Acessibilidade / Reportar erro

Essential Oil Compositions and Antimicrobial Activities of Thymbra spicata L. var. spicata L., Lavandula X Intermedia Emeric ex Loisel., Satureja macrantha C. A. MEYER and Rosmarinus officinalis L.

Abstract

Medicinal and aromatic plants have been widely using in folk medicine as antimicrobial, anti-inflammatory and antinociceptive agents. The aim of this study was to determine essential oil composition and antimicrobial activity of T. spicata, L. X Intermedia, S. macrantha and R. officinalis. Essential oil components of these plants were obtained by water vapor distillation method using Neo-Clevenger apparatus. Essential oil components were determined by gas chromatography-mass spectroscopy (GC-MS). The main components of these plants are carvacrol (74.26 %) and γ-terpinene (10.28%) in T. spicata, 1,8-cineol (32.48%), linalool (24.38%) and camphor (14.73%) in L. X Intermedia, p-cymene (56.70%), carvacrol (10.96 %) in S. macrantha and camphor (18.26 %), α-pinene (15.51%), 1,8-cineole (11.86%) and borneol (10.39%) in R. officinalis were determined. T. spicata and S. macrantha showed strong effects against three microorganisms. L. X Intermedia and R. officinalis showed strong activity against Candida albicans, while they had moderate effects against Staphylococcus aureus, Escherichia coli.

Keywords:
medicinal and aromatic plants; essential oils; major compounds; GC-MS

GRAPHICAL ABSTRACT

HIGHLIGHTS

  • Essential oil contents of T. spicata, L. X Intermedia, S. macrantha and R. officinalis was determined.

  • The main components of these plants were monoterpenoid

  • T. spicata and S. macrantha showed strong effects against three microorganisms.

HIGHLIGHTS

  • Essential oil contents of T. spicata, L. X Intermedia, S. macrantha and R. officinalis was determined.

  • The main components of these plants were monoterpenoid

  • T. spicata and S. macrantha showed strong effects against three microorganisms.

INTRODUCTION

Antibiotics have contributed to saving lives of millions of people by treating the microbial infections and achieving significant gains in life expectancy. However, clinical efficacy of many existing antibiotics is threatened by the emergence of multiple drug resistant (MDR) pathogens [11 Bandow JE, Brötz H, Leichert LI, Labischinski H, Hecker M. Proteomic approach to understanding antibiotic action. Antimicrob Agents Chemother. 2003;47:948-55. doi:10.1128/aac.47.3.948-955.2003.
https://doi.org/10.1128/aac.47.3.948-955...
], and unwanted side effects of some antibiotics [22 Cunha BA. Antibiotic side effects. Med Clin North Am. 2001;85:149-85. doi:10.1016/s0025-7125(05)70309-6.
https://doi.org/10.1016/s0025-7125(05)70...
]. Antibiotic resistance is rising to dangerously high levels in all around the world. The overuse and misuse of these drugs are also important factors in development of antibiotic resistance. The emergence of antibiotic resistance increases the burden on the health system and economy because of prolonged hospital stays and higher medical costs [33 Ventola CL, The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther. 2015; 40: 277-83.,44 Warnes SL, Keevil CW. Lack of Involvement of Fenton Chemistry in Death of Methicillin-Resistant and Methicillin-Sensitive Strains of Staphylococcus aureus and Destruction of Their Genomes on Wet or Dry Copper Alloy Surfaces. Appl Environ Microbiol. 2016;82:2132-6. doi:10.1128/AEM.03861-15.
https://doi.org/10.1128/AEM.03861-15....
]. Antibiotics are not taken only by using for their therapeutic purposes, but also with consumption as food by humans of livestocks given antibiotic [55 Golkar Z, Bagazra O, Pace DG. Bacteriophage therapy: a potential solution for the antibiotic resistance crisis. J Infect Dev Ctries. 2014; 13: 129-36. doi:10.3855/jidc.3573.
https://doi.org/10.3855/jidc.3573....
].

One of the MDR pathogens that has become a major problem all over the world, Staphylococcus aureus (Gram positive bacterium) is among the most common bacterial pathogens that a significant cause of soft tissue infections, arthritis, pneumonia, sepsis, osteomyelitis and skin infections [66 Tong SY, Davis JS, Eichenberger E, Holland TL, Jr Fowler VG. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015; 28: 603-61. doi:10.1128/CMR.00134-14.
https://doi.org/10.1128/CMR.00134-14...
], Escherichia coli, a Gram-negative bacterium, is a pathogen that cause food-borne outbreaks [77 Minogue TD, Daligault HA, Davenport KW, Bishop-Lilly KA, Broomall SM, Bruce DC, et al. Complete genome assembly of Escherichia coli ATCC 25922, a serotype O6 reference strain. Genome Announc. 2014; 2(5): e00969-14. doi:10.1128/genomeA.00969-14.
https://doi.org/10.1128/genomeA.00969-14...
] and Candida albicans is a pathogen thrush [88 Latifah-Munirah B, Himratul-Aznita WH, Mohd Zain N. Eugenol, an essential oil of clove, causes disruption to the cell wall of Candida albicans (ATCC 14053). Front Life Sci. 2015;8:231-40. doi:10.1080/21553769.2015.1045628.
https://doi.org/10.1080/21553769.2015.10...
].

Plants synthesize a wide range of molecules formed as a result of their metabolic activities. These compounds are known as secondary metabolites including; phenolics, flavonoids, alkaloids and terpenoids, and normally produced to protect themselves against viruses, fungi, bacteria and environment stresses [99 Erb M, Kliebenstein DJ. Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy. Plant Physiol. 2020;184(1):39-52. doi: 10.1104/pp.20.00433.
https://doi.org/10.1104/pp.20.00433...
], at the same time plant secondary metabolites are a main source of many raw materials used in cosmetics, flavouring and in making drugs or direct use as herbal medicine to treat sickness and ailments [1010 Wurtzel ET, Kutchan TM. Plant metabolism, the diverse chemistry set of the future. Science. 2016;353(6305):1232-6. doi:10.1126/science.aad2062.
https://doi.org/10.1126/science.aad2062...
]. Almost 25% of medicines used in treatment are originated from medicinal plants [1111 De Luca V, Salim V, Atsumi SM, Yu F. Mining the biodiversity of plants: a revolution in the making. Science. 2012;336(6089):1658-61. doi: 10.1126/science.1217410.
https://doi.org/10.1126/science.1217410....
]. Medicinal and aromatic plants are the main source of many essential oils [1212 Cox-Georgian D, Ramadoss N, Dona C, Basu C. Therapeutic and Medicinal Uses of Terpenes. J Med Plant. 2019; 333-359. doi:10.1007/978-3-030-31269-5_15.
https://doi.org/10.1007/978-3-030-31269-...
,1313 Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils-A review. Food Chem Toxicol. 2008;46:446-75. doi:10.1016/j.fct.2007.09.106.
https://doi.org/10.1016/j.fct.2007.09.10...
]. Carvacrol, thymol, menthol, and 1,8-cineol are the most common essential oils in medicinal and aromatic plants including oregano, mint and thyme [1414 Ekren S, Yerlikaya O, Tokul HE, Akpınar A, Acu M. Chemical composition, antimicrobial activity and antioxidant capacity of some medicinal and aromatic plant extracts. Afr J Microbiol Res. 2013;7:383-88. doi:10.5897/AJMR12.1765.
https://doi.org/10.5897/AJMR12.1765...
].

