Total Alkaloid content and In vitro Antiplasmodial activity of Grangea maderaspatana collected from Burkina Faso
Yougoubo Abdoulaye1*, Dabiré Constantin M.1,2, Sore Harouna3, Bationo K. Remy1,4,
Ganame Arouna1, Sawadogo Assétou5, Roamba Noëlle Edwige6, Bazié Benjamin1,
Kabore S. Dominique1, Koala Moumouni1,7, Palé Eloi1, Nebie C. H. Roger4, Nacro Mouhoussine1
1Laboratoire de Chimie Organique et de Physique appliquées.
Université Joseph KI-ZERBO, 03 BP 7021 Ouagadougou 03, Burkina Faso.
2Laboratoire de Chimie et Energies Renouvelables,
Université Nazi BONI. 01 BP 1091. Bobo-Dioulasso 01, Burkina Faso.
3Centre National de Recherche et de Formation sur le Paludisme (CNRFP)
01 BP 2208 Ouagadougou 01, Burkina Faso.
4Institut de Recherche en Sciences Appliquées et Technologies (IRSAT), Centre National de la Recherche Scientifique et Technique (CNRST) 03 BP 7023 Ouagadougou 03, Burkina Faso.
5Laboratoire de Recherche et d’Enseignement en Santé et Biotechnologies Animales,
Université Nazi BONI. 01 BP 1091. Bobo-Dioulasso 01, Burkina Faso.
6Laboratoire de Biochimie. Biotechnologie, Technologie Alimentaire et Nutrition.
Université Joseph Ki-ZERBO, 03 BP 7021 Ouagadougou 03, Burkina Faso.
7Institut de Recherche en Sciences de la Santé (IRSS), Centre National de la Recherche Scientifique et Technique (CNRST) 03 BP 7047 Ouagadougou 03, Burkina Faso.
*Corresponding Author E-mail: yougabdou@gmail.com
ABSTRACT:
Malaria is a blood parasitosis transmitted to humans by the bite of an infected female anopheles mosquito. It is caused by intraerythrocytic protozoa of Plasmodium genus. Malaria remains a public health problem in Sub-Saharan Africa as it is one of the major causes of morbidity and mortality. According to WHO report, 241 million people are victims of this disease in the world, 95% of which are in Africa1. In Burkina Faso, out of 12,231,036 cases of malaria, 605,504 severe cases causing 4,355 deaths were recorded in 20212. To overcome this scourge, multidisciplinary research involving destruction of breeding sites, biological science, genetic science, and chemical science is being implemented3. Despite the combination of control methods, the number of cases still remains high and worrisome.
Plants are potential sources of bioactive molecules that can fight malaria. According to WHO, nearly 80% of populations in developing countries use plants to prevent and/or cure certain diseases4. To fight malaria, research on plants led to the discovery of quinine, which is the first antimalarial molecule. Quinine is an alkaloid isolated from the bark of a traditional South American plant (Cinchona). This is same to artemisinin a lactone isolated from Artemisia annua, a traditional Chinese medicine plant currently used in malaria control5. However, limited number of antimalarial molecules and the emergence of resistance in Plasmodium strains observed in recent years constitute a big concern. Thus, the search for new antimalarial molecules is urgent. Many reports on plants are undertaken throughout the world to identify new antimalarial molecules. Africa in general, and Burkina Faso in particular, is rich in medicinal plants. This is the case of Grangea maderaspatana, an aromatic plant belonging to Asteraceae family used by the populations for its numerous pharmacological properties. This aromatic plant is traditionally used to treat several pathologies such as eye and ear pain, headache6, paralysis, hepatitis, muscle and joint pain7-8. The roots of this plant are reported to be an aperient, gut astringent, diuretic, anthelmintic, emmenagogue, and galactagogue7-9. Essential oil of this plant was reported to be a good source of antioxidants with excellent antimicrobial properties10-11. Similarly, organic extracts from plant organs are rich in secondary metabolites and antioxidant compounds including phenolic compounds in general and flavonoids in particular12. Although there are many interests in this plant, few works, to our knowledge were reported on total alkaloid contents and antiplasmodial activity of extracts of different parts of this plant. This work aimed to investigate on total alkaloid contents and antiplasmodial activity of different part (roots, flowers, leafy branches) extracts of G. maderaspatana.
MATERIAL AND METHODS:
Plant material:
Plant material included flowers, roots, leafy branches and the whole plant of G. maderaspatana, collected in Ouagadougou district (12°23’32,16624’’N, latitude; 1°32’33,04896’’W, longitude). The different parts of the plant were shade dried separated and then ground into powder. Plant was identified by Professor Adjima THOMBIANO and a specimen was deposited at Joseph KI-ZERBO University of Burkina Faso herbarium.
