Improved screening procedure for biogenic amine production by lactic acid bacteria and Enterobacteria

https://doi.org/10.17221/197/2014-CJFSCitation:Shiling L., Caihong J., Xinglian X., Chengjian X., Kaixiong L., Ruihua S. (2015): Improved screening procedure for biogenic amine production by lactic acid bacteria and Enterobacteria. Czech J. Food Sci., 33: 19-26.
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An improved screening procedure was developed for the detection of amino acid decarboxylase-positive microorganisms (especially lactic acid bacteria and Enterobacteria). Monolayer culture and double layer colour development methods for the detection of amino acid decarboxylase-positive lactic acid bacteria and Enterobacteria were established. Biogenic amine-positive bacteria strain was isolated directly from the samples. The applicability and detection level of the designed medium were quantitatively evaluated by the confirmation of the amine-forming capacity using an HPLC procedure, while tyrosine decarboxylase and lysine decarboxylase genes were detected by PCR with specific primers. The screening method showed a good correlation with the chemical analysis and molecular detection. Enterobacter aerogenes, Enterobacter cloacae, Escherichia coli, Enterococcus faecium, and Enterococcus faecalis were obtained from traditional Chinese sausage. The isolation and screening of amino acid decarboxylase-positive lactic acid bacteria and Enterobacteria can be carried out simultaneously by the improved method.
References:
Ansorena D, Montel M.C, Rokka M, Talon R, Eerola S, Rizzo A, Raemaekers M, Demeyer D (2002): Analysis of biogenic amines in northern and southern European sausages and role of flora in amine production. Meat Science, 61, 141-147  https://doi.org/10.1016/S0309-1740(01)00174-7
 
Ayhan Kamuran, Kolsarici Nuray, Özkan Güleren Alsancak (1999): The effects of a starter culture on the formation of biogenic amines in Turkish soudjoucks. Meat Science, 53, 183-188  https://doi.org/10.1016/S0309-1740(99)00046-7
 
Bhardwaj Arun, Gupta Hittu, Kapila Suman, Kaur Gurpreet, Vij Shilpa, Malik Ravinder Kumar (2010): Safety assessment and evaluation of probiotic potential of bacteriocinogenic Enterococcus faecium KH 24 strain under in vitro and in vivo conditions. International Journal of Food Microbiology, 141, 156-164  https://doi.org/10.1016/j.ijfoodmicro.2010.05.001
 
Bover-Cid Sara, Holzapfel Wilhelm Heinrich (1999): Improved screening procedure for biogenic amine production by lactic acid bacteria. International Journal of Food Microbiology, 53, 33-41  https://doi.org/10.1016/S0168-1605(99)00152-X
 
Bover-Cid Sara, Hugas Marta, Izquierdo-Pulido Maria, Vidal-Carou M.Carmen (2001): Amino acid-decarboxylase activity of bacteria isolated from fermented pork sausages. International Journal of Food Microbiology, 66, 185-189  https://doi.org/10.1016/S0168-1605(00)00526-2
 
Buňková Leona, Buňka František, Klčovská Pavlína, Mrkvička Vladimír, Doležalová Magda, Kráčmar Stanislav (2010): Formation of biogenic amines by Gram-negative bacteria isolated from poultry skin. Food Chemistry, 121, 203-206  https://doi.org/10.1016/j.foodchem.2009.12.012
 
Capozzi Vittorio, Ladero Victor, Beneduce Luciano, Fernández María, Alvarez Miguel A., Benoit Bach, Laurent Barnavon, Grieco Francesco, Spano Giuseppe (2011): Isolation and characterization of tyramine-producing Enterococcus faecium strains from red wine. Food Microbiology, 28, 434-439  https://doi.org/10.1016/j.fm.2010.10.005
 
Carelli Donatella, Centonze Diego, Palermo Carmen, Quinto Maurizio, Rotunno Taddeo (2007): An interference free amperometric biosensor for the detection of biogenic amines in food products. Biosensors and Bioelectronics, 23, 640-647  https://doi.org/10.1016/j.bios.2007.07.008
 
