A synthesis and review of medicinal uses, phytochemistry and biological activities of Markhamia zanzibarica

Alfred Maroyi

doi:https://doi.org/10.26452/ijrps.v11i4.3260

A synthesis and review of medicinal uses, phytochemistry and biological activities of Markhamia zanzibarica

1 Department of Botany, University of Fort Hare, Private Bag X1314, Alice 5700, South Africa, +27406022322

Abstract

Markhamia zanzibarica (Bojer ex DC.) K. Schum.has been used in herbal medicine in tropical Africa since ancient times. Markhamia zanzibarica is indigenous to central, eastern and southern Africa. This extensive literature review synthesizes the information currently available on the medicinal uses, phytochemistry and biological activities of M. zanzibarica. The University library and electronic search engines Google Scholar, Scopus, Web of Science, ScienceDirect and PubMed were searched for pertinent information on the medicinal uses, phytochemistry and biological activities of M. zanzibarica. Traditionally, the species has been used as anthelmintic, and traditional medicine for backache, female reproductive problems, sexually transmitted infections, respiratory infections and gastro-intestinal problems. In vitro studies have confirmed the biological activities of M. zanzibarica which include antibacterial, antimycobacterial, antioxidant and cytotoxicity. Various phytochemicals such as alkaloids, anthraquinones, fatty acids, flavonoids, glycosides, phenolics, saponins, sterols, tannins and triterpenes have been isolated from M. zanzibarica. Documentation of the medicinal uses, phytochemistry and pharmacological properties of M. zanzibarica is essential as this information provides baseline data required for future research and development of health-promoting and pharmaceutical products. However, further pharmacological studies including phytochemical, toxicological, in vitro and in vivo experiments are needed to provide evidence for the clinical effectiveness of remedies prepared from the species.

Keywords

Bignoniaceae, indigenous knowledge, Markhamia zanzibarica, traditional medicine, tropical Africa

Introduction

Markhamia zanzibarica (Bojer ex DC. K. Schum), is a shrub or small tree in the family Bignoniaceae. The family Bignoniaceae consists of 104 genera and 860 plant species which are usually trees, shrubs or lianas and rarely herbs (Fischer, Thiesen, Lohmann, & Bignoniaceae, 2004). The family Markhamia, Consists of ten species, eight of these have been recorded in tropical Africa while two species have been recorded in southeast Asia (Fischer et al., 2004). The genus name Markhamia is in honour of Sir Clements Robert Markham (1830-1916), an English geographer, writer, traveller and explorer (Palmer & Pitman, 1972). The species name “zanzibarica” means from Zanzibar (Bruschi, Morganti, Mancini, & Signorini, 2011), an island regarded as a region of Tanzania. The synonyms of M. zanzibarica include Dolichandrone hirsuta Baker, D. Latifolia Baker. M. acuminata (Klotzsch) K. Schum., M. Puberula (Klotzsch) K. Schum., M. Stenocarpa (Baker) K. Schum, Muenteria Puberula Seem., M. Stenocarpa Seem., M. zanzibarica (Bojer ex DC.)

