Spoilage of Cooked Meat and Meat Products
I Guerrero-Legarreta, Uniiversidad Autónoma Metropolitana, México D.F., Mexico
Ó 2014 Elsevier Ltd. All rights reserved.
This article is a revision of the previous edition article by Isabel Guerrero, Lourdes Pérez Chabela, volume 2, pp. 1266–1272, Ó 1999, Elsevier Ltd.
Introduction
Meat spoilage can develop as a result of a wide variety of
factors, such as improper handling, exposure to air and high
temperature, and other conditions that initiate adverse chem-
ical reactions or result in microbial contamination. However,
the most common cause of meat spoilage is the presence of
microorganisms and their metabolites. Deleterious changes
of a chemical or microbial nature lead to consumer rejection of
products, with consequent economic losses.
Because of the complex and diverse compositions of meat
and meat products, a wide variety of microorganism can be
present in meat spoilage flora. There is a naturally occurring
microflora selected by the meat environment, including
intrinsic and extrinsic factors. A combination of these factors
and the processing conditions lead to the selection of specific
microorganisms and thus determine the reactions that finally
spoil meat products.
Meat shelf-life extension is achieved by various techniques,
applied to either raw or processed products, and depending
on the desired characteristics of the final product. All these
processes are aimed at inhibiting, to various degrees, the
growth of the microbial population, and undesirable reactions
involving meat components, so that the product wholesome-
ness is preserved for an extended time.
The most frequent undesirable alterations of meat products
are the development of off-odors and off-flavors due to micro-
bial metabolites; development of slime on the product surface;
color changes due to pigment alteration, such as greening or
browning as a result of pigment oxidation; package blowing due
to gas production by specific microorganisms; and lipid oxida-
tion, which can be accelerated as a result of the actions of
microbial lipases. Although meats and meat products are
rendered inedible mostly be off-odors and flavors, consumer
rejection can also be due to discoloration, or any other alteration
that is considered to indicate unwholesome product.
Heat Processed Meat
The various operations used in meat processing give more
palatable products and, at the same time, ensure their sanita-
tion, diversify the product inventory and, in most cases,
improve digestibility. By following the hurdle technology
concept, and depending on the desired characteristics of the
food, a given meat product will be subjected to one or several
means of preservation.
Preservation by thermal processing is the result of the
destruction of spoilage microorganisms and enzyme inactivation.
Depending on the required shelf life, a treatment of the necessary
severity is applied. Therefore, heat treatments vary from cooking,
which can be a relatively mild treatment, to commercial sterili-
zation, which is a drastic process ensuring that practically all
508 Encyclopedia of Food Microbiology, Volume 2
microorganisms are destroyed. Under certain circumstances,
the toxins produced by some microorganisms are also destroyed.
Initial Microbial Population
The growth of a given microorganism depends on its ability to
utilize components of meat as growth substrates. However,
processing, packaging, and storage conditions (temperature,
additives, and oxygen availability) select specific microflora
that can alter the organoleptic qualities of fabricated products.
Microorganisms (bacteria, yeast, and molds) first utilize low
molecular weight nutrients, such as glucose, glucose-6-phos-
phate, ribose, glycerol, amino acids, and lactate, which alter the
flavor, odor, and general appearance of meats. If the rate of
glucose utilization by microorganisms growing on the surface
of an otherwise sterile product is higher than its rate of
diffusion from the inner part, amino acids are utilized by
pseudomonads and Enterobacteriaceae, with the production of
ammonia and offensive sulfurous and nitrogenous by-products.
Therefore, the glucose content in a meat product can be critical
for determining the time of spoilage onset.
Microorganisms contaminate raw meat during slaughtering
and evisceration operations. The main sources of contami-
nants are the animal’s skin and feces, the abattoir’s floor, and
carcass handling by the workers. These microbial populations
are mainly yeast, bacilli, micrococcus, staphylococcus, cor-
ynebacteria, and other bacteria (Moraxella, Acinetobacter,
Pseudomonas, Enterobacteria, Salmonella spp., Listeria spp., and
Shewanella putrefaciens). Prolonged refrigeration allows colo-
nization of carcass surfaces by psychrotrophs, mainly Brocho-
thrix thermosphacta, Carnobacterium spp., Lactobacillus spp.,
Leuconostoc spp., and Weissella spp. Microflora of raw meat
stored in air under refrigeration is dominated by aerobic
psychrotrophs, mainly Pseudomonas spp. and Psychrobacter
inmobilis. In the case of raw poultry, spoilage microflora is
dominated by Acinetobacter, Brochothrix, Pseudomonas, lactic
acid bacteria (LAB), and yeasts.
