BALANITES MAUGHAMII SPRAGUE (ZYGOPHYLLACEAE) IN TROPICAL AFRICA: A SYNTHESIS AND REVIEW OF ITS CHEMISTRY, PHARMACOLOGY, AND MEDICINAL POTENTIAL

Balanites maughamii is an important medicinal plant species in Southern Africa. This study is aimed at providing a critical review of the biological activities, phytochemistry, and medicinal uses of B. maughamii. Documented information on biological activities, medicinal uses, and phytochemistry of B. maughamii was collected from several online sources which included BMC, Scopus, SciFinder, Google Scholar, Science Direct, Elsevier, PubMed, and Web of Science. Additional information on the biological activities, phytochemistry and medicinal uses of B. maughamii were collected from preelectronic sources such as book chapters, books, journal articles, theses, and scientific publications sourced from the university library. This study showed that the bark, fruits, leaves, and roots of B. maughamii are traditionally used for magical purposes, as emetic, tonic, fish poison, insecticidal, and herbal medicine for bilharzia. Phytochemical compounds identified from the bark, fruits, and leaves of B. maughamii are aliphatic alcohols, aliphatic ketones, benzenoid compounds, aliphatic acids, amino acids, coumarin, aliphatic esters, flavonoids, aliphatic aldehydes, and sterol. Pharmacological research revealed that B. maughamii extracts have adulticidal, antibacterial, antiplasmodial, bitterness, molluscicidal, and mutagenic activities. Future research should focus on evaluating the phytochemical, pharmacological, and toxicological properties of B. maughamii crude extracts as well as compounds isolated from the species.


INTRODUCTION
Balanites maughamii Sprague is a member of the Zygophyllaceae family. The Zygophyllaceae family is a heterogeneous family consisting of about 23 genera and 235 to 240 species in the dry regions of Africa, America, Australia, Asia, and Europe [1]. Delimitation of taxa within the Zygophyllaceae family has repeatedly changed over time. For example, the genus Balanites Delile has been assigned its own family Balanitaceae due to unique morphological and anatomical characteristics [2][3][4]. However, other researchers, for example, Cronquist [5], Fahn et al. [6], and Narayana et al. [7] included the genus Balanites in Zygophyllaceae family. Evaluation of phylogenetic relationships within the Zygophyllaceae family based on DNA sequences of non-coding trnL-F and plastid gene rbcL region support assignment of the genus Balanites in the Zygophyllaceae family [1,[8][9][10][11]. The genus name "Balanites" was derived from a Greek word which means "acornshaped" in reference to the fruits of the genus [12,13]. The species name "maughamii" is in honor of Mr. Maugham, the former British Consul at Lourenco Marques (now Maputo in Mozambique) who collected the type specimen of the species in Southern Mozambique [13][14][15][16]. The synonym of B. maughamii is B. dawei Sprague [17]. The English common names of the species "torchwood," "torch fruit tree," and "y-thorned torchwood" are in reference to the dry kernels of the species which have traditionally been burnt as torches [13,14,[16][17][18][19]. B. maughamii is one of the valuable medicinal plant species in South Africa, and the species is included in the book "medicinal plants of South Africa," a photographic guide to the most commonly used herbal medicines in the country, including its botany, major medicinal applications active phytochemical compounds [20]. According to Van Wyk and Gericke [21] and Van Wyk et al. [20], B. maughamii is considered an important tonic in Southern Africa. Due to the popularity of B. maughamii as traditional medicine, the bark of the species is marketed as a traditional medicine in the traditional medicine informal markets in Gauteng, KwaZulu-Natal, and Mpumalanga Provinces in South Africa [22][23][24][25][26][27][28][29][30][31]. B. maughamii is also categorized as declining in KwaZulu-Natal Province [22], and research by Mander [32] ranked the species thirteenth out of 70 most widely demanded herbal medicine by consumers in the province. Similarly, Twine [33] ranked B. maughamii as third out of 36 tree species harvested for their bark in Southern Maputaland in KwaZulu-Natal Province, South Africa. Based on these reports, it is clear that B. maughamii has an enormous contribution to primary health care of local people in many areas of South Africa. Several people in developing countries depend on medicinal plants such as B. maughamii for their primary health care needs [34,35]. Therefore, this review is aimed at providing a comprehensive appraisal of the biological activities, phytochemistry, and medicinal uses of B. maughamii crude extracts.

