Salmonella Framework for Raw Poultry Products

Federal RegisterAug 7, 2024

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DEPARTMENT OF AGRICULTURE

Food Safety and Inspection Service

9 CFR Part 381

[Docket No. FSIS-2023-0028]

RIN 0583-AD96

Salmonella Framework for Raw Poultry Products

AGENCY:

Food Safety and Inspection Service (FSIS), U.S. Department of Agriculture (USDA).

ACTION:

Proposed rule and Proposed Determination.

SUMMARY:

FSIS is announcing its proposed determination that raw chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey products contaminated with certain

Salmonella

levels and serotypes are adulterated within the meaning of the Poultry Products Inspection Act (PPIA). The proposed determination would establish final product standards based on these

Salmonella

levels and serotypes and would prevent raw chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey products that contain

Salmonella

at the levels and serotypes that would render them adulterated from entering commerce. FSIS is also proposing to revise the regulations that require that all poultry slaughter establishments develop, implement, and maintain written procedures to prevent contamination by enteric pathogens throughout the entire slaughter and dressing operation to clarify that these procedures must include a microbial monitoring program (MMP) that incorporates statistical process control (SPC) monitoring methods, to require sampling at rehang instead of pre-chill, and to require that all establishments conduct paired sampling at rehang and post-chill.

DATES:

Comments on this proposal must be received on or before October 7, 2024.

ADDRESSES:

FSIS invites interested persons to submit comments on this document. Comments may be submitted by one of the following methods:

•

Federal eRulemaking Portal:

This website provides the ability to type short comments directly into the comment field on this web page or attach a file for lengthier comments. Go to:

https://www.regulations.gov.

Follow the on-line instructions at that site for submitting comments.

•

Mail:

Send to Docket Clerk, U.S. Department of Agriculture, Food Safety and Inspection Service, 1400 Independence Avenue SW, Mailstop 3758, Washington, DC 20250-3700.

•

Hand- or courier-delivered submittals:

Deliver to 1400 Independence Avenue SW, Jamie L. Whitten Building, Room 350-E, Washington, DC 20250-3700.

Instructions:

All items submitted by mail or electronic mail must include the Agency name and docket number FSIS-2023-0028. Comments received in response to this docket will be made available for public inspection and posted without change, including any personal information, to

https://www.regulations.gov.

Docket:

Go to the Federal eRulemaking Portal at

https://www.regulations.gov

for access to the rulemaking docket, including any background documents and the plain-language summary of the proposed rule of not more than 100 words in length required by the Providing Accountability Through Transparency Act of 2023. For in-person access to background documents or comments received, call (202) 720-5046 to schedule a time to visit the FSIS Docket Room at 1400 Independence Avenue SW, Washington, DC 20250-3700.

FOR FURTHER INFORMATION CONTACT:

Rachel Edelstein, Assistant Administrator, Office of Policy and Program Development, FSIS, USDA; Telephone: (202) 205-0495.

SUPPLEMENTARY INFORMATION:

Executive Summary

FSIS is responsible for verifying that the nation's commercial supply of meat, poultry, and egg products is safe, wholesome, and properly labeled. In support of this mission, FSIS established a

Salmonella

verification testing program in 1996 as part of the “Pathogen Reduction; Hazard Analysis and Critical Control Point Systems” (PR/HACCP) final rule (61 FR 38805). Among other things, the PR/HACCP final rule established

Salmonella

pathogen reduction performance standards for raw product to allow FSIS to verify whether establishments have effective process controls to address

Salmonella.

The current performance standards for young chicken and turkey carcasses, raw chicken parts, and comminuted chicken and turkey products are represented as a fraction of the maximum number of allowable

Salmonella

-positive results over a targeted number of samples collected and analyzed in a 52-week moving window. FSIS categorizes establishments based on the

Salmonella

verification sampling results and posts the performance categorization of all establishments subject to the performance standards on the FSIS website. FSIS uses

Salmonella

performance standard categorization as a basis to prioritize in-depth evaluations of failing establishments' food safety systems, including their HACCP plan and sanitation Standard Operating Procedures (SOPs).

While the results of FSIS'

Salmonella

verification sampling show that the current prevalence-based performance standards approach has been effective in reducing the proportion of poultry products contaminated with

Salmonella,

these measures have yet to have an observable impact on human illness rates. The estimated rate of human

Salmonella

infections from all sources has remained consistent over the last two decades, with over 1.3 million illnesses estimated in the United States each year. Additionally, while current

Salmonella

performance standards are designed to achieve the Department of Health and Human Services' Healthy People Initiative

targets for foodborne illness reduction, the 2010 and 2020 Healthy People targets for a reduction in

Salmonella

infections from all sources were not met. The Healthy People 2030 target is to reduce

Salmonella

infections from all sources to a national case rate of no more than 11.5 per 100,000 consumers per year. To reach this 2030 target,

Salmonella

illnesses must be reduced by 25 percent.

Launched by the U.S. Department of Health and Human Services (HHS) in 1980, the Healthy People Initiative sets out to create widely accessible plans to help organizations, communities and individuals improve public health. Each decade, HHS releases new goals after evaluating the successes and areas of growth from the previous ten years. They monitor the progress toward Healthy People's objectives using high-quality data and feedback., the HHS benchmark continues to focus on reducing poultry-based

Salmonella

infections by 25 percent, a goal that has not been reached over the last decade. The Healthy People 2030 objectives were released on August 18, 2020.

Poultry is among the leading sources of

Salmonella

foodborne illness acquired domestically in the United States.

Therefore, on October 19, 2021, FSIS announced that it was mobilizing a stronger, and more comprehensive effort to reduce

Salmonella

illnesses associated with poultry products. In the

announcement, FSIS stated that it had initiated several activities designed to gather data and information to inform and support future actions related to this new effort. FSIS charged the National Committee on Microbiological Criteria for Food (NACMCF) to provide guidance on the types of microbiological criteria the Agency might use to better prevent

Salmonella

infections associated with poultry products. The Agency also conducted a risk profile for pathogenic

Salmonella

subtypes in poultry and developed two quantitative risk assessments

—

one for

Salmonella

in chicken and one for

Salmonella

in turkey. Additionally, FSIS conducted an exploratory sampling program for young chicken carcasses to generate microbial data to help inform future policies and added quantification to its

Salmonella

testing program.

Interagency Food Safety Analytics Collaboration (FSAC). Foodborne illness source attribution estimates for 2020 for Salmonella, Escherichia coli O157, and Listeria monocytogenes using multi-year outbreak surveillance data, United States. GA and DC: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Food and Drug Administration, U.S. Department of Agriculture's Food Safety and Inspection Service. 2022. Available at:

https://www.cdc.gov/ifsac/php/annual-reports/?CDC_AAref_Val=https://www.cdc.gov/foodsafety/ifsac/annual-reports.html.

In addition to initiating these activities, on October 17, 2022, FSIS shared with stakeholders a draft regulatory framework that the Agency was considering for a new strategy to control

Salmonella

in poultry products and announced that FSIS would be hosting a virtual public meeting on November 3, 2022, to discuss the framework. The three components under consideration in the draft framework included:

Component One.

Requiring that establishments characterize

Salmonella

as a hazard reasonably likely to occur at receiving and requiring that incoming flocks be tested for

Salmonella

before entering an establishment.

Component Two.

Enhancing establishment process control monitoring and FSIS verification.

Component Three.

Implementing an enforceable final product standard that would define whether certain raw poultry products contaminated with certain levels and/or serotypes of

Salmonella

are adulterated.

The draft framework under consideration also addressed cross-cutting issues associated with testing for

Salmonella,

considerations for small and very small establishments, and data sharing. At the November 2022 public meeting, stakeholders presented oral comments on the three separate components of the draft framework and the cross-cutting issues. Stakeholders also had an opportunity to submit written comments to FSIS by December 16, 2022.

After carefully evaluating the written comments and other stakeholder input provided on the October 2022 draft framework, along with new studies and information that have become available since the Agency made the October 2022 draft framework available to the public, FSIS is proposing a new regulatory framework targeted at reducing

Salmonella

illnesses associated with poultry products. The proposed regulatory framework reflects the draft framework with some modifications.

First, consistent with Component Three of the October 2022 draft framework, FSIS is proposing final product standards that would define whether certain raw poultry products contaminated with certain

Salmonella

levels and serotypes are adulterated as defined in the Poultry Products Inspection Act (PPIA) (21 U.S.C. 451

et seq.

). Specifically, FSIS has tentatively determined that raw chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey are adulterated if they contain any type of

Salmonella

at or above 10 colony forming units/per milliliter or gram (10 cfu/mL(g)) in analytical portion (

i.e.,

mL of rinsate or gram of product) and contain any detectable level of at least one of the

Salmonella

serotypes of public health significance identified for that commodity. The proposed

Salmonella

serotypes of public health significance identified for raw chicken carcasses, chicken parts, and comminuted chicken are Enteritidis, Typhimurium, and I 4,[5],12:i:-, and for raw comminuted turkey are Hadar, Typhimurium, and Muenchen. These are the most highly virulent

Salmonella

serotypes associated with these products identified in the FSIS chicken and turkey risk assessments.

The

Salmonella

serotypes of public health significance will likely change over time as the serotypes commonly associated with human illnesses change. FSIS would continue to track annual targets for reducing the proportion of poultry samples that contain

Salmonella

serotypes of public health significance as well as data on rates for additional serotypes commonly associated with human illness to inform future revisions to the

Salmonella

serotypes of public health significance. Should FSIS finalize the proposed final product standards, the Agency intends to further evaluate and, if necessary, refine these standards as advances in science and technology related to pathogen levels, serotypes, and virulence genes become available. If FSIS finalizes the proposed final product standards, the Agency intends to re-evaluate the serotypes of public health concern every 3-5 years at a minimum and whenever new information on

Salmonella

serotypes associated with human illness become available. When evaluating the serotypes, FSIS would consider, among other things, outbreak illness data, foodborne illness surveillance data, product testing data, and animal testing data. FSIS would publicly announce any modifications to the final products standards in the

Federal Register

. FSIS requests comments on this proposed timeline for re-evaluating serotypes of public health concern.

Should FSIS finalize these proposed standards, the Agency intends to conduct a routine sampling and verification testing program for

Salmonella

in chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey in which the Agency would collect samples of raw final products and analyze them for

Salmonella

levels and serotypes to determine whether the final product is adulterated. Under the proposed

Salmonella

verification testing program, FSIS intends to only collect and analyze samples of the final raw poultry products produced by an establishment,

i.e.,

chicken carcasses to be shipped in commerce as whole chickens, chicken parts to be shipped in commerce as chicken parts, comminuted chicken to be shipped in commerce as comminuted chicken products, and comminuted turkey to be shipped in commerce as comminuted turkey products. Under this proposed determination, chicken parts subject to the final product standards would include legs, thighs, breasts, wings, quarters, and halves.

When FSIS tests a product sample for adulterants, establishments must maintain control of products tested for adulterants to ensure that the products do not enter commerce while waiting for receipt of the test results. Thus, if FSIS finalizes its proposed routine

Salmonella

verification testing program for chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey, establishments that produce these raw products would need to control and maintain the integrity of the sampled lot pending the availability of test results. If test results detect

Salmonella

at a level of 10 cfu/mL(g) or higher and at least one

Salmonella

serotype of public health significance, FSIS would consider products represented by the sampled lots to be adulterated and would issue a non-compliance record (NR). Therefore, all products in the lot represented by the sample would be prohibited from entering commerce. If any product from the lot represented by the product samples has entered and remains available in commerce, FSIS would request that the producing establishment recall the implicated products. Depending on the circumstances, in addition to issuing an NR, FSIS could take other appropriate

enforcement action as authorized in 9 CFR part 500 because the establishment would have produced and shipped adulterated product. Such actions may include immediately suspending inspection or issuing a Notice of Intended Enforcement (NOIE).

As FSIS implements the final product standards verification sampling program, the Agency has tentatively decided to phase out all current

Salmonella

performance standards for poultry. Thus, when the proposed final product verification sampling program is fully implemented, FSIS has tentatively decided that it would no longer use

Salmonella

sampling results to categorize establishments that produce poultry products and would no longer publish these establishments' performance standards categories on the FSIS website. The Agency is requesting comments on this issue.

Consistent with Component Two of the initial proposed framework, FSIS is proposing to revise the regulations in 9 CFR 381.65(g) and (h) that require that all poultry slaughter establishments develop, implement, and maintain written procedures to prevent contamination by enteric pathogens throughout the entire slaughter and dressing operation and maintain records documenting those procedures. FSIS is proposing to amend these regulations to establish new requirements pertaining to how establishments monitor and document whether their processes for preventing microbial contamination are in control. The proposed revisions are intended to clarify existing regulatory requirements related to process control monitoring in 9 CFR 381.65(g) and (h).

Under this proposal, establishments would be required to incorporate statistical process control (SPC) monitoring principles into their microbial monitoring programs (MMPs). The proposed revisions would require that establishments use only validated and fit for purpose microbial sampling and analysis procedures, generate and record statistically meaningful microbial monitoring data, set benchmarks by which to evaluate microbial monitoring data, and otherwise define the statistical methods the establishment will use to evaluate the recorded data against the predefined limits. To offset the costs associated with this proposal, eligible very small (VS) and very low volume (VLV) establishments would have access to laboratory services provided by FSIS at no charge to analyze the establishments' microbial monitoring samples for them.

FSIS is further proposing to revise the regulations to ensure that establishments comply with the corrective action provisions required under HACCP as they apply to the establishment's MMP. FSIS is proposing to specifically require establishments to, at a minimum, implement written corrective actions, including a root cause assessment, when microbial monitoring results deviate from the predefined criteria in the MMP, the other process control monitoring results, or the process control determination made for the entire HACCP system.

FSIS has developed new guidance to help establishments meet the proposed updated sampling and analysis requirements under 9 CFR 381.65(g). The new guidance includes a SPC sampling plan based on paired sampling for Aerobic Count (AC) at the rehang and post-chill locations, with a one-sided process control statistical model that charts and calculates against minimum monitoring criteria at the minimum required frequency. Establishments that incorporate the guidance into their MMPs would not be required to provide FSIS with additional scientific or technical information to support their chosen statistical methods. FSIS also is proposing to make available to all poultry slaughter establishments an electronic spreadsheet file that is pre-programmed to calculate the monitoring measures for the guidance sampling plan as results are entered.

In addition, FSIS is proposing to amend the recordkeeping requirements under 9 CFR 381.65(h) to require that establishments submit their microbial monitoring sampling results to FSIS electronically. FSIS is developing a web portal that will allow external partners to securely upload sampling information and submit it to FSIS electronically in a machine-readable format.

Should FSIS finalize this proposal, the Agency would provide a template that establishments could use to record and submit their monthly results. Establishments that use the template to record the microbial monitoring results may upload their completed template into the portal or they may enter the information manually into the portal. Establishments that do not use the template provided by FSIS to record their results would need to manually enter microbial sampling data into the portal to submit the monthly data.

In a format that provides a digital representation of data or information that can be imported and read into a computer system for further processing.

Under Component One of the October 2022 draft framework, FSIS considered whether it should require poultry slaughter establishments to characterize

Salmonella

as a hazard reasonably likely to occur at receiving and require that incoming flocks be tested for

Salmonella

before entering an establishment. This approach would require the flock to meet a predetermined target level for

Salmonella

at receiving.

