Survival assessment of Salmonella enterica in inoculated pork salami
DOI:
https://doi.org/10.5433/1679-0359.2020v41n6p2613Keywords:
Fermentation, Maturation, Microorganism, Ripening, Sausage.Abstract
Pork salami is an embedded, cured and ripened product commonly consumed in Brazil, and the presence of Salmonella enterica has already been reported in this product. During its preparation, the microbiological safety depends on the meat quality, addition of ingredients with antimicrobial activity, hygiene during processing, pH and water activity (Aw) reduction during maturation. In Brazil, the maturation protocol has not been determined in food regulation; therefore, the objectives of this study were (a) to identify the fermentation and drying phases during salami maturation; (b) to test the survival of S. enterica during salami processing; and (c) to compare xylose lysine deoxycholate (XLD) and thin agar layer (TAL) agar for recovering Salmonella. The salami samples were prepared with a cocktail of S. enterica strains, fermented at 30°C and dried at 20°C with controlled relative humidity (RH). Periodic sampling for S. enterica quantification and Aw and pH analyses were performed during maturation, and curves were constructed. Fermentation occurred during the first 66 hours, and the pH decreased while the population of S. enterica increased over the first 21 hours. The drying step was able to reduce the bacterial population by approximately 5 log CFU after 875 hours, reaching an Aw of less than 0.78. However, elimination of S. enterica was not achieved. For Salmonella recovery, TAL agar was more efficient than XLD agar.References
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Barbosa, M. S., Todorov, S. D., Jurkiewicz, C. H., & Franco, B. D. G. M. (2015). Bacteriocin production by Lactobacillus curvatus MBSa2 entrapped in calcium alginate during ripening of salami for control of Listeria monocytogenes. Food Control, 47(1), 147-153. doi: 10.1016/j.foodcont.2014.07.005
Beales, N. (2004). Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Comprehensive Reviews in Food Science and Food Safety, 3(1), 1-20. doi: 10. 1111/j.1541-4337.2004.tb00057.x
Caccioppoli, J., Custódio, F. B., Vieira, S. M., Coelho, J. V., & Glória, M. B. A. (2006). Aminas bioativas e características físico-químicas de salames tipo italiano. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 58(4), 648-657. doi: 10.1590/S0102-09352006000400029
Campagnol, P. C. B., Fries, L. L. M., Terra, N. N., Santos, B. A. dos, Furtado, A. S., Toneto, E. R. L., & Campos, R. M. L. D. (2011). The influence of achyrocline satureioides (“ Marcela”) extract on the lipid oxidation of salami. Ciência e Tecnologia de Alimentos, 31(1), 101-105. doi: 10.1590/S0101-20612011 000100013
Chang, V. P., Mills, E. W., & Cutter, C. N. (2003). Comparison of recovery methods for freeze-injured Listeria monocytogenes, Salmonella Typhimurium, and Campylobacter coli in cell suspensions and associated with pork surfaces. Journal of Food Protection, 66(5), 798-803. doi: 10.4315/0362-028X-66 .5.798
Chasco, J., Lizaso, G., & Beriain, M. J. (1996). Cured colour development during sausage processing. Meat Science, 44(3), 203-211. doi: 10.1016/S0309-1740(96)00092-7
Cirolini, A., Fries, L. L. M., Terra, N. N., Milani, L. I. G., Urnau, D., Santos, B. A. dos, … Rezer, A. P. de S. (2010). Salame tipo italiano elaborado com culturas starters nativas. Ciência e Tecnologia de Alimentos, 30(1), 171-179. doi: 10.1590/S0101-20612010000500026
Coroller, L., Kan-King-Yu, D., Leguerinel, I., Mafart, P., & Membré, J. M. (2012). Modelling of growth, growth/no-growth interface and nonthermal inactivation areas of Listeria in foods. International Journal of Food Microbiology, 152(3), 139-152. doi: 10.1016/j.ijfoodmicro.2011.09.023
Ferreira, F. S., Horvath, M. B., & Tondo, E. C. (2013). Assessing the growth and recovery of Salmonella Enteritidis SE86 after sodium dichloroisocyanurate exposure. Brazilian Journal of Microbiology, 44(3), 785-790. doi: 10.1590/S1517-83822013000300018
