Part III

Quality and Safety of Frozen Foods

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CONTENTS

Quality and Safety of Frozen Meat and Meat Products

Sandra Moorhead
University of Guelph, Guelph, Ontario, Canada

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. Meat Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Prefreezing Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Preslaughter Factors Affecting Meat Quality . . . . . . . . . . . . . . . . . . . . . . . 2. Processing Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. The Freezing Process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Freezing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Frozen Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Thawing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Processed Meats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . III. Meat Safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. General Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Spoilage Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Pathogenic Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

311 312 312 312 312 313 313 313 314 314 317 317 318 318 320 320

I. INTRODUCTION
Historically, meat has been a major component of the diet in many cultures around the world, and remains so today. However, meat is a highly perishable food commodity which unless appropriately modied or stored, will rapidly spoil from the growth and by-products of microorganisms, as well as develop unpalatable characteristics because of endogenous biochemical degradation of the meat components. Before the advent of technology enabling refrigeration and freezing as preservation methods, traditional means of meat preservation were largely either drying or salting. However, these methods change the taste and texture of the meat and meat products. Meat preservation by freezing has been used for centuries as local production of meat exceeded the immediate requirements for consumption. An approximate storage life for frozen meat is between 10 and 24 months if stored at 2 188C, and between 15 and 24 months if stored at 2 248C [1]. Research in the late 19th century indicated that frozen storage did not compromise the quality of red meats, and one of the rst practical demonstrations of this was on 5th February, 1882, when a cargo of frozen meat was dispatched from New Zealand to England and arrived in excellent condition [2]. The retail revolution in consumer packs of frozen meats began in the 1930s in the USA, with fruit and vegetables, meats and shes being successfully marketed. Since then, the number and variety of frozen foods has grown immensely, adapting to changing consumer needs. The range of meat cuts and meat products available to processors, retailers, and consumers is now huge, and meat
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may be frozen as carcasses, as packaged primal or consumer cuts, or as a range of processed meat products. Many factors can affect the quality of frozen meat, including the state of the animal upon slaughter, the slaughter and conditioning process, processing techniques, and freezing conditions. Freezing technology includes three steps: a freezing process, storage at freezer temperatures, and a thawing process; physical, chemical, and nutritional changes can occur during each process. This chapter will discuss the quality and safety of frozen meat and meat products, resulting from preslaughter, slaughter, processing and nally freezing, frozen storage, and thawing conditions.

II. MEAT QUALITY

The quality characteristics that meat producers have to be concerned with include organoleptic and physicochemical qualities such as color, texture, avor, exudate (drip) loss, nutrient content, and fat oxidation.

A. PREFREEZING CONSIDERATIONS
1. Preslaughter Factors Affecting Meat Quality One of the major preslaughter factors inuencing meat quality is the concentration of muscle glycogen at slaughter [3]. Postslaughter, muscle glycogen is converted into lactic acid by way of glycolysis; gradually lowering the muscle pH to a nal value is termed the ultimate pH. The ultimate pH of table quality muscles from a well-fed, rested animal is approximately 5.6. Stressful conditions in the days and hours leading to slaughter can result in low glycogen concentrations at slaughter. The resultant ultimate pH is higher than normal. When approximately more than pH 6.0 the meat takes on a dark, rm, and dry (DFD) character, with concomitant changes in avor and keeping quality in the chilled state. Other processing factors that may affect meat quality include the intrinsic postmortem glycolytic rate of the species concerned. Decrease in muscle pH to below 6.0 in a typical chilling environment occurs quickly in pigs (5 10 h), but more slowly in sheep (16 24 h) and cattle (up to 36 h) [4]. During this time, if the carcass is cooled too quickly, exposed muscles can cold-shorten, toughening the meat when frozen. Electrical stimulation accelerates glycolysis, decreasing the muscle pH and hastening the onset of rigor to the point that muscles can no longer cold-shorten [5]. 2. Processing Factors Another advantage of electrical stimulation is that postslaughter animal movement is reduced, resulting in a fresher brighter meat color at 48 h [6]. The mechanism for this is believed to be destruction of mitochondrial enzyme activity such that postmortem oxidation is reduced. Concentrations of the bright red oxymyoglobin increase at the meat surface. The color of raw meat is determined by the concentration and chemical nature of the haemoproteins present [7,8]. The overall redness of the meat is because of oxymyoglobin, the oxygenated form of myoglobin, whereas the unattractive brown color after prolonged storage is because of metmyoglobin, the oxidized form of myoglobin [9 11]. With the recent trend towards centralized packaging and distribution of consumer packs to retail outlets [12], it is necessary for meat distributors to ensure that display is desirable, but only at the point of display. Color at prior times is not important (it could be argued that color is never important for eating quality, but to buy meat unseen would require consumer re-education). Aging, the enzymatic breakdown of myobrillar proteins resulting in tenderness, is most rapid at high temperatures. Aging can also occur during frozen storage, as free water exists in frozen water. Reactions continue, although not at the pace above freezing point [13].

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Hot boning, where the meat is removed from the skeletal structure before the onset of rigor mortis, often increases the risk of muscle toughening, but this is almost certainly because of cold-shortening. Provided cooling is controlled (e.g., by immersion in temperature-controlled baths), hot-boned meat can be as tender as cold-boned meat and maybe more so. Oxidative rancidity develops in frozen whole tissue as well as ground meats if there is excessive exposure to air. This can be achieved with modied atmospheres or vacuum packaging.

