1 Ficus species good sources of natural antioxidant drugs
Parul AKHTAR1, Zahira YAAKOB1,*, Yunus AHMED1,2, Md. SHAHINUZZAMAN1
1Department of Chemical and Process Engineering, Faculty of Engineering and Built Environment, Universiti Kebangsaan Malaysia, Bangi, Selangor 43600, Malaysia.
2Department of Chemistry, Chittagong University of Engineering & Technology, Chittagong-4349, Bangladesh.
*Corresponding author.
Prof. Ir. Dr. Zahira Yaakob
Email: [email protected] Tel.: +60389216420; Fax: +60389216148.
ABSTRACT
Objectives: Ficus species are a major crop, and are utilised worldwide. The objectives of this study was to examine the antioxidant activity, total phenolic content and yield of extract of different parts of twelve Ficus species and to compare these activities by different extraction processes.
Materials and Methods: DPPH, ABTS free radical scavenging assay and total phenolic contents (TPC) were performed to assess the antioxidant activity. The cluster and correlation analysis were also performed.
Results: The highest percentages of inhibition were 94.58±0.88 % of DPPH and 99.66±0.55 % of ABTS inhibition. In addition, Trolox equivalent antioxidant capacity (mg TE/g dry parts) were 39.23±0.34 for DPPH and 29.18±0.16 for the ABTS assay.
The highest total phenolic contents were between the ranges of 22.29±0.69 and 27.03±0.53 mg GAE/g, respectively and extraction yields were 8.63±0.19 and 11.77±0.21 %, respectively, for maceration and ultrasonication extraction.
Conclusion: Most of the extracts from Ficus sp. obtained by UAE process showed the highest activity and yields in comparison to the maceration process. In a comparison amongst all the parts, fruits of ‘Ficus grossularioides Burm. f’ showed the highest antioxidant activity, and fruits of ‘F. fistulosa Reinw. ex Blume’ exhibited the highest phenolic content and yield of extract in both the extraction process. These
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2 results show that Ficus species are by-products with strong radical scavengers and can be considered as good sources of natural antioxidants for food applications, amongst other purposes.
Keywords: Ficus species, Moraceae, Antioxidant activity, Phenolic compounds; Yield percentages
INTRODUCTION
The genus Ficus belongs to the Moraceae family, containing about 800 species and 2000 varieties, constituting the largest genera of angiosperms in the world. These species include woody trees, shrubs, vines, hemiepiphytes, climbers, and creepers, which are present in most tropical and subtropical forests.1 Different parts of these species have been used in folk medicine for a variety of purposes, due to their antimicrobial, antidiabetic, anticarcinogenic, anti-inflammatory, anthelmintic, mild laxative, hypotensive, antirheumatic, digestive and anti-dysentery drugs and antioxidant activities.2,3 Furthermore, these species provide a rich source of chemicals, such as alkaloid, coumarin, flavonoid, polyphenols, sterol, triterpenes, anthocyanin and other metabolites.1,3 Among natural antioxidants, polyphenolic compounds are one of the most abundant and are extensively distributed in the plants, acting as free radical scavengers and antioxidants. Therefore, the discovery of polyphenolic compounds from natural sources have received increased attention for their potential role in the prevention of human diseases,4 where these antioxidants can be included as part of the diet in the form of a food supplement or as a drug.
A few studies have reported the antioxidant activity and other pharmacological activities on the common Ficus sp., which include F. auriculata Lour,5,12 F.
benghalensis L,9,11,14 F. religiosa L,22 F. microcarpa L.f 23 and F. racemose L,9,13 F.
carica L.10,15,16,24,26 However, the antioxidant activity and profiling of phenolic compounds of most of the Ficus species have remained unexamined and lack extensive documentation. Most of the researchers investigated the antioxidant activity, phenolic content, and others bioactivities on the leaves of Ficus species.5-7 On the contrary, few studies have focused on fruits,8-10 barks11,12 and others parts13,14 of the Ficus sp., investigating a low number of species or from concrete regions. However, some studies suggest that leaves exhibited higher phenolic content and antioxidant
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3 capacity in comparison to other parts of the Ficus species, due to the presence of phenolic compounds.15,16 Concomitantly, leaves of Ficus species displayed higher antioxidant activity through both the mechanisms of single electron transfer and hydrogen atom transfer.16 Most of the researchers analysed native Ficus species pertaining to their geographical regions, but there are hundreds of common species available worldwide. Currently, there are no reports dealing with the extraction processes to maximize antioxidant activity and compare this activity across different parts of the Ficus species.
The aim of this work was to determine the antioxidant activity, total phenolic content and yield of extract of different parts of twelve Ficus species and to compare these activities by using two widely used extraction processes, ultrasonication and maceration, which are widely used. This is the first report, where maximum numbers of Ficus species and its different parts were examined, and correlating different techniques and extraction methods used for analysing antioxidant activity. Also, a process was developed for identifying the phenolic compounds, which exhibited maximum antioxidant activity. The cluster and correlation analysis were also performed for these species in both the extraction processes. The results from this study could have the potential to aid in the development of antioxidant formulations for food and health applications.
MATERIAL AND METHODS Chemicals and reagents
1,1-Diphenyl-2-picrylhydrazyl(DPPH),2,2'-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) and 6-hydroxy-2, 5, 7, 8-tetramethylchroman-2-carboxylic acid (Trolox) were purchased from Sigma-Aldrich, USA. Folin-Ciocalteu reagent was purchased from Merck, Germany. Potassium persulfate, 99.9 % pure ethanol, monohydrate gallic acid and anhydrous sodium carbonate were purchased from Friendemann Schmidt (FS) Chemicals, Australia. All the chemicals used were analytical grade. 18 mΩ deionised water was used to prepare the standard materials and extraction.
Sample preparations
Different parts of twelve Ficus species were collected from the Universiti Kebangsaan Malaysia (UKM) main campus from different locations, with the exception of F. carica
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4 L , which was collected from the Fig garden, Living lab energy and Future crops laboratories at Kuala Pilah under the Faculty of Engineering and Built Environment (FKAB), UKM in May 2016. Every part of Ficus species was washed with deionized water, given an airing at room temperature, and then dried at 35-40 ºC with the help of Septree Food Dehydrator, China. All the parts of the Ficus species were powdered using a special grinder (XY-2200B, Shenzhen Yason General Machinery Co., Ltd, Guangdong, China) and stored in an airtight container.
