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Multistate Outbreak of Salmonella Typhimurium Infections Associated with Eating Ground Beef --- United States, 2004

Salmonella infections cause an estimated 1.4 million human illnesses and 400 deaths annually in the United States (1). Although the incidence of several other foodborne bacterial infections decreased substantially during 1996--2004, the incidence of Salmonella infections declined modestly (2). In September 2004, the New Mexico Department of Health received reports from the New Mexico Scientific Laboratory Division of eight Salmonella enterica serotype Typhimurium isolates that had indistinguishable pulsed-field gel electrophoresis (PFGE) patterns using XbaI and BlnI restriction enzymes. The patients were from three New Mexico counties and had onsets of illness during August 18--29. A review of PFGE patterns submitted to the National Molecular Subtyping Network for Foodborne Disease Surveillance (PulseNet) database for Salmonella revealed 31 indistinguishable patient isolates of S. Typhimurium from nine states (Colorado, Kansas, Minnesota, New Jersey, New Mexico, New York, Ohio, Tennessee, and Wisconsin) and the District of Columbia, with illness onset occurring during August 11--October 2, 2004. The S. Typhimurium isolates were susceptible to all antimicrobial agents tested. An investigation conducted by state health departments, CDC, and the U.S. Department of Agriculture Food Safety and Inspection Service (FSIS) identified ground beef purchased at a national chain of supermarkets as the source of S. Typhimurium infections. Traceback results indicated product originating from a common supplier; however, evaluators determined that plant practices conformed to FSIS production guidelines, and no product recalls were made. This report describes the investigation and underscores the risk for salmonellosis from contact with contaminated ground beef, despite regulatory directives to reduce Salmonella contamination in beef production. Reduced contamination and consumption of raw or undercooked meat and further education of the food service industry and consumers are critical to reducing foodborne salmonellosis.

A case was defined as infection with S. Typhimurium with a PFGE pattern indistinguishable from the outbreak pattern. Participating health departments (Colorado, Kansas, Minnesota, New Mexico, Ohio, Wisconsin, and District of Columbia) used questionnaires to collect detailed information about patient history of food consumption before illness onset. After careful review of food histories and information on other possible exposures among patients, contaminated ground beef was suspected as the vehicle for this outbreak. Several patients reported having eaten ground beef purchased at the same national chain of supermarkets (chain A). To identify exposures associated with illness and to investigate the source of potentially contaminated ground beef, the participating health departments conducted a case-control study during September 30--October 19, 2004. The case-control study included case-patients from the six states and the District of Columbia and controls identified by sequential telephone digit dialing. The controls were matched by age group (ages 2--10, 11--17, 18--60, and >60 years) to case-patients and had no reported gastrointestinal illness within 7 days before onset of illness of the matched case-patients. Case-patients and controls were asked detailed questions regarding ground beef consumption and brand, location, and date of purchase of ground beef.

Twenty-six of 31 case-patients (Figure) and 46 controls were enrolled in the case-control study. Five patients were not enrolled in the study; three were from states that declined to participate, and two could not be contacted. Fourteen (53.9%) case-patients were female, and the median age was 30.5 years (range: 2--80 years). Twenty-one (47.7%) controls were female, and the median age was 35 years (range: 2--87 years). Symptoms reported by the case-patients included diarrhea (100%), abdominal cramps (92%), fever (92%), vomiting (65%), and bloody diarrhea (46%). Median duration of illness was 7.5 days (range: 2--30 days); 35% of patients were hospitalized. No patients died.

Of the 26 case-patients, 23 with matched controls were included in the analyses (three with no matched controls were excluded). Among 23 matched case-patients, 21 (91%) reported eating ground beef during the 7 days before illness, compared with 37 (80%) of 46 controls (matched odds ratio [mOR] = 2.4; 95% confidence interval [CI] = 0.5--11.8). Ten (44%) matched case-patients reported eating raw or undercooked ground beef or tasting the beef while cooking, compared with eight (17%) controls (mOR = 7.4; CI = 1.2--44.6). Among 21 case-patients who ate ground beef, 15 (71%) purchased the beef within 3 weeks before illness onset from chain A, compared with nine (24%) controls (mOR = 12.7; CI = 1.6--99.2).

