[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Special Issue Produce Handling and Processing Practices Larry R. Beuchat and Jee-Hoon Ryu University of Georgia, Griffin, Georgia, USA --------------------------------------------------------------------------- In the past decade, outbreaks of human illness associated with the consumption of raw vegetables and fruits (or unpasteurized products produced from them) have increased in the United States. Changes in agronomic, harvesting, distribution, processing, and consumption patterns and practices have undoubtedly contributed to this increase. Pathogens such as Listeria monocytogenes, Clostridium botulinum, and Bacillus cereus are naturally present in some soil, and their presence on fresh produce is not rare. Salmonella, Escherichia coli O157:H7, Campylobacter jejuni, Vibrio cholerae, parasites, and viruses are more likely to contaminate fresh produce through vehicles such as raw or improperly composted manure, irrigation water containing untreated sewage, or contaminated wash water. Contact with mammals, reptiles, fowl, insects, and unpasteurized products of animal origin offers another avenue through which pathogens can access produce. Surfaces, including human hands, which come in contact with whole or cut produce represent potential points of contamination throughout the total system of growing, harvesting, packing, processing, shipping, and preparing produce for consumption. Treatment of produce with chlorinated water reduces populations of pathogenic and other microorganisms on fresh produce but cannot eliminate them. Reduction of risk for human illness associated with raw produce can be better achieved through controlling points of potential contamination in the field; during harvesting; during processing or distribution; or in retail markets, food-service facilities, or the home. Advances in agronomic, processing, preservation, packaging, shipping, and marketing technologies on a global scale have enabled the fresh fruit and vegetable industry to supply consumers with a wide range of high-quality produce year round. Some of the same technologies and practices have also introduced an increased risk for human illness associated with pathogenic bacteria, mycotoxigenic molds, viruses, and parasites. The use of manure rather than chemical fertilizer, as well as the use of untreated sewage or irrigation water containing pathogens, viruses, or parasites, undoubtedly contributes to this increased risk. Changes in the produce industry, social demographics, food consumption patterns, and awareness of fresh fruits and vegetables as potential vehicles of infection may also be contributing to an increase in documented produce-associated outbreaks of human illness. Changing factors that contribute to the epidemiology of diseases that may be associated with fresh fruits and vegetables were discussed by Hedberg et al. (1). Increases in foodborne illness during the summer are not fully understood, although fresh produce is likely to play a role since it is consumed in higher quantities during the summer. The per capita consumption of fresh produce has increased in the United States in recent years (Figure 1), not only in the summer but also in other seasons, partly because of increased importation. Knowledge of the presence and numbers of specific pathogens on produce imported to the United States from countries that may have lower sanitation standards is minimal. However, produce from a single grower, packinghouse, or shipper, whether located outside or within the United States, may be routinely distributed throughout the country, thus facilitating widespread dissemination of potential pathogens. The epidemiology of foodborne diseases is greatly influenced by these global changes. Control or elimination of pathogenic microorganisms from fresh fruits and vegetables can be achieved only by addressing the entire system, from the field, orchard, or vineyard to the point of consumption. [Figure not available in ASCII.] We reviewed some of the practices (particularly preharvest practices) used by the fresh fruit and vegetable industry that may promote contamination of produce with pathogenic microorganisms. Sources of Contamination The presence of pathogenic bacteria, viruses, and parasites on fresh fruits and vegetables has been extensively documented (3). Contamination of produce can occur in the field or orchard; during harvesting, postharvest handling, processing, shipping, or marketing; or in the home (Table). Table. Sources of pathogenic microorganisms on fresh fruits vegetables* ------------------------------------------------- Preharvest Feces Soil Irrigation water Water used to apply fungicides, insecticides Green or inadequately composted manure Air (dust) Wild and domestic animals (including fowl and reptiles) Insects Human handling Postharvest Feces Human handling (workers, consumers) Harvesting equipment Transport containers (field to packing shed) Wild and domestic animals (including fowl and reptiles) Insects Air (dust) Wash and rinse water Sorting, packing, cutting, and further processing equipment Ice Transport vehicles Improper storage (temperature, physical environment) Improper packaging (including new packaging technologies) Cross-contamination (order foods in storage, preparation, and display areas) Improper display temperature Improper handling after wholesale or retail purchase ------------------------------------------------- *Adapted from Beuchat Preharvest Sources Spores of Clostridium species, including C. botulinum and C. perfringens, as well as spores of enterotoxigenic Bacillus cereus, are commonly found in soil, so their occasional presence on fruits and vegetables should not be unexpected. Numbers of clostridial spores on some types of vegetables appear to increase during the summer (4). Perhaps the most prevalent disease-causing microorganism in soil is Listeria monocytogenes (5,6). Twenty-seven strains were isolated from soil and vegetation taken from 19 sites in the Netherlands (7). Plant materials from which the organism was isolated included dead and decayed corn and soybean plants and wild grasses, indicating its preference to exist in nature as a saprophyte. A study of soil and domestic animal feces has shown that Listeria is more often present during July to September than other months (8). L. monocytogenes and L. innocua were predominant in feces, whereas L. ivanovi and L. seeligeri were most common in soil. Vegetation in a rural area in Virginia where clinical listeriosis is rare was analyzed for L. monocytogenes (9). Dead soybean plant material and stalks, leaves, and tassels of corn were collected in April following the previous planting year. Eight of twelve sampling sites yielded plant materials positive for L. monocytogenes. Only 25% of the strains were pathogenic for mice, a low frequency compared with the percentage of pathogenic strains isolated from Listeria-positive humans and animals in Virginia and the United States as a whole. These observations suggest that the predominance of certain serotypes of L. monocytogenes may be influenced by the environment and that some strains indigenous to decaying plant vegetation are incapable of causing human illness. Weiss and Seeliger (10) isolated 154 strains of L. monocytogenes in Germany from soil and plants, 16 from feces of deer and stag, nine from moldy fodder and wildlife feeding grounds, and eight from birds. Corn, wheat, oats, barley, and potato plants and soils from the fields in which they were growing were among the materials analyzed. Nearly 10% of the corn plants and 13% of the grain plants were infected with L. monocytogenes. Plants from cultivated fields had a lower incidence (12.5%) than plants from uncultivated fields (44%). Twenty-three percent of samples collected from wildlife feeding grounds were positive for L. monocytogenes. It was suggested that L. monocytogenes is a saprophyte that lives in a plant-soil environment and could therefore be contracted by humans and animals through many possible routes from many sources. Birds and animals are unlikely to be the only sources responsible for the distribution of L. monocytogenes in nature and its presence on fruits and vegetables. The presence of other pathogenic bacteria, viruses, and parasites in soil likely results largely from application of feces or untreated sewage, either by chance or design. Whatever the case, soil on the surface of fruits and vegetables may harbor pathogenic microorganisms that remain viable through subsequent handling to the point of consumption unless effective sanitizing procedures are administered. Irrigation and surface run-off waters can be sources of pathogenic microorganisms that contaminate fruits and vegetables in the field. Irrigation water containing raw sewage or improperly treated effluents from sewage treatment plants may contain hepatitis A, Norwalk viruses, or enteroviruses (poliomyelitis, echoviruses, and Coxsackie viruses) (11). Rotaviruses are known to retain viability on the surface of vegetables held at 4°C for up to 30 days (12). Listeria and other potentially pathogenic bacteria have been reported in sewage. Watkins and Sleath (13) analyzed 52 sewage, river water, and industrial effluents for pathogens. Effluents were from abattoirs, cattle markets, and poultry packing plants. L. monocytogenes was isolated from all samples. In many instances, populations of L. monocytogenes were higher than those for salmonellae and, in some instances, L. monocytogenes was isolated when no salmonellae were detected. Application of sludge containing L. monocytogenes and salmonellae to soil showed that L. monocytogenes could survive longer. Populations of L. monocytogenes in soil remained essentially unchanged during 7 weeks after application. Treatment of sewage does not always yield a sewage sludge cake or a final discharge free of Listeria (14). The use of sewage as a fertilizer could contaminate vegetation destined for human consumption. MacGowan et al. (8) examined sewage at 2-month intervals in 1991 to 1992 and found 84% to 100% contained L. monocytogenes or L. innocua. Application of sewage sludge or irrigation water to soil is one avenue through which parasites can contaminate fruits and vegetables. Ascaris ova sprayed onto tomatoes and lettuce remain viable for up to 1 month, while Endamoeba histolytica could not be recovered 1 week after spraying (15,16). If sewage irrigation or night soil application is stopped 1 month before harvest, the produce would not likely be vectors for transmission of diseases caused by these parasites. Wang and Dunlop (17,18) recovered Salmonella, Ascaris ova, and Endamoeba coli cysts from more than half of irrigation water samples contaminated with either raw sewage or primary-treated, chlorinated effluents. Only one of 97 samples of vegetables irrigated with this water yielded Salmonella, but Ascaris ova were recovered from two of 34 vegetable samples. Barbier et al. (19) concluded that application of sewage sludge containing Taenia saginata eggs offers a serious risk for cattle even after a 3-week no-grazing period. Feces have been suspected as sources of pathogens on contaminated fruits, vegetables, or minimally processed produce that have subsequently been associated or confirmed as causes of human disease outbreaks (3). Among the more recent outbreaks are those linking unpasteurized apple juice to Escherichia coli O157:H7 infections. This pathogen can remain viable in bovine feces for up to 70 days, depending on inoculum level and temperature (17). Cryptosporidium infection linked to consumption of unpasteurized apple juice was hypothesized to have been caused by contamination of apples by calf feces (20). Contact of fruits and vegetables by pickers and handlers at the time of harvest also offers a mechanism by which pathogens in feces can contaminate raw produce. Wild birds are known to disseminate Campylobacter (21,22), Salmonella (22,23), Vibrio cholerae (24), and Listeria species (25). More recently, E. coli O157:H7 has been isolated from wild bird feces. In a survey of wild birds (mainly gulls), 0.9% of the bacterial isolates from fecal samples at an urban landfill and 2.9% of bacterial isolates from fecal samples on intertidal sediments were Vero cytotoxin-producing E. coli O157:H7 (26). Pathogenic bacteria are apparently picked up as a result of birds feeding on garbage, sewage, fish, or lands that are grazed with cattle or have had applications of fresh manure. Control of preharvest contamination of fruits and vegetables with pathogenic bacteria by wild birds would be exceptionally difficult. Postharvest Sources Some of the possible preharvest sources of pathogenic microorganisms may also be postharvest sources (Table). The fecal-oral route of transmission of pathogens broadens to include workers handling fruits and vegetables from the point of removal from the plant through all stages of handling, including preparation at the retail and food service levels and in the home. Changes in eating habits, particularly the increased