Food Research International 45 (2012) 780–788

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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, Università degli Studi di Urbino “Carlo Bo”, Italy

a r t i c l e i n f o a b s t r a c t

Article history: Seafood products are appreciated worldwide for their high nutritional value and are increasingly popular
Received 15 February 2011 among consumers. Consumer preferences range from fresh products, eaten raw or minimally processed, to
Accepted 7 June 2011 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
Keywords:
these factors expose seafood to various contaminants, including those of microbiological origins, such as
Salmonella
Seafood
Salmonella. The presence of Salmonella in seafood may derive from contamination occurring in the natural
Incidence aquatic environment, in aquaculture or during processing. In addition, the isolation of Salmonella serovars that
Aquaculture are resistant and multiresistant to antibiotics continues to raise concerns. In this review various aspects
Public health associated with the microbiological risk posed by the presence of Salmonella in seafood are examined. The
Prevention strategies most recent data of incidence are presented, and some prevention and control strategies are considered.
© 2011 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 780
1.1. Search strategy and selection criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 781
2. Seafood consumption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 781
3. Microbiological risk associated with seafood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 781
4. General aspects of Salmonella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 781
5. Salmonella in the aquatic environment and live fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 782
6. Epidemiological data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 782
6.1. Data from the EU . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 783
6.2. Data from the US . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 783
6.3. Data from India and other Asian countries. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 783
7. Risks associated with aquaculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 784
8. Salmonella contamination and the fish trade . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 784
9. Antimicrobial resistance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 785
10. Seafood safety control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 786
11. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 787
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 787
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 787

1. Introduction identified as the cause of seafood related outbreaks in the European

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: Università di Urbino “Carlo Bo”, Dipartimento di Scienze
Biomolecolari, Sez. di Scienze Tossicologiche, Igienistiche e Ambientali, v. S. Chiara, 27-
61029 Urbino, Italy. Tel.: + 39 0722 303540; fax: + 39 0722 303541.
E-mail address: giulia.amagliani@uniurb.it (G. Amagliani).
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 fish and shellfish, including
ready-to-eat (RTE) seafood products, seafood products requiring
minimal cooking, and shellfish 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.

0963-9969/$ – see front matter © 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2011.06.022
 G. Amagliani et al. / Food Research International 45 (2012) 780–788
However, this information appears very heterogeneous in terms of
incidence, the fish products involved, the responsible serovars, and
the geographical origins of the products in question.
Fish and shellfish 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 fish
products are frequently shipped very long distances. Another risk
factor for consumers is the widespread use of antimicrobial drugs in
fish 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”, “Salmo-
nella + fish”, “Salmonella + epidemiology + seafood”, “HACCP + Sal-
monella + seafood”, and “Salmonella + aquaculture”. Articles and
reviews about Salmonella incidence in seafood and related epide-
miological 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), finfish (e.g., salmon and tuna), marine mammals (e.g., seal
and whale), fish 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 fish consumption
(60.78 kg/capita/yr), and China showed a consumption level of
26.46 kg/capita/yr. In addition, fish 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 Asia–Pacific region, accounts for
46% of the total world seafood supply (FAO, 2010a). The contribution
of aquaculture to global supplies of fish, 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 significant
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 prepara-
tions are also based on traditions. Processed fishery products, ranging
from ready-to-cook, partly cooked or even RTE dishes, are increas-
ingly popular among consumers, who have less time for preparing
meals (Failler, 2007). The most important fish products destined for
direct human consumption are fresh fish (40%), frozen fish (32%),
canned fish (16%) and cured fish (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 fish although
they can be concentrated by filter-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) classified seafood into risk
categories. According to this ranking system, the highest risk category
includes molluscs (fresh and frozen mussels, clams, oysters) and fish
that is served raw. The next highest risk category includes crustaceans
and fish, fresh or frozen, to be eaten after cooking. Finally, low risk
categories include lightly preserved fish products (salted, marinated,
fermented, cold smoked and gravad fish); semi-preserved fish
(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, Gram-
negative bacterium; most strains are motile by means of flagella. 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 Vibrio, Aeromonas, Plesiomonas, Clostridium
environment (indigenous) botulinum type E, Helminths, Amoeba
Human and animal origin Salmonella, Shigella, Escherichia coli, Legionella,
Campylobacter, Staphylococcus
Enteric viruses: Enteroviruses, Adenoviruses,
HAV, Noroviruses, Rotaviruses)
Parasites: Cryptosporidium, Giardia
General environment Listeria, proteolytic C. botulinum, Staphylococcus
782 G. Amagliani et al. / Food Research International 45 (2012) 780–788

qualities (Murray, 1999); in addition, the ability of Salmonella to are outlined in Table 2. Critical factors are rainfall and stormwater
survive relatively high salt conditions has also been demonstrated (Bienfang et al., in press) and, as a reducing factor, intense sunlight
(Jay, Diane, Dundas, Frankish, & Lightfoot, 2003). (Martinez-Urtaza et al., 2004; Setti et al., 2009).
There are formally two species of Salmonella, S. enterica and S. Of particular interest are the studies by Brands et al. (2005) and
bongori. The former has been further classified into six subspecies: S. DePaola et al. (2010), who reported the presence of Salmonella in live
enterica subsp. enterica, S. enterica subsp. salamae, S. enterica subsp. oysters collected from waters approved for shellfish harvesting in the
arizonae, S. enterica subsp. diarizonae, S. enterica subsp. houtenae and US. In shellfisheries in the US, the presence of fecal coliform is
S. enterica subsp. indica. Differences in lipo-polysaccharide and assessed to determine the risk of exposure to pathogens through
flagellar structures generate the antigenic variation that is reflected shellfish consumption (FDA, 2007). However, these results suggest
in the more than 2500 serovars, considered as potential pathogens in that Salmonella contamination may not only be linked to poor
both animals and humans (Norhana, Poole, Deeth, & Dykes, 2010a). hygiene, and the simple control of fecal contamination by monitoring
This pathogen has been isolated from a large number of animal levels of indicator organisms may be insufficient to guarantee the
species including poultry, cows, pigs, sheep, birds, and reptiles (CDC, absence of the pathogen in fish and fishery products.
