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Outbreaks of Salmonella enteritidis Gastroenteritis -- California, 1993

Foodborne infections cause an estimated 6.5 million cases of human illness and 9000 deaths annually in the United States (1). Salmonella is the most commonly reported cause of foodborne outbreaks, accounting for 28% of such outbreaks of known etiology and 45% of outbreak-associated cases during 1973-1987 (2). During 1985-1992, state and territorial health departments reported 437 Salmonella enteritidis (SE) outbreaks (Table_1), which accounted for 15,162 cases of illness, 1734 hospitalizations, and 53 deaths. This report describes three SE outbreaks in California during a 4-month period in 1993. Outbreak 1: Los Angeles County

In January 1993, routine surveillance for salmonellosis identified four unrelated persons with gastroenteritis and stool cultures yielding SE who recently had eaten at a local restaurant; one person had been hospitalized. The mean period from eating at the restaurant to onset of illness was 20 hours (range: 11-24 hours); duration of symptoms ranged from 1 to 14 days. All four isolates were phage type 13a and plasmid profile type 2 (36 and 3.7 megadalton plasmids), an unusual pattern among SE isolates. All four ill persons reported having eaten an egg-based dish (omelette, scrambled eggs, or egg salad) at the restaurant during December 26, 1992-January 6, 1993.

An investigation by the Los Angeles County Department of Health Services involved the four reported cases, five well meal companions, and 100 restaurant patrons identified through credit card receipts; two additional cases were identified. A case was defined as onset of diarrhea (three or more loose stools in a 24-hour period) plus fever, abdominal cramps, nausea, and/or vomiting within 3 days after eating at the restaurant. Five of the six case-patients had eaten an egg-based dish, compared with 16 (16%) of 103 well persons (odds ratio {OR}=27.2; 95% confidence interval {CI}=2.7-1300); no other food was associated with illness.

Inspection of the restaurant revealed that egg salad was stored on a cold table at a holding temperature of 60 F (15.5 C), a temperature that allows growth of Salmonella. For pooled egg dishes, 22-30 dozen extra-large grade AA eggs were pooled several times daily and stored in a walk-in refrigerator. A 2-quart container of pooled eggs was stored in a reach-in refrigerator. The temperature of the pooled eggs in the reach-in refrigerator was 50 F (10 C); California regulations require eggs to be refrigerated at less than or equal to 45 F ( less than or equal to 7.2 C).

In February, cultures of swabs of utensils used for pooling and storing the eggs were negative for SE, and rectal swabs obtained from all 43 food handlers at the restaurant also were negative. No eggs from the implicated shipment remained. Eggs from a later shipment from the same distributor, delivered February 9, did not yield SE.

The U.S. Department of Agriculture (USDA) Salmonella enteritidis Control Program and the California Department of Food and Agriculture (CDFA) attempted to trace the implicated eggs back to the farm of origin. However, the traceback was terminated because the eggs were purchased from a distributor who bought and mixed eggs from many different suppliers. Current USDA Salmonella regulations limit the testing of flocks to a single, clearly implicated flock. Outbreak 2: San Diego County

In February 1993, 23 persons who had eaten at a local restaurant on February 16 developed abdominal cramps and diarrhea; two were hospitalized. The mean period from eating at the restaurant to onset of illness was 20 hours (range: 3.5-77.0 hours); duration of symptoms ranged from 2 to 14 days. Stool cultures from 11 of 13 ill persons tested yielded SE; all isolates were phage type 13a and plasmid profile type 2, indistinguishable from the SE strains in outbreak 1.

An investigation by the San Diego County Department of Health Services involved the 23 reported cases and 24 well meal companions. A case was defined as onset of diarrhea (three or more loose stools in a 24-hour period) within 5 days after eating at the restaurant. Eighteen (78%) of the 23 case-patients had eaten an entree served with hollandaise or bearnaise sauce, compared with three (13%) of 24 well persons (OR=25.2; 95% CI=4.4-170.7).

The hollandaise sauce, also used as a base for the bearnaise sauce, was prepared with 12 pooled raw egg yolks. A new batch was prepared at the beginning of each meal shift and placed in a clean dispenser. The dispenser was kept under a heat lamp for up to 3-1/2 hours at approximately 100 F-120 F (37.8 C-48.9 C).

