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579
Journal of Food Protection, Vol. 63, No. 5, 2000, Pages 579–592
Incidence of
Salmonella
in Fish and Seafood†
MAXINE L. HEINITZ, RAMONA D. RUBLE, DEAN E. WAGNER,
AND
SITA R. TATINI*
U.S. Food and Drug Administration, 240 Hennepin Avenue, Minneapolis, Minnesota 55401-1999, USA
MS 99-344: Received 17 November 1999/Accepted 13 January 2000
ABSTRACT
Field laboratories of the U.S. Food and Drug Administration collected and tested 11,312 import and 768 domestic seafood
samples over a 9-year period (1990 to 1998) for the presence of Salmonella. The overall incidence of Salmonella was 7.2%
for import and 1.3% for domestic seafood. Nearly 10% of import and 2.8% of domestic raw seafood were positive for
Salmonella. The overall incidence of Salmonella in ready-to-eat seafood and shellfish eaten raw was 0.47% for domestic—
one shucked oyster and one shark cartilage powder. The incidence in the 2,734 ready-to-eat import seafoodwas 2.6%—cooked
shrimp, shellfish or fish paste, smoked fish, salted/dried fish, and caviar. The incidence in import shellfish consumed raw was
1% in oyster, 3.4% in clams, and 0% in mussels. The incidence in raw, import fish was 12.2%. Distribution of Salmonella in
seafood on a regional basis indicated the incidence to be highest in central Pacific and Africa and lowest in Europe/Russia
and North America (12% versus 1.6%). Data on a country basis indicated Vietnam to have the highest (30%) and Republic
of Korea the lowest (0.7%). While the most frequent serotypes in import seafood were Salmonella Weltevreden (1st), Sal-
monella Senftenberg (2nd), Salmonella Lexington, and Salmonella Paratyphi-B (3rd, equal numbers for each serotype), the
top 20 list included Salmonella Enteritidis (5th), Salmonella Newport (6th), Salmonella Thompson (7th), Salmonella Typhi-
murium (12th), and Salmonella Anatum (13th), commonly involved in foodborne illness in the United States. Because the
incidence in the present study is based on only a small fraction of the seafood imported into the United States, efforts should
be directed toward implementation of hazard analysis and critical control points to reduce the incidence of Salmonella in
seafood without relying on testing for Salmonella.
Centers for Disease Control and Prevention estimates
nontyphoidal Salmonella foodborne disease attributes to a
total of 1,341,873 cases, 15,608 hospitalizations, and 553
deaths (30.6% of total foodborne deaths) of all known food-
borne pathogens in the United States annually (61). The
incidence of Salmonella in which fish or shellfish was the
vehicle of transmission accounted for 8 of the 160 out-
breaks (7.42%) (14). The major etiological agents of sea-
foodborne disease associated with fish in the United States
are scombroid, ciguatoxin, and viruses (59).
The incidence of salmonellosis has been increasing
over the past 50 years (86), but the number of infections
that go unreported have been estimated to be between 20
and 100 times greater than the number of reported infec-
tions, resulting in an estimated 1% of the population in-
fected each year (24). It is currently estimated that the num-
ber of salmonellosis cases in the United States is 38 times
the number of reported cases (61). Archer and Kvenberg
estimated the cost of diarrheal disease and chronic health
problems and complications as sequelae to acute salmonel-
losis to be in the billions of dollars (11). They stated that
foodborne sources of Salmonella are generally preventable
and money spent on research, surveillance, and public ed-
ucation would be a small fraction of the cost otherwise
* Author for correspondence. Present address: Science advisor to the U.S.
Food and Drug Administration from Department of Food Science and
Nutrition, University of Minnesota, 1334 Eckles Avenue, St. Paul, MN
55108. Tel: 612-624-7412.
† The opinions expressed in this paper are those of the authors and not
necessarily those of the U.S. Food and Drug Administration.
borne by the economy when foodborne disease occurs. The
potential for salmonellosis to lead to reactive arthritis,
which can be chronic in nature, underscores the economic
burden foodborne salmonellosis can impose (30, 43, 56).
Few Salmonella outbreaks associated with fish or shell-
fish are documented in the literature. An outbreak of Sal-
monella Paratyphi-B in the United Kingdom associated
with a fish-and-chip shop was linked to a food handler who
was asymptomatic but confirmed to be a carrier (36). Im-
properly prepared chilled, boiled salmon was the food-poi-
soning vehicle in two successive outbreaks of Salmonella
Montevideo affecting 87 people, 4 of whom were hospi-
talized, 1 requiring an appendectomy (20). An outbreak of
Salmonella Paratyphi-B and Salmonella Litchfield was as-
sociated with smoked halibut (52). Rare Salmonella Enter-
itidis phage type 19 was linked to consumption of cooked
cockles harvested from a busy English Port (41).
The British Surveillance Group within the Public
Health Laboratory System reported the incidence of Sal-
monella in 22 of 566 raw shellfish examined, while only 1
of 774 samples of ready-to-eat seafood was positive for
Salmonella (75). Heinitz and Johnson reported a 3.2% in-
cidence of Salmonella in 156 smoked fish samples (47).
