Medicinal Plants Used in Traditional Management of Cancer in Uganda: A Review of Ethnobotanical Surveys, Phytochemistry, and Anticancer Studies

Omara, Timothy; Kiprop, Ambrose K.; Ramkat, Rose C.; Cherutoi, Jackson; Kagoya, Sarah; Moraa Nyangena, Decrah; Azeze Tebo, Tsedey; Nteziyaremye, Papias; Nyambura Karanja, Lucy; Jepchirchir, Abigael; Maiyo, Alfayo; Jematia Kiptui, Betty; Mbabazi, Immaculate; Kiwanuka Nakiguli, Caroline; Nakabuye, Brenda Victoria; Chepkemoi Koske, Margaret

doi:https://doi.org/10.1155/2020/3529081

Evidence-Based Complementary and Alternative Medicine

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Abstract Introduction Results and Discussion Conclusions Disclosure Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2020 | Article ID 3529081 | https://doi.org/10.1155/2020/3529081

Medicinal Plants Used in Traditional Management of Cancer in Uganda: A Review of Ethnobotanical Surveys, Phytochemistry, and Anticancer Studies

Timothy Omara,^1,2,3Ambrose K. Kiprop,^1,3Rose C. Ramkat,^3,4Jackson Cherutoi,¹Sarah Kagoya,^5,6Decrah Moraa Nyangena,^1,3Tsedey Azeze Tebo,⁷Papias Nteziyaremye,^1,3Lucy Nyambura Karanja,^1,3Abigael Jepchirchir,^1,3Alfayo Maiyo,^1,3and Betty Jematia Kiptui^1,3 et al.

Academic Editor: Konrad Urech

Received29 Dec 2019

Accepted18 Feb 2020

Published16 Mar 2020

Abstract

The burden of neoplastic diseases is a significant global health challenge accounting for thousands of deaths. In Uganda, about 32,617 cancer cases were reported in 2018, accompanied by 21,829 deaths. In a view to identify some potential anticancer plant candidates for possible drug development, the current study was designed to compile the inventory of plants with reported anticancer activity used in rural Uganda and the evidences supporting their use in cancer therapy. An electronic survey in multidisciplinary databases revealed that 29 plant species belonging to 28 genera distributed among 24 families have been reported to be used in the management of cancer in Uganda. Anticancer plants were majorly from the families Bignoniaceae (7%), Caricaceae (7%), Fabaceae (7%), Moraceae (7%), and Rutaceae (7%). Most species occur in the wild (52%), though some are cultivated (48%). The growth habit of the plants is as trees (55%) or herbs (45%). Anticancer extracts are usually prepared from leaves (29%), bark (24%), roots (21%), and fruits (13%) through decoctions (53%), as food spices (23%) or pounded to produce ointments that are applied topically (10%). Prunus africana (Hook.f.) Kalkman, Opuntia species, Albizia coriaria (Welw. ex Oliver), Daucus carota L., Cyperus alatus (Nees) F. Muell., Markhamia lutea (Benth.) K. Schum., and Oxalis corniculata L. were the most frequently encountered species. As per global reports, Allium sativum L., Annona muricata L., Carica papaya L., Moringa oleifera Lam., Opuntia species, Prunus africana (Hook.f.) Kalkman, and Catharanthus roseus (L.) G. Don. are the most studied species, with the latter having vincristine and vinblastine anticancer drugs developed from it. Prostate, cervical, breast, and skin cancers are the top traditionally treated malignancies. There is a need to isolate and evaluate the anticancer potential of the bioactive compounds in the unstudied claimed plants, such as Cyperus alatus (Nees) F. Muell., Ficus dawei Hutch., Ficus natalensis Hochst., and Lovoa trichilioides Harms, and elucidate their mechanism of anticancer activity.

1. Introduction

Cancer ascribes a collection of diseases triggered by the uncontrolled proliferation of malignant cells. It is a global health burden that has left anintolerable death toll worldwide. Conservative estimates indicate that cancer (of the liver, breasts, lungs, cervix uteri, stomach, and colorectal) causes about 13% of annual deaths globally [1]. In Uganda, there have been reports on cancer cases, though collected data are not usually coherent [2]. The commonest types of cancer encountered in Uganda include cervical, prostate, breast, lung, and skin cancers, Kaposi sarcoma, Burkitt’s lymphoma, and cancer of the bone, eye, colon, and blood (leukemia) [3]. Between 1952 and 1953, 796 cases of cancer were reported in Uganda, 15 of which were stage IV cases of cancer of the cervix uteri [4]. The 1990s recorded Kaposi sarcoma, prostate, and oesophageal cancers among men and Kaposi sarcoma, cervical, and breast cancers among women as the most prevalent cancers in Uganda [5].

