International Journal of Food Microbiology 29 (1996) 213-231

Biogenic amines: their importance in foods

M.H. Silla Santos
Institute de Agroquimica

y Tecnologia de Alimentos. Apdo. de Correos 73, 46100 Burjassot, Valencia, Spain

Received 21 February 1995; revised 15 May 1995; accepted 3 June 1995

Abstract
Biogenic amines are important nitrogen compounds of biological importance in vegetable, microbial and animal cells. They can be detected in both raw and processed foods. In food

microbiology they have sometimes been related to spoilage and fermentation processes. Some toxicological characteristics and outbreaks of food poisoning are associated with histamine and tyramine. Secondary amines may undergo nitrosation and form nitrosamines. A better knowledge of the factors controlling their formation is necessary in order to improve the quality and safety of food.
Keywords: Biogenic amines; Food quality; Microbiology; Toxicity

1. Biogenic

amines

Definition: Biogenic amines are basic nitrogenous compounds formed mainly by decarboxylation of amino acids or by amination and transamination of aldehydes and ketones (Askar and Treptow, 1986; Maijala et al., 1993). They are organic bases with low molecular weight and are synthesized by microbial, vegetable and animal metabolisms (Brink et al., 1990). Biogenic amines in food and beverages are formed by the enzymes of raw material or are generated by microbial decarboxylation of amino acids (Brink et al., 1990; Hal&z et al., 1994) but it has been found that some of the aliphatic amines can be formed Iin viva by amination from corresponding aldehydes (Hartmann, 1967; Maijala et al., 1993). The chemical structure of biogenic amines can either be: aliphatic (putrescine,

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cadaverine, spermine, spermidine); aromatic (tyramine, phenylethylamine); heterocyclic (histamine, tryptamine). Amines such as polyamines, putrescine, spermidine, spermine and also cadaverine are indispensable components of living cells and are important in the regulation of nucleic acid function and protein synthesis and probably also in the stabilization of membranes (Bard&z et al., 1993; Maijala et al., 1993; Hal&z et al., 1994). The precursors of the main biogenic amines involved in food poisoning are: histidine + histamine tyrosine + tyramine hydroxytryptophane + serotonin tryptophane + tryptamine lysine -+ cadaverine ornithine -+ putrescine arginine + spermine arginine --f spermidine Prerequisites for biogenic amine formation by microorganisms are: - Availability of free amino acids, but not always leading to amine production (Marklinder and Liinner, 1992). - Presence of decarboxylase-positive microorganisms (Tiecco et al., 1986; Brink et al., 1990; Huis int Veld et al., 1990). - Conditions that allow bacterial growth, decarboxylase synthesis and decarboxylase activity (Brink et al., 1990).

2. Biogenic amines in food In virtually all foods that contain proteins or free amino acids and are subject to conditions enabling microbial or biochemical activity biogenic amines can be expected. The total amount of the different amines formed strongly depends on the nature of the food and the microorganisms present (Brink et al., 1990). Biogenic amines are present in a wide range of food products including fish products, meat products, dairy products, wine, beer, vegetables, fruits, nuts and chocolate (Askar and Treptow, 1986; Brink et al., 1990). 2. I. Non-fermented food

In non-fermented foods, the presence of biogenic amines above a certain level is considered as indicative of undesired microbial activity. Therefore, the amine level could be used as an indicator of microbial spoilage. However, the presence of biogenic amines in food does not necessarily correlate with the growth of spoilage organisms, because they are not all decarboxylase-positive (Santos et al., 1985; Vidal et al., 1990). Levels of histamine, putrescine and cadaverine usually increase during spoilage of fish and meat whereas levels of spermine and spermidine decrease during this process (Brink et al., 1990). In rainbow trout, Dawood et al. (1988) isolated cadaverine, putrescine,

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spermine and spermidine in higher amounts during the storage period, varying with temperature. Fish. Scombroid fish have most commonly been associated with incidents of histamine intoxication (scombrotoxicosis). The formation of histamine in scombroid and other marine fish containing abundant endogenous histidine has been attributed to microbial action rather than to endogenous histidine decarboxylase activity (Baranowski et al., 1985; Hal&z et al., 1994). The histidine can be catabolized by two ways in fish muscle. The amino acid deamination to obtain urocanic acid or the histidine decarboxylation to form histamine (Mackie and Femandez, 1977). The deamination activity is the principal way in normal physiological conditions; decarboxylation activity can be most important in other circumstances, e.g. bacterial contamination (Vidal and Marine, 1984). Several studies of the normal microbial population of marine fish revealed their ability to produce high amounts of histamine at low temperatures (Baranowski et al., 1985; Klausen and Huss, 1987; Hal&z et al., 1994; Valeiro and Pilas, 1994). Different biogenic amines (histamine, putrescine, cadaverine, tyramine, spermine, spermidine) have been detected in fish such as mackerel, herring, tuna, sardines (Vidal and Marine, 1984; Baranowski et al., 1985; Ramesh and Venugopalan, 1986; Dawood et al., 1988; Middlebrooks et al., 1988; Lebiedzinska et al., 199 1; Gajewska and Ganowiak, 1992; Luten et al.,1992; Wendakoon and Sakaguchi, 1992; Yatsunami and Echigo. 1993; Shalaby, 1994). Other amines, such as trimethylamine and dimethylamine are present in fish and fish products at levels determined by the fish freshness (Hotchkiss, 1989; Pfundstein et al., 1991; Tricker et al., 1991; Gajewska and Ganowiak, 1992; Kolodziejska et al., 1994). Fruit, juices and vegetables. Several juices, nectars and lemonades made from oranges, raspberries, lemons, grapefruit, mandarins, strawberries, currants and grapes contain different biogenic amines in variable concentrations, putrescine being the most important (Maxa and Brandes, 1993). Hal&z et al. (1994) have reported high amine levels in orange juice (noradrenaline, tryptamine), tomato (tyramine, tryptamine, histamine), banana (tyramine, noradrenaline, tryptamine, serotonin), plum (tyramine, noradrenaline) and spinach leaves (histamine). Phenylethylamine is also a natural constituent of cocoa beans and thus occurs in chocolate, chocolate products and confectionery containing chocolate. Some species of mushrooms also contain high levels of phenylethylamine and in white and black pepper and soya sauce high levels of pyrrolidine have been detected (Pfundstein et al., 1991). Histamine and cadaverine have been detected in carrageenan from algae (Barwell, 1994). Meat. Fresh and processed pork meat contain high levels of adrenaline, spermidine and spermine but low levels of noradrenaline, putrescine, histamine, cadaverine and tyramine (Hal&z et al., 1994). In cooked and uncooked ground beef and in pork meat various biogenic amines have been identified (Nemeth-Szerdahelyi et al., 1993). Histamine and the factors determining its synthesis have been determined in bovine and sheep muscle by TeodoroviC et al. ( 1994) and in other kinds of meat and meat products (Santos et al., 1985). Meat from harp seal (Phoca groenlandica) has a high protein content and is well-balanced in its essential amino acid composition (Shahidi et al., 1990) and

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non-protein nitrogen compounds such as amines, including ethanolamine, spermine and spermidine (Shahidi et al., 1993). Milk. In rat and human milk, spermine, spermidine and putrescine have been detected with great individual variability. A case of human milk even showed a pronounced variation in the concentration of spermine and spermidine between the left and right breast (Romain et al., 1992). In full cream and semi-skimmed cows milk low amounts of these polyamines have been detected (Bard&z et al., 1993).

