A National Outbreak of Salmonella enteritidis Infections from Ice Cream
Thomas W. Hennessy, M.D., Craig W. Hedberg, Ph.D., Laurence Slutsker, M.D., M.P.H., Karen E. White, M.P.H., John M. Besser-Wiek, M.S., Michael E. Moen, M.P.H., John Feldman, B.S., William W. Coleman, M.S., Larry M. Edmonson, M.P.H., Kristine L. MacDonald, M.D., M.P.H., Michael T. Osterholm, Ph.D., M.P.H., for The Investigation Team
Background In September 1994, the Minnesota Department of Healthdetected an increase in the number of reports of Salmonellaenteritidis infections. After a casecontrol study implicateda nationally distributed brand of ice cream (Schwan's) in theoutbreak, the product was recalled and further epidemiologicand microbiologic investigations were conducted.
Methods We defined an outbreak-associated case of S. enteritidisinfection as one in which S. enteritidis was cultured from aperson who became ill in September or October 1994. We establishednational surveillance and surveyed customers of the implicatedmanufacturer. The steps involved in the manufacture of ice creamassociated with cases of S. enteritidis infection were comparedwith those of products not known to be associated with infectionmatched for the date of manufacture. Cultures for bacteria wereobtained from ice cream samples, the ice cream plant, and tankertrailers that had transported the ice cream base (premix) tothe plant.
Results We estimate that S. enteritidis gastroenteritis developedin 224,000 persons in the United States after they ate Schwan'sice cream. The attack rate for consumers was 6.6 percent. Icecream associated with infection contained a higher percentageof premix that had been transported by tanker trailers thathad carried nonpasteurized eggs immediately before (P = 0.02).S. enteritidis was isolated from 8 of 266 ice cream products(3 percent), but not from environmental samples obtained fromthe ice cream plant (n = 157) or tanker trailers (n = 204).
Conclusions This nationwide outbreak of salmonellosis was mostlikely the result of contamination of pasteurized ice creampremix during transport in tanker trailers that had previouslycarried nonpasteurized liquid eggs containing S. enteritidis.To prevent further outbreaks, food products not destined forrepasteurization should be transported in dedicated containers.
Source Information
From the Acute Disease Epidemiology Section (T.W.H., C.W.H., K.E.W., K.L.M., M.T.O.), the Public Health Laboratory (J.M.B.-W.), and the Executive Office (M.E.M.), Minnesota Department of Health, Minneapolis; the Division of Field Epidemiology and Epidemic Intelligence Service (T.W.H.), and the Foodborne and Diarrheal Diseases Branch, National Center for Infectious Diseases (L.S.), Centers for Disease Control and Prevention, Atlanta; the Food and Drug Administration, Minneapolis (J.F.); the Division of Dairy and Food Inspection, Minnesota Department of Agriculture, St. Paul (W.W.C.); and Disease Prevention and Control, Olmsted County Health Department, Rochester, Minn. (L.M.E.).
Address reprint requests to Dr. Osterholm at the Acute Disease Epidemiology Section, Minnesota Department of Health, 717 Delaware St., SE, P.O. Box 9441, Minneapolis MN 55440-9441.
Jeffery, C., Ozonoff, A., White, L. F., Nuno, M., Pagano, M.
(2009). Power to Detect Spatial Disturbances under Different Levels of Geographic Aggregation. J. Am. Med. Inform. Assoc.
16: 847-854
[Abstract][Full Text]
Dembek, Z. F., Smith, L. A., Rusnak, J. M.
(2007). Botulism: Cause, Effects, Diagnosis, Clinical and Laboratory Identification, and Treatment Modalities. dmphp
1: 122-134
[Abstract][Full Text]
Esteves, C. L. C., Jones, B. D., Clegg, S.
(2005). Biofilm Formation by Salmonella enterica Serovar Typhimurium and Escherichia coli on Epithelial Cells following Mixed Inoculations. Infect. Immun.
