Testing for Salmonella in Raw Meat and Poultry Products Collected at Federally Inspected Establishments in the United States, 1998 through 2000

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1 9 Journal of Food Protection, Vol. 6, No. 6,, Pages 9 94 Testing for Salmonella in Raw Meat and Poultry s Collected at Federally Inspected Establishments in the United States, 998 through BONNIE E. ROSE, * WALTER E. HILL, ROBERT UMHOLTZ, GERRI M. RANSOM, AND WILLIAM O. JAMES 4 Microbiology Branch, Biosciences Division, Laboratory Sample Data Management Staff, and 4 Food Animal Sciences Division, Of ce of Public Health and Science, Food Safety and Inspection Service, U.S. Department of Agriculture, 4 Independence Avenue S.W., Room 44, Aerospace Center, Washington, D.C. -, USA MS -: Received October /Accepted 4 February ABSTRACT The Food Safety and Inspection Service (FSIS) issued Pathogen Reduction; Hazard Analysis and Critical Control Point (HACCP) Systems; Final Rule (the PR/HACCP rule) on July 996. To verify that industry PR/HACCP systems are effective in controlling the contamination of raw meat and poultry products with human disease causing bacteria, this rule productspeci c Salmonella performance s that must be met by slaughter establishments and establishments producing raw ground products. These performance s are based on the prevalence of Salmonella as determined from the FSIS s nationwide microbial baseline studies and are expressed in terms of the maximum number of Salmonella- that are allowed in a given sample set. From 6 January 998 through December, federal inspectors collected 98,4 and, completed sample for Salmonella analysis from large, small, and very small establishments that produced at least one of seven raw meat and poultry products: broilers, market hogs, cows and bulls, steers and heifers, ground beef, ground chicken, and ground turkey. Salmonella prevalence in most of the product categories was lower after the implementation of PR/HACCP than in pre-pr/haccp baseline studies and surveys conducted by the FSIS. The results of years of testing at establishments of all sizes combined show that.8 of the sample met the following Salmonella prevalence performance s:. for broilers, for market hogs,. for cows and bulls,. for steers and heifers,. for ground beef, for ground chicken, and for ground turkey. The decreased Salmonella prevalences may partly re ect industry improvements, such as improved process control, incorporation of antimicrobial interventions, and increased microbial-process control monitoring, in conjunction with PR/HACCP implementation. The Food Safety and Inspection Service (FSIS) is the U.S. Department of Agriculture (USDA) agency that is responsible for ensuring the safety, wholesomeness, and accurate labeling of meat, poultry, and egg products. On July 996, the FSIS issued Pathogen Reduction; Hazard Analysis and Critical Control Point (HACCP) Systems; Final Rule (the PR/HACCP rule) (). This rule (i) requires all meat and poultry establishments to develop and implement written sanitation operating procedures; (ii) requires meat and poultry slaughter establishments to conduct microbial testing of carcasses for generic Escherichia coli to verify the adequacy of their process controls for the prevention of fecal contamination; (iii) requires all meat and poultry establishments to develop and implement a system of preventive controls, known as HACCP, to improve the safety of their products; and (iv) performance s for Salmonella prevalence that must be met by slaughter establishments and establishments producing raw ground products. The requirements of the PR/HACCP rule were implemented in stages. The requirements for sanitation operating procedures in all establishments and for generic * Author for correspondence. Tel: ; Fax: ; bonnie.rose@fsis.usda.gov. The mention of speci c products does not constitute an endorsement by the U.S. Department of Agriculture, Food Safety and Inspection Service. E. coli testing in slaughter establishments became effective on January 99. The requirements for PR/HACCP systems and the Salmonella performance s were phased in on the basis of establishment size. All large establishments (those with or more employees) were required to implement these requirements by 6 January 998. establishments (those with or more but fewer than employees and having annual sales of.$. million) were required to implement these requirements by January 999. establishments (those having fewer than employees or annual sales of,$. million) were required to implement these requirements by January. The FSIS initiated Salmonella testing in very small establishments in May. The Salmonella performance s are product speci c and are based on the prevalence of Salmonella as determined from nationwide microbial baseline studies ( 9) conducted by the FSIS before PR/HACCP was implemented. Raw products currently covered by performance s are carcasses of cows and bulls, steers and heifers, market hogs, and broilers, as well as ground beef, ground chicken, and ground turkey. The performance s were established to verify that industry PR/HACCP systems are effective in controlling harmful bacterial contaminants on raw meat and poultry products. To verify that establishments are meeting the s, federal inspection

