Food Research International 45 (2012) 780788

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Food Research International

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / f o o d r e s

Review

Incidence and role of Salmonella in seafood safety

G. Amagliani , G. Brandi, G.F. Schiavano
Dipartimento di Scienze Biomolecolari, Sez. di Scienze Tossicologiche, Igienistiche e Ambientali, Universit degli Studi di Urbino Carlo Bo, Italy

a r t i c l e

i n f o

Article history:
Received 15 February 2011
Accepted 7 June 2011
Keywords:
Salmonella
Seafood
Incidence
Aquaculture
Public health
Prevention strategies

a b s t r a c t
Seafood products are appreciated worldwide for their high nutritional value and are increasingly popular
among consumers. Consumer preferences range from fresh products, eaten raw or minimally processed, to
variously prepared (salted, smoked, cured, canned) and ready-to-eat (RTE) products. Moreover, seafood
products are a major food category in international trade and are frequently shipped very long distances. All
these factors expose seafood to various contaminants, including those of microbiological origins, such as
Salmonella. The presence of Salmonella in seafood may derive from contamination occurring in the natural
aquatic environment, in aquaculture or during processing. In addition, the isolation of Salmonella serovars that
are resistant and multiresistant to antibiotics continues to raise concerns. In this review various aspects
associated with the microbiological risk posed by the presence of Salmonella in seafood are examined. The
most recent data of incidence are presented, and some prevention and control strategies are considered.
2011 Elsevier Ltd. All rights reserved.

Contents
1.

Introduction . . . . . . . . . . . . . . . . . . .
1.1.
Search strategy and selection criteria . . . .
2.
Seafood consumption . . . . . . . . . . . . . . .
3.
Microbiological risk associated with seafood . . . .
4.
General aspects of Salmonella . . . . . . . . . . .
5.
Salmonella in the aquatic environment and live sh.
6.
Epidemiological data . . . . . . . . . . . . . . .
6.1.
Data from the EU . . . . . . . . . . . . .
6.2.
Data from the US . . . . . . . . . . . . .
6.3.
Data from India and other Asian countries. .
7.
Risks associated with aquaculture . . . . . . . . .
8.
Salmonella contamination and the sh trade . . . .
9.
Antimicrobial resistance. . . . . . . . . . . . . .
10.
Seafood safety control . . . . . . . . . . . . . .
11.
Conclusions . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction
In addition to being a healthy food with high nutritional value,
seafood can be associated with potential risks, particularly those
related to microbiological contamination. Salmonella has been
Corresponding author at: Universit di Urbino Carlo Bo, Dipartimento di Scienze
Biomolecolari, Sez. di Scienze Tossicologiche, Igienistiche e Ambientali, v. S. Chiara, 2761029 Urbino, Italy. Tel.: + 39 0722 303540; fax: + 39 0722 303541.
E-mail address: [email protected] (G. Amagliani).
0963-9969/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2011.06.022

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780
781
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781
781
782
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783
783
783
784
784
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786
787
787
787

identied as the cause of seafood related outbreaks in the European

Union (EFSA, 2010), the United Stated (CSPI, 2009) and other
countries worldwide.
The U.S. Food and Drug Administration (FDA) has demonstrated the
presence of salmonellae in a variety of sh and shellsh, including
ready-to-eat (RTE) seafood products, seafood products requiring
minimal cooking, and shellsh eaten raw (Brands et al., 2005; Duran
& Marshall, 2005; Heinitz, Ruble, Wagner, & Tatini, 2000).
There is a considerable amount of epidemiological data available
regarding the presence of Salmonella in seafood and related illnesses.

G. Amagliani et al. / Food Research International 45 (2012) 780788

However, this information appears very heterogeneous in terms of

incidence, the sh products involved, the responsible serovars, and
the geographical origins of the products in question.
Fish and shellsh can acquire Salmonella from polluted waters or
they can be contaminated with Salmonella during storage and
processing (Panisello, Rooney, Quantick, & Stanwell-Smith, 2000).
Aquaculture is a major source of seafood and the largest producers
are Asian countries. This implies that considerable quantities of sh
products are frequently shipped very long distances. Another risk
factor for consumers is the widespread use of antimicrobial drugs in
sh farming, and the related risk of the emergence and spread of
resistance among human pathogens (Serrano, 2005).
National provisions call for the constant monitoring of the
microbiological quality and safety of seafood products through Hazard
Analysis and Critical Control Points (HACCP) plans, together with
good manufacturing (GMP), good handling (GHP) practices and
Sanitation Standard Operating Procedures (SSOPs) (Aruoma, 2006;
Arvanitoyannis & Varzakas, 2009).
The harmonization of these practices on an international level
ensures a high level of safety of food products and allows countries
able to demonstrate that they have implemented such practices to
access international trade.
This review is intended to provide a general overview of the
incidence of Salmonella in seafood and the public health risks posed by
this contamination.
1.1. Search strategy and selection criteria
The PubMed database of NCBI website was searched for English
language articles (from December 2010), published during the last
ten years, using the search terms Salmonella + seafood, Salmonella + sh, Salmonella + epidemiology + seafood, HACCP + Salmonella + seafood, and Salmonella + aquaculture. Articles and
reviews about Salmonella incidence in seafood and related epidemiological information were selected, including cited references.
Further, textbook information have been obtained through http://
books.google.com/. Additional information were obtained through
institutional websites of FAO, FDA, EFSA, and EC.
2. Seafood consumption
Because of its nutritional value, seafood is increasingly recognized
as a healthy dietary component by consumers worldwide, offering
high quality protein, omega-3 fatty acids, essential micronutrients and
minerals. Seafood includes molluscs (e.g., oysters, clams, and
mussels), nsh (e.g., salmon and tuna), marine mammals (e.g., seal
and whale), sh eggs (roe), and crustaceans (e.g., shrimp, crab, and
lobster) (Iwamoto, Ayers, Mahon, & Swerdlow, 2010).
Seafood consumption levels and trends have recently been
estimated by the Food and Agriculture Organization (FAO) of the
United Nations and are available in the FAOSTAT Database (www.
faostat.fao.org). According to these data, 24.05 kg/capita/yr were
consumed in the USA and 22.03 kg/capita/yr in the EU. Japan had one
of the highest global per capita levels of sh consumption
(60.78 kg/capita/yr), and China showed a consumption level of
26.46 kg/capita/yr. In addition, sh provides at least 50% of total
animal protein intake in some small developing island states
(Laurenti, 2007), and it is estimated that future demand will grow
(Failler, 2007).
Aquaculture, mainly based in the AsiaPacic region, accounts for
46% of the total world seafood supply (FAO, 2010a). The contribution
of aquaculture to global supplies of sh, crustaceans, molluscs and
other aquatic animals has grown considerably over the past four
decades. It increased from 3.9% of total production by weight in 1970
to 36% in 2006, and it is expected to continue growing in the future
(Failler, 2007). This trend could potentially lead to an increase in