2010c).
Salmonella bacteria are believed to cause two distinct disease
syndromes, described simply as systemic disease and gastroenteritis. In 6. Epidemiological data
developed countries gastroenteric disease is most frequently associated
with food-borne transmission (Bremer, Fletcher, & Osborne, 2003). Epidemiological data regarding seafood-borne diseases and
Ninety-nine percent of human infections are caused by S. enterica, illnesses are published by various organizations and reporting
which has about 1500 serotypes. Based on analysis of globally reported systems in different countries. In the EU, data are collected by
foodborne outbreaks, the non-typhoid Salmonella serotypes most often Member States (MS) and reported to the ECDC (European Centre for
encountered in human infections are Enteritidis followed by Typhimur- Disease Prevention and Control) and EFSA (European Food Safety
ium (Greig & Ravel, 2009). However, the predominant serovars found in Authority). In the US, the main source of information is the Centers
human infections vary both geographically and over time. For example, for Disease Control and Prevention (CDC) Foodborne Active Disease
S. Weltevreden was the second most common serovar in Asia during Surveillance Network (FoodNet), with data provided by state health
2000–2001, but this serovar dropped to fourth place in 2002 surpassed departments. Seafood-borne illness data for Japan are published
by S. Rissen and S. Typhimurium (Galanis et al., 2006). annually by the Inspection and Safety Division, Department of Food
Safety, Pharmaceutical and Food Safety Bureau of the Ministry of
5. Salmonella in the aquatic environment and live fish Health, Labour and Welfare, as part of annual statistics compiled for
all food-borne illnesses (Japan Food Poisoning Statistics, 2009).
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
Table 2
and animal wastes. Although there are few comparable studies, Salmonella prevalence in aquatic environment and seafood.
results suggest that persistence and dissemination of Salmonella are From FAO (2010a, 2010b) with some modifications.
analogous in saltwater and freshwater fish (FAO, 2010b). It is
Climate Sample Prevalence Reference
important to note that once Salmonella reaches soil and aquatic characteristics type (%)
environments, it can survive over long periods, months or even years and countries
(Winfield & Groisman, 2003), thus ensuring its passage into Cold-temperate seawaters
new hosts. Spain Molluscs 3 Martinez-Urtaza et al. (2004)
Human infections have arisen from contact with both turtles and Seawater 2.5
frogs kept in aquariums (CDC, 2010c). Salmonella has also been found in Morocco Mussels 10 Setti et al. (2009)
Sediments 6.8
the guts of river fish (Gaertner et al., 2008), and, via the gastrointestinal
Seawater 4.1
tract, entered the internal organs and muscle tissue in several Morocco Seafood 9 Bouchrif et al. (2009)
freshwater species, e.g. rainbow trout (Salmo gairdneri), Israeli mirror Mexico Wastewater 16.2 Simental and Martinez-Urtaza
carp (Cyprinus carpio) and tilapia (Tilapia aurea), and Atlantic salmon Streamwater 10.6 (2008)
(Salmo salar) in saltwater (Nesse et al., 2005). Even marine mammals Molluscs 7.4
Seawater 2.3
harbor Salmonella (Higgins, 2000). Serovar Arizonae is the only serovar US Oysters 7.4 Brands et al. (2005)
that has been described as a possible fish pathogen (FAO, 2010b). US Oysters 1.5 DePaola et al. (2010)
Saltwater and freshwater wetlands and ponds serve as important (8.3 by Real-
habitats for juvenile fish and shellfish, and migratory birds (Shellen- Time PCR)
barger, Athearn, Takekawa, & Boehm, 2008), and it has been reported
Tropical seawaters
that bird feces can contain zoonotic organisms such as Salmonella Asian Shrimps 1.6 Koonse, Burkhardt, Chirtel, and
(Hubalek, 2004; Roy et al., 2002). Salmonella have been detected in countries Holding pond 2.5 Hoskin (2005)
surface waters in Canada (Gannon et al., 2004; Johnson et al., 2003), water
along the Mediterranean Coast (Baudart, Lemarchand, Brisabois, & Pond 1.0
sediment
Lebaron, 2000; Martinez-Urtaza et al., 2004; Touron, Berthe, Pawlak, & Pond 3.5
Petit, 2005), and the US Gulf coast (Haley, Cole, & Lipp, 2006). grow-out
Shellenbarger et al. (2008) found the Salmonella serovars Typhimurium, water
Javiana, and Heidelberg (in winter), and Kentucky, Glostrup, Infantis, Source water 5.0
Source 24
Bovismorbificans and Give (in the summer) in water samples from the
sediment
San Francisco estuary in California. Salmonella has also been found in Vietnam Shellfish 18.0 Van, Moutafis, Istivan, Tran,
river systems, such as the upper Oconee river basin in Georgia, US and Coloe (2007)
(Meinersmann et al., 2008). India Fish 30.5 Kumar et al. (2008a)
Salmonella prevalence in seawater and seafood is influenced by Shrimps 29
Clams 34.1
climate conditions; two different patterns have been described, and
 G. Amagliani et al. / Food Research International 45 (2012) 780–788
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; fish and fish
products were the source in 1.4%, while crustaceans, shellfish,
molluscs and products thereof, accounted for 1% (EFSA, 2010)
(Table 3). Germany, Hungary, Italy, Lithuania and Spain reported
Salmonella positive samples of fish and fishery 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 shellfish, 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 shellfish). At the batch level, 2.1% of cooked crustaceans
and molluscan shellfish 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 fish products, such as ‘fish 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 confirmed 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
identified serotypes are summarized in Table 4. A total of 838
foodborne illness outbreaks with 7298 illnesses were linked to
Table 3
Epidemiological data about salmonellosis outbreaks and Salmonella occurrence in seafood.