2 98 ROSE ET AL. J. Food Prot., Vol. 6, No. 6 personnel collect randomly selected product and send them to FSIS laboratories for Salmonella analysis. Salmonella was selected as the target pathogen because it is one of the most common causes of foodborne illness, is present at varying frequencies on all types of raw meat and poultry products, and can be easily analyzed in a variety of products. In addition, various intervention strategies aimed at reducing Salmonella on raw products could also effectively reduce other foodborne pathogens. This report presents the results of FSIS Salmonella testing of broilers, market hogs, cows and bulls, steers and heifers, ground beef, ground chicken, and ground turkey from federally inspected establishments from the beginning of PR/HACCP implementation through December. MATERIALS AND METHODS Sample collection and shipment. All were aseptically collected by FSIS inspectors following the procedures described in appendix E of the PR/HACCP rule () and instructions provided on computer-generated sample request forms. Compliance consisted of for broiler carcasses, for market hog carcasses, 8 for cow and bull carcasses, 8 for steer and heifer carcasses, and for raw ground beef, ground chicken, and ground turkey. Inspection personnel were instructed to randomly collect one sample for each production day until sample were completed. Samples were placed in an insulated shipper with chilled gel-ice packs capable of maintaining refrigeration temperatures and shipped on the day of sample collection via an overnight delivery service to one of three FSIS Field Service Laboratories: the Eastern Laboratory, Athens, Ga.; the Midwestern Laboratory, St. Louis, Mo.; or the Western Laboratory, Alameda, Calif. Broiler carcasses were randomly sampled after they emerged from the immersion chill tank at the end of the drip line or at the last readily accessible point prior to packing or cut-up. Each carcass was rinsed in a sterile,-ml stomacher-type plastic bag with 4 ml of chilled buffered peptone water (BPW). At least ml of the rinse uid was decanted into a sterile sample container and shipped to an FSIS laboratory for analysis. Market hog carcasses were randomly sampled from those that had been in the cooler for $ h after slaughter. The carcasses were aseptically sampled by swabbing three -cm sites (belly, ham, and jowls) with a sterile sponge moistened with ml of chilled BPW. After swabbing, the sponge was placed in a sterile bag and shipped to an FSIS laboratory for analysis. Cow and bull carcasses and steer and heifer carcasses were randomly sampled from those that had been in the cooler for $ h after slaughter. The carcasses were aseptically sampled by swabbing three -cm sites ( ank, brisket, and rump) with a sterile sponge moistened with ml of chilled BPW. After swabbing, the sponge was placed in a sterile bag and shipped to an FSIS laboratory for analysis. Raw ground beef, ground chicken, and ground turkey were randomly selected and collected after the grinding process and, if possible, before any addition of spices or seasoning, but prior to nal packaging. A -g sample of ground product was aseptically collected with a sterile rigid plastic ring template, placed in a plastic bag, chilled, and transported to a laboratory for analysis. Sample preparation and analysis. At the laboratory, were prepared for Salmonella analysis by the addition of ml of BPW to ml of broiler carcass rinse uid, ml of BPW to the premoistened sponge, or ml of BPW to g of ground product. The prepared were mixed well and then analyzed according to procedures described in the FSIS Microbiology Laboratory Guidebook (). Sample enrichment cultures were screened with a commercially available automated immunoassay system (). All presumptive were con rmed by culture as described in the Microbiology Laboratory Guidebook. Salmonella isolates from each of the three FSIS laboratories were forwarded for serotyping to the USDA Animal and Plant Health Inspection Service, National Veterinary Services Laboratories, Ames, Iowa. Salmonella data selection criteria. For an establishment to pass the performance s established by the FSIS under the PR/HACCP rule, the maximum allowable numbers of Salmonella in a sample set were of broiler carcasses, 6 of market hog carcasses, of 8 cow and bull carcasses, of 8 steer and heifer carcasses, of ground beef, 6 of ground chicken, and 9 of ground turkey. The maximum number of allowed in a sample set was statistically designed to provide an 8 probability of the test when the establishment is operating at the established by the baseline prevalence. Establishments are sampled under a series of enforcement sequence codes. They are initially sampled randomly under sequence code A. Most establishments that are subject to one or more of the Salmonella performance s have been selected for testing at least