16

Quality and Safety of Frozen Poultry and Poultry Products

Nahed Kotrola
Food and Beverage, Ecolab, Auburn, USA

CONTENTS
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutritional Aspects of Frozen Poultry and Poultry Products . . . . . . . . . . . . . . . . . . A. Nutrient Composition of Poultry Meat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Ingredients Added to Poultry Products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . III. Quality of Poultry Products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Freezing, Packaging, and Thawing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Frozen Poultry Product Quality during Storage . . . . . . . . . . . . . . . . . . . . . . . . 1. Carcass Changes during Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Bone Darkening during Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Palatability Changes during Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Protein Changes during Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Intrinsic Chemical Reactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Protein Denaturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Enzyme Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. The Concern for Quality and Consumer Acceptance . . . . . . . . . . . . . . . . . . . 1. Preservatives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Acidulants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Antioxidants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Stability and Acceptability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. Protecting the Quality of Frozen Poultry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Product Processing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Product Packaging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Product Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Safety of Poultry Products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Concern for Food Safety and Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Preventive Measures in the Processing Plant . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Phosphate Treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Chlorine Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Ozonation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Organic Acid Treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Hot Wash Treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Temperature Treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I. II. 326 327 327 329 329 329 330 330 332 332 332 332 333 333 333 333 333 334 334 334 335 335 335 336 336 336 337 337 338 338 338 338 338 339 339
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I. INTRODUCTION
In the United States, production and consumption of poultry have increased more rapidly than that of other meat sources since the 1960s. Consequently, poultry meat has become one of the meats most commonly chosen by consumers and is generally preferred by health-conscious consumers. In 1993, U.S. production of broilers reached 6.65 billion birds worth almost US$10 billion and production of turkeys totaled almost 300 million birds with a value of US$2.4 billion. Both of these statistics represent new records in production volume. The production, processing, and marketing of such large volumes of highly perishable food products make temperature control critical for this industry. Freezing and frozen storage constitutes the most effective long-term means of maintaining high quality and safety of the products for consumers. The poultry industry has seen tremendous innovation in the past years and with this change has come alternative methods of processing, storage, and treatment of poultry meat. From the onset of refrigeration, freezing of poultry on a regular basis has been commonplace. However, with the current state of the market, in which consumers look for increasing convenience and extended preservation and safety of their food, frozen poultry has come to play a tremendous role. The modern home does not necessarily have a designated cook, as may have been the case in previous years. In dual income households, dinner needs to be easily prepared with less time involved. At the same time, consumers are demanding the same quality that the industry has come to be known for in the past. Additionally, now more than ever, food safety is at the forefront of concern for the consumer who remembers food safety failures of the past. As frozen poultry does indeed appear to answer the needs of the common consumer, it is important to understand that this type of product carries with it several pitfalls that researchers are attempting to explore. Product tenderness is one of the primary concerns of the producer looking to freeze poultry. Compromise of the ideal consistency of the poultry product can be avoided in the freezing process. This may involve the temperature at which the meat is frozen, how quickly it is frozen, or perhaps ingredients that are added to preserve the eating quality of the meat. Product dehydration is the other major concern of the poultry processor when attempting to freeze a poultry product. With dehydration, essentially there are problems to avoid. The rst is product appearance and sensory characteristics. As we know, consumers eat with their eyes. If the surface of the chicken product is dehydrated, it may appear discolored or washed out, making it unappealing to the consumer. Additionally, the dehydration may cause the meat to become tough or off-avored. The second major problem with dehydration is the economic concern. As poultry is sold on a weight basis, any loss in product weight is interpreted as a nancial loss in the end. This is why producers are so concerned with preserving the weight of the poultry product by preventing dehydration. It is here that producers turn to researchers to answer the question of product preservation in the realm of frozen poultry. In addition to the meat quality concerns that producers have with frozen poultry, there is the concern of food safety. Although the simple process of freezing inhibits the growth of a large number of microorganisms, there are still a substantial number of organisms that are still present in many of these products, not only food spoilage organisms but also pathogenic microorganisms. Psychrotrophic organisms will be in the greatest abundance in this type of product, which can contribute to spoilage of food as well as human illness. It becomes apparent that with the freezing of poultry, we not only need to look at lipid oxidation as a means of spoilage but also the presence of microorganisms. Once again, it is the burden of the researcher to determine the effect of freezing on poultry safety as well as shelf life.

II. NUTRITIONAL ASPECTS OF FROZEN POULTRY AND POULTRY PRODUCTS

Although there has been much research into the nutrition of the chicken itself, there has been relatively little research on the nutritional value of poultry products for the consumer. Therefore, this
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section will draw inferences to the nutritional value of poultry products using information on the composition of poultry and poultry products and the nutritional requirements of adult humans. Certain nutrients known to have benecial or detrimental effects on human nutrition will be discussed relative to their occurrence in poultry products as well.

