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Article

Chemical Composition, Antibacterial and Combinatorial Effects of the Essential Oils from Cymbopogon spp. and Mentha arvensis with Conventional Antibiotics

by
Neha Sharma
1,
Zahid Nabi Sheikh
1,
Saud Alamri
2,
Bikarma Singh
3,
Mahipal Singh Kesawat
4 and
Sanjay Guleria
1,*
1
Division of Biochemistry, Faculty of Basic Sciences, Sher-e Kashmir University of Agricultural Sciences and Technology of Jammu, Main Campus Chatha, Jammu 180009, Jammu and Kashmir, India
2
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
3
Botanic Garden Division, CSIR-National Botanical Research Institute, Lucknow 226001, Uttar Pradesh, India
4
Institute for Molecular Biology and Genetics, School of Biological Sciences, Seoul National University, Seoul 08826, Republic of Korea
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(4), 1091; https://doi.org/10.3390/agronomy13041091
Submission received: 16 January 2023 / Revised: 24 March 2023 / Accepted: 26 March 2023 / Published: 11 April 2023
(This article belongs to the Section Agricultural Biosystem and Biological Engineering)
Review Reports Versions Notes

Abstract

:
This work aimed to evaluate the chemical composition and antibacterial activity of essential oils of Cymbopogon citratus (CCEO), Cymbopogon khasianus (CKEO), and Mentha arvensis (MAEO) against two Gram-negative (Escherichia coli, Klebsiella pneumoniae) and three Gram-positive (Staphylococcus aureus, Micrococcus luteus, Bacillus subtilis) microbial strains and their combination with antibiotics (chloramphenicol, ampicillin, erythromycin) to observe the synergistic behavior between them. The essential oils (EOs) were investigated by the GC-MS (gas chromatography mass spectrometry) method. The synergistic effect between EOs and antimicrobial agents was analyzed by broth dilution assay. (-)-carvone (52.48%), geraniol (57.66%), and citral (37.83%) were the major components identified in EOs of MAEO, CKEO, and CCEO, respectively. According to the antibacterial activity, EOs demonstrated strong antibacterial activity with MIC values ranging from 0.7 to 18 mg/mL. The interaction between the combination of EOs and antibiotics was determined in terms of FICI (Fractional Inhibitory Concentration Index). Some combinations displayed a partial synergistic effect, and some showed a synergistic and others displayed no effect against bacterial strains. The best synergistic action was shown by the combination of CCEO and Chloramphenicol against E. coli with a FICI value of 0.4. Three to four fold reductions in the MIC value of both essential oil and antibiotics were observed. Therefore, this synergistic interaction of the most active EOs with synthetic antibiotics could lead to new combination therapies for combating infections caused by multidrug-resistant microbes at sufficiently low concentrations in the pharmaceutical and food industry.

