Antibacterial and antibiofilm activity of microencapsulated and non-microencapsulated Syzygium aromaticum essential oil
DOI:
https://doi.org/10.33448/rsd-v11i6.29076Keywords:
Clove; Biofilm; Staphylococcus aureus; Microencapsulation.Abstract
The aim of this work was to evaluate the antibacterial and antibiofilm activity of microencapsulated and non-microencapsulated clove (Syzygium aromaticum) essential oil on multidrug-resistant Staphylococcus aureus strains. Antibacterial activity was performed by disk diffusion and broth microdilution techniques to determine the Minimum Inhibitory Concentration (MIC) and Minimum Bactericidal Concentration (MBC) of the essential oil. For the antibiofilm activity, strains of S. aureus that were sensitive to the action of the essential oil were used. Five isolates were sensitive to the action of the essential oil by the disk diffusion test whose MIC was 10 μL.mL-1 and the CBM was 20 μL.mL-1. Of these five, four were able to form biofilms with adhesion greater than 107 CFU.cm-2. The microencapsulated oil showed a better antibiofilm effect with a reduction of about 2 log CFU.cm-2 in the multiresistant S. aureus analyzed, and the non-microencapsulated oil reduced approximately 1.1 log CFU.cm-2 showing the high efficiency of the oil with microencapsulation. The use of microencapsulated Syzygium aromaticum essential oil could serve as a promising alternative in the control of multiresistant and biofilm forming bacteria on stainless steel surfaces, presenting some advantages compared to the one used in its original form, mainly with regard to transport, content preservation, handling and use in food matrices.
References
Almeida, A. C., Oliveira, L., Paulo, P. D., Martins, E. R., Souza, R. M., Figueiredo, L. S., Santos, C. A. & Fonseca, H. C. (2013). Potencial antimicrobiano dos óelos essenciais de cravo da índia e alfavação em carne moída de ovinos contaminas experimentalmente com S. aureus. Rev Bras Cien Vet, 20(4), 248-251.
Almeida, J. C., Almeida, P. P., Gherardi, S. R. M (2020). Potencial antimicrobiano de óleos essenciais: uma revisão de literatura de 2005 a 2018. Rev Elect Nutri Time, 17(1), 8623-33.
Alves, P. I. C. (2019). Potencial antimicrobiano de óleos essenciais de Pimpinella anisum L., Syzygium aromaticum L. e Origanum vulgare L., e desenvolvimento de coberturas comestíveís a base de quitosana incorporadas de óleos essenciais para produtos cárneos (Dissertação). Programa de Pós-Graduação em Nutrição e Alimentos, Universidade Federal de Pelotas. Pelotas, Rio Grande do Sul, Brasil. Recuperado de: http://repositorio.ufpel.edu.br:8080/bitstream/prefix/7608/1/Dissertacao_Pamela_Inchauspe_Correa_Alves.pdf.
Andrade, N. J., Bridgman, T. A. & Zottola, E. A. (1998). Bacteriocidal activity of sanitizers against Enterococcus faecium attached to stainless steel as determined by plat count and impedance methods. J Food Prot, 61(7), 833-838.
Araújo, J. S. F. (2019). Micropartículas de óleo essencial de laranja doce (Citruss aurantium var.dulcis) em matriz de gelatina e maltodextrina (Dissertação). Programa de Pós-Graduação em Sistemas Agroindústrias, Universidade Federal de Campina Grande. Pombal, Paraíba, Brasil. Recuperado de: http://dspace.sti.ufcg.edu.br:8080/jspui/handle/riufcg/6336.
Bakry, A., Abbas, S., Ali, B., Majeed, H., Abouelwafa, M., Mousa, A. & Liang, L. (2015). Microencapsulation of Oils: A Comprehensive Review of Benefits, Techniques, and Applications. Comprehensive Reviews in Food Science and Food Safety, 15, 143–182. https://doi.org/10.1111/1541-4337.12179
Baranauskaite, J., Kopustinskiene, D. M., & Bernatoniene, J. (2019). Impact of Gelatin Supplemented with Gum Arabic, Tween 20, and β-Cyclodextrin on the Microencapsulation of Turkish Oregano Extract. Molecules, 24(176), 1-16. https://doi.org/10.3390/molecules24010176
Benincá, M. C. (2018). Efeito inibitório de óleos essenciais contra Staphylococcus aureus multirresistentes e formadores de biofilmes (Dissertação). Universidade de Passo Fundo. Passo Fundo, Rio Grande do Sul, Brasil.
Beraldo, C., Daneluzzi, N. S., Scanavacca, J., Doyama, J. T., Fernandes Júnior, A. & Moritz, C. M. F. (2013). Eficiência de óleos essenciais de canela e cravo da índia como sanitizantes na indústria de alimentos. Pesq Agropec Trop, 43(4), 436-440. https://doi.org/10.1590/S1983-40632013000400006.
