SPOILAGE, FACTORS AFFECTING
Contents
Microbiological
Oxidative and Enzymatic
Microbiological
CO Gill, Agriculture and Agri-Food Canada, Lacombe, AB, Canada
r 2014 Elsevier Ltd. All rights reserved.
This article is a revision of the previous edition article by CO Gill, volume 3,
pp 1324–1330, © 2004, Elsevier Ltd.
Glossary
Catabolite repression The quick adaptation of bacteria to
a preferred carbon and energy source through inhibition of
synthesis of enzymes involved in catabolism of carbon
sources other than the preferred one.
Gram-negative bacteria Bacteria that are decolorized
when stained with crystal violet dye after treatment with
ethanol according to Gram's procedure.
Gram-positive bacteria Bacteria that retain the crystal
violet dye on treatment with ethanol according to Gram's
procedure.
Introduction
Meats are spoiled by microorganisms when microbes on or in
the product cause changes to meat qualities that consumers
perceive as being undesirable or frankly offensive. Undesirable
or offensive changes can involve the appearance, odor, and/or
flavor of the meat. Visible changes include the appearance of
visible colonies or a layer of slime on the product surface; or
changes in the color of meat, from red to brown, gray, or
green. Changes in the odor of meat can range from strong,
putrid, or sulfurous odors to mild, stale, aromatic, or acid
odors. Flavor changes can be similarly variable, but during the
development of microbial spoilage flavor changes can often be
detected before spoilage odors are apparent.
The spoilage conditions that develop will depend on the
types of organisms that are present in the spoilage microflora.
The composition of the spoilage flora will be affected by in-
trinsic properties of the meat, such as the pH and the water
activity (aw) of the product; and by extrinsic factors, such as
the atmosphere around the product and the temperature at
which it is held. In addition, the form of spoilage that is
manifest can be affected by the amounts of specific nutrients
for some elements of the microflora that are present in the
product. As meats are not necessarily homogeneous products,
388
Partial pressure The pressure due to an individual gas in a
mixture of gases.
Spoilage flora (plural flora) A group of microorganisms
that grow on food with ultimately deleterious effects.
Water activity (aw) The ratio of vapor pressure of water in
a food or substance to that of pure water at the same
temperature.
Wiltshire bacon The pork cured by immersion in brine.
spoilage need not be uniform over all parts of an item of meat.
For example, spoilage of moist fat tissue of a meat cut may
precede spoilage of the muscle tissue. Moreover, the environ-
ment around an item of meat need not be homogenous. For
example, meat in clipped chub packs may be exposed to an
aerobic environment in the regions of the clips but be anaer-
obic elsewhere. However, spoilage of one part of an item will
usually render the whole item unacceptable.
Aerobic Spoilage of Raw Muscle Tissue
Muscle tissue in the carcass immediately after slaughter is es-
sentially sterile. The tissue is contaminated with bacteria from
the hide and from the packing plant equipment and en-
vironment during the dressing and breaking of carcasses.
Consequently, meat surfaces are contaminated with a variety
of organisms that include psychrotrophs from environmental
sources, which can grow at chiller temperatures, as well as
mesophiles derived from flora associated with animals, which
cannot grow on chilled meat. Initial numbers of bacteria on
the surfaces of meat can exceed 104 cfu cm−2. However, im-
provement of processing hygiene at packing plants in recent
Encyclopedia of Meat Sciences, Volume 3 doi:10.1016/B978-0-12-384731-7.00090-8

years has resulted in some plants at least routinely producing
carcasses and cuts with initial numbers ofo102 cfu cm−2.
Postrigor muscle tissue provides a rich medium for the
support of bacterial growth. Although the major potential
nutrient for bacteria is protein, most bacteria do not elaborate
enzymes to attack complex compounds when simple com-
pounds are readily available to support their growth. As lactic
acid, amino acids, and glucose are readily utilized by most
bacteria, and are generally abundant in muscle tissue, such
simple substances, not proteins, are the initial nutrients for the
spoilage flora (Table 1).
