364 Modern Food Microbiology
to be Leuconostoc mesenteroides, 115 were heterofermentative, and 44 were homofermentative lactobacilli. Using high-barrier oxygen film, the dominant biota of vacuum-packaged beef loin steaks
after 12 and 24 days consisted of heterofermentative lactobacilli, with Lactobacillus cellobiosus being
isolated from 92% of the steaks.
90 In 59% of the samples, L. cellobiosus constituted 50% or more of
the biota. The latter investigators found that when medium-oxygen-barrier film was used, high percentages of organisms such as Aeromonas, Enterobacter, Hafnia, B. thermosphacta, pseudomonads,
and Morganella morganii were usually found.
When high concentrations of nitrites are present, they generally inhibit B. thermosphacta and
psychrotrophic Enterobacteriaceae, and the lactic acid bacteria become dominant because they are
relatively insensitive to nitrites.
69 However, low concentrations of nitrites appear not to affect B. thermosphacta growth, especially in cooked, vacuum-packaged products. When Egan et al.
19 inoculated
this organism and a homo- and a heterofermentative lactobacillus into corned beef and sliced ham
containing 240 ppm nitrate and 20 ppm nitrite, B. thermosphacta grew with no detectable lag phase. It
had a generation time of 12–16 hours at 5
◦ C, whereas the generation time for the heterofermentative
lactobacillus was 13–16 hours and 18–22 hours for the homofermentative. Times to reach 10
8 cells/g
were 9, 9–12, and 12–20 days, respectively. Although off-flavors developed 2–3 days after the numbers
attained 10
8 /g for B. thermosphacta, the same did not occur for the homo- and heterofermentative
lactobacilli until 11 and 21 days, respectively. The lactic acid bacteria are less significant than B. thermosphacta in the spoilage of vacuum-packaged luncheon meats.
20 On the other hand, this organism
has a longer lag phase and a slower growth rate than the lactobacilli.
31 When the two groups are present
in equal numbers, the lactobacilli generally dominate. In a study of spoiled vacuum-packed smoked
Vienna sausage, 540 isolates were examined and 58% were homofermentative lactics and 36.3% were
leuconostocs, and they attained numbers of 10
7 –10
8 /g of spoiled product.
91 No carnobacters were
found in these products.
It appears that at least two Leuconostoc spp. are uniquely adapted to vacuum-packaged and MAP
meats: L. carnosum and L. gelidum. Unnamed Leuconostoc spp. were found in one study of loins
packaged under high O 2 and CO 2 to constitute from 88% to 100% of the biota
78 and to be the
dominant members of the biota in another similar study.
40 Following an extensive study of lactic acid
bacteria isolated from vacuum-packaged meats, L. carnosum and L. geldium were established.
81 Both
species grow at 1
◦ C but not at 37
◦ C, and both produce gas from glucose. In spoiled vacuum-packaged,
sliced, cooked ham, Leuconostoc carnosum was found to be the specific spoilage organism.
5
The genus Carnobacterium is important in the spoilage of MAP and vacuum-stored meats. These
catalase-negative bacteria are heterofermentative, produce only l(+)-lactic acid, and produce gas from
glucose (the typical heterofermentative betabacteria produce both d- and l-lactate). Prior to 1987,
the carnobacteria were regarded as being lactobacilli. Of 159 isolates of lactobacilli from vacuumpackaged beef, 115 could not be identified to species level.
46 Similar strains were isolated from vacuumpackaged beef, pork, lamb, and bacon.
81 Another group of investigators isolated similar organisms
from vacuum-packaged beef, and upon further study named these unique organisms Lactobacillus
divergens.
47 In the latter study, this organism constituted 6.7% of 120 psychrotrophic isolates, none of
which grew either at pH 3.9 or at 4
◦ C in MRS broth. Following DNA–DNA hybridization and other
studies, the genus Carnobacterium was erected, and L. divergens and two other species were placed
in the new genus.
12 C. divergens is associated with vacuum-packaged meats, and C. piscicola and C.
mobile are associated with fish and irradiated chicken, respectively. Because it does not produce H 2 S
or other foul-odor compounds, C. divergens may not be a spoilage bacterium. Indeed, it, along with the
two leuconostocs noted, has the potential of being beneficial in gas-impermeable packages, where they
may produce enough CO 2 to inhibit undesirable organisms. In spoiled packaged beef, Carnobacterium
was favored by 100% N 2 at −1
◦ C, whereas vacuum and 100% CO 2 favored leuconostocs.
