Advanced Articles (September 25, 1997) [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Consumer Concerns: Motivating to Action Christine M. Bruhn University of California, Davis, California, USA ------------------------------------------------------------------------ Microbiologic safety is consumers' most frequently volunteered food safety concern. An increase in the level of concern in recent years suggests that consumers are more receptive to educational information. However, changing lifestyles have lessened the awareness of foodborne illness, especially among younger consumers. Failure to fully recognize the symptoms or sources of foodborne disease prevents consumers from taking corrective action. Consumer education messages should include the ubiquity of microorganisms, a comprehensive description of foodborne illnesses, and prevention strategies. Product labels should contain food-handling information and warnings for special populations, and foods processed by newer safety-enhancing technologies should be more widely available. Knowledge of the consequences of unsafe practices can enhance motivation and adherence to safety guidelines. When consumers mishandle food during preparation, the health community, food industry, regulators, and the media are ultimately responsible. Whether inappropriate temperature control, poor hygiene, or another factor, the error occurs because consumers have not been informed about how to handle food and protect themselves. The food safety message has not been delivered effectively. Consumer Knowledge and Concern Consumers are receptive to information about microbiologic hazards. Nationwide surveys by the Food Marketing Institute indicate that more people volunteer concerns about microbiologic hazards than about any other potential food safety issue. From 1992 to 1996, volunteered concern about microbiologic safety increased from 36% to 49% (1). Specifically, concern about contamination by bacteria or other microorganisms was 77%, more than concern about pesticide residues (66%), product tampering (66%), antibiotic residues (42%), or any other food safety risk. Food-Handling Practices Although many consumers recognize the potential seriousness of foodborne bacteria, they lack information on safe handling and storage of food products (2). Williamson et al. (3) found that consumers under 35 years of age knew less about food safety terms and concepts than those over 35. Specific safe food handling was not practiced by 15% to 30% of survey respondents. For example, consumers did not cool cooked food rapidly, with 29% indicating they would let roasted chicken cool completely before refrigerating. Only 32% indicated they would use small, shallow containers to refrigerate leftovers. Consumers did not know that failure to refrigerate may jeopardize safety, with 18% not concerned or uncertain about the safety of cooked meat and 14% not concerned about poultry left unrefrigerated for more than 4 hours. The need for sanitation was not recognized, with only 54% indicating they would wash a cutting board with soap and water between cutting raw meat and chopping vegetables. Food safety experts have identified the most common food-handling mistakes made by consumers at home. These mistakes include serving contaminated raw food, cooking or heating food inadequately, obtaining food from unsafe sources, cooling food inadequately, allowing 12 hours or more between preparation and eating, and having a colonized person handle implicated food or practice poor hygiene (4). The same factors were identified in mishandling associated with specific pathogens (5). Changing Lifestyles Many factors have contributed to consumers' lack of familiarity with safe food handling and increased foodborne illnesses. Increased participation in the paid labor force has lessened the exposure of young people to food-handling practices in the home; few schools offer or require food preparation classes; and partially prepared foods may have different, less familiar handling requirements (2,6). People eat out more frequently today, thereby increasing their exposure to the food service industry, noted for high turnover rates and minimal job training in personal hygiene (7). Furthermore, the population is shifting, with an increased percentage of persons at higher risk for foodborne illness because of age or health status (8,9). Additionally, some food safety recommendations related to temperature and acidity do not eliminate risks from some pathogens (2). Nature and Source of Foodborne Illness Consumer perceptions and behavior related to foodborne illness changed little between 1988 and 1993 (10). Consumers misperceived the nature of foodborne illness and the most likely pathogen source. Consumer belief about the type of food responsible for foodborne illness--meat, poultry, seafood, eggs--was consistent with expert opinions; however, consumers believed that foodborne illness was generally mild, without fever, and occurred within a day of eating contaminated food. Infections caused by Salmonella and Campylobacter, the most common foodborne illnesses in the United States (11), are not consistent with the symptoms consumers described, because these organisms have longer latency and cause fever. Most consumers believed that their foodborne illness was caused by food prepared somewhere other than the home. Williamson (3) found that about one-third of consumers thought food safety problems most likely occurred at food manufacturing facilities, and one-third blamed unsafe restaurant practices. Only 16% thought mishandling was most likely to occur in the home. Fein et al. (10) found that 65% of consumers attributed foodborne illness to food prepared at a restaurant, 17% to mishandling at the supermarket, and 17% to mishandling at home. In contrast, food safety experts believe sporadic cases and small outbreaks in the home are far more common than recognized outbreaks (2). Failure to recognize the home as a likely source of foodborne illness is not unexpected because illness traced to a food establishment affects many people and may receive widespread publicity (12). Illness that occurs at home is rarely reported unless severe (2). If consumers misperceive the nature and origin of foodborne illness, they underestimate the frequency of serious consequences and are less motivated to change. Schafer et al. (13) found that motivation for proper food handling requires viewing the mishandling of food as a direct threat to one's health. The failure to associate mishandling of food in the home with foodborne illness interferes with foodborne disease education efforts (10). Ubiquity of Organisms Consumers do not seem to be aware of the ubiquity of microorganisms in the environment. During foodborne disease outbreaks, press accounts focus on fecal contamination of food. Government standards classify natural microorganisms as contaminants, which suggests that microorganisms are only present as a result of mishandling. In contrast, Hazard Analysis and Critical Control Points (HACCP) programs recognize and attempt to control potential dangers related to pathogenic microorganisms. When consumers in a national sampling were asked on whom they rely for product safety, the percentage responding "myself as an individual" decreased from 48% in 1989 to 25% in 1996 (1). As self-reliance decreased, consumer reliance on food manufacturers and supermarkets increased. This may be a response to the message that if raw food contains microorganisms, it is contaminated. It suggests some consumers are shifting the responsibility for safe food to manufacturers and retailers. Consumers may not realize they can introduce pathogens during food handling. In 1990, the Food Marketing Institute asked consumers what steps they took at home to ensure the safety of food (14). Respondents volunteered refrigeration (58%), proper storage (35%), checking expiration dates (26%), washing and cleaning the food (25%), cooking properly (22%), and wrapping food properly (20%). No one volunteered washing hands or preventing cross-contamination. Labeling Products must contain safety labels instructing consumers how to handle food. In 1989, the National Advisory Committee on Microbiological Criteria for Foods recommended a mandatory uniform logo for perishable refrigerated foods, uniform labeling for frozen food, "Use by" dates, and time/temperature indicators wherever possible (15). Although products are currently labeled when they require refrigeration, the label is ineffective because the warning is difficult to find or read. As the proportion of older people increases, print must be larger. Labels should also display symbols to further enhance the effectiveness of the message. Safe-handling labels on meat products appear to have made a difference. The Food Marketing Institute (1) found that 60% of survey respondents had seen the labels. Of those aware of the labels, 65% said the labels increased their awareness of safety, and 43% said they changed their behavior as a result of the information. The most common volunteered change was