Centeno J (1999): Effects of the addition of Enterococcus faecalis in Cebreiro cheese manufacture. International Journal of Food Microbiology, 48, 97-111  https://doi.org/10.1016/S0168-1605(99)00030-6
 
Chang Mi, Chang Hae Choon (2012): Development of a screening method for biogenic amine producing Bacillus spp.. International Journal of Food Microbiology, 153, 269-274  https://doi.org/10.1016/j.ijfoodmicro.2011.11.008
 
Coïsson J (2004): Production of biogenic amines in “Salamini italiani alla cacciatora PDO”. Meat Science, 67, 343-349  https://doi.org/10.1016/j.meatsci.2003.11.007
 
Curiel J.A., Ruiz-Capillas C., Rivas B. de las, Carrascosa A.V., Jiménez-Colmenero F., Muñoz R. (2011): 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, 88, 368-373  https://doi.org/10.1016/j.meatsci.2011.01.011
 
de las Rivas B., Marcobal A., Carrascosa A., Muñoz R.(2006): PCR detection of food bacteria producing the biogenic amines histamine, tyramine, putrescine and cadaverine. Journal of Food Protection, 69: 2509–2514.
 
Durlu-Özkaya Fügen, Ayhan Kamuran, Vural Nilüfer (2001): Biogenic amines produced by Enterobacteriaceae isolated from meat products. Meat Science, 58, 163-166  https://doi.org/10.1016/S0309-1740(00)00144-3
 
Fadhlaoui-Zid Karima, Curiel José Antonio, Landeta Gerardo, Fattouch Sami, Reverón Inés, de las Rivas Blanca, Sadok Saloua, Muñoz Rosario (2012): Biogenic amine production by bacteria isolated from ice-preserved sardine and mackerel. Food Control, 25, 89-95  https://doi.org/10.1016/j.foodcont.2011.10.032
 
Fernández M., Linares D.M., Alvarez M.A. (2004): Sequencing of the tyrosine decarboxylase cluster of Lactococcus lactis IPLA 655 and the development of a PCR method for detecting tyrosine decarboxylating lactic acid bacteria. Journal of Food Protection, 69: 2521–2529.
 
Gardini Fausto, Martuscelli Maria, Caruso Marisa Carmela, Galgano Fernanda, Crudele Maria Antonietta, Favati Fabio, Guerzoni Maria Elisabetta, Suzzi Giovanna (2001): 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, 64, 105-117  https://doi.org/10.1016/S0168-1605(00)00445-1
 
Gençcelep Hüseyin, Kaban Güzin, Aksu Muhammet İrfan, Öz Fatih, Kaya Mükerrem (2008): Determination of biogenic amines in sucuk. Food Control, 19, 868-872  https://doi.org/10.1016/j.foodcont.2007.08.013
 
Halász Anna, Baráth Ágnes, Simon-Sarkadi Livia, Holzapfel Wilhelm (1994): Biogenic amines and their production by microorganisms in food. Trends in Food Science & Technology, 5, 42-49  https://doi.org/10.1016/0924-2244(94)90070-1
 
Hsu Hsiu-Hua, Chuang Tin-Chen, Lin Hung-Chou, Huang Yu-Ru, Lin Chia-Min, Kung Hsien-Feng, Tsai Yung-Hsiang (2009): Histamine content and histamine-forming bacteria in dried milkfish (Chanos chanos) products. Food Chemistry, 114, 933-938  https://doi.org/10.1016/j.foodchem.2008.10.040
 
Hu P., Xu X.L., Zhou G.H., Han Y.Q., Xu B.C., Liu J.C. (2008): Study of the Lactobacillus sakei protective effect towards spoilage bacteria in vacuum packed cooked ham analyzed by PCR–DGGE. Meat Science, 80, 462-469  https://doi.org/10.1016/j.meatsci.2008.01.011
 