The accumulation of lactic acid in the muscle tissue during
the development of rigor can reduce the tissue pH to 5.5 or a
little lower. The aerobic growth of many bacteria is not af-
fected by such pH values, and the concentrations of solutes do
not reduce the water activity to values that inhibit bacteria
growth. Thus, aerobic growth of many bacteria on muscle
tissue is initially constrained by temperature alone. In these
circumstances, the organisms that can grow most rapidly at the
prevailing temperatures will tend to overgrow competitors, to
predominate in the spoilage flora.
The extent to which the fastest-growing species dominate
the flora will depend not only on the extent to which their
rates of growth exceed those of competitors, but also on the
absolute numbers of the initial flora and the initial fraction of
the potentially dominant organisms. If the initial numbers of
the flora are low, then the relatively large number of gener-
ations required before maximum numbers are attained will
allow extensive expression of a growth rate advantage. How-
ever, if the initial numbers are high, but the numbers of the
faster-growing organisms are relatively low, then the final flora
may contain relatively large fractions of slower-growing
organisms.
Under aerobic conditions, the organisms that grow best on
muscle tissue at chiller temperatures are Gram-negative, strictly
aerobic pseudomonads and moraxellaceae (Table 2). The lat-
ter group includes acinetobacteria, moraxellae, and psychro-
bacteria. Although organisms of the latter groups are usually
found in aerobic spoilage flora, they generally do not produce
offensive metabolic by-products; pseudomonads, which do
produce offensive by-products, are generally major com-
ponents of the flora at spoilage onset, and often predominant.
Consequently, aerobic spoilage at chiller temperatures is
largely the result of the activities of pseudomonads.
Table 1 Typical concentrations of low-molecular weight soluble
components of beef muscle tissue of normal pH from pasture-fed
animals
Substance Concentration (mg g−1)
Lactic acid 9.0
Creatine 5.5
Amino acids 3.5
Dipeptides 3.0
Inosine monophosphate 3.0
Nucleotides 1.0
Glycogen 1.0
Glucose 6-phosphate 0.2
Glucose 0.1
Spoilage, Factors Affecting | Microbiological 389
The pseudomonads are nutritionally versatile but generally
exhibit strong catabolite repression during the utilization of
substrates from complex media. Catabolite repression ensures
that while a preferred substrate is available, metabolic path-
ways for the utilization of other substrates are suppressed. For
pseudomonads, glucose and related substances are the pre-
ferred substrates. When these are metabolized, no by-products
that impart objectionable odors or flavors to meat are pro-
duced. However, when such substrates are exhausted amino
acids are utilized, with the production of ammonia and other
by-products, such as organic sulfides, esters, and acids, which
impart strong, putrid odors and flavors to meat.
The amounts of glucose present in muscle tissues are lim-
ited. When glucose diffusing from within a piece of muscle can
no longer meet the demand of bacteria proliferating at the
surface, then pseudomonads in the flora will attack amino
acids. When glucose is at concentrations in the tissue of ap-
proximately 0.1 mg g−1, as is typical for beef from pasture-fed
animals, this will occur when the aerobic flora numbers ap-
proach 108 cm−2. With meat from feed-lotted cattle, glucose
concentrations may exceed 1 mg g−1 and overt spoilage may
not occur until numbers are 4108 cm−2. At these high num-
bers, offensive by-products are rapidly generated in organo-
leptically detectable quantities from amino acids. Thus, in
these circumstances the onset of spoilage is abrupt, with the
tissue being wholly unspoiled when glucose is available at the
surface even though bacterial numbers are high.
The abundance of nutrients other than glucose precludes
growth of the aerobic spoilage flora being limited by the
availability of nutrients. Instead, numbers increase to exceed
109 cm−2. At these numbers, putrid spoilage is visibly aug-
mented by a layer of slime on the tissue surface. Growth of the
aerobic flora is then limited by the rate at which oxygen can
diffuse from the atmosphere into the slime layer. As catabolic
activities decline because of the increasingly limited avail-
ability of oxygen, catabolite repression is relieved, and
exoenzymes that degrade proteins and other complex sub-
strates are synthesized. Such enzymes degrade structural
elements of muscle tissue, which allows bacteria to move from
the surface into the deeper tissues, between muscle fibers.
If muscle tissue is deficient in glycogen at the time an
animal is slaughtered, then the amount of lactic acid formed
will be lower than usual, the pH of the tissue will remain high,
and little or no glucose will be present in the postrigor muscle.
