552 Modern Food Microbiology
aureus isolates that produced a slow, weak positive or negative coagulase reaction, and were negative
for the anaerobic fermentation of mannitol, produced SED.
33 The isolates were from poultry. From
Nigerian ready-to-eat foods, about 39% of 248 isolates were enterotoxigenic, with 44% of these
producing SED.
2 Among 449 coagulase-positive S. aureus isolates from a variety of Nigerian foods,
57%, 15%, 6%, and 5% were SEA, SEB, SED, and SEC, respectively.
99 From sheep milk, SEA and
SED constituted 35% each of 124 strains, including four coagulase-negative strains.
9 Of 48 isolates
from dairy and 134 from meat products, 46% and 49%, respectively, were enterotoxigenic,
84 and of
80 strains from food-poisoning outbreaks, 96% produced SEA.
22 SEC was produced by 67.9% of 342
isolates of both coagulase-positive and coagulase-negative species from healthy goats.
111 SEA, SEB,
and SEC were detected in the milk of 17 of 133 healthy goats.
111
In a study of S. aureus strains that produce SEH, 10 of 21 that induced emesis in monkeys but which
were negative for SEA through F produced SEH at levels from 13 to 230 ng/ml.
103 When another
set of 20 strains that were known to produce at least one SE was examined for SEH, one SEC strain
produced 142 ng/ml of SEH, and two SED strains produced 52 and 164 ng/ml, respectively.
103 An
ELISA method was developed for SEH and its minimum detection level was about 2.5 ng/ml.
Regarding the percentage of strains that are enterotoxigenic, widely different percentages have been
found depending on the source of isolates. Only 10% of 236 raw milk isolates were enterotoxigenic
22
whereas 62.5% of 200 food isolates were positive.
85 In one study, 33% of 36 food isolates were
enterotoxigenic.
97
An outbreak of 50 cases of staphylococcal food poisoning occurred in Brazil, and the vehicle food
was Minas cheese.
20 The etiologic agent was a thermostable-nuclease (TNase) positive strain of S.
aureus; and SEA, SEB, and SEC were found. Another outbreak with 328 victims was traced to raw
milk, and the etiologic agent was a TNase-negative staphylococcal species other than S. aureus.
20 The
milk contained SEC and SED, and >2 × 10
8 cfu/ml of the etiologic agent. Bovine mastitis and food
handlers appeared to be the sources of the causative organisms.
In a study of SEs from mastitic cows in Italy in 1999, the 2,343 composited quarter samples yielded
160 isolates that contained S. aureus.
23 Of the 160 isolates, 22 produced SEs with 7.5% being SED;
4.4% SEC; and 1.9% SEC and SEA. From 504 cafeteria foods examined in Spain, 19 (3.8%) yielded
SE-positive isolates with 10 of the SEs being SEC, 4 SED, 3 SEB, and 2 SEA.
100
Attempts to associate enterotoxigenicity with other biochemical properties of staphylococci such as
gelatinase, phosphatase, lysozyme, lecithinase, lipase, and DNase production or the fermentation of
various carbohydrates have been unsuccessful. Enterotoxigenic strains appear to be about the same as
other strains in these respects. Attempts to relate enterotoxigenesis with specific bacteriophage types
have been unsuccessful also. Most enterotoxigenic strains belong to phage group III, but all phage
groups are known to contain toxigenic strains. Of 54 strains from clinical specimens that produced
SEA, 5.5%, 1.9%, and 27.8% belonged, respectively, to phage groups I, II, and III, with 20.4% being
untypeable.
21 Among poultry isolates, 49% were phage nontypeable.
21 In a study of 452 strains from
meat plant workers, veterinary students, and meat plants, along with meat isolates and isolates from
meat animals, 29.6% were nontypeable and 22.5% of the typeables belonged to group III.
57 Of 230
raw milk isolates in Trinidad, 50.2% were typeable with 23.6% and 9.8% belonging to phage groups
I and III, respectively.
1
Chemical and Physical Properties
Some of the properties of SEs that have been studied are summarized in Table 23–4. All are simple
proteins which, upon hydrolysis, yield 18 amino acids, with aspartic, glutamic, lysine, and tyrosine
aureus isolates that produced a slow, weak positive or negative coagulase reaction, and were negative
for the anaerobic fermentation of mannitol, produced SED.
