256 ◾ Fundamental Food Microbiology
concentrations of carbohydrates (ca. 1.3 mg/g glycogen, glucose, glucose-6-phosphate) with a pH
of approximately 5.5 and A W more than 0.97. Dark-firm-dry (DFD) meats have almost no carbohydrates and a pH of 6.0 or above.
To delay microbial spoilage, fresh meats are stored at refrigerated temperatures (≤5°C) unless
the facilities are not available. Thus, normally psychrotrophic bacteria are the most predominant
types in raw meat spoilage. Under aerobic storage at low temperatures, growth of psychrotrophic
aerobes and facultative anaerobes is favored. In retail-cut meats, because of a shorter generation
time, Pseudomonas spp. grows rapidly, using glucose first and then amino acids; the metabolism of
amino acids is accompanied by the production of malodorous methyl sulfides, esters, and acids. In
meats with high pH or low glucose content, or both, Acinetobacter and Moraxella, which preferentially metabolize amino acids instead of glucose, can grow rapidly and produce undesirable odors.
Spoilage by these strict aerobes in the form of off-odor is detected at a population of approximately 10 7–8 cells/cm 2 and slime at approximately 10 8–9 cells/cm 2 . The oxygenated red color of
myoglobin undergoes oxidation to produce gray or brown metmyoglobin. DFD meats are spoiled
more rapidly inasmuch as the bacteria utilize amino acids immediately because of the absence of
carbohydrates.
Refrigerated meat in a modified atmosphere, such as in a mixture of CO 2 and O 2 , favors growth
of facultative anaerobic Brochothrix thermosphacta, especially in meat with pH 6.0 or higher (DFD
meat). It metabolizes glucose to acetic acid and acetoin and leucine and valine to isovaleric and
isobutyric acids to produce off-odor (cheesy odor). Under anaerobic conditions, it metabolizes
glucose to produce small amounts of lactic acid (which is not considered a cause of spoilage).
Psychrotrophic facultative anaerobes and anaerobes can grow in vacuum-packaged meat to
produce different types of spoilage. Lactobacillus curvatus and Lab. sake metabolize glucose to
produce lactic acid and the amino acids leucine and valine to isovaleric and isobutyric acids. These
volatile fatty acids impart a cheesy odor in meat at a population level of more than 10 7–8 cells/
cm 2 . This spoilage is not considered to be highly undesirable because, after opening the package,
the odor disappears. However, when they metabolize cysteine and produce H 2 S gas, the products
have an undesirable odor and color. Heterofermentative Leuconostoc carnosum and Leu. gelidum
produce CO 2 and lactic acid, causing accumulation of gas and liquid in the package. Shewanella
putrefacience, which can grow under both aerobic and anaerobic conditions, metabolizes amino
acids (particularly cysteine) to produce methylsulfides and H 2 S in large quantities. Along with
offensive odors, they adversely affect the normal color of meats. H 2 S oxidizes myoglobin to a
form of metmyoglobin, causing a green discoloration. Facultative anaerobic Enterobacter, Serratia,
Proteus, and Hafnia species metabolize amino acids while growing in meat to produce amines,
ammonia, methylsulfides, and mercaptans and cause putrefaction. Some strains also produce H 2 S
in small amounts to cause greening of the meat. Because amines and ammonia are produced,
the pH of the meat usually changes to alkaline range, and meat can have a pinkish to red color.
Psychrotrophic Clostridium spp., such as Clostridium laramie, have been found to cause spoilage
associated with proteolysis and loss of texture of meat, accumulation of liquid in the bag, and
offensive odor, with an H 2 S smell predominating. The color of the meat becomes unusually red
initially and then changes to green (because of oxidation of myoglobin by H 2 S). Some Clostridium
spp., and probably Enterococcus, can cause spoilage of beef rounds and ham deep near the bone
designated as bone sour or bone taint.
Comminuted meats spoil more rapidly than retail cuts because they have more surface area.