Extraction procedures of Antioxidants Ultrasound-assisted extraction (UAE)
Ultrasonication extraction was fulfilled in a Thermoline ultrasonic bath (220 V and 40 kHz) at 35 0C. 250 mg of dried and ground powdered sample was transferred in a capped long test-tube (50 mL) and 10 mL of 75% of the ethanolic solution was poured in the sample. Then the mixture was immersed in the ultrasonic bath and fixed to in the same position during sonication (30 minutes). After the extraction, the suspension sample was centrifuged at 4000 rpm for 15 min. Then the supernatant liquid was filtered and the extract was obtained and used directly for the determining the required properties
Maceration extraction
The same amount of dried and powdered sample (250 mg) was kept in a capped long test-tube and extracted by the same volume and percentages of aqueous ethanol. The samples were extracted at room temperature for half an hour (30 min) with an orbital shaker at 200 rpm. After shaking, all the suspension samples were placed in a centrifuge machine at 4000 rpm for 15 min, and subsequently, the liquid was filtered and the aforementioned extracts were stored at 40C for the analysis of biological activity within 2 days.
Total antioxidant capacity
DPPH free radical scavenging assay
The DPPH activity of different parts of Ficus species were measured by using pre- reported methods with some modifications.17 In brief, 0.1 mM of fresh DPPH was prepared with the 75% of aqueous ethanol. 100 μL of the standard Trolox solution (positive control) or appropriate dilutions of different extract were mixed with 3.9 mL of
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5 0.1 mM DPPH solution. Then the control, standard and sample absorbance were measured at 520 nm after 30 minutes incubation at room temperature. Trolox equivalent antioxidant capacity (TEAC) was calculated by prepare a trolox curve (the standard curve equation: y = -0.001x + 1.0338, R2 = 0.9997) from 31.25 µg/mL to 1.0 mg/mL of standard trolox solution and the results were expressed as mg trolox equivalent (TE)/ g dry leaves (DL). The DPPH scavenging activity was expressed as a percentage of inhibition. The scavenging capacity or inhibition of DPPH (%) was calculated by using the equation below:
Antioxidant capacity (% inhibition) = [ (Acontrol – Asample) / Acontrol] ×100 (1)
Where Acontrol is the absorbance of radical solution with 70% of aqueous ethanol;
Asample is the absorbance of radical solution mixed with sample extract or standard.
Each sample and standard were measured in three replicates. The absorbance was measured with 756 PC UV–Visible spectrophotometer (Shanghai Yuefeng Instruments & Meters Co., Ltd.).
ABTS+ free radical scavenging assay
The ABTS radical scavenging assay was calculated based on18 with some modifications. First the radical solution was prepared by mixing both the stock solutions, 7 mM aqueous solution of ABTS and 2.45 mM potassium persulfate (K2S2O8) solution at a ratio of 1:119. The mixture was kept for 12-16 hours in the dark at room temperature. Then the fresh working solution was prepared for each bioassay by diluting 1 ml ABTS radical solution with required amount of ethanol to obtain the absorbance of 0.700 ± 0.02 units at 750 nm. Afterwards, 100 μL of different extracts or different standard Trolox solution was added to 3.9 mL of an ABTS+ solution. The absorbance was measured immediately at 745 nm, after 6 minutes incubation at room temperature. 75% of aqueous ethanol and Trolox were used as blank and positive control respectively, and Trolox was taken as a positive control. TEAC was calculated by preparing a trolox curve for ABTS assay (the standard curve equation: y = -0.0008x + 0.5856, R2 = 0.9999) from 31.25 µg/mL to 730 µg/mL of standard trolox solution and the results were designated as mg TE/g DL. The percentages of inhibition of ABTS was calculated by equation 1. The equipment used was described before.
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6 Determination of total phenolic content
The phenolic content of different parts of Ficus species was analysed by using Folin- Ciocalteu (FC) reagent with some modifications20. FC reagent was used as an oxidising agent. Firstly, 100 μL of the standard gallic acid or crude extract were mixed with 3.4 mL of 20 times pre-diluted of Folin-Ciocalteu reagent. The samples and standards were properly mixed and allowed to stand for 7 min; then 500 µL of 20%
Na2CO3 was added to the test tube containing the main solution and incubated for 2 hours at room temperature under dark conditions. Finally, the absorbance was recorded at 760 nm based on a colorimetric redox reaction from a standard curve (y = 0.0039x + 0.0396, R² = 0.9998), and using standard gallic acid solution of 31.25 µg/mL to 1.0 mg/mL. The results were presented as mg gallic acid equivalent (GAE)/g DL.
Each standard and extract was measured in three times (n= 3).
Statistical analysis
To study the variance of antioxidant activity and phenolic content of different parts of the Ficus species, data was processed by one-way analysis of variance (ANOVA) using STATGRAPHICS Centurion XVII (Version 17.2.00, StatPoints Technologies Inc.
1982 - 2016). Correlation, regression and cluster analysis were also carried out in STATGRAPHICS Centurion XVII. Statistically significant differences were determined by the Tukey honest significant difference (HSD) post hoc test. For the F values obtained, p < 0.05 were considered statistically significant. Three replicates of each sample were used for statistical analysis. All data presented are expressed as means
± SD.
RESULTS AND DISCUSSION
Antioxidant activity
Antioxidant activity of plant materials can be analysed, and can be attributed to various reported mechanisms. Generally, two modes of action, such as single electron transfer and hydrogen atom transfer have been described.9 Therefore, in this research, the antioxidant activities of different parts of twelve Ficus species were analysed by two most common in vitro assays, namely DPPH and ABTS. Their results were expressed
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7 by different methods, such as percentage of inhibition (%) and trolox equivalent antioxidant capacity (mg TE /g DL), shown in Figure 1-3 and Table 1.
