Abstract
Food-fermenting lactic acid bacteria (LAB) are generally considered to be non-toxic and non-pathogenic. Some species of LAB, however, can produce biogenic amines (BAs). BAs are organic, basic, nitrogenous compounds, mainly formed through decarboxylation of amino acids. BAs are present in a wide range of foods, including dairy products, and can occasionally accumulate in high concentrations. The consumption of food containing large amounts of these amines can have toxicological consequences. Although there is no specific legislation regarding BA content in many fermented products, it is generally assumed that they should not be allowed to accumulate. The ability of microorganisms to decarboxylate amino acids is highly variable, often being strain specific, and therefore the detection of bacteria possessing amino acid decarboxylase activity is important to estimate the likelihood that foods contain BA and to prevent their accumulation in food products. Moreover, improved knowledge of the factors involved in the synthesis and accumulation of BA should lead to a reduction in their incidence in foods.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Arena ME, Landete JM, Manca de Nadra MC, Pardo I, Ferrer S (2008). Factors affecting the production of putrescine from agmatine by Lactobacillus hilgardii X1B isolated from wine. J Appl Microbiol 105, 158–165.
Bodmer S, Imark C, Kneubühl M (1999). Biogenic amines in foods: histamine and food processing. Inflam Res 48, 296–300.
Bover-Cid S, Holzapfel WH (1999). Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53, 33–41.
Caston JC, Eaton CL, Gheorghui BP, Ware LL (2002). Tyramine induced hypertensive episodes, panic attacks in hereditary deficient monoamine oxidase patients: case reports. JSC Med Assoc 98, 187–192.
Constantini A, Cersosimo M, Del Prete V, Garcia-Moruno E (2006). Production of biogenic amines by lactic acid bacteria: screening by PCR, thin layer chromatography, and HPLC of strains isolated from wine and must. J Food Protect 69, 391–396.
Coton E, Coton M (2005). Multiplex PCR for colony direct detection of Gram positive histamine- and tyramine-producing bacteria. J Microbiol Methods 63, 296–304.
Coton E, Coton M (2009). Evidence of horizontal transfer as origin of strain to strain variation of the tyramine production trait in Lactobacillus brevis. Food Microbiol 26, 52–57.
Coton E, Rollan G, Bertrand A, Lonvaud-Funel A (1998). Histamine-producing lactic acid bacteria in wines: early detection, frequency and distribution. American J Enol Viticul 49, 199–204.
Dapkevicius MLNE, Nout MJR, Rombouts FM, Houben JH, Wymenga W (2000). Biogenic amine formation and degradation by potential fish silage starter microorganisms. Int J Food Microbiol 57, 107–114.
EFSA (2007). Opinion of the Scientific Committee on a request from EFSA on the introduction of a Qualified Presumption of Safety (QPS) approach for assessment of selected microorganisms referred to EFSA. The EFSA J 587, 1–16.
Fernández M, del Río B, Linares DM, Martín MC, Alvarez MA (2006). Real time polymerase chain reaction for quantitative detection of histamine-producing bacteria: use in cheese production. J Dairy Sci 89, 3763–3769.
Fernández M, Linares DM, Alvarez MA (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. J Food Prot 67, 2521–2529.
Fernández M, Linares DM, Rodríguez A, Alvarez MA (2007). Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl Microbiol Biotechnol 73, 1400–1406.
Garai G, Dueñas MT, Irastorza A, Martín-Álvarez PJ, Moreno-Arribas MV (2006). Biogenic amines in natural ciders. J Food Prot 69, 3006–3012.
Garai G, Dueñas MT, Irastorza A, Moreno-Arribas MV (2007). Biogenic amine production by lactic acid bacteria isolated from cider. Lett Appl Microbiol 45, 473–478.
Gardner DM, Shulman KI, Walker SE, Tailor SA (1996). The making of a user friendly MAOI diet. J Clin Psychiatry 57, 99–104.
Griswold AR, Jameson-Lee M, Burne RA (2006). Regulation and physiologic significance of the agmatine deiminase system of Streptococcus mutans UA159. J Bacteriol 188, 834–841.
Guerrini S, Mangani S, Granchi L, Vincenzini M (2002). Biogenic amine production by Oenococcus oeni. Current Microbiol 44, 374–378.
Igarashi K, Ito K, Kashiwagi K (2001). Polyamine uptake systems in Escherichia coli. Res Microbiol 152, 271–278.
