Evaluation of the innocuousness and microbiological characterization of minas artisanal cheese produced in Santa Vitória, Brasil
DOI:
https://doi.org/10.33448/rsd-v9i7.4004Keywords:
Raw milk; Maturation; Good manufacturing practices.Abstract
The manufacture of artisanal cheeses is one of the most important activities of the family agroindustry in Minas Gerais. Given the economic and cultural importance of Minas Artesanal Cheese, the objective of this study was to evaluate the microbiological characteristics and safety of Minas Artisanal Cheese (MAC) produced in a rural property in Santa Vitória-MG. Twelve cheese samples were evaluated in January 2019 (summer), and 12 samples were evaluated in July 2019 (winter) at four maturation times (1, 7, 14 and 21 days). Evolution of the moisture and pH of the cheese during maturation were evaluated. Coliforms were counted at 30 °C and 45 °C, and the presence/absence of Staphylococcus aureus, lactic acid bacteria (LAB), mold, yeast and Salmonella were evaluated. Microbiological characteristics of the cheese water supply, milk, endogenous yeast and the cheese surface were also evaluated. There was variation between the two seasons in terms of humidity and LAB. Significant differences were observed in the coliform counts at 30°C and 45°C, and the presence of S. aureus, LAB, mold and yeasts in the cheese were evaluated during maturation in both seasons. Maturation influenced the moisture content but did not influence the pH. There was a reduction over time in the pathogen count. At the end of ripening, the cheese did not exhibit parameters that would guarantee its microbiological safety. Maturation significantly reduced the microorganism counts, but the MAC did not comply with current legislation. Thus, the cheese was not harmless and presented risks when consumed due to the possibility of causing foodborne diseases.
References
Almeida, AC, Diniz, TT, Souza, MR, Pinto, MS, de Souza, RM, Silva, NO & Queiroz, MRA. (2013). Characterization of production of artisanal cheese in the region of Montes Claros-MG, Brazil. Acta Veterinaria Brasilica, 6(4), 312-20.
Andrews, W, Wang, H, Jacobson, A & Hammack, T. (2016). Salmonella. In Food and Drug Administration (FDA) (Eds.), Bacteriological Analytical Manual (p. 1-21). FDA/CFSAN.
Banjara, N, Suhr, MJ & Hallen-Adams, HE. (2015). Diversity of Yeast and Mold Species from a Variety of Cheese Types. Current Microbiology, 70(6), 792-800.
Bennett, RW, Hait, JM & Tallent, SM. (2015). Staphylococcus aureus and Staphylococcal Enterotoxins. In Y. Salfinger, & M. L. Tortorello (Eds.), Compendium of methods for the microbiological examination of foods (p. 509-26). Washington: American Public Health Association.
Beresford, TP, Fitzsimons, NA, Brennan, NL & Cogan, TM. (2001). Recent advances in cheese microbiology. International Dairy Journal, 11(4-7), 259-74.
Borges, MF, Pereira, JL, Feitosa, T & Kuaye, AY. (2008). Enterotoxigenic Staphylococcus in milk and dairy products, its enterotoxins and related genes: a review. Boletim CEPPA, 26(1), 71-86.
Braun-Howland, EB & Hunt, ME. (2017). Part 9000 - Microbiological Examination: 9921 - Multiple-tube Fermentation Technique for Members of the Coliform Group. In: W.E. Federation (Ed.), Standard methods for the examination of water and wasterwater. Washington D.C.: American Public Health Association, American Water Works Association, and Water Environment Federation.
Brazil. (2018). Ficam estabelecidos como oficiais os métodos constantes do Manual de Métodos Oficiais para Análise de Alimentos de Origem Animal (Instrução Normativa N° 30, de 26 de junho de 2018). Diário Oficial da República Federativa do Brasil. Ministério da Agricultura Pecuária e Abastecimento.
Campagnollo, FB, Margalho, LP, Kamimura, BA, Feliciano, MD, Freire, L, Lopes, LS, Alvarenga, VO, Cadavez, VAP, Gonzales-Barron, U, Schaffner, DW & Sant’Ana, AS. (2018). Selection of indigenous lactic acid bacteria presenting anti-listerial activity, and their role in reducing the maturation period and assuring the safety of traditional Brazilian cheeses. Food Microbiology, 73, 288-97.
Cardoso, V, Borelli, BM, Lara, CA, Pataro, C, Bodevan, EC & Rosa, CA. (2015). The influence of seasons and ripening time on yeast communities of a traditional Brazilian cheese. Food Research International, 69, 331-40.
