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Albizia Adianthifolia: Botany, Medicinal Uses, Phytochemistry, and Pharmacological Properties.

1. Introduction

Albizia adianthifolia (Schumach.) W. Wight is a medium to large tree (Figure 1) which belongs to the plant family Fabaceae and subfamily Mimosoideae. The species is a member of Albizia Durazz., a genus that is recognized worldwide for its high ecological, economical, and medicinal value [1]. Albizia species have been used in folk medicine for the treatment of cough, diarrhoea, insomnia, irritability, rheumatism, stomach ache, tuberculosis, and wounds [2]. Phytochemical studies done on different species of Albizia lead to the isolation of different classes of secondary metabolites, such as saponins, terpenes, alkaloids, and flavonoids [2, 3]. The saponin compounds isolated from the genus Albizia have been reported to possess cancer related activities and other pharmacological properties which include analgesic, anthelmintic, antidysenteric, antihistaminic, anti-inflammatory, antimicrobial, antimutagenic, antiseptic, antispermatogenic, antitumour, anxiolytic, cytotoxic, immunomodulatory, nootropic, and apoptosis inducing properties [3]. According to Louppe et al. (2008) [1], A. adianthifolia is among 13 Albizia species regarded as socially and economically important in tropical Africa as sources of high quality timber, gum, fodder, and herbal medicines. It is, therefore, not surprising that A. adianthifolia is considered as one of the most important African medicinal plants by Iwu [4] and, recently, Van Wyk [5] listed the bark of the species as commercially relevant medicinal and aromatic component of herbal medicines in Kenya and South Africa. Albizia adianthifolia is also included in the book "medicinal plants of South Africa", a photographic guide to the most commonly used plant medicines in the country, including their botany, main traditional uses, and active ingredients. Research by Mander [6] showed that A. adianthifolia is ranked among the most frequently demanded medicinal plants in KwaZulu-Natal province in South Africa. Similarly, Williams et al. (2000, 2001) [7, 8] showed that the bark of the species is commonly traded in medicinal informal markets in Johannesburg, Gauteng province, South Africa. According to Williams et al. (2000) [7], A. adianthifolia was available in more than two-thirds (66%) of herbal medicine informal markets in Johannesburg. About 9050 kg to 10400 kg of A. adianthifolia bark were traded per annum as herbal medicine in 2001 in Gauteng province alone [9] and 21 200 kg traded per annum in KwaZulu-Natal province, South Africa [10-12]. Overcollection of A. adianthifolia bark as herbal medicine in KwaZulu-Natal province, South Africa, and the trade of its bark in informal herbal medicine markets in the country is causing a population decline and was identified as one of the 15 species becoming increasingly scarce in the province by urban herbalists [10, 13]. It is within this context that the current study was carried out aimed at reviewing the botany, medicinal uses, phytochemical, and pharmacological properties of A. adianthifolia so as to provide baseline data required for evaluating the therapeutic potential of the species.

2. Research Methodology

Search for information relevant to the botany, medicinal uses, phytochemical, and pharmacological properties of A. adianthifolia was carried out from October 2017 to May 2018. Online electronic databases including Google Scholar, SciFinder, ScienceDirect, Medline, Pubmed, SCOPUS, EThOS, ProQuest, OATD, and Open-thesis were used to search for relevant literature. Preelectronic literature of conference papers, scientific articles, books, book chapters, dissertations, and theses were carried out at the University of Fort Hare library. The keywords used in the electronic search criteria were "Albizia adianthifolia", synonyms of the plant species "A. chirindensis (Swynn. ex Baker f.) Swynn. ex Steedman, A. ealaensis De Wild., A. fastigiata (E. Mey.) Oliv., A. gummifera auct. non (J. F. Gmel.) C.A. Sm., A. intermedia De Wild. & T. Durand, Inga fastigiata (E. Mey.) Oliv., Mimosa adianthifolia Schumach. and Zygiafastigiata E. Mey.", English common names "flat-crown albizia, rough-bark flat-crown albizia and West African albizia". The following keywords were used in combination with the species name, synonyms, and English common names to search for relevant information: "biological properties", "ethnobotany", "ethnomedicinal uses", "ethnopharmacological properties", "medicinal uses", "pharmacological properties", and "phytochemistry". Publications included in this study were published between 1939 and 2018, including 60 articles published in international journals, books (13), conference, working papers and other scientific publications (eight), book chapters (three), dissertation, and website (one each). Three of the research articles were published before 1970, while four were published between 1970 and 1979, 1980 and 1989 (seven articles), 1990 and 1999 (10), 2000 and 2009 (32), and 2010 and 2010 (30 articles).

3. Botanical Profile and Description of Albizia adianthifolia

Albizia is a large genus comprising about 120 to 140 species that are widely distributed in tropical Africa (including Madagascar), central South America, south east Asia, and Malaysia [14]. The genus name Albizia was first published by Durazzini in 1772 based on a description of A. julibrissin Durazzin grown from seeds imported from Constantinople to Tuscany, Florence, in Italy by Fillippo Degli Albizzi in 1749 [15]. The species name "adianthifolia" refers to the resemblance of the leaves of the species to maidenhair fern, genus Adiantum L., family Pteridaceae [16, 17]. Literature studies revealed the existence of two accepted infraspecifics, A. adianthifolia var. adianthifolia [18, 19] and A. adianthifolia var. intermedia (De Wild. & T. Durand) Villiers [19, 20], and no attempt has been made to provide infraspecific circumscription and geographical distribution of the two varieties. Therefore, A. adianthifolia sensu lato will be used throughout this manuscript. Synonyms of A. adianthifolia include A. chirindensis, A. ealaensis, A. fastigiata, A. gummifera, A. intermedia, Inga fastigiata, Mimosa adianthifolia, and Zygia fastigiata.

Albizia adianthifolia is a medium to large deciduous tree growing up to 35 m in height [16, 21]. The bole is up to 95 cm in diameter and is straight and cylindrical in closed forest but often crooked and/or twisted in more open savannah and bushland localities, usually without buttresses but with small, thick buttresses in forest localities [16]. The bark is yellowish brown to grey, smooth or rough, inner bark granular, creamy to yellowish in colour with clear gum. Albizia adianthifolia has a flattened crown, with large, spreading branches, young branches densely yellowish or reddish pubescent. Leaves are alternate, bipinnately compound with 3 to 10 pairs of pinnae with ovate to lanceolate stipules and leaflets in 5 to 17 pairs per pinna [16, 21]. The inflorescence is an axillary head with bisexual small flowers which are reddish to greenish white in colour. The fruit is an oblong, flat pod, densely but finely pubescent, transversely veined, and pale brown when ripe. The seeds are flattened, swollen, globose in shape and brown in colour [21]. Albizia adianthifolia has been recorded in forests, woodlands, and areas that are transitional to woodland. The species occurs from South Africa through Madagascar, central and east Africa, to Senegal in the north (Figure 2).

The bark of A. adianthifolia is one of the most commonly stocked herbal medicine products in the informal herbal medicine markets in South Africa [7-13] and Grace et al. (2003) [22] tried to authenticate dried bark of the species using thin layer chromatography (TLC). This study showed that dried bark of A. adianthifolia is often confused with dried bark of Acacia sieberiana DC., Acacia xanthophloea Benth. (family Fabaceae), and Croton sylvaticus Hochst. ex C. Krauss (family Euphorbiaceae), other three plant species sold as herbal medicines in the informal herbal medicine markets in South Africa. Grace et al. [22] argued that the notable similarities in the phytochemical fingerprints of Acacia sieberiana, Acacia xanthophloea, A. adianthifolia, and Croton sylvaticus maybe an indicator of close usage relationships as similarities shown by TLC chromatograms may sometimes explain the phytochemical properties common to bark products that are purposefully substituted for one another, particularly in cases where taxonomically unrelated species are used [23].

4. Medicinal Uses of Albizia adianthifolia

The bark, leaf sap, leaves, roots, and stem bark of A. adianthifolia are used as remedies for human and animal diseases (Table 1). Ethnomedicinal uses of the species have been recorded in Burundi, Cameroon, the Democratic Republic of Congo (DRC), Guinea, Madagascar, Guinea-Bissau, Mozambique, Nigeria, Sierra Leone, Rwanda, Swaziland, South Africa, Tanzania, Uganda, Zimbabwe, and Togo, representing 51.6% of the countries where the species is indigenous (Figure 3). Major diseases and ailments recorded in at least two countries include diabetes, eye problems, gastrointestinal problems, haemorrhoids, headache, neurodegenerative disorders, purgative, reproductive problems in women, respiratory problems, wounds and pain, skin diseases, sexually transmitted infections, and ethnoveterinary medicine (Figure 3). Albizia adianthifolia is used to manage and treat top three ailments and diseases regarded by the World Health Organization [24] as the leading causes of death in low-income countries, and these are lower respiratory infections, diarrhoeal diseases, and ischaemic heart disease. The bark, leaves, and stem bark of A. adianthifolia are used as herbal remedies against bronchitis, cough, respiratory problems, and sinusitis in Cameroon, Mozambique, Nigeria, and South Africa [25-29], which can be categorized as the lower respiratory infections. The bark, leaves, and roots of A. adianthifolia are used as herbal remedies against diarrhoea, dysentery, and stomach ache in the DRC, Madagascar, Mozambique, South Africa, and Tanzania [26, 30-36]. The leaves of A. adianthifolia are used as herbal remedies against hypertension in Togo [37], which is one of the most common chronic diseases in modern societies. There is, therefore, a need for further research aimed at correlating some of the ethnomedicinal uses of A. adianthifolia to the phytochemical and biological activities of both the crude extracts and chemical compounds isolated from the species. Moreover, the World Health Organization has recognized the important role played by traditional medicines in the provision of primary healthcare in the resource-poor regions like tropical and subtropical Africa [38]. In addition to this, several studies have demonstrated the efficacy and importance of medicinal plants in the development of new pharmaceutical drugs and health products [39, 40].