Medicinal plants are preferred in the treatment of diseases due to their possibility of use in various forms [1515 Tuzlacı E, Aymaz PE, Turkish folk medicinal plants, part IV: Gönen (Balıkesir). Fitoterapia. 2001;72:323-43. doi:10.1016/s0367-326x(00)00277-x.
https://doi.org/10.1016/s0367-326x(00)00...
, 1616 Ray A, Jena S, Dash B, Kar B, Halder T, Chatterjee T, et al. Chemical diversity, antioxidant and antimicrobial activities of the essential oils from Indian populations of Hedychium coronarium Koen. Ind Crops Prod. 2018;112:353-62. doi: 10.1016/j.indcrop.2017.12.033
https://doi.org/10.1016/j.indcrop.2017.1...
], effective, economical, and easily accessible [1717 Hosseinzadeh S, Jafarikukhdan A, Hosseini A, Armand R. The Application of Medicinal Plants in Traditional and Modern Medicine: A Review of Thymus vulgaris. J Clin Med. 2015;6:635-42. doi:10.4236/ijcm.2015.69084.
https://doi.org/10.4236/ijcm.2015.69084....
] and not toxic. Plant essential oils are odorous and volatile compounds accumulated in special cells of many medicinal and aromatic plants including glandular hair, glands, resin and oil ducts. These components are obtained with various extraction methods by hydro distillation, pressing and steam distillation from different parts of plants such as the parts of leaves, flowers and seeds. Essential oils are used in the treatment of several disorders in animals, humans, foods and plants, safer than antibiotics and chemical drugs [1818 Tanhaeian A, Sekhavati MH, Moghaddam M. Antimicrobial activity of some plant essential oils and an antimicrobial-peptide against some clinically isolated pathogens. Chem Biol Technol Agric. 2020;7:13. doi:10.1186/s40538-020-00181-9.
https://doi.org/10.1186/s40538-020-00181...
, 1919 Moghaddam M, Mehdizadeh L. Essential oil and antifungal therapy. In: Basak A., Chakraborty R., Mandal S. (eds) Recent Trends in Antifungal Agents and Antifungal Therapy. New Delhi: Springer; 2016. doi:10.1007/978-81-322-2782-3_2.
https://doi.org/10.1007/978-81-322-2782-...
]. Because synthetic drugs and antibiotics have the serious adverse effects and the development of resistance mechanisms in pathogenic microorganisms [2020 Anand U, Jacobo-Herrera N, Altemimi A, Lakhssassi NA. Comprehensive Review on Medicinal Plants as Antimicrobial Therapeutics: Potential Avenues of Biocompatible Drug Discovery. Metabolites. 2019;9:258. doi:10.3390/metabo9110258.
https://doi.org/10.3390/metabo9110258....
].

The Lamiaceae family includes a large number of plants that are well known for their antioxidant properties [2121 Yuce E, Yildirim N, Yildirim NC, Paksoy MY, Bagci E. Essential Oil Composition, Antioxidant and Antifungal Activities of Salvia sclarea L. from Munzur Valley in Tunceli, Turkey‎. Cell Mol Biol. 2014;60(2):1-5.]. T. spicata, L. X Intermedia, S. macrantha and R. officinalis belonging to the Lamiaceae family are essential oil plants and are used as medicinal herbs. The part of T. spicata used as food is fresh shoots collected in spring and dried leaves and flower cases. The essential oil 'thyme oil' obtained by steam distillation from the dried flowers and leaves of the plant is used as a folk medicine [2222 Baytop T. Treatment Plant in Turkey with Past and Present. Istanbul: Nobel Bookstores; 1999.]. There are 39 Lavandula species, mostly of Mediterranean origin [2323 Weiss EA. Essential Oil Crops. New York: CAB International; 1997.]. Essential oils obtained from Lavandula are especially used in the production of perfumes, cosmetics and medicines [2424 Guenther E. The Essential Oils. R.E. Krieger Publication Coorparation. 1952;5:3-38.]. In addition, Lavandula oil is used as a nervous system treatment, dermatological treatment, antiseptic and antibiotic effects [2525 Kara N, Baydar H. Determination of lavender and lavandin cultivars (Lavandula sp.) containing high quality essential oil in Isparta, Turkey. Turkish J Field Crop. 2013;18(1):58-65.].

Figure 1
T. spicata

Figure 2
L. X Intermedia

The genus Satureja is representing by 16 species and 17 taxa [2626 Baser KHC, Kirimer N. Essential oils of Anatolian Lamiaceae-An update. Nat Vol Essent Oil. 2018;5:1-28.]. The essential oil obtained from the leaves of this genus is used in the treatment of some diseases such as diarrhea, wounds, gastroenteritis and upper respiratory and urinary tract infections [2727 Behravan J, Ramezani M, Kasaian J, Sabeti Z. Antimycotic Activity of the Essential Oil of Satureja Mutica Fisch & C.A. Mey from Iran. Flavour Fragr J. 2004;19:421-3. doi: 10.1002/ffj.1328.
https://doi.org/10.1002/ffj.1328...
]. R. officinalis is an economically important plant that grows naturally mainly in the Mediterranean region. Essential oil derived from rosemary is widely used in cosmetics, sweetening and preserving food products. It also has anti-inflammatory, chemo preventive, anti-cancer, anti-proliferative, antimicrobial activities [2828 Del Pilar Sánchez-Camargo A, Herrero M. Rosemary (Rosmarinus officinalis) as a functional ingredient: recent scientific evidence. Curr Opin Food Sci. 2017;14:13-9. doi: 10.1016/j.cofs.2016.12.003.
https://doi.org/10.1016/j.cofs.2016.12.0...
].

Figure 3
S. macrantha

Figure 4
R. officinalis

The aim of this study was to investigate the essential oil contents of T. spicata, L. X Intermediata, S. macrantha and R. officinalis and their antimicrobial efficacy against C. albicans, S. aureus and E. coli.

MATERIAL AND METHODS

Plant Materials

The leaves of T. spicata, L. X Intermediata, S. macrantha and R. officinalis harvested in the pre-flowering period and grown in the trial field of Republic of Turkey Ministry of Agriculture and Forestry GAP International Agricultural Research and Training Center (GAPUTAEM) were used as material.

The plants were identified by Dr. Mehmet FİDAN from Siirt University, Department of Biology. Voucher specimens (T. spicata: SUFAF 1558, L. X Intermedia: SUFAF 1559, S. macrantha: SUFAF 1560, R. officinalis: SUFAF 1561) were deposited at herbarium of Siirt University Flora and Fauna Center (SUFAF) Siirt University, Siirt, Turkey.

Extraction of the essential oil

The leaves of each plant were dried at room temperature and powdered in a laboratory mill. The essential oil extraction (mL g-1) was carried out by hydro distillation using Neo-Clevenger. Therefore, 20 grams of dry herb were weighed, and 200 mL of water was added in 1 L round bottom flask. The balloon was boiled for 2 h using an Electromantle™ (EM2000 CE, Electrothermal Engineering Ltd., UK, 500 W). Oils obtained were dried with anhydrous sodium sulphate and stored tightly closed vials at 4 °C prior to analyses. The qualitative and quantitative analyses of the essential oils were performed by Gas chromatography-mass spectrometry (GC-MS).

