CHEMICAL COMPOSITION, ANTIOXIDANT AND ANTIMICROBIAL ACTIVITIES OF THE ESSENTIAL OIL OF DETARIUM MICROCARPUM GUILL. AND PERR. LEAVES FROM BURKINA FASO

CHEMICAL COMPOSITION, ANTIOXIDANT AND ANTIMICROBIAL ACTIVITIES OF THE ESSENTIAL OIL OF DETARIUM MICROCARPUM GUILL. AND PERR. LEAVES FROM BURKINA FASO

Z. Semde^{*1, 2}, J. Koudou ³, C. Zongo ¹, M. K. Somda ¹, G. Figueredo ⁴, L. Ganou ² and A. S. Traore ¹

Centre de Recherche en Sciences Biologiques Alimentaires et Nutritionnelles¹, Université Ouaga I JKZ, 03 BP7021 Ouagadougou 03, Burkina Faso.

Institut de Recherche en Sciences Appliquées et Technologies (IRSAT/CNRST) ², 03 BP7047 Ouagadougou 03, Burkina Faso.

Ecole Doctorale Pluridisciplinaire ³, Université Aube Nouvelle, 06 BP9283 Ouagadougou 06, Burkina Faso.

Laboratoire d’Analyse des Extraits Végétaux (LEXVA Analytique) ⁴, 63360 Saint - Beauzire, France.

ABSTRACT: Chemical composition and biological activities of the essential oil of Detarium microcarpum leaves were assessed in vitro. The essential oil was obtained using a Clevenger type apparatus and analyzed by GC and GC/MS. The essential oil was investigated for antioxidant power using the DPPH radical scavenging method and the FRAP test. Antimicrobial activity of the essential oil was also evaluated by agar disk diffusion and broth micro dilution methods. Chemical analysis showed that the major components of the essential oil of D. microcarpum were caryophyllene oxide (28.186%), β-caryophyllene (11.894%), humulene-1, 2-epoxide (4.05%), neryl acetone (2.452%), salvia-4(14)-ene-1-one (2.423%) and linalol (2.098%). The essential oil showed a low radical scavenging power with an IC₅₀ of 21.99 ± 0.17 µl and a weak reducing power. The essential oil exhibited strong to moderate antimicrobial activity against Bacillus subtilis, Escherichia coli, Bacillus cereus, Clostridium perfringens, Enterococcus faecalis, Listeria monocytogenes, Micrococcus luteus, Staphylococcus, Candida kefir and Saccharomyces cerevisiae with inhibition zone diameters ranging from 12 ± 0.00 mm to 22 ± 1.41 mm. Minimum inhibitory concentrations of the essential oil were between 0.5% and 8% (v/v) with minimum bactericidal concentrations of 1% to 8% and minimum fungicidal concentrations of 1% to 8%. The leaves essential oil of D. microcarpum had an absolute bactericidal action against Staphylococcus aureus ATCC2523. This study provided data on the proximate composition and biological activities of the essential oil of D. microcarpum leaves and these results confirmed some traditional usage of this plant. The essential oil of D. microcarpum could be a good candidate in the research of novel antimicrobial compound.

Detarium microcarpum, Essential oil, Antioxidant, Antimicrobial

INTRODUCTION: Herbal medicines, traditional treatments, and traditional practitioners are the main source of health care, and sometimes the only source of care for many millions of people.

This is care that is close to homes, accessible and affordable, it is also culturally acceptable and trusted by large numbers of people ¹.

