Antimicrobial Activity of Diverse Chemotypes of Lippia graveolens Against Aeromonas hydrophila Isolated from Oreochromis niloticus
DOI:
https://doi.org/10.15359/ru.38-1.30Keywords:
essential oil, oregano, tilapia, aquaculture, thymolAbstract
[Objective] This study aimed to evaluate the antimicrobial efficacy of essential oil (EO) from diverse chemotypes of Lippia graveolens against oxytetracycline-resistant Aeromonas hydrophila, which primarily affects the tilapia aquaculture (O. niloticus) in Guatemala. [Methodology] L. graveolens were collected in three departments in Guatemala. The EO was obtained by hydrodistillation and characterized using gas chromatography and mass spectrometry (GC/MS). Subsequently, an antimicrobial assay was conducted using disk and dilution susceptibility tests and evaluation of synergistic interactions among the chemotypes. Each test was performed in triplicate. [Results] The analysis revealed the presence of twenty-seven compounds in the EO obtained from the chemotypes, with the main class being monoterpenes. The major constituents identified were cis-Dihydro-β-terpineol (8.84%) in chemotype I, carvacrol (51.82%) in chemotype II, and thymol (79.62%) in chemotype III. All EO chemotypes of L. graveolens demonstrated the ability to inhibit the A. hydrophila growth. Thymol chemotype exhibited the strongest inhibitory effect against bacterial growth, with a minimum inhibitory concentration (MIC) of 92.4 µg/mL and a minimum bactericidal concentration (MBC) of 184.8 µg/mL. Furthermore, the results suggest that there is no synergistic or additive effect when combining different chemotypes of L. graveolens. [Conclusions] This is the first report of L. graveolens chemotypes exhibiting antimicrobial activity against oxytetracycline-resistant A. hydrophila. The findings suggest that the chemotype thymol could be a potential treatment for infections in the tilapia aquaculture in Guatemala.
References
Adams, R. P. (2007). Identification of essential oil components by gas chromatography/mass spectroscopy. Allured Pub. Corp.
Alanazi, F., Almugbel, R., Maher, H. M., Alodaib, F. M., & Alzoman, N. Z. (2021). Determination of tetracycline, oxytetracycline, and chlortetracycline residues in seafood products of Saudi Arabia using high-performance liquid chromatography-photo diode array detection. Saudi Pharmaceutical Journal, 29(6), 566–575. https://doi.org/10.1016/j.jsps.2021.04.017
Alderman, D. J. & Smith, P. (2001). Development of draft protocols of standard reference methods for antimicrobial agent susceptibility testing of bacteria associated with fish diseases. Aquaculture, 196(1), 211–243. https://doi.org/10.1016/S0044-8486(01)00535-X
Arana-Sánchez, A., Estarrón-Espinosa, M., Obledo-Vázquez, E. N., Padilla-Camberos, E., Silva-Vázquez, R. and Lugo-Cervantes, E. (2010). Antimicrobial and antioxidant activities of Mexican oregano essential oils (Lippia graveolens H. B. K.) with different composition when microencapsulated in β-cyclodextrin. Letters in Applied Microbiology, 50(6), 585–590. https://doi.org/10.1111/j.1472-765X.2010.02837.x
Bassole, I. H. N., Nebie, R., Savadogo, A., Ouattara, C. T., Barro, N. and Traore, S. A. (2005). Composition and antimicrobial activities of the leaf and flower essential oils of Lippia chevalieri and Ocimum canum from Burkina Faso. African Journal of Biotechnology, 4(10), 1156–1160. https://www.ajol.info/index.php/ajb/article/view/71260
Bauer, A. W., Kriby, W. M. M., Sherris, J. C., Turck, M., (1966). Antibiotic Susceptibility Testing by a Standardized Single Disk Method. American Journal of Clinical Pathology, 45(4), 493–496, https://doi.org/10.1093/ajcp/45.4_ts.493