BOTANICAL DESCRIPTION OF B. MAUGHAMII
B. maughamii is a medium-sized deciduous or semi-deciduous tree reaching 20-25 m in height [17,19]. B. maughamii has a spreading crown, branching at about 2 m above the ground level [14] with a straight, deeply folded, fluted, and buttressed trunk which is up to 30 cm or more in diameter [17]. The bark is smooth, yellowish brown, mottled, or gray in color and becoming roughly fissured in larger and older specimens [14,18]. The branches are usually yellow to grayishgreen in color, covered with short grayish-green hairs when young but becoming smooth with age, characterized by strong, robust, sharp conspicuous forked spines on the upper bole and branches as well as the younger stems. The leaves are compound made up of two leaflets on very short furry stalks, alternate and arranged spirally, with triangular stipules [14,17,18]. The leaflets are ovate to almost round in shape, acute or shortly acuminate, entire margins, dark gray-green in color, with velvet hairs when young and these persisting on the undersurface to maturity [18]. The flowers are small, inconspicuous, borne in small bunches, yellowish green in color, sessile or with short peduncle, petals with dense hairs on the outer surface [14,18]. The fruit is a oneseeded drupe, oblong-ellipsoid in shape, depressed at both ends and reddish brown in color at ripening [19]. The skin of the fruit is firm but thin, eventually brittle, containing spongy and fibrous, dark and oily mesocarp and a stone with thick endocarp [14,[17][18][19].

Maroyi
B. maughamii is subdivided into two subspecies, subsp. maughamii and subsp. acuta Sands which are distinguished mainly by leaflet shape and pubescence. The leaflets on fertile shoots of subsp. maughamii are rounded or obtuse in shape and are pubescent, while those of subsp. acuta are acute to shortly acuminate and glabrous. The subsp. maughamii is widespread in distribution and has been recorded in Zimbabwe, Kenya, Mozambique, Malawi, South Africa, Zambia, and Swaziland [16][17][18][19][36][37][38][39][40][41][42][43][44]. The subsp. maughamii has been recorded in clay-loam, fine clay silt and sandy soil in sand forest, dry open woodland, bushland, seasonally waterlogged flood-plains, along river banks, near springs, around pans, dunes, sandstone outcrops, and termitaria at an altitude ranging from sea level to 1000 m above sea level [14,[17][18][19]40]. The subsp. acuta has been recorded in Southeast Kenya and Northeast Tanzania in alkaline soil and light sandy soil on coral rag or lava in mixed coastal, lowland evergreen rainforest, ground-water forest, coastal thicket, and riverine thicker at an altitude ranging from sea level to 500 m above sea level [17]. However, most ethnobotanical and ethnopharmacological literature do not separate B. maughamii into specific subspecies, but rather B. maughamii sensu lato, and this is the approach that has been adopted in the current review.
The fruits of B. maughamii which have a pleasant sweet scent and taste, but later become bitter are edible in Southern Africa mainly as a snack [14,18,[45][46][47][48][49][50][51][52]. According to Mahlo [53], the fruits of B. maughamii are used in South Africa as additives in the production of sweets and alcoholic beverages. The kernels of B. maughamii yield large quantities (about 60%) of tasteless, odorless, clear and yellow edible oil that burns well and have good lubricative qualities and used as a massage oil [14,19,38,45,48,54,55]. Research by Grace and Sands [19] showed that oil pressed from the seed kernels of B. maughamii is used in the Limpopo Province in South Africa as a dressing for hides and skins. Since the oil from B. maughamii kernels is flammable, it is, therefore, suitable for industrial use [19].

MEDICINAL USES OF B. MAUGHAMII
The bark, fruits, leaves, and roots of B. maughamii are used for various traditional and medicinal applications (Table 1). B. maughamii is mainly used for magical purposes (good luck, wards off evil spirits, bath said to be stimulating, and exhilarating), as emetic, tonic, fish poison, insecticidal, and herbal medicine for bilharzia (Table 1 and Figure 1). Other minor medicinal applications recorded in a single country include use of the species as arrow poison, mosquito repellent, snail poison, purgative and panacea, and as herbal medicine for cough, malaria and nervous complaints [19][20][21][55][56][57][58][59][60][61][62]. In Mozambique, the bark of B. maughamii is mixed with Phaseolus vulgaris L. as an herbal medicine for hematuria [21]. In South Africa, the leaves of B. maughamii are used as ethnoveterinary medicine for diarrhea in cattle [53,63,64].