Huang Yu-Ru, Liu Kuan-Ju, Hsieh Hung-Sheng, Hsieh Cheng-Hong, Hwang Deng-Fwu, Tsai Yung-Hsiang (2010): Histamine level and histamine-forming bacteria in dried fish products sold in Penghu Island of Taiwan. Food Control, 21, 1234-1239  https://doi.org/10.1016/j.foodcont.2010.02.008
 
Komprda T., Sládková P., Petirová E., Dohnal V., Burdychová R. (2010): Tyrosine- and histidine-decarboxylase positive lactic acid bacteria and enterococci in dry fermented sausages. Meat Science, 86, 870-877  https://doi.org/10.1016/j.meatsci.2010.07.013
 
Landete José María, de las Rivas Blanca, Marcobal Angela, Muñoz Rosario (2007): Molecular methods for the detection of biogenic amine-producing bacteria on foods. International Journal of Food Microbiology, 117, 258-269  https://doi.org/10.1016/j.ijfoodmicro.2007.05.001
 
Lorenzo José M., Cachaldora Aida, Fonseca Sonia, Gómez María, Franco Inmaculada, Carballo Javier (2010): Production of biogenic amines “in vitro” in relation to the growth phase by Enterobacteriaceae species isolated from traditional sausages. Meat Science, 86, 684-691  https://doi.org/10.1016/j.meatsci.2010.06.005
 
Lu S., Xu X., Shu R., Zhou G., Meng Y., Sun Y., Chen Y., Wang P. (2010): Characterization of biogenic amines and factors influencing their formation in traditional Chinese sausages. Journal of Food Science, 75: M366–M372.
 
Maijala Riitta, Eerola Susanna (1993): Contaminant lactic acid bacteria of dry sausages produce histamine and tyramine. Meat Science, 35, 387-395  https://doi.org/10.1016/0309-1740(93)90043-H
 
McCabe-Sellers Beverly J., Staggs Cathleen G., Bogle Margaret L. (2006): Tyramine in foods and monoamine oxidase inhibitor drugs: A crossroad where medicine, nutrition, pharmacy, and food industry converge. Journal of Food Composition and Analysis, 19, S58-S65  https://doi.org/10.1016/j.jfca.2005.12.008
 
Moreno-Arribas V., Torlois S., Joyeux A., Bertrand A., Lonvaud-Funel A. (2000): Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. Journal of Applied Microbiology, 88, 584-593  https://doi.org/10.1046/j.1365-2672.2000.00997.x
 
Moreno-Arribas M. Victoria, Carmen Polo M. (2008): Occurrence of lactic acid bacteria and biogenic amines in biologically aged wines. Food Microbiology, 25, 875-881  https://doi.org/10.1016/j.fm.2008.05.004
 
Pérez-Pulido R., Abriouel H., Ben Omar N., Lucas R., Martínez-Cañamero M., Gálvez A. (2006): Safety and potential risks of enterococci isolated from traditional fermented capers. Food and Chemical Toxicology, 44, 2070-2077  https://doi.org/10.1016/j.fct.2006.07.008
 
Roseiro C., Santos C., Sol M., Silva L., Fernandes I. (2006): Prevalence of biogenic amines during ripening of a traditional dry fermented pork sausage and its relation to the amount of sodium chloride added. Meat Science, 74, 557-563  https://doi.org/10.1016/j.meatsci.2006.03.030
 
Şenoz B., Işikli N., Coksoyler N. (2000): Biogenic Amines in Turkish Sausages (Sucuks). Journal of Food Science, 65, 764-767  https://doi.org/10.1111/j.1365-2621.2000.tb13583.x
 
Sparo M., Nuñez G.G., Castro M., Calcagno M.L., García Allende M.A., Ceci M., Najle R., Manghi M. (2008): Characteristics of an environmental strain, Enterococcus faecalis CECT7121, and its effects as additive on craft dry-fermented sausages. Food Microbiology, 25, 607-615  https://doi.org/10.1016/j.fm.2008.01.008
 
