Advanced Articles  (September 25, 1997)

[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997]

Consumer Concerns: Motivating to Action

Christine M. Bruhn
University of California, Davis, California, USA
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      Microbiologic safety is consumers' most frequently volunteered
      food safety concern. An increase in the level of concern in
      recent years suggests that consumers are more receptive to
      educational information. However, changing lifestyles have
      lessened the awareness of foodborne illness, especially among
      younger consumers. Failure to fully recognize the symptoms or
      sources of foodborne disease prevents consumers from taking
      corrective action. Consumer education messages should include
      the ubiquity of microorganisms, a comprehensive description of
      foodborne illnesses, and prevention strategies. Product labels
      should contain food-handling information and warnings for
      special populations, and foods processed by newer
      safety-enhancing technologies should be more widely available.
      Knowledge of the consequences of unsafe practices can enhance
      motivation and adherence to safety guidelines. When consumers
      mishandle food during preparation, the health community, food
      industry, regulators, and the media are ultimately responsible.
      Whether inappropriate temperature control, poor hygiene, or
      another factor, the error occurs because consumers have not
      been informed about how to handle food and protect themselves.
      The food safety message has not been delivered effectively.

Consumer Knowledge and Concern

Consumers are receptive to information about microbiologic hazards.
Nationwide surveys by the Food Marketing Institute indicate that more
people volunteer concerns about microbiologic hazards than about any other
potential food safety issue. From 1992 to 1996, volunteered concern about
microbiologic safety increased from 36% to 49% (1). Specifically, concern
about contamination by bacteria or other microorganisms was 77%, more than
concern about pesticide residues (66%), product tampering (66%), antibiotic
residues (42%), or any other food safety risk.

Food-Handling Practices

Although many consumers recognize the potential seriousness of foodborne
bacteria, they lack information on safe handling and storage of food
products (2). Williamson et al. (3) found that consumers under 35 years of
age knew less about food safety terms and concepts than those over 35.
Specific safe food handling was not practiced by 15% to 30% of survey
respondents. For example, consumers did not cool cooked food rapidly, with
29% indicating they would let roasted chicken cool completely before
refrigerating. Only 32% indicated they would use small, shallow containers
to refrigerate leftovers. Consumers did not know that failure to
refrigerate may jeopardize safety, with 18% not concerned or uncertain
about the safety of cooked meat and 14% not concerned about poultry left
unrefrigerated for more than 4 hours. The need for sanitation was not
recognized, with only 54% indicating they would wash a cutting board with
soap and water between cutting raw meat and chopping vegetables.

Food safety experts have identified the most common food-handling mistakes
made by consumers at home. These mistakes include serving contaminated raw
food, cooking or heating food inadequately, obtaining food from unsafe
sources, cooling food inadequately, allowing 12 hours or more between
preparation and eating, and having a colonized person handle implicated
food or practice poor hygiene (4). The same factors were identified in
mishandling associated with specific pathogens (5).

Changing Lifestyles

Many factors have contributed to consumers' lack of familiarity with safe
food handling and increased foodborne illnesses. Increased participation in
the paid labor force has lessened the exposure of young people to
food-handling practices in the home; few schools offer or require food
preparation classes; and partially prepared foods may have different, less
familiar handling requirements (2,6).

People eat out more frequently today, thereby increasing their exposure to
the food service industry, noted for high turnover rates and minimal job
training in personal hygiene (7). Furthermore, the population is shifting,
with an increased percentage of persons at higher risk for foodborne
illness because of age or health status (8,9). Additionally, some food
safety recommendations related to temperature and acidity do not eliminate
risks from some pathogens (2).

Nature and Source of Foodborne Illness

Consumer perceptions and behavior related to foodborne illness changed
little between 1988 and 1993 (10). Consumers misperceived the nature of
foodborne illness and the most likely pathogen source. Consumer belief
about the type of food responsible for foodborne illness--meat, poultry,
seafood, eggs--was consistent with expert opinions; however, consumers
believed that foodborne illness was generally mild, without fever, and
occurred within a day of eating contaminated food. Infections caused by
Salmonella and Campylobacter, the most common foodborne illnesses in the
United States (11), are not consistent with the symptoms consumers
described, because these organisms have longer latency and cause fever.

Most consumers believed that their foodborne illness was caused by food
prepared somewhere other than the home. Williamson (3) found that about
one-third of consumers thought food safety problems most likely occurred at
food manufacturing facilities, and one-third blamed unsafe restaurant
practices. Only 16% thought mishandling was most likely to occur in the
home. Fein et al. (10) found that 65% of consumers attributed foodborne
illness to food prepared at a restaurant, 17% to mishandling at the
supermarket, and 17% to mishandling at home. In contrast, food safety
experts believe sporadic cases and small outbreaks in the home are far more
common than recognized outbreaks (2).

Failure to recognize the home as a likely source of foodborne illness is
not unexpected because illness traced to a food establishment affects many
people and may receive widespread publicity (12). Illness that occurs at
home is rarely reported unless severe (2).

If consumers misperceive the nature and origin of foodborne illness, they
underestimate the frequency of serious consequences and are less motivated
to change. Schafer et al. (13) found that motivation for proper food
handling requires viewing the mishandling of food as a direct threat to
one's health. The failure to associate mishandling of food in the home with
foodborne illness interferes with foodborne disease education efforts (10).

Ubiquity of Organisms

Consumers do not seem to be aware of the ubiquity of microorganisms in the
environment. During foodborne disease outbreaks, press accounts focus on
fecal contamination of food. Government standards classify natural
microorganisms as contaminants, which suggests that microorganisms are only
present as a result of mishandling. In contrast, Hazard Analysis and
Critical Control Points (HACCP) programs recognize and attempt to control
potential dangers related to pathogenic microorganisms.

When consumers in a national sampling were asked on whom they rely for
product safety, the percentage responding "myself as an individual"
decreased from 48% in 1989 to 25% in 1996 (1). As self-reliance decreased,
consumer reliance on food manufacturers and supermarkets increased. This
may be a response to the message that if raw food contains microorganisms,
it is contaminated. It suggests some consumers are shifting the
responsibility for safe food to manufacturers and retailers.

Consumers may not realize they can introduce pathogens during food
handling. In 1990, the Food Marketing Institute asked consumers what steps
they took at home to ensure the safety of food (14). Respondents
volunteered refrigeration (58%), proper storage (35%), checking expiration
dates (26%), washing and cleaning the food (25%), cooking properly (22%),
and wrapping food properly (20%). No one volunteered washing hands or
preventing cross-contamination.

Labeling

Products must contain safety labels instructing consumers how to handle
food. In 1989, the National Advisory Committee on Microbiological Criteria
for Foods recommended a mandatory uniform logo for perishable refrigerated
foods, uniform labeling for frozen food, "Use by" dates, and
time/temperature indicators wherever possible (15).

Although products are currently labeled when they require refrigeration,
the label is ineffective because the warning is difficult to find or read.
As the proportion of older people increases, print must be larger. Labels
should also display symbols to further enhance the effectiveness of the
message.

Safe-handling labels on meat products appear to have made a difference. The
Food Marketing Institute (1) found that 60% of survey respondents had seen
the labels. Of those aware of the labels, 65% said the labels increased
their awareness of safety, and 43% said they changed their behavior as a
result of the information. The most common volunteered change was washing
the counter and utensils after contact with meat (approximately 40%),
followed by washing hands more frequently (approximately 20%) and cooking
to the proper temperature (approximately 20%).

Labels do not consistently contain needed information. When foodborne
illness was related to consumption of unpasteurized apple juice, consumers
were not able to determine from the label which products were pasteurized.
Many major manufacturers do not indicate whether their fresh juice product
is pasteurized.

