Extraction, Chemical Composition and <i>in vitro</i> Antibacterial Activity of the Essential Oil of <i>Lippia origanoides</i> Kunth from Northeast Brazil

Silva, Monique Ellen Torres da; Monte, Antônia Lucivânia de Sousa; Damaceno, Marlene Nunes; Braga, Renata Chastinet; Coimbra, Jane Sélia dos Reis; Ramanathan, Srinivasan; Almeida, Felipe Alves de

doi:10.1590/1678-4324-2022210480

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Article - Biological and Applied Sciences • Braz. arch. biol. technol. 65 • 2022 • https://doi.org/10.1590/1678-4324-2022210480 copy

Extraction, Chemical Composition and in vitro Antibacterial Activity of the Essential Oil of Lippia origanoides Kunth from Northeast Brazil

Authorship SCIMAGO INSTITUTIONS RANKINGS

HIGHLIGHTS

Thymol was identified as the main metabolite in the EOLO.
EOLO has antibacterial activity against Gram-negative and Gram-positive bacterial pathogens.
The antibacterial effect of EOLO may be associated with the presence of thymol.

Abstract

Lippia origanoides Kunth has among its synonyms Lippia sidoides Cham. and is popularly known as ‘alecrim-pimenta’ or ‘rosemary pepper’. Essential oil of L. origanoides (EOLO) has been previously reported for several biological activities without significant acute toxicity, even at higher doses. In this study, essential oil (EO) was extracted from dried leaves, inflorescences, and branches of L. origanoides from Limoeiro do Norte, Ceará, Brazil by hydrodistillation at 3.63% (w/w) yield. Posteriorly, the presence of chemical compounds in the EOLO was identified by gas chromatography coupled to mass spectrometry (GC-MS). The analysis allowed to identify the thymol as the main metabolite (83.53%), followed by p-cymene (5.92%), caryophyllene (4.31%), γ-terpinene (3.27%), thymol methyl ether (1.18%), β-myrcene (1.00%), and α-terpinene (0.79%). The minimal inhibitory concentration (MIC) of EOLO was assessed against Gram-negative and Gram-positive bacterial pathogens such as Enterobacter aerogenes, Klebsiella pneumoniae, Pseudomonas aeruginosa, Salmonella enterica serovar Typhimurium, and Staphylococcus aureus. At 10 µL/mL concentration, the EOLO exhibited antibacterial activity against all the tested bacterial pathogens, and this concentration was considered as the MIC. The minimum bactericidal concentration (MBC) of EOLO was assessed at the MIC concentration, which inhibited the complete growth of all tested bacterial pathogens after 3 h. Therefore, concentrations less than 10 µL/mL were set as MBC. Thus, our findings suggest that the EOLO can be used as a promising antibacterial agent in the industries.

Keywords:
Gram-negative bacterium; Gram-positive bacterium; monoterpene; pathogen; thymol.

GRAPHICAL ABSTRACT

*Peak^ * Peaks identified in the chromatogram in Figure 1; RT = Retention time; [M-H] = Molecular ion.**	RT (min)	[M-H] *(m/z)*	Percentage of similarity (%)	Chemical compound	Relative percentage (%)
6	20.805	135.15	95	thymol	83.53	Aromatic monoterpene
3	10.715	119.15	96	p-cymene	5.92	Aromatic monoterpene
7	24.860	93.10	96	caryophyllene	4.31	Sesquiterpene
4	11.953	93.10	97	γ-terpinene	3.27	Monoterpene
5	18.410	149.15	97	thymol methyl ether	1.18	Aromatic monoterpene
1	9.548	41.10	96	β-myrcene	1.00	Acyclic monoterpene
2	10.416	121.15	94	α-terpinene	0.79	Monoterpene
				TOTAL	100.00