In the maceration extraction, the percentages of inhibition and trolox equivalent antioxidant capacity of different parts of twelve (12) Ficus species were analysed in DPPH assay and ranged from 7.33 ± 0.86 to 91.48 ± 0.88 % and 3.16 ± 0.36 to 37.84
± 0.36 mgTE/g DL respectively for leaves (Figure 1 and Table 1), 15.45 ± 0.92 to 91.46
± 0.75 % and 6.51 ± 0.38 to 37.83 ± 0.31 mgTE/g DB respectively for barks (Figure 2 and Table 1) and 8.82 ± 1.55 to 92.78 ± 1.25 % and 3.78 ± 0.64 to 38.38 ± 0.52 mgTE/g DF respectively for fruits (Figure 3). On the other hand, in the extraction through ultrasound, these values range from 8.15 ± 0.78 to 94.49 ± 0.81 % and 5.35 ± 0.31 to 39.19 ± 0.32 mgTE/g DL respectively for leaves (Figure 1 and Table 1), 20.22 ± 0.89 to 94.47 ± 0.90 % and 10.08 ± 0.35 to 39.18 ± 0.35 mgTE/g DB respectively for barks (Figure 2 and Table 1) and 2.36 ± 0.88 to 94.58 ± 0.88 % and 3.08 ± 0.34 to 39.23 ± 0.34 mgTE/g DF respectively for fruits (Figure 3 and Table 1). In ultrasound- assisted extraction (UAE), most of the parts of Ficus sp. showed higher percentages of inhibition and trolox equivalent antioxidant capacity than the maceration extraction, shown in Table 1. The highest antioxidant activity were observed in the leaves of ‘F.
auriculata Lour’ and ‘F. microcarpa’, but were the lowest in the leaves of F. aurata Miq.
From the ANOVA and Tukey’s post hoc analysis, it was revealed that there was no significant statistical difference between the leaves of ‘F. auriculata Lour’ and ‘F.
microcarpa L.f’ (P< 0.05) (Table 1). In case of barks, the highest antioxidant activity were detected in ‘F. deltoidea Jack’ and ‘F. racemose L’, but were lowest in the barks of F. carica L. On the other hand, the highest antioxidant activity were found in the fruits of ‘F. grossularioides Burm. f ’ and ‘F. fistulosa Reinw. ex Blume’, but were the lowest in the fruits of ‘F. carica L ’. These results are supported by other studies, where solvent systems, extraction process and drying temperatures could affect the recovery of phenolic compounds and antioxidant activity. However, it was been reported that non-antioxidant compounds may also interfere the antioxidant activity,21 which also needs to be taken into consideration.
The ABTS free radical scavenging method is another important assay for analysing antioxidant activity. In ABTS assay, the percentages of inhibition of different parts of twelve (12) Ficus species were analysed, and the values ranged from 17.31 ± 1.86 %
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8 to 99.25 ± 0.56 % and 7.44 ± 0.92 to 99.66 ± 0.37, respectively, for maceration and ultrasonication extraction (Figure 4 - 6). The Trolox equivalent antioxidant capacity (TEAC) varied from 5.45± 0.52 to 28.56 ± 0.16 and 2.11 ± 0.27 to 29.18 ± 0.11 mg TE/
g DP, respectively, for maceration and ultrasonication extraction, and are shown in Figure 4 – 6. The highest trolox equivalent antioxidant activity was detected in the leaves of F. auriculata Lour (29.18 ± 0.16 mg TE/ g DL), followed by F. fistulosa Reinw.
ex Blume fruits (29.16 ± 0.18 mg TE/ g DF), F. grossularioides Burm.f fruits (29.15 ± 0.19 mg TE/ g DF), F. microcarpa L.f. leaves (29.14 ± 0.21 mg TE/ g DL), F. benjamina L leaves (29.14 ± 0.14 mg TE/ g DL) and F. racemosa L. barks (29.12 ± 0.19 mg TE/
g DB). On the other hand, the lowest values was obtained from the fruits of F. aurata Miq (2.11 ± 0.27 mg TE/ g DF) (Table 1).
The DPPH and ABTS+ assays of our studied species showed favourable results with previous studies reported for Southwest China native Ficus species,6 African Ficus species2, Indian Ficus sp.8 leaf extract of F. carica L and F. elastica Roxb. ex Hornem
19, leaf extract of F. auriculata Lour5, root extract of F. racemosa L22 and the bark, fruits and leaf extracts of F. microcarpa L.f23.
Total phenol content
The phenolic content of the twelve Ficus species obtained by ultrasound and maceration extraction process is shown in Table-2. In the extraction of phenolic compounds of the Ficus species, using the UAE method obtained higher phenolic content, which ranged from 1.04 ± 0.19 to 25.21 ± 0.45 mg GAE/gm for leaves (Figure 7 and Table 2 ), 1.70 ± 0.23 to 19.21 ± 0.24 mg GAE/gm DL for barks (Figure 8) and 0.42 ± 0.10 to 27.03 ± 0.53 mg GAE/gm DL for fruits (Figure 9). On the other hand, the TPC content extracted by maceration varied from 1.42 ± 0.23 to 20.43 ± 0.64 mg GAE/gm for leaves, 1.06 ± 0.26 to 14.83 ± 0.63 mg GAE/gm DL for barks and 0.44 ± 0.17 to 22.29 ± 0.69 mg GAE/gm DL for fruits. Therefore, at the studied environments, higher phenolic content was observed for most of the parts of Ficus species through the use of ultrasound extraction. When the total phenol content of each part was compared with others parts studied in the Ficus species, the fruits extract of F. fistulosa Reinw. ex Blume (27.03 ± 0.53 mg GAE/g DL) was found to be highest in content (p˂
0.05), followed by leaf extracts of F. microcarpa L.f. and F. fistulosa Reinw. ex Blume with total polyphenol content of 25.21 ± 0.45 and 23.89 ± 0.44 mg GEA/g DL,
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9 respectively. The fruit extract with the lowest phenol content were F. carica L , F.
aurata Miq and F. benjamina L, with a total phenolic content of 0.64 ± 0.17, 0.59 ± 0.11 and 0.42 ± 0.10 mg GAE/g dry leaves, respectively. One-way ANOVA and Tukey’s HSD post hoc revealed that there was no significant variance between ‘F.
fistulosa Reinw. ex Blume’ fruits and ‘F. microcarpa’ leaves (Table 2) in both the total phenolic content and antioxidant activity as described previously.
