Poultry: the most common food in outbreaks with known
pathogens, United States, 1998–2012
S. J. CHAI, D. COLE, A. NISLER AND B. E. MAHON*
Enteric Diseases Epidemiology Branch; Division of Foodborne, Waterborne, and Environmental Diseases;
Centers for Disease Control and Prevention, Atlanta, GA, USA
Received 14 May 2016; Final revision 19 September 2016; Accepted 19 September 2016;
first published online 26 October 2016
SUMMARY
As poultry consumption continues to increase worldwide, and as the United States accounts
for about one-third of all poultry exports globally, understanding factors leading to poultry-
associated foodborne outbreaks in the United States has important implications for food safety.
We analysed outbreaks reported to the United States’ Foodborne Disease Outbreak Surveillance
System from 1998 to 2012 in which the implicated food or ingredient could be assigned to one
food category. Of 1114 outbreaks, poultry was associated with 279 (25%), accounting for the
highest number of outbreaks, illnesses, and hospitalizations, and the second highest number of
deaths. Of the 149 poultry-associated outbreaks caused by a confirmed pathogen, Salmonella
enterica (43%) and Clostridium perfringe ns (26%) were the most common pathogens. Restaurants
were the most commonly reported location of food preparation (37% of poultry-associated
outbreaks), followed by private homes (25%), and catering facilities (13%). The most commonly
reported factors contributing to poultry-associated outbreaks were food-handling errors (64%)
and inadequate cooking (53%). Effective measures to reduce poultry contamination, promote
safe food-handling practices, and ensure food handlers do not work while ill could reduce
poultry-associated outbreaks and illnesses.
Key words: Foodborne infections, food safety, outbreaks.
INTRODUCTION
Poultry is the second-most commonly consumed meat
worldwide, and consumption of poultry is projected to
increase more quickly than any other major meat [1].
The United States is one of the top two poultry suppli-
ers worldwide, accounting for about one-third of all
poultry exports during 2011–2014. Similar to world-
wide trends, poultry is an important and increasing
part of the US diet. Per capita consumption doubled
during 1970–2007, and poultry accounted for almost
a quarter of meat consumed in the United States in
2007 [2]. Therefore, understanding the contribution
of poultry to foodborne outbreaks in the United
States is important not only for the United States
but also globally. Foodborne outbreak investigations
provide the most readily available information about
the sources and circumstances of food contamination
leading to illness.
In the United States, consumption of food contami-
nated with known pathogens causes an estimated 9·4
million illnesses every year [3]. Poultry is an important
source of these foodborne infections [4–7]. Poultry
* Author for correspondence: Dr B. E. Mahon, Centers for Disease
Control and Prevention, 1600 Clifton Road, MS C-09, Atlanta, GA
30333, USA.
(Email: bdm3@cdc.gov)
Epidemiol. Infect. (2017), 145, 316–325. © Cambridge University Press 2016
doi:10.1017/S0950268816002375
https://doi.org/10.1017/S0950268816002375 Published online by Cambridge University Press
products are contaminated frequently with som e of
the most common bacterial pathogens associated
with foodborne illness [8]. In 2011, cultures of 13%
of chicken samples and 6% of ground turkey samples
yielded Salmonella, and 38% of chicken samples
yielded Campylobacter [8].
Large multistate outbreaks associated with poultry
have focused industry, regulatory, and consumer at-
tention on the safety of poultry products. For ex-
ample, in 2013–2014, a 29-state outbreak of
multidrug-resistant Salmonella enterica serotype
Heidelberg infections associated with chicken caused
634 illnesses and 241 hospitalizations [9]. We con-
ducted a detailed analysis of the pathogens, settings,
contamination factors, and poultry types leading to
poultry-associated foodborne outbreaks in the
United States to guide interventions to decrease ill-
nesses associated with poultry consumption.
METHODS
Data source
The Foodborne Disease Outbreak Surveillance
System (FDOSS) collects reports of foodborne disease
outbreaks from state, local, and territorial public
health agencies in the United States. The Centers for
Disease Control and Prevention (CDC) runs
FDOSS, and defines a foodborne disease outbreak
as the occurrence of two or more similar illnesses
resulting from ingestion of the same food. Reported
data include the number of illnesses, hospitalizations,
and deaths; the pathogen; the implicated food(s); and
the settings of food preparation and consumption.