Analysis of essential oils

Samples were diluted with n-hexane in a 1:100 ratio for analysis. GC‐MS analysis of the essential oil was performed on a GC‐MS. GC (Agilent 7890A) was equipped with HP Innowax capillary column (60.0 mm x 0.25 mm x 0.25 μm). Helium was used as a carrier gas at a flow rate of 0.8 mL min-1. The oven temperature was kept at 60 °C for 10 min, heated at 4 °C min-1 to 220 °C at 10 min held, finally raised 240 at a rate of 1 °C min-1. Injector and transfer line temperature were 250 °C and 260 °C, respectively [2929 Ray A, Jena S, Kar B, Sahoo A, Panda PC, Nayak S, et al. Volatile metabolite profiling of ten Hedychium species by gas chromatography mass spectrometry coupled to chemometrics. Ind Crops Prod. 2018; 126,135-42. doi: 10.1016/j.indcrop.2018.10.012
https://doi.org/10.1016/j.indcrop.2018.1...
] and 1 µL of essential oil was injected, with split ratio of 40:1, to the instrument, for analysis. The total run time was 60 min. The scanning range (m z-1) 35-450 atomic mass units and electron bombardment ionization 70 eV were used for the mass detector (Agilent 5975C). Flame ionization detector (FID) temperature was 250 °C. To calculate the retention indices, satandard alkane series (C8-C40) were used. The percentage amounts of components were measured electronically from a FID peak areas, without using correction factors, and the identification of the components of the essential oils was performed by matching data from Wiley GC-MS Library and NIST Chemistry WebBook, SRD 69 [3030 National Institute of Standards and Technology, NIST Chemistry WebBook SRD 69, 2021. http://webbook.nist.gov/chemistry/
http://webbook.nist.gov/chemistry...
].

Antimicrobial activity

The antimicrobial activities of the plant essential oils were determined according to the Bauer and coauthors method [3131 Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic Susceptibility Testing by a Standardized Single Disk Method. Am J Clin Pathol.1966; 45(4): 493-496. doi:10.1093/ajcp/45.4_ts.493.
https://doi.org/10.1093/ajcp/45.4_ts.493...
]. Briefly, the disc diffusion test was carried out in sterile petri dishes of 90 mm diameter containing a suitable sterile solid media. It was used the test microorganisms (S. aureus ATCC 25923, E. coli ATCC 25922 and C. albicans ATCC 14053) providing from the culture collections of the Medical Microbiology Laboratory, Research Hospital of Dicle University in Diyarbakir, Turkey.

The isolates were separately sub-cultured in liquid growth media and incubated at 37 oC for overnight in an orbital shaker. The cultures were harvested using 5 mL of sterile 0.9% salt solution and absorbances were adjusted to a 0.5 McFarland turbidity standard (5 × 105 CFU mL-1) via spectrophotometer (Biochrom).

The bacteria of S. aureus and E. coli were inoculated on Mueller-Hinton agar (Oxoid, UK) and C. albicans was inoculated on Sabouraud dextrose agar (Oxoid, UK). 200 μL of each microbial suspension was inoculated to the solid culture medium then allowed the surface of the media to dry for 3-5 min. Sterilized filter paper (Whatman No. 1) discs (6 mm in diameter) containing various concentrations (15, 7.5, 3 and 1. 5 μL) of essential oils were placed in the centre of the medium surface. After impregnation with different doses (1.5, 3, 7 and 15 μL) of the essential oil to the sterile paper discs, they were placed on the surface of agar. The plates were incubated at room temperature for 1 h to ensure the diffusion of essential oils and then incubated at 37 °C for 24-48 h. The negative control was a disc containing 15 μL of n-hexane. Reference antibiotics of gentamicin (10 μg/disc), ciprofloxacin (10 μg/disc), clindamycin (2 μg/disc), ampicillin (10 μg/disc) and fluconazole (25 μg/disc) discs (Oxoid, UK) were used as the positive control. The antimicrobial activities of the oils were measured by a inhibition zone (mm) around the paper disc (6 mm). All experiments were performed in triplicate, and standard deviations were calculated using Microsoft Excel as the square root of the sum of the squares of the differences from the arithmetic mean of the obtained data divided by the number of elements of the data minus one. All the data were expressed as Means ± SD of triplicate determinations.

RESULTS AND DISCUSSIONS

Essential Oil Composition of the Plants

In the present study, it was identified the essential oils of four plant species using GC/MS. Essential oil contents in the aerial parts of selected medicinal and aromatic plant varieties are given in Table 1. According to the results of GC/MS analyzes, a total of 45 compounds were identified between 97.53-98.63% (Table 1). The major part of the components was monoterpenes, in all tested plant samples. Oxygenated monoterpenes (28.38-80.47%) had the highest fraction followed by monoterpene hydrocarbons (11.56-65.85%). The quantities of sesquiterpenes was quite low, according to the monoterpenes. The sesquiterpene hydrocarbons and oxygenated sesquterpenes were between 0.91-4.09% and 1.12-4.40%, respectively (Table 1).

As shown in Table 1., it was determined thirteen essential oil components and among these, carvacrol (74.26%), γ-terpinene (10.28%) and p-cymene (5.21%) were the main components of T. spicata. Gedikoğlu and coauthors [3232 Gedikoğlu M, Sökmen M, Çivit A. Evaluation of Thymus vulgaris and Thymbra spicata essential oils and plant extracts for chemical composition, antioxidant, and antimicrobial properties. Food Sci Nutr. 2019; 7: 1704-14. doi:10.1002/fsn3.1007.
https://doi.org/10.1002/fsn3.1007....
] reported that carvacrol (68.20%), γ‐terpinene (13.25%), p‐cymene (5.37%), β‐caryophyllene (2.59%), and thymol (1.19%) were major components of T. spicata. Barakat and coauthors [3333 Barakat A, Wakim LH, Apostolides NA, Srour GS, Beyrouthy ME. Variation in the essential oils of Thymbra spicata L. growing wild in Lebanon according to the date of harvest. J Essent Oil Res. 2013; 25: 506-11. doi:10.1080/10412905.2013.809321.
https://doi.org/10.1080/10412905.2013.80...
], Hancı and coauthors [3434 Hancı S, Şahin S, Yılmaz L. Isolation of volatile oil from thyme (Thymbra spicata) by steam distillation. Nahrung/Food. 2003; 47(4): 252-5. doi:10.1002/food.200390059.
https://doi.org/10.1002/food.200390059...
], Baydar and coauthors [3535 Baydar H, Sağdiç O, Özkan G, Karadogan T. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control. 2004; 15(3): 169-72. doi: 10.1016/S0956-7135(03)00028-8.
https://doi.org/10.1016/S0956-7135(03)00...
] and Markovic and coauthors [3636 Markovic T, Chatzopoulou P, Siljegovic J, Nikolic M, Glamočlıja J, Cıric A, et al. Chemical analysis and antimicrobial activities of the essential oils of Satureja thymbra L. and Thymbra spicata L. and their main components. Arch Biol Sci. 2011; 63(2): 457-464. doi:10.2298/ABS1102457M.
https://doi.org/10.2298/ABS1102457M....
] reported that carvacrol, γ-terpinene and p-cymene were the major components of the essential oils of T. Spicata and their amounts varied according to the different growth seasons.

