Enterococcus faecium in artisanal ripening cheese: technological and safety aspects

Priscila Lima Magarotto de Paula; Marina Levorato de  Moraes; Janaína Schueler; Nathália Aparecida Andrade de  Souza; Márcia Cristina  Furlaneto; Luciana Furlaneto-Maia; Marly Sayuri Katsuda

doi:10.33448/rsd-v9i11.9452

Autores/as

Priscila Lima Magarotto de Paula Federal University of Technology https://orcid.org/0000-0002-8563-7099
Marina Levorato de Moraes Federal University of Technology https://orcid.org/0000-0002-1392-1357
Janaína Schueler Federal University of Technology https://orcid.org/0000-0001-9841-6757
Nathália Aparecida Andrade de Souza State University of Londrina https://orcid.org/0000-0001-7485-2829
Márcia Cristina Furlaneto State University of Londrina https://orcid.org/0000-0002-1188-1320
Luciana Furlaneto-Maia Federal University of Technology https://orcid.org/0000-0002-7164-3391
Marly Sayuri Katsuda Federal University of Technology https://orcid.org/0000-0003-2387-7895

DOI:

https://doi.org/10.33448/rsd-v9i11.9452

Palabras clave:

Sensibilidad a medicamentos; Actividad antagónica; Fermentación.

Resumen

Este trabajo tuvo como objetivo caracterizar propiedades tecnológicas del aislado Enterococcus faecium durante la maduración de quesos. El estudio evaluó el potencial tecnológico de seis aislados de E. faecium (EFM55, EFM67, EFM9A, EFM16A, EFM19A y EFM44) de quesos artesanales, según sus características probióticas y perspectiva tecnológica. En relación a la sensibilidad antimicrobiana, 71% de los E. faecium analizados fueron sensibles a todos los antimicrobianos. Ningún otro medicamento inhibió la actividad de E. faecium, excepto la dipirona para las cepas EFM19A y EFM9A. Los aislados mostraron elevada actividad antagónica contra gram-negativos, con destaque para los aislados EFM9A, EFM55 y EFM67. La mayor tasa de fermentación fue observada a 42 ºC, siendo la variación de pH de 4,15 a 5,15, después de 48 horas. Todos los aislados presentaron reducción del pH a 20 ºC. Sim embrago, a la temperatura de 42 °C, todos desenvolvieron la mayor acidez titulable en el tiempo de 48 horas. Los aislados EFM55 y EFM9A también presentaron características probióticas, bioquímicas y de susceptibilidad satisfactorias, teniendo en cuenta su potencial tecnológico en la producción de derivados lácteos.

Citas

Acuña, L., Picariello, G., Sesma, F., Morero, R. D., & Bellomio, A. (2012). A new hybrid bacteriocin, Ent35-MccV, displays antimicrobial activity against pathogenic Gram-positive and Gram-negative bacteria. FEBS Open Bio, 2, 12–19. https://doi.org/10 .1016/j.fob.2012.01.002

Anderson, A. C., Andisha, H., Hellwig, E., Jonas, D., Vach, K., & Al-Ahmad, A. (2018). Antibiotic resistance genes and antibiotic susceptibility of oral enterococcus faecalis isolates compared to isolates from hospitalized patients and food. In Advances in Experimental Medicine and Biology (Vol. 1057, pp. 47–62). https://doi.org/10.1007/5584_2017_53

Andrighetto, C., Knijff, E., Lombardi, A., Torriani, S., Vancanneyt, M., Kersters, K., Swings, J., & Dellaglio, F. (2001). Phenotypic and genetic diversity of enterococci isolated from Italian cheeses. Journal of Dairy Research, 68(2), 303–316. https://doi.org/10.1017/S0022029901004800

AOAC – Association of Official Analytical Chemists. (2003). Official methods of analysis of the Association of Official. Analytical Chemistry. 17. ed. Washington: AOAC, v. 1 e 2

Badarinath, V., & Halami, P. M. (2011). Purification of new β-galactosidase from enterococcus faecium mtcc 5153 with transgalactosylation activity. Food Biotechnology, 25(3), 225–239. https://doi.org/10.1080/08905436.2011.590766

Ben Braïek, O., Ghomrassi, H., Cremonesi, P., Morandi, S., Fleury, Y., Le Chevalier, P., Hani, K., Bel Hadj, O., & Ghrairi, T. (2017). Isolation and characterisation of an enterocin P-producing Enterococcus lactis strain from a fresh shrimp (Penaeus vannamei). Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 110(6), 771–786. https://doi.org/10.1007/s10482-017-0847-1