Concentration of EOLO (µL/mL)	Mean of the diameter of the inhibition zone + standard deviation (mm)
Concentration of EOLO (µL/mL)	*E. aerogenes*	*K. pneumoniae*	*P. aeruginosa*	Salmonella Typhimurium	*S. aureus*
0.00	0.0 + 0.0^e	0.0 + 0.0^f	0.0 + 0.0^f	0.0 + 0.0^f	0.0 + 0.0^e
1.25	0.0 + 0.0^e	0.0 + 0.0^f	0.0 + 0.0^f	0.0 + 0.0^f	0.0 + 0.0^e
2.50	7.2 + 0.8^d	6.7 + 1.0^e	8.2 + 0.8^e	7.9 + 0.8^e	7.3 + 0.3^d
5.00	8.5 + 0.5^d	9.1 + 0.5^d	9.7 + 0.3^de	8.2 + 0.8^e	8.6 + 0.4^cd
10.00	11.7 + 0.3 ^c	10.6 + 0.4 ^d	10.3 + 0.7 ^d	11.8 + 0.5 ^de	10.2 + 0.8 ^cd
20.00	13.0 + 0.5^bc	14.2 + 0.5^c	14.1 + 0.2^c	14.3 + 1.2^cd	15.4 + 0.4^bc
40.00	14.5 + 0.7^b	16.3 + 0.5^b	15.3 + 0.6^bc	16.4 + 1.1^bc	18.4 + 1.1^b
80.00	15.0 + 1.0^b	17.0 + 2.1^b	16.0 + 0.7^b	19.8 + 2.5^b	22.2 + 2.6^ab
160.00	20.6 + 1.5^a	19.4 + 0.5^a	21.4 + 1.7^a	24.8 + 2.9^a	26.6 + 6.2^a

