Introduction

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, processing, 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 somewhat longer shelf-life. Recognition of the perishability of these products has led to the common practice of "sell by date" labeling 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, unpasteurized milk was a major vehicle for transmission to humans of diseases such as typhoid, diphtheria, septic sore throat, tuberculosis, and brucellosis (Bryan, 1983). Recognition of these problems by government and industry led to a series of recommendations embodied in the Milk Ordinance of 1924 and an interpretation 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 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 exclusively 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 8-4). Furthermore, the testing of dried milk products for Salmonella is provided for in accordance with a Memorandum of Understanding (FDA, 1975) (see Chapter 8).

There can be little doubt that application of microbiological criteria has contributed significantly to the provision of high-quality, safe dairy products. 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 likelihood of noncompliance. This has the salutary effect of providing reasonable assurance that products are esthetically acceptable and that aerobic plate count levels are maintained well below those likely to cause deteriorative 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, 1975). 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 produce 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: (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. Microbiological 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 organisms in finished products or at critical control points does not necessarily indicate the absence of post-heat treatment contaminants.

References

• Bryan, F. L. 1983. Epidemiology of milkborne diseases. J. Food Prot. 46:637–649. [PubMed: 30921943]
• 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. [PubMed: 6896719]
• 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. [PubMed: 6420659]
• 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. 2^nd 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.

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:

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, temperature, 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-contamination).

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 referred to the following reports (APHA, 1984; Ayres, 1955, 1960; ICMSF, 1980; Ingram and Roberts, 1976; and Roberts, 1974).

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 5.5). Under aerobic storage conditions, 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 development of Serratia liquefaciens and Alteromonas putrefaciens, which produce off-odors. For these reasons DFD meat spoils more rapidly than normal meat (Gill and Newton, 1981). Stress also may increase the prevalence of Salmonella in pigs as they are transported from production units to slaughtering facilities (Ingram, 1972; Williams and Newell, 1970).

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 bacteria) 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 animal (surface and gastro-intestinal tract), workers, clothing of workers, utensils, equipment, air, and water. Hence, the level of microbial contamination of a carcass at this stage depends upon the degree of sanitation practiced during the slaughter-dressing procedures. Aerobic plate counts (APCs) of freshly dressed beef, pork, and lamb carcasses in the United States usually range from 10²–10⁴ per cm², most of which are not psychrotrophic. Microbial types reflect the various sources of contamination and include Micrococcus, Staphylococcus, Bacillus, Enterobacteriaceae, Pseudomonas, yeasts and molds, and others. Because of location and handling practices certain areas of a carcass are more likely to be contaminated or to remain contaminated than are others. For these reasons, microorganisms are not uniformly distributed over the surface.

Under conditions of rapid chilling, low storage temperature (-1 to + 1°C/30.2 to 33.8°F), proper air movement, and relative low humidity, the number of microorganisms on a carcass may increase little or in some cases actually decrease during the first 24 to 48 hours. During further refrigerated storage, psychrotrophic bacteria will become a more prominent part of the microbial flora.

Fabrication of carcasses into primal, subprimal, and retail cuts involves extensive handling of the meat, markedly increases the surface area, and increases the a_w as newly cut surfaces are made. Because these operations are carried out at refrigeration temperature, contamination at this stage is likely to include a high proportion of psychrotrophic bacteria.

In recent years, approximately 60–70% of the beef leaving meat-packing plants in the United States is vacuum-packaged. Storage of cuts in vacuum packages results in a predominance of lactic acid bacteria, whereas gram-negative, aerobic, psychrotrophic rods such as Pseudomonas spp. predominate on aerobically stored cuts. The latter are more active spoilage producers than the lactic acid bacteria. Thus, vacuum-packaged cuts with 10⁶–10⁷ bacteria per cm² may be organoleptically acceptable whereas comparable cuts stored in air-permeable films with similar numbers of gram-negative, aerobic psychrotrophic rods may exhibit off-odors. In vacuum-packaged red meat, high levels of lactic acid bacteria (10⁷–10⁸ per cm²) frequently contribute to odors characterized as sour, acid, buttermilk-like, cheesy and less frequently "sulphur-like" or "H₂S-like" (Hanna et al., 1983). When vacuum-packaged cuts are fabricated into steaks or chops and then repackaged in oxygen-permeable films, gram-negative aerobic rods will soon become predominant on the cuts in the display cases.

Conditions of refrigerated storage in the distribution chain (plant, wholesale, retail, food service establishment, home) can have a profound effect on the microbial condition and therefore shelf-life of the product. Cuts with initial low numbers of psychrotrophic bacteria held at proper refrigeration temperature (-1 to + 1°C/30.2 to 33.8°F) will have a greater shelf-life than will meats produced under less sanitary conditions. Even meats produced under good sanitary conditions will have reduced shelf-life when stored at marginal refrigeration temperatures.

Improper cooking and handling of raw meats in homes and food service establishments is one of the main reasons for foodborne illness caused by consumption of "cooked" meats. It is not yet commercially feasible to produce red meat free from pathogenic bacteria. Small numbers of a variety of pathogenic organisms such as Salmonella, Clostridium perfringens, Yersinia enterocolitica, Campylobacter jejuni, and Staphylococcus aureus can be present on raw red meats. (See Chapter 4 for more detailed information on these bacteria.) In pork Trichinella spiralis can be present. Adequate heat treatment of the meat will destroy most of these pathogens. Spores of C. perfringens, however, may survive in cooked meats. If such meats are held at temperatures between 20 to 50°C/68 to 122°F, growth of C. perfringens may occur, during either serving operations or subsequent storage, thus creating a health hazard.

To produce red meats with optimum shelf-life and safety requires the monitoring of a series of critical control points pertinent to each of the conditions or events listed above. Most of these critical control points can be monitored by careful inspection of the animals, evaluating the procedures and practices used, and by checking temperatures during chilling operations.

Microbiological guidelines can be applied to monitor some of the critical control points. For example, several relatively simple procedures (APHA, 1984) are available to check the sanitary condition of equipment and utensils. They are useful to evaluate the effectiveness of cleaning and sanitizing procedures. Microbiological count data on freshly dressed carcasses need to be interpreted cautiously (Ingram and Roberts, 1976) because (1) microorganisms are not distributed evenly over the carcass, (2) there is considerable variation in contamination between carcasses, (3) there are differences in contamination due to processing on different days in the same plant and (4) there are differences between plants. In addition, the tests that can be applied to examine carcasses under commercial conditions recover only a fraction (often a variable fraction) of the organisms present, usually from a rather small surface area of the total carcass. Nevertheless, APCs on freshly dressed carcasses may provide data that indicate a trend in the handling of animals during the slaughter-dressing operations.

Several other methods have been tried to monitor microbial activity in red meats such as pH, dye reduction, titratable acidity, volatile nitrogen compounds, volatile acids, extract-release-volume, and others (see Chapter 5). None of these has proved to be a sensitive and reproducible indicator of incipient spoilage applicable to various raw meats. Critical control points associated with handling in retail outlets, food service establishments, and in the home are beyond the control of the meat processor. To obtain optimum shelf-life and wholesomeness, the HACCP concept has to be applied along the entire production, processing, distribution, and food preparation chain.

Need for Microbiological Criteria

Microorganisms of public health significance such as Salmonella, C. perfringens, S. aureus, Y. enterocolitica, and C. jejuni often are present in small numbers as part of the natural microbial flora of live animals. Even the best production and processing practices do not eliminate these organisms from raw meats. Therefore, limits for pathogenic microorganisms in microbiological criteria for raw meats are impractical. The same is true for indicator organisms such as the coliform group (coliforms, fecal coliforms, and Escherichia coli) because there is no direct relationship between the presence of these types and the presence or absence of pathogens. The courts have held that Salmonella is an inherent defect in raw meats (APHA v. Butz, 1974). This decision was based upon the fact that even with the use of the best manufacturing practices consistent with present technology, Salmonella cannot be eliminated from raw meat.

The APC of refrigerated red meats in distribution channels reflects microorganisms acquired from a series of events: slaughter-dressing procedures, chilling, fabrication into primals, subprimals, and retail samples, and growth during refrigerated storage. At points remote from the processing line the APC does not distinguish between microorganisms from the carcass, those acquired during processing, and those resulting from growth during normal refrigerated storage. Although the APCs may be similar, vacuum-packaged cuts on which lactic acid bacteria frequently predominate can be organoleptically acceptable, whereas comparable cuts under aerobic storage, with gram-negative aerobic rods predominating, may be unacceptable. The APC may be of some value to a meat processor to evaluate processing conditions and perhaps shelf-life of a product under well-defined conditions of refrigerated storage. However, the APC of perishable red meats in distribution channels is of little value in the evaluation of the microbial quality of the carcass and processing practices and has no relevance to health.

The history of the Oregon Meat Standard is directly related to the above discussion. In 1973, the state of Oregon adopted a microbiological standard for fresh or frozen red meat at the retail level with limits of APC 5x10⁶ and 50 E. coli per gram. The standard was revoked in 1977 (State of Oregon, 1977) for the following reasons:

1.

There was no evidence that application of the standard improved sanitary conditions in the retail market.

2.

There was no evidence of a significant change in the numbers of microorganisms in ground meat and probably no change in quality characteristics of the meat.

3.

There was no evidence of a reduction of foodborne illness.

4.

The promulgation of the standard may have created the impression on the part of the public that ground meat produced under the standard would have lower microbial counts, improved quality, and fewer health hazards. There was no clear evidence that the expectations were materialized.

5.

The additional costs of the program were not justified because the expected benefits, namely lower microbial counts, improved organoleptic quality, and reduced risk to public health, were not clearly demonstrated.

The working group of the Codex Committee on Food Hygiene (FAO/WHO, 1979) also concluded that no benefits would result for either public health or quality through the application of microbiological criteria for raw meats.

In summary:

1.

Carcasses, primal, subprimal, and retail cuts of meat from normal, healthy animals contain a variety of microorganisms including low levels of some pathogens.

2.

Refrigerated raw meats will spoil eventually even if they are produced from the carcasses of normal, healthy animals, fabricated under good manufacturing conditions, and properly refrigerated.

3.

If red meats are not properly cooked, held, cooled, and stored, they can cause foodborne illness.

4.

Microbiological standards for raw meats will prevent neither spoilage nor foodborne illness and thus do not appear warranted. Instead, application of the HACCP system to the entire processing and distribution chain including the meat-packing plant, retail units, food service establishment, and home should be used to produce a product with satisfactory shelf-life and public health safety.

5.

Microbiological guidelines are applicable to monitor certain critical control points in the processing of raw meats such as the sanitary condition of equipment and utensils and the condition of freshly dressed carcasses.

References

• APHA v. Butz 1974. American Public Health Association et al., Appellants vs. Earl Butz, Secretary of Agriculture et al. D.C. Civil Court. Suit to enjoin the Secretary of Agriculture against alleged violations of the Wholesome Meat Act. Pp.331–338. 511 F. 2d 331 (D.C. Civ. 1974).
• APHA (American Public Health Association) 1984. Compendium of Methods for the Microbiological Examination of Foods. 2^nd Ed., M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• Ayres, J. C. 1955. Microbiological implications in handling, slaughtering, and dressing meat animals. Adv. Food Res. 6:109–161.
• 1960. Temperature relationships and some other characteristics of the microbial flora developing on refrigerated beef. Food Res. 25:1–18.
• FAO/WHO (Food and Agriculture Organization/ World Health Organization) 1979. Report of a FAO/WHO working group on microbiological criteria for foods. Geneva: FAO/WHO.
• Gill, C. O. 1979. A review. Intrinsic bacteria in meat. J. Appl. Bacteriol. 47:367–378. [PubMed: 396298]
• Gill, C. O., and K. G. Newton 1981. Microbiology of DFD beef. Pp. 305–327 in The Problem of Dark-cutting in Beef, D. E. Hood, editor; and P. V. Tarrant, editor. , eds. The Hague: Martines Nijhoff.
• Hanna, M. O., J. W. Savell, G. C. Smith, D. E. Purser, F. A. Gardner, and C. Vanderzant 1983. Effect of growth of individual meat bacteria on pH, color and odor of aseptically prepared vacuum-packaged round steaks. J. Food Prot. 46:216–221, 225. [PubMed: 30913665]
• ICMSF (International Commission on Microbiological Specifications for Foods) 1980. Microbial Ecology of Foods. 2. Food Commodities. New York: Academic Press.
• Ingram, M. 1972. Meat processing past, present and future. R. Soc. Health J. 92:121–131. [PubMed: 5074060]
• Ingram, M., and T. A. Roberts 1976. The microbiology of the red meat carcass and the slaughterhouse. R. Soc. Health J. 96:270–276. [PubMed: 1035427]
• Roberts, T. A. 1974. Hygiene in the production of meat. Meat Research Institute Memoir No. 696. Langford, Bristol.
• State of Oregon 1977. Report of the meat bacterial standards review committee. Salem, Oregon: Department of Agriculture.
• Williams, L. P., and K. W. Newell 1970. Salmonella excretion in joy-riding pigs. Am. J. Publ. Health 60:926–929. [PMC free article: PMC1348911] [PubMed: 5462567]

Introduction

After the animal carcass is chilled, it is generally broken down into primal, subprimal, and ultimately retail cuts. Unlike poultry, where the various separated parts of the carcass are classified as ''processed," the various cuts derived from carcass meat are still classified as "red meat," i.e., unprocessed.

Sensitivity of Products Relative to Safety and Quality

Need for Microbiological Criteria

Assessment of Information Necessary for Establishment of a Criterion if One Seems to be Indicated

These considerations have been largely addressed in sections above. With respect to criteria utilized to assess the microbiological status of various raw materials, e.g., meat trimmings or the adequacy of equipment cleanup, baseline information must be established by the processor. Only on the basis of such information can useful limits be established.

Where Criteria Should Be Applied

See sections on sensitivity of products relative to safety and quality and on need for microbiological criteria.

