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Selection of Foods for Criteria Related to Safety As discussed in Chapter 2, microbiological criteria can serve several purposes. They may give an indication of safety of a product; they may reveal breaches in good manufacturing and handling practices; they may tell something of the keeping quality or shelf-life of a product; and they may reflect suitability for special uses such as canning, infant feeding, or long-term refrigerated storage. Every microbiological criterion specifies some kind of test. A criterion may require the absence of certain pathogenic organisms or their toxins from a specific quantity of the product. Such a criterion is routine for Salmonella spp. in milk chocolate, milk powder, dried eggs, and other ready-to-eat products that have a history of Salmonella contamination. Normally foods are tested for pathogenic or toxigenic microorganisms only if there is reason to believe they may be present. For example, cheese that is suspected in a staphylococcal food poisoning outbreak may be tested directly for enterotoxins. Similarly, a low-acid canned food that is suspected of being underprocessed may be tested for Clostridium botu- linum or its toxin. However, microbiological criteria that are aimed at assuring safety often rely on tests for organisms that indicate a possibility of hazard, not the hazard itself. Coliforms in drinking water, for example, often indicate a failure of the purification process with the possibility that sewage and therefore salmonellae or other intestinal microorganisms might be present. Excessive numbers of fecal coliforms in raw shellfish also may indicate sewage contamination and the presence of pathogens. Large numbers of coagulase-positive staphylococci in cheese, fermented sausage, or frozen 65

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66 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA food suggest that enterotoxin may be present or that mistreatment may lead rapidly to its formation. It should be emphasized that direct tests for pathogenic microorganisms and their toxins, excepting Salmonella spp. and Staphylococcus aureus, are not routinely applied to foods for quality control purposes. Most criteria aimed at assuring safety are based on tests for indicator organisms whose presence suggests the possibility of hazard; the tests do not reveal the hazard itself. It is impractical and unnecessary to develop microbiological criteria for every food. Instead' criteria should be developed only for those foods with potential danger that can be reduced or eliminated by the imposition of microbiological criteria. The following sections describe some of the factors that go into the selection of candidate foods. These factors form the basis of the ICMSF "case plan" (ICMSF, 1985), which reflects varying degrees of health hazard (see Table 6-11. Exactly the same con- siderations go into the Hazard Analysis Critical Control Point system, which is discussed further in Chapters 1 and 10. EPIDEMIOLOGICAL EXPERIENCE Around the turn of the century many countries, including the United States, suffered devastating outbreaks of milkborne disease. Thousands of people contracted typhoid fever, brucellosis, tuberculosis, scarlet fever, diarrhea! disease, and diphtheria from commercial dairy products. Even as late as the mid-1920s, 50 to 60 people died every year in the United States from milkborne disease (Bryan, 1983; Foster, 19731. Public health authorities and the dairy industry then imposed controls on milk produc- tion, developed safe and effective pasteurization procedures, and set sen- sible microbiological limits that ensured a better quality of commercial milk supplies. The net effect of these measures was to change milk from one of the United States' most dangerous foods to one of its safest. How much of this can be attributed to microbiological criteria is not clear, but surely they helped. A similar story can be told for drinking-water. A combination of water purification, waste treatment, and microbiological criteria has led to the production of safe municipal water supplies throughout the nation. Like- wise, the problem of Salmonella in processed egg products, first revealed by epidemiological observations during World War II, has been solved by mandatory pasteurization and the application of microbiological criteria to the finished products. Thus the recognition of foodborne disease out- breaks is an important first step in the consideration of the application of

