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4 Scientific Criteria and Performance Standards to Control Hazards in Meat and Poultry Products DESCRIPTION OF THE MEAT AND POULTRY INDUSTRY Animal production in the United States has undergone a transformation over the last 50 years from a system mainly comprised of independent animal producers to one mainly comprised of concentrated animal feeding operations. The major production animal species, beef cattle, swine, chickens, and turkeys, are produced under a variety of conditions that may have significance in regard to the presence or absence of potential foodborne pathogens. The following is a brief synopsis of animal production in the United States. Beef A major percentage of the world's beef is produced in the United States both for domestic use and for export. The U.S. fed-cattle industry is the largest in the world (ERS,2000~. Most beef produced in and exported from the United States is the grain-finished, high-quality, choice-cut variety, while imported beef is gener- ally grass-fed and is used primarily for processing as ground beef (ERS, 2002~. Red meat production is a concentrated industry. Feedlots and steer and heifer slaughter facilities are geographically concentrated in the Great Plains (MacDonald et al., 2000~. Iowa, Kansas, Nebraska, and Texas accounted for over 51 percent of the U.S. commercial red meat production in 2001 (NASS, 2002~. Since cows generally move directly to plants from dairy farms and beef cow-calf operations, cow and bull sales and slaughter plants are more widely distributed across the country (MacDonald et al., 2000~. In commercial plants, red meat 133

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34 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD production totaled 45.7 billion pounds in 2001, of which beef production accounted for 26.2 billion pounds (NASS, 2002~. Four companies slaughter and process 82 percent of the beef in the United States (MacDonald et al., 2000; REAP, 2001~. Twenty percent of beef consumed originates from cull cows of the dairy industry (University of Vermont, 2003; Wallace, 2003~. Over 25 years ago, most beef was sold as whole or half carcasses that were fabricated by other processors or retailers. The advent of boxed meat (i.e., assem- bly cut and packaged meat) revolutionized the beef industry so that most fresh beef is sold as vacuum-packaged primals (large sections of a carcass cut for wholesale, such as the round, chuck, or rib) and subprimals (retail cuts) (Kinsman, 1994~. Case-ready beef (retail cuts packaged and brand labeled) is a new concept currently being embraced by some companies (Eilert and Rathje,2001~. Processed beef products (i.e., those in which the carcass identity is lost or that are subject to some treatment that affects its texture, color, and flavor) accounted for 13.9 per- cent of beef consumed in 2001 (Nalivka, 2002~. Poultry The U.S. poultry industry is comprised primarily of three segments: broilers, turkeys, and eggs. Of these three, broilers (i.e., young chickens) dominate with 66 percent of the dollar value of production (Nalivka, 2002~. The United States produced more than 8.2 billion chickens, 2.6 billion turkeys, and more than 71 billion table eggs in 2000. The U.S. broiler and turkey industries are referred to as "vertically inte- grated." The company or integrator controls all aspects of the process but con- tracts with individual landowners for growing services. The landowners furnish the poultry houses, energy, and labor, while the companies furnish the animals, feed, and technical support. The basic unit of this arrangement is the "complex," which consists of parent flocks, multiplier flocks, hatchery, feed mill, and processing plant (Figure 4.1~. Breeder farms, also called multiplier flocks, supply all of the eggs that will become the chickens for processing. For each day of processing, the hatchery must hatch enough chicks to account for losses in the field and for a standard amount of weight gain to match sales projections for the time period when these birds will be processed. The feed mill must supply feed for all of the houses within the complex to ensure that no chicken goes hungry. The complex also usually has water treatment facilities and also may have rendering capabilities for by-products. The typical complex processes over 1 mil- lion chickens per week. A typical young broiler plant can have from one to four processing lines. The maximum speed of each line is determined by the amount of inspection in place from the U.S. Department of Agriculture's (USDA) Food Safety and Inspection Service (FSIS). The categories of inspection are:

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36 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD The Streamlined Inspection System, which allows 70 birds/min with two inspectors per evisceration line (35 birds/min/inspector) The New Enhanced Line Speed, which allows 91 birds/min with three inspectors and additional plant inspection (30.3 birds/min/inspector) The New Evisceration Systems: Maestro (Meyn Poultry, Gainesville, GA) and Nu-Tech (Stork Gamco, Gainesville, GA), which allow 140 birds/ min with four inspectors per line (35 birds/min/inspector). Pork The United States is a major pork producer, second only to China. The U.S. pork industry rapidly expanded during the 1990s; more pork was produced (nearly 19 billion pounds) and more hogs slaughtered (more than 99 million head) in the United States in 1998 than ever before. Previous records in production had been set in 1992, 1994, and 1995. Approximately 85,000 pork producers are in business today compared with nearly 3 million in 1950. Farms have grown in size; over 80 percent of the hogs are grown on farms producing 1,000 or more hogs per year, while over half are grown on farms producing 2,000 or more hogs per year. These operations, which are often very technically sophisticated, are still predominantly individual family farms. The geographic location of pork production is shifting as well. While the traditional Corn Belt represents the overwhelming share of production, growth is also occurring in nontraditional hog states such as Texas, Colorado, and Okla- homa. North Carolina, which ranked fourteenth in pork production 30 years ago, now ranks second. MEAT AND POULTRY INSPECTION The Federal Inspection System Under the Federal Meat Inspection Act and the Poultry Products Inspection Act, USDA, through FSIS, inspects all domestic meat and poultry to be sold in interstate commerce in the United States (FSIS, 2001c). Approximately 6,000 meat and poultry processing plants and 130 import establishments are inspected by FSIS (FSIS, 2002c). Products inspected under FSIS authority include all products from cattle, sheep, swine, goats, horses and other equines, chickens, turkeys, ducks, geese, and guinea fowl (FSIS, 1998a). It also applies to ostriches and emus (FSIS, 2001b). Processed products containing 3 percent or more raw meat and poultry or 2 percent or more cooked meat and poultry are also included (FSIS, 2001c), with some exceptions. Products that do not cross state lines may be inspected by state rather than federal inspection agencies; there are approxi- mately 1,500 meat and poultry establishments that are inspected by state pro-

