Microbes and Infection, 2, 2000, 1651−1660

© 2000 Éditions scientifiques et médicales Elsevier SAS. All rights reserved

S1286457900013216/REV

Review

The role of seafood in bacterial

foodborne diseases
Frerk Feldhusen*
State Veterinary Institute for Fish and Fishery Products, Schleusenstr., D-27472 Cuxhaven, Germany

ABSTRACT – Pathogenic bacteria, when present in marine seafood and in fresh cultured products,
are usually found at fairly low levels, and where these products are adequately cooked, food safety
hazards are insignificant. A few bacteria associated with faecal contamination of seafood continue to
pose a large-scale health threat through seafood. © 2000 Éditions scientifiques et médicales
Elsevier SAS
seafood hazards / bacteria / foodborne diseases

1. Introduction tamination with human or animal faeces or otherwise

Fishery products are of great importance for human
nutrition worldwide. The catch in 1996 was about 120
million tons, about 26% of which was of aquaculture
origin [1]. During the past 20 years there has been an
intensive global increase in fish farming. Approximately
90% of global aquaculture production is based in Asia.
Food safety issues associated with aquaculture products
differ from region to region and from habitat to habitat and
vary according to the method of production, management
practices and environmental conditions [2]. The microbial
status of seafood after catch is closely related to environ-
mental conditions and microbiological quality of the water:
water temperature, salt content, distance between locali-
sation of catch and polluted areas (human and animal
faeces), natural occurrence of bacteria in the water, inges-
tion of food by fish, methods of catch, and chilling condi-
tions.
Generally there are differences in the microbial status of
seafood depending on the locality of catch, i.e. from the
sea far from the coast, near the coast, or rivers and lakes far
or near the coast. Risks to consumer health from fishery
products from the unpolluted marine environment are
low. Potential food safety hazards of aquaculture products
vary according to the culture system and may include
foodborne trematode infections, foodborne disease asso-
ciated with pathogenic bacteria and viruses, veterinary
drug residues, and contamination by agrochemicals and
toxic metals. The hazards associated with human patho-
genic bacteria in finfish and crustaceans produced in
aquaculture can be divided into two groups: bacteria
naturally present in the aquatic environment, referred to as
indigenous bacteria, and those present as a result of con-
* Correspondence and reprints.
E-mail address: FeldhusenVUACux@t-online.de (Frerk Feldhusen).
introduced into the aquatic environment. Hazards may
also occur through the introduction of bacteria during
post-harvest handling or processing [2, 3].
During storage, indigenous spoilage bacteria will out-
grow the indigenous pathogenic bacteria, normally fish
will spoil before becoming toxic due to the presence of
greater amounts of pathogens. Pathogenic species of bac-
teria can be introduced into coastal regions and aquacul-
ture ponds by animal manure and human waste and are
usually found in fish and crustaceans after catch at fairly
low levels.
Apathogenic and pathogenic bacteria were found on
the skin, the gills and in the intestines of fish [4]. The
poikilotherm nature of fish allows a broad range of bacte-
ria to grow. The microflora of temperate water fish is
dominated by psychrotrophic Gram-negative rod-shaped
bacteria belonging to the genera Pseudomonas, Moraxella,
Acinetobacter, Shewanella, Flavobacterium, Vibrionaceae
and Aeromonadaceae. Shewanella putrefaciens and
Pseudomonas spp. are the specific spoilage bacteria of
iced fresh fish regardless of the origin of fish. Modified
atmosphere-stored marine fish from temperate waters are
spoiled by the CO2-resistant Photobacterium phosporeum,
whereas Gram-positive bacteria are likely spoilers of CO2-
packed fish from tropical waters [5].
Investigations in Spain [6] do not support the generally
accepted thesis about the influence of the environment on
the bacterial flora of fish. Thus, it was common that
microorganisms that predominated or that were a signifi-
cant part of the microflora recovered from the outer sur-
faces of fish were not detected among water isolates. The
variety of microorganisms in the intestinal tract is related
to the environment as well as to the quantity and origin of
food consumed by fish [7, 8]. Intestinal microflora of fresh
or sea water fishes consists mainly of aeromonas or vibrio
and aeromonas, respectively; while the predominant bac-