It was determined twenty-three essential oil components in L. X Intermedia and 1,8-cineol (32.48%), linalool (24.38%), camphor (14.73%), β-caryophyllene (4.09%) and borneol (3.92 %) were the main components (Table 1). Nogueira and Romano [3737 Nogueira JMF, Romano A. Essential oils from micropropagated plants of Lavandula viridis. Phytochem Anal. 2002; 13: 4-7. doi: 10.1002/pca.609.
https://doi.org/10.1002/pca.609....
] found that the highest essential oil components of L. viridis were 1,8-cineole (18.2-25.1 %). Yilmaz [3838 Yilmaz MA. Essential Oil Composition of Lavandin (Lavandula x Intermedia) cultivated in Bismil-Turkey. ACPERPRO. 2018; 1: 1120-1125. doi:10.33793/acperpro.01.01.179.
https://doi.org/10.33793/acperpro.01.01....
] reported that linalool, linalyl acetate, eucalyptol, camphor and α-terpineol were the main components of L. Intermedia.

As seen in Table 1., it was determined twenty-two components and among these component, p-cymene (56.70%), carvacrol (10.96%), thymol (7.76%), γ-terpinene (3.68%) and borneol (3.50%) were major components in S. macrantha. Sefidkon and Jamzad [3939 Sefidkon F, Jamzad Z. Chemical composition of the essential oil of three Iranian Satureja species (S. mutica, S. macrantha and S. Intermedia). Food Chem. 2005;91:1-4.doi:10.1016/j.foodchem.2004.01.027.
https://doi.org/10.1016/j.foodchem.2004....
] reported that p-cymene (25.8%), limonene (16.3%) and thymol (8.1%) were major components of S. macrantha grown in Iran. Aghbash and coauthors [4040 Aghbash BN, Pouresmaeil M, Dehghan G, Nojadeh MS, Mobaiyen H, Maggi F. Chemical Composition, Antibacterial and Radical Scavenging Activity of Essential Oils from Satureja macrantha C.A.Mey. at Different Growth Stages. Foods. 2020;9:494. doi:10.3390/foods9040494.
https://doi.org/10.3390/foods9040494...
], also reported that p-cymene, γ-terpinene and carvacrol were the major compounds at all phenological stages.

Camphor (18.26%), α-pinene (16.81%), 1,8-cineole (14.83%), borneol (10.39%), verbenone (7.88%), camphene (6.79%), bornyl acetate (4.58%), linalool (4.26 %) and limonene (3.81%) were major components of R. officinalis (Table 1). Hussain and coauthors [4141 Hussain AI, Anwar F, Chatha SA, Jabbar A, Mahboob S, Nigam PS. Rosmarinus officinalis essential oil: antiproliferative, antioxidant and antibacterial activities. Braz J Microbiol. 2010;41:1070-8.doi:10.1590/S1517-838220100004000027.
https://doi.org/10.1590/S1517-8382201000...
] found that 1,8-cineol (38.5%), camphor (17.1%), α-pinene (12.3%), limonene (6.23%), camphene (6.00%), and linalool (5.70%) were the major constituents of R. officinalis. Dıraz Yıldırım [4242 Dıraz Yıldırım E. The Effect of Seasonal Variation on Rosmarinus officinalis (L.) Essential Oil Composition. Int J Agr Wildlife Sci (IJAWS). 2018;4(1):33-8. doi: 10.24180/ijaws.381564.
https://doi.org/10.24180/ijaws.381564....
], Sienkiewicz and coauthors [4343 Sienkiewicz M, Łysakowska M, Pastuszka M, Bienias W, Kowalczyk E. The potential of use basil and rosemary essential oils as effective antibacterial agents. Molecules. 2013;18(8):9334-51.] and Jiang and coauthors [4444 Jiang Y, Wu N, Fu YJ, Wang W, Luo M, Zhao CJ, Zu YG, Liu XL. Chemical composition and antimicrobial activity of the essential oil of Rosemary. Environ Toxicol Pharmacol. 2011;32(1):63-8.] stated that the major compounds of R. officinalis were found as α-pinene, 1.8-cineole, α-terpineol, α-pinene, camphor, isoborneol.

Table 1
Chemical composition of essential oils of T. spicata, L. X Intermedia, S. macrantha and R. officinalis (%)

Antimicrobial activity

The antimicrobial activity tests were carried out with disk diffusion method. The antibacterial activities of T. spicata, L. Intermedia, S. macrantha and R. officinalis essential oils were tested against multidrug resistant S. aureus, E. coli and C. albicans (Table 2). The antibiotics of ampicillin, gentamicin, ciprofloxacin, clindamycin and fluconazole were tested against S. aureus, E. coli and C. albicans (Table 3).

The highest antimicrobial activity of essential oil of T. spicata was 36±1.0 mm diameter zone of inhibition against C. Albicans, 26±1.52 mm diameter zone of inhibition against S. aureus and 28±1.52 mm diameter zone of inhibition against E. coli (Table 2). T. spicata displayed the potent antimicrobial activity against C. albicans (36 mm) in all doses. This activity was more powerful than flukonazol (24±1.15 mm), an antibiotic using against C. albicans. Essential oils of T. spicata had highly effective against E. coli and S. aureus. The doses of 15 μL (28±1.52 mm), 7.5 μL (26±0.57 mm) and 3 μL (24±1.52 mm) were more effective than ampicillin (20±1.0 mm) and gentamicin (22±0.57 mm) antibiotics against E. coli, but their effects were lower than ciprofloxacin (34±1.15 mm). The dose of 15 μL essential oils of T. spicata showed more powerful effect than gentamicin (22±0.28 mm) and ciprofloxacin (25±0.57 mm), but its effect was lower than clindamycin (26±1.0 mm) against S. aureus (Table 2, 3). In studies investigating the antimicrobial activity of T. spicata essential oil in various bacterial and fungal strains by disk diffusion methods; It has been determined that the essential oil of the plant has an antimicrobial effect against the tested bacteria and fungi [3535 Baydar H, Sağdiç O, Özkan G, Karadogan T. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control. 2004; 15(3): 169-72. doi: 10.1016/S0956-7135(03)00028-8.
https://doi.org/10.1016/S0956-7135(03)00...
,4545 Erturk O, Tanrikulu GI, Yavuz C, Can Z, Cakir HE. Chemical compositions, antioxidant and antimicrobial activities of the essential oil and extracts of Lamiaceae family (Ocimum basilicum and Thymbra spicata) from Turkey. Int J Second Metab. 2017; 4: 340-348. doi:10.21448/IJSM.373828.
https://doi.org/10.21448/IJSM.373828...
,4646 Akın M, Oğuz D, Saraçoglu HT. Antibacterial Activity of Essential oil from Thymbra spicata var. spicata L. and Teucrium polium (Stapf Brig.). Int J Pharm Sci Res. 2010; 1(1): 55-8.]. Bioactivity of essential oil might be attributed to a single major constituent or to the synergistic/ additive behaviours of minor components [4747 Jena S, Ray A, Sahoo A, Panda PC, Nayak S. Deeper insight into the volatile profile of essential oil of two Curcuma species and their antioxidant and antimicrobial activities. Ind Crops Prod. 2020; 155: 112830.]. In this study, the essential oils were characterised by high contents of carvacrol. Similar results having been reported in other studies, Baydar and coauthors [3535 Baydar H, Sağdiç O, Özkan G, Karadogan T. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control. 2004; 15(3): 169-72. doi: 10.1016/S0956-7135(03)00028-8.
https://doi.org/10.1016/S0956-7135(03)00...
] stated that the essential oil of T. spicata (containing mainly carvacrol 75.5%) was the inhibitory against E. coli and S. aureus. It is thought that carvacrol interacts with the cytoplasmic membrane and causes passive transport of ions across the membrane [4848 Chouhan S, Sharma K, Guleria S. Antimicrobial activity of some essential oils present status and future perspectives. Medicines. 2017;4:58.]. Carvacrol is also capable of aligning with fatty acid chains of lipid bilayers by interacting with transmembrane proteins and forming channels through the cytoplasmic membrane leading to the increase of membrane fluidity and alteration of proton motive force and cell permeability [4040 Aghbash BN, Pouresmaeil M, Dehghan G, Nojadeh MS, Mobaiyen H, Maggi F. Chemical Composition, Antibacterial and Radical Scavenging Activity of Essential Oils from Satureja macrantha C.A.Mey. at Different Growth Stages. Foods. 2020;9:494. doi:10.3390/foods9040494.
https://doi.org/10.3390/foods9040494...
]. Carvacrol is considered as one of the fast-acting essential oil compounds as it inactivates E. coli and Salmonella in about five minutes [4949 Al S, Yildirim Y. Antimicrobial activity of Thymbra spicata L. essential oil in Turkish dry fermented sausages. Ankara Univ Vet Fak Derg. 2020;67:227-33. doi:10.33988/auvfd.583325.
https://doi.org/10.33988/auvfd.583325...
]