Bacteria	Inhibition zone diameter (mm)				MIC	MBC	MID	Main metabolite	Reference
	10 µL	20 µL	10 µL/mL	Undefined				Main metabolite
Gram-negative
Aeromonas hydrophila ATCC 7966	-	-	-	-	1.25 mg/mL	1.25 mg/mL	-	thymol	Majolo et al. [⁴⁰40 Majolo C, Rocha SIB, Chagas EC, Chaves FCM, Bizzo HR. Chemical composition of Lippia spp. essential oil and antimicrobial activity against Aeromonas hydrophila. Aquac Res. 2016;48(5):2380-7.]
Aeromonas hydrophila ATCC 7966	-	-	-	-	1.25 mg/mL	1.25 mg/mL	-	-	Majolo et al. [³⁹39 Majolo C, Silva AMS, Monteiro PC, Brandão FR, Chaves FCM, Chagas EC. Antibacterial activity of essential oil and extracts of Lippia sidoides and thymol against Aeromonas hydrophila. Biota Amaz. 2020;10(2):46-9.]
Enterobacter aerogenes ATCC 13048	-	-	-	-	2.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Enterobacter aerogenes ATCC 13048	-	-	11.7	-	-	< 10.0 µL/mL	-	thymol	This study
Enterobacter cloacae	-	-	-	-	0.256 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Enterobacter cloacae HMA/FT502	-	-	-	-	2.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Escherichia coli	13.5	23.0	-	-	< 50.0 µL/mL	-	-	thymol	Bertini et al. [¹⁷17 Bertini LM, Pereira AF, Oliveira CLL, Menezes EA, Morais SM, Cunha FA, et al. Perfil de sensibilidade de bactérias frente a óleos essenciais de algumas plantas do Nordeste do Brasil. Informa. 2005;17(3/4):80-3.]
Escherichia coli	-	-	-	-	0.00125 mg/mL	-	-	carvacrol	Pereira et al. [⁵⁸58 Pereira AMS, Franca SC, Fachin AL, Bertoni BW, Pina ES, Coppede JS. Phytotherapic pharmaceutical combination of Lippia salviifolia and Lippia sidoides, phytotherapic pharmaceutical composition, process for preparing a phytotherapic pharmaceutical composition and veterinary uses. United States Pat. 2016;2(12).]
Escherichia coli	-	-	-	-	0.512 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Escherichia coli ATCC 11229	-	-	-	-	2.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Escherichia coli ATCC 25753	-	-	-	-	< 3.0 µL/mL	-	-	-	Castro et al. [²³23 Castro CE, Ribeiro JM, Diniz TT, Almeida AC, Ferreira LC, Martins ER, et al. Antimicrobial activity of Lippia sidoides Cham. (Verbenaceae) essential oil against Staphylococcus aureus and Escherichia coli. Ver Bras Plantas Med. 2011;13(3):293-7.]
Escherichia coli ATCC 25922	-	-	-	5.0	< 0.015 mg/mL	-	-	thymol	Linden et al. [³⁸38 Linden L, Farias I, Santos A, Silveira K, Sampaio F. Antimicrobial evaluation of sutures containing Lippia sidoides Cham. essencial oil. MOL2NET. 2016;2(14).]
Pool of 30 samples of Escherichia coli isolated of homemade Minas cheese	-	23.0	-	-	13.0 µL/mL	25.0 µL/mL	-	-	Castro et al. [²³23 Castro CE, Ribeiro JM, Diniz TT, Almeida AC, Ferreira LC, Martins ER, et al. Antimicrobial activity of Lippia sidoides Cham. (Verbenaceae) essential oil against Staphylococcus aureus and Escherichia coli. Ver Bras Plantas Med. 2011;13(3):293-7.]
Klebsiella pneumoniae	-	-	-	-	0.256 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Klebsiella pneumoniae ATCC 10031	-	-	10.6	-	-	< 10.0 µL/mL	-	thymol	This study
Providencia rettgeri	-	-	-	-	0.256 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Pseudomonas aeruginosa	0.0	0.0	-	-	-	-	-	thymol	Bertini et al. [¹⁷17 Bertini LM, Pereira AF, Oliveira CLL, Menezes EA, Morais SM, Cunha FA, et al. Perfil de sensibilidade de bactérias frente a óleos essenciais de algumas plantas do Nordeste do Brasil. Informa. 2005;17(3/4):80-3.]
Pseudomonas aeruginosa	-	-	-	-	1.25 mg/mL	1.25 mg/mL	-	-	Melo et al. [⁴³43 Melo CBF, Barreto JO, Regis RR, Silva FJA, Silva-Lovato CH, Oliveira VC, et al. Desenvolvimento de um produto à base de óleo essencial de Lippia sidoides como auxiliar para prevenção e tratamento da estomatite protética. J Heal Sci. 2017;19(5):188.]
