1713

Journal of Food Protection, Vol. 84, No. 10, 2021, Pages 1713–1721
https://doi.org/10.4315/JFP-21-144
Copyright Ó, International Association for Food Protection

Research Paper

Risk Factors for Salmonella Contamination of Whole Chicken

Carcasses following Changes in U.S. Regulatory Oversight
AARON T. E. BECZKIEWICZ https://orcid.org/0000-0002-0996-619X1 AND BARBARA B. KOWALCYK1,2*

1Department of Food Science and Technology and 2Translational Data Analytics Institute, The Ohio State University, Columbus, Ohio 43210, USA
MS 21-144: Received 2 April 2021/Accepted 25 May 2021/Published Online 28 May 2021

ABSTRACT
Salmonella is a common cause of foodborne illness in the United States and often is linked to chicken products. Salmonella
contamination has been associated with meat processing facility characteristics, such as the number of employees (i.e., hazard
analysis critical control point [HACCP]–based definition of size). The risk factors for Salmonella contamination in U.S. poultry
have not been evaluated since implementation of the New Poultry Inspection System (NPIS) in 2014. The goal of this study was
to determine whether risk factors for Salmonella contamination changed after implementation of the NPIS. Presence or absence
of Salmonella in whole chicken carcasses was modeled using microbiological testing data collected from 203 poultry processing
establishments by the U.S. Department of Agriculture Food Safety and Inspection Service between May 2015 and December
2019. A model was fit using generalized estimating equations for weekly presence or absence of Salmonella, and production
volume, geographic location, and season were included as potential covariates among other establishment demographics. Odds
ratios (ORs) and 95% confidence intervals (CIs) were calculated from the marginal model. Of the 40,497 analyzable samples,
1,725 (4.26%) were positive for Salmonella. Odds of contamination was lower among establishments slaughtering
10,000,000
birds per year (OR ¼ 0.466; 95% CI, [0.307, 0.710]) and establishments producing ready-to-eat finished products (OR ¼ 0.498;
95% CI, [0.298, 0.833]) and higher among establishments historically (previous 84 days) noncompliant with HACCP
regulations (OR ¼ 1.249; 95% CI, [1.071, 1.456]). Contamination also significantly varied by season and geographic region,
with higher odds of contamination during summer and outside the MidEast Central region. These results support continuation of
targeted food safety policies and initiatives promoting pathogen reduction by establishments with smaller volumes and those
noncompliant with HACCP regulations.

HIGHLIGHTS
 Low production volume and summer season are risk factors for Salmonella contamination.
 Salmonella contamination varied by region, even after adjusting for seasonality.
 Facilities producing ready-to-eat product have lower odds of contaminated raw product.
 HACCP noncompliance (9 CFR §417.4) was associated with Salmonella contamination.

Key words: Chicken; Hazard analysis critical control point; Inspection noncompliance; Risk factor; Salmonella

Salmonella is a common cause of foodborne illness in
the United States, accounting for approximately 1.02 million
illnesses, 20,000 hospitalizations, and 400 deaths annually
(18). Three of the most common Salmonella serotypes
associated with human illness (Enteritidis, Newport, and
Infantis) are frequently recovered from poultry. Approxi-
mately 196,000 illnesses are linked to chicken consumption
annually, resulting in annual economic losses of $1.1 billion
to $2.8 billion (2, 19, 20). These cost estimates do not
include government or industry costs such as those
associated with investigations, recalls, and legal action (17,
26). Given the magnitude and scope of this Salmonella issue,
targeted efforts regarding chicken and other poultry products
could significantly reduce the burden of salmonellosis.
* Author for correspondence. Tel: 614-292-6281; Fax: 614-292-0218;
E-mail: kowalcyk.1@osu.edu.
Identification of risk factors for Salmonella contami-
nation of food is an important step for reducing disease
burden, and mitigating these risk factors will likely have the
greatest impact. Risk factor research often focuses on
preharvest conditions (e.g., rearing conditions (8) and feed
withdrawal times (10)), but such mitigation strategies can
be difficult to implement industry-wide due to the
complexity of pathogen control in animal agriculture (1).
Mandatory control of pathogens already exists in processing
facilities, and industry-wide mitigation strategies may be
easier to implement if they target specific risk factors.
Further, food safety practices are driven in large part by
processing facility characteristics, such as the number of
employees or the amount of product produced (4, 12).
In previous studies, the U.S. Department of Agriculture
(USDA) Food Safety and Inspection Service (FSIS) has
evaluated the relationship between establishment character-
1714 BECZKIEWICZ AND KOWALCYK J. Food Prot., Vol. 84, No. 10

TABLE 1. Major changes in U.S. regulatory oversight of poultry processing since 2011a
Noticeb Date (mo-day-yr) Policy change Reference