2.2. Fermented-food

During the preparation of fermented food one can expect the presence of many kinds of microorganisms, some of them being capable of producing biogenic amines. Most products in which lactic acid bacteria grow contain considerable amounts of putrescine, cadaverine, histamine and tyramine (Brink et al., 1990). Cheeses and dairy products. After fish, cheese is the next most commonly implicated food item associated with histamine poisoning and the first reported case occurred in 1967 in the Netherlands and involved Gouda cheese (Stratton et al., 19911. Many studies have been undertaken to determine the amine content of cheese products. A variety of amines, such as histamine, tyramine, cadaverine, putrescine, tryptamine and phenylethylamine have been found in many types of cheeses (Sumner et al., 1985; Iiligo et al., 1986; Vidaud et al., 1987; Stratton et al., 1991; Besanson et al., 1992; Celano et al., 1992; Diaz et al., 1992; Moret et al., 1992a, b; Lavanchy and Sieber, 1993). Histamine and tyramine occur in levels varying extensively not only between different cheese varieties but within the varieties (Stratton et al., 1991). Fermented vegetables. In sauerkraut production a succession of micropopulations are seen and biogenic amines can be expected (Taylor et al., 1978; Brink et al., 19901, especially putrescine, accumulated in sauerkraut brine. Very low levels of biogenic amines were detected in a study of Asian foods. Low levels of tyramine were found in commercial samples of Japanese pickled vegetables (urume-zuke and in kim thee, a traditional Korean fermented cabbage) (Stratton et al., 1991). Miso, an important, popular fermented soybean food in the Orient, is a semisolid fermented soy paste produced by fermentation of cereal grain, soybeans and salt by the action of moulds, yeasts and bacteria (Chin and Koehler, 1986). In miso, tyramine and histamine have been detected by Ibe et al., 1991a, Ibe et al., 1992a, Ibe et al., 1992b). Fermented meat products. Fermented meat products have not been extensively studied, and it has been pointed out that starter cultures result in the formation of smaller amounts of biogenic amines than when natural microflora is responsible of fermentation (Silla, 1985; Bun% et al., 1993; Maijala et al., 1993). In a study of changes in histamine and tyramine contents during storage/spoilage of beef and pork meat at both refrigerated and room temperatures and the subsequent fermentation process, Vidal et al., 1990 detected a notable increase in the content of amines at both temperatures. Maijala and Eerola, 1993 detected increased concentrations of histamine and tyramine during sausage fermentation. Fermentation may be important in the formation of histamine in certain types of sausages. Semi-dry sausages are

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fermented for short periods, often with lactic acid cultures, while dry sausages are allowed to ferment through the action of natural microflora for a longer period. During this sausage-ripening process, the histamine concentration increases at least IO-fold during the first 3 days of ripening (Shalaby, 1993). Dry sausages not added with starter cultures showed variable concentrations of biogenic amines, probably due to variations in the ripening process and the composition of the microflora responsible for the spontaneous fermentation (Butturini et al., 1995; Cantoni, 1995). The use of acidulants such as GDL may influence amine production (Santos et al., 1986b; BunciC et al., 1993; Maijala et al., 1993). In Italian sausages the presence of biogenic amines has been related to the composition of the microflora during ripening (Tiecco et al., 1986). In various Spanish meat products, Santos et al. (1985) detected higher levels of tyramine in fermented and cured products than in fresh products. Polyamines, putrescine, cadaverine and histamine, tyramine and 2-phenylethylamine have also been detected in fermented sausages (Straub et al., 1993). Cured meat products with high levels of histamine and tyramine have been linked with food poisoning (Santos et al., 1985, 1986b; Tiecco et al., 1986; Vidal et al., 1990; Beutling, 1993; Bun&C et al., 1993; Maijala et al., 1993; Maijala and Eerola, 1993; Shalaby, 1993; TeodoroviC et al., 1994). Wine and beer. Agmatine, cadaverine, ethanolamine, histamine, putrescine and tyramine are produced in higher quantities during alcoholic fermentation (Buteau et al., 1984). Histamine and tyramine in red wine has been reported by Bravo et al. (19831, Ough et al. (19871, Hanna et al. (1988), Littlewood et al. (1988), Stratton et al. (1991) and Pogorzelski (1992). Many types of biogenic amine have been detected in both white and red wine: tyramine, histamine, tryptamine, monomethylamine, 2-phenethylamine, putrescine, cadaverine, spermidine, iso- and n-amylamine, pyrrolidine, iso- and n-butylamine, iso- and n-propylamine and ethylamine (Ibe et al., 1991b; Lehtonen et al., 1992). In beers the presence of tyramine (Wheatley and Tinton, 1987; Hal&z et al., 1994) and histamine (Dumont et al., 1992) has also been demonstrated. Fermented fish products. Although little research has been conducted to determine the biogenic amine content of fermented fish products, it appears that the levels of these amines can vary extensively. The evolution of volatile nitrogen compounds during the processing and storage of a Ghananian fermented fish has been studied by Yankah et al., 1993. They detected trace quantities of putrescine, tyramine, agmatine and tryptamine; histamine was not detected. Only spermidine was higher after fermentation. Mizutani et al., 1992 detected omithine and citrulline as decomposition products of arginine in fish sauce and histamine was also found. In a study on anchovies, Ayensa, 1993 found a high level of biogenic amines during the manufacturing process, due to the long processing time which favours bacterial growth (Santos et al., 1986a; Veciana et al., 1989). The level of histamine which constitutes a toxic limit is uncertain as enhancers of toxicity which lower the effective dosage may be present in fish. The formation of histamine is very variable and dependent on time, temperature, and the type and quantity of the microorganisms present. Good correlation has been found between expert sensory decisions on quality and levels of putrescine and cadaverine in fish (Sims et al., 1992).

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3. Microorganisms

producing

biogenic amines

Although aminoacid decarboxylases are not widely distributed among bacteria, species of many genera such as Bacillus, Citrobacter, Clostridium, Klebsiella, Escherichia, Proteus, Pseudomonas, Salmonella, Shigella, Photobacterium, and the lactic bacteria Lactobacillus, Pediococcus and Streptococcus are capable of decarboxylating one or more amino acid (Rice et al., 1976; Brink et al., 1990; Huis int Veld et al., 1990). Organisms like Morganella morganii (Proteus morganii), certain strains of Klebsiella pneumoniae and a few strains of Hafnia aluei, are prolific histamine producers and are important in the microbiology of fish products (Femandez and Mackie, 1979; Yamani and Untermann, 1985; Bryan, 1987; Stratton et al., 1991; Wendakoon and Sakaguchi, 1992; Valeiro and Pilas, 1994). Ground beef inoculated with Proteus morganii contained histamine at a concentration of 595 pg/g while the level of histamine of meat without P. morganii was 8.26 pg/g (Teodorovic et al., 1994). Luminous bacteria can also produce histamine. These organisms are halophilic, and both mesophilic and psychrophilic species have been reported to exist (Stratton et al., 1991). Morii et al. (1986, Morii et al., 1988) reported that Photobacterium phosphoreum, a psychrophile, maybe primarily responsible for histamine production in scombroid fish at low temperatures. Tyrosine and histidine decarboxylase activities have been detected in Escherichia coli (Blackwell and Mabbitt, 1965) and Pseudomonas spp. (Rice et al., 1976; Diaz et al., 1992). Enterococcusfaecalis has been associated with tyramine in Cheddar cheese (Celano et al., 1992). In miso tyrosine decarboxylase bacteria have been identified as Enterococcus faecium and Lactobacillus bulgaricus and histamine decarboxylase has been associated with Lactobacillus spp. and Lactobacillus sanfrancisco (Ibe et al., 1992a, b). Staphylococcus spp., Vibrio spp., and Pseudomonas spp. have been identified as histamine-producing bacteria in fermented fish (Yankah et al., 1993; Yatsunami and Echigo, 1993). Amine-producing lactic bacteria such as Lactobacillus breuis, Lactobacillus buchnerii, Lactobacillus curuatus, Lactobacillus carnis, Lactobacillus dicergens (Carnobacterium piscicola, Carnobacterium dinergens, respectively) and Lactobacillus hilgardii have been isolated from meat and meat products (Maijala et al., 1993). In salami, Tiecco et al (1986) associated histamine synthesis with Gram negative bacteria like Pseudomonas fluorescens, Citrobacter ,freudii and Acinetobacter calcoaceticus car. anitratum and a few Gram positive, including micrococci and staphylococci. In a laboratory medium, tyramine was produced by Enterococcus, Lactococcus, Proteus and Pseudomonas but not by Acinetobacter, Bacillus, Escherichia, Hafnia, Salmonella arizonae, Serratia marcescens, Shigella or Yersinia enterocolitica, nor by the yeast species examined with the exception of Candida krusei (Beutling, 1993). Results from studies on the malo-lactic fermentation of wine do not support the hypothesis that histamine is formed by the yeasts and bacteria involved (Ough et al., 1987). However, recent investigations have indicated that the malo-lactic fermentation bacterium Pediococcus cereuisiae, which withstands the presence of sulphur dioxide

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better than Leuconostoc oenos, can be regarded as histamine producer in certain wines (Pogorzelski, 1992). During fermentation of the classical local Belgium beers cadaverine, putrescine and spermine concentrations fluctuate linked with the evolution of different yeast species which respectively produce and use biogenic amines in their metabolism (Dumont et al., 1992). All in all it appears that amino acid decarboxylase enzymes are not well distributed amongst beer and wine yeasts and the more commonly used malo-lactic fermentation bacteria (Ough et al., 1987). In the case of fermented food and beverages the introduction of starter cultures can affect the production of biogenic amines either directly or indirectly through interaction between different microbial populations, which are probably very important (Huis int Veld et al.,1990). Appropiate selection criteria for bacteria use as starter cultures should include analyses of amine production.

