Serotypes Profile of Salmonella Isolates from Meat and Poultry Products January 1998 through December 2012
Tables and figures are available in the PDF version of this document, beginning on page 5.
This report is the 2012 annual report of the Salmonella serotype data. The Food Safety and Inspection Service (FSIS) conducts Salmonella serotype testing at all facilities producing select classes of food-animal carcasses and raw ground products under the Pathogen Reduction Hazard Analysis and Critical Control Point (PR/HACCP) program. Results are published once a year. The Agency believes that this information can serve as a basis for comparison of PR/HACCP data over time and provide an opportunity to examine the association between serotypes isolated from meat and poultry products and serotypes isolated from human salmonellosis cases in the United States (3).
In the early- to mid- 1990s FSIS conducted nationwide microbiological baseline studies that estimated the prevalence and levels of bacteria of public health concern, and used these to develop performance standards for carcasses of cow/bulls, steers/heifers, market hogs, broilers and also ground beef, ground chicken, and ground turkey (5). In July 1996, the Food Safety and Inspection Service (FSIS) published the PR/HACCP Systems, Final Rule, which established Salmonella performance standards for establishments that slaughter or produce selected classes of food animals or raw ground products (4). The Salmonella performance standards provide a measurable standard by which industry can calibrate their HACCP systems and FSIS inspection personnel can monitor the effectiveness of an establishment’s HACCP controls. The performance standards include a description of the maximum number of positive samples acceptable in a sample set. The number of samples in a sample set varies by product class. Later, in June, 2006, FSIS implemented Salmonella performance standards for turkey carcasses. Most recently, in 2011, FSIS implemented new performance standards for Salmonella and Campylobacter in poultry carcasses (chicken/turkey) (10).
Prior to 2006, there were two phases of the PR/HACCP for Salmonella in raw products: non-targeted and targeted testing. FSIS collected non-targeted or "A" set samples at establishments randomly selected from the population of eligible establishments with a goal of scheduling every eligible establishment at least once a year. Establishments that failed a set underwent targeted testing, which includes "B", "C", and "D" sets.
In June 2006, FSIS began to schedule establishments based on new criteria that are risk-based, rather than random (6). The new scheduling criteria focused FSIS resources on establishments with the most Salmonella-positive samples, including serotypes most frequently associated with human salmonellosis as defined by the CDC. As a result of this change in sampling, results from establishments prior to 2006 cannot be compared to those taken from 2006 onwards.
The results presented here provide an estimate of relative serotype distributions in raw products for each product class during the 16-year period following implementation of the PR/HACCP final rule (1996-2012).
FSIS inspection personnel randomly collect and submit product samples from specified establishments to one of three FSIS Field Service Laboratories (FSLs) in Athens, GA, Alameda, CA, or St. Louis, MO for Salmonella analysis (4). Prior to 2012, isolates of Salmonella-positive samples were sent to the National Veterinary Services Laboratory (NVSL) for serotyping. Since 2012, the Salmonella isolates have been serotyped by the Outbreaks Section of the Eastern Laboratory (OSEL) at the FSL in Athens, GA, using a molecular serotyping method developed by the CDC (9, 11). Any sample that cannot be serotyped using this method is sent to the USDA Animal and Plant Health Inspection Service’s (APHIS) National Veterinary Services Laboratories (NVSL) in Ames, Iowa, for traditional serotyping methodology (antisera agglutination).
Salmonella serotype sample results are stored in the FSIS Data Warehouse (DW). The DW is the Agency’s primary repository for data across FSIS for use in data analysis and reporting.
The tables presented in this report identify the ten most common Salmonella serotypes isolated annually per specific product class (1998-2012). When more than one serotype ranks in tenth place, each serotype in tenth place is listed (Tables 1-8). Therefore, the 10 most common serotypes isolated from a specified product class during a given year are identified by name while less commonly identified serotypes are included in the "other serotypes" category. Each table includes the number of isolates of each serotype and category, the percent of total serotyped isolates, and the percent of total samples collected.
