Psychrotrophic microorganisms in raw milk and the cheese quality

Authors

DOI:

https://doi.org/10.33448/rsd-v9i9.7217

Keywords:

Refrigeration; Enzymes; Good practices.

Abstract

Psychrotrophic microorganisms, especially Pseudomonas spp., are present in the microbiota of refrigerated milk as they can grow at refrigeration temperatures irrespective of their optimal growth temperature. Psychrotrophic counts ranging from 105 to 108 CFU/mL in refrigerated raw milk effect cheese quality, since the synthesized thermoresistant enzymes affect the nutritional value, sensory properties, and texture. Cheese is the dairy product with the highest growth rate in the food industry in Brazil in recent years and meets the current consumption trends of nutritious and practical foods. The objective of this review was to address the importance and influence of the psychrotrophic raw milk microbiota on the quality and sensory properties of cheese. The enzymes produced by psychrotrophic microorganisms lead to taste changes, undesirable clotting times, increased concentrations of free fatty acids and free amino acids, and a reduced shelf-life, in addition to negatively affecting cheese yields. Proteases from psychrotrophs are also associated with slicing problems and progressive loss of the elasticity of cheese, a bitter taste, and increased clotting times of cheese produced with pasteurized milk. On the other hand, their lipases increase the clotting time and have a negative effect on the sensory properties by providing a rancid, soap, metallic, or oxidized smell and taste. The control of the psychrotrophic population found in refrigerated raw milk contributes to better cheese production yields and desirable texture and sensory properties, which extends the shelf-life of cheese and improves consumer acceptance.

References

Aehle, W. (2007). Industrial enzymes. In Enzymes in Industry: Production and Applications (3rd ed.), 140. Netherlands: Wiley- VCH.

Aguiar, B. M., Longhi, R., Poli-Frederico, R. C., Fagnani, R. & Santana, E. H. W. (2019). Lipoproteolytic capacity and potential of Pseudomonas spp. isolated from cold raw milk. Journal of. Dairy Research, 86 (4), 467–469. doi:10.1017/ S0022029919000645

Al-Rodhan, A. M., & Nasear, H. A. (2015). PCR - based detection of Pseudomonas fluorescens in cows and buffaloes raw milk. Basrah Journal of Veterinary Research,15 (1),194-208.

Arslan, S., Eyi, A., & Ozdemir, F. (2011). Spoilage potentials and antimicrobial resistance of Pseudomonas spp. isolated from cheeses. Journal of Dairy Science, 94 (12), 5851-5856. doi: 10.3168/jds.2011-4676

Arcuri, E. F., Brito, V. P., Brito, J. R. F., Pinto, S. M., Ângelo, F. F., & Souza, G. N. (2006) Microbiological quality of refrigerated milk on farms. Brazilian Journal of Veterinary and Animal Sciences, 58 (3), 440-446. doi: 10.1590/S0102-09352006000300024

Arcuri, E. F., Silva, P. D. L, Brito, M. A. V. P., Brito, J. R. F.; Lange, C. C., & Magalhães, M. M. A. (2008). Counting, isolation and characterization of psychrotrophic bacteria from refrigerated raw milk. Ciência Rural, 38 (8), 2250-2255. doi: 10.1590/S0103-84782008000800025

Ayyash, M. M. & Shah, N. P. (2011). The effect of substitution of NaCl with KCl on chemical composition and functional properties of low-moisture Mozzarella cheese. Journal of Dairy Science, 94 (8), 3761-3768. doi: 10.3168/jds.2010-4103

Baglinière, F; Mateos, A., Tanguy, G., Jardin, J., ValérieBriard-Bion, V., Rousseau, F. , Robert, B., Beaucher, E., Gaillard, J.L., Amiel, C., Humbert, G., Dary, A. G Gaucheron, F. (2013) Proteolysis of ultra high temperature-treated casein micelles by AprX enzyme from Pseudomonas fluorescens F induces their destabilization. International Dairy Journal, 31, 55–61. doi: 10.1016/j.idairyj.2013.02.011

Cleto, S., Matos, S., Kluskens, L. & Vieira, M. J. (2012). Characterization of contaminants from a sanitized milk processing plant. Plos One, 7 (6), 40-189. doi: 10.1371/journal.pone.0040189

Cousin, M. A. (1982). Presence and activity of psychrotrophic microorganisms in milk and dairy products: a review. Journal of Food Protection, 45 (2), 172-207. doi: 10.4315/0362-028X-45.2.172

Bramley, A. J., & McKinnon, C. H. (1990). The microbiology of raw milk. In R. K. Robinson (Ed), Dairy Microbiology (pp. 163-208).London: Elsevier Science Publishers.