References

• AMI (American Meat Institute) 1982. Good Manufacturing Practices. I. Voluntary Guidelines for the Production of Dry Fermented Sausage; II. Voluntary Guidelines for the Production of Semi-dry Fermented Sausage. Washington, D.C.: American Meat Institute.
• Bailey, J. W. 1974. Encyclopedia of labeling meat and poultry products. St. Louis: Meat Plant Magazine.
• Barber, J. E., and R. H. Deibel 1972. Effect of pH and oxygen tension on staphylococcal growth and enterotoxin formation in fermented sausage. Appl. Microbiol. 24:891–898. [PMC free article: PMC380692] [PubMed: 4631103]
• Bryan, F. L. 1980. Foodborne diseases in the United States associated with meat and poultry. J. Food Prot. 43:140–150. [PubMed: 30822910]
• CDC (Centers for Disease Control) 1960. Botulism. Morb. Mort. Weekly Rpt. 9:2.
• 1976. a. Salmonella Saint-Paul in precooked roasts of beef—New Jersey. Morb. Mort. Weekly Rpt. 25(5):34, 39.
• 1976. b. Salmonella bovis-morbificans in precooked roasts of beef. Morb. Mort. Weekly Rpt. 25(42):333–334.
• 1977. a. Multistate outbreak of Salmonella newport transmitted by precooked roasts of beef. Morb. Mort. Weekly Rpt. 26(34)277–278.
• 1977. b. Follow-up on Salmonella organisms in precooked roast beef. Morb. Mort. Weekly Rpt. 26(38):310.
• 1978. Salmonellae in precooked roasts of beef—New York. Morb. Mort. Weekly Rpt. 27(24):315.
• 1981. a. Multistate outbreak of salmonellosis caused by precooked roast beef. Morb. Mort. Weekly Rpt. 30:391–392. [PubMed: 6790931]
• 1981. b. Multiple outbreaks of salmonellosis associated with precooked roast beef—Pennsylvania, New York, Vermont. Morb. Mort. Weekly Rpt. 30:569–570. [PubMed: 6795438]
• 1982. Isolation of E. coli 0157:H7 from sporadic cases of hemorrhagic colitis—United States. Morb. Mort. Weekly Rpt. 31:580, 585. [PubMed: 6817062]
• 1983. Botulism and commercial pot pie—California. Morb. Mort. Weekly Rpt. 32:39–40, 45. [PubMed: 6405175]
• Fontaine, R. E., S. Arnon, W. T. Martin, T. M. Vernon, E. J. Gangarosa, J. J. Farmer, A. B. Moran, J. H. Silliker, and D. L. Decker .
• 1978. Raw hamburger: An interstate common source of human salmonellosis. Am. J. Epidemiol. 107:36–45. [PubMed: 623088]
• Gardner, G. A. 1981. Brochothrix thermosphacta (Microbacterium thermosphactum) in the spoilage of meats. A review. Pp. 139–173 in Psychrotrophic Microorganisms in Spoilage and Pathogenicity, T. A. Roberts, editor; , G. Hobbs, editor; , J.H.B. Christian, editor; , and N. Skovgaard, editor. , eds. New York: Academic Press.
• Goodfellow, S. J., and W. L. Brown 1978. Fate of Salmonella inoculated into beef for cooking. J. Food Prot. 41:598–605. [PubMed: 30795117]
• Greenberg, R. A., and J. H. Silliker 1961. Evidence for thermal injury in enterococci. J. Food Sci. 26:622–625.
• ICMSF (International Commission on Microbiological Specifications for Foods) 1974. Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and specific applications. Toronto: University of Toronto Press. Pp.143–146.
• 1980. Microbial Ecology of Foods. Volume 2. Food Commodities. New York: Academic Press. Pp.378–383.
• Johnston, R. W., and R. B. Tompkin 1984. Meat and meat products. In Compendium of Methods for the Microbiological Examination of Foods. 2^nd Ed. M. L. Speck, editor. , ed. Washington, D.C.: American Public Health Association.
• Mundt, J. O., and H. M. Kitchen 1951. Taint in southern country-style hams. Food Res. 16:233–238. [PubMed: 14840516]
• Niven, C. F. 1956. Vinegar pickled meats. A discussion of bacterial and curing problems encountered in processing. Bulleting No. 27. Chicago: American Meat Institute Foundation.
• Niven, C. F., L. G. Bultner, and J. B. Evans 1954. Thermal tolerance studies on the heterofermentative lactobacilli that cause greening of cured meat products. Appl. Microbiol. 2:26. [PMC free article: PMC1056948] [PubMed: 13125340]
• NRC (National Research Council) 1964. An Evaluation of Public Health Hazards from Microbiological Contamination of Foods. Publication No. 1195. Washington, D.C.: National Academy of Sciences.
• State of California (Department of Health Services) 1975. Botulism—home canned figs and chicken pot pie. Calif. Morbidity No. 46.
• 1976. Type A botulism associated with commercial pot pie. Calif. Morbidity No. 51.
• USDA (U.S. Department of Agriculture) 1983. Production requirements for cooked beef, roast beef and cooked corned beef. Federal Register 48 (106):24314–24318.

Sensitivity of Products Relative to Safety and Quality

The poultry industry is one of the most integrated food industries in the United States. A single organization may control an entire operation including breeder farm, hatchery, grow-out farm, processing, and retail operations. Fertile eggs from breeder farms are delivered to hatcheries where the eggs are incubated and then placed in hatchers. After hatching, chicks or poults are delivered to grow-out farms, reared until ready for slaughter, and then transported to processing plants.

The microbiological condition of eviscerated, ready-to-cook poultry (chickens, turkeys, ducks, and quail) is the result of a series of conditions and events (ICMSF, 1980) including:

1.

conditions at the breeding farm and hatchery

2.

health of the live animal

3.

feed supply

4.

environmental conditions under which the flock was raised (cross-contamination by man, rodents, wild birds, litter, drinking water)

5.

transportation

6.

scalding

7.

picking (defeathering)

8.

washing

9.

evisceration (opening of body cavity, viscera pull, inspection, viscera removal)

10.

chilling

11.

packaging

12.

sanitary practices and conditions in the processing plant (involving workers, equipment, utensils)

13.

storage (time-temperature profile)

14.

thawing, storage, and handling practices in retail stores and kitchens

Microbial contamination of the egg can occur in the ovaries during the development of the egg or later as a result of penetration of the egg shell. Fumigation at the breeder farm is generally practiced to control microbial penetration of eggs. Breeding flocks are tested for the presence of Salmonella by blood agglutination tests and subsequent culturing of internal organs. The National Poultry Improvement Plan (USDA, 1982) is the most recognized plan charged with the elimination of Salmonella pullorum and Salmonella gallinarum from breeder flocks. Chicks or poults on hatching contain an extensive microbial flora.

Microorganisms associated with live poultry are located primarily on the surface of the bird (skin, feet, feathers) and in the gastro-intestinal tract. The numbers and types depend largely on the environmental conditions under which the flock was raised. This population nearly always includes a large variety of microbial types such as Pseudomonas, Moraxella, Acinetobacter, Micrococcus, Enterobacteriaceae, Staphylococcus, Bacillus, Clostridium, Flavobacterium, molds, and yeasts. Soil, litter, feed, and drinking water are primary sources of these microbes. Other reservoirs include insects, rodents, wild birds, and farm workers. These sources contribute not only saprophytic species but may infect or contaminate birds with pathogens such as Salmonella, Yersinia, and Campylobacter. During transportation to processing plants, the incidence of contamination increases because of further distribution of microorganisms from bird to bird primarily through contact with fecal material.

During the overall processing operation in modern broiler or turkey processing plants a significant reduction (90–95%) in total bacterial numbers can be achieved by the scalding, washing, and chilling operations (Gardner and Golan, 1976). In the first, microbial destruction is effected by heat; in the latter two operations, reduction is achieved by the rinsing effect (mechanical removal) of the spray or wash. Bacterial numbers on the carcass may increase during evisceration because of extensive manual handling. This is particularly so for turkey carcasses because of handling associated with carcass trussing, draining, and packaging. Post-chill operations in broiler processing, however, are largely automated.

Microbial contamination of carcasses during processing should be kept to a minimum by employing sanitary handling procedures, proper cleaning and sanitation of equipment and utensils that come in contact with carcasses, and use of adequate quantities of rinse and chill waters.

Microorganisms on freshly processed carcasses are located primarily on the surface, normally at a level of 10³ to 10⁴ per cm². They constitute a variety of species including psychrotrophic bacteria and originate from various sources such as the incoming bird (feet, feathers, intestinal tract), water, ice, and air, and are spread from carcass to carcass by processing equipment, utensils, and line workers.

The shelf-life of freshly processed carcasses depends on the number and types of microorganisms present, the time and temperature of storage, and the method of packaging. Shelf-life will be short when initial numbers of psychrotrophic spoilage bacteria are high, particularly when the carcasses are stored at marginal (above 1.7°C/35°F) refrigeration temperatures. When counts of psychrotrophic gram-negative bacteria such as Pseudomonas, Moraxella-Acinetobacter, and Flavobacterium on chilled poultry reach 10⁷-10⁸ per cm², off-odors often followed by slime formation occur. When carcasses are stored refrigerated in vacuum-packages or in modified gaseous atmospheres containing CO₂, lactic acid bacteria usually become predominant. Both of these packaging procedures significantly increase the shelf-life of raw poultry compared to that observed when oxygen-permeable films are used. In vacuum packages and in modified atmospheres containing elevated levels of CO₂, gram-negative aerobic psychrotrophic bacteria are inhibited. Although large numbers of psychrotrophic lactic acid bacteria develop during refrigerated storage, sensory degradation of the product is not as rapid as is observed when gram-negative aerobic psychrotrophic bacteria predominate.

Subsequent handling of carcasses in food service establishments or in homes can spread microorganisms, including pathogens, that may be associated with the carcass to the cooked product or to other foods through contact with knives, tables, cutting boards, and cleaning cloths. Thawing frozen turkeys and then leaving them under conditions that allow microbial growth may lead to increases in bacterial count on the carcass. Proper thawing should be done under refrigeration or in cold running water.

Eviscerated, ready-to-cook poultry carcasses often contain small numbers of pathogens such as Salmonella, Staphylococcus aureus, Clostridium perfringens, Campylobacter fetus subsp. jejuni, and Yersinia enterocolitica . These organisms enter processing plants with live birds and are spread to carcass surfaces during processing. At the present time there are no commercially applicable methods employed in the United States to eliminate pathogens from carcasses, although ionizing radiation could accomplish this. Good sanitary processing practices, however, can reduce the prevalence and extent of spread of pathogens in a processing plant. The presence of pathogens on ready-to-cook carcasses can lead to health hazards if the product is mishandled in a plant, food service establishment, or in the home (Bryan, 1980; Bryan and McKinley, 1974). These faulty practices include:

1.

inadequate cooking of poultry resulting in survival of pathogens such as Salmonella, C. fetus subsp. jejuni, Y. enterocolitica, and S. aureus (spores of C. perfringens may survive adequate cooking);

2.

transfer of pathogens from the raw carcass via hands, cleaning cloths, equipment, and utensils to cooked poultry or to foods that will not receive further heat treatment;

3.

temperature abuse of adequately cooked poultry containing surviving spores of C. perfringens or of inadequately cooked poultry containing Salmonella or other pathogens (this could involve improper cooling, hot-holding, and reheating);

4.

time-temperature abuse of cooked poultry subsequently sliced or chopped and recontaminated with S. aureus or of salads in which this recontaminated poultry is used as an ingredient.

Poultry products so abused have been identified as vehicles in outbreaks of foodborne disease. From 1968–1977, poultry was responsible for 14% of foodborne disease outbreaks in which a vehicle was ascertained (Bryan, 1980). Salmonellosis accounted for 19% of these outbreaks, staphylococcal intoxication for 16%, C. perfringens enteritis for 10%, other foodborne diseases of known etiology for 2%, and diseases of unknown etiology for 53%. In summary, cooked poultry products may become a hazard when raw or cooked products are mishandled.

Need for Microbiological Criteria

Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

Adequate data base is available (ICMSF, 1974, 1980, 1985; APHA, 1976, 1984) to guide processors in establishing and interpreting microbiological guidelines that they may wish to apply.

Where Criteria Should Be Applied

A HACCP program should be applied to the entire poultry production, processing, distribution, and food preparation chain. Critical control points at the farm include sanitary condition of feed, drinking water, equipment, and surroundings in which the birds are raised, and control of microbial contamination by farm workers, insects, rodents, and wild birds. Although each of these control measures can affect the general microbial population, the principal focus should be on reducing the incidence of pathogens, primarily Salmonella and Campylobacter.

Critical control points to be monitored at the processing plant (eviscerated ready-to-cook carcasses only) should include (1) carcass washing, cooling, and storage procedures, which include amount of water, degree of chlorination and temperature of water, and temperature of storage; (2) cleaning and sanitation of equipment; and (3) employee sanitary practices during processing. Microbiological guidelines should be applicable to: (1) periodic evaluation of equipment surfaces to check cleaning and sanitizing procedures and to check on potential buildup of microbial contaminants, and (2) examination [APC at 20–25°C (68–77°F) for 2–3 days and coliforms] of freshly processed carcasses. Excessive counts should alert the processor to check the product at various stages of processing to pinpoint the problem. Reduction of the number of birds infected with Salmonella perhaps will be possible sometime in the future by application of several measures such as use of Salmonella -free feed, application of the Nurmi concept, and irradiation of packaged raw poultry.

References

• Anonymous 1979. Report on the Scandinavian Salmonella control programs in poultry with added observations from Finland, Germany and Switzerland. Health/Agriculture/Industry Committee on Salmonella, Ottawa, Canada.
• APHA (American Public Health Association) 1976. Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• 1984. Compendium of Methods for the Microbiological Examination of Foods. 2^nd Ed. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• Bryan, F. L. 1980. Foodborne diseases in the United States associated with meat and poultry. J. Food Prot. 43:140–150. [PubMed: 30822910]
• Bryan, F. L., and T. W. McKinley 1974. Prevention of foodborne illness by time-temperature control of thawing, cooking, chilling and reheating turkeys in school lunch kitchens. J. Milk Food Technol. 37:420–429.
• Bryan, F. L., J. C. Ayres, and A. A. Kraft 1968. a. Contributory sources of salmonellae on turkey products. Am. J. Epidemiol. 87:578–591. [PubMed: 5690213]
• 1968. b. Salmonellae associated with further-processed turkey products. Appl. Microbiol. 16:1–9. [PMC free article: PMC547292] [PubMed: 5688832]
• Clark, G. M., A. F. Kaufman, E. J. Gangarosa, and M. A. Thompson 1973. Epidemiology of an international outbreak of Salmonella agona. Lancet ii:490–493. [PubMed: 4125005]
• Cunningham, F. E. 1982. Microbiological aspects of poultry and poultry products—An update. J. Food Prot. 45:149–1164. [PubMed: 30913717]
• FAO/IAEA/WHO 1977. Wholesomeness of irradiated food. Report of a joint FAO/IAEA/WHO Expert Committee. WHO Techn. Rep. Ser. 604. [PubMed: 6785929]
• FAO/WHO (Food and Agriculture Organization/World Health Organization) 1979. Report of an FAO/WHO working group on Microbiological Criteria for Foods. Geneva: FAO/WHO.
• GAO (U.S. General Accounting Office) 1974. Report to the Congress, Salmonella in raw meat and poultry: An assessment of the problem [B-164031 (2), July 22, 1974]. Washington, D.C.: U.S. General Accounting Office.
• Gardner, F. A., and F. A. Golan 1976. Water usage in poultry processing—An effective mechanism for bacterial reduction. Pp. 338–355 in Proc. 7^th Natl. Symposium on Food Processing Wastes, Atlanta, GA. Cincinnati: U.S. Envir. Prot. Agency.
• ICMSF (International Commission on Microbiological Specifications for Foods) 1974. Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and specific applications. Toronto: University of Toronto Press.
• 1980. 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, 2^nd Ed. In preparation.
• Kampelmacher, E. H. 1983. Irradiation for control of Salmonella and other pathogens in poultry and fresh meats. Food Technol. 37(4):117–119, 169.
• NRC (National Research Council) 1969. An evaluation of the Salmonella problem. Committee on Salmonella. Washington, D.C.: National Academy of Sciences.
• Pivnick, H., B. Blanchfield, and J.-Y. D'Aoust 1981. Prevention of Salmonella infections in chicks by treatment with fecal cultures from mature chickens (Nurmi Cultures). J. Food Prot. 44:909–916. [PubMed: 30856733]
• Rowe, B. 1980. Salmonella hadar—England and Wales. Morb. Mort. Weekly Rpt. 29:506–508, 513.
• Silliker, J. H. 1982. The Salmonella problem: Current status and future direction. J. Food Prot. 45:661–666. [PubMed: 30866253]
• Stersky, A., B. Blanchfield, C. Thacker, and H. Pivnick 1981. Reduction of Salmonella excretion into drinking water following treatment of chicks with Nurmi culture. J. Food Prot. 44:917–920. [PubMed: 30856734]
• USDA (U.S. Department of Agriculture) 1982. National Poultry Improvement Plan and Auxiliary Provisions. APHIS-Veterinary Services, APHIS 91–40.
• Vas, K. 1977. General survey of irradiated food products cleared for human consumption in different countries. Joint FAO/IAEA/ WHO advisory group on international acceptance of irradiated food. GA-143/INF/2-IAEA, Vienna.

