E. coli O157:H7 outbreaks associated with lettuce or spinach, specifically the “pre-washed” and “ready-to-eat” varieties sold under various brand and trade names, are by no means a new phenomenon. In October 2003, 13 residents of a California retirement center were sickened and 2 died after eating E. coli-contaminated “pre-washed” spinach. In September 2003, nearly 40 patrons of a California restaurant chain became ill after eating salads prepared with bagged, “pre-washed” lettuce. In July 2002, over 50 young women were stricken with E. coli at a dance camp after eating “pre-washed” lettuce, leaving several hospitalized and one with life-long kidney damage. The Center for Science in the Public Interest found that, of 225 food-poisoning outbreaks from 1990 to 1998, nearly 20 percent (55 outbreaks) were linked to fresh fruits, vegetables, or salads.
It is clear that the risks associated with E. coli O157:H7 and lettuce were well known to Dole and the industry prior to the 2005 outbreak. For some time prior to the outbreak, the FDA had been aggressively trying to get the industry to address serious deficiencies that were creating a critical risk to consumers. The response by Dole and many of its industry brethren was woefully inadequate.
In November 2005, the FDA elucidated its past efforts and present concerns in its “Letter to California Firms that Grow, Pack, Process, or Ship Fresh and Fresh-Cut Lettuce.” The letter begins:
This letter is intended to make you aware of the Food and Drug Administration’s (FDA’s) serious concern with the continuing outbreaks of foodborne illness associated with the consumption of fresh and fresh-cut lettuce and other leafy greens.
The FDA goes on to identify 18 outbreaks of E. coli O157:H7 associated with fresh or fresh-cut lettuce, resulting in 409 illnesses and two deaths since 1995. According to the FDA, completed traceback investigations in eight of the outbreaks”the 2005 Dole outbreak included”were traced to Salinas, California. The FDA further states that the industry’s role in preventing these illnesses is crucial because “these products are commonly consumed in their raw state without processing to reduce or eliminate pathogens.”
The FDA efforts to lead the lettuce industry to safer practices were nothing new. In 1998, the FDA issued guidance to the industry entitled “Guide to Minimize Microbial Food Safety Hazards for Fruits and Vegetables.” The guide is specifically designed to assist growers and packers in the implementation of safer manufacturing practices. On February 5, 2004, the FDA issued a letter to the lettuce and tomato industries to “make them aware of [FDA’s] concerns regarding continuing outbreaks associated with these two commodities and to encourage the industries to review their practices.”
The 2005 Dole outbreak prompted even more industry-admonition by the FDA: “In light of continuing outbreaks associated with fresh and fresh-cut lettuce and other leafy greens, particularly from California, we are issuing this second letter to reiterate our concerns and to strongly encourage firms in your industry to review their current operations.” This November 2005 FDA letter explicitly rejected industry excuses for not having taken prior action. Further, the FDA cited to research linking some or all of the outbreaks to sewage exposure, animal waste, and other contaminated water sources. The research further indicated that industry practices, including irrigation and field drainage methods, may have led directly to the contamination of the lettuce with E. coli O157:H7. As a result the FDA stated that it considers “adulterated” any ready to eat crops that have come in contact with flood waters. The FDA closed by warning industry members that food produced under unsanitary conditions is adulterated under 402(a)(4) of the Food, Drug, and Cosmetic Act, and that enforcement actions would be considered.
THE DOLE OUTBREAK
“DOLE Classic Romaine is triple washed and ready-to-eat. As a result, it is not necessary to wash the salad prior to eating.” From Dole Food webpage
On September 22, 2005 the Minnesota Department of Health (MDH) Public Health Laboratory (PHL) received an E. coli O157:H7 isolate for confirmatory testing and Pulse Field Gel Electrophoresis (PFGE) subtyping. PFGE results were reported on September 26 and uploaded to PulseNet, a national database of PFGE patterns or “fingerprints” maintained at the federal Centers for Disease Control and Prevention (CDC). The pattern derived from digestion with the restriction endonuclease Xba I was assigned Pattern number EXHX01.0238. The isolate was soon tested with a second enzyme, Bln I, and the resulting pattern was assigned pattern number EXHA26.1040. Prior to September 19, the Bln I pattern had not been posted on PulseNet.
Isolates obtained from culture of stool submitted by two new ill patients were received at the MDH PHL on September 23, 2005 and subtyped. PFGE results showed that the two new isolates and the isolate received on September 22 were indistinguishable by two enzymes. By September 29, 2005 isolates obtained from seven more patients arrived at the MDH PHL for further analysis. Public health investigators recognized that an E. coli O157:H7 outbreak was underway in Minnesota.
