Introduction
Man’s food supply consists primarily of plants and animals and products derived from them. Microorganisms are naturally present in the soil, water, and air, and therefore exterior surfaces of plants and animals are contaminated with a variety of microorganisms. There is little specificity to this microflora since it reflects that of the environment in which the plants were grown and the animals were raised. Interior tissues of plants and animals usually contain few, if any, microorganisms. The gastrointestinal tracts of animals, however, contain large numbers of organisms. But if proper slaughtering-dressing procedures are used, contamination of interior muscle tissue can be avoided.
From the time of slaughter, catch, or harvest, the surface and interior tissues of animals and plants are subject to contamination. This is due in part to the breakdown of normal defense mechanisms, particularly in animals. Each processing step subjects the raw material to additional opportunities for contamination. Sources of contamination include surfaces of the harvested plant or slaughtered animal, water, equipment, utensils, workers, and the processing environment.
Microbial Activities in Foods
Historical Aspects
During their existence, human beings have been confronted with the problem of limited shelf-life of animal and plant foods in part due to
microbial activities. During the last 5,000 to 10,000 years a variety of techniques (such as drying, salting, heating, fermentation, refrigeration, or freezing) evolved empirically and contributed to the increased shelf-life of plant and animal foods. These techniques, which controlled microbial activity to a greater or lesser extent, were applied before the mechanism of their effect was understood. In the early 1800s Francois Nicholas Appert was awarded a patent for a practical method of food preservation, namely, “canning.” Since that time, and particularly during the last 40 years, new processes have been developed to extend shelf-life of foods. Although some others may have suggested microbial involvement in food spoilage at earlier dates, it was Louis Pasteur who in the mid-1800s first established a scientific basis for the direct relationship between food spoilage and microbial activity. Microorganisms responsible for foodborne diseases were first recognized around 1880. Since that time, the number of microbial agents recognized as involved in foodborne illness has increased steadily.
Spoilage, Pathogenic, and Useful Microorganisms
Microorganisms associated with foods can be categorized as “spoilage,” “pathogenic,” or “useful.” Spoilage microorganisms are those that can grow in a food and cause undesirable changes in flavor, consistency (body and texture), color, or appearance. Also bacterial enzymes may effect slow deterioration of frozen or dried foods during long-time storage. These changes diminish the quality characteristics of foods and may render them ultimately unfit for human consumption. For example, refrigerated perishable foods such as milk, fresh meat, poultry, fish, fruits, and vegetables lose some quality characteristics during normal storage and ultimately spoil, due in part to the activity of microorganisms capable of growth at refrigeration temperatures. Usually, extensive microbial growth (millions of organisms per g or cm2) occurs before quality losses are perceptible. These changes, when perceived by the consumer, serve as an alert that extensive microbial activity has taken place.
Pathogenic microorganisms can render foods harmful to humans in a variety of ways. Foods may serve as the vehicle for the introduction of infectious microorganisms into the gastrointestinal tract, e.g., Salmonella and Shigella. Multiplication of certain microorganisms in foods prior to consumption may result in production of toxins, e.g.,Clostridium botulinum, Staphylococcus aureus, and Bacillus cereus. Foods may also be the vehicle for microorganisms that form toxins in vivo, e.g., Clostridium perfringens and certain pathogenic Escherichia coli.
With some foods, conditions are chosen to favor the development of useful microorganisms such as lactic acid bacteria and yeasts, which are either naturally present or added intentionally. Such foods as cheeses, yogurt, breads, pickles, and fermented sausages offer desirable organoleptic properties and shelf-life.
Food as a Selective Environment
Microbial activities in foods can be viewed from the perspective of the food as a “selective environment,” despite the diversity of microorganisms that contaminate the surfaces of the raw materials. The selectivity is imposed by the physical-chemical characteristics of the food, the additives it contains, the processing techniques, the packaging material, and the storage conditions. It is necessary to distinguish between the shelf-life of two broad categories of foods, namely those that are shelf-stable and those that are perishable. For this discussion, shelf-life will be treated as it relates to microbial activity only.