The eruption of the ill-fated virus (HIV) and the AIDS epidemic led to an unprecedented increase in the incidences of Kaposi sarcoma, squamous cell carcinoma of the conjunctiva, and non-Hodgkin’s lymphoma in the penultimate year [6]. Cervical cancer, the fourth most prevalent cancer globally, subsequently registered an alarming relative frequency in Uganda, with 3, 915 new cases and 2, 275 annual deaths reported [7, 8]. The situation is complicated by the fact that very few (averagely less than 10% of the 10.22 million susceptible Ugandan females) have been screened for cervical cancer [7, 9]. Reluctancy to screen, stigma, lack of awareness, chronic poverty, and inadequate medical services are largely responsible for the magnitude of the cancer epidemic in Uganda [9–11]. Thus, most cancer cases registered in hospitals are usually in their advanced stages that cannot be treated optimistically [12, 13].

Cancer trends for two decades (1991–2010) in the Kampala cancer registry have indicated that there has been an increase in cancer cases, peculiarly for breast cancer and prostate cancer in women and men, respectively [14]. On the other hand, the incidence of the oesophagus, liver, and large bowel (colon, rectum, and anus) cancers has remained relatively constant [14]. According to a recent report based on Gulu and Kampala cancer registries [15], 32,617 cancer cases were registered in the country in 2018 and about 21,829 of these victims succumbed to death. In Uganda, the survival of cancer patients is alarmingly deplorable in comparison to other non-African third world nations [2, 16]. The risk factors cited for the high cancer incidences in Uganda include acquisition from family lines, hormonal imbalances, consumption of mycotoxin (aflatoxin) contaminated foods, exposure to chemicals, irradiation, viruses, and bacteria [3, 17–19].

Conventional therapies for the management of cancer have several side effects due to their lack of specificity and are limited in rural settings [20]. Further, the sturdy resistance of cancerous cells to cytotoxic and antineoplastic drugs has presented a fresh challenge, giving unsatisfactory ministration outcomes and capricious resistance to antineoplastic agents [21, 22]. Coupled with the prohibitive costs, unavailability of allopathic drugs, and chronic poverty in Uganda, there is a need to fold back on home grown solutions, exploring flora and fauna [23]. Uganda, the pearl of Africa, is part of the East African botanical block and is blessed with over 6,000 plant species [24, 25]. Plants are regaining shape and emerging as an integral part of the ethnomedical approach for the management of diseases in Uganda [26]. The most cathartically notable anticancer botanical species in Uganda are Prunus africana (Hook.f.) Kalkman and the periwinkle plant (Catharanthus roseus (L.) G. Don) from which antitumor drugs vinblastine and vincristine have been developed [23, 27]. Over 5,000 phytochemicals such as phenolics, carotenoids, glucosinolates, terpenoids, and alkaloids from over 3,000 plant species have been reported to be key actors in cancer therapy [28–30]. In Uganda, anecdotal reports reveal that there exists a pool of plants utilized locally for the management of cancer [23]. Indeed, information on indigenous medicinal plants used for various maladies has been reported by preceding authors, but none of them scrutinized anticancer plants. This review seeks to obtain a list of medicinal plants reported by ethnobotanical surveys in Uganda as anticancer plants and identify the active phytochemicals in the claimed plants and the anticancer studies done on them as per global studies. Potential candidates from this review which are scantily studied will be investigated in penultimate studies.

2. Methodology

A comprehensive literature search was performed in Scopus, Web of Science Core Collection, PubMed, Science Direct, Google Scholar, and Scientific Electronic Library Online (SciELO) from August 2019 to November 2019 following procedures previously employed elsewhere [26]. The search was performed independently in all databases. The study databases included original articles published in peer-reviewed journals, books, thesis, dissertations, patents, and other reports covering anticancer plants, dated until November 2019. All publishing years were considered, and articles with information on cancer or medicinal plants in Uganda were given utmost priority. Thus, references contained within the returned results were assessed concerning their inclusion in this study, and further searches were carried out at the Google search engine using more general search terms, to broaden the search, as follows: words cancer, plants, plant extract, vegetal, vegetal species, vegetal extract, traditional medicine, alternative medicine, complementary therapy, natural medicine, ethnopharmacology, ethnobotany, herbal medicine, herb, herbs, decoction, infusion, macerate, cancerous, hepatocellular carcinoma, carcinoma, prostate cancer, breast cancer, Kaposi sarcoma, Burkitt’s lymphoma, cancer of the bone, cancer of the eye, cancer of the colon, cancer of the blood, leukemia, anticancer, cancer of the cervix uteri, lung cancer, liver cancer, skin cancer, and Uganda were used. The last search was done on 25^th November 2019. The search outputs were saved where possible on databases and the authors received notification of any new searches meeting the search criteria from Science Direct, Scopus, and Google scholar.

