The Impact of the Cell-Free Solution of Lactic Acid Bacteria on Cadaverine Production by Listeria monocytogenes and Staphylococcus aureus in Lysine-Decarboxylase Broth
The influences of cell-free solutions (CFSs) of lactic
acid bacteria (LAB) on cadaverine and other biogenic amines
production by Listeria monocytogenes and Staphylococcus aureus
were investigated in lysine decarboxylase broth (LDB) using HPLC.
Cell free solutions were prepared from Lactococcus lactis subsp.
lactis, Leuconostoc mesenteroides subsp. cremoris, Pediococcus
acidilactici and Streptococcus thermophiles. Two different
concentrations that were 50% and 25% CFS and the control without
CFSs were prepared. Significant variations on biogenic amine
production were observed in the presence of L. monocytogenes and S.
aureus (P < 0.05). The function of CFS on biogenic amine production
by foodborne pathogens varied depending on strains and specific
amine. Cadaverine formation by L. monocytogenes and S. aureus in
control were 500.9 and 948.1 mg/L, respectively while the CFSs of
LAB induced 4-fold lower cadaverine production by L.
monocytogenes and 7-fold lower cadaverine production by S. aureus.
The CFSs resulted in strong decreases in cadaverine and putrescine
production by L. monocytogenes and S. aureus, although remarkable
increases were observed for histamine, spermidine, spermine,
serotonin, dopamine, tyramine and agmatine in the presence of LAB
in lysine decarboxylase broth.
[1] A. Halàsz, A. Barath, L. Simon-Sarkadi, W. Holzapfel, “Biogenic
amines and their production by microorganisms in food,” Trends in
Food Science and Technology, vol. 5, 1994, pp. 42–49.
[2] V. Ladero, M. Coton, M. Fernández, N. Buron, M.C. Martin, H.
Guichard, E. Coton, M.A, Alvarez, “Biogenic amines content in Spanish
and French natural ciders: application of qPCR for quantitative detection
of biogenic amine-producers,” Food Microbiology, vol. 28, 2011, pp.
554–561.
[3] M. Marino, M. Maifreni, S. Moret, & G. Rondinini, “The capacity of
Enterobacteriaceae species to produce biogenic amines in cheese,”
Letters in Applied Microbiology, vol. 31, 2000, pp. 169–173.
[4] L. Prester, “Biogenic amines in fish, fish products and shellfish: a
review,” Food Additives and Contaminants” vol. 28, 2011, pp. 1547–
1560.
[5] G. Suzzi, F. Gardini, “Biogenic amines in dry fermented sausages: a
review,” International Journal of Food Microbiology, vol. 88, 2003, pp.
41–51.
[6] B. Ten Brink, C. Damink, H.M.L.J. Joosten, J.H.J. Huis In't Veld,
“Occurrence and formation of biologically active amines in foods,”
International Journal of Food Microbiology, vol. 11, 1990, pp. 73–84.
[7] G. Gasarasi, M. Kelgtermans, J. Van Roy, F. Delvaux, & G.
Derdelinckx, “Occurrence of biogenic amines in beer: Causes and
proposals of remedies,” Monatsschrift für Brauwissenschaft, vol. 56,
2003, pp. 58–63.
[8] M. Krizek, T. Pelikanova, “Determination of seven biogenic amines in
foods by micellar electrokinetic capillary chromatography,” J.
Chromatog. A, vol. 815, 1998, pp. 243-250
[9] C. W. Taylor, J. Y. Hui, & D. E. “Lyons, Toxicology of scombroı¨d
poisoning,” In E. P. Ragelis (Ed.) “Seafood toxins Washington’ USA:
American Chemical Society, 1984, pp.417–420.
[10] H. M. Joosten, “The biogenic amine content of Dutch cheese and their
toxicological significance,” Netherlands Milk Dairy Journal, vol. 42,
1987, pp. 25–42.
[11] M. C. Vidal-Carou, M. J. Isla Gavin, A. Marine Font, & R. Codony
Salcedo, “Histamine and tyramine in natural sparkling wine, vermouth,
cider and vinegar,” Journal of Food Composition and Analysis, vol. 2,
1989, pp. 210–218.
[12] S. Bardo´cz, “Polyamines in food and their consequences for food
quality and human health,” Trends in Food Science and Technology, vol.
6(10), 1995, pp. 341–346.
[13] M. H. Silla Santos, “Biogenic amines: their importance in foods,” Int. J.
Food Microbiol, vol. 29 1996, pp. 213-231.