Sexually transmitted infections are treated with multitherapeutic applications involving A. adianthifolia herbal concoctions. For example, in Sierra Leone, stem bark of A. adianthifolia is mixed with fruits of Citrus aurantiifolia (Christm.) Swingle and taken orally as herbal medicine for gonorrhoea [41]. In South Africa, the leaves of A. adianthifolia are mixed with the bark of Trichilia dregeana Sond. and taken orally as herbal medicine for syphilis [42]. In the Democratic Republic of Congo, leaves of A. adianthifolia are mixed with those of Gynura scandens O. Hoffm. and fruits of Musa paradisiaca L. and applied topically as herbal medicine for visible blisters on livestock [43].

5. Phytochemistry

To date, about 90 secondary metabolites have been isolated from the heartwood, leaves, roots, root, and stem bark of A. adianthifolia. The isolated phytochemical compounds which included apocarotenoids, dipeptide, elliptosides, essential oils, fatty acids, flavonoids, histamines, imidazolyl carboxylic acids, steroids, triterpene saponins, and triterpenoids were identified and characterized using fast atom bombardment mass spectroscopy (FABMS), gas chromatographymass spectrometry (GC-MS), high performance liquid chromatography (HPLC), high-resolution electrospray ionisation mass spectroscopy (HRESIMS), and nuclear magnetic resonance (NMR) techniques (Table 2). The essential oils, fatty acids, triterpene saponins, flavonoids, and phenolics are considered the most prominent family of phytochemical compounds occurring in A. adianthifolia [27, 28, 63-71]. Research by Akande et al. (2018) [70] revealed that [beta]-caryophyllene 54 (23.0%), E-geranyl acetone 7 (7.4%), acorenone 38 (6.4%), viridiflorol 48 (6.4%), azingiberene 52 (6.3%), and ar-curcumene 51 (4.6%) were the major constituents in the leaf oil, while essential oils 54 (39.3%), selin-11-en-4-a-ol 44 (10.4%), 53 (9.6%), 51 (7.2%), caryophyllene oxide 40 (6.4%), and a-humulene 50 (5.6%) were the major constituents in the stem bark oil and essential oils 54 (32.1%), 44 (13.1%), 41 (8.4%), pentadecanal 28 (6.1%), and 50 (4.4%) were the major constituents in the root bark oil of A. adianthifolia. The gas chromatography-mass spectrometry analyses of n-hexane heartwood extract of A. adianthifolia resulted in the identification of n-hexadecanoic acid 66 (34.9%), stigmasterol 75 (28.6%), oleic acid 68 (6.3%), 24S,5[alpha] stigmast-7-en-3[beta]-ol 76 (4.4%), and chondrillasterol 74 (18.2%), while 9, 12-octadecadienoic acid (Z,Z), methyl ester 64 (17.6%), and trans-13-octadecanoic acid, methyl ester 69 (37.2%) were identified from the chloroform extract [68]. Candy et al. (1978) [64] and Beppe et al. (2014) [28] identified flavonoids 3-methoxyflavanone 70, apigenin 71, and melanoxetin 72 from the heartwood and leaves of A. adianthifolia. Beppe et al. (2014) [28] estimated the total flavonoids in leaves of A. adianthifolia to be 0.53 [+ or -] 0.001 mg rutoside/g lyophilized powder, while the total phenolics in the leaves and stem bark of the species was estimated to be 1.5 to 30.2 [micro]g gallic acid equivalents/g dry weight [27, 28, 69]. Roques et al. (1977) [63] and Haddad et al. (2003, 2004) [66, 67] identified triterpene saponins as major phytochemical compounds in the roots and root bark of A. adianthifolia, and these included 16[alpha]-hydroxy-21[beta] -[(2-hydroxybenzoyl)oxy]-3[beta]-[(O-[beta]-D-xylopyranosyl -(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L -rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77, 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O-[beta]-D -glucopyranosyl-(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]-[beta]-D-glucopyranosyl)oxy]olean -12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl -(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78, 3-O-{O-[alpha]-L-arabinopyranosyl -(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-O-[[beta] -dglucopyranosyl-(1 [right arrow] 2)]- [beta]-d-glucopyranosyl}-21-O- {(2E, 6S)-6-{{4-O-[(2E,6S)-2,6-dimethyl-6-([beta]-D-quinovopyranosyloxy)octa-2,7-dienoyl] -[beta]-d-quinovopyranosyl}oxy}-2-(hy-droxymethyl)-6-methylocta-2,7-dienoyl}acacic acid 28-{Oa-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 79, 21-O-{(2E,6S)-6-{{4-O-[(2E,6S)-2,6-dimethyl-6-([beta] d-quinovopyranosyloxy)octa-2,7-dienoyl]-[beta]-d-quinovopyr-anosyl}oxy} -2-(hydroxymethyl)-6-methylocta-2,7-dienoyl}3-O-{O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-dglucopyranosyl} ester 80, 21-O-{(2E,6S)-6-{{3-O-[(2E,6S)2,6-dimethyl-6-([beta]-d-quinovopyranosyloxy)octa-2,7 -dieno-yl]-[beta]-d-quinovopyranosyl}oxy}-2,6-dimethylocta-2,7-dienoyl}-3-O-{O-[beta]-D-xylopyranosyl -(1 [right arrow] 2)-O-[beta]-d-fucopyran-osyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-dglucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)[beta]-d-glucopyranosyl} ester 81, and 3-O-{O-[alpha]-L-arabinopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 2)]-[beta]-d-glucopyranosyl}-21-O-{(2E,6S)2,6-dimethyl-6-([beta]-d-quinovopyranosyloxy)octa-2,7 -dieno-yl}acacic acid 28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-dglucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)[beta]-d-glucopyranosyl} ester 82 which have been shown to be cytotoxic against a large panel of cancer cells [3, 66]. Further comprehensive studies focusing on chemical constituents of A. adianthifolia and their pharmacological activities are required. Chemical structures of aurantiamide acetate 9, docosanoic acid 65, n-hexadecanoic acid 66, octadecanoic acid 67, oleic acid 68, 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)oxy] -3[beta]-[(O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-Dfucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L -rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77, 16ahydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O-[beta]-D-gluco-pyranosyl -(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl -(1 [right arrow] 6)]--[beta]-D-glucopyranosyl) oxy]-olean12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78, 3-O-{O-[alpha]-L-arabinopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 2)]-[beta]-d-glucopyranosyl}-21-O-{(2E,6S)-6-{{4O-[(2E,6S)-2,6-dimethyl-6-([beta]-D -quinovopyranosyloxy)oc-ta-2,7-dienoyl]-[beta]-d-quinovopyranosyl}oxy}-2-(hydroxymethyl)-6-methylocta-2,7 -dienoyl}acacic acid 28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl -(1 [right arrow] 3)]-Oa-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 79, 21-O-{(2E,6S)-6-{{4-O-[(2E,6S)-2,6-dimethyl-6-([beta]-d-quinovopyranosyloxy)octa-2,7-dienoyl]-[beta]-d-quinovopyranosyl} oxy}-2-(hydroxymethyl)-6-methylocta-2,7-dienoyl}-3-O-{O[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 80, 21-O-{(2E,6S)-6-{{3-O-[(2E,6S)-2,6-dimethyl6-([beta]-d-quinovopyranosyloxy)octa -2,7-dienoyl]- [beta]-d-quinovopyranosyl}oxy}-2,6-dimethylocta-2,7-dienoyl}-3-O-{O-[beta]-D -xylopyranosyl-(1 [right arrow] 2)-O-[beta]- d-fucopyranosyl-(1 [right arrow] 6)-2(acetylamino) -2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 81 and 3-O-{O-[alpha]-L-arabinopyranosyl-(1 [right arrow] 2)O -[beta]-d-fucopyranosyl-(1 [right arrow] 6)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 2)]-[beta]-d-glucopyranosyl}-21-O-{(2E,6S)-2,6-dimethyl-6-([beta]d-quinovopyranosyloxy)octa -2,7-dienoyl}acacic acid 28-{Oa-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 82, acacic acid 3-O-beta-D-xylopyranosyl-(1 [right arrow] 2)-beta-D-fucopyranosyl -(1 [right arrow] 6)-2-acetylamino-2-deoxy-beta-D-glu-copyranoside 84, acacic acid 3-O-(beta-D-xylopyranosyl (1 [right arrow] 2)-beta-D-fucopyranosyl-(1 [right arrow] 6)--[beta-D-glucopyranosyl-(1 [right arrow] 2)] -beta-D-glucopyranosyl)-21-O-(6(S)-2-hydroxym-ethyl-6-methyl-6-O-(beta-D-quinovopyranosyl)-2,7-octadienoyl) ester 85, and lupeol 86 which exhibited pharmacological properties [27, 65-68] are shown in Figure 4.