Pseudomonas aeruginosa	-	-	-	-	0.00037 mg/mL	-	-	carvacrol	Pereira et al. [⁵⁸58 Pereira AMS, Franca SC, Fachin AL, Bertoni BW, Pina ES, Coppede JS. Phytotherapic pharmaceutical combination of Lippia salviifolia and Lippia sidoides, phytotherapic pharmaceutical composition, process for preparing a phytotherapic pharmaceutical composition and veterinary uses. United States Pat. 2016;2(12).]
Pseudomonas aeruginosa	-	-	-	-	0.512 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Pseudomonas aeruginosa ATCC 25619	-	-	10.3	-	-	< 10.0 µL/mL	-	thymol	This study
Pseudomonas aeruginosa ATCC 9027	-	-	-	-	2.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Pseudomonas aeruginosa ATCC15442	-	-	-	-	-	-	< 0.001 mg/mL air	thymol	Veras et al. [⁷³73 Veras HNH, Araruna MKA, Costa JGM, Coutinho HDM, Kerntopf MR, Botelho MA, et al. Topical antiinflammatory activity of essential oil of Lippia sidoides Cham: possible mechanism of action. Phyther Res. 2012;27(2):179-85.]
Pseudomonas aeruginosa SPM1	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Pseudomonas syringae pv.	4.7	5.9	-	-	-	-	-	carvacrol	Guimarães et al. [³⁴34 Guimarães LDLG, Cardoso MG, Souza RM, Zacaroni AB, Santos GR. Essential oil of Lippia sidoides native to Minas Gerais: composition, secretory structures and antibacterial activity. Rev Cienc Agron. 2014;45(2):267-75.]
Salmonella enterica serovar Enteritidis ATCC 13076	34.7	-	-	-	-	-	-	-	Ambrosio et al. [¹²12 Ambrosio CMS, Alencar SM, Sousa RLM, Moreno AM, Gloria EM. Antimicrobial activity of several essential oils on pathogenic and beneficial bacteria. Ind Crops Prod. 2017;97:128-36.]
Salmonella enterica serovar Typhi ATCC 19430	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Salmonella enterica serovar Typhimurium ATCC 14028	-	-	11.8	-	-	< 10.0 µL/mL	-	thymol	This study
Serratia marcenscens ATCC 14756	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Xanthomonas campestris pv. vesicatoria	3.9	4.9	-	-	-	-	-	carvacrol	Guimarães et al. [³⁴34 Guimarães LDLG, Cardoso MG, Souza RM, Zacaroni AB, Santos GR. Essential oil of Lippia sidoides native to Minas Gerais: composition, secretory structures and antibacterial activity. Rev Cienc Agron. 2014;45(2):267-75.]
Cont. Table 3
Gram-positive
Bacillus cereus ATCC 14579	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Bacillus subtilis ATCC 6633	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Clavibacter michiganensis subsp. Michiganensis	3.0	5.6	-	-	-	-	-	carvacrol	Guimarães et al. [³⁴34 Guimarães LDLG, Cardoso MG, Souza RM, Zacaroni AB, Santos GR. Essential oil of Lippia sidoides native to Minas Gerais: composition, secretory structures and antibacterial activity. Rev Cienc Agron. 2014;45(2):267-75.]
Enterococcus faecalis	-	-	-	-	0.512 mg/mL	-	-	thymol	Veras et al [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Lactobacillus plantarum ATCC 8014	37.8	-	-	-	-	-	-	-	Ambrosio et al. [¹²12 Ambrosio CMS, Alencar SM, Sousa RLM, Moreno AM, Gloria EM. Antimicrobial activity of several essential oils on pathogenic and beneficial bacteria. Ind Crops Prod. 2017;97:128-36.]
Listeria monocytogenes L2	-	-	-	-	-	1.0 µL/mL	-	thymol	Vázquez-Sánchez et al. [⁷⁰70 Vázquez-Sánchez D, Galvão JA, Ambrosio CMS, Gloria EM, Oetterer M. Single and binary applications of essential oils effectively control Listeria monocytogenes biofilms. Ind Crops Prod. 2018;121:452-60.]
Listeria monocytogenes L8	-	-	-	-	-	5.0 µL/mL	-	thymol	Vázquez-Sánchez et al. [⁷⁰70 Vázquez-Sánchez D, Galvão JA, Ambrosio CMS, Gloria EM, Oetterer M. Single and binary applications of essential oils effectively control Listeria monocytogenes biofilms. Ind Crops Prod. 2018;121:452-60.]
Micrococcus luteus ATCC 9341	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Micrococcus roseus ATCC 1740	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Staphylococcus aureus	28.0	33.5	-	-	< 50.0 µL/mL	-	-	thymol	Bertini et al. [¹⁷17 Bertini LM, Pereira AF, Oliveira CLL, Menezes EA, Morais SM, Cunha FA, et al. Perfil de sensibilidade de bactérias frente a óleos essenciais de algumas plantas do Nordeste do Brasil. Informa. 2005;17(3/4):80-3.]
