V Perishable, cooked poultry products

A wide variety of perishable cooked ready-to-eat poultry products are available (Table 2.1), prepared by many different processes (Tompkin, 1986, 1995b; Acuff et al., 2001), but most involve three general processes. Whole carcass or part of it may be injected with a solution containing desired ingredients and then placed onto racks or into stockinettes for cooking. If desired, smoke is applied during cooking. These products may be frozen or refrigerated for distribution and sale.

Large, boneless products can be made by injecting the meat; tumbling or massaging to extract soluble protein; stufﬁng into a desired mold, casing, stockinet, or plastic barrier ﬁlm package; and then cooking. These products may be given additional treatments during or after cooking (e.g. smok- ing, caramel coating, oven browning, browning in hot oil, or applying spices or condiments). Some products are sliced and packaged. These products may be frozen or refrigerated for distribution and sale.

Cooked products consisting of ground poultry are usually made on continuous systems that involve grinding meat, adding other ingredients, forming to the desired size and shape, applying a batter and breading, cooking, freezing, and packaging. Large quantities of chicken parts (breasts, wings, drum- sticks) are cooked in oil on continuous systems, seasoned, frozen, and then packaged. Frozen cooked ground products and parts are normally distributed, frozen, and then thawed at the retail level and sold refrigerated. Some frozen cooked poultry products may be placed at refrigerated temperature for display and sale at the retail level.

A Effects of processing on microorganisms The microbial content of cooked products is inﬂuenced by the method of processing, packaging, and

storage (Denton and Gardner, 1982; Tompkin, 1986; Tompkin, 1995b; Acuff et al., 2001). All the products in this category should be cooked at a time and temperature to obtain a cooked appearance, appropriate tenderness, and other desirable organoleptic qualities. In addition, the processes should be adequate to ensure destruction of enteric pathogens. For example, in contrast to some beef products (e.g. ground beef patties, rare roast beef), thermal processes for cooked poultry products can be designed

and controlled to ensure the destruction of 10 7 salmonellae/g in the coldest area of the product and still

149 have acceptable organoleptic quality. Thermal processes of this nature should be more than adequate to

POULTRY PRODUCTS

destroy the levels of salmonellae, C. jejuni, L. monocytogenes, and Staph. aureus that normally occur in raw poultry meat. To achieve the organoleptic characteristics expected, poultry products are usually cooked more extensively than comparable beef products.

Vegetative bacteria and, perhaps, some spores on the surface of poultry products are killed during cooking, but some in the center of the product may survive depending on the thermal process (e.g. enterococci, Lactobacillus viridescens). The thermal processes are not adequate to assure destruction of sporeforming pathogens (Cl. perfringens, Cl. botulinum). Cooked products are subjected to post-process contamination during slicing and packaging.

Barbecued poultry is cooked on a grill or in a rotisserie often at temperatures below those used for baking poultry, but for longer periods of time. Microbial growth can occur if the cooked barbecued products become contaminated and stored for several hours at abnormal temperatures (Pivnick et al., 1968; Seligmann and Frank-Blum, 1974).

C or higher, which is lethal to vegetative bacteria but not spores. These products are also subject to post-process contamination during subsequent handling and packaging.

During the frying of chicken in oil, temperatures at the geometric center usually reach 93 ◦

B Spoilage Cooked poultry products that are stored, distributed, and displayed at refrigeration temperatures will

eventually spoil. The rate and type of microbial spoilage depends on how the product has been processed, packaged, and stored.

Products that are cured (i.e. contain sodium nitrite) often have higher salt and lower moisture and will generally spoil in the same manner as similar cured meats made of beef, pork, lamb, or veal (see Chapter 1). When exposed to the processing environment before final packaging, the spoilage flora is mixed. If oxygen is excluded, e.g. by vacuum or modified atmosphere packaging, the spoilage flora often becomes dominated by lactic acid bacteria, such as Lactococcus, Carnobacterium, and Lactobacillus spp. (Barakat et al., 2000). In the absence of oxygen, these packaged products may develop a milky exudate; gassiness; and, if a fermentable carbohydrate has been added, sourness with decreased pH.