Fieira, C., Marchi, J. F., Marafão, D., & Alfaro, A. T. da. (2018). The impact of the partial replacement of sodium chloride in the development of starter cultures during Italian salami production. Brazilian Journal of Food Technology, 21(1), 1-8. doi: 10.1590/1981-6723.03615
Hwang, C. A., Porto-Fett, A. C. S., Juneja, V. K., Ingham, S. C., Ingham, B. H., & Luchansky, J. B. (2009). Modeling the survival of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium during fermentation, drying, and storage of soudjouk-style fermented sausage. International Journal of Food Microbiology, 129(3), 244-252. doi: 10.1016/j.ijfoodmicro.2008.12.003
Instrução Normativa nº 22, de 31 de julho de 2000. Aprova o Regulamento Técnico de Identidade e Qualidade de de Copa, de Jerked Beef, de Presunto tipo Parma, de Presunto Cru, de Salame, de Salaminho, de Salaminho tipo Alemão, de Salame tipo Calabrês, de Salame tipo Friolano, de Salame tipo Napolitano, de Salame tipo hamburguês, de Salame tipo Italiano, de Salame tipo Milano, de Lingüiça Colonial e Pepperoni. Diário Oficial da União, Brasília. Recuperado de http://extranet. agricultura.gov.br/sislegis-consulta/consultarLegislacao.do?operacao=visualizar&id= 2239
Kang, D. H., & Fung, D. Y. C. (2000). Application of thin agar layer method for recovery of injured Salmonella typhimurium. International Journal of Food Microbiology, 54(1-2), 127-132. doi: 10.1016/ S0168-1605(99)00174-9
Kang, D. H., & Siragusa, G. R. (1999). Agar underlay method for recovery of sublethally heat-injured bacteria. Applied and Environmental Microbiology, 65(12), 5334-5337. doi: 10.1128/aem.65.12.5334-
Lindqvist, R., & Lindblad, M. (2009). Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage. International Journal of Food Microbiology, 129(1), 59-67. doi: 10.1016/j.ijfoodmicro.2008.11.011
Mataragas, M., Bellio, A., Rovetto, F., Astegiano, S., Greci, C., Hertel, C.,... Cocolin, L. (2015). Quantification of persistence of the food-borne pathogens Listeria monocytogenes and Salmonella enterica during manufacture of Italian fermented sausages. Food Control, 47(1), 552-559. doi: 10.1016/ j.foodcont.2014.07.058
Mauriello, G., Casaburi, A., Blaiotta, G., & Villani, F. (2004). Isolation and technological properties of coagulase negative staphylococci from fermented sausages of Southern Italy. Meat Science, 67(1), 149-158. doi: 10.1016/j.meatsci.2003.10.003
Ministério da Saúde (2019). Surtos de doenças transmitidas por alimentos no Brasil. Recuperado de http://portalarquivos2.saude.gov.br/images/pdf/2019/fevereiro/15/Apresenta----o-Surtos-DTA---Fevereiro-2019.pdf
Nightingale, K. K., Thippareddi, H., Phebus, R. K., Marsden, J. L., & Nutsch, A. L. (2006). Validation of a traditional Italian-Style Salami manufacturing process for control of Salmonella and Listeria monocytogenes. Journal of Food Protection, 69(4), 794-800. doi: 10.4315/0362-028x-69.4.794
Quinn, P. J., Markey, B. K., Leonard, F. C., Hartigan, P. J., Fanning, S., & Fitzpatrick, E. S. (2011). Veterinary Microbiology and microbial disease. New Jersey: Wiley-Blackwell
Resolução RDC nº 12, de 2 de janeiro de 2001. Aprova o Regulamento Técnico Sobre Padrões Microbiológicos para Alimentos. Diário Oficial da União, Brasília. Recuperado de http://portal. anvisa.gov.br/documents/33880/2568070/RDC_12_2001.pdf/15ffddf6-3767-4527-bfac-740a0400829b
Riordan, D. C. R., Duffy, G., Sheridan, J. J., Eblen, B. S., Whiting, R. C., Blair, I. A. N. S., & Mcdowelv, D. A. (1998). Survival of Escherichia coli 0157: H7 during the manufacture of pepperoni. Journal of Food Protection, 61(2), 146-151. doi: 10.4315/0362-028x-61.2.146
Roccato, A., Uyttendaele, M., Barrucci, F., Cibin, V., Favretti, M., Cereser, A.,… Ricci, A. (2017). Artisanal Italian salami and soppresse: identification of control strategies to manage microbiological hazards. Food Microbiology, 61(1), 5-13. doi: 10.1016/j.fm.2016.07.010
Santa, O. R. D., Macedo, R. E. F. de, Santa, H. S. D., Zanette, C. M., Freitas, R. J. S. de, & Terra, N. N. (2014). Use of starter cultures isolated from native microbiota of artisanal sausage in the production of Italian sausage. Food Science and Technology, 34(4), 780-786. doi: 10.1590/1678-457X.6467
