Generic HACCP Application in Broiler Slaughter and Processing t

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1 579 Journal of Food Protection, Vol. 60, No.5, 1997, Pages Copyright, International Association of Milk, Food and Environmental Sanitarians General Interest Generic HACCP Application in Broiler Slaughter and Processing t NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS Ann Marie McNamara* Executive Secretariat, FSIS, Room 3175 South Building, Independence Avenue S. w., Washington, D.C , USA (MS# : Received 20 August 1996/ Accepted 24 December 1996) X. XI. OUTLINE I. Introduction II. Epidemiology A. Sources and limitations of data B. Outbreak data C. Sporadic case data D. Mechanisms of transmission and risk factors for foodbome pathogens associated with raw poultry III. Farm Management Practices A. Introduction B. Salmonella and Campylobacter IV. Microbiological Profile of Raw Chicken A. General microbiological parameters B. Effect of slaughter operations C. Potential for foodbome pathogens V. Hazard Analysis VI. Generic HACCP for Slaughter and Processing VII. Guidelines for Distribution, Retailing, and Preparation VIII. IX. Role of Regulators and Industry in a Broiler Processing HACCP System New Technologies and Improvements in Commercial Practices and Procedures Research Needs Appendices A. Good manufacturing practices for fresh broiler products B. General guidelines for the handling of raw chicken products in retail food stores and food service establishments C. General guidelines for the handling of raw chicken products by consumers * Author for correspondence. t Sponsored by U.S. Department of Agriculture, Food Safety and Inspection Service, U.S. Department of Health and Human Services, Food and Drug Administration; U.S. Department of Commerce, National Marine Fisheries Service; and the U.S. Department of Defense, Office of the Surgeon General, Committee Management. ABSTRACT The Meat and Poultry Working Group of the National Advisory Committee on Microbiological Criteria in Foods (NAC- MCF) has prepared a generic Hazard Analysis Critical Control Point (HACCP) plan for the slaughter and processing of raw broiler chickens. This report includes a review of existing scientific information, a hazard analysis, and use of this information to develop a generic HACCP plan that focuses on the microbiological safety of raw broiler products. This generic plan provides general guidance material for manufacturers to use in developing plantspecific plans. A brief discussion of the role of regulatory agencies and industry in HACCP is also presented. Key words: HACCP, Poultry, Farm, Processing INTRODUCTION The following generic Hazard Analysis Critical Control Point (HACCP) plan for raw broiler chickens focuses on the slaughter and processing portions of the total "farm to consumption" scope of a complete HACCP program. A broiler is defined as "a young chicken (usually under I3 weeks of age), of either sex, that is tender-meated with soft, pliable, smooth-textured skin and breastbone cartilage" (1). The consumption of all poultry products in the United States has increased dramatically over the last 20 years. In 1991, total broiler consumption was 63.6 Ibs, turkey and other ready to cook chicken was 19.8 Ibs, a total of 83.41bs of poultry consumed per person (3). In 1993, over 7.5 billion fertile hatching eggs were set with about 6.5 billion broilers grown in the U.S. Typically, a producer will have from two to six houses which will hold from 10,000 to 25,000 adult broilers. Time of grow-out is from six weeks for birds to be sold as whole processed broilers to eight weeks for birds to be cut up and further processed. To supply this large number of broiler chickens, production practices have changed significantly from the time most farmers had a few chickens in small backyard flocks. Integrators maintain breeder flocks and hatcheries to provide chicks for their contract growers,

2 580 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS and they own processing plants, fleets of transport trucks, and rendering plants. The Committee recognizes that animal production practices can be significant in controlling microorganisms out of concern for food safety. An overview of the key attributes of live animal management that significantly impact introduction or control of food borne pathogens relative to the ultimate microbiological safety of raw poultry products is included in Section III. Likewise, specific practices and procedures are required to ensure the microbiological integrity of poultry products while they are in distribution networks and during retailing. Improper handling of products in processing, distribution, retail food stores, food service establishments, or in the home, can result in the introduction, survival, or growth of pathogenic microorganisms. A lack of adequate controls throughout the complex food chain will increase the risk of foodborne disease. This portion of the total HACCP program is introduced in Section VII. At the request of the USDA, the National Research Council (NRC) established a committee "to develop a risk assessment model for comparing the effects on public health that might result from different postmortem inspection goals and strategies, to evaluate the public health risks associated with broilers, and to review the advantages of a sampling program as part of an overall quality assurance program for poultry slaughter" (8). The committee concluded that "existing inspection procedures do not significantly reduce contamination of broilers by microorganisms that are pathogenic to humans, nor were they designed to do so." To address this concern, the committee developed a flow diagram and identified certain potential chemical and biological hazards. The NRC committee described how this information could be used to assess the impact of alternative inspection procedures on public health. The NRC approach has led to the phrase "risk based inspection." Although the NRC committee identified the hazards, they left it to the discretion of the agency how this information should be used to develop and implement alternative inspection procedures and new strategies. The National Advisory Committee on Microbiological Criteria for Foods (NACMCF) is focused on microbiological safety and is charged with considering the potential use of microbiological criteria for enhancing food safety. The committee is convinced that a multiple approach is the most effective means to enhance food safety. This approach consists of applying HACCP as defined by the NACMCF. The following report consists of a review of existing information, a hazard analysis, and use of the information to develop a generic HACCP plan. The generic HACCP plan reviews the processing steps of slaughter operations for young chickens (i.e., broilers). Although there are many similarities to other types of poultry, the differences limit the use of the current plan to broilers. The goal of HACCP for slaughter operations is to prevent, eliminate, or reduce both the incidence and level of microorganisms that are pathogenic for humans and to control bacterial recontamination and/or outgrowth. Although poultry slaughter operations do not include a thermal process that ensures elimination of pathogens, a number of the processing steps can be controlled to minimize and reduce microbiological hazards. The overall objective of the HACCP program is to ensure that processing is conducted to enhance the microbiological safety of the product. This is achieved through effective management of key operations that realistically prevent or control the introduction or growth of pathogens. Integral to HACCP systems is adherence to good manufacturing practices (GMPs) which are common to all well-controlled food production facilities. These practices address effective sanitation, effective equipment/facility design and maintenance (4, 2, 7). A knowledgeable, welltrained workforce is essential in carrying out these practices. The National Broiler Council "Good Manufacturing Practices for Fresh Broiler Products" (7) is included as an example of GMPs that have been identified by industry (Appendix A). Several new technologies for broiler slaughter are in various stages of development, testing, and implementation. New technologies likely to become operational in the near future are included in the generic HACCP plan. A summary that discusses each of the new technologies and the anticipated benefits of implementation is included in Section IX. Areas where additional research is needed are discussed in Section X. Academic, government, and industry researchers should be encouraged to address these and related areas that provide new knowledge and technologies for enhancing the microbiological safety of poultry products. The generic plan provides general guidance for developing plant-specific plans. Such individualized HACCP plans for specific products and facilities should be developed and implemented by each manufacturer as the optimal means for food safety management (5). HACCP is also recommended as a tool for inspection. The food processor has the responsibility for developing and implementing welldefined HACCP plans. The role of the regulatory agency is to verify that the processor's HACCP plans are effective and are being followed. The USDA inspector should use the plant's HACCP plan for verification as necessary. A brief discussion of the role of regulatory agencies and industry in HACCP is included in Section VIII. In addition, a more detailed generic document which outlines the specific roles of the regulatory agencies and industry in a HACCP program is available (6). The Committee recommends the adoption of HACCP principles to reduce the presence of pathogenic microorganisms on raw broilers. In accordance with the NACMCF focus on safety (5), the current plan specifically addresses microbiological safety. However, it is worth noting that the increased process and product control achieved through HACCP is also likely to enhance the microbiological quality of raw poultry products. Successful utilization of HACCP systems is dependent on factors, such as employee education and training, records monitoring, proper reaction to noncompliant findings, and systematic verification to ensure the system's operation. Management is responsible for implementing and maintaining these factors. Full implementation is critical for HACCP plans to be successful. Therefore, management's understanding and commitment to the HACCP concept is imperative. The Committee recommends that

3 HACCP IN BROILER SLAUGHTER AND PROCESSING 581 HACCP plans include consideration of specific mechanisms for facilitating communication among and between all levels of plant operations and management. REFERENCES I. CFR (Code of Federal Regulations) Standards for kinds and classes, and for cuts of raw poultry. 9 CFR Chap. III ( edition), p Druce, E Ensuring the compliance of food manufacture with the design of the food. Food Sci. Technol. Today 2(1): Duewer, L. A., K. R. Krause, and K. E. Nelson U.S. poultry and red meat consumption, prices, spreads and margins. USDA, ERS, Agric. Info. Bull. No ICMSF (International Commission on Microbiological Specification for Foods) Microorganisms in Foods 4. Application of the Hazard Analysis Critical Control Point (HACCP) System to Ensure Microbiological Safety and Quality. Blackwell Scientific Pub. London, pp NACMCF (National Advisory Committee on Microbiological Criteria for Foods) Hazard analysis and critical control point system. Int. J. Food Microbiol. 16: NACMCF. 1994a. The role of the regulatory agencies and industry in HACCP. Int. J. Food Microbiol. 21: NBC (National Broiler Council) Good Manufacturing Practices. National Broiler Council. Washington, D.C. 8. NRC (National Research Council) Poultry Inspection-The Basis for a Risk-Assessment Approach. National Academy Press. Washington, D.C. pp EPIDEMIOLOGY OF FOODBORNE ILLNESS ATTRIBUTED TO POULTRY Foodbome disease is an important cause of morbidity in the United States. Both surveillance of foodbome diseases and prospective studies have identified foods of animal origin as important causes of human illness. A primary source of the pathogens associated with foodbome disease is the animals being slaughtered. During the slaughtering process, workers, equipment, and the processing environment can serve as sources of contamination for birds in process. This section will focus on agents that are the primary cause of morbidity and mortality associated with raw poultry. Sources and limitations of data Foodbome disease data in the United States are derived from retrospective and prospective studies, outbreak investigations, and sporadic disease surveillance by public health organizations. The Centers for Disease Control and Prevention (CDC) have maintained a national foodbome disease surveillance system since 1967 (1). This system is based primarily on reports of outbreaks from local and state health departments. There are limitations and strengths to the data collected by this system (6), but it is most useful for identifying trends in foodbome disease, not absolutely defining the importance of specific food vehicles. The system also provides a large body of data which can be analyzed in different ways to examine the characteristics of specific vehicles of foodbome disease, the characteristics of specific pathogens causing foodbome disease, and changes in these characteristics over time. The relative importance of poultry as vehicles of specific microorganisms which cause foodbome disease cannot be determined from outbreak surveillance data alone. As with other foods, it is likely that the surveillance data underestimate the importance of poultry as a cause of foodbome disease. Other available epidemiological data including prospective studies and sporadic case surveillance are needed to fully assess the role of poultry in foodbome illness. Outbreak data In the United States between 1973 and 1991, chicken products and foods containing chicken accounted for 226 (5%) outbreaks and 10,878 (5%) cases of outbreakassociated foodbome disease reported to CDC for which an etiologic agent was identified (7). During the period of , poultry products were associated with 13 (5%) of the 245 reported foodbome outbreak deaths (1). These data do not allow differentiation of cases where the identified pathogen was present in the live animal from those where raw or cooked products were contaminated from other sources during processing, distribution, or handling. However, comparisons of serovars of Salmonella commonly isolated from poultry and those from poultry-associated cases of salmonellosis suggest that the primary source is the original flock (15). Outbreak data also do not allow cases resulting from inadequate cooking to be distinguished from those caused by cross-contamination. However, the general consumer preference for well-done poultry meat supports the latter. This is reenforced by evaluations indicating that cross-contamination and inadequate holding temperatures are two factors often contributing to outbreaks of foodbome disease (5). Of the 115 outbreaks of known etiology, 112 were bacterial (7). The primary bacterial agents for poultry related outbreaks were Salmonella (61%), Staphylococcus aureus (17%), and Clostridium perfringens (12%). Salmonella and C. perfringens accounted for 11 of 13 poultryassociated deaths during the 15-year period from 1973 to 1987 (1). Sporadic case data Studies of foodbome illness indicate that different commodities can be associated with outbreaks and sporadic foodbome disease caused by a specific microorganism. In addition, certain microorganisms can be an important cause of sporadic foodbome illness, yet can be an infrequent cause of foodbome outbreaks. In the case of chicken products, CDC data indicate that Campylobacter may be a more common cause of bacterial diarrheal disease than Salmonella, although Campylobacter rarely is associated with outbreaks. In a prospective study of diarrheal disease in Seattle, Washington, Campylobacter and Salmonella were isolated at rates of 50/100,000 and 21/100,000, respectively (14, 15). Epidemological studies of sporadic cases in the United States and Europe indicate an association of campylobacteriosis with inappropriately handled or cooked poultry products (9, 14, 10). Another foodbome pathogen, Listeria monocytogenes, has been associated with poultry products and is also under represented in the foodbome outbreak surveillance data (11). At that time it was estimated that there were approximately

