp of black g, maintain both the
last positions in the antioxidant capacity scale. Black peel holds the
higher antioxidant potential. This study is in agreement with other
Fig. 8. DPPH free radical scavenging activity at different concentrations (220 mg/ml) of a reference antioxidant: ascorbic acid and different g parts juices of three varieties
in Tunisia. (a) Kohli, (b) Hamri, (c) Bidhi. Values performed in triplicate.
261
studies suggesting that common fruits and vegetables with dark
blue or red colors have the highest antioxidant capacity (Liu et al.,
2002; Wu et al., 2006; Celik et al., 2008). Our results are consistent
with those of Solomon et al. (2006) who reported that dark-colored
gs exhibited the highest antioxidant capacity.
Fig varieties with dark peel contain higher levels of polyphenols,
avonoids anthocyanins, and accompanied by higher anti-oxidant
activity compared with g variety with light peel. Peel of black g
might be rich sources of natural antioxidants.
While eating the fruit, consumers tend most often to remove the
peel; however fruit peels are clearly the major source of phenolic
compounds, acting as antioxidants that should not be discarded; in
fact, the consumption of total ripe fruits, fresh or as a juice is recom-
mended. A part the presence of antioxidants, g juice is a rich source
of carbohydrates and organic acids (Oliveira et al., 2009), known for
their health promoting effects. Its consumption may contribute to
its protective role against diseases related to oxidative stress.
262 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 9. Reducing power (RP) of different concentrations (220 mg/ml) of a reference antioxidant: ascorbic acid and different g parts juices of three varieties in Tunisia. (a)
Kohli, (b) Hamri, (c) Bidhi. The reducing power was estimated based on the absorbance reading at 700 nm. Values performed in triplicate.

3.3. Changes in total phytochemical composition during fruit
development
The phytochemical composition consisting of the total polyphe-
nol (TPC), total avonoid (TFC), total ortho-diphenol (TOPC), total
tannin (TTC) and total anthocyanin (TAC) levels was compared
between 1st crop (partially mature fruit) and 2nd crop (mature
fruit) gs. Phytochemical composition level increased in all ripe
fruits compared with partially ripe ones. Results are shown in
Fig. 10.
Amounts of polyphenol and avonoid contents show a sig-
nicant increase (p < 0.05) between two crops. Total polyphenol
content ranged from 48.0 mg GAE/g FW (Bidhi) to 70.9 mg GAE/g
FW (Hamri) in partially ripe fruit and from 88.5 mg GAE/g FW
(Bidhi) to 153 mg GAE/g FW (Hamri) in ripe fruit. Total avonoid
content ranged from 6.7 mg CE/g FW (Bidhi) to 9 mg CE/g FW
(Hamri) in partially ripe fruit and from 12.2 mg CE/g FW (Bidhi)
to 24.7 mg CE/g FW (Hamri) in ripe fruit. A signicant (p < 0.01)
increase in TFC of Kohli variety was shown. Ripe gs are 2 times
richer in polyphenols than partially ripe ones and 23 times richer
in avonoids.
Total orthodiphenol content values ranged from to 3.8 mg
hydroxytyrosol/g FW (Bidhi) to 16.0 mg hydroxytyrosol/g FW
(Kohli) for ripe fruit and from 0.3 mg hydroxytyrosol/g FW (Bidhi)
to 4.1 mg hydroxytyrosol/g FW (Hamri) for partially ripe fruit. Total
tannin content values ranged from 45.5 mg TAE/g FW (Kohli) to
134.4 mg TAE/g FW (Bidhi) for ripe fruit and from 14.0 mg TAE/g FW
(Kohli) to 21.0 mg TAE/g FW (Bidhi) for partially ripe fruit. Results
showed that TTC content in total g fruit was 3 and 6 times higher in
ripe g than in partially ripe ones, respectively for Kohli and Bidhi
varieties, however, the increase is very marked (p < 0.01) in ripe
fruit of Hamri variety where TTC achieved an amount of 109.73 mg
TAE/g FW.
Total anthocyanin content in partially ripe fruits was 1150.9 mg
cyanidin-3-glucoside/100 g FW for Kohli and was approximately
similar and low in Hamri and Bidhi varieties (respectively
637.5 mg cyanidin-3-glucoside/100 g FW and 529.8 mg cyanidin-
3-glucoside/100 g FW). Total anthocyanin content increased, with
different degrees, in all ripe fruits compared with unripe ones.
