A Review of the Phytochemical Compounds and Pharmacological Activities from Selected Ficus Plants

Insanu M; Santoso F R C; Fidrianny I

doi:https://doi.org/10.26452/ijrps.v11iSPL4.4225

A Review of the Phytochemical Compounds and Pharmacological Activities from Selected Ficus Plants

Insanu M ✉ ¹ , Santoso F R C ¹ , Fidrianny I ¹

1 Department of Pharmaceutical Biology, School of Pharmacy, Bandung Institute of Technology, Bandung-40132, Indonesia, +62-222504852

Abstract

The Ficus genus belongs to the Moraceae family were used for medicinal purposes. Distributed in America, Asia, Africa, and Australia, there were sixteen species accepted in Indonesia. They were Ficus callosa, Ficus melinocarpa, Ficus elastica, Ficus drupaceae, Ficus geocarpa, Ficus Superba, Ficus heteropoda, Ficus fistulosa, Ficus hirta, Ficus ampelas, Ficus adenosperma, Ficus ardisioides, Ficus consociate, Ficus ribes, Ficus lyrata, Ficus virens Aiton. This article reviewed the scientific work of the Ficus genus. Their traditional usage, phytochemical compounds, and pharmacological activity were summarized. This study aims at providing a collection of publications on selected species of Ficus genus. A critical review of the literature data revealed secondary metabolite like triterpenoid, steroid, saponin, flavonoid, phenolic compound and alkaloid were found in some species of Ficus. Some pure compounds such as quercetin, quercetin 3-O-α-L-arabinopyranoside, epilupeol acetate, oleanolic acid, friedelin, elastiquinone, pinocembrin-7-O-β-D-glucoside, and ficusoside B were isolated. A wide range of pharmacological activities was observed. Antimicrobial, antioxidant, antiviral, antiparasitic, cytotoxic, and antimalarial were found in previous researches. Ficus genus was potential to be developed as a medicinal plant.

Keywords

Ficus, Moraceae, Traditional, Phytochemical

Introduction

Family Moraceae consists of over 50 genera and nearly 1400 species distributed in the tropical and subtropical region as American, Asia, Afrika, and Australia (Zerega, Clement, Datwyler, & Weiblen, 2005). Ficus is one large family plant comprises of over 800 species (Herre, Jandér, & Machado, 2008) and one of about 40 genera of mulberry family Moraceae (Hamed, 2011). Twenty-two species were recorded in Indonesian, among which 16 are accepted name and six synonyms, which are all deciduous plants, and most are essentially hemi-epiphytic. Ficus plant species can be edible food and traditional medicine to improve the human health of about ten thousand years. Several species used were recorded in Ayurvedic and traditional Chinese medicine (Lansky, Paavilainen, Pawlus, & Newman, 2008). People who live at Xishuangbanna in Southwest China consumed Ficus leaves as wild vegetables by the ethnic group. Ficus have many edible species such as Ficus virens Ait var. sublanceolata (Miq.) Corner, Ficus auriculata Lour., Ficus vasculosa Wall ex Miq., Ficus callosa Willd, Ficus virens Ait var. verins, Ficus racemosa L. and Ficus oligodon Miq (Shi, Xu, Hu, Na, & Wang, 2011).

Table 1: Traditional uses of Ficus genus in Pakistan

Ficus species	Local name	Plant Part	Traditional uses
F. elastica	rabber plant	bark, fruits and leaves	Enlargement of liver and spleen, dysentery, diarrhea, diabetes, leprosy, lung complaints, leucorrhoea, heart diseases, cough, asthma, piles, ulcers, gonorrhea, rheumatism and for different skin diseases	(Nisar et al., 2014; Teinkela et al., 2018)
F. lyrata	beeri patta	whole plant	Gastrointestinal problems, anthelmintic, diabetes, anti- tumor activity, asthma, cough, sexual disorders, diarrhea, ear-ache and toothache, migraine, eye troubles, scabies, gonorrhea, bleeding, paralysis, bone fracture, antiseptic and astringent	(Nisar et al., 2014).
F. virens	jangli pipit	leaves, fruit and bark	Diabetes, ulcer, menstrual disorder, leucorrhea	(Khan et al., 2011)