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS 137 grams (GAO, 2001~. Twenty-seven states have established inspection systems equivalent to the federal system; however, products that are state-inspected can only enter intrastate commerce. To ensure the safety of imported meat and poultry products, FSIS maintains a wide-ranging system of inspection and controls. On an annual basis, FSIS evaluates the inspection systems in all foreign countries eligible to export meat and poultry to the United States to ensure that their inspection systems are equiva- lent to the U.S. system (FSIS, 2001c). This evaluation consists of a document review of the country's laws, regulations, and other written information, and an on-site review of plant facilities and equipment, laboratories, and training pro- grams. In addition, all imported meat and poultry products may be reinspected (including testing) upon entering the United States (FSIS, 2003~. The 1997 implementation of the Pathogen Reduction; Hazard Analysis and Critical Control Point Final Rule (PR/HACCP rule) initiated a significant change in the regulatory philosophy and roles of both inspectors and industry. In the past, some plants relied heavily on USDA inspectors to identify plant and process deficiencies before the company would take action to correct them. The PR/ HACCP rule defined the respective roles, tasks, and responsibilities of both industry and FSIS (FSIS, 1996~. Businesses that produce the meat and poultry products are now directly accountable for their safety (FSIS, 1998b). The introduction and implementation of the PR/HACCP rule attempted a significant change in regulatory philosophy and respective roles and responsibili- ties of industry and inspectors over a relatively short time period. The transition has not been entirely smooth; there have been some inconsistencies and setbacks in the start-up process. In response to reports published by the General Account- ing Office, USDA's Office of the Inspector General, and its own self-assessment, FSIS is taking steps to provide supplemental guidance and clarification to assist inspection staff and industry in adapting to these changes (GAO, 2002~. U.S. Department of Agriculture Inspection Models Project Pilot Program USDA began the HACCP-based Inspection Models Project (HIMP) pilot program in 1997 (FSIS, 1997, 2001a). This program was designed to explore extending HACCP and process controls to the slaughter of young animals to further improve food safety and reduce or eliminate product quality defects. A key component of HIMP includes setting performance standards by FSIS and requiring the meat and poultry processors to use process control techniques to meet the performance standards. However, the collection of the data needed to assess the effectiveness of the program has not been completed, so an evaluation of HIMP at this point would be premature. The committee supports the conclusion of previous National Academies reports (NRC, 1985b, NRC, 1987) that carcass-by-carcass inspection is ineffective from a food safety perspective. If successful, HIMP may provide a useful model

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38 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD to reduce FSIS dependence on carcass-by-carcass inspection and increase the use of process control techniques to assure the safety of meat and poultry products. State Inspection Programs with Federal Oversight Twenty-seven states operate state meat and poultry inspection programs. These state programs, with federal oversight, were established with the passage of the Wholesome Meat Act of 1967 and the Wholesome Poultry Act of 1968. State meat and poultry inspection programs were required to implement the inspection system mandated by USDA in the PR/HACCP rule beginning in 1997. The transition from traditional meat and poultry inspection to the HACCP system represents a major philosophical, cultural, and procedural change for the state inspection programs. USDA provides matching funds to cover 50 percent of state program costs through the administration of renewable federal grants (WI DATCP, 2002~. State meat and poultry inspection programs are required to meet standards at least equal to the federal program, and FSIS is responsible for determining that they do so. In addition to conducting their own internal audits, state meat and poultry inspection programs are audited by USDA on a one-, two-, or four-year basis, with the frequency based on prior performance. Each state submits a state performance plan as part of an annual report for review by USDA. These plans must describe the operating practices and procedures for administering the state meat and poultry inspection programs, including laws and regulations, funding and financial accountability, resource management, staffing and training, pro- gram operations, facilities and equipment, labels and standards, in-plant review and enforcement, and laboratories (WI DATCP, 2002~. Meat and poultry plants are divided into three size categories. Large plants have 500 or more employees, small plants have 10 to 499 employees; and very small plants have fewer than 10 employees or annual sales of less than $2.5 mil- lion (FSIS, 19961. While plants under federal inspection comprise all three size categories, plants under state meat and poultry inspection programs are currently small and very small plants only (FAIM, 2002~. Consequently, the state inspec- tion programs have developed specialized expertise in working with small and very small plants. In a historical context, it was believed that state inspection programs offered economic benefits such as lower ongoing costs of state inspec- tion compared with federal inspection, greater flexibility in the scheduled time of inspection, and the ability to accommodate low-volume slaughter or processing from local livestock markets (WI DATCP, 2002~. In addition, state programs inspect and monitor custom plants, which are those that slaughter and process meat and poultry products for personal use by the animals' owners (i.e., not for subsequent sale).

