Salmonella serotype Typhimurium outbreak associated with commercially processed egg salad—Oregon, 2003

Morbidity and Mortality Weekly Report, Dec 10, 2004 by W.E. Keene, K. Hedberg, P. Cieslak, S. Schafer, A. Dechet

On September 24, 2003, Oregon epidemiologists noted an increase in Salmonella enterica serotype Typhimurium isolates tested during September at the Oregon State Public Health Laboratories. Of 16 isolates, six had matching pulsed-field gel electrophoresis (PFGE) patterns. The laboratory findings prompted an investigation by Oregon Health Services and CDC that identified 18 cases of infection with S. Typhimurium linked to kits for making egg salad that were distributed by a vendor to a supermarket chain. The Food and Drug Administration (FDA) conducted an environmental investigation but was unable to determine the mechanism of contamination. This was the first reported S Typhimurium outbreak associated with a commercially processed, widely distributed, hardboiled egg product. Epidemiologists and other public health staff-should continue to investigate apparent clusters of salmonellosis and be aware that even commercially processed egg products can be a source of Salmonella.

An outbreak-associated case was defined as diarrheal illness in an Oregon or Washington resident during September-October 2003 with a stool culture yielding S. Typhimurium with a PFGE pattern matching the outbreak pattern *. Local health department staff members in Oregon routinely interview patients with salmonellosis regarding high-risk exposures, date of illness onset, and severity of illness. Interviews usually are completed before serotyping. During September 25-26, a total of 11 (of 12) patients identified by September 25 were reinterviewed by using a more extensive questionnaire covering shopping and eating venues and consumption of approximately 400 foods. A matched case-control study also was conducted.

Results of the second questionnaire and a visit by investigators to a supermarket chain A outlet where patients had shopped were used to tailor a third and final questionnaire covering foods sold in the delicatessen section. This questionnaire was administered to eight of the 11 patients, along with eight controls matched to the patients by age group and telephone exchange. Patients were asked about their exposure to the delicatessen foods during the 5 days before their symptom onsets; controls were asked about their exposure to the delicatessen foods during the first 10 days of September. Odds ratios and Fisher exact p-values were calculated.

Egg salad found in the households of two patients was tested for salmonella by enzyme-linked immunosorbent assay (ELISA). Cooked and packaged egg yolks and whites were submitted by the producer of the egg-salad kit, vendor A, to a private laboratory for culture. FDA aggregated separate samples of cooked egg yolks, egg whites, and dressing from unopened packages collected at two distribution centers of supermarket chain A and cultured for Salmonella.

Eighteen persons with outbreak-associated S. Typhimurium infections were identified (Figure): 17 residents of Oregon and one resident of Washington who sought care in an Oregon hospital. Dates of symptom onset ranged from September 6 to September 26. The median age of patients was 36 years (range: 4-58 years). They resided in nine different counties; 11 were male. Ten patients reported bloody diarrhea; two were hospitalized but recovered and were discharged after 1 day and 3 days, respectively.

No common exposures were evident from the initial interviews, and no specific food item was implicated by the results of the second questionnaire administered to the 11 patients identified by September 25. However, 10 of those 11 patients reported shopping at various outlets of supermarket chain A, and seven of the 10 reported consuming items from the delicatessen section.

Of the eight patients participating in the case-control study, the first patient to be interviewed noted that egg salad, which the patient had purchased from the delicatessen of a supermarket chain A outlet, was absent from the list of foods in the questionnaire. Egg salad, which bad not been displayed for sale when investigators visited the delicatessen, was added to the questionnaire for all the interviews. Seven of the eight patients and three controls reported shopping at supermarket chain A (matched odds ratio [mOR] = [infinity], 95% confidence interval [CI] = 0.9-[infinity] p = 0.031). All eight patients and two controls reported eating delicatessen items from supermarket chain A (mOR = [infinity] CI = 0.9-[infinity], p = 0.063); seven of the eight patients and no controls reported eating egg salad from the delicatessen (mOR = [infinity], CI = 1.44-[infinity], p = 0.008). No other foods were associated with illness.

Supermarket chain A reported that its delicatessen egg salad was sold intermittently. Investigation by Oregon Health Services and FDA determined that kits for the egg salad were produced in a California plant operated by vendor A. At the plant, eggs were boiled and peeled, yolks and whites were chopped separately, and dressing was made from mayonnaise, pepper, and preservatives (i.e., sodium benzoate and potassium sorbate). The chopped egg whites, yolks, and dressing were sealed into separate plastic pouches and boxed together as kits. The egg salad was then prepared at individual stores by combining the contents of the pouches. Kits were stamped with a use-by date 40 days beyond the date of production at the plant. Ready-for-sale egg salad had a 3-day store shelf life. According to the dates that suspected kits were delivered from vendor A to the supermarket chain A distribution center, the eggs in the kits had been cooked 5-33 days befi3re consumption. Supermarket chain A was the only customer for egg salad kits produced by vendor A.