Suzzi G (2003): Biogenic amines in dry fermented sausages: a review. International Journal of Food Microbiology, 88, 41-54  https://doi.org/10.1016/S0168-1605(03)00080-1
 
Zhu Wei-Yun, Williams Barbara A, Konstantinov Sergey R, Tamminga Seerp, De Vos Willem M, Akkermans Antoon D.L (2003): Analysis of 16S rDNA reveals bacterial shift during in vitro fermentation of fermentable carbohydrate using piglet faeces as inoculum. Anaerobe, 9, 175-180  https://doi.org/10.1016/S1075-9964(03)00083-0
 
Ansorena D, Montel M.C, Rokka M, Talon R, Eerola S, Rizzo A, Raemaekers M, Demeyer D (2002): Analysis of biogenic amines in northern and southern European sausages and role of flora in amine production. Meat Science, 61, 141-147  https://doi.org/10.1016/S0309-1740(01)00174-7
 
Ayhan Kamuran, Kolsarici Nuray, Özkan Güleren Alsancak (1999): The effects of a starter culture on the formation of biogenic amines in Turkish soudjoucks. Meat Science, 53, 183-188  https://doi.org/10.1016/S0309-1740(99)00046-7
 
Bhardwaj Arun, Gupta Hittu, Kapila Suman, Kaur Gurpreet, Vij Shilpa, Malik Ravinder Kumar (2010): Safety assessment and evaluation of probiotic potential of bacteriocinogenic Enterococcus faecium KH 24 strain under in vitro and in vivo conditions. International Journal of Food Microbiology, 141, 156-164  https://doi.org/10.1016/j.ijfoodmicro.2010.05.001
 
Bover-Cid Sara, Holzapfel Wilhelm Heinrich (1999): Improved screening procedure for biogenic amine production by lactic acid bacteria. International Journal of Food Microbiology, 53, 33-41  https://doi.org/10.1016/S0168-1605(99)00152-X
 
Bover-Cid Sara, Hugas Marta, Izquierdo-Pulido Maria, Vidal-Carou M.Carmen (2001): Amino acid-decarboxylase activity of bacteria isolated from fermented pork sausages. International Journal of Food Microbiology, 66, 185-189  https://doi.org/10.1016/S0168-1605(00)00526-2
 
Buňková Leona, Buňka František, Klčovská Pavlína, Mrkvička Vladimír, Doležalová Magda, Kráčmar Stanislav (2010): Formation of biogenic amines by Gram-negative bacteria isolated from poultry skin. Food Chemistry, 121, 203-206  https://doi.org/10.1016/j.foodchem.2009.12.012
 
Capozzi Vittorio, Ladero Victor, Beneduce Luciano, Fernández María, Alvarez Miguel A., Benoit Bach, Laurent Barnavon, Grieco Francesco, Spano Giuseppe (2011): Isolation and characterization of tyramine-producing Enterococcus faecium strains from red wine. Food Microbiology, 28, 434-439  https://doi.org/10.1016/j.fm.2010.10.005
 
Carelli Donatella, Centonze Diego, Palermo Carmen, Quinto Maurizio, Rotunno Taddeo (2007): An interference free amperometric biosensor for the detection of biogenic amines in food products. Biosensors and Bioelectronics, 23, 640-647  https://doi.org/10.1016/j.bios.2007.07.008
 
Centeno J (1999): Effects of the addition of Enterococcus faecalis in Cebreiro cheese manufacture. International Journal of Food Microbiology, 48, 97-111  https://doi.org/10.1016/S0168-1605(99)00030-6
 
Chang Mi, Chang Hae Choon (2012): Development of a screening method for biogenic amine producing Bacillus spp.. International Journal of Food Microbiology, 153, 269-274  https://doi.org/10.1016/j.ijfoodmicro.2011.11.008
 
