Critical Reviews in Food Science and Nutrition, 44:489499 (2004)

C Taylor and Francis Inc.

Copyright

ISSN: 1040-8398
DOI: 10.1080/10408690490489341

Biogenic Amines in Meat and Meat

Products

DR. CLAUDIA RUIZ-CAPILLAS and FRANCISCO JIMENEZ-COLMENERO

Instituto del fro (CSIC), Jose Antonio Novais 10, Ciudad Universitaria, Madrid, Spain

It has been recognized for some time that biogenic amines occur in a wide range of foods, among them meat and meat
products. Meat is an important component of the diet in developed countries. The presence of these amines in food is of
interest for two reasons: firstly, for toxicological reasons, in the sense that high levels of dietary biogenic amines can be
toxic for certain consumers, and secondly, for their role as possible quality indicators. Based on these two premises, the
present article offers a new analysis on aspects of toxicology and on the use of biogenic amines as a quality control method,
as well as on their presence in meat and meat products. The article focuses particularly on factors affecting the production
of biogenic amines, with reference to various parameters relating to microorganisms, meat raw materials, and processing
conditions. A better understanding of the factors determining their formation (i.e., microorganisms, raw materials used, and
technological processes applied) and their effects could lead to ways of controlling their production, limiting their presence
in the end product, and hence, rendering them less toxic.
Keywords

Biogenic amines, formation factors, meat products, quality index, toxicological aspects

INTRODUCTION
Amines are naturally present in living organisms and, hence,
in foods. Dietary amines are classified in three categories, according to their chemical structure: aromatic amines (histamine,
tyramine, serotonin, -phenylalanine, and tryptamine), aliphatic
diamines (putrescine and cadaverine), and aliphatic polyamines
(agmatine, spermidine, and spermine) (Smith, 1980). They also
have been classified as natural polyamines and biogenic
amines, depending on their synthesis (Bardozc, 1995). Natural
polyamines are formed during de novo polyamine biosynthesis.
They are produced naturally by animal, plant, and microorganism metabolism. This group consists chiefly of spermidine and
spermine along with the putrescine diamine, and also cadaverine
and agmatine in the case of plants and microorganisms. These
compounds play an important role in nucleic acid regulation and
protein synthesis, and possibly in the stabilization of membranes
(Smith, 1980; Bardocz, 1995). Biogenic amines are produced by
decarboxylation of free amino acids (FAAs) mediated by amino
acid decarboxylase enzymes. Amino acid decaboxylation occurs
through removal of the -carboxyl group to give the corresponding amines (Smith, 1980; Halazs et al., 1994; Bardocz, 1995).
This article deals exclusively with biogenic amines. These
compounds have been known for some time and are found
Address correspondence to Claudia Ruiz-Capillas, Department of Meat and
Fish Science and Technology, Instituto del Fro (CSIC), C/ Jose Antonio Novais
10, Ciudad Universitaria, 28040 Madrid, Spain. E-mail: [email protected]

in varying concentrations in a wide range of foods, including

fish, cheese, meat, wine, beer, vegetables, and chocolate (Smith,
1980; ten Brink et al., 1990; Halasz et al., 1994). Biogenic
amines are important for two reasons. Firstly, the intake of foods
containing high concentrations of biogenic amines can present a
health hazard through the direct toxic effect of these compounds
and their interaction with some medicaments (Bardocz, 1995;
Shalaby, 1996). Secondly, they may have a role as indicators of
quality and/or acceptability in some foods (Miet and Karmas,
1977; Hernandez-Jover et al., 1997; Ruiz-Capillas and Moral,
2001). There have been a number of studies along these lines,
particularly in cheese and fish, the two foods associated with
most cases of biogenic amine poisoning (histamine poisoning
and cheese reaction) (Smith, 1980; Taylor, 1985; Stratton et al.,
1991). Nevertheless, biogenic amines are also present, in widelyvarying concentrations, in meat and meat products (Table 1).
Levels tend to be highest in fermented meat derivatives (also
the type most researched), but considerable concentrations also
have been detected in fresh meat and cooked meat products.
Meat is an important component of the diet in developed countries. In the USA and most European countries, it is a major
component of total expenditure on food. It accounts for about
35% of expenditure in Denmark, France, and Belgium; 30% in
Italy, Spain, and Ireland; and 25% in the UK, the Netherlands,
and Greece (Tuley, 1996). The fact that a major component of
diet contains varying concentrations of compounds like biogenic
amines, which, in certain circumstances, can put consumers at
risk of food poisoning, surely merits special consideration. This

489

490
4.7
nd
Nd-1.1
Nd-8
31.8
85.4
9.9
0.5

3
16

nd

5.916.1
Nd-6
Nd-108.3
2.3587.3
1.95128.40
7.1078.10
3.1014.25
7.540.50
<1200
416
15.2
Nd-4.8
Nd
1.40
0.500.70

Pork raw
Pork raw
Beef raw
Minced beef and pork
Raw ground beef at 4 C for 12 days
Cooked ground beef at 4 C for 12 days
Pork storage at 5 C for 15 days
Pork storage at 20 C for 15 days
Leg Lamb storage at 5 C for 5 days
Vacuum packed beef at 1 C for 7 week Beef
Fresh pork (CO2 ) at 1.5 C for 13 weeks
Pork storage in CO2 /air at 2 1 C for 21 days
Vacuum packed sterile beef at 1 C for 8 wks
Vacuum packed beef at 1 C for 7 wks
Fresh vacuum packed beef at 1 C for 120 days
Bacon
Cooked Spanish meat products Morcilla
Hamburger
Bologna sausage
Ripened meat products Chorizo
Ripened meat products Salchichon
Ripened meat products Jamon serrano
Ripened meat products Lomo embuchado
Ripened meat products Sobrasada
Egyptian dry sausages
Dry sausages
Spanish ripened sausage Mini-salami
Spanish ripened sausage Fuet
Mortadella
Cooked ham
Cooked meat products Chopped
Cooked meat products Butifarra catalana

Nd: not detected.