Sensitivity of Products Relative to Safety and Quality

The term "further-processed poultry product" refers to any product beyond the ready-to-cook carcass, frozen or nonfrozen. Further-processed poultry products comprise a significant part of poultry marketed in the United States. In 1982, about 60% of the 16.8 billion pounds of broilers produced in the United States were in the form of cut-up parts and other further-processed products, and of the 2.5 billion pounds of turkey consumed, about 90% was in the form of further-processed products (USDA, 1983). Examples of these further-processed products are:

The microbiological condition of further-processed products and hence shelf-life and safety depends upon a series of conditions and events including:

1.

Microbiological condition of the carcass entering further processing

concern: numbers and types of microorganisms, particularly psychrotrophic bacteria and Salmonella

2.

Processing procedures

a.

parts removal—removal of drum, wings, tail, and neck

concern: sanitary handling

b.

hand deboning—removal of breast tissue and thigh tissue from carcass

concern: sanitary handling

c.

mechanical deboning—grinding of racks and other bones followed by deboning

concerns: sanitary condition of equipment, extensive increase in surface area of tissue, temperature increase of tissue at separation, handling of mechanically deboned poultry meat (MDPM): rate of cooling, time-temperature profile during storage

d.

trim operation—trimming of major muscles, breast, and thigh

concerns: sanitary handling, continuity of product flow

e.

blending—mixing of different tissues (dark, light, trim meat), seasonings and additives (salt, sugar, phosphates, erythorbate, sodium nitrite)

concerns: sanitary condition of equipment, microbial condition of additives, time-temperature profile of product, use schedule of equipment (continuity of product flow)

f.

emulsification—emulsification of tissue fractions

concerns: sanitary condition of equipment, time-temperature profile of product (heat generation), increase in tissue surface area, use schedule of equipment (continuity of product flow)

g.

stuffing—placing product in casing such as for wieners, bologna, salami, pastrami, rolls, roasts

concerns: sanitary condition of equipment, time-temperature profile of product (time between stuffing and cooking)

h.

product formation (forming)—to provide shape to a product (for example, boneless turkey breast)

concerns: sanitary condition of equipment, sanitary handling, time-temperature profile of product

i.

massaging (tumbling)—to extract protein to surface to bind product tissues together when cooked (examples turkey breast, rolls)

concerns: sanitary condition of equipment, time-temperature profile of product

j.

curing—to add or inject curing ingredients to tissue for flavor and preservative action

concerns: microbiological condition of curing ingredients or solution, sanitary condition of equipment

k.

heat treatment (cooking, smoking, canning)—to provide desirable body and texture characteristics and for destruction of microorganisms

concern: time-temperature profile of product

l.

chilling

concern: rapid chilling of cooked product

m.

packaging

concerns: sanitary condition of equipment (slicers for example), sanitary practices (particularly in repacking and weighing of cooked product), type of packaging film, container integrity, gaseous atmosphere

n.

storage of further-processed products

concerns: time-temperature profile of product, sanitary condition of coolers and freezers, inventory control and rotation

(Note: not all processing steps are applicable to each further-processed product.)

3.

Handling in food service operations and in the home

a.

storage conditions of frozen and refrigerated products

concern: time-temperature profile of product

b.

thawing of frozen product

concern: time-temperature profile of product

c.

cross-contamination

concern: contamination from raw to cooked product via cutting boards, handling, etc., and from raw product to food that receives no further heat treatment

d.

cooking of product

concern: time-temperature profile of product

e.

cooling of cooked product

concerns: rate of cooling, time-temperature profile of product

f.

storage of cooked product

concern: time-temperature profile of product

g.

reheating of product

concern: time-temperature profile of product

Quantitatively, there will be differences in the degree of "concern" depending upon the type of further-processed product. The significance of individual concerns associated with various processing, storage, and preparation practices for individual further-processed products are dealt with on the following pages. No attempt will be made to evaluate the sensitivity of all of the above-listed types of further-processed poultry products relative to safety, shelf-life, and microbiological criteria. Instead, these issues and the need for microbiological criteria will be discussed for a few typical further-processed poultry products as examples of the various factors that should be considered:

1.

tray-pack product (chilled or frozen): cut-up broilers (breast, wishbone, wings, drum, thigh, back, neck); turkeys (drum, tail, wings, neck)

2.

mechanically deboned poultry meat product: turkey wieners

3.

trim meat product: sliced turkey ham

4.

muscle product: boneless turkey breast

5.

canned product: canned chicken

6.

poultry pot pies

To evaluate shelf-life and safety of other types of products, it would be necessary to conduct a hazard analysis and establish and monitor critical control points for these products.

Need for Microbiological Criteria

Most critical control points related to further-processed poultry products can be monitored by: (1) checks of time-temperature profile of product during processing (checking temperature during cooking, cooling, and storage), (2) evaluation of sanitary condition of processing equipment and facilities, and (3) evaluation of sanitary practices of employees.

Microbiological criteria for pathogens in raw poultry would accomplish little because (1) low numbers of pathogens such as Salmonella, Campylobacter, Yersinia, C. perfringens, and S. aureus are often present on raw poultry and for the most part are unavoidable under present conditions of handling, and (2) foodborne disease problems arise when cooked products are mishandled in processing plants, food service operations, or in the home. A working group of the Codex Committee on Food Hygiene (FAO/WHO, 1979) concluded that application of microbiological criteria for raw poultry would not improve safety (see Part D, above).

Microbiological guidelines (APC) are useful to check the condition of incoming carcasses to be used for further processing, particularly if they were obtained from other sources. Relatively simple microbiological procedures (rinse, swab, direct agar contact) are available to evaluate the sanitary condition of equipment and utensils after each cleaning and sanitizing schedule and to monitor buildup of microorganisms on equipment during the processing day (APHA, 1984). The results of counts on incoming carcasses as well as those on equipment and utensils are of retrospective value. They are useful because counts on carcasses can identify suppliers that provide products with excessively high counts. High counts on equipment and utensils would alert the processor to intensify cleanup operations or review cleaning procedures. Microbiological guidelines for products after a critical control point or for finished products can be useful (1) to check conditions along the processing line and (2) to meet ''guaranteed shelf life" of product or purchaser specifications. In a cooked product the guideline should include APC (to evaluate general condition along the processing line), S. aureus (to identify lack of hygienic practices and potential temperature abuse), Salmonella (post-heat cross-contamination), and coliforms (post-heat contamination). For raw finished products, microbiological guidelines (APC) may be helpful to evaluate process control. If counts exceed guidelines that can be met when operating under good processing practices, then the processor will be alerted to check critical control points to locate and remedy the problem.

Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

Although several studies have reported on the microbiological condition of further-processed poultry products (Bryan et al., 1968a; Mercuri et al., 1970; Zottola and Busta, 1971; Robach et al., 1980), few published reports (Bryan et al., 1968b; Denton and Gardner, 1982) are available that characterize the effect of individual processing practices on the microbial flora of these products. Information in reports by ICMSF (1974, 1980, 1985) and APHA (1976, 1984) should provide useful guidelines in evaluating the microbiological condition of further-processed poultry.

Where Criteria Should Be Applied

A hazard analysis critical control point program should be applied for these products at the plant level. Various procedures including microbiological guidelines to monitor these control points have been discussed earlier in this section. Mishandling of poultry occurs in food service operations and in homes. Control of this problem should be through monitoring of critical control points, which include thawing, cooking, hot-holding, handling after cooking, chilling, and reheating. The HACCP concept described for food service operations should also be applied to the handling of foods in the home. This approach requires education of all persons in food handling procedures with particular emphasis at the grade and high school levels.

References

• APHA (American Public Health Association) 1976. Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• 1984. Compendium of Methods for the Microbiological Examination of Foods, 2^nd Ed., M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• Bailey, J. W. 1974. Encyclopedia of Labeling Meat and Poultry Products. 2^nd Ed. St. Louis: Meat Plant Magazine.
• Bryan, F. L. 1980. Foodborne diseases in the United States associated with meat and poultry. J. Food Prot. 43:140–150. [PubMed: 30822910]
• Bryan, F. L., and T. W. McKinley 1974. Prevention of foodborne illness by time-temperature control of thawing, cooking, chilling and reheating turkeys in school lunch kitchens. J. Milk Food Technol. 37:420–429.
• Bryan, F. L., J. C. Ayres, and A. A. Kraft 1968. a. Destruction of salmonellae and indicator organisms during thermal processing of turkey rolls. Poultry Sci., 47:1966–1978. [PubMed: 5716669]
• 1968. b. Salmonellae associated with further processed turkey products. Appl. Microbiol. 16:1–9. [PMC free article: PMC547292] [PubMed: 5688832]
• CDC (Center for Disease Control) 1976. Foodborne and Waterborne Disease Outbreaks. Annual Summary 1975. Atlanta: Center For Disease Control.
• Denton, J. H., and F. A. Gardner 1982. Effect of further processing systems on selected microbiological attributes of turkey meat products. J. Food Sci. 47:214–217.
• ICMSF (International Commission on Microbiological Specifications for Foods) 1974. Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and specific applications. Toronto: University of Toronto Press.
• 1980. Microbial Ecology of Foods. 2. Food Commodities. New York: Academic Press.
• 1985. Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and specific applications. In preparation.
• Mercuri, A. J., G. J. Banwart, J. A. Kinner, and A. R. Sessoms 1970. Bacteriological examination of commercial precooked Eastern-type turkey rolls. Appl. Microbiol. 19:768–771. [PMC free article: PMC376785] [PubMed: 4316271]
• Robach, M. C., E. C. To, S. Meydav, and C. F. Cook 1980. Effect of sorbates on microbiological growth in cooked turkey products. J. Food Sci. 45:638–640.
• USDA (U.S. Department of Agriculture) 1983. Poultry-Production, Disposition & Income 1981–1982. Statistical Reporting Service. Pou-2-3, April 83.
• Zottola, E. A., and F. F. Busta 1971. Microbiological quality of further-processed turkey products. J. Food Sci. 36:1001–1004.

Sensitivity of Products Relative to Safety and Quality

Eggs and egg products are regulated by the USDA, the legislative base being the Egg Products Inspection Act of 1970 (U.S. Congress, 1970). The term "egg" means the shell egg of domesticated chicken, turkey, duck, goose, or guinea. The term "egg product" means any dried, frozen, or liquid eggs with or without added ingredients, excepting products that contain eggs only in a relatively small proportion. Processors of egg products are subject to continual USDA inspection. Though shell eggs are covered under the Egg Products Inspection Act, their processing is not under continual inspection.

Historically, consumption of eggs and egg products has been an important cause of human salmonellosis. Between 1963 and 1975 there were 651 outbreaks of human salmonellosis reported to the Center for Disease Control, and the vehicle of transmission was identified in 463 (71%) of these occurrences. Of these, poultry accounted for 99 (21%), meat for 69 (15%); and eggs for 53 (11%). These data, reviewed by Cohen and Blake (1977), show that poultry, meat, and eggs were vehicles in approximately half of the outbreaks of human salmonellosis during this 13-year period. The percentage of outbreaks caused by eggs decreased dramatically after 1966 (see Figure 9-1). Of 10 egg-related outbreaks occurring between 1968 and 1975, 9 were associated with shell eggs and only 1 with egg products. The vastly improved safety position of eggs and egg products has been maintained since 1975 through to the present time. This may be traced to consumer education and to improvements made by egg producers and processors. Of great importance was enforcement of the Egg Products Inspection Act of 1970, which placed egg products, as well as shell eggs, under supervision by USDA. The Egg Products Inspection Act, as of July 1972, eliminated human consumption of high-risk shell eggs, namely, checks, dirties, incubator rejects, and leakers. Furthermore, the Egg Products Inspection Act required that all egg products be pasteurized to render them free of salmonellae.

Figure 9-1

Percentage of salmonellosis outbreaks (outbreaks caused by unidentified vehicle are eliminated) caused by poultry, meat, or eggs. United States, 1963–1975. SOURCE: Cohen and Blake, 1977.

The Salmonella Standard

As indicated above, federal law has established a standard requiring that egg products, except unpasteurized salted egg products used in acidic dressings, be free of Salmonella. The USDA is responsible for administration of this standard. Details of this activity are contained in AMS-PY instruction number 910, Egg Products-1 (USDA, 1975). This document recognizes three different types of sampling and testing, namely certification, surveillance, and confirmation.

Certification means certifying to the quality of a specific lot. Samples are drawn by the USDA inspector and submitted to a USDA laboratory. An attribute sampling plan is prescribed. Samples are randomly drawn from the final shipping containers. The number of containers sampled is determined by the number of containers in the lot. For example, with liquid and frozen egg products, the sampling plan below is used.

For dried egg products the following sampling plan is prescribed.

In applying this plan, the units randomly selected for sampling are segregated into groups of four. Two or three ounces of product are withdrawn from each unit in the group, and these samples are combined in a single container, mixed, and a 100-g composite sample is taken and analyzed Salmonella. With reference to dried products, then, a single 100-g sample is analyzed for lots comprised of 50 or fewer containers; whereas 5 x 100-g composites are analyzed for lots comprised of over 1,500 containers. Thus, the stringency of the sampling plan is related to the number of containers within a lot. If one considers a lot to be comprised of an infinite number of 25-g units, then for dried egg products, the plan applied varies from n = 4 to n = 20. For liquid and frozen egg products, the plan varies from n = 4 to n = 16. As indicated in Chapter 6, lot size has little effect on the probability of acceptance of large lots. Selecting the number of sample units as a percentage of lot size really serves no purpose. In the above case, however, lot size not only influences the number of units sampled but also the amount of sample analyzed. Thus, the USDA approach to certification samples encompasses variation in the stringency of the sampling plan with lot size, and furthermore the plan utilized may vary from one that is extremely loose to one that has a moderate degree of strigency.

