Content uploaded by Ruthanne Marcus
Author content
All content in this area was uploaded by Ruthanne Marcus on Feb 23, 2014
Content may be subject to copyright.
University of Nebraska - Lincoln
DigitalCommons@University of Nebraska - Lincoln
Public Health Resources Public Health Resources
1-1-2012
Salmonella enterica Serotype Enteritidis: Increasing
Incidence of Domestically Acquired Infections
Shua J. Chai
Centers for Disease Control and Prevention
Patricia L. White
United States Department of Agriculture Food Safety and Inspection Service
Sarah L. Lathrop
University of New Mexico Health Sciences Center
Suzanne M. Solghan
New York State Department of Health
Carlota Medus
Minnesota Department of Health
See next page for additional authors
Follow this and additional works at: hp://digitalcommons.unl.edu/publichealthresources
Part of the Public Health Commons
is Article is brought to you for free and open access by the Public Health Resources at DigitalCommons@University of Nebraska - Lincoln. It has
been accepted for inclusion in Public Health Resources by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln.
Chai, Shua J.; White, Patricia L.; Lathrop, Sarah L.; Solghan, Suzanne M.; Medus, Carlota; McGlinchey, Beth; Tobin-D'Angelo,
Melissa; Marcus, Ruthanne; and Mahon, Barbara, "Salmonella enterica Serotype Enteritidis: Increasing Incidence of Domestically
Acquired Infections" (2012). Public Health Resources. Paper 164.
hp://digitalcommons.unl.edu/publichealthresources/164
SUPPLEMENT ARTICLE
Salmonella enterica Serotype Enteritidis:
Increasing Incidence of Domestically Acquired
Infections
Shua J. Chai,
1
Patricia L. White,
2
Sarah L. Lathrop,
3
Suzanne M. Solghan,
4
Carlota Medus,
5
Beth M. McGlinchey,
1
Melissa Tobin-D'Angelo,
6
Ruthanne Marcus,
7
and Barbara E. Mahon
1
1
Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
2
United States
Department of Agriculture Food Safety and Inspection Service, Omaha, Nebraska;
3
Department of Pathology, University of New Mexico Health
Sciences Center, Albuquerque;
4
Emerging Infections Program, New York State Department of Health, Albany;
5
Acute Disease Investigation and
Control Section, Minnesota Department of Health, St. Paul;
6
Georgia Department of Public Health, Atlanta;
7
Yale School of Medicine, New Haven,
Connecticut
Background. Salmonella enterica causes an estimated 1 million cases of domestically acquired foodborne illness
in humans annually in the United States; Enteritidis (SE) is the most common serotype. Public health authorities,
regulatory agencies, food producers, and food processors need accurate information about rates and changes in
SE infection to implement and evaluate evidence-based control policies and practices.
Methods. We analyzed the incidence of human SE infection during 1996–2009 in the Foodborne Diseases
Active Surveillance Network (FoodNet), an active, population-based surveillance system for laboratory-confirmed
infections. We compared FoodNet incidence with passively collected data from complementary surveillance systems
and with rates of SE isolation from processed chickens and egg products; shell eggs are not routinely tested. We
also compared molecular subtyping patterns of SE isolated from humans and chickens.
Results. Since the period 1996–1999, the incidence of human SE infection in FoodNet has increased by 44%.
This change is mirrored in passive national surveillance data. The greatest relative increases were in young children,
older adults, and FoodNet sites in the southern United States. The proportion of patients with SE infection
who reported recent international travel has decreased in recent years, whereas the proportion of chickens from
which SE was isolated has increased. Similar molecular subtypes of SE are commonly isolated from humans and
chickens.
Conclusions. Most SE infections in the United States are acquired from domestic sources, and the problem is
growing. Chicken and eggs are likely major sources of SE. Continued close attention to surveillance data is needed
to monitor the impact of recent regulatory control measures.
Salmonella enterica infection is a significant public
health problem, causing an estimated 1 million domes-
tically acquired foodborne illnesses and .350 deaths
each year in the United States [1] and an estimated
93.8 million illnesses and 155 000 deaths each year
worldwide [2]. S. enterica serotype Enteritidis (SE) is
one of the most common serotypes and continues to
cause large numbers of human illnesses in the United
States despite ongoing implementation of targeted
control and prevention measures for .25 years [3].
Effective control of SE infection has been a moving
target. An epidemic of SE illnesses associated with shell
eggs began in the northeastern United States in 1978
and spread throughout the rest of the country. By 1994,
SE was the most common Salmonella serotype causing
salmonellosis, comprising 26% of all Salmonella iso-
lates [4]. Voluntary farm-based interventions, use of
pasteurized egg products in institutions, consumer edu-
cation, and increased attention to refrigeration of eggs
helped decrease rates of SE infection during the late
1990s [3–5].
Correspondence: Shua J. Chai, MD, MPH, Enteric Diseases Epidemiology Branch,
Centers for Di sease Contr ol and Prevention, 1600 Cl ifton Rd, MS C-09, Atlanta,
GA 30333 (scha i@cdc.gov).
Clinical Infectious Diseases 2012;54(S5):S488–97
Published by Oxford University Press on behalf of the Infectious Diseases
Society of America 2012.
DOI: 10.1093/cid/cis231
S488 dCID 2012:54 (Suppl 5) dChai et al
Several high-profile outbreaks during the late 2000s, in-
cluding the largest SE outbreak ever reported from shell eggs
in 2010 [6], have refocused national attention on food safety.
