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CLINICAL MICROBIOLOGY REVIEWS, Apr. 2010, p. 399–411
0893-8512/10/$12.00 doi:10.1128/CMR.00059-09
Copyright © 2010, American Society for Microbiology. All Rights Reserved.
Vol. 23, No. 2
Epidemiology of Seafood-Associated Infections in the United States
Martha Iwamoto,* Tracy Ayers, Barbara E. Mahon, and David L. Swerdlow
Centers for Disease Control and Prevention, Atlanta, Georgia
INTRODUCTION .......................................................................................................................................................399
PATHOGENS RESPONSIBLE FOR SEAFOOD-ASSOCIATED INFECTIONS..............................................400
Bacteria ....................................................................................................................................................................400
Vibrio species .......................................................................................................................................................400
Salmonella.............................................................................................................................................................400
Shigella species ....................................................................................................................................................401
Clostridium botulinum..........................................................................................................................................401
Other toxin-forming bacteria ............................................................................................................................401
Viruses ......................................................................................................................................................................401
Norovirus..............................................................................................................................................................401
Hepatitis A virus .................................................................................................................................................402
Parasites...................................................................................................................................................................402
Helminths.............................................................................................................................................................402
Protozoa ...............................................................................................................................................................402
EPIDEMIOLOGY OF SEAFOOD-ASSOCIATED INFECTIONS.......................................................................403
Sources of Data and Methods...............................................................................................................................403
Summary of Seafood-Associated Outbreaks and Infections .............................................................................403
General epidemiologic characteristics .............................................................................................................403
Outbreaks and infections caused by bacteria .................................................................................................405
Outbreaks caused by viruses.............................................................................................................................408
Outbreaks caused by parasites .........................................................................................................................408
DISCUSSION ..............................................................................................................................................................408
REFERENCES ............................................................................................................................................................410
seal and whale), fish eggs (roe), and crustaceans (e.g., shrimp,
crab, and lobster). Some seafood commodities are inherently
more risky than others owing to many factors, including the
nature of the environment from which they come, their mode
of feeding, the season during which they are harvested, and
how they are prepared and served. Fish, mollusks, and crustaceans can acquire pathogens from various sources. All seafood
can be susceptible to surface or tissue contamination originating from the marine environment. Bivalve mollusks feed by
filtering large volumes of seawater. During this process, they
can accumulate and concentrate pathogenic microorganisms
that are naturally present in harvest waters, such as vibrios.
Contamination of seafood by pathogens with a human reservoir can occur when growing areas are contaminated with
human sewage. Outbreaks of seafood-associated illness linked
to polluted waters have been caused by calicivirus, hepatitis A
virus, and Salmonella enterica serotype Typhi (22, 46, 55, 64).
Identified sources of seafood contamination have included
overboard sewage discharge into harvest areas, illegal harvesting from sewage-contaminated waters, and sewage runoff from
points inland after heavy rains or flooding. Additionally, seafood may become contaminated during handling, processing,
or preparation. Contributing factors may include storage and
transportation at inappropriate temperatures, contamination
by an infected food handler, or cross-contamination through contact with contaminated seafood or seawater. Adequate cooking
kills most pathogens; however, unlike other foods, such as meat
and poultry, that are usually fully cooked, seafood is often consumed raw or prepared in ways that do not kill organisms.
INTRODUCTION
Seafood is a nutrient-rich part of a healthful diet, and seafood consumption is associated with potential health benefits,
including neurologic development during gestation and infancy
(17, 28, 31, 32) and reduced risk of heart disease (20, 37, 38,
48). Seafood consumption has increased in the United States
in recent decades, reaching a high during the past decade: the
average American now eats approximately 16.5 pounds of seafood each year, compared with 10 to 12 pounds during the
1980s (49). However, along with the nutrients and benefits
derived from seafood consumption come the potential risks of
eating contaminated seafood. Chemicals, metals, marine toxins, and infectious agents have been found in seafood. Infectious agents associated with food-borne illness include bacteria, viruses, and parasites, and the illnesses caused by these
agents range from mild gastroenteritis to life-threatening syndromes. Seafood is responsible for an important proportion of
food-borne illness and outbreaks both in the United States and
worldwide. Although seafood is also an important vehicle for
marine toxins and chemical contamination, a review of these
syndromes is beyond the scope of this article; they have been
described recently elsewhere (2, 62).
Seafood includes mollusks (e.g., oysters, clams, and mussels), finfish (e.g., salmon and tuna), marine mammals (e.g.,
* Corresponding author. Mailing address: Enteric Diseases Epidemiology Branch, CDC, 1600 Clifton Road NE, Mailstop D-63, Atlanta,
GA 30333. Phone: (404) 639-4745. Fax: (404) 639-2206. E-mail:
[email protected].
Americans are eating 65% more
seafood since the 1980's
399
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IWAMOTO ET AL.
Seafood-associated infections are caused by a variety of bacteria, viruses, and parasites. This diverse group of pathogens
results in a wide variety of clinical syndromes, each with its own
epidemiology. In this article, we review the biology, clinical
features, and public health aspects of pathogens most commonly associated with seafood. We then describe the epidemiology of seafood-associated infections in the United States,
specifically reviewing national seafood-associated outbreaks
reported to the Centers for Disease Control and Prevention
(CDC) during 1973 to 2006 to explore whether the occurrence
of outbreaks is changing, whether new sources have been
emerging, and whether prevention measures have been effective in decreasing or controlling risk.
PATHOGENS RESPONSIBLE FOR SEAFOODASSOCIATED INFECTIONS
Bacteria
Vibrio species. Vibrio organisms are Gram-negative, halophilic bacteria that are widespread and naturally present in
marine and estuarine environments. Environmental factors influence their growth, and their numbers are highest when the
water is warm. The genus Vibrio includes 30 species, of which
at least 14 are recognized as pathogenic in humans. Vibrio
infections are acquired through ingestion of contaminated seafood or through exposure of an open wound to seawater. Vibrio
parahaemolyticus and Vibrio vulnificus are the species most
commonly associated with reported infection. V. parahaemolyticus has been associated with sporadic infections and outbreaks of gastroenteritis, while V. vulnificus infections occur
almost exclusively as sporadic cases in the United States. Clinical features most often associated with V. parahaemolyticus
infection include watery diarrhea, abdominal cramps, nausea,
and vomiting; wound infections and septicemia occur less commonly (18, 39, 45). V. vulnificus is particularly virulent, especially among patients with liver disease and iron storage disorders, who are at increased risk of invasive disease (4, 33, 39).
V. vulnificus infections can lead to sepsis and severe wound
infections (33, 39, 50, 60). Severe infections, such as bloodstream and wound infections, require prompt antimicrobial
therapy. The case fatality rate is about 50% for bloodstream
infections and 25% for wound infections (21, 33, 35, 60). Laboratory diagnosis is made by isolation of the organism from
clinical specimens, including blood, stool, and wound samples.
Because they can be overlooked on standard agar plates, Vibrio
organisms in stool or wound samples are best identified on
selective media, such as thiosulfate-citrate-bile salts-sucrose
(TCBS) agar (1, 34).
Cases of Vibrio infections have a marked seasonal distribution; most occur during summer and early fall, corresponding
to the period of warmer temperatures. Almost all cases of
food-borne Vibrio infection are associated with a recent history
of seafood consumption, primarily raw oyster consumption.
Like other organisms found in water, vibrios can be concentrated in the tissues of filter-feeding bivalve mollusks. Measures to prevent food-borne Vibrio infections include consumer
education regarding the dangers of eating raw or undercooked
shellfish, particularly among persons with medical conditions,
such as liver disease, that predispose them to severe illness.
CLIN. MICROBIOL. REV.
Thoroughly cooking shellfish and preventing raw seafood from
cross-contaminating other foods are effective measures for
consumers to reduce risk (25). Regulatory control measures
have included monitoring of harvest waters and microbiological sampling of oysters. However, it is important that the presence of vibrios is not associated with fecal contamination.
Therefore, monitoring waters for fecal coliform bacteria is not
effective as an indicator of the presence of Vibrio in harvest
environments. Finally, postharvest processing methods, such as
high-pressure treatment, irradiation, quick-freezing, and pasteurization, are available to make oysters safer. Vibrio infections are reportable to state health departments, and traceback
of oysters associated with human Vibrio infection is strongly
encouraged (16).
Salmonella. Salmonellae are Gram-negative bacilli. Approximately 2,500 Salmonella serotypes have been identified, causing a variety of clinical syndromes ranging from asymptomatic
carriage to invasive disease (6). Salmonella most commonly
causes acute gastroenteritis, with symptoms including diarrhea,
abdominal cramps, and fever. Other clinical manifestations can
include enteric fever, urinary tract infections, bacteremia, and
severe focal infections. Isolation of Salmonella organisms from
cultures of stool, blood, or other clinical samples is diagnostic;
isolates are referred to public health laboratories for serotype
characterization. Salmonella is a leading cause of food-borne
illness, causing approximately 1.4 million illnesses annually in
the United States (44). Incidence is highest among infants and
the elderly, and infections are more likely to occur during
summer and early fall (52). Each Salmonella serotype has its
individual biology and ecological niche. Many natural reservoirs for the different Salmonella serotypes have been identified. Humans are the only known reservoir for Salmonella
serotype Typhi; many animal hosts (birds, reptiles, and mammals) serve as reservoirs for nontyphoidal serotypes. With improvements in sanitation over the past several decades, Salmonella serotype Typhi went from being the leading cause of
Salmonella infection to becoming relatively uncommon. However, nontyphoidal Salmonella infections have emerged as a
public health problem since the 1950s (52, 63, 64).