Consumers are not advised about potential risks for special populations.
Raw milk sold in California must contain a warning statement, but other
states may not have this requirement. Because of inconsistencies in
labeling, unpasteurized juice products may be given to infants. Also,
products that contain honey do not include a warning about potential risk
for infant botulism.

Processing Technology

Consumers do not realize that pathogens can survive minimal processing, as
evidenced by a recent Escherichia coli outbreak associated with fresh apple
juice, which demonstrated that processors also may not recognize potential
risks. A fresh apple juice manufacturer in northern California claimed its
product was safe because the juice was squeezed in small batches and frozen
immediately.

Freezing is not effective against E. coli O157:H7, but other methods are
protective. Several methods have been developed to reduce pathogens and
increase the safety of foods. Once these methods are verified as effective
and safe, the food industry should be free to use them, and consumers
should have the opportunity to select safer foods. In some cases, the
regulatory approval process appears to hinder rather than facilitate the
safer handling of food.

Food irradiation, exposing food to high levels of electromagnetic energy
for specific purposes, has been approved for selected uses. A petition
before the Food and Drug Administration to permit irradiation of meat and
other muscle foods appears to have satisfied safety concerns, but approval
has not yet been granted. The requirement to seek approval for each
application of irradiation prevents rapid response in cases of foodborne
outbreaks. Although this regulatory procedure may have been reasonable when
irradiation was first introduced, it warrants a fresh look in view of the
wealth of data now available on the safety and wholesomeness of food
irradiation (16).

Attitude surveys and marketing experience consistently demonstrate that
consumers will purchase irradiated food (17). National surveys indicate
consumer concern about irradiation was lower than other food-related
concerns. When specifically asked what they considered a serious health
hazard, 29% identified irradiation, 77% identified bacteria, and 66%
identified pesticides (1). The percentage of consumers concerned about
irradiation has decreased significantly over time. In the late 1980s, 42%
to 43% classified irradiation as a serious concern, decreasing to 29% in
1996. A relative ranking of food processing methods surveyed by the Gallup
Organization found that irradiation, food preservatives, and chlorination
generated similar concern (18).

In a nationwide Food Marketing Institute survey, 69% of consumers indicated
they were very or somewhat likely to purchase products irradiated to kill
bacteria or other microorganisms (1). Surveys completed in several areas of
the country indicate 60% to 70% of consumers would prefer irradiated food
(17). In one study, information about irradiation increased interest in
purchasing to 90%, and education plus food samples increased purchase
intent to 99%.

Consumers have purchased irradiated food in select locations across the
United States since 1992 (17). Fruits from the Mainland and Hawaii have
sold well in the Midwest and California (L. Wong, pers. comm.). Irradiated
chicken gained over 60% of market share when priced 10% lower than
nonirradiated chicken and 47% when priced the same (J.A. Fox, pers. comm.).

Irradiated food is not widely available. Special interest groups threaten
companies that exchange information about irradiation processing.
Consumers, however, appear to prefer irradiated foods when the benefits of
these foods are endorsed by health professionals. Food manufacturers and
retailers should offer consumers the choice of safety-enhanced,
energy-pasteurized irradiated food.

Communicating with the Public

To respond to consumers' need for information, a multifaceted program is
needed. The HACCP strategy, which teaches consumers to critically think
through the food safety process to determine how foodborne illness could
occur, has been effective (19,20). The HACCP approach to home food
preservation is logical and highlights key control points (21).

Consumers should be informed that microorganisms are ubiquitous in the
environment, found on raw products of animal or plant origin. Pathogens may
survive minimal processing and preservation treatments. People may
introduce pathogens during any stage of food processing or handling,
including just prior to consumption. Foodborne illness can range from mild
to severe and life-threatening with chronic complications. People have
control and can reduce risks.

Communicating food safety information to the public effectively is another
challenge. Consumers obtain most of their information on food, nutrition,
and science from the media; television is cited most frequently, and
newspapers and magazines follow (22,23). Brochures enforce messages and
serve as useful references, although they are not as widely seen as media
stories.

Developing messages with the press should be a primary activity of a food
safety education program. Consumers judge a message by the credibility of
the person conveying it, its appeal to their common sense, and the
frequency of the message (24). Media presentations can motivate people to
listen and change behavior. Consultants from the USDA hotline say, "We've
seen an explosion in media coverage of food safety, and callers want more
detailed explanations of things they read and hear" (25).

Information on safe food handling must be motivating and memorable. Stories
that capture the public's attention are personal. They relate life
experiences of people with whom the public can identify. Stories of the
consequences of mistakes are memorable. They can be touching, humorous, or
grotesque. It is easy to visualize and remember the infected bakery worker
who made 5,000 people ill when he mixed a vat of buttercream frosting with
his bare hands and arms despite bouts with diarrhea (26).

Stories can be heartrending, as in the experiences of a family who lost a
child to E. coli O157:H7 infection. It is difficult to document the
effectiveness of vivid accounts of doing things right or wrong. However,
when Washington state carried extensive coverage linking the outbreak to
undercooked hamburgers, 13% of the men said they ate undercooked hamburger,
compared with 38% in Colorado (25).

Conclusions

Consumer concerns about foodborne illness can motivate change in regulatory
and industry use of technology, product labeling, and consumer education.

New Technologies

The food industry has both a right and a responsibility to use safe and
effective technology to enhance the safety of the food supply. Regulatory
authorities should expediently evaluate and facilitate new technologies,
such as food irradiation, laser light treatment, and high-pressure
processing, which enhance food safety. Health professionals, the food
industry, and regulators should challenge special interest groups that
distort information and strive to limit consumer choice.

Improved Labeling

Processed and packaged food should bear labels that clearly indicate how
food should be handled. Labels should include warnings about special risks
to select populations. Benefits from special processing that can reduce
microbes should also be encouraged.

Consumer Education

Consumers need to appreciate the seriousness of foodborne diseases. They
must learn to recognize unsafe food-handling practices, the latency period
for some microbes, and the symptoms of foodborne disease. They need to
understand how to protect themselves through kitchen and personal hygiene,
including thoroughness and frequency of hand washing, temperature control,
and safe food choices such as foods processed by heat or energy
pasteurization. Young people should be reached through age-specific school
curricula, such as personal hygiene and special "living skills" units that
address food safety and diet. Food industry and health educators should
work with the media to develop interesting and timely messages to increase
consumer knowledge about safe food handling. Messages must be consistent,
science-based, frequent, and personalized.

Address for correspondence: Christine M. Bruhn, Consumer Behavior,
University of California, Center for Consumer Research, University of
California, Davis, CA 95616-8598; fax: 916-752-3975; e-mail:
cmbruhn@udavis.edu.

