Antibacterial activity of nanoemulsion of essential oil from Brazilian pepper tree (Schinus terebinthifolia Raddi) against sensitive and multidrug-resistant strainsAbstract
Schinus terebinthifolia, a species of the Anacardiaceae family, is known for its medicinal properties and high yield of essential oil with significant biological activities, particularly antibacterial. Nanoemulsions enhance the bioavailability and efficacy of these compounds. This study evaluated the antibacterial activity of different concentrations of nanoemulsion of essential oil extracted from S. terebinthifolia fruits. Tests were conducted on sensitive strains (Escherichia coli 25922, Pseudomonas aeruginosa, Staphylococcus aureus, and Proteus mirabilis) and multidrug-resistant bacterial isolates. Formulations were characterized for their physicochemical properties, and antibacterial activity was determined using the microdilution method to assess minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC). The nanoemulsion exhibited superior antibacterial activity compared to pure essential oil. The best results were observed against sensitive strains of E. coli (MIC and MBC of 0.005 mg/mL) and S. aureus (MIC of 0.39 mg/mL and MBC of 0.78 mg/mL). Among multidrug-resistant isolates, the nanoemulsion was most effective against MCR-2 producing E. coli (MIC of 0.19 mg/mL). The nanoemulsion outperformed the pure essential oil, likely due to increased particle number and longer contact time with microbial cell surfaces. Nanoemulsions of S. terebinthifolia essential oil significantly enhance antibacterial activity and have potential applications in medicinal and cosmetic products. This study supports the development of nanoformulations to improve the bioavailability and efficacy of essential oils.
Keywords:
Anacardiaceae; gas-chromatography; secondary metabolites; nanotechnology
Resumo
Schinus terebinthifolia, uma espécie da família Anacardiaceae, é conhecida por suas propriedades medicinais e alto rendimento de óleo essencial com atividades biológicas significativas, especialmente antibacterianas. As nanoemulsões podem melhorar a biodisponibilidade e a eficácia desses compostos. Este estudo avaliou a atividade antibacteriana de diferentes concentrações de nanoemulsão do óleo essencial extraído dos frutos de S. terebinthifolia. Foram realizados testes em cepas sensíveis (Escherichia coli 25922, Pseudomonas aeruginosa, Staphylococcus aureus e Proteus mirabilis) e isolados bacterianos multirresistentes. As formulações foram caracterizadas quanto às suas propriedades físico-químicas, e a atividade antibacteriana foi determinada utilizando o método de microdiluição para avaliar a concentração inibitória mínima (CIM) e a concentração bactericida mínima (CBM). A nanoemulsão apresentou atividade antibacteriana superior em comparação com o óleo essencial puro. Os melhores resultados foram observados contra cepas sensíveis de E. coli (CIM e CBM de 0,005 mg/mL) e S. aureus (CIM de 0,39 mg/mL e CBM de 0,78 mg/mL). Entre os isolados multirresistentes, a nanoemulsão foi mais eficaz contra E. coli produtora de MCR-2 (CIM de 0,19 mg/mL). A nanoemulsão superou o óleo essencial puro, provavelmente devido ao maior número de partículas e ao maior tempo de contato com as superfícies das células microbianas. As nanoemulsões de óleo essencial de S. terebinthifolia aumentam significativamente a atividade antibacteriana e têm potencial para aplicações em produtos medicinais e cosméticos. Este estudo apoia o desenvolvimento de nanoformulações para melhorar a biodisponibilidade e a eficácia dos óleos essenciais.
Palavras-chave:
Anacardiaceae; cromatografia gasosa; metabolitos secundários; nanotecnologia
1. Introduction
Bacterial resistance has become a significant public health challenge due to the diverse physiological resistance mechanisms exhibited by bacteria. These mechanisms include reduced permeability and the production of degradative enzymes such as beta-lactamases, which directly inhibit the action of antimicrobials of the beta-lactam class (Castro et al., 2023). Additionally, certain bacteria may exhibit resistance to cephalosporins (ESBL-producing bacteria), carbapenems (KPC- and NDM-producing bacteria), and polymyxins (MCR-producing bacteria). These bacteria can significantly impact morbidity and mortality rates due to the limited availability of effective treatments (Carvalho et al., 2021).