washing the counter and utensils after contact with meat (approximately 40%), followed by washing hands more frequently (approximately 20%) and cooking to the proper temperature (approximately 20%). Labels do not consistently contain needed information. When foodborne illness was related to consumption of unpasteurized apple juice, consumers were not able to determine from the label which products were pasteurized. Many major manufacturers do not indicate whether their fresh juice product is pasteurized. Consumers are not advised about potential risks for special populations. Raw milk sold in California must contain a warning statement, but other states may not have this requirement. Because of inconsistencies in labeling, unpasteurized juice products may be given to infants. Also, products that contain honey do not include a warning about potential risk for infant botulism. Processing Technology Consumers do not realize that pathogens can survive minimal processing, as evidenced by a recent Escherichia coli outbreak associated with fresh apple juice, which demonstrated that processors also may not recognize potential risks. A fresh apple juice manufacturer in northern California claimed its product was safe because the juice was squeezed in small batches and frozen immediately. Freezing is not effective against E. coli O157:H7, but other methods are protective. Several methods have been developed to reduce pathogens and increase the safety of foods. Once these methods are verified as effective and safe, the food industry should be free to use them, and consumers should have the opportunity to select safer foods. In some cases, the regulatory approval process appears to hinder rather than facilitate the safer handling of food. Food irradiation, exposing food to high levels of electromagnetic energy for specific purposes, has been approved for selected uses. A petition before the Food and Drug Administration to permit irradiation of meat and other muscle foods appears to have satisfied safety concerns, but approval has not yet been granted. The requirement to seek approval for each application of irradiation prevents rapid response in cases of foodborne outbreaks. Although this regulatory procedure may have been reasonable when irradiation was first introduced, it warrants a fresh look in view of the wealth of data now available on the safety and wholesomeness of food irradiation (16). Attitude surveys and marketing experience consistently demonstrate that consumers will purchase irradiated food (17). National surveys indicate consumer concern about irradiation was lower than other food-related concerns. When specifically asked what they considered a serious health hazard, 29% identified irradiation, 77% identified bacteria, and 66% identified pesticides (1). The percentage of consumers concerned about irradiation has decreased significantly over time. In the late 1980s, 42% to 43% classified irradiation as a serious concern, decreasing to 29% in 1996. A relative ranking of food processing methods surveyed by the Gallup Organization found that irradiation, food preservatives, and chlorination generated similar concern (18). In a nationwide Food Marketing Institute survey, 69% of consumers indicated they were very or somewhat likely to purchase products irradiated to kill bacteria or other microorganisms (1). Surveys completed in several areas of the country indicate 60% to 70% of consumers would prefer irradiated food (17). In one study, information about irradiation increased interest in purchasing to 90%, and education plus food samples increased purchase intent to 99%. Consumers have purchased irradiated food in select locations across the United States since 1992 (17). Fruits from the Mainland and Hawaii have sold well in the Midwest and California (L. Wong, pers. comm.). Irradiated chicken gained over 60% of market share when priced 10% lower than nonirradiated chicken and 47% when priced the same (J.A. Fox, pers. comm.). Irradiated food is not widely available. Special interest groups threaten companies that exchange information about irradiation processing. Consumers, however, appear to prefer irradiated foods when the benefits of these foods are endorsed by health professionals. Food manufacturers and retailers should offer consumers the choice of safety-enhanced, energy-pasteurized irradiated food. Communicating with the Public To respond to consumers' need for information, a multifaceted program is needed. The HACCP strategy, which teaches consumers to critically think through the food safety process to determine how foodborne illness could occur, has been effective (19,20). The HACCP approach to home food preservation is logical and highlights key control points (21). Consumers should be informed that microorganisms are ubiquitous in the environment, found on raw products of animal or plant origin. Pathogens may survive minimal processing and preservation treatments. People may introduce pathogens during any stage of food processing or handling, including just prior to consumption. Foodborne illness can range from mild to severe and life-threatening with chronic complications. People have control and can reduce risks. Communicating food safety information to the public effectively is another challenge. Consumers obtain most of their information on food, nutrition, and science from the media; television is cited most frequently, and newspapers and magazines follow (22,23). Brochures enforce messages and serve as useful references, although they are not as widely seen as media stories. Developing messages with the press should be a primary activity of a food safety education program. Consumers judge a message by the credibility of the person conveying it, its appeal to their common sense, and the frequency of the message (24). Media presentations can motivate people to listen and change behavior. Consultants from the USDA hotline say, "We've seen an explosion in media coverage of food safety, and callers want more detailed explanations of things they read and hear" (25). Information on safe food handling must be motivating and memorable. Stories that capture the public's attention are personal. They relate life experiences of people with whom the public can identify. Stories of the consequences of mistakes are memorable. They can be touching, humorous, or grotesque. It is easy to visualize and remember the infected bakery worker who made 5,000 people ill when he mixed a vat of buttercream frosting with his bare hands and arms despite bouts with diarrhea (26). Stories can be heartrending, as in the experiences of a family who lost a child to E. coli O157:H7 infection. It is difficult to document the effectiveness of vivid accounts of doing things right or wrong. However, when Washington state carried extensive coverage linking the outbreak to undercooked hamburgers, 13% of the men said they ate undercooked hamburger, compared with 38% in Colorado (25). Conclusions Consumer concerns about foodborne illness can motivate change in regulatory and industry use of technology, product labeling, and consumer education. New Technologies The food industry has both a right and a responsibility to use safe and effective technology to enhance the safety of the food supply. Regulatory authorities should expediently evaluate and facilitate new technologies, such as food irradiation, laser light treatment, and high-pressure processing, which enhance food safety. Health professionals, the food industry, and regulators should challenge special interest groups that distort information and strive to limit consumer choice. Improved Labeling Processed and packaged food should bear labels that clearly indicate how food should be handled. Labels should include warnings about special risks to select populations. Benefits from special processing that can reduce microbes should also be encouraged. Consumer Education Consumers need to appreciate the seriousness of foodborne diseases. They must learn to recognize unsafe food-handling practices, the latency period for some microbes, and the symptoms of foodborne disease. They need to understand how to protect themselves through kitchen and personal hygiene, including thoroughness and frequency of hand washing, temperature control, and safe food choices such as foods processed by heat or energy pasteurization. Young people should be reached through age-specific school curricula, such as personal hygiene and special "living skills" units that address food safety and diet. Food industry and health educators should work with the media to develop interesting and timely messages to increase consumer knowledge about safe food handling. Messages must be consistent, science-based, frequent, and personalized. Address for correspondence: Christine M. Bruhn, Consumer Behavior, University of California, Center for Consumer Research, University of California, Davis, CA 95616-8598; fax: 916-752-3975; e-mail: cmbruhn@udavis.edu. References 1. Abt Associates Inc. Trends in the United States, consumer attitude and the supermarket 1996. Washington (DC): Food Marketing Institute; 1996. 