Federal Register, Volume 89 Issue 85 (Wednesday, May 1, 2024)

[Federal Register Volume 89, Number 85 (Wednesday, May 1, 2024)]
[Notices]
[Pages 35033-35053]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2024-09393]

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Notices
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Federal Register / Vol. 89, No. 85 / Wednesday, May 1, 2024 /
Notices

[[Page 35033]]

DEPARTMENT OF AGRICULTURE

Food Safety and Inspection Service

[Docket No. FSIS-2022-0013]

Salmonella Not Ready-To-Eat Breaded Stuffed Chicken Products

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

ACTION: Final determination and response to comments.

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SUMMARY: FSIS is announcing its final determination that not ready-to-
eat (NRTE) breaded stuffed chicken products that contain Salmonella at
levels of 1 Colony Forming Unit per gram (hereinafter, ``1 CFU/g'') or
higher are adulterated within the meaning of the Poultry Products
Inspection Act (PPIA). FSIS is also announcing that it intends to carry
out verification procedures, including sampling and testing of the raw
incoming chicken components used to produce NRTE breaded stuffed
chicken products prior to stuffing and breading.

DATES: This final determination will be effective on May 1, 2025.

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

SUPPLEMENTARY INFORMATION:

Table of Contents

I. Background
II. Summary of Comments and Reponses
A. FSIS' Legal Authority and Adulteration Under the PPIA
B. Need for the Proposed Action
C. Definition of NRTE Breaded Stuffed Chicken Products
D. Food Emergency Response Network Survey
E. Outbreak Data
F. Salmonella Framework
G. Wait for Additional Information
H. Infectious Dose
I. Virulence
J. Consumer Behavior
K. Laboratory Methods
L. Verification Sampling
M. Implementation Date
N. Cost Benefit Analysis
O. Additional Action
P. Alternatives to the Proposed Action
III. Implementation
A. Hazard Analysis and Critical Control Point (HACCP)
Reassessment
B. Implementation and Status of Laboratory Methods
C. Sampled Lot
D. State Programs and Foreign Government Programs
IV. Anticipated Costs and Benefits of This Final Determination
V. USDA Non-Discrimination Statement
VI. Additional Public Notification

I. Background

On April 28, 2023, FSIS published a proposed determination (88 FR
26249) in which the Agency tentatively declared that NRTE breaded
stuffed chicken products contaminated with Salmonella at levels at or
above 1 CFU/g present a significant public health concern. This
proposed determination emphasized risks that are particular to these
products, given their unique characteristics. Specifically, data from
outbreak investigations, as well as consumer behavior research studies,
show that common consumer preparation practices associated with these
products may not destroy Salmonella that may be present in the product.
Information from consumer behavior research discussed in the proposed
determination (88 FR 26257) also shows that common consumer handling of
NRTE breaded stuffed chicken products may contribute to cross-
contamination. Further, the proposed determination noted that
Salmonella has been associated with severe and debilitating human
illness and available data suggest that the Salmonella infectious dose
can be relatively low (88 FR 26261-26264). In addition, outbreak data
cited in the proposed determination indicates that NRTE breaded stuffed
chicken products have been consistently and disproportionately
associated with Salmonella illness outbreaks over the years (88 FR
26252-26259). Based on the information discussed in the proposed
determination, FSIS tentatively concluded that previous efforts to
mitigate the public health concerns associated with these products,
which primarily focused on product labeling and outreach to inform
consumers that these products are raw and how to prepare them safely,
have failed to adequately ensure that consumer preparation of NRTE
breaded stuffed chicken products will result in a product that does not
contain Salmonella at levels sufficient to cause a high risk of human
illness when consumed. As such, FSIS tentatively determined that the
appropriate response to protect public health is to ensure that NRTE
breaded stuffed chicken products contaminated with Salmonella at levels
more likely to cause human illness are excluded from commerce (88 FR
26264).
FSIS specifically proposed to declare that NRTE breaded stuffed
chicken products contaminated with Salmonella at levels of 1 CFU/g or
above as adulterated under the PPIA. As discussed in the proposal, FSIS
tentatively concluded that when present in NRTE breaded stuffed chicken
products, Salmonella at 1 CFU/g or higher meets the definition of an
``added substance'' that ``may render'' them injurious to health
pursuant to 21 U.S.C. 453(g)(1) (88 FR 26260-26261). The proposal
further explained that FSIS also believes that NRTE breaded stuffed
chicken products that contain Salmonella at 1 CFU/g or higher meets the
more stringent ``ordinarily injurious'' standard under 21 U.S.C.
453(g)(1) (88 FR 26261). Moreover, the proposed determination
tentatively concluded that such products are adulterated under 21
U.S.C. 453(g)(3) because their elevated risk of illness makes them ``.
. . unsound, unhealthful, unwholesome, or otherwise unfit for human
food'' (88 FR 26261).
After reviewing comments on the proposed determination, FSIS is
finalizing the determination as proposed, with one exception. Based on
public comments, FSIS has decided to modify the verification sampling
location originally proposed to provide greater flexibility and reduce
costs to industry. Specifically, 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. FSIS is
also clarifying that

[[Page 35034]]

establishments may incorporate raw chicken components sampled by FSIS
into finished NRTE breaded stuffed chicken products so long as such
products remain under the establishments' control pending test results.
FSIS is also clarifying, as requested by commenters, that it does not
intend to begin FSIS sampling and verification testing discussed in
this determination until May 1, 2025. In addition, FSIS has considered
the economic effects of this determination and has updated the final
Cost Benefit Analysis (CBA) in response to public comments.

II. Summary of Comments and Reponses

FSIS received 3,386 comments on the proposed determination from
individuals, a laboratory services business, an association
representing the entire food industry, research institutes associated
with the meat and frozen foods industries, a society of meat industry
professionals, an animal welfare advocacy organization, trade
associations representing the poultry products industry, members of the
meat and poultry industry, and consumer advocacy organizations.
A summary of issues raised by commenters and the Agency's responses
follows.

A. FSIS' Legal Authority and Adulteration Under the PPIA

Comment: A trade association representing the poultry industry
asserted that FSIS does not have Congressional authorization to take
the actions discussed in the proposed determination. Poultry products
trade associations, members of the poultry products industry, a society
of meat industry professionals, and an institute representing the
interests of the meat industry asserted that FSIS' determination that
Salmonella is an added substance in NRTE breaded stuffed chicken
pursuant to 21 U.S.C. 453(g)(1) is inconsistent with legal precedent,
which holds that a substance is only ``added'' if it is artificially
introduced by a person.\1\ A poultry products trade association and an
institute representing the meat industry asserted that FSIS does not
have a legal basis to declare that any level of Salmonella ordinarily
renders NRTE breaded stuffed chicken injurious to health under 21
U.S.C. 453(g)(1), given the courts have previously determined that
consumers prepare raw chicken in a manner that destroys Salmonella.\2\
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\1\ United States v. Anderson Seafoods, Inc., 622 F.2d 157 (5th
Cir. 1980). United States v. Coca Cola, 241 U.S. 265 (1915).
\2\ Texas Food Industry Association v. Espy, 870 F. Supp. 143,
149 (W.D. Tex. 1994). American Public Health Association v. Butz,
511 F.2d 331, 334 (D.C. Cir. 1974). Supreme Beef Processors, Inc. v.
USDA, 275 F.3d 432, 438-39 (5th Cir. 2001). See also, e.g., Starr
Surplus Lines Ins. Co. v. Mountaire Farms Inc., 920 F.3d 111, 117
(1st Cir. 2019). (``[T]he mere fact of the FSIS-orchestrated recall
does not give rise to the plausible inference that the type of
Salmonella found . . . could not be eliminated by proper
cooking.''); Craten v. Foster Poultry Farms Inc., 305 F. Supp.3d
1051, 1058 (D. Ariz. 2018) (observing that existing case law
``suggests Salmonella is not an adulterant'' and rejecting several
state law tort claims because Salmonella ``is killed through proper
cooking, which is how raw chicken products are intended to be
used'').
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On the other hand, consumer advocacy organizations agreed with the
Agency's tentative conclusion that Salmonella is an added substance in
NRTE breaded stuffed chicken and is thus subject to the ``may render
injurious'' standard. The commenters also agreed with FSIS' tentative
conclusion that NRTE breaded stuffed chicken products that contain
Salmonella at 1 CFU/g or higher meet the more stringent ``ordinarily
injurious'' standard, because ordinary consumer handling and
preparation preserves levels in the end product that result in illness.
Response: The PPIA provides FSIS with the authority to regulate
poultry to ensure that adulterated products do not enter commerce.\3\
Furthermore, Congress, at 21 U.S.C. 453(g)(1), declared two standards
for determining whether a product is adulterated. First, if a substance
is an ``added substance'' the product is adulterated if the substance
may render the product injurious to health. Second, if the substance is
not added, the product is adulterated if the quantity of such substance
in or on the product ordinarily renders it injurious to health.
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\3\ 21 U.S.C. 451 and 452.
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As discussed in the proposed determination (88 FR 26250-26251),
this is not the first time that FSIS has exercised its authority to
designate a foodborne pathogen as an adulterant in a raw product. In
September 1994, FSIS stated that it considered raw ground beef
contaminated with Escherichia coli O157:H7 (E. coli O157:H7) to be
adulterated within the meaning of an identical adulteration provision
in the Federal Meat Inspection Act (FMIA; 21 U.S.C. 601(m)), and that
the Agency was prepared to use the enforcement provisions of that
statute to exclude adulterated product from commerce. At the same time,
FSIS indicated that it would begin to sample raw ground beef at
federally regulated establishments and in commerce.\4\ Shortly after
the 1994 decision, a group of supermarket and meat industry
organizations filed suit in the U.S. District Court for the Western
District of Texas to reverse FSIS' determination, arguing the Agency
exceeded its statutory authority by declaring E. coli O157:H7 to be an
adulterant under the FMIA. The court ruled in favor of FSIS.\5\ The
Agency then updated its policy in 1999, declaring E. coli O157:H7 to
also be an adulterant of intact beef cuts that are to be further
processed into nonintact raw products before being distributed for
consumption. In 2011, FSIS declared that six additional Shiga Toxin-
Producing Escherichia coli (STEC) serogroups (O26, O45, O103, O111,
O121, and O145) are adulterants of raw non-intact beef products and raw
intact beef components intended to be used in these products.\6\
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\4\ Michael R. Taylor, FSIS Administrator. September 29, 1994.
``Change and Opportunity to Improve the Safety of the Food Supply.''
Speech to American Meat Institute Annual Convention, San Francisco,
CA.
\5\ See Texas Food Industry Association v. Espy, 870 F. Supp.
143 (1994).
\6\ 76 FR 58157, Sept. 20, 2011.
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FSIS is now taking similar action, declaring Salmonella to be an
adulterant in NRTE breaded stuffed chicken when present at levels at or
above 1 CFU/g. FSIS based this decision on the best available science
and data using similar criteria as in its 1994, 1999, and 2011 STEC
policymaking. This determination, like the STEC determinations, is
within the scope of the Agency's statutory authority.
The adulteration definition in 21 U.S.C. 453(g)(1) includes two
standards for determining whether a product is adulterated. Under 21
U.S.C. 453(g)(1), if a substance is an ``added substance'' the product
is adulterated if the substance ``may render'' the product injurious to
health. If the substance is not added, the product is adulterated ``if
the quantity of such substance in or on'' the product ``ordinarily''
renders it injurious to health.
FSIS has determined that when present in NRTE breaded stuffed
chicken products, Salmonella at 1 CFU per gram or higher meets the
definition of an ``added substance'' that ``may render'' these products
injurious to health. As discussed in the proposed determination (88 FR
26260-26261) and herein, (processing can add Salmonella to previously
uncontaminated NRTE breaded stuffed chicken components and may increase
the occurrence of Salmonella throughout the finished product overall.
As such, some portion of Salmonella present in the NRTE

[[Page 35035]]

breaded stuffed chicken products has been introduced by humans.
While no court has addressed whether Salmonella in processed
poultry products is an ``added substance'' under the PPIA, FSIS'
determination that Salmonella at 1 CFU/g is an added substance in NRTE
breaded stuffed chicken is consistent with the holding in United States
v. Anderson Seafoods (622 F.2d 157 (1980)). The issue directly before
the court in U.S. v. Anderson Seafoods was the meaning of the term
``added substance'' as used in an adulteration provision of the Federal
Food, Drug, and Cosmetic Act (FFDCA), which, in relevant parts, is
identical to the ``added substance'' provision in the
PPIA.^{7 8} U.S. v. Anderson Seafoods involved hazardous levels
of mercury in swordfish. Specifically, the issue before the court was
whether all mercury in the fish should be considered an ``added
substance'' under the adulteration provisions of the FFDCA and thus
subject to the ``may render injurious standard'' when some mercury in
swordfish occurs naturally and some is the result of man-made
pollution. After considering the legislative history and relevant case
law, the court found that the term ``added,'' as used in the FFDCA,
means ``artificially introduced, or attributable in some degree to the
acts of man.'' \9\ The court also held that the ``may render it
injurious to health'' standard applies to the food, not to the added
substance and, therefore, ``where some portion of a toxin present in a
food has been introduced by [humans], the entirety of that substance
present in the food will be treated as an added substance.'' \10\
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\7\ The definition in the FFDCA provides that ``A food shall be
deemed to be adulterated (a)(1) if 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
food shall not be considered adulterated under this clause if the
quantity of such substance in such food does not ordinarily render
it injurious to health'' (21 U.S.C. s 342(a)(1)).
\8\ While the PPIA defines the circumstances in which a poultry
product may be adulterated, FSIS has referred to the FFDCA as a
substantially similar statute to further elucidate the meaning that
terms are given in a similar provision. See, e.g., FSIS final
response to petition #12-02, Petition to Require Labeling of All
Ritually Slaughtered Meat and Poultry (Jan 1, 2012) p. 2. Available
at: https://www.fsis.usda.gov/federal-register/petitions/petition-require-labeling-all-ritually-slaughtered-meat-and-poultry.
\9\ United States v. Anderson Seafoods, Inc622 F.2d 157, 160
(citing United States v. Coca Cola, 241 U.S. 265 (1915)).
\10\ United States v. Anderson Seafoods, Inc622 F.2d 157, 161.
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As discussed in the proposed determination (88 FR 26260-26261) and
herein, processing can add Salmonella to previously uncontaminated NRTE
breaded stuffed chicken components and may increase the occurrence of
Salmonella throughout the finished product overall. As such, some
portion of Salmonella present in the NRTE breaded stuffed chicken
products has been introduced by man and, in accordance with the holding
in Anderson Seafoods, all Salmonella in this product should be treated
as an ``added substance'' and may be regulated under the PPIA's ``may
render injurious'' standard.
In addition, FSIS' believes 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, satisfying the
definition of ``adulterated'' under 21 U.S.C. 453(g)(1). This
determination also does not conflict with legal precedent. The Agency
recognizes that, historically, most foodborne pathogens, including
Salmonella, have not been considered adulterants of raw and other NRTE
meat and poultry based on the assumption that ordinary cooking is
generally sufficient to destroy the pathogens.
However, NRTE breaded stuffed chicken products are NRTE multi-
ingredient, further processed products that often contain multiple raw
poultry source materials and are heat treated in a manner that
typically imparts an RTE appearance. As noted in the proposed
determination (88 FR 26249), consumer research, together with
information gathered during outbreak investigations, clearly show that,
because of these unique product characteristics, which make these
products particularly risky, consumers often do not prepare these
products properly, even when the products display adequate cooking
instructions and statements on the label. FSIS is not aware of any
court that has analyzed the status of Salmonella as an adulterant in
NRTE breaded stuffed chicken products, giving due weight to the
products' unique characteristics, consumer behaviors, public health
risks associated with these products, or the most recent science and
data concerning Salmonella in NRTE breaded stuffed chicken products.
Comment: A group of consumer advocacy organizations agreed with
FSIS' position and reasoning in the proposed determination that
Salmonella is an added substance pursuant to 21 U.S.C. 453(g)(1) in
NRTE breaded stuffed chicken products. However, poultry products trade
associations, members of the poultry products industry, a society of
meat industry professionals, and an institute representing the
interests of the meat industry disagreed with FSIS' determination,
arguing that Salmonella exists naturally in chicken, and provided
studies that they assert show that Salmonella exists naturally in
muscle tissue.^{11 12 13 14} These commenters also stated that
FSIS did not adequately support its view that cross-contamination
during further processing is responsible for the presence of Salmonella
in chicken components used to create NRTE breaded stuffed chicken
products.
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\11\ Rimet, C.S., Maurer, J.J., Pickler, L., Stabler, L.,
Johnson, K.K., Berghaus, R.D., . . . & Fran[ccedil]a, M. (2019).
Salmonella harborage sites in infected poultry that may contribute
to contamination of ground meat. Frontiers in Sustainable Food
Systems, 3, 2.
\12\ Angela Cook et al., Campylobacter, Salmonella, Listeria
monocytogenes, Verotoxigenic Escherichia coli, and Escherichia coli
Prevalence, Enumeration, and Subtypes on Retail Chicken Breasts with
and without Skin, 75(1) J. Food Protection 34-40 (Jan. 2012).
\13\ Husnu Sahan Guran et al., Salmonella prevalence associated
with chicken parts with and without skin from retail establishments
in Atlanta metropolitan area, Georgia, 73(B) Food Control 462-67
(Mar. 2017).
\14\ A. Pointon et al., A Baseline Survey of the Microbiological
Quality of Chicken Portions and Carcasses at Retail in Two
Australian States (2005 to 2006), 71(6) J. Food Protection 1123-34
(Jun. 2008).
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Response: In the proposed determination, FSIS specifically
evaluated whether Salmonella should be considered an added substance in
NRTE breaded stuffed chicken (88 FR 26260-26261). Although FSIS agrees
with the commenters that Salmonella naturally exists in certain parts
of poultry before processing, such as the skin, livers, feather
follicles, and bones, the Agency noted that Salmonella is not
ordinarily found in the muscle tissue of healthy birds. NRTE breaded
stuffed chicken products contain raw, comminuted chicken breast meat,
trim, or whole chicken breast meat (i.e., further processed chicken
parts or comminuted chicken). FSIS sampling data has shown that further
processed chicken parts (legs, breasts, and wings) and comminuted
chicken have a higher occurrence of Salmonella positive results
compared to carcasses.^{15 16}
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\15\ Sampling Results for FSIS-Regulated Products. Available at:
https://www.fsis.usda.gov/science-data/sampling-program/sampling-results-fsis-regulated-products.
\16\ USDA FSIS Annual Sampling Summary Report 2022. Available
at: https://www.fsis.usda.gov/sites/default/files/media_file/documents/FY2022-Sampling-Summary-Report.pdf.
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As FSIS noted in the proposed determination (88 FR 26260), these
sampling data indicate that, during processing, Salmonella that is
regularly present in certain parts of the bird is added to the interior
of edible poultry muscle tissue, where Salmonella is not ordinarily
found. The proposed