4 582 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS 2000 cases of listeriosis per year in the U.S., most of them sporadic. Some result in serious illness, with an approximate 25% case fatality rate. Recent epidemiologic studies have implicated undercooked chicken as a risk factor for infection, particularly in persons immunosuppressed by underlying diseases (12). In one case-control study, 6% of the listeriosis cases were correlated with consumption of undercooked chicken (11, 13). Mechanism of transmission and risk factors for foodborne pathogens associated with raw poultry Epidemiologic investigations demonstrate the importance of microbial contamination of raw poultry products. Contamination of chicken coupled with food handling errors may result in the persistence or reintroduction of the microorganism. Foodborne Disease Surveillance System data indicate that food handling errors were often found to contribute to outbreaks (1, 5). These included such factors as improper holding temperatures, inadequate cooking, contaminated equipment, and poor personal hygiene. Inadequate cooking and improper holding temperatures were frequently identified as factors contributing to outbreaks associated with poultry products (1, 4, 5). Raw chickens may be the means by which human pathogens are introduced into the home and food service environments and ultimately contaminate other foods (8). Cross-contamination of ready-to-eat products is recognized as an important mechanism for Salmonella outbreaks and sporadic cases of campylobacteriosis (8,9, 10). Improper handling can also lead to foodborne disease caused by organisms such as C. perfringens or S. aureus. In the case of S. aureus, the primary source of contamination appears to be food handlers in the home or food service facilities (2, 3). Subjecting foods contaminated with S. aureus to temperature abuse may lead to multiplication to high numbers and enterotoxin production. Outbreaks of C. perfringens are usually associated with cooked foods that have been improperly cooled or exposed to improper temperatures allowing growth to high numbers (4,5). REFERENCES 1. Bean, N. H., and P. M. Griffin Foodborne disease outbreaks in the United States, : Pathogens, vehicles, and trends. J. Food Prot. 53: Bryan, F. L. 1968a. What the sanitarian should know about Staphylococci and Salmonellae in non-dairy products. 1. Staphylococci. J. Milk Food Technol. 31: Bryan, F. L. 1968b. What the sanitarian should know about Staphylococci and Salmonellae in non-dairy products. II. Salmonellae. J. Milk Food Technol. 31 : Bryan, F. L Factors that contribute to outbreaks of foodborne disease. J. Food Prot. 41 : Bryan, F. L Foodborne diseases in the United States associated with meat and poultry. J. Food Prot. 43: Buchanan, R. L., and C. M. DeRoever Limits in assessing microbiological food safety. J. Food Prot. 56: CDC. Personal Communication. 8. DeWit, J. c., G. Broekhuizen, and E. H. Kamplemacher Cross-contamination during preparation of frozen chickens in the kitchen. J. Hyg. 83: Hopkins, R. S., and A. S. Scott Handling raw chicken as a source for sporadic Campylobacter jejuni infections. J. Infect. Dis. 148: Kapperud, G., E. Skjerve, N. H. Bean, S. M. Ostroff, and J. Lassen Risk factors for sporadic Campylobacter infections: Results of a case-control study in southeastern Norway. J. Clin. Microbiol. 30: Schuchat, A., B. Swaminathan, and C. V. Broome Epidemiology of human listeriosis. Clin. Microbiol. Rev. 4: Schuchat, A., K. Deaver, J. D. Wenger, B. Swaminathan, and C. V. Broome Role of food in sporadic listeriosis: 1. Case-control study of dietary risk factors. JAMA 267: Schwartz, B., C. A. Ciesielski, C. V. Broome, G. R. Brown, A. W. Hightower, C. A. Ciesielski, S. Gaventa, B. G. Gellin, L. Mascola, and the Listeriosis study group Association of sporadic listeriosis with consumption of uncooked hot dogs and undercooked chicken. Lancet II October I, 1988: Tauxe, R. V., N. Hargrett-Bean, C. M. Patton, and 1. K. Wachsmuth Campylobacter isolates in the United States, In CDC Surveillance Summaries, June MMWR 37 (No. SS-2):I Tauxe, R. V Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. pp In Nachamkin, 1., M. J., Blaser and L. S. Tompkins (eds.), Campylobacter jejuni current status and future trends. American Society for Microbiology, Washington, D.C. FARM MANAGEMENT PRACTICES 1ntroduction Broiler production in the United States began in 1923 on the Delmarva Peninsula (20). Initially, most production took place on small family farms with only a few hundred birds raised at a time. With the development of genetically improved meat-type breeds and improved feeds, the industry continued to grow. Integrated companies incorporating hatcheries, feed companies, processing plants and even rendering plants eventually formed as the industry increased in size. In the United States, almost all producers are now growing broilers on a contract basis with a large integrator. In this arrangement, the integrator furnishes the chicks, feed, and health-related services, while the producer supplies the equipment, labor and other incidentals. Salmonella and Campylobacter The two human enteropathogens most frequently associated with broiler chickens are Salmonellae and C. jejuni. The source and location of colonization within the chicken are different for each of these organisms. Because the processing of raw broilers does not involve a lethal heat process, such as pasteurization, to reduce the level of Salmonellae and Campylobacter contamination, it is important that chickens with as few pathogens as feasible be delivered to the processing plant. Control of Salmonellae is complicated because there are numerous potential sources of Salmonellae contamination in an integrated poultry operation, including chicks, feed, rodents, birds, insects, transportation, and the processing plant environment. Exposure to Salmonellae from any of these potential reservoirs, however, does not guarantee colonization of chickens. Many factors affect the susceptibility of chickens to Salmonellae colonization (1). These include 1) age of chicken, 2) survival through gastric barrier passage, 3) effectively competing with other bacteria, 4)

5 HACCP IN BROILER SLAUGHTER AND PROCESSING 583 locating a hospitable colonization site, 5) nature of diet, 6) physiological status of the chicken, 7) health and disease status of the chicken, 8) environmental stresses, 9) effects of medication, and 10) host genetic background. Preventing chickens from becoming colonized with Salmonellae is further complicated because, in contrast to the pathogenic relationship between Salmonellae and humans, most serovars of Salmonellae generally have a commensal relationship with chickens. This makes the vaccine approach to control of Salmonellae in broiler chickens a difficult task. However, the vaccine approach may play a role in controlling Salmonellae in broiler breeders. Pathological colonization elicits defense responses (immunological and febrile) from the host to limit the damage caused by the pathogen and speed elimination of the virulent organism from the host. Adequate defense responses, normally, are not elicited with commensal colonizers. There are a number of distinct differences in the way chickens become colonized and maintain Salmonellae or Campylobacter during production. Unless there is disease, temperature, or other stress, the highest levels of intestinal colonization of Salmonellae generally occur during the second or third week of grow-out, after which, typically, there is a gradual decline in frequency until the time of processing (27). Campylobacter is rarely found in chicks before the second to third week of grow-out, but when a colonization break occurs in the house, practically all birds will become colonized within a few days and will remain colonized through grow-out. Unlike Salmonellae, Campylobacter is rarely found in poultry feed or the hatchery environment (30). The more likely vectors are flies, wild birds, rodents, or possibly untreated water or the contaminated footwear of attendants. Salmonellae are usually found in low numbers «100 cfu/carcass) on broiler carcasses exiting the processing plant whereas C. jejuni is often found in high numbers (>10,000 cfu/carcass) (32). Pathogen control Erwin (13) first recovered viable Salmonella from commercial poultry feed, and since that time the role of feed and feed ingredients in the spread of Salmonellae through the poultry industry has received a great deal of attention. Less than one Salmonella per gram of feed has been shown to establish colonization in 1 to 7-day-old chicks (28). Therefore, under some conditions, feed can be an important source of Salmonellae. Formulations of propionic and formic acid have been tested as feed additives to reduce Salmonellae (16). The results from these studies are inconsistent, and additional studies are being conducted. All sources of Salmonellae including feed are potentially important, particularly during the first week of growout; however, other sources appear to contribute more to the final processed broiler than feed. These include breeder flocks (4), hatcheries, and litter. Goren (14) showed that serotypes of Salmonella found on final processed carcasses were found in hatchery samples but were not found in the feed. Lahellec and Colin (17) reported that serotypes of Salmonella isolated on the final processed carcasses were found primarily in litter and other environmental samples. Bailey (3) found that litter was the primary source of Salmonella in control houses, but that the hatchery was the primary source of Salmonella in competitive exclusion (CE) treated broilers. The delivery of Salmonellae-free chicks to the grow-out houses is critical for control of Salmonellae in flocks. At hatch, most chicks have very little microflora in their gut and are far more susceptible to Salmonellae colonization than older chicks. Milner and Shaffer (19) first observed that colonization of chicks was dose-dependent and varied with the day of challenge. They found that day-old chicks could be colonized with less than five cells of Salmonella but that later colonization was irregular and took higher doses of Salmonella to achieve. Two-week-old chicks have mature gut micro flora (5) and, thus, are more resistant to intestinal colonization by Salmonellae. A single Salmonella-contaminated egg has been shown to substantially contaminate other eggs and chicks in a hatching cabinet (4). Several procedures and equipment within commercial hatcheries have been identified as potential sources of cross-contamination for the dissemination of Salmonella (12). Feed and environmental sources of Salmonellae still play a role in transmitting Salmonellae during chicken production, but Salmonellae that chicks bring with them into the grow-out house must be controlled before competitive exclusion or other control measures can be expected to work. The complexity of Salmonellae colonization of chickens will require a multifaceted integrated approach to successfully reduce Salmonellae in production. A promising approach to reducing salmonellae in chickens during production is CE, first reported by Nurmi and Rantala (21). CE involves the oral introduction of intestinal micro flora from Salmonellae-free adult chickens into newly hatched chicks. The CE concept was summarized by Pivnick and Nurmi (23) as follows: 1) Newly hatched chicks may be colonized by a single cell of Salmonella. 2) Older birds are resistant to colonization because of normal gut microflora. 3) The introduction of flora from an adult bird into a day-old chick speeds the maturation process of the gut microflora and increases the resistance of most chicks to Salmonellae colonization. In many laboratories around the world, the CE concept has been conclusively shown to be an effective approach (2,21,22, 29), but large-scale field trials have had mixed results (14, 15). A three-replicate field trial where CE treated and control birds were processed on separate days showed a significant reduction from 41 % to 10% in the percentage of Salmonellae-positive carcasses (8). The primary reason for the presence many of the salmonellaepositive birds in the CE treated group is that commercial hatcheries and hatchery environments have been shown to be highly contaminated with Salmonellae (9) and this hatchery contamination can limit the effectiveness of CE (14). It has been demonstrated that chemical disinfection of fertile hatching eggs (10, 11), significantly reduces Salmonellae contamination. Unlike salmonellae which colonize the epithelium of the lower intestinal tract, primarily the cecum, usually, C. jejuni is a free swimming organism in the mucin layer (7).

6 584 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS Because of the unique differences in niche distribution of the Salmonellae and C. jejuni in the intestinal tract, different bacteria will likely act as natural competitors. Mucosal CE (MCE) was developed to maximize the number of mucin layer bacteria in the exclusion culture (31). The MCE has proven to be effective in preventing Salmonellae colonization and in reducing the levels of C. jejuni carriage in isolator unit trials. Floor pen and field trials have given inconsistent results for C. jejuni (30). Waterborne viable but nonculturable Campylobacter were identified as a potential source of chicken colonization (26). When strict sanitation procedures were applied to the water supply, the isolation rate for broiler chickens was reduced from 80% to 2%. Other researchers have not obtained similar results from increased water hygiene (18). In a large-scale epidemiological study in Sweden (6), it was found that buildings, feed, water and day-old chickens were not primary sources of Campylobacter in their chickens. Improving overall farm hygiene along with increased biosecurity are the methods suggested that seem to reduce Campylobacter levels of commercial broilers. Transportation stress cannot be overlooked as a cause of cross-contamination of birds. Unless all Salmonellae and Campylobacter are eliminated from the growing broilers, transport stress may cause the birds to begin shedding (24). Chickens will be withdrawn from feed for several hours, crowded into transport coops, deprived of water, and subjected to hot or cold temperatures for several more hours. All of these factors are likely to induce shedding of Salmonellae if present. In addition to newly shed Salmonellae present in coops, Rigby (25) did a study where 86.6% of transport coops tested positive for Salmonellae, and 73.5% of these coops still tested positive after going through a commercial crate washer. In a separate study, Rigby and Pettit (24) showed that all 24 chickens placed in crates contaminated with S. alachua became carriers of this organism; 22 of these were cecal carries, and 18 were shedders. This contamination also spread to 15 of 24 chickens placed in clean crates and shipped in the same truck. These results indicate that chickens in shipping crates exposed to Salmonellae under transport conditions may readily become colonized and spread Salmonellae around the processing plant. REFERENCES 1. Bailey, J. S Factors affecting microbial competitive exclusion in poultry. Food Technol. 41(7): Bailey, J. S., L. C. Blankenship, N. J. Stern, N. A. Cox, and F. McHan Effect of anticoccidial and antimicrobial feed additives on prevention of Salmonella colonization of chicks treated with anaerobic culture of chicken feces. Avian Dis. 32: Bailey, J. S., N. A. Cox, L. C. Blankenship, and N. J. Stern Commercial field trial of mucosal competitive exclusion culture (MCE) treatment for control of Salmonella colonization on broiler chickens. Poult. Sci. 70(Supplement 1) Bailey, J. S., N. A. Cox, and L. C. Blankenship Breeder flocks and hatcheries as critical control points for reduction of commensal colonization of broiler chickens. Proc. Int. Symp. Salmonella and Salmonellosis. Ploufragen Saint-Brieu, France, pp Barnes, E. M., G. C. Mead, D. A. Barnum, ande. G. Harry The intestinal flora of the chicken in the period 2 to 6 weeks of age, with particular reference to the anaerobic bacteria. Br. Poult. Sci. 13: Berndtson, E A three-year study of Campylobacter in Swedish broiler flocks. Proc. 6th Int. Workshop on Campylobacter, Helicobacter & Related Organisms, Sydney, Austriala, p Berry, J. T., M. B. Hugdahl, and M. P. Doyle Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 54: Blankenship, L. c., J. S. Bailey, N. A. Cox, N. J. Stern, R. Brewer, and O. Williams Two-Step mucosal competitive exclusion flora treatment to diminish Salmonellae in commercial broiler chickens. Poult. Sci. 72: Cox, N. A., J. M. Mauldin, and J. S. Bailey Presence and impact of Salmonellae contamination in the commercial broiler hatcheries. Poult. Sci. 69: Cox, N. A., and J. S. Bailey Efficacy of various chemical treatments over time to eliminate Salmonella on hatching eggs. Poult. Sci. 70(Supplement I): Cox, N. A., J. S. Bailey, M. E. Berrang, R. J. Boor, and J. M. Maukin Chemical treatment of Salmonella-contaminated fertile hatching eggs using an automated egg spray sanitizing machine. J. Appl. Poult. Res. 3: Davies, R. H., and C. Wray An approach to reduction of Salmonella infection in broiler chicken flocks through intensive sampling and identification of cross-contamination hazards in commercial hatcheries. Int. J. Food Microbiol. 24: Erwin, L. E Examination of prepared poultry feeds for the presence of Salmonella and other enteric organisms. Poult. Sci. 34: Goren, E., W. A. de Jong, P. Doornenbal, N. M. Bolder, R. W. A. W. Mulder, and A. Jansen Reduction of Salmonella infection of broilers by spray application of intestinal microflora: A longitudinal study. Vet. Q. 10: HUttner, Von B., H. Landgraf, and E. Vielitz Kontrolle der Salmonelleninfektionen in mastelterntier-bestanden durch verabreichung von spf-darmflora an eintagskiiken. Dtsch. Tieraerztl. Wochenschr.88: Kaniawati, S Effects of feeding organic acids to broilers on performance and Salmonella colonization of the ceca and/or contamination of the carcass. Ph.D. dissertation. University of Arkansas, Fayetteville, AR Labellec, C., and P. Colin Relationship between serotype of Salmonellae serotypes from hatcheries and rearing farms and those from processed poultry carcasses. Br. Poult. Sci. 26: Lanning, D. G., T. J. Humphrey, A. Henley The colonization of broiler chickens with Campylobacter jejuni-some epidemiological investigations. Epidemiol. Infect. 110: Milner, K. C., and M. F. Shaffer Bacteriologic studies of experimental Salmonella infections in chicks. J. Infect. Dis. 90: North, M. O Commercial chicken production manual. The AVI Publishing Company, Westport, CT, p Nurmi, E., and M. Rantala New aspects of Salmonella infection in broiler production. Nature. 241 : Pivnick, H., B. Blanchfield, and J. Y. D. Aoust, Prevention of Salmonella infection in chicks by treatment with fecal cultures from mature chickens (Nurmi cultures). J. Food Prot. 44: Pivnick, H., and E. Nurmi The Nurmi concept and its role in the control of Salmonella in poultry, pp In Developments in food microbiology. R. Davies (ed.). Applied Science Publisher Ltd., Essex, England. 24. Rigby, C. E., and J. R. Pettit Changes in the Salmonella status of broiler chickens subjected to simulated shipping conditions. Can. J. Compo Med. 44: Rigby, C. E., J. R. Pettit, M. F. Baker, A. H. Bentley, M. O. Salomons, and H. Lior Flock infection and transport as sources of Salmonella in broiler chickens and carcasses. Can. J. Compo Med. 44: Rollins, D. M Potential for reduction in colonization of poultry by Campylobacter from environmental sources. pp In Colonization control of human bacterial enteropathogens in poultry. L. C. Blankenship, (ed.) Academic Press. N.Y.