References

  1. Abt Associates Inc. Trends in the United States, consumer attitude and
     the supermarket 1996. Washington (DC): Food Marketing Institute; 1996.
  2. Institute of Food Technologists' Expert Panel on Food Safety and
     Nutrition. Scientific status summary, foodborne illness: role of home
     food-handling practices. Food Technology 1995;49:119-31.
  3. Williamson DM, Gravani RB, Lawless HT. Correlating food safety
     knowledge with home food-preparation practices. Food Technology
     1992;46:94-100.
  4. Bryan F. Risks associated with vehicles of foodborne pathogens and
     processes that lead to outbreaks of foodborne diseases. Journal of
     Food Protection 1988;51:663-73.
  5. Bean NH, Griffin PM. Foodborne disease outbreaks in the United States,
     1973-1987; pathogens, vehicles, and trends. Journal of Food Protection
     1990;53:804-17.
  6. Dumagan JC, Hackett JW. Almost half of the food budget is spent eating
     out. Food Review 1995;18:37.
  7. Martin R. Foodborne disease threatens industry. National Restaurant
     News 1990;24:27,30.
  8. Doyle MP. Food safety in the 21st century. Dairy Food Environ Sanit
     1993;13:383.
  9. Food Institute. Population trends 1996-2050. Fair Lawn (NJ): The
     Institute; 1996. p. 31.
 10. Fein SB, Jordan CT, Levy AS. Foodborne illness: perceptions,
     experience, and preventive behaviors in the United States. Journal of
     Food Protection 1995;58:1405-11.
 11. Tauxe RV. Epidemiology of Campylobacter jejuni infections in the
     United States and other industrialized nations. In: Nachamkin J,
     Blaser MJ, Tompkins LS, editors. Campylobacter jejuni: current status
     and future trends. Washington (DC): American Society for Microbiology;
     1992. p. 9-19.
 12. Ollinger-Snyder P, Matthews ME. Food safety issues: press reports
     heighten consumer awareness of microbiological safety. Dairy, Food and
     Environmental Sanitation 1994;14:580-9.
 13. Schafer RB, Schafer E, Bultena GL, Hoiberg EO. Food safety: an
     application of the health belief model. Journal of Nutritional
     Education 1993;25:17-24.
 14. Food Marketing Institute. Opinion research, trends 90, consumer
     attitudes & and the supermarket 1990. Washington (DC): The Institute;
     1990.
 15. Rhodes ME. Educating professionals and consumers about
     extended-shelf-life refrigerated foods. Food Technology 1991;45:162-4.
 16. Diehl JF. Safety of irradiated foods. New York: Marcel Dekker, Inc.;
     1995.
 17. Bruhn CM. Consumer attitudes and market response to irradiated food.
     Journal of Food Protection 1995;58:175-81.
 18. The Gallup Organization. Irradiation: consumers' attitudes. Princeton
     (NJ): Prepared for the American Meat Institute; 1993.
 19. Hoban T. Consumer awareness and acceptance of bovine somatotropin.
     Survey conducted for the Grocery Manufacturers of America; 1994.
 20. Hoban T, Kendall PA. Consumer attitudes about the use of biotechnology
     in agriculture and food production. Raleigh (NC): North Carolina State
     University; 1992.
 21. Bruhn CM, Peterson S, Phillips P, Sakovich N. Consumer response to
     information on integrated pest management. Journal of Food Safety
     1992;12:315-26.
 22. United States Department of Agriculture. The Food Safety Educator
     1996;1:3.
 23. Beware the Norwalk virus. Food Talk (Winter) 1989;4.
 24. Reicks J, Bosch A, Herman M, Krinke UB. Effectiveness of a food safety
     teaching strategy promoting critical thinking. Journal of Nutritional
     Education 1994;26:97-100.
 25. Medeiros LC, George RT, Gruns K, Chandler C, Crusey S, Fittro J, et
     al. The safe food handling for occasional quantity cooks curriculum.
     Journal of Nutritional Education 1996;28:39-42.
 26. United States Department of Agriculture, Food Safety and Inspection
     Service. A margin of safety: the HACCP approach to food safety
     education. Washington (DC): United States Department of Agriculture
     Information and Legislative Affairs; 1990.

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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA

[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997]

Public, Animal, and Environmental Health Implications of Aquaculture

E. Spencer Garrett,* Carlos Lima dos Santos, and Michael L. Jahncke
*National Seafood Inspection Laboratory, Pascagoula, Mississippi, USA;
Food and Agriculture Organization of the United Nations, Rome, Italy;
Virginia Tech Seafood Research and Extension Center, Hampton, Virginia,
USA
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      Aquaculture is important to the United States and the world's
      fishery system. Both import and export markets for aquaculture
      products will expand and increase as research begins to remove
      physiologic and other animal husbandry barriers. Overfishing of
      wild stock will necessitate supplementation and replenishment
      through aquaculture. The aquaculture industry must have a
      better understanding of the impact of the "shrouded" public and
      animal health issues: technology ignorance, abuse, and neglect.
      Cross-pollination and cross-training of public health and
      aquaculture personnel in the effect of public health, animal
      health, and environmental health on aquaculture are also
      needed. Future aquaculture development programs require an
      integrated Gestalt public health approach to ensure that
      aquaculture does not cause unacceptable risks to public or
      environmental health and negate the potential economic
      and nutritional benefits of aquaculture.

U.S. Fisheries System

Coastal estuaries serve as a breeding ground and provide habitats for more
than 75% of commercial landings and 80% to 90% of the recreational catch of
fish and shellfish. From these habitats, hundreds of species of seafood are
produced. Aquacultured species now contribute up to 15% of the U.S. supply
(1,2). Wild species are harvested by 17,000,000 recreational anglers and
nearly 300,000 commercial harvesters. Commercial harvesters deploy 93,000
vessels, while recreational fishermen have millions of recreational fishing
boats. Nearly 5,000 domestic plants are located in every state throughout
the United States, not just in the coastal areas (3). Current per capita
consumption of commercially harvested species averages 15 pounds; it is
estimated that per capita consumption of recreationally harvested seafood
approaches an additional 3 to 4 pounds per person (4).

The seafood business community--in the United States and in other
industrialized countries--cannot rely solely on domestically produced stock.
For a number of years, more than half of U.S. seafood consumption has
relied on imported stock. Currently, the United States imports more than
50% of the consumed seafood, which originates in 172 countries around the
world (3). This trend toward economic reliance on imported stock has
steadily increased over the past 10 years so that now the United States is
the world's second largest importer of seafood. The principal seafood
imports are tuna, shrimp, salmon, lobster, and groundfish (3).

It is difficult to determine where imported fish was harvested. For
example, the United States imports salmon from Switzerland and Panama,
although neither Switzerland nor Panama is noted for vast salmon resources.
U.S. participation in the international seafood trade is very complex,
since in addition to being the world's second largest importer, the United
States is also the world's second largest exporter of seafood (3). This
dichotomy requires that U.S. marketing and import/export food control
inspection strategies be carefully planned. For example, the United States
exports seafood to 162 countries, which has come about with the full
development of northwest and Alaska fisheries and improved efficiency in
processing techniques. Major U.S. exports are salmon, crab, surimi, fish
blocks, groundfish, flatfish, shrimp, and lobster (3).

Current Aquaculture Status

In 1996, U.S. aquaculture production of nearly 227,000 metric tons
consisted of baitfish, catfish, salmon, trout, clams, crawfish, mussels,
oysters, fresh and saltwater shrimp, and miscellaneous species such as
ornamental fish, alligators, algae, aquatic plants, tilapia, and hybrid
striped bass. The United States exported principally rainbow trout,
Atlantic salmon, tilapia, catfish, freshwater crawfish, and live mussels to
19 countries in Europe, North and South America, and Asia. Freshwater
crawfish led the export seafood market at slightly over $8 million, with
the other species accounting for less than $1 million each (3). The United
States also imports large volumes of aquacultured products, approximately
$2.5 billion in cultured products, primarily shrimp and salmon. Imported
cultured seafood accounts for most of the current U.S. trade deficit for
edible fishery products, which was approximately $3.5 billion in 1995.

The Safety of Seafood

Most seafood is safe; however, like all foods, it carries some risk. The
food safety issues for seafood are highly focused, well-defined, and
limited to a very few species. For seafood-borne illnesses (in which the
cause was known) reported to the Centers for Disease Control and
Prevention, more than 90% of the outbreaks and 75% of the individual cases
were associated with ciguatoxin (from a few reef fish species) and
scombrotoxin (from tuna, mackerel, bluefish, and a few other species) and
the consumption of mollusks (mostly raw) (5-12).

Hazards associated with the consumption of all food (including seafood) can
be categorized into three areas: product safety; food hygiene (clean vs.
dirty plants, wholesome vs. unwholesome products); and mislabeling or
economic fraud. Traditionally, the food safety risks of seafood products
(aquacultured and wild-caught) have been subcategorized by environment,
process, distribution, and consumer-induced risk; the environmental risk
category is further subdivided into natural hazards, (e.g., biotoxins) and
anthropogenic contaminants (e.g., polychlorinated biphenyls) (13).