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS State and Local Government Inspection of Retail Meat Processors 139 Retailers who process meat and poultry only for direct sales to consumers are subject to different inspection processes and regulations than those whose prod- ucts are sold wholesale. The Food and Drug Administration Model Food Code (FDA, 2001), implemented in 1993 and updated biennially, is a template for the regulation of retail and food service operations. As of April 2002, 49 states had either adopted or were in the process of adopting one of the biennial versions of FDA's Model Food Code. New Mexico is not pursuing adoption of the Food Code, but the state still utilizes it for guidance and interpretation (CFSAN, 2003; FDA, 2001~. The committee recommends that collaboration among USDA, FDA, and state and local governments continue, to help ensure the production of safe meat and poultry products and consumer protection in the United States. Laboratory Analysis Microbiological testing of product samples obtained by the federal and state inspection programs is conducted at USDA-approved laboratories. These are actually lagging indicators in measuring the process performance of meat or poultry plants because samples are taken after the product is prepared and pack- aged, and even with rapid methods, there is a significant lag time between the collection of the sample and the analysis of the laboratory data. By the time these data become available, the corresponding meat and poultry products often have been in the market for varying periods of time and may already have been con- sumed. Therefore, although microbiological samples provide both the plant and regulatory agency with a "score card" for plant performance, if further significant gains in the safety of the U.S. meat and poultry supply are to be realized, meat and poultry establishments need to implement more effective process control measures. As mentioned in Chapter 3, these process control measures should be linked to a systematic continuous improvement process to achieve the level of safety demanded by the U.S. consumer. The Significance of Proper Implementation and Enforcement of the HACCP System It is important to stress that any HACCP system, including one with scien- tifically valid microbiological performance standards, must be properly imple- mented to achieve its intended effect. The Government Accounting Office (GAO) audited HACCP implementation by FSIS (GAO, 2002) and concluded that there were deficiencies in the implementation process. The GAO report identified three major areas of concern. The first relates to establishment of scientifically valid HACCP plans that properly identify hazards

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140 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD and appropriate Critical Control Points (CCPs). Some establishments have failed the hazard analysis or have omitted some legitimate hazards in it and have conse- quently not provided for adequate control or interventions of these hazards (e.g., chemical residues or Salmonella'). Validation of a HACCP plan is the responsi- bility of industry personnel. FSIS inspectors are charged with verification of the Sanitation Standard Operating Procedures and HACCP plans, which may include reviewing the plan and the records and corrective actions taken a task that requires training FSIS personnel. To this effect, a recent addition to the FSIS field staff, Consumer Safety Officers, will receive more training on HACCP than the traditional inspection personnel and will be tasked with critical evaluation of HACCP plans as part of HACCP phase-2 implementation, the "Next Steps." This program is being built slowly due to budget constraints. A second area of concern mentioned in the GAO report, which if not cor- rected would make it difficult to implement scientifically valid performance standards, is the issue of corrective action if a plant experiences deviations from its HACCP plan and is deemed to be in noncompliance. Audits of these plants suggest that a majority have repetitive incidences of noncompliance without subsequent corrective action. The third concern identified in the GAO report is that if plants fail the Salmonella performance standard, regulatory action is not necessarily taken. Regulatory action letters may be delayed up to nine months. The report also indicates that, even when conditions occur that could lead to an order for suspension of inspection, orders are often put into abeyance by USDA. As shown by GAO's analysis, complex factors appear to have hampered FSIS' s ability to effectively enforce HACCP implementation in its initial phases. It is not within the charge of this committee to audit the administrative procedures involved in implementation of performance standards, but rather to comment on the scientific criteria involved in establishing them. However, the committee believes that scientific criteria, including performance standards, may be part of a HACCP program and can only be successful in reducing contamination if they are uniformly implemented, and if this implementation is enforced in a timely fashion by the responsible regulatory agency. Promulgation of new standards and establishment of rigid scientific criteria for safe food are useless if monitoring and enforcement are not ensured. To that effect, the responsibility of meat and poultry inspectors should be redefined to reflect their role within a HACCP food safety assurance system. Consistency of the Inspection Process There has been a consolidation of the meat and poultry industries in recent years. Many of the larger meat and poultry companies manage multiple process- ing plants across the United States that are regulated by both FDA and FSIS. This presents challenges to the plants and corporate management due to the inconsis- tent interpretation and enforcement of regulations, which in turn hinders imple-