B. thermosphacta is one of the most ubiquitous spoilage
microorganisms in raw and processed meats. This gram-
positive, non-spore-forming facultative anaerobe utilizes glucose
as the only substantial component of meat that supports its
growth. When meat is stored in aerobic conditions, it produces
acetoin, and acetic, isobutyric, and isovaleric acids, as well as
their aldehydes and alcohols, all of which are highly odoriferous
compounds that are taken as spoilage indicators. However,
Pseudomonas dominate aerobic flora; B. thermosphacta being
important only when growth of pseudomonads in aerobic
atmospheres is inhibited by factors such as CO2 (carbon
dioxide) atmospheres. Red meat stored in CO2-rich atmospheres
is dominated by LAB. Meats packaged in films partially
permeable to oxygen are colonized by Aeromonas, Enterobacter,
Hafnia, B. thermosphacta, Acinetobacter, and Enterobacteriaceae.
In vacuum packages, meat is colonized by Lactobacillus
http://dx.doi.org/10.1016/B978-0-12-384730-0.00196-8
 MEAT AND POULTRY j Spoilage of Cooked Meat and Meat Products
spp., Enterobacteriaceae, Leuconostoc spp., S. putrefaciens, and
Clostridium spp.
Process Calculations
Thermal process calculations consider basic information on the
thermal resistance of a target microorganism, the destruction of
which is taken as the objective of the thermal treatment; the
temperature history of the food; the way the product has been
handled; and the required shelf life under given storage
conditions. Another heat-processing objective may be enzyme
inactivation, although the conditions for microbial destruction
will also result in enzyme inactivation. Traditionally, process
calculations consider that as heating involves the destruction of
at least one microbial enzyme necessary for bacterial metabo-
lism, vegetative cells and spores are inhibited according to
a first-order rate equation. However, Peleg (2006) considered
that the exponential inactivation rate depends on the spores’
previous thermal history, which is not considered in the
exponential inactivation rate equations that are derived from
a log-linear Arrhenius model.
As the driving force is dependent on the temperature
difference between the food and the heating medium, the larger
the difference, the higher the flux rate. Conduction occurs by
direct contact between food particles. Convective heating by air
or steam at the product surface occurs due to temperature
differences between the heating medium and the surface.
Convective heating is more efficient if forced convection is
applied. In airfree, i.e., unforced, convective heating, the transfer
coefficient is low (2.5–25 kcal h 1m2 K), and the limiting factor
is heat transfer from the heating medium to the product surface.
In contrast, with condensing steam, the heat transfer coefficient
is high (5000–15 000 kcal h
1 m2 K), and the limiting factor is
the rate of heat conduction within the product. Other parame-
ters considered for process calculations are the physical and
chemical properties of the product (in this case, the meat) and
the heat transfer coefficients of the food and the container.
Cooked Meat
Cooking treatments are often used for meat and meat products. In
the case of sausages and similar products, the meat is first stuffed
into impermeable casings. Heat is transferred from the heating
medium (e.g., hot air, steam, smoke) to the product and, at the
same time, water from the product is transferred as vapor to the
heating medium. Cooking is carried out in various ways,
depending on how the heat is applied as well as the processing
temperature. These cooking methods include oven cooking,
grilling, roasting, frying, boiling, and steam cooking. Dry heat at
more than 100  C is applied in oven cooking, grilling, and
roasting; boiling and steaming are carried out by placing the food
in water or exposing it to steam. Dry heat is less efficient than wet
heat for inactivating vegetative cells or the spores of
microorganisms.