"Shrouded" Aquaculture Hazards

The future of aquaculture is bright; aquaculture products are as safe and
wholesome as wild-caught species. However, in addition to the consumer
hazards listed above, there are some less obvious "shrouded" public health
hazards associated with ignorance, abuse, and neglect of aquaculture
technology.

Technology Ignorance

A common practice in many developing countries is the creation of numerous
small fish pond impoundments. However, this approach may have a greater
adverse effect on human health than the creation of a single large
impoundment (14). Small impoundments greatly increase the overall aggregate
shoreline of ponds, causing higher densities of mosquito larvae and
cercaria, which can increase the incidence and prevalence of diseases such
as lymphatic filariasis and schistosomiasis, respectively. Centralized
planning approaches for new freshwater and marine aquaculture sites should
include discussions of the potential effect of large or small impoundments
on such issues as disease transmission, water supply, irrigation, and power
generation (14).

Ignorance of the microbial profile of aquaculture products can also affect
human health as evidenced by the recent transmission of streptococcal
infections from tilapia to humans, which resulted in several meningitis
cases in Canadian fish processors (15). A change in marketing strategies to
sell live fish in small containers, instead of ice-packs, resulted in human
Vibrio infections from live tilapia in Israel in 1996. Such bacteria can be
present in other aquacultured and wild-caught species in addition to
tilapia.

Ignorance of the hazards associated with the use of untreated animal or
human waste in aquaculture ponds to increase production also has tremendous
human health implications (16). For centuries, food growers have cultured
species in waste-water-fed ponds and grown secondary vegetable crops in
waste water and sediment material in integrated aquaculture operations.
However, the potential for transmission of human pathogens to cultured
species and secondary vegetable crops is rarely considered by fishery
aquaculturists. For example, of more than 250 presentations at the 1997
World Aquaculture Society meeting held in Seattle, Washington, few referred
to the potential human health implications of aquaculture (17).

The potential transmission of animal pathogens from exotic aquacultured
species to wild-stock species also affects animal health. Recent outbreaks
of taura, yellow spot, and white head viruses have occurred in aquaculture
shrimp in South Carolina and Texas. Recent studies indicate that native
wild white shrimp may also be susceptible to these exotic viruses (18).

Technology Abuse

Technology abuse includes the willful misuse of therapeutic drugs,
chemicals, fertilizers, and natural fishery habitat areas. The widespread
use and misuse of antibiotics to control diseases in aquaculture species is
worldwide and will probably increase as aquaculturists move towards more
intensive animal husbandry rearing techniques and stocking densities. For
example, the illegal use of chloramphenicol in shrimp culture to control
diseases may result in violative levels in the harvested product.
Similarly, the improper or illegal use of chemicals (e.g., tributyl tin) to
control pond pests such as snails can also result in human health hazards.
The abuse and misuse of raw chicken manure as pond fertilizer may result in
the transmission of Salmonella from manure to the cultured product (16).

The destruction of mangrove areas to build aquaculture ponds can have a
drastic impact on the survival of wild aquatic species through the
degradation of essential fish habitats and nurseries. In Brazil,
destruction of mangrove areas for shrimp ponds effected climatic changes to
such an extent that the aquaculture operations have been terminated because
consequent reduced rainfall resulted in excessive pond salinity (19).

Technology Neglect

The final "shrouded" hazard associated with aquaculture involves technology
neglect, which includes such events as the abandonment of small aquaculture
ponds in tropical countries, leading to increased mosquito habitats and
concomitant increases in malaria (14). Facility management can be
responsible for technology neglect if employees are not trained in the
proper use and application of therapeutics and chemicals, for example.
Finally, from an animal health perspective, ignorance or willful neglect of
the International Council for Explorations of the Sea/European Inland
Fisheries Advisory Commission Code of Practice for the Introduction and
Transfer of Marine Organisms can result in the escape of exotic species and
animal pathogens into the environment with a potential tragic impact on
native aquatic species (20).

Health Control Considerations

Human Health

Procedures to help protect humans from aquaculture-associated risks include
better education and training of aquaculture personnel on the proper use
and storage of therapeutics and chemical compounds. Additional research on
new more effective and, we hope, safer, antibiotic and vaccine treatment of
aquaculture species is under way. Likewise, certain extralabel use
applications for selected antibiotics are under consideration. Streamlined
enforcement efforts are being developed to ensure compliance with new food
safety regulations and new regulatory control procedures such as Hazard
Analysis and Critical Control Points (HACCP) and the application of HACCP
principles to animal and environmental control procedures (21,22).

The Food and Agriculture Organization and World Health Organization
recommend that the HACCP concept be applied to fresh water aquaculture
programs to control foodborne digenetic trematode infections in humans.
Experiments are being carried out in Asia by a multidisciplinary team of
experts in public health, parasitology, aquaculture, fisheries extension,
and fish inspection (22). In one study in Vietnam, experimental activities
were conducted in two side-by-side fish ponds. In the experimental ponds,
fish were cultured in conjunction with HACCP principles, and control pond
fish were cultured according to conventional local aquaculture practices
(22). Water supply, fish fry, fish feed, and pond conditions in the
experimental pond were identified as critical control points. The HACCP
principles of hazard analysis, preventative measures, critical limits,
monitoring, recordkeeping, and verification procedures relating to the
critical control points were applied; study results showed Clonorchis
sinensis eggs and fish infected with the parasite metacercaria and the
first intermediate host (Melanoides tuberculata) in the experimental ponds
(22). Forty-five percent of control pond fish were infected with C.
sinensis metacercaria, while white fish from the experimental pond
monitored according to HACCP principles were completely free of trematode
infection (22). Preliminary results indicate that application of
HACCP-based principles to silver carp culture in North Vietnam is an
effective way to prevent and control C. sinensis. Similarly, the
application of these principles to fresh water aquaculture ponds in
Thailand and Laos to control Opisthorchis viverrini infections has also
been successful. Additional studies are recommended to confirm these
preliminary results (22).

Animal Health

Procedures to safeguard animal health are set out in the International
Council for Explorations of the Sea and the European Inland Fisheries
Advisory Commission Codes of Practice, which describe how to prevent the
adverse effects of introducing new and exotic species and emerging animal
pathogens. Education and on-site training programs for aquaculture
employees will help them understand the detrimental impact of introduction
of exotic species and animal pathogens, misuse and abuse of therapeutics
and chemicals, and willful habitat destruction. High priority issues also
include implementation of biosecurity procedures in aquaculture operations
to prevent the escape and spread of exotic species and pathogens into the
facility and surrounding natural environment and the use of the HACCP
principles to help control the spread of exotic pathogens to wild aquatic
populations (17,23).

The application of HACCP principles to control transmission of exotic
shrimp viruses from cultured to wild shrimp was proposed at a shrimp
pathogen workshop held in June 1996 in New Orleans, Louisiana (21). Natural
resource regulatory agencies are concerned about the possible transmission
of exotic shrimp pathogenic viruses, recently found in shrimp aquaculture
ponds in Texas and South Carolina, to wild native shrimp populations. The
principles of HACCP, in conjunction with International Council for
Explorations of the Sea and the European Inland Fisheries Advisory
Commission Codes of Practice, were proposed to control the spread of exotic
animal viruses into the environment. Shrimp aquaculture has the following
proposed critical control points: pond site selection; water supply
quality; pond management techniques; and transportation, especially as it
relates to the live transport of aquaculture shrimp species (21).

