Spoilage of Meat
G-JE Nychas and EH Drosinos, Agricultural University of Athens, Athens, Greece
Ó 2014 Elsevier Ltd. All rights reserved.
Introduction
Spoilage of meat is an ecological phenomenon that is a result
of changes to the composition of meat ecosystem during the
development of the microbial association. The establishment
of a particular microbial association on meat depends on the
ecological conditions that exist during processing, storage,
distribution, and retailing. In meat, five categories of ecological
determinant factors influence the development of the initial
and transient microbial associations and determine the rate of
attainment of a climax population by the ephemeral spoilage
of microorganisms (those that fill the niche available by
rapid growth in response to enrichment disturbance of an
ecosystem). These are (1) intrinsic factors associated with the
physicochemical attributes and structure of meat, such as pH,
water activity, buffering power, the presence of naturally
occurring or added antimicrobial components, Eh and redox
poising capacity, and nutrient composition, in particular,
carbohydrate content and the concentration of glucose; (2)
processing factors; (3) extrinsic parameters that have selective
influences effects, such as temperature, relative humidity, and
the composition of the gaseous atmosphere to which a product
is exposed during distribution and storage; (4) implicit factors,
such as the physiological properties that enable particular
organisms to flourish under selective conditions and inhibit the
growth of others, that play an important role in the genesis of
spoilage associations; and (5) complimentary emergent effects
resulting from the interactions of some of the aforementioned
factors to produce effects greater than would be expected from
their individual actions in isolation. In essence, all of these
determinant factors constitute the dimensions of a particular
ecological niche, which can be regarded as an n-dimensional
hypervolume. Indeed, the ecosystem approach is pertinent to
an analysis of the microbiological, chemical, and organoleptic
changes that occur in meat or meat products. In practice,
therefore, meat technologists attempt to modify some or all of
the noted dimension factors to either extend the shelf life
of meat or to create new products. Advances in the field of
molecular biology provide us with new insights for an
enhanced understanding of spoilage phenomena. In addition,
predictive microbiology and bioinformatics have given us the
necessary tools to describe and predict, in qualitative and
quantitative terms, the development of spoilage in meat food
systems.
Typical Microbiota of Fresh or Frozen Meat
Contamination and Population Dynamics
The microbiology of carcass meats greatly depends on the
conditions under which animals are reared, slaughtered, and
processed. Thus, the physiological status of the animal at
slaughter, the spread of contamination during slaughter and
processing, and the temperature and other conditions of
storage and distribution are factors that can affect the micro-
biological quality of meat. Unless effectively controlled, the
514 Encyclopedia of Food Microbiology, Volume 2
slaughtering process may cause extensive contamination of the
meat surfaces with a wide range of Gram-negative and Gram-
positive bacteria and yeasts (Table 1). Some of these micro-
organisms will be derived from the animal’s intestinal tract
and others from the environment with which the animal had
contact at some time before or during slaughter. Studies on the
origins of contaminants have shown that the source of
Enterobacteriaceae on meats can be work surfaces and not
direct fecal contamination. Moreover, psychrotrophic bacteria
can be recovered from hides and work surfaces within abat-
toirs as well as from carcasses and butchered meat at all stages
of processing.
Recent developments in molecular techniques have allowed
more complete descriptions of the microbial communities of
meat and meat plant microbial ecosystems. Moreover, the
ability to study the compositions of microbial association at
the subspecies level has enhanced the understanding of pop-
ulation dynamics. A combination of culture-dependent and
independent techniques is required, in at least some cases, for
the proper description of microbial ecosystems of meats.
Meat Spoilage Microorganisms
Although a range of microbial taxa are found in meat (Table 1),
its spoilage in countries in which meat is stored under refrig-
eration is caused by relatively few of these organisms (Table 2).
It is evident that chill storage and the gaseous environment of
meat in vacuum-packed or modified-atmosphere packaging
exert strong selective pressures on its microbiota (Table 3).