781

health issues related to seafood consumption because of the greater

risk of biological and chemical contamination in coastal areas and
freshwaters, compared to open seas, due to proximity to urbanized
areas (Feldhusen, 2000; Martinez-Urtaza et al., 2004).
As a highly perishable commodity, seafood has signicant
processing requirements, and can be consumed in a great variety of
ways and product forms. It is generally distributed as either live, fresh,
chilled, frozen, heat-treated, fermented, dried, smoked, salted,
pickled, boiled, fried, freeze-dried, minced, powdered or canned, or
a combination of these methods may be employed. Several preparations are also based on traditions. Processed shery products, ranging
from ready-to-cook, partly cooked or even RTE dishes, are increasingly popular among consumers, who have less time for preparing
meals (Failler, 2007). The most important sh products destined for
direct human consumption are fresh sh (40%), frozen sh (32%),
canned sh (16%) and cured sh (12%) (Ababouch, 2006).
3. Microbiological risk associated with seafood
The biological agents involved in seafood contamination consist of
bacteria, viruses and parasites, which can cause illnesses ranging from
mild gastroenteritis to life-threatening diseases. Some of these
pathogens are naturally present in the aquatic environment, while
others can be introduced through animal or human fecal shedding
and sewage pollution (Table 1). Bacteria naturally present in sea
water can be found in limited numbers in live and raw sh although
they can be concentrated by lter-feeding molluscs which are often
eaten raw.
Salmonella and other bacteria may contaminate seafood during
processing, and may cross-contaminate products during various
stages of preparation (Table 1).
Huss, Reilly, and Ben Embarek (2000) classied seafood into risk
categories. According to this ranking system, the highest risk category
includes molluscs (fresh and frozen mussels, clams, oysters) and sh
that is served raw. The next highest risk category includes crustaceans
and sh, fresh or frozen, to be eaten after cooking. Finally, low risk
categories include lightly preserved sh products (salted, marinated,
fermented, cold smoked and gravad sh); semi-preserved sh
(caviar); mildly heat-processed (pasteurized, hot-smoked); and
heat-processed (sterilised, packed in sealed containers).
4. General aspects of Salmonella
Salmonella is a facultatively anaerobic, nonsporulating, Gramnegative bacterium; most strains are motile by means of agella. They
are mesophilic, with optimum growth temperature between 35 and
37 C, with a growth range of 5 to 46 C. They are killed by
pasteurization temperature and time, sensitive to low pH (4.5 or
below) and do not multiply at Aw 0.94, especially in combination with
a pH at 5.5 and below (Bibek, 2001).
The cells are able to survive under frozen and dried states for a long
time, and to multiply in many foods without affecting the acceptance

Table 1
Microbiological risks associated with seafood.
Origin

Species

Naturally present in the aquatic

environment (indigenous)
Human and animal origin

Vibrio, Aeromonas, Plesiomonas, Clostridium

botulinum type E, Helminths, Amoeba
Salmonella, Shigella, Escherichia coli, Legionella,
Campylobacter, Staphylococcus
Enteric viruses: Enteroviruses, Adenoviruses,
HAV, Noroviruses, Rotaviruses)
Parasites: Cryptosporidium, Giardia
Listeria, proteolytic C. botulinum, Staphylococcus

