Surveillance

We identified E. coli O157 outbreaks in the United States using these sources: the Foodborne Disease Outbreak Surveillance System (FDOSS) for outbreaks during 2003–2012; the Waterborne Disease Outbreak Surveillance System (WBDOSS) for outbreaks during 2003–2010 (data were not available after 2010); the National Outbreak Reporting System (NORS) for outbreaks facilitated by transmission between persons, animal contact, environmental contamination, or with an unknown transmission mode during 2009–2012 (4); reports to the Centers for Disease Control and Prevention of person-to-person and animal contact–associated outbreaks during 2003–2008; and PubMed using these search terms: Escherichia coli O157 outbreak, STEC O157 outbreak, Escherichia coli O157, STEC O157, and O157. Data reported for each outbreak, with varying degrees of completeness, included primary transmission mode; states where exposure occurred; number of illnesses (culture-confirmed and epidemiologically linked); hospitalizations; HUS cases (defined by physician diagnosis; no laboratory data were collected); deaths, age, and sex distribution of patients; month the outbreak began; and setting where the outbreak occurred or, for foodborne disease outbreaks, the place of food preparation. For foodborne disease outbreaks, the implicated food (if identified) was reported. For waterborne disease outbreaks, water source type (e.g., recreational, drinking, waste water) was reported.

Definitions

An E. coli O157 outbreak was defined as an event during which ≥2 persons had culture-confirmed E. coli O157:H7 or O157:NM infection resulting from a common exposure. Epidemiologically linked, clinically compatible cases without laboratory confirmation were included in the case count. States within the contiguous United States were categorized as “north” if they were located entirely north of parallel 37 north latitude and “south” if entirely below this latitude; states crossing this line (California and Nevada) were excluded from some analyses.

Implicated foods were classified into categories by using an existing classification scheme (5) with 2 modifications: fruits and nuts were classified separately and meat acquired by hunting was classified with other meat. Implicated foods were further classified by whether they were usually consumed cooked (beef, other meats, poultry) or raw (leafy vegetables, fruits, unpasteurized dairy, sprouts). Steak was considered tenderized if described as tenderized or injected. Settings were classified as home; restaurant (e.g., restaurant, delicatessen, or banquet facility); institution (e.g., childcare center, school, or prison); fair; petting zoo; recreational area (e.g., park or beach); and other (e.g., grocery store, commercial production facility, or farm animal show).

Analysis

We summarized demographic and epidemiologic findings by transmission mode and food categories for which >3 outbreaks were reported. Two periods, 2003–2007 and 2008–2012, were evaluated to assess changes over time. Severity was assessed by calculating hospitalization (no. hospitalized/total no. ill) and HUS rates (no. physician–diagnosed HUS cases/total no. ill). Culture-confirmation rates (no. culture-confirmed/total no. ill) were also calculated. Analyses of settings were limited to outbreaks that occurred in a single setting type. For transmission modes other than food, data for age group, sex, and culture confirmation were not available before 2009. We compared the median outbreak size and state outbreak rates (outbreaks with exposure occurring in a single state/sum of state populations during 2003–2012, from U.S. Census Bureau intercensal estimates) using the Kruskal-Wallis test, and performed categorical analyses using χ² and Fisher exact tests; 2-tailed p values <0.05 were considered significant.

Vehicles

Of the 255 foodborne disease outbreak reports, 170 (67%) implicated a specific food, of which 141 (83%) could be classified into a single category. The implicated categories were beef (78 outbreaks, 55%), leafy vegetables (29, 21%), dairy (16, 11%), fruits (6, 4%), other meats (7, 5%), sprouts (3, 2%), nuts (1, 1%), and poultry (1, 1%) (Table 1). The types of beef implicated were ground beef (54 outbreaks, 69% of beef-associated outbreaks) and steak (10, 14%). The types of steak, reported in 5 outbreaks, were sirloin (4 outbreaks) and filet mignon (1). Steaks were mechanically tenderized in 5 outbreaks (2 sirloin, 1 filet mignon, 2 unknown). Other implicated meats were venison (3 outbreaks), lamb (2), and bison/buffalo (2).

