Abstract
Background: Zanthoxylum chalybeum Engl. is a traditional medicinal plant, which is native to Eastern and Southern Africa. Commonly known as the ‘Knob wood’, it has been used for centuries by several traditional healers in Kenya, Tanzania, Uganda, Zambia and Zimbabwe. The species is very well known to local communities by its common names such as ‘Kundanyoka’ (Shona), ‘Mjafari’ (Swahili) and ‘Ntaleyedungu’ (Uganda), and it grows naturally in the tropics and subtropics.
Aim: The present review describes information on the ethnomedicinal uses, phytochemical constituents, pharmacology and toxicology of Z. chalybeum.
Method: Collection of data was based on literature research from several sources including electronic databases such as Google scholar, Web of Science, Science Direct, Pubmed, books, book chapters and theses.
Results: Z. chalybeum is widely used in the treatment of malaria, cancer and diabetes. Pharmacological studies revealed that crude extracts and some isolated chemical compounds from Z. chalybeum demonstrated biological activities such as antibacterial, antidiabetic and antimalarial activities. Studies in phytochemical analysis of Z. chalybeum revealed the presence of new compounds such as 6-benzo (1, 3) dioxol-5-yl-hexa-2,5 dienoic acid isobutylamide, 4-methoxy-N-(2-methoxy-phenyl)-N methyl-benzamide, N-(2-hydroxy-methyl-propyl)-3 phenyl-acrylamide and 4-(isoprenyloxy)-3-methoxy,4-deoxymethylenedioxyfagaramide. Toxicology studies revealed moderate to high toxicity, depending on the type of cells and the extraction solvent used.
Conclusion: Z. chalybeum is a valued medicinal plant used in Eastern and Southern Africa.
Contribution: The properties of Z. chalybeum revealed in previous studies can be used to guide research scientists in future drug formulations.
Keywords: Zanthoxylum chalybeum Engl; toxicology; pharmacology; ethnobotanical; phytochemical compound.
Introduction
Plant extracts have always been used by people in various parts of Africa and Asia for the treatment of livestock and human ailments (Kokwaro 2009). According to the World Health Organization (WHO) (WHO 2001), the African and Asian communities relied on traditional medicine, especially plant-based remedies to meet their primary healthcare needs. The use of plant-derived medicines is preferred because of their affordability and safety in comparison to synthetic alternatives. Because most conventional drugs are expensive and inaccessible to locals living far away from health centres, this ever-rising cost of modern medicine has prompted most people in developing countries to resort to traditional medicine to treat a variety of ailments. Hence, decoctions, concoctions and infusions from different parts of medicinal plants are being used.
Zanthoxylum chalybeum Engl var chalybeum is a deciduous plant of the tropics and subtropics and native to the Eastern and parts of Southern African countries (Ethiopia, Somalia, Kenya, Uganda, DRC, Tanzania, Lesotho, South Africa, Rwanda, Malawi, Burundi, Namibia, Zambia, Mozambique, Eswatini and Zimbabwe) (Figure 1). It is commonly known as the ‘Knob wood’, because of its characteristic large, conical woody knobs, with sharp thorns along its trunk (Orwa et al. 2009).
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FIGURE 1: Distribution of Zanthoxylum chalybeum in native Africa. |
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Across Africa, Z. chalybeum has been used by community elders and traditional healers for the treatment of diseases, and it is prepared and used in a variety of different ways. In Kenya, it is one of the most commonly used traditional plants, and it is used to treat ailments such as rheumatism, sexually transmitted infections, amoebiasis and throat infections (Kipkore et al. 2014; Kiringe 2006). In Tanzania, the plant is used for treating malaria, jaundice, heart infections and pneumonia (Chhabra et al. 1990; Mbinile et al. 2020). In Uganda, Zambia and Zimbabwe, it is used to treat sickle cell anaemia, skin diseases and dental diseases, respectively (Chagonda et al. 1994; Chisowa, Hall & Farman 1999; Engeu et al. 2008). The plant parts mainly used are the stem bark, root bark and leaves. They are either ground to powder, burnt or prepared for decoctions or concoctions that can be drunk, chewed, applied topically or mixed with other liquids such as tea or milk.