once under sequence code A. If an establishment fails the test for sample set A, it must initiate corrective action and is then targeted for a second sample set under sequence code B. If an establishment passes the test for sample set B, it is returned to routine random testing status (code A) for the next sample set. If an establishment fails the test for sample set B, it must reassess its HACCP plan and is then tested for a third time under sequence code C to determine whether its changes to the HACCP plan have been effective. If an establishment exceeds the maximum allowed in the C set, the FSIS issues a notice of intended enforcement. If an establishment that has failed the test for sample set C takes appropriate action to correct the HACCP system and other measures to reduce the prevalence of pathogens, the enforcement action may be held in abeyance. In these cases, a subsequent sample set is begun under sequence code D to determine whether these changes are effective. Data for sequence code A, B, and C sample are included in this report. Data on the prevalence of Salmonella include all sequence code A, B, and C sample collected during the indicated year(s). No consideration is given to whether a given sample is part of a complete or an incomplete sample set. The prevalence is estimated as the number of divided by the total number of analyzed and is expressed as a percentage. Data on the percentages of sequence code A, B, and C sample meeting the Salmonella performance s are also presented. These percentages are based on sample that were completed during the speci ed year(s), as de ned by the collect date of the last sample in the sample set, and are computed by dividing the number of sample meeting the performance by the number of completed sample. Some sample were started during the previous year. Data from incomplete sample are not included. Only three sequence code D sample (two for ground beef and one for cow and bull carcasses) had been completed as of December.

3 J. Food Prot., Vol. 6, No. 6 SALMONELLA TESTING OF RAW MEAT AND POULTRY PRODUCTS 99 RESULTS From 6 January 998 through December, federal inspectors collected 98,4 for Salmonella analysis from large, small, and very small establishments that produced one of seven products: broilers, market hogs, cows and bulls, steers and heifers, ground beef, ground chicken, and ground turkey. Of these 98,4, 9,9 were from establishments being tested for sequence code A, 6,6 were from establishments being tested for sequence code B, and were from establishments being tested for sequence code C. For the same -year period,, sample were completed, as indicated by the collection date of the last sample in the sample set. Of the, total sample,,9 were sequence code A, 96 were sequence code B, and were sequence code C. The results of the Salmonella analyses of these and sample are summarized below by product category.. The performance for Salmonella in broilers is.. From 6 January 998 through December, federal inspectors collected,484 code A broiler carcass rinse for Salmonella analysis (Table ). For large broiler establishments, Salmonella prevalence in code A carcass rinse declined from.8 in calendar year (CY) 998 to 9. in CY 999 to. in CY. The overall Salmonella prevalence in broiler carcass rinse from large establishments was 9. for all years combined. For small broiler establishments, Salmonella prevalence in code A carcass rinse declined from.6 in CY 999 to. in CY. The Salmonella prevalence in the limited number (4) of collected at volunteer (early HACCP implementation) small broiler establishments in CY 998 was.. The overall Salmonella prevalence in broiler carcass rinse from small establishments was 4. for all years combined. The prevalence of Salmonella in the limited number of code A carcass rinse collected at very small broiler establishments in CY was 8.. The overall prevalence of Salmonella in code A carcass rinse from broiler establishments of all sizes for all years combined was.. From 6 January 998 through December, federal inspectors collected 48 complete code A sample from broiler establishments for Salmonella analysis, including from large establishments, 9 from small establishments, and none from very small establishments (Table ). For large broiler establishments, 9.9 of code A sample met the performance in CY 998, 9. met the in CY 999, and 96.4 met the in CY. For all years combined, 9. of code A sample from large broiler establishments met the performance. For small broiler establishments, the percentages of sample that met the performance were 8. in CY 999, 9. in CY, and for the years combined. The overall pass rate for code A sample from both large and small broiler establishments for all years combined was 9.. Federal inspection personnel collected, code B broiler carcass rinse for Salmonella analysis from CY 998 through CY, including,4 from large establishments and 69 from small establishments (Table ). The overall Salmonella prevalences in code B broiler carcass rinse for all years combined were.4 for large establishments and 4.6 for small