The Agency is proposing to declare that NRTE but appears RTE chicken products containing Salmonella at levels of 1 colony forming unit (CFU) per gram or higher are adulterated within the meaning of the Poultry Products Inspection Act (PPIA).1 The NRTE but appears RTE chicken category includes products such as frozen chicken cordon bleu and chicken Kiev. Notably, FSIS has chosen to issue this policy change in the form of a proposed policy for which it is accepting comments, rather than as a proposed regulation or an immediately effective policy change.
Although the proposed standard of 1 CFU/g would apply to finished products, FSIS proposes to conduct verification procedures by testing the raw chicken component prior to stuffing and breading but after all other preparation procedures had been conducted on the raw chicken component. This testing would require establishments to develop microbiologically independent lotting practices for incoming raw product and to maintain control of the tested product while FSIS completes its testing. FSIS states in its proposal that it estimates negative results would routinely be available within 48 hours of the samples’ shipment to the laboratory (which FSIS anticipates would take 24 hours). FSIS estimates it would take another two to four days to confirm a positive result and return the enumeration result. Based on FSIS’s predicted timeframes, it could take seven days for an establishment to receive the enumerated results for a positive raw material sample, and the establishment would have to hold the raw material pending those results. Establishments would be permitted to divert lots that test positive for Salmonella above the 1 CFU/g threshold for use in fully cooked applications or other raw products where consumer cooking practices are more likely to mitigate risk.
The proposed determination would also require establishments to reassess their HACCP plans and update their hazard analysis. Establishments that change their production process as a result of this reassessment would need to re-validate their HACCP plan.
FSIS's Policy Justification
Historically, FSIS has not considered Salmonella an adulterant in raw poultry products because proper cooking destroys the pathogen. In its proposal, FSIS asserts that “[a]lthough the labeling of NRTE breaded stuffed chicken products has undergone significant changes over time to better inform consumers that the products are raw and to provide instructions on how to prepare them safely, these products continue to be associated with Salmonella illness outbreaks.” FSIS highlights as support for the determination numerous Salmonella illness outbreaks associated with consumption of NRTE breaded stuffed chicken products dating back to 1998. However, the Agency mentions only in passing that most of these outbreaks occurred prior to 2015.
Based on this history, FSIS has concluded that public health measures that focus primarily on product labeling and consumer handling practices are “unlikely to be effective in preventing additional foodborne illnesses associated with NRTE breaded stuffed chicken products.” As support for this conclusion, FSIS notes that 2020 consumer behavior research conducted by the Agency showed that even when RTE breaded stuffed chicken product labels included additional features designed to highlight the raw nature of the product, 22 percent of study participants confused NRTE breaded stuffed chicken products with RTE products. In addition, the Agency points to a 2022 study by the Centers for Disease Control and Prevention (CDC) that found although the products’ validated cooking instructions typically require cooking the product in an oven, half of respondents used other appliances that were less likely to ensure the product reaches the proper internal temperature.
FSIS’s Legal Justification
FSIS proposes to declare Salmonella an adulterant in NRTE breaded stuffed chicken products under two separate provisions of the PPIA. First, FSIS proposes to treat Salmonella as an added substance in these products under Section 453(g)(1), which deems added poisonous or deleterious substances to be adulterants if they “may” render product injurious to health. Second, FSIS proposes to consider these products adulterated under Section 453(g)(3), which deems products adulterated if they are unsound, unwholesome, or otherwise unfit for food.
Treating Salmonella as an “Added Substance”
FSIS proposes to consider Salmonella an “added substance” under the PPIA. FSIS’s proposed determination would change its longstanding interpretation that Salmonella is “naturally occurring” in food animals, which subjects Salmonella to a different standard under the PPIA. Under the PPIA, a poultry product is adulterated if, among other circumstances,
[I]t bears or contains any poisonous or deleterious substance which may render it injurious to health; but in case the substance is not an added substance, such article shall not be considered adulterated … if the quantity of such substance in or on such article does not ordinarily render it injurious to health.2
FSIS explains its view that although Salmonella is present in the gastrointestinal tract of live birds and in poultry skin, livers, bones, and bone marrow before processing, the pathogen is not ordinarily found in chicken muscle tissue. The Agency concludes that because processed chicken muscle may become contaminated with Salmonella from parts of the chicken that naturally have Salmonella during processing, Salmonella is added to the previously uncontaminated meat intended for use in these products, rendering it an added substance. This reasoning draws heavily on arguments presented to FSIS by several recent consumer group petitions. FSIS focuses its discussion on this specific product category and does not address whether its reasoning could be extended to other chicken products or species.