Biological material:
Biological material included CQ-sensitive strain D10 and CQ-resistant strain Dd2. The following reagents were obtained through BEI Resources, NIAID, NIH: Plasmodium falciparum, Strain Dd2, MRA-150 and D10, MRA-201, contributed by ATCC. Parasite strains were maintained in continuous culture by Trager and Jensen method13 under sterile conditions in a laminar flow hood. Parasites were maintained in culture in 25cm3 flasks at 2% hematocrit in RPMI 1640 medium containing 24mM sodium bicarbonate, 0.01% hypoxanthine, 20mM HEPES and 2mM glutamine at 37°C. The contents of the flasks were gasified with a mixed gas (5% CO2, 2% O2 and 93% N2). Cultures were placed in a CO2 HERACELL 150 incubator at 37°C and 80% humidity. The culture medium was renewed every 24h and the parasitaemia was assessed by Giemsa-stained smears.
Methods:
Preparation of extracts:
The extracts were obtained by successive exhaustion using increasing polarity solvents: hexane, dichloromethane, ethyl acetate and methanol. Indeed, 100g of each plant part were macerated with 500ml of solvents and each extraction experiment was repeated three times. The filtrates obtained were combined and concentrated under reduced pressure to dryness using a rotary evaporator. Extraction yield was calculated using the following formula: yield (%) = (m/M)x100. M: plant material mass; m:mass of the extract obtained
Determination of total alkaloids contents:
Total alkaloids contents of G. maderaspatana extracts were determined by the method described by Ajanal et al14 adapted for a microplate reader. A mixture of 69.8mg of bromocresol green, 3mL of a 2N NaOH solution and 5mL of distilled water was prepared by heating until complete dissolution. Then, a dilution with distilled water is performed to obtain 1L of solution. To 5mL of this solution 0.4mL of the extract and 5mL of sodium phosphate buffer solution at pH 4.7 were successively added. After stirring the mixture, the formed complex is extracted with 10mL of chloroform. The absorbance of the yellow complex of each extract is read at 470nm using a spectrophotometer type MP96, SAFAS against a blank. The contents, expressed in micrograms of quinine equivalent per gram of extract (µg qE/g) are obtained by relating the absorbances read to the standard curve (y = 0.0291x + 0.056; R2= 0.9977) previously established from the quinine used as reference.
Antiplasmodial activity:
a) In vitro evaluation of antiplasmodial activity:
Antiplasmodial activity was determined according to Annalisa et al15. Stock solutions of extracts are prepared at concentrations of 10mg/mL in dimethyl sulfoxide (DMSO). From these concentrations, solutions of 100 µg/mL in complete culture medium are prepared under sterile conditions. From these solutions, cascade dilutions are performed in a microplate (96 wells) containing 100µL of complete culture medium. Then, 100µL of 2% parasitized blood and 2% hematocrit are added to the different concentrations of the extracts. Each dilution is tested in duplicate and the experiment is repeated three times. Control wells containing no extract (positive control) and healthy red blood cells (negative control) were also prepared. The microplate is stored in a jar and supplied with mixed gas. The whole set was placed in the CO2 incubator at 37°C for 72hours.
Antiplasmodial activity of the extracts is determined by enzyme-linked immunosorbent assay (ELISA) based on the quantification of pLDH (plasmodium Lactate Deshydrogenase) present in the culture. For this purpose, 100µL of the MALSAT solution is introduced into all the wells of a new microplate, 20µL of the NTB/PES solution is added in the dark. Then 25µL of the supernatant from each homogenized well of the test plate is added to each well of the new plate. After another 10 minutes incubation at room temperature protected from light, the absorbances are read at 650nm using a spectrophotometer type ELx808-BIOTEX. The Gen5 Fisher Scientific software version 1.10 is used to draw the inhibition curves which allow the determination of the IC50.