A. NUTRIENT COMPOSITION

OF

POULTRY MEAT

Although the requirements of humans are published by the United States Department of Agriculture (USDA) and several other sources internationally [1 6], it should be mentioned that these values are both extrapolations from a relatively small sample size and are often derived from short-term studies, which may neglect the long-term effect of a deciency in a given nutrient. In addition, many studies use decient populations to determine requirements, resulting in the use of subjects with altered metabolisms to determine the requirements of a nutrient for a population with normal metabolic rates. The nutrient requirements for adult humans are presented in Table 16.1. These values were obtained from the National Academy of Sciences and represent the recommended daily allowances (RDA) or acceptable macronutrient distribution range (AMDR) for macronutrients and select vitamins and minerals [1 5]. Table 16.2 shows the nutrient composition of poultry meat, both light and dark meat [6]. It should be noted that the sample size for the nutrient

TABLE 16.1 RDA of Macronutrients and Select Micronutrients for Adult Male and Female Humans
Nutrient Protein (g/day)a Digestible carbohydrates (g/day) Fiber (g/day) Fat (g/day) Saturated fat (g/day) Monounsaturated fat (g/day) Polyunsaturated fat (g/day) Vitamin B12 (mg/day) Calcium (g/day) Iron (mg/day) Phosphorous (mg/day) Adult Males (3150 yr of age) 1035 130 38 2035 ND ND 510 2.4 1 8 700 Adult Females (3150 yr of age) 10 35 130 25 20 35 ND ND 5 10 2.4 1 18 700

Note: ND refers to not determined and is specied for nutrients that are not required in the human diet.
a

Nutrients with a range provided represent the AMDR, representing the lower limit to prevent deciency and the upper limit to reduce the probability of developing metabolic disorders (e.g., heart disease) associated with excessive consumption of a nutrient.

Sources: Z Yang, Y Li, M Slavik. Use of antimicrobial spray applied with an insideoutside bird washer to reduce bacterial contamination on prechilled chicken carcasses. Journal of Food Protection 61:829832, 1998; H Xiong, MF Slavik, JT Walker. Spraying chicken skin with selected chemicals to reduce attached Salmonella typhimurium. Journal of Food Protection 61:272275, 1998; EC Okolocha, L Ellerbroek. The inuence of acid and alkaline treatments on pathogens and the shelf life of poultry meat. Food Control 16 (3):217225, 2005; G Purnell, K Mattick, T Humphrey. The use of hot wash treatments to reduce the number of pathogenic and spoilage bacteria on raw retail poultry. Journal of Food Engineering 62:29 36, 2004; RK Gast. Recovery of Salmonella enteritidis from inoculated pools of egg contents. Journal of Food Protection 56:2124, 1993. With permission.

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TABLE 16.2 Nutrient Composition of Dark and Light Cooked Chicken Meat with and Without the Skina
Nutrientb (85.1 g portion) Light Meat Skin-On Skin-Off 26 0 0 7 2 3 1 0.3 12 0.9 182 25 0 0 3 1 1 1 0.3 13 0.9 194 Dark Meat Skin-On Skin-Off 22 0 0 13 4 5 3 0.2 13 1.2 143 23 0 0 9 2 3 2 0.3 13 1.2 152

Protein (g) Digestible carbohydrates (g) Fiber (g) Fat (g) Saturated fat (g) Monounsaturated fat (g) Polyunsaturated fat (g) Vitamin B12 (mg) Calcium (mg) Iron (mg) Phosphorous (mg)
a

Values were summarized from Appendix A in Wardlaw, 1999 [37]. The standard portion size for meat samples before cooking was 3 oz or 85.1 g.

levels present is 85.1 g (3 oz), which is far less than the value that the average person would consume in a meal. A comparison of Table 16.1 with Table 16.2 shows that poultry meat, dark or light, has benets and shortcomings. A 85.1 g serving is more than sufcient to supply a days worth of protein for an adult. The implication of this is that when a consumer eats a more realistic portion, they will consume protein well in excess of their requirement. As amino acids are simply broken down for energy and excreted, an excess of this nutrient is not detrimental. Fat, a nutrient that is generally considered to have detrimental effects on health, is at a low concentration in poultry meat. An 85.1 g serving of white meat without the skin has a total of 3 g of total fat, 1 g of saturated fat, and 1 g of polyunsaturated fatty acids. In contrast, dark meat cooked with the skin has 13 g of fat, 4 g of saturated fat, and 3 g of polyunsaturated fat. There is no requirement for total fat, as the body is capable of synthesizing most fatty acids; however, it is recommended that no more than 35 g of fat is consumed per day, with a maximum of ten of those grams coming from saturated fat. Poultry products, especially with the skin removed, can be easily incorporated into a diet that meets these recommendations. The amounts of calcium, phosphorous, and iron in poultry meat will contribute to the RDA but will not be sufcient to meet these requirements alone. Interestingly, the vitamin B12 level in poultry is such that a single serving of chicken meat is insufcient to meet the requirement. Vitamin B12 is only present in animal products, yet the consumption of other animal products or at least seven servings of chicken would be required to meet the daily requirement. Fortunately, vitamin B12 is stored in the body and the requirement does not have to be met on a daily basis. A comparison between dark and light meat shows certain small differences. The protein level is slightly higher in white meat than in dark meat, with a correspondingly higher fat content in dark meat. This is due to the large white glycolytic bers in the breast muscle and the combination of glycolytic and oxidative bers in the dark meat. This ber difference also explains the higher level of iron in dark tissue, as myoglobin is not present in high levels in glycolytic bers. The amount of calcium and vitamin B12 are essentially the same in both types of meat. Comparisons of skin-on with skin-off chicken products show that fat levels are higher in skin-on products, with the fatty acid prole staying relatively constant. In addition to low saturated fat levels,

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cholesterol in poultry products is very low, ranging from 53 to 79 mg per 85.1 g portion [6]. There is no recommended intake of cholesterol, as it is synthesized by the body. However, in certain populations, dietary intake of cholesterol can adversely inuence health [6]. To compare with cholesterol levels in other meat products, lean beef and pork cuts contain 75 mg, beef liver contains 310 mg, and kidney contains 540 mg per 85.1 g sample [6]. With moderate intake of any meat product, cholesterol levels in the plasma should not be inuenced.

