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Abanico veterinario

Print version ISSN 2007-428X

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Abanico vet  vol. 16
https://doi.org/10.21929/abavet2025.2

Revisión de literatura

Lippia graveolens and its activity against bacteria associated with bovine mastitis: Literature review

Article Indicators
Vargas-Monter, Jorge12
http://orcid.org/0000-0001-9845-2598
Rivero-Pérez, Nallely1*
http://orcid.org/0000-0002-6154-9983
Valladares-Carranza, Benjamín3
http://orcid.org/0000-0003-0306-3560
Ojeda-Ramírez, Deyanira1
http://orcid.org/0000-0003-4649-2699
Noguez-Estrada, Juan12
http://orcid.org/0000-0002-0493-8843
Zaragoza-Bastida, Adrian**1
http://orcid.org/0000-0002-8537-5025
Author affiliation
×
  • 1Universidad Autónoma del Estado de Hidalgo, Instituto de Ciencias Agropecuarias, Área Académica de Medicina Veterinaria y Zootecnia. Hidalgo, México.
  • 2Universidad Politécnica de Francisco I. Madero, Ingeniería en Producción Animal, Hidalgo, México.
  • 3Universidad Autónoma del Estado de México. Facultad de Medicina Veterinaria y Zootecnia. Estado de México. México.
Author notes
*Autor responsable: Rivero-Pérez Nallely. **Autor de correspondencia: Zaragoza-Bastida Adrián. Rancho Universitario Av. Universidad km. 1, Ex Hacienda de Aquetzalpa, Apartado Postal No. 32, Tulancingo de Bravo, Hidalgo, México. E-mail: va472618@uaeh.edu.mx, rivero@uaeh.edu.mx, bvalladaresc@uaemex.mx, dojeda@uaeh.edu.mx, jnoguez@upfim.edu.mx, adrian_zaragoza@uaeh.edu.mx
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ABSTRACT

Bovine mastitis is an infectious disease of the mammary gland caused by the invasion of pathogens, among them the bacterial etiology is one of the most important and the treatment of these infections has currently been complicated by the resistance generated by Gram positive bacteria and Gram negative to conventional antimicrobials. The objective of this research was to carry out a bibliographic review of Lippia graveolens and its activity against bacteria associated with bovine mastitis. Scientific reports on the phytochemical composition of wild oregano (L. graveolens) and the antibacterial activity against bacteria associated with bovine mastitis were consulted. The metabolites identified in L. graveolens with the highest reported antibacterial activity were naringenin, quercetin, luteolin as well as the terpenes thymol and carvacrol. L. graveolens contains secondary metabolites with reports of antibacterial activity, so it could be an alternative treatment against bacteria associated with bovine mastitis.

Keywords: :
Lippia graveolens, secondary metabolites, antibacterial activity, mastitis

INTRODUCTION

Bovine mastitis is inflammation of the mammary gland caused by the invasion of pathogenic microorganisms that destroy milk-secreting tissues. More than 100 species associated with bovine mastitis have been reported in bacterial etiology (Sharun et al., 2021; Morales et al., 2023). The most common bacteria in cases of mastitis are: Staphylococcus aureus, Streptococcus agalactiae, Streptococcus uberis, Streptococcus dysgalactiae, Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and coagulase-negative Staphylococcus (Pascu et al., 2022; Morales et al., 2023).

Mastitis is treated with chemical antimicrobials; however, their continuous and excessive use has led to the development of antimicrobial resistance, creating a global problem in animal and human health due to the interaction of bacteria from these two populations and the transfer of intergenic resistance (Galarza et al., 2021; Wang et al., 2021; Li et al., 2023). Bacterial resistance leads to increased treatment costs and premature culling of animals, which has prompted the scientific community to search for new alternatives for the treatment of bovine mastitis (Kovačević et al., 2022; Morales et al., 2023).

