Abstract
The biogenic amines are low molecular weight organic bases present normally in the body with biological activity influencing important physiological functions. The physiological functions of these molecules are achieved by very low concentrations in the tissues. However, significantly high amounts of biogenic amines are produced during processing and storage of seafood as a result of microbial contamination and inadequate storage conditions. Microorganisms having decarboxylase enzyme activity convert amino acids to their respective biogenic amines. Biogenic amines in seafood have been implicated as a major causative agent of food borne illness, where intoxication results from the ingestion of foods containing higher amount of biogenic amines. Hence its identification, quantitation and awareness of this food borne toxin are important in relation to food safety and spoilage. The aim of this paper is to review the basic concepts of seafood quality and safety in relation to biogenic amines along with its control measures and future areas for research.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13197-016-2224-x/MediaObjects/13197_2016_2224_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13197-016-2224-x/MediaObjects/13197_2016_2224_Fig2_HTML.gif)
Similar content being viewed by others
References
Arena ME, Manca de Nadra MC (2001) Biogenic amine production by Lactobacillus. J Appl Microbiol 90:158–162
Askar A, Treptow H (1986) In: Lebensmitteln, Ulmer, Stuttgart V, Bedeutung, Bestimmung (eds) Biogene amine. Eugen Ulmer GmbH & Co, Stuttgart, p 197
Bajc Z, Gacnik KS (2009) Densitometric TLC analysis of histamine in fish and fishery products. J Planar Chromatogr 22:15–17
Bover-Cid S, Holzapfel W (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33–41
Brink B, Damink C, Joosten H, Veld JHJ (1990) Occurrence and formation of biologically active amines in foods. Int J Food Microbiol 11:73–84
Chen H, Huang Y, Hsu H, Lin C, Chen W, Lin C, Tsai Y (2010) Determination of histamine and biogenic amines in fish cubes (Tetrapturusangustirostris) implicated in a food borne poisoning. Food Control 21:13–18
Chong CY, Abu Bakar F, Russly AR, Jamilah B, Mahyudin NA (2011) The effects of food processing on biogenic amines formation. Int J Food Res 18(3):867–876
Commission Regulation (EC) No 2073/2005 Official Journal of the European Union of 15 November 2005 on microbiological criteria for foodstuffs
Dawood AA, Karkalas J, Roy RN, Williams CS (1988) The occurrence of non-volatile amines in chilled-stored rainbow trout (Salmoirideus). Food Chem 27:33–45
EFSA, European Food Safety Authority (2011) Scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA J 9(10):2393
Emborg J, Laursen BG, Dalgaard P (2005) Significant histamine formation in tuna (Thunnusalbacares) at 2°C effect of vacuum and modified atmosphere packaging on psychrotolerant bacteria. Int J Food Microbiol 101:263–279
Ezzat MA, Zare D, Karim R, Ghazali HM (2015) Trans- and cis-urocanic acid, biogenic amine and amino acid contents in ikanpekasam (fermented fish) produced from Javanese carp (Puntiusgonionotus) and black tilapia (Oreochromismossambicus). Food Chem 172:893–899
FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) (2013) Public health risks of histamine and other biogenic amines from fish and fishery products. Meeting report
Food and Drug Administration (FDA) (1996) Fish and fisheries products hazards and controls guide. Food and Drug Administration Office of Seafood, Washington DC
