Risks Associated with Fish and Seafood

ABSTRACT

Fresh fish and seafood are highly perishable, and microbiological spoilage is one of the important factors that limit their shelf life and safety. Fresh seafood can be contaminated at any point from rearing or harvesting to processing to transport or due to cross-contamination by consumer mishandling at home. With the increase in the demand for fish and seafood, aquaculture production is increasing, which could lead to new risks that will need to be addressed in the future to control foodborne pathogens.

INTRODUCTION

In the United States, the most popular fish and seafood products consumed per capita in 2015 were shrimp (4.00 lb), salmon (2.88 lb), tuna (2.20 lb), tilapia (1.38 lb), pollack (0.97 lb), pangasius (0.74 lb), cod (0.60 lb), crab (0.56 lb), catfish (0.52 lb), and clams (0.35 lb) (1). Fresh fish and seafood are highly perishable, and microbiological spoilage is one of the important factors that limit shelf life and safety. Fresh seafood can be contaminated at any point from rearing or harvesting to processing to transport or due to cross-contamination by consumer mishandling at home.

Fish and seafood have been the cause of many foodborne diseases and outbreaks in the United States and worldwide. The main microorganisms that cause foodborne outbreaks associated with fish and seafood include bacteria, viruses, and parasites (Fig. 1). The potential risk associated with fish and seafood can often be directly related to the environmental conditions and microbial quality of the water from which it was caught (2). Water qualities such as temperature, salt content, distance between location of catch and polluted areas, and natural occurrence of bacteria in the water can affect the microbial quality of the fish and seafood (2). Polluted waters have been associated with bacterial contamination of fish and seafood, and the sources of pollution have included overboard sewage discharge into harvest areas, illegal harvesting from sewage-contaminated waters, and sewage runoff from points inland after heavy rains or flooding (3). Additionally, the season during which the fish and seafood are harvested, the method of catch, chilling conditions, and how they are handled, prepared, and served can increase the risk of contamination (2, 3). Fish and seafood may also become contaminated as a result of storage or transportation at improper temperatures and contamination by food handlers or through cross-contamination.

FIGURE 1.

Foodborne illness cases associated with fish and shellfish (crustaceans and mollusks) in the United States, 1998 to 2008 (4).

Crustaceans contaminated with bacteria are often the culprit in foodborne disease outbreaks. Many of these outbreaks are due to improperly prepared or mishandled crustaceans (Fig. 1) (4). Detailed investigations of bacteria-related foodborne illnesses have frequently focused on oysters, since they are often consumed uncooked (5). However, a significant number of bacterial foodborne disease outbreaks are caused by eating crustaceans (Fig. 1). There is usually no apparent reason for crustaceans to cause foodborne illness, since they are typically cooked before being consumed (6).

There are incidents of fish and seafood becoming contaminated with foodborne pathogens such as Listeria (7–9), Salmonella (10), and Vibrio spp. (11, 12); hepatitis A (13); and norovirus (13). Some of these pathogens are naturally found in the environment (Vibrio spp., Listeria monocytogenes) and can pose serious health risks if the food is not cooked adequately to kill them. Another factor that contributes to foodborne outbreaks is that 20% of the fish and shellfish consumed in the United States are derived from recreational or subsistence fishing and are not subject to health-based control. Usually consumers rely on the color of the flesh as a parameter for doneness during cooking, which does not ensure the safety of these products. In 2007, the National Advisory Committee on Microbiological Criteria for Foods was asked to provide scientific guidance to the FDA and the National Marine Fisheries on cooking procedures for fish and seafood for consumers (14). The report found that most of the consumer cooking methods for fish and seafood were based on quality and not on scientific information to ensure destruction of foodborne pathogens.

BACTERIAL RISKS ASSOCIATED WITH FISH AND SEAFOOD

Outbreaks associated with the consumption of tainted seafood have been documented for many centuries. However, in the early 20th century, some major outbreaks gained the attention of public officials. One such outbreak occurred in 1925 on the East Coast. An outbreak of typhoid fever was eventually traced back to oysters contaminated by sewage (15). It was so severe that it prompted officials to petition the surgeon general of the United States to draw up formal guidelines for the safety of the public to replace the loose recommendations the shellfish industry followed at the time. Over time, small outbreaks continued around the country, and there were still many advances in sanitation, hygiene, and general processing that had yet to be discovered or implemented as regular practice.