National health objectives (ie, Healthy People 2020) include
as a top food safety priority reducing Salmonella infection [7].
The Food and Drug Administration (FDA) and the US De-
partment of Agriculture (USDA) Food Safety and Inspection
Service (FSIS) have made decreasing SE illnesses a high priority
performance goal and a benchmark for evaluating regulatory
effectiveness [8–10]. Progress toward food safety goals for
Salmonella, including SE, is tracked using data from the
Centers for Disease Control and Prevention (CDC) Foodborne
Diseases Active Surveillance Network (FoodNet) [11].
Public health authorities, regulatory agencies, food pro-
ducers, and food processors need clear, accurate SE sur-
veillance information to inform and evaluate evidence-based
SE control policies and practices. To examine burden of human
SE infections and understand changes over time, we analyzed
FoodNet data from the period 1996–2009. We compared
FoodNet SE data with passively collected data from
a complementary surveillance system and with rates of SE
isolation from processed chickens and egg products, 2
important sources of human SE infection. We also compared
molecular subtyping patterns of SE isolated from humans
with those from chickens.
METHODS
Data Sources
FoodNet
FoodNet actively collects data on laboratory-confirmed human
cases of infection caused by 9 pathogens transmitted commonly
through food, including Salmonella, in select sites around the
United States. FoodNet is a collaboration of the CDC, state
health departments, USDA/FSIS, and FDA. During 1996–2004,
counties and states were added to the FoodNet surveillance
area, which now includes the entire states of Connecticut,
Georgia, Maryland, Minnesota, New Mexico, Oregon, and
Tennessee and selected counties in California, Colorado, and
New York. The 2011 FoodNet population comprises approxi-
mately 47 million persons, or 15% of the US population. The
surveillance area has remained unchanged since 2004 and is,
in general, similar demographically to the US population [12].
For each case reported, FoodNet personnel collect infor-
mation on demographic characteristics (eg, age and sex),
hospitalization status (within 7 days of specimen collection
or if hospitalized as a result of infection), and outcome (alive
or dead at hospital discharge or within 7 days of specimen
collection for nonhospitalized patients). Data on recent in-
ternational travel (illness onset within 7 days after return to
United States or during travel for Salmonella)andwhether
the case was associated with an outbreak have been routinely
collected since 2004 [12].
Laboratory-based Enteric Diseases Surveillance
The CDC Laboratory-based Enteric Diseases Surveillance
(LEDS;formerlythePublicHealthLaboratoryInformation
System) passively collects information on laboratory-
confirmed isolates from state public health laboratories [13].
Clinical diagnostic laboratories submit Salmonella isolates to
state public health laboratories, which confirm the isolates as
Salmonella, perform serotyping, and voluntarily submit a report
to the CDC.
PulseNet
PulseNet is a national subtyping network for isolates for
foodborne diseases surveillance [14].Statepublichealthlab-
oratories complete pulsed-field gel electrophoresis (PFGE) on
most human Salmonella isolates and upload PFGE patterns
to the PulseNet national database, which also serves as a cen-
tral repository for PFGE data. PulseNet data are used to
identify and investigate enteric diseases outbreaks.
FSIS Salmonella Verification Testing Program
The USDA/FSIS implemented a Pathogen Reduction; Hazard
Analysis, and Critical Control Point Systems strategy [8]in
1996 that includes testing for Salmonella at US broiler chicken
processing plants. Inspectors collect and submit broiler chicken
carcass rinsates for a polymerase chain reaction (PCR)–based
screening test for Salmonella, with culture confirmation for
PCR-positive rinsates. The sampling strategy does not account
for production volume or regional or seasonal effects. It is used
to verify whether Salmonella performance standards are being
met but not to determine prevalence of contamination or to
track trends. Beginning in 2006, the testing strategy changed
from random sampling to a sampling method focusing on
establishments with the highest frequency of rinsates that
yielded Salmonella and on those serotypes most frequently
associated with human salmonellosis [15].
FSIS Microbiological Testing Program for Pasteurized Egg
Products
Shell eggs that originate from SE-positive flocks or are at higher
risk of Salmonella contamination for other reasons are diverted
for processing into pasteurized egg products; not all shell eggs
entering processing facilities are at increased risk for contami-
nation. FSIS inspects liquid, frozen, and dried egg products and
tests samples from pasteurization processes monthly with use
of PCR for Salmonella, followed by culture for PCR-positive
samples [16].
VetNet
Modeled after PulseNet, VetNet collects molecular subtyping
data for isolates obtained from the FSIS Salmonella Verification
Testing Program. The USDA Agricultural Research Service
subtypes SE isolates by PFGE and uploads patterns into the
VetNet database. USDA VetNet and CDC PulseNet PFGE
Rise in Salmonella Enteritidis Incidence dCID 2012:54 (Suppl 5) dS489
patterns are compared for surveillance and investigation of
foodborne illness outbreaks.
Statistical Analyses
FoodNet
We included all reported human cases of SE infection during
1996–2010 in the analyses. We used a negative binomial re-
gression model to estimate incidence of SE infection, adjust-
ingforchangestothesurveillanceareasandsite-to-site
variation in disease rates [17]. We compared model-adjusted
incidence of SE infection across all sites for each year during
2000–2009 with the mean model-adjusted incidence during
1996–1999. When the data were further stratified, the model
no longer converged. Therefore, for stratified analyses, we ex-
amined crude incidence during 2004–2009, when the FoodNet
catchment population was unchanged. Change in relative in-
cidence from 2004 through 2009 was calculated from a least
squares best-fit line through the plotted 2004–2009 incidence
rates.
