Evaluation of the antibacterial activity of essential oils from oregano (Origanum vulgare) against Escherichia coli strains isolated from meat products

Avaliação da atividade antibacteriana do óleo essencial do orégano (Origanum vulgare) contra cepas Escherichia coli isoladas de produtos cárneos

Abstract

The objective of this study was to analyze the antimicrobial and anti-stick capacity of essential oil extracted from oregano (Origanum vulgare) in relation to various strains of Escherichia coli (Ec 41, Ec 42, Ec 44, Ec 45) isolated from meat products. Techniques such as Determination of Minimum Inhibitory Concentration were used (MIC) and Minimum Bactericidal Concentration (CBM). Furthermore, the method was used disk diffusion method to examine the interaction between O. vulgare essential oil and synthetic antibiotics. Determination of the Inhibitory Concentration was also carried out Minimum Adhesion (CIMA). The results indicated that O. vulgare oil demonstrated antimicrobial activity against the E. coli strains tested, with values of MIC ranging between 256 μg/mL and 512 μg/mL, and MBC values ranging between 256 μg/mL and 1.024 μg/mL. Regarding associations, it was observed that O. vulgare had an antagonistic effect towards certain antibiotics, mainly ampicillin, showing greater interference from the essential oil. Furthermore, the oil was effective in inhibiting the adherence of E. coli bacterial strains, demonstrating a more significant antibiofilm agent than 0.12% chlorhexidine digluconate, a commonly used antibacterial. In short, O. vulgare essential oil exhibited antimicrobial potential against E. coli strains isolated from meat products, suggesting which, upon more detailed investigations, could be used both in isolation or in combination with synthetic antibiotics to combat infections caused by this pathogen.

Keywords:
medicinal plants; ethnobotany; one health; bacteria

Resumo

O objetivo deste estudo foi realizar uma análise a capacidade antimicrobiana e antiaderente do óleo essencial extraído de orégano (Origanum vulgare) em relação às várias cepas de Escherichia coli (Ec 41, Ec 42, Ec 44, Ec 45) isoladas de produtos cárneos. Foram empregadas técnicas como a Determinação da Concentração Inibitória Mínima (CIM) e da Concentração Bactericida Mínima (CBM). Além do mais, utilizou-se o método de difusão em disco para examinar a interação entre o óleo essencial de O. vulgare e antibióticos sintéticos. Foi feito também a Determinação da Concentração Inibitória Mínima de Aderência (CIMA). Os resultados indicaram que o óleo de O. vulgare demonstrou atividade antimicrobiana contra as cepas de E. coli testadas, com valores de CIM variando entre 256 μg/mL e 512 μg/mL, e valores de CBM variando entre 256 μg/mL e 1,024 μg/mL. Em relação às associações, foi observado que o óleo de O. vulgare teve um efeito antagônico em relação a certos antibióticos, principalmente a ampicilina, mostrando uma interferência maior do óleo essencial. Ademais, o óleo foi eficaz na inibição da aderência das cepas bacterianas de E. coli, demonstrando um efeito antibiofilme mais significativo do que o digluconato de clorexidina a 0,12%, um agente antibacteriano comumente usado. Em suma, o óleo essencial de O. vulgare exibiu potencial antimicrobiano contra cepas de E. coli isoladas de produtos cárneos, sugerindo que, mediante investigações mais detalhadas, poderia ser empregado tanto isoladamente quanto em combinação com antimicrobianos sintéticos para o combate de infecções ocasionadas por esse microrganismo.

Palavras-chave:
plantas medicinais; etnobotânica; saúde única; bactérias

1. Introdução

Waterborne and foodborne disease (also known as food poisoning) is any disease that results from the consumption of water and/or food contaminated with pathogenic bacteria, viruses or parasites (Belina et al., 2021).

Every individual needs nutrients to survive; however, the consumption of certain foods can cause illness and even death in individuals with symptoms of diarrhea, headache, vomiting, nausea, abdominal cramps, etc. (Lee and Yoon, 2021). Foodborne pathogens (FBP) cause millions of cases of sporadic illnesses and chronic complications, as well as large and challenging outbreaks in many countries and between countries. The effect of these pathogens also varies from region to region, as the level of public awareness about food hygiene varies in different countries (Belina et al., 2021).