2. Institute of Food Technologists' Expert Panel on Food Safety and Nutrition. Scientific status summary, foodborne illness: role of home food-handling practices. Food Technology 1995;49:119-31. 3. Williamson DM, Gravani RB, Lawless HT. Correlating food safety knowledge with home food-preparation practices. Food Technology 1992;46:94-100. 4. Bryan F. Risks associated with vehicles of foodborne pathogens and processes that lead to outbreaks of foodborne diseases. Journal of Food Protection 1988;51:663-73. 5. Bean NH, Griffin PM. Foodborne disease outbreaks in the United States, 1973-1987; pathogens, vehicles, and trends. Journal of Food Protection 1990;53:804-17. 6. Dumagan JC, Hackett JW. Almost half of the food budget is spent eating out. Food Review 1995;18:37. 7. Martin R. Foodborne disease threatens industry. National Restaurant News 1990;24:27,30. 8. Doyle MP. Food safety in the 21st century. Dairy Food Environ Sanit 1993;13:383. 9. Food Institute. Population trends 1996-2050. Fair Lawn (NJ): The Institute; 1996. p. 31. 10. Fein SB, Jordan CT, Levy AS. Foodborne illness: perceptions, experience, and preventive behaviors in the United States. Journal of Food Protection 1995;58:1405-11. 11. Tauxe RV. Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In: Nachamkin J, Blaser MJ, Tompkins LS, editors. Campylobacter jejuni: current status and future trends. Washington (DC): American Society for Microbiology; 1992. p. 9-19. 12. Ollinger-Snyder P, Matthews ME. Food safety issues: press reports heighten consumer awareness of microbiological safety. Dairy, Food and Environmental Sanitation 1994;14:580-9. 13. Schafer RB, Schafer E, Bultena GL, Hoiberg EO. Food safety: an application of the health belief model. Journal of Nutritional Education 1993;25:17-24. 14. Food Marketing Institute. Opinion research, trends 90, consumer attitudes & and the supermarket 1990. Washington (DC): The Institute; 1990. 15. Rhodes ME. Educating professionals and consumers about extended-shelf-life refrigerated foods. Food Technology 1991;45:162-4. 16. Diehl JF. Safety of irradiated foods. New York: Marcel Dekker, Inc.; 1995. 17. Bruhn CM. Consumer attitudes and market response to irradiated food. Journal of Food Protection 1995;58:175-81. 18. The Gallup Organization. Irradiation: consumers' attitudes. Princeton (NJ): Prepared for the American Meat Institute; 1993. 19. Hoban T. Consumer awareness and acceptance of bovine somatotropin. Survey conducted for the Grocery Manufacturers of America; 1994. 20. Hoban T, Kendall PA. Consumer attitudes about the use of biotechnology in agriculture and food production. Raleigh (NC): North Carolina State University; 1992. 21. Bruhn CM, Peterson S, Phillips P, Sakovich N. Consumer response to information on integrated pest management. Journal of Food Safety 1992;12:315-26. 22. United States Department of Agriculture. The Food Safety Educator 1996;1:3. 23. Beware the Norwalk virus. Food Talk (Winter) 1989;4. 24. Reicks J, Bosch A, Herman M, Krinke UB. Effectiveness of a food safety teaching strategy promoting critical thinking. Journal of Nutritional Education 1994;26:97-100. 25. Medeiros LC, George RT, Gruns K, Chandler C, Crusey S, Fittro J, et al. The safe food handling for occasional quantity cooks curriculum. Journal of Nutritional Education 1996;28:39-42. 26. United States Department of Agriculture, Food Safety and Inspection Service. A margin of safety: the HACCP approach to food safety education. Washington (DC): United States Department of Agriculture Information and Legislative Affairs; 1990. ------------------------------------------------------------------------ Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Public, Animal, and Environmental Health Implications of Aquaculture E. Spencer Garrett,* Carlos Lima dos Santos,† and Michael L. Jahncke‡ *National Seafood Inspection Laboratory, Pascagoula, Mississippi, USA; †Food and Agriculture Organization of the United Nations, Rome, Italy; ‡Virginia Tech Seafood Research and Extension Center, Hampton, Virginia, USA ------------------------------------------------------------------------ Aquaculture is important to the United States and the world's fishery system. Both import and export markets for aquaculture products will expand and increase as research begins to remove physiologic and other animal husbandry barriers. Overfishing of wild stock will necessitate supplementation and replenishment through aquaculture. The aquaculture industry must have a better understanding of the impact of the "shrouded" public and animal health issues: technology ignorance, abuse, and neglect. Cross-pollination and cross-training of public health and aquaculture personnel in the effect of public health, animal health, and environmental health on aquaculture are also needed. Future aquaculture development programs require an integrated Gestalt public health approach to ensure that aquaculture does not cause unacceptable risks to public or environmental health and negate the potential economic and nutritional benefits of aquaculture. U.S. Fisheries System Coastal estuaries serve as a breeding ground and provide habitats for more than 75% of commercial landings and 80% to 90% of the recreational catch of fish and shellfish. From these habitats, hundreds of species of seafood are produced. Aquacultured species now contribute up to 15% of the U.S. supply (1,2). Wild species are harvested by 17,000,000 recreational anglers and nearly 300,000 commercial harvesters. Commercial harvesters deploy 93,000 vessels, while recreational fishermen have millions of recreational fishing boats. Nearly 5,000 domestic plants are located in every state throughout the United States, not just in the coastal areas (3). Current per capita consumption of commercially harvested species averages 15 pounds; it is estimated that per capita consumption of recreationally harvested seafood approaches an additional 3 to 4 pounds per person (4). The seafood business community--in the United States and in other industrialized countries--cannot rely solely on domestically produced stock. For a number of years, more than half of U.S. seafood consumption has relied on imported stock. Currently, the United States imports more than 50% of the consumed seafood, which originates in 172 countries around the world (3). This trend toward economic reliance on imported stock has steadily increased over the past 10 years so that now the United States is the world's second largest importer of seafood. The principal seafood imports are tuna, shrimp, salmon, lobster, and groundfish (3). It is difficult to determine where imported fish was harvested. For example, the United States imports salmon from Switzerland and Panama, although neither Switzerland nor Panama is noted for vast salmon resources. U.S. participation in the international seafood trade is very complex, since in addition to being the world's second largest importer, the United States is also the world's second largest exporter of seafood (3). This dichotomy requires that U.S. marketing and import/export food control inspection strategies be carefully planned. For example, the United States exports seafood to 162 countries, which has come about with the full development of northwest and Alaska fisheries and improved efficiency in processing techniques. Major U.S. exports are salmon, crab, surimi, fish blocks, groundfish, flatfish, shrimp, and lobster (3). Current Aquaculture Status In 1996, U.S. aquaculture production of nearly 227,000 metric tons consisted of baitfish, catfish, salmon, trout, clams, crawfish, mussels, oysters, fresh and saltwater shrimp, and miscellaneous species such as ornamental fish, alligators, algae, aquatic plants, tilapia, and hybrid striped bass. The United States exported principally rainbow trout, Atlantic salmon, tilapia, catfish, freshwater crawfish, and live mussels to 19 countries in Europe, North and South America, and Asia. Freshwater crawfish led the export seafood market at slightly over $8 million, with the other species accounting for less than $1 million each (3). The United States also imports large volumes of aquacultured products, approximately $2.5 billion in cultured products, primarily shrimp and salmon. Imported cultured seafood accounts for most of the current U.S. trade deficit for edible fishery products, which was approximately $3.5 billion in 1995. The Safety of Seafood Most seafood is safe; however, like all foods, it carries some risk. The food safety issues for seafood are highly focused, well-defined, and limited to a very few species. For seafood-borne illnesses (in which the cause was known) reported to the Centers for Disease Control and Prevention, more than 90% of the outbreaks and 75% of the individual cases were associated with ciguatoxin (from a few reef fish species) and scombrotoxin (from tuna, mackerel, bluefish, and a few other species) and the consumption of mollusks (mostly raw) (5-12). Hazards associated with the consumption of all food (including seafood) can be categorized into three areas: product safety; food