In vitro antimicrobial activity of a blend of cashew and castor vegetable oils and clove, eugenol, thymol, and vanillin essential oils against Gram-negative and Gram-positive ruminal bacteria
DOI:
https://doi.org/10.33448/rsd-v10i8.16900Keywords:
Encapsulate compounds; Growth inhibition; Natural additives; Rumen environment; Ruminal modulation.Abstract
Public concern over the routine use of antibiotics and ionophores in ruminant diets has increased due to the emergence of antibiotic-resistant bacteria that may represent risks to human health. Thus, efforts have been employed toward the development of alternative compounds to replace antibiotics and ionophores in ruminants’ diets. This study was carried out to investigate the in vitro effects of a blend containing cashew and castor vegetable oils and clove, eugenol, thymol, and vanillin essential oils on the activity of Gram-negative and Gram-positive ruminal bacteria. The experiments were designed so that each bacterium would be exposed to doses of 1.5,3.0, 4.5, and 6.0 mg/mL of the blend, with six replicates. Bacteria were cultivated on Hobson’s M2 medium in Hungate tubes. Antimicrobial activity was evaluated using a spectrophotometer at 600 nm. Readings were performed 0, 8, 12, and 24 hours after inoculation at 39º C. The four (1.5, 3.0, 4.5, and 6.0 mg/mL) concentrations of the blend of vegetable and essential oils inhibited the growth of Prevotella albensis, Prevotella bryantii, Prevotella ruminicola, and Anaerovibrio lipolyticus at 8 and 12 hours after the incubation. For Ruminococcus albus and Ruminococcus flavefaciens the addition of the blend of EO of concentrations of 3.0 and 4.5 mg/mL resulted in a greater impact on growth dynamics, with a reduction in optical density after 12 h of incubation. The findings of this research establish the combined action of the vegetable and essential oils was found to influence the growth of gram-negative and gram-positive bacteria and can be used as a rumen modulator. The study contributes to new information about the combined action of the vegetable and essential oils as antimicrobial agents on ruminant production.
References
Akhtar, N., Ihsan, U. H., & Mirza, B. (2018). Phytochemical analysis and comprehensive evaluation of antimicrobial and antioxidant properties of 61 medicinal plant species. Arabian Journal of Chemistry, 11(8), 1223–1235. https://doi.org/10.1016/j.arabjc.2015.01.013.
Babaoglu, H. C., Bayrak, A., Ozdemir, N., & Ozgun, N. (2017). Encapsulation of clove essential oil in hydroxypropyl beta‐cyclodextrin for characterization, controlled release, and antioxidant activity. Journal of Food Processing and Preservation, 41(5), e13202. https://doi.org/10.1111/jfpp.13202.
Benchaar, C., Calsamiglia, S., Chaves, A. V, Fraser, G. R., Colombatto, D., McAllister, T. A., & Beauchemin, K. A. (2008). A review of plant-derived essential oils in ruminant nutrition and production. Animal Feed Science and Technology, 145(1–4), 209–228. https://doi.org/10.1016/j.anifeedsci.2007.04.014.
Biondo, P. B. F., Carbonera, F., Zawadzki, F., Chiavelli, L. U. R., Pilau, E. J., Prado, I. N., & Visentainer, .V. (2017). Antioxidant capacity and identification of bioactive compounds by GC-MS of essential oils from spices, herbs and citrus. Current Bioactive Compounds, 13(2), 137–143. https://doi.org/10.2174/1573407212666160614080846.
Burt, S. A. (2004). Essential oils: their antibacterial properties and potential applications in foods—a review. International Journal of Food Microbiology, 94(3), 223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022.
Cruz, O. T. B., Valero, M. V., Zawadzki, F., Rivaroli, D. C., Prado, R. M., Lima, B. S., & Prado, I. N. (2014). Effect of glycerine and essential oils (anacardium occidentale and ricinus communis) on animal performance, feed efficiency and carcass characteristics of crossbred bulls finished in a feedlot system. Italian Journal of Animal Science, 13(4). https://doi.org/10.4081/ijas.2014.3492.
Davidson, P. M. (1997). Chemical preservatives and natural antimicrobial compounds. In M. P. Doyle, L. R. Beuchat, & T. J. Montville (Eds.), Food microbiology: fundamentals and frontiers (pp. 520–556). American Society for Microbiology.