7 HACCP IN BROILER SLAUGHTER AND PROCESSING Sadler, W. W., 1. R. Brownell, andm. J. Fanelli Influence of age and inoculum level on shed pattern of Salmonella typhimurium in chickens. Avian Dis. 13: Schleifer, J. H., B. 1. Juven, C. W. Beard, and N. A. Cox The susceptibility of chicks to Salmonella montevideo in artificially contaminated poultry feed. Avian Dis. 28: Snoeyenbos, G. H., O. M. Weinack, and C. F. Smyser Protecting chicks and poults from Salmonellae by oral administration of "normal" gut microflora. Avian Dis. 22: Stem, N. J Reservoirs for Campylobacter jejuni and approaches for intervention in poultry. pp In Campylobacter jejuni Current Status and Future Trends. I. Nachamkin, M. Blaser and L. Tompkins (eds.). American Society for Microbiology, Washington, D.C. 31. Stem, N. J Mucosal competitive exclusion (MCE) to diminish colonization of chickens by Campylobacter jejuni. Poult. Sci. 73: Waldroup, A. L., B. M. Rathgeber, R. H. Forsythe, and L. Smoot Effects of six modifications on the incidence and levels of spoilage and pathogenic organisms on commercially processed postchill broilers. J. Appl. Poult. Res. 1: MICROBIOLOGICAL PROFILE OF RAW CHICKEN General microbiological parameters The skin and muscle tissue of raw chicken are both nutrient-rich substrates that can support the growth of a wide range of microorganisms. The skin has diverse microflora, whereas it is generally assumed that the interior of an intact muscle from a healthy bird is free of microorganisms. Occasionally, bacteria can be isolated from areas adjacent to bone joints, particularly if they are inflamed. Microorganisms are introduced into the interior of muscle tissue as a result of bacterial translocation from the surface of the carcass. The initial microflora of the live bird is diverse at the time of slaughter, and includes Gram-negative and Gram-positive mesophiles and psychrotrophs (2). Potential sources of bacteria include the skin and feathers (73), intestinal and crop contents (75), and the processing plant environment (2,42). Commonly encountered genera include Lactobacillus, Escherichia, Flavobacterium, Acinetobacter, Achromobacter, Corynebacterium, Streptococcus, Staphylococcus, Clostridium, Pseudomonas, Micrococcus, and Bacillus. The microflora is modified by slaughter and processing operations. The bacterial load of freshly processed chickens typically ranges from 0.8 to 4.3 IOglObacteria/g based on whole carcass rinses (85, 117). There can be significant variability in bacterial loads among processing plants and carcass lots. However, the greatest variability is among individual carcasses (85, (85, 117). Factors influencing overall bacterial levels on the carcasses include time of feed withdrawal prior to slaughter (12, 57, 112, 117, 118), transport time from farm to plant (85), crating time (85,117), outside air temperature (117), temperature within the plant (87, 117), and time during the processing day (117). In addition, equipment malfunction (100) inadequate chilling (6, 90, 139), chill tank (31, 69), and other equipment (57, 62, 73). Processing steps (13, 26, 74, 75) in the slaughter process can also influence bacterial loads on the carcass. Subsequent storage conditions of the raw chicken can be selective for a much more limited group of aerobic psychrotrophic species, particularly members of the genera Pseudomonas, Shewenella, Moraxella, and Acinetobacter. Microbial spoilage of raw chickens occurs primarily on the surface. The specific genera encountered are dependent on the storage temperature, moisture content, ph, oxygen availability/atmospheric composition, and processing practices. These factors are discussed below. Storage temperature. Microbial growth on raw poultry is strongly influenced by storage temperature. As storage temperatures are lowered toward freezing, there is a significant decrease in the rate of microbial growth and a reduction in the diversity of the microflora. With storage at temperatures just above freezing (-2 to +2 C), the shelflife of raw poultry is extended greatly (7, 9). At warmer refrigeration temperatures (::S5 C), Pseudomonas species are the primary cause of spoilage (8). At temperatures >5 C, a wider variety of bacteria will grow. Spoilage of aerobically stored raw poultry is generally associated with Gram-negative bacteria. As temperature is increased, Gram-positive species play an increasingly more important role. Moisture content. Fresh chicken meat has a water activity (a w ) of ~0.98 which supports the growth of a wide variety of bacteria, yeast, and molds. The specific a w on the surface of the bird will dependent on the extent of dry-air cold storage. However, most poultry is packaged to prevent desiccation. ph. The ph of chicken meat varies among the muscle types, reflecting inherent differences in muscle physiology and glycogen stores. Post rigor breast muscle has a ph of , whereas the ph ofleg muscle (dark meat) is (25, 143). The ph of chicken skin increases with age, an average of 6.6 for 9-week birds compared to 7.2 for 25-week birds. The differential in ph among muscle types can lead to differences in both the rate of microbial spoilage and the composition of the spoilage flora (6,81,82). Acidification of chicken tissue can reduce microbiological spoilage rates (154). Oxygen availability and atmospheric composition. The rate of microbial growth and the composition of the microflora on raw poultry can be influenced by the atmosphere surrounding the product. The effects of atmospheric composition are largely a function of oxygen availability and carbon dioxide concentrations. The surface of raw poultry is aerobic, an environment that permits rapid growth of aerobic psychrotrophs, such as Pseudomonas. However, the poising capacity of meat tissue is high, and an anaerobic environment predominates a few millimeters below the surface. This selects for psychrotrophic microaerophiles and facultative anaerobes. Restricting oxygen availability can substantially alter microbial growth on the meat surface. Since raw poultry meat is actively respiring, even a partial restriction of oxygen permeability can cause a depletion of oxygen and an accompanying increase in carbon dioxide. Grinding raw chicken meat increases the surface area exposed to oxygen and distributes any contamination present on the surface throughout the meat. The increased surface area also increases the amount of exposed actively respiring muscle

8 586 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS tissue, leading to rapid oxygen depletion when packaged in materials that restrict oxygen availability. In general, restricting oxygen levels surrounding refrigerated raw chicken shifts the microflora from predominately Gram-negative aerobic bacteria, particularly Pseudomonas, to a mixture of Gram-positive and Gram-negative facultative anaerobes and microaerophiles, such as Lactobacillus, Shewenella putrefaciens, Brochothrix thermosphacta, Enterobacteriaceae, and Aeromonas (1, 40, 83, 84, 123, 133). The presence of high levels of carbon dioxide (>20%) can suppress the normal aerobic Gram-negative microflora of raw poultry and significantly extend shelf-life (51,58, 151). Such atmospheric composition leads to a micro flora that is predominately microaerophilic. The effect of carbon dioxide strongly depends on storage temperature, and effectiveness increases as the temperature is lowered. Modified atmospheres may not be effective at temperatures above 10 _ 15 C (51, 55, 151), and as such cannot be relied on as a secondary barrier to control pathogen growth during temperature abuse. Effect of slaughter operations The diverse microflora present on the bird immediately before and after killing are influenced by the processing steps that follow. Scalding. Scalding is a process by which the bird is subjected to moist heat for a short time to facilitate the removal of feathers. Although there are a number of potential means for scalding, most broilers in the U.S. are processed by immersion scalding. Two types of scalding are differentiated based on processing temperatures; soft scalds (:S55 C) and hard scalds (>55 C). A soft scald retains the cuticle/epidermis of the skin, which is removed with a hard scald. Broilers are primarily soft scalded in the U.S. When the birds are immersed in the scald water tank, some of the dirt, fecal material, and other contaminants on the surface of the bird are removed. However, due to the continuous overflow used with immersion scalders, the level of bacteria in the tank generally does not exceed 4.7 IOglO bacteria per ml (98, 146). This heating step influences the microflora on the surface of the bird. The extent of the effect depends on the processing temperatures and time. Soft scalds decrease the levels of psychrotrophs to a lesser extent than Enterobacteriaceae, but have little effect on the total bacterial load as measured by aerobic plate counts (97, 107). Bacterial counts on carcasses are generally in the order of 4.0 Log1O/cm 2 Harder scalds have a greater effect on total numbers (107). However, this treatment can cause changes in tissues, making them better substrates for microbial attachment and growth (24, 36, 62, 70, 153). Scalding tends to be selective for the more heat resistant mesophiles and spore-forming organisms and can serve as a means for cross-contamination. C. perfringens and low levels of S. aureus are routinely isolated from scald water, but Salmonellae and Campylobacter are rarely isolated (2). Scalding appears to have little significance relative to the incidence or level of C. jejuni contamination on the final carcass (41, 110, 149, 152). Overall, scalding has relatively little effect on the microbiology of refrigerated eviscerated chickens purchased at retail (2). Countercurrent scalders generally have a greater impact on reducing the levels of microorganisms on the carcass. Defeathering. Defeathering can act as both a means of cross-contamination and a source of specific organisms during poultry processing. Mechanical defeathering leads to an increase in total bacterial levels but not psychrotrophs (26, 146). Defeathering has been reported to result in increases in S. aureus. This is associated with the rubber fingers used to remove the feathers (91, 129), because the microorganism becomes established in cracks in the rubber of the fingers. Defeathering has been identified as a major site of cross-contamination for poultry carcasses including pathogens and indicator organisms, such as Campylobacter, Salmonella, and E. coli (16, 32, 41, 94, 99, 106, 110, 149, 144, 152). Further, the extraction of the feather from the follicle can lead to deep entrapment of bacteria which are difficult if not impossible to remove during later processing steps (104, 106). Evisceration. Evisceration can be a major source of additional fecal contamination, particularly if the intestines are cut. This would be expected to increase contamination by mesophilic bacteria, including intestinal pathogens (i.e., Salmonella, Campylobacter, and C. perfringens). Cut intestines can lead to contamination of equipment, workers, and inspectors and can be a major source of cross-contamination (21,88,124,150). Washing. Spray washing or other forms of rinsing is used to remove organic material and some of the microorganisms that may have been acquired during defeathering and evisceration. This step helps reduce bacterial levels on the skin of broilers, including levels of Enterobacteriaceae and salmonellae (6, 59, 89, 97, 121). Frequent multiple sprays from bleeding to chilling are more effective in reducing bacterial levels than a single final wash (96, 108). However, water can be an important source of Pseudomonas associated with the spoilage of broilers (5). Chlorinated sprays can help prevent the buildup of bacterial counts on evisceration equipment (2). However, it is unclear if the addition of acids or chlorine to sprays impact the microbiological shelf life of refrigerated eviscerated poultry (77, 100, 143). Immediate spray washing has been demonstrated to be as effective as trimming for removal of fecal contamination acquired during evisceration (13, 14). Chilling. Although several types of chilling procedures are employed commercially, immersion chilling is the most common in the U.S. because of its effectiveness and low cost. Achieving refrigerated temperatures in the interior of muscle tissue can take a substantial amount of time. However, cooling at the surface is rapid. Thus, the site of most microbial contamination is cooled rapidly, halting the growth of mesophilic bacteria, The impact of a properly maintained and operated immersion chiller on the overall bacterial levels on poultry carcasses seems to be minimal, with small increases and decreases having been reported by various investigators (26, 68, 139, 140, 141, 144). However, immersion chilling can be an important site of crosscontamination for spoilage bacteria, indicator organisms, and pathogens (23, 48, 75, 94, 144). Chlorination of chiller

9 HACCP IN BROILER SLAUGHTER AND PROCESSING 587 water at levels >25 ppm has been reported to control or reduce cross-contamination of the Gram-negative spoilage microflora and Salmonellae (28, 31, 69, 86, 93, 102), but was not effective for S. aureus (114) and clostridial spores (34). Potential for foodborne pathogens It is not surprising that raw, refrigerated chicken harbors a number of pathogenic bacteria. This is results from the presence of various pathogenic bacteria as part of the normal microflora of healthy chickens, the complex nature of chicken slaughtering operations, the lack of lethal processing steps, the significant potential for contamination from environmental sources and food handlers, and the requirement for extended refrigeration. The specific levels vary substantially among the specific microorganisms. However, in general the levels are low. Salmonella. Salmonella is the human pathogen that consumers most commonly associate with raw poultry products. The ultimate source of the Salmonella is the original flock (21, 79, 80). The prevalence of Salmonellapositive birds among a flock entering a processing plant is generally low (119, 120), but there are substantial opportunities for carcass to carcass spread during slaughter and subsequent processing (21, 27, 75, 80, 89, 95, 105). The results of numerous studies have indicated that the incidence of Salmonella on raw poultry leaving the processor or at the retail market can range from 1% to > 50%. However, the level of these pathogens is typically low, in the range of 1 to 30 cells/carcass (134). If temperature abused, raw poultry will support the growth of Salmonella. Gram-negative and Gram-positive pathogens can adhere quite tenaciously to the surface of chicken skin and muscle, making their removal difficult. The process has been most extensively studied with Salmonella spp. and appears to involve multiple mechanisms, including retention, entrapment, and adhesion. Retention involves bacteria present in the layer of water retained by the chicken surface after immersion or wetting (136, 137). Complete removal of this water layer is difficult. However, at least initially, the bacteria in this water layer are neither physically or chemically attached and can be removed by rinsing or showers that "dilute" the microbial population in the water layer. The changing conditions (temperature, immersion in water, etc.) that occur during processing can cause the tissue to swell and shrink, leading to the second retention, entrapment, and adhesion mechanism, entrapment. Salmonella become physically entrapped in clefts, pores, and connective tissue networks as they open and close during processing, making these bacteria more difficult to remove (10, 71, 74, 137). The third mechanism, adhesion, represents the strongest form of attachment. It appears to involve high-affinity chemical attachment of the bacteria to specific receptor sites. Adhesion is not dependent on flagella, fimbriae, or electrostatic charge (122, 71, 74, 136). Salmonella attachment of this type is associated with connective tissue, particularly collagen (10, 61, 122, 136, 137, 147, 148). The specific receptor site is still being investigated, though adhesion to hyaluronan has been identified as a likely receptor site (122). Removal of fully adhered Salmonella is very difficult but is enhanced somewhat by the use of sodium, calcium, or magnesium salts (10, 71, 72). Adhesion of Salmonella is increased by high scald temperatures that remove the epidermis (62). Salmonella attached to poultry surfaces appear to be more resistant to biocides and antimicrobials, such as chlorine (76). Attachment mechanisms of a similar nature are likely to be involved in the attachment of other pathogens. For example, E. coli, including serovar 0157: H7, and S. aureus appear to bind preferentially to collagen (38, 67, 115, 127). Fibronectin binding has also been reported to be involved in the adhesion of Salmonella, Staphylococcus, and E. coli to tissues (4,33,67, 78). Campylobacter jejuni. The Committee has reviewed the significance of raw poultry as a source of C. jejuni (101). In recent years, the presence of C. jejuni on raw poultry has received increased attention as the microorganism's role in human disease has been better defined. This pathogen has been isolated from raw poultry products worldwide, often at prevalence rates exceeding 50% (37, 63, 113, 126, 128). The pathogen is a common inhabitant of the intestinal tract of live, healthy birds (15, 47, 135). Scalding and defeathering have been identified as potential sites during slaughter operations that could spread the microorganisms to previously uncontaminated carcasses. The levels of C. jejuni are generally higher than other enteric bacteria, and on occasion they can be present at levels as high as /carcass (11, 110, 126, 130). The role of C. jejuni as a significant foodborne pathogen is somewhat surprising considering its microbial characteristics. The microorganism requires a microaerophilic environment (e.g., 5% O 2 /10% CO 2 ) (60), is readily inactivated by minimal cooking (46), declines when stored at refrigerated temperatures (63), and grows poorly, if at all, at temperatures below 32 C (101). It is unlikely that this bacterium would grow significantly on raw poultry, even if temperature abused. Listeria monocytogenes. Unlike Salmonella and C. jejuni, L. monocytogenes is capable of growth at refrigeration temperatures. However, the prevalence on newly slaughtered broilers is substantially lower than either Salmonella or C. jejuni. The slaughter and processing environments appear to be a primary source for this psychrotrophic pathogen (42, 54), though it is likely that the original source of the microorganism is contamination of the equipment or environment with feces or ingesta (35). This microorganism is a common contaminant of poultry products worldwide, with isolation rates reaching 50% (3, 42, 54, 116, 125, 145). Its growth on raw poultry meat depends on the interaction of several factors including ph, storage temperature, and atmospheric composition. The microorganism did not grow on chicken stored at 1 C (51), but did grow at temperatures ~3 C (22, 51, 55, 151). It is likely that leg meat will support the growth of L. monocytogenes at lower refrigeration temperatures because of its higher ph. Modified atmospheres that inhibit the growth of the aerobic microflora of chicken do not necessary inhibit the growth of L. monocytogenes (51,55,151). The heat resistance of L. monocytogenes