Cardoso, VM, Dias, RS, Soares, BM, Clementino, LA, Araújo, CP & Rosa, CA. (2013). The influence of ripening period length and season on the microbiological parameters of a traditional Brazilian cheese. Brazilian Journal of Microbiology, 44(3), 743-49.
Carvalho, ASS, Serra, JL, Rodrigues, LC, de Souza, LRJ, Mouchrek, AN & Ferreira, EM. (2018). Susceptibility of Staphylococcus aureus isolated from raw milk to commercial antibiotics. Ciência Animal Brasileira, 19(e-47159), 1-8.
Castro, RD, Oliveira, LG, Sant’Anna, FM, Luiz, LMP, Sandes, SHC, Silva, CIF, Silva, AM, Nunes, AC, Penna, CFAM & Souza, MR. (2016). Lactic acid microbiota identification in water, raw milk, endogenous starter culture, and fresh Minas artisanal cheese from the Campo das Vertentes region of Brazil during the dry and rainy seasons. Journal of Dairy Science, 99(8), 6086-96.
Chambers, JV. (2005). The Microbiology of Raw Milk. In RK. Robinson (Eds.), Dairy microbiology handbook: the microbiology of milk and milk products (p. 39-90). New Jersey: John Wiley & Sons.
Cosby, CM, Costello, CA, Morris, WC, Haughton, B, Devereaux, MJ, Harte, F & Davidson, PM. (2008). Microbiological analysis of food contact surfaces in child care centers. Applied and Environmental Microbiology, 74(22), 6918-22.
Costa Jr, LCG, Costa, RGB, Magalhães, FAR, Vargas, PIR, Fernandes, AJM & Pereira, AS. (2009). Changes in composition of artesanal minas cheese from the “Canastra-MG” area in four seasons. Revista do Instituto de Laticínios Cândido Tostes, 64(371), 13-21.
Costa Jr, LCG, Moreno, VJ, Magalhães, FAR, Costa, RGB, Resende, EC & Carvalho, KB. A. (2014). Ripening of artisanal Minas cheese from the "Campo das Vertentes" region and the effects of dry and wet periods. Revista do Instituto de Laticínios Cândido Tostes, 69(2), 111-20.
Davidson, PM, Roth, LA, Gambrel-Lenarz, SA & Bruhn, J. (2004). Coliform and Other Indicator Bacteria. In: Wehr, HM & Frank, JF (Eds.), Standard methods for the examination of dairy products (p. 187-226). Washington: American Public Health Association.
Dias, MAC, Sant’Ana, AS, Cruz, AG, de Assis F, Faria, J, Oliveira, CAF & Bona, E. (2012). On the implementation of good manufacturing practices in a small processing unity of mozzarella cheese in Brazil. Food control, 24(1-2), 199-205.
Dores, MT & Ferreira, CLLF. (2012). Minas artisanal cheese, centennial tradition: threats and challenges. Revista Brasileira Agropecuária Sustentável, 2(2), 26-34.
Dores, MT, Nobrega, JE & Ferreira, CLLF. (2013). Room temperature aging to guarantee microbiological safety of Brazilian artisan Canastra-MG cheese. Food Science and Technology, 33(1), 180-85.
Favaro, L, Penna, ALB & Todorov, SD. (2015). Bacteriocinogenic LAB from cheeses – Application in biopreservation? Trends in Food Science & Technology, 41(1), 37-48.
Figueiredo, SP, Boari, CA, Costa Sobrinho, PS, Chaves, ACSD, Silva, RB & Silva, HBF. (2015). Characteristics of raw milk and artisanal cheese produced in Serro-MG, Minas Gerais State, Brazil, in different months. Archives of Veterinary Science, 20(1), 68-81.
Fox, PF, Guinee, TP, Cogan, TM & McSweeney, PLH. (2017). Microbiology of Cheese Ripening. In Fox, PF, Guinee, TP, Cogan, TM & McSweeney, PL (Eds.), Fundamentals of cheese science (p. 333-90). Boston: Springer.
Frank, JF, Yousef, AE & Frank, JF. (2004). Tests for Groups of Microorganisms. In H. M. Wehr, & J. F. Frank (Eds.), Standard methods for the examination of dairy products (p. 227-47). Whashington: American Public Health Association.
Galinari, E, Nóbrega, JE, Andrade, NJ & Ferreira, CLLF. (2014). Microbiological aspects of the biofilm on wooden utensils used to make a Brazilian artisanal cheese. Brazilian Journal of Microbiology, 45(2), 713-20.
