We have described the epidemiology of infections associated with seafood consumption in the United States from 1973 to 2006. Seafood—finfish, marine mammals, mollusks, and crustaceans—is an important cause of food-borne illness and outbreaks in the United States. Our analysis identified specific seafood vehicles frequently associated with illness. This information can help to guide future prevention efforts. Seafood-associated outbreaks of infection were most often attributed to consumption of molluscan shellfish, particularly raw oysters, and most often caused Vibrio illnesses and norovirus infections. Over the study period, both the absolute number of outbreaks and the proportion of outbreaks caused by molluscan shellfish increased. Botulism cases associated with fish were also reported frequently, although these outbreaks were reported almost exclusively from Alaska. Etiologies and implicated seafood commodities changed over time during the study period. The cause of these changes is likely multifactorial: enhanced food-borne outbreak surveillance began in the late 1990s; laboratory diagnostic capacities have improved, particularly for norovirus but also for other pathogens, resulting in better detection of outbreaks; control efforts, especially in shellfish sanitation, have evolved; and changes in environmental factors may favor the occurrence of some pathogens.
Our analysis of surveillance data is subject to several limitations. The true burden of illnesses associated with seafood consumption is probably much greater than what we report. Our understanding of foods and pathogens responsible for illness is largely derived from information gained from outbreak investigations. However, many outbreaks likely go unrecognized and uninvestigated. Moreover, the Food-Borne Disease Outbreak Surveillance System is a passive system that relies on voluntary reporting, which may lead to further underestimation of the actual number of outbreaks and illnesses that occur. Outbreak reporting may not be uniform across states, which may be due in part to whether states have dedicated food-borne disease epidemiologists. Also, outbreaks comprise only a small proportion of all cases of food-borne illness. No information is available on seafood-borne transmission in sporadic cases of infection other than Vibrio illnesses. Enhanced surveillance for food-borne outbreaks began in 1998. As a result, an abrupt increase in reported outbreaks occurred, which should not be interpreted as a true increase in the number of outbreaks. Also, improved laboratory methods and surveillance increased the ability to detect and investigate outbreaks during the study period. For example, subtype-based laboratory surveillance has improved the ability to detect outbreaks of infections associated with seafood items that are widely distributed, as in multistate outbreaks, and with pathogens with long incubation periods, such as hepatitis A virus. Other laboratory methods that evolved during the past decade include testing for the presence of norovirus by PCR and increased use of appropriate selective media to detect Vibrio organisms in stool.
Contamination of seafood can occur before harvest or at any point from harvest through final preparation. The types and numbers of pathogens present in seafood are affected by the environment from which the seafood was harvested and by sanitation during subsequent handling, processing, storage, transportation, and final preparation. Survival of food-borne pathogens is more likely to occur in foods that are consumed undercooked or raw and in those that experience time and temperature abuse, such as may occur during delays between harvest and refrigeration.
Control strategies to prevent seafood-associated illnesses include monitoring harvest waters, identification and implementation of process controls, and consumer education. Federal agencies, state governments, and private industry all bear responsibility for reducing seafood-associated infections. The FDA plays an important role in establishing guidelines and providing oversight to ensure safer fish and fishery products. Prevention strategies developed by the FDA and the seafood industry to minimize the risk of microbial contamination and decrease the risk of seafood-associated infection include good manufacturing practices, which address sanitation conditions and practices, and a seafood hazard analysis and critical control point (HACCP) program. The purpose of a HACCP is to identify sources and points in processes at which the risk of contamination is high, from harvest to consumption, so that processes to decrease these risks can be implemented and monitored. During the mid-1990s, the FDA issued regulations for the seafood industry, relying on HACCP-based principles. Every seafood harvester and processor is now required to use a HACCP-based system. Examples of HACCP-based principles include candling of fish to detect parasites, a low-acid canning program for canned tuna and salmon to prevent botulism, and rapid chilling of fish after death to prevent scombrotoxin formation (24
Shellfish regulation has a distinctive history. Control strategies in addition to those mentioned above and specifically aimed at promoting the safety of molluscan shellfish are implemented through the National Shellfish Sanitation Program (NSSP). The NSSP guidelines are uniform shellfish safety standards that regulate the harvesting, processing, and shipping of shellfish for interstate commerce. The NSSP was established in response to large outbreaks of typhoid fever associated with contaminated mollusks that occurred in the 1920s. Through the ensuing decades, NSSP guidelines have evolved to address public health problems. Since 1985, NSSP guidelines have been established through the Interstate Shellfish Sanitation Conference (ISSC), which is a cooperative organization with representation from the FDA and other federal agencies, state health departments and shellfish authorities, and private industry. Commercial shellfish harvesting is regulated by states in accordance with NSSP guidelines. The standards for harvesting shellfish are established by state rules and regulations, and harvesting occurs in designated approved areas.