FSIS considered the available scientific research as well as input from the NACMCF and concluded that, at this time, the research does not support the use of a threshold for test results at the receiving step to reduce or eliminate

Salmonella

from raw poultry products. In addition, FSIS received several comments from small poultry processors and producers and trade associations representing the meat and poultry industries that expressed concerns that the measures under consideration in Component One would impose an overwhelming burden on small producers and processors. The comments also stated that requiring that establishments determine that

Salmonella

is a hazard reasonably likely to occur at receiving is inconsistent with HACCP principles. While FSIS has decided at this time not to establish a regulatory requirement that establishments characterize

Salmonella

as a hazard reasonably likely to occur at receiving or that incoming flocks be tested for

Salmonella

before entering an establishment, the Agency is focusing on a non-regulatory approach for reducing the

Salmonella

load on incoming birds. The Agency intends to provide updated guidance on pre-harvest interventions and practices for preventing or reducing

Salmonella

colonization of live birds. The Agency also will continue to explore and develop strategies for industry to address

Salmonella

contamination risk at receiving.

Costs and Benefits of the Proposed Rule and Proposed Determination

FSIS estimates this proposal would have a net benefit of $4.1 million per year, ranging from $1.1 million to $6.7 million, assuming the proposed implementation schedule and annualizing over 10 years at a 7 percent discount rate, as discussed below (Table 1). This proposal is estimated to cost industry $16.4 million per year, ranging from $3.3 to $32.3 million. The main cost component in this proposal is the requirement that establishments subject to FSIS verification sampling for adulterants maintain control of sampled product pending test results. This cost is likely an overestimate as discussed below. Industry may also incur costs associated with HACCP plan

reassessments and changes to process control requirements.

FSIS estimates this proposal would result in benefits to society of $20.5 million per year, ranging from $4.4 million to $39.0 million. The majority of the benefits are derived from prevented illnesses of $12.9 million per year, ranging from $0.3 to $28.7 million. FSIS also estimated avoided costs from a reduction in the risk of outbreak-related recalls for industry. Additional industry actions in response to this proposal may lead to additional benefits.

Table 1—Summary of Costs and Benefits

Description

Total (million $)

Low

Medium

High

Costs:

Costs associated with the proposed rule:

Statistical Process Control

0.04

Electronic data submission

0.18

HACCP plan reassessment

0.09

0.18

0.26

Costs associated with the proposed determination:

Maintaining control of sampled product

2.11

14.47

29.26

Lost value to the industry

0.87

1.52

2.43

Microbiological sampling plan reassessment

0.02

0.04

0.08

Total costs

3.31

16.43

32.25

Benefits and Avoided Costs:

Prevented illnesses from consumption of chicken products

0.09

4.35

15.11

Prevented illnesses from consumption of comminuted turkey

0.19

8.58

13.55

Prevented outbreak-related recalls

4.16

7.56

10.34

Total benefits

4.45

20.49

39.00

Net benefits

1.14

4.06

6.75

Note:

All costs and benefits are annualized over 10 years at a 7 percent discount rate. Numbers in table may not sum to totals due to rounding.

Table of Contents

I. Background

A. Salmonella in Poultry and Human Illnesses

1. Salmonella Illnesses Attributed to Poultry

2. Salmonella Performance Standards for Poultry

3. Salmonella Performance Standards and Illnesses

B. Consideration of Need for a New Framework To Control Salmonella in Poultry

1. Petitions and Initial Stakeholder Input

2. FSIS Announces New Salmonella Effort

3. Activities Initiated To Support a New Salmonella Framework

4. Initial Measures Implemented To Address Salmonella Illnesses Associated With Consumption of Poultry Products

C. Public Meeting on Salmonella Framework Under Consideration and Public Comments

1. Public Meeting and Proposed Framework

2. Public Comments on the Proposed Framework

3. Additional Stakeholder Input

4. Overview of Modifications to the Proposed Salmonella Framework

5. Severability

II. Component Three: Proposed Final Product Standards

A. Current Salmonella Performance Standards and Consideration of an Alternative Approach

B. Pathogens as Adulterants in Raw and Not-Ready-To Eat Meat and Poultry Products

C. The Adulteration Standard for Raw Poultry Products

1. Pathogen Serogroups or Types Associated With Human Illness

2. Dose Considerations

3. Severity of Illnesses

4. Consumer Cooking Practices

E. Risk per Serving, Salmonella Levels, and Proposed Determination

1. Final Product Standards Salmonella Levels and Risk per Serving

2. Proposed Determination

F. Proposed Policy Implementation

1. HACCP Reassessment

2. Proposed Implementation and Status of Laboratory Methods

III. Component Two: Enhanced Establishment Process Control Monitoring

A. Background and Current Regulatory Requirements

B. Need To Enhance Establishment Process Control Monitoring

1. NACMCF Charge and Recommendations

2. PHIS Inspection Data

3. Exploratory Sampling Program Data

4. FSIS Risk Assessments

C. Proposals To Enhance Establishment Process Control Monitoring

1. SPC Monitoring

2. Microbial Monitoring Organism

3. Sampling Location

4. Sample Collection Monitoring Frequency

5. Corrective Actions

6. Recordkeeping Requirements

IV. Component One: Pre-Harvest Measures

A. Scientific Support and Public Comments

B. Possible Approaches To Control Salmonella at Pre-Harvest

1. National Poultry Improvement Program

2. Vaccination

3. Supply Chain Control Programs

4. Updated Pre-Harvest Guidance

V. State Programs and Foreign Government Programs

VI. Executive Orders 12866, as Amended by 14094, and 13563

VII. Regulatory Flexibility Act Assessment

VIII. Paperwork Reduction Act

IX. E-Government Act

X. Executive Order 12988, Civil Justice Reform

XI. E.O. 13175

XII. USDA Non-Discrimination Statement

XIII. Environmental Impact

XIV. Additional Public Notification

I. Background

A. Salmonella in Poultry and Human Illnesses

1. Salmonella Illnesses Attributed to Poultry

Salmonella

in poultry is a significant food safety and public health concern. The Centers for Disease Control and Prevention (CDC) estimates that non-typhoidal

Salmonella

from all sources is responsible for over 1.3 million illnesses, 26,500 hospitalized, and 420 deaths each year in the United States.

From this overall number, FSIS estimates that there are 125,115 chicken-associated and 42,669 turkey-associated foodborne

Salmonella

illnesses per year. These values are

calculated as the product of the total number of CDC FoodNet cases per year (7,600),

the share of these cases that are foodborne (66 percent)

and of domestic origin (89 percent),

and the under-diagnosis multiplier for

Salmonella

(24.3),

then dividing by the FoodNet catchment area (15 percent).

Finally, this number is multiplied by the portion the Interagency Food Safety Analytics Collaboration (IFSAC) estimates is attributable to chicken (17.3 percent) or turkey (5.9 percent).

Uncertainty remains in the FSIS estimation of chicken- and turkey-associated foodborne

Salmonella

illnesses per year. These illness estimates are subject to the same limitations encountered with other illness estimates.

Nevertheless, FSIS believes these are the best available estimates.

Collier SA, Deng L, Adam EA, et al. Estimate of Burden and Direct Healthcare Cost of Infectious Waterborne Disease in the United States. Emerging Infectious Diseases. 2021;27(1):140-149.

https://doi.org/10.3201%2Feid2701.190676.

Collins JP, Shah HJ, Weller DL, et al. Preliminary Incidence and Trends of Infections Caused by Pathogens Transmitted Commonly Through Food—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2016-2021. MMWR Morb Mortal Wkly Rep 2022;71:1260-1264. DOI:

https://doi.org/10.15585/mmwr.mm7140a2. Note: the most recent annual FoodNet report was used for the total estimated FoodNet cases annually.

Beshearse E, Bruce BB, Nane GF, Cooke RM, Aspinall W, Hald T, et al. Attribution of Illnesses Transmitted by Food and Water to Comprehensive Transmission Pathways Using Structured Expert Judgment, United, States. Emerg Infect Dis. 2021;27(1):182-195.

https://doi.org/10.3201/eid2701.200316.

Note: This article represented a recent appraisal of the foodborne share of all

Salmonella

illnesses.

Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011 Jan;17(1):7-15. doi: 10.3201/eid1701.p11101. PMID: 21192848; PMCID: PMC3375761. Note: This article outlines the general approach to estimating the burden of domestic foodborne illnesses. It provides an estimate for share of foodborne illnesses associated with foreign travel (11%) that was supported in the more recent Collins et al. (2022) article referenced above.

Ebel, E.D., Williams, M.S., & Schlosser, W.D. (2012). Parametric distributions of underdiagnosis parameters used to estimate annual burden of illness for five foodborne pathogens. J Food Prot, 75, 775-778.

https://doi.org/10.4315/0362-028X.JFP-11-345.

Note: This article estimated parametric distributions for uncertainty about the under-diagnosis multiplier based on the Scallan et al. (2011) model assumptions.

Scallan et al. (2011).

Interagency Food Safety Analytics Collaboration. Foodborne illness source attribution estimates for 2020 for Salmonella, Escherichia coli O157, and Listeria monocytogenes using multi-year outbreak surveillance data, United States. GA and DC: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Food and Drug Administration, U.S. Department of Agriculture's Food Safety and Inspection Service. 2022. Annually, IFSAC releases a report that estimates foodborne illness source attribution for major commodity groups, including

Salmonella

in poultry products. At the time this proposal was developed, the 2019 IFSAC attribution estimates were the most recent data available. IFSAC released a new annual report in November 2023, which includes attribution estimates for 2020. In the 2023 report, IFSAC estimated that 18.6 percent of

Salmonella

illnesses are attributed to chicken products and 5.5 percent to turkey products, for a total 24.1 percent attributed to poultry products. FSIS intends to incorporate the 2023 report attribution estimates if this rule becomes final.

Illness estimates from any risk assessment model are limited by uncertainty, simply because they are models. As explained by Food and Agriculture Organization of the World Health Organization (FAO/WHO), “uncertainty is a property of the methodology and data used. Assessments with different methodologies and data will have different levels of uncertainty regarding their outputs. An understanding of uncertainty is important because it provides insight into how the lack of knowledge can affect decisions.”

See

FAO/WHO

Microbiological Risk Assessment Guidance for Food (MRA 36)

at 206. FAO/WHO goes on to say, “It is the risk managers' role to decide if the uncertainty of a risk assessment output allows for a decision to be made or not.”

Id.

FSIS fully explored uncertainty in its risk assessment models to allow risk managers to make a fully informed decision. Full details are on pages 116-128 of the chicken risk assessment and pages 94-99 of the turkey risk assessment. The code for these analyses has also been provided.

Salmonella

illnesses associated with poultry also represent a considerable economic burden, particularly when accounting for not just the direct medical costs, but also productivity losses, lost life expectancy, chronic illness, and other associated pain and suffering. A recent study estimates that the economic costs of

Salmonella

illnesses in the United States associated with chicken is $2.8 billion annually.

Scharff R.L. Food Attribution and Economic Cost Estimates for Meat and Poultry-Related Illnesses. Journal of Food Protection. 2020; 83(6): 959-967.

2. Salmonella Performance Standards for Poultry

FSIS is responsible for verifying that the nation's commercial supply of meat, poultry, and egg products is safe, wholesome, and properly labeled. In support of this mission, FSIS began its

Salmonella

verification testing program with the PR/HACCP final rule, published on July 25, 1996 (61 FR 38806). Among other things, the PR/HACCP final rule established

Salmonella

pathogen reduction performance standards for establishments that slaughter selected classes of food animals and/or that produce selected classes of raw ground products.

The purpose of the

Salmonella

performance standards for raw product is to allow FSIS to verify whether establishments have effective process controls to address

Salmonella.

Since publishing the PR/HACCP final rule, FSIS has updated the performance standards for poultry products through a series of

Federal Register

notices.

When FSIS initially implemented the

Salmonella

performance standards, the regulations authorized FSIS to suspend inspection if an establishment failed to take the corrective actions necessary to comply with the performance standards, or if an establishment failed to meet the standards on the third consecutive series of FSIS-conducted tests for that product. However, the Agency's ability to directly enforce the pathogen reduction performance standards has been limited since 2001, after a ruling by the U.S. Court of Appeals for the Fifth Circuit in

Supreme Beef Processors, Inc.

USDA,

275 F.3d 432 (5th Cir. 2001). In that case, the court enjoined FSIS from suspending inspection services against a meat grinding operation for failure to meet the

Salmonella

performance standards. Since that time, FSIS has used

Salmonella

failures as a basis to conduct an in-depth evaluation of the establishment's food safety systems, including its HACCP plan and sanitation SOPs.

See

Salmonella Verification Sample Result Reporting: Agency Policy and Use in Public Health Protection

(71 FR 9772, Feb 27, 2006);

New Performance Standards for Salmonella and Campylobacter in Young Chicken and Turkey Slaughter Establishments: Response to Comments and Announcement of Implementation Schedule

(76 FR 15282, Mar 21, 2011);

New Performance Standards for Salmonella and Campylobacter in Not-Ready-to-Eat Comminuted Chicken and Turkey Products and Raw Chicken Parts and Changes to Related Agency Verification Procedures: Response to Comments and Announcement of Implementation Schedule

(81 FR 7285, Feb 11, 2016);

Changes to the Salmonella and Campylobacter Verification Testing Program: Revised Categorization and Follow-Up Sampling Procedures

(83 FR 56046, Nov 9, 2018).

FSIS has established

Salmonella

performance standards for young chicken and turkey carcasses, raw chicken parts, and comminuted chicken and turkey products. The current performance standards are expressed as a fraction of the maximum number of allowable

Salmonella

-positive results over a targeted number of samples collected and analyzed in a 52-week moving window (see Table 2). FSIS categorizes establishments based on the

Salmonella

verification sampling results and posts the categorization of all establishments subject to the performance standards on the FSIS website.

15 16

In addition, FSIS schedules follow-up verification sampling, a Public Health Risk Evaluation (PHRE),

and possibly a Food Safety Assessment (FSA)

for establishments that do not meet the pathogen reduction performance standards. If, after 90 days, an establishment has not been able to regain process control, as determined from FSIS' follow-up sampling and from the results of the PHRE or FSA, and the establishment has not taken corrective actions, FSIS may take enforcement actions, such as by issuing a NOIE or by suspending inspection, under the conditions and according to the procedures described in 9 CFR part 500 (81 FR 7285, 7289). FSIS does not issue an NOIE or suspend inspection based solely on the fact that an establishment did not meet a performance standard.

Salmonella

Categorization of Individual Establishments for Poultry Products at:

https://www.fsis.usda.gov/science-data/data-sets-visualizations/microbiology/salmonella-verification-testing-program-monthly.

The category definitions under verification sampling are as follows:

• Category 1: Establishments that have achieved 50 percent or less of the maximum allowable percent positive during the most recently completed 52- week moving window;

• Category2: Establishments that meet the maximum allowable percent positive but have results greater than 50 percent of the maximum allowable percent positive during the most recently completed 52-week moving window; and

• Category 3: Establishments that have exceeded the maximum allowable percent positive during the most recently completed 52-week moving window.

The PHRE is an analysis of establishment performance based on “For-cause” and “Routine risk-based” criteria, FSIS Directive 5100.4 Revision 2—Public Health Risk Evaluation Methodology (

usda.gov

The purpose of an FSA is to conduct a risk-based, targeted review of establishment food safety systems to verify that the establishment is able to produce safe and wholesome meat or poultry products in accordance with FSIS statutory and regulatory requirements. FSIS Directive 5100.1—Food Safety Assessment Methodology (

usda.gov

Table 2—Salmonella Performance Standards for Poultry Products

Product

Performance standard *

Maximum

acceptable

percent

positive

Minimum number of samples to

assess process

control

Broiler Carcasses

5 of 51

9.8

Turkey Carcasses

4 of 56

7.1

Comminuted Chicken

13 of 52

25.0

Comminuted Turkey

7 of 52

13.5

Chicken Parts

8 of 52

15.4

* The performance standard is represented as a fraction of the maximum allowable positives over the target number of samples collected and analyzed in a 52-week window.