Escherichia coli is a Gram-negative rod-shaped bacterium, classified as a member of the Enterobacteriaceae family (Tenaillon et al., 2016). There are six well-studied intestinal pathotypes of E. coli, including Shiga toxin-producing E. coli (STEC), enteropathogenic E. coli (EPEC), enterotoxigenic E. coli (ETEC), enteroaggregative E. coli (EAEC), E. coli adherent and enteroinvasive E. coli. These strains are classified by virulence properties and pathogenicity mechanisms that cause gastrointestinal diseases, such as diarrhea (Nataro and Kaper, 1998; Kaper et al., 2004; Jang et al., 2017).

Gram-negative bacilli (GNB) infections are a growing problem in clinical practice mainly due to the emergence of antimicrobial resistance mechanisms to all or almost all antimicrobials used to treat patients (Souli et al., 2008). In fact, it is known that the indiscriminate use of antimicrobials selects 9 mutant clones due to their increased capacity to produce rare mutations. These clones are also known to exhibit greater recombination capacity. In samples of natural isolates of Escherichia coli, it was found that clones with intermediate mutation phenotypes carry significantly more antimicrobial resistance (AR) mutations (Durão et al., 2018).

It should also be taken into account that, generally, multidrug-resistant bacteria are resistant to three or more classes of antimicrobials (Gajdács, 2019) and that, in the last three decades, the number of antimicrobials developed and approved has fallen by more than half (Ventola, 2015), leading to a growing demand for new antimicrobial agents or strategies, with phytotherapy entering this context.

Food consumers and industries insist on the need for natural alternatives to ensure food safety and quality. As a response, the use of natural herb and spice products is an alternative to synthetic additives associated with toxic problems (Rodrigues, 2018).

Essential oils (EOs) of herbs and spices have been extensively studied due to their antipathogenic properties. Numerous in vitro and in vivo surveys have been conducted to evaluate the potential antibacterial, antiviral, and antifungal activities of EOs (Rodrigues, 2018). This type of study is of great importance due to the emergence of strains resistant to antimicrobials, the increase in the population with lower immunity and the increased incidence of infections associated with drug-resistant biofilms (Leyva-López et al., 2017).

Oregano is a plant that has been used as a food seasoning since ancient times. This name is used to refer to a wide variety of plants that share a particular flavor and odor (Calpouzos, 1954).

The use of OEO in the pharmaceutical, food and cosmetic industries has gained special interest. The limitation of synthetic food additives in the food industry has promoted their replacement by natural additives. OEO can be used as a stabilizer for 13 edible oils or meat products and even increases the oxidative stability of other products, such as French fries. In addition to its antioxidant properties, the antimicrobial properties of OEO make it a good candidate as a natural preservative (Dimarco Palencia et al., 2020).

Given the above, the general objective of the work is to evaluate the antibacterial activity of oregano essential oil (Origanum vulgare) against Escherichia coli strains isolated from meat products.

2. Materials and Methods

2.1. Study location

The laboratory tests were carried out in the Microbiology laboratory of the Central Laboratories of the Biological Sciences Academic Unit (UACB) of the Federal University of Campina Grande (UFCG)/Patos - PB.

2.2. Obtaining the essential oil

Oregano essential oil (Origanum vulgare) was purchased from Quinare (Ponta Grossa - Paraná). To carry out pharmacological tests, the compound was solubilized in the presence of the dispersants Tween 80 and dimethyl sulfoxide (DMSO) and diluted in distilled water (Allegrini et al., 1973).

2.3. Bacterial strains

Escherichia coli strains (Ec 41, Ec 42, Ec 44, Ec 45) were used isolated from meat products of animal origin, originating from the Microbiology at the UACB Laboratory Center – UFCG.

These strains were maintained on Muller-Hinton Agar (AMH) at 4 °C. The inocula were obtained through overnight cultures, overnight in AMH at 35 ± 2 °C and diluted in 0.9% sterile saline solution to reach the final concentration of approximately 1.5 x 10⁸ colony forming units per mL (CFU/mL), adjusted for turbidity compared to a suspension of barium sulfate and acid McFarland scale sulfur 0.5 (Bona et al., 2014).

2.4. Antimicrobials

Ampicillin (10 μg/mL), gentamicin (10 μg/mL), ceftazidime (30 μg/mL) and ciprofloxacin (5 μg/mL) were used according to recommendations from the Clinical and Laboratory Standards 35 Institute (CLSI, 2018).

2.5. Culture media

The culture media used in the tests were Mueller Hinton broth and solid Mueller Hinton Agar solid. Culture media were purchased from Difco® and prepared according to the manufacturer's instructions.