Routes of Salmonella transmission include food-borne and
waterborne routes, person-to-person contact, and contact with
animals, particularly reptiles. Most cases of nontyphoidal salmonellosis are caused by ingestion of contaminated food, and
outbreaks have been associated with a wide range of food
vehicles in the United States. Seafood-associated outbreaks
have been caused by fish, shrimp, oysters, and clams. Studies to
determine the prevalence of Salmonella spp. in oysters from
domestic bays and testing of sampled oysters from domestic
seafood samples by the U.S. Food and Drug Administration
(FDA) have demonstrated the presence of salmonellae in a
variety of fish and shellfish, including seafood intended for
consumption without further preparation upon distribution,
requiring minimal cooking, and shellfish eaten raw (5, 30). Fish
and shellfish can acquire Salmonella from polluted waters.
Historically, sewage contamination of shellfish harvest beds led
to large shellfish-associated outbreaks of Salmonella serotype
Typhi infections. Control measures aimed at detecting contamination of harvest waters, such as monitoring fecal coliform
counts in these waters, have been effective at reducing the risk
of Salmonella contamination of seafood occurring before har-
VOL. 23, 2010
vest. Additionally, seafood can become contaminated with Salmonella during storage and processing (7, 29). Salmonella infection can be prevented by adequate cooking, proper storage
and processing after harvest, and avoidance of cross-contamination during seafood handling (24, 25).
Shigella species. Shigella species are Gram-negative bacilli.
Four species have been identified, and clinical presentations
vary by species. Clinical manifestations of Shigella infection
range from watery, loose stools to more severe symptoms,
including fever, abdominal pain, tenesmus, and bloody diarrhea. Complications are rare and include seizures in young
children, toxic megacolon, bacteremia, Reiter’s syndrome, and
hemolytic-uremic syndrome. Diagnosis is made by isolation of
Shigella from feces or rectal swabs. Cases occur worldwide, in
endemic and epidemic forms. Most cases occur among children aged ⬍10 years.
Humans are the primary reservoir of Shigella. Transmission
occurs through direct or indirect contact with feces of infected
persons. Shigella infection is highly communicable, because
ingestion of as few as 10 viable organisms is sufficient for
infection to occur. The low infectious dose contributes to the
potential for large outbreaks. Outbreaks have been associated
with person-to-person transmission in crowded or unhygienic
environments and with ingestion of contaminated food and
water. Foods can become contaminated during handling or
preparation by an infected food handler. With seafood, contamination can occur if seafood is harvested from sewagecontaminated water, as occurred in an outbreak caused by
consumption of raw oysters harvested from waters where sewage was dumped overboard from the oyster harvest boat (57).
Shigella organisms can survive outside the host, but they are
killed readily by cooking. Control strategies to prevent shigellosis associated with seafood have included monitoring of harvest water for fecal coliforms, prohibition of harvesting from
sewage-contaminated areas, enforced control of dumping sewage overboard, and guidelines for seafood handling in restaurants.
Clostridium botulinum. Clostridium botulinum is a sporeforming, anaerobic, Gram-positive bacillus that is widespread
in the environment. The bacterium produces a potent neurotoxin under anaerobic, low-acid conditions. Seven types of
botulism toxin have been identified; toxin types A, B, and E
cause most human illnesses. Food-borne botulism is caused by
the ingestion of food contaminated with preformed toxin produced by spores of C. botulinum. Botulism is characterized by
an acute, symmetric, descending flaccid paralysis. Early signs
and symptoms of botulism often include cranial nerve palsies,
with diplopia, ptosis, slurred speech, and difficulty swallowing
progressing to descending weakness and paralysis. Symptoms
can progress to cause paralysis of the respiratory muscles,
requiring ventilatory support. Cases of botulism are rare but
serious; an estimated 60 food-borne cases occur each year in
the United States (44). Most cases are sporadic, but foodborne botulism outbreaks are reported each year.
Food-borne botulism cases are most often associated with
home-canned foods. Other food vehicles identified in outbreak
investigations have included fermented or salted seafood, potatoes baked in aluminum foil, garlic in oil, onions held under
butter, and homemade salsa (61). Most seafood-associated
cases are caused by toxin type E, which is associated most
SEAFOOD-ASSOCIATED INFECTIONS
401
commonly with eating traditional Alaska Native foods, such as
fermented salmon heads, salmon eggs, and blubber and skin
from marine animals (muktuk) (14). C. botulinum type E
spores are commonly found in fish and aquatic animals, and
implicated seafood has been fermented under anaerobic conditions that favor the germination of C. botulinum (43, 66).
Measures to prevent seafood-borne botulism have included
educational efforts to promote proper methods to ferment
foods and to boil fermented foods before consumption, especially if they were stored in tightly sealed plastic or glass containers (10).
Other toxin-forming bacteria. Staphylococcus aureus, Clostridium perfringens, and Bacillus cereus can form enterotoxins
that cause acute gastrointestinal illness. The illness typically
seen with S. aureus and B. cereus intoxication is the onset of
nausea, vomiting, and mild diarrhea within 1 to 6 h after
ingestion of contaminated food. Incubation periods are very
short because preformed toxin is present in the ingested food.
Intoxication with C. perfringens has a slightly longer incubation
period, because toxin is not preformed but is produced in the
gastrointestinal tract. Symptoms include watery diarrhea and
abdominal cramps starting 8 to 16 h after ingestion of contaminated food. Duration of symptoms is usually less than 24 h;
therefore, many cases likely go undiagnosed. Diagnosis is confirmed by isolation of the organism in samples of stool, vomitus, or food. Additionally, S. aureus enterotoxin can be detected in food samples, which can be useful in situations in
which the organism has been killed in food processing or preparation and therefore cannot be cultured.
Only certain strains of S. aureus produce a toxin that causes
gastrointestinal illness. The main reservoir is humans, who
carry the bacterium in their nasal passages, skin, or wounds. S.
aureus contamination of food, including seafood, is usually due
to contamination by a food worker during food preparation (7,
65). B. cereus and C. perfringens are found in the soil and are
ubiquitous. Only a few reports of illness due to the presence of
these organisms in seafood have been published, but the mechanisms in these cases appear to be similar to those for other
foods (7). To prevent outbreaks of toxin-mediated illnesses, it
is important to keep foods refrigerated and to ensure proper
cooling of hot foods to refrigerator temperatures. Outbreaks
are usually associated with foods left at inappropriate temperatures for prolonged periods, allowing multiplication of the
organism and enterotoxin production (7, 51).
Viruses
Norovirus. Norovirus is a small structured RNA virus that is
among the caliciviruses recognized as human pathogens. Norovirus infection causes a self-limited illness characterized by
diarrhea, vomiting, nausea, abdominal cramps, and sometimes
headache, myalgias, and low-grade fever. The virus may be
identified by electron microscopy or reverse transcriptase PCR
of stool samples and by enzyme immunoassay for detection of
viral antigen in serum samples. Humans are the only known
reservoir, and norovirus is transmitted by person-to-person
spread through the fecal-oral route or through contaminated
food or water. The infectious dose is low, and attack rates are
high. Noroviruses can persist in the environment and can infect
large numbers of people of all ages. Most outbreaks are re-
402
IWAMOTO ET AL.
CLIN. MICROBIOL. REV.
ported from child care centers, cruise ships, long-term care
facilities, and other closed populations. Norovirus is a leading
cause of food-borne illness and outbreaks (44, 68), although
the number of reported outbreaks is likely grossly underestimated because of a lack of routine availability or use of diagnostic testing. The adoption of reverse transcriptase PCR by
the CDC and state public health laboratories in the 1990s has
greatly improved and increased the identification of norovirus
as the etiologic agent of food-borne outbreaks (68).
Seafood harvested from sewage-contaminated waters has
caused outbreaks of norovirus gastroenteritis. Large outbreaks
have been associated with consumption of raw or inadequately
cooked shellfish, such as a series of oyster- and clam-associated
outbreaks in which northeastern coastal waters were implicated (46). Shellfish, particularly bivalve mollusks that are filter
feeders, can accumulate large numbers of viruses. Contamination of harvest areas with human sewage, which has occurred
following overboard sewage dumping by oyster harvest boats
and from sewage runoff into harvest areas following heavy
rains, has been an important source of outbreaks. Additionally,
insufficient cooking, such as steaming clams only until they
open rather than to higher temperatures that kill noroviruses,
has contributed to illness and outbreaks (23, 46). Control measures have focused on monitoring harvest waters for fecal
coliforms and encouraging adequate cooking of seafood; however, continued outbreaks of illness have brought renewed
attention to the risks associated with oyster consumption (36,
41, 46).