Becker, T. A., Negrelo, I. F., Racoulte, F., & Drunkler, D. L. (2010). Evaluation of the sanitary quality of integral milk in nature, pasteurized, UHT and powder commercialized in Medianeira and Serranópolis do Iguaçu – Paraná. Semina Ciencias Agrarias, 31 (3), 707- 716. doi: 0.5433/1679-0359.2010v31n3p707

Brasil. Ministério da Agricultura, Pecuária e Abastecimento (MAPA) (2018). Instrução Normativa 76 de novembro de 2018. Aprova os Regulamentos Técnicos que fixam a identidade e as características de qualidade que devem apresentar o leite cru refrigerado, o leite pasteurizado e o leite pasteurizado tipo A. Retrieved from http://www.in.gov.br/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/52750137/do1-2018-11-30-instrucao-normativa-n-76-de-26-de-novembro-de-2018-52749894IN%2076

Cempírková, R., Mikulová, M., & Trávníček, J. (2009). Counts of psychrotrophic lipolytic bacteria in cow’s raw milk samples from the aspect of technological quality. Journal of. Agrobiology, 26 (2), 113-121.

Chambers, J. V. (2002).The microbiology of raw milk. In R. K. Robinson (Ed) Dairy Microbiology Handbook, (3rd ed.), 39-90. Nova York: John Willey and Sons Inc.

Champagne, C. P., Laing, R. R., Roy, D., Mafu, A. A., & Griffiths, M. W. (1994). Psychrotrophs in dairy products: Their effects and their control. Critical Reviews in Food Science and Nutrition, 34 (1), 1-30. doi: 10.1080/10408399409527671

Chen, L., Daniel, R. M. & Collbera, T. (2003). Detection and impact of protease and lipase activities in milk and milk powders. International Dairy Journal, 13 (4), 255-275. doi: 10.1016 / S0958-6946 (02) 00171-1

Costa, L. M., Gomez, F. S., Molina, L. H. C., Simpson, R. R., & Romero, A. M. (2002). Purification and characterization of proteases from Pseudomonas fluorescens and their effects on milk proteins. Archivo Latinoamericano de Nutricion, 52 (2), 1-13.

Cousin, M. A. (1989). Physical and biochemical effects on milk components.In R. C. Mckellar, Enzymes of Psychrotrophs in raw milk (pp. 2016-221). Florida: CRC Press.

Decimo, M., Morandi, S., Silvetti, T., & Brasca, M. (2014). Characterization of gram-negative psychrotrophic bacteria isolated from Italian bulk tank milk. Journal of Food Science, 79 (10), 2081-2090. doi: 10.1111/1750-3841.12645

De Kruif, C. G., & Holt, C. (2003). Casein micelle structure, functions and interactions. In P.F. Fox & P. L. H. Mcsweeney, Advanced Dairy Chemistry- 1 proteins, (3a ed.), 233-276. Boston: Springer.

Deeth, H. C., & Fitz-Gerald, C. H. (2006) Lipolytic enzymes and hydrolytic rancidity. In P.F. Fox & P. L. H. Mcsweeney, Advanced dairy chemistry: lipids, (3rd ed.), 481-556. Nova York: Springer.

Deeth, H. C. (2011). Milk lipids:Lipolysis and hydrolytic rancidity. In J. W Fuquay, P.F. Fox & P. L. H. Mcsweeney Encyclopedia of Dairy Sciences, (2nd ed.), 721-726. Australia: Elsevier.

Dogan, B., & Boor, K. J. (2003). Genetic diversity and spoilage potentials among Pseudomonas spp. isolated from fluid milk products and dairy processing plants. Applied and Environmental Microbiology, 69 (1), 130-138. doi: 10.1128/aem.69.1.130-138.2003

Downey, W. K. (1980). Review of the progress of dairy science: flavor impairment from pre- and post-manufacture lipolysis in milk and dairy products. Journal of Dairy Research, 47 (2), 237-252. doi: 10.1017/S0022029900021117

Ercolini, D., Russo, F., Ferrocino, I., & Villani, F. (2009). Molecular identification of mesophilic and psychrotrophic bacteria from raw cow’s milk. Food Microbiology, 26 (2), 228-231. doi: 10.1016 / j.fm.2008.09.005

Fagundes, C. M., Fischer, V., Silva, W. P., Carbonera, N., & Araújo, M. R. (2006). Presence of Pseudomonas spp in milking phases with different hygienic handling procedures and in refrigerated milk. Ciencia Rural, 36 (2), 568-572. doi: 10.1590/S0103-84782006000200032

Frank, J. F., & Yousef, A. E. (2004). Tests for groups of microorganisms. In R. T. Marshall, Standard methods for the examination of dairy products, (16th ed.), 227-247. Nova York: American Public Health Association: Nova York, 1992.

