Multistate Outbreak of Salmonella Serotype Typhimurium Infections Associated with Drinking Unpasteurized Milk --- Illinois, Indiana, Ohio, and Tennessee, 2002--2003

On December 10, 2002, the Clark County Combined Health District and the Ohio Department of Health (ODH) were notified of two hospitalized children infected with Salmonella Enterica serotype Typhimurium. Initial investigation implicated consumption of raw, unpasteurized milk purchased at a local combination dairy-restaurant (dairy) during November 27--December 13, 2002, as the cause. This report summarizes the subsequent investigation. Because 27 states still allow the sale of raw milk, and organizations continue their efforts to allow marketing and sale of raw milk to the public directly from the farm (1,2), consumer education about the hazards of raw milk and a careful review of existing policies are needed.

The dairy comprised a working dairy farm, restaurant, snack bar, and petting zoo with goats, cows, calves, lambs, and pigs. At the time of the epidemiologic investigation in December 2002, the workforce comprised 211 workers, including 16 members of the owner family. In 2002, the dairy was the only place in Ohio that sold raw milk in jugs and served raw milk and milk shakes made with raw milk legally to customers. In 2001, approximately 1,350,000 customers visited the dairy.

During November 30, 2002--February 18, 2003, ODH laboratory received 94 S. Typhimurium clinical isolates for pulsed-field gel electrophoresis (PFGE) testing. Of these, 60 had an indistinguishable pattern. In addition, patterns from Illinois, Indiana, and Tennessee matched the Ohio pattern.

A case of S. Typhimurium was defined as PFGE--matched S. Typhimurium isolated during November 30, 2002--February 18, 2003, from clinical samples from a person with an epidemiologic link to the dairy. Case finding was conducted by reviewing laboratory culture results from hospital, private, and ODH laboratories, comparing PFGE patterns of S. Typhimurium isolates with background isolates statewide and nationwide, screening dairy workers, interviewing meal companions, and alerting public health officials of the outbreak nationwide by using CDC's Epidemic Information Exchange (Epi-X).

A total of 62 persons had illness consistent with the case definition, including 40 customers, six household contacts, and 16 (7.6%) of 211 dairy workers; patients were from four states (Illinois, Indiana, Ohio, and Tennessee); the median age was 18 years (range: 1--70 years), and 34 (54.8%) were females. Of the 62 patients, 54 (87.1%) reported signs and symptoms of illness, including diarrhea (52 [96.3%]), cramps (41 [75.9%]), fever (37 [68.5%]), chills (29 [53.7%]), body aches (29 [53.7%]), bloody diarrhea (27 [50.0%]), nausea (25 [46.3%]), vomiting (24 [44.4%]), and headache (21 [38.9%]). A total of 50 (80.6%) exhibited more than one symptom. Disease onset occurred during November 30, 2002--January 14, 2003 (Figure).

A case-control study was conducted to verify the initial findings implicating raw milk and to identify other potential sources of infection. The 40 case-patients who were dairy customers were included in the study. Controls were a convenience sample of well meal companions of case-patients. Because of numerous potential exposures to S. Typhimurium, dairy workers were excluded from the study; secondary infections among friends or households contacts of case-patients also were excluded. Food histories were obtained through telephone interviews by using a standard questionnaire. State and local investigators reviewed milking, bottling, and capping procedures and collected and tested samples from the food, stools of dairy cows, and the environment.

A total of 40 case-patients and 56 controls were eligible for the case-control study. The median age of case-patients was 8 years (range: 1--69 years); 24 (60.0%) were females. The median age of controls was 35 years (range: 1--74 years); 34 (60.7%) were females. In the univariate analysis of potential risk factors, only consumption of raw milk was associated significantly with illness. Among 39 case-patients and 55 controls for whom date of milk purchase was known, 37 (94.9%) and 16 (29.1%), respectively, consumed raw milk (odds ratio [OR] = 45.1; 95% confidence interval [CI] = 8.8--311.9). Consumption of other food items, visiting the petting zoo, and petting animals were not associated with illness.

Of the 32 food samples tested, five were positive for S. Typhimurium, including three raw skim milk samples, one sample of butter made from raw milk purchased by a customer, and one sample of cream. Skim milk samples were taken from milk either bought or bottled on November 29. The PFGE pattern for all five food isolates matched the outbreak pattern. The 31 animal stool samples collected from cows providing milk and the 23 environmental samples taken from dairy equipment and storage sites were negative for S. Typhimurium.

The review of the dairy operation and results of worker screening tests revealed that four barn workers had asymptomatic S. Typhimurium infection. Barn workers milked the cows, bottled the milk, and made ice cream.

On December 13, 2002, following an order from local health authorities, the dairy discontinued the sale of all raw milk products. On January 13, 2003, the Ohio Department of Agriculture (ODA) recommended that the sale of all dairy products made with raw milk, including bottled raw whole milk, skim milk, and cream, be discontinued permanently. Several sanitation improvements, primarily for the barn workers, also were recommended, including more frequent hand washing, replacement of the some of the equipment and utensils (e.g., mixing bowls), and enhanced general cleaning in the entire property.