Microbiological shelf-stability of many foods is related to storage conditions. For example, dried and frozen foods are microbiologically shelf-stable as long as they remain dry or frozen. Shelf-stable foods are not necessarily sterile; indeed, many do contain microorganisms. Some shelf-stable canned foods may undergo microbiological spoilage if they are exposed to elevated temperatures permitting the growth of surviving thermophilic sporeforming bacteria, whereas these organisms are inactive at ambient temperatures and indeed tend to die during normal storage. Shelf-stable food is distinguished from perishable food in that an attribute or attributes of the shelf-stable food prevent(s) the growth of contaminating microorganisms. For example, certain canned products are heat processed to the degree that they are sterile; the attribute assuring stability of such products is elimination of all living forms. With many shelf-stable foods, other attributes prevent microbial growth. Dried beans are shelf-stable because they contain insufficient moisture to permit microbial growth. Mayonnaise is shelf-stable because it contains sufficient quantities of acetic acid in the moisture phase of the product to prevent growth of contaminating organisms. Certain canned cured meats are shelf-stable, not because they are sterile, but because sublethal heat treatment so injures surviving spores that they are incapable of outgrowth in the presence of salt and nitrite. The distinguishing characteristic of shelf-stable foods, then, is their resistance to microbiological spoilage. Microbial growth in such products is an abnormal and unexpected event.
Perishable foods, on the other hand, have a finite shelf-life and if not consumed, will spoil at some time during storage. The exact time of spoilage depends upon a great number of variables. Though various processing procedures, additives, packaging methods, and storage conditions may be applied to increase shelf-life, microorganisms capable of growth survive and ultimately grow. When such growth proceeds to the extent that undesirable changes are perceptible to the processor, preparer, or consumer, the food is deemed of inferior quality or spoiled and is rejected. The distinguishing feature of perishable foods, in contrast to shelf-stable foods, is that microbiological spoilage is an expected event. It will ultimately occur even if the food has been prepared from wholesome raw materials and has been properly processed, packaged, and stored.
Microflora of Processed Foods
Although the microflora of raw materials is usually heterogeneous, processing of foods (except those that are sterile) often imposes a characteristic and highly specific microbiological flora. The normal flora of severely heat processed, but not sterilized, low-acid canned foods is comprised of thermophilic sporeforming bacteria, the most heat-resistant microbial components of the raw materials. The predominating flora of shelf-stable canned cured meats consists of mesophilic aerobic and anaerobic sporeforming bacteria, the predominant organisms resistant to the heat process applied to these products. The normal flora of mayonnaise and salad dressing is comprised of small numbers of sporeforming bacteria, yeasts, and lactic acid bacteria. Aerobic sporeforming bacteria predominate in dry spices and in a number of dry vegetable products. Molds and yeasts predominate in dried fruits. The normal flora in carbonated beverages is comprised of yeasts. In each of the foregoing, the surviving and predominating microflora reflects the nature of the raw materials, processing conditions, packaging, and storage of the shelf-stable product. However, spoilage is still possible. If the severely heat-processed canned foods were exposed to high temperatures during storage, spoilage due to the germination and outgrowth of thermophilic sporeforming bacteria might occur. If shelf-stable canned cured meat were to contain excessive numbers of aerobic sporeforming bacteria, growth of these organisms might result in spoilage, despite an adequate heat process and normal levels of salt and nitrite. Excessive levels of yeasts or lactic acid bacteria might result in their growth and subsequent spoilage of the mayonnaise, despite levels of acetic acid that would assure the stability of a product containing “normal” levels of the same organisms. Time/temperature abuse of an ingredient of a carbonated beverage (for example, a flavor) may lead to the development of large numbers of yeasts that could overcome the effect of carbonic acid, which would normally render the same beverage stable. The normal flora in microbiologically shelf-stable products is, therefore, rather specific. If the stabilizing nature of the system should be overcome, this microflora may multiply and cause spoilage—an unexpected event.