3. Salmonella Performance Standards and Illnesses

The current

Salmonella

performance standards are based on risk assessments

and are designed to achieve the Healthy People targets for foodborne illness reduction. When FSIS implemented the performance standards, the Agency expected that there would be an observed reduction in

Salmonella

illnesses rates because a smaller proportion of certain raw poultry products would likely be contaminated with

Salmonella

than had been the case without standards (81 FR 7285). The results of FSIS'

Salmonella

verification sampling show that the current prevalence-based performance standards approach has been effective in reducing

Salmonella

contamination in poultry.

20 21 22

However, these measures have yet to have an observable impact on

Salmonella

illnesses. With respect to foodborne illness reduction goals, the Healthy People 2020 objectives had aimed to reduce the annual number of foodborne illnesses caused by

Salmonella

from 15.0 per 100,000 population in 2006-2008

. However, the CDC estimated that in 2019, Americans experienced 17.1 per 100,000 population

Salmonella

illnesses.

This represents an increase of 14 percent from the 2006-2008 baseline. As discussed below, there are likely several reasons why the reduction in

Salmonella

contamination in poultry products has not resulted in an observable impact on

Salmonella

illnesses.

Ebel, E.D., Williams, M.S., Golden, N.J., Marks, H.M., 2012. Simplified framework for predicting changes in public health from performance standards applied in slaughter establishments. Food Control 28, 250-257; Williams, M.S., Ebel, E.D., Vose, D., 2011. Framework for microbial food-safety risk assessments amenable to Bayesian modeling. Risk Analysis 31, 548-565.

Ebel E.D., Williams M.S., and Schlosser W.D. (2017). Estimating the Type II error of detecting changes in foodborne illness via public health surveillance.

Microbial Risk Analysis

7: 1-7.

https://doi.org/10.1016/j.mran.2017.10.001.

Ebel, ED and Williams MS (2020). Assessing the effectiveness of revised performance standards for Salmonella contamination of comminuted poultry.

Microbial Risk Analysis

14:100076.

https://doi.org/10.1016/j.mran.2019.05.002.

Williams MS, Ebel ED, Golden NJ, Saini G, Nyirabahiizi E, and Clinch N (2022). Assessing the effectiveness of performance standards for Salmonella contamination of chicken parts.

International Journal of Food Microbiology

378: 109801.

https://doi.org/10.1016/j.ijfoodmicro.2022.109801.

HHS Office of Disease Prevention and Health Promotion archive. Healthy People 2020 at:

https://wayback.archive-it.org/5774/20220414163116/https://www.healthypeople.gov/2020/topics-objectives/topic/food-safety/objectives.

Tack DM, Ray L, Griffin PM, et al. Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food—Foodborne Disease Active Surveillance Network, 10 U.S. Sites, 2016-2019, MMWR Morb Mortal Wkly Rep 202;69:509-514. Available at:

https://www.cdc.gov/mmwr/volumes/69/wr/mm6917a1.htm#T1_down.

With respect to

Salmonella

illnesses associated with chicken and turkey, one study found that the proportion of outbreaks associated with these commodities was essentially unchanged from 1998-2017 and that both the proportion of outbreaks and number of outbreaks associated with chicken remained essentially constant.

During that period, the per capita annual consumption for pork, beef, and turkey all declined between 9 percent and 22 percent, while annual consumption of chicken increased by 15 percent.

Williams, M.S., & Ebel, E.D. (2022). Temporal changes in the proportion of

Salmonella

outbreaks associated with 12 food commodity groups in the United States.

Epidemiology and infection, 150,

e126.

https://doi.org/10.1017/S0950268822001042.

The overall findings of another study indicated declining trends in illness due to

Salmonella

serotypes associated with poultry and increasing trends in illness due to

Salmonella

serotypes not associated with poultry.

However, illness attribution was not an objective of the analysis. Thus, the observed illness declines may have been caused by reduced risk in non-poultry sources that have poultry-like serotype profiles.

Powell M.R. (2023). Trends in reported illnesses due to poultry-and nonpoultry associated Salmonella serotypes; United States 1996-2019.

Risk Analysis. https://doi.org/10.1111/risa.14181.

The Healthy People 2030 target is to reduce the

Salmonella

illness national case rate of 15.3 per 100,000 population in 2016-2018 by 25 percent, or to no more than 11.5 per 100,000 population per year.

Thus, to reach the 2030 target, illnesses must be reduced by 25 percent. Although this target is for

Salmonella

illnesses from all sources, FSIS has adopted the same target for foodborne illnesses linked to FSIS-regulated products and aims to reduce these

Salmonella

illnesses by 25 percent. To move closer to achieving this target, FSIS has determined that it will need to adopt a new approach to more effectively reduce foodborne illness associated with FSIS-regulated products, starting with poultry as one of the leading food sources.

HHS Office of Disease Prevention and Health Promotion archive. Healthy People 2030 at:

https://health.gov/healthypeople/objectives-and-data/browse-objectives/foodborne-illness/reduce-infections-caused-Salmonella-fs-04/data?group=None&state=United+States&from=2016&to=2018&populations=&tab=data-table#data-table.

B. Consideration of Need for a New Framework To Control Salmonella in Poultry

1. Petitions and Initial Stakeholder Input

Consumer advocacy organizations and other stakeholders have noted that the Healthy People

Salmonella

reduction targets have not been met and have submitted petitions and letters to FSIS requesting that the Agency revise its current approach for reducing

Salmonella

illnesses associated with poultry. For example, in January 2020, Marler Clark LLP submitted a petition on behalf of several individuals and consumer advocacy organizations requesting FSIS to issue an interpretive rule to declare 31

Salmonella

serotypes that have been associated with foodborne illness outbreaks to be adulterants of all meat and poultry products.

According to the petition, such action is needed to protect the health and welfare of consumers by encouraging the meat and poultry industry to engage in more effective oversight measures and create and implement effective preventative measures.

Marler Clark LLP petition # 20-01 “Petition for an Interpretive Rule Declaring `Outbreak' Serotypes of

Salmonella enteritica

subspecies to be Adulterants” dated January 19, 2020. Available at:

https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella-serotypes

In May 2022, FSIS denied the petition without prejudice, citing a lack of sufficient data available to support the sweeping actions requested in the petition. In the response, FSIS agreed that an updated

Salmonella

strategy is necessary to reduce

Salmonella

illnesses associated with poultry and described how FSIS was working towards gathering data and information necessary to support a revised strategy.

FSIS Final Response to Petition #20-01, May 31, 2022. Available at:

https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella-serotypes

On January 25, 2021, the Center for Science in the Public Interest (CSPI) and other consumer advocacy organizations petitioned FSIS to establish enforceable standards targeting

Salmonella

types of greatest public health concern and all

Campylobacter

in poultry.

Referencing the Healthy People reduction goals, the petition asserted that FSIS' current performance standards have not been effective in reducing

Salmonella

illnesses because they aim to reduce the prevalence of all

Salmonella

rather than prioritizing control efforts for the

Salmonella

serotypes most likely to make people sick. The petition laid out several suggestions for standards that FSIS could use to address

Salmonella

in poultry. The petition recommended that FSIS work with stakeholders and other public health agencies to establish enforceable final product standards to target

Salmonella

serotypes of greatest public health concern with an aim to eliminate these strains from poultry products over time. The petition also suggested that FSIS consider revising the current prevalence-based

Salmonella

performance standard to provide for quantitative testing and add

Salmonella

levels to the performance standards criteria to better ensure that when

Salmonella

is present on a product, it is present at low levels less likely to cause human illness. The petition asserted that FSIS is authorized to deem poultry products that contain virulent

Salmonella

strains and that contain pathogen levels above a set threshold to be adulterated under the PPIA because more virulent serotypes and certain levels of

Salmonella

are more likely to render poultry products injurious to health as defined in 21 U.S.C. 453(g)(1).

While the CSPI requested that FSIS take actions related to both

Salmonella

and Campylobacter, FSIS is currently focusing on re-evaluating its approach to prevent

Salmonella

illnesses associated with poultry.

CSPI petition #21-01, “Petition to Establish Enforceable Standards Targeting

Salmonella

Types of Greatest Public Health Concern while Reducing all

Salmonella

and

Campylobacter

in Poultry, and to Require Supply Chain Controls” (January 25, 2021) at:

https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest.

The 2021 CSPI petition also requested that FSIS initiate rulemaking to require that poultry establishments identify and control foodborne hazards within their supply chains, including

Salmonella.

The petition stated that supply chain interventions may include targeted vaccines developed for specific

Salmonella

serotypes and purchasing chicks from suppliers certified to be free of priority serotypes. The petition asserted that FSIS is authorized to require supply chain controls through the current HACCP regulations, which direct establishments to address, as appropriate, hazards both introduced in the establishment and introduced outside the establishment, including food safety hazards that occur before entry into the establishment (9 CFR 417.2). The petition also asserted that FSIS has authority to verify the effectiveness of supply chain controls under the PPIA's antemortem inspection authority, which requires FSIS to conduct an antemortem inspection in each official establishment processing poultry or poultry products for commerce or otherwise subject to inspection under the PPIA “where and to the extent considered . . . necessary,” “[f]or the purpose of preventing the entry into or flow or movement in commerce of . . . any poultry product which is capable of use as human food and is adulterated” (21 U.S.C. 455(a)). FSIS has not yet responded to the 2021 CSPI petition but has considered the issues raised in developing this proposal.

In September 2021, FSIS received a letter from the Food Safety Coalition (FSC), a coalition of several food safety leaders, public health and consumer advocates, scientists, and members of the food industry. Like the CSPI petition, the FSC letter noted that although FSIS' current prevalence-based pathogen reduction performance standards have led to reduced occurrence of

Salmonella

contamination in poultry products, the Healthy People 2020 goals set by the Department of Health and Human Services in 2010 for lowering

Salmonella

and

Campylobacter

illness rates were not being met. The FSC letter stated that the likely reason is that FSIS' current

Salmonella

performance standards do not effectively target the particular types of

Salmonella

and products containing

Salmonella

levels that pose the greatest risks of illness. The letter stated that a new approach is needed to achieve the new Healthy People 2030

Salmonella

illness rate target and presented several suggested changes to help reduce the rates of foodborne illness. The proposed changes recommended by the FSC included establishing modernized enforceable pathogen standards that “invite innovation,” as well as modernizing the HACCP framework to address risk reduction across the full production process, including defining the responsibility of poultry processors to consider pre-harvest practices and interventions in their HACCP plans.

Food Safety Coalition Letter, September 2, 2021. Available at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry.

2. FSIS Announces New Salmonella Effort

After considering the available data on

Salmonella

illnesses associated with poultry as well as the initial stakeholder input discussed above, on October 19, 2021, FSIS announced that it was mobilizing a stronger, and more comprehensive effort to reduce

Salmonella

illnesses associated with poultry products.

In the

announcement, FSIS explained that the Agency would be initiating several key activities to gather the data and information necessary to support future action and move closer to the national target of a 25 percent reduction in

Salmonella

illnesses. The announcement also stated that FSIS intended to seek stakeholder feedback on specific

Salmonella

control and measurement strategies as well as using data to determine if there are other approaches to reduce

Salmonella.

The announcement noted that the effort would leverage USDA's strong research capabilities and highlighted that FSIS would ask the National Advisory Committee for Microbiological Criteria in Foods (NACMCF) to advise the Agency on how it can build on the latest science to improve its approach to

Salmonella

control. The announcement emphasized that FSIS would work closely with stakeholders on informing and implementing key activities of this framework.

USDA Press Release, “USDA Launches New Effort to Reduce

Salmonella

Illnesses Linked to

Poultry” (October 19, 2021) at:

https://www.usda.gov/media/press-releases/2021/10/19/usda-launches-new-effort-reduce-salmonella-illnesses-linked-poultry.

Following this announcement, the Coalition for Poultry Safety Reform, a multistakeholder coalition that includes individuals and organizations representing consumers, victims of foodborne illness, food safety scientists, food safety officials, and members of the poultry industry, submitted a letter to the USDA Deputy Under Secretary for Food Safety in 2022 expressing support for a new effort to address

Salmonella.

The letter requested that FSIS focus its efforts on developing new regulatory standards related to

Salmonella

covering both products and supply chains and that these standards be informed by a risk assessment based on existing data.

The letter recommended that FSIS adopt enforceable product standards aimed at reducing risk of illness and develop and conduct a risk assessment to understand illness reduction benefits of various product standards.

Coalition for Poultry Safety Reform Letter, February 2, 2022. Available at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry.

3. Activities Initiated To Support a New Salmonella Framework

After FSIS announced its new initiative to reduce

Salmonella

illnesses associated with poultry products, the Agency initiated several activities designed to gather data and information to inform and support future actions related to this new effort.

National Advisory Committee Charge.

On October 20, 2021, FSIS announced a public meeting of NACMCF from November 17, 2021, to November 19, 2021, to discuss, among other things, a new charge focused on enhancing

Salmonella

control in poultry products.

Specifically, FSIS charged the NACMF Subcommittee on Enhancing

Salmonella

Control in Poultry Products to provide guidance on the overarching risk management question: What types of microbiological criteria (

e.g., Salmonella

performance standards) might FSIS use to encourage reductions in

Salmonella

in poultry products so that they are more effective in preventing human

Salmonella

infections associated with these products?

FSIS also requested that the Subcommittee provide guidance on nine additional specific risk management questions. On April 25, 2022, NACMCF held a Subcommittee meeting for the workgroups addressing each of the questions in FSIS' charge to provide an update to the entire Subcommittee on their progress and to look at the overall timeline for completing the work of the Subcommittee.

On November 15, 2022, NACMCF held a virtual public meeting to discuss and vote on the Subcommittee's report on

Enhancing Salmonella Control in Poultry Products,

which had been posted to the FSIS website on November 1, 2022.

NACMCF adopted the final report pending finalization with consideration given to oral comments provided at the virtual public meeting and written comments submitted as directed in a

Federal Register

notice announcing the public meeting.

The comment period for the NACMCF report was scheduled to close on November 15, 2022, but was extended to December 30, 2022, to provide 60 days for public review.

After considering the public comments, NACMCF finalized its report on March 13, 2023. The final report “Response to Questions Posed by the Food Safety and Inspection Service: Enhancing

Salmonella

Control in Poultry Products” (referred to as the 2023 NACMCF report in this document) is available to the public on the FSIS website at:

https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.

National Advisory Committee Meeting on Microbiological Criteria for Foods (NACMF) Public Meeting —November 2021. Available at:

https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-2.

2021-2023 National Advisory Committee Meeting on Microbiological Criteria for Foods (NACMF); FSIS Charge: Enhancing

Salmonella

Control in Poultry Products Available at:

https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.

NACMCF FSIS Charge: Enhancing

Salmonella

Control in Poultry, April 25, 2022. Available at:

https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-fsis.

Public Meeting; National Advisory Committee on Microbiological Criteria for Food, Nov 15, 2022. Available at:

https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-national-advisory-committee-microbiological-criteria.

Public Meeting National Advisory Committee on Microbiological Criteria for Food (87 FR 64001). Available at:

https://www.fsis.usda.gov/policy/federal-register-rulemaking/federal-register-notices/public-meeting-national-advisory.

FSIS Constituent Update—Nov 10, 2022:

Deadline Extended to Comment on NACMCF Document.

Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-november-10-2022.

Pilot Projects.

In December 2021, FSIS announced in its

Constituent Update

that the Agency was inviting poultry slaughter and processing establishments to submit proposals for pilot projects that will test different control strategies for

Salmonella

contamination in poultry products.