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SELECTION OF FOODS 67 microbiological criteria aimed at assuring a safe food supply. On the other hand, while raw meat and poultry are notorious as vehicles in foodborne salmonellosis outbreaks, the application of microbiological criteria for these products would be impractical as a control means as they would not lessen the problem (see Chapter 9, parts B and D). OPPORTUNITIES FOR CONTAMINATION Some raw foods are commonly contaminated with potentially dangerous pathogenic and toxigenic microorganisms. Salmonella spp. and Campy- lobacter spp. are frequently found on raw meat and poultry. Recent surveys have shown that 37% of the broiler chickens on the market carried viable salmonellae. The incidence of these organisms in fresh pork is somewhat lower than that in poultry, and in beef it is lower still (Bryan et al., 1979; Tompkin, 19781. Salmonellae cannot be assumed to be absent from any raw animal product and have been ruled by the courts as an inherent defect in red meats and poultry (APHA v. Butz, 19741. Vegetables may carry spores of C. botulinum, Clostridium perfringens, and Bacillus cereus from the soil. Also, up to 50% of food handlers shed staphylococci from their upper respiratory tracts. While small numbers of these organisms can be expected in foods, they present no hazard. Mi- crobiological criteria, therefore, are not indicated unless opportunities for growth occur. Shellfish from polluted waters may be contaminated with various intestinal pathogens, including salmonellae and viruses (e.g., hepatitis A, ECHO, and Norwalk-like agent). Use of microbiological cri- teria as part of the National Shellfish Sanitation Program assists in pro- viding protection from these agents. On the other hand, marine fish and crustaceans, particularly those from warm waters, often carry Vibrio parahaemolyticus. In this instance, mi- crobiological criteria for this bacterium would be unwise (see Chapter 4~. It would be unrealistic to exclude these and similar raw products from the food supply simply because they contain a potentially dangerous micro- organism; they can be rendered safe by appropriate processing and cook- ing. OPPORTUNITIES FOR GROWTH Growth of pathogenic microorganisms in a food increases the likelihood of disease. Multiplication of hazardous microorganisms in a food is de- termined by the usual conditions that affect growth, i.e., available nu- trients, pH, water activity, concentration of inhibitory chemicals (e.g.,

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68 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA sulfur dioxide, nitrite, phosphate, salt, sugar), temperature of storage, gaseous atmosphere within the container, and the presence of competing microorganisms. In fermented foods, for example, harmless and desirable organisms are often added to the raw product as starter cultures, and conditions are provided for their rapid growth and fermentation. The resulting acid or alcohol normally serves as an effective preservative against organisms that can cause disease. Under normal circumstances, one or more of the above conditions is deliberately manipulated to prevent growth of undesirable microbes and thereby effect preservation. Safety exists when the appropriate preservative factors are under control. However, danger can result when events do not follow the expected course. S. aureus may grow during the manufacture of cheese and fermented sausage if the lactic starter culture does not produce acid fast enough. Botulinal toxin has developed in homemade dill pickles that did not contain enough salt. There have been instances of botulism from home-canned tomatoes that had mold growth on the surface apparently the mold metabolized the acid, the pH rose, and conditions became suitable for growth of C. botulinum. New technological procedures and marketing methods may introduce hazards that did not exist before. For example, the application of vacuum packing to Great Lakes smoked fish (see Chapter 1) greatly extended the keeping time, but it also provided time for C. botulinum to grow when the fish was not properly refrigerated. This happened in 1960 and again in 1963 when two outbreaks of Type E botulism led to 19 cases and 7 deaths (CDC, 1979; Osheroff et al., 19641. Canned mushrooms present another example of hazard resulting from technological change. When mushroom canners switched to vibrating fill- ers, they consequently packed more product into each can. This changed the heat penetration characteristics with the result that the heat processes previously used were no longer adequate. Underprocessing resulted and a serious botulism hazard was created. During 1973 five mushroom pro- cessors recalled products because of survival of C. botulinum; no deaths, however, were reported from these products (FDA, 19731. Pressures to reduce the concentration of inhibitory chemicals in foods can be expected to increase the incidence of disease. Some nations severely limit the concentration of sulfur dioxide. The United States has already reduced the amount of nitrite in cured meats, and individuals are being urged to restrict the intake of salt. Phosphate, a rather effective antibot- ulinal agent in cheese spreads, faces mounting opposition to its use at current levels. Foods affected by these actions will have reduced stability and safety and may thereby become candidates for microbiological criteria.

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SELECTION OF FOODS 69 OPPORTUNITIES FOR SURVIVAL As a general rule, foodborne pathogens will survive for long periods in dry or frozen foods. Salmonellae will die off slowly in milk chocolate or dried eggs, but there is never certainty that all are dead. Spores, of course, will survive indefinitely. These facts argue for the usefulness of microbiological criteria in judging the safety of a processed product. Special situations that require careful interpretations do exist. For ex- ample, enterotoxigenic strains of S. aureus sometimes grow in cheese during manufacture. Population levels of one to five million cells per gram of food produce detectable amounts of enterotoxin. During ripening the numbers of staphylococci may decline substantially, but the active enter- otoxin level remains unchanged and the product continues to be hazardous. A viable count of 10,000 S. aureus per gram of aged cheese has been proposed as a suitable basis for suspecting that enterotoxin may be present (NRC, 1975; see also Chapter 4 and Chapter 9, part A). A positive test for thermonuclease (TNase) strengthens this suspicion and justifies testing for enterotoxin itself. On the other hand, commercial mayonnaise provides an extremely hos- tile environment to enteric pathogens. Both salmonellae and staphylococci die within a few days when exposed to the acidity of mayonnaise (Smittle, 1977) and therefore no microbiological criteria for these organisms are needed. However, microbiological criteria to control spoilage organisms are usefully applied during the manufacture of mayonnaise and salad dressing (see Chapter 9, part N). PROCESSING CONDITIONS Many processes include a bactericidal treatment that will eliminate some or all organisms of public health significance. Such treatments range in severity from the pasteurization of eggs, which will eliminate salmonellae, through the pasteurization of milk, which will destroy all nonsporeforming pathogens, to the commercial sterilization of low-acid canned foods, which will inactivate the spores of C. botulinum. Acidification of certain canned foods such as palm hearts and pimientos reduces the heat treatment nec- essary for preservation. Another bactericidal agent of limited use is eth- ylene oxide, which can be applied to spices and a few other items. The effectiveness of all these treatments is known; the need is to ensure that they are carried out properly. Direct measurements are often simpler and more effective for assuring safety than are microbiological criteria. Examples include temperature in