Hepatitis A virus. Hepatitis A virus is an RNA virus that is
classified as a picornavirus. Although clinical manifestations
vary in severity, hepatitis A virus infection is the most serious
viral infection associated with seafood consumption. Most
commonly, it is an acute, self-limited illness associated with
fever, malaise, jaundice, anorexia, and nausea; symptoms may
last from several weeks to several months. However, deaths
from fulminant hepatitis can occur. Severity increases with age,
and in rare cases, a prolonged, relapsing hepatitis can occur. In
infants and young children, infection is often asymptomatic.
Diagnosis is made using serologic tests that measure immunoglobulin M antibody against hepatitis A virus. The illness’s long
incubation period (2 to 8 weeks) can make the identification of
the source of infection difficult, and hepatitis A virus infection
associated with seafood is likely underreported. Sporadic and
epidemic cases occur worldwide. In the United States, since
the implementation of routine hepatitis A vaccination of children, rates of reported illnesses, especially among children,
have declined considerably (67).
Humans are the only reservoir of hepatitis A virus, and
transmission is generally by the fecal-oral route. Commonsource food-borne outbreaks occur, and outbreaks of hepatitis
A virus infections associated with oysters and clams have been
described in the United States since the 1960s (22, 40, 55). The
infectious dose is thought to be low, and the virus is taken up
by the mollusk during feeding. Hepatitis A virus is heat resistant and able to withstand steaming, and appropriate cooking
of seafood lessens the chance of ingesting live hepatitis A virus.
But because shellfish is commonly prepared in ways that are
insufficient to inactivate the virus, many prevention strategies
are aimed at controlling contamination prior to food preparation. Contamination most commonly occurs when shellfish
growing areas are contaminated with human sewage (22, 55).
The largest reported outbreak occurred in China in 1988; almost 300,000 persons were infected after consuming clams
harvested from a sewage-contaminated area (56). Fewer outbreaks of hepatitis A virus infection associated with seafood
consumption have been reported in the United States in the
past 2 decades, which may be attributable, at least in part, to
implementation of increased control measures to prevent fecal
contamination of harvest beds during the 1980s. This decrease
suggests that control strategies may have been effective in
reducing the risk of infection via seafood. Recently, the availability of molecular sequencing methods to enhance epidemiologic data has been critical in linking dispersed cases in multiple states to contaminated food products (3). Increases in
public health laboratory capacities for molecular sequencing
will improve our ability to identify outbreaks of hepatitis A
virus infections.
Parasites
Helminths. Helminths are large, worm-like parasites. Helminthic infections associated with the consumption of raw seafood include infections caused by nematodes, trematodes, and
cestodes, notably eustrongyloides, species of Diphyllobothrium
(58), and members of the family Anisakidae (59, 69). Clinical
manifestations associated with helminthic infections range
from no symptoms to mild, chronic gastrointestinal symptoms,
allergic reactions, and, rarely, intestinal perforation and invasive disease. Diagnosis of most parasitic infections is confirmed
by detection of ova or segments of worms in stool samples.
Many worms are present naturally in marine and fresh waters,
and most marine animals are infected. Despite the high prevalence of helminths in seafood, however, outbreaks associated
with seafood are rarely reported. This observation is likely due
to several factors: first, helminths are not able to multiply in
food; second, long incubation periods make identification of
the source of infection difficult; and third, infections are likely
underdiagnosed and underreported, due in part to a lack of
routine diagnostic tests (51, 59). Nonetheless, the potential for
helminthic infection exists with the consumption of raw seafood. Helminths are killed by adequate freezing and by cooking. Control strategies for industry to reduce the risk of helminthic infections also include visually inspecting fish, by
means such as candling, for parasites that are large enough to
be detected visually.
Protozoa. Protozoa are an uncommon cause of food-borne
illnesses in the United States, and common-source outbreaks
are almost always waterborne (44, 70). Protozoa causing recognized seafood-associated illnesses have included Giardia
spp. (54). Giardia is one of the most commonly identified
intestinal parasites in the United States. Clinical manifestations may include abdominal pain, flatulence, anorexia, and a
protracted course of watery, malodorous diarrhea; asymptomatic infection is common. Laboratory diagnosis is most often
made by identification of trophozoites or cysts in stool specimens or by detection of stool antigens by enzyme immunoassay. Humans and other animals are the reservoir of infection.
Food-borne outbreaks of giardiasis have been reported in
which transmission occurred through contamination of food by
infected food handlers (54). Protozoa are sensitive to heat and
References 22, 40,
and 55
VOL. 23, 2010
SEAFOOD-ASSOCIATED INFECTIONS
to prolonged freezing (8). Strategies to prevent food-borne
transmission include adequate cooking and preventing contamination of food during preparation.
EPIDEMIOLOGY OF SEAFOODASSOCIATED INFECTIONS
Sources of Data and Methods
We examined two data sources to understand the epidemiology of seafood-associated illnesses in the United States: the
Food-Borne Disease Outbreak Surveillance System and the
Cholera and Other Vibrio Illness Surveillance System (COVIS).
Determining the food that caused an individual illness is difficult, except during investigations of outbreaks or of certain
infections which are almost always associated with a specific
type of food. Investigations of outbreaks of food-borne illnesses are used to determine the food vehicles for pathogens
that cause illness and to improve our understanding of the
epidemiology of these outbreaks. State and local health departments identify and investigate food-borne outbreaks and,
in turn, report these outbreaks to the CDC. Since the early
1970s, the CDC has collected reports from all states and territories on recognized food-borne disease outbreaks, defined
as 2 or more cases of a similar illness resulting from ingestion
of a common food (53). Information reported includes the
number of persons affected, the etiologic agent identified,
characteristics of illnesses, the month of illness onset, the implicated food item, possible sources of contamination, and
other contributing factors. These surveillance data have been
maintained in a central, electronic database since 1973. In
1998, the reporting procedures were modified to provide feedback to reporting states, and the CDC began verifying outbreak reports with states on a yearly basis.
For this analysis, we included outbreaks with an implicated
seafood vehicle and a single confirmed infectious etiologic
agent. Seafood vehicles were categorized into the following
three commodity groups: (i) mollusks (e.g., oysters, clams, and
scallops); (ii) crustaceans (e.g., shrimp, crab, and lobster); and
(iii) finfish (e.g., salmon, tuna, and finfish eggs) and other
aquatic vertebrates (e.g., whale and seal), or “fish” for brevity.
Outbreaks caused by multiple etiologic agents and outbreaks
for which implicated foods could not be classified into the
single overarching food commodity class “seafood” were not
included in this analysis, unless a single seafood was identified
as the contaminated ingredient responsible for the outbreak.
Additionally, we examined surveillance case reports of
Vibrio illnesses reported through COVIS, which is a collaborative effort of state and county health departments, the FDA,
and the CDC. For the investigation of cases of vibriosis, a
standard report form is used to collect detailed information on
the Vibrio species causing illness; demographic information,
medical history, and travel and food history of the patient; and
shellfish traceback information, when available. COVIS data
are used to help define Vibrio-related syndromes, describe the
epidemiology of vibriosis, and identify vehicles of infection.
Surveillance for vibriosis began in 1988 in Gulf Coast states
and subsequently expanded nationally. In January 2007, vibriosis became a nationally notifiable disease (16).
403
Summary of Seafood-Associated Outbreaks and Infections
General epidemiologic characteristics. During 1973 to 2006,
188 outbreaks of seafood-associated infections, causing 4,020
illnesses, 161 hospitalizations, and 11 deaths, were reported to
the Food-Borne Disease Outbreak Surveillance System. Most
of these seafood-associated outbreaks (143 [76.1%]) were due
to a bacterial agent; 40 (21.3%) outbreaks had a viral etiology,
and 5 (2.6%) had a parasitic cause (Table 1). The number of
confirmed outbreaks reported increased greatly during 1998,
when enhanced surveillance of food-borne outbreaks began
(Fig. 1). Otherwise, the number of outbreaks fluctuated from
year to year during the study period, with no significant increasing or decreasing trends seen. Outbreaks ranged in size
from 2 to 400 affected persons, with an overall median outbreak size of 5 persons affected. The median size of outbreaks
was stable through the 1970s and 1980s. Starting in the early
1990s, the median outbreak size varied substantially, with large
peaks seen during 1993, 1995, and 2004.