Consequently, a characteristic microbial association is present
on meat in different packagings at the time of spoilage, and
each type of community will manifest characteristic forms of
spoilage. For example, when meat is stored aerobically at chill
temperatures and high relative humidity, Pseudomonas spp. are
the main spoilage organisms. Gram-positive bacteria (lactic
acid bacteria and Brochothrix thermosphacta) are the main
spoilage organisms of chilled meat stored in modified atmo-
sphere rich in oxygen and carbon dioxide. To date, studies on
the contribution of yeasts to the spoilage of meat, whole or
minced, has attracted little attention even though they are
common contaminants. Yeasts do not outgrow bacteria on
meat or most meat products, but they can do so if a product
contains a bacteriostatic agent, such as sulfite, which is an
additive in British fresh sausages, or if the low water activity of
a product inhibits bacterial growth.
Spoilage under aerobic conditions
Although the Gram-negative aerobic psychrotrophic bacteria
found on meat include the species of a number of genera
(Table 2), it is now well established that under aerobic
conditions, three species of Pseudomonas – Ps. fragi, Ps. fluo-
rescens, and Ps. lundensis – are the most important spoilage
organisms. Off-odors can be detected when the population of
pseudomonads exceeds 107 colony forming units (cfu) cm
2,
and slime appears when these organisms exceed 108 cfu cm
2.
Off-odors become evident when the pseudomonads have
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 MEAT AND POULTRY j Spoilage of Meat 515

Table 1 The genera of bacteria and yeasts most frequently found on Table 2 Psychrotrophic bacteria associated with chilled meats and
meats and poultry meat products

Genus Fresh meat Processed meat VP/MAP Poultry Gram-negative bacteria Gram-positive bacteria

Bacteria Aerobes Facultative anaerobes

Acinetobacter xx x x xx Pseudomonas spp. Brochothrix thermosphacta
Aeromonas xx x x rRNA homology, Group I [Ps. Strict anaerobes
Alcaligenes x x fluorescens Biovars I, II, III, Clostridium spp., C. estertheticum,
Alteromonas x x x x IV, V (includes 7 clusters) C. tagluense, C. putrefacien,
Arthrobacter x x x x Ps. lundensis, Ps. fragi] C. algidicarnis, C. frigoris/
Bacillus x x x Pseudomonas-shewanella group estertheticum, C. gasigenes
Bacteroides x Shewanella putrefaciens
Brochothrix x x xx x Alteromonas spp.
Campylobacter xx Alcaligenes spp.
Carnobacterium x x xx x Achromobacter spp.
Chromobacterium x Flavobacterium spp.
Citrobacter x x Moraxella spp.
Clostridium x x x Psychrobacter spp.
Corynebacterium x x x x P. immobilis, P. phenylpyruvicus
Cronobacter x x x x Acinetobacter spp.
Enterococcus xx A. lwoffii, A. johnsonii
Escherichia x x Facultative anaerobes Aerotolerant anaerobes
Flavobacterium x xx Photobacterium spp. Lactobacillus spp.
Hafnia x x Vibrio spp. L. sakei, L. curvatus,
Janthinobacterium x Aeromonas spp. L bavaricus
Klebsiella xx Plesiomonas spp. Carnobacterium spp.
Kluyvera xx Serratia spp. C. divergens
Kurthia x x S. liquefaciens, S. marcescens C. piscicola
Lactobacillus x xx xx S. proteamaculans Leuconostoc spp.
Leuconostoc x x x Citrobacter spp. L. carnosum, L. gelidum,
Listeria x C. freundii, C. koseri L. amelibiosum,
Micrococcus x x x x Providencia spp. L. mesenteroides subsp.
Moraxella xx x P. aerogenes, P. alcalifaciens, mesenteroides
Neisseria x x x P. stuartii, P. rettgeri Weissella spp.
Pantoea x Hafnia spp. W. hellenica,
Pediococcus x x x Hafnia alvei W. paramesenteroides
Planococcus x Pantoea agglomerans Lactococcus raffinolactis
Plesiomonas x Enterobacter spp.
Providencia x E. cloacae, E. agglomerans,
Proteus x x E. aerogenes
Pseudomonas xx x x xx Erwinia spp.
Psychrobacter x Erwinia herbicola
Serratia x x x x Klebsiella spp.
Shewanella x K. pneumoniae
Streptococcus x xx x x Kluyvera spp.
Streptomyces x x Proteus spp.