[14] A. L. Cinquina, A. Calı`, F. Longo, L. De Santis, A. Severoni, & F.
Abballe, “Determination of biogenic amines in fish tissues by ionexchange
chromatography with conductivity detection,” Journal of
Chromatography A, vol. 1032 (1–2), 2004, pp. 73–77.
[15] R. Conca, M. C. Bruzzoniti, E. Mentasti, C. Sarzanini, & P. Hajos, “Ion
chromatographic separation of polyamines: Putrescine, spermidine and
spermine,” Analytical Chimica Acta, vol. 439, 2001, pp. 107–114.
[16] C. Ruiz-Capillas, & F. Jimenez-Colmenero, “Biogenic amines in meat
and meat products,” Critical Reviews in Food Science and Nutrition,
vol. 44, 2004, pp. 489–499.
[17] J.A. Curiel, C. Ruiz-Capillas, B. de las Rivas, A.V. Carrascosa, F.
Jiménez-Colmenero, R. Muñoz, “Production of biogenic amines by
lactic acid bacteria and enterobacteria isolated from fresh pork sausages
packaged in different atmospheres and kept under refrigeration,” Meat
Science, vol. 88, 2011, pp. 368–373.
[18] E. Fernández-García, J. Tomillo, M. Nuñez, “Formation of biogenic
amines in raw milk Hispánico cheese manufactured with proteinases and
different levels of starter culture,” Journal of Food Protection, vol. 63,
2000, pp. 1551–1555 [19] S. Bover-Cid, M. Hugas, M. Izquierdo-Pulido, M.C. Vidal-Carou,
“Amino acid decarboxylase activity of bacteria isolated from fermented
pork sausages,” International Journal of Food Microbiology, vol. 66,
2001, pp. 185–189.
[20] F. Durlu-Özkaya, K. Ayhan, N. Vural, “Biogenic amines produced by
Enterobacteriaceae isolated from meae isolated from meat products,”
Meat Science, vol. 58, 163–166.
[21] T. Lavizzari, M. Breccia, S. Bover-Cid, M. C. Vidal-Carou, M. T.
Veciana-Nogués, ‘Histamine, cadaverine and putrescine produced in
vitro by Enterobacteriaceae and Pseudomonadaceae isolated from
spinach,” Journal of Food Protection, vol. 73, 2010, pp. 385–389.
[22] J.M. Lorenzo, Cachaldora, A. Fonseca, S. Gomez, M. Franco, I. J.
Carballo, ‘Production of biogenic amines “in vitro” in relation to the
growth phase by Enterobactericeae species isolated from traditional
sausages,” Meat Science, vol. 86, 2010, pp. 684–691.
[23] A. Pircher, F. Bauer, P. Paulsen, “Formation of cadaverine, histamine,
putrescine and tyramine by bacteria isolated from meat, fermented
sausages and cheeses,” European Food Research and Technology, vol.
226, 2007, pp. 225–231.
[24] M.H. Silla Santos, “Amino acid decarboxylase capability of
microorganisms isolated in Spanish fermented meat products,”
International Journal of Food Microbiology, vol. 39, 1998, pp. 227–230.
[25] .M. E. Arena, J. M. Landete, M.C. Manca de Nadra, I. Pardo, S. Ferrer,
“Factors affecting the production of putrescine from agmatine by
Lactobacillus hilgardii X1B isolated from wine,” Journal of Applied
Microbiology, vol.105, 2008, pp.158–165.
[26] M. Fernández, D. M. Linares, A. Rodrìguez, M. A. Alvarez, “Factors
affecting tyramine production in Enterococcus durans IPLA 655,”
Applied Microbiology and Biotechnology, vol. 73, 2007, pp. 1400–1406.
[27] F. Gardini, M. Martuscelli, M. C. Caruso, F. Galgano, M. A. Crudele, F.
Favati, M. E. Guerzoni, G. Suzzi, “Effects of pH, temperature and NaCl
concentration on the growth kinetics, proteolytic activity and biogenic
amine production of Enterococcus faecalis,” International Journal of
Food Microbiology, vol. 64, 2001, pp. 105–117.
[28] A. Marcobal B. de las Rivas, R. Muñoz, “Methods for the detection of
bacteria producing biogenic amines on foods: A Survey,”J Verbrauch
Lebensm, vol. 1, 2006, pp. 187-196.
[29] S. Bover-Cid, M. Izquierdo-Pulido, & M. C. Vidal-Carou, “Mixed
starter cultures to control biogenic amine production in dry fermented
sausages,” Journal of Food Protection, vol. 63, 2000, pp. 1556–1562.