consumption of meals away from home, must be considered when attempting to provide reasons for increased frequency of outbreaks associated with fresh produce. Proper training of food-service workers in hygienic practices is essential. One cannot assume that newly hired personnel have even rudimentary knowledge of food microbiology. This is particularly critical among teenagers who, partly because they and their parents are eating more meals away from home, have had minimal or no exposure to proper food-handling practices. Instruction in elementary principles of food hygiene at the high school or middle school levels has diminished greatly in the past two decades. Traditionally recognized postharvest control points for access of pathogens to whole or cut produce include transport containers and vehicles and sorting, packing, cutting, and further processing equipment. The development of new processing equipment and technologies should include a team of experts in food microbiology as well as engineering. Too often, aspects of sanitizing equipment are not considered or are an afterthought and can increase the risk for contaminated end products. Temperature control is absolutely critical at every stage of postharvest handling if any success is to be achieved in minimizing the growth of pathogens. Removal of Pathogens Sanitizers that can be used to wash or to assist in lye peeling of fruits and vegetables are regulated by the U.S. Food and Drug Administration in accordance with the Federal Food, Drug and Cosmetic Act as outlined in the Code of Federal Regulations, Title 21, Ch. 1, Section 173.315. As noted by Barmore (27), no chlorine substitute effective for washing fruits and vegetables is available. Numerous alternatives for sanitizing equipment (28) can be used in a total sanitation program, but none has as broad a spectrum of activity as chlorine. Chlorine is routinely used as a sanitizer in wash, spray, and flume waters used in the fresh fruit and vegetable industry. Antimicrobial activity depends on the amount of free available chlorine (as hypochlorous acid) in water that comes in contact with microbial cells. The efficacy of chlorine in killing pathogenic microorganisms has been extensively studied. Possible uses in packinghouses and during washing, cooling, and transport to control postharvest diseases of whole produce have been reviewed by Eckert and Ogawa (29). The effect of chlorine concentration on aerobic microorganisms and fecal coliforms on leafy salad greens was studied by Mazollier (30). Total counts were markedly reduced with increased concentrations of chlorine up to 50 ppm, but a further increase in concentration up to 200 ppm did not have an additional substantial effect. A standard procedure for washing lettuce leaves in tap water was reported to remove 92.4% of the microflora (31). Including 100 ppm available free chlorine in wash water reduced the count by 97.8%. Adjusting the pH from 9 to 4.5 to 5.0 with inorganic and organic acids resulted in a 1.5- to 4.0-fold increase in microbicidal effect. Increasing the washing time in hypochlorite solution from 5 to 30 minutes did not decrease microbial levels further, whereas extended washing in tap water produced a reduction comparable to hypochlorite. The addition of 100 ppm of a surfactant (Tween 80) to a hypochlorite washing solution enhanced lethality but adversely affected sensory qualities of lettuce. Dipping Brussels sprouts into chlorine solution (200 ppm) for 10 seconds decreased the number of viable L. monocytogenes cells by about 2 log (subscript 10) CFU/g (32). The maximum log(subscript 10) reduction of L. monocytogenes on shredded lettuce and cabbage treated with 200 ppm chlorine for 10 minutes was 1.3 to 1.7 log(subscript 10) CFU/g and 0.9 to 1.2 log(subscript 10) CFU/g, respectively (12). Numbers decreased only marginally with increased exposure time from 1 to 10 minutes, which agrees with observations made by Brackett (32) that the action of chlorine against L. monocytogenes occurs primarily during the first 30 seconds of exposure. Nguyen-the and Carlin (33) concluded that the elimination of L. monocytogenes from the surface of vegetables by chlorine is unpredictable and limited. Populations of Salmonella Montevideo on the surface and in the stem core tissue of tomatoes can be substantially reduced by dipping fruits 2 minutes in a solution containing 60 or 110 ppm chlorine, respectively; however, treatment in a solution containing 320 ppm chlorine does not result in complete inactivation (34). The ineffectiveness of 100 ppm chlorine against S. Montevideo injected into cracks in the skin of mature green tomatoes was demonstrated by Wei et al. (35). Treatment of alfalfa seeds injected with Salmonella Stanley (10(superscript 2) to 10(superscript 3) CFU/g) in 100 ppm chlorine solution for 10 minutes has been reported to cause a substantial reduction in population, and treatment in 290 ppm chlorine solution resulted in a substantial reduction compared with treatment with 100 ppm chlorine (36). Initial free chlorine concentrations up to 1,000 ppm, however, did not result in further reductions. Treatment of seeds containing 10(superscript 1) to 10(superscript 2) CFU/g of S. Stanley for 5 minutes in a solution containing 2,040 ppm chlorine reduced the population to less than 1 CFU/g. We have studied the efficacy of chlorine, hydrogen peroxide, and ethanol in removing Salmonella from injected alfalfa sprouts. Sprouts were dipped in solutions containing 200, 500, or 2,000 ppm chlorine for 2 minutes. The pathogen was reduced by about 2 log(subscript 10) CFU/g after treatment with 500 ppm chlorine, compared with the control, and to an undetectable level (<1 CFU/g) after treatment with 2,000 ppm chlorine (Figure 2). Chlorine treatment (2,000 ppm) of cantaloupe cubes injected with the same five-serotype cocktail of Salmonella resulted in less than 1 log10 reduction in viable cells (Figure 2). The very high level of organic matter in the juice released from cut cantaloupe tissue apparently neutralizes the chlorine before its lethality can be manifested. [Figure not available in ASCII.] As noted by Lund (37), the inaccessibility of chlorine to microbial cells in crevices, creases, pockets, and natural openings in the skin also undoubtedly contributes to the overall lack of effectiveness of chlorine in killing pathogens. The hydrophobic nature of the waxy cuticle on tissue surfaces protects surface contaminants from exposure to chlorine and other produce sanitizers that do not penetrate or dissolve these waxes. Surface-active agents lessen the hydrophobicity of fruit and vegetable skins as well as the surfaces of edible leaves, stems, and flowers, but they may also cause deterioration of sensory qualities (31,38). Sanitizers that contain a solvent that would remove the waxy cuticle layer, and with it enmeshed contaminants, without adversely affecting sensory characteristics would hold greater potential than chlorinated water in reducing microbial populations on whole raw produce. Such sanitizers may be limited to use on produce that will be further processed into juice or cut products, or on whole fruits, vegetables, or plant parts destined for immediate consumption, since their application could adversely affect visual appearance. Clearly, chlorine, at concentrations currently permitted for use by the industry to wash fresh fruits and vegetables, cannot be relied upon to eliminate pathogens. Address for correspondence: Larry R. Beuchat, Center for Food Safety and Quality Enhancement, University of Georgia, Griffin, Georgia 30223 USA; fax: 770-229-3216; e-mail: lbeucha@cfsqe.griffin.peachnet.edu. References 1. Hedberg CW, MacDonald KL, Osterholm MT. Changing epidemiology of food-borne disease: a Minnesota perspective. Clin Infect Dis 1994;18:671-82. 2. United States Department of Agriculture. Vegetables and specialties/VGS-269/July. Fruits and tree nuts/FTS-278/October. Washington (DC): USDA Economic Research Service; 1996. p. 22,81. 3. Beuchat LR. Pathogenic microorganisms associated with fresh produce. Journal of Food Protection 1996;59:204-6. 4. Ercolani GL. Occurrence and persistence of culturable clostridial spores on the leaves of horticultural plants. Journal of Applied Microbiology 1997;82:137-40. 5. Beuchat LR. Listeria monocytogenes: incidence in vegetables. Food Control 1996;7:223-8. 6. Welshimer HJ. Survival of Listeria monocytogenes in soil. J Bacteriol 1960;80:316-20. 7. Welshimer HJ, Donker-Voet J. Listeria monocytogenes in nature. Appl Environ Microbiol 1971;21:516-9. 8. MacGowan AP, Bowker K, McLauchlin J, Bennett PM, Reeves DS. The occurrence and seasonal changes in the isolation of Listeria spp. in shop bought food stuffs, human feces, sewage and soil from urban sources. Int J Food Microbiol 1994;21:325-34. 9. Welshimer HJ. Isolation of Listeria monocytogenes from vegetation. J Bacteriol 1968;95:300-3. 10. Weiss J, Seeliger HPR. Incidence of Listeria monocytogenes in nature. Appl Microbiol 1975; 29:29-32. 11. Bagdasargan GA. Survival of viruses of the enterovirus group (poliomyelitis, ECHO, Coxsackie) in soil and on vegetables. Journal of Hygiene, Epidemiology, Microbiology and Immunology 1964;8:497-505. 12. Badaway AS, Gerba CP, Kelly LM. Survival of rotavirus SA-11 on vegetables. Food Microbiology 1985;2:199-205. 13. Watkins J, Sleath KP. Isolation and enumeration of Listeria monocytogenes from sewage sludge and river water. J Appl Bacteriol 1981;50:1-9. 14. Al-Ghazali MR, Al-Azawi SK. Detection and enumeration of Listeria monocytogenes in a sewage treatment plant in Iraq. J Appl Bacteriol 1986;60:251-4. 15. Rudolfs W, Falk LL, Ragotzkie RA. Contamination of vegetables grown in polluted soil. III. Field studies on Ascaris eggs. Sewage and Industrial Waste 1951;23:656-60. 16. Rudolfs W, Falk LL, Ragotzkie RA. Contamination of vegetables grown in polluted soil. II. Field and water studies on Endamoeba cysts. Sewage and Industrial Waste 1951;23:478-85. 17. Wang G, Zhao R, Doyle MP. Fate of enterohemorrhagic Escherichia coli O157:H7 in bovine feces. Appl Environ Microbiol 1996;62:2567-70. 18. Dunlop SG, Wang W-LL. Studies on the use of sewage effluent for irrigation of truck crops. Journal of Food Protection 1961;24:44-7. 19. Barbier D, Perrine D, Duhamel C, Doublet R, Georges P. Parasitic hazard with sewage sludge applied to land. Appl Environ Microbiol 1990;56:1420-2. 20. Millard PG, Gensheimer KF, Addiss DG, Sosin DM, Beckett GA, Houck-Jankoski A, Hudson A. An outbreak of cryptosporidiosis from fresh-pressed apple cider. JAMA 1994;272:1592-6. 21. Luechtefeld N, Blaser M, Reller L, Wang W. Isolation of Campylobacter fetus subsp. jejuni from migratory wildfowl. J Clin Microbiol 1980;12:406-8. 22. Jones F, Smith P, Watson DC. Pollution of a water supply catchment by breeding gulls and the potential environmental health implications. Journal of the Institute of Water and Engineering Science 1978;32:469-82. 23. Lee JV, Basford D, Donovan T, Furniss A, West D. The incidence of Vibrio cholerae in water, animals and birds in Kent, England. J Appl Bacteriol 1982;52:281-91. 24. Fenlow DR. Wild birds and silage as reservoirs of Listeria in the agricultural environment. J Appl Bacteriol 1985;59:537-44. 25. Wallace JS, Cheasty T, Jones K. Isolation of Vero cytotoxin-producing Escherichia coli O157:H7 from wild birds. J Appl Microbiol 1997;82:399-404. 26. Barmore CR. Chlorineare there alternatives? Cutting Edge 1995; Spr 1995; 4-5. 27. Cords BR, Dychdala GR. Sanitizers: halogens, surface-active agents and peroxides. In: Davidson PM, Branen AL, editors. Antimicrobials in Foods. 2nd ed. New York: Marcel Dekker, Inc.; 1993. p. 469-537. 28. Eckert JW, Ogawa JM. The chemical control of postharvest diseases: deciduous fruits, berries, vegetables and root/tubers crops. Annu Rev Phytopathol 1988;26:433-63. 29. Mazollier J. Ivč gamme. Lavage-desinfection des salades. Infros-Crifl 1988;41:19. 30. Adams MR, Hartley AD, Cox LJ. Factors affecting the efficiency of washing procedures used in the production of prepared salads. Food Microbiology 1989;6:69-77. 31. Brackett RE. Antimicrobial effect of chlorine on Listeria monocytogenes. Journal of Food Protection 1987;50:999-1003. 32. Nguyen-the C, Carlin F. The microbiology of minimally processed fresh fruits and vegetables. Crit Rev Food Sci Nutr 1994;34:371-401. 33. Zhuang R-Y, Beuchat LR, Angulo FJ. Fate of Salmonella montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Appl Environ Microbiol 1995;61:2127-31. 34. Wei CI, Huang TS, Kim JM, Lin WF, Tamplin ML, Bartz JA. Growth and survival of Salmonella montevideo on tomatoes and disinfection with chlorinated water. Journal of Food Protection 1995;58:829-36. 35. Jaquette CB, Beuchat LR, Mahon BE. Efficacy of chlorine and heat treatment in killing Salmonella stanley inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl Environ Microbiol 1996;62:2212-5. 36. Lund BM. Bacterial spoilage. In: Dennis C, editor. Post-harvest pathology of fruits and vegetables. London: Academic Press; 1983. p. 219. 