establishments. Twenty-nine complete code B sample were collected from broiler establishments from CY 998 through CY, including from large establishments and 8 from small establishments (Table 4). For all years combined, the percentages of code B sample that met the performance were 6. for large broiler establishments and 8. for small establishments. The overall pass rate for code B sample from both large and small broiler establishments for all years combined was 9.. Federal inspection personnel collected code C broiler carcass rinse from large establishments for Salmonella analysis from CY 998 through CY (Table ). The overall Salmonella prevalence in these for all years combined was 9.. Five complete code C sample were collected from large broiler establishments from CY 999 through CY (Table 6), and all ve met the performance.. The performance for Salmonella in market hogs is. From 6 January 998 through December, federal inspectors collected 8,48 code A market hog carcass sponge for Salmonella analysis (Table ). For large market hog establishments, Salmonella prevalence in code A carcass sponge declined from.8 in CY 998 to.8 in CY 999 and then increased to 4. in CY. The overall Salmonella prevalence in market hog carcass sponge from large establishments was 4. for all years combined. For small market hog establishments, Salmonella prevalence in code A carcass sponge was 8. in CY 999 but declined to. in CY, with an overall prevalence of.9 for the years combined. The prevalence of Salmonella in code A carcass sponge collected at very small market hog establishments in CY was.. The overall prevalence of Salmonella in code A carcass sponge from market hog establishments of all sizes for all years combined was.. From 6 January 998 through December, federal inspectors collected complete code A sample from market hog establishments for Salmonella analysis, including 4 from large establishments, 46 from small establishments, and none from very small establishments (Table ). For large market hog establishments, 68.8 of code A sample met the performance in CY 998,. met the in CY 999, and 9.8 met the in CY. For all years combined, 9. of code A sample from large market hog establishments met the performance. For small market hog establishments, the percentages of sample that met the performance were. in CY 999,.6 in CY, and 6. for the years combined. The overall pass rate for code A sample from both

4 94 ROSE ET AL. J. Food Prot., Vol. 6, No. 6 TABLE. Prevalence of Salmonella in the PR/HACCP veri cation testing program for calendar years (CY) 998 through for code A sample a CY 998 CY 999 ()....,64,9 8 4, ,69,9 9 4, , ,8 9,4, ,68,9, 8 6, 9, a Prevalence estimates include all collected during the indicated CY. large and small market hog establishments for all years combined was 8.8. Federal inspection personnel collected, code B market hog carcass sponge for Salmonella analysis from CY 998 through CY, including 8 from large establishments and 64 from small establishments (Table ). The overall Salmonella prevalences in code B market hog carcass sponge for all years combined were 4.4 for large establishments and 4. for small establishments. Eighteen complete code B sample were collected from market hog establishments from CY 998 through CY, including from large establishments and from small establishments (Table 4). For all years combined, the percentages of code B sample that met the performance were.4 for large market hog establishments and 4. for small establishments. The overall pass rate for code B sample from both large and small market hog establishments for all years combined was 6.. Federal inspection personnel collected 9 code C market hog carcass sponge for Salmonella analysis from CY 999 through CY, including from large establishments in CY 999 and 8 from small establishments in CY (Table ). The Salmonella prevalences in code C market hog sponge were. for large establishments and 8.4 for small establishments. Two complete code C sample were collected from large market hog establishments during CY 999 (Table 6), and both met the performance. Cows and bulls. The performance for Salmonella in cows and bulls is.. From 6 January 998 through December, federal inspectors collected,69 code A cow and bull carcass sponge for Salmonella analysis (Table ). For large cow and bull establishments, Salmonella prevalences in code A carcass sponge were. in CY 998,.9 in CY 999, and.6 in CY. The overall Salmonella prevalence in cow and bull carcass sponge from large establishments was.6 for all years combined. For small cow and bull establishments, Salmonella prevalences in code A carcass sponge were. in CY 998 (volunteer small establishments),. in CY 999, and. in CY. The overall Salmonella prevalence in cow and bull carcass sponge from small establishments was. for all years combined. The prevalence TABLE. Percentages of code A sample meeting the Salmonella performance s for calendar years (CY) 998 through a CY 998 CY 999 () a Sample were completed during the indicated calendar year, although they may have been started during an earlier year.