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS 141 mentation of consistent product safety strategies. Anecdotal stories abound in the industry about inconsistencies in the enforcement of rules and regulations be- tween plants and between districts. The committee recommends that FSIS continue its training program and the development of means to measure and evaluate the performance of its inspection team (i.e., Inspectors-in-Charge, Supervisory Veterinary Medical Officers, and inspectors), and state meat and poultry inspection teams, to ensure that regula- tions are consistently enforced across the country. Concurrently, the committee recommends that FDA also continue to develop training programs and various means to measure and evaluate the performance of FDA inspectors and state regulatory agencies that conduct FDA inspections. REVIEW OF CURRENT STANDARDS FOR MEAT AND POULTRY Current Criteria and Performance Standards USDA specifically charged this committee to develop definitions for terms such as "performance criteria" and "performance standard." The definitions of these and other relevant terms are presented in tabular form in Appendix A. The definitions adopted by the committee that are of particular relevance to the remaining sections of this chapter are those of performance standard and micro- biological criterion. Within the last decade, FSIS has established several criteria, including per- formance standards, as part of the current regulatory and inspection system for meat and poultry. These include criteria for process control and standards for pathogen reduction in raw products, adulteration, standards for cooked products, and general sanitation standards. Among these, criteria for process control and standards for pathogen reduction in raw products involve microbiological sam- pling and testing programs. The results of these testing programs are used by the agency to determine whether processors receive a "fail" or "pass." In contrast to these microbiological standards and criteria, which apply to a broad range of products, "adulteration" is very narrowly interpreted for a specific bacterium and product, Escherichia cold 0157:H7 in raw ground beef. Standards for cooked products differ from the standards for raw meat and poultry in that they require the reduction of a stated number of a specific pathogen, as well as validation of the process used to achieve that reduction, instead of a testing and sampling program. Sanitation standards (as they are specifically referred to in the Code of Federal Regulations) are less prescriptive and contain vague descriptors such as "adequate" and "sufficient." Consequently, these standards are subject to more interpretation than either the cooking process or microbiological criteria or stan- dards. Several types of standards or criteria are summarized and discussed in the following sections.

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142 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD Contamination with Microorganisms; Process Control Verification Criteria and Testing; Pathogen Reduction Standards for Red Meats (9 Vol 2 C.F.R. 310.25) These criteria are part of the PRIHACCP rule and include both process control criteria for E. cold Biotype I (generic E. coli) and performance standards for a specific pathogen (salmonellae). The process control criteria are based on the quantitative level of generic E. cold on or in fresh meats. The sampling technique includes a swab or excision method for intact carcasses and a destruc- tive analysis for ground products. The sampling frequency varies both by species and by the relative size of the processing establishment (Table 4.1~. The sampling and testing protocol for the process control criteria are based on a three-class sampling program. In a three-class plan, m is the analytical value that differentiates good quality from marginally acceptable quality, M is defined as the analytical value that differentiates marginally acceptable quality from unacceptable quality, n is the number of samples taken, and c is the maximum number of samples out of n that may exceed the value set for m. For a sample set to pass, no sample may exceed the M value and no more than c samples may exceed the m value. The values for the various species are given in Table 4.2. TABLE 4.1 Sampling Frequency for Process Control Indicator (Generic Escherichia coli) for Fresh Meat Species or Size of Establishment Samples per Number of Carcasses Cattle, sheep, or horses Swine Very low-volume establishments 1 per 300 1 per 1,000 At least 1 per week, beginning June 1 of each year, until 13 in-compliance samples are collected in a row SOURCE: 9 C.F.R. 310.25. TABLE 4.2 Values for m, M, n, and c for the Process Control Indicator (Generic Escherichia coli) for Fresh Meata Species m M n c Cattle Negativeb 100 13 3 Swine 10 10,000 13 3 a m = the analytical value that differentiates good quality from marginally acceptable quality, M= the analytical value that differentiates marginally acceptable quality from unacceptable quality, n = the number of samples taken, c = is the maximum number of samples out of n that may exceed the value set for m. b Negative is defined by the sensitivity of the method used in the baseline study, with a limit of sensitivity of at least 5 cfu/cm2 carcass surface area. SOURCE: 9 C.F.R. 310.25.