4. Factors affecting amine-decarboxylase activity Since amines are formed by enzymatic activity of the food or decarboxylase active bacteria, inhibition of such activity and prevention of bacterial growth would be very important for controlling the amine content of food. Manufacturing conditions influence the production of biogenic amines. Thus, tyramine, putrescine and cadaverine concentrations in tempeh were low or high depending on the applied manufacturing process: soaked soybeans, type of fern-tentative microorganisms, boiling, home cooking by stewing or frying in oil, and storage temperature (Nout et al., 1993). Histamine production in cheese has been related to factors such as availability of substrate, pH, salt concentration and temperature. The proper storage temperature is probably the most important method of prevention (Stratton et al., 1991). The pH level is an important factor influencing aminodecarboxylase activity. Santos et al., 1986a found a higher tyramine level in mackerel when the pH was low, and Pogorzelski, 1992 found that the histamine concentration in wine was higher with a pH above 3.77, which confirms previous investigations (Mayer, 1976; Aerny, 1982). The optimum level for tyramine synthesis in cheese is pH 5.0 (Diaz et al., 19921, coinciding with the optimum for histidine decarboxylase activity, but it was not defined by which microorganism, being assumed to Escherichia coli, Pseudomonas spp. and Proteus spp. Baranowski et al., 198.5 found that the conversion of histidine to histamine by Klebsiella pneumoniae UH-2 isolated from skipjack tuna has an optimum pH of 4.0, with ca. 70% of this activity maintained at pH 6.0. Several factors influence the pH of dry sausage, and the addition of GDL (glucono&lactone) to dry sausages resulted in a significant decrease in pH and in the levels of histamine and putrescine as well as the levels of faecal streptococci, aerobic mesophilic bacteria and coliforms, but did not affect growth of lactic acid bacteria (Maijala et al., 1993). The presence of fermentable carbohydrates such as glucose enhances both growth and amino acid decarboxylase activity in bacteria. Glucose concentrations in the range of OS-2.0% (w/v) have been reported to be optimal, while levels in excess of 3% (w/v> inhibited enzyme formation (Hal&z et al., 1994). Amino acid decarboxylase activity was stronger in an acidic environment, being the optimum pH between 4.0 and

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5.5 (Sinell, 1978; TeodoroviE et al., 1994). Furthermore, in such an environment bacteria are more strongly encouraged to produce these enzymes, as a part of their defence mechanisms against the acidity (BunEiC et al., 1993; Hal&z et al., 1994; TeodoroviC et al., 1994). With respect to the influence of temperature on the synthesis of biogenic amines there are differing reports. Storage temperature may affect the content of biogenic amines in food. However, Santos et al., 1986a found that storage temperature did not significantly influence maximum tyramine content in anchovies, though refrigeration temperatures delayed the start of the increase. Disagreeing with the above information, Diaz et al., 1992 found that histamine and tyramine concentrations increased with the time and storage temperature of Chihuahua cheese. Putrescine biosynthesis by Enterobacter cloacae was detected at 20C after 24 hours of incubation but not at lOC, and Klebsiella pneumoniae showed less extensive cadaverine production at 10C than at 20C. In foods, histamine production is slowed at 10C and nearly terminated at 5C due to the slow growth of histamine-producing bacteria at low temperatures. No histamine was formed by Pseudomonas morganis, Pseudomonas vulgaris, or Hajizia strains after one month of incubation at 1C (Hal&z et al., 1994). Similarly, Klausen and Lund, 1986 reported that amine contents were temperature- dependent and at 10C were two to 20 times higher than at 2C in both mackerel and herring. Sayem-El-Daher et al., 1984 reported that the levels of putrescine, 1,3-diaminopropane, spermine, spermidine, cadaverine and tyramine were all positively correlated with both storage time and temperature. Ababouch et al., 1991 indicate that low storage temperatures are not sufficient to inhibit the formation of toxic amines such as histamine. Baranowski et al., 1985 detected that Klebsiella pneumoniae UH-2 produces large amounts of histamine at 10, 25 and 37C. No growth occurred at 2C but histamine was found because the resting cells were capable of producing histamine during storage at low temperature. During the storage of pork meat, putrescine and cadaverine contents increased during storage at 5C and at - 2OC, while spermidine and spermine decreased in the same conditions (Hal&z et al., 1994). Sayem-El-Daher et al., 1984 reported that histamine levels were apparently unaffected by storage conditions (4, 7 and 10C during 12 days in raw and cooked ground beef). Amine concentrations were also unaffected by cooking, with the exception of spermine, which decreased during heat treatment of cooked ground beef at 200C for 2 h. Luten et al., 1992 and Wendakoon and Sakaguchi, 1993 also indicate that histamine is thermally stable during the cooking process. Once these amines are formed, it is difficult to destroy them. Nevertheless, the original concentration of amines in food can change as a result of storage conditions and these should be controlled. Histamine formation was inhibited by salting and hardly any was formed, regardless of brine concentration, during storage of mackerel muscle at 5C. During storage at 25C, the inhibition effect of histamine was proportional to the increase in brine concentration. When glucose and sucrose were added to mackerel muscle it was detected more histamine formation than in ground muscle. Glycine (10% w/v>, sorbic acid (O. l-0.2% w/v) and 10% (w/v) of citric, malic and succinic acids have a diminishing effect on its synthesis (Kang and Park, 1984a, Kang and Park, 1984b). Histamine levels

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recorded in the presence of 3.50% (w/v> salt or 0.02% (w/v> sodium nitrite were very similar to those found in the additive-free control broth (Teodorovic et al., 1994). Nevertheless, histamine, tyramine and tryptamine synthesis by Streptococcus cremoris has been reported to be suppressed considerably by the addition of 0.5% (w/v> of NaCl to the base medium (Babu et al., 1986). Yatsunami and Echigo, 1993 found that with 2% NaCl (w/w) added to Sardinops melasnosticta during storage at 30C histamine and cadaverine increased rapidly, and with 12% NaCl (w/w> at 30C histamine, putrescine and cadaverine were formed. Thus it is suggested that Staphylococcus spp., Vibrio spp. and Pseudomonas spp. produce non-volatile amines in sardine meat with 12% NaCl (w/w>. In order to avoid the N-nitrosoamines formation by the secondary amines, seal meat was washed with 0.5% (w/v> of sodium bicarbonate solution and it was found to be the most effective way of removing ethanolamine, spermine and spermidine (Shahidi et al., 1993). Oxygen supply also appears to have a significant effect on the biosynthesis of amines. Enterobacter cloacae produces about half the quantity of putrescine in anaerobic compared with aerobic conditions, and Klebsiella pneumoniae synthesizes significantly less cadaverine but acquires the ability to produce putrescine under anaerobic conditions (Hal&z et al., 1994). On the other hand, it has been reported that reducing the redox potential of the medium also stimulates histamine production, and histidine decarboxylase activity seems to be inactivated or destroyed in the presence of oxygen activity of (Arnold and Brown, 1978; Hal&z et al., 1994). Histidine decarboxylase Proteus morganii is inhibited in atmospheres of 80% CO2 (Watts and Brown, 1982; Vidal and Marine, 1984). Modified atmosphere packaging gives only slight inhibition of histamine-forming bacteria in big-eye tuna and the histamine formation was not attributable to the histamine-producing bacteria studied: Morganella morganii (Proteus morganii), Klebsiella pneumoniae and Hufnia alcei (Oka et al., 1993). Repression of histidine-decarboxylase has also been detected when the amount of histamine is accumulated in the medium (Omure et al., 1978; Vidal and Marine, 1984). The presence of histamine had an inhibiting effect on the histidine decarboxylation activity of Photobacterium histaminum C-8; histamine, agmatine and putrescine inhibited the histidine decarboxylation activity of Ph. phosphoreum N-14 (Kurihara et al., 1993). A better understanding of the mechanisms by which biogenic amines are being produced is necessary to prevent their formation. Generally, biogenic amines in food can be controlled by strict use of good hygiene in both raw material and manufacturing environments with corresponding inhibition of spoiling microorganisms. In fermented food, the use of short fermentations with carefully selected active starter cultures instead of wild fermentations will help to prevent the formation of toxic amines.

