In January 2024, a report written by the National Advisory Committee on Microbiological Criteria for Foods (NACMCF), titled, “Response to Questions Posed by the Food Safety and Inspection Service: Enhancing Salmonella Control in Poultry Products,” was published in the Journal of Food Protection. The report was adopted on November 15, 2022, and was revised in response to public comments on March 13, 2023.

NACMCF provides impartial scientific advice to federal food safety agencies, including the U.S. Department of Agriculture’s Food Safety and Inspection Service (FSIS), among others. In light of FSIS’ ongoing efforts to reduce Salmonella infections attributable to poultry, which includes a new regulatory framework that was proposed in October 2022 and elaborated upon in April 2023, the purpose of the newly published report from NACMCF is to provide guidance to FSIS and the poultry industry on types of microbiological criteria that might be used to identify and incentivize effective pre- and postharvest Salmonella intervention strategies. The report takes into consideration scientific evidence on Salmonella control in the U.S. and abroad, foodborne illness surveillance data, quantitative microbial risk assessments, and microbiological testing of indicator organisms versus Salmonella on poultry throughout the farm‐to‐fork continuum.

The Landscape of Salmonella in Poultry, and an Overview of and Recommendations for Interventions and Testing

According to the report, the infectious dose of Salmonella varies widely between serotypes, with recent data suggesting that most poultry-associated outbreaks in the U.S. involve S. Enteritidis, S. Typhimurium, S. I:4,5,12:i:‐, S. Infantis, and S. Heidelberg. Furthermore, four of the five aforementioned serotypes (all excluding S. Heidelberg) account for 83 percent of chicken‐associated illnesses in the U.S.

Vaccination against specific serotypes, such as S. Typhimurium, are common among U.S. broiler breeders, a strategy which has reduced the incidence of contamination of that serotype. However, vaccine development takes years and lags behind the shifting of predominant serotypes found in flocks. Other U.S. preharvest management practices include competitive exclusion, controlling the quality of feed, biosecurity, moisture control in poultry houses, and clean transport coops.

The relative number of salmonellosis cases in the U.S. caused by S. Typhimurium and S. Heidelberg has declined during the past 20 years, likely due in part to the commercial poultry vaccine used against S. Typhimurium also delivering cross‐protection against S. Heidelberg. Although progress has been made against these two serotypes, overall cases of salmonellosis attributed to poultry remain unchanged, suggesting that it may be necessary to develop alternate methods for controlling and detecting Salmonella that do not rely solely on serotype. Furthermore, attribution data does not specifically identify whether sources of Salmonella were whole carcasses, parts, comminuted product, or breaded raw poultry products. NACMCF underlines that more granular data will help determine if all poultry products pose the same risk and allow a targeted management program.

Qualitative testing for total Salmonella at breeder or broiler farms can be focused on environmental samples and cecal testing, but sufficiently sensitive tests and specific serotype testing are needed to determine if any changes are required to control Salmonella serovars that are most often associated with human illness. NACMCF suggests targeting highly contaminated birds for logistic slaughter (i.e., scheduling their slaughter after less contaminated flocks) or other interventions, based on results from microbial testing at farms.

Although Indicator organisms such as Enterobacteriaceae (Eb) or aerobic plate counts (APCs) have been used by industry to gauge the efficacy of process control and to measure microbial reduction on carcasses from slaughter to post-chill, some studies have shown that populations of these indicators are not directly correlated to populations of Salmonella. In light of the “conflicting and weak” correlation between the presence or levels of indicator organisms and that of Salmonella post-carcass wash, NACMCF suggests basing microbiological criteria on Salmonella enumeration.

Moreover, microbial risk assessments have shown that diverting ground turkey product which tests above a set threshold of Salmonella colony forming units (CFU) per gram, compared to current protocols (i.e. not diverting), is expected to remove product from the market that has higher chances of causing illness. Such a threshold would need to be clearly linked to health‐based targets. This concept is currently used by industry whereby poultry used in breaded and stuffed raw chicken product are enumerated for Salmonella by quantitative polymerase chain reaction (qPCR), not by targeting specific serotypes. qPCR is more actionable than most probable number (MPN) methods due to its relatively rapid time to detection.

NACMCF Recommendations to FSIS Regarding the Proposed Regulatory Framework to Reduce Salmonella Illnesses Attributable to Poultry

Key components of FSIS’s proposed regulatory framework include requiring that incoming flocks be tested for Salmonella before entering an establishment, that establishments enhance process control monitoring, and that the agency implements an enforceable final product standard. Current performance standards include all Salmonella serotypes, rather than quantification of specific highly pathogenic serotypes. NACMCF believes that an approach targeting highly pathogenic serotypes could trigger additional mitigating actions and could be more effective in diverting products that have higher infectious potential. The public health benefits of such an approach should be evaluated through a comprehensive quantitative risk assessment.

NACMCF identified a multitude of data gaps that could affect findings and recommendations to FSIS, including the need for completion of the two quantitative risk assessments for chicken and turkey, which were in progress at the time of the report’s completion. According to a summary of FSIS achievements that was published in January 2024, the quantitative risk assessments for Salmonella in chicken and turkey were completed in 2023.

NACMCF’s recommendations to FSIS, some of which FSIS may have already progressed, include:

1. Collecting appropriate data to refine food attribution models and determine which form(s) of raw poultry exposure (e.g., consuming processed, parts, whole carcasses, handling live poultry, exposure to poultry manure, and etc.) and food handler practices contribute most to salmonellosis associated with chicken and turkey
2. Expanding systematic sampling for Salmonella levels, prevalence, and serotypes on poultry preharvest (hatcheries, feed, poultry houses) and FSIS postharvest sampling (slaughter through processing), prioritizing product lines that historically are more frequently contaminated (those that are not further processed using a validated lethality step and have been linked to illness, such as comminuted poultry products, chicken parts/pieces, and breaded stuffed raw chicken products)
3. Incentivize industry to deposit anonymous, nonpunitive data on levels of indicator organisms and Salmonella prevalence, concentration, and serotypes found at various stages of processing along with practices that may mitigate contamination, and analyze this data to identify alternate process control indicators, to use in risk assessments to update performance standards, and to determine how non‐Salmonella quality indicator sampling could be established for targeting flock houses with a higher probability of contamination.
4. Every 2–3 years, compare serotypes isolated from salmonellosis patients with those isolated from poultry products to determine if intervention strategies used by industry are effective against all Salmonella serotypes or are selecting for specific serotypes
5. Develop and validate quantitative testing methods to determine if and how testing and processing scheduling can reduce the likelihood that carcasses and parts with higher levels of Salmonella that are most capable of causing illness are released into commerce
6. Complete risk assessments for chicken and turkey to assess public health impacts of different risk‐based Salmonella control strategies, including qualitative and quantitative performance standards, possibly complemented by serotype identification
7. Upon completion of the risk assessments, consider developing changes to performance standards based on the findings
8. Incentivize industry to develop, validate, and universally implement robust Salmonella mitigation programs and qualitative Salmonella testing at the breeder, hatchery, grow-out, and transport levels; targeting for conditions in houses, transport crates, and holding areas that harbor and transmit Salmonella by universal implementation of known and validated mitigation strategies
9. Reevaluate NACMCF’s report and suggestions within 3–5 years, after appropriate data have been collected and risk assessments are complete, addressing the gaps identified by the committee.