Table 2: IC₅₀ from various extracts of Ficus species

Ficus species	Plant Part	Extract	IC₅₀	Ref.
F. carica	Leaves	Water	76.38 mg/ml	(Wahyuni & Hertiani, 2016).
	Leaves	Methanol	275.23 µg/ml	(Ayoub, Hassan, Hamid, Abdelhamid, & Souad, 2019)
	Fruits	Water	33.38 mg/ml	(Wahyuni et al., 2016).
F. pareintalis	Leaves	Water	44.01 mg/ml	(Wahyuni et al., 2016).
F. pareintalis	Fruits	Water	35.69 mg/ml	(Wahyuni et al., 2016).
F. deltoidea	Leaves	Methanol	111.2 µg/ml	(Misbah, Aziz, & Aminudin, 2013).
F. deltoidea	Leaves	Ethanol	16.5 µg/ml	(Aslam, Sin, Mamat, & Ahmad, 2017)
F. maclellandii	Fruits	Ethanol	210.3 µg/ml	(Tamuly, Buragohain, Hazarika, Bora, & Gajurel, 2015)
F. racemosa	Fruits	Ethanol	228.4 µg/ml	(Tamuly, Buragohain, Hazarika, Bora, & Gajurel, 2015)

Table 3: Antimicrobial activity of Ficus genus

Ficus species	Plant Part	Extract	Bacterial/Fungi
F. callosa	Leaves	Methanol	Escherichia coli, Staphylococcus aureus, Bacillus subtilis	(Wibowo, Kurniati, Wirasutisna, & Insanu, 2018)
F. drupacea	Leaves	Methanol	E. coli, S. aureus, B. subtilis	(Wibowo, Kurniati, Wirasutisna, & Insanu, 2018)
	Stem bark	n-Hexane	Aspergillus flavus, A. versicolor, A. niger, A. ochraceus, Candida albicans, Penicillium funiculosum, P. ochrochloron	(Yessoufou, Elansary, Mahmoud, & Skalicka-Woźniak, 2015)
	Stem bark	n-Hexane	B. cereus, Listeria monocytogenes, Micrococcus flavus, S. aureus, E. coli, Salmonella typhimurium, Pseudomonas aeruginosa, Enterobacter cloacae	(Yessoufou, Elansary, Mahmoud, & Skalicka-Woźniak, 2015)
F. melinocarpa	Leaves	Methanol	S. aureus, B. subtilis	(Wibowo et al., 2018)
F. geocarpa	Leaves	Methanol	E. coli, S. aureus, B. subtilis
F. consociata	Leaves	Methanol	E. coli, S.aureus, B. subtilis
F. ribes	Leaves	Methanol	E. coli, S. aureus, B. subtilis
F. ardisioides	Leaves	Methanol	E. coli, S. aureus, B. subtilis	(Wibowo et al., 2018)
F. heteropoda	Leaves	Methanol	S. aureus, B. subtilis
F. hirta	Leaves	Methanol	S. aureus
F. elastica	Roots	Methanol	S. aureus, E. coli, Proteus vulgaris, Providencia stuartii, P. aeruginosa, C. albicans	(Teinkela et al., 2018)
F. elastica	Root barks	MeOH/ CHCl3	Enterococcus faecalis, S. aureus, S. saprophyticus, S. epidermididis, Trichophyton rubrum, C. albican, E. coli, Klebsiella pneumoniae, and S. typhi	(Mbosso et al., 2012)
F. fistulosa	Leaves	Methanol, Water	E. coli, E. coli mutants, S. aureus, B. subtilis, K. pneumoniae, P. aeruginosae	(Raka, Rahman, & Kaium, 2019)
F. hirta	Fruits	Ethanol	Penicillium italicum	(Wan et al., 2017)
F. lyrata	Latex	Ethyl acetate	C. albicans	(Bidarigh, Khoshkholgh, Massiha, & Issazadeh, 2011)
F. lyrata	Leaves	Ethanol	S. aureus, E. coli, K. pneumonia, P. aeruginosa, methicillin-resistant Staphylococcus aureus, S. pneumoniae	(Tkachenko et al., 2016)
F. carica	Leaves	Ethanol	E. coli, P. aeruginosa, MRSA, S. aureus	(Tkachenko, Buyun, Osadowski, Honcharenko, & Prokopiv, 2017)