3. Results and Discussion

Only articles in English and local languages were considered. After the multidisciplinary database and Google search engine result assessments, sixteen reports of interest specifically on the subject of anticancer plants in Uganda were retrieved (Table 1). The botanical names of the plants listed were vetted in botanical databases: The Plant List [47], International Plant Names Index (IPNI) [48], NCBI taxonomy browser [49], and Tropicos [50]. Where a given species was considered as distinct species in different reports, the nomenclature as per the botanical databases above took precedence in the review. The botanical families used, the plant local names (Lango, Ateso, Luganda, Rukiga, Rutoro, Lusoga, Lugisu, Ngakarimojong, and Lugbara), the life forms, part(s) used, conservation status, preparation and administration mode, and the districts where the plants were reported are captured (Table 1). On anticancer potential, species studied as per global reports, the active phytochemicals reported and tested with positive results in the plant species identified by this review are reported (Table 2; Figure 1). A brief review of other ethnomedical uses of the reported species as per Ugandan and global studies is also presented (Table 3).

(a)

(b)

3.1. Traditional Concept of Cancer in Uganda

From the electronic survey, it is clear that local communities in Uganda have some information about cancer. Not all Ugandans are fully aware of cancer because most information on it is disseminated through television and radio stations which not all have access to. Another striking challenge is that there is no word for cancer in any of the Ugandan local languages. Thus, many ignore cancer because it is not anywhere recited as a health problem in their local vocabulary [16]. To many, being diagnosed with any type of cancer is equated to receiving a death sentence [234]. Some believe that conventional treatments usually cause cancer to spread, fastening the death of victims [16]. In addition, due to the ever-changing landscape of available treatment options, most patients believe that cancer can only be cured using herbal medicine and the best way to deal with cancers is through prevention [23]. Many Ugandans assume that herbal products are safer to use than allopathic drugs. In Northern Uganda, the use of shea (Vitellaria nilotica) butter, simsim (Sesame indicum L.), and groundnut (Arachis hypogea L.) pastes as substitutes for refined cooking oil and vaseline with the belief that the latter are carcinogenic is known. Unfortunately, recent reports have pointed out that some of these food items are contaminated with mycotoxins, particularly aflatoxins which are potential carcinogens [19, 235].

3.2. Anticancer Plants Used in Local Communities of Uganda

Cancer chemoprevention which involves the inhibition or reversion of cancer through the administration of natural or synthetic agents has gained a wider audience in Uganda. Chemopreventive agents may inhibit cancer development either by limiting exposure to carcinogens (carcinogen formation inhibitors and blocking agents) or by decreasing tumor promotion or progression stages (suppressing agents) [236]. Many compounds from medicinal or dietary plants have been reported as chemopreventive agents capable of inhibiting DNA damage and retarding or reversing carcinogenesis in in vitro and in vivo bioassays [237].

From our survey, 29 plant species from 28 genera belonging to 24 botanical families claimed as anticancer plants in Uganda have been reported (Table 1). The most cited families were Bignoniaceae (7%), Caricaceae (7%), Fabaceae (7%), Moraceae (7%), and Rutaceae (7%). Most families encountered in this study have reported use in the traditional management of cancer in other countries across the globe. For example, Apocynaceae, Asteraceae, Bignoniaceae, Caricaceae, Fabaceae, Malvaceae, Meliaceae, Moraceae, Rutaceae, Sapindaceae, and Solanaceae were cited in Kenya [170], Ethiopia [238], Tanzania [97], and Near East (Arabian Peninsula, Egypt, Iraq, Iran, Israel, Jordan, Lebanon, Palestinian territories, Syria, and Turkey) [239], Lamiaceae in Morocco [240], and Apocynaceae, Meliaceae, and Malvaceae in Sri Lanka [241].

