Salmonella enteritidis

Related Key Words and Synonyms:

Overview
Egg-associated salmonellosis is an important public health problem in the United States and several European countries. A bacterium, Salmonella enteritidis, can be inside perfectly normal-appearing eggs, and if the eggs are eaten raw or undercooked, the bacterium can cause illness. During the 1980s, illness related to contaminated eggs occurred most frequently in the northeastern United States, but now illness caused by S. enteritidis is increasing in other parts of the country as well. Consumers should be aware of the disease and learn how to minimize the chances of becoming ill.

A person infected with the Salmonella enteritidis bacterium usually has fever, abdominal cramps, and diarrhea beginning 12 to 72 hours after consuming a contaminated food or beverage. The illness usually lasts 4 to 7 days, and most persons recover without antibiotic treatment. However, the diarrhea can be severe, and the person may be ill enough to require hospitalization.

The elderly, infants, and those with impaired immune systems may have a more severe illness. In these patients, the infection may spread from the intestines to the blood stream, and then to other body sites and can cause death unless the person is treated promptly with antibiotics.

Epidemiology and Demographics
During the 1980s, illness related to contaminated eggs occurred most frequently in the northeastern United States, but now illness caused by S. enteritidis is increasing in other parts of the country as well. Consumers should be aware of the disease and learn how to minimize the chances of becoming ill.

Who can be infected?

The elderly, infants, and persons with impaired immune systems are at increased risk for serious illness.

Healthy adults and children are at risk for egg-associated salmonellosis, but the elderly, infants, and persons with impaired immune systems are at increased risk for serious illness. In these persons, a relatively small number of Salmonella bacteria can cause severe illness. Most of the deaths caused by Salmonella enteritidis have occurred among the elderly in nursing homes. Egg-containing dishes prepared for any of these high-risk persons in hospitals, in nursing homes, in restaurants, or at home should be thoroughly cooked and served promptly.

Risk Factors
What is the risk?

In affected parts of the United States, we estimate that one in 50 average consumers could be exposed to a contaminated egg each year. If that egg is thoroughly cooked, the Salmonella organisms will be destroyed and will not make the person sick. Many dishes made in restaurants or commercial or institutional kitchens, however, are made from pooled eggs. If 500 eggs are pooled, one batch in 20 will be contaminated and everyone who eats eggs from that batch is at risk. A healthy person's risk for infection by Salmonella enteritidis is low, even in the northeastern United States, if individually prepared eggs are properly cooked, or foods are made from pasteurized eggs.

Pathophysiology & Etiology
A bacterium, Salmonella enteritidis, can be inside perfectly normal-appearing eggs, and if the eggs are eaten raw or undercooked, the bacterium can cause illness.

How eggs become contaminated:

Unlike eggborne salmonellosis of past decades, the current epidemic is due to intact and disinfected grade A eggs. Salmonella enteritidis silently infects the ovaries of healthy appearing hens and contaminates the eggs before the shells are formed.

Most types of Salmonella live in the intestinal tracts of animals and birds and are transmitted to humans by contaminated foods of animal origin. Stringent procedures for cleaning and inspecting eggs were implemented in the 1970s and have made salmonellosis caused by external fecal contamination of egg shells extremely rare. However, unlike eggborne salmonellosis of past decades, the current epidemic is due to intact and disinfected grade A eggs. The reason for this is that Salmonella enteritidis silently infects the ovaries of healthy appearing hens and contaminates the eggs before the shells are formed.

Although most infected hens have been found in the northeastern United States, the infection also occurs in hens in other areas of the country. In the Northeast, approximately one in 10,000 eggs may be internally contaminated. In other parts of the United States, contaminated eggs appear less common. Only a small number of hens seem to be infected at any given time, and an infected hen can lay many normal eggs while only occasionally laying an egg contaminated with the Salmonella bacterium.

Natural History
Summary of Salmonella serotype Enteritidis Outbreaks Reported to the CDC in 2001

State and local health departments reported 46 confirmed outbreaks of Salmonella serotype Enteritidis (SE) infection to CDC for calendar year 2001. These outbreaks resulted in 1681 reported illnesses, 102 hospitalizations and no deaths among residents of 23 states (Table). Compared with 2000 data, there were 4 fewer outbreaks, 49 fewer hospitalizations, and 720 more illnesses in 2001. The median number of cases per outbreak was 10 in 2001, compared with 6 in 2000.

A suspected food vehicle was identified for 29 (63%) of 46 outbreaks; 24 of these were confirmed by culture or statistical association. Eggs were an ingredient in 15 (63%) of 24 confirmed vehicles, including meringue pie, home-made ice cream, and butter. In addition, eggs were an ingredient in one (20%) outbreak in which the suspected food item was not confirmed. Between 1993 and 1999, an average of 80% of vehicleconfirmed outbreaks have been egg-associated.