1. Introduction

Food safety has become an issue of great concern on a global scale as multidrug-resistant bacteria pose one of the main causes of mortality and morbidity [1]. Therefore, there is a pressing need to explore new novel drugs and strategies to respond to the global public health concern.
Due to safety concerns, the trend is shifting toward non-toxic natural antimicrobials as an alternative to synthetic antibiotics to maintain the efficacy of antimicrobials [2].
Among plants, spices, and extracts, EOs have attracted much attention because of their high content of volatile phytochemicals and have been widely used for their antibacterial, antioxidant, fungicidal, and insecticidal properties in various food packing, food preservatives, and pharmaceuticals industries [3,4]. Additionally, due to the complex structure of EOs and a wide range of bioactive compounds, it can be attributed to the broad range of biological and structural interactions [5,6]. However, despite the wide range of applications, its use in industry is constrained by the following factors: (i) requirement for a high dosage to achieve bactericidal and bacteriostatic effects; (ii) higher costs due to needing a higher dosage; and, (iii) adverse effects after essential oil treatment (changes in the organoleptic properties) [7]. To overcome these issues, new techniques of using EOs are now being researched to address these concerns.
One of the most effective strategies regarding antibacterial complexes is combination therapy to achieve a synergistic interaction against a broad range of the bacterial spectrum. Combinatorial therapy has proven to be an essential feature of antimicrobial treatment due to several important factors: (i) they thwart drug resistance; (ii) increase activity through the use of components with additive or synergistic activity; (iii) reduce the effective doses, reducing both cost/toxic effect, and (iv)increase the spectrum of activity [8]. However, combinations of two or more agents lead to synergistic, additive, partial, and antagonistic effects [9]. Such knowledge could be applied and helpful in developing new, more effective natural antimicrobial agents in food preservation, cosmetics, pharmaceuticals etc [10].
Therefore, the present study has been designed to verify an antibacterial synergistic interaction between essential oils (Cymbopogon citratus, Cymbopogon khasianus, and Mentha arvensis) and conventional antibiotics. The Genus Cymbopogon (family: Gramineae) is a tall, densely tufted perennial grass with profuse tillering known for its medicinal use [11]. Cymbopogon citratus is one of the most mentioned species with various medical applications. This plant is known for its calmative, anti-depressant, blood depurative, sedative, analgesic, antifungal, antimicrobial, anti-inflammatory, and diuretic effects [12]. Essential oil of Lemongrass has been shown to effectively inhibit the growth of many different bacteria, including Staphylococcus aureus (MRSA), Staphylococcus epidermidis (MRSE), and Gram-negative bacteria [13]. Cymbopogon khasianus, also known as Himrosa, is a perennial grass native to India and subtropical Asia. The essential oil of Cymbopogon khasianus is reported to have strong antimicrobial, antioxidant, and anti-inflammatory properties [11,14]. The herbaceous perennial plant, Mentha arvensis, also known as corn mint or wild mint, belongs to the lamiaceae family. It is widely distributed in the temperate regions of Europe and western and central Asia, east to the Himalayas and eastern Siberia and North America. The essential oil of Mentha arvensis has attracted much interest from re searchers due to its worldwide occurrence and several biological activities, including antibacterial, antifungal, antiviral, and cytotoxic activities [15].

2. Experimental Material Methods

2.1. Material

Essential oils of Cymbopogon citratus, Cymbopogon khasianus, and Mentha arvensis were procured from the Council of Scientific & Industrial Research, Indian Institute of Integrative Medicine (CSIR-IIIM) Canal Road, Jammu. Two Gram-negative (Escherichia coli, Klebsiella pneumoniae) and three Gram-positive (Staphylococcus aureus, Micrococcus luteus, Bacillus subtilis) microbial strains used in the study were obtained from IMTECH, Chandigarh, India. Antimicrobial agents (chloramphenicol, ampicillin and erythromycin) were purchased from Hi-media, Mumbai, India.

2.2. Chemical Profiling of EOs

The EOs and bioactive components separation were analyzed using gas chromatography and mass spectrometry. A GC/MS 4000 Varian system (Varian Inc., Palo Alto, CA, USA) with HP-5 MS Agilent column (Agilent Technologies, Santa Clara, CA, USA) (30 × 0.25 mm id, film thickness 0.25 μm) was used. Working conditions of setup-the injector temperature was set at 280 °C, the oven temperature was set at 50 °C, programmed to rise to 300 °C every 3 °C rise/min. Helium was used as a carrier gas at a constant flow of 1.0 mL/min. 0.2 µL of each essential oil solution was injected into the column and analyzed. The mass spectra were recorded with electron impact voltage and the mass range at 70 eV and 40–500 m/z, respectively, at the speed of one scan per second. The volatile organic compounds were identified by comparing each component’s obtained mass spectra with the authentic reference compound present in the NIST database or with the literature [16,17].