6. Pharmacological Activities

Over the years, pharmacological studies on A. adianthifolia extracts and compounds extracted from the species showed potent in vitro and in vivo pharmacological activities including acetylcholinesterase enzyme inhibitory [69,72,73], anthelmintic [70, 74], antiamoebic [74], antibacterial [27, 53, 68, 73, 75], antimycobacterial [76], anti-sexually transmitted infections [77], antifungal [27, 68], anti-inflammatory [73, 78], antioxidant [27, 28, 69, 79, 80], anxiolytic and antidepressant [79], cognitive-enhancing [28], haemolytic [66, 81], hypoglycemic and antihyperglycemic [45], immunomodulatory [66], cytotoxicity [77, 80-84].

7. Acetylcholinesterase Enzyme Inhibitory Activities

Risa et al. (2004) [72] evaluated the acetylcholinesterase inhibiting activities of aqueous and ethanol stem bark extracts of A. adianthifolia using thin layer chromatography (TLC) and microtitre plate assays. The aqueous and ethanol extracts yielded 14% and 8% inhibition at 0.1 mg/ml in the microplate assay and the ethanol extract exhibited weak inhibiting zone in the TLC assay [72]. Eldeen et al. (2005) [73] evaluated acetylcholinesterase enzyme inhibitory activities of ethanol and ethyl acetate bark and root extracts of A. adianthifolia using thin layer chromatography (TLC) and microplate assays with galanthamine as the positive control. The extracts exhibited moderate activities with percentage inhibition ranging from 45% to 61% and half maximal inhibitory concentration (I[C.sub.50]) values ranging from 0.4 mg/ml to 1.2 mg/ml; these values were lower than percentage inhibition of 93% and I[C.sub.50] value of 2[micro]M exhibited by the control, galanthamine, at a concentration of 2[micro]M [73]. Sonibare et al. (2017) [69] evaluated the acetylcholinesterase inhibitory activities of methanol, ethyl acetate, chloroform, and n-hexane leaf extracts of A. adianthifolia. All extracts showed activities with I[C.sub.50]values ranging from 10.0 [micro]g/mL to 124.4 [micro]g/mL [69]. The ability of A. adianthifolia extracts to inhibit acetylcholinesterase corroborates the traditional use of the species in the management of memory loss and neurodegenerative disorders in South Africa and Nigeria [32, 51].

8. Anthelmintic Activities

McGaw et al. (2000) [74] evaluated anthelmintic activities of hexane, ethanol, and water leaf extracts of A. adianthifolia on the mortality and reproductive ability of the free-living nematode Caenorhabditis elegans in two different assays. All extracts exhibited activities at both concentrations of 1 mg/ml and 2 mg/ml after two-hour and seven-day incubation periods [74]. Akande et al. (2018) [70] evaluated the anthelmintic activities of essential oils isolated from the leaves, root bark, and stem bark of A. adianthifolia using Eudrilus eugeniae adult earthworm with albendazole as the standard. The time of paralysis and death of Eudrilus eugeniae worms decreased as concentration was increased. The leaf essential oil showed the best activity with time of paralysis and death at 12.6 minutes and 60.2 minutes, respectively, which was higher than 82.8 minutes and 154.6 minutes exhibited by albendazole, the anthelmintic drug [70].

9. Antiamoebic Activities

McGaw et al. (2000) [74] evaluated antiamoebic activities of ethanol and water leaf extracts of A. adianthifolia using microdilution technique against the enteropathogenic Entamoeba histolytica with metronidazole as the positive control. The extracts showed weak activities with I[C.sub.50] value of >5.0 mg/ml which was higher than 0.20 [micro]g/ml exhibited by metronidazole [74].

10. Antibacterial Activities

Van Puyvelde et al. (1983) [53] evaluated antibacterial activities of leaf extracts of A. adianthifolia against Neisseria gonorrhoeae, Neisseria meningitidis, Streptococcus pyogenes, and Staphylococcus aureus using the disk diffusion method. The extracts showed activities against Neisseria gonorrhoeae and Neisseria meningitidis with zone of inhibition ranging from 10 mm to 12 mm [53]. Eldeen et al. (2005) [73] evaluated antibacterial activities of aqueous, ethanol, and ethyl acetate bark and root extracts of A. adianthifolia against Bacillus subtilis, Staphylococcus aureus, Micrococcus luteus, Escherichia coli, and Klebsiella pneumoniae using the disc-diffusion and microdilution assays with neomycin (0.2 mg/ml) as the positive control. Ethanol bark extracts were active against all tested bacteria with minimum inhibitory concentration (MIC) values ranging from 3.13 mg/ml to 6.25 mg/ml, while ethyl acetate bark extract was active against all the pathogens except Klebsiella pneumoniae with MIC values ranging from 6.25 mg/ml to 12.5 mg/ml [73]. Abubakar and Majinda [68] evaluated antibacterial activities of chloroform and n-hexane extracts of heartwood of A. adianthifolia against Escherichia coli, Pseudomonas aeruginosa, Bacillus subtilis and Staphylococcus aureus using the modified agar overlay method with chloramphenicol as the positive control. The n-hexane and chloroform extracts showed the best activities against Escherichia coli with minimum inhibition quantity (MIQ) of 1 [micro]g each while other extracts exhibited moderate activities with MIQ value of 50 [micro]g and chloramphenicol exhibited activities with MIQ values ranging from 0.25 [micro]g to 10 [micro]g [68]. Tchinda et al. (2017) [75] evaluated antibacterial activities of methanol bark and root extracts of A. adianthifolia against Pseudomonas aeruginosa, Klebsiella pneumoniae, Enterobacter aerogenes, Escherichia coli, and Providencia stuartii using the broth microdilution assay. The extracts showed moderate to weak activities against tested pathogens with MIC values ranging from 128 [micro]g/mL to 1024 [micro]g/mL [75].

Tamokou et al. (2012) [27] evaluated the antibacterial activities of ethyl acetate extract, aurantiamide acetate 9, docosanoic acid 65, n-hexadecanoic acid 66, octadecanoic acid 67, oleic acid 68, and lupeol 86 isolated from the stem bark of A. adianthifolia against Enterococcus faecalis, Staphylococcus aureus, Pseudomonas aeruginosa, Escherichia coli, Klebsiella pneumoniae, Proteus mirabilis, Shigella flexneri, and Salmonella typhi using the broth microdilution method with gentamicin as the positive control. The ethyl acetate extract and aurantiamide acetate 9 were active against all the tested pathogens with MIC values ranging from 0.09 mg/ml to 0.78 mg/ml and 0.05 mg/ml to 0.1 mg/ml, respectively [27]. The compound lupeol 86, a mixture of n-hexadecanoic acid and oleic acid 68, and a mixture of compounds docosanoic acid 65, n-hexadecanoic acid 66, and octadecanoic acid 67 were active against Enterococcus faecalis, Staphylococcus aureus, Proteus mirabilis, and Shigella flexneri with MIC values ranging from 0.1 mg/ml to 0.4 mg/ml, 0.05 mg/ml to 0.4 mg/ml, and 0.1 mg/ml to 0.8 mg/ml, respectively. The exhibited minimum bactericidal concentrations (MBC) were 0.39 mg/ml to 1.56 mg/ml for ethyl acetate extract, 0.1 mg/ml to 0.4 mg/ml (n-hexadecanoic acid 66 and oleic acid 68), 0.2 mg/ml to 0.8 mg/ml (docosanoic acid 65, n-hexadecanoic acid 66 and octadecanoic acid 67), 0.2 mg/ml to 0.4 mg/ml (compound lupeol 86), and 0.05 mg/ml to 0.1 mg/ml (aurantiamide acetate 9) [27]. The documented antibacterial activities exhibited by different extracts and compounds isolated from A. adianthifolia corroborate the traditional application of the species as herbal medicine against bacterial infections causing diarrhoea, dysentery, and stomachache in DRC, Madagascar, Mozambique, South Africa, and Tanzania [26, 30-36].

11. Antimycobacterial Activities

Eldeen and Van Staden [76] evaluated the antimycobacterial activities of dichloromethane, ethyl acetate, and ethanol bark and leaf extracts of A. adianthifolia against Mycobacterium aurum A+ using the broth microdilution method. Only the ethanol root extract exhibited moderate activity with MIC value of 6.3 mg/ml [76]. These findings show potential of A. adianthifolia in the treatment and management of respiratory problems such as bronchitis, cough, and sinusitis in Cameroon, Mozambique, Nigeria, and South Africa [25-29].