Numerous researchers reported the total phenolic content for the fruits,8-10 leaves2, 7,
19, 24 and various others parts13, 14 of the Ficus species. However, the leaves exhibited higher phenolic content and antioxidant capacity in comparison to others parts.15 The results obtained in this study can be supported by previous studies, where the phenolic content is equivalent or higher. It was observed that total phenolic content of the extract from F. fistulosa Reinw. ex Blume and F. microcarpa L.f. species were lower than the leaf extracts of the Egyptian Ficus sp.,7 leaves extract of F. lutea (56.85 ± 1.82 mg GEA/g DL); fruit extract of Ficus maclellandii (26.41 mg GAE/g DF); Tunisian fig cultivars, 25,26 and Algerian fig cultivars 24. However, our studied TPC content was also higher than the seven Southwest China native Ficus species;6 African nine Ficus species 2; Indian Ficus sp.8, leaf extract of F. carica L and F. elastic,19 as well as the six commercial fig cultivars10, Croatian fig cultivars27 and Albanian fig cultivars.28 The values are also comparable to those of the leaf extracts of F. auriculata Lour,5 root extracts of F. racemosa L. 22 and the bark, fruits and leaf extracts of F. microcarpa.23 From the TPC value listed previously, we can easily consider that the leaf of F.
auriculata Lour; fruits of F. grossularioides Burm. f; barks of F. elastic and F. racemosa L. as well as the whole plants of F. fistulosa Reinw. ex Blume and F. microcarpa L.f.
are good sources of phenolic compounds. In this sense, F. fistulosa Reinw. ex Blume and F. microcarpa L.f. were the most interesting species.
Yields of the extract
The yield of extract obtained for ultrasound assisted extraction and maceration extraction of Ficus species are shown in Figure 10-12 and Table 2. In ultrasound assisted extraction, the percentages of yields were calculated and ranged from 1.72 ± 0.15 to 8.63 ± 0.19 % and 1.55 ± 0.15 to 11.77 ± 0.21 %, respectively, for maceration and ultrasonication extraction, where the fruit extracts of F. fistulosa Reinw. ex Blume had the highest yield (11.77± 0.21 %), followed by F. grossularioides Burm.f fruits
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10 (11.08 ± 0.30 %). On the other hand, the bark extracts of F. carica L (1.55 ± 0.15%) and F. aurata Miq had the lowest yields (1.72 ± 0.21%). The percentages of yields of our studied leaf extracts were higher than those reported by Olaokun and co (2013), where they obtained leaf extract percentages of F. lutea (3.70%), F. polita (3.15%), F.
natalensis (2.35%) and F. capreifolia (2.32%).2 A lower yield can also be observed from Manian el al. (2008), in their study with methanolic aerial roots extract of F.
bengalensis and the stem bark of F. racemose L,9 as well as in the work conducted by Mahmoudi et al. (2016) with ten cultivars of F. carica L .24 The extraction yield using UAE yielded a higher percentage compared to the maceration extraction for most of the Ficus species extraction. The higher yield of extract in ultrasound assisted extraction is due to the ultrasound disrupting the cell walls and rapidly releasing cell content.29
Cluster analysis
The hierarchical cluster analysis is useful in solving classification problems. In our study, the objective of using cluster analysis was to reveal clusters based on the antioxidant activity and total phenolic content. In case of antioxidant activity, two main clusters can be distinguished at euclidean distances of about 4.0 (Figure 13a). The upper portion of the cluster includes 22 different parts of Ficus species, while bottom portion of the cluster contains residual 12 parts of Ficus species, which indicated the least amount of antioxidant activity. However, upper portions of the cluster was divided into further three groups. The parts that exhibited the most antioxidant activity were placed in the upper group of the first cluster. The second and third parts with the most antioxidant activity were placed in the next groups of the first cluster. All the parts of F. auriculata Lour, F. deltoidea Jack, F. fistulosa Reinw. ex Blume and F. microcarpa L.f. showed the highest antioxidant activity and at distances of about 4.0. The bottom portion of the cluster contained species F. aurata Miq, F. carica L and F. hispida L.f, which showed the lowest antioxidant activity. Some parts of the other species exhibited the higher antioxidant activity in both the DPPH and ABTS methods. The highest total phenolic contents were detected in both the leaves and fruits of F.
fistulosa Reinw. ex Blume and leaves of F. macrocarpa L.f, which were placed in same cluster, and the lowest were F. aurata Miq, F. carica L and F. hispida L.f. While 26 parts of Ficus sp. were placed in the upper site of TPC dendogram, this cluster showed lowest phenolic content and include ‘F. aurata Miq’, ‘F. carica L ’ ‘F. hispida L.f’ and
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11
‘F. religeosa’ species (Figure 13b), as observed in antioxidant activity measured by both using the scavenging method.
Correlation analysis
The correlation analysis between ABTS, DPPH, and total phenolic contents of Ficus species were displayed in Figure 14. A positive relationship (p< 0.05) was found between maceration DPPH assay and ultrasonic DPPH (r= 0.97), maceration ABTS (r= 0.95), and the ultrasonic ABTS (r= 0.57). Another significant correlation was observed between the maceration DPPH and maceration total phenolic content (TPC), and the ultrasonic TPC, but with poor r-values (r= 0.73 and 0.75 respectively). These significant correlations suggests that the outcomes of 73% and 75% of the DPPH scavenging capacity of Ficus species may be due to the involvement of phenolic compounds. The remaining percentage may also come from others antioxidant compounds such as volatile oils, amino acids, vitamins and others, which are not limited to phenolics30. Moreover, a significant correlation between ABTS and TPC contents, indicated that phenolic compounds may also contribute to the ABTS radical scavenging assay in Ficus sp. Several studies have previously reported the significant positive relationship between total phenolic content and antioxidant activity.31 Therefore, the present study showed that Ficus species are by-products with strong radical scavengers and can be considered as good sources of natural antioxidants for food applications, amongst others.
CONCLUSIONS
Ultrasound-assisted extraction (UAE) is a new, simple, and economical extraction process. This was used to extract antioxidants from different parts of twelve Ficus species and compared with the maceration extraction method. Based on the antioxidant activity, phenolic content and yield of extract, it can be summarised that the extracts obtained by UAE process showed potent antioxidant activity, and may be related to their phenolic content. Fruits of F. grossularioides Burm. f showed the highest antioxidant activity in both extraction methods and free radical scavenging assays, followed by the fruits of F. fistulosa Reinw. ex Blume, which exhibited the highest phenolic contents and yield of extract in both the extraction process.