Within the flora diversity, Mexican oregano (Lippia graveolens) is a plant of interest due to its phytochemical composition. This wild shrub has been used for culinary purposes and in traditional medicine to treat respiratory and digestive diseases, inflammation, headaches, and rheumatism (Bautista et al., 2021). There are reports that demonstrate the antibacterial activity of L. graveolens using different methods of secondary metabolite extraction and concentrations at which antibacterial activity has been determined against various bacterial genera, including those associated with bovine mastitis (Bautista et al., 2021;Cortés et al., 2021; Kovačević et al., 2022; Garcia et al., 2022). The objective of this research was to conduct a literature review of L. graveolens and its activity against bacteria associated with bovine mastitis.

METHODOLOGY

To conduct this review, an exhaustive search was carried out in the following databases: PubMed, ScienceDirect, and Google Scholar, for studies published up to 2024. The following headings and keywords were used: L. graveolens, plant extracts, bovine mastitis, and antibacterial activity. Full-text documents were reviewed, and duplicate documents were removed. The exclusion criteria were inadequate methods and lack of access to the full text.

PLANT BOTANY

L. graveolens is a perennial shrub that grows to a height of two meters. It has exfoliating bark branches with opposite petiolate leaves that are oval-lanceolate in shape, with a rough, scabrous upper surface, glandular striae, densely hairy underside, obtuse apex, and variously crenate margin (Ocampo et al., 2009). Flowering occurs during the rainy season (Bueno, 2014). Its inflorescence is indeterminate, subglobose spike-like, with white, zygomorphic corollas and small, 4 mm hermaphroditic flowers, in quantities of 2 to 20 flowers. It has small indehiscent capsule fruits with seeds without endosperm (Figure 1) (Ocampo et al., 2009).

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Lippia graveolens in Orizabita, Ixmiquilpan, Hidalgo, Mexico
Figure 1
Lippia graveolens in Orizabita, Ixmiquilpan, Hidalgo, Mexico

The plant is wild and is found in the hills of temperate, arid, and semi-arid areas of Mexico. It adapts to altitudes between 1 400 and 2 300 meters, in stony soils with a sandy loam texture. It prefers a dry and semi-dry climate, with temperatures ranging from 20 to 24 °C and precipitation between 182 and 267 mm (Figure 1) (Martínez et al., 2014). It is an aromatic plant used in cooking and herbal medicine for the treatment of digestive disorders. In Chihuahua, Durango, Tamaulipas, Coahuila, Jalisco, Zacatecas, Querétaro, Hidalgo, and Baja California, its foliage is collected for sale in local markets (Bueno, 2014).

COMPOSICIÓN FITOQUÍMICA PHYTOCHEMICAL COMPOSITION

The phytochemical characterization of L. graveolens from aqueous extracts, hydroalcoholic extracts, and essential oils shows differences in its phytochemical composition (González et al., 2017; Bernal et al., 2022). Extraction has been carried out using conventional techniques such as maceration with alcohols and water in different proportions, and by current technologies such as ultrasound-assisted extraction using eutectic solvents and supercritical fluid extraction using carbon dioxide as a solvent (Bernal et al., 2023). The presence of metabolites differs depending on the extraction methods, as shown in Table 1, with phenolic compounds and monoterpenes standing out (González et al., 2017).