Microbes and Infection 1651

2000, 1651-1660
Review
Table I. German report on seafood-related pathogenic
bacteria 1996/1997 [11, 12].
Investigated
Pathogenic bacteria Positive samples
samples (n)
1996 1997 1996 1997
Salmonella 5 060 3 948 0.16% 0.66%
S. enteritidis 5 060 3 948 0.00% 0.08%
S. thyphimurium 5 060 0.02% 0.08%
Campylobacter jejuni 90 1.11%
L. monocytogenes 2 453 1 321 4.40% 14.84%
Y. enterocolitica 484 0.21%
E. coli, VTEC 291 0.00%
teria obtained from fresh or seawater samples were fla-
vobacterium or pseudomonas, respectively [9]. The intes-
tines of farmed rainbow trout yielded high numbers of
psychrotrophic bacillus and coryneformes (ca. 45%) [6].
2. Bacterial pathogens in seafood
At least ten genera of bacterial pathogens have been
implicated in seafood-borne diseases. Pathogenic bacteria
associated with seafood can be categorised into three
general groups [2–4]. These are i) bacteria which are
normal components of the marine or estuarine environ-
ment (indigenous bacteria): Vibrio cholerae, Vibrio parahä-
molyticus, Vibrio vulnificus, Listeria monocytogenes,
Clostridium botulinum and Aeromonas hydrophila (only
virulent strains); ii) enteric bacteria which are present due
to faecal contamination (nonindigenous bacteria): Salmo-
nella spp., pathogenic Escherichia coli, Shigella spp.,
Campylobacter spp., and Yersinia enterocolitica (very few
pathogenic serotypes); iii) bacterial contamination during
processing: Bacillus cereus (only toxigenic strains),
L. monocytogenes, Stapylococcus aureus and Clostridium
perfringens.
Indigenous pathogenic bacteria, when present in fresh
cultured products, are usually found at fairly low levels,
and where these products are adequately cooked, food
safety hazards are insignificant.
A few bacteria associated with faecal contamination of
seafood continue to pose a large-scale health threat
through seafood consumption. The development of guide-
lines to minimize faecal contamination of shellfish and
harvesting waters has greatly reduced the incidence of
enteric bacteria in seafood [10]. However in the European
Community, Germany, and other parts of the world these
bacteria are still isolated from various seafoods, indicating
the potential for transmission to humans (tables I and II).
The live animals are caught in the sea or fresh water,
handled and (in most cases) processed without any use of
additives or chemical preservatives and finally distributed
with chilling or freezing as the only means of preservation.
Most fish and crustaceans are cooked before eating
although a few countries (e.g., Japan) have a tradition of
eating raw fish. The epidemiological records show that
fish cooked immediately before consumption have caused
1652
Feldhusen
a number of food poisoning outbreaks, but nearly all
related to the presence of heat-stable toxins (e.g., biotoxins
and histamine) [13]. Live fish and crustaceans may be
contaminated with a number of pathogenic bacteria nor-
mally found in the aquatic environment such as C. botu-
linum, various Vibrio spp., L. monocytogenes and Aero-
monas spp. However, only the growth of these organisms
can be regarded as a hazard. The severity of diseases
related to these organisms may be high (botulism, cholera)
or low (Aeromonas infections), but the likelihood of pro-
voking diseases (risk) is very low. The pathogenic strains
mostly require temperatures > 5 °C for growth and they
are competing with the normal spoilage flora which pro-
liferate comparatively more rapidly at low temperatures.
Thus the products are likely to be spoiled before produc-
tion of toxin or development of high numbers of patho-
gens. When the products are cooked before consumption,
and afterwards no recontamination takes place, this will
completely eliminate the risk, as the bacteria and their
toxins are heat sensitive.
2.1. Vibrio spp.
Vibrio spp. are very common in estuarine and coastal
environments, and a number of these organisms are human
pathogens. They are particularly prevalent in tropical
waters and can be isolated in temperate zones during the
summer months [3]. The presence does not correlate with
faecal contamination [14]; if anything, there are sugges-
tions that vibrios are more common in clean, ‘pristine’
areas away from sewage outflows. Vibrios are a frequent
isolate from seafood and, in particular, shellfish. V. chol-
erae, V. parahaemolyticus, and V. vulnificus are univer-
sally recognised as important human pathogens (table III);
with V. hollisae, V. alginolyticus, V. fluvalis and V. mim-
icus each responsible for a smaller, but substantial, num-
ber of cases [16].
V. cholerae (table IV) is the aetiological agent of chol-
era, a devasting disease that can cause severe, dehydrating
diarrhoea and death in healthy people. Cholera toxin
(CT)-producing, human illness associated strains have
tended to be within V. cholerae O group 1 or O group 139.
CT-producing, ‘epidemic’ O1 V. cholerae strains can be
isolated from the environment. In Peru investigations [17]
have shown that counts of CT-producing strains in the
environment correlate significantly with the number of
cholera cases reported in the community two months
later; the initial risk in counts in the environment appears
to be linked with increases in water temperature. The
organism may be transmitted from the environment to
humans by a number of routes, including consumption of
undercooked seafood or shellfish. In the South American
epidemics in 1991, ceviche (a marinated, raw fish dish)
was initially implicated epidemiologically as a vehicle of
transmission, while crabs have been repeatedly impli-
cated as the source of US Gulf coast-associated cholera
cases [18]. V. cholerae strains which lack the genetic
potential for causing epidemic disease have generally
been referred to as non-O group 1, or non-O1 V. cholerae.
In work done by the US Food and Drug Administration
(FDA), V. cholerae non-O1 were isolated from 14% of
freshly harvested oyster lots [19, 20]. V. cholerae O1 and
Microbes and Infection
2000, 1651-1660
The role of seafood in bacterial foodborne diseases Review

