An Eggsamination of the
Multistate Outbreak of
Salmonella Enteritidis
Josh Rounds, MPH
Epidemiologist
Minnesota Department of Health
Outline
 Salmonella Background
 History of Salmonella Enteritidis
 Minnesota Outbreak Investigations
 National Outbreak Investigation
 Recalls
 FDA Inspection Report
Background
 Over 2,000 serotypes
 Principal reservoirs = food animals
 Sources and Risk Factors

Animal Contact
• Reptiles, baby chicks, any animal

Person-to-person
• Daycares, group homes

Almost any food
• Foods of animal origin
• Produce
• Restaurants
Complexity of Salmonella in
Restaurants
Patron Illness
Undercooked
Food of Animal
Origin
Contaminated
Ready-to-Eat Foods
Contaminated Food of
Animal Origin in the
Restaurant Kitchen
Infected
Foodworkers
Environmental
Contamination
Salmonella Enteritidis
 Emerged in the 1970’s and incidence
increased dramatically peaking in the early
1990’s
 Replaced S. Gallinarum

Chicken pathogen but rarely causes human
illness
 Reservoir in commercially produced shell
eggs
Salmonella Enteritidis
 One of the most common serotypes of
Salmonella in the US
 Eggs can be internally
contaminated via
transovarian
transmission of SE
Minnesota Investigations
 Three

restaurant outbreaks in MN
Invoices provided very specific egg
information
 Sporadic


Repackaging of eggs
Cases unable to recall specific egg brand info
 Very


cases difficult to link
common PFGE pattern (SE1B1)
Most common SE PFGE pattern nationally
Also common in MN
 Had
been associated with eggs previously
0
2008-01
2008-02
2008-03
2008-04
2008-05
2008-06
2008-07
2008-08
2008-09
2008-10
2008-11
2008-12
2009-01
2009-02
2009-03
2009-04
2009-05
2009-06
2009-07
2009-08
2009-09
2009-10
2009-11
2009-12
2010-01
2010-02
2010-03
2010-04
2010-05
2010-06
2010-07
2010-08
ReceivedDate
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5
5
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7
11
11
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16
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31
30
2
1
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3
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3
8
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15
2
2
Salmonella Enteritidis SE1B1
25
20
Minnesota Investigation Timeline
Salmonella Enteritidis Mi Rancho
Investigation May, 2010
 May 20, routine interview of two cases
reveals that both report eating at Mi
Rancho
 Both cases report consuming Chili
Rellenos
 Routine interviews of 3 additional cases
with matching PFGE patterns report eating
at the restaurant
Outbreak Investigation Methods
 May 21, Environmental Assessment at
restaurant

Sanitarians collect credit card receipts and
interview restaurant staff
 Case-control study
 In total 7 cases identified (5 lab confirmed)
 Meal dates May 5, 6, 7th
Case-Control Study Results
Exposure
Chili Relleno
Cases Controls
4/7
* OR = odds ratio
†
CI = confidence interval
2/34
OR*
22.7
95% CI† p-value
2.1–339.0
0.004
Environmental Assessment Results
 All 16 employees interviewed; none
reported illness
 Review of chilli relleno preparation
 Chili’s dipped in egg whites, fried, and
refrigerated
 High potential for cross-contamination

Cook didn’t wash hands after cracking eggs
and separating whites
Traceback
 Minnesota Department of Agriculture
Conclusion
 Consumption of chili rellenos associated
with illness
 Cross-contamination from raw eggs to
cooked chili rellenos and other ready-to
to-eat foods identified as the likely
mechanism for food contamination
Salmonella Enteritidis Kingdom
Buffet Investigation June, 2010
 June 13, routine interview of two cases
reveals that both report eating at Kingdom
Buffet on May 20
 June 14, Olmsted County Public Health
Services conducts environmental
assessment of the restaurant

