Viability of Clostridium difficile in mortadella with added essential oils and reduced sodium nitrite content
DOI:
https://doi.org/10.33448/rsd-v11i9.31106Keywords:
Clostridium difficile; Essential oils; Food safety; Meat product; Natural additives.Abstract
The effects of additioning essential oil mixtures and reducing the sodium nitrite content (75 ppm) on Clostridium difficile inoculated in mortadellas and on the product’s technological characteristics were evaluated. 15 essential oils were tested preliminarily, but only four were selected. The minimum bactericidal concentrations found were 1.2 % for Ocimum basilicum, 0.3 % for Origanum vulgare and for Thymus vulgaris and 0.15 % for Litsea cubeba. There wasn`t significant difference in viable cell growth between treatments and the control; however, there was an increase in viable cells of approximately 2.5 log10 MPN/g after the fifth day. Combinations of oils didn`t prevent sporulation, however a synergistic effect was observed in vitro. There was a reduction in pH during storage and a greater amount of residual nitrite for the F1 treatment (Origanum vulgare (0.2 %); Thymus vulgaris (0.05 %) and Litsea cubeba (0.025 %), with 10.23 ppm, and reduction of residual nitrite during the storage period from 18.75 ppm on the first day of storage to 5.11 ppm on the last. No significant changes were observed in the technological characteristics of the product with the analyzed treatments.
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. 10.1111/ijfs.12369
Adams, R. P. (2007). Identification of essential oils components by gás chromatog- raphy/quadrupole mass spectroscopy (4th ed.). Carol Stream: Allured.
Aleixo, G. C., Silva, M. S., Martins, H. H, A., Carvalho, R. M. B., Ramos, E. M. & Piccoli, R. H. (2022). Effect of essential oils and major compound on Clostridium botulinum endospores inoculated in meat product. Research, Society and Development, 11(1), 1-13. http://dx.doi.org/10.33448/rsd-v11i1.XXXXX
Aloui, H. & Khwaldia, K. (2016). Natural antimicrobial edible coatings for microbial safety and food quality enhancement. Comprehensive Reviews in Food Science and Food Safety, 15 (6), 1080-1103. https://doi.org/10.1111/1541-4337.12226
Alves, E. (2004). Introdução à microscopia eletrônica de varredura e de transmissão. FAEPE-UFLA.
AOAC. (1995). Association of Official Analytical Chemists. Official methods of analysis of AOAC international. Virginia, 1995. v.16.
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. 10.1111/ijfs.12604
Bakkali, F., Averbeck, S., Averbeck, D. & Idaomar, M. (2008). Biological effects of essential oils – A review. Food and Chemical Toxicology, 46 (2), 446–475. https://doi.org/10.1016/j.fct.2007.09.106
Borch, E., Kant-Muermans, M. L & Blixt, Y. (1996). Bacterial spoilage of meat and cured meat products. International Journal of Food Microbiology, 33 (1), 103-120. https://doi.org/10.1016/0168-1605(96)01135-X
Burt, S. (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
Calo, J. R., Crandall, P. G., O’ Bryan, C. A. & Ricke, S. C. (2015). Essential oils as antimicrobials in food systems – A review. Food Control, 54, 111-119. https://doi.org/10.1016/j.foodcont.2014.12.040
Carson, C. F., Mee, B. J. & Riley, T. V. (2002). Mechanism of action of Melaleuca alternifolia (Tea Tree) Oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrobial Agents and Chemotherapy, 46 (6), 1914–1920. https://doi.org/10.1128/AAC.46.6.1914-1920.2002
Cassens, R. G. (1997). Residual nitrite in cured meat. Food Technology, 51(2), 53–55.