Monfort et al. reported Salmonella isolation rates of 8 to
35% (depending on the method used) from 133 bivalve
samples harvested from a more contaminated shellfish
growing area in France (64). Greenwood et al. analyzed 484
samples of shellfish, shrimp, and prawns collected from re-
tail outlets for bacteriological quality (40). No Salmonella
was isolated. Bouchriti et al. (18) reported only 5 of 66
J. Food Prot., Vol. 63, No. 5580 HEINITZ ET AL.
TABLE 1. Summary of FDA’s inspections of U.S. seafood processors.
Fiscal year
a
1990 1991 1992 1993 1994 1995 1996 1997 1998
No. firms in violation of the regulations
b
No. of firms inspected
% of firms in violation
195
815
23.9
619
3,359
18.4
499
2,171
23.0
398
1,851
21.5
512
1,487
36.3
613
1,689
33.0
959
1,804
33.0
636
2,119
30.0
2,427
4,123
58.9
a
Fiscal year is 1 October through 30 September.
b
Seafood processors were regulated under the Good Manufacturing Practice for Human Food (Code of Federal Regulations) 1990
through 1997.
TABLE 2. Incidence of Salmonella in seafood, 1990 through 1998.
Results of analysis
Type of seafood
Domestic
a
Negative Positive % positive
Import
Negative Positive % positive
All samples
Total % positive
Crab/crab products
Raw crustaceans (except crab)
b
Dried/salted seafood
Fin fish/skin fish
Other aquatic creatures
c
70
124
14
75
4
0
5
0
1
1
0.0
3.9
0.0
1.3
20.0
217
3,946
753
1,790
711
11
365
25
248
87
4.8
8.5
3.2
12.2
10.9
298
4,440
792
2,114
803
3.7
8.3
3.2
11.8
11.0
Prepared items
d
Shellfish
Smoked fish/seafood
Seafood products n.e.c.
e
Total
213
79
89
90
758
1
1
0
1
10
0.5
1.2
0.0
1.1
1.3
1,521
1,087
245
222
10,492
31
37
10
6
820
2.0
3.3
3.9
2.6
7.2
1,766
1,204
344
319
12,080
1.81
3.2
2.9
2.2
6.9
a
One sample imported from Indonesia but collected after it was in U.S. commerce and 10 U.S. samples exported and returned are
included among Domestic samples.
b
Includes raw lobster, shrimp, langostinos, prawns, and crayfish.
c
Includes raw frog/frog legs, squid, alligator, octopus, jellyfish, sea squirt, cuttlefish, sea cucumber, seahorse, and sea urchin.
d
Includes all cooked seafood (except crab), seafood cakes or balls, fish paste, breaded seafood, lox/cream cheese spread, seafood salads,
caviar, marinated seafood, and prepared entrees such as stuffed seafood, seafood with vegetables, etc.
e
Includes roe, imitation seafood, seafood mixtures, powdered fish products, and fish entrails.
Moroccan mussels were found satisfactory according to the
guidelines published by the United States National Shellfish
Sanitation Program standards, but none were positive for
Staphylococcus, Salmonella spp., or Vibrio parahaemoly-
ticus. A survey of 331 food samples including 55 seafood
in the Malaysian market place reported a 25% incidence of
Salmonella in raw prawns (4 of 16 samples positive; se-
rotypes isolated were Salmonella Blockley, Salmonella
Weltevreden, and Salmonella Agona) and shrimp paste (2
of 19 samples; serotypes isolated were Salmonella Chincol
and Salmonella Newport) (12). A study of Salmonella in
imported Moroccan food snails, Helix aspersa, reported an
incidence of 31% in 84 samples (9). Wilson studied the
bacterial quality of marine bivalve molluscs, including the
incidence of Salmonella, harvested from authorized har-
vesting beds in the United Kingdom from waters around
Northern Ireland. Of 433 shellfish samples examined, 36
(8%) were positive, 7 (2%) were in molluscs from beds
classified as category A (may go for direct consumption if
end product standard is met) (101). Andrews et al. reported
60 of 539 oyster samples (Crassostrea virginica) positive
for Salmonella, 85% of the positive samples contained ser-
ovars Salmonella Derby, Salmonella Infantis, or Salmonella
Newport (5). It is obvious that Salmonella in oysters could
contribute to Salmonella outbreaks because oysters are con-
sumed raw.
This study examines the incidence of Salmonella spp.
in fresh and saltwater fish, shellfish, crustaceans, other sea-
food and aquatic food creatures, and ready-to-eat foods
whose primary ingredient is seafood. Throughout the paper
the group will be referred to as seafood. The microbiolog-
ical analyses were conducted over the period 1990 to 1998.
MATERIALS AND METHODS
Sampling. Samples of fin fish, skin fish, shellfish, crusta-
ceans, and other aquatic creatures, or prepared seafood items in-
cluding caviar, seafood salads, and prepared entrees harvested and
processed in the United States were obtained from local seafood
processors or distributors. Samples of foreign origin were col-
lected at the consignee of the shipment. In most cases at least 15
units of product (packages or fillets) or at least 0.25 kg from each
of 15 cases were aseptically collected and sealed in individual
plastic bags from each lot sampled. In the case of a large seafood
item, such as a large top shell, geoduck, or a large eviscerated
fish, one unit was collected.
