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Terminalia Macroptera Haidara et al. Malar J (2018) 17:68 https://doi.org/10.1186/s12936-018-2223-7 Malaria Journal RESEARCH Open Access In vivo validation of anti‑malarial activity of crude extracts of Terminalia macroptera, a Malian medicinal plant Mahamane Haidara1,2, Mohamed Haddad1, Adama Denou2, Guillaume Marti1, Sandra Bourgeade‑Delmas1, Rokia Sanogo2,3, Geneviève Bourdy1 and Agnès Aubouy1* Abstract Background: Plasmodium falciparum malaria is still one of the most deadly pathology worldwide. Efcient treatment is jeopardized by parasite resistance to artemisinin and its derivatives, and by poor access to treatment in endemic regions. Anti-malarial traditional remedies still ofer new tracks for identifying promising antiplasmodial molecules, and a way to ensure that all people have access to care. The present study aims to validate the traditional use of Termi- nalia macroptera, a Malian plant used in traditional medicine. Methods: Terminalia macroptera was collected in Mali. Leaves (TML) and roots ethanolic extracts (TMR) were pre‑ pared and tested at 2000 mg/kg for in vivo acute toxicity in Albino Swiss mice. Antiplasmodial activity of the extracts was assessed against a chloroquine resistant strain P. falciparum (FcB1) in vitro. In vivo, anti-malarial efcacy was assessed by a 4-day suppressive test at 100 mg/kg in two malaria murine models of uncomplicated malaria (Plasmo- dium chabaudi chabaudi infection) and cerebral malaria (Plasmodium berghei strain ANKA infection). Constituents of TMR were characterized by ultra-high-performance liquid chromatography coupled to high resolution mass spec‑ trometry. Top ranked compounds were putatively identifed using plant databases and in silico fragmentation pattern. Results: Lethal dose of TML and TMR were greater than 2000 mg/kg in Albino Swiss mice. According to the OECD’s Globally Harmonized System of Classifcation, both extracts are non-toxic orally. Antiplasmodial activity of T. macrop- tera extracts was confrmed in vitro against P. falciparum FcB1 strain with IC50 values of 1.2 and 1.6 µg/mL for TML and TMR, respectively. In vivo, oral administration of TML and TMR induced signifcant reduction of parasitaemia (37.2 and 46.4% respectively) in P. chabaudi chabaudi infected mice at the 7th day of infection compared to untreated mice. In the cerebral malaria experimental model, mice treated with TMR and TML presented respectively 50 and 66.7% sur‑ vival rates at day 9 post-infection when all untreated mice died. Eleven major compounds were found in TMR. Among them, several molecules already known could be responsible for the antiplasmodial activity of the roots extract of T. macroptera. Conclusions: This study confrms both safety and anti-malarial activity of T. macroptera, thus validating its traditional use. Keywords: Antimalarial activity, Terminalia macroptera, In vitro, Mice models, Plasmodium berghei ANKA, Plasmodium chabaudi, Toxicity *Correspondence: [email protected] 1 UMR 152 PHARMA‑DEV, IRD, UPS, Université de Toulouse, Toulouse, France Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Haidara et al. Malar J (2018) 17:68 Page 2 of 10 Background Methods Malaria is still one of the most deadly pathology world- Plant collection wide with 429,000 deaths reported in 2015 [1]. Africa Te leaves and roots of T. macroptera were collected in is by far the most afected region, accounting for 92% August 2015 from Siby village in the Koulikoro region of of malaria deaths. Despite a recent decrease in malaria Mali. Authorization for collection of plant materials at mortality due to extensive malaria control through insec- the Traditional Medicinal Department of the National ticide-impregnated bed nets and increased use of arte- Institute of Public Health (DMT/NIRPH) was obtained misinin derivatives, the state of artemisinin resistance prior to collection. After collection, botanical identifca- is highly worrying [2]. Artemisinin-based combination tion was confrmed at the national herbarium of DMT/ therapy constitutes the frst-line treatment for malaria NIRPH in Bamako, Mali. A specimen of the plant with in the large majority of countries in which the disease is voucher number (3752/DMT) was deposited in the her- endemic, and intravenous artesunate the most efcacious barium of DMT/NIRPH. treatment for severe malaria. However, Plasmodium falciparum has become resistant to almost all available Preparation of plant extracts anti-malarial drugs in Southeast Asia [3], and an isolate Terminalia macroptera leaves and roots were dried under originating from Equatorial Guinea has been recently shade at room temperature for 2 weeks and ground to found resistant to artemisinin [4]. New efective mol- a powder before extraction. A