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Outbreaks of Salmonella Serotype Enteritidis Infection

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Outbreaks of Salmonella Serotype Enteritidis Infection
A Salmonella serotype Enteritidis (SE) epidemic emerged in the 1980s, when increasing numbers of infections were detected in the Northeastern and Mid-Atlantic regions of the United States. In the early 1990s, while SE rates in the Northeast began to decline, the SE epidemic expanded to the Pacific region. Nationwide, the number of SE isolates reported to CDC peaked at 3.8 per 100,000 population in 1995. Although rates of culture-confirmed SE infection reported to CDC declined to 1.9 by 1999 (Figure 1), rates did not decline further through 2001, and outbreaks continue to occur. Investigations of outbreaks and sporadic cases have indicated repeatedly that, when a food vehicle is identified, the most common sources of SE infection are undercooked and raw shell eggs. This report describes two SE outbreaks associated with eating shell eggs and underscores the need to strengthen SE-control measures.



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During February-March 2001, outbreaks of gastroenteritis occurred among inmates in four prison facilities of the South Carolina Department of Corrections (SCDC). The first outbreak occurred in a men's facility (M1) on February 6. The three other outbreaks, all occurring on March 2, affected a second men's facility (M2) and two women's facilities (F1 and F2). Among 2,317 inmates in the four prisons, 688 reported to prison infirmaries with gastrointestinal symptoms (e.g., abdominal cramps, diarrhea, and nausea). Stool specimens from ill inmates yielded SE phage types 2, 13a, and 23. No illness was reported among SCDC staff members.

The South Carolina Department of Health and Environmental Control conducted two case-control studies in M2 and F1, which shared a common kitchen. A case-patient was defined as any SCDC inmate who reported to the prison infirmary with acute gastrointestinal symptoms. Case-patients were selected at random from a list of ill inmates. Controls were inmates without illness who were selected at random from an inmate roster provided by the prisons and who were matched by prison facility. A tuna salad served for lunch on March 2 was eaten by 88% of the male case-patients (odds ratio [OR]=7.0; 95% confidence interval [CI]=1.8-30.5) and by 89% of the female case-patients (OR=16.7; 95% CI=4.1-74.7). The tuna salad was prepared with eggs that were reportedly hard-boiled by kitchen staff, who also were inmates. At the time of the outbreaks, all eggs used by the four involved SCDC facilities were supplied from a single vendor. Eggs supplied to M2 and F1 were traced back to the vendor's farm (Farm A). In February 2001, eggs submitted from Farm A to the South Carolina Egg Quality Assurance Program tested positive for SE phage types 2,13a, 22, 23, and 28. Phage type 2 was the predominant SE strain isolated from both ill patients and eggs from Farm A. To protect the inmates, SCDC switched to pasteurized egg products in April 2001.

In June 2001, the Statistical Outbreak Detection Algorithm at CDC signaled an increase in SE cases reported from North Carolina. The Division of Public Health in North Carolina was alerted and began to review SE cases throughout the state. The North Carolina State Laboratory of Public Health reported 51 cases in July and 31 in August, compared with 11 cases in each of those months during 2000. Cases occurred throughout the state.

A case-control study was performed. A case was defined as culture-confirmed SE in a resident of North Carolina reported during July 1-September 7, 2001. One to two neighbor controls were matched to each case. SE isolates were subtyped by pulsed-field gel electrophoresis (PFGE) and phage typing. Analysis of 53 patients and 78 controls indicated that illness was associated with eating eggs (matched odds ratio [MOR]=2.8; 95% CI=1.1-9.5). Isolates from 21 (40%) of 53 patients had PFGE pattern A. Analysis restricted to patients with pattern A indicated a stronger association with egg consumption (MOR=10.7; 95% CI=1.3-88.1). PFGE pattern A also was identified in isolates from patients in the South Carolina SE outbreak. All isolates from SE patients in both outbreaks that were PFGE pattern A also were phage type 13a. Among 14 random, nonoutbreak phage type 13a SE isolates tested subsequently at CDC, seven distinct PFGE patterns were identified; none was PFGE pattern A. A traceback of implicated eggs purchased from retail outlets in North Carolina was inconclusive for implicating a farm.

Reported by:D Drociuk, MSPH, S Carnesale, MD, G Elliot, LJ Bell, MD, JJ Gibson, MD, South Carolina Dept of Health and Environmental Control. L Wolf, D Briggs, B Jenkins, JM Maillard, MD, North Carolina Dept of Health and Human Svcs. M Huddle, MPH, F Virgin, C Braden, MD, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; P Srikantiah, MD, A Stoica, MD, T Chiller, MD, EIS officers, CDC.

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