76 FR 15282 03-21-2011 Salmonella and Campylobacter performance standards updated for establishments 23
processing young chickens and turkeys to accept 5 positive chicken samples per 51-
sample set as initially proposed by FSISc on 14 May 2010 (75 FR 27288).
78 FR 53017 08-28-2013 FSIS requested comment on adoption of a continuous sampling approach for 25
performance standard verification for all product classes.
79 FR 49566 08-21-2014 Poultry product regulations (9 CFR §381) (22) amended to establish a New Poultry 28
Inspection System (NPIS) for young chicken and turkey slaughter establishments. The
NPIS requires establishments to sort and remove unacceptable carcasses before
inspection by FSIS, shifts FSIS personnel from online inspection of carcasses to offline
inspection activities (e.g., verification of sanitation standard operating procedures),
requires establishments to demonstrate that product meets definition of ready-to-cook
poultry, and allows establishments to increase line speeds to 140 birds per min.
80 FR 3940 01-26-2015 Continuous sampling for performance standard verification adopted. Under this 29
approach, largest volume establishments are sampled approximately once per week.
Fewer samples are collected for smaller establishments. A “moving window”
approach for determining performance standard compliance adopted. Process control
categories (71 FR 9772) updated to reflect whether establishments meet a given
percentage of positive samples relative to the performance standard.
83 FR 56046 11-09-2018 Process control categories to be determined from the 52-week moving window ending 31
on the last Saturday of the previous month. The updated approach excludes follow-up
sampling results from process control category determination.
a
For major changes in regulatory oversight before 2011, see Ollinger et al. (13).
b
FR, Federal Register.
c
FSIS, USDA Food Safety and Inspection Service.

istics and Salmonella contamination (6, 11). However, these
studies were conducted before implementation of major
changes to regulatory oversight of poultry processors (Table
1). In 2014, the FSIS began implementing the New Poultry
Inspection System (NPIS), which was designed to focus
FSIS efforts on inspection activities more directly related to
public health outcomes such as process control systems for
Salmonella (28). Major changes to sampling protocols for
performance standard verification have also been imple-
mented. In previous risk factor studies, data from set-based
sampling (i.e., 51 samples collected in an establishment over
consecutive days) were used. However, in 2015 the FSIS
(29) adopted a continuous sampling approach (i.e., approx-
imately one sample collected per establishment per week on
a continuous basis). In 2016, the FSIS (30) also began
collecting carcass rinse samples with neutralizing buffered
peptone water (nBPW) to neutralize the antimicrobial
chemicals that are widely used in the poultry industry but
negatively impact recovery of Salmonella from samples (7).
Given these recent changes in sampling and regulatory
oversight of poultry production, a reevaluation of risk factors
for Salmonella contamination is warranted. The purpose of
this study was to provide such an update by identifying risk
factors for Salmonella contamination of whole chicken
carcasses, such as establishment characteristics and inspec-
tion compliance history, through an evaluation of Salmonel-
la-positive test results among FSIS Salmonella performance
standard verification data.
MATERIALS AND METHODS
Data source. Risk factors for Salmonella contamination of
whole chicken carcasses were evaluated based on Salmonella
performance standard verification data from the Raw Chicken
Carcass Sampling Program obtained through the FSIS Web site;
data on establishment characteristics obtained from the FSIS Meat,
Poultry and Egg Product Inspection (MPI) Directory; and FSIS
inspection and noncompliance data for individual establishments
obtained through a Freedom of Information Act request to FSIS.
The primary outcome of interest was presence or absence of
Salmonella in individual samples collected by FSIS inspectors.
Based on previous studies and preliminary analyses, the primary
risk factors considered were year, season, region (as defined by
FSIS Office of Field Operations District), whether the sample was
collected in nBPW, annual slaughter volume, product class(es)
slaughtered by establishment (e.g., turkey and other poultry),
monthly processing volume, type of finished product (e.g., raw
intact and raw nonintact), and noncompliance with individual
regulations in Title 9 of the Code of Federal Regulations (21).
To address data sparsity issues, several variables were
dichotomized (Table 2). Slaughter volume was dichotomized to
indicate whether an establishment slaughtered
10,000,000 birds
per year (i.e., the largest of five slaughter volume categories
assigned by FSIS within the MPI Directory). The FSIS Salmonella
verification testing program (25, 28, 29) includes a routine
sampling approach in which approximately five and two sample
units (carcass rinses) are collected per month from higher volume
establishments (i.e.,
5,000,000 lb [2,267,962 kg] of product per
month) and lower volume establishments (i.e., ,5,000,000 lb of
product per month), respectively. To align with these sample
allocation practices, monthly processing volume (calculated by
multiplying mean daily processing volume by the number of
production days per month) was dichotomized to indicate a high or
low processing volume. Dichotomous variables were also created
to indicate hazard analysis critical control point (HACCP) product
categories produced by each establishment.
Establishment compliance was determined for 146 individual
regulations by combining data on scheduled and performed
J. Food Prot., Vol. 84, No. 10 RISK FACTORS FOR SALMONELLA CONTAMINATION OF CHICKEN 1715

