Understanding the Public Health Significance of Salmonella. Betsy Booren, Ph.D. Director, Scientific Affairs

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Understanding the Public Health Significance of Salmonella Betsy Booren, Ph.D. Director, Scientific Affairs June 18, 2012

2011 Salmonella Outbreaks Ground Beef Salmonella Typhimurium Kosher Broiled Chicken Livers Salmonella Heidelberg African Dwarf Frogs Salmonella Typhimurium Ground Turkey Salmonella Heidelberg Whole, Fresh Imported Papayas Salmonella Agona Alfalfa and Spicy Sprouts Salmonella Enteritidis Turkey Burgers Salmonella Hadar Cantaloupe Salmonella Panama Turkish Pine Nuts Salmonella Enteritidis Chicks and Ducklings Salmonella Agona Salmonella Johannesburg http://www.cdc.gov/salmonella/outbreaks.html; accessed May 23, 2012

2012 Salmonella Outbreaks Dry Dog Food Salmonella Infantis Raw Scraped Ground Tuna Product Salmonella Bareilly Salmonella Nchanga Small Turtles Salmonella Sandiego Salmonella Pomona Salmonella Poona Restaurant Chain A Salmonella Enteritidis http://www.cdc.gov/salmonella/outbreaks.html; accessed May 23, 2012

CDC Statements* Salmonella infection has not declined in 15 years Salmonella infections cause more hospitalizations and deaths than any other pathogen found in food One million people a year get sick from eating Salmonella contaminated food *CDC. 2011. Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010. MMWR. 60(22);749-755. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6022a5.htm. Accessed May 21, 2012.

Annual Foodborne Illness Estimates Known Foodborne Pathogens 1 Unspecified Agents 2 Total Illnesses 9.4 million 38.4 million 47.8 million Hospitalizations 55,961 71,878 127,839 Deaths 1,351 1,686 3,037 Total Illnesses estimated for all FSIS Regulated Products 3 394,770 1 Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, and Griffin PM. (2011). Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 17(1): 7-15. 2 Scallan E, Griffin PM, Angulo FJ, Tauxe RV, and Hoekstra RM. (2011). Foodborne illness acquired in the United States unspecified agents. Emerg Infect Dis. 17(1): 16-22. 3 USDA FY 2013 Budget Summary and Annual Performance Plan. http://www.obpa.usda.gov/budsum/fy13budsum.pdf. Accessed April 15, 2012.

Illnesses Attributed to Foodborne Transmission of Known Pathogens 9.4 million Parasites 2% Viruses 59% Bacteria 39% Source: Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, and Griffin PM. (2011). Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 17(1): 7-15.

Illnesses Attributed to Foodborne Transmission of Known Pathogens 9.4 million Other Viruses 1% Campylobacter 9% STEC O157:H7 1% Non-O157 STEC 1% Listeria monocytogenes 0% Salmonella 11% Norovirus 58% Other Bacteria 17% Parasites 2% Source: Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, and Griffin PM. (2011). Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 17(1): 7-15.

Illnesses Attributed to Foodborne Transmission of Known Pathogenic Bacteria 3.6 million Streptococcus spp. Group A 0% Shigella 4% Staphylococcus aureus 7% S. enterica serotype Typhi 0% Salmonella 28% V. cholerae 0% V. vulnificus 0% V. parahaemolyticus 1% Brucella 0% Vibrio spp. Other 0% Yersinia enterocolitica 3% Bacillus cereus 2% Campylobacter 23% Mycobacterium bovis 0% Listeria monocytogenes 0% Diarrheagenic E. coli 0% ETEC 0% Non-O157 STEC 3% STEC O157:H7 2% Source: Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, and Griffin PM. (2011). Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 17(1): 7-15. Clostridium botulinum 0% Clostridium perfringens 26%

Hospitalizations Attributed to Foodborne Transmission of Known Pathogens 55,961 Other Viruses 1% Campylobacter 9% STEC O157:H7 4% Norovirus 26% Non-O157 STEC 0% Parasites 9% Listeria monocytogenes 0% Other Bacteria 7% Salmonella 35% Source: Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, and Griffin PM. (2011). Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 17(1): 7-15.

Deaths Attributed to Foodborne Transmission of Known Pathogens 1,351 Norovirus 11% Other Viruses 0% Campylobacter 6% STEC O157:H7 1% Non-O157 STEC 0% Listeria monocytogenes 19% Parasites 25% Other Bacteria 10% Salmonella 28% Source: Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, and Griffin PM. (2011). Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis. 17(1): 7-15.