5 J. Food Prot., Vol. 6, No. 6 SALMONELLA TESTING OF RAW MEAT AND POULTRY PRODUCTS 94 TABLE. Extended CY All years (998 ) Very Very,,99, 69, ,8,44,9 69, , 9, ,,,99,9,844 44, , 4,8 4 8,6 8, ,,94,9, 6, , 9, ,484 8,48,69,88,, of Salmonella in code A carcass sponge collected at very small cow and bull establishments in CY was.. The overall prevalence of Salmonella in code A carcass sponge from cow and bull establishments of all sizes for all years combined was.. From 6 January 998 through December, federal inspectors collected complete code A sample from cow and bull establishments for Salmonella analysis, including from large establishments, 4 from small establishments, and none from very small establishments (Table ). For large cow and bull establishments, the single code A sample set collected in CY 998, both collected in CY 999, and both collected in CY all met the performance. For small cow and bull establishments, the percentages of sample that met the performance were 6. in CY 999, 8. in CY, and 8.9 for the years combined. The overall pass rate for code A sample from both large and small cow and bull establishments for all years combined was. Federal inspection personnel collected 66 code B cow and bull carcass sponge for Salmonella analysis from small establishments from CY 999 through CY (Table ). The overall Salmonella prevalence in these for both years combined was 4.6. Six complete code B sample were collected from small cow and bull establishments from CY 999 through CY (Table 4). For both years combined,. of these six code B sample met the performance. Federal inspection personnel collected 4 code C cow and bull carcass sponge from small establishments for Salmonella analysis during CY 999 (Table ). The average Salmonella prevalence in these 4 code C was.. The one complete code C sample set collected from a small cow and bull establishment during CY 999 failed to meet the performance (Table 6). Steers and heifers. The performance for Salmonella in steers and heifers is.. From 6 January 998 through December, federal inspectors collected,88 code A steer and heifer carcass sponge for Salmonella analysis (Table ). For large steer and heifer establishments, Salmonella prevalences in code A carcass sponge were. in CY 998,.4 in CY 999, and. in CY. The overall Salmonella prevalence in steer and heifer carcass sponge from large establishments was. for all years combined. For small steer and heifer establishments, Salmonella prevalences in TABLE. Extended CY All years (998 )

6 94 ROSE ET AL. J. Food Prot., Vol. 6, No. 6 TABLE. Prevalence of Salmonella in the PR/HACCP veri cation testing program for calendar years (CY) 998 through for code B sample a CY 998 CY 999 () Samples Samples Samples Samples a Prevalence estimates include all collected during the indicated CY. code A carcass sponge were. in CY 999 and.6 in CY, with an overall prevalence of.4 for the years combined. The prevalence of Salmonella in code A carcass sponge collected at very small steer and heifer establishments in CY was.. The overall prevalence of Salmonella in code A carcass sponge from steer and heifer establishments of all sizes for all years combined was.. From 6 January 998 through December, federal inspectors collected 8 complete code A sample from steer and heifer establishments for Salmonella analysis, including from large establishments, from small establishments, and none from very small establishments (Table ). For large steer and heifer establishments, the single code A sample set collected in CY 998, the three collected in CY 999, and the three collected in CY all met the performance. For small steer and heifer establishments, the percentages of sample that met the performance were. of three collected in CY 999 and 8. of eight collected in CY, with an overall pass rate of 9.9 for the years combined. The overall pass rate for code A sample from both large and small steer and heifer establishments for all years combined was Federal inspection personnel collected 6 code B steer and heifer carcass sponge for Salmonella analysis from small establishments during CY (Table ). The Salmonella prevalence in these 6 was.. No complete code B sample were collected from steer and heifer establishments from CY 998 through CY (Table 4). No code C steer and heifer carcass sponge or sample were collected from CY 998 through CY (Tables and 6).. The performance for Salmonella in ground beef is.. From 6 January 998 through December, federal inspectors collected, code A ground beef for Salmonella analysis (Table ). For large establishments, Salmonella prevalences in code A ground beef were 4.9 in CY 998, 6. in CY 999, and.4 in CY. The overall Salmonella prevalence in ground beef from large establishments was. for all years combined. For small establishments, Salmonella prevalences in code A ground beef were 6.4 (of from volunteer small establishments) in CY 998, 4. in CY 999, and.4 in CY. The overall Salmonella prevalence in ground beef from small establishments was.8 TABLE 4. Percentages of code B sample meeting the Salmonella performance s for calendar years (CY) 998 through a CY 998 CY 999 () a Sample were completed during the indicated calendar year, although they may have been started during an earlier year.

