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9 Application of Microbiological Criteria to Foods and Food Ingredlients INTRODUCTION In preceding chapters, conditions necessary for establishing meaningful microbiological criteria were presented. In this chapter recommendations are given regarding the need or lack thereof for microbiological criteria for each of 22 food products or groups of products. The subcommittee elected not to give specific recommendations relative to microbiological limits but chose instead to emphasize that any criteria that are developed should be realistic and should be based on relevant background infor- mation. Although the organization of the individual sections of this chapter may vary for each of the foods or groups of foods, the subcommittee has attempted to address the following basic issues in each section: (1) the sensitivity of the food products relative to safety and quality, (2) the needs for a microbiological standards and/or guidelinets), (3) assessment of information necessary for establishment of a criterion if one seems to be indicated, and (4) where the criterion should be applied. The following foods and food groups are included in this chapter in the order in which they are listed below: A. Dairy Products B. Raw Meats C. Processed Meats D. Raw (Eviscerated, Ready To-Cook) Poultry E. Processed Poultry Products 184 F. Eggs and Egg Products G. Fish, Molluscs, and Crustaceans H. Fruits and Vegetables I. Fruit Beverages J. Low-Acid Canned Foods

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APPLICATION TO FOODS AND FOOD INGREDIENTS K. Acid Canned Foods L. Water Activity-Controlled Canned Foods M. Cereals and Cereal Products N. Fats and Oils O. Sugar, Cocoa, Chocolate, and Confectioneries P. Spices A. DAIRY PRODUCTS Introduction 185 Q. Yeasts R. Formulated Foods S. Nuts T. Miscellaneous Additives U. Bottled Water, Processing Water, and Ice V. Pet Foods Microbial growth in the more perishable dairy products, i.e., pasteurized milks, condensed milks, ice cream mixes, creams, cottage cheese, and fermented milks, often results in development of objectionable flavors and textural changes. Even under conditions of good production, pro- cessing, distribution, and storage (including care in the home) such changes are inevitable and may be expected to occur within two to three weeks or less. However, the high acidity of cottage cheese and fermented milks and the high heat treatment given to ultrapasteurized milk permits some- what longer shelf-life. Recognition of the perishability of these products has led to the common practice of "sell by date" labelling as a means of alerting distributors and consumers to the products' limited shelf-life. On the other hand, the relatively stable dairy products, i.e., dried milks, evaporated milk, sterilized milk, ice cream, ripened cheese, butter, and sweetened condensed milk, may remain free of microbiologically induced deterioration for several months or years. In the early part of this century, health of dairy animals and production, processing, and distribution practices were often poor. At that time, un- pasteurized milk was a major vehicle for transmission to humans of dis- eases such as typhoid, diphtheria, septic sore throat, tuberculosis, and brucellosis (Bryan, 19831. Recognition of these problems by government and industry led to a series of recommendations embodied in the Milk Ordinance of 1924 and an interpretion of these recommendations in the Code in 1927. This model milk ordinance, now titled the "Grade A Milk Ordinance" (see below), is an example of the application of the HACCP system to a major food industry. Maintenance of the quality and safety of dairy products, which includes optimum shelf-life, is now a well-accepted industry responsibility and is a necessity for economic survival in this highly competitive industry. Furthermore, it has become traditional for the public to expect, if not

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186 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRlTERlA demand, high-quality products that are safe and esthetically acceptable. Therein lies the basis for current safety and quality assurance programs of regulatory agencies and of industry. As a component of such programs, microbiological criteria play an important role. Sensitivity of Products Relative to Quality Currently, most state and local regulatory agencies utilize almost ex- clusively the Grade A Pasteurized Milk Ordinance (USPHS/FDA, 1978) and USDA Standards for Grades of Dairy Products (USDA, 1975) as the bases for their regulatory programs for dairy products. As an integral part of these two documents, microbiological criteria are specified for most products (see Chapter 8, Table 8-41. Furthermore, the testing of dried milk products for Salmonella is provided for in accordance with a Mem- orandum of Understanding (FDA, 1975) (see Chapter 81. There can be little doubt that application of microbiological criteria has contributed significantly to the provision of high-quality, safe dairy prod- ucts. With the exception noted below and as needs are uncovered by future investigations and research, there appears to be no basis for imposing more severe standards or additional criteria. Industry imposes on itself criteria far more stringent than those that must be met to avoid the like- lihood of noncompliance. This has the salutary effect of providing rea- sonable assurance that products are esthetically acceptable and that aerobic plate count levels are maintained well below those likely to cause dete- riorative changes within a reasonable shelf-life period. One of the exceptions referred to above is the bacterial count limit for Grade 2 raw milk for manufacturing purposes as specified in the USDA "Standards for Grades" (USDA, 19751. Recent research has revealed the potential for heat-resistant enzymes of microbial origin to be involved in the deterioration of processed dairy products held for prolonged storage periods. Furthermore, these enzymes have been implicated in lowered cheese yields. Psychrotrophs are among the principal organisms that pro- duce these enzymes and because of modern milk-handling practices, they can comprise a large proportion of the microflora of raw milk. Thus, bacterial count levels as high as the 3 million per ml permitted in Grade 2 milk would appear to be excessive. Consideration might well be given to modifying this standard. Certainly, lower count levels are easily attained through application of modern milk-handling practices. Sensitivity of Products Relative to Safety Currently the microbiological safety of dairy products can be assured only through application of three preventive measures. These are:

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APPLICATION TO FOODS AND FOOD INGREDIENTS 187 (1) pasteurization or more severe heat treatments; (2) prevention of post- heat treatment contamination; and, (3) for certain products, end-product testing for microorganisms and toxins for certain products. Microbiol- ogical criteria are useful in the application of the preventive measures listed above. Current standards for coliforms as specified in the Grade A Pasteurized Milk Ordinance and the USDA Standards for Grades are useful in detecting post-heat treatment contamination. However, failure to find these organ- isms in finished products or at critical control points does not necessarily indicate the absence of post-heat treatment contaminants. Dried Milk There is ample justification for continued finished-product testing and surveillance of dried milk products for the presence of Salmonella. These products are susceptible to Salmonella contamination and are often used without further heat treatment for fluid consumption as recombined milk or as ingredients in formulated foods. Furthermore, these recombined or formulated products are often consumed by high-risk populations. Monthly reports of the USDA's Salmonella surveillance program (USDA, 1980) administered in accordance with the USDA/FDA Memorandum of Un- derstanding (FDA, 1975) reveal a continuing low level of Salmonella- positive environmental samples and finished products from dried milk plants. Concurrent with the USDA/FDA programs, industry conducts ex- tensive testing. Subsequent routine follow-up procedures undoubtedly have prevented contaminated product from reaching the market. The above-mentioned program as well as FDA surveillance of products offered for import should be continued, strengthened when indicated, and reviewed periodically to ascertain that sampling plans, including methods used, are consistent with the hazards presented and in accord with current developments in methodology and with appropriate statistical concepts. Reference is here made to the USDA document entitled "Salmonella Surveillance Program" (USDA, 19801. This document refers to the Na- tional Academy of Sciences publication An Evaluation of the Salmonella Problem (NRC, 1969) and states that the report classifies dried milk and dried milk product in Food Category II and proposes acceptance of a lot on the basis of all negative results on twenty-nine 25-g samples (n = 291. The USDA document states "Instead of analyzing 25-g samples this In- struction provides a procedure whereby each test shall comprise a com- posite of four 100-g samples." It further states that, "based on low incidence of contamination, this procedure provides comparable sensitivity and permits greater coverage at a reduced cost." In this case n = 16. The sampling plan applies to finished products analyzed quarterly in ac

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188 EVALUATION OF TlIE ROLE OF MICROBIOLOGICAL CRITERIA cordance with the surveillance program. This subcommittee does not agree that a sampling plan of n = 16 provides "comparable sensitivity" to the recommended plan where n = 29, though obviously it must agree that the cost is reduced. In essence the USDA Quarterly Surveillance Program should require the analysis of Weather than 1 composite sample. In this case the sampling plan would be n = 32, which would be only slightly more stringent than the plan recommended by the Salmonella committee. In practice, on a quarterly basis, the USDA collects samples from 3 days' production (preferably consecutive days). Four samples of product from each day are drawn, for a total of 12 samples. The four samples for each day are composited to yield a 400-g analytical unit that is analyzed for Salmonella. Thus, the quarterly finished-product surveillance consists of the analysis of three 400-g samples for a given plant. If the plant produces products other than a nonfat dried milk, i.e., buttermilk and whey, a separate set of 12 samples is taken from the dryerts) that is (are) used for each product. If the plant has several dry-milk dryers, each with its own bagging head, the product from only one dryer is sampled. The "Instruc- tion" directs that alternately a different dryer be sampled on each suc- cessive quarterly survey. This subcommittee believes that samples should be drawn from each dryer since each is an integral unit of production equipment. At the time of the quarterly survey three environmental samples are also collected, these being waste material from the vacuum cleaner, air filters, and tailings. When the surveillance on a plant's production shows a positive test, a letter is sent to the plant manager informing him of the single positive test and the three available options by which the positive product can be handled. These options appear to be adequate to provide reasonable assurance that contaminated product will not reach the market. They provide that the day's production having the positive Sal- monella test shall be either: 1. segregated, reprocessed and the reprocessed product tested for Sal- monella; 2. segregated and disposed of in a manner that poses no health problem to humans or animals, e.g., USDA certification that the product was discarded in a sanitary landfill; or 3. retested (verification test) at the rate of twelve 100-g samples. For test purposes the laboratory will composite 4 samples for a total of 3 tests in = 481. If none of the composites shows a positive test, the results are interpreted as meaning that the incidence of Salmonella is insignificant, and the day's production may be used for human purposes. If one or more of the composites shows a positive test, the day's production represented by the test is then handled as in

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APPLlCATlON TO FOODS ID FOOD INGREDIENTS 189 (1) or (2) above, i.e., segregated, reprocessed, and retested or dis- posed of. In addition, eight 100-g samples are collected from product manufactured on each of two days immediately preceding the day(s) in which the positive product was noted and this rate of sampling and testing is also performed on each day's production made sub- sequent to the day(s) having a positive product test until the plant effects a complete cleanup of its drying facilities. This procedure would represent a sampling plan of n = 32, a plan comparable in stringency to that recommended by the Salmonella committee. If, in connection with a quarterly survey, more than one of the three finished product samples are positive, then verification testing (as outlined above) is not permitted. Positive lots are reconstituted and repasteurized or disposed of in a manner that poses no threat to human or animal health. The plant ~nanager is requested to furnish a list of production back to at least two days prior to the positive lot and up to the time of special cleanup. The list should show the date of manufacture, lot number, number of containers in each lot, and the present location of the product. "Because of possible serious contamination, the product should be recalled from distribution channels and held for sampling and testing for Salmonella." In this connection eight samples are drawn from each day's production held from distribution. If all eight test results on a day's production are negative, that product may be released for use or distribution. If a positive test is obtained on product for any day, all the product for that day shall be disposed of in such a manner so as to pose no health problem to humans or animals. This subcommittee believes that the actions taken subsequent to the detection of positive lots at time of quarterly surveillance sampling are adequate for the purposes intended. The effectiveness of cleanup (required as part of one of the three options indicated above) is determined on the basis of tests made on product manufactured subsequent to cleanup. Sampling involves the collection of eight 100-g samples on each of three production days immediately fol- lowing the cleanup (n = 321. In this instance, if a lot is declared positive, there is no option for verification testing; management must dispose of the product "in such a manner as to pose no health problem to humans or animals" or reprocess the lot and again test it for Salmonella. Fur- thermore, three environmental samples are taken presumably on each post- cleanup production day. The environmental sampling program is an integral part of the USDA Salmonella Surveillance Program. Concomitant collection of environ- mental samples at the time quarterly finished-product samples are taken materially strengthens the program. Experience has taught that if a Sal