[[Page 35036]]

determination cited several instances of how such cross-contamination
could occur (88 FR 62260). For one, when poultry is cut, Salmonella in
the skin and feather follicles can be exposed and spread during
processing to previously uncontaminated product. ^{17 18 19}
Additionally, many NRTE breaded stuffed chicken products are made with
comminuted chicken. Because of the nature of comminution, Salmonella
contamination in chicken skin and bone can spread throughout an entire
batch or lot through cross-contamination. FSIS sampling data show that
ground and other raw comminuted chicken products that were produced
using either bone-in or skin-on source materials were more likely to be
contaminated with Salmonella than those fabricated from deboned,
skinless source materials.\20\ In addition, Salmonella-negative raw
poultry parts and comminuted poultry may become cross-contaminated by
contact with Salmonella-contaminated equipment or when they are
commingled with Salmonella-positive products, such as when they are
collected in combo bins for further processing.^{21 22}
Salmonella-contaminated equipment used to incorporate the stuffed
ingredients into the chicken component of NRTE breaded stuffed chicken
products may also contribute to Salmonella contamination in these
products. For these reasons, FSIS considers Salmonella an added
substance in NRTE breaded and stuffed chicken products. It is important
to note that the determination that Salmonella is an added substance in
NRTE breaded and stuffed chicken products is based on the circumstances
under which these particular products are fabricated and processed and
that FSIS has not made a determination about whether Salmonella is an
added substance in any other raw poultry products. FSIS will address
the status of Salmonella in other raw poultry products in a subsequent
rulemaking proceeding after considering the comments received in that
proceeding.
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\17\ Kim J-W and Slavik MF. 1996. Cetylpyridinium Chloride (CPC)
treatment on poultry skin to reduce attached Salmonella. J. Food
Prot. 59: 322-326.
\18\ Wu D, Alali WQ, Harrison MA, and Hofacre CL. 2014.
Prevalence of Salmonella in neck skin and bone of chickens. J Food
Prot. 77(7): 1193-1197.
\19\ FSIS Guidance for Controlling Salmonella in Raw Poultry
(June 2021) pp. 59-60. Available at: https://www.fsis.usda.gov/guidelines/2021-0005.
\20\ FSIS Guidance for Controlling Salmonella in Raw Poultry
(June 2021) pp. 65-66, Table 4 FSIS exploratory sampling test
results, raw comminuted chicken by source material composition (6/1/
13-6/30/15, 2,688 samples. Available at: https://www.fsis.usda.gov/guidelines/2021-0005.
\21\ FSIS Guidance for Controlling Salmonella in Raw Poultry
(June 2021) pp. 59. Available at: https://www.fsis.usda.gov/guidelines/2021-0005.
\22\ Codex Guideline for the Control of Campylobacter and
Salmonella in Chicken Meat at https://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCXG%2B78-2011%252FCXG_078e.pdf.
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Industry commenters provided a study in which researchers tested
poultry muscle tissue for the presence of Salmonella.\23\ However, the
study was not sensitive enough to draw the conclusion that Salmonella
at 1 CFU/g or higher is ordinarily present in such tissue. In the
study, 1-day old chicks were deliberately inoculated with highly
pathogenic Salmonella before development of healthy gut microflora.
Thus, the initial load of Salmonella in the tested birds was not
necessarily representative of the pathogen levels ordinarily present in
farm-raised poultry.\24\ Moreover, the study had a very small sample
size and, in the end, only one out of five muscle tissue samples
collected from 42-day old birds were positive for the Salmonella
serotypes tested.\25\ Thus, this study does not serve as demonstrable
evidence that Salmonella is ordinarily present in the muscle tissue of
farm-raised poultry. In fact, the study concluded that the high
prevalence of Salmonella in the skin of infected poultry significantly
contributes to contamination of ground chicken and turkey and suggested
that the exclusion of skin as a component of ground poultry may be the
best option for reducing Salmonella contamination in ground poultry
products. This finding, therefore, supports FSIS' position that,
amongst other things, Salmonella contaminated chicken skin
substantively contributes to the spread of the pathogen in NRTE breaded
stuffed chicken products, including to components that do not
ordinarily contain Salmonella.
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\23\ Rimet, C.S., Maurer, J.J., Pickler, L., Stabler, L.,
Johnson, K.K., Berghaus, R.D., . . . & Fran[ccedil]a, M. (2019).
Salmonella harborage sites in infected poultry that may contribute
to contamination of ground meat. Frontiers in Sustainable Food
Systems, 3, 2.
\24\ FSIS notes that--for farm raised birds--there are many
options to eliminate or reduce the Salmonella contamination,
including pre-harvest food safety control measures. Elimination
efforts can include rearing and management practices, pre and
probiotic use, antimicrobial therapy, and/or vaccination of birds.
See, e.g., Foley, S.L., Nayak, R., Hanning, I.B., Johnson, T.J.,
Han, J., & Ricke, S.C. (2011). Population dynamics of Salmonella
enterica serotypes in commercial egg and poultry production. Applied
and environmental microbiology, 77(13), 4273-4279.
\25\ Forty-two days is the approximate age when broilers are
slaughtered. FSIS also notes that in the four weeks prior, only one
sample in the study tested positive for either serotype and only
after enrichment.
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Industry also cites three other papers they say show that
Salmonella prevalence is the same in skin-on and skin-off
chicken.^{26 27 28} The commenters assert these studies prove
that Salmonella naturally occurs in poultry muscle tissue. However,
these papers show variable results for Salmonella detection in skin-off
versus skin-on chicken.^22-24 Two studies, Cook 2012 and
Pointon 2008, showed similar rates of Salmonella between the skin-on
and skin-off parts using a rinse sampling method. In contrast, the
third study, Guran 2017, showed Salmonella presence in skin-on chicken
parts was significantly higher than in the skin-off parts with 44.7% vs
12.3% positive for chicken breast and 40.9% vs 22.8% positive for
chicken thighs when samples were mixed by stomaching.\23\ The variable
results from the studies discussed could be due to methodology
differences. Researchers have noted that rinse sampling methods may not
recover Salmonella that are firmly attached to the skin or trapped
within skin folds and feather follicles, while vigorous mixing using a
stomacher may release attached Salmonella therefore increasing
detection.^{29 30} A study by Wu 2014 supports this, showing
rinsed skin samples recovered significantly less Salmonella than skin
that was stomached (2.3 vs. 20.7%).\31\
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\26\ Angela Cook et al., Campylobacter, Salmonella, Listeria
monocytogenes, Verotoxigenic Escherichia coli, and Escherichia coli
Prevalence, Enumeration, and Subtypes on Retail Chicken Breasts with
and without Skin, 75(1) J. Food Protection 34-40 (Jan. 2012).
\27\ Husnu Sahan Guran et al., Salmonella prevalence associated
with chicken parts with and without skin from retail establishments
in Atlanta metropolitan area, Georgia, 73(B) Food Control 462-67
(Mar. 2017).
\28\ A. Pointon et al., A Baseline Survey of the Microbiological
Quality of Chicken Portions and Carcasses at Retail in Two
Australian States (2005 to 2006), 71(6) J. Food Protection 1123-34
(Jun. 2008).
\29\ Wu D, Alali WQ, Harrison MA, and Hofacre CL. 2014.
Prevalence of Salmonella in neck skin and bone of chickens. J Food
Prot. 77(7): 1193-1197.
\30\ Husnu Sahan Guran et al., Salmonella prevalence associated
with chicken parts with and without skin from retail establishments
in Atlanta metropolitan area, Georgia, 73(B) Food Control 462-67
(Mar. 2017).
\31\ Wu D, Alali WQ, Harrison MA, and Hofacre CL. 2014.
Prevalence of Salmonella in neck skin and bone of chickens. J Food
Prot. 77(7): 1193-1197.
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At an industry level, poultry skin is a known source of Salmonella
contamination due to bacteria being trapped in the skin folds and
feather follicles.\32\ These areas may not be accessible until they are
disturbed

[[Page 35037]]

during cutting or grinding. When this processing exposes and releases
the pathogen, it can spread, resulting in higher contamination levels
in the product. FSIS sampling data clearly indicates Salmonella poultry
rates rise as poultry is further processed, from chicken carcasses at
4.14% to legs, breasts, wings at 7.62% to comminuted at 24.2%.\33\ This
is a pattern FSIS has observed yearly and based on more than 25,000
samples analyzed in FY2022 alone.\34\
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\32\ FSIS Guidance for Controlling Salmonella in Raw Poultry
(June 2021). Available at: https://www.fsis.usda.gov/guidelines/2021-0005.
\33\ USDA FSIS Annual Sampling Summary Report 2022. Available
at: https://www.fsis.usda.gov/sites/default/files/media_file/documents/FY2022-Sampling-Summary-Report.pdf
\34\ Moreover, national prevalence data from chicken parts
baseline sampling indicate that skin-on parts were more likely to be
positive for Salmonella than parts without skin. See The Nationwide
Microbiological Baseline Data Collection Program: Raw Chicken Parts
Survey (2012), available at: https://www.fsis.usda.gov/sites/default/files/media_file/2020-07/Baseline_Data_Raw_Chicken_Parts.pdf.
---------------------------------------------------------------------------

Comment: A few commenters, including trade associations
representing the poultry products and frozen foods industries, asserted
that the evidence cited in the proposed determination does not indicate
that NRTE breaded stuffed chicken products contaminated with Salmonella
are ordinarily injurious to health. First, they argued that the
outbreak data cited does not indicate that the products have harmed a
substantial amount of people. They also argued that outbreak
investigations do not indicate that consumers ordinarily prepare NRTE
breaded stuffed chicken in a manner that renders them unsafe to eat.
Response: NRTE breaded stuffed chicken products pose a substantive
risk to public health. The data available show that NRTE breaded
stuffed chicken products are inherently risky, given their unique
characteristics, and have a disparate impact on public health.
Specifically, as noted above and in the proposed determination (88 FR
26252), an analysis of all chicken associated outbreaks identified in
the Centers for Disease Control and Prevention's (CDC) National
Outbreak Reporting System (NORS) \35\ or in the scientific literature
from 1998-2020 found that, during this time, NRTE breaded stuffed
chicken products accounted for less than 0.15 percent of the total
domestic chicken supply yet represented approximately five percent of
all chicken-associated Salmonella outbreaks in the United States.
Specifically, although NRTE breaded stuffed chicken products make up a
very small percentage of the total domestic supply of chicken, they
have been associated with 14 Salmonella outbreaks between 1998 and
2021, resulting in 195 reported illnesses and 41 reported
hospitalizations (88 FR 26258-26259). The actual number of cases is
likely higher than the number of reported cases.\36\
---------------------------------------------------------------------------

\35\ CDC National Outbreak Reporting System available at:
https://www.cdc.gov/nors/index.html.
\36\ Scallan, et al. 2011; Mead, P.S., et al., Food related
illnesses and deaths in the United States. Emerging Infect Dis,
Oct1999. 5(5) p. 607-625.
---------------------------------------------------------------------------

As discussed in the proposed determination (88 FR 26263),
Salmonella can cause bloody diarrhea, fever, abdominal cramps, nausea,
and vomiting. In some instances, Salmonella enters the blood 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.\37\ 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 and can cause
debilitating, long-lasting conditions including inflammatory bowel
disease, irritable bowel syndrome and reactive arthritis.\38\
---------------------------------------------------------------------------

\37\ 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.
\38\ Mughini-Gras, L. et al. Increased colon cancer risk after
severe Salmonella infection. PLoS ONE, 2018. 13(1): p. 1-19. https://doi.org/10.1371/journal.pone.0189721.
---------------------------------------------------------------------------

Comment: A few poultry products trade associations stated that the
proposed determination did not explain or support why Salmonella,
particularly at 1 CFU/g, would render a NRTE breaded stuffed chicken
product adulterated under 21 U.S.C. 453(g)(3).
Response: 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, unwholesome,
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).
As discussed in the proposal (88 FR 26261), FSIS evaluated the
available information on Salmonella associated with human illnesses,
the Salmonella infectious dose, the severity of human illnesses caused
by Salmonella, and consumer preparation practices associated with NRTE
breaded stuffed chicken product as documented in outbreak
investigations associated with these products and consumer behavior
research studies. Based on this evaluation, FSIS concluded that NRTE
breaded stuffed chicken products contaminated with Salmonella at levels
of 1 CFU/g present a sufficiently serious risk of causing Salmonella
illness. Thus, as discussed in the proposed rule, FSIS has determined
that such products 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'' (82 FR 26261).