5. Function

and physiological

significance

In addition to their biological role as sources of nitrogen and precursors for the synthesis of hormones, alkaloids, nucleic acids and proteins, amines are also important food aroma components and potential precursors for the formation of carcinogenic N-nitroso compounds (Pfundstein et al., 1991; Shahidi et al., 1994).

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Polyamines (putrescine, spermidine and spermine) are indispensable components of all living cells. Although they have long been known to be essential for growth, their exact biological role in cell metabolism is still unclear. Due to the diversity of their roles in cellular metabolism and growth, they are required in rapidly growing tissues in large amounts (Bard&z, 1989). All cells have the capacity to synthesize polyamines, which may also be derived from external sources, of which the diet appears to be the most likely. Polyamines are essential for maintaining the high metabolic activity of the normally functioning and immunological system of gut. Spermine and spermidine have also been implicated in the evolution of intestinal tissue (Romain et al., 1992; Bard&z et al., 1993). Although every cell has some ability to synthesize polyamines, it appears &hat the body also relies on a continuous supply of polyamines from food, most of which are not retained by the gut tissues but distributed to different organs in the body. It is likely that there is a body storage pool for polyamines from which they are released in a controlled way when needed (Bard&z et al., 1993). Certain classes of amines, the catecholamines, indolamines and histamine, fulfil important metabolic functions in humans, especially in the nervous system and the control of blood pressure (Hal&z et al., 1994). Phenylethylamine and tyramine cause a rise in blood pressure; by contrast, histamine reduces blood pressure. Histamine possesses a powerful biological function, serving as a primary mediator of the immediate symptons noted in allergic responses (Taylor, 1986; Stratton et al., 1991). Putrescine, cadaverine and agmatine have been identified as potentiators that increase the toxicity of histamine to humans by depressing histamine oxidation (Ibe et al., 1991b). The rapidity of the reaction, in some cases within 5 min., suggests that absorption of at least part of the amine may take place through the oral mucous membrane, bypassing the intestinal aminooxidases (Hal&z et al., 1994). Furthermore, determination of the biogenic amines histamine, tyramine, agmatine, putrescine, cadaverine, spermine and spermidine is important not only from the point of view of their toxicity but also because they can be used as indicators of the degree of freshness or spoilage of food (Hal&z et al., 1994). A fishy odour is derived from a variety of components, of which trimethylamine (TMA) is predominant. Biogenic amines such as putrescine, cadaverine, spermidine, etc. have been reported to be radical scavengers (Yen and Kao, 1993). Lovaas, 1991 has demonstrated that polyamines, spermine, spermidine and putrescine inhibit the oxidation of polyunsaturated fatty acids, and this antioxidative effect is correlated with the number of amine groups in the polyamine. Yen and Kao, 1993 demonstrated that tyramine has a markedly antioxidative activity which increases with tyramine concentration, and they conclude that this antioxidative effect may be attributed to its amine and hydroxy groups. Nitrosable secondary amines (agmatine, spermine, spermidine) can form nitrosamines by reaction with nitrite and produce carcinogenic compounds (Smith, 1981; Hal&z et al., 1994). In general, N-nitroso compounds can be formed by the interaction of amino compunds with nitrosating reagents such as nitrite and nitrogen oxides during the storage, conservation and cooking of foods (Hotchkiss, 1987). The reaction of nitrosating agents with primary amines produces short-lived alkylating species that react with other components in the food matrix to generate products (mainly alcohols) devoid of

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toxic activity in the relevant concentrations (Ahmad et al., 1987). The nitrosation of secondary amines leads to the formation of stable N-nitroso compounds, while that of tertiary amines produces a range of labile N-nitroso products (Pfundstein et al., 1991). It has been difficult to evaluate the endogenous formation of N-nitroso compounds from ingested dietary amines and nitrosating agents because of the lack of adequate data on exogenous exposure to amines (Pfundstein et al., 1991).

6. Toxicology Although biogenic amines such as histamine, tyramine and putrescine are needed for many critical functions in man and animals, consumption of food containing high amounts may have toxicological effects. The most notorious foodborne intoxications caused by biogenic amines are related to histamine. Several outbreaks of histamine poisoning have occurred after eating cheese or fish. On the other hand, it must be taken into account that secondary amines such as putrescine and cadaverine can react with nitrite to form heterocyclic carcinogenic nitrosamines, nitrosopyrrolidine and nitrosopiperidine (Huis int Veld et al., 1990). Histamine exerts its toxic effects by interacting with two types of receptors (H, and Hz) on cellular membranes of humans and other species. Histamine causes dilatation of peripheral blood vessels, capillaries and arteries, thus resulting in hypotension, flushing, and headache (Stratton et al., 199 1). Histamine-induced contraction of intestinal smooth muscle, mediated by H, receptors, may account for abdominal cramps, diarrhoea and vomiting (Taylor, 1986). Gastric acid secretion is regulated by histamine through HZ receptors located on the parietal cells (Sol1 and Wollin, 19771, but it is unknown whether this action accounts for some of the symptoms observed in cases of histamine poisoning (Taylor, 1986). Histamine is the most toxic amine detected in foods, i.e. fish, cheese, wine and meat products (Brink et al., 1990; Huis int Veld et al., 1990). The toxicological effect depends on histamine intake concentration, presence of other different amines, aminooxidase activity and the intestinal physiology of the individual. Clifford et al., 1989, Clifford et al., 1991a, Clifford et al., 1991b and Ijomah et al., 1989, Ijomah et al., 1991 a, Ijomah et al., 1991b have concluded that the role of dietary histamine, as opposed to endogenous histamine is slight, and there is no compelling evidence for the potentiation of dietary histamine by other dietary amines. Non-protein nitrogen compounds such as amines and peptides contribute to the flavour and taste of food (Maga, 1978). The characteristic red colour of cured meat develops after the addition of nitrite to raw meat. Concern over the use of nitrite due to its possible reactions with amines and amino acids present in meat has been the subject of many investigations (Hotchkiss, 1987, Hotchkiss, 1989; Pfundstein et al., 199 1; Shahidi et al., 1992, Shahidi et al., 1993). A fairly efficient detoxification system exists in the intestinal tract of mammals, which is capable of metabolizing normal dietary intakes of biogenic amines (Huis int Veld et al., 1990). Under normal conditions in humans exogenous amines absorbed from food are rapidly detoxified by the action of amine oxidases or by conjugation, but in the case of allergenic individuals or if monoamine oxidase inhibitors are applied or when