2.6. Determination of the Minimum Inhibitory Concentration (MIC)

The minimum inhibitory concentration was determined using the microdilution in a 96-well plate with a “U” bottom. Initially, in eachwell, 100 μL of Mueller Hinton broth, double concentrated, and 100 μL of the compound studied (essential oil from Origanum vulgare) were added to the plate, performing a serial dilution (proportion of two), obtaining concentrations of 1024, 512, 256, 128, 64, 32 and 16 μg/mL. The MIC determination was produced using 10 μL of suspension of microorganisms in each well, with approximately 1.5x10⁸ CFU/mL. In the penultimate well, the sterile control was produced containing 100 μL only of Muller Hinton broth, and in the final well, growth control was performed, containing only 10 μL of the suspension of microorganisms in 100 μL of broth. O assay was performed in duplicate. Plates were incubated at 35 ± 2 °C for 24 hours and, after this period of adequate bacterial incubation, the first reading was carried out of the results, in which 20 μL of sodium resazurin solution (SIGMA) was added, previously solubilized in sterilized distilled water, at a concentration of 0.01% (w/v). Resazurin is recognized as a colorimetric indicator of oxide- reduction for bacteria. Subsequently, a new incubation at 35 ± 2 °C. The reading was done visually to verify the absence or presence of microorganisms through formation of a cluster of cells (bud), as well as observation of changes in the color of the solution, from blue to pink, indicating growth. The MIC was determined as the lowest concentration of the compound that inhibits visible growth of the microorganism, verified by changing the color of the solution, from blue to pink, which indicates the growth of the microorganism (Palomino et al., 2002; Ostrosky et al., 2008; CLSI, 2012; Bona et al., 2014).

2.7. Determination of the Minimum Bactericidal Concentration (MBC)

After reading the Minimum Inhibitory Concentration results, inocula (10 μL) of dilutions from the MIC into Mueller-Hinton broth medium (100 μL/well) in a sterile microdilution plate for CBM determination. After incubation at 35 ± 2 °C for 24 hours, 20 μL of resazurin was added. One new incubation was carried out at 35 ± 2 °C to confirm the concentration capable of inhibiting the growth of bacterial species completely, which would be verified by the absence indicator dye color change (Ncube et al., 2008; Guerra et al., 2012).

2.8. Study of the association of O. vulgare oil with synthetic antimicrobials

To investigate the association of the product with antimicrobial agents, a disk diffusion technique in solid media using filter paper disks (Bauer et al., 1966; Oliveira et al., 2006). Using a sterile swab, a volume of approximately 1 mL of each bacterial suspension was inoculated onto the solid surface. Muller Hinton agar on sterile flat plates. Then paper disks (impregnated with microbial agents) were spread on MH agar medium with the bacterial suspension. Immediately thereafter, 20μL (MIC) of the compound tested were transferred to plates containing antimicrobial agents. A control negative, with the presence of only bacterial suspension and antimicrobial plaques was also done. Plates were incubated at 35 ± 2 °C for 24-48 hours and then reading. A synergistic effect was considered for the growth inhibitory halo microbial formed from the combination (oil + antimicrobial) presented diameter ≥ 2 mm compared to the inhibition halo formed by the action of antimicrobial alone. When the formation of the inhibition halo resulting from association resulting from the combined action (oil + antimicrobial) was lower in diameter than that developed by the isolated action of the antimicrobial, considered if an antagonistic effect. The effect was considered indifferent if the inhibition halo of combined application (oil + antimicrobial) showed the same result in diameter than that resulting from the use of an antimicrobial agent alone (Cleeland; Squires, 1991; Oliveira et al., 2006).

2.9. Determination of Minimum Adhesion Inhibitory Concentration (CIMA)

The Minimum Adhesion Inhibitory Concentration (MICA) of the compound was determined in the presence of 5% sucrose according to Albuquerque et al. (2010), using concentrations corresponding to the compound up to dilution 1:1024. From the growth of bacteria, the bacterial strain was cultivated in Mueller Hinton broth at 37 °C, then aliquoted 0.9 mL of subculture into test tubes, and then 0.1 mL of the corresponding solution was added to the test tubes dilutions of the compound. Incubation was carried out at 37 °C for 24 hours in inclined tubes at 30°. The reading was done by visual observation of the adhesion of the bacteria to the tube walls after shaking. The assay was performed in duplicate. O The same procedure was performed with the positive control, digluconate chlorhexidine 0.12% (Riohex Gard, Rioquímica, São José do Rio Preto, São Paulo). He was considered CIMA the concentration of a substance in contact with sucrose that prevented from adhering to the glass tube.

