Hygienic-health quality and microbiological hazard of clandestine Minas Frescal cheese commercialized in north Tocantins, Brazil
DOI:
https://doi.org/10.5433/1679-0359.2021v42n2p679Keywords:
EHEC, EPEC, Foodborne diseases, Public Health, STEC.Abstract
Cheese is a popular product that integrates the diet of the majority of the population, almost on a daily basis. It is rich in nutrients and, therefore, also an excellent substrate for the multiplication of microorganisms, including pathogens. The microbiological contamination of these products is highly relevant to the industry, resulting in an economic loss, and to public health, due to the risk of causing foodborne diseases. The aim of this study was to evaluate the hygienic-sanitary quality and the presence of bacterial pathogens in the clandestine Minas Frescal cheeses sold in the street open markets of Araguaína, TO, Brazil. Twenty-one samples were collected to evaluate the presence of total (TC) and thermotolerant (TTC) coliforms, Escherichia coli, and the pathotypes enteropathogenic E. coli (EPEC), and shiga toxin-producing E. coli (STEC) and enterohemorrhagic E. coli (EHEC), coagulase-positive staphylococci (CPS), Salmonella spp., and Listeria monocytogenes. The results showed that 100% of the cheese samples were in disagreement with the maximum standards of TC and TTC defined in the Brazilian legislation that regulates food quality control. In addition, 85.71% of the samples had values above the standard Brazilian maximum limit. In the study of diarrheagenic E. coli, 52.38%, 66.6%, and 4.76% of the samples were positive for EPEC, STEC, and EHEC, respectively, indicating fecal origin contamination of the samples and a potential consumer risk. No Salmonella spp. or Listeria monocytogenes were detected in these cheese samples. The high count of total and thermotolerant coliforms found in the samples demonstrates unsatisfactory sanitary conditions in the production, storage, and/or commercialization of this food product. The presence of EPEC, STEC, EHEC, and coagulase-positive staphylococci at high concentrations shows the health risk of the imminent consumption of Minas Frescal cheese.References
Apolinário, T. C. C., Santos, G. S., & Lavorato, J. A. A. (2014). Avaliação da qualidade microbiológica do queijo minas frescal produzido por laticínios do estado de Minas Gerais. Revista do Instituto Laticínios Cândido Toste, 69(6), 433-442. doi: 10.14295/2238-6416.v69i6.290
Argudín, M. A., Mendoza, M. C., & Rodicio, M. R. (2010). Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2(7), 1751-1773. doi: 10.3390/toxins2071751
Arruda, M. L. T., Nicolau, E. S., Reis, A. P., Araújo, A. S., & Mesquita, A. J. (2007). Ocorrência de Staphylococcus coagulase positiva em queijos tipos Frescal e Padrão comercializados nas feiras-livres de Goiânia - GO. Ver. Instituto Adolfo Lutz, 66(3), 292-298. Recuperado de http://periodicos.ses.sp.bvs.br /scielo.php?script=sci_arttext&pid=S0073-98552007000300013&lng=pt
Anvisa (2001). Agencia Nacional de Vigilância Sanitária. Resolução de Diretoria Colegiada nº 12, de 2 de janeiro de 2001. Regulamento Técnico sobre padrões microbiológicos para alimentos, Diário Oficial da União, Brasília.
Barreto de Deus, T., Barros, L. S. S., Silva, R. M., Lima, W. K. S., Lima, D. D. V., & Silva, A. S. (2017). Staphylococcus aureus and Escherichia coli in Curd Cheese Sold in the Northeastern Region of South America. International jornal of Microbiology, 2017(1), 8173741. doi: 10.1155/2017/8173741
Beloti, V. (2015). Leite: obtenção, inspeção e qualidade. Londrina: Editora Planta.