B. INGREDIENTS ADDED

TO

POULTRY PRODUCTS

The ingredients added to poultry products during further processing can affect the nutritional value of the product. Typically, these ingredients are not included at levels that would be likely to signicantly reduce the nutritional value of the product. An example of a potentially harmful ingredient is salt [6]. Although sodium and chlorine are essential nutrients, the overconsumption of table salt has been linked to an increased incidence of high blood pressure. Although salt added to further processed products will add to dietary salt intake, it is unlikely that enough poultry products will be consumed to adversely affect the health of the consumer. Other ingredients, such as sodium triphosphate, may also contribute to the overall intake of sodium. Interestingly, the addition of certain nutrients to the chicken feed can increase the level of those nutrients in the meat and inuence both nutritional value and shelf life. Examples of these nutrients are vitamin E, specic fatty acids, and ascorbic acid [7]. Many of the ingredients used to alter the texture or water-holding ability of the product are comprised of starches or proteins. Although it was mentioned earlier that the protein requirement for the standard adult was exceeded by an 85.1 g serving of chicken, the additional protein and starch may be of nutritional benet and certainly will not cause harm. Organic acids that are added to the food are a source of energy, as well as a preservative, and will be of nutritional value to the consumer. Many of the ingredients that perform enzymatic functions are likely of no nutritional value.

C. PROTEINS
Freezing may induce some protein denaturation, as evidenced by research on freezing rates, structural changes, and drip losses. However, changes in digestibility and nutritive value of proteins, even in denatured form, are very slight and appear to be of no practical signicance. The drip losses that occur during thawing and cooking can include water-soluble protein, vitamins, and minerals, but the amount lost relative to that remaining is small. Vitamin B is among the most labile nutritive components, and evidence exists that thawing and cooking may lead to signicant losses of vitamin B6, but the losses are produced largely by the subsequent thawing and cooking treatments rather than by freezing.

III. QUALITY OF POULTRY PRODUCTS

The concept of quality may be dened differently by those producing the meat than those consuming it. For the purposes of this chapter, quality will be dened by the color, texture, and tenderness of the product, the factors that most closely determine the perception of product quality. The safety of the product will be discussed subsequently. All steps of the production and processing of the meat, beginning with the transport of poultry and ending with the shipment of a consumable product, affect the quality of frozen poultry and poultry products.

A. FREEZING, PACKAGING, AND THAWING

Ideally, poultry products are frozen immediately after fabrication and held at 2 17.8 to 2 28.98C and at approximately 85% relative humidity and retain product quality for 6 10 months [8].

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Quality is maintained at temperatures below 2 108C because most microbial growth, biochemical activities, and enzymatic activities are reduced to almost zero due to the xture of cellular water molecules in a crystalline structure [9]. However, appearance and palatability are inuenced by the rate of freezing, temperature, and duration of storage, packaging, and handling during and after thawing. Rapid freezing rates produce small ice crystals and result in a higher quality product. Reduced freezing rates permit larger ice crystal formation, which results in decreased product quality due to the destruction of protein structure in the muscle cell. In addition, poor or improper packaging will not protect the product surface from excessive drying and will result in freezer burn [8,9]. Lipid oxidation is a concern in certain products due to the resulting rancid off-avors and odors but can be controlled with antioxidants and modied atmosphere packaging [10]. Proper product thawing procedures will prevent excess purge loss and reduce the risk of microbial growth. Retaining the product in the original package after thawing will prevent dehydration and drip loss. Refreezing the previously frozen products is not recommended because it drastically reduces quality and safety, causing loss of proteins, avor, juiciness, excess drip, and increasing the likelihood of microbial growth and product deterioration [8].

B. FROZEN POULTRY PRODUCT QUALITY

DURING

STORAGE

The quality of frozen poultry meat may be affected by storage in a number of ways. The carcasses themselves may deteriorate externally due to dehydration, which causes the loss of the natural soft glossy appearance of the poultry meat. Additionally, with the absence of this moisture may come the hydrolysis or oxidation of the fat and protein not only on the surface of the meat but within it as well. As these things take place, the palatability of the cooked product suffers and the eating quality is subsequently lowered. A study published as early as 1941 by the USDA [11] recognizes these effects in the quality of frozen poultry. The trend seen at this time was in contrast to the previous years. Prior to 1925, poultry carcasses were stored at temperatures typically below 108C. As more was known about the process of freezing poultry, these temperatures tended to get lower. Processors began to store these carcasses below 08C and, more commonly, near 2 208C. In the 3-year study conducted by Harshaw for the USDA [11], it was found that the poultry stored at the lower temperatures (2 208C) tended to lose less weight from dehydration. Additionally, the colder carcasses also tended to have a lower incidence of off-avors. It is also interesting to note that in the experiment, half of the birds stored were quartered. It was found that at equally low temperatures, the quartered birds lost more weight, especially with time. This result certainly makes logical sense, as the quartered birds would have a higher surface area and thus a higher likelihood of losing moisture. This perhaps shed insight into the ideal method of storing carcasses for longer periods of time in the future. In addition, worthy of note in this experiment was the absence of quick chilling by freezing the carcasses. The time that it takes to reach the desired frozen temperature had not yet been addressed. As it became more apparent to researchers that dehydration or drip loss during thawing was at the top of the list of concerns for frozen poultry, the next step was to attempt to prevent this phenomenon. As it is understood with the physical action of freezing a meat product, the water within the tissues begins to form crystals. With a slower freezing comes a larger crystal. The faster the freezing takes place, the smaller the ice crystals. The crystal is of concern because as it forms, it punctures the cells in the tissue. As the product thaws, the water that was within the cell is lost, which we refer to as drip loss. Therefore, the rst step in attempting to retain moisture within the product is to hasten the freezing process. The addition of nonmeat ingredients was the next logical step in attempting to retain moisture in the meat product. A study conducted by Yoon [12] examined the effect of the addition of phosphate to the product to retain water. Phosphate has been used for many years to improve the quality of

