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Serotypes Profile of Salmonella Isolates from Meat and Poultry Products, January 1998 through December 2014

This is a summary page. The complete report, including all tables and figures, is available in PDF.

Summary

The Food Safety and Inspection Service (FSIS) conducts nontyphoidal1 Salmonella serotype testing on isolates recovered from raw meat and poultry products subject to sampling under the Pathogen Reduction Hazard Analysis and Critical Control Point (PR/HACCP) verification testing program. The results presented here provide an estimate of relative serotype distributions for each product class during the 16-year period following implementation of the PR/HACCP program (1998-2014). All data sets are reported by calendar year (CY).

Introduction

Salmonella is the leading cause of bacterial foodborne illness in the United States and causes an estimated 1.2 million illnesses, 19,000 hospitalizations and 380 deaths, each year (4). Attribution data from 2014 estimates that 360,000 (30%) of foodborne illnesses are attributed to FSIS-regulated products, which is a 9.3% decrease when compared to 2010 (16,22). The Centers for Disease Control and Prevention (CDC) reports that the severity of disease depends on a variety of factors including host-specific and pathogen-specific factors including the serotype designation (6). Although there are more than 2,500 Salmonella serotypes, it is estimated that less than 100 of them cause human illness (6).

FSIS is committed to implementing, revising and enforcing programs that align with FSIS’ strategic goals and Healthy People 2020 Goals to reduce Salmonella illnesses attributable to FSIS-regulated products (16,17,18). To this end, FSIS reviews serotype data generated through PR/HACCP sampling to monitor trends of isolates identified in various products to proactively guide decisions affecting food safety and public health.

PR/HACCP program

In the early- to mid-1990s, FSIS conducted nationwide microbiological baseline studies to estimate the prevalence and levels of bacteria of public health concern in specific food commodities (7,8). In July 1996, FSIS published the (PR/HACCP) Systems, Final Rule, based on these baseline studies which established pathogen reduction performance standards for Salmonella for establishments that slaughter selected classes of food animals or produce raw ground products including carcasses of cow/bulls, steers/heifers, market hogs2, broilers (young chicken), ground beef, ground chicken, and ground turkey (7). In June 2006, FSIS implemented Salmonella performance standards for turkey carcasses (13). In 2011, FSIS implemented performance standards for Campylobacter and more stringent standards for Salmonella in poultry carcasses (chicken/turkey) (14,15).

The Salmonella performance standards provide a measure by which industry and FSIS inspection personnel can evaluate whether the food safety system at a particular establishment is effectively controlling Salmonella. Under a performance standard, each establishment is subjected to a series of sampling events. The number of samples and allowable positives in a set of samples (sample set) vary by product class and pathogen (7,8). The Agency believes that a reduction in human illness should result from the implementation and enforcement of performance standards because a smaller proportion of raw meat and poultry products will likely be contaminated with Salmonella than would be the case without standards (11).

Serotyping

Serotyping is a process by which the types of Salmonella can be differentiated based on their surface antigens (1). The serotypes are based on standard nomenclature according to the Kaufmann-White scheme maintained by the World Health Organization (WHO) (21).

FSIS inspection personnel collect and submit product samples to one of three FSIS Field Service Laboratories (FSLs) in Athens, GA; Alameda, CA; or St. Louis, MO for Salmonella analysis. 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 (1). 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).

FSIS PR/HACCP Salmonella Data Collection

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. Additional sampling represented sets (referred to as "B", "C", and "D") collected from establishments targeted for follow-up testing following a failed set (7,8,9).

From June 2006 until the end of 2014, FSIS has scheduled establishments based on criteria that are risk-based rather than random (7,8). The new scheduling criteria focused on establishments with the most Salmonella-positive samples, including serotypes most frequently associated with human salmonellosis within each product class. (7,8,9,10). As a result of this change in sampling, results from establishments prior to June 2006 cannot be compared to those reported following the new schedule.

This report includes aggregate data based on large numbers of test results. Although these data provide insight into Salmonella contamination in products sampled under the program, FSIS verification sampling is not designed to estimate national prevalence of Salmonella by class of products. A true estimate of prevalence can only be derived from randomly selected samples in a nationwide baseline study designed specifically to determine prevalence (8).

Future Direction of PR/HACCP Sampling

In January 2015, FSIS announced changes to its current set-based model of sampling to be able to estimate the prevalence of Salmonella in FSIS products and monitor trends. The Agency has implemented routine sampling and a method called the “moving window” to assess process control (15). A moving window is one in which FSIS evaluates a set time period, 52 weeks, in a single establishment to assess process control. Routine sampling and the moving window together allows FSIS to distinguish between compliant and non-compliant establishments while collecting prevalence data. Routine sampling began with young chicken and young turkey carcasses in May 2015 (20).