TABLE 2. Univariable association of establishment characteristics with Salmonella-positive results among whole chicken carcassesa
No. of No. of positive/ % positive Odds
Establishment characteristic establishmentsb total samples samples ratio 95% CI P (Wald)c

Geographic regiond
South West, District 05 7 81/1,326 6.11 1.948 1.184, 3.203 0.009*
North West, District 15 6 25/873 2.86 0.883 0.617, 1.262 0.493
West North Central, District 25 7 38/886 4.29 1.342 0.531, 3.389 0.534
MidWest Central, District 35 29 144/5,718 2.52 0.773 0.566, 1.057 0.107
South Central, District 40 22 226/4,350 5.20 1.641 1.008, 2.670 0.046*
East North Central, District 50 11 123/1,742 7.06 2.274 1.442, 3.587 ,0.001*
North Atlantic, District 60 14 136/1,978 6.88 2.210 1.423, 3.434 ,0.001*
MidAtlantic, District 80 37 329/7,520 4.38 1.370 0.980, 1.914 0.065
South Atlantic, District 85 29 303/6204 4.88 1.537 1.074, 2.200 0.019*
MidEast Central, District 90 41 320/9,900 3.23 REF
Slaughter volume (birds/yr)

10,000,000 157 1,395/37,313 3.74 0.336 0.261, 0.432 ,0.001*
,10,000,000 46 330/3,184 10.36 REF
Slaughter turkey
Yes 41 273/2,876 9.49 2.613 1.961, 3.481 ,0.001*
No 162 1,452/37,621 3.86 REF
Slaughter other poultry
Yes 26 194/1,972 9.84 2.636 1.967, 3.533 ,0.001*
No 177 1,531/38,525 3.97 REF
Processing volume (lb [kg] chicken/mo)

