BLBS102-c43 BLBS102-Simpson March 21, 2012 14:30 Trim: 276mm X 219mm Printer Name: Yet to Come
43 Biogenic Amines in Foods 827produce decarboxylases and hydrolytic enzymes like proteases
and lipases. Generally, when the microbial load is high, the bio-
genic amine levels also tend to be high (Du et al. 2002).
Approximately, one-third of the microorganisms isolated from
spoiled tuna and mackerel are decarboxylase enzyme produc-
ers. These includeAcinetobacter iwoffi, Aeromonas hydrophila,
Clostridium perfringens, Enterobacter aerogenes, Hafnia alvei,
Morganella morganii, Proteus mirabilis, Proteus vulgaris, Pseu-
domonas fluorescens, Pseudomonas putrefaciens,andVibrio al-
ginolyticus,and they are members from both mesophilic and psy-
chrophilic organisms. In this regard, the mesophilic types tend
to play a relatively more significant role in histamine production
and fish flesh deterioration than their psychrophilic counterparts,
and species likeMorganella morganii,aswellasEnterobacte-
riaceae,Clostridium,andLactobacillusare of particular impor-
tance in terms of histamine production in fish (Omura et al. 1978,
Taylor 1986, Middlebrooks et al. 1988, Lakshmanan et al. 2002,
Kim et al. 2006).
Environmental factors (e.g., temperature, pH, and salt content)
also play a role in biogenic amines formation and accumulation
in fish tissues, and these factors may be manipulated to slow
down biogenic amine formation.
Fish muscle type also influences the amounts of biogenic
amines that form and/or accumulate in fish tissues. In this con-
nection, red-fleshed fish tend to have higher levels of histamine
in their tissues than their white-fleshed counterparts. This is due
to the relatively higher content of the precursor molecule, his-
tidine, in red-fleshed fish tissues, as well as higher amounts of
carbohydrates and lipids, and a slightly more acidic environ-
ment, all conditions that favor the growth and proliferation of
decarboxylase positive microorganisms.
The importance of temperature as a foremost manipulative
factor to limit the formation of biogenic amines in fish tissues is
due to the fact that several of the major histidine-decarboxylase-
positive bacteria associated with fish are mesophilic. Thus, a de-
crease in temperature slows down their growth and metabolism
(Ababouch et al. 1991). For example, icing decreases the ini-
tial mesophilic microorganism population while increasing the
lag phase of growth. Nevertheless, decreasing product tempera-
ture is not an absolute means of control. This is because certain
psychrophilic bacteria can also produce decarboxylases that can
lead to the formation of biogenic amines, even at proper refrig-
eration temperatures. Furthermore, the decarboxylase enzymes
released in fish tissues are still functional at low temperatures
although at a reduced rate. Thus, proper postharvest fish man-
agement is crucial to control formation and accumulation of
biogenic amines in fish flesh.MeatFresh meats (beef, pork, and poultry) are also non-fermented
foods known to have biogenic amines. Their high proteinaceous
nature makes them prone to proteolysis to form free amino acids
that may subsequently be decarboxylated by microbial enzymes
into the biogenic amines. Spermine and spermidine are believed
to be present in all fresh meats (beef, pork, and poultry) at fairly
constant levels, unlike the other biogenic amines that occur invarying amounts. Other predominant biogenic amines in fresh
meats are putrescine and cadaverine, together with relatively
lower levels of histamine, tryptamine, and tyramine (Paulsen
and Bauer 2007, Galgano et al. 2009). For beef, tyramine or a
combination of the three most prevalent biogenic amines, tyra-
mine, putrescine, and cadaverine, have been recommended for
use as index of quality or spoilage (Vinci and Antonelli 2002).
Fresh poultry meat can also have significant amounts of bio-
genic amines and the accumulation of compounds such as sper-
midine, putrescine, cadaverine, histamine, and tyramine tend to
increase during storage. In poultry, putrescine and cadaverine
tend to be the predominant biogenic amines and may attain to-
tal levels of 50–100 mg/kg when stored over extended periods.
Biogenic amines also accumulate more rapidly in raw poultry
meat because of the higher susceptibility of white muscle fibers
to proteolysis versus the darker muscle fibers of red meats, beef,
or pork (Perez et al. 1998, Balamatsia et al. 2006, Patsias et al.
2006).
Enterobacteriaceaespecies are believed to be primarily re-
sponsible for putrescine, cadaverine, and histamine formation
in poultry meat. Other microorganisms that have been identified
as major biogenic amine producers includeBrochothrix thermo-
sphacta, Carnobacterium divergens, Carnobacterium piscicola,
Citrobacter freundii, Enterobacter agglomerans, Escherichia
coli, Escherichia vulnaris, Hafnia alvei, L. curvatus, Morganella
morganii, Proteus alcalifaciens, and Serratia liquifaciens
(Masson et al. 1996, Pircher et al. 2007).
Biogenic amine formation and/or accumulation in non-
fermented meats are influenced by essentially the same fac-
tors as for fermented meats. For example, the type of meat is
important, as it determines the availability of the substrate or
precursor molecules. Relatively larger quantities of cadaverine
are produced in both red and white meat due to the high levels
of free lysine in both muscle types; however, red meats tend to
have higher tyramine contents from their higher free tyrosine
contents.
In fresh meats, temperature, salt content, and pH all play an
important role in biogenic amine production. However, this at-
tribute varies from species to species. For example, low pHs
enhance the production of histamine, tyramine, and tryptamine
in poultry meats by lactic acid than at a higher pH, whileEn-
terobacteriaceaeproduced less cadaverine at low pHs. High
salt concentrations also has a greater inhibitory effect on the
formation of biogenic amines, and this is due to inhibition of
microbial growth by the reducedAwfrom the high salt content;
higher temperatures promote more biogenic amines formation in
beef, pork, and poultry samples than frozen temperatures. Thus,
a higher salt content or lower storage temperature (or both) is
recommended for curtailing biogenic amine formation and ex-
tending the shelf life of meat products (Chander et al. 1989,
Karpas et al. 2002).SIGNIFICANCE TO THE FOOD INDUSTRY
Biogenic amines are of particular interest to the food industry
due to their toxicity, and their use as indicators of food qual-
ity or spoilage (Ruiz-Capillas and Moral 2004). For example,