Staphylococcus x P. vulgaris, P. mirabilis
Vibrio x
Weisella x x
Yeasts
Candida xx xx x Serratia proteamaculans are the major representatives of this
Debaryomyces x x family (Table 2). Brochothrix thermosphacta has been detected in
Rhodotorula x xx the aerobic spoilage biota of chilled meat, but it is usually not
Saccharomyces x important in the spoilage of meat exposed to air, except
Torulaspora xx
possibly lamb. This organism has been isolated from beef
Trichosporon x x
carcasses during boning, dressing, and chilling. Moreover,
x, reported occasionally; xx, reported frequently; VP/MAP, meat stored under lairage slurry, cattle hair, rumen contents, soil from the walls of
vacuum or in modified-atmosphere packaging. slaughter houses, the hands of workers, air in the chill room,
neck and skin of the animal, and cut muscle surfaces have been
depleted the glucose and lactate available to them on meat shown to be contaminated with this organism. Brochothrix
surfaces and begin to metabolize the amino acids. thermosphacta is one of the main – if not the most important –
Enterobacteriaceae rarely, if ever, contribute significantly to causes of spoilage that can be recognized as souring rather than
the spoilage biota on meat and meat products. In ground beef, putrefaction. This type of spoilage is commonly associated with
Pantoea agglomerans, Escherichia coli, Serratia liquefaciens, and meat packed under modified atmospheres. A possible role of
516 MEAT AND POULTRY j Spoilage of Meat
Table 3 Substrates used for growth by major meat spoilage microorganisms
Microorganism Under aerobic conditions
Pseudomonas spp. Glucose, glucose 6-phosphate, lactic acid, pyruvate,
gluconate, gluconate 6-p, amino acids, creatine,
creatinine, citrate, aspartate, glutamate
Acinetobacter/Moraxella Amino acids, lactic acid
Shewanella putrefaciens Glucose, lactic acid, pyruvate, gluconate, propionic acid,
ethanol, acetate, amino acids
Brochothrix thermosphacta Glucose, amino acids, ribose, glycerol
Enterobacter spp. Glucose, glucose 6-p, amino acids, lactic acid
Lactobacillus spp. Glucose
Photobacterium spp. in aerobic spoilage has been indicated by
its detection in aerobic spoilage biota by culture-independent
techniques.
Spoiler under vacuum or modified atmospheres
The atmosphere to which meat is exposed may be modified by
vacuum packaging or packaging of meat under atmospheres
containing a mixture of gasses (N2, CO2, and O2). Meat in
vacuum pack or modified atmosphere has an extended shelf
life when compared with meat stored aerobically. Shelf life is
determined by the type of atmosphere, storage temperature,
and meat type. The growth of strictly aerobic, Gram-negative
bacteria (in particular, pseudomonads) is restricted by the
relative high concentration of CO2 or oxygen limitation.
Consequently, Gram-positive lactic acid bacteria, such as
Lactobacillus sakei, Leuconostoc spp., and Weissella viridescens are
usually the main components of the spoilage association
(Table 3).
As the Gram-positive organisms grow more slowly than the
Gram-negative organisms in air, the shelf life of meat is
extended beyond that attained in air. Because there are differ-
ences in the metabolic attributes of the two groups of spoilage
organisms, spoilage occurs at different times, is manifest in
different ways, and is characterized by different off-odors.
Psychrophilic microorganism, Clostridium estertheticum,
causes gross distension of packs of vacuum-packaged meat after
relatively short times of storage at chiller temperature. The
optimum growth temperature of this strictly anaerobic
organism is 10  C. The spores produced by this organism are
resistant to those factors in meat processing that kill wholly
vegetative psychrophiles. Other cold-tolerant clostridia associ-
ated with spoiled vacuum-packaged meat are shown in Table 2.
Spoilage of frozen meat
Studies of microbial growth at subfreezing temperatures clearly
indicate that microbial growth does not occur in meat ecosys-
tems at temperatures of less than
8  C. Thus, the main
determinants of the storage life of properly frozen meat are
physical, chemical, or biochemical changes that are unrelated
to microbiological activities.
