Reducing biogenic-amine-producing bacteria, decarboxylase activity, and biogenic amines in raw milk cheese by high-pressure treatments

Applied and Environmental Microbiology

Volumn 79, Issue 4, 2013, Pages 1277-1283

  Calzada, Javier ^a   Del Olmo, Ana ^a   Picón, Antonia ^a   Gaya, Pilar ^a   Nuñez, Manuel ^a  

^a INIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO PEPTIDASE; BIOGENIC AMINES; DECARBOXYLASES; DRY MATTERS; FREE AMINO ACIDS; HEALTH CONCERNS; HIGH-PRESSURE TREATMENT; IN-CONTROL; LACTIC ACID BACTERIA; RAW MILK CHEESE; SUBSTRATE DEPLETION;

AMINES; AMINO ACIDS; BACILLI; LACTIC ACID;

CHEESES;

BIOGENIC AMINE; CARBOXYLYASE;

AMINO ACID; BACTERIUM; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; HIGH PRESSURE; LIMITING FACTOR; MILK; PUBLIC HEALTH; SUBSTRATE;

ANIMAL; ARTICLE; BACTERIAL LOAD; CHEESE; CHEMISTRY; DISINFECTION; FOOD HANDLING; HYDROSTATIC PRESSURE; ISOLATION AND PURIFICATION; LACTOBACILLALES; METABOLISM; METHODOLOGY; MICROBIOLOGY; MILK; TIME;

ANIMALS; BACTERIAL LOAD; BIOGENIC AMINES; CARBOXY-LYASES; CHEESE; DISINFECTION; FOOD TECHNOLOGY; HYDROSTATIC PRESSURE; LACTOBACILLALES; MILK; TIME FACTORS;

EID: 84874747930     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03368-12     Document Type: Article

References (38)