Ladero VM, Linares DM, Fernández M, Alvarez MA (2008). Real time quantitative PCR detection of histamine-producing lactic acid bacteria in cheese: relation with histamine content. Food Res Int 41, 1015–1019.
Landete JM, Ferrer S, Pardo I (2007). Biogenic amine production by lactic acid bacteria, acetic bacteria and yeast isolated from wine. Food Control 18, 1569–1574.
Landete JM, Ferrer S, Polo L, Pardo I (2005). Biogenic amines in wines from three Spanish regions. J Agricul Food Chem 53, 1119–1124.
Lee YH, Kim BH, Kim JH, Yoon WS, Bang SH, Park YK (2007). CadC has a global translational effect during acid adaptation in Salmonella enterica serovar typhimurium. J Bacteriol 189, 2417–2425.
Lehane L, Olley J (2000). Histamine fish poisoning revisited. Int J Food Microbiol 58, 1–37.
Leitão MC, Marques AP, San Romão MV (2005). A survey of biogenic amines in commercial Portugese wines. Food Control 16, 199–204.
Leuschner RG, Heidel M, Hammes WP (1998). Histamine and tyramine degradation by food fermenting microorganisms. Int J Food Microbiol 39, 1–10.
Linares DM, Cruz Martín M, Ladero V, Alvarez MA, Fernández M (2010). Biogenic amines in dairy products. Critical Rev Food Sci Nutr (in press).
Livingston MG, Livingston HM (1996). Monoamine oxidase inhibitors. An update on drug interactions. Drug Saf 14, 219–227.
Lonvaud-Funel A (2001). Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 199, 9–13.
Lucas P, Lonvaud-Funel A (2002). Purification and partial gene sequence of the tyrosine decarboxylase of Lactobacillus brevis IOEB 9809. FEMS Microbiol Lett 211, 85–89.
Lucas PM, Claisse O, Lonvaud-Funel A (2008). High frequency of histamine producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl Environ Microbiol 74, 811–817.
Lucas PM, Wolken WAM, Claisse O, Lolkema JS, Lonvaud-Funel A (2005). Histamine-producing pathway encoded on an unstable plasmid in Lactobacillus hilgardii 0006. Appl Environ Microbiol 71, 1417–1424.
Lyte M (2004). The biogenic amine tyramine modulates the adherence of Escherichia coli O157:H7 to intestinal mucosa. J Food Prot 67, 878–883.
Maijala RL (1993). Formation of histamine and tyramine by some lactic acid bacteria in MRS-broth and modified decarboxylation agar. Lett Appl Microbiol 17, 40–43.
Marcobal A, de las Rivas B, Moreno-Arribas MV, Muñoz R (2005). Multiplex PCR method for the simultaneous detection of histamine-, tyramine-, and putrescine producing lactic acid bacteria in foods. J Food Prot 68, 874–878.
Marcobal Á, de las Rivas B, Moreno-Arribas MV, Muñoz R (2006a). Evidence for horizontal gene transfer as origin of putrescine production in Oenococcus oeni RM83. App Environ Microbiol 72, 7954–7958.
Marcobal A, de las Rivas B, Muñoz R (2006b). Methods for the detection of bacteria producing biogenic amines on foods: a survey. J Con Prot Food Safety 1, 187–196.
Marques AP, Leitão MC, San Romão MV (2008). Biogenic amines in wines: influence of oenological factors. Food Chem 107, 853–860.
Martín MC, Fernández M, Linares DM, Alvarez MA (2005). Sequencing, characterization and transcriptional analysis of the histidine decarboxylase operon of Lactobacillus buchneri. Microbiol 151, 1219–1228.
Martín-Álvarez PJ, Marcobal Á, Polo C, Moreno-Arribas MV (2006). Influence of technological practices on biogenic amine contents in red wines. Eur Food Res Technol 222, 420–424.
Molenaar D, Bosscher JS, Ten Brink B, Driessen AJM, Konings WN (1993). Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J Bacteriol 175, 2864–2870.
Moreno-Arribas V, Lonvaud-Funel A (1999). Tyrosine decarboxylase activity of Lactobacillus brevis IOEB 9809 isolated from wine and L. brevis ATCC 367. FEMS Microbiol Lett 180, 55–60.
Moreno-Arribas V, Polo MC, Jorganes F, Muñoz R (2003). Screening of biogenic amine production by lactic acid bacteria isolated from grape must and wine. Int J Food Microbiol 84, 117–123.
Moreno-Arribas V, Torlois S, Joyex A, Bertrand A, Lonvaud-Funel A (2000). Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. J Appl Microbiol 88, 584–593.