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS TABLE 4.3 Values for n and c for the Pathogen Reduction Standard (Salmonella Performance Standard) for Fresh Meat 143 Performance Standard Product (% positive for salmonellae) Maximum Number of Number of Positives to Achieve Samples Tested (n) Standard (c) Steers/heifers 1.0 82 1 Cows/bulls 2.7 58 2 Ground beef 7.5 53 5 Hogs 8.7 55 6 Fresh pork sausage NAa NA NA a NA = not applicable. SOURCE: 9 C.F.R. 310.25. The sampling frequency for the pathogen reduction standard for Salmonella is identical to that for the process control indicator (Table 4.1~. The sampling technique includes a swab or excision method for intact carcasses and a destruc- tive analysis for ground products. In practice, FSIS will take an initial sample set (the A set). If an establishment fails the A set, FSIS will take up to two more sample sets (the B and C sets). Failure of all three sample sets would be grounds for USDA to withdraw inspection from an establishment. The pathogen reduction standard is based on a two-class sampling plan, in which n is the number of samples taken and c is the number of samples allowed to fail the specification. The standard is based on a qualitative assay for the presence or absence of Salmonella. The values for the various species and prod- ucts are given in Table 4.3. Contamination with Microorganisms; Process Control Verification Criteria and Testing; Pathogen Reduction Standards in Raw Poultry (9 Vol 2 C.F.R. 381.94) The process control criteria and the pathogen reduction standard for raw poultry are structured in an identical manner to those for red meats. The process control criteria are based on the numerical populations of E. cold Biotype I (generic E. coli) on or in fresh poultry meats. The sampling technique includes a whole- bird rinse for intact carcasses and a destructive analysis for ground product. The sampling frequency varies both by species and by the relative size of the process- ing establishment (Table 4.4~. The sampling and testing protocols are based on a three-class sampling program, as previously described. The values for the various species are given in Table 4.5. For the pathogen reduction standard for Salmonella, the sampling frequency is identical to that for the process control indicator (Table 4.4~. The sampling

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68 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD assessment may have overestimated the costs. The authors also attempted to test which of the two FSIS cost scenarios is more appropriate. They suggested that if the selection of an intervention strategy is made on a least-cost basis, then actual process modification costs may be higher than suggested in the regulatory impact assessment for large pork-slaughter plants. Jensen and Unnevehr (2000) present a clear framework for incorporating pathogen reduction data into their assessment of least-cost interventions. How- ever, care must be taken in applying these microbiological results. As the authors admit, their data come from two separate (although small) sources. One study tested interventions in a plant environment; the other did not. One used inoculated samples; the other did not. The inoculation procedure effectively elevates patho- gen populations to an observable level, thus implying that although real-world reductions (the results of interventions) will not be of the same magnitude, they will be of the same relative order. This remains an untested hypothesis for most interventions. Without further analysis, it cannot be presumed that a certain logic reduction due to an intervention will be an improvement over current strategies; that it will be achieved in all plants at all times, regardless of the "cleanliness" of animals being presented for slaughter; or that it will lead to a risk reduction downstream at the point of consumption. Therefore, it may be more appropriate to presume that this analysis overestimated the benefits to the consumer. Broader Economic Impacts: What Needs to Be Assessed? Several potential indirect impacts should be considered in the broader eco- nomic analysis of the PR/HACCP rule. First are scale effects or implementation costs, which differ significantly by plant size. As HACCP-based regulations expand in their coverage (e.g., to the retail sector with many small and very small firms), it is argued that scale effects will be of paramount importance. The food safety system put in place by a plant can also impact nonsafety quality attributes, thus increasing overall efficiency (Unnevehr and Roberts, 1997~. That HACCP can help limit product rejection or rework, thus reducing the variability inherent to all production processes, also deserves more attention. This benefit allows for increased customer and consumer satisfaction (e.g., reduced complaints and product return); and may increase, although it is often difficult to quantify, measures of consumer confidence. Also, international trade is clearly facilitated when harmonized HACCP-based regulations are adopted (Caswell and Hooker, 1996~. Potential legal liability and insurance cost savings can arise from the use of innovative food safety controls. An advantage can be achieved by those plants and firms that are first to adopt a proven intervention. This can improve the overall company image, potentially providing a competitive and marketing advantage. Such innovation offset dynamics are discussed by Cockbill (1991)

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS 169 and Hobbs and Kerr (1992) and may or may not be candidates for inclusion in future regulatory impact assessments, depending upon the details of the HACCP- based regulation under consideration. Difficulties in Forecasting Costs and Benefits for Novel Innovations The PR/HACCP rule has an admirable degree of flexibility (i.e., minimal process criteria). Further, the performance standard elements of the rule seem to have provided some incentive to promote innovation in the pathogen reduction strategies employed. However, in part due to such success in regulatory design, ex post costs may differ significantly from ex ante estimates as more plants adopt validated pathogen reduction strategies that differ from those that USDA pre- sumed would be used. This is further confounded when the selection of such strategies is not made on a least-cost basis. Limited economic research exists to provide reliable estimates of costs and resultant benefits of many food safety interventions. Several pathogen reduction strategies, particularly multiple-hurdle techniques, incorporate novel approaches for which only limited commercial applications exist, thus requiring a cautious approach to forecasting potential costs. Further, plant-level pathogen reduction benefits of multiple-hurdle interventions are not always simply additive. The potential use of novel individual interventions, as well as innovative combinations of traditional interventions, clearly make the prerule estimation of costs and benefits extremely difficult. It seems likely that in future regulatory impact assessments, the role of pilot programs to forecast real-world impacts will be expanded. Hopefully, these studies will utilize representative firms' experiences with HACCP (or whatever food safety controls are being considered) and consider all state-of-the-art interventions. Special care must be taken in estimating the impact of any novel intervention not widely adopted in the industry based on plant-level experiences and not just on laboratory or theoretical assessments. At all times, the effectiveness of novel interventions should be compared with current systems on a microbiological as well as a cost basis. THE NEED FOR ADDITIONAL APPROACHES TO REDUCE MICROBIAL HAZARDS Preventing Pathogen Contamination and Amplification Before Slaughter Pathogens, including E. cold 0157:H7, Salmonella, and Campylobacter, on hides and in internal organs of live animals arriving for slaughter are important sources of contamination of meat. Substantial surveys of pathogen prevalence in dairy herds, feedlot populations, and culled dairy cattle have been conducted. Surveys of dairy farms show that a small percentage of farms or animal feces are