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nished poultry products and to provide greater processing exibility. The addition of trisodium phosphate not only improves water binding, texture, color, and avor [13], but it also has an antimicrobial effect [14]. The Yoon study concluded that no signicant texture toughening was observed in frozen chicken breasts after 10 months of storage at frozen temperature regardless of treatment. This suggests that toughening is not a determinant factor in the quality loss of frozen chicken breasts. Instead, improving water-binding ability of chicken meat without the ice crystal formation during frozen storage is most important for preserving the eating quality of frozen chicken breasts. This result can be accomplished by treating chicken breasts with 10% trisodium phosphate or STPP before frozen storage. In further research, it has been shown that there has been actually less drip loss from carcasses that have been stimulated before harvest and then treated with a phosphate solution before freezing. This is due to the interaction with the pH decline that takes place naturally as a part of rigor mortis. A study conducted by Young and Buhr [15] went one step further in attempting to observe this phenomenon. In this study, the carcasses were slaughtered, and the breasts were harvested 1 h postmortem. They were then treated with a phosphate solution and frozen. The difference in this study was that the carcasses were exposed to electrical stimulation in the slaughter process so as to rapidly decrease the pH. In the study, electrical stimulation had no direct effect on pH, cooking loss, or shear values, whereas polyphosphate increased pH and decreased cooking loss. Polyphosphate treatment caused llets from unstimulated carcasses to absorb more marinade and yielded more drip than those from stimulated carcasses. Fillets from stimulated carcasses marinated in NaCl solution without polyphosphate yielded less drip than those from unstimulated carcasses [15]. It becomes evident that to alter the capacity of the meat to retain water, it is important to remember the natural physiology and biochemistry of the meat as it passes through the rigor process. Freezing may trigger a moisture loss; however, there are mechanisms within the meat that can indeed hinder this from occurring. Phosphate solution has certainly been the most popular and explored additive to improve the quality of frozen or fresh poultry products. There have been, however, other means of altering poultry quality that have been explored as well. For example, the addition of dietary tea catechins as an effect on broiler quality in the fresh or frozen state was explored [6]. The study showed that the dietary catechins inhibited lipid oxidation in long term frozen stored chicken. In another study [7], the effect of selenium, vitamin E, and ethoxyquin on lipid peroxidation was explored. It was found that dietary selenium and other factors affecting selenium status may be useful in retarding the development of oxidative rancidity in frozen poultry products. Regardless of the approach that the researcher takes, whether it is to treat the product after harvest or to alter the dietary intake of the bird before harvest, it is apparent that many avenues have been explored to nd a method to keep the quality integrity of the frozen poultry product. When considering frozen poultry, a widely overlooked aspect of the product quality discussion is the means in which it is thawed or cooked. Keeping in mind that the consumer ultimately desires a product that is convenient and quick to prepare, research does indeed need to reect this goal. Younathan et al. [16] had this concept in mind when they set out to determine the effect of microwave energy as a rapid thawing method for frozen poultry. There has been tremendous growth in recent years in the use of the microwave oven for practically every aspect of meal preparation. Samples in this study were frozen in a similar fashion and then thawed using a microwave oven. The samples were then compared to samples thawed overnight in a refrigerator. Microwave defrosting of frozen breasts resulted in a slightly more tender product. However, the breasts that were thawed in the microwave experienced more drip loss. Hence, it can be seen that this widely used means of preparing poultry has a mixed effect on the quality of the meat. While preserving tenderness, it actually loses moisture.

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1. Carcass Changes during Storage Fast freezing results in lighter colored carcasses than slow-frozen poultry. During slow freezing, the skin dries, shrinks, and becomes more transparent and, as a result, has a darker appearance than if the same carcass were frozen rapidly. Light-colored frozen carcasses are generally considered to be more desirable than dark-colored ones. During slow freezing, large ice crystals are formed with a resulting transparent surface layer and a darker appearance on the surface of the frozen carcass. A major portion of the darkening takes place in the skin and the remainder in the surface layer of the esh. The rate of freezing of the esh below the surface has no effect on the surface color. Although well-nished carcasses are desirable, fat acts as an insulator and retards the freezing rate regardless of freezing method. Research reported that when carcasses were held for 6 24 h before freezing, the breast muscles were tendered than those of fryers held only 40 min before freezing. In addition, turkey carcasses held for 1 h and then frozen at 2 2.88C (278F) for 3 days provided adequate tenderization and no adverse avor changes were observed after 14 days at 2 2.88C (278F). When the birds were frozen before the onset of rigor, wide differences in the rate of thawing did not adversely affect tenderness. 2. Bone Darkening during Storage It is known that chilling before freezing will not prevent bone darkening. However, storing at temperatures below 2 9.48C (158F) lowers or prevents bone darkening entirely. This is caused by the leaching of hemoglobin from bone marrow to adjacent muscle as result of the freeze or thaw treatment. Leaching only occurs in the carcasses from relatively young birds because the bones are not completely calcied and are more porous than in mature birds. Although product quality does not change, the appearance constitutes a negative factor in consumer acceptance. Many attempts have been made to eliminate bone darkening in young frozen birds. Although some reduction can be achieved, only removing the bone marrow or cooking before freezing will eliminate this defect. 3. Palatability Changes during Storage Palatability changes are the most critical for producers because of the need to ultimately provide consumers with a pleasurable eating experience. Palatability differences in poultry resulting from freezing treatments are often reported as small or nonexistent. When several freezing rates were compared, it was found that surface color differed, whereas cooking yields or palatability differences were not found. Similarly, no difference in tenderness was found for chicken breasts frozen at temperatures from 2 18 to 2 688C. 4. Protein Changes during Storage Some protein denaturation and solubility changes are known to occur as a result of freezing, but the practical signicance of these changes is not clear. Comparisons of thermal gelation properties of poultry dark meat frozen at different rates showed little effects of freezing or freezing rates on rheology or gel strength. Freezing, regardless of rate, resulted in somewhat greater waterholding capacity, which might be caused by increasing charged sites on the meat proteins. However, freezing does not appear to be a major detriment to processing functionality of poultry meat.