3. Results

3.1. Minimum Inhibitory Concentration (MIC)

Data regarding the minimum inhibitory concentration of O. vulgare essential oil against different strains of E. coli are detailed in Table 1. Efficacy was evaluated by observing bacterial growth, which occurred with an MIC of 256 μg/mL.

Table 1
Minimum Inhibitory Concentration (MIC) in μg/mL of Origanum vulgare against Escherichia coli strains isolated from meat products.

	Ec 41	Ec 42	Ec 44	Ec 45
1024 ìg/mL	+	+	+	+
512 ìg/mL	+	+	+	+
256 ìg/mL	+	+	+	+
128 ìg/mL	-	-	-	-
64 ìg/mL	-	-	-	-
32 ìg/mL	-	-	-	-

• Caption: (+) Inhibition of bacterial growth (-) Did not inhibit bacterial growth.

3.2. Minimum Bactericidal Concentration (MBC)

The results regarding the Minimum Bactericidal Concentration of the essential oil extracted from O. vulgare against E. coli are outlined in Table 2. An analysis of the data reveals that, for the most part, the MBC was recorded as being 256μg/mL.

Table 2
Minimum Bactericidal Concentration (MBC) in μg/mL of Origanum vulgare against Escherichia coli strains isolated from meat products.

	Ec 41	Ec 42	Ec 44	Ec 45
1024 ìg/mL	+	+	+	+
512 ìg/mL	+	+	+	+
256 ìg/mL	+	+	-	+
128 ìg/mL	-	-	-	-
64 ìg/mL	-	-	-	-
32 ìg/mL	-	-	-	-

• Caption: (+) Inhibition of bacterial growth (-) Did not inhibit bacterial growth.

3.3. Association of O. vulgare oil with synthetic antimicrobials

The diameters of the inhibition halos (mm) generated by the combination of O. vulgare essential oil with synthetic antimicrobials in E. coli strains are documented in Table 3. An analysis of the results indicates that, in the majority of strains, O. vulgare has been shown to have an antagonistic effect when combined with synthetic antibacterials.

Table 3
Interference of Origanum vulgare essential oil in association with synthetic antimicrobials for Escherichia coli strains.

Antibiotics		Microorganisms
		E. coli	E. coli	E. coli	E. coli
		Ec 41	Ec 42	Ec 44	Ec 45
Ampicilin	HIA	18 mm	20 mm	32 mm	30 mm
	HIA w/ OV	20 mm ↑	12 mm ↓	0 mm ↓	20 mm ↓
Gentamicin	HIA	24 mm	26 mm	18 mm	18 mm
	HIA w/ OV	14 mm ↓	20 mm ↓	20 mm ↑	20 mm ↑
Ciprofloxacin	HIA	40 mm	38 mm	26 mm	28 mm
	HIA w/ OV	30 mm ↓	30 mm ↓	16 mm ↓	24 mm ↓
Ceftazidime	HIA	24 mm	25 mm	22 mm	20 mm
	HIA w/ OV	18 mm ↓	26 mm ↑	26 mm ↑	20 mm *

• Caption: HIA: Antimicrobial inhibition halo. OV: Origanum vulgare. Synergistic effect (↑); Antagonistic effect (↓); Indifferent effect (*).

3.4. Minimum Inhibitory Concentration for Adherence (MICA)

The results of the Minimum Adhesion Inhibitory Concentration (MICA) of O. vulgare essential oil, as well as a comparison with the positive control (chlorhexidine 0.12%) against the Escherichia coli strain (Ec 41), are presented in Table 4. When analyzing the data, it is noted that the essential oil of O. vulgare managed to inhibit biofilm adhesion in a ratio of 1:32, thus demonstrating antibiofilm effects against the strain under study.

Table 4
Minimum Adhesion Inhibitory Concentration (MICA) of Origanum vulgare essential oil and 0.12% chlorhexidine digluconate against the Escherichia coli strain (Ec 41).

Origanum vulgare
1:1	1:2	1:4	1:8	1:16	1:32	1:64	1:128
-	-	-	-	-	-	+	+
0.12% Chlorhexidine digluconate
1:1	1:2	1:4	1:8	1:16	1:32	1:64	1:128
-	+	+	+	+	+	+	+

• Legend: (+) Adhesion to the tube wall (-) No adherence to the tube wall.