Histamine

Levels of biogenic amines in meat and meat products

Products

Table 1

Nd-3.5
Nd
Nd-39
12.4
25.1

6
60
0.7

286

Nd-8.4
1.535.5
Nd-29
76.5477.8
67.5465.2
0.4569.50
60.5099.25
14.1577.55
9.552.8
3320
312
156.9
Nd-66.0
Nd-11.9
17.60
14.95151.8

Tyramine
13.3
Nd-0.7
Nd
Nd-96
Nd
Nd
43.0
41.2
1.3
54
68
39.6
0.3
90158

Nd-5

1.310.2
Nd-57
3.934.9
2.168.5

5.638.5
<1790
Nd
367
0.67.0
Nd-0.9

Cadaverine
7.8
Nd-0.6
Nd-1.75
Nd-69
74.1
85.4
18.9
11.2
3.3
18
20
6.6
1
22110

Nd-1

0.312.3
Nd-29
31.6361.9
85.9184.5

12102
<1580
42139
64.7
Nd-3.9
Nd-3.9

Putrescine

Nd

49

2.313.5

5.765.1
12.947.4

2.533.2
<1091

10.0
Nd-1.0
nd

Tryptamine

Biogenic amines (mg/kg)

40

Nd

Nd-2.5

Nd-7.7
2.734.7

1.580.7
<148

10.1
Nd-1.4
nd

Phenylalanine
7.0
2.24.1
1.94.2
Nd-5
113.3
189.0
3.1
4.3

3
9
3.2

16

1.65.1
1.54
1.47.9
2.53.9

5.311.7
<114
51010.3
1.98.9
1.73.0

Spermidine
67.1
25.538.6
28.744.6
1439
331.3
382.1
31.2
42.8

25
600
26.5

2049

2.16.1
1536
15.437.8
8.919.4

1.55.2
1948
25
30.6
7.832.2
18.125.4

Spermine

Halasz et al., 1994

Hernandez-Jover et al., 1996a
Hernandez-Jover et al., 1996a
Wortberg and Woller, 1982
Sayen-El-Daher et al., 1984
Sayen-El-Daher et al., 1984
Halasz et al., 1994
Halasz et al., 1994
Edwards et al., 1983
Edwards et al., 1987
Nadon et al., 2001
Ordonez et al., 1991
Edwards et al., 1985
Edwards et al., 1985
Smith et al., 1993
Nakamura et al., 1979
Santos et al., 1985
Durlu-Ozkaya et al., 2001
Wortberg and Woller, 1982
Hernandez-Jover et al., 1997
Hernandez-Jover et al., 1997
Vidal-Carou et al., 1990
Vidal-Carou et al., 1990
Vidal-Carou et al., 1990
Shalaby, 1993
Eerola et al., 1998
Trevino et al., 1997
Bover-Cid et al., 1999
Hernandez-Jover et al., 1996a
Hernandez-Jover et al., 1996a
Vidal-Carou et al., 1990
Vidal-Carou et al., 1990

References

BIOGENIC AMINES IN MEAT

is particularly true for the meat industry, where health-related

incidents have been all too frequent in recent years.
Today, society is increasingly aware of the importance of
diet for health, and hence, any issue relating to food safety has
a considerable impact on consumer behavior and official policy.
At the same time, consumers increasingly prefer high-quality
products that are minimally processed, safe, etc., and the meat
industry is, therefore, looking for emerging technologies that
can achieve this in processing and storage. However, the conditions in which traditional or emerging technologies are applied
affect the characteristics of the products, and such modifications
may produce changes in the formation of different compounds,
some of which may be toxic and/or mutagenic, with implications
for consumer health. There is, therefore, a clear interest in the
study of toxicity and/or mutagenicity of biogenic amines and
the factors determining their formation in the context of food
processing conditions and preservation.
Although there are such studies on biogenic amines in meat
products, these are generally based on fermented products, and
much less work is available in relation to other types of products,
such as boiled food or fresh meat. In most of the available reviews
(Smith, 1980; Halasz et al., 1994; Silla, 1996; Shalaby, 1996),
many of the aspects most closely related to myosystems are
addressed only tangentially in broad analyses, focusing on other
foods more generally associated with biogenic amine poisoning.
As far as we know, no detailed, specific analysis on the formation
of biogenic amines in different types of processed meat has been
done yet, despite their outstanding presence in this kind of food.
What is original about this study is that it is the first such
analysis and should help to gain a better understanding of the
factors entailed in the production of biogenic amines and to indicate possible ways of limiting their presence in the product
and reduce dietary biogenic amines. Given their health implications, the achievement of these aims could be of considerable
benefit to consumers. The aim of this study, then, is to analyze,
on the one hand, toxicological aspects and the use of biogenic
amines as a quality control method in meat and meat products,
and on the other hand, their formation, with particular emphasis
on factors related to microorganisms, raw meat materials, and
processing conditions.

