Effect of essential oils and major compound on Clostridium botulinum endospores inoculated in meat product

Authors

DOI:

https://doi.org/10.33448/rsd-v11i7.29854

Keywords:

Clostridium botulinum; Endospore; Essential oil; Foodborne pathogen; Mortadella; Natural preservative.

Abstract

Mortadella is a widely consumed product due to its sensory characteristics, however, nitrite is used as a preservative and this synthetic additive has been linked to some diseases. In this sense, this study aimed to evaluate the antimicrobial effect of oregano and clove essential oils, besides the major compound carvacrol on Clostridium botulinum endospores inoculated in mortadella and the physicochemical effect of them on the product. The minimum sporicidal concentration of the essential oils and the major compound was determined by the broth microdilution method and the best results used to prepare the mortadellas containing 0 and 150 ppm of nitrite. All the evaluated treatments showed decrease of nitrite levels over time and lower lipid oxidation. The combinations of essential oils and carvacrol did not affect the mortadella color in the final product. In the mortadellas added of combinations of essential oils and of major compound there was reduction in the population of C. botulinum, whereas in mortadella without essential oils the antimicrobial effect was attributed only to the nitrite. The results are promising and suggest the use of clove and oregano essential oils together with carvacrol compound in meat sausages as a natural preservative and action against foodborne pathogens.

References

Abdollahi, M., Rezaei, M. & Farzi, G. (2014). Influence of chitosan/ clay functional bionanocomposite activated with rosemary essential oil on the shelf life of fresh silver carp. Inernational Journal of Food Science and Technology, 49 (3), 811–818. doi:10.1111/ijfs.12369

Ajourloo, M., Khanjari, A., Misaghi, A., Basti, A. A., Kamkar, A., Yadegar, F., Gholami, F., Khansavar, F. & Fallah, f. (2021). Combined effects of Ziziphora clinopodioides essential oil and lysozyme to extend shelf life and control Listeria monocytogenes in Balkan-style fresh sausage. Food Science and Nutrition. 9 (3), 1665–1675. doi: 10.1002/fsn3.2141

Alahakoon, A. U., Jayasena, D. D., Ramachandra, S. & Jo, C. (2015). Alternatives to nitrite in processed meat: Up to date. Trends in Food Science and Technology, 45 (1), 37–49. doi: 10.1016/j.tifs.2015.05.008

Al-shuibi, A. M. & Al-abdullah, B. M. (2002). Substitution of nitrite by sorbate and the effect on properties of mortadella. Meat Science, 62 (4), 473-478. doi: 10.1016/S0309-1740(02)00041-4

Angelo, P. M. & Jorge, N. (2007). Phenolic compounds in food: a brief review. Revista Instituto Adolfo Lutz 66 (1), 232-240. Retrieved from https://pesquisa.bvsalud.org/portal/resource/pt/vti-453047

Arsi, K., Donoghue, A. M., Venkitanarayanan, K., Kollanoor‐johny, A., Fanatico, A. C., Blore, P. J & Donoghue, D. J. (2014). The efficacy of the natural plant extracts, thymol and carvacrol against Campylobacter colonization in broiler chickerns. Journal of Food Safety, 34 (4), 321-325. doi: 10.1111/jfs.12129

Asensio, C. M., Gallucci, N., Oliva, M. M., Demo, M. S. & Grosso, N.R. (2014). Sensory and bio-chemical preservation of ricotta cheese using natural products. International Journal of Food Science and Technoogy, 49 (12), 2692–2702. doi: 10.1111/ijfs.12604

AOAC. (1998). Official Methods of Analysis. Maryland, USA: Association of Official Analytical Chemists.

Bakkali, F., Averbecka, S., Averbecka, D & Idaomarb, M. (2008). Biological effects of essential oils. Food Chemistrt and Toxicological 46 (2), 446–475. doi: 10.1016/j.fct.2007.09.106

Bassanetti, I., Carcelli, M., Buschini, A., Montalbano, S., Leonardi, G., Pelagatti, P., Tosi, G., Massi, P., Fiorentini, L. & Rogolino, D. (2017). Investigation of antibacterial activity of new classes of essential oils derivatives. Food Control 73, 606-612. doi: 10.1016/j.foodcont.2016.09.010

Blanco-lizarazo, C. M., Betancourt-cortés, R., Lombana, A., Carrillo-Castro, k. & Sotelo-díaz, I. (2017). Listeria monocytogenes behaviour and quality attributes during sausage storage affected by sodium nitrite, sodium lactate and thyme essential oil. Food Science and Technology International, 23 (3), 277–288. doi: 10.1177/1082013216686464