The announcement explained that pilot projects would last for a defined period, during which establishments would experiment with new or existing pathogen control and measurement strategies and share data collected during the pilots with FSIS. The announcement included instructions on how interested establishments could submit proposals for pilots to FSIS. FSIS intended to analyze the data generated under the pilots to determine whether it supports changes to FSIS' existing

Salmonella

control strategies.

FSIS Constituent Update—Dec 3, 2021:

FSIS Seeking Proposals for Pilot Projects to Control Salmonella in Poultry Slaughter and Processing Establishments.

Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-december-3-2021.

Since March 2023, FSIS has granted pilot projects to 9 establishments to examine the merits and logistics of excluding

Salmonella

poultry vaccine strains from the FSIS

Salmonella

performance categorization calculations. After evaluating the data collected under these pilots, on March 1, 2024, FSIS announced that beginning April 1, 2024, it intends to exclude current commercial vaccine subtypes confirmed in FSIS raw poultry samples from the calculation used to categorize establishments under the raw poultry

Salmonella

performance standards.

This action is intended to remove barriers to the use of vaccination as an important pre-harvest intervention to

control

Salmonella

in poultry. A summary report of the data from these pilots is posted on the Pilot Projects:

Salmonella

Control Strategies page of the FSIS website at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot.

FSIS Constituent Update—March 1, 2024:

FSIS Intends to Exclude Vaccine Strains from the FSIS Salmonella Performance Categorization

at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-march-1-2024.

On September 23, 2023, FSIS granted a pilot to 2 establishments to examine the merits of using preharvest results to optimize establishment interventions.

The data generated under the pilot will be shared with and analyzed by FSIS to determine whether it supports changes to FSIS'

Salmonella

control strategies.

Pilot Projects:

Salmonella

control strategies. Current

Salmonella

Pilot Participants available at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot.

Research and Science Roundtable.

On February 15, 2022, FSIS held a research and science roundtable on

Salmonella

in poultry.

The intent of the roundtable was to convene research scientists to discuss the scientific support for various potential components of a revised strategy for

Salmonella

control in poultry. Among the topics discussed at the roundtable were: research on surveillance and risk assessments to evaluate the public health impact of the presence of

Salmonella

serotypes of concern and levels of contamination at production; research on

Salmonella

serotype dynamics in poultry production; research to identify pre-harvest food safety challenges and solutions; research modeling and correlation analysis work on pre-harvest in poultry; research on interventions to control

Salmonella

in preharvest and postharvest poultry production; and research in the area of microbial biomapping of indicators and pathogenic loads throughout the processing chain and using pre-harvest and post-harvest quantification data to develop SPC programs. The presentations on these topics and other materials associated with the research roundtable are available to the public on the FSIS website at:

https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable

Salmonella

in Poultry: Research and Science Roundtable. Available at:

https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable.

Exploratory Sampling Program and New Salmonella Quantification System.

In April 2022, FSIS initiated an exploratory program that expanded young chicken carcass sampling at establishments subject to the young chicken carcass performance standard.

The purpose of the exploratory sampling program was to generate microbial data to inform the Agency's effort to reduce

Salmonella

illnesses attributable to poultry. Under the program, in addition to the FSIS

Salmonella

verification sample already collected at post-chill, FSIS inspection program personnel (IPP) began collecting a second carcass sample at rehang from the same flock. In addition, FSIS IPP were instructed to collect the regularly scheduled National Antibiotic Resistance Monitoring System (NARMS) cecal samples from the same flock as the rehang and post-chill samples. The samples collected under the exploratory sampling program were initially analyzed for the presence of

Salmonella

and AC. FSIS IPP also completed a questionnaire at the time they collected exploratory samples to collect data on pre-harvest and slaughter interventions applied to the same flocks. A report on the exploratory sampling results is available at:

https://www.regulations.gov/docket/FSIS-2023-0028.

FSIS Constituent Update—April 22, 2022:

FSIS Expands Salmonella Sampling for Young Chicken Carcasses.

Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-april-22-2022.

In August 2022, FSIS announced that FSIS laboratories would begin using new technology to quantify

Salmonella

in raw poultry rinses and updated the exploratory sampling program for young chickens to quantify confirmed

Salmonella

positive rehang and post-chill carcass results using the new quantification system.

These analyses were in addition to the whole genome sequencing (WGS) that FSIS had already been performing on confirmed

Salmonella

-positive post-chill carcass samples.

FSIS Constituent Update—Aug 5, 2022:

FSIS to include Salmonella Quantification in all Poultry Rinse Samples.

Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-august-5-2022-0.

FSIS Notice 44-22,

Revised Young Chicken Exploratory Sampling Program,

Aug 11, 2022.

On January 30, 2023, FSIS added

Salmonella

quantification testing and AC indicator analyses to chicken part rinsates.

FSIS added these two analyses to comminuted chicken testing on February 27, 2023, and to comminuted turkey on April 3, 2023.

Salmonella

quantification is a significant step in updating the diagnostic capabilities of FSIS' food testing laboratories. The data generated from the new quantification system along with the data collected from the young chicken carcass exploratory sampling program were used to help inform the policies discussed in this document, including the quantitative microbial risk assessments to evaluate

Salmonella

in raw poultry discussed below. The data generated from the quantification system have also been added to FSIS' quarterly dataset release and are available at:

https://www.fsis.usda.gov/science-data/data-sets-visualizations/laboratory-sampling-data.

FSIS Constituent Update—Feb 3, 2023: FSIS to Expand

Salmonella

Enumeration and Aerobic Count Indicator Testing to Other Poultry Products. Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-february-3-2023.

Notice 83-23,

New Sampling Instructions and Testing for Chicken Parts and NRTE Comminuted Poultry,

Feb 3, 2023. Available at:

https://www.fsis.usda.gov/policy/fsis-notice/08-23.

Risk Profile.

In May 2022, FSIS initiated a risk profile for

Salmonella

subtypes in poultry linked to foodborne illness. FSIS developed the risk profile to provide information on whether certain serotypes or subtypes of

Salmonella

should be considered as adulterants in specific poultry products within the meaning of the PPIA (21 U.S.C. 453(g)). The risk profile involved a comprehensive systematic review of literature and supporting data designed to provide responses to the following six risk management questions:

1. What

Salmonella

serotypes or subtypes are linked to foodborne illness or outbreaks from consuming specific raw or not-ready-to-eat chicken or turkey products?

2. Are these

Salmonella

serotypes or subtypes of concern present in live chickens, live turkeys, and poultry products?

3. Can exposure to a small number of these

Salmonella

serotypes or subtypes of concern result in foodborne illness?

4. Can exposure to these

Salmonella

serotypes or subtypes of concern cause severe, debilitating health outcomes?

5. How can these

Salmonella

serotypes or subtypes of concern be differentiated from other

Salmonella

subtypes?

6. Would ordinary consumer handling or preparation practices affect exposure to

Salmonella

serotypes or subtypes of concern?

The risk profile was submitted for independent peer-review

and updated in response to peer review comments. The results of the risk profile and how they were used to inform specific measures proposed in this document are discussed below. The final

Risk Profile for Pathogenic Salmonella in Poultry

(referred to as the 2023 risk profile in

this document) is available at:

https://www.regulations.gov/docket/FSIS-2023-0028.

Peer Review Plan: Risk Profile for Salmonella Subtypes in Poultry Products Linked to Foodborne Illness (usda.gov).

Risk Assessments FSIS Developed to Inform Rulemaking.

FSIS conducted two new quantitative microbial risk assessments, one for

Salmonella

in chicken and one for

Salmonella

in turkey, to inform the Agency's new framework for reducing

Salmonella

attributed to poultry consumed in the United States. FSIS expanded on this work through a Cooperative Agreement (FSIS-02152022) with the University of Maryland's Joint Institute for Food Safety and Applied Nutrition (UMD-JIFSAN), in partnership with EpiX Analytics, to differentiate

Salmonella

serotypes by virulence using advanced bioinformatics (

i.e.,

machine learning) to evaluate genomic data.

The risk assessments address the following risk management questions:

FSIS Constituent Update—July 1, 2022:

FSIS Announces Cooperative Agreement on Salmonella Risk Assessments.

Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-july-1-2022.

Salmonella

Risk Assessments and Risk Management Questions at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/Salmonella-1.

1. What is the public health impact (change in illnesses, hospitalizations, and deaths) achieved by eliminating at receiving a proportion of chicken (or turkey) contaminated with specific levels of

Salmonella

and/or specific

Salmonella

subtypes?

2. What is the public health impact (change in illnesses, hospitalizations, and deaths) achieved by eliminating final product contaminated with specific levels of

Salmonella

and/or specific

Salmonella

subtypes?

3. What is the public health impact of monitoring/enforcing process control from rehang to post-chill? Monitoring could include analytes such as

Enterobacteriaceae Count

(EB), AC, or other indicator organisms, analysis could include presence/absence or levels and the monitoring could also include variability of actual result versus expected result, log reduction, absolute sample result, or other individual establishment specific criteria.

4. What is the public health impact of implementing combinations of the risk management options listed above?

The risk assessments were submitted for independent peer-review

and updated in response to peer review comments. The risk assessments, and the manner in which the results were used to inform specific measures proposed in this document, are discussed below. The final

Quantitative Risk Assessment for Salmonella in Raw Chicken and Raw Chicken Products

and

Quantitative Risk Assessment for Salmonella in Raw Turkey and Raw Turkey Products

(referred to as the 2023 risk assessments in this document) are available at:

https://www.regulations.gov/docket/FSIS-2023-0028.

Peer Review Plan: Quantitative Microbial Risk Assessment of Salmonella in Chicken Products available at:

https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Chicken.pdf.

Peer Review Plan: Quantitative Microbial Risk Assessment of Salmonella in Turkey Products available at:

https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Turkey.pdf.

4. Initial Measures Implemented To Address Salmonella Illnesses Associated With Consumption of Poultry Products

After FSIS announced its new

Salmonella

initiative in October 2021, in addition to initiating the activities to gather data to inform and support a new

Salmonella

Framework discussed above, the Agency implemented some initial measures to support this effort.

Salmonella Key Performance Indicator.

As part of USDA's strategic and performance planning process for fiscal years (FY) 2022-2026, FSIS established a new “key performance indicator” (KPI) targeted to reduce the proportion of poultry samples with

Salmonella

serotypes commonly associated with human illnesses.

This KPI is a measure that is used to evaluate FSIS' progress towards reaching its objectives and goals identified in both Agency and USDA strategic plans and will serve as a metric for success for the USDA FY 2022-2026 Strategic Plan. FSIS analyzed historical Agency sampling data, in addition to FoodNet Fast data from the CDC, to determine the top three

Salmonella

serotypes commonly associated with human illness for this measure. The analysis found that these serotypes are Infantis, Enteritidis, and Typhimurium. FSIS will use annual targets to track progress toward reducing the proportion of poultry samples with the KPI serotypes and is seeking a 2 percent reduction each year, with the goal of achieving a 10 percent reduction by FY 2026. KPI serotypes are useful for strategic and performance planning purposes, and these may differ from the serotypes of public health significance (which will likely change over time as the serotypes commonly associated with human illnesses change).

FY2022-2024 Food Safety Key Performance Indicator. Available at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/Salmonella-0#:~:text=FY2022-2026FoodSafetyKeyPerformanceIndicatorA,theUSDAFiscalYear28FY292022-2026StrategicPlan.

Final Determination.

On August 1, 2022, FSIS announced that it would be declaring

Salmonella

as an adulterant in breaded and stuffed not-ready-to-eat (NRTE) chicken products (also referred to as “NRTE breaded stuffed chicken products”).

These products contain raw, comminuted chicken breast meat, trim, or whole chicken breast meat, but the finished product is heat-treated only to set the batter or breading on the exterior of the product, which may impart an RTE appearance.

Although 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. Based on information from

Salmonella

illness outbreaks associated with NRTE breaded stuffed chicken products and information from research on consumer handling practices with respect to these products, FSIS concluded that labeling that informs consumers that these products are raw and how to prepare them safely fails to sufficiently protect consumers from illness.

Salmonella

as an Adulterant in Breaded Stuffed Raw Chicken Products (Aug 1, 2022). Available at:

https://www.usda.gov/media/press-releases/2022/08/01/usda-announces-action-declare-Salmonella-adulterant-breaded-stuffed.

FSIS Directive 5300.1, Revision 1. Managing the Establishment Profile in the Public Health Information System. (usda.gov). See attachment 2 “NRTE Stuffed Chicken Products that appear RTE.”

On April 28, 2023, FSIS published a proposed determination to declare that NRTE breaded stuffed chicken products that contain

Salmonella

at levels of 1 cfu per gram or higher are adulterated within the meaning of the PPIA (88 FR 26249). FSIS also proposed to carry out verification procedures, including sampling and testing of the chicken component of NRTE breaded stuffed chicken products prior to stuffing and breading, to ensure producing establishments control

Salmonella

in these products. The comment period for the proposed determination was scheduled to close on June 27, 2023, but was extended to August 11, 2023, in response to requests from members of the regulated industry.

FSIS Constituent Update—July 21, 2023:

FSIS Extends Comment Period on Proposed Determination: Salmonella in Not-Ready-To-Eat Breaded Stuffed Chicken Products.

Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-july-21-

2023#:~:text=FSISisextendingthecommentperiodonthe,FSISextendedthedeadlineuntilJuly272023.

FSIS received 3,386 comments on the proposed determination. After careful consideration of the comments, on May 1, 2024, FSIS finalized the determination as proposed, with one change (89 FR 35033). Instead of collecting samples after the establishment has completed all processes needed to prepare the chicken component to be stuffed and breaded to produce a final NRTE breaded stuffed chicken product, as was proposed, FSIS will collect verification samples on the raw incoming chicken components. This change was intended to provide greater flexibility and reduce costs to industry.

As noted above, NRTE breaded stuffed chicken products are adulterated if they contain

Salmonella

at 1 cfu/g or higher, regardless of the

Salmonella

serotype. FSIS adopted this approach for NRTE breaded stuffed chicken products because these products present a unique public health risk. Unlike raw chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey, NRTE breaded stuffed chicken products may have a cooked appearance, are thicker in diameter than many other poultry products, contain multiple ingredients, and are typically cooked from a frozen state. In addition, outbreak data cited in the NRTE breaded stuffed chicken proposal indicate that these products have been consistently and disproportionately associated with

Salmonella

illness outbreaks over the years. As FSIS acknowledged in the NRTE breaded stuffed chicken proposed and final determination, although not all

Salmonella

serotypes are equally likely to cause illness, all serotypes have the ability to invade, replicate, and survive in human host cells, resulting in potentially serious disease. Thus, because of the unique public health risk associated with NRTE breaded stuffed chicken products, FSIS determined that these products are adulterated if they contain any

Salmonella

stereotypes at or above 1 cfu/g.

C. Public Meeting on Salmonella Framework Under Consideration and Public Comments

1. Public Meeting and Proposed Framework

On October 17, 2022, FSIS published a

Federal Register

notice announcing that it was hosting a virtual public meeting on November 3, 2022, to discuss a regulatory framework that the Agency was considering for a new strategy to control

Salmonella

in poultry products and more effectively reduce foodborne

Salmonella

infections linked to these products (

87 FR 62784

). In the notice, FSIS shared the key elements of the framework under consideration and stated that the Agency was soliciting comments from stakeholders on all elements of the draft framework, both at the public meeting and in written comments submitted in response to the

Federal Register

notice, before moving forward with any proposed changes to regulations or other actions. The Agency also made a document outlining the regulatory framework under consideration available to the public before the public meeting by publishing it on the FSIS website.

