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Foodborne Outbreaks of Enterotoxigenic Escherichia coli -- Rhode Island and New Hampshire, 1993

Infections with enterotoxigenic Escherichia coli (ETEC) are a frequent cause of diarrhea in developing countries but not in the United States and other industrialized countries. This report describes two foodborne ETEC outbreaks that occurred in the United States in 1993. Rhode Island

On March 25, the Rhode Island Department of Health was notified of gastrointestinal illness among passengers on an airline flight from Charlotte, North Carolina, to Providence, Rhode Island, on March 21. The flight carried 98 passengers; 47 (64%) of 74 passengers who were interviewed met the case definition of three or more loose stools in 24 hours beginning within 4 days after the flight. Additional symptoms included abdominal cramps (94%), nausea (70%), headache (57%), fever (13%), and vomiting (13%). The only common meal for all ill passengers was dinner served on board the flight. The median incubation period was 41 hours (range: 12-77 hours); two (5%) of 44 persons recovered within 48 hours of onset of illness.

Illness was most strongly associated with eating garden salad made from shredded carrots and iceberg, romaine, and endive lettuce (46 {98%} of 47 ill passengers compared with six {22%} of 27 well passengers; relative risk {RR}=4.4; 95% confidence interval {CI}=2.2-8.9). Investigators from the Food and Drug Administration (FDA) contacted 18 passengers who had traveled on March 21 on a different flight operated by the airline and who had been served the same meal; nine passengers reported gastrointestinal illness. On March 21, approximately 4000 portions of salad had been prepared by one catering service for 40 flights operated by the same airline that day. The FDA traceback determined that all of the salad ingredients were of U.S. origin.

Stool specimens obtained from 20 passengers from the index flight were negative on culture for Salmonella, Shigella, Campylobacter, Yersinia, and Vibrio, and viral particles were not observed in 12 stool specimens examined by electron microscopy at CDC. E. coli isolates from 10 ill passengers were tested for ETEC at CDC. ETEC strains (serotype O6:non-motile {NM}) that produced heat stable (ST) and heat labile (LT) toxins were identified in isolates from three passengers.

FDA inspection of the caterer's facilities did not identify deficiencies in sanitary conditions. In addition, all food handlers denied gastrointestinal illness or recent travel outside the United States. Samples of food collected for culture on March 27 did not yield ETEC. New Hampshire

On April 5, the New Hampshire Division of Public Health Services was notified of gastrointestinal illness in eight persons who ate a buffet dinner served at a mountain lodge on March 31. A total of 202 persons ate the dinner, including 132 guests and 70 lodge employees. A case was defined as diarrhea (three or more loose or watery stools in a 24-hour period) and one other symptom (cramps, fever, headache, nausea, or vomiting) with onset from April 1 through April 7 in a guest or employee who had eaten the dinner. Of the 123 guests and 56 employees who were interviewed, 96 (78%) and 25 (45%), respectively, had illness that met the case definition. Additional symptoms included cramps (92%), nausea (59%), myalgias (50%), headache (49%), fever (22%), and vomiting (11%). Illness began a median of 38 hours after foods from the buffet were eaten (range: 3-159 hours); 60 (65%) of 93 persons for whom information was available reported continuing illness 4-6 days after symptom onset.

Illness among guests was most strongly associated with consumption of tabouleh salad (cases occurred in 78 {94%} of 83 guests who ate the tabouleh and 18 {53%} of 34 guests who did not {RR=1.8; 95% CI=1.3-2.5}). Tabouleh was the only food associated with illness among lodge employees (RR=6.4; 95% CI=2.2-18.8). The tabouleh was prepared from onions, carrots, zucchini, peppers, broccoli, mushrooms, green onions, tomatoes, parsley, bulgur wheat, olive oil, lemon juice, and bottled garlic. All of the produce was of U.S. origin. The salad was prepared the evening before the banquet. All food preparers denied gastrointestinal illness or travel outside the United States the week before the banquet.

Cultures of stool specimens obtained from 14 persons were negative for Salmonella, Shigella, Campylobacter, and Yersinia; neither ova nor parasites were detected in stool specimens from seven ill persons. However, ETEC (serotype O6:NM) that produced LT and ST was isolated from stool specimens from seven of nine ill guests and from one of five well employees. Additional ETEC serotypes also were isolated from six specimens. Follow-up Investigation

Plasmid profiles of the O6:NM strains from the outbreaks in New Hampshire and Rhode Island were identical but differed from those of 10 other serotype O6:NM ETEC strains from other sources. Carrots were the only item common to the tabouleh salad implicated in New Hampshire and the garden salad implicated in Rhode Island. Carrots used in both salads were grown in the same state; however, a traceback conducted by the New Hampshire Division of Public Health Services in collaboration with FDA and CDC did not identify a single source. FDA is investigating the implicated carrot sales agency in the state where the carrots were grown. Reported by: V Benoit, P Raiche, MG Smith, MD, State Epidemiologist, New Hampshire Div of Public Health Svcs. J Guthrie, MD, Univ of Rhode Island Infirmary; EF Donnelly, MPH, EM Julian, PhD, R Lee, MS, S DiMaio, M Rittmann, BT Matyas, MD, State Epidemiologist, Rhode Island Dept of Health. Atlanta District Office and Div of Emergency and Epidemiology Operations, Food and Drug Administration. Div of Field Epidemiology, Epidemiology Program Office; Respiratory and Enterovirus Br, Div of Viral and Rickettsial Diseases; Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