5,000,000 [2,267,961.85] 147 1,335/35,086 3.80 0.509 0.386, 0.671 ,0.001*
,5,000,000 56 390/5,411 7.21 REF
Produce raw nonintact chicken products
Ground, comminuted, mechanically separated
Yes 69 514/13,144 3.91 0.879 0.675, 1.143 0.334
No 134 1,211/27,353 4.43 REF
Injected, tenderized, vacuum tumbled
Yes 104 960/25,299 3.79 0.744 0.586, 0.945 0.015*
No 99 765/15,198 5.03 REF
Other
Yes 3 24/736 3.26 0.754 0.473, 1.202 0.235
No 200 1,701/39,761 4.28 REF
Produce raw intact chicken products
Whole Bird
Yes 126 1,121/26,454 4.24 0.985 0.778, 1.246 0.897
No 77 604/14,043 4.30 REF
Parts
Yes 187 1,653/38,727 4.27 1.051 0.618, 1.789 0.853
No 16 72/1,770 4.07 REF
Other
Yes 53 438/12,327 3.55 0.770 0.609, 0.972 0.028*
No 150 1,287/28,170 4.57 REF
Produce cooked, not shelf stable, RTE, poultry products
Yes 11 50/1,924 2.60 0.588 0.372, 0.929 0.023*
No 192 1,675/38,573 4.34 REF
Produce not fully cooked, not shelf stable, NRTE, poultry products
Yes 15 104/3,247 3.20 0.727 0.488, 1.084 0.118
No 188 1,621/37,250 4.35 REF
a
CI, confidence interval; REF, reference group; RTE, ready-to-eat; NRTE, not ready-to-eat.
b
Missing demographic factors led to exclusion of 22 establishments from the analytical data set. Eight establishments were no longer active;
three establishments changed from federal to state inspection during study period; eight establishments had addresses associated with
multiple names, identifications, or numbers; and three establishments were no longer listed in the MPI Directory with no known cause.
c
* P , 0.05.
d
As defined by the FSIS Office of Field Operations District.
1716 BECZKIEWICZ AND KOWALCYK
inspection tasks with noncompliance records issued to establish-
ments. To align with the time frame used in determination of
public health regulations (PHRs) by the FSIS (32), a variable
indicating compliance, noncompliance, or nonobservance in the
84 days preceding sample collection was created for each
regulation (Supplemental Table S1).
Because seasonality has been associated with Salmonella
contamination, season was assigned for each observation using
week definitions from the Morbidity and Mortality Weekly Report:
winter, weeks 48 through 52 and 1 through 8 (roughly December
through February); spring, weeks 9 through 21 (roughly March
through May); summer, weeks 22 through 35 (roughly June
through August); and autumn, weeks 36 through 47 (roughly
September through November). To limit the impact of potential
uncontrolled confounders, establishments for which demographic
data were missing were excluded from analyses. A complete list
and description of variables in the analytical data set are provided
in Table S1.
Statistical analyses and model development. Descriptive
statistics were estimated for establishment characteristics, micro-
biological results, and inspection data. Odds ratios (ORs) and 95%
confidence intervals (CIs) were estimated for potential risk factors
in the analyses. Appropriateness of the multivariable model was
evaluated using methods described by Preisser and Qaqish (15).
All analyses were conducted in SAS 9.4 (SAS Institute, Cary,
NC), and code for the multivariable risk factor model is provided
in Supplemental Material S2.
A generalized estimating equation (GEE) approach was used
to develop a multivariable risk factor model for Salmonella
contamination of whole chicken carcasses (16, 37). Although the
GEE approach to statistical modeling requires no assumptions
about the distribution of data beyond specifying an appropriate
link (e.g., logit for binary data), a pairwise chi-square analysis of
establishment demographic factors (e.g., slaughter volume and
processing volume) was conducted to test for independence of
predictor variables and to inform the model building process.
Variables were tested for association with a Salmonella-positive
test result using a working independence correlation structure.
Establishment characteristic variables were included in the
multivariable model selection process when marginally associated
(P , 0.20) with a Salmonella-positive result. Only 84-day
historical compliance variables with ,10% of observations
classified as not observed and a marginally significant (P ,
0.20) univariable association with a Salmonella-positive result
were considered in the multivariable process.
The multivariable model was developed using a multistaged
approach in a manner that minimized the quasi-likelihood under
the independence model criterion statistic first proposed by Pan
(14) for assessing GEE model fit (5). Ideally, all risk factors
univariably associated with a Salmonella-positive result would be
jointly modeled with backward selection of the final multivariable
model. Nonconvergence of this model paired with a high number
of not observed values among historical compliance variables
necessitated a modified approach. To avoid potential model
misspecification from not observed inspection data, an initial
multivariable model containing only establishment characteristics
and administrative information (e.g., year or season of sample
collection) was developed through backward selection of variables
marginally associated with a Salmonella-positive result. Historical
compliance variables that met the inclusion criteria were then
sequentially added through forward selection and kept in the
multivariable model when statistically significant (P , 0.05)
according to the Wald test.
J. Food Prot., Vol. 84, No. 10
FIGURE 1. FSIS Salmonella performance standard verification
test results for whole chicken carcasses. Test results are reported
for 40,497 carcass rinse samples collected from 2015 through
2019. Proportion of samples testing positive for Salmonella is
reported by year and season. This proportion should not be
interpreted as an industry-wide prevalence because verification
sampling programs were not designed for prevalence estimation.
RESULTS
Samples were collected from 225 establishments
through the whole chicken carcass Salmonella verification
testing program from 2015 through 2019, but 22 establish-
ments were excluded from this analysis because of missing
demographic factors. Of the remaining 203 establishments,
72.4% slaughtered
10,000,000 birds per year (high
volume) and 27.6% slaughtered ,10,000,000 birds per
year (low volume) (Table 2). A total of 40,497 carcass rinse
samples were collected and tested from the 203 establish-
ments during the study period, and 1,725 (4.26%) were
positive for Salmonella, although this rate differed by year
and season (Fig. 1). Of the 1,722 Salmonella isolates that
were serotyped, 872 (50.6%) were Salmonella Kentucky,
244 (14.2%) were Salmonella Enteritidis, 168 (9.8%) were
Salmonella Infantis, 167 (9.7%) were Salmonella Typhi-
