Proposed Rule2024-16963
Salmonella Framework for Raw Poultry Products
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Published
August 7, 2024
Issuing agencies
Agriculture DepartmentFood Safety and Inspection Service
Abstract
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.
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[Federal Register Volume 89, Number 152 (Wednesday, August 7, 2024)]
[Proposed Rules]
[Pages 64678-64748]
From the Federal Register Online via the Government Publishing Office [<a href="http://www.gpo.gov">www.gpo.gov</a>]
[FR Doc No: 2024-16963]
[[Page 64677]]
Vol. 89
Wednesday,
No. 152
August 7, 2024
Part IV
Department of Agriculture
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Food Safety and Inspection Service
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9 CFR Part 381
Salmonella Framework for Raw Poultry Products; Proposed Rule
Federal Register / Vol. 89, No. 152 / Wednesday, August 7, 2024 /
Proposed Rules
[[Page 64678]]
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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.
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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:
<bullet> 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: <a href="https://www.regulations.gov">https://www.regulations.gov</a>. Follow the on-line instructions at that site for
submitting comments.
<bullet> 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.
<bullet> 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 <a href="https://www.regulations.gov">https://www.regulations.gov</a>.
Docket: Go to the Federal eRulemaking Portal at <a href="https://www.regulations.gov">https://www.regulations.gov</a> 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 \1\ 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.
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\1\ 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.
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Poultry is among the leading sources of Salmonella foodborne
illness acquired domestically in the United States.\2\ 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
[[Page 64679]]
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.
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\2\ 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: <a href="https://www.cdc.gov/ifsac/php/annual-reports/?CDC_AAref_Val=https://www.cdc.gov/foodsafety/ifsac/annual-reports.html">https://www.cdc.gov/ifsac/php/annual-reports/?CDC_AAref_Val=https://www.cdc.gov/foodsafety/ifsac/annual-reports.html</a>.
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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
[[Page 64680]]
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.\3\ 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.
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\3\ 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.
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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
[[Page 64681]]
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
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Total (million $)
Description -----------------------------------------------
Low Medium High
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Costs:
Costs associated with the proposed rule:
Statistical Process Control................................. 0.04 0.04 0.04
Electronic data submission.................................. 0.18 0.18 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
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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
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Total benefits.......................................... 4.45 20.49 39.00
Net benefits........................................ 1.14 4.06 6.75
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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.\4\ 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
[[Page 64682]]
calculated as the product of the total number of CDC FoodNet cases per
year (7,600),\5\ the share of these cases that are foodborne (66
percent) \6\ and of domestic origin (89 percent),\7\ and the under-
diagnosis multiplier for Salmonella (24.3),\8\ then dividing by the
FoodNet catchment area (15 percent).\9\ 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).\10\ 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.\11\ Nevertheless,
FSIS believes these are the best available estimates.
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\4\ 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.
<a href="https://doi.org/10.3201%2Feid2701.190676">https://doi.org/10.3201%2Feid2701.190676</a>.
\5\ 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: <a href="https://doi.org/10.15585/mmwr.mm7140a2">https://doi.org/10.15585/mmwr.mm7140a2</a>. Note: the most recent
annual FoodNet report was used for the total estimated FoodNet cases
annually.
\6\ 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.
<a href="https://doi.org/10.3201/eid2701.200316">https://doi.org/10.3201/eid2701.200316</a>. Note: This article
represented a recent appraisal of the foodborne share of all
Salmonella illnesses.
\7\ 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.
\8\ 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. <a href="https://doi.org/10.4315/0362-028X.JFP-11-345">https://doi.org/10.4315/0362-028X.JFP-11-345</a>. Note: This article estimated parametric distributions for
uncertainty about the under-diagnosis multiplier based on the
Scallan et al. (2011) model assumptions.
\9\ Scallan et al. (2011).
\10\ 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.
\11\ 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.
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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.\12\
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\12\ Scharff R.L. Food Attribution and Economic Cost Estimates
for Meat and Poultry-Related Illnesses. Journal of Food Protection.
2020; 83(6): 959-967.
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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.\13\ 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.\14\
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\13\ 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. v. 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.
\14\ 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).
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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.<SUP>15 16</SUP> In addition, FSIS
schedules follow-up verification sampling, a Public Health Risk
Evaluation (PHRE),\17\
[[Page 64683]]
and possibly a Food Safety Assessment (FSA) \18\ 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.
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\15\ Salmonella Categorization of Individual Establishments for
Poultry Products at: <a href="https://www.fsis.usda.gov/science-data/data-sets-visualizations/microbiology/salmonella-verification-testing-program-monthly">https://www.fsis.usda.gov/science-data/data-sets-visualizations/microbiology/salmonella-verification-testing-program-monthly</a>.
\16\ The category definitions under verification sampling are as
follows:
<bullet> 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;
<bullet> 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
<bullet> Category 3: Establishments that have exceeded the
maximum allowable percent positive during the most recently
completed 52-week moving window.
\17\ 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
(<a href="http://usda.gov">usda.gov</a>).
\18\ 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 (<a href="http://usda.gov">usda.gov</a>).
