Malaria in Guinean Rural Areas: Prevalence, Management, and Ethnotherapeutic Investigations in Dionfo, Sub-Prefecture of Labe^{[ # ]}

• Abstract
• Introduction
• Results
• Discussion
• Material and Methods
• Study area description
• Prevalence
• Parasitological assessment
• Ethnomedicinal/ethnobotanical investigations
• Ethnotherapeutic evaluation
• Plant material
• Preparation and administration
• Inclusion criteria
• Exclusion criteria
• Parasitological and clinical follow-up
• Ethical considerations
• Contributorsʼ Statement
• References

Abstract

As part of a validation program of antimalarial traditional recipes, an ethnotherapeutic approach was applied in Dionfo, a meso-endemic Guinean rural area where conventional health facilities are insufficient. A prevalence investigation indicated a malarial burden of 4.26%. Ethnomedical and ethnobotanical surveys led to a collection of 63 plant species used against malaria from which Terminalia albida (Combretaceae) was one of the most cited. Ethnotherapeutic evaluation of a remedy based on T. albida was applied to 9 voluntary patients suffering from uncomplicated malaria. Treatment of 7 to 14 days led to an improvement of clinical symptoms and a complete parasite clearance achievement of 8/9 patients without side effects. In addition to antiplasmodial activity in vitro and in vivo previously described, this study indicates an efficacy to support the antimalarial traditional use of T. albida, which could constitute a first-aid treatment when access to other medicines is delayed in the Dionfo community. Ethnotherapeutical investigation could be a valuable approach to guide subsequent investigations on traditional remedies.

Introduction

In Guinea, with a population of 12.6 million, malaria is endemic, and the burden is still not negligible. According to the Guinean Ministry of Health, with a prevalence of 44%, malaria is the primary cause of consultations (41%), hospitalizations (45%), and deaths (36%) in the global population of 12.6 million people [1], [2]. The majority of infections are caused by Plasmodium falciparum, the most dangerous plasmodium species causing the most severe form of malaria.

The national malaria strategy involves the free continuous distribution of long-lasting insecticide-treated nets (LLITNs) and artemisinin-based combination therapies, along with the rollout of rapid diagnostic tests (RDT) [3], [4].

But, inadequate applications of LLITNs, weak district management capacity, poor coordination, inadequate monitoring, and lack of training of key staff make health coverage low, especially in rural areas [5], [7].

It is well known that under low transmission intensity, Aremisinin-based Combination Therapies (ACTs) have an additional public health benefit of reducing the overall malaria transmission. But, among others, limiting factors are high cost, lack of suitable drug formulations, lack of post-marketing surveillance systems, and the imbalance between demand and supply [8]. Given that access to conventional medicine is still difficult in rural areas, the use of traditional herbal remedies is popular either by choice or by necessity. Consequently, there is a need for its closer integration into health systems. In this regard, the Declaration of Astana, adopted at the Global Conference on Primary Health Care in October 2018, made clear that the success of primary health care will be driven by applying scientific as well as traditional knowledge and extending access to a range of health care services, including traditional medicines [9]. Policymakers and consumers should consider how Traditional and Complementary Medicine (T&CM) may improve patient experience and population health. Aiming that, various declarations and invitations relating to the rational exploration and exploitation of the potential of traditional medicine have been made by international, regional, and national organizations [9], [10], [11], [12], [13]. But, understanding traditional medicine without understanding the broad outlines of the foundation of traditional society is not realistic [14]. Therefore, an ethnotherapeutic approach was adopted to evaluate an antimalarial traditional remedy widely used within rural communities of Dionfo, a sub-prefecture of Labé. Such an approach could be an alternative tool to assess the efficacy and security of traditional remedies within a specific community. Requiring a true upstream partnership between traditional healers and scientific investigators, the approach was articulated around 3 steps: a prevalence survey, ethnomedical and ethnobotanical investigations, and a therapeutic evaluation of the most popular recipe within the social context and conditions of the owner healer. Apart from its impact in situ, the results of ethnotherapeutic investigation are likely to guide subsequent biological and phytochemical research.