Werlang, G. O., Haubert, L., Peter, C. M., & Cardoso, M. (2019). Isolation of Salmonella Typhimurium, Listeria monocytogenes and coagulase-positive Staphylococcus from salami sold at street fairs in Porto Alegre, Brazil. Arquivos do Instituto Biológico, 86(1), 1-6. doi: 10.1590/1808-1657000072019
Wu, V. C. H., Fung, D. Y. C., & Kang, D. H. (2001). Evaluation of thin agar layer method for recovery of cold-injured foodborne pathogens. Journal of Rapid Methods and Automation in Microbiology, 9(1), 11-25. doi: 10.1111/j.1745-4581.2001.tb00224.x
Back, K.-H., Kim, S.-O., Park, K.-H., Chung, M.-S., & Kang, D.-H. (2012). Spray method for recovery of heat-injured Salmonella Typhimurium and Listeria monocytogenes. Journal of Food Protection, 75(10), 1867-1872. doi: 10.4315/0362-028x.jfp-11-512
Barbosa, M. S., Todorov, S. D., Jurkiewicz, C. H., & Franco, B. D. G. M. (2015). Bacteriocin production by Lactobacillus curvatus MBSa2 entrapped in calcium alginate during ripening of salami for control of Listeria monocytogenes. Food Control, 47(1), 147-153. doi: 10.1016/j.foodcont.2014.07.005
Beales, N. (2004). Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: a review. Comprehensive Reviews in Food Science and Food Safety, 3(1), 1-20. doi: 10. 1111/j.1541-4337.2004.tb00057.x
Caccioppoli, J., Custódio, F. B., Vieira, S. M., Coelho, J. V., & Glória, M. B. A. (2006). Aminas bioativas e características físico-químicas de salames tipo italiano. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 58(4), 648-657. doi: 10.1590/S0102-09352006000400029
Campagnol, P. C. B., Fries, L. L. M., Terra, N. N., Santos, B. A. dos, Furtado, A. S., Toneto, E. R. L., & Campos, R. M. L. D. (2011). The influence of achyrocline satureioides (“ Marcela”) extract on the lipid oxidation of salami. Ciência e Tecnologia de Alimentos, 31(1), 101-105. doi: 10.1590/S0101-20612011 000100013
Chang, V. P., Mills, E. W., & Cutter, C. N. (2003). Comparison of recovery methods for freeze-injured Listeria monocytogenes, Salmonella Typhimurium, and Campylobacter coli in cell suspensions and associated with pork surfaces. Journal of Food Protection, 66(5), 798-803. doi: 10.4315/0362-028X-66 .5.798
Chasco, J., Lizaso, G., & Beriain, M. J. (1996). Cured colour development during sausage processing. Meat Science, 44(3), 203-211. doi: 10.1016/S0309-1740(96)00092-7
Cirolini, A., Fries, L. L. M., Terra, N. N., Milani, L. I. G., Urnau, D., Santos, B. A. dos, … Rezer, A. P. de S. (2010). Salame tipo italiano elaborado com culturas starters nativas. Ciência e Tecnologia de Alimentos, 30(1), 171-179. doi: 10.1590/S0101-20612010000500026
Coroller, L., Kan-King-Yu, D., Leguerinel, I., Mafart, P., & Membré, J. M. (2012). Modelling of growth, growth/no-growth interface and nonthermal inactivation areas of Listeria in foods. International Journal of Food Microbiology, 152(3), 139-152. doi: 10.1016/j.ijfoodmicro.2011.09.023
Ferreira, F. S., Horvath, M. B., & Tondo, E. C. (2013). Assessing the growth and recovery of Salmonella Enteritidis SE86 after sodium dichloroisocyanurate exposure. Brazilian Journal of Microbiology, 44(3), 785-790. doi: 10.1590/S1517-83822013000300018
Fieira, C., Marchi, J. F., Marafão, D., & Alfaro, A. T. da. (2018). The impact of the partial replacement of sodium chloride in the development of starter cultures during Italian salami production. Brazilian Journal of Food Technology, 21(1), 1-8. doi: 10.1590/1981-6723.03615
Hwang, C. A., Porto-Fett, A. C. S., Juneja, V. K., Ingham, S. C., Ingham, B. H., & Luchansky, J. B. (2009). Modeling the survival of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium during fermentation, drying, and storage of soudjouk-style fermented sausage. International Journal of Food Microbiology, 129(3), 244-252. doi: 10.1016/j.ijfoodmicro.2008.12.003
Instrução Normativa nº 22, de 31 de julho de 2000. Aprova o Regulamento Técnico de Identidade e Qualidade de de Copa, de Jerked Beef, de Presunto tipo Parma, de Presunto Cru, de Salame, de Salaminho, de Salaminho tipo Alemão, de Salame tipo Calabrês, de Salame tipo Friolano, de Salame tipo Napolitano, de Salame tipo hamburguês, de Salame tipo Italiano, de Salame tipo Milano, de Lingüiça Colonial e Pepperoni. Diário Oficial da União, Brasília. Recuperado de http://extranet. agricultura.gov.br/sislegis-consulta/consultarLegislacao.do?operacao=visualizar&id= 2239
