In early July 2004, while conducting routine surveillance, Pennsylvania Department of Health (PDOH) personnel noted an increase in reported Salmonella Group D infections occurring in state residents. Salmonella is a reportable disease in Pennsylvania and laboratories throughout the state are asked to submit isolates to the PDOH Public Health Laboratory (PHL) for serotyping. By July 9 the PDOH PHL had serotyped more than twelve Salmonella isolates as Salmonella javiana, a substantially higher number than the one or two cases of Salmonella javiana reported to the PDOH in a typical month. Local health departments and area laboratories were asked to promptly report all cases of Salmonella to the PDOH.
The number of reported Salmonella Group D cases continued to climb. Cases were geographically distributed throughout central and western Pennsylvania indicating that the problem was related to a contaminated product in the supply chain versus a food safety error at a specific food service facility. The PDOH notified the federal Centers for Disease Control and Prevention (CDC) that an apparent foodborne outbreak was occurring and that cases of Salmonella javiana might be reported in other states. Active case finding was expanded to include nearby states. Ohio, Maryland, and West Virginia all reported an increase in Salmonella javiana cases.
Hypothesis generating interviews with case patients implicated food prepared and purchased at Sheetz convenience stores in Pennsylvania and Ohio. The association between Salmonella and Sheetz had not been seen in cases reported in previous months. Cases indicated that a variety of Sheetz menu items had been consumed in the 72 hours before symptom onset. Produce appeared to be a common ingredient of the foods consumed. In particular, many of the ill individuals said they had eaten lettuce and/or tomatoes as part of sandwiches and salads prepared at Sheetz deli counters.
Health officials notified Sheetz company officials that food prepared and served at Sheetz stores was suspected to be the source of a foodborne outbreak. On July 12 Sheetz officials authorized removal of all produce with an expiration date of July 12, 2004 from its stores. The company alerted Coronet Foods, a Wheeling, West Virginia based company, that Coronet supplied produce might be contaminated with Salmonella. The U.S. Food and Drug Administration (FDA) began working with Sheetz and Coronet Foods on a product trace back.
On July 14, 2004 a PDOH spokesperson, Richard McGarvey, announced that an outbreak of salmonellosis associated with food prepared at Sheetz convenience stores was being investigated. The CDC and the PDOH began a coordinated multi-state case-control outbreak investigation. By this time 4 states – Pennsylvania, West Virginia, Maryland and Ohio – were reporting a combined total of 56 cases of salmonellosis in persons who had eaten food at a Sheetz store. Dates of illness onset ranged from July 2 to July 10. States with laboratory confirmed cases of Salmonella Group D or Salmonella javiana were asked to administer a standardized questionnaire developed for the outbreak.
For the case control study, cases were defined as persons with culture confirmed Salmonella who ate at a Sheetz convenience store in late June or early July. Controls were Sheetz customers who had not become ill with vomiting or diarrhea within seven days of eating Sheetz prepared food. Controls, identified by cases, were either dining companions or were known to be regular Sheetz customers. Cases and controls were asked about consumption of specific menu items and ingredients included in each item.
Media reports of the outbreak were aired on July 15 identifying tainted produce, possibly Roma or plum tomatoes, as the potential source of illness. This information was reaffirmed on July 16, 2004 when the PDOH issued a Health Advisory, stating that an outbreak of Salmonella javiana with more than 70 reported cases had been associated with eating at Sheetz deli counters throughout the state. See Health Advisory #13, as Attachment No. 1.
Also on July 16, 2004, Coronet Foods publicly responded to PDOH preliminary findings, acknowledging that it had supplied sliced Roma tomatoes to Sheetz stores and had thereafter taken precautionary measures. Coronet ceased purchasing and processing Roma tomatoes, moved existing stock off-site, and re-sanitized its entire tomato processing line. The FDA collected multiple foods samples from the Coronet facility for laboratory testing.
By July 19, 2004 over 100 cases of Salmonella linked to consumption of food purchased at Sheetz had been reported in persons residing in Pennsylvania, Maryland, Ohio, West Virginia, and Virginia. Preliminary results of data collected in the case control study showed a statistical association with illness and consumption of tomatoes (Odds Ratio=7.6, p=0.0045). There was no association between illness and consumption of lettuce.
The association between illness and tomato consumption was bolstered that day when the Pennsylvania Department of Agriculture (PDOA) announced that Salmonella had been found in an unopened bag of sliced Roma tomatoes obtained from a Sheetz store in Greencastle, Pennsylvania on July 13. The tomatoes had been distributed to the Sheetz store by Coronet Foods. See Department of Agriculture Press Release, and laboratory reports, as Attachment No. 2. Further analysis revealed that the tomatoes were contaminated with Salmonella anatum, a strain of Salmonella different from Salmonella javiana. Investigators expanded their investigation to include cases of Salmonella anatum. Finding two or more Salmonella strains in a single outbreak was unusual but had happened before. Three strains were found in beef jerky that sickened 93 people in New Mexico in 1995 (See CDC. Outbreak of salmonellosis associated with beef jerky. MMWR 1995; Oct. 27; 44(42):785-788.) and two Salmonella strains were associated with orange juice that sickened people in Florida (See Cook KA, Dobbs TE, Hlady WG, et al. Outbreak of salmonella serotype Hartford infections associated with unpasteurized orange juice. JAMA 1999; 281(20):1892-1893.).