Staphylococcus aureus	-	-	-	-	0.039 mg/mL	0.039 mg/mL	-	-	Melo et al. [⁴³43 Melo CBF, Barreto JO, Regis RR, Silva FJA, Silva-Lovato CH, Oliveira VC, et al. Desenvolvimento de um produto à base de óleo essencial de Lippia sidoides como auxiliar para prevenção e tratamento da estomatite protética. J Heal Sci. 2017;19(5):188.]
Staphylococcus aureus	-	-	-	-	0.00063 mg/mL	-	-	carvacrol	Pereira et al. [⁵⁸58 Pereira AMS, Franca SC, Fachin AL, Bertoni BW, Pina ES, Coppede JS. Phytotherapic pharmaceutical combination of Lippia salviifolia and Lippia sidoides, phytotherapic pharmaceutical composition, process for preparing a phytotherapic pharmaceutical composition and veterinary uses. United States Pat. 2016;2(12).]
Staphylococcus aureus	-	-	-	-	0.128 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Staphylococcus aureus ATCC 15656	-	-	-	20.0	< 0.015 mg/mL	-	-	thymol	Linden et al. [³⁸38 Linden L, Farias I, Santos A, Silveira K, Sampaio F. Antimicrobial evaluation of sutures containing Lippia sidoides Cham. essencial oil. MOL2NET. 2016;2(14).]
Staphylococcus aureus ATCC 25923	-	74.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus ATCC 25923	-	-	-	-	0.5 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Staphylococcus aureus ATCC 25923	-	-	10.2	-	-	< 10.0 µL/mL	-	thymol	This study
Staphylococcus aureus ATCC 29213	-	-	-	-	< 3.0 µL/mL	-	-	-	Castro et al. [²³23 Castro CE, Ribeiro JM, Diniz TT, Almeida AC, Ferreira LC, Martins ER, et al. Antimicrobial activity of Lippia sidoides Cham. (Verbenaceae) essential oil against Staphylococcus aureus and Escherichia coli. Ver Bras Plantas Med. 2011;13(3):293-7.]
Staphylococcus aureus ATCC 6538	-	-	-	-	0.5 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Staphylococcus aureus ATCC12624	-	-	-	-	-	-	0.000125 mg/mL air	thymol	Veras et al. [⁷³73 Veras HNH, Araruna MKA, Costa JGM, Coutinho HDM, Kerntopf MR, Botelho MA, et al. Topical antiinflammatory activity of essential oil of Lippia sidoides Cham: possible mechanism of action. Phyther Res. 2012;27(2):179-85.]
Staphylococcus aureus BH1	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH10	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH13	-	15.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH14	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH15	-	15.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH17	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH18	-	16.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH19	-	21.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH2	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH20	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH5	-	18.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus BH8	-	15.0	-	-	0.4 µL/mL	-	-	-	Oliveira et al. [⁵¹51 Oliveira FP, Lima EDO, Souza EL, Helena B, Santos C, Barreto HM. Effectiveness of Lippia sidoides Cham. (Verbenaceae) essential oil in inhibiting the growth of Staphylococcus aureus strains isolated from clinical material. Brazilian J Pharmacogn. 2006;16(4):510-6.]
Staphylococcus aureus S8	-	-	-	-	-	0.25 µL/mL	-	thymol	Vázquez-Sánchez et al. [⁷¹71 Vázquez-Sánchez D, Galvão JA, Mazine MR, Gloria EM, Oetterer M. Control of Staphylococcus aureus biofilms by the application of single and combined treatments based in plant essential oils. Int J Food Microbiol. 2018;286:128-38.]
Staphylococcus aureus S10	-	-	-	-	-	0.5 µL/mL	-	thymol	Vázquez-Sánchez et al. [⁷¹71 Vázquez-Sánchez D, Galvão JA, Mazine MR, Gloria EM, Oetterer M. Control of Staphylococcus aureus biofilms by the application of single and combined treatments based in plant essential oils. Int J Food Microbiol. 2018;286:128-38.]