Table II. Pathogenic bacteria in rejected seafood imports into the European Community in the years 1998/1999, rapid
alert system of EC.
Argentina 1 frozen fish Vibrio cholerae
Aserbaidschan 1 sevruga caviar Staphylococcus spp.
Bahrain 1 frozen prawns Salmonella spp.
Bangladesh 4 frozen shrimps Vibrio cholerae (4)
Chile 2 frozen mackerels, frozen fillets Salmonella spp. (2)
China 28 frozen crustaceae, fish fillets, squid Vibrio cholerae (9), Vibrio parahaemoyticus (2),
Salmonella spp. (9), Salmonella dublin (1),
Salmonella enteriditis (1), Staphylococcus aureus
(3), Vibrio fluvalia (1), Vibrio vulnificus (1), Bacillus
cereus (2)
Ivory Coast 3 frozen squid, fishfillets, tuna Salmonella spp. (2), Vibrio parahaemolyticus (1)
Ecuador 2 frozen shrimps Vibrio parahaemolyticus, Vibrio alginolyticus
Ghana 1 tuna Salmonella senftenberg
Guinea 2 fish fillets Salmonella spp. (2)
India 10 frozen squids, frozen shrimps Salmonella spp. (3), Salmonella barelly (1), Vibrio
parahaemolyticus (3), Vibrio cholerae non-O1 (2),
Vibrio cholerae (1)
Indonesia 3 frozen shrimps, frozen squids, frozen frogs legs Salmonella spp. (3)
Mozambique 2 frozen prawns Vibrio parahaemolyticus, Salmonella spp.
Nigeria 1 frozen crustaceae C. botulinum
Pakistan 1 frozen crustaceae coagulase-positive staphylococcus
Senegal 12 frozen squids, frozen fish, frozen shrimps, frozen Salmonella (8), Vibrio parahaemolyticus (3), Vibrio
tuna cholerae (1)
Sri Lanka 1 shrimps Vibrio parahaemolyticus, Vibrio cholerae,
Salmonella weltewreden u. thomson
Tanzania 4 frozen squid, frozen crustaceae, frozen fillets Salmonella spp. (3), Vibrio parahaemolyticus (1)
Thailand 16 mussels, frozen fish, frozen squids, frozen shrimps Vibrio parahaemolyticus (9), Vibrio cholerae (5),
Vibrio cholerae non-O1 (1), Vibrio cholerae non-O2
(1), Salmonella augustenborg (1), Salmonella spp.
(2), Salmonella paratyphi B (1)
Turkey 7 frozen squids and shrimps, frozen crustaceae, frozen Staphylococcus aureus (2), Vibrio cholerae (2),
fish, frozen tuna, frozen snails Vibrio cholerae non-O1 (1), Salmonella spp. (1),
Vibrio parahaemolyticus (1), E. coli (1), Listeria
monocytogenes (1)
Uganda 4 frozen fish fillets Salmonella spp. (4), Vibrio cholerae (1)
USA 1 salmon Salmonella spp.
Vietnam 12 frozen crustaceae, frozen shrimps, squids, tuna Salmonella spp. (6), Vibrio parahaemolyticus (2),
Vibrio cholerae non-O1 (3), Vibrio cholerae (1)

non-O1 was isolated in brackish water cultured shrimp in significance of these isolates [16]. Preventing seafood-
Southeast Asia (2 and 33%) and in cultured shrimp in India associated cholera in the long term will depend on main-
[2]. In the absence of a clear method for differentiating taining sewage-free harvest beds and improving sanitation
pathogenic from non-pathogenic V. cholerae non-O1 in processing plants. In coastal areas where the organism
strains, it becomes very difficult to assess the clinical persists in the environment, even in the absence of sewage
contamination, education to discourage the consumption
of raw or undercooked shellfish is also needed.
Table III. Bacterial hazards associated with seafood in V. parahaemolyticus (table IV) is the most commonly
the United States [15]. isolated ‘non-cholera’ vibrio. In Japan, it has been impli-
cated as a cause of at least a quarter of total foodborne
Annual Annual diseases. In India V. parahaemolyticus was isolated in
Hazard
reported cases estimated cases
3.5–23.9% of patients with diarrhoea [16]. In outbreak
Campylobacter jejuni 2 200 studies infection has been linked with consumption of
Clostridium botulinum 4 10 seafood [21]. V. parahaemolyticus frequently has been
Clostridium perfringens 7 200 detected in tropical and subtropical regions. Growth is
Vibrio spp. (excl. V. vulnificus) 43 1 000 possible at temperatures > 15 °C. It has been isolated from
Vibrio vulnificus 24 60
the coastal regions of the North Sea and Baltic Sea of
Non-typhi Salmonella 2 200
Shigella 7 200
Germany [22], and 77% of oysters from Brazil and 25% of
shelled frozen prawns have been contaminated [23, 24].

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2000, 1651-1660
Review Feldhusen

Table IV. Bacterial pathogens in seafood [4].

