In The United States, 2003-2012: Escherichia Coli O157 Outbreaks
In The United States, 2003-2012: Escherichia Coli O157 Outbreaks
In The United States, 2003-2012: Escherichia Coli O157 Outbreaks
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Learning Objectives
Upon completion of this activity, participants will be able to:
Identify the most common source of outbreaks of Escherichia coli O157 in the United States
Identify the most common specific food source associated with foodborne outbreaks of E. coli O157 in
the United States
Evaluate epidemiologic variables associated with the severity of E. coli O157 outbreaks
Assess other epidemiologic data from outbreaks of E. coli O157 in the United States
CME Editor
Jean Michaels Jones, BSN, Technical Writer/Editor, Emerging Infectious Diseases. Disclosure: Jean Michaels
Jones, BSN, has disclosed no relevant financial relationships.
CME Author
Charles P. Vega, MD, Clinical Professor of Family Medicine, University of California, Irvine. Disclosure:
Charles P. Vega, MD, has disclosed the following financial relationships: served as an advisor or consultant for
McNeil Pharmaceuticals.
Authors
Disclosures: Katherine E. Heiman, MPH; Rajal K. Mody, MD, MPH; Shacara D. Johnson, MSPH; Patricia M.
Griffin, MD; and L. Hannah Gould, PhD, MS, MBA, have disclosed no relevant financial relationships.
Infections with the Shiga toxinproducing bacterium Esch- 1,272 hospitalizations, and 33 deaths. Transmission was
erichia coli O157 can cause severe illness and death. We through food (255 outbreaks, 65%), person-to-person con-
summarized reported outbreaks of E. coli O157 infections tact (39, 10%), indirect or direct contact with animals (39,
in the United States during 20032012, including demo- 10%), and water (15, 4%); 42 (11%) had a different or un-
graphic characteristics of patients and epidemiologic known mode of transmission. Beef and leafy vegetables,
findings by transmission mode and food category. We combined, were the source of >25% of all reported E. coli
identified 390 outbreaks, which included 4,928 illnesses, outbreaks and of >40% of related illnesses. Outbreaks at-
tributed to foods generally consumed raw caused higher
Author affiliation: Centers for Disease Control and Prevention, hospitalization rates than those attributed to foods gener-
Atlanta, Georgia, USA ally consumed cooked (35% vs. 28%). Most (87%) water-
borne E. coli outbreaks occurred in states bordering the
DOI: http://dx.doi.org/10.3201/eid2108.141364
Mississippi River.
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SYNOPSIS
1294 Emerging Infectious Diseases www.cdc.gov/eid Vol. 21, No. 8, August 2015
E. coli O157, United States, 20032012
Table 1. Characteristics of Escherichia coli O157 outbreaks by transmission mode and food category, United States, 20032012*
Outbreaks (% of Illnesses (median Hospitalizations Physician-diagnosed HUS Deaths (% of
Transmission source all outbreaks) outbreak size) (% of all illnesses) (% of all illnesses) all illnesses)
Food 255 (65) 3,667 (6) 1,035 (29) 209 (6) 25 (0.7)
Beef 78 (20) 1,144 (7) 316 (28) 67 (6) 5 (0.4)
Poultry 1 (0) 60 5 (8) 0 0
Other meat 7 (2) 39 (4) 12 (31) 4 (10) 0
Dairy 16 (4) 140 (6) 52 (37) 22 (16) 0
Leafy vegetables 29 (7) 922 (16) 321 (35) 53 (6) 7 (0.8)
Fruits 6 (2) 57 (8) 20 (35) 5 (9) 6 (10.5)
Sprouts 3 (1) 35 (13) 4 (11) 0 0
Nuts 1 (0) 8 3 (38) 0 0
Other foods 29 (7) 580 (11) 123 (21) 24 (4) 0
Food unknown 85 (22) 682 (5) 179 (26) 32 (5) 10 (1.5)
Animal contact 39 (10) 552 (6) 127 (23) 51 (9) 2 (0.4)
Person-to-person 39 (10) 322 (5) 45 (14) 24 (7) 2 (0.6)
Water 15 (4) 154 (6) NA NA 1 (0.6)
Other or unknown 42 (10) 233 (4) 65 (28) 15 (6) 3 (1.3)
Total 390 (100) 4,928 (6) 1,272 (27) 299 (6) 33 (0.7)
*HUS, hemolytic uremic syndrome; NA, not available.
Poultry was thought to be cross-contaminated by ground beef (http://www.ct.gov/dph/lib/dph/infectious_diseases/ctepinews/vol29no5.pdf).