B. Need for the Proposed Action

Comment: Many commenters, including an animal welfare organization,
two consumer advocacy groups, and several individuals, stated FSIS'
proposed action is necessary to assure NRTE breaded stuffed chicken
products are safe to eat. However, a few poultry products trade
associations and an institute representing the meat industry asserted
that the proposed determination is not necessary to protect public
health. These commenters specifically asserted the rate of
salmonellosis associated with all chicken products has decreased over
the past ten years. They also stated that public health efforts by the
industry and FSIS have already made NRTE breaded stuffed chicken
products safe to eat.
Response: As discussed throughout the proposed determination (88 FR

[[Page 35038]]

26249), FSIS is specifically targeting Salmonella in NRTE breaded
stuffed chicken products because their unique characteristics make them
particularly risky, and they pose a disparate impact on consumers'
health. There have been 14 recorded outbreaks associated with the
consumption of NRTE breaded stuffed chicken products since 1998, with
the latest outbreak occurring as recently as 2021. Salmonella outbreaks
have been disproportionately associated with NRTE breaded stuffed
chicken products. Specifically, an analysis of all chicken associated
outbreaks identified in the CDC's NORS \39\ and in the scientific
literature from 1998-2020 found that, during this time, NRTE breaded
stuffed chicken products accounted for less than 0.15 percent of the
total domestic chicken supply yet represented approximately five
percent of all chicken-associated outbreaks in the United States (88 FR
26252). Outbreaks associated with these products have continued to
occur regularly despite updated labeling instructions, outreach, and
other industry and Agency efforts to make the products safer and ensure
consumers are aware of how to prepare them (88 FR 26259-26260).
Moreover, data from outbreak investigations and consumer research
discussed in the proposed determination show that many consumers
continue to cook NRTE breaded stuffed chicken products in a manner that
does not adequately destroy Salmonella in these products (88 FR 26252-
26260).
---------------------------------------------------------------------------

\39\ CDC National Outbreak Reporting System available at:
https://www.cdc.gov/nors/index.html.
---------------------------------------------------------------------------

C. Definition of NRTE Breaded Stuffed Chicken Products

Comment: Trade associations and institutes representing the meat
and poultry foods industries asked FSIS to clarify what products are
subject to this final determination and noted that it should not apply
to frozen NRTE products that are not breaded or stuffed, or that appear
raw. A trade association representing the poultry products industry
specifically asserted that the determination should not include NRTE
breaded stuffed chicken products intended for use by hotel, restaurant,
or institutional consumers.
Response: As discussed in the proposed determination (88 FR 26252),
FSIS specifically defines NRTE breaded stuffed chicken products as
those NRTE products that are both breaded and stuffed, contain raw
chicken components (e.g., comminuted chicken breast meat, trim, or
whole chicken breast meat), and where 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. Only products that
specifically meet this definition are subject to the 1 CFU/g or higher
adulteration standard discussed in this final determination. As
discussed in the proposed determination (88 FR 26266--26267) and
herein, FSIS will also conduct verification sampling in federally
regulated establishments that produce such products. Thus, this final
determination does not apply to RTE products (e.g., fully cooked RTE
chicken cordon bleu). In addition, NRTE products that are stuffed and
breaded, but are not ``par-fried,'' ``pre-browned,'' or otherwise heat
treated to only set the batter or breading, are not subject to this
final determination.\40\ This final determination also does not apply
to NRTE stuffed products that are not breaded, such as turducken or
whole stuffed chickens--nor to NRTE breaded products that are not
stuffed, such as chicken nuggets. Under this determination, NRTE
breaded stuffed chicken that contain Salmonella at or above 1 CFU/g
will be considered adulterated even if intended for hotel, restaurant,
or institutional use because, regardless of intended use, NRTE breaded
stuffed chicken products have characteristics that can make effective
cooking of these products more challenging, i.e., they may appear fully
cooked, are typically cooked from a frozen state, and are thicker in
diameter and have a different composition than other par-fried breaded
products (82 FR 26252).
---------------------------------------------------------------------------

\40\ For example, if a meat counter at a retail store were to
stuff a chicken breast with cheese and roll it in breadcrumbs, but
not heat treat the product to set the breading, the product would
not be subject to this determination.
---------------------------------------------------------------------------

D. Food Emergency Response Network Survey

Comment: A few poultry product trade associations asserted that
they did not have the time or information necessary to respond to the
Food Emergency Response Network (FERN) Survey.\41\ Specifically, these
commenters argued that the Agency published the FERN Survey during the
proposed determination's comment period, leaving inadequate time for
analysis and comment. They also asserted that FSIS never explained why
this survey was relevant or how it supported the proposed
determination.
---------------------------------------------------------------------------

\41\ FSIS, Survey of Not Ready-to-Eat Breaded and Stuffed
Chicken Products for Salmonella, Docket ID No FSIS-2022-0013-0015
(June 2023).
---------------------------------------------------------------------------

A few poultry product trade associations and an institute
representing the meat industry also raised some specific issues with
the FERN Survey. First, they noted that it did not utilize the
laboratory or sampling methods discussed in the proposed determination.
Second, these commenters stated that the samples were not weighted to
reflect relative production volume, they were not geographically
dispersed, and that no statistical analysis was performed on the base
results. The commenters also stated that the study lacked statistical
power, given minimal samples were collected over a short period of
time.
Response: FSIS disagrees with the assertion that the Agency never
explained why the FERN Survey was relevant or how it was used to inform
the proposed determination. The proposed determination discussed the
FERN Survey report in detail (88 FR 26265-26266). FSIS gave the public
adequate time and information to respond to the FERN Survey report.
After release of the FERN Survey report, FSIS extended the proposed
determination's comment period to August 11, 2023, to give the public
more time to review the materials and formulate comments. Furthermore,
the survey's methodology and results--as well as FSIS' analysis--were
discussed in detail in the proposed determination (88 FR 26265-26266),
which published 105 days prior to the close of the comment
period.^{42 43}
---------------------------------------------------------------------------

\42\ FSIS Constituent Update--June 23, 2023. Available at:
https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-june-23-2023.
\43\ FSIS, Survey of Not Ready-to-Eat Breaded and Stuffed
Chicken Products for Salmonella, Docket ID No FSIS-2022-0013-0015
(June 2023).
---------------------------------------------------------------------------

In regard to the specific issues with the FERN Survey raised by
commenters, the FERN Survey report made clear that the data were
derived from convenient sampling of eligible products available to the
participating laboratories and that FSIS made no claims about the
statistical significance of any differences observed \44\ or about how
this survey supports FSIS enumeration methodology. Indeed, FSIS
explained that the survey was intended to collect information on the
positive rate of Salmonella in NRTE breaded stuffed chicken purchased
at retail and differences in testing strategies, which were intended to
help inform the FSIS verification sampling plan resulting from this
determination. The FERN Survey results indicate that the current FSIS
testing methods are acceptable for these products because the FERN labs

[[Page 35039]]

tested samples using the validated methods. The survey was also
conducted to help inform the FSIS sampling and verification testing
resulting from this determination.
---------------------------------------------------------------------------

\44\ Survey of Not Ready-to-Eat Breaded and Stuffed Chicken
Products for Salmonella (usda.gov).
---------------------------------------------------------------------------

As explained in the proposed determination (88 FR 26265), the FERN
Survey gathered data at retail to provide information about the
Salmonella-positive rate of NRTE breaded stuffed chicken products. In
the proposal, FSIS noted that when using FSIS methods and a larger test
portion, the survey found that the 27 percent positive rate for
Salmonella in NRTE breaded stuffed chicken products detected in retail
samples is comparable to the 29 percent positive rate detected in FSIS
sampling of comminuted chicken.\45\ The Agency also noted that these
rates are higher than the Salmonella-positive rates for other raw
chicken products, which suggests that NRTE breaded stuffed chicken
products and comminuted chicken have a higher risk than other raw
chicken. However, as noted in the proposal, consumer preparation
practices are more likely to mitigate the risk associated with
comminuted or ground chicken because, unlike NRTE breaded stuffed
chicken products, ground chicken clearly appears raw and is not
typically cooked from a frozen state (88 FR 26265).
---------------------------------------------------------------------------

\45\ USDA Food Safety and Inspection Service Annual Sampling
Report Fiscal Year 2021: https://www.fsis.usda.gov/sites/default/files/media_file/2022-02/FY2021-Sampling-Summary-Report.pdf.
---------------------------------------------------------------------------

E. Outbreak Data

Comment: A poultry products trade association argued that FSIS
placed too much emphasis on the duration of outbreaks associated with
NRTE breaded stuffed chicken products to support its decision, noting
that the length of an outbreak is not necessarily related to its
severity. It also asserted that statements gathered during outbreak
investigations are anecdotal and, thus, not adequate to support FSIS'
conclusion that consumers do not safely prepare NRTE breaded stuffed
chicken products. Moreover, the commenter noted that most of the
outbreak investigations FSIS discussed were associated with outdated
product labeling and used antiquated investigational methods.
Response: The outbreak data--together with the other evidence
discussed in the proposed determination (88 FR 26249)--supports the
conclusion that NRTE breaded stuffed chicken products are
disproportionately associated with Salmonella illnesses compared to
other raw poultry products and that, despite industry and Agency
efforts, consumers continue to prepare such products in a manner that
does render them safe to eat. The outbreak investigation findings
discussed in the proposed determination (88 FR 26252-26259) were not
based on anecdotal evidence or antiquated investigational methods. The
findings were based on exposure and food-history information gathered
and analyzed by local, state, and Federal health partners, including
the CDC. These investigations used accepted investigational practices
at the time of the outbreak.
Although FSIS mentioned the length of such outbreaks in the
proposed determination, the Agency judges the severity of such
outbreaks on their overall public health impact, not the length of the
outbreaks. As noted in the proposed determination, despite making up a
very small percentage of the total domestic supply of chicken (88 FR
26252), NRTE breaded stuffed chicken products were associated with 14
Salmonella outbreaks between 1998 and 2021, resulting in 195 reported
illnesses and 41 hospitalizations (88 FR 26258-26259).

F. Salmonella Framework

Comment: A poultry establishment and a poultry products trade
association noted that FSIS has not finished its Salmonella Framework,
which contemplates reviewing FSIS' comprehensive approach to Salmonella
and that, considering this ongoing effort, it is premature to set
specific standards for NRTE breaded stuffed chicken at this time. The
commenters stated that pursuing a separate policy for NRTE breaded
stuffed chicken products risks creating inconsistencies or redundant
policies.
Response: The Agency is confident it can address the persistent
Salmonella outbreaks caused by NRTE breaded stuffed chicken products,
as stated in this notice, and also propose to address illness
associated from Salmonella in raw poultry generally in a future
proposed rule. This will not lead to inconsistent or redundant
policies. FSIS develops food safety requirements based on pathogens,
consumption data, and other food safety factors, which can vary
depending on the product.
For the reasons discussed in the proposed determination, FSIS
believes that NRTE breaded stuffed chicken products pose different
exposure risks to consumers than other types of raw poultry products
and are more likely to result in Salmonella outbreaks than other
products; therefore, FSIS has determined to hold NRTE breaded stuffed
chicken products to a more stringent Salmonella adulteration standard
than for other raw poultry products. FSIS is not delaying its efforts
concerning this product. Consistent with this final determination, as
the Agency develops the proposed Salmonella Framework,\46\ it will
consider measures that will be most effective in addressing the public
health risks associated with other raw poultry products.
---------------------------------------------------------------------------

\46\ FSIS, Proposed Regulatory Framework to Reduce Salmonella
Illnesses Attributable to Poultry, available https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/proposed.
---------------------------------------------------------------------------

G. Wait for Additional Information

Comment: Poultry products trade associations, a poultry products
establishment, and a society of meat industry professionals noted that
FSIS needs to gather more information about Salmonella in NRTE breaded
stuffed chicken products before finalizing this determination.
Specifically, they stated that FSIS needs to gather more data on the
frequency that products currently exceed the 1 CFU/g threshold, whether
enforcing the 1 CFU/g standard would be feasible, and what impact the
proposed determination would have on public health. The commenters
further stated that FSIS needs more insight into which serotypes are
most prevalent in these products, as well as better information
regarding infectious dose and host susceptibility. The commenters said
that FSIS should build a comprehensive microbiological baseline before
moving forward and use that information to conduct a risk assessment.
Response: FSIS has sufficient information to finalize this
determination. As discussed in the proposed determination (88 FR
26249), available data from outbreak investigations and consumer
behavior research show that NRTE breaded stuffed chicken products
contaminated with Salmonella pose a significant public health risk. As
noted in the proposal, these data show that common consumer preparation
practices associated with NRTE breaded stuffed chicken products may not
destroy organisms that may be present in the product and may also
contribute to cross contamination (88 FR 26264). The proposal also
described available data that show Salmonella has been associated with
severe and debilitating human illnesses and that the Salmonella
infectious dose is relatively low (88 FR 26264). Thus, because
Salmonella can survive ordinary handling and cooking practices for NRTE
breaded stuffed chicken products,

[[Page 35040]]

FSIS has determined that the appropriate response to protect public
health is to ensure that products contaminated with Salmonella at
levels more likely to cause human illness are excluded from commerce.
As explained in the proposed determination, assuming a minimum of 0.5
log (68%) Salmonella reduction likely achieved with even partial
cooking, considering a level of Salmonella at 1 CFU/g (assuming a
typical 70-88 gram chicken component portion size) to adulterate
product should significantly mitigate the risk of illness associated
with NRTE breaded stuffed chicken products (88 FR 26263). Additionally,
as discussed in the proposed determination, all Salmonella serotypes
have the potential to cause illness, and the disparity in serotypes may
be related to factors other than serotype-specific differences in human
virulence. Thus, given the unique public health risk associated with
NRTE breaded stuffed chicken products, FSIS has determined that any
Salmonella at levels of 1 CFU/g or higher is an adulterant in these
products. FSIS will continue to evaluate and, if necessary, refine its
policies and standards related to the oversight of NRTE breaded stuffed
chicken products as advances in science and technology related to
pathogen levels, serotypes, and infectious dose become available.
FSIS typically performs baseline studies to estimate the national
prevalence of bacteria of public health concern in situations where a
large number of establishments produce a product and uniform
verification sampling is performed. Here, a baseline study isn't
warranted for NRTE bread stuffed chicken products because there are
currently only six federally regulated establishments producing such
products. Due to the public health risk posed by the product type,
which is supported by recurring Salmonella illness outbreaks, the
Agency decided to move forward with the proposed determination.

H. Infectious Dose

Comment: Poultry products trade associations, a member of the
poultry products industry, and a meat industry research institute
asserted there were several deficiencies in the infectious dose data
FSIS relied on to support its proposed determination that NRTE breaded
stuffed chicken with 1 CFU/g Salmonella are adulterated. Specifically,
the commenters stated that FSIS relied on a single dose-response study
to support the 1 CFU/g proposed determination.\47\ Moreover, commenters
asserted that this study (hereinafter, ``Teunis 2010'') contained
insufficient and outdated data. The commenters, therefore, provided an
updated study by the same author for FSIS' consideration (hereinafter,
``Teunis 2022'').\48\ The commenters also suggested that Salmonella
serotypes used in Teunis 2010 were not representative of the serotypes
that caused NRTE breaded stuffed chicken product outbreaks or are found
in raw chicken.
---------------------------------------------------------------------------

\47\ Teunis P.F. et al., Dose-response modeling of Salmonella
using outbreak data, 144(2) Int. J. Food Microbial 243-9 (2010).
\48\ Peter F.M. Teunis, Dose response for Salmonella Typhimurium
and Enteritidis and other nontyphoid enteric salmonellae, 41
Epidemics (2022).
---------------------------------------------------------------------------

Response: The Agency considered Teunis 2022 along with the evidence
already cited on infectious dose in the proposed determination.
However, upon review, FSIS does not conclude that the updated dose-
response model in Teunis 2022, in consideration with the other evidence
previously cited, warrants a change in the proposed adulterant
threshold of 1 CFU/g of Salmonella in NRTE breaded stuffed chicken
products.
FSIS' 1 CFU/g determination was not based on a single study. FSIS
cited seven Salmonella outbreak papers in the proposed determination
where the infectious dose was found to be very low, i.e., 10 or fewer
Salmonella organisms. FSIS cited an additional nine papers noted in the
proposed determination that found an infectious dose between 11 and 420
organisms resulted in human illness. Finally, FSIS cited an additional
dose-response paper written by the World Health Organization (WHO) that
supports Salmonella illness can result, on average, from small
doses.\49\
---------------------------------------------------------------------------

\49\ World Health Organization, Risk assessment of Salmonella in
eggs and broiler chickens, March 25, 2002. Available at: https://www.who.int/publications/i/item/9291562293.
---------------------------------------------------------------------------

FSIS also did not rely on outdated data. Teunis 2022 specifically
states the outbreak data analyzed in the study ``. . . are the same
that were used in a previous analysis,'' i.e., Teunis 2010. In fact,
most of the data from the human challenge feeding trials \50\ used in
Teunis 2022 were published in 1951, about 70 years before the
publication of Teunis 2022. These data are scientifically debated. In
these trials, healthy volunteers were fed Salmonella, but none of the
strains used in Teunis 2022 had been isolated from a person with
salmonellosis.\51\ Some of the volunteers had been vaccinated for
Salmonella typhoid and paratyphoid. Blaser and Newman summarize the
issues as follows, ``the ability to generalize about what happens in
nature from the experimental data concerning the infective dose of
salmonellae is limited by several factors, including choice of strains,
repeated testing of the same subjects, failure to assess minimal
infective doses, and use of too few volunteers at the lower dosages.''
FSIS also disagrees with the commenters' assertion that a transposition
of an outbreak dose from 344 CFU to 3.44 CFU in Teunis 2010 was
``significant'' and, thus, evidence that FSIS' dose-response analysis
was based on an outdated model. Teunis 2022 specifically states that
``It was checked that correction of the dose changed the estimates of
Salmonella Enteritidis infectivity and pathogenicity only by a minute
amount, putting to rest concerns that quantitative risk assessments
might have been caused to use an incorrect model.'' \52\
---------------------------------------------------------------------------

\50\ McCullough, N.B., Wesley Eisele, C., 1951a. Experimental
human salmonellosis. I. Pathogenicity of strains of Salmonella
meleagridis and Salmonella anatum obtained from spray-dried whole
egg. J. Infect. Dis. 88, 278-289; McCullough, N.B.,
\51\ Blaser, M.J. and L.S. Newman, A Review of Human
Salmonellosis .1. Infective Dose. Reviews of Infectious Diseases,
1982. 4(6): p. 1096-1106.
\52\ Peter F.M. Teunis, Dose response for Salmonella Typhimurium
and Enteritidis and other nontyphoid enteric salmonellae, 41
Epidemics (2022).
---------------------------------------------------------------------------

The commenters also suggested that Salmonella serotypes used in
Teunis 2010 are not representative of the serotypes that caused NRTE
breaded stuffed chicken product outbreaks or are found in raw chicken.
However, as stated in the proposed determination, all known NRTE
breaded stuffed chicken product outbreaks have been Typhimurium,
Heidelberg, I 4,[5],12:i:-, and Enteritidis. Teunis 2010 and Teunis
2022 used 48 outbreaks to estimate the Salmonella dose-response for all
serotypes. Eighty-three percent of those outbreaks represent serotypes
that have been associated with NRTE breaded stuffed chicken product
outbreaks.
Lastly, as mentioned, the proposed determination cited an
additional dose-response model, which was developed by the WHO Food and
Agriculture Organization of the United Nations for risk assessments for
Salmonella in eggs and broiler chickens.\53\ Also using outbreaks, the
model estimated a 13 percent chance of becoming ill if ingesting 100
organisms. Even at the level of 1 organism ingested, there was still a
non-zero chance of illness (0.25%).
---------------------------------------------------------------------------

\53\ World Health Organization, Risk assessment of Salmonella in
eggs and broiler chickens, March 25, 2002. Available at: https://www.who.int/publications/i/item/9291562293.