There are particular problems with the enumeration of
microbial populations on frozen meats. Microorganisms are
injured by exposure to freezing temperatures, leading to
sublethal injury, the effects of which include increased lag
Substrates used for growth
Under oxygen limitation or modified atmospheres
Glucose, lactic acid, pyruvate, gluconate, amino acids
Amino acids
Glucose, serine, cysteine
Glucose
Glucose, glucose 6-p, amino acids
Glucose, lactic acid, amino acids
times and the inability to grow on selective media that do not
inhibit the uninjured bacteria. Appropriate resuscitation of
frozen meat biota before their enumeration is essential if their
numbers are to be determined properly. Resuscitation of the
injured biota may take place in meat ecosystem during thaw-
ing, or in or on nonselective culture media. Studies on the effect
of different environmental stresses on the enumeration and the
recovery of microorganisms have been focused largely on
pathogenic microorganisms with an emphasis on ascertaining
the presence or absence of the pathogenic bacteria rather than
their numbers. The results obtained in such studies are required
for the evaluation of microbiological hazards.
Roles of Microbes and Enzymes in Spoilage
The metabolic activities of the organisms that grow in a meat
ecosystem lead to the changes that are perceived as spoilage.
The type and magnitude of a spoilage condition is related to the
size of the bacterial population and the amounts of bacterial
substrates in the meat. Irrespective of whether the meat is held
under aerobic conditions, in vacuum pack or under modified
atmospheres, the predominant organisms in the various biota
that develop all preferentially catabolize glucose for growth.
When the amount of glucose available to the organisms is
reduced to growth-limiting levels, organoleptically detectable
changes and, subsequently, overt spoilage develop, because of
bacterial catabolism of amino acids and other nitrogenous
compounds as well as secondary metabolic reactions. The
contribution of indigenous meat enzymes to spoilage is
negligible compared with the effects of the activities of the
microbial biota.
Biochemistry of Spoilage
The critical physicochemical changes occurring during spoilage
take place in the aqueous phase of meat. This phase contains
glucose, lactic acid, certain amino acids, nucleotides, and urea
that are utilized by bacteria of the meat microbiota. The
concentrations of these low–molecular weight compounds are
sufficient to support extensive microbial growth. Glucose is the
preferentially utilized nutrient in a meat ecosystem, and it is
catabolized initially during microbial growth. This substrate is
attacked by almost all groups of spoilage bacteria, under both
aerobic and anaerobic conditions (Table 4). Until spoilage is
evident organoleptically, a major detectable effect of bacterial
 MEAT AND POULTRY j Spoilage of Meat 517

Table 4 Utilization of substrates, formation of metabolic by- Table 5 End-products formed by Gram-negative bacteria (e.g.,
products, and proteolytic activities of three species of Pseudomonads Pseudomonas spp., Shewanella putrefaciens, Moraxella spp., etc.) when
growing in meat juice at 0–4  C grown in broth, a sterile meat model system, and naturally spoiled meat

Pseudomonas spp. Sulfur compounds Aliphatic hydrocarbons

Sulfides, dimethylsulfide, Hexane
Substrate or by-product P. fragia
P. lundensis P. fluorescens dimethyldisulfite, methyl 2,4-Dimethylhexane and
D-glucose c c c mercaptan, methanethiol, methylheptone
hydrogen sulfide,
D-glucose 6-p c c –
D-gluconate f f f dimethyltrisulfide
D-gluconate 6-p f f – Esters Aldehydes
Methyl esters (acetate), 2-Methylbutanal
L-lactic acid c c c
D-lactic acid c c c ethyl esters (acetate)
Pyruvate f/c f/c f/c Ketones Alcohols
Acetic acid c nd nd Acetone, 2-butanone, Methanol, ethanol,
acetoin/diacetyl 2-methylpropanol,
Amino acids c c c
Creatine c – – 2-methylbutanol,
Creatinine c – – 3-methylbutanol
Proteolysis yes nd yes Aromatic hydrocarbons Biogenic amines – Other compounds
Diethyl benzene, trimethylbenzene, Cadaverine, ammonia, putrescine,
Ammonia f f f
toluene methylamine, trimethylamine
a
The substrate was c, catabolized during growth; f, formed during growth; or –,
neither catabolized nor formed during growth; nd, no available data.

volatile compounds found in spoiled meat is given in Table 6.

growth is a reduction of the glucose concentration. This does Pseudomonads growing on the surface of meat preferentially
not alter the organoleptic properties of meat. When this consume glucose until the rate of diffusion of glucose from
substrate or its oxidative products are reduced to levels insuf- underlying tissues becomes inadequate to meet their demand.
ficient to support growth, lactic acid is catabolized. When this When high numbers (108 per cm2) are reached and glucose
second major carbon and energy source is exhausted, the becomes depleted on the meat surface, the pseudomonads start
microbial association is at its climax stage. proteolysis or use amino acids and other nitrogenous com-
pounds as their growth substrate, with production of
Chemistry under aerobic conditions malodorous amines sulfides and esters (Table 6).