Burt, S. (2004). Essential oils: Their antimicrobial properties and potential applications in foods: A review. International Journal of Food Microbiology, 94 (3), 223–253. doi: 10.1016/j.ijfoodmicro.2004.03.022

Cassens, R. G. (1997). Composition and safety of cured meats in the USA. Food Chemistry, 59 (4), 561-566. doi: 10.1016/S0308-8146(97)00007-1

Chaibi, A., Ababoucha, I. H., Belasri, K., Boucetta, L. & Busta, F. F. (1997). Inhibition of germination and vegetative growth of Bacillus cereus T and Clostridium botulinum 62 A spores by essential oils. Food Microbiology, 14 (2), 161-174. doi: 10.1006/fmic.1996.0075

Chen, L. & Opara, U.L. (2013). Approaches to analysis and modeling texture in fresh and processed foods – A review. Journal of food Engineering, 119 (3), 497–507. doi: 10.1016/j.jfoodeng.2013.06.028

Cheng, J-H, Wang, S-T. & Wockerman, H. (2007). Lipid oxidation and color change of salted pork patties. Meat Science, 75 (1), 71-77. doi: 10.1016/j.meatsci.2006.06.017

Decker, E. A. (1997). Phenolics: prooxidants or antioxidants? Nutrition Reviews, 55 (11) 396-407. doi: 10.1111/j.1753-4887.1997.tb01580.x

Delaquis, P. J., Stanich, K., Girard, B & Mazza, G. (2002). Antimicrobial activity of individual and mixed fractions of dill, cilantro, coriander and eucalyptus essential oils. International Journal of Food Microbiology, 74 (1-2), 101–109. doi: 10.1016/s0168-1605(01)00734-6

Dias. N. A., Rodrigues, I. T. S., Palhares, P. C., Ramos, E. M. & Piccoli, R. H. (2015). Antimicrobial activity of essential oils on Clostridium perfringens type A inoculated in mortadella. Journal of Food Safety, 35(4), 466–472. doi: 10.1111/jfs.12196

Dimitrijević, S. I., Mihajlovski, K. R., Antonović, D. G., Milanović-Stevanović, M. R. & Mijin, D. Z. (2007). A study of the synergistic antilisterial effects of a sub-lethal dose of lactic acid and essential oils from Thymus vulgaris L., Rosmarinus officinalis L. and Origanum vulgare L. Food Chemistry, 104(2), 774–782. doi: 10.1016/j.foodchem.2006.12.028

Dong, Q-L., Tu, K., Guo, L-Y., Yang, J-L., Wang, H. & Chen, Y-Y. (2007). The effect of sodium nitrite on the textural properties of cooked sausage during cold storage. Journal of Texture Studies, 38 (5), 537–554. doi: 10.1111/j.1745-4603.2007.00112.x

Dutra, M. P., Ramos, E. M., Ramos, A. L. S., Fontes, P. R., Cardoso, G. P. & Leal, A. S. (2011). Gamma radiation and storage time on lipidic oxidation, color, heme pigments and residual nitrite of bologna-type sausages formulated with different nitrite additions. Ciência Rural 41(12), 2203-2209. doi: 10.1590/S0103-84782011005000143

Dutra, M. P., Aleixo, G. C., Ramos, A. L. S., Silva, M. H. L., Pereira, M. T., Piccoli, R. H & Ramos, E.M. (2016). Use of gamma radiation on control of Clostridium botulinum in mortadella formulated with different nitrite levels. Radiation Physics and Chemistry, 119, 125-129. doi: 10.1016/j.radphyschem.2015.10.008

Fernandes, R. V. B., Guimarães, I. C., Ferreira, C. L. R., Botrel, D. A., Borges, S. V. & Souza, A. U. (2015). Microencapsulated rosemary (rosmarinusofficinalis) essential oil as a biopreservativein minas frescal cheese. Journal of Food Processing and Preservation, 41 (1), 1-9. doi: 10.1111/jfpp.12759

Ghabraie, M., Vu, K. D., Tnani, S. & Lacroix, M. (2016). Antibacterial effects of 16 formulations and irradiation against Clostridium sporogenes in a sausage model. Food Control, 63, 21-27. doi: 10.1016/j.foodcont.2015.11.019