Controlling the incidence of bacteria impacting healthcare processes is crucial. A potential solution is using antimicrobial drugs derived from the essential oil extracted from the fruits of Schinus terebinthifolia, as these plants possess biological activities and yield high amounts of essential oil (Barraqui et al., 2023; Gomes et al., 2020).
Schinus terebinthifolia Raddi is a species of the Anacardiaceae family, native to South America, mainly found in Brazil, Paraguay, and Argentina. It is commonly referred to as the Brazilian pepper tree, aroeira, or pink pepper. The fruits of this species are widely marketed as dried fruits and used as a food condiment. They are also utilized in the cosmetics and pharmaceutical industries (Oliveira et al., 2020). The S. terebinthifolia species is recognized for its ability to produce essential oils in various plant parts, such as leaves, fruits, and stems (Ennigrou et al., 2017). However, the fruit is the commonly used part for obtaining essential oil, with yields ranging from 5.50% to 8.81%. The essential oil is predominantly composed of monoterpenes, such as α-phellandrene, α-pinene, and limonene, and sesquiterpenes, such as germacrene-D (Tlili et al., 2018; Barraqui et al., 2023).
The essential oil extracted from the fruits of S. terebinthifolia has been found to possess several biological activities, such as antioxidant (Oliveira et al., 2020), antifungal (Mohamed et al., 2020), insecticidal (Belhoussaine et al., 2022), anti-inflammatory (Marangoni and Pinto, 2023), and antibacterial (Uliana et al., 2016; Costa da Silva et al., 2023) properties. S. terebinthifolia essential oils were found to have antibacterial activity against American Type Culture Collection (ATCC) and multidrug-resistant strains, which may promote bacteriostatic or bactericidal effects, supporting the development of bacterial control measures.
Nanotechnology can enhance the efficacy of active ingredients in essential oils through the production of nanoformulations and nanomaterials that increase the bioavailability of active compounds and the permeability of less soluble and turbid compounds in contrast to conventional emulsion systems, as pointed out by Sheth et al. (2020). Nanoemulsions have various applications in industries such as cosmetics, topical pharmaceuticals, and polymer films to improve disease treatment (Fernandes et al., 2023). In addition, they improve the bioavailability and efficacy of antibiotics, making them a promising strategy for the development of new products (Gharsan et al., 2022).
The aim of this study was to evaluate a nanoemulsion of essential oil extracted from the fruits of Schinus terebinthifolia and its antibacterial activity against sensitive and multiresistant strains.
2. Methodology
2.1. Obtaining of Schinus terebinthifolia essential oil
S. terebinthifolia essential oil was obtained from Nativa da Foz, a company representing family farmers in São Mateus, Espírito Santo, Brazil.
2.2. Chromatographic analysis
Gas chromatography coupled to mass spectroscopy (GC/MS) was used to analyze the essential oil of Schinus terebinthifolia. The analysis was performed using an Agilent GCMS-5977C model and HP-5MS UI capillary columns (30 m × 250 μm × 0.25 μm). The oven temperature was programmed to increase from 50 to 250 °C (3 °C/min) and held for 10 min at 250 °C. Helium was used as the carrier gas with an injection volume of 2 μL in split ratio mode 1:10 and a flow rate of 1 mL/min. The interface temperature was set to 250 °C, with the MS source and MS quadrupole temperatures set to 230 °C and 150 °C, respectively. The ionization energy was set to 70 eV and the scan range was 35-550 units. Compounds were identified using their retention indices and mass spectra.
A series of n-alkanes was also analyzed under the same chromatographic conditions to calculate the retention index of the substances. The chemical constituents of the samples were identified by comparing the mass spectra with the NIST library database and the retention indices with the literature (Adams, 2009).