Parasites would hardly grow if the extract generates hemolysis. Thus, the observed antiplasmodial effect would not reflect extract action on the plasmodium. It is so important to make hemolysis test. Performing the hemolysis test makes it possible to verify the absence of false positives with human erythrocytes and to avoid unnecessary bioguided fractionations by detecting "false positive" results.
b) In vitro hemolysis tests:
Hemolytic activity of the extracts expressed as a percentage (%) is determined by the method described by Laurencin et al16 and Séverine et al17. In EDTA tubes (50mM) are collected 5mL of human blood and the whole set is kept in an ice bath. The contents of each EDTA tube are transferred to a 15mL falcon tube and washed with Phosphate Buffered Saline (PBS) at pH 7.4. The whole set is centrifuged at 2200rpm at 4°C for 15min. This operation is repeated in duplicate after removal of the supernatant. The density of the pellet obtained is adjusted to 1.5 at 550nm by spectrophotometer. At room temperature, the pellet is diluted to 10% (v/v) in PBS buffer. In order to verify that the red blood cells are still in whole after this operation, mixtures called positive control (10μL of 20% Triton X-100 + 190μL of 10% red blood cells) and negative control (10μL of PBS + 190μL of 10% red blood cells) are centrifuged at 2200rpm for 5min. The positive control should contain no pellet while the negative should have a clear supernatant and a red pellet.
Hemolytic test of the extracts required the preparation of two stock solutions from each extract (50µg/mL and 100µg/mL) in PBS buffer. Then, to 10µL of each stock solution placed in eppendorf tubes. 190µL of 10% red blood cells were added, Each sample is in triplicate including the positive and negative controls. Then, all tubes are incubated at room temperature with slow shaking for 1 hour and centrifuged at 2200rpm for 5min. 150µL of the supernatant from each centrifuged tube is placed in a multiwell plate (96 wells). The absorbance is read at 550nm with a plate reader type ELx808-BIOTEX. The experiment is repeated three times.
The percentage of hemolysis is calculated using the following formula:
A(sample tested)-A(negative control)
% Hemolysis= -------------------------------------- x100
A(positive control)-A(negative control)
A: absorbance at 550nm
Statistical analysis:
Data were subjected to statistical analysis using IBM SPSS Statistics version 25.0. These data were analyzed by the ANOVA channel for multiple comparisons between extracts. The experiments on the assays are triplicated. Results are expressed as mean±standard deviation and p˂0.05 values are considered statistically significant.
RESULTS AND DISCUSSION:
Extraction yields:
Extraction yields recorded in Table 1 showed considerable variation depending on the solvent and organ used. The percentages recorded range from 0.305% in dichloromethane extract of roots to 9.756% in methanol extract of flowers. Methanol extracts recorded the best yields followed by ethyl acetate extracts except for whole plant. These results are in agreement with those of Vittaya et al18 after successive extraction of different organs of Derris indica and Ampelocissus martini from hexane, ethyl acetate and methanol, the best yields are obtained with methanol extracts, followed by ethyl acetate extracts. The lowest yields are obtained with dichloromethane extracts18-19. Indeed, extraction yields depend on several factors that may influence extraction performance. These factors include particle size, temperature, solvent nature, extraction time and agitation degree20. According to some authors, in extraction processes, yields are optimal with hydroalcoholic solvents because with polar solvents secondary metabolites offer a large solubility20.
Table 1: Extraction yield
|
Extract |
Extract Extraction yield |
|||
|
Whole plant |
Leafy branches |
Flowers |
Roots |
|
|
Hexane |
1.819 |
1.831 |
1.903 |
0.579 |
|
DCM |
0.779 |
1.081 |
0.866 |
0.305 |
|
AcOEt |
1.649 |
1.983 |
2.520 |
1.236 |
|
MeOH |
6.158 |
7.379 |
9.756 |
5.216 |
DCM: Dichloromethane; AcOEt: Ethyl acetate; MeOH: Methanol
Total alkaloids contents:
Total alkaloids contents of G. maderaspatana extracts are gathered in Table 2. Statistical analysis shows a significant difference between the different contents obtained (p < 0.05). For whole plant, alkaloids contents vary from 78.393 in methanolic extract to 1074µg qE/g in dichloromethane extract. In leafy branches, methanol and dichloromethane extracts, total alkaloids contents vary from 21.036 to 972.351µg qE/g respectively. Concerning flowers extracts, these contents are included between 40.620 methanol extract and 264.569µg of qE/g in ethyl acetate extract. In roots, they vary from 43.767 in ethyl acetate extract to 226.558µg qE/g in hexanic extract. Dichloromethane extracts recorded highest contents in whole plant and leafy branches while in the flowers and roots, ethyl acetate and hexane extracts respectively contained highest contents of total alkaloids. Alkaloids search in plants interest many researchers. Thus, Karama et al21 showed that total alkaloids contents in methanol extract of Securidaca longepedunculata leaves were 246.43µg AE/g. Ajanal et al14 also determined total alkaloids contents in methanol extract of Piper nigrum Linn., Pipper longum Linn., Citrus limon Linn and Apium leptophyllum fruits. They obtained the contents of 1123.9, 610.9, 3679 and 556.4µg/g of material respectively. In methanol extract of Plumbago zeylanica Linn. and Pipper longum Linn. roots, they obtained 246.43 and 140.7µg/g of material respectively. This authors reported 106.5µg/g of material in stem methanol extract of Rhum emodi Wall14. Alkaloids are nitrogenous substances with significant pharmacological activity at low doses22. These pharmacological activities are useful in various fields such as anesthetic (cocaine), antifibrillant (quinidine), antitumor (vinblastine), antimalarial (artemisinin). G. maderaspatana could be a potential source of alkaloids compounds. Alkaloids contained in this plant extracts could confer a particular activity to the plant.