Hamri and Bidhi fruits of 2nd crop were 1.5 times richer in
anthocyanins than 1st crop fruits. Kohli ripe fruits were 4 times
richer in anthocyanins than Kohli partially ripe fruits. In fact,
Kohli variety showed the highest anthocyanin content in ripe
fruits (4447.1 mg cyanidin-3-glucoside/100 g FW) with a signicant
increase (p < 0.01) compared to partially unripe gs. However, there
was not a signicant difference in anthocyanin amounts between
the partially ripe and rip gs of the purple (Hamri) and the light
(Bidhi) varieties were TAC values remain very low (respectively
 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 263

Fig. 10. Bar graphics comparing total polyphenols content (TPC), total avonoids content (TFC), total tannins content (TTC), total O-diphenols content (TOPC) and total antho-
cyanins content (TAC) between ripe fruit (2nd crop: August crop) and partially ripe fruit (1st crop: July crop) in three g varieties. Results are expressed as means standard
deviation (n = 3).
264 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 11. (a) Principal components analysis (scores and loading plots, biplot) based on different phytochemical compounds analyzed in peel juices of three Tunisian g varieties
and their antioxidant activity (%DPPH and reducing power (RP)). TPC: total polyphenols content; TOPC: total O-diphenols content; TFC: total avonoids content; TTC: total
tannins content; TAC: total anthocyanins content. (b) Principal components analysis (scores and loading plots, biplot) based on different phytochemical compounds analyzed
in pulp juices of three Tunisian g varieties and their antioxidant activity (%DPPH and reducing power (RP)). TPC: total polyphenols content; TOPC: total O-diphenols content;
TFC: total avonoids content; TTC: total tannins content; TAC: total anthocyanins content. (c) Principal components analysis (scores and loading plots, biplot) based on
different phytochemical compounds analysed in total fruit juices of three Tunisian g varieties and their antioxidant activity (%DPPH and reducing power (RP)). TPC: total
polyphenols content; TOPC: total O-diphenols content; TFC: total avonoids content; TTC: total tannins content; TAC: total anthocyanins content.
 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267
949 mg cyanidin-3-glucoside/100 g FW and 697.1 mg cyanidin-3-
glucoside/100 g FW).
The variety (Oliveira et al., 2009) and the maturity stage inter-
act between each other to affect fruit properties (Crisosto et al.,
2010). Many changes develop during fruit ripening such as, peel
colour, antioxidant capacity (Toor and Savage, 2005) and physic-
ochemical properties (Alkarkhi et al., 2011) in particular acidity
decrease (Wu et al., 2007; Crisosto et al., 2010; Zhang et al., 2010),
sugar increase (Wu et al., 2007) and aromatic composition (Trad
et al., 2012; Braga et al., 2013), therefore the production of phy-
tochemicals is also inuenced. Total phenolic (Josefa et al., 2006)
and total anthocyanin (Shiow and Lin, 2000) contents were shown
increased in ripe fruits. However, the present results are not consist
with those of Kubola and Siriamornpun (2011) who mentioned that
fruit total phenolic and total avonoid contents decreased during
the fruit development stage.
Fruit ripening process is always accompanied by a change in
fruit softening and texture. Enzymes are shown to have a role in
fruit ripening. Expression of enzymes involved in the degradation
of many different cell wall polymers present in different g tissue is
coordinated both in time and amount with the fruit development
(Owino et al., 2004). Peroxidase, polyphenol oxidase (PPO), pro-
tease and carbohydrases are involved in mango peel ripening (Ajila
et al., 2007).
Differences in phytochemical content between the two crops
can be explained by weather conditions too. At last of August,
when 2nd crop was picked, environment was more warm, dry and
sunny than at the beginning of July (1st crop), and so, was favor-
able for fruits growth and development. The sun-exposed peel of
apples terminal fruit had higher anthocyanin levels than shaded
peel (Awad et al., 2000). Results were in accordance with those of
Veberic et al. (2008) for gs varieties from northern Mediterranean
region who stated that the sun-shining weather in August is more
favorable for gs growth than in September which is marked by
cooler and moister weather. However, phenolic concentration lev-
els reported were several times higher than those noticed in the
present study. This could be explained by the difference of vari-
ety, climate and environment, as Tunisia is located in the south
Mediterranean region. The inuence of the region of cultivation
(north or south) on the concentration of phenolics in bananas was
conrmed (Mndez et al., 2003). The level of anthocyanin in the
fruit depends on various factors, namely: species, varieties, growing
conditions, seasonal variations, maturity index, processing meth-
ods, and storage conditions (Melgarejo et al., 2000; zkan, 2002). In
contrast, Vallejo et al. (2012) mentioned that g fruit from a crop in
(MayJune) showed even further highest values of total phenolics
comparing to a second crop in (AugustSeptember). However, this
difference is signicant in peels and not in the pulps of g fruit.