hygiene (clean vs. dirty plants, wholesome vs. unwholesome products); and mislabeling or economic fraud. Traditionally, the food safety risks of seafood products (aquacultured and wild-caught) have been subcategorized by environment, process, distribution, and consumer-induced risk; the environmental risk category is further subdivided into natural hazards, (e.g., biotoxins) and anthropogenic contaminants (e.g., polychlorinated biphenyls) (13). "Shrouded" Aquaculture Hazards The future of aquaculture is bright; aquaculture products are as safe and wholesome as wild-caught species. However, in addition to the consumer hazards listed above, there are some less obvious "shrouded" public health hazards associated with ignorance, abuse, and neglect of aquaculture technology. Technology Ignorance A common practice in many developing countries is the creation of numerous small fish pond impoundments. However, this approach may have a greater adverse effect on human health than the creation of a single large impoundment (14). Small impoundments greatly increase the overall aggregate shoreline of ponds, causing higher densities of mosquito larvae and cercaria, which can increase the incidence and prevalence of diseases such as lymphatic filariasis and schistosomiasis, respectively. Centralized planning approaches for new freshwater and marine aquaculture sites should include discussions of the potential effect of large or small impoundments on such issues as disease transmission, water supply, irrigation, and power generation (14). Ignorance of the microbial profile of aquaculture products can also affect human health as evidenced by the recent transmission of streptococcal infections from tilapia to humans, which resulted in several meningitis cases in Canadian fish processors (15). A change in marketing strategies to sell live fish in small containers, instead of ice-packs, resulted in human Vibrio infections from live tilapia in Israel in 1996. Such bacteria can be present in other aquacultured and wild-caught species in addition to tilapia. Ignorance of the hazards associated with the use of untreated animal or human waste in aquaculture ponds to increase production also has tremendous human health implications (16). For centuries, food growers have cultured species in waste-water-fed ponds and grown secondary vegetable crops in waste water and sediment material in integrated aquaculture operations. However, the potential for transmission of human pathogens to cultured species and secondary vegetable crops is rarely considered by fishery aquaculturists. For example, of more than 250 presentations at the 1997 World Aquaculture Society meeting held in Seattle, Washington, few referred to the potential human health implications of aquaculture (17). The potential transmission of animal pathogens from exotic aquacultured species to wild-stock species also affects animal health. Recent outbreaks of taura, yellow spot, and white head viruses have occurred in aquaculture shrimp in South Carolina and Texas. Recent studies indicate that native wild white shrimp may also be susceptible to these exotic viruses (18). Technology Abuse Technology abuse includes the willful misuse of therapeutic drugs, chemicals, fertilizers, and natural fishery habitat areas. The widespread use and misuse of antibiotics to control diseases in aquaculture species is worldwide and will probably increase as aquaculturists move towards more intensive animal husbandry— rearing techniques and stocking densities. For example, the illegal use of chloramphenicol in shrimp culture to control diseases may result in violative levels in the harvested product. Similarly, the improper or illegal use of chemicals (e.g., tributyl tin) to control pond pests such as snails can also result in human health hazards. The abuse and misuse of raw chicken manure as pond fertilizer may result in the transmission of Salmonella from manure to the cultured product (16). The destruction of mangrove areas to build aquaculture ponds can have a drastic impact on the survival of wild aquatic species through the degradation of essential fish habitats and nurseries. In Brazil, destruction of mangrove areas for shrimp ponds effected climatic changes to such an extent that the aquaculture operations have been terminated because consequent reduced rainfall resulted in excessive pond salinity (19). Technology Neglect The final "shrouded" hazard associated with aquaculture involves technology neglect, which includes such events as the abandonment of small aquaculture ponds in tropical countries, leading to increased mosquito habitats and concomitant increases in malaria (14). Facility management can be responsible for technology neglect if employees are not trained in the proper use and application of therapeutics and chemicals, for example. Finally, from an animal health perspective, ignorance or willful neglect of the International Council for Explorations of the Sea/European Inland Fisheries Advisory Commission Code of Practice for the Introduction and Transfer of Marine Organisms can result in the escape of exotic species and animal pathogens into the environment with a potential tragic impact on native aquatic species (20). Health Control Considerations Human Health Procedures to help protect humans from aquaculture-associated risks include better education and training of aquaculture personnel on the proper use and storage of therapeutics and chemical compounds. Additional research on new more effective and, we hope, safer, antibiotic and vaccine treatment of aquaculture species is under way. Likewise, certain extralabel use applications for selected antibiotics are under consideration. Streamlined enforcement efforts are being developed to ensure compliance with new food safety regulations and new regulatory control procedures such as Hazard Analysis and Critical Control Points (HACCP) and the application of HACCP principles to animal and environmental control procedures (21,22). The Food and Agriculture Organization and World Health Organization recommend that the HACCP concept be applied to fresh water aquaculture programs to control foodborne digenetic trematode infections in humans. Experiments are being carried out in Asia by a multidisciplinary team of experts in public health, parasitology, aquaculture, fisheries extension, and fish inspection (22). In one study in Vietnam, experimental activities were conducted in two side-by-side fish ponds. In the experimental ponds, fish were cultured in conjunction with HACCP principles, and control pond fish were cultured according to conventional local aquaculture practices (22). Water supply, fish fry, fish feed, and pond conditions in the experimental pond were identified as critical control points. The HACCP principles of hazard analysis, preventative measures, critical limits, monitoring, recordkeeping, and verification procedures relating to the critical control points were applied; study results showed Clonorchis sinensis eggs and fish infected with the parasite metacercaria and the first intermediate host (Melanoides tuberculata) in the experimental ponds (22). Forty-five percent of control pond fish were infected with C. sinensis metacercaria, while white fish from the experimental pond monitored according to HACCP principles were completely free of trematode infection (22). Preliminary results indicate that application of HACCP-based principles to silver carp culture in North Vietnam is an effective way to prevent and control C. sinensis. Similarly, the application of these principles to fresh water aquaculture ponds in Thailand and Laos to control Opisthorchis viverrini infections has also been successful. Additional studies are recommended to confirm these preliminary results (22). Animal Health Procedures to safeguard animal health are set out in the International Council for Explorations of the Sea and the European Inland Fisheries Advisory Commission Codes of Practice, which describe how to prevent the adverse effects of introducing new and exotic species and emerging animal pathogens. Education and on-site training programs for aquaculture employees will help them understand the detrimental impact of introduction of exotic species and animal pathogens, misuse and abuse of therapeutics and chemicals, and willful habitat destruction. High priority issues also include implementation of biosecurity procedures in aquaculture operations to prevent the escape and spread of exotic species and pathogens into the facility and surrounding natural environment and the use of the HACCP principles to help control the spread of exotic pathogens to wild aquatic populations (17,23). The application of HACCP principles to control transmission of exotic shrimp viruses from cultured to wild shrimp was proposed at a shrimp pathogen workshop held in June 1996 in New Orleans, Louisiana (21). Natural resource regulatory agencies are concerned about the possible transmission of exotic shrimp pathogenic viruses, recently found in shrimp aquaculture ponds in Texas and South Carolina, to wild native shrimp