Estimated minimal
Bacteria Symptoms Associated seafood Importance
infectious dose
C. botulinum Typ E 0.1–1 µg toxin weakness, visual spores on surface, in intestine, on worldwide, ubiquitous in
lethal dose defects, death by gills (trout, herring, salmon); aquacultures, seawater, freshwater,
respiratory vacuum packaged smoked fish little risk for correctly chilled
paralysis, cardiac products, cans products (production of toxin > 6 °C),
arrest botulism rarely associated with
seafood
C. perfringens 106–108 CFU/g diarrhoea, seldom sporadic some cases in USA
lethal
Salmonella spp. 102 CFU/g depends vomiting, in intestine (tilapia and carp); worldwide by faecal contamination,
on species diarrhoea, fever, prawns, molluscs, alaska pollack; Asia, Africa, USA, South America,
seldom lethal eel and catfish Europe, normally small risk (heating
of seafood)
Shigella spp. 101–102 CFU/g dysentery shellfish hazard in USA, Mexiko (uptake of
raw seafood)
Campylobacter 101–102 CFU/g diarrhoea shellfish USA, small hazard, few infections
jejuni
Yersinia (107–109 CFU/g) diarrhoea, fish, shellfish form aquacultures infections?
enterocolitica vomiting, fever
Staphylococcus toxin level 105–106 vomiting, contamination from infected frequency of intoxication unknown
aureus CFU/g 0.14–0.19 diarrhoea, persons
µg/kg bodyweight weakness
Bacillus cereus 106–109 CFU/g vomiting, diarrhoea for example marinades rare, small hazard
Vibrio cholerae 103 to 108–109 cholera prawns, shellfish, squid, seafood epidemic in Asia, Africa, South
Serovar O1 and CFU/g America, small hazard for healthy
O139 people
Non-O1 strains weak small hazard for healthy people
gastroenteritis
V. parahaemolyticus 105–106 g CFU/g diarrhoea, nausea, at coastal areas in sediment, frequent reason of seafood related
vomiting plankton, in the seawater at warm infections in some regions of the
temperature < 1 000 CFU/mL world, India, Japan, South Asia
(North Sea, Baltic Sea) shellfish,
crustaceaens on the skin, gills,
intestine
V. vulnificus wound infection, Europe? water > 20 °C, fish, in Germany no seafood related cases,
death by mussels, oysters, prawns seafood related cases especially
septicaemia known from USA
L. monocytogenes > 102 CFU/g acute septicaemia ubiquitous, 3–10% human infections related to seafood rare,
in new-born carriers; rarely in seawater or small hazard
children, seawater fish, more frequently in
meningitis, local freshwater and aquaculture fish,
infections cold smoked products, salted fish
products, hot smoked products,
raw fish, prawns, mussels, oysters