Many cooked breast meat products do not contain sodium nitrite. If these products become contaminated after cooking (e.g. during slicing) and packaged in the absence of oxygen, a substantial population of Gram-negative bacteria develops that includes a variety of species within the family Enterobacteriaceae. Spoilage is characterized by very strong offensive odors that may not be detected until the packages are opened. There is a potential for biogenic amine formation. This defect can be prevented by applying a shorter code date (e.g. days rather than weeks), reducing contamination through more effective GHP and/or by adding adequate levels of sodium lactate and/or sodium diacetate to the product. There have been reports that sodium lactate can delay botulinal toxin production in products of non-cured poultry products. At the level (e.g. 2% w/w) that is normally used to extend shelf-life, sodium lactate is of marginal value as an antibotulinal agent. There have been no reports of botulism from non-cured breast meat products, since they were moved from the frozen to refrigerated storage and distribution in the 1980s.

Cooked non-cured breast meat products are also cooked in an oxygen impermeable ﬁlm and then chilled. These cook-in-bag products have a relatively long shelf-life (e.g. >60 days) when stored at less than 4 ◦

C. Occasionally, spoilage occurs due to the growth of psychrotrophic sporeformers that survive the cooking process (Kalinowski and Tompkin, 1999; Meyer et al., 2003). Products of this type also may be frozen for storage and distribution.

Two other defects of microbial origin have been observed in cooked non-cured poultry products. Both can be due to microbial growth in the raw meat before cooking. One defect involves the formation

MICROORGANISMS IN FOODS 6

of small holes similar to those found in certain cheeses. This defect has been observed in products that have been injected and held for some time at refrigeration temperatures before cooking and is due to multiplication of certain bacteria (e.g. Aeromonas spp.) that can multiply at ≤10 ◦

C in breast muscle injected with a solution containing salt and phosphate. The holes are thought to be due to the production of carbon dioxide that is released from the meat and expands during cooking. Apart from the small holes in the cooked product, there is no other loss of quality. The products are otherwise normal in appearance and odor and do not contain recoverable microorganisms. This defect can be confused with small holes that develop when an excessive quantity of carbon dioxide in the form of dry ice (i.e. carbon dioxide in frozen, solid form) has been used to chill the meat at a step prior to cooking. Controlling the time and temperature of holding the raw meat prior to cooking prevents the defect. It is possible that the time-temperature factor after injecting the salt–phosphate solution may be important for two reasons. The injection process contaminates the interior of the meat and, perhaps, certain ingredients play a role.

The second defect is a pink discoloration throughout the interior of the product. There are several potential causes for the development of a pink color in cooked non-cured poultry breast meat (Cornforth, 1991; Cornforth et al., 1998; Schwarz et al., 1999). One involves the reduction of nitrate in processing water to nitrite, by the microbial ﬂora of raw poultry meat. The best means to prevent this cause of pink discoloration is to remove nitrate from the water. Pink discoloration of microbial origin in cook- in-bag breast products can be due to the growth of psychrotrophic clostridia. In addition to the pink discoloration, a strong hydrogen sulﬁde odor is produced. Since no gas is produced, the product in the package appears normal until opening. The combined offensive odor and internal pinkness results in product rejection (Kalinowski and Tompkin, 1999; Meyer et al., 2003).