populations. The principles of HACCP, in conjunction with International Council for Explorations of the Sea and the European Inland Fisheries Advisory Commission Codes of Practice, were proposed to control the spread of exotic animal viruses into the environment. Shrimp aquaculture has the following proposed critical control points: pond site selection; water supply quality; pond management techniques; and transportation, especially as it relates to the live transport of aquaculture shrimp species (21). Approximately 600 million pounds of shrimp are also imported for further processing into the United States on a yearly basis, half of which are aquacultured species (3). Natural resource managers, particularly at the state level, are concerned about the possible transmission of exotic shrimp pathogens into the environment from shrimp processing plant wastewater discharge and solid waste material landfill leakage. Proposed HACCP shrimp processing plant critical control points include unload/receive; de-ice/wash; thaw; dehead/peel/devein; wash; re-ice; de-ice/wash; re-ice; and dip/glaze (21). Application of HACCP principles at aquaculture site and processing plant locations has the potential to control transmission of exotic human and animal pathogens. However, to our knowledge, except for the application of HACCP principles to control of human pathogens in Asia (17), no research has been conducted on this issue. Address for correspondence: Michael Jahncke, Virginia Tech Seafood Research and Extension Center, 102 King Street, P.O. Box 369, Hampton, VA 23669 USA; fax: 757-727-4871; e-mail: mjahncke@vt.edu. References 1. Ratafia M. Aquaculture today: a worldwide status report. Aquaculture News 1994;3:12-13,18-19. 2. Rhodes RJ. Status of world aquaculture. Aquaculture Magazine 17th Annual Buyers Guide 1987;4-18. 3. National Marine Fisheries Service. Fisheries of the United States 1995. Current Fisheries Statistics No. 9500. Washington (DC): U.S. Department of Commerce; 1996. 4. Krebs-Smith SM. Report on per capita consumption and intake of fishery products [letter]. In: National Academy of Sciences Committee on the Evaluation of the Safety of Fishery Products 1991 Seafood Safety Report. Washington (DC): National Academy Press; 1991. 5. Centers for Disease Control. Annual summary of foodborne diseases (1978). Atlanta (GA):CDC;1979. 6. Centers for Disease Control. Annual summary of foodborne diseases (1979). Atlanta (GA):CDC;1981. 7. Centers for Disease Control. Annual summary of foodborne diseases (1981). Atlanta (GA):CDC;1983. 8. Centers for Disease Control. Annual summary of foodborne diseases (1980 and 1981). Atlanta (GA):CDC;1983. 9. Centers for Disease Control. Annual summary of foodborne diseases (1982). Atlanta (GA):CDC;1985. 10. Centers for Disease Control. Annual summary of foodborne diseases, unpublished data. Atlanta (GA):CDC;1989. 11. Centers for Disease Control. Foodborne disease outbreaks, 1983-87. MMWR CDC Surveill Summ 1990;39(SS-1):1-45. 12. National Marine Fisheries Service. The draft report of the model seafood surveillance project. A report to Congress. Pascagoula (MS): Office of Trade and Industry Services, National Seafood Inspection Laboratory;1995. 13. Garrett ES. Role of diseases in marine fisheries management. Transactions of the 50th North American Wildlife and Natural Resources. NOAA Conference 1986. Tech. Memo. NMFS, F/NWR-16. Washington (DC): National Marine Fisheries Service;1986. 14. Mott KE. A proposed national plan of action for schistosomiasis control in the United Republic of Cameroon. Geneva: World Health Organization (unpublished document WHO/SCHISTO/86,88); 1996. 15. Centers for Disease Control and Prevention. Invasive infection with Streptococcus iniae-Ontario, 1995-1996. MMWR Morb Mort Wkly Rep 1996; 45(30):650-3. 16. Buras N. Microbial safety of produce from wastewater fed aquaculture. In: Pullin RVC, Rosenthal H, Maclean JL, editors. Environment and aquaculture in developing countries. Proceedings of the 31st International Center for Living Aquatic Resources Management Conference; 1993; Manila, Philippines. Manila: The Center; 1993. p. 285-95. 17. World Aquaculture Society. Abstracts of the Annual International Conference and Exposition of the World Aquaculture Society and The National Aquaculture Conference and Exposition of National Aquaculture Association; 1997 Feb 19-23; Seattle, WA. 18. Virus re-emerges at shrimp farm. The Aquaculture News 1996;4(11):1-15. 19. Pullin RSV. Discussion and recommendations on aquaculture and the environment in developing countries. In: Pullin RSV, Rosenthal H, Maclean JL, editors. Environment and aquaculture in developing countries. Proceedings of the 31st ICLARM Conference 1993. p. 312-338. 20. Turner GE, editor. Codes of practice and manual of procedures for consideration of introductions and transfers of marine and freshwater organisms. EIFAC Occasional Paper 23. Rome: FAO; 1988. 21. Jahncke JL. The application of the HACCP concept to control exotic shrimp viruses. Proceedings of the NMFS Workshop on Exotic Shrimp Viruses. 1996 June; New Orleans, LA. 22. Son TQ, Hoi VS, Dan TV, Nga C, Toan TQ, Chau LV, et al. Application of hazard analysis critical control point (HACCP) as a possible control measure against Clonorchis sinensis in cultured silver carp Hypophthalmichthys molitrix. Paper presented at 2nd Seminar on Food-Borne Zoonoses: Current Problems, Epidemiology and Food Safety; 1995 Dec 6-9; Khon Kaen, Thailand. 23. Austin B. Environmental issues in the control of bacterial diseases of farmed fish. In: Pullin RVC, Rosenthal H, Maclean JL, editors. Environmental and aquaculture in developing countries. Proceedings of the 31st International Center for Living Aquatic Resources Management Conference; 1993; Manila, Philippines. Manila: The Center; 1993. p. 237-51. ------------------------------------------------------------------------ Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Historical Overview of Key Issues in Food Safety E. M. Foster Madison, Wisconsin, USA ------------------------------------------------------------------------ Foodborne transmission of pathogenic and toxigenic microorganisms has been a recognized hazard for decades. Even half a century ago we knew about the dangers of botulism from underprocessed canned foods; staphylococcal poisoning from unrefrigerated cream-filled pastries, sliced ham, meat, and poultry salads; and salmonellosis from infected animal products. Despite new protective measures, changes in preservation techniques and failure to follow recognized procedures have created new dangers. Moreover, we now recognize new organisms that can cause foodborne illness--Listeria monocytogenes, Escherichia coli O157:H7, Campylobacter jejuni, Vibrio parahaemolyticus, Yersinia enterocolitica, and others. Controlling these organisms will require widespread education and possibly new regulatory initiatives. When I was growing up on my parents' farm in East Texas, we never thought about food poisoning or unsafe food. The only foods we bought were sugar, salt, flour, and oatmeal; everything else we produced and preserved on the farm. My mother spent all summer canning fruits and vegetables for winter. We had no refrigeration; we cured our own meat and drank raw milk. But I never heard of botulism, staph poisoning, or salmonellosis or perfringens poisoning until I studied bacteriology in college. Only then did I wonder how we survived with no refrigeration in a hot climate. Finally, the answer came to me. We just did not give the bacteria time enough to develop so they could hurt us. Leftovers from breakfast--hot biscuits, eggs, ham, bacon or sausage, oatmeal, coffee or milk--went right out to the chickens. Lunch leftovers--biscuits, cornbread, vegetables, or fried chicken--were saved for a cold supper 4 or 5 hours later. Any food left went to the pigs. The bacteria had only a maximum of 3 or 4 hours to grow, and that usually is not enough. I survived and went on to study food microbiology, which included what was known then about food poisoning. The guru of food poisoning in those days was professor Gail M. Dack at the University of Chicago. Dr. Dack was a protege of Professor E.O. Jordan, who in 1917 published a 107-page book entitled Food Poisoning. Dr. Dack took over the book and published his first version of Food Poisoning in 1943. In 1949 and 1956, subsequent editions appeared in which certain truisms became apparent. Botulism was considered a problem of canners, both home and commercial. Thus, adequate heat processing would seem to solve the problem. Perhaps it did for the canner, but now we know that heating will not eliminate all botulism. Many foods, including salmon eggs, smoked fish, garlic in oil, vacuum packaged lotus roots, and baked potatoes, can support growth and botulinum toxin formation if the storage temperature is suitable. Similarly, we thought staphylococcal poisoning was limited to cream-filled pastries and cured ham. In recent years, outbreaks of staphylococcal poisoning have been traced to cheese, whipped butter, ham salad, fermented sausages, and