Pulsed field gel electrophoresis (PFGE) analysis of Salmonella javiana isolates was conducted at state public health laboratories and at the CDC. An indistinguishable pattern was found in isolates obtained from persons who had consumed tomatoes included as an ingredient on food prepared at Sheetz as well as in isolates obtained from persons who had consumed tomatoes at places other than Sheetz. In fact, Pennsylvania and Maryland reported more than 40 cases of individuals who were ill with the outbreak strain but did not eat tomatoes in food prepared at a Sheetz convenience store. These individuals were re-interviewed to determine the source of their exposure to the contaminated tomatoes.
By July 23, 2004, 289 cases of Salmonella had been reported in Pennsylvania, Ohio, Maryland, Virginia, and West Virginia. Both the PDOH and the FDA, working with the CDC, publicly identified the Roma tomatoes as the likely source of the outbreak. See PDOH Press Release, as Attachment No. 3.
On July 30, 2004, the PDOH issued a new Health Update regarding the outbreak. Over 300 cases had been reported in Pennsylvania, and dozens more in adjoining states. Salmonella javiana continued to be the serotype most commonly associated with the outbreak, but by then three additional human cases had tested positive for Salmonella anatum, the rare strain that had been identified in the case of unopened tomatoes distributed by Coronet Foods. The PDOH announced that similar multi-serotype Salmonella outbreaks were unusual, but certainly not unprecedented. See Health Update #05-04, Attachment No. 4.
The PDOH issued another related Health Update on August 6, 2004. By then, over 330 cases of Salmonella javiana had been recorded in Pennsylvania, and over 80 cases in neighboring states. See Health Update #06-04, as Attachment No. 5.
Preliminary data suggest that as many as 564 confirmed cases of salmonellosis associated with consumption of contaminated tomatoes were reported in five states, Pennsylvania, Maryland, Ohio, West Virginia, and Virginia. Seventy percent were associated with tomatoes in food prepared at Sheetz convenience stores. Dates of exposure ranged from July 2 to July 16. Five separate serotypes of Salmonella were eventually associated with the outbreak. Most of the cases were infected with Salmonella javiana; other outbreak associated strains were Salmonella typhimurium, Salmonella anatum, Salmonella Thompson, and Salmonella Muenchen.
FDA investigators traced the contaminated tomatoes back to farms in Florida and possibly South Carolina, but the investigators were also told that farms from five different states may have supplied tomatoes to Coronet Foods at relevant times. The FDA will continue its investigation in early 2005 to observe farm conditions during spring planting.
Prior Salmonella Outbreaks Associated with Tomatoes
Salmonella outbreaks have previously been associated with raw tomatoes, which accordingly should have been recognized as a potential source of contamination. In 1990, a reported 174 Salmonella javiana illnesses, as part of a four state outbreak, were linked to raw tomatoes. In 1993, 84 reported cases of Salmonella Montevideo were part of a three state outbreak that was linked to raw tomatoes.
More recently, in January 1999, Salmonella Baildon was recovered from 86 infected persons in eight states. Raw restaurant-prepared tomatoes were implicated in multiple case-controlled studies. Many restaurants across several states were involved, suggesting the tomatoes were likely contaminated early on, at the farm or during packing, and before distribution.
In July 2002, an outbreak of Salmonella javiana occurred associated with attendance at the 2002 U.S. Transplant Games held in Orlando, Florida during late June of that year. Ultimately, the outbreak investigation identified 141 ill persons in 32 states who attended the games. The epidemiological investigation implicated fresh, pre-packaged, and diced Roma tomatoes as the probable vehicle for the outbreak.
During August and September 2002, a Salmonella Newport outbreak affected the East Coast. Ultimately, over 404 confirmed cases were identified, in over 22 states. Epidemiological analysis indicated that tomatoes were the most likely vehicle, and were traced back to the same tomato packing facility in the mid-Atlantic region. Inspections of that packing facility revealed numerous violations of the Good Agricultural Practices and Good Manufacturing Practices published by the FDA.
In fact, Salmonella bacteria can grow on tomato skin surfaces and infiltrate core tissues during tomato harvest, packing, and transportation. Dicing and pooling of contaminated tomatoes may play a role in further amplifying the amount of contaminated product. Contamination of internal tissue from the outer skin and stem scar can also occur during cutting and slicing. Finally, many Salmonella strains grow rapidly in cut tomatoes held at room temperature, enhancing the risk if tomatoes are maintained at room temperature for extended periods.