Proposed Regulatory Framework to

Salmonella

Illnesses Attributable to Poultry. Available at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/proposed.

The three components under consideration in the draft framework included:

1. Requiring that incoming flocks be tested for

Salmonella

before entering an establishment;

2. Enhancing establishment process control monitoring and FSIS verification; and

3. Implementing an enforceable final product standard.

The framework under consideration also addressed cross-cutting issues associated with testing for

Salmonella,

considerations for small and VS establishments, and data sharing. FSIS specifically requested comments on factors the Agency should consider relative to the approaches outlined in each of the components, how each component can be strengthened, and where are there gaps in the framework. FSIS also requested comments on relevant scientific evidence or examples of how the components may be implemented or the impacts they may have on human

Salmonella

illnesses.

At the November 3, 2022, public meeting, stakeholders presented oral comments to FSIS panels comprised of FSIS leadership and experts on the three separate components of the framework and the cross-cutting issues. The primary purpose of the panels was to listen to stakeholder input and ask clarifying questions as needed.

In addition to the oral comments presented at the public meeting, FSIS also provided an opportunity for the public to submit written comments on the framework. The comment period for submitted written comments was scheduled to close on November 16, 2022, but was extended to December 16, 2022, to allow stakeholders sufficient time to take into consideration the discussion at the November 3, 2022, public meeting.

A summary of the general issues raised by the public comments is discussed below.

A transcript of the public meeting and other related materials are available to the public on the FSIS website at:

https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-reducing-Salmonella-poultry.

FSIS Constituent Update—Oct 28, 20222: FSIS Extends Public Meeting and Comment Period on Proposed

Salmonella

Framework. Available at:

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-october-28-2022-1.

2. Public Comments on the Proposed Framework

During the comment period for the proposed framework, FSIS received 1,034 comments. Seven hundred seventy-three comments were identical or similar comment letters from individuals in support of the proposed framework, and 75 were identical or similar comment letters from individuals opposed to the proposed framework. One consumer advocacy organization submitted a comment letter with a spreadsheet containing 4,916 names in support of the framework. Another consumer advocacy organization submitted a comment letter with a spreadsheet containing 3,487 names in support of the framework. FSIS also received 149 unique comments from individuals, most in opposition to the proposed framework. In addition to the individual comments and form letters, FSIS received approximately 35 separate comment letters from trade associations representing the meat and poultry industries, consumer advocacy organizations, animal welfare advocacy organizations, small poultry growers and processors, organizations that support independent family farmers, a large meat producer, a trade association representing the veterinary profession, a State Department of Agriculture, an organic/sustainable agriculture organization, a biotech company representative, a meat scientist, and academics. The general issues raised on each of the components under consideration in the framework and on the cross-cutting issues are described below.

Comments on Component One.

Component One of the draft framework considered whether FSIS should require slaughter establishments to characterize

Salmonella

as a hazard reasonably likely to occur at receiving and require that incoming flocks be tested for

Salmonella

before entering an establishment. Under this approach, the flock would be required to meet a predetermined target for

Salmonella

receiving, which may be industry-wide or establishment-specific. The establishment would be required to demonstrate that its subsequent process will be effective in reducing

Salmonella

so that the product meets the final product standard under consideration in Component Three.

Comments from individuals, consumer advocacy organizations, and animal welfare advocacy organizations expressed general support for the measures under consideration in Component One. A consumer advocacy organization commented that requiring incoming flocks be tested for

Salmonella

would provide incentives for producers to adopt effective pre-harvest measures and for establishments to take action to further reduce food safety risks from flocks failing the incoming

Salmonella

target, such as slaughtering more contaminated flocks at the end of the day.

Comments from small poultry processors and producers, organizations representing small poultry producers and independent family farmers, and trade associations representing the meat and poultry industries expressed concerns that the measures under consideration in Component One would impose an overwhelming burden on small producers. An organization representing small poultry producers and several individual comments stated that requiring that flocks be tested for

Salmonella

before they enter an establishment would add delays and costs that small operators cannot afford.

Several comments, including comments from trade associations representing the meat and poultry industries and organizations that support independent family farmers, asserted that FSIS lacks legal authority to require the measures under consideration in Component One, particularly the requirements that incoming flocks be tested for

Salmonella.

The commenters stated that FSIS' authority under the PPIA begins at the official establishment and does not extend to the farm. The commenters also asserted that Component One conflicts with HACCP principles in that under HACCP, establishments, not FSIS, are responsible for making decisions on how to execute their food safety system.

Comments from trade associations representing the meat and poultry industries asserted that FSIS had presented no data to demonstrate that an incoming

Salmonella

threshold or limit is necessary for an establishment to maintain process control and sufficiently reduce

Salmonella

during processing. They also stated that FSIS did not explain how on-farm sampling several weeks before a flock is processed correlates to actual incoming

Salmonella

loads or provide data to show that reducing incoming loads would have any public health impact. The commenters noted that many producers and processors currently employ interventions aimed at reducing

Salmonella

on farms and suggested that FSIS consider other measures to incentivize pre-harvest controls without requiring testing, such as encouraging establishments to consider

Salmonella

a hazard reasonably likely to occur and providing guidance for addressing

Salmonella

pre-harvest. Some of the commenters that opposed Component One suggested removing this component entirely.

Comments on Component Two.

The measures under consideration in Component Two of the proposed framework would build on HACCP regulations, which provide a prevention-based approach to food safety. To ensure pathogen control throughout slaughter and processing operations, Component Two would modify the existing requirements for microbial organism testing for process control in 9 CFR 381.65(g) and establish additional parameters to better define the required analysis of the data. Establishments would be required to test for indicator organisms (

e.g.,

AC or EB) at rehang and post-chill and would be required to use a standardized statistical approach to process control. FSIS would consider production volume when determining the frequency that establishments must collect samples.

FSIS received several comments in support of the measures under consideration in Component Two from consumer advocacy organizations and academia. These commenters generally agreed with the proposal but recommended that FSIS consider additional measures, such as requiring establishments to test more broadly for indicator organisms and/or requiring testing at more sampling points. These commenters also recommended that FSIS work with stakeholders to develop the SPC approach after conducting research to determine the best points predictive of end product

Salmonella

levels and tailor the SPC for differences in processors' equipment and plant layouts.

Trade associations representing the meat and poultry industries, a State Department of Agriculture, and an organic/sustainable agriculture organization expressed concerns about some of the measures under consideration in Component Two. The commenters asserted that there is a lack of necessary data to support creating a rigid SPC framework for all establishments. An organic/sustainable agriculture organization requested that small producers be exempt from this component. A trade association representing the meat and poultry industry suggested that FSIS consider conducting verification sampling at specific locations and allow establishments to develop their own sampling plans. An association representing small and VS poultry establishments stated that the Component Two measures under consideration will be costly and will not reduce

Salmonella.

Comments on Component Three.

Component Three of the draft framework under consideration would implement an enforceable final product standard to prevent raw poultry products with certain levels and/or types of

Salmonella

contamination from entering the stream of commerce. FSIS would establish the standard by classifying certain

Salmonella

levels and/or serotypes as adulterants in raw poultry and take action against poultry products that exceed the final product standard.

Consumer advocacy organizations, coalitions promoting food safety, and individuals with expertise in food and meat science generally supported Component Three and recommended that FSIS prioritize developing and implementing Component Three. According to these commenters, it is the most critical part of the framework. These commenters recommended an enforceable approach to combatting

Salmonella.

The commenters stated that such an approach would provide much greater safety to consumers by preventing highly contaminated product from reaching store shelves and would motivate industry to adequately control

Salmonella

because of the direct financial cost of losing product that does not meet the final standard.

Some of the comments in support of Component Three requested that FSIS provide increased transparency and data regarding how the product standards under consideration would look. One consumer advocacy organization emphasized that FSIS should use scientifically sound risk assessments in determining final product standards. A consumer advocacy organization recommended establishing separate standards for different poultry products and stated that, for chicken, the standard could be based on FSIS' KPI serotypes Enteritidis, Infantis, and Typhimurium, and that for turkey, the standard could be based on serotypes Reading, Infantis, and Typhimurium. A

consumer advocacy organization stated that FSIS should set stricter standards for certain products if the risk assessment identifies higher risk poultry products and that the risk assessments would determine whether the final product standards should be based on

Salmonella

enumeration, serotypes, or a combination of both.

Comments from trade associations representing the meat and poultry industries, trade associations representing small poultry processors and family farmers, a state government entity, and both large and small businesses associated with poultry production did not support the establishment of enforceable final product standards. These comments opposed considering

Salmonella

to be an adulterant in raw poultry. Many of the commenters stated that FSIS has historically not considered

Salmonella

as an adulterant in raw poultry because: (1)

Salmonella

is not an “added substance” and (2)

Salmonella

is not present in levels that render chicken or turkey injurious to health because customary poultry cooking practices destroy

Salmonella.

The commenters stated that FSIS has not provided any new information to support a change in this interpretation. Comments from these trade associations and a state government entity also stated that FSIS' comparison of

Salmonella

in raw poultry to

Escherichia coli

(E.

oli) in non-intact beef is not relevant, given that the two are very different in how they occur in products and how they are destroyed through cooking.

On the other hand, comments from consumer advocacy organizations stated that

Salmonella

may be considered as an “added substance” because it is not found in the muscle tissue of healthy animals but rather is deposited through cross-contamination during slaughter and processing. The commenters asserted that regardless of whether FSIS considers certain

Salmonella

levels or serotypes most associated with human illness to be an “added substance,” they are adulterants because they “ordinarily render” contaminated poultry products injurious to health.

Commenters that opposed Component Three expressed concern about the delay that would result from a national verification testing program. A trade association representing the chicken industry argued that the extra time required for poultry producers to hold their product pending FSIS'

Salmonella

testing results will significantly decrease the number of poultry products that can safely reach store shelves. An organization representing small poultry producers and processors stated that waiting for acceptable test results would particularly affect small producers who may not have the capability to hold poultry for a long period of time.

Some commenters recommended alternatives to Component Three that the commenters believed would more effectively reduce

Salmonella

infection rates from poultry. For example, a large company that processes poultry recommended that, instead of developing new final product standards based on product adulteration, FSIS update the current performance standards to include a new metric based on a quantification target that measures beyond the prevalence of

Salmonella,

which the commenter said would work well within a current or an updated HACCP system.

Many comments opposed to Component Three asserted that the proposed measures under consideration lacked information on the data and methods that would be used to establish the final product standards. A trade association representing the chicken industry questioned whether FSIS had sufficient laboratory space needed to sample different product lots for

Salmonella

levels or serotypes. An organization representing independent family farmers recommended that, instead of establishing final product standards, FSIS should identify the

Salmonella

strains that cause most illnesses and target those strains specifically rather than providing more general product standards. The 75 similar comment letters that opposed the framework stated that FSIS should remove Component Three from the framework until the Agency provides a clear statement of the levels and/or strains of

Salmonella

that would define the final product standards.

Comments on other issues raised.

In addition to comments about the above Components, there were comments raised about the framework in general. Among these comments were write-in campaigns that expressed general support for the proposed framework. A trade association representing the chicken industry argued that the proposed framework under consideration is not necessary because FSIS' existing framework for addressing

Salmonella

control has been working. A trade association representing the poultry industry commented that there is a need for consumer research and education regarding safe handling of poultry. Some comments expressed concern that adopting the framework would lead to an increase in food waste.

Comments on data sharing.

FSIS received five comments regarding the need to share data. An academic suggested FSIS work with stakeholders to facilitate sharing of industry data that would provide additional insights into the sampling points that would be most predictive of process control. Trade associations representing the poultry industry urged FSIS to create a pathway for companies to share confidential proprietary data with the Agency and indicated it would be necessary to ensure that data is shared only with FSIS. A sustainable agriculture organization emphasized the need for an enhanced ability to share information among agencies, the academic community, and industry.

3. Additional Stakeholder Input

In addition to the November 2022 public meeting, FSIS also participated in technical meetings with representatives from the poultry industry, consumer advocacy organizations, academia, and other stakeholders to further discuss aspects of the proposed

Salmonella

ramework. These technical meetings were organized and hosted by the regulated industry. The first technical meeting was held on March 21, 2023. Among the topics discussed were differences in production practices and

Salmonella

control strategies between chicken and turkeys, review of ongoing risk assessments, pre-harvest control risk management measures, creating, implementing, and reacting to statistical process control measures, and

Salmonella

quantification methods. A second technical meeting was held on April 12, 2023. Among the topics discussed at that meeting were incentivizing use of pre-harvest interventions, how statistical process control is used in the poultry industry and educational needs, and addressing lot size and microbiological independence, and a review of the key differences between beef and poultry. FSIS officials also held a virtual meeting with small and VS establishment owners in February 2023 to seek input on the

Salmonella

Framework under consideration.

Officials' Calendar of Meetings (Feb 2023) at:

https://www.fsis.usda.gov/news-events/events-meetings/officials-calendar-meetings.

4. Overview of Modifications to the Proposed

Salmonella

Framework

FSIS has carefully evaluated the written comments and other stakeholder input provided on the proposed

Salmonella

Framework, along with new studies and information that have become available since the Agency made the information about the framework under consideration

available to the public in November 2022. Based on this evaluation, FSIS has decided to modify some of the measures it had been considering as part of the

Salmonella

Framework and is proposing these modified measures in this document. FSIS requests comments on all measures proposed in this document. If, after the close of the comment period, the Agency determines that some portions of the modified

Salmonella

Framework can be finalized sooner than others, FSIS will finalize those portions separately from the others so as not to delay regulatory action on this important public health initiative.

The proposed modified framework components are discussed in more detail under separate headings in this document. The headings for the proposed modified framework correspond to the component headings used for the draft framework that FSIS presented to the public,

i.e.,

Component One, Component Two, Component Three. The components are discussed in this proposal in an order that emphasizes the most significant proposed changes first. Therefore, the discussion begins with Component Three: Final Product Standards, followed by Component Two: Enhanced Establishment Process Control Monitoring, and finally Component One: Pre-Harvest Measures.

Following is a general summary of the modifications.

Component Three Modifications.

Consistent with Component Three of the draft framework that was under consideration, FSIS is proposing enforceable final product standards to prevent raw poultry products with certain levels and

Salmonella

serotypes from entering commerce. Under this proposal, FSIS has tentatively determined that certain raw poultry products that contain

Salmonella

in an amount that exceeds a specified level and that contain any detectable level of certain

Salmonella

serotypes are adulterated as defined in the PPIA. The proposed final product standards are as follows:

•

Chicken carcasses and chicken parts: Salmonella

at or above 10 cfu per milliliter of rinsate collected in any sample

and

any detectable level of at least one of the

Salmonella

serotypes of public health significance (

i.e.,

Enteritidis, Typhimurium, and I 4,[5],12:i:-);

•

Comminuted chicken: Salmonella

at or above 10 cfu per gram of product collected in any sample

and

any detectable level of at least one of the

Salmonella

serotypes of public health significance (

i.e.,

Enteritidis, Typhimurium, and I 4,[5],12:i:-);

•

Comminuted turkey: Salmonella

at or above 10 cfu per gram of product collected in any sample

and

any detectable level of at least one of the

Salmonella

serotypes of public health significance (

i.e.,

Hadar, Typhimurium, and Muenchen).

FSIS is also proposing that the Agency would routinely collect samples of raw final products subject to the proposed standards and analyze them for

Salmonella

levels and serotypes to determine whether the product is adulterated.

Component Two Modifications.