Chen, W. & Viljoen, A. M. (2010). Geraniol—a review of a commercially important fragrance material. South African Journal of Botany, 76 (4), 643-651. https://doi.org/10.1016/j.sajb.2010.05.008
Deans, S. G. & Ritche, 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
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. https://doi.org/10.1016/S0168-1605(01)00734-6
de Oliveira, T. L. C., de Carvalho, S. M., Soares, R. A., Andrade, M. A., Cardoso, M. D. G., Ramos, E. M. & Piccoli, R. H. (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. https://doi.org/10.1016/j.lwt.2011.09.006
Dias, N. A. A., Rodrigues, L. T. S., Palhares, P., 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. https://doi.org/10.1111/jfs.12196
Dutra, M. P., Aleixo, G. C., Ramos, A. D. 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. https://doi.org/10.1016/j.radphyschem.2015.10.008
Dutra, M. P., Ramos, E. M., Cardoso, G. P. & Leal, A. S. (2011). Radiação gama e tempo de armazenamento sobre a oxidação lipídica , cor objetiva , pigmentos heme e nitrito residual de mortadelas elaboradas com diferentes níveis de nitrito. Ciência Rural, 41(12), 2203-2209. https://doi.org/10.1590/S0103-84782011005000143
Feiner, G. (2006). Meat products handbook practical science and technology. Boca Raton: CRC, p. 627.
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. 10.1111/jfpp.12759
Fiorda, F. A. & de Siqueira, M. I. D. (2009). Avaliação do pH e atividade de água em produtos cárneos. EVS- Revista de Ciências Ambientais e Saúde, 36 (4), 817-826. http://dx.doi.org/10.18224/est.v36i4.1132
Giarratana, F., Muscolino, D., Ragonese, C., Beninati, C., Sciarrone, D., Ziino, G. & Panebianco, A. (2016). Antimicrobial activity of combined thyme and rosemary essential oils against Listeria monocytogens in Italian mortadella packaged in modified atmosphere: Thyme & Rosemary EOs vs L. monocytogenes. Journal of Essential Oil Research, 28 (6), 467-474. https://doi.org/10.1080/10412905.2016.1165744
Gill, A. O., Delaquis, P., Russo, P. & Holley, R. A. (2002). Evaluation of antilisterial action of cilantro oil on vacuum packed ham. International Journal of Food Microbiology, 73 (1), 83-92. https://doi.org/10.1016/S0168-1605(01)00712-7
Glass, K. A. & Johnson, E. A. (2004). Antagonistic effect of fat on the antibotulinal activity of food preservatives and fatty acids. Food Microbiology, 21 (6), 675–682. https://doi.org/10.1016/j.fm.2004.03.002
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/10.1016/j.foodchem.2009.03.058
Grosso, C., Ferraro, V., Figueiredo, A. C., Barroso, J. G., Coelho, J. A. & Palavra, A. M. (2008). Supercritical carbon dioxide extraction of volatile oil from Italian coriander seeds. Food Chemistry, 111 (1), 197–203. https://doi.org/10.1016/j.foodchem.2008.03.031
Gutierrez, J., Barry-Ryan, C. & 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
Honikel, K. O. (2008). The use and control of nitrate and nitrite for the processing of meat products. Meat Science, 78 (1-2), 68–76. https://doi.org/10.1016/j.meatsci.2007.05.030
Hoover, D. G. & Rodriguez-Palacios, A. (2013). Transmission of Clostridium difficile in foods. Infectious Disease Clinics, 27(3), 675–685. https://doi.org/10.1016/j.idc.2013.05.004
Ismaiel, A. A. & Pierson, M. D. (2006). Inhibition of growth and germination of C. botulinum 33 A, 40 B e 1623E by essential oil spices. Journal of Food Science, 55(6), 1676–1678. https://doi.org/10.1111/j.1365-2621.1990.tb03598.x
Jayasena, D. D. & Jo, C. (2013). Essential oils as potential antimicrobial agents in meat and meat products: A review. Trends in Food Science and Technology, 34 (2), 96–108. https://doi.org/10.1016/j.tifs.2013.09.002
Karolyi, D. (2003). Cured meat and consumer health. Meso, 5 (5), 16-18.