Table 1
Phytochemical compounds identified in plant extracts of Lippia graveolens
Extract Extraction method Solvent Compounds Reference
Aqueous Ultrasound and supercritical fluid using CO2 Choline chlorideethylene glycol, choline chlorideglycerol, and choline chloridelactic acid. Caffeic, protocatechuic, and rosmarinic acids. Quercetin, luteolin, naringenin, eriodictyol, carvacrol Garcia et al. (2022)) González et al. (2017) Soto et al. (2019) Bernal et al.(2023)
Hexane Maceration Hexane Thymol, m-cymene-8-ol, methyl salicylate, carvacrol, and linalool. González et al.(2017)
Ethyl acetate Maceration Ethyl acetate p-cymene, thymol, cirsimaritin, naringenin
Ethanolic Maceration Ethanol Supercritical CO2 modified with ethanol after steam distillation Naringenin, taxifolin, eriodictyol, caffeic acid, luteolin, coumaric acid, quercetin 3 O-glucoside, 2-hydroxybenzoic acid, apigenin, quercetin, phloridzin, acacetin, sakuranetin, cirsimaritin, chrysoeriol. Arias et al. (2023) Bernal et al. (2023) González et al. (2017)
Hydroalcoholic Maceration Methanol and Chloroform Loganin, secologanin, secoxiloganin, dimethylsecologanoside, loganic acid, 8-epi-loganic acid, carioptosidic acid and its 6-O-p-coumaroyl and 6-O-caffeoyl derivatives, naringenin, pinocembrin, lapachenol and icterogenin, luteolin-7-O-glucoside, apigenin 7-O-glucoside, phloridzin, taxifolin, eriodictyol, scutellarein, luteolin, quercetin, and galangin. Cortes et al. (2021) Picos et al. (2021) Leyva et al. (2016) Rastrelli et al. (1998) Lin et al. (2007)
Essential oil Hydro- distillation Carvacrol, α-terpinyl acetate, m-cymene, thymol, β-pinene, and α-thujene, linalool, humulene Sesquiterpene: isocaryophyllene, γ-terpinene. Hernández et al.(2009) Martínez et al. (2014) Nonato et al. (2022) Castillo et al. (2023)

In L. graveolens, the most abundant flavonoids are: quercetin, luteolin, naringenin, eriodictyol, luteolin, hesperidin, and phloridzin (Bernal et al., 2023). The metabolites naringenin, quercetin, phloridzin, and cirsimaritin are chemical markers of the Lippia genus (Bernal et al., 2022). The best flavonoid profile is obtained from methanolic leaf extract, in which three major iridoids have been found: carioptosidic acid with two derivatives: 6'-O-p-coumaroyl and 6'-O-caffeoyl, and seven minor iridoids: loganin, secologanin, secoxiloganin, dimethyl, secologanoside, loganic acid, 8-epi-loganic acid, and carioptoside (Rastrelli et al., 1998; Lin et al., 2007). Monoterpenes are the main components of essential oils of the Lippia genus (Cortés et al., 2021; Bernal et al., 2023). In water-, hexane-, and methyl acetate-based extracts and in hydrodistillation processes for obtaining essential oil, the presence of the following monoterpenes has been reported: thymol, carvacrol, limonene, b-caryophyllene, r-cymene, camphor, linalool, and a-pinene, which may vary according to the chemotype and extraction method (Calvo et al., 2014; Garcia et al., 2022). In this regard, Vernin (2001) reported that the essential oil of L. graveolens from Mexico and Central America has concentrations of 35 to 71% carvacrol and 5 to 7% thymol. Calvo et al. (2014) reported the presence of more than 70 compounds in its essential oils and identified three chemotypes of the plant: two phenolic (carvacrol and thymol) and one non-phenolic chemotype of oxygenated sesquiterpenes (βcaryophyllene, α-humulene, and caryophyllene oxide). Plant's habitat determines the oil composition, with the highest concentration of carvacrol obtained from plants growing in a semi-arid climate with thin, rocky soils (Torres et al., 2022). However, there are reports of young plants growing in less arid conditions with deep soils, which provide a higher presence of thymol, and those growing in sub-humid climates have a higher amount of oxygenated sesquiterpenes (Llamas et al., 2022).

METABOLITES AND ANTIBACTERIAL ACTIVITY

Terpenes

Carvacrol and thymol are most prevalent in L. graveolens (Calamaco et al., 2023), and their concentration is affected by edaphic and climatic factors in the plant's habitat (Cortés et al., 2021). Carvacrol (2-methyl-5-1-methylethylphenol) provides the characteristic aroma of oregano (Ultee et al., 2000). It is synthesized from cymene via the mevalonate pathway and is a monoterpene that is insoluble in water and soluble in ethanol, carbon tetrachloride, and diethyl ether (Lee et al., 2017). Its stereochemistry (Figure 2) of a single phenolic ring with three substituents of functional groups (Memar et al., 2017) gives it antibacterial, antioxidant, anticancer, and anti-inflammatory properties (Tapia et al., 2017).