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170 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD positive for E. cold 0157:H7 at a single point in time but, with repeated sampling, the organism is likely to be detected on most farms (Hancock et al., 1998~. In a survey of 36 dairy herds, with repeated sampling over six months, the pathogen was ultimately detected on 75 percent of the herds, probably because carriage lasts no more than a few weeks in any animal (Hancock et al., 1997a, 1997b). The prevalence of fecal shedding of E. cold 0157:H7 was 0.9 percent among dairy cows and 2.9 percent among dairy cows about to be culled; these data suggest that culling either selects for animals likely to be contaminated or contributes to their contamination. On average, 24.2 percent of dairy operations had at least one positive animal; this prevalence was seasonal, increasing in the summer months. Surveys of beef cattle in feedlots show a similar pattern, though the prevalence of contamination is generally higher (Veterinary Services, 2001a). Lately, methods based on immunomagnetic separation have allowed better detection of animals shedding low levels of E. cold 0157:H7 (Besser et al., 2001~. Due to the higher sensitivity methods, it is currently believed that the prevalence of E. cold 0157:H7 is higher than previously thought. Given that about 23 percent of the nation's dairy herd is culled and sent for slaughter annually (APHIS, 1996) and that much of it becomes ground beef (Troutt et al., 2001), the committee concludes that prevalence data on E. cold 0157:H7 in culled animals is needed. Better understanding of the circumstances associated with the presence of pathogens could lead to targeted efforts to miti- gate or prevent their circulation among live animals. E. cold 0157:H7 is a hardy pathogen, able to survive in damp cattle manure for up to 70 days, to survive and multiply in the sediment of cattle water troughs for months, to rapidly grow in moist cattle ration, and to be carried by wild deer (Keene et al., 1997; LeJeune et al., 2001; Lynn et al., 1998; Wang et al., 1996~. Epidemiological studies that link the presence or absence of the organism in a herd to various management practices have suggested stronger association with using corn-based feed or feeding barley than with feeding soy meal or spreading fresh manure on forage crops (Dargatz et al.,1997; Hancock et al., 1997b; Herriott et al., 1998~. The rumen of a fasted animal may be more hospitable to growth of Salmonella and E. cold 0157, and it has been suggested that the common practice of fasting animals preslaughter may increase the shedding and spread of E. cold 0157:H7 (Hancock et al., 1998; Rasmussen et al., 1993~. Salmonella are also commonly present among dairy herds and feedlots. The 1996 NAHMS survey of dairy cattle reported a prevalence of 5.4 percent among animals and 27 percent among dairy operations sampled a single time (Wells et al., 1998~. As with E. cold 0157:H7, the data also suggest that the level is higher in culled animals. Among feedlot cattle, the prevalence of Salmonella was 6.3 percent in animals, 22.3 percent in pens, and 51 percent in feedlots (Veterinary Services, 2001b). Factors associated with the presence of Salmonella on farms have not been examined as thoroughly as for E. cold 0157:H7. Nevertheless, some general principles of control of Salmonella among cattle herds have been