Table 2--Salmonella Performance Standards for Poultry Products
----------------------------------------------------------------------------------------------------------------
Minimum number of
Performance Maximum samples to
Product standard * acceptable assess process
percent positive control
----------------------------------------------------------------------------------------------------------------
Broiler Carcasses...................................... 5 of 51 9.8 11
Turkey Carcasses....................................... 4 of 56 7.1 14
Comminuted Chicken..................................... 13 of 52 25.0 10
Comminuted Turkey...................................... 7 of 52 13.5 10
Chicken Parts.......................................... 8 of 52 15.4 10
----------------------------------------------------------------------------------------------------------------
* 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 \19\ 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.<SUP>20 21 22</SUP>
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 \23\. However, the CDC estimated that
in 2019, Americans experienced 17.1 per 100,000 population Salmonella
illnesses.\24\ 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.
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\19\ 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.
\20\ 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. <a href="https://doi.org/10.1016/j.mran.2017.10.001">https://doi.org/10.1016/j.mran.2017.10.001</a>.
\21\ Ebel, ED and Williams MS (2020). Assessing the
effectiveness of revised performance standards for Salmonella
contamination of comminuted poultry. Microbial Risk Analysis
14:100076. <a href="https://doi.org/10.1016/j.mran.2019.05.002">https://doi.org/10.1016/j.mran.2019.05.002</a>.
\22\ 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. <a href="https://doi.org/10.1016/j.ijfoodmicro.2022.109801">https://doi.org/10.1016/j.ijfoodmicro.2022.109801</a>.
\23\ HHS Office of Disease Prevention and Health Promotion
archive. Healthy People 2020 at: <a href="https://wayback.archive-it.org/5774/20220414163116/https://www.healthypeople.gov/2020/topics-objectives/topic/food-safety/objectives">https://wayback.archive-it.org/5774/20220414163116/https://www.healthypeople.gov/2020/topics-objectives/topic/food-safety/objectives</a>.
\24\ 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:
<a href="https://www.cdc.gov/mmwr/volumes/69/wr/mm6917a1.htm#T1_down">https://www.cdc.gov/mmwr/volumes/69/wr/mm6917a1.htm#T1_down</a>.
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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.\25\ 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.
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\25\ 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. <a href="https://doi.org/10.1017/S0950268822001042">https://doi.org/10.1017/S0950268822001042</a>.
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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.\26\ 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.
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\26\ Powell M.R. (2023). Trends in reported illnesses due to
poultry-and nonpoultry associated Salmonella serotypes; United
States 1996-2019. Risk Analysis. <a href="https://doi.org/10.1111/risa.14181">https://doi.org/10.1111/risa.14181</a>.
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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.\27\
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.
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\27\ HHS Office of Disease Prevention and Health Promotion
archive. Healthy People 2030 at: <a href="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">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</a>.
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[[Page 64684]]
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.\28\ 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.
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\28\ 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: <a href="https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella">https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella</a>-serotypes.
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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.\29\
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\29\ FSIS Final Response to Petition #20-01, May 31, 2022.
Available at: <a href="https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella">https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella</a>-serotypes.
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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 \30\ in poultry.\31\
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).
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\30\ 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.
\31\ 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:
<a href="https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest">https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest</a>.
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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.\32\
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\32\ Food Safety Coalition Letter, September 2, 2021. Available
at: <a href="https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry">https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry</a>.
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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.\33\ In the
[[Page 64685]]
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.
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\33\ USDA Press Release, ``USDA Launches New Effort to Reduce
Salmonella Illnesses Linked to Poultry'' (October 19, 2021) at:
<a href="https://www.usda.gov/media/press-releases/2021/10/19/usda-launches-new-effort-reduce-salmonella-illnesses-linked-poultry">https://www.usda.gov/media/press-releases/2021/10/19/usda-launches-new-effort-reduce-salmonella-illnesses-linked-poultry</a>.
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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.\34\ 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.
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\34\ Coalition for Poultry Safety Reform Letter, February 2,
2022. Available at: <a href="https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry">https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry</a>.
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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.\35\ 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?
\36\ 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.\37\ 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.\38\ 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.\39\ 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.\40\ 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:
<a href="https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021">https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021</a>.
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\35\ National Advisory Committee Meeting on Microbiological
Criteria for Foods (NACMF) Public Meeting --November 2021. Available
at: <a href="https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-2">https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-2</a>.
\36\ 2021-2023 National Advisory Committee Meeting on
Microbiological Criteria for Foods (NACMF); FSIS Charge: Enhancing
Salmonella Control in Poultry Products Available at: <a href="https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021">https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021</a>.
\37\ NACMCF FSIS Charge: Enhancing Salmonella Control in
Poultry, April 25, 2022. Available at: <a href="https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-fsis">https://www.fsis.usda.gov/news-events/events-meetings/national-advisory-committee-microbiological-criteria-foods-nacmcf-fsis</a>.
\38\ Public Meeting; National Advisory Committee on
Microbiological Criteria for Food, Nov 15, 2022. Available at:
<a href="https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-national-advisory-committee-microbiological-criteria">https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-national-advisory-committee-microbiological-criteria</a>.
\39\ Public Meeting National Advisory Committee on
Microbiological Criteria for Food (87 FR 64001). Available at:
<a href="https://www.fsis.usda.gov/policy/federal-register-rulemaking/federal-register-notices/public-meeting-national-advisory">https://www.fsis.usda.gov/policy/federal-register-rulemaking/federal-register-notices/public-meeting-national-advisory</a>.
\40\ FSIS Constituent Update--Nov 10, 2022: Deadline Extended to
Comment on NACMCF Document. Available at: <a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-november-10-2022">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-november-10-2022</a>.
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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.\41\ 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.
