Journal of Food Protection 87 (2024) 100293
Contents lists available at ScienceDirect
Journal of Food Protection
ELSEVIE
Protecting the Global Food Supply
journal homepage: www.elsevier.com/locate/jfp
Research Paper
Environmental Antecedents of Foodborne Illness Outbreaks, United States, ®
Check for
2017-2019 —
Meghan M. Holst’, Sabrina Salinas *, Waimon T. Tellier °, Beth C. Wittry '
1 Centers for Disease Control and Prevention, National Center for Environmental Health, 4770 Buford Highway, Atlanta, GA 30341, USA
? Harris County Public Health, Environmental Public Health, 1111 Fannin Street, Houston 77002, USA
3 Washington State Department of Health, Office of Communicable Disease Epidemiology, 1610 NE 150th Street, Shoreline, WA 98155, USA
ARTICLE INFO ABSTRACT
Keywords:
Environmental antecedents
Foodborne outbreak investigations often provide data for public health officials to determine how the environ-
ment contributed to the outbreak and on how to prevent future outbreaks. State and local health departments
are responsible for investigating foodborne illness outbreaks in their jurisdictions and reporting the data to
national-level surveillance systems, including information from the environmental assessment. This assessment
is designed to describe how the environment contributed to the outbreak and identifies factors that contributed
to the outbreak and environmental antecedents to the outbreak. Environmental antecedents, also referred to as
root causes, are specific reasons that allow biological or chemical agents to contaminate, survive, or grow in
food. From 2017 to 2019, 24 jurisdictions reported 1,430 antecedents from 393 outbreaks to the National
Environmental Assessment Reporting System. The most reported antecedents were lack of oversight of employ-
ees/enforcement of policies (89.1%), lack of training of employees on specific processes (74.0%), and lack of a
food safety culture/attitude towards food safety (57.5%). These findings highlight the critical role that employ-
ees play in restaurant food safety and are heavily influenced by restaurant management, who can exercise
active managerial control to manage these antecedents. Identifying antecedents during investigations is essen-
tial for understanding the outbreak’s root cause and implementing sustainable corrective actions to stop the
Environmental assessment
Environmental health
Foodborne illness outbreak
Illness prevention
Root cause
immediate outbreak and future outbreaks.
The Centers for Disease Control and Prevention (CDC) estimates
that around 48 million foodborne illnesses occur each year in the Uni-
ted States. This number includes 128,000 hospitalizations and 3,000
deaths (Scallan et al., 2011). Illnesses associated with outbreaks
account for a small portion of the annual foodborne illness incidence
(Dewey-Mattia et al., 2018). However, data from foodborne outbreak
investigations can provide detailed information that helps determine
how the environment contributes to outbreaks. That information can
be used to prevent future outbreaks (Dewey-Mattia et al., 2018). The
lessons we learn from outbreak investigations can also be used to pre-
vent sporadic cases of foodborne illnesses.
State and local health departments are responsible for investigat-
ing foodborne illness outbreaks and reporting the data to national-
level surveillance systems managed by the CDC. CDC aggregates
these data to detect national trends and identify systematic food
safety issues. The National Environmental Assessment Reporting Sys-
tem (NEARS) is a CDC surveillance system through which some state
and local health departments voluntarily report data from their
* Corresponding author.
E-mail address: [email protected] (M.M. Holst).
https://doi.org/10.1016/j.jfp.2024.100293
Received 7 March 2024; Accepted 30 April 2024
Available online 6 May 2024
investigations of foodborne illness outbreaks at retail food establish-
ments (Centers for Disease Control and Prevention, 2022b). Specifi-
cally, they report data from the environmental health component
of the investigation, typically called the environmental assessment.
The assessment is designed to describe how the outbreak environ-
ment contributed to the introduction or transmission of the agent
that caused the outbreak (Centers for Disease Control and
Prevention, 2022c). NEARS collects two key sets of environmental
assessment data about the outbreak (Freeland et al., 2019; Moritz
et al., 2023).
The first set is outbreak contributing factors—the practices that
most likely led to contamination, proliferation, or survival of agents
in the environment (Centers for Disease Control and Prevention,
2023). The second set is environmental antecedents, hereafter referred
to as antecedents, of the outbreak. Antecedents are the circumstances
and situations that led to the contributing factors. For example, an
investigation may identify the contributing factor to a norovirus out-
break as contamination of food by an ill employee, and the antecedent
0362-028X/Published by Elsevier Inc. on behalf of International Association for Food Protection.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
M.M. Holst et al.
as insufficient staffing, which led to the employee not being allowed to
stay home while ill.