FDOSS also collects information regarding certain
contributing factors (e.g. food not adequately cooked
or not kept at the right temperature before consump-
tion) [10]. Demographic data are reported as percen-
tages of ill persons in defined age and gender
categories. Pathogens are reported as confirmed if
specific diagnostic criteria were met [11]. During the
period of this study, 1998–2012, FDOSS classified
foods into 17 categories (fish, crustaceans, molluscs,
dairy, eggs, beef, game, pork, poultry, grains-beans,
oils-sugars, fruits-nuts, fungi, leafy, root, sprout, and
vine-stalk) [12].
Analysis
We included outbreaks satisfying the following cri-
teria: (1) the outbreak occurred from 1998 to 2012,
(2) the investigation implicated a food using either
statistical or laboratory evidence, (3) the food con-
tained a single contaminated ingredient or multiple
contaminated ingredients belonging to a single food
category, and (4) a suspected or confi rmed pathogen
was reported. We conducte d three analyses. First, we
examined all outbreaks with a confirmed or suspected
pathogen in which inv estiga tors implica ted poultry
and contrasted the number of illnesses, hospitalizations,
and deaths with outbreaks caused by other food
categories. Second, we examined poultry-associa ted
outbreaks with a confirmed pathogen by pathogen.
Third, we compared poultry-associated outbreaks with
aconfirmed pathogen by type of poultry implicated.
For outbreaks with demographic information reported,
we estima ted the number of ill persons in defined age
and sex categories by multiplying the reported percent-
age in the category by the reported number of ill per-
sons in the outbreak.
Reports could contain one or more contributing
factors for each outbreak. We classified these factors
into broad categories, including food-handling errors,
inadequate cooking, contamination before food prep-
aration, contaminated equipment, and poor personal
hygiene of a food handle r (Supplementary Table S1).
For statistical analysis, we assumed that the out-
breaks included in our analysis represented a random
sample of foodborne outbreaks occurring in the
United States during the study period. We evaluated
categorical variables using frequencies and using a χ
2
test (Fisher’s exact test for comparisons with cell
counts <5) for comparisons. We used one-way
fixed-effects analysis of variance to compare means
of counts of illnesses between poultry and non-poultry
outbreaks and between chicken and turkey outbreaks.
We used the Wilcoxon rank sum test to compare dis-
tributions of percentages of demographic characteris-
tic variables that were not normally distributed. We
used a cut-off of α = 0·05 to indicate statistical signifi-
cance and conducted analyses using SAS v. 9.3 (SAS
Institute, USA).
RESULTS
All outbreaks with a confirmed or suspected pathogen
During 1998–2012, FDOSS received 1114 reports of
foodborne disease outbreaks that met the inclusion
criteria. Poultry was the most frequently reported
food category (279 outbreaks, 25%), followed by fish
(181, 16%) and beef (135, 12%). The 279 outbreaks
Poultry-linked US foodborne outbreaks 317
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associated with poultry accounted for more illnesses
(9760 of 35622, 27%) and hospitalizations (565 of
2640, 21%) than outbreaks caused by any other food
category; poultry accounted for the second greatest
number of deaths (22 of 86, 26%). In the poultry-
associated outbreaks, the mean number of reported
illnesses was 35 [95% confidence interval (CI)
25–45], which was not significantly larger than those
associated with foods in the other categories (mean
31, 95% CI 25–36) (P = 0·47). Overall, the distribu-
tions of age group and sex of patients were similar
(all P50·05) in poultry-associated outbreaks and
those associated with other food categories.
Poultry-associated outbreaks with a confirmed
pathogen
Among the 279 poultry-associat ed outbreaks, 149
(53%) had a confirmed pathogen and are the focus of
the remainder of the analysis. Salmonella caused the
largest number of outbr eaks (64, 43%), followed by
C. perfringens (39, 26%) (Table 1). Other causes wer e
Campylobacter spp. (10, 7%), norovirus (10, 7%),
Staphylococcus aureus enterotoxin (8, 5%), Listeria
monocytogenes (5, 3%), Bacillus cereus (4,3%),and
other agents (9, 6%). Four serotypes [Enteritidis, 11 out-
breaks (17%); Heidelberg, 11 (17%); Typhimurium, 10
(16%); Newport, 6 (9%)] caused more than half of the
Salmonella outbreaks. Salmonella outbreaks resulted
in the most illnesses (2614, 50%) and the most hospita-
lizations (425, 80%) (Table 2).