1. Silla-Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29:213-231.
2. Til HP, Falke HE, Prinsen MK, Willems MI. 1997. Acute and subacute toxicity of tyramine, spermidine, spermine, putrescine and cadaverine in rats. Food Chem. Toxicol. 35:337-348.
3. Stratton JE, Hutkins RW, Taylor SL. 1991. Biogenic amines in cheese and other fermented foods. J. Food Prot. 54:460-470.
4. Hotchkiss JH, Scanlan RA, Libbey LM. 1977. Formation of bis(hydroxyalkyl)-n-nitrosamines as products of nitrosation of spermidine. J. Agric. Food Chem. 25:1183-1189.
5. Eliassen KA, Reistad R, Risøen U, Rønning HF. 2002. Dietary polyamines. Food Chem. 78:273-280.
6. ten Brink B, Damink C, Joosten HMLJ, Huis in't Veld JHJ. 1990. Occurrence and formation of biologically-active amines in foods. Int. J. Food Microbiol. 11:73-84.
7. Taylor SL. 1986. Histamine food poisoning: toxicology and clinical aspects. Crit. Rev. Toxicol. 17:91-128.
8. Halász A, Baráthá, Simon-Sarkadi L, Holzapfel W. 1994. Biogenic amines and their production by microorganisms in food. Trends Food Sci. Technol. 5:42-49.
9. Komprda P, Burdychová R, Dohnal V, Cwiková O, Sládková P. 2008. Some factors influencing biogenic amines and polyamines content in Dutch-type semi-hard cheese. Eur. Food Res. Technol. 227:29 -36.
10. Joosten HMLJ, Northolt MD. 1987. Conditions allowing the formation of biogenic amines in cheese. 2. Decarboxylase properties of some nonstarter bacteria. Neth. Milk Dairy J. 41:259 -280.
11. Sarantinopoulos P, Andrighetto C, Georgalaki MD, Rea MC, Lombardi A, Cogan TM, Kalantzopoulos G, Tsakalidou E. 2001. Biochemical properties of enterococci relevant to their technological performance. Int. Dairy J. 11:621-647.
12. Krause I, Bockhardt A, Klostenmeyer H. 1997. Characterization of cheese ripening by free amino acids and biogenic amines and influence of bactofugation and heat-treatment of milk. Lait 77:101-108.
13. Lanciotti R, Patrignani F, Iucci L, Guerzoni ME, Suzzi G, Belletti N, Gardini F. 2007. Effects of milk pressure homogenization on biogenic amine accumulation during ripening of ovine and bovine Italian cheeses. Food Chem. 104:693-701.
14. Novella-Rodríguez S, Veciana-Nogués MT, Trujillo-Mesa AJ, Vidal-Carou MC. 2002. Profile of biogenic amines in goat cheese made from pasteurized and pressurized milks. J. Food Sci. 67:2940 -2944.
15. Ordóñez AI, Ibañez FC, Torre P, Barcina Y. 1997. Formation of biogenic amines in Idiazábal ewe's-milk cheese: effect of ripening, pasteurization and starter. J. Food Prot. 60:1371-1375.
16. Joosten HMLJ, Nuñez M. 1996. Prevention of histamine formation in cheese by bacteriocin-producing lactic acid bacteria. Appl. Environ. Microbiol. 62:1178 -1181.
17. Rabie MA, Siliha HI, El-Saidy SM, El-Badawy AA, Malcata FX. 2011. Effect of -irradiation upon biogenic amine formation in blue cheese during storage. Int. Dairy J. 21:373-376.
18. Arqués JL, Garde S, Gaya P, Medina M, Nuñez M. 2006. Inactivation of microbial contaminants in raw milk La Serena cheese by high pressure treatments. J. Dairy Sci. 89:888-891.
19. O'Reilly CE, O'Connor PM, Kelly AL, Beresford TP, Murphy PM. 2000. Use of hydrostatic pressure for inactivation of microbial contaminants in cheese. Appl. Environ. Microbiol. 66:4890-4896.
20. Novella-Rodríguez S, Veciana-Nogués MT, Saldo J, Vidal-Carou MC. 2002. Effects of high hydrostatic pressure treatments on biogenic amine contents in goat cheeses during ripening. J. Agric. Food Chem. 50:7288-7292.
21. Børresen T, Klausen NK, Larsen LM, Sørensen H. 1989. Purification and characterization of tyrosine decarboxylase and aromatic-L-amino-acid decarboxylase. Biochim. Biophys. Acta 993:108 -115.
22. Linares D, Del Rio B, Ladero V, Martinez N, Fernandez M, Martin MC, Alvarez MA. 2012. Factors influencing biogenic amines accumulation in dairy products. Front. Microbiol. 3:180. doi:10.3389/fmicb.2012.00180.
23. Pircher A, Bauer F, Paulsen P. 2007. Formation of cadaverine, histamine, putrescine and tyramine by bacteria isolated from meat, fermented sausages and cheeses. Eur. Food Res. Technol. 226:225-231.
24. Gaya P, Sánchez C, Fernández-García E, Nuñez M. 2005. Proteolysis during ripening of Manchego cheese made from raw or pasteurized ewes' milk. Seasonal variation. J. Dairy Res. 72:287-295.
25. Mayer HK, Fiechter G, Fischer E. 2010. A new ultra-pressure liquid chromatography method for the determination of biogenic amines in cheese. J. Chromatogr. A 1217:3251-3257.
26. O'Reilly CE, Kelly AL, Oliveira JC, Murphy PM, Auty MAE, Beresford TP. 2003. Effect of varying high-pressure treatment conditions on acceleration of ripening of cheddar cheese. Innov. Food Sci. Emerg. Technol. 4:277-284.
27. Joosten HMLJ, Northolt MD. 1989. Detection, growth and amine producing capacity of lactobacilli in cheese. Appl. Environ. Microbiol. 55: 2356-2359.
28. Rodríguez E, Arqués JL, Nuñez M, Gaya P, Medina M. 2005. Combined effect of high-pressure treatments and bacteriocin-producing lactic acid bacteria on the inactivation of Escherichia coli O157:H7 in raw milk cheese. Appl. Environ. Microbiol. 71:3399 -3404.
29. González de Llano D, Cuesta P, Rodríguez A. 1998. Biogenic amine production by wild lactococcal and leuconostoc strains. Lett. Appl. Microbiol. 26:270 -274.
30. Chaves-López C, De Angelis M, Martuscelli M, Serio A, Paparella A, Suzzi G. 2006. Characterization of the Enterobacteriaceae isolated from an artisanal Italian ewe's cheese (Pecorino Abruzzese). J. Appl. Microbiol. 101:353-360.
31. Connil N, Le Breton Y, Dousset X, Auffray Y, Rincé A, Prévost H. 2002. Identification of the Enterococcus faecalis tyrosine decarboxylase operon involved in tyramine production. Appl. Environ. Microbiol. 68:3537-3544.
32. Rossi F, Gardini F, Rizzotti L, La Gioia F, Tabanelli G, Torriani S. 2011. Quantitative analysis of histidine decarboxylase gene (hdcA) transcription and histamine production by Streptococcus thermophilus PRI60 under conditions relevant to cheese making. Appl. Environ. Microbiol. 77:2817-2822.
33. Leuschner RG, Heidel M, Hammes WP. 1998. Histamine and tyramine degradation by food fermenting microorganisms. Int. J. Food Microbiol. 39:1-10.
34. Herrero-Fresno A, Martínez N, Sánchez-Llana E, Díaz M, Fernández M, Martin MC, Ladero V, Alvarez MA. 2012. Lactobacillus casei strains isolated from cheese reduce biogenic amine accumulation in an experimental model. Int. J. Food Microbiol. 157:297-304.
35. Malone AS, Shellhammer TH, Courtney PD. 2002. Effects of high pressure on the viability, morphology, lysis, and cell wall hydrolase activity of Lactococcus lactis subsp. cremoris. Appl. Environ. Microbiol. 68:4357-4363.
36. Yvon M, Rijnen L. 2001. Cheese flavor formation by amino acid catabolism. Int. Dairy J. 11:185-201.
37. Fernández-García E, Tomillo J, Nuñez M. 1999. Effect of added proteinases and level of starter culture on the formation of biogenic amines in raw milk Manchego cheese. Int. J. Food Microbiol. 52:189 -196.
38. Leuschner RGK, Kurihara R, Hammes WP. 1998. Effect of enhanced proteolysis on formation of biogenic amines by lactobacilli during Gouda cheese ripening. Int. J. Food Microbiol. 44:15-20.