Detarium microcarpum Guill. and Perr. (Caesalpiniaceae) is a well-known wild edible fruit species growing in Saharan and sub-Saharan countries and is found mostly in savannah forest of dried type ^{2, 3}. D. microcarpum is a small straight trunk tree of 8 - 10 m high with spherical, fairly dense top. The leaves are alternate, imparipinnated with 3 - 6 pairs of alternate or sub-opposed, oval, oblong or elliptic leaflets with rounded apex. The petal flowers have 4 sepals and 8 - 10 prominent cream-white stamens. The fruit is an ovoid or globular drupe, more or less flattened, 2.5 - 5 cm in diameter, with a cracked surface at maturity, containing a large central nucleus surrounded by a greenish, fibrous and sweet farinaceous pulp ⁴. The leaves, flowers, fruits and seeds of D. microcarpum are used in human food. The fruits are rich in Vitamin C and can be eaten raw or cooked, leaves and flowers are used as condiments and vegetables for the preparation of sauces ^{4, 5}. Leaves, bark, roots, fruits and seeds of D. microcarpum are also used as a pharmacopoeia for the treatment of stomach pain, dysentery, malaria, jaundice, furunculosis, panaris, mining and sexually transmitted diseases ^{4, 5}. The leaves, roots and trunk bark of D. microcarpum are used in Burkina Faso by the Sanan in the treatment of infections and infestations, musculoskeletal, skin, digestive, nutritional and pregnancy disorders ⁶.

Staphylococcus aureus, Escherichia coli, Salmonella typhi, Pseudomonas aeruginosa, Klebsiella pneumoniae, Streptococcus pyogenes, Bacillus subtilis, Corynebacteria and Candida albicans were susceptible to ethyl acetate extract of D. microcarpum stem bark ⁷.

D. microcarpum stem bark extract show antifungal activity when tested by the agar diffusion method against dermatophytes ⁸. Phytochemical analysis, antimicrobial, antioxidant activities, nutritional, toxicological and enzymes inhibition properties of D. microcarpum have been investigated by several authors ^{2, 3, 9, 10}. However we have found least literature data on D. microcarpum essential oils. This study aimed to determine the chemical composition, antioxidant and antimicrobial properties of the essential oil of Detarium microcarpum leaves from Burkina Faso.

MATERIAL AND METHODS:

Plant Material: Detarium microcarpum leaves were collected in the bush of Peyiri, a village located on the outskirts of the town of Koudougou during the months of July and August 2014. A voucher specimen is deposited under the number ID 16965, at the herbarium of Biodiversity Information Center of University Ouaga I. J. K. Z.  The harvested leaves were dried in the laboratory at room temperature during two weeks and reduced to powder before extraction.

Essential oil Extraction: The dried and ground leaves of Detarium microcarpum were subjected to hydro-distillation for 4 h using a Clevenger-type apparatus ¹¹. The obtained essential oil was then dried over anhydrous sodium sulfate and stored at 4°C waiting for analyzes. The extraction yield was determined by the following equation:

R (%) = V / W × 100

Where V is the volume of essential oil (ml) and W the weight of dried leaves (g).

Chemical Analyzes: Chemical analyzes of leaves essential oil of D. microcarpum was carried out by gas chromatography (GC) and gas chromatography / mass spectrometry (GC / MS). GC analysis was performed on a Hewlett-Packard HP 6890 equipped with a split / splitless injector (280 °C), a split ratio 1:10, using a HP - 5 capillary column (25 m × 0.25 mm, film thickness 0.25 m). The oven temperature was programmed from 50 to 300 °C at a rate of 5 °C / min. Helium was used as carrier gas at a flow rate of 1.1 mL / min. The injected sample consisted of 1.0 µl of oil diluted to 10% (v/v) with acetone.

GC/MS analysis was done on a Hewlett-Packard 5973/6890 system operating in EI mode (70eV) using two different columns: a fused silica HP - 5 MS capillary column (25 m × 0.25 mm, film thickness 0.25 m), and a HP-Innowax capillary column (60 m × 0.25 mm, film thickness 0.25 m). The temperature program for HP-5MS column was 50 °C (5 min) rising to 300 °C at a rate of 5 °C / min and for the HP-Innowax column, 50 - 250 °C at a rate of 5 °C / min. Helium was used as carrier gas at a flow rate of 1.1 ml / min.