Identifying the contributing factors and antecedents is essential to
understanding the outbreak’s root cause and implementing sustainable
corrective actions to stop the outbreak and future outbreaks (Firestone
et al., 2018). Collecting and analyzing these data at a national level are
essential for informing efforts to prevent future outbreaks in retail
environments across the country. The data can be used to inform
national food safety policy and training focused on reducing contribut-
ing factors and antecedents (Centers for Disease Control and
Prevention, 2022a; Matis et al., 2017; Wittry et al., 2022). To con-
tribute to these goals, the current study presents data on the contribut-
ing factors and antecedents for outbreaks reported to NEARS from
2017 to 2019.
Materials and Methods
Between 2017 and 2019, state and local health departments
reported data to NEARS from 799 outbreak investigations with a sus-
pected or confirmed foodborne agent. CDC defines a foodborne illness
outbreak as an incident in which two or more people experience a sim-
ilar illness resulting from the ingestion of a common food (Centers for
Disease Control and Prevention, 2015). The dataset for this paper is
limited to the 393 outbreaks that had at least one reported antecedent.
The outbreaks occurred in Alaska, California, Connecticut, Delaware,
Fairfax County (VA), Georgia, Harris County (TX), Indiana, Iowa, Jef-
ferson County (CO), Maricopa County (AZ), Massachusetts, Michigan,
Minnesota, New York City, New York State, North Carolina, Oregon,
Rhode Island, South Carolina, the Southern Nevada Health District,
Tennessee, Washington, and Wisconsin.
Investigators conducting environmental assessments for outbreaks
in retail food establishments engage in a variety of data collection
activities. These include kitchen observations, reviews of records,
and staff interviews. Data from these activities, along with data
obtained from epidemiological and laboratory investigations, are
reported to NEARS (Lipcsei et al., 2019; Moritz et al., 2023). Addition-
ally, investigators report any contributing factors or antecedents they
identified during their outbreak investigation. The identification is
based on their review of the totality of the data collected during the
observation and their professional judgment and experience. Investi-
gators select contributing factors from a predetermined list of 32 con-
tributing factors. The list of factors is derived from an analysis of
historical data from outbreak investigations (Bryan, 1978; Weingold
et al., 1994). The investigators also select antecedents from a list of
17 potential antecedents and an option to write in an ‘other’ response.
This list was developed by food safety experts using the food system
environmental antecedent conceptual model (Selman & Guzewich,
2014). The model theorizes that there are five main groups of environ-
mental antecedents that influence food safety in establishments. The
groups are people (behaviors, characteristics, and attitudes of people
working in the establishments); processes (characteristics of the pro-
cesses used to prepare food and food preparation complexity); eco-
nomics (costs and profit margins); equipment (the physical layout and
equipment of establishments); and food (the inherent qualities of food
prepared in establishments). Investigators can report multiple con-
tributing factors and antecedents for each outbreak.
We created the dataset for this study with SAS 9.3 statistical soft-
ware (SAS Institute, Cary, NC), then used Microsoft Excel to conduct
descriptive analyses on the data. The analyses focused on outbreak eti-
ologic agents, contributing factors, and antecedents. Additionally, to
better understand how outbreak antecedents vary by etiologic agent
and contributing factor, we disaggregated the antecedent data by the
most common etiologic agents and contributing factors. We also disag-
gregated the antecedent data on the most common outbreak etiologic
agents, contributing factors, and year.
Journal of Food Protection 87 (2024) 100293
Results
Outbreak characteristics. Of the 393 foodborne outbreaks
included in this analysis, 79.1% (311) had an identified agent. Over
70% (72.7% [226]) of these outbreaks with an identified agent had
a confirmed etiologic agent and the remaining outbreaks (27.3%
[85]) had a suspected etiologic agent. The most common agents were
norovirus (39.7%), Salmonella (13.5%), and Clostridium perfringens
(6.4%) (Table 1). Investigations did not identify an etiologic agent in
20.9% (82) of outbreaks. The most commonly identified contributing
factors fell into the contamination category: other mode of contamina-
tion by a suspected infectious worker (24.4%), cross-contamination of
ingredients (14.2%), and bare-hand contact by a suspected infectious
worker (14.2%) (Table 2).
Outbreak antecedents. Investigators identified 1,430 antecedents
associated with the 393 outbreaks. The majority of identified antece-
dents fell into the people category (67.4%), followed by the process
(13.4%), equipment (8.7%), economics (5.9%), other (i.e., antecedents
that do not fall into existing categories) (3.3%), and food (1.3%) cate-
gories (Table 3).