Geographic Salmonellosis outbreaks linked to seafood
area/country (% of total salmonellosis outbreaks)
US Molluscs (4 outbreaks, 32 cases)
Crustaceans (4 outbreaks, 81 cases)
Finfish (10 outbreaks, 261 cases)
Total: 18 outbreaks, 374 cases of
salmonellosis between 1973 and 2006
EU Fish and fish products (5 outbreaks, 1%)
Crustaceans, shellfish, molluscs
and products thereof (7 outbreaks, 1.4%)
India
Japan Fish and shellfish (1 outbreak, 1.5%)
China
Thailand
Morocco
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). Specifically, gefilte fish, a traditional dish made from
ground deboned fish, was implicated in 4 outbreaks, with whitefish
implicated in 2 outbreaks, bass in 1 outbreak, and unspecified fish in
the rest (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 fish being the most likely
causative food. Results from a survey in fishing harbors and fish
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 fish and shellfish 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 fish and shellfish 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 Shellfish”
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 (10–20% per year) The prevalence of
Product type with Reference
prevalence (%)
Not reported Iwamoto
et al. (2010)
Fish and fishery products (0.3) EFSA (2010)
Crustaceans (0.5), live bivalve molluscs
(0.9), molluscan shellfish (1.1)
Clam (34.2) Kumar et al. (2009)
Mussel (31)
Finfish (28.2)
Shrimp (26.7)
Squid (17.3)
Octopus (16.6)
Oyster (12.5)
Crab (9.6)
Lobster (4.7)
Total seafood (23)
Japan Food Poisoning Statistics report (2009)
Seafood (20.8) Yan et al. (2010)
Open market shrimp (53) Minami et al. (2010)
Seafood (1.9) Bouchrif et al. (2009)
784 G. Amagliani et al. / Food Research International 45 (2012) 780–788

Table 4 Some of these potential microbiological hazards may be associated

Predominant Salmonella serovars in seafood. with poor hygienic standards (including contaminated feed) or run-
Geographic Product type Serovar Reference off waters from human sewage, livestock farming, or industry
area/country (number or % of all isolates) (Martinez-Urtaza & Liebana, 2005), although Salmonella can be
US All tested Enteritidis (16%), CDC (2009) detected in seafood even in areas managed through fecal coliform
products Typhimurium (15%), monitoring (DePaola et al., 2010). In addition, stress factors, such as
Newport (10%), environmental conditions or overcrowding, may increase suscepti-
I 4,[5],12:i: – (5%), Javiana
bility to fish diseases and/or pathogen carriage. Pal and Marshall
(5%), Heidelberg (4%), and
Montevideo (3%) (2009) examined Salmonella contamination in farm raised catfish,
EU Fish and fish S. Enteritidis (1.7% of human EFSA (2010) both from US (33% prevalence) and Vietnam (50%).
products cases) However, the risk is significantly reduced thanks to a high level of
Crustaceans, S. Enteritidis (1.37%) and S. control achieved through good aquaculture practices (GAP) (Doyle,
shellfish, Typhimurium (0.15%)
Kaspar, Archer, & Klos, 2009). Hence fish farmed worldwide have a
molluscs and
products thereof good safety record with respect to Salmonella, as confirmed by the lack
India Seafood S. Worthington (18 isolates), Kumar (2009) of reports linking salmonellosis to the consumption of finfish
S. Weltevreden (13), S. aquaculture products (EFSA, 2008).
Typhimurium (9), S.
As recently outlined at the FAO expert workshop on the
Enteritidis (9), S. Bareilly (7),
S. Gallinarum (4) and S. application of biosecurity measures to control Salmonella contamina-
Infantis (3) tion in sustainable aquaculture, contamination can occur through the
S. Weltevreden (22), S. Rissen Kumar et al. following pathways: run off of organic matter into ponds in rainfall
(20), S. Typhimurium (17) (2009) events; animal waste, introduced directly (bird droppings or frogs) or
and S. Derby (16)
indirectly (runoff); fertilization of ponds with non-composted
Thailand Seafood S. Weltevreden (26%) Bangtrakulnonth
Water S. Weltevreden (14.5%) et al. (2004) manures; integrated farming systems with animals housed in
Open markets S. Stanley Minami et al. proximity to ponds, and toilets discharging into ponds; contaminated
shrimp (2010) source water (wildlife, untreated domestic sewage, animal farms);
unsanitary ice, water, containers, and poor hygienic handling
practices; contaminated feed (FAO, 2010a). Several authors have
Salmonella contamination in seafood samples in China was 20.8% (Yan reported the prevalence of Salmonella in shrimp culture environments
et al., 2010) (Table 3). (Norhana et al., 2010a).