canned corned beef. We now know how to prevent staphylococcal poisoning, but not all food handlers understand and fully comply with the appropriate control measures. Salmonellosis was once thought a problem with meat from infected animals. Now we know that a variety of food products can serve as vehicles of this disease. As early as World War II, we found that dried eggs from the United States could transmit this disease to our British allies. Thousands of cases of human salmonellosis in the United States and other industrialized countries have been transmitted by ice cream, chocolate, potato salad, cheddar cheese, raw milk, black pepper, pate, aspic, ham, pasteurized milk, and drinking water. Clostridium perfringens, known since the 1940s, causes a problem only when there is gross temperature abuse of cooked food. Clostridium botulinum, Staphylococcus aureus, C. perfringens, and the salmonellae were well known in Dr. Dack's day, although the food vehicles might have changed. Not so well known were many of the organisms that preoccupy us today. For example, we used to think of Escherichia coli as merely an indicator organism that suggested insanitary handling. Now we know forms of E. coli can kill. Thirty years ago, Listeria monocytogenes, Campylobacter jejuni, Aeromonas hydrophila, Plesiomonas shigelloides, Vibrio parahaemolyticus, and Yersinia enterocolitica were not known; now these are well-established foodborne pathogens that we must control. Although not part of a historical overview, other key issues deserve attention during this meeting. For example, we once thought that fresh, uncracked eggs were essentially sterile and safe to eat. We did not recognize the ability of Salmonella Enteritidis to invade the laying hen and thereby the yolk of an egg. An outbreak of S. Enteritidis at a Chicago hotel taught us not to rely on the safety of eggs merely because the shell was intact. S. Enteritidis in shell eggs is still a serious health problem and a growing concern to egg and poultry producers. Of equal, if not greater, concern is Salmonella Typhimurium strain DT 104. Widely distributed in cattle herds of England, Scotland, and Wales, this organism is resistant to several antibiotics, including ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline. Between 1990 and 1995, the number of S. Typhimurium DT 104 isolated from humans in Britain increased from 259 to 3,837 per year--a 15-fold increase. Moreover, the percentage of drug-resistant isolates increased from 39% in 1990 to 97% in 1995. S. Typhimurium DT 104 has been isolated in the United States from sheep, pigs, horses, goats, emus, cats, dogs, elk, mice, coyotes, ground squirrels, raccoons, chipmunks, and birds. American egg and poultry producers are concerned about its entry into U.S. poultry flocks. S. Typhimurium DT 104 infection in humans has been associated with the consumption of chicken, sausage, and meat paste as well as with the handling of sick animals. More than one-third of the patients have required hospitalization, and 3% have died; these figures are very unusual for ordinary Salmonella infections and indicate serious problems ahead. Address for correspondence: E. M. Foster, Professor Emeritus, Food Research Institute, University of Wisconsin, Madison, WI 53706 USA; fax: 608-263-1114. ------------------------------------------------------------------------ Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Animal Diseases of Public Health Importance Gregory D. Orriss Food and Agriculture Organization of the United Nations, Rome, Italy ------------------------------------------------------------------------ The Food and Agriculture Organization's (FAO) interest in emerging diseases caused by foodborne pathogens derives from its role as the leading United Nations agency with a mandate for food quality and safety matters. The Food Quality and Standards Service of FAO's Food and Nutrition Division is active in all areas related to food safety and implements the FAO/World Health Organization Food Standards Program. Its activities include providing assistance to FAO's member nations in addressing problems and strengthening infrastructure and promoting standardization as a means of facilitating trade and safeguarding the interests of consumers. This paper considers the importance of emerging foodborne diseases from the perspectives of the consumer, international trade in food, producers and processors, and developing countries and addresses prevention and control measures. In recent years, public concern regarding food safety has increased as a consequence of the outbreak of bovine spongiform encephalopathy (BSE) in cattle, the prevalence of Salmonella serotype Enteritidis illnesses (from poultry, meat, eggs), and the more localized outbreaks of illnesses associated with Listeria monocytogenes (from dairy products, pâté, salads) and Escherichia coli O157:H7 (from ground or minced beef, unpasteurized apple juice, vegetables). Emerging pathogens and the appearance of problems such as BSE have resulted in enactment of specific controls in many countries, while the general heightening of interest internationally has prompted health professionals and the food industry in many countries to scrutinize the control of emerging infectious agents. Animal Feeding and Food Safety The Food and Agriculture Organization (FAO) of the United Nations has had a long-standing interest in the area of food safety and food quality. Because of problems such as BSE and emerging pathogens, FAO convened an Expert Consultation on Animal Feeding and Food Safety in Rome in March 1997 to address these issues and provide the scientific basis for improving practices in the feeding of animals for the production of food. The ultimate objective of food industry and safety regulators is to ensure that food reaching the consumer is safe and wholesome. This objective does not imply that food can ever be completely free of risk but rather that the level of risk to the consumer can be acceptable. Foods generally expected to be safe may become unsafe as a result of hazards introduced during production, processing, storage, transport, or final preparation by the consumer. For food derived from animal sources, the hazards may originate from a number of sources, including the consumption of contaminated feed. Hazards in food that may relate to animal feed include salmonellosis, mycotoxicosis, and ingestion of unacceptable levels of veterinary drugs and agricultural and industrial chemicals. In addition, if the postulated link between BSE and new variant--Creutzfeldt-Jakob disease is established, this disease would also be an example of contamination originating from animal feed. The FAO consultation limited its considerations to food safety matters that pertained strictly to animal feeds; it did not consider plant toxins, radionuclides, or parasites spread by human sewage. The risk to human health from other infectious agents that may contaminate either feed or forage appears to be negligible or nonexistent and was, therefore, not considered by the consultation. Only the standard domestic animals from which food is derived in large quantities, such as meat and meat products, milk and milk products, and eggs and egg products, as well as fish products derived from aquaculture that involves the feeding of fish, were considered. All aspects of animal feed, other than natural unrestricted grazing, were considered. The consultation concluded that emerging pathogens are generally not identified through traditional animal surveillance and epidemiology. Hazards Associated with Animal Feed Mycotoxins are secondary metabolites produced by fungi of various genera when fungi grow on agricultural products before or after harvest or during transportation or storage. Some fungi such as Aspergillus spp. and Penicillium spp. can invade grain after harvest and produce mycotoxins, while others, such as Fusarium spp., typically infest grains and produce mycotoxins before harvest. In some circumstances, Aspergilli can grow and produce mycotoxins before the crop is harvested. Both intrinsic and extrinsic factors influence fungal growth and mycotoxin production on a substrate. Intrinsic factors include water activity, pH, and redox potential; extrinsic factors are relative humidity, temperature, and availability of oxygen. Many mycotoxins with different chemical structures and widely differing biologic activities have been identified. Mycotoxins may be carcinogenic (e.g., aflatoxins B1, ochratoxin A, fumonisin B1), estrogenic (zearalenone and I and J zearalenols), nephrotoxic (ochratoxins, citrinin, oosporeine), dermonecrotic (trichothecenes), or immunosuppressive (aflatoxin B1, ochratoxin A, and T-2 toxin). Much of the published information on toxicity comes from studies in experimental animals, and these may not reflect the effects of mycotoxins on humans and other animals. In addition, their significance in human foods of animal origin is incompletely understood. Mycotoxins are regularly found in animal feed ingredients such as maize, sorghum grain, rice meal, cottonseed