[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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  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.
---------------------------------------------------------------------------

    \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\
---------------------------------------------------------------------------

    \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.
---------------------------------------------------------------------------

    \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-
UPTM 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.
---------------------------------------------------------------------------

    \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