Zanthoxylum chalybeum has been previously studied for its pharmacological properties. Research has shown tremendous results on the antibacterial, antifungal, antiplasmodial, antidiabetic, anticancer and antisickling properties of Z. chalybeum (Agwaya, Natundu & Vuzi 2016; Engeu et al. 2008; Njenga et al. 2016; Omosa et al. 2021; Pierre, Munyabuhoro & Emmanuel 2011; Taniguchi et al. 1978). Analysis of active chemical compounds of Z. chalybeum has shown the presence of reducing sugars, alkaloids, anthracenosides, coumarine derivatives, flavonoids, steroid glycosides, triterpenes, anthocyanocides, saponins and cardiac glycosides (Adia et al. 2016; Nalule, Mbaria & Kimenju 2013). Studies on the safety levels of Z. chalybeum have generally established that the plant has fairly low to moderate toxicity. However, some researchers have reported high toxicity in some plant parts using the brine shrimp lethality assay (Chrian et al. 2011; Nguta et al. 2011). The study aims to review the ethnomedicinal uses, pharmacological properties, phytochemical and toxicology of Z. chalybeum. An understanding of Z. chalybeum from science-backed evidence may allow for potentially new drugs that can address the growing problem of multi-drug resistant pathogens.
Methods
Relevant information on the ethnobotanical uses, pharmacological, phytochemistry and toxicology of Z. chalybeum was collected from various scientific studies. A search using the web search engine Google and other databases of scientific journals such as PubMed (https://pubmed.ncbi.nlm.nih.gov/), Science direct (www.sciencedirect.com), Web of Science (www.webofknowledge.com), Springerlink (www.link.springer.com) and google scholar (www.scholar.google.com) were used to retrieve valuable information. Keywords such as Z. chalybeum, ethnomedicinal, phytochemistry, toxicity and pharmacology were used to collect relevant information. Other relevant scientific publications were obtained from the Tshwane University of Technology library, South Africa, in order to include books, theses and scientific write-ups with known academic rating. Studies were not limited to a time frame as this review has never been done. Criteria were set to screen the search results for relevance in the study. Only scientific articles published in English were considered. Exclusion criteria were publications containing no original research, samples collected outside Africa and studies that excluded Z. chalybeum.
Review findings
Search criteria
Online search strategy identified 122 articles. Articles not meeting the selection criteria (59) and those that were not written in English (2) were excluded. Thirteen articles were added after manual search from retrieved articles. A total of 74 relevant articles were chosen and full text manuscripts were read. Sixty-three articles met the inclusion criteria, 19 articles yielded information on ethnobotanical uses, 15 on pharmacological uses, 6 on phytochemical, 5 on toxicological and 18 on more than one category. Figure 2 shows a schematic depicting of the study selection process. Table 1 to Table 4 summarise the results on ethnomedicinal, pharmacological, phytochemical and toxicological properties of Z. chalybeum studied in this review.
| TABLE 1: Ethnomedicinal uses of Zanthoxylum chalybeum in Africa. |
| TABLE 2: Pharmacological properties of Zanthoxylum chalybeum. |
| TABLE 3: Classes of compounds isolated from Zanthoxylum chalybeum. |
| TABLE 4: Toxicological properties of Zanthoxylum chalybeum in reviewed studies. |
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FIGURE 2: Flow diagram of study selection process. |
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Ethnomedicinal uses of Zanthoxylum chalybeum
A total of 35 ethnomedicinal uses of Z. chalybeum are documented in the literature (Table 1), from eight countries. Tanzania had the most ethnomedicinal uses (13), followed by Kenya (12), Uganda (6), Zambia (5), Zimbabwe (3), Somalia (2), Rwanda (1) and Ethiopia (1). In Uganda, Kenya and Tanzania, Z. chalybeum was most frequently used ethnobotanically to treat malaria. The most widely used plant parts were the roots (23), followed by the stem (12), leaves (8) and lastly berries (3) (Table 1). According to literature, Z. chalybeum decoctions or concoctions can be boiled and then drank alone or mixed with other beverages like tea or milk (Kiringe 2006). In Kenya, the bark and seeds of Z. chalybeum are combined with most traditional preparations as a synergistic herb to improve efficiency (Kiringe 2006). Matata et al. (2018) established that Z. chalybeum is used to treat breast and cervical cancer, and the people of Mkuranga and some districts in Tanzania use the stem and root barks to prepare the concoctions. Zanthoxylum chalybeum can be mixed with plant parts of other medicinal plants; for example, the bark can be used alone or in combination with Terminalia spinose in the treatment of malaria (Mbinile et al. 2020). It can also be mixed with different parts of Zehneria scabra, and the concoction is administered after surgery (Kipkore et al. 2014). Table 1 lists the ethnomedicinal applications of Z. chalybeum in Africa.