General environment

782

G. Amagliani et al. / Food Research International 45 (2012) 780788

qualities (Murray, 1999); in addition, the ability of Salmonella to

survive relatively high salt conditions has also been demonstrated
(Jay, Diane, Dundas, Frankish, & Lightfoot, 2003).
There are formally two species of Salmonella, S. enterica and S.
bongori. The former has been further classied into six subspecies: S.
enterica subsp. enterica, S. enterica subsp. salamae, S. enterica subsp.
arizonae, S. enterica subsp. diarizonae, S. enterica subsp. houtenae and
S. enterica subsp. indica. Differences in lipo-polysaccharide and
agellar structures generate the antigenic variation that is reected
in the more than 2500 serovars, considered as potential pathogens in
both animals and humans (Norhana, Poole, Deeth, & Dykes, 2010a).
This pathogen has been isolated from a large number of animal
species including poultry, cows, pigs, sheep, birds, and reptiles (CDC,
2010c).
Salmonella bacteria are believed to cause two distinct disease
syndromes, described simply as systemic disease and gastroenteritis. In
developed countries gastroenteric disease is most frequently associated
with food-borne transmission (Bremer, Fletcher, & Osborne, 2003).
Ninety-nine percent of human infections are caused by S. enterica,
which has about 1500 serotypes. Based on analysis of globally reported
foodborne outbreaks, the non-typhoid Salmonella serotypes most often
encountered in human infections are Enteritidis followed by Typhimurium (Greig & Ravel, 2009). However, the predominant serovars found in
human infections vary both geographically and over time. For example,
S. Weltevreden was the second most common serovar in Asia during
20002001, but this serovar dropped to fourth place in 2002 surpassed
by S. Rissen and S. Typhimurium (Galanis et al., 2006).
5. Salmonella in the aquatic environment and live sh
Salmonella serovars are widely distributed in nature. These
bacteria can enter the aquatic environment through wild animals,
domestic stock, poor sanitation and inappropriate disposal of human
and animal wastes. Although there are few comparable studies,
results suggest that persistence and dissemination of Salmonella are
analogous in saltwater and freshwater sh (FAO, 2010b). It is
important to note that once Salmonella reaches soil and aquatic
environments, it can survive over long periods, months or even years
(Wineld & Groisman, 2003), thus ensuring its passage into
new hosts.
Human infections have arisen from contact with both turtles and
frogs kept in aquariums (CDC, 2010c). Salmonella has also been found in
the guts of river sh (Gaertner et al., 2008), and, via the gastrointestinal
tract, entered the internal organs and muscle tissue in several
freshwater species, e.g. rainbow trout (Salmo gairdneri), Israeli mirror
carp (Cyprinus carpio) and tilapia (Tilapia aurea), and Atlantic salmon
(Salmo salar) in saltwater (Nesse et al., 2005). Even marine mammals
harbor Salmonella (Higgins, 2000). Serovar Arizonae is the only serovar
that has been described as a possible sh pathogen (FAO, 2010b).
Saltwater and freshwater wetlands and ponds serve as important
habitats for juvenile sh and shellsh, and migratory birds (Shellenbarger, Athearn, Takekawa, & Boehm, 2008), and it has been reported
that bird feces can contain zoonotic organisms such as Salmonella
(Hubalek, 2004; Roy et al., 2002). Salmonella have been detected in
surface waters in Canada (Gannon et al., 2004; Johnson et al., 2003),
along the Mediterranean Coast (Baudart, Lemarchand, Brisabois, &
Lebaron, 2000; Martinez-Urtaza et al., 2004; Touron, Berthe, Pawlak, &
Petit, 2005), and the US Gulf coast (Haley, Cole, & Lipp, 2006).
Shellenbarger et al. (2008) found the Salmonella serovars Typhimurium,
Javiana, and Heidelberg (in winter), and Kentucky, Glostrup, Infantis,
Bovismorbicans and Give (in the summer) in water samples from the
San Francisco estuary in California. Salmonella has also been found in
river systems, such as the upper Oconee river basin in Georgia, US
(Meinersmann et al., 2008).
Salmonella prevalence in seawater and seafood is inuenced by
climate conditions; two different patterns have been described, and

are outlined in Table 2. Critical factors are rainfall and stormwater

(Bienfang et al., in press) and, as a reducing factor, intense sunlight
(Martinez-Urtaza et al., 2004; Setti et al., 2009).
Of particular interest are the studies by Brands et al. (2005) and
DePaola et al. (2010), who reported the presence of Salmonella in live
oysters collected from waters approved for shellsh harvesting in the
US. In shellsheries in the US, the presence of fecal coliform is
assessed to determine the risk of exposure to pathogens through
shellsh consumption (FDA, 2007). However, these results suggest
that Salmonella contamination may not only be linked to poor
hygiene, and the simple control of fecal contamination by monitoring
levels of indicator organisms may be insufcient to guarantee the
absence of the pathogen in sh and shery products.

6. Epidemiological data
Epidemiological data regarding seafood-borne diseases and
illnesses are published by various organizations and reporting
systems in different countries. In the EU, data are collected by
Member States (MS) and reported to the ECDC (European Centre for
Disease Prevention and Control) and EFSA (European Food Safety
Authority). In the US, the main source of information is the Centers
for Disease Control and Prevention (CDC) Foodborne Active Disease
Surveillance Network (FoodNet), with data provided by state health
departments. Seafood-borne illness data for Japan are published
annually by the Inspection and Safety Division, Department of Food
Safety, Pharmaceutical and Food Safety Bureau of the Ministry of
Health, Labour and Welfare, as part of annual statistics compiled for
all food-borne illnesses (Japan Food Poisoning Statistics, 2009).

Table 2
Salmonella prevalence in aquatic environment and seafood.
From FAO (2010a, 2010b) with some modications.
Climate
characteristics
and countries

Sample
type

Cold-temperate seawaters
Spain
Molluscs
Seawater
Morocco
Mussels
Sediments
Seawater
Morocco
Seafood
Mexico
Wastewater
Streamwater
Molluscs
Seawater
US
Oysters
US
Oysters

Tropical seawaters
Asian
Shrimps
countries
Holding pond
water
Pond
sediment
Pond
grow-out
water
Source water
Source
sediment
Vietnam
Shellsh
India

Fish
Shrimps
Clams

Prevalence
(%)

Reference

3
2.5
10
6.8
4.1
9
16.2
10.6
7.4
2.3
7.4
1.5
(8.3 by RealTime PCR)

Martinez-Urtaza et al. (2004)

1.6
2.5

Koonse, Burkhardt, Chirtel, and

Hoskin (2005)

Setti et al. (2009)

Bouchrif et al. (2009)

Simental and Martinez-Urtaza
(2008)

Brands et al. (2005)

DePaola et al. (2010)

1.0
3.5

5.0
24
18.0
30.5
29
34.1

Van, Moutas, Istivan, Tran,

and Coloe (2007)
Kumar et al. (2008a)