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190 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA monella problem exists within a milk-dr~ving plant, one is far more apt to detect this problem through the analysis of environmental samples than through finished product analysis. Thus, given an adequate finished prod- uct sampling plan (n = 29-30) combined with the testing of environmental samples, there is reasonable assurance that if all samples are negative, a serious Salmonella problem did not exist at the time of the quarterly inspection. Furthermore, the sampling programs followed in verification tests have a stringency comparable to that recommended by the Salmonella committee (NRC, 19691. The overall weakness of the program lies in the fact that (1) samples are collected only on a quarterly basis; (2) sampling plans used at time of quarterly sampling are not sufficiently stringent, i.e., consistent with recommendations of the NAS/NRC Salmonella report (NRC, 19691; and (3) in plants having more than one dryer for a given product, the product from only one of the dryers is sampled. Thus, the USDA surveillance program cannot substitute for in-house surveillance by the processor. As with the USDA program on eggs and egg products, the control of the Salmonella hazard in dry milk requires continuous testing of finished product and environmental samples by the processor. The present USDA program is to be commended and should be strengthened as indicated above and continued, with the realization that it is not a substitute for microbiological control by the manufacturer. Accordingly, the dry milk industry should be encouraged to test finished products reg- ularly and in accordance with sampling plans recommended in the NAS/ NRC Salmonella report. Cheese Cheese is the second dairy product for which finished product testing for presence of a pathogen or its toxins may be indicated. The organism of primary concern is Staphylococcus aureus; although pathogenic Esch- erichia cold have caused some concern. Also, the recent series of outbreaks of brucellosis due to unripened raw goat milk queso blanco cheese sold primarily from roadside vendors in the Houston, Texas area has empha- sized the hazard of cheese made from unpasteurized milk (Perkins et al., 19834. As in the case of the hazard of raw milk consumption, pasteurization of milk used in the manufacture of this cheese is the only rational means of control. Routine microbiological testing would not serve as an effective control measure. Certain cheese varieties have served as the vehicle involved in outbreaks of staphylococcal food poisoning. Others, although not involved in out- breaks, have been shown to permit the buildup of potentially hazardous levels of S. aureus under certain conditions of manufacture. Although few

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APPLICATION TO FOODS AND FOOD INGREDIENTS 191 outbreaks have been reported in the United States in recent years, the problem does persist. The nature and control of the problem, including application of microbiological criteria, has been reviewed recently (ICMSF, 1980, 19851. The following is a brief summary of these considerations. The hazard of staphylococcal food poisoning presented by cheese is limited largely to hard varieties, i.e., Cheddar and similar types and Swiss or Emmenthaler. Although S. aureus has been demonstrated to grow in certain other varieties, i.e., Gouda, Brick, Roquefort, Blue, and Moz- zarella, their involvement in outbreaks has been rare or unreported (ICMSF, 19801. At some point during manufacture and subsequent handling, the first group of cheeses undergoes a sufficiently long period at moderate temperatures, which permits growth of lactic starter cultures. Impairment of such growth during these periods permits relatively unrestricted growth of various other organisms that may be present, including S. aureus. If the initial population and period of time of favorable growth conditions are sufficient, the number of S. aureus may reach several million per gram of product, at which point hazardous levels of enterotoxin may be present. Adequate heat treatment of cheese milk, good sanitary practices to avoid post-heat treatment contamination, and unimpaired starter culture activity are essential elements of good manufacturing practices for control of S. aureus in cheese. Appropriate analytical methods are available for the testing of cheese and the monitoring of critical control points in cheese manufacture. Ad- equate and relatively simple methods for detection and enumeration of S. aureus in cheese are available. S. aureus enterotoxins may be detected with specificity, although the procedures are somewhat complicated. Fur- thermore, a rapid test for staphylococcal thermonuclease is sufficiently reliable for determining whether a particular lot of cheese may contain enterotoxin or whether it may be safely released for distribution (see Chapter 15 of ICMSF, 19851. At present the incidence of staphylococcal food poisoning by domest- ically produced cheese does not justify routine testing by regulatory agen- cies. However, industry should be encouraged to (l) routinely monitor critical control points for presence or indication of staphylo.~occal growth and to (2) test all cheese for S. aureus and/or thermonuclease if abnormal lactic culture activity occurred during manufacture or if other conditions that might lead to extensive staphylococcal growth were encountered. FDA should routinely test all susceptible cheese varieties offered for import for presence of thermonuclease. This routine testing is advisable as regulatory agencies generally do not have knowledge of the cheese production con- ditions. Lots positive for thermonuclease should be further tested for presence of enterotoxins.

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192 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA Outbreaks of foodborne illness due to certain pathogenic strains of E. cold in imported Camembert cheese occurred in the United States in 1971. These were the first documented foodborne outbreaks due to E. cold to be reported in the United States. Nevertheless, they caused con- siderable concern about cheese as a vehicle for transmission of pathogenic E. cold to humans. No further outbreaks of cheeseborne illness due to E. cold were reported until 1983. In 1983 several outbreaks occurred again, resulting from consuming imported soft cheese (Brie and Camembert) of French origin. Investigations were not completed at time of this writing, but they seem to indicate that a certain strain of E. cold (027: H20) pro- ducing a heat-stable toxin was the causative organism (Francis and Davis, 19841. . Following the first episode in 1971 certain control measures were in- troduced by the French government and the industry. Apparently these measures were effective in view of the 12-year interval between the two series of outbreaks. However, now it would appear prudent for FDA to initiate appropriate research relative to the E. cold problem in soft cheese as well as the routine testing of soft cheese offered at import, i.e., Ca- membert, Brie, and similar varieties, for the presence and quantitative level of E. colt. Such studies would serve to further delineate the problem and assist in development of an appropriate control program. Fluidt Milk . Milkborne disease outbreaks caused by consuming legally purchased contaminated raw milk as well as raw milk cheese (see preceding dis- cussion of queso blanco cheese) continue with regularity. Even certified raw milk, which is produced under the most exacting sanitary conditions, continues to cause outbreaks (Werner et al., 19841. Recently, Bryan (1983) reviewed the epidemiology of milkborne dis- eases and concluded, as many others have done previously j that pasteur- ization is an essential process in providing milk that is free of disease- producing microorganisms. Application of microbiological criteria, al- though useful, cannot assure that contaminated raw milk will be detected. The problems of preventing the sale and consumption of raw milk have been emphasized in a recent editorial by Chin (1982) (see Appendix F). The sale of raw milk is still legal in some 20 states in spite of the fact that infectious disease professionals consider the scientific case against raw milk to be irrefutable. Nevertheless, the legal aspects involved in preventing the sale of raw milk are complex and provide impediments toward that end. Unfortunately, the small segment of the dairy industry that engages in public sale of raw milk for fluid consumption, deliberately or through ignorance of the consequences, continues to make available to