Lambert, R. J. W., Skandamis, P.N., Coote, P. J. & 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 (3), 453–462. https://doi.org/10.1046/j.1365-2672.2001.01428.x
Liao, P. C., Yang, T. S., Chou, J. C., Chen, J., Lee, S. C., Kuo, Y. H. & Chao, L. K. P. (2015). Anti-inflammatory activity of neral and geranial isolated from fruits of Litsea cubeba Lour. Journal of Functional Foods, 19, 248-25. https://doi.org/10.1016/j.jff.2015.09.034
Martins, H. H. A., Simões, L. A., Isidoro, S. R., Nascimento, S. S., Alcântara, J. P. Ramos, E. M. & Piccoli, R. H. (2021). Preservative of essencial oil blends: Control of Clostidium perfringens Type a in mortadella. Brazilian Archives of Bioloby, 64, 1-9. https://doi.org/10.1590/1678-4324-2021200106
Mejlholm, O. & Dalgaard, P. (2002).Antimicrobial effect of essential oils on the seafood spoilage micro-organism Photobacterium phosphoreum in liquid media and fish products. Letters in Applied Microbiology, 34 (1), 27–31. https://doi.org/10.1046/j.1472-765x.2002.01033.x
Mitchell, W. J. (2001). General biology and physiology. In: Bahl, H., Dürre, P. Clostridia: biotechnology and medical applications. New York: J. Wiley.
Nazer, A. I., Kobilinsky, A., Tholozan, J. L. & Dubois-Brissonnet, F. (2005). Combinations of food antimicrobials at low levels to inhibit the growth of Salmonella sv. Typhimurium: a synergistic effect? Food Microbiology, 22 (5), 391-398. https://doi.org/10.1016/j.fm.2004.10.003
Nazzaro, F., Fratianni, F., de Martino, L., Coppola, R. & de Feo, V. (2013). Effect of essential oils on pathogenic bacteria. Pharmaceuticals (Basel), 6 (12), 1451–1474. https://doi.org/10.3390/ph6121451
NCCLS (National Committee for Clinical Laboratory Standards) (2019). Performance standards for antimicrobial susceptibility testing, 29th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
Oliveira, T. L. C., Soares, R. A., Ramos, E. M., Cardoso, M. G., Alves, E. & Piccoli, R. H. (2011). Antimicrobial activity of Satureja montana L. essential oil against Clostridium perfringens type A inoculated in mortadella-type sausages formulated with different levels of sodium nitrite. International Journal of Food Microbiology, 144 (3), 546–555. https://doi.org/10.1016/j.ijfoodmicro.2010.11.022
Oliveira, T. L. C., Soares, R. D. A. & Piccoli, R. H. (2013). A Weibull model to describe antimicrobial kinetics of oregano and lemongrass essential oils against Salmonella Enteritidis in ground beef during refrigerated storage. Meat Science, 93 (3), 645–651. https://doi.org/10.1016/j.meatsci.2012.11.004
Oussalah, M., Caillet, S., Saucier, L. & Lacroix, M. (2007). Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157 : H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control, 18 (5), 414–420. https://doi.org/10.1016/j.foodcont.2005.11.009
Parthasarathy, D. K. & Bryan, N. S. (2012). Sodium nitrite: The “cure” for nitric oxide insufficiency. Meat Science, 92 (3), 274-279. https://doi.org/10.1016/j.meatsci.2012.03.001
Pereira, A. D., Piccoli, R. H., Batista, N. N., Camargos, N. G. & Oliveira, M. M. M. (2014). Thermochemical inactivation of Escherichia coli, Staphylococcus aureus and Salmonella enterica Enteritidis by essencial oils. Ciência Rural, 44 (11), 2022–2028. https://doi.org/10.1590/0103-8478cr20140092
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. 10.1016/j.lwt.2021.111123