---------------------------------------------------------------------------

[[Page 35041]]

Comment: Industry members, poultry products trade associations, and
a meat industry research institute said FSIS should establish a new
adulteration threshold equal to or higher than 10 CFU/g for NRTE
breaded stuffed chicken products. These commenters noted that the FERN
Survey and FSIS data on NRTE breaded stuffed chicken products show that
more than a quarter of all Salmonella positives were Salmonella
Kentucky, which they claimed would not result in illness at 1 CFU/
g.\54\ A poultry products trade association also suggested FSIS based
its adulteration threshold on the infectious dose for Salmonella
Enteritidis, given it was the serotype most commonly associated with
NRTE breaded stuffed chicken outbreaks documented in the proposed
determination. Specifically, the trade association stated that FSIS
should base its threshold on the median dose of Salmonella Enteritidis
that is predicted to have a 50% probability of causing illness, which
was reported as 3,360 CFU. The comment asserted that assuming that the
average chicken component of an NRTE breaded stuffed chicken product is
70-88 grams as noted in the proposal, this provides a range of 38-48
CFU/g in NRTE breaded stuffed chicken products.
---------------------------------------------------------------------------

\54\ Laboratory Quality Assurance, Response, and Coordination
Staff (LQARCS) Office of Public Health Science Food Safety and
Inspection Service U.S. Department of Agriculture. Survey of Not
Ready-to-Eat Breaded and Stuffed Chicken Products for Salmonella.
June 2023.
---------------------------------------------------------------------------

Response: FSIS is finalizing the 1 CFU/g threshold as described in
the proposed determination because outbreaks associated with products
have continued to occur regularly despite updated labeling
instructions, outreach, and other industry and Agency efforts to make
the products safer. FSIS is not establishing a higher adulteration
threshold of 10 CFU/g or greater based on the dose at which 50% of
individuals exposed to 3,360 CFU of Salmonella Enteritidis are
predicted to become ill. Use of such a metric where half (50%) of
individuals exposed could become ill is not acceptable for a public
health regulatory program aimed at reducing the risk posed by NRTE
breaded stuffed chicken products, which are habitually undercooked by
consumers. Salmonella Enteritidis is not the only serotype of concern
in NRTE breaded stuffed chicken product, nor it is representative of
the infectious dose of all Salmonella serotypes. For example, Teunis
2022 states Infantis is predicted to have an InfD50 of 0.7
CFU and InfD01 0.01 CFU. Infantis is also predicted to have
an IllD50 of 1 CFU and an IllD01 of 0.07 CFU. All
four measures of infection and illness would be below the proposed 1
CFU/g adulteration threshold. Using the IllD01, Teunis 2022
supports the limit of 1 CFU/g for Enteritidis, Typhimurium, and
Infantis.
FSIS is not only concerned about Salmonella Enteritidis and
Infantis, but numerous serotypes that have been shown to be in NRTE
breaded stuffed chicken product. As discussed below, FSIS determined
numerous serotypes were of concern based on three data sources: (1)
verification sampling of raw comminuted chicken (a major component of
NRTE breaded stuffed chicken), (2) outbreak associated investigated
sampling of NRTE breaded stuffed chicken products, and (3) the recent
FERN survey of NRTE breaded stuffed chicken at retail.
First, using FSIS raw poultry sampling verification datasets for
comminuted chicken from 2015 to CYQ3 2021,\55\ FSIS serotyped 2,921
Salmonella positives and 58 unique serotypes. FSIS found the following
five most frequent serotypes in the following rank order from most to
least: Infantis, Enteritidis, Kentucky, Typhimurium, and
Schwarzengrund. Since NRTE breaded stuffed chicken products can be made
by grinding intact chicken, with trim and chicken skin, these
comminuted verification data suggest these serotypes are found in NRTE
breaded stuffed chicken products. The second data source was a 2015,
FSIS investigative sampling of NRTE breaded stuffed chicken comminuted
source components, finished products, and the processing environment
from two NRTE establishments associated with an outbreak.\56\ Among the
1,433 samples, 518 were positive for Salmonella, a 36% positive rate.
FSIS found the following serotypes in the following rank order from
most to least: Kentucky, Typhimurium, Infantis, Enteritidis,
Heidelberg, Schwarzengrund, I 4,[5],12:i:-, Montevideo, Mbandaka, and
Muenchen indicating virulent Salmonella serotypes can be directly found
in NRTE breaded stuffed chicken products. Lastly, in the FERN Survey,
NRTE breaded stuffed chicken products were purchased at retail from
July 1, 2022, to September 30, 2022. In total, 58 of the 487 samples,
12%, were positive for Salmonella. Fifty-three were serotyped finding
Infantis, Enteritidis, Kentucky, and Typhimurium, in that order of
frequency.
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\55\ https://www.fsis.usda.gov/news-events/publications/raw-poultry-sampling.
\56\ https://www.fsis.usda.gov/news-events/publications/raw-poultry-sampling.
---------------------------------------------------------------------------

As FSIS acknowledged in the proposed determination, not all
Salmonella serotypes (e.g., Salmonella Kentucky), are equally likely to
cause illness (88 FR 26262). However, all Salmonella serotypes,
including Salmonella Kentucky, have the ability to invade, replicate,
and survive in human host cells, resulting in potentially fatal
disease,\57\ and the disparity among serotypes may be related to
factors other than serotype-specific differences in human
virulence.\58\ With Salmonella, higher virulence is associated with
enhanced ability to survive and grow in the gut or to attach to and
invade human cells, which is driven by changes to several mechanisms,
including mobile genetic elements and resident genes as well as
variations in gene sequence and expression. In an August 2018 report,
the National Advisory Committee on Microbiological Criteria for Foods
(NACMCF) was unable to find evidence in the literature for any
determinant that correlated with high virulence in human foodborne
disease.\59\ NACMCF noted that a few Salmonella serotypes are
consistently associated with the greatest incidence of human disease.
However, this disparity among serotypes may be related to survival in
animal hosts or during food harvesting and processing rather than
serotype-specific differences in human virulence.
---------------------------------------------------------------------------

\57\ Shu-Kee Eng, Priyia Pusparajah, NurulSyakima 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,
\58\ FSIS decision to declare all Salmonella at certain levels
as an adulterant was also based on a review of the current state of
laboratory technology (88 FR 26262).
\59\ NACMCF (2019). Response to Questions Posed by the Food
Safety and Inspection Service Regarding Salmonella Control
Strategies in Poultry. Journal of Food Protection 82(4): 645-668.
---------------------------------------------------------------------------

Comment: A meat industry research institute and industry member
asserted that current support for the 1 CFU/g standard is based, in
part, on data that include products whose characteristics are not the
same as raw chicken. According to the commenters, FSIS cited studies/
data associated with cheese, chocolate, and dressings, which are all
RTE products of high fat content, and have known Salmonella protective
characteristics during digestion. They noted that high fat content
protects Salmonella against gastric acidity resulting in a reduction of
dose-response curve with a low infectious

[[Page 35042]]

dose.^{60 61 62 63} They argued that raw chicken, unlike these
other products, provides increased heat lethality, is expected to be
heated, and is lower in fat and not emulsified.
---------------------------------------------------------------------------

\60\ Naschimento, et.al., (2012) Inactivation of Salmonella
during cocoa roasting and chocolate conching. International Journal
of Food Microbiology 159 (3):225. 718-727.
\61\ Krapf, Tamara, and Corinne Gantenbein-Demarchi. ``Thermal
inactivation of Salmonella spp. during conching.'' LWT-Food Science
and Technology 43, no. 4 (2010): 720-723.
\62\ Podolak, Richard, Elena Enache, Warren Stone, Darryl G.
Black, and Philip H. Elliott. ``Sources and risk factors for
contamination, survival, persistence, and heat resistance of
Salmonella in low-moisture foods.'' Journal of food protection 73,
no. 10 (2010): 1919-1936.
\63\ D'aoust, J.Y. ``Salmonella and the chocolate industry. A
review.'' Journal of Food Protection 40, no. 10 (1977).
---------------------------------------------------------------------------

Response: FSIS does not agree with the assertion that the dose-
response models, including Teunis 2010, Teunis 2022, and the WHO Risk
assessment of Salmonella in eggs and broiler chickens, are not
applicable to chicken-specific outcomes. The commenters indicated that
many of the outbreaks used in the dose-response models reported low
doses for high-fat products (some reported in the range of 10\1\).
Looking at the outbreaks used in the Salmonella Enteritidis dose-
response model,\64\ there are many outbreaks that are presumably high-
fat but are also high dose. For example, (food vehicle and dose (CFU))
Hollandaise 4.48 x 10\4\, Macaroni salad 4.40 x 10\4\, Scallop/cream
1.00 x 10\6\, Yam/soup 1.94 x 10\6\, Bavarois (Bavarian ice-cream) 1.01
x 10\5\, Ice cream 3.84 x 10\6\, Tiramisu 1.29 x 10\8\, Cake 6.06 x
10\5\, Mayonnaise 5.57 x 10\4\. These outbreak doses range from about
10,000 to 100,000,000 organisms. Further, the commenter suggested that
the chicken matrix is low-fat and the only ingredient of concern. NRTE
breaded stuffed chicken products can be made from comminuted (ground)
chicken where high-fat chicken skin may be combined and comminuted with
skinless, boneless chicken. Additionally, NRTE breaded stuffed chicken
products include high-fat ingredients, such as cheese, cream, butter,
and ham, that could act to encourage pathogen survival.
---------------------------------------------------------------------------

\64\ Peter F.M. Teunis, Dose response for Salmonella Typhimurium
and Enteritidis and other nontyphoid enteric salmonellae, 41
Epidemics (2022).
---------------------------------------------------------------------------

FSIS agrees that very few of the outbreaks used in any of the dose-
response models mentioned in the public comments or the proposed
determination are specifically associated with an outbreak where the
contaminated ingredient was determined to be chicken. However, there
are several outbreaks used in the dose-response models that are based
on animal products. These include beef, chicken, egg, prawn, scallop,
and octopus. The commenters did not provide an explanation for how the
lack of chicken outbreaks would impact the dose-response except to
imply it would not be representative. However, dose-response models
describe pathogens and are rarely, if ever, specific to the
transmission pathway.

I. Virulence

Comment: A poultry industry commenter stated that FSIS needs to
gather more information on Salmonella virulence.
Response: As discussed in the proposed determination (88 FR 26262),
the basis for Salmonella virulence is not fully understood. Many
virulence factors have been identified that contribute to Salmonella
pathogenicity. The interactions of these factors and the resulting
strain virulence and pathogenicity has not been completely elucidated,
but single genes and pathogenicity islands have been identified as key
virulence traits. However, there is currently no agreed-upon definition
of virulence genes presence/absence profile that can reliably predict
severity of disease.\65\ FSIS, as discussed in the proposed
determination (88 FR 26262), is working to better understand Salmonella
characteristics, including virulence, and actively engages in and
encourages research in this area. As science and laboratory
technologies advance, FSIS will continue to use the most innovative and
sensitive methods available to protect public health.
---------------------------------------------------------------------------

\65\ NACMCF (2022). Response to questions Posed by FSIS:
Enhancing Salmonella Control in Poultry Products. Available at:
https://www.fsis.usda.gov/sites/default/files/media_file/documents/NACMCF_Salmonella-Poultry_Response_for_Committee_Review.pdf.
---------------------------------------------------------------------------

J. Consumer Behavior

Comment: Poultry products trade associations and a meat industry
research institute argued that consumers prepare raw chicken in a
manner that destroys Salmonella and, thus, Salmonella cannot be
considered an adulterant in products that include raw poultry
components. One poultry products trade association also specifically
asserted that FSIS cannot take the action discussed in the proposed
determination because it has not proved that consumers must cook NRTE
breaded stuffed chicken products to a temperature higher than other raw
poultry products in order to effectively kill Salmonella. A poultry
products trade association also asserted that the 2020 consumer study
\66\ and the 2022 CDC Appliance Report \67\ cited in the proposed
determination do not prove that consumers mishandle or use the
incorrect appliances to prepare NRTE breaded stuffed chicken products.
The commenter also noted that FSIS' analysis of consumer behavior
pertaining to food thermometer use relied on an outdated paper
explicitly focused on microwavable products from 1998-2006.\68\
---------------------------------------------------------------------------

\66\ S.C. Cates, et al., Food Safety Consumer Research Project:
Meal Preparation Experiment on Raw Stuffed Chicken Breasts, RTI
Project No. 0215472, ES-1-2 (Sept. 23, 2020).
\67\ Marshall, K.E., Canning, M., Ablan, M., Crawford T.N.,
Robyn, M. Appliances Used by Consumers to Prepare Frozen Stuffed
Chicken Products-United States, May-July 2022. Morb Mortal Wkly Rep
Dec 2,2022; 71(48);1511-1516. Available at: http://dx.doi.org/10.15585/ mmwr.mm7148a2.
\68\ Smith, K.E., Medus, C., Meyer, S.D., Boxrud, J.D., Leano,
F., Hedburg, C., Elfering, K., Braymen, C., Bender, J.B., Danila,
R.N. 2008. Outbreaks of Salmonellosis in Minnesota (1998 through
2006) Associated with Frozen, Microwaveable, Breaded Stuffed Chicken
Products. Journal of Food Protection. 71(10): 2153-2160.
---------------------------------------------------------------------------

Response: FSIS disagrees. As FSIS noted in the proposed
determination (88 FR 26252), there are special considerations to take
into account with these particular products that are relevant to
consumer cooking practices. For one, unlike most raw poultry products,
NRTE breaded stuffed chicken products often appear fully cooked and,
thus, some consumers may only reheat the product for aesthetic or
palatability purposes rather than subject it to cooking sufficient to
kill pathogenic bacteria. Second, consumers typically cook NRTE breaded
stuffed chicken from a frozen state, which increases the risk that the
products will not reach an internal temperature needed to destroy
Salmonella organisms that may be in the product. Third, NRTE breaded
stuffed chicken products have a thicker diameter and a different
composition than most other raw chicken products that are not stuffed,
including other par-fried breaded products, which can make effective
cooking of NRTE breaded stuffed chicken more challenging. In addition,
it may be difficult for a consumer to determine an accurate internal
temperature of these products because they contain multiple
ingredients, such as cheese and vegetables, that may cook at different
rates. FSIS has recommended in the past that consumers check the
temperature at multiple locations throughout the product using a food
thermometer, but this is not always practical or accurate.
As discussed in the proposed determination (88 FR 26252-26259),

