Adapted from CAST (1994) and Schmidt (1998).

Adapted from CAST (1994) and Schmidt (1998).

frozen and improperly thawed food product may be an even more favorable substrate for microbial growth than the fresh food if the freeze-thaw process has caused sufficient cellular damage for nutrient release.

Relative humidity The relative humidity (RH) of the storage or packaging environment is important for maintaining an optimal «w in the food and controlling the growth of microorganisms on the surface of the food. If a food aw has been set, it is important that the food not pick up moisture from its environment and thereby increase its aw and allow microorganism growth. Foods placed in low-RH environments will lose water and equilibrate with their environment. Conversely, foods with low av, will gain moisture (increase aw) when stored in a high-RH environment.

The relationship between temperature and RH value—in general, the higher the temperature, the lower the RH—should be kept in mind when storing foods. Foods that undergo surface spoilage by molds, yeast, and bacteria should be stored under low-RH conditions. When improperly wrapped, foods such as meats, whole chickens, and fish stored in a refrigerator tend to suffer surface spoilage before deep spoilage occurs because of the high RH of the refrigerator and the fact that surface spoilage bacteria on meats tend to be aerobic. Therefore, in selecting proper storage conditions, consideration must be given to the potential for surface growth as well as to the need to maintain desirable qualities in the food. Altering the gaseous environment of the food (as discussed in the following section) can retard surface spoilage without the need to lower the relative humidity.

Atmospheric composition Modification of the atmosphere during food storage, referred to as controlled-atmosphere (CA) or modified-atmosphere (MA) storage, has become widely accepted in certain segments of the food industry as a means to improve shelf life (see Chapter 4). Atmospheric modification can be achieved by the use of various gas mixtures that are high in car-

bon dioxide (CO2) or nitrogen (N2) either in the storage chamber or in the packaging, or by vacuum packaging. The use of O3 as a preservative during storage has also received consideration in recent years. O3 is a highly effective broad-spectrum bacteriocide. However, its strong oxidative properties have limited its use to applications where lipid oxidation and equipment corrosion are not concerns.

Increasing the level of CO2 during fruit storage has been shown to retard fungal rotting of fruits. CO2 also acts as a competitive inhibitor of ethylene and thus delays fruit ripening. Vacuum packaging, as well as C02 or N2 enrichment, is also being used in meat storage. The overall effect of these practices is to inhibit gram-negative spoilage microorganisms (e.g., Pseudomonas) and molds. Growth of beneficial lactic acid bacteria is also encouraged, which enhances the shelf life of the meat products (Blickstad and Molin, 1983; see Presence of other microorganisms, below). In most applications, C02 has been shown to be more effective than either vacuum packaging or N2 in improving meat shelf life.

Although more research is needed, atmospheric enrichment and/or vacuum packaging are also thought to inhibit most foodborne pathogens. A notable exception is the concern for the possible germination of C. botulinum spores under highly anaerobic environments, which occur at extremely high pressure of C02 or N2 gases and under high-vacuum conditions (Lambert et al., 1991). More typically, high CO2 pressures have been shown to be quite lethal to Salmonella (Wei et al., 1991). Effects of atmosphere modification on L. monocytogenes vary, with C02 being more effective than N2.

Presence Of other microorganisms The microflora of food products consists of a mixture of microorganisms, which may include spoilage microorganisms, pathogens, and innocuous microorganisms as well as desirable microorganisms that aid in food preservation. The most notable of these desirable microorganisms are the lactic acid bacteria. These are essential to the production of a variety of fermented food products, including cheese and cultured dairy products, pickles, sauerkraut, and sausages. Furthermore, their growth and activity enhance the shelf life of packaged meat products. In addition to the direct effect of the lowered pH from the lactic acid, lactate itself is also inhibitory to other bacteria (Williams et al., 1995). Many lactic acid bacteria possess the lactoperoxidase system (see Indigenous antimicrobial agents, above), and this results in synthesis of hydrogen peroxide, which inhibits other bacteria. Certain lactic acid bacteria also produce another class of antimicrobial compounds, termed bacteriocins (Klaenhammer, 1988).

