Salmonella in Beef. USDA/ARS/USMARC/MSQR, Clay Center, Nebraska Texas Tech University, Lubbock, Texas USDA/ARS/SPARC/FFSR, College Station, Texas

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1 Guy H. Loneragan Salmonella in Beef Dayna M. Harhay Sara E. Gragg Tom S. Edrington Mindy M. Brashears USDA/ARS/USMARC/MSQR, Clay Center, Nebraska Texas Tech University, Lubbock, Texas USDA/ARS/SPARC/FFSR, College Station, Texas Texas Tech University, Lubbock, Texas Meat and Poultry Research Conference Marriott Country Club Plaza Kansas City, Missouri, 01-02NOV2011

2 Background Information Greatly improved microbial process control Industry development and implementation of PR/HACCP Regulatory oversight contribution Many plants now excelling at process control No manufacturing process is perfect Limited microbial control of raw commodity Successes observed in public health

3 Incidence of E. coli O157 Success: E. coli O157 Success in Progress CDC FoodNet Estimate 2010 HP Objective 2020 HP Objective 50% decline from baseline years 2.5 RGB positives/1,000 samples 2010 CY 0.7 RGB positives/1,000 samples YTD

4 Salmonella Metrics for Salmonella not as encouraging No significant change from baseline years 15.2 cases per 100,000 people per yr HP /100,000 HP /100,000 Complex > many sources, several serotypes, AMR Beef approximately 10% of cases (CDC estimate) Despite tremendous improvements in sanitary slaughter outcomes, Salmonella still a challenge Some plants struggle with RGB and its components Recalls/outbreaks have focused attention on why

5 Salmonella positives (%) Why Lack of Improvement? Could it be there are real improvements in beef that parallel E. coli O157 improvements??? Need other commodities to have gotten worse Likely some improvements in beef Certainly not parallel or E. coli O157 improvements % of 9,256 GB samples positive for Salmonella

6 Why this Lack of Improvement? Potential that Salmonella is evading effective carcass decontamination procedures Recent comments (paraphrased): We feel like we have our sanitary process under control but still have problems with Salmonella We cannot find Salmonella on the surface of our carcasses but when we grind, it is positive Salmonella harborage in the lymph nodes may contribute to these failures (JFP 71:1685-8) Research initiated by industry through the Beef Checkoff program

7 Surveillance Study Funded by the Beef Checkoff Objective: characterize prevalence of Salmonella in lymph nodes of cattle presented for harvest Fed cattle Cull dairy cattle Cattle that have passed inspections Approximately 75 subiliac lymph nodes per plant per collection window Most plants have 6 collection windows Samples trimmed, surface sterilized, cultured for Salmonella per JFP 2008;71: Subset quantified

8 From: Ruminant Lymphatic System (Saar and Getty) In Anatomy of the Domestic Animals. Eds Sisson and Grossman

9 Surveillance Study Funded by the Beef Checkoff Objective: characterize prevalence of Salmonella in lymph nodes of cattle presented for harvest Fed cattle Cull dairy cattle Cattle that have passed inspections Approximately 75 subiliac lymph nodes per plant per collection window Most plants have 6 collection window Samples trimmed, surface sterilized, cultured for Salmonella per JFP 2008;71: Subset quantified

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13 Results from Surveillance Plants from which samples were received: 5 in Texas (categorized as southern) 2 in Nebraska (categorized as northern) 2 in California (included in northern category) Most plants have 6 collection windows; 2 each in: Sep-Nov, Feb-Mar, Jul-Aug 3,254 nodes assayed to date 7.4% positive 95% CL = 6.5 to 8.3% Seasonal, regional and animal type variation

14 Prevalence of Salmonella Preliminary Results 50 Funded by the Beef Checkoff 40 Feedlot Cull cows Sep/Oct 2010 Oct/Nov 2010 Dec-10 Jan-11 Feb-11 Mar-11 Apr-11 May-11 Jun-11 Jul-11 Aug-11

15 Prevalence of Salmonella Preliminary Results 50 Funded by the Beef Checkoff 40 Feedlot Cull cows Sep/Oct 2010 Oct/Nov 2010 Dec-10 Jan-11 Feb-11 Mar-11 Apr-11 May-11 Jun-11 Jul-11 Aug-11

16 Prevalence of Salmonella Prevalence of Salmonella Feedlot Cull cows Northern Plants Feedlot Cull cows Sep/OctOct/Nov Dec-11 Jan-11 Feb-11 Mar-11 Apr-11 May-11 Jun-11 Jul-11 Aug Southern Plants Sep/OctOct/Nov Dec-11 Jan-11 Feb-11 Mar-11 Apr-11 May-11 Jun-11 Jul-11 Aug

17 Preliminary Serotype Results Results from ~40% of isolates Serotype Frequency Type (Fed/Cull/Both) Anatum 39.6 Both Montevideo 27.7 Both O7:RH 18.8 Fed Meleagridis 5.9 Fed Cerro 2.0 Fed Mbandaka 1.0 Fed Reading 1.0 Cull Typhimurium 1.0 Cull Dublin 1.0 Cull Cubana 1.0 Cull O9:R1 1.0 Cull

18 Percent of Nodes Preliminary Quantitative Estimates Load of Salmonella per gram of node 2.0 log 10 CFU/g (extreme values -0.4 to 3.8) Average weight of node 18.1 g (SEM=1.0 g) Also bimodal Mean a poor measure of central tendency Concentration generally much > than or < than mean >3 Log 10 CFU/node