Seafood-associated outbreaks occurred throughout the year,
with a peak during late summer (Fig. 2). However, seasonality
differed by etiology. Bacterial pathogens, especially vibrios,
caused more outbreaks during warmer months, whereas outbreaks of seafood-associated norovirus infections occurred
more frequently during colder months. Seafood-associated
outbreaks from all causes were reported most commonly from
the following coastal states (Fig. 3): Alaska (39), New York
(19), California (17), Florida (16), Oregon (11), and Washington (16). All other states reported fewer than 10 outbreaks
during the study period. Etiologic agents and implicated seafood vehicles varied by state. Almost all outbreaks reported
from Alaska, which reported 39 (20.7%) outbreaks, were due
to botulism. States in the Pacific Northwest reported a disproportionate number of Vibrio and norovirus outbreaks, largely
associated with molluscan shellfish (11, 12). Notably, in recent
years, outbreaks of infections due to some pathogens usually
associated with seafood harvested from warm waters were reported from more northerly areas of the country that had not
previously reported outbreaks. For example, the first outbreak
of Vibrio parahaemolyticus infections in Alaska was reported in
2004, during a period when waters in the area experienced
historically high temperatures (42). Nine multistate seafoodassociated outbreaks were reported to the CDC, and almost all
of these outbreaks occurred after the mid-1990s. Each of these
multistate outbreaks was associated with oysters that were
widely distributed.
Seafood-associated outbreaks of infection varied by seafood
commodity. Mollusks were implicated in 85 (45.2%) outbreaks, followed by fish in 73 (38.8%) outbreaks and crustaceans in 30 (16.0%) outbreaks (Table 1). All of the molluskassociated outbreaks were associated with bivalve mollusks,
including oysters (implicated in 72 outbreaks) and clams (11
outbreaks.) In fish-associated outbreaks, the most commonly
implicated fish was salmon (15 outbreaks); “salmon” included
fermented fish parts and fermented salmon eggs, which accounted for 10 of these outbreaks. Other commonly reported
fish vehicles were tuna (10 outbreaks), seal meat (9 outbreaks),
whale (7 outbreaks), and whitefish (not further specified) (4
outbreaks). Among crustacean-associated outbreaks, the most
commonly implicated items were crab (15 outbreaks) and
1 (1)
1 (1)
0 (0)
1 (1)
3 (4)
73 (100)
Parasites
Anisakidae
Giardia lamblia
Paragonimus
Diphyllobothrium
Total
Total (1973–2006)
1,210 (100)
14 (1)
29 (2)
0 (0)
10 (1)
53 (4)
418 (35)
7 (1)
425 (35)
0 (0)
0 (0)
261 (22)
259 (21)
7 (1)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
732 (60)
0 (0)
0 (0)
10 (14)
6 (8)
3 (4)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
65 (89)
4 (5)
1 (1)
5 (7)
7 (1)
0 (0)
152 (13)
46 (4)
0 (0)
93 (100)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
15 (16)
17 (18)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
93 (100)
0 (0)
0 (0)
61 (66)
0 (0)
0 (0)
No. (%) of
No. (%) of
illnesses
hospitalizations
Fish
2 (3)
0 (0)
43 (59)
1 (1)
0 (0)
No. (%) of
outbreaks
Viruses
Norovirus
Hepatitis A virus
Total
Bacteria
Bacillus cereus
Campylobacter spp.
Clostridium botulinum
Clostridium perfringens
Escherichia coli,
enteroaggregative
E. coli, enterohemorrhagic
Listeria monocytogenes
Salmonella
Shigella spp.
Staphylococcus aureus
Vibrio cholerae, toxigenic
Vibrio cholerae, nontoxigenic
Vibrio parahaemolyticus
Vibrio vulnificus
Vibrio spp., not specified
Total
Etiology
30 (100)
0 (0)
0 (0)
1 (0)
0 (0)
1 (0)
0 (0)
1 (3)
1 (3)
1 (3)
1 (3)
4 (13)
1 (3)
2 (7)
3 (10)
0 (0)
12 (40)
0 (0)
0 (0)
28 (93)
2 (7)
0 (0)
0 (0)
1 (3)
1 (3)
No. (%) of
outbreaks
609 (100)
0 (0)
0 (0)
18 (0)
0 (0)
18 (0)
0 (0)
7 (1)
7 (1)
21 (3)
2 (0)
81 (13)
25 (4)
22 (4)
10 (2)
0 (0)
234 (38)
0 (0)
0 (0)
584 (96)
122 (20)
0 (0)
0 (0)
55 (9)
12 (2)
No. (%) of
illnesses
Crustaceans
13 (100)
0 (0)
0 (0)
2 (0)
0 (0)
2 (0)
0 (0)
0 (0)
0 (0)
0 (0)
1 (8)
8 (62)
0 (0)
0 (0)
1 (8)
0 (0)
1 (8)
0 (0)
0 (0)
11 (85)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
No. (%) of
hospitalizations
85 (100)
0 (0)
1 (1)
0 (0)
0 (0)
1 (1)
27 (32)
7 (8)
34 (40)
0 (0)
0 (0)
4 (5)
5 (6)
0 (0)
0 (0)
4 (5)
33 (39)
1 (1)
1 (1)
50 (59)
0 (0)
2 (2)
0 (0)
0 (0)
0 (0)
No. (%) of
outbreaks
2,201 (100)
0 (0)
3 (0)
0 (0)
0 (0)
3 (0)
747 (34)
121 (6)
868 (39)
0 (0)
0 (0)
32 (1)
118 (5)
0 (0)
0 (0)
12 (1)
1,159 (53)
2 (0)
2 (0)
1,330 (60)
0 (0)
5 (0)
0 (0)
0 (0)
0 (0)
No. (%) of
illnesses
Mollusks
55 (100)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
16 (29)
7 (13)
23 (42)
0 (0)
0 (0)
5 (9)
3 (5)
0 (0)
0 (0)
0 (0)
23 (42)
1 (2)
0 (0)
32 (58)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
No. (%) of
hospitalizations
TABLE 1. Seafood-associated outbreaks of infection, by etiology and seafood commodity, 1973 to 2006
188 (100)
1 (1)
2 (1)
1 (0)
1 (1)
5 (3)
31 (16)
9 (5)
40 (21)
1 (1)
1 (1)
18 (10)
12 (6)
5 (3)
3 (2)
4 (2)
45 (24)
1 (1)
1 (1)
143 (76)
4 (2)
2 (1)
43 (23)
2 (1)
1 (1)
No. (%) of
outbreaks
4,020 (100)
14 (0)
32 (1)
18 (0)
10 (1)
74 (2)
1,165 (29)
135 (3)
1,300 (32)
21 (1)
2 (0)
374 (9)
402 (10)
29 (1)
10 (0)
12 (0)
1,393 (35)
2 (0)
2 (0)
2,646 (66)
129 (3)
5 (0)
152 (4)
101 (3)
12 (0)
No. (%) of
illnesses
All seafood
161 (100)
0 (0)
0 (0)
2 (0)
0 (0)
2 (1)
16 (10)
7 (4)
23 (14)
0 (0)
1 (1)
28 (17)
20 (12)
0 (0)
1 (1)
0 (0)
24 (15)
1 (1)
0 (0)
136 (84)
0 (0)
0 (0)
61 (38)
0 (0)
0 (0)
No. (%) of
hospitalizations
404
IWAMOTO ET AL.
CLIN. MICROBIOL. REV.
VOL. 23, 2010
SEAFOOD-ASSOCIATED INFECTIONS
405
FIG. 1. Number of confirmed seafood-associated outbreaks and outbreak-related cases, by year and etiology, 1973 to 2006.
shrimp (15 outbreaks). Comparing seafood categories within
different periods, the number and proportion of mollusk-associated outbreaks increased greatly during the study period,
from 10% of outbreaks during 1973 to 1979 to 56.6% of outbreaks during 1998 to 2006 (Fig. 4). The proportion of outbreaks due to fish decreased during the study period, from
90.0% of outbreaks to 24.2% of outbreaks during the last part
of the study period. The proportion due to crustaceans varied,
ranging from no outbreaks during the first decade to 19.2% of
outbreaks.
Outbreaks and infections caused by bacteria. Bacteria were
reported as the etiologic agent in 143 (76.1%) outbreaks, caus-
FIG. 2. Number of confirmed seafood-associated outbreaks, by etiology and month of occurrence, 1973 to 2006.
406
IWAMOTO ET AL.
CLIN. MICROBIOL. REV.
FIG. 3. Number of confirmed seafood-associated outbreaks in the United States, by state, 1973 to 2006.
ing 2,646 illnesses, 136 hospitalizations, and 11 deaths. The
median size of seafood-associated outbreaks caused by bacteria was 4 cases, with a range of 2 to 400 cases. Almost all
outbreaks associated with fish (89.0%) and crustaceans
(93.3%) were caused by a bacterial agent; among outbreaks
associated with mollusks, 50 outbreaks (58.8%) were caused by
a bacterium.
Vibrios were the most commonly reported cause of seafood-
FIG. 4. Percentages of seafood-associated outbreaks of infection attributable to seafood commodities in four multiyear ranges.