33 The isolates were from poultry. From
Nigerian ready-to-eat foods, about 39% of 248 isolates were enterotoxigenic, with 44% of these
producing SED.
2 Among 449 coagulase-positive S. aureus isolates from a variety of Nigerian foods,
57%, 15%, 6%, and 5% were SEA, SEB, SED, and SEC, respectively.
99 From sheep milk, SEA and
SED constituted 35% each of 124 strains, including four coagulase-negative strains.
9 Of 48 isolates
from dairy and 134 from meat products, 46% and 49%, respectively, were enterotoxigenic,
84 and of
80 strains from food-poisoning outbreaks, 96% produced SEA.
22 SEC was produced by 67.9% of 342
isolates of both coagulase-positive and coagulase-negative species from healthy goats.
111 SEA, SEB,
and SEC were detected in the milk of 17 of 133 healthy goats.
111
In a study of S. aureus strains that produce SEH, 10 of 21 that induced emesis in monkeys but which
were negative for SEA through F produced SEH at levels from 13 to 230 ng/ml.
103 When another
set of 20 strains that were known to produce at least one SE was examined for SEH, one SEC strain
produced 142 ng/ml of SEH, and two SED strains produced 52 and 164 ng/ml, respectively.
103 An
ELISA method was developed for SEH and its minimum detection level was about 2.5 ng/ml.
Regarding the percentage of strains that are enterotoxigenic, widely different percentages have been
found depending on the source of isolates. Only 10% of 236 raw milk isolates were enterotoxigenic
22
whereas 62.5% of 200 food isolates were positive.
85 In one study, 33% of 36 food isolates were
enterotoxigenic.
97
An outbreak of 50 cases of staphylococcal food poisoning occurred in Brazil, and the vehicle food
was Minas cheese.
20 The etiologic agent was a thermostable-nuclease (TNase) positive strain of S.
aureus; and SEA, SEB, and SEC were found. Another outbreak with 328 victims was traced to raw
milk, and the etiologic agent was a TNase-negative staphylococcal species other than S. aureus.
20 The
milk contained SEC and SED, and >2 × 10
8 cfu/ml of the etiologic agent. Bovine mastitis and food
handlers appeared to be the sources of the causative organisms.
In a study of SEs from mastitic cows in Italy in 1999, the 2,343 composited quarter samples yielded
160 isolates that contained S. aureus.
23 Of the 160 isolates, 22 produced SEs with 7.5% being SED;
4.4% SEC; and 1.9% SEC and SEA. From 504 cafeteria foods examined in Spain, 19 (3.8%) yielded
SE-positive isolates with 10 of the SEs being SEC, 4 SED, 3 SEB, and 2 SEA.
100
Attempts to associate enterotoxigenicity with other biochemical properties of staphylococci such as
gelatinase, phosphatase, lysozyme, lecithinase, lipase, and DNase production or the fermentation of
various carbohydrates have been unsuccessful. Enterotoxigenic strains appear to be about the same as
other strains in these respects. Attempts to relate enterotoxigenesis with specific bacteriophage types
have been unsuccessful also. Most enterotoxigenic strains belong to phage group III, but all phage
groups are known to contain toxigenic strains. Of 54 strains from clinical specimens that produced
SEA, 5.5%, 1.9%, and 27.8% belonged, respectively, to phage groups I, II, and III, with 20.4% being
untypeable.
21 Among poultry isolates, 49% were phage nontypeable.
21 In a study of 452 strains from
meat plant workers, veterinary students, and meat plants, along with meat isolates and isolates from
meat animals, 29.6% were nontypeable and 22.5% of the typeables belonged to group III.
57 Of 230
raw milk isolates in Trinidad, 50.2% were typeable with 23.6% and 9.8% belonging to phage groups
I and III, respectively.
1
Chemical and Physical Properties
Some of the properties of SEs that have been studied are summarized in Table 23–4. All are simple
proteins which, upon hydrolysis, yield 18 amino acids, with aspartic, glutamic, lysine, and tyrosine