Outbreaks transmitted from other foods were 2 each of: guacamole, pico de gallo, salsa, and potato salad; and 1 each of: cookie dough; alfalfa sprouts
and iceberg lettuce; baked beans and unknown fruit; meatballs, steak and green salad; cantaloupe and hamburger; lamb and beef; lettuce and green
grapes; lime and bean dip; macaroni; Mexican wheat snack; sandwich; seafood; vegetable-based salad; pepperoni; jerky; multiple foods. Agencies
sometimes report >1 food vehicle when epidemiologic evidence cannot distinguish between them even when it is likely that only one was the source.
Excludes 154 illnesses from the denominator that were associated with waterborne disease outbreaks because no data was collected for hospitalization
and physician-diagnosed HUS cases for this transmission mode.
(15, 4%), and other or unknown (42, 11%). Foodborne dis- Vehicles
ease outbreaks caused the most illnesses (3,667, 74%), hos- Of the 255 foodborne disease outbreak reports, 170 (67%)
pitalizations (1,035, 81%), physician-diagnosed HUS cas- implicated a specific food, of which 141 (83%) could be
es (209, 70%), and deaths (25, 70%). During 20092012, classified into a single category. The implicated categories
when data for culture-confirmed infections were collected were beef (78 outbreaks, 55%), leafy vegetables (29, 21%),
for all outbreaks, the proportions of transmission were un- dairy (16, 11%), fruits (6, 4%), other meats (7, 5%), sprouts
known modes (76%), foodborne (69%), person-to-person (3, 2%), nuts (1, 1%), and poultry (1, 1%) (Table 1). The
(62%), and animal contact (40%). types of beef implicated were ground beef (54 outbreaks,
The median annual number of outbreaks reported 69% of beef-associated outbreaks) and steak (10, 14%).
during 20082012 was lower than during 20032007 (45 The types of steak, reported in 5 outbreaks, were sirloin
vs. 33, p = 0.12) (Figure 1). The median annual number (4 outbreaks) and filet mignon (1). Steaks were mechani-
of foodborne disease outbreaks did not change, although cally tenderized in 5 outbreaks (2 sirloin, 1 filet mignon,
the number attributed to dairy (11 vs. 5) and fruits (5 vs. 2 unknown). Other implicated meats were venison (3 out-
2) more than doubled. The median annual number of breaks), lamb (2), and bison/buffalo (2).
outbreaks attributed to other modes of transmission did In all 16 outbreaks attributed to dairy, unpasteurized
not change. products were implicated; 13 (81%) to unpasteurized milk
Figure 1. Number of
Escherichia coli O157
outbreaks by transmission
mode and year (n = 390),
United States, 20032012.
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SYNOPSIS
and 3 (9%) to cheese made from unpasteurized milk. foods generally consumed raw than for cooked foods (35%
Most outbreaks attributed to leafy vegetables implicated vs. 28%, p = 0.0001). Deaths occurred most commonly in
lettuce (22 outbreaks, 76%), including romaine (3), ice- outbreaks attributed to leafy vegetables (7 deaths, 0.8% of
berg (1), and mesclun mix (1); others in this category illnesses in leafy vegetable outbreaks), fruits (6, 11%), and
were spinach (4, 13%) and salads with unspecified types beef (5, 0.4%).
of greens (3,10%). Outbreaks attributed to fruit impli-
cated unpasteurized apple cider (4 outbreaks), fruit salad Demographic Characteristics
(1), and strawberries (1), a newly identified food vehicle Age group distribution of cases varied by transmission
for this pathogen. Other newly identified food vehicles mode and food category (Figure 2). Patient age group
were hazelnuts sold in the shell (1 outbreak), packaged was available for 2,884 (81%) illnesses in foodborne out-
cookie dough (1), salsa (2), and pico de gallo (2). A to- breaks, 63 (90%) illnesses in waterborne outbreaks, and,
tal of 39 outbreaks were transmitted by contact with ani- during 20092012, 121 (96%) illnesses in person-to-person
mals; >1 animal type was reported for 24 (62%), includ- outbreaks and 189 (73%) illnesses in animal contact out-
ing cattle (15), goats (12), sheep (8), pigs (3), rabbits (3), breaks. Most of the illnesses in person-to-person outbreaks
chickens (2), and 1 each of elk, llama, alpaca, hedgehog, (73, 60%) were among children <5 years old. The highest
and dog. Every outbreak that identified a reported animal proportions of illnesses in waterborne and animal contact
type included >1 ruminant animal. Although no specific outbreaks (67% and 43%, respectively) were among per-
animal types were listed for the remaining 14 outbreaks, sons 519 years of age. Foodborne disease occurred among
livestock were reported for 2 and petting zoos or county persons in all age groups; only 8% of foodborne illnesses
fairs for 11. occurred among children <5 years of age, but >25% of
Of the 15 waterborne disease outbreaks, 10 were at- dairy-associated illnesses were among children of this age
tributed to recreational water (3 treated, 7 untreated), 3 to group. The largest proportions of illnesses in outbreaks at-
drinking water, and 1 possibly to wastewater. The water tributed to beef and dairy were among persons 519 years
source was unknown for the remaining outbreak. old (38% and 47%, respectively), whereas the largest pro-
portion reported in outbreaks attributed to sprouts and leafy
Severity vegetables was among persons 2049 years old (71% and
The severity of outbreaks differed by transmission mode 45%, respectively).