murium, and 271 (15.7%) were identified as other
serotypes. These proportions of samples positive for
Salmonella should not be interpreted as an industry-wide
prevalence because verification sampling programs are not
designed for prevalence estimation. A total of 7,487,102
inspection tasks were scheduled among the 203 establish-
ments during the study period, resulting in a total of
193,664 noncompliance records.
Eight of the 13 establishment demographic factors
considered in the univariable GEE model were significantly
associated (P , 0.05) and 1 factor was marginally
associated (P , 0.20) with a Salmonella-positive test result
(Table 2). Year and sample collection method (i.e., in nBPW
or not in nBPW) were significantly associated (P , 0.05)
and season was marginally associated (P , 0.20) with a
Salmonella-positive result (Fig. 2). Of the 146 historical
compliance variables evaluated by univariable analysis, 30
were significantly associated (P , 0.05) and 25 were
marginally associated (P , 0.20) with a Salmonella-
J. Food Prot., Vol. 84, No. 10 RISK FACTORS FOR SALMONELLA CONTAMINATION OF CHICKEN
FIGURE 2. Univariable association of sample-specific factors
with Salmonella-positive test results among whole chicken carcass
samples. Odds ratios (with 95% confidence intervals) are reported.
Each variable’s reference group is indicated by [ref]. Year (P ,
0.001) and sample collection in nBPW (P , 0.001) were
significantly associated with Salmonella-positive results. Season
(P ¼ 0.088) was marginally associated with Salmonella-positive
results.
positive result (Table S3). Only 22 of the 146 variables
considered had a not observed value for ,10% of
observations; 13 of these were at least marginally associated
with a Salmonella-positive result in the univariable analysis
and were considered in the multivariable model (Table 3).
Although exclusion of 124 regulation variables from further
analyses was not ideal, doing so limits the potential for
model misspecification, which could negatively impact
generalizability of the results. Historical compliance
variables considered in the multivariable model pertained
to a wide range of regulations, including general labeling,
product weight labeling, poultry product inspection, sanita-
tion, and HACCP.
Backward selection of establishment demographic
factors followed by forward selection of historical compli-
ance variables resulted in a multivariable model with eight
factors significantly (P , 0.05) or marginally (P , 0.10)
associated with a Salmonella-positive result (Table 4). As
expected, odds of contamination were higher for samples
collected in summer than for those collected in winter. After
adjusting for seasonal and establishment-specific character-
istics (e.g., annual slaughter volume), region was also
significantly associated with contamination. Higher odds of
contamination were identified among establishments locat-
ed in the South West (District 05), South Atlantic (District
85), and the East North Central (District 50) regions of the
United States compared with establishments in the MidEast
Central (District 90) region. Only two inspection variables
remained significant in the multivariable model: 9 CFR
§417.4 (HACCP system validation, verification, and
reassessment) and 9 CFR §317.2 (label definition and
required features) (21). Further investigation revealed that
compliance with 9 CFR §317.2 provided minimal improve-
ment in model fit but led to exclusion of 2,265 observations
(5.6% of all observations) due to not observed values. To
1717
avoid biasing other model estimates, this variable was
excluded from the final multivariable model. Of all factors
included in the model, the use of nBPW during sampling
was by far the strongest predictor of a Salmonella-positive
result.
DISCUSSION
As governmental regulatory agencies and food manu-
facturers work to continue improving the safety of meat and
poultry products, our understanding of how different
practices or factors impact the safety of such products also
needs improvement. In response to recent major changes in
U.S. regulatory oversight of poultry production, this study
was conducted to reevaluate risk factors for Salmonella
contamination of whole chicken carcasses. The results of
this study (i) confirmed that establishment volume and
season remain risk factors for Salmonella contamination;
(ii) revealed new potential risk factors for Salmonella
contamination; and (iii) revealed how accounting for
correlation between observations can impact results.
Confirmation of prior risk factors. Following the
major changes to regulatory oversight of poultry, establish-
ment size remains a risk factor for Salmonella contamina-
tion. Eblen et al. (6) found that large establishments (as
defined by the number of employees) had lower odds of
failing to meet the Salmonella performance standard than
did small establishments. Our study, in which establishment
size was defined by slaughter and processing volume,
revealed that high-volume establishments had significantly
lower odds of a Salmonella-positive test result than did low-
volume establishments. Although both studies found lower
odds of contamination among larger establishments, the
difference in how establishment size was defined in the two
studies is significant. HACCP-based size could be indica-
tive of processing capacity (e.g., greater volume requires
more employees to process), but defining establishment size
by either slaughter volume or processing volume provides a
more accurate estimate of how much product is routing
through an establishment. This approach would be espe-
cially important for poultry processing in which scalding,
picking, and chilling of carcasses can lead to serial cross-
contamination (3). Thus, the number of carcasses slaugh-
tered and processed could truly impact contamination.
Because of data limitations, size was defined in the present
study by dichotomous indicators for slaughter and process-
ing volume; these two variables were highly correlated
(results not shown), and only one (slaughter volume) was
kept in the model by the backward selection process.
Regardless of how establishment size is defined, the
higher odds of contamination among establishments with
lower slaughter volume is logical. For example, facilities
processing a larger volume are more likely to implement
processing technologies that improve safety (e.g., inside-
outside bird washer), microbiological testing, and food
safety trainings for employees (4, 12). In contrast, lower
volume facilities rely more on sanitation practices and
modification to daily operations to maintain food safety
(12). Extending this work, an index for food safety
1718 BECZKIEWICZ AND KOWALCYK J. Food Prot., Vol. 84, No. 10