2.3. Determination of Minimum Inhibitory Concentration (MIC)

The broth dilution method was employed to assess the MIC of essential oils and antibiotics with minor modifications [18]. The fresh inoculum was prepared in Muller Hinton broth (MHB) and adjusted to 0.5 Mc Farland standards. In brief, each essential oil was dissolved in DMSO (1:1 v/v ratio) for the preparation of stock solution and then the final volume raised to 1mL. In a similar way, MHB was also used to dilute the EOs. Similarly, dilutions for antibiotics were performed. Next, 100 µL of each diluted necessary oil/antibiotics were put into sterilized tubes containing 90 μL of MHB and 10 μL of microbial suspension (106 CFU/mL), resulting in a total final volume of 200 μL. Appropriate positive control (broth and microbial suspension) and negative control (no inoculum) were used to test the bacterial growth. The sterilized tubes were then kept at 37 °C for 24 h. After incubation, 40 µL of the p-iodonitrotetrazolium violet solution was added to examine the bacterial growth for another 20 min. Development of a pink color was denoted as bacterial growth, and the tubes in which there was no change in color were defined as MIC for particular oil/antibiotics.

2.4. Synergistic Studies of EOs with Synthetic Antibiotics

The broth dilution method was used to determine the interaction between EOs and synthetic drugs (chloramphenicol, ampicillin, and erythromycin). In sterile tubes, 50 µL of each drug dilution, 90 µL of Muller Hinton broth, and 10 µL of microbial suspension were added and kept at 37 °C for 24 h. After incubation, 40 µL of 0.4 mg/mL of p-iodonitrotetrazolium violet solution was added to examine the bacterial growth for another 20 min. The appearance of pink color indicated the growth of bacteria. The FIC Index was used to determine the interaction between two drugs to calculate the fractional inhibitory concentration index (FICI). Fractional inhibitory concentration indices (FICI) were determined as follows:
(FICI = FIC of agent I + FIC of agent II)
FIC of agent I =MIC of agent I in combination with agent II/MIC of agent I alone, and FIC of agent II = MIC of agent II in combination with the agent I/MIC of agent II alone. Where agent I and agent II are two distinct constituents (EOs/or antibiotics) and the results were elucidated as ≤ 0.5 FICI synergy, 0.5 < FICI ≤ 0.75 partial synergy; 0.75 < FICI ≤ 2 no effect; >2 antagonism [19].

3. Results and Discussion

3.1. Chemical Composition of Plant EOs

The chemical composition of hydro-distilled essential oils was determined by GC-MS analysis. The percentage content and Kovats index of each compound of essential oil CKEO and MAEO are presented in Table 1. The phytochemical constraints with their area percent of CCEO were presented in our previous study [20]. The volatile composition of EOs of CKEO and MAEO, a total of 43 primary compounds, were identified, which accounted for 92.32–95.48% of the total volatile oils. GC-MS analysis revealed that the principal component present in the essential of CKEO were geraniol (57.66%) followed by geranyl acetate (8.24%), cis-p-menth-2-en-1-ol (4.68%), and β-ocimene (3.55%) with some minor constituents. Regarding MAEO, there was a prevalence of monoterpenes (84.64%), bicyclic monoterpene (4.67%), and a lower concentration of diterpene alcohol (2.45%) and sesquiterpene (0.55%). The most abundant bioactive components were (-)-carvone (52.48%), limonene (12.83%), and menthol (7.96%). The major constituent found in the essential oil of CKEO was similar to that reported for the essential oil of C. khasianus, with variation in the percentages [11,21]. In another study, carvone (60.25%) was identified as a major constituent in the essential oil of M. arvensis [22]. Some relevant studies on plant essential oil of M. arvensis found menthol as the main constituent, which may be explained by the fact that the composition of essential oil is influenced by numerous factors such as genetic variations, the occurrence of different chemotypes, geographical origin, maturity stage of the plant, harvesting season, and method of essential oil extraction [23]. The ratio of phytochemical constituents present in the essential oils and the interactions between the various bioactive components considerably impact the biological activity of EOs [24,25].