Traceback of implicated eggs by USDA and CDFA indicated they had been purchased from the same distributor that had provided eggs to the restaurant involved in outbreak 1. Again, traceback was terminated. Outbreak 3: Santa Clara County

In March 1993, 22 persons who had eaten at a local sandwich shop during February 28-March 4 developed diarrhea, fever, and abdominal cramps; none were hospitalized. Stool cultures from all 22 ill persons yielded SE; all isolates were phage type 13a and plasmid profile type 2, indistinguishable from the SE strains in outbreaks 1 and 2. Preliminary findings of a case-control study conducted by the Santa Clara County Health Department implicated sandwiches as the vehicle of transmission; no other food was associated with illness. Further investigation revealed that mayonnaise was the only food ingredient containing a raw product of animal origin and was common to all sandwiches eaten by ill persons. None of the implicated mayonnaise remained at the time of the investigation, but unrefrigerated eggs from the implicated shipment obtained from the sandwich shop were cultured in five pools of 10 eggs each; one of the pools yielded SE. This isolate was phage type 13a and plasmid profile type 2. Traceback of implicated eggs by USDA and CDFA indicated they had been purchased from the same distributor that had provided eggs to the two restaurants in outbreaks 1 and 2. Again, traceback was terminated. Reported by: D Ewert, MPH, N Bendana, MS, M Tormey, L Kilman, L Mascola, MD, Los Angeles County Dept of Health Svcs, Los Angeles; LS Gresham, MPH, MM Ginsberg, MD, PA Tanner, ME Bartzen, S Hunt, RS Marks, CR Peter, PhD, San Diego County Dept of Health Svcs, San Diego; J Mohle-Boetani, MD, M Fenstersheib, MD, J Gans, K Coy, MS, S Liska, DrPH, Disease Control and Prevention Unit, Santa Clara County Health Dept, San Jose; S Abbott, R Bryant, L Barrett, DVM, K Reilly, DVM, M Wang, PhD, SB Werner, MD, RJ Jackson, MD, GW Rutherford, III, State Epidemiologist, California Dept of Health Svcs. Animal and Plant Health Inspection Svc, US Dept of Agriculture. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

Editorial Note

Editorial Note: Although most reported SE outbreaks have occurred in the New England and Mid-Atlantic states (3), an increasing proportion of outbreaks has been reported from other areas (Table_1). From 1976 through 1991, the proportion of reported Salmonella isolates in the United States that were SE increased from 5% to 20%; SE was second only to S. typhimurium, except in 1989 and 1990, when SE was the most frequently reported serotype. In California, only four SE outbreaks had been reported since 1985, when active surveillance for SE outbreaks began; the proportion of reported Salmonella isolates that were SE increased from 5% to 13% from 1985 through 1992 and to 21% for the first half of 1993.

An estimated 0.01% of all shell eggs contain SE, although this percentage may be higher in the northeastern United States (4). Consequently, foods containing raw or undercooked eggs (e.g., homemade mayonnaise, hollandaise sauce, and runny omelettes) pose a slight risk for infection with SE. In contrast, commercial mayonnaise is made with pasteurized eggs and is safe. Outbreaks of salmonellosis -- some of substantial magnitude -- may occur when commercial kitchens serve foods made with contaminated shell eggs that have not been sufficiently cooked to kill Salmonella. This is particularly likely when refrigeration is inadequate or holding temperatures are too low and when eggs are pooled, whereby a single contaminated egg can contaminate a large pool. However, egg-handling practices of affected restaurants may be similar to the routine practices of many other restaurants (5). In August 1990, FDA issued recommendations to state agencies that directly regulate commercial establishments concerning the proper handling of shell eggs by restaurants, grocery stores, caterers, institutional feeders, and vending operators. These recommendations include guidelines on refrigeration, cooking, pooling, and substitution with pasteurized eggs.

The temporal clustering of the outbreaks in this report and the same unusual combination of phage type and plasmid profile type common to all three outbreaks suggest that one farm supplied contaminated eggs to all three restaurants. However, because eggs are distributed nationwide and 70% of eggs sold by the distributor in California were obtained or purchased from other states, the source farm may have been outside California. During most egg-associated traceback efforts, the outbreak strain of SE is almost always found on the source farm (6).

Most SE infections occur as sporadic cases or in limited family outbreaks, rather than as part of large common-source outbreaks. Such sporadic cases also are often associated with eating undercooked eggs (7). The risk for infection acquired through consumption of contaminated foods prepared in the kitchens of private homes can be reduced through improved education of consumers regarding the risks of eating raw or undercooked eggs and through increased availability of pasteurized eggs in the retail marketplace. Because most serious illnesses and deaths associated with salmonellosis occur among infants, the elderly, and immunocompromised persons (8,9), persons in these groups should not be served foods containing raw or undercooked eggs. In addition, hospitals, nursing homes, and commercial kitchens should use pasteurized egg products for all recipes requiring pooled eggs or lightly cooked eggs and should refrigerate all eggs and egg products.