C. INTRINSIC CHEMICAL REACTIONS

The chemical reactions of greatest concern with frozen poultry, those involving lipid oxidation, constitute a major determinant of frozen product shelf life, because poultry lipids are relatively unsaturated and susceptibility to oxidation is high. Freezing results in concentration of solutes, which catalyzes the initiation of oxidative reactions. The greater the concentration of these

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catalysts, the greater the acceleration of changes. Freezing also disrupts and dehydrates cell membranes, exposing membrane phospholipids to oxidation. 1. Protein Denaturation Chemical reactions during freezing and frozen storage may also contribute to some protein denaturation and decreased solubility. Decreases in sulfhydryl groups and ATPase activity occur during frozen storage and are indicative of protein changes. Peptides and amino acids are also increased in the drip uid, as are nucleic acids, indicating protein changes and structural cellular damage, respectively. 2. Enzyme Activity Biochemical reactions involving muscle enzymes may occur at very slow rates in frozen poultry, depending on storage temperature. For example, glycolysis may continue if not completed before freezing and may reach completion if enough time is available. Phosphatase activity is not completely inhibited by frozen storage. Muscle ATPase activity may continue during frozen storage, and some proteolytic enzyme activity has been suggested.

D. THE CONCERN

FOR

QUALITY AND CONSUMER ACCEPTANCE

Poultry genetics, particularly for broiler chickens, does not contribute to much variability in quality. Diets of live birds generally do not inuence meat quality, with the exception of the wellrecognized effect of highly unsaturated oils such as sh oils. A possible positive contribution of dietary factors may come from vitamin E (tocopherol), which has been shown to be effective in frozen and frozen or thawed beef for improving color stability and reducing oxidative changes. Similar effects of tocopherol have been observed in poultry for suppressing lipid oxidation. Although the implementation of innovative intervention strategies are necessary in the processing plant to improve storage stability and safety, they are worthless if the desired palatability and organoleptic attributes including avor, texture, color, and odor are compromised. 1. Preservatives There are many antimicrobial products that may be incorporated into poultry products to increase shelf life and prevent spoilage. Salt can be added to reduce the water activity of the product and reduce the water available for the microbes to use in metabolic processes. Salt alone, however, must be added at 15% to completely prevent microbial growth [17]. This level of salt is generally not acceptable for most products, which precludes the use of salt alone as a preservative. Sodium nitrite may, as well, be used as a preservative [17 19]. The USDA has strict regulations regarding the use of nitrite in food products [17]. This is due to the potential toxic effects of nitrite itself and of nitrosamine, the product of a reaction between nitrite and amino acids when subject to high temperature. Owing to the potential formation of nitrosamines, an antioxidant must also be incorporated into the product to ensure that NO2 is reduced to NO. This prevents any reaction with amino acids and the formation of nitrosamines. 2. Acidulants Sodium acetate, sodium diacetate, and lactate have also been used in poultry products to reduce microbial growth. These products act as acidulants and may be incorporated at levels of 0.25% [18]. These organic acids are also commonly used in carcass rinses and chiller water to control microbial growth without incurring the avor-altering effects of chlorine. Owing to their acidic nature, the organic acids also alter the avor of the product, but most often the acidic avor is desirable in the products in which they are used.

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3. Antioxidants Antioxidants can be used to preserve the product in terms of preventing lipid oxidation. Many compounds, most commonly butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT), can be incorporated into the product [18,20]. Antioxidants are particularly important in frozen poultry products, as the rate of lipid oxidation usually determines shelf life [20]. Liquid smoke products also provide antioxidant and antimicrobial action due to the phenols that they contain. Additionally, alpha-tocopherol and ascorbic acid (vitamins E and C, respectively) can be added to the product as antioxidants. Ascorbic acid is thought to chelate iron, which is a catalyst for oxidative pathways [18]. These compounds are fat-soluble and function to quench free radicals that are the main cause of lipid oxidation. Off-avors and rancid odors that result from lipid oxidation are often indications of impending microbial spoilage [17]. Delaying the onset of lipid oxidation can improve the shelf life of the product. The list of ingredients discussed here is by no means exhaustive. Topics such as spices and avors have been omitted entirely due to space considerations and the length of their potential discussions. There is a long list of ingredients that can be used to improve the water-binding ability of poultry products. Ingredients such as salt and phosphates are commonly injected into whole meat products as part of a marinade and function to increase water binding and retention of the marinade. Other products, such as the plant protein and starch ingredients described, are more useful in further processed products. The texture and water-binding properties of further processed products can be manipulated through an innite number of combinations of the various ingredients. Careful consideration must be taken when choosing an ingredient or set of ingredients for a given product. Several antimicrobial products are also available for incorporation into poultry products. The use level of these products may be controlled by the USDA, and careful control of their incorporation and the choice of preservatives must be implemented. 4. Stability and Acceptability The important factors in determining stability and acceptability are those that inuence oxidative and organoleptic change. As discussed previously, the amount of unsaturated lipids and the oxidative or antioxidant environment surrounding membrane phospholipids are major factors. In addition, important processes are treatments such as cooking, which initiate oxidative change and decrease practical frozen storage life by about 50%. Addition of salt as well as chopping or grinding also greatly shortens frozen storage life. The effects of packaging are critical. High barrier vacuum nearly doubles storage life in most cases when compared with a low-barrier polyethylene lm. The nal major determinant is storage temperature. In general, intact poultry carcasses and cuts will remain acceptable for at least 12 months if they are well packaged and held at 2 188C. Lowering storage temperature increases stability. Thus, 24 months of acceptability may be expected with temperatures of 2 258C or less. Cooked poultry products such as fried chicken may be expected to have a practical storage life of 6 9 months or more at 2 308C. The stability of the frozen products can be summarized as dependent on the product characteristics, the processes used for the product, and the packaging system chosen.