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APPLICATION TO FOODS AND FOOD INGREDIENTS 193 consumers a product that sometimes is hazardous. The subcommittee agrees with Dr. Chin's conclusion that, "It is the responsibility of all health professionals to see that the public and the policymakers are ade- quately informed about the scientific findings so that public policy on raw milk may be compatible with scientific knowledge and protective of the public's health." References Bryan, F. L. 1983 Epidemiology of milk-borne diseases. J. Food Prot. 46:637-649. Chin, J. 1982 Raw milk: A continuing vehicle for the transmission of infectious disease agents in the United States. J. Infect. Dis. 46: 440-441. FDA (Food and Drug Administration) 1975 Memorandum of Understanding USDA/FDA on Salmonella Inspection of Dry Milk Plants. No. FDA 225-75-4002. Washington, D.C.: U.S. Department of Agriculture. Francis, B. J., and J. P. Davis 1984 Update: gastrointestinal illness associated with imported semi-soft cheese. Morb. Mort. Weekly Rpt. 33: 16, 22. ICMSF (International Commission on Microbiological Specifications for Foods) 1980 Milk and milk products. Pp. 470-520 in Microbial Ecology of Foods. Vol. 2. Food Commodities. New York: Academic Press. 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. Perkins, P., A. Rogers, M. Key, V. Pappas, R. Wende, J. Epstein, M. Thapar, F. Jensen, T. L. Gustafson, and E. Young 1983 Brucellosis Texas. Morb. Mort. Weekly Rpt. 32:548-553. USDA (U.S. Department of Agriculture) 1975 General specifications for approved dairy plants and standards for grades of dairy products. Federal Register 40(198):47910-47940. 1980 Salmonella Surveillance Program. DA Instruction No. 918-72. Washington, D.C.: U.S. Department of Agriculture. USPHS/FDA (U.S. Public Health Service/Food and Drug Administration) 1978 Grade A Pasteurized Milk Ordinance. 1978 Recommendations. PHS/FDA Publ. No. 229. Washington, D.C.: U.S. Government Printing Office. Werner, S. B., F. R. Morrison, G. L. Humphrey, R. A. Murray, and J. Chin 1984 Salmonella dublin and raw milk consumption California. Morb. Mort. Weekly Rpt. 33: 196-198. B. RAW MEATS Sensitivity of Products Relative to Safety and Quality The microbiological condition of retail cuts of red meat (beef, pork, and lamb) is the result of a series of conditions and events including:

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194 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA 1. the health and condition of the live animal; 2. slaughtering-dressing practices; 3. conditions of chilling of the carcass such as rate of cooling, tem- perature, and humidity; 4. sanitary conditions and practices during fabrication of a carcass into primal, subprimal, and retail cuts; 5. packaging conditions such as air versus vacuum-packaging; 6. conditions of distribution and storage (time-temperature profiles); 7. handling of cuts in food service establishments and in the home (proper refrigerated storage, adequate heat treatment, avoiding cross-con- tamination). Following is a brief summary of these conditions and events as they relate to shelf-life and wholesomeness of meat and the potential need for microbiological criteria. For more detailed information, the reader is re- ferred to the following reports (APHA, 1984; Ayres, 1955, 1960; ICMSF, 1980; Ingram and Roberts, 1976; and Roberts, 19741. Conditions prior to slaughter can have an impact on the microbiological condition of meat. Muscle tissue from carcasses of animals that have undergone prolonged muscular activity or long-term stress (lack of feed, temperature changes) before slaughter is often dark, firm, and dry (DFD meat), contains little or no glucose and has a higher pH ~-6.0) than that of unstressed animals (approximately 5.51. Under aerobic storage con- ditions, normal meat spoils when glucose is exhausted and amino acids are attacked. In DFD meat, however, amino acids are attacked without delay. The high pH of vacuum-packaged DFD meat allows the devel- opment of Serratia liquefaciens and Alteromonas putrefaciens, which pro- duce off-odors. For these reasons DFD meat spoils more rapidly than normal meat (Gill and Newton, 19811. Stress also may increase the prev- alence of Salmonella in pigs as they are transported from production units to slaughtering facilities (Ingram, 1972; Williams and Newell, 19701. Microorganisms associated with the live animal are located primarily on the surface of the animal (hide, hair, hooves) and in the gastrointestinal tract. The number of microorganisms in the muscle tissue (intrinsic bac- teria) of healthy animals is small (Gill, 1979~. Carcasses of normal, healthy animals appear to have considerable residual ability to maintain tissue sterility. It is often reported that muscle tissue from stressed animals is more likely to contain "intrinsic" bacteria. It is possible that certain forms of stress depress the immune defense mechanisms and therefore allow the survival of bacteria that otherwise would have been destroyed. Sources of microbial contamination of a carcass include: the anima (surface and gastro-intestinal tract), workers, clothing of workers, utensils