37. Zhang S, Farber JM. The effects of various disinfectants against Listeria monocytogenes on fresh-cut vegetables. Food Microbiology 1996;13:311-21. --------------------------------------------------------------------------- Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA URL: ftp://ftp.cdc.gov/pub/EID/vol3no4/ascii/beuchat.txt [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Special Issue Indentifying and Controlling Emerging Foodborne Pathogens: Research Need Robert L. Buchanan USDA ARS Eastern Regional Research Center, Wyndmoor, PA, USA --------------------------------------------------------------------------- Systems for managing the risks associated with foodborne pathogens are based on detailed knowledge of the microorganisms and the foods with which they are associated—known hazards. An emerging pathogen, however, is an unknown hazard; therefore, to control it, key data must be acquired to convert the pathogen from an unknown to a known hazard. The types of information required are similar despite the identity of the new agent. The key to rapid control is rapid mobilization of research capabilities targeted at addressing critical knowledge gaps. In addition, longer-term research is needed to improve our ability to respond quickly to new microbial threats and help us become more proactive at anticipating and preventing emergence. The type of contingency planning used by the military in anticipating new threats serves as a useful framework for planning for new emergence. The microbiologic safety of food has been advanced substantially by the introduction and implementation of Hazard Analysis and Critical Control Points (HACCP). HACCP provides a systematic conceptual framework for identifying hazards and focusing efforts on the proper functioning of key food production, processing, and marketing steps. When applied appropriately, HACCP is a cost-effective means of controlling known hazards in foods. Its successful implementation depends on knowledge of such issues as the pathogenic microorganisms' virulence, cultural characteristics, ways in which they contaminate the food, effects of food processing and preparation on their survival, and food consumption patterns. Because it requires substantial knowledge, HACCP cannot be expected to control unknown hazards, such as emerging foodborne pathogens. Therefore, controlling a new foodborne microbial threat requires moving the hazard as quickly as possible from being unknown to being known. The key to this transition is the timely acquisition of needed research data. This article identifies classes of research information needed and discusses a conceptual approach for addressing unknown microbial threats. Anticipating the Next Emerging Pathogen Two types of emergence are encountered with pathogenic foodborne microorganisms. A true emergence, where a microorganism that had not been identified as a public health threat begins to cause disease, is relatively rare. More common is reemergence, where a known microorganism causes disease in a new way, for example, by causing new types of infections, being associated with new foods, or appearing in new geographic locations. For both types, the operational requirement is to control an unanticipated public health threat. The timeliness of response is critical since the public health and economic costs of an emerging pathogen are directly related to the time between its emergence and its control. The events that lead to emergence are often complex, with the cause often being obscure and only indirectly related to the new agent. Past emergence of foodborne pathogens has been associated with changes in microbial genotypes, demographics, food production and processing methods, marketing and preparation practices, medical diagnostics, globalization of the food industry, changes in consumer education, and general socioeconomic trends (1-3). Planning for a microbial threat is a challenge because one does not know what the agent will be, what food it will be associated with, or where or when emergence will occur. While there are several potential ways of anticipating and responding to microbial threats, the contingency planning used by the military to anticipate threats seems well suited for emerging pathogens. Military contingency planning can be viewed as having four major components: intelligence, personnel and facilities, rapid response, and strategic planning. Intelligence is the gathering of medical, scientific, and other information that allows emergence to be identified. In the United States, this role is filled to a great extent by the Centers for Disease Control and Prevention (CDC). In addition to providing information on known foodborne pathogens, CDC works with local public health agencies and the medical and scientific communities to investigate new disease syndromes and identify unrecognized foodborne pathogens. This type of intelligence gathering played a pivotal role in the recent recognition of Cyclospora as a cause of foodborne gastroenteritis. CDC's new sentinel site program, FoodNet, is expected to greatly enhance the identification of new foodborne diseases. However, these surveillance activities are largely limited to the United States, whereas an effective intelligence system for foodborne disease must be worldwide. For example, Cyclospora was identified as a likely foodborne or waterborne pathogen in Asia and South America before an outbreak was reported in the United States. Intelligence related to foodborne disease can be acquired from several sources: the World Health Organization's surveillance program, the U.S. military's international network of laboratory and medical investigators, medical and scientific reports, and the Internet. The Internet is increasingly an important source of intelligence related to emerging pathogens; through news groups and bulletin boards such as ProMed, scientists and public health practitioners share their experiences on almost a real-time basis. Such advances in intelligence gathering are critical to reducing the time between emergence and control. However, limiting intelligence to medical considerations is not enough: intelligence gathering must include awareness of changes and advances in food production methods, agricultural practices and conditions, veterinary medicine, environmental and water microbiology, food technologies, consumer trends, and general socioeconomic conditions. The second component of contingency planning is ensuring sufficient personnel and facilities to characterize a new biologic agent and develop control strategies. The inability to predict the agent or the associated food, coupled with the degree of specialization required of investigators, requires a broad range of capabilities and resources. However, no one organization is likely to maintain the capabilities needed to deal with all contingencies. If we were to follow the military pattern, we would have reserve groups that could be mobilized as needed. However, even this approach requires planning and support to ensure the needed expertise and facilities. For example, the number of researchers and laboratories studying Clostridium botulinum has dropped to a point where it would be difficult to rapidly mobilize a research team, despite this pathogen's history of reemerging in a surprisingly wide range of foods. Rapid mobilization of resources is the third component. This component is particularly important for free-living infectious agents because one goal is to limit their dissemination to prevent them from establishing secondary reservoirs. It is much easier to fight a small, contained war than a global one. The mobilization of resources to respond to an emergence must be appropriate to the severity of the threat. Overreacting hurts the credibility of the entire system, while underreacting increases both the public health and economic impact. Rapid response efforts have focused at identifying new agents and removing suspect food from the marketplace, two key initial steps. However, research to prevent another occurrence of the emerging pathogen has been much less organized and timely. The fourth component of contingency planning, strategic planning, is actually the first chronologically. This is the phase where members of war colleges pose "what we would do if" scenarios and plan appropriate responses. This type of contingency planning has generally received attention in relation to emerging pathogens only in connection with the use of biologic warfare agents. This process relies on futurist thinking to consider how changes in society, economics, technology, agriculture, medicine, and international trade may affect the microbiologic safety of the food supply. Such a broad view is needed because more general events or trends in society cause most disease emergence. This type of strategic planning is undertaken with the realization that the probability of any specific "what if" scenario is low, but the probability that one scenario will materialize is extremely high. Research Needs Research, an integral part of responding to a new foodborne microbial threat, is the key for moving a new or reemerging biologic agent from being an unknown pathogen to being one for which control measures are available. Two areas of research can be classified on the basis of time constraints. Acute research needs are deficiencies in knowledge that must be addressed to establish control of an emerging pathogen. This research is highly targeted and specific for the microorganism and food of concern; it must be accomplished as quickly as possible. Acute needs generally require applied research, although basic research may have to be conducted if the deficiencies in knowledge are great. The second class encompasses longer-term basic and applied research needs not mandatory to immediate control. Acute Needs While the data needed for any single emerging biologic agent are highly specific, acute research needs fall into general categories that are virtually the same for all new pathogens. Common research questions include the following: Are methods available for detecting and categorizing the agent? What food is the vehicle for the pathogen? How do the implicated foods become contaminated? What is the pathogen's reservoir in nature? Is the pathogen's presence in contaminated food the result of an error or breakdown in normal controls? Does the pathogen grow in foods? Does the pathogen survive normal food processing, distribution, and preparation? How infectious/toxigenic is the pathogen? Are there subpopulations of consumers at increased risk for this pathogen? Is the pathogen's ability to cause disease restricted to specific strains with identifiable virulence characteristics? Answering these questions requires specific data that do not differ substantially from pathogen to pathogen (Table). Table. Research data needed for most emerging foodborne pathogens. ------------------------------------------------------------------- Research Area Knowledge gaps ------------------------------------------------------------------- Sampling and enrichment techniques Cultivating Biochemical/taxonomic char. Antibodies for capture and differentiation Detection methods Subtyping Virulence-associated char. Detecting injured or viable-but-nonculturable cells Contaminated foods Reservoirs and routes of transmission Life cycles Microbial ecology Geogr. range and seasonality Route of contamination and location of pathogen in food Dis. char. and diagnosis Sequelae Pathogenicity Host range Infectious dose Subpopulations at risk Animal models Free-living vs. obligate parasite Growth Growth requirements characteristics Temperature pH Water activity Oxygen Heat resistance D-values Z-values Survival Susceptibility to antimicrobial food characteristics additives Acid resistance Sensitivity to disinfectants or dessication Sensitivity to radiation UV Ionizing Effectiveness of food preservation Control Inspection systems to segregate contamination materials ------------------------------------------------- The criteria for classifying needs as acute are reasonably straightforward: Is the research needed to prevent a recurrence of the disease or to modify current HACCP plans? However, these questions have different priorities, which depend on when the information is needed. To deal with emerging pathogens, we should learn from modern business practices, especially the concept of "just-in-time" research. Little consideration has been given to how to assess and set research priorities for emerging foodborne pathogens. One attempt was provided as an appendix of the U.S. Pathogen Reduction Task Force. A relatively simple decision tree used a series of questions to identify what research was the limiting step in responding to the foodborne pathogen (4). The timeliness of addressing research needs must be an integral part of the planning process, but has been generally overlooked. Past research mobilization efforts for new foodborne microbial threats can be best described as haphazard, likely because they reflect the way research is funded. The traditional means of ensuring strong research