Change in incidence was examined for age groups of ,1,
1–4, 5–59, and $60 years. Seasonality of (1) incidence of SE
infection and (2) percentage of all reported cases of Salmonella
infection due to SE were examined using month of specimen
collection. We examined changes in the proportion of persons
who reported international travel, whose infections were re-
ported to be associated with outbreaks, and who were hos-
pitalized or died; we report data only for years when ,25%
of these data were missing.
LEDS
Because of wide state-to-state variation in reporting of Sal-
monella serotypes to LEDS, a state was excluded if, in any
of the years during 2000–2009, it reported serotype in-
formation for ,80% of Salmonella isolates or it reported no
SE isolates. We compared crude SE incidence during 2000–2009
with the mean crude incidence during 1996–1999.
FSIS Salmonella Verification Testing Program
We examined SE contamination of broiler chickens during
2000–2005, the period of random sampling. We describe
yearly changes in the percentage of broiler chicken rinsates
collected that yielded SE.
FSIS Microbiological Testing Program for Pasteurized Egg
Products
We examined yearly percentages of samples of pasteurized egg
products that yielded SE during 2000–2009.
PulseNet
Because reporting to PulseNet was limited before 2005, we
examined data during 2005–2009 for yearly changes in the
most common PFGE patterns in SE isolated from humans.
Because SE is a clonal organism that has a limited number of
different PFGE patterns, we examined changes in the 5 most
commonly reported patterns by year. PFGE pattern names for
SE are reported by a numerical designation (ie, PFGE pattern
JEGX01.0004 is reported as ‘‘pattern 4’’).
VetNet
We described yearly changes in available PFGE patterns in SE
isolated from broiler chicken rinsates. The same PFGE pattern
might have different names in VetNet and PulseNet (eg, VetNet
pattern Xba1.0003 corresponds to PulseNet pattern JEGX01.
0004). For consistency, we report VetNet PFGE patterns by
their PulseNet numerical designation (ie, VetNet pattern
Xba1.0003 is reported as ‘‘pattern 4’’).
Statistical analyses were performed using SAS, version 9.2
(SAS Institute). This surveillance data review was determined
not to be research; thus, the project did not undergo human
subjects review.
RESULTS
FoodNet
Model-adjusted annual incidence of SE infection during
2000–2003 remained similar to the 1996–1999 mean of 1.9
cases per 100 000 population (Figure 1). Incidence then
steadily increased to a maximum of 2.8 cases per 100 000 pop-
ulation in 2008, representing a 44% increase since the period
1996–1999.
During 2004–2009, 6777 SE infections were reported.
Incidences among male and female individuals were similar
during this period (Table 1). Incidence was highest in the
youngest age groups (#4 years of age; 4.7–6.9 cases per
100 000). In the youngest and oldest age groups, the relative
increase in incidence (44%–75%) from 2004 through 2009
was substantially higher than among persons in the group
aged 5–59 years (25%). By FoodNet site, the mean annual
incidence was highest in Maryland, followed by Connecticut
and California. Relative incidence increased from 2004
through 2009 in states in the southern half of the United
States (Maryland, Georgia, Tennessee, and New Mexico;
range, 36%–140%) and in New York (69%); relative
incidence remained generally unchanged (#20% change) at
other sites.
Before 2006, $25% of reports were missing data on in-
ternational travel; therefore, changes in international travel
were examined using reports from the period 2006–2009
(15%–22% of reports were missing data on international
travel). The percentage of patients with SE infection who did
not report recent international travel increased steadily during
2006–2009, from 74.9% to 88.4% (Table 2). The percentage of
cases reported to be sporadic (ie, not part of an outbreak) and
the percentage of patients who were hospitalized or who died
remained generally stable during 2004–2009.
Incidence of SE infection in FoodNet during 2004–2009
peaked during the summer months and was lowest during the
S490 dCID 2012:54 (Suppl 5) dChai et al
late winter months. Conversely, the percentage of all reported
Salmonella infections due to SE peaked during the winter
months (Figure 2).
LEDS
For $1 year during 2000–2009, 11 states and the District of
Columbia reported either zero isolates of SE or serotype in-
formation for ,80% of Salmonella isolates; these states were
excluded from analysis. In the remaining 39 states, 55 221 SE
isolations were reported during 2000–2009. Incidence of SE
infection steadily decreased from the mean during 1996–1999 to
a low in 2003. The trend then reversed, with incidence generally
increasing, to a maximum in 2008 (Figure 1). The annual in-
cidences reported through LEDS during 1996–2001 were higher
than those reported through FoodNet. However, since full 10-
state representation was reached in FoodNet in 2004, the an-
nual incidence of reported SE infection has been similar in the 2
systems.
FSIS Salmonella Verification Testing Program and
Microbiological Testing Program for Pasteurized Egg Products
During 2000–2005, the percentage of young chicken rinsates
that yielded SE steadily increased, from 0.2% in 2000 to .5-fold
higher (1.3%) in 2005 (Table 3). During 2000–2009, a mean
of 0.06% of samples of pasteurized egg products tested
yielded SE.