TABLE 3. Historical verification status and univariable association of 9CFR regulations (21) with Salmonella-positive test results for
whole chicken carcassesa
Historical verification status (84-day history)

Not compliant Compliant Not observed

9 CFR section No. % No. % No. % Odds ratio 95% CI P (Wald)b

317.2, Labeling, definition 841 2.0767 37,391 92.3303 2,265 5.5930 1.563 1.132, 2.160 0.007*
381.65, PP inspection, general 37,492 92.5797 3,005 7.4203 0 0 0.454 0.352, 0.585 ,0.001*
381.76, PP inspection, inspection 23,228 57.3573 16,831 41.5611 438 1.0816 0.881 0.724, 1.073 0.208
381.117, PP inspection, name of product 6,650 16.4210 32,934 81.3245 913 2.2545 1.081 0.858, 1.362 0.507
381.121, PP inspection, quantity 4,048 9.9958 34,720 85.7347 1,729 4.2695 1.327 0.898, 1.962 0.156
381.122, PP inspection, identification 1,747 4.3139 37,658 92.9896 1,092 2.6965 0.734 0.495, 1.087 0.122
381.123, PP inspection, official marks 2,856 7.0524 37,042 91.4685 599 1.4791 0.938 0.707, 1.244 0.657
381.125, PP inspection, handling 658 1.6248 38,001 93.8366 1,838 4.5386 1.087 0.604, 1.954 0.781
381.175, PP inspection, requirements 341 0.8420 38,099 94.0786 2,057 5.0794 1.861 1.047, 3.307 0.034*
416.1, Sanitation, rules 19,046 47.0306 21,450 52.9669 1 0.0025 0.978 0.814, 1.173 0.808
416.2, Sanitation, grounds and facilities 37,244 91.9673 3,084 7.6154 169 0.4173 0.691 0.521, 0.916 0.010*
416.4, Sanitation, sanitary operations 38,544 95.1774 1,628 4.0201 325 0.8025 0.55 0.403, 0.752 0.000*
416.5, Sanitation, employee hygiene 13,942 34.4272 24,690 60.9675 1,865 4.6053 1.05 0.878, 1.254 0.595
416.12, Sanitation, development SSOPs 4,277 10.5613 36,154 89.2757 66 0.1630 0.985 0.745, 1.304 0.919
416.13, Sanitation, implementation SSOPs 38,158 94.2243 2,339 5.7757 0 0 0.513 0.383, 0.687 ,0.001*
416.14, Sanitation, maintenance SSOPs 12,138 29.9726 28,326 69.9459 33 0.0815 1.098 0.905, 1.331 0.343
416.16, Sanitation, records 16,557 40.8845 23,940 59.1155 0 0 0.997 0.838, 1.185 0.972
417.2, HACCP systems, hazard analysis
and HACCP plan 28,204 69.6447 12,290 30.3479 3 0.0074 0.831 0.693, 0.998 0.047*
417.3, HACCP systems, corrective actions 9,159 22.6165 30,646 75.6747 692 1.7088 1.185 0.975, 1.440 0.089
417.4, HACCP systems, validation,
verification, reassessment 7,100 17.5322 33,395 82.4629 2 0.0049 1.333 1.104, 1.610 0.003*
417.5, HACCP systems, records 16,373 40.4302 24,122 59.5649 2 0.0049 1.101 0.953, 1.272 0.191
442.2, Weight labeling, net weight
compliance 4,190 10.3464 33,316 82.2678 2,991 7.3857 1.293 0.893, 1.872 0.173
a
Regulations presented when eligible for inclusion in multivariable model (,10% of observations not observed in 84-day compliance
history). Historical verification and univariable association with a positive Salmonella result for all regulations considered provided in
Table S3. CFR, Code of Federal Regulations; CI, confidence interval; PP, poultry product.
b
* P , 0.05.