To ensure that poultry slaughter establishments are effectively controlling

Salmonella

throughout their operations, FSIS is proposing to revise the current regulations in 9 CFR 381.65(g) that require that all poultry slaughter establishments develop, implement, and maintain written procedures to prevent contamination by enteric pathogens throughout the entire slaughter and dressing operation. FSIS is proposing to revise these regulations to clarify that these procedures must include an MMP that incorporates SPC monitoring methods. These proposed amendments would also specify that the pre-chill sampling location is at rehang and specify the use of appropriate microbial organisms for monitoring process control. In addition, VS and VLV establishments operating under Traditional Inspection

would have to test at both rehang and post-chill, instead of at post-chill only, although some of these establishments would have the option to use laboratory services provided by FSIS to analyze their monitoring samples. FSIS has developed proposed guidance to help establishments meet the proposed sampling and analysis requirements. Under this proposal, the guidance would be considered as a “safe harbor” in that establishments that follow the guidance will have met the proposed MMP requirements in 9 CFR 381.65(g). FSIS is also proposing to amend the recordkeeping requirements in 9 CFR 381.65(h) to require that establishments submit their microbial monitoring results to the Agency electronically.

Traditional Inspection is typically employed at smaller lower production volume establishments that eviscerate carcasses by hand (77 FR 4410).

Component One Modifications.

Based on the need for additional research and due to implementation challenges, FSIS has decided, at this time, not to establish a regulatory requirement that establishments characterize

Salmonella

as a hazard reasonably likely to occur at receiving or that incoming flocks be tested for

Salmonella

before entering an establishment. FSIS, however, will focus on achieving the goal of Component One—reduce the amount and type of

Salmonella

contamination that enters the establishment—through non-regulatory strategies. These include actively encouraging the wider use of modified-live vaccines, which have been demonstrated to have a very effective role in mitigating the hazard associated with specific

Salmonella

serotypes, while reducing the entire load of similar serogroup

Salmonella

through cross-protection. FSIS is also working with the Animal and Plant Health Inspection Service (APHIS) to explore ways to expand the National Poultry Improvement Program (NPIP), which has been effective in reducing the prevalence of particular

Salmonella

serotypes.

The Agency will continue to explore and develop strategies for addressing

Salmonella

contamination risk at receiving. FSIS also intends to revise its existing compliance guideline on

Controlling Salmonella in Raw Poultry

to provide effective guidance on pre-harvest interventions and practices for preventing or reducing

Salmonella

colonization of live birds.

FSIS Guideline for Controlling Salmonella in Raw Poultry

(July 2021). Available at:

https://www.fsis.usda.gov/guidelines/2021-0005.

5. Severability

While the three components in this proposal support a comprehensive approach to controlling

Salmonella

in poultry, they are each separate actions that could operate independently of each other to address

Salmonella

illnesses associated with poultry products. Therefore, the following portions of this proposal are mutually severable from each other: The proposed determination that would establish final product standards for certain raw poultry products proposed under Component Three; the proposed amendments to 9 CFR 381.65 (g) and (h) that would enhance process control monitoring in all poultry slaughter establishments under Component Two; and the proposed non-regulatory approach to address pre-harvest measures in Component One. Should FSIS finalize this proposal, if any of the above portions were to be set aside by a reviewing court, FSIS would intend for the remainder of this action to remain in effect.

These proposals are discussed in more detail below.

II. Component Three: Proposed Final Product Standards

A. Current Salmonella Performance Standards and Consideration of an Alternative Approach

As discussed above, although FSIS sampling data show that the occurrence of

Salmonella

in raw poultry products has decreased since FSIS implemented its prevalence-based

Salmonella

performance standards, there has not been a corresponding observed reduction in

Salmonella

illnesses in the United States. There are likely multiple reasons for the disconnect between the reduced

Salmonella

contamination in poultry products and continued illnesses. Individuals who become ill may be exposed to more virulent

Salmonella

strains or higher concentrations of

Salmonella,

and, as noted above, consumption of poultry has increased.

Additionally, as discussed below, several consumer behavior research studies suggest that ordinary consumer cooking and preparation practices for many raw chicken and turkey products do not provide adequate assurance that these products will not be contaminated with

Salmonella

when consumed. Therefore, FSIS has decided to reconsider its current approach to

Salmonella

performance standards for poultry and has tentatively concluded that the Agency should adopt an alternative approach to more effectively reduce

Salmonella

illnesses associated with poultry products. This proposal addresses the disconnect between

Salmonella

contamination on poultry and human illnesses because it targets specific

Salmonella

serotypes more frequently associated with illness and limits the concentration of

Salmonella

permitted in certain raw poultry products.

FSIS Risk Profile for Pathogenic Salmonella in Poultry

(2023); FAO/WHO (Food and Agriculture Organization/World Health Organization)

“Microbiological Risk Assessment Series 3: Hazard Characterization for Pathogens in Food and Water”.

Geneva, Rome: World Health Organization, Food and Agricultural Organization of the United Nations; 2003; Cheng, RA, Eade CR, and Wiedmann M (2019). Embracing Diversity: Differences in Virulence Mechanisms, Disease Severity, and Host Adaptations Contribute to the Success of Nontyphoidal

Salmonella

as a Foodborne Pathogen. Frontiers in Microbiology, Volume 10 at:

https://doi.org/10.3389/fmicb.2019.01368;

Teunis, Peter FM (2022).Dose response for

Salmonella

Typhimurium and Enteritidis and other nontyphoid enteric salmonellae. Epidemics 41: 100653.

https://doi.org/10.1016/j.epidem.2022.100653.

Williams, M.S., & Ebel, E.D. (2022). Temporal changes in the proportion of

Salmonella

outbreaks associated with 12 food commodity groups in the United States.

Epidemiology and infection, 150,

e126.

https://doi.org/10.1017/S0950268822001042.

FSIS' current

Salmonella

performance standards focus on reducing the prevalence of all

Salmonella

without considering differences in virulence among individual

Salmonella

serotypes, strains, and genotypes. Thus, the current standards do not focus on the types of

Salmonella

most likely to cause human illnesses. In addition, the current

Salmonella

performance standards consider only the presence or absence of

Salmonella

in the product, while the quantity of the pathogen may also have an impact on illness. Thus, the current performance standards do not distinguish between poultry products that are heavily contaminated and that contain the most virulent type of

Salmonella

from those that contain trace amounts of a

Salmonella

with types not typically associated with foodborne illnesses in the United States.

Additionally, and independently, the Agency's ability to directly enforce the pathogen reduction performance standards has been limited since 2001, after a ruling by the U.S. Court of Appeals for the Fifth Circuit in

Supreme Beef Processors, Inc.

USDA,

275 F.3d 432 (5th Cir. 2001). In that case, the court enjoined FSIS from suspending inspection services against a meat grinding operation for failure to meet the

Salmonella

performance standards. Since that time, FSIS has used

Salmonella

performance standard failures as a basis to conduct an in-depth evaluation of the establishment's food safety systems, including its HACCP plan and sanitation SOPs. However, because

Salmonella

is not currently considered an adulterant in raw poultry, the Agency cannot withhold the mark of inspection or otherwise prevent products produced in an establishment that has failed the performance standards from entering commerce based solely on the establishment's performance standard results (75 FR 27288, 27293-4). This proposal, on the other hand, would set an enforceable final product standard that prevents raw poultry products with certain levels and types of

Salmonella

contamination, which would be classified as adulterants, from entering the stream of commerce.

When FSIS initially established the pathogen reduction

Salmonella

performance standards in 1996, the Agency noted that, except for

E. coli

O157:H7, FSIS had not taken the position that some amount of a pathogen necessarily renders a raw meat or poultry product unsafe and legally adulterated (

61 FR 38806,

38835). At the time, the Agency believed that it was constrained by the lack of a scientific basis for determining the levels at which specific pathogens do or do not present a safety hazard, and it also relied in part on the fact that proper cooking kills pathogens on raw product (

60 FR 6774,

6799). Therefore, the initial pathogen reduction performance standards were based on a statistical evaluation of the prevalence of bacteria in each establishment's products, measured against the nationwide prevalence of the bacteria in the same products (61 FR 38806, 38836). The

Salmonella

performance standards were and still are not used to determine whether specific product lots are legally adulterated. However, when FSIS established the initial performance standards, the Agency made clear that “as more research is done and more data become available, and as more sophisticated techniques are developed for quantitative risk assessment for microbiological agents, it may be possible and appropriate to develop performance standards that use a different approach” (61 FR 38806, 38836).

Since FSIS implemented the

Salmonella

performance standards, the Agency has evaluated whether certain types of

Salmonella

should be considered as adulterants in raw meat and poultry in response to petitions submitted to the Agency in 2011, 2014, and 2022. For example, in response to two petitions submitted by CSPI in 2011 and 2014, FSIS evaluated whether certain antibiotic-resistant (ABR)

Salmonella

serotypes could be considered as adulterants in raw meat and raw poultry products under the Federal Meat Inspection Act (FMIA) and PPIA. The 2011 petition asked FSIS to declare four strains of ABR

Salmonella

as adulterants when found in ground meats and poultry.

FSIS denied the 2011 petition without prejudice on July 31, 2014. In its response, FSIS explained that the data available at that time “did not support giving the four strains of ABR

Salmonella

identified in the petition a different status as an adulterant in raw ground beef and raw ground poultry than

Salmonella

strains that are susceptible to antibiotics.”

The response stated that additional data on the characteristics of ABR

Salmonella

are needed to determine whether certain strains could qualify as adulterants under the FMIA and PPIA.

The response also noted that because the Agency's denial was without prejudice, the petitioner was not precluded from submitting a revised petition that includes additional information to support the requested action.

CSPI petition #11-06 (May 25, 2011), “Petition for an Interpretive Rule Declaring Specific Strains of Antibiotic Resistant

Salmonella

to be Adulterants Withing the Meaning or 21 U.S.C. 601(m)(1) and (2)(a) and 21 U.S.C. 453(g)(1) and (2)(a).” FSIS final response (July 31, 2014) at:

https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest-0.

FSIS final response to petition #11-06, p. 1.

The CSPI 2014 petition was a refiling of the 2011 petition and asked that FSIS declare certain strains of ABR

Salmonella

as adulterants in all meat and poultry products based on evidence attained since 2011 that, according to the petition, demonstrates both ground and intact poultry products are associated with outbreaks from ABR

Salmonella.

Based on the data available at the time, FSIS denied the 2014 petition without prejudice on February 7, 2018. In its response to the petition, the Agency concluded that, with respect to its status as an adulterant, “

Salmonella

does not appear to present the same issues as [

E. coli

O157:H7], regardless of whether it is resistant or susceptible to antibiotics.”

Therefore, the Agency stated that it “had no basis to conclude that either ABR-

Salmonella

or non-ABR

Salmonella

would render injurious to health what consumers consider to be properly cooked meat or poultry.”

CSPI petition #14-01 (October 1, 2014), “Request for an Interpretive Rule Declaring Certain Antibiotic-Resistant Strains of

Salmonella

to be Adulterants” and FSIS final response (February 7, 2018) at:

https://www.fsis.usda.gov/federal-register/petitions/request-interpretive-rule-declaring-certain-antibiotic-resistant-strains.

FSIS final response to petition #14-06, p. 6.

FSIS final response to petition #14-06, p. 7.

As discussed above, FSIS also considered whether certain

Salmonella

serotypes should be considered as adulterants in all meat and poultry products in response to the January 2020 petition submitted by Marler Clark LLP requesting FSIS to declare 31

Salmonella

serotypes that have been associated with foodborne illness outbreaks to be adulterants of all meat and poultry products.

As noted above, FSIS denied the petition without prejudice. However, in its response, the Agency explained that it believes that an updated

Salmonella

strategy is necessary to reduce

Salmonella

illnesses associated with poultry products and that FSIS had initiated several activities designed to gather data and information to inform and support future actions related to

Salmonella

in poultry. These activities were discussed in the

Background

section of this document.

Marler Clark LLP petition # 20-01 “Petition for an Interpretive Rule Declaring `Outbreak' Serotypes of

Salmonella enteritica

subspecies to be Adulterants” dated January 19, 2020. Available at:

https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella

-serotypes

Since FSIS denied the 2020 Marler petition, many of the activities that were initiated to inform an updated

Salmonella

strategy have generated new studies and information that FSIS has determined support a revised approach on the use of standards to address

Salmonella

in final raw poultry products. For example, after FSIS issued the 2020 Marler petition denial, the Agency completed its chicken carcass exploratory sampling program, NACMCF issued its final 2023 report, FSIS completed the peer-reviewed 2023 risk profile as well as the peer-reviewed 2023 risk assessments for chicken and turkey. The Agency also held the November 3, 2022, public meeting and received written and oral stakeholder input on the proposed

Salmonella

Framework that the Agency was considering.

As part of Component Three of the draft

Salmonella

Framework, FSIS stated that it was assessing whether certain levels and/or types of

Salmonella

on raw poultry present an elevated risk of causing human illness such that they should be considered adulterants. To evaluate the status of

Salmonella

in raw poultry under the PPIA, FSIS has considered stakeholder input received in response to the draft

Salmonella

Framework together with the available scientific information on

Salmonella

in poultry, including recommendations in the 2023 NACMCF report, the findings of the 2023 risk profile

and the results of the 2023 quantitative risk assessments for

Salmonella

in chicken and turkey. Additionally, because FSIS has relied in part on ordinary consumer cooking practices to determine the status of pathogens as adulterants in raw products, the Agency also considered the available consumer behavior research to evaluate whether ordinary consumer cooking and handling practices are able to consistently mitigate the risk associated with certain raw poultry products contaminated with certain levels and/or types of

Salmonella.

Based on its evaluation of scientific evidence, the Agency has tentatively concluded that there are certain raw poultry products and

Salmonella

levels and serotype pairs that have characteristics that distinguish them from other raw products contaminated with

Salmonella.

FSIS has also tentatively determined that, based on its evaluation of available scientific evidence,

Salmonella,

when present in these specific products at the specified levels and serotypes, should be considered as an adulterant.

Accordingly, FSIS is proposing final product standards that would define whether certain raw poultry products contaminated with certain

Salmonella

levels and serotypes are adulterants as defined in the PPIA. Specifically, FSIS had tentatively determined that chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey are adulterated if they contain

Salmonella

at or above 10 cfu/per milliliter or gram (10 cfu/mL(g)) in analytical portion (

i.e.,

mL of rinsate or gram of product) and contain any detectable level of at least one of the

Salmonella

serotypes of public health significance identified for that product. The

Salmonella

serotypes of public health significance identified for chicken carcasses, chicken parts, and comminuted chicken are Enteritidis, Typhimurium, and I 4,[5],12:i:- and for comminuted turkey are Hadar, Typhimurium, and Muenchen. As discussed below, these serotypes were the three most highly virulent serotypes associated with a commodity identified in the 2023 risk assessments. The

Salmonella

serotypes of public health significance will likely change over time as the serotypes commonly associated with human illnesses change. FSIS will continue to track annual targets for reducing the proportion of poultry samples that contain

Salmonella

serotypes of public health significance, as well as data on rates for serotypes commonly associated with human illness to inform future revisions to the

Salmonella

serotypes of public health significance. FSIS would publicly announce and request comments on any changes to the serotypes of public health significance in the

Federal Register

. Additionally, should FSIS finalize the proposed final product standards, the Agency intends to further evaluate and, if necessary, refine these standards as advances in science and technology related to pathogen levels, serotypes, and virulence genes become available. As discussed above, if FSIS finalizes the proposed final product standards, the Agency intends to re-evaluate the serotypes of public health concern every 3-5 years at a minimum and whenever new information on

Salmonella

serotypes associated with human illness become available.