Things started changing in the 1970s with advances in fields such as bacteriology and microbiology. For example, in 1978, when over 1,100 people became ill with Vibrio parahaemolyticus at a shrimp dinner in Port Allen, LA, a thorough investigation of this foodborne disease outbreak was conducted. Upon further examination, it was discovered that the food was grossly mishandled: not only were the shrimp cross-contaminated after cooking, but they were held unrefrigerated for 8 hours in the middle of the Louisiana summer before being served (16). Those are two extreme examples, and since then, federal agencies such as the FDA and the CDC have instituted strict shellfish industry regulations, have developed sanitization practices that minimize cross-contamination, Hazard Analysis Critical Control Point (HACCP), and in general, have tried to ensure safe food handling and consumer safety. However, recent statistics have shown that foodborne disease outbreaks due to shellfish are still a concern for consumers (17). Currently, conditions in processing plants are very strict, but there is still typically at least one outbreak per year that leads to a product recall. Recently, fish and seafood-associated bacterial or viral illnesses have typically been caused by cross-contamination or mishandling, either in private residences or in restaurant/delicatessen settings (18).

Salmonella

Reports to the CDC of outbreaks associated with fish and seafood have shown that Salmonella was the leading cause of these outbreaks. Of these Salmonella outbreaks, 10, with 224 cases, were caused by crustaceans; 14 outbreaks, with 852 cases, were caused by fish; and 2 outbreaks, with 13 cases, were caused by molluscan shellfish (17). Salmonella has a prevalence rate of 7.4% along the U.S. coastlines, with Salmonella enterica serovar Newport occurring at a higher percentage (75%) than other serovars (19). Acute gastroenteritis caused by Salmonella spp. continues to be a worldwide public health concern (19). In humans, salmonellosis is usually due to the consumption of contaminated food or water. The fecal wastes from infected animals and humans are important sources of bacterial contamination of the environment and the food chain (20). During a 9-year study (1990 to 1998), the FDA noted an overall incidence of Salmonella in 7.2% of 11,312 samples from imported and 1.3% of 768 samples from domestic U.S. seafood (10). Salmonella has also been detected in U.S. market oysters (19) and in other imported seafood from different countries (21). The incidence of Salmonella in seafood is highest in the central Pacific and African countries and lowest in Europe, including Russia, and North America (12% versus 1.6%) (10). The presence of Salmonella spp. in seafood has been reported in Vietnam (22), India (20, 23, 24), Sri Lanka (25), Thailand (26), Taiwan (27), and Japan (28). All of these countries export seafood into the United States, and the FDA is concerned about possible contamination of these products with Salmonella.

The FDA has conducted studies which showed that aquacultured seafood was more likely than wild-caught seafood to contain Salmonella (29). Many researchers also have evaluated the presence of Salmonella, fecal coliforms, and Escherichia coli in shrimp aquaculture ponds (6, 30–32). The relationship between the occurrence of Salmonella in shrimp from aquaculture operations, and the concentration of fecal bacteria in the source and grow-out pond water has been described by Koonse et al. (29). These could be the possible routes of contamination of shrimp and other seafood with this pathogen.

Salmonella infection presents as either enteric syndrome, also called typhoid, or as gastroenteritis, which is more common (5). Many species of Salmonella can be found on seafood because Salmonella is present in estuaries. However, it is still debated if Salmonella is in waters because it is a part of the natural marine flora, if it is due to contamination from sewage run-off, or both (33). When a pathogen is commonly found on surfaces, the environment, and the food product, it is almost impossible to tell if the contamination is from a processing failure, improper storage conditions, unsanitary workers, or some combination of factors (10).

It is generally believed that the gastroenteritis syndrome of Salmonella is one of the most underreported foodborne illnesses because it is self-limiting. Salmonella has been implicated in many foodborne outbreaks involving seafood mixtures such as crab cakes. In these cases, it is not clear which component of the crab mixture is responsible for contributing the Salmonella. Many outbreaks are caused by eggs used as a binding agent in the seafood mixtures, but some have no obvious cause. For example, a 10-person outbreak in Ohio caused by crab cakes, lobster cakes, and crab-stuffed lobster served in a restaurant in July 2001 was eventually traced back to contaminated eggs (34). However, that same year, another 10-person outbreak caused by crab cakes served in a Washington, DC, restaurant could not be traced to any egg contamination source (34). Therefore, more investigation into the possible source of contamination of Salmonella in fish and seafood should be considered because it is one of the major foodborne bacterial pathogens.

L. monocytogenes

L. monocytogenes is prevalent in nature and can be found in soil, foliage, and the feces of animals and humans (2). This species is indigenous to the marine and estuarine environments, so its association with fish and seafood should be expected (35). It has also been known to establish itself as an in-house bacterium in a processing facility. It can create a biofilm on stainless steel surfaces and can be isolated from equipment, cold stores, and floors, enabling it to recontaminate products in the production environment (2). In-house reservoirs of L. monocytogenes have been reported from fish-processing establishments (2), and the bacterium has been isolated from domestic and imported fresh, frozen, and processed seafood products, including crustaceans, molluscan shellfish, and fish (36).