Results

The present study was carried out in 13 sites of Dionfo, a sub-prefecture of Labé in Middle Guinea. Of these, 12 localities are 3 to 13 km from Dionfo-Center. As indicated in [Table 1], the population (14,587 inhabitants) still lacks adequate health services: only 1 health center and 8 health posts, which were managed by 1 nurse and 10 technical health workers (i.e., 1 conventional health worker per 1326 inhabitants). A total of 540 subjects (47.04% men; 53.00% women) aged 1 to 94 y participated in the study, with a majority (359/540; 66.48%) of adults aged 45 and over and a minority (10/540; 1.85%) of children aged 1 to 5 y.

Most of the participating subjects (participants) were illiterate (84.25%; 455/540) and had a traditional lifestyle mainly based on agriculture and arts and crafts (95.37%; 515/540). Concerning Plasmodium species, only P. falciparum cases were detected. From the 540 participants, only 4.26% (23/540) or 4.62% (25/540) were diagnosed with malaria cases based on microscopic analysis or with RDTs, respectively ([Table 2]). Parasite load ranged from 319 to 1407 parasites/µL. Participants from 3 sites all tested negative. The highest burden was found in Balaya (3/17; 17.65%), Doubhel (5/51; 9.80%), and Dionfo Centre (3/42; 7.34%). Fever, pain, nausea, and vomiting were the main clinical signs observed. Regarding fever, 69.56% (16/23) of positive malaria subjects (patients) had a fever over 37.5 °C, with the highest temperature being 39.70 °C.

Only 16.29% (88/540) of participants exclusively used conventional medicine for their health needs. The availability of antimalarial drugs was largely insufficient. No regular distribution such as the first-line treatment of ACT has been reported. Access to drugs was generally only possible by supply from illegal markets like that of the prefecture of Labé. The distribution of LLITNs was free but sporadic and also insufficient in Dionfo. In addition, under the pretext of suffocation or a burning sensation, the use of LLITNs appears to be very low for both adults and children.

Knowledge of malaria was globally good in these communities. Transmission, symptoms, and risk factors were relatively known, although 35% (189/540) of participants felt under-informed. The majority of the population (i.e., 83.70% [452/540] use traditional medicine either by choice [77%, 348/452] or by necessity [23%, 104/452]).

Traditionally considered as a “weeks disease,” malaria is well known to the population through direct or indirect experience. The expression “malaria” has been adopted in vernacular languages and adapted to any symptom associated with a feverish state, headache, nausea, a bitter taste in the mouth, vomiting, lack of appetite, or shivering. Over the 13 visited districts, a total of 100 traditional practitioners of all skills have been reported: 55 healers and 45 herbalists (i.e., 146 inhabitants to 1 traditional practitioner ratio). As indicated in [Table 1], all the visited localities have a sufficient number of traditional practitioners compared to their respective populations. In addition, herbal self-medication is a common practice based on previous personal experiences.

During the ethnobotanical survey, a total of 98 participants (81 males and 17 females) aged between 40 and 75 y were interviewed. The survey conducted in collaboration with both traditional healers and consumers allowed to us to inventory antimalarial recipes based on 63 endemic plant species. Among these, 55 plant species belonging to 29 families were botanically identified ([Table 3]). Of these, the most frequently cited were Cochlospermum tinctorium A. Rich. (Cochlospermaceae), Terminalia albida Sc. Elliot. (Combretaceae), T. macroptera Guill. et Perr. (Combretaceae), Nauclea latifolia Sim. (Rubiaceae), and Aframomum melegueta K.Schum (Zingiberaceae) with 331, 274, 37, 32, and 31 citations, respectively.

In the management of malaria, C. tinctorium and T. albida were well known and enjoy a great reputation as “essential drugs” among traditional healers, herbalists, and consumers of all visited districts.