2.3. Nanoemulsion preparation
The nanoemulsions were prepared using the low-energy phase inversion method. The oil phase consisted of essential oil at a concentration of 5% and the emulsifiers polysorbate 20, polysorbate 80, sorbitan monooleate, and sorbitan trioleate. The emulsifiers were combined to obtain mixtures with hydrophilic-lipophilic balance (HLB) values of 10, 11, 13, and 15, with concentrations of 5%, 10%, 15%, and 20%. To complete the aqueous phase, water was added until the final volume of the solution reached 1.0 g. The oil phase was stirred while the aqueous phase was added using a Vortex (Model VX-38).
The stability of the nanoemulsions was assessed over a 60-day period through macroscopic analysis, evaluating color, visual appearance, and phase separation. The nanoemulsions were kept in glass tubes at room temperature (25 ± 2 °C) during this period.
2.4. Dynamic light scattering (DLS) analysis of nanoemulsions
The dynamic light scattering (DLS) technique was used to determine the average particle size of the nanoparticles. A Microtrac DLS instrument (Ding et al., 2017) was employed to measure the particle size of nanoemulsion samples containing a 5% concentration of Schinus terebinthifolia essential oil. DLS analysis was performed on the day of nanoemulsion preparation, as well as after three days and four months of storage. This approach allowed for the evaluation of possible variations in nanoemulsion particle size over time.
2.5. Antimicrobial activity of Schinus terebinthifolia nanoemulsion
2.5.1. Sample preparation for tests
The nanoemulsion samples were prepared at a concentration of 50.0 mg/mL of Schinus terebinthifolia essential oil. For the positive control, 100 µL of Mueller Hinton broth and 5 µL of bacterial suspension were added. A second positive control was prepared containing 100 µL of Mueller Hinton broth, 100 µL of Polysorbate 80, and 5 µL of bacterial suspension. For the negative control, 100 µL of Mueller Hinton broth and 100 µL of nanoemulsion were used.
In the experiments, pure S. terebinthifolia essential oil at a concentration of 50.0 mg/mL was diluted in Polysorbate 80 for comparison purposes, following the same procedure. The tests were conducted in triplicate according to the standardized broth microdilution methods, ensuring reproducibility and accuracy of the results obtained.
2.5.2. Bacterial isolates
The study tested the sensitive ATCC strains Escherichia coli ATCC 25922, Pseudomonas aeruginosa ATCC 27853, Staphylococcus aureus ATCC 25923, and Proteus mirabilis ATCC 25933, as well as several bacterial isolates with a multidrug-resistant profile. ESBL-producing E. coli, KPC2-producing E. coli, IMP-1-producing E. coli, ESBL- and KPC-producing E. coli, and MCR-1, MCR-2, MCR-3, MCR-4, and MCR-5-producing E. coli; KPC-2- and NDM-1-producing Klebsiella pneumoniae; and SPM-1-producing P. aeruginosa. The following strains were inoculated and incubated: Gram-negative strains were inoculated onto MacConkey agar, while gram-positive strains were inoculated onto Mannitol agar. The inoculated strains were then incubated in a bacteriological incubator for 18 - 24 hours at 36 ± 1 °C.
2.5.3. Determination of minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC)
The MIC was determined using the broth microdilution method, adapted from the Clinical and Laboratory Standards Institute (CLSI) guidelines (NCCLS document M7-A7, 2006). The analyses were performed in triplicate using sterile 96-well V-bottom microplates made of polystyrene and sterilized by gamma radiation. One hundred microliters of cation-adjusted Mueller Hinton broth were added to each well of the microplate.