VOL. 23, 2010
SEAFOOD-ASSOCIATED INFECTIONS
407
FIG. 5. Numbers of outbreaks and sporadic cases of Vibrio infection, by species and year, 1997 to 2006.
associated outbreaks. Specifically, Vibrio parahaemolyticus
caused more outbreaks and illnesses than any other pathogen
(45 outbreaks [23.9% of all infectious disease outbreaks], 1,393
illnesses, and no deaths) during the study period. Other Vibrio
species reported included toxigenic V. cholerae (3 outbreaks,
10 illnesses, and no deaths), non-O1, non-O139 V. cholerae (4
outbreaks, 12 illnesses, and no deaths), and V. vulnificus (1
outbreak, 2 illnesses, and 1 death). Among outbreaks of Vibrio
illness, 15 (27.8%) were associated with crustaceans, and the
remaining 39 (72.2%) were associated with mollusks, particularly oysters. Outbreaks of Vibrio illnesses were sharply seasonal, with 44 (81.5%) occurring during the warmer months of
May to September. The number of reported outbreaks of
Vibrio infections increased over the study period, with the
greatest number reported during the last decade, 1997 to 2006.
The largest reported seafood-associated outbreak was an outbreak in 1998 of V. parahaemolyticus infections associated with
oyster consumption, causing 416 illnesses among persons in 13
states (19). During 1997 to 2006, there was substantial yearto-year variability in the number of outbreaks of Vibrio infections, with large multistate outbreaks associated with oysters
occurring during 1998 and 2006 (12, 19).
During the past decade, the increases in the number and size
of Vibrio outbreaks mirrored the trends in reports of sporadic
cases of infections nationally, as reported to COVIS (Fig. 5).
During 1997 to 2006, 4,755 cases of Vibrio illness were reported
to COVIS; of these, 3,406 (71.6%) were classified as foodborne infections. The most commonly reported Vibrio species
causing food-borne infections were V. parahaemolyticus (1,931
[56.7%] food-borne Vibrio infections) and V. vulnificus (459
[13.5%] infections). V. parahaemolyticus infections were most
often food borne (89.0% [1,931/2,170 infections]). Among patients with food-borne V. parahaemolyticus infections who reported food exposures, almost all (94.5%) patients reported
eating seafood during the week before illness onset, most commonly oysters (72.5% [1,143/1,577 patients]). Larger numbers
of sporadic cases of Vibrio infection were reported in years
during which multistate outbreaks were also reported. During
these years, warmer sea temperatures were documented (12,
18, 42). Similarly, the distribution of sporadic cases was sharply
seasonal, with most cases (72.8%) occurring during summer
months, corresponding to warmer water temperatures. Of the
944 V. vulnificus cases, 459 (47.0%) were classified as foodborne infections; among patients with food-borne V. vulnificus
infection who reported food exposures, 91.1% reported seafood consumption during the week before illness, most commonly oysters (80.5% [289/361 patients]). Nearly all patients
(92.2%) with food-borne V. vulnificus infection were reported
to have a preexisting medical condition, most commonly liver
disease. The case fatality rate for food-borne V. vulnificus infections was 48.3%.
During the study period, the second most commonly reported bacterial pathogen causing seafood-associated outbreaks was Clostridium botulinum, which caused 43 outbreaks,
152 illnesses, 61 hospitalizations, and 9 deaths. Most (86.0%
[37/43 reports]) reports came from Alaska. Most of these outbreaks occurred among Alaska Natives and were associated
with the consumption of traditional Alaska Native seafood
dishes, which are often fermented under anaerobic conditions
where botulinum spores may germinate (66). Botulinum toxin
type E was most frequently identified in these seafood-associated outbreaks of botulism. Seafood associated with the outbreaks included fish, particularly salmon eggs and fish heads,
seal, and whale meat (43). No botulism outbreaks were associated with consumption of mollusks or crustaceans.
Other bacterial etiologies of seafood-associated outbreaks
included Salmonella, which caused 18 outbreaks, 374 illnesses,
and 28 hospitalizations. Fish were implicated in 10 outbreaks;
specifically, gefilte fish, a traditional dish made from ground
deboned fish, was implicated in 4 outbreaks, with whitefish
implicated in 2 outbreaks, bass in 1 outbreak, and unspecified
fish in the rest (3). Mollusks and crustaceans were each impli-
408
IWAMOTO ET AL.
cated in 4 outbreaks. Most outbreaks of Salmonella infection
occurred during warmer months. Shigella was the etiologic
agent in 12 outbreaks, causing 402 illnesses and 20 hospitalizations. Implicated seafood included fish in 6 outbreaks, raw
oysters in 4 outbreaks, scallops in 1 outbreak, and crab in 1
outbreak.
Outbreaks caused by viruses. During the study period, 40
(21.3%) seafood-associated outbreaks were caused by viruses.
Seafood associated with these outbreaks included mollusks (34
outbreaks [85.0% of outbreaks caused by viruses]), fish (5
outbreaks [12.5%]), and crustaceans (1 outbreak [2.5%]). The
median size of viral outbreaks was 10 cases (range, 2 to 380
cases). Overall, norovirus was the third most commonly reported pathogen associated with seafood and the most common viral agent, causing 31 (77.5%) outbreaks of viral illness.
Mollusk-associated, especially raw oyster-associated, outbreaks of norovirus were common (27 outbreaks) and made up
almost one-third (31.8% [27/85 outbreaks]) of all molluscan
outbreaks. Unlike outbreaks of bacterial illness, outbreaks of
norovirus illness were more common during cooler months,
with more than three-fourths (77.4%) of outbreaks occurring
during October to March. Confirmed outbreaks of norovirus
infection were reported more commonly during the past decade; 26 of 31 (83.8%) outbreaks were reported during 1998 to
2006. However, the etiology of outbreaks changed over the
course of the study period. During the early 1980s, large outbreaks of viral gastroenteritis caused by molluscan shellfish
(46) were prominent. These were followed by a decrease in
reported outbreaks of viral illness that lasted until 2000, when
reports again increased, likely due to better diagnostic testing,
an improved ability to confirm etiology, and improved public
health surveillance for outbreaks.
Hepatitis A virus was the cause of 9 seafood-associated
outbreaks. Most outbreaks of hepatitis A virus infection (7
outbreaks [77.7%]) were associated with mollusks. Tuna and
crab were each implicated in one outbreak. Most outbreaks
occurred during the 1980s (22, 46), none were reported during
the 1990s, and only 2 were reported after 2000 (3).
Outbreaks caused by parasites. Seafood-associated outbreaks caused by parasites were rare, with 5 outbreaks reported during the study period. Outbreaks ranged in size from
3 to 29 persons affected; the median size of outbreaks was 14
cases. Reported outbreaks included 2 outbreaks of giardiasis,
one caused by salmon (54) and one by oysters, an outbreak of
Paragonimus infections associated with the consumption of live
crabs (15), an outbreak of Diphyllobothrium infection associated with salmon consumption (9, 58), and an outbreak of
anisakiasis associated with consumption of an unspecified fish.
DISCUSSION
We have described the epidemiology of infections associated
with seafood consumption in the United States from 1973 to
2006. Seafood—finfish, marine mammals, mollusks, and crustaceans—is an important cause of food-borne illness and outbreaks in the United States. Our analysis identified specific
seafood vehicles frequently associated with illness. This information can help to guide future prevention efforts. Seafoodassociated outbreaks of infection were most often attributed to
consumption of molluscan shellfish, particularly raw oysters,
78% Main Outbreak is Shellfish
CLIN. MICROBIOL. REV.
and most often caused Vibrio illnesses and norovirus infections.
Over the study period, both the absolute number of outbreaks
and the proportion of outbreaks caused by molluscan shellfish
increased. Botulism cases associated with fish were also reported frequently, although these outbreaks were reported almost exclusively from Alaska. Etiologies and implicated seafood commodities changed over time during the study period.
The cause of these changes is likely multifactorial: enhanced
food-borne outbreak surveillance began in the late 1990s; laboratory diagnostic capacities have improved, particularly for
norovirus but also for other pathogens, resulting in better
detection of outbreaks; control efforts, especially in shellfish
sanitation, have evolved; and changes in environmental factors
may favor the occurrence of some pathogens.
Our analysis of surveillance data is subject to several limitations. The true burden of illnesses associated with seafood
consumption is probably much greater than what we report.
Our understanding of foods and pathogens responsible for
illness is largely derived from information gained from outbreak investigations. However, many outbreaks likely go unrecognized and uninvestigated. Moreover, the Food-Borne
Disease Outbreak Surveillance System is a passive system that
relies on voluntary reporting, which may lead to further underestimation of the actual number of outbreaks and illnesses
that occur. Outbreak reporting may not be uniform across
states, which may be due in part to whether states have dedicated food-borne disease epidemiologists. Also, outbreaks
comprise only a small proportion of all cases of food-borne
illness. No information is available on seafood-borne transmission in sporadic cases of infection other than Vibrio illnesses.
Enhanced surveillance for food-borne outbreaks began in
1998. As a result, an abrupt increase in reported outbreaks
occurred, which should not be interpreted as a true increase in
the number of outbreaks. Also, improved laboratory methods
and surveillance increased the ability to detect and investigate
outbreaks during the study period. For example, subtype-based
laboratory surveillance has improved the ability to detect outbreaks of infections associated with seafood items that are
widely distributed, as in multistate outbreaks, and with pathogens with long incubation periods, such as hepatitis A virus.