These plant species were mainly used in monotherapy and sometimes in combination with N. latifolia or Ficus spp, or Persea americana Mill. (Lauraceae) as biotherapy. The traditional recipes are prepared as a decoction (96%, 67/70) or maceration (61%, 43/70). The administration is generally oral and sometimes followed by a bath for a period of 3 to 14 days or continuous treatment until recovery. Regarding the right to collect samples in the area, C. tinctorium has been reported as a species specially protected by strict social regulations prohibiting the harvesting of roots during rainy seasons. In deference to this socio-cultural rule, our choice of ethnotherapeutic study has been focused on T. albida.

In situ assessment of antimalarial activity was considered for T. albida-containing recipes to promote safe and effective use of one of the most cited traditional antimalarial recipes within the Dionfo socio-cultural context. The study was conducted under the control of the traditional healer, owner of the recipe in terms of disease comprehension, plant species harvesting, preparation, and administration. As an antimalarial, the drug consisted of T. albida stem bark prepared as a decoction at a rate of approximately 1 kg of fresh bark in 5 liters of spring water. The dosage is a tea glass (around 100 mL), twice a day, for 7 days or 14 days (if not cured at day 7). The remedy was administered to 9 volunteer patients derived from the prevalence survey, all living in the targeted areas. They were 2 males (15 and 47 y old) and 7 women aged 23 – 66 y. All patients complied with the instruction in drinking the decoction as indicated and completed the study. A 21-day follow-up period was applied. Enrolled patients were followed weekly on days 7, 14, and 21. Administration of T. albida extract to patients suffering from uncomplicated malaria with a 21-day follow-up period led to a good clearance of the parasitemia and an improvement of the clinical status of 8 patients. After 7 days (d7) of treatment, parasitemia clearance was observed in 4/9 patients. On d14 and d21, clearance was noted in 3/5 patients and 1/2 patients, respectively. Overall, on d21, 8/9 were cleared of the parasites. As shown in [Table 3], only 1 patient remained malaria positive with an increase of parasite load from 890 to 1224 trophozoites/µL. Moreover, on day 21, all symptoms were well resolved in 4 patients. The persistence of 1 symptom (headache or stiffness) in 3 patients and 2 symptoms (headache with pain or fever) in 2 patients was recorded. At each control, the axillary temperature was normal for all patients except those of the patients with fevers of 37.80 °C (d7), 37.70 °C (d14), and 38.20 °C (d21). Regarding side effects, the treatment was well tolerated. No patient reported an adverse reaction requiring discontinuation of treatment. This antimalarial treatment was free of charge and thus cost-effective.

Discussion

In Guinea, due to a weak healthcare system, the majority of rural populations depend on traditional and herbal medicines for their healthcare needs. Although this study was conducted in the rainy season and in an area where conventional facilities were insufficient, the prevalence of malaria of 4.26% (23/540) was lower in Dionfo when compared with that of 27 – 34% at the national level or that of the meso-endemic area of the prefecture of Labé of 23 – 47% [1], [2], [3]. Of 10 children aged from 1 to 5 y, only 1 malaria case has been detected with 509 parasites/µL. This could be following the significant changes observed in the prefecture of Labé with a moderate prevalence of 37% in 2012 and a light one of 8% in 2016 [2], [3], [4]. This low prevalence in Dionfo could be the consequence either of a positive impact of the traditional recipes used in the Dionfo area or the result of a lifestyle that is well adapted and well adopted by the population, or the combination of these 2 factors.

In Dionfo, the treatment of malaria was based essentially on traditional medicine: 84% (452/540) of the interviewed participants were assumed to use predominantly traditional remedies to treat malaria or any kind of fever. Of these remedies, the rhizomes of C. tinctorium and the stem-bark of T. albida were the most common as traditional antimalarials.

Out of respect for a social rule prohibiting any harvest of C. tinctorium in the rainy season, our choice of ethnotherapeutic evaluation was carried out on T. albida stem bark which is endemic in the area.