3.2. Antibacterial Activity (MIC) of EOs

The results of the individual antibacterial effects of EOs and antibiotics against a wide range of bacterial strains are presented in Table 2. The essential oil of C. khasianus and C. citratus was found to be effective at low concentrations against all tested bacterial strains with MIC values lying within the range 700–1400 µg/mL, followed by M. arvensis with MIC values lying between 2500–5000 µg/mL against all the microbial strains. The different EOs exhibited varied antibacterial activity, which may be due to different volatile constituents present in them as well as the nature of the test organism [26]. The stronger potency of EO of C. khasianus and C. citratus may be due to the presence of a high level of principal components geraniol and citral, respectively, against all the microbial strains, which are described to possess magnificent antimicrobial properties [27,28,29,30,31,32]. The antibacterial activity of M. arvensis may be attributed to its predominant constraints, (-)-carvone, limonene and menthol, which are reported to possess good antibacterial potential [33,34,35]. All these compounds have a monoterpenes class, which has been shown to display antibacterial activity by damaging the cell organelle, inhibiting important processes like ion transport and respiration [36]. It is believed that essential oils containing monoterpenes can accumulate in the bacterial cell membrane, causing loss of integrity, and leakage of intracellular content, leading to cell lysis and death [37]. In addition to major compounds, minor components also contribute to the antibacterial activity of EO as the whole essential oil contains a complex mixture of bioactive compounds, and it is difficult to possess antimicrobial efficacy with a single component alone. This may be due to synergistic interaction between dominant and minor features that enhance the whole EO’s activity [38].

3.3. Synergistic Studies of EOs with Synthetic Antibiotics

Combinatorial therapy is a promising strategy to overcome antibiotic resistance by combining synthetic antibiotics and natural products such as essential oils [39,40]. Such combinations of antimicrobial agents may exhibit different interactions, i.e., synergism, additive, antagonistic, and no effect. Synergistic interactions, in particular, show increased efficiency and lower toxicity due to their multi-target action, which may avoid antibiotic resistance and be effective against multidrug-resistant bacteria strains [41,42]. The results of the combined effect of EOs and chloramphenicol are displayed in Table 3. Synergism was observed against S. aureus, K. pneumoniae, and E. coli in the combination of chloramphenicol with the EOs of C. khasianus (1/4 MIC C. khasianus + 1/4 MIC chloramphenicol) and C. citratus (1/4 MIC C. citratus + 1/4 MIC chloramphenicol), showing a FIC index lying between 0.40 and 0.50. Regarding M. luteus, all the combinations showed no effect. Partial synergistic interaction was noted when M. arvensis was combined with chloramphenicol against all five microbial strains (FICI = 0.63) except M. luteus. Also, C. citratus showed partial synergism against S. aureus. A total of three to four fold reductions were observed in the MIC of essential oils and antibiotics in partial synergistic and synergistic interactions, respectively. Out of 15 combinations tested, 3 combinations showed synergism, 5 combinations displayed partial synergism, and the remaining 7 binary mixtures showed no effect.
Furthermore, synergistic behavior was shown against S. aureus, M. luteus and E. coli in the combination of ampicillin with the EO of M. arvensis (1/4 MIC M. arvensis + 1/4 MIC ampicillin). Regarding the combined effect against S. aureus and B. subtilis, CKEO and CCEO displayed synergistic interaction with FICI lying between 0.49 and 0.50. Nonetheless, a partial synergy was observed for the combination of EO of M. arvensis against K. pneumoniae and B. subtilis, EO of C. citratus against E. coli, and EO of C. khasianus against M. luteus with ampicillin (FICI = 0.66). Notably, no combination of EOs and ampicillin showed antagonistic behavior (Table 4).
The results of the combined antibacterial activity of EOs with standard antibiotic (erythromycin) are given in Table 5. Synergism was observed in the combination of erythromycin with EO of M. arvensis (1/4 MIC M. arvensis+ 1/4 MIC erythromycin) against E. coli, S. aureus, and K. pneumoniae. The synergistic combinations correspond to 1/4 MIC C. khasianus+ 1/4 MIC erythromycin were potent against M. luteus and B. subtilis. Also, EO from C. citratus showed synergism against E. coli and M. luteus with FICI 0.50. The remaining combinations showed a partial synergism, decreasing the MIC of the antibiotic and essential oils by three-fold. No combinations displayed antagonistic behavior. These results indicated that the essential oils tested could potentiate the effect of antibiotics. Thus, these essential oils could serve as an adjuvant in therapy with ampicillin, chloramphenicol, and erythromycin. Normally, combinations of drugs have been demonstrated as an important feature of antimicrobial therapy because of various essential contemplations like (i) they utilize compounds having synergistic or additive action to elevate the activity, (ii) they impede resistivity of the drug, (iii) they reduce requisite doses, thereby, decreasing cost and unfavorable/dangerous after effects, and (iv) they elevate the range of activity [43].
Essential oils contain a wide range of metabolites with diverse mechanisms of action. However, the fact that crucial oils alter the permeability of the bacterial cell membrane is well known. In combination with antibiotics (which have different mechanisms of action), essential oils can help maximize the therapeutic potential [44,45]. The synergistic interactions observed in the present study could result from the inhibition of a common biochemical pathway and increase in cell permeability resulting in enhanced uptake of the antibiotics by the bacterial cells [46]. The most likely effect may be related to the fact that essential oil constituents act by unblocking the cell membrane channels, facilitating the passage of antimicrobial agents to reach the internal target [47]. All of our findings support the use of essential oils as a biotechnological tool for therapeutic use as tropical formulations, antifouling coatings, food preservations, and other uses, either use one or in combination with antibiotics.
In conclusion, combining natural products with conventional antibiotics has proven to be a promising alternative for lowering the MIC of these drugs (chloramphenicol, ampicillin, and erythromycin) and allowing the use of lower dosages against multidrug-resistant bacteria. The same conclusion has been previously reported for other medicinal plants [40,42,48,49,50,51]. As a result, additional research is needed to understand these oils’ mechanism of action and identify the best essential oil/antibiotic combination for medical therapy.