Sample preparation. Samples were prepared according to
the Bacteriological Analytical Manual, chapter 1 (6).
J. Food Prot., Vol. 63, No. 5 SALMONELLA IN FISH AND SEAFOOD 581
TABLE 3. Results of domestic samples positive for Salmonella
State Product Salmonella
serotype
Florida
Louisiana
Frozen shrimp
Frozen shrimp
Shucked oysters
Peeled crawfish
Peeled crawfish
Crawfish
Species
Species
Newport
Tennessee
Rubislaw
Rubislaw
Minnesota
Mississippi
New York
U.S. returned goods
a
Pollock fillets
Catfish nuggets
Frog legs
Shark cartilage powder
Tennessee
Species
Group C
1
Anatum
a
U.S. manufactured goods exported and returned to the United
States. The state of origin was not given. FIGURE 1. Distribution of seafood product types analyzed for
Salmonella.
FIGURE 2. Location of United States fish and seafood processors sampled and results of Salmonella analysis.
Salmonella species. The conventional Food and Drug Ad-
ministration (FDA) culture method for Salmonella spp. was used
(7). A 25-g portion of product (fish fillet, shrimp, or seafood item,
except frog legs, for which the preenrichment procedure is de-
tailed in the method) was taken from each of 15 units of the
sample. The 375-g composite was blended with lactose broth in
a blender, and the final volume was adjusted to 3,375 ml and
incubated 24 62hat358C for preenrichment followed by selec-
tive enrichment in selenite cystine and tetrathionate broths, or in
Rappaport–Vassiliadis medium and tetrathionate broth. Rappa-
port–Vassiliadis medium and tetrathionate broth was first recom-
mended for only raw shrimp in 1992 (3) and for all raw flesh
foods in 1995 (7). The selective enrichments were streaked onto
xylose lysine desoxycholate, Hektoen enteric, and bismuth sulfite
agars. Typical colonies from these plates were screened biochem-
ically and serotyped in some instances with commercial or Centers
for Disease Control antisera (Difco Laboratories, Detroit, Mich.;
Centers for Disease Control and Prevention, Atlanta, Ga.)
RESULTS AND DISCUSSION
Because of the concerns of pathogens such as Salmo-
nella, the FDA placed greater emphasis on inspection of
J. Food Prot., Vol. 63, No. 5582 HEINITZ ET AL.
TABLE 4. Summary of Salmonella isolated and ready-to-eat seafood
a
Type of
seafood No. of samples
positive Total no.
samples Country Salmonella serotype or
serogroup isolated
Cooked crab
b
4 151 Vietnam (3)
Taiwan
Paratyphi-B bioser java
Enteritidis
Groups C
1
,E
1
, and E
2
Lexington
Smoked fish 10 255 Republic of Korea
Philippines (7)
Taiwan
United Kingdom
Group B
Brunei
Senftenberg
Group D
1
,E
1
, and E
4
Newport
Weltevreden
Dried/salted fish 25 778 Hong Kong (3)
Japan (5)
Isangi
Krefeld
Group C
1
Group C
1
and E
1
Spp.
c
Philippines (6) Anatum
Hvittingfoss
Saintpaul
Tennessee
Group B and E
1
People’s Republic of China
Thailand (8) Mbandaka
Cerro
Hvittingfoss
Rissen
Senftenberg
Venezuela
Vietnam
Virchow
Weltevreden
Group B and E
1
Group B
Brunei
Senftenberg
Prepared items 31 1,550 Bolivia
Canada (2)
Gambia (2)
Enteritidis
Typhimurium
Spp.
c
Hull
Redba
Hong Kong
India
Japan (2)
Paratyphi-B
Oslo
Schwarzengrund
Spp.
c
Malaysia
People’s Republic of China (2)
Philippines (3)
Weltevreden
Albany
Derby
Paratyphi-B
Senftenberg
Taiwan (2)
Thailand (10)
Group C
1
Derby
Spp.
c
Albany
Anatum
Anfo
Enteritidis
Urbana
Weltevreden
Group B and C
1
Vietnam (4) Derby
Enteritidis
London
Thompson
Total 70 2,734 (2.6%)
a
More than one serotype or serogroup may have been isolated from a single sample.
b
Seventy-seven crab samples were raw and not included in this table.
c
Not submitted for serotyping.
J. Food Prot., Vol. 63, No. 5 SALMONELLA IN FISH AND SEAFOOD 583
seafood processors. Data on the number of domestic sea-
food processors inspected each year and the number of
firms having a violation is summarized in Table 1. The data
on violations do not distinguish between insanitary condi-
tions and inadequate labeling. On 18 December 1995, reg-
ulations were published in the Federal Register (34) that
required processors of fish and fishery products to develop
and implement hazard analysis critical control point
(HACCP) systems for the operations, effective 18 Decem-
ber 1997. The new regulations also applied to fishery ware-
houses, seafood salad manufacturers, and foreign seafood
processors. In addition, the regulations state that each sea-
food processor shall document the eight key sanitation con-
ditions and practices that are: (i) safety of water; (ii) food
contact surfaces; (iii) prevention of cross contamination;
(iv) employee hand-washing, hand-sanitizing, and toilet fa-
cilities; (v) protection from adulterants; (vi) storage and use
of toxic substances; (vii) employee health conditions; and
(viii) exclusion of pests. Because many violations are read-
ily documented from inspectional evidence without collec-
tion of a sample of product, the number of investigations
each year is much greater than the number of seafood sam-
ples collected for analysis. The number of firms inspected
increased significantly in 1998 as did the proportion of
firms in violation of the regulations (34) because FDA de-
cided that all seafood firms would be inspected each year.