Terminalia species in Guinea included T. albida, T. avicennioides Guill. & Perr, T.catalpa L, T. glaucescens Planch., T. ivorensis A. Chev, T. laxiflora Engl, T. macroptera Guil., T. mantaly H. Perr., T. mollis Laws., T. scutifera Planch., and T. superba Engl. & Diels-Limba. In Dionfo, T. albida and T. macroptera are endemic and widely distributed [15], [16]. Worldwide, the Terminalia genus. is distributed mainly in southern Asia, the Himalayas, Madagascar, Australia, and the tropical and subtropical regions of Africa, with around 250 species in Africa, 30 species in Ghana and 11 species in Guinea [14], [17], [18].

Beyond the ethnomedical and ethnobotanical studies, we used an ethnotherapeutic investigation to evaluate a traditional remedy based on a decoction of the stem bark of T. albida. Under the main auspice of the traditional ownerʼs recipe, such an approach was applied to 9 voluntary malarious patients. All patients complied with the instruction of drinking the decoction as indicated and completed the study. From d7 to d21, oral administration of the decoction (100 ml × 2 daily) led to a progressive parasitemia clearance and a decreasing axillary temperature (≤ 37.50 °C) in 8/9 patients, without significant adverse effects.

As shown in [Table 4], overall, 8/9 of the treated patients benefited from parasitological clearance and good clinical responses. Only 1 patient (15 y old) still positive on day 21 may have had a concurrent infection for which a medical examination in a conventional structure was suggested, with the guarantee that the costs related to this measure would be covered.

In Dionfo, T. albida and T. macroptera are both used as antimalarials and have a long history of use in human health maintenance, including the treatment of hepatobiliary diseases, diabetes, inflammatory diseases, chickenpox, hemorrhoids, and high blood pressure. However, T. albida (cited 274 times) was more popular as an antimalarial than T. macroptera (cited 37 times). It is noteworthy that in a previous study, T. macroptera was one of the plant species most cited as an antimalarial drug on the Guinean scale [1], [19].

Previous biological and phytochemical investigations were showed the antimalarial potency of T. albida as well as T. macroptera. In vitro, polar or apolar extract of T. albida stem bark had shown IC₅₀ values of 0.6 µg/mL [20], 1.5 µg/mL [21], 0.8 – 2.4 µg/mL [21] or 8.5 µg/mL [18]. In vivo, the extract of the stem bark of T. albida considerably increased the survival rate in mice infected with P. berghei and significantly decreased parasitemia. The antimalarial activity was related to anti-inflammatory properties, as T. albida treatment decreased the expression of pro-inflammatory markers in the brains of treated mice [22].

Regarding T. macroptera, roots and stem bark showed strong in vitro antiplasmodial activity (IC₅₀ = 2.46 – 2.70 µg/mL and IC₅₀ = 2.35 µg/mL, respectively) [18], [23]. In vivo, oral administration of root and stem bark extracts induced a significant reduction of parasitemia (37.2% and 46.4%, respectively) in P. chabaudi chabaudi-infected mice. In the cerebral malaria experimental model, mice treated with the roots and leaves presented 50% and 66.7% survival rates respectively at day 9 post-infection while all untreated mice died [24].

Among the other Guinean Terminalia species, strong in vitro antiplasmodial activity was recorded for the roots and stem bark of T. glaucescens (IC₅₀: 2.91 and 3.45 µg/mL, respectively), T. ivorensis (IC₅₀: 2.22 and 3.13 µg/mL, respectively), T. superba (IC₅₀: 2.39 and 5.23 µg/mL, respectively) and T. catappa (IC₅₀: 6.70 and 8.70 µg/mL, respectively) [18]. Worldwide, plants of the genus Terminalia are amongst the most widely used plants for traditional medicinal purposes [25]. Indeed, the genus Terminalia has received more attention to assess and validate therapeutic potential and clinical use due to its many folk medicinal and traditional applications. Of note, among these properties, antidiabetic, antiobesity, anticancer, anti-inflammatory, antimicrobial, antimalarial, antioxidant, and antitumor activities have been reported in several plant species [15]. T. chebula, a popular herbal remedy in India and South-East Asia, is called the “King of Medicine” in Tibet and is always listed at the top of the list of “Ayurvedic Materia Medica” because of its extraordinary property of healing [26]. Root bark decoctions of T. schimperiana (synonym T. glaucescens) are used in Nigeria to treat malaria and hepatitis [27]. Extract of T. avicennioides from Nigeria has been described to suppress malarial parasitemia at day 5 better than artesunate in P. berghei (NK-65) infected mice [28]. T. bellerica and T. chebula showed in vitro antimalarial activity (IC₅₀ values ranging from 14.33 ± 0.25 to 15.41 ± 0.61 µg/mL) along with good 4-day suppression activity ranging from 53.40% to 69.46% when tested on P. berghei-infected mice [20]. In vitro antiplasmodial activity of T. mantaly (IC₅₀ = 0.26 µg/mL) and T. superba (IC₅₀ = 0.57 µg/mL) has been reported [21].

