Introduction

CDC collaborated with public health and agriculture officials in many states and the U.S. Department of Agriculture’s Food Safety and Inspection Service (USDA-FSIS) to investigate a multistate outbreak of Salmonella Heidelberg infections. Epidemiologic, laboratory, and traceback investigations indicated that consumption of Foster Farms brand chicken was the source of this outbreak.

Public health investigators used the PulseNet system to identify cases of illness that were part of this outbreak. PulseNet is the national subtyping network of public health and food regulatory agency laboratories coordinated by CDC. PulseNet obtains DNA “fingerprints” of Salmonella bacteria through diagnostic testing and uses pulsed-field gel electrophoresis, or PFGE, to identify cases of illness.

Seven strains of Salmonella Heidelberg bacteria were identified as being linked to this outbreak. Before this outbreak, four of these strains were rarely reported to PulseNet. The other three strains were more common, with several ill persons infected with each strain reported to CDC monthly. Since some of these strains are more commonly reported to PulseNet, some illnesses may be part of the expected background and may not be linked to consumption of Foster Farms chicken. The DNA fingerprints of the Salmonella Heidelberg bacteria associated with this outbreak include the strain that was also associated with a multistate outbreak of Salmonella Heidelberg linked to Foster Farms brand chicken processed at an establishment in Washington during 2012-2013.

A total of 634 individuals infected with the outbreak strains of Salmonella Heidelberg were reported from 29 states and Puerto Rico from March 1, 2013 to July 11, 2014. Most of the ill persons (77%) were reported from California. The total number of ill persons identified in each state was as follows: Alaska (1), Alabama (1), Arkansas (1), Arizona (25), California (490), Colorado (9), Connecticut (1), Delaware (1), Florida (4), Georgia (1), Hawaii (1), Idaho (5), Illinois (4), Kentucky (1), Louisiana (1), Michigan (4), Missouri (5), Montana (1), Nevada (11), New Mexico (2), North Carolina (1), Oregon (17), Tennessee (1), Texas (13), Utah (6), Virginia (4), Washington (20), West Virginia (1), and Wisconsin (1); one illness was reported from Puerto Rico.

Among 633 persons for whom information was available, illness onset dates ranged from March 1, 2013 to July 11, 2014. Ill persons ranged in age from younger than 1 year to 93 years, with a median age of 18 years. Fifty percent of ill persons were male. Among 528 persons for whom information was available, 200 (38%) were hospitalized. Fifteen percent of ill persons developed blood infections as a result of their illness. Typically, approximately 5% of persons ill with Salmonella infections develop blood infections. No deaths were reported.

The current outbreak appears to be over as the number of reported infections has returned to the expected number for this time of year. Since some of the outbreak strains are reported to PulseNet even in the absence of an outbreak, several ill persons infected with these strains are still expected to be reported to CDC monthly.

Epidemiologic Investigation

In interviews, ill persons answered questions about foods consumed and other exposures during the week before becoming ill. Two hundred and sixty (74%) of 350 ill persons interviewed reported consuming chicken prepared at home in the week before becoming ill. This proportion was significantly higher when compared with results from a survey of healthy persons Cdc-pdf [PDF – 29 pages] in which 65% reported consuming chicken prepared at home in the week before they were interviewed. Among those who had brand information available, 152 (87%) of 175 ill persons reported that they consumed Foster Farms brand chicken or another brand likely produced by Foster Farms.

Additionally, among the 490 ill persons reported in California, state and local health officials identified at least 25 ill persons as part of a cluster of illnesses in October 2013 during this outbreak. The ill persons consumed food purchased from the same Costco store location in South San Francisco in the week before they became sick. Based on interviews of ill persons, cooked rotisserie chicken purchased from this store location was linked to the illnesses. Shopper card information was successfully used to determine the specific food linked to illnesses and allowed investigators to identify the chicken involved as being supplied by Foster Farms. Ill persons gave permission for public health officials to retrieve purchase information based on shopper card numbers.

Laboratory Testing

During the outbreak investigation, health departments in California and Washington collected leftover chicken from the homes of ill persons for laboratory testing. Testing conducted by the Washington State Public Health Laboratories identified one of the outbreak strains of Salmonella Heidelberg in one unopened package of raw Foster Farms chicken collected from an ill person’s home in Washington. The unopened package did not contain information for the establishment in which the chicken was processed. Two samples of leftover rotisserie chicken were collected by California Department of Public Health from the homes of ill persons infected with outbreak strains of Salmonella Heidelberg identified during the cluster investigation in South San Francisco; laboratory testing conducted by the California Food and Drug Laboratory Branch identified one of the outbreak strains of Salmonella Heidelberg in both samples of leftover rotisserie chicken. Additional testing by California also identified one of the outbreak strains of Salmonella Heidelberg in sample of leftover raw Foster Farms chicken collected from an ill person’s home. The outbreak strain isolated from this person was different from the strain isolated from the leftover chicken sample.

Testing conducted by USDA-FSIS identified one of the outbreak strains of Salmonella Heidelberg in a sample of leftover raw Foster Farms chicken from an ill person’s home in California. The outbreak strain isolated from this person was different from the strain isolated from the leftover chicken sample.