The Minnesota Department of Agriculture tested a sample of leftover frozen ground beef provided by a Minnesota case-patient. The sample yielded S. Typhimurium with a PFGE pattern indistinguishable from the outbreak pattern.

For seven case-patients who reported consumption of ground beef purchased at chain A, shopper cards or purchase receipts were used to determine the source of ground beef and its production date. Traceback results indicated that the ground beef was packaged at three processing plants. One supplier common to all three plants was identified, although beef was mixed at the three processing plants with ingredients from other suppliers. Two other case-patients provided approximate dates for when they purchased ground beef at chain A; records indicated that their purchases could have been from one of the three implicated plants with product originating from the common supplier.

FSIS evaluators assessed the three processing plants and their common supplier by reviewing existing FSIS records and internal plant Hazard Analysis and Critical Control Point plans, processes, and records, including microbial analyses conducted by FSIS officers for the relevant production periods. After extensive investigation, evaluators determined that plant practices conformed to current FSIS production guidelines. No products were recalled.

Reported by: A Cronquist, MPH, Colorado Dept of Public Health and Environment. S Wedel, MPH, Minnesota Dept of Health. B Albanese, MD, CM Sewell, DrPH, New Mexico Dept of Health. D Hoang-Johnson, Wisconsin Dept of Health. T Ihry, DVM, US Dept of Agriculture, Food Safety and Inspection Svc. M Lynch, MD, J Lockett, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; N Kazerouni, DrPH, C O'Reilly, PhD, D Ferguson, MD, EIS officers, CDC.

Editorial Note:

Salmonella species colonize the gastrointestinal tracts of cattle and other animals. Many infected cattle are asymptomatic carriers. Carcasses can become contaminated with Salmonella spp. during slaughter operations. Although FSIS has documented a decrease in Salmonella spp. in ground beef, from a baseline prevalence of 7.5% in 1996 to 1.6% of 30,984 regulatory samples collected in 2004 (3,4), outbreaks of human Salmonella infections associated with ground beef continue to occur.

Investigation of this outbreak of S. Typhimurium infection implicated ground beef, particularly consumption of raw or undercooked ground beef, as the source of infection. Ground beef has been implicated as the vehicle for transmission of Salmonella spp. in previous foodborne outbreaks (5--7). Outbreaks of nontyphoidal Salmonella infections and sporadic illness have been associated with various causes, particularly foods of animal origin (1). Recently, the first multistate outbreak of multidrug-resistant S. Typhimurium phage type DT104 associated with consumption of store-bought ground beef occurred in the northeastern United States (8). Epidemiologic and traceback investigations performed during the outbreak described in this report suggested one common supplier as the source. However, processing plant practices appeared to adhere to current FSIS production guidelines. In light of these findings and the findings from previous salmonellosis outbreak investigations (5--8), regulatory requirements and guidelines along the beef production chain, from farming through consumption, should be reviewed to determine whether current critical control points (i.e., preventive measures to control food safety hazards) and pathogen reduction strategies are adequate for Salmonella control.

Although the overall incidence of salmonellosis declined by only 8% from 1996 to 2004, infection with S. Typhimurium declined by 41% (2). A proportion of the decline in the incidence of S. Typhimurium infection might be a consequence of increased pathogen reduction strategies for E. coli O157:H7 in ground beef. In 2003 and 2004, incidence of human infections caused by E. coli O157:H7 declined, according to cases reported to the CDC Foodborne Diseases Active Surveillance Network (FoodNet) (2). This decline in human illness was consistent with declines in E. coli O157:H7 contamination of ground beef reported by FSIS during the same period (9). These declines might have been attributable to multiple interventions by regulators (e.g., USDA's declaration of E. coli O157:H7 as an adulterant in ground beef and a compulsory reassessment of the Pathogen Reduction/Hazard Analysis Critical Control Point plans) and beef industry (e.g., increased product testing, more efficient cleaning and sanitizing of carcasses, and diversion of contaminated product from raw ground-beef manufacturing [9]). Such interventions might have concurrently reduced Salmonella contamination of ground beef and salmonellosis in humans. However, regulatory and industry prevention measures and public health education need to be strengthened to meet the national health objective for reducing Salmonella infection.*