Some spoilage microorganisms also inhibit the growth of pathogenic microorganisms through competition; others, however, can stimulate pathogen growth. For example, Pseudomonas species have been shown to stimulate L. monocytogenes (Marshall and Schmidt, 1988) and S. aureus (Seminiano and Frazier, 1966), among others, by providing more available substrates for their growth through proteolysis and lipolysis.

Although this has not been as extensively studied as bacterial effects, the presence of yeast and molds and/or their metabolites can alter the growth and activity of bacteria. For example, it is generally accepted that the yeast metabolites (such as carbon dioxide and ethanol) in alcoholic beverages and bread products are inhibitory to many spoilage and pathogenic bacteria. During the ripening of Camembert and related cheese products, the naturally occurring yeast exerts an antilisterial effect (Ryser and Marth, 1987). On the other hand, the growth of L. monocytogenes may in fact be stimulated by the mold Pénicillium camemberti that is associated with Camembert manufacture (Ryser and Marth, 1988).


With the exception of how they may be affected by improper manufacturing techniques or poor sanitation practices, the intrinsic factors discussed above do not generally fall under regulatory scrutiny. However, many of the extrinsic factors, especially heat treatment and food storage temperature requirements, do fall under federal, state, and international regulations.

Heat Treatment

Commercial sterilization of hermetically sealed food products domestically manufactured or imported into the U.S. is regulated by the Food and Drug Administration (FDA; 1998a). These regulations cover low-acid canned foods (LACF) that have a pH > 4.6 and an aw of >0.85 and acidified foods (AF) that have been acidified to a pH of <4.6. Although the FDA does not approve, license, or issue permits for finished food products in interstate commerce, all commercial processors and importers of LACF and AF are required to register their establishments and file processing information with the FDA.

According to the milk pasteurization regulations defined in the Grade A Pasteurized Milk Ordinance (USPHS/FDA, 1995), it is necessary to ensure that every particle of milk is heated to the appropriate temperature for the appropriate time and, furthermore, that the equipment used meets strict regulatory testing and controls to avoid any risk of cross-contamination with raw product or risk of postpasteurization contamination. Recommendations for pasteurization temperature and time parameters have not been as specifically defined for juice and other liquid food products. Recommended cooking procedures for meats, seafood, and other products prepared in retail food systems are described in the FDA Food Code (USPHS/FDA, 1997).

Temperature Requirements for Food Storage and Transportation

Maximum regulatory storage temperature requirements have been traditionally set at 7°C (45°F) by state and federal regulations for a number of commercial food products including milk, meat, and seafood products. Because of concerns about psychrotrophic growth of certain pathogens, the FDA-recommended temperature for food storage in retail establishments has been reduced from 7°C (45°F) to the current 5°C (41°F) or below (USPHS/FDA, 1997). A proposed rule was recently issued jointly by the Food Safety and Inspection Service (FSIS) and the FDA directed at reducing the potential contamination of Salmonella enteritidis in eggs (FDA, 1998b). In the proposed rule, FSIS will amend its regulations to require that shell eggs packed for consumer use be stored and transported at <7°C (45°F) and that these eggs be labeled to indicate that refrigeration is required. Although some states already specify a 7°C (45°F) temperature for egg storage, others have retained the 15.5°C (60°F) traditionally required under USDA grading programs.


In recent years, acidic food products, including mayonnaise, apple cider and other fruit juices, and yogurt, have been implicated in foodborne disease outbreaks that have primarily involved E. coli 0157:H7 or Salmonella (USDA, 1998). As discussed above, the acid survival characteristics of these microorganisms are dependent on a variety of factors. In general, acid survival is greater during low-temperature storage.

Current research has primarily been directed at improved understanding of acid adaptation and its importance in food safety. Acid adaptation by prior incubation at pH 5.0 has recently been shown to greatly enhance the acid survival characteristics [especially at 5°C (41°F)] of strains of E. coli 0157:H7 and Salmonella in various acidic condiments (Tsai and Ingham, 1997). In general, acid-adapted strains of E. coli 0157:H7 survived longer than did Salmonella or nonpathogenic E. coli strains. The incidence of acid-adapted E. coli 0157:H7 in feces of feedlot cattle has been related to the type of feed and may decrease in animals fed grass-based compared with grain-based diets (Stanton, 1997).