technology among meat and poultry plants was developed,
and smaller volume facilities had lower technology indices
than did larger volume facilities and facilities owned by
multiplant firms (13). This higher technology index was
also observed among meat and poultry plants that were
subject to food safety auditing (i.e., third-party food safety
evaluations).
Season also remained a risk factor; the odds of
Salmonella contamination were higher in the summer than
in winter. Poultry contamination typically follows a
seasonal pattern (35). Further temporality was seen with
decreasing odds of contamination across years, even after
adjusting for other variables. The FSIS started using
nBPW for collecting samples in 2016 because of the
negative impact of antimicrobial chemicals used in poultry
processing on Salmonella recovery from carcass rinses (7,
36). Our results were consistent with these findings; the
odds of testing positive for Salmonella were significantly
higher for samples collected in nBPW. However, the
introduction of nBPW did not account fully for the
temporal trends in contamination. After adjusting for
nBPW use, significantly higher odds of contamination
were found for 2016 and 2017 samples than for samples
from 2019. Although results from this study cannot be
used for causal interpretation, we hypothesized that the
apparent increase in Salmonella contamination following
introduction of nBPW encouraged establishments to
implement additional control measures that lead to
contamination reductions over time. The FSIS continues
to collect samples under the Salmonella verification testing
program, and follow-up evaluations of data collected after
2018 could provide more insight into temporal trends and
identify additional risk factors that may have been masked
by the change to nBPW.
Identification and reevaluation of risk factors.
Region and type of finished product were identified as
new risk factors for Salmonella contamination. In contrast
to previous studies, region (as defined by FSIS district) was
significantly associated with a Salmonella-positive result in
the present study. The South West (District 05), South
Atlantic (District 85), and East North Central (District 50)
regions had significantly higher odds of contamination than
did the MidEast Central (District 90) region. The MidEast
J. Food Prot., Vol. 84, No. 10 RISK FACTORS FOR SALMONELLA CONTAMINATION OF CHICKEN 1719

TABLE 4. Multivariable risk factor models for association of establishment characteristics and 9 CFR regulations (21) with Salmonella-
positive test results for whole chicken carcassesa
Model variable Variable value Odds ratio 95% CI P (Wald)b

Year 2015 1.514 0.990, 2.315 0.056

2016 1.384 1.089, 1.758 0.008*
2017 1.252 1.010, 1.553 0.040*
2018 1.069 0.924, 1.238 0.368
2019 REF
Season Spring 1.043 0.899, 1.210 0.581
Summer 1.150 1.006, 1.314 0.040*
Fall 1.037 0.911, 1.180 0.584
Winter REF
Geographic regionc South West, District 05 1.541 1.043, 2.278 0.030*
North West, District 15 0.647 0.424, 0.990 0.045*
West North Central, District 25 0.980 0.513, 1.871 0.950
MidWest Central, District 35 0.807 0.604, 1.079 0.148
South Central, District 40 1.500 0.934, 2.409 0.094
East North Central, District 50 1.491 1.012, 2.198 0.043*
North Atlantic, District 60 1.321 0.804, 2.170 0.272
MidAtlantic, District 80 1.229 0.896, 1.687 0.201
South Atlantic, District 85 1.490 1.039, 2.137 0.030*
MidEast Central, District 90 REF
Sample collection nBPW 3.812 2.822, 5.149 ,0.001*
Non-nBPW REF
Slaughter volume
10,000,000 birds/yr 0.466 0.307, 0.710 ,0.001*
,10,000,000 birds/yr REF
Slaughter turkey Yes 1.557 0.973, 2.491 0.065
No REF
Produce cooked, not shelf stable, Yes 0.498 0.298, 0.833 0.008*
RTE poultry products No REF
Noncompliant with 9 CFR §417.4 Yes 1.249 1.071, 1.456 0.005*
(84-day history)d No REF
a
CFR, Code of Federal Regulations; CI, confidence interval; REF, reference group; nBPW, neutralizing buffered peptone water.
b
* P , 0.05.
c
As defined by the FSIS Office of Field Operations District.
d
Regulation applies to HACCP systems (validation, verification, and reassessment).

