Significance of biogenic amines to food safety and human health

doi:10.1016/S0963-9969(96)00066-X

Food Research International

Volume 29, Issue 7, October 1996, Pages 675-690

https://doi.org/10.1016/S0963-9969(96)00066-X Get rights and content

Abstract

Biogenic amines are natural antinutrition factors and are important from a hygienic point of view as they have been implicated as the causative agents in a number of food poisoning episodes, and they are able to initiate various pharmacological reactions. Histamine, putrescine, cadaverine, tyramine, tryptamine, β-phenylethylamine, spermine, and spermidine are considered to be the most important biogenic amines occurring in foods. These amines are designated as biogenic because they are formed by the action of living organisms. Histamine has been implicated as the causative agent in several outbreaks of food poisoning, while tyramine and β-phenylethylamine have been proposed as the initiators of hypertensive crisis. The toxicity of biogenic amines to chicks in terms of loss of weight and mortality was also reported. The toxicity of histamine appeared to be enhanced by the presence of other amines such as cadaverine, putrescine, and tyramine. Biogenic amines may also be considered as carcinogens because of their ability to react with nitrites to form potentially carcinogenic nitrosamines. The biogenic amine content of various foods and feed have been widely studied and found in cheese, fish and meat products, eggs and mushrooms. Food substances that have been prepared by a fermentative process, or have been exposed to microbial contamination during aging or storage, are likely to contain amines. Alcoholic beverages such as beers can contain biogenic amines, as do some other fermented foods such as sauerkraut and soy bean products. Amines were also considered as endogenous to plant substance that is commonly used for food, where some fruits and vegetables were found to contain high concentrations of various amines.

References (165)

S.H. Arnold et al.
Histamine toxicity from fish products
Adv. Food Res.
(1978)
A.M. Asatoor et al.
Tranylcypromine and cheese
Lancet
(1963)
L.F. Bjeldanes et al.
On the aetiology of scombroid poisoning: cadaverine potentiation histamine toxicity in the guinea pig
Food Cosmet. Toxicol.
(1978)
B. Blackwell
Hypertensive crises due to monoamine oxidase inhibitors
Lancet
(1963)
B. Blackwell et al.
Tyramine in cheese related to hypertensive crises after monoamine oxidase inhibition
Lancet
(1965)
S. Buncic et al.
Effect of gluconodeltalactone and Lactobacillus plantarum on the production of histamine and tyramine in fermented sausages
Int. J. Food Micro.
(1993)
M.E. Doyle et al.
S. Eerola et al.
Liquid chromatography deteminatin of biogenic amines in dry sausages
J. AOAC Int.
(1993)
F. Franzen et al.
A.K. Halama
Muskelmagenulzera der Jung-masthiihner-ein Fanahrungsscha-den?
Wiener TierarAche Monatsschrift
(1973)

R. Ijomah et al.

The importance of endogenous histamine relative to dietary histamine in the aetiology of scombrotoxicosis

Food Add. Contam.

(1991)

H.M.L.G. Joosten et al.

Conditions allowing the formation of biogenic amines in cheese. 1. Decarboxylative properties of starter bacteria

Neth. Milk Dairy J.

(1987)

R. Maijala et al.

The effect of GDL-induced pH decrease on the formation of biogenic amines in meat

J. Food Protection

(1993)

A. Marine-Font

Alimentos y medicamentos: Interactions (3a parte)

Cire. Farm.

(1978)

C.K. Murray et al.

Scombrotoxin and scombrotoxin-like poisoning from canned fish

J. Hyg. Comb.

(1982)

M.J.R. Nout et al.

Effect of processing conditions on the formation of biogenic amines and ethyl carbarnate in soybean tempe

J. Food Safety

(1993)

M.A. Abdalla et al.

Correlation between biogenic amines, chemical changes and stability of sea bream fish during storage at -18 °C

Grasa y Aeites

(1990)

R.E. Andersson

Biogenic amines in lactic acid fermented vegetables

Leben- Wiss.- Technol.

(1988)

Normas sanitarias apficables a la produccion y a la puesta en el mercado de los productos pesqueros

(1991)

S.H. Arnold et al.

