Viruses and Some Other Proven and Suspected Foodborne Biohazards 733
The bacteria most often associated with this syndrome are Morganella spp., especially M. morganii,
of which all strains appear to produce histamine at levels >5,000 ppm. Among other bacteria shown
to produce histidine decarboxylase are Raoulella planticola and R. ornithinolytica,
55 and Hafnia
alvei, Citrobacter freundii, Clostridium perfringens, Enterobacter aerogenes, Vibrio alginolyicus and
Proteus spp. A Morganella morganii isolate from temperature-abused albacore produced 5,253 ppm
histamine in a tuna fish infusion medium at 25
◦ C, and 2,769 ppm at 15
◦ C.
59 Neither growth nor
histamine production occurred at 4
◦ C. P phosphoreum produces histamine at temperatures at and
below 10
◦ C.
From room-temperature spoiled skipjack tuna, 31% of bacterial isolates produced from 100 to 400
mg/dl of histamine in broth.
83 The strong histamine formers were M. morganii,Proteus spp., and a
Raoutella sp., whereas weak formers included H. alvei and Proteus spp. Skipjack tuna spoiled in
seawater at 38
◦ C contained C. perfringens and V. alginolyticus among other histidine decarboxylase
producers.
117 A strain of M. morganii isolated from anchovies was shown to produce 2,377 ± 350 ppm
histamine in a culture medium at 37
◦ C in 24 hours.
91 This strain also produced detectable levels of
putrescine and cadaverine. From an outbreak of scombroid poisoning associated with tuna sashimi,
K. pneumoniae was recovered and shown to produce 442 mg/dl of histamine in a tuna fish infusion
broth.
102 This syndrome has been associated with foods other than scombroid fish, particularly cheeses,
including Swiss cheese, which in one case contained 187 mg/dl of histamine; the symptoms associated
with the outbreak occurred in 30 minutes to 1 hour after ingestion.
103
The number of outbreaks reported to the CDC for the years 1972–1986 were 178 with 1,096 cases
but no deaths.
26 The largest outbreaks of 51, 29, and 24 occurred in Hawaii, California, and New
York, respectively. The three most common vehicle foods were mahi mahi (66 outbreaks), tuna (42
outbreaks), and bluefish (19 outbreaks). Although fresh fish normally contains 1 mg/dl of histamine,
some may contain up to 20 mg/dl, a level that may lead to symptoms in some individuals. The FDA
hazardous level for tuna is 50 mg/dl.
26 The cooking of toxic fish may not lead to safe products.
The histamine content of stored skipjack tuna can be estimated if incubation times and temperatures
of storage are known. Frank et al.
37 found that 100 mg/dl formed in 46 hours at 70
◦ F, in 23 hours
at 90
◦ F, and in 17 hours at 100
◦ F. A nomograph was constructed over the temperature range of
70–100
◦ F, underscoring the importance of low temperatures in preventing or delaying histamine
formation. Vacuum packaging is less effective than low-temperature storage in controlling histamine
production.
114 The culture medium of choice for detecting histamine-producing bacteria is that of
Niven et al.
82
Histamine production is favored by low pH, but it occurs more when products are stored above the
refrigerator range. The lowest temperature for production of significant levels was found to be 30
◦ C
for H. alvei, C. freundii, and E. coli; and 15
◦ C for two strains of M. morganii.
6
The syndrome is contracted by eating fresh or processed fish of the type noted; symptoms occur
within minutes and for up to 3 hours after ingestion of toxic food, with most cases occurring within 1
hour. Typical symptoms consist of a flushing of the face and neck accompanied by a feeling of intense
heat and general discomfort, and diarrhea. Subsequent facial and neck rashes are common. The flush
is followed by an intense, throbbing, headache tapering to a continuous dull ache. Other symptoms
include dizziness, itching, faintness, burning of the mouth and throat, and the inability to swallow.
50
The minimum level of histamine thought necessary to cause symptoms is 100 mg/dl. Large numbers
of M. morganii in fish of the type incriminated in this syndrome and a level of histamine more than
10 mg/dl is considered significant relative to product quality.
The first 50 incidents in Great Britain occurred between 1976 and 1979, with all but 19 occurring in
1979. Canned and smoked mackerel was the most common vehicle, with bonita, sprats, and pilchards
involved in one outbreak each. The most common symptom among the 196 cases was diarrhea.