Davidson, P. M., & Naidu, A. S. (2000). Phyto-phenols. In A. S. Naidu (Ed.), Natural Food Antimicrobial Systems (pp. 265–294). CRC - Press. https://doi.org/http://dx.doi.org/10.3168/jds.2007-0347
Deans, S. G., & Ritchie, G. (1987). Antibacterial properties of plant essential oils. International Journal of Food Microbiology, 5(2), 165–180. https://doi.org/10.1016/0168-1605(87)90034-1
Diggle, P., Diggle, P. J., Heagerty, P., Liang, K.-Y., Heagerty, P. J., & Zeger, S. (2002). Analysis of longitudinal data. Oxford University Press. https://doi.org/10.2307/2291352.
Dorman, H. J. D., & Deans, S. G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88(2), 308–316. https://doi.org/10.1046/j.1365-2672.2000.00969.x
Dušková, D., & Marounek, M. (2001). Fermentation of pectin and glucose, and activity of pectin‐degrading enzymes in the rumen bacterium Lachnospira multiparus. Letters in Applied Microbiology, 33(2), 159–163. https://doi.org/10.1111/j.1472-765X.2004.01492.x.
Enemark, J. M. D. (2008). The monitoring, prevention and treatment of sub-acute ruminal acidosis (SARA): A review. The Veterinary Journal, 176(1), 32–43. https://doi.org/10.1016/j.tvjl.2007.12.021.
Fugita, C. A., Prado, R. M., Valero, M. V., Bonafé, E. G., Carvalho, C. B., Guerrero, A., Sañundo, C., & Prado, I. N. (2018). Effect of the inclusion of natural additives on animal performance and meat quality of crossbred bulls (Angus vs. Nellore) finished in feedlot. Animal Production Science, 58(11), 2076–2083. https://doi.org/10.1071/AN16242.
Gedam, P. H., & Sampathkumaran, P. S. (1986). Cashew nut shell liquid: Extraction, chemistry and applications. Progress in Organic Coatings, 14(2), 115–157. https://doi.org/10.1016/0033-0655(86)80009-7
Goñi, P., López, P., Sánchez, C., Gómez-Lus, R., Becerril, R., & Nerín, C. (2009). Antimicrobial activity in the vapour phase of a combination of cinnamon and clove essential oils. Food Chemistry, 116(4), 982–989. https://doi.org/http://dx.doi.org/10.1016/j.foodchem.2009.03.058.
Guerrero, A., Rivaroli, D. C., Sañudo, C., Campo, M. M., Valero, M. V, Jorge, A. M., & Prado, I. N. (2018). Consumer acceptability of beef from two sexes supplemented with essential oil mix. Animal Production Science, 58(9), 1700–1707. https://doi.org/10.1071/AN15306.
Guil-Guerrero, J. L., Ramos, L., Moreno, C., Zúñiga-Paredes, J. C., Carlosama-Yepez, M., & Ruales, P. (2016). Antimicrobial activity of plant-food by-products: A review focusing on the tropics. Livestock Science, 189, 32–49. https://doi.org/http://dx.doi.org/10.1016/j.livsci.2016.04.021.
Gyawali, R., Hayek, S. A., & Ibrahim, S. A. (2015). Plant extracts as antimicrobials in food products: Mechanisms of action, extraction methods, and applications. Handbook of Natural Antimicrobials for Food Safety and Quality, 1, 49–68. https://doi.org/http://dx.doi.org/10.1016/B978-1-78242-034-7.00003-7.
Hammer, K. A., Carson, C. F., & Riley, T. V. (1999). Antimicrobial activity of essential oils and other plant extracts. Journal of Applied Microbiology, 86(6), 985–990.
Helander, I. M., Alakomi, H.-L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., Gorris, L. G. M., & 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.
Hobson, P. N. (1969). Rumen bacteria. Methods in Microbiology, 3B, 133–149. https://doi.org/10.1016/S0580-9517(08)70504-X.
Hosein, A. M., Breidt, F., & Smith, C. E. (2011). Modeling the effects of sodium chloride, acetic acid, and intracellular pH on survival of Escherichia coli O157: H7. Applied and Environmental Microbiology, 77(3), 889–895. https://doi.org/10.1128/AEM.02136-10.