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70 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA processing of pork products to destroy trichinellae, pH in monitoring fermentation in dry and semidry sausages, residual chlorine in cannery cooling water, and phosphatase to detect faulty pasteurization. These mea- surements provide information at the time of processing when it is most needed. While certain processing steps can reduce the incidence of foodborne pathogens in a product, other steps can do the reverse. Staphylococci may be added to crab meat during hand picking. Exposure of cooked food to work surfaces and utensils previously used for raw animal products can result in transfer of salmonellae to the finished food. Even canned foods can become recontaminated from cooling water through minute defects in the containers. SUSCEPTIBILITY OF PROBABLE CONSUMERS Infants, the aged, the malnourished, and the infirm are more susceptible to salmonellae and other infectious agents than are healthy adults. There- fore, foods intended primarily for these susceptible groups are expected to meet more rigid microbiological requirements than are foods for the general population (NRC, 19694. ULTIMATE TREATMENT Although regulatory agencies make no special point of the ultimate treatment before consumption, the fact remains that food to be cooked shortly before eating is less likely to carry viable pathogenic organisms than is food prepared and last handled some time previously. That is to say, a Salmonella organism in a dry turkey soup mix that will be cooked before eating is less hazardous than another Salmonella in a bar of milk chocolate. Thus, microbiological criteria have less importance with food that must be cooked than they have for ready-to-use products. REFERENCES APHA v. Butz 1974 American Public Health Association, et al., Appellants v. Earl Butz, Secretary of Agriculture, et al. D.C. Civil Court. Suit to enjoin Secretary of Agriculture against alleged violations of the Wholesome Meat Act. Pp. 331-338. 511 F. 2d. 331 (D.C. Civ. 1974). Bryan, F. L. 1983 Epidemiology of milk-borne diseases. J. Food Prot. 46:637-649. Bryan, F. L., M. S. Fanelli, and H. Riemann 1979 Salmonella infections. In Food-borne Infections and Intoxications, H. Riemann and F. L. Bryan, eds. New York: Academic Press.

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SELECTION OF FOODS 71 CDC (Center for Disease Control) 1979 Botulism in the United States, 1899- 1977. Handbook for Epidemiologists, Clinicians, and Laboratory Workers. Atlanta: CDC. FDA (Food and Drug Administration) 1973 FDA orders examination of all canned mushrooms. FDA Consumer, October, p. 28. Foster, E. M. 1973 Preservation of foodstuffs and beverages. Pasteur Sesquicentenniel Commemorative Symposium. ASM News 39(1): 32-35. ICMSF (International Commission on Microbiological Specifications for Foods) 1985 Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and specific applications. 2nd Ed. In preparation. NRC (National Research Council) 1969 An Evaluation of the Salmonella Problem. Committee on Salmonella. Washington, D.C.: National Academy of Sciences. 1975 Prevention of Microbial and Parasitic Hazards Associated with Processed Foods. A Guide for the Food Processor. Committee on Food Protection. Washington, D.C.: National Academy of Sciences, pp. 82-83. Osheroff, B. J., G. G. Slocum, and W. M. Decker 1964 Status of botulism in the United States. Pub. Health Reports: 79(10):871. Smittle, R. B. 1977 Microbiology of mayonnaise and salad dressing: A review. J. Food Prot. 40:415- 422. Tompkin, R. B. 1978 The red meat processor's role in salmonellosis prevention. In Proceedings, National Salmonellosis Seminar, W. B. Bixler, ed. Washington, D.C.