The components of the essential oil of D. microcarpum leaves were identified by comparison of their mass spectra and their retention indices with those of reference compounds or with literature data ^{12, 13}.

Antioxidant Activity: The DPPH radical scavenging assay and the ferric reduction antioxidant power (FRAP) test were used to evaluate the antioxidant activity of leaves essential oil of Detarium microcarpum.

DPPH Radical Scavenging Assay: Radical scavenging power of D. microcarpum leaves essential oil was assessed by DPPH radical scavenging assay ¹⁴. Different amounts of the essential oil of D. microcarpum (5, 10, 15, 20 and 25 μl) were added to 5 ml of an ethanolic solution of DPPH (0.004%) and mixed. The mixture obtained was incubated in the dark for 30 min and the absorbance read at 517 nm using a spectrophotometer (JASCO V-530 UV / VIS Spectrophotometer). Reference antioxidants, ascorbic acid (0.005 M) and quercetin (0.005 M) and a negative control were also included in each test. The DPPH inhibition percentage was calculated according to the following equation:

% inhibition = [(A_blank ⎯ A_sample) / A_blank] × 100

Where A_blank is the absorbance of the negative control and A_sample the absorbance of the essential oil.

Antioxidant activity of the essential oil of D. microcarpum leaves was expressed as inhibitory concentration 50 (IC₅₀), which is the amount of essential oil required to cause a 50% decrease in initial DPPH concentration. A linear regression was used to calculate the IC₅₀.

All tests were performed in triplicate; the standards and DPPH solutions were prepared and used daily.

Ferric Reduction Antioxidant Power (FRAP) Assay: Reducing power of the essential oil of D. microcarpum leaves was assessed by the FRAP test ¹⁵. Different amounts of D. microcarpum leaves essential oil (5, 10, 15, 20 and 25 μl) were mixed with 2.5 ml of phosphate buffer (200 mM, pH 6.6) and 2.5 ml of potassium ferricyanide (1%). The mixture was incubated at 50 °C for 30 min and 2.5 ml of trichloroacetic acid (10%) were added followed by centrifugation at 600 g for 10 min. The supernatant was collected (5 ml) and mixed with 5 ml of distilled water and then 1 ml of iron chloride (0.1% FeCl₃) was added and the absorbance recorded at 700 nm using a spectrophotometer (JASCO V-530 UV/VIS Spectrophotometer). Ascorbic acid (0.1 M) and quercetin (0.1 M) were used as positive control and a negative control was also included in each test. An increase in absorbance indicates an increase of the reducing power.

Antimicrobial Activity:

Microbial Strains: The essential oil of Detarium microcarpum leaves was tested against a panel of microorganisms including ten Gram positive bacteria, ten Gram negative bacteria and four fungal strains.

Agar Disc Diffusion Method: The antimicrobial activity of the essential oil of D. microcarpum leaves was evaluated by the agar disc diffusion method. Mueller Hinton agar was used for the bacterial strains and Sabouraud dextrose agar for the fungal strains ¹¹.

Microbial cultures of 18 - 24 hours were prepared in nutrient broth for the bacterial strains and in Sabouraud broth for the fungal strains. The inoculums density was then adjusted to that of McFarland standard 0.5 with sterile saline solution (NaCl 0.9%). The Petri dishes containing sterile and solid Mueller-Hinton agar or Sabouraud dextrose agar were inoculated with this microbial suspension. The essential oil of D. microcarpum was impregnated on sterile blank discs of 6 mm diameter (15 μl per disc) and the discs were then placed on the surface of the agar previously inoculated. The Petri dishes were aerobically incubated at 37 °C for the bacterial strains and at 30 °C for the fungal strains for 24 hours. The inhibitory action of the essential oil of D. microcarpum on the tested microorganisms was determined by measuring the inhibition zone diameter (ID). Inhibition zone diameters (ID) were evaluated using the following criteria ¹⁶:

• ID ˃ 15 mm: high inhibitory action.
• 10 mm ≤ ID ≤ 15 mm: moderate inhibitory action.
• ID ˂ 10 mm: weak inhibitory action.