TOXICOLOGICAL ASPECTS OF BIOGENIC AMINES:

IMPORTANCE IN MEAT AND MEAT PRODUCTS
The intake of foods with high concentrations of biogenic
amines can cause migraine, headaches, gastric and intestinal
problems, and pseudo-allergic responses, chiefly brought about
by the toxic action of histamine and tyramine, known respectively as histamine poisoning and cheese reaction (Smith,
1980; Taylor, 1985; Stratton et al., 1991). The most common
symptoms of histamine poisoning are due to the effect on the
cardiovascular system, producing low blood pressure, reddening
of the skin, and headaches, oedemas and rashes typical of allergic reactions (Stratton et al., 1991; Van Gelderem et al., 1992;

491

Bardocz, 1995). Typical symptoms of tyramine poisoning are

migraines, headaches, and increased blood pressure (Joosten,
1987). Tyramine also causes the release of noradrenaline from
the sympathetic nervous system (Bardocz, 1995). Other amines,
such as spermidine or spermine, have also been associated with
the development of food allergy (Lux et al., 1980). In normal
circumstances, the human body is able to rapidly detoxify histamine and tyramine absorbed from foods by acetylation and
oxidation mediated by the enzymes monoamine oxidase (MAO;
EC 1.4.3.4), diamine oxidase (DAO; EC 1.4.3.6), and polyamine
oxidase (PAO; EC 1.5.3.11) (Rice et al., 1976; Bardocz, 1995).
However, if these detoxifying mechanisms are upset, either because of high amine intake or because the individual is allergic or is deficient in aminooxidases due to consumption of
or treatment with oxidase enzymes (e.g., monoamine oxidase
inhibitorMAOI), biogenic amines may build up in the body
and could cause serious toxicological problems (McCabe, 1986;
Halasz et al., 1994). The toxic potential of these dietary amines
is even more alarming if we consider that approximately 20% of
the European population regularly consume MAOI drugs as antidepressants, which inhibit aminooxidase activity (Sattler et al.,
1988; Maijala and Eerola, 1993).
Putrescine and cadaverine, although not considered toxic individually, can enhance the effect of histamine and tyramine
by interacting with the aminooxidases and interfering with the
detoxifying mechanism (Rice et al., 1976; Taylor, 1985; Sattler
et al., 1988). Similarly, other compounds, like alcohol and acetaldehyde, also can augment the toxic potential of biogenic
amines, since they promote the transportation of these through
the intestinal wall.
It is generally very difficult to establish limits of toxicity of
biogenic amines in a given product, because their effect does
not depend on their presence alone (type of amine and levels
present), but is also influenced by other compounds (modulating their effect) and by the specific efficiency of the detoxifying
mechanisms in different individuals. Hence, the toxicity of biogenic amines will depend on factors associated with the food
itself (quantitative and qualitative) and also on factors associated with the consumer (individual susceptibility and state of
health).
There are large gaps in our understanding of the toxicological importance of these compounds and the mechanics of their
toxicity. Various international studies of epidemiological outbreaks (Lipp and Rose, 1997) have failed to establish a clear
dose-effect relationship (Clifford et al., 1989). The role of various substances that enhance the toxicity of biogenic amines
and the existence of synergic effects have been demonstrated
(Leigh et al., 2000), and therefore the determination of the amine
concentrations in each case is not enough to assess their toxic
potential. In recent years, there have been some studies on the
in vitro toxicity and mutagenicity of biogenic amines (Badolo
et al., 1998), in which the effect has been analyzed on the basis
of the cytotoxicity of individual compounds.
The most prevalent biogenic amines in meat and meat products are tyramine, cadaverine, putrescine, and also histamine.


C. RUIZ-CAPILLAS AND F. JIMENEZ-COLMENERO

492

The concentrations of these amines tend to vary depending on

the different products (Table 1). The concentrations of some
of these amines, such as histamine, are usually quantitatively
lower than those found in other foods (e.g., fish) and their toxicological effects, therefore, appear to be severely limited.
However, there are some meat products where this is not
the case. It has been observed that histamine concentrations in
cured products can reach 100 mg/kg or considerably higher, for
example, in dry sausages (Table 1). Given that 100 mg/kg is the
accepted threshold for the appearance of food poisoning symptoms in a normal person with no health problem (ten Brink et al.,
1990; Stratton et al., 1991), such products should be excluded
from the diet of persons also ingesting MAOIs. In an analysis of
biogenic amine concentrations in commercial processed foods,
Vidal-Carou et al. (1990) determined that 63% of salchichon
samples and 64% of chorizo samples (both ripened meat products) contained enough tyramine to poison MAOI consumers;
in this case, it was considered that 6 mg/kg of tyramine would
be toxic if ingested with MAOIs (McCabe, 1986). In normal
persons, 125 mg/kg would be required for tyramine to be toxic.
Similarly, Santos et al. (1985) suggested that an intake of 100 g
of any of a number of meat products (chorizo, salami, lomo embuchado, Spanish meat products, blood sausage, or hamburger)
containing up to 8.4 mg/kg could be toxic in the event of interaction with MAOIs. In the absence of MAOIs, on the other
hand, none of these processed meats would be toxic if ingested
in normal amounts, but always depending on the susceptibility
of the individual.
Apart from the toxic effects described above, biogenic amines
can play a role in other kinds of processes harmful to human
health. Various biogenic amines (spermidine, spermine, tyramine, putrescine, and cadaverine), when subjected to heat, can
give rise to the formation of secondary amines, and in the presence of nitrites, these can generate nitrosamines, chemical agents
considered to possess major carcinogenic properties (Patterson
and Mottram, 1974; Warthesen et al., 1975). This is particularly important in some meat products with high biogenic amine
levels and added nitrates and nitrites (Table 1).
Evidently there are difficulties and limitations in determining true levels of toxicity, but considering the figures produced
Table 2