L. monocytogenes has many serotypes, but it is serotype ½b that is associated with seafood contamination (37). L. monocytogenes has unique survival properties: it is psychrotrophic (able to grow at refrigeration temperatures) (38), can survive irradiation (39), can grow in high salt concentration, and can survive a wide range of pH (37). The greatest threat from L. monocytogenes is through ready-to-eat products such as processed crabmeat. A study by Farber (40) demonstrated that L. monocytogenes grows better on crabmeat than on other seafood. Since it can grow to high concentrations in refrigerated, vacuum-packed, ready-to-eat foods that will not be subjected to further processing such as heating, there is a serious health risk associated with this organism (41). This has caused some safety and regulation issues, since there is no established infectious dose (36, 37).

Raw fish and shrimp have been linked to an outbreak of L. monocytogenes which caused nine deaths in New Zealand (7). Since this outbreak, the seafood industry has been concerned with the ability of L. monocytogenes to grow to high levels in shrimp when stored at refrigerated temperatures (7–9). Consumers buy raw fish and seafood from their local grocery store and cook it at home, which greatly reduces the risk of outbreaks, but the extent of cooking depends on various factors such as the size of the seafood product and the type of cuisine or dish. The shelf life of seafood is greatly influenced by microbial load, added to the fact that these are highly perishable commodities (8). The National Advisory Committee on Microbiological Criteria for Foods report concluded that L. monocytogenes is a pathogen of concern in ready-to-eat seafood products but not for raw fish and seafood products that will be cooked by consumers (14).

Vibrio cholerae

V. cholerae is a bacterium that many believe is no longer a threat, especially to U.S. citizens. Cholera is thought to be an issue for countries with questionable sanitation practices. Unfortunately, there are approximately one to two cases of cholera reported per week in the United States (42). While many of these cases of cholera are associated with travel to places with endemic cholera outbreaks, it should be remembered that the Gulf Coast has a long history of cholera. The first confirmed case was in Louisiana in 1832, and the last case was in 1873.

There were no more reported cases of cholera in the Gulf Coast states until 1973. Then a 4-case cluster of 11 people infected with V. cholerae O1 biotype El Tor serotype Inaba was reported in Abbeville, LA, in 1978, the result of eating contaminated crabs that had been boiled between 10 and 20 minutes or steamed up to 35 minutes (43). V. cholerae has been repeatedly isolated in blue crabs from the Gulf Coast. The Gulf Coast has been a reservoir of naturally occurring environmental toxigenic V. cholerae, and the crabs harvested from that area remain a risk to consumers, especially during the warmer months (44). In 2005 there were two confirmed cases of toxigenic V. cholerae O1, serotype Inaba, biotype El Tor, isolated from a couple from Louisiana after they ate locally caught crabs and shrimp (45).

V. cholerae O1, due to its higher resistance compared to other Vibrio bacteria, could lead to safety hazards in seafood products (46). A majority of fish and seafood products are cooked at home by the consumer or in commercial/institutional settings. This reduces the number of microorganisms in shrimp (47), but the extent of cooking plays a large role in destruction of this bacteria. V. cholerae O1 is recognized as a bacterium that is indigenous in the marine environment (48). Marine foods have been identified as vehicles for the transmission of cholera (49). The factors and mechanisms that affect the bacterium’s survival in the aquatic environment are not completely understood (50). However, some research groups have stated that this pathogen is able to attach to abiotic surfaces, to zooplankton and phytoplankton, and to the carapaces of crustaceans such as shrimp and crab (12, 51, 52). Vibrio bacteria are generally considered to be heat-sensitive, but some reports show that V. cholerae O1 has some resistance in hot foods (53).

V. parahaemolyticus

In the Unites States, V. parahaemolyticus was first noted in the Chesapeake Bay in association with dead and dying blue crabs in 1969, whereas the first fully documented case occurred in Maryland in 1971, which was also associated with steamed crab (54). The ecology of Chesapeake Bay was examined, and it was found that the incidence of V. parahaemolyticus was correlated with water temperatures. The organism was not found in sea waters during the winter months, but it could be isolated from sediments in small numbers. It was later established that V. parahaemolyticus could survive the winter months by attaching to planktons and then proliferate inside the planktons (55). With the increase in water temperatures, V. parahaemolyticus is released from the planktons and can be easily detected in the waters.

V. parahaemolyticus illness is mainly associated with consumption of contaminated raw or undercooked shellfish. Oysters, clams, and mussels and cooked crustaceans such as shrimp and crab have also been implicated in V. parahaemolyticus infections (6). V. parahaemolyticus can increase to high levels in oysters because of its ability to enhance its concentration and survival in oysters. Oysters are filter feeders, and V. parahaemolyticus is associated with zooplanktons, which results in enhancing the bioconcentration of the bacteria in oysters (56).