Borges, M. F., Nassu, R. T., Pereira, J. L., Andrade, A. P. C., & Kuaye, A. Y. (2008). Perfil de contaminação por Staphylococcus e suas enterotoxinas e monitorização das condições de higiene em uma linha de produção de queijo de coalho. Ciência Rural, 38(5), 1431-1438. doi: 10.1590/S0103-847820080005000 37
Ministério da Agricultura, Pecuária e Abastecimento (1996). Portaria nº 146, de 07 de março de 1996. Aprova os regulamentos técnicos de identidade e qualidade dos produtos lácteos, Diário Oficial da República Federativa do Brasil, Poder Executivo, Brasília.
Campos, A. C. L. P. de, Puño-Sarmiento, J. J., Medeiros, L. P., Gazal, L. E. S., Maluta, R. P., Navarro, A.,... Nakazato, G. (2018). Virulence Genes and Antimicrobial Resistance in Escherichia coli from Cheese Made from Unpasteurized Milk in Brazil. Foodborne Pathogens Disease, 15(2), 94-100. doi: 10.1089/ fpd.2017.2345
Carmo, L. S., Dias, R. S., Linardi, V. R., Sena, M. J., Santos, D. A., Faria, M. E.,... Heneine, L. G. (2002). Food poisoning due to enterotoxigenic strains of Staphylococcus present in Minas cheese and raw milk in Brazil. Food Microbiology, 19(1), 9-14. doi: 10.1006/fmic.2001.0444
, Y., & Knabel, S. J. (2007). Multiplex PCR for simultaneous detection of bacteria of the genus Listeria, Listeria monocytogenes, and major serotypes and epidemic clones of L. monocytogenes. Applied and Environmental Microbiology, 73(19), 6299-6304. doi: 10.1128/AEM.00961-07
Correll, W. A. (2014). Letter to American Cheese Society (ACS) with an update on what has been done with respect to non-toxigenic Escherichia coli (E. coli) in raw milk cheese. Public Health Service, Food and Drug Admin, College Park, MD.
Costa, G. M. D., Pereira, U. D. P., Custódio, D. A. D. C., & Silva, N. D. (2011). Caracterização de Staphylococcus coagulase-positiva utilizando plasmas de diferentes espécies animais. Revista do Instituto Adolfo Lutz, 70(4), 584-588. Recuperado de http://periodicos.ses.sp.bvs.br/scielo.php?script=sci_ arttext&pid=S0073-98552011000400021&lng=pt&nrm=iso
Cruz, C. D., Martinez, M. B., & Destro, M. T. (2008). Listeria monocytogenes: um agente infeccioso ainda pouco conhecido no Brasil. Alimentos e Nutrição Araraquara, 19(2), 195-206. Recuperado de https://www.researchgate.net/publication/49599808_Listeria_monocytogenes_UM_AGENTE_INFECCIOSO_AINDA_POUCO_CONHECIDO_NO_BRASIL
Dailey, R. C., Martin, K. G., & Smiley, R. D. (2014). The effects of competition from non-pathogenic foodborne bacteria during the selective enrichment of Listeria monocytogenes using buffered Listeria enrichment broth. Food Microbiology, 44(1º), 173-179. doi: 10.1016/j.fm.2014.05.004
Dias, B. F., Ferreira, S. M., Carvalho, V. S., & Soares, D. S. B. (2016). Qualidade microbiológica e físico-química de queijo minas frescal artesanal e industrial. Journal of Neotropical Agriculture, 3(3), 57-64. doi: 10.32404/rean.v3i3.1211
Elbagory, A. M., Eman, S. H., & Eman, K. F. (2015). Impact of probiotic strains on growth of some food poisoning bacteria from milk and soft cheese. Nutrition and Food Technology, 1(2). doi: 10.16966/2470-6086.107
Fai, A. E. C., Figueredo, E. A. T., Verdin, S. E. F., Pinheiro, N. M. S., Braga, A. R. C., & Stamford, T. L. M. (2011). Salmonella sp e Listeria monocytogenes em presunto suíno comercializado em supermercados de Fortaleza (CE, Brasil), fator de risco para a saúde pública. Ciência & Saúde Coletiva, 16(2), 657-662. doi: 10.1590/S1413-81232011000200029
Farrokh, C., Jordan, K., Auvray, F., Glass, K., Oppegaard, H., Raynaud, S.,... Cerf, O. (2013). Review of Shiga-toxin-producing Escherichia coli (STEC) and their significance in dairy production. International. Journal of. Food Microbology, 162(2), 190-212. doi: 10.1016/j.ijfoodmicro.2012.08.008
Franco, B. D. G. M., & Landgraf, M. (2002). Microbiologia dos alimentos. São Paulo: Atheneu.