Coïsson J (2004): Production of biogenic amines in “Salamini italiani alla cacciatora PDO”. Meat Science, 67, 343-349  https://doi.org/10.1016/j.meatsci.2003.11.007
 
Curiel J.A., Ruiz-Capillas C., Rivas B. de las, Carrascosa A.V., Jiménez-Colmenero F., Muñoz R. (2011): 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, 88, 368-373  https://doi.org/10.1016/j.meatsci.2011.01.011
 
de las Rivas B., Marcobal A., Carrascosa A., Muñoz R.(2006): PCR detection of food bacteria producing the biogenic amines histamine, tyramine, putrescine and cadaverine. Journal of Food Protection, 69: 2509–2514.
 
Durlu-Özkaya Fügen, Ayhan Kamuran, Vural Nilüfer (2001): Biogenic amines produced by Enterobacteriaceae isolated from meat products. Meat Science, 58, 163-166  https://doi.org/10.1016/S0309-1740(00)00144-3
 
Fadhlaoui-Zid Karima, Curiel José Antonio, Landeta Gerardo, Fattouch Sami, Reverón Inés, de las Rivas Blanca, Sadok Saloua, Muñoz Rosario (2012): Biogenic amine production by bacteria isolated from ice-preserved sardine and mackerel. Food Control, 25, 89-95  https://doi.org/10.1016/j.foodcont.2011.10.032
 
Fernández M., Linares D.M., Alvarez M.A. (2004): Sequencing of the tyrosine decarboxylase cluster of Lactococcus lactis IPLA 655 and the development of a PCR method for detecting tyrosine decarboxylating lactic acid bacteria. Journal of Food Protection, 69: 2521–2529.
 
Gardini Fausto, Martuscelli Maria, Caruso Marisa Carmela, Galgano Fernanda, Crudele Maria Antonietta, Favati Fabio, Guerzoni Maria Elisabetta, Suzzi Giovanna (2001): 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, 64, 105-117  https://doi.org/10.1016/S0168-1605(00)00445-1
 
Gençcelep Hüseyin, Kaban Güzin, Aksu Muhammet İrfan, Öz Fatih, Kaya Mükerrem (2008): Determination of biogenic amines in sucuk. Food Control, 19, 868-872  https://doi.org/10.1016/j.foodcont.2007.08.013
 
Halász Anna, Baráth Ágnes, Simon-Sarkadi Livia, Holzapfel Wilhelm (1994): Biogenic amines and their production by microorganisms in food. Trends in Food Science & Technology, 5, 42-49  https://doi.org/10.1016/0924-2244(94)90070-1
 
Hsu Hsiu-Hua, Chuang Tin-Chen, Lin Hung-Chou, Huang Yu-Ru, Lin Chia-Min, Kung Hsien-Feng, Tsai Yung-Hsiang (2009): Histamine content and histamine-forming bacteria in dried milkfish (Chanos chanos) products. Food Chemistry, 114, 933-938  https://doi.org/10.1016/j.foodchem.2008.10.040
 
Hu P., Xu X.L., Zhou G.H., Han Y.Q., Xu B.C., Liu J.C. (2008): Study of the Lactobacillus sakei protective effect towards spoilage bacteria in vacuum packed cooked ham analyzed by PCR–DGGE. Meat Science, 80, 462-469  https://doi.org/10.1016/j.meatsci.2008.01.011
 
Huang Yu-Ru, Liu Kuan-Ju, Hsieh Hung-Sheng, Hsieh Cheng-Hong, Hwang Deng-Fwu, Tsai Yung-Hsiang (2010): Histamine level and histamine-forming bacteria in dried fish products sold in Penghu Island of Taiwan. Food Control, 21, 1234-1239  https://doi.org/10.1016/j.foodcont.2010.02.008
 
Komprda T., Sládková P., Petirová E., Dohnal V., Burdychová R. (2010): Tyrosine- and histidine-decarboxylase positive lactic acid bacteria and enterococci in dry fermented sausages. Meat Science, 86, 870-877  https://doi.org/10.1016/j.meatsci.2010.07.013
 