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APPLICATION TO FOODS AND FOOD INGREDIENTS 297 Kokal, D., and D. W. Thorpe 1969 Occurrence of Escherichia cold in almonds of nonpareil variety. Food Technol. 23(2):93- 98. Marth, E. H., and B. G. Calanog 1976 Toxigenic fungi. In Food Microbiology: Public Health and Spoilage Aspects, M. P. DeFigueiredo and D. F. Splittstoesser, eds. Westport, Conn.: AVI Publishing. Meyer, M. T., and R. H. Vaughn 1969 Incidence of Escherichia cold in black walnut meats. Appl. Microbiol. 18:925-931. Schaffner, C. P., K. Mosbach, V. C. Bibit, and C. H. Watson 1967 Coconut and Salmonella infection. Appl. Microbiol. 15:471-475. T. MISCELLANEOUS ADDITIVES A number of food additives used by the food industry are derived from animals, plants, or microorganisms. Three of the larger classes of additives are gums, enzymes, and food colors. Only limited published information is available regarding the microbiology of these substances. Sensitivity of Products Relative to Safety and Quality Gums Gums hydrate in water to form viscous solutions or dispersions and thus exhibit useful suspending, dispersion, and stabilizing properties. They function in foods as emulsifiers, gelling agents, binders, flocculating agents, film farmers, foam stabilizers, release agents, and lubricants. With this range of functional properties, they are widely used in dairy products, sauces, pie fillings, whipped toppings, salad dressings, puddings, and jellies. The sources of these useful polysaccharides are the resinous exudates of trees (acacia, karaya, tragacanth), seeds (locust bean, guar), seaweed (agar, alginates, carrageenan), and microorganisms (xanthan). Starches and pectins from plants and gelatin from animals (Cottrell and Baird, 1980) are also used. Synthetic hydrocolloids include starch derivatives and modified celluloses (Whistler and Zysk, 1978~. The highest microbial populations in the major botanical gums (about 108/g) have been found in raw, unprocessed acacia, carrageenan, and tragacanth (Souw and Rehm, 1975, 19761. Pretreated products such as alginates, carrageenan powder, locust bean gum, and guar flour yielded lower counts. The predominant organisms in the unprocessed gums were the Bacillus species and Streptococcus faecalis; Escherichia coli, how- ever, was not recovered. Coagulase-positive staphylococci with counts of up to 105/g have been found in tragacanth and locust bean; Clostridium

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298 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA perfringens has been recovered from these two gums as well as from acacia. Most gums will support bacterial growth when sufficient moisture is present. Enzymes secreted by Bacillus species can degrade gels and gum solutions reducing viscosity. Gums most susceptible to degradation are tragacanth, acacia, karaya, guar, locust bean, carrageenan, and sodium alginates (Souw and Rehm, 1975, 1976~. Enzymes The enzymes added to foods consist mainly of carbohydrates (amylase, cellulase, invertase, pectinase, etc.) and proteases (e.g., papain and rennet). Plants, animals, and microorganisms are sources of the enzymes. Little is known about the microbiology of enzyme preparations. Animal and microbial rennets, the enzymes whose microbiology has been studied most extensively, may yield high counts but appear to be free of pathogenic bacteria (de Becze, 19701. Never has a health problem been traced to the use of an enzyme per se in food processing (Pariza and Foster, 19831. Colors Natural colors, including annatto, anthocyanins, beet red, carotene, carmine, and saffron, have long been added to foods. Except for carmine, which comes from an insect, these colors are derived from plants. They are extracted into oil or aqueous systems from seeds, skins, or flowers. There are virtually no published data about the microbiological quality of natural food colors. Some anthocyanins have limited antimicrobial activity and thus may restrict growth of certain microorganisms. The one recorded disease outbreak traced to a food color was due to salmonellae in carmine. Salmonella cabana was found to be responsible although additional samples of insects contained Salmonella newport and Salmo- nella enteritidis (Lang et al., 19671. Need for Microbiological Criteria Since many of these additives are raw agricultural products, the usual indices such as APCs usually would be of little value. The type of criteria that might be applied would depend upon end use of the additive. For example, additives to be used in canned foods should not be a significant source of heat-resistant bacterial spores. At present there is little published information to suggest that microbiological criteria would be useful for most gums, enzymes, and colors. This also was the conclusion of a

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APPLICATION TO FOODS AND FOOD INGREDIENTS 299 committee of FAD/WHO who examined the subject a number of years ago (de Becze, 19701. References Cottrell, I. W., and J. K. Baird 1980 Gums. Pp. 45-66 in Vol. 12 of Kirk-Othmer Encyclopedia of Chemical Technology, 3rd Ed. New York: John Wiley and Sons. de Becze, G. I. 1970 Food enzymes. Critical Reviews in Food Technology 1(4): 479-518. Lang, D. J., L. J. Kunz, A. R. Martin, S. A. Schroeder, and L. A. Thomson 1967 Carmine as a source of nosocomial salmonellosis. N. Eng. J. Med. 276:829-832. Pariza, M. W., and E. M. Foster 1983 Determining the safety of enzymes used in food processing. J. Food Prot. 46:453 468. Souw, P., and H. J. Rehm 1975 IV. Microbiological degradation of three plant exudates and two seaweed extracts. Z. Lebensm. Unters.-Forsch. 159(5): 297-304. 1976 V. Degradation of the galactomannans guar gum and locust bean gum by different bacilli. European J. Appl. Microbiol. 2: 47-58. Whistler, R. L., and J. R. Zysk 1978 Carbohydrates. Pp. 535-555 in Vol. 4 of Kirk-Othmer Encyclopedia of Chemical Technology, 3rd Ed. New York: John Wiley and Sons. U. BOTTLED WATER, PROCESSING WATER, AND ICE Sensitivity of Products Relative to Safety and Quality Drinking water has been and still is an important vehicle for transmitting disease-causing agents (bacteria, viruses, parasites, chemicals) to man. From 1977-1981, 189 outbreaks of water-related diseases involving an estimated 49,453 persons occurred in the United States (CDC, 1979, 1980, 1981, 1982 a,b). As for foodborne disease outbreaks, these figures should not be the basis for firm conclusions about the true incidence of waterborne disease outbreaks as it is most likely many times greater than that reported. Of the 189 outbreaks, 100 (53%) were of unknown etiology and were designated "acute gastrointestinal illness" (AGI). The remaining 89 (47%) outbreaks were of a confirmed etiology: Giardia (31), chemical (27), Shigella (9), Norwalk agent (7), Salmonella (5), Campylobacter (3), Parvo- virus-like agent (3), hepatitis A (2), Vibrio cholerae Of (1), and Rotavirus (11. In none of these outbreaks, however, were bottled waters identified as vehicles. Public interest in pure, better-tasting water has created a large demand for bottled drinking water. Bottled water is defined by FDA (1982a) as