G. Amagliani et al. / Food Research International 45 (2012) 780788

However, the actual incidence of seafood-borne outbreaks and cases

is usually underestimated, as with other foodborne diseases, due to
non-reporting or, failed recognition, mainly in the case of brief and
mild symptoms. (Cato, 1998).
6.1. Data from the EU
According to the last published EFSA Community Summary
Report on Trends and Sources of Zoonoses, Zoonotic Agents and
Food-borne Outbreaks, Salmonella remained the main causative
agent, responsible for 35.4% of all reported outbreaks; sh and sh
products were the source in 1.4%, while crustaceans, shellsh,
molluscs and products thereof, accounted for 1% (EFSA, 2010)
(Table 3). Germany, Hungary, Italy, Lithuania and Spain reported
Salmonella positive samples of sh and shery products with low
average incidence (0.3%), although the highest proportion (8.5%)
was found in Lithuania (EFSA, 2010). Regarding crustaceans, live
bivalve molluscs and molluscan shellsh, positive samples were
reported by Belgium (14.3%, raw crustaceans destined for retail
sale), Germany (0.5%, crustaceans destined for retail sale), Greece
and Spain (0.9% and 1.6%, live bivalve molluscs), and Italy (1.2%,
molluscan shellsh). At the batch level, 2.1% of cooked crustaceans
and molluscan shellsh were non-compliant with microbiological
criteria (Regulations (EC) No 2073/2005 and No 1441/2007, EC,
2005, 2007) in force in the EU. S. Enteritidis and S. Typhimurium
serovars were the most frequently isolated (Table 4).
Additional data on Salmonella seafood-borne infection in the EU
related to sh products, such as sh gratin and sesame prawn toast
have been reported by some Authors (Guerin et al., 2004; Holtby et al.,
2006), however, in both cases the responsibility should be ascribed to
eggs used as an ingredient in the products.
6.2. Data from the US
The last FoodNet Surveillance Report (CDC, 2009) indicated that
most laboratory conrmed infections were caused by Salmonella
(41%), although there had been a 10% decline in incidence since
FoodNet surveillance began (CDC, 2010a). The seven most commonly
identied serotypes are summarized in Table 4. A total of 838
foodborne illness outbreaks with 7298 illnesses were linked to

783

seafood and seafood dishes between 1998 and 2007 (CSPI, 2009).
More detailed data regarding seafood involvement were obtained
from the Morbidity and Mortality Weekly Report of the CDC (CDC,
2010b), which reported 44 illnesses caused by Salmonella in raw tuna.
A very comprehensive study by Iwamoto et al. (2010) focused on
seafood associated Salmonella outbreaks between 1973 and 2006 in
the US (Table 3). Specically, gelte sh, a traditional dish made from
ground deboned sh, was implicated in 4 outbreaks, with whitesh
implicated in 2 outbreaks, bass in 1 outbreak, and unspecied sh in
the rest (Bialek et al., 2007).
6.3. Data from India and other Asian countries
Distribution trends of Salmonella serovars in India between 2001
and 2005 can be obtained from the National Salmonella and
Escherichia Centre (NSEC), Central Research Institute (Kasauli),
which is a national reference laboratory, previously under the control
of WHO, and have been reported by Kumar (2009). During the study
period, 70 non-typhoidal serovars were isolated from seafood. The
most common serovars in order of their frequency in seafood are
listed in Table 4. An outbreak of food poisoning in Mangalore (India)
involving 34 students caused by S. Weltevreden was reported by
Antony, Dias, Shetty, and Rekha (2009), with sh being the most likely
causative food. Results from a survey in shing harbors and sh
markets in Cochin (India) (Kumar, Surendran, & Thampuran, 2009)
are indicated in Tables 3 and 4.
Additional epidemiological data were provided by the Japanese
Food Poisoning Statistics report (2009), recording the number of
outbreaks, cases and deaths. It reported that sh and shellsh were
involved in the highest number (94) of outbreaks, of which 69
involving two or more persons, and 25 only one person. A seasonal
trend was noted, since sh and shellsh were implicated most
frequently during the winter seasons. Bacteria were responsible for
56.6% of all the food poisoning cases and, in the Fish and Shellsh
category, one incident was caused by Salmonella involving 27 patients
with no reported deaths (Table 3).
In China, the report released from the National Foodborne Diseases
Surveillance Network regarding the period between 1992 and 2005,
indicates salmonellosis as the second leading cause of bacterial
foodborne illness outbreaks (1020% per year) The prevalence of

Table 3
Epidemiological data about salmonellosis outbreaks and Salmonella occurrence in seafood.
Geographic
area/country

Salmonellosis outbreaks linked to seafood

(% of total salmonellosis outbreaks)

Product type with

prevalence (%)

Reference

US

Molluscs (4 outbreaks, 32 cases)

Crustaceans (4 outbreaks, 81 cases)
Finsh (10 outbreaks, 261 cases)
Total: 18 outbreaks, 374 cases of
salmonellosis between 1973 and 2006
Fish and sh products (5 outbreaks, 1%)
Crustaceans, shellsh, molluscs
and products thereof (7 outbreaks, 1.4%)

Not reported

Iwamoto
et al. (2010)

Fish and shery products (0.3)

Crustaceans (0.5), live bivalve molluscs
(0.9), molluscan shellsh (1.1)
Clam (34.2)
Mussel (31)
Finsh (28.2)
Shrimp (26.7)
Squid (17.3)
Octopus (16.6)
Oyster (12.5)
Crab (9.6)
Lobster (4.7)
Total seafood (23)

EFSA (2010)

EU

India

Japan
China
Thailand
Morocco

Fish and shellsh (1 outbreak, 1.5%)

Seafood (20.8)
Open market shrimp (53)
Seafood (1.9)

Kumar et al. (2009)

Japan Food Poisoning Statistics report (2009)

Yan et al. (2010)
Minami et al. (2010)
Bouchrif et al. (2009)

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G. Amagliani et al. / Food Research International 45 (2012) 780788