Tables and Figures

Each table presented in this report identifies the ten most common Salmonella serotypes isolated annually per specific product class (1998-2014). When more than one serotype ranks in tenth place, each serotype in tenth place is listed (Table 1-8). 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. When FSIS could not identify a specific serotype or identified an isolate as monophasic3 or nonmotile4, the isolate was entered as “Unidentified” in the tables. Isolates that FSIS was unable to serotype are listed in the tables as “Not typed." 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.

Highlights of PR/HACCP Salmonella serotype data, CY 2014

In 2014, FSIS sampled across three Salmonella risk-based sampling projects including: young chicken (broiler) carcass (HC11_BR), young turkey carcass (HC11_TU), and ground beef (HCO1_GB). Among the 18055 samples collected, 472/18055 (2.6%) of the isolates were positively identified and serotyped. Among serotyped results, young chicken carcass represented the abundance of positives 324/472 (68.6%), followed by ground beef 116/472 (24.6%) and turkey carcass 32/472 (6.8%).

The top 10 Salmonella serotypes identified from PR/HACCP testing in 2014 are listed in Table 1a. FSIS uses this ranking along with the ranking of product specific serotype results to monitor industry’s compliance with regulatory standards, inform future performance standards and compare with complementary active (i.e.The Foodborne Diseases Active Surveillance Network (FoodNet)) and passive (CDC’s Public Health Laboratory Information System (PHLIS)) Salmonella surveillance data that estimate the burden of salmonellosis in the U.S. (3,4,5). Because human salmonellosis cases are commonly attributable to non-FSIS regulated foods and non-food sources, FSIS works closely with its public health partners to identify the proportion of human salmonellosis attributable to FSIS regulated products.

Table 1a.

Top 10 Salmonella serotypes (CY 2014)
*FSIS PR/HACCP

Serotype

Number of Isolates

Percent of Total Positive

Kentucky

205

43

Enteritidis

45

9.5

Montevideo

29

6.1

Typhimurium

28

5.9

Infantis

23

4.8

Dublin

16

3.4

Heidelberg
Reading
Cerro

12
12
12

2.5
2.5
2.5

Newport
Muenchen

10
10

2.3
2.3

Anatum

6

1.3

Agona

6

1.3

Total (includes all serotyped isolates)

472

 

*Commodities Include: Young Chicken (Broiler), Young Turkey and Ground Beef.

Young Chicken Carcass (Broiler):

In 2014, 8,816 young chicken carcass samples were analyzed under the PR/HACCP program (Table 1). Salmonella was isolated from 3.7% (325/8816) of these samples. Of the positive broiler samples, 60.8% (197/325) were positive for S. Kentucky followed by Salmonella Enteritidis 13.6% (44/324).

Young chicken carcasses are regarded as the product class with the greatest potential to cause exposure of the public to Salmonella (18). For this reason, FSIS continues to direct its resources toward implementing and revising performance standards to reduce the load of Salmonella in chicken carcasses. Since 1998, Salmonella Kentucky has ranked as the most common serotype identified among PR/HACCP young chicken isolates. Salmonella Kentucky, from chicken carcasses, however, is not among the serotypes commonly associated with human illness in the U.S.

Salmonella Enteritidis was the second most common serotype identified in young chicken carcasses and is currently the most common serotype associated with human illness (3,12). It also ranks as the second most common cultured confirmed isolate from PHLIS (3,5). Eggs are reported to be the most common food commodity associated with S. Enteritidis outbreaks (23). There has been a steady decline in the PR/HACCP percent positive results for S. Enteritidis in young chicken since 2010 (14.8% to 9.4%).

Ground Beef

In 2014, 7,320 ground beef samples were analyzed under the PR/HACCP program. Salmonella was isolated from 1.6% (116/7,320) of these samples which is a decrease since 2011. Of the ground beef positive samples, 22.4% (26/116) were positive for Salmonella Montevideo followed by Salmonella Dublin (12.1%) 14/116 (Figure 2). Since 1998, S. Montevideo has ranked as the most common serotype identified among PR/HACCP ground beef isolates. S. Montevideo, from ground beef, however, is not among the serotypes commonly associated with human illness in the U.S. (3,4,5,24).