On October 27, 1992, the USDA Agricultural Marketing Service published a proposed rule on requirements for storage and transport temperatures of eggs and for carton labeling aimed at increasing the safety of raw shell eggs nationwide. * The comment period for this proposed rule ended March 29, 1993; final regulations are pending and subject to revised legislation. In addition, on August 2, 1993, the USDA Animal and Plant Health Inspection Service (APHIS) published a proposed rule that would revise current USDA regulations concerning chicken infection caused by SE. ** These proposed changes will improve control of the spread of SE in commercial egg-type chicken flocks and include a provision that allows identification of more than one flock as the probable source of eggs causing an SE outbreak. The comment period for this proposed rule has been extended to November 15, 1993. Additional information is available from Dr. John Mason, Director Salmonella enteritidis Control Program, Veterinary Services, APHIS, USDA, Room 205, Presidential Building, 6525 Belcrest Road, Hyattsville, MD 20782; telephone (301) 436-4363.

References

  1. Bennett JV, Holmberg SD, Rogers MF, Solomon SL. Infectious and parasitic diseases. In: Amler RW, Dull HB, eds. Closing the gap: the burden of unnecessary illness. Am J Prev Med 1987;3(suppl):102-

  2. Bean NH, Griffin PM. Foodborne disease outbreaks in the United States, 1973-1987: pathogens, vehicles and trends. J Food Protect 1990;53:804-17.

  3. 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-

  4. 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.

  5. Vugia DJ, Mishu B, Smith M, Tavris DR, Hickman-Brenner FW, Tauxe RV. Salmonella enteritidis outbreak in a restaurant chain: the continuing challenges of prevention. Epidemiol Infect 1993;119:49-

  6. Altekruse S, Koehler J, Hickman-Brenner FW, Tauxe RV, Ferris K. A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks. Epidemiol Infect 1993;110:17-22.

  7. 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.

  8. Levine WC, Buehler JW, Bean NH, Tauxe RV. Epidemiology of nontyphoidal Salmonella bacteremia during the human immunodeficiency virus epidemic. J Infect Dis 1991;164:81-7.

  9. Levine WC, Smart JF, Archer DL, Bean NH, Tauxe RV. Foodborne disease outbreaks in nursing homes, 1975 through 1987. JAMA 1991;266:2105-9.

* 58 FR 48569-48575. 

** 58 FR 41048-41061. +------------------------------------------------------------------- ------+ | Erratum: Vol. 42, No. 41 | |             | | SOURCE: MMWR 42(42);826 DATE: Oct. 29, 1993 | |             | | In the article "Outbreaks of Salmonella enteritidis | | Gastroenteritis -- California, 1993," on page 795, the first sentence | | under the heading "Outbreak 3: Santa Clara County" should read "In | | March 1993, 22 persons who had eaten at a local sandwich shop | | during February 28-March 4 developed diarrhea, fever, and abdominal | | cramps; three were hospitalized." In addition, the third sentence | | of the paragraph should read "Preliminary findings of a | | case-control study conducted by the Santa Clara County Health | | Department identified 16 additional cases and implicated sandwiches | | as the vehicle of transmission; no other food was associated with | | illness."   | |             | +------------------------------------------------------------------- ------+
Table_1
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TABLE 1. Reported outbreaks* of Salmonella enteritidis infection, by region -- United
States, 1985-1992
====================================================================================================
                Northeast+       Outside Northeast          Total
              -------------      -----------------      -------------
 Year         No.      (%)         No.      (%)         No.      (%)
---------------------------------------------------------------------
 1985          21      (81)          5      (19)         26     (  6)
 1986          39      (81)          9      (19)         48     ( 11)
 1987          40      (77)         12      (23)         52     ( 12)
 1988          24      (60)         16      (40)         40     (  9)
 1989          58      (77)         17      (23)         75     ( 17)
 1990          32      (48)         35      (52)         67     ( 16)
 1991          34      (51)         33      (49)         67     ( 16)
 1992          39      (71)         16      (29)         55     ( 13)

 Total        287      (67)        143      (33)        430     (100)
---------------------------------------------------------------------
* Seven outbreaks that originated outside the United States and its territories were not included.
+ Connecticut, Maine, Massachusetts, New Hampshire, New Jersey, New York, Pennsylvania,
  Rhode Island, and Vermont.
====================================================================================================


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