Table 4
Predominant Salmonella serovars in seafood.
Geographic
Product type
area/country

Serovar
(number or % of all isolates)

Reference

US

All tested
products

CDC (2009)

EU

Enteritidis (16%),
Typhimurium (15%),
Newport (10%),
I 4,[5],12:i: (5%), Javiana
(5%), Heidelberg (4%), and
Montevideo (3%)
S. Enteritidis (1.7% of human
cases)
S. Enteritidis (1.37%) and S.
Typhimurium (0.15%)

Fish and sh
products
Crustaceans,
shellsh,
molluscs and
products thereof
Seafood
S. Worthington (18 isolates),
S. Weltevreden (13), S.
Typhimurium (9), S.
Enteritidis (9), S. Bareilly (7),
S. Gallinarum (4) and S.
Infantis (3)
S. Weltevreden (22), S. Rissen
(20), S. Typhimurium (17)
and S. Derby (16)
Seafood
S. Weltevreden (26%)
Water
S. Weltevreden (14.5%)
Open markets
S. Stanley
shrimp

India

Thailand

EFSA (2010)

Kumar (2009)

Kumar et al.
(2009)
Bangtrakulnonth
et al. (2004)
Minami et al.
(2010)

Salmonella contamination in seafood samples in China was 20.8% (Yan

et al., 2010) (Table 3).
The World Health Organization (WHO) National Salmonella and
Shigella Centre in Bangkok (Thailand) examines all Salmonella
suspected isolates from various diagnostic laboratories, including
those of the Fisheries Department. Prevalence data have been
presented by Bangtrakulnonth et al. (2004) and Minami et al.
(2010) (Tables 3 and 4).
Very few data are available for Africa. David, Wandili, Kakai, and
Waindi (2009), recently described the isolation of Salmonella from
sh harvested in Lake Victoria, Kenya, which supports the most
productive freshwater shery in the world.
Bouchrif et al. (2009) found Salmonella in 10 out of 526 seafood
products analyzed in Morocco between 2002 and 2005 (Table 3).

7. Risks associated with aquaculture

The current denition of aquaculture, according to FAO/NACA/WHO
(1997), is the farming of aquatic organisms including sh, molluscs,
crustaceans and aquatic plants.
The growing global demand for sh and shery products has led to
a signicant expansion of aquaculture production. The Fishery and
Aquaculture Statistics database of FAO (http://www.fao.org/shery/
statistics/global-aquaculture-production/en) reported a world aquaculture production of more than 52 million tons (t) in 2008, with Asia
as the leading continent (46 million t) and, at a remarkable distance,
Europe and Americas (approximately 2 million t each). Currently,
aquaculture meets about 50% of the global demand for sh and shery
products, with about 90% of aquaculture products coming from the
Asian region. This dominance is mainly due to China's enormous
production, which accounts for 62% of global production in terms of
quantity and 51% in terms of global value (FAO, 2010a). The
importance of aquaculture production makes it imperative to assess
microbiological risks and hence to implement control measures to
protect consumer health. Various factors inuence food safety risk
associated with aquaculture products: location, farmed species,
husbandry practices, postharvest processing, and cultural habits of
food preparation and consumption.

Some of these potential microbiological hazards may be associated

with poor hygienic standards (including contaminated feed) or runoff waters from human sewage, livestock farming, or industry
(Martinez-Urtaza & Liebana, 2005), although Salmonella can be
detected in seafood even in areas managed through fecal coliform
monitoring (DePaola et al., 2010). In addition, stress factors, such as
environmental conditions or overcrowding, may increase susceptibility to sh diseases and/or pathogen carriage. Pal and Marshall
(2009) examined Salmonella contamination in farm raised catsh,
both from US (33% prevalence) and Vietnam (50%).
However, the risk is signicantly reduced thanks to a high level of
control achieved through good aquaculture practices (GAP) (Doyle,
Kaspar, Archer, & Klos, 2009). Hence sh farmed worldwide have a
good safety record with respect to Salmonella, as conrmed by the lack
of reports linking salmonellosis to the consumption of nsh
aquaculture products (EFSA, 2008).
As recently outlined at the FAO expert workshop on the
application of biosecurity measures to control Salmonella contamination in sustainable aquaculture, contamination can occur through the
following pathways: run off of organic matter into ponds in rainfall
events; animal waste, introduced directly (bird droppings or frogs) or
indirectly (runoff); fertilization of ponds with non-composted
manures; integrated farming systems with animals housed in
proximity to ponds, and toilets discharging into ponds; contaminated
source water (wildlife, untreated domestic sewage, animal farms);
unsanitary ice, water, containers, and poor hygienic handling
practices; contaminated feed (FAO, 2010a). Several authors have
reported the prevalence of Salmonella in shrimp culture environments
(Norhana et al., 2010a).
Salmonella and other Enterobacteriaceae constitute a hazard in
aquaculture feeds (Lunestad et al., 2007). Carnivorous aquaculture
species may be fed with trash sh or with feed that has been
improperly stored or prepared under poor hygienic conditions. Trash
sh can also be used in the manufacture of shmeal and sh oil. In the
last EFSA Report (2010), sh meal was among the feed materials most
often reported Salmonella-positive (2.1% tested units). In a recent
study on Salmonella prevalence in feed and feed producer plants in
Norway, conducted between 2000 and 2004, S. Senftenberg, S. Agona,
S. Montevideo and S. Kentucky were the most frequently found
serovars (Lunestad et al., 2007).
Since sh are often typically cooked prior to consumption,
Salmonella should not pose a risk to human health. However, it is
important for aquaculture farms to apply the best practices to control
this pathogen and prevent cross contamination.
8. Salmonella contamination and the sh trade
World trade of shery and aquaculture products has developed
remarkably in the last three decades. Around 40% of sh producers are
engaged in international trade, and half of those is based in Asian
countries (Ababouch, 2006). China is the leading sh exporter,
followed by Thailand and Vietnam (FAO, 2010a), and Japan is the
largest importer. The EU and the US are also major importers of
seafood (Ababouch, 2006). Shrimp is now the most important
internationally traded seafood commodity in terms of value (Gillet,
2008). Prepared products made from crustaceans, molluscs and other
aquatic invertebrates and sh, as well as cured and fresh/chilled sh
from the aquaculture production of salmon, trout, sea bass and sea
bream also appear to be increasingly important commodities.
However, the increasing globalization of the sh trade is
accompanied by a greater risk of cross-border diffusion of infectious
agents, hence prevention measures have been put in place by the US
and EU, based on the principle of quality management and processoriented controls throughout the entire food chain (from the shing
vessel or aquaculture farm to the consumer's table). Implementation
of hygienic practices must be veried and certied by the national