Scalding and pasteurization are processes similar to cook-
ing, and they are applied to raw meat to inactivate spoilage and
to pathogenic bacteria on meat surfaces. Partial cooking of
emulsion products, like bologna, or scalding of dried or
semidried fermented sausages are applied to inactivate lactic
509
starters and to control acid production. Scalding is carried out
by treating the product with hot water or steam at 90–100  C
for a given time, depending on the processing objective
(enzyme/microbial inactivation or partial cooking). Pasteuri-
zation is carried out at temperatures below 100  C to kill most,
but not all, viable cells in or on a product. Therefore, it is
applied to meats that will be subject to additional preservation
treatments, such as refrigeration or preservative addition, alone
or in combination with preservative packaging of product.
Mild heat treatments (scalding or pasteurization) do not
necessarily inactivate all heat-resistant psychrotrophs, such as
Lactobacillus viridescens or enterococci; the surviving cells of
which may grow to spoil the product by off-flavor, gas produc-
tion, or greening. Temperature, pH, and salt concentration are
the main factors that select the spoilage microflora of cooked
meats. Under refrigeration conditions, gram-positive bacteria
such as Leuconostoc mesenteroides subsp. mesenteroides, Lactococcus
lactis subsp. Lactis, and Leuconostoc citreum are predominant in
the microflora of cooked meats. Spoilage by these and other LAB
generally require microbial growth, unless sulfide-producing
strains are present. The LAB cause undesirable sensory changes
due to the formation of acetate, formate, ethanol, and, some-
times, H2S. Although LAB generally become dominant, other
organisms such as B. thermosphacta or Enterobacteriaceae may be
present in cooked meat spoilage flora. LAB are destroyed during
cooking, but recontamination by these organisms can occur if
the product is not properly handled and packaged after cooking.
Mesophiles grow in cooked meats stored at temperatures
above 10  C; Enterobacteriaceae can predominate at levels above
107 cfu g
1. Spoilage of cooked meat of high pH (>6.5),
evident by texture and odor changes, is due to the growth of
oxygen-dependent Bacillus cereus and Bacillus licheniformis,
although microflora are mainly composed of Yersinia enter-
ocolitica, Serratia liquefaciens, S. putrefaciens, and Lactobacillus sp.
Canned Meat
The objective of canning is to destroy microbial populations,
spores as well as vegetative cells, and enzymes that can cause
spoilage. Canning treatments are based on time–temperature
conditions that consider the heat resistance of the specific micro-
organisms of concern. Inactivation of a pathogen or spoilage
microorganisms is calculated by reference to the heat penetration
rate and the shelf-life extension required for the specific food.
Process calculations for cooked meat or meat products are based
on the destruction of target pathogens and spoilage microorgan-
isms. Vegetative cells are inactivated at temperatures somewhat
above the optimum for the growth of an organism, but the spores
formed by some bacteria are highly resistant to inactivation by
heating. For long shelf-life products, heating sufficient to inacti-
vate spores of botulinum organisms is applied.
Although total sterility is not achieved for canned foods, from
a commercial point of view, a food can be considered sterile if it is
free from viable spores of Bacillus stearothermophilus or Clostridium
perfringens. In general, spores of proteolytic organisms of the strict
anaerobic Clostridium botulinum group are taken as the target due
to the pathogenicity of the bacteria and the high heat resistance of
their spores. In addition to specific pathogens, other target spore-
forming microorganisms include B. stearothermophilus, Bacillus
thermoacidurans, Bacillus macerans, and Bacillus polymyxa. In the
510 MEAT AND POULTRY j Spoilage of Cooked Meat and Meat Products
case of poultry products, the targets include C. prefringens spores,
or the vegetative cells of Salmonella spp., Staphylococcus spp., and
Campylobacter spp. Spore-forming thermophiles are also of
concern if the food is stored at high temperatures. This is the case
for canned foods marketed in tropical regions that are expected to
have at least a 1-year shelf life at temperatures above 35  C and
high humidity. Heat treatment conditions that destroy Clos-
tridium sporogenes spores result in a thermostable food with
a considerably longer guaranteed shelf life without the need for
other preservation measures.
Because most canned meats undergo a drastic heat treatment
calculated to inactivate most spoilage microorganisms, they do
not require further refrigeration. Spoilage of canned meats is due
to errors in heat processing or to recontamination after pro-
cessing because of can failure. It is important to note that the
rheological (fluidity) characteristics of products may change
during heat processing. This is the case for canned emulsions,
such as luncheon meats and pâtés, in which the product changes
from a semifluid to a solid with the mechanism of heat transfer
within the product changing from convection to conduction.