The essential oil of S. macrantha with 38±1.25 mm diameter zone of inhibition showed highest activity against C. albicans whereas lowest inhibition zone was observed in 1.5 μL dose of essential of S. macrantha against E. coli (8 ± 0 mm). The doses of 15 μL (32±1.25 mm) and 7.5 μL (28±0.57 mm) of S. macrantha were more effective than ampicillin (20±1.0 mm) and gentamicin (22±0.57 mm), but lower than ciprofloxacin (34±1.15 mm) against E. coli. Essential oils of S. macrantha were very effective against S. aureus, in all doses. p-Cymene is hydrophobic in nature and has been reported to cause swelling of the cytoplasmic membrane and affect protein synthesis in E. coli. [5050 Aligiannis N, Kalpoutzakis E, Mitaku S. I B Chinou. Composition and antimicrobial activity of the essential oils of two Origanum species. J Agric Food Chem. 2001;49:4168-70., 5151 Bagamboula CF, Uyttendaele M, Debevere J. Inhibitory effect of thyme and basil essential oils, carvacrol, thymol, estragol, linalool and p-cymene towards Shigella sonnei and S. flexneri. Food Microbiol. 2004;21:33-42.] p-cymene and γ-terpinene are biosynthetically related to thymol and carvacrol and their presence may lead to synergistic effects in the bacterial cell [4040 Aghbash BN, Pouresmaeil M, Dehghan G, Nojadeh MS, Mobaiyen H, Maggi F. Chemical Composition, Antibacterial and Radical Scavenging Activity of Essential Oils from Satureja macrantha C.A.Mey. at Different Growth Stages. Foods. 2020;9:494. doi:10.3390/foods9040494.
https://doi.org/10.3390/foods9040494...
].

Table 2
Antimicrobial activity of different doses of essential oil of T. spicata, L. Intermedia, S. macrantha and R. officinalis

Essential oils of L. Intermedia showed slight effect against E. coli (12-7±1.0 mm) and S. aureus (13-6±1.0 mm) in all doses. These components showed potent effects against C. albicans at doses of 15 μL (30±1.8 mm) and 7.5 μL (20±1.15 mm), but moderate effects at doses of 3 μL (12±0.76 mm) and 1.5 μL (6±1.0 mm). It was reported that essential oils of L. Intermedia had moderate effects at the doses of 5, 10 and 15 μL, while they showed powerful effect at dose of 20 μL against E. coli and S. aureus [5252 Jianu C, Pop G, Gruia AT, Horhat FG. Chemical composition and antimicrobial activity of essential oils of lavender (Lavandula angustifolia) and lavandin (Lavandula x Intermedia) grown in Western Romania. Int J Agric Biol. 2013;15:772-6.]. The antibacterial activity of essential oil of Lavandula seems closely related to amount of 1,8-cineol [5353 Minooeianhaghighi MH, Sepehrian L, Shokri H. Antifungal effects of Lavandula binaludensis and Cuminum cyminum essential oils against Candida albicans strains isolated from patients with recurrent vulvovaginal candidiasis. J Mycol Med. 2017; 27(1): 65-71.]. In other study, in vitro antimicrobial activity of essential oil of lavender against S. aureus and E. coli were investigated by Predoi and coauthors [5454 Predoi D, Iconaru SL, Buton N, Badea ML, Marutescu L. Antimicrobial activity of new materials based on lavender and basil essential oils and hydroxyapatite. Nanomaterials. 2018; 8(5): 291.]. The antibacterial activity of these essential oil of lavender could be due to their ability to degrade membrane proteins and cell permeability.