Other laboratory methods that evolved during the past decade
include testing for the presence of norovirus by PCR and
increased use of appropriate selective media to detect Vibrio
organisms in stool.
Contamination of seafood can occur before harvest or at any
point from harvest through final preparation. The types and
numbers of pathogens present in seafood are affected by the
environment from which the seafood was harvested and by
sanitation during subsequent handling, processing, storage,
transportation, and final preparation. Survival of food-borne
pathogens is more likely to occur in foods that are consumed
undercooked or raw and in those that experience time and
temperature abuse, such as may occur during delays between
harvest and refrigeration.
Control strategies to prevent seafood-associated illnesses
include monitoring harvest waters, identification and implementation of process controls, and consumer education. Federal agencies, state governments, and private industry all bear
responsibility for reducing seafood-associated infections. The
FDA plays an important role in establishing guidelines and
VOL. 23, 2010
SEAFOOD-ASSOCIATED INFECTIONS
providing oversight to ensure safer fish and fishery products.
Prevention strategies developed by the FDA and the seafood
industry to minimize the risk of microbial contamination and
decrease the risk of seafood-associated infection include good
manufacturing practices, which address sanitation conditions
and practices, and a seafood hazard analysis and critical control point (HACCP) program. The purpose of a HACCP is to
identify sources and points in processes at which the risk of
contamination is high, from harvest to consumption, so that
processes to decrease these risks can be implemented and
monitored. During the mid-1990s, the FDA issued regulations
for the seafood industry, relying on HACCP-based principles.
Every seafood harvester and processor is now required to use
a HACCP-based system. Examples of HACCP-based principles include candling of fish to detect parasites, a low-acid
canning program for canned tuna and salmon to prevent botulism, and rapid chilling of fish after death to prevent scombrotoxin formation (24).
Shellfish regulation has a distinctive history. Control strategies in addition to those mentioned above and specifically
aimed at promoting the safety of molluscan shellfish are implemented through the National Shellfish Sanitation Program
(NSSP). The NSSP guidelines are uniform shellfish safety standards that regulate the harvesting, processing, and shipping of
shellfish for interstate commerce. The NSSP was established in
response to large outbreaks of typhoid fever associated with
contaminated mollusks that occurred in the 1920s. Through
the ensuing decades, NSSP guidelines have evolved to address
public health problems. Since 1985, NSSP guidelines have been
established through the Interstate Shellfish Sanitation Conference (ISSC), which is a cooperative organization with representation from the FDA and other federal agencies, state
health departments and shellfish authorities, and private industry. Commercial shellfish harvesting is regulated by states in
accordance with NSSP guidelines. The standards for harvesting
shellfish are established by state rules and regulations, and
harvesting occurs in designated approved areas.
Under the NSSP, standards for harvesting shellfish involve
monitoring of environmental factors, including coliform
counts, marine biotoxins, levels of V. parahaemolyticus in sampled oysters, water salinity levels, and ambient and water temperatures. Fecal coliforms are used as an indicator of bacterial
contamination and to classify shellfish harvesting areas as safe
or unsafe. While they have been useful as an indicator of the
presence of feces-related bacteria in harvest beds, they are less
reliable for naturally occurring pathogens (e.g., Vibrio species)
and for enteric viruses. Our surveillance data suggest that the
greatest current seafood safety risks involve bivalve mollusks
contaminated with naturally occurring pathogens. Therefore,
prevention of initial contamination at or before the time of
harvest is important, and environmental monitoring is critical.
Investigation of seafood-associated outbreaks and traceback
information on shellfish implicated in sporadic cases of Vibrio
illness have indicated that illness is often associated with consumption of shellfish harvested from warmer waters (18, 19, 27,
42, 60). The recent investigation of an outbreak of V. parahaemolyticus infections associated with Alaskan oysters underscores the need to examine the emerging health risks posed by
changing environmental factors, such as rising water temperatures (42). In an effort to further reduce the risk of shellfish-
409
associated Vibrio illnesses, the ISSC has established additional
control measures based on environmental conditions such as
air and water temperature (26).
Additional control measures exist to prevent contamination
during postharvest handling, processing, and distribution of
shellfish. Bacterial proliferation and toxin formation can occur
if contaminated seafood is not maintained at appropriate temperatures; therefore, minimizing the time between harvest and
refrigeration is critical, especially during summer months (27).
The FDA and ISSC have established NSSP guidelines for
storage times and temperatures for specific seafood products.
However, the potential benefits of implementing strict requirements to shorten the time between shellfish harvest and refrigeration are countered by concerns for the potential economic
burden to the shellfish industry. A unique control strategy for
molluscan shellfish is the labeling of all containers containing
bivalve mollusks with tags containing information about the
harvest site and date. These tags are maintained by harvesters,
dealers, shippers, and restaurants for at least 90 days after sale.
This information on the location of harvesting facilitates traceback to harvest waters of lots associated with illness. It is
important that industry-implemented postharvest processing
methods for seafood, particularly oysters, are available to reduce microbial hazards. Established and well-accepted methods include individually quick-freezing oysters, pasteurization,
irradiation, and high hydrostatic pressure, and new methods
continue to be developed. These processing techniques reduce
microorganisms to nondetectable levels and reduce the risk of
illness (27).
Consumers should be aware of the potential health risks
associated with eating seafood. Seafood-borne infections can
be prevented by cooking seafood thoroughly, storing foods
properly, and avoiding cross-contamination after cooking.
However, some seafood is commonly consumed raw or minimally cooked. Persons with underlying medical conditions such
as liver disease, diabetes, or immunosuppressing conditions are
at higher risk of acquiring severe infection and should be
especially careful. Educational strategies have focused particularly on those persons. Messages warning consumers of the
potential risks of infection associated with raw oyster consumption are posted in restaurants in states where illnesses caused
by Vibrio vulnificus are prevalent; however, cases continue to
occur, suggesting that these educational strategies by themselves may not prevent all cases (47) and that additional regulatory measures, as well as more effective consumer education, may be needed to further reduce the incidence of illness.
For clinicians and laboratorians, prompt recognition of infection in patients who seek medical attention for illness after
eating raw or undercooked seafood is important for appropriate testing (e.g., use of TCBS agar for culture of stool samples)
and early treatment, as necessary. Rapid reporting of these
cases to public health authorities is critical to identify both
contaminated seafood and risky harvest areas in order to implement timely control measures.
Seafood is part of a healthful diet, but seafood consumption
is not risk-free. Multiple outbreaks of seafood-associated infections, especially mollusk-associated outbreaks of Vibrio infections, continue to occur every year in the United States,
suggesting that existing control strategies have not been optimally effective. Prevention of seafood-associated infections re-
Outbreak = More than 2
410
IWAMOTO ET AL.
quires an understanding not only of the etiologic agents and
seafood commodities associated with illness but also of the
mechanisms of contamination that are amenable to control.
Defining these problem areas, which relies on surveillance of
seafood-associated infections through outbreak and case reporting, can lead to targeted research and help to guide control
efforts. Coordinated efforts are necessary to further reduce the
risk of seafood-associated illnesses. Continued surveillance will
be important to assess the effectiveness of current and future
prevention strategies.
REFERENCES
1. Abbott, S. L., J. M. Janda, J. A. Johnson, and J. J. Farmer. 2007. Vibrio and
related organisms, 9th ed. ASM Press, Washington, DC.
2. Ayers, T., M. Iwamoto, D. L. Swerdlow, and I. Williams. 2008. Epidemiology
of seafood-associated outbreaks in the United States, 1973–2006, abstr. P370. Abstr. Int. Assoc. Food Prot. Annu. Meeting, Columbus, OH.
3. Bialek, S. R., P. A. George, G. L. Xia, M. B. Glatzer, M. L. Motes, J. E.
Veazey, R. M. Hammond, T. Jones, Y. C. Shieh, J. Wamnes, G. Vaughan, Y.
Khudyakov, and A. E. Fiore. 2007. Use of molecular epidemiology to confirm
a multistate outbreak of hepatitis A caused by consumption of oysters. Clin.
Infect. Dis. 44:838–840.
4. Blake, P. A., M. H. Merson, R. E. Weaver, D. G. Hollis, and P. C. Heublein.
1979. Disease caused by a marine vibrio: clinical characteristics and epidemiology. N. Engl. J. Med. 300:1–5.
5. Brands, D. A., A. E. Inman, C. P. Gerba, J. Mare, S. J. Billington, L. A. Saif,
J. F. Levine, and L. A. Joens. 2005. Prevalence of Salmonella spp. in oysters
in the United States. Appl. Environ. Microbiol. 71:893–897.
6. Brenner, F. W., R. G. Villar, F. J. Angulo, R. Tauxe, and B. Swaminathan.
2000. Salmonella nomenclature. J. Clin. Microbiol. 38:2465–2467.
7. Bryan, F. L. 1980. Epidemiology of foodborne diseases transmitted by fish,
shellfish and marine crustaceans in the United States, 1970–1978. J. Food.
Prot. 43:859–876.