Tetracycline (30 µg) and ciprofloxacin (5 µg) were used as reference antibiotics for bacterial strains and nystatin (100 UI) for fungal strains. The assay was performed in duplicate.

Determination of Minimum Inhibitory Concentration (MIC), Minimum Bactericidal Concentration (MBC) and Minimum Fungicidal Concentration (MFC): The broth micro-dilution method ¹¹ was used to determine the minimum inhibitory concentration (MIC), the minimum bactericidal concentration (MBC) and the minimum fungicidal concentration (MFC) of the essential oil of D. microcarpum leaves. The tests were performed in Mueller-Hinton broth (MH) for bacterial strains and in Sabouraud broth for fungal strains. The broth was supplemented with Tween 80 at a concentration of 0.5% (v/v) to enhance the solubility of the essential oil. A serial double dilution of the essential oil of D. microcarpum leaves was prepared in a 96 well microplate containing MH broth or Sabouraud broth in a range of 0.03% to 8% (v/v). Microbial cultures of 18 - 24 hours were prepared in nutrient broth for the bacterial strains and in Sabouraud broth for the fungal strains and the inoculums density adjusted to that of McFarland standard 0.5 with sterile saline solution (0.9% NaCl). Then 10 μl of these inoculums was added to each well, positive and negative growth controls were included in each assay.

The microplate was then incubated aerobically at 30 °C for the fungal strains and at 37 °C for the bacterial strains. The lowest concentration of the essential oil which did not demonstrate visible growth after 24 h of incubation was considered to be the MIC. To determine the MBC or MFC, 10 μl of microbial suspension was taken from the wells of concentration greater than or equal to MIC and inoculated on sterile Mueller-Hinton agar or Sabouraud agar and incubated for 24 hours at 37 °C or 30 °C. The lowest concentration of the essential oil at which no growth was recorded on the agar after 24 h of incubation was considered to be the MBC or MFC. The ratio MBC/MIC or MFC/MIC was used to determine the intrinsic activity (bactericidal or bacteriostatic) of the essential oil of D. microcarpum leaves, considering that:

• MBC / MIC = 1: absolute bactericidal activity.
• 1 < MBC / MIC ≤ 4: bactericidal activity.
• 8 ˂ MBC / MIC ˂ 16: bacteriostatic activity.

Statistical Analysis: The data were entered and processed on Microsoft excel. The results are presented as mean ± SD (standard deviation).

RESULTS AND DISCUSSION:

Chemical Composition: The hydro-distillation of D. microcarpum dry leaves gave a yellowish-colored essential oil with a yield of 0.052 ± 0.002 % (v/w).

Chemical analysis of the essential oil of D. microcarpum leaves allowed the identification of thirty compounds representing 69.11% of the essential oil. The relative abundance of some components of the essential oil is shown in Fig. 1. Chemical composition of the essential oil is presented in Table 1, the major components were caryophyllene oxide (28.186%), β-caryophyllene (11.894%), humulene-1,2-epoxide (4.05%), neryl acetone (2.452%), salvia-4(14)-ene-1-one (2.423%), linalol (2.098%), spathulenol (1.886%), γ-muurolene (1.589%), α-copaene (1.238%), intermedeol (1.208%), β-selinene (1.108%), α-muurolene (1.027%), γ-cadinene (1.13%) and δ-cadinene (1.254%).

In our best knowledge, it is the first time that the chemical composition of the essential oil of D. microcarpum leaves is determined.

