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From the Centers for Disease Control and Prevention
March 1, 2000

Outbreaks of Salmonella Serotype Enteritidis Infection Associated With Eating Raw or Undercooked Shell Eggs—United States, 1996-1998

JAMA. 2000;283(9):1132-1134. doi:10.1001/jama.283.9.1132

MMWR. 2000;49:73-79

2 figures, 1 table omitted

During the 1980s and 1990s, Salmonella serotype Enteritidis (SE) emerged as an important cause of human illness in the United States. The rate of SE isolates reported to CDC increased from 0.6 per 100,000 population in 1976 to 3.6 per 100,000 in 1996. Case-control studies of sporadic infections and outbreak investigations found that this increase was associated with eating raw or undercooked shell eggs.1 From 1996 to 1998, the rate of culture-confirmed SE cases reported to CDC declined to 2.2 per 100,000; however, outbreaks of illness caused by SE continue to occur. This report describes four SE outbreaks during 1996-1998 associated with eating raw or undercooked shell eggs and discusses measures that may be contributing to the decline in culture-confirmed SE cases.

Los Angeles County, California

In August 1997, the Los Angeles County Department of Health Services (LACDHS) received reports of gastrointestinal illness in members of a Girl Scout troop and some of their parents. The ill persons had eaten food prepared in a private residence by the scouts. Stool cultures taken from 12 ill persons yielded SE; selected isolates tested were phage type 4.

An investigation by LACDHS found that of 17 persons at the dinner, 13 had gastrointestinal illness consistent with salmonellosis. Cheesecake served at the dinner was associated with illness; all 13 ill persons and two well persons ate the cheesecake (attack rate = 87%; relative risk [RR] = undefined; p = 0.04). The cheesecake contained raw egg whites and egg yolks that were cooked in a double boiler until slightly thickened. California Department of Health Services and Department of Food and Agriculture investigated the farm that supplied the eggs and found SE contamination. Of 476 environmental cultures taken from manure, feed, and water, 21 (4.4%) yielded SE; all positive cultures were from manure. Nineteen isolates were phage type 4, and two were phage type 7. SE also was isolated from one (0.5%) of 200 pooled egg samples obtained at the farm. On the basis of these findings, the layer flock was depopulated to prevent further SE cases.

District of Columbia

In October 1997, the District of Columbia Bureau of Epidemiology and Disease Control (DCBEDC) received reports of gastroenteritis among 75 attendees at seven events (a workshop dinner, nursing home luncheon, and five meals in private residences) at which lasagna from the same commercial manufacturer was served. Forty-three cases of illness compatible with salmonellosis were identified among attendees. Stool cultures from nine patients yielded Salmonella group D or SE; at least one culture-confirmed case was associated with each event. Isolates tested from attendees at five events were phage type 8. Three patients were hospitalized; none died.

DCBEDC interviewed 48 of the 75 attendees. Of the 47 persons who ate lasagna at the events, 39 became ill; the only person who did not eat lasagna did not become ill (attack rate = 83%; RR = undefined; p = 0.19). Lasagna was not associated statistically with illness but was implicated because it was the only food item common to all events. Cultures of two leftover lasagnas and one lasagna made on the same day but not eaten yielded SE phage type 8. The lasagnas were prepared commercially by a company in Gaithersburg, Maryland, using fully cooked meat or spinach sauce and a mixture of raw shell eggs, ricotta and mozzarella cheeses, and spices. Although the lasagnas were not labeled with a manufacture date, investigators determined that most, if not all, of the lasagnas implicated were made on the same day from a single batch of the egg-cheese mixture. The product was then frozen (except for one event in which the lasagnas were kept refrigerated as a special order) and held without further cooking until purchased. In at least four of six events for which lasagnas were purchased frozen, the lasagna was not thawed before reheating.

A traceback investigation led to two egg processors. Sampling of the farms that supplied eggs to these processors showed that five of 13 poultry houses had environmental samples positive for SE. In compliance with recommendations from DCBEDC, the manufacturer voluntarily switched to using pasteurized eggs in egg-containing foods.

Clark County, Nevada

In November 1997, 91 persons who ate either of two meals served 2 weeks apart at a hotel restaurant in Las Vegas, Nevada, developed gastroenteritis. Fifteen patients were hospitalized; none died. Stool cultures taken from ill persons yielded SE; selected isolates tested were phage type 13A.