The high pH does not affect the composition of the spoilage
Table 2 Rates of growth of Gram-negative bacteria from aerobic
spoilage flora on muscle tissues of normal and high pH stored in air
at 2 °C
Organisms Growth rate (generations/day)
pH 5.6 pH 6.4
Pseudomonas spp. 2.03 2.11
Moraxella spp. 1.85 1.82
Acinetobacter spp. 1.58 1.55
Flavobacterium spp. 1.18 1.14
Enterobacteriaceae 1.13 1.20
Aeromonas spp. 0.96 1.36
390 Spoilage, Factors Affecting | Microbiological
flora. However, in the near or total absence of glucose, the
pseudomonads will degrade amino acids at an early stage of
spoilage flora development. At first, the amounts of offensive
by-products produced by the relatively few bacteria are
undetectable organoleptically. However, as the flora increases,
offensive by-products accumulate until putrid spoilage is ap-
parent when numbers are approximately 106 cm−2. Therefore,
the deficiency of glucose in muscle tissue of high pH results in
the meat being prone to early spoilage.
Psychotrophic pseudomonads usually dominate aerobic
spoilage flora when meat is held at temperatures ≤20 °C. At
higher temperatures, mesophilic enterobacteria will pre-
dominate on moist meat surfaces. However, the enterobacteria
also utilize glucose preferentially, and thus the course of
spoilage with these organisms is similar to that resulting from
the activities of pseudomonads.
Aerobic Spoilage of Fat and Organ Tissues and
Minced Meats
As moisture that evaporates from fat tissue surfaces cannot be
replenished from within the tissue, fat tissue surfaces can dry
and hence preclude the growth of bacteria. However, if fat
tissues remain moist because the meat is held in a humid
environment, then an aerobic flora will develop on the fat as
on muscle tissue. Fat tissue surfaces are contaminated with
exudate, from cut blood vessels and/or muscle tissues, that
contains bacterial nutrients. However, the concentrations of
bacterial nutrients on fat surfaces are generally low and the
nutrients cannot be replenished from the underlying tissues.
Thus, glucose is rapidly exhausted, and growth continues with
the utilization of amino acids, and then lactic acid when
preferred amino acids are depleted. Consequently, putrid
spoilage becomes evident when numbers approach 106 cm−2,
as with high-pH meat. However, the total amount of nutrients
available may be inadequate for the flora to grow to numbers
at which a visible slime layer is formed. That is, growth may be
nutrient-limited rather than oxygen-limited.
Organ tissues are generally of pH46 but can contain
substantial concentrations of glucose. For example, liver can
contain glucose at concentrations up to several milligrams per
gram. Unlike muscle tissue, the tissue structures of liver and
other organs allow bacteria from the surface to invade the deep
tissues. However, the deep tissues are anaerobic, and thus
growth of bacteria within the tissues is slower, and the bacteria
growing these do not include the strictly aerobic organisms
that predominate in the flora on the surface. Spoilage at sur-
faces exposed to air will then precede spoilage of deep tissues.
Aerobic spoilage will proceed as with muscle tissue, but the
formation of visible colonies or slime may precede or be
contemporaneous with the development of spoilage odors
when glucose concentrations are high. In addition, the tissues
may be acidified, because when glucose is abundant it is
converted extracellularly by pseudomonads to gluconic and 2-
oxogluconic acids.
For minced meat products that are not preserved by high
concentrations of solutes or acidification, spoilage at surfaces
exposed to air will also precede deep spoilage, and proceed as
for muscle tissue. Again, colony or slime formation may be
among the first symptoms of spoilage, if carbohydrates pref-
erentially utilized by pseudomonads have been added to a
product.
Anaerobic Spoilage
The pigments in muscle and organ tissues – myoglobin and
hemoglobin – react readily with oxygen at all partial pressures.