by various authors and the restrictions that they imply, there is

undoubtedly a large number of meat products containing biogenic amines that present some potential risk. Despite all the
foregoing, there is a general absence of specific legislation setting limits on biogenic amines in meat products; at best, there is
reference to histamine in some foods, but there is no reference
at all to maximum concentrations of other biogenic amines. For
instance, there is European legislation (Directive 91/439/EEC)
that limits permitted histamine levels in fishery products from
the scombrid or cupleoid family to 100200 mg/kg for fresh fish
and up to 400 mg/kg for cured products. Similarly, the Food and
Drug Administration (FDA, 1990) sets the limit of histamine tolerance in fresh fish at 100 mg/kg. Some laboratories have made
more general recommendations; for example, the Netherlands
Institute of Dairy Research (ten Brink et al., 1990) sets a limit of
100 mg/kg on histamine in foods. As noted earlier, some authors
(Smith et al., 1993; Hernandez-Jover et al., 1996a; Eerola et al.,
1996; Eerola et al., 1998; Bover-Cid et al., 2001a) have used
this limit to establish the potential health risk in certain sectors
of society where some products are consumed beyond a given
storage period.

BIOGENIC AMINES AS A QUALITY INDEX

The concentrations of some biogenic amines (tyramine, putrescine, and cadaverine) normally increase during the processing and storage of meat and meat products, whereas others (spermidine and spermine) decrease or remain constant (ten Brink
et al., 1990; Halazs et al., 1994; Bardozc, 1995). There have,
therefore, been attempts to establish a relationship between meat
quality and changes in the content (individual or combined) of
such compounds in different meat derivatives (Table 2). The
usefulness of biogenic amines as a quality index will depend on
the nature of the product; results tend to be more satisfactory in
fresh meat and heat-treated products than in fermented products.
In the latter, they seem to be of very limited use.
Biogenic amines have been used as quality indexes and indicators of unwanted microbial activity in meat and cooked meat
products (Table 2). A combination of putrescine and cadaverine

Index of biogenic amines in meat and meat products

Products

Biogenic amines

References

Fresh beef meat

Bologna sausage
Minced beef and pork
Pork meat at 68 C
Raw and cooked ground beef
Hamburger
Vacuum packed beef at 1 C
Vacuum packed beef at 1 C
Wrapped and unwrapped fresh
meat (pork, beef and rabbit)
Cooked Spanish products
Jamon york, chopped and butifarra
Dry sausages

Putrescine and cadaverine

BAI = putrescine + cadaverine + histamine + tyramine

Slemr, 1981
Wortberg and Woller (1982)

BAI = putrescine + cadaverine + histamine + tyramine

Putrescine tyramine and 1,3 diaminopropane
Tyramine, histamine, putrescine and cadaverine
Putrescine and cadaverine
Tyramine
Putrescine and cadaverine

Hernandez-Jover et al., 1996b

Sayem-El-Daher et al., 1984
Durlu-Ozkaya et al., 2001
Edwards et al., 1985
Edwards et al., 1987
Guerrero-Lejarreta and Chavez-gallardo, 1991

Putrescine and cadaverine

Vidal-Carou et al., 1990

Tyramine, histamine, putrescine and cadaverine

Eerola et al., 199698

BIOGENIC AMINES IN MEAT

has been suggested as an index of acceptability in fresh meat,

because their concentrations increase prior to spoilage and correlate well with the microbial load (Slemr, 1981; Edwards et al.,
1985). Wortberg and Woller (1982) found that a high cadaverine
concentration was clearly indicative of spoilage. These authors
proposed a biogenic amine index (BAI) consisting of the sum
of putrescine, cadaverine, histamine, and tyramine and established 500 mg/kg as the limit for Bologna sausage, minced beef
and pork. Using the same index, Hernandez-Jover et al. (1996b)
suggested the following limits: BAI <5 mg/kg for good quality
fresh meat; between 5 and 20 mg/kg for acceptable meat, but
with initial spoilage signs; between 20 and 50 mg/kg for low
meat quality; finally, >50 mg/kg for spoiled meat.
It generally has proven more difficult to apply similar quality
criteria to fermented products. This is at least partly because
biogenic amine concentrations vary much more widely in fermented products than in fresh meat and cooked meat products
(Table 1), because of the number of different factors involved in
their formation. These factors include the type and degree of contamination of raw materials, which are promoted by structural
breakdown, manufacturing practices, certain processing stages,
and the use of starters. All these factors vary according to the
nature of the product and, in some cases, can mask changes in
the type and concentration of biogenic amines through the different phases of treatment and storage, delaying visible signs of
spoilage and/or off-odor development (Edwards et al., 1983).
The following example illustrates the problem. Not all spoilage
or starter microorganisms can decarboxylate FAAs. Even within
the same species, not all strains develop the same decarboxylating capacity, so that a low biogenic amine concentration does
not always signal good microbiological quality (Santos et al.,
1985, Dainty et al., 1987, Halasz et al., 1994). It is, therefore, no
simple matter to establish a biogenic amine index that reliably
predicts quality for products of this kind (Eerola et al., 1998).