The first well received 100 µL of S. terebinthifolia essential oil nanoemulsion at a concentration of 50 mg/mL. Serial dilutions were performed on the microdilution plate, reaching concentrations of 25mg/mL; 12.5mg/mL; 6.25 mg/mL; 3.12 mg/mL; 1.56 mg/mL; 0.78 mg/mL; 0.39 mg/mL; 0.19 mg/mL; 0.09 mg/mL; 0.04 mg/mL; 0.02mg/mL; 0.01 mg/mL; 0.005 mg/mL; 0.025 mg/mL; 0.001 mg/mL; 0.0006 mg/mL; 0.0003 mg/mL; 0.00015 mg/mL; 0.00007 mg/mL; 0.000035 mg/mL.
Bacterial suspensions were then prepared at a concentration of 1.5 × 108 bacteria mL-1. One hundred microliters of the bacterial suspension were added to tubes containing 900 µL of autoclaved distilled water, resulting in a 1:10 dilution. After, 5 µL of this diluted bacterial suspension were added to the microplate wells.
The positive control consisted of adding 5 µL of the bacterial suspension to 100 µL of Mueller Hinton broth. The negative control comprised of adding 100 µL of nanoemulsion to the Mueler Hinton broth. To each well of the microplate, 100 µL of cation-adjusted Mueller-Hinton broth was added.
The microplates were incubated in a bacteriological incubator for 18-24 hours at 36 ± 1 °C. The MIC was determined as the lowest concentration with no visible bacterial growth. The MBC was determined by addition of 100 µL withdrawn from wells with no visible bacterial growth and inoculated onto Petri dishes containing Mueller Hinton agar by surface spreading with a Drigalski spatula. The plates were incubated in a bacteriological incubator for 18-24 hours at 36 ± 1 °C. The MBC was determined as the lowest concentration with no colony growth.
3. Results and Discussion
3.1. Essential oil composition
The GC/MS analysis of the essential oil of S. terebinthifolia revealed the presence of 10 major compounds, including eight monoterpenes (α-pinene; myrcene; α-phellandrene; o-cymene; α-thujene; camphene; pinene; δ-3 carene) and two sesquiterpenes (sylvestrene and terpinolene) (Table 1 and Figure 1).
Schimitberger et al. (2018) identified the primary components of the essential oil from mature fruits of Schinus terebinthifolia as δ-3-carene (46.67%), α-pinene (14.98%), myrcene (1.76%), α-phellandrene (4.38%), sylvestrene (9.24%), and terpinolene (1.33%), corroborating the chemical profile presented in this study.
Conversely, Cavalcanti et al. (2015) highlighted δ-3-carene (41.01%), α-phellandrene (14.40%), limonene (12.36%), and α-pinene (10.36%) as the major constituents. In the study by Barraqui et al. (2023), the volatile compounds of aroeira fruits were analyzed using GC/MS with a headspace injector, revealing a predominance of germacrene-D, limonene, p-cymene, α-phellandrene, α-pinene, β-caryophyllene, β-phellandrene, β-myrcene, and δ-3-carene.
Variations in the chemical profile of essential oils can be attributed to fluctuations in the secondary metabolism of plants, biosynthesis, or accumulation due to abiotic factors such as temperature, circadian cycle, and soil nutrients (Zhang et al., 2023). These variations may also be influenced by factors such as collection methods, extraction time, extraction type, and biotic factors, including interactions with insects and microorganisms (Gobbo-Neto and Lopes, 2007).
3.2. Development of nanoemulsions
Macroscopic analysis of the samples indicated that colloids system containing 10% and 20% emulsifiers with various hydrophilic-lipophilic balance (HLB) values (10, 11, 13, and 15) exhibited a whitish and milky appearance, suggesting the absence of nanoemulsion formation (Figure 2).
Samples with 10% emulsifier, 20% emulsifier and 15% emulsifier with different hydrophilic-lipophilic balance (HLB) values.
From the series of analyses examining concentration and HLB variations, the most promising results were observed in samples containing polysorbate 20 and sorbitan trioleate with an HLB of 15. These samples consisted of 5% essential oil, 80% water, and 15% emulsifier; and 5% essential oil, 75% water, and 20% emulsifier (Figure 2). The samples were diluted at a 1:10 ratio, i.e., 900 µL of water were added to 100 µL of the colloid system, to assess the stability of the nanoemulsion.