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\41\ FSIS Constituent Update--Dec 3, 2021: FSIS Seeking
Proposals for Pilot Projects to Control Salmonella in Poultry
Slaughter and Processing Establishments. Available at: <a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-december-3-2021">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-december-3-2021</a>.
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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.\42\ This action is intended to remove barriers to the use of
vaccination as an important pre-harvest intervention to
[[Page 64686]]
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: <a href="https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot">https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot</a>.
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\42\ FSIS Constituent Update--March 1, 2024: FSIS Intends to
Exclude Vaccine Strains from the FSIS Salmonella Performance
Categorization at: <a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-march-1-2024">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-march-1-2024</a>.
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On September 23, 2023, FSIS granted a pilot to 2 establishments to
examine the merits of using preharvest results to optimize
establishment interventions.\43\ 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.
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\43\ Pilot Projects: Salmonella control strategies. Current
Salmonella Pilot Participants available at: <a href="https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot">https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/pilot</a>.
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Research and Science Roundtable. On February 15, 2022, FSIS held a
research and science roundtable on Salmonella in poultry.\44\ 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: <a href="https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable">https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable</a>.
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\44\ Salmonella in Poultry: Research and Science Roundtable.
Available at: <a href="https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable">https://www.fsis.usda.gov/news-events/events-meetings/Salmonella-poultry-research-and-science-roundtable</a>.
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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.\45\ 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: <a href="https://www.regulations.gov/docket/FSIS-2023-0028">https://www.regulations.gov/docket/FSIS-2023-0028</a>.
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\45\ FSIS Constituent Update--April 22, 2022: FSIS Expands
Salmonella Sampling for Young Chicken Carcasses. Available at:
<a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-april-22-2022">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-april-22-2022</a>.
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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.\46\ 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.
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\46\ FSIS Constituent Update--Aug 5, 2022: FSIS to include
Salmonella Quantification in all Poultry Rinse Samples. Available
at: <a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-august-5-2022-0">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-august-5-2022-0</a>. FSIS Notice 44-22, Revised Young
Chicken Exploratory Sampling Program, Aug 11, 2022.
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On January 30, 2023, FSIS added Salmonella quantification testing
and AC indicator analyses to chicken part rinsates.\47\ 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: <a href="https://www.fsis.usda.gov/science-data/data-sets-visualizations/laboratory-sampling-data">https://www.fsis.usda.gov/science-data/data-sets-visualizations/laboratory-sampling-data</a>.
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\47\ FSIS Constituent Update--Feb 3, 2023: FSIS to Expand
Salmonella Enumeration and Aerobic Count Indicator Testing to Other
Poultry Products. Available at: <a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-february-3-2023">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-february-3-2023</a>.
Notice 83-23, New Sampling Instructions and Testing for Chicken
Parts and NRTE Comminuted Poultry, Feb 3, 2023. Available at:
<a href="https://www.fsis.usda.gov/policy/fsis-notice/08-23">https://www.fsis.usda.gov/policy/fsis-notice/08-23</a>.
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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 \48\ 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
[[Page 64687]]
this document) is available at: <a href="https://www.regulations.gov/docket/FSIS-2023-0028">https://www.regulations.gov/docket/FSIS-2023-0028</a>.
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\48\ Peer Review Plan: Risk Profile for Salmonella Subtypes in
Poultry Products Linked to Foodborne Illness (<a href="http://usda.gov">usda.gov</a>).
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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.\49\ The risk assessments address the following
risk management questions:
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\49\ FSIS Constituent Update--July 1, 2022: FSIS Announces
Cooperative Agreement on Salmonella Risk Assessments. Available at:
<a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-july-1-2022">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-july-1-2022</a>. Salmonella Risk Assessments and Risk
Management Questions at: <a href="https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/Salmonella-1">https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/Salmonella-1</a>.
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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
\50\ 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: <a href="https://www.regulations.gov/docket/FSIS-2023-0028">https://www.regulations.gov/docket/FSIS-2023-0028</a>.
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\50\ Peer Review Plan: Quantitative Microbial Risk Assessment of
Salmonella in Chicken Products available at: <a href="https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Chicken.pdf">https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Chicken.pdf</a>.Peer Review Plan:
Quantitative Microbial Risk Assessment of Salmonella in Turkey
Products available at: <a href="https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Turkey.pdf">https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS_Salmonella_Peer_Review_Plan_Turkey.pdf</a>.
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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.\51\ 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).
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\51\ 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.
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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'').\52\ 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.\53\
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.
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\52\ Salmonella as an Adulterant in Breaded Stuffed Raw Chicken
Products (Aug 1, 2022). Available at: <a href="https://www.usda.gov/media/press-releases/2022/08/01/usda-announces-action-declare-Salmonella-adulterant-breaded-stuffed">https://www.usda.gov/media/press-releases/2022/08/01/usda-announces-action-declare-Salmonella-adulterant-breaded-stuffed</a>.
\53\ FSIS Directive 5300.1, Revision 1. Managing the
Establishment Profile in the Public Health Information System.
(<a href="http://usda.gov">usda.gov</a>). See attachment 2 ``NRTE Stuffed Chicken Products that
appear RTE.''
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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.\54\
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\54\ 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,FSISextendedthedead
lineuntilJuly272023.
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[[Page 64688]]
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.\55\
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\55\ Proposed Regulatory Framework to Salmonella Illnesses
Attributable to Poultry. Available at: <a href="https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/proposed">https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-Salmonella-poultry/proposed</a>.
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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.\56\ 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.\57\ A summary of
the general issues raised by the public comments is discussed below.