PulseNet and VetNet
In PulseNet, approximately 80% of all human isolates of SE
from the period 2005–2009 had 1 of 5 dominant PFGE pat-
terns (Table 3). Pattern 4 was the most common (43%), fol-
lowed by pattern 5 (14%), and pattern 2 (12%). No trends
were apparent.
In VetNet, 2 PFGE patterns predominated among SE iso-
lates recovered during FSIS Salmonella broiler chicken testing
during 2000–2003: pattern 4 (39%) and pattern 5 (41%)
(Table 3). Together, these patterns represented 70%–88% of
SE isolates each year.
DISCUSSION
Although the incidence of laboratory-confirmed SE infection
decreased during the late 1990s after implementation of egg
safety measures [3], it has rebounded substantially in both
active and passive surveillance and in chicken carcass test
results. In 2008, incidence rates in FoodNet were the highest
since surveillance began in 1996. The increase in incidence
of SE infection has affected many parts of the country and
involves several dominant PFGE patterns. Salmonella is esti-
mated to be the most common cause of domestically acquired
bacterial foodborne illness in the United States [1], and SE is
the most common serotype causing salmonellosis; therefore,
addressing the reasons for the increase is important. Decreasing
Figure 1. Model-adjusted incidence of Salmonella serotype Enteritidis infection by year, Foodborne Diseases Active Surveillance Network (adjusted,
includes 95% confidence intervals) and Laboratory-based Enteric Diseases Surveillance (crude; excludes data from Arkansas, Colorado, District of
Columbia, Florida, Louisiana, Maine, Maryland, Montana, Nebraska, Tennessee, Texas, and Wyoming because of zero counts or incomplete data),
2000–2009 compared with mean of 1996–1999 baseline.
Rise in Salmonella Enteritidis Incidence dCID 2012:54 (Suppl 5) dS491
the number of SE infections will be necessary to meet the
Healthy People national objective of decreasing the incidence
of Salmonella infection by 25% by 2020 [7].
The rebound in incidence of SE infection is likely to have
been a result of several factors; one important risk factor is
eating chicken. In a FoodNet case-control study conducted
during 2002–2003, eating chicken outside the home ac-
counted for a higher percentage (36%) of domestically acquired
SE infection than any other exposure studied [20], including
eating undercooked eggs inside the home (31%). Per capita
broiler chicken consumptionintheUnitedStateshasin-
creased steadily from the early 1980s (approximately 32 pounds)
through the late 2000s (65–70 pounds) [21]. In our study, the
increase in the percentage of chicken rinsates contaminated
with SE mirrors increases in incidence of human infection,
providing ecological evidence of a possible relationship be-
tween chicken contamination with SE and human infection.
PFGE subtyping results also support this link. Although SE
isolates were taken from somewhat different periods, pat-
tern 4 represented approximately 40% of both human and
chicken isolates. In addition, patterns 4 and 5 were the 2 most
common patterns from human and chicken isolates. Because
SE isolates have few distinct PFGE patterns (the top 2 patterns
represented 80% of chicken and approximately 60% of human
isolates in these data), the pattern similarities do not provide
conclusive evidence of a connection but do indicate that
a connection is plausible.
FSIS has implemented several new measures to decrease
Salmonella contamination of broiler chickens. In 2006, FSIS
launched an initiative to reduce Salmonella contamination
Table 1. Number of Cases and Annual Crude Incidence per 100 000 Persons of Salmonella Serotype Enteritidis Infection, by
Demographic Characteristics and Site, Foodborne Diseases Active Surveillance Network, 2004–2009
Characteristic
Annual Crude Incidence, no./100 000
Mean Annual
Cases
Mean Annual
Incidence
Change in Incidence
a
2004–2009
2004 2005 2006 2007 2008 2009 No. (%) No./100 000 (%)
Overall (crude) 2.0 2.4 2.4 2.4 3.0 2.7 1130 100 2.5 34
By sex
Male 1.9 2.4 2.4 2.4 3.0 2.5 545 48 2.5 34
Female 2.0 2.4 2.5 2.3 3.0 2.8 582 52 2.4 34
By age group, years
,1 6.1 6.4 5.6 6.1 8.3 8.6 43 4 6.9 48
1–4 4.0 4.3 4.6 3.8 6.0 5.5 115 10 4.7 44
5–59 1.8 2.4 2.4 2.3 2.8 2.3 815 72 2.3 25
$60 1.6 1.7 1.9 1.8 2.5 2.7 154 14 2.0 75
By site
Connecticut 3.1 3.6 3.7 3.1 3.9 3.5 121 11 3.5 12
New York 1.5 2.1 2.0 2.7 2.7 2.6 97 9 2.3 69
Maryland 3.7 4.3 4.1 4.1 5.5 4.8 247 22 4.4 36
Georgia 1.2 1.6 1.5 1.9 2.7 2.7 182 16 1.9 140
Minnesota 2.2 2.5 3.1 2.7 3.2 2.3 138 12 2.7 12
Tennessee 1.1 1.7 1.7 1.5 1.9 1.8 98 9 1.6 45
Colorado 2.8 2.2 2.4 2.2 2.9 1.7 63 6 2.4 –20
New Mexico 0.8 0.8 1.4 1.0 1.8 1.4 24 2 1.2 87
Oregon 1.6 2.0 2.1 1.3 2.1 1.6 66 6 1.8 –8
California 2.4 3.8 2.9 2.8 2.2 3.1 94 8 2.9 –5
A total of 6777 cases of Salmonella serotype Enteritidis infection were reported.
a
Calculated from least squares best-fit line through plotted 2004–2009 incidence data.