Approximately 600 million pounds of shrimp are also imported for further
processing into the United States on a yearly basis, half of which are
aquacultured species (3). Natural resource managers, particularly at the
state level, are concerned about the possible transmission of exotic shrimp
pathogens into the environment from shrimp processing plant wastewater
discharge and solid waste material landfill leakage. Proposed HACCP shrimp
processing plant critical control points include unload/receive;
de-ice/wash; thaw; dehead/peel/devein; wash; re-ice; de-ice/wash; re-ice;
and dip/glaze (21).

Application of HACCP principles at aquaculture site and processing plant
locations has the potential to control transmission of exotic human and
animal pathogens. However, to our knowledge, except for the application of
HACCP principles to control of human pathogens in Asia (17), no research
has been conducted on this issue.

Address for correspondence: Michael Jahncke, Virginia Tech Seafood Research
and Extension Center, 102 King Street, P.O. Box 369, Hampton, VA 23669 USA;
fax: 757-727-4871; e-mail: mjahncke@vt.edu.

References

  1. Ratafia M. Aquaculture today: a worldwide status report. Aquaculture
     News 1994;3:12-13,18-19.
  2. Rhodes RJ. Status of world aquaculture. Aquaculture Magazine 17th
     Annual Buyers Guide 1987;4-18.
  3. National Marine Fisheries Service. Fisheries of the United States
     1995. Current Fisheries Statistics No. 9500. Washington (DC): U.S.
     Department of Commerce; 1996.
  4. Krebs-Smith SM. Report on per capita consumption and intake of fishery
     products [letter]. In: National Academy of Sciences Committee on the
     Evaluation of the Safety of Fishery Products 1991 Seafood Safety
     Report. Washington (DC): National Academy Press; 1991.
  5. Centers for Disease Control. Annual summary of foodborne diseases
     (1978). Atlanta (GA):CDC;1979.
  6. Centers for Disease Control. Annual summary of foodborne diseases
     (1979). Atlanta (GA):CDC;1981.
  7. Centers for Disease Control. Annual summary of foodborne diseases
     (1981). Atlanta (GA):CDC;1983.
  8. Centers for Disease Control. Annual summary of foodborne diseases
     (1980 and 1981). Atlanta (GA):CDC;1983.
  9. Centers for Disease Control. Annual summary of foodborne diseases
     (1982). Atlanta (GA):CDC;1985.
 10. Centers for Disease Control. Annual summary of foodborne diseases,
     unpublished data. Atlanta (GA):CDC;1989.
 11. Centers for Disease Control. Foodborne disease outbreaks, 1983-87.
     MMWR CDC Surveill Summ 1990;39(SS-1):1-45.
 12. National Marine Fisheries Service. The draft report of the model
     seafood surveillance project. A report to Congress. Pascagoula (MS):
     Office of Trade and Industry Services, National Seafood Inspection
     Laboratory;1995.
 13. Garrett ES. Role of diseases in marine fisheries management.
     Transactions of the 50th North American Wildlife and Natural
     Resources. NOAA Conference 1986. Tech. Memo. NMFS, F/NWR-16.
     Washington (DC): National Marine Fisheries Service;1986.
 14. Mott KE. A proposed national plan of action for schistosomiasis
     control in the United Republic of Cameroon. Geneva: World Health
     Organization (unpublished document WHO/SCHISTO/86,88); 1996.
 15. Centers for Disease Control and Prevention. Invasive infection with
     Streptococcus iniae-Ontario, 1995-1996. MMWR Morb Mort Wkly Rep 1996;
     45(30):650-3.
 16. Buras N. Microbial safety of produce from wastewater fed aquaculture.
     In: Pullin RVC, Rosenthal H, Maclean JL, editors. Environment and
     aquaculture in developing countries. Proceedings of the 31st
     International Center for Living Aquatic Resources Management
     Conference; 1993; Manila, Philippines. Manila: The Center; 1993. p.
     285-95.
 17. World Aquaculture Society. Abstracts of the Annual International
     Conference and Exposition of the World Aquaculture Society and The
     National Aquaculture Conference and Exposition of National Aquaculture
     Association; 1997 Feb 19-23; Seattle, WA.
 18. Virus re-emerges at shrimp farm. The Aquaculture News 1996;4(11):1-15.
 19. Pullin RSV. Discussion and recommendations on aquaculture and the
     environment in developing countries. In: Pullin RSV, Rosenthal H,
     Maclean JL, editors. Environment and aquaculture in developing
     countries. Proceedings of the 31st ICLARM Conference 1993. p. 312-338.
 20. Turner GE, editor. Codes of practice and manual of procedures for
     consideration of introductions and transfers of marine and freshwater
     organisms. EIFAC Occasional Paper 23. Rome: FAO; 1988.
 21. Jahncke JL. The application of the HACCP concept to control exotic
     shrimp viruses. Proceedings of the NMFS Workshop on Exotic Shrimp
     Viruses. 1996 June; New Orleans, LA.
 22. Son TQ, Hoi VS, Dan TV, Nga C, Toan TQ, Chau LV, et al. Application of
     hazard analysis critical control point (HACCP) as a possible control
     measure against Clonorchis sinensis in cultured silver carp
     Hypophthalmichthys molitrix. Paper presented at 2nd Seminar on
     Food-Borne Zoonoses: Current Problems, Epidemiology and Food Safety;
     1995 Dec 6-9; Khon Kaen, Thailand.
 23. Austin B. Environmental issues in the control of bacterial diseases of
     farmed fish. In: Pullin RVC, Rosenthal H, Maclean JL, editors.
     Environmental and aquaculture in developing countries. Proceedings of
     the 31st International Center for Living Aquatic Resources Management
     Conference; 1993; Manila, Philippines. Manila: The Center; 1993. p.
     237-51.

------------------------------------------------------------------------

Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA

[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997]

Historical Overview of Key Issues in Food Safety

E. M. Foster
Madison, Wisconsin, USA
------------------------------------------------------------------------

      Foodborne transmission of pathogenic and toxigenic
      microorganisms has been a recognized hazard for decades. Even
      half a century ago we knew about the dangers of botulism from
      underprocessed canned foods; staphylococcal poisoning from
      unrefrigerated cream-filled pastries, sliced ham, meat, and
      poultry salads; and salmonellosis from infected animal
      products. Despite new protective measures, changes in
      preservation techniques and failure to follow recognized
      procedures have created new dangers. Moreover, we now recognize
      new organisms that can cause foodborne illness--Listeria
      monocytogenes, Escherichia coli O157:H7, Campylobacter jejuni,
      Vibrio parahaemolyticus, Yersinia enterocolitica, and others.
      Controlling these organisms will require widespread education
      and possibly new regulatory initiatives.

When I was growing up on my parents' farm in East Texas, we never thought
about food poisoning or unsafe food. The only foods we bought were sugar,
salt, flour, and oatmeal; everything else we produced and preserved on the
farm. My mother spent all summer canning fruits and vegetables for winter.
We had no refrigeration; we cured our own meat and drank raw milk. But I
never heard of botulism, staph poisoning, or salmonellosis or perfringens
poisoning until I studied bacteriology in college. Only then did I wonder
how we survived with no refrigeration in a hot climate. Finally, the answer
came to me. We just did not give the bacteria time enough to develop so
they could hurt us. Leftovers from breakfast--hot biscuits, eggs, ham, bacon
or sausage, oatmeal, coffee or milk--went right out to the chickens. Lunch
leftovers--biscuits, cornbread, vegetables, or fried chicken--were saved for
a cold supper 4 or 5 hours later. Any food left went to the pigs. The
bacteria had only a maximum of 3 or 4 hours to grow, and that usually is
not enough. I survived and went on to study food microbiology, which
included what was known then about food poisoning. The guru of food
poisoning in those days was professor Gail M. Dack at the University of
Chicago. Dr. Dack was a protege of Professor E.O. Jordan, who in 1917
published a 107-page book entitled Food Poisoning. Dr. Dack took over the
book and published his first version of Food Poisoning in 1943. In 1949 and
1956, subsequent editions appeared in which certain truisms became
apparent.