With perishable products, the microflora that survives processing may be heterogeneous, but that portion of it developing during storage and causing spoilage is usually quite specific. For example, a heterogeneous flora exists on raw red meats, poultry, and fish as a result of contamination from the animal and/or the processing environment. Yet, during refrigerated storage of such products, spoilage is caused predominantly by a highly specific group of microorganisms, namely Pseudomonas and closely related aerobic, psychrotrophic gram-negative bacteria. If the same products are vacuum-packed in oxygen-impermeable films, a different microflora becomes predominant, namely, lactic acid bacteria that grow under both aerobic and anaerobic conditions. In both examples, despite the heterogeneous flora of the finished product, a rather restricted group of microorganisms may develop and ultimately cause sensory changes in the product. Similar relationships exist for many other perishable foods.
It follows that since most classes of perishable foods constitute selective environments for rather restricted groups of microorganisms, the spoilage caused by the growth of these microorganisms manifests itself in a characteristic manner, i.e., normal spoilage pattern. For example, when pseudomonads and other closely related gram-negative psychrotrophic aerobic bacteria grow to large numbers on the surface of refrigerated fresh meat, poultry, and fish, sensory changes occur. The first manifestation of spoilage is development of off-odor. As growth proceeds, slime may develop and the off-odor may intensify. The normal spoilage pattern of a perishable food can be a safeguard, since under certain situations it warns the processor, preparer, or consumer that the food is no longer edible.
Changes in processing of perishable foods must take into account the effect these changes may have on the spoilage flora, and thus on the normal spoilage pattern of the food involved. If such changes tend to alter the normal patterns of spoilage the public health aspects must be taken into account. A classic example of this relates to the merchandising of smoked whitefish. For generations this product was merchandised under conditions where the fish was exposed to air. Spoilage was evidenced by the development of bacteria which produced off-odors and slime that were readily recognized by the consumer and caused rejection of the product. Then it was discovered that the shelf-life of smoked fish could be significantly increased if the product was packed in an oxygen-impermeable film. With extended storage of the product under these conditions, C. botulinum type E was able to grow and produce toxin, just as it would have been able to do in the conventionally packaged product. However, under these storage conditions the aerobic bacteria producing off-odor and slime could not develop and the normal spoilage flora was now comprised of lactic acid bacteria that did not produce off-odors. This change in the normal spoilage pattern of the product reduced the probability that the consumer would reject a product that had been held in storage out of refrigeration for an extended period of time. This led to a multistate outbreak of type E botulism (Kautter, 1964). Thus, it is essential that if changes are made in the processing or merchandising of a perishable product, the influence of these changes on the normal spoilage patterns of the product be taken into account.
Control of Microorganisms in Foods
Control must be exercised over three different categories of microorganisms that may be present in foods: (1) those that have the potential for producing foodborne disease, (2) those that cause food spoilage, and (3) those that grow in food and produce desirable changes.
Effective food control programs eliminate the potential for foodborne illness in a variety of ways. Processing techniques that cause destruction of pathogens may be employed, e.g., the pasteurization of milk to destroy Coxiella burnetii and Mycobacterium tuberculosis and less heat resistant pathogens such as the diphtheria bacillus, salmonellae, and pyogenic streptococci, and the 12-D process1 for the destruction of C. botulinum in low-acid canned foods. In other cases, toxigenic and infectious microorganisms are controlled by product formulation (acetic acid in mayonnaise) or storage conditions (the refrigeration of perishable pasteurized canned cured meats to control the growth of C. botulinum). In yet other situations, the ultimate control is exercised by the person who prepares the food (adequate cooking of poultry to eliminate salmonellae and of pork to eliminate trichinellae). Despite such efforts, food control programs have fallen short of their goals for controlling foodborne pathogens (see in particular where foodborne illness of microbiological origin is treated in detail).
