Outbreaks of E. coli O157:H7 and Shiga toxin–producing E. coli O157:NM (subsequently referred to as E. coli O157) investigated by state and local health departments were reported to CDC by telephone, outbreak report, or through the routine foodborne disease outbreak surveillance system (9). In preparation for this summary, an epidemiologist reviewed all reports including published outbreaks not otherwise reported. Information collected from each outbreak report included city, setting, and suspected transmission route and vehicle. The date of first illness, hospitalizations, number of ill persons, bloody diarrhea, culture-confirmed illness, HUS, and deaths were also obtained. We defined an outbreak as >2 cases of E. coli O157 infection (at least 1 culture-confirmed) with a common epidemiologic exposure. For purposes of defining an outbreak, we considered a case as a stool culture yielding E. coli O157, or bloody diarrhea, or HUS. Each investigator reported the total number of outbreak-related cases, often including those with compatible clinical illness but without culture confirmation of illness. Infections acquired outside the United States were not included.

We defined outbreak onset as month and year first illness onset was reported, and outbreak setting as place where exposure occurred. Outbreaks due to a distributed food item and not isolated to a single venue or event were classified as communitywide. Fast-food settings were defined as establishments where payment is made before receiving food. Outbreaks were classified into 1 of 6 transmission routes on the basis of how most patients acquired the infection (foodborne, person-to-person, recreational water, drinking water, animal exposure, or laboratory). Outbreaks with a common exposure but in which a major transmission route was not identified were classified as unknown transmission route. Median outbreak sizes were compared by using the Kruskal-Wallis test. Outbreak-related HUS and death rates were compared by using a chi-square test.

Foodborne outbreaks were defined as the occurrence of >2 cases of E. coli O157 infection resulting from ingestion of a common food, or if food vehicle was undetermined, sharing a common meal or food facility. Food vehicles were grouped into the following categories: ground beef, other beef, produce, dairy, other, or unknown. Food vehicles were implicated statistically in case-control studies (p < 0.05), by isolation of E. coli O157 from a suspect item, or by being the only common food item consumed by cases. A multistate outbreak was defined as exposure to a common vehicle occurring in >1 state. HUS cases were classified by individual investigators and included those cases diagnosed as thrombotic thromobocytopenic purpura following E. coli O157 infection.

Figure 1

Figure 1. Escherichia coli O157 outbreaks by year, 1982–2002 (n = 350).

Figure 2

Figure 2. Median size of Escherichia coli O157 outbreaks by year.

From 1982 to 2002, a total of 350 outbreaks were reported from 49 states, accounting for 8,598 cases of E. coli O157 infection. Among cases, there were 1,493 (17.4%) hospitalizations, 354 (4.1%) cases of HUS, and 40 (0.5%) deaths. The number of reported outbreaks began rising in 1993, and peaked in 2000 with 46 (Figure 1). Outbreak size ranged from 2 to 781 cases, with a median of 8 cases. Median outbreak size appears to have declined from 1982 to 2002 (Figure 2). Most outbreaks (89%) occurred from May to November. Of the 326 outbreaks reported from a single state, Minnesota reported the most (43 outbreaks), followed by Washington (27 outbreaks), New York (22 outbreaks), California (18 outbreaks), and Oregon (18 outbreaks). Among the 350 outbreaks, transmission routes for 183 (52%) were foodborne, 74 (21%) unknown, 50 (14%) person-to-person, 21 (6%) recreational water, 11 (3%) animal contact, 10 (3%) drinking water, and 1 (0.3%) laboratory-related transmission route (Table).

Foodborne Outbreaks

Figure 3

Figure 3. Transmission routes of Escherichia coli O157 outbreaks by year.