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Terpenes reported in Lippia graveolens
Figure 2
Terpenes reported in Lippia graveolens

In bacteria, carvacrol induces cell lysis by altering lipophilic compounds and hydrophobic parts of the cytoplasmic membrane, increasing cation permeability (H+ and K+), generating lipopolysaccharide efflux and reactive oxygen species production, inhibiting ATPase activity, microbial DNA replication, and energy synthesis, causing cell death (Gallegos et al, 2022). However, Ultee et al. (2000) reported that bacteria can adapt to carvacrol and modify the fatty acid composition of the membrane and reduce its permeability.

Thymol is an isomer of carvacrol (Figure 2). It is an aromatic substance with a white crystalline color, low solubility in water, and high solubility in organic solvents. It has a neutral pH but can have alkaline characteristics in aqueous solutions due to the deprotonation of phenol (Chizzola, 2013). It has bactericidal, fungicidal, insecticidal, nematicidal, and varroacidal activity (Gallegos et al., 2022). Its antibacterial effect in vitro against Escherichia coli, Salmonella spp. and S. aureus has been reported at a concentration of 0.75 mg/mL (Shapira-Mimran 2007; Gallegos et al., 2019). At concentrations of 1 and 2 % in oregano essential oil, it has greater antimicrobial activity against Gram-positive bacteria and less against Gram-negative bacteria (Du et al., 2015; Erazo et al., 2017). In vitro studies on Gram-negative enterobacteria found greater antibacterial activity of thymol from Lippia berlandieri compared to other antimicrobials (Garcia et al., 2022; Garcia et al., 2022). The antibacterial mechanism of action is similar to that of carvacrol, binding to bacterial membranes in a hydrophobic manner via hydrogen bonds, affecting the outer and inner membranes, increasing permeability and the loss of potassium ions and intracellular ATP, causing cell death (Di Pasqua et al., 2010).

Flavonoids

In L. graveolens, the flavonoids (Figure 3) with the highest reported biological activity are naringenin, quercetin, and luteolin (Lin et al., 2007). Naringenin is a bioactive compound with hepatoprotective, antiatherogenic, anti-inflammatory, antimutagenic, anticarcinogenic, and antimicrobial activity (Ke et al., 2017). In reaction with alkyl iodides, it forms O-alkyl compounds of naringenin with antibacterial potential against Escherichia coli, Staphylococcus aureus, and Bacillus subtilis (Kozłowska et al., 2019). A derivative of O-alkyl naringenin is sakuranetin (7-O-methylnaringenin), which has significant antimicrobial activity against Gram-negative and Gram-positive bacteria. Naringenin inhibits the growth of Staphylococcus aureus by affecting the cell membrane and fatty acid composition. In Escherichia coli, it acts on the genes associated with the biosynthesis of membrane fatty acids (Wang et al., 2018).

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Flavonoids reported in Lippia graveolens
Figure 3
Flavonoids reported in Lippia graveolens

Quercetin is a flavonol based on the flavone structure nC6 (ring A)-C3 (ring C)-C6 (ring B). It has broad-spectrum antibacterial activity, breaks down the cell wall of bacteria, inhibits nucleic acid synthesis, and reduces enzyme activity (Wang et al.,2018). Specifically, in Escherichia coli, it alters the activity of adenosine triphosphate (Plaper et al., 2003). According to Hooda et al. (2020), impregnating quercetin with silver nanoparticles inhibits the growth of bacteria: Klebsiella pneumoniae (ATCC790603), Enterococcus faecalis (ATCC51299), Proteus vulgaris (ATCC426), Escherichia coli (ATCC25922), Staphylococcus aureus (ATCC4330), and Pseudomonas aeruginosa (ATCC27853).