Botulism was considered a problem of canners, both home and commercial.
Thus, adequate heat processing would seem to solve the problem. Perhaps it
did for the canner, but now we know that heating will not eliminate all
botulism. Many foods, including salmon eggs, smoked fish, garlic in oil,
vacuum packaged lotus roots, and baked potatoes, can support growth and
botulinum toxin formation if the storage temperature is suitable.
Similarly, we thought staphylococcal poisoning was limited to cream-filled
pastries and cured ham. In recent years, outbreaks of staphylococcal
poisoning have been traced to cheese, whipped butter, ham salad, fermented
sausages, and canned corned beef. We now know how to prevent staphylococcal
poisoning, but not all food handlers understand and fully comply with the
appropriate control measures.

Salmonellosis was once thought a problem with meat from infected animals.
Now we know that a variety of food products can serve as vehicles of this
disease. As early as World War II, we found that dried eggs from the United
States could transmit this disease to our British allies. Thousands of
cases of human salmonellosis in the United States and other industrialized
countries have been transmitted by ice cream, chocolate, potato salad,
cheddar cheese, raw milk, black pepper, pate, aspic, ham, pasteurized milk,
and drinking water.

Clostridium perfringens, known since the 1940s, causes a problem only when
there is gross temperature abuse of cooked food. Clostridium botulinum,
Staphylococcus aureus, C. perfringens, and the salmonellae were well known
in Dr. Dack's day, although the food vehicles might have changed. Not so
well known were many of the organisms that preoccupy us today. For example,
we used to think of Escherichia coli as merely an indicator organism that
suggested insanitary handling. Now we know forms of E. coli can kill.
Thirty years ago, Listeria monocytogenes, Campylobacter jejuni, Aeromonas
hydrophila, Plesiomonas shigelloides, Vibrio parahaemolyticus, and Yersinia
enterocolitica were not known; now these are well-established foodborne
pathogens that we must control.

Although not part of a historical overview, other key issues deserve
attention during this meeting. For example, we once thought that fresh,
uncracked eggs were essentially sterile and safe to eat. We did not
recognize the ability of Salmonella Enteritidis to invade the laying hen
and thereby the yolk of an egg. An outbreak of S. Enteritidis at a Chicago
hotel taught us not to rely on the safety of eggs merely because the shell
was intact. S. Enteritidis in shell eggs is still a serious health problem
and a growing concern to egg and poultry producers.

Of equal, if not greater, concern is Salmonella Typhimurium strain DT 104.
Widely distributed in cattle herds of England, Scotland, and Wales, this
organism is resistant to several antibiotics, including ampicillin,
chloramphenicol, streptomycin, sulfonamides, and tetracycline. Between 1990
and 1995, the number of S. Typhimurium DT 104 isolated from humans in
Britain increased from 259 to 3,837 per year--a 15-fold increase. Moreover,
the percentage of drug-resistant isolates increased from 39% in 1990 to 97%
in 1995. S. Typhimurium DT 104 has been isolated in the United States from
sheep, pigs, horses, goats, emus, cats, dogs, elk, mice, coyotes, ground
squirrels, raccoons, chipmunks, and birds. American egg and poultry
producers are concerned about its entry into U.S. poultry flocks. S.
Typhimurium DT 104 infection in humans has been associated with the
consumption of chicken, sausage, and meat paste as well as with the
handling of sick animals. More than one-third of the patients have required
hospitalization, and 3% have died; these figures are very unusual for
ordinary Salmonella infections and indicate serious problems ahead.

Address for correspondence: E. M. Foster, Professor Emeritus, Food Research
Institute, University of Wisconsin, Madison, WI 53706 USA; fax:
608-263-1114.
------------------------------------------------------------------------

Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA

[Emerging Infectious Diseases * Volume 3 * Number 4 * October - December 1997]

Animal Diseases of Public Health Importance

Gregory D. Orriss
Food and Agriculture Organization of the United Nations, Rome, Italy
------------------------------------------------------------------------

      The Food and Agriculture Organization's (FAO) interest in
      emerging diseases caused by foodborne pathogens derives from
      its role as the leading United Nations agency with a mandate
      for food quality and safety matters. The Food Quality and
      Standards Service of FAO's Food and Nutrition Division is
      active in all areas related to food safety and implements the
      FAO/World Health Organization Food Standards Program. Its
      activities include providing assistance to FAO's member nations
      in addressing problems and strengthening infrastructure and
      promoting standardization as a means of facilitating trade and
      safeguarding the interests of consumers. This paper considers
      the importance of emerging foodborne diseases from the
      perspectives of the consumer, international trade in food,
      producers and processors, and developing countries and
      addresses prevention and control measures.

In recent years, public concern regarding food safety has increased as a
consequence of the outbreak of bovine spongiform encephalopathy (BSE) in
cattle, the prevalence of Salmonella serotype Enteritidis illnesses (from
poultry, meat, eggs), and the more localized outbreaks of illnesses
associated with Listeria monocytogenes (from dairy products, pt, salads)
and Escherichia coli O157:H7 (from ground or minced beef, unpasteurized
apple juice, vegetables). Emerging pathogens and the appearance of problems
such as BSE have resulted in enactment of specific controls in many
countries, while the general heightening of interest internationally has
prompted health professionals and the food industry in many countries to
scrutinize the control of emerging infectious agents.

Animal Feeding and Food Safety

The Food and Agriculture Organization (FAO) of the United Nations has had a
long-standing interest in the area of food safety and food quality. Because
of problems such as BSE and emerging pathogens, FAO convened an Expert
Consultation on Animal Feeding and Food Safety in Rome in March 1997 to
address these issues and provide the scientific basis for improving
practices in the feeding of animals for the production of food.

The ultimate objective of food industry and safety regulators is to ensure
that food reaching the consumer is safe and wholesome. This objective does
not imply that food can ever be completely free of risk but rather that the
level of risk to the consumer can be acceptable. Foods generally expected
to be safe may become unsafe as a result of hazards introduced during
production, processing, storage, transport, or final preparation by the
consumer. For food derived from animal sources, the hazards may originate
from a number of sources, including the consumption of contaminated feed.

Hazards in food that may relate to animal feed include salmonellosis,
mycotoxicosis, and ingestion of unacceptable levels of veterinary drugs and
agricultural and industrial chemicals. In addition, if the postulated link
between BSE and new variant--Creutzfeldt-Jakob disease is established, this
disease would also be an example of contamination originating from animal
feed.

The FAO consultation limited its considerations to food safety matters that
pertained strictly to animal feeds; it did not consider plant toxins,
radionuclides, or parasites spread by human sewage. The risk to human
health from other infectious agents that may contaminate either feed or
forage appears to be negligible or nonexistent and was, therefore, not
considered by the consultation. Only the standard domestic animals from
which food is derived in large quantities, such as meat and meat products,
milk and milk products, and eggs and egg products, as well as fish products
derived from aquaculture that involves the feeding of fish, were
considered. All aspects of animal feed, other than natural unrestricted
grazing, were considered. The consultation concluded that emerging
pathogens are generally not identified through traditional animal
surveillance and epidemiology.

Hazards Associated with Animal Feed

Mycotoxins are secondary metabolites produced by fungi of various genera
when fungi grow on agricultural products before or after harvest or during
transportation or storage. Some fungi such as Aspergillus spp. and
Penicillium spp. can invade grain after harvest and produce mycotoxins,
while others, such as Fusarium spp., typically infest grains and produce
mycotoxins before harvest. In some circumstances, Aspergilli can grow and
produce mycotoxins before the crop is harvested.

Both intrinsic and extrinsic factors influence fungal growth and mycotoxin
production on a substrate. Intrinsic factors include water activity, pH,
and redox potential; extrinsic factors are relative humidity, temperature,
and availability of oxygen.

Many mycotoxins with different chemical structures and widely differing
biologic activities have been identified. Mycotoxins may be carcinogenic
(e.g., aflatoxins B1, ochratoxin A, fumonisin B1), estrogenic (zearalenone
and I and J zearalenols), nephrotoxic (ochratoxins, citrinin, oosporeine),
dermonecrotic (trichothecenes), or immunosuppressive (aflatoxin B1,
ochratoxin A, and T-2 toxin). Much of the published information on toxicity
comes from studies in experimental animals, and these may not reflect the
effects of mycotoxins on humans and other animals. In addition, their
significance in human foods of animal origin is incompletely understood.
Mycotoxins are regularly found in animal feed ingredients such as maize,
sorghum grain, rice meal, cottonseed meal, groundnuts, legumes, wheat, and
barley. Most are relatively stable compounds, are not destroyed by feed
processing, and may even be concentrated in screenings.

Various animal species metabolize mycotoxins in different ways. In pigs,
ochratoxin A can undergo enterohepatic circulation and is eliminated very
slowly, whereas in poultry species it is rapidly excreted. The polar
mycotoxins such as fumonisins tend to be excreted rapidly. Mycotoxins, or
their metabolites, can be detected in meat, visceral organs, milk, and
eggs. However, their concentration in these food products is usually
considerably lower than in the feed consumed by the animals; at these
levels, mycotoxins are unlikely to cause acute intoxication in humans
consuming these products. Residues in animal products of carcinogenic
mycotoxins, such as aflatoxin B1, M1, and ochratoxin A, pose a threat to
human health, and their levels should be monitored and controlled.

In most instances, the principal source of mycotoxins for humans is
contaminated grains and cereals, rather than animal products. This means
that the hazard is much greater in developing countries in which maize and
other grains form the staple diet and the intake of animal products,
including meat, is low.

Only limited information is available regarding mycotoxin residues in
animal products intended for human consumption. The metabolism of
mycotoxins by animals and the residues of mycotoxins and their metabolites
in animal tissues should be studied further.

Infectious Agents

Agent Causing Transmissible Spongiform Encephalopathies in Ruminants

Transmissible spongiform encephalopathies are nonfebrile neurologic
diseases with a long incubation period and are fatal. These diseases are
associated with incompletely defined agents termed prions, which are
resistant to normal heat treatments of feed and food. Sheep scrapie has
been recognized for over 250 years. BSE was first recognized in the United
Kingdom during 1986. For BSE, the infectious agent enters the feed
primarily through rendered infected tissues (notably the central nervous
system and the reticuloendothelial system) under insufficient heat to
reduce the concentration of the infectious agent to an ineffective dose. In
the case of sheep scrapie, infection is naturally maintained by
transmission between sheep. Humans have likely been exposed to the scrapie
agent by eating brain and other tissues, although there is no evidence that
Creutzfeldt-Jakob disease in humans has been associated with scrapie.

Humans can potentially be exposed to BSE through consumption of infected
tissues. The occurrence of a new variant of the human transmissible
spongiform encephalopathy, Creutzfeldt-Jakob disease, has raised the
possibility of an association with the BSE agent. With the limited number
of cases now, there is no proven link between this new variant and the
possible transmission of the agent from infected bovine tissue to humans.
The FAO consultation recommended risk reduction measures to address the
elimination of BSE from cattle.

Salmonella enterica

The more than 2,000 Salmonella serotypes can be divided into three groups:
species-specific, such as gallinarum (in poultry); invasive, which may
cause systemic infections in their host, such as Enteritidis (in laying
hens); and noninvasive, which tend to remain within the intestinal tract.
Members of the first group are infrequently feedborne pathogens. Among the
second group, the principal manifestation of human infection is
gastroenteritis, with septicemia occurring in some patients. The third
group may be associated with subclinical infections in farm livestock; it
sometimes causes disease in livestock and is associated with food poisoning
in humans.

Salmonellae are widely distributed, and animal feed is only one of many
sources of infection for farm animals. Animal feed ingredients of both
animal and plant origin are frequently contaminated with salmonellae,
although the most common serotypes associated with human disease,
Enteritidis and Typhimurium, are rarely isolated from animal feed. Feed can
be contaminated from raw ingredients.

Toxoplasma gondii

The protozoon T. gondii is found in cats and, according to serologic
surveys, also in birds and other domesticated species including sheep,
pigs, goats, and horses. The primary source of infection for animals is
feed contaminated with feces of cats and possibly with rodent tissues.

Cats are an important source of infection for humans; however, some human
infections may be due to the handling or consumption of raw meat. Pregnant
women may miscarry or give birth prematurely, and infants often get central
nervous system disorders and ocular disease.

Trichinella spiralis

T. spiralis is a nematode that parasitizes the intestinal tract of mammals,
particularly pigs. The larvae encyst in the tissues, particularly the
muscles, which act as a source of infection for humans who consume raw or
partially cooked meat. The clinical manifestations include fever, muscle
pain, encephalitis, meningitis, myocarditis, and (rarely) death.

The cysts in infected carcasses can be killed by freezing (-18C for 20
days) or traditional rendering temperatures. Adequate cooking of raw meat
and table scraps before feeding to farm animals would eliminate this
hazard.

The FAO consultation also addressed potential hazards associated with
veterinary drugs and agricultural and other chemicals and recommended risk
reduction measures to prevent, eliminate, or reduce the hazards to
acceptable levels. The consultation participants prepared a draft Code of
Practice for Good Animal Feeding to be considered by the Codex Alimentarius
Commission (CAC).

Codex Alimentarius Commission

Since 1962, CAC has been responsible for implementing the Joint FAO/World
Health Organization (WHO) Food Standards Program. "Codex Alimentarius,"
whose name is taken from Latin and translates literally as "food code" or
"food law," was founded in response to the worldwide recognition of the
importance of international trade and the need to facilitate trade while
ensuring the quality and safety of food for the world consumer.

It follows, therefore, that the commission's primary objectives are the
protection of the health of consumers, the assurance of fair practices in
the food trade, and the coordination of all food standards. Food standards,
guidelines, and recommendations are the work of CAC. With the adoption of
the World Trade Organization's Agreement on the Application of Sanitary and
Phytosanitary Measures and the Agreement on Technical Barriers to Trade, a
new emphasis and dimension have been placed on Codex standards.

Codex Committee on Food Hygiene

The Codex Committee on Food Hygiene (CCFH) has overall responsibility for
all provisions of food hygiene prepared by Codex commodity committees and
contained in commodity standards, codes of practice, and guidelines. CCFH
also develops general principles, codes of practice, guidelines for food
hygiene, and microbiologic criteria for food to be applied horizontally
across Codex committees. Food hygiene is defined as "all conditions and
measures necessary to ensure the safety and suitability of food at all
stages of the food chain."

According to the deliberations at the 29th session of CCFH, the
microbiologic safety of foods is principally ensured by control at the
source, product design, process control, and good hygienic practices during
production, processing, handling, distribution, storage, sale, preparation,
and use, preferably in conjunction with the application of the Hazard
Analysis and Critical Control Points (HACCP) system. This preventive system
offers more control than end-product testing because of the limited
effectiveness of microbiologic examination to assess the safety of food.

When they have been established by Codex or national risk managers,
objectives for food safety can be taken up by industry; by applying HACCP
(or an equivalent food safety management system), industry can ensure that
these objectives are met. This is the use of HACCP as a corrective risk
management option: a risk is identified, and a management option is
selected and implemented. HACCP is also used as a preventive risk
management tool. In this case, hazard analysis identifies potential hazards
in raw materials, production line, and line-environments to the consumer.
Hazard analysis is defined as "The process of collecting and evaluating
information on hazards and conditions leading to their presence to decide
which are significant for food safety and therefore should be addressed in
the HACCP plan." Input concerning the potential hazards and their control
could come from risk analysis, but often such information is not available
and industries need to apply their best judgment.