Figure 1

493

FACTORS INFLUENCING THE FORMATION

OF BIOGENIC AMINES
As noted earlier, biogenic amines are produced by enzymatic
decarboxylation of certain free amino acids (Figure 1). Bacterial decarboxylases are not very specific, but their activity varies
according to the bacterial species and strain (Bardocz, 1995).
Thus, biogenic amine formation requires the presence of free
amino acids, the decarboxylase enzyme and suitable environmental conditions. Hence, all the factors bearing on production
of the substrate (FAAs), the enzyme, and also their level of activity, effect the type and amount of biogenic amines present in
each case. Factors associated with the raw material (meat composition, pH, handling conditions, etc.) as the substrate source
and reaction medium directly affect the availability of FAAs,
whereas the presence of the enzyme is closely tied to microbiological aspects (bacterial species and strain, bacterial growth,
etc.). It is also apparent from the literature that diamine oxidase formation by histaminolytic bacteria can influence final
histamine levels (Ienistea, 1971). These factors are obviously
interdependent and are further influenced by the technological
processes associated with types of meat derivative (steak, roast,
ham, ground, restructured, comminuted, fresh, cooked, smoked,
fermented, etc.) and storage conditions (time/temperature, packaging, temperature abuses, etc.). The combined action of these
factors is what chiefly determines final concentrations of biogenic amines, because it either directly or indirectly determines
the presence and the activity of substrate and enzyme (Figure 2).
More knowledge of these factors would, therefore, help to better
understand the mechanics of biogenic amine formation and find
means of keeping them at nontoxic levels.
Following is a specific analysis of the most important factors.
We chose this approach for the sake of clarity of exposition, at
the risk of occasional simplification. Many of these factors are

Formation of biogenic amines.

494

C. RUIZ-CAPILLAS AND F. JIMENEZ-COLMENERO

Figure 2

Factors influencing the formation of biogenic amines.

interrelated and would otherwise have to be addressed in several

sections requiring more complex analyses.

Microorganisms
Bacterial amino acid decarboxylase enzymes play a fundamental role in the formation of biogenic amines, and therefore,
the microorganisms that produce them are an extremely important element (Figure 2). Slemr (1981), and Slemr and Beyermann
(1985) reported that there was no formation of biogenic amines
in sterile meat, and that when concentrations increased in meat,
they did so along with microorganisms. Biogenic amine production is influenced by the microbial load in the product and
the type of microbiot constituting that load (bacterial species and
strain) (Bardocz, 1995). This, in turn, depends on various factors:
characteristics of the meat raw material, use of thermal treatments, use of additives, etc. (Figure 2). Numerous researchers
have sought to establish a relationship between the formation
of biogenic amines in meat and meat products and the activity of various types of microorganisms (Table 3). Eitenmiller
et al. (1978) attributed the formation of biogenic amines in
dry sausages to a bacterial response that maintains cellular viability, when this is threatened by acidity in the medium. In
general, decarboxylase activity in meat products is attributed
chiefly to Enterobacteriaceae, Pseudomonadaceae, Micrococcaceae, and lactic bacteria (Table 3). In fresh meat, Enterobacteriaceae have been identified as the main producers of cadaverine
(Edwards et al., 1983; Guerrero-Lejarreta and Chavez-Gallardo,
1991; Ordonez et al., 1991, Bover-Cid et al., 2001a), while

putrescine has been associated with high total aerobic viable

counts (TAVCs) (Edwards et al., 1983, Bauer et al., 1996).
Lactic bacteria appear to be the main producers of biogenic
amines in fermented products; high Lactobacillus counts have
been associated with the formation of high histamine concentrations. However, amine formation seems to be a characteristic only of some Lactobacillus strains, as other strains do not
produce them (Maijala and Eerola, 1993; Straub et al., 1994;
Roig-Sagues and Eerola, 1997). Differences in concentrations
and types of lactic bacteria could help to explain the high variation of biogenic amine concentrations found in products of
this kind (Table 1). Masson et al. (1996) found that tyramineproducing strains in dry sausage belonged to Carnobacterium,
L. curvatus and L. plantarum, whereas Micrococcaceae and
L. sake did not produce tyramine. It has been suggested that
the use of amino-negative starters comprised of L. sakei or
Pediococus pentosaceus could prevent the formation of biogenic amines in dry sausage (Maija et al., 1995; Bover-Cid
et al., 2001b), although any reduction would always depend on
other factors influencing formation, especially the raw material
(Figure 2).

Meat Raw Materials

Meat raw material is the natural source of the substrate (FAAs)
from which biogenic amines are produced. It also is the largest
component of the matrix in which the decarboxylation reactions take place and is, therefore, basic in determining essential factors in enzymatic activity: pH, ionic strength, substrate

495

BIOGENIC AMINES IN MEAT

Table 3

Production of biogenic amines by microorganisms in meat and meat products

Products

Microorganisms

Biogenic amines

References

Fresh meat
Fresh beef
Raw Pork

Pseudomonads

Putrescine

Carnobacterium
Lactobacillus curvatus
Lactobacillus plantarum
Enterobacter cloacae
Klebsiella pneumoniae
Enterobacteriaceae
Total aerobic viable counts (TAVC)
Enterobacteriaceae
Pseudomonads
Enterobacteriaceae

Tyramine

Bauer et al., 1996

Edwards et al., 1987
Masson et al., 1996

Raw pork at 5 C
Beef, pork lamb at 5 C
Wrapped and unwrapped fresh
meat (pork, beef and rabbit)
Ground meat and processed meat
Vacuum packed beef at 1 C
Vacuum packed beef at 1 C
Pork stored in CO2/air at 2 C

Dry products (sausages)