programs, competitive funding of projects after proposals have undergone extensive peer review, is time-consuming and often not appropriate for the acute phase of responding to an emerging foodborne pathogen. Further, the peer-review process tends not to select the often mundane research needed during the acute phase of an emergence. Two alternative approaches may be more effective. The first is to have a series of designated laboratories that have as part of their mission and funding the task of being able to modify their research programs to address acute research needs. Such laboratories would need to have a critical mass of facilities and expertise in various aspects of food safety microbiology. The second approach is to have a group of reserve scientists with unique expertise or access to facilities not available at the designated laboratories or needed to supplement those capabilities. Funds could be earmarked to noncompetitively fund such reserve scientists on an as-needed basis, with the understanding that research needs designated as acute would take precedence over other research needs. Longer-Term Needs The three areas of longer-term research associated with emerging pathogens are amenable to more traditional funding. The first area, specific to the new pathogen, consists of research for improvements or alternatives to the detection and control methods initially devised. With initial disease control established, basic and applied research can seek to understand the microorganism and develop more optimal approaches for its prevention, control, or elimination. The second area concerns activities to help reduce the time between the emergence of a pathogen and its initial control (e.g., improved surveillance through the development of new diagnostic methods and further identification and characterization of virulence determinants and modes of pathogenicity to accelerate detection of new agents). Just as important as acquiring research data is rapid data dissemination. The continuing development of computer-based information networks is a component of this second research area. The third area focuses on identifying research factors that will allow new microbial threats to be anticipated. Of necessity, the current response to emerging pathogens is almost entirely reactive. The public health community detects a new syndrome, and only then is research-mobilized, often during a crisis. While reactive response will always be part of dealing with emerging microbial threats, a more proactive approach is needed if prevention is to be even partially realized. In military terms, war is the last resort and represents the failure of diplomats to predict and prevent a crisis. Microbial threats, like wars, do not spontaneously emerge but are the result of a series of events or conditions. There is a need to reexamine how food is produced, processed, marketed, and prepared to identify conditions that contribute to emergence. For example, organic acids are used extensively throughout the food industry to control spoilage and pathogenic microorganisms. Archer (5) hypothesized that over time, exposure to pH conditions that stress but do not kill may lead to the emergence of hardier and possibly more virulent foodborne pathogens. It is already well established that the induction of acid tolerance can enhance both the survival and virulence of foodborne pathogens (6). Further, one of the basic tenets of microbial genetics is that conditions that kill most, but not all, of a bacterial population foster the development of resistance. This is supported by recent studies that suggest that bacterial stress responses may select for hypermutability (7,8). While these findings do not mean that organic acids should not be used as a tool for controlling foodborne pathogens, they suggest that proactive research should be conducted to find ways of using these agents that minimize the potential for resistance. Proactive research, including research that might appear unrelated to the emergence of foodborne pathogens, can draw on the already substantial body of basic research related to the conditions and requirements for gene transfer among biologic agents. For example, Baur et al. (9) reported on the conditions that led to the competence of Escherichia coli for genetic transformation in freshwater environments. Maximal competence occurred when the bacterium was exposed to 2 mM Ca2+ as temperatures increased from 10°C to 20°C. With such information, researchers could examine food processing operations to determine the presence and importance of such conditions. For example, fruits and vegetables are often treated with calcium under fluctuating temperatures to enhance the texture during later processing. A key to being more proactive in addressing the threat of microbial foodborne pathogens—consideration of root causes—will likely require food microbiologists to become involved in nontraditional research areas. If new biologic agents arise as the result of changes in technology, society, or global economics, predicting and preventing emergence will ultimately require better understanding of how such factors influence pathogen introduction and dissemination. Conclusions One of the critical lessons of the past 10 years is that we cannot become complacent about infectious diseases (1). Only a few diseases (e.g., smallpox) have actually been eliminated. The rest, including virtually all foodborne diseases, we hold in check, winning battles but not the war. Eventually, our weapons (e.g., antibiotics) become obsolete; pathogens (e.g., E. coli) become more dangerous; or we become complacent. Contingency planning must be developed and undertaken with a long-term commitment. Without that commitment and without understanding that planning is successful when problems are avoided or minimized, programs of this type lapse quickly. In the long term, the costs of planning, both in terms of economics and human suffering, are a fraction of those incurred as the result of the emergence of a major microbial threat. Address for correspondence: Robert L. Buchanan, USDA ARS Eastern Regional Research Center, 600 East Mermaid Lane, Wyndmoor, PA, 19038 USA; fax: 215-233-6445; e-mail: rbuchanan@arserrc.gov. References 1. Lederberg J, Shope RE, Oaks S. Emerging infections, microbial threats to health in the United States. Washington (DC): U.S. National Academy of Sciences Press; 1992. 2. Nathanson N. The emergence of infectious diseases: societal causes and consequences. American Society of Microbiology News 1996;62:83-8. 3. Potter ME. Factors for the emergence of foodborne disease. In: Amgar A, editor. Food Safety `96: Proceedings of the 4th ASEPT International Conference. Laval, France: ASEPT; 1996:185-95. 4. United States Department of Agriculture. Subcommittee report for the pathogen reduction taskforce: identifying research and education needs. Washington (DC): USDA Food Safety and Inspection Service; 1994. 5. Archer DL. Preservation microbiology and safety: evidence that stress enhances virulence and triggers adaptive mutations. Trends in Food Science Technology 1996;7:91-5. 6. Foster JW. Low pH adaptation and the acid tolerance response of Salmonella typhimurium. Crit Rev Microbiol 1995;21:215-37. 7. Moxon ER, Rainey PB, Nowak MA, Lenski RE. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 1994;4:24-33. 8. LeClerc JE, Li B, Payne WL, Cebula TA. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 1996;274:1208-11. 9. Baur B, Hanselmann K, Schlimme W, Jenni B. Genetic transformation in freshwater: Escherichia coli is able to develop natural competence. Appl Environ Microbiol 1996;62:3673-8. --------------------------------------------------------------------------- Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA URL: ftp://ftp.cdc.gov/pub/EID/vol3no4/ascii/buchanan.txt [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Special Issue Impact of Changing Consumer Lifestyles on the Emergence/Reemergence of Foodborne Pathogens Janet E. Collins American Meat Institute, Arlington, Virginia, USA --------------------------------------------------------------------------- Foodborne illness of microbial origin is the most serious food safety problem in the United States. The Centers for Disease Control and Prevention reports that 79% of outbreaks between 1987 and 1992 were bacterial; improper holding temperature and poor personal hygiene of food handlers contributed most to disease incidence. Some microbes have demonstrated resistance to standard methods of preparation and storage of foods. Nonetheless, food safety and public health officials attribute a rise in incidence of foodborne illness to changes in demographics and consumer lifestyles that affect the way food is prepared and stored. Food editors report that fewer than 50% of consumers are concerned about food safety. An American Meat Institute (1996) study details lifestyle changes affecting food behavior, including an increasing number of women in the workforce, limited commitment to food preparation, and a greater number of single heads of households. Consumers appear to be more interested in convenience and saving time than in proper food handling and preparation. Reporting of foodborne and waterborne diseases in the United States began more than 50 years ago (1). At that time, state and territorial health offices were concerned about the levels of morbidity and mortality caused by typhoid fever and infantile diarrhea; cases were to be investigated and reported. The underlying purpose of reporting was to obtain information regarding the role of food, milk, and water in outbreaks of intestinal illness to provide a basis for public health action. In 1923, the Public Health Service began publishing summaries of outbreaks of gastrointestinal illness attributed to milk; in 1938, it added summaries of outbreaks due to any foods. In 1966, the present system of surveillance of foodborne and waterborne diseases began to incorporate into an annual summary all reports of enteric disease outbreaks attributed to microbial or chemical contamination of food or water. Comprehensive surveillance should result in greater awareness of the most important food-protection methods. Between 1983 and 1987, the etiologic agent in foodborne disease outbreaks was not determined in 62% of the outbreaks (2); between 1988 and 1992, the foodborne disease was of unknown etiology in 59% of the outbreaks (1). Bacterial pathogens caused the largest percentage of outbreaks (79%) when etiology was known—Salmonella caused 69% of bacterial outbreaks. For each year from 1983 through 1992, the most commonly reported food preparation practice that contributed to foodborne disease concerned improper holding or storage temperatures. The second most common practice was poor personal hygiene of the food handler. Food from unsafe sources was the least commonly reported factor in each of the 10 years of reporting. It is now time to examine food handling and determine how to reverse the trend. Foodborne disease surveillance has traditionally served three purposes. The first is disease prevention and control. Prevention and control measures include early identification and removal of contaminated products from the commercial market and correction of faulty food-preparation practices in both food-service establishments and the home. Surveillance also provides knowledge of disease causation. The responsible pathogen is not identified in more than half of the foodborne disease outbreaks for various reasons, including late initiation of laboratory investigation, inability of available technology to identify the pathogen, and lack of identification of the pathogen with a particular food. Finally, surveillance assists in administrative guidance. Information enables assessment of trends in prevalence of outbreaks caused by specific etiologic agents and in vehicles of transmission. This information assists in identifying common errors in food handling. In July 1995, the Centers for Disease Control and Prevention (CDC), Food and Drug Administration (FDA), and Food Safety and Inspection Service (FSIS) began a comprehensive effort to track major bacterial pathogens that cause foodborne illnesses (3). CDC provides the overall management and coordination with state health departments in the five survey sites of the FSIS/CDC/FDA Sentinel Site Study. The program actively seeks out specific cases of foodborne illness to identify whether a food was of concern and to better establish frequency and source of foodborne disease outbreaks and cases. CDC will use the data to identify emerging foodborne pathogens and monitor incidence of foodborne illness; FSIS will use the data to evaluate the effectiveness of new food-safety programs and regulations to reduce foodborne pathogens in meat and poultry; FDA will use the data to evaluate its efforts to reduce foodborne pathogens in seafood, dairy products, fruits, and vegetables. According to a recent report to Congressional committees (4), experts believe that the risk for foodborne illness is increasing. The food