B. THE FREEZING PROCESS

Freezing meat offers a product with a nutritional quality close to fresh meat, however, it may signicantly affect the organoleptic properties of meat such as color [14]. Freezing of aged, well treated meat does not necessarily have any signicant effect on the cooked color, avor, odor, or juiciness of that meat, and in fact in some circumstances produces a slight tenderizing effect as in the case of frozen pork loin roasts [15], although it was also found that off-avors developed on prolonged storage, presumably through oxidative rancidity.

1. Freezing Freezing is the transition of water in the muscle tissue crystallizing into ice. The freezing rate refers to the rate at which any given part of the food is cooled. The undesirable changes in meat during freezing is because of mechanical damage to muscle cells from large ice crystals, and to chemical damage arising from increase in concentration of tissue solutes. Before freezing, the meat is chilled to between typically 0 and 108C. The changes that occur in this period have an important effect on the subsequent quality of the frozen product. They include the unwanted growth of microorganisms, leading to early onset of spoilage, as well as undesirable chemical changes such as rancidity, which if initiated during the chilled phase prefreezing, will continue at an accelerated rate after freezing. Therefore, the time meat is held chilled affects the overall quality of the meat or meat product. Moisture loss during chilling has both positive and negative effects on meat quality. The processor has to achieve enough surface drying to minimize microbial growth, while at the same time minimizing weight loss and preserving meat surface appealing to the consumer. Factors affecting moisture loss include muscle type, preslaughter factors that affect the ultimate pH, area of cut surface exposed, freezing rate, storage conditions, and thawing rate. et al. [16] investigated a range of freezing rates from 0.22 to 5.66 cm/h on beef Petrovic M. longissimus dorsi, studying physicochemical properties including weight loss, pH, and waterbinding capacity. Mechanical tenderness, myobrillar solubility, and sensory evaluation on the cooked product were also examined. The greatest weight losses were registered at slow freezing rates (0.22 and 0.39 cm/h), and the meat was found to be tougher and less soft. At these slow freezing rates, myobrillar proteins were least soluble. However, very quick freezing rates (4.92 and 5.66 cm/h) caused myobrillar damage, lower water-binding capacity, and tougher, drier meat. These authors found that a freezing rate between 3 and 4 cm/h had the least effect on muscle structure and the state of myobrillar proteins, and cooked muscles from samples frozen at these rates were evaluated as the most tender [16]. In another study, slowly frozen meat resulted in more drip than fast frozen meat but otherwise freezing rate had no effect on the functional attributes of protein solubility, sulfydryl content, surface hydrophobicity, emulsion activity index, or meat color [17]. These authors [16,17] concluded that the current practice of blast-freezing and storage at 2 18 to 2 208C was sufcient to maintain the quality of manufacturing beef.

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2. Frozen Storage Frozen meat storage temperatures are ideally at or below 2 188C [1]. Fluctuations above this temperature, caused by a range of actions from electrical or equipment failure to movement of the product around cool-stores or during transportation, will result in a product of poorer quality. This is caused by denaturation of proteins occurring as solute concentration increases, damaging ice crystals growing in size, lipids oxidation, and dehydration of surfaces (freezer burn). These events can be partially controlled by suitable packaging and by a reduced oxygen concentration to reduce lipid oxidation. The effect of storage time and temperature on the functional attributes of meat were assessed by Farouk et al. [17]. Storage temperatures of 2 18, 2 35, and 2 758C were examined and found to affect the solubility of both myobrillar and sarcoplasmic proteins minimally, but not other attributes such as emulsion activity and stability, water-holding capacity, color, drip, and tenderness [17]. Storage time alone had the greatest effect on thawed beef in this study. Storage times of 0, 3, 6, 9, and 12 months were studied, and increases in pH, emulsion activity, and stability were recorded, while total protein solubility decreased, indicating denaturation of proteins, responsible for loss of quality over time. Conversely, the meat became more tender over storage time, which is attributed to the breakdown of muscle structure caused by enzyme activity and ice crystal formation. These authors concluded that expensive ultra-low temperature storage of meat was unnecessary for manufacturing beef, but that extended storage times were more detrimental to meat quality. Most nutrients were retained during freezing and subsequent storage (Table 15.1) [18]. Experiments to measure these nutrients were performed between the 1950s and 1970s, with no further work published subsequently. Soluble proteins and vitamins have been shown to be lost with drip during thawing, but the uid lost with drip approximates the uid lost when fresh meat is cooked, therefore the net loss of nutrients is minimal [6]. 3. Thawing Regulatory authorities advocate commercially thawing meats at low temperatures (, 108C) or that processors show equivalency for microbiological growth rates during thawing [26]. Early research focused on the effect of household thawing on the organoleptic quality of meats [27], nding that variations in thawing methods have a limited but not insignicant effect on total end product quality as shown in Table 15.2. Stoll et al. [27] found that a slow thawing process at not too low a temperature is preferable for beef. Thawing meat results in an approximately 2 6% decrease in yield because of drip loss [28], with subsequent vitamin losses (however, the drip loss may be included in the food preparation meaning no losses). Drip loss depends on the species, the muscle, and the rate of thawing which in Table 15.3 [28] was standardized at either for 4 h at room temperature, or 20 h at 48C. Pearson et al. [29] found a much higher nutrient loss, but thawing was at 14 15 h at 268C, and the percent drip loss in beef was not recorded. In contrast, Ngapo et al. [30] observed only subtle differences in drip loss and in the ultra-structure of samples of pork after frozen storage and thawing.