In Germany in 1997 a total of 1 539 samples of fish
including shellfish were investigated. Members of the
family Vibrionaceae were isolated in 344 (21.6%) cases
[25]. 2.4% (n = 37) of the samples (frozen raw and heated
shrimp and frozen squid) were V. cholerae-positive.
V. parahaemolyticus could be isolated in 2.6% (n = 40) of
the samples (frozen Alaska pollock fillets and mush, raw
and heated frozen shrimp, fresh mussels). Data from Euro-
pean border inspection show a number of seafood samples
with V. parahaemolyticus isolated. Increasing efforts to
improve hygienic conditions and the quality assurance
systems should be able to reduce this problem within the
next decade.
V. vulnificus (table IV) can cause serious illness and
death in persons with pre-existing liver disease or compro-
1654
mised immune systems. Biotype 1 of this bacterium can be
lethal to humans, biotype 2 is known to be pathogenic for
Asian and European eels and may be an opportunistic
pathogen for humans. V. vulnificus can cause wound infec-
tions and primary septicaemia (septicaemia resulting from
ingestion of the organism without any other obvious
source, such as a wound). The ingestion of raw oysters or
the exposure of wounds to seawater are the major causes
of human infection. Human infections from this organism
are rare and the population most at risk are those with
underlying illnesses or who are immunocompromised.
V. vulnificus is a ubiquitous bacterium and part of the
normal microflora of marine environment. The presence
of V. vulnificus is strongly correlated with water tempera-
ture. It is also a natural inhabitant of the intestinal tract of
Microbes and Infection
2000, 1651-1660
The role of seafood in bacterial foodborne diseases
oysters (Crassostrea virginica). During the unusually warm
summer in Denmark in 1994, 11 clinical cases of V. vulnifi-
cus infection were reported [26]. Authors from Israel [27]
reported 49 patients with a wide variety of hand infec-
tions, which developed after injuries from St Peter’s fish
(Tilapia zillii). Some skin or wound contamination cases
due to V. vulnificus have been described in Belgium,
Denmark, Germany, Spain, Sweden and The Netherlands.
The organism is the leading cause of seafood-related infec-
tions (table III) and of shellfish-associated deaths in the US
[16]. In the US, from 1981 through 1992, 125 persons with
V. vulnificus infections, of whom 44 (35%) died, were
reported to the human health authorities in Florida. Of the
40 deaths caused by septicaemia, 35 (88%) were associ-
ated with raw oyster consumption. Nine of these deaths
occurred in 1992. V. vulnificus has been isolated in the US
along the Gulf coasts [28]. During the winter, densities of
V. vulnificus were low and the organism was isolated
more frequently from sheepshead fish than from sediment
and seawater. From April to October V. vulnificus densi-
ties were considerably higher (2–5 logs) in estuarine fish
than in surrounding water, sediment, or nearby oysters and
crustacea. Highest densities were found in the intestinal
contents of certain bottom-feeding fish, particularly those
that consume molluscs and crustaceans. V. vulnificus was
found infrequently in offshore fish. In Europe, V. vulnificus
was found in British coastal waters and up to the Baltic
Sea. A recent Danish study showed the occurrence of
V. vulnificus in eels of a Danish eel farm which used
brackish water [29]. V. vulnificus was found in mussels in
seven of 17 samples analysed. It was also isolated from
gills, intestinal contents, and mucus from wild fish.
As the consumption of raw oysters is a tradition in
European countries, it is very interesting to observe that
any cases of foodborne infection due to the consumption
of raw oysters have never been signalled in European
countries. Nevertheless food and public health authorities
in Europe should observe the further developments in this
field.
2.2. L. monocytogenes
During the last 15–20 years there has been an increas-
ing concern worldwide about L. monocytogenes and its
implications for food safety. Several large well-documented
outbreaks and sporadic cases have been described and
L. monocytogenes has been isolated from a wide range of
raw and ready-to-eat meats, poultry, dairy products, veg-
etables and seafoods.
L. monocytogenes is widespread in nature and can be
found in soil, foliage and the faeces of animals and humans.
The prevalence in food animals seems to be between
1–10% and a typical report is from Germany in 1997
where 49 324 samples from food animals were analysed
and 1 800 samples (4%) were found positive for L. mono-
cytogenes [30]. Listeria spp., including L. monocytogenes
have been isolated from processed seafood products such
as cooked and frozen seafood, marinated fish, surimi
products, sushi and smoked fish. A sampling survey on
ready-to-eat fish products at both the wholesale and retail
level indicated that shrimp and smoked salmon are often
contaminated with L. monocytogenes (6–36%) [13,
Microbes and Infection
2000, 1651-1660
Review
32].The German Zoonosis Report of 1997 [12] indicates
that in 14.8% of 1 321 investigated samples of fishery
products L. monocytogenes could be found (table I). Inves-
tigations in fish-smoking plants indicate that raw fish espe-
cially from aquacultures or polluted marine seawater from
coastal sites is contaminated. Earlier investigations of fresh
and frozen fish show L. monocytogenes-positive results in
< 50%, of processed fish < 26%, of prawns < 20% and of
shellfish < 7.5% [13].
Several studies indicate that humans can be carriers of
L. monocytogenes; a prevalence between 5–10% has been
indicated [33]. Some investigations show that L. moncy-
togenes can establish itself within a processing factory as
an in-house bacteria. Like other bacteria L. monocytoge-
nes can create a biofilm on stainless steel surfaces and can
be isolated from equipment, cold stores and floors [34].
Food receiving a heat treatment can be recontaminated in
the production environment. In-house reservoirs of listeria
have been reported from fish-processing establishments.
Some production plants can function without L. monocy-
togenes problems, while comparable plants have continu-
ous problems [35]. L. monocytogenes is a psychrotrophic
pathogen and is capable of growth at refrigerator tempera-
tures (> 0 °C). The minimum pH for growth in foods is