Heat Resistance

Foodborne illness outbreaks associated with commercial hamburger products and isolation of E. coli 0157:H7 from ground beef have stimulated concern regarding appropriate cooking temperatures in retail and home cooking applications for destruction of this microorganism. This concern has led to redefinition of cooking recommendations and requirements for retail preparation (USPHS/FDA, 1997).

The potential association of pathogens with unpasteurized juice products discussed above has opened debate over the necessity for mandating pasteurization of fruit and vegetable juices. Short of requiring pasteurization,

FDA is proposing that all juice manufacturers develop a Hazard Analysis Critical Control Point (HACCP) system that would include validation that the processing/handling system used is capable of a 5-log reduction in a pertinent pathogen (defined as E. coli 0157:H7 or L. monocytogenes-, USDA, 1998).

Because of concerns regarding the alleged heat resistance of Mycobacterium paratuberculosis in milk, milk pasteurization requirements in the U.S. and worldwide are currently under scrutiny. This microorganism, the causative agent for Johne disease in cattle and possibly associated with Crohn disease in humans, has been isolated from raw and pasteurized milk samples in the United Kingdom (Streeter et al., 1995). Experimental data on the survival of this organism to pasteurization treatment have been conflicting and inconclusive. The heat resistance of this microorganism is related to initial population as well as its physical state (clumped vs. nonclumped). M. paratuberculosis may survive typical pasteurization treatments in test tube heating experiments (Sta-bel et al., 1997; Sung and Collins, 1998) or using laboratory scale high temperature short time (HTST) pasteurization equipment at initial inoculation levels of >102 (Grant et al., 1996; Grant et al., 1998). Other investigations using laboratory scale HTST pasteurization equipment have resulted in complete inac-tivation using an initial inoculation of 104 and 106 cfu/ml (Stabel et al., 1997).

Heat-inducible thermal tolerance, a property acquired after sublethal heat treatment or "heat shock," has been described for many bacteria. For example, it has recently been shown that Clostridium perfringens strains with acquired thermal tolerance—which are capable of surviving normal cooking treatments—can result from "heat shocking" vegetative cells at 55°C (131°F) for 30 min (Heredia et al., 1997). Exposure to low heat has also been shown to increase the heat resistance of E. coli 0157:H7. In investigations in which beef gravy inoculated with 0157:H7 was preheated to 46°C (114.8°F) for 15-30 min, the heat resistance of the microorganism at 60°C (140°F) increased by 1.5fold (Murano and Pierson, 1993). Heat-induced thermal tolerance may have implications for manufacturers of refrigerated, cook-in-the-bag foods, such as filled pastas, gravies, or beef stews.

Resistance to Antimicrobial Agents

Subtherapeutic use of antimicrobial drugs in animal husbandry and their use in medicine may introduce selective pressures that enhance the emergence of resistant strains of enteric pathogens. For example, poultry have been suggested to be an important reservoir of antibiotic-resistant Salmonella strains because of selection and spread of transferable multiple resistance factors (R factors; D'Aoust et al., 1992). Antibiotic resistance profiles and R factors of Salmonella and E. coli isolates from 104 broiler carcasses have recently been characterized (Tessi et al., 1997).

Although primarily investigated in Great Britain, zoonotic infection of S. typhimurium [definitive type (DT) or phage type] 104 has become a well-recognized problem throughout the world (Dargatz et al., 1998). Multidrug-

resistant S. typhimurium (mrDTl04) has known resistance to five antibiotics (ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline) and may have acquired resistance to other drugs. Although occurrence of S. typhimurium mrDTl04, and related phage types I04b and U302, has not been well established in the U.S., it may have been present since the early 1990s. A multiresistant S. enterica serotype has also recently emerged in the U.S. (1998).

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