Outbreaks reported in the Mountain and Pacific states decreased from 22 in 1999 to six in 2001. Although the precise reason for the decrease in both regions is unclear, it may be a combination of increased participation in egg quality assurance programs on farms, improvements in egg preparation practices, and food handler education.

Summary of Salmonella serotype Enteritidis Outbreaks Reported to the CDC in 1999

As of March 1, 2000, 44 confirmed outbreaks of Salmonella serotype Enteritidis were reported in 1999, affecting U.S. residents in 17 states (Table). Of the 1,080 ill persons, 63 (6%) were hospitalized, and none died. Although the total number of SE outbreaks reported in 1999 is similar to the number reported in 1998, there were approximately twice as many illnesses. The median number of cases per outbreak was 15 in 1999.

Of the 19 outbreaks in 1999 for which a vehicle could be confirmed, 15 (79%) were associated with shell eggs; implicated vehicles included lasagna, ice cream, tira misu, stuffing, and manicotti. Between 1993 and 1998, an average of 82% of vehicle-confirmed outbreaks have been egg-associated.

Twenty-two (50%) of the 44 outbreaks occurred in commercial food establishments (e.g., restaurants, delis, bakeries, caterers), compared with 198 (63%) between 1993 and 1998 (Table). Six (14%) outbreaks occurred in college campuses or schools (e.g., preschools, elementary schools), compared with 3% from 1993 to 1998. Two (5%) of outbreaks occurred in nursing homes in 1999, compared with 5% from 1993 to1998.

SE phage type 4 continued to emerge, causing an increase in sporadic illness in the western United States. Of the 37 outbreaks for which an isolate was submitted to CDC for phage typing, 18 (49 %) were caused by SE PT 4 (Table). Of these, 14 (78%) occurred in California, two in Utah, and one each in Hawaii and Virginia. Although most outbreak investigations and studies of sporadic illness due to SE phage type 4 in the United States have implicated eggs, in Europe SE phage type 4 is also transmitted by eating chicken. In the United States in 1999, two vehicleconfirmed outbreaks and one outbreak in which the vehicle was suspected but not confirmed were associated with eating chicken.

Phage type 8 accounted for 4 (11%) of the 37 SE outbreaks in 1999 for which isolates were submitted; of these, 2 occurred in eastern states with the other two occurring in Wisconsin and Michigan. Phage type 13a caused 4 (11%) of the SE outbreaks, and phage type 2, rare in the United States, was responsible for 4 (11%) outbreaks.

While the number of SE outbreaks in the New England and Mid-Atlantic states decreased from 42 in 1992 to 9 in 1999, the number reported by the Mountain and Pacific states increased from 3 in 1992 to 22 in 1999. Although the precise reason for the decrease in the northeastern states is unclear, it may be a combination of increased participation in egg quality assurance programs on farms, improvements in egg preparation practices, and food handler education.

Summary of Salmonella serotype Enteritidis Outbreaks Reported to the CDC in 1998

As of March 1, 1999, 45 confirmed outbreaks of SE were reported, affecting U.S. residents in 19 states (Table). Of the 666 ill persons, 90 (14%) were hospitalized, and 3 died. Although the total number of SE outbreaks reported in 1998 is similar to the number reported in 1997, there were approximately half as many illnesses. This continues a recent trend whereby the median number of cases per outbreak has decreased from 17 in 1993 to 10 in 1998.

Of the 18 outbreaks in 1998 for which a vehicle could be confirmed, 15 (83%) were associated with eggs; implicated vehicles included chiles rellenos, homemade ice cream, lasagna, stuffing, tira misu, and ziti. Between 1993 and 1997, an average of 80% of vehicle-confirmed outbreaks have been egg-associated, with a range of 68%-95%.

Twenty-three (51%) of the 45 outbreaks occurred in commercial food establishments (e.g. restaurants, delis), compared with 31 (70%) in 1997 (Table). Twelve (27%) of outbreaks occurred in private homes, compared with 7 (16%) in 1997. Three (6%) of outbreaks and all of the reported deaths occurred in nursing homes in 1998, compared with one nursing home outbreak and no associated deaths in 1997.

SE phage type 4 continues to emerge, causing an increase in sporadic illness in the western United States. Of the 30 outbreaks for which an isolate was submitted to CDC for phage typing, 15 (50%) were SE PT 4 (Table). Of these, 11 (73%) occurred in California, two in Utah, and one each in Hawaii and Wyoming. Although most outbreak investigations and studies of sporadic illness due to SE phage type 4 in the United States have implicated eggs, in Europe SE phage type 4 is also transmitted by eating chicken. In the United States in 1998, one vehicle-confirmed outbreak and two outbreaks in which the vehicle was suspected but not confirmed were associated with eating chicken.