Bautista-Hernández, I., Aguilar, C. N., Martínez-Ávila, G. C. G., Torres-León, C., Ilina, A., Flores-Gallegos, A. C., Kumar Verma, D. and Chávez-González, M. L. (2021). Mexican oregano (Lippia graveolens Kunth) as source of bioactive compounds: A review. Molecules, 26(17), 1–19. https://doi.org/10.3390/molecules26175156
Benjemaa, M., Snoussi, M., Falleh, H., Hessini, K., Msaada, K., Flamini, G. and Ksouri, R. (2022). Chemical composition, antibacterial and antifungal activities of four essential oils collected in the North-East of Tunisia. Journal of Essential Oil Bearing Plants, 25(2), 338–355. https://doi.org/10.1080/0972060X.2022.2068971
Bussmann, R. W., Malca-García, G., Glenn, A., Sharon, D., Chait, G., Díaz, D., Pourmand, K., Jonat, B., Somogy, S., Guardado, G., Aguirre, C., Chan, R., Meyer, K., Kuhlman, A., Townesmith, A., Effio-Carbajal, J., Frías-Fernandez, F. and Benito, M. (2010). Minimum inhibitory concentrations of medicinal plants used in Northern Peru as antibacterial remedies. Journal of Ethnopharmacology 132(1), 101–108. https://doi.org/10.1016/j.jep.2010.07.048
Castellanos-Hernández, O. A., Rodríguez-Sahagún, Martha., Acevedo-Hernández, Gustavo., Aarland-Rayn, Clarenc. and Rodríguez-Sahagún, Araceli. (2020). Evaluation of the essential oil of Lippia graveolens as a growth inhibitor of Salmonella sp, E. coli and Enterococcus sp. E-CUCBA, 7(14), 1–6. https://doi.org/10.32870/e-cucba.v0i14.155
García-Pérez, J., Marroquín-Mora, D. and Pérez-González, M. (2019). Inclusión de extracto de Lippia graveolens (Kunth) en la alimentación de Oreochromis niloticus (Linnaeus, 1758) para la prevención de estreptococosis por Streptococcus agalactiae (Lehmann y Neumann, 1896). Revista AquaTIC, 54(1), 15–24. https://dialnet.unirioja.es/servlet/articulo?codigo=7681118#:~:text=La%20presente%20investigaci%C3%B3n%20evalu%C3%B3%20el%20efecto%20de%20la,L.%20graveolens%2C%20en%20una%20dieta%20comercial%20para%20tilapia.
García-Pérez, J. & Marroquín Mora, D. (2021). Evaluación in vitro de extractos de plantas medicinales como posibles agentes antimicrobianos para bacterias patógenas en tilapia. Kuxulkab', 27(57), 27-35. https://doi.org/10.19136/kuxulkab.a27n57.3702
García-Pérez, J., Ulloa-Rojas, J. B. and Mendoza-Elvira, S. (2021). Bacterial pathogens and their antimicrobial resistance in tilapia culture in Guatemala. Uniciencia, 35(2), 1–17. https://doi.org/10.15359/RU.35-2.4
Gutierrez, J., Barry-Ryan, C., and Bourke, P. (2008). The antimicrobial efficacy of plant essential oil combinations and interactions with food ingredients. International Journal of Food Microbiology, 124(1), 91–97. https://doi.org/10.1016/j.ijfoodmicro.2008.02.028
Ham, Y., Yang, J., Choi, W. S., Ahn, B. J. and Park, M. J. (2020). Antibacterial activity of essential oils from Pinaceae leaves against fish pathogens. Journal of The Korean Wood Science and Technology, 48(4), 527–547. https://doi.org/10.5658/WOOD.2020.48.4.527
Helander, I. M., Alakomi, H.-L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., Gorris, L. G. M. and von Wright, A. (1998). Characterization of the action of selected essential oil components on Gram-negative Bacteria. Journal of Agricultural and Food Chemistry, 46(9), 3590–3595. https://doi.org/10.1021/jf980154m
Hernández, T., Canales, M., Avila, J. G., García, A. M., Meraz, S., Caballero, J. and Lira, R. (2009). Composition and antibacterial activity of essential oil of Lippia graveolens H.B.K. (Verbenaceae). Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas, 8(4), 295–300. https://www.redalyc.org/pdf/856/85611265010.pdf
Höferl, M., Wanner, J., Tabanca, N., Ali, A., Gochev, V., Schmidt, E., Kaul, V. K., Singh, V. and Jirovetz, L. (2020). Biological activity of Matricaria chamomilla essential oils of various chemotypes. Planta Medica International Open, 07(03), 114–121. https://doi.org/10.1055/a-1186-2400.