Borborema, D. P. S. (2021) Óleo essencial de Syzygium aromaticum microencapsulado na redução da produção de biofilmes produzidos por Staphylococcus aureus multirresistentes à antimicrobianos (Dissertação). Universidade Federal de Minas Gerais. Montes Claros, Minas Gerais, Brasil.
Budri, P. E., Silva, N. C., Bonsaglia, E. C., Fernandes Junior, A., Araujo Junior, J. P., Doyama, J. T., Goncalves, J. L., Santos, M. V, Fitzgerald-Hughes, D., & Rall, V. L. (2015). Effect of essential oils of Syzygium aromaticum and Cinnamomum zeylanicum and their major components on biofilm production in Staphylococcus aureus strains isolated from milk of cows with mastitis. J Dairy Sci, 98(9), 5899–5904. https://doi.org/10.3168/jds.2015-9442
Burt, S. Essential oils: their antibacterial properties and potential applications in foods – a review. Int J Food Microbiol, 94, 233-253.
Chaieb, K., Hajlaoui. H., Zmantar, T., Kahla-Nakbi, A. B., Rouabhia, M., Mahdouani, K. & Bakhrouf, A. (2007). The chemical composition and biological activity of clove essential oil, Eugenia caryophyllata (Syzygium aromaticum, L. Myrtaceae): a short review. Phytotherapy Research, 21, 501-506.
CLSI. Clinical and Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically (2015b).
CLSI. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk Susceptibility Tests (2015a).
Comunian, T., Gómez-Estaca, J., Furtado, R., Conceição, G., Moraes, I., Castro, I., & Favaro-Trindade, C. (2016). Effect of different polysaccharides and crosslinkers on echium oil microcapsules. Carbohydrate Polymers, 150. https://doi.org/10.1016/j.carbpol.2016.05.044
Cortés-Rojas, D. F., de Souza, C. R. F., & Oliveira, W. P. (2014). Clove (Syzygium aromaticum): a precious spice. Asian Pacific Journal of Tropical Biomedicine, 4(2), 90–96. https://doi.org/https://doi.org/10.1016/S2221-1691(14)60215-X
Cunha, R. C., Rosa, M. D. H., Silva, C., Santos, D. S. & Leite, F. P. L. (2019). Staphylococcal slime layers and biofilm from different origins. Ciência Rural, Santa Maria, 49(05), 1-9. http://dx.doi.org/10.1590/0103-8478cr20180783
Cui, H.; Zhao, C.; Lin, l. (2015). The specific antibacterial activity of lipossome-encapsulated Clove oil ant its application in tofu. Food Control, 56, 128-134.
Dias, C., Borges, A., Saavedra, M. J. & Simões, M. (2018). Biofilm formation and multidrug-resistant Aeromonas spp. from wild animals. Journal of Global Antimicrobial Resistance, 12, 227-234.
Donlan, R. M. (2002). Biofilms: Microbial Life on Surfaces. Emerging Infectious Diseases, 8, 881-890.
Farias, P. K. S., Silva, J. C. R. L., Souza, C. N. de, Fonseca, F. S. A. da, Brandi, I. V., Martins, E. R., Azevedo, A. M., & Almeida, A. C. de. (2019). Antioxidant activity of essential oils from condiment plants and their effect on lactic cultures and pathogenic bacteria. Cienc Rural, 49(2). https://doi.org/10.1590/0103-8478cr20180140
Favaro-Trindade, C., Pinho, S. (2008). Revisão: microencapsulação de ingredientes alimentícios. Braz. J. Food Technol., 11(2), 103-112. Recuperado de: https://www.researchgate.net/publication/237521407_Revisao_Microencapsulacao_de_ingredientes_alimenticios.
Friedriczewski, A.B., Gandram E.A, Conceição, R. C. S., Cereser, N.D., Moreira, L.M. & Timm, C.D. (2018). Formação de biofilme por Staphylococcus aureus isolados de queijo mussarela elaborado com leite de búfala e seu efeito sobre a sensibilidade a santinizantes. Acta Scien Veter, 46, 1528. https://doi.org/10.22456/1679-9216.81813
Gotardo, F. M. (2021). Microencapsulação de óleos essenciais de orégano e canela combinados com ação sobre Listeria monocytogenes em produto cárneo (Dissertação). Universidade Passo Fundo, Passo Fundo. Passo Fundo, Rio Grande do Sul, Brasil.
Guimaraes, C. C., Ferreira, T. C., Oliveira, R. C. F., Simioni, P. U. & Ugrinovich, L. A. (2017). Atividade antimicrobiana in vitro do extrato aquoso e do óleo essential do alecrim (Rosmarinus officinalis L.) e cravo-da-índia (Caryophyllus aromaticus L.). Revista Brasileira de Biociências, 15(2), 83-89.
Kopp, V. V. (2020). Óleo essencial de cravo encapsulado como microbiota natural (Dissertação de mestrado). Universidade Federal do Rio Grande do Sul, Rio Grande do Sul, Brasil.