Henning, DR, Flowers, R, Reiser, R, Ryser, ET & Frank, JF. (2004). Pathogens in milk and milk products. In H. M. Wehr, & JF. Frank (Eds.), Standard methods for the examination of dairy products (p. 103-51). Whashington: American Public Health Association.
International Organization For Standardization (2004). Cheese and processed cheese. Determination of the total solids content (Reference method). Brussels: International Dairy Federation.
Irlinger, F & Mounier, J. (2009). Microbial interactions in cheese: implications for cheese quality and safety. Current Opinion in Biotechnology, 20(2), 142-48.
Kamimura, BA, Magnani, M, Luciano, WA, Campagnollo, FB, Pimentel, TC, Alvarenga, VO, Pelegrino, BO, Cruz, AG & Sant’Ana, AS. (2019). Brazilian Artisanal Cheeses: An Overview of their Characteristics, Main Types and Regulatory Aspects. Comprehensive Reviews in Food Science and Food Safety, 18(5), 1636-57.
Kornacki, JL, Gurtler, JB & Stawick, BA. (2015). Enterobacteriaceae, Coliforms, and Escherichia coli as Quality and Safety Indicators. In: Salfinger, Y & Tortorello, ML (Eds.), Compendium of methods for the microbiological examination of foods (p. 103-20). Washington: American Public Health Association.
Laird, DT, Gambrel-Lenarz, SA, Scher, FM, Graham, TE, Reddy, R & Maturin, LJ. (2004). Microbiological Count Methods. In: Wehr, HM & Frank, JF (Eds.), Standard methods for the examination of dairy products (p. 153-86). Washington: American Public Health Association.
Lortal, S, Di Blasi, A, Madeca, MN, Pediliggieri, C, Tuminello, L, Tanguya, G, Fauquant, J, Lecuona, Y, Campo, P, Carpino, S & Licitra, G. (2009). Tina wooden vat biofilm: A safe and highly efficient lactic acid bacteria delivering system in PDO Ragusano cheese making. International Journal of Food Microbiology, 132(1), 1-8.
Luiz, LMP, Castro, RD, Sandes, SHC, Silva, JG, Oliveira, LG, Sales, GA, Nunes, AC & Souza, MR. (2016). Isolation and identification of lactic acid bacteria from Brazilian Minas artisanal cheese. Cyta – Journal of Food, 15(1), 125-28.
Martin, JGP, Silva, GO, Fonseca, CR, Morales, CB, Silva, CSP, Miquelluti, DL & Porto, E. (2016). Efficiency of a cleaning protocol for the removal of enterotoxigenic Staphylococcus aureus strains in dairy plants. International Journal of Food Microbiology, 238, 295-301.
Martins, JM, Galinari, E, Pimentel-Filho, NJ, Jr, JIR, Furtado, MM & Ferreira, CL. (2015). Determining the minimum ripening time of artisanal Minas cheese, a traditional Brazilian cheese. Brazilian Journal of Microbiology, 46(1), 219-30.
McSweeney, PLH. (2004). Biochemistry of cheese ripening. International Journal of Dairy Technology, 57(2-3), 127-44.
McSweeney, PLH. (2007). Cheese Problems Solved. Ireland: Woodhead Publishing.
Minas Gerais. (2002). Dispõe sobre o processo de produção de Queijo Minas Artesanal (Decreto N° 42.645, de 05 de junho de 2002). Palácio da Liberdade, Belo Horizonte.
Minas Gerais. (2008). Dispõe sobre o processo de produção de Queijo Minas Artesanal (Decreto N° 44.864, de 01 de agosto de 2008). Belo Horizonte: Diário Oficial do Estado.
Minas Gerais. (2011). Dispõe sobre o processo de produção do Queijo Minas Artesanal e dá outras providências (Lei N° 19.492, de 13 de janeiro de 2011). Belo Horizonte: Palácio Tiradentes.
Minas Gerais. (2018). Dispõe sobre os parâmetros e padrões físico-químico e microbiológicos de alimentos de origem animal e água de abastecimento (Portaria do Instituto Mineiro de Agropecuária N° 1.837, de 05 de julho de 2018). Belo Horizonte: Instituto Mineiro de Agropecuária.
Miranda, GR, Souza, AM, Oliveira Martins, AD, Cocaro, ES & Martins, JM. (2016). Artesan cheese: physical chemical and microbiological quality and evaluation of sanitary conditions of handlers and production environment. Extensão Rural, 23(1), 78-92.
Monteiro, RP. (2018). Queijo Minas Artesanal: Valorizando a Agroindústria Familiar. Brasília-DF: Embrapa Agroindústria de Alimentos.