Thus, when meats are sealed, with little or no headspace, in
packs composed of materials that are nearly or wholly im-
permeable to oxygen, the residual oxygen will be removed from
the meat environment quite rapidly. With raw tissues packaged
in an essentially gas-impermeable material, such as laminated
plastic films that include two layers of metalized film, anaerobic
conditions will develop and be maintained. However, vacuum
packages for meats are usually composed of plastic films with
various low, but measurable, oxygen transmission rates at
temperatures above 0 °C. In addition, some raw tissues, such
as fat, and some meat products have only limited oxygen-
scavenging capabilities. Thus, in many circumstances, the
environment at the surface of vacuum-packed product can be
microaerobic rather than anaerobic. In either environment,
growth of the strictly aerobic organisms that predominate in
aerobic spoilage flora will usually be suppressed. Instead,
spoilage flora dominated by anaerobic or facultatively anaer-
obic organisms develop. Unlike with aerobic spoilage, the types
of organisms that contribute to the spoilage flora are deter-
mined by the pH of the meat as well as the storage temperature.
Many spoilage organisms are unable to grow under anaer-
obic conditions on muscle tissue of normal pH (5.5) held at
chiller temperatures. Under these conditions, the flora that
develops is composed of Gram-positive lactic acid bacteria such
as lactobacilli, carnobacteria, and leuconostocs, with organisms
of the last group tending to predominate. The lactic acid bac-
teria are metabolically anaerobic, although they are aero-
tolerant. The substrates they can ferment to support growth on
muscle tissue are limited to glucose and some other carbo-
hydrates available in lower amounts. Thus, growth of the lactic
flora ceases when the concentration of glucose at the tissue
surface is depleted. This substrate limitation of the flora growth
typically occurs when numbers are approximately 108 cm−2.
When fermenting glucose, the lactic acid bacteria do not
produce offensive by-products. Although most lactic acid
bacteria cannot utilize amino acids to support growth, some
amino acids, notably valine and leucine, may be metabolized
with the production of volatile fatty acids as byproducts. The
slow accumulation of such substances can impart acid/dairy
flavors and, ultimately, odors to meat. Such flavors and odors
are unusual for meat rather than grossly offensive, but they
finally render the meat unacceptable to consumers some time
after the flora has reached maximum numbers. Some strains of
lactic acid bacteria can metabolize sulfur-containing amino
acids, with slow production of hydrogen sulfide. Hydrogen
sulfide can react with muscle or blood pigments to spoil the
meat by green discoloration. Hydrogen peroxide produced by
some lactic acid bacteria under microaerobic conditions can
also cause the green discoloration of fresh and cured meats.
If the pH of the meat is above 5.8, facultative anaerobes of
high spoilage potential can grow on products held under

anaerobic conditions at chiller temperatures. Such organisms
include psychrotophic enterobacteria, Shewanella putrefaciens,
and Brochothrix thermosphacta.
Under anaerobic conditions, the enterobacteria will fer-
ment glucose while it is available, and then utilize amino acids
when glucose is exhausted. Some amino acids are dec-
arboxylated to give malodorous amines, while hydrogen sul-
fide as well as organic sulfides may be produced from others.
All such by-products grossly affect the odor and flavor of meat,
and hydrogen sulfide can cause green discoloration.
Shewanella putrefaciens can form part of an aerobic spoilage
flora, in which its behavior is similar to that of the pseudo-
monads. However, unlike the pseudomonads, it utilizes the
amino acids serine and cysteine even when glucose is available.
Hydrogen sulfide and organic sulfides derived from the latter
substrate contribute to spoilage odors and flavors. The organism
is not fermentative, but under anaerobic conditions it can
utilize a variety of terminal electron acceptors other than oxygen
to maintain respiratory metabolism. Under anaerobic con-
ditions, hydrogen sulfide is produced in abundance, with con-
sequent degradation of the color, odor, and flavor of product.
Brochothrix thermosphacta ferments glucose to lactic acid,
and therefore under strictly anaerobic conditions its spoilage
potential is limited. Under aerobic conditions, glucose is me-
tabolized to acetoin, diacetyl, and a variety of fatty acids and
alcohols. These products of aerobic metabolism impart strong,
stale, and sour odors and flavors to meat. Thus, under con-
ditions where some aerobic metabolism is maintained, these
by-products can spoil meat.
Unlike pseudomonads, enterobacteria, and lactic acid
bacteria, which produce offensive by-products only when
preferred carbohydrate substrates are unavailable, B. thermo-
sphacta and S. putreficiens can produce offensive by-products at
all times during their growth on meat. Therefore, even when
the numbers of these organisms are less than 106 cm−2, of-
fensive by-products may be produced in detectable quantities
to spoil the meat, irrespective of the state of growth of the
spoilage flora as a whole.