The World Health Organization (WHO) National Salmonella and Salmonella and other Enterobacteriaceae constitute a hazard in
Shigella Centre in Bangkok (Thailand) examines all Salmonella aquaculture feeds (Lunestad et al., 2007). Carnivorous aquaculture
suspected isolates from various diagnostic laboratories, including species may be fed with trash fish or with feed that has been
those of the Fisheries Department. Prevalence data have been improperly stored or prepared under poor hygienic conditions. Trash
presented by Bangtrakulnonth et al. (2004) and Minami et al. fish can also be used in the manufacture of fishmeal and fish oil. In the
(2010) (Tables 3 and 4). last EFSA Report (2010), fish meal was among the feed materials most
Very few data are available for Africa. David, Wandili, Kakai, and often reported Salmonella-positive (2.1% tested units). In a recent
Waindi (2009), recently described the isolation of Salmonella from study on Salmonella prevalence in feed and feed producer plants in
fish harvested in Lake Victoria, Kenya, which supports the most Norway, conducted between 2000 and 2004, S. Senftenberg, S. Agona,
productive freshwater fishery in the world. S. Montevideo and S. Kentucky were the most frequently found
Bouchrif et al. (2009) found Salmonella in 10 out of 526 seafood serovars (Lunestad et al., 2007).
products analyzed in Morocco between 2002 and 2005 (Table 3). Since fish 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
7. Risks associated with aquaculture this pathogen and prevent cross contamination.

The current definition of aquaculture, according to FAO/NACA/WHO
(1997), is “the farming of aquatic organisms including fish, molluscs,
crustaceans and aquatic plants”.
The growing global demand for fish and fishery products has led to
a significant expansion of aquaculture production. The Fishery and
Aquaculture Statistics database of FAO (http://www.fao.org/fishery/
statistics/global-aquaculture-production/en) reported a world aqua-
culture 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 fish and fishery
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 influence food safety risk
associated with aquaculture products: location, farmed species,
husbandry practices, postharvest processing, and cultural habits of
food preparation and consumption.
8. Salmonella contamination and the fish trade
World trade of fishery and aquaculture products has developed
remarkably in the last three decades. Around 40% of fish producers are
engaged in international trade, and half of those is based in Asian
countries (Ababouch, 2006). China is the leading fish 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 fish, as well as cured and fresh/chilled fish
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 fish 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 process-
oriented controls throughout the entire food chain (from the fishing
vessel or aquaculture farm to the consumer's table). Implementation
of hygienic practices must be verified and certified by the national
 G. Amagliani et al. / Food Research International 45 (2012) 780–788
competent authority of the exporter country and, after formal
recognition, the EU annually draws up a list of countries from which
the importation of fish 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 notifications of Salmonella
contamination, which is considered common in various types of
food of animal origin, including fish, 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 scientific 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 Com-
mittee 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 identified in countries with
tropical environmental temperatures, where post-harvest contami-
nations may occur because of inadequate use of ice, long supply
chains, poor access to roads and electricity, and inadequate infra-
structure 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 fish and fishery products shows that current
strategies for Salmonella control in the aquaculture production and
processing sectors are not completely effective (FAO, 2010b) and data
from scientific literature confirmed Salmonella occurrence both in
imported and domestic seafood products in the US (Heinitz et al.,
2000; Pal & Marshall, 2009).
9. Antimicrobial resistance
Resistance is defined 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 difficult to estimate. Horizontal transfer can occur between
bacteria from terrestrial animals, fish 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). Conse-
quently, 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 fish farming sector, has been
associated with the development of antibiotic resistance in environ-
mental 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 microflora, and adverse impact on the environment.
The following antibiotics are authorized for use in aquaculture:
oxytetracycline, florfenicol, 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 verified by EU FVO missions (EU Food and Veterinary Office,
http://ec.europa.eu/food/fvo/inspectprog/index_en.htm).
Both the EFSA (EFSA, 2007) and the NARMS (National Antimicro-
bial 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 definitive type 104 (DT 104),
characterized by the ACSSuT (resistant to ampicillin, chloramphen-
icol, 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, Senften-
berg, 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, sulfisoxazole, ampicillin, tetracy-
cline 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 sulfisoxazole, streptomycin and tetracycline.
786 G. Amagliani et al. / Food Research International 45 (2012) 780–788
In China, Yan et al. (2010) described Salmonella serovars from
seafood resistant to various categories of antibiotics such as beta-
lactams, aminoglycosides, nitrofurans, sulfonamides, quinolones and
fluoroquinolones, also showing multiresistance patterns to between 2
to 10 or more drugs.
As a final consideration, careful and judicious use of antimicro-
bials should be recommended. Although their use on fish farms is
necessary, it should be considered complementary to good man-
agement, biosecurity, vaccination, disease surveillance, optimal
nutrition and farm hygiene (EFSA, 2008). These criteria must be
applied globally to preserve the efficacy 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 specific
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 defined by the WHO as the assurance that food will
not cause harm to the consumer.
The safety of seafood products varies considerably and is
influenced by a number of factors, therefore it is important to
determine whether the hazard is significant 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 final 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 fish and fishery
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 Shellfish Sanitation Program
(NSSP) guidelines, that regulate the harvesting, processing, and
shipping of shellfish for interstate commerce in US, are aimed at
promoting the safety of molluscan shellfish (Iwamoto et al., 2010).
Control strategies to prevent seafood-associated illnesses include
monitoring harvest waters, identification 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 post-
harvest 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 time–temperature 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 cross-
contamination or recontamination between raw and cooked products
at processing plants (Norhana et al., 2010a). A number of fish products
receive heat treatment during processing. Examples of such products
include: pasteurized or cooked and breaded fish fillets, cooked shrimp
and crabmeat, cook-chill products and hot smoked fish. 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 fish 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 (fish) 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 fish chain
since it may guarantee freshness, which is, almost exclusively a
function of time and temperature. Moreover, it may trace fish 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 identification 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
identification is required. However, a prolonged analysis time does
not appear to be fully compatible, especially with highly perishable
food items, such as fish.
Effective alternatives are now offered by the so-called rapid
methods, like membrane filtration, 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 specificity.
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) 780–788
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 applica-
tion 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 fish 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 under-
estimated. Hence surveillance systems adopted by national govern-
ments and competent authorities worldwide are fundamental to
prevent contaminations and protect public health.