Table 4: Cytotoxic activity of isolated compound

Compounds	Tumor cell line (IC₅₀ µg/ml)
Compounds	HeLa	MCF-7	Jurkat	HT-29	T24
Oleanolic acid	20.38 ± 2.6	16.28 ± 1.3	21.17 ± 2.2	25.58 ± 1.3	27.61 ± 1.3
Friedelin	20.42 ± 2.3	22.81 ± 2.1	29.15 ± 2.3	37.21 ± 3.61	12.81 ± 1.4
Epilupeol acetate	15.16 ± 1.6	20.03 ± 3.2	19.64 ± 2.6	26.21 ± 1.7	58.26 ± 2.3

Traditional uses

Several of Ficus plants have been applied in traditional medicine for many countries. Thailand people used fresh young leaves of leab (F. Superba) and phak huead Daeng (F. virens) as a vegetable as a curry or used in a salad (Chantarasuwan & Welzen, 2012). The Ayurveda book recorded that traditional people use bark, latex, leaves and fruit of F. virens Aiton for vertigo, blood diseases, diabetes, rheumatism and antioxidant (Rajani, Anandjiwala, Bagul, & Parabia, 2008). People in Vanuatu used latex from leaves of F. adenosperma for menorrhagia; this plant is added to the coconut water (Bourdy & Walter, 1992). Different from people in Papua New Guinea, used for sores and scabies, but fresh roots of F. adenosperma is chewed to treat malaria (Mahyar, Burley, Gyllenhaal, & Soejarto, 1991). In Vietnam, leaves of F. drupaceae is taken to treat malaria, paragonimiasis, nasosinusitis, sinusitis, and anasarca (Phan et al., 2013). Still, the leaves, roots and bark from F. microcarpa were applied to reduce fever and anti-inflammatory. The usage of Ficus species in Pakistan for traditional medicine can be seen in Table 1.

Many kinds of Ficus have been used in Indonesian culture like leaves of uyah-uyah (F. quercifolia) to treat skin disease in Balinese people. Gayo ethnic used leaves of leng (F. deltoidea) for aphrodisiac like Sundanese people. Another kind of Ficus, fruits of amis Mata (Ficus Montana) is used by Sundanese ethnic to treat urinary stones. Ficus fistulosa leaves also are used to treat wounds by sharp objects and for anthelmintic in Sumba people. The bark of Ficus septic is used for sprue, but the leaves can use for mothers who have just given birth.

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/16c1d01a-9b95-4ce4-bd65-e20a9eb4f930/image/4bf3bcd6-5b6f-4de3-9b06-31b7cf3875b9-upicture1.png — **Figure 1: Structure of chemical compounds isolated from Ficus genus**

Phytochemical compound

Phytochemical screening found that many secondary metabolites such as flavonoid and phenolic compound, p-coumaric acid, caffeic acid, kaemferol, quercetin and leucoanthocyanins frequently occurred in leaves. Triterpenoid (Chiang, Chang, Kuo, Chang, & Kuo, 2005; Chiang, Su, Liu, & Kuo, 2001), steroid, flavonoid (Kiem et al., 2011), lignin (Li & Kuo, 2000), saponin, and alkaloid were known from some species of Ficus (Berg, Corner, & Jarrett, 2006). The structure of some phytochemical compound is shown in Figure 1.