Surveillance as applied to the Egg Products Inspection Act means "the sampling of pasteurized products on a statistical basis and analyzing for the presence of Salmonella by any laboratory using the USDA method of analysis" (AMS-PY instruction no. 910) (USDA, 1975). Plants without an established history of producing products free of Salmonella are required to start sampling 100% of the lots in the order produced. As indicated in Figure 9-2, if 83 consecutive lots are found negative for Salmonella, the plan permits inspection of every other lot. If 83 inspected lots at this level are found negative for Salmonella then the frequency is shifted to one lot in four level (level 2). If 83 inspected lots are found negative, then the sampling rate becomes one in eight lots (level 3). As further indicated in Figure 9-2, the finding of a positive lot "triggers" an increased frequency of sampling. The sampling plan initially applies to each day's production, each category of product, or each product. When a product is found to be positive, that product or category of product has a separate sampling plan until a satisfactory history of analyses is established. Any reduction or tightening of frequency of sampling applies separately to each product or category and not to cumulative results. It is of interest to note that the USDA instruction (AMS-PY instruction no. 910) (USDA, 1975) states that no rigid or set sampling pattern is to be followed. It suggests alternation between frozen and liquid product and between first and last product packed. For surveillance sampling a single 100-g frozen or liquid product is subjected to analysis. For dried samples three separate 25-g samples are analyzed (H. Maguire, 1982. Personal communication). Thus, again considering a lot to be composed of an infinite number of 25-g units, for liquid products n = 4 and for dried products n = 3.

Figure 9-2

Flow process chart for multilevel continuous sampling plans (i = 83, f = 1/2, f² = 1/4, f³ = 1/8). SOURCE: USDA, 1975 (From AMS-PY Instruction No. 910 [Egg Products]—1; Exhibit 8.)

Confirmation is "sampling and analyses, at government expense and direction, to verify the accuracy of the company's surveillance program

and analyses" (USDA, 1975). The USDA inspector draws confirmation samples from pasteurized liquid, frozen, and dried egg products in the final type of package in which the product is to be shipped. The inspector does not draw confirmation samples when the plant submits all their surveillance samples to a USDA laboratory. A 4-oz. sample is submitted for analysis, and the USDA laboratory analyzes 100 grams (n = 4). The confirmation sampling program is a "spot check" program for frozen and liquid products; the frequency of sampling is related to the surveillance sampling rate. For example, if a plant is on a 100% or a one in two surveillance sampling program for frozen or liquid products, then one confirmation sample per week is submitted for analysis. For a surveillance sampling program of one in four, two confirmation samples per month are submitted. For a surveillance level of one in eight, one confirmation sample per month is analyzed. For dried products the frequency of confirmation samples is one per week for yellow products (whole egg or yolk), two per month for spray dried egg whites, and one per month for pan-dried egg whites.

The USDA provides for retesting of lots found positive for Salmonella (USDA, 1977). Plants with known Salmonella problems are not permitted to resample. When permission is granted to resample, product is divided into sublots of not more than 100 containers or not more than 3,000 pounds. The number of containers to be drilled for a sample is the square root of each sublot. A 100-g sample is analyzed from each sublot, and each sublot is analyzed separately. The product may be released when the retest results of all the sublots are negative for Salmonella. If the retest result of any one sublot is positive for Salmonella, the entire original lot or day's production for the product involved is repasteurized and retested.

Probabilities Associated with the "Salmonella Standard"

The National Research Council (NRC) Committee on Salmonella categorized foods according to degree of risk to the consumer (NRC, 1969). Egg products, most conservatively, would be placed in Category III as they have historically been considered potential sources of salmonellae in finished products. Furthermore, during their use egg products may be exposed to conditions permitting the growth of salmonellae. Since egg products are subjected to a pasteurizing step capable of destroying salmonellae, they are subject, in theory, to only two of the three hazard potentials delineated in the NRC report. One might argue that pasteurized egg products are subject to post-pasteurization contamination or, on the other hand, that they are consumed by high-risk populations. Accordingly, a case may be made for placing them in a higher hazard category, namely I or II. Thus, these products could be placed in Category I, II, or III, depending upon one's point of view. According to the NRC report, Category III products are to be analyzed by a sampling scheme involving the analysis of thirteen 25-g samples, all of which must be negative. Given these results, there is a 95% probability of one organism or less in 125 g of product. The USDA surveillance sampling plan for dried eggs, based upon the analyses of three 25-g samples per lot, falls far short of NRC recommendations. Indeed, based upon the assumption of random distribution of salmonellae within a particular lot, the probability of accepting a lot with an average Salmonella contamination of one organism per 125 grams is 55% (see Figure 9-3). Thus a lot of the quality that should be rejected according to the NRC Category III sampling plan would be accepted by the USDA sampling plan 55% of the time. And this, in fact, is the USDA surveillance sampling plan that is used to determine how frequently a given processor must conduct Salmonella tests on his products. The statistics are only slightly more favorable using the sampling plan prescribed for liquid or frozen eggs wherein a single 100-g sample is analyzed (n = 4 instead of n = 3).

Figure 9-3

Operating characteristic curve—homogeneous distribution of salmonellae contamination. SOURCE: Recommendations by the Subcommittee on Sampling and Methodology for Salmonellae in Eggs, Egg Products and Prepared Mixes, Inter-Industry Committee on (more...)

With respect to certification samples, the USDA program similarly falls short of the NRC recommendations. Here, the number of samples analyzed (n) is determined by the number of shipping containers within a lot. The virtue of this approach, of course, lies in the fact that the larger the number of units, the more individuals at risk, ignoring the unit weight of the containers themselves. But for the smallest lot (50 containers or less), n = 4, thus employing a consumer's risk far greater than contemplated by the NRC committee. For the largest lot (greater than 1,500 shipping containers of dried eggs), n = 20, the sampling plan is somewhere between a Category II and Category III, according to the NRC report. For liquid and frozen eggs, the sampling plan for the largest lot involves the analyses of three 100-g composite samples (n = 12), which falls short of the stringency recommended by the NRC. In terms of assessing the microbiological safety of individual lots of product, it is difficult to justify the stringency of varying sampling plans depending upon lot size (see Chapter 6).

Likewise, the USDA confirmation sampling program falls far short of NRC recommendations. A single 100-g sample (n = 4) is analyzed.

Since the USDA surveillance sampling program is based upon somewhat unsound statistical premises, it may be argued that the total surveillance program is in question. The credibility of the USDA certification, surveillance and confirmation sampling plans could be significantly improved simply by increasing the weight of the samples analyzed in connection with this program. If one classifies these products as Category III, then the analysis of a single composite 325-g sample (n = 13) would give 95% probability of 1 Salmonella or less in 125 g of product. If one were to consider these products in Category II, then the analysis of a total of 725 g of product would give a 95% probability of 1 organism or less in 250 g. The present USDA sampling schemes fall far short of those recommended by the NRC and reliance upon them carries far too great a consumer risk.

Fortunately there has been only one outbreak of human salmonellosis traced to egg products since the Egg Products Inspection Act (CDC, 1977a,b). This outbreak was caused by dried egg albumen, contaminated with Salmonella infantis. The product was an ingredient of a ''Precision Isotonic Diet," a formula for oral or tube feedings used in hospitalized individuals of all ages. One cannot, however, attribute the good recent public health record of egg products to the effectiveness of the USDA sampling programs. The fact is that producers of these products have employed far more stringent sampling plans than those prescribed by the USDA. Furthermore, users of egg products have, through their purchase specifications, required that products be analyzed according to the sampling plans recommended by the NRC Committee on Salmonella.

The dramatic decrease in egg-associated outbreaks attests to the success of mandatory pasteurization of egg products, as well as the Egg Products Inspection Program of USDA. The subcommittee recommends the continuation of the USDA program, with the intensification of the Salmonella sampling and testing indicated in this chapter.

References

• Anonymous 1966. Recommendations for sampling and laboratory analysis of eggs, egg products and prepared mixes. A report. Food Technol. 20(4):121–129.
• Bergquist, D., A. Kraft, O. Cotterill, and H. Maguire 1984. Eggs and Egg Products. In Compendium of Methods for the Microbiological Examination of Foods, M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• CDC (Center for Disease Control) 1977. a. Salmonella infantis—California, Colorado. Morb. Mort. Weekly Rpt. 26:41.
• 1977. b. Follow-up on Salmonella infantis—United States. Morb. Mort. Weekly Rpt. 26:84.
• Cohen, M. L., and P. A. Blake 1977. Trends in foodborne salmonellosis outbreaks: 1963–1975. J. Food Protect. 40:798–800. [PubMed: 30736229]
• NRC (National Research Council) 1969. An Evaluation of the Salmonella Problem. Committee on Salmonella. Washington, D.C.: National Academy of Sciences.
• U.S. Congress 1970. Eggs Products Inspection Act. P.L. 95–597 (H. R. 19888). Dec. 29.
• USDA (U.S. Department of Agriculture) 1975. Section 8—Sampling for bacteriological, chemical and physical testing. AMS-PY Instruction No. 910 (Egg Products)—1. Implementation of Egg Products Inspection Act. Washington, D.C.: Agricultural Marketing Service, USDA.
• 1977. Implementation of Egg Products Inspection Act. Section 9—Handling Salmonella Positive Samples. Revised. Washington, D.C.: Agricultural Marketing Service.
• 1980. Regulations governing the inspection of eggs and egg products. Code of Federal Regulations 7 CFR Part 2859.

Sensitivity of Products Relative to Safety and Quality

Need for Microbiological Criteria

The safety and quality of fish and fishery products can best be assured by application of the HACCP system. For fresh products, monitoring of critical control points should consist primarily of inspection of incoming materials for odor and appearance, proper temperature control (refrigeration and/or freezing), cleaning and sanitizing of equipment and utensils, and handling of product by employees. In addition, for molluscan shellfish it should include analysis of the growing water and the product (at wholesale) for fecal coliforms and of the product for saxitoxin and related toxins. For processed tuna, histamine is the agent of concern (see previous discussion on scombroid poisoning). For cooked ready-to-eat products such as cooked peeled deveined shrimp and crabmeat, microbiological guidelines

for the finished products should include APC, E. coli, and S. aureus . These parameters are useful to evaluate faulty processing and/or handling practices such as inadequate heating, cross-contamination with raw product, contamination from workers, and inadequate refrigeration which may create health hazards. For all processed fish and seafoods, the HACCP system is recommended as the basis for assuring safety and quality and within this system microbiological guidelines should be implemented where needed to monitor critical control points.

An examination of microbiological criteria that exist for fishery products in the various states shows that the most common criterion is that for shellfish as developed by the NSSP, or one closely resembling that criterion (Martin and Pitts, 1981). However, some states and local regulatory agencies have additional microbiological criteria for fish and seafoods (Wehr, 1982). Unfortunately, most of these criteria are not based on sound data or experience and are impractical from the standpoint of compliance or enforcement. If there is a need for additional microbiological criteria these should be based on properly designed and executed studies.

Recently, quality standards have been recommended for frozen crab cakes, frozen fish cakes, and frozen fish sticks (FDA, 1980, 1981). However, these products constitute neither a health hazard nor a serious quality problem. In addition, the methods used to establish "m" and "M" for these microbiological criteria are inconsistent with the principles on which the 3-class plan was established (Clark, 1982; ICMSF, 1974; see Chapter 6). The limit "M" represents the level at which a food is considered defective and unacceptable because (1) the number of organisms is so high that shelf-life is unacceptably short, (2) the microbiology is indicative of unacceptable sanitary conditions during manufacturing or handling, or (3) the microbiological data indicate that the product is unsafe or is a health hazard. "M'' for frozen crab cakes, fish cakes, and fish sticks was so selected that it exceeded 99% of the survey population with 99% confidence. In addition, data used for these criteria were based on bacteriological surveys conducted at the retail level. Because of the potential for changes in the microbiological characteristics of the food between manufacture (at the plant level) and the time of purchase, it would be difficult to place the responsibility for unsatisfactory condition at the retail level on unsatisfactory processing or handling at the manufacturing level. (For further discussion of microbiological quality standards, see Chapter 2.)

Where Criteria Should Be Applied

As described above, for certain products, microbiological criteria are applied to the growing water (shellfish); for others, they are applied at the processing plant level. Purchase specifications may be useful to food service operators to monitor incoming products as part of their HACCP program unless the manufacturer can provide data about the quality and safety of the products.

References

• Blake, P. A., D. T. Allegra, J. D. Snyder, T. J. Barrett, L. McFarland, C. T. Caraway, J. C. Feeley, J. P. Craig, J. V. Lee, N. D. Puhr, and R. A. Feldman 1980. Cholera—a possible endemic focus in the United States. New Engl. J. Med. 302:305–309. [PubMed: 7350497]
• Bryan, F. L. 1980. Epidemiology of foodborne diseases transmitted by fish, shellfish and marine crustaceans in the United States, 1970–1978. J. Food Prot. 43:859–876. [PubMed: 30836460]
• CDC (Centers for Disease Control) 1981. Cholera—Texas. Morb. Mort. Weekly Rpt. 30:389–390. [PubMed: 6790930]
• Clark, D. S. 1982. International perspectives for microbiological sampling and testing of foods. J. Food Prot. 45:667–671. [PubMed: 30866250]
• Colwell, R. R., J. Kaper, and S. W. Joseph 1977. Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 198:394–396. [PubMed: 910135]
• Colwell, R. R., R. J. Seidler, J. Kaper, S. W. Joseph, S. Garges, H. Lockman, D. Maneval, H. Bradford, N. Roberts, E. Remmers, I. Huq, and A. Huq . [PMC free article: PMC243732] [PubMed: 7235699]
• 1981. Occurrence of Vibrio cholerae serotype O1 in Maryland and Louisiana estuaries. Appl. Environ. Microbiol. 41:555–558. [PMC free article: PMC243732] [PubMed: 7235699]
• Eklund, M. W. 1982. Significance of Clostridium botulinum in fishery products preserved short of sterilization. Food Technol. 36(12):107–112, 115.
• Eyles, M. J., and A. D. Warth 1981. Assessment of the risk of botulism from vacuum-packaged raw fish: A review. Food Technol. Austral. 33(11):574–580.
• FDA (Food and Drug Administration) 1980. Frozen fish sticks, frozen fish cakes, and frozen crab cakes; Recommended microbiological quality standards. Federal Register 45 (108):37524–37526.
• 1981. Frozen fish sticks, frozen fish cakes, and frozen crab cakes; Recommended microbiological quality standards. Federal Register 46 (113):31067–31068.
• 1982. Defect action levels for histamine in tuna; availability of guide. Federal Register 47 (178):40487–40488.
• Hickman, F. W., J. J. Farmer, III, D. G. Hollis, G. R. Fanning, A. G. Steigerwalt, R. E. Weaver, and D. J. Brenner 1982. Identification of Vibrio hollisae sp. nov. from patients with diarrhea. J. Clin. Microbiol. 15:395–401. [PMC free article: PMC272106] [PubMed: 7076812]
• Hood, M. A., G. E. Ness, and G. E. Roderich 1981. Isolation of Vibrio cholerae serotype O1 from the Eastern oyster, Crassostrea virginica. Appl. Environ. Microbiol. 41:559–560. [PMC free article: PMC243733] [PubMed: 7235700]
• ICMSF (International Commission on Microbiological Specifications for Foods) 1974. Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and specific applications. Toronto: University of Toronto Press.
• Kaper, J., H. Lockman, R. R. Colwell, and S. W. Joseph 1979. Ecology, serology and enterotoxin production of Vibrio cholerae in Chesapeake Bay. Appl. Environ. Microbiol. 37:91–103. [PMC free article: PMC243406] [PubMed: 367273]
• Lee, D. A., M. Solberg, D. Furgang, and J. J. Specchio 1983. Time to toxin detection and organoleptic deterioration in Clostridium botulinum inoculated fresh fish fillets during modified atmosphere storage. Paper (No. 483) presented at the 43^rd Annual IFT Meeting, New Orleans.
• Lerke, P. A., M. N. Porcuna, and H. B. Chin 1983. Screening test for histamine in fish. J. Food Sci. 48:155–157.
• Lindsay, R. C. 1983. Safety and technology of modified-atmosphere packaging of fresh fish. Paper (No. 152) presented at the 43^rd Annual IFT Meeting, New Orleans.
• Llobera, A. T. 1983. Bacteriological safety assessment of Clostridium botulinum in fresh fish and shellfish packaged in modified atmosphere containing CO₂. Ph.D. dissertation, Texas A&M University, College Station. August.
• Martin, R. E., and G. T. Pitts 1981. Handbook of State and Federal Microbiological Standards and Guidelines. Washington, D.C.: National Fisheries Institute.
• National Blue Crab Industry Association 1982. Tri-State Seafood Committee GMP Recommendations. Washington, D.C.: National Blue Crab Industry Association.
• Nickelson, R., L. E. Wyatt, and C. Vanderzant 1975. Reduction of Salmonella contamination in commercially processed frog legs. J. Food Sci. 40:1239–1241.
• Phillips, F. A., and J. T. Peeler 1972. Bacteriological survey of the blue crab industry. Appl. Microbiol. 24:958–966. [PMC free article: PMC380704] [PubMed: 4568256]
• USDHEW (U.S. Department of Health, Education and Welfare) 1965. National Shellfish Sanitation Program. Manual of Operations. Part 1—Sanitation of Shellfish Growing Areas. PHS Pub. 33 (Revised 1965). Washington, D.C.: U.S. Government Printing Office.
• USPHS (U.S. Public Health Service) 1975. National Shellfish Safety Program. Federal Register 40 (119):25916–25935.
• Wehr, H. M. 1982. Attitudes and policies of governmental agencies on microbial criteria for foods—an update. Food Technol. 36(9):45–54, 92.