Landete José María, de las Rivas Blanca, Marcobal Angela, Muñoz Rosario (2007): Molecular methods for the detection of biogenic amine-producing bacteria on foods. International Journal of Food Microbiology, 117, 258-269  https://doi.org/10.1016/j.ijfoodmicro.2007.05.001
 
Lorenzo José M., Cachaldora Aida, Fonseca Sonia, Gómez María, Franco Inmaculada, Carballo Javier (2010): Production of biogenic amines “in vitro” in relation to the growth phase by Enterobacteriaceae species isolated from traditional sausages. Meat Science, 86, 684-691  https://doi.org/10.1016/j.meatsci.2010.06.005
 
Lu S., Xu X., Shu R., Zhou G., Meng Y., Sun Y., Chen Y., Wang P. (2010): Characterization of biogenic amines and factors influencing their formation in traditional Chinese sausages. Journal of Food Science, 75: M366–M372.
 
Maijala Riitta, Eerola Susanna (1993): Contaminant lactic acid bacteria of dry sausages produce histamine and tyramine. Meat Science, 35, 387-395  https://doi.org/10.1016/0309-1740(93)90043-H
 
McCabe-Sellers Beverly J., Staggs Cathleen G., Bogle Margaret L. (2006): Tyramine in foods and monoamine oxidase inhibitor drugs: A crossroad where medicine, nutrition, pharmacy, and food industry converge. Journal of Food Composition and Analysis, 19, S58-S65  https://doi.org/10.1016/j.jfca.2005.12.008
 
Moreno-Arribas V., Torlois S., Joyeux A., Bertrand A., Lonvaud-Funel A. (2000): Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. Journal of Applied Microbiology, 88, 584-593  https://doi.org/10.1046/j.1365-2672.2000.00997.x
 
Moreno-Arribas M. Victoria, Carmen Polo M. (2008): Occurrence of lactic acid bacteria and biogenic amines in biologically aged wines. Food Microbiology, 25, 875-881  https://doi.org/10.1016/j.fm.2008.05.004
 
Pérez-Pulido R., Abriouel H., Ben Omar N., Lucas R., Martínez-Cañamero M., Gálvez A. (2006): Safety and potential risks of enterococci isolated from traditional fermented capers. Food and Chemical Toxicology, 44, 2070-2077  https://doi.org/10.1016/j.fct.2006.07.008
 
Roseiro C., Santos C., Sol M., Silva L., Fernandes I. (2006): Prevalence of biogenic amines during ripening of a traditional dry fermented pork sausage and its relation to the amount of sodium chloride added. Meat Science, 74, 557-563  https://doi.org/10.1016/j.meatsci.2006.03.030
 
Şenoz B., Işikli N., Coksoyler N. (2000): Biogenic Amines in Turkish Sausages (Sucuks). Journal of Food Science, 65, 764-767  https://doi.org/10.1111/j.1365-2621.2000.tb13583.x
 
Sparo M., Nuñez G.G., Castro M., Calcagno M.L., García Allende M.A., Ceci M., Najle R., Manghi M. (2008): Characteristics of an environmental strain, Enterococcus faecalis CECT7121, and its effects as additive on craft dry-fermented sausages. Food Microbiology, 25, 607-615  https://doi.org/10.1016/j.fm.2008.01.008
 
Suzzi G (2003): Biogenic amines in dry fermented sausages: a review. International Journal of Food Microbiology, 88, 41-54  https://doi.org/10.1016/S0168-1605(03)00080-1
 
Zhu Wei-Yun, Williams Barbara A, Konstantinov Sergey R, Tamminga Seerp, De Vos Willem M, Akkermans Antoon D.L (2003): Analysis of 16S rDNA reveals bacterial shift during in vitro fermentation of fermentable carbohydrate using piglet faeces as inoculum. Anaerobe, 9, 175-180  https://doi.org/10.1016/S1075-9964(03)00083-0
 
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