supply is changing in ways that can promote foodborne illness, and there are no comprehensive data to explain at what point pathogens are introduced into food. Further, because of demographic changes, more people are at a greater risk of contracting a foodborne illness. According to Ollinger-Snyder and Matthews (5), changes in agricultural practices, a growing population susceptible to infectious diseases, lifestyle changes, the emergence of new foodborne pathogens, and the high turnover rate reported for workers in the food-service industry indicate that new approaches are needed to allay consumers' fears and to prevent the spread of foodborne disease in the United States. They recommend implementation of Hazard Analysis and Critical Control Points (HACCP) systems and certification of food-service managers. The food processing industries are developing and implementing HACCP systems; the meat and poultry industries are mandated to do so beginning in January 1998 (6). Hazard analysis has been defined as the identification of sensitive ingredients, critical processing points, and human factors that affect product safety. Critical control points have been described as processing determinants whose loss of control would result in an unacceptable food-safety risk. Most contend that the HACCP system approach must be implemented at each stage of the farm-to-family continuum. Where are the critical control points and the HACCP system development in the home, food-service or retail establishments, or the car when food is carried from one location to another? The consumer is a complex and critical control point in the process. Take the case of the barbecued chicken served to 260 guests at an outdoor barbecue in 1983. Guests were served chicken that was parboiled in the morning by one set of cooks and then placed in a large container and refrigerated. The evening cooks assumed the chicken had been adequately cooked, so they basted it in barbecue sauce and warmed it over the fire. Some 71% of the guests got sick from the chicken that was insufficiently cooked and improperly held (5). What of the infected bakery worker who stirred a vat full of buttercream frosting with a bare hand and arm? Some 5,000 cases of viral gastroenteritis were caused by the infected worker who claimed he had washed his hands. Other more recent outbreaks (7) appear in Table 1. Table 1. Foodborne illness reports from restaurants, 1996 ------------------------------------------------------------ Date Description Cause ------------------------------------------------------------ Employees did not 6/96 Salmonella-contaminated wash hands food, 38 cases before handling food Escherichia Raw food 9/95 coli O157:H7 cross-contaminated "beef," 11 cases other Salmonella newport Raw meat on 8/95 "chicken," >850 cuting cases board with vegetables Hepatitis A, Human fecal 1/95 contaminated food, matter from 95 cases handling-handwashing Salmonella, Holding 8/94 hollandaise sauce, temperature 56 cases too low for 9 hours Clostridium Unrefrigerated 1/93 botulinum, canned storage of cheese sauce, 7 opened cases, 1 death container ------------------------------------------------------------ Source: Center for Science in the Public Interest, 1996 Recent data (1) indicate that 80% of reported foodborne illness outbreaks occur outside the home. Even though illnesses would be expected to be reported more often when they occur as a result of eating in restaurants, the numbers are large. National standards for restaurant safety are contained in the Food Code (8). FDA has the legal authority to impose the standards on state and local jurisdictions. The Food Code, which is updated every 2 years, includes temperatures for cooking, cooling, refrigeration, reheating, and holding food in food-service establishments. County or city employees are generally charged with responsibility for inspecting restaurants; each state or locality has its own laws governing restaurant safety. Food service outside the home is big business, with sales of more than $300 billion (9) and nearly 10 million employees. The restaurant industry's share of the food dollar is 43%, and the typical consumer more than 8 years of age had more than four meals per week away from home in 1996. Given those statistics, it is clear that food-service establishments play a critical role in food safety. The Center for Science in the Public Interest (7) conducted a survey of 45 agencies across the country to determine if state and local agencies were enforcing 12 key food-safety standards in the FDA Food Code. The standards chosen for the study affect consumer health and safety and include such areas as food cooking and refrigeration temperatures, frequency of inspections, and consumer warnings for raw foods. Not one of the 45 agencies surveyed was following all of the Food Code recommendations. In the survey, only 13% of agencies enforced the Food Code and recommended cooking temperatures for pork, eggs, fish, and poultry; only 64% of agencies required hamburgers to be cooked to 155°F. Recommendations for cooling cooked food were followed by only 20% of the agencies, and only 11% required refrigeration of food at FDA-recommended temperatures. Every restaurant can take steps to ensure the safety of the food it prepares and serves to its customers. Continuous employee training and institution of HACCP-type systems should assist restaurants and other food-service institutions in improving their food-safety records. Programs available through the national restaurant trade organization could assist even the smallest establishments in achieving food-safety goals. For more than 25 years, the Food Marketing Institute (10) has surveyed consumers about their changing needs and priorities in food attitudes and behavior. The 1996 trends report has an expanded focus on the primary grocery store or supermarket, including questions to help retailers learn more about take-out foods (Table 2). In 1996, nearly 40% of the 2,000 shoppers surveyed purchased fresh deli items from their primary supermarket at least once per week, and more than 10% reported purchasing ready-to-eat take-out foods as frequently. Three-fourths of these shoppers purchased food from the deli at least once per month, and half bought take-out food from the supermarket as often. Table 2. Sources of take-out food (%) --------------------------------------------------------------------------- Source 86 87 88 89 90 91 92 93 94 95 96 --------------------------------------------------------------------------- Fast-food restaurant 43 44 41 41 46 51 55 46 46 41 48 Restaurant 38 33 38 33 27 23 24 27 25 22 25 Supermarket 10 9 11 12 14 14 12 15 15 17 12 Deli/pizza parlor/bagel shop/coffee shop/ donut shop * * * * * * * * * 8 4 Gourmet or specialty shop * * * * * * * * * * 3 Convenience store * * * * 2 2 2 2 2 2 1 Some other place 2 7 3 6 2 1 * 1 1 1 2 It varies 1 1 1 3 4 5 3 5 3 2 0 Don't eat out * * * 7 6 4 4 4 4 3 2 Not sure 3 3 4 1 * 1 1 1 2 3 2 --------------------------------------------------------------------------- *Data not collected for this year. Source: Food Marketing Institute, 1996 According to the survey, fast-food restaurants dominate (48%) all food outlets as the primary source of take-out food; only 12% purchase take-out foods from the supermarket. A recent article in Food Processing Magazine (11) states, "Somewhere on their way to the supermarket, consumers have been getting lost." Home-meal replacement, ready-made meals approximating what Mom used to make, have begun to rapidly compete for the food dollars of time-pressed consumers. According to Hollingsworth (12), consumers are eating more meals at home, but they are not cooking more. Consumers want to get food in a take-out location and go home to eat it (Figure). [Figure not available in ASCII] These take-out or eat-at-home foods have built-in food-safety hazards. Consumers are time-pressed, and they are buying these foods. Are they treating them as perishable? The U.S. Department of Agriculture (13) has expressed concerns about these foods; they say that take-out foods need to be handled with care. Hot foods need to be picked up or received hot and eaten within 2 hours. If eaten later, hot foods should be divided into shallow containers, covered loosely, and refrigerated immediately. Are consumers ready for all of this food handling? Most consumers are confident that the food they purchase is safe to eat (10). Spoilage of foods is considered the greatest threat to food safety by the largest group (49%) of respondents. They count on freshness and expiration dates (22%) and increasingly see bacteria and contamination as threats (17%). It is interesting to note, however, that between 1992 and 1996 these shoppers were less likely (15% vs. 7%) to see spoilage as a threat; similarly, processing and preparation of foods was less an issue in 1996 than in 1992 (8% vs. 10%). Consumers are concerned about handling of foods by other shoppers and by supermarket employees. Consumers rely increasingly on food stores (16%), manufacturers (21%), government (21%), and themselves (25%) for food-safety protection. Consumers apparently are willing to share responsibility for food safety with others, but they want to know that steps are taken during the processing and distribution of foods to reduce the likelihood of pathogen or other bacterial contamination. According to Technomics (14), these supermarket issues noted in the Food Market Institute trends data (10) will be shared with food-service operators as the share of consumer food expenditures changes from 51% vs. 49%, 48% vs. 52%, and 45% vs. 55% (projected) for retail expenditures versus food-service expenditures in 1991, 1996, and 2001, respectively. The number of households earning more than $75,000 annually continues to grow, and these households exhibit the highest levels of spending on food service. Consumer demands are changing the way that food-service operators and suppliers of food services must react. The area of convenience, highly prized by consumers today, has profound implications for food. Consumers want fast service with easy-to-eat foods and no stress, which means a far greater emphasis on portable foods. Technology has conditioned us to demand and receive near-immediate satisfaction. There will be even greater emphasis on faster service, meaning more emphasis on convenient food formats to expedite preparation. Packaging and storage will greatly affect product quality and safety. According to Technomics (14) packaging will need to be temperature-tolerant and breathable. Preparation and processing technologies will need to have greater ability to rapidly cool and chill. And then there is the food-safety concern associated with dispensing equipment. Food will be required to have an extended shelf-life. The safety factors associated with these new formats will also change. Consumers want easy access to portable foods. Accessibility to variety in food options translates to a proliferation in nontraditional locations. These smaller sites may include back-of-house preparation facilities. This easy access to smaller operations also suggests a need for more of such operations and more variety in menu options. While to the consumer this may translate to upscale menus with indulgence foods such as new and different bakery items, microbrewery beverages, and gourmet coffees, to the food-service operator it may mean greater cross-contamination with cream fillings, unpasteurized fermented drinks, and spoiled milk. New menu options create new challenges for service and for safety. According to Steve Harrison, brewmaster of the Sierra Nevada Brewing Company (Chico, CA), "The concept that a beer will automatically go bad in `X' number of days is a very untrue one." Consumers do not know that. What is "skunky beer"? Starting in late 1996, Anheuser-Busch began a freshness strategy in their advertising. Other large brewers are catching on, so freshness is associated with quality and safety. Imagine freshness dating, "born-on dating," as a quality parameter in brewing. Consumers' increased emphasis on food-safety issues directly affects food service. The perceived healthfulness and quality of foods affects food sales; the increasing considerations of cleanliness as healthfulness and quality as safety become even greater shared responsibilities as food-service operators take over the roles historically associated with home kitchens. "On-the-spot exhibition" cooking is of increasing interest to today's consumers. In June 1996, the Food Marketing Institute (15) published a review of foodborne illness. They note that the organisms that cause foodborne illnesses are found throughout nature and that mishandling and poor refrigeration are responsible for most contamination. The most common causes are cross-contamination of cooked foods with raw foods, contaminated utensils or serving plates, poor hygiene of food handlers, and time or temperature abuse. Agreement is widespread that the most serious food-safety problem is foodborne illness of microbial origin (Table 3). Foodborne