Gomes, T. A. T., Elias, W. P., Scaletsky, I. C. A., Guth, B. E. C., Rodrigues, J. F., Piazza, R. M. F.,... Martinez, M. B. (2016). Diarrheagenic Escherichia coli. Brazolian Journal of medical Microbioly, 47(Suppl. 1), 3-30. doi: 10.1016/j.bjm.2016.10.015
Hobbs, B. C., & Roberts, D. (1999). Toxinfecções e controle higiênico-sanitário de alimentos. São Paulo: Varela.
Johler, S., Wender, D., Bridy, C., Huguenin, M. C., Robert, L., Hummerjohann, J., & Stephan, R. (2015). Outbreak of staphylococcal food poisoning among children and staff at a Swiss boarding school due to soft cheese made from raw milk. Journal od Dairy Science, 98(5), 2944-2948. doi: 10.3168/jds.2014-9123
Lopes, M. A., Carmo, E. A., Lima, A. L. R., & Carvalho, F. M. (2006). Análise de rentabilidade de uma empresa com opção de comercialização de queijo ou leite. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 58(4), 642-647. doi: 10.1590/S0102-09352006000400028
Mehli, L., Hoel, S., Bjorge, G. M., Nordeng, A., & Karlsen, H. (2017). The prevalence, genetic diversity and antibiotic resistance of Staphylococcus aureus in milk, whey, and cheese from artisan farm dairies. International Dairy Journal, 65(1), 20-27. doi: 10.1016/j.idairyj.2016.10.006
Miszczycha, S. D., Thevenot, J., Denis, S., Callon, C., Livrelli, V., Alric, M.,... Thevenot-Sergentet, D. (2014). Survival of Escherichia coli O26:H11 exceeds that of Escherichia coli O157:H7 as assessed by simulated human digestion of contaminated raw milk cheeses. International Journal Food Microbiology, 172(1), 40-48. doi: 10.1016/j.ijfoodmicro.2013.11.029
Murray, P. R., Rosenthal, K. S., Kobayashi, G. S., & Pfaller, M. A. (2014). Microbiologia médica (7a ed.). Rio de Janeiro: Elsevier.
Nataro, J. P., & Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clinical Microbiology Reviews, 11(1), 142-201. doi: 10.1128/CMR.11.1.142
Paton, A. W., & Paton, J. C. (1998). Detection and characterization of shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfb O111, andrfb O157. Journal Clinica lMicrobiology, 36(2), 598-602. doi: 10.1128/CMR.11.1.142
Ribeiro, J. C., Jr., Silva, F. F., Lima, J. B. A., Ossugui, E. H., Teinder, P. I., Jr., Campos, A. C. L. P.,... Beloti, V. (2019). Short communication: Molecular characterization and antimicrobial resistance of pathogenic Escherichia coli isolated from raw milk and Minas Frescal cheeses in Brazil. Journal of Dairy Science, 102(12), 10850-10854. doi: 10.3168/jds.2019-16732
Ribeiro, J. C., Jr., Tamanini, R., Soares, B. F., Oliveira, A. M., Silva, F. G., Silva, F. F.,... Beloti, V. (2016). Efficiency of boiling and four other methods for genomic DNA extraction of deteriorating spore-forming bacteria from milk. Semina: Ciências Agrárias, 37(5), 3069-3078. doi: 10.5433/1679-0359.2016v37n5 p3069
Salvador, F. C. (2012). Avaliação da qualidade microbiológica do leite pasteurizado comercializado em Apucarana-PR e região. Revista Fapciências, 9(5), 30-41. Recuperado de https://docplayer.com.br/222 54320-Avaliacao-da-qualidade-microbiologica-do-leite-pasteurizado-comercializado-em-apucarana-pr-e-regiao.html
Sato'o, Y., Omoe, K., Naito, I., Ono, H. K., Nakane, A., Sugai, M.,... Hu, D. L. (2014). Molecular epidemiology and identification of a Staphylococcus aureus clone causing food poisoning outbreaks in Japan. Journal Clinical Microbiology, 52(7), 2637-2640. doi: 10.1128/JCM.00661-14