Sensitivity of Products Relative to Safety and Quality

Raw fruits and vegetables are not common causes of foodborne illnesses in the United States (CDC, 1971; 1972; 1973; 1974; 1976a,b; 1977; 1979; 1981a,b). The high acidity of many fruits inhibits the growth of bacteria pathogenic for humans and the edible portions often are protected from contamination by a skin or thick rind. Although the vegetables that are eaten raw, such as in salads, may yield APCs of 10⁷/g or greater (Fowler and Foster, 1976), they have not presented a serious public health problem in the United States and Canada because the microorganisms are mainly saprophytic species (Splittstoesser, 1970). However, in countries where polluted water or raw sewage are used for irrigation or fertilization of crops, enteric pathogens such as salmonellae and parasites are common contaminants (Ercolani, 1976; Tamminga et al., 1978). Certain imported fruits and vegetables, then, might be potential sources of foodborne illness.

A recently recognized potential problem has been the presence of Clostridium botulinum spores on raw potatoes that will be baked in foil. It has been hypothesized that a botulism outbreak occurred because foil-wrapped baked potatoes that were used in a potato salad had been held at room temperature for a number of days. Laboratory studies showed that botulinum spores can survive baking and that vegetative growth and toxin production can occur in the foil-wrapped product (Seals et al., 1981).

Mung bean and other vegetable sprouts that are often consumed raw develop high populations of bacteria during the sprouting process. Although sprouts usually are negative for foodborne pathogens (Patterson and Woodburn, 1980), at least one outbreak has been attributed to Bacillus cereus (Portnoy et al., 1976).

Nonsterile processed fruits and vegetables, such as frozen and desiccated products, have rarely been responsible for foodborne illnesses. The few cases that are reported each year have generally been due to contamination or mishandling by persons in food service establishments or home kitchens (see for example CDC, 1981b).

Commercially canned fruits and vegetables have an excellent public health record (see sections on canned foods). Home-canned vegetables, on the other hand, have been a major cause of botulism in the United States with 48 outbreaks occurring during the period 1970 to 1979 (CDC, 1971; 1972; 1973; 1974; 1976a,b; 1977; 1979; 1981a,b). The application of microbiological criteria would not have reduced the incidence of botulism since the outbreaks were due to underprocessing in the home.

Need for Microbiological Criteria

Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

The microbiology of frozen vegetables depends upon the vegetable type and the method of processing (Barnard et al., 1982; Duran et al., 1982; Splittstoesser and Corlett, 1980). For example, green beans usually show higher aerobic plate counts than do peas, and French-style green beans are more heavily contaminated than are the cut variety. Presently lacking are modern data that would relate the microbiology of these foods to Good Manufacturing Practices. This information can be generated only through extensive factory surveys. Similar studies would be needed for frozen fruits as well as for nonsterile fruits and vegetables that are preserved by other means.

The Howard mold count and rot fragment standards have been used for many years (FDA, 1978). Although G. candidum has long been promulgated by FDA as an indicator of insanitation in tomato processing (Eisenberg and Cichowicz, 1977), more data would be needed (again, developed from extensive factory surveys) before meaningful limits based on filament counts could be established for this and other vegetables (Splittstoesser et al., 1980b).

A number of states have guidelines for horticultural products such as frozen potatoes, frozen onion rings, and pasteurized fruit juices (Wehr, 1982). There is little evidence to justify them.

Where Criteria Should Be Applied

Microbiological guidelines would usually be applied to frozen and dried fruits and vegetables following packaging. The samples can therefore be taken from the processing plant, warehouses, or retail markets. While market samples would show the microbiological condition of a food as purchased by the consumer, they might not permit an interpretation as to the reason for the particular findings.

When the objective of the guideline is to monitor a critical control point in the process line, samples would be collected at or following this point.

References

• AOAC (Association of Official Analytical Chemists) 1980. Official Methods of Analysis, 13^th Ed. Washington, D.C.: AOAC.
• Barnard, R. J., A. P. Duran, A. Swartzentruber, A. H. Schwab, B. A. Wentz, and R. B. Read, Jr. 1982. Microbiological quality of frozen cauliflower, corn and peas obtained at retail markets. Appl. Environ. Microbiol. 44:54–58. [PMC free article: PMC241967] [PubMed: 6751226]
• CDC (Centers for Disease Control) 1971. Foodborne Outbreaks. Annual Summary 1970. Atlanta: Centers for Disease Control.
• 1972. Foodborne Outbreaks. Annual Summary 1971. Atlanta: Centers for Disease Control.
• 1973. Foodborne Outbreaks. Annual Summary 1972. Atlanta: Centers for Disease Control.
• 1974. Foodborne and Waterborne Disease Outbreaks. Annual Summary 1973. Atlanta: Centers for Disease Control.
• 1976. a. Foodborne and Waterborne Disease Outbreaks. Annual Summary 1974. Atlanta: Centers for Disease Control.
• 1976. b. Foodborne and Waterborne Disease Outbreaks. Annual Summary 1975. Atlanta: Centers for Disease Control.
• 1977. Foodborne and Waterborne Disease Outbreaks. Annual Summary 1976. Atlanta: Centers for Disease Control.
• 1979. Foodborne and Waterborne Disease Outbreaks. Annual Summary 1977. Atlanta: Centers for Disease Control.
• 1981. a. Foodborne Disease Outbreaks. Annual Summary 1978. Atlanta: Centers for Disease Control.
• 1981. b. Foodborne Disease Outbreaks. Annual Summary 1979. Atlanta: Centers for Disease Control.
• Duran, A. P., A. Swartzentruber, J. M. Lanier, B. A. Wentz, A. H. Schwab, R. J. Barnard, and R. B. Read, Jr.
• 1982. Microbiological quality of five potato products obtained at retail markets. Appl. Environ. Microbiol. 44:1076–1080. [PMC free article: PMC242151] [PubMed: 6758695]
• Eisenberg, W. V., and S. M. Cichowicz 1977. Machinery mold—Indicator organism in food. Food Technol. 31(2):52–56.
• Ercolani, G. L. 1976. Bacteriological quality assessment of fresh marketed lettuce and fennel. Appl. Environ. Microbiol. 31:847–852. [PMC free article: PMC169844] [PubMed: 820256]
• FDA (Food and Drug Administration) 1978. The food defect action levels. Food and Drug Administration, HFF-342, Washington, D.C.
• Fowler, J. L., and J. F. Foster 1976. A microbiological survey of three fresh green salads—Can guidelines be recommended for these foods? J. Milk Food Technol. 39:111–113.
• Hill, E. C., and F. W. Wenzel. 1957. The diacetyl test as an aid for quality control of citrus products. 1. Detection of bacterial growth in orange juice during concentration. Food Technol. 11:240–243.
• Patterson, J. E., and M. J. Woodburn 1980. Klebsiella and other bacteria on alfalfa and bean sprouts at the retail level J. Food Sci. 45:492–495.
• Portnoy, B. L., J. M. Goepfert, and S. M. Harmon 1976. An outbreak of Bacillus cereus food poisoning resulting from contaminated vegetable sprouts. Am. J. Epidemiol. 103:589–593. [PubMed: 820192]
• Seals, J. E., J. D. Snyder, T. A. Edell, C. L. Hatheway, C. J. Johnson, R. C. Swanson, and J. M. Hughes 1981. Restaurant-associated type A botulism: Transmission by potato salad. Am. J. Epidemiol. 113:436–444. [PubMed: 7010999]
• Splittstoesser, D. F. 1970. Predominant microorganisms on raw plant foods. J. Milk Food Technol. 33:500–505.
• 1973. The microbiology of frozen vegetables. Food Technol. 27(1):54–56, 60.
• Splittstoesser, D. F., J. Bowers, L. Kerschner, and M. Wilkison 1980. b. Detection and incidence of Geotrichum candidum in frozen blanched vegetables. J. Food Sci. 45:511–513.
• Splittstoesser, D. F., and D. A. Corlett, Jr. 1980. Aerobic plate counts of frozen blanched vegetables processed in the United States. J. Food Protect. 43:717–719. [PubMed: 30822831]
• Splittstoesser, D. F., and J. O. Mundt 1976. Fruits and vegetables. In Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D.C.: American Public Health Association.
• Splittstoesser, D. F., and B. Segen 1970. Examination of frozen vegetables for salmonellae. J. Milk Food Technol. 33:111–113.
• Splittstoesser, D. F., G. E. R. Hervey II, and W. P. Wettergreen 1965. Contamination of frozen vegetables by coagulase positive staphylococci. J. Milk Food Technol. 28:149–151.
• Splittstoesser, D. F., D. T. Queale, J. L. Bowers, and M. Wilkison 1980. a. Coliform content of frozen blanched vegetables packed in the United States. J. Food Safety 2:1–11.
• Tamminga, S. K., R. R. Beumer, and E. H. Kampelmacher 1978. The hygienic quality of vegetables grown in or imported into the Netherlands: A tentative survey. J. Hyg., Camb. 80:143–154. [PMC free article: PMC2129984] [PubMed: 340581]
• Wehr, H. M. 1982. Attitudes and policies of governmental agencies on microbiological criteria for foods—An update. Food Technol. 36(9):45–54, 92.

Sensitivity of Products Relative to Safety and Quality

Fruit beverages have had an excellent public health record. Most possess a low pH, which prevents growth of pathogenic bacteria, and many juice products are given a thermal process that kills microorganisms of spoilage and public health significance.

While it is believed that enteric pathogens usually die off rapidly when in a highly acidic environment, Salmonella typhimurium has been shown to survive when inoculated into apple juice (Goverd et al., 1979) and nonpasteurized cider was responsible for a large outbreak of salmonellosis (CDC, 1975).

Heat-resistant molds, mainly species of Byssochlamys, Aspergillus fisheri, and Penicillium vermiculatum may cause spoilage of pasteurized fruit beverages because their ascospores are sufficiently resistant to survive the usual heat treatments that are given to these foods (Splittstoesser and Splittstoesser, 1977; Van der Spuy et al., 1975). The spores are present in orchards and vineyards (Splittstoesser et al., 1971), and thus are introduced into the beverage via the fruit. It is not uncommon to find low numbers of viable ascospores in juice concentrates.

Usually only a limited amount of mold growth occurs in a canned fruit beverage due to the low levels of oxygen present. However, off-flavors may be apparent and some heat-resistant molds may produce mycotoxins such as patulin (Rice et al., 1977).

Need for Microbiological Criteria

Standards are not needed because fruit juice beverages are rarely responsible for foodborne illnesses.

Guidelines are useful for the assessment of good manufacturing practices. Counts of yeasts and lactic acid bacteria in most fruit juices (Luthi, 1959; Murdock, 1976) and levels of diacetyl in citrus juices (Hill and Wenzel, 1957) often can be correlated with conditions of sanitation. Trace levels of patulin in apple juice are indicative of the pressing of fruit rotted by Penicillium expansum and other molds (Lindroth and Niskanen, 1978). A criterion for patulin in apple juice might be useful. Testing for coliforms is of limited value because they constitute a part of the normal processing line microflora and their presence does not indicate fecal contamination (Dack, 1955; Patrick, 1953).

Purchase specifications that limit heat-resistant mold spores in juice concentrates are useful. Also, specifications for mesophilic bacteria, yeasts, and molds in sugar to be used in nonpasteurized beverages are applicable (see Chapter 9, Part O).

Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

While companies may possess a wealth of data that relate processing conditions to the microbiology of their products, little information is available in the literature. Therefore, extensive surveys of fruit beverage processing lines might be required if a guideline were to be applied.

Where Criteria Should Be Applied

Guidelines can be applied to frozen, nonsterile products such as fruit juice concentrates at all stages of processing including the end product. With thermally processed beverages, on the other hand, analyses are most useful at critical control points prior to pasteurization. Beverages to be treated with preservatives are usually analyzed prior to packaging. Ingredients subjected to specifications should be tested after receipt by the purchaser.

References

• CDC (Center for Disease Control) 1975. Salmonella typhimurium outbreak traced to a commercial apple cider. Morb. Mort. Weekly Rpt. 24:87.
• Dack, G. M. 1955. Significance of enteric bacilli in foods. Am. J. Pub. Health 45:1151–1156. [PMC free article: PMC1623446] [PubMed: 13249004]
• Goverd, K. A., F. W. Beech, R. P. Hobbs, and R. Shannon 1979. The occurrence and survival of coliforms and salmonellae in apple juice and cider. J. Appl. Bacteriol. 46:521–530. [PubMed: 39057]
• Hill, E. C., and F. W. Wenzel 1957. The diacetyl test as an aid for quality control of citrus products. 1. Detection of bacterial growth in orange juice during concentration. Food Technol. 11:240–243.
• Lindroth, S., and A. Niskanen 1978. Comparison of potential patulin hazard in home made and commercial apple products. J. Food Sci. 43:446–448.
• Luthi, H. 1959. Microorganisms in noncitrus juices. Pp. 221–284 in Advances in Food Research. Vol. 9. E. M. Mrak, editor; and G. F. Steward, editor. , eds. New York: Academic Press.
• Murdock, D. I. 1976. Fruit drinks, juices, and concentrates. In Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D. C.: American Public Health Association.
• Patrick, R. 1953. Coliform bacteria from orange concentrate and damaged oranges. Food Technol. 7:157–159.
• Rice, S. L., L. R. Beuchat, and R. E. Worthington 1977. Patulin production by Byssochlamys spp. in fruit juices. Appl. Environ. Microbiol. 34:791–796. [PMC free article: PMC242749] [PubMed: 596876]
• Splittstoesser, D. F., and C. M. Splittstoesser 1977. Ascospores of Byssochlamys fulva compared with those of a heat resistant Aspergillus. J. Food Sci. 42:685–688.
• Splittstoesser, D. F., F. R. Kuss, W. Harrison, and D. B. Prest 1971. Incidence of heat-resistant molds in eastern orchards and vineyards. Appl. Microbiol. 21:335–337. [PMC free article: PMC377171] [PubMed: 5544294]
• Van der Spuy, J. E., F. N. Matthee, and D. J. A. Crafford 1975. The heat resistance of moulds Penicillium vermiculatum Dangeard and Penicillium brefeldianum Dodge in apple juice. Phytophylactica 7(3):105–107.