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too high levels are consumed the detoxification process is disturbed and biogenic amines accumulate in the body. Amino oxidases are inducible enzymes in the presence of mono- or diamines (Wendakoon and Sakaguchi, 1993). The enzymes monoamine oxidase (MAO) and diamine oxidase (DAO) play an important role in this detoxification process. However, when the activity is suppressed by one or more substances known as potentiators the detoxification is inhibited, and their presence may explain why spoiled fish or aged cheese are more toxic than histamine in aqueous solution. Potentiators can be classified as either foodbome putrefactive amines or pharmacological agents (Stratton et al., 1991). Certain drugs have been implicated as contributing factors in cases of histamine poisoning. Also, certain antihistamines, antimalaria agents, and other medications can inhibit histamine-metabolizing enzymes (Brink et al., 1990; Stratton et al., 1991). Some amines, specifically putrescine and cadaverine, inhibit histamine-detoxifying enzymes. Other amines that may act as potentiators include tyramine (which can inhibit MAO) and tryptamine (which inhibits DAO). Phenylethylamine is a DA0 and HMT (histamine N-methyltransferase) inhibitor (Stratton et al., 1991). Some types of microorganisms, e.g. lactococci, Aspergillus niger and Trichosporon spp., contain monoamine and diamine oxidase (Yamada et al., 1967; Voigt and Eitenmiller, 1978; Silla, 1985). Some types of yeasts found in Roquefort cheese are capable of assimilating cadaverine, putrescine and histamine (Besanqon et al., 1992). The toxicological level of amines is very difficult to establish because it depends on individual characteristics and the presence of other amines. A legal upper limit of 100 mg histamine/Kg food and 2 mg/l alcoholic beverage have been suggested. Values of 100-800 mg/Kg for tyramine and 30 mg/Kg for phenylethylamine have been reported as toxic doses in foods (Brink et al., 1990; Hal&z et al., 1994). The levels reported for histamine and its potentiators in food would not be expected to pose any problem if normal amounts were consumed. Sandler et al., 1974 reported that 3 mg of phenylethylamine causes migraine headaches in susceptible individuals, while 6 mg total tyramine intake was reported to be a dangerous dose for patients receiving monoamine oxidase inhibitors (Shalaby, 1993). The level of 1000 mg/Kg (amine/food) is considered dangerous for health. This level is calculated on the basis of foodbome histamine intoxications related to amine concentration in food (Taylor, 1985). The discrepancy in the toxic histamine level in food might be due to the absence or presence of other synergistic biogenic amines like putrescine and cadaverine. The European Community has recently proposed that the average content of histamine should not exceed lo-20 mg/lOO g of fish (Luten et al., 1992).

7. Analytical

methods

The AOAC procedure is the official method for analyzing histamine in foods in the USA (Williams, 1984; Stratton et al., 1991). According to this procedure, the food sample is homogenized with methanol, filtered, and then applied to an anion exchange column prior to derivatization with o-phthalaldehyde (OPT). The fluorescence of the resulting compound is then measured. Diverse techniques based on fluorescence have

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been reported for detecting histamine in fish (Williams, 1984; Taylor, 1985; Stratton et al., 1991). In addition to these methods, numerous chromatographic methods utilizing thin layer chromatography (TLC), high performance liquid chromatography (HPLC) and gas chromatography (GC) techniques have been developed (Lyons et al., 1983; Taylor and Sumner, 1986; Feier and Goetsch, 1993) and liquid chromatography (LC) (Ibe et al., 199la, Ibe et al., 199lb). Few reports have been published on me simultaneous detection of multiple amines. Gradient HPLC with pre- or post-column derivation is a reproducible and accurate method for the determination of histamine, putrescine, cadaverine and tyramine in fish (Luten et al., 1992). Continuous flow analysis and isocratic HPLC with precolumn derivation is suitable for the analysis of histamine alone. Good repeatability and reproducibility have been reported by Feier and Goetsch, 1993 with extraction into trichloroacetic acid clean-up by cation exchange and HPLC separation using UV and fluorescence separation for determining putrescine, cadaverine, histamine and tyramine in fish and fish products. A convenient method is described by Lehtonen et al., 1992 and Straub et al., 1993 for the analysis of biogenic amines by means of reversed-phase HPLC. The method is characterized by multi-channel UV detection (diode-array), subsequent post-column derivation with o-phthaldialdehyde and 3-mercaptopropionic acid, and fluorescence detection. The simplest method for determination of biogenic amines in foods is by chromatography in an amino acid analyser, including the ion-exchange chromatographic method (Simon-Sarkadi and Holzapfel, 1994). Yamani and Untermann, 1985 have described a liquid medium capable of detecting histidine-decarboxylase activity in pure bacterial cultures within 24 h. Another method with good results is based on automated conductance measurements in a histidine-containing medium incubated at 25C (Klausen and Huss, 1987). The histamine can be extracted and measured fluorometrically or by a method utilizing diamine oxidase and leucocrystal violet which is applied directly to the growth media (Sumner and Taylor, 1989). De Man, Rogosa and Sharpe (MRS) medium containing melicitose (instead of glucose), bromocresol purple and acid-base indicator has been used to differentiate the histamine-producer Lacrobacillus buchneri (Sumner et al., 1990). Enzymatic methods including radioimmunoassays and enzyme-linked immunosorbent assay system (ELISA) have been applied to detect histamine (Guesdon et al., 1986; Stratton et al., 1991), with the advantages of rapidity and not requiring expensive instrumentation like HPLC (Stratton et al., 1991). A major research and knowledge of the microorganisms and conditions which lead to biogenic amines formation in food will be helpful in order to prevent food poisoning caused by the intake of biogenic amines. Acknowledgements The author is grateful to the C.1.C.Y T. (Commission of Scientific Research and Technology) of the Ministry of Education and Science for the financial support given to research project number ALI94- 143 1-E.

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References
Ababouch, L., Afilal, M.E. and Benabdeljelil, H. (1991) Quantitative changes in bacteria, amino acids and biogenic amines in sardine (Sardina pilchardus) stored at ambient temperature (25-28(Z) and in ice. bit. J. Food Sci. Technol. 26, 297-306. Aemy, J. (1982) Lhistamine. Presence dans les den&es alimentaires et dans le vin en particulier. Rev. Suisse Vitic. Arboric. Hortic. 14, 7-13. Ahmad, M.U., Libbey, L.M. and Scanlan, R.A. (1987) Identification of minor nitrosation products of the alkaloid gramine by mass spectrometry. Food Chem. Toxicol. 25, 867-870. Arnold, S.H. and Brown, W.D. (1978) Histamine toxicity from fish products. In: CO. Chichester, E.M. Mark and G.F. Stewart (Eds.), Advances Food Research. Vol 24, Academic Press, New York, pp. 113-154. Askar, A. and Treptow, H. (1986) Biogene amine in Lebensmitteln. Vorkommen, Bedeutung und Bestimmung, Eugen Ulmer GmbH and Co, Stuttgart, Germany. Ayensa Aguirre, M.G. (1993) Estudio de la evoluci6n de1 proceso de anchoado de sardina (Sardina pilchardus, Wulb) Aliment. 248, 71-85. Babu, S., Chander, H., Batish, V.K. and Bhatia, K.L. (1986) Factors affecting amine production in Sfreprococcus cremoris. Food Microbial. 3, 359-362. Baranowski, J.D., Brust, P.A. and Frank, H.A. (1985) Growth of Klebsiellu pneumoniae UH-2 and properties of its histidine decarboxylase system in resting cells, J. Food B&hem. 9, 349-360. Bard&, S. (1989) Polyamines in tissue regeneration. In: U. Barhrach and Y.M. Heimer (Eds.), Physiology of Polyamines. Vol. 1, C.R.C. Press, Boca Raton, FL, U.S.A, pp. 96-106. Bard&z, S., Grant, G., Brow, D.S., Ralph, A. and Pusztai, A. (1993) Polyamines in food - implications for growth and health. J. Nutr. B&hem. 4, 66-7 1. Barwell, C.J. (1994) Pharmacologically-active amines in some marine algae and algal food products. J. Home Consum. Hart. 1, 72-82. Besan$on, X., Smet, C., Chabalier, C., Rinemale, M., Reverbel., J.P., Ratomehenina, R. and Galzy, P. (1992) Study of surface yeast flora of Roquefort cheese. Int. J. Food Microbial. 17, 9- 18. Beutling, D. von, (1993) Studies on the formation of tyramine by microbes with food hygienic relevance. Arch. Lebensmittelhyg. 44, 83-87. Blackwell, B.A. and Mabbitt, L.A. (1965) Tyramine in cheese related to hypertensive crisis after monoamine oxidase inhibition. Lancet 2, 938-940. Bravo, F., Burdaspal, P., Suhez, J.A. and Iiiigo, B. (1983) Histaminogenesis en vines. III. Fermentaciones de mosto de uva por asociaciones binarias levadura-bacteria, Aliment. 148, 31-34. Brink, B. ten, Damink, C., Joosten H.M.L.J. and Huis int Veld, J.H.J. (1990) Occurrence and formation of biologically active amines in foods. Int. J. Food Microbial. 11, 73-84. Bryan, F.L. (1987) Seafood-transmitted infections and intoxications in recent years. In: D.E. Kramer and J. Liston (Eds.), Seafood Quality Determination, Dev. Food Sci., ns 15, Elsevier Publishers, Amsterdam, pp. 319-337. Bun%, S., PaunoviC, Lj., TeodoroviC, V., RadiSiC, D., VojinoviC, G., SmiljaniC, D. and Baltic, M. (1993) Effects of gluconodeltalactone and Lacrobacillus pluntarum on the production of histamine and tyramine in fermented sausages. Int. Food Microbial. 17, 303-309. Buteau, C., Duitschaever, C.L. and Ashton, G.C. (1984) A study of the biogenesis of amines in a Villard noir wine. Am. J. Enol. Vitic. 35, 228-236. Butturini, A., Aloisi, P., Tagliazucchi, R. and Cantoni, C. (1995) Production of biogenic amines by enterobacteria and lactic acid bacteria isolated from meat products. Ind. Aliment. 34, 105-107. Cantoni, C. (1995) Amines in Italian meat products, Ind. Aliment. 34, 9-12. Celano, G.V., Cafarchia, C., Buja, F. and Tiecco, G. (1992) Ricerca di amine biogene in alcuni formaggi. Ind. Aliment. 3 1, 764-768. Chin, K.D.H. and Koehler, P.E. (1986) Effect of salt concentration and incubation temperature on formation of histamine, phenethylamine, tryptamine and tyramine during miso fermentation. J. Food Prot. 49, 423-427. Clifford, M.N., Walker, R., Ijomah, P., Wright, J., Murray, C.K. and Hardy, R. (1991a) Is there a role for amines other than histamine in the aetiology of scombrotoxicosis? Food Addit. Contam. 8, 641-652. Clifford, M.N., Walker, R., Wright, J., Hardy, R. and Murray, C.K. (1989) Studies with volunteers on the role of histamine in suspected scombrotoxicosis. J. Sci. Food Agric. 47, 365-375.