Food remained the predominant transmission route from 1982 to 2002 (Figure 3), accounting for 52% of 350 outbreaks and 61% of 8,598 outbreak-related cases. Foodborne outbreaks most frequently occurred in communities (53 [29%] of 183), restaurants/food facilities (51 [28%]), and schools (16 [9%]). Median size of foodborne outbreaks varied by setting: the smallest occurred in individual residences (3 cases), and the largest outbreaks in residential facilities (44 cases), followed by camps (36 cases). Among 51 restaurant and food facility outbreaks, 22 were from chain establishments (including 12 fast-food establishments) and 29 from single establishments. The median number of cases per restaurant/food facility outbreak was larger in chain than single establishments (21 vs. 8, p < 0.001). Among the 183 foodborne outbreaks, the food vehicle for 75 (41%) was ground beef, 42 (23%) unknown, 38 (21%) produce, 11 (6%) other beef, 10 (5%) other foods, and 7 (4%) dairy products.

Ground Beef

Figure 4

Figure 4. Vehicles of foodborne Escherichia coli O157 outbreaks by year.

The first E. coli O157 outbreak was reported in 1982 and linked to ground beef, which remains the most common vehicle among foodborne outbreaks (75 [41%] of 183) (Figure 4), although it accounts for only 33% of 5,269 foodborne-related cases. Outbreaks involving ground beef peaked in summer months: 71% occurred from May to August. Of the 40 outbreaks for which ground beef preparation style was reported, 27 (68%) were linked to hamburgers and 5 (13%) to meat sauce. Ground beef outbreaks occurred most frequently at the communitywide level (36 of 75 [48%]), followed by 11 (15%) at picnics or camps, 8 (11%) at individual residences, 7 (9%) at restaurants, and 4 (5%) at schools. Of the 7 ground beef–associated restaurant outbreaks, 5 occurred in fast-food restaurants in 1982 (2 outbreaks), 1992–1993 (1 outbreak), 1995 (1 outbreak), and 1999 (1 outbreak). The last hamburger-associated fast-food restaurant outbreak was reported in 1995.

Produce

Produce-associated outbreaks were first reported in 1991 and have remained a prominent food vehicle (Figure 4), accounting for 38 (21%) of 183 foodborne outbreaks and 34% of 5,269 foodborne outbreak-related cases. Produce outbreaks peaked in summer and fall; 74% occurred from July to October. Thirteen (34%) produce outbreaks were from lettuce, 7 (18%) apple cider or apple juice, 6 (16%) salad, 4 (11%) coleslaw, 4 (11%) melons, 3 (8%) sprouts, and 1 (3%) grapes. Produce outbreaks most commonly occurred in restaurants (15 [39%]), and 7 (47%) of these were reported to be due to cross-contamination during food preparation. Twenty (53%) produce outbreaks did not involve kitchen-level cross-contamination, including the 7 apple cider or apple juice outbreaks, 7 of 10 lettuce outbreaks, 3 of 4 coleslaw outbreaks, and the 3 alfalfa or clover sprout outbreaks. None were reported to be due to imported produce. The median number of cases in produce outbreaks was significantly larger than that of ground beef outbreaks, 20 vs. 8, (p < 0.001).

Other Beef

Types of beef other than ground beef were implicated in 11 outbreaks. Five outbreaks were due to roast beef, 2 to steak, 1 to sirloin tips, and 1 to salami. The other 2 outbreaks included on identified only as “beef” and one as “raw roast beef.”

Dairy Products

Seven outbreaks were due to dairy products, including 4 from consuming raw milk. The others were due to cheese curds made from raw milk, from butter made from raw milk, and from commercial ice cream bars (possibly due to cross-contamination).

HUS Cases

Figure 5

Figure 5. Hemolytic uremic syndrome (HUS) and case-fatality rate per 100 outbreak-related illnesses.

Among 346 outbreaks that reported HUS cases, 132 (38%) reported at least 1 case of HUS (range 1–55 cases, median 2 cases), for a total of 354 HUS cases. The HUS rate (number of cases per 100 outbreak-related illnesses) was 4.1. From 1982 to 2002, the HUS rate appeared to decline overall (Figure 5). The HUS rate differed significantly by transmission route (p < 0.001) and was highest among swimming outbreaks (10.7), followed by person-to-person (6.8), unknown (6.7), animal contact (5.6), foodborne (3.5), and drinking water (2.1) related–outbreaks. Among foodborne outbreaks, the HUS case rate was significantly higher among ground beef–associated outbreaks compared with all other foodborne outbreaks (5.5 vs. 2.5, p < 0.001).