19 Sources of Variation Season Fairly consistent with ecology studies (feces/hides) Region Fairly consistent with empirical data (feces) Canada 1.0% 21 feedlots (FPD 2010;7:449) Nebraska 9.1% 3 plants (JFP 2003;66:1978) TX 30.0% 37 sites (AEM 2008;74:345) Animal Type Somewhat unexpected Generally associate dairy cows with Salmonella 81.0% on feedlot cattle and 71.0% on cull cows Concentration 10-fold greater on fed cattle AEM 2008;74:345

20 Salmonella s Route to the Node? Traditional viewpoint is from gut to nodes Paired fecal and hide samples ~70 healthy dairy cattle on 3 dairies Evaluate diversity of serotypes within and on animals Multiple aliquots/animal of each sample-type cultured for Salmonella Within animals, multiple serotypes were recovered from feces (up to 3) and hides (up to 4) Serotype diversity between sample matrices

21 Serotype Diversity Serotype Hides (n=180) Sample Type Feces (n=133) P value Anatum <0.01 Cerro <0.01 Kentucky Meleagridis Montevideo <0.01 Muenchen Muenster

22 Salmonella s Route to the Node? Observations have led to a hypothesis: Transdermal route of infection from hide to lymph nodes At least for peripheral nodes Sampled by immune system >>> lymphatics >>> nodes Salmonella is a very good intracellular survivor Much more direct pathway than from the gut Image from UNL Dept of Entomology Image from Cornell NYS IPM

23 Opportunities for Control? A Discussion of Prevalence We measured prevalence That is, prevalence of Salmonella in a lymph nodes Prevalence = incidence * duration of infection To reduce prevalence, therefore, we could exploit interventions that reduce either: Rate of new infections (infections.t -1 ); or Duration of infection (t) Interventions could be technology, behavior, etc. Preliminary data provide an some insights into opportunities for control

24 Salmonella SRP Vaccine Funded by the Beef Checkoff Enrolled a convenience sample of 9 West Texas dairies (all >2,000 cows) Sampled 706 cull cows from the dairies On site or at regional auction markets (assembly) Cultured for Salmonella Serotype, susceptibility testing, quantification Salmonella recovered from 32.6% of samples Varied by month and dairy Dairy prevalence ranged from 4.4% to 86.3%

25 Prevalence, % Prevalence Variation Dairy

26 Prevalence, % Prevalence Variation Dairy

27 Prevalence, % Salmonella SRP Vaccine Association with prevalence (P=0.05) SRP Vaccine used No SRP vaccine

28 Salmonella SRP Vaccine Follow-up cohort observational study Evaluate an association between Salmonella vaccine use and Salmonella prevalence Outcome measured healthy milking cows Exposed cohort: 11 dairies that practiced whole-herd vaccination Funded by the Beef Checkoff Unexposed cohort: 11 dairies that did not Each visited on 4 occasions 50 fecal samples collected from healthy milk cows

29 Prevalence of Salmonella (%) Salmonella SRP Vaccine 28.3 versus 16.6%; P< Funded by the Beef Checkoff Round 1 Round 2 Round 3 Round 4

30 Duration of Infection Funded by the Beef Checkoff Challenge studies currently underway to evaluate vaccination and duration of infection in nodes Tom Edrington (USDA/ARS/FFSRU) Animals vaccinated on d0 and d21 Orally challenged on d35 with 10 8 to Salmonella Lymph nodes harvested over time from groups of animals

31 Summary Salmonella recovery from lymph nodes of healthy cattle presented for harvest not uncommon Likely long-standing phenomenon Generally no history of salmonellosis As sanitary processes improve, a greater proportion of Salmonella positives will be due to lymph node harborage Salmonella protected from traditional methods used in carcass decontamination Presumably protected from low-dose carcass irradiation Salmonella burden in feces, on hides, and in lymph nodes appear to be correlated (regionally)

32 Summary How do we define risk? Does any Salmonella constitute risk? Is risk associated with specific phenotypes? E.g., serotype or MDR Is risk associated with specific genotypes? E.g., virulence markers for pathogenic variants Strategies for control and surveillance may be different depending on definition

33 Research Plans Beef Checkoff Program and USDA/NIFA/NIFSI Contract # Partnership between Texas Tech, USDA/ARS/USMARC, and USDA/ARS/FFSRU Goal is to discover, evaluate, and deliver best practices to reduce the risk associated with Salmonella in lymph nodes Pre-harvest Harvest/Fab Post-harvest

34 Research Plans Beef Checkoff Program and USDA/NIFA/NIFSI Contract # Includes a series of studies to evaluate: How Salmonella survives in nodes Duration of infection Interventions (chlorate) Surveillance In-plant evaluation Risk reduction Carcass mapping Best practice development and dissemination Stay tuned

35 Collaborators to Date Chance Brooks Texas Tech University Todd Brashears Texas Tech University Kendra Nightingale Texas Tech University Mike Ballou Texas Tech University Mark Miller Texas Tech University Many Graduate Students Texas Tech University Tommy Wheeler USDA/ARS USMARC Terry Arthur USDA/ARS USMARC Mick Bosilevac USDA/ARS USMARC N. Kalchayanand USDA/ARS USMARC R. Wang USDA/ARS USMARC S. Shackelford USDA/ARS USMARC Beef industry partners Plants, advisors, facilitators USDA/FSIS Stakeholder input Funded by the Beef Checkoff

36 Many thanks to MPRC Conference organizers from several associations Research partners Beef Checkoff Program USDA/NIFA/NIFSI Contract # Texas Tech & USDA/ARS Contact Information: Guy.Loneragan@TTU.edu Texas Tech University +1 (806) x 268 Funded by the Beef Checkoff