7 J. Food Prot., Vol. 6, No. 6 SALMONELLA TESTING OF RAW MEAT AND POULTRY PRODUCTS 94 TABLE. Extended CY All years (998 ) Very Very , , , , ,, 66 6, for all years combined. The prevalence of Salmonella in code A ground beef collected at very small establishments in CY was.. The overall prevalence of Salmonella in code A ground beef from ground beef establishments of all sizes for all years combined was.. From 6 January 998 through December, federal inspectors collected 8 complete code A sample from ground beef establishments for Salmonella analysis, including from large establishments, 96 from small establishments, and from very small establishments (Table ). For large establishments, 88.9 of code A sample met the performance in CY 998, met the in CY 999, and 8. met the in CY. For all years combined, 84. of code A sample from large ground beef establishments met the performance. For small establishments,the percentages of sample that met the performance were 8. in CY 999, 9.9 in CY, and 89.9 for the years combined. Of the code A sample collected at very small ground beef establishments in CY, 9. met the performance. The overall pass rate for code A sample from ground beef establishments all of sizes for all years combined was Federal inspection personnel collected,8 code B ground beef for Salmonella analysis from CY 998 through CY, including 8 from large establishments,,4 from small establishments, and 84 from very small establishments (Table ). The overall Salmonella prevalences in code B ground beef for all years combined were. for large establishments, 8. for small establishments, and. for very small establishments. Thirty-eight complete code B sample were collected from ground beef establishments from CY 999 through CY, including 4 from large establishments and 4 from small establishments (Table 4). For both years combined, the percentages of code B sample that met the performance were. for large ground beef establishments and.6 for small establishments. The overall pass rate for code B sample from both large and small ground beef establishments for both years combined was.. Federal inspection personnel collected 9 code C ground beef from small establishments for Salmonella analysis from CY 999 through CY (Table ). The overall Salmonella prevalence in these code C ground beef for both years combined was.9. Five complete code C sample were collected from TABLE 4. Extended CY All years (998 )

8 944 ROSE ET AL. J. Food Prot., Vol. 6, No. 6 TABLE. Prevalence of Salmonella in the PR/HACCP veri cation testing program for calendar years (CY) 998 through for code C sample a CY 998 CY 999 () a Prevalence estimates include all collected during the indicated CY. small ground beef establishments from CY 999 through CY (Table 6). The two collected in CY 999 both failed to meet the performance, and all three collected in CY met the performance. During CY, one of the two subsequent code D sample from small ground beef establishments passed the performance, and the other failed to meet the performance (data not included in this report).. The performance for Salmonella in ground chicken is. From 6 January 998 through December, federal inspectors collected code A ground chicken for Salmonella analysis (Table ). For large establishments, Salmonella prevalences in code A ground chicken were 4. in CY 998,. in CY 999, and.4 in CY. The overall Salmonella prevalence in ground chicken from large establishments was.9 for all years combined. For small establishments, Salmonella prevalences in code A ground chicken were 6.9 in CY 999,. in CY, and.8 for the years combined. The prevalence of Salmonella in code A ground chicken collected at very small establishments in CY was 8.. The overall prevalence of Salmonella in code A ground chicken from ground chicken establishments of all sizes for all years combined was 4.4. From January 999 through December, federal inspectors collected complete code A sample from ground chicken establishments for Salmonella analysis, including from large establishments, from small establishments, and none from very small establishments (Table ). For large ground chicken establishments, no code A sample were collected in CY 998, but both of the sample collected in CY 999 and all three sample collected in CY met the performance. For small ground chicken establishments, all three code A sample collected in CY 999 and both of the sample collected in CY met the performance. The overall pass rate for code A sample from both large and small ground chicken establishments for both years combined was.. No code B or code C ground chicken or sample were collected from CY 998 through CY (Tables through 6).. The performance for Salmonella in ground turkey is. From 6 January 998 through December, federal inspectors collected,9 code A ground turkey for Salmonella anal- TABLE 6. Percentages of code C sample meeting the Salmonella performance s for calendar years (CY) 998 through a CY 998 CY 999 () a Sample were completed during the indicated calendar year, although they may have been started during an earlier year.