Central region was selected as the reference group because
it has the highest concentration of poultry processing
establishments. These observed differences may have been
due to differences in establishment characteristics or
preharvest seasonal conditions, but because the differences
remained after adjusting for seasonal conditions and
establishment characteristics, region may represent an
unmeasured risk factor. For example, region could be a
surrogate measure for differences in management approach-
es between corporations and/or district offices. Given
sustained interest in food safety culture and the impact of
human behavior on food safety, collection of such data
within regulatory contexts could facilitate inclusion of
human factors and management approaches in future work
on Salmonella contamination of meat and poultry products.
Finished product type, which was not considered in
previous studies, was associated with Salmonella contam-
ination in the present study. Lower odds of contamination
were found for establishments that produce both raw and
ready-to-eat (RTE) poultry products. Although larger
establishments typically process a wider variety of products,
slaughter volume and production of RTE products were not
significantly correlated in this study (results not shown).
Further exploration of how the 11 establishments producing
raw and RTE finished products differed from other
establishments could identify future areas for targeted
improvement in Salmonella reduction.
One area that might help explain the inverse association
between Salmonella contamination in raw product and
regulation for RTE products is the establishment’s HACCP
system. In this study, the odds of a Salmonella-positive test
result among establishments noncompliant with any com-
ponent of HACCP system validation, verification, and
reassessment (9 CFR §417.4) (22) in the 84 days before
sample collection were higher than those for establishments
that were compliant. Noncompliance with 9 CFR §417.4
could indicate a systematic process control issue for finished
products, and additional exploration of the relationship
between HACCP noncompliance and Salmonella contam-
ination is warranted.
None of the sanitation regulations univariably associat-
ed with a Salmonella-positive result remained significant in
the final multivariable model, even though an association
between sanitation noncompliance and Salmonella control
1720 BECZKIEWICZ AND KOWALCYK
performance was found by Muth et al. (11). These authors
defined compliance as the percentage of establishments
compliant for the specified inspection task code. In contrast,
the present study used a categorical variable indicating 84-
day historical compliance, noncompliance, or not observed
status for individual regulations. The approach used by Muth
et al. was, until recently, fairly common and used in risk
assessments conducted by the FSIS (24, 27). However, our
approach aligns more closely with current methods used by
the FSIS to determine PHRs for meat and poultry processing
on an annual basis (32) and, thus, identifies risk factors that
could be more easily targeted through policy initiatives.
GEE approach to risk factor analyses. Regarding
interpretation of our results in the context of previous work,
odds ratios presented here are not directly comparable to
those in previous risk factor studies conducted with U.S.
regulatory data. Risk factor analyses conducted by Eblen et
al. (6) and Muth et al. (11) included a different outcome
measure: a dichotomous variable indicating whether an
establishment met a given level of the Salmonella
performance standard based on a set of 51 samples. This
difference is important because there are multiple ways to
address correlation between observations made in the same
establishment. In previous studies, a derived-variable
approach was used in which correlated observations (e.g.,
51 samples collected within the same establishment) were
collapsed into a single observation and then analyzed using
independent data methods such as logistic regression. In
contrast, a GEE approach was used in the present study in
which correlation between observations was addressed by
postestimation adjustments to model parameter standard
errors (9, 34, 37). This approach maintains a larger effective
sample size (e.g., 40,497 observations instead of the 203
observations obtained with the derived-variable approach),
which allows for a more granular analysis. Muth et al. (11)
noted that analysis of regulatory data is often limited by the
need for large data sets. As revealed in the present study,
this issue can be resolved by using a GEE approach to
identify risk factors.
Several limitations to the present study were identified.
Twenty-two establishments were excluded from the analyt-
ical data set due to missing information for demographic
variables. Missing data (e.g., no longer active or multiple
establishment names or identifications associated with an
address) could have resulted from a lack of Salmonella
control within the establishment. Although the primary goal
of this study was to identify risk factors following
implementation of the NPIS, this study was not designed
to assess the direct impact of the NPIS on Salmonella
contamination within the poultry industry. The present study
criteria for determining eligibility of historical inspection
variables were less restrictive than those used in other
studies. When determining PHRs, the FSIS requires that a
regulation be verified at least 30 times within the historical
window for inclusion in analyses; this stipulation is meant
to reduce the potential for biased values. Such a restriction
was not applied in the present study because the vast
majority of regulations would have been excluded. Instead,
J. Food Prot., Vol. 84, No. 10
the researchers addressed not observed values by including
only those historical variables with ,10% of observations
being not observed.
Although meat and poultry safety has improved since
implementation of the pathogen reduction HACCP rule in
1996 (22), Salmonella remains a major concern. The
proposed Healthy People 2030 goals continue to target a
reduction in outbreaks of Salmonella infection (among other
foodborne pathogens) linked to poultry (33). Future policies
and initiatives targeting the risk factors identified by our
GEE approach could reduce Salmonella contamination of
whole chicken carcasses and contribute to meeting the
Healthy People 2030 goals. Predictive modeling of
information collected on a regular basis, such as compliance
with regulations as measured during daily inspection
activities, could inform directed real-time interventions for
controlling Salmonella contamination. Such an approach
would likely be limited by not observed values among
compliance data; therefore, future work in this area should
explore alternative ways to model historical compliance
such as use of lagged and latent variables.
ACKNOWLEDGMENTS
The authors thank Isabel Walls, Eric Ebel, Rebecca Fields, Selena
Kremer, and Breauna Branch for providing input during the modeling
process and reviewing this manuscript. This research was supported by
The Ohio State University and an appointment to the FSIS Research
Participation Program administered by the Oak Ridge Institute for Science
and Education (ORISE) through an interagency agreement between the
U.S. Department of Energy (DOE) and the National Institute of
Environmental Health Sciences. ORISE is managed by Oak Ridge
Associated Universities (ORAU) under DOE contract DE-SC0014664.
All opinions expressed in this article are the authors’ and do not
necessarily reflect the policies and views of USDA, FSIS, DOE, ORAU, or
ORISE.
SUPPLEMENTAL MATERIAL
Supplemental material associated with this article can be
found online at: https://doi.org/10.4315/JFP-21-144.s1; https://doi.
org/10.4315/JFP-21-144.s2
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