Histamine formation by bacteria isolated from skipjack tuna Katsuwonus plamis

Bull. Jpn. Soc. Sci. Fish.

(1980)

A. Askar

A. Askar et al.

Biogene Amine in Lebensmitteln. Vorkommen, Bedeutung und Bestimmung

(1986)

A. Askar et al.

Biogenic amines in fish products

Deutsche lebensmittel Rundschau

(1986)

J.C. Ayres et al.

N.P.M. Bakker et al.

The effect of biogenie amines in young chickens

B.A. Bartholomew et al.

Scombrotoxic fish poisoning in Britain: features of over 250 suspected incidents from 1976–1986

Epidem. Inf.

(1987)

A.A. Boulton et al.

Hypertensive crises in a patients on MAOI antidepressants following a meal of beef liver

Can. Med. Anoc. J.

(1970)

C. Cantoni et al.

Amino acids, histamine and tyramine variation during ripening of dry sausage (salami)

Ind. Aliment.

(1974)

C.-M. Chen et al.

Relationship between changes in biogenic amine contents and freshness of pork during storage at different temperatures

J. Chin. Agri. Chem. Soc.

(1994)

K.D.H. Chin et al.

Identification and estimation of histamine, tryptamine, phenylethylamine, and tyramine in soy sauce by thin layer chromatography of dansyl derivatives

J. Food Sci.

(1983)

C.H. Chu et al.

Effect of diamines, polyamines and tuna fish extracts on the binding of histamine to mucin in vitro

J. Food Sci.

(1981)

C.H. Chu et al.

Effect of diamines, polyamines and tuna fish extracts on the binding of histamine to mucin in vitro

J. Food Sci.

(1981)

M.N. Clifford et al.

Studies with volunteers on the role of histamine in suspected scombrotoxicosis

J. Sci. Food Agric.

(1989)

M.A. Degheidi et al.

Development of some biogenic amines during Ras cheese ripening with special reference to different starters

N. Dierick et al.

Changes in nonprotein nitrogen compounds during dry sausage ripening

J. Food Sci.

(1974)

H.M.G. Doeglas et al.

Histamine intoxication after cheese

Lancet

(1967)

F. Durr et al.

Biogenic amines in raw fish and fried fish products

Lebensmittelindustrie

(1980)

R.A. Edwards et al.

Amines in fresh beef of normal pH and the role of bacteria in changes in concentration observed during storage in vacuum packs at chill temperature

J. Appl. Bacterial.

(1987)

R.A. Edwards et al.

The relationship of bacterial numbers and types to diamine concentration in aerobically stored beef, pork, and lamb

J. Food Technol.

(1983)

S.T. Edwards et al.

Public health significance of amines in cheese

J. Dairy Sci.

(1981)

R.R. Eitenmiller et al.

Enzymatic mechanisms for amine formation in fish

A.T. El-Akel

Biogenic amines and other quality changes in sardine uninculated and insulated with P. morganii

M.M. El-Sayed

Biogenic amines in processed cheese available in Egypt

Int. J. Dairy Sci.

(1997)

A.I. El-Zayat et al.

Tryptamine, tyramine, and histamine content of Domiati, Ras, and Roquefort cheese

Egypt. J. Food Sci.

(1988)

F. Ender et al.

Isolation and identification of a hepatotoxic factor in herring meal produced from sodium nitrite preserved herring

Naturwissenschaften

(1964)

FDA

Defect action levels for histamine in tuna; availability of guide

Fed. Reg.

(1982)

M. Ferencik

Formation of histamine during bacterial decarboxylation of histidine in the flesh of some marine fishes

J. Hyg. Epidemiol. Microbial. Immunol.

(1970)

G. Fran et al.

Chemical indices of decomposition in tuna

H.A. Frank et al.

Histamine formation and hortycombing during decomposi tion of skipjack tuna (Kalsuwotius pelamis) at elevated temperatures

Mar. Fish. Rev.

(1981)

H.A. Frank et al.

Identification and decarboxylase activities of bacteria isolated from decomposed mahimahi after incubation at 0 and 32 °C

Int. J. Food Microbiol.