The relative spoilage potential of bacteria depends on their
abilities to predominate in spoilage flora and to form
malodorous compounds, such as H2S, volatile amines, esters, Table 6 End-products of homfermentative lactic acid bacteria (HO),
and acetoin. Pseudomonas spp. are important because of their heterofermentative lactic acid bacteria (HT), and Brochothrix
dominance in the aerobic climax associations at chill temper- thermosphacta (BT) when grown in broth, a sterile meat model system,
atures. The key chemical changes associated with the metabolic and naturally contaminated meat
attributes of pseudomonads have been studied extensively in
Atmosphere
broth and in model system, such as meat juice. A synopsis of
key metabolic attributes of pseudomonads is shown in Table 5. Microaerobic/
Among the major attributes are (1) the sequential catabolism Aerobic Anaerobic
of D-glucose and L- and D-lactic acid with D-glucose being used End-product HO HT BT HO HT BT
preferentially to lactate, and (2) the oxidization of glucose and
glucose 6-phosphate via the extracellular pathway that caused Carbon dioxide þ þ þ – – –
a transient accumulation of D-gluconate and an increase in the Formic acid þ þ þ þ þ þ
concentration of 6-phosphogluconate. The increase in the Acetic acid þ þ þ þ þ þ
L-Lactic acid þ þ þ þ þ þ
concentration of D-gluconate led to a proposed control of
D-Lactic acid þ þ – þ þ –
the microbial activity in meat by the addition of glucose to
Isobutyric acid – – þ – – –
meat, with its transformation to gluconate by pseudomonads. Isovaleric acid – – þ – – –
The rationale for this is the fall in pH caused by the accumu- 2-Methylbutyric acid – – þ – – –
lation of the oxidative products. The transient pool of gluco- Ethanol þ þ þ þ þ þ
nate, which cannot be utilized by all the taxa of the association 2-Methylbutanol – – þ – – –
spoilage biota may provide an additional selective determinant 3-Methylbutanol – – þ – – –
for the meat ecosystem. 2-3-Butanediol – – þ – – –
Another important feature is the catabolism of creatine and 2-Methylpropanal – – þ – – –
creatinine by P. fragi. The release of ammonia and the increase 2-Methylpropanol – – þ – – –
Acetoin þ þ þ þ – –
in pH are linked inextricably with the catabolism of these
Diacetyl þ þ þ – – –
substrates. Ammonia, which is the major cause of the increase
Free fatty acids – – þ – – –
of pH, is produced by many microbes, including pseudomo- Hydrogen peroxide þ þ – – – –
nads during their catabolism of amino acids. A list of other
518 MEAT AND POULTRY j Spoilage of Meat
Enterobacteriaceae can be important in spoilage if the meat
ecosystem favors their growth. As with the pseudomonads,
this group preferentially utilizes glucose, but also glucose
6-phosphate, as the main carbon sources, and only after the
exhaustion of these substances will they utilize amino acids.
Some members of this family produce volatile sulfides,
including H2S and malodorous amines from amino acid
metabolism (Table 6).
Species of Acinetobacter and Moraxella usually form a major
part of populations of aerobic spoilage bacteria. These organ-
isms are of low spoilage potential. They utilize amino acids as
their growth substrates, but they do not form malodorous by-
products from amino acid degradation. They rather enhance
the spoilage activities of pseudomonads and Shewanella putre-
faciens by restricting the availability of O2 to these organisms.
When O2 limits growth, pseudomonads attack amino acids,
even when glucose is present, with the subsequent production
of malodorous substances. Under anaerobic conditions
S. putrefaciens will generate H2S, resulting in discoloration
(greening) of meat due to sulfmyoglobin formation.