Dry sausage

Ripened sausages
Fermented sausages

Lactobacillus divergens
Lactobacillus carnis
Hafnia alvey
Serratia liquefaciens
Brochothrix thermosphacta
Lactobacilli
Enterobacteriaceae
Lactobacilli
Carnobacterium
Lactobacillus carvatus
Lactobacillus plantarum
Enterococci
Lactic acid bacteria (LAB)
LAB
Enterobacteriaceae

concentration, inhibitors, and their mobility, etc. Therefore, any

conditions that alter its nature and characteristics will influence the formation of biogenic amines in one way or another
(Figure 2).
Some biogenic amines (e.g., putrescine and cadaverine) also
are formed and broken down during normal cell metabolism
(Bardocz, 1995) and are, therefore, naturally present in muscle
and meat. However, when an amine exceeds these natural concentrations, it clearly must have some other origin. Thus, the
amount of biogenic amines in the meat raw material will contribute to the pool of biogenic amines in the end products. It is
vital to achieve guaranteed use of suitable raw materials in order
to limit the presence of amines in the end product and, hence,
assure better quality.
Free amino acids play a fundamental role in the formation
of amines in meat, in that they are their precursors and, moreover, constitute a substrate for microbial growth (Smith 1980;
Arnold and Brown, 1978). Concentrations increase in association with proteolytic events taking place in the course of treatment and storage, due essentially to many of the microorganisms
present. However, in meat such as fish, it has not been possible
to establish a clear relationship between FAA concentrations
and formation of the corresponding biogenic amines (Eerola
et al., 1996; Ruiz-Capillas and Moral, 2001). Various studies
have shown that fat content influences the formation of biogenic
amines (Hernandez-Jover et al., 1997; Kebary et al., 1999). This
phenomenon has been most intensively studied in cheese, where

Putrescine
Cadaverine
Cadaverine
Putrescine
Cadaverine
Putrescine
Putrescine, tyramine,
Histamine
Tyramine

Halasz et al., 1994

Cadaverine
Putrescine
Cadaverine
Putrescine

Dainty et al., 1986

Histamine
Tyramine

Maijala and Eerola, 1993

Masson et al., 1996

Tyramine

Roig-Sagues et al., 1997

Tyramine
Cadaverine

Bover-Cid et al., 2001a

Edwards et al., 1983

Guerrerolejarreta and Chavez-Gallardo, 1991
Durlu-Ozkaya et al., 2001
Edwards et al., 1987

Ordonez et al., 1991

it has been observed that the concentration of biogenic amines

decreases along with fat content. Banwart (1981) attributes this
fact to changes in the water activity (Aw) rather than the actual
amine content; Aw causes some inhibition of growth of proteolytic bacteria and, hence, a fall in the concentration of free
amino acids in the medium.
It has been noted that the meat source can influence the formation of biogenic amines. Some authors (Wortberg and Woller,
1982; Vidal-Carou et al., 1990) have reported that histamine and
tyramine formation tends to be found less in packed meats made
only with pork (e.g., cooked ham and cured ham) than in other
meat derivatives containing mixtures of beef and pork (salami,
salchichon, chorizo or Bologna sausages), where there was a
greater tendency to form tyramine.
The conditions in the reaction medium are a key factor in
enzymatic activity, quite apart from their effect on the actual
production of the enzyme through their impact on microbial
growth. Histidin decarboxylase activity increased in acid media,
with an optimum pH range of 4 to 5.5 (Arnold and Brown,
1978; Halazs et al., 1994). The final pH of the meat, which
can vary depending on a variety of factors, could, therefore,
have a considerable influence. High pHs, for instance in DFD
(dark, firm and dry) meat, favor microbial proliferation, which
promotes FAAs, but limits decarboxylase activity. The opposite
is true of PSE (pale, soft, exudative) meat. We are not aware
of any studies on the influence of meat type (DFD, PSE) on
biogenic amine formation, but such an influence cannot be ruled

496

C. RUIZ-CAPILLAS AND F. JIMENEZ-COLMENERO

out, given that the meat type affects factors directly involved
in the activity of amino descarboxylases enzymes and the final
presence of biogenic amines in these meat.

Meat Processing
Meat processing and storage conditions influence the formation of biogenic amines, because they affect some of the elements
implicated in biogenic amine production (Figure 2). We know
that any processing step, directly or indirectly, affects the concentration of substrate and enzyme and determines the presence
of other compounds or conditions that modulate decarboxylase
activity; therefore, there are many factors to be considered, especially in connection with the technology applied (fresh, cooking,
curing, fermenting, etc.). Thus, to limit the formation of biogenic
amines, it is not enough to have suitable raw materials; it also is
necessary to optimize the processing conditions.
The production of biogenic amines is affected by the conditions in which meat raw materials are handled. For example, after
the decontamination of beef carcasses (washing with chlorine
and lactic acid), followed by vacuum packing of cuts, of all the
amines monitored (histamine, phenylethylamine, tryptamine,
and tyramine), only tyramine was consistently detected over
120 d storage at 1 C (Smith et al., 1993). Any process entailing structural breakdown (grinding, chopping, sectioning, slicing, etc.) favors microbial contamination. Santos et al. (1985)
attributed tyramine formation in hamburgers to increased contamination, as a result of grinding.
Chilling storage conditions considerably affect amine production. Unsuitable storage temperatures (i.e., temperatures
>5 C), prolonged storage, or temperature abuses during storage
have a two-fold effect: on proteolysis due to increased microbial
growth promoting penetration in the muscle; on amino decarboxylase activity (Maijala and Nurmi, 1995). There have been
numerous studies on the formation of biogenic amines in the
course of fresh meat storage, frequently with conflicting results.
Nakamura et al. (1979) detected no changes in biogenic amine
concentrations (<100 g/kg) in pork stored at 4 C for 16 d, even
after rejection for the onset of decomposition; however, other
authors (Wortberg and Woller, 1982; Edwards et al., 1983) reported increased concentrations, especially of cadaverine, which
is possibly associated with the onset of spoilage. Halasz et al.
(1994) reported increased putrescine and cadaverine concentrations in pork meat over 15 d storage at 5 C. Sayem El Daher et al.
(1984) found that putrescine, spermidine, spermine, cadaverine,
and tyramine concentrations correlated with both time (12 d)
and temperature (4, 7, and 10 C) of storage, while histamine
concentration was apparently unaffected by storage conditions.
In addition to storage temperature and time, biogenic amine
production is dependent on packaging conditions (vacuum or
modified atmosphere), which decisively influence microbial
flora (Wortberg and Woller, 1982; Dainty et al., 1986; Edwards
et al., 1987). Vacuum or modified atmosphere packaging, commonly used to prolong the shelf life of these kinds of products,