Moberg, L & Kornacki, JL. (2015). Microbiological Monitoring of the Food Processing Environment. In Y. Salfinger, & M. L. Tortorello (Eds.), Compendium of methods for the microbiological examination of foods (p. 27-40). Washington: American Public Health Association.
Njongmeta, NA, Hall, PA, Ledenbach, L & Flowers, RS. (2015). Acid-Producing Microorganisms. In: Salfinger,Y & Tortorello, ML (Eds.), Compendium of methods for the microbiological examination of foods (p. 229-36). Washington: American Public Health Association.
Oliveira, AL, Cruz, RG, Passo, LP, Alves, LC & Dores, MT. (2017). Characterization of artisanal minas cheese of the mining closure of the region of Alto Paranaíba. The Journal of Engineering and Exact Sciences, 3(6), 824-28.
Pereira, AS, Shitsuka, DM, Parreira, FJ & Shitsuka, R. (2018). Metodologia da pesquisa científica. [e-book]. Santa Maria. Ed. UAB/NTE/UFSM. Disponível em: https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_Metodologia-Pesquisa-Cientifica.pdf?sequence=1.
Pinto, MS, Ferreira, CLLF, Martins, JM, Teodoro, VAM, Santos, ACP, Fontes, LBA & Vargas, PIR. (2009). Food safety of minas traditional cheese of Serro-MG, Minas Gerais state, Brazil, as a result of good manufacturing practices. Pesquisa Agropecuária Tropical, 39(4), 342-47.
Ryser, ET & Schuman, JD. (2015). Mesophilic Aerobic Plate Count. In Salfinger, Y & Tortorello, ML (Eds.), Compendium of methods for the microbiological examination of foods (p. 95-01). Washington: American Public Health Association.
Ryu, D & Wolf-Hall, C. (2015). Yeasts and Molds. In Salfinger, Y & Tortorello, ML (Eds.), Compendium of methods for the microbiological examination of foods (p. 277-97). Washington: American Public Health Association.
Santos, CG, Naves, EAA, Paiva, AD, Vianna, PCB & Toloi, FT. (2017). Hygienie sanitary conditions in production of artesanal cheese made in Uberaba – MG. Revista do Instituto de Laticínios Cândido Tostes, 72(2), 96-07.
Seo, K.S., & Bonach, GA. (2007). Staphylococcus aureus. In Doyle, MP & Beuchat, LR (Eds.), Food microbiology: Fundamentals and frontiers (p. 493-518). Washington: American Society For Microbiology.
Silva, JG, Abreu, LR, Magalhães, FAR, Piccoli, RH & Ferreira, EB. (2011). Physicochemical properties of handcrafted Canastra-MG minas cheese. Revista do Instituto de Laticínios Cândido Tostes, 66(380), 16-22.
Soares, DB, Monteiro, GP, Fonseca, BB, Freitas, EA, Mendonça, EP, Melo, RT, Iasbeck, JR, & Rossi, DA. (2018). Sanitary and physicochemical analysis and bacteriological adequacy of minas artisanal cheese produced in two properties. Ciência Animal Brasileira, 19, 1-13.
Sobral, D, Costa, RGB, Paula, JCJ, Teodoro, VAM, Moreira, GMM & Pinto, MS. (2017). Major defects in artisanal Minas cheese: a review. Revista do Instituto de Laticínios Cândido Tostes, 72(2), 108-120.
Takashi, JA, Lima, GS, Santos, GF, Lyra, HF, Hughes, AFS & Gonçalves, FAG. (2017). Filamentous Fungi and Chemistry: Old Friends, New Allies. Revista Virtual de Química, 9(6), 2351-82.
Teshome, G. (2015). Review on lactic acid bacteria function in milk fermentation and preservation. African Journal of Food Science, 9(4), 170-75.
Verraes, C, Vlaemynck, G, Weyenberg, SV, Zutter, LD, Daube, G, Sindic, M, Uyttendaele, M & Herman, L. (2015). A review of the microbiological hazards of dairy products made from raw milk. International Dairy Journal, 50, 32-44.
Verdier-Metz, I, Michel, V, Delbès, C & Montel, M. (2009). Do milking practices influence the bacterial diversity of raw milk? Food Microbiology, 26(3), 305-10.
Yoon, Y, Lee, S & Choi, K. (2016). Microbial benefits and risks of raw milk cheese. Food control, 63, 201-15.
Zegarra, JJQ, Botteon, RCCM, Oliveira, BCRS, Botteon, PTL & Souza, MM. (2009). Search for microorganisms in utensils, milk and cheese of the craft production in small units of production in Seropédica, Rio de Janeiro. Ciência Animal Brasileira, 10(1), 312-21.
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