Food and Drug Administration (FDA) (2001) Fish and fisheries products hazards and controls guidance, 3rd edn. US FDA Center for Food Safety and Applied Nutrition, Maryland
Food and Drug Administration (FDA) (2011) Fish and Fishery Products Hazards and Controls Guidance, 4th edn. Department of Health and Human Services, Food and Drug Administration, Center for Food Safety and Applied Nutrition, Washington DC
Gadbois DF, Ravesi EM, Lundstrom RC, Maney RS (1975) N-nitrosodimethylamine in cold-smoked Sablefish. J Agric Food Chem 23:665–668
Halasz A, Barath A, Simon-Sarkadi L, Holzapfel W (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci Technol 5:42–49
Hernandez-Jover T, Izquierdo-Pulido M, Veciana-Nogues MT, Marine-Font A, Vidal Carou MC (1997) Biogenic amines and polyamine content in meat and meat products. J Agric Food Chem 45:2098–2102
Hu Y, Huang Z, Li J, Yang H (2012) Concentrations of biogenic amines in fish, squid and octopus and their changes during storage. Food Chem 135:2604–2611
Hungerford J, Wu WH (2012) Comparison study of three rapid test kits for histamine in fish: bioscientific max signal enzymatic assay, neo genveratox ELISA, and the neogen reveal histamine screening test. Food Control 25:448–457
Hungerford JM, Arefyev AA (1992) Flow injection assay of enzyme inhibition in fish using immobilized diamine oxidase. Anal Chim Acta 261:351–359
Hwang C, Lee Y, Huang Y, Lin C, Shiau C, Hwang D, Tsa Y (2010) Biogenic amines content, histamine-forming bacteria and adulteration of bonito in tuna candy products. Food Control 21:845–850
Ibe A, Saito K, Nakazato M, Kikuchi Y, Fujinuma K, Nishima T (1991) Quantitative determination of amines in wine by liquid chromatography. J AOAC Int 74(4):695–698
Kantaria UD, Gokani RH (2011) Quality and safety of biogenic amines. Int J Res Pharm Biomed Sci 2(4):1461–1468
Karovicova J, Kohajdova Z (2005) Biogenic amines in food. Chem Pap 59(1):70–79
Kim JH, Ahn HJ, Kim DH, Jo C, Yook HS, Park HJ, Byun MW (2003) Irradiation effects on biogenic amines in Korean fermented soybean paste during fermentation. J Food Sci 68(1):80–84
Kung H, Wang T, Huang Y, Lin C, Wu W, Lin C, Tsai Y (2009) Isolation and identification of histamine-forming bacteria in tuna sandwiches. Food Control 20:1013–1017
Kung H, Lee Y, Huang Y, Lin W, Lin C, Chenb W, Tsai Y (2010) Biogenic amines content, histamine-forming bacteria, and adulteration of pork and poultry in tuna dumpling product. Food Control 21:977–982
Kung HF, Huang CY, Lin CM, Liaw LH, Lee YC, Tsai YH (2015) The histamine content of dried flying fish products in Taiwan and the isolation of halotolerant histamine-forming bacteria. J Food Drug Anal 23:335–342
Ladero V, Calles-Enríquez M, Fernández M, Alvarez MA (2010) Toxicological effects of dietary biogenic amines. Curr Nutr Food Sci 6:145–156
Latorre-Moratalla ML, Bosch-Fusté J, Lavizzari T, Bover-Cid S, Veciana-Nogués MT, Vidal-Carou MC (2009) Validation of an ultra-high pressure liquid chromatographic method for the determination of biologically active amines in food. J Chromatogr A 1216:7715–7720
Lee YC, Lin CS, Liu FL, Huang TC, Tsai YH (2015a) Degradation of histamine by Bacillus polymyxa isolated from salted fish products. J Food Drug Anal 23:836–844
Lee YC, Kung HF, Wu CH, Hsu HM, Chen HC, Huang TC, Tsai YH (2015b) Determination of histamine in milkfish stick implicated in food-borne poisoning. J Food Drug Anal 30:1–9
Lee YC, Kung HF, Huang CY, Huang TC, Tsai YH (2015c) Reduction of histamine and biogenic amines during salted fish fermentation by Bacillus polymyxa as a starter culture. J Food Drug Anal 30:1–7
