Abstract
Enterobacteriaceae (EB, n = 149), Lactobacillus (LB, n = 162) and Leuconostoc sp. (LC, n = 89) and enterococci (EC, n = 137), isolated from raw meat (n = 65), fermented sausages (n = 50) and cheese (n = 55) samples, were cultivated in a broth containing precursor amino acids (each 3 g/l). After incubation, the liquid culture was chemically analysed for cadaverine (CAD), putrescine (PUT), histamine (HIS) and tyramine (TYR) formation at pH 5.2 and at pH 6.7. The majority of EB isolates (147 of 149) was capable of forming >100 mg/l of either CAD or PUT. Among the most frequently isolated species Hafnia alvei and Serratia liquefaciens, formation of >100 mg/l HIS occurred, but with low prevalence (1.6 and 6.5%, respectively). Twelve of 149 isolates (8%) were able to produce more than 10 mg/l HIS. One hundred forty-two isolates (95.3%) produced less than 10 mg/l TYR, and 7 isolates (4.7%) 10 mg/l to a maximum of 35.3 mg/l TYR. For LB + LC, one isolate (Leuconostoc mesenteroides ssp. mesenteroides) formed >100 mg/l PUT and one >100 mg/l CAD (of all 251 LB + LC isolates 0.4% each). Formation of >100 mg/l HIS and TYR was detected in 3.6 and 19% of the LB + LC isolates, respectively. For the EC isolates, maximum levels for PUT, CAD and HIS were 25.4 mg/l, 6.0 mg/l and 15.7 mg/l, respectively. TYR was formed in quantities of 100–1000 mg/l by 47.9% of EC faecalis (n = 75), and 59.7% of EC faecium (n = 62) isolates. More than 1000 mg/l TYR were formed by 50.7 and 35.5% of the isolates, respectively. A low initial pH of 5.2 compared to the initial pH of 6.7 favoured tyramine production by lactic acid bacteria, but was associated with lower CAD yield by EB.
A considerable intra-species variability in amine formation was observed.
Similar content being viewed by others
References
Beutling D (1996) Biogene Amine in der Ernährung. Springer, Wien Berlin New York
Bardocz S (1995) Trends Food Sci Tech 6(19):341–346
Stratton JE, Hutkins RW, Taylor SL (1991) J Food Prot 54(6):460–470
Dainty RH, Edwards RA, Hibbard CM, Ramantanis SV (1986) J Appl Bacteriol 61:117–123
Edwards RA, Dainty RH, Hibbard CM (1983) J Food Technol 18(6):777–788
Vinci G, Antonelli ML (2002) Food Control 13(8):519–524
Lüthy J, Schlatter C (1983) Z Lebensm Unters Forsch 177:439–443
Shalaby AR (1996) Food Res Int 29(7):675–690
Lehane L, Olley J (2000) Int J Food Microbiol 58:1–37
Maijala R, Eerola S (1993) Meat Sci 35:387–395
Maijala R (1993) Lett Appl Microbiol 17(1):40–43
Eerola S, Maijala R, Roig-Sagues AX, Salminen M, Hirvi T (1996) J Food Sci 61(6):1243–1246
Paulsen P, Bauer F (1997) Fleischwirtschaft 77(4):362–364
Kalac P, Spicka J, Krizek M, Pelikanova T (2000) Food Chem 70(3):355–359
Bover-Cid S, Hugas M, Izquierdo-Pulido M, Vidal-Carou MC (2001) Int J Food Microbiol 66:185–189
Spicka J, Kalac P, Bover-Cid S, Krizek M (2002) Eur Food Res Technol 215(6):515–519
Beutling D (1994) Arch Lebensmittelhyg 47(4):97–102
Suzzi G, Gardini F (2003) Int J Food Microbiol 88(1):41–54
Bover-Cid, S, Holzapfel WH (1999) Int J Food Microbiol 53:33–41