A single known location of food preparation was
reported for 125 (84%) of these outbreaks. Most
were restaurants (46, 37%), followed by private
homes (31, 25%) and catering facilities (16, 13%). In
restaurant-associated outbreaks, Salmonella (35%),
C. perfringens (26%), Campylobacter (11%), and nor-
ovirus (11%) were the most common aetiologies. In
outbreaks in which food was prepared in a private
home, Salmonella caused 65% of outbreaks, and C.
perfringens caused 26%. C. perfringens caused most
of the caterer-associated outbreaks (56%).
Information on one or more factors contributing to
the outbreak was reported in 120 (81%) outbreaks. In
these outbreaks, the most commonly reported contribut-
ing factors wer e food-handling err ors (64%) and inad-
equate cooking (53%). Among outbreaks caused by
Salmonella, inadequate cooking (63%) and contamin-
ation of the uncooked poultry before food prepara tion
(63%) were the mos t commonly reported contributing
factors, followed by food-handling errors (50%). In
100% of outbreaks of norovirus infection, investiga tors
reported poor personal hygiene of a food handler as a
contributing factor. In outbreaks caused by C. perfrin-
gens, B. cereus,andS. aureus enterotoxin, food-handling
errors were the most common contributing factor.
Table 1. Reported foodborne disease outbreaks with a confirmed pathogen associated with poultry and with foods
other than poultry*, by pathogen, United States, 1998–2012
Poultry, n (%)
Foods other
than poultry,
n (%)
Pathogen Chicken Turkey Other poultry Total Total
Salmonella enterica† 39 (41) 25 (48) 0 (0) 64 (43) 160 (40)
Clostridium perfringens 23 (24) 16 (31) 0 (0) 39 (26) 67 (17)
Campylobacter spp. 7 (7) 2 (4) 1 (33) 10 (7) 37 (9)
Norovirus 6 (6) 3 (6) 1 (33) 10 (7) 56 (14)
Staphylococcus aureus 7 (7) 1 (2) 0 (0) 8 (5) 43 (11)
Listeria monocytogenes 1 (1) 4 (8) 0 (0) 5 (3) 10 (3)
Bacillus cereus 4 (4) 0 (0) 0 (0) 4 (3) 17 (4)
Other‡ 7 (7) 1 (2) 1 (33) 9 (6) 8 (2)
Total reports identifying a pathogen 94 (100) 52 (100) 3 (100) 149 (100) 398 (100)
* Either a single contaminated ingredient was identified or all ingredients in the implicated food belonged to a single food
category
† Includes serotypes Berta (1 turkey outbreak), Braenderup (1 chicken outbreak), Enteritidis (9 chicken, 2 turkey), Hadar
(3 turkey), Heidelberg (7 chicken, 4 turkey), Javiana (1 chicken), Montevideo (1 chicken), Muenchen (1 chicken), Newport
(3 chicken, 3 turkey), Thompson (1 chicken), Typhimurium (5 chicken, 5 turkey), and unspecified (10 chicken, 7 turkey)
‡ Includes: chemicals, Clostridium botulinum, Cyclospora cayetanensis, Escherichia coli, heavy metals, multiple, other bacter-
ial, other parasites, sapovirus, Shigella sonnei, Streptococcus group A, toxins, Trichinella spiralis, Vibrio spp., and Yersinia
enterocolitica.
318 S. J. Chai and others
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The 13 outbreaks that involved >100 ill persons
(range 101–312) accounted for 42% (2200) of all ill-
nesses in poultry-associated outbreaks. Salmonella
caused seven (54%) and C. perfringens caused six
(46%). Three of these large outbreaks, including the lar-
gest (312 illnesses), occurred in prisons for men; five
were restaurant-associated.
Outbreaks by poultry type
Reports implicated duck in one outbreak and poultry
of an unspeci fied type in two outbreaks; we excluded
these three outbreaks from further analyses by poultry
type. In the remaining 146 (98%) poultry-associated
outbreaks, investigators implicated chicken in 94 out-
breaks (64%) and turkey in 52 (36%) (Table 1).