Salmonella Dublin was identified as the second most common serotype among ground beef samples, in 2014. S. Dublin is reported to cause more severe illness than any other non-typhoidal Salmonella, although it is an uncommon cause of human illness (1,3,4,5).

Salmonella Dublin is a host adapted serotype found in cattle and occasionally in swine, sheep and horses that rarely infects humans (1). In a study by Jones et al., comparing the severity of illness outcomes caused by different serotypes, Salmonella Dublin was found to cause highest rate of hospitalization (67%), invasive infection (64%) and deaths (3%) when compared to other serotypes analyzed in the study. In cattle herds, S. Dublin can cause high fever, respiratory illness (especially in calves) abortions and death (26). Compounding the ability of S. Dublin to cause severe disease in both humans and animals is its increasing levels of resistance to ceftriaxone (i.e., 0-92% in humans and 0-85% in animals) the primary treatment over the last 15 years (25). Also, salmonellosis caused by S. Dublin is frequently multi-drug resistant leading to poorer clinical outcomes (24,25). Salmonella Dublin was first identified in FSIS PR/HACCP ground beef samples in 2003. Since 2003, among positive ground beef samples, S. Dublin has ranged between 5%-13%. A few positive isolates have also been noted, historically, in steer/heifer and cow/bull carcasses.

Young Turkey Carcass

In 2014, 1,919 young turkey samples were analyzed under the PR/HACCP program. Salmonella was isolated from 1.7% (32/1919) of these samples which is a decrease from 2013.Of the young turkey positive samples, 25.0% (8/32) were positive for S. Reading. Since 2012, Salmonella Reading has ranked among the top three serotypes identified among PR/HACCP isolates. S. Reading has not been considered a major contributor to human salmonellosis from turkey products in the U.S. (3,4,5).


[1] Nontyphoidal refers to all serotypes of Salmonella except for Typhi, Paratyphi A, Paratyphi B (tartrate negative) and Paratyphi C.
 
[2] 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.
 
[3] Monophasic means that the Salmonella will produce only one kind of flagellin based on its genetic make-up.
 
[4] Non-motile means that there is no genetic code in the Salmonella for the development of a functional flagellin.

 

References

1. Association of Public Health Laboratories. 2014. Salmonella serotyping in public health laboratories. Available at: http://www.aphl.org/AboutAPHL/publications/Documents/FS_SalmonellaSustainabilityWhitePaper_Nov2014.pdf

2. Bulgin, M. S. 1983. Salmonella Dublin: What Veterinarians Should Know. J. Am. Vet. Med. Assoc. 182:116–118.

3. CDC. 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. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6215a2.htm?s_cid=mm6215a2_w

4. CDC. 2014. Foodborne Disease Active Surveillance Network. Available at: http://www.cdc.gov/foodnet/trends/2014/number-of-salmonella-infections-by-serotype-2014.html

5. CDC. 2015. National Surveillance of Bacterial Foodborne Illnesses (Enteric Diseases). Available at: http://www.cdc.gov/ncidod/dbmd/phlisdata/salmonella.htm

6. CDC. 2015. Salmonella. Available at: http://www.cdc.gov/salmonella/index.html

7. Federal Register. 1996. Pathogen Reduction; Hazard Analysis and Critical Control Point (HACCP) Systems, Final Rule.

8. Federal Register. 2005. Generic E. coli and Salmonella Baseline Results. Available at: http://www.fsis.usda.gov/wps/wcm/connect/d6fe7505-36be-4a1f-afe6-4e633d2dacc8/02-046N.pdf?MOD=AJPERES

9. Federal Register. 2006. Salmonella Verification Sample Results Reporting: Agency Policy and Use in Public Health Protection. Available at: http://www.fsis.usda.gov/wps/wcm/connect/fea66683-f22a-43d2-a97e-e6c850fd67bc/04-026N.pdf?MOD=AJPERES

10. Federal Register. 2008. Salmonella Verification Sampling Program: Response to Comments and New Agency Policies. Available at: http://www.fsis.usda.gov/wps/wcm/connect/dab45316-44b2-4d75-a91e-a70f83b0cf7d/2006-0034.pdf?MOD=AJPERES

11. Federal Register. 2011. New Performance Standards for Salmonella and Campylobacter in Young Chicken and Turkey Slaughter Establishments: Response to Comments and Announcement of Implementation Schedule. Available at: http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/2010-0029.pdf

12. Foley, S., Nayak, R., Hanning, I., Johnson, T., Han, J., and Ricke S. Appl Environ Microbiol (2011). Population Dynamics of Salmonella enterica Serotypes in Commercial Egg and Poultry Production. Jul; 77(13): 4273–4279. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3127710/

