Salmonella Enteritidis Outbreaks Associated with Egg-Producing Farms Not Regulated by Food and Drug Administration's Egg Safety Rule

Introduction

Locally produced food items have seen an increase in demand but there have been limited changes in food safety interventions covering them. Locally produced eggs have become sought after by both consumers and restaurant chefs (Curtis et al., 2008; Lillywhite and Simonsen, 2014; Berkhoff et al., 2020), including targeted marketing to consumers regarding the source. This increase coincides with the recent rise in backyard poultry ownership across the United States (Behravesh et al., 2014; Elkhoraibi et al., 2014; Marmulak et al., 2015; Pires et al., 2019). These trends are, in part, owing to the belief that small farm or backyard-raised eggs are healthier or safer than their commercial counterparts (Pollock et al., 2012; Elkhoraibi et al., 2014; Pires et al., 2019). Overall, 87 outbreaks of foodborne illness associated with eggs were reported to the National Outbreak Reporting System (NORS) between 2010 and 2018 with 50 caused by Salmonella spp. (CDC, 2021).

The Food and Drug Administration (FDA) is responsible for governing policies related to shell egg production in the United States. Since enforcement of their Egg Safety Rule began in July 2010, producers with >3000 layer hens were required to register a protocol targeting decreased contamination of their eggs by Salmonella enterica serotype Enteritidis (SE) during production, storage, and transport (FDA, 2009). Many small local farms and backyard flocks have <3000 layer hens, and are not specifically regulated by the Egg Safety Rule, creating a gap that poses a public health risk. Furthermore, additional risk factors unique to smaller egg farms have also been identified in the literature, which may further exacerbate this risk. They include gaps in knowledge of proper food animal husbandry, a lack of consistent veterinary care, and a general lack of public knowledge concerning the relationship between animal contact and foodborne illness (Behravesh et al., 2014; Elkhoraibi et al., 2014; Pires et al., 2019, 2020).

Salmonella spp. are recognized by the Centers for Disease Control and Prevention (CDC) as the most common bacterial foodborne pathogen in the United States. Egg-associated salmonellosis ranks among their top five causes of outbreak-associated hospitalizations and deaths in the United States for 2017 (CDC, 2021). The role of SE in egg-associated outbreaks is well described and major regulatory initiatives have been enacted to address this food safety risk. We reviewed outbreaks of egg-associated salmonellosis in Tennessee since enforcement of the Egg Safety Rule began. We describe epidemiologic, environmental health, and laboratory findings from these outbreaks in the context of the Egg Safety Rule to illustrate the efficacy of current regulations, identify gaps, and make recommendations to prevent future outbreaks.

Methods

Outbreaks of foodborne, waterborne, and other vehicles of enteric disease in the United States are reported by local, state, and territorial health departments to CDC through NORS. Outbreaks reviewed for this study were identified using the NORS Dashboard. Search criteria included all foodborne outbreaks between 2010 and 2018 within Tennessee reporting Salmonella spp. as the etiologic agent and either “egg,” “eggs,” or “shell eggs” as an exposure. Outbreaks before July 2010 were excluded from this study because the Egg Safety Rule was not yet being enforced. Tennessee outbreaks within these search parameters were cross-referenced with surveillance and outbreak records from the Tennessee Department of the Health (TDH). Outbreaks that occurred from 2019 to 2020 were not yet published in NORS at the time of this search. Instead, the same search criteria were applied to a search of TDH records for those years.

Data were extracted from TDH records for all identified outbreaks. Documents analyzed included outbreak reports, case interview records, and communications from partnering agencies. The following items were collected: case demographics, signs and symptoms reported, food vehicles implicated, environmental findings, and laboratory findings.

Results

Four outbreaks were identified from the NORS Dashboard meeting the study criteria. After cross-referencing outbreak entries with state health department records, it was determined that two entries from 2018 represented the same outbreak. One additional outbreak from 2020 not yet available in NORS was identified using TDH records. In total, four outbreaks were selected for inclusion in the study.