Table 2. International Travel, Outbreak Association, and Outcomes
Among Persons With Salmonella Serotype Enteritidis Infection,
Foodborne Diseases Active Surveillance Network, 2004–2009
Characteristic
Annual Percentage of Cases
2004 2005 2006 2007 2008 2009 Mean, %
No international
travel
a
..74.9 76.7 84.9 88.4 81.2
Not outbreak
related
95.1 90.0 93.5 95.5 94.3 96.8 94.2
Hospitalized 25.5 25.4 29.5 24.4 26.8 28.9 26.7
Died 1.0 0.5 0.4 0.4 0.8 0.5 0.6
a
International travel: illness date of onset within 7 days of return to United
States or during travel.
S492 dCID 2012:54 (Suppl 5) dChai et al
of poultry products and other meats, focusing on testing
young chickens from establishments that had increasing per-
centages of contaminated samples [8,15]. In a 2007–2008 FSIS
baseline survey of young broilers that estimated product
volume–adjusted pathogen prevalence, 8.1% of all chicken
rinsates yielded Salmonella by PCR screening and culture;
0.4% of all rinsates yielded SE [22]. In May 2011, FSIS
published a tightened performance standard for broilers for
its Salmonella Verification Testing Program of 7.5% positivity
of collected chicken carcass rinsate sets for Salmonella at in-
dividual slaughter establishments [9].
Although multiple interventions to improve shell egg safety
likely contributed to the decrease in incidence of human SE
infection during the late 1990s [3], shell eggs continue to cause
illness. During 2006–2007, shell eggs accounted for 8 out-
breaks of SE infection, resulting in close to 300 illnesses [23,24].
The largest SE outbreak due to shell eggs, which caused an
estimated 1900 illnesses, occurred in 2010 [6]. Shell eggs are
not routinely tested; therefore, the prevalence of SE contami-
nation is not known. Models have estimated SE contamination
of US-produced shell eggs as 1 in 20 000, or 0.005% [25]. The
0.06% positivity of pasteurized egg product samples cannot
be directly compared with model-based estimates, because it
reflects the entire egg breaking, pooling, pasteurization, and
packaging process and facility sanitation and postprocessing
contamination. FSIS requires pasteurized egg products to be
tested and found negative for Salmonella before distribution
into commerce.
In July 2010, the FDA implemented the Egg Rule [26], which
requires that large producers of shell eggs implement specific
measures to prevent SE from contaminating eggs on the farm,
prevent SE growth during storage and transportation, maintain
records documenting compliance, and register with the FDA.
The FDA began conducting inspections of egg producers, in-
cluding environmental testing for SE and evaluation of SE pre-
vention plans, practices, and records. Shell eggs are tested if
environmental samples test positive for SE but are only di-
verted for pasteurization if egg tests yield SE. Before 2010,
shell eggs were not required to be tested for pathogens. Finding
SE in environmental samples, such as layer manure, is asso-
ciated with egg contamination [27], and US layer flocks have
a high prevalence of environmental SE (7%–10% of flocks)
[28]. SE-infected flocks only produce SE-infected eggs inter-
mittently, and challenges exist in detecting SE in eggs; with the
required shell egg sampling scheme, there is an approximately
95% probability that a positive egg will be detected from a flock
that is producing SE-contaminated eggs.
Both incidence of SE infection and relative increases in in-
cidence were highest among persons in the youngest and oldest
age groups by 2009. Although apparent differences in incidence
amongage groups might occur because of detection bias (ie, ill
persons at the extremes of age might be more likely to have
stool cultured), detection bias cannot explain the differences in
the relative increase over time among age groups [29]. Lower
infectious dose thresholds in these age groups might help
explain these differences. Uniform increases in exposure to
SE across all ages would increase likelihood of illness most
in persons with the lowest thresholds, which are more likely
in those at the extremes of age. Situations with uniformly
increased exposure to pathogens, such as large-scale municipal
Figure 2. Mean monthly incidence of Salmonella serotype Enteritidis infection and percentage of all reported Salmonella infections that were due
to serotype Enteritidis, Foodborne Diseases Active Surveillance Network, 2004–2009.