13. FSIS. 2010. New Performance Standards for Salmonella and Campylobacter in Young Chicken and Turkey Slaughter Establishments; New Compliance Guides. Available at: http://www.fsis.usda.gov/wps/wcm/connect/49d574f1-b0cc-4777-ab08-98f1c50455f2/2009-0034.pdf?MOD=AJPERES

14. FSIS. 2011. Establishment Eligibility Criteria for the Salmonella Verification Sampling Program and FSIS Scheduling Algorithm for the Salmonella Verification Sampling Program for Raw Meat and Poultry FSIS http://www.fsis.usda.gov/wps/wcm/connect/f759693b-2fa9-46ee-8564-825ab4584859/Salmonella_Scheduling_Algorithm_Functions.pdf?MOD=AJPERES

15. FSIS. 2011. New Performance Standards for Salmonella and Campylobacter in Chilled Carcasses at Young Chicken and Turkey Slaughter Establishments. Available at: http://www.fsis.usda.gov/wps/wcm/connect/49d574f1-b0cc-4777-ab08-98f1c50455f2/2009-0034.pdf?MOD=AJPERES

16. FSIS. 2014. A year in Review – 2014. Available at: http://www.fsis.usda.gov/wps/wcm/connect/6f85bdf5-475a-4c15-8060-7d478ed1fd99/FY-2014-Year-in-Review.pdf?MOD=AJPERES

17. FSIS. 2014. Progress Report on Salmonella and Campylobacter Testing of Raw Meat and Poultry Products, CY 1998-2014. Available at: http://www.fsis.usda.gov/wps/portal/fsis/topics/data-collection-and-reports/microbiology/annual-progress-reports

18. FSIS. 2015. The FSIS Salmonella Action Plan: A Year One Update. Available at: http://www.fsis.usda.gov/wps/portal/fsis/topics/food-safety-education/get-answers/food-safety-fact-sheets/foodborne-illness-and-disease/salmonella/sap-one-year

19. FSIS. 2015. Baseline data. Available at: http://www.fsis.usda.gov/wps/portal/fsis/topics/data-collection-and-reports/microbiology/baseline/baseline

20. FSIS. 2015. Changes to the Salmonella and Campylobacter Verification Testing Programs for Poultry Carcasses. Available at: http://www.fsis.usda.gov/wps/wcm/connect/3379df49-cc8d-47f7-83c3-d4d802668f6c/22-15.pdf?MOD=AJPERES&CONVERT_TO=url&CACHEID=3379df49-cc8d-47f7-83c3-d4d802668f6c

21. Grimont, Patrick A.D., Weill, François-Xavier (2007). Antigenic Formulae of the Salmonella Serovars [9th Edition]. World Health Organization (WHO) Collaborating Centre for Reference and Research on Salmonella. Available at: http://www.scacm.org/free/Antigenic%20Formulae%20of%20the%20Salmonella%20Serovars%202007%209th%20edition.pdf

22. InterAgency Food Safety Analytics Collaboration (IFSAC) Project, 2015. Estimates for Salmonella, Escherichia coliO157 (E. coli O157), Listeria monocytogenes (Lm), and Campylobacter using Outbreak Surveillance Data. Available at: http://www.cdc.gov/foodsafety/pdfs/ifsac-project-report-508c.pdf

23. Jackson, B.R., Griffin, P.M., Cole, D., Walsh, K.A., Chai, S.J. 2013. Outbreak-associated Salmonella enterica Serotypes and Food Commodities, United States, 1998–2008. Available at: http://wwwnc.cdc.gov/eid/article/19/8/12-1511_article

24. Jones, T.F., Ingram, L.A., Cieslak, P.R., Vugia, D.J., Tobin-D’Angelo, M., Hurd, S., Medus, C., Cronquist, Al. 2008. Salmonellosis outcomes differ substantially by serotype. J. Infectious Dis. July 1;198 (1):109-114.

25. National Antimicrobial Resistance Monitoring System (NARMS) Integrated Report, 2013. Available at: http://www.fda.gov/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/ucm059103.htm

26. Thompson, Belinda, 2016. Salmonella Dublin Test for Blood or Milk Samples from Cattle. Available at: https://ahdc.vet.cornell.edu/news/salmonelladublin.cfm

Tables and figures are available in the PDF version of this document, beginning on page 10.

 

 

Last Modified Aug 11, 2016