Pharmacological properties of Zanthoxylum chalybeum
Studies have demonstrated that Z. chalybeum exhibits antimicrobial activity for some microorganisms (Chrian et al. 2011; Taniguchi et al. 1978). Pierre et al. (2011) revealed that the ethanolic extract showed activity against Salmonella typhimurium, Pseudomonas aeruginosa and Staphylococcus aureus and reduced the growth of Gram-negative S. typhi and P. aeruginosa. Maima and Munyendo (2018) established antimicrobial activity against Methicillin-resistant Staphylococcus aureus (MRSA), while Schultz et al. (2020) established that Z. chalybeum root bark displayed high inhibitory activities against two multidrug-resistant ESKAPE pathogens, Enterococcus faecium (MIC 32 µg/mL) and S. aureus (MIC 16 µg/mL). Interestingly, Mahamadi and Wunganayi (2018) conducted a study on the development of silver nanoparticles using root extracts of Z. chalybeum, where Z. chalybeum was used both as a reducing and stabilising agent. Their results showed that silver nanoparticles synthesised using Z. chalybeum increased the zones of inhibition against Bacillus subtilis, Escherichia coli and P. aeruginosa as compared to the control antibiotic drug and the plant extract alone, and the root extract alone also exhibited a satisfactory result. However, some studies have established that bacteria such as E. coli cannot be inhibited by Z. chalybeum extracts (Kaigongi et al. 2014; Nguta & Kiraithe 2019). Olila, Olwa-Odyek and Opuda-Asibo (2001) demonstrated that all Z. chalybeum stem bark and seed ethanolic, petroleum ether and aqueous extracts did not exhibit antimicrobial activity against E. coli, S. aureus and Candida albicans. Likewise, Nguta and Kiraithe (2019) observed no antibacterial activity against E. coli. Zanthoxylum chalybeum has also been studied for its antiplasmodial properties. Recently, Mollel et al. (2022) reported antiviral activity of Z. chalybeum root bark against the respiratory syncytial virus (RSV), human parainfluenza virus 2 (HPIV-2) and the herpes simplex virus 2 (HSV-2). Njenga et al. (2016) and Waiganjo et al. (2020) revealed significant antiplasmodial activity against drug- sensitive and drug-resistant strains of P. falciparum. Studies have also revealed noteworthy antidiabetic (Agwaya & Natundu 2016; Agwaya et al. 2016; Nyongesa 2019), anticancer (Omosa et al. 2021) and anti- sickling (Engeu et al. 2008) activity of Z. chalybeum. Table 2 depicts the reviewed pharmacological properties of Z. chalybeum in African countries.
Phytochemistry of Zanthoxylum chalybeum
A variety of phytochemical constituents have been isolated from Z. chalybeum root barks, stem barks, leaves and seeds. Generally, Z. chalybeum contains tannins, reducing sugars, saponins, alkaloid salts, anthraenosides, flavinosides, steroidglycosides triterpenes and anthocyanosides (Nalule et al. 2013). A detailed phytochemical analysis of essential oils in Z. chalybeum revealed the presence of neral, limonene, geranial and terpinene-4-ol (Chagonda et al. 1994; Chisowa et al. 1999; Ocheng et al. 2015). However, 3-careen, 4-careen, Cis-β-Ocimene, β-Phellandrene, α- Phellandrene, α-Pinene, β-Pinene, geraniole, geranyl acetate, linalool, Cis-β-terpineol and decanal were only present in Z. chalybeum plants that are found in Uganda (Ocheng et al. 2015). Neryl acetate, linalyl propionate and camphene were only found in Zimbabwe (Chagonda et al. 1994) and sabinen, and trans-p-menth-2-en-1-ol was isolated from Zambian samples (Chisowa et al. 1999). Omosa et al. (2021) isolated a new compound, 4-(isoprenyloxy)-3-methoxy,4-deoxymethylenedioxyfagaramide, from the MeOH/CH2Cl2 (1:1) extract of Z. chalybeum.