TABLE 1: CHEMICAL COMPOSITION OF THE ESSENTIAL OIL OF DETARIUM MICROCARPUM LEAVES

FIG. 1: CHROMATOGRAM OF DETARIUM MICROCARPUM LEAVES ESSENTIAL OIL

Antioxidant Activity: Antioxidant activity of the essential oil of D. microcarpum leaves was assessed by the DPPH radical scavenging assay in comparison with ascorbic acid and quercetin, two standard antioxidants. DPPH is a stable free radical which can readily experience reduction in the presence of an antioxidant. DPPH radical scavenging power of the essential oil of D. microcarpum and the standards is shown in Fig. 2.

FIG. 2: DPPH RADICAL SCAVENGING POWER

The inhibitory concentrations 50 (IC₅₀) of DPPH were calculated using a linear regression and are presented in Table 2. The IC₅₀ was 21.99 ± 0.17 µl for the essential oil, 18.33 ± 0.65 µl for ascorbic acid and 12.45 ± 0.25 µl for quercetin. The essential oil of D. microcarpum leaves had a low radical scavenging power relative to ascorbic acid and quercetin.

TABLE 2: IC₅₀ RADICAL SCAVENGING POWER

The results of the FRAP test are represented by Fig. 3. Reducing power of the essential oil of D. microcarpum leaves was increased with increasing concentration but was low compared with ascorbic acid and quercetin.

FIG. 3: REDUCING POWER OF THE ESSENTIAL OIL OF DETARIUM MICROCARPUM LEAVES AND STANDARDS

Phenolic compounds are major antioxidant constituents in selected plants, and there are direct relationships between their antioxidant activity and total phenolic content ¹⁷. Oxygenated monoterpenes and monoterpene hydrocarbons are mainly responsible for the antioxidant potential of essential oil ¹⁸. Some structural features, such as the presence of strongly activated methylene groups in the molecule, are probably the reason for antioxidant activity of monoterpene hydrocarbons ¹⁹.

In the DPPH test, the ability of the essential oil to act as the donor of hydrogen atoms or electrons in transformation of DPPH into its reduced form DPPH-H was measured spectrophotometrically ²⁰. The absence of antioxidant activity observed for the terpene compounds in the DPPH reduction can be explained by the fact that they are not capable of donating an hydrogen atom and the low solubility provided by them in the reaction medium of the assay, because this test utilizes methanol or ethanol as solvent ²¹.

Hence the low antioxidant power of the essential oil of D. microcarpum leaves which contains a small proportion of monoterpenes and phenolic compounds.

Antimicrobial Activity: The inhibition diameters of the essential oil of D. microcarpum leaves are shown in Table 3. The essential oil of D. microcarpum was active on all the microbial strains tested with inhibition diameters ranging from 08 mm (Salmonella infantis, Salmonella nigeria, Yersinia enterocolitica) to 22 mm (Bacillus subtilis). According to the criteria ¹⁶, the essential oil of D. microcarpum had:

• Strong inhibitory action (ID ˃ 15 mm) on the strains of Bacillus subtilis and Escherichia coli;
• Moderate inhibitory action (10 ≤ ID ≤ 15 mm) on the strains of Bacillus cereus, Clostridium perfringens, Enterococcus faecalis, Listeria monocytogenes, Micrococcus luteus, Pseudomonas aeruginosa, Shigella flexnerii, Staphylococcus, Candida albicans, Candida kefir and Saccharomyces cerevisiae;
• Weak inhibitory action (10 mm ˂ ID) on the strains of Salmonella, Shigella dysenteria, Yersinia enterocolitica and Candida tropicalis.

MIC, MBC and MFC: Minimum inhibitory concentrations (MIC), minimum bactericidal concentrations (MBC) and minimum fungicidal concentrations (MFC) of the essential oil of D. microcarpum leaves are given in Table 4. MICs of the essential oil ranged from 0.5% to 8% (v/v) for eighteen (18) microbial strains and greater than 8% for the other tested strains. The lowest MIC was obtained with Bacillus subtilis, Staphylococcus aureus ATCC 25923, Staphylococcus hominis and Saccharomyces cerevisiae.