From 1982 to 2002, a total of 350 E. coli O157 outbreaks were reported in the United States from 49 states. Despite regulatory efforts to improve the safety of the U.S. food supply, foodborne E. coli O157 outbreaks remain common. Ground beef remains the most frequently identified vehicle, and produce-associated outbreaks are commonly reported. In addition, nonfoodborne transmission routes remain prominent. Person-to-person outbreaks occur most frequently in child daycare centers. Waterborne outbreaks caused by both drinking and recreational water continue to be reported, and outbreaks due to animal contact are increasingly reported.

In January 1993, the largest E. coli O157 outbreak from ground beef was reported in 4 western states, involving >700 ill persons, mostly children; more than one quarter were hospitalized, HUS developed in 7.5%, and 4 children died (3,10). Illness was linked to eating undercooked hamburgers at a chain fast-food restaurant, prompting a recall of >250,000 hamburgers, which likely prevented many additional illnesses and deaths.

Outbreak investigations that implicated fast-food hamburgers have led to major improvements in meat safety in the U.S fast-food industry. In 1993, the U.S. Food and Drug Administration revised the Model Food Code for restaurants, with new temperature guidelines for ground beef (11). In 1994, the National Livestock and Meat Board’s Blue Ribbon Task Force developed objective measures of meat “doneness” and encouraged use of automated cooking systems (12). No fast-food hamburger-associated outbreaks have been reported since 1995, demonstrating that changes in the fast-food industry, such as carefully regulating cooking temperature of hamburgers, are both possible and effective.

In addition, outbreak investigations coupled with traceback investigations of implicated meat have identified contaminated beef lots, leading to large recalls of potentially contaminated beef (3). These recalls of up to 25 million pounds of beef (13) likely prevented many additional infections. Despite these improvements, ground beef continues to be frequently implicated in E. coli O157 outbreaks. Raw beef, especially ground beef, can be contaminated with E. coli O157 and should be cooked thoroughly to kill pathogens and handled carefully to avoid cross-contamination of other food items. As ground beef outbreaks are commonly reported from home-prepared ground beef, educational efforts should be focused on teaching consumers safer handling and cooking practices.

Outbreaks provide information about inadequacy of processing methods. For example, in 1994, an E. coli O157 outbreak due to eating commercially distributed dry-cured salami product involved 23 persons; HUS developed in 13% (14). This outbreak prompted U. S. Department of Agriculture officials to develop regulations to ensure the safety of shelf-stable fermented sausages (15); no further E. coli O157 outbreaks due to U.S.–manufactured salami have been reported since.

E. coli O157 outbreaks due to produce have become increasingly common. While half of produce-associated outbreaks were due to kitchen-level cross-contamination, which calls for further prevention efforts targeting food preparers, the other half were due to produce already contaminated with E. coli O157 before purchase, including lettuce, sprouts, cabbage, apple cider, and apple juice (16–20). These produce items could have become contaminated in the field from manure or contaminated irrigation water; during processing due to contaminated equipment, wash water, or ice or poor handling practices; during transport; or through contaminated storage equipment. Washing produce with water or a chlorine-based solution reduces E. coli O157 counts only modestly (21,22); therefore, once consumers obtain contaminated produce intended for raw consumption, little can be done to prevent illness. Efforts by industry to decrease contamination of sprouts have had limited success (23,24). Until effective measures for preventing E. coli O157 contamination of produce items such as lettuce, cabbage, and sprouts can be implemented, consumers should be educated about potential risk of consuming these items raw. Further regulatory and educational efforts are needed to improve the safety of produce items.

In 1996, a large E. coli O157 outbreak occurred in 3 western states and British Columbia, involving 70 illnesses, mostly children; more than one third of patients were hospitalized, HUS developed in 20%, and 1 child died (20). Illness was attributable to drinking commercial unpasteurized apple juice. However, as a result of this outbreak investigation, apple cider and apple juice that are shipped interstate in the United States since 1998 are either pasteurized or, if sold raw, carry a warning label advising consumers of potential harmful bacteria in the product (25). Since 1998, only 2 outbreaks due to unpasteurized apple cider have been reported, 1 at a local fair and 1 from locally produced cider that carried a warning label.