[[Page 35043]]

outbreak investigations indicate that, despite industry and Agency
efforts, consumers' cooking practices continue to be insufficient to
destroy Salmonella in NRTE breaded stuffed chicken products and, as
such, they continue to have a disparate impact on public health.
Despite industry updates to labeling and Agency outreach on the safe
preparation of NRTE breaded stuffed chicken products, outbreak
investigations consistently indicate that case patients erroneously
believed these products were precooked, did not ordinarily use food
thermometers to check the internal temperature of the product, and used
a microwave or other unsuitable appliance to cook the products.
Moreover, many case patients became ill even when they used an oven to
prepare the product.
Further, FSIS disagrees with commenters' assertions that the
consumer research cited in the proposed determination was flawed or did
not indicate that a significant percentage of consumers customarily
mishandle NRTE breaded stuffed chicken products despite reading the
manufacturer's labeling and instructions. As commenters noted, the
proposed determination cited a 2008 report published in the Journal of
Food Protection. FSIS appropriately cited this report to describe four
separate salmonellosis outbreaks associated with NRTE breaded stuffed
chicken that occurred between 1998-2006, related investigative
findings, and the subsequent actions taken in response.\69\ The report
indicated that most consumers sickened in a 1998 outbreak reported
using a microwave to prepare the product, and no consumers reported
using a food thermometer. In response, the company responsible for the
outbreak updated the preparation instructions on its product labeling.
Then, in 2005, the report indicated that another outbreak occurred.
Again, the manufacturer responsible for the outbreak updated its
labeling instructions. FSIS also issued a public health alert to remind
consumers that frozen meat and poultry products must be fully cooked
before they are consumed. According to the report, following these
additional communications with consumers and labeling changes by the
manufacturers, two additional outbreaks occurred in the 2005-2006
timeframe. Again, most of the case patients used a microwave oven to
cook the products and none of the case patients took the internal
temperature of the product after cooking it. FSIS, therefore, issued
another public health alert, emphasizing that consumers must cook NRTE
breaded stuffed chicken products to 165 [deg]F. FSIS sent a letter to
an establishment involved in one of the outbreaks recommending they
enhance and validate the cooking instructions to ensure that they
address the intended use by the consumer.\70\ FSIS then posted the
letter online as guidance to all industry and requested that all such
establishments update their labeling to include a statement such as
``Uncooked: For Safety, Must be Cooked to an Internal Temperature of
165 degrees F as Measured by Use of a Thermometer.'' As discussed in
the proposed determination, despite these efforts, consumers continued
to prepare NRTE breaded stuffed chicken products in a manner that did
not adequately destroy Salmonella, resulting in several more outbreaks
and subsequent unsuccessful efforts to update labeling instructions and
educate the public on how to properly cook such products (88 FR 26252-
26259).
---------------------------------------------------------------------------

\69\ Smith, K.E., Medus, C., Meyer, S.D., Boxrud, J.D., Leano,
F., Hedburg, C., Elfering, K., Braymen, C., Bender, J.B., Danila,
R.N. 2008. Outbreaks of Salmonellosis in Minnesota (1998 through
2006) Associated with Frozen, Microwaveable, Breaded Stuffed Chicken
Products. Journal of Food Protection. 71(10): 2153-2160.
\70\ Letter to industry about the safe handling labeling of
uncooked, breaded, boneless poultry products (March 2006) at:
https://www.fsis.usda.gov/guidelines/2006-0007.
---------------------------------------------------------------------------

In addition to analyzing outbreak data, FSIS discussed the results
of two consumer behavior studies that helped inform its determination
that a significant percentage of consumers do not customarily cook NRTE
breaded stuffed chicken products in a manner that adequately destroys
Salmonella. In the 2020 Meal Preparation Experiment cited in the
proposed determination (88 FR 26257),\71\ FSIS contracted with RTI
International and North Carolina State University to conduct five
separate iterations of a meal preparation study to evaluate consumer
food handling behaviors in a test kitchen. The third iteration of the
study specifically examined participants' meal preparation related to
NRTE breaded stuffed chicken products. Half of the participants were
assigned to a control group, whereas the other half was assigned to a
treatment group. Amongst other things, the study found that consumers
may confuse frozen NRTE breaded stuffed chicken products with RTE
products. Specifically, the study concluded that even though 99% of all
participants read the manufacturer's instructions for NRTE breaded
stuffed chicken products, nearly a quarter reported they were not sure
if the products were raw or fully cooked, twenty-two percent reported
they were unaware that the product was raw, and eleven percent of the
participants incorrectly believed the product was fully cooked. The
study also found that a significant number of participants did not use
food thermometers to check that the NRTE breaded stuffed chicken
product reached a safe internal temperature of 165 [deg]F, with some
using other methods to determine doneness such as time, visual cues,
and touch. Thirty-eight percent of participants also self-reported not
using their food thermometer at home to check that NRTE breaded stuffed
chicken products were properly cooked. Moreover, the study observed
that a significant number of participants did not adequately wash their
hands during meat preparation. The study concluded that these issues
were likely attributable to participants preparing a NRTE breaded
stuffed chicken product rather than raw, unfrozen poultry that is not
breaded and stuffed. This indicates that the appearance of NRTE breaded
stuffed chicken products and the fact that they are typically cooked
from a frozen state may contribute to Salmonella cross-contamination in
the home.
---------------------------------------------------------------------------

\71\ Final Report: Food Safety Consumer Research Project: Meal
Preparation Experiment on Raw Stuffed Chicken Breasts (September 23,
2020) at: https://www.fsis.usda.gov/sites/default/files/media_file/2021-04/fscrp-yr3-nrte-final-report.pdf.
---------------------------------------------------------------------------

The proposed determination also discussed the results of a 2022
survey that collected information from thousands of participants from
May 31-July 6, 2022, to determine the demographic characteristics of
persons who prepare NRTE breaded stuffed chicken products and the
appliances they use to prepare them.\72\ Even though NRTE breaded
stuffed chicken product labels typically instruct consumers to cook the
product in an oven and specifically warns against the use of a
microwave, 54 percent of participants reported that they prepared these
products using appliances other than, or in addition to, ovens.\73\
Specifically, 30 percent reported preparing the products using air
fryers, 29 percent reported using microwaves, approximately 14 percent
reported using toaster ovens, and approximately 4 percent reported
using another appliance. Economic and other factors might affect
certain groups'

[[Page 35044]]

access to recommended cooking appliances and, thereby, the customary
manner in which these groups cook NRTE breaded stuffed chicken
products.
---------------------------------------------------------------------------

\72\ Marshall, K.E., Canning, M., Ablan, M., Crawford T.N.,
Robyn, M. Appliances Used by Consumers to Prepare Frozen Stuffed
Chicken Products-United States, May-July 2022. Morb Mortal Wkly Rep
Dec 2,2022; 71(48);1511-1516. Available at: https://www.cdc.gov/mmwr/volumes/71/wr/mm7148a2.htm.
\73\ Participants in the study were allowed to choose more than
one cooking option.
---------------------------------------------------------------------------

FSIS also disagrees that, in order to finalize the proposed
determination, it must show that consumers must cook NRTE breaded
stuffed chicken products to a temperature higher than other raw poultry
products in order to effectively kill Salmonella. As noted in the
proposed determination, the status of NRTE breaded stuffed chicken
products contaminated with Salmonella must depend on whether there is
adequate assurance that consumer handling of the product will result in
a product that does not contain Salmonella at levels sufficient to
cause human illness when consumed (64 FR 2803). The evidence cited in
the proposed determination, including the consumer research cited
above, shows consumers routinely do not fully cook NRTE breaded stuffed
chicken nor do they routinely use a food thermometer to test the
internal temperature of the product and, thus, has concluded that the
appropriate response to protect public health is to ensure that
products contaminated with Salmonella at levels sufficient to cause
human illness (1 CFU/g) are excluded from commerce.

K. Laboratory Methods

Comment: Poultry products trade associations, a meat products
research institute, a member of the poultry products industry, a trade
group representing the frozen foods industry, and a society of meat
industry professionals raised some issues regarding the laboratory
methods FSIS intends to implement. Generally, they stated that
Salmonella enumeration testing technology is still under development,
that current methods are limited, and that FSIS needs to ensure that
its methods are validated prior to implementation of this
determination. Specifically, they noted that available Salmonella
enumeration methods are not currently validated for NRTE breaded
stuffed chicken products or at a detection level of 1 CFU/g. A poultry
products trade association and an industry member also asserted that
there is a margin of variability inherent in the available laboratory
methods and asked for clarity on how FSIS would account for this. An
industry member also asked FSIS to use polymerase chain reaction (PCR)-
based limit of detection testing, until quantification methods are
improved and validated.
Response: FSIS laboratories performed a thorough verification of
validated methods by independent organizations. FSIS' current qPCR
method is validated for 1 CFU/g in NRTE breaded stuffed chicken.\74\
The Most Probable Number (MPN) method is another enumeration technique
that FSIS has adopted.\75\ FSIS intends to routinely evaluate new
methods of Salmonella quantification, as they become available, that
provide both accuracy and fitness for a high-throughput laboratory
environment.
---------------------------------------------------------------------------

\74\ BioMerieux GENE-UP QUANT Salmonella, AOAC Performance
Tested Methods\SM\ Certification Number 082104 is the current
validation.
\75\ See https://www.fsis.usda.gov/news-events/publications/microbiology-laboratory-guidebook.
---------------------------------------------------------------------------

Comment: To expedite test results, a poultry products trade
association requested that the Agency consider conducting the
quantitative assay concurrently with the assay being conducted to
screen the sample for the general presence of Salmonella, not based on
that assay. The commenters also asked for clarity on if quantitative
and general detection results will be obtained from the same
homogenized sample to avoid conflicting results that could arise if
using different analytical sample portions due to factors such as the
nonhomogeneous distribution of Salmonella.
Response: FSIS intends to use the same homogenized sample for the
quantitative and detection screen protocols. Enumeration results will
be reported on the same day. For samples that are potential positives,
an additional 3 days may be necessary for a confirmed positive or
negative result. These timeframes and methods may change as FSIS
incorporates new laboratory technologies into its sampling and
verification testing.
Comment: A poultry products trade group stated that Salmonella
levels in finished product are typically less than 1 CFU/g but that the
levels in samples may grow beyond the 1 CFU/g threshold during
transport of the sample to Federal laboratories. The commenters asked
the Agency to account for this phenomenon in its final determination,
given even a slight difference in results may have a negative impact on
industry.
Response: Current FSIS procedures ensure the temperature of the
Salmonella samples to be 15 [deg]C or less upon receipt at the field
service laboratories.\76\ The laboratories will discard samples that
arrive at a temperature above 15 [deg]C.\77\ This upper temperature
limit is intended to prevent the outgrowth of competitors that could
affect pathogen recovery in the lab. These limits also ensure that
growth during shipment does not occur. While 15 [deg]C is the upper
allowable limit, samples received at the laboratory typically do not
approach that temperature. USDA studies have shown no significant
difference in the levels of Salmonella in ground beef samples if kept
at refrigerator temperatures for 24-48 hours (Narang et al, 2005).
---------------------------------------------------------------------------

\76\ USDA FSIS MLG 1.01 FSIS Laboratory System Introduction,
Method Performance Expectations, and Sample Handling for
Microbiology, available at https://www.fsis.usda.gov/sites/default/files/media_file/2022-03/MLG_1.01.pdf.
\77\ FSIS Directive 10250.1, Salmonella and Campylobacter
Verification Program for Raw Meat and Poultry Products.
---------------------------------------------------------------------------

Comment: A commercial laboratory suggested that FSIS consider using
third-party laboratories that are part of the Accredited Laboratory
Program (ALP) when including laboratories that will be assisting the
Agency. Further, a member of the poultry products industry stated that
FSIS should utilize industry analytical data from ALP on the levels of
Salmonella to conduct their verification, to assist small and very
small processors.
Response: Currently, FSIS labs analyze all samples that FSIS
inspectors collect to verify that product is wholesome and not
adulterated. Also, FSIS labs currently have the capacity to conduct
verification sampling and testing of NRTE breaded stuffed chicken
products. Thus, at this time, FSIS intends to collect all samples and
use its own labs for verification testing conducted under this final
determination.

L. Verification Sampling

Comment: Poultry products trade associations, industry members, and
a meat industry research institute asked FSIS to consider sampling
earlier in the NRTE breaded stuffed chicken product production process
to give establishments more flexibility to divert failed product for
other uses. Specifically, commenters asked FSIS to consider conducting
sampling on the raw incoming chicken components used to produce NRTE
breaded stuffed chicken, prior to those materials being comminuted and
combined. They indicated that, if FSIS finalized the sampling location
as discussed in the proposed determination, establishments would have
less flexibility to divert product exceeding the 1 CFU/g adulteration
threshold, given the chicken components, once processed and prepared
for breading and stuffing, have a short shelf life and a unique
formulation that can only be utilized to produce NRTE breaded stuffed
chicken products. Thus, the commenters asserted that sampling at the
location discussed in the proposed determination would lead to
substantial food waste and lost product costs.

[[Page 35045]]

Response: In the proposed determination (88 FR 26249), FSIS
proposed to collect verification samples after the establishment has
completed all processes needed to prepare the chicken component to be
stuffed and breaded to produce final NRTE breaded stuffed chicken
products. However, FSIS agrees with commenters that sampling earlier in
the production process may provide some establishments with additional
flexibility to divert sampled source products for other uses, thereby
reducing food waste, lost product costs, and establishment operations
changes due to the collection event. As such, FSIS will collect
verification samples from incoming raw poultry source materials at the
establishment producing the NRTE breaded stuffed chicken prior to
breading and stuffing at an appropriate point in the establishment's
process. In assessing the suitability of the sampling location at any
individual establishment, FSIS will take into account the
establishments' production process and the Agency's ability to collect
the sample safely and effectively. Any Salmonella detected in NRTE
breaded stuffed chicken source materials will be enumerated and source
materials that exceed 1 CFU/g of Salmonella must be diverted for other
uses.
Comment: A poultry products trade association asked for clarity on
whether the Salmonella adulteration threshold for NRTE breaded stuffed
chicken products applies only to the chicken components tested by FSIS
or to the finished product itself. The commenter also asked for clarity
on whether establishments may complete the production of NRTE breaded
stuffed chicken products while awaiting sampling results, so long as
such products remain under establishment control and are not released
into commerce. Further, the commenter asked FSIS to provide that
establishments may divert raw chicken source material confirmed
positive for Salmonella at 1 CFU/g for uses other than the production
of NRTE breaded stuffed chicken products.
Response: Under this determination, all finished NRTE breaded
stuffed chicken products that are contaminated with Salmonella at 1
CFU/g or greater are adulterated within the meaning of 21 U.S.C.
453(g)(1) and 21 U.S.C. 453(g)(3). This adulteration standard applies
to finished NRTE breaded stuffed chicken products, not the raw incoming
chicken components tested by FSIS. Tested chicken components and those
components represented by the sampled lot before incorporation into
NRTE-BSC products would not be considered adulterated for certain other
uses if confirmed positive for 1 CFU/g or greater of Salmonella. Thus,
establishments may divert such raw material components to another
appropriate application (e.g., breaded nugget or fully cooked
products). Chicken components subject to sampling and verification
testing and confirmed positive for 1 CFU/g or greater of Salmonella
would be ineligible for use in NRTE breaded stuffed chicken products
under 9 CFR 417.2(c)(3).
In the proposed determination (88 FR 26266), FSIS stated that,
pending test results, establishments should not incorporate sampled
lots into finished NRTE breaded stuffed chicken products. However, in
response to public comments, FSIS is clarifying that this statement was
only meant to apply to sampled lots incorporated into NRTE breaded
stuffed chicken products released into commerce. Establishments that
produce NRTE breaded stuffed chicken may, at their discretion,
incorporate sampled lots into finished NRTE breaded stuffed chicken
products, so long as those finished products remain under establishment
control awaiting acceptable test results.
Comment: A poultry products trade association and a meat industry
research institute noted that, upon entering commerce, NRTE breaded
stuffed chicken may be subject to additional testing by state or local
health authorities, customers, consumer advocacy organizations, or even
FSIS and other Federal partners. The commenters asked for clarity on
how FSIS would interpret such downstream testing and what public health
actions it would take if such testing showed that finished NRTE breaded
stuffed chicken products in commerce contain Salmonella at 1 CFU/g or
greater.
Response: Under this determination, all finished NRTE breaded
stuffed chicken products that are contaminated with Salmonella at 1
CFU/g or greater are adulterated within the meaning of 21 U.S.C.
453(g)(1) and 21 U.S.C. 453(g)(3). If FSIS receives test results from a
third party (e.g., a state health department, advocacy organization, or
consumer), the Agency will address those results in accordance with
FSIS Directive 10,000.1, Policy on Use of Results for Non-FSIS
Laboratories. Assuming the test results are deemed acceptable, FSIS may
use the results to inform Agency action, such as detaining the product
or initiating a recall.
Comment: To minimize product storage costs, a poultry products
trade association asserted that FSIS should provide establishments with
enumeration results as soon as they are available, without waiting for
serotype or WGS information.
Response: FSIS will transmit test results to establishments as soon
as possible and will not withhold such results while awaiting other
information. FSIS intends to use the LIMS-Direct system and Biological
Information Transfer Email System (BITES) messages to alert
establishments and Office of Field Operations personnel prior to the
confirmed positive and WGS or serotyping steps of the analysis.
Comment: Poultry products trade associations, a poultry products
industry member, and a meat industry research institute requested
clarity on how production lots would be defined for purposes of FSIS'
verification and sampling program.
Response: Establishments are responsible for defining a production
lot. Establishments should ensure that there is a scientifically
supportable basis for their lotting practices to ensure microbiological
independence. To create independence between production lots,
establishments need to consider the way in which the hazard is likely
to be introduced to the process, such as from the addition of chicken
skin, and during handling and processing of chicken parts, and grinding
of chicken trim that may be used in the production of NRTE breaded
stuffed chicken products. When applicable and available, FSIS and
establishment microbial sampling, as well as the lotting of received
source materials must also be considered and support the establishments
product lot definition. A production lot can be defined by the
establishment in several ways. FSIS does not consider ``clean-up to
clean-up'' alone as a supportable basis for distinguishing one portion
of raw chicken production from another portion of production.
Establishments may decide to use a robust, statistically based sampling
program, one or more processing interventions that have been validated
to limit or control Salmonella, or other scientifically supportable
process to define the lot.\78\
---------------------------------------------------------------------------