[30] A. Tosukhowong, W. Visessanguan, L. Pumpuang, P. Tepkasikul, A.
Panya, & R. Valyasevi, “Biogenic amine formation in Nham, a Thai
fermented sausage, and the reduction by commercial starter culture
Lactobacillus plantarum BCC 9546,” Food Chemistry, vol. 129, 2011,
pp. 846–853.
[31] S. Bunc’ic, L. J. Paunovic, V. Teodorovic, D. Radišic, G. Vojinovic, D.
Smiljanic, et. al. “Effects of glucono-deltalactone and Lactobacillus
plantarum on the production of histamine and tyramine in fermented
sausages,” International Journal of Food Microbiology, vol. 17, 1993,
pp. 303–309.
[32] S. L. Rice, & P. E. Koehler, “Tyrosine and histidine decarboxylase
activities of Pediococcus cerevisiae and Lactobacillus species and the
production of tyramine in fermented sausages,” Journal of Milk and
Food Technology, vol. 39, 1977, pp. 166–169.
[33] X. Nie, Q. S. Zhang Lin “Biogenic amine accumulation in silver carp
sausage inoculated with Lactobacillus plantarum plus Saccharomyces
cerevisiae” Food Chemistry, vol. 153, 2014, pp. 432–436.
[34] T. M. Hernandez-Jover, M. T. Izquirdo-Pulido, A. Veciana-Nogues, M.
Marine-Font, & M. C. Vidal-Carou, “Biogenic amine and polyamine
contents in meat and meat products” Journal of Agricultural and Food
Chemistry, vol. 45, 1997, pp. 2098–2102.
[35] A. Marine´-Font, M. C. Vidal-Carou, M. Izquierdo-Pulido, M. T.
Veciana-Nogue´s, T. Herna´ndez-Jover, “Les amines bioge`nes dans les
aliments: leur signification, leur analyse Ann” Fals. Exp. Chim. vol. 88,
1995, pp.119–140.
[36] I. Geornaras, G. A. Dykes, & A. V. Holy, “Biogenic amine formation by
poultry-associated spoilage and pathogenic bacteria,” Letters in Applied
Microbiology, vol. 21, 1995, pp. 164–166.
[37] F. Ozogul, & Y. Ozogul, “The ability of biogenic amines and ammonia
production by single bacterial cultures,” European Food Research
Technology, vol. 225, 2007, pp. 385–394.
[38] J. H. Mah, & H. J. Hwang, “Inhibition of biogenic amine formation in a
salted and fermented anchovy by Staphylococcus xylosus as a protective
culture,” Food Control, vol. 20, 2009, pp.796–801.
[39] A. Marine´-Font, M. C. Vidal-Carou, M. Izquierdo-Pulido, M. T.
Veciana-Nogue´s, T. Herna´ndez-Jover, “Les amines bioge`nes dans les
aliments: leur signification, leur analyse Ann,” Fals. Exp. Chim. vol. 88,
1995, pp.119–140.
[40] F. Ozogul, “Production of biogenic amines by Morganella morganii,
Klebsiella pneumoniae and Hafnia alvei using a rapid HPLC method,”
European Food Research and Technology, vol. 219, 2004. pp.465–469.
[41] V. Møller, “Distribution of amino acid decarboxylases in
Enterobacteriaceae,” Acta Pathologica et Microbiologica Scandinavica,
Vol. 35, 1954, pp. 259−277.
[42] G. Landeta, B. Rivas, A. V. Carrascosa, R. Mun˜oz, “Screening of
biogenic amine production by coagulase-negative staphylococci isolated
during industrial Spanish dry-cured ham processes,” Meat Science, vol.
77, 2007, pp. 556–561
[43] M. Z. Zaman, A. S. Abdulamir, F. A. Bakar, J. Selamat, & J. Bakar,
“Microbiological, physicochemical and health impact of high level of
biogenic amines in fish sauce,” American Journal of Applied Sciences,
6, 2009, pp. 1199–1211.
[44] M. M. Brashears, D. Jaroni, & J. Trimble, Isolation, selection, and
characterization of lactic acid bacteria for a competitive exclusion
product to reduce shedding of Escherichia coli O157:H7 in cattle.
Journal of Food Protection, vol. 66, 2003, pp. 355–363.