Table 2: Total alkaloid contents
|
Extract |
Total alkaloid contents (µg qE/g extract) |
|||
|
Whole plant |
Leafy branches |
Flowers |
Roots |
|
|
Hexane |
551.299±36.154g |
572.911±4.380g |
111.533±9.048d |
226.558±9.324e |
|
DCM |
1074.752±9.194j |
972.351±21.053i |
66.977±2.978bcd |
103.755±8.719d |
|
AcOEt |
914.378±39.183h |
436.079±33.767f |
264.569±14.739e |
43.767±4.289abc |
|
MeOH |
78.393±5.356cd |
21.036±0.993ab |
40.62±2.149abc |
nd |
qE: quinine equivalent; nd: not detected; The means in each column followed by a different letter are significantly different (p <0.05)
Antiplasmodial and hemolytic activities:
The results of antiplasmodial expressed as IC50 (µg/mL) and hemolytic activities of G. maderaspatana extracts are recorded in Table 3. The analysis of these results shows that antiplasmodial activity evaluated on CQ-sensitive strain D10 and CQ-resistant strain Dd2 of Plasmodium falciparum varies according to extract and the plant part used. Indeed, antiplasmodial activity of whole plant evaluated on strain D10 varies from 6.248 in hexanic extract to 18.018µg/mL in ethyl acetate extract while on strain Dd2, it varies from 5.501 in dichloromethane extract to 8.499µg/mL hexanic extract.
For leafy branches, the activity evaluated on strain D10 ranged from 5.148 to 13.117µg/mL in dichloromethane and ethyl acetate extracts, respectively, while on strain Dd2, it ranged from 4.504 in dichloromethane extract to 7.811µg/mL in hexane extract.
For the flowers, antiplasmodial activity on strain D10 varies from 12.488 in dichloromethane extract to 24.588µg/mL in ethyl acetate extract. On the other hand, on strain Dd2, activity ranged from 7.197 in ethyl acetate extract to 24.806µg/mL in hexane extact.
For the roots, antiplasmodial activity evaluated on sensitive strain (D10) varies from 8.164 in hexane extract to 32.651µg/mL in ethyl acetate extract, whereas on resistant strain (Dd2), the activity ranged from 9.133 in dichloromethane extract to 19.087µg/mL in hexane extract.
According to WHO guidelines and some researchers previous reports23-24-25, a crude extract is inactive for a IC50>50µg/mL), has moderate activity (15˂ IC50˂50µg/mL), promising activity (5≤ IC50 ≤15µg/mL)), or very active for a IC50 ˂5µg/mL). Based on these guidelines, among all the extracts used for this antiplasmodial activity, hexane and dichloromethane extracts of whole plant and leafy branches are the most active. They have promising activity (5˂IC50˂15µg/mL) on both CQ-sensitive and CQ-resistant strains. Among the extracts showing considerable activity on CQ-sensitive strain, the most active was dichloromethane extract of leafy branches, followed by its hexane extract and hexane extract of whole plant. In addition, on CQ-resistant strain, the most active was dichloromethane extract of leafy branches, followed by dichloromethane extract of the whole plant and hexane extract of leafy branches. These results are in agreement with those of Bationo et al26 and Jansen et al14. Bationo et al work on the evaluation of the antiplasmodial potential of organic extracts (DCM, AcOEt, Methanol) of different organs of Cymbopogon giganteus. Bationo et al showed that dichloromethane extracts were the most active on strains 3D7 and K1, followed by ethyl acetate and methanol. In 2012, Jansen et al. also showed that in contrast to petroleum ether, hexane, diethyl ether, ethyl acetate, methanol and ethanol extracts, dichloromethane extracts of Dicoma tomentosa exhibited the best antiplasmodial activity on strains 3D7 and W214. The results obtained and the related analyses suggest the use of the leafy branches or the whole plant of Grangea maderaspatana in the promotion of phytomedicines and in the management of malaria in developing countries. The observed antiplasmodial activity could be due to the presence of alkaloids considering the high contents of organic compounds group