4.6–5.0 [36], the maximum NaCl concentration is about
10%. L. monocytogenes can grow under aerobic,
microaerophilic, and anaerobic conditions, and under
vacuum [37]. The combination of several ‘hurdles’ such as
salting, smoking, vacuum packaging, storage at chilled
temperatures and addition of preservatives has been used
to maintain food safety and increase the shelf-life of these
products. L. monocytogenes survived but did not grow on
raw salmon stored at 4 °C for 3 weeks or at 5 °C for 6 days,
whereas after a 10-day lag phase more than 1 log count
growth on raw cod fillets was recorded after 17 days of
storage at 5 °C [31]. A number of studies have shown that
the growth rate of L. monocytogenes in cold smoked
salmon (vacuum packed, 3–5% water-phase NaCl) stored
at 5 °C is in the order of 1–2 log cycles per week [38].
In Germany there are an estimated 200 cases of listerio-
sis per year for a population of 80 million [39]. At present
there are no reports on epidemic outbreaks due to con-
sumption of fish products worldwide, and a causal asso-
ciation between sporadic cases of listeriosis and contami-
nated fish products was rarely established.
L. monocytogenes has been identified as the causative
agent in four sporadic cases of seafood-borne listeriosis
[40–43] and has been suspected to be the causative agent
in at least two other outbreaks involving seafood [44, 45].
The overall risk of listeriosis to the human population
appears to be around 1–10 per million per year based on
internationally published incidence data. At the present
time it is difficult to state the risk relative to the relevant
food commodities. At present no sub-typing systems seem
to offer the possibility of relating specific human strains to
specific food types. This would correspond to the patho-
gen account principle applicable to Salmonella spp. [30].
Several European countries have concluded that a com-
plete absence of L. monocytogenes for certain ready-to-
eat foods is an unattainable and unrealistic requirement
that would restrict food production and consumption with-
1655
Review
out having a positive impact on public health. Conse-
quently such risk management action might detract
resources from other potentially more efficient measures
against L. monocytogenes [30]. The scientific committee
of the EU [30] therefore concluded that L. monocytogenes
levels above 100 CFU/g may be reached after in-food
growth. Risk management efforts should be focused on
those food commodity types where L. monocytogenes can
multiply. The potential for accidents in production should
not be neglected.
2.3. C. botulinum
C. botulinum (tables II and III) is a spore-forming bac-
terium that grows at anaerobic conditions. The spores
survive normal cooking temperature and the bacteria grow
in a vacuum-packaged and modified atmosphere environ-
ment. C. botulinum produces a neurotoxin that causes
botulism, a disease that attacks the central nervous system
of humans and can cause death within 3–6 days of inges-
tion if not properly treated [46].
The C. botulinum type E that is most common on fish
and fishery products is of particular concern because it
grows at temperatures as low as 3–5 °C and produces little
noticeable evidence of spoilage. Proper thermal processes
for canned seafood destroy the spores (80 °C, 15 min.)
and the heat-labile toxin (80 °C, 6 min.). Heavy salting or
drying to reduce the water activity below 0.93 and fer-
mentation or acidification to below pH 4.7 are effective
means of preventing C. botulinum growth.
C. botulinum is ubiquitous in aquatic environments
and has been isolated from water, ocean sediments, the
intestinal tracts of fish, and the gills and viscera of crabs
and other shellfish [47]. C. botulinum spores can also
adhere to the surface of fish. For these reasons C. botuli-
num can be found in the environment of most fish proces-
sors and cannot be totally eliminated using reasonable
means. Moreover, even though a fish might be cleaned,
gutted, and air packaged, some risk will still exist because
C. botulinum spores can find their way into muscle tissue
during processing. Muscle tissue below the surface of fish
can provide an anaerobic environment where outgrowth
and toxin production can occur if time and temperature
permit [15].
Investigations on growth and toxigenesis by C. botuli-
num type E in vacuum-packaged unprocessed, raw pick-
led and cold smoked rainbow trout stored at slightly
abusive temperatures were recently compared to predic-
tions generated by two currently available predictive
microbiological programmes. The results demonstrate the
need for further development and rigorous validation of
the models before they are accepted for wider use by
inspecting officials and the food industry [48]. Because
C. botulinum produces heat-resistant spores and requires
the absence of oxygen for growth, botulism has been most
commonly associated with improperly canned food (usu-
ally home canned). Semi-preserved seafoods including
smoked, salted and fermented fish, have also been identi-
fied as causes of botulinum. From 1980 to 1994 three of
four seafood-associated deaths in New York were caused
by C. botulinum [20]. Despite adequate understanding of
how foodborne botulism may be avoided, outbreaks still
1656
Feldhusen
occur, particularly among people consuming certain high-
risk or ethnic foods. In Israel and New York an outbreak of
fishborne botulism caused by C. botulinum type E with
eight cases was reported [49]. The cases resulted from the
consumption of ribbetz or kapchunka, a freshwater white-
fish soaked in brine and air-dried, that was processed
commercially in New York. The oldest victim died. In
April 1991 91 hospitalized patients in Cairo were reported
with botulism type E intoxication; 18 patients died [50].
The outbreak was associated with eating faseikh (unevis-
cerated, salted mullet fish). On January 1997 two Germans
got botulism after eating hot-smoked Canadian whitefish
produced in Finland [51]. The prevalence of C. botulinum
type E gene in fish and fishery products of commercial
importance in Finland was determined using a PCR analy-
sis. The contamination level in 438 raw fish samples from
intestines, surface and whole fish and 208 fish roe samples
varied from 10–40% and from 4–14%, respectively,