Therefore, the leaves of F. auriculata Lour; fruits of F. grossularioides Burm. f; barks
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12 of F. elastic and F. racemosa L. as well as the whole plants of F. fistulosa Reinw. ex Blume and F. microcarpa L.f could be potential sources of antioxidants from a natural origin that could be significant contribution as a therapeutic agent (in preventing or slowing oxidative stress and chronic related disorders), as well as for food applications (as antioxidant additives). Therefore, the Ficus species with the highest antioxidant activity could be desirable to be used in in vitro and in vivo studies to elucidate their mode of action as antioxidant. Furthermore, these species can be potential candidates for further phytochemical and pharmacological studies to isolate and identify secondary metabolites correlated to antiradical activity or other bioactivities.
ACKNOWLEDGEMENTS
The authors would like to thank Universiti Kebangsaan Malaysia for its financial support to this research work under the grant LIV-2015-04. The authors would also like to thank SAF FA FIG GARDEN to provide sample.
Conflicts of interest: No conflict of interest was declared by the authors.
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239-245.
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31. Ghasemzadeh A, Jaafar HZ, Juraimi AS, et al. Comparative evaluation of different extraction techniques and solvents for the assay of phytochemicals and antioxidant activity of Hashemi Rice Bran. Molecules, 2015, 20(6): 10822-10838.
uncorrected
proof
Figure 1. The percentages of inhibitions and TEAC of leaves of Ficus species in DPPH method.
Figure 2. The percentages of inhibitions and TEAC of barks of Ficus species in DPPH method.
0 5 10 15 20 25 30 35 40
0 10 20 30 40 50 60 70 80 90 100
TEAC (mg TE /g DL)
DPPH scavenging capacity (%)
Leaves of Ficus speceies
Maceration extraction Ultrasonication extraction a
h
b
g d
c
f g
a ab
e ab
g g g
ab b ab a ab
c d
e f
0 5 10 15 20 25 30 35 40
0 10 20 30 40 50 60 70 80 90 100
TEAC (mg TE /g DB)
DPPH scavenging capacity (%)
Barks of Ficus speceies
Maceration extraction Ultrasonication extraction a
a ab
d c c b
e f
h
g
b a
ab abc bc
cd cd cd
d
e
g f
h
uncorrected
proof
Figure 3. The percentages of inhibitions and TEAC of fruits of Ficus species in DPPH method.
Figure 4. The percentages of inhibitions and TEAC of leaves of Ficus species in ABTS method.
0 4 8 12 16 20 24 28
0 10 2030 40 50 60 7080 90 100
TEAC (mg TE /g DL)
ABTS scavenging capacity (%)
Leaves of Ficus speceies
Maceration extraction Ultrasonication extraction
a a ab
ab ab b c
de d e
f g
a a a a a a a
b b
c c
d 0 5 10 15 20 25 30 35 40
0 10 20 30 40 50 60 70 80 90 100
TEAC (mg TE /g DF)
DPPH scavenging capacity (%)
Fruits of Ficus speceies
Maceration extraction Ultrasonication extraction
a a a a
b
c
de ef f d
a a a
b
c d
e f
f g
uncorrected
proof
Figure 5. The percentages of inhibitions and TEAC of barks of Ficus species in ABTS method.
Figure 6. The percentages of inhibitions and TEAC of fruits of Ficus species in ABTS method.
0 4 8 12 16 20 24 28
0 10 20 30 40 50 60 70 80 90 100
TEAC (mg TE /g DB)
ABTS scavenging capacity (%)
Barks of Ficus speceies
Maceration extraction Ultrasonication extraction
a a ab a
ab b d c
d
e f
g
a a
a a ab
ab ab b
c
d e e
0 4 8 12 16 20 24 28
0 10 20 30 40 50 60 70 80 90 100
TEAC (mg TE /g DF)
ABTS scavenging capacity (%)
Fruits of Ficus speceies
Maceration extraction Ultrasonication extraction
b a a ab
c c
d
e e
f
a a a a a
b
c c d
e
uncorrected
proof
Figure 7. Total phenolic contents of leaves of Ficus species in maceration and UAE extraction.
Figure 8. Total phenolic contents of barks of Ficus species in maceration and UAE extraction.
0 5 10 15 20 25
TPC (mg GAE/g)
Leaves of Ficus speceies Maceration Ultrasonication
hi
a b b
d c
e
e f f
f f f
b a c
e d
f g
h j ij hij
0 4 8 12 16 20
TPC (mg GAE/g)
Barks of Ficus speceies Maceration Ultrasonication
a bc b
c d d
e e e
f f f
a
b c
d d
e
f g g f
h h
uncorrected
proof
Figure 9. Total phenolic contents of fruits of Ficus species in maceration and UAE extraction.
Figure 10. Percentages of yields of leaves of Ficus species in maceration and UAE extraction.
0 5 10 15 20 25 30
TPC (mg GAE/g)
Fruits of Ficus speceies Maceration Ultrasonication
a
b
d d c
e f f
f f
a
c d b d
f e
f f f
0 2 4 6 8 10 12
Percentages of yields (%)
Leaves of Ficus speceies Maceration Ultrasonication
a b
bc c bc
d d
e
e e e
f
b c
de d e
f f
g g g
h a
uncorrected
proof
Figure 11. Percentages of yields of barks of Ficus species in maceration and UAE extraction.
Figure 12. Percentages of yields of fruits of Ficus species in maceration and UAE extraction.