Oysters which were harvested from the Gulf of Mexico, in particular, showed high Vibrio counts. A survey of retail oysters in the Gulf of Mexico, North Atlantic, Pacific, and Mid-Atlantic regions found high V. parahaemolyticus and Vibrio vulnificus counts during the summer months (57), when V. parahaemolyticus counts in freshly harvested oysters could exceed 10⁴ most probable number/g (57).

V. parahaemolyticus is the Vibrio spp. most associated with blue crabs (58). Due to the halophilic nature of the Vibrio spp., V. parahaemolyticus grows very well in the same high-salinity habitat necessary for blue crabs to complete their life cycle (59). Both V. cholerae and V. parahaemolyticus have been found to bio-accumulate in the gut and gills of blue crabs, most likely due to the crabs’ omnivorous diet (60). V. parahaemolyticus was recognized as an emerging foodborne illness in 1950 (61). In 1971, the United States experienced its first major V. parahaemolyticus foodborne outbreak, which was associated with crabs in Maryland. The outbreak caused approximately 425 people to become ill and was traced to improperly steamed crabs (54, 62). In 1998, the CDC received a report that 13 people in Florida became ill with V. parahaemolyticus from eating crabs (58). In New York in 2006, 80 people were diagnosed with V. parahaemolyticus after eating crab in a restaurant (63). Approximately 25 serotypes of V. parahaemolyticus are being monitored by the CDC (64). In addition, emerging research has determined that a specific gene, the tdh gene, was responsible for a virulence factor capable of causing the hemolytic syndrome when V. parahaemolyticus colony counts were well below the FDA-accepted V. parahaemolyticus limits (5). Less than 5% of environmental isolates produce tdh (65).

V. vulnificus

V. vulnificus is considered the most serious of all the pathogenic Vibrio spp. because it has been identified as being the leading cause of seafood-related fatalities (61). The infectious dose of V. vulnificus is 10³ bacteria/g of food, but it is one of the more heat-sensitive bacteria and is easily destroyed with proper cooking (66). Of the thermal death times listed in the FDA fish and fishery products hazards and control guidance manual, those for the most virulent strains of V. vulnificus were much lower than those for L. monocytogenes (2). The danger with foodborne illness associated with V. vulnificus is its propensity to progress into severe necrotizing wound infections or fatal septicemia in patients with pre-existing conditions such as hemochromatosis or cirrhosis (67, 68). Liver disease plays a particular factor in the virulence of V. vulnificus due to the availability of free iron in the patient’s serum (67, 68). Of the Vibrio cases that occur, V. vulnificus has the highest mortality rate: approximately 50% of the cases result in death approximately 48 hours postconsumption (64). Interestingly, it is very common for only one member of a family to show symptoms of V. vulnificus, mainly due to only specific family members having compromised immune systems (61). V. vulnificus and V. parahaemolyticus are regularly isolated together in crabs sampled for bacterial titers (69).

Clostridium botulinum

C. botulinum is found in marine sediments mainly as spores and can contaminate fish and seafood. If the conditions are right, the spores can germinate into the vegetative state and start producing neurotoxins that cause botulism. The optimal conditions for C. botulinum to produce toxins are anaerobic conditions and at pH above 4.6.

Each year about 150 confirmed cases of botulism occur in the United States for all food categories (70). Controlling the growth of C. botulinum in fish and seafood can be achieved by reducing the pH below 4.6, using salt or sodium nitrite, by lowering the moisture content, and by lowering the temperature (71).

VIRAL RISKS ASSOCIATED WITH FISH AND SEAFOOD

Seawater can become contaminated with enteric viruses and pose a health risk to people. These viruses enter source waterways through the direct or indirect discharge of treated and untreated human and animal waste into rivers, streams, and estuaries (72). In general, waterborne human enteric viruses pose a greater health risk than enteric bacteria due to the low infectious dose, which may be as little as one virion (73).

Enteric viruses replicate in the gastrointestinal tract and are shed in the feces of infected individuals. Most enteric viruses are morphologically similar and consist of an icosahedral, nonenveloped capsid, which surrounds a single-stranded RNA (e.g., norovirus, hepatitis A virus) molecule. Noroviruses and hepatitis A are the most common enteric viruses transmitted by fish and seafood (13).

Studies have shown that sediments may entrap enteric viruses and that when disturbed they can release viruses into the body of water (74, 75). Some aquatic organisms such as bivalve molluscan shellfish are filter feeders and are able to accumulate microorganisms from the surrounding water to a high titer with a concentration factor up to 99-fold (76). Unlike bacteria, viruses can be retained in oyster tissue for a long period of time and make the depuration process relatively ineffective (77). Consequently, even after shellfish are considered safe from a bacteriological standpoint (e.g., following conventional depuration), the risk to consumers’ health may still exist.

The National Shellfish Sanitation Program (NSSP) routinely determines the absence of bacterial pathogens from shellfish growing areas by using coliform bacteria as indicators of water quality. However, when growing areas are implicated as the source of shellfish causing illness consistent with viral etiology, the NSSP requires closure for a minimum of 21 days.