Control measures directed toward prevention of spoilage have also fallen short of the ideal. Although precise figures are difficult to obtain, it is estimated that one-fourth of the world’s food supply is lost through microbial activity alone. The control of food spoilage is a prime economic objective of control programs. For products designed to be shelf-stable, control is accomplished through processing and/or formulation procedures that result in the inhibition of spoilage organisms. With perishable foods, the object is to achieve the longest possible shelf-life consistent with product safety. In general, this is attempted by instituting measures that will result in products with low microbial loads, since shelf-life and initial level of contamination are usually directly related in perishable foods. Control of remaining microorganisms is most often achieved by proper refrigerated storage.
The desirable organoleptic properties (taste, odor, body, and texture) of such foods as cheeses, yogurt, cultured buttermilk, sour cream, pickles, and fermented sausages result in part from the activities of a specific microbial flora. Extensive microbiological control procedures are needed to produce “cultured products” of high quality and to ensure that the microbial activities are guided in such a manner that the end products have the desirable sensory properties. For example, in cultured dairy products this is achieved by (1) proper selection and handling of starter cultures, (2) control of the presence of antibiotics and bacteriophages, and (3) checking by chemical and organoleptic means the progress of microbial activity in raw and finished products. These measures can influence both the quality and the safety of the food. For example, the lack of acidity caused by culture failure can allow the development of S. aureus, which could result in cheese containing staphylococcal enterotoxin.
Another objective of food control programs is to keep filth and other foreign substances out of food. In some cases, extraneous matter is of public health concern, e.g., rodent pellets and hairs; in other instances, the foreign material is of aesthetic rather than health significance, e.g., certain cereal insects.
Finally, another objective of food control programs is to ensure that packaging, storage, handling, transportation, display, and sale of foods are all properly carried out. Processors and regulatory officials can exert control over a product while it is packaged, stored, and readied for distribution from the plant of origin. But beyond that point, the intensity of control rapidly diminishes.
The bulk of the problems with foodborne disease and food spoilage results from events that occur after food has left the processing plant—during transport, during retail sales, and ultimately in the food service establishment or home (CDC, 1981). In these locations, control on occasion either does not exist or is executed ineffectively, thus producing the weakest link in the food chain. Many improvements in food control that are made at the processing level will be nullified if handling procedures beyond the plant are not effectively controlled.
Approaches to Microbiological Control in Foods
Traditionally, three principal means have been used by regulatory agencies and food processors to control microorganisms in foods. These are (1) education and training, (2) inspection of facilities and operations, and (3) microbiological testing.
Although food handlers have the potential for contaminating foods with disease-producing microorganisms, i.e., staphylococci, salmonellae, and hepatitus virus, health examination of food handlers is a nonproductive approach to the control of foodborne illness. Specimens from food handlers have traditionally been examined only for a few microorganisms, and such tests do not always detect carriers. Screening tests cannot be made with sufficient frequency to be effective in detecting the carrier status in persons who are continually exposed to the risk of acquiring foodborne pathogens. Negative tests convey to food handlers, managers, and public health personnel the erroneous concept that the workers are free of infections and therefore incapable of transmitting foodborne pathogens to the foods they handle. Although direct transfer of pathogens from food handlers to food is a hazard, far more frequently improper food-handling practices create a hazard that is not circumvented by health examinations.
Education and Training Programs
These programs are directed primarily toward developing an understanding of the causes and consequences of microbial contamination and of measures to prevent contamination and subsequent growth. The extent of training required of personnel within processing plants and food service establishments depends upon the technical complexity of the food operation and the level of responsibility of the individuals being trained. In-depth training may be necessary for supervisory personnel, while for others training may relate only to specific aspects of a food operation. Although education and training are necessary parts of any food control program, standing alone they have certain limitations and shortcomings. Personnel turnover in the food industry is both constant and rapid, and thus education of workers must be a continuing rather than a sporadic exercise. It is essential that supervisory personnel be properly trained with respect to the hazards associated with the operations for which they have responsibility.