Process calculations must account for these changes.
In the case of recontaminated cans, spoilage microorgan-
isms find their way into the can through sealing defects or
punctures. Gas-producing microorganisms cause can blowing,
that is, swelling, or souring with no gas production, as is the
case of contamination with homo-fermentative LAB. In many
cases, the contaminant microflora of canned meats consists of
spore-forming bacteria. If the can was not properly exhausted
(i.e., air was not completely removed from the can) due to
underprocessing during scalding or sterilization, Bacillus subtilis
and Bacillus mycoides can be present.
Processed Meats
Processed meats undergo one or more preservation treatments.
Processed products are expected to have a longer shelf life than
raw meat because microbial populations and enzymatic
activity have been partially or totally inactivated. Depending on
the product type, the required shelf life, and the expected
distribution and storage conditions, one or more preservation
treatments may be applied. However, meat products can still
undergo spoilage, with the particular spoilage process and time
it takes to start developing depending on the product’s intrinsic
characteristics and the storage conditions.
Smoking
Smoking is a form of cooking meat products, such as finely or
coarsely comminuted sausages or whole pieces of meat, by
placing them in moisture-permeable casings that act as a barrier
between the heating medium and the meat. Heat is transferred
from the hot air in the smokehouse, along with chemicals in the
smoke, to the casing surface. Smoke components diffuse though
the casing and into the meat. The main components of wood,
cellulose, hemicelluloses, and lignins are degraded at tempera-
tures from 180 to 300  C, 260 to 350  C, and 300 to 500  C,
respectively, although the temperature of burning wood can
reach up to 900  C. More than 30 000 chemical compounds
have been identified in wood smoke. The precise composition of
the smoke depends on the type of wood, the combustion
temperature, and oxygen availability. For meat preservation, the
compounds commonly present in the smoke that migrates into
smoked products include phenols, organic acids and furans,
carbonyls, lactones, alcohols, and esters. Of these, phenols are
particularly effective as antioxidants and microbial inhibitors.
More than 40 phenols have been isolated, including 4-methyl-
guayacol, 4-ethylguayacol, o-, m- and p-cresol, eugenol, vainillin,
dimethoxyphenol, and 1,2- and 1,4-dihydroxibenzene. All are
formed by lignin combustion at temperatures between 200 and
400  C. However, coagulation of proteins at the product surface
during smoking inhibits the diffusion of these compounds into
the product. Therefore, most of the antimicrobial compounds
remain at the product surface.
The various bacterial genera are not equally sensitive to the
compounds acquired from smoke. Escherichia coli is more
resistant to smoke components than Staphylococcus aureus. For
E. coli, 1250 ppm of smoke solids is needed to extend the lag
phase, whereas for S. aureus only 500 ppm are needed. In
addition, formaldehyde, acetic acid, and phenol derivatives in
the smoke prevent bacterial sporulation and growth. Low
smoking temperatures are sufficient to inhibit the microflora
of meat products. Indeed, smoke generated at 350  C has better
antibacterial qualities than that generated at 400  C, because
at the high temperature, phenol and carbonyl compound
production is reduced.
Cured Meats
Most cured and processed meats are ready-to-eat products.
Examples of these products include cooked ham, sausages,
bacon, and bologna. The addition of curing salts containing
nitrate, nitrate, sodium chloride, phosphates, extracts, and
flavorings inhibits the growth of bacteria. The addition of
sodium lactate reduces water activity (aw), which also inhibits
microbial growth. A subsequent heat treatment, sometimes
followed by other treatments, such as smoking or ripening,
inactivates most bacteria and enzymes.
Gram-positive bacteria, such as B. thermosphacta, LAB, and
S. aureus, as well as some lactate-sensitive gram-negative
bacteria are inhibited by curing. Although cured products
usually undergo aw and pH reductions, bacterial spoilage can
occur during processing before the aw and pH are reduced
sufficiently to prevent microbial growth. Thus, in the case of dry
cured ham, spoilage can originate in the raw meat by enter-
obacteria and Clostridium spp. that grow in the product core
before the curing salts reach the appropriate concentration to
prevent bacterial proliferation. In general, cured meat products
such as wieners, pâtés, and bologna need refrigerated storage as
they undergo spoilage at temperatures higher than 10  C.