71
to be Leuconostoc mesenteroides, 115 were heterofermentative, and 44 were homofermentative lactobacilli. Using high-barrier oxygen film, the dominant biota of vacuum-packaged beef loin steaks
after 12 and 24 days consisted of heterofermentative lactobacilli, with Lactobacillus cellobiosus being
isolated from 92% of the steaks.
90 In 59% of the samples, L. cellobiosus constituted 50% or more of
the biota. The latter investigators found that when medium-oxygen-barrier film was used, high percentages of organisms such as Aeromonas, Enterobacter, Hafnia, B. thermosphacta, pseudomonads,
and Morganella morganii were usually found.
When high concentrations of nitrites are present, they generally inhibit B. thermosphacta and
psychrotrophic Enterobacteriaceae, and the lactic acid bacteria become dominant because they are
relatively insensitive to nitrites.
69 However, low concentrations of nitrites appear not to affect B. thermosphacta growth, especially in cooked, vacuum-packaged products. When Egan et al.
19 inoculated
this organism and a homo- and a heterofermentative lactobacillus into corned beef and sliced ham
containing 240 ppm nitrate and 20 ppm nitrite, B. thermosphacta grew with no detectable lag phase. It
had a generation time of 12–16 hours at 5
◦ C, whereas the generation time for the heterofermentative
lactobacillus was 13–16 hours and 18–22 hours for the homofermentative. Times to reach 10
8 cells/g
were 9, 9–12, and 12–20 days, respectively. Although off-flavors developed 2–3 days after the numbers
attained 10
8 /g for B. thermosphacta, the same did not occur for the homo- and heterofermentative
lactobacilli until 11 and 21 days, respectively. The lactic acid bacteria are less significant than B. thermosphacta in the spoilage of vacuum-packaged luncheon meats.
20 On the other hand, this organism
has a longer lag phase and a slower growth rate than the lactobacilli.
31 When the two groups are present
in equal numbers, the lactobacilli generally dominate. In a study of spoiled vacuum-packed smoked
Vienna sausage, 540 isolates were examined and 58% were homofermentative lactics and 36.3% were
leuconostocs, and they attained numbers of 10
7 –10
8 /g of spoiled product.
91 No carnobacters were
found in these products.
It appears that at least two Leuconostoc spp. are uniquely adapted to vacuum-packaged and MAP
meats: L. carnosum and L. gelidum. Unnamed Leuconostoc spp. were found in one study of loins
packaged under high O 2 and CO 2 to constitute from 88% to 100% of the biota
78 and to be the
dominant members of the biota in another similar study.
40 Following an extensive study of lactic acid
bacteria isolated from vacuum-packaged meats, L. carnosum and L. geldium were established.
81 Both
species grow at 1
◦ C but not at 37
◦ C, and both produce gas from glucose. In spoiled vacuum-packaged,
sliced, cooked ham, Leuconostoc carnosum was found to be the specific spoilage organism.
5
The genus Carnobacterium is important in the spoilage of MAP and vacuum-stored meats. These
catalase-negative bacteria are heterofermentative, produce only l(+)-lactic acid, and produce gas from
glucose (the typical heterofermentative betabacteria produce both d- and l-lactate). Prior to 1987,
the carnobacteria were regarded as being lactobacilli. Of 159 isolates of lactobacilli from vacuumpackaged beef, 115 could not be identified to species level.
46 Similar strains were isolated from vacuumpackaged beef, pork, lamb, and bacon.
81 Another group of investigators isolated similar organisms
from vacuum-packaged beef, and upon further study named these unique organisms Lactobacillus
divergens.
47 In the latter study, this organism constituted 6.7% of 120 psychrotrophic isolates, none of
which grew either at pH 3.9 or at 4
◦ C in MRS broth. Following DNA–DNA hybridization and other
studies, the genus Carnobacterium was erected, and L. divergens and two other species were placed
in the new genus.
12 C. divergens is associated with vacuum-packaged meats, and C. piscicola and C.
mobile are associated with fish and irradiated chicken, respectively. Because it does not produce H 2 S
or other foul-odor compounds, C. divergens may not be a spoilage bacterium. Indeed, it, along with the
two leuconostocs noted, has the potential of being beneficial in gas-impermeable packages, where they
may produce enough CO 2 to inhibit undesirable organisms. In spoiled packaged beef, Carnobacterium
was favored by 100% N 2 at −1
◦ C, whereas vacuum and 100% CO 2 favored leuconostocs.
71