An investigation by the Clark County Health District found 28 culture-confirmed and 63 probable salmonellosis cases. A case was defined as diarrheal illness in a patient who ate at restaurant A on November 13 or November 27. Two separate case-control studies implicated broccoli with hollandaise sauce: one study among persons who ate at the restaurant on November 13 (odds ratio [OR] = 25.5; p = 0.04) and a second among persons who ate at the restaurant on November 27 (OR = 27.8; p = <0.001). Broccoli with hollandaise sauce was offered on a special menu that rotated biweekly. The hollandaise sauce was prepared from pooled shell eggs, cooked to a temperature inadequate to kill SE, and kept at room temperature for several hours until served.

Maricopa County, Arizona

In July 1998, 58 persons developed gastroenteritis associated with eating at any of four Mexican restaurants that were part of a local chain. Eleven persons were hospitalized; none died. Stool cultures taken from 22 persons yielded Salmonella group D or SE; selected isolates tested were phage type 6A.

An investigation by the Maricopa County Environmental Services Department found that 14 (64%) of the 22 persons with culture-confirmed infections had eaten chiles rellenos, a precooked commercial product. Cultures of chiles rellenos from all four restaurants yielded SE with the same phage type as the patient isolates. The chiles rellenos consisted of raw egg-white batter on roasted green chile peppers stuffed with cheese, and were commercially processed in Mexico where they were cooked, packed, and frozen. Local public health officials observed that the internal temperature of the chiles rellenos was not checked after reheating at the restaurants. Improper foodhandling and cross-contamination were presumed responsible for the other cases among persons who did not consume chiles rellenos. Cultures of chiles rellenos from other lots distributed in the United States also yielded SE. The distributor of the chiles rellenos voluntarily recalled all products.

Reported by:

R Reporter, MD, L Mascola, MD, Acute Communicable Disease Control Unit, L Kilman, Bacteriology Public Health Laboratory, A Medina, Food and Milk Program, Environmental Health Svcs, Los Angeles County Dept of Health Svcs, Los Angeles; J Mohle-Boetani, MD, J Farrar, DVM, D Vugia, MD, Acting State Epidemiologist, California Dept of Health Svcs. M Fletcher, PhD, M Levy, MD, Bur of Epidemiology and Disease Control, District of Columbia Dept of Health. O Ravenholt, MD, L Empey, D Maxson, P Klouse, A Bryant, Clark County Health District, Las Vegas; R Todd, DrPH, State Epidemiologist, Nevada State Health Div. M Williams, Maricopa County Health Dept, Phoenix; G Cage, MS, L Bland, MPH, Acting State Epidemiologist, Arizona Dept of Health Svcs. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; and EIS officers, CDC.

CDC Editorial Note:

SE was recognized as a public health problem in northeastern states during the 1980s and has since spread throughout the United States.1 During 1985-1998, state and territorial health departments reported 796 SE outbreaks that accounted for 28,689 illnesses, 2839 hospitalizations, and 79 deaths. Of the 360 SE outbreaks with a confirmed source, 279 (82%) were associated with raw or undercooked shell eggs. This report illustrates that outbreaks can occur because of breakdowns in procedures at multiple steps in egg production from farm to table. SE prevention measures include on-farm control programs, refrigeration, consumer and food worker education about food preparation and consumption, adoption of the Food and Drug Administration (FDA) Food Code2 in restaurants and institutions, and improved surveillance.

On-farm control measures may include actions resulting from egg traceback investigations and quality assurance programs (QAPs). When eggs are implicated in SE outbreaks, state health departments and/or FDA may conduct tracebacks to identify the source farm(s) and conduct environmental sampling of poultry houses to detect SE. When SE is detected in a house, eggs are voluntarily diverted to pasteurization facilities until egg testing has shown negative results for SE. Tracebacks have been successful in removing potentially contaminated eggs from the market. During the early 1990s, the U.S. Department of Agriculture (USDA), the egg industry, state departments of agriculture, and academia collaborated to design QAPs.3 Elements may include purchasing chicks from SE-monitored breeders, stringent rodent and pest control, cleaning and disinfecting hen houses, routine environmental cultures with diversion of eggs to pasteurization if SE is found, and proper refrigeration of eggs. Currently, 13 states participate in voluntary QAPs.4 Northeastern states were the first to implement such QAPs. The decrease in SE outbreaks from 61 in 1989 to eight in 1998, and in sporadic cases in the region may reflect these collaborative preventive efforts.