The number of firms inspected also increased in 1998 be-
cause the new regulations also applied to seafood ware-
houses and seafood salad manufacturers as firms (Federal
Register). Also, in 1998 HACCP systems for seafood op-
erations as published in the Federal Register (34) became
an inspectional condition. It may be anticipated that the
number of firms in violation of the regulations willdecrease
in the coming years as firms develop and implement
HACCP plans for their seafood operations.
Field laboratories of FDA tested a total of 12,080 fish,
crustaceans, shellfish, other aquatic creatures including
squid, octopus, frogs, smoked fish, and other prepared and
ready-to-eat seafood entrees and salads for the presence of
Salmonella during 1990 to 1998. The results are summa-
rized in Table 2. The distribution of the types of products
sampled is shown in Figure 1. Salmonella was isolated
from 6.9% of all the samples. Ninety-four percent of the
samples were imported from foreign countries. The inci-
dence of Salmonella in seafood differed between products
of domestic and import origin (1.3% and 7.2%, respective-
ly). The high proportion of imported products sampled is a
result of FDA’s increased emphasis of sampling imported
seafood from certain countries or certain products (such as
shrimp) where past samplings indicated a higher probability
of finding Salmonella.
The data in Table 2 show that the incidence of Sal-
monella varied with the type of product. Raw fin fish/skin
fish had the highest incidence (12.2%). The incidence in
raw crustaceans (8.5%) and other raw aquatic creatures
(10.9%) was also high. As might be expected the processed,
prepared items (including imported, cooked shrimp) had the
lowest incidence (2%). Because most crab sold in the mar-
ket place is usually cooked, crab products were segregated
from other crustaceans in this study. FDA guidelines con-
sider a seafood product violative if Salmonella, including
Salmonella Arizonae, which is recently recognized as a
subspecies of Salmonella (57, 70–73), is detected (35) and
imported products would be detained at the port of entry
and refused admission into the U.S. commerce. Samples of
domestic origin found positive for Salmonella would be
recalled from distribution in the market place by the re-
sponsible firm. FDA regulations are based upon isolation
of viable Salmonella without quantification of the organ-
ism. Several studies have shown a relationship between in-
fective dose and severity of disease related to specific Sal-
monella serotypes (16, 31, 37, 49).
Of the 768 samples collected in the U.S., 10 were pos-
itive for Salmonella. Details of the positive samples are
summarized in Table 3. Figure 2 shows the results of anal-
ysis of domestic products by the geographic origin of the
responsible firm of the 758 samples for which the state of
origin was known. Ten of the domestic samples (U.S. man-
ufactured seafood, for which the state of origin was not
known) were exported and returned to the U.S. Another
sample included in domestic products was manufactured in
Indonesia but was already in U.S. commerce when sam-
pled. Two of the Salmonella serovars isolated from U.S.
samples (Salmonella Newport and Salmonella Anatum) ap-
pear on the Centers for Disease Control and Prevention list
of the 20 most frequently reported Salmonella serotypes
isolated from humans in 1997 (48). Other Salmonella se-
rotypes isolated were Rubislaw and Tennessee.
The overall incidence of Salmonella in samples of for-
eign origin was 7.2% (Table 2). Salmonella was isolated
from 11 of 228 (4.8%) imported crab samples. The seafood
products of greatest concern are the ready-to-eat products:
cooked crab, dried/salted seafood, smoked seafood, and
prepared items. Analytical results of ready-to-eat seafood
are summarized in Table 4. Seventy of 2,734 (2.6%) ready-
to-eat seafood were positive for Salmonella. Four of the
151 cooked crab samples were positive for Salmonella
(2.6%). Serotypes isolated from cooked, ready-to-eat crab
were Salmonella Enteritidis and Salmonella Paratyphi-B
bioser java. Salmonella Enteritidis is extremely virulent. It
was the serovar most commonly related to deaths as re-
ported by Bean et al. (14). Lee et al. report the invasive
complications of Salmonella Enteritidis, Salmonella Para-
typhi-B, and Salmonella Bovis-morbificans in seven chil-
dren (55). Taylor et al. (88) reported an outbreak of Sal-
monella Enteritidis in a nursing home which affected one
third of the residents. Seven persons were bacteremic, 11
were hospitalized, and 4 died. Possible sources of contam-
ination of the cooked crab in this study are the picking
process, cooling water or ice, or storage conditions.