Rise in Salmonella Enteritidis Incidence dCID 2012:54 (Suppl 5) dS493
Table 3. Salmonella Serotype Enteritidis Testing Results From Broiler Chickens, Egg Products, and Humans, US Department of Agriculture/Food Safety and Inspection Service and
PulseNet, 2000–2009 [18,19]
Source/Type
Year
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 Total
Broiler chicken
rinsates
No. SE positive/
no. tested (%)
23/10 057 (0.2) 17/8955 (0.2) 33/9183 (0.4) 29/6468 (0.5) 58/7072 (0.8) 120/9592 (1.3) ....280/51 327 (0.5)
Top PFGE
patterns,
a
no. (%)
5 5 (22) 10 (63) 13 (42) 12 (43) . . .... 40 (41)
4 11 (48) 4 (25) 14 (45) 9 (32) . . .... 38 (39)
34 1 (4) 0 (0) 1 (3) 3 (11) . . .... 5 (5)
30 0 (0) 0 (0) 2 (6) 0 (0) . . .... 2 (2)
All others 6 (26) 2 (13) 1 (3) 4 (14) . . .... 13 (13)
Egg product
samples
No. SE positive/
no. tested (%)
0/1761 (0.00) 2/1656 (0.12) 0/1647 (0.00) 1/1560 (0.06) 1/1558 (0.06) 1/1610 (0.06) 2/1502 (0.13) 0/1421 (0.00) 1/1506 (0.07) 1/1441 (0.07) 9/15 661 (0.06)
Human isolates
Top PFGE
patterns,
no. (%)
4. ....1922 (38) 2071 (42) 2285 (43) 2731 (44) 3003 (47) 12 012 (43)
5. ....918 (18) 703 (14) 696 (13) 759 (12) 853 (13) 4238 (14)
2. ....579 (11) 847 (17) 861 (16) 658 (11) 530 (8) 3475 (12)
21 . ....601 (12) 262 (5) 282 (5) 460 (7) 504 (8) 2109 (8)
34 . ....123 (2) 181 (4) 261 (5) 321 (5) 284 (4) 1170 (4)
All others . ....934 (18) 905 (18) 969 (18) 1292 (21) 1176 (19) 5276 (19)
Abbreviations: PFGE, pulsed-field gel electrophoresis; SE, Salmonella serotype Enteritidis.
a
Pattern names provided are the equivalent PulseNet numerical designations (ie, JEGX01.0004 is pattern 4) of the matching VetNet patterns.
S494 dCID 2012:54 (Suppl 5) dChai et al
water contamination with Salmonella,haveresultedinthe
highest attack rates in the youngest age groups [30]. Exposure
to antibiotics, which can predispose to Salmonella infection
through suppression of normal gut flora and can be more
frequent in young individuals, might contribute to the dif-
ference in illness threshold [31]. In addition, the protective
acidity of the stomach against infection is lower in infants [32]
and, in older individuals, might be lowered through the in-
creased use of antacids [33].
Similar to a prior FoodNet report [5], we found substantial
regional differences in incidence of SE infection. Particularly
large relative increases in incidence occurred at sites in the
southern United States, and a northeastern state had the highest
mean annual incidence in FoodNet. Targeted studies of re-
gional factors, such as egg or chicken suppliers, state egg
quality assurance programs, and consumer and food handler
educational initiatives, might help clarify reasons for the re-
gional incidence variability. Regional differences also help to
explain why FoodNet reported lower SE incidence than LEDS
before 2002; FoodNet continued to add reporting counties
from states with a high SE incidence, such as Maryland and
Georgia, through 2001. Because 22% of states were excluded
from LEDS data because of limited reporting, 2 of which have
some of the largest populations in the United States and more
than half of which are in the southern United States, LEDS
incidence rates should be interpreted with caution and could
be underestimated. SE infections showed less seasonal vari-
ability by month than Salmonella infections as a group
(Figure 2), which suggests that exposures might not be as
seasonally variable as they are for other serotypes. Although
our data do not address the causes of this summer blunting,
they are consistent with the pattern expected if exposure
occurs primarily through foods consumed commonly through-
out the year, such as chicken and eggs.
Enteritidis is the most commonly reported serotype among
travel-associated nontyphoidal Salmonella infections in the
United States [34], and decreasing domestic sources of SE
will not affect the approximately 1 in 5 SE infections that are
acquired abroad. However, despite increases in international
travel for US residents during the 2000s, which peaked during
2006–2008 [35], the percentage of persons with SE infection
who reported no recent international travel increased con-
sistently during 2006–2009. In addition to the increasing
importance of domestically acquired SE infection, this implies
that the rates of increase of domestically acquired SE infection
are even higher than the overall numbers indicate. Although
imports of chilled or frozen chicken have increased exponen-
tially since the late 1990s, imports (including live chickens)
represent ,1% of all chicken estimated to be consumed in
the United States [36]. Imports of eggs have remained stable
at ,0.1% of all eggs estimated to be consumed in the United
States [21,36]. Together, these data indicate that the sources
of most SE infection are domestic and that the problem of
domestically acquired SE infection is increasing.
Antimicrobial resistance of human SE isolates is highest to
nalidixic acid and ampicillin. SE resistance to nalidixic acid in-
creased from 1.6% during 1996–1999 to 4.2% during 2000–2004
and 5.6% during 2005–2009, whereas resistance to ampicillin
decreased from 13.9% during 1996–1999 to 6.0% during
2000–2004 and 3.4% during 2005–2009 [37,38]. Nalidixic
acid resistance has been correlated with reduced susceptibility
to ciprofloxacin, a first-line antimicrobial agent often used to
treat severe Salmonella infection [38].
The rebound in incidence of domestically acquired SE in-
fection, particularly in the southern part of the United States,
is a growing problem that is disproportionately affecting the
youngest and oldest populations. Eggs and broiler chickens
are the main food sources of SE illness. Reviewing egg and
poultry outbreak data and continuing to develop methods to
attribute illnesses to foods can help clarify their relative con-
tributions to the burden of SE. The testing of shell eggs under
the 2010 FDA Final Egg Rule [26]isanimportantstepfor-
ward for SE control. It will also improve tracking of the
contribution of shell eggs to human SE illness. The success
of efforts by industry in collaboration with public health au-
thorities in Denmark and the United Kingdom, which have
included improved biosecurity, enhanced testing, and, in the
United Kingdom, poultry vaccination, shows that multifac-
eted, preharvest, flock-based approaches such as the FDA
Final Egg Rule can lead to substantial reductions in human
SE infection [39,40]. Ultimately, surveillance data on human
SE infection will reflect, in part, the impact of the FDA Final
Egg Rule. Because broiler chickens are a major food source of
human SE infection, similar multifaceted preharvest ap-
proaches might also be needed for chickens to supplement the
tighter processor-level standards now being implemented by
the FSIS.