Prevention efforts focused on hygiene are needed to reduce transmission in daycare settings. In outbreaks of other primary transmission routes, secondary cases occur, which emphasizes the importance of educating caretakers to avoid direct contact with fecal matter and to apply stringent handwashing rules.

Drinking and recreational water have the potential to infect many persons. The largest U.S. E. coli O157 outbreak occurred in 1999 at a county fair due to contaminated drinking water and involved 781 ill persons; 9% were hospitalized, HUS developed in 2%, and 2 died (26). The implicated water was from a temporary unregulated well at the fairground. Properly functioning water systems with adequate chlorine levels should protect against E. coli O157 contamination. Many U.S. households, however, receive municipal water that is not chlorinated. Further safeguards are therefore needed to ensure the safety of unchlorinated water systems and to ensure that chlorinated water systems are properly functioning. Educational efforts targeted at caretakers of young children should continue to help reduce contamination of recreational water areas by fecal matter (27,28).

Outbreaks associated with animal contact represent a newly recognized transmission route for E. coli O157 in the United States. Cattle hides may become contaminated from fecal matter. Persons touching cattle or surfaces in the cattle’s environment may contaminate their hands with E. coli O157. If hands are not washed thoroughly after contact with cattle or their environments, the bacteria can infect these persons through a hand-to-mouth route. Recent strategies published to help reduce transmission of enteric pathogens from farm animals to children include informing the public about risk for transmission of enteric pathogens from farm animals to humans, separating eating facilities from animal contact areas, and providing adequate handwashing facilities (29).

The overall decreased HUS and case-fatality rates in the last 2 decades likely represent increased reporting of less clinically severe outbreaks, especially after E. coli O157 became a reportable disease. The high HUS rate found in swimming-associated outbreaks may be due partly to the higher proportion of young children involved and their vulnerability to development of HUS. The reason for the higher HUS rate found among ground beef–related outbreaks is unclear and may reflect reporting bias. Outbreaks occurring in residential facilities such as nursing homes had a particularly high case-fatality rate, which emphasizes the need for prevention efforts, both educational and regulatory, to lower the incidence of E. coli O157 infections in such facilities.

Since 1992, molecular subtyping of E. coli O157 by pulsed-field gel electrophoresis has improved early outbreak detection. PulseNet (30), the national network for comparing molecular subtypes of common foodborne bacterial pathogens, including E. coli O157 since 1997, has greatly assisted in both identifying outbreaks and linking apparently unrelated outbreaks. Continued molecular subtyping of E. coli O157 strains from both humans and the environment will assist in detecting outbreaks and allow for identification of multistate, geographically dispersed outbreaks due to contaminated commercial products (30).

Outbreak surveillance has several limitations. E. coli O157 outbreaks captured by CDC’s surveillance system likely represent only a small proportion of outbreaks that occur. Many outbreaks go unrecognized, are classified as outbreaks of unknown etiology, and are not reported to local public health officials or CDC (31). Smaller outbreaks and outbreaks with unknown transmission routes and vehicles are less likely to be reported, and this summary likely under represents such outbreaks. Including patients with compatible clinical illness without culture confirmation is another limitation of outbreak surveillance. However, given the broad clinical spectrum of E. coli O157 infection, and the limited number of infected persons with culture-confirmed illness (5), such inclusion allows us to better assess the true public health impact of E. coli O157. In addition, outbreak reporting may not be uniform across time periods or states. Therefore, trends should be interpreted carefully, given the changing factors that may impact outbreak detection and reporting. The increased numbers of outbreaks reported since 1993 but with smaller sizes are likely due to increased awareness of disease, improved diagnostics, increased E. coli O157 testing, and improved outbreak detection through molecular subtyping.

Outbreak investigations, especially for emerging pathogens such as E. coli O157, are critical for better understanding these pathogens’ epidemiology, which affect policy and behavior changes. While a summary of outbreaks cannot draw firm conclusions on disease trends, illustration of transmission routes, food vehicles, outbreak size, and clinical outcomes over time empowers public health officials, regulatory agencies, and health educators to target appropriate interventions and reevaluate current prevention strategies.