Significant 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 mar-
keting 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.
References
Ababouch, L. (2006). Assuring fish safety and quality in international fish trade. Marine
Pollution Bulletin, 53, 561–568.
Allshouse, J., Buzby, J., Harvey, D., & Zorn, D. (FDA) (2004). Seafood safety and trade.
USDA Agriculture Information Bullettin No 789-7.
Amagliani, G., Omiccioli, E., Brandi, G., Bruce, I. J., & Magnani, M. (2010). A multiplex
magnetic capture hybridisation and multiplex Real-Time PCR protocol for pathogen
detection in seafood. Food Microbiology, 27, 580–585.
Anonymous (2004). Microbiology of food and animal feeding stuffs — Horizontal method
for the detection of Salmonella spp. UNI EN ISO 6579:2004. Geneva, Switzerland:
International Organization for Standardization.
Antony, B., Dias, M., Shetty, A. K., & Rekha, B. (2009). Food poisoning due to Salmonella
enterica serotype Weltevreden in Mangalore. Indian Journal of Medical Microbiology,
27, 257–258.
Arkoudelos, J. S., Samaras, F. J., & Tassou, C. C. (2003). Survival of Staphylococcus aureus
and Salmonella Enteritidis on salted sardines (Sardina pilchardus) during ripening.
Journal of Food Protection, 66, 1479–1481.
Aruoma, O. I. (2006). The impact of food regulation on the food supply chain. Toxicology,
127, 119–221.
Arvanitoyannis, I. S., & Varzakas, T. H. (2009). Seafood. In I. S. Arvanitoyannis (Ed.),
HACCP and ISO 22000: Application to foods of animal origin (pp. 377). Oxford:
Blackwell Publishing Ltd.
Bangtrakulnonth, A., Pornreongwong, S., Pulsrikarn, C., Sawanpanyalert, P., Hendriksen,
R. S., Lo Fo Wong, D. M. A., et al. (2004). Salmonella Serovars from humans and other
sources in Thailand, 1993–2002. Emerging Infectious Diseases, 10, 131–137.
Baudart, J., Lemarchand, K., Brisabois, A., & Lebaron, P. (2000). Diversity of Salmonella
strains isolated from the aquatic environment as determined by serotyping and
amplification of the ribosomal DNA spacer regions. Applied and Environmental
Microbiology, 66, 1544–1552.
787
Bialek, S. R., George, P. A., Xia, G. L., Glatzer, M. B., Motes, M. L., Veazey, J. E., et al. (2007). Use
of molecular epidemiology to confirm a multistate outbreak of hepatitis A caused by
consumption of oysters. Clinical Infectious Disease, 44, 838–840.
Bibek, R. (2001). Fundamental food microbiology (2nd edition). London: CRC Press LLC.
Bienfang, P. K., DeFelice, S. V., Laws, E. A., Brand, L. E., Bidigare, R. R., Christensen, S.,
et al., (in press). Prominent human health impacts from several marine microbes:
History, ecology, and public health implications. International Journal of Microbi-
ology. doi:10.1155/2011/152815.
Boinapally, K., & Jiang, X. (2007). Comparing antibiotic resistance in commensal and
pathogenic bacteria isolated from wild caught South Carolina shrimps vs. farm
raised imported shrimps. Canadian Journal of Microbiology, 53, 919–924.
Bouchrif, B., Paglietti, B., Murgia, M., Piana, A., Cohen, N., Ennaji, M. M., et al. (2009).
Prevalence and antibiotic-resistance of Salmonella isolated from food in Morocco.
Journal of Infections in Developing Countries, 3, 35–40.
Brands, D. A., Inman, A. E., Gerba, C. P., Mare, J., Billington, S. J., Saif, L. A., et al. (2005).
Prevalence of Salmonella spp. in oysters in the United States. Applied Environmental
Microbiology, 71, 893–897.
Bremer, P. J., Fletcher, G. C., & Osborne, C. (2003). Salmonella in seafood. New Zealand
Institute for Crop & Food Research Limited. http://www.crop.cri.nz/home/
research/marine/pathogens/Salmonella.pdf Last access April 2011.
Cato, J. C. (1998). Economic values associated with seafood safety and implementation
of seafood Hazard Analysis Critical Control Point (HACCP) programmes. FAO
Fisheries Technical Paper, No. 381, Rome: FAO 70 pp.
CDC, Centers for Disease Control and Prevention (2009). FoodNet 2007 surveillance
report. Atlanta: U.S. Department of Health and Human Services.
CDC, Centers for Disease Control and Prevention (2010a). Multistate outbreak of human
Salmonella Typhimurium infections associated with aquatic frogs — United States,
2009. Morbidity and Mortality Weekly Report, 58, 1433–1436.
CDC, Centers for Disease Control and Prevention (2010b). FoodNet 2010 surveillance report.
Atlanta: U.S. Department of Health and Human Services. http://www.cdc.gov/
foodborneburden/trends-in-foodborne-illness.html, lastly accessed February 2011.
CDC, Centers for Disease Control and Prevention (2010c). Surveillance for foodborne disease
outbreaks — United States, 2007. Morbidity and Mortality Weekly Report, 59, 973–979.
CSPI, Center for Science in the Public Interest (2009). Outbreak alert. http://cspinet.org/
new/pdf/outbreakalertreport09.pdf last access April 2011.
David, O. M., Wandili, S., Kakai, R., & Waindi, E. N. (2009). Isolation of Salmonella and
Shigella from fish harvested from the Winam Gulf of Lake Victoria, Kenya. Journal of
Infections in Developing Countries, 3, 99–104.
DePaola, A., Jones, J. L., Woods, J., Burkhardt, W., Calci, K. R., Krantz, J. A., et al. (2010).