Koba, K., Poutoli, P. W., Raynaud, C., Chautmont, J. P. and Sanda, K. (2009). Chemical composition and antimicrobial properties of different basil essential oils chemotypes from Togo. Bangladesh Journal of Pharmacology, 4(1), 1–8. https://doi.org/10.3329/bjp.v4i1.998
Lambert, R. J. W., Skandamis, P. N., Coote, P. J. and Nychas, G.-J. E. (2001). A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. Journal of Applied Microbiology, 91(1), 453–462. https://doi.org/10.1046/j.1365-2672.2001.01428.x
Levison, M. E. (2004). Pharmacodynamics of antimicrobial drugs. Infectious Disease Clinics of North America, 18(3), 451–465. https://doi.org/10.1016/j.idc.2004.04.012
Leyva-López, N., Gutiérrez-Grijalva, E. P., Vazquez-Olivo, G. and Heredia, J. B. (2017). Essential oils of oregano: Biological activity beyond their antimicrobial properties. Molecules, 22(6), 1–24. https://doi.org/10.3390/molecules22060989
Majolo, C., Pilarski, F., Chaves, F. C. M., Bizzo, H. R. and Chagas, E. C. (2018). Antimicrobial activity of some essential oils against Streptococcus agalactiae, an important pathogen for fish farming in Brazil. Journal of Essential Oil Research, 30(5), 388–397. https://doi.org/10.1080/10412905.2018.1487343
Martínez, J. Ramy., Chérigo, Lilia. & Ríos, Nivia. (2021). Evaluation of antibacterial properties of three Panamanian plants against multi-drug resistant bacteria. Tecnociencia, 23(1), 351–358. https://doi.org/10.48204/j.tecno.v23n1a19
Martínez-Natarén, D. A., Parra-Tabla, V., Dzib, G. and Calvo-Irabién, L. M. (2011). Morphology and density of glandular trichomes in populations of Mexican oregano (Lippia graveolens H.B.K., Verbenaceae), and the relationship between trichome density and climate. Journal of the Torrey Botanical Society, 138(2), 134–144. https://doi.org/10.3159/TORREY-D-10-00007.1
Martínez-Natarén, D. A., Parra-Tabla, V., Ferrer-Ortega, M. M. and Calvo-Irabién, L. M. (2014). Genetic diversity and genetic structure in wild populations of Mexican oregano (Lippia graveolens H.B.K.) and its relationship with the chemical composition of the essential oil. Plant Systematics and Evolution 300(3), 535–547. https://doi.org/10.1007/s00606-013-0902-y
Mazumder, A., Choudhury, H., Dey, A. and Sarma, D. (2020). Bactericidal activity of essential oil and its major compound from leaves of Eucalyptus maculata Hook. Against two fish pathogens. Journal of Essential Oil Bearing Plants. Plants, 23(1), 149–155. https://doi.org/10.1080/0972060X.2020.1729248
Nikkhah, M., Hashemi, M., Habibi Najafi, M. B. & Farhoosh, R. (2017). Synergistic effects of some essential oils against fungal spoilage on pear fruit. International Journal of Food Microbiology, 257(1), 285–294. https://doi.org/10.1016/j.ijfoodmicro.2017.06.021
Noga, E. (2010). Fish disease: Diagnosis and treatment. Iowa: Blackwell Publishing. https://doi.org/10.1002/9781118786758
Nwanosike, E., Fatokun, O. T., Okhale, S. E., Nwanosike, M. and Folashade Kunle, O. (2016). Phytochemistry and ethnopharmacology of Lippia genus with a statement on chemotaxonomy and essential oil chemotypes. International Journal of Pharmacognosy, 3(5), 201–211.