FSIS’s Proposed Bases for Treating Salmonella as an Adulterant
As proposed, FSIS would treat Salmonella as an added substance in NRTE but appears RTE breaded and stuffed chicken products. Under the PPIA, an added “poisonous or deleterious substance” adulterates a product if that added substance “may render it injurious to health.”3 21 USC 453(g)(1). The PPIA also states that poultry products may be adulterated when they are “unsound, unhealthful, unwholesome, or otherwise unfit for human food.”4 The Agency explains that with current science, the basis for Salmonella virulence is not fully understood, and “all Salmonella serotypes have the potential to cause illness.” As such, the presence of Salmonella at certain levels in the products “may render” them injurious to health and make them “unsound, unhealthful, unwholesome, or otherwise unfit for human food.”5
The proposal “tentatively concludes” Salmonella in breaded, stuffed raw chicken products at levels of 1 CFU/g or higher “may render” the products injurious to health and make them “unsound, unhealthful, unwholesome, or otherwise unfit for food” such that they are adulterated.6 In explaining its position, FSIS draws on its previous decision to declare E. coli O157:H7 and certain non-O157 Shiga toxin-producing E. coli (STEC) an adulterant in raw non-intact beef. In FSIS’s view, these E. coli strains adulterate raw non-intact beef because they “render injurious to health” what many consumers believe are fully cooked beef products. FSIS says its reasoning Salmonella in raw breaded and stuffed chicken follows the same considerations it followed for E. coli in raw non-intact beef, where it considered information on the serotypes associated with human illnesses, the infectious dose, the severity of human illnesses caused by E. coli, and consumer preparation practices associated with the products.
The Agency explains that it views Salmonella in NRTE but appears RTE breaded and stuffed chicken products similarly and considered the following factors:
- Pathogen serogroups or types associated with human illness: FSIS explains its current thinking that nearly all Salmonella serotypes can cause human illness, and that several are associated with outbreaks associates with these products. FSIS explains that current technology requires 14 days from sample collection for results to be reported for Salmonella serotypes, and the basis for Salmonella virulence is not fully understood, and so it is proposing to target all Salmonella rather than specific serotypes.
- Infectious dose: FSIS “tentatively concludes” that a concentration of lower than 1 CFU/g would not ordinarily render the product injurious to health or make it unwholesome. FSIS based this level on four factors: in FSIS’s outbreak modeling, the average Salmonella median illness dose was 36 CFU; most consumers will cook NRTE breaded stuffed chicken products to some degree; the average amount of chicken in a portion of the product is 70-88 g; and at this point, technology does not allow timely serotype pathogenicity identification.
- Severity of illness: FSIS points to the long history of documented Salmonella illness out breaks associated with the NRTE breaded stuffed chicken category and the high incidence of illnesses that required hospitalization, notably the 2021 outbreak where of 36 cases in 11 states, 12 were hospitalized. FSIS also concludes that deaths occur at a greater frequency with Salmonella illnesses than foodborne illnesses from E. coli.
- Consumer cooking practices: FSIS highlights findings from its 2020 consumer behavior research report, which it states that like raw ground beef, NRTE breaded stuffed chicken products “are frequently consumed after preparation that may not destroy pathogens in the product.”
FSIS concludes, “because Salmonella can survive ordinary handling and cooking practices for NRTE breaded stuffed chicken products, FSIS has tentatively concluded that the appropriate response to protect public health is to ensure that products contaminated with Salmonella at levels sufficient to cause human illness are excluded from commerce.” FSIS focuses the majority of its discussion on explaining why it tentatively views Salmonella as being injurious to health under Section 453(g)(1). The Agency provides little additional explanation for why the product separately would be otherwise unfit for food under Section 453(g)(3), although the Agency repeats that assertion throughout.
Cost Benefit Analysis
The Agency’s cost-benefit-analysis assesses the total estimated industry cost of the proposal at $4.33 million annually. The costs considered in the assessment include the need for establishments to hold the relevant products while waiting for the results of FSIS’s verification testing, reassessing establishment HACCP plans to reflect the new policy, and implementing a Salmonella sampling and testing program. The analysis recognizes that establishments may incur additional expenses “with actions they choose to take in response to the proposed new policy, such as HACCP plan validation, training, formula changes, process changes, and label changes,” but FSIS appears not to have included these costs in its analysis because of uncertainty about what actions establishments would take. FSIS assesses the estimated quantified benefit of one prevented outbreak-related recall being $25.85 million, concluding that “total benefits would exceed total costs if the proposed new policy prevents at least 1 outbreak-related recall every 5.96 years.”
The proposed determination has significant implications for the food industry beyond the specifically targeted category of NRTE but appears RTE breaded and stuffed chicken products. FSIS is currently evaluating its approach to Salmonella control in raw poultry through its proposed Salmonella Framework, released last Fall. That proposed framework referenced FSIS’s plan for NRTE but appears RTE breaded and stuff chicken products, and the proposed framework also draws heavily on FSIS’s policy for certain strains of E. coli in raw non-intact beef. Although FSIS in the proposed determination reserves its ability to view Salmonella differently in other raw poultry products, the approach taken in the proposed determination is highly suggestive of how FSIS might proceed with addressing Salmonella in raw poultry more broadly. Should FSIS implement this policy, especially its proposed treatment of Salmonella as an added substance in raw poultry, it could have significant implications for other raw commodities.
Comments on the proposed determination are due on June 27, 2023. A copy of the USDA press release announcing the proposed determination can be found here. Please do not hesitate to reach out with any questions in the meantime.
Authored by Brian D. Eyink and Connie Potter.
2 21 U.S.C. § 453(g)(1).
3 Id. § 453(g)(1).
4 Id. § 453(g)(3).
5 Id. §§ 453(g)(1), 453(g)(3).
6 See id.