Fao. Food and Agriculture Organization of the United Nations (2020). Dairy market review. Overview of global dairy market developments in 2019. Retrieved from http://www.fao.org/3/ca8341en/CA8341EN.pdf

Fao, Food and Agriculture Organization of the United Nations (2019). Gateway to dairy production and products. Milk composition. Retrieved from http://www.fao.org/dairy-production-products/products/milk-composition/en/.

Fox, P. F.; Mcsweeney, P. L. H. (1998). Dairy Chemistry and Biochemistry. Londres: Thomson Science.

Fox, P. F., Mcsweeney, P. L. H., Cogan, T. M. & Guinee, T. P. (2004). Cheese: chemistry, physics and microbiology: General Aspects, (3rd ed.), Londres: Elsevier Academic Press.

Gasparini, G. B. F. B., Amorim, F. R., Correa, S. S., Bruzaroski, S. R., Fagnani, R., Souza, C. H. B., Domião, B. C. M. & Santana, E. H. W. (2020). Psychrotrophs in raw milk: effect on texture, proteolysis index, and sensory evaluation of smoked provolone cheese. Journal of the Science Food and Agriculture, 100 (8), 3291-3296. doi: 10.1002/jsfa.10329

Goursaud, J. (1991). Composición y propriedades físico-químicas. In F. M Luquet, Leche y productos lácteos. La leche de la mama a la lechería (pp. 3-92). Zaragoza: Acribia.

Hammad, A. M. (2015). Spoilage Potential of Pseudomonas spp. isolated from Domiati Cheese. Assiut Veterinary Medical Journal, 61 (147), 18-23.

Haryani, S., Datta, N., Elliott, A. J. &Deeth, H. (2003). Production of proteinases by Psychrotrophic bacteria in raw milk stored at low temperature. Australian Journal of Dairy Technology, 58 (1), 15-20.

Jensen, R. G., & Newburg, D. S. (1995). Bovine milk lipids. In R. G Jensen, Handbook of milk composition (pp. 543-575). San Diego: Academic Press.

Jonghe, V., Coorevits, A., Hoorde, K. V., Messens, W., Landschoot, A. V., Vos, P., & Heyndickx, M. (2011). Influence of storage conditions on the growth of Pseudomonas species in refrigerated raw milk. Applied and Environmental Microbiology, 77( 2), 460-470. doi: 10.1128 / AEM.00521-10

Kindstedt, P. S., & Fox, P. F. (1993). Effect of manufacturing factors, composition, and proteolysis on the functional characteristics of Mozzarella cheese. Critical Reviews in Food Science and Nutrition, 33 (2), 167-187. doi: 10.1080/10408399309527618

Kumaresan, G., Annalvilli, R. & Sivakumar, K. (2007). Psychrotrophic spoilage of raw milk at different temperatures of storage. Journal of Applied Sciences Research, 3(1), 1383-1387.

Lawrence, R. C., Creamer, L. K., & Gilles, J. (1987). Texture development during cheese ripening. Journal of Dairy Science, 70 (8), 1748-1760. doi: 10.3168/jds.S0022-0302(87)80207-2

Mahieu, H. (1991). Modificaciones de la leche después de su recogida.In F. M. Luquet, Leche y productos lácteos. la leche de la mama a la lechería (pp. 22-181). Zaragoza: Acribia.

Mendoza, J. (2020). Brazil: cheese production volume 2010-2019. Retrieved from https://www.statista.com/statistics/1004455/brazil-cheese-production-volume/#statisticContainer

Mcauley, C. M., Singh, T. K., Haro-Maza, J. F., Williams, R. & Buckow, R. (2016) Microbiological and physicochemical stability of raw, pasteurised or pulsed electric field-treated milk. Innovative Food Science and Emerging Technologies, 38, 365-373. doi: 10.1016/j.ifset.2016.09.030

Mcphee, J. D., & Griffiths, M. W. (2011). Psychrotrophic bacteria Pseudomonas spp. In W. F John, Encyclopedia of Dairy Sciences, (2nd ed.),379-383. San Diego, Academic Press.