[45] N. Toy, F. Özogul, Y. Özogul, “The influence of the cell free solution of
lactic acid bacteria on tyramine production by food borne-pathogens in
tyrosine decarboxylase broth” Food Chemistry, 173, 2015, pp. 45–53.
[46] L. Topisirovic, K. Veljovic, A. Terzic Vidojevic, I. Strahinic, & M.
Kojic, “Comparative analysis of antimicrobial and proteolytic activity of
lactic acid bacteria isolated from Zlatar cheese” Genetika, vol. 39, 2007,
pp.125–138.
[47] S. Bover-Cid, S. Schoppen, M. Izquierdo-Pulido, & M. C. Vidal-Carou,
“Relationship between biogenic amine contents and the size of dry
fermented sausages,” Meat Science, 51(4), 1999, pp. 305–311.
[48] M. L. N. E. Dapkevicius, M. J. R. Nout, F. M. Rombouts, J. H.
Houben& W. Wymenga, “Biogenic amine formation and degradation by
potential fish silage starter microorganisms,” International Journal of
Food Microbiology, 57(1–2), 2000, pp. 107–114.
[49] J. Fernández-García, J. Tomillo, & M. Nunez, “Effect of added
proteinases and level of starter culture on the formation of biogenic
amines in raw milk manchego cheese,” International Journal of Food
Microbiology, 52(3), 1999, pp. 189–196.
[50] Y. Hu, W. Xia, & X. Liu, “Changes in biogenic amines in fermented
silver carp sausages inoculated with mixed starter cultures,” Food
Chemistry, 104(1), 2007, pp. 188–195.
[51] B. O. Omafuvbe, & L. C. “Enyioha, Phenotypic identifi-cation and
technological properties of lactic acid bacteria isolated from selected
commercial Nigerian bottled yoghurt,” African Journal of Food Science
and Technology, 5, 2011, pp. 340–348.
[52] D. Beutling, “Prufung von Starterorganismen auf ihre Befahigung zur
bildung von histamin und tyramin” Monatshefte für veterinär medizine,
47, 1992, pp. 587–591.
[53] M. T. Veciana-Nogues, A. Marine Font, & M. C. Vidal-Carou,
“Biogenic amines as hygienic quality indicators of tuna. Relationships
with microbial counts. ATP related compounds, volatile amines, and
organoleptic changes,” Journal of Agricultural and Food Chemistry, 45,
1997, 2036–2041.
[54] L. Zhong-Yi, L. Zhong-Hai, Z. Miao-Ling, & D. Xiao-Ping, “Effect of
fermentation with mixed starter cultures on biogenic amines in bighead
carp surimi” International Journal of Food Science & Technology, vol.
45, 2010, pp. 930–936.
[55] M. Rabie, L. Simon-Sarkadi, H. Siliha, S. El-seedy, & A. A. El Badawy,
“Changes in free amino acids and biogenic amines of Egyptian
saltedfermented fish (Feseekh) during ripening and storage,” Food
Chemistry, vol. 115, 2009, pp. 635–638.
[56] A. Butturini, P. Aloisi, R. Tagliazucchi, & C. Cantoni, “Production of
biogenic amines by enterobacteria and lactic acid bacteria isolated from
meat products,” Industrial Alignment, vol. 34, 1995, pp. 105–107.
[57] A. X. Roig-Sagues, M. Hernandez-Herrero, E. I. Lopez-Sabater, J. J.
Rodriguez-Jerez, & M. T. Mora-Ventura, “Histidine decarboxylase
activity of bacteria isolated from raw and ripened Salsichon, a Spanish
cured sausage” Journal of Food Protection, vol. 59, 1996, pp. 516–520.
[58] J. J. Rodriguez-Jerez, M. T. Mora-Ventura, E. I. Lopez-Sabater& M. M.
Hernandez-Herrero, “Histidine, lysine and ornithine decarboxylase
bacteria in salted semi-preserved anchovies,” Journal of Food
Protection, 57, 1994, 784–787. [59] M. Martuscelli, M. A. Crudele, F. Gardini, & G. Suzzi, “Biogenic amine
formation and oxidation by Staphylococcus xylosus strains from
artisanal fermented sausages” Letters in Applied Microbiology, 31, 2000,
pp. 228–232.
[60] F. Ozogul, “Effects of specific lactic acid bacteria species on biogenic
amine production by foodborne pathogen,” International Journal of Food
Science and Technology, 46, 2011, 478–484.
[1] A. Halàsz, A. Barath, L. Simon-Sarkadi, W. Holzapfel, “Biogenic
amines and their production by microorganisms in food,” Trends in
Food Science and Technology, vol. 5, 1994, pp. 42–49.