Ochieng et al. (2020) also isolated 6-benzo (1, 3) dioxol-5-yl-hexa-2,5 dienoic acid isobutylamide, 4-methoxy-N-(2-methoxy-phenyl)-N methyl-benzamide and N-(2-hydroxy-methyl-propyl)-3 phenyl -acrylamide from the methanolic root bark extract of Z. chalybeum. Other noteworthy compounds identified include sesamin, 3-(1-isopenoloxy)-4-methoxyfagaramide and fagaramide (Gacheru 2018), 2 3-epoxy 6, 7-methylenedioxy coniferylalcohol, dihydrochelerythrine (Anza et al. 2014), N-isobutyl-3-(3, 4-methylene dioxyphenyl)-2E-propenamide (Adia et al. 2016) and skimianine (Olila, Olwa-Odyek & Opuda-Asibo 2001).
Toxicology of Zanthoxylum chalybeum
Analysis of toxicity studies on Z. chalybeum shows that the stem bark has the most potent toxicity compared to other plant parts. The stem and root bark extracts exhibited highly potent toxicity using the Brine shrimp lethality (BSL) assay. Although the CHCl3/methanol 1:1 root bark extract exhibited a high toxicity on BSL (11 µg/mL) (Nguta et al. 2011), Matata et al. (2018) exhibited moderate (38.5 µg/mL) toxicity, and this could be attributed to differences in geographical locations that contribute to differences in phytochemical constituents. Aqueous extracts exhibited mostly low to moderate potency (Nguta et al. 2011; Waiganjo et al. 2020) from all plant parts. Adia et al. (2016) and Gacheru (2018) isolated fagaramide from stem barks of Z. chalybeum and both exhibited potent toxicity on both leukaemia and P. falciparum cell lines. In other studies, Sesamin, 3-(1-isopenoloxy)-4 methoxyfagaamide and 4-(isoprenyloxy)-3-methoxy, 4-deoxymethylenedioxyfagaramide isolated from stem barks of Z. chalybeum exhibited significant toxicity on both sensitive and resistant leukaemia and P. falciparum cell lines (Omosa et al. 2021; Gacheru 2018), and these could attribute to the high levels of toxicity in stem barks.
Implications and recommendations
Herbal medicines have been used in medical practice for many years and have contributed immensely to the maintenance of human health especially in developing countries. Scientific research on Z. chalybeum suggests a huge biological potential of the plant. The most common plant part that is used by traditional medical practitioners is the root bark. Kitula (2007) reported that roots and stems contain high concentrations of active compounds than other plant parts. However, high utilisation of these parts may harm their sustainability, unless proper harvesting techniques are implemented (Mbinile et al. 2020). Although Z. chalybeum is abundantly distributed in East, West and Central Zimbabwe and is not listed on the red data list of the threatened plant species in Zimbabwe, such actions may jeopardise its conservation efforts. The widespread utilisation of the plant’s roots can have negative consequences as it can result in the complete depletion of the plant. This, in turn, may pose a risk to the species, making it increasingly rare, endangered or possibly extinct.