E. PROTECTING

THE

QUALITY OF FROZEN POULTRY

Product quality can be dened using many factors including appearance, yields, eating characteristics, and microbial characteristics. The objective of the freezing process is to preserve product characteristics at a desirable level as long as possible. The use of high-quality initial materials is essential to high-quality frozen products. The USDA inspects each bird for wholesomeness and tness for consumption and also grades ready-to-cook carcasses as A, B, or C quality. Determinants of these grade levels are conformation, eshing fat cover, pinfeathers, and defects such as exposed

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esh, discoloration, or broken bones. Freezing effects are also considered; a freezing defects category is used, with darkening, pockmarks, or freezer burn resulting in lower grades. 1. Product Processing Slaughter, processing, and handling can affect carcass quality by inducing bruises, tears, or even broken bones. Most of these defects will be obvious and result in downgrading. Following slaughter and evisceration, rapid and well-controlled chilling of poultry carcasses is essential to maintaining microbiological quality and tenderness. It is undesirable to freeze poultry meat immediately following slaughter, as meat tenderness is likely to be decreased. Electrical stimulation of carcasses can be used to speed up postmortem tenderization if deemed necessary. Poultry must be chilled to a temperature of 48C or less within a time limit depending on carcass weight. A large majority of poultry carcasses are chilled in ice water slush because of relatively fast chilling and because some moisture is absorbed by the carcasses, thereby increasing yields. Maximum tolerances based on carcass weight for absorbed moisture have been established by the USDA and range from 4.3% for heavy turkeys to 8% for lightweight chickens. The absorbed water is signicant to the freezing process because it can inuence freezing rate and the extent of ice crystal formation. This excess moisture must be drained away before packaging and freezing to prevent excessive drip or separated water from occurring during thawing. The second and perhaps more critical consideration for freezing is that adequate time before freezing must be given for the meat to achieve optimum tenderness (6 8 h for chickens and 12 24 h for turkeys). Product preparation before freezing may include cutting, deboning, slicing, and other operations to provide greater convenience. Preparation of products by cooking before freezing is becoming increasingly more popular as a greater variety of poultry products, including breaded and fried portions, cured and smoked products, and items in marinades or broths, are offered to consumers. Poultry products, according to the USDA Food Safety Inspection Service, must be either raw or fully cooked before freezing. Fully cooked means that an internal temperature of 718C for uncured products or 688C for cured products must be reached. Breaded products such as patties may be fried to set the breading without further cooking of the product. 2. Product Packaging Following product preparation, packaging requirements become a consideration. Packaging is one of the most important factors in maintaining quality during frozen storage and is especially important for cooked products. Most important are protection from exposure to oxygen and from loss of moisture. As a result, packaging must provide a good barrier to oxygen, to prevent off-avor development, to moisture, to avoid dehydration or freezer burn. It has been suggested that the packaging system is of paramount importance to the quality of frozen products and of even greater importance than the freezing treatment itself because the stability of the product during storage is dependent on the protection provided by the package. Use of PPP (product, process, and packaging) concepts has been suggested to be the most important overall consideration for frozen product quality. 3. Product Storage Poultry and poultry products are frequently frozen to achieve long-term storage with minimal loss of quality. Poultry accommodates freezing treatments relatively well, and the quality level at the time of freezing can be maintained as long as the freezing process and storage conditions are adequate. Research on frozen poultry generally indicates that a storage temperature of about 2 188C or lower will minimize deterioration if products are well packaged and temperature uctuation is minimal. Over a range of 2 10 to 2 308C, a reduction of 108C in storage will apparently double or triple the number of days that broilers retain stability and acceptability. Storage needs to be at

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2 188C or less, using an appropriate high-barrier package with minimal temperature change during the storage period.

IV. SAFETY OF POULTRY PRODUCTS

In recent years, the safety of food has received an increasing amount of attention. Internationally, a Hazard Analysis and Critical Control Point (HACCP) process for the production of food has been adopted. Poultry products are no exception. The presence of physical, biological, or chemical hazards in poultry products pose health risks to the consumer and economic risks to the company. The production of wholesome, unadulterated poultry products is essential to maintain public health and to maintain product condence. Although biological hazards are the most prevalent and dangerous of the hazards, chemical and physical hazards must also be considered in designing a HACCP plan designed to minimize these hazards. Biological hazards have received the most attention in the literature relating to poultry products. Salmonella and Campylobacter contamination remain signicant concerns in the poultry industry. Physical hazards are also a signicant concern in the poultry industry, although the consequences of adulteration are generally lower than for biological hazards. Chemical hazards have a low prevalence in the industry and will remain low due to sanitation standard operating procedures (SSOPs) and HACCP plans.