However, the maximum numbers of the potent spoilage
organisms in an anaerobic flora are usually constrained by the
lactic acid bacteria, which sequester nutrients and produce
inhibitory bacteriocins. The inhibition of other organisms by
lactic acid bacteria occurs only as the flora approaches its
maximum numbers. Before that, the various types of bacteria
grow at rates that are determined by the temperature and the
environment provided by the meat, without any obvious
interactions between types of bacteria. Thus, whether or not
the potent spoilage organisms contribute to the spoilage of
anaerobically stored meat, when pH does not inhibit their
growth, will depend on their numbers in the initial flora. If
their numbers are low relative to the numbers of lactic acid
bacteria, growth of the potent spoilage organisms can be
suppressed before they reach numbers sufficient to elaborate
offensive by-products in detectable quantities; but if their
numbers are relatively high, they will reach numbers sufficient
to cause spoilage before growth ceases.
Although lactic acid bacteria, particularly leuconostocs,
have a growth rate advantage at chiller temperatures, that
advantage reduces at increasing temperatures (Table 3). At
abusive temperatures, enterobacteria and B. thermosphacta can
Spoilage, Factors Affecting | Microbiological 391
Table 3 Rates of anaerobic growth of bacteria from anaerobic
spoilage flora at abusive and warm temperatures
Organism(s) Growth rate (generations/day)
10 °C 20 °C 30 °C
Leuconostoc spp. 3.9 10.4 15.0
Enterobacter spp. 2.8 10.9 12.6
Brochrothrix thermosphacta 2.5 14.1 15.7
Escherichia coli 1.9 11.4 17.1
compete effectively with the lactic acid bacteria; and at warm
temperatures, anaerobic flora can be dominated by
enterobacteria.
In addition to the usual microbial spoilage conditions
of vacuum-packed meats, both raw and cooked meats may
be spoiled by psychrotrophic clostridia. A number of species
can apparently be involved in such spoilage, which often in-
volves some swelling (blowing) of packs. However, gross
swelling of vacuum-packed chilled meats stored for short
times at non-abusive temperatures appears to be due largely to
the fermentation of lactic acid by Clostridium estertheticum.
Other clostridia can cause softening of meat, with the release
of large volumes of exudate and the development of putrid
and sulfurous odors. The organisms responsible for the pro-
duction of the large volumes of gas and the proteolytic deg-
radation of the muscle tissue are often difficult to recover.
Usual methods for enumerating and isolating bacteria from
meat generally recover a flora of mainly lactic acid bacteria
from meat spoiled by psychrotrophic clostridia. In view of the
difficulties with their recovery and the limited understanding
of the circumstances under which they appear in meat spoilage
flora, it is possible that psychrotrophic clostridia are involved
in meat spoilage more often than is now recognized. Studies
aimed at characterizing meat spoilage flora by molecular
methods, and identifying the metabolic activities of psychro-
tolerant clostridia growing on meat, may resolve the current
uncertainties about their roles in meat spoilage.
Spoilage in Modified and Controlled-Atmosphere
Packagings
Modified-atmosphere packagings are filled with aerobic at-
mospheres that are usually rich in oxygen, and which have
concentrations of carbon dioxide (CO2) sufficient to inhibit
growth of pseudomonads. As large volumes of CO2 can dissolve
in meat, and CO2 and oxygen can exchange across packaging
films, the atmosphere can change during storage. Controlled-
atmosphere packagings are those in which a stable atmosphere
is maintained throughout storage of the product. The only
packagings of this type used with meats employ pouches made
of gas-impermeable films that are filled with an atmosphere of
CO2 to obtain an anaerobic atmosphere.