Spoilage of cured meats can be due to greening. This is
a consequence of sulfhemoglobin formation, which is due to
a reaction between oxymyoglobin and H2S, produced by
microorganisms such as S. putrefaciens, Enterobacteriaceae, and
Lactobacillus sake.
Sausages
Because of the diversity of sausage formulations and process-
ing, the spoilage microflora of these products vary widely.
 MEAT AND POULTRY j Spoilage of Cooked Meat and Meat Products
Sausage microbial populations generally include a wide range
of microorganisms because spices and other ingredients
frequently carry their own microflora. Sausage spoilage is evi-
denced by slime formation on the casing surface, souring, and
greening. Slime starts forming as separated colonies that finally
merge. Slime-forming organisms include yeasts, LAB (Lacto-
bacillus, Enterococcus), and B. thermosphacta. Slime formation is
favored by wet surfaces. It is limited to the outside of the casing
and sometimes can be removed by hot-water washing, without
degrading the product.
Lactobacillus viridescens is frequently present in sausage
microflora, either because it survives heat processing or because
of post-process recontamination. In fact, the heat tolerance
of L. viridescens causes major hygienic problems in sausage
manufacture, because the organism has a D-value of 40 min
at 68  C.
Sausage souring occurs inside the casing because of the
growth of lactobacilli, enterococci, and related microorganisms
that possibly originate from dairy ingredients in the sausage
formulation. Souring is due to utilization of lactose and other
sugars by acid-producing microorganisms, mainly Lactobacillus
sake and L. curvatus growing on the sausage surface.
If the finish sausage is stored at high humidity and
temperature, the main spoilage microorganisms are yeasts and
bacteria, with B. thermosphacta being considered the main
spoilage microorganism. Molds seldom spoil the product
except when the surface is relatively dry, such as with dry or
semidry sausages, when growth of bacteria is prevented.
Spoilage by greening occurs in sausages as well as in cured
meats, but with sausages, it is caused by H2O2-producing
microorganisms, which result from the low oxidoreduction
potential in the sausage internal meat and which are promoted
by oxygen depletion. The microorganisms involved are
L. viridescens, Lactobacillus fructovorans, and Lactobacillus jensenii,
leuconostocs, Enterococcus faecium, and Enterococcus faecalis.
Discoloration can arise from chemical reactions promoted by
oxidants, such as hydrogen peroxide, metals, or ultraviolet light
that affect the hemopigment structure.
Finely comminuted, or emulsion, sausages of large format,
such as mortadella and bologna, are commonly spoiled by
molds that develop from spores that contaminated the raw
meat and survived cooking. An initial alteration, a slightly gray
discoloration, is observed in the batter surface where Mucor
grows, although Penicillium, Rhizopus, and Aspergillus spp. can
also be responsible. If large format sausage are stored at high
temperatures (25–35  C) or are not rapidly cooled down after
processing, spoilage can be due to bacilli and mesophilic
clostridia.
In dry sausages, the aw is considerably reduced, usually
below 0.8. This is achieved by ripening during a long period
and through the addition of large amounts of salt or salt and
nitrate. These products are stable but can be colonized by LAB,
including Leuconostoc carnosum.
Packaged Meat Products
In addition to product preparation, packaging plays an
important role in the selection of spoilage microflora, and the
sequence of events by which spoilage becomes evident. Storage
511
temperature and package atmosphere are the main factors
affecting spoilage flora development during product storage.
Meats packaged in films of high oxygen permeability
(>1000 cc m
2 atm
1 24 h
1) are mostly colonized by Aero-
monas, Enterobacter, Hafnia, B. thermosphacta, Pseudomonas, and
Proteus morganii. B. thermosphacta spoilage potential in vacuum-
packaged cooked meats is low and only related to souring,
because under anaerobic conditions, it produces lactic acid and
only small amounts of volatiles.
When vacuum-packaged meats are stored under refrigera-
tion, psychrotrophic clostridia, such as Clostridium estertheticum,
can grow with the production of CO2, which can cause pack
blowing, as well as butanol, butanoic acid, ethanol, acetic acid,
and sulfur-containing compounds. Pseudomonas is responsible
for putrid odors, but the volatiles produced appear only when
the substrates metabolize from glucose to amino acids, with
production of malodorous esters and acids.