Flavonoid was discovered in all Ficus genus, and several isolates were found from methanol extract of F. callosa leaves as megastigmane glycoside, ficalloside (Van et al., 2011). Quercetin, quercetin-3-O-α-D-arabinopyranoside, quercetin-3-O-β-D- galactopyranoside, kaempferol-3-O-α-D-arabinopyranoside, kaempferol-3-O-β-D- galactopyranoside, and vogelin J. were obtained from methanol extract of F. virens Aiton (Orabi & Orabi, 2016). Other biochemical compounds from stem bark extracts of F. drupaceae included β-amyrin, β -sitosterol-3-O- β-D-glucopyranoside, 5-O-methyllatifolin, oleanolic acid, epifriedelanol, friedelin and epilupeol acetate were isolated and identified (Yessoufou et al., 2015).

Chemical investigation of the ethyl acetate extract of F. consociata leaves led to the isolation and structural elucidation of seven compounds. They were luteolin, cirsiliol, isoquercetin, quercetin 3-O-α-L-arabinopyranoside, nikotoflorin, hesperidin, and (2E,4E,1'S,2'R,4'S,6'R)- dihydrophaseic acid (Dat et al., 2019). Ursolic acid and oleanolic acid were isolated from the dichloromethane extract F. ampelas. Butyrospermol cinnamate and isolation of lutein from leaves of F. ampelas were also exposed (Ragasa, Cuevas, Mandia, Bernardo, & Shen, 2014).

Methanol extract roots of Ficus elastic contained steroidal glucosides called as sitosteryl 3-O-β-D-glucopyranoside, elasticamide, and the highest antimicrobial are elastiquinone, ficusoside B (Teinkela et al., 2018), ficusamide, and elasticoside (Mbosso et al., 2012). Pinocembrin-7-O-β-D-glucoside, in the ethanol extract of F. hirta fruits, had antifungal activity (Wan et al., 2017).

Pharmacological activities

Pharmacological activities of some Ficus species were shown in the explanation below:

Antioxidant Activity

Ethanol extract of young leaves of F. virens Aiton and Ficus callosa had antioxidant activity with DPPH and ABTS assays, which IC₅₀ of DPPH F. virens Aiton was 0.34 mg/ml, and IC₅₀ of ABTS 0.23 mg/ml. It was different with F. callosa, IC₅₀ of DPPH 0.95 mg/ml, and ABTS 0.35 mg/ml. F. virens Aiton had higher flavonoid and phenolic compounds, which correlated with its antioxidant activity (Shi et al., 2011).

Quercetin from methanol leaves extract of F. virens Aiton was the most active DPPH radical scavenging activity with IC₅₀ 14 ± 1.12 µg/ml (Orabi et al., 2016). (Hilfi, 2019), reported that ethanol extract of F. elastic gave antioxidant activity with EC₅₀ DPPH 6.4166 mg/ml and 0.0768 mg/ml with ABTS. Ficuselastic acid and (1'S,6'R)-8-O-β-D- glucopyranosyl abscisate sodium showed antioxidant activity (Kiem et al., 2012). The methanol extract of leaves of Ficus fistulosa presented IC₅₀ DPPH 16.66 µg/ml (Raka et al., 2019).

Some Ficus from other country had antioxidant compounds, such as C-glycosylflavone from ethanolic leaves extract of F. microcarpa (Kiem et al., 2011), and aqueous roots extracts of F. beecheyana (Yen et al., 2018). Philippines peoples used antioxidants from the ethanol extract of leaves and fruits of F. nota (Santiago et al., 2017). F. sur is a traditional medicine from Togo, had antioxidant activity for the whole plant, the highest activity was given by ethanolic bark extract (56.50 ± 0.29 µg QE/mg), and the ripe fruit had lowest activity (7.3 ± 0.30 µg QE/mg) (Saloufou et al., 2018). The old leaves of F. deltoidea had more potent antioxidant activity than the fresh leaves (Manurung, Kustiawan, & Kusuma, 2017). The value of IC₅₀ from other extracts of Ficus species are reported in Table 2.

Antiparasitic Activity

Methanol roots extract of Ficus elastica exhibited antiparasitic activity against Trypanosoma brucei, with IC₅₀ 0.9 µg/mL (Teinkela et al., 2018). The antischistosomal activity was shown by ether latex extract of F. elastica (after washing off toxic rubber materials) (el-Din et al., 2014).