\78\ For additional information on lotting see the FSIS
Guideline for Holding and Controlling Meat, Poultry, and Egg
Products Pending FSIS Test Results. Available at: https://www.fsis.usda.gov/policy/fsis-guidelines.
---------------------------------------------------------------------------

M. Implementation Date

Comment: A meat industry research institute stated that the Agency
must allow a reasonable timeframe to implement the final determination.
The commenter noted that establishments

[[Page 35046]]

will need to adjust and put processes in place to hold product during
testing and divert positive product. Moreover, according to the
commenter, establishments may need to weigh the costs of these
processes to determine whether continued production of these types of
products is viable. According to the commenter, an effective date one
year from the publication of a final determination would be reasonable.
Response: FSIS agrees that industry will need a reasonable amount
of time to adjust to this determination. As such, this final
determination will not be effective until 12 months after publication
of this final determination. Also, FSIS inspection verification
sampling will be implemented 12 months after publication of this final
determination.

N. Cost Benefit Analysis

Comment: Poultry products trade associations, a meat industry
research institute, and a member of the poultry products industry,
asserted that storage costs under the proposal would be greater than
anticipated in the proposed determination; however, they did not
provide any costs estimates to support their assertion. Specifically,
the commenters argued that some establishments do not have enough
storage capacity to hold products awaiting test results and would,
thus, have to purchase off-site storage. Further, commenters stated
that the proposed determination did not adequately account for
transportation or labor costs, associated with moving product to and
from off-site storage facilities. Commenters also asserted that FSIS
test results are likely to take longer than estimated in the proposed
determination's CBA and that test and hold requirements will reduce
shelf life for these products.
Response: FSIS disagrees that the anticipated costs for cold
storage will be greater than estimated in the proposed determination.
FSIS requires that establishments maintain control of sampled product
pending FSIS verification testing results so that product does not
enter commerce, while allowing establishments the flexibility of
determining where to hold product as well as deciding whether to divert
product into other uses. Additionally, as mentioned above,
establishments will be able to complete the production process using
sampled product, provided they maintain control of any finished
products and do not release them into commerce, pending acceptable test
results. This will likely reduce an establishment's need for cold
storage capacity. To be conservative, FSIS' preliminary cost benefit
analysis (CBA; 88 FR 26267) accounted for cold storage costs assuming
every lot would be sampled and held. The final CBA assumes FSIS would
sample up to 5 lots per establishment per month. The preliminary CBA
also assumed that sampling would take place right before the chicken
component was stuffed and formed into a NRTE breaded stuffed chicken
product. However, as discussed above, FSIS has updated the sampling
location to give establishments greater flexibility to divert products
for other uses and otherwise reduce operating costs. Given FSIS'
assumed lower sampling frequency, greater flexibility in sampling
location and establishments' ability to divert components or products,
FSIS does not expect establishments to have challenges holding or
controlling FSIS sampled product or have additional labor or
transportation issues. Moreover, FSIS does not believe the quality or
shelf-life of NRTE breaded stuffed chicken products would be impacted
during cold storage while industry awaits FSIS sampling results because
these products are frozen. In response to comments, FSIS updated the
final CBA by conservatively using the higher estimate for frozen cold
storage costs instead of the refrigerated cold storage costs used in
the preliminary CBA.
FSIS also does not foresee an issue with cold storage capacity.
Cold storage construction in the United States has increased since 2020
to meet higher refrigeration demands. According to the U.S. Bureau of
Labor Statistics, the number of private refrigerated warehouse
facilities increased by 7.5 percent from 2020 to 2021 and an additional
6.8 percent from 2021 to 2022.\79\ This increase compares to an average
annual growth rate of 2.5 percent per year from 2013 to 2020.\80\ With
the increase in the number of cold storage establishments, FSIS does
not expect the cold storage availability to impact the establishments'
ability to store lots of product when FSIS collects a sample. For a
conservative estimate, the Agency assumed that all costs of storing
product for the sampled lots are due to this final determination;
however, establishments may already store the chicken components for
NRTE breaded stuffed chicken products in their facilities or in an off-
site location for a certain amount of time.
---------------------------------------------------------------------------

\79\ Bureau of Labor of Statistics. Number of Establishments in
Private NAICS 49312 Refrigerated warehousing and storage for All
establishment sizes in U.S. TOTAL, NSA. Annual totals from 2013 to
2022. Accessed on September 27, 2023.
\80\ Bureau of Labor of Statistics. Number of Establishments in
Private NAICS 49312 Refrigerated warehousing and storage for All
establishment sizes in U.S. TOTAL, NSA. Annual totals from 2013 to
2022. Accessed on September 27, 2023.
---------------------------------------------------------------------------

FSIS is confident in its estimated sampling timeframes. In the
final determination, FSIS estimates all product sampled and tested by
FSIS will be held for 2 days pending screening and enumeration results.
At the 1 CFU/g limit, FSIS estimates that about 97 percent of product
could be released after two days. Receiving the enumeration results
within two days will help industry make more timely decisions about
their product and save on cold storage and lost product costs.
Comment: A poultry products trade association and meat industry
research institute stated that there are issues with FSIS' analysis of
costs in the proposed determination associated with diverted or
destroyed product. Specifically, these commenters noted that there is
not a market for raw chicken components that are already formulated for
use in NRTE breaded stuffed chicken products and, thus, establishments
producing raw poultry products cannot readily divert such products for
other uses.
Response: FSIS proposed an inspection verification sampling program
for Salmonella in NRTE breaded stuffed chicken products in which the
Agency would collect a sample from the chicken component of NRTE
breaded stuffed chicken product prior to breading and stuffing, but
after the establishment had completed all the processes needed to
prepare the chicken to be stuffed and breaded. However, in the final
determination, and based on public comment, FSIS decided to modify the
verification sampling location by collecting verification samples on
the incoming chicken components. This change may provide establishments
with additional flexibility and allow them to divert chicken components
more readily.
Comment: A poultry products trade association and meat industry
research institute noted that many establishments would be hesitant to
divert Salmonella-positive product for other NRTE purposes. According
to the commenters, to avoid potential liability, many establishments
may cook the affected product or employ some other lethality step,
resulting in a lower value product. The commenters also asserted that
many establishments would need to incorporate sampled lots into
finished NRTE breaded stuffed chicken products to avoid spoilage.
Response: FSIS accounts for the lost value in the CBA by assuming
diverted chicken components would lose \2/3\ of their market value.
Alternatively, the establishment is not required to divert

[[Page 35047]]

product because FSIS collected a sample and thus, may choose to
continue to produce NRTE breaded stuffed chicken and hold the finished
product pending verification, which FSIS also included in its estimates
for cold storage costs. NRTE breaded stuffed chicken finished product
produced from chicken components that FSIS detects to contain
Salmonella at levels of 1 CFU/g or higher are considered adulterated;
however, establishments may be able to fully cook these finished
products to achieve lethality resulting in a ready-to-eat product.
Comment: Industry asked FSIS to clarify how it estimated lot sizes
in the proposed determination's CBA and noted that the lot sizes may be
larger than estimated in the preliminary CBA.
Response: The lot size estimates used in the preliminary CBA were
an assumption based on the Agency's data on annual production volumes
at these establishments. The preliminary CBA assumed establishments
producing at least 1 million pounds of NRTE breaded stuffed chicken
annually were high volume establishments with 10,000-pound lots. This
assumption was based on examples from the 2013 FSIS Compliance
Guideline: Controlling Meat and Poultry Products Pending FSIS Test
Results.\81\ The preliminary CBA assumed establishments producing less
than 1 million pounds of NRTE breaded stuffed chicken annually were
low-volume establishments with 1,000-pound lots. This assumption was
based on production data from FSIS' Public Health Information System.
FSIS requested comments on these assumptions but did not receive
specific comments on lot size for these products. However, in responses
to the comments that the lot sizes may be larger, the final CBA has
been updated to consider a day's production as a lot at both high and
low volume establishments. This is a conservative estimate because the
lot sizes may be smaller than a day's production. Establishments
ultimately define and support their lot sizes.
---------------------------------------------------------------------------

\81\ FSIS Compliance Guideline: Controlling Meat and Poultry
Products. Pending FSIS Test Results. 2013. https://www.fsis.usda.gov/sites/default/files/media_file/2021-09/FSIS-GD-2013-0003.pdf. Accessed on: November 9, 2023.
---------------------------------------------------------------------------

Comment: A meat industry research institute and a poultry products
industry member stated that FSIS' CBA should have accounted for
different employee types to estimate sampling or HACCP plan
reassessment labor costs. The same commenters stated that a food
safety, quality assurance, or a laboratory employee are more likely to
conduct sampling. They stated that establishments typically do not use
line personnel to conduct sampling and, thus, would need to hire
additional personnel to conduct tasks associated with sampling and
testing. Another commenter suggested that FSIS should better account
for the wages of an ``experienced production employee'' in estimating
the labor costs of HACCP plan reassessment.
Response: In response to comments, the final CBA has been updated
to include that sample collection is conducted by food scientists and
technologists. In addition, the final CBA has been updated to included
wage ranges for all the wage estimates to account for the variability
in wage rates within the professions. FSIS maintains the assumption
that establishments would use and train current employees to implement
any new or additional sampling in response to this final determination.
While the CBA conservatively assumed every establishment would begin or
increase sampling in response to this new policy, some establishments
already have robust sampling procedures in place and may not make any
changes to their sampling in response to the final determination, while
other establishments may choose not to conduct any sampling.
Additionally, the Agency did not receive any information on the number
of additional employees an establishment would hire in response to this
final determination.
Comment: Poultry product trade associations, a member of the
poultry products industry, and a meat industry research institute
stated that FSIS' CBA underestimated miscellaneous costs associated
with the proposed determination, such as testing by industry, employee
training, applying new Salmonella interventions, changing production
processes, and validating new production methods and cooking
instructions. These commenters also stated that the CBA underestimated
the market price of NRTE breaded stuffed chicken products and,
specifically, failed to adjust the price for inflation.
Response: FSIS disagrees that miscellaneous costs are
underestimated. FSIS included the cost of HACCP reassessment in the CBA
for all establishments producing NRTE breaded stuffed chicken products.
Sanitation procedures are a prerequisite to HACCP and according to 9
CFR 416.1, ``Each official establishment must be operated and
maintained in a manner sufficient to prevent the creation of insanitary
conditions and to ensure that product is not adulterated.'' \82\ Any
sanitation issues should be addressed as a condition for the
establishment's grant of inspection. Any costs associated with
sanitation will not be a result of the new policy.
---------------------------------------------------------------------------

\82\ National Archives. Code of Federal Regulations. Part 416.1
Sanitation Rules: General Rules. Accessed on October 11, 2023:
https://www.ecfr.gov/current/title-9/chapter-III/subchapter-E/part-416.
---------------------------------------------------------------------------

FSIS did not include the cost of validating cooking instructions in
the CBA because industry has already made the recommended changes after
the 2015-2016 outbreaks. Any expenses establishments incur to validate
cooking instructions or update labels are outside the scope of the
policy.
FSIS updated the final CBA to 2022 dollars and used the 2022
average price of chicken breast to represent the price of chicken
components for NRTE breaded stuffed chicken product. To be
conservative, FSIS used the retail price of boneless chicken breast,
which is the premium chicken component utilized in these products.
Comment: Poultry product trade associations, a member of the
poultry product industry, and a meat industry research institute noted
that sampling and testing alone does not change pathogen loads. Thus,
according to commenters, the CBA should assume that establishments will
bear the costs of updating their processes to control Salmonella.
Response: The final determination and FSIS inspection verification
of the adequacy of the HACCP system to control the Salmonella hazard,
will require industry to use effective methods to control Salmonella in
NRTE breaded stuffed chicken products regardless of whether FSIS
collects an inspection verification sample. FSIS included the cost for
establishment-led sampling and testing in the CBA. Establishment-led
sampling is an establishment HACCP validation and verification activity
that would allow for establishments to support the adequacy of their
HACCP system to control the Salmonella hazard at one or more steps in
the process and verify that they are producing NRTE breaded stuffed
chicken products with less than 1 CFU/g Salmonella.
Establishments may implement additional interventions to reduce the
pathogen loads on their chicken component, but since FSIS did not
receive specific comments on the interventions that establishments
would use to reduce the Salmonella levels on the product, the cost of
interventions are not included in the total cost estimate. Though the
cost of interventions is not

[[Page 35048]]

included in the CBA, establishments would only adopt new interventions
if the new interventions and the cost to implement interventions is
more beneficial than diverting or destroying product. Any new
interventions used should offset the cost of diverted or destroyed
product already accounted for in the CBA.
Comment: A poultry products trade association stated that the
benefits of the proposed determination would need to be greater than
estimated to achieve the breakeven effect noted in FSIS' CBA, as costs
were underestimated. According to the commenter, the use of the Grocery
Manufacturers Association (GMA) data does not address the specific
nature of recalls for this product class, and the CBA should account
for every recall and not every outbreak. The commenter also argued that
since trends show the number of outbreaks in these products has
decreased over the years, industry may already be implementing
interventions and trending toward less outbreaks through voluntary
actions.
Response: FSIS disagrees that costs are underestimated and that
benefits need to be higher for the final breakeven analysis. FSIS also
disagrees that the GMA report \106\ is not in scope for NRTE breaded
stuffed chicken products. The GMA report is based on survey results
from 36 companies and nearly 91 percent of respondents came from the
food and beverage industry. FSIS used this report to determine the
average impact of a recall on industry. The cost of recalls in NRTE
breaded stuffed chicken products would be similar to the cost of
recalls averaged over other food products represented in the GMA
report.
While the number of outbreaks has slowed slightly in recent years,
outbreaks are still occurring regularly, and we have no reason to
believe that there would be a downward trend absent this new policy.
The most recent 2021 outbreak resulted in more hospitalizations than
any of the 14 other NRTE breaded stuffed chicken product outbreaks,
with 36 illnesses, and 12 hospitalizations (88 FR 26258-26259).
Salmonella outbreaks have been disproportionately associated with NRTE
breaded stuffed chicken products, which account for less than 0.15
percent of the total domestic chicken supply yet represented
approximately five percent of all chicken-associated outbreaks in the
United States (88 FR 26252). Based on the available data, FSIS believes
that a downward trend in Salmonella outbreaks and illnesses from NRTE
breaded stuffed chicken can only be achieved by a policy change. The
new policy is expected to cause industry to use more effective methods
to control for Salmonella in NRTE breaded stuffed chicken products,
including diverting, or destroying chicken components with Salmonella
levels at or over the 1 CFU/g limit.

