Mathematical models that estimate the proportion of foodborne illnesses attributable to food commodities at specific points in the food chain may be useful to risk managers and policy makers to formulate public health goals, prioritize interventions, and document the effectiveness of mitigations aimed at reducing illness. Using human surveillance data on laboratory-confirmed Salmonella infections from the Centers for Disease Control and Prevention and Salmonella testing data from U.S. Department of Agriculture Food Safety and Inspection Service's regulatory programs, we developed a point-of-processing foodborne illness attribution model by adapting the Hald Salmonella Bayesian source attribution model. Key model outputs include estimates of the relative proportions of domestically acquired sporadic human Salmonella infections resulting from contamination of raw meat, poultry, and egg products processed in the United States from 1998 through 2003. The current model estimates the relative contribution of chicken (48%), ground beef (28%), turkey (17%), egg products (6%), intact beef (1%), and pork (<1%) across 109 Salmonella serotypes found in food commodities at point of processing. While interpretation of the attribution estimates is constrained by data inputs, the adapted model shows promise and may serve as a basis for a common approach to attribution of human salmonellosis and food safety decisionmaking in more than one country.
The Food Safety and Inspection Service (FSIS) conducted microbiological testing programs for ready-to-eat (RTE) meat and poultry products produced at approximately 1,800 federally inspected establishments. All samples were collected at production facilities and not at retail. We report results here for the years 1990 through 1999. Prevalence data for Salmonella, Listeria monocytogenes, Escherichia coli O157:H7, or staphylococcal enterotoxins in nine different categories of RTE meat and poultry products are presented and discussed. The prevalence data have certain limitations that restrict statistical inferences, because these RTE product-testing programs are strictly regulatory in nature and not statistically designed. The cumulative 10-year Salmonella prevalences were as follows: jerky, 0.31%; cooked, uncured poultry products, 0.10%; large-diameter cooked sausages, 0.07%; small-diameter cooked sausages, 0.20%; cooked beef, roast beef, and cooked corned beef, 0.22%; salads, spreads, and pâtés, 0.05%; and sliced ham and luncheon meat, 0.22%. The cumulative 3-year Salmonella prevalence for dry and semidry fermented sausages was 1.43%. The cumulative 10-year L. monocytogenes prevalences were as follows: jerky, 0.52%; cooked, uncured poultry products, 2.12%; large-diameter cooked sausages, 1.31%; small-diameter cooked sausages, 3.56%; cooked beef, roast beef, and cooked corned beef, 3.09%; salads, spreads, and pâtés, 3.03%; and sliced ham and luncheon meat, 5.16%. The cumulative 3-year L. monocytogenes prevalence for dry and semidry fermented sausages was 3.25%. None of the RTE products tested for E. coli O157:H7 or staphylococcal enterotoxins was positive. Although FSIS and the industry have made progress in reducing pathogens in these products, additional efforts are ongoing to continually improve the safety of all RTE meat and poultry products manufactured in federally inspected establishments in the United States.
A screening method was developed for the isolation of Escherichia coli O157:H7 from raw ground beef. Suspensions at a 1:10 dilution of beef were made in a modified EC broth with novobiocin (mEC+n; EC broth with 1.12 g/L instead of 1.5 g/L Bile salts #3 and novobiocin at 20 mg/L). The samples were macerated in a Stomacher for 2 min and either shaken at 37°C (100 RPM) for 6 h, or incubated static at 35°C for 24 h. Appropriate dilutions of the cultures were then spread plated on 150×15 mm plates of MacConkey sorbitol agar (MSA). The MSA plates were incubated at 42°C overnight. A set of two plates consisting of a deep (40 ml/plate) phenol red sorbitol agar plate with 4-methylumbelliferyl ß-D-glucuronide (PRS-MUG), and a Levine EMB agar plate with added agar for a final concentration of 3%, were gridded into 12 numbered sections. Sorbitol negative colonies were picked from the MSA plates, spread on the appropriate section of the EMB, and stabbed into the corresponding section on the PRS-MUG plate. Those cultures that were sorbitol negative and MUG negative on PRS-MUG and were typically E. coli on EMB were confirmed biochemically and serologically. By this procedure O157:H7 was isolated from 5 of 10 meat samples inoculated at 0.6 organisms/g, and 10 of 10 samples at the 5/g level using the 6 h shaken method. With the 24 h static incubation method, O157:H7 was isolated from 8 of 10 samples at the 0.6/g level and 10 of 10 at the 5/g level. Thirteen strains of O157:H7 inoculated at levels between 0.4 and 0.6/g were tested and 9 of the 13 were isolated with the 6 h method, and 13 of the 13 with the 24 h method. The method is reliable and simple enough to be used in large screening programs.