Biochemical changes in meat under vacuum and modified-
atmosphere packaging conditions
A shift from a diverse initial biota to one dominated by Gram-
positive aerotolerant and facultative anaerobic microbiota
(lactic acid bacteria and B. thermosphacta) usually occurs in
meat during its storage under modified atmospheres. The
physiological attributes of the lactic acid bacteria and
B. thermosphacta have been studied extensively. Environmental
conditions, such as the oxygen tension, glucose concentration,
and the initial pH, have a major influence on the physiology of
these organisms and hence on the end-products formed. Bro-
chothrix thermosphacta has a much greater spoilage potential
than lactobacilli and can be important in both aerobic and
anaerobic spoilage of meat. This organism utilizes glucose and
glutamate but no other amino acid during aerobic incubation.
It produces a mixture of end-products, including acetoin, ace-
tic, iso-butyric and iso-valeric acids, 2,3-butanediol, diacetyl,
3-methylbutanal, 2-methylpropanol, and 3-methylbutanol
during its aerobic metabolism in media containing glucose,
ribose, or glycerol as the main carbon and energy source. The
precise proportion of these end-products is affected by the
concentration of glucose, pH, and temperature.
Lactobacillus spp. constitute only a small proportion of the
spoilage bacteria in the initial bacterial population of meat.
When the oxygen concentration is low, as in vacuum-packed
meats, the developing microbiota is usually dominated by
Lactobacillus spp. These fermentative organisms probably grow
faster than would-be competitors because they are unaffected
by pH and antimicrobial products, such as lactic acid, H2O2,
and bacteriocins. These organisms utilize glucose for growth
and produce lactic acid. When carbohydrates are exhausted,
amino acids are utilized with the consequent production of
volatile fatty acids, which impart a ‘dairy’ or ‘cheesy’ odor to the
vacuum-packaged meat. The cheesy odors that develop in meat
stored in gas mixtures containing CO2 probably are produced
by B. thermosphacta and lactic acid bacteria. They also form
diacetyl, acetoin, and alcohols from glucose under aerobic
conditions or low partial pressures of oxygen (pO2). Ethanol
and propanol are present at only trace levels at the beginning of
storage, but their concentrations can increase significantly
before the onset of spoilage. They may then be the most
promising compounds as indicators of spoilage microbiota
development.
Evaluation of spoilage
Enumeration of bacterial populations of meats, by culture on
agar media, most probable number (MPN) techniques, or
rapid methods (malthusian; e.g., Impedance), is used as an
indicator of their hygienic conditions. As the spoilage of meat is
caused by specific spoilage bacteria, appropriate selective
media rather than nonselective media should be used for this
purpose. Because correlations between populations of specific
spoilage bacteria and sensorial manifestations of spoilage are
imprecise, bacterial numbers do not allow unambiguous esti-
mation of the spoilage status of meats.
It would be desirable to replace time-consuming microbi-
ological analyses with chemical, enzymatic, or physicochemical
tests for the rapid indication of the extent of microbial growth
on meat. Many chemical or physical methods have been
proposed for the estimation of the spoilage status of meats.
There is as yet no single test that is satisfactory. The perception
of spoilage is a subjective evaluation, and there is a lack of
general agreement on the signs of incipient spoilage of meat.
Moreover, changes in the technology of meat preservation,
such as vacuum and modified-atmosphere packaging, has
further complicated the task of identifying spoilage indicators.
Indicators of meat spoilage status, such as microbial
metabolites, should meet the following criteria:
1. The indicator should be absent or initially at low levels in
meat.
2. It should increase proportionally with the storage period.
3. It should be produced by the dominant biota and correlate
well with organoleptic evaluations.
The identification of an ideal metabolite that meets the
noted criteria has proved difficult for several reasons:
1. Most metabolites are specific to certain organisms (e.g.,
gluconate to pseudomonads).
2. Although the metabolites are the product of the metabolism
of a specific substrate, the absence of the given substrate or
its presence in low quantities does not preclude spoilage.
3. The rate of microbial metabolite production and the
metabolic pathways of spoilage bacteria are affected by the
environmental conditions (e.g., pH, oxygen tension,
temperature).
4. The accurate detection and quantification of metabolites
require sophisticated methodologies.
Many metabolites, such as lactate, gluconate, or acetate,
provide information only after spoilage has developed. Bio-
informatics and chemometrics using data obtained during the
analysis of meat, however, can provide useful information for
the evaluation of spoilage. Predictive microbiology, which
uses mathematic equations to describe the growth kinetics of
microorganisms, has gained increasing attention as a means
of estimating the remaining shelf life of meat. A multivariate
analytical approach to associate meat spoilage with microbi-
ological and physicochemical parameters might allow for
more accurate assessment of the spoilage status. Multivariate

analysis involves the statistical analysis of data for several
variable components and qualities of meat. A mathematical
model is used to describe the correlations between variables.