entails altering O2 levels and, hence, the growth and selection

of some microorganism strains that can affect the production of
biogenic amines. For example, Enterobacter cloacae produces
half the amount of putrescine in an aerobic atmosphere and Klebsiella pneumoniae synthesizes significantly less cadaverine and
produces more putrescine in anaerobic conditions (Halasz et al.,
1994). Nadon et al. (2001) reported that by using CO2 atmospheres it was possible to prolong the shelf life of pork stored at
1.5 C by up to 13 wk, as this limited the formation of biogenic
amines, chiefly during the first 2 wk.
Freezing and frozen storage can cause chemical and structural
changes in meat, depending on species and storage conditions
(temperature, duration, temperature fluctuations, etc.). Most decarboxylases are unstable to freezing; for example, histidine
decarboxylase becomes inactive after 815 d at 20 C (Halasz
et al., 1994; Silla, 1996; Chen et al., 1994). Although dependent on conditions, the effect of freezing and frozen storage
on microbial growth and enzymatic activity does not generally
favor the formation of biogenic amines. The existing concentrations must, therefore, come mainly from the fresh product and
will be strongly influenced by prefreezing treatment and storage
conditions. In this connection, Hernandez-Jover et al. (1996b)
found that the proportion of biogenic amines remained stable in
pork stored for 12 d at 18 C. On the other hand, other authors
(Halasz et al., 1994) have reported an increase of cadaverine
and putrescine and a decrease of histamine, spermidine, and
spermine after 8 d at 20 C.
There are various meat products that are usually prepared
in the meat industry with frozen meat rather than fresh meat.
However, there are few studies that attempt to assess the impact
of frozen meat on the formation of biogenic amines in processed
products. Maijala et al. (1995) reported that the thawing time of
raw materials affected microbial flora and the amounts of free
amino acids available as precursors and, hence, the formation of
biogenic amines. On the other hand, Bover-Cid et al. (2001b)
found that the formation of biogenic amines during ripening of
dry sausage made with thawed pork was dependent on the use of
a starter culture rather than the thawing time of the raw materials.

Processing of Meat Products

The different types of processing and storage conditions that
are applied to meat products can influence the formation of biogenic amines in them. It has generally been found that cooking
processes reduce biogenic amine concentrations to between 4
and 10 times less than in cured and ripened products, mainly due
to the elimination of biogenic amines in cooking loss (Lakritz
et al., 1975). Given that cooking does not favor amine formation,
its presence in cooked meat products (Table 1) would appear to
be closely linked to the quality of the meat raw material used;
high concentrations of biogenic amines indicate low quality
meat containing high concentrations of these compounds at origin (Paulsen et al., 1997; Bover-Cid et al., 2001b). Another
factor to be considered is the thermal treatment conditions (i.e.,

BIOGENIC AMINES IN MEAT

final temperature or heating rate); these influence decarboxylase, which in some cases, becomes inactive (Maija et al., 1995;
Kebary et al., 1999) at over 65 C, a temperature reached in
most cooked products. The cadaverine and putrescine detected
in these meat products (Table 1) merit special attention, in that
during heating they can undergo transformation to pyrrolidine
and piperidine, respectively; if they react with the nitrites in the
meat, they can form nitrosamines, which are highly carcinogenic (Patterson and Mottram, 1974; Wathensen et al., 1975).
Generally, although initially all boiled food contains low levels
of biogenic amines, the storage system applied to these kind of
products should be taken into account, because it could increase
the final level of biogenic amines. Such an increase implies a
heightened toxicological risk in the product.
Fermentation processes also generally promote the formation of biogenic amines, and in fact, this is the group of meat
products that presents the greatest amount and diversity of these
compounds (Table 1). Fermented products contain large quantities of microorganisms, accompanied by proteolysis giving
rise to high concentrations of the amino acids constituting the
nutrient required by the bacteria and the substrate on which
decarboxylase enzymes work. However, these circumstances
are affected by several factors, such as the temperature of the
medium, the microorganisms present, and the presence of additives. The temperature at which fermentation takes place (usually between 728 C), influences the formation of biogenic
amines; indeed, it has been suggested that temperature could
be a very useful parameter for preventing tyramine formation in
dry sausage, chiefly by assuring conditions favorable to starter
growth (Maijala et al., 1995; Eerola et al., 1998). One explanation for the influence of processing temperature is that the higher
fermentation temperature gives the starter culture the opportunity to outgrow nonstarter lactic acid bacteria. Maijala et al.
(1995) detected low levels of amines in the final processing
phase at a higher temperature (24 C). However, Kranner et al.
(1991) also found that histamine formation was reduced when
the ripening temperature was reduced (718 C). These results
suggest that low temperatures can make for improved quality
and longer shelf-life.
In some cases, the presence of biogenic amines in fermented
products has been attributed to poor quality of raw materials
and defective processing. The quality of raw meat material is
an essential factor in the formation of these products (Maijala
et al., 1995). Nevertheless, while the source of biogenic amines
in ripened meat products may derive partly from the raw materials, the largest proportion appears to arise in the various processing stages (Maijala et al., 1995; Vidal-Carou et al., 1990;
Bover-Cid et al., 2001a). However, not all processing stages
influence amine formation equally. Some authors (Maijala and
Eerola, 1993; Santos-Buelga et al., 1986) have reported higher
biogenic amine concentrations during ripening than during drying and salting. Zee et al. (1983) and Hernandez-Jover et al.
(1997) reported similar results, also noting a reduction in the
concentration of biogenic amines. This might be explained by a
decrease of Aw, which, combined with fat, could inhibit biogenic

