80
Modern Food Microbiology
and Rhodotorula, with C. lipolytica and C. zeylanoides being the two most abundant species in spoiled
ground beef.
89
Unlike the spoilage of fresh beef carcasses, ground beef or hamburger meat is spoiled exclusively
by bacteria, with the following genera being the most important: Pseudomonas, Alcaligenes, Acinetobacter, Moraxella, and Aeromonas. Those generally agreed to be the primary cause of spoilage
are Pseudomonas and Acinetobacter-Moraxella spp., with others playing relatively minor roles in
the process. Findings from two studies suggest that Acinetobacter and Moraxella spp. may not be as
abundant in spoiled beef as once reported.
50,51 In another study, Psychrobacter and Moraxella were
relatively abundant on fresh lamb carcasses but few were detected after carcass spoilage.
143
It should be noted that over the past 70 years, the Pseudomonas spp. have been shown to be the most
dominant spoilage bacteria of refrigerated fresh meats, poultry, and seafoods, but the true position of
the newly defined genus has been called into question by the transfer of at least 40 species to >10 new
genera (see Chapter 2). As presently defined, the genus Pseudomonas belongs to the gamma-subclass
of the Proteobacteria, and it includes P. fluorescence, P. fragi; the type species P. aeruginosa, and
others. Some of the species formerly in this genus have been transferred to the alpha-subclass of the
Proteobacteria (Brevundimonas, Devosia, Sphingomonas), while others (Acidovorax, Comamonas,
and Telluria) are now in the beta-subclass. It remains to be determined where these genera belong
among the organisms previously classified as pseudomonads. Until this is sorted out, references to
pseudomonads in this and subsequent chapters include all species of the genus Pseudomonas as defined
in the 1986 edition of Bergey’s Manual.
A study of the aerobic Gram-negative bacteria recovered from beef, lamb, pork, and fresh sausage,
revealed that all 231 polarly flagellated rods were pseudomonads and that of 110 nonmotile organisms,
61 were Moraxella and 49 were Acinetobacter.
32 The pseudomonads that cause meat spoilage at low
temperatures generally do not match the named species in Bergey’s Manual.
Numerical taxonomic studies by Shaw and Latty
156,157 led them to group most of their isolates
into four clusters based on carbon source utilization tests. Of 787 Pseudomonas strains isolated
from meats, 89.7% were identified, with 49.6% belonging to their cluster 2, 24.9% to cluster 1, and
11.1% to cluster 3.
157 The organisms in clusters 1 and 2 were nonfluorescent and eggyolk negative
and resembled P. fragi; those in cluster 3 were fluorescent and gelatinase positive. P. fluorescens
biotype I strains were represented by 3.9%, biotype III by 0.9%, and P. putida by only one strain.
The relative incidence of the clusters on beef, pork, and lamb, and on fresh and spoiled meats, was
similar.
157
Beef rounds and quarters are known to undergo deep spoilage, usually near the bone, especially the
“aitch” bone. This type of spoilage is often referred to as “bone taint” or “sours.” Only bacteria have
been implicated, with the genera Clostridium and Enterococcus being the primary causative agents.
Temperature of incubation is the primary reason that only a few genera of bacteria are found in
spoiled meats as opposed to fresh. In one study, only four of the nine genera present in fresh ground
beef could be found after the meat underwent frank spoilage at refrigerator temperatures.
93 It was noted
by Ayres
5 that after processing, more than 80% of the total population of freshly ground beef may
be composed of chromogenic bacteria, molds, yeasts, and spore-forming bacteria, but after spoilage,
only nonchromogenic, short Gram-negative rods are found. Although some of the bacteria found in
fresh meats can be shown to grow at refrigerator temperatures on culture media, they apparently lack
the capacity to compete successfully with the Pseudomonas and Acinetobacter-Moraxella types.
Beef cuts, such as steaks or roasts, tend to undergo surface spoilage; whether the spoilage organisms
are bacteria or molds depends on available moisture. Freshly cut meats stored in a refrigerator with
high humidity invariably undergo bacterial spoilage preferential to mold spoilage. The essential feature
Modern Food Microbiology
and Rhodotorula, with C. lipolytica and C. zeylanoides being the two most abundant species in spoiled
ground beef.