4. Conclusions

In the present investigation, all the tested essential oils (M. arvensis, C. citratus, and C. khasianus) showed antimicrobial activity with greater potency against both Gram-positive and Gram-negative bacterial strains. In combination with antibiotics, these essential oils showed synergistic behavior against some bacterial isolates, with FIC lying between 0.40 and 0.50. They contributed a three to four fold decrease in individual MICs of all standard antibiotics tested. Using essential oils in combination with antibiotics reduced the minimum effective dosage and decreased the probability of selecting resistant strains. Furthermore, using essential oils as adjuvants can reduce side effects and treatment expenses. Our results suggest developing a new class of antimicrobial agents based on a combination of antimicrobial compounds having potential applications in addressing the ever-increasing incidence of antimicrobial resistance. Future research is warranted onfurther investigations on these plant species for their potential use in combinatorial antibiotic therapy for minimizing the effective dose of drugs and their mechanism of action.

Author Contributions

Conceptualization, methodology, data curation, writing-original draft, N.S., Conceptualization, methodology, data curation S.G.; methodology, editing, Z.N.S.; formal analysis and funding acquisition: S.A., M.S.K., editing, reviewing and providing material (EOs), B.S.; All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Researchers Supporting Project number (RSP2023R194), King Saud University, Riyadh, Saudi Arabia.

Data Availability Statement

Data will be available only on authors behalf.