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\56\ A transcript of the public meeting and other related
materials are available to the public on the FSIS website at:
<a href="https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-reducing-Salmonella-poultry">https://www.fsis.usda.gov/news-events/events-meetings/public-meeting-reducing-Salmonella-poultry</a>.
\57\ FSIS Constituent Update--Oct 28, 20222: FSIS Extends Public
Meeting and Comment Period on Proposed Salmonella Framework.
Available at: <a href="https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-october-28-2022-1">https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-october-28-2022-1</a>.
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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 at
[[Page 64689]]
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
[[Page 64690]]
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. coli) 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.\58\
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\58\ Officials' Calendar of Meetings (Feb 2023) at: <a href="https://www.fsis.usda.gov/news-events/events-meetings/officials-calendar-meetings">https://www.fsis.usda.gov/news-events/events-meetings/officials-calendar-meetings</a>.
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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
[[Page 64691]]
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:
<bullet> 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:-
);
<bullet> 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:-);
<bullet> 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 \59\ 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.
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\59\ Traditional Inspection is typically employed at smaller
lower production volume establishments that eviscerate carcasses by
hand (77 FR 4410).
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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 \60\ to provide effective guidance on pre-
harvest interventions and practices for preventing or reducing
Salmonella colonization of live birds.
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\60\ FSIS Guideline for Controlling Salmonella in Raw Poultry
(July 2021). Available at: <a href="https://www.fsis.usda.gov/guidelines/2021-0005">https://www.fsis.usda.gov/guidelines/2021-0005</a>.
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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.
[[Page 64692]]
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,\61\ and, as noted above, consumption of poultry has
increased.\62\ 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.
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\61\ 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: <a href="https://doi.org/10.3389/fmicb.2019.01368">https://doi.org/10.3389/fmicb.2019.01368</a>; Teunis, Peter FM (2022).Dose response for
Salmonella Typhimurium and Enteritidis and other nontyphoid enteric
salmonellae. Epidemics 41: 100653. <a href="https://doi.org/10.1016/j.epidem.2022.100653">https://doi.org/10.1016/j.epidem.2022.100653</a>.
\62\ 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. <a href="https://doi.org/10.1017/S0950268822001042">https://doi.org/10.1017/S0950268822001042</a>.
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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. v. 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.\63\ 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.''
\64\ 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.
[[Page 64693]]
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.
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\63\ 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: <a href="https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest">https://www.fsis.usda.gov/policy/petitions/petition-submitted-center-science-public-interest</a>-0.
\64\ FSIS final response to petition #11-06, p. 1.
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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.\65\ 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.'' \66\ 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.'' \67\
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\65\ 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: <a href="https://www.fsis.usda.gov/federal-register/petitions/request-interpretive-rule-declaring-certain-antibiotic-resistant-strains">https://www.fsis.usda.gov/federal-register/petitions/request-interpretive-rule-declaring-certain-antibiotic-resistant-strains</a>.
\66\ FSIS final response to petition #14-06, p. 6.
\67\ FSIS final response to petition #14-06, p. 7.
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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.\68\ 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.
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\68\ 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: <a href="https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella">https://www.fsis.usda.gov/policy/petitions/petition-interpretive-rule-related-certain-Salmonella</a>-serotypes.
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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
[[Page 64694]]
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.\69\ \70\ 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.\71\ FSIS had also determined that when
contaminated with these pathogens, raw, non-intact beef products are
``unhealthful, unwholesome, and otherwise unfit for human food.'' \72\
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\69\ 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 v. Butz,
511 F.2d 331 (U.S. App. DC, 1974).
\70\ 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.
\71\ See Texas Food Industry Association v. Espy, 870 F. Supp.
143 (1994).
\72\ Shiga-Toxin Producing Escherichia coli in Certain Raw Beef
Products (76 FR 58157, 58159).
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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.\73\ 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.
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\73\ Salmonella in Not-Ready-To-Eat Breaded Stuffed Chicken
Products; May 1, 2024 (89 FR 35033) at: <a href="https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS-2022-0013F.pdf">https://www.fsis.usda.gov/sites/default/files/media_file/documents/FSIS-2022-0013F.pdf</a>.
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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
[[Page 64695]]
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.'' \74\ The basis for this tentative determination is discussed
below.
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\74\ 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).
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1. Pathogen Serogroups or Types Associated With Human Illness
Approximately 2,500 Salmonella serotypes have been identified,\75\
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,\76\ 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.
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\75\ 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.
\76\ 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.
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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-
[[Page 64696]]
response models.\77\ 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.
---------------------------------------------------------------------------
\77\ 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.''
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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 \78\ and appeared in the top ten CDC FoodNet
annual summary from 2020.\79\
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\78\ National Microbiological Baseline Data Collection Program:
Young Turkey Survey available at: <a href="https://www.fsis.usda.gov/node/1972">https://www.fsis.usda.gov/node/1972</a>
\79\ CDC FoodNet Reports available at: <a href="https://www.cdc.gov/foodnet/reports/index.html">https://www.cdc.gov/foodnet/reports/index.html</a>.
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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.\80\ 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.
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\80\ 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%2
0Fiscal%20Year%20%28FY%29%202022-2026%20Strategic%20Plan.
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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 v. 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
[[Page 64697]]
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.\81\ 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,\82\ 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.
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\81\ NACMCF final report ``Response to Questions Posed by the
Food Safety and Inspection Service: Enhancing Salmonella Control in
Poultry Products'' (March 2023).