In contrast, Reinhard et al. (78) reported results of 240
freshly cooked, hand-picked blue crab meat samples ana-
lyzed for Salmonella and other enteric pathogens collected
from 12 of 57 processing facilities inspected by Virginia
Department of Health. No Salmonella was found. No in-
formation was available on the Salmonella-positive cooked
crab samples in the present study to allow us to speculate
J. Food Prot., Vol. 63, No. 5584 HEINITZ ET AL.
TABLE 5. Frequency of Salmonella groups and serotypes isolated by region of the world
a
Region of the world
No.
samples
positive
Total
samples
analyzed % positive Salmonella
group isolated
Frequency
of group
isolated Serotype isolated
Frequency
of serotype
isolated
Africa 11 96 11.5 C
1
D
1
D
2
E
1
1
3
1
2
Redba
Enteritidis
Miami
Onireke
1
1
1
2
E
2
F
G
2
16
1
2
1
2
Parera
Rubislaw
Telelkebir
Hull
1
1
1
2
42
43
47
Spp.
1
1
1
1
Nairobi
Ahepe
Saka
1
1
1
Central America 26 510 5.1 B
C
1
1
4Typhimurium
Infantis
Mbandaka
Oranienburg
Oslo
1
1
1
1
1
C
2
D
1
5
1
Glostrup
Manhattan
Newport
Javiana
1
2
2
1
E
1
E
4
F
3
1
4
Anatum
Give
Weltevreden
Senftenberg
Abaetetuba
Rubislaw
1
1
1
1
1
2
G
1
H
28
43
51
Spp.
1
1
2
2
1
6
Poona
Carrau
Pomona
Houten
Harmelen
1
1
2
1
1
Central Pacific
b
152 1,213 12.5 B 17 Agona 2
C
1
16
Chester
Derby
Heidelberg
Paratyphi-B bioser java
Saintpaul
Stanley
Tennessee
1
2
1
6
3
2
1
C
2
14
Thompson
Virchow
Bovis-morbificans
Duesseldorf
Hadar
Newport
Tananarive
6
5
1
1
1
5
1
C
3
D
1
E
1
6
6
58
Brunei
Kentucky
Enteritidis
Javiana
Pullorum
Anatum
Lexington
4
1
2
2
1
3
18
E
2
E
4
16
21
7
7
10
1
London
Meleagridis
Weltevreden
Manila
Senftenberg
Orientalis
2
1
31
2
6
1
J. Food Prot., Vol. 63, No. 5 SALMONELLA IN FISH AND SEAFOOD 585
TABLE 5. Continued
Region of the world
No.
samples
positive
Total
samples
analyzed % positive Salmonella
group isolated
Frequency
of group
isolated Serotype isolated
Frequency
of serotype
isolated
30
35
43
Arizonae
Subspecies 2
Spp.
1
1
4
2
1
11
Hilversum
Houten
Arizonae
1
4
2
Eastern Caribbean
c
12 199 6.0 B
C
1
E
1
E
4
3
4
6
3
Typhimurium
Infantis
Oranienburg
Anatum
Muenster
Uganda
Senftenberg
2
2
2
1
1
1
3
F
G
2
21
Spp.
1
1
1Havana
Gwaai 1
1
Europe and Russia 5 408 1.2 B
E
1
F
1
3
1
Anatum
Weltevreden 1
1
Mexico 56 737 7.6 B
C
1
7
7
Agona
Saintpaul
Typhimurium
Bareilly
1
3
2
1
C
2
5
Ohio
Oranienburg
Tennessee
Thompson
Muenchen
1
1
2
1
2
C
3
D
1
E
1
2
1
15
Newport
Kentucky
Enteritidis
Anatum
Meleagridis
1
1
1
3
1
E
2
E
4
5
5
Weltevreden
Lanka
Newbrunswick
Newington
Cannstatt
8
3
1
1
1
F
G
1
16
1
1
1
Llandoff
Senftenberg
Rubislaw
Poona
Saphra
1
2
1
1
1
17
21
28
Arizonae
Spp.
1
1
1
4
4
Michigan
Minnesota
Pomona
Arizonae
1
1
1
4
Middle East
d
5 50 10.0 B
C
2
E
4
Spp.
2
1
2
1
Saintpaul
Hadar
Senftenberg
1
1
1
Multiple Countries
e
1 36 2.9 B 1
North America
f
7 444 1.6 B
C
1
C
2
D
1
Spp.
2
2
1
1
1
Saintpaul
Typhimurium
Thompson
Virchow
Newport
Enteritidis
1
1
1
1
1
1
J. Food Prot., Vol. 63, No. 5586 HEINITZ ET AL.
TABLE 5. Continued
Region of the world
No.
samples
positive
Total
samples
analyzed % positive Salmonella
group isolated
Frequency
of group
isolated Serotype isolated
Frequency
of serotype
isolated
South America 65 1,488 4.4 B 15 Agona
Bredeney
Heidelberg
Saintpaul
Sandiego
Typhimurium
1
1
1
1
2
2
C
1
C
2
C
3
2
5
2
Yaounde
Oranienburg
Newport
Litchfield
Kentucky
1
1
2
1
2
D
1
E
1
6
8
Enteritidis
Javiana
Mendoza
Panama
Anatum
1
3
1
1
3
E
2
E
4
F
18
3
4
2
1
Weltevreden
Newington
Senftenberg
Abaetetuba
Bullbay
Cerro
5
1
4
1
1
1
21
42
43
1
2
2
Baguida
Nairobi
Houten
Mosselbay
1
2
1
1
45
47
48
Arizonae
Spp.