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS 171 defined and are also applicable to the control of Salmonella Typhimurium DT104 (Dargatz et al., 1998) and other important animal-borne illnesses such as Johne's Disease (Groenendaal and Galligan, 1999; Wells et al., 1999~. In addition to the prevalence on the farm, other factors that may increase the risk of pathogens in meat relate to the transportation of herds in trucks from a pasture or barn through auction yards, feedlots, and holding pens, where they are exposed to fecal or other means of contamination from animals previously or currently there. The 1996 NAHMS survey of dairy cattle reported that 15 percent of feces from individual culled dairy cattle were positive for Salmonella at market and that 67 percent of markets had at least one animal shedding Salmonella (Wells et al., 1998~. Furthermore, a recent systematic national survey of 5,000 culled dairy cattle reported that 23 percent of animals carried Salmonella at the point of slaughter, with a range of O to 93 percent on a given day at a given establishment (Troutt et al., 2001~. Similarly, the prevalence of E. cold 0157:H7 among culled dairy cattle at market in the NAHMS study was 1.8 percent, twice that on the farm, and, when tested a single time, 31 percent of the markets had a positive animal (Wells et al., 1998~. In a recent survey of cattle in 29 pens in 5 major feedlots, and based on a single fecal sample from each animal, 23 percent of individual animals and 100 percent of feedlot pens were positive for E. cold 0157:H7 (Smith et al., 2001~. The environmental conditions in the pen (e.g., muddy grounds after a rain) were associated with the likelihood of finding the pathogen. The final point of potential introduction and amplification of live-animal contamination with pathogens is the holding pens immediately before slaughter- ing. Two recent studies suggest that, for swine and cattle, the abattoir terminal holding pen is a significant point of contamination with E. cold 0157:H7 and that, therefore, sanitation of the terminal holding pen is likely to be an important control point for this pathogen (Avery et al., 2002; Hurd et al., 2001~. In summary, the committee concludes that efforts to reduce preslaughter contamination are likely to be an important part of a farm-to-table food safety strategy, not only to reduce pathogen load at the slaughter plant, but also to prevent the hazard from direct contact with infected animals, from runoff on feedlots and farms, and from contaminated water supplies (Crump et al., 2002; Hilborn et al., 1999; Kassenborg et al., 1998; Martin et al., 1986; O'Brien and Adak, 2002; PPHB,2000~. This prevention process, beneficial to both animal and human health, comprises on-farm management practices that may reduce the spread and amplification of pathogens, as may sanitation practices during trans- portation and in feedlots, final holding pens, and slaughter boxes. Moreover, measures that increase the resistance of animals to intestinal contamination in the last days of their lives should be examined and evaluated through formal inter- vention trials.

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72 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD Therefore, the committee recommends that USDA conduct or fund research on the role of nonfocal carriage and commingling prior to and after slaughter to elucidate the factors that contribute to the microbial pathogen contamination of live animals, carcasses, and products. The committee also recommends a research focus on intervention trials at all stages of the production process of meat and poultry products. The committee further concludes that the level of contamination of animals coming to slaughter is likely to be associated with the contamination of the meat; therefore, monitoring levels of contamination on and in the incoming animals is likely an important measurement of the level of risk and could help determine or require the use of mitigation steps. More importantly, measures that may reduce such contamination, such as changing what animals are fed in the last week of life, reducing fecal contamination on hides in the muddy seasons, or sanitizing the terminal holding pen and kill box, should be rapidly evaluated so that the level of contamination at the slaughter plant may be reduced. Consequently, the committee recommends that industry and regulatory agen- cies continue to place greater emphasis on contamination prevention rather than rely on inspection and end-product testing to ensure the safety of meat. Monitoring Pathogen Contamination of Herds and Flocks to Assign Raw Foods to Further Processing The nature of foodborne hazards has changed dramatically over the last century since the first federal meat inspection system was created. The hazard posed by diseased and dying animals has been replaced by hazards that are more difficult to detect. Common zoonotic pathogens such as Campylobacter in broilers, S. Enteritidis in layers, E. cold 0157:H7 in cattle, and Yersinia enterocolitica in pork cause no apparent illness in the food animals that harbor them, yet can contaminate the foods produced from these animals. Public health surveillance and investigations have attempted to measure the human illness burden that these and other foodborne pathogens cause, and have traced them back to food animal reservoirs. In the absence of grossly visible markers for contamination of live animals with microbial pathogens, the effectiveness of new systems for control may depend on such measures as accurate separation of higher-risk flocks or herds from others. The Pennsylvania Egg Quality Assurance Program, for example, is an S. Enteritidis control program in layer flocks that began in 1992 (FSIS, 2002b). Routine monitoring of flocks for the presence of S. Enteritidis is part of this program and is linked to vigorous efforts to prevent contamination of the next generation of birds that will enter the farm, as well as to the diversion to pasteurization of eggs from contaminated flocks. The result has been a slow but steady decline in the proportion of egg-producing facilities that have S. Enteritidis, from 25.7 percent in 1994 to 7.3 percent in 1998 (PFMA, 2000~.