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 25 July 1996. 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 sets product-specific Salmonella performance standards that must be met by slaughter establishments and establishments producing raw ground products. These performance standards 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-positive samples that are allowed in a given sample set. From 26 January 1998 through 31 December 2000, federal inspectors collected 98,204 samples and 1,502 completed sample sets 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 3 years of testing at establishments of all sizes combined show that >80% of the sample sets met the following Salmonella prevalence performance standards: 20.0% for broilers, 8.7% for market hogs, 2.7% for cows and bulls, 1.0% for steers and heifers, 7.5% for ground beef, 44.6% for ground chicken, and 49.9% for ground turkey. The decreased Salmonella prevalences may partly reflect industry improvements, such as improved process control, incorporation of antimicrobial interventions, and increased microbial-process control monitoring, in conjunction with PR/HACCP implementation.
Five enrichment broths and five selective and differentia] plating media were tested for efficiency of isolation of Aeromonas spp. from chicken, beef and pork. An overnight incubation of sample in Trypticase soy broth containing 10 μg of ampicillin/ml which was spread on starch ampicillin agar or on MacConkey mannitol ampicillin agar, gave the best results. A small survey was conducted on 10 samples each of chicken thigh-meat, ground beef, and pork sausage or ground unseasoned pork purchased from local food stores. Aeromonads were found in all of the samples in numbers ranging from 4.44 × 10−2−>4.44× 103/g except for two of the pork products from which the organisms could not be isolated. Fifty-eight isolates from this survey were tested for hemolysin production and cytotoxin production; 36 isolates were tested for production of cholera-like toxin. Cytotoxin, as detected by mouse adrenyl Y1 cells and Chinese hamster ovary cells, was produced by 92.8% of the Aeromonas hydrophila isolates, by 84.6% of the Aeromonas sobria isolates and by 17.6% of the Aeromonas caviae isolates. Hemolysin production paralleled cytotoxin production in A. hydrophila and A. caviae. Of the A. sobria isolates, 69.2% were hemolysin producers. None of the isolates tested produced cholera-like toxin. It is not known whether the presence of cytotoxin- and hemolysin-producing Aeromonas species in retail meat and poultry has any public health significance, since to date there have been no reported outbreaks of Aeromonas-caused gastroenteritis traced to meat or poultry.
Escherichia coli 0157 specific antibody, coated on magnetic beads, was used to concentrate and remove the E. coli 0157:H7 from mixed cultures and meat samples. The problem of nontarget organism carryover was addressed by adding Protamine to the culture-bead sample, washing the beads three times in saline, and changing the test tubes with each wash. These modifications reduced the nontarget colony counts obtained from uninoculated meat samples. This procedure enabled consistent recovery of E. coli 0157:H7 from inoculated meat samples. The percentage of E. coli 0157:H7 cells captured, compared to the total number of cells captured, ranged from 48 to 100%. Two strains of E. coli 0157, H7 and :non-H7, appeared to compete with one another and thus reduce or prevent isolation.
The current Food Safety and Inspection Service method for detection and recovery of Escherichia coli O157:H7, (including modified EC broth with novobiocin (mEC+n) and a direct blot ELISA). was used to analyze beef and environmental samples during an investigation of a food-borne disease outbreak attributed to consumption of undercooked hamburger patties. Double-modified trypticase soy broth (dmTSB) and a commercially available dipstick immunoassay were also used to improve detection/recovery of E. coli O157:H7. A total of 1,115 beef and environmental samples was screened with the direct blot ELISA and the dipstick immunoassay; 178 presumptive-positive samples (by either or both of the screening methods) were subjected to recovery/isolation procedures. Toxigenic E. coli O157:H7 was recovered from 45 samples: 40 hamburger-patty samples produced on the epidemiologically identified date, 3 hamburger-patty samples produced on another date, and 2 beef briskets. The organism was not recovered from environmental samples. Limited quantitative analyses indicated that contaminated hamburger patties contained fewer than 4.3 CFU of E. coli O157:H7 per g. Atypical, toxigenic ornithine decarboxylase–negative E. coli O157:H7 and nontoxigenic sorbitol-positive E. coli O157:H29 were also recovered. Both enrichment broths gave strong positive reactions with the two immunoassay screening methods, but E. coli O157:H7 was recovered more often from mEC+n broth than from dmTSB. Both screening methods gave positive results for 44 of the 45 beef samples found to contain E. coli O157:H7. False-positive results were frequently observed with both screening methods.
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