8. Casemore, D. P. 1990. Foodborne protozoal infection. Lancet 336:1427–
1432.
9. CDC. 1981. Diphyllobothriasis associated with salmon. MMWR Morb. Mortal. Wkly. Rep. 30:331–338.
10. CDC. 31 July 2000, posting date. Keeping your family safe from botulism.
CDC, Atlanta, GA. http://www2.cdc.gov/phtn/botulism/default/default.asp.
11. CDC. 1998. Outbreak of Vibrio parahaemolyticus infections associated with
eating raw oysters—Pacific Northwest, 1997. MMWR Morb. Mortal. Wkly.
Rep. 47:457–461.
12. CDC. 2006. Vibrio parahaemolyticus infections associated with consumption
of raw shellfish—three states, 2006. MMWR Morb. Mortal. Wkly. Rep.
55:854–856.
13. Reference deleted.
14. CDC. 9 January 2009, posting date. Summary of botulism cases. CDC,
Atlanta, GA. http://www.cdc.gov/nationalsurveillance/botulism_surveillance
.html. Accessed 2 February 2010.
15. CDPH. 18 August 2006, posting date. Consumers warned against eating raw,
imported, freshwater crabs after two restaurant diners suffer from unusual lung
infection. California Department of Health Services, Sacramento, CA. http:
//www.cdph.ca.gov/pubsforms/Guidelines/Documents/fdb%20Paragonimus%
20Rel.pdf.
16. CSTE. 14 September 2006, posting date. CSTE position statement: national
reporting for non-cholera Vibrio infections. CSTE, Atlanta, GA. http://www
.cste.org/PS/2006pdfs/PSFINAL2006/06-ID-05FINAL.pdf.
17. Daniels, J. L., M. P. Longnecker, A. S. Rowland, and J. Golding. 2004. Fish
intake during pregnancy and early cognitive development of offspring. Epidemiology 15:394–402.
18. Daniels, N. A., L. C. MacKinnon, R. Bishop, S. Altekruse, B. Ray, R. M.
Hammond, S. Thompson, S. Wilson, N. H. Bean, P. M. Griffin, and L.
Slutsker. 2000. Vibrio parahaemolyticus infections in the United States, 1973–
1998. J. Infect. Dis. 181:1661–1666.
19. Daniels, N. A., B. Ray, A. N. Easton, N. N. Marano, E. Kahn, A. L. McShan,
L. Del Rosario, T. Baldwin, M. A. Kingsley, N. D. Puhr, J. G. Wells, and F. J.
Angulo. 2000. Emergence of new Vibrio parahaemolyticus serotype in raw
oysters: a prevention quandary. JAMA 284:1541–1545.
20. Daviglus, M. L., J. Stamler, A. J. Orencia, A. R. Dyer, K. Liu, P. Greenland,
M. K. Walsh, D. Morris, and R. B. Shekelle. 1997. Fish consumption and the
30-year risk of fatal myocardial infarction. N. Engl. J. Med. 336:1046–1053.
21. Dechet, A. M., P. A. Yu, N. Koram, and J. Painter. 2008. Nonfoodborne
Vibrio infections: an important cause of morbidity and mortality in the
United States, 1997–2006. Clin. Infect. Dis. 46:970–976.
22. Desenclos, J. C., K. C. Klontz, M. H. Wilder, O. V. Nainan, H. S. Margolis,
and R. A. Gunn. 1991. A multistate outbreak of hepatitis A caused by the
consumption of raw oysters. Am. J. Public Health 81:1268–1272.
CLIN. MICROBIOL. REV.
23. DuPont, H. L. 1986. Consumption of raw shellfish—is the risk now unacceptable? N. Engl. J. Med. 314:707–708.
24. FDA. 2001. Fish and fisheries products hazards and controls guide, 3rd ed.
FDA, Rockville, MD.
25. FDA. 2006, posting date. Fresh and frozen seafood: selecting and serving it
safely. FDA, Rockville, MD. http://www.fda.gov/Food/ResourcesForYou
/Consumers/ucm077331.htm.
26. FDA. 29 May 2009, posting date. National Shellfish Sanitation Program:
guide for the control of molluscan shellfish 2007. FDA, Rockville, MD.
http://www.fda.gov/Food/FoodSafety/Product-SpecificInformation/Seafood
/FederalStatePrograms/NationalShellfishSanitationProgram/default.htm.
Accessed 2 February 2010.
27. FDA. 2005. Quantitative risk assessment on the public health impact of
pathogenic Vibrio parahaemolyticus in raw oysters. FDA, College Park, MD.
28. Fewtrell, M. S., R. A. Aboott, K. Kennedey, A. Singhal, R. Morley, E. Caine,
C. Jamieson, F. Cockburn, and A. Lucas. 2004. Randomized, double-blind
trial of long-chain polyunsaturated fatty acid supplementation with fish oil
and borage oil in preterm infants. J. Pediatr. 144:471–479.
29. Gangarosa, E. J., A. L. Bisno, E. R. Eichner, M. D. Treger, M. Goldfield,
W. E. DeWitt, R. Fodor, S. M. Fish, W. J. Dougherty, J. B. Murphy, J.
Feldman, and H. Vogel. 1968. Epidemic of febrile gastroenteritis due to
Salmonella Java traced to smoked whitefish. Am. J. Public Health 58:114–
121.
30. Heinitz, M. L., R. D. Ruble, D. E. Wagner, and S. R. Tatini. 2000. Incidence
of Salmonella in fish and seafood. J. Food Prot. 63:579–592.
31. Helland, I. B., L. Smith, K. Saarem, O. D. Saugstad, and C. A. Drevon. 2003.
Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children’s IQ at 4 years of age. Pediatrics
111:e39–e44.
32. Hibbeln, J. R., J. M. Davis, C. Steer, P. Emmett, I. Rogers, C. Williams, and
J. Golding. 2007. Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational
cohort study. Lancet 369:578–585.
33. Hlady, W. G., and K. C. Klontz. 1995. The epidemiology of Vibrio infections
in Florida, 1981–1993. J. Infect. Dis. 173:1176–1183.
34. Janda, J. M., C. Powers, R. G. Bryant, and S. L. Abbott. 1988. Current
perspectives on the epidemiology and pathogenesis of clinically significant
Vibrio spp. Clin. Microbiol. Rev. 1:245–267.
35. Klontz, K. C., S. Lieb, M. Schreiber, H. T. Janowski, L. M. Baldy, and R. A.
Gunn. 1988. Syndromes of Vibrio vulnificus infections. Clinical and epidemiologic features in Florida cases, 1981–87. Ann. Intern. Med. 109:318–323.
36. Kohn, M. A., T. A. Farley, T. Ando, M. Curtis, S. A. Wilson, Q. Jin, S. S.
Monroe, S. S. Baron, L. M. McFarland, and R. I. Glass. 1995. An outbreak
of Norwalk virus gastroenteritis associated with eating raw oysters. Implications for maintaining safe oyster beds. JAMA 273:466–471.
37. Kris-Etherton, P. M., W. S. Harris, and L. J. Appel. 2002. Fish consumption,
fish oil, omega-3 fatty acids, and cardiovascular disease: AHA scientific
statement. Circulation 106:2747–2757.
38. Kromhout, D., E. B. Bosschieter, and C. de Lezenne Coulander. 1985. The
inverse relationship between fish consumption and 20-year mortality from
coronary heart disease. N. Engl. J. Med. 312:1205–1209.
39. Levine, W. C., and P. M. Griffin. 1993. Vibrio infections on the Gulf coast:
results of first year of regional surveillance. J. Infect. Dis. 167:479–483.
40. Mason, J. O., and W. R. McLean. 1962. Infectious hepatitis traced to the
consumption of raw oysters. Am. J. Hygiene 75:90–111.
41. McDonnell, S., K. B. Kirkland, W. G. Hlady, C. Aristeguieta, R. S. Hopkins,
S. S. Monroe, and R. I. Glass. 1997. Failure of cooking to prevent shellfishassociated viral gastroenteritis. Arch. Intern. Med. 157:111–116.
42. McLaughlin, J. B., A. DePaola, C. A. Bopp, K. A. Martinek, N. P. Napolilli,
C. G. Allison, S. L. Murray, E. C. Thompson, M. M. Bird, and J. P. Middaugh. 2005. Outbreak of Vibrio parahaemolyticus gastroenteritis associated
with Alaskan oysters. N. Engl. J. Med. 353:1463–1470.
43. McLaughlin, J. B., J. Sobel, T. Lynn, E. Funk, and J. P. Middaugh. 2004.
Botulism type E outbreak associated with eating a beached whale, Alaska.
Emerg. Infect. Dis. 10:1685–1687.
44. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro,
P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the
United States. Emerg. Infect. Dis. 5:607–625.
45. Morris, J. G., and R. E. Black. 1985. Cholera and other vibrioses in the
United States. N. Engl. J. Med. 312:343–350.
46. Morse, D. L., J. J. Guzewich, J. P. Hanrahan, R. Stricof, M. Shayegani, R.
Deibel, J. C. Grabau, N. A. Nowak, J. E. Herrmann, G. Cukor, et al. 1986.