Table 1: Medicinal uses of Markhamia zanzibarica

Medicinal use	Part used	Country	Reference
Abdominal pain	Bark and root decoction taken orally	Kenya and Tanzania	(Chhabra, Mahunnah, & Mshiu, 1987; Kigen et al., 2016)
Anthelmintic	Roots decoction taken orally	Kenya and Tanzania	(Kokwaro, 2009; Louppe, Oteng-Amoako, & A, 2012)
Aphrodisiac	Roots mixed with those of Uvaria acuminata Oliv.	Kenya	(Kaingu, 2016; Kaingu, Oduma, Mbaria, & Kiama, 2013)
Backache	Root infusion taken orally	Malawi and South Africa	(Morris, 1996; Palgrave & Keith, 2002)
Breast cancer	Root infusion taken orally	Kenya	(Kaingu, 2016; Kaingu, Mbaria, Oduma, & Kiama, 2014)
Constipation	Roots mixed with those of Albizia anthelmintica Brongn., Byrsocarpus boivinianus (Baill.) Baill., Carpolobia goetzei Güerke and Clausena anisata (Willd.) Hook. f. ex Benth.	Tanzania	(Chhabra et al., 1987)
Excessive bleeding during child birth	Bark and root infusion taken orally	Kenya	(Kigen et al., 2016; Pakia, Cooke, & Staden, 2003)
Female reproductive problems (abortifacient, contraceptive, bleeding during child birth, fibroids, infertility, menstrual problems and retained placenta)	Roots mixed with those of Salvadora persica L. and Uvaria acuminata	Kenya	(Kaingu, 2016; Kaingu, Oduma, Mbaria, & Kiama, 2013)
Gastro-intestinal problems (diarrhoea, dysentery and stomach problems)	Bark, leaf and root decoction taken orally	Botswana, South Africa and Tanzania	(Arnold & Gulumian, 1984; Hedberg & Staugård, 1989)
General pains	Root decoction taken orally	Mozambique	(Bruschi et al., 2011; Watt & Breyer-Brandwijk, 1962)
Headache	Leaf infusion applied topically	South Africa	(Semenya & Maroyi, 2018; Watt et al., 1962)
Hernia	Root decoction taken orally	Tanzania	(Chhabra et al., 1987)
Oedema	Bark infusion taken orally	Kenya	(Kigen et al., 2016)
Oxyuriasis	Root decoction taken orally	Tanzania	(Chhabra et al., 1987)
Protective charm (against evil spirits)	Leaves	Tanzania	(Hilonga et al., 2019)
Psychiatric problems	Root decoction taken orally	Tanzania	(Chhabra et al., 1987)
Respiratory infections (cough, expectorant and pneumonia)	Bark and root infusion or decoction taken orally	Kenya, South Africa and Tanzania	(Arnold et al., 1984; Kokwaro, 2009)
Rheumatic fever	Roots mixed with those of Phyllanthus ovalifolius Forssk.	Malawi	(Morris, 1996)
Snake bite	Leaf and root decoction applied topically	Kenya	(Dharani, 2019; Pakia et al., 2003)
Sexually transmitted infections (syphilis and venereal diseases)	Bark decoction taken orally	Kenya and Tanzania	(Chhabra et al., 1987; Kokwaro, 2009)
Toothache	Bark decoction applied topically	Tanzania	(Kokwaro, 2009; Watt et al., 1962)
Uterus prolapse	Roots mixed with those of Vangueria infausta Burch. ssp. rotundata (Robyns) Verdc.	Tanzania	(Chhabra, Mahunnah, & Mshiu, 1991)
Yellow fever	Stem bark is mixed with that of Mangifera indica L., Maesopsis eminii Engl. and Erythrina abyssinica DC.	Tanzania	(Moshi, Otieno, Mbabazi, & Weisheit, 2009)