C. PROCESSED MEATS
The product quality of processed meats is directly attributable to the quality of the raw materials. Often meat for further processing has already been frozen, amplifying the effects of further freezing, storage, and thawing. Additional ingredients are usually added which affect the quality, shelf life, and overall acceptability of these products, and the physicochemical reactions occurring during the freezing process.

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Handbook of Frozen Food Processing and Packaging

TABLE 15.1 Percent Retention of Nutrients in Frozen Stored Pork and Beef (Longissimus dorsi )
Species Pork Pork Pork Pork Pork Pork Pork Beef Beef Note: nt, not tested. Frozen storage (days) 180 180 365 180 168 90 120 180 300 Temperature (8 C) 2 18 2 26 2 18 2 18 2 18 2 20 2 16 2 18 2 18 Thiamin 68 83 89 101 85 92 78 92 98 Riboavin 66 97 144 81 94 nt nt 91 57 Niacin 90 98 114 106 95 nt nt 101 96 Pantothenic Acid nt nt 106 84 nt nt nt 91 nt Pyridoxin nt nt nt 64 nt nt nt 76 nt Retinol nt nt nt nt nt 92 nt nt nt Reference [19] [19] [20] [21] [22] [23] [24] [25] [25]

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TABLE 15.2 Effects of Various Methods of Thawing Beef Frozen in 600 g Pieces (Score: 9, highest; 5, Unsatisfactory)
Methods and Thawing Times Room temperature 16 h, then cooked for 2 h Refrigerator 24 h, then cooked 2 h Cold tap water 3 h, cooled 2 h Pressure cooked 45 min, 8 min standing High pressure steam cooked 1 h Microwave 2100 W, 27 min in glass dish with gravy Color 7.8 7.3 7.5 8.0 5.0 6.3 Organoleptic Evaluations Form Flavor 7.8 7.8 7.8 7.8 6.5 6.8 7.5 8.0 8.0 7.5 7.0 6.0 Texture 7.5 7.3 8.3 6.8 7.0 5.0

Source: Reprinted from The Quality of Frozen Foods, M Juls (Ed.), p. 261, 1984, with permission from Elsevier.

Tempering frozen blocks of meat (partial thawing) is often employed to reduce drip loss, bacterial growth, and to facilitate comminution where this is applied. Thus tempering allows better control of quality of these processed meat products [31]. However, vitamins are likely to be lost to some extent during further processing [32]. Ashby and James [33,34] examined the effects of freezing and packaging methods on shrinkage and freezer burn in cooked hams. They found that hams frozen in a blast freezer (2 278C) sustained less shrinkage compared to ham frozen by forced air (2 228C) and still air cold rooms (2 208C). Forced air freezing increased amounts of freezer burn between 4 and 6 months frozen storage, compared with blast or still air-freezing methods, although differences in degree of freezer burn were lost after 6 months of frozen storage. In another ham experiment, uncured hams were frozen on racks at 2 298C, then stored at 2 188C for 3 months before various thawing and curing treatments [35]. Weight loss, raw color, aroma, and general appearance were evaluated. Table 15.4 shows the results for weight loss. From an economic consideration, Kemp et al. [35] suggested that there was a considerable advantage in curing frozen hams.

TABLE 15.3 Percent Drip Loss and B-vitamins Loss of Original Content
Cut Pork Tenderloin Loin Chop Blade roast Rib steaka Rib steak Rib roast Leg roast % Drip 1.4 1.9 2.0 2.2 6.3 5.7 3.2 2.2 Thiamin 0.9 2.1 2.4 5.1 16.8 14.3 5.3 2.3 Riboavin 0.70 2.9 3.0 0.4 6.3 8.6 3.2 1.5 Niacin 0.72 1.5 1.5 3.1 1.5 9.0 5.3 3.6

Beef

Lamb
a

Thawed at room temperature, all others thawed in refrigerator. Source: Derived from LH Kotschevar. Journal of the American Dietetics Association 31:589596, 1951.

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TABLE 15.4 Percent Weight Loss because of Thawing Method of Uncured Hams After Thawing and Dry-Curing
Processing Cured Smoked Aged 1 month Aged 2 months Aged 3 months Frozen 3.1 12.9 17.5 22.0 24.9 Treatment Preprocessing Cooler-Thawed, 38 C Room-Thawed, 158 C 6.1 15.7 21.0 25.5 29.3 5.4 16.1 20.6 25.3 27.8 Water-Thawed, 388 C 5.0 16.8 21.4 26.0 28.7

Source: From JD Kemp, BE Langlois, JD Fox. Journal of Food Science 43:860863, 1978. Reprinted with permission from The Institute of Food Technologists.

The effects of freezing and frozen storage were evaluated on all-beef and soy-extended patties by Berry [36], who reported that patties stored at 2 78C had greater surface discoloration and freezer burn than patties stored at 2 18 or 2 238C. Patties were stored for 0, 6, 9, 12, 18, or 24 months before evaluation, and results indicated that storage of patties at 2 78C should be avoided owing to reduction in quality after 6 months (and longer) of storage.