depending on the fish species studied. Five percent of 214
vacuum-packaged, and 3% of 123 air-packaged fishery
product samples were positive for the neurotoxin type E
gene. A contamination level of 10% in vacuum-packaged
hot-smoked whitefish was detected. The results demon-
strate that C. botulinum type E poses a serious health risk
for those consuming fishery products from the Baltic Sea
[52]. Temperature monitoring and the use of time–tem-
perature indicators are to be recommended in order to
ensure adequate storage temperature from processing to
consumption. Allowing the use of nitrate and nitrite
together with sufficiently high NaCl concentration in this
particular product should also be considered. The safety
problems associated with vacuum-packaged hot-smoked
fish seem to be of utmost concern and the product is one of
the most important botulism food vehicles processed on
an industrial scale.
2.4. Aeromonas spp.
Aeromonas spp. are widely found in aquatic environ-
ments. Some strains are important fish pathogens in aquac-
ulture [53], while oysters have been implicated in food-
borne disease [54]. Mesophilic Aeromonas spp. are
increasingly recognized as pathogens. Bacteria of this
group can be associated with sometimes fatal infections in
humans after contact with fish or water. Persons at risk are
patients with chronic or malignant diseases, immunocom-
promised hosts and children. Mesophilic Aeromonas spp.
are isolated regularly from cases of gastrointestinal infec-
tion and have markers indicative of enteropathogenicity
[55]. Results from Bangladesh indicate that Aeromonas
infection is common in young children presenting with
diarrhoea [56]. Swiss results show 10.9–14.3% positive
samples from hot- and cold-smoked fish and 10.5% posi-
tive samples from graved salmon. The high contamination
rate of cooked or hot-smoked foods suggests recontami-
nation after cooking or smoking, e.g., at the slicing and
packaging stage. 61.2% of the identified strains were
Aeromonas hydrophila, followed by 22.5% Aeromonas
caviae and 16.3% Aeromonas sobria [57]. Psychrotropic
Aeromonas strains are able to grow at 4–5 °C and to
produce toxins in oysters at 5 °C [58]. In investigations
from Finland [59] Aeromonas spp. were identified in 27
Microbes and Infection
2000, 1651-1660
The role of seafood in bacterial foodborne diseases
(93%) samples of 29 fish, in 17 (100%) samples of fish
eggs, in two (16%) out of 12 shrimp samples and in 23
(100%) freshwater samples. A. hydrophila hybridization
group (HG) 1, A. caviae HG 4, A. veronii subspecies
sobria or subspecies veronii HG8/10 known to be associ-
ated with human diarrhoea were uncommon in all
samples. During two suspected foodborne outbreaks three
strains of A. hydrophila HG 2 and HG 3 were isolated
from frozen shrimp. The results suggest that Aeromonas
strains could be of public health significance in food
products that have an extended shelf-life at refrigeration
temperature.
2.5. Salmonella spp.
Salmonella are among the most important causes of
gastrointestinal disease worldwide and many seafood-
importing countries will restrict the import of raw food
products containing these pathogens. Salmonella can
occur both in water, especially of contaminated coastal
regions or ponds, and in the fresh fish from these areas, but
low incidence and even absence is not uncommon. Fish
from offshore marine regions normally is not contami-
nated with Salmonella spp. The presence of salmonella in
water depends on many factors, for instance the pollution
from a nearby poultry farm. Contamination of Nile perch
with Salmonella spp. could be associated with cattle and
human hygienic conditions near the landing sites. The
presence of multiple antibiotic-resistant pathogenic bac-
teria in surface and pond waters as well as in fish is of
serious concern because it may hamper the efficiency of
important medical drugs. The fact that resistance charac-
teristics can be transferred to non-resistant recipient cells
adds yet another dimension to this problem [6]. Salmo-
nella spp. have been detected in the gut of tilapia and carp
[60–62]. A survey in Japan has shown that Salmonella
species were present in 21% of eel culture ponds [63]. In
the US, freshwater cultured catfish have been found to
harbour Salmonella species, with an overall incidence
rate of about 5% [64]. Aquatic birds are known to harbour
strains of Salmonella, and have been suggested as one
possible means of spreading this organism from area to
area [65]. The occurrence of salmonella in brackish water
ponds was monitored over a 2-year period in one of the
major prawn-exporting countries in Southeast Asia [66].
Salmonella were present in 16% of prawns and 22.1% of
mud/water samples. S. weltevreden was identified as the
principal serotype found in ponds, and to a lesser extent
S. anatum (11%) S. wandsworth (8%) and S. potsdam (8%).
In India, S. typhi was the most predominant among Sal-
monella isolates and S. paratyphi B biovar Java heavily
contaminated samples of marine prawns in Calcutta mar-
kets [67].
In the 1990s occurrence of human cases of salmonel-
losis increased; the predominant serovar in Europe was
S. enteritidis. In Germany [12] in 0.66% of fishery prod-
ucts, salmonella has been found (table I) – S. enteritidis
only a few times; therefore the risk of S. enteritidis infec-
tion from raw or contaminated processed fishery products
is quite low. In the US, non-typhoidal salmonellae have
been associated with fish and shellfish, S. paratyphi and
S. enteritidis with shrimp and bivalves. S. typhi was the
Microbes and Infection
2000, 1651-1660
Review
most common bacterium associated with shellfish-
vectored disease. Due to more effective surveillance and
improved water quality, the incidence of S. typhi in shell-
fish harvested in the US has declined. The risk of S. typhi
infection from shellfish is still quite low in the US; how-
ever, infections continue to occur in other parts of the
world. In the UK, S. typhi was detected in more than 1.6%
of shellfish sampled from open harvesting waters [10,
68–70].
Generally, disease surveillance reports from public
health authorities in Europe and North America indicate
that human salmonellosis associated with the consump-
tion of farmed freshwater and marine fish and crustaceans
occurs very rarely compared to those associated with
other foods, for instance poultry products [2]. On the basis