Acknowledgments

The authors would like to extend their sincere appreciation to the Researchers Supporting Project number (RSP2023R194), King Saud University, Riyadh, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. Chemical composition of essential oils obtained from fresh leaves of plants.
Table 1. Chemical composition of essential oils obtained from fresh leaves of plants.
KICompoundMAEOCKEO
985α-pinene2.07-
993Camphene0.050.07
1003Sabinene0.67-
1005β-pinene1.88-
1010β-myrcene0.36-
1017α-phellandrene-1.49
1024o-cymene0.280.73
1026Limonene12.831.45
1027Eucalyptol2.37-
1032β-ocimene-3.55
1037γ-terpinene-0.26
1041α-citronellol0.11-
1051Linalool0.152.16
1060cis-p-menth-2-en-1-ol-4.68
1065 Alloocimene-0.16
10712-Hexen-1-al3.88-
1075p-mentha-1,5-dien-8-ol-0.23
1079Terpinen-4-ol-0.14
1082α-terpineol0.66-
1083γ-terpineol1.26
1084cis-piperitol-0.72
1085(E)-Isopiperitenol0.18-
1095Neral-0.39
1096Pulegone0.43-
1098Geraniol-57.66
1099(-)-carvone52.48-
1100Isopulegol1.70-
1101Piperitone0.831.89
1173Menthol7.96-
1206Menthyl acetate3.04-
1231Geranyl acetate-8.24
1279Hexadec-7-yn-1-ol1.48-
1404Caryophyllene-1.61
1409Calarene-0.18
1420Geranyl butyrate 2.37
1421Humulene-0.10
1435GermacreneD0.280.08
1455B-cadinene-0.49
1464Kessane-0.21
1488Spathulenol0.12-
1490Caryophyllene oxide0.430.12
1699Neryl hexanoate-0.96
1724Diisobutylphthalate-2.38
Total95.48%92.32%
Table
Table 2. Minimum inhibitory concentration of essential oils against different bacterial strains.
Table 2. Minimum inhibitory concentration of essential oils against different bacterial strains.
ComponentMinimum Inhibitory Concentration (μg/mL)
B. subtilisE. coliK. pneumoniaeM. luteusS. aureus
CCEO800130090011501200
CKEO70090080010001400
MAEO25003500250050005000
Chloramphenicol2221.51.5
Ampicillin0.500.500.500.400.40
Erythromycin11.5111
Table
Table 3. Effect of combinations between essential oils and chloramphenicol.
Table 3. Effect of combinations between essential oils and chloramphenicol.
MicroorganismsCombinationsMIC
(μg/mL)		MICc
(μg/mL)		FICFICIInteraction
S. aureusM. arvensis50001666.660.330.63Partial synergistic
Chloramphenicol1.50.50.3
C. citratus12004000.330.63Partial synergistic
Chloramphenicol1.50.50.3
C. khasianus14003500.250.50Synergistic
Chloramphenicol1.50.30.25
M. luteusM. arvensis500025000.51No effect
Chloramphenicol1.50.750.5
C. citratus11505750.51No effect
Chloramphenicol1.50.750.5
C. khasianus10005000.51No effect
Chloramphenicol1.50.750.5
E. coliM. arvensis35001166.660.330.63Partial synergistic
Chloramphenicol20.60.3
C. citratus13003250.20.4Synergistic
Chloramphenicol20.40.2
C. khasianus9004500.51No effect
Chloramphenicol210.5
B. subtilisM. arvensis2500833.330.330.63Partial synergistic
Chloramphenicol20.60.3
C. citratus8004000.51No effect
Chloramphenicol210.5
C. khasianus7003500.51No effect
Chloramphenicol210.5
K. pneumoniaeM. arvensis2500833.330.330.63Partial synergistic
Chloramphenicol20.60.3
C. citratus9004500.51No effect
Chloramphenicol210.5
C. khasianus8002000.250.45Synergistic
Chloramphenicol20.40.2
Table
Table 4. Effect of combinations between essential oils and ampicillin.
Table 4. Effect of combinations between essential oils and ampicillin.
MicroorganismsCombinationsMIC
(μg/mL)		MICc
(μg/mL)		FICFICIInteraction