[2] V. Ladero, M. Coton, M. Fernández, N. Buron, M.C. Martin, H.
Guichard, E. Coton, M.A, Alvarez, “Biogenic amines content in Spanish
and French natural ciders: application of qPCR for quantitative detection
of biogenic amine-producers,” Food Microbiology, vol. 28, 2011, pp.
554–561.
[3] M. Marino, M. Maifreni, S. Moret, & G. Rondinini, “The capacity of
Enterobacteriaceae species to produce biogenic amines in cheese,”
Letters in Applied Microbiology, vol. 31, 2000, pp. 169–173.
[4] L. Prester, “Biogenic amines in fish, fish products and shellfish: a
review,” Food Additives and Contaminants” vol. 28, 2011, pp. 1547–
1560.
[5] G. Suzzi, F. Gardini, “Biogenic amines in dry fermented sausages: a
review,” International Journal of Food Microbiology, vol. 88, 2003, pp.
41–51.
[6] B. Ten Brink, C. Damink, H.M.L.J. Joosten, J.H.J. Huis In't Veld,
“Occurrence and formation of biologically active amines in foods,”
International Journal of Food Microbiology, vol. 11, 1990, pp. 73–84.
[7] G. Gasarasi, M. Kelgtermans, J. Van Roy, F. Delvaux, & G.
Derdelinckx, “Occurrence of biogenic amines in beer: Causes and
proposals of remedies,” Monatsschrift für Brauwissenschaft, vol. 56,
2003, pp. 58–63.
[8] M. Krizek, T. Pelikanova, “Determination of seven biogenic amines in
foods by micellar electrokinetic capillary chromatography,” J.
Chromatog. A, vol. 815, 1998, pp. 243-250
[9] C. W. Taylor, J. Y. Hui, & D. E. “Lyons, Toxicology of scombroı¨d
poisoning,” In E. P. Ragelis (Ed.) “Seafood toxins Washington’ USA:
American Chemical Society, 1984, pp.417–420.
[10] H. M. Joosten, “The biogenic amine content of Dutch cheese and their
toxicological significance,” Netherlands Milk Dairy Journal, vol. 42,
1987, pp. 25–42.
[11] M. C. Vidal-Carou, M. J. Isla Gavin, A. Marine Font, & R. Codony
Salcedo, “Histamine and tyramine in natural sparkling wine, vermouth,
cider and vinegar,” Journal of Food Composition and Analysis, vol. 2,
1989, pp. 210–218.
[12] S. Bardo´cz, “Polyamines in food and their consequences for food
quality and human health,” Trends in Food Science and Technology, vol.
6(10), 1995, pp. 341–346.
[13] M. H. Silla Santos, “Biogenic amines: their importance in foods,” Int. J.
Food Microbiol, vol. 29 1996, pp. 213-231.
[14] A. L. Cinquina, A. Calı`, F. Longo, L. De Santis, A. Severoni, & F.
Abballe, “Determination of biogenic amines in fish tissues by ionexchange
chromatography with conductivity detection,” Journal of
Chromatography A, vol. 1032 (1–2), 2004, pp. 73–77.
[15] R. Conca, M. C. Bruzzoniti, E. Mentasti, C. Sarzanini, & P. Hajos, “Ion
chromatographic separation of polyamines: Putrescine, spermidine and
spermine,” Analytical Chimica Acta, vol. 439, 2001, pp. 107–114.
[16] C. Ruiz-Capillas, & F. Jimenez-Colmenero, “Biogenic amines in meat
and meat products,” Critical Reviews in Food Science and Nutrition,
vol. 44, 2004, pp. 489–499.
[17] J.A. Curiel, C. Ruiz-Capillas, B. de las Rivas, A.V. Carrascosa, F.
Jiménez-Colmenero, R. Muñoz, “Production of biogenic amines by
lactic acid bacteria and enterobacteria isolated from fresh pork sausages
packaged in different atmospheres and kept under refrigeration,” Meat
Science, vol. 88, 2011, pp. 368–373.
[18] E. Fernández-García, J. Tomillo, M. Nuñez, “Formation of biogenic
amines in raw milk Hispánico cheese manufactured with proteinases and
different levels of starter culture,” Journal of Food Protection, vol. 63,
2000, pp. 1551–1555 [19] S. Bover-Cid, M. Hugas, M. Izquierdo-Pulido, M.C. Vidal-Carou,
“Amino acid decarboxylase activity of bacteria isolated from fermented
pork sausages,” International Journal of Food Microbiology, vol. 66,
2001, pp. 185–189.