meal, groundnuts, legumes, wheat, and barley. Most are relatively stable compounds, are not destroyed by feed processing, and may even be concentrated in screenings. Various animal species metabolize mycotoxins in different ways. In pigs, ochratoxin A can undergo enterohepatic circulation and is eliminated very slowly, whereas in poultry species it is rapidly excreted. The polar mycotoxins such as fumonisins tend to be excreted rapidly. Mycotoxins, or their metabolites, can be detected in meat, visceral organs, milk, and eggs. However, their concentration in these food products is usually considerably lower than in the feed consumed by the animals; at these levels, mycotoxins are unlikely to cause acute intoxication in humans consuming these products. Residues in animal products of carcinogenic mycotoxins, such as aflatoxin B1, M1, and ochratoxin A, pose a threat to human health, and their levels should be monitored and controlled. In most instances, the principal source of mycotoxins for humans is contaminated grains and cereals, rather than animal products. This means that the hazard is much greater in developing countries in which maize and other grains form the staple diet and the intake of animal products, including meat, is low. Only limited information is available regarding mycotoxin residues in animal products intended for human consumption. The metabolism of mycotoxins by animals and the residues of mycotoxins and their metabolites in animal tissues should be studied further. Infectious Agents Agent Causing Transmissible Spongiform Encephalopathies in Ruminants Transmissible spongiform encephalopathies are nonfebrile neurologic diseases with a long incubation period and are fatal. These diseases are associated with incompletely defined agents termed prions, which are resistant to normal heat treatments of feed and food. Sheep scrapie has been recognized for over 250 years. BSE was first recognized in the United Kingdom during 1986. For BSE, the infectious agent enters the feed primarily through rendered infected tissues (notably the central nervous system and the reticuloendothelial system) under insufficient heat to reduce the concentration of the infectious agent to an ineffective dose. In the case of sheep scrapie, infection is naturally maintained by transmission between sheep. Humans have likely been exposed to the scrapie agent by eating brain and other tissues, although there is no evidence that Creutzfeldt-Jakob disease in humans has been associated with scrapie. Humans can potentially be exposed to BSE through consumption of infected tissues. The occurrence of a new variant of the human transmissible spongiform encephalopathy, Creutzfeldt-Jakob disease, has raised the possibility of an association with the BSE agent. With the limited number of cases now, there is no proven link between this new variant and the possible transmission of the agent from infected bovine tissue to humans. The FAO consultation recommended risk reduction measures to address the elimination of BSE from cattle. Salmonella enterica The more than 2,000 Salmonella serotypes can be divided into three groups: species-specific, such as gallinarum (in poultry); invasive, which may cause systemic infections in their host, such as Enteritidis (in laying hens); and noninvasive, which tend to remain within the intestinal tract. Members of the first group are infrequently feedborne pathogens. Among the second group, the principal manifestation of human infection is gastroenteritis, with septicemia occurring in some patients. The third group may be associated with subclinical infections in farm livestock; it sometimes causes disease in livestock and is associated with food poisoning in humans. Salmonellae are widely distributed, and animal feed is only one of many sources of infection for farm animals. Animal feed ingredients of both animal and plant origin are frequently contaminated with salmonellae, although the most common serotypes associated with human disease, Enteritidis and Typhimurium, are rarely isolated from animal feed. Feed can be contaminated from raw ingredients. Toxoplasma gondii The protozoon T. gondii is found in cats and, according to serologic surveys, also in birds and other domesticated species including sheep, pigs, goats, and horses. The primary source of infection for animals is feed contaminated with feces of cats and possibly with rodent tissues. Cats are an important source of infection for humans; however, some human infections may be due to the handling or consumption of raw meat. Pregnant women may miscarry or give birth prematurely, and infants often get central nervous system disorders and ocular disease. Trichinella spiralis T. spiralis is a nematode that parasitizes the intestinal tract of mammals, particularly pigs. The larvae encyst in the tissues, particularly the muscles, which act as a source of infection for humans who consume raw or partially cooked meat. The clinical manifestations include fever, muscle pain, encephalitis, meningitis, myocarditis, and (rarely) death. The cysts in infected carcasses can be killed by freezing (-18°C for 20 days) or traditional rendering temperatures. Adequate cooking of raw meat and table scraps before feeding to farm animals would eliminate this hazard. The FAO consultation also addressed potential hazards associated with veterinary drugs and agricultural and other chemicals and recommended risk reduction measures to prevent, eliminate, or reduce the hazards to acceptable levels. The consultation participants prepared a draft Code of Practice for Good Animal Feeding to be considered by the Codex Alimentarius Commission (CAC). Codex Alimentarius Commission Since 1962, CAC has been responsible for implementing the Joint FAO/World Health Organization (WHO) Food Standards Program. "Codex Alimentarius," whose name is taken from Latin and translates literally as "food code" or "food law," was founded in response to the worldwide recognition of the importance of international trade and the need to facilitate trade while ensuring the quality and safety of food for the world consumer. It follows, therefore, that the commission's primary objectives are the protection of the health of consumers, the assurance of fair practices in the food trade, and the coordination of all food standards. Food standards, guidelines, and recommendations are the work of CAC. With the adoption of the World Trade Organization's Agreement on the Application of Sanitary and Phytosanitary Measures and the Agreement on Technical Barriers to Trade, a new emphasis and dimension have been placed on Codex standards. Codex Committee on Food Hygiene The Codex Committee on Food Hygiene (CCFH) has overall responsibility for all provisions of food hygiene prepared by Codex commodity committees and contained in commodity standards, codes of practice, and guidelines. CCFH also develops general principles, codes of practice, guidelines for food hygiene, and microbiologic criteria for food to be applied horizontally across Codex committees. Food hygiene is defined as "all conditions and measures necessary to ensure the safety and suitability of food at all stages of the food chain." According to the deliberations at the 29th session of CCFH, the microbiologic safety of foods is principally ensured by control at the source, product design, process control, and good hygienic practices during production, processing, handling, distribution, storage, sale, preparation, and use, preferably in conjunction with the application of the Hazard Analysis and Critical Control Points (HACCP) system. This preventive system offers more control than end-product testing because of the limited effectiveness of microbiologic examination to assess the safety of food. When they have been established by Codex or national risk managers, objectives for food safety can be taken up by industry; by applying HACCP (or an equivalent food safety management system), industry can ensure that these objectives are met. This is the use of HACCP as a corrective risk management option: a risk is identified, and a management option is selected and implemented. HACCP is also used as a preventive risk management tool. In this case, hazard analysis identifies potential hazards in raw materials, production line, and line-environments to the consumer. Hazard analysis is defined as "The process of collecting and evaluating information on hazards and conditions leading to their presence to decide which are significant for food safety and therefore should be addressed in the HACCP plan." Input concerning the potential hazards and their control could come from risk analysis, but often such information is not available and industries need to apply their best judgment. The Revised Principles for the Establishment and Application of Microbiological Criteria For Foods states, "Microbiological criteria should be established according to these principles, and be based on scientific analysis and advice, and where sufficient data are available, on a risk analysis appropriate to the foodstuff and its uses." These criteria