In addition, some of the plant species recapitulated have been documented in the treatment of cancer globally; for example; Carica papaya L., Catharanthus roseus (L.) G. Don, and Prunus africana (Hook.f.) Kalkman were reported to be used for traditional treatment of cervical, colorectal, prostate, and breast cancers [114, 170, 242] while Albizia coriaria Welw. ex Oliver, Capsicum frutescens L., and Kigelia africana (Lam.) Benth. has been reported for the treatment of squamous cell carcinoma, throat, and breast cancers in Kenya [170]. Zanthoxylum chalybeum Engl. is used in Ethiopia and Tanzania for the treatment of breast and cervical cancers [97, 243], Blighia unijugata Baker is used for the treatment of breast and cervical cancers in Tanzania [97], while Cymbopogon citratus (DC.) Stapf is used against colorectal cancer in Kenya [170]. Interestingly, some of these plants are consumed as food spices; for example, Cymbopogon citratus (DC.) Stapf is used by most communities in Northern Uganda who cannot afford tea (Camellia sinensis (L.) Kuntze) leaves, and Beta vulgaris L. and Daucus carota L. are common ingredients in Ugandan culinary recipes [93]. Indeed, epidemiological studies have supported that dietary intake of fruits, vegetables, and teas tends to lower the risk of human cancers [244].

Further, some of the botanical species have been reported as recipes of anticancer preparations in other countries. For example, P. africana stem bark is used in combination with Harungana madagascariensis Lam. ex Poir, Zanthoxylum gilletii (De Wild.) P.G. Waterman (stem bark), Spathodea campanulata P. Beauv, and Vernonia lasiopus O. Hoffman (stem bark), and P. africana (stem bark and roots), Aloe volkensii leaves, Spathodea campanulata P. Beauv (leaves and stem bark), and Harungana madagascariensis Lam. ex Poir (stem bark) boiled with Trichilia emetica Vahl. are used for the treatment of skin, breast, and colorectal cancers in Kenya [170]. Similarly, Markhamia lutea (Benth.) K. Schum stem bark alone or in combination with Albizia gummifera stem bark and Conyza sumatrensis (Retz.) E.H Walker leaves is used in the management of squamous cell carcinoma of the gums, colorectal, throat, and breast cancers in Kenya [170]. In Tanzania, Kigelia africana (Lam) Benth. stem bark mixed with approximately equal weights of root barks of Maclura africana (Bureau) corner, Harrisonia abyssinica Oliv., and Warburgia stuhlmannii Engl. is drunk for the treatment of breast, liver, and colon cancers [97]. Euclea natalensis A. DC. root bark boiled with the root barks of Harrisonia abyssinica is drunk as a treatment for leukemia in Tanzania [97].

Some of the plants have been reported to have cytotoxic and antitumor properties (Table 2) and many possess other ethnomedical applications (Table 3) both in Uganda and internationally. Interestingly, the isolation, characterization, and purification of the anticancer and cytotoxic phytoconstituents have been successfully done in some species (Figure 1). Striking examples are Prunus africana (Hook.f.) Kalkman which have been patented in France for the management of prostate cancer [245] and Catharanthus roseus (L.) G. Don from which the commercial anticancer drugs vincristine and vinblastine have been developed [246].

Phytochemicals from plants are reported to be effective against cancer cells because they have many molecular targets [247]. For example, -sitosterol present in P. africana has been shown to exhibit anti-inflammatory, antineoplastic, and immunomodulating activities [248]. It is worth mentioning that antioxidant activities and antitumor or anticancer properties of plant extracts are always reported concomitantly in several plants [166], and some studies demonstrated that there is a positive linear relationship between antioxidant activity and anticancer effect of plant extracts [249]. Plant phytochemicals such as artemisinin from the Artemisia genus are reported to have an endoperoxide moiety which is strategic for their bioactivity. The cleavage of this is reported to produce reactive oxygen species, inducing oxidative stress. Furthermore, in the presence of ferrous iron or reduced heme, artemisinin can convert itself into cytotoxic carbon-centred radical, a highly potent alkylating agent, to induce direct oxidative damage to cancer cells [250, 251]. Thus, they are reported to induce apoptosis and ferroptosis, reduce cell proliferation through cell cycle arrest, and inhibit angiogenesis and tissue invasion of the tumor as well as cancer metastasis [184, 250, 251].

3.3. Growth Habit, Parts Used, Preparation, and Mode of Administration

Most anticancer plant species reported in Uganda occur in the wild (52%) though some are cultivated (48%). The growth habit of the plants is as trees (55%) or herbs (45%). Anticancer extracts are usually prepared from leaves (29%), bark (24%), roots (21%), fruits (13%), seeds (5%), bulb (5%), or rhizomes (3%). The regular use of roots and leaves in traditional medicine is a characteristic feature of materia medica in Uganda [26]. As reported elsewhere [238, 240], embryonal plant parts such as fruits, seeds, buds, bulbs, and flowers which are reported to accumulate bioactive compounds are less frequently used in anticancer therapy in Uganda.