Under this proposed determination, chicken parts subject to the final product standards would include legs, breasts, wings, thighs, quarters, and halves. FSIS is not proposing final product standards for turkey carcasses or parts because historically there have been very few

Salmonella

-positive detections in turkey carcasses. Additionally, the Agency does not

quantify

Salmonella

on turkey carcass sponge samples and has never had a

Salmonella

verification sampling program for turkey parts. Thus, it was not possible for the 2023 turkey risk assessment to assess the risk management questions for turkey parts or provide a robust assessment on final product standards for turkey carcasses that FSIS could use to inform the development of final product standards for these products.

The basis for the proposed final product standards and FSIS' proposed determination that products that contain the

Salmonella

levels and serotypes identified in the proposed final product standards are adulterated is discussed below.

B. Pathogens as Adulterants in Raw and Not-Ready-To Eat Meat and Poultry Products

Under the FMIA (21 U.S.C. 601

et seq.

) and the PPIA (21 U.S.C 451

et seq.

), a meat or poultry product is adulterated if, among other circumstances, “it 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” (21 U.S.C. 601(m)(1); 21 U.S.C. 453(g)(1)). Meat and poultry products are also adulterated if they are “unsound, unhealthful, unwholesome, or otherwise unfit for human food” (21 U.S.C. 601(m)(3)); 21 U.S.C. 453(g)(3)).

Historically, most foodborne pathogens, including

Salmonella,

have not been considered as adulterants of raw and other NRTE meat and poultry products based on the assumption that ordinary cooking is generally sufficient to destroy the pathogens.

One exception to date is

E. coli

O157:H:7 and certain non-O157 Shiga toxin-producing

Escherichia coli

(STEC) in raw, non-intact beef products and intact cuts that are to be further processed into non-intact products before being distributed for consumption. These pathogens are considered adulterants in these specific raw products because they render “injurious to health” what many consumers believe to be properly cooked non-intact beef products.

FSIS had also determined that when contaminated with these pathogens, raw, non-intact beef products are “unhealthful, unwholesome, and otherwise unfit for human food.”

See proposed rule “Pathogen Reduction; Hazard Analysis and Critical Control Point (HACCP) Systems,” February 4, 1993 (60 FR 6774 at 6798-6799) and final rule “Pathogen Reduction; Hazard Analysis and Critical Control Point (HACCP) Systems,” July 25, 1996 (61 FR 38806 at 38835.) See also

Amer. Public Health Ass'n

Butz,

511 F.2d 331 (U.S. App. DC, 1974).

When raw meat or poultry products are associated with an illness outbreak and contain pathogens that are not considered adulterants in those products, FSIS considers the product linked to the illness outbreak to be adulterated under 21 U.S.C. 601(m)(3) or 453(g)(3) because the product is “. . . unsound, unhealthful, unwholesome, or otherwise unfit for human food” (77 FR 72681, 72689 (Dec. 6, 2012). Products that contain an adulterant are considered adulterated under 21 U.S.C. 601(m)(1) or 453(g)(1) even if they are not linked to an illness outbreak.

See

Texas Food Industry Association

Espy,

870 F. Supp. 143 (1994).

Shiga-Toxin Producing Escherichia coli in Certain Raw Beef Products (76 FR 58157, 58159).

When FSIS determined that certain STEC are adulterants in non-intact raw beef products, the Agency identified characteristics associated with both the pathogen and the product that distinguish them from other raw products contaminated with other pathogens. Specially, FSIS considered that these STEC had been associated with illnesses and outbreaks, have a relatively low infectious dose, cause serious human illness, and can survive what many consumers consider to be ordinary preparation and cooking practices of non-intact beef products.

As discussed above, on May 1, 2024, FSIS published a final determination to declare that NRTE breaded stuffed chicken products that contain

Salmonella

at levels of 1 cfu/g or higher are adulterated within the meaning of the PPIA.

In that determination, FSIS stated that while certain STEC have been the only pathogens to date that are considered adulterants in a raw product, certain other pathogens may also exhibit characteristics that would meet the standard to be considered as adulterants in a specific raw product. In the proposed determination, FSIS also stated that if the Agency became aware of evidence to show that a specific pathogen and product pair presents a significant public health risk, it would consider the factors it identified to distinguish certain STEC from other pathogens as adulterants in certain raw beef products to determine the pathogen's status as an adulterant,

i.e.,

pathogen serogroups or types associated with human illnesses; pathogen infectious dose; pathogen and serious human illnesses; and traditional or ordinary cooking practices. After applying these factors to

Salmonella

in NRTE breaded stuffed chicken products, FSIS decided to declare that NRTE breaded stuffed chicken products that contain

Salmonella

at levels of 1 cfu/g or higher are adulterated within the meaning of the PPIA.

Salmonella

in Not-Ready-To-Eat Breaded Stuffed Chicken Products; May 1, 2024 (89 FR 35033) at:

https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS-2022-0013F.pdf.

Specifically, FSIS determined that NRTE breaded stuffed chicken products that contain

Salmonella

at 1 cfu/g or higher are adulterated under 21 U.S.C. 453 (g)(1) because, in these particular products,

Salmonella

is an added substance that may render them injurious to health (89 FR 35034-35035). FSIS also determined that

Salmonella

at 1 cfu/g in NRTE breaded stuffed chicken meets the more stringent “ordinarily injurious to health” standard for substances that are not added as provided in 21 U.S.C. 453(g)(1)) (89 FR 35035). Finally, FSIS determined that NRTE breaded stuffed chicken products contaminated with

Salmonella

at levels of 1 cfu/g or higher present a serious risk of causing

Salmonella

illnesses and that this elevated risk of illness makes them “unhealthful, unwholesome, or otherwise unfit for human food” as defined in 21 U.S.C. 453(g)(3) (89 FR 35037).

C. The Adulteration Standard for Raw Poultry Products

Consistent with its approach used to determine the status of certain STEC in certain raw beef products and to determine the status of

Salmonella

at certain levels in NRTE breaded stuffed chicken products, FSIS has evaluated the available information on

Salmonella

serotypes associated with human illnesses, the

Salmonella

infectious dose, the severity of human illnesses caused by

Salmonella,

and ordinary consumer preparation practices associated with these raw poultry products to assess the status of

Salmonella

in chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey. Based on this evaluation, FSIS is proposing final product standards for levels and serotypes of

Salmonella

in chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey. FSIS has also tentatively determined that chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey that contain the

Salmonella

levels and serotypes identified in the final product standard are adulterated as defined in the PPIA because they contain a poisonous or deleterious substance that renders them “injurious to health” as defined in 21 U.S.C. 453(g)(1). Additionally, FSIS has tentatively determined that chicken carcasses, chicken parts, comminuted chicken, and comminuted turkey that contain the

Salmonella

levels and

serotypes identified in the final product standards are adulterated as defined in 21 U.S.C. 453(g)(3) because their elevated risk of illness makes them “unhealthful, unwholesome, or otherwise unfit for human food.”

The basis for this tentative determination is discussed below.

Under 21 U.S.C. 601(m)(3) of the FMIA and 21 U.S.C. 453(g)(3) of the PPIA, a meat or poultry product is adulterated “if it consists in whole or in part of any filthy, putrid, or decomposed substance or is for any other reason unsound, unhealthful, unwholesome, or otherwise unfit for human food.” Historically, FSIS has interpreted the phrase “is for any other reason unsound, unhealthful, or otherwise unfit for human food” as providing a separate basis for adulteration than consists of “any filthy, putrid, or decomposed substance.” Thus, meat or poultry products that FSIS has determined are “otherwise unfit for human food” within the meaning of 21 U.S.C. 601(m)(3) and 21 U.S.C. 453(g)(3) do not also need to consist “in whole or in part of any filthy, putrid, or decomposed substance.” For example, when raw meat or poultry products are associated with an illness outbreak but contain pathogens that are not considered adulterants in raw products, FSIS has found products linked to the illness outbreak to be adulterated under 21 U.S.C. 601(m)(3) or 21 U.S.C. 453(g)(3) because they are “unsound, unhealthful, unwholesome or otherwise unfit for human food” (77 FR 72689). FSIS has also determined that certain materials from cattle as well as the carcasses of non-ambulatory disabled cattle are adulterated because they present a sufficient risk of exposing humans to the bovine spongiform encephalopathy agent such as to render them “unfit for human food” under 21 U.S.C. 601(m)(3) (69 FR 1862).

1. Pathogen Serogroups or Types Associated With Human Illness

Approximately 2,500

Salmonella

serotypes have been identified,

though not all serotypes have been isolated from poultry. Most human infections have been epidemiologically linked to fewer than 100 serotypes. Almost all strains of

Salmonella

are pathogenic as they can invade, replicate and survive in human host cells, resulting in potentially fatal disease,

though not all are equally likely to cause illness. To evaluate which

Salmonella

serotypes are most likely to be associated with human illness, FSIS considered information from the 2023 NACMCF report, the 2023 risk profile, and the 2023 risk assessments.

Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swaminathan B.

Salmonella

nomenclature. J Clin Microbiol. 2000 Jul;38(7):2465-7. doi: 10.1128/JCM.38.7.2465-2467.2000. PMID: 10878026; PMCID: PMC86943.

Shu-Kee Eng, Priyia Pusparajah, Nurul-Syakima Ab Mutalib, Hooi-Leng Ser, Kok-Gan Chan & Learn-Han Lee (2015)

Salmonella:

A review on pathogenesis, epidemiology and antibiotic resistance, Frontiers in Life Science, 8:3, 284-293, DOI: 10.1080/21553769.2015.1051243.

NACMCF report.

In the 2023 NACMCF report, the committee considered how foodborne illness surveillance data on human

Salmonella

illnesses, data from foodborne outbreaks associated with

Salmonella

in poultry, and data on

Salmonella

serotypes in poultry products can be used to identify the

Salmonella

serotypes of greatest public health concern associated with specific poultry products. The report stated that the relevant serotypes of greatest public health concern are those that are common causes of reported human illness, are present in poultry, and are transmitted through foods. The report noted that CDC surveillance provides data on the frequency of diagnosed illness caused by each serotype and that FSIS data from slaughterhouses and retail surveys can confirm the presence and frequency of serotypes in raw poultry. The report also concluded that outbreak investigations of foodborne salmonellosis can provide direct evidence that foodborne transmission of a particular serotype occurs.

The NACMCF report noted that several approaches have been used to attribute human salmonellosis to specific foods and sources. These include case-control studies, analysis of reported foodborne outbreaks, and most recently, source attribution based on WGS genotyping. The report concluded that attribution based on outbreak data and on genotype both give the greatest weight to data from the most recent years. NACMCF found that poultry is the leading source of human salmonellosis, based on both reported outbreaks and genotype-based attribution methods. The committee also stated that these data show that a small number of serotypes account for most poultry-associated salmonellosis led by Enteritidis, Typhimurium, I:4,5,12:i:-, Infantis, and Heidelberg, and even fewer serogroups: groups O:4 (formerly group B), O:7 (group C1), and O:9 (group D1).

Risk profile.

In the 2023 risk profile, FSIS conducted a review of all information on

Salmonella

outbreaks reported in the CDC National Outbreak Reporting System (NORS), PubMed, and the web pages FSIS uses for maintaining records on outbreak investigations to determine which

Salmonella

serotypes or subtypes are linked to foodborne illnesses or outbreaks from consuming specific raw and NRTE chicken or turkey products. From these data sources, the risk profile identified 210 foodborne

Salmonella

outbreaks linked to poultry products between 1998 and 2020. Of these 210 foodborne

Salmonella

outbreaks, 84.8 percent (178/210) were linked to chicken products and 15.2 percent (32/210) to turkey products. Serotype information was available for 93.3 percent (196/210) of these outbreaks, including 2.4 percent (5/210) associated with multiple serotypes.

For the purposes of the risk profile,

Salmonella

subtypes associated with human illness outbreaks attributed to consuming chicken or turkey are referred to as “subtypes of concern.” The 196 outbreaks in which serotype information was available involved 32 subtypes of concern. Seventeen serotypes of concern were only linked to chicken products. One serotype of concern, Reading, was linked to a turkey product but not to chicken. There were 10 serotypes linked to both chicken and turkey products.

According to the data compiled for the risk profile, the 210 outbreaks include 7,018 illnesses, 1,202 hospitalizations, and 10 deaths attributed to poultry products. When considering outbreaks associated with either chicken or turkey products, nine serotypes accounted for 85 percent (5,794/7,018) of illnesses. Each of these subtypes caused 200 or more outbreak associated illnesses in chicken and/or turkey from 1998-2020. The top seven subtypes associated with chicken were Enteritidis, Heidelberg, Typhimurium, I 4,[5],12:i:-, Montevideo, Thompson, and Infantis. The top four subtypes associated with turkey were Enteritidis, Reading, Muenchen, and Heidelberg. The most common subtypes of concern associated with poultry products overall were Enteritidis, Heidelberg, Typhimurium, and I 4,[5],12:i:-.

Risk assessments.

The chicken and turkey risk assessments leveraged FSIS' 2023 risk profile to identify

Salmonella

serotypes in chicken and turkey linked to foodborne illness and adopted the guidance on risk assessment recommendations from the 2023 NACMCF report. FSIS developed a probabilistic risk assessment model describing current

Salmonella

contamination in raw poultry products and the potential human exposure through consumption of servings derived from these raw products. Data from FSIS microbiological baseline studies, routine PR/HACCP sampling, and exploratory sampling programs were used to describe

Salmonella

in chicken carcasses, fabricated chicken parts, and comminuted chicken and turkey products. FSIS partnered with EpiX Analytics through a Cooperative Agreement with the University of Maryland to incorporate genomics into the risk assessment models developed by FSIS. FSIS selected the grouping of serotypes into two “clusters” (

i.e.,

“higher virulence” and “lower virulence”) based on the virulence profiles, exposure in food, and foodborne epidemiological data and EpiX Analytics then derived two virulence-adjusted

Salmonella

dose-

response models.

FSIS used these dose-response models in its quantitative risk assessment models for

Salmonella

in chicken and turkey. FSIS assessed public health benefits, in terms of annual illnesses prevented, by modeling the impact of removal of lots with

Salmonella

at or above a certain level or with certain serotypes and simulated the probability of illness per serving.

Full details of the EpiX Analytics methodology are provided in Appendix A of the chicken Risk Assessment in the report entitled “

Using genomics to identify nontyphoidal Salmonella serovars of concern and estimating dose-response models amenable to risk assessments in poultry.”

The analysis in the chicken risk assessment found the probability of illness from chicken contaminated with “higher virulence” serotypes exposures is 5.66 times larger than the probability of illness from chicken contaminated with “lower virulence” serotypes. In FSIS sampling, the average annual percentage of “higher virulence” serotypes is approximately 26 percent for chicken carcasses, 32 percent for comminuted chicken product, and 35 percent for chicken parts. The chicken risk assessment identified Enteritidis, Typhimurium, I 4,[5], 12:i:-, Hadar, and Litchfield as the five most frequent “higher virulence” serotypes in chicken. The chicken risk assessment identified Kentucky, Infantis, Schwarzengrund, Heidelberg, and Thompson as the five most frequent “lower virulence” serotypes in chicken.

The analysis in the turkey risk assessment found there are 49 different serotypes in comminuted turkey products, as compared to only 19 serotypes isolated on turkey carcasses in the Agency's pathogen reduction

Salmonella

sampling program. Reading and Hadar ranked as the top two in both carcasses and comminuted, comprising more than 30 percent of the serotype samples for each commodity. Hadar was also observed most often in the FSIS microbiological baseline studies for

Salmonella

in turkey

and appeared in the top ten CDC FoodNet annual summary from 2020.

National Microbiological Baseline Data Collection Program: Young Turkey Survey available at:

https://www.fsis.usda.gov/node/1972

CDC FoodNet Reports available at:

https://www.cdc.gov/foodnet/reports/index.html.