Spoilage organisms growing on processed meats packaged
in films of low oxygen permeable (<200 cc m
2 atm
1 24 h
1),
and stored at less than 10  C, produce decoloration, milky
exudate, slime, gas, and the development of acid flavors.
This type of spoilage is mainly due to hetero- and homo-
fermentative LAB. Slime is due to dextrane production by
Leuconostoc spp. and L. sake. Greening in the inner part of the
product is mainly due to L. viridescens. Although LAB generally
do not produce off-flavors or odors, they often cause souring.
In contrast to Leuconostoc spp. that cause rapid decreases in
flavor scores before reaching their maximum numbers, Lacto-
bacillus spp. cause rapid decreases in sensory scores only when
the maximum bacterial numbers are reached.
Vacuum-packaged meat microfloras are dominated by
hetero- and homo-fermentative lactobacilli. The dominant
spoilage organism in vacuum-packaged sliced cooked beef is
L. sake, whereas L. carnosum is the dominant spoilage organism
in vacuum-packaged sliced cooked ham. Homo-fermentative
lactobacilli and leuconostocs can cause pack blowing, product
souring, and exudate formation in vacuum-packaged wieners.
Numbers of Enterobacteriaceae, B. thermosphacta, and Pseudo-
monas can be 10- to 100-fold on vacuum packaged high-pH
meat as compared to normal-pH meat. Carbon dioxide pack-
aging extends the shelf life of high-pH meat. Under this
atmosphere, the bacterial flora on both high- and normal-pH
meats is largely composed of LAB.
By the 1980s, the relationship between volatile production
and the microbial metabolism in meat substrates was fully
understood. Chemical analysis can identify the amount of
a given compound present in a product exhibiting a specific
spoilage condition, which allows for the elucidation of the
quantitative relationship between substrate consumption and
the production of individual metabolites.
In meat products packed under either aerobic or anaerobic
atmospheres, biogenic amines are formed from amino acids. The
reaction is catalyzed by decarboxylases, which are enzymes
produced by various members of the Enterobacteriaceae and
Bacillaceae, as well as species of Lactobacillus, Pedicococcus,
and Streptococcus. Pseudomonas and B. thermosphacta are decar-
boxylase-negative microorganisms. The most abundant biogenic
amines found in meat products are cadaverine, putrescine, sper-
midine, histamine, tryptamine, agmantine, ornithin, tyramine,
and spermine. The concentrations of these compounds can be
512 MEAT AND POULTRY j Spoilage of Cooked Meat and Meat Products
determined to indicate spoilage. Biosensors have been developed
to quantify biogenic amines in food products.
Chemical Spoilage
Chemical spoilage also can lead to consumer rejection of
a product. Color changes and the development of off-odors
and off-flavors from lipid degradation, that is, autooxidation or
rancidity, can occur. In some cases, microbial and chemical
spoilage develop together in meat products.
Autooxidation
Meat lipids are composed mainly of triglycerides, with small
fractions of phospholipids and cholesterol. Although antioxi-
dants are usually included in meat product formulations, fat
oxidation, mainly of unsaturated fats, occurs in the presence of
oxygen, and several species of bacteria can promote this reac-
tion. Lipid autooxidation with the development of rancidity
involves a complex sequence of chemical changes that result
from spontaneous reaction of double bonds of unsaturated
fatty acids with oxygen via free radicals reactions. During the
initial induction period, no off-odor or off-flavor is detected. At
the end of this initial stage, fat oxidation occurs rapidly, with
the liberation of odoriferous volatiles. The duration of the
second phase depends on the production of minor compo-
nents that act as prooxidants. Aldehydes are the most abun-
dantly produced compounds and include hexanal, heptanal,
octanal, nonanal, undecanal, 2-nonenal, 2-docenal, 3-hexanal,
4-decenal, 2,3-nonadienal, and 2,4-decadienal. Ketones are
also formed at the same time as aldehydes. Some of the
compounds responsible for rancid odors can be produced by
microbial activities. Diacetyl, which is formed by Pseudomonas
and, in some circumstances, by LAB, is also a lipid oxidation
product. This aroma is not acceptable in meats as it is associ-
ated with dairy products.