All four outbreaks were caused by SE. A total of 93 egg-associated salmonellosis cases across the four outbreak events were reported (Table 1). Forty-one (44%) cases were men. Seventy-two (77%) cases occurred in patients between 20 and 49 years old. Forty-seven (51%) cases reported seeking medical care from a health care provider or visited an emergency room, and 9 (10%) cases were hospitalized. No deaths were reported. Among 86 cases for whom full symptom histories were collected, diarrhea was the most common symptom, reported by 85 (99%) cases. Abdominal cramps and fever were reported by 60 (70%) and 55 (64%) cases, respectively. Sixty-eight (79%) cases reported experiencing additional symptoms, including nausea, headache, fatigue, chills, malaise, or others. Laboratory methods included pulsed-field gel electrophoresis (PFGE) (Ribot et al., 2006), multiple locus variable-number tandem repeat analysis (MLVA) (CDC, 2016a), and whole genome sequencing (WGS) (CDC, 2016b).

Discussion

On average, TDH investigates ∼23 foodborne disease outbreaks each year. Egg-associated SE outbreaks have been detected four times in Tennessee since implementation of the Egg Safety Rule. Foodborne outbreaks are influenced by several contributing factors, including etiology, food vehicle, and regulatory policies. In addition, surveillance and laboratory methods for public health response have improved in recent years. A recent review suggested that the Egg Safety Rule has reduced the number of egg-associated outbreaks of Salmonella (Minor and Parrett, 2016). However, our findings suggest that egg-associated SE outbreaks continue to occur and are mainly associated with farms that do not meet the criteria for regulation.

Shell eggs implicated in all four outbreaks were traced to farms that were not covered by the Egg Safety Rule or were not in compliance. Both Kentucky farms implicated in 2012 and 2020 had <3000 layer hens at the time the outbreaks occurred. The Alabama farm implicated in 2018 had 2600 layer hens when last inspected and was not covered by the Egg Safety Rule at that time. However, during the outbreak, site visits revealed they had grown to >15,000 layer hens and failed to register with FDA or their state egg program. As a result, FDA issued a warning letter notifying them of their violations (FDA, 2019). Of note, the Tennessee farm implicated in 2016 housed their layer hens at three separate locations and aggregated eggs for sale. Each physical location had <3000 layer hens on the property, so the farm in question was not technically covered by the Egg Safety Rule despite having enough hens in total across all three facilities to qualify for regulation.

All SE outbreaks detected in Tennessee following enforcement of the Egg Safety Rule were associated with small, local operations. The association of SE with shell eggs is well known and these outbreaks highlight the risks posed by smaller unregulated farms. In addition, food safety has been reported as a critical motivator for where consumers purchase food items from (Smithers et al., 2008; Nonini, 2013; Feldmann and Hamm, 2015). Many consider locally produced food items to be healthier than their nationally or globally sourced counterparts, which may explain the recent rise in backyard poultry and shift toward locally sourced ingredients (Elkhoraibi et al., 2014; Lillywhite and Simonsen, 2014). However, our findings indicate that a local origin does not always correspond to a safer food product. Standard food safety precautions must still be taken regardless of a food item's source or the size of the farming operation.

Signs and symptoms reported across all outbreaks were consistent with those routinely reported for cases of salmonellosis. SE is one of the most common causes of foodborne diarrheal disease and is frequently accompanied by other signs like abdominal cramps, fever, and vomiting (Chlebicz and Śliżewska, 2018). Hematuria was reported by one case. It is unknown whether this was caused by SE or if the patient had an unrelated concurrent urinary tract infection (UTI). Foodborne UTIs are rare, but a recent study suggests this is owing to underreporting because the average incubation for one is ∼10 days longer than that of gastrointestinal illness, falling outside the timeframe specified during patient interviews (Jacobs Slifka et al., 2020). In addition, despite identifying 93 total cases, it is likely that a large proportion of cases were never captured. It is estimated that for every reported case of sporadic nontyphoidal salmonellosis, 29.3 cases go unreported or undiagnosed (Scallan et al., 2011).