10 588 NATIONAL ADVISORY COMMITIEE ON MICROBIOLOGICAL CRITERIA FOR FOODS IS substantially greater than Gram-negative enteric pathogens. Clostridium perfringens. Clostridium perfringens is an oxygen-tolerant, spore-forming anaerobe that commonly inhabits the lower intestinal tract of both chickens and humans. Low levels of the microorganism are typically found on the surface of a large percentage of broilers and other poultry (20, 49, 92, 132). Its spores are more resistant than vegetative cells and unaffected by the processes associated with poultry slaughter, such as scalding (2). Because C. perfringens gastroenteritis is only associated with consumption of high levels of vegetative cells (2: 10 6 cfu/g) (30, 53), raw poultry would require substantial temperature abuse (> 15 C) to result in spore germination and outgrowth. However, once germinated C. perfringens has a very short generation time (8 to 12 minutes) under optimal conditions (37 to 42 C). Cooking and other mild heating stimulates spore germination, enhancing growth of the pathogen. Clostridium perfringens outbreaks have been commonly associated with improper cooling, improper hot holding, and inadequate reheating of cooked food products (18, 19), but not temperature abuse of raw chicken. Staphylococcus aureus. Staphylococcus aureus is part of the microflora of chickens, commonly associated with bruised or infected tissue, nasal passages, skin surfaces, and arthritic joints. Typically, these are poultry-associated strains which can be differentiated from human isolates (44, 45). Low levels of S. aureus are commonly found on the surface of poultry and throughout poultry processing plants (43, 109, 134, 138). Scalding would be expected to reduce the initial level of S. aureus on the birds. However, the carcasses are recontaminated by plant-specific strains during defeathering (44, 91, 109). A percentage of these isolates are enterotoxigenic (43, 52, 56). However, they do not seem to be important in the etiology of poultry product associated staphylococcal intoxications. Instead, most staphylococcal outbreaks appear to be related to recontamination of cooked products by food handlers followed by improper holding temperatures (16, 17, 19). Evisceration and immersion chilling have also been identified as sites in the processing plant associated with the contamination or cross-contamination by S. aureus (109). Other pathogens. Other Gram-negative bacteria that are occasionally associated with foodborne disease can be isolated from raw poultry. There are a number of reports of non-pathogenic environmental strains of Y. enterocolitica being isolated at relatively high rates from chicken carcasses and raw poultry meat samples (29,66, 103). This species is of interest because it is psychrotrophic. However, raw poultry has not been associated with either outbreaks or sporadic cases of yersiniosis. The isolates from poultry do not belong to the pathogenic biogroups. Psychrotrophic species of the genus Aeromonas, particularly A. hydrophila and A. sobria, are commonly associated with refrigerated raw poultry, often at high levels (39, 50, 64, 111). The role of Aeromonas spp. as a foodborne pathogen is still unclear but appears to be primarily a concern with immunocompromised individuals. The prevalence of Aeromonas in the intestinal tract of live birds has been reported to be low (131), suggesting that the processmg environment may be an important source. REFERENCES 1. Bailey, J. S., J. O. Reagen, J. O. Carpenter, and G. A. Schuler Microbiological condition of broilers as influenced by vacuum and carbon dioxide in bulk shipping packs. J. Food Sci. 44: Bailey, J. S., J. E. Thomson, and N. A. Cox Contamination of poultry during processing. In The Microbiology of Poultry Meat Products. Cunningham, F. E., and N. A. Cox (eds.). Academic Press, Inc. Orlando, FL. pp Bailey, J. S., D. L. 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J. App!. Bacterio!. 44: Gibbs, P. A., J. T. Patterson, and J. K. Thompson. 1978b. The distribution of Staphylococcus aureus in a poultry processing plant. J. App!. Bacteriol. 44: Gibbs,P. A., J. T. Patterson, and J. K. Thompson. 1978c. Characterization of poultry isolates of Staphylococcus aureus by a new set of poultry phages. J. App!. Bacterio!. 44: Gill, C. 0., and L. M. Harris Hamburgers and broiler chickens as potential sources of human Campylobacter enteritis. 1. Food Prot 47: Grant, 1. H., N. J. Richardson, and V. D. Bokkenheuser Broiler chickens as potential source of Campylobacter infections in humans. 1. Clin. Microbio!. 11: Green, S. S., A. B. Moran, R. W. Johnston, P. Uhler, and J. Chiu The incidence of Salmonella species and serotypes in young whole chicken carcasses in 1979 as compared with Poult. Sci. 61: Hall, H. E., and R. Angellotti Clostridium perfringens in meat and meat products. App!. Microbio!. 13: Hlinninen, M. L Occurrence of Aeromonas spp. in samples of ground meat and chicken. Int. J. Food Microbio!. 18: Hart, C. D., G. C. Mead, and A. P. Morris Effects of gaseous environment and temperature on the storage behaviour of Listeria monocytogenes on chicken breast meat J. Appl. Bacterio!. 70: Harvey, J., J. T. Patterson, and P. A. Gibbs Enterotoxigenicity of Staphylococcus au reus strains isolated from poultry: Raw poultry carcasses as a potential food-poisoning hazard. J. App!. Bacterio!. 52: Hauschild, A. H. w., L. Niilo, and W. J. Dorward Clostridium perfringens type A infection of ligated intestinal loops in lambs. App!. Microbiol. 16: Hudson, W. R., and G. C. Mead Listeria contamination at a poultry processing plant. Lett App!. Microbio!. 9: Ingham, S. C., J. M. Escude, and P. McCown Comparative growth rates of Listeria monocytogenes and Pseudomonas fragi on cooked chicken loaf stored under air and two modified atmospheres. J. Food Prot. 53: Isigidi, B. K., A. M. Mathieu, L. A. Devriese, C. Godard, and J. van Hoof Enterotoxin production in different Staphylococcus aureus biotypes isolated from food and meat plants. J. App!. Bacterio!. 72: Izat, A. L., M. Colberg, C. D. Driggers, and R. A. Thomas Effects of sampling method and feed withdrawal period on recovery of microorganisms from poultry carcasses. J. Food Prot 52: Kakouri, A., and G. J. E. Nychas Storage of poultry meat under modified atmospheres or vacuum packs: Possible role of microbial metabolites as indicator of spoilage. J. App!. Bacterio!. 76: Keel, J. E., and C. F. Parmelee Improving the bacteriological quality of chicken fryers. J. Milk Food Techno!. 31: Kiggings, E. M., and W. N. Plastridge Effects of gaseous environment on growth and catalase content of Vibrio fetus cultures of bovine origin. J. Bacterio!. 72: Kim, J. W., and S. Doores Attachment of Salmonella typhimurium to skins of turkey that had been defeathered through three different systems: Scanning electron microscopic examination. J. Food Prot 56: Kim, J. w., M. F. Slavik, C. L. Griffis, and J. T. Walker Attachment of Salmonella typhimurium to skins of chicken scalded at various temperatures. J. Food Prot. 56: Kinde, H., C. A. Genigeorgis, and M. Pappaioanou Prevalence of Campylobacter jejuni in chicken wings. App!. Environ. Microbio!. 45: Kirov, S. M., M. J. Anderson, and T. A. McMeekin A note on Aeromonas spp. from chickens as possible foodborne pathogens. J. App!. Bacterio!. 68: Knoop, G. N., C. E. Parmelee, and W. J. Stadelman Microbiological characteristics of wet- and dry-chilled poultry. Poult Sci. 50: Leistner, L., H. Hechelmann, M. Kashiwazaki, and R. Albertz Nachweis von Yersinia enterocolitica in faeces und fleisch von schweinen, rindern und gefluge!. Die Fleischwirtschaft 55: Liang, O. D., F. Ascencio, R. Vazquez-Juarez, and T. Wadstrom Binding of collagen, fibronection, lactoferrin, laminin, vitronectin, and heparan sulphate to Staphylococcus au reus strain V8 at various growth phases and under nutrient stress conditions. Zb!. Bakt 279: Lillard, H. S Occurrence of Clostridium perfringens in broiler processing and further processing operations. J. Food Sci. 59: Lillard, H. S Effect of broiler carcasses and water of treating chiller water with chlorine or chlorine dioxide. Poult. Sci. 59: Lillard, H. S Bacterial cell characteristics and conditions influencing their adhesion to poultry skin. 48: Lillard, H. S. 1988a. Effect of surfactant or changes in ionic strength on the attachment of Salmonella typhimurium to poultry skin and muscle. J. Food Sci. 53: Lillard, H. S. 1988b. Comparison of sampling methods and implications for bacterial decontamination of poultry carcasses by rinsing. J. Food Prot 51:

12 590 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS 73. Lillard, H. S. 1989a. Incidence and recovery of Salmonellae and other bacteria from commercially processed poultry carcasses at selected pre- and postevisceration steps. J. Food Prot. 52: Lillard, H. S. 1989b. Factors affecting the persistence of Salmonella during the processing of poultry. J. Food Prot. 52: Lillard, H. S The impact of commercial processing procedures on the bacterial contamination and cross-contamination of broiler carcasses. J. Food Prot. 53: Lillard, H. S Bactericidal effect of chlorine on attached Salmonellae with and without sonification. J. Food Prot. 56: Lillard, H. S., L. C. Blankenship, J. A. Dickens, S. E. Craven, anda. D. Shackelford Effect of acetic acid on the microbiological quality of scalded picked and unpicked broiler carcasses. J. Food Prot. 50: Ljungh, A., L. Emody, P. Aleljung, O. Olusanya, and T. Wadstrom Growth conditions for the expression of fibronectin, collagen type I, vitronectin, and 1aminin binding to Escherichia coli strain NG7C. Curr. Microbiol. 22: McBride, G. B., B. Brown, and B. J. Skura Effect of bird type, growers, and season on the incidence of Salmonellae in turkeys. J. Food Sci. 43: McBride, G. B., B. J. Skura, R. Y. Yada, and E. J. Bowmer Relationship between incidence of Salmonella contamination among prescalded, eviscerated and postchilled chickens in a poultry processing plant. J. Food Prot. 43: McMeekin, T. A Spoilage association of chicken breast muscle. App!. Microbiol. 29: McMeekin, T. A Spoilage association of chicken leg muscle. Appl. Environ. Microbiol. 33: McMeekin, T. A Microbial spoilage of meats. In Developments in Food Microbiology-I. R. Davies (ed.). Appl. Sci. Pub. London. pp McMeekin, T. A., P. 1. Pennington, and C. J. Thoman Effect of potassium sorbate on the microbiology of vacuum-packed poultry. J. Food Safety 6: McNab, W. B., S. A. Renwick, H. R. Lowman, and R. C. Clarke Variability of broiler carcass bacterial load at three abattoirs, as measured by a hydrophobic grid membrane filter interpreter. J. Food Prot. 56: McVicker, R. J., L. E. Dawson, W. L. Mallmann, S. Walters, and E. Jones Effect of certain bacterial inhibitors on shelf life of fresh fryers. Food Technol. 12: May, J. D., S. L. Branton, J. W. Deaton, and J. D. Simmons Effect of environmental temperature and feeding regimen on quantity of digestive tract contents of broilers. Poult. Sci. 67: May, K. N Skin contamination of broilers during commercial evisceration. Poult. Sci. 40: May, K. N Changes in microbial numbers during final washing and chilling of commercially slaughtered broilers. Poult. Sci. 53: Mead, G. C Hygiene aspects of the chilling process. Qual. Poult. Meat, Proc. Eur. Symp. Poult. Meat, 2nd, Oosterbeck, The Netherlands, pp Mead, G. C., and C. E. R. Dodd Incidence, origin and significance of Staphylococci in processed poultry. J. Appl. Bacteriol. Symp. Supplement 81S-9IS. 92. Mead, G. C., and C. S. Impey The distribution of Clostridia in poultry processing plants. Br. Poult. Sci. 11: Mead, G. C., and N. L. Thomas Factors affecting the use of chlorine in the spin chilling of eviscerated poultry. Br. Poult. Sci. 14: Morris, G. K., and J. G. Wells Salmonella contamination in a poultry-processing plant. Appl. Microbiol. 19: Morris, G. K., B. L. McMurray, M. M. Galton, and 1. G. Wells A study of the dissemination of salmonellosis in a commercial broiler chicken operation. Am. J. Vet. Res. 30: Mulder, R. W. A. W Decrease microbial contamination during poultry processing. Poult. (March): Mulder, R. W. A. w., and L. W. J. Dorresteijn Hygiene beim bruhen von schlachtgeflugel. (Hygiene during the scalding of broilers.) Die Fleischwirtschaft 57: Mulder, R. W. A. W., and C. H. Veerkamp Improvements in poultry slaughterhouse hygiene as a result of cleaning before cooling. Poult. Sci. 53: Mulder, R. W. A. W., L. W. J. Dorresteijn, and J. van der Brock Cross-contamination during the scalding and plucking of broilers. Br. Poult. Sci. 19: Mulder, R. W. A. w., M. C. van der Hulst, and N. M. Bolder Salmonella decontamination of broiler carcasses with lactic acid, L-cystein, and hydrogen peroxide. Poult. Sci. 66: NACMCF. 1994c. Campylobacter jejunilcoli. J. Food Prot. 57:12: Nilsson, T., and B. Regner The effect of chlorine in the chilling water on Salmonellae in dressed chicken. Acta Vet. Scand. 4: Norberg, P Enteropathogenic bacteria in frozen chicken. Appl. Environ. Microbiol. 42: Notermans, S., and E. H. Kampelmacher Attachment of some bacterial strains to the skin of broiler chickens. Br. Poult. Sci. 15: Notermans, S., F. M. van Leusden, M. van Schothorst, and E. H. Kampelmacher. 1975a. Salmonella-contaminatie van slachtkuikens tijdens het slachtproces in enkele pluimvesslachterijen. (Contamination of broiler chicken by Salmonella during processing in a number of poultry-processing plants.) Tijdschr. Diergeneesk. 100: Notermans, S., M. van Schothorst, and E. H. Kampelmacher. 1975b. Der einfluss des keimgehaltes des spinchiller-wassers auf den keimgehalt des tauwassers von gefrierhahnchen. (The influence of the bacterial content of spin-chiller water on the bacterial content of thaw water from frozen chickens.) Die Fleischwirtschaft 55: Notermans, S., F. M. van Leusden, and M. van Schothorst Suitability of different bacterial groups for determining faecal contamination during postscalding stages in the processing of broiler chickens. J. AppL Bacteriol. 43: Notermans, S., R. J. Terbijhe, and M. van Schothorst Removing faecal contamination of broilers by spray cleaning during evisceration. Br. Poult. Sci. 21: Notermans, S., J. Dufrenne, and W. van Leeuwen Contamination of broiler chickens by Staphylococcus aureus during processing: Incidence and origin. J. Appl. Bacteriol. 52: Oosterom, J., G. J. A. de Wilde, E. de Boer, L. H. de Blaauw, and H. Karman Survival of Campylobacter jejuni during poultry processing and pig slaughtering. J. Food Prot. 46: Ill. Palumbo, S. A., F. Maxino, A. C. Williams, R. L. Buchanan, and D. W. Thayer Starch-ampicillin agar for the quantitative detection of Aeromonas hydrophila. Appl. Environ. Microbiol. 50: Papa, C. M., and J. A. Dickens Lower gut contents and defecatory responses of broiler chickens as affected by feed withdrawal and electrical treatment at slaughter. Poult. Sci. 68: Parks, C. E., Z. K. Stankiewicz, J. Lovett, and J. Hunt Incidence of Campylobacter jejuni in fresh eviscerated whole market chickens. Can. J. Microbiol. 27: Patterson, J. T Bacterial flora of chicken carcasses treated with high concentrations of chlorine. J. Appl. BacterioL 31: Patti, J. M., T. Bremell, D. Krajewska-Pietrasik, A. Abdelnour, A. Tarkowski, C. Ryden, and M. Hook The Staphylococcus aureus collagen adhesion is a determinant in experimental septic arthritis. Infect. Immun. 62: Pini, P. N., and R. J. Gilbert A comparison of two procedures for the isolation of Listeria monocytogenes from raw chickens and soft cheeses. Int. 1. Food MicrobioL 7: Renwick, S. A., W. B. McNab, H. R. Lowman, and R. C. Clarke Variability and determinants of carcass bacterial load at a poultry abattoir. J. Food Prot. 56: Rigby, C. E., and J. R. Pettit Effects of feed withdrawal on the weight, fecal excretion and Salmonella status of market age broiler chickens. Can. 1. Compo Med. 45: Sadler, W. W., R. Yamamoto, H. E. Adler, and G. F. Stewart Survey of market poultry for Salmonella infection. AppL Microbiol. 9:72-76.