Several multivariate models are used for different purposes,
such as likelihood equations, factor analysis, and time-series
analysis.
Role of Cooking in Susceptibility to Spoilage
Cooking raw meat results in the death of its microbial associ-
ation, with the exception of heat-resistant spores. Recontami-
nation of the cooked meat and subsequent storage at chiller or
ambient temperatures leads to the development of new
spoilage associations. As the competitors of the initial micro-
biota of raw meat are absent, pathogens that may contaminate
cooked meat may be constrained in their proliferation only by
temperature. The microbiological stability of cooked meat
products depends not only on extrinsic factors, mainly the
packaging method and storage temperature, but also on the
intrinsic factors of product composition.
Special Problems Associated with Meat
Production of biogenic amines by microbial biota of stored
meat is a matter of concern. Amines have been detected in fresh
meat stored in air, in vacuum pack, or under modified atmo-
spheres. Among the amines, putrescine, and cadaverine
increase progressively during storage. Concentration of sper-
mine, spermidine, and tryptamine do not change substantially.
Small increases in the concentration of tyramine are usually
observed after long storage periods.
Consumer Risks from Meat Products
Hazards associated with the consumption of meat and meat
products arise mainly from the possible presence of pathogens
on meat. Although pathogenic bacteria are not a part of the
spoilage association as such, their occurrence in the microbiota
is possible because of their presence on the raw meat or their
transfer to a product during unhygienic processing.
It is generally recognized that the ecosystems of meat stored
under modified atmosphere do not result in novel microbial
hazards and that their safety characteristics are equivalent to
those of meat stored aerobically under refrigeration. The safety
of modified-atmosphere-packaged meat is affected mainly by
two basic but indirect factors: (1) the suppression of the
spoilage biota with consequent reduction in its potential to
MEAT AND POULTRY j Spoilage of Meat 519
suppress the growth of pathogens, and (2) the delay or
suppression of the normal course of spoilage.
Studies with psychrotrophic pathogen bacteria have shown
that vacuum and modified-atmosphere packaging with ni-
trogen creates atmospheres that may readily support the growth
of Yersinia enterocolitica, Aeromonas hydrophila, and Listeria
monocytogenes. The growth of these organisms, however, is
inhibited by the enrichment of atmosphere with carbon
dioxide. Generally, the higher the CO2 concentration and the
lower the temperature and pH, the greater the inhibition of
these organisms. At normal meat pH (5.5) and low tempera-
ture (1  C), the growth of the psychrotrophic pathogens is
stopped when the CO2 concentration is 40% (v/v). When
the meat pH is high (6.0) or the product is stored
at abusive temperatures, however, these organisms and non-
psychrotolerant pathogens may grow from pathogens despite
there being no unacceptable change in the organoleptic qual-
ities of the product.
Further Reading
Corry, J.E.L., 2007. Spoilage organisms of red meat and poultry. In: Mead, G.C. (Ed.),
Microbiological Analysis of Red Meat, Poultry and Eggs. Woodhead Publishing,
Cambridge, UK, pp. 101–122.
Dainty, R.H., Mackey, B.M., 1992. The relationship between the phenotypic properties
of bacteria from chill-stored meat and spoilage processes. Journal of Applied
Bacteriology Symposium Supplement 73, 103S–114S.
Davies, A.R., Board, R.G. (Eds.), 1998. The Microbiology of Meat and Poultry. Blackie
Academic and Professional, London.
Ercolini, D., Russo, F., Nasi, A., et al., 2009. Mesophilic and psychrotrophic bacteria
from meat and their spoilage potential in vitro and in beef. Applied and Environ-
mental Microbiology 75, 1990–2001.
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Relevant Websites
http://www.fsis.usda.gov/Fact_Sheets/Meat_Preparation_Fact_Sheets/.
http://safemeat.org/.
http://www.prosafebeef.eu/ – Prosafebeef.
http://www.q-porkchains.org/ – Q-Pork Chains.
http://elvis.ccc.cranfield.ac.uk/sorf/faces/ResearchArea/home.xhtml – Symbiosis.