Nannelli F, Claisse O, Gindreau E, de Revel G, Lonvaud-Funel A, Lucas PM (2008). Determination of lactic acid bacteria producing biogenic amines in wine by quantitative PCR methods. Lett Appl Microbiol 47, 594–599.
Novella-Rodríguez S, Veciana-Nogués MT, Izquierdo-Pulido M, Vidal-Carou MC (2003a). Distribution of biogenic amines and polyamines in cheese. J Food Sci 68, 750–755.
Novella-Rodríguez S, Veciana-Nogués MT, Trujillo-Mesa AJ, Vidal-Carou MC (2003b). Profile of biogenic amines in goat cheese made from pasteurized and pressurized milks. J Food Sci 67, 2940–2944.
Önal A (2007). A review: current analytical methods for the determination of biogenic amines in food. Food Chem 103, 1475–1486.
Premont RT, Gainetdinov RR, Caron MG (2001). Following the trace of elusive amines. Proc Natl Acad Sci USA 98, 9474–9475.
Rhee JE, Rhee JH, Ryu PY, Choi SH (2002). Identification of the cadBA operon from Vibrio vulnificus and its influence on survival to acid stress. FEMS Microbiol Lett 208, 245–251.
Satomi M, Furushita M, Oikawa H, Yoshikawa-Takahashi M, Yano Y (2008). Analysis of a 30 kbp plasmid encoding histidine decarboxylase gene in Tetragenococcus halophilus isolated from fish sauce. Int J Food Microbiol 126, 202–209.
Sattler J, Hesterberg R, Lorenz W, Schmidt U, Crombach M, Stahlknecht CD (1985). Inhibition of human and canine diamine oxidase by drugs used inan intensive care unit: relevance for clinical side effects? Agents Actions 16, 91–94.
Shalaby AR (1996). Significance of biogenic amines to food safety and human health. Food Res Int 29, 675–690.
Silla Santos MH (1996). Biogenic amines: their importance in foods. Int J Food Microbiol 29, 213–231.
Soufleros E, Barrios ML, Bertrand A (1998). Correlation between the content of biogenic amines and other wine compounds. Am J Enol Viticul 49, 266–269.
Taylor SL (1983). Monograph on histamine poisoning. In: Codex Alimentarius Commission, FAO/WHO, Rome. 19th session of the Codex Committee on Food Hygiene, Washington, DC, 26–30 September 1983.
Ten Brink B, Damink C, Joosten HMLJ, Huisint-Veld JHJ (1990). Occurrence and formation of biologically amines in food. Int J Food Microbiol 11, 73–84.
Tkachenko A, Nesterova L, Pshenichnov M (2001). The role of the natural polyamine putrescine in defense against oxidative stress in Escherichia coli. Arch Microbiol 176, 155–157.
Van de Guchte M, Serror P, Chervaux C, Smokvina T, Ehrlich SD, Maguin E (2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82, 187–216.
Vido K, Le Bars D, Mistou MY, Anglade P, Gruss A, Gaudu P (2004). Proteome analyses of heme-dependent respiration in Lactococcus lactis: involvement of the proteolytic system. J Bacteriol 186, 1648–1657.
Acknowledgements
This work was funded by the EU commission in the framework of the BIAMFOOD project (Controlling Biogenic Amines in Traditional Food Fermentations in Regional Europe—project No. 211441).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Spano, G., Russo, P., Lonvaud-Funel, A. et al. Biogenic amines in fermented foods. Eur J Clin Nutr 64 (Suppl 3), S95–S100 (2010). https://doi.org/10.1038/ejcn.2010.218
Published:
Issue Date:
DOI: https://doi.org/10.1038/ejcn.2010.218
Keywords
This article is cited by
-
Bioactive properties and therapeutic aspects of fermented vegetables: a review
Food Production, Processing and Nutrition (2024)
-
Fermented foods and gastrointestinal health: underlying mechanisms
Nature Reviews Gastroenterology & Hepatology (2023)
-
Miniaturized wireless sensor enables real-time monitoring of food spoilage
Nature Food (2023)
-
Multifunctional effects of Lactobacillus sakei HEM 224 on the gastrointestinal tract and airway inflammation
Scientific Reports (2023)
-
Bacteriocin and Antioxidant Production, a Beneficial Properties of Lactic Acid Bacteria Isolated from Fermented Vegetables of Northwest Bulgaria
Probiotics and Antimicrobial Proteins (2023)