13 HACCP IN BROILER SLAUGHTER AND PROCESSING Sadler, W. W., and R. E. Corstvet Second survey of market poultry for Salmonella infection. App!. Microbio!. 13: Sanders, D. H., and C. D. Blacksher Effect of chlorination in the final washer on bacterial counts of broiler chicken carcasses. Poult. Sci. 50: Sanderson, K., C. J. Thomas, and T. A. McMeekin Molecular basis of the adhesion of Salmonella serotypes to chicken muscle fascia. Biofouling 5: Sawaya, W. N., A. S. Abu-Ruwaida, A. J. Hussain, M. S. Khalafawi, and B. H. Dashti Shelf life of vacuum-packaged eviscerated broiler carcasses under simulated market storage conditions. J. Food Safety 13: Schuler, G. A., and A. F. Badenhop Microbiology survey of equipment in selected poultry processing plants. Pou!. Sci. 51: Seneviratna, P., J. Robertson, I. D. Robertson, and D. J. Hampson Listeria species in foods of animal origin. Aust. Vet. J. 67: Shanker, S., J. A. Rosenfield, G. R. Davey, and T. C. Sorrel! Campylobacter jejuni: Incidence in processed broilers and biotype distribution in human and broiler isolates. App!. Environ. Microbio!. 43: Shen, w., and A. Ljungh Collagen binding to Escherichia coli strain NG7C. Curro Microbio!. 27: Simmons, N. A., and F. J. Gibbs Campylobacter spp. in oven-ready poultry. J. Infect. 1: Simonsen, B Microbiological aspects of poultry meat quality. Qua!. Poult. Meat Proc. Eur. Symp. Poultry Meat Qua!., 2nd, Oosterbeck, Netherlands, 2: Stern, N. J Influence of season and storage on Campylobacter contaminating broiler carcasses. J. App!. Poult. Res. (In press) Stern, N. J., E. S. Drazek, and S. W. Joseph Low incidence of Aeromonas sp. in livestock feces. J. Food Prot. 50: Strong, D. H., J. C. Canada, and B. B. Griffiths Incidence of Clostridium perfringens in American foods. Appl. Microbio!. 11: Studer, P., R. E. Schmidt, L. Gallo, and W. Schmidt-Lorenz Microbial spoilage of refrigerated fresh broilers. II. Effect of packaging on microbial association of poultry carcasses. Lebensmit.- Wissenschaft Techno!. 21 : Surkiewicz, B. F., R. W. Johnston, A. B. Moran, and G. W. Krumm A bacteriological survey of chicken eviscerating plants. Food Techno!. 23: Svedhiem, A., and B. Kaijser Campylobacter fetus subspecies jejuni. A common cause of diarrhea in Sweden. J. Infect. Dis. 142: Thomas, C. J., and T. A. McMeekin Attachment of Salmonella spp. to chicken muscle surfaces. App!. Environ. Microbio!. 42: Thomas, C. J., T. A. McMeekin, andj. T. Patterson Prevention of microbial contamination in the poultry processing plant. In Elimination of Pathogenic Organisms from Meat and Poultry. F. J. M. Smulders (ed.). Elsiever, Amsterdam. pp Thompson, J. K., P. A. Gibbs, and J. T. Patterson Staphylococcus aureus in commercial laying flocks: Incidence and characteristics of strains isolated from chicks, pullets, and hens in an integrated commercial enterprise. Br. Poult. Sci. 21: Thomson, J. E., A. J. Mercuri, J. A. Kinner, and D. H. Sanders Effect of time and temperature of commercial continuous chilling of fryer chickens on bacterial counts. Poult. Sci. 44: Thomson, J. E., G. J. Banwart, D. H. Sanders, and A. J. Mercuri Effect of chlorine, antibiotics, l3-propiolactone, acids and washing on Salmonella typhimurium on eviscerated fryer chickens. Poult. Sci. 46: Thomson, J. E., W. K. Whitehead, anda. J. Mercuri Chilling poultry meat-a literature review. Poult. Sci. 53: Thomson,J. E., N.A. Cox, W. K. Whitehead,A. J. Mercuri, andb. J. Juven Bacterial counts and weight changes of broiler carcasses chilled commercially by water immersion and air blast. Poult. Sci. 54: Tompkin, R. B Control by chlorination. In "Proceedings of the International Symposium on Salmonella and Prospects for Contro!. University of Guelph, Guelph, Canada, pp van Schothorst, M., S. Notermans, and E. H. Kampelmacher Einige hygienische aspekte der gefliigelschlactung (Hygiene in poultry slaughter). Die Fleischwirtschaft 52: Varbioff, y Incidence and recovery of Listeria from chicken with a pre-enrichment technique. J. Food Prot. 53: Walker, W. H., and J. C. Ayres Incidence and kinds of organisms associated with commercially dressed poultry. App!. Microbio!. 4: Walls, I., P. H. Cooke, R. C. Benedict, and R. L. Buchanan. 1993a. Sausage casings as a model for attachment of Salmonella to meat. J. Food Prot. 56: Walls, I., P. H. Cooke, R. C. Benedict, and R. L. Buchanan. 1993b. Factors affecting attachment of Salmonella typhimurium to sausage casings. Food Microbio!. 10: Wempe, J. M., C. A. Genigeorgis, T. B. Farver, and H. I. Yusufu Prevalence of Campylobacter jejuni in two California chicken processing plants. App!. Environ. Microbio!. 45: Wilder, A. N., and R. A. MacCready Isolation of Salmonella from poultry. Poultry products and poultry processing plants in Massachusetts. N. Eng!. J. Med. 274: Wimpfheimer, L., N. S. Altman, and J. H. Hotchkiss Growth of Listeria monocytogenes Scott A., serotype 4 and competitive spoilage organisms in raw chicken packaged under modified atmospheres and in air. Int. J. Food Microbio!. 11: Yusufu, H. I., C. Genigeorgis, T. B. Farver, and J. M. Wempe Prevalence of Campylobacter jejuni at different sampling sites in two California turkey processing plants. J. Food Prot. 46: Zeitoun, A. A. M., and J. M. Debevere Decontamination with lactic acid/sodium lactate buffer in combination with modified atmosphere packaging effects on the shelf life of fresh poultry. Int. J. Food Microbio!. 16: Ziegler, F., and W. J. Stadelman The effect of different scald water temperatures on the shelf life of fresh, non frozen fryers. Poult. Sci. 34: HAZARD ANALYSIS The information in sections II and III has been used in the hazard analysis. The epidemiological data in section II indicate that there are two public health concerns associated with raw poultry. One involves outbreaks of foodborne illness; the other involves sporadic cases of foodborne illness. Three bacterial agents, Salmonella, S. aureus, and C. perfringens, accounted for 90% of the poultry or chicken related outbreaks for which a bacterial agent has been identified (1). Although all three pathogens can be present on raw poultry, the major source of S. aureus associated with outbreaks is believed to be food handlers during food preparation at the consumer level. The illness associated with C. perfringens involves an enterotoxin which is produced after a large number of vegetative cells are consumed, and they subsequently sporulate in the intestinal tract. Thus, for illness to occur, the poultry product must be held for a sufficient length of time in the temperature range (i5-50 D C) for multiplication to grow to high numbers (e.g., 2:10 6 /g) in the food. This information indicates that the rate of cooling and subsequent holding temperatures of cooked poultry products are the most important factors in preventing illness from C. perfringens. This pathogen is widespread in nature and the source of C. perfringens in outbreaks is not limited to raw poultry. Environmental contamination and other ingredients used by the consumer can also serve as sources of C. perfringens. Therefore, the most effective control is proper food handling at the level of final food preparation and handling.

14 592 NATIONAL ADVISORY COMMITIEE ON MICROBIOLOGICAL CRITERIA FOR FOODS Sporadic cases of foodbome illness are rarely reported. Available information, however, indicates that campylobacteriosis occurs primarily as sporadic cases and has been associated with improperly cooked or handled poultry products. Case control studies suggest that undercooked poultry may be involved in human listeriosis in persons who are highly susceptible because of pregnancy or an underlying illness (2, 3). This has not been confirmed in the U.S., and there have been no studies to demonstrate the number or presence of L. monocytogenes in "undercooked" poultry. C. jejuni and most serovars of Salmonella are nonpathogenic to live poultry. Thus, the birds appear normal when received at the plant for processing. These pathogens are associated with the intestinal tracts of live birds and can be present on the feathers of the birds at the time of receipt at the plant. Thus, an important goal during the slaughtering process is to remove the feathers and intestinal tract from the birds in a manner that will minimize contamination of the raw poultry with these pathogens. Subsequent steps in processing should also focus on minimizing and reducing contamination. The foregoing leads to the conclusion that raw poultry serves as a significant source and processing provides a practical level of control for two microbiological hazards, Salmonella and C. jejuni. Foodbome illness from Salmonella and C. jejuni consists of an infection of the human intestinal tract, and infectious doses appear to involve a small number of cells. Salmonella can grow in raw and cooked poultry products if held at appropriate temperatures (about 7 to 46 C). Higher numbers can increase the severity of an outbreak of illness. Multiplication of C. jejuni is not likely to occur due to its higher temperature limit for growth and more fastidious growth requirements. This information indicates that adequate cooking and preventing crosscontamination from raw poultry to cooked poultry or other ready-to-eat foods are important factors to control in preventing illness from these bacteria. REFERENCES 1. Bean, N. H., and P. M. Griffin Foodborne disease outbreaks in the United States, : Pathogens, vehicles, and trends. J. Food Prot. 53: Gellin, B. G., C. V. Broome, W. F. Bibb, R. E. Weaver, S. Gaventa, L. Mascola, and the Listeriosis Study Group The epidemiology of listeriosis in the United States Amer. J. Epidem. 133 : Schuchat,A., B. Swaminathan, and C. V. Broome Role of foods in sporadic listeriosis. I. Case-control study of dietary risk factors. JAMA267: GENERIC HACCP FOR SLAUGHTER AND PROCESSING Operations associated with broiler chicken slaughter, cut-up and boning are summarized in Figure 1. A CCP within a Hazard Analysis and Critical Control Point (HACCP) plan is defined as any point, step, or procedure at which control can be applied and a food safety hazard can be prevented, eliminated, or reduced to accept- FIGURE CCP-2 ANAL WASHER INSIDEIOUTSIDE 1. Process flowchart for broiler chicken slaughter. able levels (12). Six CCPs have been identified in the slaughter and processing of broilers (Figure I and Table 1). These include venting/opening/evisceration, final wash, chilling, cut-up/boning/packing/product chilling, labeling, and refrigerated storage. Critical limits are defined for each of the CCPs. Ideally, CCPs are monitored on a continuous basis. However, for several of the identified CCPs, this is not feasible. In such instances, the CCPs must be monitored at a frequency sufficient to ensure process control. Corrective actions to be taken when CCPs do not meet critical limits should be specified clearly in the HACCP plan. This should include the priorities of actions to be taken and the individuals to be notified of the deviation. The HACCP system should be verified according to HACCP principle #7 (12). The six CCPs with procedures associated with the processing step are described in the following outline. The effectiveness of the CCPs outlined in this document is based on the concept of additive impact (13). It takes the integrated control of all of the CCPs to effectively reduce and control microbiological risks associated with raw broilers. IMPLEMENTATION AND MANAGEMENT OF HACCP CRITICAL CONTROL POINTS WASH CCP 1: Venting/Opening/Evisceration. The intestinal tract is a major source of enteric pathogens during the slaughter process. During this step the body cavity is opened and the viscera are drawn out and exposed for inspection. During this primarily mechanical process, intestinal contents can leak onto the carcass from the vent or ruptured intestines