may be relevant to the examination of foods, including raw materials and ingredients of unknown or uncertain origin, and may be used when no other means of verifying the efficacy of HACCP-based systems and good hygienic practices are available. Microbiologic criteria may also be used to determine that processes are consistent with the General Principles of Food Hygiene. Microbiologic criteria are not normally suitable for monitoring critical limits as defined in the HACCP system. Establishing microbiologic criteria and food safety objectives in general is difficult because of the considerable knowledge gap relating to biologic hazards and their relationship to human illness. This has led to many evaluations by CCFH, which are based on subjective or qualitative assessments and serve as the basis for recommendations. Although aware of these limitations, CCFH is now developing a framework of principles and guidelines for the application of microbiologic risk assessment. CCFH's action was in response to the recommendation of the 1995 Joint FAO/WHO Consultation on the Application of Risk Analysis to Food Standards relating to the application of risk assessment within the Joint FAO/WHO Food Standards Program. International Commission for Microbiological Specifications for Foods and CCFH delegations are also in the process of developing background papers on a number of foodborne pathogens to better conduct quantitative risk assessments and set subsequent food safety objectives. Notwithstanding the development of risk analysis approaches by these groups, the work of CCFH and all Codex committees would benefit from advice from an expert body on foodborne biologic hazards for purposes of risk management. The committee could be modeled on the FAO/WHO Joint Expert Committee on Food Additives and Joint Meeting on Pesticide Residues, allowing for the unique consideration of epidemiologic and clinical data related to pathogens causing human illness, and of the dynamics of microbial populations in food throughout the food chain. Control of Listeria monocytogenes in foods is an example of the need to consider a structured risk management approach. Listeria are frequently consumed in small amounts by the general population without apparent ill effects. Only higher levels of Listeria are thought to cause serious disease problems. It is believed that Listeria will always be present in the environment. Therefore, the critical issue may not be how to prevent Listeria in foods, but how to control its survival and growth to minimize the potential risk. In many foods, complete absence of Listeria is unrealistic and unattainable; trying to achieve this goal can limit trade without having any appreciable benefit to public health. A relevant risk management option, therefore, is to focus on foods that have historically been associated with human disease and support the growth of Listeria to high levels, rather than focusing on foods that do not support growth. Thus, establishing tolerably low levels of Listeria in specific foods may be one food safety objective achieved by risk managers after a rigorous and transparent risk analysis. Such an approach is now being considered by CCFH after an initial risk assessment by the International Commission for Microbiological Specifications for Foods and CCFH delegations. Although Listeria presents unique challenges in terms of its widespread occurrence and the particular susceptibility of vulnerable groups, pathogens such as E. coli O157:H7, Salmonella, and Campylobacter are also being addressed. These microbial pathogens produce acute foodborne illnesses and can cause severe chronic sequelae, creating an important public health problem and food safety concerns. Codex Codes of Hygienic Practice are based on good manufacturing practices, HACCP principles, and risk analysis. CCFH is responsible for coordinating and overseeing the work of specific Commodity Committees in this area. In the specific area of food hygiene, Codex has revised its main document, Recommended International Code of Practice: General Principles of Food Hygiene, to incorporate risk assessment principles and include specific references to the HACCP system. FAO Programs on Food Quality and Safety The Food Quality and Standards Service is a service within the Food and Nutrition Division of the FAO, located in Rome. The Secretariat of CAC is also located there. The Regular Program of the Food Quality and Standards Service provides the technical and scientific basis for FAO for all food quality matters, including food safety. This includes providing the Secretariat for the Joint Expert Committee on Food Additives and participation in both the Joint Meeting of the FAO Panel of Experts on Pesticide Residues in Food and the Environment and the WHO Expert Group on Pesticide Residues and in the Joint Expert Committee on Food Irradiation. The Food Quality and Standards Service develops and publishes guidelines and manuals (including the FAO Food and Nutrition Paper Series and Manuals of Food Quality Control), arranges expert consultations and conferences (e.g., the Joint FAO/WHO Expert Consultation on Biotechnology and Food Safety, September 30 to October 4, 1996; the Joint FAO/WHO Expert Consultation on the Application of Risk Management to Food Safety Matters, January 27-31, 1997; the Joint FAO/WHO Consultation on Food Consumption and Exposure Assessment to Chemicals, February 10-14, 1997; and the FAO Consultation on Animal Feeding and Food Safety, March 10-14, 1997), and has a major and continuing program of providing technical assistance regarding food standards and food control to member countries, particularly developing countries and countries in transition from a centrally planned to a market economy. The Joint Expert Committee on Food Additives, the Joint Meeting on Pesticide Residues, and the Joint Expert Committee on Food Irradiation are expert committees that provide independent scientific advice that forms the basis for the development of food safety recommendations used in international trade. These committees are forums in which independent, invited experts assess the state of scientific knowledge of food additives, pesticide and veterinary drug residues in food, mycotoxins, other chemical contaminants in food, and food irradiation treatments and make recommendations to member governments and to Codex. FAO's Food Quality and Standards Service also develops and publishes Manuals of Food Quality Control. These manuals provide recommendations for the development and operation of food quality and safety systems. While aimed primarily at providing advice to developing countries, the manuals document modern approaches, including the development of quality control programs throughout the food chain that apply to all countries. Such an approach is instrumental in facilitating international trade in food. Key titles in the series include Food Inspection, Food for Export, Management of Food Control Programs, Imported Food Inspection, and Quality Assurance in the Food Control Laboratory. The program of technical assistance projects undertaken by the Food Quality and Standards Service handles assistance in food quality control, including safety; such projects have established or strengthened the food control systems in a number of developing countries. Typically, they assist in establishing the infrastructure for an enhanced food control program, assessing laboratory service requirements, providing guidance to develop legislation and procedural manuals, setting up reputable inspection and certification systems, and providing training and staff development. In these assistance projects, the standards established by the CAC are basic guides to international requirements. Conclusion Food will always represent some biologic risk; it is the task of the food industry to maintain the level of risk at the minimum that is practical and technologically feasible. It should be the role of regulatory bodies to use risk assessment to determine realistic and achievable risk levels for foodborne hazards and to base their risk management and food safety policies on the practical application of the results of these analyses. Foodborne illnesses are preventable. Adherence to good manufacturing practices and good hygienic practices and application of the HACCP system can result in food safety and ensure food quality. Food safety is the shared responsibly of governments, academia, the food industry, and the consumer. Codex standards, guidelines, and recommendations have the objective of protecting the consumer and facilitating international food trade. Adherence to Codex provides the basis for food safety and quality and meets the requirements of international trade. Address for Correspondence: Gregory D. Orriss, Chief, Food Quality and Standards Service; Food and Nutrition Division; Food and Agriculture Organization of the United Nations; fax: 39-6-5705-4593; e-mail: Gregory.Orriss@fao.org. ------------------------------------------------------------------------ Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA