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Where we are in retail food safety, how we got to where we are, and how do we get there? (Guest Commentary).

Where We Are in Food Safety

It is often said that the United States has the safest foods in the world. But is this really so? We receive foods that are produced, harvested, and processed in many regions of the world. Some production and harvesting sites are in countries and regions that are underdeveloped economically and that lack modern sanitary facilities. Only a few incoming foods are ever subjected to testing, and any testing is limited to a few pathogens if any at all. Furthermore, a negative test does not mean that food is free of contamination; it only means that the contaminant sought was not detected in the number and size of samples tested. Our foods may be subject to more stringent regulations (e.g., Food and Drug Administration [FDA], U.S. Department of Agriculture [USDA], state, and local regulations) than foods in many other countries. But it must be recognized that (a) the largest foodborne-disease outbreak in history occurred in this country; (b) hundreds of outbreaks and tens of thousands of cases are investigated and reported each year, and reporting of gastroenteritis is poor; (c) scores of deaths have occurred in some out-breaks; (d) high estimates are made for the incidents (tens of thousands) and deaths (thousands) associated with foodborne disease in this country; and (e) the costs of the outbreaks to those afflicted and their families, to the food industry, and to insurance companies are high.

Reported Outbreaks

Surveillance data from the Centers for Disease Control and Prevention (CDC) on the incidence of foodborne-disease outbreaks in the United States from 1993 to 1997 show results similar to those of previous summaries (Olsen, MacKinon, Goulding, Bean, & Slutsker, 2000). The number of annual outbreaks ranged from 477 to 653, and the number of associated cases ranged from 11,940 to 22,607. Typically, the largest percentage of outbreaks of known etiology (75 percent) and the largest percentages of cases of known etiology (86 percent) were bacterial. Salmonellosis, led by Salmonella enteritidis infections, accounted for the highest percentage of bacterial outbreaks and cases. The next most common etiological agents were Escherichia coli, Clostridium perfringens, Staphylococcus aureus, and Shigella. Diseases in the so-called chemical-agents category (which is a misnomer because over half are scombroid poisonings with bacterial causes) and animal or plant toxins accounted for 17 percent of outbreaks and 1 percent of cases. Viral agents accounted for 6 percent of outbreaks and 8 percent of cases. Parasites accounted for 2 percent of outbreaks and 5 percent of cases. Therefore, the problem reported by CDC is primarily caused by bacteria, which has been the major problem in previous summaries.

Other data in the CDC foodborne-outbreak summaries are of limited value because of the way they are classified. The place foods were eaten was usually a food service establishment, and the next most common place was private residence. This information, however, does not directly relate to the places where foods were contaminated and/or mishandled, which is the information that would be useful for planning preventive measures. Food vehicles are often grouped into general categories, which provides minimal information about the source and type of contamination and about the intrinsic nature of the food or extrinsic environment that contributed to survival and propagation of the etiological agents. Fishes other than shellfish, for example, often rank high as vehicles, but if vehicles associated with ciguatoxin and scombrotoxin (which are fishborne and affect only the few persons who eat the toxigenic fish) are subtracted, the numbers drop considerably. Figures on the categories of salads (other than potato, pou ltry, fish, and egg), fruits, and vegetables are often high. In such situations, the data should be broken down to assign specific foods as vehicles and give some idea of the nature of the problem.

Data on contributing factors are grouped into very general categories, and, therefore, it is difficult to identify specific operations that failed or were improperly done. The category of improper holding temperatures was the most common contributory factor each year. This category, however, is so general that it gives little information about whether the mishandling involved (a) holding at room or warm outdoor ambient temperatures, (b) holding in steam tables or hot-holding cabinets, (c) slow cooling, (d) thawing, (e) holding at improper cold storage temperatures, or (f) time of holding. There are significant differences in these operations about preventive and control actions. The data need to be separated into these (a-f) subcategories. Inadequate cooking and reheating practices are not specified. The poor-personal-hygiene category is too vague to interpret the improper actions or health status of workers. Furthermore, the data come from boxes checked on a report form, which are often unrelated to factors stated in the narrative reports. Potentially, the database could be quite revealing about the causative and contributing factors associated with outbreaks, but it, as in the past, lacks effective categorization, definition of terms, and specificity The factors must relate to specific operations where preventive and control measures can be applied (Bryan, 1988). These matters have been critiqued and recommendations given, and they could be repeated (Bryan, Guzewich, & Todd, 1997; Bryan, Todd, & Guzewich, 1997; Guzewich, Bryan, & Todd, 1997; Todd, Guzewich, & Bryan, 1997). The new Investigation of a Foodborne Outbreak Form has been improved to collect more useful data (CDC, 2000)

Laboratory-Confirmed Incidence

Another approach being taken by CDC is the FoodNet, based on surveillance for laboratory-confirmed cases of diseases caused by Campylobacter Escherichia coli O157, Listeria monocytogenes, Salmonella, Shigefla, Vibrio, and, in some regions, Cryptosporidium spp. and Cyclospora cayetanensis (Shallow et al., 2001). The data refer to laboratory-confirmed incidence of the diseases, but the diseases have not been confirmed as foodborne, although the presentation of the data implies this. Many of these agents are transmitted by person-to-person spread. Others can be transmitted by contact with animals. Others may be waterborne. Despite the limitation of the data relative to foodborne transmission, valuable information has been accumulated. From 1996 to 2000, Campylobacter was the most commonly diagnosed infection from the list, accounting for 17.5 to 25.2 percent of the reports. It can be acquired by handling foods, carcasses, raw poultry and meats, and perhaps animals, as well as by ingestion of foods. Next in perce ntages is Salmonella, ranging from 12.0 to 14.5 percent. Salmonellae are usually foodborne, but these bacteria also can be spread by direct contact with animals. Shigella ranked next, with 5.0 to 11.6 percent of the diagnoses. Shigellosis often is not foodborne; it is more commonly spread person to person. Escherichia coli O157, at 2.1 to 2.9 percent, and Cryptosporidium, at 1.8 to 3.7 percent, followed in the ranking. The former has a fecal-oral route of transmission, and the latter is more commonly transmitted by water than by foods. Data from these sources are extrapolated for the nation, and they are used to estimate the incidence of foodborne disease. This approach has many limitations. One is that the information comes from approximately 10 percent of the population, and there is substantial local variation, which may not be representative nationally. Another is that the data are from laboratory isolations, and most foodborne illnesses are neither laboratory confirmed nor reported to health departments. Not all laboratories test for all of the pathogens, and there are variations in testing protocol. Also, the source of infections may be from nonfood routes (e.g., water, person-to-person contact, animal contact).


Current estimates for known foodborne pathogens are that there are 38.6 million "foodborne" illnesses each year, which is similar to some previous estimates (Shallow et al., 2001). Hospitalizations attributed to foodborne illnesses are estimated to be 60,854 per year (a little over 1.5 percent). Deaths from foodborne transmission are estimated to be 1,809. (That number is down considerably from a previous estimate of 9,000. It is quite high, however, compared with the deaths identified during outbreak investigations. And where are the lawsuits and the crisis presented by the media, if indeed these estimates are correct?) There must be caution in interpretation of these data as real incidences. They are estimates based upon available databases and assumptions.

On the basis of multiple surveillance systems and other sources, CDC epidemiologists have made even higher estimates: approximately 76 million illnesses, 325,000 hospitalizations, and 5,000 deaths (Mead et al., 2000). These higher numbers are based on foodborne illness caused by pathogens or agents that have not yet been identified and undiagnosed. Many common pathogens today were not recognized as causes of foodborne diseases two decades ago. Even greater assumptions are made to derive these estimates.

Out-of-Compliance Risk Factors

To develop an inspection database, each of 20 regional food specialists made inspections of five of nine types of retail food facilities (FDA, Retail Food Program Steering Committee, 2000). The facility types were hospitals, nursing homes, elementary schools, fast-food restaurants, full service restaurants, and the deli, meat and poultry, produce and salad bars, and seafood departments of food markets. A total of 900 establishments were inspected. Inspection items related to the CDC contributory (risk) factors were evaluated during the visits. The evaluation was on whether the items were in compliance or out of compliance with the Food Code. Of particular interest is that if an operation related to the item was neither occurring nor applicable, it was not included in the counts and was classified as either not observed or not applicable. In the "improper holding time and temperature" category (15 inspection items evaluated), out-of-compliance finding varied by type of facility from 32.0 to 63.2 percent. In th e "poor personal hygiene" category (five inspection items evaluated), out-of-compliance findings ranged, by type of facility, from 15.8 to 53.4 percent. In the "contaminated equipment and protection from contamination" category (five inspection items evaluated), out-of-compliance findings varied by type of facility from 11.0 to 43.6 percent. Inadequate cooking (12 inspection items evaluated) was not observed often (60 percent of visits); hence, individual operations were not evaluated frequently. When this problem was observed, less than 10 percent of the observations had out-of-compliance findings. Full-service restaurants had the highest out-of-compliance percentages. This is not surprising because these restaurants (a) prepare more types of foods; (b) have a multiple sequence of operations, any of which could go wrong; (c) often have the greatest number of employees; and (d) use the greatest numbers of equipment units. Therefore, they have greater opportunities for out-of-compliance situations. The most si gnificant out-of-compliance individual item was potentially hazardous foods cooled to 70[degrees]F in two hours and then to 41[degrees]F in an additional four hours. This item was out of compliance 73 percent of the time. If these data are compared with factors that commonly contribute to foodborne-disease outbreaks (Bryan, 1988), those commonly found out of compliance or not able to be evaluated are frequently the same as the contributory factors.

Conclusion of Where We Are in Food Safety

So where are we regarding food safety? We are somewhere between reasonable sanitation within establishments and assurance of food safety. We are beyond gross lack of sanitation and at aesthetic values that are satisfactory to most of the public. Building construction and facilities, and equipment design, construction, and layout are good, with a few exceptions. Regulations and their enforcement have improved the sanitation level in the food industry. Some food workers and supervisors have been trained in food sanitation and related topics, though many have not. Nevertheless, contaminated foods are sold in retail markets and reach kitchens in food service establishments and homes, and outbreaks of foodborne diseases occur from foods prepared in food service and catering establishments. So the objective of retail food safety has not yet been attained. The approaches used so far, while improving the retail food environment and some operations, have failed to attain the objective of preventing foodborne diseases, which is what food safety is all about.

How We Got to Where We Are

The standard of living in this country is relatively high. This has aided in acquiring the present physical facilities in retail establishments. Public-health agencies have improved foodborne-disease surveillance to detect ecological agents that cause some of the illnesses, and many food vehicles and factors that have contributed to outbreaks have been identified. Food regulatory agencies have developed regulations and inspection protocols, and these have been updated on the basis of outbreak information, research, observations, and interpretations during inspections, food industry technology, and consultations from persons knowledgeable about food operations and risks. Significant activities that have been carried out to attempt to make foods safer are discussed in the subsections below.

Foodborne-Disease Surveillance Data

We obviously have not attained retail food safety since foodborne-disease outbreaks are still occurring. Besides those reported, many illnesses never come to the attention of health authorities. Many persons who develop gastroenteritis neither seek medical attention nor complain to health authorities. Even when medical assistance is sought, reports to health authorities are not always made. All reports are not investigated, and many of those that are investigated do not result in a conclusion as to (a) vehicle, (b) the mode of contamination and/or the source, and (c) the way the pathogen survived processing and grew to quantities sufficient to cause illness. The iceberg effect is obvious for foodborne-illness reporting.

Data have shown that when outbreaks are investigated, the places of mishandling or mistreatment of the foods are commonly food service establishments. The proportion has been as high as 75 to 80 percent of reported outbreaks. At these places, infected or pathogen-colonized workers have sometimes contaminated foods that are not subsequently heated. This has been done primarily by touching foods, which are not subsequently cooked, with bare hands. Furthermore, worker practices have lead to cross-contamination from raw to cooked foods via hands or equipment and utensils that contact the foods. The contaminated raw foods may be insufficiently cooked, or cooked foods may be insufficiently reheated to attain time-temperature exposures sufficient to kill the pathogens present. Afterward, the foods may be held under conditions that are conducive to bacterial growth for durations sufficient to allow massive populations of pathogenic bacteria or toxins to generate. All of the blame, however, cannot be given to food ser vice establishments. Incoming raw foods may be (and frequently are) contaminated. If this were not so, many pathogens would be absent from the foods and kitchen environment, and thus no outbreaks would occur, despite some forms of mishandling. Contaminated incoming foods can contribute to the spread of contaminants to other foods, and mishandling follows. Therefore, retail food safety awaits further improvements in production, harvesting, processing, and preparation practices.

Food Sampling and Testing

Food sampling and testing of foods sound like a panacea to laymen and some regulators: Examine finished food products, and if pathogens are found, either eliminate the foods for human consumption or treat them to render them safe. But it just doesn't work that way There are many reasons for this. The most significant is that a sufficient number of samples is not collected to give a high confidence that the product under investigation is not contaminated. For example, three samples showing negative results for the pathogen under investigation give 95 percent confidence that the lot or batch is 75 percent or less contaminated. Even 60 samples showing negative results only give this level of confidence that the lot or batch is 5 percent or less contaminated. It would take 300 negative samples to provide this level of confidence that the lot or batch is 1 percent or less contaminated. These figures assume homogeneous contamination. If contamination is not homogeneous, there is even less confidence in the results. Of further concern is that tests are not available or not routinely done for all possible contaminants. Often, indirect tests are used, testing for indicator organisms rather than for the pathogens, and these tests often have no hearing on the presence of certain pathogens. Furthermore, the sample collected may not contain the pathogen even though the product is contaminated, or too small a quantity of sample may be taken to recover the pathogen. If there is improper handling of the sample, the pathogen may decline, die off, or be outgrown by other microorganisms. The media used, incubation temperature and time, confirmatory tests, or other laboratory actions may be inappropriate for detection of the pathogen under consideration. Therefore negative results give a false sense of security if they are interpreted as meaning that the product is free of the microorganism sought. In addition, corrective actions cannot begin until the results of the tests are received, which is often a few days or a week or longer after samples are collected. This is a particular problem for retail foods, which would be sold or eaten before results would be received. Furthermore, the shelf life of the foods remaining from the batch sampled would be shortened. If end-products are tested and found defective, then a hazard analysis of all previous operations and appropriate testing at some of these have to be done to detect the problem. Furthermore, the costs of analyses are high.

Swabbing and Testing of Utensils

A few decades ago, swabbing of eating and drinking utensils was done to evaluate microbial counts on their surfaces. If standards were exceeded, the cleaning procedures for the utensils were considered unsatisfactory. Although this procedure no doubt aided in improving dish washing and equipment cleaning, it fell into disuse because of the delay of a few days before results were available and the cost of laboratory analyses. Improved technology, however, has resulted in more rapid testing. The same sampling limitations as stated for foods apply More effective evaluations can be achieved by watching cleaning operations and supplementing observation with single physical tests. Priority of inspections in most jurisdictions is now on foods and handling procedures rather than on utensils and equipment.

Inspections and Enforcement of Regulations

Most present-day food safety measures rest on inspections and enforcement of regulations, yet there are still many outbreaks (Olsen et al., 2000) and many out-of-compliance situations (FDA, Retail Food Program Steering Committee, 2000). Something just isn't working as wanted and planned. With the inspection approach, hazards are identified only when inspections are made, which may be hours, days, or months after the first occurrence of the hazards. Multiple hazards may occur, and some even disappear during intervals between inspections. Furthermore, inspections seldom are made during weekends or evenings, at which times contamination and mishandling can occur. Interpretations of code requirements and satisfactory compliance, and the operations or facilities given attention may differ with different inspectors or in different jurisdictions. Therefore, some, or perhaps many, hazardous situations may be missed. The greatest limitation of the inspection approach, however, is that the hazards, or even the operatio ns in which the hazards are likely to occur (and which are considered the critical control points), may not be occurring, or the foods associated with the hazards may not be processed or prepared, at the time of the inspection and thus may not be evaluated. Yet an unchecked item on an inspection form implies satisfactory compliance or gives operators this impression. In this regard, check sheets should have a column that shows whether an operation was evaluated during the inspection. On a score sheet, points should not be awarded for operations that were not evaluated. The duration in an establishment may not allow time for education of persons responsible for the deficiency. Corrective actions await identification of hazards during inspections and willingness of the operators and workers to make changes based on the recommendations given or to otherwise correct the condition and carry out preventive measures.

Food Codes

The Food Code has changed emphasis over the decades, from an emphasis on physical facilities to an emphasis on sanitation of the facilities, equipment, utensils, and tableware (i.e., cleaning and disinfection) to an emphasis on protecting foods from contamination; now it is covering measures to kill pathogens and to minimize chances of rapid and progressive growth of bacteria on or in the foods. The latest code and its periodic revisions put more emphasis on microbial controls (FDA, 1999; FDA, Retail Food Program Steering Committee, 2000). These are to minimize contamination, reduce or kill pathogens on and in foods, and prevent or delay propagation of pathogens.

Nevertheless, the regulations still need modifications to be directed at prevention and control of foodborne pathogens. A few time-temperature code criteria can be critiqued. For example, there is a questionable effect in killing of pathogens when unspecified foods are cooked to a temperature of 145[degrees]F and held for 15 seconds, This time-temperature exposure, according to the public-health reasons given for the criterion, is apparently set for a small reduction (i.e., 3-decimal [3D] reduction--that is, 99.9 percent) of salmonellae in liquid eggs. (Typical decimal reductions range from 5 to 12D.) Pasteurization of liquid eggs practices, however, are to heat to 142[degrees]F and hold for 3.5 minutes, and to heat 10 percent sugared or salted yolks to 146[degrees]F and hold for 6.2 minutes. Solid or more viscous foods and those with a greater likelihood of contamination need more stringent criteria. The different time-temperature values for different foods relate to heat resistance of the pathogens of conc ern and characteristics of the food (e.g., thickness of mass, solid or liquid and viscosity, amount of water and fat). For solid meat products, criteria similar to that for roast beef should apply The current criteria would not even reduce salmonellae in such products by 1D (90 percent). Remember, the criterion for vat pasteurization of milk is 145[degrees]F for 30 minutes.

If a pork product is being cooked, a regulation may be aimed at the destruction of trichinellae. The hazards under consideration, however, ought to include at least salmonellae and yersiniae, which are more heat resistant than parasites and are common contaminants of pork. Therefore, time-temperature exposures must be increased over that stated in a trichina-kill regulation. Something similar to the roast beef criterion should apply.

Criteria, in general, relate to destruction of salmonellae, but there are other pathogens (e.g., Listeria monocytogenes) that are more heat resistant. Some present standards are questionable in giving a 5D reduction of pathogens of concern in the specified foods.

Furthermore, the time-temperature values relate to moist foods, and foods that have less moisture (decreased water activity) because of drying, dehydration, or addition of solutes require considerably higher temperatures or longer exposures. For example, the [D.sub.145] for salmonellae is 0.7 minutes for roast beef, a high-water-activity product; but the [D.sub.158] for salmonellae varies from 720 to 1,050 minutes for milk chocolate, a low-water-activity product. This is more than a thousand times higher.

Specifications for monitoring (including site or location to monitor in or on foods, when to monitor, how to monitor, and instruments to use) are not given. These should be specified for every time-temperature criteria. They may differ for different foods cooked in different devices. Although the geometric center is a common site to evaluate, the site for monitoring should be at or near the surface for microwave-cooked foods.

There is a dichotomy concerning cooking and hot holding. Some temperatures specified for cooking are below that required for hot holding. How can kill temperatures be hazardous during hot holding?

Some foodborne pathogenic bacteria (e.g., Listeria monocytogenes, Clostridium botulinum Type E, and Yersinia enterocolitica, Aeromonas hydrophila) can multiply at temperatures below that specified in the regulation (41[degrees]F/5[degrees]C). Refrigerated storage can impede or delay microbial growth by prolonging the lag phase and limiting the rate of log-phase multiplication of pathogens at low temperatures. Therefore, either a lower temperature criterion or limiting the duration of storage must be used as a critical limit when these bacteria are considered as hazards for the foods under consideration.

The two-temperature criteria for cooling are good. Evaluating cooling to 70[degrees]F is practical within the duration of some inspections or verification visits and for workers in an establishment, although 60[degrees]F might be considered a better first-temperature criterion. Below these temperatures, bacterial growth slows as temperatures decrease. To attain either criterion, however, either rapid cooling techniques must be used or shallow layers must be placed in pans that have no lids or that allow rapid transfer of heat. The second part of these criteria, however, is more difficult to attain under conditions that employ air cooling. Cooling rates decrease as food temperatures approach the ambient temperature of the cooling medium. The shortening of the cooling time required and the lowering of the required unit temperature (which is not a bad decision) complicate this. Most air-cooling procedures for most foods are going to violate this criterion. Therefore, either the situation will have to be left une valuated or ignored, which is often the case, or the time criterion extended or effective rapid cooling specified and air cooling restricted to very shallow layers of foods under specified conditions.

Some rationales specified in public-health reasons must be questioned. It is hoped that these and other regulation deficiencies will be corrected as the regulations are periodically modified. Knowledge of food microbiology and related rational attitudes must override ignorance and desires by some persons to subjugate or circumvent regulations.

On-Site Hazard Analyses and Resulting Recommendations to Prevent Microbial Hazards

Hazard analyses have been done as (a) a part of epidemiologic investigations to identify food vehicles and the events that led to outbreaks (b) as an initial phase for setting up hazard analysis critical control point (HACCP) systems, and (c) as a means to determine ongoing conditions that relate to food safety. Hazard analyses evaluate sources and modes of contamination, survival, or destruction of pathogens, and growth and propagation of foodborne pathogens. Such analyses should be done for all potentially hazardous products and should cover receiving and storage of the primary product and ingredient and all steps in processing and preparation until the foods are eaten, sold, or delivered. The analyses should consider operations from the start to the finish and include clean-up activities. In addition, the operators and evaluators should be cognizant of preceding processing and anticipated subsequent handling that can affect contamination, survival, and growth, and should modify processing, if necessary, to counter the effects of these. These analyses use (a) observations of operations, (b) measurements of time and temperatures, (c) measurements of intrinsic characteristics of foods and ingredients (e.g., pH, water activity, microbial contents), and (d) sampling of foods after critical operational steps. The hazards upon which to concentrate are the factors that have contributed to food-borne-disease outbreaks. These are listed in the sidebar on page 34 (Bryan, 1988; Bryan, Guzewich, & Todd, 1997). The major limitation of this approach is that it is underutilized. Other limitations are the need for certain instruments, equipment, and support facilities, and the time it requires. The analyses must be done by knowledgeable, technically competent personnel who have appropriate equipment and access to testing laboratories.

On-site Monitoring of Preventive or Control Measures and Prompt Corrective Actions at Operations (Critical Control Points) Where Hazards Are Likely to Occur and Where Risks of These Are High

This is what the HACCP concept was meant to do. But with its utilization, many other aspects of regulations and records have made a concept that was meant to be a direct and simple approach to food safety quite complex. And it appears that this trend is going to continue. The term has acquired the meaning "total food protection" and everything that must be done toward this end, rather than its initial meaning of determining and monitoring a few operations where control can be accomplished. Perhaps we need to return to the original three components of the HACCP concept as set down by the International Commission on Microbiological Specifications for Foods (International Commission on Microbiological Specifications for Foods, 1988). These are hazard analysis, critical control point identification, and monitoring. The process was to evaluate foods and their processing and to identify hazards and assess their risks, It continued by determining one or a few operations that were critical for control (called critica l control points). Criteria to ensure food safety at that operation were established, and the operation monitored to ensure that the criteria were met and promptly corrected if they were not. If this system is properly designed, carried out, and maintained, there ought to be high assurance of food safety, despite possible aesthetically undesirable situations.

Applied Research and Challenge Testing

Because of information uncovered during outbreak investigations, hazard analyses, serendipitous observations, and scientific curiosities, applied research and challenge testing are ways by which hazards can be identified, risks assessed, and control measure evaluated. Over the past few decades, much has been learned about the epidemiology, ecology, microbiology, and chemistry of foodborne pathogens and toxins by these means. These activities need to be intensified and the results communicated to those who need to know.

Training of Public-Health and Food Regulatory Personnel

Personnel hired as sanitarians and inspectors have a variety of educational backgrounds and experience. In some agencies, public-health and food regulatory personnel are given very little initial training, other than perhaps a set of regulations to read and the instruction to go out and look for violations. Some have not been taught the scientific principles necessary to understand the rationale for regulations and their interpretations. Others may be initially educated or trained satisfactorily to do the job, but they are not stimulated and updated by periodic refresher training. At the current rate of reported and estimated incidence of foodborne disease and out-of-compliance code situations, there is an obvious deficiency in recruitment, education, training, and/or supervision of public-health and regulatory personnel or inappropriate focus of programs. Training is an investment in attaining the objectives of food safety.

Training of Food Workers, Supervisors, and Managers

Much of what was stated for training of public-health personnel applies to the food industry. In addition, these individuals must be aware of hazards that are associated with the foods they prepare, and procedures and criteria to maintain the foods in a safe state or to render them safe. Food workers in some regions are required to have a basic knowledge of food safety, but this is not universally the case. Others have undergone a few hours of classroom training, read a manual, or watched company videos on the subject. Some have had more extensive training and have been certified as having completed the training. All the training received is positive, but there is still a lack of either training, understanding, recall, or supervision that allows the events leading to foodborne-disease outbreaks and out-of-compliance code situations to occur.

Education of the Public

Although the American public (other than some immigrants from developing countries) has basic education, that education does not cover elements of food safety very extensively. The economy is such that most of the population have facilities for personal hygiene, cleaning, cooking, and refrigeration in their homes, and they have at least a basic understanding of their uses. Public-health agencies and university cooperative-extension services have prepared a variety of materials that help inform the public about hazardous food-handling and storage procedures and preventive measures. These materials are seen, however, by only a small percentage of the public and are put to use by even a smaller percentage. The mass media subject the public periodically to reports of crises and sometimes present brief guidelines for improving behavior. These announcements, as often presented, however, can lead to panic rather than learning. Consumer groups also may act on issues related to food safety, but they may have a political agenda or policies that are scientifically unsound or technically impractical or unreasonable. The public is expected to modify behavior based on these messages, which may appear conflicting.

The public must understand that (a) foods brought into their kitchens are often contaminated with foodborne pathogens, (b) there are no zero risks, and (c) they must be responsible for the safety of foods within their kitchens just as the food industry should be responsible for the foods before they reach the kitchens and when they eat out. It is the responsibility of consumers to kill the incoming pathogens by thorough cooking, to minimize spread of the contaminants by sanitary practices, and to prevent growth of bacteria by prompt and effective refrigeration. These issues should be the thrust of consumer education by governmental agencies, school systems, the food industry, and consumer groups.

Conclusion to How We Got to Where We Are

Where we are in food safety is the result of varying degrees of the efforts discussed above and related ones. Despite these efforts, we have not yet attained food safety in retail establishments.

How Do We Get There? (Or: How Do We Attain Food Safety?)

All foodborne diseases are preventable, but there are no zero risks.

First, we can attain a high degree of food safety by using common (microbiological) sense and by understanding the following principles--"Doctor Bryan's Laws of Practical Food Microbiology and Food Safety (And How We Understand and Solve Foodborne-Disease Hazards)":

1. Raw foods must be considered to be contaminated. Raw foods can be expected to be contaminated with a variety of microorganisms, some of which can cause foodborne illness. These include raw vegetables, fruits, grains, and spices, as well as raw products of animal origin. There are few practical ways to avoid their contamination. There is, at best, low assurance that pathogens are absent, despite present-day food production and processing technologies, and inspection and testing activities. These actions can minimize or reduce but not eliminate contamination.

2. Spores survive cooking. Spore forms of bacteria usually survive routine cooking/heat processing and reheating. Therefore, the process must be designed to kill spores (e.g., retorting), or we must expect that, after the heating step, spores will be present.

3. Vegetative forms of foodborne pathogens also may survive heating. Principle 1 indicates the risks of eating raw foods and suggests the importance of a kill step during processing or preparation. Vegetative forms of microorganisms, however, may or may not survive cooking/heat processing and reheating, depending on time-temperature exposures of the foods. This exposure is influenced by the intrinsic characteristics of the food (e.g., its pH and water activity), initial microbial population types and quantity, thickness of food mass, and viscosity of the food.

4. Some microbial toxins are heat stable. Certain bacterial toxins (e.g., staphyloenterotoxin, the emetic toxin of B. cereus, histamines) survive reheating (e.g., boiling). If these toxins are allowed to generate during storage, reheating cannot be expected to render the foods safe.

5. Post-heating contamination can readily occur. Foods, particularly cooked/heatprocessed foods, can readily become contaminated when they are touched either by bare hands or by hands, gloves, or equipment or utensil surfaces that previously (and without intervening thorough washing) contacted raw foods. In addition, cleaning cloths and cleaning aids can spread contaminants, and when they remain damp for long durations, bacteria can multiply on them. Contamination can be spread from other environmental sources (e.g., contaminated cooling or cleaning waters, aerosols, dust, splash, drippage, back-siphonage), but typically these are minor sources compared with raw incoming foods and the bare hands of workers.

6. Pathogenic foodborne bacteria can multiply in foods. If cooked foods are contaminated by bacterial spores, the spores may germinate, and the resulting vegetative cells, as well as those bacteria that subsequently reach the foods, will multiply--

if the foods contain essential nutrients; have a pH, a water activity ([a.sub.w]), and a redox potential at which the bacteria can multiply; and do not contain sufficient quantities of inhibitory substances or competitive microorganisms that inhibit growth of pathogens--

if given enough time within a temperature range at which the bacteria can multiply. Temperatures close to the optimum at which the bacteria multiply will result in the most rapid increase in populations. The multiplication rate decreases progressively as temperatures move toward the maximum and minimum limits.

7. Bacteria can multiply in foods even during refrigerated storage. Bacteria will multiply in large masses of foods and in foods that are stored in large containers (i.e., greater than 3 inches, or greater than 7.5 centimeters) while in refrigerators. Lids impede cooling. When lids are used, food depths must be reduced to compensate. Stacking of pans impedes air circulation. Furthermore, even in properly stored foods, some foodborne pathogens (e.g., Listeria, Yersinia, Aeromonas, and non-proteolytic varieties of Clostridium botulinum) can multiply at temperatures below 41[degrees]F (5[degrees]C), but their growth rate is slow

8. Foodborne diseases are expensive. In addition to suffering caused by illness, sometimes hospitalization, and occasionally deaths, the economic impact of foodborne illness can be quite high to the patient and family, and to the place where the implicated foods were produced, processed, prepared, and served.

9. Murphy's Law is always apt to apply. That is: "If something can go wrong, it will"-- and someday something wrong will occur unless effective food safety measures are designed into an operation, are implemented, and are maintained.

10. Foodborne diseases are preventable. For prevention to occur, however, all persons involved with food production, distribution, processing, preparation, and storage must (a) be aware of the hazards associated with their (and previous and subsequent) operations, (b) employ means either to prevent or control the hazards, (c) set control limits (criteria) at vulnerable operations (critical control points), (d) monitor operations at the critical control points, and (e) immediately correct deviations from established criteria or when the operation gets out of control. This is implementation of the HACCP system (without confusion and intermixing of less important issues that relate to aesthetics and general sanitation) for all potentially hazardous foods.

These principles apply for all foods during all phases of food production, processing, and preparation. They are certainly applicable for retail foods. With an understanding of them, we are prepared to take the food safety measures given in the 10th principle.

Second, to attain food safety, attitudes must change from "We have the safest foods in the world" to "We have some problems (hazards and risks) that must be defined and addressed." Our present food protection programs, while developed to a rather high level of sophistication, have not achieved the degree of food safety that is desired. The "inspection mentality" must be modified to a rational and science-based attitude to determine hazards and assess their risks. This change must be followed by focusing on and putting into effect preventive and control measures of (a) eliminating or killing pathogens or otherwise excluding or reducing contamination, (b) inhibiting or delaying growth of pathogenic bacteria and toxigenic molds, and (c) preventing or minimizing contamination. So change is necessary!

Bryan, F.L. (1988). Risks of practices, procedures and processes that lead to outbreaks of foodborne diseases. Journal of Food Protection, 51(8), 663-673.