Bacterial and viral pathogens in live oysters: 2007 United States market survey.
Applied and Environmental Microbiology, 76, 2754–2768.
Doyle, M. E., Kaspar, C., Archer, J., & Klos, R. (2009). White Paper on human illness caused by
Salmonella from all food and non-food vectors. Food Research Institute, UW-Madison,
Dec. 2008/February 2009. http://fri.wisc.edu/docs/pdf/FRI_Brief_Salmonella_Human_
Illness_6_09.pdf. Last access April 2011.
Duran, G. M., & Marshall, D. L. (2005). Ready to eat shrimp as an international vehicle of
antibiotic resistant bacteria. Journal of Food Protection, 68, 2395–2401.
EC (2002). Regulation (EC) No 178/2002 of the European Parliament and of the Council of
28 January 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.
EC (2003). Regulation 1831/2003/EC on additives for use in animal nutrition, replacing
Directive 70/524/EEC on additives in feeding-stuffs.
EC (2005). Commission Regulation No 2073/2005 of 15 November 2005 on microbiological
criteria for foodstuffs.
EC (2007). Commission Regulation No 1441/2007 of 5 December 2007 amending
Regulation (EC) No 2073/2005 on microbiological criteria for foodstuffs.
EFSA, European Food Safety Authority (2007). The community summary report on
trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and
foodborne outbreaks in the EU in 2006. The EFSA Journal, 130.
EFSA, European Food Safety Authority (2008). SCIENTIFIC OPINION. Food safety
considerations of animal welfare aspects of husbandry systems for farmed fish. The
EFSA Journal, 867, 1–24.
EFSA, European Food Safety Authority (2010). The community summary report on
trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the
European Union in 2008. The EFSA Journal, 8, 1496.
EU Food and Veterinary Office (e). http://ec.europa.eu/food/fvo/inspectprog/index_en.
htm, lastly accessed April 2011.
Failler, P. (2007). Future prospects for fish and fishery products. 4. Fish consumption in the
European Union in 2015 and 2030. Part 1. European overview. FAO Fisheries Circular,
No. 972/4, Part 1, (pp. 204). Rome: FAO Publishing Management Service.
FAO Fisheries and Aquaculture Department (2010a). The state of world fisheries and
aquaculture 2010. Rome: FAO Publishing Management Service.
FAO, Food and Agriculture Organization (2010b). Report of the FAO expert workshop
on the application of biosecurity measures to control Salmonella contamination in
sustainable aquaculture. Mangalore, India, 19–21 January 2010. FAO Fisheries
Circular, No. 937, Rome: FAO Publishing Management Service.
FAO, Food and Agriculture Organization (n). FAOSTAT food supply data, 2007. Available
from: http://faostat.fao.org (last accessed January 2011).
FAO/NACA/WHO (1997). Joint Study Group. Food safety issues associated with
products from aquaculture. WHO Technical Report Series, No. 883.
FAO/WHO (2005). The Codex Alimentarius Commission. Available from: http://www.
codexalimentarius.net/web/index_en (Last visited 11 st February 2011).
FDA, Food and Drug Administration (2007). Guide for the control of molluscan shellfish—
Section IV, chapter 2, 2007, growing areas. 01 Total coliform standards. http://www.
issc.org/
788 G. Amagliani et al. / Food Research International 45 (2012) 780–788
FDA, Food and Drug Administration. (2006). National antimicrobial resistance
monitoring system-enteric bacteria (NARMS): 2003 executive report. US Department
of Health and Human Services, US Food and Drug Administration, Rockville, MD.
FDA, Food and Drug Administration, Center for Veterinary Medicine (e). www.fda.gov/
cvm, lastly accessed April 2011.
Feldhusen, F. (2000). The role of seafood in bacterial foodborne diseases. Microbes and
Infection, 2, 1651–1660.
Fishery and Aquaculture Statistics database of FAO (O). http://www.fao.org/fishery/
statistics/global-aquaculture-production/en, Last access February 2011.
Foley, S. L., & Lynne, A. M. (2008). Food animal-associated Salmonella challenges:
Pathogenicity and antimicrobial resistance. Journal of Animal Science, 86,
173–187.
Gaertner, J., Wheeler, P. E., Obafemi, S., Valdez, J., Forstner, M. R. J., Bonner, T. H., et al.
(2008). Detection of Salmonellae in fish in a natural river system. Journal of Aquatic
Animal Health, 20, 150–157.
Galanis, E., Danilo, M. A., Wong, L. F., Patrick, M. E., Binsztein, N., Cieslik, A., et al. (2006).
Web-based surveillance and global Salmonella distribution, 2000–2002. Emerging
and Infectious Diseases, 12, 381–387.
Gannon, V. P. J., Graham, T. A., Read, S., Ziebell, K., Muckle, A., Mori, J., et al. (2004).
Bacterial pathogens in rural water supplies in southern Alberta, Canada. Journal of
Toxicology and Environmental Health, 67, 1643–1653.
Gillet, R. (2008). Global study of shrimp fisheries. FAO Fisheries Technical Paper, No. 475,
(pp. 331). Rome: FAO Publishing Management Service.
Greig, J. D., & Ravel, A. (2009). Analysis of foodborne outbreak data reported
internationally for source attribution. International Journal of Food Microbiology,
130, 77–87.
Guerin, P. J., De Jong, B., Heir, E., Hasseltvedt, V., Kapperud, G., Styrmo, K., et al. (2004).
Outbreak of Salmonella Livingstone infection in Norway and Sweden due to
contaminated processed fish products. Epidemiology and Infection, 132, 889–895.
