1. Salmonella: Was It the Tomatoes? Multistate Outbreak of Salmonella Saintpaul Infections Associated with Fresh Produce C. Mack Sewell, DrPH, MS New Mexico State Epidemiologist

2. Poll Question News reports in my area about the recent Salmonella outbreak have reported an association with A. Tomatoes B. Jalapeño peppers C. Salsa D. All of the above Click on the down arrow if you can’t see the response choices.

3. Overview Outbreak recognition/salmonella surveillance Advances from genetic testing of bacteria (Pulse Net) Outbreak timeline Summary of analytic studies Laboratory investigations Summary and conclusions

4. Learning Objectives Identify key factors that allowed for the recognition of the Salmonella Saintpaul outbreak Describe important findings from the epidemiology, laboratory, and trace- back investigations Describe important observations from early stages of the outbreak and lessons for future outbreaks

5. New Mexico Notifiable Foodborne Diseases Hepatitis A Listeriosis* Shigellosis* Salmonellosis* Trichinosis Vibrio infections* Yersiniosis* Brucellosis Campylobacteriosis Cryptosporidiosis* Cyclosporiasis* Shiga toxin-producing E. coli infections (STEC)* Giardiasis *Specimen submission required Emergency Reporting (immediate) Botulism Cholera Typhoid fever* Routine Reporting (within 24 hours) Suspected foodborne or waterborne illness in two or more unrelated persons Other conditions of public health significance

6. PulseNet DNA “fingerprinting” by pulsed-field gel electrophoresis (PFGE) Salmonella, Shigella, Listeria, STEC Uploaded to state and national databases Regular searches for clusters

7. Reporting Timeline Exposure Symptom onset Stool sample collected Lab result available Report received by ID EPI or local health office Specimen received at state lab 1–3 days 1–5 days 1–3 days 0–7 days

8. State Laboratory Timeline Serotyping completed Specimen received at state lab 3–5 days 1–2 days PFGE completed Salmonella Saintpaul Pulsed-field gel electrophoresis

9. Outbreak Detection Lab reports and investigations entered into NM-EDSS (New Mexico-Electronic Disease Surveillance System) Routine analysis by surveillance team and foodborne disease epidemiologist  Condition trends  Serotype trends  PFGE trends

10. Outbreak Detection by Condition Report run on 5/21/08 70 60 50 40 30 20 10 0 JanFebMarAprMayJunJulAugSepOctNovDec Month Average 2003–2007 Incidence of Salmonellosis in New Mexico by Month, 2008 Number of Cases

11. Outbreak Detection by Condition (cont.) Report run on 5/21/08 70 60 50 40 30 20 10 0 JanFebMarAprMayJunJulAugSepOctNovDec Month Average 2003–2007 Incidence of Salmonellosis in New Mexico by Month, 2008 Number of Cases

12. Outbreak Detection by Serotype

13. Outbreak Detection by PFGE Gel ID: NM8070 Date Gel Run: 5/20/08 LaneAgeGenderSubmitterSubmittedSerotypeEnzymePatternMatch 258FemaleGallup Med Group 5/15/08SaintpaulXbalSpX009aYes 320MalePlains Reg Med Cen - Clovis 5/17/08SaintpaulXbalSpX009aYes 437Male5/17/08SaintpaulXbalSpX009aYes

14. Outbreak Detection by PFGE (cont.) OrganismPattern# in May 2008 # in Apr 2008 # up to date in 2008 # in 2007 Salm B, one phase (14,5,12:i:-) TyX06114511 Salm B, ser Typhimurium TyX1182020 Salm B, ser. Agona AgX0311010 Salm B, ser. Heidelberg HeX0201021 Salm B, ser. Paratyphi B PRX0111010 Salm B, ser. Saintpaul SpX009a360 1 New Mexico Excerpt of Summary Report — May 2008

15. Early Timeline Wednesday, 5/21  NM State Lab reports 4 PFGE matched S. Saintpaul cases to epi  15 other isolates pending typing and PFGE  NM epi begins shotgun (hypothesis-generating) interviews Thursday, 5/22  NM epi organizes outbreak team  Email to foodborne listserv  CDC notified, conference call with NM partners  Shotgun interviews continue statewide Friday, 5/23  PFGE matches in TX (2) and CO (1)  First multistate conference call

16. Early Timeline (cont.) Sunday, 5/25  20 shotgun interviews completed  Raw tomatoes most commonly consumed item (84%)  Case control study planning begins Friday, 5/30  Preliminary analysis of NM case control study suggests association with tomatoes  FDA joins conference calls Saturday, 5/31  Combined NM and TX analysis by CDC shows strong association with tomatoes and not salsa  NM DOH announces link to tomatoes  FDA initiates tracebacks

17. Grand Timeline May 21Outbreak detected by NM DOH. May 31Case control study (NM, TX, CDC). June 3FDA issues tomato advisory for consumers (NM, TX). June 7FDA widens tomato advisory to all states. JuneClusters of cases mostly in TX associated with Mexican-style food restaurants; other states affected. June 30MN cluster of cases associated with garnish (raw jalapenos, red bell peppers— but no tomatoes). JuneMultistate case control study. Cases associated with eating at Mexican-style restaurants and salsa.

18. Grand Timeline (cont.) July AZ, NM, Navajo Nation, and IHS complete another case control study—raw jalapenos in the home associated with illness, but no association at the individual level with jalapeno consumption. July 7NC DOH cluster of cases at Mexican-style restaurant associated with guacamole. JulyFDA traces jalapenos to distributors in TX and Mexico, and a Mexican farm.  Outbreak strain cultured from jalapeno (from a Mexican farm that also grows roma tomatoes and serrano peppers).  Strain was grown from a serrano and water sample at another Mexican farm.