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300 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA water that is sealed in bottles or other containers and intended for human consumption. The following types of bottled drinking water are available (APHA, 1984~: Spring or Well Water. This water is taken directly from a spring or well and bottled with minimum treatment. 2. Specially Prepared Drinking Water. This is water in which the mineral content has been adjusted and controlled to improve the taste. The source may be a public water supply or a well. 3. Purified Water. This water conforms to the United States Pharma copeia standard (USP, 1980) for purified water with minerals removed to less than 10 mg/l. Water can be "purified" by distillation, ion-exchange treatment, or reverse osmosis. Method of preparation must be indicated. Only water prepared by distillation can be called "distilled water." 4. Fluoridated Water. Fluoride has been added to drinking water at the optimum concentration as set forth in the FDA Quality Standards (FDA, 1982a). No definition or quality standard for "mineral" water has yet been established in the United States. In view of the potential for water-related illnesses in humans, it is essential that bottled water be from a safe source (spring, artesian well, drilled well, municipal water supply, or other source) and that it be pro- cessed, bottled, held, and transported under sanitary conditions. Water containing small numbers of enteric pathogens can cause disease in humans, whereas the same organisms ingested with food may require larger quantities of bacteria. Small amounts of water taken between meals pass the pyloric area with very little delay. Under such conditions enteric pathogens are hardly exposed to the bactericidal effect of gastric juice and reach the duodenum virtually unchanged (Levine and Nalin, 1976; Mossel and Oei, 19751. When the same bacteria are ingested with solid food, intragastric retention times are considerable. This results in a reduction in viable bacterial cells in individuals with normal gastric secretions. In the United States, few published data are available on the micro- biological condition of bottled drinking water or on the incidence of human disease outbreaks resulting from their use. According to two reports (EPA, 1972; Geldreich et al., 1975), the bacteriological quality of freshly bottled water varied greatly from brand to brand and from sample to sample within brand. Only 10% of samples had an initial APC greater than 500/ml. Coliforms were detected in 6 of 129 samples but only two of these samples exceeded the USPHS Drinking Water Standards. One of these samples also contained fecal coliforms and the other contained Pseudomonas aeru

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APPLICATION TO FOODS AND FOOD INGREDIENTS 301 ginosa. During storage of bottled water pulsating changes in aerobic plate counts frequently occurred. Over 90% of counts of 10,000 bacteriological analyses of bottled water in California in 1977 were less than 100 per ml at time of bottling (Sheneman, 19831. Over 99.8% of these samples were free of coliforms. Although there is no epidemiological evidence that bottled water pro- cessed in the United States has been a public health problem, bottled water has been cited as a cause of human disease in other parts of the world. For example, bottled noncarbonated mineral water was implicated as one of the primary vehicles involved in a cholera epidemic in Portugal in 1974 (Blake et al., 19771. FDA microbiological standards for bottled water (FDA, 1982a) are based on the presence of coliforms. With the multiple tube fermentation method not more than one unit in a sampling of 10 (subsamples) shall have a MPN of 2.2 or more coliforms per 100 ml and no analytical unit shall have a MEN of 9.2 or more coliforms per 100 ml. With the membrane filter method, not more than one of the analytical units in the sample shall have 4.0 or more coliforms per 100 ml and the arithmetic mean of the coliform density of the sample shall not exceed one coliform per 100 ml. The FDA GMPs for bottled water (FDA, 1982b) require coliform anal- ysis at least once a week of a representative sample from a batch or segment of a continuous production run for each type of bottled drinking water produced during a day's production. Additionally, source water obtained from other than public water systems is to be sampled and analyzed for coliforms at least once each week. In addition, at least once each three months, a bacteriological swab and/or rinse count should be made from at least four containers and closures selected just before filling and sealing. No more than one of the four samples may exceed more than one bacterium per ml of capacity or one colony per cm2 of surface area. All samples shall be free of coliforms. In addition to the federal standards, state and local microbiological criteria and good manufacturing practice codes exist to monitor the pro- duction, processing, and distribution of bottled drinking water (Wehr, 19821. To promote high standards of quality in the bottled water industry, the International Bottled Water Association has published a technical man- ual containing a quality control program to assure compliance with FDA standards (IBWA, 19831. The American Sanitation Institute (ASI) inspects all IBWA-member plants for conformance with the regulations. The indigenous microflora of bottled drinking water usually consists of gram-negative bacteria belonging to genera such as Pseudomonas, Cy- tophaga, Flavobacterium, and Alcaligenes. Although no total count is specified, good-quality drinking water at time of bottling usually contains