Since viruses persist longer than bacteria in growing waters and in shellfish (78), it takes considerably longer for shellfish to eliminate viruses (78), and, while the persistence of these coliform bacteria in shellfish growing areas is comparable to that of bacterial pathogens, the relationship between bacterial indicators and the presence of enteric viruses such as noroviruses is poor (78, 79). Therefore, if shellfish harvest areas become unexpectedly contaminated, the likelihood exists that viral pathogens may remain viable in shellfish long after growing waters appear safe according to the NSSP bacteriological criteria. Recognizing these facts, and lacking an alternative viral indicator or any other reasonable way to judge, the NSSP originally stipulated a 3-week closing period as the criterion for achieving safe shellfish when viral pathogens are known or suspected to be involved.

NOROVIRUS

A majority of seafood outbreaks result from the consumption of raw or undercooked bivalve molluscan shellfish contaminated with enteric viruses (80). One of the major enteric viruses associated with shellfish is norovirus, which is one of the causative agents of viral gastroenteritis in humans and has caused several outbreaks throughout the world (81). Norovirus is associated with up to 10% of hospitalizations in the United States, up to 200,000 deaths in children under 5 years old in developing countries, and mortality in the elderly (82). According to the CDC, norovirus was the number-one foodborne illness in the United States in 2011 and had the highest death rate (83).

Norovirus outbreaks are frequently reported in the United States. According to the FDA, many norovirus outbreaks have been linked to consumption of oysters obtained from commercial harvesting areas along the Gulf Coast: Louisiana (Port Sulphur, 2010, and Calcasieu Basin, 2013), Mississippi (Pass Christian, 2009), and Texas (San Antonio Bay, 2007). On 28 and 29 April 2012, 14 people became ill with norovirus after consuming oysters at a restaurant in New Orleans, LA. The oysters were traced back to oyster harvesting area 23, Terrebonne Parish, off the coast of Louisiana, which resulted in the temporary closure of the harvesting area (84).

In 2013 scientists investigated the occurrence of norovirus and microbial indicators of fecal contamination in eastern oysters (Crassostrea virginica) and water from commercial harvesting areas along the Louisiana Gulf Coast (January to November of 2013). All the sampling locations (harvesting areas 9 through 13) were among the most active commercial oyster harvesting areas and remained open during the sampling period. The results of this study found that the microbial fecal indicators (aerobic plate count, enterococci, fecal coliforms, E. coli, male-specific coliphages, and somatic coliphages) were detected at levels lower than public health concerns. Despite low levels of fecal contamination in the open areas for oyster and harvesting water collection, norovirus GII was detected in oysters collected from area 12 in June 2013 (85).

An outbreak of norovirus occurred in January 2013 in Cameron Parish, Louisiana. The individuals who became ill had eaten oysters collected from Louisiana Gulf Coast area 30. A stool specimen was obtained from an infected individual, and the suspected oysters were also analyzed. The norovirus strain in the stool belonged to GII.4 Sydney; however, the oysters were negative and could not be linked to the outbreak (85).

Current regulations regarding the safety of seafood rely on the levels of fecal coliforms and/or E. coli present in seafood and/or harvest waters. Studies have found that norovirus can be detected in seafood even when microbial indicators are low and in compliance with the U.S. federal standards. As such, there could be a potential health hazard to seafood consumers. This emphasizes the need for regular monitoring of norovirus in commercial fish and seafood harvesting areas to reduce the risk of viral outbreaks.

HEPATITIS A

Enteric viruses such as hepatitis A virus are responsible for a large proportion of food- and waterborne illnesses. These viruses are transmitted to humans via the fecal-oral route, usually from contaminated water or foods such as raw shellfish (86). Hepatitis A infection is the leading worldwide cause of acute viral hepatitis, and outbreaks have occurred among consumers of shellfish harvested from fecally polluted waters. Outbreaks of hepatitis A virus caused by the consumption of raw shellfish have been reported regularly since 1962, and raw or undercooked clams or oysters were implicated as the most frequent vehicles of infection (75, 87–89). In 2005 a multistate outbreak of hepatitis A occurred in Alabama, Florida, South Carolina, and Tennessee due to consumption of oysters obtained from Louisiana harvesting sites (89). There is a greater likelihood of shellfish harboring hepatitis A virus in autumn and winter, coinciding with the seasons that shellfish are among the most popular dining choices (86).

Hepatitis A virus appears to be extremely stable in the environment, with only a 100-fold decline in infectivity over 4 weeks at room temperature, and up to 12 months in fresh or salt water (6). Hepatitis A virus appears to be relatively resistant to free chlorine, especially when the virus is associated with organic matter.