Reported by: J Holt, D Propes, C Patterson, MBA, Clark County Combined Health District, Springfield; T Bannerman, PhD, L Nicholson, M Bundesen, E Salehi, MPH, M DiOrio, MD, Ohio Dept of Health; C Kirchner, R Tedrick, MS, Ohio Dept of Agriculture. R Duffy, DDS, Division of Adult and Community Health, National Center for Chronic Diseases Prevention and Health Promotion; J Mazurek, MD, EIS Officer, CDC.

Editorial Note:

Each year in the United States, foodborne disease causes an estimated 76 million illnesses. Of these, an estimated 1.4 million are caused by Salmonella, resulting in approximately 16,000 hospitalizations and 580 deaths (3). Raw bulk tank milk can contain one or more species of pathogenic bacteria, including Salmonella spp. (4,5). During 1972--2000, a total of 58 raw milk--associated outbreaks were reported to CDC, of which 17 (29%) were caused by Salmonella spp. (1,6).

This report describes a large multistate outbreak of S. Typhimurium transmitted through consumption of raw milk and milk products. Although animal and environmental samples were negative for S. Typhimurium, four barn workers were infected with S. Typhimurium. In addition, all S. Typhimurium isolates from clinical specimens and foods had indistinguishable PFGE patterns. The source for contamination was not determined; however, the findings suggest that contamination of milk might have occurred during the milking, bottling, or capping process.

In 2002, intrastate sale of raw milk for human consumption was legal in 28 states, including Ohio (1). As of October 1997, Ohio law did not allow the sale of raw milk except for dairies that were engaged continuously in the business of selling or offering for sale raw milk directly to consumers before October 31, 1965 (7). The dairy in this outbreak had been in operation since 1958 and was the only place in Ohio selling raw milk legally. After ODA issued its recommendations, the dairy voluntarily relinquished its license for selling raw milk. As a result, no businesses now sell raw milk to the public legally in Ohio.

Molecular subtyping of S. Typhimurium isolates had an important role in identifying cases that were part of this outbreak and defining its extent (8). Typhimurium is one of the most common Salmonella serotypes isolated from persons in Ohio, and without the specificity of PFGE typing, identifying cases that were part of the outbreak would have been difficult.

Despite the known association of raw milk with disease-causing organisms, some consumers believe that raw milk is of better quality than pasteurized milk (9). In several states, producers circumvent regulations and provide raw milk to consumers by establishing cow-leasing programs in which farmers keep and milk cows owned by individuals (CDC, unpublished data, 2003). Consumer education about the hazards of raw milk consumption is needed. Retail milk regulations should be reviewed and strengthened, if needed, to minimize exposure of the public to the hazards of raw milk consumption.

Acknowledgments

This report is based on data contributed by B Kluesener, P Pontones, Indiana Dept of Health. J Fernandez, Chicago Dept of Public Health, Illinois. D Scheer, Auglaize County Health Dept, Wapakoneta; T Anglin, Butler County Health Dept, Hamilton; S Edwards, Clermont County General Health District, Batavia; L Hines, Delaware General Health District, Delaware; M Fornadley, Franklin County Board of Health, Columbus; D Brannen, A Woodard, Greene County Combined Health District, Xenia; S Lester, Hamilton County General Health District, Cincinnati; A McCoppin, Highland County Health Dept, Hillsboro; C Alderman, Madison County Health District, London; J Close, J Reed, Combined General Health District of Montgomery, Dayton; E Meyer, Preble County General Health District, Eaton; R Hart, Sidney-Shelby County Health District, Sidney; V Johnson, Warren County Combined Health District, Lebanon; B Mitchell, L Holbert, Ohio Dept of Health.

References

1. Headrick ML, Korangy S, Bean NH, et al. The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am J Public Health 1998;88:1219--21.
2. Ohio Farm Bureau Federation. Ohio Farm Bureau Federation's 84th annual meeting, Cincinnati, Ohio, December 4--6, 2002. Available at http://www.ofbf.org/ofbweb/ofbwebengine.nsf/$LookUpPageID/REVN-5H8RTA/?OpenDocument.
3. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607--25.
4. Jayarao BM, Wang L. A study on the prevalence of gram-negative bacteria in bulk tank milk. J Dairy Sci 1999;82:2620--4.
5. Jayarao BM, Henning DR. Prevalence of foodborne pathogens in bulk tank milk. J Dairy Sci 2001;84:2157--62.
6. CDC. U.S. foodborne disease outbreaks. Available at http://www2.cdc.gov/ncidod/foodborne/fbsearch.asp3.
7. Ohio Revised Code, Title IX Agriculture-Animals-Fences, Chapter 917: Dairy products, section 917.04: sale and labeling of raw milk. Available at http://onlinedocs.andersonpublishing.com/oh/lpExt.dll?f=templates&fn=mainh.htm&cp=PORC.
8. Bender JB, Hedberg CW, Boxrud DJ, et al. Use of molecular subtyping in surveillance for Salmonella Enterica serotype Typhimurium. N Engl J Med 2001;344:189--95.
9. Hegarty H, O'Sullivan MB, Buckley J, Foley-Nolan C. Continued raw milk consumption on farms: why? Commun Dis Public Health 2002;5:151--6.

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