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302 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA less than 100 bacteria per ml (APHA, 1984~. Higher initial counts represent a lack of good manufacturing practices. The presence of coliform bacteria in bottled water indicates either a lack of good manufacturing practices and/or a potential health problem. Ozone may be applied as a disinfectant just prior to bottling. Some surviving bacteria may multiply in the water after the ozone has dissipated. No one microorganism or group of microorganisms can serve as an ideal indicator of pollution of various types of water. Although many organisms such as Aeromonas, Streptococcus, Escherichia colt, fecal col- iforms, coliforms, sulfite-reducing Clostridium, P. aeruginosa, Vibrio, and E. cold phages have been suggested as potential indicator organisms of drinking water safety, total coliforms appear at the present to be the best indicator organisms (Ptak and Ginsberg, 19771. Processing Water and Ice Water is used extensively in the food-processing industry. It comes in direct contact with major food commodities such as meat, poultry, fish, fruits, vegetables, and cheese curd during washing or chilling operations. In addition, water is used in the cleanup operations of equipment and utensils that come in contact with food. Water also is used as an ingredient in the preparation of foods. Ice is used widely to chill foods such as fish and poultry and is added to some foods as in the preparation of some processed meats. In many food-processing industries, water is chlorinated to control levels of microorganisms, for example in cooling water of canning plants. Chlorination of processing water requires an understanding of needed chlorine concentration, effect of water characteristics such as pH on available chlorine, and proper testing procedures to periodically examine for available chlorine (FPI, 19821. Water used in food production and processing can be a source of spoilage microorganisms and, if obtained from a nonpotable source or subsequently contaminated, it can be a source of pathogens. Several outbreaks of food- borne disease have been associated with or traced to the use of contam- inated water, e.g., salmonellosis from fish (Gangarosa et al., 1968), typhoid fever from canned corned beef (Howie et al., 1968), and yersiniosis from tofu (Nolan et al., 19824. Need for Microbiological Criteria There is no epidemiological evidence to indicate that bottled water as available currently in retail channels offers a significant health hazard to

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APPLICATION TO FOODS AND FOOD INGREDIENTS 303 the American public. Therefore, there appears to be little evidence of need for additional or modifications of criteria currently in FDA regulations. However, the commercial vending of bottled water including import sup- plies and the variety of sources from which water for bottling is obtained has proliferated. These recent increases suggest that a periodic reassess- ment should be made of practices in this industry relative to the micro- biological quality and safety of bottled water offered to the public. Water or ice that comes in contact with or becomes part of a food should be from a potable supply and the microbiological criteria for them should meet the standards set for drinking water (Greenberg et al., 19811. Where Criteria Should Be Applied Microbiological examination of bottled drinking water for compliance with standards or guidelines should be camed out on samples collected at the processing plant. Examination of samples for APC at the retail level has little merit. References APHA (American Public Health Association) 1984 Compendium of Methods for the Microbiological Examination of Foods. 2nd Ed., M. L. Speck, ed. Washington, D.C.: APHA. Blake; P. A., M. L. Rosenberg, J. Florencia, J. B. Costa, L. D. P. Quintino, and E. J. Gangarosa 1977 Cholera in Portugal, 1974. II. Transmission by bottled mineral water. Am. J. Epi- demiol. 105 :344-348. CDC (Centers for Disease Control) 1979 Foodborne and Waterborne Disease Outbreaks. Annual summary 1977. Atlanta: Cen ter for Disease Control. 1980 Water-related Disease Outbreaks. Annual Summary 1978. Atlanta: Centers for Disease Control. 1981 Water-related Disease Outbreaks. Annual Summary 1979. Atlanta: Centers for Disease Control. 1982a Water-related Disease Outbreaks. Annual Summary 1980. Atlanta: Centers for Disease Control. 1982b Water-related Disease Outbreaks. Annual Summary 1981. Atlanta: Centers for Disease Control. EPA (U.S. Environmental Protection Agency) 1972 Bottled water study. A pilot survey of water bottlers and bottled water. Washington, D.C.: Water Supply Division, EPA. FDA (Food and Drug Administration) 1982a Quality standards for foods with no identity standards, bottled water. Code of Federal Regulations 21 CFR 103 (as corrected in Federal Register 47(205):47003-47004.) 1982b Processing and bottling of bottled drinking water. Code of Federal Regulations 21 CFR 129.

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304 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA FPI (The Food Processors Institute) 1982 Canned Foods, Principles of Thermoprocess Control, Acidification and Container Closure Evaluation, 4th Ed. Washington, D.C.: FPI. Gangarosa, E. J., A. L. Bisno, E. R. Eichner, M. D. Treger, M. Goldfield, W. E. DeWitt, T. Fodor, S. M. Fish, W. J. Dougherty, J. B. Murphy, J. Feldman, and H. Vogel 1968 Epidemic of febrile gastroenter~tis due to Salmonella Java traced to smoked whitefish. Am. J. Pub. Health 58:114-121. Geldreich, E. E., H. D. Nash, D. J. Reasoner, and R. H. Taylor 1975 The necessity of controlling bacterial populations in potable waters Bottled water and emergency water supplies. J. Amer. Water Works Assoc. 67:117-124. Greenberg, A. E., J. J. Conners, D. Jenkins, and M. A. H. Franson 1981 Standard Methods for the Examination of Water and Wastewater, 15th Ed. Wash- ington, D.C.: American Public Health Association. Howie, J. W. 1968 Typhoid in Aberdeen, 1964. J. Appl. Bacter~ol. 31:171-178. IBWA (International Bottled Water Association) 1983 International Bottled Water Association Technical Bulletin, Winter. Alexandria, Va. IBWA. Levine, R. J., and D. R. Nalin 1976 Cholera is primarily waterborne in Bangladesh. Lancet 2:1305. Mossel, D. A. A., and H. Y. Oei 1975 Person-to-person transmission of enters bacterial infection. Lancet 1:751. Nolan, C., N. Hands, J. Ballard, J. Allard, and J. Kobayashi 1982 Outbreak of Yersinia enterocolitica Washington State. Morb. Mort. Weekly Rpt. 31 :562-564. Ptak, D. J., and W. Ginsberg 1977 Bacterial indicators of drinking water quality. Pp. 218-221 in Bacterial Indicators/ Health Hazards Associated with Water. Spc. Techn. Publ. 635. Philadelphia: Amer- ican Society for Testing and Materials. Sheneman, J. 1983 Memorandum from the California Food and Drug Section. Water bottling plants bacteriological analysis summary. In International Bottled Water Association, Tech- nical Bulletin, Winter. Alexandria, Va.: IBWA. USP (United States Pharrnacopeia) 1980 Purified water. P. 851 in The United States Pharmacopeia. Rockville, Maryland: U.S. Pharmacopeial Convention. Wehr, H. M. 1982 Attitudes and policies of governmental agencies on microbial criteria for foods an update. Food Technol. 36(9):45-54, 92. V. PET FOODS Companion animals of man have been a source of diseases, including salmonellosis, in humans (Morse and Duncan, 1974, 1975; Morse et al., 1976; Pace et al., 1977) and contaminated pet foods have at times been incriminated as the original cause (Pace et al., 19771. Interest in the microbiology of these foods is influenced by the above and the fact that certain pet foods, mainly canned products, are at times consumed by humans.

