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Outbreak of Salmonella enteritidis Infection Associated with Consumption of Raw Shell Eggs, 1991

Salmonella enteritidis (SE) is the most frequently reported Salmonella serotype in the United States. From January through December 1991, state health departments reported 66 outbreaks of SE in the United States to CDC. This report describes an SE outbreak associated with consumption of raw shell eggs and underscores the necessity of adequately cooking shell eggs.

During October 1991, 15 persons who ate at a restaurant during a 9-day period developed gastroenteritis. A case was defined as a positive culture for SE in a person who had eaten at the restaurant during October 17-25 and/or diarrhea and vomiting that developed within 3 days of eating at the restaurant on those dates. Predominant symptoms were diarrhea (100%), fever (92%), abdominal cramping (92%), nausea (83%), and chills (75%). The median incubation period was 24 hours (range: 12-48 hours); median duration of illness was 7 days (range: 4-10 days). Thirteen ill patrons sought medical care, eight required intravenous rehydration, and six were hospitalized. Salmonella group D was isolated from stool of all 13 ill patrons who submitted specimens; all of the eight isolates further typed were identified as SE. Fourteen of the 15 ill patrons and none of 11 well patrons interviewed had eaten Caesar salad (Yates corrected chi-square, p less than 0.01). Illness was not associated with consumption of any of the restaurant's other uncooked egg dishes.

During the outbreak, 23 (29%) of the restaurant's 78 employees had onset of gastroenteritis. Predominant symptoms were diarrhea (100%), abdominal cramps (70%), chills (61%), nausea (57%), and fever (52%). Median duration of illness was 5 days. Two employees sought medical care; neither was hospitalized. Of the 66 employees for whom cultures were obtained, SE was isolated from stool samples of 15 (68%) of the 22 ill employees and six (14%) of 44 asymptomatic employees. Stool specimens from all three employees who reported eating Caesar salad during the outbreak were culture-positive for SE; however, most (18 (86%) of 21) culture-positive employees did not report eating this food. Confirmed SE infection among employees was associated with exposure to raw eggs at the restaurant through consumption or handling. Employees with confirmed SE infection were more likely than those not confirmed (i.e., culture-negative or not cultured) to have eaten the restaurant's raw egg dishes (six (50%) of 12 versus seven (18%) of 40; odds ratio (OR)=4.7; 95% confidence interval (CI)=1.0-24.2), or to have handled raw eggs in the restaurant kitchen (seven (54%) of 13 versus five (17%) of 38; OR=7.7; 95% CI=1.5-42.8).

The Caesar salad dressing was prepared early in the morning by combining 36 yolks from hand-cracked eggs with olive oil, anchovies, garlic, and warm water. Neither lemon juice nor vinegar were included in the recipe. Batches of Caesar dressing were prepared daily except for one 3-day period when a single batch was used. The dressing was refrigerated until the restaurant opened, when it was placed in a chilled compartment in the salad preparation area for approximately 8-12 hours until the restaurant closed. By the time a restaurant inspection was conducted, the restaurant had eliminated Caesar salad from the menu. However, at the time of the inspection, the temperature of other salad dressings present in this compartment was 60 F (15.6 C).

The restaurant obtained eggs from a single supplier twice weekly and stored them in a walk-in refrigerator until use. No eggs from the shipment implicated in the outbreak were available for testing at the time of the restaurant inspection, but three cases of eggs from a different shipment from the same supplier were available. Two pools of 10 eggs each from each of the three cases were sampled and submitted for culture. SE was isolated from one of the six pools. Phage typing of the SE isolate from the eggs and of one from an ill employee revealed that both were phage type 8. A traceback by the SE Task Force, U.S. Department of Agriculture (USDA), determined that the source flock for eggs used during the outbreak was the same flock from which the SE-positive eggs were obtained. The flock had been destroyed before recognition of the outbreak.

Reported by: Enteric Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

Editorial Note

Editorial Note: From 1976 through 1990, isolation rates for SE increased in the United States (Figure 1). In 1990, the 8591 SE isolates reported through CDC's Salmonella Surveillance System represented 21% of all reported Salmonella isolates, surpassing S. typhimurium to become the most frequently reported serotype.

During 1985-1991, state and territorial health departments reported 375 SE outbreaks, which accounted for 12,784 cases of illness, 1508 hospitalizations, and 49 deaths (Table 1). Most SE outbreaks have historically occurred in the New England and mid-Atlantic states; however, in 1991, 39 (59%) of the 66 reported outbreaks occurred outside these areas.

An estimated 0.01% of all shell eggs contain SE; however, this percentage may be higher in the northeastern United States (1). Consequently, foods containing raw or undercooked eggs (e.g., homemade eggnog or ice cream, hollandaise sauce, and Caesar salad dressing) pose a small risk for infection with SE. Because most serious illnesses or deaths associated with these infections occur among infants, the elderly, or immunocompromised persons, special attention should be directed to the diets of these persons to prevent the consumption of foods containing raw or undercooked eggs. In contrast, commercial eggnog is made with pasteurized eggs and is safe.

Most cases of SE infection occur as sporadic cases or in limited family outbreaks, rather than as part of large common-source outbreaks. Many sporadic cases are caused by the same phage types as egg-associated outbreaks and are likely to have the same source (2). However, when commercial kitchens serve foods made with contaminated eggs that have not been sufficiently cooked to kill Salmonella, large numbers of persons may potentially become infected. The outbreak described in this report may be the first time SE infection has been documented as a potential occupational hazard for employees preparing raw egg dishes in restaurants. Commercial food-service establishments can reduce the risk for outbreaks and infections among employees by using pasteurized egg products or eliminating eggs in such recipes. Infections acquired by eating foods prepared in the kitchens of private homes can be reduced through improved education of consumers regarding the risks for eating raw or undercooked eggs and through increased availability of pasteurized eggs in the retail marketplace.

To address concerns regarding the SE infection issue and consumption of contaminated shell eggs, both USDA and the Food and Drug Administration have implemented a series of control measures. Beginning in February 1990, USDA began investigating egg-laying flocks whose eggs are epidemiologically implicated in human SE outbreaks. Eggs from flocks infected with SE (by culture of the flock environment and internal organs of hens) are diverted to pasteurization or the flocks are voluntarily destroyed. In 1991, Congress enacted legislation that mandates refrigeration of eggs during interstate shipping. These efforts are part of the concerted effort needed to ensure safe eggs for consumers. Commercial food-service establishments can reduce the risk for foodborne SE illness if they substitute pasteurized eggs for pooled eggs whenever possible, serve pooled egg dishes immediately after cooking, and do not serve foods containing raw or undercooked eggs.

References

  1. Mason J, Ebel E. APHIS Salmonella enteritidis control program (Abstract). In: Snoeyenbos GH, ed. Proceedings of the Symposium on the Diagnosis and Control of Salmonella. Richmond, Virginia: US Animal Health Association, 1992:78.

  2. Rodrigue DC, Cameron DN, Puhr ND, et al. Comparison of plasmid profiles, phage types, and antimicrobial resistance patterns of Salmonella enteritidis isolates in the United States. J Clin Microbiol 1992;30:854-7.

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