III. MEAT SAFETY A. GENERAL CONSIDERATIONS

One of the major advantages of freezing meats is the slowing or prevention of growth of spoilage and pathogenic microorganisms present on either the meat surface or within the meat product. However, some microbial enzymes may remain active at freezing temperatures, and cause spoilage, for example, the storage life of frozen pork is limited by rancidity caused in part by microbial or tissue lipolysis [37]. Meat, although initially a sterile surface, is microbiologically contaminated at all stages of the slaughter, dressing, chilling or freezing, storage, processing, and packaging chain [38]. Sources of contamination include the animal itself (external surfaces such as eece, hide or skin, and the gastrointestinal and respiratory tract). The process workers and the processing environment also contribute to the microora found on the end-product. Contaminating bacteria are to be kept to a minimum through strict adherence to hygienic handling and processing practices. However, the same bacteria species can be isolated from beef, pork, and sheep, and numbers on fresh carcasses are commonly between 101 and 103 colony forming units (cfu)/cm2 for beef [39 43], between 102 and 104 cfu/cm2 for sheep [42,44 46], and between 103 and 104 cfu/cm2 for pork [39,47]. Freezing may reduce these numbers slightly, but thawing provides the condition where proliferation of bacteria can begin. Regulatory authorities generally advocate that commercial thawing be undertaken at temperatures below 108C to ensure that the hygienic status of the product is not compromised [26]. There are two broad groups of microorganisms of concern in meat safety, those that in large numbers cause spoilage and those that cause food-borne illness. For the latter, some species need only be present in very small numbers. Meat presents a nutritious substrate for microorganisms, and depending on the packaging used, either aerobic or anaerobic bacteria can dominate the microora.

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Freezing affects bacterial cells as much as the muscle cells of meat. Intracellular ice formation and water diffusion, resulting in a sublethal concentration of solutes is also damaging to microorganisms [48]. Ironically, freezing regimes to optimize quality in muscle cells also optimizes survival of contaminating bacterial cells [49]. For example, almost 100% of super-cooled Saccharomyces cerevisiae and Escherichia coli were able to survive frozen storage at 2 16 and 2 108C, respectively [50]. Repeated freezethaw cycles can disrupt and destroy bacteria [48]; however, the effects of cyclic freezing are not well documented on most microbial pathogens. An important consideration for microbial growth is the water activity (Aw) of the substrate, or in general terms, the available moisture. Most food spoilage bacteria require an Aw of above 0.9, with the exception of Staphylococcus aureus (0.86) [51]. Approximate minimum Aw values for foodrelated fungi are lower, but still average around 0.8. At 2 188C, frozen meat containing ice in equilibrium will have an Aw of around 0.84, a condition under which few bacteria can grow [51]. Other factors that affect the survival of microorganisms during freezing and thawing include the type and strain of the microorganism, phase of growth, nutritional status, rate of cooling, substrate, the holding temperature, time frozen, and rate of thawing. Some bacteria are able to form spores as a survival mechanism, and these spores are extremely resistant to the effects of freezing and repeated freezethaw cycles [49]. Freezing has little effect of on viruses [52,53], but in contrast, nematode parasites are very susceptible to freezing. In fact, freezing is a regulated procedure for inactivating trichinae in pork [54].

B. SPOILAGE BACTERIA
Spoilage bacteria include Pseudomonas spp., Acinetobacter or Moraxella spp., Aeromonas spp., Alteromonas putrifaciens, Lactobacillus spp., and Brochothrix thermosphacta. These psychrotrophic bacteria originate from soil, vegetation, and water on the animal hide or eece. The processing environment can also cause contamination. The initial microora on pork will differ from that of other red meats because of the dehairing processes. However, normal processing events recontaminate the pork with a microora similar to that of other red meats [55]. Until spoilage is evident to the senses, the only detectable effect of bacterial growth is reduction in glucose levels, which does not alter the organoleptic qualities of meat. Once glucose supplies are depleted, microorganisms then degrade proteins, resulting in suldes, amines, acetic acid, lactic acid, isovaleric acid, isobutyric acid, esters, and nitriles being produced. These by-products result in spoilage odors and avors. Growth characteristics of the spoilage bacteria on meat depend on the initial ora, level of contamination, storage time, temperature, and packaging regime. The microora of anaerobically stored meat is usually dominated by species of Lactobacilli, which of necessity grow slowly and fermentatively, therefore resulting in little effect on the organoleptic quality of meat. However, spoilage avors will develop over time because of the accumulation of volatile organic acids. Under aerobic condition, as the temperature is decreased, psychrotrophic bacteria begin to dominate the microora, with Pseudomonas spp. the most dominant strain [56]. While growth of the above bacteria is stopped at temperatures below 2 28C, xerotolerant molds and yeasts can continue growing. The more common meat-spoilage molds have a minimum growth temperature near 2 88C [57], and cause conditions known as black spot, white spot, bluegreen mold, and whiskers. At this temperature visible colonies will take several months to develop [58]. Some species of molds, for example, Penicillium expansum, when frozen on growth medium at a freezing rate of 28C/min, resulted in shrinkage of hyphae, and at a faster freezing rate of 208C/min, intracellular ice was formed [59].

