The Impact of the Cell-Free Solution of Lactic Acid Bacteria on Cadaverine Production by Listeria monocytogenes and Staphylococcus aureus in Lysine-Decarboxylase Broth
Commenced in January 2007
Frequency: Monthly
Edition: International
Paper Count: 32804
The Impact of the Cell-Free Solution of Lactic Acid Bacteria on Cadaverine Production by Listeria monocytogenes and Staphylococcus aureus in Lysine-Decarboxylase Broth

Authors: Fatih Özogul, Nurten Toy, Yesim Özogul

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.

Digital Object Identifier (DOI): doi.org/10.5281/zenodo.1099936

Procedia APA BibTeX Chicago EndNote Harvard JSON MLA RIS XML ISO 690 PDF Downloads 2076

References:


[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.