9 J. Food Prot., Vol. 6, No. 6 SALMONELLA TESTING OF RAW MEAT AND POULTRY PRODUCTS 94 TABLE. Extended CY All years (998 ) Very Very ysis (Table ). For large establishments, Salmonella prevalences in code A ground turkey were 6. in CY 998,. in CY 999, and 6. in CY. The overall Salmonella prevalence in ground turkey from large establishments was.8 for all years combined. For small establishments, Salmonella prevalences in code A ground turkey were.8 in CY 999,. in CY, and. for the years combined. The single code A ground turkey sample collected at a very small establishment in CY tested negative for Salmonella. The overall prevalence of Salmonella in code A ground turkey from ground turkey establishments of all sizes for all years combined was 9.. From 6 January 998 through December, federal inspectors collected 4 complete code A sample from ground turkey establishments for Salmonella analysis, including 4 from large establishments, from small establishments, and none from very small establishments (Table ). For large establishments, of code A sample met the performance in CY 998, 94.4 met the in CY 999, and 9. met the in CY. For all years combined, 9. of code A sample from large ground turkey establishments met the performance. For small establishments, the percentages of sample that met the performance were 8. in CY 999,. (one of two passed) in CY, and.4 for the years combined. The overall pass rate for code A sample from large and small ground turkey production establishments for all years combined was Federal inspection personnel collected 6 code B ground turkey for Salmonella analysis from CY 998 through CY, including 9 from large establishments and 6 from small establishments (Table ). The overall Salmonella prevalences in code B ground turkey for both years combined were 4. for large establishments and 6.4 for small establishments. Five complete code B sample were collected from ground turkey establishments from CY 998 through CY, including three from large establishments and two from small establishments (Table 4). For both years combined, the percentages of code B sample that met the performance were. for large ground turkey establishments and. for small establishments. The overall pass rate for code B sample from both large TABLE 6. Extended CY All years (998 )

10 946 ROSE ET AL. J. Food Prot., Vol. 6, No. 6 and small ground turkey establishments for all years combined was 6.. Federal inspection personnel collected 4 code C ground turkey from large establishments for Salmonella analysis during CY (Table ). The overall Salmonella prevalence in these 4 code C ground turkey was.. No complete code C sample were collected from ground turkey establishments from CY 998 through CY (Table 6). DISCUSSION The prevalence data reported here for Salmonella in raw meat and poultry products have certain limitations that restrict the range of valid statistical inferences. The HACCP veri cation program is strictly regulatory in nature and was designed to track establishment performance rather than to estimate national product Salmonella prevalence. During the rst years of the implementation of this regulatory program, the requirements for PR/HACCP systems and the Salmonella performance s were phased in on the basis of establishment size (large, small, and very small). Because the program is not statistically designed, different establishments may be sampled from year to year, confounding rigorous trend analyses. Furthermore, it is important to note that the prevalence estimates computed from the FSIS s pre-haccp baseline studies and surveys were nationally representative because they were weighted on the basis of the production volume of the sampled establishments. In contrast, the PR/HACCP Salmonella prevalences from the regulatory testing program reported here represent unweighted test results. Nonetheless, Salmonella prevalences for most of the product categories appeared to be lower after PR/HACCP implementation than they were shown to be in FSIS baseline studies and surveys conducted before the implementation of PR/HACCP. The results of years of testing in large establishments under HACCP show that the average Salmonella prevalence in enforcement sequence code A met the performance for all seven product categories. After years of testing in small establishments under HACCP, the average Salmonella prevalence in code A was lower than the performance for all product categories except market hogs (a.9 average prevalence compared with the performance ). However, the Salmonella prevalence in code A market hog carcass sponge from small establishments decreased from 8. in CY 999 to. in CY. The limited data available