Luteolin (3',4',5,7-tetrahydroxyflavone) is a polyphenol of the flavone family, with a molecular structure (C6-C3-C6) of two benzene rings and a third ring containing oxygen, and a double bond between carbons C2 and C3 (Figure 3). Its structure favors its biochemical and biological activity (Wu et al., 2019). This flavonoid has various biological activities, such as antioxidant, anti-inflammatory, antimicrobial, anticarcinogenic, and hypoglycemic, hypolipidemic, hypotensive, and immunomodulatory effects (Wu et al., 2019). In bacteria, luteolin affects the integrity of the cell wall and membrane, inhibiting nucleic acid synthesis and protein expression and interfering with energy metabolism (Guo et al., 2022). In a study, Qian et al. (2021) found that luteolin impairs cell membrane morphology and affects biofilm formation in Staphylococcus aureus and Escherichia coli. In studies against Trueperella pyogenes, a minimum inhibitory concentration (MIC) of luteolin of 78 μg/mL was reported, and at half the MIC, susceptibility to methicillin- and macrolide-resistant Staphylococcus increases, providing an alternative treatment for resistant pathogens (Guo et al., 2022).

ACTIVITY OF Lippia spp. AGAINST RESISTANT BACTERIA ASSOCIATED WITH BOVINE MASTITIS

There are reports of the antibacterial activity of Lippia spp. extracts on resistant bacteria such as Streptococcus spp., Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella pneumoniae, and Escherichia coli (Gupta et al., 2020; Pinheiro et al., 2022; Nonato et al., 2022). The minimum inhibitory concentration in the evaluation of Lippia spp. extracts and metabolites on bacteria varies depending on the species evaluated, extraction methodology, and evaluation (Rani et al., 2022; Nonato et al., 2022; Suarez et al., 2024).

In Streptococcus spp., an MIC of 67 mg/mL is reported for supercritical fluid from L. graveolens, while for metabolites: thymol, MICs of 0.31 to 8.0 mg/mL are reported, and for carvacrol, 0.31 to 9 mg/mL (Table 2). In Staphylococcus spp., the MIC for ethanolic extracts of Lippia spp. is reported to be 128 to 512 µg/mL, for essential oil 53.3 to 512 µg/mL, while for thymol it was 0.15 to 0. 75 µg/mL and carvacrol from 0.38 to 1.3 µg/mL (Dal Pozzo et al., 2011; Rani et al., 2022; Gallegos et al., 2019; Nonato et al., 2022).

Tabla 2
Actividad antibacteriana de Lippia spp y sus metabolitos contra patógenos resistentes asociados a mastitis bovina
Bacteria Extracts and compounds Minimum Inhibitory Concentration (MIC) Reference
Streptococcus spp. Thymol

Carvacrol

 0.31-0.63 µL/mL

0.16-0.63 µL/mL

 Gupta et al. (2020)
Streptococcus agalactiae Supercritical fluid from L. graveolens 67 mg/mL García et al. (2019)
Thymol Carvacrol 8.0 mg/mL 9.0 mg/mL Gupta et al. (2020)
Staphylococcus aureus Ethanolic extract of L. alba

Ethanolic extract of L. sidoides

Ethanolic extract of L. gracilis

Essential oil of L. alba

Essential oil of L. sidoides

Essential oil of L. gracilis

 853 µg/mL

128 µg/mL

512 µg/mL

256 µg/mL

53.3 µg/mL

512 µg/mL

 Nonato et al. (2022)
Essential oil of L. graveolens 12 µL/mL Suarez et al. (2024)
Thymol 0.15-0.75 mg/mL Gallegos et al. (2019)
Carvacrol 0.38-0.45 mg /mL Rani et al. (2022)
Staphylococcus spp. L. graveolens essential oil

Thymol

Carvacrol

 1.6 mg /mL

0.4 a 0.5 mg/mL

0.8 a 1.3 mg/mL

 Dal Pozzo et al. (2011)
Pseudomonas aeruginosa Ethanolic extract of L. alba

Ethanolic extract of L. sidoides

Ethanolic extract of L. gracilis

Essential oil of L. alba

Essential oil of L. sidoides

Essential oil of L. gracilis

 213.3 µg/mL

128 µg/mL

512 µg/mL

1024 µg/mL

298.6 µg/mL

 Nonato et al. (2022)
Essential oil of L. berlandieri 682 µg/mL
Essential oil of L. origanoides 80 µg/mL Reyes et al. (2020)
Essential oil of L. origanoides 2500 μg/mL Pinheiro et al. (2022)
Mixture of essential oils of L. salvifolia: L. sidoides (9:1) 0.37 µg/mL >Gupta et al. (2020)
Escherichia coli Extracto etanólico de L. origanoides 5.0 μL Castellanos et al. (2020)
Ethanolic extract of L. alba