and among foodborne disease outbreaks by food category Overall, 55% of patients were women; the percent-
(Table 1). Hospitalization rates were lower for person-to- age did not vary significantly by transmission mode. Pa-
person outbreaks compared with all other transmission tient sex was available for 3,385 (92%) illnesses in food-
modes (14% vs. 28%, p<0.0001). Physician-diagnosed borne disease outbreaks, 63 (90%) illnesses in waterborne
HUS rates were higher for animal contact outbreaks than outbreaks, and, from 20092012, 126 (97%) illnesses
for all other modes (9% vs. 6%, p = 0.0005). The 33 deaths in person-to-person outbreaks and 193 (80%) illnesses
occurred in foodborne (25 deaths), person-to-person (2), in animal contact outbreaks. In foodborne disease out-
animal contact (2), and waterborne (1) disease outbreaks; breaks, the proportion of female patients was highest in
transmission mode was unknown for 3 deaths. outbreaks attributed to fruits (67%) and leafy vegetables
Among foodborne disease outbreaks, hospitalization (65%) and lowest in outbreaks attributed to meats other
rates were lower for outbreaks attributed to beef than for than beef (31%) (p<0.0001); cases were evenly distrib-
all other food vehicles (28% vs. 35%, p<0.001). Hospi- uted among women and men in outbreaks attributed to
talization rates were higher among outbreaks attributed to beef and dairy.
Figure 2. Percentage of Escherichia coli O157 outbreak illnesses by age group and A) transmission mode (n = 3,417) and B) selected
food categories (n = 1,574), United States, 20032012.
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E. coli O157, United States, 20032012
Figure 3. Number of Escherichia coli O157 outbreaks by month and by A) transmission mode (n = 390) and B) selected food categories
(n = 255), United States, 20032012.
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SYNOPSIS
Figure 4. Single-state Escherichia coli O157 outbreaks (n = 346) by state and transmission mode, United States, 20032012.
A) Foodborne transmission (n = 211); B) animal contact transmission (n = 39); C) person-to-person transmission (n = 39);
D) waterborne transmission (n = 15). Curved line denotes 37N latitude.
and systematic, electronic reporting of outbreaks of all virulence factors. Outbreaks attributed to foods generally
transmission modes (4). consumed raw had higher hospitalization rates than those
Beef, particularly ground beef, continues to be the ma- attributed to cooked foods. Outbreaks with high propor-
jor source of E. coli O157 outbreaks, likely because cattle tions of illnesses among young children, especially those
are the main reservoir for E. coli O157. Contamination of attributed to animal contact, dairy products, other meats,
raw beef usually occurs during slaughter and meat process- and fruits, also had the highest rates of physician-diag-
ing by contact with hides contaminated with feces (11,12). nosed HUS, which might relate to the higher risk for HUS
Grinding can spread contamination through vast amounts among children (18). However, this finding was not true for
of ground beef (11). Mechanically tenderizing steaks inter- person-to-person outbreaks, in which the proportion of ill-
nalizes surface contamination (13,14), so steaks not cooked nesses among young children was highest. The reasons for
thoroughly could harbor E. coli O157. The risk for con- this finding are unknown, but intensive case finding efforts
tamination varies for different locations on the carcass (15). during suspected person-to-person outbreak investigations
Cattle carcasses sampled for microbial contamination had might identify more mild illnesses and asymptomatic pa-
higher bacteria counts on sites on the rear (16,17). tients, decreasing the overall hospitalization rate.