[20] F. Durlu-Özkaya, K. Ayhan, N. Vural, “Biogenic amines produced by
Enterobacteriaceae isolated from meae isolated from meat products,”
Meat Science, vol. 58, 163–166.
[21] T. Lavizzari, M. Breccia, S. Bover-Cid, M. C. Vidal-Carou, M. T.
Veciana-Nogués, ‘Histamine, cadaverine and putrescine produced in
vitro by Enterobacteriaceae and Pseudomonadaceae isolated from
spinach,” Journal of Food Protection, vol. 73, 2010, pp. 385–389.
[22] J.M. Lorenzo, Cachaldora, A. Fonseca, S. Gomez, M. Franco, I. J.
Carballo, ‘Production of biogenic amines “in vitro” in relation to the
growth phase by Enterobactericeae species isolated from traditional
sausages,” Meat Science, vol. 86, 2010, pp. 684–691.
[23] A. Pircher, F. Bauer, P. Paulsen, “Formation of cadaverine, histamine,
putrescine and tyramine by bacteria isolated from meat, fermented
sausages and cheeses,” European Food Research and Technology, vol.
226, 2007, pp. 225–231.
[24] M.H. Silla Santos, “Amino acid decarboxylase capability of
microorganisms isolated in Spanish fermented meat products,”
International Journal of Food Microbiology, vol. 39, 1998, pp. 227–230.
[25] .M. E. Arena, J. M. Landete, M.C. Manca de Nadra, I. Pardo, S. Ferrer,
“Factors affecting the production of putrescine from agmatine by
Lactobacillus hilgardii X1B isolated from wine,” Journal of Applied
Microbiology, vol.105, 2008, pp.158–165.
[26] M. Fernández, D. M. Linares, A. Rodrìguez, M. A. Alvarez, “Factors
affecting tyramine production in Enterococcus durans IPLA 655,”
Applied Microbiology and Biotechnology, vol. 73, 2007, pp. 1400–1406.
[27] F. Gardini, M. Martuscelli, M. C. Caruso, F. Galgano, M. A. Crudele, F.
Favati, M. E. Guerzoni, G. Suzzi, “Effects of pH, temperature and NaCl
concentration on the growth kinetics, proteolytic activity and biogenic
amine production of Enterococcus faecalis,” International Journal of
Food Microbiology, vol. 64, 2001, pp. 105–117.
[28] A. Marcobal B. de las Rivas, R. Muñoz, “Methods for the detection of
bacteria producing biogenic amines on foods: A Survey,”J Verbrauch
Lebensm, vol. 1, 2006, pp. 187-196.
[29] S. Bover-Cid, M. Izquierdo-Pulido, & M. C. Vidal-Carou, “Mixed
starter cultures to control biogenic amine production in dry fermented
sausages,” Journal of Food Protection, vol. 63, 2000, pp. 1556–1562.
[30] A. Tosukhowong, W. Visessanguan, L. Pumpuang, P. Tepkasikul, A.
Panya, & R. Valyasevi, “Biogenic amine formation in Nham, a Thai
fermented sausage, and the reduction by commercial starter culture
Lactobacillus plantarum BCC 9546,” Food Chemistry, vol. 129, 2011,
pp. 846–853.
[31] S. Bunc’ic, L. J. Paunovic, V. Teodorovic, D. Radišic, G. Vojinovic, D.
Smiljanic, et. al. “Effects of glucono-deltalactone and Lactobacillus
plantarum on the production of histamine and tyramine in fermented
sausages,” International Journal of Food Microbiology, vol. 17, 1993,
pp. 303–309.
[32] S. L. Rice, & P. E. Koehler, “Tyrosine and histidine decarboxylase
activities of Pediococcus cerevisiae and Lactobacillus species and the
production of tyramine in fermented sausages,” Journal of Milk and
Food Technology, vol. 39, 1977, pp. 166–169.
[33] X. Nie, Q. S. Zhang Lin “Biogenic amine accumulation in silver carp
sausage inoculated with Lactobacillus plantarum plus Saccharomyces
cerevisiae” Food Chemistry, vol. 153, 2014, pp. 432–436.
[34] T. M. Hernandez-Jover, M. T. Izquirdo-Pulido, A. Veciana-Nogues, M.
Marine-Font, & M. C. Vidal-Carou, “Biogenic amine and polyamine
contents in meat and meat products” Journal of Agricultural and Food
Chemistry, vol. 45, 1997, pp. 2098–2102.