Notes
Acknowledgments. We thank Olga L. Henao, Robert M. Hoekstra, and
Kelley B. Hise; the Minnesota Department of Health (Team Diarrhea); and
the New York State Emerging Infections Program (Glenda Smith, Nancy
Spina, Jillian Karr, Timothy Root, and Dianna Schoonmaker-Bopp).
Disclaimer. The contents of this work are solely the responsibility of
the authors and do not necessarily represent the official views of the
Centers for Disease Control and Prevention.
Financial support. This work was supported in part by the Centers for
Disease Control and Prevention (CDC; Cooperative Agreement U60/
CD303019). FoodNet is funded by the Food Safety Office and the Emerging
Infections Program of the Centers for Disease Control and Prevention, the
US Department of Agriculture Food Safety and Inspection Service, and the
Food and Drug Administration.
Supplement sponsorship. This article was published as part of a sup-
plement entitled ‘‘Studies From the Foodborne Diseases Active Surveil-
lance Network,’’ sponsored by the Division of Foodborne, Waterborne,
Rise in Salmonella Enteritidis Incidence dCID 2012:54 (Suppl 5) dS495
and Environmental Diseases of the National Center for Emerging and
Zoonotic Infectious Diseases from the Centers for Disease Control and
Prevention, and the Association of Public Health Laboratories.
Potential conflicts of interest. All authors: No reported conflicts.
All authors have submitted the ICMJE Form for Disclosure of Potential
Conflicts of Interest. Conflicts that the editors consider relevant to the
content of the manuscript have been disclosed.
References
1. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired
in the United States–major pathogens. Emerg Infect Dis 2011; 17:7–15.
2. Majowicz SE, Musto J, Scallan E, et al. The global burden of non-
typhoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50:882–9.
3. Braden CR. Salmonella enterica serotype Enteritidis and eggs: a na-
tional epidemic in the United States. Clin Infect Dis 2006; 43:512–7.
4. Patrick ME, Adcock PM, Gomez TM, et al. Salmonella enteritidis in-
fections, United States, 1985–1999. Emerg Infect Dis 2004; 10:1–7.
5. Marcus R, Rabatsky-Ehr T, Mohle-Boetani JC, et al. Dramatic decrease
in the incidence of Salmonella serotype Enteritidis infections in
5 FoodNet sites: 1996–1999. Clin Infect Dis 2004; 38(Suppl 3):S135–41.
6. Centers for Disease Control and Prevention. Investigation update:
multistate outbreak of human Salmonella enteritidis infections asso-
ciated with shell eggs. Available at: http://www.cdc.gov/salmonella/
enteritidis/. Accessed 15 December 2010.
7. Department of Health and Human Services. Healthy people 2020, 2020
topics & objectives, food safety. Available at: http://healthypeople.gov/
2020/topicsobjectives2020/overview.aspx?topicid514. Accessed 2 August
2011.
8. Department of Agriculture Food Safety and Inspection Service.
Salmonella verification sampling program: response to comments
and New Agency Policies. Fed Regist. 2008; 73:4767–74.
9. Department of Agriculture Food Safety and Inspection Service. New
performance standards for Salmonella and Campylobacter in young
chicken and Turkey slaughter establishments: response to comments
and announcement of implementation schedule. Fed Regist. 2011;
76:15282–90.
10. Department of Health and Human Services. HHS strategic plan FY
2010–2015 appendix B: HHS performance measures. Goal 3: advance
the health, safety and well-being of the American people. Objective E:
reduce the occurrence of infectious diseases. 3.E.1 Decrease the rate
of Salmonella Enteritidis (SE) illness in the population (cases per
100,000). Available at: http://www.hhs.gov/secretary/about/appendixb_
goal3.html. Accessed 2 August 2011.
11. Centers for Disease Control and Prevention. Vital signs: incidence and
trends of infection with pathogens transmitted commonly through
food–foodbornediseasesactivesurveillancenetwork,10U.S.sites,1996–
2010. MMWR Morb Mortal Wkly Rep 2011; 60:749–55.
12. Centers for Disease Control and Prevention. Foodborne Diseases
Active Surveillance Network (FoodNet): FoodNet surveillance re-
port for 2009 (final report). Atlanta, GA: U.S. Department of Health
and Human Services, Centers for Disease Control and Prevention,
2011.
13. Centers for Disease Control and Prevention. National Salmonella sur-
veillance overview. Atlanta, GA: US Department of Health and Human
Services, Centers for Disease Control and Prevention, 2011.
14. Gerner-Smidt P, Hise K, Kincaid J, et al. PulseNet USA: a five-year
update. Foodborne Pathog Dis 2006; 3:9–19.
15. Department of Agriculture Food Safety and Inspection Service.
Pathogen Reduction; Hazard Analysis and Critical Control Point
(HACCP) systems; final rule. Fed Regist. 2006; 71:38806–989.