4. Discussion

A growing challenge is bacterial resistance to traditional antimicrobial agents, resulting in an obvious search for substances with new properties antimicrobials. In this context, natural products are an alternative viable treatment because it is widely accepted and available (Khadake et al., 2021; Bezerra et al., 2017). Certain characteristics of natural products, especially essential oils, place them as a promising option for treat bacterial infections, as certain plants contain compounds that demonstrated safety and efficacy against bacteria (Nakagawa et al., 2020). Therefore, essential oils have aroused interest as an object of research due to different antibacterial mechanisms (Cutrim et al., 2019).

According to the results of the Minimum Inhibitory Concentration (MIC), the essential oil of O. vulgare demonstrated an MIC of 256 μg/mL against the growth of different strains of Escherichia coli. For an antimicrobial activity to be classified as strong, its MIC should be up to 500 µg/mL, while MICs between 600 and 1500 µg/mL are considered moderate, and weak activity is indicated by MICs above 1500 µg/mL, as described by Sartoratto et al. (2004). Therefore, the strains investigated in this study showed strong antimicrobial activity.

The oil extracted from O. vulgare showed minimal bactericidal concentration (CBM) of 256 μg/mL for most strains, indicating their bactericidal activity. It was observed that the CBM value coincided in most of the strains tested with the MIC, indicating the bactericidal activity of this essential oil. Hafidh et al. (2011), classifies the compound as bactericidal or bacteriostatic is determined by the relationship between MBC and MIC. If this relationship is between 1:1 and 2:1, the composition is considered bactericidal, while the proportion greater than 2:1 indicates bacteriostatic character.

The results showed that the essential oil of O. vulgare presented strong inhibitory activity and bactericidal activity against strains of E. coli, which may be associated with a significant concentration of the compound 5-Isopropyl-2-methylphenol; 2-Methyl-5-(1-methyllethyl)phenol (carvacrol), whose concentration can vary from 40.52% to 69.1% (Silva et al., 2023; Penteado et al., 2021). Carvacrol is recognized for its antimicrobial properties (Oliveira et al., 2008), being able to disintegrate the outer membrane of gram-negative bacteria (Ultee et al., 2002).

In a study by Diniz et al. (2024), O. vulgare oil showed strong inhibitory and bactericidal activity against Klebsiella pneumoniae, Pseudomonas aeruginosa and Staphylococcus saprophyticus isolated from meat products, making it a natural product that may represent a viable option in the fight against DTHAs.

Another study that confirmed the data obtained in this work also evaluated the antibacterial activity of the essential oil against strains of E. coli (Ec 41, Ec 42, Ec 44 and Ec 45) isolated from meat products. This study carried out by Santos et al. (2024), who tested the antimicrobial potential of the essential oil of Eucalyptus radiata species, showed that these strains presented moderate antimicrobial activity when exposed to E. radiata.

The results of the effect of O. vulgare essential oil on the antibacterial activity of synthetic antibiotics (Table 3) are analyzed considering comparisons of the diameters of the halos that prevent the growth of bacteria in experiments with antibiotics alone and with essential oils. Some interactions indicate that the essential oil can affect the antibacterial effectiveness of antibiotics (Oliveira et al., 2006). Antagonistic effects of antibacterial agents, especially ampicillin, were observed in this study. This result contradicts the results of Santos et al. (2024) who discovered a synergistic effect of some antibiotics, mainly ceftriaxone, when combined with E. radiata essential oil.

The minimum anti-adhesion concentrations (MICA) of O. vulgare are shown in Table 4. Observing the results, O. vulgare essential oil effectively inhibited the adhesion of E. coli strains in the presence of sucrose, which showed better inhibition than 0.12% chlorhexidine digluconate.

In a previous study, Diniz et al. (2024) obtained effective inhibition of the adhesion of Pseudomonas aeruginosa using O. vulgare essential oil in the presence of sucrose, and Santos et al. (2024) obtained inhibition of E. coli adhesion when using the essential oil of E. radicata.

5. Conclusion

It can be concluded that the essential oil extracted from Origanum vulgare effectively inhibits the development of Gram-negative Escherichia coli isolated from meat products. Furthermore, O. vulgare oil increased the antibacterial activity of synthetic antimicrobials against several strains of E. coli. Furthermore, its effectiveness against E. coli bacterial strains exceeds the effectiveness of the antibacterial agent 0.12% chlorhexidine digluconate. In summary, O. vulgare oil showed promising antibacterial potential against strains of E. coli isolated from meat products, suggesting its viability both alone and in combination with synthetic antimicrobials to combat infections caused by this pathogen, although further studies are needed. to assess its full effectiveness.

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Publication Dates

• Publication in this collection
  10 Jan 2025
• Date of issue
  2024

History

• Received
  02 May 2024
• Accepted
  22 Sept 2024