from very small establishments after approximately 8 months of testing under HACCP show that the Salmonella prevalence met the performance for all product categories except cows and bulls (a. prevalence compared with the. performance ). However, any speculation pertaining to the signi cance of the. Salmonella prevalence for very small cow and bull establishments would be premature, since this value is based on only 9 and no completed sample. The results of years of testing show that the majority of completed code A sample met the Salmonella performance. Salmonella compliance levels, based on the number of meeting the performance, for all sizes of establishments and all years combined were 9. for broilers, 8.8 for market hogs, for cows and bulls, 94.4 for steers and heifers, 89.6 for ground beef,. for ground chicken, and 89.4 for ground turkey. The majority of code B and C sample collected as a result of code A sample set failures also met the performance. From CY 998 through CY, only three code C sample failed to meet the performance, two from small ground beef production establishments and one from a small cow and bull establishment. Only one of the three subsequent code D sample, a set from a small ground beef production establishment, failed to meet the performance. The decreased Salmonella prevalences may partly re- ect changes due to HACCP implementation. Many establishments have incorporated antimicrobial treatments (e.g., trisodium phosphate, organic acid rinses, steam) or process adjustments (e.g., counter ow chillers or scalders, steam vacuum) in order to meet the PR/HACCP Salmonella performance s. In addition, increased attention to quality control concepts and microbial-process control monitoring, such as generic E. coli testing, probably enabled establishments to decrease process uctuations after the PR/ HACCP rule was implemented. The FSIS nds it encouraging that most establishments achieve the Salmonella performance s. While establishments failing to meet the performance s are few, they may bene t from targeted outreach and technical assistance to help them meet the performance in subsequent sample. The attainment of a reduction in pathogens reduces the risk of illness; however, all segments of the food chain as well as consumers should continue to properly handle, cook, and store all meat and poultry products in order to guard against foodborne illness. ACKNOWLEDGMENTS We gratefully acknowledge the signi cant contributions of all of the USDA/FSIS inspection personnel who collected the and the laboratory and data entry personnel at the three FSIS Field Service Laboratories. We extend a special thank you to Ms. Nancy Clyburn for her assistance with manuscript preparation. REFERENCES. Andrews, C. D., L. Dillard, M. Pratt, and J. Rivera.. FSIS procedure for the use of Salmonella rapid screening immunoassay kits, p. 4A-. In B. P. Dey and C. P. Lattuada (ed.), USDA/FSIS microbiology laboratory guidebook, rd ed., vol.. U.S. Government Printing Of ce, Washington, D.C. ( OPHS/microlab/mlgchp4a.pdf).. Rose, B. 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11 J. Food Prot., Vol. 6, No. 6 SALMONELLA TESTING OF RAW MEAT AND POULTRY PRODUCTS 94 Safety and Inspection Service, Washington, D.C., [Internet, WWW], ADDRESS: U.S. Department of Agriculture, Food Safety and Inspection Service, 996, Nationwide Broiler Chicken Microbiological Baseline Data Collection Program, U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C., [Internet, WWW], AD- DRESS: 6. U.S. Department of Agriculture, Food Safety and Inspection Service, 996, Nationwide Federal Plant Raw Ground Beef Microbiological Survey, U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C., [Internet, WWW], ADDRESS: U.S. Department of Agriculture, Food Safety and Inspection Service, 996, Nationwide Pork Microbiological Baseline Data Collection Program: Market Hogs, U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C., [Internet, WWW], ADDRESS: 8. U.S. Department of Agriculture, Food Safety and Inspection Service, 996, Nationwide Raw Ground Chicken Microbiological Survey, U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C., [Internet, WWW], ADDRESS: usda.gov/ophs/baseline/rwgrchck.pdf. 9. U.S. Department of Agriculture, Food Safety and Inspection Service, 996, Nationwide Raw Ground Turkey Microbiological Survey, U.S. Department of Agriculture, Food Safety and Inspection Service, Washington, D.C., [Internet, WWW], ADDRESS: usda.gov/ophs/baseline/rwgrturk.pdf.. U.S. Department of Agriculture, Food Safety and Inspection Service Pathogen reduction; hazard analysis and critical control point (HACCP) systems; nal rule. Fed. Regist. 6: (