[35] A. Marine´-Font, M. C. Vidal-Carou, M. Izquierdo-Pulido, M. T.
Veciana-Nogue´s, T. Herna´ndez-Jover, “Les amines bioge`nes dans les
aliments: leur signification, leur analyse Ann” Fals. Exp. Chim. vol. 88,
1995, pp.119–140.
[36] I. Geornaras, G. A. Dykes, & A. V. Holy, “Biogenic amine formation by
poultry-associated spoilage and pathogenic bacteria,” Letters in Applied
Microbiology, vol. 21, 1995, pp. 164–166.
[37] F. Ozogul, & Y. Ozogul, “The ability of biogenic amines and ammonia
production by single bacterial cultures,” European Food Research
Technology, vol. 225, 2007, pp. 385–394.
[38] J. H. Mah, & H. J. Hwang, “Inhibition of biogenic amine formation in a
salted and fermented anchovy by Staphylococcus xylosus as a protective
culture,” Food Control, vol. 20, 2009, pp.796–801.
[39] A. Marine´-Font, M. C. Vidal-Carou, M. Izquierdo-Pulido, M. T.
Veciana-Nogue´s, T. Herna´ndez-Jover, “Les amines bioge`nes dans les
aliments: leur signification, leur analyse Ann,” Fals. Exp. Chim. vol. 88,
1995, pp.119–140.
[40] F. Ozogul, “Production of biogenic amines by Morganella morganii,
Klebsiella pneumoniae and Hafnia alvei using a rapid HPLC method,”
European Food Research and Technology, vol. 219, 2004. pp.465–469.
[41] V. Møller, “Distribution of amino acid decarboxylases in
Enterobacteriaceae,” Acta Pathologica et Microbiologica Scandinavica,
Vol. 35, 1954, pp. 259−277.
[42] G. Landeta, B. Rivas, A. V. Carrascosa, R. Mun˜oz, “Screening of
biogenic amine production by coagulase-negative staphylococci isolated
during industrial Spanish dry-cured ham processes,” Meat Science, vol.
77, 2007, pp. 556–561
[43] M. Z. Zaman, A. S. Abdulamir, F. A. Bakar, J. Selamat, & J. Bakar,
“Microbiological, physicochemical and health impact of high level of
biogenic amines in fish sauce,” American Journal of Applied Sciences,
6, 2009, pp. 1199–1211.
[44] M. M. Brashears, D. Jaroni, & J. Trimble, Isolation, selection, and
characterization of lactic acid bacteria for a competitive exclusion
product to reduce shedding of Escherichia coli O157:H7 in cattle.
Journal of Food Protection, vol. 66, 2003, pp. 355–363.
[45] N. Toy, F. Özogul, Y. Özogul, “The influence of the cell free solution of
lactic acid bacteria on tyramine production by food borne-pathogens in
tyrosine decarboxylase broth” Food Chemistry, 173, 2015, pp. 45–53.
[46] L. Topisirovic, K. Veljovic, A. Terzic Vidojevic, I. Strahinic, & M.
Kojic, “Comparative analysis of antimicrobial and proteolytic activity of
lactic acid bacteria isolated from Zlatar cheese” Genetika, vol. 39, 2007,
pp.125–138.
[47] S. Bover-Cid, S. Schoppen, M. Izquierdo-Pulido, & M. C. Vidal-Carou,
“Relationship between biogenic amine contents and the size of dry
fermented sausages,” Meat Science, 51(4), 1999, pp. 305–311.
[48] M. L. N. E. Dapkevicius, M. J. R. Nout, F. M. Rombouts, J. H.
Houben& W. Wymenga, “Biogenic amine formation and degradation by
potential fish silage starter microorganisms,” International Journal of
Food Microbiology, 57(1–2), 2000, pp. 107–114.
[49] J. Fernández-García, J. Tomillo, & M. Nunez, “Effect of added
proteinases and level of starter culture on the formation of biogenic
amines in raw milk manchego cheese,” International Journal of Food
Microbiology, 52(3), 1999, pp. 189–196.
[50] Y. Hu, W. Xia, & X. Liu, “Changes in biogenic amines in fermented
silver carp sausages inoculated with mixed starter cultures,” Food
Chemistry, 104(1), 2007, pp. 188–195.
[51] B. O. Omafuvbe, & L. C. “Enyioha, Phenotypic identifi-cation and
technological properties of lactic acid bacteria isolated from selected
commercial Nigerian bottled yoghurt,” African Journal of Food Science
and Technology, 5, 2011, pp. 340–348.