Haley, B., Cole, D., & Lipp, E. K. (2006). Impact of climate and weather on Salmonella
densities in the aquatic environment. EOS, Transactions - American Geophysical
Union, 87 Abstract No. OS25M-07.
Heinitz, M. L., Ruble, R. D., Wagner, D. E., & Tatini, S. R. (2000). Incidence of Salmonella in
fish and seafood. Journal of Food Protection, 63, 579–592.
Higgins, R. (2000). Bacteria and fungi of marine mammals: A review. Canadian
Veterinary Journal, 41, 105–116.
Holtby, I., Tebbutt, G. M., Anwar, S., Aislabie, J., Bell, V., Flowers, W., et al. (2006). Two
separate outbreaks of Salmonella enteritidis phage type 14b food poisoning linked
to the consumption of the same type of frozen food. Public Health, 120, 817–823.
Hubalek, Z. (2004). An annotated checklist of pathogenic microorganisms associated
with migratory birds. Journa of Wildlife Disease, 40, 639–659.
Huss, H. H., Reilly, A., & Ben Embarek, K. P. (2000). Prevention and control of hazards in
seafood. Food Control, 11, 149–156.
Iwamoto, M., Ayers, T., Mahon, B. E., & Swerdlow, D. L. (2010). Epidemiology of seafood-
associated infections in the United States. Clinical Microbiology Reviews, 23,
399–411.
Japan Food Poisoning Statistics. (2009). Inspection and Safety Division, Department of
Food Safety, Pharmaceutical and Food Safety Bureau, Ministry of Health Labour and
Welfare (http://www.mhlw.go.jp/english/topics/foodsafety/index.html, last access
7th February 2011).
Jay, S., Diane, D., Dundas, M., Frankish, E., & Lightfoot, D. (2003). Salmonella. In A. D.
Hocking (Ed.), Foodborne microorganisms of public health significance
(pp. 207–266). (6th ed.). Waterloo, NSW, Australia: Australian Institute of Food
Science and Technology Inc.
Johnson, J. Y. M., Thomas, J. E., Graham, T. A., Townshend, I., Byrne, J., Sellinger, L. B., et al.
(2003). Prevalence of Escherichia coli O157:H7 and Salmonella spp. in surface
waters of southern Alberta and its relation to manure sources. Canadian Journal of
Microbiology, 49, 326–335.
Khan, A. A., Cheng, C. M., Van, K. T., Summage West, C., Nawaz, M. S., & Khan, S. A.
(2006). Characterization of class 1 integron resistance gene cassettes in Salmonella
enterica serovars Oslo and Bareily from imported seafood. Journal of Antimicrobial
Chemotherapy, 1308–1310.
Koonse, B., Burkhardt, W., Chirtel, S., & Hoskin, G. P. (2005). Salmonella and the sanitary
quality of aquacultured shrimp. Journal of Food Protection, 68, 2527–2532.
Kumar, R. (2009). Distribution trends of Salmonella serovars in India (2001–2005).
Transactions of the Royal Society of Tropical Medicine and Hygiene, 103, 390–394.
Kumar, R., Surendran, P. K., & Thampuran, N. (2008a). Evaluation of culture, ELISA and
PCR assays for the detection of Salmonella in seafood. Letters in Applied Microbiology,
46, 221–226.
Kumar, R., Surendran, P. K., & Thampuran, N. (2008b). An eight-hour PCR-based
technique for detection of Salmonella serovars in seafood. World Journal of
Microbiology and Biotechnology, 24, 627–631.
Kumar, R., Surendran, P. K., & Thampuran, N. (2009). Distribution and genotypic
characterization of Salmonella serovars isolated from tropical seafood of Cochin,
India. Journal of Applied Microbiology, 106, 515–524.
Kumar, R., Surendran, P. K., & Thampuran, N. (2010). Rapid quantification of Salmonella
in seafood using Real-Time PCR assay. Journal of Microbiology and Biotechnology, 20,
569–573.
Laurenti, G. (2007). 1961–2003 fish and fishery products: world apparent consumption
statistics based on food balance sheets. FAO Fisheries Circular, No.821, Rev.8,
(pp. 429). Rome: FAO Publishing Management Service.
Liebert, C. A., Hall, R. M., & Summers, A. O. (1999). Transposon Tn21, flagship of the
floating genome. Microbiology and Molecular Biology Review, 63, 507–522.
Lunestad, B. T., Nesse, L., Lassen, J., Svihus, B., Nesbakken, T., Fossum, K., et al. (2007).
Salmonella in fish feed; occurrence and implications for fish and human health in
Norway. Aquaculture, 265, 1–8.
Martinez, I., James, D., & Loreal, H. (2005). Application of modern analytical techniques
to ensure seafood safety and authenticity. FAO Fisheries Technical Paper, No. 455,
(pp. 26). Rome: FAO Publishing Management Service.
Martinez-Urtaza, J., & Liebana, E. (2005). Use of pulsed-field gel electrophoresis to
characterize the genetic diversity and clonal persistence of Salmonella senftenberg
in mussel processing facilities. International Journal of Food Microbiology, 105,
153–163.
Martinez-Urtaza, J., Saco, M., de Novoa, J., Perez-Pieiro, P., Peiteado, J., Lozano-Leon, A.,
et al. (2004). Influence of environmental factors and human activity on the
presence of Salmonella serovars in a marine environment. Journal of Applied and
Environmental Microbiology, 70, 2089–2097.
McKean, J. D. (2001). The importance of traceability for public health and consumer
protection. Review of Science and Technique Office International Epizootes, 20, 363–371.
Meinersmann, R. J., Berrang, M. E., Jackson, C. R., Fedorka-Cray, P., Ladely, S., Little, E.,
et al. (2008). Salmonella, Campylobacter and Enterococcus spp.: their antimicrobial
resistance profiles and their spatial relationships in a synoptic study of the Upper
Oconee river basin. Microbial Ecology, 55, 444–452.