Bryan, F.L., Guzewich, J.J., & Todd, E.C.D. (1997). Surveillance of foodborne disease. Part III: Summary and presentation of data on vehicles and contributory factors, their value and limitations. Journal of Food Protection, 60(6), 701-714.

Bryan, F.L., Todd, E.C.D., & Guzewich, J.J. (1997). Surveillance of foodborne disease. Part II: Summary and presentation of descriptive data and epidemiologic patterns, their value and limitations. Journal of Food Protection, 60(5), 567-578.

Centers for Disease Control and Prevention. (2000). Investigation of a foodborne outbreak (Form CDC 52.13). Atlanta, GA: Author.

Food and Drug Administration, Retail Food Program Steering Committee. (2000). Report of the FDA retail food program database of foodborne illness risk factors. Washington, DC: Author.

Food and Drug Administration. (1999). Food code. Washington, DC: Author.

Guzewich, J.J., Bryan, F.L., & Todd, E.C.D. (1997). Surveillance of foodborne disease. Part I: Purpose and types of surveillance systems and networks. Journal of Food Protection, 60(5), 555-566.

International Commission on Microbiological Specifications for Foods. (1988). Microorganisms in foods 4. Application of the hazard analysis critical control point (HACCP) system to ensure microbiological safety and quality. Oxford, England: Blackwell Scientific Publications.

Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M., & Tauxe, R.V. (2000). Food-related illness and death in the United States. Emerging Infectious Diseases, 5(5), 1-39.

Olsen, S.J., MacKinon, L.C., Goulding, J.S. Bean, N.H., & Slutsker, L. (2000). Surveillance for foodborne disease outbreaks--United States, 1993-1997. Morbidity and Mortality Weekly Report, 49(SS01), 1-51.

Shallow, S., Samuel, M., McNees, A., Rothrock, G., Vugia, D., Fiorentino, T., Marcus, E., Hurd, S., Mshar, P., Phan, Q., Cartter, M., Hadler, J., Farley, M., Baugbman, W, Segler, S., Lance-Parker, S., MacKenzie, W, McCombs, K., Blake, P., Morris, J.G., Hawkins, M., Roche, J., Smith, K., Besser, J., Swanson, F., Stenzel, S., Medus, C., Moore, K., Zansky, S., Hibbs, J., Morse, D., Smith, P., Cassidy, M., McGivern, T., Shiferaw, B., Cieslak, P, Kohn, M., Jones, T., Craig, A., Moore, W, Food Safety and Inspection Service, U.S. Department of Agriculture; Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration; Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases; Parasitic Diseases Epidemiology Branch, Division of Parasitic Diseases, and Office of Director, National Center for Infectious Diseases, Centers for Disease Control and Prevention. (2001). Preliminary FoodNet data on the incidence of foodbome illnesses--Selected sites, United States, 2000. Morbidity and Mortality Weekly Report, 50(13), 241-246.

Todd, E.C.D., Guzewich, J.J., & Bryan, F.L. (1997). Surveillance of foodborne disease. Part IV: Dissemination and uses of surveillance data. Journal of Food Protection, 60(6), 715-723.

RELATED ARTICLE: Important Factors That Contribute to Foodborne-Disease Outbreaks, Classified According to Categories of Contamination, Survival, and Growth *


* Pathogen-colonized person touching with bare hands cooked/heat-processed foods or foods not subsequently heated

* Cross-contamination (i.e., contaminated raw food spreads pathogens to cooked/heat-processed food via hands of worker, equipment/utensils used for both types of foods, or cleaning cloths/sponges)

* Inadequate cleaning of processing and preparation equipment, particularly equipment used for heat-processed foods

* Ingestion of raw foods of animal origin (e.g., shellfish, milk, ground meats) and of nonanimal origin (berries, melons, salad ingredients) or addition of such raw ingredients to foods that are not subsequently heated


* Insufficient cooking temperatures or time

* Insufficient reheating temperatures or times for foods prepared a day or more ahead of service


* Leaving cooked/heat-processed foods at room or warm outdoor temperatures

* Improper refrigeration (e.g., storing large masses of foods in large containers)

* Preparing foods several hours before serving (e.g., a half-day or a day before)

* Improper hot holding of cooked foods

* These factors should direct attention to operations that ought to be considered as critical control points in HACCP systems and emphasized during inspections.

Corresponding Author: Frank L. Bryan, Food Safety Consultation and Training, 8233 Pleasant Hill Road, Lithonia, GA 30058.

Editor's note: The author gave a version of this paper at the 53rd Annual Educational Meeting of the Florida Environmental Health Association on July 26, 2001.
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Author:Bryan, Frank L.
Publication:Journal of Environmental Health
Article Type:Brief Article
Geographic Code:1USA
Date:Sep 1, 2002
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