\82\ 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.
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However, FSIS is aware Salmonella Infantis remains of considerable
concern in terms of potential severity of illness \83\ and
antimicrobial resistance, as can be observed in its routine inclusion
in national lists of top serotypes by outbreak numbers and sporadic
case counts.\84\ 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.\85\ 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.
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\83\ 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 [beta]-
Lactamase-Producing Salmonella enterica Serotype Infantis, United
States. Emerging Infectious Diseases. 2018;24(12):2284-2291.
doi:10.3201/eid2412.180500.
\84\ Centers for Disease Control and Prevention (CDC). BEAM
(Bacteria, Enterics, Amoeba, and Mycotics) Dashboard. Atlanta,
Georgia: U.S. Department of Health and Human Services. <a href="http://www.cdc.gov/ncezid/dfwed/BEAM-dashboard.html">www.cdc.gov/ncezid/dfwed/BEAM-dashboard.html</a>. 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:
<a href="http://wwwn.cdc.gov/norsdashboard">wwwn.cdc.gov/norsdashboard</a>.; 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: <a href="https://www.cdc.gov/foodnet/foodnet-fast.html">https://www.cdc.gov/foodnet/foodnet-fast.html</a>.
\85\ 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: <a href="https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021">https://www.fsis.usda.gov/policy/advisory-committees/national-advisory-committee-microbiological-criteria-foods-nacmcf/2021</a>.
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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.\86\ 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.
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\86\ 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. <a href="https://doi.org/10.1111/0272-4332.204048">https://doi.org/10.1111/0272-4332.204048</a>.
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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 0.69-1.26x10\7\ cfu).\87\ 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.\88\ Also
[[Page 64698]]
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).
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\87\ Teunis P.F., et al., Dose-response modeling of Salmonella
using outbreak data. Int J Food Microbiol, 2010. 144(2): p. 243-9;
<a href="https://doi.org/10.1016/j.ijfoodmicro.2010.09.026">https://doi.org/10.1016/j.ijfoodmicro.2010.09.026</a>.
\88\ World Health Organization, Risk assessment of Salmonella in
eggs and broiler chickens, March 25, 2002. Available at: <a href="https://www.who.int/publications/i/item/9291562293">https://www.who.int/publications/i/item/9291562293</a>.
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A study published after the 2023 FSIS risk profile was peer-
reviewed revisited the 2010 Teunis study discussed above.\89\ 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<INF>50</INF>) was 3,360 cfu (95 percent range: 18-3.2x10\9\),
1,500 cfu (38-8.8x10\7\), and 1 cfu (0.69-1.0x10\6\) 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<INF>01</INF>) was 0.6 cfu (95 percent range: 0.24-
1.9), 9.9 cfu (0.32-57), and 0.07 cfu (0.01-2.0x10\4\) 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<INF>50</INF>=323 cfu and IllD<INF>01</INF>=1 cfu) and
Schwarzengrund (IllD<INF>50</INF>=0.8 cfu and IllD<INF>01</INF>=0.04
cfu).
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\89\ Teunis P.F.M. Dose response for Salmonella Typhimurium and
Enteritidis and other nontyphoid enteric salmonellae. Epidemics 41
(2022) 100653; <a href="https://doi.org/10.1016/j.epidem.2022.100653">https://doi.org/10.1016/j.epidem.2022.100653</a>.
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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.\90\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.\91\ Thus, in these published studies, illnesses resulted from
doses ranging from 1 to 420 Salmonella organisms per person.
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\90\ 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 Caused by
a Strain Lacking the 60-Megadalton Virulence Plasmid. J Clin
Microbiol, 1990. 28(12): p. 2597-601.; Hockin, J.C. et al., An
International Outbreak of Salmonella Nima from Imported Chocolate. J
Food Prot. 1989. 52(1): p. 51-54.; Lehmacher, A., Bockemuhl, J., and
Aleksic. S. Nationwide outbreak of human salmonellosis in Germany
due to contaminated paprika and paprika-powdered potato chips. 1995.
Epidemiol Infect. 115: p. 501-11.
\91\ Kasuga F.et al., Archiving of food samples from restaurants
and caterers--Quantitative profiling of outbreaks of foodborne
Salmonella in Japan. Journal of Food Protection, 2004. 67: p. 2024-
2032; Blaser, M.J., and Newman, L.S. A review of human
salmonellosis: I. Infective dose. Rev Infect Dis., 1982.4: p.1096-
106; Abe, K., N. et al., Prolonged incubation period of
Salmonellosis associated with low bacterial doses. Journal of food
protection, 2004. 67: p. 2735-2740; Hara-Kudo, Y. and K. Takatori,
Contamination level and ingestion dose of foodborne pathogens
associated with infections. Epidemiology and Infection, 2011. 139:
p. 1505-1510; Hennessy T.W., et al., A national outbreak of
Salmonella enteritidis infections from ice cream. N Engl J Med,
1996. 334(20): p. 1281-6; Hedberg C.W., et al., A multistate
outbreak of Salmonella javiana and Salmonella oranienburg infections
due to consumption of contaminated cheese. JAMA, 1992. 268(22): p.
3203-7; Todd, E.C., et al., Outbreaks where food workers have been
implicated in the spread of foodborne disease. Part 4. Infective
doses and pathogen carriage. J Food Prot, 2004. 71: p. 2339-73;
Scheil W., et al., A South Australian Mdbandaka outbreak
investigation using a database to select controls. Aust NZ J Public
Health, 1998. 22(5): p. 536-9; Tamber, S., E. Swist, and D. Oudit,
Physicochemical and bacteriological characteristics of organic
sprouted chia and flax seed powders implicated in a foodborne
Salmonellosis outbreak. Journal of Food Protection, 2016. 79(5): p.