15 HACCP IN BROILER SLAUGHTER AND PROCESSING 593 contaminating equipment, workers, and inspectors, and leading to subsequent cross-contamination (8, 15). Proper equipment operation is essential to minimize intestinal leakage. Continuous rinsing of equipment with chlorinated water helps to minimize cross-contamination. Assurance of adequate feed withdrawal periods prior to slaughter can enhance the effectiveness of this step. Corrective action for this CCP involves adjusting equipment, slowing line speeds, or adding operators to assure that the defect rate is below the critical limit. In addition, it is imperative that trained operators adequately reprocess all defective carcasses in accordance with the defect protocols established in their HACCP plan. Proper reprocessing reduces pathogen numbers to levels not significantly different from those of contaminated carcasses (3, 4). Care must be exercised during subsequent separation of the entire gastrointestinal tract from the heart, liver, and gizzard to prevent contamination of the carcass surfaces (8). Giblet removal, washing, chilling, and stuffing were excluded from consideration of a CCP because the Committees emphasis was on carcass processing only. CCP2: Final washer. An in-line, potable water wash containing 20 ppm chlorine at ambient temperature reduces total counts and limits pathogen cross-contamination (2, 6, 9, 11, 14). This final wash with chlorinated water also helps minimize carriage of pathogens into the chiller and through the cut-up, boning and packing of product. Monitoring of this CCP involves assuring that water flow rates, spray patterns, and residual chlorine levels are maintained at specific levels and that visible defects are adequately removed from carcasses during washing. Corrective actions involve adjusting chlorine levels, slowing lines and/or adding operators, adjusting/correcting spray nozzles, and trimming defects on-line or directing defective carcasses to reprocessmg. CCP3: Chilling. Current USDA poultry slaughter guidelines require achieving a deep breast muscle temperature of :::;40 F CC) within 1-2 hours following evisceration. This cooling rate will prevent the growth of enteric pathogens. In-line immersion chillers contain:ing sufficient chlorine to achieve 2: I ppm of residual chlorine in the overflow water will significantly reduce total counts on the product and control cross-contamination by pathogens (7, 9). This CCP is monitored by measuring overflow rates, monitoring chlorine levels in overflow water, and measuring temperature in the breast. Corrective actions include adjustment of input water flow rate, chlorine meter adjustment, adjustment of chiller temperature or addition of ice to attain proper carcass temperature. Properly chilled carcasses reduce the risk of pathogen growth during subsequent cut-up, boning, and packaging. CCP4: Cut-up/boning/packing/re-chilling. Cutting, boning, packing, and rechilling can be a source of contamination from equipment and operators. Timely movement of product is necessary to minimize temperature rise, avoid product accumulation, and, thus, prevent pathogen growth. Prompt movement of packaged product to refrigerated storage to return the surface temperature to :s;40 F will control pathogen growth. Accumulated. product temperature and the temperature of the packaged product chill room should be monitored. The specific critical limit for this CCP should assure that there is insufficient time for enteric pathogens to multiply. Corrective actions may include icing of product, flow correction to prevent product accumulation, and adjustment of chill room temperature. It is recommended that cut-up/boning/packing rooms be refrigerated to minimize risks of excessive product warming. CCP5: Labeling. Accurate product identification (e.g., code dates, lot identification) is essential to facilitate product control if it becomes necessary to trace and retrieve product. In accordance with prior recommendations (13) for enhancing product safety throughout distribution and consumption, all raw poultry products should be labelled with instructions for use by distributors, retailers, food service operators, and consumers. These instructions should state that the product must be refrigerated, handled, and cooked properly to ensure safety. The labels should be appropriate for the targeted retail or institutional customers and should provide adequate cooking and sanitary handling instructions. The consumer safe handling labels recently required by the USDA for all raw and partially cooked meat and poultry products meet the essential requirements for this CCP (16). The CCP is monitored by visual inspection of the labeling operation and recording of code dates on daily production reports. Corrective action for this CCP involves relabeling incorrectly labeled product since the last check when the labels were correct and placing the instructional label on packages lacking the proper label. CCP6: Refrigerated storage. Following chilling, all raw or partially cooked products must be kept refrigerated at s40 F throughout the various stages of handling and distribution. Because this CCP involves adherence to control parameters by diverse groups, such as manufacturers, distributors, retailers, food service operators, and consumers, each group must be responsible for keeping the products adequately refrigerated. Adequate refrigeration maintained as close to freezing as possible will also enhance control of psychrotrophic pathogens. Product temperature or storage facility temperature should be monitored at a frequency sufficient to maintain process control, ideally on a continuous basis. Scalding was seriously considered as a potential CCP. However, evaluation of available data indicated that it was not possible to establish a scientifically valid critical limit and that this process step did not contribute to the concept of additive impact. The feathers and skin of broilers carry a microflora indicative of the environment of the farm and specific house in which the chickens were raised. During scalding, carcasses are immersed in hot water which facilitates subsequent feather removal. Numerous studies have shown that the general levels of bacteria and some specific pathogens are reduced during scalding and that some cross-contamination occurs (1, 10, 18). However, the temperature of the water is self-limiting in that feather removal becomes impossible if the temperature is too low, and unacceptable skin damage results if it is too high. Accord-

16 594 NATIONAL ADVISORY COMMITIEE ON MICROBIOLOGICAL CRITERIA FOR FOODS TABLE I. Generic HACC? plan critical control points for whole bird poultry slaughter and processing Monitoring Process step CCP Criticallimi ts procedure/ frequency Corrective action Records CCP verification Venting, opening, CCPI ~2% of carcasses Operator observes Adjust equipment Carcass defect log. Examination of and eviscera- with visible con- carcasses for and/or chlori- Chlorination log. random carcasses tion tamination from defects. nator. after evisceration the intestinal tract Operator records Slow line and/or using sampling (below the giz- chlorine level at add operators. plan sufficient to zard). least two times Trained employees assure process All equipment per shift. trim defects or control. should be con- direct carcasses Supervisory review tinuously rinsed to reprocessing. of records each with ambient shift. temperature Review defect conwater containing trol charts to con- 2:20 ppm chlo- firm that samrine or other piing frequency is demonstrably sufficient to effective dis in- detect 2% defect fectant. criteria. Final washer CCP2 2: ppm chlo- Record chlorine Adjust chlorine Chlorine concentra- Supervisory daily rine water at levels and surface concentration tion and surface review of ambient tempera- coverage 4 times in wash water. coverage logs. records. ture or other per shift. Adjust washer Carcass defect log. Periodic microbial demonstrably Hourly logs for coverage. assays for aerobic effective antimi- defects on car- Slow line and/or mesophiles crobial. casses. add operators. and/or Entero- Sufficient coverage Trained employees bacteriaceae to to flush external trim defects or confirm an and internal car- direct carcasses adequate reduccass surfaces. to reprocessing. tion in bacterial ~0.5% of carcasses numbers. with visible Periodic testing of digestive tract equipment to (below the giz- ensure operation zard) contamina- in accordance tion. with design specifications. Chilling CCP3 Water flow rates per Continuous Adjust flow rate. Log/chart of water Supervisory daily FSIS regulations recording water Adjust line speed, flow rates. review of (one-half gallon flow rate and log add ice, or adjust Carcass temperature records. per broiler). of water flow rate chiller to attain log. Periodic calibration Exit carcass tem- checks twice per proper carcass Chlorine content of of temperature perature: ~40 F shift. exit temperature. overflow water monitoring internal in the Measurement of Place product on log. devices. center of the internal carcass hold (i.e., retain, Carcass defect log. Periodic testing of breast muscle. temperature at rechill, or equipment for 2: I ppm residual least once per destroy). proper operation. chlorine in over- hour. Periodic microbial flow water (or Operator records assays for aerobic other demon- chlorine level at mesophiles strablyeffective overflow at least and/or enterobacantimicrobial). two times per teriaceae to conshift. firm an adequate reduction in bacterial numbers. ingly, the prime determinant of this process step is product quality. Safety is a secondary issue. Minimum water overflow rates are already specified by the USDA. Counterflow scalders followed by a washer have been shown to be a significant innovation, reducing total counts and the levels of certain pathogens (5, 17). The NACMCF recommends highly that a counterflow scalder followed by a washer be required in all plants.

17 HACCP IN BROILER SLAUGHTER AND PROCESSING 595 TABLE I. (Continued) Monitoring Process step CCP Critical limits procedurel frequency Corrective action Records CCP verification Cut-up, boning, CCP4 Product internal Record product and packaging temperature temperature four :s50 F. times per shift. Adequate move- Record product ment of product accumulation to prevent pile four times per up. In rooms not shift. below 50 F, rinse Record room temall equipment at perature four midshift breaks. times per shift. Labeling/code CCP5 Safe handling label At start of operadating on all packages. tion, visual check Accurate product for accurate date date to assure lot and safe handling identification. label. Periodic check to assure label is affixed correctly. Visual check for accurate lot identification at start of each new lot. Refrigerated CCP6 Product temperature Record product storage. of :S40 F. temperature each shift. Continuous monitoring of storage facility temperature. Place product on hold (i.e., retain), rechill, or destroy. Ice product or increase flow rate. Rearrange flow to prevent accumulation. Correct label Place product on hold (i.e., retain, release, or destroy). Adjust temperature of storage facility. Temperature records. Accumulation log. Product disposition log. Labeling/code records. date Temperature records. Product disposition records. Supervisory review of records each shift. Supervisory review of the adequacy of equipment rinse down for each shift having rooms over 50 F. Supervisory review of records each shift. Supervisory daily review of temperature charts. Periodic calibration of temperature monitoring devices. Periodic microbial assays for aerobic mesophiles and/or Enterobacteriaceae to verify process control. REFERENCES I. Bailey, J. S., J. E. Thomson, and N. A. Cox Contamination of poultry during processing. In The Microbiology of Poultry Meat Products. F. E. Cunningham and N. A. Cox (eds.). Academic Press, Inc. Orlando, FL. pp Barnes, E. M., and C. S. Impey The shelf-life of uneviscerated and eviscerated chicken carcasses stored at 10 C and 4 C. Br. Poult. Sci. 16: Blankenship, L. C., N. A. Cox, S. E. Craven, A. J. Mercuri, and R. L. Wilson Comparisonof the microbiologicalquality of inspectionpassed and fecal contamination-condemned broiler carcasses. J. Food Sci. 40: Blankenship, L. C., J. S. Bailey, N. A. Cox, M. T. Musgrove, M. E. Berrang, R. L. Wilson, M. J. Rose, and S. K. Dua Broiler carcass reprocessing, a further evaluation. J. Food Prot. 56: James, W.O., W. O. Williams, Jr., J. C. Prucha, R. Johnston, and W. Christensen Profile of selected bacterial counts and Salmonella prevalence on raw poultry in a poultry slaughter establishment. J. Am. Vet. Med. Assoc. 200: Keel, J. E., and C. F. Parmelee Improving the bacteriological quality of chicken fryers. J. Milk Food Techno\. 31: Lillard, H. S The impact of commercial processing procedures on the bacterial contamination and cross-contamination of broiler carcasses. J. Food Prot. 53: May, K. N Skin contamination of broilers during commercial evisceration. Poult. Sci. 40: May, K. N Changes in microbial numbers during final washing and chilling of commercially slaughtered broilers. Poult. Sci. 53: Mulder, R. W. A. W., and C. H. Veerkamp Improvements in poultry slaughterhouse hygiene as a result of cleaning before cooling. Poult. Sci. 53: II. Mulder, R. W. A. w., Dorresteijn, L. W. J., Hofmans, G. J. P., and Veerkamp, C. H Experiments with continuous immersion chilling of broiler-carcasses according to the code of practice. J. Food Sci. 41: NACMCF (National Advisory Committee on Microbiological Criteria for Foods) Hazard analysis and critical control point system. Int. J. Food Microbio\. 16: NACMCF (National Advisory Committee on Microbiological Criteria for Foods). 1994b. 14. Sanders, D. H., and C. D. Blacksher Effect of chlorination in the final washer on bacterial counts of broiler chicken carcasses. Poult. Sci. 50: Schuler, G. A., and A. F. Badenhop Microbiology survey of equipment in selected poultry processing plants. Poult. Sci. 51: USDA (Food Safety and Inspection Service) Mandatory safe

18 596 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS handling statements on labelling of raw meat and poultry products. Fed. Register 59(59): ] Waldrop, A. L., B. M. Rahgeber, R. H. Forsythe, and L. Smoot Effects of six modifications on the incidence and levels of spoilage and pathogenic organisms on commercially processed post chill broilers. J. App!. Poult. Res. 1: Walker, W. H., and J. C. Ayres Incidence and kinds of organisms associated with commercially dressed poultry. App!. MicrobioI. 4: GUIDELINES FOR DISTRIBUTION, AND PREPARATION RETAILING, An effective HACCP plan for the production, slaughter, and initial processing of raw chicken will greatly increase control of pathogenic microorganisms. However, even under the best operating conditions, low numbers of pathogens may be present on the carcass. Mter slaughter and processing, raw chicken goes through a complex system of distribution and marketing (including wholesalers, distributors, retail food stores, and food service establishments) before ultimately reaching the individuals who consume these products. Throughout the distribution system and during the preparation of raw chicken, there is a significant potential for product mishandling, leading to the introduction of additional pathogenic microorganisms or the spread to other foods of any pathogens remaining on raw chicken. Improper handling and storage practices, including improper holding temperatures, inadequate cooking, contaminated equipment, and food worker hygiene, have all contributed to chicken-associated foodborne outbreaks (1). The microbiological hazards associated with raw chicken can be controlled by extending HACCP principles to product handling activities in retail stores, food service establishments, institutional feeding facilities, and homes. The goal of the HACCP system in food distribution and preparation is to minimize microbial contamination, reduce the opportunities for pathogens that may be present to multiply, assure the destruction of pathogenic microorganisms through proper cooking procedures, and prevent the cross-contamination of pathogens from raw to cooked, ready-to-eat foods. HACCP properly applied to all segments of distribution and preparation has the potential for (i) reducing the opportunities for pathogen growth, thereby reducing the risk of foodborne disease; (ii) assuring the destruction of enteric and other non-spore-forming pathogens through proper cooking procedures; (iii) preventing the reintroduction of pathogens to the cooked product and cross-contamination of other foods; and, (iv) controlling the growth of sporeforming pathogens (e.g., C. perfringens) by the use of proper time/temperature relationships for storage, holding, and servmg. An effective HACCP system in food distribution and preparation depends on a general understanding of and adherence to the principles of sanitation, good manufacturing and food preparation practices, and proper facility layout, equipment design, and maintenance (see Appendices A and B) (2). Thorough education and training of all personnel is critical to the processing and effectiveness of any HACCP program. HACCP plans for handling and processing raw chicken should be developed and implemented by food retailers and food service establishments as the optimal system for assuring food safety. In institutional feeding operations, such as hospitals, nursing homes, day care centers and prisons, where the populations may be more vulnerable to foodborne disease, special care must be taken in preparing all foods, including raw chicken products. The Committee recommends that HACCP systems be implemented immediately by food service establishments and institutions preparing foods for these special groups with increased susceptibility. The Food Code developed by the FDA provides specific guidelines for the safe handling and preparation of foods and is a useful reference (2). General guidelines for the safe handling of raw chicken in retail food stores and food service establishments are provided in Appendix B. Several national surveys (3, 4) have shown that the public has a limited understanding of the basic principles of food microbiology and safe home food handling and preparation practices. In households, the successful use ofhaccp principles depends on the interest, knowledge, and skills of the food preparer. General guidelines for the safe handling of raw chicken by consumers are provided in Appendix C. REFERENCES I. Bryan, F. L Risks of practices, procedures, and processes that lead to outbreaks of foodbome diseases. J. Food Prot. 51 : USPHS, FDA The Food Code. 3. Weimer, J., and J. Jones Food safety: Homemaker attitudes and practices. USDA Report No. 360, p Williamson, D. M., R. B. Gravani, and H. T. Lawless Correlating food safety knowledge with home food preparation practices. Food Techno!. 46(5): ROLE OF REGULATORS AND INDUSTRY IN A BROILER PROCESSING HACCP SYSTEM It is recommended that the poultry slaughter and processing industries and the associated regulatory agency(s) adopt the principles of HACCP (1) and the roles of regulatory agencies and industry as described by the NAC- MCF (2). The NACMCF's recommendations include uniformity in adopting HACCP principles, the characteristics of a HACCP-based inspection program, and procedures to facilitate the adoption and implementation of HACCP. Industry has the primary responsibility for the development, implementation, and maintenance of an effective HACCP system for poultry slaughter, processing, packaging, and distribution. The system should consider the entire food system from production to consumption. Each facility should develop a HACCP team and provide for proper training in HACCP principles. It is the processor's responsibility to provide HACCP records to the regulatory agency(s). The processor must assure that the records are complete, accurate, and up-to-date. Records for review must include pertinent information for verification and revalidation of the HACCP plan. When necessary, amendments to the HACCP plan will be made in response to regulatory inspection.