The National Antimicrobial Resistance Monitoring System (NARMS)External is a U.S. public health surveillance system that tracks antibiotic resistance in foodborne and other enteric bacteria found in people, raw meat and poultry, and food-producing animals. NARMS is an interagency partnership among CDC, the U.S. Food and Drug Administration (FDA), USDA, and state and local health departments.

The NARMS human surveillance program at CDC monitors antibiotic resistance in Salmonella and other bacteria isolated from clinical specimens submitted to NARMS by public health laboratories. CDC’s NARMS laboratory conducted antibiotic resistance testing on a total of 68 clinical isolates collected from ill persons infected with each of the seven outbreak strains of Salmonella Heidelberg. Of the 68 isolates tested, 24 (35%) were not resistant to any of the antibiotics tested by NARMS and 44 (65%) were drug resistant (defined as resistance to one or more antibiotics). Twenty-four (35%) of the 68 isolates were multidrug resistant (defined as resistance to one or more antibiotics in three or more drug classes). Not all drug-resistant isolates exhibited the same antibiotic resistance pattern. Isolates collected from ill persons were resistant to combinations of the following antibiotics: ampicillin, chloramphenicol, gentamicin, kanamycin, streptomycin, sulfisoxazole, and tetracycline. Although these antibiotics are not typically used to treat Salmonella blood infections or other severe Salmonella infections, antibiotic resistance can be associated with increased risk of hospitalization in infected individuals.

Additionally, CDC’s NARMS laboratory received isolates from five chicken products produced by Foster Farms: four collected from ill people’s homes in California and Washington, and one collected from a warehouse chain store located in California. Of the five isolates tested, one (20%) was not resistant to any of the antibiotics tested by NARMS and four (80%) were drug resistant. One (20%) of these five isolates was multidrug resistant. Not all drug-resistant isolates exhibited the same antibiotic resistance pattern. Isolates collected from chicken were resistant to combinations of the following antibiotics: kanamycin, streptomycin, sulfisoxazole, and tetracycline.

The NARMS retail meat and poultry surveillance programExternal monitors antibiotic resistance in Salmonella and other bacteria isolated from raw retail meat and poultry. NARMS laboratorians isolated five of the seven outbreak strains from nine retail samples of Foster Farms chicken breasts and wings collected in California. Susceptibility testing was conducted on 8 of the 9 isolates; 8 out of 8 (100%) were drug resistant, and none (0%) were pansusceptible. Four out of the 8 (50%) isolates were multidrug resistant. Not all isolates from poultry exhibited the same antibiotic resistance pattern. Isolates collected from poultry were resistant to combinations of the following antibiotics: ampicillin, chloramphenicol, gentamicin, kanamycin, streptomycin, sulfisoxazole, and tetracycline.

Regulatory Investigation

During September 2013, FSIS conducted intensified in-facility testing for Salmonella at four Foster Farms production establishments in California and Washington. Six of the seven outbreak strains of Salmonella Heidelberg were isolated from raw chicken samples collected from the three Foster Farms establishments in California.

On October 7, 2013, USDA-FSIS issued a Public Health AlertExternal due to concerns that illnesses caused by strains of Salmonella Heidelberg were associated with raw chicken products produced by Foster Farms at three facilities in California. On October 10, 2013, USDA-FSIS announced that Foster Farms submitted and implemented immediate substantive changes to their slaughter and processing to allow for continued operations.

On October 12External and October 17External , 2013, a California warehouse store initiated recalls of Foster Farms rotisserie chicken products due to possible Salmonella Heidelberg contamination. USDA-FSIS, CDC, the California Department of Public Health, and the San Mateo Public Health Department determined through epidemiologic and traceback investigations that there was a link between the rotisserie chicken products and illness.

USDA-FSIS reinstated intensified sampling at the affected establishments following corrective actions in October 2013 and continues to monitor these establishments. Since October 2013, there has been a steady decrease of Salmonella-positive samples in all three of the establishments after implementation of the corrective actions began.

On July 3, 2014, Foster Farms recalledExternal an undetermined amount of chicken products that may be contaminated with a particular strain of Salmonella Heidelberg. The recall resulted from USDA-FSIS identifying one of the outbreak strains of Salmonella Heidelberg in an intact sample of Foster Farms brand chicken collected from the home of a person in California infected with the same strain. The chicken breasts were packaged with critical labeling information to associate the product with the establishment and a specific production date. The ill person’s family purchased their chicken in March; however, it was stored in the family’s freezer and some of it was consumed in late April.

Foster Farms has implemented and continues to utilize multiple interventions to reduce Salmonella throughout its entire poultry production process. This strategy includes interventions at the breeder level, at hatcheries, at grow-out farms, and at the processing plant where the final product is packaged. Supported by data from continuous testing by Foster Farms, these interventions have reduced Salmonella prevalence to less than 5 percent in the Foster Farms establishments linked to this outbreak.

FSIS has determined that process control measures undertaken by the firm to consistently minimize Salmonella contamination of raw chicken have been successful.