The essential oil of D. microcarpum had MBCs values ranging from 1% to 8% (v/v). The lowest MBC was determined with Staphylococcus aureus ATCC 25923 and Staphylococcus hominis.

The essential oil of D. microcarpum leaves was absolute bactericidal (MBC / MIC = 1) against Staphylococcus aureus ATCC 2523 and bactericidal (1˂ MBC / MIC ≤ 4) against the strains of Bacillus, Clostridium perfringens, Escherichia coli, Listeria monocytogenes, Micrococcus luteus, Staphylococcus aureus ATCC 25923, Staphylococcus aureus toxin (A + B) and Staphylococcus hominis.

The MFCs of the essential oil of D. microcarpum ranged from 1% to 8%, the lowest MFC was given by Saccharomyces cerevisiae. The essential oil of D. microcarpum leaves had a fungicidal action (1˂ MFC / MIC ≤ 4) on Candida albicans, Candida kefir and Saccharomyces cerevisiae.

TABLE 3: INHIBITION ZONE DIAMETERS (MEAN ± SD) OF THE ESSENTIAL OIL OF DETARIUM MICROCARPUM LEAVES (15 µL) INCLUDING THE DISC DIAMETER (6 mm)

SD: Standard Deviation

EO: Essential oil

ATCC: American Type Culture Collection

CRSBAN: Centre de Recherche en Sciences Biologiques Alimentaires et Nutritionnelles.

TABLE 4: MIC, MBC AND MFC OF THE ESSENTIAL OIL OF D. MICROCARPU LEAVES 0.03% TO 8% (v/v)

The antimicrobial activity of volatile constituents was decreased in this decreasing order: phenols (highest active) > alcohols > aldehydes > ketones > ethers > hydrocarbons ²².

Antimicrobial activity of the essential oil of D. microcarpum leaves could be attributed to its major components, caryophyllene oxide (28.186%), β-caryophyllene (11.894%), humulene-1,2-epoxide (4.05%), neryl acetone (2.452%), salvia-4(14)-ene-1-one (2.423%) and linalool (2.098%). β-caryophyllene and caryophyllene oxide are known to have a good to high antimicrobial activity ²³. β-caryophyllene and caryophyllene oxide possessed antibacterial activity and caryophyllene oxide had a high activity against Candida albicans ²⁴. Essential oil of D. microcarpum leaves is more active on Gram-positive bacterial strains than Gram-negative bacterial strains except Escherichia coli strains. Most studies investigating the action of whole essential oils against food spoilage organisms and food borne pathogens agree that, generally, essential oils are slightly more active against gram-positive than gram-negative bacteria ^{25, 26, 23, 27, 28}.

CONCLUSION: This study provided data on chemical composition, antioxidant and anti-microbial properties of the essential oil of Detarium microcarpum dry leaves. The major components of this essential oil were caryophyllene oxide, β-caryophyllene and humulene-1, 2-epoxide. The essential oil of D. microcarpum showed a good antimicrobial activity but exhibited a weak antioxidant activity. These results confirmed the traditional usage of D. microcarpum. The essential oil of D. microcarpum leaves could serve as a basis for the research of new antimicrobials.

ACKNOWLEDGEMENT: The authors thank MIHIN Henriette Bougnitébiéhin, a master's student at CRSBAN for her technical support in data collection.

CONFLICTS OF INTEREST: No conflict of interest.

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    How to cite this article:

    Semde Z, Koudou J, Zongo C, Somda MK, Figueredo G, Ganou L and Traore AS: Chemical composition, antioxidant and antimicrobial activities of the essential oil of Detarium microcarpum guill. and perr. Leaves from Burkina faso. Int J Pharm Sci Res 2018; 9(3): 956-64. doi: 10.13040/IJPSR.0975-8232.9(3). 956-64.

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