12. Anti-Sexually Transmitted Infections Activities

Naidoo et al. (2013) [77] evaluated anti-sexually transmitted infections activities of aqueous and dichloromethane and methanol (1:1) bark extracts of A. adianthifolia against Candida albicans, Gardnerella vaginalis, Neisseria gonorrhoeae, Oligella ureolytica, Trichomonas vaginalis, and Ureaplasma urealyticum using the microtitre plate dilution method with ciprofloxacin and amphotericin B as positive controls. The anti-sexually transmitted infections interaction of A. adianthifolia used in combination with Trichilia dregeana was determined by calculating the sum of the fractional inhibitory concentrations ([SIGMA]FIC) against Oligella ureolytica. The extracts exhibited activities with MIC values ranging from 0.3 mg/mL to >16.0 mg/mL with average MIC value of 6.3 mg/mL while the controls, ciprofloxacin (0.01 mg/mL) and amphotericin B (0.1 mg/mL), exhibited MIC values of 0.04 [micro]g/mL to 0.6 [micro]g/mL and 2.5 [micro]g/mL, respectively [77]. The combination of A. adianthifolia with Trichilia dregeana resulted in MIC values ranging from 0.8 mg/mL to > 16.0 mg/mL while [SIGMA]FIC values ranged from 0.2 to 0.5, implying synergistic effects irrespective of the ratio at which these two species were combined, thus supporting the traditional method of mixing the two species as herbal medicine for syphilis in South Africa [42].

13. Antifungal Activities

Abubakar and Majinda [68] evaluated antifungal activities of chloroform and n-hexane extracts of heartwood of A. adianthifolia against Candida albicans using the modified agar overlay method with miconazole as the positive control. The extracts exhibited weak activities with MIQ value of >100 [micro]g which was much higher than MIQ value of 0.25 [micro]g exhibited by miconazole [68]. Similarly, Tamokou et al. (2012) [27] evaluated the antifungal activities of ethyl acetate extract and compounds aurantiamide acetate 9, docosanoic acid 65, n-hexadecanoic acid 66, octadecanoic acid 67, oleic acid 68, and lupeol 86 isolated from the stem bark of A. adianthifolia against Candida albicans, Candida parapsilosis, Candida lusitaniae, Candida tropicalis, Candida krusei, Candida glabrata, and Cryptococcus neoformans using the broth microdilution method with nystatin as the positive control. The ethyl acetate extract and aurantiamide acetate 9 were active against all the tested pathogens with MIC values ranging from 0.4 mg/ml to 6.3 mg/ml and 0.01 mg/ml to 0.05 mg/ml, respectively [27]. The compound lupeol 86 was active against Candida albicans, Candida parapsilosis, Candida lusitaniae, Candida krusei, and Cryptococcus neoformans with MIC values ranging from 0.1 mg/ml to 0.4 mg/ml. A mixture of n-hexadecanoic acid 66 and oleic acid 68, and a mixture of docosanoic acid 65, n-hexadecanoic acid 66, and octadecanoic acid 67 were active against Candida albicans, Candida lusitaniae, Candida tropicalis, and Cryptococcus neoformans with MIC values ranging from 0.1 mg/ml to 0.4 mg/ml. The exhibited minimum fungicidal concentration (MFC) values were 0.8 mg/ml to 6.3 mg/ml for ethyl acetate extract, 0.8 mg/ml (compounds n-hexadecanoic acid 66 and oleic acid 68), 0.2 mg/ml to 0.8 mg/ml (docosanoic acid 65, n-hexadecanoic acid 66 and octadecanoic acid 67), 0.2 mg/ml to 0.4 mg/ml (lupeol 86), and 0.006 mg/ml to 0.05 mg/ml (aurantiamide acetate 9) [27].

14. Anti-Inflammatory Activities

Jager et al. (1996) [78] evaluated anti-inflammatory activities of aqueous and ethanolic bark extracts of A. adianthifolia in an in vitro assay for cyclooxygenase inhibitors with indomethacin (0.5 [micro]g) as the control. The ethanolic extract of A. adianthifolia showed an inhibition of 69% which was higher than 66.5% inhibition exhibited by the indomethacin control. Based on these results, there might be a rationale for the ethnopharmacological claim that A. adianthifolia possess anti-inflammatory properties [78]. Similarly, Eldeen et al. (2005) [73] evaluated anti-inflammatory activities of aqueous, ethanol, and ethyl acetate bark and root extracts of A. adianthifolia using the cyclooxygenase (COX-1 and COX-2) assays. Aqueous, ethanol, and ethyl acetate bark and root extracts were active against COX-1 with inhibition percentage ranging from 61% to 90% while bark and root ethyl acetate, ethanol, and aqueous bark extracts were active against COX-2 with inhibition percentage ranging from 58% to 87% [73]. These finding support the traditional use of A. adianthifolia as herbal medicine for abdominal pains, back pain (lumbago), and anal wounds in Cameroon, Guinea-Bissau, and Mozambique [27, 36, 50, 60].

15. Antioxidant Activities

Beppe et al. (2014) [28] evaluated the antioxidant activities of aqueous leaf extracts of A. adianthifolia using the 1, 1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging assay. The DPPH method showed total antioxidant activities of 58.2% [28]. Sonibare et al. (2017) [69] evaluated the antioxidant activities of methanol, ethyl acetate, chloroform, and n-hexane leaf extracts of A. adianthifolia using DPPH free radical scavenging activity assay. All the extracts showed activities with I[C.sub.50] values ranging from 55.8 [micro]g/mL to 232.2 [micro]g/mL [69]. Tamokou et al. (2012) [27] evaluated the antioxidant activities of ethyl acetate extract and compounds aurantiamide acetate 9 and lupeol 86 isolated from the stem bark of A. adianthifolia using the DPPH free radical scavenging and trolox equivalent antioxidant capacity (TEAC) assays. Both with the DPPH and TEAC methods, compound 10 showed activities with half maximal effective concentration (E[C.sub.50]) value of 9.5 [micro]g/mL and TEAC value of 78.8 [micro]g/mL showed the highest antioxidant activity while ethyl acetate extract exhibited E[C.sub.50] value of 70.1 [micro]g/mL and TEAC value of 46.7 [micro]g/mL [27]. Beppe et al. (2015) [79] evaluated the antioxidant activity of aqueous leaf extracts of A. adianthifolia using superoxide dismutase, glutathione peroxidase and catalase specific activities, the total content of the reduced glutathione, protein carbonyl, and malondialdehyde levels. The increased activities of superoxide dismutase, glutathione peroxidase, catalase, and glutathione level and the decreased levels of protein carbonyl and malondialdehyde induced by administration of the aqueous extract of A. adianthifolia leaves implied that this plant extract possesses strong antioxidant property [79]. Sulaiman et al. (2017) [80] evaluated the antioxidant activities of magnetic iron oxide nanoparticles synthesized using A. adianthifolia leaf extracts by using the DPPH free radical scavenging assay. The free radical scavenging potential of the magnetic iron oxide nanoparticles was confirmed based on its stable antioxidant effects [80].

16. Anxiolytic and Antidepressant Activities

Beppe et al. (2015) [79] evaluated the anxiolytic and antidepressant activities of aqueous leaf extracts of A. adianthifolia in the amygdala of 6-hydroxydopamine treated rats model of Parkinson's disease. The extract was administered orally to male Wistar rats at 150 mg/kg and 300 mg/kg daily for 21 days and anxiety and depression were assessed using elevated plus-maze and forced swimming tests. Administration of the extract resulted in anxiolytic and antidepressant-like effects which included a decrease of the exploratory activities, the percentage of the time spent, and the number of entries in the open arm within elevated plus-maze tests and decrease of swimming time and increase of immobility time within forced swimming test [79].

17. Cognitive-Enhancing Activities

Beppe et al. (2014) [28] evaluated the cognitive-enhancing activities of aqueous leaf extracts of A. adianthifolia in the 6-hydroxydopamine-lesion rodent model of Parkinson's disease. The extract was administered orally to male Wistar rats at 150 mg/kg and 300 mg/kg daily for 21 days and spatial memory performance was assessed using y-maze and radial arm-maze tasks. The 6-hydroxydopamine-treated rats exhibited a decrease of spontaneous alternations percentage within y-maze task and an increase of working memory errors and reference memory errors within radial arm-maze task. Administration of the aqueous extract of A. adianthifolia leaves significantly improved these parameters, suggesting positive effects on spatial memory formation [28].

