Salmonella Serotype Typhimurium Outbreak Associated with Commercially Processed Egg Salad --- Oregon, 2003

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, hard-boiled 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 had 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] = ∞; 95% confidence interval [CI] = 0.9--∞; p=0.031). All eight patients and two controls reported eating delicatessen items from supermarket chain A (mOR = ∞; CI = 0.9--∞; p=0.063); seven of the eight patients and no controls reported eating egg salad from the delicatessen (mOR = ∞; CI = 1.44--∞; 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 before consumption. Supermarket chain A was the only customer for egg salad kits produced by vendor A.

Vendor A supplied its egg salad kits to supermarket chain A distribution centers in Arizona, California, Colorado, Oregon, and Washington. However, no case-patients in states other than Oregon and Washington were identified by review of PulseNet, communication with neighboring states, or via postings on Epi-X^†. A spring 2004 query of PulseNet revealed that four S. Typhimurium isolates from Arizona that matched the outbreak pattern had been collected during September 14--24, 2003, but had not been assigned a pattern designation until November 21. In May, Arizona Department of Health Services could not locate three of these patients; the fourth did not recall eating egg salad.

Although the isolates from Arizona suggest more widespread distribution of contaminated product, at the time of the investigation, all patients appeared to have eaten egg salad provided to supermarket chain A by a single distribution center in Oregon. No unopened samples of lots distributed through this center were available for testing. Testing with ELISA detected no Salmonella antigen in either of the leftover egg salad samples obtained from patient households. Salmonella serotype Heidelberg was cultured from cooked egg yolk obtained at a distribution center in Washington. Salmonella serotype Braenderup was cultured from samples submitted by vendor A to a private laboratory. Vendor A voluntarily discontinued production of egg salad kits.

Reported by: WE Keene, PhD, K Hedberg, MD, P Cieslak, MD, Acute and Communicable Disease Program, Oregon Health Svcs. S Schafer, MD, A Dechet, MD, EIS officers, CDC.

Editorial Note:

Each year in the United States, salmonellosis causes approximately 1.3 million cases of foodborne illness, 15,000 hospitalizations, and 500 deaths (1). S. Typhimurium, the most common serotype, represented 22% of human Salmonella isolates reported to CDC in 2002 (2). Contaminated eggs have been implicated as the vehicle in many Salmonella outbreaks (3). Salmonella serotype Enteritidis has been most commonly linked with shell eggs, but S. Typhimurium also has been the cause of numerous outbreaks (4) and might be just as likely as S. Enteritidis to colonize the reproductive tracts of chickens and eggs forming in the oviduct (5). Sporadic cases in Minnesota also have been linked to egg consumption (6). Although industry control measures have reduced overall egg contamination, S. Enteritidis still is found in approximately one in 20,000 eggs (7).

In this outbreak, S. Typhimurium was not found in cooked and packaged egg yolks and whites or in egg salad samples, and the specific mechanism of contamination remains undetermined. However, potential contributing causes could be inadequate cooking of the eggs, improper cooling of cooked eggs, or improper employee handling practices that allowed for recontamination of cooked eggs. Discovery of two other Salmonella serotypes in unopened packages in distribution centers suggests quality-control problems at the plant of vendor A.

Salmonella can survive inadequate cooking of eggs (8). Cooked eggs were implicated in a restaurant-associated S. Enteritidis outbreak in California (9). The Oregon outbreak in this report is the first in which a commercially processed, widely distributed hard-boiled egg product was identified as the vehicle for salmonellosis.

To avoid the possibility of foodborne illness, fresh eggs should be stored at <45^ºF (<7^ºC). Eggs should be cooked until both the yolk and white are firm. Recipes containing eggs mixed with other foods should be cooked to an internal temperature of 160^ºF (71^ºC). In addition, pasteurized egg products should be substituted for raw eggs in dishes served without further cooking and care taken to prevent cross-contamination with raw eggs during preparation (10).

This investigation implicated egg salad kits from vendor A, contaminated before their distribution, as the common source of the outbreak. Public health surveillance led to rapid detection and investigation of the outbreak and to voluntary discontinuance of egg salad kit production by vendor A, likely preventing additional illness. Consumers and food producers should be reminded that eggs need to be stored properly and cooked thoroughly.

Acknowledgments

J Bancroft, MPH, E DeBess, DVM, C Franzini, MD, Oregon Health Svcs. G Briggs, Arizona Dept of Health Svcs. MS Van Duyne, MA, D Sheehan, MS, J Lockett, J Painter, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

References

1. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607--25.
2. CDC. Salmonella surveillance: annual summary, 2002. Atlanta, GA: US Department of Health and Human Services, CDC; 2003.
3. Tauxe RV, Pavia AT. Salmonellosis: nontyphoidal (Chapter 31). In: Evans AS, Brachman PS, eds. Bacterial infections of humans, epidemiology and control. 3rd ed. New York, NY: Plenum Medical Book Co.;1998:613--30.
4. St Louis ME, Morse DL, Potter ME, et al. The emergence of grade A eggs as a major source of Salmonella Enteritidis infections: new implications for the control of salmonellosis. JAMA 1988;259:2103--7.
5. Keller LH, Schifferli DM, Benson CE, Aslam S, Eckroade RJ. Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella Enteritidis. Avian Dis 1997;41:535--9.
6. Hedberg CW, David MJ, White KE, MacDonald KL, Osterholm MT. Role of egg consumption in sporadic Salmonella Enteritidis and Salmonella Typhimurium infections in Minnesota. J Infect Dis 1993;167:107--11.
7. US Department of Agriculture. Salmonella Enteritidis risk assessment: shell eggs and egg products. Washington, DC: US Department of Agriculture, Food Safety and Inspection Service; 1998. Available at http://www.fsis.usda.gov/ophs/risk.
8. Humphrey TJ, Greenwood M, Gilbert RJ, Rowe B, Chapman PA. The survival of salmonellas in shell eggs cooked under simulated domestic conditions. Epidemiol Infect 1989;103:35--45.
9. CDC. Outbreaks of Salmonella Enteritidis gastroenteritis---California, 1993. MMWR 1993;42:793--7.
10. Food and Drug Administration. Food safety facts for consumers: playing it safe with eggs. Rockville, MD: US Department of Health and Human Services, Food and Drug Administration, Center for Food Safety and Applied Nutrition; 2001. Available at http://www.cfsan.fda.gov/~dms/fs-eggs.html.

^† The Epidemic Information Exchange is a web-based communications network (available at http://www.cdc.gov/epix) enabling the secure exchange of information among epidemiologists, laboratorians, and other public health professionals at CDC and state and local agencies.

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