In general way, during the ripening period, weather conditions
could be either favorable or stressful for the fruit growth. Pro-
duction of avonoids, classied as environmental compounds
because of their production in direct response to environmental
conditions, is dependent on ultraviolet light and CO2 levels (Daniel
et al., 1999; Caldwell et al., 2005).
3.4. Chemometric analysis
The chemometric analysis results generated three biplots show-
ing groupings and subgroupings: the principal component analysis
(PCA) (Fig. 11) was carried on the data to compare the phytochem-
ical composition of peels (Fig. 11a), pulps (Fig. 11b) and total fruits
(Fig. 11c) juices of three studied varieties of gs and to identify
the factors inuencing each one. The position of each variable in
the loading plot describes its relationship with the other variables.
Variables that are close to each other have high correlations.
265
The rst PCA (Fig. 11a) accounted 87.65% of the total variance
(99.25%), the second PCA (Fig. 11b) accounted 67.49% of the total
variance (93.23%) and the third PCA (Fig. 11c) accounted 81.08% of
the total variance (97.74%) on the rst component while the second
component accounted 16.68%.
Comparisons between PCAs plots indicated that for three PCAs,
PC1 was dominated by the following variables: TAC, TOPC, TFC and
TPC that were correlated positively with Kohli and Hamri varieties
and so they were the mainly responsible for the discrimination of
dark peels. However, Bidhi group (green variety) was negatively
associated with PC1 and positively with PC2 and was characterized
by the abundance of tannins.
Reducing power and DPPH groups were correlated positively
with Kohli and Hamri groups for peel and total fruit PCAs with a
slightly higher correlation for Kohli variety (Fig. 11a and b). Antho-
cyanin, avonoid and polyphenol, concentrated in Kohli variety
more than in Hamri one, seem to be the principal contributors to
strong the antioxidant activity revealed by the reducing power and
%DPPH scavenging activity. However, for PCAs pulp, RP and DPPH
were correlated negatively with PCA1 (Fig. 11c). Tannins provided
by green gs were apparently responsible of the antioxidant capac-
ity of g pulps. Tannins are well known as potent antioxidants.
The soluble tannins are gradually converted into non-soluble con-
densed form as the fruit begins to ripen and advances progressively
(Myhara et al., 1999).
Chemometric observations were consistent with those obtained
during the evaluation of antioxidant activity of juices. The principal
component analysis gave further information about the differences
among the g parts as well as their implication on the antioxidant
activity revealed by the reducing power and %DPPH scavenging
activity. Results clearly indicated that each variety could be distin-
guishable from the other. Phytochemical compounds accumulate
differently depending on the fruit part and the variety.
4. Conclusion
This is the rst study comparing juices of F. carica peels, pulps
and total fruits, contributing to more knowledge about the nutri-
tional aspects of an important fruit of the Mediterranean diet.
The content level of phytochemicals (TPC, TFC, TOPC, TTC, and
TAC) is usually inuenced not only by the variety, but also varies
signicantly from one fruit part to the other. Antioxidant capacity
of g seemed to be mostly related to the peel part and not the
pulp part. Facts suggest that in a general way, the peel color allow
distinguishing the fruit phenol and anthocyanin contents. The large
amount of tannins contained in different compartments of green g
may cause its non-negligible antioxidant capacity.
The phytochemical composition of g including phenols,
avonoids, ortho-diphenols tannins and anthocyanins contents is
inuenced by the ripening stage and varieties of g.
Total polyphenol, total avonoid, total ortho-diphenol, total tan-
nin and total anthocyanin contents can be used as indicators of the
antioxidant activity of foods.
Results of this study would stimulate further researches on dark
gs, especially; g peel, which is a by-product, to be utilized a useful
source of natural food preservative from a nutritional related point
of view and other g parts as a potential new source of natural
antioxidants for food and pharmaceutical industries.
Acknowledgments
This study was supported by a grant (to Arij Harzallah) from
MOBIDOC device launched under the Supported Project to the
research and Innovation System (PASRI), funded by the European
266 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267
Union and managed by ANPR, Tunisia. It is a part of collaboration
with Sano Winthrop-Tunisia Pharmaceutical.
This study is a part of research program of the Research
Unit LR12ES05 Nutrition-Functional food and Vascular Health
LR-NAFS and DGRST-USCR-Mass Spectrometry nanced by the
Ministry of Higher Education and Scientic Research (Tunisia).
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