18. Haemolytic Activities

Haddad et al. (2003) [66] evaluated the haemolytic activities of the crude saponin mixture, compounds 84, 85, and 78 isolated from the roots of A. adianthifolia using the haemolysis assay against sheep erythrocytes. The crude saponin mixture exhibited good haemolytic activities with half maximal haemolytic concentration (HC50) value of 12 [micro]g/mL, while compounds 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl) oxy] -3[beta]-[(O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-Larabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]O-[alpha] -L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77 and 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta] -[(O[beta]-D-glucopyranosyl-(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]-[beta]-D-glucopyranosyl)oxy] olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl -(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78 exhibited activities with H[D.sub.50] values of 17.5 [micro]g/mL and 48 [micro]g/mL, respectively [66]. Similarly, Haddad et al. [81] evaluated the haemolytic activities of compounds 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)oxy] -3[beta]-[(O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl -(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77, 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O-[beta]-D-glucopy- ranosyl-(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta] -D-fucopyranosyl-(1 [right arrow] 6)]-[beta]-D-glucopyranosyl)oxy]-olean-12en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-Dglucopyranosyl -(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 78, and 21-O-{(2E,6S)-6-{{4-O-[(2E, 6S)-2,6-dimethyl-6-([beta]-d-quinovopyranosyloxy)octa-2,7-dienoyl] -[beta]-d-quinovopyranosyl} oxy}-2-(hydroxymethyl) -6methylocta-2,7-dienoyl}-3-O-{O-[beta]-D-xylopyranosyl -(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha] -L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 80 isolated from the roots of A. adianthifolia using the haemolysis assay against sheep erythrocytes. The compounds 16[alpha]-hydroxy21[beta]-[(2-hydroxybenzoyl) oxy]-3[beta]-[(O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6) -2-(acetylamino)-2-deoxy-[beta]-D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77, 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]3[beta]-[(O-[beta]-D-glucopyranosyl -(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]--[beta]-D-glucopyranosyl)oxy] -olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl -(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78, and 21-O-{(2E,6S)-6 -{{4-O-[(2E,6S)-2,6-dimethyl-6-([beta]-d-quinovo-pyranosyloxy)octa-2,7-dienoyl] -[beta]-d-quinovopyranosyl}oxy}2-(hydroxymethyl)-6-methylocta-2,7-dienoyl}-3-O-{O-[beta] -D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-2 -(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28-{Oa-L-arabinofuranosyl -(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 80 exhibited haemolytic activities with H[C.sub.50] values ranging from 12.5 [micro]g/mL to 36.6 [micro]g/mL [81].

19. Hypoglycemic and Antihyperglycemic Activities

Amuri et al. (2017) [45] evaluated the hypoglycemic and antihyperglycemic activities of leaf extracts of A. adianthifolia by administering 500 mg/kg to guinea pigs (Cavia porcellus), both in glucose baseline conditions and in oral glucose tolerance test with follow-up over 210 minutes. In hypoglycemic tests, the extract induced activities, lowering the normal glycemia by 33% which was comparable to the activities of the positive control, and glibenclamide (6 mg/kg) which induced a blood glucose lowering effect of 55%. In oral glucose tolerance test, the extract was active, causing inhibition of glycemia increase of 57% which was comparable to the hyperglycemic inhibition rate of glibenclamide of 50% [45]. These findings support the traditional use of A. adianthifolia leaf and stem bark decoction as herbal medicine for diabetes in the DRC [45] and Nigeria [29].

20. Immunomodulatory Activities

Haddad et al. (2003) [66] evaluated the immunomodulatory activities of the crude saponin mixture, compounds acacic acid 3-O-beta-D-xylopyranosyl-(1 [right arrow] 2)-beta-D-fucopyranosyl -(1 [right arrow] 6)-2-acetylamino-2-deoxy-beta-D-glucopyranoside 84, acacic acid 3-O-(beta-D-xylopyranosyl-(1 [right arrow] 2)-beta -D-fucopyranosyl-(1 [right arrow] 6)-[beta-D-glucopyranosyl -(1 [right arrow] 2)]-beta-D-glucopyranosyl)-21-O-(6(S)-2-hydroxymethyl -6-methyl6-O-(beta-D-quinovopyranosyl)-2,7-octadienoyl) ester 85, and 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta] -[(O-[beta]D-glucopyranosyl-(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]--[beta]-D-glucopyranosyl) oxy] olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)] -O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78 isolated from the roots of A. adianthifolia using an in vitro lymphocyte proliferation assay. The cellular proliferation was measured by 3H-thymidine incorporation in Jurkat tumor cell lines (human T cell leukemia). The compounds acacic acid 3-Obeta-D-xylopyranosyl -(1 [right arrow] 2)-beta-D-fucopyranosyl-(1 [right arrow] 6)-2-acetylamino -2-deoxy-beta-D-glucopyranoside 84 and acacic acid 3-O-(beta-D-xylopyranosyl -(1 [right arrow] 2)-beta-D-fucopyranosyl-(1 [right arrow] 6)-[beta-D-glucopyranosyl -(1 [right arrow] 2)]-b eta-D-gluglucopyranosyl)-21-O-(6(S)-2-hydroxymethyl-6-methyl -6O-(beta-D-quinovopyranosyl)-2,7-octadienoyl) ester 85 exhibited a dose-dependent immunomodulatory effect in the concentration range of 0.01 [micro]M to 10 [micro]M, whereas compound 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O[beta] -D-glucopyranosyl-(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]-[beta]-D-glucopyranosyl)oxy] olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl -(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78 showed a lymphoproliferative activity in the concentration range of 0.01 [micro]M to 10 [micro]M [66].

21. Cytotoxicity Activities

Naidoo et al. (2013) [77] evaluated cytotoxicity activities of aqueous and dichloromethane and methanol (1:1) bark extracts of A. adianthifolia using the 3-[4,5-dimethyl-2-thiazol-yl]-2,5-diphenyl2H-tetrazolium bromide (MTT) cellular viability assay on the human embryonic kidney epithelial (Graham, HEK-293) cell line. The cell viability assay indicated that the extracts were nontoxic at 100 mg/ml against the human kidney epithelial cell line, but 110% and 112% cell growth exhibited by aqueous and organic extracts, respectively, appeared to increase cellular activity, which would be effective in wound healing [77]. Kuete et al. (2016) [84] evaluated the cytotoxicity activities of methanol bark and root extracts of A. adianthifolia against the sensitive leukemia CCRF-CEM cells. The extracts were further tested on a panel of eight human cancer cell lines, including MDR phenotypes. In the preliminary assay using CCRF-CEM cells, the bark and root extracts exhibited activities with I[C.sub.50] values of 0.98 [micro]g/mL and 1.5 [micro]g/mL, respectively. Both bark and root extracts were active against other cell lines and normal AML12 hepatocytes with I[C.sub.50] values ranging from 2.7 [micro]g/mL to 10.8 [micro]g/mL towards glioblastoma U87MG.[DELTA]EGFR cells, breast adenocarcinoma MDA-MB-231-BCRP cells, and colon carcinoma HCT116([p53.sup.-/-]) cells. The root extracts induced apoptosis in CCRF-CEM cells through caspases activation and loss of mitochondrial membrane potential [84]. Sulaiman et al. (2017) [80] evaluated the cytotoxic activities of magnetic iron oxide nanoparticles synthesized using A. adianthifolia leaf extracts on human breast (AMJ-13) and (MCF-7) cancer cells. The observed antiproliferative effects towards AMJ-13 and MCF-7 are due to cell death and inducing apoptosis. Mitochondrial membrane potential and acridine orange-propidium iodide staining assays as well as single cell and DNA gel electrophoresis analyses indicated that magnetic iron oxide nanoparticles induce cell death only by apoptosis [80].