S. aureusC. khasianus14003500.250.5Synergistic
Ampicillin0.400.10.25
C. citratus12006000.51No effect
Ampicillin0.400.20.5
M. arvensis500012500.250.5Synergistic
Ampicillin0.400.10.25
M. luteusC. khasianus10003330.30.6Partial synergistic
Ampicillin0.400.130.3
C. citratus11505750.51No effect
Ampicillin0.400.20.5
M. arvensis500012500.250.5Synergistic
Ampicillin0.400.10.25
E. coliC. khasianus7003520.51No effect
Ampicillin0.500.250.5
C. citratus8002660.30.6Partial synergistic
Ampicillin0.500.160.3
M. arvensis25006250.250.49Synergistic
Ampicillin0.500.120.24
B. subtilisC. khasianus9004500.51No effect
Ampicillin0.500.250.5
C. citratus13003520.250.49Synergistic
Ampicillin0.500.120.24
M. arvensis350011660.30.6Partial synergistic
Ampicillin0.500.160.3
K. pneumoniaeC. khasianus8004000.51No effect
Ampicillin0.500.250.5
C. citratus9004500.51No effect
Ampicillin0.500.250.5
M. arvensis25008330.330.66Partial synergistic
Ampicillin0.500.160.33
Table
Table 5. Effect of combinations between essential oils and erythromycin.
Table 5. Effect of combinations between essential oils and erythromycin.
MicroorganismsCombinationsMIC
(μg/mL)		MICc
(μg/mL)		FICFICIInteraction
S. aureusC. khasianus14004660.330.66Partial synergistic
Erythromycin10.330.33
C. citratus12004000.330.66Partial synergistic
Erythromycin10.330.33
M. arvensis500012500.250.50Synergistic
Erythromycin10.250.25
M. luteusC. khasianus10002500.250.50Synergistic
Erythromycin10.250.25
C. citratus1150287.50.250.50Synergistic
Erythromycin10.250.25
M. arvensis500016660.330.66Partial synergistic
Erythromycin10.330.33
E. coliC. khasianus7002330.330.66Partial synergistic
Erythromycin1.50.50.33
C. citratus8002000.250.50Synergistic
Erythromycin1.50.370.25
M. arvensis25006250.250.50Synergistic
Erythromycin1.50.370.25
B. subtilisC. khasianus9002250.250.50Synergistic
Erythromycin10.250.25
C. citratus13004330.330.66Partial synergistic
Erythromycin10.330.33
M. arvensis350011660.330.66Partial synergistic
Erythromycin10.330.33
K. pneumoniaeC. khasianus8002660.330.66Partial synergistic
Erythromycin10.330.33
C. citratus9003000.330.66Partial synergistic
Erythromycin10.330.33
M. arvensis25006250.250.50Synergistic
Erythromycin10.250.25
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Sharma, N.; Sheikh, Z.N.; Alamri, S.; Singh, B.; Kesawat, M.S.; Guleria, S. Chemical Composition, Antibacterial and Combinatorial Effects of the Essential Oils from Cymbopogon spp. and Mentha arvensis with Conventional Antibiotics. Agronomy 2023, 13, 1091. https://doi.org/10.3390/agronomy13041091

AMA Style

Sharma N, Sheikh ZN, Alamri S, Singh B, Kesawat MS, Guleria S. Chemical Composition, Antibacterial and Combinatorial Effects of the Essential Oils from Cymbopogon spp. and Mentha arvensis with Conventional Antibiotics. Agronomy. 2023; 13(4):1091. https://doi.org/10.3390/agronomy13041091

Chicago/Turabian Style

Sharma, Neha, Zahid Nabi Sheikh, Saud Alamri, Bikarma Singh, Mahipal Singh Kesawat, and Sanjay Guleria. 2023. "Chemical Composition, Antibacterial and Combinatorial Effects of the Essential Oils from Cymbopogon spp. and Mentha arvensis with Conventional Antibiotics" Agronomy 13, no. 4: 1091. https://doi.org/10.3390/agronomy13041091

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