Under aerobic storage, growth of aerobic bacteria (predominantly Pseudomonas spp.) causes
changes in odor, texture, color, and sliminess. The inside is initially microaerophilic (because of
dissolved oxygen from trapped air), which then changes to anaerobic, and growth of facultative
concentrations of carbohydrates (ca. 1.3 mg/g glycogen, glucose, glucose-6-phosphate) with a pH
of approximately 5.5 and A W more than 0.97. Dark-firm-dry (DFD) meats have almost no carbohydrates and a pH of 6.0 or above.
To delay microbial spoilage, fresh meats are stored at refrigerated temperatures (≤5°C) unless
the facilities are not available. Thus, normally psychrotrophic bacteria are the most predominant
types in raw meat spoilage. Under aerobic storage at low temperatures, growth of psychrotrophic
aerobes and facultative anaerobes is favored. In retail-cut meats, because of a shorter generation
time, Pseudomonas spp. grows rapidly, using glucose first and then amino acids; the metabolism of
amino acids is accompanied by the production of malodorous methyl sulfides, esters, and acids. In
meats with high pH or low glucose content, or both, Acinetobacter and Moraxella, which preferentially metabolize amino acids instead of glucose, can grow rapidly and produce undesirable odors.
Spoilage by these strict aerobes in the form of off-odor is detected at a population of approximately 10 7–8 cells/cm 2 and slime at approximately 10 8–9 cells/cm 2 . The oxygenated red color of
myoglobin undergoes oxidation to produce gray or brown metmyoglobin. DFD meats are spoiled
more rapidly inasmuch as the bacteria utilize amino acids immediately because of the absence of
carbohydrates.
Refrigerated meat in a modified atmosphere, such as in a mixture of CO 2 and O 2 , favors growth
of facultative anaerobic Brochothrix thermosphacta, especially in meat with pH 6.0 or higher (DFD
meat). It metabolizes glucose to acetic acid and acetoin and leucine and valine to isovaleric and
isobutyric acids to produce off-odor (cheesy odor). Under anaerobic conditions, it metabolizes
glucose to produce small amounts of lactic acid (which is not considered a cause of spoilage).
Psychrotrophic facultative anaerobes and anaerobes can grow in vacuum-packaged meat to
produce different types of spoilage. Lactobacillus curvatus and Lab. sake metabolize glucose to
produce lactic acid and the amino acids leucine and valine to isovaleric and isobutyric acids. These
volatile fatty acids impart a cheesy odor in meat at a population level of more than 10 7–8 cells/
cm 2 . This spoilage is not considered to be highly undesirable because, after opening the package,
the odor disappears. However, when they metabolize cysteine and produce H 2 S gas, the products
have an undesirable odor and color. Heterofermentative Leuconostoc carnosum and Leu. gelidum
produce CO 2 and lactic acid, causing accumulation of gas and liquid in the package. Shewanella
putrefacience, which can grow under both aerobic and anaerobic conditions, metabolizes amino
acids (particularly cysteine) to produce methylsulfides and H 2 S in large quantities. Along with
offensive odors, they adversely affect the normal color of meats. H 2 S oxidizes myoglobin to a
form of metmyoglobin, causing a green discoloration. Facultative anaerobic Enterobacter, Serratia,
Proteus, and Hafnia species metabolize amino acids while growing in meat to produce amines,
ammonia, methylsulfides, and mercaptans and cause putrefaction. Some strains also produce H 2 S
in small amounts to cause greening of the meat. Because amines and ammonia are produced,
the pH of the meat usually changes to alkaline range, and meat can have a pinkish to red color.
Psychrotrophic Clostridium spp., such as Clostridium laramie, have been found to cause spoilage
associated with proteolysis and loss of texture of meat, accumulation of liquid in the bag, and
offensive odor, with an H 2 S smell predominating. The color of the meat becomes unusually red
initially and then changes to green (because of oxidation of myoglobin by H 2 S). Some Clostridium
spp., and probably Enterococcus, can cause spoilage of beef rounds and ham deep near the bone
designated as bone sour or bone taint.
Comminuted meats spoil more rapidly than retail cuts because they have more surface area.
Under aerobic storage, growth of aerobic bacteria (predominantly Pseudomonas spp.) causes
changes in odor, texture, color, and sliminess. The inside is initially microaerophilic (because of
dissolved oxygen from trapped air), which then changes to anaerobic, and growth of facultative