703-709.
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The 2023 risk profile identified 32 Salmonella serotypes of concern
linked to foodborne Salmonella outbreaks from chicken and turkey
products. These identified serotypes of concern informed all subsequent
risk management questions, including whether exposure to a small number
of these serotypes result in foodborne illness. Because the Salmonella
serotypes of public health significance identified in the final product
standards are among the 32 Salmonella serotypes of concern identified
in the risk profile and risk assessments, it is reasonable to conclude
that the serotypes of public health significance in the final product
standards all cause illness at a relatively low dose.
3. Severity of Illnesses
The 2023 risk profile found that exposure to the profile's
Salmonella subtypes of concern, which include the final product
standards serotypes of public health significance, can cause severe or
debilitating human health outcomes. Although the symptoms of Salmonella
infections are typically not reported to be as severe as some of those
associated with STEC, Salmonella can cause bloody diarrhea, fever,
abdominal cramps, nausea, and vomiting. In some instances, Salmonella
enters the blood stream and makes its way to other areas of the body
including, but not limited to, the heart, lung, bone, joints and the
central nervous system.\92\ This can result in severe illness requiring
hospitalizations and even death, especially in vulnerable populations,
such as very young, elderly, and immunocompromised individuals. Even
when Salmonella is no longer detectable in the body, prior Salmonella
illness has also been associated with an increased risk in colon
cancer.\93\ Also, the illness can cause debilitating, long-lasting
conditions including inflammatory bowel disease, irritable bowel
syndrome and reactive arthritis.
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\92\ Batz, M.B., et al., Long-Term consequences of foodborne
illness. Infect Dis Clin North Am, Sept 2013. 28(3) p. 599-661;
Hohmann, E.L., Nontyphoidal Salmonellosis, Clin Infect Dis, Sept
2001. 32 p. 263-269; Heymann, D. Salmonellosis. Control of
Communicable Disease Manual, 2021.
\93\ Mughini-Gras, L. et al. Increased colon cancer risk after
severe Salmonella infection. PLoS ONE, 2018. 13(1): p. 1-19, <a href="https://doi.org/10.1371/journal.pone.0189721">https://doi.org/10.1371/journal.pone.0189721</a>.
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[[Page 64699]]
Furthermore, a study that allows for a comparison of case-fatality
proportions of both Salmonella and STEC O157 demonstrates a higher
frequency of deaths among Salmonella cases than among STEC O157
cases.\94\ The estimated annual domestic foodborne illnesses reported
in the study were 1,027,561 and 63,153 for Salmonella and STEC O157,
respectively. Annual deaths from domestic foodborne illnesses are 378
and 20 for Salmonella and STEC O157, respectively. Therefore,
Salmonella deaths occur at a frequency of 4 per 10,000 illnesses, while
STEC O157 deaths occur at a frequency of 3 per 10,000 illnesses.
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\94\ Scallan, et al., 2011.
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4. Consumer Cooking Practices
As noted above, until recently, with the publication of the
proposed determination on Salmonella in NRTE breaded stuffed chicken
products, FSIS historically has not taken the position that certain
Salmonella levels or serotypes render raw poultry products adulterated
as defined in the PPIA. This position was based in part on the fact
that proper cooking kills pathogens on raw product. However, as
discussed below, several consumer behavior research studies suggest
that ordinary consumer cooking and preparation practices for chicken
carcasses, chicken parts, comminuted chicken, and comminuted turkey do
not provide adequate assurance that these products will not be
contaminated when consumed.
Consumer behavior research. FSIS recommends cooking poultry
products until the center of the thickest part of the meat reaches a
minimum internal temperature of 165 [deg]F measured by using a
thermometer to eliminate the presence of Salmonella and other foodborne
pathogens.\95\ However, although using a thermometer is the only
reliable way to ensure that poultry is properly cooked, studies show
that many consumers do not ordinarily use a thermometer to determine
whether whole chicken, chicken parts, comminuted chicken, and
comminuted turkey have reached an internal temperature sufficient to
destroy Salmonella. Studies also show that many consumers that do use a
thermometer do not always do so correctly.
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\95\ FSIS Safe Minimum Internal Temperature Chart. 2020;
Available at: <a href="https://www.fsis.usda.gov/food-safety/safe-food-handling-and-preparation/food-safety-basics/safe-temperature-chart">https://www.fsis.usda.gov/food-safety/safe-food-handling-and-preparation/food-safety-basics/safe-temperature-chart</a>.
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In a study published in 2017, a web-enabled panel survey of U.S.
adult grocery shoppers (n = 1,504) was conducted to describe consumers'
handling and preparation practices for raw poultry.\96\ The purpose of
the study was to characterize consumer food thermometer use and
barriers to use. The study found that of the 62 percent of the survey
respondents who reported owning a food thermometer, thermometer usage
was highest among those cooking whole turkeys (73.2 percent). Fewer
respondents reported using a thermometer when cooking whole chickens
(56.7 percent), chicken breasts or other parts (26.3%), and meatloaf or
a similar dish containing ground chicken or turkey (22.8 percent).
Reported thermometer use was lowest among respondents cooking patties
made with ground chicken or turkey (11.7 percent).