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APPLICATION TO FOODS AND FOOD INGREDIENTS Sensitivity of Products Relative to Safety and Quality 305 Although the true incidence of salmonellosis in animals is unknown (NRC, 1969), Salmonella are widely distributed in warm- and cold-blooded species and have been isolated from dogs, cats, horses, caged birds, turtles, frogs, skunks, raccoons, opossums, and others. The role of pets in the distribution of Salmonella has been recognized in a report by the Com- mittee on Salmonella (NRC, 19691: Of the many routes by which man can acquire salmonellosis, special mention should be made of household pets, including dogs, cats, turtles, chicks and ducklings. . Pet animals can become infected with Salmonella by a wide variety of routes, e.g., through coprophagy, by direct contact with infected animals, through eating diseased carrion and wildlife, and by the consumption of contaminated pet food. The latter is probably the least important source since the present day incidence of Salmonella in commercial pet food is very low (Pace et al., 1977~. Pet foods, which are sold predominantly for dogs and cats, may be marketed as canned, intermediate moisture (aw 0.80-0.90), or dried prod- ucts. Canned pet foods are terminally heat processed in hermetically sealed containers and are commercially sterile. They are subject to the regulations for low-acid canned foods and when in compliance are not of public health concern. Intermediate moisture pet foods and the dry products are given a heat process, generally during extrusion and pelleting, that will destroy the vegetative cells of pathogenic bacteria. The prevention of recontam- ination following heating, then, is the critical control step in their pro- cessing. Monitoring of environmental samples as well as finished product for Salmonella is thus important. Recontamination of dry pet food with Salmonella is of special concern because water is often added to the food prior to feeding. Significant growth of the pathogen can occur if the food is held at ambient temperature for an extended time period following rehydration. A potential would then exist not only for infection of the pet but for cross-contamination of household items such as equipment, utensils, and human foods. Need for Microbiological Criteria Canned pet foods are subject to the regulations for low-acid foods and thus the main applications of criteria are to assure that ingredients are free of bacterial spores that might survive the thermal process. Dry and intermediate moisture pet foods should be free of Salmonella, and a standard exists for this pathogen (U.S. Congress, 19801. Specifi- cations and guidelines for these products are especially useful if applied

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306 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA at critical control points identified within a HACCP system. Guidelines and specifications serve to: 1. assess suitability, including safety, of incoming ingredients (The elimination of salmonellae from feed ingredients, particularly those of animal origin, would greatly reduce the occurrence of these organisms in finished pet foods, but this goal does not appear to be readily attainable at this time [USDA, 1978] . ); 2. identify acceptable ingredient suppliers; 3. assess control effectiveness at critical control points in manufactur- ~ng; 4. determine the acceptability of a finished product. Information Necessary for Establishment of a Criterion if One Seems To Be Indicated Extensive information is available regarding those feed ingredients that may be contaminated with Salmonella (ICMSF, 1980) and therefore may require specifications that limit this pathogen. Information is also available on the occurrence of Salmonella in pets (Morse, 1978), and in pet foods (D'Aoust, 1978; ICMSF, 1980; Pace et al., 19771. It is advisable for pet food manufacturers to conduct appropriate microbiological surveillance studies that will generate the information required for the development of guidelines. Where Criteria Should Be Applied Analyses for salmonellae might be conducted on the packaged product. Guidelines and specifications would best be applied at the plant processing level as components of an ongoing HACCP program. Their application at critical control points and on the finished product should assist in minimizing the contamination of pet foods with undesirable microorgan- isms. References D'Aoust, J. Y. 1978 Salmonella in commercial pet foods. Can. Vet. J. 19:99-100. ICMSF (International Commission on Microbiological Specifications for Foods) 1980 Microbial Ecology of Foods. Vol 2. Food Commodities. New York: Academic Press. Morse, E. V. 1978 Salmonellosis and pet animals. In Proceedings of the Salmonellosis Seminar. Wash- ington, D.C.: U.S. Department of Agriculture.

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APPLICATION TO FOODS AND FOOD INGREDIENTS 307 Morse, E. V., and M. A. Duncan 1974 Salmonellosis An environmental health problem. J. Am. Vet. Med. Assoc. 165: 1015- 1019. 1975 Canine salmonellosis: Prevalence, epizootiology, signs, and public health signifi- cance. J. Am. Vet. Med. Assoc. 167:817-820. Morse, E. V., M. A. Duncan, D. A. Estep, W. A. Riggs, and B. O. Blackburn 1976 Canine salmonellosis: A review and report of dog to child transmission of Salmonella enteritidis. Am. J. Publ. Health 66:82-84. NRC (National Research Council) 1969 An Evaluation of the Salmonella Problem. Committee on Salmonella. Washington, D.C.: National Academy of Sciences. Pace, P. J., K. J. Silver, and H. J. Wisniewski 1977 Salmonella in commercially produced dried dog food: Possible relationship to a human infection caused by Salmonella enteritidis serotype Havana. J. Food Prot. 40(5):317- 321. U.S. Congress 1980 Federal Food, Drug and Cosmetic Act, as amended. Washington, D.C.: U.S. Govt. Printing Office. USDA (U.S. Department of Agriculture) 1978 Recommendations for Reduction and Control of Salmonellosis. A Report of the U.S. Advisory Committee on Salmonella. Washington, D.C.: USDA.