O. Additional Action

Comment: One individual stated that, in addition to the actions
discussed in the proposed determination, FSIS should incentivize
establishments to only implement validated control programs in their
HACCP Systems.
Response: FSIS regulations at 9 CFR 417.4(a) require that every
establishment validate their HACCP plan's adequacy in controlling the
food safety hazards identified during the hazard analysis and verify
that the plan is being effectively implemented. Therefore,
establishments are currently required to implement control programs
into their HACCP Systems that are validated. FSIS has published
guidance for industry on how to validate their HACCP Systems.\83\
---------------------------------------------------------------------------

\83\ FSIS Compliance Guideline: HACCP Systems Validation. April
2015. Available at: https://www.fsis.usda.gov/sites/default/files/import/HACCP_Systems_Validation.pdf.
---------------------------------------------------------------------------

Comment: In addition to the actions discussed in the proposed
determination, a consumer advocacy organization suggested that FSIS
create final product standards for all poultry products contaminated
with Salmonella.
Response: This determination is only concerned with Salmonella in
NRTE breaded stuffed chicken products. The recommendation is, thus,
outside the scope of the proposed determination. FSIS intends to
address issues related to Salmonella illnesses associated with other
raw poultry products separately through the Salmonella Framework
Initiative.\84\
---------------------------------------------------------------------------

\84\ FSIS, Proposed Regulatory Framework to Reduce Salmonella
Illnesses Attributable to Poultry, available https://www.fsis.usda.gov/inspection/inspection-programs/inspection-poultry-products/reducing-salmonella-poultry/proposed.
---------------------------------------------------------------------------

Comment: One animal welfare organization noted that stress can
cause or exacerbate Salmonella infections in live poultry and, thereby,
increase contamination in final products. Thus, in addition to the
actions discussed in the proposed determination, the commenter asked
FSIS to consider strategies to minimize the time poultry spend awaiting
slaughter, protect live poultry from severe environmental conditions
during holding, ensure stun baths are designed to prevent pre-stun
shocks, and otherwise minimize stress, bruising, and injury to birds
during transport.
Response: The final determination is concerned with Salmonella in
NRTE breaded stuffed chicken products and specifically, establishing an
adulteration threshold, and inspection verification of the new policy.
Thus, the commenters' suggestions are not within the scope of this
action. However, FSIS guidance specifically addresses best practices to
control Salmonella prior to and during slaughter and processing.\85\
FSIS inspection program personnel (IPP) also routinely verify that
poultry establishments operate in accordance with Good Commercial
Practices, which includes the employment of humane methods of handling
and slaughtering.\86\
---------------------------------------------------------------------------

\85\ FSIS Guideline for Controlling Salmonella in Raw Poultry.
June 2021. Available at: https://www.fsis.usda.gov/sites/default/files/media_file/2021-07/FSIS-GD-2021-0005.pdf.
\86\ FSIS Directive 6110.1, Verification of Poultry Good
Commercial Practices, available at: https://www.fsis.usda.gov/policy/fsis-directives/6110.1.
---------------------------------------------------------------------------

Comment: An industry member asked FSIS to partner with the U.S.
Food and Drug Administration (FDA) to implement the 1 CFU/g standard
for other RTE items such as peanut butter, lettuce, tomatoes, and other
goods that have been linked to Salmonella outbreaks so there is a
consistent standard for all such products.\87\ Another industry member
recommended that FSIS partner with universities to develop education
programs aimed at ensuring that robust statistical process control
systems are implemented at establishments. The commenter also asked
FSIS to work with the USDA Animal and Plant Health Inspection Service
to promote vaccine approval, and with other Federal partners to develop
more widespread salmonellosis risk assessments.
---------------------------------------------------------------------------

\87\ Foodborne illness source attribution estimates for 2019 for
Salmonella, Escherichia coli O157, Listeria monocytogenes, and
Campylobacter using multi-year outbreak surveillance data, United
States. The Interagency Food Safety Analytics Collaboration (IFSAC);
October 2021.
---------------------------------------------------------------------------

Response: Recommendations, petitions, and comments on non-FSIS-
regulated food products should be directed to FDA. FSIS regularly
partners with Federal and State health partners and academia to address
issues pertaining to Salmonella in FSIS-regulated products. FSIS will
continue these partnerships to ensure food safety and further consumer
protections.
Comment: A poultry products trade association and an industry
member stated that FSIS should amend 9 CFR 381.173 and 381.174 to
prohibit mechanically separated chicken (MSC) from being used as a
component of NRTE breaded stuffed chicken products.

[[Page 35049]]

Response: At this time, FSIS does not believe that 9 CFR 381.173
and 381.174 need to be revised because, under this determination, all
source material received and used to produce NRTE breaded stuffed
chicken must be considered in the establishment's hazard analysis to
support the Salmonella hazard control required and intended by the
HACCP system. Any raw chicken components establishments use to produce
NRTE breaded stuffed chicken, including MSC, will be subject to FSIS'
food safety inspection verification. MSC must also appear in the
ingredients statement.

P. Alternatives to the Proposed Action

Comment: In lieu of the proposed action, a poultry products trade
association and an industry member stated that FSIS should take the
actions described in the 2022 supplement to the National Chicken
Council's 2016 petition \88\ and otherwise focus on improved labeling
for NRTE breaded stuffed chicken products.
---------------------------------------------------------------------------

\88\ FSIS Petition 16-03, Establish Labeling Requirements for
Not-Ready-To-Eat Stuffed Chicken Products. Originally submitted on
May 24, 2016. Supplemented on February 25, 2022. Available at:
https://www.fsis.usda.gov/federal-register/petitions/establish-labeling-requirements-not-ready-eat-stuffed-chicken-products.
---------------------------------------------------------------------------

Response: As discussed throughout the proposed determination and
above, over the years, establishments have repeatedly updated their
NRTE breaded stuffed chicken product labeling practices in response to
reoccurring illness outbreaks caused by these products in an attempt to
reduce future instances of salmonellosis. However, these attempts have
been unsuccessful. Thus, FSIS does not believe codifying special
labeling requirements for NRTE breaded stuffed chicken products is
likely to address the Salmonella concerns related to these types of
products.
Comment: In lieu of the proposed action, a poultry products trade
association stated that FSIS should, amongst other actions, require all
NRTE breaded stuffed chicken to reassess their HACCP plan, noting that
FSIS has taken similar approaches in the past.
Response: HACCP system regulations require that every establishment
reassess the adequacy of its HACCP plan at least annually and whenever
any changes occur that could affect the underlying hazard analysis or
alter the HACCP plan (9 CFR 417.4(a)(3)). This final determination that
Salmonella at levels of 1 CFU/g or higher is an adulterant in NRTE
breaded stuffed chicken products constitutes such a change. Thus, all
establishments that produce NRTE breaded stuffed chicken products must
reassess their HACCP plans. Establishments that make changes to their
production process as a result of their reassessment would also need to
re-validate their HACCP plans. FSIS will issue instructions to IPP in
establishments that produce NRTE breaded stuffed chicken products to
verify that these establishments have completed their reassessment
before the effective date of this final determination. That said, FSIS
does not believe that a HACCP reassessment, in the absence of a change
in policy, is likely to be a sufficient option to address the
Salmonella concerns related to these types of products. As discussed in
the proposed determination, FSIS believes the appropriate response to
protect public health is to ensure that NRTE breaded stuffed chicken
products contaminated with Salmonella at levels sufficient to cause
human illness are excluded from commerce.
Comment: In lieu of the proposed action, a poultry products trade
association and meat industry research institute suggested that FSIS,
amongst other things, develop guidance for processing NRTE breaded
stuffed chicken products to reinforce best practices and help small
establishments.
Response: FSIS currently has several applicable industry guidance
resources available. FSIS has, for example, published industry guidance
on NRTE breaded stuffed chicken product labeling \89\ and industry
guidance for controlling Salmonella in raw poultry to assist
establishments that slaughter or process raw poultry products to
prevent and minimize the risk of Salmonella in their operations.\90\
These documents contain best practices and recommendations for industry
to consider in their food safety system(s). FSIS will continue to
publish and revise relevant guidance, as needed. However, FSIS does not
believe that new or updated guidance, in the absence of a change in
policy, is likely to be a sufficient option to address the Salmonella
concerns related to these types of products.
---------------------------------------------------------------------------

\89\ FSIS Labeling Policy Guidance: Uncooked, Breaded, Boneless
Poultry Products. Available at: https://www.fsis.usda.gov/sites/default/files/import/Labeling_Policy_Guidance_Uncooked_Breaded_Boneless_Poultry_Products.pdf.
\90\ FSIS Guideline for Controlling Salmonella in Raw Poultry.
June 2021. Available at: https://www.fsis.usda.gov/sites/default/files/media_file/2021-07/FSIS-GD-2021-0005.pdf.
---------------------------------------------------------------------------

Comment: In lieu of the proposed action, a poultry products trade
association stated that FSIS should, amongst other things, conduct food
safety assessments (FSAs) at establishments producing NRTE breaded
stuffed chicken products to verify that food safety systems are being
implemented properly for these products. The commenter also noted that
these FSAs could also help identify best food safety practices for
producing such products.
Response: FSIS does not believe that conducting FSAs, in lieu of
this final determination, would sufficiently address the Salmonella
concerns related to these types of products.
FSIS assigns and conducts Public Health Risk Evaluations (PHREs) as
described in FSIS Directive 5100.4 \91\ using both for-cause and
routine risk-based PHRE criteria. PHREs are an analysis of
establishment performance and use risk-based criteria to determine if
FSIS will conduct an FSA. FSAs, as described in FSIS Directive
5100.1,\92\ are conducted to assess an establishment's food safety
system and verify that meat, poultry, or egg products are safe,
wholesome, and produced in accordance with FSIS statutory and
regulatory requirements. FSIS will continue to conduct PHREs and FSAs
following the criteria described in these FSIS Directives at
establishments that produce NRTE breaded stuffed chicken products.
---------------------------------------------------------------------------

\91\ FSIS Directive 5100.4, Public Health Risk Evaluation
Methodology, available at:https://www.fsis.usda.gov/sites/default/files/media_file/2021-08/5100.4.pdf.
\92\ FSIS Directive 5100.1, Public Health Risk Evaluation
Methodology, available at: https://www.fsis.usda.gov/sites/default/files/media_file/2021-08/5100.4.pdf.
---------------------------------------------------------------------------

Comment: A poultry products trade association and a trade
association representing the frozen food industry stated that FSIS
should implement the recommendations outlined in NACMPI's 2021
report.\93\
---------------------------------------------------------------------------

\93\ National Advisory Committee on Meat and Poultry Inspection,
Subcommittee II: Stuffed Not Ready-to-Eat Poultry Products, USDA
(Sept. 28, 2021).
---------------------------------------------------------------------------

Response: As discussed in the proposed determination (88 FR 26259),
the report provided several recommendations that primarily focus on the
labeling of NRTE breaded stuffed chicken products. Specifically, the
subcommittee recommended that FSIS re-verify that companies continue to
voluntarily label NRTE breaded stuffed chicken products as raw in
several places on the label and that labels of these products include
validated cooking instructions. The subcommittee also recommended that
FSIS update the 2006 labeling guidance to warn consumers not to use
microwaves and air fryers if validated instructions are not provided
for these methods and to cook the product to a minimum of

[[Page 35050]]

165 [deg]F as measured using a food thermometer. The subcommittee
further recommended that FSIS add label verification for these products
as a recurring task for inspectors and review labels from the 2021
outbreak. In addition, the subcommittee recommended that FSIS require
establishments that produce these products to reassess their HACCP
plans in light of the outbreaks and encouraged FSIS to conduct targeted
consumer outreach regarding these types of products, including creating
an FSIS web page highlighting NRTE breaded stuffed chicken products.
The subcommittee also recommended that FSIS establish requirements for
the labeling of NRTE breaded stuffed chicken products and publish
industry guidance explaining how to validate cooking instructions for
such products.
In light of the 2021 Salmonella outbreak and earlier outbreaks
associated with these products, the Agency concluded and shared with
NACMPI in 2023 that the recommendations, which focus primarily on
product labeling and consumer handling practices, are unlikely to be
effective in preventing additional foodborne illnesses associated with
NRTE breaded stuffed chicken products. Therefore, FSIS concluded that
public health measures that focus primarily on product labeling and
consumer handling practices have not been effective in preventing
additional foodborne illnesses associated with NRTE breaded stuffed
chicken products.

III. Implementation

A. HACCP Reassessment

FSIS' regulations require that every establishment reassess the
adequacy of its HACCP plan at least annually and whenever any changes
occur that could affect the underlying hazard analysis or alter the
HACCP plan (9 CFR 417.4(a)(3)). This final determination that
Salmonella at levels of 1 CFU/g or higher is an adulterant in NRTE
breaded stuffed chicken products constitutes such a change. Thus, as
discussed in the proposed determination (88 FR 26264), FSIS is
announcing that all establishments that produce Heat Treated but Not
Fully Cooked--Not Shelf Stable NRTE breaded stuffed chicken products
must reassess their HACCP plans; establishments can reassess as part of
their annual reassessment if their annual reassessment occurs before
the effective date. Establishments that make changes to their
production process as a result of their reassessment would also need to
revalidate their HACCP plans. Prior to the effective date of this final
determination, FSIS will issue instructions to IPP in establishments
that produce NRTE breaded stuffed chicken products to verify that these
establishments have completed their reassessment. Establishments must
complete the reassessment and revalidate their HACCP plans by May 1
2025.

B. Implementation and Status of Laboratory Methods

As explained in the proposed determination (88 FR 26264-26266),
FSIS will implement routine sampling and verification testing for
Salmonella in NRTE breaded stuffed chicken products. In the proposed
determination (88 FR 26264), FSIS stated that it would collect samples
from the chicken component of a NRTE breaded stuffed chicken product
prior to breading and stuffing after the establishment had completed
all the processes needed to prepare the chicken to be stuffed and
breaded. However, in response to public comments, FSIS has decided to
modify the proposed verification sampling location to give
establishments greater flexibility to divert source components for
other appropriate uses and, thereby, lower lost product costs.
Therefore, instead of collecting verification 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 used to
produce NRTE breaded stuffed chicken product. In implementing sampling
and verification testing for these products, FSIS will consider the
production process at each impacted establishment and the Agency's
ability to collect samples safely and effectively.
FSIS intends to perform, evaluate, determine, and report whole
genome sequencing (WGS), serotype, levels, and antimicrobial resistance
(AMR) profile for Salmonella isolates identified.\94\ As noted in the
proposed determination (88 FR 26262), FSIS intends to continuously
evaluate and, if necessary, refine the status of Salmonella as an
adulterant in NRTE breaded stuffed chicken products as advances in
science and technology related to pathogen levels, serotypes, virulence
genes, and product matrices become available. FSIS will likewise refine
its sampling and verification testing for these products, as needed.
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\94\ This information would be reported as with any test result.
Inspectors would get result through the Public Health Information
System (PHIS). FSIS would report out through Laboratory Information
Management System (LIMS) Direct for industry as well as the result
would be in the new PHIS sample result history report. The results
would also be in public release data sets that the Agency does
quarterly. The WGS data would also be uploaded to NCBI as are other
Salmonella isolates.
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The detection and isolation methodology for Salmonella is described
in chapter 4.14, of the FSIS Microbiology Laboratory Guidebook
(MLG).\95\ When sampling the raw incoming chicken components of NRTE
breaded stuffed chicken products under this final determination, FSIS
will collect one pound of the selected incoming chicken component from
the establishment to analyze 325 grams per test for Salmonella. Samples
will be initially screened, post-enrichment, for the presence or
absence of Salmonella. Samples that screen negative will be reported as
``negative.'' For samples that screen positive, FSIS will then analyze
Salmonella levels. Potential positives that screen positive for
Salmonella presence and contain levels >=1 CFU/g will then be analyzed
using selective and differential culture-based media to identify the
presumptive positive samples. Presumptive positives will then be
confirmed by molecular-based mass spectrometric identification. A
sample is only considered a ``confirmed positive'' for Salmonella after
completion of both cultural and confirmatory testing. If any chicken
component is ``confirmed positive'' with Salmonella levels of 1 CFU/g
or higher, the entire sampled lot will need to be diverted to a use
other than NRTE breaded stuffed chicken products. Any NRTE breaded
stuffed chicken products that contain a chicken component from a
sampled lot confirmed positive with Salmonella levels of 1 CFU/g or
higher prior to stuffing and breading will be considered adulterated
and excluded from commerce.
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\95\ FSIS Microbiology Laboratory Guidebook available at:
https://www.fsis.usda.gov/news-events/publications/microbiology-laboratory-guidebook.
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FSIS estimates that negative results will routinely be available
within two days of sample collection, assuming overnight sample transit
to the laboratory coupled with an overnight sample enrichment followed
by screening and quantification at the laboratory. Enumeration is
conducted from the same sample as screen testing and both results will
be reported on the same day. For samples that are potential positives,
an additional 3 days may be necessary for a confirmed positive or
negative result. These timeframes and methods may change as FSIS
incorporates new laboratory

[[Page 35051]]

technologies into its sampling and verification testing.\96\
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\96\ For example, on July 8, 2022, FSIS announced that it had
awarded a contract to bioM[eacute]rieux to incorporate its non-
enrichment quantification system for Salmonella, `GENE-
UP^TM QUANT Salmonella,' into the Agency's laboratory
system. The Agency evaluated commercially available quantification
systems and determined that this technology is the most appropriate
for use in the high throughput FSIS laboratory environment. FSIS
stated that in the future, the Agency would announce when the method
is available and when it will be implemented in all three FSIS food
testing laboratories. FSIS also stated that it plans to extend
pathogen quantification technology to sample types other than raw
poultry rinses in the future (see FSIS Constituent Update, Jul 8,
2022, FSIS to include Salmonella Quantification in Raw Poultry Rinse
Samples. Available at: https://www.fsis.usda.gov/news-events/news-
press-releases/constituent-update-july-8-
2022#:~:text=Salmonella%20quantification%20is%20a%20significant%20ste
p%20in%20FSIS%E2%80%99,regulatory%20sample%2C%20not%20solely%20its%20
presence%20or%20absence.
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FSIS does not intend to begin the sampling and verification testing
discussed in this final determination until May 1, 2025. This should
give establishments enough time to adjust their relevant procedures and
processes to facilitate such sampling and testing.