M.H. Silla Sanros/Int

J. Food Microbiology 29 (19%) 213-231

227

Clifford, M.N., Walker, R., Wright, J., Ijomah, P., Hardy, R., Murray, C.K. and Rainsford, K.D. (199lb) Evidence of histamine being the causative toxin in scombroid-fish poisoning. N. Engl. J. Med. 325, 515-516. Dawood, A.A., Karkalas, J., Roy, R.N. and Williams, C.S. (19881 The occurrence of non-volatile amines in chilled-stored rainbow trout (Salmo irideus). Food Chem. 27, 33-45. Diaz-Cinco. M.E., Fraijo, Cl., Grajeda, P., Lozano-Taylor, J. and Gonzalez de Mejia, E. (1992) Microbial and chemical analysis of Chihuahua cheese and relationship to histamine. J. Food Sci. 57, 355-356, 365 Dumont. E., De Geeter, H. and Huyghebaert, A. (1992) Presence and formation of biogenic amines in local Belgian beers. Med. Fat. Landbauww. Univ. Gent. 57, 423-427. Feier, U. and Goetsch. P.H. (1993) Inter-laboratory studies on precision characteristics of analytical methods. Determination of biogenic amines in fish and fish products - HPLC method. Arch. Lebensmit. 44. 134-135. Fernander, J. and Mackie, I.M. (1979) Histidine metabolism in mackerel (Scombrer tcombrus). Studies on histidine decarboxylase activity and histamine formation during frozen storage of flesh and liver under sterile and non-sterile conditions. J. Food Technol. 14, 131- 139. Gajewska, R. and Ganowiak, 2. (19921 Histamine and trimethylamine contents as freshness indicators for fish and fish products. Rocz. Panstw. Zakl. Hig. 43, 245-251. Guesdon. J.L., Chenrier, J.C., Mazie, B., David, B. and Avrameas, S. (1986) Monoclonal antihistamine antibody. Preparation, characterization, and application to enzyme immunoassay of histamine. J. Immunol. Methods 87, 69-78. Hal&z, A., Barath. A., Simon-Sarkadi, L. and Holzapfel, W. (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci. Technol. 5, 42-48. Hanna. P., Glover, V. and Sandler, M. (19881 Tyramine in wine and beer. Lancet 1, 879. Hartmann,T. (19671 Biosynthese fhichtiger Amine in Apfeln durch aldehyd-Aminierung. 2. Pfanzenphysiol. 57. 368-375. Hotchkiss, J.H. (1987) A review of current literature on N-nitroso compounds in foods. Adv. Food Res. 31, 53-115. Hotchkiss, J.H. (1989) Preformed N-nitrosocompounds in foods and beverages. Cancer Surv. 8. 295-321. Huis int Veld, J.H.J., Hose, H., Schaafsma, G.J., Silla, H. and Smith, J.E. (19901 Health aspects of food biotechnology. In: P. Zeuthen, J.C. Cheftel, C. Ericksson, T.R. Gormley, P. Link and K. Paulus (Eds.). Processing and Quality of Foods. Vol 2. Food Biotechnology: avenues to healthy and nutritious products, Elsevier Applied Science, London and New York, pp. 2.73-2.97. Ibe. A., Nishima, T. and Kasai, N. (1992a) Bacteriological properties of and amine-production conditions for tyramine- and histamine-producing bacterial strains isolated from soybean paste (miso) starting materials. Japan. J. Toxicol. Environ. Health 38, 403-409. Ibe, A., Nishima, T. and Kasai, N. (1992b) Formation of tyramine and histamine during soybean paste (mine) fermentation. Japan. J. Toxicol. Environ. Health 38, 181-l 87. Ibe, A., Tamura. Y., Kamimura, H., Tab&o, S., Hashimoto, H., Iida, M. and Nishima, T. (1991a) Determination and contents of non-volatile amines in soybean paste and soy sauce. Japan. J. Toxicol. Environ. Health 37, 379-386. Ibe. H., Saito, K., Nakazuto, M.. Kikuchi, Y., Fujinuma, K. and Nishima, T. (199lb) Quantitative determination of amines in wine by liquid chromatography. J. Assoc. Off. Anal. Chem. 74. 695-698. Ijomah, P., Clifford, M.N., Walker, R., Wright, J., Hardy, R. and Murray, C.K. (1989). Tony Research Station: Diamond Jubilee Conference. Aberdeen, August 1989. Conference papers, Further volunteer studies on scombrotoxicosis. Ijomah, P., Clifford, M.N., Walker, R., Wright, J., Hardy, R. and Murray. C.K. (199la) Further volunteer studies on scombrotoxicosis. In: J.R. Burt, R. Hardy and K.J. Whittle (Eds.). Pelagic Fish: The Resource and its Exploitation, Oxford: Fishing News Books Ltd. Pp. 194-199. Ijomah, P., Clifford, M.N., Walker, R., Wright, J., Hardy, R. and Murray, C.K. (199lb) The importance of endogenous histamine relative to dietary histamine in the aetiology of scombrotoxicosis. Food Addit. Contam. 8, 531-542. Ihigo, B., Martin, D., Barneto, R., Quintana, M.A., Garrido, M.P., Burdaspal, P. and Bravo, F. (1986) Histaminogtnesis en quesos. I. Cambios en la microflora y en el contenido en histamina durante la maduracion. Aliment, 177, 33, 35-38.

228

M.H. Silla Santos/Int.