Editorial Note

Editorial Note: Since 1975, 13 outbreaks of ETEC gastroenteritis in the United States have been reported to CDC; four (31%) of these outbreaks, including the two described in this report, occurred in 1993. Although each of the four outbreaks in 1993 and five outbreaks reported previously were foodborne, ETEC outbreaks associated with waterborne and person-to-person transmission have been described (1,2). At least one foodborne ETEC outbreak in the United States was attributed to spread from an infected food handler (3) and another to imported contaminated food (4). However, none of the recent foodborne outbreaks were associated with these sources. Salads containing raw vegetables have been associated with ETEC infection (5).

Because ETEC is not detected by standard stool culture methods for Salmonella, Shigella, Vibrio, or other enteric bacterial pathogens and because symptoms of ETEC infection are relatively nonspecific, outbreaks caused by ETEC may be incorrectly attributed to a viral etiology. Watery diarrhea is the predominant symptom of ETEC infection, usually reported by more than 90% of patients (3- 5). The diarrhea is often accompanied by abdominal cramps and is generally mild, although severe dehydrating diarrhea has been reported (6). Two percent to 13% of patients report vomiting (3-5).

In contrast to illness caused by ETEC, gastroenteritis from infection with Norwalk virus is usually characterized by vomiting but not by diarrhea (7). Because nausea, headache, and myalgias occur with varying frequency in association with ETEC and Norwalk virus infections, these symptoms are less useful for differentiating the two illnesses (3-5,7). The incubation periods are similar for ETEC and Norwalk gastro- enteritis (range: 24-48 hours) (2-4,7). However, duration of illness is shorter for Norwalk gastroenteritis (usually less than or equal to 3 days) and longer for illness caused by ETEC infection (often greater than 4 days) (1-5,7).

Laboratory identification of ETEC depends on testing E. coli isolates by methods that are not widely available. For well characterized outbreaks of watery diarrheal illness for which no pathogen has been identified during routine bacteriologic examinations, arrangements can be made through local and state health departments to send E. coli isolates to CDC for testing. ETEC previously has been recognized primarily as a cause of traveler's diarrhea. However, the findings in this report indicate that clinicians and microbiologists may need to consider ETEC in patients with diarrheal illness who did not travel (8).


  1. Rosenberg ML, Koplan JP, Wachsmuth IK, et al. Epidemic diarrhea at Crater Lake from enterotoxigenic Escherichia coli: a large waterborne outbreak. Ann Intern Med 1977;86:714-8.

  2. Ryder RW, Wachsmuth IK, Buxton AE. Infantile diarrhea produced by heat-stable enterotoxigenic Escherichia coli. N Engl J Med 1976;295:849-53.

  3. Taylor WR, Schell WL, Wells JG, et al. A foodborne outbreak of enterotoxigenic Escherichia coli diarrhea. N Engl J Med 1982;306:1093-5.

  4. MacDonald KL, Eidson M, Strohmeyer C, et al. A multistate outbreak of gastrointestinal illness caused by enterotoxigenic Escherichia coli in imported semisoft cheese. J Infect Dis 1985; 151:716-20.

  5. Merson MH, Morris GK, Sack DA, et al. Traveler's diarrhea in Mexico: a prospective study of physicians and family members attending a conference. N Engl J Med 1976;294:1299-305.

  6. Sack RB, Gorbach SL, Banwell JG, Jacobs B, Chatterjee BD, Mitra RC. Enterotoxigenic Escherichia coli isolated from patients with severe cholera-like disease. J Infect Dis 1971; 123:378-85.

  7. Kaplan JE, Gary GW, Baron RC, et al. Epidemiology of Norwalk gastroenteritis and the role of Norwalk virus in outbreaks of acute nonbacterial gastroenteritis. Ann Intern Med 1982; 96:756-61.

  8. Osterholm MT, Hedberg CW, MacDonald KL. Prevention and treatment of traveler's diarrhea {Letter}. N Engl J Med 1993;329:1584-5.

+------------------------------------------------------------------- ------+ | Erratum: Vol. 43, No. 5 | |             | | SOURCE: MMWR 43(07);127 DATE: Feb. 25, 1994 | |             | | In the article "Foodborne Outbreaks of Enterotoxigenic | | Escherichia coli -- Rhode Island and New Hampshire, 1993," in the | | third paragraph of the editorial note, the first sentence should | | read "In contrast to illness caused by ETEC, gastroenteritis from | | infection with Norwalk virus is usually characterized by vomiting | | in addition to diarrhea." | |             | +------------------------------------------------------------------- ------+

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