Salmonella: Was It the Tomatoes?Multistate Outbreak of Salmonella Saintpaul Infections Associated with Fresh Produce

C. Mack Sewell, DrPH, MSNew Mexico State Epidemiologist

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.

Overview

• Outbreak recognition/salmonella surveillance

• Advances from genetic testing of bacteria (Pulse Net)

• Outbreak timeline

• Summary of analytic studies

• Laboratory investigations

• Summary and conclusions

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

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

PulseNet

• DNA “fingerprinting” by pulsed-field gel electrophoresis (PFGE)

• Salmonella, Shigella, Listeria, STEC

• Uploaded to state and national databases

• Regular searches for clusters

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

0–7 days

State Laboratory Timeline

Serotyping completed

Specimen received at

state lab 3–5 days

1–2 days

PFGE completed

Salmonella Saintpaul

Pulsed-field gel electrophoresis

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

Outbreak Detection by Condition

Report run on 5/21/08

70

60

50

40

30

20

10

0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov DecMonth

Average 2003–2007

Incidence of Salmonellosis in New Mexico by Month, 2008N

umbe

r of

Cas

es

Outbreak Detection by Condition (cont.)

Report run on 5/21/08

70

60

50

40

30

20

10

0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov DecMonth

Average 2003–2007

Incidence of Salmonellosis in New Mexico by Month, 2008N

umbe

r of

Cas

es

Outbreak Detection by Serotype

Outbreak Detection by PFGEGel ID: NM8070 Date Gel Run: 5/20/08

Lane Age Gender Submitter Submitted Serotype Enzyme Pattern Match

2 58 Female Gallup Med Group

5/15/08 Saintpaul Xbal SpX009a Yes

3 20 Male Plains Reg Med Cen - Clovis

5/17/08 Saintpaul Xbal SpX009a Yes

4 37 Male 5/17/08 Saintpaul Xbal SpX009a Yes

Outbreak Detection by PFGE (cont.)

Organism Pattern # in May 2008

# in Apr 2008

# up to date in 2008

# in 2007

Salm B, one phase (14,5,12:i:-)

TyX061 1 4 5 11

Salm B, ser Typhimurium

TyX118 2 0 2 0

Salm B, ser. Agona

AgX031 1 0 1 0

Salm B, ser. Heidelberg

HeX020 1 0 2 1

Salm B, ser. Paratyphi B

PRX011 1 0 1 0

Salm B, ser. Saintpaul

SpX009a 36 0 36 1

New Mexico Excerpt of Summary Report—May 2008

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

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

Grand TimelineMay 21 Outbreak detected by NM DOH.

May 31 Case control study (NM, TX, CDC).

June 3 FDA issues tomato advisory for consumers (NM, TX).

June 7 FDA widens tomato advisory to all states.

June Clusters of cases mostly in TX associated with Mexican-style food restaurants; other states affected.

June 30 MN cluster of cases associated with garnish (raw jalapenos, red bell peppers—but no tomatoes).

June Multistate case control study. Cases associated with eating at Mexican-style restaurants and salsa.

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 7 NC DOH cluster of cases at Mexican-style restaurant associated with guacamole.

July FDA 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.

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.

Salmonella Cases

Source: CDC

Cases infected with Salmonella Saintpaul, as of 8/21/08

Incidence of Salmonella

Source: CDC

Incidence of cases infected with Salmonella Saintpaul, as of 8/21/08

Infections by Date of Onset

504540353025201510

50

Num

ber

of p

erso

ns

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 5/13

5/20

5/27 6/3 6/1

06/1

76/2

4 7/1 7/8 7/15

7/22

7/29 8/5 8/1

28/1

98/2

6

Infections of Salmonella Saintpaul, by date of illness onset,* as of 8/21/08

N = 1707 for whom information was reported

Source: CDC

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.

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

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.

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.

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).

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.

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.

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.

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.

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.

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.

Acknowledgments

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