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\96\ KM Kosa, et al. (2017). Barriers to Using a Food
Thermometer When Cooking Poultry at Home: Results from a National
Survey. Food Protection Trends, 37/2, 116-125, available at: <a href="https://www.foodprotection.org/files/food-protection-trends/mar-apr-17-kosa.pdf">https://www.foodprotection.org/files/food-protection-trends/mar-apr-17-kosa.pdf</a>.
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Participants who reported owning a food thermometer identified
various reasons for not using a thermometer the last time they cooked
poultry at home. For all cuts of poultry, the most common reason
reported for not using a thermometer was use of another method to
determine that the product was properly cooked (49.8 to 61.5 percent of
respondents). The next most common reason selected was that the
respondent never thought to use a thermometer (27 to 37.6 percent of
respondents), which the researcher concluded suggests that these
respondents do not consider it very important to use a food
thermometer.
Of the respondents that reported using another method instead of a
food thermometer, most reported that they determined that poultry is
properly cooked by using visual cues, i.e., color, juice clarity, and
cleanliness of probing utensil. Of the 61.5 percent of the respondents
that reported using another method to determine that a whole turkey or
chicken is properly cooked, 42.2 percent cut the food to check that it
was no longer pink, 42.2 percent relied on cooking time, and 41 percent
checked that the juices ran clear. Of the 56.1 percent of the
respondents that reported using another method to determine that
chicken and turkey parts were properly cooked, 67.6 percent cut the
food to check that it was no longer pink, 46.2 percent relied on
cooking time and 40 percent checked that the juices ran clear. And of
the 49 percent of the respondents that reported using another method to
determine whether ground chicken or turkey was properly cooked, 61.5
percent inserted a knife, toothpick, or other utensil to see if it came
out clean, 55.4 percent relied on cooking time, and 21.0 percent cut
the food to check that it was no longer pink.
In an observational study published in 2016, 101 participants were
observed as they prepared poultry and egg items to determine whether
they followed food safety guidelines.\97\ The poultry items prepared
for the study were a baked whole chicken breast and a pan-fried ground
turkey patty. The study found that thermometer use for all products was
low. Only 37 percent of participants used a thermometer to determine
that a chicken breast was properly cooked, and only 22 percent used a
thermometer to determine that a turkey patty was properly cooked. For
the chicken breast, the most common method used to determine doneness
was cutting into the chicken (50 percent), followed by color (33
percent) and thermometer use (33 percent). For the turkey patty, the
most common indicator used was color (39 percent), followed by cutting
into it (30 percent), using a thermometer (22 percent), and looking at
the juices (18 percent). The study also found that the participants who
used a food thermometer often would use other methods, such as cutting
into them or observing the juices, to determine if the poultry items
were properly cooked.
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\97\ Maughan, et al. (2016). Food Handling Behaviors Observed in
Consumers When Cooking Poultry and Eggs. Journal of Food Protection,
79:6, 970-977, available at: <a href="https://www.sciencedirect.com/science/article/pii/S0362028X22080814?via%3Dihub">https://www.sciencedirect.com/science/article/pii/S0362028X22080814?via%3Dihub</a>.
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The study also highlighted the importance of correctly using a
thermometer to determine that poultry is properly cooked. Of the study
participants who used a thermometer, 36 percent did not use it
correctly in the chicken breast, the turkey patty, or both. The study
also found that there was no statistical difference between a
participant who did and did not use a thermometer in achieving an end
point temperature of at least 165 [deg]F in both the chicken breast and
the turkey patty. Seventy-eight percent of participants that used a
thermometer to cook the chicken breast reached a final internal
temperature above 165 [deg]F, compared to 75 percent for those who did
not use a thermometer. Seventy-seven percent of participants who used a
thermometer to cook a turkey patty reached a final internal temperature
of at least 165 [deg]F, compared to 66 percent of participants who did
not use a thermometer.
[[Page 64700]]
In another observational study published in 2014,\98\ 120
volunteers were observed as they prepared chicken and salad in their
homes. The study participants chose the manner of chicken preparation.
Three volunteers prepared whole chicken, and all others prepared
chicken parts. The study found that the most common method of
determining whether the chicken was properly cooked was appearance. In
response to a questionnaire administered after meal preparation, the
study participants stated that to determine whether chicken was
properly cooked, they looked for white colored meat, absence of blood
or pink spots, and firm meat. The study found that 40 percent of the
chicken that the participants considered to be properly cooked
registered a temperature below 165 [deg]F.
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\98\ Bruhn, C.M. (2014). Chicken preparation in the home: An
observational study. Food Protection Trends, 34(5):318-330.
Available at: <a href="https://www.proquest.com/trade-journals/chicken-preparation-home-observational-study/docview/1640787777/se-2">https://www.proquest.com/trade-journals/chicken-preparation-home-observational-study/docview/1640787777/se-2</a>.
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In this study, fewer than 5 percent of the participants voluntarily
used a thermometer to record chicken temperature during meal
preparation. When asked by the researcher if they wanted to check the
cooked chicken's temperature, 34 percent of the participants checked
the internal temperature using either their own thermometer or the
thermometer provided by the researcher. When chicken temperature was
taken, the internal temperature of 60 percent of the cooked chicken
registered 165 [deg]F or above. However, 39 percent of households
stopped cooking even though the internal temperature of the poultry
registered below 165 [deg]F.