497

amine formation to some extent (Eerola et al., 1996; Trevino

et al., 1997). On the other hand, Spinelli, Labritz, and Wasserman
(1974) reported no significant change in the presence of these
amines during the drying and smoking of pork bellies.
The additives used in preparation of fermented products also
are important factors in the formation of biogenic amines during
this process, and their effect appears to depend on several factors
(concentration, processing conditions, and others). However, the
results in this respect have been contradictory. Vandekerckhove
(1977) found that none of the various types of sugar used for
ripening dry fermented sausages influenced the formation of
biogenic amines, while other authors (Bover-Cid et al., 2001a)
have reported that the sugar limited biogenic amine formation
in fermented sausages. It has been demonstrated that the acidification produced by these sugars in the fermentation process
influences the formation of biogenic amines (Arnold and Brown,
1978; Smith, 1980; Masson et al., 1996). The optimum glucose
concentration for the formation of decarboxylase enzymes is
.52%, whereas concentrations above 3% inhibit it. This is related to the effect of reduced pH on microorganism growth and
the activity of enzymatic systems (Kranner et al, 1991; Masson
and Montel, 1995; Hernandez-Jover et al., 1997).
Bover-Cid et al. (2001a) reported that sodium sulphite in
sausages inhibited cadaverine production and promoted production of tyramine and putrescine. Potassium sorbate, a microbial
inhibitor, may be used to limit the formation of biogenic amines
in foods (Shalaby, 1996). Various authors (Santos et al., 1985;
Straub et al., 1994) also have reported that neither potassium
nitrate nor potassium nitrite affected the production of biogenic
amines in ripened meat products, such as salchichon, but that
the presence of these additives in soy hamburger texturizers
produced appreciable concentrations of tyramine. Besides, salt
(NaCl) significantly affects biogenic amine production, mainly
through its role in reducing Aw. It has been reported that 30 g
NaCl/l in fermented sausages enhanced tyramine production by
promoting the growth of Lactobacillus curvatus (Straub et al.,
1994).
Other factors, like sausage diameter in fermented products,
also have been reported to affect the formation of biogenic
amines during ripening (Bover-Cid et al., 1999). These authors found that the concentrations of biogenic amines in largerdiameter sausages were greater than in sausages of smaller diameter; moreover, the concentration was higher in the central
part than in the ends. This could be related to Aw, which influences the growth of microorganisms in products of this type
(Eerola et al., 1996).

CONCLUSIONS
Biogenic amines are very frequently involved in human
pathologies the world wide: neurological disorders, gastrointestinal diseases, abnormal immune responses, cancer, etc. They
are potentially toxic. They could be used as quality indexes
in food, and they are known to occur in commonly-consumed

498

C. RUIZ-CAPILLAS AND F. JIMENEZ-COLMENERO

foods, like meat and meat products. There is, therefore, a need
for thorough research into their formation and their possible effects on consumers, in order to avoid new food safety problems.
More research is needed to evaluate the impact of the factors discussed, regarding biogenic amine formation and to shed
some light on how toxic compunds of this kind could affect
consumers. Such research would be useful, with regard to technological and biochemical aspects and aspects relating to toxicology and/or mutagenicity. We need to expand our knowledge of technological factors relating to meat raw materials and
meat processing that influence the amount and proportion of
biogenic amine formation. Their importance varies according
to the type of product and the technological treatment used.
Many of the factors that promote or inhibit biogenic amine
formation can be considerably altered by the application of
emerging technologies (e.g., vacuum cooking, high pressure,
and modified atmospheres) or meat product reformulation (incorporation of new ingredients/additives, changes in cooking
temperature, reduction of fat content, salt, and so on). Such
knowledge would be helpful in introducing compositional
and/or technological changes that reduce the formation of these
amines.
Further research also is needed for the activity of the decarboxylase enzymes responsible for their formation and the
factors that modulate this activity. At the same time, research
into toxicity and/or mutagenicity is required to gain new and
useful information about the toxicity of biogenic amines and
possible synergisms. And again, we need to expand our understanding of the relationship between dose and effect, in order to
explain some of the outbreaks that have occurred after the intake
of foods containing different concentrations of biogenic amines.
In recent years, there have been some studies of in vitro toxicity
and mutagenicity of biogenic amines, but these have basically
addressed the effects of compounds taken individually.
All the proposed lines of research would make it possible to
limit the presence of biogenic amines in raw materials and/or
end products and would help health authorities to set safe, legal
limits for consumers on biogenic amines in general and not only
on histamine.
Regarding the presence of biogenic amines in meat, it also
would be useful to study their role in the formation of certain
flavor precursors in meat and meat products and their connection with antioxidant action (Lovaas, 1991). There are a number
of possibilities to be explored here. We, therefore, think it is
essential to combine efforts in the technological, biochemical,
and toxicological spheres, with a clear end in viewnamely,
to improve and guarantee consumer safety, an issue that is of
increasing concern today.

ACKNOWLEDGEMENTS
Claudia Ruiz-Capillas acknowledges funding support from
the Ministry of Science and Technology (Project Ramon y Cajal
and AGL2003-00454).

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