PARASITIC RISKS ASSOCIATED WITH FISH AND SEAFOOD

The most common parasites associated with outbreaks in fish and seafood include round worms (Anisakis spp., Pseudoterranova spp., Eustrongylides spp., and Gnathostoma spp.), tape worms (Diphyllobothrium spp.), and flukes (Clonorchis sinensis, Opisthorchis spp., Heterophyes spp., Metagonimus spp., Nanophyetus salmincola, and Paragonimus spp.).

Parasitic outbreaks in fish and seafood are rare in the United States. Most outbreaks have been associated with eating raw or undercooked fish and seafood. The heat process used to control bacterial pathogens will also kill parasites (71).

AQUACULTURE PRODUCTION RISKS ASSOCIATED WITH FISH AND SEAFOOD

Aquaculture production has greatly increased outside and inside the United States, and now supplies 46% of the world’s seafood supply (90). This trend could lead to increased risks of safety hazards related to fish and seafood consumption due to biological contamination in farm culture waters compared to natural seawater as a result of the proximity of culture farms to urban areas (2). A number of factors have been shown to influence the safety of aquaculture products including location, farmed species, husbandry practices, postharvest processing, and cultural habits of food preparation and consumption (91).

Salmonella contamination in cultured shrimp products is a problem, and contamination of culture environments can occur through the following routes: run-off of organic water into ponds during rainfall; animal waste introduced directly (bird droppings or frogs) or indirectly (runoff); fertilization of ponds with noncomposted manures; integrated farming systems with animals housed in proximity to ponds; toilets discharging into ponds; contaminated source water; unsanitary ice, water, containers, and poor hygienic handling practices; and contaminated feed (90, 91). A study by the FDA showed that aquacultured seafood was more likely to contain Salmonella than wild-caught seafood (29). Additionally, several reports have been made on the prevalence of Salmonella in shrimp culture environments (91).

Another major issue facing the aquaculture industry is the fact that extensive use of antibiotics in agricultural animal production can result in the development of antibiotic-resistant pathogens and that these pathogens can infect and transfer resistance to humans (92). The development of resistant pathogens in aquaculture environments has been well documented, and the transfer of resistance-encoding plasmids between aquaculture environments and humans has been reported (21, 92). The term “resistance” refers to the microorganism’s ability to adapt and survive antimicrobials (91). The public health consequences of resistance include failure of treatment, increased severity and duration of infections, hospitalization, and mortality (93). Antibiotics that are authorized for use in aquaculture include oxytetracycline, florfenicol, chorionic gonadotropin, formalin solutions, tricaine methanesulfate, sulfadimethoxine/ormetropin, and hydrogen peroxide (71).

The concern about antibiotic-resistant pathogens has been spotlighted by an increased prevalence of antimicrobial-resistant Salmonella in shrimp and other claims that ready-to-eat shrimp is an international vehicle of antibiotic-resistant bacteria (35). Both the European Food Safety Authority and the National Antimicrobial Resistance Monitoring System have reported on resistant and multiresistant Salmonella isolates (91). A Salmonella strain resistant to extended-spectrum beta-lactamase has been recognized worldwide (93). Furthermore, a study of antibiotic use in shrimp farming in Thailand revealed that the use of antibiotics among farmers in that area could result in a severe risk of development of antibiotic-resistant bacterial strains (92). Of particular concern in this study was the prophylactic use of antibiotics at subtherapeutic levels. The study claimed that 74% of the farmers used antibiotics in farm management, and a minimum of 13 antibiotics were used. Additionally, the farmers either used higher doses or what they considered more potent antibiotics for treatment rather than prevention. It was discovered that many of the farmers studied did not have enough information on the efficient use of the antibiotics. A main cause of concern was the farmers’ widespread use of fluoroquinolones, which are important due to their treatment of a broad range of human pathogens (92).

CAUSES OF SEAFOOD RISKS

Food safety concerns among consumers have been growing over time. A survey conducted by the International Food Information Council Foundation in 2008 asked consumers the following question: “To what extent, if at all, do you feel confident in the safety of the U.S. food supply?” Over 50% of the respondents felt confident about the safety of the U.S. food supply (n = 1,000). Food safety practices do not always match confidence. This was evident when the same survey asked the following question: “Which of the following actions do you perform regularly when cooking, preparing, and consuming food products? 1) Wash my hands with soap and water, 2) Cook to required temperature (such as 165 degrees F for poultry), 3) Use different cutting boards for each product (such as raw meat or poultry or produce), 4) Use a food thermometer to check the doneness of meat and poultry items.” The survey revealed that most consumers washed their hands before cooking (79%) and cooked food to the proper temperature (68%). However, consumers did not use different cutting boards for each food product (71%) or use a thermometer to check temperature (29%). It is unclear how the consumers determined if they had cooked the food product to the proper temperature if they had not used a thermometer. Furthermore, the survey found that most consumers felt that the science-based information related to food and health is confusing and conflicting (94).