19. Poll Question Which one of the following states has not reported a case of Salmonella Saintpaul infection during this outbreak? A. Washington B. Idaho C. Alaska D. Oregon Click on the down arrow if you can’t see the response choices.

20. Salmonella Cases Source: CDC Cases infected with Salmonella Saintpaul, as of 8/21/08

21. Incidence of Salmonella Source: CDC Incidence of cases infected with Salmonella Saintpaul, as of 8/21/08

22. Infections by Date of Onset 50 45 40 35 30 25 20 15 10 5 0 Number of persons Illnesses that began during this time may not yet be reported *Some illness onset dates have been estimated from other reported information Date of illness onset 4/1 4/8 4/15 4/22 4/29 5/6 5/135/20 5/27 6/3 6/10 6/176/24 7/1 7/8 7/15 7/22 7/29 8/5 8/12 8/19 8/26 Infections of Salmonella Saintpaul, by date of illness onset,* as of 8/21/08 N = 1707 for whom information was reported Source: CDC

23. Study Results 1438 cases in 43 states, DC, and Canada by August 21, 2008 13 analytic studies in multiple states Initial case-control study (NM, TX, CDC): 51 cases and 106 controls  Association with raw tomatoes O.R = 6.71; 95% CI = 1.94–36.04).  Illness was not associated with other food items including salsa, pico de gallo, and guacamole. Raw jalapenos not specifically asked about; however, there was a question about peppers.

24. Case Control Studies in Texas and CDC Cluster in a Mexican-style restaurant in north Texas (47 cases and 36 controls) Illness associated with eating salsa (OR = 62.3, 95% CI = 12.4–632.1) Salsa made with several ingredients including raw tomatoes and raw jalapenos Another cluster in two north Texas cities (33 cases and 62 controls) Illness associated with salsa (OR = 7.5, 95% CI = 1.13–undefined) Salsa made with several ingredients including canned tomatoes and raw jalapenos

25. Case Control Study in Minnesota Cluster associated with a restaurant in Roseville, MN. 19 cases and 73 controls. Illness associated with a garnish made with raw jalapenos and red bell peppers, but not tomatoes (OR = 62.0, 95% CI 12.0–321.0). Provided evidence that raw jalapenos were a source of illness.

26. Multistate Case Control Study CDC, 29 states, and one American Indian nation participated in study in mid-June. 141 cases and 281 controls. Illness associated with eating at a Mexican-style restaurant (OR = 4.64, 95% CI = 2.05–undefined). Pico de gallo (OR = 4.01, 95% CI = 1.47–17.76), freshly prepared salsa (OR = 2.08, 95% CI = 1.13–3.90), and corn tortillas (OR = 2.31, 95% CI = 1.18–4.99). Analysis by ingredients indicated an association with food items often eaten together in Mexican food, including tomatoes, jalapenos, and cilantro, but no clear association with any one item.

27. Third Multistate Case Control Study NM, AZ, Navajo Nation, IHS, and CDC conducted a third study. 41 cases and 107 controls. Illness associated with raw jalapenos in the household (OR = 3.37, 95% CI = 1.35–9.26) and a borderline association with raw serranos (OR = 2.95, 95% CI = 0.94–96.0). Illness was not associated with raw jalapenos or other foods in an associated study at the individual level (OR = 1.97, 95% CI = 0.78– 5.20).

28. North Carolina Case Control Study July: NC DOH investigated a cluster of illnesses associated with a Mexican-style restaurant in Charlotte, NC. 4 cases and 113 controls. Illness associated with eating guacamole (OR = 8.7, 95% CI = 1.1–undefined). Guacamole prepared with several ingredients including raw roma tomatoes and raw serranos; no raw jalapenos were used. This study supports the conclusion that more than one produce item was involved.

29. Produce and Environmental Microbiologic Findings Culture of large number of tomatoes did not yield outbreak strain. FDA isolated outbreak strain from a jalapeno obtained from a McAllen, TX distributor. This jalapeno was grown on a farm (Farm A) in Tamualipas, Mexico, that also grows roma tomatoes and serranos. FDA also isolated outbreak strain from a serrano and a water sample from a second farm (Farm B) in Tamualipas, Mexico, that grows jalapenos and serranos. Farm A and B sent produce to common packing facility in Mexico, which imports to the US.

30. Poll Question The following statement best represents my opinion about this outbreak: A. “Much ado about nothing.” B. “Routine and important but not serious.” C. “Reveals serious flaws in the nation’s food safety program.” D. “An embarrassment to public health.” Click on the down arrow if you can’t see the response choices.

31. Summary and Conclusions Large outbreak (over 1400 cases) of Salmonella Saintpaul occurred in spring and summer 2008. This is the largest foodborne outbreak in the past decade. Delays in initial recognition due to lack of prompt PFGE testing in some state laboratories. Epidemiologic studies suggest that there were multiple produce items that contributed to the outbreak. These produce items originated in Mexico.

32. Summary and Conclusions (cont.) Early cases were not associated with restaurants; however, many later cases were associated with restaurant clusters. Association with salsa not present until later studies. Traceback of produce is complicated and limited due to lack of labeling and adequate records of distribution. FDA is unable to share (other than in a general way) timely findings with state and local public health officials.

33. Recommendations State laboratories need to prioritize the rapid collection and PFGE testing of salmonella isolates. State and local health departments need to rapidly investigate clusters of unusual serotypes and unique PFGE patterns. Congress needs to pass legislation to improve FDA traceback of food products and increase transparency. Congress should consider legislation to require routine microbiologic testing of produce and other food items.

34. Acknowledgments State and local public health personnel throughout the country that worked on this outbreak