Ensuring that eggs are sold soon after being produced and that they are kept refrigerated are important steps in reducing egg-associated SE illness. Although required in 17 states, no federal law exists that requires an expiration or "sell-by" date on egg cartons. Currently, USDA requires that eggs be stored and transported at ≤45 F (≤7.2 C) and that consumer containers be labeled to indicate that refrigeration is required.5 A proposed rule scheduled to be finalized in 2000 by FDA also would require that eggs sold at retail stores be refrigerated at ≤45 F (≤7.2 C).6

The education of consumers and food service workers to store, handle, and cook eggs appropriately can prevent many SE infections in humans (see box). FDA has a proposed rule that would require safe handling messages on all egg cartons.6 FDA's Food Code for retail food stores, food service establishments, nursing homes, and day care centers recommends that pasteurized eggs be substituted for raw shell eggs in preparing foods such as Caesar salad, hollandaise sauce, ice cream, and egg-fortified beverages that are not cooked.2 The outbreaks described in this report could have been prevented if pasteurized eggs had been used or if the eggs used in the recipes had been cooked fully. FDA's Food Code recommendations are especially important for children, the elderly, immunocompromised persons, and pregnant women who are at increased risk for severe complications from SE infection. The effectiveness of these recommendations and education efforts are demonstrated by the decline in the number of deaths in health-care facilities, particularly nursing homes.

Throughout the 1980s, SE phage type 4 emerged as the predominant phage type in Europe, causing a marked increase in human infections. Phage type 4 had not been seen in the United States except among persons who became ill after international travel. In 1993, the first U.S. outbreak of SE phage type 4 infections occurred in Texas,7 and during the next several years, phage type 4 caused human illness in Arizona, California, Hawaii, Nevada, and Utah. Since then, the isolation rate and number of SE outbreaks in the western United States have increased dramatically; most of these outbreaks have been phage type 4. SE phage type 4 also has been isolated from eggs and the farm environment of laying flocks implicated as sources for human outbreaks in that region.8 CDC monitors the spread of phage type 4 by phage typing isolates from U.S. outbreaks of SE and sporadic cases.

Further reductions in SE incidence and SE-related outbreaks will require multiple interventions along the entire farm-to-table continuum. To address SE prevention issues, on December 10, 1999, the President's Council on Food Safety announced an Egg Safety Action Plan, which calls for a 50% reduction in egg-associated SE illnesses by 2005.9 The plan's objectives are aimed at reducing consumer exposure to SE-containing foods; expanding and upgrading surveillance systems for human and poultry SE infection; improving communication among federal, state, and local agencies to accelerate SE outbreak detection and initiation of investigations; conducting research; and educating persons using science-based materials.

Additional information about preventing SE infections associated with eating raw or undercooked shell eggs is available on the World-Wide Web at http://www.cdc.gov/ncidod/dbmd/diseaseinfo/salment_g.htm; http://vm.cfsan.fda.gov/~dms/fs-eggs.html; http://vm.cfsan.fda.gov/~dms/fs-eggs2.html; and http://www.foodsafety.gov/~fsg/ceggs.html.

References
1.
Angulo  FJSwerdlow  DL Salmonella Enteritidis infections in the United States. J Am Vet Med Assoc. 1998;2131729- 31
2.
Food and Drug Administration, Food code.  Washington, DC US Department of Health and Human Services, Food and Drug Administration1999;
3.
Hogue  AWhite  PGuard-Petter  J  et al.  Epidemiology and control of egg-associated Salmonella Enteritidis in the United States of America. Rev Sci Off Int Epiz. 1997;16542- 53
4.
US General Accounting Office, Food safety: U.S. lacks a consistent farm-to-table approach to egg safety.  Washington, DC US General Accounting Office1999;report no. GAO/RCED-99-184.
5.
Food Safety Inspection Service, Refrigeration and labeling requirements for shell eggs [Final rule]. Federal Register. 1998;6345663- 75
6.
Food and Drug Administration, Safe handling label statement and refrigeration at retail requirements for shell eggs [Proposed rule]. Federal Register. 1999;6436491- 516
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Boyce  TGKoo  DSwerdlow  DL  et al.  Recurrent outbreaks of Salmonella Enteritidis infections in a Texas restaurant: phage type 4 arrives in the United States. Epidemiol Infect. 1996;11729- 34Article
8.
Kinde  HRead  DHChin  RP  et al.  Salmonella Enteritidis phage type 4 infection in a commercial layer flock in southern California: bacteriologic and epidemiologic findings. Avian Dis. 1996;40665- 71Article
9.
President's Council on Food Safety, Egg safety from production to consumption: an action plan to eliminate Salmonella Enteritidis illnesses due to eggs.  Washington, DC President's Council on Food Safety1999;
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