Usually, anticancer preparations are presented as decoctions and teas (53%) and spices eaten in food (23%) or pounded to produce ointments that are applied topically (10%). The plants are collected from the wild, cultivated fields, or home gardens when needed. Traditional medicine practitioners either collect herbal plants personally or hire collectors. All traditional medical practitioners cultivate some medicinal plants especially fast growing ones around their homes and shrines in order to have them within easy access when needed [26]. The preparations are majorly administered orally, except in cases of skin cancers where they are applied topically as ointments.

3.4. Other Ethnomedicinal Uses and Toxicity of the Reported Anticancer Plants

Almost all the plants recapitulated in this review are employed for the treatment of various ailments other than cancer. Albizia coriaria (Welw. ex) Oliver used in the management of venereal diseases (syphilis, HIV, and gonorrhoea), postpartum haemorrhage, sore throats, menorrhagia, threatened abortion, skin diseases, jaundice, cough, and sore eyes [33, 179] is a good representative example. Such plants tend to be used in different communities for treating cancer and can be a good justification for their pharmacological efficacy [26].

On the other hand, some of the anticancer plants cited exhibit marked toxicity. A striking example is Catharanthus roseus (L.) G. Don. The alkaloids in it are neurotoxic, especially vincristine [252]. Vincristine and vinblastine are highly toxic antimitotics, blocking mitosis in metaphase after binding to the microtubules [253]. Evidently, side effects such as myelosuppression, alopecia, abdominal cramps, constipation, nausea, paralytic ileus, ulcerations of the mouth, hepatocellular damage, kidney impairment, pulmonary fibrosis, urinary retention, amenorrhoea, azoospermia, orthostatic hypotension, and hypertension [254–256] have been reported for the commercial drugs vincristine and vinblastine derived from this plant. In essence, the administration of these drugs must be carefully controlled to reduce the side effects [257]. This observation explains, in part, why some anticancer preparations in Uganda are applied topically or ingested in small amounts. Fortuitously, topical application is a better approach for reducing the local action of cancer cells at externally affected parts.

3.5. Clinical Studies

At present, clinical trials utilizing standardized extracts of anticancer plants reported in Uganda or their bioactive compounds have not been done with the exception of Prunus africana (Hook.f.) Kalkman and Catharanthus roseus (L.) G. Don. which have been investigated in other countries [245, 246]. Prostafx, Tadenan, and Pygenil are some of the herbal preparations of Prunus africana (Hook.f.) Kalkman on the market. Due to the paucity of data generated from preclinical tests (pharmacokinetic and toxicological studies) and the regulatory requirements for clinical studies, the safety and efficacy of traditional anticancer plant preparations used in Uganda remain a secret yet to be unveiled. Although there are many research institutes such as Uganda Virus Research Institute, Natural Chemotherapeutic Research Institute, Uganda Industrial Research Institute, and National Agricultural Research Institute, none is designed to have an in-depth focus on drug discovery and development to the level of commercialization. Thus, the government of Uganda should establish an institute that handles drug discovery and development to enhance the utilization of medicinal plants in Uganda.

4. Conclusions and Recommendations

The inventory of plants utilized by Ugandan communities presents considerable potential for the treatment of cancer. Cyperus alatus (Nees) F. Muell, Ficus dawei Hutch, Ficus natalensis Hochst, and Lovoa trichilioides Harms are some of the plants with claimed anticancer potential that have been hardly studied and therefore warrant further investigations. More ethnobotanical surveys should be done in the unsurveyed districts to identify other potential anticancer plants. Albizia coriaria Welw. ex Oliver which doubles as an antivenin plant will be investigated for its anticancer potential in a penultimate study.

Disclosure

Timothy Omara and Sarah Kagoya are co-first authors.

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Authors’ Contributions

Timothy Omara and Sarah Kagoya contributed equally.

Acknowledgments

TO, DMN, PN, LNK, AJ, AM, BJK, IM, CKN, and MKC are grateful to the World Bank and the Inter-University Council of East Africa for the scholarship awarded to them through the Africa Center of Excellence II in Phytochemicals, Textiles, and Renewable Energy (ACE II PTRE) hosted at Moi University that prompted this concerted ethnomedical communication. The authors commend preceding authors for their useful quest for knowledge on medicinal plants in Uganda, the reports of which this study was based.

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Copyright © 2020 Timothy Omara et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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