Taking into account these data, it is interesting to note the same antimalarial use of Terminalia species in geographically remote places and by culturally different communities in Africa as well in Asia.

Chemical screening on T. albida stem bark extract indicated the presence of triterpenes, saponosides, flavonoids, and tannins. These constituents have been described in plant species of the genus Terminalia, along with phenylpropanoids and phenolic acids [16].

Phytochemical investigations on the root extract of T. albida led to the isolation and identification of 3,4,3′-tri-O-methyl-ellagic-acid, pantolactone, calophymembranside B, and a series of triterpenes (i.e., friedelin, sericic acid, arjunolic acid, arjungenin, arjunic acid, 2α,3β,21β,23-tetrahydroxyolean-12-en-28-oic-acid, terminolic acid, arjunglycoside I, arjunglucoside II, chebuloside II, sericoside, albidanoside A, 3β,19α,23-tetrahydoxy-11-oxo-olean-12-en-28-oic acid 28-O-β-D-glucopyranosyl ester, ivorenoside C, albidoside A, albidinolic acid, albidienic acid, albidolic acid, albidiolic acid, albidic acid A, albidic acid B, and albidic acid C [21].

From a bioassay-guided fractionation, the highest antiplasmodial activity was obtained for pantolactone with an IC₅₀ of 0.6 ± 0.03 µM. Good to moderate antiplasmodial activity was obtained with albidic acid B (IC₅₀ of 6,1 µM), albidic acid C (IC₅₀ of 6,1 µM), albidienic acid (IC₅₀ of 6,9 µM), ivorenoside C (IC₅₀ of 11,3 µM), albidic acid A (IC₅₀ of 10,1 µM), and 2α,3β,19α,23-tetrahydroxy-11-oxoolean-12-en-28-oic acid 28-Oβ-D-glucopyranosyl ester (13,9 µM) [29].

Beyond ethnomedical and ethnobotanical studies, ethnotherapeutic investigation could be a valuable approach to guide subsequent investigations on traditional remedies and to help in identifying the best method of giving priority to the clientʼs benefit. However, more preclinical and clinical studies are needed to establish standardization and quality control and to detect rare adverse events, which are especially important if this preparation is to be used widely beyond specific communities. In the meantime, T. albida could constitute a first aid treatment when access to other antimalarials is delayed in the Dionfo community.

Material and Methods

Study area description

The study was conducted in Dionfo, a sub-prefecture of 14,587 inhabitants, located 31 km from the prefecture of Labé (Guinea). Malaria is meso-endemic there, with intense transmission between May and November [4], [5]. All investigations were carried out from May 29 to September 1, 2014, on 13 sites viz Dionfo-center and 12 villages located 3 to 13 km from Dionfo-center.

Prevalence

A total of 540 participants were recruited. Malaria cases were confirmed either by microscopy or RDT.

Parasitological assessment

The parasitological test was made with the classical microscopic and RDT methods [30], [31]. A binocular microscope Optika B-157-AL was used. CareStart Malaria Pf(HRP2) Ag RDT RMOM-02571 from ACCESS BIO NJ 08873 USA was the RDT supplied by the Programme National de Lutte contre le Paludisme (National Malaria Control Program). The blood smears were examined by 2 microscopists. Parasites were counted per 500 leukocytes. Total parasite clearance was defined as no parasites seen by either microscopist. Microscopy samples were prepared and examined at the health center site of Dionfo.