C. Sampled Lot

When FSIS tests a product for adulterants, the Agency withholds its
determination as to whether product is not adulterated, and thus
eligible to enter commerce, until all test results that bear on the
determination have been received.\97\ Under this policy, 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, when FSIS samples raw incoming chicken components
intended for use in NRTE breaded stuffed chicken products,
establishments will need to control and maintain the integrity of the
sampled chicken components (i.e., the sampled lots) pending the
availability of test results. As noted above, establishments may
incorporate sampled lots into finished NRTE breaded stuffed chicken
products, so long as those finished products remain under establishment
control awaiting test results.
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\97\ Not Applying the Mark of Inspection Pending Certain Test
Results, 77 FR 73401, December 10, 2012.
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FSIS IPP will give establishments that produce NRTE breaded stuffed
chicken product advance notice before they collect a product sample for
verification testing to give the establishment enough time to hold or
control the sampled lot. Establishments are responsible for providing a
supportable basis for defining the sampled lot. For sampling purposes,
production lots should be defined such that they are microbiologically
independent. Microbiological independence is documented by separation,
(e.g., physical, temporal, or by sanitation intervention), that clearly
delineates the end of one production lot and the beginning of the next.
The microbiological results from one test are independent of prior or
later lots. In other words, if a chicken component sample collected
prior to stuffing and breading tests positive for Salmonella at a level
of 1 CFU/g or higher, products from other chicken component lots should
not be implicated if the lots are microbiologically independent.
Generally, FSIS recommends that establishments develop and
implement in-plant sampling plans that define production lots or sub-
lots that are microbiologically independent of other production lots or
sub-lots. Production lots that are so identified may bear distinctive
markings on the shipping cartons. FSIS has issued guidance to help
establishments comply with the requirement that product that FSIS has
tested for adulterants does not enter commerce until test results
become available.\98\ FSIS intends to update the guidance to add NRTE
breaded stuffed chicken products. In addition to providing guidance on
adequate control measures establishments can implement for products
tested for adulterants, the document also includes guidance on how
establishments can define a product lot in order to determine the
amount of product that must be controlled pending test results. Before
implementation, FSIS will update the guidance to cover sampling and
verification testing for Salmonella in the selected raw incoming
chicken components intended for use in NRTE breaded stuffed chicken
products.
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\98\ FSIS Compliance Guideline: Controlling Meat and Poultry
Product Pending FSIS Test Results (2013) at: https://www.fsis.usda.gov/guidelines/2013-0003.
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D. State Programs and Foreign Government Programs

States that have their own poultry inspection programs for poultry
products produced and transported solely within the State are required
to have mandatory ante-mortem and post-mortem inspection, reinspection,
and sanitation requirements that are at least equal to those in the
PPIA (21 U.S.C. 454(a)(1)). In accordance with this final
determination, these States will need to adopt sampling procedures and
testing methods to detect Salmonella at 1 CFU/g or above in the chicken
component in NRTE breaded stuffed chicken products that are at least
equal to FSIS' procedures and testing methods for State-inspected
establishments that produce these products.\99\ Any State participating
in a Cooperative Interstate Shipment Program will need to adopt FSIS'
sampling procedures and testing methods to detect Salmonella at 1 CFU/g
or above in NRTE breaded stuffed chicken products in selected
establishments that produce these products for shipment in interstate
commerce that are the ``same as'' those utilized by FSIS (21 U.S.C.
472).
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\99\ FSIS is not aware of any State-inspected establishments
that produce NRTE stuffed chicken products.
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Foreign countries that are eligible to export poultry products to
the United States must apply inspection, sanitation, and other
standards that are equivalent to those that FSIS applies to those
products (21 U.S.C. 466). At this time, no foreign countries export
NRTE breaded stuffed chicken products to the United States. As
discussed in the proposed determination (88 FR 26267), in evaluating a
foreign country's poultry products inspection system to determine the
country's eligibility to export NRTE breaded stuffed chicken products
to the United States, FSIS would consider whether the sampling
procedures and testing methods the country uses to detect Salmonella at
1 CFU/g in these products are equivalent to those that FSIS uses.

IV. Anticipated Costs and Benefits of This Final Determination

FSIS has considered the economic effects of this determination and
has updated the final CBA in response to public comments. In the final
CBA, FSIS updated the estimated costs and benefits for the final policy
from those published in the preliminary CBA from 2021 to 2022 dollars.
Also, in response to public comments, FSIS updated the assumed lot size
for FSIS and industry sampling, included a range of wages, updated the
assumed type of employee that will conduct establishment led sampling,
and updated the assumptions used to estimate cold storage time and
costs. With input from the Centers for Disease Control and Prevention
(CDC), the Agency included an under-reporting multiplier of 25.5 to
estimate the actual number of Salmonella illnesses associated with
outbreaks from NRTE breaded stuffed chicken products.^{100 101}

[[Page 35052]]

In the final determination, the Agency also includes an estimated
opportunity cost for the Agency to implement the new sampling and
testing program and updated the impact on small businesses
analysis.\102\ The full analysis is available at: https://www.regulations.gov/docket/FSIS-2022-0013/document.
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\100\ 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 pdf icon [PDF--9 pages]. Emerging
Infectious Diseases. 2011;17(1):7-15: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3375761/.
\101\ FSIS used the under-reporting multiplier of 25.5 estimated
in Scallan et al. for a group of pathogens for which only outbreak
data were available to approximate the total number of cases for
NRTE stuffed chicken products. FSIS used this under-reporting
multiplier as only outbreak data is available for NRTE stuffed
chicken products.
\102\ As noted by the Office of Management and Budget in the
Circular No. A-4 published on November 9, 2023. Opportunity costs
``is the cost attributable to a regulation if an agency will be
performing enforcement activities or otherwise using resources in
connection with that regulation, even if the agency's budget is not
increasing.'' https://www.whitehouse.gov/wp-content/uploads/2023/11/CircularA-4.pdf. Accessed on 02/15/2024.
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Summary of Estimated Costs and Benefits
The final determination is expected to impact six domestic
establishments and cost industry at least $5.29 million annually,
assuming a 7 percent discount rate over a ten-year period. These costs
are associated with HACCP plan reassessments, holding sampled chicken
components or finished products in storage awaiting FSIS test results,
the costs associated with developing and implementing an establishment-
conducted sampling program and destroying or diverting the chicken
components of NRTE breaded stuffed chicken with Salmonella levels at or
over the 1 CFU/g limit. Industry may also incur other costs associated
with their individual responses to this policy, including applying
interventions, training, product reformulation and label changes, and
subsequent HACCP plan validation. However, based on public comments,
the Agency does not expect establishments to make these changes. If
establishments were to implement these additional changes, then we
would expect both additional costs and benefits. The Agency would incur
an opportunity cost of $0.02 million associated with sampling and
testing for Salmonella., FSIS will be able to shift existing resources
as necessary to conduct sampling, testing, and associated FSAs to
implement the final determination. The estimated total cost for this
policy is $5.31 million: $5.29 million in costs to industry and $0.02
million in opportunity costs for FSIS, assuming a 7 percent discount
rate over a 10-year period.
The estimated benefits for this policy are derived from preventing
outbreak-related recalls.\103\ Each prevented outbreak-related recall
has an estimated benefit of $34.99 million ($1.42 million in health
benefits + $33.57 million in industry benefits). Between 2006 and 2021
there was one outbreak every 1.36 years on average (15 years / 11
outbreaks). Total benefits will exceed total costs if the new policy
prevents at least 1 outbreak-related recall every 6.6 years ($34.99
million / $5.31million).\104\ Though the policy may not prevent every
possible outbreak-related recall, the Agency expects it will prevent at
least 1 every 6.6 years.
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\103\ Though each reported outbreak between 2006 and 2021 did
not result in a recall, FSIS assumes there is a risk of recall with
each possible Salmonella outbreak.
\104\ Numbers may not add up due to rounding.
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Without this policy, there is a higher risk of Salmonella illnesses
from NRTE breaded stuffed chicken products. When only considering
health benefits, the policy would break-even if 1,134 illnesses were
avoided annually ($5.31 million / $4,682).\105\ The smallest number of
cases associated with an outbreak from NRTE breaded stuffed chicken
products occurred in 2009, with 2 reported cases, which represents an
estimated 51 cases and a cost burden of $0.24 million, when applying
the under-reporting multiplier of 25.5.\106\ The largest number of
reported cases associated with outbreaks occurred between 2008-2009,
with 47 reported cases, which represents 1,199 estimated cases and a
cost burden of $5.6 million, when applying the under-reporting
multiplier.^{107 108} Despite proper labeling, the most recent
outbreak in 2021 occurred with 36 reported cases, which represents 918
estimated cases and a cost burden of $4.3 million. In the final
determination, FSIS is declaring NRTE breaded stuffed chicken products
that contain Salmonella at levels of 1 CFU/g or higher adulterated.
FSIS intends to carry out verification procedures, including sampling
and testing of the raw incoming chicken components used to produce NRTE
breaded stuffed chicken products, to verify that producing
establishments do not produce adulterated products. This determination,
and the associated FSIS verification procedures, should decrease the
number of illnesses associated with Salmonella in NRTE breaded stuffed
chicken products.
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\105\ Number rounded to the nearest whole number.
\106\ 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 pdf icon [PDF--9 pages]. Emerging
Infectious Diseases. 2011;17(1):7-15: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3375761/.
\107\ Food Safety and Inspection Service, USDA. Salmonella in
Not Ready-To-Eat Breaded Stuffed Chicken Products. Final
Determination. Docket No. FSIS-2022-0013, available at: https://www.regulations.gov/docket/FSIS-2022-0013.
\108\ The FSIS estimate for the cost of Salmonella-related
illness $4,682 per case, (2022 dollars) was developed using the
USDA, Economic Research Service, Cost Estimates of Foodborne Illness
Salmonella (October 2014) updated for inflation. https://www.ers.usda.gov/data-products/cost-estimates-of-foodborne-illnesses/. The cost model accounts for medical costs (including
hospitalizations), premature death and productivity loss. Numbers
may not calculate due to rounding.
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Impact on Small Businesses
In the CBA, FSIS defines high-volume establishments as
establishments that produce at least 1 million pounds of NRTE breaded
stuffed chicken products annually and low-volume establishments as
establishments that produce less than 1 million pounds annually. Using
these categories, three of the six establishments that produce NRTE
stuffed chicken products were classified as high-volume, and three
establishments as low volume. All three of the low-volume
establishments are HACCP size small or very small.\109\ FSIS expects
the cost burden of this determination on low-volume establishments
would be under 4.2 percent of the estimated revenue from NRTE stuffed
chicken for these three establishments. Establishments are not required
to develop and implement their own sampling programs in response to
this determination. If establishments chose to avoid these voluntary
costs, the final determination is estimated to cost low-volume
establishments about 1.9 percent of estimated revenue from NRTE breaded
stuffed chicken products produced at these three establishments. In
addition, nearly 90 percent of production at two of the three low-
volume establishments is product other than NRTE breaded stuffed
chicken. Thus, the impact of this final determination would represent a
smaller percentage of these establishments' overall total revenue.
Further, once the policy is implemented, FSIS does not intend to begin
the FSIS sampling and the verification testing discussed in the final
determination until 12 months after the date of publication in the
Federal Register. A small business would have this time to prepare for
changes, lowering the burden. Finally, establishments needing monetary
assistance with this new policy may be able to take advantage of the
grants and financial options available to small

[[Page 35053]]

establishments, reducing potential burden. More information on these
loans and grants can be found on the FSIS website.\110\
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\109\ Under the HACCP size definitions, large establishments
have 500 or more employees, small establishments have between 10 and
499 employees, and very small establishments have less than 10
employees or less than $2.5 million in annual revenue. 61 FR 38806.
\110\ Grants and Financial Options, USDA FSIS https://www.fsis.usda.gov/inspection/apply-grant-inspection/grants-financial-options.
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V. USDA Non-Discrimination Statement

In accordance with Federal civil rights law and USDA civil rights
regulations and policies, USDA, its Mission Areas, agencies, staff
offices, employees, and institutions participating in or administering
USDA programs are prohibited from discriminating based on race, color,
national origin, religion, sex, gender identity (including gender
expression), sexual orientation, disability, age, marital status,
family/parental status, income derived from a public assistance
program, political beliefs, or reprisal or retaliation for prior civil
rights activity, in any program or activity conducted or funded by USDA
(not all bases apply to all programs). Remedies and complaint filing
deadlines vary by program or incident.
Program information may be made available in languages other than
English. Persons with disabilities who require alternative means of
communication to obtain program information (e.g., Braille, large
print, audiotape, American Sign Language) should contact the
responsible Mission Area, agency, or staff office; the USDA TARGET
Center at (202) 720-2600 (voice and TTY).
To file a program discrimination complaint, a complainant should
complete a Form AD-3027, USDA Program Discrimination Complaint Form,
which can be obtained online at https://www.usda.gov/forms/electronicforms, from any USDA office, by calling (866) 632-9992, or by
writing a letter addressed to USDA. The letter must contain the
complainant's name, address, telephone number, and a written
description of the alleged discriminatory action in sufficient detail
to inform the Assistant Secretary for Civil Rights (ASCR) about the
nature and date of an alleged civil rights violation. The completed AD-
3027 form or letter must be submitted to USDA by:
(1) Mail: U.S. Department of Agriculture, Office of the Assistant
Secretary for Civil Rights, 1400 Independence Avenue SW, Washington, DC
20250-9410;
(2) Fax: (833) 256-1665 or (202) 690-7442; or
(3) Email: usda.gov">program.intake@usda.gov.
USDA is an equal opportunity provider, employer, and lender.

VI. Additional Public Notification

Public awareness of all segments of rulemaking and policy
development is important. Consequently, FSIS will announce this Federal
Register publication on-line through the FSIS web page located at:
https://www.fsis.usda.gov/federal-register. FSIS also will make copies
of this publication available through the FSIS Constituent Update,
which is used to provide information regarding FSIS policies,
procedures, regulations, Federal Register notices, FSIS public
meetings, and other types of information that could affect or would be
of interest to our constituents and stakeholders. The Constituent
Update is available on the FSIS web page. Through the web page, FSIS is
able to provide information to a much broader, more diverse audience.
In addition, FSIS offers an email subscription service which provides
automatic and customized access to selected food safety news and
information. This service is available at: https://www.fsis.usda.gov/subscribe. Options range from recalls to export information,
regulations, directives, and notices. Customers can add or delete
subscriptions themselves and have the option to password protect their
accounts.

Paul Kiecker,
Administrator.
[FR Doc. 2024-09393 Filed 4-30-24; 8:45 am]
BILLING CODE 3410-DM-P