0 2 4 6 8 10
Percentages of yields (%)
Barks of Ficus speceies Maceration Ultrasonication
a b c
c cd
d
e e e
e e e
a b c c
d
e e
f f g
h h
0 2 4 6 8 10 12
Percentages of yields (%)
Fruits of Ficus speceies Maceration Ultrasonication
a
b b
c
d d
de e e
f
a a
b b
c d d
e
f f
uncorrected
proof
(a)
Rescaled Distance Cluster Combine C A S E 0 5 10 15 20 25 Name of species parts Num +---+---+---+---+---+ F. racemosa leaves 11 ─┐ F. microcarpa fruits 33 ─┤ F. fistulosa leaves 7 ─┤ F. benjamina leaves 3 ─┤ F. microcarpa barks 22 ─┤ F. elastica barks 18 ─┤ F. fistulosa barks 19 ─┼─┐ F. auriculata fruits 26 ─┤│ F. fistulosa fruits 30 ─┤│ F. grossularioides fruits 31 ─┤│ F. microcarpa leaves 10 ─┤│ F. racemosa barks 23 ─┤├───┐ F. auriculata leaves 2 ─┤│ │ F. deltoidea barks 17 ─┘│ │ F. elastica leaves 6 ─┐│ │ F. benjamina barks 15 ─┤│ ├─────────────────────────────────────────┐ F. religeosa barks 24 ─┼─┘ │ │ F. auriculata barks 14 ─┘ │ │ F. grossularioides barks 20 ─┐ │ │ F. racemosa fruits 34 ─┤ │ │ F. deltoidea leaves 5 ─┼─────┘ │ F. deltoidea fruits 29 ─┘ │ F. benjamina fruits 27 ─┐ │ F. hispida fruits 32 ─┤ │ F. aurata fruits 25 ─┼───┐ │ F. carica fruits 28 ─┘ │ │ F. grossularioides leaves 8 ─┐ ├───────────────────────────────────────────┘ F. hispida leaves 9 ─┤ │ F. aurata leaves 1 ─┼───┘ F. religeosa leaves 12 ─┤ F. aurata barks 13 ─┤ F. carica leaves 4 ─┤ F. carica barks 16 ─┤ F.hispidabarks21─┘
uncorrected
proof
(b)
Figure 13. Dendrogram of Ficus species based on (a) antioxidant activity and (b) total phenolic content.
Rescaled Distance Cluster Combine C A S E 0 5 10 15 20 25 Name of species parts Num +---+---+---+---+---+ F. aurata fruits 25 ─┐ F. benjamina fruits 27 ─┤ F. carica fruits 28 ─┤ F. grossularioides leaves 8 ─┼─┐ F. religeosa leaves 12 ─┤│ F. aurata barks 13 ─┤│ F. hispida leaves 9 ─┤│ F. hispida fruits 32 ─┤├───────────────────┐ F. aurata leaves 1 ─┤│ │ F. carica barks 16 ─┤│ │ F. carica leaves 4 ─┘│ │ F. grossularioides barks 20 ─┬─┘ │ F. hispida barks 21 ─┘ │ F. auriculata fruits 26 ─┐ ├─────────────────────────┐ F. racemosa fruits 34 ─┤ │ │ F. auriculata barks 14 ─┼─────┐ │ │ F. microcarpa fruits 33 ─┤ │ │ │ F. deltoidea leaves 5 ─┤ │ │ │ F. elastica leaves 6 ─┤ │ │ │ F. deltoidea fruits 29 ─┘ ├───────────────┘ │ F. racemosa leaves 11 ─┐ │ │ F. fistulosa barks 19 ─┼─┐ │ │ F. benjamina leaves 3 ─┤│ │ │ F. benjamina barks 15 ─┤├───┘ │ F. deltoidea barks 17 ─┘│ │ F. religeosa barks 24 ───┘ │ F. fistulosa leaves 7 ─┬─┐ │ F. fistulosa fruits 30 ─┘├───────┐ │ F. microcarpa leaves 10 ───┘ ├─────────────────────────────────────┘ F. auriculata leaves 2 ─┬───┐ │ F. microcarpa barks 22 ─┘ ├─────┘ F. elastica barks 18 ─┐ │ F. racemosa barks 23 ─┼───┘ F. grossularioides fruits 31 ─┘
uncorrected
proof
Figure 14. Pearson Product- Moment correlation matrix of the studied parameters (P <0.05).
Pearson Product-Moment Correlations
DPPH-MAC
DPPH-MAC
DPPH-ULT
DPPH-ULT
ABTS-MAC
ABTS-MAC
ABTS-ULT
ABTS-ULT
TPC-MAC
TPC-MAC
TPC-ULT
TPC-ULT
0.97 0.95 0.57 0.73 0.75
0.97 0.94 0.58 0.71 0.75
0.95 0.94 0.61 0.66 0.69
0.57 0.58 0.61 0.42 0.46
0.73 0.71 0.66 0.42 0.97
0.75 0.75 0.69 0.46 0.97
-1.0 1.0
uncorrected
proof
Table 1. Antioxidant activity of different parts of Ficus species in different extraction process
Name of Ficus species
DPPH radical scavenging capacity ABTS radical scavenging capacity
Maceration Ultrasonication Maceration Ultrasonication
Inhibition (%) TEAC
(mg TE/g DP*) Inhibition (%) TEAC
(mg TE/g DP*) Inhibition (%) TEAC
(mg TE/g DP*) Inhibition (%) TEAC (mg TE/g DP*) Leaves