total of 250 g dried sam- ecules are thus urgently needed to combat this pathology. ples were macerated in 1 L of 90% ethanol for 24 h. Te Plants constitute a huge reservoir for bioactive mol- mixtures were fltered using Whatman flters No 1. ecules, as evidenced by the Cinchona tree and Artemisia Te unfltered residues were macerated in 90% etha- annua that contain quinine and artemisinin, respectively. nol for 24 h and fltered again as before. Tis operation Africa ofers an extremely rich fora and proposes numer- was repeated three times. Filtrates were combined and ous medicinal plants [5–7]. Terminalia macroptera is a evaporated in vacuo to dryness (Büchi® rotary evapora- Combretaceae (syn. Terminalia chevalieri, Myrobalanus tor Model R-200). Crude extracts of T. macroptera leaves macroptera) widespread in West Africa from Senegal (TML) and roots (TMR) were stored in the refrigerator at to Cameroon [8]. In Mali, T. macroptera is one of the 4–8 °C until use. Each extract was dissolved in methanol most cited plant used in traditional medicine to treat a to provide a stock solution (10 mg/mL) kept at 4–8 °C. large variety of diseases including malaria [9]. In addi- Before in vitro and in vivo experiments, stock solu- tion, traditional remedies allow an afordable access tion was dissolved in distilled water to provide working to anti-malarial drugs for the most deprived [10–13]. concentrations. First studies on T. macroptera have been performed in Guinea-Bissau, where extracts of roots and leaves dem- In vitro antiplasmodial activity onstrated antibacterial activities in vitro [14–16]. Its tra- Te in vitro anti-malarial activity of T. macroptera ditional anti-malarial use was frst reported from Burkina extracts was investigated using the SYBR Green I-based Faso; in vitro antiplasmodial activity of the total extract fuorescence assay [19]. Te asexual intra-erythrocytic of T. macroptera was confrmed (IC50 = 1 µg/mL for the stage of P. falciparum laboratory strain FcB1 (chloro- aqueous extract) [17]. Prepared from the plant collected quine-resistant strain) was maintained in RPMI 1640 in Guinea, the ethanolic root bark extract displayed a medium containing l-glutamine 200 µM, Hepes 25 mM moderate antiplasmodial activity (IC50 = 6.8 µg/mL) and 5% human serum (Etablissement français du Sang— [18]. However, in vivo anti-malarial activity of T. macrop- EFS, Toulouse, France) using the culture technique tera has not been assessed yet. Hence, this study aims to described by Trager and Jensen [20]. For anti-malarial validate the traditional use of T. macroptera roots and drug assays, stock solutions of plant extracts were diluted leaves against malaria, a potentially fatal disease, through serially in RPMI 1640 culture medium to test fnal con- a dual in vivo experimental approach aiming to mimic centrations between 1 and 100 µg/mL in triplicates in a uncomplicated malaria and cerebral malaria, the most 96-well plate. Final concentration of methanol was 0.5%. severe form of the disease. Tus, Plasmodium chabaudi A suspension of sorbitol-synchronized, infected red chabaudi and Plasmodium berghei strain ANKA infec- blood cells (iRBCs) was adjusted to 1% parasitaemia and tion in Albino Swiss mice, the respective experimental 2% haematocrit in complete medium and added to the models for uncomplicated and cerebral malaria, were wells. Negative controls were prepared with a suspension used to evaluate anti-malarial activity of root and leave of iRBCs and 0.5% methanol. Chloroquine was used as extracts of T. macroptera. Finally, the nature of the positive control. Test plates were incubated at 37 °C for major chemical compounds present in the plant was 48 h. Afterwards, 100 μL SYBR Green I fuorescent lysis investigated. bufer were added to each well and incubated in a dark Haidara et al. Malar J (2018) 17:68 Page 3 of 10 place at room temperature for 2 h. Fluorescence data (positive control) and distilled water (negative control). were acquired using a fuorescence plate reader (BMG On the 1st day (D0), mice were inoculated intraperito- Fluostar Galaxy Labtech) with excitation and emis- neally with 0.2 mL of infected blood containing about 6 sion wavelengths at 485 and 518 nm, respectively. Te 1 × 10 parasitized erythrocytes. Two hours after infec- fuorescence values (after subtraction of the background tion, the two tested groups of each infection model were fuorescence of the non-parasitized RBCs) were plotted treated orally with 100 mg/kg of TML or TMR. Positive against the log of the drug concentration, and analysed by and negative control mice received 5 mg/kg of chloro- non-linear regression (sigmoidal dose response/variable quine and 25 mL/kg of distilled water, respectively.
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