Leyva, J., Bello-Pérez, L., Alvarez-Ramirez, J., & Garcia, H. (2016). Microencapsulation using starch as wall material: A review. Food Reviews International, 34. https://doi.org/10.1080/87559129.2016.1261298
Marques, E.B.P. (2017). Nanoencapsulação de óleo essencial de cravo em matrizes lipidicas (Monografia). Universidade Federal de Santa Catarina. Florianópolis, Santa Catarina, Brasil.
Menon, K. V. (2016). Biofilm and food industry. International Journal of Advanced Research in Biological Sciences, 4, 137-142.
Millezi, A. F., Costa, K. A. D., Oliveira, J. M., Lopes, S. P., Pereira, M. O. & Picolli, R. H. (2019). Antibacterial and anti-biofilm activity of cinnamon essencial oil and eugenol. Ciência Rural, 49 (1), 1-7.
Nascimento, L.D. (2021). Óleo essencial de Lippia thymoides Mart. Schauer: Obtenção, caracterização química e microencapsulação (Tese de doutorado). Universidade Federal do Pará. Belém, Pará, Brasil.
Oliveira, F. S. (2017). Atividade antioxidante e antimicrobiana de óleos essenciais aplicados na conservação de linguiça frescal de frango (Dissertação de mestrado). Universidade Federal de Minas Gerais, Montes Claros, Minas Gerais, Brasil.
Oliveira, T. F., Ferreira, J. S., Boa Sorte, P. M. F., Reis, V. M., Baldani, J. I. & Schwab, S. (2009). Concentração mínima inibitória (CMI) de antibióticos para oito estirpes de bactérias diazotróficas da coleção de culturas da Embrapa Agrobiologia. Boletim de Pesquisa e Desenvolvimento. Recuperado de: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/663940/3/bot049092013.pdf.
Percival, S. L.; Knottenbelt, D. C.; Cochrane, C. A (2011). Biofilms and veterinary medicine, Springer, Berlin.
Radaelli, M., Silva, B. P., Weidlich, L., Hoehne, L., Flach, A., Costa, L. A. M. A. & Ethur, E. M. (2016). Antimicrobial activities of six essential oils aommonly used as condiments in Brazil against Clostridium perfringens. Brazilian Journal of Microbiology, 47, 424-430.
Radunz, M., Trindade, M. L. M., Camargo, T. M., Radunz, A. L., Borges, C. D., Gandra, E. A. & Helbig, E. (2019). Antimicrobial and antioxidant activity of unencapsulated and encapsulated clove (Syzygium aromaticum, L.) essential oil. Food Chemistry, 276, 180-186.
Santos, J. R. N., Teles, A. M., Ferreira, C. G. & Mouchrek, A. N. (2020). Avaliação da atividade bactericida e antioxidade do óleo essencial e do extrato hidroalcoólico de orégano (Origanum vulgare). Research, Society and Development, 9(10), 1-17.
Sousa, J.B.G. (2018). Atividade antioxidante, antimicrobiana e citotoxicidade do óleo essencial do gênero Lippia spp (Dissertação de mestrado). Universidade Federal de Campina Grande. Pombal, Paraíba, Brasil.
Souza, G. A. A. D., Almeida, A. C., Xavier, M. A. S., Silva, L. M. V., Sousa, C. N., Sanglard, D. A & Xavier, A. R. E. (2019). Characterization and molecular epidemiology of Staphylococcus aureus strains resistant to beta-lactams isolated from the milk of cows diagnosed with subclinical mastitis. Veterinary World, 12(12), 1931-1939. https://doi.org/10.14202/vetworld.2019.1931-1939
Szweda, P., Schielmann, M., Milewski, S., Frankowska, A., Jakubczak, A. (2012). Biofilm production and presence of ica and bap genes in Staphylococcus aureus strains isolated from cows with mastitis in the Eastern Poland. Polish Journal of Microbiology, 61(1), 65-69.
Xu, J.G., Liu, T., Hu, Q.P., & Cao, X.M. (2016). Composição química, propriedades antibacterianas e mecanismo de ação do óleo essencial de cravo-da-índia contra Staphylococcus aureus. Molecules, 21(9), 1194. https://doi.org/10.3390/molecules21091194.
Weerasekera, M. M., Wijesinghe, G. K., Jayarathna, T. A., Gunasekara, C. P., Fernando, N., Kottegoda, N. & Samaranayake, L. P. (2016). Culture media profoundly affect Candida albicans and Candida tropicalis growth, adhesion and biofilm development. Mem Inst Oswaldo Cruz, 111(11), 697-702.
Walmiki, M. R., Ravishankar, R. (2017). Cell Attachment and Anti-biofilm activity of Syzygium aromaticum, Cuminum cyminum and Piper nigrum essential oil against pathogenic bactéria. TEOP, 20(1), 59-69.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Daniele Pereira de Souza Borborema; Cintya Neves de Souza; Carolina Magalhães Caires Carvalho; Charles Martins Aguilar; Fernando Eustáquio de Matos Júnior; Ulisses Alves Pereira; Ester Dias Xavier; Alessandra Rejane Ericsson de Oliveira Xavier; Janaína Teles de Faria; Anna Christina de Almeida
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