De Vuyst, L., & Leroy, F. (2007). Bacteriocins from lactic acid bacteria: Production, purification, and food applications. Journal of Molecular Microbiology and Biotechnology, 13(4), 194–199. https://doi.org/10.1159/000104752

Dunne, C., O’Mahony, L., Murphy, L., Thornton, G., Morrissey, D., O’Halloran, S., Feeney, M., Flynn, S., Fitzgerald, G., Daly, C., Kiely, B., O’Sullivan, G. C., Shanahan, F., & Collins, J. K. (2001). In vitro selection criteria for probiotic bacteria of human origin: Correlation with in vivo findings. American Journal of Clinical Nutrition, 73(2 SUPPL.), 386S-392S. https://doi.org/10.1093/ajcn/73.2.386s

El-Garhi, H. E. M., El-Aidie, S. A. M., Rashid, N. A., & Hayee, Z. A. (2018). Quality improvement of spreadable processed cheese made from ultrafiltered milk retentates using commercial starter cultures. Food Science and Technology International, 24(6), 465–475. https://doi.org/10.1177/1082013218766979

El-Ghaish, S., Dalgalarrondo, M., Choiset, Y., Sitohy, M., Ivanova, I., Haertlé, T., & Chobert, J. M. (2010). Screening of strains of Lactococci isolated from Egyptian dairy products for their proteolytic activity. Food Chemistry, 120(3), 758–764. https://doi.org/10.1016/j.foodchem.2009.11.007

Elmoslih, A., Zanzan, M., Aissa, R., Hamadi, F., Baddi, G., Aoumar, A., & Achemchem, F. (2017). Isolation and Characterization of Bacteriocinogenic Enterococcal and Lactococcal Strains from South of Morocco Dairy Product. Biotechnology Journal International, 18(4), 1–16. https://doi.org/10.9734/bji/2017/32919

Fernández, M., Hudson, J. A., Korpela, R., & De Los Reyes-Gavilán, C. G. (2015). Impact on human health of microorganisms present in fermented dairy products: An overview. BioMed Research International, 2015(ID 412714), 13 p. https://doi.org/10.1155/2015/412714

Foulquié Moreno, M. R., Sarantinopoulos, P., Tsakalidou, E., & De Vuyst, L. (2006). The role and application of enterococci in food and health. International Journal of Food Microbiology, 106(1), 1–24. https://doi.org/10.1016/j.ijfoodmicro.2005.06.026

Franz, C. M. A. P., Muscholl-Silberhorn, A. B., Yousif, N. M. K., Vancanneyt, M., Swings, J., & Holzapfel, W. H. (2001). Incidence of Virulence Factors and Antibiotic Resistance among Enterococci Isolated from Food. Applied and Environmental Microbiology, 67(9), 4385–4389. https://doi.org/10.1128/AEM.67.9.4385-4389.2001

Furlaneto Maia, L., Giazzi, A., Brandalize, C., Katsuda, M. S., Rocha, K. R., Terra, M. R., & Furlaneto, M. C. (2017). Isolation and characterization of potential probiotic enterococci strains from soft cheese flora. African Journal of Microbiology Research, 11(12), 482–487. https://doi.org/10.5897/ajmr2017.8429

García, M. T., Martínez Cañamero, M., Lucas, R., Omar, N. Ben, Pérez Pulido, R., & Gálvez, A. (2004). Inhibition of Listeria monocytogenes by enterocin EJ97 produced by Enterococcus faecalis EJ97. International Journal of Food Microbiology, 90(2), 161–170. https://doi.org/10.1016/S0168-1605(03)00051-5

Giraffa, G. (2002). Enterococci from foods. FEMS Microbiology Reviews, 26(2), 163–171. https://doi.org/10.1016/S0168-6445(02)00094-3

Giraffa, G. (2003). Functionality of enterococci in dairy products. International Journal of Food Microbiology, 88(2–3), 215–222. https://doi.org/10.1016/S0168-1605(03)00183-1

Hankin, L., & Anagnostakis, S. L. (1975). The Use of Solid Media for Detection of Enzyme Production by Fungi. Mycologia, 67(3), 597. https://doi.org/10.2307/3758395

İspirli, H., Demirbaş, F., & Dertli, E. (2017). Characterization of functional properties of Enterococcus spp. isolated from Turkish white cheese. LWT - Food Science and Technology, 75, 358–365. https://doi.org/10.1016/j.lwt.2016.09.010

Moreno, M. R. F., Rea, M. C., Cogan, T. M., & De Vuyst, L. (2003). The role and application of enterococci in food and health. International Journal of Food Microbiology, 106(1), 1–24.