Ethnomedicinal/ethnobotanical investigations

The ethnomedical and ethnobotanical data were collected from traditional healers and herbalists who are well known and recognized as professionals by their community.

Botanical identifications of plant species were made by the botanists of the Institute of Research and Development of Medicinal and Food Plants of Guinea (IRDPMAG).

Ethnotherapeutic evaluation

The study was a prospective 1-arm evaluation of the clinical and parasitological responses to directly observed treatment with T. albida among volunteers recruited from the prevalence survey.

Plant material

Plant material consisted of Boori billel stem bark harvested in Dionfo. Its botanical identification was done by the botanists from the “IRDPMAG-Dubreka” as T. albida. A voucher specimen was deposited at the Herbarium of the IRDPMAG with N°. 38HK457.

Preparation and administration

Under the conditions of the traditional healer, a decoction of the fresh bark of T. albida was prepared (about 1 kg in 5 L of water) and about 100 ml × 2 of the filtrate was administered orally, every morning and evening during 7 to 14 days.

Inclusion criteria

Consenting malarious patients having participated in the prevalence survey, living within the investigated areas and aged 15 y or more with parasitemia > 300 trophozoits/µL were included.

Exclusion criteria

We excluded women who were pregnant or breastfeeding, patients with severe malnutrition or who received antimalarial therapy within the previous 2 wk, those with an inability to take oral medication, and those experiencing continuous vomiting.

Parasitological and clinical follow-up

Parasitemia and clinical signs were determined on day 0, day 7, day 14, and day 21. Parasitemia was estimated by microscopic examination and counted at 0 (0 – 2 h). Parasites were counted per 200 leukocytes or per 500 leukocytes if there were fewer than 10 parasites per 200 leucocytes. All blood films were read by 2 qualified microscopists. Total parasite clearance was defined as no parasites seen when an absence of parasites was noted in a slide after 1 – 2 h of 100-field examination.

At each visit, patients were clinically examined by a nurse, and clinical parameters were recorded.

The main recorded symptoms related to baseline were fever, pain, aches, headache, nausea, and vomiting. The armpit (axillary) temperature was measured with an electronic thermometer (JOCCA) The treatment was provided free of charge. In case of aggravation of the health condition, the patient was fully supported by IRDPMAG.

Ethical considerations

Approval was obtained as an interventional investigation from the internal Ethics Committee of IRDPMAG, under N°04/EC/CRVPM/MESRS/2014; May 15, 2014.

Contributorsʼ Statement

Design of the study: A. M. Baldé; data collection: A. O. Balde, B. Bah, S. Traore, H. Barry, I. K. Sylla, S. Diallo; drafting the manuscript: A. M. Baldé, A. O. Balde; analysis and interpretation of the data: A. M. Baldé, A. O. Balde; redaction of the manuscript: A. M. Baldé; critical revision of the manuscript: S. Balde, M. S. Traore, M. A. Balde, A. Camara, B. Bah, F. Bah.

Conflict of Interest

The authors declare that they have no conflict of interest.

Acknowledgements

We are grateful to the healers, herbalists, and the people of Dionfoʼs rural communities for their cooperation in the study as well as the Programme National de Lutte contre le Paludisme (National Malaria Control Program).

^# Dedicated to Professor Arnold Vlietinck on the occasion of his 80th birthday.