Gengan et al. (2013) [82] evaluated cytotoxic activities of silver nanoparticles (AgNP) synthesized from aqueous leaf extracts of A. adianthifolia on the A549 human lung cancer cell line and normal healthy human peripheral lymphocytes using MTT, ATP, and lactate dehydrogenase assays. Viability data for A549 cells showed a 21% (10 [micro]g/ml) and 73% (50 [micro]g/ml) cell viability after 6 hours exposure to AgNPs compared to 117% (10 [micro]g/ml) and 109% (50 [micro]g/ml) cell viability of normal peripheral lymphocytes [82]. Govender et al. (2013) [83] evaluated the cytotoxicity activities of silver nanoparticles (AgNP) synthesized from aqueous leaf extracts of A. adianthifolia on A549 lung cells. Cell viability was determined by the MTT assay by determining cellular oxidative status, lipid peroxidation and glutathione levels, ATP concentration, caspase-3/-7, caspase-8, and caspase-9 activities, apoptosis, mitochondrial membrane depolarization (flow cytometry) and DNA fragmentation, and CD95 receptors, p53, bax, PARP-1, and smac/DIABLO [83]. The silver nanoparticles of A. adianthifolia caused a dose-dependent decrease in cell viability with a significant increase in lipid peroxidation, decreased intracellular lipid peroxidation and glutathione, decrease in cellular ATP, elevation in mitochondria depolarization, higher apoptosis, decline in expression of CD95 receptors, reduction in caspase-8 activity, and increases in caspase-3/-7 and caspase-9 activities; western blots showed increased expression ofsmac/DIABLO and increased expression of p53, bax, and PARP-1 [83]. Haddad et al. (2004) [81] evaluated the cytotoxic activities of compounds acacic acid 3-O-beta-D-xylopyranosyl-(1 [right arrow] 2)-beta-D-fucopyranosyl-(1 [right arrow] 6)-2-acetylamino-2-deoxy-beta-D-glucopyranoside 84, acacic acid 3-O-(beta-D-xylopyranosyl-(1 [right arrow] 2)-beta-D-fucopyranosyl-(1 [right arrow] 6)-[beta -D-glucopyranosyl-(1 [right arrow] 2)]-beta-D-glucopyranosyl)-21-O-(6(S)-2-hydroxymethyl -6-methyl-6-O(beta-D-quinovopyranosyl)-2,7-octadienoyl) ester 85, 16ahydroxy-21[beta]-[(2-hydroxybenzoyl)oxy]-3[beta]-[(O-[beta]-D-xylopy-ranosyl -(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77, 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O-[beta] -D-glucopyranosyl-(1 [right arrow] 2)-O-[O-[beta]-Dxylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]-[beta]-D-glucopyranosyl)oxy]-olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-Oa-L-rhamnopyranosyl -(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78, and 21-O-{(2E,6S)-6-||4-O-[(2E,6S)-2,6-dimethyl-6-([beta]-dquinovopyranosyloxy)octa -2,7-dienoyl]-[beta]-d-quinovopyran-osyl}oxy}-2-(hydroxymethyl)-6-methylocta-2,7-dienoyl} -3O-{O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 80 isolated from the roots of A. adianthifolia on human leukemia T-cells (Jurkat cells) and on splenocytes. The compounds 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)oxy]-3[beta]-[(O-[beta]-D-xylopyranosyl -(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-Dglucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-Oa-L-rhamnopyranosyl -(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77, 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O-[beta]-Dglucopyranosyl-(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)]--[beta]-D-glucopyranosyl) oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78, and 21-O-|(2E,6S)6-{{4-O-[(2E,6S)-2,6-dimethyl-6-([beta]-d-quinovopyranosyl-oxy)octa -2,7-dienoyl]-[beta]-d-quinovopyranosyl}oxy}-2-(hydroxymethyl)-6-methylocta-2,7-dienoyl}-3-O-{O-[beta]-D-xylo-pyranosyl -(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl-(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl}acacic acid 28-{O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 80 exhibited cytotoxic activities on Jurkat cells, while the compounds acacic acid 3-O-beta-D-xylopyranosyl-(1>2)-beta-D-fucopyranosyl-(1 [right arrow] 6)-2 -acetylamino-2-deoxy-beta-D-glucopyranoside 84 and acacic acid 3-O-(beta-Dxylopyranosyl-(1 [right arrow] 2) -beta-D-fucopyranosyl-(1 [right arrow] 6)-[beta-D-glucopyranosyl-(1 [right arrow] 2)] -beta-D-glucopyranosyl)-21-O-(6(S)-2- hydroxymethyl-6-methyl-6-O-(beta-D-quinovopyranosyl)-2,7-octadienoyl) ester 85 exhibited lymphoproliferative activities on this cell type. Cytotoxic activity on Jurkat cells was observed at 10-1 [micro]M and 1 [micro]M for compound 21-O-{(2E,6S)-6-{{4-O-[(2E,6S)-2,6-dimethyl-6 -([beta]-d-quinovo-pyranosyloxy)octa-2,7-dienoyl]-[beta]-d-quinovopyranosyl}oxy}2-(hydroxymethyl) -6-methylocta-2,7-dienoyl}-3-O-{O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-d-fucopyranosyl -(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-d-glucopyranosyl} acacic acid 28-{O-[alpha]L -arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-d-glucopyranosyl-(1 [right arrow] 3)]O-[alpha] -L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-d-glucopyranosyl} ester 80 and at 1 [micro]M for compounds 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl) oxy] -3[beta]-[(O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O[beta]-D-fucopyranosyl -(1 [right arrow] 6)-2-(acetylamino)-2-deoxy-[beta]-Dglucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)-O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)] -O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)-[beta]-D-glucopyranosyl ester 77 and 16[alpha]-hydroxy-21[beta]-[(2-hydroxybenzoyl)-oxy]-3[beta]-[(O-[beta]D-glucopyranosyl -(1 [right arrow] 2)-O-[O-[beta]-D-xylopyranosyl-(1 [right arrow] 2)-O-[beta]-D-fucopyranosyl-(1 [right arrow] 6)] -[beta]-D-glucopyranosyl)oxy]olean-12-en-28-oic acid 28-O-[alpha]-L-arabinofuranosyl-(1 [right arrow] 4)O-[[beta]-D-glucopyranosyl-(1 [right arrow] 3)]-O-[alpha]-L-rhamnopyranosyl-(1 [right arrow] 2)[beta]-D-glucopyranosyl ester 78 [81].

22. Conclusion

Albizia adianthifolia has been used as herbal medicine in tropical Africa for several centuries and significant breakthrough has been made in the last 40 years elucidating the phytochemical and pharmacological properties of the species. However, there are still some research gaps regarding correlating the ethnomedicinal applications of the species with the chemical compounds and pharmacological properties of the compounds and extracts of the species. Detailed studies on the pharmacokinetics, in vivo, and clinical research involving compounds isolated from A. adianthifolia and extracts of the species are required. The bark of A. adianthifolia is known to be toxic [25] and roots of the species are used as fish poison in Mozambique [85]. Similarly, in southern Cameroon, the gum from the bark of A. adianthifolia is used as a hunting poison and in the Central African Republic, the bark and leaves of the species are used as fish poison [86]. These reports highlight the need for detailed toxicological evaluations of both the extracts of the species as well as the compounds isolated from A. adianthifolia to establish the toxicity and/or any side effects that can arise when the species and its products are used as herbal medicines.

https://doi.org/10.1155/2018/7463584

Conflicts of Interest

The author declares that there are no conflicts of interest regarding the publication of this paper.

Acknowledgments

The author would like to express his gratitude to the National Research Foundation (NRF), South Africa, and Govan Mbeki Research and Development Centre (GMRDC), University of Fort Hare, for financial support to conduct this study.

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[81] M. Haddad, V. Laurens, and M.-A. Lacaille-Dubois, "Induction of apoptosis in a leukemia cell line by triterpene saponins from Albizia adianthifolia," Bioorganic & Medicinal Chemistry, vol. 12, no. 17, pp. 4725-4734, 2004.

[82] R. M. Gengan, K. Anand, A. Phulukdaree, and A. Chuturgoon, "A549 lung cell line activity of biosynthesized silver nanoparticles using Albizia adianthifolia leaf," Colloids and Surfaces B: Biointerfaces, vol. 105, pp. 87-91, 2013.

[83] R. Govender, A. Phulukdaree, R. M. Gengan, K. Anand, and A. A. Chuturgoon, "Silver nanoparticles of Albizia adianthifolia: the induction of apoptosis in human lung carcinoma cell line," Journal of Nanobiotechnology, vol. 11, no. 5, 2013.

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[86] R. H. M. J. Lemmens, "Albizia adianthifolia (Schumach.) W. Wight," in Plant Resources of Tropical Africa 7(1). Timbers 1, D. Louppe, A. A. Oteng-Amoako, and M. Brink, Eds., vol. 1, pp. 40-43, PROTA Foundation, Wageningen, The Netherlands, 1 edition, 2008.

Alfred Maroyi (iD)

Medicinal Plants and Economic Development (MPED) Research Centre, Department of Botany, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa

Correspondence should be addressed to Alfred Maroyi; amaroyi@ufh.ac.za

Received 26 June 2018; Accepted 29 August 2018; Published 20 September 2018

Academic Editor: Juei-Tang Cheng

Caption: Figure 1: Albizia adianthifolia, a branch showing leaves and flowers (photo: MA Hyde).

Caption: Figure 2: Distribution of Albizia adianthifolia in tropical Africa.

Caption: Figure 3: Major medicinal uses of Albizia adianthifolia in tropical Africa based on literature records.

Caption: Figure 4: Chemical structures of some compounds isolated from Albizia adianthifolia that exhibited pharmacological activities.
Table 1: Medicinal applications of Albizia adianthifolia
in tropical Africa.