.I. Food Microbiology

29 (1996) 213-231

Kang, J.H. and Park, Y.H. (1984a) Effect of salt, acidulants and sweetenings on histamine formation during processing and storage of mackerel. Bull. Korean Fisher. Sot. 17, 383-390. Kang, J.H. and Park, Y.H. (1984b) Effect of glucose, sucrose and sorbic acid on histamine formation during processing and storage of mackerel. Bull. Korean Fisher. Sot. 17, 485-491. Klausen. N.K. and Huss, H.H. (19871 Rapid method for detection of histamine-producing bacteria. Int. J. Food Microbial. 5, 137-146. Klausen, N.K. and Lund, E. (19861 Formation of biogenic amines in herring and mackerel. Z. Lebensm. Unters. Forsch. 182, 459-463. Kolodziejska, I., Niecikowska, C. and Sikorski, Z.E. (1994) Dimethylamine and formaldehyde in cooked squid (I&x argentinus) muscle extract and mantle. Food Chem. 50, 281-283. Kurihara, K., Wagatuma, Y., Jujii, T. and Okuzumi, M. (1993) Effect of reaction conditions on L-histidine decarboxylation activity of halophilic histamine-forming bacteria. Bull. Jap. Sot. Sci. Fisher. 59, 17451748. Lavanchy, P. and Sieber, R. (19931 Proteolysis in different hard and semihard cheeses. II. Amines. Schweiz. Milchwirtsch. Forsch. 22, 65-68. Lebiedzinska, A., Lamparczyk, H., Ganowiak, Z. and Eller, K.I. (1991) Differences in biogenic amine patterns in fish obtained from commercial sources. Z. Lebensm. Unters. Forsch. 192, 240-243. Lehtonen, P., Saarinen, M., Vesanto, M. and Riekkola, M.L. (1992) Determination of wine amines by HPLC using automated precolumn derivatisation with o-phthalaldehyde and fluorescetree detection. Z. Lebensm. Unters. Forsch. 194, 434-437. Littlewood, J.T.. Gibbs, C., Glover, V., Sandler, M., Davies, P.T.G. and Rose, F. (1988) Red wine as a cause of migraine. Lancet 1, 5588.559. Lovaas, E. (1991) Antioxidative effects of polyamines. J. Am. Oil Chem. Sot. 68, 353-358. Luten, J.B., Bouquet, W., Seuren, L.A.J., Burggraaf, M.M., Riekwel-Booy, G., Durand, P., Etienne, M., Gouyou, J.P., Landrein, A., Ritchie, A., Leclerq, M. and Guinet, R. (1992) Biogenic amines in fishery products: standardization methods within E.C. In: H.H. Huss et al. (Eds.), Quality Assurance in the Fish Industry, Elsevier Science Publishers B.V., Amsterdam, pp. 427-439. Lyons, D.E., Beet-y, J.T., Lyons, S.A. and Taylor, S.L. (1983) Cadaverine and aminoguanidine potentiate the uptake of histamine in vitro in perfused intestinal segments of rats. Appl. Pharmacol. 70, 445-458. Mackie. M. and Fernandez, J. (19771 Histidine metabolism in fish. Urocanic acid in mackerel (Scomber scombrus). J. Sci. Food Agric. 28, 935-940. Maga, J.A. (19781 Amines in foods. Crit. Rev. Food Sci. Nutr. 12, 373-403. Maijala, R.L. and Eerola, S.H. (19931 Contaminant lactic acid bacteria of dry sausages produce histamine and tyramine. Meat Sci. 35, 387-395. Maijala, R.L., Eerola, S.H., Aho, M.A. and Hirn, J.A. (1993) The effect of GDL-induced pH decrease on the formation of biogenic amines in meat. J. Food Prot. 50, 125-129. Marklinder, I. and Liinner, C. (19921 Fermentation properties of intestinal strains of Lactobacillus, of a sour dough and of a yoghurt starter culture in an oat-based nutritive solution. Food Microbial. 9, 197-205. Maxa, E. and Brandes, W. (19931 Biogene Amine in Fruchtsaften. Mitt. Klosterneuburg 43, 101-106. Mayer, K. (19761 Biogenic amines in food. Investigation in wine and sauerkraut. Qua1 Plant Foods Human Nutrit. 16, 17 1- 179. Middlebrooks, B.L., Toom, P.M., Douglas, W.L., Harrison, R.E. and McDowell, S. (1988) Effects of storage time and temperature on the microflora and amine development in Spanish mackerel (Scomberomorus macularus). J. Food Sci. 53, 1024- 1029. Mizutani, T., Kimizuka, A., Ruddle, K. and Ishige, N. (1992) Chemical components of fermented fish products. J. Food Comps. Anal. 5, 152-159. Moret, S., Bortolomeazzi, R., Feruglio. M. and Lercker, G. (1992a) Determination of biogenic amines in Italian Cheeses. Sci. Teen. Latt. Casearia 43, 187-198. Moret, S.. Bortolomeazzi, R. and Lercker, G. (1992b) Improvement of extraction procedure for biogenic amines in foods and their high-performance liquid chromatographic determination, J. Chromat. 591, 175-180. Morii, H.. Cann, D.C., Taylor, L.Y. and Murray, C.K. (1986) Formation of histamine by luminous bacteria isolated from scombroid fish. Bull. Japan Sot. Sci. Fisher. 52, 2135-2141.

M.H. Silla Santos/Int.

J. Food Microbiology

29 ~19961213-231

229

M&i, H., Cann, D.C. and Taylor, L.Y. (1988) Histamine formation by luminous bacteria in mackerel stored at low temperatures. Nippon Suisan Gakkai-Shi, 54, 299-305. Nemeth-Szerdahelyi, E., Freudenreich, P. and Fischer, K. (1993) Studies on biogenic amine contents in pork. Fleischwirtsch. 73, l89- 190. Nout, M.J.R., Ruikes. M.M.W., Bouwmeester, H.M. and Beljaars, P.R. (1993) Effect of processing conditions on the formation of biogenic amines and ethyl carbamate in soybean Tempeh. J. Food Safety 13, 293-303. Oka, S., Fukunaga, K., Ito, H. and Takama, K. (1993) Growth of histamine producing bacteria in fish fillets under modified atmospheres. Bull. Fat. Fisher. Hokkaido Univ. 44, 46-54. Omure, Y., Price. R.J. and Olcott, H.S. (1978) Histamine forming bacteria isolated from spoiled skipjack tuna and jack mackerel. J. Food Sci. 43, 1779-1781. Ough. C.S., Crowell. E.A., Kunkee, R.E., Vilas, M.R. and Lagier, S. (1987) A study of histamine production by various wine bacteria in model solutions and in wine. J. Food Proc. Preserv. 12, 63-70. Pfundstein, B., Tricker, A.R., Theobald, E., Spiegelharder. B. and Preussmann, R. (1991) Mean daily intake of primary and secondary amines from foods and beverages in West Germany in 1989-1990. Fd. Chem. Toxic. 29, 733-739. Pogorzelski. E. (1992) Studies on the formation of histamine in must and wines from elderberry fruit. J. Sci. Agric. 60, 239-244. Ramesh, A. and Venugopalan, V.K. (1986) Densities and characteristics of histamine-forming luminous bacteria of marine fish. Food Microbial. 3, 103-105. Rice. S.L., Eitenmiller, R.R. and Koehler, P.E. (1976) Biologically active amines in food. A review. J. Milk Food Technol. 39, 353-358. Romain, N., Dandrifosse, G., Jensette. F. and Forget, P. (1992) Polyamine concentration in rat milk and food, human milk, and infant formulas, Pediatric Res. 32, 58-63. Sandler, M., Youdin, M.B.H., Hanington, E. (1974) A phenylethylamine oxidizing defect in migraine. Nature 250, 335-336. Santos. C., Jalon, M. and Marine, A. (1985) Contenido de tiramina en alimentoa de origen animal. I. came. derivados carnicos y productos relacionados. Rev. Agroquim. Tecnol. Aliment. 25, 362-368. Santos. C.. Marine, A. and Rivas. J.C. (1986a) Changes of tyramine during storage and spoilage of anchovies. J. Food Sci. 51, 512-513, 515. Santos. C., Peiia. M.J. and Rivas. J.C. (1986b) Changes in tyramine during chorizo-sausage ripening. J. Food Sci. 51. 518-519, 527. Sayem-El-Daher, N.. Simard, R.E. and Fillion, J. (1984) Changes in the amine content of ground beef during storage and processing. Lebensm.-Wiss-Technol. 17. 319-323. Shahidi, F.. Pegg, R.B. and Sen. N.P. (1994) Absence of volatile N-nitrosamines in cooked nitrite-free cured muscle foods. Meat Sci. 37, 327-336. Shahidi. F., Synowiecki, J. and Sen, N. (1992) Color characteristics and absence of N-nitrosamines in nitrite-cured seal meal. J. Agric. Food Chem. 40, 1398-1402. Shahidi, F., Synowiecki. J., Dunajski, E. and Chong, X. (1993) Nonprotein nitrogen compounds in harp seal (Phoca gwenlandica) meat. Food Chem. 46, 407-413. Shahidi. F., Synowiecki, J. and Naczk. M. (1990) Seal meat, A potential source of muscle food: chemical composition, essential amino acids and color characteristics, Can. Inst. Food Sci. Technol. J. 23, 137- 139. Shalaby, A.R. (1993) Survey on biogenic amines in Egyptian foods: sausage. J. Sci. Food Agric. 62, 291-293. Shalaby, A.R. (1994) Separation, identification and estimation of biogenic amines in foods by thin-layer chromatography. Food Chem. 49, 305-310. Silla, M.H. (1985) Utilizaci6n de microorganismos fermentadores en la conservation de alimentos. A.T.A. 25. 176-182. Simon-Sarkadi, L. and Holzapfel, W.H. (1994) Determination of biogenic amines in leafy vegetables by amino acid analyser. Z. Lebensm. Unters. Forsch. 198, 230-233. Sims. G.G., Fam, G. and York, R.K. (1992) Quality indices for canned Skipjack tuna: correlation of sensory attributes with chemical indices. J. Food Sci. 57, I1 12- 1115. Sinell. H.J. (1978) Biogenic Amine als Risikofaktoren in der Fischhygiene. Arch. Lebensmittelhyg. 29, 206-210. Smith, T.A. (198 I) Amines in Food. Food Chem. 6, 169-200.