Under the NSSP, standards for harvesting shellfish involve monitoring of environmental factors, including coliform counts, marine biotoxins, levels of V. parahaemolyticus
in sampled oysters, water salinity levels, and ambient and water temperatures. Fecal coliforms are used as an indicator of bacterial contamination and to classify shellfish harvesting areas as safe or unsafe. While they have been useful as an indicator of the presence of feces-related bacteria in harvest beds, they are less reliable for naturally occurring pathogens (e.g., Vibrio
species) and for enteric viruses. Our surveillance data suggest that the greatest current seafood safety risks involve bivalve mollusks contaminated with naturally occurring pathogens. Therefore, prevention of initial contamination at or before the time of harvest is important, and environmental monitoring is critical. Investigation of seafood-associated outbreaks and traceback information on shellfish implicated in sporadic cases of Vibrio
illness have indicated that illness is often associated with consumption of shellfish harvested from warmer waters (18
). The recent investigation of an outbreak of V. parahaemolyticus
infections associated with Alaskan oysters underscores the need to examine the emerging health risks posed by changing environmental factors, such as rising water temperatures (42
). In an effort to further reduce the risk of shellfish-associated Vibrio
illnesses, the ISSC has established additional control measures based on environmental conditions such as air and water temperature (26
Additional control measures exist to prevent contamination during postharvest handling, processing, and distribution of shellfish. Bacterial proliferation and toxin formation can occur if contaminated seafood is not maintained at appropriate temperatures; therefore, minimizing the time between harvest and refrigeration is critical, especially during summer months (27
). The FDA and ISSC have established NSSP guidelines for storage times and temperatures for specific seafood products. However, the potential benefits of implementing strict requirements to shorten the time between shellfish harvest and refrigeration are countered by concerns for the potential economic burden to the shellfish industry. A unique control strategy for molluscan shellfish is the labeling of all containers containing bivalve mollusks with tags containing information about the harvest site and date. These tags are maintained by harvesters, dealers, shippers, and restaurants for at least 90 days after sale. This information on the location of harvesting facilitates traceback to harvest waters of lots associated with illness. It is important that industry-implemented postharvest processing methods for seafood, particularly oysters, are available to reduce microbial hazards. Established and well-accepted methods include individually quick-freezing oysters, pasteurization, irradiation, and high hydrostatic pressure, and new methods continue to be developed. These processing techniques reduce microorganisms to nondetectable levels and reduce the risk of illness (27
Consumers should be aware of the potential health risks associated with eating seafood. Seafood-borne infections can be prevented by cooking seafood thoroughly, storing foods properly, and avoiding cross-contamination after cooking. However, some seafood is commonly consumed raw or minimally cooked. Persons with underlying medical conditions such as liver disease, diabetes, or immunosuppressing conditions are at higher risk of acquiring severe infection and should be especially careful. Educational strategies have focused particularly on those persons. Messages warning consumers of the potential risks of infection associated with raw oyster consumption are posted in restaurants in states where illnesses caused by Vibrio vulnificus
are prevalent; however, cases continue to occur, suggesting that these educational strategies by themselves may not prevent all cases (47
) and that additional regulatory measures, as well as more effective consumer education, may be needed to further reduce the incidence of illness. For clinicians and laboratorians, prompt recognition of infection in patients who seek medical attention for illness after eating raw or undercooked seafood is important for appropriate testing (e.g., use of TCBS agar for culture of stool samples) and early treatment, as necessary. Rapid reporting of these cases to public health authorities is critical to identify both contaminated seafood and risky harvest areas in order to implement timely control measures.
Seafood is part of a healthful diet, but seafood consumption is not risk-free. Multiple outbreaks of seafood-associated infections, especially mollusk-associated outbreaks of Vibrio infections, continue to occur every year in the United States, suggesting that existing control strategies have not been optimally effective. Prevention of seafood-associated infections requires an understanding not only of the etiologic agents and seafood commodities associated with illness but also of the mechanisms of contamination that are amenable to control. Defining these problem areas, which relies on surveillance of seafood-associated infections through outbreak and case reporting, can lead to targeted research and help to guide control efforts. Coordinated efforts are necessary to further reduce the risk of seafood-associated illnesses. Continued surveillance will be important to assess the effectiveness of current and future prevention strategies.