C. PATHOGENIC BACTERIA
The presence of a pathogen on frozen meat is directly affected by the prevalence of the pathogen on slaughter animals. Any organism associated with the gastrointestinal tract of slaughter animals has

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TABLE 15.5 Microbiological Baseline Data of Beef Sides, Market Hogs, and Ground Beef in the United States (% positive)
Microorganism Indicator Organisms Aerobic plate count ( 100,000 cfu/cm2 or cfu/g) Total coliforms, ( 100 cfu/cm2 or cfu/g) E. coli, ( 10 cfu/cm2 or cfu/g) Pathogenic Bacteria C. jejuni or coli E. coli O157:H7 Salmonella spp. C. perfringens S. aureus L. monocytogenes Steers or Cows or Bulls Pork Ground Beef Heifers (n 5 2079) (n 5 2112) (n 5 2112) (n 5 563)

93.1 96.4 95.9

96.3 92.2 91.8

91.6 84.2 80.0

100 92.0 78.6

2.6 0.2 1.0 2.6 4.2 4.1

1.1 nd 2.7 8.3 8.4 11.3

31.5 nd 8.7 10.4 16.0 7.4

0.002 nd 7.5 53.3 30.0 11.7

Note: nd, not detected. (Sources: From Anonymous. Nationwide beef microbiological baseline data collection program: steers and heifers. In: United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1994, pp. 19; Anonymous. Nationwide beef microbiological baseline data collection program: cows and bulls. In: United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1996, pp. 113; Anonymous. Nationwide pork microbiological baseline data collection program: market hogs, in United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1996, pp. 113; Anonymous. Nationwide federal plant raw ground beef microbiological survey, in United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1996, pp. 18.

the potential to contaminate meat from direct or indirect fecal contact. The processing environment is also a source of contamination, from equipment where biolm-containing pathogens have become established to the hands of process workers. Table 15.5 indicates the level of contamination found in a survey of cattle and pork in the United States between 1993 and 1996 [60 63]. Most bacteria are able to survive in a nongrowing state at chilled and frozen storage temperatures, but temperatures for vegetative growth are usually higher than 08C. For example, the minimum growth temperature for some of the more common pathogens are: Yersinia enterocolitica, 2 28C; Listeria monocytogenes, 18C, enterotoxigenic E. coli, 38C; Aeromonas hydrophila, 0 58C; non-proteolytic Clostridium botulinum, 3.38C; Salmonella, 7 108C; Bacillus cereus, 6 108C; S. aureus, 7 108C; proteolytic C. botulinum, 108C; and C. perfringens, 128C [64]. For ethical reasons, there have been limited studies on the doseresponse relationship of pathogens in foods, but from results of outbreaks and a few voluntary trials, the infectious dose has been estimated for Salmonella spp. (. 105 organisms) and C. jejuni (500 organisms) [65]. However, only a limited number of pathogenic bacteria genera have caused outbreaks associated with frozen foods, indicating that human pathogenic microorganisms are susceptible to freezing. This may be because of inherently low numbers present (below the infectious dose) or the inability to survive and grow on frozen meats by these organisms. Investigations on the growth and survival characteristics of pathogenic microorganisms were performed to determine if pathogenic bacteria are susceptible to freezing and or frozen storage. The survival of E. coli O157:H7 strains on beef trimmings frozen to 2 18 or 2 358C was determined in one trial. Counts on nonselective media remained constant throughout the 12-week storage trial, while counts on selective media decreased signicantly, indicating a degree of sublethal injury [66]. The growth and survival of E. coli O157:H7 has also been examined on comminuted product.

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Doyle and Schoeni [67] inoculated ground beef with E. coli O157:H7, formed hamburger patties, which were subsequently frozen and stored at 2 208C for up to 9 months. There was inconsequential loss of viability following these procedures. Sage and Ingham [68] found a reduction in E. coli O157:H7 numbers in ground beef patties after frozen storage and thawing, but again, enumeration was performed on selective media. In another experiment where E. coli O157:H7 was inoculated onto ground beef, then formed into patties, strains survived 12 months frozen storage at 2 208C, but gave a 1 2 log10 reduction in numbers [69]. The survival of three Salmonella serotypes inoculated onto beef trimmings and frozen to 2 18 or 2 358C was investigated by Dykes and Moorhead [70] who found that bacterial numbers did not decrease over the 9-month storage trial. Salmonella typhimurium was shown to be sublethally damaged but not destroyed by freezing in sausage and ground beef stored at temperatures between 2 18 and 2 208C, because more cells were recovered on nonselective media than selective [71]. With some localized exceptions relating to pork-borne C. coli infections, campylobacteriosis is not commonly acquired as a consequence of beef, lamb, or pork consumption, this may in part reect the low meat pH of these species compounded by the adverse conditions for Campylobacter survival prevailing at the carcass surface during air-chilling. Moorhead and Dykes [72] studied the susceptibility of C. jejuni in beef trimmings during freezing and frozen storage at 2 188C. Within 7 days, reductions in numbers from 0.6 to 2.2 log10 were observed, but there was no further loss of viability during subsequent storage. Earlier studies in ground beef showed that the addition of a cryoprotectant, such as 10% glycerol increased survival of C. jejuni during freezing [73]. Little work has been done on the effect of freezing on Listeria spp., but in one report, L. monocytogenes was shown to survive freezing well in ground beef, with the food found to contribute a protective effect [74]. Storage of raw, ground beef inoculated with S. aureus at 2 228C for 4 months, or frozen beef for 168 days, resulted in a decrease in numbers of approximately 1 log10 [75,76]. Demchick et al. [77] studied the survival of S. aureus in lean ground beef at two pH levels, over repeated freezethaw cycles, and also found a 1 log10 reduction in numbers. Freezing did not inactivate staphylococcal enterotoxin. Both spores and vegetative cells of C. perfringens are frequently found in small numbers on raw meats, and this organism often serves as an indicator for the more serious contamination of C. botulinum. Fresh meat products were inoculated with C. perfringens vegetative cells (and spores) and frozen to 2 278C. The number of viable cells was reduced by 90% in 42 days [78]. These same authors [78] found that while vegetative cell numbers decreased, the numbers of spores present remained unchanged. While these examples are not exhaustive, they do show that freezing is a poor bactericidal process.