Medicinal use           Parts of the plant used

Antidote                Root and stem bark
Anthrax                 Leaves
Aphrodisiac             Leaves and stem bark
Conjunctivitis          Bark, leaves, leaf sap,
and eye problems        roots and stem bark
Diabetes                Leaves and stem bark
Epilepsy                Stem bark
Gastro-intestinal
problems
Diarrhoea,              Bark, leaves and roots
dysentery
and stomach ache
Haemorrhoids            Leaves, roots and stem bark
Headache                Bark and stem bark
Hiccup                  Leaves and stem bark
Hypertension            Leaves
Love charm              Bark
Memory loss and         Leaves and roots
neuro degenerative
disorders
Purgative               Bark, leaves and roots
Respiratory problems
Bronchitis, cough,
respiratory problems    Bark, leaves and
and sinusitis           stem bark
Reproductive
problems in women
Sterility and           Bark, leaves and roots
uterine problems
Sexually transmitted
infections
Gonorrhoea, Sexually    Bark, leaves, roots
transmitted diseases    and stem bark
and syphilis
Gonorrhoea              Stem bark mixed with
                        Citrus aurantiifolia
                        (Christm.) Swingle
                        fruits
Syphilis                Leaves mixed with
                        Trichilia dregeana
                        Sond. bark
Skin diseases
Abscesses, chicken
pox, eczema,            Bark, leaves and
purulent rashes,        roots
scabies and
skin diseases
Toothache               Leaves and roots
Typhoid fever           Stem bark
Urinary problems        Stem bark
Wounds and pain
Abdominal pains,
back pain (lumbago)     Bark, leaves and
and anal wounds         stem bark
Yaws                    Root bark
Ethnoveterinary
medicine
Coccidiosis and         Roots
wounds
Ethnoveterinary         Blisters treated with
medicine                leaves mixed with
                        those of Gynura
                        scandens O. Hoffm.
                        and fruits of Musa
                        paradisiaca L.

Medicinal use           Country                         References

Antidote                Cameroon                           [27]
Anthrax                 Rwanda                             [44]
Aphrodisiac             DRC                                [45]
Conjunctivitis          Cameroon, Nigeria,             [26-29, 32,
and eye problems        South Africa and                33, 46-49]
                        Swaziland
Diabetes                DRC and Nigeria                  [29, 45]
Epilepsy                Swaziland                        [46, 47]
Gastro-intestinal
problems
Diarrhoea,              DRC, Madagascar,                [26, 30-36]
dysentery               Mozambique, South
and stomach ache        Africa and Tanzania
Haemorrhoids            Nigeria and South Africa         [29, 32]
Headache                Cameroon and South Africa      [26, 33, 50]
Hiccup                  DRC                                [45]
Hypertension            Togo                               [37]
Love charm              South Africa                   [17, 25, 26]
Memory loss and         Nigeria and South Africa
neuro degenerative                                       [32, 51]
disorders
Purgative               Cameroon and South Africa     [26, 28, 31-33]
Respiratory problems
Bronchitis, cough,
respiratory problems    Cameroon, Mozambique,             [25-29]
and sinusitis           Nigeria and South Africa
Reproductive
problems in women

Sterility and           Cameroon and Swaziland         [47, 49, 52]
uterine problems
Sexually transmitted
infections
Gonorrhoea, Sexually    Cameroon, DRC, Guinea,         [29, 45-47,
transmitted diseases    Nigeria, Rwanda,                49, 53-55]
and syphilis            Swaziland and Uganda

Gonorrhoea              Sierra Leone                       [41]

Syphilis                South Africa                       [42]

Skin diseases
Abscesses, chicken
pox, eczema,            Burundi, Cameroon,             [28, 33, 44,
purulent rashes,        South Africa and               47, 49, 52,
scabies and             Swaziland                         56-59]
skin diseases
Toothache               South Africa                       [32]
Typhoid fever           Cameroon                           [27]
Urinary problems        Cameroon                           [27]
Wounds and pain
Abdominal pains,
back pain (lumbago)     Cameroon, Guinea-Bissau          [27, 36,
and anal wounds         and Mozambique                    50, 60]
Yaws                    Rwanda                             [44]
Ethnoveterinary
medicine
Coccidiosis and         Zimbabwe                         [61, 62]
wounds
Ethnoveterinary         DRC                                [43]
medicine

Table 2: Phytochemical compounds identified from Albizia
adianthifolia.

                                          Method of
                                          compound
No.             Compound                   analyses

             Apocarotenoids
1          [beta]-cyclocitral            GC and GC-MS
2        [beta]-cyclohomocitral          GC and GC-MS
3            cis-a-ambrinol              GC and GC-MS
4          (E)-[alpha]-ionone            GC and GC-MS
5        (E)-[beta]-damascenone          GC and GC-MS
6          (E)-[beta]-ionone             GC and GC-MS
7         (E)-geranyl acetone            GC and GC-MS
8               Safranal                 GC and GC-MS
               Dipeptide
9         Aurantiamide acetate              GC-MS
              Elliptosides
10        Monodesmonoterpenyl                NMR
             elliptoside A
             Essential oils
        Non-terpene derivatives
11           1-octen-3-one               GC and GC-MS
12        1,4-dimethyltetralin           GC and GC-MS
13            1,8-cineole                GC and GC-MS
14            2-heptanone                GC and GC-MS
15             2-octanone                GC and GC-MS
16          2-pentadecanone              GC and GC-MS
17      2-phenylethyl butanoate          GC and GC-MS
18      2,4-dimethylbenzaldehyde         GC and GC-MS
19          5-methyltetralin             GC and GC-MS
20      6-methyl-5-hepten-2-one          GC and GC-MS
21           [alpha]-ionone              GC and GC-MS
22            Benzaldehyde               GC and GC-MS
23              Decanal                  GC and GC-MS
24         Dehydro-ar-ionene             GC and GC-MS
25             Mesitylene                GC and GC-MS
26            Naphthalene                GC and GC-MS
27              Nonanal                  GC and GC-MS
28            Pentadecanal               GC and GC-MS
29           n-tetradecane               GC and GC-MS
30            n-tridecane                GC and GC-MS
31             Seudenone                 GC and GC-MS
32            Tetradecanal               GC and GC-MS
33     (Z,E)-undeca-l,3,5-triene         GC and GC-MS
        Oxygenated monoterpenes
34            oc-terpineol               GC and GC-MS
35              Linalool                 GC and GC-MS
36         p-menth-4-en-3-one            GC and GC-MS
37               Thymol                  GC and GC-MS
       Oxygenated sesquiterpenes
38             Acorenone                 GC and GC-MS
39      Caryophylla-4(14),8(15)-         GC and GC-MS
               dien-5-ol
40        Caryophyllene oxide            GC and GC-MS
41           (E)-nerolidol               GC and GC-MS
42        Humulene epoxide II            GC and GC-MS
43            Occidentalol               GC and GC-MS
44        Selin-ll-en-4-oc-ol            GC and GC-MS
45             T-cadinol                 GC and GC-MS
46       trans-[beta]-elemenone          GC and GC-MS
47             Valerianol                GC and GC-MS
48            Viridiflorol               GC and GC-MS
       Sesquiterpene hydrocarbons
49         [alpha]-bulnesene             GC and GC-MS
50          [alpha]-humulene             GC and GC-MS
51            ar-curcumene               GC and GC-MS
52        [alpha]-zingiberene            GC and GC-MS
53         [beta]-bisabolene             GC and GC-MS
54        [beta]-caryophyllene           GC and GC-MS
55           [beta]-elemene              GC and GC-MS
56     [beta]-sesquiphellandrene         GC and GC-MS
57              Cyperene                 GC and GC-MS
58          [delta]-cadinene             GC and GC-MS
59          Isocaryophyllene             GC and GC-MS
60             Italicene                 GC and GC-MS
61           Sesquisabinene              GC and GC-MS
62       trans-[gamma]-cadinene          GC and GC-MS
63         [gamma]-muurolene             GC and GC-MS
               Fatty acid
64     9,12-octadecadienoic acid            GC-MS
          (Z,Z)-,methyl ester
65          Docosanoic acid                 GC-MS
66        n-hexadecanoic acid               GC-MS
67         Octadecanoic acid                GC-MS
68             Oleic acid                   GC-MS
69       trans-13-octadecanoic              GC-MS
           acid, methyl ester
               Flavonoids
70         3-methoxyflavanone                 MS
71              Apigenin                     HPLC
72         Chalcone (okanin)                  MS
73            Melanoxetin                     MS
                Steroids
74          Chondrillasterol                GC-MS
75            Stigmasterol                  GC-MS
76       24S,5[alpha] stigmast-             GC-MS
            7-en-3[beta]-ol
          Triterpene saponins
77        Adianthifoliosides A      FABMS, HRESIMS and NMR
78        Adianthifoliosides B      FABMS, HRESIMS and NMR
79        Adianthifoliosides C               NMR
80        Adianthifoliosides D               NMR
81        Adianthifoliosides E               NMR
82        Adianthifoliosides F               NMR
83           Julibroside A3                  NMR
84           Prosapogenin 1         FABMS, HRESIMS and NMR
85           Prosapogenin 2         FABMS, HRESIMS and NMR
             Triterpenoids
86               Lupeol                     GC-MS
87        3[beta]e,16[beta]e-                NMR
         dimethoxyolean-12-en-
           28-21[beta]a-olide
               Histamine
88             Histamine                    GC-MS
89          Acetylhistamine                 GC-MS
       Imidazolyl carboxylic acid
90        Imidazoleacetic acid              GC-MS