Antimalarial Activity

The methanol extract of F. elastica roots demonstrated plasmocidal activity (IC₅₀ 9.5 µg/ml) against Plasmodium falciparum strain 3D7 (Teinkela et al., 2018).

Antimicrobial Activity

The antimicrobial activity of Ficus species has been evaluated by the agar diffusion method. It can be proposed that flavonoids, triterpenoid, and steroid had antimicrobial activities (Wibowo, Kurniati, Wirasutisna, & Insanu, 2018). Ficus species showed antimicrobial activity against at least one bacteria, which can be seen in Table 3.

Antiviral Activity

Antiviral activity in vitro of flavonoids, which was found from F. virens Aiton on Coxsackie B4 (CVB4), and hepatitis A virus (HAV) were also carried out. Antiviral activities were also given by quercetin and quercetin-3-O-β-D- galactopyranoside isolated from F. virens Aiton. It was tested by 3-(4,5- dimethylthiazol-2-yl)-2,5 diphenyltetrazolium bromide (MTT) assay. Quercetin gave the highest inhibitory activity (20.3%) on CVB4; meanwhile, quercetin-3-O-β-D- galactopyranoside presented the highest inhibitory activity (12.3%) on HAV (Orabi et al., 2016).

F. fistulosa leaves extract showed antiviral activity (IC₅₀ 15.0 µg/ml) against HCV J6/JFH1-P47 strain and HCV J6/JFH1-P1 strain with IC₅₀ 5.7 µg/ml. The chloroform fraction had an anti-HCV activity with IC₅₀ 5.67 ± 1.54 µg/ml, while butanol fraction gave lower activity (IC₅₀ 74.10 ± 18.24 µg/ml) (Hafid et al., 2016). Methanol leaves extract of F. septica had antiviral activity against Dengue virus (DENV-1 and DENV-2) with IC₅₀ 13.3±2.6 µg/ml and 10.6±1.1 µg/ml (Huang et al., 2017).

Cytotoxic Activity

Flavonoid compounds are the secondary metabolites responsible for pharmacological activity in Ficus species. The flavonoid from F. virens Aiton showed low cytotoxic activity in Vero cells by the MTT method (Orabi et al., 2016). The ethanol leaves extract of F. fistulosa had cytotoxicity concentration (CC₅₀) >200 μg/ml, which was not toxic, while butanol and chloroform fractions gave CC₅₀ >100 μg/ml (Hafid et al., 2016). The methanol extract of F. septica root inhibited nasopharyngeal carcinoma (HONE-1) and gastric adenocarcinoma (NUGC) cell (Damu, Kuo, Li, Su, & Wu, 2009) while the ethanolic extract of roots from F. beecheyana inhibited HL-60 cell (Yen et al., 2018).

Ficusamide is an isolated compound from F. elastica that had medium cytotoxic activity on A-549 lung cancer (Mbosso et al., 2012). Other compounds from F. elastica showed weak cytotoxic activity (IC₅₀ values 20 µg/ml) on HeLa cell (Teinkela et al., 2018). Meanwhile, compounds from F. drupacea stem barks demonstrated the highest antiproliferative activities against most cancer cells, are reported in Table 4 (Yessoufou et al., 2015).

Other Pharmacological Activities

Methanol fruit extract of Ficus carica with a concentration of 924 µmol/l reduced 54% the formation of uric acid in mice, which injected with potassium oxonate (Mohamed & Al-Okbi, 2008). F. carica leaves showed oedema inhibitory activity (anti-inflammatory) in rats induced by carrageenan as much as 48.8% (Ali et al., 2012). Previous research demonstrated that ethanolic fruit extract of F. carica could inhibit α-glucosidase, α-amylase, and pancreatic lipase (Mopuri & Islam, 2016).

Conclusions

We summarized the traditional usage, phytochemical compounds, and pharmacological activity of selected Ficus plants. Based on the literature review was reported that most of the species were used as a traditional medicine in Asian countries such as Indonesia, Papua New Guinea, Vietnam, Pakistan, Thailand, and Vanuatu. Some species of the Ficus genus need further research on pharmacological activities, based on mechanisms and chemical contents.

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