Minami, A., Chaicumpa, W., Chongsa-Nguan, M., Samosornsuk, S., Monden, S., Takeshi,
K., et al. (2010). Prevalence of foodborne pathogens in open markets and
supermarkets in Thailand. Food Control, 21, 221–226.
Murray, P. R. (1999). Manual of clinical microbiology (7th ed.). Washington, D.C.: ASM
Press (Chapter 28).
NACMCF (2008). Response to the questions posed by the Food and Drug Administration
and the National Marine Fisheries Service regarding determination of cooking
parameters for safe seafood for consumers. Journal of Food Protection, 71(6),
1287–1308.
Nawaz, M. S., Erickson, B. D., Khan, A. A., Khan, S. A., Pothulari, J. V., Rafii, F., et al. (2001).
Human health impact and regulatory issues involving antimicrobial resistance in
the food animal production environment. Regulatory Research Perspectives, 1, 1–10.
Nesse, L. L., Løvold, T., Bergsjø, B., Nordby, K., Wallace, C., & Holstad, G. (2005).
Persistence of orally administered Salmonella enterica serovars Agona and
Montevideo in Atlantic salmon (Salmo salar L.). Journal of Food Protection, 68,
1336–1339.
Newell, D. G., Koopmans, M., Verhoef, L., Duizer, E., Aidara-Kane, A., Sprong, H., et al.
(2010). Food-borne diseases — The challenges of 20 years ago still persist while
new ones continue to emerge. International Journal of Food Microbiology, 139,
S3–S15.
Norhana, M. N. W., Poole, S. E., Deeth, H. C., & Dykes, G. A. (2010a). Prevalence,
persistence and control of Salmonella and Listeria in shrimp and shrimp products: A
review. Food Control, 21, 343–361.
Norhana, M. N. W., Poole, S. E., Deeth, H. C., & Dykes, G. A. (2010b). The effects of
temperature, chlorine and acids on the survival of Listeria and Salmonella strains
associated with uncooked shrimp carapace and cooked shrimp flesh. Food
Microbiology, 27, 250–256.
Pal, A., & Marshall, D. L. (2009). Comparison of culture media for enrichment and
isolation of Salmonella spp. from frozen Channel catfish and Vietnamese basa fillets.
Food Microbiology, 26, 317–319.
Panisello, P. J., Rooney, R., Quantick, P. C., & Stanwell-Smith, R. (2000). Application of
foodborne disease outbreak data in the development and maintenance of HACCP
systems. International Journal of Food Microbiology, 59, 221–234.
Ponce, E., Khan, A. A., Cheng, C. M., Summage-West, C., & Cerniglia, C. E. (2008).
Prevalence and characterization of Salmonella enterica serovar Weltevreden from
imported seafood. Food Microbiology, 25, 29–35.
Rapid Alert System for food, Feed (RASFF) (2010). RASFF annual report 2009.
Luxembourg: Publications Office of the European Union.
Ristori, C. A., dos Santos Pereira, M. A., & Gelli, D. S. (2007). Behaviour of Salmonella
Rubislaw on ground black pepper (Piper nigrum L.). Food Control, 18, 268–272.
Roy, P., Dhillon, A. S., Lauerman, L. H., Schaberg, D. M., Bandli, D., & Johnson, S. (2002).
Results of Salmonella isolation from poultry products, poultry, poultry environ-
ment, and other characteristics. Avian Disease, 46, 17–24.
Serrano, P. H. (2005). Responsible use of antibiotics in aquaculture. FAO Fisheries Technical
Paper, No. 469, Rome: FAO 97 pp.
Setti, I., Rodriguez-Castro, A., Pata, M. P., Cadarso-Suarez, C., Yacoubi, B., Bensmael, L., et al.
(2009). Characteristics and dynamics of Salmonella contamination along the coast of
Agadir, Morocco. Applied and Environmental Microbiology, 75, 7700–7709.
Shabarinath, S., Kumar, H. S., Khushiramani, R., Karunasagar, I., & Karunasagar, I. (2007).
Detection and characterization of Salmonella associated with tropical seafood.
International Journal of Food Microbiology, 114, 227–233.
Shellenbarger, G. G., Athearn, N. D., Takekawa, J. Y., & Boehm, A. B. (2008). Fecal
indicator bacteria and Salmonella in ponds managed as bird habitat, San Francisco
Bay, California, USA. Water Resaearch, 42, 2921–2930.
Simental, L., & Martinez-Urtaza, J. (2008). Climate patterns governing the presence and
permanence of Salmonella in coastal areas of Bahia de Todos Santos, Mexico. Applied
and Environmental Microbiology, 74, 5918–5924.
Touron, A., Berthe, T., Pawlak, B., & Petit, F. (2005). Detection of Salmonella in
environmental water and sediment by a nested multiplex polymerase chain
reaction assay. Research Microbiology, 156, 541–553.
Van, T. T., Moutafis, G., Istivan, T., Tran, L. T., & Coloe, P. J. (2007). Detection of Salmonella
spp in retail raw food samples from Vietnam and characterisation of their antibiotic
resistance. Applied and Environmental Microbiology, 73, 6885–6890.
Winfield, M. D., & Groisman, E. A. (2003). Role of nonhost environments in the lifestyles
of Salmonella and Escherichia coli. Applied and Environmental Microbiology, 69,
3687–3694.
Yan, H., Li, L., Alam, M. J., Shinoda, S., Miyoshi, S., & Shi, L. (2010). Prevalence and
antimicrobial resistance of Salmonella in retail foods in northern China. Interna-
tional Journal of Food Microbiology, 143, 230–234.