G. Amagliani et al. / Food Research International 45 (2012) 780788

competent authority of the exporter country and, after formal

recognition, the EU annually draws up a list of countries from which
the importation of sh for human consumption is authorized. In the
US, where the FDA is responsible for inspections, seafood products
account for approximately 1/10 of refused products, and the detection
of Salmonella is the second most frequently cited reason for the
rejection of several seafood preparations, ranging from cooked, RTE,
raw and frozen products; 58% of violations for Salmonella in seafood
are due to contamination of shrimp and prawns, farm raised and wild
caught (Allshouse, Buzby, Harvey, & Zorn, 2004).
The European Commission has put into effect a Rapid Alert
System for Food and Feed (RASFF). The legal basis of the RASFF is
Regulation EC/178/2002 laying down the general principles and
requirements of food law, establishing the European Food Safety
Authority and laying down procedures in matters of food safety. The
last RASFF Report (2009) refers to notications of Salmonella
contamination, which is considered common in various types of
food of animal origin, including sh, bivalve molluscs, cephalopods
and crustaceans (RASFF, 2010).
Effective prevention relies on a fully coordinated approach.
Harmonization of global trading standards is based on the application
of internationally agreed upon risk-based scientic principles which
form the basis of the recommendations and standards of the Codex
Alimentarius Commission (FAO, 2010b).To achieve this aim, the
World Trade Organization (WTO) member countries should follow
international standards, guidelines and other recommendations
adopted by the FAO/World Health Organization Codex Alimentarius
Commission (CAC) (FAO/WHO, 2005), particularly the Codex Committee on Fish and Fishery Products (CCFFP) and the Codex
Committee on Food Hygiene (CCFH), which are the global points of
reference for national food safety strategies.
Critical points have sometimes been identied in countries with
tropical environmental temperatures, where post-harvest contaminations may occur because of inadequate use of ice, long supply
chains, poor access to roads and electricity, and inadequate infrastructure and services in physical markets, although outbreaks of
salmonellosis associated with aquacultured products from these
countries are not frequent (FAO, 2010b). However, the detection of
this pathogen in sh and shery products shows that current
strategies for Salmonella control in the aquaculture production and
processing sectors are not completely effective (FAO, 2010b) and data
from scientic literature conrmed Salmonella occurrence both in
imported and domestic seafood products in the US (Heinitz et al.,
2000; Pal & Marshall, 2009).
9. Antimicrobial resistance
Resistance is dened as the ability of microorganisms to adapt and
survive antimicrobials. This capacity is determined by antimicrobial
resistance genes, carried on mobile genetic elements, such as plasmids,
trasposons and integrons, which can disseminate by horizontal or
vertical transfer (Liebert, Hall, & Summers, 1999). Consequences for
public health include failure of treatment, increased severity and
duration of infections, hospitalization and mortality (Newell et al.,
2010). Antibiotic resistance is a complex issue and resistant bacteria
have emerged in various sectors, including human medicine, animal
husbandry, and agriculture. Such bacteria have also been found in
aquatic environments and aquaculture products. Dissemination of
resistant microorganisms may occur in both hospitals and communities.
The relative contribution of each route to the development of resistance
is very difcult to estimate. Horizontal transfer can occur between
bacteria from terrestrial animals, sh and humans and through various
routes including food (Newell et al., 2010). Indeed, the role of the food
chain in the transmission of resistant microorganisms from animals to
humans has been recognized, and sometimes it has been linked to the
zootechnical use of antimicrobials agents in farming (Nawaz et al.,

