Incidence and role of Salmonella in seafood safety

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

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 fish. 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 fish 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: Università 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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identified 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 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.

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”, “Salmonella + fish”, “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), 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

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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 preparations are also based on traditions. Processed fishery 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 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, Gramnegative 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 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

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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 classified 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 flagellar structures generate the antigenic variation that is reflected 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 2000–2001, 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 fish 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 fish (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 (Winfield & 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 fish (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 fish pathogen (FAO, 2010b). Saltwater and freshwater wetlands and ponds serve as important habitats for juvenile fish and shellfish, 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, Bovismorbificans 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 influenced 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 shellfish harvesting in the US. In shellfisheries in the US, the presence of fecal coliform is assessed to determine the risk of exposure to pathogens through shellfish 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 insufficient to guarantee the absence of the pathogen in fish and fishery 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 modifications. 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 Shellfish 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, Moutafis, Istivan, Tran, and Coloe (2007) Kumar et al. (2008a)

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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

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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

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) Finfish (10 outbreaks, 261 cases) Total: 18 outbreaks, 374 cases of salmonellosis between 1973 and 2006 Fish and fish products (5 outbreaks, 1%) Crustaceans, shellfish, molluscs and products thereof (7 outbreaks, 1.4%)

Not reported

Iwamoto et al. (2010)

Fish and fishery products (0.3) Crustaceans (0.5), live bivalve molluscs (0.9), molluscan shellfish (1.1) Clam (34.2) 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)

EFSA (2010)

EU

India

Japan China Thailand Morocco

Fish and shellfish (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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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 fish products Crustaceans, shellfish, 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 fish harvested in Lake Victoria, Kenya, which supports the most productive freshwater fishery 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 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 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 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.

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 fish diseases and/or pathogen carriage. Pal and Marshall (2009) examined Salmonella contamination in farm raised catfish, both from US (33% prevalence) and Vietnam (50%). However, the risk is significantly reduced thanks to a high level of control achieved through good aquaculture practices (GAP) (Doyle, Kaspar, Archer, & Klos, 2009). Hence fish farmed worldwide have a good safety record with respect to Salmonella, as confirmed by the lack of reports linking salmonellosis to the consumption of finfish 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 fish or with feed that has been improperly stored or prepared under poor hygienic conditions. Trash fish can also be used in the manufacture of fishmeal and fish oil. In the last EFSA Report (2010), fish 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 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 this pathogen and prevent cross contamination. 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 processoriented 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

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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 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 identified 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 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.,

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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 fish 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 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 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 definitive 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, sulfisoxazole, 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 sulfisoxazole, streptomycin and tetracycline.

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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 fluoroquinolones, also showing multiresistance patterns to between 2 to 10 or more drugs. As a final consideration, careful and judicious use of antimicrobials should be recommended. Although their use on fish 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 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 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 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 crosscontamination 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

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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 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 underestimated. Hence surveillance systems adopted by national governments 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 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. 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.

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