Hungate, R. E. (1966). The Rumen and its microbes. In The rumen and its microbes (Academic P). https://doi.org/10.1016/B978-1-4832-3308-6.50005-X
Hyldgaard, M., Mygind, T., & Meyer, R. L. (2012). Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Frontiers in Microbiology, 3(12), 1–24. https://doi.org/10.3389/fmicb.2012.00012.
Jayasena, D. D., & Jo, C. (2013). Essential oils as potential antimicrobial agents in meat and meat products: A review. Trends in Food Science & Technology, 34(2), 96–108. https://doi.org/10.1016/j.tifs.2013.09.002.
Kempinski, E. M. B. C., Vital, A. C. P., Monteschio, J. O., Alexandre, S., Nascimento, K. F., Madrona, G. S., Mikcha, J. M. G., & Prado, I. N. (2017). Development and quality evaluation of infant food with oregano essential oil for children diagnosed with cerebral palsy. LWT - Food Science and Technology, 84, 579–585. https://doi.org/10.1016/j.lwt.2017.06.016.
Latham, M. J., & Wolin, M. J. (1977). Fermentation of cellulose by Ruminococcus flavefaciens in the presence and absence of Methanobacterium ruminantium. Applied and Environmental Microbiology, 34(3), 297–301. https://doi.org/10.1128/aem.34.3.297-301.1977.
Li, X. M., Tian, S. L., Pang, Z. C., Shi, J. Y., Feng, Z. S., & Zhang, Y. M. (2009). Extraction of Cuminum cyminum essential oil by combination technology of organic solvent with low boiling point and steam distillation. Food Chemistry, 115(3), 1114–1119. https://doi.org/10.1016/j.foodchem.2008.12.091.
Monteschio, J. O., Souza, K. A., Vital, A. A. C. P., Guerrero, A., Valero, M. V, Kempinski, E. M. B. C., Barcelos, V. C., Nascimento, K. F., & Prado, I. N. (2017). Clove and rosemary essential oils and encapsuled active principles (eugenol, thymol and vanillin blend) on meat quality of feedlot-finished heifers. Meat Science, 130, 50–57. https://doi.org/10.1016/j.meatsci.2017.04.002.
Monteschio, J. O., Vargas Junior, F. M., Almeida, F. L. A., Pinto, L., Kaneko, I. N., Almeida, A. A., Freitas, L. W., Alves, S. P., Bessa, R. J. B., & Prado, I. N. (2019). The effect of encapsulated active principles (eugenol, thymol and vanillin) and clove and rosemary essential oils on the structure, collagen content, chemical composition and fatty acid profile of Nellore heifers muscle. Meat Science, 155, 27–35. https://doi.org/10.1016/j.meatsci.2019.04.019.
Nikaido, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews, 67(4), 593–656. https://doi.org/http://dx.doi.org/10.1128/MMBR.67.4.593–656.2003.
Nikmaram, N., Budaraju, S., Barba, F. J., Lorenzo, J. M., Cox, R. B., Mallikarjunan, K., & Roohinejad, S. (2018). Application of plant extracts to improve the shelf-life, nutritional and health-related properties of ready-to-eat meat products. Meat Science, 145, 245–255. https://doi.org/10.1016/j.meatsci.2018.06.031.
O’Herrin, S. M., & Kenealy, W. R. (1993). Glucose and carbon dioxide metabolism by Succinivibrio dextrinosolvens. Applied and Environmental Microbiology, 59(3), 748–755. https://doi.org/10.1128/aem.59.3.748-755.1993.
Olagaray, K. E., & Bradford, B. J. (2019). Plant flavonoids to improve productivity of ruminants–A review. Animal Feed Science and Technology, 251, 21–36. https://doi.org/10.1016/j.anifeedsci.2019.02.004.
Ornaghi, M. G., Guerrero, A., Vital, A. C. P., Souza, K. A., Passetti, R. A. C., Mottin, C., Castilho, R. C., Sañudo, C., & Prado, I. N. (2020). Improvements in the quality of meat from beef cattle fed natural additives. Meat Science, 163, 1–9. https://doi.org/10.1016/j.meatsci.2020.108059.