Nami, Y., Bakhshayesh, R. V., Jalaly, H. M., Lotfi, H., Eslami, S., & Hejazi, M. A. (2019). Probiotic properties of enterococcus isolated from artisanal dairy products. Frontiers in Microbiology, 10(FEB), 13 p. https://doi.org/10.3389/fmicb.2019.00300

Nguyen, Y., & Sperandio, V. (2012). Enterohemorrhagic E. coli (EHEC) pathogenesis. Frontiers in Cellular and Infection Microbiology, 2(July), 90. https://doi.org/10.3389/fcimb.2012.00090

Nueno-Palop, C., & Narbad, A. (2011). Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut. International Journal of Food Microbiology, 145(2–3), 390–394. https://doi.org/10.1016/j.ijfoodmicro.2010.12.029

Ogaki, M. B., Rocha, K. R., Terra, M. R., Furlaneto, M. C., & Furlaneto-Maia, L. (2016). Screening of the enterocin-encoding genes and antimicrobial activityin Enterococcus species. Journal of Microbiology and Biotechnology, 26(6), 1026–1034. https://doi.org/10.4014/jmb.1509.09020

Ogier, J. C., & Serror, P. (2008). Safety assessment of dairy microorganisms: The Enterococcus genus. International Journal of Food Microbiology, 126(3), 291–301. https://doi.org/10.1016/j.ijfoodmicro.2007.08.017

Öncül, N., & Yıldırım, Z. (2019). Inhibitory effect of bacteriocins against Escherichia coli O157:H7. Food Science and Technology International, 25(6), 504–514. https://doi.org/10.1177/1082013219840462

Ozturkoglu-Budak, S., Wiebenga, A., Bron, P. A., & de Vries, R. P. (2016). Protease and lipase activities of fungal and bacterial strains derived from an artisanal raw ewe’s milk cheese. International Journal of Food Microbiology, 237(21), 17–27. https://doi.org/10.1016/j.ijfoodmicro.2016.08.007

Perin, L. M., Miranda, R. O., Camargo, A. C., Colombo, M., Carvalho, A. F., & Nero, L. A. (2013). Antimicrobial activity of the nisin Z producer Lactococcus lactis subsp. lactis lc08 against listeria monocytogenes in skim milk. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 65(5), 1554–1560. https://doi.org/10.1590/S0102-09352013000500037

Psoni, L., Kotzamanides, C., Andrighetto, C., Lombardi, A., Tzanetakis, N., & Litopoulou-Tzanetaki, E. (2006). Genotypic and phenotypic heterogeneity in Enterococcus isolates from Batzos, a raw goat milk cheese. International Journal of Food Microbiology, 109(1–2), 109–120. https://doi.org/10.1016/j.ijfoodmicro.2006.01.027

Rocha, K. R., Perini, H. F., de Souza, C. M., Schueler, J., Tosoni, N. F., Furlaneto, M. C., & Furlaneto-Maia, L. (2019). Inhibitory effect of bacteriocins from enterococci on developing and preformed biofilms of Listeria monocytogenes, Listeria ivanovii and Listeria innocua. World Journal of Microbiology and Biotechnology, 35(7), 1–11. https://doi.org/10.1007/s11274-019-2675-0

Todorov, S. D., Furtado, D. N., Saad, S. M. I., & De Melo Franco, B. D. G. (2011). Bacteriocin production and resistance to drugs are advantageous features for Lactobacillus acidophilus La-14, a potential probiotic strain. New Microbiologica, 34(4), 357–370.

Vinderola, G., Burns, P., & Reinheimer, J. (2017). Probiotics in Nondairy Products. In Vegetarian and Plant-Based Diets in Health and Disease Prevention. 809–835. https://doi.org/10.1016/B978-0-12-803968-7.00044-7

Walstra, P., Wouters, J. T. M., & Geurts, T. J. (2006). Dairy Science and Technology. (2nd ed.) Roca Ranton: CRC Press.

Yerlikaya, O., & Akbulut, N. (2019). Potential use of probiotic Enterococcus faecium and Enterococcus durans strains in Izmir Tulum cheese as adjunct culture. Journal of Food Science and Technology, 56(4), 2175–2185. https://doi.org/10.1007/s13197-019-03699-5

Enterococcus faecium en queso de curado artesanal: aspectos tecnológicos y de seguridad

Autores/as

DOI:

Palabras clave:

Resumen

Citas

Descargas

Publicado

Cómo citar

Número

Sección

Licencia

JOURNAL METRICS

Idioma

Enviar un artículo