in hexane and dichloromethane extracts of leafy branches and whole plant. Statistical analysis of the regression curves using Pearson correlation was performed. Thus, significant correlations were observed between total alkaloid contents and antiplasmodial activity on the strains of Plasmodium falciparum. G. maderaspatana alkaloid would be responsible of antiplasmodial activity on the CQ-sensitive D10 (-61.2%) and CQ-resistant Dd2 (-64.5%) strains. This is in agreement with reports of many other authors. Thus, Ancolio et al. showed that the isolated alkaloids (harman and tetrahydroharman) from chloroform extract of Guiera senegalensis roots have antimalarial activity (IC50 ˂ 4 µg/mL)27. Rumalla et al also showed that alkaloids such as vertine and epi-lyfoline isolated from Heimia salicifolia have antimalarial activity with an IC50 of 10.9 and 6.7µM respectively28. In addition, five alkaloids such as budmunchiamine, 6-hydroxybudmunchiamine, 5-normethylbudmunchiamine, 6-hydroxy-5-normethylbudmunchiamine and 9-normethylbudmunchiamine isolated from methanolic extract of Albizia gummifera showed good activity on CQ-sensitive strain NF54 and CQ-resistant strain ENT3029. All the extracts showed a hemolytic activity lower than 0.5% both at 50µg/mL and 100µg/mL (Table 3). It was also found that G. maderaspatana extracts did not generate any hemolysis. A hemolytic activity is defined if the percentage of hemolysis is greater than 5% 16-23. Thus, the observed antiplasmodial effect reflect extract action on CQ-sensitive strain D10 and CQ-resistant strain Dd2 of Plasmodium falciparum.
Table 3: Antiplasmodial and hemolytic activities
|
Plant Organ |
Antiplasmodial activity (µg/mL) and hemolytic activity (%) |
||||
|
|
Extract |
IC50 (µg/mL) |
Hemolytic activity |
||
|
|
D10 |
Dd2 |
50µg/mL |
100µg/mL |
|
|
Whole plant |
Hexane |
6.248±1.144ab |
8.499±0.577cd |
0 |
0 |
|
DCM |
7.216±0.744ab |
5.501±0.621ab |
0 |
0 |
|
|
AcOEt |
18.018±0.374d |
7.929±0.637cd |
0 |
0.00767 |
|
|
MeOH |
>50 |
nt |
0 |
0.09979 |
|
|
Leafy branches |
Hexane |
6.035±0.421ab |
7.811±0.230cd |
0 |
0.01535 |
|
DCM |
5.148±0.866a |
4.504±0.21a |
0 |
0 |
|
|
AcOEt |
13.117±0.737c |
6.806±0.787bc |
0 |
0.00767 |
|
|
MeOH |
>50 |
nt |
0 |
0.04605 |
|
|
Flowers |
Hexane |
12.864±1.614c |
24.806±0.807g |
0 |
0 |
|
DCM |
12.488±1.296c |
18.145±0.803f |
0 |
0 |
|
|
AcOEt |
24.702±0.286e |
7.197±0.949bc |
0 |
0 |
|
|
MeOH |
>50 |
nt |
0 |
0 |
|
|
Roots |
Hexane |
8.164±0.325b |
19.087±1.021f |
0 |
0 |
|
DCM |
12.474±0.220c |
9.133±0.335d |
0 |
0 |
|
|
AcOEt |
32.651±0.459f |
12.516±0.779e |
0 |
0 |
|
|
MeOH |
>50 |
nt |
0 |
0 |
|
nt: not tested; The means in each column followed by a different letter are significantly different (p <0.05)
CONCLUSION:
This study showed that organic extracts of G. maderaspatana different organs contain alkaloids whose contents vary according to the organ and the extraction solvent. Dichloromethane extract of leafy branches showed the best antiplasmodial activity on CQ-sensitive D10 and CQ-resistant Dd2 strains. This extract did not generate any hemolysis at 50 and 100µg/ml. Further studies are needed to isolate and identify the molecules responsible for this antiplasmodial activity. These results suggest that dichloromethane extract of leafy branches of G. maderaspatana could be used in the promotion and formulation of phytomedicines for the management of malaria, especially in developing countries.
CONFLICT OF INTEREST:
The Authors have no conflicts of interest regarding this investigation.
ACKNOWLEDGEMENTS:
The authors are gratefully to Centre National de Recherche et de Formation sur le Paludisme (CNRFP) and Joseph KI-ZERBO University for conducting this study.
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Received on 21.07.2023 Modified on 16.10.2023
Accepted on 26.12.2023 ©AJRC All right reserved
Asian J. Research Chem. 2024; 17(1):31-36.