Phage type 8 accounted for 4 (14%) of 29 SE outbreaks in 1998; of these, 3 (75%) occurred in eastern states. Phage type 13a caused 6 (21%) of the SE outbreaks, and phage type 6a, rare in the United States, was responsible for 2 (7%) outbreaks.

While the number of SE outbreaks in the New England and Mid-Atlantic states decreased from 42 (67%) of 63 reported outbreaks in 1992 to 8 (18%) of 45 SE outbreaks in 1998, the number reported by the Mountain and Pacific states increased from 3 (5%) in 1992 to 23 (51%) in 1998. Although the precise reason for the decrease in the northeastern states is unclear, it may be a result of increased participation in egg quality assurance programs on farms and improvements in egg preparation practices.

The high incidence of SE infections, as well as the association of SE with foods containing raw or lightly cooked eggs, highlights the importance of conducting timely egg tracebacks to prevent SE outbreaks. To this end, CDC’s Foodborne and Diarrheal Diseases Branch requests notification of SE outbreaks and outbreaks of group D Salmonella infections as soon as health departments become aware of them, regardless of whether or not a vehicle has been implicated. This preliminary notification need not be in the form of a final report. Early notification of possible egg-associated outbreaks will allow FDA and/or the Department of Agriculture in your state to prepare to conduct rapid tracebacks. See Appendix for detailed guidelines on investigating SE outbreaks.

History and Symptoms
A person infected with the Salmonella enteritidis bacterium usually has fever, abdominal cramps, and diarrhea beginning 12 to 72 hours after consuming a contaminated food or beverage. The illness usually lasts 4 to 7 days, and most persons recover without antibiotic treatment. However, the diarrhea can be severe, and the person may be ill enough to require hospitalization.

Primary Prevention
What you can do to reduce risk:

Eggs, like meat, poultry, milk, and other foods, are safe when handled properly. Shell eggs are safest when stored in the refrigerator, individually and thoroughly cooked, and promptly consumed. The larger the number of Salmonella present in the egg, the more likely it is to cause illness. Keeping eggs adequately refrigerated prevents any Salmonella present in the eggs from growing to higher numbers, so eggs should be held refrigerated until they are needed. Cooking reduces the number of bacteria present in an egg; however, an egg with a runny yolk still poses a greater risk than a completely cooked egg. Undercooked egg whites and yolks have been associated with outbreaks of Salmonella enteritidis infections. Both should be consumed promptly and not be held in the temperature range of 40 to 140 for more than 2 hours.

Reducing the risk of Salmonella enteritidis infection: 


 * Keep eggs refrigerated.
 * Discard cracked or dirty eggs.
 * Wash hands and cooking utensils with soap and water after contact with raw eggs.
 * Eat eggs promptly after cooking. Do not keep eggs warm for more than 2hours.
 * Refrigerate unused or leftover egg- containing foods.
 * Avoid eating raw eggs (as in homemade ice cream or eggnog). Commercially manufactured ice cream and eggnog are made with pasteurized eggs and have not been linked with Salmonella enteritidis infections.
 * Avoid restaurant dishes made with raw or undercooked, unpasteurized eggs. Restaurants should use pasteurized eggs in any recipe (such as Hollandaise sauce or caesar salad dressing) that calls for pooling of raw eggs.

Secondary Prevention
Government agencies and the egg industry have taken steps to reduce Salmonella enteritidis outbreaks. These steps include the difficult task of identifying and removing infected flocks from the egg supply and increasing quality assurance and sanitation measures.

The Centers for Disease Control has advised state health departments, hospitals, and nursing homes of specific measures to reduce Salmonella enteritidis infection. Some states now require refrigeration of eggs from the producer to the consumer. The U.S. Department of Agriculture is testing the breeder flocks that produce egg-laying chickens to ensure that they are free of Salmonella enteritidis. Eggs from known infected commercial flocks will be pasteurized instead of being sold as grade A shell eggs. The U.S. Food and Drug Administration has issued guidelines for handling eggs in retail food establishments and will be monitoring infection in laying hens.

Research by these agencies and the egg industry is addressing the many unanswered questions about Salmonella enteritidis, the infections in hens, and contaminated eggs. Informed consumers, food-service establishments, and public and private organizations are working together to reduce, and eventually eliminate, disease caused by this infectious organism.

Acknowledgements
The content on this page was first contributed by: C. Michael Gibson, M.S., M.D.