Progress towards Healthy People Objectives for Foodborne Illnesses 6.8 8.5 11.4 13.6 12.3 17.6 0.9 1 0.6 0.3 0.24 0.2 Incidence in 2010 Healthy People 2010 Healthy People 2020 0 4 8 12 16 **Shiga toxin-producing Escherichia coli Source: Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Incidence of Foodborne Illness 1996-2010: Listeria* 0.6 Incidence per 100,000 Population 0.5 0.4 0.3 0.2 0.1 0 2010 National Health Objective:.25 2020 National Health Objective:.20 *Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Incidence of Foodborne Illness 1996-2010: Campylobacter* 30 Incidence per 100,000 Population 25 20 15 10 5 2010 National Health Objective: 12.3 2020 National Health Objective: 8.5 0 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 *Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Incidence of Foodborne Illness 1996-2010: E. coli O157* 3 Incidence per 100,000 Population 2.5 2 1.5 1 0.5 2010 National Health Objective: 1.0 2020 National Health Objective: 0.6 0 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 *Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Incidence per 100,000 Population 20 18 16 14 12 10 8 6 4 2 0 Incidence of Foodborne Illness 1996-2010: Salmonella* 2010 National Health Objective: 6.8 2020 National Health Objective: 11.4 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 *Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Incidence of Foodborne Illness 1996-2010 Incidence per 100,000 Population 28 26 24 22 20 18 16 14 12 10 8 6 4 2 0 28 26 24 22 20 18 16 14 12 10 8 6 4 2 0 Salmonella* 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 E. coli O157* 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 28 26 24 22 20 18 16 14 12 10 8 6 4 2 0 28 26 24 22 20 18 16 14 12 10 8 6 4 2 0 Campylobacter* 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 Listeria* 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 *Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Change in E. coli O157 and Salmonella infection, 1996 2010 Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

CDC Outbreaks Among Pathogens Important to the Meat Industry - All Food : 1998-2008 Source: CDC Foodborne Outbreak Online Database. http://wwwn.cdc.gov/foodborneoutbreaks/. Accessed February 18, 2011.

Foods Associated with Salmonella Outbreaks 1 Other 2 20% Poultry 29% Vine vegetables, fruits and nuts 13% Beef 8% Pork 12% Eggs 18% 1 These contaminated ingredients or single foods (belonging to one food category) were associated with 1/3 of the Salmonella outbreaks. 2 Other includes: Sprouts, leafy greens, roots, fish, grains-beans, shellfish, oil-sugar, and dairy. Source: CDC National Outbreak Reporting System, 2004 2008.

Laboratory Confirmed Salmonella Isolates From Human Sources, 2009 Rank Serotype 2009 2004 1999 Enteritidis 1 2 2 Typhimurium 2 1 1 Newport 3 3 3 Javiana 4 4 6 Heidelberg 5 5 4 Montevideo 6 6 7 I 4,[5],12:i:- 7 7 28 Oranienburg 8 13 8 Saintpaul 9 9 14 Muenchen 10 8 5 http://www.cdc.gov/ncezid/dfwed/pdfs/salmonellaannualsummarytables2009.pdf; accessed May 23, 2012

Salmonella Enteritidis Salmonella Heidelberg Salmonella Newport Salmonella Typhimurium http://www.cdc.gov/ncezid/dfwed/pdfs/salmonellaannualsummarytables2009.pdf; accessed May 23, 2012

Laboratory Confirmed Salmonella Isolates From Nonhuman Sources, 2009 Clinical Serotype 1. Typhimurium 2. Newport 3. Dublin 4. Cerro 5. Derby Non-Clinical Serotype 1. Kentucky 2. Enteritidis 3. Heidelberg 4. Typhimurium 5. Senftenberg http://www.cdc.gov/ncezid/dfwed/pdfs/salmonellaannualsummarytables2009.pdf; accessed May 23, 2012