Lehane L, Olley J (2000) Histamine fish poisoning revisited. Int J Food Microbiol 58:1–37
Lima AS, Gloria MBA (1999) Aminas bioativas em alimentos. Bol Soc Bras Ciênc Technol Aliment 33:70–79
Mah JH, Hwang HJ (2009) Effects of food additives on biogenic amine formation in Myeolchi-jeot, a salted and fermented anchovy (Engraulisjaponicus). Food Chem 114:168–173
Maijala RL, Eerola SH, Aho MA, Hirn JA (1993) The effect of GDL-induced pH decrease on the formation of biogenic amines in meat. J Food Protect 56:125–129
Makarios-Laham IK, Lee TC (1993) Protein hydrolysis and quality deterioration of refrigerated and frozen seafood due to obligately psychrophilic bacteria. J Food Sci 58(2):310–313
Malle P, Valle M, Bouquelet S (1996) Assay of biogenic amines involved in fish decomposition. JAOAC Int 79:43–49
Medina MA, Urdiales JL, Rodriguez-Caso C, Ramirez FJ, Sánchez-Jimenez F (2003) Biogenic amines and polyamines: similar biochemistry for different physiological missions and biomedical applications. Crit Rev Biochem Mol 38(1):23–59
Mieltz JL, Karmas E (1977) Polyamine and histamine content of rock-fish, salmon, lobster and shrimp as an indicator of decomposition. J AOAC Int 61(1):139–145
Mohamed R, Livia S, Hassan S, Soher E, Ahmed-Adel EB (2009) Changes in free amino acids and biogenic amines of Egyptian salted-fermented fish (Feseekh) during ripening and storage. Food Chem 115:635–638
Mohan CO, Ravishankar CN, Srinivasa Gopal TK, Ashok Kumar K, Lalita KV (2009) Biogenic amines formation in seer fish (Scomberomoruscommerson) steaks packed with O2 scavenger during chilled storage. Food Res Int 42:411–416
Montel M, Masson F, Talon R (1999) Comparison of biogenic amine content in traditional and industrial French dry sausages. Sci Aliment 19:247–254
Naila A (2012) Control of histamine in Rihaakuru: emerging approaches. PhD Thesis Massey University, New Zealand
Naila A, Flint S, Fletcher G, Bremer P, Meerdink G (2010) Control of biogenic amines in food-existing and emerging approaches. J Food Sci 75:R139–R150
Naila A, Flint S, Fletcher GC, Bremer PJ, Meerdink G, Morton RH (2012) Prediction of the amount and rate of histamine degradation by diamines oxidase (DAO). Food Chem 135:2650–2660
Nishikawa H, Tabata T, Kitani S (2012) Simple detection method of biogenic amines in decomposed fish by intramolecular excimer fluorescence. Food Nutr Sci 3:1020–1026
Onal A (2007) A review: Current analytical methods for the determination of biogenic amines in foods. Food Chem 103:1475–1486
Onal A, Tekkeli SEK, Onal C (2013) A review of the liquid chromatographic methods for the determination biogenic amines in foods. Food Chem 138:509–515
Oshima H, Bartsch H (1981) Quantitative estimation of endogenous nitrosation in humans by monitoring V-nitrosoproline excreted in the urine. Cancer Res 41:3658–3662
Ozogul F, Ozogul Y (2006) Biogenic amine content and biogenic amine quality indices of sardines (Sardinapilchardus) stored in modified atmosphere packaging and vacuum packaging. Food Chem 99:574–578
Parente E, Matuscelli M, Gadrini F, Grieco S, Crudele MA, Suzzi G (2001) Evolution of microbial populations and biogenic amines production in dry sausages produced in southern Italy. J Appl Microbiol 90:882–891
Phuvasate S, Su YC (2010) Effects of electrolyzed oxidizing water and ice treatments on reducing histamine-producing bacteria on fish skin and food contact surface. Food Control 21:286–291