In 1996 Buzby and Ready (95) reported on >1,000 respondents to a national survey about where they obtained their food safety information, whether they trusted this information, and their major concerns about food safety. Thirty seven percent obtained their information from newspapers and magazines, and only 16.5% from government publications. Over 40% of the survey respondents did not trust the accuracy of food safety information in any form, including government publications and food labeling.

The Cooperative Extension System in several states has included food safety education and a food behavior checklist in their Food Stamp Nutrition Education Program. Texas Agriculture Extension completed a behavior checklist phone survey with 459 participants. The self-reported behavior survey was used to identify changes in the amount of time food was left out at room temperature and hand washing for 20 seconds before handling food (96). The University of California Cooperative Extension’s Food Stamp Nutrition Education Program reported that participants did improve safe food-handling practices after participating in the “Be Food Safe” curriculum with 1,900 people in 19 counties (97).

Raw or Minimally Processed Fish and Seafood

During the past several decades, researchers have continuously emphasized foodborne infection cases in humans which were caused by consuming contaminated fresh, raw fish and seafood. Vibrio spp. have been identified as the most significant cause of foodborne hospitalizations that can lead to death from eating raw seafood. The magnitude of the risk increases when food preparation and consumption trends do not change regarding eating raw or undercooked seafood.

Ready-to-Eat Fish and Seafood

Ready-to-eat seafood items are potentially high-risk foods, and regulatory agencies in the United States have adopted a zero-tolerance policy toward contamination of these products with L. monocytogenes, which can grow easily on the surface of ready-to-eat food products. The salt content, pH, addition of less preservative, and water activity of smoked fish permits the growth of undesirable microorganisms on the surface of this product. A major concern about smoked fish products is L. monocytogenes and Salmonella spp. (98). The highest incidence of L. monocytogenes is associated with cold-smoked fish rather than hot-smoked fish because this pathogen does not survive the hot-smoke process (98). Contamination of smoked fish with L. monocytogenes ranges from 17.9 to 22.3% (99). Studies have shown that cold-smoked salmon is a good substrate for L. monocytogenes, which grows well at refrigerated temperatures on the surface of this product even under vacuum conditions (100). Salmonella spp. have been associated with smoked fish outbreaks (10). The incidence of Salmonella in smoked fish is 3.9%, and Salmonella Newport and Salmonella Anatum are the most prominent serotypes isolated from smoked fish in the United States (98). Reducing the risk of ready-to-eat fish and seafood can be achieved through sanitation practices and HACCP plans in the processing plants.

Fully Cooked Fish and Seafood

The freshness and safety of fish and seafood vary depending on many factors such as contamination during farming, harvesting, and handling and other postharvest activities. Consumers can store fresh raw fish and seafood for days at refrigerated temperatures ranging from 0.5 to 4.5°C. However, at this temperature some pathogenic bacteria such as L. monocytogenes have the potential to multiply. Heat treatment such as proper cooking has an important role in the safety and sensory acceptance of fish and seafood. The definition of cooking is as follows: “The application of heat to a food to modify raw product properties in order to meet sensory expectations of consumers and to reduce its microbial load, which improves its safety and may extend its shelf life” (101). For this definition, it is important to determine consumer acceptance of cooked fish and seafood, which influences consumers’ willingness to employ proper cooking methods such as using a thermometer during cooking to monitor the internal temperature of products.

However, cooking does not eliminate certain hazards such as heat-stable natural or microbial toxins and biogenic amines (e.g., histamine) if they are already present. Such hazards are generally controlled through effective use of Good Manufacturing Practices (GMPs) and HACCP plans. The various cooking methods for fish and seafood include baking en papillote (in a folded pouch) for 10 minutes to reach an internal temperature of 400 to 450°F, barbequing, deep-fat-frying at an oil temperature of 375°F for 3 to 5 minutes, grilling, broiling, microwaving, oven frying at 500 to 550°F, pan frying, sautéing at 375°F, planking at 400°F for 10 minutes, smoking at 245°F for 30 minutes in 2.5 to 3.5% NaCl, steaming 1 to 2 inches above water, and stir frying at 375°F.

A number of foodborne outbreaks occur due to improper cooking of food by consumers. Inadequate cooking and storage of food is considered to be the main cause of foodborne infection (102). It has been suggested that domestic household conditions and inadequate cooking account for 11% and inappropriate storage for up to 50% of outbreaks. This leaves room for extensive research in food safety for developing guidelines at the consumer or domestic household level that will aid in reducing the number of outbreaks. There clearly is a need for consumer-friendly guidelines to ensure the maximum possible food safety.

