Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Biogenic amines in fermented foods

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 options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

    CAS  Article  Google Scholar 

  • Bodmer S, Imark C, Kneubühl M (1999). Biogenic amines in foods: histamine and food processing. Inflam Res 48, 296–300.

    CAS  Article  Google Scholar 

  • Bover-Cid S, Holzapfel WH (1999). Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53, 33–41.

    CAS  Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Fernández M, Linares DM, Rodríguez A, Alvarez MA (2007). Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl Microbiol Biotechnol 73, 1400–1406.

    Article  Google Scholar 

  • Garai G, Dueñas MT, Irastorza A, Martín-Álvarez PJ, Moreno-Arribas MV (2006). Biogenic amines in natural ciders. J Food Prot 69, 3006–3012.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Gardner DM, Shulman KI, Walker SE, Tailor SA (1996). The making of a user friendly MAOI diet. J Clin Psychiatry 57, 99–104.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Guerrini S, Mangani S, Granchi L, Vincenzini M (2002). Biogenic amine production by Oenococcus oeni. Current Microbiol 44, 374–378.

    CAS  Article  Google Scholar 

  • Igarashi K, Ito K, Kashiwagi K (2001). Polyamine uptake systems in Escherichia coli. Res Microbiol 152, 271–278.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Landete JM, Ferrer S, Polo L, Pardo I (2005). Biogenic amines in wines from three Spanish regions. J Agricul Food Chem 53, 1119–1124.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Lehane L, Olley J (2000). Histamine fish poisoning revisited. Int J Food Microbiol 58, 1–37.

    CAS  Article  Google Scholar 

  • Leitão MC, Marques AP, San Romão MV (2005). A survey of biogenic amines in commercial Portugese wines. Food Control 16, 199–204.

    Article  Google Scholar 

  • Leuschner RG, Heidel M, Hammes WP (1998). Histamine and tyramine degradation by food fermenting microorganisms. Int J Food Microbiol 39, 1–10.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Lonvaud-Funel A (2001). Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 199, 9–13.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Lyte M (2004). The biogenic amine tyramine modulates the adherence of Escherichia coli O157:H7 to intestinal mucosa. J Food Prot 67, 878–883.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Marques AP, Leitão MC, San Romão MV (2008). Biogenic amines in wines: influence of oenological factors. Food Chem 107, 853–860.

    CAS  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Önal A (2007). A review: current analytical methods for the determination of biogenic amines in food. Food Chem 103, 1475–1486.

    Article  Google Scholar 

  • Premont RT, Gainetdinov RR, Caron MG (2001). Following the trace of elusive amines. Proc Natl Acad Sci USA 98, 9474–9475.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • Shalaby AR (1996). Significance of biogenic amines to food safety and human health. Food Res Int 29, 675–690.

    CAS  Article  Google Scholar 

  • Silla Santos MH (1996). Biogenic amines: their importance in foods. Int J Food Microbiol 29, 213–231.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

  • 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.

    CAS  Article  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to G Spano.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints 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, S95–S100 (2010). https://doi.org/10.1038/ejcn.2010.218

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2010.218

Keywords

  • biogenic amines
  • lactic acid bacteria
  • risk assessment
  • food fermentation
  • acid stress
  • toxicological effects

Further reading

Search

Quick links