Hoffmann, F. L., Souza, S. J. F., Gracia-Cruz, C. H., Vinturim, T. M. & Dutra, A. L. (1999). Determinação da atividade antimicrobiana in vitro de quatro óleos essenciais de condimentos e especiarias. Boletim do Centro de Pesquisa de Processamento de Alimentos, 17 (1), 11-20. doi: 10.5380/cep.v17i1.13794

Hughes. E., Cofrades, S. & Troy, D. J. (1997). Effects of fat level, oat fibre and carrageenan on frankfurters formulated with 5, 12 and 30% Fat. Meat Science, 45, 273-281. doi: 10.1016/S0309-1740(96)00109-X

Juneja, V. K. & Friedman, M. (2007). Carvacrol, Cinnamaldehyde, Oregano Oil, and Thymol Inhibit Clostridium perfringens Spore Germination and Outgrowth in Ground Turkey during Chilling. Journal of Food Protection, 70 (1), 218-222. doi: 10.4315/0362-028X-70.1.218

Kim, S. A. & Rhee, M. S. (2016). Highly enhanced bactericidal effects of medium chain fatty acids (caprylic, capric and lauric acid) combined with edible plant essential thymol and vanillin against Escherichia coli. Food Control, 60, 447-454. doi: 10.1016/j.foodcont.2015.08.022.

Marino, M., Bersani, C. & Comi, G. (2001). Impedance measurements to study theantimicrobial activity of essential oils from Lamiaceae and Compositae. International Journal of Food Microbiology, 67, 187-195. doi: 10.1016/S0168-1605(01)00447-0

Misaghi, A. & Basti, A. A. (2007). Effects of Zataria multiflora Boiss. essential oil and nisin on Bacillus cereus ATCC 11778. Food Control 18 (9), 1043–1049. doi: 10.1016/j.foodcont.2006.06.010

Murray, P. R. (1999). Manual of Clinical Microbiology. Washington, USA: American Society for Microbiology.

Oliveira, J. M., Araújo, W. M. C. & Borgo, L. A. (2005). Quantification of Nitrate and Nitrite in Fresh Sausage. Journal of Food Science and Technology, 25 (4), 736-742. doi: 10.1590/S0101-20612005000400018

Oliveira, T. L. C. (2012). Antioxidant effects of Satureja montana L. essential oil on TBARS and color of mortadella-type sausages formulated with different levels of sodium nitrite. LWT Food Science and Technology, 45(2), 204-212. doi: 10.1016/j.lwt.2011.09.006

Ouattara, B., Simard, R. E., Holley, R. A., Piette, G. J-P. & Bégin, A. (1997). Antibacterial activity of selected fatty acids and essential oils against six meat spoilage organisms. International Journal of Food Microbiology, 37 (2-3), 155-162. doi: 10.1016/S0168-1605(97)00070-6

Pei, R., Zhou, F., Ji, B. & Xu, J. (2009). Evaluation of Combined Antibacterial Effects of Eugenol, Cinnamaldehyde, Thymol, and Carvacrol against E. coli with an Improved Method. Journal of Food Science, 74 (7), 379–383. doi: 10.1111/j.1750-3841.2009.01287.x

Pinelli, J. J., Martins, H. H. A., Guimarães, A. S., Isidoro, S. R., Gonçalves, M. C., Moraes, T. S. J., Ramos, E. M. & Piccoli, R. R. (2021). Essential oil nanoemulsions for the control of Clostridium sporogenes in cooked meat product: An alternative? LWT Journal of Food Science and Technology, 143, 1-10. doi: 10.1016/j.lwt.2021.111123

Pinheiro, P. F., Costa, A. V., Alves, T. A., Galter, I. N., Pinheiro, C. A., Pereira, A. F., Oliveira, C. M. R. & Fontes, M. M. P. (2015). Phytotoxicity and cytotoxicity of essential oil from leaves of Plectranthus amboinicus, carvacrol, and thymol in plant bioassays. J. Agric. Food Chem. 63 (41), 8981-8990. doi: 10.1021/acs.jafc.5b03049

Peck, M. V., Plowman, J., Aldus, C. F., Wyatt, G. M., Izurieta, W. P., Stringer, S. C. & Barker, G. C. (2010). Development and application of a new method for specific and sensitive enumeration of spores of nonproteolytic Clostridium botulinum types B, E and F in foods and food materials. Applied Environental Microbiology, 76(19), 6607-6614. doi: 10.1128/AEM.01007-10

Raharjo, S., Sofos, J. N. & Schmidt, G. R. (1992). Improved speed, specificity, and limit of determination of an aqueouso acid extraction thiobarbituric acid-C18 method for measuring lipid peroxidation in beef. Journal of Agricultural and Food Chemistry, 40, 2182-2185. doi: 10.1021/jf00023a027

Ramos, E. M. & Gomide, L. A. M. (2017). Avaliação da Qualidade de Carnes: Fundamentos e Metodologias. Viçosa, BR: UFV.