Price RJ, Melvin EF (1994) Recommendations for on Board Handling of Albacore Tuna. Sea Grant Extension Program, Food Science and Technology Extension, University of California, Davis
Santos MHS (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29(2–3):213–231
Sato T, Okuzumi M, Fujii T (1995) Evaluation of polyamines of common mackerel during storage as indicators of decomposition. J Food Hyg Soc Jpn 36(6):743–747
Self R, Wu W (2012) Determination of eight biogenic amines in selected seafood products by MSPD extraction followed by UHPLC-Orbitrap MS. J Food Compos Anal 27:169–173
Self RL, Wu WH, Marks HS (2011) Simultaneous quantification of eight biogenic amine compounds in tuna by matrix solid-phase dispersion followed by HPLC-Orbitrap Mass Spectrometry. J Agric Food Chem 9:5906–5913
Sen NP, Schwinghamer LA, Donaldson BA, Miles WF (1972) N-Nitrosodimethyl amine in fish meal. J Agric Food Chem 20(6):1280–1281
Silla-Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213
Stadnik J, Dolatowski ZJ (2010) Biogenic amines in meat and refrigerated meat products. Acta Sci Pol Technol Aliment 9(3):251–263
Stratton JE, Hutkins RW, Taylor SL (1991) Biogenic amines in cheese and other fermented foods: a review. J Food Protect 54:460–470
Suyama M, Yoshizawa Y (1973) Free amino acid composition of skeletal muscle of migratory fish. Bull Jpn Soc Sci Fish 39:1339–1343
Til HP, Falke HE, Prinsen MK, Willems MI (1997) Acute and subacute toxicity of tyramine, spermidine, spermine, putrescine and cadaverine in rats. Food Chem Toxicol 35(3–4):337–348
Tsai YH, Lin CY, Chang SC, Chen HC, Kung HF, Wei CI et al (2005) Occurrence of histamine and histamine-forming bacteria in salted mackerel in Taiwan. Food Microbiol 22:461–467
Tsai YH, Lin CY, Chien LT, Lee TM, Wei CI, Hwang DF (2006) Histamine contents of fermented fish products in Taiwan and isolation of histamine forming bacteria. Food Chem 98:64–70
Veciana-Nogues MT, Marine FA, Vidal CMC (1997) Biogenic amines as hygienic quality indicators of tuna. Relationships with microbial counts, ATP-related compounds, volatile amines and organoleptic changes. J Agric Food Chem 45:2036–2041
Wei CI, Chen CM, Koburger JA, Otwell WS, Marshall MR (1990) Bacterial growth and histamine production on vacuum packed tuna. J Food Sci 55(1):59–63
Yassoralipour A, Bakar J, Rahman RA, Bakar FA (2012) Biogenic amines formation in barramundi (Latescalcarifer) fillets at 8°C kept in modified atmosphere packaging with varied CO2 concentration. LWT Food Sci Technol 48:142–146
Yatsunami K, Echigo T (1993) Studies on halotolerant and halophilic histamine forming bacteria. III. Changes in the number of halotolerant histamine forming bacteria and contents of non-volatile amines in sardine meat with addition of NaCl. Bull Jpn Soc Sci Fish 59:123–127
Zarei M, Najafzadeh H, Enayati A, Pashmforoush M (2011) Biogenic amines content of canned tuna fish marketed in Iran. American-Eurasian J Toxicol Sci 3:190–193
Zeisel SH, DaCosta K-A (1986) Increase in human exposure to methylamine precursors of 7V-Nitrosamines after eating fish. Cancer Res 46:6136–6138
Zou XN, Lu SH, Liu B (1994) Volatile N-nitrosamines and their precursors in Chinese salted fish-a possible etiological factor for NPC in China. Int J Cancer 59:155–158
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Biji, K.B., Ravishankar, C.N., Venkateswarlu, R. et al. Biogenic amines in seafood: a review. J Food Sci Technol 53, 2210–2218 (2016). https://doi.org/10.1007/s13197-016-2224-x
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-016-2224-x