Table 2: Nutritional and phytochemical composition of Markhamia zanzibarica

Nutritional or phytochemical component	Value	Plant part	Reference
Nutritional component
Acid detergent fibre (%)	19.3–51.1	Leaves and twigs	(Dierenfeld, Toit, & Braselton, 1995)
Acid detergent bound protein (%)	1.8–2.0	Leaves and twigs	(Dierenfeld et al., 1995)
Ash (%)	4.8–10.8	Leaves and twigs	(Dierenfeld et al., 1995)
Calcium (%)	1.6	Leaves and twigs	(Dierenfeld et al., 1995)
Copper (μg/g)	11.0	Leaves and twigs	(Dierenfeld et al., 1995)
Crude protein (%)	9.0–16.3	Leaves and twigs	(Dierenfeld et al., 1995)
Iron (μg/g)	215.0	Leaves and twigs	(Dierenfeld et al., 1995)
Magnesium (%)	0.7	Leaves and twigs	(Dierenfeld et al., 1995)
Manganese (μg/g)	160.0	Leaves and twigs	(Dierenfeld et al., 1995)
Neutral detergent fibre (%)	38.2–66.9	Leaves and twigs	(Dierenfeld et al., 1995)
Phosphorus (%)	0.1	Leaves and twigs	(Dierenfeld et al., 1995)
Potassium (%)	0.8	Leaves and twigs	(Dierenfeld et al., 1995)
Sodium (%)	0.005	Leaves and twigs	(Dierenfeld et al., 1995)
Sulfuric acid lignin (%)	7.5–18.3	Leaves and twigs	(Dierenfeld et al., 1995)
α-tocopherols (μg/g)	13.5–94.1	Leaves and twigs	(Dierenfeld et al., 1995)
γ-tocopherols (μg/g)	1.0–1.7	Leaves and twigs	(Dierenfeld et al., 1995)
Water (%)	39.2–46.0	Leaves and twigs	(Dierenfeld et al., 1995)
Zinc (μg/g)	17.3	Leaves and twigs	(Dierenfeld et al., 1995)
Phytochemical component
3',4',5,7-tetrahydroxy-5'-methoxy-flavanone	-	Leaves	(Gormann, Kaloga, & Kolodziej, 2006)
5,7,3`,5`tetrahydroxy flavanone	-	Aerial parts	(El-Kersh, El-Dine, Abou-Hussein, Sakhawy, & Elmazar, 2016)
Apigenin	-	Leaves	(Gormann et al., 2006)
Apigenin 5-O-α-L-rhamnopyranosyl-7-O-ß-D-glucopyranoside	-	Leaves	(Gormann et al., 2006)
Apigenin-7-O-rutinoside	-	Aerial parts	(El-Kersh et al., 2016)
Campesterol (%)	0.003	Stem bark	(Khan & Mlungwana, 1999)
Eriocitrin	-	Leaves	(Gormann et al., 2006)
Hederagenin (%)	0.01	Leaves	(Gormann, Schreiber, & Kolodziej, 2004)
Hentriacontane (%)	2.9	Leaves	(Gormann et al., 2004)
Heptacosane (%)	0.1	Leaves	(Gormann et al., 2004)
Hexacosanoic (%)	0.1	Leaves	(Gormann et al., 2004)
Hexadecanoic (%)	0.2	Leaves	(Gormann et al., 2004)
Luteolin	-	Aerial parts and leaves	(El-Kersh et al., 2016; Gormann et al., 2006)
Luteolin-7-rutinosid	-	Leaves	(Gormann et al., 2006)
Luteolin-7-O- -D-glucoside	-	Aerial parts	(El-Kersh et al., 2016)
Naringenin	-	Leaves	(Gormann et al., 2006)
Naringenin-7-rutinosid	-	Leaves	(Gormann et al., 2006)
Nigaichigoside F2	-	Aerial parts	(El-Kersh et al., 2016)
Nonacosane (%)	0.6	Leaves	(Gormann et al., 2004)
Octacosanol (%)	0.1	Leaves	(Gormann et al., 2004)
Octadecanoic (%)	0.1	Leaves	(Gormann et al., 2004)
Oleanolic acid (%)	23.1	Aerial parts and leaves	(El-Kersh et al., 2016; Gormann et al., 2004)
Oleic acid (%)	35.8	Aerial parts	(El-Kersh et al., 2016)
Palmitic acid (%)	29.5	Aerial parts	(El-Kersh et al., 2016)
Pentacosane (%)	23.2	Aerial parts	(El-Kersh et al., 2016)
Phytol (%)	2.2	Aerial parts	(El-Kersh et al., 2016)
Quadrangularic acid L	-	Aerial parts	(El-Kersh et al., 2016)
Quadrangularic acid K	-	Aerial parts	(El-Kersh et al., 2016)
β-Sitosterol (%)	0.01–12.8	Aerial parts and leaves	(El-Kersh et al., 2016; Gormann et al., 2004)
γ-Sitosterol (%)	0.004-14.0	Aerial parts and root wood	(El-Kersh et al., 2016; Khan et al., 1999)
Squalene (%)	32.6	Aerial parts	(El-Kersh et al., 2016)
Stigmasterol (%)	0.01–0.9	Aerial parts and leaves	(El-Kersh et al., 2016; Gormann et al., 2004)
Total flavonoid content (mg LE/g)	14.4	Aerial parts	(El-Kersh et al., 2016)
Total phenolic content (mg GAE/g)	177.4	Aerial parts	(El-Kersh et al., 2016)
Tritriacontane (%)	0.009–3.2	Leaves	(Gormann et al., 2004; Khan et al., 1999)
Ursolic acid (%)	36.6	Aerial parts and leaves	(El-Kersh et al., 2016; Gormann et al., 2004)
Verbascoside	-	Aerial parts	(El-Kersh et al., 2016)
isoverbascoside	-	Aerial parts	(El-Kersh et al., 2016)