Sensitivity of Products Relative to Safety and Quality

Need for Microbiological Criteria

The presence of C. botulinum in processed low-acid canned foods is expected to occur so infrequently that no conceivable sampling plan for microbiological testing of finished product or by incubation test is a practical means of assuring safety. The Food and Drug Administration (FDA, 1973a) suggests finished product incubation and evaluation for aseptically processed canned foods, the primary purpose of which is to detect sterility breaks in the aseptic canning system. The U.S. Department of Agriculture requires incubation of approximately 1 container of meat and poultry containing low-acid canned foods per 1,000 processed as a check against gross underprocessing or container failure.

The safety of low-acid canned foods is based upon the establishment of heat processes capable of destroying C. botulinum, or in the case of shelf-stable cured meat, the control of the interrelated factors preventing C. botulinum outgrowth in the cured meat environment. The control of spoilage depends upon the establishment of heat processes capable of destroying spoilage organisms, some of which are more resistant than C. botulinum, and/or controlling the numbers of these organisms through judicious selection of raw materials.

The control of safety and stability is accomplished through the application of the HACCP system. In no phase of food processing is monitoring of critical control points so essential to the safety and stability of finished products as it is in the manufacture of low-acid canned foods. Indeed, monitoring, the extent of which has been reviewed by Ito (1974), is subject to federal regulations (FDA, 1973a,b; FPI, 1975). Physical and chemical tests are performed during production to ensure that all factors necessary to the application of the established safe processes have been adequately controlled. Numerous checks and tests are made at various critical control points, including the adequacy of ingredient blending, determination of consistency, ratio between solids and liquids, weight of product placed in the container, amount of head space, adequacy of double seam, time and temperature during sterilization, quality of cooling water, and post-processing handling of cooled cans. There is no intent above to indicate all the points that are monitored. Rather, the object is to emphasize the importance of checking each critical control point to ensure that the established procedures have been properly carried out. This necessitates specification of the method for measuring each parameter, determination of satisfactory limits for each test, determination of the frequency with which tests and checks should be employed, and recording of the results of these tests. If a defect is observed, remedial action should be taken and documented.

The U.S. Food and Drug Administration requires that operators of retorts, aseptic processing and packaging systems, product-formulating systems, and container closure inspectors be under the supervision of a person who has satisfactorily completed prescribed courses approved by the FDA Commissioner. At the same time, FDA inspectors are trained in the elements of the HACCP system as it relates to low-acid canned foods. The net result is a cost-effective approach to the control of safety and stability based upon both industry and regulatory knowledge of effective control of critical control points.

It is the opinion of this subcommittee that the HACCP system as applied to low-acid canned foods should serve as a model for the rest of the food industry. The identification of critical control points and the establishment of effective monitoring systems for these foods evolved as a result of joint government/industry efforts. Were the same approach to be taken in other phases of the food industry, similar cost-effective solutions to the problems of food safety and stability might be achieved. Training of inspectors in the HACCP approach should likewise be extended to other types of food-processing operations.

Where Criteria Should Be Applied

Microbiological criteria to determine the adequacy of raw materials can and are in most cases incorporated as a part of purchase specifications. The application of National Food Processors Association (formerly the National Canners Association) criteria to such commodities as sugar and starch has a well-established and effective history in the food industry.

Microbiological criteria are also useful for monitoring critical control points such as cooling water and equipment surfaces.

References

• APHA (American Public Health Association) 1976. Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• 1984. Compendium of Methods for the Microbiological Examination of Foods. 2^nd Ed., M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• Esty, J. R., and K. F. Meyer 1922. The heat resistance of spores of B. botulinus and allied anaerobes. XI. J. Infect. Dis. 31:650–663.
• FDA (Food and Drug Administration) 1973. a. Thermally processed low-acid foods packaged in hermetically sealed containers. Part 128B (recodified as Part 113). Federal Register 38(16):2398–2410, Jan. 14.
• 1973. b. Emergency permit control. Part 90 (recodified as Part 109), Federal Register 38(92):12726–12721. May 14.
• 1983. Thermally processed low-acid foods packaged in hermetically sealed containers. General provisions. Definitions. Code of Federal Regulations 21 CFR 113.3.
• FPI (Food Processors Institute) 1975. Canned Foods—Principles of thermal process control in container closure evaluation, 2^nd Ed. National Canners Association, eds. Berkeley, Calif.: FPI.
• ICSMF (International Commission on Microbiological Specifications for Foods) 1980. Microbial Ecology of Foods. Vol. 1. Factors affecting life and death of organisms. New York: Academic Press.
• Ito, K. 1974. Microbiological critical control points in canned foods. Food Technol. 28(9):46–48.
• NFPA-CMI (National Food Processors Association—Can Manufacturers Institute, Container Integrity Task-force).
• 1984. Botulism risk from post-processing contamination of commercially canned foods in metal containers. J. Food Prot. 47(10):801–816. [PubMed: 30934512]
• Townsend, C. T., J. R. Esty, and F. C. Baselt 1938. Heat-resistant studies on spores of putrefactive anaerobes in relation to determination of safe processes for canned foods. Food Res. 3:323–346.

Sensitivity of Products Relative to Safety and Quality

Quality

Certain acid and acidified canned foods are susceptible to spoilage by flat-sour microorganisms such as Bacillus coagulans. Care must be taken to use ingredients with low initial counts of this organism and to destroy them with thermal treatment or limit their ability to reproduce by choice of a suitably low pH and/or high titratable acidity.

Need for Microbiological Criteria

Acid canned foods are considered less critical than low-acid canned foods with respect to control of manufacture. However, the U.S. Food and Drug Administration in 1979 promulgated Good Manufacturing Practices for Acidified Foods (FDA, 1983b). Many of the controls, records, and procedures listed for low-acid canned foods must also be followed for acidified foods.

The critical issues unique to successful processing of acid and acidified canned foods are: (1) destruction of microorganisms capable of reproduction in the food and (2) provision of a pH/acidity barrier to the growth of those microorganisms that survive. This barrier must control not only the acid-generating flat-sour types that would cause spoilage of economic (but not public health) concern but also acid utilizing microorganisms whose reproduction might result in the elevation of pH to the point where a pathogenic sporeformer such as C. botulinum could grow. Criteria, usually purchase specifications, should be applied to ingredients such as starch and sugar to prevent the use of raw materials that could lead to these types of spoilage.

Where Criteria Should Be Applied

The critical control points in the manufacture of acid and acidified canned foods are much the same as those already outlined for low-acid canned foods. Selection of ingredients of low spore load is important. The thermal process is of great importance to prevent loss of product due to spoilage. Control of pH and the provision of sound containers are critical. The presence and growth of microorganisms that can elevate the pH of the food and permit reproduction of pathogens must be precluded.

References

• FDA (Food and Drug Administration) 1983. a. Acidified foods. General provisions. Definitions. Code of Federal Regulations. Title 21: part 114.3.
• 1983. b. Acidified foods. General provisions. Good manufacturing practices. Code of Federal Regulations 21 CFR 114.5.

Sensitivity of Products Relative to Safety and Quality

Need for Microbiological Criteria and Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

Because reduced water activity is the barrier to growth of those microorganisms surviving the mild thermal treatments given these foods, control of water activity is critical. However, the level of reduced water activity needed for commercial sterility may vary depending on food composition. For example, C. botulinum has not been demonstrated to grow under ideal conditions in laboratory media below a water activity of 0.93, the exact level for inhibition depending upon the humectant used to control available water. Therefore, it is reasonable to expect that complex foods of varying ingredient mixtures combined with sublethal heat treatments will prevent the growth of C. botulinum at water activities somewhat higher than 0.93. There is a need to destroy vegetative forms, particularly Staphylococcus aureus, yeasts, and molds in all thermally processed, water activity-controlled canned foods.

Where Criteria Should Be Applied

Careful control of finished product water activity is essential for the low-acid foods that do not receive the botulinum process. This control must include a thorough procedure to monitor and standardize the accuracy and precision of the instrument used to measure water activity. Checks on each batch of product prepared are indicated. Microbiological criteria are not applicable.

References

• FDA (Food and Drug Administration) 1983. Thermally processed low-acid foods packaged in hermetically sealed containers. General provisions. Definitions. Code of Federal Regulations CFR 21 113.3.

Sensitivity of Products Relative to Safety and Quality

Need for Microbiological Criteria

Cereal grains and their milled products have seldom been implicated as vehicles of foodborne disease and thus there does not appear to be a need for bacterial standards. On the other hand, because these foods are susceptible to mold growth, regulatory action levels for aflatoxins exist and are appropriate. Similar criteria for other mycotoxins may also be necessary if future studies show that there is a health hazard. Soy products that do not receive a heat treatment should be free of salmonellae and Yersinia.

Because grains, flour, grits, and related items are essentially raw agricultural products, and there is little opportunity for microbial growth during their processing, the microbiology of these foods usually does not correlate well with manufacturing practices. Guidelines for these foods, therefore, have little application.

Specifications may be useful when flour or some other grain product is used as a food ingredient, e.g., limits on thermophilic spores. Ready-to-eat cereal products, such as bakery items, should be free of enteric pathogens and toxins. The application of the HACCP concept is the best means for assuring that these foods will not be vehicles for foodborne illnesses.

Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

Information that can be utilized for the development of microbiological criteria is available in the literature (APHA, 1976; ICMSF, 1978, 1980; Rayman et al., 1981). It is advisable for manufacturers to develop additional data through appropriate microbiological surveillance studies.

Where Criteria Should Be Applied

Criteria for mycotoxins should be applied to grain shipments as received at the mill. Microbiological specifications and guidelines for milled products, and especially for foods that contain them, might best be applied at the factory processing level as a component of an ongoing HACCP program. These criteria should be used for monitoring in-process critical control points as well as finished products for safety, wholesomeness, and stability.

References

• APHA (American Public Health Association) 1976. Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• Aulisio, C.C.G., J. T. Stanfield, S. D. Weagant, and W. E. Hill 1983. Yersiniosis associated with tofu consumption; serological, biochemical and pathogenicity studies of Yersinia enterocolitica isolates. J. Food Prot. 46:226–230, 234. [PubMed: 30913675]
• Bryan, F. L. 1976. Public health aspects of cream-filled pastries. A review. J. Milk Food Technol. 39:289–296.
• Bryan, F. L., C. A. Bartleson, and N. Christopherson 1981. Hazard analysis in reference to Bacillus cereus of boiled and fried rice in Cantonesestyle restaurants. J. Food Prot. 44:500–512. [PubMed: 30836565]
• Busby, W. F., and G. N. Wogan 1979. Foodborne Mycotoxins and Alimentary Mycotoxicoses. In Foodborne Infections and Intoxications. 2^nd Ed., H. Riemann, editor; and F. L. Bryan, editor. , eds. New York: Academic Press.
• CDC (Centers for Disease Control) 1981. a. Foodborne Disease Outbreaks. Annual Summary 1978. Atlanta: Centers for Disease Control.
• 1981. b. Foodborne Disease Outbreaks. Annual Summary 1979. Atlanta: Centers for Disease Control.
• Denny, C. B., P. L. Tan, and C. W. Bohrer 1966. Heat inactivation of staphylococcal enterotoxin A. J. Food Sci. 31:762–767.
• Elliott, R. P. 1967. Bacteriological Problems in the Manufacture of Oilseed Proteins. A presentation at the Conference on Engineering of Unconventional Protein Production. Santa Barbara, Calif.: American Institute of Chemical Engineers.
• FDA (Food and Drug Administration) 1982. Macaroni and Noodle Products. Code of Federal Regulations 21 CFR 139.
• Hesseltine, C. W., R. F. Rogers, and R. J. Bothast 1978. Microbiological study of exported soybeans. Cereal Chem. 55(3):332–340.
• Hsieh, F., K. Acott, and T. P. Labuza 1976. Death kinetics of pathogens in a pasta product. J. Food Sci. 41:516–519.
• ICMSF (International Commission on Microbiological Specifications for Foods) 1978. Microorganisms in Foods. 1. Their significance and methods of enumeration. Toronto: University of Toronto Press.
• 1980. Microbial Ecology of Foods. Vol. 2: Food Commodities. New York: Academic Press.
• Lee, W. H., C. L. Staples, and J. C. Olson, Jr. 1975. Staphylococcus aureus growth and survival in macaroni dough and the persistence of enterotoxins in the dried products. J. Food Sci. 40:119–120.
• Pylor, E. J. 1973. Baking Science and Technology. 2^nd Ed., Vol. 1. Chicago: Seibel Publishing.
• Rayman, M. K., K. F. Weiss, G. W. Riedel, S. Charbonneau, and G. A. Jarvis 1981. Microbiological quality of pasta products sold in Canada. J. Food Prot. 44:746–749. [PubMed: 30856753]
• Rogers, L. A., W. M. Clark, and A. C. Evans 1915. The characteristics of bacteria of the colon type occurring on grains. J. Infect. Dis. 17:137–159.
• Swain, E. W., H. L. Wang, and C. W. Hesseltine 1981. Heat-Resistant Aerobic Bacterial Spores in Soybeans. Peoria, Ill.: Northern Regional Research Center, ARS, USDA.
• Swartzentruber, A., W. L. Payne, B. A. Wentz, R. J. Barnard, and R. B. Read, Jr. 1982. Microbiological quality of macaroni and noodle products obtained at retail markets. Appl. Environ. Microbiol. 44:540–543. [PMC free article: PMC242054] [PubMed: 7137999]
• Trenholm, H. L., W. P. Cochrane, H. Cohen, J. I. Elliot, E. R. Farnworth, D. W. Friend, R.M.G. Hamilton, G. A. Neish, and J. F. Standish 1981. Survey of vomitoxin contamination of the 1980 white winter wheat crop in Ontario, Canada. J. Amer. Oil Chem. Soc. 58(12):992A–994A.
• Walsh, D. E., and B. R. Funke 1975. The influence of spaghetti extruding, drying and storage on survival of Staphylococcus aureus. J. Food Sci. 40:714–716.
• Walsh, D. E., B. R. Funke, and K. R. Graalum 1974. Influence of spaghetti extruding conditions, drying and storage on the survival of Salmonella typhimurium. J. Food Sci. 39:1105–1106.