In all 16 outbreaks attributed to dairy, unpasteurized products were implicated; 13 (81%) to unpasteurized milk and 3 (9%) to cheese made from unpasteurized milk. Most outbreaks attributed to leafy vegetables implicated lettuce (22 outbreaks, 76%), including romaine (3), iceberg (1), and mesclun mix (1); others in this category were spinach (4, 13%) and salads with unspecified types of greens (3,10%). Outbreaks attributed to fruit implicated unpasteurized apple cider (4 outbreaks), fruit salad (1), and strawberries (1), a newly identified food vehicle for this pathogen. Other newly identified food vehicles were hazelnuts sold in the shell (1 outbreak), packaged cookie dough (1), salsa (2), and pico de gallo (2). A total of 39 outbreaks were transmitted by contact with animals; >1 animal type was reported for 24 (62%), including cattle (15), goats (12), sheep (8), pigs (3), rabbits (3), chickens (2), and 1 each of elk, llama, alpaca, hedgehog, and dog. Every outbreak that identified a reported animal type included >1 ruminant animal. Although no specific animal types were listed for the remaining 14 outbreaks, livestock were reported for 2 and petting zoos or county fairs for 11.

Of the 15 waterborne disease outbreaks, 10 were attributed to recreational water (3 treated, 7 untreated), 3 to drinking water, and 1 possibly to wastewater. The water source was unknown for the remaining outbreak.

Severity

The severity of outbreaks differed by transmission mode and among foodborne disease outbreaks by food category (Table 1). Hospitalization rates were lower for person-to-person outbreaks compared with all other transmission modes (14% vs. 28%, p<0.0001). Physician-diagnosed HUS rates were higher for animal contact outbreaks than for all other modes (9% vs. 6%, p = 0.0005). The 33 deaths occurred in foodborne (25 deaths), person-to-person (2), animal contact (2), and waterborne (1) disease outbreaks; transmission mode was unknown for 3 deaths.

Among foodborne disease outbreaks, hospitalization rates were lower for outbreaks attributed to beef than for all other food vehicles (28% vs. 35%, p<0.001). Hospitalization rates were higher among outbreaks attributed to foods generally consumed raw than for cooked foods (35% vs. 28%, p = 0.0001). Deaths occurred most commonly in outbreaks attributed to leafy vegetables (7 deaths, 0.8% of illnesses in leafy vegetable outbreaks), fruits (6, 11%), and beef (5, 0.4%).

Demographic Characteristics

Age group distribution of cases varied by transmission mode and food category (Figure 2). Patient age group was available for 2,884 (81%) illnesses in foodborne outbreaks, 63 (90%) illnesses in waterborne outbreaks, and, during 2009–2012, 121 (96%) illnesses in person-to-person outbreaks and 189 (73%) illnesses in animal contact outbreaks. Most of the illnesses in person-to-person outbreaks (73, 60%) were among children <5 years old. The highest proportions of illnesses in waterborne and animal contact outbreaks (67% and 43%, respectively) were among persons 5–19 years of age. Foodborne disease occurred among persons in all age groups; only 8% of foodborne illnesses occurred among children <5 years of age, but >25% of dairy-associated illnesses were among children of this age group. The largest proportions of illnesses in outbreaks attributed to beef and dairy were among persons 5–19 years old (38% and 47%, respectively), whereas the largest proportion reported in outbreaks attributed to sprouts and leafy vegetables was among persons 20–49 years old (71% and 45%, respectively).