[52] D. Beutling, “Prufung von Starterorganismen auf ihre Befahigung zur
bildung von histamin und tyramin” Monatshefte für veterinär medizine,
47, 1992, pp. 587–591.
[53] M. T. Veciana-Nogues, A. Marine Font, & M. C. Vidal-Carou,
“Biogenic amines as hygienic quality indicators of tuna. Relationships
with microbial counts. ATP related compounds, volatile amines, and
organoleptic changes,” Journal of Agricultural and Food Chemistry, 45,
1997, 2036–2041.
[54] L. Zhong-Yi, L. Zhong-Hai, Z. Miao-Ling, & D. Xiao-Ping, “Effect of
fermentation with mixed starter cultures on biogenic amines in bighead
carp surimi” International Journal of Food Science & Technology, vol.
45, 2010, pp. 930–936.
[55] M. Rabie, L. Simon-Sarkadi, H. Siliha, S. El-seedy, & A. A. El Badawy,
“Changes in free amino acids and biogenic amines of Egyptian
saltedfermented fish (Feseekh) during ripening and storage,” Food
Chemistry, vol. 115, 2009, pp. 635–638.
[56] A. Butturini, P. Aloisi, R. Tagliazucchi, & C. Cantoni, “Production of
biogenic amines by enterobacteria and lactic acid bacteria isolated from
meat products,” Industrial Alignment, vol. 34, 1995, pp. 105–107.
[57] A. X. Roig-Sagues, M. Hernandez-Herrero, E. I. Lopez-Sabater, J. J.
Rodriguez-Jerez, & M. T. Mora-Ventura, “Histidine decarboxylase
activity of bacteria isolated from raw and ripened Salsichon, a Spanish
cured sausage” Journal of Food Protection, vol. 59, 1996, pp. 516–520.
[58] J. J. Rodriguez-Jerez, M. T. Mora-Ventura, E. I. Lopez-Sabater& M. M.
Hernandez-Herrero, “Histidine, lysine and ornithine decarboxylase
bacteria in salted semi-preserved anchovies,” Journal of Food
Protection, 57, 1994, 784–787. [59] M. Martuscelli, M. A. Crudele, F. Gardini, & G. Suzzi, “Biogenic amine
formation and oxidation by Staphylococcus xylosus strains from
artisanal fermented sausages” Letters in Applied Microbiology, 31, 2000,
pp. 228–232.
[60] F. Ozogul, “Effects of specific lactic acid bacteria species on biogenic
amine production by foodborne pathogen,” International Journal of Food
Science and Technology, 46, 2011, 478–484.
@article{"International Journal of Biological, Life and Agricultural Sciences:69380", author = "Fatih Özogul and Nurten Toy and Yesim Özogul", title = "The Impact of the Cell-Free Solution of Lactic Acid Bacteria on Cadaverine Production by Listeria monocytogenes and Staphylococcus aureus in Lysine-Decarboxylase Broth", abstract = "The influences of cell-free solutions (CFSs) of lactic
acid bacteria (LAB) on cadaverine and other biogenic amines
production by Listeria monocytogenes and Staphylococcus aureus
were investigated in lysine decarboxylase broth (LDB) using HPLC.
Cell free solutions were prepared from Lactococcus lactis subsp.
lactis, Leuconostoc mesenteroides subsp. cremoris, Pediococcus
acidilactici and Streptococcus thermophiles. Two different
concentrations that were 50% and 25% CFS and the control without
CFSs were prepared. Significant variations on biogenic amine
production were observed in the presence of L. monocytogenes and S.
aureus (P < 0.05). The function of CFS on biogenic amine production
by foodborne pathogens varied depending on strains and specific
amine. Cadaverine formation by L. monocytogenes and S. aureus in
control were 500.9 and 948.1 mg/L, respectively while the CFSs of
LAB induced 4-fold lower cadaverine production by L.
monocytogenes and 7-fold lower cadaverine production by S. aureus.
The CFSs resulted in strong decreases in cadaverine and putrescine
production by L. monocytogenes and S. aureus, although remarkable
increases were observed for histamine, spermidine, spermine,
serotonin, dopamine, tyramine and agmatine in the presence of LAB
in lysine decarboxylase broth.
", keywords = "Cell-free solution, lactic acid bacteria, cadaverine,
food borne-pathogen.", volume = "9", number = "3", pages = "309-9", }