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• 24 Cock IE. The medicinal properties and phytochemistry of plants of the genus Terminalia (Combretaceae). Inflammopharmacology 2015; 23: 203-229
  CrossrefPubMedSearch in Google Scholar
• 25 Bag A, Bhattacharyya SK, Chattopadhyay RR. The development of Terminalia chebula Retz. (Combretaceae) in clinical research. Asian Pac J Trop Biomed 2013; 3: 244-252
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• 26 Muluh EK, Lodiya MB, Muniratu M. Phytochemical analyses of Terminalia schimperiana (Combretaceae) root bark extract to isolate stigmasterol. Adv J Chem A 2019; 2: 327-334
  CrossrefPubMedSearch in Google Scholar
• 27 Omonkhua AA, Cyril-Olutayo MC, Akanbi OM, Adebayo OA. Antimalarial, hematological, and antioxidant effects of methanolic extract of Terminalia avicennioides in Plasmodium berghei-infected mice. Parasitol Res 2013; 112: 3497-3503
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• 28 Khosit P, Wanwarang H, Noppamas S, Krisada J, Seewaboon S, Siripen T. In vitro and in vivo antiplasmodial activity and cytotoxicity of water extracts of Phyllanthus emblica, Terminalia chebula, and Terminalia bellerica . J Med Assoc Thai 2010; 93 (Suppl. 07) S120-S126
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Correspondence

Publication History

Received: 30 January 2021

Accepted after revision: 30 May 2021

Article published online:
06 July 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

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  CrossrefPubMedSearch in Google Scholar
• 23 Traore MS, Diané S, Diallo MST, Balde EB, Balde MA, Camara A, Diallo A, Keita A, Cos P, Maes L, Pieters L, Balde AM. In-Vitro antiprotozoal and cytotoxic activity of ethnopharmacologically selected Guinean plants. Planta Med 2014; 80: 1340-1344
  Thieme ConnectPubMedSearch in Google Scholar
• 24 Cock IE. The medicinal properties and phytochemistry of plants of the genus Terminalia (Combretaceae). Inflammopharmacology 2015; 23: 203-229
  CrossrefPubMedSearch in Google Scholar
• 25 Bag A, Bhattacharyya SK, Chattopadhyay RR. The development of Terminalia chebula Retz. (Combretaceae) in clinical research. Asian Pac J Trop Biomed 2013; 3: 244-252
  CrossrefPubMedSearch in Google Scholar
• 26 Muluh EK, Lodiya MB, Muniratu M. Phytochemical analyses of Terminalia schimperiana (Combretaceae) root bark extract to isolate stigmasterol. Adv J Chem A 2019; 2: 327-334
  CrossrefPubMedSearch in Google Scholar
• 27 Omonkhua AA, Cyril-Olutayo MC, Akanbi OM, Adebayo OA. Antimalarial, hematological, and antioxidant effects of methanolic extract of Terminalia avicennioides in Plasmodium berghei-infected mice. Parasitol Res 2013; 112: 3497-3503
  CrossrefPubMedSearch in Google Scholar
• 28 Khosit P, Wanwarang H, Noppamas S, Krisada J, Seewaboon S, Siripen T. In vitro and in vivo antiplasmodial activity and cytotoxicity of water extracts of Phyllanthus emblica, Terminalia chebula, and Terminalia bellerica . J Med Assoc Thai 2010; 93 (Suppl. 07) S120-S126
  PubMedSearch in Google Scholar
• 29 Baldé MA, Tuenter E, Traore MS, Metheeussen A, Cos P, Maes L, Camara A, Haba NL, Gomou K, Diallo MST, Balde ES, Pieters L, Balde AM, Foubert K. Antimicrobial investigation of ethnobotanically selected Guinean plant species. J Ethnopharmacol 2020; 263: 113232
  CrossrefPubMedSearch in Google Scholar
• 30 Willcox ML, Graz B, Diakite C, Falquet J, Dackouo F, Sidibe O, Giani S, Diallo D. Is parasite clearance clinically important after malaria treatment in a high transmission area? A 3-mo follow-up of home-based management with herbal medicine or ACT. Trans R Soc Trop Med Hyg 2011; 105: 23-31
  CrossrefPubMedSearch in Google Scholar
• 31 Graz B, Willcox ML, Diakite C, Falquet J, Dackuo F, Sidibe O, Giani S, Diallo D. Argemone mexicana decoction versus artesunate-amodiaquine for the management of malaria in Mali: policy and public-health implications. Trans R Soc Trop Med Hyg 2010; 104: 33-41
  CrossrefPubMedSearch in Google Scholar