Overall, 55% of patients were women; the percentage did not vary significantly by transmission mode. Patient sex was available for 3,385 (92%) illnesses in foodborne disease outbreaks, 63 (90%) illnesses in waterborne outbreaks, and, from 2009–2012, 126 (97%) illnesses in person-to-person outbreaks and 193 (80%) illnesses in animal contact outbreaks. In foodborne disease outbreaks, the proportion of female patients was highest in outbreaks attributed to fruits (67%) and leafy vegetables (65%) and lowest in outbreaks attributed to meats other than beef (31%) (p<0.0001); cases were evenly distributed among women and men in outbreaks attributed to beef and dairy.

Seasonality

E. coli O157 outbreaks occurred year-round; however, nearly half occurred during July–September (175, 46%) (Figure 3). The seasonality of foodborne outbreaks varied by food category. Beef-associated outbreaks occurred most often in July (21 outbreaks, 27%), and leafy vegetable-associated outbreaks in September (8, 28%). Waterborne disease outbreaks occurred most often during June (6, 40%) and outbreaks associated with animal contact during August (13, 37%).

Geographic Distribution of Outbreaks and Multistate Outbreaks

Outbreaks were reported by 43 states (Figure 4). The median outbreak rate in northern states was >2× the rate in southern states (0.015 vs. 0.006/100,000 population, p = 0.005), which was also true for foodborne disease outbreaks (0.007 vs. 0.002, p = 0.02). Most waterborne disease outbreaks were reported in states bordering the Mississippi River (13, 87%), including all 3 drinking water outbreaks and all 7 recreational water outbreaks associated with lakes or other natural, untreated bodies of water. Waterborne disease outbreaks reported by California (1) and Idaho (1) were associated with treated recreational water.

Of the 390 outbreaks reported, 44 (17%), all foodborne, were multistate. Multistate outbreaks were larger than single state outbreaks (median 22 cases vs. 5, p<0.0001). The food categories implicated in multistate outbreaks were beef (22 outbreaks, 17 attributed to ground beef), leafy vegetables (12), unpasteurized dairy products (3), sprouts (1), nuts (1), and other meats (bison, 1).

Settings

Among 222 foodborne outbreaks for which food preparation settings were reported, a single setting was reported for 183 (84%). Restaurants were the most common settings (73 outbreaks, 40%), followed by private homes (60, 33%) (Table 2). Beef was most frequently prepared in a home (34, 56%), followed by restaurants (15, 25%). Leafy vegetables were most often prepared in restaurants (13, 59%), followed by homes (4, 18%).

Most (17, 89%) outbreaks with person-to-person transmission and a reported setting occurred in institutions; all except 1 institutional outbreak occurred in a childcare center. Petting zoos and fairs were the most common setting for outbreaks attributed to animal contact (17, 71%). Waterborne outbreaks occurred most often in recreational settings (7, 47%), including lakes (4), a pool (1), a sports complex (1), and an interactive fountain (1).

Conclusions

More E. coli O157 outbreaks were reported during 2003–2012 than during the previous 20 years (3), probably because of continued improvements in surveillance. Outbreaks in the United States continue to be caused mostly by contaminated food, especially beef. People can protect themselves through proper handling of raw beef, by cooking nonintact beef products such as ground beef and mechanically tenderized steak to internal temperatures of at least 160°F, and by thorough handwashing after contact with animals or their environment. Clearly labeling mechanically tenderized beef might help consumers make safer choices. Pasteurizing dairy products and fruit juices is recommended. Further research is needed to identify interventions to reduce the risk of illness caused by consumption of raw produce. Ways must be found to encourage implementation of interventions such as decreasing contamination in the production of produce, vaccinating cattle, and irradiating foods (40). Consideration of the proximity of agriculture fields to cattle operations, as well as adherence to Good Agricultural Practices specified by the US Department of Agriculture (http://www.ams.usda.gov/AMSv1.0/gapghp) during production, will also help reduce risk. Continued surveillance is needed to monitor changes in food vehicles of contamination and to improve our understanding of the geographic distribution of outbreaks.