Table 3
Antimicrobial activity of different antibiotics doses

Essential oils of R. officinalis showed moderate effects against E. coli and S. aureus in all doses but these components had very strong effects against C. albicans in at doses of 15 μL (30±1.0 mm) and 7.5 μL (24±0.76 mm) compared with fluconazole (24 mm). It was reported that essential oils of R. officinalis had weak or moderate antibacterial activity [5555 Teixeira B, Marques A, Ramos C, Neng NR, Nogueira JMF, Saraiva JA, Nunes ML. Chemical composition and antibacterial and antioxidant properties of commercial essential oils. Ind Crops Prod. 2013;43:587-95. doi:10.1016/j.indcrop.2012.07.069.
https://doi.org/10.1016/j.indcrop.2012.0...
]. Sienkiewicz and coauthors [4343 Sienkiewicz M, Łysakowska M, Pastuszka M, Bienias W, Kowalczyk E. The potential of use basil and rosemary essential oils as effective antibacterial agents. Molecules. 2013;18(8):9334-51.], Burt [5656 Burt S. Essential oils: their antibacterial properties and potential applications in foods--a review. Int J Food Microbiol. 2014;94(3):223-53.] Sirocchi and coauthors [5757 Sirocchi V, Caprioli G, Cecchini C, Coman MM, Cresci A, Maggi F, et al. Biogenic amines as freshness index of meat wrapped in a new active packaging system formulated with essential oils of Rosmarinus officinalis. Int J Food Sci Nutr. 2013;64(8):921-8.] and Yildirim and coauthors [5858 Yildirim N, Matpan Bekler F, Cikcikoglu Yildirim N. A. Dikici. In Vitro Antimicrobial Evaluation of Commercial Tea Extracts Against Some Pathogen Fungi And Bacteria. Dig J Nanomater Biostructures. 2010;5(4):821-7.] demonstrated the antibacterial activities of R. officinalis in their studies. Rosmarinic acid, rosmaridiphenol, carnosol, epirosmanol, carnosic acid, rosmanol and isorosmanol in rosemary are inhibitory in cells due to their interaction with the cell membrane, which causes loss of membrane functionality and structure, changes in genetic material and nutrients, changes in electron transport, leakage of cellular components, and changes in fatty acid production [5959 Fung DYC, Taylor S, Kahan J. Effect of butylated hydroxyanisole (BHA) and buthylated hydroxytoluebe (BHT) on growth and aflatoxin production of Aspergillus flavus. J. Food Saf. 1977; 1: 39-51. doi: 10.1111/j.1745-4565.1977.tb00258.x.
https://doi.org/10.1111/j.1745-4565.1977...
]. One of the main components of rosemary is α-pinene, a monoterpene. As noted by Bajpai and coauthors [6060 Bajpai VK, Kwang-Hyun Baek K, Kang SC. Control of Salmonella in foods by using essential oils: A review. Food Res. Int. 2012; 45: 722-34. doi: 10.1016/j.foodres.2011.04.052.
https://doi.org/10.1016/j.foodres.2011.0...
] and Nieto and coauthors [6161 Nieto G, Ros G, Castillo J. Antioxidant and Antimicrobial Properties of Rosemary (Rosmarinus officinalis, L.) A Review. Medicines (Basel). 2018;5(3):98. doi:10.3390/medicines5030098.
https://doi.org/10.3390/medicines5030098...
], the inhibitory effect may be associated with terpenes' ability to disorganize the cytoplasmic membrane and therefore promote lysis.

The results from the present study highlight the potential of the essential oils of T. spicata, L. X Intermedia, S. macrantha and R. officinalis as effective antimicrobials against C. albicans, E. coli and S. aureus. Comparing inhibition zones, all concentrations of T. spicata and S. macrantha and high dose of L. X Intermedia and R. officinalis were most effective on C. albicans. In addition, high doses of essential oils of all plants were effective S. aureus and E. coli, but the effect decreased as the concentration decreased. As a result, essential oils obtained from all plants used in the study had antimicrobial activity on test microorganisms.

CONCLUSION

The essential oils of T. Spicata, L. X Intermedia, S. macrantha and R. officinalis were constituted mainly by monoterpenoid (84.54% for T. Spicata, 71.59% for L. X Intermedia, 75.42% for S. macrantha and 47.95% for R. officinalis). The major compounds of the T. Spicata was carvacrol (74.26%), for L. Intermedia was 1,8-cineol (32.48%), for S. macrantha was p-cymene (56.70%) and for R. officinalis was camphor (18.26%). The current study demonstrated the antimicrobial activity of the essential oils of T. spicata, L. X Intermedia, S. macrantha and R. officinalis. The results indicated that T. spicata and S. macrantha had strong and the best antimicrobial activity against all test microorganisms. The high doses of essential oils of L.X Intermedia and R. officinalis had potent activity against C. albicans but moderate/less activity against E. coli and S. aureus.