Credit card receipts collected and staff
interviewed
 One additional case identified
 Case Control Study
 Buffet restaurant offering 200 items daily
 Advertised as “the biggest buffet in town”
 Buffet restaurant offering 200 items daily
 Advertised as “the biggest buffet in town”
Case-Control Study Results
Exposure
Cases
Controls
p-value
2/3
0/11
0.04
Cheese Stuffed 2/3
Mushroom
Caps
0/11
0.04
Honeydew
0/11
0.04
Hard Boiled
Eggs
2/3
* Odds ratios and 95% confidence
intervals were undefined
Environmental Assessment Results
 All 12 employees interviewed; none
reported illness
 Environmental samples all negative
 Handwashing stations without hot water
and no soap in employee bathroom
 Employees handling raw products and
ready-to-eat foods without washing hands
 Soiled kitchen surfaces
Conclusion
 Specific food vehicle was not confirmed
 Multiple potential cross-contamination
issues identified
 Traceback of shell eggs conducted at later
date because of national context
Traceback
 Minnesota Department of Agriculture
Salmonella Enteritidis Muffuletta
Investigation July 2010
 July 23, routine interview of three cases
reveals that all three report eating at
Muffuletta on July 4
 July 23, City of Saint Paul Environmental
Health Services conducts environmental
assessment of the restaurant

Reservation list collected and staff
interviewed
 Case Control Study
 The restaurant was particularly helpful

Provided reservation list with patron names
and phone numbers
Case-Control Study Results
Exposure
Cases Controls
OR*
95% CI† p-value
Any eggs
4/4
8/25
3.5
1.5 – ∞
0.021
Hollandaise
Sauce
4/4
4/26
8.4
3.4 – ∞
≤0.01
* OR = odds ratio
†
CI = confidence interval
Environmental Assessment Results
 All 32 employees interviewed; none
reported illness prior to July 4

Waitress reported illness on July 24; negative
for Salmonella
 Hollandaise Sauce and Caesar dressing
made with raw eggs
Traceback
 Minnesota Department of Agriculture
Conclusion
 Hollandaise sauce and eggs associated
with illness
 Restaurant ordered to use pasteurized
eggs in hollandaise sauce and Caesar
dressing
Nationally
 From May 1 to September 14, 2010, 1,600
more cases than expected
 States notification of increase on July 21
 29 restaurants or event clusters in 11
states
 Wright County Egg was an egg supplier in
15 of these 29 restaurants or events
 Formal trace back conducted in CA, CO,
and MN
Number of Salmonella Enteritidis cases matching PFGE pattern
JEGX01.0004 reported to PulseNet, United States, 2010
*Date of isolation by week.
Epi Timeline
Regulatory Timeline







Pullets: Must be raised under SE-monitored conditions
Biosecurity: Take steps to ensure that there is no
introduction or transfer of SE into or among poultry
houses
Rodents, Flies, and Other Pest Control
Cleaning and Disinfection: Required at depopulation
ONLY if that house had an SE-positive environmental or
egg test during the life of the flock that was housed in the
house prior to depopulation
Refrigeration: Hold and transport eggs at or below 45ºF
ambient temperature beginning 36 hours after time of lay
Environmental Sampling/Testing
Egg Sampling/Testing


Eggs were repackaged under many brand
names
Albertsons, Bayview, Boomsma, Country Eggs,
Dutch Farms, Farm Fresh, Glenview, Hillandale,
James Farms, Kemps, Lucerne, Lund, Mountain
Dairy, Nulaid, Pacific Coast, Ralphs, Shoreland,
Sunshine, Sun Valley, Trafficanda, Alta Dena
Dairy, Becky, Cal Egg, Cardenas Market,
Challenge Dairy, Country Eggs, Driftwood Dairy,
E&M Ranch, Hidden Villa Ranch, Mi Pueblo,
Wagon Trail, Yucaipa Valley
 Multiple recalls were
confusing for the public
Wright County Egg
 Five facilities
with over 5
million laying
hens
 Producing over
100 million
eggs per
month
FDA Inspection Report
FDA Inspection Report
 Rodent and insect infestations
 Live wild birds observed in laying houses
and nesting in the feed mill
 Manure piled so high that “the outdoor
access doors to the manure pits at these
locations had been pushed out by the
weight of the manure, leaving open access
to wildlife or domesticated animals”
FDA Inspection Report
 17 environmental samples positive for
outbreak strain (manure, walkways,
equipment, and the feed mill)
 No final determination of original source of
contamination
Past Issues
 Poor or unsafe working
conditions, environmental
violations, the harassment of
workers and the hiring of
illegal immigrants
 Previous Salmonella
outbreaks
Congressional Hearing
 Environmental sample reports between
2008 and 2010 indicate that Wright County
Egg received 426 positive results for
Salmonella, including 73 samples that
were potentially positive for Salmonella
Enteritidis
 “We apologize to everyone who may have
been sickened by eating our eggs.”
Questions