National Outbreak of Multidrug Resistant Salmonella Heidelberg Infections Linked to a Single Poultry Company

Abstract

ImportanceThis large outbreak of foodborne salmonellosis demonstrated the complexity of investigating outbreaks linked to poultry products. The outbreak also highlighted the importance of efforts to strengthen food safety policies related to Salmonella in chicken parts and has implications for future changes within the poultry industry.ObjectiveTo investigate a large multistate outbreak of multidrug resistant Salmonella Heidelberg infections.DesignEpidemiologic and laboratory investigations of patients infected with the outbreak strains of Salmonella Heidelberg and traceback of possible food exposures.SettingUnited States. Outbreak period was March 1, 2013 through July 11, 2014PatientsA case was defined as illness in a person infected with a laboratory-confirmed Salmonella Heidelberg with 1 of 7 outbreak pulsed-field gel electrophoresis (PFGE) XbaI patterns with illness onset from March 1, 2013 through July 11, 2014. A total of 634 case-patients were identified through passive surveillance; 200/528 (38%) were hospitalized, none died.ResultsInterviews were conducted with 435 case-patients: 371 (85%) reported eating any chicken in the 7 days before becoming ill. Of 273 case-patients interviewed with a focused questionnaire, 201 (74%) reported eating chicken prepared at home. Among case-patients with available brand information, 152 (87%) of 175 patients reported consuming Company A brand chicken. Antimicrobial susceptibility testing was completed on 69 clinical isolates collected from case-patients; 67% were drug resistant, including 24 isolates (35%) that were multidrug resistant. The source of Company A brand chicken consumed by case-patients was traced back to 3 California production establishments from which 6 of 7 outbreak strains were isolated.ConclusionsEpidemiologic, laboratory, traceback, and environmental investigations conducted by local, state, and federal public health and regulatory officials indicated that consumption of Company A chicken was the cause of this outbreak. The outbreak involved multiple PFGE patterns, a variety of chicken products, and 3 production establishments, suggesting a reservoir for contamination upstream from the production establishments. Sources of bacteria and genes responsible for resistance, such as farms providing birds for slaughter or environmental reservoir on farms that raise chickens, might explain how multiple PFGE patterns were linked to chicken from 3 separate production establishments and many different poultry products.

Salmonella enterica subsp. enterica Serovar Heidelberg Food Isolates Associated with a Salmonellosis Outbreak Have Enhanced Stress Tolerance Capabilities

“…Overall, the data indicated that isolate pairs from the same strain were not necessarily highly related. This is not surprising, as the outbreak involved multiple processing establishments, which were in turn sourced from multiple farms (28,29 (39). This makes JF6X01.0045 isolates unusually dissimilar for isolates from the same strain FIG 9 Differences in expression of genes encoding antibiotic resistance genes and multidrug efflux pumps during stationary phase at 37°C for each isolate compared to SL476 gene expression levels at the same temperature.…”

“…The heat tolerance of SL476 was similar to that found in published data for Salmonella Enteritidis, but with more extreme tailing of the survival curve (15,47,48), while Salmonella Typhimurium ATCC 14028 had a somewhat lower heat tolerance than SL476 (not statistically significant). R1-0006 and R1-0003 were from strain JF6X01.0258, a strain that caused 186/634 outbreak illnesses, yet represented less than 1% of the Salmonella Heidelberg isolates in PulseNet prior to the start of the outbreak (28). This strain was also associated with illnesses from rotisserie chicken (28).…”

Reducing Risk of Salmonellosis through Egg Decontamination Processes

“…In 2011, the Centers for Disease Control and Prevention reported that annually there are one million cases of salmonellosis in the USA [8]. Even though several food items such as peanuts [9], beef [10], pork [8] and chicken [11] have been associated with outbreaks of salmonellosis, the primary cause is raw eggs and egg products [12,13]. According to Painter [12], in the United States from 1998 to 2008, 57% of S. Enteritidis outbreaks were linked to food products prepared using eggs.…”

Genome divergence and increased virulence of outbreak associated Salmonella enterica subspecies enterica serovar Heidelberg

“…Heidelberg in the United States. According to the CDC reports, five of these outbreaks were traced back to either chicken or turkey related products as the source of infection [13][14][15][16][17][18][19][20][21]. However, a very recent multistate outbreak caused by this serovar has been linked to contact with calves as the source of infection [22].…”

“…Previous epidemiological studies on Salmonella ser. Heidelberg have mostly focused on outbreaks associated with poultry products [23][24][25][26][27]. Most of these analyses were carried out with a limited number of isolates from a small geographical region with a limited number of strains.…”