1
2
1
1
9
Tornow
Phoenix
Marina
Arizonae
1
2
1
1
Southeast Asia
g
480 6,131 7.8 B 82 Agona
Derby
Heidelberg
Paratyphi-B
Paratyphi-B bioser java
Reading
4
12
1
5
19
1
C
1
95
Schleissheim
Stanley
Typhimurium
Schwarzengrund
Augustenborg
1
10
6
6
1
Bareilly
Braenderup
Infantis
Isangi
Livingstone
8
3
3
1
1
Mbandaka
Montevideo
Ohio
Oranienburg
Oslo
Potsdam
6
3
2
2
4
3
Rissen
Singapore
Tennessee
Thompson
Virchow
4
9
5
13
10
C
2
50 Albany
Blockley
Bovis-morbificans
Hadar
Muenchen
1
2
8
7
3
J. Food Prot., Vol. 63, No. 5 SALMONELLA IN FISH AND SEAFOOD 587
TABLE 5. Continued
Region of the world
No.
samples
positive
Total
samples
analyzed % positive Salmonella
group isolated
Frequency
of group
isolated Serotype isolated
Frequency
of serotype
isolated
C
3
D
1
12
22
Newport
Brunei
Emek
Kentucky
Tananarive
Enteritidis
11
6
3
1
2
17
E
1
99 Javiana
Anatum
Biafra
Lexington
London
3
2
1
14
2
E
2
E
3
21
2
Meleagridis
Muenster
Weltevreden
Lanka
Drypool
2
2
69
15
2
E
4
F
G
1
24
7
2
Krefeld
Liverpool
Senftenberg
Aberdeen
Srinagar
Poona
1
1
22
2
1
1
G
2
16
17
5
7
1
Idikan
Worthington
Hvittingfoss
Weston
Kirkee
1
3
6
1
1
18
21
30
35
2
1
4
2
Cerro
Minnesota
Kumasi
Morehead
Urbana
2
1
2
2
2
38
39
43
Arizonae
Species
2
10
7
4
33
Lansing
Anfo
Wandsworth
Houten
Arizonae
2
5
5
7
4
a
All samples were not submitted for serotyping or were not in condition for complete serotyping. More than one serogroup and/or
serotype may have been isolated from a sample. References to human salmonellosis associated with serotype isolated in this study:
Agona (84, 89); Anatum (1, 19, 68, 91); Arizonae (98); Bareilly (42, 62); Bovis-morbificans (38, 76); Chester (80); Enteritidis (28,
41, 45, 49, 50, 58, 85, 87, 93, 94); Hadar (33, 83); Heidelberg (94); Infantis (17, 68, 99); Montevideo (46); Newport (2, 53);
Oranienburg (67); Paratyphi-B (36) Paratyphi-B bioser java (29); Poona (21); Saintpaul (65); Senftenberg (51, 54, 79, 82); Stanley
(76); Thompson (87); Typhimurium (10, 25–27, 31, 39, 60, 63, 69, 83, 87, 90, 93, 94); Virchow (13, 81, 95, 96, 100); Weltevreden
(66, 38). Countries and islands included in each region of the world follow.
b
Australia, Cocos Islands, Fiji, Indonesia, Malaysia, New Zealand, New Guinea and Singapore.
c
Antilles, Aruba, Cayman Islands, Dominican Republic, Grenada, Haiti, Jamaica, Martinique, Trinidad and Tobago, and Turks and
Caicos Islands.
d
Bahrain, Greece, Israel, Kuwait, Lebanon, Oman, Saudi Arabia, Turkey and United Arab Emirates.
e
Shipping documents indicated more than one country of origin.
f
Canada and Greenland.
g
Bangladesh, Burma, Cambodia, Democratic People’s Republic of Korea, Hong Kong, India, Japan, Pakistan, People’s Republic of
China, Republic of Korea, Sri Lanka, Thailand, and Taiwan.
J. Food Prot., Vol. 63, No. 5588 HEINITZ ET AL.
TABLE 6. The 20 most frequently isolated Salmonella serotypes
from imported seafood samples 1990 to 1998
Rank Serotype Number
1
2
3
4
5
Weltevreden
Senftenberg
Lexington
Paratyphi-B
Enteritidis
117
39
32
32
26
6
7
8
9
10
Newport
Thompson
Lanka
Virchow
Hvittingfoss
22
22
18
18
17
11
12
13
14
15
16
Brunei
Typhimurium
Anatum
Derby
Arizonae
Bovis-morbificans
15
15
14
13
11
10
17
18
19
20
Stanley
Hadar
Javiana
Singapore
10
9
9
9
where the contamination of the four samples might have
occurred.
Arumugaswamy et al. expressed concern over the pres-
ence of Salmonella in shrimp paste, stating that shrimp
paste is served as a sauce and would not be subjected to
severe heat treatment prior to consumption (12).