The growth rates of pseudomonads decrease with increas-
ing CO2 concentrations up to approximately 20%. Increases in
CO2 concentrations beyond that do not greatly reduce the rate
of growth provided the atmosphere is aerobic. The maximum
reduction in the rate of growth of pseudomonads is
392 Spoilage, Factors Affecting | Microbiological

Table 4 Examples of conditions tolerated by spoilage organisms growing on meats

Organisms Conditions

Minimum aw Minimum pH Maximum salt Maximum sorbate

concentration (%) concentration (ppm)

Gram-negative bacteria 0.95 4.4 10 100

Gram-positive bacteria 0.90 3.8 15 700
Yeasts 0.80 2.0 20 400
Molds 0.75 1.7 o20 1000

approximately 50%. A reduction of that order is sufficient to Table 5 Growth rates of bacteria, yeasts, and molds at 0 °C and
allow lactic acid bacteria, which are not affected by CO2 at subzero temperatures
such concentrations, to outgrow pseudomonads and dominate
the spoilage flora. However, B. thermosphacta and enter- Type of Name of organism(s) Growth rate (per day)a
organism(s)
obacteria are also unaffected by the CO2, and thus can form 0 °C −2 °C −5 °C
large fractions of the spoilage flora. In such circumstances, B.
thermosphacta can cause early spoilage of a product as the flora Bacteria Pseudomonas spp. 1.75 1.00 –
develops. Enterobacteria cause spoilage as glucose is exhausted Leuconostoc spp. 0.48 0.19 –
by the activities of the total flora. Yeasts Cryptococcus infirmo-miniatus 1.03 0.57 0.11
Cryptococcus laurentii 0.60 0.43 0.09
As a controlled atmosphere of carbon dioxide is anaerobic,
Molds Thamniduim elegans 0.67 0.50 0.03
growth of pseudomonads is totally inhibited. Such an at-
Cladosporium herbarum 0.31 0.18 0.03
mosphere also inhibits the growth of enterobacteria, raises the Penicillium hirsutum 0.35 0.17 –
minimum temperature for growth of B. thermosphacta, and Penicillium corylophilum 0.19 – –
probably affects some elements of the lactic flora. Con-
a
sequently, meat in a carbon dioxide atmosphere generally Growth rates of bacteria and yeasts are generations/day. Growth rates of molds are
supports a lactic flora and develops acid/dairy flavors only well increase in length per unit length per day of hyphae from newly germinated spores.
after the flora attains maximum numbers.

prevent bacterial growth. Most yeasts and molds can grow only
aerobically and are inhibited by relatively low concentrations
Bacterial Spoilage of Preserved Meats of carbon dioxide, and therefore atmospheres other than air
do not favor their growth. However, yeasts and molds can
Meats are preserved by drying; by the addition of salt or other
commonly tolerate lower water activities and more acidic
solutes in quantities sufficient to reduce the water activity to
conditions than spoilage bacteria, and some can grow at lower
levels at which growth of spoilage bacteria is affected; by fer-
temperatures or are less affected by preservatives than the
mentation of added carbohydrates or addition of acidulants, to
bacteria. Yeasts generally grow more rapidly than molds, and
reduce the pH; or/and by addition of antimicrobial agents, such
hence when conditions allow the growth of both, but prevent
as curing salts (nitrate/nitrite), sulfite, and benzoate. The Gram-
the growth of bacteria, spoilage will likely be caused by yeasts.
negative organisms that spoil products rapidly are mostly sus-
Spoilage by molds or yeasts is usually due to the development
ceptible to relatively mild preservative treatments (Table 4).
of visible colonies on product surfaces.
Inclusion of preferentially utilized carbohydrates in preserved
On raw meats, mold spoilage occurs when desiccation of
meats also tends to inhibit the production of ill-tasting and
the surface prevents the growth of spoilage bacteria. The sur-
malodorous byproducts. Bacterial flora of preserved meats is
faces of chilled carcasses can become desiccated and develop
then commonly dominated by Gram-positive organisms of low
mold colonies when circulating air of low humidity prevents
spoilage potential, with microbial spoilage being first manifest
the dry surfaces of muscle tissues being rehydrated by the
as slime or visible colonies, or discoloration of cured products.
water that moves from within the muscle. Fat surfaces will
However, certain preserved meats tend to develop a flora en-
obviously remain dry under such conditions and may also
riched for specific spoilage organisms and thus undergo spoil-
support mold growth.
age in a product-typical fashion. Examples of such products are
Mold spoilage also occurs on frozen raw meats that ex-
raw sausages preserved with sulfite, which are usually spoiled by
perience prolonged periods of temperature abuse. The min-
B. thermosphacta, as that organism is tolerant of the preservative,
imum temperature for growth of spoilage bacteria is
and Wiltshire bacons, which can be spoiled by the activities of
approximately −3 °C, whereas that for molds and yeast is
salt-requiring vibrios.