Salmonella Positives in Broilers* Percent Positives 25 20 15 10 5 20 67% Reduction 6.7 0 Performance Standard 2010 *FSIS results of broilers analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Broilers* Percent Positives 18 16 14 12 10 8 6 4 2 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of broilers analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Market Hogs* Percent Positives 10 9 8 7 6 5 4 3 2 1 0 8.7 72% Reduction 2.4 Performance Standards 2010 *FSIS results of market hogs analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Market Hogs* Percent Positives 5 4.5 4 3.5 3 2.5 2 1.5 1 0.5 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of market hogs analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Cows/Bulls* Percent Positives 3 2.5 2 1.5 1 0.5 2.7 81% Reduction 0.5 0 Performance Standards 2010 *FSIS results of cows/bulls analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Cows/Bulls* Percent Positives 2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of cows/bulls analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Steers/Heifers* Percent Positives 1.2 1 0.8 0.6 0.4 0.2 1 90% Reduction 0.1 0 Performance Standards 2010 *FSIS results of steers/heifers analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Steers/Heifers* 0.7 0.6 Percent Positives 0.5 0.4 0.3 0.2 0.1 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of steers/heifers analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Ground Beef* 8 7 7.5 71% Reduction Percent Positives 6 5 4 3 2 1 0 2.2 Performance Standard 2010 *FSIS results of ground beef analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Ground Beef* 3 Percent Positives 2.5 2 1.5 1 0.5 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of ground beef analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Ground Chicken* Percent Positives 50 45 40 35 30 25 20 15 10 5 0 44.6 58% Reduction 18.8 Performance Standard 2010 *FSIS results of ground chicken analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Ground Chicken* Percent Positives 50 45 40 35 30 25 20 15 10 5 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of ground chicken analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Ground Turkey* Percent Positives 60 50 40 30 20 10 49.9 80% Reduction 10.2 0 Performance Standards 2010 *FSIS results of ground turkey analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Ground Turkey* 30 25 Percent Positives 20 15 10 5 0 98-03 04 05 06 07 08 09 10 98-10 Year *FSIS results of ground turkey analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Turkey* Percent Positives 25 20 15 10 5 19.6 77% Reduction 4.6 0 Performance Standards 2010 *FSIS results of turkey analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Salmonella Positives in Turkey* 8 7 Percent Positives 6 5 4 3 2 1 0 06 07 08 09 10 Year *FSIS results of turkey analyzed for Salmonella http://www.fsis.usda.gov/pdf/progress_report_salmonella_testing.pdf#page=19; accessed May 22, 2012

Recent Activities

Petition to Declare Adulterants Salmonella Heidelberg Salmonella Newport Salmonella Hadar Salmonella Typhimurium Petition for an Interpretive Rule Declaring Specific Stains of Antibiotic-Resistant Salmonella in Ground Meat and Poultry, Centers for Science in the Public Interest, May 25, 2011

Changes in Performance Standards On July 1, 2012, new performance standards were implemented: Broilers from 20% to 7.5% Turkeys from 19.6% to 1.7%

Incidence per 100,000 Population 20 18 16 14 12 10 8 6 4 2 0 Incidence of Foodborne Illness 1996-2010: Salmonella* 2010 National Health Objective: 6.8 2020 National Health Objective: 11.4 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 *Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996 2010

Public Health Agencies Meat/Food Industry Consumer Regulatory Agencies

What is needed Public health agencies provide accurate and timely foodborne illness attribution data. Allow stakeholders to allocate resources and scientifically justify food safety decisions. Regulators and the meat and poultry industry can accurately identify and improve any food safety gaps that may exist. Help to identify emerging foodborne risks Especially when risks not previously associated with specific foods.

What is needed Rapid adjustment to improve food safety can only occur if accurate data is made available as soon as possible to all food safety stakeholders. To complement public health data, FSIS/FDA should consider and evaluate how public health would be improved if new regulatory paths are implemented and determine if there are alternative regulatory paths that could be more effective.

What is needed One-size fits all regulatory approach is not appropriate as differences in Salmonella spp. exist across the products regulated by FSIS/FDA. Industry should also employee a process management system that addresses all Salmonella spp. not specific serovars. Process management systems are used to assess the adequacy of control within a food safety program using microbiological monitoring and could be used to make decisions in mitigating the risk of Salmonella in meat and poultry products

What is needed Consumers should better understand the risks associated with raw agricultural products in order to make the best purchasing and handling decisions for their lifestyle.

Conclusions Greater understanding of human salmonellosis is needed. Illnesses attributed to Salmonella have remained virtually stagnant since 1996 and have increased 24% since 2000. This is even more disturbing as the scientific regulatory data for the meat and poultry indicate decreases in Salmonella positives.

Final Thoughts The last decade has shown the important role cooperation and communication between public health officials, regulators, the meat industry, and other allied stakeholders have had on improving food safety. This collaborative success story, lessons learned, and the need for additional research can develop the blueprint in mitigating the Salmonella risk in meat and poultry products

Final Thoughts But additional research is needed to examine the human acquisition factors of Salmonella and examine the causative species that cause illness; if causative species are commodity specific; how to better attribute Salmonella to specific food illnesses; address what is the role of competitive exclusion in preventing illness, among others.

Understanding the Public Health Significance of Salmonella Betsy Booren, Ph.D. Director, Scientific Affairs June 18, 2012