pathogens include a wide array of microorganisms, which have various physiologic effects on people, ranging from mild to severe, and are associated with a wide array of foods. Cross-contamination and association of foods within mixed dishes complicate environmental control. Further, some of the microbes have evolved and become more resistant to food preparation and storage techniques. Several industry and government publications (1,2,8,15,16) summarize biologic hazards associated with foodborne illness. Table 3. Sources of reported outbreaks with confirmed causes (%) ---------------------------------------------------- Restaurant Other Known Place 1983- 1988- 1983- 1988- 1996 87 92 87 92 ---------------------------------------------------- Salmonella 50 60 46 58 30 Escherichia coli <1 <1 2 1 5 Hepatitis A virus 6 7 3 4 Staphyloccus aureus 2 3 10 5 Campylobacter 1 2 6 3 45 Shigella 8 2 6 2 17 ---------------------------------------------------- Sources: Centers for Disease Control and Prevention and U.S. Department of Agriculture for 1996, the 1996 Sentinel Site Study Mishandling can occur at any point in the food chain—in processing, at supermarkets or restaurants, or in homes. Many food manufacturers and retailers have HACCP plans in place, and over the next few years that number will increase. Consumers, however, must assume responsibility for the safety of food in the home. Proper preparation and sanitation methods are key to preventing foodborne illness in the home as in other areas of food handling. The messages for each of the segments of the food chain are the same—keep it clean (e.g., wash your hands) and control the temperatures (keep hot things hot and cold things cold) (Table 4). Table 4. Pathogen control in foods to reduce foodborne illness ---------------------------------------------------- Pathogen Control mechanism ---------------------------------------------------- Campylobacter Heat foods >= 140°F Proper handling Rapid chilling <40°F Salmonella Hot storage >140°F Cooking >165°F Escherichia coli O157:H7 Heat foods >155°F Avoid cross-contamination Staphylococcus aureus Rapid cooling <40°F Personal hygiene Clostridium botulinum Boil food 10-15 minutes Clostridium perfringens Refrigerate <40°F Proper handling Listeria Pasteurization of milk Adequate cooking ---------------------------------------------------- Source: Food Marketing Institute, 1996 For the food-service industry, a number of programs have been developed to educate food handlers about food-related and personal behaviors that affect the safety of foods. For example, the Food Marketing Institute (17) has a Food Protection Certification Program for supermarket personnel to learn about the FDA Food Code requirements regarding food handling and hygiene. Similarly, the National Restaurant Association has developed a food-safety program called Serve Safe, intended to educate food-service workers about safe food handling. Who or what teaches the average consumer about food safety? Common sense? Family? Health and fitness magazines? In May 1996, the Food Marketing Institute (17) conducted a series of consumer focus groups to establish the importance of food safety to consumers and to identify barriers to consumers' safe food purchase, handling, and preparation. They report that how consumers manage food safety reflects years of conditioning, observation, and reinforcement from mothers and grandmothers. In some cases, the more often consumers shop, the less concerned they seem to be about food safety when it comes to shopping, storage, and handling. Consumers link safety to fresh food, and they assume that when they shop more often, they purchase food in smaller quantities and food safety is less an issue. Respondents in the study also tended to think that cooked food was generally "safer" than raw food. For example, they believed that recontamination of unrefrigerated food was less a problem with cooked than with raw food. Some safe food practices are observed for convenience, esthetics, or taste rather than for food safety. Thawing meat is messy; covering food prevents it from drying out; separating foods in the refrigerator is tidier. These kinds of behavior improve safety, but consumers may not understand the food-safety implications. Overall, the consumers in the Food Marketing Institute study (17) find food-safety messages generally are "common sense," "basic," "practical," and "believable." Messages about such subjects as the order in which to choose foods in the supermarket, sell-by dates, storage and freezing of products, ways of keeping hot foods hot and cold foods cold are not considered too elementary. They also believe that storage times for food safety do not apply equally across food groups; they do not understand hazards from vegetables or fruits. Barriers to safe food-handling behavior in this study included historical (and cultural) practices, feeling of invulnerability, taste preferences, timing and planning, and space and convenience. A 1992 survey conducted at Cornell University and designed to assess consumer food-safety awareness documented a substantial lack of knowledge about safe home food preparation practices. Seventy-five percent of those surveyed knew that Salmonella is associated with meat, poultry, and eggs, but only 65% would refrigerate a roasted chicken breast immediately; 29% would leave it on the kitchen counter until it reached room temperature. Further, 18% said they would not be concerned or were not sure about the safety of cooked meat left unrefrigerated for more than 4 hours; 14% said the same for cooked poultry. In April 1996, the American Meat Institute (16) commissioned a study of 1,000 adults in the United States. Compared with 98% of respondents in the study who know that harmful bacteria can be present on meat and poultry products, only 74% made the link to dairy products and eggs; two in five respondents (43%) recognized that fruits and vegetables may contain harmful bacteria. These conclusions could be drawn for consumers who responded to the American Meat Institute (1996) questions. While the U.S. population is growing (up 10% since 1980), households are becoming smaller. In the 1980s, the number of households grew 17%, while the average household size decreased from 2.8 to 2.6 persons. This shift in family size and the increase in single heads of households has resulted in increased stress in the family with less time for shopping and food preparation. In addition, more women are in the workforce. Today, 70% of women ages 25 to 44 years are in the workforce; 75% work full time. Therefore, no adult is likely to be in the home for 70% of American households, and many children are preparing food for themselves. Finally, consumers spend less time on food preparation. More than 85% of employed women shop and cook, but most spend less than 30 minutes preparing every meal and 20% spend less than 15 minutes. Consumers are using convenience foods and quick methods of food preparation, including partially cooked foods that may require special handling. The study results provided further documentation that the risk for foodborne illness is increasing, largely because of societal changes that affect the way consumers purchase and prepare food. Contributing to this are changes in the family structure, more women in the workforce, and less available time for food preparation. Consumers in this study were not able to correctly separate home preparation issues from food service, nor did they know correct cooking temperatures to use in their own homes. The ways in which consumers spread microorganisms to one another and to themselves include more than just coughing and sneezing. Not washing hands before, during, and after handling foods clearly contributes to the spread of foodborne infections and intoxication. Hands can spread disease-causing microbes to foods from other foods and from infected persons. In a comprehensive review of 91 scientific articles published after 1986, Bryan et al.(18) attempted to link hand washing and infections. They report that hand washing has become an integral component of the tradition and ritual of prevention practice for the spread of infection, but several factors confound the ability to establish the effectiveness of hand washing for reducing infectious disease. Hand-washing practices were shown to significantly reduce infections transmitted by the fecal-oral route and in situations of poor personal hygiene. Hand washing is clearly a critical step in reducing personal contamination of food and cross-contamination between foods. Hand washing is but one practice that could dramatically affect risk, if not incidence, of foodborne disease. According to data provided by the American Society for Microbiology (19), people do not wash their hands as often as they think they do (Table 5). In telephone surveys, 94% of respondents claim they always wash up after using the rest room; however, researchers contend that almost one-third of people do not wash their hands after using the bathroom. Of the more than 7,000 people nationwide who participated in the study, 81% said they wash their hands before handling or eating food. However, most say they do not wash up after petting an animal (48%), coughing or sneezing (33%), or handling money (22%). Table 5. American Society for Microbiology/Bayer handwashing survey, 1996 -------------------------------------------------------- What they What they Behavior/Location: say(a) (%) do(b) (%) -------------------------------------------------------- Wash hands: After using public restroom 94 68 Women 74 Men 61 New York (Penn Station) 60 Chicago (Navy Pier) 78 New Orleans (casino) 71 San Francisco (Golden Gate Park) 69 Atlanta (Braves game) 64 Women 89 Men 46 -------------------------------------------------------- (a)1,004 adults; (b)6,330 adults Source: American Society for Microbiology In early 1997 (8), the U.S. Departments of Agriculture and Health and Human Services and the U.S. Environmental Protection Agency developed a program intended to coordinate a food-safety initiative among federal agencies, immediately after an announcement by U.S. President Clinton (January 1997) to promote an initiative designed to improve the safety of the nation's food supply. The president charged the federal agencies to work with consumers, producers, industry, states, tribes, universities, and the public to identify ways to improve food safety through government and private sector action, including public-private partnerships. The interagency response is a multifaceted program designed to include surveillance, coordination of activities within the various programs and agencies, risk assessment, research, inspections, and education. The underlying premise upon which this program was developed is that foodborne infections remain a major public health problem. Further, sources of food contamination are said to be almost as numerous and varied as the contaminants; bacteria and other infectious organisms are pervasive in the environment. The current systems for protecting food in the United States include a broad range of government agencies and industries, many of which have been discussed in this paper. Responsibilities are shared among the U.S. Department of Agriculture (Food Safety and Inspection Service and Animal and Plant Health Inspection Service), the U.S. Department of Health and Human Services (FDA and CDC), and the U.S. Environmental Protection Agency. These responsibilities include oversight on the farm, in the processing facilities, during transportation and distribution (including food from foreign countries), and in food marketing channels including restaurants, supermarkets, and institutional food services (such as schools and hospitals). Surveillance of foodborne illness outbreaks and their causes is a responsibility of FDA and CDC. Education is shared among the agencies and is not the primary concern or responsibility of any one of the agencies. Pivotal to this new initiative is the element of education. Specifically, the program is intended to reinvigorate education of all those involved in food preparation, focusing on the use of safe practices. According to USDA et al. (8), educating people about steps they must take to prevent and control foodborne illness is a vital link in the food preparation chain. In spite of the education efforts of the government, both state and federal, consumer groups, and industry, which have occurred historically, foodborne illness occurs from a lack of knowledge of the risks involved at all stages of food preparation. Choices consumers make about how they handle food at home and about eating food that increases the risk for illness can have an important effect on foodborne disease incidence. USDA et al. (8) will develop a program to improve consumer education; retail, food service, and institutional education; veterinary and producer education; and industry education in the transportation area. They propose developing an alliance among industry, consumer groups, and governmental agencies to mount a comprehensive food-safety awareness campaign for consumers. Highly focused messages and tactics for the general public and consumers at high risk will be developed. This thrust is in perfect harmony with the strategies and tactics proposed by the American Meat Institute (16) as an outcome to a series of studies and roundtable discussions held with medical doctors, dietitians, educators, and others. The ability of industry and consumer groups to work with the government in a program with common themes and elements is critical to the positive outcome of the effort. As one of the focus group members in the Food Marketing Institute (17) said, the more often the message is repeated, the more likely is the listener to hear it. The broad-based approach to education, which includes data from surveillance and inspections, should provide the foundation for changes in consumer behavior. It is critical that consumers not only take responsibility for their actions regarding food safety, but that they also take seriously the learning that must occur for consumers of all ages to prevent contamination, cross-contamination, and mishandling of foods at home and in restaurants. Convenience, taste, and variety are welcome qualities in foods that we enjoy; safety in foods is critical to the public health and safety of consumers and to the government and businesses that support those consumers. Address for correspondence: Janet E. Collins, American Meat Institute 1700 N. Moore Street, Suite 1600, Arlington, VA 22209 USA; fax: 703-527-0938; e-mail: ami@interramp.com. References 1. Centers for Disease Control and Prevention. Surveillance for foodborne disease outbreaks, United States, 1988—1992. MMWR CDC Surveill Summ 1996;45:1-66. 