In 2012 there were 1,312 Salmonella-positive meat or poultry samples analyzed and serotyped by FSIS. The 10 most common serotypes identified were:
- Kentucky (311/1312)
- Enteritidis (205/1312)
- Typhimurium (125/1312)
- Heidelberg (100/1312)
- Montevideo (95/1312)
- Schwarzengrund (37/1312)
- Hadar (37/1312)
- Infantis (35/1312)
- Thompson (31/1312)
- Dublin (30/1312)
- I 4,,12:i:- (30/1312)
In 2012, the CDC identified Enteritidis, Typhimurium (including Typhimurium var. 5-), Newport, Javiana, I 4,,12:i:-, Montevideo, Heidelberg, Muenchen, Infantis, and Braenderup as the ten most commonly identified serotypes causing human salmonellosis in the United States (3). The serotypes found in meat and poultry products that were among this list were Enteritidis, Typhimurium, Heidelberg, Infantis and I 4,,12:i:- and Montevideo.
Figure 2 identifies the proportion of these serotypes out of the total salmonellae isolated through PR/HACCP testing of meat and poultry products. There was year-to-year variation both within and between product classes of these more commonly isolated human serotypes.
Tables include entries classified as "not typed" and "unidentified" in the serotype profile. "Not typed" Salmonella entries were not able to be serotyped. Unidentified entries include isolates in which a single specific serotype could not be determined, those partially serotyped, and those identified as monophasic or nonmotile.
Figure 1 displays, by year, the most common serotype isolated in young chicken/broilers and the percentage of each serotype isolated in each product class during the previous 15 years.
FSIS compares the Centers for Disease Control and Prevention (CDC) data on serotypes isolated from human cases of salmonellosis to data on Salmonella serotypes isolated from meat and poultry products (2, 3). Some of the more common serotypes isolated from meat and poultry products are rarely isolated from human patients. Conversely, some of the serotypes frequently responsible for human cases of salmonellosis occur in various meat and poultry products. Of course, human salmonellosis cases are also attributable to non-FSIS regulated foods, and to non- food sources. FSIS continues to work with its public health partners to identify the proportion of human salmonellosis attributable to FSIS-regulated products.
The PR/HACCP Salmonella verification program was designed to evaluate the performance of FSIS regulated establishments using prescribed performance standards. Since the sampling program uses a risk-based sampling method, the collected data does not represent the national prevalence of serotypes within a respective product class. In response to this limitation, FSIS is considering changing its current set-based sampling to a continuous sampling model using moving windows to assess process control (8).
The restructuring of Salmonella set scheduling prevents the comparison of results from 2006 onwards to previous years. To be able to compare laboratory results, periodic nationwide baseline study results provide valid estimates of the prevalence of certain pathogens of public health concern and allow for valid statistical comparisons over time.
 Egg products under jurisdiction of USDA/FSIS are not currently under HACCP regulations.
 FSIS suspended scheduling cows/bulls from sampling in 2011 and market hogs and steer/heifers in 2012 because of the low number of positive samples.
 Monophasic means that the Salmonella will produce only one kind of flagellin based on its genetic make-up.
 Non motile means that there is no genetic code in the Salmonella for the development of functional flagellin.
1CDC.2006. PHLIS Surveillance Data, Salmonella Annual Summary. Available at: http://www.cdc.gov/ncidod/dbmd/phlisdata/salmonella.htm. .
2CDC. 2013. Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food – Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 – 2012. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6215a2.htm?s_cid=mm6215a2_w.
3CDC. 2012. National Enteric Disease Surveillance: Salmonella Annual Report, 2011
5Federal Register. 2005. Generic E. Coli and Salmonella Baseline Results. Available at: http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/02-046N.pdf.
8Federal Register. 2013. Changes to the Salmonella Verification Sampling Program: Analysis of Raw Beef for Shiga Toxin-Producing Escherichia coli and Salmonella. http://www.fsis.usda.gov/wps/wcm/connect/d6372360-f296-43c7-bc79-bbdd29441cf7/2012-0038.htm?MOD=AJPERES.
9Fitzgerald C., Collins, M., Duyne, S., Mikoleit, M., Brown, T., Fields, P. 2007. Multiplex, Bead-Based Suspension Array for Molecular Determination of Common Salmonella Serotypes. J Clin Microbiol. 2007 October; 45(10): 3323–3334. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2045348/.
10FSIS. 2011. New Performance Standards for Salmonella and Campylobacter in Chilled Carcasses at young chicken and Turkey Slaughter Establishments. http://www.fsis.usda.gov/OPPDE/rdad/FSISNotices/31-11.pdf.
11McQuiston, J., Waters, R., Dinsmore, B., Mikoleit, L., Fields, P. 2011. Molecular Determination of H Antigens of Salmonella by Use of a Microphere-Based Liquid Array. J Clin Microbiol. 2011 February; 49(2): 565–573. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3043481/.