Zanthoxylum chalybeum has displayed a wide range of pharmacological activities in Eastern and Southern Africa. Ochieng et al (2020) established that alkaloids from Z.chalybeum root barks played a significant role in inhibiting α-amylase and β-glucosidase activities. Their results confirmed the antihyperglycemic potential of alkaloids from Z. chalybeum, which lends credence to its use towards diabetes susceptibilities. Kaigongi et al. (2022) recently demonstrated that there is a correlation between antimicrobial and antioxidant activity in Z. chalybeum. They showed that the lower the DPPH value for antioxidant activity, the higher the antimicrobial activity. Despite most researchers showing inhibition of pathogenic organisms (Kaigongi et al. 2014; Maima & Muyendo 2018), some did not show any inhibition (Nguta & Kiraithe 2019; Olila, Olwa-Odyek & Opuda-Asibo 2001). It should be noted that traditional medicine involves the use of combinations of plants in the form of decoctions and infusions which use water as a solvent. These combinations may help activate inactive chemicals or may have a stronger synergistic effect when combined. An alternative explanation is that extracts from Z. chalybeum may exert their effects indirectly, and it is possible that the active components may exist as precursors necessitating activation within the body through unknown mechanisms (Olila, Olwa-Odyek and Opuda-Asibo 2001).
The qualitative phytochemical analysis of Z. chalybeum still needs to be exhausted. Although essential oils of Z. chalybeum have been analysed in three countries in Africa (Chagonda et al. 1994; Chisowa et al. 1999; Ocheng et al. 2015), more research is still needed in order to determine the constituents of other phytochemicals.
This could prove valuable for scientists and researchers seeking to identify novel chemical compounds responsible for the reputed applications of the plant. Differences in phytochemical quality and quantity could be attributed to climatic differences, seasonal differences, soil and the age of plants. The solvent used may also play a significant role in determining the chemicals extracted. It is known that phenolic compounds, flavonoids and alkaloids are easily extracted in high amounts by polar solvents such as methanol, ethanol, ethyl acetate and aqueous solvents (Iloki-Assanga et al. 2015). Non-polar solvents such as acetone, n-hexane, petroleum ether and diethyl ether are known to extract chemicals like liphophilic compounds including alcanas, waxes, colour pigments, sterols, several terpenoids and some alkaloids.
Herbal medicines have demonstrated efficacy in treating a range of infections, yet their safety has often been neglected. Although there are a few studies on phytochemical analysis and toxicity, Z. chalybeum extracts and phytochemicals may generally be toxic especially in higher concentrations, and this may be attributed by unknown compounds. The time of collection has a significant impact on the cytotoxicity of the plant. Muganga et al. (2010) collected samples, during the dry and rainy seasons. The samples collected during the dry season were less active (IC50 38.3 µg/mL) than those collected during the rainy season (IC50 4.2 µg/mL), suggesting that the rainy season is appropriate for the synthesis of active ingredients. Differences in toxicity assays may produce different results. Although the BSL assay is not a reliable method of testing toxicity because of the movement of live cells, which may result in wrongful counting, it could serve as a baseline for evaluating and contrasting the cytotoxic effects of different plants. There is, therefore, a need to standardise the toxicological properties of Z. chalybeum and their detailed clinical trials.
Conclusion
This review has established that Z. chalybeum is a valued medicinal plant species used by several local communities in East and Southern Africa. Despite its wide range of ethnomedicinal applications, more scientific evaluation still needs to be done to merge traditional and folkloric claims with scientific knowledge.
An understanding of Z. chalybeum phytochemicals and the determination of toxicities of potential phytochemicals is inevitable. The inhibition of the growth of ESKAPE pathogens by Z. chalybeum root barks is a major breakthrough that calls for more investigations of the plant as multi-drug resistant pathogens are a global concern. No studies have also been done to understand the molecular mechanisms of how Z. chalybeum phytochemicals lead to the death of these pathogens.
Acknowledgements
The authors would like to thank the Tshwane University of Technology for all the technical support.
Competing interests
The authors declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.
Authors’ contributions
F.M. conceived the main conceptual ideas and proof outline. S.M. collected the data and wrote the manuscript with support and supervision from F.M., and L.J.S. and C.K-M. were in consultation and supervision.
Ethical considerations
This article does not contain any studies involving human participants performed by any of the authors. Ethical clearance waiver received from the Ethics Committee-Faculty Committee for Research Ethics-Science (FCRE-SCI) Tshwane University of Technology FCRE 2022/05/002 (SCI) (FCPS 01).
Funding information
This research received no specific grant from any funding agency in the public, commercial or not-for- profit sectors.
Data availability
Data sharing is not applicable to this article as no new data were created or analysed in this study.
Disclaimer
The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of any affiliated agency of the authors.
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