Ornaghi, M. G., Passetti, R. A. C., Torrecilhas, J. A., Mottin, C., Vital, A. C. P., Guerrero, A., Sañudo, C., Campo, M. M., & Prado, I. N. (2017). Essential oils in the diet of young bulls: Effect on animal performance, digestibility, temperament, feeding behaviour and carcass characteristics. Animal Feed Science and Technology, 234, 274–283. https://doi.org/10.1016/j.anifeedsci.2017.10.008.
Paster, B. J., & Canale-Parola, E. (1985). Treponema saccharophilum sp. nov., a large pectinolytic spirochete from the bovine rumen. Applied and Environmental Microbiology, 50(2), 212–219. https://doi.org/10.1128/aem.50.2.212-219.1985.
Patra, A. K., & Saxena, J. (2009). Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie Van Leeuwenhoek, 96(4), 363–375.
Patra, A. K., & Saxena, J. (2010). A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen. Phytochemistry, 71(11–12), 1198–1222. https://doi.org/10.1016/j.phytochem.2010.05.010.
Pereira A.S. et al. (2018). Metodologia da pesquisa científica. [eBook]. Santa Maria. Ed. UAB/NTE/UFSM. Available at: https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_Metodologia-Pesquisa-Cientifica.pdf?sequence=1
Radünz, M., Trindade, M. L. M., Camargo, T. M., Radünz, 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. https://doi.org/10.1016/j.foodchem.2018.09.173.
Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., & Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine, 26(9), 1231–1237.
Ricke, S. C. (2003). Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poultry Science, 82(4), 632–639. https://doi.org/10.1093/ps/82.4.632.
Rivaroli, D. C., Guerrero, A., Valero, M. V., Zawadzki, F., Eiras, C. E., Campo, M. D. M., Sañudo, C., Jorge, A. M., & Prado, I. N. (2016). Effect of essential oils on meat and fat qualities of crossbred young bulls finished in feedlots. Meat Science, 121, 278–284. https://doi.org/10.1016/j.meatsci.2016.06.017.
Russell, J B, & Hino, T. (1985). Regulation of lactate production in Streptococcus bovis: a spiraling effect that contributes to rumen acidosis. Journal of Dairy Science, 68(7), 1712–1721. https://doi.org/10.3168/jds.S0022-0302(85)81017-1.
Russell, J B, & Strobel, H. J. (1989). Effect of ionophores on ruminal fermentation. Applied and Environmental Microbiology, 55(1), 1–6. https://doi.org/10.1128/aem.55.1.1-6.1989.
Russell, James B, & Rychlik, J. L. (2001). Factors that alter rumen microbial ecology. Science, 292(5519), 1119–1122. https://doi.org/http://doi.org/10.1126/science.1058830.
Saavedra, M. J., Borges, A., Dias, C., Aires, A., Bennett, R. N., Rosa, E. S., & Simões, M. (2010). Antimicrobial activity of phenolics and glucosinolate hydrolysis products and their synergy with streptomycin against pathogenic bacteria. Medicinal Chemistry, 6(3), 174–183. https://doi.org/10.2174/1573406411006030174.
Sánchez, E., García, S., & Heredia, N. (2010). Extracts of edible and medicinal plants damage membranes of Vibrio cholerae. Applied and Environmental Microbiology, 76(20), 6888–6894. https://doi.org/10.1128/AEM.03052-09.
Sary, C., Carbonera, F., Silva, M. C. D., Oliveira, M., Lewandowski, V., Todesco, H., Visentainer, J. V., Prado, I. N., & Ribeiro, R. P. (2019). Effect of clove (Eugenia caryophyllus) and cinnamon (Cinnamomum zeylanicum) essential oils in Nile tilapia diets on performance, antioxidant power and lipid oxidation in fillets. Aquaculture Research, 50(2). https://doi.org/10.1111/are.13944.
Schäberle, T. F., & Hack, I. M. (2014). Overcoming the current deadlock in antibiotic research. Trends in Microbiology, 22(4), 165–167. https://doi.org/10.1016/j.tim.2013.12.007.
Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16(3), 144–158.