A. CONCERN

FOR

FOOD SAFETY AND QUALITY

According to the Centers for Disease Control and Prevention, 76 million illnesses, 325,000 hospitalizations, and 5200 deaths related to foodborne illness occur in the United States each year. Of these statistics, known pathogens account for an estimated 14 million illnesses, 60,000 hospitalizations, and 1800 deaths annually [21]. Consequently, the estimated annual costs of human foodborne illness in the United States range from $8.5 billion to $20 billion [22]. Mead et al. [23] reported that nearly 2.4 million cases are caused by Campylobacter spp., 1.4 million cases are caused by nontyphoidal Salmonella serovars, and 270,000 cases are caused by pathogenic Escherichia coli including E. coli O157:H7. Unfortunately, for the poultry industry, poultry and poultry products have been implicated as a major source of Campylobacter and Salmonella infections in humans [24]. A recent study conducted by Zhao et al. [25] demonstrated the prevalence of Campylobacter spp., S. serovars, and E. coli in raw retail meats, including chicken and turkey products, obtained from four supermarket chains in the greater Washington, D.C. area over a 14-month period. The majority (70.7%) of chicken samples (n 184) were positive for Campylobacter, 38.7% of the chicken samples (n 212) were positive for E. coli, and only 4.2% of the chicken samples were positive for Salmonella. As a result of their ndings, Zhao et al. [25] suggest focusing on effective prevention strategies such as implementing on-farm practices that reduce pathogen contamination, increasing hygiene in both slaughter and meat processing, continuing implementation of HACCP systems, and increasing consumer education efforts to reduce the presence of foodborne bacterial pathogens in meat products at the retail level. Understanding that multiple entry points exist for contamination of poultry during various phases of the growth period and processing procedures is required to develop multifaceted intervention guidelines to successfully control contamination. Although product quality is certainly an important factor when considering frozen poultry, there is also the consideration of microbiological spoilage or even pathogenic effects. As mentioned earlier, consumers eat with their eyes, and thus any type of off-condition will affect eating experience. Dehydration can alter the external appearance of the poultry so can microbiological growth. Product safety is also at the top of the list of priorities that the modern consumer has. With the stress that producers have on biosecurity coupled to a history of food recalls, the microbiology of food products is very important.

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The misconception of the common consumer is that the food is safe if it has been frozen. This is perhaps the most dangerous mistake that an individual can make. As we have come to nd through research, a number of organisms grow in refrigerated and even frozen temperatures. Thus, it is crucial that processors who are looking to produce frozen poultry do not neglect the microbial safety of their product. Perhaps, the only thing more important to understand that microbes can grow in frozen conditions is knowing what type of organisms can grow under this condition. A study conducted by Norberg [26] in 1981 set out to determine just what are the organisms growing in frozen poultry. It is the conception of the public and even some food scientists that Salmonella sp. is the only organism of concern in poultry. This impression is reinforced by the idea that very little growth of any organism occurs in frozen poultry. The study [26] concluded that this was certainly not the case. The investigation showed that frozen chicken does contain other pathogenic bacteria than Salmonellae. Namely, Campylobacter and Yersinia enterocolitica were isolated in much higher frequency. C. jejuni was found in 22% of the samples, Y. enterocolitica was found in 24.5% of the samples, and S. typhimurium was found in one sample. Aerobic plate counts (APCs) and numbers of coliform bacteria at 378C were not found to be noticeably higher in samples containing pathogens than in pathogen-free samples.

B. PREVENTIVE MEASURES

IN THE

PROCESSING PLANT

In addition to the existing critical control points, which include proper equipment maintenance, product and washer temperature controls, water replacements, and counter-ow technology in the scalder and chiller, chemical intervention strategies have been implemented in the processing plant to control foodborne pathogens [27]. These methods include phosphate dips or sprays (e.g., trisodium phosphate and polyphosphates), ionizing radiation, ozonation, and organic acid sprays to reduce the numbers of bacterial pathogens present on raw animal products. 1. Phosphate Treatments Trisodium phosphate (TSP) is a GRAS product approved in 1992 by the U.S. Department of Agriculture and can be used as a dip or a spray [28]. Several concurring studies proved that TSP is active against gram-negative bacteria, including salmonellae, coliforms, E. coli O157:H7, campylobacters, and pseudomonads on the skin of chicken carcasses [28 30]. It is anticipated that the antimicrobial mechanisms of TSP include (a) exposing microorganisms to high pH, which would affect cell membrane components; (b) enhancing detachment of bacteria from food surfaces by sequestration of metal ions; and (c) removing fat from the skin surface, thereby allowing bacteria to be more effectively washed from the food surface. Recently, Sampathkumar et al. [30] demonstrated the efcacy of high pH during TSP treatments against S. enterica serovar enteritidis. The process involved immersing postchill whole birds for 15 sec in a 10% solution of Av-Gard TSP and then allowing the excess TSP solution to drip from the bird. Subsequent microbiological testing demonstrated the effectiveness of TSP treatments and the pH concentrations adjusted to pH 11.0 0.2. Both tests resulted in the loss of cell viability and membrane integrity, demonstrating that alkaline pH treatments permeabilize and disrupt the cytoplasmic and outer membranes of serovar enteritidis cells, instigating the release of intracellular contents and eventually causing cell death [30]. 2. Chlorine Compounds Chlorine is commonly used in poultry processing facilities at levels less than 50 ppm in the immersion chillers to facilitate the reduction of bacterial contaminants. The efcacy of chlorine decreases as pH, organic load, temperature, bacterial concentrations, and trace minerals change in the same environment. Acidied sodium chlorite (SanovaR) is a mixture of sodium chlorite and citric acid and results in an effectively low pH antimicrobial spray product. SanovaR is effective against E. coli, Salmonella, Listeria, Campylobacter, and other potential bacterial contaminants [31].