Staphylococcus aureus S102	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S14	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S16	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S26	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S27	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S46	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S81	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S82	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S83	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Staphylococcus aureus S86	-	29.0 - 60.4	-	-	-	-	-	thymol	Costa et al. [²⁴24 Costa RA, Cavalcante TTA, Melo CTV, Barroso DLA, Machado MH, Carvalho MG, et al. Antioxidant and antibacterial activities of essential oil of Lippia sidoides against drug-resistant Staphylococcus aureus from food. African J Biotechnol. 2018;17(8):232-8.]
Pool of 30 samples of Staphylococcus aureus isolated of homemade Minas cheese	-	26.0	-	-	13.0 µL/mL	25.0 µL/mL	-	-	Castro et al. [²³23 Castro CE, Ribeiro JM, Diniz TT, Almeida AC, Ferreira LC, Martins ER, et al. Antimicrobial activity of Lippia sidoides Cham. (Verbenaceae) essential oil against Staphylococcus aureus and Escherichia coli. Ver Bras Plantas Med. 2011;13(3):293-7.]
Staphylococcus epidermidis	-	-	-	-	0.00063 mg/mL	-	-	carvacrol	Pereira et al. [⁵⁸58 Pereira AMS, Franca SC, Fachin AL, Bertoni BW, Pina ES, Coppede JS. Phytotherapic pharmaceutical combination of Lippia salviifolia and Lippia sidoides, phytotherapic pharmaceutical composition, process for preparing a phytotherapic pharmaceutical composition and veterinary uses. United States Pat. 2016;2(12).]
Staphylococcus epidermidis ATCC 12229	-	-	-	-	1.0 mg/mL	-	-	isoborneol	Morais et al. [⁴⁷47 Morais SR, Oliveira TLS, Oliveira LP, Tresvenzol L, Conceição E, Rezende M, et al. Essential oil composition, antimicrobial and pharmacological activities of Lippia sidoides Cham. (Verbenaceae) from São Gonçalo do Abaeté, Minas Gerais, Brazil. Pharmacogn Mag. 2016;12(48):262-70.]
Streptococcus agalactiae KJ561060	-	-	-	-	0.3125 mg/mL	0.4167 mg/mL	-	thymol	Majolo et al. [⁴¹41 Majolo C, Pilarski F, Chaves FCM, Bizzo HR, Chagas EC. Antimicrobial activity of some essential oils against Streptococcus agalactiae, an important pathogen for fish farming in Brazil. J Essent Oil Res. 2018;30(5):388-97.]
Streptococcus mitis	10.0	-	-	-	10.0 mg/mL	40.0 mg/mL	-	thymol	Botelho et al. [¹⁹19 Botelho MA, Nogueira NAP, Bastos GM, Fonseca SGC, Lemos TLG, Matos FJA, et al. Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Brazilian J Med Biol Res. 2007;40(3):349-56.]
Streptococcus mutans	-	-	-	-	0.256 mg/mL	-	-	thymol	Veras et al. [⁷⁴74 Veras HNH, Rodrigues FFG, Botelho MA, Menezes IRA, Coutinho HDM, Costa JGM. Enhancement of aminoglycosides and β-lactams antibiotic activity by essential oil of Lippia sidoides Cham. and the thymol. Arab J Chem. 2013;10:S2790-5.]
Streptococcus mutans ss-980	18.7	-	-	-	5.0 mg/mL	20.00 mg/mL	-	thymol	Botelho et al. [¹⁹19 Botelho MA, Nogueira NAP, Bastos GM, Fonseca SGC, Lemos TLG, Matos FJA, et al. Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Brazilian J Med Biol Res. 2007;40(3):349-56.]
Streptococcus salivarius	8.5	-	-	-	10.0 mg/mL	40.0 mg/mL	-	thymol	Botelho et al. [¹⁹19 Botelho MA, Nogueira NAP, Bastos GM, Fonseca SGC, Lemos TLG, Matos FJA, et al. Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Brazilian J Med Biol Res. 2007;40(3):349-56.]
Streptococcus sanguis	12.0	-	-	-	10.0 mg/mL	40.0 mg/mL	-	thymol	Botelho et al. [¹⁹19 Botelho MA, Nogueira NAP, Bastos GM, Fonseca SGC, Lemos TLG, Matos FJA, et al. Antimicrobial activity of the essential oil from Lippia sidoides, carvacrol and thymol against oral pathogens. Brazilian J Med Biol Res. 2007;40(3):349-56.]

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[1] *Correspondence: monique.ellen@ufjf.edu.br (M.E.T.S).