Shanmugasamy, M., Velayutham, T., & Rajeswar, J. (2011). InvA gene specific PCR for detection of Salmonella from broilers. Veterinari World, 4(12), 562-564. doi: 10.5455/vetworld.2011.562-564
Silva, J. A., & Silva, D. (2005). Escherichia coli Enteropatogênica (EPEC), ao contrário da Echerichia coli comensal, adere, sinaliza e lesa enterócitos. Revista de Patologia Tropical, 34(3), 175-196. doi: 10.5216/ rpt.v34i3.1925
Silva, N., Junqueira, V. C. A., Silveira, N. F. A., Taniwaki, M. H., Gomes, R. A. R., & Okazaki, M. M. (2017). Manual de métodos de analises microbiológica de alimentos e água (5a ed.). São Paulo: Blucher.
Souza, C. D. O., Melo, T. R. B., Melo, C. D. S. B., Menezes, Ê. M., Carvalho, A. C. D., & Monteiro, L. C. R. (2016). Escherichia coli enteropatogênica: uma categoria diarreiogênica versátil. Revista Pan-Amazônica de Saúde, 7(2), 79-91. doi: 10.5123/S2176-62232016000200010
Souza, I. A., Giovannetti, A. C. S., Santos, L. G. F., Gandra, S. O. S., Martins, M. L., & Ramos, A. L. S. (2017). Qualidade microbiológica de queijo minas frescal comercializado na zona da mata mineira. Revista do Instituto Laticínios Cândido Tostes, 72(3), 152-162. doi: 10.14295/2238-6416.v72i3.598
Teider, P. I., Jr., Ribeiro, J. C., Jr., Ossugui, E. H., Tamanini, R., Ribeiro, J., Santos, G. A.,... Beloti, V. (2019). Pseudomonas spp. and other psychrotrophic microorganisms in inspected and non-inspected Brazilian Minas Frescal Cheese: proteolytic, lipolytic and AprX production potential. Pesquisa Veterinária Brasileira, 39(10), 807-815. doi: 10.1590/1678-5150-PVB-6037
Trmcic, A., Chauhan, K., Kent, D. J., Ralyea, R. D., Martin, N. H., Boor, K. J., & Wiedmann, M. (2016). Coliform detection in cheese is associated with specific cheese characteristics, but no association was found with pathogen detection. Jounal of Dairy Science, 99(8), 6105-6120. doi: 10.3168/jds.2016-11112
Vigilância Epidemiológica do Município de Araguaína-TO (2019). Comunicação pessoal. Araguaína: Secretaria Municipal de Saúde de Araguaína. TO.
World Health Organization (2019). Saumonella (no-typhoidal). Retrieved from https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal)
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Semina: Ciências Agrárias
![Creative Commons License](http://i.creativecommons.org/l/by-nc/4.0/88x31.png)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Semina: Ciências Agrárias adopts the CC-BY-NC license for its publications, the copyright being held by the author, in cases of republication we recommend that authors indicate first publication in this journal.
This license allows you to copy and redistribute the material in any medium or format, remix, transform and develop the material, as long as it is not for commercial purposes. And due credit must be given to the creator.
The opinions expressed by the authors of the articles are their sole responsibility.
The magazine reserves the right to make normative, orthographic and grammatical changes to the originals in order to maintain the cultured standard of the language and the credibility of the vehicle. However, it will respect the writing style of the authors. Changes, corrections or suggestions of a conceptual nature will be sent to the authors when necessary.