The turkey risk assessment identified Hadar, I 4,[5], 12:i: -, Muenchen Typhimurium, and Saintpaul as the five most frequent “higher virulence” serotypes in turkey. The turkey risk assessment identified Reading, Infantis, Schwarzengrund, Uganda, and Agona as the five most frequent “lower virulence” serotypes in turkey.

The list of serotypes of public health significance is highly important for this framework, as it determines whether products are adulterated as defined in the PPIA. FSIS recognizes that science constantly evolves and therefore our understanding of virulence and other factors will evolve over time.

The FSIS risk assessments utilized bioinformatic tools and methods for clustering

Salmonella

serotypes, and an optimized new dose-response model developed by EpiX Analytics. This model was genomically validated, and results corresponded with other standard bioinformatic techniques differentiating serotypes based on lineage features. Genomic virulence factors were used for the initial grouping of serotypes and the higher virulence serotypes of public health significance were validated by CDC illness outcome data and FSIS sampling data. FSIS did not rely solely on the genomic component of the risk assessment model to determine the list of serotypes of public health significance. FSIS developed a cohesive risk model that incorporates virulence factors, epidemiological outcomes, and frequency of exposure and conducted sensitivity and uncertainty analyses of the full model and the virulence component. FSIS requests comments on the full risk model and the uncertainty and sensitivity analyses, whether they are fit for the purpose of determining the serotypes of public health significance, and what model adjustments or other approaches FSIS should consider in the determination to adapt to evolving data, technology, and analytical methods.

FSIS recognizes that science consistently evolves, and therefore the Agency's understanding of virulence and other factors will evolve over time. Because the scientific understanding of virulence and other relevant factors evolves, FSIS is requesting comments on whether the EpiX Analytics serotype clustering and dose-response adjustment (

i.e.,

risk multiplier) used the best available data and genetic factors relevant to

Salmonella

risk and contamination in the United States poultry population. Additionally, FSIS is requesting comment on potential improvements to the serotype clustering robustness analysis and the risk multiplier sensitivity analysis.

Final product standards serotypes of public health significance.

As noted above, as part of USDA's strategic and performance planning process for FY2022-2026, FSIS established a new KPI targeted to reduce the proportion of FSIS poultry samples with

Salmonella

serotypes commonly associated with human illnesses.

The KPI serotype list was determined using summary statistics, namely comparison of historical Agency sampling data for poultry products and CDC FoodNet data to determine the

Salmonella

serotypes commonly associated with human illness. It is important to note that the KPI is used as an internal performance measure for FSIS, which is not intended to assess industry performance, and, as such, was not externally peer reviewed. FSIS' analysis found that these serotypes are Infantis, Enteritidis, and Typhimurium. Thus, FSIS selected these serotypes as a KPI target for all raw poultry.

FY2022-2024 Food Safety Key Performance Indicator. Available at:

https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/salmonella-0#:~:text=FY%202022-2026%20Food%20Safety%20Key%20Performance%20Indicator%20A,the%20USDA%20Fiscal%20Year%20%28FY%29%202022-2026%20Strategic%20Plan.

When developing the proposed final product standards, FSIS considered incorporating the KPI serotypes as the “serotypes of public health significance” as suggested by some of the comments on the initial draft

Salmonella

Framework. However, after evaluating the information on serotypes discussed above, FSIS concluded that, while the KPI serotypes are useful for strategic and performance planning purposes, the KPI was not a robust scientific tool by which to identify serotypes of public health concern as adulterants. Further, the KPI identified serotypes of public health concern for poultry as a whole, and not by individual product (

chicken

turkey

). The KPI does not reflect the serotypes most commonly associated with illnesses from turkey, and the chicken risk assessment determined that Infantis is not a highly virulent serotype.

Therefore, instead of proposing serotypes of public health significance based solely on the KPI criteria, FSIS has decided that the proposed serotypes of public health significance should be based on a thorough review of multiple FSIS scientific analyses in this area, including the 2023 NACMCF report, the externally peer-reviewed 2023 risk profile, and the two externally peer-reviewed risk assessments. Based on consideration of these scientific efforts, these serotypes are Enteritidis, Typhimurium, and I 4,[5],12:i:- for chicken carcasses, chicken parts, and comminuted chicken, and Hadar, Typhimurium, and Muenchen for comminuted turkey. FSIS has determined that these serotypes more accurately reflect serotypes most likely

to cause illnesses because they are based on the same epidemiological evidence used in the risk profile and the 2023 NACMCF report, but pivotally also include analyses conducted in the risk assessments, which includes an additional analysis of virulence factors, epidemiological outcomes, and frequency of exposure.

The 2023 NACMCF report, the 2023 risk profile, and the Agency's KPI all identify Infantis as among the serotypes commonly associated with poultry-related illnesses, the scientific evidence does not support that the rising trend in Infantis illnesses is associated with chicken consumption. The emergence of Infantis in FSIS chicken sampling in 2016 did not correspond to a proportional increase in human Infantis illnesses, which have been on the rise in the United States since 2010.

Put another way, given the volume of chicken consumed by the American public—much of which is contaminated with Infantis—if it were a high-risk poultry serotype, we would predict more Infantis illnesses. Furthermore, the 2023 chicken risk assessment, which used published genomic methods,

also determined that Infantis is less virulent than many other serotypes with the exception of Kentucky. Additionally, the risk profile found that Infantis accounted for 2 percent of outbreaks identified in the CDC NORS, while I 4,[5],12:i:- accounted for 4.1 percent of those outbreaks.

NACMCF final report “Response to Questions Posed by the Food Safety and Inspection Service: Enhancing Salmonella Control in Poultry Products” (March 2023).

Fenske GJ, Pouzou JG, Pouillot R, Taylor DD, Costard S, Zagmutt FJ. The genomic and epidemiological virulence patterns of Salmonella enterica serovars in the United States. PLoS One. 2023 Dec 5;18(12):e0294624. doi: 10.1371/journal.pone.0294624. PMID: 38051743; PMCID: PMC10697515.

However, FSIS is aware

Salmonella

Infantis remains of considerable concern in terms of potential severity of illness

and antimicrobial resistance, as can be observed in its routine inclusion in national lists of top serotypes by outbreak numbers and sporadic case counts.

CDC estimates that the serotypes of public health significance represent 66 percent of outbreaks and 68 percent of outbreak-associated illnesses in the past five years of outbreak data; including Infantis as a fourth serotype increases these figures to 75 percent and 79 percent, respectively.

Given the notable concern of the

Salmonella

Infantis REPJFX01 strain raised by the CDC and other public health experts, FSIS is requesting comment on the possible inclusion of Infantis as a serotype of public health significance. As discussed above, FSIS was not able to validate that chicken consumption is the major direct driver of the increased Infantis rates and is additionally asking for comment on scientific studies and data sources on this topic that are in line with regulatory evidence guidelines.

FSIS is aware only of results on Infantis severity of illness that reinforce it is not a high risk serotype: Brown AC, Chen JC, Watkins LK, et al. CTX-M-65 Extended-Spectrum β-Lactamase-Producing

Salmonella

enterica Serotype Infantis, United States. Emerging Infectious Diseases. 2018;24(12):2284-2291. doi:10.3201/eid2412.180500.

Centers for Disease Control and Prevention (CDC). BEAM (Bacteria, Enterics, Amoeba, and Mycotics) Dashboard. Atlanta, Georgia: U.S. Department of Health and Human Services.

www.cdc.gov/ncezid/dfwed/BEAM-dashboard.html.

Accessed 06/07/2024.; Centers for Disease Control and Prevention (CDC). National Outbreak Reporting System Dashboard. Atlanta, Georgia: U.S. Department of Health and Human Services, CDC. Last accessed 06/07/2024. Available from URL:

wwwn.cdc.gov/norsdashboard.;

Centers for Disease Control and Prevention (CDC). FoodNet Fast Dashboard. Atlanta, Georgia: U.S. Department of Health and Human Services, CDC. Last accessed 06/07/2024. Available from URL:

https://www.cdc.gov/foodnet/foodnet-fast.html.

These estimates are based a CDC pilot analysis of data (CDC unpublished data) presented in 2023 to the National Advisory Committee on Microbiological Criteria for Foods. See: NACMCF final report “Response to Questions Posed by the Food Safety and Inspection Service: Enhancing

Salmonella

Control in Poultry Products” (March 13, 2023), available at:

https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021.

As research into

Salmonella

virulence factors and their gene functions continues to develop, clustering should be revisited to ensure reliability and consistency. FSIS took care to align the virulence modeling in the risk assessments with epidemiological and clinical patterns in surveillance data: however, current bioinformatics methods are based on the serotypes that have been the consistently highest illness causes (Enteriditis and Typhimurium) across time rather than the full genetic landscape of

Salmonella.

Furthermore, lower virulence serotypes can still outcompete higher virulence serotypes and pose public health risks. As noted above, the list of serotypes of public health significance is essential to this framework, as it determines whether products are adulterated as defined in the PPIA. FSIS requests comments on the initial proposed serotypes of public health significance and what scientific evidence and genetic

Salmonella

data sources beyond the most often studied serotypes should be considered, in addition to that already considered, in the identification of the most highly virulent serotypes identified in the risk assessments, which includes a thorough review of multiple FSIS efforts in this area, including the 2023 NACMCF report and the externally peer reviewed 2023 risk profile.

2. Dose Considerations

As summarized in the 2023 risk profile, although

Salmonella

data are limited, international and domestic outbreak investigations associated with a variety of food products have been used to estimate the relationship between the number of organisms consumed and the probability of illness. These estimates, and more broadly the emergence of dose-response modeling and quantitative risk assessment over the past 25 years, are all based on the concept that a single bacterium is all that is necessary to cause infection and/or illness, that is to say the single-hit model.

FSIS' evaluation and summarization of dose-response models, as well as analysis of outbreak data where estimates for the number of organisms consumed were available, demonstrate that the scientific consensus is that exposure to a small number of

Salmonella

organisms can result in foodborne illness.

Teunis, P.F., & Havelaar, A.H. (2000). The Beta Poisson dose-response model is not a single-hit model. Risk analysis: an official publication of the Society for Risk Analysis, 20(4), 513-520.

https://doi.org/10.1111/0272-4332.204048.

In a study published in 2010 (the Teunis 2010 study), and included in the 2023 risk profile, using a dose-response model approach utilizing outbreak data, and accounting for variation among outbreaks represented by the data, the

Salmonella

median illness dose was 36 cfus (with 95 percent prediction interval of 0.69-1.26×10

cfu).

The median illness dose refers to the dose at which 50 percent of individuals in an exposed population will experience symptomatic illness. The median illness dose and its prediction interval reflect variability among outbreak strains and exposed populations and uncertainty about the dose-response relationship. Thus, it serves as a useful metric for comparing the pathogenicity of different serotypes. Additionally, the World Health Organization Food and Agriculture Organization of the United Nations developed a dose-response approach for risk assessments for

Salmonella.

Also

using outbreaks, the model estimated a 13 percent chance of becoming ill if ingesting an average dose of 100 organisms. Even at the level of 1 organism ingested, there was still a non-zero chance of illness (0.25 percent).

Teunis P.F., et al., Dose-response modeling of

Salmonella

using outbreak data.

Int J Food Microbiol,

2010. 144(2): p. 243-9;

https://doi.org/10.1016/j.ijfoodmicro.2010.09.026.

World Health Organization, Risk assessment of

Salmonella

in eggs and broiler chickens, March 25, 2002. Available at:

https://www.who.int/publications/i/item/9291562293.

A study published after the 2023 FSIS risk profile was peer-reviewed revisited the 2010 Teunis study discussed above.

Using outbreak serotype data, and accounting for variation among outbreaks within a particular serotype, the median

Salmonella

dose predicted to result in 50 percent of exposed individuals becoming ill (IllD

) was 3,360 cfu (95 percent range: 18-3.2×10

), 1,500 cfu (38-8.8×10

), and 1 cfu (0.69-1.0×10

) for Enteritidis, Typhimurium and Infantis, respectively. For the same study, the median

Salmonella

dose predicted to result in 1 percent of exposed individuals becoming ill (IllD

) was 0.6 cfu (95 percent range: 0.24-1.9), 9.9 cfu (0.32-57), and 0.07 cfu (0.01-2.0×10

) for Enteritidis, Typhimurium and Infantis, respectively. These results describe that individuals exposed to small doses of

Salmonella

can experience symptomatic illness. Other

Salmonella

serotypes were also found to cause illness at small doses including Heidelberg (IllD

=323 cfu and IllD

=1 cfu) and Schwarzengrund (IllD

=0.8 cfu and IllD

=0.04 cfu).

Teunis P.F.M. Dose response for Salmonella Typhimurium and Enteritidis and other nontyphoid enteric salmonellae.

Epidemics

41 (2022) 100653;

https://doi.org/10.1016/j.epidem.2022.100653.

Furthermore, the 2023 FSIS risk assessments developed two virulence-adjusted dose-response models (one for low virulence

Salmonella

serotypes, and another for high virulence

Salmonella

serotypes), which utilize the work described in the 2023 FSIS risk profile to poultry specific serotypes. The high virulence dose-response model (which includes the serotypes of public health significance) was estimated using outbreak data and employed a beta-Poisson model of infection for a given dose as outlined in the 2023 risk profile. Risk multipliers, derived from epidemiological outbreak data attributed to poultry sources, with consideration of prevalence in animal sources from FSIS poultry sampling programs, were then used to scale the relative risk of illness from exposures to each cluster. The probability of illness from consuming chicken containing high virulence

Salmonella

serotypes exposures is 5.66 times greater than the probability of illness from exposure to chicken products containing low virulence

Salmonella

serotypes. The dose-response findings of the 2023 risk assessment rely on the single-hit model, and the virulence adjusted dose-response models estimate of a 1 in 100 probability of illness at 1 cfu of high virulence

Salmonella

per serving and a 0.2 in 100 probability of illnesses at 1 cfu of low virulence

Salmonella

per serving. While the median illness is not attained by the low virulence

Salmonella

dose response model, the median illness dose described by the dose-response model for serotypes of public health significance is approximately 2000 cfu.

As summarized in the 2023 risk profile, five

Salmonella

foodborne outbreaks have shown that

Salmonella

can cause illness from exposure of 10 or fewer organisms per person.

Additionally, several outbreaks from a range of

Salmonella

serotypes in various food products have shown that exposure from 11 to 420 organisms per person can result in illness.

Thus, in these published studies, illnesses resulted from doses ranging from 1 to 420

Salmonella

organisms per person.

Killalea, D., et al., International Epidemiological and Microbiological Study of Outbreak of

Salmonella

Agona Infection from a Ready to Eat Savoury Snack—I: England and Wales and the United States. 1996, British Medical Journal Publishing Group.; Shohat, T., et al., International Epidemiological and Microbiological Study of Outbreak of

Salmonella

Agona Infection from a Ready to Eat Savoury Snack—Ii: Israel. BMJ, 1996. 313(7065): p. 1107-1109.; D'aoust, J.Y. and J.Y.D. Aoust, Infective Dose of

Salmonella

Typhimurium in Cheddar Cheese. American Journal of Epidemiology, 1985. 122(4): p. 717-720.; D'aoust, J.Y., D.W. Warburton, and A.M. Sewell,

Salmonella

Typhimurium Phage-Type 10 from Cheddar Cheese Implicated in a Major Canadian Foodborne Outbreak. Journal of Food Protection, 1985. 48(12): p. 1062-1066.; Kapperud, G., et al., Outbreak of

Salmonella

Typhimurium Infection Traced to Contaminated Chocolate and

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