Inspection of Facilities and Operations
Inspections of facilities and operations are commonly used to evaluate adherence to good handling practices. The U.S. Department of Agriculture (USDA) relies almost entirely upon this approach in the regulation of meat and poultry operations. Resident inspectors observe all phases of processing from the live animal to the finished product. Little reliance is placed upon microbiological testing in the meat and poultry control programs. In its activities with respect to dried milk and egg processing, the USDA relies not only on inspections but also on microbiological testing of the finished products.
The Food and Drug Administration (FDA) also relies heavily on inspection of facilities and operations. In addition, both in-process and finished product samples are collected and analyzed. Results of such analyses are used to corroborate observations made during inspections; they are not intended to perform the processors’ responsibility of microbiological control on a day-to-day basis. The FDA inspection program is designed to determine whether or not processors are operating in compliance with the Federal Food, Drug and Cosmetic Act. Thus, this activity is in sharp contrast to that of the USDA meat and poultry inspection, wherein resident inspectors are charged to assure that plants are in compliance with the Federal Meat Inspection Act and Poultry Products Inspection Act on a day-to-day basis.
Procedures vary widely at the state, county, and municipal levels, but the approach to regulatory control is primarily through periodic inspection of facilities and operations.
Just as with the education and training approach to food control, inspection of facilities and operations alone is not sufficient. Generally, the inspector relies upon advisory or mandatory documents such as Good Manufacturing Practice (GMP) guidelines and Codes of Hygienic Practice or local food control laws, ordinances, or regulations. Unfortunately, such documents often refer to stated requirements without specifying what is considered to be in compliance with the requirements.2 This lack of specificity, or failure to indicate the relative importance of the requirements, leaves interpretation of compliance solely at the discretion of the inspector. Lack of discrimination between important and relatively unimportant requirements may result in overemphasis upon unnecessary or relatively minor requirements, and thus increase costs without significantly reducing hazards. Requirements that are critical to the safety of the product may be overlooked or underestimated.
Microbiological Testing
Samples of ingredients, materials obtained from selected points during the course of processing or handling, and finished products may be examined microbiologically to determine adherence to Good Manufacturing Practices. In some instances, foods are examined for a specific pathogen or its toxins, but more often examinations are made to detect organisms that are indicative of the possible presence of pathogens or spoilage or to detect presence of the specific spoilage organisms or their products. Microbiological testing is absolutely essential to the control of certain products, e.g., to assure that dried milk and eggs and confectionery products are free of a Salmonella hazard. Testing is essential to assure that critical raw materials are satisfactory for their intended use, e.g., to assure that the sugar used in canning meets established standards and to assure that critical products used in dried blends are free of Salmonella.
Microbiological testing has severe limitations as a control option. The most serious shortcoming is the constraint of time. Most microbiological test results are not available until several days after testing. Therefore, if finished product acceptability must be measured by microbiological testing, the product is held pending results. With perishable foods, this is generally not possible; with shelf-stable foods, the warehousing of finished product increases costs. If in-line samples are collected and analyzed, the results are of retrospective value since the finished product has already been produced. Other difficulties are related to sampling , analytical methods, and the use of indicator organisms for pathogens .
Composite Programs
Sophisticated microbiological control programs encompass the three approaches, namely education and training, inspection of facilities and operations, and microbiological testing. The emphasis varies from plant to plant, product to product, and establishment to establishment, as does the success of the various microbiological control programs.
The Hazard Analysis Critical Control Point (HACCP) System
The HACCP system, first presented at the 1971 National Conference on Food Protection (APHA, 1971), provides a more specific and critical approach to the control of microbiological hazards than that achievable by traditional inspection and quality control procedures. The system consists of: (1) identification and assessment of hazards associated with growing, harvesting, processing-manufacturing, marketing, preparation, and/or use of a given raw material or food product; (2) determination of critical control points to control any identifiable hazard(s); and (3) establishment of procedures to monitor critical control points. Analysis of factors to be considered in hazard analyses, detailed in, leads to establishment of the control points to be monitored. Depending upon the situation, the monitoring may involve inspections, physical or chemical measurements, and/or microbiological testing.