REFERENCES

  • 1
    Bandow JE, Brötz H, Leichert LI, Labischinski H, Hecker M. Proteomic approach to understanding antibiotic action. Antimicrob Agents Chemother. 2003;47:948-55. doi:10.1128/aac.47.3.948-955.2003.
    » https://doi.org/10.1128/aac.47.3.948-955.2003
  • 2
    Cunha BA. Antibiotic side effects. Med Clin North Am. 2001;85:149-85. doi:10.1016/s0025-7125(05)70309-6.
    » https://doi.org/10.1016/s0025-7125(05)70309-6.
  • 3
    Ventola CL, The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther. 2015; 40: 277-83.
  • 4
    Warnes SL, Keevil CW. Lack of Involvement of Fenton Chemistry in Death of Methicillin-Resistant and Methicillin-Sensitive Strains of Staphylococcus aureus and Destruction of Their Genomes on Wet or Dry Copper Alloy Surfaces. Appl Environ Microbiol. 2016;82:2132-6. doi:10.1128/AEM.03861-15.
    » https://doi.org/10.1128/AEM.03861-15.
  • 5
    Golkar Z, Bagazra O, Pace DG. Bacteriophage therapy: a potential solution for the antibiotic resistance crisis. J Infect Dev Ctries. 2014; 13: 129-36. doi:10.3855/jidc.3573.
    » https://doi.org/10.3855/jidc.3573.
  • 6
    Tong SY, Davis JS, Eichenberger E, Holland TL, Jr Fowler VG. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015; 28: 603-61. doi:10.1128/CMR.00134-14.
    » https://doi.org/10.1128/CMR.00134-14
  • 7
    Minogue TD, Daligault HA, Davenport KW, Bishop-Lilly KA, Broomall SM, Bruce DC, et al. Complete genome assembly of Escherichia coli ATCC 25922, a serotype O6 reference strain. Genome Announc. 2014; 2(5): e00969-14. doi:10.1128/genomeA.00969-14.
    » https://doi.org/10.1128/genomeA.00969-14.
  • 8
    Latifah-Munirah B, Himratul-Aznita WH, Mohd Zain N. Eugenol, an essential oil of clove, causes disruption to the cell wall of Candida albicans (ATCC 14053). Front Life Sci. 2015;8:231-40. doi:10.1080/21553769.2015.1045628.
    » https://doi.org/10.1080/21553769.2015.1045628.
  • 9
    Erb M, Kliebenstein DJ. Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy. Plant Physiol. 2020;184(1):39-52. doi: 10.1104/pp.20.00433.
    » https://doi.org/10.1104/pp.20.00433
  • 10
    Wurtzel ET, Kutchan TM. Plant metabolism, the diverse chemistry set of the future. Science. 2016;353(6305):1232-6. doi:10.1126/science.aad2062.
    » https://doi.org/10.1126/science.aad2062
  • 11
    De Luca V, Salim V, Atsumi SM, Yu F. Mining the biodiversity of plants: a revolution in the making. Science. 2012;336(6089):1658-61. doi: 10.1126/science.1217410.
    » https://doi.org/10.1126/science.1217410.
  • 12
    Cox-Georgian D, Ramadoss N, Dona C, Basu C. Therapeutic and Medicinal Uses of Terpenes. J Med Plant. 2019; 333-359. doi:10.1007/978-3-030-31269-5_15.
    » https://doi.org/10.1007/978-3-030-31269-5_15
  • 13
    Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils-A review. Food Chem Toxicol. 2008;46:446-75. doi:10.1016/j.fct.2007.09.106.
    » https://doi.org/10.1016/j.fct.2007.09.106.
  • 14
    Ekren S, Yerlikaya O, Tokul HE, Akpınar A, Acu M. Chemical composition, antimicrobial activity and antioxidant capacity of some medicinal and aromatic plant extracts. Afr J Microbiol Res. 2013;7:383-88. doi:10.5897/AJMR12.1765.
    » https://doi.org/10.5897/AJMR12.1765
  • 15
    Tuzlacı E, Aymaz PE, Turkish folk medicinal plants, part IV: Gönen (Balıkesir). Fitoterapia. 2001;72:323-43. doi:10.1016/s0367-326x(00)00277-x.
    » https://doi.org/10.1016/s0367-326x(00)00277-x.
  • 16
    Ray A, Jena S, Dash B, Kar B, Halder T, Chatterjee T, et al. Chemical diversity, antioxidant and antimicrobial activities of the essential oils from Indian populations of Hedychium coronarium Koen. Ind Crops Prod. 2018;112:353-62. doi: 10.1016/j.indcrop.2017.12.033
    » https://doi.org/10.1016/j.indcrop.2017.12.033
  • 17
    Hosseinzadeh S, Jafarikukhdan A, Hosseini A, Armand R. The Application of Medicinal Plants in Traditional and Modern Medicine: A Review of Thymus vulgaris. J Clin Med. 2015;6:635-42. doi:10.4236/ijcm.2015.69084.
    » https://doi.org/10.4236/ijcm.2015.69084.
  • 18
    Tanhaeian A, Sekhavati MH, Moghaddam M. Antimicrobial activity of some plant essential oils and an antimicrobial-peptide against some clinically isolated pathogens. Chem Biol Technol Agric. 2020;7:13. doi:10.1186/s40538-020-00181-9.
    » https://doi.org/10.1186/s40538-020-00181-9.
  • 19
    Moghaddam M, Mehdizadeh L. Essential oil and antifungal therapy. In: Basak A., Chakraborty R., Mandal S. (eds) Recent Trends in Antifungal Agents and Antifungal Therapy. New Delhi: Springer; 2016. doi:10.1007/978-81-322-2782-3_2.
    » https://doi.org/10.1007/978-81-322-2782-3_2.
  • 20
    Anand U, Jacobo-Herrera N, Altemimi A, Lakhssassi NA. Comprehensive Review on Medicinal Plants as Antimicrobial Therapeutics: Potential Avenues of Biocompatible Drug Discovery. Metabolites. 2019;9:258. doi:10.3390/metabo9110258.
    » https://doi.org/10.3390/metabo9110258.
  • 21
    Yuce E, Yildirim N, Yildirim NC, Paksoy MY, Bagci E. Essential Oil Composition, Antioxidant and Antifungal Activities of Salvia sclarea L. from Munzur Valley in Tunceli, Turkey‎. Cell Mol Biol. 2014;60(2):1-5.
  • 22
    Baytop T. Treatment Plant in Turkey with Past and Present. Istanbul: Nobel Bookstores; 1999.
  • 23
    Weiss EA. Essential Oil Crops. New York: CAB International; 1997.
  • 24
    Guenther E. The Essential Oils. R.E. Krieger Publication Coorparation. 1952;5:3-38.
  • 25
    Kara N, Baydar H. Determination of lavender and lavandin cultivars (Lavandula sp.) containing high quality essential oil in Isparta, Turkey. Turkish J Field Crop. 2013;18(1):58-65.
  • 26
    Baser KHC, Kirimer N. Essential oils of Anatolian Lamiaceae-An update. Nat Vol Essent Oil. 2018;5:1-28.
  • 27
    Behravan J, Ramezani M, Kasaian J, Sabeti Z. Antimycotic Activity of the Essential Oil of Satureja Mutica Fisch & C.A. Mey from Iran. Flavour Fragr J. 2004;19:421-3. doi: 10.1002/ffj.1328.
    » https://doi.org/10.1002/ffj.1328
  • 28
    Del Pilar Sánchez-Camargo A, Herrero M. Rosemary (Rosmarinus officinalis) as a functional ingredient: recent scientific evidence. Curr Opin Food Sci. 2017;14:13-9. doi: 10.1016/j.cofs.2016.12.003.
    » https://doi.org/10.1016/j.cofs.2016.12.003
  • 29
    Ray A, Jena S, Kar B, Sahoo A, Panda PC, Nayak S, et al. Volatile metabolite profiling of ten Hedychium species by gas chromatography mass spectrometry coupled to chemometrics. Ind Crops Prod. 2018; 126,135-42. doi: 10.1016/j.indcrop.2018.10.012
    » https://doi.org/10.1016/j.indcrop.2018.10.012
  • 30
    National Institute of Standards and Technology, NIST Chemistry WebBook SRD 69, 2021. http://webbook.nist.gov/chemistry/
    » http://webbook.nist.gov/chemistry
  • 31
    Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic Susceptibility Testing by a Standardized Single Disk Method. Am J Clin Pathol.1966; 45(4): 493-496. doi:10.1093/ajcp/45.4_ts.493.
    » https://doi.org/10.1093/ajcp/45.4_ts.493
  • 32
    Gedikoğlu M, Sökmen M, Çivit A. Evaluation of Thymus vulgaris and Thymbra spicata essential oils and plant extracts for chemical composition, antioxidant, and antimicrobial properties. Food Sci Nutr. 2019; 7: 1704-14. doi:10.1002/fsn3.1007.
    » https://doi.org/10.1002/fsn3.1007.
  • 33
    Barakat A, Wakim LH, Apostolides NA, Srour GS, Beyrouthy ME. Variation in the essential oils of Thymbra spicata L. growing wild in Lebanon according to the date of harvest. J Essent Oil Res. 2013; 25: 506-11. doi:10.1080/10412905.2013.809321.