3.3. Physical stability of nanoemulsion
Mixtures containing the emulsifiers polysorbate 20 and sorbitan trioleate with an HLB of 15, at emulsifier proportions of 15% and 20%, exhibited a homogeneous, translucent appearance with a bluish color under direct light, as observed in the macroscopic analysis (Figure 3).
Nanoemulsion with 5% Schinus terebinthifolia essential oil, 15% polysorbate 20, 20% sorbitan trioleate, with hydrophilic-lipophilic balance (HLB) of 15, showing a bluish color.
The primary distinction between nanoemulsions and traditional emulsions is that nanoemulsion droplets are in the nanoscale range (between 20 and 200 nm), presenting a translucent single-phase appearance with a bluish color due to the Tyndall optical effect of light scattering. In this context, the Tyndall effect indicates the potential existence of a more stable nanostructured system based on its light scattering properties (Pinto et al., 2023).
The Tyndall effect, resulting from light scattering by particles in the nanoscale range, indicated the formation of a more stable nanostructured system. Dynamic light scattering (DLS) analysis confirmed the presence of nanoscale particles, with average diameters of 31.2 nm for samples with 15% emulsifier. This result is consistent with the literature, suggesting that nanoemulsions with smaller particles tend to be more stable due to their larger surface area and reduced tendency for coalescence.
3.4. Dynamic light scattering (DLS)
Nanostructured systems presenting stability in macroscopic analyses were subjected to DLS analysis for determining the size of the particles and their frequency in the colloidal system in terms of volume and intensity (Figure 4).
Dynamic light scattering (DLS) of nanoemulsions of Schinus terebinthifolia essential oil containing 15% emulsifier (polysorbate 20 and sorbitan trioleate) with hydrophilic-lipophilic balance (HLB) of 15, analyzed on the day of preparation (A), after three days (B), and after four months (C). DLS of S. terebinthifolia essential oil nanoemulsions containing 20% emulsifier (polysorbate 20 and sorbitan trioleate) with HLB 15, analyzed on the day of preparation (D), after three days (E), and after four months (F).
The DLS analysis results (Figure 4) revealed significant differences between more concentrated and more diluted samples. A comparison of samples with an HLB of 15 and 15% emulsifier to those containing 20% emulsifier revealed that the samples with 15% emulsifier contained particles with a smaller diameter (31.2 nm).
According to Toma (2019), the diameter of particles is influenced by the arrangement of water molecules in suspension, as emulsifiers cause water molecules to form a highly ordered envelope around each solute molecule. The addition of a larger volume of water induces non-polar regions to cluster more tightly, forming a smaller hydrophobic region and further reducing the size of the oil droplets in the nanoemulsion. Larger particles exhibit higher intensity values due to increased diffusion speed.
A key factor in the stability of nanoemulsions is the suppression of Ostwald ripening, a phenomenon where larger droplets grow at the expense of smaller ones due to the difference in solubility between different-sized droplets. Ostwald ripening can significantly affect the long-term stability of nanoemulsions, leading to phase separation and loss of the nanoscale size distribution. The selection of appropriate emulsifiers and HLB values in this study likely contributed to minimizing Ostwald ripening, as evidenced by the stable particle size distribution observed over four months.
The stability tests and all DLS analyses were conducted to identify the optimal conditions for preparing samples for microbiological analyses. Consequently, nanoemulsions with an HLB of 15 and 15% emulsifier were selected for their particle diameter of approximately 30 nm. These samples-maintained stability even after four months, with a particle diameter of approximately 60 nm.
3.5. Antimicrobial activity
The results of the minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) indicated that the nanoemulsion exhibited superior values compared to the pure essential oil (Table 2).