Although the mean number of illnesses appeared
greater in turkey-associated outbreaks than in
chicken-associated outbreaks, this finding was not stat-
istically significant (45 vs. 31, P = 0·12). Of the largest
outbreaks (>100 ill persons), turkey was implicated in
seven (54%) and chicken in six (46%). List eria caused
a gr ea ter percentage of turkey-associated than
chicken-associated outbreaks, although this difference
was not statistically significant (8% vs. 1%, P =0·05);
delicatessen meat was the source of all turkey-associa ted
Listeria outbreaks.
Of the 77 chicken-associated outbreaks with a sin-
gle reported known location of food preparation,
45% (35 of 77) were associated with food prepared
in a restaurant, much greater than the 20% (9 of 45)
of turkey-associated outbreaks that were associated
with a restaurant (P = 0·006).
Of the 52 turkey-associated outbreaks, 22 (42%) oc-
curred during November and December (Fig. 1).
Chicken-associated outbreaks had a small seasonal
peak during the 3-month span from April to June
[39 (41%) out of 94 reported] (Fig. 2). Although the
distribution of pathogens in turkey-associated out-
breaks was generally similar across months, C. perfrin-
gens caused 55% of turkey-associated outbreaks that
occurred during November and December but only
13% during the other months (P = 0·002). Improper
food handling was a contributing factor more fre-
quently during November and December than during
the other months for both turkey-associated outbreaks
(85% vs. 45%, P = 0·01) and chicken-associated out-
breaks (100% vs. 58%, P = 0·006).
In all, 20 deaths were reported in seven outbreaks
with a confirmed pathogen and known poultry type.
Salmonella caused four outbreaks with one death
each (two turkey-associated, two chicken-associated).
Listeria caused three outbreaks with 16 deaths – 80%
of all reported deaths – and all were linked to turkey
delicatessen meat. The last death in the study period
in a Listeria outbreak associated with turkey delicates-
sen meat was in 2005.
DISCUSSION
This report highlights the role of poultry as a major
source of foodborne outbreaks in the United States.
Table 2. Illnesses, hospitalizations, and deaths in reported poultry-associated* foodborne disease outbreaks with a
confirmed pathogen, United States, 1998–2012
Pathogen
Illnesses
n (% of total)
Hospitalizations
n (% of total )
Deaths
n (% of total)
Salmonella enterica 2614 (50) 425 (80) 4 (20)
Clostridium perfringens 1764 (33) 8 (2) 0 (0)
Norovirus 191 (4) 0 (0) 0 (0)
Staphylococcus aureus 133 (3) 19 (4) 0 (0)
Listeria monocytogenes 127 (2) 45 (8) 16 (80)
Bacillus cereus 31 (1) 1 (0) 0 (0)
Campylobacter spp. 81 (2) 5 (1) 0 (0)
Other† 325 (6) 28 (5) 0 (0)
Total 5266 (100) 531 (100) 20 (100)
* Either poultry was identified as the contaminated food or ingredient or all ingredients in the implicated food belonged to the
poultry category.
† Includes: Shiga toxin-producing Escherichia coli O157, Shigella sonnei, Vibrio parahaemolyticus, multiple pathogens, and
other bacterial pathogens
Poultry-linked US foodborne outbreaks 319
https://doi.org/10.1017/S0950268816002375 Published online by Cambridge University Press
With poultry consumption increasing globally, this
finding has implications for food safety both within
and beyond the United States. From 1998 to 2012,
poultry accounted for more reports of foodborne dis-
ease outbreaks than any other single food category.
Poultry-associated outbreaks accounted for the great-
est number of illnesses and hospitalizations and over a
quarter of the deaths in outbreaks associated with a
single food category. Our analysis of the pathogens,
contributing factors, settings, and poultry types asso-
ciated with foodborne disease outbreaks suggests
that breakdowns in food safety at multiple points
along the farm-to-fork continuum commonly lead to
these outbreaks.
Contamination before food preparation and in-
adequate cooking were two of the most common
contributing factors associated with Salmonella out-
breaks. Salmonella is a common contaminant of
poultry [5]. In whole chicken carcass testing conducted
from 1998 to 2014, cultures of about 4–16% of carcass
rinses in production plants yielded Salmonella [13].
Testing data suggest that contamination of whole
Fig. 1. Number of foodborne disease outbreaks with confirmed pathogen associated with turkey, by pathogen and month,
United States, 1998–2012. (a) Non-toxin-producing pathogens; (b) toxin-producing pathogens.
320 S. J. Chai and others
https://doi.org/10.1017/S0950268816002375 Published online by Cambridge University Press