The findings in this report also highlight the importance of using PFGE (10) to identify clusters of illness, particularly for S. Typhimurium. Use of PulseNet to disseminate PFGE subtype data, combined with specific case interview information, allowed for an efficient and timely traceback investigation. State and local health departments should continue to conduct timely epidemiologic investigations of Salmonella cases. Routine subtyping of isolates of common Salmonella spp. serotypes such as S. Typhimurium and comparison of isolate PFGE patterns through PulseNet might help focus limited epidemiologic resources by identifying cases that likely are linked (10). Investigation of Salmonella spp. clusters associated with raw or undercooked ground beef consumption can 1) elucidate the mechanisms and possible sources of contamination of ground beef, 2) help determine whether regulatory requirements for the beef industry are adequate, and 3) help identify control points for reducing Salmonella spp. in the meat supply.

Salmonellosis outbreaks associated with ground beef continue, despite Hazard Analysis and Critical Control Point systems, enhanced adherence to good manufacturing practices, and education of food processors, preparers, and servers at all levels in the food industry and in the home. Targeting interventions at various steps, from beef production through consumption, might help prevent salmonellosis. Consumers should continue to be made aware of the risks associated with eating raw or undercooked ground beef, tasting ground beef during food preparation, and cross-contamination from raw meat to ready-to-eat foods, as well as the importance of hand washing after handling raw ground beef.


This report is based, in part, on data contributed by D Neises, MPH, Kansas Dept of Health; E Salehi, MPH, A Arendt, MPH, Ohio Dept of Health; S Soubagleh, District of Columbia Dept of Health; M Landen, MD, A Robbins, MPH, D Sena, New Mexico Dept of Health; K Elfering, K Vought, Minnesota Dept of Agriculture; K Holt, DVM, M Karinen, US Dept of Agriculture, Food Safety and Inspection Svc; and M Mueller, MPH, Public Health Prevention Svc Fellow, CDC.


  1. Voetsch AC, Van Gilder TJ, Angulo FJ, et al. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 2004;38(Suppl 3):S127--34.
  2. CDC. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food---10 sites, United States, 2004. MMWR 2005;54:352--6.
  3. US Department of Agriculture. Salmonella testing of raw meat & poultry products, 1998--2004: progress report. Washington, DC: US Department of Agriculture; 2006. Available at
  4. US Department of Agriculture. Nationwide Federal Plant Raw Ground Beef Microbiological Survey, August 1993--March 1994. Washington, DC: US Department of Agriculture; 1996. Available at
  5. CDC. Salmonella Typhimurium---Minnesota, Wisconsin, Michigan. MMWR 1972;21:411--6.
  6. CDC. Outbreak of Salmonella serotype Typhimurium infection associated with eating raw ground beef---Wisconsin, 1994. MMWR 1995;44:905--9.
  7. CDC. Outbreak of multidrug-resistant Salmonella Newport---United States, January--April 2002. MMWR 2002;51:545--8.
  8. Dechet AM, Scallan E, Gensheimer K, et al. Outbreak of multidrug-resistant Salmonella enterica Typhimurium definitive type 104 infection linked to commercial ground beef, northeastern United States, 2003--2004. Clin Infect Dis 2006;42:747--52.
  9. Naugle AL, Holt KG, Levine P, Eckel R. Food safety and inspection service regulatory testing program for Escherichia coli O157:H7 in raw ground beef. J Food Prot 2005;68:462--8.
  10. 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.

* Healthy People 2010 objective 10-1d is to reduce the incidence of Salmonella species infections to 6.8 per 100,000 population.


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