Our finding that outbreaks attributed to leafy veg- Higher hospitalization rates in outbreaks attributed to
etables, dairy products, fruits, and other meats were more certain foods might be influenced by patient sex. For ex-
severe than outbreaks attributed to beef could have several ample, hospitalization rates were 35% for outbreaks asso-
explanations, including strain virulence and patient age and ciated with leafy vegetables, and 66% of illnesses were in
sex. Outbreak reports did not provide information on strain female patients. Studies have found that women were at
1298 Emerging Infectious Diseases www.cdc.gov/eid Vol. 21, No. 8, August 2015
E. coli O157, United States, 20032012
Table 2. Escherichia coli O157 outbreaks by setting (n = 357), United States, 20032012
Setting/no. outbreaks
Restaurant/ Fair/petting Recreational
Transmission source banquet facility Home Institutional* zoo area/facility Other Unknown Total
Food 73 60 16 2 0 32 39 222
Beef 15 34 3 0 0 9 8 69
Poultry 0 0 1 0 0 0 0 1
Other meat 1 5 0 0 0 0 0 6
Dairy 0 2 0 0 0 11 0 13
Leafy vegetables 13 4 3 0 0 2 4 26
Fruits 0 2 0 1 0 2 0 5
Sprouts 1 0 0 0 0 0 0 1
Nuts 0 1 0 0 0 0 0 1
Other foods 13 6 0 0 0 2 3 24
Food unknown 30 6 9 1 0 6 24 76
Animal contact 0 1 2 17 0 4 15 39
Person-to-person 0 2 17 0 0 0 20 39
Water 0 2 2 0 7 4 0 15
Other or unknown 0 0 0 0 0 0 42 42
All outbreaks 73 65 37 19 7 38 116 357
*Institutional setting comprises camp, daycare, hospital, nursing home, prison, school, church, and workplace cafeteria.
Recreational area/facility comprises county and state park, beach, and a sports complex.
Other settings comprise a grocery store, commercial products, a 4H steer competition, communities, a farm, a National Western Stock Show, a public
outdoor area, and a club.
Setting was not available for 3 outbreaks involving leafy vegetables.
increased risk for HUS after E. coli O157 infection (18 feces and longer day length than with higher ambient tem-
20), although others have not found an association (21,22). perature, although both were statistically significant (30).
Additionally, the proportion of illnesses in female patients However, several studies of prevalence of E. coli O157 in
might relate to gender-specific food preferences. cattle feedlots have found either no variation by geography
Most outbreaks occurred during the summer. Cattle (31) or higher prevalence in herds in the south (32), where
shed the largest number of E. coli O157 organisms in their summertime daylight hours are shorter but ambient tem-
feces during summer months (23,24), coinciding with a peratures are higher. Geographic distribution might also
higher prevalence of E. coli O157 on hides in processing be influenced by presence of cattle called super shedders
plants (25). However, leafy vegetable-associated outbreaks that shed higher numbers of E. coli O157 bacteria (33). Dif-
exhibited distinct fall seasonality, which could be the re- ferences in reporting by state could also affect geographic
sult of summertime application to seedlings of irrigation patterns (4).
water, soil amendments, or fertilizers that might contain Several factors might have contributed to our finding
more E. coli O157 organisms than other seasons. There- that waterborne outbreaks were reported primarily among
fore, leafy vegetables harvested during fall might be more states bordering the Mississippi River. Cattle density is
likely to become contaminated than those grown at other high in the Midwest (25). E. coli O157-containing feces
times. Seasonality of leafy vegetableassociated outbreaks from cattle and other animals can be washed into nearby
could also relate to harvest location. Nearly three quar- bodies of water, especially during heavy rainfall (34). Karst
ters of leafy vegetable-associated outbreaks occurred dur- formations, which are rock formations that occur in several
ing AprilOctober; during this same time each year, most Midwest states, develop when acidic water begins to break
US-produced lettuce is harvested from the Salinas Valley down bedrock surfaces, allowing surface water to enter
(California) (26). For 4 of 5 recent outbreaks (20112012), fractures in limestone and contaminate ground water; stud-
detailed traceback information implicated lettuce harvested ies have shown that E. coli can survive in karst streams for
from farms in Salinas Valley (K.E. Heiman, unpub. data). prolonged periods (35). Karst formations exist in the coun-
The cause of higher infection rates in northern states ties that reported 2 of the 3 E. coli O157 outbreaks in which
than southern states is unknown (27). Cattle density might drinking water was the source; all were associated with
play a role. In other countries, areas with the highest cat- well water. The remaining well waterassociated outbreak
tle density had some of the highest rates of human E. coli occurred on a farm after heavy rain and flooding. However,
O157 infection (28). Cattle density does not appear to be karst formations are unlikely to explain outbreaks associ-
higher in northern states compared with southern states ated with untreated recreational water. Only 15 waterborne
(25), although it is very high in counties in California outbreaks were reported; therefore, interpretation of these
where most lettuce is produced (29). Other environmental findings is limited.
factors might have a role. Edrington et al. found a stronger Our study had several limitations. Reported out-
correlation between prevalence of E. coli O157 in cattle breaks likely underrepresent the number that occur (36).
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1300 Emerging Infectious Diseases www.cdc.gov/eid Vol. 21, No. 8, August 2015
E. coli O157, United States, 20032012
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Address for correspondence: Katherine E. Heiman, Centers for Disease
http://dx.doi.org/10.1017/S0950268814000880
28. Frank C, Kapfhammer S, Werber D, Stark K, Held L. Cattle density Control and Prevention, 1600 Clifton Rd NE, Mailstop A38, Atlanta, GA
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