Ethanolic extract of L. sidoides

Ethanolic extract of L. gracilis

Essential oil of L. alba

1

Essential oil of L. sidoides

Essential oil of L. gracilis

 768 µg/mL

74.6 µg/mL

256 µg/mL

106.6 µg/mL

106.6 µg/mL

426.6 µg/mL

 Nonato et al. (2022)
L. origanoides essential oil 312 μg/mL Pinheiro et al. (2022)
L. berlandieri essential o 4 μg/mL Bautista et al. (2021)
Mixture of L. salvifolia essential oils: L. sidoides (9:1) 0.37 µg/mL Gupta et al. (2020)
Thymol 0.15-0.38 mg/mL Gallegos et al. (2019)
Carvacrol 0.15-0.75 mg/mL Rani et al. (2022)
Klebsiella pneumoniae L. origanoides essential oil

Thymol

Carvacrol

 312 μg/mL

0.75 mg/mL

0.75 mg/mL

 Pinheiro et al. (2022) Rani et al. (2022)

In Pseudomonas aeruginosa, an MIC for ethanolic extracts of 128 to 512 µg/mL is reported, while for essential oils it is 0.37 to 80 µg/mL. In the case of Escherichia coli, the following MIC reports were found: ethanolic extracts (74.6 to 256 µg/mL), essential oils (0.37 to 426 µg/mL), thymol (0.15 to 0.38 µg/mL), and carvacrol (0.15 to 0.75 µg/mL).

Essential oils and their compounds (carvacrol and thymol) have the highest antibacterial activity in resistant bacteria isolated from mastitis (Rani et al., 2022; Nonato et al., 2022; Suarez et al., 2024). Pinheiro et al. (2022) mention that the essential oil has inhibitory and bactericidal action against strains of Escherichia coli and Klebsiella pneumoniae, but not against Pseudomonas aeruginosa, where its effectiveness is reduced by the formation of biofilm and the action of efflux pumps, intrinsic characteristics of this species. The combination of ethanolic extracts of Lippia spp. with antimicrobials reduces the MICs of amikacin, gentamicin, and cephalothin, but has an antagonistic effect with benzylpenicillin and other natural extracts (Nonato et al., 2022). Currently, synergies between extracts and antimicrobials are being investigated to improve efficacy, reduce toxicity, and bacterial resistance (Garcia et al., 2019; Pinheiro et al., 2022; Nonato et al., 2023; Suarez et al., 2024).

CONCLUSIONS

The main secondary metabolites of L. graveolens are flavonoids and monoterpenes, and their concentration varies according to the soil and climate conditions of the plant's habitat. Its antibacterial activity has been demonstrated against various bacterial genera of importance in health, including those associated with bovine mastitis. The greatest antibacterial activity of L. graveolens has been associated with thymol and carvacrol; however, activity has also been reported due to the presence of naringenin, quercetin, and luteolin. In the search for alternatives to combat resistant or multidrug-resistant bacteria associated with bovine mastitis, the secondary metabolites of Lippia graveolens represent an option for studying new treatments.

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Lippia graveolens and its activity against bacteria associated with bovine mastitis: Literature review
  • Abanico vet  vol. 16Lippia graveolens and its activity against bacteria associated with bovine mastitis: Literature review 0000-0001-9845-2598 Vargas-Monter Jorge 1 2 0000-0002-6154-9983 Rivero-Pérez Nallely 1 * 0000-0003-0306-3560 Valladares-Carranza Benjamín 3 0000-0003-4649-2699 Ojeda-Ramírez Deyanira 1 0000-0002-0493-8843 Noguez-Estrada Juan 1 2 0000-0002-8537-5025 Zaragoza-Bastida Adrian ** 1 Author affiliationPermissions
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