Weber H (1996) Mikrobiologie der Lebensmittel: Fleisch und Fleischerzeugnisse. Behrs’, Hamburg, Germany, pp 313–338
Zickrick K (1996) In: Weber H (ed) Mikrobiologie der Lebensmittel: Milch und Milchprodukte. Behrs’, Hamburg, Germany, pp 255–352
Mietz JL, Karmas E (1977) J Food Sci 42:155–158
Lozan L, Kausch H (1998) Angewandte Statistik für Naturwissenschaftler. Parey, Berlin, pp 127–129
Özogul F, Özogul Y(2006) Eur J Food Res Technol. DOI 10.1007/s00217-006-0429-3
Kordesch M (1996) Formation of biogenic amines during storage and spoilage of modified-atmosphere packaged meat. Thesis. Univ Vet Med, Vienna, 96p
Pötzelberger D (1996) Formation of biogenic amines during storage and spoilage of packaged raw meat, Thesis. Univ Vet Med, Vienna, Austria, 149p
Anonymous (1993) Oxoid manual, 5th edn. Unipath Corp, Wesel, Germany
Behling AR, Taylor SL (1982) J Food Sci 47:1311–1314, 1317
Pircher A (2004) Die Bildung biogener Amine durch Mikrorganismen, isoliert aus Fleisch, Käse und Rohwürsten aus dem Wiener Raum, Thesis. Univ Vet Med, Vienna, 97p
Koessler KK, Hanke MT, Sheppard MS (1928) J Infect Dis 43:363–377
Diaz-Cinco ME, Fraijo G, Grajeda P, Lozano-Taylor J, Gonzalezde E (1992) J Food Sci 57:355–365
Teodorovic V, Buncic S (1999) Fleischwirtschaft 5:85–88
Bearson S, Bearson B, Foster JW (1997) FEMS Microbiol Lett 147(2):173–180
Chander H, Batish VH, Babu S, Singh RS (1989) J Food Sci 54:940–942
Straub BW, Tichaczek PS, Kicherer H, Hammes WP (1994) Z Lebensm Unters Forsch 199:9–12
Maijala R, Eerola S, Lievonen S, Hill P, Hirvi T (1993) J Food Prot 56:125–129
Silla-Santos MH (1998) Int J Food Microbiol 39:227–230
Marino M, Maifreni M, Moret S, Rondinini G (2000) Lett Appl Microbiol 31:169–173
Durlu-Özkaya F, Ayhan K, Vural N (2001) Meat Sci 58(2):163–166
Moreno-Arribas MV, Polo MC, Jorganes F, Munoz R (2003) Int J Food Microbiol 84:117–123
Joosten HMLJ, Northolt MD (1989) Appl Environ Microbiol 55:2356–2359
Gonzalez de Llano D, Cuesta P, Rodriguez A (1998) Lett Appl Microbiol 26:270–274
Giraffa G, Pepe G, Locci F, Neviani E, Carminati D (1995) Ital J Food Sci 7(4):341–349
Galgano F, Suzzi G, Favati F, Caruso M, Martuschelli M, Gardini F, Sakzani G (2001) Int J Food Sci Technol 36:153–160
Cosentino S, Pisano MB, Corda A, Fadda ME, Piras C (2004) J Dairy Res 71(4):444–450
Brandl E, Asperger H, Pfleger F, Iben C (1985) Arch Lebensm Hygiene 36(1):18–22
Paulsen P, Bauer F (2006) Eur Food Res Technol. DOI 10.007/s00217-006-0464-0
Hagen U, Bauer F, Paulsen P (2005) Fleischwirtschaft 85(12):128–130
Paulsen P, Hagen U, Bauer F (2006) Eur Food Res Technol 223:603–608
Ziegler W, Hahn M, Wallnöfer PR (1994) Dt Lebensm Rundsch 90:108–112
Acknowledgements
The assistance of the Viennese Food Inspection Laboratories (MA 38) in obtaining bacterial samples is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pircher, A., Bauer, F. & Paulsen, P. Formation of cadaverine, histamine, putrescine and tyramine by bacteria isolated from meat, fermented sausages and cheeses. Eur Food Res Technol 226, 225–231 (2007). https://doi.org/10.1007/s00217-006-0530-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00217-006-0530-7