of available evidence, strains isolated from most human
cases of salmonellosis appear to be different from those
found in farmed products [66], leading to the conclusion
that these products constitute a very low risk to public
health. Evidence exists to suggest that certain serotypes of
Salmonella are part of the indigenous microflora of fish
farms (table II) and these pose minimal risks to public
health as most crustaceans and other seafood are cooked
prior to consumption [3]. On the other hand, European
border inspection results show identification of Salmo-
nella spp. in heated products related to cross-
contamination (table II).
2.6. Pathogenic E. coli
E. coli is often used as an indicator of faecal contami-
nation. The bacteria have been isolated from unpolluted
warm tropical waters where they are part of the natural
microflora [71]. Some strains are also capable of causing
foodborne disease. Shiga toxin-producing E. coli (STEC)
O157:H7 infection, which can cause haemolytic uraemic
syndrome and death, is a global public health concern.
Patients younger than 5 years of age are at high risk for
haemolytic uraemic syndrome [72]. Where animal
manures, particularly bovine, are used as pond fertilizers,
there is a risk that pathogenic strains of E. coli may be
present in the pond water [2]. For instance there is good
evidence of waterborne infection by E. coli O157:H7
[73]. In 1997, German investigations of seafood samples
showed no contamination with E. coli O157:H7 (table I),
but in the future the situation (especially for raw shellfish)
has to be observed.
2.7. Campylobacter spp.
Campylobacter jejuni, an emerging foodborne patho-
gen not recognized as a cause of human illness until the
late 1970s is now considered one of the leading causes of
foodborne bacterial infection (table IV). An estimated four
million C. jejeuni infections occur each year in the US.
Incidence of campylobacteriosis is particularly high among
young men. The high incidence in this group may reflect
poor food preparation skills [74]. Campylobacter are not
part of the normal flora of unpolluted aquatic environ-
ments. However these organisms are frequently isolated
from waste water. There is little information on the occur-
rence of Campylobacter spp. in aquaculture, although the
use of raw manures for fertilizing ponds may constitute a
1657
Review
public health risk in inland and coastal environments.
Some reports exist on the occurrence of campylobacter in
shellfish, but there is insufficient information about its
occurrence in farmed finfish and crustaceans. Campylo-
bacter has a short survival time in marine waters. How-
ever, the survival rate increases dramatically within shell-
fish, suggesting a protective relationship [75, 76]. In Ireland
thermophilic Campylobacter spp. were found in 42% of
380 shellfish. These findings show that classification on
the basis of indicator microorganisms alone is not suffi-
cient to assure the absence of bacterial pathogens. There-
fore microbiologists should consider whether tests for
pathogens such as campylobacter should be included
when determining the suitability of shellfish for human
consumption [76]. Available data suggest that the risk of
Campylobacter infection associated with the consump-
tion of farmed fish products is low [2].
2.8. Shigella spp.
In the US, shigella was implicated in 111 shellfish-
related cases and four outbreaks from 1898 to 1990 [10].
In 1994 and 1995 the FDA [15, 69] reported seven cases of
Shigella infections associated with seafood per year and
200 estimated cases per year (table III). In Mexico, 200
Shigella-related cases were reported in 1994 [69]. The
bacteria have been isolated in shellfish. Shigella may be
an important potential disease agent as it has a low infec-
tious dose and long survival time in clams and oysters
[68].
2.9. Y. enterocolitica
Y. enterocolitica infections result in appendicitis-like
symptoms, including fever and abdominal pain, accom-
panied by diarrhoea or vomiting. Most Yersinia infections
are not associated with a seafood vector [10]. However,
strains of Y. enterocolitica have been identified in fish and
shellfish in both wild and aquaculture settings [68, 77].
Additionally, yersinia is a psychrotrophic bacterium which
can multiply at low temperatures. This may increase the
potential for cold-stored or frozen seafood to become a
vector for human illness, but no report about outbreaks
related to seafood could be found.
2.10. B. cereus
B. cereus, an infectious cause of foodborne illness,
accounted for 2% of outbreaks with confirmed aetiology
that were reported to the Centers for Disease Control and
Prevention of the US FDA during 1973–1987 [78]. The
bacterium causes two types of illness – diarrhoeal and
vomiting (emetic) types. A wide variety of foods including
meats, milk, vegetables, and fish have been associated
with the diarrhoeal type food poisoning. In 1981, eight
outbreaks were reported which primarly involved rice and
shellfish. Other outbreaks go unreported or are misdiag-
nosed because of symptomatic similarities to S. aureus
intoxication (B. cereus vomiting type) or C. perfringens
food poisoning (B. cereus diarrhoeal type). In German fish
plants B. cereus could be identified in herring marinades
after addition of contaminated spices. The bacillus spores
could sporulate because of incorrect chilling after finish-
ing the pasteurizing process (unpublished results).
1658
Feldhusen
3. Conclusions
Due to the production and consumption conditions of
seafood in Europe and the activities of the European
food-related authorities, there are little bacterial risks in
Europe. Seafood investigations of imports into the Euro-
pean Community show contamination with human patho-
gens, i.e. Salmonella spp. and Vibrio spp. Reducing the
number of seafood-related outbreaks worldwide will
require continued and coordinated efforts by many differ-
ent agencies, including those involved with water quality,
disease surveillance, consumer education, and seafood
harvesting, processing, and marketing. A basic demand is
to increase the bacteriological quality of seafood through
the general implementation of hazard analysis and critical
control point system worldwide for the complete food
chain from water to table.
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