89
Unlike the spoilage of fresh beef carcasses, ground beef or hamburger meat is spoiled exclusively
by bacteria, with the following genera being the most important: Pseudomonas, Alcaligenes, Acinetobacter, Moraxella, and Aeromonas. Those generally agreed to be the primary cause of spoilage
are Pseudomonas and Acinetobacter-Moraxella spp., with others playing relatively minor roles in
the process. Findings from two studies suggest that Acinetobacter and Moraxella spp. may not be as
abundant in spoiled beef as once reported.
50,51 In another study, Psychrobacter and Moraxella were
relatively abundant on fresh lamb carcasses but few were detected after carcass spoilage.
143
It should be noted that over the past 70 years, the Pseudomonas spp. have been shown to be the most
dominant spoilage bacteria of refrigerated fresh meats, poultry, and seafoods, but the true position of
the newly defined genus has been called into question by the transfer of at least 40 species to >10 new
genera (see Chapter 2). As presently defined, the genus Pseudomonas belongs to the gamma-subclass
of the Proteobacteria, and it includes P. fluorescence, P. fragi; the type species P. aeruginosa, and
others. Some of the species formerly in this genus have been transferred to the alpha-subclass of the
Proteobacteria (Brevundimonas, Devosia, Sphingomonas), while others (Acidovorax, Comamonas,
and Telluria) are now in the beta-subclass. It remains to be determined where these genera belong
among the organisms previously classified as pseudomonads. Until this is sorted out, references to
pseudomonads in this and subsequent chapters include all species of the genus Pseudomonas as defined
in the 1986 edition of Bergey’s Manual.
A study of the aerobic Gram-negative bacteria recovered from beef, lamb, pork, and fresh sausage,
revealed that all 231 polarly flagellated rods were pseudomonads and that of 110 nonmotile organisms,
61 were Moraxella and 49 were Acinetobacter.
32 The pseudomonads that cause meat spoilage at low
temperatures generally do not match the named species in Bergey’s Manual.
Numerical taxonomic studies by Shaw and Latty
156,157 led them to group most of their isolates
into four clusters based on carbon source utilization tests. Of 787 Pseudomonas strains isolated
from meats, 89.7% were identified, with 49.6% belonging to their cluster 2, 24.9% to cluster 1, and
11.1% to cluster 3.
157 The organisms in clusters 1 and 2 were nonfluorescent and eggyolk negative
and resembled P. fragi; those in cluster 3 were fluorescent and gelatinase positive. P. fluorescens
biotype I strains were represented by 3.9%, biotype III by 0.9%, and P. putida by only one strain.
The relative incidence of the clusters on beef, pork, and lamb, and on fresh and spoiled meats, was
similar.
157
Beef rounds and quarters are known to undergo deep spoilage, usually near the bone, especially the
“aitch” bone. This type of spoilage is often referred to as “bone taint” or “sours.” Only bacteria have
been implicated, with the genera Clostridium and Enterococcus being the primary causative agents.
Temperature of incubation is the primary reason that only a few genera of bacteria are found in
spoiled meats as opposed to fresh. In one study, only four of the nine genera present in fresh ground
beef could be found after the meat underwent frank spoilage at refrigerator temperatures.
93 It was noted
by Ayres
5 that after processing, more than 80% of the total population of freshly ground beef may
be composed of chromogenic bacteria, molds, yeasts, and spore-forming bacteria, but after spoilage,
only nonchromogenic, short Gram-negative rods are found. Although some of the bacteria found in
fresh meats can be shown to grow at refrigerator temperatures on culture media, they apparently lack
the capacity to compete successfully with the Pseudomonas and Acinetobacter-Moraxella types.
Beef cuts, such as steaks or roasts, tend to undergo surface spoilage; whether the spoilage organisms
are bacteria or molds depends on available moisture. Freshly cut meats stored in a refrigerator with
high humidity invariably undergo bacterial spoilage preferential to mold spoilage. The essential feature