(1985)

O.K. Fossum et al.

Gizzard erosions as a cause of mortality in white leghorn chickens

Avion Pathol.

(1988)

Cited by (1110)

A polydiacetylene (PDA) based dual-mode optical sensor for the ppb level selective detection of biogenic polyamines
2024, Sensors and Actuators B: Chemical
Biogenic polyamines (BPAs), specifically spermine and spermidine, play vital roles in cellular physiology, influencing processes like cell growth and proliferation. Beyond their cellular implications, these amines serve as biomarkers for cancer and aging-related diseases. This study presents a dual-output optical sensor for BPAs using polydiacetylene (PDA). The sensor utilizes alendronate's phosphate groups as recognition units for BPAs in liquid and solid phases. Ammonium groups of BPAs interact with negatively charged alendronate-modified PDA (PDAPH) liposomes causing a color change from blue to red accompanied by a gradual increase in fluorescence output at λ_max 622 nm. The sensor exhibits high sensitivity with low detection limits of 4.3 ppb and 5.1 ppb for spermine and spermidine in colorimetric analysis, and lower limits of 1.6 and 1.4 ppb in fluorimetric measurements respectively, demonstrating its dual output ability. PDAPH liposomes also respond to cadaverine and putrescine indicating the probe's ability to detect key BPAs. The sensor shows minimal responses to interfering species, confirming its selective affinity towards BPAs. Practical validation in real water, urine, and serum samples demonstrates the sensor's efficiency. Immobilization of PDAPH liposomes into sodium alginate results in the creation of PDA beads. These beads exhibit a discernible color change when exposed to BPA concentrations exceeding 0.3 μM with a sufficiently low detection limit of 11.7 ppb in the solid phase. These findings highlight the efficiency of the PDAPH liposome sensor for accurate and reliable biogenic polyamine detection.
Effects of the physical structure and surface charge of activated carbon on the reduction of biogenic amines in anchovy fish sauce
2024, Food Chemistry
This study aimed to efficiently reduce a large number of biogenic amines in salt-fermented fish sauce while minimizing sensory reduction using various activated carbons. Aromatic amines, such as tryptamine and phenethylamine, were reduced by 86.1–100 % after treating with activated carbon. Histamine with a heterocyclic structure decreased by 13–42 %. No significant effects were observed on the levels of aliphatic amines, putrescine, cadaverine, spermine, and spermidine. The major taste component, amino acid nitrogen, was reduced to within 3 %, and brown color removal was reduced depending on the type of activated carbon used. Acid-modified AC-A and AC-B had rough surfaces, high total acidity, low point of zero charge (pHpzc), and rich surface functional groups. Owing to its smooth surface, low total acidity, high pHpzc, and few surface functional groups, AC-C exhibited a higher histamine elimination and less color reduction despite its lower surface area compared to other activated carbons.
Packaged europium/fluorescein-based hydrogen bond organic framework as ratiometric fluorescent probe for visual real-time monitoring of seafood freshness
2024, Talanta
The freshness of sea food has always been the focus of attention from consumers, and food-safety issues are in urgent need of efficient approaches. A HOF-based ratiometric fluorescence probe (HOF-FITC/Eu) featuring superior amine-response, offers the real-time and visual detection of seafood freshness. Via intermolecular hydrogen bond interaction to form hydrogen-bonded organic frameworks (HOFs), which serve as a structural basis for the conjugate loading of pH-sensitive fluorescein (5-FITC) and coordination doping of lanthanide Eu³⁺. Amine vapors stimulate the dual-wavelength (525 nm and 616 nm) characteristic fluorescence of HOF-FITC/Eu with an inverse trend, resulting in an increase of the ratio of I₅₂₅ to I₆₁₆ accompanied by a distinct color transition from red to green. Prepared HOF-FITC/Eu featuring sensitive red-green color change characteristics of amine response are readily dripped into composite films of filter paper through integrated smartphone and 254 nm UV lamp as mobile observation devices to on-site monitor the freshness of raw fish and shrimp samples. The intelligent food probe HOF-FITC/Eu opens a novel material assembly type for fluorescence sensing and a potential pathway for other functional materials in the field of investigational food.
Charge-driven complexes formed by conjugated polyelectrolytes as sensing platforms for biogenic amines
2024, Journal of Photochemistry and Photobiology A: Chemistry