approximately −5 °C. It has therefore been assumed that
temperature alone can dictate mold instead of bacterial
spoilage. In fact, molds grow very slowly at −5 °C compared
Spoilage by Yeast and Molds with yeasts (Table 5), so when only temperature and the de-
pression of water activity associated with freezing affect mi-
Yeast and molds grow far more slowly than the spoilage bac- crobial growth, visible yeast colonies can be formed long
teria and thus will cause meat spoilage only when conditions before mold colonies appear. Mold colonies are the main

manifestation of spoilage when substrate limitation precludes
the formation of yeast colonies, or when surfaces desiccate to
give water activities below those tolerated by yeasts. Such
desiccation can occur by sublimation of ice from frozen tis-
sues, but in practice the appropriate conditions for mold
spoilage of frozen meat seem to arise when surfaces thaw,
perhaps cyclically, and water evaporates into the dry, refriger-
ated air.
Yeasts and mold colonies can also cause spoilage of cured
and preserved meats of low water activity, whereas raw meats
preserved by the addition of sulfite can be spoiled by fer-
mentative yeasts.
See also: Bacon Production: Bacon; Wiltshire Sides. Chemical
and Physical Characteristics of Meat: Adipose Tissue; Chemical
Composition; pH Measurement. Curing: Brine Curing of Meat; Dry.
Meat Marketing: Cold Chain. Microbiological Safety of Meat:
Hurdle Technology. Packaging: Equipment; Modified and Controlled
Atmosphere; Overwrapping; Vacuum. Refrigeration and Freezing
Technology: Applications; Principles; Thawing. Sausages, Types
of: Cooked; Dry and Semidry; Fresh
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. Cambridge, UK:
Woodhead Publishing, pp. 101–122.
Davies, A., Board, R., 1998. The Microbiology of Meat and Poultry. London: Blackie
Academic.
Spoilage, Factors Affecting | Microbiological 393
Gill, A.O., Gill, C.O., 2010. Preservative packagings for fresh meats, poultry and fin
fish. In: Han, J.H. (Ed.), Innovations in Food Packaging. Amsterdam: Elsevier,
pp. 204–226.
Gill, C.O., 1988. Microbiology of edible meat by products. In: Pearson, A.M.,
Dutson, T.R. (Eds.), Edible Meat By-Products. London: Elsevier, pp. 47–82.
Nychas, G.J.E., Douglas, L.M., Sofos, J.N., 2007. Meat, poultry and seafood. In:
Doyle, M.P., Beuchat, L.R. (Eds.), Food Microbiology. Fundamentals and
Frontiers. Washington, DC: ASM Press, pp. 105–140.
Pennacchia, C., Ercolini, D., Villani, F., 2011. Spoilage-related microbiota associated
with chilled beef stored in air or vacuum pack. Food Microbiology 28, 84–93.
Samelis, J., Kakouri, A., Rementzis, J., 2000. Selective effect of the product type and
the packaging conditions on the species of lactic acid bacteria dominating the
spoilage microbial association of cooked meats at 4 °C. Food Microbiology 17,
329–340.
Yang, X., Balamurugan, S., Gill, C.O., 2011. Effects on the development of blown
pack spoilage of the initial numbers of Clostridium estertheticum spores and
Leuconostoc mesenteroides on vacuum packed beef. Meat Science 88, 361–367.
Relevant Websites
http://www.meatupdate.csiro.au/data/Chilled_meat_for_export_02-91.pdf
Commonwealth Scientific and Industrial Research Organization (CSIRO),
Australia.
http://www.ime13.org/programs/presentations/mhardin%20presentation-mprc.pdf
IEH Laboratories.
http://www.redmeatinnovation.com.au/innovation-areas/food-safety/food-safety-
publications
Meat and Livestock Australia.
http://www.beefresearch.org/CMDocs/BeefResearch/Beef%20shelf-life.pdf
National Cattlemen's Beef Association.
http://www.scientificamerican.com/article.cfm?id=how-do-salt-and-sugar-pre
Scientific American.