Thermal resistance in microorganisms can vary from one genus to other and also between species. Chintagari (103) inoculated three Vibrio spp., Salmonella spp., and Listeria spp. on the surface of shrimp and then stored the samples at 3°C. On days 0, 1, and 2 the shrimp samples were placed in a boiling water bath and were removed at different internal temperatures. Vibrio spp. were the least resistant to heat, with bacterial counts reaching nondetectable levels at 55°C (Fig. 2). Salmonella reached nondetectable levels on shrimp at 75°C (Fig. 3), and Listeria spp. showed the highest resistance, reaching nondetectable levels at 85°C (Fig. 4).

FIGURE 2.

Thermal resistance of V. vulnificus, V. parahaemolyticus, and V. cholerae O1 at different internal temperatures in shrimp when subjected to boiling. UC, Uncooked shrimp sample. Data presented in the bar diagram are the mean of three different experiments, and the bars with different letters are significantly different from each other (P < 0.05).

FIGURE 3.

Thermal resistance of Salmonella enterica serovars Enteritidis (S. enteritidis above), Infantis (S. infantis above), and Typhimurium (S. Typhimurium above) at different internal temperatures in shrimp when subjected to boiling. UC, Uncooked shrimp sample. Data presented in the bar diagram are the mean of three different experiments, and the bars with different letters are significantly different from each other (P < 0.05).

FIGURE 4.

Thermal resistance of Listeria welshimeri, Listeria monocytogenes, and Listeria innocua at different internal temperatures in shrimp when subjected to boiling. UC, Uncooked shrimp sample. Data presented in the bar diagram are the mean of three different experiments, and the bars with different letters are significantly different from each other (P < 0.05).

Thermal resistance can also be affected by factors such as the conditions under which foods contaminated with pathogens are stored. Consumers generally store fish and seafood at refrigerated temperatures for several days before using. This could promote biofilm formation and increase the heat resistance of some foodborne pathogens. Comparatively high resistance of V. cholerae O1 has been linked to its ability to form colonies on the shells of shrimps. Several studies have demonstrated that once V. cholerae O1 has attached to chitin particles or crustacean external surfaces, the microorganism is able to initiate a process of colonization (51, 104). This process can be associated with increased resistance to various stresses such as temperature but also to those caused by chemical disinfectants (105), low temperatures (106), and low pH levels (104). Chintagari (103) found that three species of Vibrio were more resistant to heat treatment when surface-inoculated shrimp were stored at refrigerated temperatures before boiling (Fig. 2). Shultz et al. (107) conducted a similar kind of experiment with cockles and concluded that cockles should be cooked until the slowest-heating cockles reach 71°C, for 1 minute. The difference in temperature requirements for cockles and shrimp may be due to the differences in sizes and composition.

A popular method of cooking shrimp is by boiling. Consumers often boil shrimp until they float to the surface of the water and change to a red color. Edwards et al. (108) found that boiling shrimp until they float reduces Listeria and Salmonella spp. to nondetectable levels, but color change was not a good indication of the reduction of foodborne pathogens due to color variation. Baking and broiling are two popular methods of cooking catfish. Consumers often follow the 10-minute rule as a general rule of thumb when cooking catfish. This rule says to measure the dressed fish, fillet, or steak at its thickest part and then allow 10 minutes of cooking time per inch of thickness. For fish that are less than 1 inch thick, the cooking time is shortened proportionally. Additionally, a common method used by consumers to determine doneness when cooking is to observe the color change of the cooked product. For example, when boiling crab, the color change from gray to red is associated with it being thoroughly cooked. For a serving size of crab (4 crabs), to reduce foodborne pathogens to nondetectable levels, it is recommended to boil the crabs for 10 minutes and cool 5 additional minutes for an internal temperature of at least 85°C and a total cooking time of 15 minutes; steam four crabs for 15 minutes and cool 5 additional minutes to reach an internal temperature of at least 85°C, with a total cooking time of 20 minutes (109) (Fig. 5 and Fig. 6). For catfish, consumers look for the meat to turn opaque when cooked. This color change is used for safety evaluation and is also associated with sensory acceptance. Further scientific research needs to be done to verify that color change is a good indication of safety in fish and seafood products.

FIGURE 5.

Graph of below-detection-limit/nondetectable level reached for boiling a serving size of four crabs at each time point and the optimum temperature each achieved for L. monocytogenes (Lm) and V. parahaemolyticus (Vp).

FIGURE 6.

Graph of below-detection-limit/nondetectable level reached for steaming a serving size of four crabs at each time point and the optimum temperature each achieved for L. monocytogenes (Lm) and V. parahaemolyticus (Vp).

CONCLUSION

Risks associated with fish and seafood will continue to be a problem unless consumers’ attitudes change toward eating these products raw. Most consumers know of the risks associated with eating raw oysters but continue to eat them. With the increase in the demand for fish and seafood, aquaculture production is increasing. Aquaculture production of fish and seafood could lead to new risks that will need to be addressed in the future to control foodborne pathogens.