F. aurata Miq. 7.33 ± 0.86h 3.16 ± 0.36h 8.15 ± 0.78g 5.35 ± 0.31g 47.21 ± 1.15f 13.88 ± 0.32f 50.30 ± 1.18b 14.69 ± 0.35b F. auriculata Lour. 91.48 ± 0.88a 37.84 ± 0.36a 93.78 ± 0.83ab 38.91 ± 0.33ab 98.30 ± 1.33ab 28.29 ± 0.37ab 99.66 ± 0.55a 29.18 ± 0.16a F. benjamina L. 87.76 ± 1.05b 36.31 ± 0.43b 91.81 ± 1.02b 38.14 ± 0.40b 97.83 ± 1.32ab 28.16 ± 0.37ab 99.52 ± 0.66a 29.14 ± 0.19a F. carica L. 16.11 ± 1.25g 6.78 ± 0.52g 25.07 ± 0.81e 11.98 ± 0.32e 41.27 ± 1.09g 12.20 ± 0.31g 51.58 ± 0.82b 15.07 ± 0.24b F. deltoidea Jack. 61.86 ± 1.09d 25.64 ± 0.45d 64.14 ± 0.95d 27.29 ± 0.37d 95.79 ± 0.70b 27.58 ± 0.20b 97.48 ± 0.83a 28.54 ± 0.24a F. elastic Roxb. ex Hornem. 74.45 ± 1.07c 30.82 ± 0.44c 85.11 ± 1.06c 35.52 ± 0.42c 92.44 ± 1.21c 26.64 ± 0.34c 98.14 ± 1.32a 28.73 ± 0.39a F. fistulosa Reinw. ex Blume. 88.58 ± 0.90ab 36.64 ± 0.37ab 92.54 ± 0.72ab 38.43 ± 0.28ab 98.91± 0.88a 28.46 ± 0.25a 99.17 ± 0.63a 29.04 ± 0.19a F. grossularioides Burm. f. 21.64 ± 0.79f 9.06 ± 0.32f 9.18 ± 0.82g 5.75 ± 0.32g 52.34 ± 1.08de 15.32 ± 0.30de 39.99 ± 1.23c 11.67 ± 0.36c F. hispida L.f. 15.36 ± 0.73g 6.47 ± 0.30g 9.25 ± 0.85g 5.78 ± 0.34g 53.99 ± 1.06d 15.79 ± 0.30d 39.92 ± 1.42c 11.65 ± 0.42c F. macrocarpa L.f 90.78 ± 1.40a 37.55 ± 0.58a 94.49 ± 0.81a 39.19 ± 0.32a 98.98 ± 0.73a 28.48 ± 0.21a 99.53 ± 0.71a 29.14 ± 0.21a F. racemose L 89.83 ± 0.94ab 37.16 ± 0.39ab 92.79 ± 1.12ab 38.52 ± 0.44ab 98.18 ± 0.67ab 28.25 ± 0.19ab 98.93 ± 0.69a 28.97 ± 0.20a F. religeosa L. 28.52 ± 1.37e 11.89 ± 0.56e 18.70 ± 1.17f 9.48 ± 0.46f 50.34 ± 0.74e 14.76 ± 0.21e 32.77 ± 0.81d 9.55 ± 0.24d Barks
F. aurata Miq. 38.61 ± 0.73f 16.06 ± 0.30f 26.88 ± 0.84g 12.69 ± 0.33g 54.50 ± 1.23e 15.93 ± 0.35e 44.47 ± 1.08e 12.98 ± 0.32e F. auriculata Lour. 79.48 ± 1.22c 32.89 ± 0.50c 87.30 ± 1.29d 36.37 ± 0.50d 86.54 ± 0.79d 24.97 ± 0.22d 98.55 ± 0.73ab 28.85 ± 0.21ab F. benjamina L. 77.14 ± 1.00c 31.93 ± 0.41c 90.07 ± 0.81cd 37.46 ± 0.32cd 97.07 ± 1.09ab 27.94 ± 0.31ab 99.00 ± 0.64a 28.99 ± 0.19a F. carica L. 15.45 ± 0.92h 6.51 ± 0.38h 20.22 ± 0.89h 10.08 ± 0.35h 40.52 ± 1.05g 11.99 ± 0.30g 44.43 ± 1.01e 12.97 ± 0.30e F. deltoidea Jack. 91.26 ± 0.89a 37.75 ± 0.37a 93.94 ± 0.96ab 38.98 ± 0.38ab 98.98 ± 0.82a 28.48 ± 0.23a 99.42 ± 0.57a 29.11 ± 0.17a F. elastic Roxb. ex Hornem. 87.61 ± 1.17b 36.25 ± 0.48b 91.82 ± 0.97abc 38.14 ± 0.38abc 96.04 ± 0.84b 27.65 ± 0.24b 98.58 ± 0.63ab 28.86 ± 0.18ab F. fistulosa Reinw. ex Blume. 91.46 ± 0.75a 37.83 ± 0.31a 89.83 ± 0.96cd 37.37 ± 0.37cd 99.20 ± 0.84a 28.54 ± 0.24a 96.69 ± 1.04b 28.31 ± 0.31b
uncorrected
proof
F. grossularioides Burm. f. 55.08 ± 1.58e 22.84 ± 0.65e 58.53 ± 1.04e 25.10 ± 0.41e 88.68 ± 1.91d 25.58 ± 0.54d 92.65 ± 0.69c 27.12 ± 0.20c F. hispida L.f. 25.03 ± 1.21g 10.46 ± 0.50g 34.33 ± 0.97f 15.61 ± 0.38f 49.44 ± 0.79f 14.51 ± 0.22f 57.39 ± 1.01d 16.77 ± 0.30d F. macrocarpa L.f 86.95 ± 1.33b 35.97 ± 0.55b 91.11 ± 1.27bc 37.87 ± 0.50bc 98.40 ± 0.89ab 28.32 ± 0.25ab 98.99 ± 0.64a 28.98 ± 0.19a F. racemose L 90.31 ± 1.51ab 37.36 ± 0.62ab 94.47 ± 0.90a 39.18 ± 0.35a 98.95 ± 0.53a 28.47 ± 0.15a 99.47 ± 0.64a 29.12 ± 0.19a F. religeosa L. 67.50 ± 1.04d 27.96 ± 0.43d 89.52 ± 1.16cd 37.24 ± 0.45cd 92.90 ± 0.64c 26.77 ± 0.18c 98.92 ± 0.59ab 28.96 ± 0.17ab Fruits
F. aurata Miq. 14.01 ± 1.13de 5.92 ± 0.46de 6.75 ± 0.91f 4.80 ± 0.36f 17.31 ± 1.86e 5.45 ± 0.52e 7.44 ± 0.92f 2.11 ± 0.27f F. auriculata Lour. 91.29 ± 0.94a 37.76 ± 0.39a 89.40 ± 0.83b 37.20 ± 0.32b 98.46 ± 0.85a 28.33 ± 0.24a 96.47 ± 0.83b 28.24 ± 0.24b F. benjamina L. 11.33 ± 0.76ef 4.81 ± 0.31ef 2.36 ± 0.88g 3.08 ± 0.34g 23.90 ± 1.10c 7.30 ± 0.31c 13.27 ± 0.96e 3.82 ± 0.28e F. carica L. 8.82 ± 1.55f 3.78 ± 0.64f 11.84 ± 0.78e 6.79 ± 0.31e 26.42 ± 1.15c 8.01 ± 0.32c 31.12 ± 0.71d 9.06 ± 0.21d F. deltoidea Jack. 81.50 ± 0.91b 33.73 ± 0.37b 49.69 ± 0.82d 21.63 ± 0.32d 99.08 ± 0.61a 28.51 ± 0.17a 91.50 ± 1.46c 26.78 ± 0.43c F. fistulosa Reinw. ex Blume. 92.40 ± 0.96a 38.22 ± 0.39a 94.25 ± 1.27a 39.10 ± 0.50a 97.66 ± 0.88a 28.11 ± 0.25a 99.58 ± 0.62a 29.16 ± 0.18a F. grossularioides Burm. f. 92.78 ± 1.25a 38.38 ± 0.52a 94.58 ± 0.88a 39.23 ± 0.34a 99.25 ± 0.56a 28.56 ± 0.16a 99.57 ± 0.66a 29.15 ± 0.19a F. hispida L.f. 15.11 ± 0.88d 6.37 ± 0.36d 6.87 ± 1.00f 4.85 ± 0.39f 20.27 ± 0.90d 6.28 ± 0.25d 13.67 ± 1.49e 3.94 ± 0.44e F. macrocarpa L.f 89.94 ± 0.74a 37.21 ± 0.30a 92.54 ± 1.31a 38.43 ± 0.51a 98.01 ± 0.84a 28.21 ± 0.24a 98.94 ± 0.68ab 28.97 ± 0.20ab F. racemose L. 59.39 ± 0.95c 24.62 ± 0.39c 61.54 ± 1.03c 26.28 ± 0.41c 81.22 ± 0.75b 23.47 ± 0.21b 90.59 ± 0.74c 26.52 ± 0.22c
*DP: Dry Parts (DL: Dry Leaves; DB: Dry Barks; DF: Dry Fruits)
uncorrected
proof
Table 2. Total phenolic content and yields of extract of different parts of Ficus species in different extraction process.