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CONTROLS FOR HAZARDS IN MEAT AND POULTRY PRODUCTS 173 A review of the change in prevalence of the four most common Salmonella serotypes found in broiler chickens in the United States indicated that all four declined substantially and significantly after the PR/HACCP rule was imple- mented (RTI, 2002~. In other countries, even more dramatic declines have been achieved by using microbial monitoring to drive farm- or flock-based control efforts. Sweden has largely controlled S. Enteritidis in chicken-rearing operations (Wierup et al., 1995~. This achievement, however, has come at a high cost derived from destruction of contaminated flocks. The European Union, in turn, issued a directive in 1992 mandating the screening of flocks and herds for S. Enteritidis and S. Typhimurium with a view to subsidized destruction of those found to be contaminated (EC, 1992~; Denmark, Finland, Sweden, and Ireland joined the program by 1999 (Murder and Schlundt, 1999~. However, given the vast differ- ence in the scale of poultry production between the United States and European countries, such an approach would need to be structured differently in the United States. In 2001, Norway launched a national control program for Campylobacter based on the testing of chicken flocks and of finished carcasses; chickens from positive flocks are slaughtered after the negative flocks to minimize cross- contamination, and the carcasses are either sent for supervised cooking or are frozen (Norwegian Zoonosis Centre, 2002~. It is too soon to tell whether carcass contamination with Campylobacter has actually been reduced as a result of this program. DO MEAT AND POULTRY PERFORMANCE STANDARDS IMPROVE PUBLIC HEALTH? The committee recognizes that substantial declines in four bacterial foodborne diseases observed in the United States via FoodNet surveillance since 1996 indicate that the collective efforts to improve food safety are having an effect (CDC, 2002~. As the most prominent declines are in infections caused by the meat-associated pathogens Campylobacter, Listeria, and Y. enterocolitica- 27, 35, and 49 percent declines, respectively it is likely that the PR/HACCP rule is contributing to this effect, although concurrent changes in distribution, retail, and consumer behavior could also be important in decreasing infections due to such pathogens (CDC, 2002~. The fact that no sustained decline has been observed yet in infections caused by E. cold 0157:H7 may mean that the estab- lished zero tolerance for this pathogen does not offer added protection, perhaps because the principal determinants of contamination are preslaughter, or perhaps because it was effective and blunted what otherwise would have been an increase. The data needed to distinguish between these possibilities are lacking. The de- cline in listeriosis is particularly noteworthy. Listeriosis declined between 1988 and 1995 and had appeared to reach a plateau. Further industry efforts, including formulation and process changes, stimulated by a large outbreak associated with

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74 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD hot dogs in 1999, as well as efforts to educate high-nsk populations, may have resulted in an additional 35 percent decline (CDC, 2002) in human cases. A persistent challenge is that attributing such changes to any one factor is difficult because many food safety measures may be taking place at the same time, and because a given infection may have multiple possible food and nonfood sources. As was recommended in Chapter 2, measuring changes in consumer behavior, as well as microbial subtyping of pathogen strains from different food sources and comparison with isolates from human infections, could help conquer this challenge. REFERENCES APHIS (Animal and Plant Health Inspection Service). 1996. Dairy '96. Part 1: Reference of 1996 Dairy Management Practices. Online. U.S. Department of Agriculture (USDA). Available at http://www.aphis.usda.gov/vs/ceah/cahm/Dairy_Cattle/dr96desl.pdf. Accessed July 19, 2002. Avery S. Small A, Reid CA, Buncic S. 2002. Pulsed field gel electrophoresis characterization of Shiga-toxin producing Escherichia cold 0157:H7 from hides of cattle at slaughter. J Food Prot 65: 1 172-1 176. Becker E. 2003, January 23. Government in showdown in bid to shut beef processor. New York Times. P. A16. Besser TE, Richards BL, Rice DH, Hancock DD. 2001. Escherichia cold 0157:H7 infection of calves: Infectious dose and direct contact transmission. Epidemiol Infect 127:555-560. Caswell JA, Hooker NH. 1996. HACCP as an International Trade Standard. Am JAgric Econ 78:775- 779. CDC (Centers for Disease Control and Prevention). 2002. Preliminary FoodNet Data on the inci- dence of foodborne illnesses Selected sites, United States, 2001. Morb Mortal Wkly Rep 51 :325-329. CFSAN (Center for Food Safety and Applied Nutrition). 2003. Real Progress in Food Code Adop- tions. Online. Food and Drug Administration (FDA). Available at http://vm.cfsan.fda.gov/~ear/ fcadopt.html. Accessed April 10, 2003. Cockbill C. 1991. The Food Safety Act: An introduction. Br Food J 93:4-7. Conner DE, Davis MA, Zhang L. 2001 Poultry-borne pathogens: Plant considerations in poultry meat processing. In: Sams AR, ed. Poultry Meat Processing. Boca Raton, FL: CRC Press. Pp. 137-158. Crump J. Sulka A, Angulo FJ. 2002. An outbreak of Escherichia cold 0157:H7 infections among visitors to a dairy farm. N Engl J Med 347:555-560. CVM (Center for Veterinary Medicine). 2002a. Animal Medicinal Drug Use Clarification Act of 1994 (AMDUCA). Online. FDA. Available at http://www.fda.gov/cvm/index/amducca/ amducatoc.htm. Accessed February 14, 2003. CVM. 2002b. Guidance for Industry. Evaluating the Safety of Antimicrobial New Animal Drugs with Regard to Their Microbial Effects on Bacteria of Human Health Concern. Online. FDA. Avail- able at http://www.fda.gov/OHRMS/DOCKETS/98fr/80040a56.pdf. Accessed May 13, 2003. Dargatz D, Scott W. Thomas LA, Hancock D, Garber L. 1997. Factors associated with the presence of Escherichia cold in feces of feedlot cattle. J Food Prot 60:466-470. Dargatz D, Wells S. Fedorka-Cray P. Akkina, J. 1998. The veterinarian's role in diagnosis, treat- ment, and prevention of multidrug resistant Salmonella Typhimurium DT104. Bovine Practi- tioner 32: 1-6.

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