We developed sensing platforms to detect and differentiate various types of biogenic amines, cadaverine, putrescine, spermine, histamine, tyramine and tryptamine by monitoring the changes in fluorescence signal. The sensing platforms comprised a carboxylated polyfluorene derivative doped with benzothiadiazole acceptor moieties in a small fraction (20%). When utilized as an individual sensing component, the conjugated polyelectrolyte detects all BAs nonselectively via binding-induced fluorescence quenching. If the conjugated polyelectrolyte forms an intermediary charge-driven complex with an oppositely charged surfactant, a Förster resonance energy transfer (FRET) response is triggered. Biogenic amines are detected through their effects on the FRET signal as enhancement, reduction, or no effect. We formed intermediary charge-driven complexes at nonstoichiometric, cation deficient and excess conditions. Supramolecular interactions governed the co-assembly and disassembly caused by the targeted amines on the conjugated polyelectrolyte-surfactant complex. Therefore, structural and charge-related differences enabled their selective detection in our sensing platforms. Among them, spermine exhibited the highest FRET enhancement effect due to its polycationic aliphatic structure by engaging in multi-point interchain contacts among conjugated polyelectrolyte chains. In contrast, tryptamine showed a unique quenching effect on the FRET signal due to the steric hindrance created by its bulky, heterocyclic structure, leading to the dissociation of the complexes.
A ratiometric fluorescence platform for on-site screening meat freshness
2024, Food Chemistry
Meat freshness is related to food safety and human health. Developing a simple and effective method for on-site detection of meat freshness is essential to ensure food safety. This study aimed to explore a ratiometric fluorescence platform for on-site screening of meat freshness. We synthesized a series of benzothiazole-based fluorescent compounds (BM, BHM and BTH), each with different recognition groups for detecting meat freshness biomarkers cadaverine (Cad) and putrescine (Pte). The optimized 2-(2′-hydroxyphenyl-3-aldehyde-5–1,3-indanedione) benzothiazole (BTH) demonstrated a noticeable color and fluorescence change, a fast response (<15 min), and high selectivity and sensitivity (LOD = 70 nM) to Cad. Portable test strips based on BTH were prepared for rapid visual detection of meat freshness, which exhibited visible color and fluorescen color changes to Cad and Pte. Furthermore, a portable smartphone–based fluorescence device integrated with a self-programmed Python program was fabricated and used on-site to monitor Cad and Pte within 5 min. The BTH-loaded portable test strips were successfully employed as low-cost, high-contrast, fast-response, and smartphone-adaptable fluorescent labels for detecting Cad and Pte in meat samples under different temperatures (25 °C, 4 °C, and –20 °C). This enabled consumers and food supply chain stakeholders to quickly and visually monitor the meat freshness in real beef, chicken, and pork products.
Development and evaluation of a gas chromatography-mass spectrometry method for biogenic amines to assess decomposition in seafood
2024, Journal of Food Composition and Analysis
Biogenic amines (BAs) are low molecular mass compounds formed by the microbial-induced decarboxylation of specific amino acids. These molecules are markers of quality index and can indicate potential spoilage of a product. Currently, the FDA relies on sensory analysis as well as indole and histamine levels to evaluate the degree of seafood decomposition. However, there is a need for alternative analytical methods to corroborate those analyses. An optimized dispersive liquid-liquid microextraction (DLLME) method was developed for the extraction of four BAs (putrescine, cadaverine, histamine and tyramine) from various decomposition stages of nine seafood species previously tested by the FDA Seafood Sensory Experts. The BAs depicted very different concentration patterns between species and were able to distinguish within-species decomposition stages classified by the organoleptic analysis as “borderline increments”. The results suggest that all four analyzed BAs can be potentially used as biomarkers of seafood decomposition, but the choice of biomarker is species dependent. Some of the prominent associations were putrescine in shrimp, cadaverine in weakfish, histamine in canned tuna, and tyramine in scallops. The differentiation between “borderline” stages of decomposition also demonstrates the suitability of the method to support the FDA sensory analyses of seafood, ultimately leading to improved consumer protection.