The Revised Principles for the Establishment and Application of
Microbiological Criteria For Foods states, "Microbiological criteria should
be established according to these principles, and be based on scientific
analysis and advice, and where sufficient data are available, on a risk
analysis appropriate to the foodstuff and its uses." These criteria may be
relevant to the examination of foods, including raw materials and
ingredients of unknown or uncertain origin, and may be used when no other
means of verifying the efficacy of HACCP-based systems and good hygienic
practices are available. Microbiologic criteria may also be used to
determine that processes are consistent with the General Principles of Food
Hygiene. Microbiologic criteria are not normally suitable for monitoring
critical limits as defined in the HACCP system.

Establishing microbiologic criteria and food safety objectives in general
is difficult because of the considerable knowledge gap relating to biologic
hazards and their relationship to human illness. This has led to many
evaluations by CCFH, which are based on subjective or qualitative
assessments and serve as the basis for recommendations. Although aware of
these limitations, CCFH is now developing a framework of principles and
guidelines for the application of microbiologic risk assessment. CCFH's
action was in response to the recommendation of the 1995 Joint FAO/WHO
Consultation on the Application of Risk Analysis to Food Standards relating
to the application of risk assessment within the Joint FAO/WHO Food
Standards Program. International Commission for Microbiological
Specifications for Foods and CCFH delegations are also in the process of
developing background papers on a number of foodborne pathogens to better
conduct quantitative risk assessments and set subsequent food safety
objectives. Notwithstanding the development of risk analysis approaches by
these groups, the work of CCFH and all Codex committees would benefit from
advice from an expert body on foodborne biologic hazards for purposes of
risk management. The committee could be modeled on the FAO/WHO Joint Expert
Committee on Food Additives and Joint Meeting on Pesticide Residues,
allowing for the unique consideration of epidemiologic and clinical data
related to pathogens causing human illness, and of the dynamics of
microbial populations in food throughout the food chain.

Control of Listeria monocytogenes in foods is an example of the need to
consider a structured risk management approach. Listeria are frequently
consumed in small amounts by the general population without apparent ill
effects. Only higher levels of Listeria are thought to cause serious
disease problems. It is believed that Listeria will always be present in
the environment. Therefore, the critical issue may not be how to prevent
Listeria in foods, but how to control its survival and growth to minimize
the potential risk. In many foods, complete absence of Listeria is
unrealistic and unattainable; trying to achieve this goal can limit trade
without having any appreciable benefit to public health. A relevant risk
management option, therefore, is to focus on foods that have historically
been associated with human disease and support the growth of Listeria to
high levels, rather than focusing on foods that do not support growth.
Thus, establishing tolerably low levels of Listeria in specific foods may
be one food safety objective achieved by risk managers after a rigorous and
transparent risk analysis. Such an approach is now being considered by CCFH
after an initial risk assessment by the International Commission for
Microbiological Specifications for Foods and CCFH delegations.

Although Listeria presents unique challenges in terms of its widespread
occurrence and the particular susceptibility of vulnerable groups,
pathogens such as E. coli O157:H7, Salmonella, and Campylobacter are also
being addressed. These microbial pathogens produce acute foodborne
illnesses and can cause severe chronic sequelae, creating an important
public health problem and food safety concerns.

Codex Codes of Hygienic Practice are based on good manufacturing practices,
HACCP principles, and risk analysis. CCFH is responsible for coordinating
and overseeing the work of specific Commodity Committees in this area. In
the specific area of food hygiene, Codex has revised its main document,
Recommended International Code of Practice: General Principles of Food
Hygiene, to incorporate risk assessment principles and include specific
references to the HACCP system.

FAO Programs on Food Quality and Safety

The Food Quality and Standards Service is a service within the Food and
Nutrition Division of the FAO, located in Rome. The Secretariat of CAC is
also located there. The Regular Program of the Food Quality and Standards
Service provides the technical and scientific basis for FAO for all food
quality matters, including food safety. This includes providing the
Secretariat for the Joint Expert Committee on Food Additives and
participation in both the Joint Meeting of the FAO Panel of Experts on
Pesticide Residues in Food and the Environment and the WHO Expert Group on
Pesticide Residues and in the Joint Expert Committee on Food Irradiation.

The Food Quality and Standards Service develops and publishes guidelines
and manuals (including the FAO Food and Nutrition Paper Series and Manuals
of Food Quality Control), arranges expert consultations and conferences
(e.g., the Joint FAO/WHO Expert Consultation on Biotechnology and Food
Safety, September 30 to October 4, 1996; the Joint FAO/WHO Expert
Consultation on the Application of Risk Management to Food Safety Matters,
January 27-31, 1997; the Joint FAO/WHO Consultation on Food Consumption and
Exposure Assessment to Chemicals, February 10-14, 1997; and the FAO
Consultation on Animal Feeding and Food Safety, March 10-14, 1997), and has
a major and continuing program of providing technical assistance regarding
food standards and food control to member countries, particularly
developing countries and countries in transition from a centrally planned
to a market economy.

The Joint Expert Committee on Food Additives, the Joint Meeting on
Pesticide Residues, and the Joint Expert Committee on Food Irradiation are
expert committees that provide independent scientific advice that forms the
basis for the development of food safety recommendations used in
international trade. These committees are forums in which independent,
invited experts assess the state of scientific knowledge of food additives,
pesticide and veterinary drug residues in food, mycotoxins, other chemical
contaminants in food, and food irradiation treatments and make
recommendations to member governments and to Codex.

FAO's Food Quality and Standards Service also develops and publishes
Manuals of Food Quality Control. These manuals provide recommendations for
the development and operation of food quality and safety systems. While
aimed primarily at providing advice to developing countries, the manuals
document modern approaches, including the development of quality control
programs throughout the food chain that apply to all countries. Such an
approach is instrumental in facilitating international trade in food. Key
titles in the series include Food Inspection, Food for Export, Management
of Food Control Programs, Imported Food Inspection, and Quality Assurance
in the Food Control Laboratory.

The program of technical assistance projects undertaken by the Food Quality
and Standards Service handles assistance in food quality control, including
safety; such projects have established or strengthened the food control
systems in a number of developing countries. Typically, they assist in
establishing the infrastructure for an enhanced food control program,
assessing laboratory service requirements, providing guidance to develop
legislation and procedural manuals, setting up reputable inspection and
certification systems, and providing training and staff development. In
these assistance projects, the standards established by the CAC are basic
guides to international requirements.

Conclusion

Food will always represent some biologic risk; it is the task of the food
industry to maintain the level of risk at the minimum that is practical and
technologically feasible. It should be the role of regulatory bodies to use
risk assessment to determine realistic and achievable risk levels for
foodborne hazards and to base their risk management and food safety
policies on the practical application of the results of these analyses.

Foodborne illnesses are preventable. Adherence to good manufacturing
practices and good hygienic practices and application of the HACCP system
can result in food safety and ensure food quality. Food safety is the
shared responsibly of governments, academia, the food industry, and the
consumer.

Codex standards, guidelines, and recommendations have the objective of
protecting the consumer and facilitating international food trade.
Adherence to Codex provides the basis for food safety and quality and meets
the requirements of international trade.

Address for Correspondence: Gregory D. Orriss, Chief, Food Quality and
Standards Service; Food and Nutrition Division; Food and Agriculture
Organization of the United Nations; fax: 39-6-5705-4593; e-mail:
Gregory.Orriss@fao.org.
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Emerging Infectious Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Atlanta, GA