A 2020 study used a randomized experimental design and direct
observation of meal preparation to test the effectiveness of a USDA
food safety video intervention for consumer thermometer use.\99\ The
study was conducted in test kitchen facilities in which cameras
recorded participants' meal preparation from beginning to end. A total
of 383 people participated in the study, 201 in the control group (the
group that did not watch the food safety video) and 182 in the
treatment group. Before preparing the meal, the treatment group watched
a 3-minute USDA food safety video on the importance of using a food
thermometer. Participants in the control and treatment groups were
observed while cooking turkey burgers and preparing a salad to
determine whether the participants used a thermometer to determine
whether the turkey patties were properly cooked. Following meal
preparation, all participants responded to a post observation interview
about food handling behaviors.
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\99\ Duong M, Shumaker ET, Cates SC, Shelley L, Goodson L,
Bernstein C, Lavallee A, Kirchner M, Goulter R, Jaykus LA, Chapman B
(2020). An Observational Study of Thermometer Use by Consumers When
Preparing Ground Turkey Patties. J Food Prot. 83(7):1167-1174.
Available at: <a href="https://www.sciencedirect.com/science/article/pii/S0362028X2210339X">https://www.sciencedirect.com/science/article/pii/S0362028X2210339X</a>.
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Sixty-one percent of the control group participants and 63 percent
of the treatment group participants reported owning a food thermometer,
which is consistent with the percentage of the respondents that
reported owning a food thermometer in the 2017 study discussed above
(62 percent). During the meal preparation session, the control group
used a thermometer to determine whether the turkey patties were
properly cooked 34 percent of the time, while the treatment group used
a thermometer 75 percent of the time. The control participants were
also less likely to insert the thermometer into the side of the patty
(23 percent), the recommended practice, than the treatment participants
(52 percent). Of the participants that used a thermometer and for whom
temperature data were available, the turkey patties were observed to
reach an internal temperature of 165 [deg]F 54 percent of the time for
the control group and 73 percent of the time for the treatment group.
Thus, while both the control and treatment groups were likely to own a
food thermometer, the control group was much less likely to use a food
thermometer, correctly place a thermometer, and cook patties to a safe
internal temperature than the treatment group.
The study also addressed whether the participants used methods
other than a thermometer to determine whether the turkey patty was
properly cooked. The study found that 45 percent of all participants
used a method other than a thermometer to determine that the turkey
patty was done cooking. Among participants who did not use the
thermometer and for whom usable data were available, 46 percent of
control group participants and 29 percent of the treatment group
participants relied on the firmness or texture of the patty to
determine that it was properly cooked, and 4 percent in the control
group and 16 percent in the treatment group relied on patty color.
Twenty-five percent of control group and 42 percent of treatment group
were observed using both firmness and color of the patty.
Thus, consumer research shows that, rather than using a thermometer
to check the internal temperature of whole chicken, chicken parts,
comminuted chicken products, and comminuted turkey products, many
consumers ordinarily rely on visual and textural cues to determine that
these products are properly cooked. However, because these subjective
cues have not been correlated with safe internal cooking temperature,
they are unreliable for gauging whether poultry products have reached
an internal temperature sufficient to destroy Salmonella that may be
present.\100\ As noted above, a 2014 observational study found that 40
percent of the chicken that participants considered to be properly
cooked based on subjective cues registered a temperature below 165
[deg]F. The 2017 survey study discussed above also cited a published
summary of food safety literature that concluded that 70 percent of
chicken pieces visually judged by consumers as ``done'' had not reached
a safe internal temperature.\101\ A European study that assessed the
effect of household cooking methods on the presence and numbers of
Salmonella Typhimurium in different types of raw poultry products found
that improper cooking produced inadequate heat treatments that did not
fully eliminate Salmonella from the products even when the initial
contamination levels were as low as 10 cfu/g.\102\ Thus, based on its
review of the available consumer research, FSIS has concluded that many
consumers do not cook chicken carcasses, chicken parts, comminuted
chicken, and comminuted turkey thoroughly and therefore, ordinary
consumer cooking practices associated with these products fail to
provide adequate assurance that the products will not be contaminated
when consumed.
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\100\ M. Duong et. al (2020).
\101\ Kosa, et al. (2017) citing CJ Byrd-Bredbenner et al.
(2013.) Food safety in home kitchens: a synthesis of the literature.
Int. J. Environ Res Publ Hlth 10:4060-4085.
\102\ Roccato A, Uyttendaele M, Cibin V, Barrucci F, Cappa V,
Zavagnin P, Longo A, Ricci A (2015). Survival of Salmonella
Typhimurium in poultry-based meat preparations during grilling,
frying and baking. Int J Food Microbiol 197:1-8. Available at:
<a href="https://www.sciencedirect.com/science/article/pii/S0168160514006011?via%3Dihub">https://www.sciencedirect.com/science/article/pii/S0168160514006011?via%3Dihub</a>.
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Cross-Contamination. In addition to consumer behavior research that
found that many consumers ordinarily rely on visual and textural cues
to determine that raw chicken and turkey products are properly cooked,
recent studies also found that there are other ordinary consumer
practices that create conditions for Salmonella exposure from raw
poultry regardless of whether the products are properly cooked.
Consumer hand washing practices are
[[Page 64701]]
one example of this cross-contamination concern.
A 2015 observational study of consumers handling raw poultry as
part of an at-home meal preparation event found that hands were washed
12 percent of the time after handling raw poultry.\103\ Of note, 100
percent of the s
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This is legal information, not legal advice. Laws vary by jurisdiction and change frequently. Always verify current law with official sources and consult a licensed attorney in your jurisdiction for advice on your specific situation.