Rodríguez-Pardo, D., Mirelis, B. & Navarro, F. (2013). Infecciones producidas por Clostridium difficile. Enfermedades Infecciosas y Microbiologia Clinica, 31 (4), 254-263. https://doi.org/10.1016/j.eimc.2012.12.010
Rota, M. C., Herrera, A., Martínez, R. M., Sotomayor, J. A. & Jordán, M. J. (2008). Antimicrobial activity and chemical composition of Thymus vulgaris, Thymus zygis and Thymus hyemalis essential oils. Food Control, 19(7), 681–687. https://doi.org/10.1016/j.foodcont.2007.07.007
Rywotycki, R. (2002). The effect of selected functional additives and heat treatment on nitrosamine content in pasteurized pork ham. Meat Science, 60 (4), 335–339.https://doi.org/10.1016/S0309-1740(01)00138-3
Sebranek, J. G. & Bacus, J. N. (2007). Cured meat products without direct addition of nitrate or nitrite: what are the issues? Meat science, 77(1), 136-147. https://doi.org/10.1016/j.meatsci.2007.03.025
Scott, V. N., Anderson, J. E. & Wang, G. (2001). Mesophilic anaerobic sporeformers, In: Downes, F.P., Ito, K. (Eds.), Compendium of Methods for the Microbiological Examination of Foods, 4 ed. American Public Health Association, Washington, pp. 325–330.
Shelef, L.A. (1984). Antimicrobial effects of spices. Journal of Food Safety, 6 (1), 29-44. https://doi.org/10.1111/j.1745-4565.1984.tb00477.x
Stefanakis, M. K., Touloupakis, E., Anastasopoulos, E., Ghanotakis, D., Katerinopoulos, H. E. & Makridis, P. (2013). Antibacterial activity of essential oils from plants of the genus Origanum. Food Control, 34 (2), 539–546. https://doi.org/10.1016/j.foodcont.2013.05.024
Sunenshine, R. H. & McDonald, L. C. (2006). Clostridium difficile-associated disease: new challenges from an established pathogen. Cleveland Clinic Journal of Medicine, 73 (2), 187-197. Retrieved from https://www.sociedad-iih.cl/doc_biblioteca/consejos_guias/6-Clostridiumdifficile.pdf
Tajkarimi, M. M., Ibrahim, S. A. & Cliver, D. O. (2010). Antimicrobial herb and spice compounds in food. Food Control, 21 (9), 1199–1218. https://doi.org/10.1016/j.foodcont.2010.02.003
Ultee, A. &Smid, E. J. (2001). Influence of carvacrol on growth and toxin production by Bacillus cereus. International Journal of Food Microbiology, 64 (3), 373–378. https://doi.org/10.1016/S0168-1605(00)00480-3
Vergis, J., Gokulakrishnan, P., Agarwal, R. K. & Kumar, A. (2015). Essential oils as natural food antimicrobial agents: a review. Critical Reviews in Food Science and Nutrition, 55 (10), 1320-1323. https://doi.org/10.1080/10408398.2012.692127
Viuda-Martos, M., Ruiz-Navajas, Y., Fernández-López, J. & Pérez-Álvarez, J. A. (2010). Effect of added citrus fibre and spice essential oils on quality characteristics and shelf-life of mortadella. Meat Science, 85 (3), 568–576. https://doi.org/10.1016/j.meatsci.2010.03.007
Weese, J. S. (2010). Clostridium difficile in food-innocent bystander or serious threat? Clinical Microbiology and Infection, 16 (1), 3–10. https://doi.org/10.1111/j.1469-0691.2009.03108.x
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Nayane Aparecida Araújo Dias; Juliana Junqueira Pinelli; Monique Suela Silva; Silas Rodrigo Isidoro ; Heloísa Helena de Abreu Martins; Michelle Carlota Gonçalves; Eduardo Mendes Ramos; Roberta Hilsdorf Piccoli

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.