Widespread outbreaks of clam- and oyster-associated gastroenteritis. Role of
Norwalk virus. N. Engl. J. Med. 314:678–681.
47. Mouzin, E., L. Mascola, M. P. Tormey, and D. E. Dassey. 1997. Prevention
of Vibrio vulnificus infections: assessment of regulatory educational strategies. JAMA 278:576–578.
48. Mozaffarian, D., and E. B. Rimm. 2006. Fish intake, contaminants, and
human health. JAMA 296:1885–1899.
49. NOAA. 2005. Fisheries of the United States, 2005. National Marine Fisheries
Service, Silver Spring, MD.
VOL. 23, 2010
50. Oliver, J. D. 2005. Wound infections caused by Vibrio vulnificus and other
marine bacteria. Epidemiol. Infect. 133:383–391.
51. Olsen, S. J., J. N. Aucott, and D. L. Swerdlow. 2002. Food poisoning, p.
199–214. In M. Blaser, P. Smith, J. Ravdin, H. Greenberg, and R. Guerrant
(ed.), Infections of the gastrointestinal tract, 2nd ed. Lippincott Williams and
Wilkins, Philadelphia, PA.
52. Olsen, S. J., R. Bishop, F. W. Brenner, T. H. Roels, N. Bean, and R. V. Tauxe.
2001. The changing epidemiology of Salmonella: trends in serotypes isolated
from humans in the United States, 1987–1997. J. Infect. Dis. 83:753–761.
53. Olsen, S. J., L. C. MacKinnon, J. S. Goulding, N. H. Bean, and L. Slutsker.
2000. Surveillance for foodborne-disease outbreaks—United States, 1993–
1997. MMWR CDC Surveill. Summ. 49:1–62.
54. Osterholm, M. T., J. C. Forfang, T. L. Ristinen, A. G. Dean, J. W. Washburn,
J. R. Godes, R. A. Rude, and J. G. McCullough. 1981. An outbreak of
foodborne giardiasis. N. Engl. J. Med. 304:24–28.
55. Portnoy, B. L., P. A. Mackowiak, C. T. Caraway, J. A. Walker, T. W. McKinley, and C. A. Klein. 1975. Oyster-associated hepatitis: failure of shellfish
certification programs to prevent outbreaks. JAMA 233:1065–1068.
56. Potasman, I., A. Paz, and M. Odeh. 2002. Infectious outbreaks associated
with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis.
35:921–928.
57. Reeve, G., D. L. Martin, J. Pappas, R. E. Thompson, and K. D. Greene. 1989.
An outbreak of shigellosis associated with the consumption of raw oysters.
N. Engl. J. Med. 321:224–227.
58. Ruttenbur, A. J., B. G. Weniger, F. Sorvillo, R. A. Murray, and S. A. Ford.
1984. Diphyllobothriasis associated with salmon consumption in Pacific
Coast states. Am. J. Trop. Med. Hyg. 33:455–459.
59. Schantz, P. M. 1989. The dangers of eating raw fish. N. Engl. J. Med.
320:1143–1145.
60. Shapiro, R. L., S. Altekruse, L. Hutwagner, R. Bishop, R. Hammond, S.
Wilson, B. Ray, S. Thompson, R. Tauxe, and P. M. Griffin. 1998. The role of
Martha Iwamoto is a medical epidemiologist with the Division of
Healthcare Quality Promotion, National Center for Zoonotic and
Emerging Infections, Centers for Disease Control and Prevention
(CDC). Previously, she was a medical epidemiologist with the Enteric
Diseases Epidemiology Branch and worked with surveillance of foodborne bacterial infections. She is board certified in pediatrics and
preventive medicine. Her undergraduate education was at Davidson
College, Davidson, North Carolina; she received her medical degree at
Medical College of Georgia in Augusta, Georgia; and she received a
Master of Public Health degree from the Rollins School of Public
Health, Atlanta, Georgia. She completed her clinical training in pediatrics at the University of Virginia, Charlottesville, Virginia. She
trained in CDC’s Epidemic Intelligence Service and Preventive Medicine Residency Program.
Tracy Ayers is an analytical epidemiologist in the Division of FoodBorne, Bacterial and Mycotic Diseases at CDC. She served as a surveillance coordinator for the Hawaii State Department of Health for 4
years, where she had the opportunity to work on several large-scale
surveillance systems and analytical projects. She began her employment with the CDC in 2005 and has been involved in several crosscutting activities within the division, with a focus on food-borne
attribution.
SEAFOOD-ASSOCIATED INFECTIONS
61.
62.
63.
64.
65.
66.
67.
68.
69.
70.
411
Gulf Coast oysters harvested in warmer months in Vibrio vulnificus infections in the United States, 1988–1996. J. Infect. Dis. 178:752–759.
Shapiro, R. L., C. Hatheway, and D. L. Swerdlow. 1998. Botulism in the
United Sates: a clinical and epidemiologic review. Ann. Intern. Med. 129:
221–228.
Sobel, J., and J. Painter. 2005. Illnesses caused by marine toxins. Clin. Infect.
Dis. 41:1290–1296.
Tauxe, R. V. 1991. Salmonella: a postmodern pathogen. J. Food Prot. 54:
563–568.
Tauxe, R. V., and A. T. Pavia. 1998. Salmonellosis: nontyphoidal, p. 613–630.
In A. S. Evans and P. S. Brachman (ed.), Bacterial infection of humans:
epidemiology and control, 3rd ed. Plenum Publishing Corporation, New
York, NY.
Tranter, H. S. 1990. Foodborne staphylococcal illness. Lancet 336:1044–
1046.
Wainwright, R. B., W. L. Heyward, J. P. Middaugh, C. L. Hatheway, A. P.
Harpster, and T. R. Bender. 1988. Food-borne botulism in Alaska, 1947–
1985: epidemiology and clinical findings. J. Infect. Dis. 157:1158–1162.
Wasley, A., S. Grytdal, and K. Gallagher. 2008. Surveillance for acute viral
hepatitis—United States, 2006. MMWR CDC Surveill. Summ. 57:1–24.
Widdowson, M., A. Sulka, S. N. Bulens, S. Beard, S. S. Chaves, R. Hammond, E. Salehi, E. Swanson, J. Totaro, R. Woron, P. S. Mead, J. S. Bresee,
S. S. Monroe, and R. I. Glass. 2005. Norovirus and foodborne disease,
United States, 1991–2000. Emerg. Infect. Dis. 11:95–102.
Wittner, M., J. W. Turner, G. Jacquette, L. R. Ash, M. P. Salgo, and H. B.
Tanowitz. 1989. Eustongylidiasis—a parasitic infection acquired by eating
sushi. N. Engl. J. Med. 320:1124–1126.
Yoder, J., V. Roberts, G. F. Craun, V. Hill, L. Hicks, N. T. Alexander, V.
Radke, R. L. Calderon, M. C. Hlvasa, M. J. Beach, and S. L. Roy. 2008.
Surveillance for waterborne disease and outbreaks associated with drinking
water and water not intended for drinking—United States, 2005–2006.
MMWR CDC Surveill. Summ. 57:39–62.
Barbara E. Mahon received her M.D. and clinical training in pediatrics
from the University of California, San Francisco, and her M.P.H. from
the University of California, Berkeley. She trained in CDC’s Epidemic
Intelligence Service (EIS). Dr. Mahon leads the FoodNet and Outbreak Surveillance Team in the Enteric Diseases Epidemiology and
Surveillance Branch at the Centers for Disease Control and Prevention
(CDC). The team is responsible for the FoodNet active food-borne
disease surveillance system and for national surveillance for outbreaks
of food-borne disease. It conducts epidemiologic studies of the burden,
trends, and food source attribution of food-borne diseases caused by
Salmonella, Listeria, and Escherichia coli O157, among other pathogens. Dr. Mahon has a broad background in infectious disease epidemiology, as she has worked on food-borne diseases, vaccine-preventable diseases, and sexually transmitted diseases in academic and
industry positions as well as in government. She holds an adjunct
faculty appointment at the Boston University School of Public Health.
David L. Swerdlow is Senior Advisor for Epidemiology and Emergency
Response, National Center for Immunizations and Respiratory Diseases, Centers for Disease Control and Prevention. He has served in
the pandemic influenza H1N1 response since April 2009, as co-team
leader of the Regional and Epidemiologic Field Investigations Team
and co-team leader of the Epidemiology and Laboratory Task Force.
Previously, he was team leader of the National Surveillance Team,
Enteric Diseases Epidemiology Branch. The team conducted national
surveillance for food-borne bacterial infections, including seafoodassociated diseases. He is board certified in internal medicine and
infectious diseases. His undergraduate education was at the University
of California, San Diego, and he graduated from Harvard Medical
School in 1986. His internal medicine residency was at the University
of Washington, Seattle, and he completed his infectious diseases fellowship at the Massachusetts General Hospital in Boston. He was in
the Epidemic Intelligence Service at CDC from 1989 to 1991.