C Pathogens Certain microbial pathogens should be considered in a hazard analysis for the production and use of

perishable cooked poultry products. Salmonellae present on raw poultry meat can survive as a result of undercooking or contaminate products that are exposed to the processing environment and handled before ﬁnal packaging. Proper controls for cooking can prevent survival of salmonellae. Likewise, proper layout of the production facility to separate raw meat processing areas from cooking, chilling, storing, and packaging areas can virtually eliminate the risk of recontamination by salmonellae. This is evident from two extensive surveys conducted at manufacturing plants. During an extensive survey involving 6 606 analyses of cooked poultry products collected over four years from processing plants in the United States, only four analyses were positive for salmonellae (Green, 1993). Ready-to-eat meat and poultry products sampled at manufacturing plants for regulatory compliance during the years 2001 and 2002 yielded only 23 samples positive for salmonellae in over 14 000 tested (USDA-FSIS, 2003). The few positive products could have been prevented through effective application of GHP and HACCP principles (Simonsen et al., 1987; ICMSF, 1988; Tompkin, 1990, 1994, 1995a,b).

The potential exists for food-borne illness from sporeforming pathogens (e.g. Cl. botulinum, Cl. perfringens) that survive the cooking of perishable poultry products. Food-borne illness from these anaerobic pathogens could occur only after raw poultry is cooked and then held at >10 ◦ C (Cl. botulinum) or >15 ◦

C (Cl. perfringens) for sufﬁcient time for extensive multiplication to occur. Large numbers of vegetative cells of Cl. perfringens (≥10 7 ) must be consumed for illness to occur (Brynestad and Granum, 2002). The number of Cl. perfringens spores present after cooking meat and poultry products in commercial operations are typically below detectable levels (Kalinowski et al., 2003; Taormina et al., 2003). There does not appear to be any documented evidence that Cl. perfringens food-borne illness has occurred with the commercially produced products that are likely to appear in international commerce. These products, however, have been implicated when they are mishandled at the user level (e.g. food-service, retailer, homes, institutional cooking). Historically, it has been at this level

151 that food-handling errors in storage times and temperatures have occurred and perishable ready-to-eat

POULTRY PRODUCTS

foods have been implicated in food-borne illness. For example, from 1970 to 1996, 94% of 1 525 of the reported outbreaks of Cl. perfringens illness in the UK were due to mishandling at the food-service level (Brett and Gilbert, 1997; Brett, 1998). A similar experience has been noted in Australia and Norway (Bates and Bodnaruk, 2003; Brynestad and Granum, 2002) and very likely represents the more common scenario for many other countries. Outbreaks attributed to Cl. perfringens have involved a wide variety of prepared foods, including large pieces of meat or poultry and others containing meat or poultry as one of many ingredients. The signiﬁcance of poultry meat as the source of Cl. perfringens in foods containing gravies, spices and other ingredients is not known. Cured meat or poultry products have rarely been implicated in Cl. perfringens illness. This should not be unexpected considering the relative sensitivity of Cl. perfringens to the combined effect of salt and sodium nitrite present in these products (Roberts and Derrick, 1978; Gibson and Roberts, 1986). There are conﬂicting views on the rate of chilling and what might be considered a tolerable level of Cl. perfringens (e.g. performance objective) in cooked poultry products manufactured in commercial establishments. Inoculated studies (Juneja and Marmer, 1996) suggest a need for greater caution and rapid chilling than manufacturing facilities generally have used historically but epidemiologic data and commercial experience do not support this conclusion (Kalinowski et al., 2003; Taormina et al., 2003). A risk assessment might help clarify this issue.

Contamination with Staph. aureus, usually at low levels, can occur during handling and packaging; however, proper refrigeration will prevent multiplication and the risk of enterotoxin production in these products. Staphylococcal food-borne illness is primarily associated with poultry products that are cooked and served in homes or food-service establishments where contamination occurs and the foods are then improperly held at higher temperatures for sufﬁcient time for enterotoxin production to occur. Almost all staphylococcal food-borne illness from poultry has been due to recontamination of cooked meat by a food handler rather than from the raw poultry (Bryan, 1968, 1980; Cox and Bailey, 1987; Mead, 1992).