2. Centers for Disease Control. Foodborne disease outbreaks, 5-year summary, 1983—1987. MMWR CDC Surveill Summ 1990;39:15-57. 3. Food Safety and Inspection Service. FSIS/CDC/FDA sentinel site study: the establishment and implementation of an active surveillance system for bacterial foodborne diseases in the United States. Washington (DC): USDA Report to Congress; 1997. 4. United States General Accounting Office. Food safety: information on foodborne illnesses. Report to Congressional Committees. Washington (DC): GAO/RCED-96-96; 1996. 5. Ollinger-Snyder P, Matthews ME. Food safety issues: press reports heighten consumer awareness of microbiological safety. Dairy, Food and Environmental Sanitation 1994;14:580. 6. FSIS Pathogen Reduction/HACCP. Washington (DC): Federal Register 1996 Jul 6. 7. Center for Science in the Public Interest. Dine at your own risk: the failure of local agencies to adopt and enforce national food safety standards for restaurants. Washington (DC): The Center; 1996. 8. United States Department of Agriculture, United States Department of Health and Human Services, United States Environmental Protection Agency. Food safety from farm to table: a new strategy for the 21st century. Discussion Draft. Washington (DC): United States Department of Agriculture; 1997. 9. National Restaurant Association. In: 1997 Restaurant Industry Pocket Factbook. Washington (DC): The Association; 1997. 10. Food Marketing Institute. Trends in the United States: consumer attitudes and the supermarket. Washington (DC): The Institute; 1996. 11. Neff J. Will home meal replacement replace packaged foods? Food Processing 1996;57:35. 12. Hollingsworth P. The changing role of fast food. Food Technology 1997;51:24. 13. United States Department of Agriculture, Food Safety and Inspection Service. Take out foods—handle with care. The Food Safety Educator 1996;1:2. 14. Management summary update: critical strategic issues 1996-2001. Chicago: Technomics, Inc.; 1997. 15. Food Marketing Institute. Backgrounder: foodborne illness. Washington (DC): The Institute; 1996. 16. American Meat Institute. Putting the food-handling issue on the table: the pressing need for food safety education. Washington (DC): American Meat Institute and Food Marketing Institute; 1996. 17. Food Marketing Institute. Food safety: a qualitative analysis. Washington (DC): The Institute; 1996. 18. Bryan JCL, Chorine J, Larson EL. Handwashing: a ritual revisited. Infection and Control in Critical Care 1995;7:617-24. 19. American Society for Microbiology. Americans get caught dirty handed. Fact Sheets. Washington --------------------------------------------------------------------------- Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA URL: ftp://ftp.cdc.gov/pub/EID/vol3no4/ascii/collins.txt [Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997] Special Issue Communicating Foodborne Disease Risk Baruch Fischhoff and Julie S. Downs Carnegie Mellon University, Pittsburgh, Pennsylvania, USA --------------------------------------------------------------------------- The food industry, like many others, has a risk communication problem. That problem is manifested in the public's desire to know the truth about outbreaks of foodborne diseases; ongoing concern about the safety of foods, additives, and food-processing procedures; and continued apathy regarding aspects of routine food hygiene. If these concerns are addressed in a coherent and trustworthy way, the public will have better and cheaper food. However, sloppy risk communication can itself cause public health damage. Because citizens are ill-equipped to discriminate among information sources, the food industry as a whole bears responsibility for the successes and failures of its individual members. We review risk communication research and practice for their application to the food industry. The guardians of the world's food supply face a communication challenge of extraordinary complexity. They need to be ready at short notice to deal with various crises, often involving baffling combinations of foods, pathogens, handling and distribution practices, dietary norms, and interactions with medical conditions and medications. Their response to this challenge may have important health, economic, and even political implications. Conflicting pressures may come from groups that bear the cost when the public health response is too swift or too slow. Quick, confident explanations are expected after outbreaks that may never be fully understood. When consumers (and producers) need information, they cannot wait for more research. Consumers can read between the lines, especially when they perceive their lives or livelihoods at risk. If they misread messages, the communicators may still be held responsible. Moreover, consumers know that silence is also a form of communication. At the same time, the guardians of the food supply must wage a continuing struggle to improve the handling of food. In the United States, campaigns are under way for cooking beef more thoroughly, separating raw meat from salad ingredients, and improving the sanitation of food handlers (e.g., Operation Clean Hands). To some extent, these campaigns are the incarnations of old messages that have not been communicated effectively. At the same time, the campaigns are responses to changes in the food supply that have increased the risks associated with conventional practices. For example, as the incidence or severity of foodborne disease pathogens increases, the effectiveness of customary food-handling practices decreases. This article briefly reviews risk perception and communication research as a possible resource for better understanding (and perhaps meeting) the public's needs (1-3). Communication research provides a set of general tools and theories, as well as a body of results, showing a complex picture of strengths and weaknesses in lay understanding of risk. We explore here the implications for anticipating public response to emerging foodborne pathogens and offer a proposal for how an effective communication campaign might be organized. Although risk communication research does not directly address emerging foodborne pathogens, it is compatible with the model of risk assessment that the food industry seems to be adopting (4). Drawn from the National Research Council's (5) volume, Improving Risk Communication, the model involves overlapping processes of assessing the magnitude of risks (through analytical procedures), managing their level (through practical measures), and communicating with the public about them. Like many other risks, emerging foodborne pathogens are of primary concern to some specialists but one more thing to worry about for ordinary citizens. The thought processes that people rely on for making decisions are the focus of much research (Table; 6). Table. Thought processes involved in decision-making --------------------------------------------------------------------------- People simplify. Many decisions require people to deal with more details than they can readily handle at any one time. To cope with the overload, people simplify. People want to know if foods are "safe," rather than treating safety as a continuous variable; they demand proof from scientists who can provide only tentative findings; and they divide the participants in risk disputes into good guys and bad guys. Such simplifications help people cope, yet also lead to predictable biases (7). Once people's minds are made up, it's hard to change them. People are adept at maintaining faith in their beliefs unless confronted with overwhelming evidence to the contrary. One psychologic process that helps people to maintain their current beliefs is underestimating the need to seek contrary evidence. Another process is exploiting the uncertainty surrounding negative information to interpret it as consistent with existing beliefs (8). People remember what they see. People are good at keeping track of events that come to their attention (9),(10). As a result, if the appropriate facts reach people in a credible way before their minds are made up, their first impression is likely to be the correct one. Unfortunately, it is hard for people to gain firsthand knowledge of many risks, leaving them to decipher the incomplete reports they get. People cannot readily detect omissions in the evidence they receive. It is unusual both to realize that one's observations may be biased and to undo the effects of such biases. Thus people's risk perceptions can be manipulated in the short run by selective presentations. People will not know and may not sense how much has been left out (11). What happens in the long run depends on whether the missing information is revealed by other experiences or sources. People may disagree more about what "risk" is than about how large it is. One obstacle to determining what people know about specific risks is disagreement about the definition of "risk" (12-15). For some risk experts, the natural unit of risk is an increase in probability of death; for others, it is reduced life expectancy; for still others, it is the probability of death per unit of exposure. If lay people and risk managers use the term "risk" differently, they may agree on the facts of a hazard, but disagree about its riskiness. How much does the public know and understand? The answer to this question depends on the risks consumers face and the opportunities they have to learn about them. The next section discusses strategies for improving those opportunities. ------------------------------------------------------------------------ Communicating Risk An overarching theme of risk communication is that people understand risks that draw their attention and are presented comprehensibly. Whether the public's attention is aroused spontaneously or as a result of a message, the opportunity must be seized. The right information must be selected and communicated appropriately (1,16,17). The hallmarks of effective communication should be used. Match the audience's level of technical sophistication. Do not talk down. Clarify terms (e.g., virus) that are used in everyday speech but not very precisely (e.g., risk). Organize information. Provide the audience with a quick logical overview. Make the desired level of detail easy to read. Use numbers to communicate quantities. Avoid ambiguous verbal quantifiers, such as "rare" or "likely". Ensure source credibility. Realize that messengers are a part of the message and essential to its interpretation. Use knowledgeable sources that will not misrepresent the message. Avoid risk comparisons with rhetorical implications. Comparing one uncontrollable accident risk with another, more familiar one (e.g., half as likely as being injured by lightning) can be useful; however, people dislike comparisons that imply they should accept one risk because they accept another, e.g., comparing the risks of nuclear power with those of eating peanut butter (from aflatoxin). However useful communication research may be, there is no substitute for empirical testing of messages. With heterogeneous audiences, any fixed message will work better for some people than for others. In such cases, universal understanding may require providing the opportunity for the public to ask questions through public information sessions, agricultural extension services, science teachers, or