While laboratory testing was performed, MDH epidemiologists conducted preliminary interviews with patients who were laboratory confirmed with E. coli O157:H7. On the morning of September 28 investigators had identified pre-packaged lettuce produced by Dole Food Company, Inc. as the likely vehicle of transmission for infection with E. coli O157:H7. A supplemental questionnaire focusing on the type and brand of lettuce consumed and where it was purchased, was developed and administered to case-patients previously interviewed and newly identified cases. On September 29 Minnesota Department of Agriculture (MDA) staff collected a bag of Dole lettuce at the home of a case patient and began microbiologic testing for the presence of E. coli O157:H7.
On September 30 the MDH issued a press release advising the public that 11 cases of E. coli O157:H7 had been identified in Minnesota residents who had eaten Dole lettuce purchased from at least four different stores in the Twin Cities area. See Attachment No. 2, Minnesota Department of Health News Release, September 30, 2005. Dr. Kirk Smith, an MDH foodborne disease specialist, advised consumers to discard Dole pre-packaged lettuce mixes with the “Best if Used by 09/23/05” date. Persons with symptoms of E. coli were told to contact the MDH and their physician. Dr. Chris Braden at the Foodborne and Diarrheal Disease Branch at the CDC announced that no other states were reporting outbreak associated cases.
Meanwhile MDA microbiologists continued to process lettuce specimens obtained from households with cases of confirmed E. coli O157:H7. On Monday, October 3 the agency reported that sample number M-05-2310, Lot Number B250215B received on September 30 had tested positive for E. coli O157:H7. The isolate obtained from the sample was sent to the MDH for PFGE analysis. The resulting pattern was indistinguishable to the pattern identified in case-patients. A second specimen, M-05-2318, lot number unavailable, would also yield positive results. See Attachment No. 3, Minnesota Department of Agriculture Laboratory Analysis Report dated 10/20/2005.
News of the positive lettuce specimen prompted the Food and Drug Administration (FDA) to issue a nationwide health alert regarding Dole pre-packaged salads on October 2. See Attachment No. 4, FDA Issues Nationwide Health Alert on Dole Pre-Packaged Salads. The FDA announcement reiterated warnings expressed in the MDH press release and further described the Dole products associated with illness, Classic Romaine, American Blend, and Greener Selection. Although cases had only been identified in Minnesota, the product was noted to have been distributed nationwide.
It would not be long before cases of E. coli O157:H7 in Wisconsin and Oregon would be recognized. The Wisconsin case was a 12 year old female with E. coli O157:H7 who had a history of eating Dole pre-packaged lettuce. PFGE subtyping showed that her isolate was indistinguishable to the EXHX01.0238 pattern and one band different on the second enzyme pattern. Despite the one band difference, MDH molecular epidemiologists considered the girl to be part of the outbreak concluding that the difference was not enough to preclude the case from being considered outbreak related.
The Oregon case was indisputably associated with consumption of Dole pre-packaged salad mix. A 60 year old Portland resident was hospitalized and laboratory confirmed with E. coli O157:H7 on September 21, 2005. The patient had experienced onset of symptoms on September 18, four days after purchasing and consuming Dole brand “Classic Romaine” salad mix. Michael Roberson, representative for Albertsons’, the grocery store of purchase, confirmed that the chain’s Portland area distributing center had received Dole Greener Selection and Dole Classic Romaine. See Attachment No. 5, email message from Michael Roberson to William E. Keene, dated 10/6/2005. A portion of the salad mix was still in the patient’s refrigerator. A photograph taken of the packaging documents that Ms. Scheetz purchased Dole salad mix with a “Best if Used By” date of 9/23/05, lot number was B250215B. See Attachment No. 6, email message from Bill Keene to Dr. Melvin N. Kramer, dated 10/24/2005. PFGE subtyping showed that the Oregon isolate was indistinguishable by two enzymes to other ill Dole lettuce consumers in Minnesota.
Aware of the potential severity of an E. coli O157:H7 outbreak, the FDA and the Food and Drug Branch at the California Department of Health Services initiated an investigation at the Dole processing plant. Preliminary information indicated that 22,321 cases of Dole pre-packaged lettuce with a “Best If Used By” date of 9/23/05 and a production code starting with “B250” were shipped from a single Dole processing facility in central California to 34 states in early September. Investigators estimated that since each case contained between 6 and 12 bags, approximately 244,866 bags of lettuce had made it to market.
On October 11, 2005 the MDH counted 23 laboratory confirmed cases of E. coli O157:H7 and seven epidemiologically linked cases. Illness onset dates ranged from September 16 to September 30. Two cases had developed Hemolytic Uremic Syndrome (HUS). Oregon and Wisconsin reported one case each. Case control study data show a statistically significant association between illness and consuming Dole pre-packaged lettuce with a matched odds ratio of 6.8, 95% confidence interval, 1.4-31.9, and a p-value of 0.01.