785

2001). In animal husbandry, including aquaculture, antibiotics are used

mainly for therapeutic purposes and as prophylactic agents. In addition,
their use as growth promoters in subtherapeutic doses has contributed
to promoting the development of resistance (Serrano, 2005). Consequently, the EU banned the use of all growth promoters from 1st January
2006 (EC, 2003; Newell et al., 2010).
The use of antibiotics in the sh farming sector, has been
associated with the development of antibiotic resistance in environmental species (Serrano, 2005), with potential human health risks in
the case of transfer of resistance genes from these bacteria to human
pathogens (EFSA, 2008). Additional negative effects include toxicity
or allergenic properties of antibiotic residues, alteration of human
intestinal microora, and adverse impact on the environment.
The following antibiotics are authorized for use in aquaculture:
oxytetracycline, orfenicol, chorionic gonadotropin, formalin solutions,
tricaine methanesulfonate, sulfadimethoxine/ormetoprim, hydrogen
peroxide (FDA Center for Veterinary Medicine, www.fda.gov/cvm).
Countries that intend to get authorisation to export aquaculture products
to the EU should have a clear policy on the use of veterinary medicines
and should demonstrate implementation of a national residue control
program veried by EU FVO missions (EU Food and Veterinary Ofce,
http://ec.europa.eu/food/fvo/inspectprog/index_en.htm).
Both the EFSA (EFSA, 2007) and the NARMS (National Antimicrobial Resistance Monitoring System, a collaborative program among
the FDA, the USDA, and the CDC) (FDA, 2006; Foley & Lynne, 2008)
have reported on resistant and multiresistant Salmonella isolates, such
as the S. enterica serotype Typhimurium denitive type 104 (DT 104),
characterized by the ACSSuT (resistant to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracyclines) phenotype.
Though declining in incidence in Europe, this strain remains an
international public health hazard (Newell et al., 2010). Moreover,
Salmonella bacteria resistant to extended spectrum betalactamase
(ESBL) have been recognized worldwide (Newell et al., 2010).
A review of recently published papers allowed us to recognize the
worldwide diffusion of Salmonella resistant strains in seafood.
Boinapally and Jiang (2007) described the isolation of a Salmonella
strain resistant to ampicillin, ceftriaxone, gentamicin, streptomycin
and trimethoprim from farm cultured shrimp imported into the US.
Khan et al. (2006) examined a total of 105 S. enterica strains isolated
from imported seafoods from 20 countries into the US from 2000 to
2005, testing these strains for levels of resistance to antibiotics
commonly used in either clinical or veterinary medicine. These
Salmonella strains belonged to 36 different serovars, of which the
most predominant were Weltevreden, Newport, Saintpaul, Senftenberg, Lexington, Enteritidis and Bareily. Twenty isolates showed
resistance to at least one of the sixteen antibiotics tested. Five strains
(serovars Bareily, Oslo, Hadar, Weltevreden and Rissen) were
resistant to two or more antibiotics. Two S. enterica strains (serovars
Bareily and Oslo) from seafood from Vietnam and India were resistant
to trimethoprim/sulfamethoxazole, sulsoxazole, ampicillin, tetracycline and chloramphenicol. Ponce, Khan, Cheng, Summage-West, and
Cerniglia (2008) tested several S. enterica serovar Weltevreden strains
for susceptibility to a panel of seven antibiotics. In this investigation, a
low frequeny (2/37 isolates) of resistance was recorded.
A total of 106 S. Senftenberg isolates from 8 Spanish mussel
processing facilities (mussels, feed and environmental samples) were
characterized for antimicrobial resistance to a panel of 16 antibiotics
by Martinez-Urtaza and Liebana (2005). The authors found 9 strains
resistant to one or more antibiotics.
Bouchrif et al. (2009) observed several Salmonella serovars in
Morocco (Blockley, Hadar, Labadi and Typhimurium) showing
resistance and multiple resistance to tetracicline, nalidixic acid,
ampicillin and streptomycin.
Minami et al. (2010) tested Salmonella serovars isolated from
shrimp sold in open markets in Thailand. Some of these strains
showed resistance to sulsoxazole, streptomycin and tetracycline.

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G. Amagliani et al. / Food Research International 45 (2012) 780788

In China, Yan et al. (2010) described Salmonella serovars from

seafood resistant to various categories of antibiotics such as betalactams, aminoglycosides, nitrofurans, sulfonamides, quinolones and
uoroquinolones, also showing multiresistance patterns to between 2
to 10 or more drugs.
As a nal consideration, careful and judicious use of antimicrobials should be recommended. Although their use on sh farms is
necessary, it should be considered complementary to good management, biosecurity, vaccination, disease surveillance, optimal
nutrition and farm hygiene (EFSA, 2008). These criteria must be
applied globally to preserve the efcacy of existing drugs and to
limit the risk of the transfer of resistant foodborne pathogens to
humans (Khan et al., 2006).
Further preventive measures rely on the rapid and specic
detection of the genetic determinant of resistance to aid monitoring
and control the spread of resistance. Hence the FAO (Martinez, James,
& Loreal, 2005) has recently underlined the need for more rapid and
accurate microbiological diagnostic tools, such as molecular assays, to
identify resistance genes. PCR and, in particular, multiplex PCR, for the
simultaneous detection of several resistance determinants, appear
promising.

10. Seafood safety control

Food safety is dened by the WHO as the assurance that food will
not cause harm to the consumer.
The safety of seafood products varies considerably and is
inuenced by a number of factors, therefore it is important to
determine whether the hazard is signicant for a particular product,
and how it should be controlled.
Currently, major risk associated with seafood safety originates
from the environment; contamination of seafood can occur before
harvest or at any point from harvest through nal preparation.
However, survival of food-borne pathogens is more likely to occur in
foods that are consumed undercooked or raw, particularly bivalve
molluscs, as well as in those that experience time and temperature
abuse, such during delays between harvest and refrigeration
(Iwamoto et al., 2010).
Every seafood harvester and processor is required to use an
HACCP-based system, able of identifying sources and points of
process, from harvest to consumption, at high risk of contamination,
so that strategies aimed to decrease these risks can be implemented
and monitored.
In this contest, the FDA plays an important role in establishing
guidelines and providing oversight to ensure safer sh and shery
products. HACCP, GMP, GHP and SSOPs are major components of the
safety management systems in the food supply chain (Aruoma, 2006;
Arvanitoyannis & Varzakas, 2009). HACCP has also been endorsed
worldwide by Codex Alimentarius, the EU and by several countries,
including Canada, Australia, New Zealand and Japan. Additional
control strategies, such as the National Shellsh Sanitation Program
(NSSP) guidelines, that regulate the harvesting, processing, and
shipping of shellsh for interstate commerce in US, are aimed at
promoting the safety of molluscan shellsh (Iwamoto et al., 2010).
Control strategies to prevent seafood-associated illnesses include
monitoring harvest waters, identication and implementation of
process controls, and consumer education (Iwamoto et al., 2010).
The most common factors contributing to salmonellosis outbreaks
are improper cooking, inadequate storage, cross-contamination and
use of raw ingredients in the preparation of seafood. Main postharvest CCPs for Salmonella control in seafood, irrespective of whether
the primary source is a marine or an aquaculture product, include:
primary chilling immediately in an ice-water slurry on vessels and at
harvest site; in cooked products, applying timetemperature regimes
to give log reductions of contamination levels at sites of microbio-