Molineri, A. I., Signorini, M. L., Cuatrín, A. L., Canavesio, V. R., Neder, V. E., Russi, N. B., Bonazza, J. C. & Calvinho, L. F. (2012). Association between milking practices and psychrotrophic bacterial counts in bulk tank milk. Revista Argentina de Microbiologia, 44(3), 187-194.

Moyer, C. L. & Morita, R. Y. (2007). Psychrophiles and psychrotrophs. In R. Y. Morita, Encyclopedia of Life Sciences,1-6. Chichester: John Wiley & Sons Ltd.

Muir, D. D. (1996). The Fresh-life of Dairy Products: 1. Factors Influencing Raw Milk and Fresh Products. International Journal of Dairy Technology, 49 (1), 24-32. doi: 10.1111/j.1471-0307.1996.tb02616.x

Neubeck, M., Baur, C., Krewinkel, M., Stoeckel, M., Kranz, B., Stressler, T., Fischer, L., Hinrichs, J., Scherer, S. & Wenning, M. (2015). Biodiversity of refrigerated raw milk microbiota and their enzymatic spoilage potential. International Journal of Food Microbiology, 211(15), 57-65. doi: 10.1016/j.ijfoodmicro.2015.07.001

Nielsen, S. S. (2002). Plasmin system and microbial proteases in milk: characteristics, roles and relationship. Journal of Agricultural and Food Chemistry, 50 (22), 6628-6624. doi: 10.1021/jf0201881

Nornberg, M. F. B. L., Tondo, E. C. & Brandelli, A. (2009). Bactérias psicrotróficas e atividade proteolítica no leite cru refrigerado. Acta Scientiae Veterinariae, 37 (2), 157-163. doi: 10.22456/1679-9216.16243

Nuñez, M., & Nuñez, J. A. (1983). Proteasas de psicrotrofos gram negativos. Efectos sobre la leche y los productos lácteos. Revista Espanhola de Leche, 130, 251-260

Oliveira, G. B., Favarin. L., Luchese, R. H. & Mclintosh, D. (2015). Psychrotrophic bacteria in milk: How much do we really know?. Brazilain Journal of Microbiology, 46 (2), 313-321. doi: 10.1590 / S1517-838246220130963

Olivecrona, T., Vilaro, S., & Olivecrona, G.(2003). Lipases in milk. In P. F Fox &P. Mcsweeney, Advanced Dairy Chemistry: Protein, 473-494. Nova York: Kluwer Academic.

Ordonez-Pereda, J. A., Rodriguez, M. I. C., Alvarez, L. F.;,Garcia-Sanz, M. L., Minguillón, G. G. F., Hoz-Perales, L. & Cortecero, M. D. S.(2005). Tecnologia de alimentos: componentes dos alimentos e processos, Vol 2. Porto Alegre: Artmed.

Pereira, A. S., Shitsuka, D. M., Parreira, F. J. & Shitsuka, R (2018). Methodology of cientific research. [e-Book]. Santa Maria: UAB / NTE / UFSM. Retrieved from https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_Metodologia-Pesquisa-Cientifica.pdf?sequence=1

Pereira, F. A. B., Luiz, L. L., Bruzaroski, S. R., Poli-Frederico, R. C., Fagnani, R. & Santana, E. H. W. (2019). The effect of cold storage, time and the population of Pseudomonas species on milk lipolysis. Grasas y Aceites, 70 (2), e300. doi: 10.3989/gya.0583181

Ray, P. R., Chatterjee, K., Chakraborty, C. & Ghatak, P. K. (2013). Lipolysis of milk: a review. International Journal of Agricultural Sciences and Veterinary, 1 (1), 58-74.