    » https://doi.org/10.1080/10412905.2013.809321
  • 34
    Hancı S, Şahin S, Yılmaz L. Isolation of volatile oil from thyme (Thymbra spicata) by steam distillation. Nahrung/Food. 2003; 47(4): 252-5. doi:10.1002/food.200390059.
    » https://doi.org/10.1002/food.200390059
  • 35
    Baydar H, Sağdiç O, Özkan G, Karadogan T. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control. 2004; 15(3): 169-72. doi: 10.1016/S0956-7135(03)00028-8.
    » https://doi.org/10.1016/S0956-7135(03)00028-8.
  • 36
    Markovic T, Chatzopoulou P, Siljegovic J, Nikolic M, Glamočlıja J, Cıric A, et al. Chemical analysis and antimicrobial activities of the essential oils of Satureja thymbra L. and Thymbra spicata L. and their main components. Arch Biol Sci. 2011; 63(2): 457-464. doi:10.2298/ABS1102457M.
    » https://doi.org/10.2298/ABS1102457M.
  • 37
    Nogueira JMF, Romano A. Essential oils from micropropagated plants of Lavandula viridis. Phytochem Anal. 2002; 13: 4-7. doi: 10.1002/pca.609.
    » https://doi.org/10.1002/pca.609.
  • 38
    Yilmaz MA. Essential Oil Composition of Lavandin (Lavandula x Intermedia) cultivated in Bismil-Turkey. ACPERPRO. 2018; 1: 1120-1125. doi:10.33793/acperpro.01.01.179.
    » https://doi.org/10.33793/acperpro.01.01.179
  • 39
    Sefidkon F, Jamzad Z. Chemical composition of the essential oil of three Iranian Satureja species (S. mutica, S. macrantha and S. Intermedia). Food Chem. 2005;91:1-4.doi:10.1016/j.foodchem.2004.01.027.
    » https://doi.org/10.1016/j.foodchem.2004.01.027
  • 40
    Aghbash BN, Pouresmaeil M, Dehghan G, Nojadeh MS, Mobaiyen H, Maggi F. Chemical Composition, Antibacterial and Radical Scavenging Activity of Essential Oils from Satureja macrantha C.A.Mey. at Different Growth Stages. Foods. 2020;9:494. doi:10.3390/foods9040494.
    » https://doi.org/10.3390/foods9040494
  • 41
    Hussain AI, Anwar F, Chatha SA, Jabbar A, Mahboob S, Nigam PS. Rosmarinus officinalis essential oil: antiproliferative, antioxidant and antibacterial activities. Braz J Microbiol. 2010;41:1070-8.doi:10.1590/S1517-838220100004000027.
    » https://doi.org/10.1590/S1517-838220100004000027
  • 42
    Dıraz Yıldırım E. The Effect of Seasonal Variation on Rosmarinus officinalis (L.) Essential Oil Composition. Int J Agr Wildlife Sci (IJAWS). 2018;4(1):33-8. doi: 10.24180/ijaws.381564.
    » https://doi.org/10.24180/ijaws.381564.
  • 43
    Sienkiewicz M, Łysakowska M, Pastuszka M, Bienias W, Kowalczyk E. The potential of use basil and rosemary essential oils as effective antibacterial agents. Molecules. 2013;18(8):9334-51.
  • 44
    Jiang Y, Wu N, Fu YJ, Wang W, Luo M, Zhao CJ, Zu YG, Liu XL. Chemical composition and antimicrobial activity of the essential oil of Rosemary. Environ Toxicol Pharmacol. 2011;32(1):63-8.
  • 45
    Erturk O, Tanrikulu GI, Yavuz C, Can Z, Cakir HE. Chemical compositions, antioxidant and antimicrobial activities of the essential oil and extracts of Lamiaceae family (Ocimum basilicum and Thymbra spicata) from Turkey. Int J Second Metab. 2017; 4: 340-348. doi:10.21448/IJSM.373828.
    » https://doi.org/10.21448/IJSM.373828
  • 46
    Akın M, Oğuz D, Saraçoglu HT. Antibacterial Activity of Essential oil from Thymbra spicata var. spicata L. and Teucrium polium (Stapf Brig.). Int J Pharm Sci Res. 2010; 1(1): 55-8.
  • 47
    Jena S, Ray A, Sahoo A, Panda PC, Nayak S. Deeper insight into the volatile profile of essential oil of two Curcuma species and their antioxidant and antimicrobial activities. Ind Crops Prod. 2020; 155: 112830.
  • 48
    Chouhan S, Sharma K, Guleria S. Antimicrobial activity of some essential oils present status and future perspectives. Medicines. 2017;4:58.
  • 49
    Al S, Yildirim Y. Antimicrobial activity of Thymbra spicata L. essential oil in Turkish dry fermented sausages. Ankara Univ Vet Fak Derg. 2020;67:227-33. doi:10.33988/auvfd.583325.
    » https://doi.org/10.33988/auvfd.583325
  • 50
    Aligiannis N, Kalpoutzakis E, Mitaku S. I B Chinou. Composition and antimicrobial activity of the essential oils of two Origanum species. J Agric Food Chem. 2001;49:4168-70.
  • 51
    Bagamboula CF, Uyttendaele M, Debevere J. Inhibitory effect of thyme and basil essential oils, carvacrol, thymol, estragol, linalool and p-cymene towards Shigella sonnei and S. flexneri. Food Microbiol. 2004;21:33-42.
  • 52
    Jianu C, Pop G, Gruia AT, Horhat FG. Chemical composition and antimicrobial activity of essential oils of lavender (Lavandula angustifolia) and lavandin (Lavandula x Intermedia) grown in Western Romania. Int J Agric Biol. 2013;15:772-6.
  • 53
    Minooeianhaghighi MH, Sepehrian L, Shokri H. Antifungal effects of Lavandula binaludensis and Cuminum cyminum essential oils against Candida albicans strains isolated from patients with recurrent vulvovaginal candidiasis. J Mycol Med. 2017; 27(1): 65-71.
  • 54
    Predoi D, Iconaru SL, Buton N, Badea ML, Marutescu L. Antimicrobial activity of new materials based on lavender and basil essential oils and hydroxyapatite. Nanomaterials. 2018; 8(5): 291.
  • 55
    Teixeira B, Marques A, Ramos C, Neng NR, Nogueira JMF, Saraiva JA, Nunes ML. Chemical composition and antibacterial and antioxidant properties of commercial essential oils. Ind Crops Prod. 2013;43:587-95. doi:10.1016/j.indcrop.2012.07.069.
    » https://doi.org/10.1016/j.indcrop.2012.07.069
  • 56
    Burt S. Essential oils: their antibacterial properties and potential applications in foods--a review. Int J Food Microbiol. 2014;94(3):223-53.
  • 57
    Sirocchi V, Caprioli G, Cecchini C, Coman MM, Cresci A, Maggi F, et al. Biogenic amines as freshness index of meat wrapped in a new active packaging system formulated with essential oils of Rosmarinus officinalis. Int J Food Sci Nutr. 2013;64(8):921-8.
  • 58
    Yildirim N, Matpan Bekler F, Cikcikoglu Yildirim N. A. Dikici. In Vitro Antimicrobial Evaluation of Commercial Tea Extracts Against Some Pathogen Fungi And Bacteria. Dig J Nanomater Biostructures. 2010;5(4):821-7.
  • 59
    Fung DYC, Taylor S, Kahan J. Effect of butylated hydroxyanisole (BHA) and buthylated hydroxytoluebe (BHT) on growth and aflatoxin production of Aspergillus flavus. J. Food Saf. 1977; 1: 39-51. doi: 10.1111/j.1745-4565.1977.tb00258.x.
    » https://doi.org/10.1111/j.1745-4565.1977.tb00258.x.
  • 60
    Bajpai VK, Kwang-Hyun Baek K, Kang SC. Control of Salmonella in foods by using essential oils: A review. Food Res. Int. 2012; 45: 722-34. doi: 10.1016/j.foodres.2011.04.052.
    » https://doi.org/10.1016/j.foodres.2011.04.052.
  • 61
    Nieto G, Ros G, Castillo J. Antioxidant and Antimicrobial Properties of Rosemary (Rosmarinus officinalis, L.) A Review. Medicines (Basel). 2018;5(3):98. doi:10.3390/medicines5030098.
    » https://doi.org/10.3390/medicines5030098

Edited by

Editor-in-Chief:

Alexandre Rasi Aoki

Associate Editor:

Jane Manfron Budel

Publication Dates

  • Publication in this collection
    21 Mar 2022
  • Date of issue
    2022

History

  • Received
    08 May 2021
  • Accepted
    02 Sept 2021
Instituto de Tecnologia do Paraná - Tecpar Rua Prof. Algacyr Munhoz Mader, 3775 - CIC, 81350-010 Curitiba PR Brazil, Tel.: +55 41 3316-3052/3054, Fax: +55 41 3346-2872 - Curitiba - PR - Brazil
E-mail: babt@tecpar.br