IV. CONCLUSIONS
The quality and safety of meat and meat products is governed mainly by the presentation of slaughter stock; their state of stress and cleanliness are dominant factors. Freezing technology should be designed to ensure that the product does not signicantly deteriorate in eating quality and safety from its original state. Research has shown that correct freezing regimes can produce meat of acceptable quality with regard to consumer preferences and nutritional value. However, these freezing regimes rapid freezing followed by storage at nonuctuating, low temperatures may also optimize survival of contaminating bacterial cells. However, the incidence of food-borne illness from frozen meats is extremely low, indicating that there are both low numbers of pathogens that survive the antimicrobial practices in the processing system, and freezing techniques in practice are sufcient to prevent growth of any pathogens present.

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REFERENCES
1. Anonymous. Recommendations for the Processing and Handling of Frozen Foods. 3rd ed. Paris: International Institute of Refrigeration, 1986, pp. 42 131. 2. MFG Boast. The technology of freezing. In: RK Robinson, Ed., Microbiology of Frozen Foods. London: Elsevier Applied Science Publishers Ltd., 1985, pp. 1 39. 3. JR Bendall. Post mortem changes in muscle. In: GH Bourne, Ed., The Structure and Function of Muscle. Vol. 11. New York: Academic Press, 1973, pp. 244 311. 4. W Davenport. Chilling innovations. Meat Processing 28:44 47, 1989. 5. BB Chrystall, CE Devine. Electrical stimulation developments in New Zealand. In: AM Pearson, TR Dutson, Eds, Advances in Meat Research. Vol. 1. Electrical Stimulation. Westport, CT: AVI Publishing, 1986, pp. 73 119. 6. CE Devine, RG Bell, S Lovatt, BB Chrystall, LE Jeremiah. Red meats. In: LE Jeremiah, Ed., Freezing Effects on Food Quality. New York: Marcel Dekker, Inc., 1996, pp. 51 84. 7. DA Ledward, Colour of raw and cooked meat. In: DA Ledward, DE Johnston, MK Knight, Eds., The Chemistry of Muscle-based Foods. Cambridge: Royal Society of Chemistry, 1992, pp. 128 144. 8. C Faustman, RG Cassens, The biochemical basis for discoloration in fresh meat: a review. Journal of Muscle Foods 1:217 243, 1990. 9. M Renerre. Review: Factors involved in the discoloration of beef. International Journal of Food Science and Technology 25:613 630, 1990. 10. D Cornforth. Color: its basis and importance. In: AM Pearson, TR Dutson, Eds., Advances in Meat Research, Vol. 9. Quality Attributes and their Measurement in Meat, Poultry and Fish Products. London: Blackie Academic and Professional, 1994, pp. 34 78. 11. DE Hunt, DH Kropf. Color and appearance. In: AM Pearson, TR Dutson, Eds., Advances in Meat Research, Vol. 3. Restructured Meat and Poultry Products. New York: Van Nostrand Publishers, 1987, pp. 125 159. 12. Y Tomioka. Fresh meat. In: T Kadoya, Ed., Food Packaging. Sandiego, CA: Academic Press, 1990, pp. 309 321. 13. CL Davey, KV Gilbert. Thaw contracture and the disappearance of adenosine triphosphate in frozen lamb. Journal of the Science of Food and Agriculture 27:1085 1092, 1976. 14. MC Lanari, RG Cassens, DM Schaefer, KK Scheller. Dietary vitamin E enhances color and display life of frozen beef from holstein steers. Journal of Food Science 58:701 704, 1993. 15. LE Jeremiah, AC Murray, LL Gibson. The effects of differences in inherent muscle quality and frozen storage on the avor and texture proles of pork loin roasts. Meat Science 27:305 327, 1990. , R Grujic , M Petrovic . Denition of the optimal freezing rate-2. Investigation of the 16. L Petrovic physico-chemical properties of beef M longissimus dorsi at different freezing rates. Meat Science 33:319 331, 1993. 17. MM Farouk, KJ Wieliczko, I Merts. Ultra-fast freezing and low storage temperatures are not necessary to maintain the functional properties of manufacturing beef. Meat Science 66:171 179, 2003. 18. PP Engler, JA Bowers. B-vitamin retention in meat during storage and preparation. A review. Journal of the American Dietetics Association 69:253 257, 1976. 19. WP Lehrer, AC Wiese, WR Harvey, PR Moore. Effect of frozen storage and subsequent cooking on the thiamine, riboavin, and nicotinic acid of pork chops. Food Research 16:485 491, 1951. 20. BD Westerman. B-complex vitamins in meat. IV. Inuence of storage time and temperature on the vitamins in pork roasts. Journal of the American Dietetics Association 28:331 335, 1952. 21. FA Lee, RF Brooks, AM Pearson, JI Miller, JJ Wanderstock. Effect of rate of freezing on pork quality, appearance, palatability, and vitamin content. Journal of the American Dietetics Association 30:351 354, 1954. 22. BD Westerman, B Oliver, DI MacKintosh. Inuence of chilling rate and frozen storage on B-complex vitamin content of pork. Journal of Agricultural and Food Chemistry 3:603 605, 1955. 23. N Nestorov, Kozhuharova. Studies on the changes in thiamin and retinol content in pig liver and muscles after sharp freezing and long cold storage. Proceedings of the European Meeting of Meat Research Workers. Vol. 20, 1975, pp. 269 271. 24. JD Kemp, RE Montgomery, JD Fox. Chemical, palatability and cooking characteristics of normal and low quality pork loins as affected by freezer storage. Journal of Food Science 41:1 3, 1976.

