86
Modern Food Microbiology
organisms/cm.
71,73 Among the heterogeneous fresh-meat biota, the organisms that grow the fastest
and utilize glucose at refrigerator temperatures are the pseudomonads, and available surface O 2 has
a definite effect on their ultimate growth.
73 Brochothrix thermosphacta also utilizes glucose and
glutamate, but because of its slower growth rate, it is a poor competitor of the pseudomonads. Upon
reaching a surface population of about 10
8 /cm
2 , the supply of simple carbohydrates is exhausted,
and off-odors may or may not be evident at this point, depending on the extent to which free amino
acid utilization has occurred. Once simple carbohydrates have been exhausted, pseudomonads along
with other Gram-negative psychrotrophs such as Moraxella, Alcaligenes, Aeromonas, Serratia, and
Pantoea utilize free amino acids and related simple nitrogenous compounds as sources of energy.
Acinetobacter spp. utilize amino acids first, lactate next, and their growth is reduced at and below pH
5.7.
73 With regard to poultry, the conversion of glucose to glucsonate appears to give pseudomonads
the competitive advantage.
95
Employing lamb juice at pH 6.0 and 4
◦ C, one group of investigators suggested that the dominance
of P. fragi was due to its ability to utilize creatine and creatinine.
40 It has been observed by a number
of investigators that P. fluorescens is more abundant on fresh meats than P. fragi but that the latter
becomes dominant over time.
107
The foul odors generally associated with spoiling meats owe their origin to free amino acids and
related compounds (H 2 S from sulfur-containing amino acids, NH 3 from many amino acids, and indole
from tryptophan). Off-odors and off-flavors appear only when amino acids begin to be utilized (see
below). In the case of dark, firm, and dry (DFD) meats, which have ultimate pH > 6.0 and a considerably
lower supply of simple carbohydrates, spoilage is more rapid and off-odors are detectable with cell
numbers around 10
6 /cm
2 .
134 With normal or DFD meats, the primary proteins are not attacked until
the supply of the simpler constituents has been exhausted. It has been shown, for example, that the
antigenicity of salt-soluble beef proteins is not destroyed under the usual conditions of low-temperature
spoilage.
118
In the case of fish spoilage, it has been shown that raw fish press juice displays all the apparent
aspects of fish spoilage as may be determined by use of the whole fish.
110 This can be taken to indicate
a general lack of attack on soluble proteins by the fish-spoilage organisms because these proteins were
absent from the filtered press juice. The same is apparently true for beef and related meats. Incipient
spoilage is accompanied by a rise in pH, an increase in bacterial numbers, and an increase in the
hydration capacity of meat proteins, along with other changes. In ground beef, pH may rise as high
as 8.5 in putrid meats, although at the time of incipient spoilage, mean pH values of about 6.5 have
been found.
161 By plotting the growth curve of the spoilage biota, the usual phases of growth can be
observed and the phase of decline may be ascribed to the exhaustion of utilizable nutrients by most of
the biota and the accumulation of toxic byproducts of bacterial metabolism. Precisely how the primary
proteins of meat are destroyed at low temperatures is not well understood. For a review, see reference
91.
Dainty et al.
31 inoculated beef slime onto slices of raw beef and incubated them at 5
◦ C. Off-odors
and slime were noted after 7 days with counts at 2 × 10
9 /cm
2 . Proteolysis was not detected in either
sarcoplasmic or myofibrillar fractions of the beef slices. No changes in the sarcoplasmic fractions
could be detected even 2 days later, when bacterial numbers reached 10
10 /cm
2 . The first indication
of breakdown of myofibrillar proteins occurred at this time with the appearance of a new band and
the weakening of another. All myofibrillar bands disappeared after 11 days, with the weakening of
several bands of the sarcoplasmic fraction. With naturally contaminated beef, odors and slime were
first noted after 12 days when the numbers were 4 × 10
8 /cm
2 . Changes in myofibrillar proteins were
not noted until 18 days of holding. By the use of pure culture studies, these workers showed that
pseudomonads were active against myofibrillar proteins, whereas others were more active against
Modern Food Microbiology
organisms/cm.