230

M.H. Silla Santos/lnt.

J. Food Microbiology

29 (1996) 213-231

Soll, A.H. and Wollin, A. (1977) The effects of histamine postglanding E,, and secretin on cyclic AMP in separated canine fundic mucosal cells. Gastroenterology 72, 1166. Stratton, J.E., Hutkins, R.W. and Taylor, S.L. (19911 Biogenic amines in cheese and other fermented foods, A review. J. Food Prot. 54, 460-470. Straub, B.. Schollenberger, M., Kicherer. M., Luckaa, B. and Hammes, W.P. (1993) Extraction and determination of biogenic amines in fermented sausages and other meat products using reversed-phaseHPLC. Z. Lebensm. Unters. Forsch. 197, 230-232. Sumner, S.S., Roche, F. and Taylor, S.L. (1990) Factors controlling histamine production in Swiss cheese inoculated with Lactobaciilus buchneri. J. Dairy Sci. 73, 3050-3058. Sumner, S.S., Speckhard, H.W.. Somers, E.B. and Taylor, S.L. (1985) Isolation of histamine-producing Luctobacillus buchneri from Swiss cheese implicated in a food poisoning outbreak. Appl. Environ. Microbial. 50, 1094-1096. Sumner, S.S. and Taylor, S.L. (1989) Detection method for histamine producing dairy-related bacteria using diamine oxidase and leucocrystal violet. J. Food Prot. 52, 105-108. Taylor, S.L. (1985) Histamine poisoning associated with fish, cheese and other foods. World Health Organization. WPH/FOS/85( 11, I-47. Taylor, S.L. (19861 Histamine food poisoning, toxicology and clinical aspects. Crit. Rev. Toxicol. 17, 9 1- 128. Taylor, S.L., Leatherwood, M. and Lieber, E.R. (1978) Histamine in sauerkraut. J. Food Sci. 43, 1030-1032. Taylor, S.L. and Sumner, S.S. (1986) Determination of histamine, putrescine and cadaverine. In: D.T. Kramer and J. Liston (Eds.1, Seafood Quality Determination, Elsevier Science Publisher, B.V., Amsterdam, pp. 235.245. TeodoroviC, V., BunEiC, S. and Smiljanic, D. (1994) A study of factors influencing histamine production in meat. Fleischwirtsch. 74, 170- 172. Tiecco, G., Tantillo, G., Francioso, E., Paparella, A. and De Natale, G. (19861 Ricerca quali-quantitativa di alcune amine biogene in insaccati nel torso delli stagionatura. Ind. Aliment. 5, 209-213. Tricker, A.R., Pfundstein, B., Theobald. E., Preussmann, R. and Spiegelharder, B. (1991) Mean daily intake of volatile N-nitrosamines from foods and beverages in West Germany in 1989-1990. Food Chem. Toxicol. 29, 729-732. Valeiro Novo, C. and Pilas Perez. A. (1994) Problemas sanitarios asociados al consume de pescados. Aliment. 250, 55-67. Veciana, M.T., Vidal, M.C. and Marine, A. (1989) Histamine and tyramine during storage and spoilage of anchovies Engraulis encrasichohu: relationships with other fish spoilage indicators. J. Food Sci. 55, 1192-l 195. Vidal, M.C., Izquierdo, M.L., Martin, M.C. and Marine, A. (1990) Histamine and tyramine in meat products: relationship with meat spoilage. Food Chem. 37. 239-249. Vidal. M.C. and Marine, A. (1984) Histamina en pescados y derivados. Formation y posible papel coma indicador de1 estado de 10s mismos. Aliment. 15 1, 93-97, 99-102. Vidaud, Z.E., Chaviano, J., Gonzales, E. and Garcia Rocht, M.O. (19871 Tyramine content of some Cuban cheeses. Die Nahrung 31, 221-224. Voigt, M.N. and Eitenmiller, R.R. (1978) Role of histidine and tyrosine decarboxylases and mono and diamine oxidases in amine build-up in cheese. J. Food Prot. 41, I X2- 186. Watts, D.A. and Brown, W.D. (1982) Histamine formation in abusively stored Pacific mackerel: effect of CO? modified atmosphere. J. Food Sci. 47, 1386-1387. Wendakoon, C.N. and Sakaguchi, M. (1992) Effects of spices on growth and biogenic amine formation by bacteria in fish muscle. In: H.H. Huss et al. (Eds.1, Quality Assurance in the Fish Industry, Elsevier Science Publisher B.V., Amsterdam, pp. 306-313. Wendakoon, C.N. and Sakaguchi, M. (1993) Combined effect of sodium chloride and clove on growth and biogenic amine formation of Enterobncter aerogenes in Mackerel muscle extract. J. Food Prot. 56, 410-413. Wheatley. A.M. and Tinton, K.F. (1987) Determination of tyramine in alcoholic and nonalcoholic beers by high performance liquid chromatography with electrochemical detection. J. Food Biochem. 1 I, 133-142. Williams, S. (Ed.) (19841 Official methods of analysis of the Association of Official Analytical Chemists, 141h edn. Association of Official Analytical Chemists. Arlington, VA, p. 341.

M.H. Silla Santos/Int.

.I. Food Microbiolop

29 (19961 213-231

231

Yamada, H., Uwajima, T., Kumagai, H., Watanabe, M. and Ogata, K. (1967) Bacterial monoamine oxidases. Part I. Purification and Crystallization of tyramine oxidase of Sarcina lutea. Agr. Biol. Chem. 31, 890-896. Yamani, M.I. and Untermann, F. (1985) Development of a histidine decarboxylase medium and its application to detect other amino acid decarboxylases. Int. .I. Food Microbial. 2, 273-278. Yankah, V.V., Ohshima, T. and Koizumi, C. (1993) Effects of processing and storage on some chemical characteristics and lipid composition of a Ghanaian fermented fish product. J. Sci. Food Agric. 63. 227-235. Yatsunami, K. and 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. Japan Sot. Sci. Fisher. [Nippon Suisan Gakkai-Shi] 59, 123-127. Yen, G.C. and Kao, H.H. (1993) Antioxidative effect of biogenic amine on the peroxidation of linoleic acid. Biosci. Biotech. Biochem. 57, 115-l 16.