logical concern; rapid chilling after cooking; plate freezing, followed

by frozen storage (Arvanitoyannis & Varzakas, 2009).
Studies have shown that there is an additional risk of crosscontamination or recontamination between raw and cooked products
at processing plants (Norhana et al., 2010a). A number of sh products
receive heat treatment during processing. Examples of such products
include: pasteurized or cooked and breaded sh llets, cooked shrimp
and crabmeat, cook-chill products and hot smoked sh. After the
heat-treatment, the various products may pass through further
processing steps before being packed and stored/distributed as chilled
or frozen products. Some of these products may receive additional
heat treatment before consumption or they may be eaten without
further treatment (RTE). The last category includes products that are
extremely sensitive to secondary contaminations. Hence, in the
application of the HACCP system, the heat-treatment is a very critical
processing step.
Heinitz et al. (2000) found that the incidence of Salmonella in RTE
seafood samples including salted/dried sh was 2.6%. Salmonella spp
can tolerate many stressful conditions and survive in low-Aw foods for
long periods (Arkoudelos, Samaras, & Tassou, 2003; Ristori, dos Santos
Pereira, & Gelli, 2007). Long term survival of Salmonella has been
shown in salted sardines at 0.69 Aw for 60 days (Arkoudelos et al.,
2003). Hence understanding the behavior of Salmonella in salted
and/or dried products is important from a food safety standpoint.
Shrimp and shrimp products, including RTE shrimp, can support
the survival and/or growth of Salmonella and there are reports of
foodborne disease outbreaks where shrimp have been implicated
(NACMCF, 2008). Unlike carapace, attachment and colonization of
cooked shrimp tissue resulted in growth and multiplication of
Salmonella at 4 C. Salmonella on shrimp could survive the acidic
environment of shrimp products such as shrimp salad and marinated
or brined shrimp (Norhana, Poole, Deeth, & Dykes, 2010b).
A further important aspect of quality and safety assurance is the
ability to trace products, ingredients, suppliers, retailers, processing
operations or storage procedures throughout the food production
chain (McKean, 2001). Many food (sh) processing companies
already have effective internal traceability systems as part of their
HACCP-based quality assurance systems. This is especially relevant
when failures occur. Traceability is important in the fresh sh chain
since it may guarantee freshness, which is, almost exclusively a
function of time and temperature. Moreover, it may trace sh from
polluted waters.
Achieving food safety in the global marketplace is a fundamental
human right and a global responsibility, in order to protect both the
public and the economic health of a nation.
Federal agencies, state governments, and private industry all bear
responsibility for reducing seafood-associated infections (Iwamoto et
al., 2010).
The effective control of Salmonella occurrence in seafood can also
be implemented through the prompt identication of the pathogen.
Detection of Salmonella is commonly carried out through the UNI EN
ISO 6579:2004 (Anonymous, 2004), that takes several days to be
completed, and additional time is needed if serovar or strain
identication is required. However, a prolonged analysis time does
not appear to be fully compatible, especially with highly perishable
food items, such as sh.
Effective alternatives are now offered by the so-called rapid
methods, like membrane ltration, automated electrical techniques
and immunological assays (Martinez et al., 2005), but the most
promising are those based on PCR and Real-Time PCR (Amagliani,
Omiccioli, Brandi, Bruce, & Magnani, 2010; DePaola et al., 2010; Kumar,
Surendran, & Thampuran, 2008a, 2008b, 2010; Minami et al., 2010;
Shabarinath, Kumar, Khushiramani, Karunasagar, & Karunasagar,
2007), thanks to their high sensitivity and specicity.
One of the main limitations imputable to DNA-based diagnostic
methods concerns the possibility of detection of nucleic acids from

G. Amagliani et al. / Food Research International 45 (2012) 780788

non-living (thus non-infecting) microorganisms, leading to false

positive results. This problem is usually circumvented by adding a
culture-enrichment step of the food under inspection, before DNA
extraction, which ensures that positive results are obtained only from
viable cells.
Also, epidemiological surveillance takes advantage of the application of molecular typing (i.e. PFGE, Martinez-Urtaza & Liebana, 2005
and Ponce et al., 2008; PCR-ribotyping and ERIC-PCR, Kumar,
Surendran, & Thampuran, 2009), which makes it possible to trace
related strains and vehicles, and prevent the spread of infection.
11. Conclusions
Several factors contribute to increase consumers' exposure to food
safety risks. Seafood is a food category that can be contaminated by
various foodborne pathogens, included Salmonella.
As shown by international data, seafood consumption is constantly
growing and consumers' preferences are moving toward minimally
processed and RTE products.
These changes, along with the expansion of international trade and
the growing aquaculture contribution to the sh trade, increase the
risk of seafood-borne illnesses.
Several salmonellosis outbreaks associated with seafood products
have recently been reported by international surveillance agencies,
however, the real incidence of these illnesses is probably underestimated. Hence surveillance systems adopted by national governments and competent authorities worldwide are fundamental to
prevent contaminations and protect public health.
Signicant progress has been made in recent years, but more still
needs to be done. Reducing the number of seafood-related outbreaks
worldwide will require continued and coordinated efforts by many
different agencies. An integrated approach involving public health,
veterinary and food safety experts, with multidisciplinary skills, that
can be applied to water quality monitoring, disease surveillance,
consumer education, and seafood harvesting, processing, and marketing is essential in order to ensure the priority of food hygiene.
Acknowledgments
The authors would like to thank Professor Timothy Bloom of the
University of Urbino Carlo Bo for a critical reading of the manuscript.
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