Minimum inhibitory concentration (MIC; mg/mL) and minimum bactericidal concentration (MBC; mg/mL) of pure essential oil of Schinus terebinthifolia and essential oil nanoemulsion against sensitive and multidrug-resistant bacterial strains.
This demonstrates both bacteriostatic and bactericidal activity of the pure essential oil against the bacteria. The essential oil exhibited an antibacterial spectrum, except for MCR-5-producing E. coli, ESBL-producing E. coli, and SPM-1-producing Pseudomonas aeruginosa.
Salem et al. (2018) found antibacterial activity of essential oil extracted from ripe fruits of S. terebinthifolia against sensitive strains S. aureus and P. aeruginosa. Additionally, Gundidza et al. (2009) reported antibacterial activity of S. terebinthifolia essential oil against E. coli.
The antibacterial activity of S. terebinthifolia essential oil against S. aureus found in the present study was similar to that reported by Oliveira et al. (2020), who found MIC ranging between 0.5 and 1.0 mg/mL. However, the MIC against P. aeruginosa found in the present study was higher than that reported by Santos et al. (2019), who found an MIC of 0.039 mg/mL when using S. terebinthifolia essential oil.
The MIC determined for the nanoemulsion of S. terebinthifolia essential oil against the tested microorganisms demonstrated its antibacterial potential. According to Krishnamoorthy et al. (2018), nanoemulsions are effective antimicrobials with broad-spectrum bactericidal activity, causing damage to the functional structures of bacteria.
Regarding MBC, the nanoemulsion showed bactericidal activity against S. aureus (up to a dilution of 1.34 mg/mL), P. aeruginosa (up to 5.37 mg/mL), Proteus mirabilis (up to 2.68 mg/mL), and E. coli (up to 0.005 mg/mL).
Considering multidrug-resistant isolates, the nanoemulsion demonstrated better antibacterial activity against MCR-1, MCR-2, and MCR-3-producing E. coli; however, it exhibited no antimicrobial activity against MCR-5-producing E. coli, ESBL-producing E. coli, SPM-1-producing P. aeruginosa, and KPC-2- and NDM-1-producing K. pneumoniae.
The MIC and MBC results indicated the active biological activity of the tested nanoemulsions in inhibiting S. aureus, P. aeruginosa, P. mirabilis, and E. coli. According to Dannenberg et al. (2019), natural products exhibit suitable antimicrobial activity when the inhibitory concentration is less than 100 mg/mL. The MIC and MBC found in the present study for the nanoemulsion of S. terebinthifolia essential oil were significantly low, denoting high antimicrobial activity.
Similarly, Cutro et al. (2023) found higher antibacterial activity against E. coli and attributed this result to the bacterial structure. Therefore, the use of nanoemulsions of S. terebinthifolia essential oils is a strategy for reducing essential oil concentrations while improving their antimicrobial activity (Donsi and Ferrari, 2016).
4. Conclusions
The nanoformulations of Schinus terebinthifolia essential oil containing 15% emulsifier (polysorbate 20 and sorbitan trioleate) with a hydrophilic-lipophilic balance of 15 at room temperature were the most stable, as they formed smaller, more cohesive, and resistant particles.
The nanoemulsion of S. terebinthifolia essential oil showed antibacterial activity against sensitive strains (ATCC) of Staphylococcus aureus, Pseudomonas aeruginosa, Proteus mirabilis, and Escherichia coli. Regarding multidrug-resistant isolates, the nanoemulsion showed better antibacterial activity against MCR-1, MCR-2, and MCR-3-producing E. coli.
Therefore, nanoformulations of S. terebinthifolia essential oil can significantly contribute to improve the biological activities of the essential oil.
Acknowledgements
The authors thank the Federal University of Espírito Santo (UFES), the Federal Institute of Education, Science, and Technology of Espírito Santo (IFES - Vila Velha campus) by support from PRODIF, and the Espírito Santo Research and Innovation Support Foundation (FAPES). Federal University of Espirito Santo - Brazil (UFES) for all the infrastructure provided to carry out the research.
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