19 HACCP IN BROILER SLAUGHTER AND PROCESSING 597 The primary role of the regulatory agency(s) is to verify that the processor's RACCP system is effective and working as intended. In general, this includes assurance that following the RACCP plan fulfills the intended purpose of providing a product that is safe when properly handled and prepared for consumption. The regulatory agency(s), in cooperation with industry and other RACCP experts, should be actively involved in promoting the RACCP principles and their application to assure uniformity and common understanding. Regulations and guidelines that are promulgated by the regulatory agency(s) should be consistent with the principles recommended by the NACMCF (1, 2). The focus of the regulatory agency(s) should be on those activities associated with verification of the RACCP system. The processor must make RACCP records available to the regulatory agency(s). These records would include the processor's RACCP plan, CCPs, critical limits, monitoring, deviations, product disposition, and corrective actions. The RACCP plan and associated processor records must be considered proprietary information that must not be made available outside the regulatory agency(s). Specific verification procedures may include establishing verification inspection schedules based on risk, review of the RACCP plan, review of CCP records, review of deviations and corrective actions, visual inspection of operations, sample collection, and analysis, review of critical limits, review of the processors verification records, review of revalidation of the RACCP plan, and review of RACCP plan modifications. The regulatory agency(s) should establish the manner and frequency of verification, the format for verification reports, and other activities based on the RACCP Subcommittee recommendations (1, 2). REFERENCES 1. NACMCF (National Advisory Committee on Microbiological Criteria for Foods) Hazard analysis and critical control point system. Int. J. Food Microbiol. 16: NACMCF The role of regulatory agencies and industry in HACCP. Int. J. Food Microbiol. 21 : New technologies and procedures for improved microbiological control will be addressed at the live poultry production level and at the slaughter and processing level. In addition, identification of flock source and product coding can be beneficial for determining the source of microbial pathogens. This section includes those new technologies or improvements in existing procedures which can be used during live bird production, slaughter, and processing to reduce contamination from current levels to lower levels. Poultry growers should be encouraged to have adequate moisture control for waste and litter management. Integrators should take advantage of new methods to dispose of dead birds. New methods for disposal include composting dead birds in a closed concrete tank with the addition of a bacterial starter, such as Streptobacillus, that facilitates the composting. Other methods may include grinding the dead birds, then, transporting the material to a rendering facility for processing. In addition, dead birds can be frozen, stored, and transported to a rendering facility at a later date. All of these methods could also be used by the processing plant to dispose of dead birds that arrive at the plant. Integrators should also be encouraged to purchase and process feed and feed ingredients that are pathogen controlled. Feeds should be processed with heat, pr adjusting compounds, or other methods that help control microbiological pathogens. Just prior to slaughter (8 to 12 hours), feed should be withdrawn from live birds. This will help control the potential for contamination during evisceration.. The following are new technologies that can be incorporated at the live bird production level. Integrators are also encouraged to utilize probiotics or other available biotechnologically developed products creating an environment that competitively excludes pathogens in the G. I. tract. Extensive biosecurity programs should be implemented on breeder and grow-out farms. Chemical disinfection of fertile hatching eggs have been demonstrated to be effective measures to reduce Salmonellae contamination. These treatments are more effective when applied on the farm but may also be applied at the hatchery. The use of microaerosoled disinfectants in the hatching cabinet are recommended to reduce cross-contamination of Salmonellae during the hatch time. Efforts should be made to reduce stress on cooped chickens and to effectively sanitize transport coops. During the slaughter and processing of poultry, operators should be encouraged to develop enhanced procedures to reduce and control pathogens from feces, feathers, etc. These systems may include improved equipment and procedures for scalding, defeathering, and evisceration that minimize contamination on equipment and product. Equipment should be cleaned and sanitized frequently to prevent any direct or cross-contamination. Methods for trimming and product cutting should be developed that minimize any cross-contamination. Adherence to proper equipment cleaning and sanitation should be strictly followed. NEW TECHNOLOGIES AND IMPROVEMENTS IN COMMERCIAL PRACTICES AND PROCEDURES Decontamination Cost-effective measures for decontamination of broiler carcasses should be encouraged. Success in decontamination procedures depends on strict adherence to RACCP plans and Good Manufacturing Practices. The number of enteric pathogens on the carcasses should be as low as possible before any methods of decontamination are applied. Carcass decontamination. Research results and commercial experience have demonstrated that microbial contaminants on the surface of carcasses can be reduced through the use of chlorine, organic acids, trisodium phosphate, hot water, steam, and various combinations of these and other approved bactericidal materials. There may be more than one combination of treatments at one or more steps during slaughtering, processing, and/or chilling. The NACMCF (4) encourages implementing such bactericidal systems to reduce the number and the incidence of enteric pathogens on carcasses and other poultry products. The conditions (e.g., time, temperature, pr, chemical concentration, pressure of

20 598 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS application etc.) for effective operation of the decontamination system should be specified in the HACCP plan of the slaughter and processing establishment. Trisodium phosphate. Trisodium phosphate is an effective sanitizer and has interim approval for use during poultry slaughter and processing. (2). It has been demonstrated to be an effective means of reducing overall microbial levels and specific human pathogens present on the surface of broiler carcasses when integrated into a poultry slaughter unit operation. Irradiation. Irradiation is an effective technology for destroying enteric pathogens in fresh meats. The irradiation of poultry for pathogen control has been approved in the U.S. (1) and ten other countries (3). Poultry processors may choose to implement this technology on all finished poultry products. Used appropriately, irradiation is an effective method for assuring the safety of poultry. Poultry product identification and coding Procedures should be developed to identify the farm source of poultry carcasses to enhance traceback to the farm. In addition, minimum requirements for the coding of raw poultry products should be developed so that information can be obtained relative to processing establishment(s), sources of raw materials, and time of production. REFERENCES 1. 9 CFR FSIS Fed. Regist. 59(3): ICGF! Ninth Meeting of the International Consultative Group on Food Irradiation. Inventor of product clearances. International Consultative Group on Food Irradiation, Joint FAO/IAEA Division. International Atomic Energy Agency, Vienna. 4. NACMCF Campylobacter jejunilcoli. J. Food Prot. 57: RESEARCH NEEDS 1. Efforts should be continued to develop husbandry practices and other preventive measures which will minimize or eliminate Salmonellae and other human enteric pathogens in broiler breeder and broiler flocks. This includes approaches, such as development of efficacious vaccines, disinfection of fertile hatching eggs, control of crosscontamination within hatching cabinets, design and management of grow-out houses to minimize stress on birds and maximize biosecurity, and use of competitive exclusion microflora to control human pathogen colonization of young chicks. 2. Studies are needed which enumerate levels of Salmonella and other pathogens at various slaughter processing steps to perform a more accurate analysis of hazards, prioritize interventions, and evaluate the effectiveness of various decontamination procedures. Quantitative data will also allow a more accurate assessment of risks associated with the end product than that provided by sampling methods which only determine prevalence. 3. The emergence of antibiotic-resistant Salmonella of epidemiological significance should be weighed in a comprehensive evaluation of the risks involved and benefits derived from the use of subtherapeutic and prophylactic medications in feeds. 4. Elucidate the mechanisms of Salmonella attachment to broiler skin. Develop measures to prevent or inhibit this event through the use of chemical, physical, or biological treatments. Alternatively, generate techniques which induce detachment or by which the accessibility of bacterocides to attached organisms can be enhanced. 5. Technological advances in washing, defeathering and scalding equipment, counterflow chilling, and other processing operations should be continued with foremost consideration of optimizing the microbial safety of the poultry carcass. When technological advances are made, standard operating conditions should be fully delineated. 6. Develop safe, environmentally acceptable methods to disinfect wash/chill water. Determine the public health significance of chlorinated hydrocarbons in processing water. Study processes other than chlorination which will allow chill water to be hygienically recycled. 7. Investigate innovative means to rapidly and economically pasteurize poultry surfaces as a terminal processing step without adulterating or degrading the raw product. 8. Determine if human outbreaks of S. aureus are associated with broiler production/processing or are a postprocessing contamination problem. Isolates of S. aureus associated with live chickens and with the defeatherer and other processing equipment should be genetically compared to strains of S. aureus from human outbreaks. 9. Conduct additional studies to assess the relative importance of cleaning and sanitizing cages used for transport of birds. Development of improved methods for cage decontamination. 10. Studies are needed to investigate the possibility that undercooked chicken is a risk factor in cases of listeriosis. These investigations should include a determination of events that could lead to listeriosis from undercooked chicken and the likelihood of occurrence. 11. One of the long-standing questions with raw foods of animal origin has been the epidemiological significance of low numbers of infectious bacteria, such as Salmonella, Listeria, Campylobacte!; and E. coli OI57:H7. Recent biotechnological advances allow the active tracing of such foodborne pathogens from the farm, through the processing operations, and to ultimate isolation in a clinical setting. An active surveillance study should be undertaken to establish, unequivocally, the role of raw foods of animal origin in transmission of human enteric diseases. This research should be designed and conducted to identify the major points of introduction and/or dissemination of bacterial pathogens. This is needed to perform accurate hazard analyses and risk assessments to develop preventive measures based on sound information. The studies should be conducted to permit acquisition of quantitative information of the levels of pathogens related to overt disease. Although the establishment of an absolute Minimum Infectious Dose for individuals is not a reasonable objective, there is a need to know, on a population basis, the incidence of active infections likely to occur as a function of levels of enteric pathogens ingested.

21 HACCP IN BROILER SLAUGHTER AND PROCESSING Determine how techniques in microbial risk assessment can be applied to the transmission of bacterial pathogens via raw broiler chicken products. This includes quantifying the relative importance of both the different potential sources of pathogenic bacteria and the critical control points that control the microbiological hazards associated with broiler chicken slaughter and processing operations. 13. Establish baseline data for the types and extent (level) of microbial contamination that can be expected on raw broiler chicken products produced under good manufacturing conditions. These data could serve as the basis for assessing the efficacy of alternative intervention approaches. 14. Surveys of the adequacy of refrigeration in distribution channels, retail markets, food service establishments, and the home have indicated that there is a significant potential that raw foods of animal origin will be temperature abused before consumption. There is a need to establish quantitative data on the impact of transitory or marginal temperature abuse on the growth of pathogens on raw broiler chicken products. Data on time/temperature relationships would provide a scientific basis for courses of action that should be followed when there is a loss of temperature control. 15. The continued development of improved methods for identifying foodborne pathogens in products produced from raw foods of animal origin should be encouraged. This includes rapid methods that can be used to identify animals that harbor enteric pathogens prior to slaughter and to periodically verify the effectiveness of HACCP operations. Studies to improve means for sampling to decrease lower limits of detection, enhance accuracy, and decrease the number of samples required for statistical validity should also be encouraged. Appendix A: Good Manufacturing Practices For Fresh Broiler Products National Broiler Council, Good Manufacturing Council, February 1994 INTRODUCTION The recommended Good Manufacturing Practices address every control point in the production and processing of broiler chickens and are designed to enhance both product quality and consumer protection. Unique to products regulated by the U.S. Department of Agriculture, the procedures are drawn from quality control programs throughout the broiler industry, the scientific literature, and existing regulatory documents. This document has two important functions: (i) to serve as a check list for industry to identify necessary controls and make sure they are in place; and (ii) to make public the extent and sophistication of the technical controls used to produce today's broilers. Additional descriptive language may be found in the documents which legally govern the broiler industry: (i) Title 9 of the Code of Federal Regulations, Chapter III, Subchapter C, Part 381, Sections (9CFR38 1). (ii) Meat and Poultry Inspection Manual, Food Safety and Inspection Service, U.S. Department of Agriculture. (iii) Title 21 of the Code of Federal Regulations, Chapter I, Part 110, Sections (2ICFR110). PRODUCTION Management practices and production technologies Each company should have a Breeder/Broiler Production Manual which includes pesticide use and microbiological control recommendations. Copies should be provided to all independent grower contractors and company-owned farm managers. 1. Maintain proper facilities standards. Minimum standards should be established for location and maintenance of roads, maintenance of external grounds, construction of buildings, size of buildings, drainage, ventilation, water supply, equipment construction and maintenance, and physical pest control measures. 2. Provide growers with pesticide use information. Processing/contracting companies should work with growers to insure that the Federal Insecticide, Fungicide and Rodenticide Act, and appropriate FDA, USDA, and EPA regulations are followed. The Production Manual, contracts, and other educational materials should be used to insure that the processing/contracting company controls any use of pesticides and that no use is allowed without the express approval of the processing/contracting company. 3. Grower contracts should include pesticide use statements. Prior to flock delivery, growers should certify that the Federal Insecticide, Fungicide and Rodenticide Act and all pertinent state and federal regulations have been adhered to with respect to any pesticide use. 4. Enforce Biosecurity programs. Biosecurity programs are designed to minimize flock contract or contamination from humans, other flocks, wild birds or other animals, pets, feeds not provided by the contracting company, unsafe water, or contaminated equipment. Visitor control programs must protect against inter- and intrahouse, or inter- and intrafarm contamination and should include the use of plastic or rubber boots and foot baths for disinfecting boots between flocks. Control programs should include procedures for proper disposal of all flock mortalities. Compliance with company standards and any state laws or regulations must be moni-