Souza, K. A., Monteschio, J. O., Mottin, C., Ramos, T. R., Pinto, L. A. M., Eiras, C. E., Guerrero, A., & Prado, I. N. (2019). Effects of diet supplementation with clove and rosemary essential oils and protected oils (eugenol, thymol and vanillin) on animal performance, carcass characteristics, digestibility, and ingestive behavior activities for Nellore heifers finished in feedl. Livestock Science, 220, 190–195. https://doi.org/10.1016/j.livsci.2018.12.026.
Stewart, C. S., Flint, H. J., & Bryant, M. P. (2012). The rumen bacteria. In P. N. Hobson & C. S. Stewart (Eds.), Rumen microbial ecosystem (2nd ed., Vol. 1, pp. 10–72). Blackie Academic & Professional.
Teixeira, B., Marques, A., Ramos, C., Neng, N. R., Nogueira, J. M. F., Saraiva, J. A., & Nunes, M. L. (2013). Chemical composition and antibacterial and antioxidant properties of commercial essential oils. Industrial Crops and Products, 43, 587–595. https://doi.org/10.1016/j.indcrop.2012.07.069.
Valero, M. V, Farias, M. S., Zawadzki, F., Prado, R. M., Fugita, C. A., Rivaroli, D. C., Ornaghi, M. G., & Prado, I. N. (2016). Feeding propolis or essential oils (cashew and castor) to bulls: performance, digestibility, and blood cell counts. Revista Colombiana de Ciencias Pecuarias, 29(1), 33–42.
Vignolo, R., & Naughton, F. (1991). Castor: a new sense of direction. Inform, 2(8), 692–699.
Vital, A. C. P., Guerrero, A., Kempinski, E. M. B. C., Monteschio, J. O., Sary, C., Ramos, T. R. R., Campo, M. ., & Prado, I. N. (2018). Consumer profile and acceptability of cooked beef steks with edible and active coating containing oregano and rosemary essential oils. Meat Science, 143, 153–158. https://doi.org/10.1016/j.meatsci.2018.04.035.
Vital, A. C. P., Guerrero, A., Monteschio, J. D. O., Valero, M. V., Carvalho, C. B., Abreu Filho, B. A., Madrona, G. S., & Prado, I. N. (2016). Effect of edible and active coating (with rosemary and oregano essential oils) on beef characteristics and consumer acceptability. PLoS ONE, 11(8). https://doi.org/10.1371/journal.pone.0160535.
Wallace, R. J., Onoder, R., & Cotta, M. A. (2012). Metabolism of nitrogen-containing compounds. In P. N. Hobson & C. S. Stewart (Eds.), Rumen microbial ecosystem (2nd ed., Vol. 1, pp. 283–328). Blackie Academic & Professional.
Zhu, Q. Y., Hackman, R. M., Ensunsa, J. L., Holt, R. R., & Keen, C. L. (2002). Antioxidative activities of oolong tea. Journal of Agricultural and Food Chemistry, 50(23), 6929–6934. https://doi.org/10.1021/jf0206163.
Zotti, C. A., Silva, A. P., Carvalho, R., Marino, C. T., Rodrigues, P. H. M., Silva, L. F. P., McAllister, T. A., & Leme, P. R. (2017). Monensin and a blend of castor oil and cashew nut shell liquid used in a high-concentrate diet abruptly fed to Nellore cattle. Journal of Animal Science, 95(9), 4124–4138. https://doi.org/10.2527/jas2017.1580.
Zuzarte, M., Gonçalves, M. J., Cavaleiro, C., Cruz, M. T., Benzarti, A., Marongiu, B., Maxia, A., Piras, A., & Salgueiro, L. (2013). Antifungal and anti-inflammatory potential of Lavandula stoechas and Thymus herba-barona essential oils. Industrial Crops and Products, 44(0), 97–103. https://doi.org/10.1016/j.indcrop.2012.11.002.
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Copyright (c) 2021 Aylle Medeiros Matos; Mariana Garcia Ornaghi; Venício Macêdo Carvalho; Vicente Alfonso Diaz Avila; Edinéia Bonin; Ricardo de Araújo Castilho; Anderson Valdiney Gomes Ramos; Debora Cristina Baldoqui; Rodolpho Martin do Prado; Ivanor Nunes do Prado
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