Name of Ficus species Total phenolic content
(mg GAE/gm DP*) Yields of extract (%)
Maceration Ultrasonication Maceration Ultrasonication
Leaves
F. aurata Miq. 1.63 ± 0.41f 1.98 ± 0.14hi 3.83 ± 0.18f 5.16 ± 0.20g F. auriculata Lour. 14.67 ± 0.47b 19.28 ± 0.53c 6.88 ± 0.21bc 10.88 ± 0.16b F. benjamina L. 8.12 ± 0.33d 10.02 ± 0.39e 4.47 ± 0.19e 8.16 ± 0.17e F. carica L. 1.54 ± 0.33f 2.28 ± 0.21h 5.16 ± 0.18d 6.88 ± 0.19f F. deltoidea Jack. 4.47 ± 0.52e 6.61 ± 0.30f 6.53 ± 0.19c 8.76 ± 0.28de F. elastic Roxb. ex
Hornem. 4.88 ± 0.43e 5.66 ± 0.17g 6.88 ± 0.23bc 9.04 ± 0.20d
F. fistulosa Reinw. ex
Blume. 20.43 ± 0.64a 23.89 ± 0.44b 7.88 ± 0.19a 11.48 ± 0.22a
F. grossularioides Burm. f. 2.48 ± 0.41f 1.04 ± 0.19j 4.47 ± 0.11e 5.16 ± 0.26g F. hispida L.f. 1.42 ± 0.23f 1.33 ± 0.17ij 4.44 ± 0.20e 5.16 ± 0.21g F. macrocarpa L.f 15.79 ± 0.69b 25.21 ± 0.45a 7.22 ± 0.21b 10.16 ± 0.20c F. racemose L 9.64 ± 0.55c 11.16 ± 0.27d 4.49 ± 0.16e 6.88 ± 0.19f F. religeosa L. 2.30 ± 0.19f 1.82 ± 0.26jij 5.16 ± 0.23d 3.72 ± 0.16h Barks
F. aurata Miq. 3.32 ± 0.35e 2.24 ± 0.18h 2.06 ± 0.15e 1.72 ± 0.21h F. auriculata Lour. 3.53 ± 0.34e 5.34 ± 0.16f 2.26 ± 0.21e 5.16 ± 0.16e F. benjamina L. 7.24 ± 0.19d 9.58 ± 0.34e 4.82 ± 0.23d 6.88 ± 0.15d F. carica L. 1.47 ± 0.20f 1.70 ± 0.23h 2.58 ± 0.25e 1.55 ± 0.15h F. deltoidea Jack. 6.63 ± 0.46d 10.40 ± 0.50d 5.44 ± 0.27c 7.88 ± 0.11c
uncorrected
proof
F. elastic Roxb. ex
Hornem. 9.79 ± 0.42c 15.96 ± 0.30b 6.19 ± 0.13b 8.25 ± 0.15c
F. fistulosa Reinw. ex
Blume. 10.72 ± 0.52bc 10.36 ± 0.25d 5.50 ± 0.12c 4.82 ± 0.12e
F. grossularioides Burm. f. 1.06 ± 0.26f 4.39 ± 0.19g 2.06 ± 0.18e 2.82 ± 0.30g F. hispida L.f. 1.08 ± 0.15f 3.81 ± 0.18g 2.58 ± 0.15e 3.96 ± 0.14f F. macrocarpa L.f 14.83 ± 0.63a 19.21 ± 0.24a 7.23 ± 0.21a 9.78 ± 0.23a F. racemose L 11.34 ± 0.46b 15.20 ± 0.23c 5.16 ± 0.17cd 9.02 ± 0.21b F. religeosa L. 3.03 ± 0.13e 5.21 ± 0.21f 2.44 ± 0.18e 3.99 ± 0.19f Fruits
F. aurata Miq. 0.75 ± 0.20f 0.59 ± 0.11f 3.75 ± 0.15de 2.40 ± 0.23f F. auriculata Lour. 6.85 ± 0.30c 6.29 ± 0.25d 3.16 ± 0.21e 5.83 ± 0.24c F. benjamina L. 0.71 ± 0.15f 0.42 ± 0.10f 5.50 ± 0.19c 4.84 ± 0.26d F. carica L. 0.44 ± 0.17f 0.64 ± 0.17f 4.30 ± 0.14d 3.44 ± 0.25e F. deltoidea Jack. 5.59 ± 0.22d 4.31 ± 0.19e 7.60 ± 0.21b 7.22 ± 0.17b F. fistulosa Reinw. ex
Blume. 22.29 ± 0.69a 27.03 ± 0.53a 8.63 ± 0.19a 11.77 ± 0.21a
F. grossularioides Burm. f. 8.10 ± 0.21b 14.92 ± 0.40b 7.61 ± 0.32b 11.08 ± 0.30a F. hispida L.f. 1.13 ± 0.20f 0.95 ± 0.19f 3.44 ± 0.33e 2.24 ± 0.19f F. macrocarpa L.f 3.37 ± 0.15e 5.91 ± 0.22d 1.72 ± 0.15f 5.16 ± 0.19d F. racemose L. 5.69 ± 0.20d 7.67 ± 0.19c 4.13 ± 0.19d 6.76 ± 0.18b
*DP: Dry Parts (DL: Dry Leaves; DB: Dry Barks; DF: Dry Fruits)