No.             Compound                    Plant part

             Apocarotenoids
1          [beta]-cyclocitral                 Leaves
2        [beta]-cyclohomocitral               Leaves
3            cis-a-ambrinol                   Leaves
4          (E)-[alpha]-ionone          Leaves and stem bark
5        (E)-[beta]-damascenone               Leaves
6          (E)-[beta]-ionone                  Leaves
7         (E)-geranyl acetone                 Leaves
8               Safranal                      Leaves
               Dipeptide
9         Aurantiamide acetate               Stem bark
              Elliptosides
10        Monodesmonoterpenyl                  Roots
             elliptoside A
             Essential oils
        Non-terpene derivatives
11           1-octen-3-one                   Root bark
12        1,4-dimethyltetralin                Leaves
13            1,8-cineole           Leaves, roots and stem bark
14            2-heptanone                     Leaves
15             2-octanone                     Leaves
16          2-pentadecanone                  Root bark
17      2-phenylethyl butanoate              Root bark
18      2,4-dimethylbenzaldehyde              Leaves
19          5-methyltetralin                  Leaves
20      6-methyl-5-hepten-2-one               Leaves
21           [alpha]-ionone                   Leaves
22            Benzaldehyde                   Root bark
23              Decanal                       Leaves
24         Dehydro-ar-ionene                  Leaves
25             Mesitylene                    Root bark
26            Naphthalene              Leaves and root bark
27              Nonanal                       Leaves
28            Pentadecanal          Leaves, roots and stem bark
29           n-tetradecane                    Leaves
30            n-tridecane                     Leaves
31             Seudenone                      Leaves
32            Tetradecanal              Roots and stem bark
33     (Z,E)-undeca-l,3,5-triene              Leaves
        Oxygenated monoterpenes
34            oc-terpineol                    Leaves
35              Linalool               Leaves and root bark
36         p-menth-4-en-3-one                 Leaves
37               Thymol                      Stem bark
       Oxygenated sesquiterpenes
38             Acorenone               Leaves and stem bark
39      Caryophylla-4(14),8(15)-       Leaves and stem bark
               dien-5-ol
40        Caryophyllene oxide       Leaves, roots and stem bark
41           (E)-nerolidol             Leaves and stem bark
42        Humulene epoxide II           Roots and stem bark
43            Occidentalol                   Root bark
44        Selin-ll-en-4-oc-ol           Roots and stem bark
45             T-cadinol               Leaves and stem bark
46       trans-[beta]-elemenone              Stem bark
47             Valerianol                    Root bark
48            Viridiflorol          Leaves, roots and stem bark
       Sesquiterpene hydrocarbons
49         [alpha]-bulnesene                 Stem bark
50          [alpha]-humulene        Leaves, roots and stem bark
51            ar-curcumene             Leaves and stem bark
52        [alpha]-zingiberene          Leaves and stem bark
53         [beta]-bisabolene                 Stem bark
54        [beta]-caryophyllene      Leaves, roots and stem bark
55           [beta]-elemene                  Stem bark
56     [beta]-sesquiphellandrene       Leaves and stem bark
57              Cyperene                     Root bark
58          [delta]-cadinene                 Root bark
59          Isocaryophyllene                 Stem bark
60             Italicene                      Leaves
61           Sesquisabinene                  Stem bark
62       trans-[gamma]-cadinene              Stem bark
63         [gamma]-muurolene                 Stem bark
               Fatty acid
64     9,12-octadecadienoic acid             Heartwood
          (Z,Z)-,methyl ester
65          Docosanoic acid                  Stem bark
66        n-hexadecanoic acid         Heartwood and stem bark
67         Octadecanoic acid                 Stem bark
68             Oleic acid             Heartwood and stem bark
69       trans-13-octadecanoic               Heartwood
           acid, methyl ester
               Flavonoids
70         3-methoxyflavanone                Heartwood
71              Apigenin                      Leaves
72         Chalcone (okanin)                 Heartwood
73            Melanoxetin                    Heartwood
                Steroids
74          Chondrillasterol                 Heartwood
75            Stigmasterol                   Heartwood
76       24S,5[alpha] stigmast-              Heartwood
            7-en-3[beta]-ol
          Triterpene saponins
77        Adianthifoliosides A                 Roots
78        Adianthifoliosides B                 Roots
79        Adianthifoliosides C                 Roots
80        Adianthifoliosides D                 Roots
81        Adianthifoliosides E                 Roots
82        Adianthifoliosides F                 Roots
83           Julibroside A3                    Roots
84           Prosapogenin 1                    Roots
85           Prosapogenin 2                    Roots
             Triterpenoids
86               Lupeol                      Stem bark
87        3[beta]e,16[beta]e-                Root bark
         dimethoxyolean-12-en-
           28-21[beta]a-olide
               Histamine
88             Histamine                Root and stem bark
89          Acetylhistamine             Root and stem bark
       Imidazolyl carboxylic acid
90        Imidazoleacetic acid          Root and stem bark

No.             Compound           References

             Apocarotenoids
1          [beta]-cyclocitral         [70]
2        [beta]-cyclohomocitral       [70]
3            cis-a-ambrinol           [70]
4          (E)-[alpha]-ionone         [70]
5        (E)-[beta]-damascenone       [70]
6          (E)-[beta]-ionone          [70]
7         (E)-geranyl acetone         [70]
8               Safranal              [70]
               Dipeptide
9         Aurantiamide acetate        [27]
              Elliptosides
10        Monodesmonoterpenyl         [67]
             elliptoside A
             Essential oils
        Non-terpene derivatives
11           1-octen-3-one            [70]
12        1,4-dimethyltetralin        [70]
13            1,8-cineole             [70]
14            2-heptanone             [70]
15             2-octanone             [70]
16          2-pentadecanone           [70]
17      2-phenylethyl butanoate       [70]
18      2,4-dimethylbenzaldehyde      [70]
19          5-methyltetralin          [70]
20      6-methyl-5-hepten-2-one       [70]
21           [alpha]-ionone           [70]
22            Benzaldehyde            [70]
23              Decanal               [70]
24         Dehydro-ar-ionene          [70]
25             Mesitylene             [70]
26            Naphthalene             [70]
27              Nonanal               [70]
28            Pentadecanal            [70]
29           n-tetradecane            [70]
30            n-tridecane             [70]
31             Seudenone              [70]
32            Tetradecanal            [70]
33     (Z,E)-undeca-l,3,5-triene      [70]
        Oxygenated monoterpenes
34            oc-terpineol            [70]
35              Linalool              [70]
36         p-menth-4-en-3-one         [70]
37               Thymol               [70]
       Oxygenated sesquiterpenes
38             Acorenone              [70]
39      Caryophylla-4(14),8(15)-      [70]
               dien-5-ol
40        Caryophyllene oxide         [70]
41           (E)-nerolidol            [70]
42        Humulene epoxide II         [70]
43            Occidentalol            [70]
44        Selin-ll-en-4-oc-ol         [70]
45             T-cadinol              [70]
46       trans-[beta]-elemenone       [70]
47             Valerianol             [70]
48            Viridiflorol            [70]
       Sesquiterpene hydrocarbons
49         [alpha]-bulnesene          [70]
50          [alpha]-humulene          [70]
51            ar-curcumene            [70]
52        [alpha]-zingiberene         [70]
53         [beta]-bisabolene          [70]
54        [beta]-caryophyllene        [70]
55           [beta]-elemene           [70]
56     [beta]-sesquiphellandrene      [70]
57              Cyperene              [70]
58          [delta]-cadinene          [70]
59          Isocaryophyllene          [70]
60             Italicene              [70]
61           Sesquisabinene           [70]
62       trans-[gamma]-cadinene       [70]
63         [gamma]-muurolene          [70]
               Fatty acid
64     9,12-octadecadienoic acid      [68]
          (Z,Z)-,methyl ester
65          Docosanoic acid           [27]
66        n-hexadecanoic acid       [27, 68]
67         Octadecanoic acid          [27]
68             Oleic acid           [27, 68]
69       trans-13-octadecanoic        [68]
           acid, methyl ester
               Flavonoids
70         3-methoxyflavanone         [64]
71              Apigenin              [28]
72         Chalcone (okanin)          [64]
73            Melanoxetin             [64]
                Steroids
74          Chondrillasterol          [68]
75            Stigmasterol            [68]
76       24S,5[alpha] stigmast-       [68]
            7-en-3[beta]-ol
          Triterpene saponins
77        Adianthifoliosides A        [66]
78        Adianthifoliosides B        [66]
79        Adianthifoliosides C        [67]
80        Adianthifoliosides D        [67]
81        Adianthifoliosides E        [67]
82        Adianthifoliosides F        [67]
83           Julibroside A3         [65, 67]
84           Prosapogenin 1         [65, 66]
85           Prosapogenin 2         [65, 66]
             Triterpenoids
86               Lupeol               [27]
87        3[beta]e,16[beta]e-         [63]
         dimethoxyolean-12-en-
           28-21[beta]a-olide
               Histamine
88             Histamine              [71]
89          Acetylhistamine           [71]
       Imidazolyl carboxylic acid
90        Imidazoleacetic acid        [71]
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