Data in Table 4 also show that the incidence of Sal-
monella in smoked fish was 3.9%. The serovars isolated
from smoked fish, with the exception of Salmonella New-
port, are relatively rare in the United States. The incidence
of Salmonella in dried and or salted fish was 3.2%. Three
of the serotypes isolated from dried/salted fish (Salmonella
Anatum, Salmonella Mbandaka, and Salmonella Saintpaul)
appeared on the CDC’s list of 20 most frequently isolated
serotypes from humans in 1997 (48). The remaining sero-
types are rarely associated with salmonellosis in the United
States. Salmonella Brunei was associated with human ill-
ness in the U.S. only twice out of 441,863 isolates over the
period 1987 to 1997 (48). Of the prepared items in the
present study Salmonella was isolated from four fish paste
samples that may be consumed as sauce without further
heat treatment. Salmonella Enteritidis, which is extremely
virulent, was isolated from three of the fish paste samples,
as was Salmonella Thompson (on CDC’s list of 20 most
commonly isolated serotypes from humans) (48).
Other Salmonella-positive, ready-to-eat prepared items
included cooked shrimp, caviar, cooked periwinkles,
steamed fish, fish flakes, and boiled top shell. Eight pre-
pared items that may require cooking before consumption
were breaded scallops, breaded shrimp, shrimp balls,
stuffed clams, cuttlefish roll, pollack balls, stuffed fish, and
prepared smelt. It must be emphasized that none of the
Salmonella-positive products in this study entered U.S.
commerce. Foreign seafood processors who ship product to
the U.S. will now be regulated by the new seafood regu-
lations (34). Thus, one can speculate that the incidence of
Salmonella in import seafood will likely decrease as foreign
seafood processors institute HACCP plans.
Segregation of those shellfish in Table 2 that are com-
monly consumed raw or only slightly cooked showed the
following results for the presence of Salmonella: 1 of the
101 (1%) oysters were positive, 6 of 178 clams were pos-
itive (3.4%), and none of the 115 mussels were positive.
The Salmonella serotypes isolated from clams were Sal-
monella Group B, Salmonella Anfo, Salmonella Enteritidis,
Salmonella Newport, Salmonella Saintpaul, Salmonella Ty-
phimurium, and Salmonella Virchow. Andrews et al. iso-
lated Salmonella Typhimurium, Salmonella Paratyphi-B,
Salmonella Anatum, Salmonella Thompson, and Salmonel-
la Derby from hard shell clams (Quahaug, Mercenaria
mercenari) from classified shellfish-growing areas of north-
eastern U.S. (4). Isolation of virulent serotypes such as Sal-
monella Enteritidis (14) and invasive serotypes such as Sal-
monella Paratyphi-B (55) and Salmonella Virchow (92)
from seafood usually consumed raw or only slightly
warmed is alarming. Segments of the population such as
small children, very old, or immunocompromised individ-
uals should be aware of the risks of consuming raw or
slightly cooked shellfish.
The incidence of Salmonella in raw, imported crusta-
ceans was 8.5%. Of the 3,683 raw shrimp samples collect-
ed, Salmonella was isolated from 4.3% of the 47 prawns,
8.7% of the 528 lobster samples, and none of the 26 lan-
gostino samples. The terms shrimp and prawn are recog-
nized by the Food and Agricultural Organization as being
distinct species, prawns being larger than shrimp. However,
these distinctions do not apply in commerce (32). The dis-
tinction is made in this study because shipping documents
described the product more specifically. Bhaskar et al. re-
ported isolation of Salmonella from all 18 cultured shrimp
collected from an aquaculture shrimp farm situated off the
coast of southern India, suggesting that Salmonella may be
inherently associated with shrimp culture environment (15).
Another study of cultured prawns from 131 brackish water
ponds in Southeast Asia, isolated Salmonella from 16% of
the prawns examined (the most frequently isolated Salmo-
nella serotyped was Salmonella Weltevreden) (77). The au-
thors concluded that Salmonella was part of the natural flo-
ra of these farms (77). Data on whether the shrimp in the
present study were harvested from the wild or from aqua-
culture was not available nor was the exact location from
which the shrimp from India were harvested available.
However, data from this study indicate that it is possible to
achieve production of shrimp free of Salmonella.
The most frequently isolated serotypes from the coun-
tries listed in Table 5 were Salmonella Weltevreden fol-
lowed by Salmonella Senftenberg, Salmonella Lexington,
and Salmonella Paratyphi-B (Table 6). The former three are
also the top three serotypes found in a previous FDA study
reported in 1986 by Wagner and McLaughlin for all foods,
92% of which were seafood (97). Salmonella isolation rates
of 14.25% in 735 fish and 17.4% in 276 crustaceans was
reported for samples collected from fish markets in Coim-
batore, South India (44). The most commonly isolated
J. Food Prot., Vol. 63, No. 5 SALMONELLA IN FISH AND SEAFOOD 589
strains in Hatha’s study were Salmonella Typhi, Salmonella
Typhimurium, Salmonella Paratyphi-B, Salmonella Senf-
tenberg, Salmonella Weltevreden, and Salmonella Mgulani.