71,73 Among the heterogeneous fresh-meat biota, the organisms that grow the fastest
and utilize glucose at refrigerator temperatures are the pseudomonads, and available surface O 2 has
a definite effect on their ultimate growth.
73 Brochothrix thermosphacta also utilizes glucose and
glutamate, but because of its slower growth rate, it is a poor competitor of the pseudomonads. Upon
reaching a surface population of about 10
8 /cm
2 , the supply of simple carbohydrates is exhausted,
and off-odors may or may not be evident at this point, depending on the extent to which free amino
acid utilization has occurred. Once simple carbohydrates have been exhausted, pseudomonads along
with other Gram-negative psychrotrophs such as Moraxella, Alcaligenes, Aeromonas, Serratia, and
Pantoea utilize free amino acids and related simple nitrogenous compounds as sources of energy.
Acinetobacter spp. utilize amino acids first, lactate next, and their growth is reduced at and below pH
5.7.
73 With regard to poultry, the conversion of glucose to glucsonate appears to give pseudomonads
the competitive advantage.
95
Employing lamb juice at pH 6.0 and 4
◦ C, one group of investigators suggested that the dominance
of P. fragi was due to its ability to utilize creatine and creatinine.
40 It has been observed by a number
of investigators that P. fluorescens is more abundant on fresh meats than P. fragi but that the latter
becomes dominant over time.
107
The foul odors generally associated with spoiling meats owe their origin to free amino acids and
related compounds (H 2 S from sulfur-containing amino acids, NH 3 from many amino acids, and indole
from tryptophan). Off-odors and off-flavors appear only when amino acids begin to be utilized (see
below). In the case of dark, firm, and dry (DFD) meats, which have ultimate pH > 6.0 and a considerably
lower supply of simple carbohydrates, spoilage is more rapid and off-odors are detectable with cell
numbers around 10
6 /cm
2 .
134 With normal or DFD meats, the primary proteins are not attacked until
the supply of the simpler constituents has been exhausted. It has been shown, for example, that the
antigenicity of salt-soluble beef proteins is not destroyed under the usual conditions of low-temperature
spoilage.
118
In the case of fish spoilage, it has been shown that raw fish press juice displays all the apparent
aspects of fish spoilage as may be determined by use of the whole fish.
110 This can be taken to indicate
a general lack of attack on soluble proteins by the fish-spoilage organisms because these proteins were
absent from the filtered press juice. The same is apparently true for beef and related meats. Incipient
spoilage is accompanied by a rise in pH, an increase in bacterial numbers, and an increase in the
hydration capacity of meat proteins, along with other changes. In ground beef, pH may rise as high
as 8.5 in putrid meats, although at the time of incipient spoilage, mean pH values of about 6.5 have
been found.
161 By plotting the growth curve of the spoilage biota, the usual phases of growth can be
observed and the phase of decline may be ascribed to the exhaustion of utilizable nutrients by most of
the biota and the accumulation of toxic byproducts of bacterial metabolism. Precisely how the primary
proteins of meat are destroyed at low temperatures is not well understood. For a review, see reference
91.
Dainty et al.
31 inoculated beef slime onto slices of raw beef and incubated them at 5
◦ C. Off-odors
and slime were noted after 7 days with counts at 2 × 10
9 /cm
2 . Proteolysis was not detected in either
sarcoplasmic or myofibrillar fractions of the beef slices. No changes in the sarcoplasmic fractions
could be detected even 2 days later, when bacterial numbers reached 10
10 /cm
2 . The first indication
of breakdown of myofibrillar proteins occurred at this time with the appearance of a new band and
the weakening of another. All myofibrillar bands disappeared after 11 days, with the weakening of
several bands of the sarcoplasmic fraction. With naturally contaminated beef, odors and slime were
first noted after 12 days when the numbers were 4 × 10
8 /cm
2 . Changes in myofibrillar proteins were
not noted until 18 days of holding. By the use of pure culture studies, these workers showed that
pseudomonads were active against myofibrillar proteins, whereas others were more active against