toll-free numbers. What To Say The effort to communicate is wasted if the information is not worth communicating, either because people already know it or because it makes no difference to them. Indeed, communication can backfire if consumers think that their time is being wasted with useless messages while they are being denied pertinent information. An analytical effort to determine what is worth knowing and a coordinated empirical effort to determine what people know already are required. These efforts take different forms in situations where consumers face well-formulated decisions and need only a few quantitative estimates before making choices, and in situations where consumers are trying to understand the processes creating and controlling a risk, in order to follow public discussion, devise decision options, or understand quantitative estimates. Identifying Relevant Estimates The tools of decision analysis provide ways to determine how sensitive well-structured choices are to uncertainty in different decision parameters (18,19). The more sensitive parameters should receive more attention, unless consumers know them already (and need no reminder). If conditions do not permit sensitivity analyses for individual decision makers, one can model the information needs of a population similar to the intended audience. Merz et al. (20) demonstrated this approach for communicating to carotid endarterectomy candidates. Scraping out the main artery to the brain reduces the probability of stroke for patients with arteriosclerosis. However, the procedure can cause many problems, including strokes. Decision analysis computed the attractiveness of surgery for a hypothetical population of patients, with a distribution of physical states (e.g., stroke risks) and values (e.g., time horizons). The analysis found that three of the potential complications (stroke, facial paralysis, and persistent headaches) posed sufficient risk that learning about them should dissuade about 30% of candidates from surgery. Learning about the other side effects should affect few additional patients. Therefore, physicians trying to secure informed consent should (while not hiding other information) make sure that patients understand the risks of these three complications. Identifying Relevant Processes Risk analysis provides one way to identify the critical processes in creating and controlling risks. Figure 1 shows a simple model for the risks of foodborne pathogens. It uses the formalism of the influence diagram (21,22). Such a model can be used both to assess risks and to characterize the comprehensiveness of lay understanding. In this model, people incur food-related risks as a result of decisions, which possibly lead to actions or exposures. These decisions concern such actions as eating a bite of suspicious food, choosing a particular diet, or opting for school (or home) lunch. Those decisions depend, in part, on the perceived risks of those actions as well as other nonrisk factors (i.e., other costs and benefits). Exposure may follow, if a pathogen is actually present; it can lead, in turn, to transmission of the pathogen and to changed health states, depending on the resistance to disease that the person's health provides. [Figure not available in ASCII] Figure 2 elaborates on this model. It shows that food pathogenicity depends on both the prevalence of pathogens in the environment and the quality of food handling. A person's own health influences risk perceptions through the intermediate variable of perceptions of health, which in turn is influenced by the person's history of food consumption (or avoidance). Actual pathogenicity influences risk perceptions through awareness, a variable that communicators might affect. Nonrisk factors include visceral factors (e.g., hunger), external social factors (e.g., social pressure to eat any food offered by a host), norms (e.g., not eating dog), and the expected benefits of consumption (e.g., taste, texture, and other gustatorial pleasures). Computing risks with this model would require specifying each variable and estimating the contingencies by using statistical sources or expert judgment. For risk communication purposes, even a qualitative model can define the universe of discourse and allow approximate estimates of the most important relationships (23). [Figure not available in ASCII] Identifying Current Knowledge Determining what people already know about quantitative estimates is relatively straightforward, although there are various pitfalls (24,25). Eliciting knowledge of processes is more difficult. Respondents should be given the focus of the problem and maximum freedom to express their ideas and reveal which of the processes in Figure 2 are on their minds. Studies using open-ended techniques often find that people speak the language of risk without understanding its terms. For example, in a study about radon, we found that respondents often knew that it was a colorless, odorless, radioactive gas that caused lung cancer. However, when pressed, respondents often revealed inappropriate notions of radioactivity, believing that anything radioactive would permanently contaminate their homes. Some told us that they would not test for radon because there was nothing that they could do if they found a problem (26). In studies with adolescents, we found other forms of false fluency; for example, teens used terms such as "safe sex" and "clean needles" without understanding them (23). Without open-ended probing, we miss misconceptions that a technical expert never would have imagined, or we use language that does not communicate effectively with our audience (27). Food Industry Communication Strategies Technical experts (in any industry) generally want to get the facts in order before saying anything. Although that is an appropriate norm within the scientific community, refusing to address a concerned public can evoke mistrust and anger, as can failing to arouse an apathetic public. To steer an appropriate course, communicators need an explicit policy that balances the risks of saying too much with the risks of saying too little. The policy must consider both what to say and when to say it. From a decision theory perspective, citizens need information critical to identifying actions that will help them achieve personal goals. As a result, any recommendations should reflect both scientific knowledge and citizens' values. That is, consumers need to know what is the best gamble, given the trade-offs between, for example, the risks of throwing out good food and the risks of eating food that might make them sick. At times, there may be a temptation not to tell it like it is. For example, one might argue that risks should be exaggerated when a frank report would leave people unduly apathetic, as judged by their own standards. That is, people should say "Thanks for getting my attention" once the grounds for the overstatement were made clear. Such gratitude requires a public that not only recognizes the limits of its own understanding, but also accepts paternalistic and manipulative authorities. That acceptance seems more likely for misrepresentations intended to get a complacent public moving than for ones intended to allay a hysterical public's fears. In either case, once the secret is out, all future communications may be subjected to second guessing ("How seriously should we take them this time?"). One situation in which paternalistic authority is needed arises when a single message must be sent to a heterogeneous audience—for example, when officials must decide whether to declare a particular food "safe." Safety is a continuous variable, and any cut-off represents a value judgment. For any given food, different groups may face different risks, derive different benefits, and want to make different trade-offs. For example, a few people are strongly allergic to sulfur dioxide as a dried food preservative. Marketing such foods signals their safety to all. Labels that declare preservatives in foods allow consumers to customize their risk levels, but only if they know their own risks (i.e., whether they are strongly allergic, which they may learn only through a bad reaction whose source they identify). The Food and Drug Administration faces a similar challenge in its effort to standardize risk labels for over-the-counter drugs. For example, other things being equal, producing bilingual labels will require either reducing print size or omitting information about some side effects. These modifications would, in turn, increase the risks for consumers with limited vision (e.g., some of the elderly) or those particularly sensitive to the omitted effects. Whatever labeling, warning, or communication strategy is chosen will leave some residual risk, with an uneven distribution depending on the heterogeneous sensitivities of the audience. Thus, the strategy reflects the authorities' notion of the "acceptable level of misunderstanding" (28). What that acceptable level should be is a political and ethical question, which could be resolved by properly constituted public or private groups, and a scientific question, partially resolvable by research of the sort described here. Rigorous empirical testing is needed to determine whether communications fulfill the hopes placed in them (27). Emerging foodborne pathogens provide a particular challenge to safety communications—and a particular need for evaluation. Their novelty and ability to produce outbreaks in diverse places in the world and the food chain encourage treating them as unique. If a communication strategy is improvised only when a crisis hits, or as it evolves, the chances for a misstep increase. Those chances are especially large if the outbreak is the first major risk problem for the health authorities involved (16). As a result, communications about these unique situations should be routine. A standard format for reporting risk information should be adopted. Funtowicz and Ravetz (29) propose a notation that includes a best-guess risk estimate (expressed in standard units), a measure of variability, and a "pedigree" (indicating the quality of the research). Although new, such notation might become familiar, much as degrees Fahrenheit, miles per gallon, probability of precipitation, and recommended daily allowance have become familiar. Another part of communication planning is to adopt standard scripts for reporting complex procedural information regarding what citizens should do and what food specialists are doing. The adoption process should include empirically testing the comprehensibility of concrete messages with an audience like the intended audience. Influence diagrams offer one template for organizing procedural information. Risk analyses provide one way to identify the crises most likely to occur and may allow not only testing the most likely messages, but also identifying the persons most likely to do the communicating and preparing them accordingly. The chemical industry's Community Awareness and Emergency Response program might provide some useful lessons in how to organize for unlikely events, although the challenges of dealing with the relatively identifiable community surrounding a chemical plant are different from those presented by dealing with the diffuse national (or even international) audience concerned about a food. The chemical industry's experience may also provide guidance on how to achieve voluntary industry compliance with a set of communication principles. Public goodwill is eroded every time an industry spokesperson violates the public trust by misrepresenting, or just explaining inadequately, the state of affairs. Reducing misrepresentation requires institutional discipline; reducing inadequate communication requires a scientific approach to communication. Acknowledgments Our research was supported in part by the National Institute for Allergy and Infectious Diseases, the National Institute of Alcohol Abuse and Alcoholism, and the National Science Foundation. Address for correspondence: Baruch Fischhoff, Department of Social and Decision Sciences, Department of Engineering and Public Policy, Carnegie Mellon University, Pittsburgh, PA 15213 USA; fax: 412-268-6938; e-mail: baruch@andrew.cmu.edu. References 1. Fischhoff B, Bostrom A, Quadrel MJ. Risk perception and communication. In: Detels R, McEwen J, Omenn G, editors. Oxford textbook of public health. London: Oxford University Press; 1997. p. 987-1002. 2. Krimsky S, Golding D, editors. Social theories of risk. Westport (CT): Praeger; 1992. 3. Slovic P. Perception of risk. Science 1987;236:280-5. 4. Lammerding AM. Quantitative microbial risk assessment. Emerg Infect Dis. In press 1997. 5. National Research Council. Improving risk communication. 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London: Kluwer; 1990. --------------------------------------------------------------------------- Emerging Infectious Diseases National Center for Infectious Diseases Centers for Disease Control and Prevention Atlanta, GA URL: ftp://ftp.cdc.gov/pub/EID/vol3no4/ascii/fischof.txt