Seem., Spathodea acuminata Klotzsch, S. puberula Klotzsch, S. tenuifolia Bojer and S. zanzibarica Bojer ex DC. The English common names of M. zanzibarica include “bean tree”, “bell bean”, “golden bean tree” and “maroon bell-bean”. Markhamia zanzibarica is a slender, much-branched and sometimes straggling shrub or small tree with crooked branches growing up to 10 metres in height (Lovett, Ruffo, Gereau, & Taplin, 2007). The bark is grey, smooth to rough, vertically and narrowly flaky and young branches with conspicuous lenticels. The leaves of M. zanzibarica are pinnately compound with obovate leaflets. The leaf margins are smooth or toothed with attenuate apex and broadly tapering to rounded base. The flowers of M. zanzibarica vary from yellow densely flecked with maroon to dark maroon inside and paler outside, occurring in terminal or axillary racemes.

The fruit is a slender, pendulous capsule, hairless with pale dots or lenticels, splitting into two halves. Markhamia zanzibarica has been recorded in deep sand, rocky ridges, hill slopes and riverine fringes in dry evergreen coastal forest, dry lowland forest, woodland, bushveld, grassland, secondary bush at sea level to 1500 m above sea level (Bidgood, Verdcourt, Vollesen, & Bignoniaceae, 2006; Diniz, 1988). Markhamia zanzibarica is indigenous to Zimbabwe, Angola, Somalia, Botswana, Malawi, the Democratic Republic of Congo (DRC), Zambia, Kenya, Mozambique, Tanzania and Namibia (Bidgood et al., 2006; Diniz, 1988). Markhamia zanzibarica is used as a non-alcoholic beverage or famine food in Namibia and South Africa (Fox & Young, 1982; Koenen, 2001). The leaves of M. zanzibarica are browsed by game and livestock (Komwihangilo, Goromela, & Bwire, 1995; Mtengeti & Mhelela, 2006). The leaves of M. zanzibarica are sold as traditional medicines in informal herbal medicine markets in Tanzania (Hilonga et al., 2019). Therefore, this extensive review was undertaken to evaluate the medicinal uses, phytochemistry and biological activities of M. zanzibarica.

Materials and Methods

The University library and electronic search engines Google Scholar, Scopus, Web of Science, ScienceDirect and PubMed were searched for pertinent information on on the medicinal uses, phytochemistry and biological activities of M. zanzibarica. The keywords such as Markhamia zanzibarica, its synonyms, biological activities, phytochemistry, ethnopharmacology, toxicity, botany and ethnobotany were used separately and in combination used within the electronic databases of ScienceDirect, Scopus, PubMed, Web of Science and Google Scholar.

Results and Discussion

Medicinal uses of Markhamia zanzibarica

The bark, leaf and root decoction or infusion of M. zanzibarica are mainly used as anthelmintic, and traditional medicine against backache, female reproductive problems, sexually transmitted infections, respiratory infections and gastro-intestinal problems (Table 1, Figure 1). Other medicinal applications of M. zanzibarica supported by at least two literature reports include the use of the bark, leaf and root infusion or decoction as an aphrodisiac (Kaingu, 2016; Kaingu et al., 2013), and traditional medicine for abdominal pains (Chhabra et al., 1991; Kigen et al., 2016), breast cancer (Kaingu, 2016; Kaingu et al., 2014), general body pains (Bruschi et al., 2011; Watt et al., 1962), headache (Semenya et al., 2018; Watt et al., 1962) and snakebite (Dharani, 2019; Pakia et al., 2003).

Nutritional and phytochemical composition of Markhamia zanzibarica

Dierenfeld et al. (1995) investigated the nutritional properties of the leaves and twigs of M. zanzibarica (Table 2). Some health-promoting nutrients such as calcium, copper, crude fibre, iron, magnesium, manganese, phosphorus, potassium, proteins, sodium and zinc have been identified from the species, and these reports corroborate the utilization of M. zanzibarica as fodder for both game and livestock in tropical Africa (Komwihangilo et al., 1995; Mtengeti et al., 2006). Phytochemical compounds identified from the aerial parts, leaves, roots and root wood of M. zanzibarica include alkaloids, anthraquinones, fatty acids, flavonoids, glycosides, phenolics, saponins, sterols, tannins and triterpenes.