Sensitivity of Products Relative to Safety and Quality

Fats and oils per se do not support growth of microorganisms. However, when in the presence of moisture and other essential nutrients, these products are subject to degradation by a variety of microorganisms. Such a condition is provided by several processed foods in which fats and oils are the major ingredients. Among such products, mayonnaise, salad dressings, peanut butter, margarine, and butter are of concern. Peanut butter differs from mayonnaise, salad dressing, margarine, and butter in that the water content (a_w) is too low to permit microbial growth and spoilage. If moisture is permitted to deposit on the surface of peanut butter, mold growth might, however, be possible. Each of these products is an emulsion. Butter, margarine, and peanut butter represent foods that are emulsions comprised of oil (or fat) as the continuous phase and water as the discontinuous phase. Mayonnaise, salad dressing, and related products are emulsions in which water is the continuous phase and fat the discontinuous phase.

The form of emulsion has a profound relationship to microbial stability. With oil-in-water emulsions such as mayonnaise the growth rate of microorganisms is not affected by the water dispersion; only the chemical composition of the water phase plays a role. On the other hand, with water-in-oil emulsions such as butter the water exists as microscopic droplets that are dispersed throughout the oil matrix. If microorganisms are present in these droplets, their growth is restricted by limited water and food supply as well as by inhibitory factors in the aqueous phase, such as salt, preservatives, and organic acids (ICMSF, 1980).

Need for Microbiological Criteria

Where Criteria Should Be Applied

Microbiological guidelines are most usefully applied at the processing plant level at the critical control points for each of the products as identified earlier in this section.

References

• CDC (Center for Disease Control) 1970. Staphylococcal food poisoning traced to butter—Alabama. Morb. Mort. Weekly Rpt. 19:271.
• 1977. Presumed staphylococcal food poisoning associated with whipped butter. Morb. Mort. Weekly Rpt. 26:268.
• Davies, R. F., and A. H. Wahba 1976. Salmonella infections of charter flight passengers. Report on a visit to Spain (Canary Islands) February 26^th–March 2, 1976. Copenhagen: World Health Organization, Regional Office, Europe.
• FDA (Food and Drug Administration) 1978. a. Mayonnaise. Code of Federal Regulations 21 CFR 169.140.
• 1978. b. Salad Dressings. Code of Federal Regulations 21 CFR 169.150. Washington, D.C.: U.S. Government Printing Office.
• 1978. c. Peanut Butter. Code of Federal Regulations 21 CFR 164.150. Washington, D.C.: U.S. Government Printing Office.
• 1978. d. Margarine. Code of Federal Regulations 21 CFR 166.110. Washington, D.C.: U.S. Government Printing Office.
• ICMSF (International Commission on Microbiological Specifications for Foods). 1980. Microbial Ecology of Foods. Vol. 2. Food Commodities. New York: Academic Press.
• Kurtzman, C. P., and R. B. Smittle 1984. Salad dressings. In Compendium of Methods for the Microbiological Examination of Foods. 2^nd Ed. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• Minor, T. E., and E. H. Marth 1972. Staphylococcus aureus and enterotoxin A in cream and butter. J. Dairy Sci. 55:1410–1414. [PubMed: 4627806]
• Smittle, R. B. 1977. Microbiology of mayonnaise and salad dressing: A review. J. Food Prot. 40:415–422. [PubMed: 30731604]

Sensitivity of Products Relative to Safety and Quality

These products have been involved only infrequently in foodborne disease outbreaks (ICMSF, 1980). Although the risks are low, the potential of such products to lead to major outbreaks cannot be ignored. Witness to this was the 1973–1974 outbreak of salmonellosis involving chocolate candy (D'Aoust, 1977).

Microbial spoilage of these commodities is rare due to low water activities, although specific problems involving yeasts, molds, and sporeformers have been documented (ICMSF, 1980). The HACCP system should be applied in the production of cocoa, chocolate products, and confections. Critical control points should be monitored microbiologically when indicated.

Needs for Microbiological Criteria and Where Criteria Should Be Applied

References

• Anonymous 1971. Beverage Production and Plant Operation. Washington, D.C.: National Soft Drink Association.
• Barrile, J. C., K. Ostovar, and P. G. Keeney 1971. Microflora of cocoa beans before and after roasting at 150°C. J. Milk Food Technol. 34: 369–371.
• Collins-Thompson, D. L., K. F. Weiss, G. W. Riedel, and S. Charbonneau 1978. Sampling plans and guidelines for domestic and imported cocoa from a Canadian national microbiological survey. Can. Inst. Food Sci. Technol. J. 11: 177–179.
• Collins-Thompson, D. L., K. F. Weiss, G. W. Riedel, and C. B. Cushing 1981. Survey of and microbiological guidelines for chocolate and chocolate products in Canada. Can. Inst. Food Sci. Technol. J. 14: 203–208.
• Craven, P. C., D. C. Mackel, W. B. Baine, W. H. Barker, E. J. Gangarosa, M. Goldfield, H. Rosenfeld, R. Altman, G. Lachapelle, J. W. Davies, and R. C. Swanson 1975. International outbreak of Salmonella eastbourne infection traced to contaminated chocolate. Lancet 1: 788–793. [PubMed: 48010]
• D'Aoust, J. Y. 1977. Salmonella and the chocolate industry. A review. J. Food Prot. 40: 718–727. [PubMed: 30736240]
• D'Aoust, J. Y., B. J. Aris, P. Thisdele, A. Durante, N. Brisson, D. Dragon, G. Lachapelle, M. Johnston, and R. Laidley 1975. Salmonella eastbourne outbreak associated with chocolate. Can. Inst. Food Sci. Technol. J. 8:181–184.
• Gabis, D. A., B. E. Langlois, and A. W. Rudnick 1970. Microbiological examination of cocoa powder. Appl. Microbiol. 20: 644–645. [PMC free article: PMC377010] [PubMed: 4925246]
• ICMSF (International Commission on Microbiological Specifications for Foods) 1980. Sugar, cocoa, chocolate, and confectioneries. Pp. 778–821 in Microbial Ecology of Foods. Vol. 2. Food Commodities. New York: Academic Press.
• National Soft Drink Association 1975. Quality Specifications and Test Procedures for Bottlers: Granulated and Liquid Sugar. Washington, D.C.: National Soft Drink Association.
• NCA (National Canners Association) 1972. Bacterial Standards for Sugar. June 1972. Revised. Washington, D.C.: NCA.
• NRC (National Research Council) 1969. An Evaluation of the Salmonella Problem. Committee on Salmonella. Publication 1683. Washington, D.C.: National Academy of Sciences.

Sensitivity of Products Relative to Safety and Quality

As raw agricultural commodities, uncleaned and untreated spices commonly contain high microbial populations (APHA, 1976; ICMSF, 1980; Julseth and Deibel, 1974; Schwab et al., 1982). Spice-bearing plants are exposed to a wide variety of microorganisms from the environment in which they are grown and harvested. Furthermore, during drying, often a simple procedure utilizing the sun, significant microbial growth may occur. Numerous species of bacteria, yeasts, and molds constitute the normal microflora of dried spices (Christensen et al., 1967; Julseth and Deibel, 1974; Schwab et al., 1982), although aerobic sporeforming bacteria usually predominate (APHA, 1976; ICMSF, 1980). While bacteria generally are not responsible for the spoilage of spices, growth of fungi during storage and shipping may result in the development of off-flavors and in the production of undesirable enzymes (ICMSF, 1980).

Spices can be a source of spoilage microorganisms when they are used as seasonings for processed foods. For example, they may introduce heat-resistant spores into canned foods and a variety of spoilage bacteria into refrigerated products such as processed meats (ICMSF, 1980).

Bacteria of public health significance, e.g., Clostridium perfringens (Krishnaswamy et al., 1971; Leitao et al., 1975; Powers et al., 1975), Bacillus cereus (Kim and Goepfert, 1971; Powers et al., 1976), Escherichia coli (Kadis et al., 1971), Staphylococcus aureus (Julseth and Deibel, 1974; Schwab et al., 1982) and Salmonella (ICMSF, 1980; Laidley et al., 1974; Health and Welfare Canada, 1983) may be present but usually in low numbers. Mycotoxin-generating molds also have been isolated from spices (Christensen et al., 1967) and low levels of aflatoxin, usually under 10 µg/kg, have been detected (Scott and Kennedy, 1975).

Although contaminated spices have not been major causes of foodborne disease, a potential hazard exists, especially if the spice is to be used as a table condiment. Contaminated pepper, for example, was responsible for at least 126 cases of salmonellosis (CDC, 1982).

Need for Microbiological Criteria

The end use for a spice will determine the type of criterion that might be needed. Table spices and those used as ingredients of processed foods that do not receive a subsequent lethal treatment should be free of infectious pathogens such as Salmonella; therefore they should be tested for this pathogen.

Guidelines may be useful for monitoring processes applied to spices, in particular the treatment used to destroy much of the intrinsic microflora. Exposure to ethylene oxide gas is the common process, although there is concern at present about some of the products that are formed. The Environmental Protection Agency has set residue tolerances of 50 ppm ethylene oxide in treated spices (EPA, 1982). Treatment of spices with ionizing irradiations, a maximum of 1 megarad, has recently been approved (FDA, 1983).

References

• APHA (American Public Health Association) 1976. Compendium of Methods for the Microbiological Examination of Foods. M. L. Speck, editor. , ed. Washington, D.C.: APHA.
• CDC (Centers for Disease Control) 1982. Outbreak of Salmonella oranienburg-Norway. Morb. Mort. Weekly Rpt. 31(48):655–656. [PubMed: 6819442]
• Christensen, C. M., H. A. Fanse, G. H. Nelson, F. Bates, and C. J. Mirocha 1967. Microflora of black and red pepper. Appl. Microbiol. 15:622–626. [PMC free article: PMC546988] [PubMed: 6035055]
• EPA (U.S. Environmental Protection Agency) 1982. Ethylene oxide; tolerances for residues. Code of Federal Regulations 40 CFR 180.151.
• FDA (Food and Drug Administration) 1983. Irradiation in the production, processing and handling of food. Final rule. Federal Register (48) 129:30613–30614. July 5.
• Health and Welfare Canada 1983. Salmonella in spices and chocolate. Canada Diseases Weekly Report 9(9):35–36.
• ICMSF (International Commission on Microbiological Specifications for Foods) 1980. Microbial Ecology of Foods. Vol. 2. Food Commodities. New York: Academic Press.
• Julseth, R. M., and R. H. Deibel 1974. Microbial profile of selected spices and herbs at import. J. Milk Food Technol. 37:414–419.
• Kadis, V. M., D. A. Hill, and K. S. Pennifold 1971. Bacterial content of gravy bases and gravies obtained in restaurants. Can. Inst. Food Technol. J. 4:130–132.
• Kim, H. U., and J. M. Goepfert 1971. Occurrence of Bacillus cereus in selected dry food products. J. Milk Food Technol. 34:12–15.
• Krishnaswamy, M. A., J. D. Patel, and N. Parthasarathy 1971. Enumeration of microorganism in spices and spice mixtures. J. Food Sci. Technol. 8:191–194.
• Laidley, R., S. Handzel, D. Severs, and R. Butler 1974. Salmonella weltevreden outbreaks associated with contaminated pepper. Epidemiol. Bull. 18:62. Ottawa: Dept. Natl. Health Welfare.
• Leitao, M. F., I. Delazari, and H. Mazzoni 1975. Microbiology of dehydrated foods (Coletanea Inst. Technol. Aliment. 5:223–241). Tech. Abstr. from Food Science 7, 9 B72.
• Powers, E. M., R. Lawyer, and Y. Masuoka 1975. Microbiology of processed spices. J. Milk Food Technol. 38:683–687.
• Powers, E. M., T. G. Latt, and T. Brown 1976. Incidence and levels of Bacillus cereus in processed spices. J. Milk Food Technol. 39:668–670.
• Schwab, A. H., A. D. Harpestad, A. Swartzentruber, J. M. Lanier, B. A. Wentz, A. P. Duran, R. J. Barnard, and R. B. Read, Jr. 1982. Microbiological quality of some spices and herbs in retail markets. Appl. Environ. Microbiol. 44:627–630. [PMC free article: PMC242068] [PubMed: 7138003]
• Scott, P. M., and B.P.C. Kennedy 1975. The analysis of spices and herbs for aflatoxins. Can. Inst. Food Sci. Technol. J. 8:124–125.

Sensitivity of Products Relative to Safety and Quality

Baker's yeast is grown in open fermentors and thus during propagation may be contaminated with low numbers of lactic acid bacteria and sometimes with coliforms including Escherichia coli (Reed and Peppler, 1973). Following the fermentation, the cells are centrifuged and washed several times and then concentrated to about 30% solids using presses or filters. The yeast may then be packed and marketed as compressed yeast cake or it may be dried at a low temperature to produce active dry yeast. A third product is nutritional yeast, which consists of cells killed by drying at high temperatures on drum dryers.

Both live yeast and nutritional yeast have on occasion been contaminated with salmonellae (NRC, 1975). They may not be present in the fermentors but can be introduced at subsequent processing steps. The dead yeast cells that collect on equipment surfaces constitute an excellent growth medium for bacteria and thus soiled equipment may be a significant source of contamination (Reed and Peppler, 1973). Since nutritional yeast is heated to a high temperature during drum drying, the presence of viable salmonellae represents contamination following this treatment.

The spores of certain bacilli are another concern because their introduction into dough may result in ropy bread.

Need for Microbiological Criteria

Many yeast companies have established internal guidelines for levels of bacteria, wild yeasts, and molds. These guidelines aid in assessing conditions of sanitation in the fermentors and during subsequent processing.

The testing of yeast products for Salmonella is appropriate, and specific methods have been developed (FDA, 1978). The presence of the pathogen in nutritional yeast is of special concern since this food may not be heated prior to consumption. Baking, on the other hand, would destroy the salmonellae introduced with the active dry or compressed yeast.

References

• FDA (Food and Drug Administration) 1978. FDA Bacteriological Analytical Manual. Washington, D.C.: Association of Official Analytical Chemists.
• NRC (National Research Council) 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.
• Reed, G., and H. J. Peppler 1973. Yeast Technology. Westport, Conn.: AVI Publishing.

Sensitivity of Products Relative to Safety and Quality

Formulated foods have been described as commercially prepared, ready-to-cook or ready-to-eat foods containing major ingredients from two or more commodity categories (ICMSF, 1985). The potential hazards of the major ingredients of these foods are discussed in other sections of this chapter. The combining of these ingredients into a single product presents not only the original hazards of each ingredient, but also the possibility of magnified or additional hazards due to further handling, process innovations, or modification of the environment. For example, the chicken, gravy, vegetables, and spices in a chicken potpie carry their own hazards and also carry additional potential hazards due to increased handling, possible temperature abuse during the time spent in such handling, and the possibility that a microbiological situation of no concern in the original ingredients is of concern in the formulated food. Beef and chicken potpies have been the cause of botulism as a result of gross abuse by the consumer when heated pies were held at room or slightly higher temperatures for extensive periods of time (CDC, 1960; State of California, 1975, 1976).

Formulated foods have increased in number, diversity, and volume to meet the public's desire for more convenience. Today less food is being prepared from the basic ingredients in the home kitchen where it is likely to be consumed soon thereafter and where any outbreaks are likely to be limited to a small number of consumers. In contrast, increased amounts of food are now produced in factories and held for some time in distribution channels before they are eaten. Under these conditions there is increased potential for abuse and any foodborne illnesses will most likely affect a much larger number of consumers.