73: 5198-5203
[Abstract][Full Text]
Wein, L. M., Liu, Y.
(2005). Analyzing a bioterror attack on the food supply: The case of botulinum toxin in milk. Proc. Natl. Acad. Sci. USA
102: 9984-9989
[Abstract][Full Text]
Lu, S., Killoran, P. B., Riley, L. W.
(2003). Association of Salmonella enterica Serovar Enteritidis YafD with Resistance to Chicken Egg Albumen. Infect. Immun.
71: 6734-6741
[Abstract][Full Text]
Fernandez, J., Fica, A., Ebensperger, G., Calfullan, H., Prat, S., Fernandez, A., Alexandre, M., Heitmann, I.
(2003). Analysis of Molecular Epidemiology of Chilean Salmonella enterica Serotype Enteritidis Isolates by Pulsed-Field Gel Electrophoresis and Bacteriophage Typing. J. Clin. Microbiol.
41: 1617-1622
[Abstract][Full Text]
Gallay, A., Vaillant, V., Bouvet, P., Grimont, P., Desenclos, J.-C.
(2000). How Many Foodborne Outbreaks of Salmonella Infection Occurred in France in 1995? : Application of the Capture-Recapture Method to Three Surveillance Systems. Am J Epidemiol
152: 171-177
[Abstract][Full Text]
Ahmed, R., Soule, G., Demczuk, W. H., Clark, C., Khakhria, R., Ratnam, S., Marshall, S., Ng, L.-K., Woodward, D. L., Johnson, W. M., Rodgers, F. G.
(2000). Epidemiologic Typing of Salmonella enterica Serotype Enteritidis in a Canada-Wide Outbreak of Gastroenteritis due to Contaminated Cheese. J. Clin. Microbiol.
38: 2403-2406
[Abstract][Full Text]
(2000). Food irradiation: Let's do it. CMAJ
162: 5-5
[Full Text]
Miao, E. A., Miller, S. I.
(1999). Bacteriophages in the evolution of pathogen-host interactions. Proc. Natl. Acad. Sci. USA
96: 9452-9454
[Full Text]
Darwin, K. H., Miller, V. L.
(1999). Molecular Basis of the Interaction of Salmonella with the Intestinal Mucosa. Clin. Microbiol. Rev.
12: 405-428
[Abstract][Full Text]
Sanders, T A B
(1999). Food production and food safety. BMJ
318: 1689-1693
[Full Text]
Simonsen, L., Conn, L. A., Pinner, R. W., Teutsch, S.
(1998). Trends in Infectious Disease Hospitalizations in the United States, 1980-1994. Arch Intern Med
158: 1923-1928
[Abstract][Full Text]
McDade, J. E., Hausler, W. J. Jr.
(1998). Modernization of Public Health Laboratories in a Privatization Atmosphere. J. Clin. Microbiol.
36: 609-613
[Full Text]
Mahler, H., Pasi, A., Kramer, J. M., Schulte, P., Scoging, A. C., Bar, W., Krahenbuhl, S.
(1997). Fulminant Liver Failure in Association with the Emetic Toxin of Bacillus cereus. NEJM
336: 1142-1148
[Abstract][Full Text]
(1996). Outbreaks of Salmonella Serotype Enteritidis Infection Associated With Consumption of Raw Shell Eggs--United States, 1994-1995. JAMA
276: 1017-1019
[Abstract]
O'Ryan, M., Djuretic, T., Wall, P. G., Nichols, G., Hennessy, T. W., Slutsker, L., Hedberg, C. W., MacDonald, K. L., Osterholm, M. T.
(1996). An Outbreak of Salmonella Infection from Ice Cream. NEJM
335: 824-825
[Full Text]
Blaser, M. J.
(1996). How Safe is Our Food? -- Lessons from an Outbreak of Salmonellosis. NEJM
334: 1324-1325
[Full Text]