Recio, I., Garcia-Risco, M. R., Ramos, M. & López-Fandiño, R. (2000). Characterization of peptides produced by action of psychrotrophic protease on κ-casein. Journal of Dairy Research, 67 (4), 625-630. doi: 10.1017 / S002202990000443X

Ribeiro, A. C. P., Bruzaroski, S. R., Pereira, F. A. B., Paião, F. G., Poli-Frederico, R. C., Santos, J. S. & Santana, E. H. W. (2018). Proteolytic behavior of isolated Pseudomonas spp. from refrigerated raw milk in different concentrations and storage temperatures. Semina: Ciências Agrárias, 39 (1), 419-424. doi: 10.5433/1679-0359.2018v39n1p419

Ribeiro Júnior, J. C., Oliveira, A. M., Silva, F. G., Tamanini, R., Oliveira, A. L. M. & Beloti, V. (2018). The main spoilage related psychrotrophic bacteria in refrigerated raw milk. Journal of Dairy Science, 101 (1), 75-83. doi: 10.3168 / jds.2017-13069

Robinson, R. K. (1980). The Microbiology of Milk. In Dairy Microbiology, (2nd ed.), Londres: Elsevier Science Ltda.

Samarzija, D., Zamberlin, S. & Pogacic, T. (2012). Psychrotrophic bacteria and milk and dairy products quality. Mljekarstvo, 62 (2), 75-95.

Scatamburlo, T. M., Yamazi, A. K., Cavicchioli, V. Q., Pieri, F. A. & Nero, L. A. (2015). Spoilage potential of Pseudomonas species isolated from goat milk. International Journal of Dairy Science, 98 (2), 759-764. doi: 10.3168/jds.2014-8747

Shah, N. P. (1994). Psychotrophs in milk: a review. Milchwissenschaft, 49 (8), 432-437.

Singh, V., Kaushal, S., Tyagi, A. & Sharma, P. (2011). Screening of bacteria responsible for the spoilage of milk. Journal of Chemical and Pharmaceutical Research, 3 (4), 348-350.

Sorhaug, T.; Stepaniak, L. (1997). Psychrotrophs and their enzymes in milk and dairy produts: quality aspects. Trends in Food Science and Technology, 8 (2), 35-37. doi: 10.1016/S0924-2244(97)01006-6

Statista (2020). Cheese Brazil. Retrieved from https://www.statista.com/outlook/40010400/115/cheese/brazil (accessed June 01, 2020).

Szczesniak, A. S. (2002). Texture is a sensory property. Food Quality and Preference, 13 (4), 215-225. doi: 10.1016/S0950-3293(01)00039-8

Tolle, A. (1980). The microflora of the udder. Factors Influencing the Bacteriological Quality of Raw Milk. Bulletin of the International Dairy Federation, Document 120.

Walstra, P., Wouters, J. T. M. & Geurts, T. J. (2006) Dairy science and technology, (2nd ed.) Boca Raton: CRC Press.

Walstra, P. (1999). Casein sub-micelles: do they exist?. International Dairy Journal,9 (3-6), 189-192. doi: 10.1016 / s0958-6946 (99) 00059-x

Wiedmann, M., Weilmeier, D., Dineen, S. S., Ralyea, R. & Boor, K. J. (2000). Molecular and phenotypic characterization of Pseudomonas spp. isolated from milk. Applied and Environmental Microbiology, 66 (5), 2085-2095. doi: 10.1128/aem.66.5.2085-2095.2000

Wiking, L., Frøst, M. B., Larsen, L. B. & Nielsen, J. H. (2002). Effects of storage condition on lipolysis, proteolysis and sensory attribute in high quality raw milk. Milchwissenschaft, 57 (4), 190-194.

Xin, L., Meng, Z., Zhang, L., Cui, Y., Han, X. & Yi, H. (2017 a) The diversity and proteolytic properties of psychrotrophic bacteria in raw cows’ milk from North China. International Dairy Journal, 66, 34-41. doi: 10.1016/j.idairyj.2016.10.014

Xin, L., Zhang, L., Menh, Z.; Di, W., Han, X., Yi, H. & Cui, Y. (2017 b). Lipolytic psychrotrophic bacteria and lipase heat-resistant property in bovine raw milk of North China Journal of Food Processing and Preservation, e13289, 1-6. Doi:10.1111/jfpp.13289

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14/08/2020

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SANTANA, E. H. W. de; LUIZ, L. L. .; PASQUIM, P. da S. .; PINTO, L. de F. B. .; PEREIRA, F. de A. B. .; GASPARINI, G. B. F. B. .; LORENZETTI, E. .; BRUZAROSKI , S. R. .; ELEODORO, J. I. . Psychrotrophic microorganisms in raw milk and the cheese quality. Research, Society and Development, [S. l.], v. 9, n. 9, p. e127997217, 2020. DOI: 10.33448/rsd-v9i9.7217. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/7217. Acesso em: 18 apr. 2024.

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Review Article