Laboratory testing of stool samples and other clinical specimens was integral to confirming SE as the etiologic agent in each outbreak. Although investigators initially relied on PFGE for subtyping bacterial isolates, this gradually transitioned to WGS over the study period (Table 2). WGS has proven to be effective in determining relatedness among isolates compared with PFGE, which historically has been unable to adequately differentiate clonal organisms, like SE (Deng et al., 2015; Kozyreva et al., 2016; Besser et al., 2019). For the 2016, 2018, and 2020 outbreaks, WGS was crucial to identifying additional cases both within and outside of Tennessee which would have otherwise been difficult to identify with PFGE alone. Accordingly, WGS has become the standard for enteric surveillance, improving the identification and investigation of local clusters while also enhancing our ability to detect multistate outbreaks.

Environmental sampling can be challenging but remains an important aspect of on-farm investigations. During the 2012 and 2020 outbreaks, all environmental samples tested negative for Salmonella (Table 2). During the 2016 investigation, environmental samples were positive for SE and Salmonella Muenchen; however, the SE strain was not related to the outbreak strain detected by PFGE or WGS. In 2018, farm eggs and environmental swabs both tested positive for the outbreak strain of SE using WGS, which is the only outbreak where this occurred. Rapidly conducting environmental assessments and sampling at the suspected farm can provide critical information leading to better food safety outcomes, including reduced morbidity and mortality.

Challenges in isolating the outbreak strain from environmental samples are numerous. Contamination of eggs during the production process can occur through many pathways. An egg's internal contents can be contaminated during formation if SE has colonized the layer hen's reproductive tract (Whiley and Ross, 2015), although this is thought to be rare. External contamination of the shell can occur as the egg passes through the cloaca during oviposition or from contact with contaminants in the environment after laying (Braden, 2006). Salmonella has also been reported to penetrate the egg's shell sometimes after laying depending on factors like temperature and shell composition and permeability (Miyamoto et al., 1998; Whiley and Ross, 2015). Thus, with so many potential routes of contamination, it is possible that eggs collected for testing could have come from uninfected hens, intermittent shedders, or may have lacked contact with environmental contaminants.

Another factor to be considered is the practice of pooling in commercial food settings, where many eggs are cracked and mixed into one container for use in preparing multiple dishes (Little et al., 2008). Practices like this are considered high risk because the presence of just one contaminated egg can contaminate the entire pooled stock. When this is combined with improper cooking practices, as observed in the 2012 and 2018 outbreaks, or the use of raw eggs in prepared foods, as observed in the 2016 and 2020 outbreaks, there is potential for one contaminated egg to cause multiple cases of foodborne illness.

Finally, the nature of outbreak investigations themselves can also be a limitation. In each of these outbreaks, the time lag from when a food item was consumed to when the outbreak was detected prevented contaminated foods from being available for testing. Accordingly, a different batch of the food item in question or ingredients used to make it were tested instead. Conditions on the farm were assessed at an even later timepoint, which could explain the lack of positive environmental samples from three of the four outbreaks.

Retrospective evaluation of these outbreaks in sequence highlighted how every investigation is unique. These investigations were triggered by different signals, including routine pathogen-specific surveillance and complaint-based surveillance. Response teams were comprised of epidemiologists, environmental health specialists, and laboratorians who brought unique strengths and assets to the collaborative investigations. All four investigations were enhanced by collaboration from multiple agencies, including local and state health departments, state departments of agriculture, and federal agencies like CDC and FDA. The need for collaboration such as this during an outbreak investigation has been highlighted previously (Perret et al., 2000; Looi and Chua, 2007; Arifa et al., 2018) and, although this falls outside the intended scope of this study, we believe our findings demonstrate the utility and practicality of a comprehensive and collaborative approach.

Conclusions

Each outbreak originated from farms in which the Egg Safety Rule was not being applied. This regulatory gap poses an ongoing food safety risk if cooking measures are accidentally overlooked or willfully ignored to prepare dishes with raw ingredients. Additional factors, like the rise in backyard poultry, the trend toward locally sourced ingredients, and evolving sociocultural beliefs surrounding food safety, are also implicated. Both nationally and in Tennessee, the process for investigating foodborne disease outbreaks continues to evolve rapidly as new technologies and methodologies emerge. Public health officials working to combat enteric disease should continue to utilize the combined strengths of epidemiologic, environmental health, and laboratory techniques and foster a collaborative approach with partner agencies. Finally, food safety measures at the state and federal level should be assessed and updated to address the risk of SE in shell eggs not currently covered by the Egg Safety Rule.