Kang, D. H., & Fung, D. Y. C. (2000). Application of thin agar layer method for recovery of injured Salmonella typhimurium. International Journal of Food Microbiology, 54(1-2), 127-132. doi: 10.1016/ S0168-1605(99)00174-9
Kang, D. H., & Siragusa, G. R. (1999). Agar underlay method for recovery of sublethally heat-injured bacteria. Applied and Environmental Microbiology, 65(12), 5334-5337. doi: 10.1128/aem.65.12.5334-
Lindqvist, R., & Lindblad, M. (2009). Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage. International Journal of Food Microbiology, 129(1), 59-67. doi: 10.1016/j.ijfoodmicro.2008.11.011
Mataragas, M., Bellio, A., Rovetto, F., Astegiano, S., Greci, C., Hertel, C.,... Cocolin, L. (2015). Quantification of persistence of the food-borne pathogens Listeria monocytogenes and Salmonella enterica during manufacture of Italian fermented sausages. Food Control, 47(1), 552-559. doi: 10.1016/ j.foodcont.2014.07.058
Mauriello, G., Casaburi, A., Blaiotta, G., & Villani, F. (2004). Isolation and technological properties of coagulase negative staphylococci from fermented sausages of Southern Italy. Meat Science, 67(1), 149-158. doi: 10.1016/j.meatsci.2003.10.003
Ministério da Saúde (2019). Surtos de doenças transmitidas por alimentos no Brasil. Recuperado de http://portalarquivos2.saude.gov.br/images/pdf/2019/fevereiro/15/Apresenta----o-Surtos-DTA---Fevereiro-2019.pdf
Nightingale, K. K., Thippareddi, H., Phebus, R. K., Marsden, J. L., & Nutsch, A. L. (2006). Validation of a traditional Italian-Style Salami manufacturing process for control of Salmonella and Listeria monocytogenes. Journal of Food Protection, 69(4), 794-800. doi: 10.4315/0362-028x-69.4.794
Quinn, P. J., Markey, B. K., Leonard, F. C., Hartigan, P. J., Fanning, S., & Fitzpatrick, E. S. (2011). Veterinary Microbiology and microbial disease. New Jersey: Wiley-Blackwell
Resolução RDC nº 12, de 2 de janeiro de 2001. Aprova o Regulamento Técnico Sobre Padrões Microbiológicos para Alimentos. Diário Oficial da União, Brasília. Recuperado de http://portal. anvisa.gov.br/documents/33880/2568070/RDC_12_2001.pdf/15ffddf6-3767-4527-bfac-740a0400829b
Riordan, D. C. R., Duffy, G., Sheridan, J. J., Eblen, B. S., Whiting, R. C., Blair, I. A. N. S., & Mcdowelv, D. A. (1998). Survival of Escherichia coli 0157: H7 during the manufacture of pepperoni. Journal of Food Protection, 61(2), 146-151. doi: 10.4315/0362-028x-61.2.146
Roccato, A., Uyttendaele, M., Barrucci, F., Cibin, V., Favretti, M., Cereser, A.,… Ricci, A. (2017). Artisanal Italian salami and soppresse: identification of control strategies to manage microbiological hazards. Food Microbiology, 61(1), 5-13. doi: 10.1016/j.fm.2016.07.010
Santa, O. R. D., Macedo, R. E. F. de, Santa, H. S. D., Zanette, C. M., Freitas, R. J. S. de, & Terra, N. N. (2014). Use of starter cultures isolated from native microbiota of artisanal sausage in the production of Italian sausage. Food Science and Technology, 34(4), 780-786. doi: 10.1590/1678-457X.6467
Werlang, G. O., Haubert, L., Peter, C. M., & Cardoso, M. (2019). Isolation of Salmonella Typhimurium, Listeria monocytogenes and coagulase-positive Staphylococcus from salami sold at street fairs in Porto Alegre, Brazil. Arquivos do Instituto Biológico, 86(1), 1-6. doi: 10.1590/1808-1657000072019
Wu, V. C. H., Fung, D. Y. C., & Kang, D. H. (2001). Evaluation of thin agar layer method for recovery of cold-injured foodborne pathogens. Journal of Rapid Methods and Automation in Microbiology, 9(1), 11-25. doi: 10.1111/j.1745-4581.2001.tb00224.x
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2020-09-19
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Werlang, G. O., Vieira, T. R., Costa, E. de F., & Cardoso, M. (2020). Survival assessment of Salmonella enterica in inoculated pork salami. Semina: Ciências Agrárias, 41(6), 2613–2620. https://doi.org/10.5433/1679-0359.2020v41n6p2613
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