PHYTOCHEMICAL AND NUTRITIONAL COMPOSITION OF B. MAUGHAMII
Very little attention has been paid to the macro-and micro-elements of B. maughamii. One report done by Dierenfeld et al. [78] partly studied this subject and reported values of the nutritional composition of leaves and twigs of B. maughamii (Table 2). Langlois [66] identified the compounds scopoletin and stigmasterol from the ethanol bark extract of B. maughamii while Olivier [55] identified alcohol precipitable solids and flavonoids from the bark extracts of the species (Table 3). The major aliphatic acids and aliphatic alcohols exceeding 10.0% identified from the fruits of B. maughamii include hexanal (14.0%), isovaleric acid (15.7%), and hexanoic acid (40.4%) [79,80]. Major amino acids exceeding 10.0 mg/g of dry weight identified from the bark and leaves of B. maughamii include alanine, alloisoleucine, aspartic acid, tryptophan, glutamic acid, glycine, isoleucine, phenylalanine, lysine, proline, leucine, serine, histidine, threonine, glutamine, tyrosine, asparagine, and valine [55]. Future research should focus on evaluating the biological activities of the isolated compounds.

Antibacterial activities
Mahlo [53] and Mahlo and Chauke [53,82] evaluated antibacterial activities of acetone leaf extracts of B. maughamii against Bacillus cereus, Pseudomonas aeruginosa, Escherichia coli, and Enterococcus faecalis using agar-dilution and serial dilution methods with tetracycline as a positive control. The minimum inhibitory concentration (MIC) values of extracts without polyethylene glycol (PEG) ranged from 0.2 mg/ml to 1.6 mg/ml while the addition of PEG resulted in a reduction of antibacterial activities with MIC values ranging from 3.1 mg/ml to 12.5 mg/ml [53,82].

Antiplasmodial activities
Prozesky et al. [67] evaluated the antiplasmodial activities of dichloromethane stem bark extracts of B. maughamii against Plasmodium falciparum by means of the flow cytometric test. The extract exhibited activities with half maximal inhibitory concentration value of 1.9 μg/ml [67].

Bitterness activities
Olivier and Van Wyk [83] evaluated the bitterness values of the bark of B. maughamii using procedures prescribed by the World Health Organization [89] and the European Pharmacopoeia [90] and compared the bitterness value of quinine hydrochloride set at 200 000. The bitterness value of 4211±2019 was obtained for B. maughamii bark. The physiological effects associated with the bitter taste of herbal medicines are ascribed to the bitter tonic (amarum) effect, that is, result in the stimulation, secretion of saliva, secretion of gastric juices, and secretion of bile through taste stimuli through the nervus vagus [83].

Molluscicidal activities
Research by Wager [84] revealed that the fruits of B. maughamii that fell in infested water were observed to inhibit proliferation of snails and cercariae. Pretorius et al. [85] evaluated the molluscicidal properties of the kernel and pulp of ripe fruits of B. maughamii. The extracts were toxic to snails at concentrations of 25 mg/ml, and molluscicidal activities were retained in powdered material for up to 122 days, but leaves and seeds showed no molluscicidal properties [85]. Ojewole [86] evaluated molluscicidal activities of the bark, fruit, and leaf extracts of B. maughamii by exposing adult Bulinus africanus and Biomphalaria pfeifferi to sublethal and lethal doses of crude and aqueous bark, leaf, and twig extracts of the species for a period of 24 h using niclosamide (Bayluscide ® ) (Coating Place Inc., Washington DC, WA, US) as reference molluscicide for comparison. The extracts demonstrated moderate to strong molluscicidal activity with lethal dose 90% value of 50 ppm-100 ppm compared to the positive control, niclosamide (Bayluscide ® ) which killed all the snails at a dose of 1 ppm [86].

AUTHOR'S CONTRIBUTIONS
The author declares that this work was done by the author named in this article.