The final group involves psychrotrophic pathogens that can establish themselves and multiply in the environment of manufacturing plants where operating temperatures for chilling and handling cooked products is too low for the growth of the above pathogens. In this group, only L. monocytogenes has been identified as a significant contaminant of commercially produced cooked poultry products. Surveys of cooked poultry products indicate that post-processing contamination can occur. For example, 12% of 527 cooked poultry products from retail stores were positive for L. monocytogenes (Gilbert et al., 1989). Cooked poultry products collected during the years 1990 through 1999 from manufacturing plants in the United States showed prevalence rates in the range of 1.0 –3.2% (Levine et al., 2001).

A survey of ready-to-eat sliced luncheon meat and poultry from retail stores found the prevalence rate among 9 199 samples was 0.89% (Gombas et al., 2003). Commercially manufactured ready-to- eat poultry products have been implicated in isolated cases and several large outbreaks of listeriosis (McLauchlin, 1991; CDC, 1999a,b, 2000, 2002; USDA-FSIS, 2002; Tompkin, 2002). The outbreaks involved persistent strains of L. monocytogenes that had become established in the manufacturing plant and contaminated the products between cooking and packaging. The existence of persistent strains in equipment and the environment in which ready-to-eat foods are exposed to contamination is a critical feature of this issue (Tompkin, 2002; Lundén et al., 2002; Autio et al., 2002; Berrang et al., 2002). A case control study in the Unite States identified undercooked chicken, presumably prepared in the home or food-service establishments, as a risk factor for human listeriosis (Schuchat et al., 1992). This and other reports of listeriosis attributed to a wide variety of ready-to-eat foods have led to modifications in industry practices (Tompkin et al., 1992; Tompkin, 1995a) and the establishment of regulatory requirements and standards for L. monocytogenes in ready-to-eat poultry products.

The FDA-FSIS risk assessment identiﬁed “deli meats” as the food group of highest risk for listeriosis in the USA (FDA-FSIS, 2003). This estimate was inﬂuenced by two major outbreaks involving non-cured

MICROORGANISMS IN FOODS 6

cooked turkey breast products that were sliced and sold through the deli counter of grocery stores. The combined data from the FDA-FSIS risk ranking of food groups and the FAO-WHO risk assessment for L. monocytogenes in ready-to-eat foods (FAO-WHO, 2004a,b) will inﬂuence national and international policies. Exporters should be aware of the regulatory requirements for each importing country.

The microbiological safety and quality of cooked products depend upon the use of GHP and HACCP to: (a) assure the use of a thermal process that destroys non-sporeforming pathogens; (b) control the chilling step to prevent the multiplication of mesophilic sporeforming pathogens; (c) prevent cross- contamination from raw meats to cooked product; (d) control the environment and handling of cooked products to minimize contamination with L. monocytogenes; (e) control storage and distribution times and temperatures to ensure microbiological safety and, where appropriate; and (f) provide food handling and preparation procedures to the end user (Tompkin, 1995b).

Three general approaches have evolved to help manage the risk of L. monocytogenes in those ready-to- eat poultry products that are stored and handled under conditions that permit growth. The first approach involves managing the manufacturing environment where cooked ready-to-eat products are exposed and subject to contamination. A considerable amount of information is being developed through research and experience that can be used to provide guidance on controlling L. monocytogenes in the environment (Tompkin et al., 1999). This is an evolving field with improvements being made in plant layout and construction, equipment design and procedures for cleaning and disinfection. In the second approach, research has identified additives (e.g. sodium lactate, sodium diacetate) that can be used to reduce, if not prevent, the growth of L. monocytogenes when stored at refrigeration temperatures (Seman et al., 2002).

A wider variety of additives than is currently available should be become available through research. The third approach is to treat products after ﬁnal packaging with a listericidal process (e.g. heat, ultra high pressure) before releasing the product for distribution (Muriana et al., 2002; Murphy and Berrang, 2002; Murphy et al., 2003a,b). A number of in-pack pasteurization systems are commercially available and used by producers of ready-to-eat poultry products in a variety of countries. As experience is gained with these systems improvements in functionality and reductions in production cost per package should lead to wider application of this approach.

V Perishable, cooked poultry products