The responsibility for preserving safety and keeping quality of foods lies with the processor or formulator of the food. As a result of the increased number and volume of formulated foods, this responsibility has shifted somewhat from the individual in the home to the commercial processor. Because of large differences in composition, preparation, and storage of the many formulated foods, each formulated food or group of foods presents particular circumstances relative to assessment of needs for microbiological criteria (see Chapter 2). Criteria for some formulated foods have been discussed by the ICMSF (1984). However, no general all-product criteria can be developed. Instead, the potential hazards of each product or group of products must be identified and appropriately monitored if microbial growth and resulting health hazard or spoilage are to be prevented during the time the product is under producer control or in appropriate storage. The HACCP systems may include control points in addition to those developed for the separate ingredients. (See for example the discussion of critical control points for frozen foods by Peterson and Gunnerson, 1974.)

Means of preventing growth during storage depend on the conditions of processing, the temperature of storage, and the composition of the product. For example, some formulated foods, e.g. beef stew, liquid infant formula, chili, and tamales, are sterilized in a sealed container. These products are shelf-stable and need no more microbiological criteria than do other low-acid canned foods (see part J).

Other formulated foods are simple blends of dry ingredients, e.g., dried infant formula, soup mix, or cake mix. These foods also are shelf-stable, but they can be hazardous if an ingredient is contaminated with a pathogenic organism such as Salmonella. Both the FDA and the international Codex Alimentarius Commission recognize the need for the imposition of stringent standards on formulated foods designed for use by high-risk populations. The FDA is the more stringent of the two in the application of microbiological criteria to this broad group of products.

The FDA prescribed (FDA, 1978) analytical procedures for ingredients such as dried yeast, cheese, and pasta frequently used in blended formulated foods. While proper use of such formulated foods or their ingredients would destroy salmonellae, regulatory concern with respect to cross-contamination or inadequate heat treatment exists. Numerous recalls of dried blended soups and other foods have occurred and standards or implied standards for salmonellae have been imposed.

The Codex Alimentarius Committee on Food Hygiene concluded that microbiological criteria are not justified in the case of dried soup mixes. However, the committee has established microbiological end product specifications for some products that do require special attention either because they contain pathogenic organisms that may survive cooking procedures or because they are typically eaten by highly susceptible persons such as the very young, the aged, or those who are ill (Codex Alimentarius Commission, 1979a). These products include coated or filled dried shelf-stable biscuits for which criteria for coliforms and Salmonella were imposed, and also dried and instant products requiring reconstitution and dried products requiring heating to boiling before consumption for which criteria for APC, coliforms, and Salmonella were established.

A few formulated foods can be stored at room temperature because of their high acidity, e.g., mustard dressings, or their low water activity, e.g., certain pastries with butter cream fillings (see part M.).

Most formulated foods are preserved by storage at low temperatures. Some are simply refrigerated, e.g., meat and seafood salads and sandwiches, but the majority are frozen, e.g., dishes such as meat potpies, egg rolls, pizza, and enchiladas. Microbiological hazards are diminished if the products are thoroughly heated before consumption.

Need for Microbiological Criteria

Owing to the wide diversity of composition, preparation, and storage conditions, it is not possible to develop a single set of microbiological criteria that are suitable for all formulated foods. However, criteria have been established and are appropriate for certain classes of formulated foods as discussed above. Establishment of criteria should be preceded by consideration of the product as outlined in the foregoing section so as to decide what, if any, microbiological criteria would offer protection against health hazards and poor quality.

Assessment of Information Necessary for Establishment of a Criterion if One Seems To Be Indicated

Factors that determine the potential usefulness of microbiological criteria with formulated foods include:

1.

The nature and extent of contamination: Ingredients that are traditionally associated with salmonellae, for example, should be subjected to routine testing for these organisms, especially if the product is likely to be consumed without thorough cooking.

2.

Likelihood of contamination during preparation: Any product that is subjected to handling can be expected to contain a few coagulase-positive staphylococci; excessive numbers suggest breaches of good manufacturing practice.

3.

Bactericidal treatment(s) during processing: Commercial pasteurization or sterilization will eliminate all pathogenic organisms from a food. Hence, the application of microbiological criteria to products that have undergone a terminal heat treatment usually is not cost-effective. Efficacy of heating can better be monitored by measuring temperature or enzyme destruction or by other appropriate means. Microbiological criteria may be appropriate, however, if there is opportunity for recontamination with pathogens after heating.

4.

Likelihood of growth during storage: Under proper conditions of storage, microorganisms do not grow in a canned (heat sterilized), frozen, or dried product. In fact, bacteria gradually die off during frozen or dry storage. Abuses such as thawing and holding prior to refreezing or inadvertent moistening of a dry product may allow microbial growth. The occurrence of such abuse is sporadic and may occur in any of a number of places in the distribution system. Therefore, routine application of microbiological criteria is not an effective way to detect specific abuse situations. In the production of refrigerated formulated foods, microbiological guidelines can be usefully applied by the processor to assess potential shelf-life. However, the application of such criteria after the product has left the processing facility is not recommended.

5.

Susceptibility consumer: The very young, the aged, and the infirm are known to be more susceptible to infection by salmonellae and other pathogens than are healthy adults. Therefore, special care must be taken with foods intended for infants, hospital patients, residents of nursing homes, and other highly susceptible groups of people at elevated risk.

Microbiological criteria often are appropriate for these foods. (For further discussion, see Chapter 3 and Codex Alimentarius Commission, 1979b.)

References

• CDC (Centers for Disease Control) 1960. Botulism Morb. Mort. Weekly Rpt. 9:2.
• 1981. Foodborne Disease Outbreaks. Annual Summary 1979. Atlanta: Centers for Disease Control.
• Codex Alimentarius Commission 1979. a. Microbiological specifications for foods for infants and children. Alinorm 79/13. Appendix V.
• 1979. b. Code of Hygienic Practices for Infants and Children, Appendix V. Report of the 16^th Session of the Codex Committee on Food Hygiene, Codex Alimentarius Commission. Rome: Food and Agriculture Organization.
• FDA (Food and Drug Administration) 1978. FDA Bacteriological Analytical Manual. Washington, D.C.: Association of Official Analytical Chemists.
• ICMSF (International Commission on Microbiological Specifications for Foods) 1985. Formulated foods. In Microorganisms in Foods. 2. Sampling for microbiological analyses: Principles and specific applications. 2 ^nd Ed. In preparation.
• Peterson, A. C., and R. E. Gunnerson 1974. Microbiological critical control points in frozen foods. Food Technol. 28 (9):37–44.
• State of California (Department of Health Services) 1975. Botulism—home canned figs and chicken pot pie. Calif. Morbidity. No. 51.
• 1976. Type A botulism associated with commercial pot pie. Calif. Morbidity. No. 51.
• Wehr, H. M. 1982. Attitudes and policies of governmental agencies on microbial criteria for foods—an update. Food Technol. 36(9):45–54, 92.

Sensitivity of Products Relative to Safety and Quality

The meats of tree nuts are usually sterile when in the intact shell. Microbial contamination may occur during their harvest, transport, and processing (Hall, 1971; Hyndman, 1963; King et al., 1970; Kokal and Thorpe, 1969; Meyer and Vaughn, 1969). Microorganisms may be introduced as a result of insect infestation, e.g., immature almonds are attacked by the navel orange worm. The shells of tree nuts may be contaminated with enteric organisms, especially if they come in contact with the ground. Permitting cattle and other animals to graze in nut groves increases the opportunity for contamination by fecal microorganisms; collecting the nuts on clean canvas minimizes this problem. Nuts exposed to water, either for washing or tempering, are prone to contamination, especially if there has been a separation of the sutures. Microorganisms present on the shell may also be introduced onto meats during the cracking operation.

Bacterial growth on nut meats is rarely a problem due to their low a_w. An exception is the coconut, which may develop leaks, become contaminated, and then support growth of various species, including salmonellae, in the coconut milk (Schaffner et al., 1967). When present, salmonellae may survive the drying process given to coconut meat. Elimination of the pathogen depends upon pasteurization in hot water prior to drying.

Peanuts (Arachis hypogaea) are subject to contamination from soil fungi, including species that produce aflatoxins. Mold growth may occur prior to harvest or when the peanuts have been dried insufficiently or stored under humid conditions (Marth and Calanog, 1976). Tree nuts such as pecans, almonds, pistachios, and Brazil nuts also may contain aflatoxins. The molds often are introduced via insect penetration.

Need for Microbiological Criteria

Nut meats are used primarily as ingredients of foods such as bakery products. Because they can be a source of spoilage organisms, purchase specifications for nut meats may contain limits on the microorganisms of concern such as molds.

Epidemiological evidence indicates that nut meats are not a significant vehicle of foodborne disease. However, a microbiological standard does exist in that the Food and Drug Administration has taken the position that the presence of Escherichia coli on nut meats is evidence of filth and thus adulteration; apparently growers and processors usually can produce a product that is free of this organism.

Salmonellae have been a problem in dried coconut; therefore, these products should be tested for this pathogen. The presence of aflatoxins in nut meats is a chronic problem, especially in peanuts and peanut products. Standards that place limits on the permitted concentration of unavoidable toxins should be continued (see Chapter 8 and this chapter, part N).

References

• Hall, H. E. 1971. The significance of Escherichia coli associated with nut meats. Food Technol. 25 (3):230–232.
• Hyndman, J. B. 1963. Comparison of enterococci and coliform microorganisms in commercially produced pecan nut meats. Appl. Microbiol. 11:268–272. [PMC free article: PMC1057987] [PubMed: 13956016]
• King, A. D., Jr., M. J. Miller, and L. C. Eldridge 1970. Almond harvesting, processing, and microbial flora. Appl. Microbiol. 20:208–214. [PMC free article: PMC376902] [PubMed: 4921060]
• Kokal, D., and D. W. Thorpe 1969. Occurrence of Escherichia coli 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, editor; and D. F. Splittstoesser, editor. , eds. Westport, Conn.: AVI Publishing.
• Meyer, M. T., and R. H. Vaughn 1969. Incidence of Escherichia coli in black walnut meats. Appl. Microbiol. 18:925–931. [PMC free article: PMC378115] [PubMed: 4905608]
• Schaffner, C. P., K. Mosbach, V. C. Bibit, and C. H. Watson 1967. Coconut and Salmonella infection. Appl. Microbiol. 15:471–475. [PMC free article: PMC546945] [PubMed: 5340650]

Sensitivity of Products Relative to Safety and Quality

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 committee of FAO/WHO who examined the subject a number of years ago (de Becze, 1970).

References

• Cottrell, I. W., and J. K. Baird 1980. Gums. Pp. 45–66 in Vol. 12 of Kirk-Othmer Encyclopedia of Chemical Technology, 3^rd 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. [PubMed: 6020738]
• Pariza, M. W., and E. M. Foster 1983. Determining the safety of enzymes used in food processing. J. Food Prot. 46:453–468. [PubMed: 30913657]
• 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. [PubMed: 817530]
• 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, 3^rd Ed. New York: John Wiley and Sons.

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), Parvovirus-like agent (3), hepatitis A (2), Vibrio cholerae O1 (1), and Rotavirus (1). 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 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):

1.

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 Pharmacopeia 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 processed, 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 the gastric juice and reach the duodenum virtually unchanged (Levine and Nalin, 1976; Mossel and Oei, 1975). 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 microbiological 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 aeruginosa.

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, 1983). Over 99.8% of these samples were free of coliforms.

Although there is no epidemiological evidence that bottled water processed 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., 1977).

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 MPN 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 analysis 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 production, processing, and distribution of bottled drinking water (Wehr, 1982). To promote high standards of quality in the bottled water industry, the International Bottled Water Association has published a technical manual containing a quality control program to assure compliance with FDA standards (IBWA, 1983). 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, Cytophaga, Flavobacterium, and Alcaligenes. Although no total count is specified, good-quality drinking water at time of bottling usually contains 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 coli, fecal coliforms, coliforms, sulfite-reducing Clostridium, P. aeruginosa, Vibrio, and E. coli 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, 1977).

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 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 supplies and the variety of sources from which water for bottling is obtained has proliferated. These recent increases suggest that a periodic reassessment should be made of practices in this industry relative to the microbiological 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., 1981).

Where Criteria Should Be Applied

Microbiological examination of bottled drinking water for compliance with standards or guidelines should be carried 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. 2^nd Ed., M. L. Speck, editor. , 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. Epidemiol. 105:344–348. [PubMed: 848484]
• CDC (Centers for Disease Control) 1979. Foodborne and Waterborne Disease Outbreaks. Annual summary 1977. Atlanta: Center 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.
• 1982. a. Water-related Disease Outbreaks. Annual Summary 1980. Atlanta: Centers for Disease Control.
• 1982. b. 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) 1982. a. 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.)
• 1982. b. Processing and bottling of bottled drinking water. Code of Federal Regulations 21 CFR 129.
• FPI (The Food Processors Institute) 1982. Canned Foods, Principles of Thermoprocess Control, Acidification and Container Closure Evaluation, 4^th 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 gastroenteritis due to Salmonella java traced to smoked whitefish. Am. J. Pub. Health 58:114–121. [PMC free article: PMC1228047] [PubMed: 5688737]
• 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, 15^th Ed. Washington, D.C.: American Public Health Association.
• Howie, J. W. 1968. Typhoid in Aberdeen, 1964. J. Appl. Bacteriol. 31:171–178. [PubMed: 5726554]
• 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. [PubMed: 63781]
• Mossel, D. A. A., and H. Y. Oei 1975. Person-to-person transmission of enteric bacterial infection. Lancet 1:751. [PubMed: 47517]
• Nolan, C., N. Harris, J. Ballard, J. Allard, and J. Kobayashi 1982. Outbreak of Yersinia enterocolitica—Washington State. Morb. Mort. Weekly Rpt. 31:562–564. [PubMed: 6817060]
• 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: American 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, Technical Bulletin, Winter. Alexandria, Va.: IBWA.
• USP (United States Pharmacopeia) 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.

Sensitivity of Products Relative to Safety and Quality

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 Committee on Salmonella (NRC, 1969):

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 (a_w 0.80–0.90), or dried products. 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 recontamination following heating, then, is the critical control step in their processing. 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, 1980). Specifications and guidelines for these products are especially useful if applied 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 manufacturing;

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., 1977). 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 microorganisms.

References

• D'Aoust, J. Y. 1978. Salmonella in commercial pet foods. Can. Vet. J. 19:99–100. [PMC free article: PMC1789378] [PubMed: 657079]
• 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. Washington, D.C.: U.S. Department of Agriculture.
• Morse, E. V., and M. A. Duncan 1974. Salmonellosis—An environmental health problem. J. Am. Vet. Med. Assoc. 165:1015–1019. [PubMed: 4613725]
• 1975. Canine salmonellosis: Prevalence, epizootiology, signs, and public health significance. J. Am. Vet. Med. Assoc. 167:817–820. [PubMed: 1102502]
• 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. [PMC free article: PMC1653365] [PubMed: 1108681]
• 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. [PubMed: 30731632]
• 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.