Ocampo-Velázquez, R. V., Malda-Barrera, G. X., Suárez-Ramos, G. (2009). Biología reproductiva del orégano mexicano (Lippia graveolens Kunth) en tres condiciones de aprovechamiento. Agrociencia, 43(5), 475–482. https://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S1405-31952009000500003
Olusola, S. E., Emikpe, B. and Olaifa, F. (2013). The potentials of medicinal plants extracts as bio-antimicrobial in aquaculture. International Journal of Medicinal and Aromatic Plants, 3(3), 404–412.
Pascual, M. E., Slowing, K., Carretero, E., Sánchez Mata, D. and Villar, A. (2001). Lippia: traditional uses, chemistry and pharmacology: a review. Journal of Ethnopharmacology, 76(3), 201–214. https://doi.org/10.1016/S0378-8741(01)00234-3
Pérez-Sabino, J. F., Mérida-Reyes, M., Farfán-Barrera, C. D. and Ribeiro da Silva, A. J. (2012). Analysis and discrimination of the chemotypes of Lippia graveolens H.B.K. of Guatemala by solid phase microextraction, GC-MS and multivariate analysis. Química Nova, 35(1), 97–101. https://doi.org/10.1590/S0100-40422012000100018
R Core Team (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
Rigos, G., Nengas, I., Alexis, M., & Troisi, G. M. (2004). Potential drug (oxytetracycline and oxolinic acid) pollution from Mediterranean sparid fish farms. Aquatic Toxicology, 69(3), 281–288. https://doi.org/10.1016/j.aquatox.2004.05.009
Romero, J., Feijoó, C. G., & Navarrete, P. (2012). Antibiotics in Aquaculture-Use, Abuse and Alternatives. In E. Carvalho, G. David, & R. Silva (Eds.), Health and Environment in Aquaculture (IntechOpen).
Salgueiro, L. R., Cavaleiro, C., Gonc Ëalves, M. J., Proenc, A. and da Cunha, A. (2003). Antimicrobial activity and chemical composition of the essential oil of Lippia graveolens from Guatemala. Planta Medica, 69(1), 80–83. https://doi.org/10.1055/s-2003-37032
Senatore, F. and Rigano, D. (2001). Essential oil of two Lippia spp. (Verbenaceae) growing wild in Guatemala. Flavour and Fragrance Journal. J, 16(3), 169–171. https://doi.org/10.1002/ffj.972
Standley, Paul., & Williams, Louis. (1970). Flora of Guatemala Part IX. In Standley, P. C., Williams, L. O. and Gibson, D. N. (Eds.), Flora of Guatemala (I, Vol. 24). Field Museum of Natural History. https://doi.org/10.5962/bhl.title.2434
Terblanché, F. C. and Kornelius, G. (1996). Essential Oil Constituents of the Genus Lippia (Verbenaceae) A Literature Review. Journal of Essential Oil Research, 8(5), 471–485. https://doi.org/10.1080/10412905.1996.9700673
Tezara, W., Coronel, I., Hererra, A., Dzib, G., Canul-Puc, K., Calvo-Irabién, L. M. and González-Meler, M. (2014). Photosynthetic capacity and terpene production in populations of Lippia graveolens (Mexican oregano) growing wild and in a common garden in the Yucatán peninsula. Industrial Crops and Products, 57, 1–9. https://doi.org/10.1016/j.indcrop.2014.03.012
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