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3. Ozonation Ozone is a soluble and unstable blue gas commercially produced by passing electric charges or ionizing radiation through air or oxygen. The powerful compound is used to inactivate bacteria through its oxidizing properties. Ozonation is effective against bacteria including E. coli O157:H7, S. typhimurium, and Pseudomonas uorescens on muscle foods [31]. 4. Organic Acid Treatments Many antimicrobial sprays have been formulated and applied with inside or outside bird washers in attempts to reduce bacterial contamination of prechilled chicken carcasses. Lactic acid has been a popular treatment applied at 1 and 2% levels. Yang et al. [32] found that a 2% lactic acid treatment was effective to reduce total aerobes by 1.03 log 10 CFU per carcass. However, this treatment caused slight chicken skin discoloration. Xiong et al. [33] also evaluated the effectiveness of a lactic acid prechill spray to reduce S. typhimurium attachment on chicken skin and found that a 1 2% lactic acid spray resulted in a 2.2 log 10 CFU per carcass reduction [33]. Subsequent research by Okolocha and Ellerbroek [34] reported that a 1% lactic acid dip (PuracR) was more effective than a spray, which resulted in a 0.6 log 10 CFU/ml APCs reduction, a 1.1 log 10 CFU/ml Enterobacteriaceae reduction, a 0.4 log 10 CFU/ml Lactobacillus reduction, and a 0.4 log 10 CFU/ml Pseudomonas reduction. Glutamal bioactiveR, a 1% formulation of active constituents (sugars, foodstuff phosphates, ascorbic/isoascorbic acid, or their inorganic salts) with lactic acid as an activator, was also more effective as a dip than a spray. Glutamal bioactiveR resulted in a 1.0 log 10 CFU/ml APC reduction, a 0.9 log 10 CFU/ml Enterobacteriaceae reduction, a 0.2 log 10 CFU/ml Lactobacillus reduction, and a 0.2 log 10 CFU/ml Pseudomonas reduction. Overall, both PuracR and Glutamal bioactiveR products effectively reduced original pathogen loads and received high acceptability scores by consumers [34]. 5. Hot Wash Treatments Recently, Purnell et al. [35] investigated the use of hot water immersion treatments to sufciently reduce bacterial numbers during processing. The hot water immersion treatments were located after the inside or outside wash cabinets and were conducted following suitable time temperature parameters previously determined. Purnell et al. [35] concluded that a heat treatment at 758C for 30 sec signicantly reduced levels of Campylobacter, Enterobacteriacae, and APC but resulted in unacceptable grades due to epidermis damage or skin tears during packaging positioning. However, at 708C for 40 sec heat treatment resulted in both reduced bacterial levels and acceptable grades relating to surface appearance [35]. 6. Temperature Treatments Varying temperature treatment studies have reported that freezing food inactivates substantial populations of C. jejuni by . 2 log 10 CFU/g [36,37]. The detrimental mechanisms of freezing and thawing to living cells is due to cell injury attributed to ice nucleation and dehydration. Oxidative damage to cells has also been implicated as a mechanism contributing to freeze thaw injury, resulting from an oxidative burst occurring within cells during thawing [38]. Zhao et al. [39] conducted several trials to determine the inactivation rates of C. jejuni on poultry exposed to short-term and long-term freezing at different temperatures and after superchilling to an internal temperature of 2 3.38C. All samples were contained in Whirl-Pak bags. Long-term holding for 812 weeks at 2 208C resulted in a 3 log 10 CFU/g reduction when compared with short-term freezing for 72 h or less at 2 208C, which resulted in a 1.7 log 10 CFU/g reduction. Superchilling only resulted in signicant bacterial reductions at 2 1968C for 20 sec. The 2 1968C for 20 sec temperature treatment may have been inuenced by the technique because to reach the desired temperature, submersion of the samples into liquid nitrogen was required. This technique is not likely to occur during commercial processing. The remaining superchilling temperatures at 2 808C for 330 sec,
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2 1208C for 220 sec, and 2 1608C for 150 sec involved sample exposure to vapor-state liquid nitrogen. Therefore, the study concluded that the superchilling conditions utilized by the poultry industry are not adequate to substantially reduce Campylobacter populations on fresh products [39].

V. CONCLUSIONS
As has been illustrated, there has been a tremendous effort for the innovation of the frozen poultry market. There will be certainly an equal or greater push to understand the many facets of producing this product in a premium condition. With the prole of the modern consumer, the frozen poultry market will certainly continue to thrive. The need for convenience and ease of preparation will continue to be a top priority for consumers in the modern market. However, the problems that are typically associated with frozen poultry must be dealt with to produce frozen poultry in an economical and safe way. Research thus far has certainly attempted to address these problems. In the future, there will continue to be a need for research dealing with frozen poultry. It is a relevant topic, and one that will continue to furnish abundant research endeavors. Intervention strategies protecting product quality and safety are vital during processing and are critical to subsequent steps including freezing and thawing. In addition to implementing intervention strategies, proper employee training, and consumer education are also key in the farm-to-fork approach. Most importantly, education is critical to reduce the incidence of foodborne illness. Education complements regulatory and research activities and instills responsibility for food safety in everyone involved.

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