43
The bacteria most often associated with this syndrome are Morganella spp., especially M. morganii,
of which all strains appear to produce histamine at levels >5,000 ppm. Among other bacteria shown
to produce histidine decarboxylase are Raoulella planticola and R. ornithinolytica,
55 and Hafnia
alvei, Citrobacter freundii, Clostridium perfringens, Enterobacter aerogenes, Vibrio alginolyicus and
Proteus spp. A Morganella morganii isolate from temperature-abused albacore produced 5,253 ppm
histamine in a tuna fish infusion medium at 25
◦ C, and 2,769 ppm at 15
◦ C.
59 Neither growth nor
histamine production occurred at 4
◦ C. P phosphoreum produces histamine at temperatures at and
below 10
◦ C.
From room-temperature spoiled skipjack tuna, 31% of bacterial isolates produced from 100 to 400
mg/dl of histamine in broth.
83 The strong histamine formers were M. morganii,Proteus spp., and a
Raoutella sp., whereas weak formers included H. alvei and Proteus spp. Skipjack tuna spoiled in
seawater at 38
◦ C contained C. perfringens and V. alginolyticus among other histidine decarboxylase
producers.
117 A strain of M. morganii isolated from anchovies was shown to produce 2,377 ± 350 ppm
histamine in a culture medium at 37
◦ C in 24 hours.
91 This strain also produced detectable levels of
putrescine and cadaverine. From an outbreak of scombroid poisoning associated with tuna sashimi,
K. pneumoniae was recovered and shown to produce 442 mg/dl of histamine in a tuna fish infusion
broth.
102 This syndrome has been associated with foods other than scombroid fish, particularly cheeses,
including Swiss cheese, which in one case contained 187 mg/dl of histamine; the symptoms associated
with the outbreak occurred in 30 minutes to 1 hour after ingestion.
103
The number of outbreaks reported to the CDC for the years 1972–1986 were 178 with 1,096 cases
but no deaths.
26 The largest outbreaks of 51, 29, and 24 occurred in Hawaii, California, and New
York, respectively. The three most common vehicle foods were mahi mahi (66 outbreaks), tuna (42
outbreaks), and bluefish (19 outbreaks). Although fresh fish normally contains 1 mg/dl of histamine,
some may contain up to 20 mg/dl, a level that may lead to symptoms in some individuals. The FDA
hazardous level for tuna is 50 mg/dl.
26 The cooking of toxic fish may not lead to safe products.
The histamine content of stored skipjack tuna can be estimated if incubation times and temperatures
of storage are known. Frank et al.
37 found that 100 mg/dl formed in 46 hours at 70
◦ F, in 23 hours
at 90
◦ F, and in 17 hours at 100
◦ F. A nomograph was constructed over the temperature range of
70–100
◦ F, underscoring the importance of low temperatures in preventing or delaying histamine
formation. Vacuum packaging is less effective than low-temperature storage in controlling histamine
production.
114 The culture medium of choice for detecting histamine-producing bacteria is that of
Niven et al.
82
Histamine production is favored by low pH, but it occurs more when products are stored above the
refrigerator range. The lowest temperature for production of significant levels was found to be 30
◦ C
for H. alvei, C. freundii, and E. coli; and 15
◦ C for two strains of M. morganii.
6
The syndrome is contracted by eating fresh or processed fish of the type noted; symptoms occur
within minutes and for up to 3 hours after ingestion of toxic food, with most cases occurring within 1
hour. Typical symptoms consist of a flushing of the face and neck accompanied by a feeling of intense
heat and general discomfort, and diarrhea. Subsequent facial and neck rashes are common. The flush
is followed by an intense, throbbing, headache tapering to a continuous dull ache. Other symptoms
include dizziness, itching, faintness, burning of the mouth and throat, and the inability to swallow.
50
The minimum level of histamine thought necessary to cause symptoms is 100 mg/dl. Large numbers
of M. morganii in fish of the type incriminated in this syndrome and a level of histamine more than
10 mg/dl is considered significant relative to product quality.
The first 50 incidents in Great Britain occurred between 1976 and 1979, with all but 19 occurring in
1979. Canned and smoked mackerel was the most common vehicle, with bonita, sprats, and pilchards
involved in one outbreak each. The most common symptom among the 196 cases was diarrhea.
43