Pharmacological properties of Markhamia zanzibarica

Mayekiso, Eloff, and Mcgaw (2009) evaluated the antibacterial activities of acetone leaf extracts of M. zanzibarica against Pseudomonas aeruginosa, Staphylococcus aureus, Enterococcus faecalis and Enterococcus coli using the following microdilution method. The extract exhibited activities against the tested pathogens with minimum inhibitory concentration (MIC) values as low as 0.02 mg/ml. Mayekiso et al. (2009) also evaluated the antimycobacterial activities of acetone leaf extracts of M. zanzibarica against Mycobacterium fortuitum and Mycobacterium smegmatis using the serial microdilution method. The extract exhibited activities against the tested pathogens with MIC values as low as 0.02 mg/ml (Mayekiso et al., 2009).

https://typeset-prod-media-server.s3.amazonaws.com/article_uploads/f9769c5d-eac1-4f4c-935e-3d2aec21cade/image/dced6850-fe63-4de2-beaa-2377dd37a5f3-u3749.png — Figure 1: Major medicinal uses of *Markhamia zanzibarica*

El-Kersh et al. (2016) evaluated the antioxidant activities of n-hexane, ethyl acetate, butanol, chloroform and ethanol extracts of the aerial parts of M. zanzibarica using the 1,1-diphenyl-2-picryl-hydrazyl (DPPH) free radical scavenging assay with ascorbic acid as standard. The ethyl acetate extract exhibited the highest activities with half-maximal inhibitory concentration (IC₅₀) value of 154.6 µg/ml (El-Kersh et al., 2016).

Khan et al. (1999) evaluated the cytotoxicity activities of the compounds γ-sitosterol, campesterol and tritriacontane isolated from M. zanzibarica using the brine shrimp (Artemia salina) assay with lapachol as reference drug. The compound γ-sitosterol exhibited activities with the median lethal concentration (LC₅₀) value of 4.0 ppm, which was lower than the LC₅₀ value of 5.0 ppm (Khan et al., 1999). McGaw, Elgorashi, and Eloff (2010) evaluated the cytotoxicity activities of acetone extracts of M. zanzibarica leaves against Vero kidney cells and bovine dermis cells. The extract exhibited activities with LC₅₀ values of less than 50.0 ug/ml against both cell types.

El-Kersh et al. (2016); McGaw et al. (2010) evaluated the cytotoxicity activities of n-hexane, ethyl acetate, butanol, chloroform and ethanol extracts of the aerial parts of M. zanzibarica against the human cervical adenocarcinoma cell line (HeLa) using the sulforhodamine B colourimetric assay with doxorubicin as a positive control.

The extracts exhibited activities with IC₅₀ values ranging from 9.2 µg/ml to 49.6 µg/ml in comparison to IC₅₀ value of 7.3 µg/ml exhibited by the positive control (El-Kersh et al., 2016).

Similarly, El-Kersh et al. (2016) evaluated the cytotoxicity activities of n-hexane, ethyl acetate, butanol, chloroform and ethanol extracts of the aerial parts of M. zanzibarica against the HeLa, MCF-7, HEPG2, PC3 and A549 using the sulforhodamine B colourimetric assay with doxorubicin as a positive control.

The extracts exhibited activities with the best activities against the cancer cells exhibiting IC₅₀ values ranging from 8.5 µg/ml to 18.4 µg/ml (El-Kersh et al., 2016).

Conclusions

This study reviewed the medicinal uses, phytochemistry and biological activities of M. zanzibarica. The current pharmacological studies indicate the potential biological activities of the phytoconstituents and crude extracts of M. zanzibarica, indicating the merit for more attention in future studies. More pharmacological studies including phytochemical, toxicological, in vitro and in vivo experiments are needed to provide evidence for the clinical effectiveness of remedies prepared from the species.

Acknowledgement

I am grateful to the reviewers who kindly commented on my manuscript.

Conflict of Interest

The authors declare that they have no conflict of interest for this study.

Funding Support

The authors declare that they have no conflict of interest for this study.

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