Temperature greatly affects the rate of lipid oxidation, with
the rate approximately doubling with each 15  C increase in
temperature. Heat treatments accelerate lipid oxidation, in
part because they promote disruption of the esters’ links to the
triglycerides with the liberation of free fatty acids that are
more reactive than the esterified acid residues. Nonetheless,
lipid oxidation can occur relatively rapidly at low tempera-
tures when fats are exposed to oxidation promoters, such as
light, metal ions, or oxidized fats, and in foods of low water
activity (aw < 0.5). Free fatty acids, both saturated and
unsaturated, undergo oxidation when heated at high
temperatures (around 200  C) in the presence of oxygen, but
they can also react in anoxic conditions to form prooxidant
monohydroxyperoxides.
Warmed-Over Flavor
A particular case of oxidation is the development of off-flavors
in chilled or frozen cooked products. This warmed-over flavor
(WOF) commonly occurs in reheated meats that were refrig-
erated for 48 h or less, and this WOF is particularly frequent in
products with a high content of polyunsaturated fatty acid.
WOF is mainly due to pentanal, hexanal, and 2,4-decadienal.
These fat-soluble molecules, formed during cooking, partition
into the melted fat where they are retained until the food is
reheated. Similar to rancidity, WOF can be prevented by the use
of synthetic antioxidants, such as butylated hydroxytoluene
(BHT) and butylated hydroxyanisole (BHA), or natural anti-
oxidants, such as vitamin E and phenols.
Discoloration and Greening
The colors of meat products can be altered by exposure to light,
oxygen, or oxidizing agents or by the presence of oxidized fat.
Greening of cured products generally takes place during
exposure to air, or after prolonged storage in oxygen-depleted
conditions. Under these conditions, H2O2 formed by some
microorganisms, such as some LAB, reacts with nitro-
sohemochrome, the pigment formed by the reaction of curing
salts and hemochromes, to produce a green oxidized porfirin.
In addition, any condition that favors the production of
hydrogen sulfide or organic sulfides will cause the development
of green color in cured meats because of the formation of
sulfmyoglobin. Another alteration of color can occur in meats
that have not been cured when they are exposed to high
temperatures, such as during barbecuing, when it is expected
that a brown, cooked color will develop. Instead, a pinkish
or reddish color develops. This coloration is due to the reaction
of meat pigments with nitrogen oxides or CO produced by
the grill, with the formation of the pink pigments nitro-
sylhemochromogen or carboxymyoglobin. A similar pinkish-
red color in some types of noncured sausages containing
paprika (Capsicum sp.) is due to small amounts of nitrite
present in the vegetable.
Lipolysis and Proteolysis
Meat lipids or proteins are degraded mainly by enzymes
produced by bacteria and only to a very small extent by
endogenous lipases or proteases. Even so, meat aging involves
endogenous as well as exogenous enzymes. However,
commercial tenderization is generally achieved by the treat-
ments, such as mechanical tenderization. In fermented
sausages, lipolysis is desirable as it contributes to flavor. Lipase
production by microorganisms is generally inhibited when
readily metabolized carbohydrates are available to the organ-
isms. Thus, it usually occurs only after other spoilage processes
are already under way.