22 600 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS tored. Programs may include provisions for incineration, rendering, or the use of disposal pits, as appropriate. Animal health care 1. Ensure that pharmaceutical laws and regulations are followed. Only FDA-approved pharmaceuticals are to be used and in an approved manner. 2. Enforce company standards for pharmaceutical use. Growers should be allowed to use only pharmaceuticals furnished by processing/contracting companies. Processing/ contracting companies should keep pharmaceutical records on an individual flock basis. Breeding operations 1. Maintain standards for breeder feeds. Specifications for breeder feeds should include ingredients, preparation methods, nutritional profiles, and controls on pharmaceuticals, microbiological and chemical residues. 2. Monitor and control breeder flock health. Companies should have both a poultry health monitoring program and a program of appropriate vaccination. The vaccination program should be designed and implemented based on flock observation, serological testing, and condemnation standards. 3. Establish procedure to control poultry pathogens. Testing for Salmonella pullorum, Salmonella ga IIina rum, Mycoplasma gallisepticum, Mycoplasma synoviae, and other poultry pathogens should be part of breeder monitoring. 4. Establish procedures to interrupt eggborne poultry disease transmission. Breeder hens should be monitored, and unhealthy birds removed from the breeder flock. 5. Monitor and control egg cleanliness. Egg cleanliness can be controlled through the use of appropriate housing, equipment and nesting materials. Cleanliness can be insured through a program of visual inspection during collection and the maintenance of effective sanitation programs for eggholding rooms on breeder farms. 6. Maintain control of breeder flock egg distribution. All broiler flock eggs that are not to be set should be pasteurized before offered for human or animal consumption or be diverted to nonfood use. Hatcheries Companies should prepare and utilize a hatchery operation manual. 1. Sanitize incubators and hatchers. Clean eggs should be placed in clean setters or incubators. After 18 days, they should be transferred to clean hatchers. As with other equipment, these may be maintained by utilizing an appropriate cycle of clean-wash-sanitize. 2. Maintain proper sanitation of facilities. Sanitation programs should be followed by each company. Programs should include proper sanitation of hatchery, egg-pickup, and chick delivery vehicles. 3. Monitor egg cleanliness. Eggs should be inspected upon arrival at the hatchery for condition and cleanliness and monitored until hatched. 4. Monitor effectiveness of microbiological control programs. Microbiological testing should include the general facility and all surfaces and equipment. The monitoring program should also include air quality testing. 5. Properly handle and dispose of eggs and chicks not selected for broiler production. Every company should have appropriate procedures which are rigidly enforced at all times. 6. Properly dispose of hatchery wastes. Company standards must follow all applicable state laws and regulations and may include provisions for either landfill or rendering of wastes. Grow-out feed preparation 1. Test for and control microbiological quality in feed ingredients. Each company should have specifications for microbiological quality in feed ingredients. Of utmost concern are aflatoxins in grain and Salmonella and other bacteria in rendered protein products. Representative samples should be taken of incoming ingredients and tested to ensure that company specifications are met and established procedures are followed. Ingredients should be purchased only from vendors who are able to meet company specifications. 2. Test for and control pesticide and other chemical residues in ingredients. Each company should have specifications for pesticide and chemical residues in feed ingredients. Suppliers should be informed of company specifications. Representative samples should be taken from incoming ingredients and tested for conformity to specifications. Ingredients should be purchased from vendors only who are able to meet company specifications. 3. Maintain records offeed distribution. Ingredient inventories should be coupled with records on ingredient use and the data and flock destination for feed delivery. 4. Maintain proper on-site pharmaceutical inventories. Daily checks should ensure compliance with FDA regulations and the security of the inventory. Compare daily physical inventory to medicated feeds actually manufactured to ensure proper usage. 5. Ensure that pharmaceutical laws and regulations are followed. Only FDA-approved pharmaceuticals are to be used, and in an approved manner. 6. Continue the prohibition on the use of hormones. Broiler producers have not used hormone growth-enhancing treatments for many years and have no desire to reinstate the practice. 7. Maintain proper sanitation and dust control. Facilities and equipment should be maintained in a sanitary condition and kept in repair and adjustment sufficient to prevent feed from becoming contaminated. 8. Pelleting of grow-out feeds is recommended. Pelleting of broiler feed improves handling and feeding, increases growth rates, decreases ingredient separation, and reduces microbial levels. 9. Test for pathogens in finished feeds. Finished feeds should be monitored to ensure that company specifications and established procedures are followed. 10. Test for pharmaceutical and chemical residues in finished feeds. Finished feeds should be monitored to ensure that company specifications and FDA regulations are met.

23 HACCP IN BROILER SLAUGHTER AND PROCESSING 601 II. Properly clean tanks, bins, and equipment. Feed mill equipment should be cleaned, as appropriate, to maintain standards without subjecting subsequent lots to moisture or chemical contamination. Environmental conditions 1. Maintain proper water quality. Each company should have a control program to ensure an appropriate supply of fresh, clean water. 2. Allow proper separation between poultry houses. Proper distance between houses allows for flock separation and improves air quality. Grow-Out 1. Control wild birds, rodents, and other pests. Keep houses properly screened to eliminate wild birds in poultry houses. Rats and mice can be controlled by using bait stations between flocks. Use only approved pesticides in the proper manner to control rodents and insect pests. 2. Maintain a program for proper litter selection and management. Litter sources should be monitored to ensure that potential problems from chemical residues in litter do not occur. Litter management programs should be designed to provide a healthy growing environment. 3. Maintain a program for used litter management and disposal. Litter should be disposed of properly in accordance with state and local regulations. 4. Establish procedures for timely bird selection. A continuous on-farm inspection should be utilized to ensure that only birds which appear healthy are submitted for processing. 5. Preslaughter chemical residue monitoring programs are recommended. Preslaughter chemical residue testing allows monitoring compliance with FDA-USDA-EPA standards. Companies should have programs to complement feed and litter monitoring programs and appropriate procedures to eliminate from the food supply birds which do not meet those standards. 6. Ensure proper drug-withdrawal procedures. Food delivery schedules and on-farm procedures must ensure that FDA drug-withdrawal regulations are followed prior to the time birds are scheduled to be slaughtered. 7. Ensure proper feed and water-withdrawal procedures. Each company should have a program to ensure that feed and water is withdrawn sufficiently prior to slaughter to minimize potential ingesta contamination during processing. Transport for slaughter. Cage, coop, and truck sanitizing are recommended. An appropriate clean-wash-sanitize cye1e can minimize crosscontamination between flocks and can also minimize contamination brought into the processing plant. SLAUGHTER OPERATIONS As noted earlier, USDA regulations (Title 9 of the Code of Federal Regulations and the Meat and Poultry Inspection Manual) establish minimum standards for broiler slaughter and processing operations. Company standards should be established for location and maintenance of roads, maintenance of external grounds, construction of buildings, drainage, ventilation, water supply, equipment construction and maintenance, and pest control measures. Preoperative sanitation procedures. 1. Microbiological monitoring. Preoperative sanitation conditions should be monitored visually each day, and a routine program of microbiological monitoring of product contact surfaces should be established. Antemortem inspection. 1. Establish access to flock records. When a flock is presented for slaughter, each company should have a system of referring to flock records, including mortality, medication, and feed delivery records. 2. Maintain flock kill records. Companies should keep kill data and location records and should be able to couple them with the existing flock pharmaceutical records. Scalding and picking operations. 1. Utilize counter flow scalder systems. USDA defines counter flow as that in which the water flows counter to the flow of birds at all points, i.e., the make-up water is introduced at the point where the birds exit the scalder, and the water overflow occurs at the point where the birds enter the scalder. 2. Maintain proper scald-tank water replacement. At least one quart of clean, heated water at the proper temperature must be introduced into the scalding tank for each bird processed. 3. Maintain proper scald temperatures. Scald water temperatures should be high enough to aid in the efficient defeathering of the bird, yet not so high as to overscald or produce broilers of unacceptable quality. 4. Ensure proper postscald bird wash. A postscald cabinet washer should be employed at the scalder exit or at some other location immediately after the scalder, but before the picker. 5. Maintain proper sanitation. Appropriate clean water should be used to prevent feather buildup in pickers and to rinse both the machines and the birds. 6. Control picker operation. Proper maintenance and adjustment are essential to the efficient and effective operations of mechanical pickers. 7. Control picking-line washer. Proper adjustment of the picking-line washer effectively rinses bird exteriors. Washer water should be chlorinated to a total level of 20 parts per million. 8. Properly rinse post-hock cutter transfer belt. Systems should be in place to provide effective and continuous rinsing of the transfer belt. Rinse water should be chlorinated to a total level of 20 parts per million. Evisceration, inspection, and dressing. 1. Ensure proper feed and water withdrawal procedure. Each company should have a program to ensure that feed and water is withdrawn sufficiently prior to slaughter to minimize potential ingesta contamination during processing. 2. Control eviscerating line equipment. Proper maintenance and adjustment of mechanical eviscerators and equipment are necessary to maintain product quality and processing line efficiency. 3. Rinse and sanitize eviscerating line equipment continuously, subject to USDA regulations. 4. Enforce standards for employee hygiene. Personnel with clean hands, clothing, and good hygiene practices are essential to the production of wholesome products. Employee standards should include outer garments, head coverings, safety and cleanliness

24 602 NATIONAL ADVISORY COMMITTEE ON MICROBIOLOGICAL CRITERIA FOR FOODS devices, such as gloves, aprons, or protective shields and should restrict jewelry and ornamentation and food or tobacco use in plants. 5. Ensure proper final bird wash. The final step in slaughter processes should be a whole-carcass rinse using water chlorinated to a total level of 20 parts per million. Chilling operations. 1. Maintain proper chiller water replacement. At least one-half gallon of clean, chilled water must be introduced into the chiller tank for each carcass, or alternative USDA-approved procedures must be followed. 2. Maintain proper water quality. Clean, potable water, chlorinated to achieve a total level of 20 to 50 parts per million in the intake water, should be utilized to facilitate the reduction of total microbiological loads and prevent product quality deterioration. The amount of chlorine added to the intake water should be sufficient to achieve one to five parts per million available chlorine at the chiller overflow. 3. Maintain proper chiller temperature. Chiller water temperatures must be regulated to ensure that end-product temperatures of 40 F or less are reached in the time required by USDA regulations. Microbiological and chemical monitoring. After slaughter processing, a statistically valid program of random monitoring of chemical residues should be employed to assure compliance with tolerances. Likewise, processors should employ a statistically valid program of sampling fresh processed poultry for determining microbiological quality to monitor quality assurance programs. POST CHILLER CUT-UP AND PACKAGING Maintain proper facility sanitation Buildings, fixtures, and equipment should be maintained in a sanitary manner sufficient to prevent product from becoming contaminated or adulterated. All equipment must be cleaned, washed, and sanitized at least once each day and must be examined to ensure that proper sanitation standards are met prior to beginning operation each day. Where the temperature of processing areas is not kept below 50 F, all equipment which comes in contact with product must be rinsed at least every 5 hours. Establish standards for employee hygiene Personnel with clean hands, clothing, and good hygienic practices are essential to the production of wholesome products. Employee standards should include outer garments, head coverings, and safety and cleanliness devices, such as gloves, aprons, or protective shields, and should restrict jewelry and ornamentation and food or tobacco use in plants. Maintain proper product temperature Product should be maintained at a temperature below 55 F. Product that will stay in a vat or cut-up bin more than 30 minutes should be iced to maintain proper temperature. Maintain rapid product movement Product should move through the entire cut-up process rapidly enough to ensure that the temperature does not rise above 55 F. DISTRIBUTION Lot identification Each company should establish appropriate lot identification procedures, such as lot codes. A lot is the food produced during a period of time, up to one day, indicated by a specific lot code. Sanitation Storage and transportation of broiler products should be under conditions that will protect food against physical, chemical, and microbial contamination and against deterioration of the food and the container. Product quality Companies should work in cooperation with distributors to develop programs ensuring proper product handling. In addition to education, companies must develop systems to provide distributors with information on the proper distribution temperature necessary to maintain the quality and safety of each type of product. Appendix B: General Guidelines for Handling Raw Broilers and Broiler Parts in Retail Food Stores and Food Service Establishments Food receiving and storage Fresh, raw broilers and broiler parts should be received in good condition and at a temperature of 41 F (2) or less. A visual inspection should be conducted to assure the condition of the products. Temperatures can be checked using accurate thermometers. Refrigerated storage Storage temperatures of less than 41 F will minimize microbial growth of Salmonella, Campylobacter, and other pathogens. Proper stock rotation should be practiced: A first-in, first-out stock rotation system should be utilized; All raw broilers and broiler parts should be kept covered,

25 HACCP IN BROILER SLAUGHTER AND PROCESSING 603 wrapped, dated, labelled and rotated; Raw broiler and broiler parts should be stored separately from processed, raw, or cooked foods to prevent cross-contamination; The cooler should be regularly inspected for good sanitary conditions and maintained at the proper temperature «41 F). Foods should be stored to assure sufficient air circulation. Food preparation Food service workers should be aware of and practice good personal hygiene at all times, especially when preparing and handling foods. "Food workers who are ill with a disease that can be spread by foods shall not work. All food workers shall wash their hands as often as necessary to prevent contamination of ready-to-eat foods. Food workers shall wash their hands in an approved handwashing facility by applying soap, using warm water, scrubbing thoroughly, rinsing, and, then, drying using approved sanitary towels or air dryers. Food workers shall wash their hands before starting work and after using the toilet or contaminating their hands by handling raw meats, poultry or fish, coughing or sneezing or handling unclean objects." (2). Clean clothing and appropriate hair covering should be worn by all personnel involved in food preparation. Raw broilers and broiler parts should be kept separate from processed, raw, or cooked foods. Equipment and utensils (such as knives, cutting boards, and pans), used in the preparation of raw chicken products should be properly cleaned and thoroughly sanitized before use with other foods. Whole broilers should be cooked to a minimum internal temperature of 165 F (74 C) (2). The temperature should be measured in the thickest part of the breast muscle with an accurate thermometer or thermocouple. Ground or restructured broiler products should be cooked to a minimum internal temperature of 16SOF for 15 seconds. Broiler products that are cooked and held for hot display should be kept at a minimum internal temperature of at least 140 F. Leftover broilers and broiler parts should be refrigerated immediately in shallow containers «2 inches in height) so quick cooling can be achieved and microbial growth can be prevented. Large broiler pieces should be cut into four-pound or smaller pieces to speed cooling. Reheat leftover broilers and broiler parts and other precooked broiler products to a minimum internal temperature of 165 F within two hours. 1. USPHAlFDA Food Code REFERENCES Appendix C: General Guidelines for the Handling of Raw Broilers and Broiler Parts by Consumers Food purchasing Buy perishable broilers and broiler parts last, after all other grocery items have been selected. Insist that grocery baggers place all raw food of animal origin (poultry, red meat, seafood, eggs, etc.) in a separate plastic bag for transport. Never allow raw meat to contact a package offood that will not be cooked before consumption. Cold foods should be placed together in a paper bag to help prevent excessive warming during transport. Take purchases home immediately, and place items to be kept refrigerated or frozen in proper storage as soon as possible. Kitchen appliances and utensils Use a thermometer to assure that the refrigerator temperature is 40 F or below and that freezer temperature is below OaF. Keep refrigerator and freezer shelves clean and sanitize periodically. Separate raw broilers and broiler parts from cooked foods in the refrigerator. Raw foods should never be stacked on top of cooked foods. Use an oven thermometer to verify that the oven temperature is approximately the same as the temperature dial selector. Most oven owner's manuals will have instructions for adjusting the temperature selector for accuracy. Countertops, sinks, and cutting surfaces should' be cleaned and sanitized after contacting any raw food. Clean surfaces with hot soapy water, and rinse thoroughly. Sanitize the surface with a chlorine solution (one cap of bleach in one gallon of cold water or other commercially available kitchen sanitizers; a new solution should be prepared as needed). If washing utensils by hand, knives and cutting boards used with raw meats should be washed with hot, soapy water, followed by a hot water rinse and sanitation with a chlorine solution after each use. Washing in a dishwasher having a hot water rinse will sufficiently sanitize utensils (the temperature of the water should be at least 120 F). Food preparation Cross-contamination occurs when utensils, plates, or hands used in preparing raw foods are not thoroughly washed and sanitized before handling or preparing cooked foods or foods that will not be cooked (e.g., salads). Never use the same plate to transport raw and cooked poultry