Salmonella Braenderup Responsible for Substantial Recall of Eggs and Disruption of Operations

The FDA press release over the weekend concerning an apparent outbreak of salmonellosis attributed to a specific complex owned by the second-largest egg-production company in the U.S. raises issues extending beyond the enterprise concerned. The outbreak and investigation required application of sound epidemiology, use of highly specific whole genome sequencing of isolates from patients and the implicated flocks. The significant question is whether The FDA considered the financial results of their action on the Company and egg industry, whether justified scientifically or not, with the low impact of the outbreak.

Not all the facts are known as of today but it is hoped that transparency will be demonstrated by both the Agency and the Company concerned in the interests of knowledge and the imperative to introduce corrective action across the Industry if required.

Simon M. Shane,  Editor, EGG-NEWS 


Rose Acre Farms has voluntarily recalled approximately 200 million eggs from their Hyde County, NC. complex (P1065) following an FDA investigation. The outbreak involving 23 cases identified to date over a three to six month period from 2.4 million eggs per day over a conservative period of 45 days of consumption does not suggest either a high transmission rate or extensive contamination of eggs after washing.

Salmonella enterica Subspecies enterica Serotype Braenderup  (S. Braenderup) belongs to the C1 Serogroup expressing O:7 antigen. Previous documented outbreaks due to the pathogen have included meat pies in Switzerland (1993); chicken in Wisconsin (2001); tomatoes in a U.S. multistate outbreak (2004 through 2005); lettuce in the U.K. (2011); mangoes in a U.S. multistate outbreak in 2012 and nut butter in a U.S. multistate outbreak in 2014. 

In order to demonstrate an epidemiological relationship between the patients and the implicated complex FDA would have to establish:-

  • That all or an overwhelming proportion of the 23 patients were infected with the same strain of S. Braenderup using whole genome sequencing.
  • That the S. Braenderup isolates if present in samples taken from the farm (drag swabs, fan blades, egg belts and conveyors, cloacal swabs from hens, wash water, plant effluent) are homologous with the outbreak strain applying whole genome sequencing
  • That there is a plausible relationship between the cluster identified and the farm with respect to possible transmission.

 The voluntary recall represents the output of approximately 3 million hens or approximately 2.4 million eggs (6,600 cases) per day  extending from Julian Dates 011 (January 11th) to 102 (April 12th) 2018. It is self-evident that all but potentially a third of these eggs have been consumed.
Implicated product was distributed to ten states including the Carolinas, New Jersey, New York, Pennsylvania, Virginia and Florida. Eggs packed with the USDA AMS code of P1065 were marketed to both retail and food service customers. Brands identified included Food Lion, Great Value (Walmart), Sunshine Farms, Coburn Farms, Country Daybreak, Crystal Farms among others.

The recall resulted from investigation of a cluster of Salmonella Braenderup isolations from patients in the Northeast with records assembled on March 5th. The cases were identified over a number of months which creates doubt as to a point source. In contrast the 2010 S. Enteritidis outbreak attributed to two affiliated farms with approximately 300,000 hens operated by Jack DeCoster in Iowa generated an epi-curve with thousands of cases over two to three months. There was a rapid drop in incident cases after diversion of eggs to pasteurization. Environmental samples and eggs from the farm yielded a high proportion of S. Enteritidis isolates.  

The FDA report indicated eggs as a potential vehicle of infection with P1065 as the probable common source. On-farm investigations by the FDA in late March and early April apparently yielded “a sample containing Salmonella Braenderup from the Hyde County Egg farm facility which matched patients” It is understood that the FDA have not as yet isolated S. Braenderup from egg pools. Data relating to whole genome sequencing including homogeneity among patient and farm isolates has not been disclosed.

The identity of samples was not specified in the FDA release dated April 14th. It is important from an epidemiologic perspective to confirm that the pathogen was present in the interior of eggs denoting vertical transmission as with Salmonella Enteritidis (a Group-D serogroup). Alternatively it should be established whether the S. Braenderup was an environmental contaminant as with numerous Salmonella serotypes including Typhimurium, Hadar, Mbandaka and others which are not generally regarded as vertically transmitted. Washing of eggs in accordance with USDA protocols should remove surface contamination on the shell provided the process is carried out before penetration through the pores by motile Salmonella.

There is some weak evidence that S. Braenderup may be vertically transmitted*. In a published study  conducted on two egg-production farms in Guangdong Province S. Braenderup  was isolated from 23 of 126 environmental samples including cages, egg belts and conveyors, wash water the packing plant environment and feces. The organism was recovered from the shell and contents of eggs in the plant and at retail.

According to CDC reports S. Braenderup was isolated from children infected by day-old chicks purchased by hatcheries supplying the backyard chicken market. This suggests indirect vertical transmission most likely from fecal and hatchery contamination but not necessarily by the trans-ovarial route.

Definitive proof of transovarial transmission of S. Braenderup would require controlled studies as with Salmonella Enteritidis and the negative results with S. Heidelberg as documented in the literature. If the FDA wish to establish vertical transovarial transmission it is hoped that hens vaccinated with S. Typhimurium mutant vaccine should be used and that realistic challenge doses (102  to 10 3 CFU) should be administered.

The role of vertical transovarial transmission in this case would have to be derived from examination of egg pools form specific flocks of various ages on the implicated complex together with a structured study to demonstrate the presence of S. Braenderup in the ovary and or oviduct of a statistically relevant sample of hens shown to be intestinally colonized with the potential pathogen. 

The question of how to respond to the situation is of financial importance to Rose Acre farms. It is evident that in the short term eggs from the complex will have to be diverted to breaking and pasteurization until the extent of environmental contamination and prevalence in specific flocks is established from manure swabs and egg pools. It is known that Rose Acre Farms has breaking and pasteurization capability but not in Hyde County. This presumes transport of eggs from North Carolina to Indiana and a reverse shipment of shell eggs to the Mid-Atlantic market.

 The longer term response to the problem is more challenging. Eradication of a Salmonella infection in the environment of a three-million complex with high-rise houses will be difficult without depopulation. Perhaps with pasteurization of current production and a program of decontamination of houses as they are depleted coupled with extremely high levels of biosecurity homologous vaccines and rodent control could suppress infection until the complex is ready for conversion to an aviary system. Any long-term program should be based on an understanding of how the infection was introduced and how it persists or may be disseminated.

If the FDA satisfied the criteria to establish a cause-and-effect relationship between the cluster and the Rose Acre Farms, Hyde County Complex they were justified in requesting a voluntary recall. If the Agency reacted prematurely without appropriate data from whole genome sequencing and subsequent analysis the Agency has created a dangerous precedent for the U.S. egg-production industry through precipitous action and generatingadverse publicity.

*Long, M. et al.Recovery of Salmonella isolated from eggs and the commercial layer farms. Gut Pathology 9:97 et seq. doi: 10.1186/s13099-017-0223-8 (2017)