See also: Acinetobacter; Aeromonas; Alcaligenes; Bacillus:
Introduction; Bacillus: Bacillus cereus; Geobacillus
stearothermophilus (Formerly Bacillus stearothermophilus);
Bacillus – Detection by Classical Cultural Techniques; Bacteria:
The Bacterial Cell; Bacterial Endospores; Classification of the
Bacteria: Traditional; Biochemical and Modern Identification
Techniques: Introduction; Biochemical Identification
Techniques for Foodborne Fungi: Food Spoilage Flora;
Brochothrix; Clostridium; Clostridium: Clostridium perfringens;
Clostridium: Clostridium botulinum; Dried Foods; Ecology of
Bacteria and Fungi: Influence of Available Water; Ecology of
Bacteria and Fungi in Foods: Influence of Temperature;
Ecology of Bacteria and Fungi in Foods: Influence of Redox
 MEAT AND POULTRY j Spoilage of Cooked Meat and Meat Products
Potential; Enterobacteriaceae: Coliforms and E. coli,
Introduction; Escherichia coli Detection of Enterotoxins of
E. coli; Fermented Meat Products and the Role of Starter
Cultures; Freezing of Foods: Damage to Microbial Cells; Heat
Treatment of Foods: Principles of Canning; Heat Treatment of
Foods: Spoilage Problems Associated with Canning; Heat
Treatment of Foods – Principles of Pasteurization; Heat
Treatment of Foods: Synergy Between Treatments; Hurdle
Technology; Lactobacillus: Introduction;
Lactobacillus: Lactobacillus acidophilus; The Leuconostocaceae
Family; Spoilage of Meat; Curing of Meat; Microbiology of
Sous-vide Products; Packaging of Foods; Pediococcus;
Preservatives: Traditional Preservatives – Oils and Spices;
Preservatives: Traditional Preservatives – Organic Acids;
Preservatives: Traditional Preservatives – Wood Smoke;
Permitted Preservatives: Nitrites and Nitrates; Pseudomonas:
Introduction; Pseudomonas: Pseudomonas aeruginosa;
Spoilage Problems: Problems Caused by Bacteria.
Further Reading
Borch, E., Kant-Muermansb, M.L., Blixta, Y., 1996. Bacterial spoilage of meat and
cured meat products. International Journal of Food Microbiology 33, 103–120.
Braun, P., Fehlhaber, K., Klug, C., Kop, K., 1999. Investigations into the activity of
enzymes produced by spoilage-causing bacteria: a possible basis for improved
shelf-life estimation. Food Microbiology 16, 531–540.
513
Dainty, R.H., Edwards, R.A., Hibbard, C.M., 1985. Time course of volatile compound
formation during refrigerated storage of naturally contaminated beef in air. Journal
of Applied Bacteriology 59, 303–309.
Guerrero-Legarreta, I., 2009. Meat spoilage detection. In: Nollet, L., Toldrá, F. (Eds.),
Handbook of Processed Meat and Poultry Analysis. CRC Press, Boca Raton, FL.
Guerrero-Legarreta, I., Hui, Y.H., 2010. Thermal processing. In: Guerrero-Legarreta, I.
(Ed.), Handbook of Poultry Science and Technology, vol. 1. John Wiley & Sons,
Hobonken, NJ.
Jones, R.J., 2004. Observations on the succession dynamics of lactic acid bacteria
populations in chill-stored vacuum-packaged beef. International Journal of Food
Microbiology 90, 273–282.
Lambropouloua, K.A., Drosinosa, E.H., Nychas, G.J.E., 1996. The effect of glucose
supplementation on the spoilage microflora and chemical composition of minced
beef stored aerobically or under a modified atmosphere at 4 C. International
Journal of Food Microbiology 30, 281–291.
Leistner, L., 2000. Basic aspects of food preservation by hurdle technology. Inter-
national Journal of Food Microbiology 55, 181–186.
Masana, M.O., Baranyi, J., 2000. Growth/no growth interface of Brochothrix ther-
mosphacta as function of pH and water activity. Food Microbiology 17, 485–493.
Peleg, M., 2006. It’s time to revise thermal processing theories. Food Technology
60 (7), 92.
Rousset, S., Renerre, M., 1991. Effect of CO2 or vacuum packaging on normal and high
pH meat shelf-life. International Journal of Food Science and Technology 26, 641–652.
Sikorski, Z.E., Kolakowski, E., 2010. Smoking. In: Toldrá, F. (Ed.), Handbook of Meat
Processing. Wiley, Blackwell, F. Ames, IA.
Thumel, H., 1995. Preserving meat and meat products: possible methods. Fleisch-
wirtschaft Int. 3, 3–8.
Yano, Y., Yokoyama, K., Tamiya, E., Karube, I., 1996. Direct evaluation of meat
spoilage and the progress of aging using biosensors. Analytica Chimica Acta 320
(2–3), 269–276.
Zamudio, M., 2006. Microorganismos patógenos y alternates. In: Hui, Y.H., Guerrero-
legarreta, I., Rosmini, M. (Eds.), Ciencia y Tecnología de Carnes. Noriega Editores,
Mexico City.