Santiesteban-López, A., Palou, E. & López-Malo, A. (2007). Susceptibility of food-borne bacteria to binary combinations of antimicrobials at selected awand pH. Journal of Applied Microbiology, 102 (2), 486–497. doi: 10.1111/j.1365-2672.2006.03092.x

Sharma, H., Mendiratta, S. K., Agarwal, R. K. & Gurunathan, K. (2020). Bio-preservative effect of blends of essential oils: natural antioxidant and anti-microbial agents for the shelf life enhancement of emulsion based chicken sausages. Journal of Food Science and Technology 57, 3040–3050. doi: 10.1007/s13197-020-04337-1

Sharma, S. K., Ferreira, J. L., Eblen, B. S. & Whiting, R. C. (2006). Detection of type A, B, E, and F Clostridium botulinum neurotoxins in foods by using an amplified enzyme-linked immunosorbent assay with digoxigenin-labeled antibodies. Applied Environmental Microbiology, 72 (2), 1231-1238. doi: 10.1128/AEM.72.2.1231-1238.2006

Šojića, B., Pavlića. B., Ikonić, P., Tomovića, V., Ikonića, B., Zekovića, Z., Kocić-Tanackova, K., Jokanovića, M., Skaljaca, S. & Ivić, M. (2019). Coriander essential oil as natural food additive improves quality and safety of cooked pork sausages with different nitrite levels. Meat Science, 157, 1-8. doi: 10.1016/j.meatsci.2019.107879

Teixeira, L. V. (2009). Sensory Analysis in the Food Industry. Journal of Candido Tostes Dairy Institute, 64 (366), 12-21. Retrieved from https://www.revistadoilct.com.br/rilct/article/view/70/76

Terra, N. N. (2009). Use of liquid whey in the preparation of mortadella. Ciência Rural 39, 885-890. DOI: 10.1590/S0103-84782009000300038

Tomovic, V., Sojic, B., Savanovic, J., Kocic-Tanackov, S., Pavlic, B., Jokanovic, M., Oordevic, V., Parunovic, N., Martinovic, A. & Vujadinovic, D. (2020). New Formulation towards Healthier Meat Products: Juniperus communis L. Essential Oil as Alternative for Sodium Nitrite in Dry Fermented Sausages. Foods 9 (8), 1-17. doi: 10.3390/foods9081066

Toldrá, F. (2014). Handbook of Fermented Meat and Poultry. United States, USA: John Wiley & Sons Inc.

Ultee, A., Slump, R. A., Steging, G. & Smid, E. J. (2000). Antimicrobial Activity of Carvacrol toward Bacillus cereus on Rice. Journal of Food Protection, 63 (5), 620–624. doi: 10.4315/0362-028x-63.5.620

Viuda-Martos, M., Ruiz-Navajas, Y., Fernández-López, J. & Pérez-Álvarez, J. A. (2010). Effect of orange dietary fibre, oregano essential oil and packaging conditions on shelf-life of bologna sausages. Food Control, 21 (4), 436-443. doi: 10.1016/j.foodcont.2009.07.004

Zhang, X., Wang, H., Li, X., Sun, Y., Pan, D., Wang, Y & Cao, J. (2019). Effect of cinnamon essential oil on the microbiological and physiochemical characters of fresh Italian style sausage during storage. Animal Science Journal, 90 (3), 435–444. doi: 10.1111/asj.13171

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Published

28/05/2022

How to Cite

ALEIXO, G. de C.; SILVA, M. S.; MARTINS, H. H. de A.; CARVALHO, R. M. B.; RAMOS, E. M. .; PICCOLI, R. H. Effect of essential oils and major compound on Clostridium botulinum endospores inoculated in meat product. Research, Society and Development, [S. l.], v. 11, n. 7, p. e38811729854, 2022. DOI: 10.33448/rsd-v11i7.29854. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/29854. Acesso em: 25 apr. 2024.

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Agrarian and Biological Sciences