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322

Quality and Safety of Frozen Meat and Meat Products

25. FA Lee, RF Brooks, AM Pearson, JI Miller, F Volz. Effects of freezing rate on meat. Appearance, palatablity, and vitamin content of beef. Food Research 15:8 15, 1950. glementation des conditions hygeniques de conge lation de conservation et de de con26. Anonymous. Re lation des denre es animales et dorigine animales, in Ministe ` re de lAgriculture, Article 20, 1974. ge twyler, M Fausch, T Neidhardt. Thawing of frozen foods by different methods. Bulletin 27. K Stoll, D Da of the International Institute of Refrigeration (Annexe 1977-1):393 397, 1977. 28. LH Kotschevar. B-vitamin retention in frozen meat. Journal of the American Dietetics Association 31:589 596, 1951. 29. AM Pearson, JE Burnside, HM Edwards, RS Glasscock, TJ Gunha, AP Novak. Vitamin losses in drip obtained upon defrosting frozen meat. Food Research 16:85 87, 1951. 30. TM Ngapo, IH Babare, J Reynolds, RF Mawson. A preliminary investigation of the effects of frozen storage on samples of pork. Meat Science 53:169 177, 1999. 31. A Bezanson. Thawing and tempering of frozen meat. Proceedings of the Meat Industry Research Conference. Chicago, Arlington, VA: American Meat Institute Foundation, 1975, pp. 51. dek, J Vel s ek, J Pokorny. Vitamins. In: J Dav dek, J Vel s ek, J Pokorny, Eds., Developments in 32. J Dav Food Science, Vol. 21. Chemical Changes During Food Processing, Amsterdam: Elsevier, 1990, pp. 230 293. 33. BH Ashby, GM James. Effects of freezing and packaging methods on freezer burn of hams in frozen storage. Journal of Food Science 38:258 260, 1978. 34. BH Ashby, GM James. Effects of freezing and packaging methods on shrinkage of hams in frozen storage. Journal of Food Science 38:254 257, 1978. 35. JD Kemp, BE Langlois, JD Fox. Composition, quality and microbiology of dry-cured hams produced from previously frozen green hams. Journal of Food Science 43:860 863, 1978. 36. BW Berry. Changes in quality of all-beef and soy-extended patties as inuenced by freezing rate, frozen storage temperature, and storage time. Journal of Food Science 55:893 897, 1990. 37. M Ingram. Freezing, an integrated procedure. In: Meat Freezing. Why and How? Langford, UK: Meat Research Institute, 1974, pp. 1.1 1.4. 38. RG Bell, Chilled and frozen raw meat, poultry and their products. In: J Milner, Ed., LFRA Microbiology Handbook, Leatherhead UK, Leatherhead Food RA, 1996, pp. 1 53. 39. IB Hansson. Microbiological meat quality in high- and low-capacity slaughterhouses in Sweden. Journal of Food Protection 64:820 825, 2001. 40. PB Vanderlinde, B Shay, J Murray. Microbiological quality of Australian beef carcass meat and frozen bulk packed beef. Journal of Food Protection 61:437 443, 1998. 41. KA Murray, A Gilmour, RH Madden. Microbiological quality of chilled beef carcasses in Northern Ireland: a baseline survey. Journal of Food Protection 64:498 502, 2001. 42. J Sumner, E Petrenas, P Dean, P Dowsett, G West, R Wiering, G Raven. Microbial contamination on beef and sheep carcasses in South Australia. International Journal of Food Microbiology 81:255 260, 2003. 43. D Phillips, J Sumner, JF Alexander, KM Dutton. Microbiological quality of Australian beef. Journal of Food Protection 64:692 696, 2001. 44. EA Duffy, KE Belk, JN Sofos, SB LeValley, ML Kain, JD Tatum, GC Smith, CV Kimberling. Microbial contamination occurring on lamb carcasses processed in the United States. Journal of Food Protection 64:503 508, 2001. 45. D Phillips, J Sumner, JF Alexander, KM Dutton. Microbiological quality of Australian sheep meat. Journal of Food Protection 64:697 700, 2001. 46. CO Gill, J Bryant, DA Brereton. Microbiological conditions of sheep carcasses from conventional or inverted dressing processes. Journal of Food Protection 63:1291 1294, 2000. 47. CO Gill, J Bryant. The contamination of pork with spoilage bacteria during commercial dressing, chilling and cutting of pig carcasses. International Journal of Food Microbiology 16:51 62, 1992. 48. B Ray, ML Speck. Freeze injury in bacteria. CRC Critical Reviews in Clinical Laboratory Sciences 4:161 213, 1973. 49. BM Lund. Freezing. In: BM Lund, TC Baird-Parker, GW Gould, Eds., The Microbiological Safety and Quality of Food. Vol. 1. Gaithersburg MA: Aspen Publishers, 2000, pp. 122 145.