16. Department of Agriculture Food Safety and Inspection Service. The FSIS
microbiological testing program for pasteurized egg products, 1995–
2009. Available at: http://www.fsis.usda.gov/Science/Sal_Pasteurized_
Egg_Products/index.asp. Accessed 14 December 2010.
17. Henao OL, Scallan E, Mahon B, Hoekstra RM. Methods for monitoring
trends in the incidence of foodborne diseases: foodborne Diseases
Active Surveillance Network 1996–2008. Foodborne Pathog Dis 2010;
7:1421–6.
18. Altekruse SF, Bauer N, Chanlongbutra A, et al. Salmonella enteritidis
in broiler chickens, United States, 2000–2005. Emerg Infect Dis 2006;
12:1848–52.
19. White PL, Naugle AL, Jackson CR, et al. Salmonella Enteritidis in meat,
poultry, and pasteurized egg products regulated by the U.S. Food Safety
and Inspection Service, 1998 through 2003. J Food Prot 2007; 70:582–91.
20. Marcus R, Varma JK, Medus C, et al. Re-assessment of risk factors
for sporadic Salmonella serotype Enteritidis infections: a case-control
study in five FoodNet Sites, 2002–2003. Epidemiol Infect 2007; 135:
84–92.
21. Department of Agriculture Economic Research Service. Livestock,
dairy, and poultry outlook: tables. Available at: http://www.ers.
usda.gov/publications/ldp/LDPTables.htm. Accessed 6 April 2011.
22. Department of Agriculture Food Safety and Inspection Service.
The nationwide microbiological baseline data collection program:
young chicken survey, July 2007–June 2008. Available at: http://
www.fsis.usda.gov/PDF/Baseline_Data_Young_Chicken_2007-2008.pdf.
Accessed 2 August 2011.
23. Centers for Disease Control and Prevention. Surveillance for foodborne
disease outbreaks—United States, 2006. MMWR Morb Mortal Wkly
Rep 2009; 58:609–15.
24. Centers for Disease Control and Prevention. Surveillance for foodborne
disease outbreaks—United States, 2007. MMWR Morb Mortal Wkly
Rep 2010; 59:973–9.
25. Ebel E, Schlosser W. Estimating the annual fraction of eggs contam-
inated with Salmonella enteritidis in the United States. Int J Food
Microbiol 2000; 61:51–62.
26. Department of Health and Human Services Food and Drug Admin-
istration. Prevention of Salmonella enteritidis in shell eggs during
production, storage, and transportation; final rule. Fed Regist. 2009;
74:33030–101.
27. Henzler DJ, Kradel DC, Sischo WM. Management and environmental
risk factors for Salmonella enteritidis contamination of eggs. Am J Vet
Res 1998; 59:824–9.
28. Kinde H, Castellan DM, Kass PH, et al. The occurrence and distri-
bution of Salmonella enteritidis and other serovars on California egg
laying premises: a comparison of two sampling methods and two
culturing techniques. Avian Dis 2004; 48:590–4.
29. Lynch MF, Tauxe RV. Salmonellosis: nontyphoidal. In: Evans AS,
Brachman PS, eds. Bacterial infections of humans. New York: Springer
Science1Business Media, 2009.
30. A waterborne epidemic of salmonellosis in Riverside, California, 1965.
Epidemiologic aspects. A collaborative report. Am J Epidemiol 1971;
93:33–48.
31. Black PH, Kunz LJ, Swartz MN. Salmonellosis–a review of some un-
usual aspects. N Engl J Med 1960; 262:864–70.
32. Alcorn J, McNamara PJ. Pharmacokinetics in the newborn. Adv Drug
Deliv Rev 2003; 55:667–86.
33. Radimer K, Bindewald B, Hughes J, Ervin B, Swanson C, Picciano MF.
Dietary supplement use by US adults: data from the National Health
and Nutrition Examination Survey, 1999–2000. Am J Epidemiol 2004;
160:339–49.
34. Kendall ME, Crim S, Fullerton K, et al. Travel-associated enteric
infections diagnosed after return to the United States, Foodborne
Diseases Active Surveillance Network (FoodNet), 2004–2009. Clin
Infect Dis 2012; 54(Suppl 5):S480–7.
35. Department of Commerce International Trade Administration.
2009 United States resident travel abroad. Washington, DC: US De-
partment of Commerce, ITA, 2009.
36. Department of Agriculture Foreign Agricultural Service. Global ag-
ricultural trade system online. Available at: http://www.fas.usda.gov/
gats/default.aspx. Accessed 6 April 2011.
37. Hariri S, McKenna MT. Epidemiology of human immunodeficiency
virus in the United States. Clin Microbiol Rev 2007; 20:478–88.
S496 dCID 2012:54 (Suppl 5) dChai et al
38. Centers for Disease Control and Prevention. National Antimicrobial
Resistance Monitoring System for Enteric Bacteria (NARMS):
human isolates final report, 2009. Atlanta, GA: U.S. Department
of Health and Human Services, Centers for Disease Control and
Prevention, 2010.
39. Cogan TA, Humphrey TJ. The rise and fall of Salmonella Enteritidis
in the UK. J Appl Microbiol 2003; 94(Suppl):114S–9.
40. Korsgaard H, Madsen M, Feld NC, Mygind J, Hald T. The effects,
costs and benefits of Salmonella control in the Danish table-egg
sector. Epidemiol Infect 2009; 137:828–36.
Rise in Salmonella Enteritidis Incidence dCID 2012:54 (Suppl 5) dS497