A study of 500 market prawn samples from the West Coast
region of India found only 5 samples (1%) positive; Sal-
monella Newport (1 sample) and Salmonella Infantis (4
samples) (74). In the present study, of the 64 samples pos-
itive for Salmonella from India, the most frequently isolated
serotypes were Salmonella Weltevreden (15), Salmonella
Lanka (14), and Salmonella Senftenberg (4). The preva-
lence of specific serotypes, especially Salmonella Typhi, in
Hatha’s study led us to speculate that some contamination
of the shrimp might have resulted from human sources such
as handling or sewage. Salmonella Typhi is only associated
with human contamination. Andrews et al. (8) reported the
relative incidence of Salmonella in frozen frog samples
from Indonesia, Bangladesh, Mexico, India, and Japan;
36%, 13%, 10%, 9%, and 0%, respectively. The most fre-
quently isolated serotypes were: Salmonella Newport, Sal-
monella Bareilly, and Salmonella Arizonae. The incidence
of Salmonella in all seafoods from Indonesia was 15%, a
considerable improvement from the results reported by An-
drews in 1977. However, Andrews only analyzed frogs (72
samples), whereas this study represents 312 samples, in-
cluding other aquatic creatures such as squid and cuttlefish.
Serotypes common to both Hatha’s study and the present
study were serovars frequently isolated from seafood from
Asian and Central Pacific in this study: Salmonella Welte-
vreden and Salmonella Senftenberg.
Table 5 also lists the incidence of Salmonella and the
serotypes isolated from all seafood sampled in this study,
grouped by region of the world and by Salmonella sero-
group. Reference is made to reported foodborne outbreaks
or human illnesses for serotypes isolated in the present
study. Data based on the regional source of seafood tested
in this study showed the highest incidence of Salmonella
from central Pacific (12.5%) and Africa (11.5%), followed
by southeast Asia (7.8%), and Mexico (7.6%). North Amer-
ica (1.6%), Europe, and Russia (1.2%) showed the lowest
incidence (Table 5). Salmonella serotypes extremely rare to
the United States, Salmonella Weltevreden and Salmonella
Lexington (48), were more frequently isolated from the
central Pacific, southeast Pacific regions, and Mexico.
Based on the examination of at least 200 samples from
each country, the incidence of Salmonella was highest in
Vietnam (32%) and lowest in the Republic of Korea
(0.7%). The incidence was 10 to 20% in Indonesia, Phil-
ippines, and India. Thailand and Mexico showed 8% inci-
dence, and it was 5% for China and Taiwan. The incidence
of Salmonella was 1.6% in Japan where raw fish (sushi) is
consumed. Perhaps this low incidence reflects their seafood
harvesting/distribution practices. As noted with Republic of
Korea, seafood with extremely low incidence can be pro-
duced.
Table 6 lists the ranking of the 20 most frequently iso-
lated Salmonella serotypes, including Salmonella Arizonae,
isolated from imported products in this study. Although
Salmonella Weltevreden is the most frequently isolated se-
rotype, it is rarely associated with foodborne disease in hu-
mans. Of those in Table 6, the most frequently encountered
serotypes isolated from humans in the U.S. are Salmonella
Enteritidis, Salmonella Typhimurium, and Salmonella
Newport (48). The top four isolates in Table 6 are very
rarely isolated from humans in the United States (,0.5%)
(48). Perhaps Salmonella Weltevreden, Salmonella Senften-
berg, Salmonella Lexington, and Salmonella Paratyphi-B
are extremely rare in human illnesses in the United States.
However, Salmonella Weltevreden was associated with hu-
man illness in other parts of the world such as Singapore.
An outbreak associated with Salmonella Weltevreden was
reported in a shipyard outbreak traced to contaminated
fruits and vegetables (66). Salmonella Weltevreden was fre-
quently isolated from seafood samples from Singapore in
the present study. However, there were many clinical iso-
lations of Salmonella Weltevreden reported from patients
in Singapore, but Salmonella Typhimurium was the most
frequently reported serovar (38).
Salmonella Enteritidis is, however, the serotype most
frequently associated with deaths in the United States. Sal-
monella Enteritidis was isolated from fish pastes that are
used as condiments, without subjecting to high heat. Some
people also consume raw clams, oysters, mussels, and fish
(as sushi). It is important to eliminate Salmonella from
these foods. Furthermore, it is extremely important to con-
trol and eliminate Salmonella in ready-to-eat seafood and
continue to reduce the incidence even in raw foods that are
cooked before consumption to prevent cross contamination
in the consumer’s kitchen. The reader should be reminded
that the sampling presented in this study represents an ex-
tremely small proportion of the seafood that is imported
into the United States. Also, the number of domestic prod-
ucts tested for Salmonella is extremely small (,90/year).
Therefore, this emphasizes the importance of the imple-
mentation of HACCP, inspection, and sampling of foreign
and domestic firms to control Salmonella hazard in seafood.
It also underscores the importance of rapid dissemination
of information during Salmonella outbreaks through the co-
operative network of state and federal agencies to enhance
traceback to the source of the food associated with the ill-
nesses (22, 23).
ACKNOWLEDGMENTS
The authors express their deep appreciation to the microbiologists in
FDA’s district and regional laboratories throughout the United States who
conducted the analyses and recorded the detailed analytical results into
FDA’s Microbiological Information System. We gratefully acknowldege
Albert Schwab and David Wieneke, FDA, for their helpful comments on
the manuscript, Magdalene D. Carolan, FDA’s Center for Drug Evaluation
and Research, for her efficient computer literature searches, the staff of
the FDA Medical Library, for assistance in gathering references for the
study, Robin Stanley, University of St. Thomas, for indexing the refer-
ences by key subjects, and Kelley Rand, University of Minnesota, for
development of a database for the references.
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