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Handbook of Frozen Food Processing and Packaging

323

50. P Mazur. Physical and chemical basis of injury in single-celled microorganisms subjected to freezing and thawing. In: HT Meryman, Ed., Cryobiology. London and New York: Academic Press, 1960, pp. 214 315. 51. JHB Christian. Drying and reduction of water activity. In: BM Lund, TC Baird-Parker, GW Gould, Eds., The Microbiological Safety and Quality of Food. Vol. 1. Gaithersburg, MA: Aspen Publishers, 2000, pp. 146 174. 52. R DiGirolamo, J Liston, JR Matches. Survival of virus in chilled, frozen, and processed oysters. Applied Microbiology 20:58 63, 1970. 53. RK Lynt. Survival and recovery of enteroviruses from foods. Applied Microbiology 14:218 222, 1966. 54. Anonymous. Prescribed treatment of pork and products containing pork to destroy trichinae. Code of Federal Regulations. Washington, DC: US Government Printing Ofce, 1987, pp. 207 215. 55. GA Gardner. Microbiology of processing: bacon and ham. In: MH Brown, Ed., Meat Microbiology. Applied Science Publishers, London, 1982, pp. 129 178. 56. J Labadie. Consequences of packaging on bacterial growth. Meat is an ecological niche. Meat Science 52:299 305, 1993. 57. WJ Scott. Water relations of food spoilage microorganisms. Advances in Food Research 7:83 127, 1957. 58. PD Lowry, CO Gill. Temperature and water activity minima for growth of spoilage moulds from meat. Journal of Applied Bacteriology 56:193 1999, 1984. 59. GJ Morris, D Smith, GE Coulson. A comparative study of the changes in the morphology of hyphae during freezing and viability upon thawing for twenty species of fungi. Journal of General Microbiology 134:2897 2906, 1988. 60. Anonymous. Nationwide beef microbiological baseline data collection program: steers and heifers. In: United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1994, pp. 1 9. 61. Anonymous. Nationwide beef microbiological baseline data collection program: cows and bulls. In: United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1996, pp. 1 13. 62. Anonymous. Nationwide pork microbiological baseline data collection program: market hogs, in United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1996, pp. 1 13. 63. Anonymous. Nationwide federal plant raw ground beef microbiological survey, in United Stated Department of Agriculture, Food Safety and Inspection Service, Washington, DC, 1996, pp. 1 8. 64. VN Scott, L Moberg. Biological hazards and controls, In: KE Stevenson, DT Bernard, Eds., HACCP Establishing Hazard Analysis Critical Control Point Programs, A Workshop Manual. Washington, DC: The Food Processors Institute, 1995, pp. 4.1 4.25. 65. MH Kothary, US Babu. Infectious dose of foodborne pathogens in volunteers: a review. Journal of Food Safety 21:49 73, 2001. 66. GA Dykes. The effect of freezing on the survival of Escherichia coli O157:H7 on beef trimmings, Food Research International 33:387 392, 2000. 67. MP Doyle, JL Schoeni. Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Applied and Environmental Microbiology 48:855 856, 1984. 68. JR Sage, SC Ingham. Survival of Escherichia coli O157:H7 after freezing and thawing ground beef patties. Journal of Food Protection 61:1181 1183, 1998. 69. SE Ansay, KA Darling, CW Kaspar. Survival of Escherichia coli O157:H7 in ground-beef patties during storage at 2, 2 2, 15 and then 2 28C, and 2 208C. Journal of Food Protection 62:1243 1247, 1999. 70. GA Dykes, SM Moorhead. Survival of three Salmonella serotypes on beef trimmings during simulated commercial freezing and frozen storage. Journal of Food Safety 21:87 96, 2001. 71. RAE Barrell. The survival and recovery of Salmonella typhimurium phage type U285 in frozen meats and tryptone soya yeast extract broth. International Journal of Food Microbiology 6:309 316, 1988. 72. SM Moorhead, GA Dykes. Survival of Campylobacter jejuni on beef trimmings during freezing and frozen storage. Letters in Applied Microbiology 34:72 76, 2002.

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324

Quality and Safety of Frozen Meat and Meat Products

73. NJ Stern, AW Kotula. Survival of Campylobacter jejuni inoculated into ground beef. Applied and Environmental Microbiology 44:1150 1153, 1982. 74. SA Palumbo, AC Williams. Resistance of Listeria monocytogenes to freezing in foods. Food Microbiology 8:63 68, 1991. 75. A White, LP Hall. The effect of temperature abuse on Staphylococcus aureus and Salmonellae and in raw beef and chicken substrates during frozen storage. Food Microbiology 1:29 38, 1984. 76. TE Minor, EH Marth. Loss of viability by Staphylococcus aureus in acidied media. Journal of Milk and Food Technology 35:548 555, 1972. 77. PH Demchick, SA Palumbo, JL Smith. Inuence of pH on freeze-thaw lethality in Staphylococcus aureus. Journal of Food Safety 4:185 189, 1982. 78. SP Trakulchang, AA Kraft. Survival of Clostridium perfringens in refrigerated and frozen meat and poultry items. Journal of Food Science 42:518 521, 1977.

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