View all citing articles on Scopus

View full text

Significance of biogenic amines to food safety and human health

Abstract

Adv. Food Res.

Lancet

Food Cosmet. Toxicol.

Lancet

Lancet

Int. J. Food Micro.

J. AOAC Int.

Wiener TierarAche Monatsschrift

Food Add. Contam.

Neth. Milk Dairy J.

J. Food Protection

Cire. Farm.

J. Hyg. Comb.

J. Food Safety

Correlation between biogenic amines, chemical changes and stability of sea bream fish during storage at -18 °C

Grasa y Aeites

Biogenic amines in lactic acid fermented vegetables

Leben- Wiss.- Technol.

Normas sanitarias apficables a la produccion y a la puesta en el mercado de los productos pesqueros

Histamine formation by bacteria isolated from skipjack tuna Katsuwonus plamis

Bull. Jpn. Soc. Sci. Fish.

Biogene Amine in Lebensmitteln. Vorkommen, Bedeutung und Bestimmung

Biogenic amines in fish products

Deutsche lebensmittel Rundschau

The effect of biogenie amines in young chickens

Scombrotoxic fish poisoning in Britain: features of over 250 suspected incidents from 1976–1986

Epidem. Inf.

Hypertensive crises in a patients on MAOI antidepressants following a meal of beef liver

Can. Med. Anoc. J.

Amino acids, histamine and tyramine variation during ripening of dry sausage (salami)

Ind. Aliment.

Relationship between changes in biogenic amine contents and freshness of pork during storage at different temperatures

J. Chin. Agri. Chem. Soc.

Identification and estimation of histamine, tryptamine, phenylethylamine, and tyramine in soy sauce by thin layer chromatography of dansyl derivatives

J. Food Sci.

Effect of diamines, polyamines and tuna fish extracts on the binding of histamine to mucin in vitro

J. Food Sci.

Effect of diamines, polyamines and tuna fish extracts on the binding of histamine to mucin in vitro

J. Food Sci.

Studies with volunteers on the role of histamine in suspected scombrotoxicosis

J. Sci. Food Agric.

Development of some biogenic amines during Ras cheese ripening with special reference to different starters

Changes in nonprotein nitrogen compounds during dry sausage ripening

J. Food Sci.

Histamine intoxication after cheese

Lancet

Biogenic amines in raw fish and fried fish products

Lebensmittelindustrie

Amines in fresh beef of normal pH and the role of bacteria in changes in concentration observed during storage in vacuum packs at chill temperature

J. Appl. Bacterial.

The relationship of bacterial numbers and types to diamine concentration in aerobically stored beef, pork, and lamb

J. Food Technol.

Public health significance of amines in cheese

J. Dairy Sci.

Enzymatic mechanisms for amine formation in fish

Biogenic amines and other quality changes in sardine uninculated and insulated with P. morganii

Biogenic amines in processed cheese available in Egypt

Int. J. Dairy Sci.

Tryptamine, tyramine, and histamine content of Domiati, Ras, and Roquefort cheese

Egypt. J. Food Sci.

Isolation and identification of a hepatotoxic factor in herring meal produced from sodium nitrite preserved herring

Naturwissenschaften

Defect action levels for histamine in tuna; availability of guide

Fed. Reg.

Formation of histamine during bacterial decarboxylation of histidine in the flesh of some marine fishes

J. Hyg. Epidemiol. Microbial. Immunol.

Chemical indices of decomposition in tuna

Histamine formation and hortycombing during decomposi tion of skipjack tuna (Kalsuwotius pelamis) at elevated temperatures

Mar. Fish. Rev.

Identification and decarboxylase activities of bacteria isolated from decomposed mahimahi after incubation at 0 and 32 °C

Int. J. Food Microbiol.

Gizzard erosions as a cause of mortality in white leghorn chickens

Avion Pathol.