The top three antecedents fell into the people category: lack of
oversight of employees (89.1%), lack of training of employees on
specific processes (74.0%), and lack of food safety (57.5%) (Table 3).
The next two most common antecedents fell into the process category:
staff not following the facility’s processes (24.9%) and insufficient pro-
cess to mitigate hazard (23.9%).
Outbreak antecedents by etiologic agent. The three most com-
mon etiologic agents were the virus norovirus, and the bacteria Sal-
monella and Clostridium perfringens. The three most common
antecedents for all three types of outbreaks were people antecedents:
lack of oversight of employees (78.8%, 60.4%, 48.0%, respectively),
lack of training of employees (51.3%, 54.7%, and 56.0%, respec-
tively), and lack of food safety culture (39.1%, 52.8%, and 36.0%,
respectively) (Table 4). However, the antecedent of lack of oversight
of employees was identified far more often for norovirus outbreaks
than for the bacterial outbreaks (78.8% vs 60.4%, 48.0%). Addition-
Table 1
Foodborne outbreak etiologic agents—National Environmental Assessment
Reporting System, 2017-2029
Agent* n % of
outbreaks”
(n = 393)
Virus
Norovirus 156 39.7
Hepatitis A 2 0.5
Bacteria
Salmonella species 53 13.5
Vibrio species 10 2.5
Clostridium perfringens 25 6.4
Campylobacter species 14 3.6
Escherichia coli, 0157: H7 5 1.3
Escherichia coli, other Shiga toxin—-producing or 7 1.8
verotoxin-producing
Shigella species 5 1.3
Bacillus cereus 7 1.8
Staphylococcus aureus 2 0.5
Parasite — Cyclospora cayetanensis 8 2.0
Toxic agent 9 2.3
Chemical agent 2 0.5
Other agent 7 1.8
Unknown agent 82 20.9
Total 394 100.4
* More than one agent can be reported per outbreak.
> The denominator is the number of outbreaks that identified an environ-
mental antecedent.
M.M. Holst et al.
Table 2
Foodborne outbreak contributing factors, National Environmental Assessment
Reporting System, 2017-2019
Journal of Food Protection 87 (2024) 100293
Table 3
Foodborne outbreak environmental antecedents, National Environmental
Assessment Reporting System, 2017-2019
n % of
outbreaks”
(n = 393)
Contamination of food with a foodborne illness agent*
Toxic substance part of the tissue 12 3.1
Poisonous substance intentionally/deliberately added 0 0.0
Poisonous substance accidentally/inadvertently added 3 0.8
Addition of excessive quantities of ingredients that are toxic 1 0.3
in large amounts
Toxic container 0 0.0
Contaminated raw product—food was intended to be 20 5.1
consumed after a kill step
Contaminated raw product—food was intended to be 32 8.1
consumed raw or undercooked/underprocessed
Foods originating from sources shown to be contaminated or 2 0.5
polluted
Cross-contamination of ingredients 56 14.2
Bare-hand contact by a food worker who is suspected tobe 56 14.2
infectious
Glove-hand contact by a food worker who is suspected to be 23 5.9
infectious
Other mode of contamination (excluding cross- 96 24.4
contamination) by a food worker who is suspected to be
infectious
Foods contaminated by non-food worker who is suspected to 8 2.0
be infectious
Storage in contaminated environment 7 1.8
Other source of contamination 28 7.1
Proliferation or growth of microbial agents in food
(increase in number of bacteria or the production of
toxins)"
Food preparation practices that support proliferation of 25 6.4
pathogens
No attempt was made to control the temperature of 15 3.8
implicated food or the length of time food was out of
temperature control
Improper adherence of approved plan to use time asa public 12 3.1
health control
Improper cold holding due to malfunctioning refrigeration 20 5.1
equipment
Improper cold holding due to an improper procedure or 15 3.8
protocol
Improper hot holding due to malfunctioning equipment 1 0.3
Improper hot holding due to improper procedure or protocol 15 3.8
Improper/slow cooling 40 10.2
Prolonged cold storage 3 0.8
Inadequate modified atmosphere packaging 0 0.0
Inadequate processing 10) 0.0
Other situations that promote or allow microbial growth or 6 1.5
toxin production
Survival of foodborne illness agents after a process, such
as cooking, that should have eliminated or reduced
them*
Insufficient time and/or temperature during cooking/heat 24 6.1
processing
Insufficient time and/or temperature during reheating 9 2.3
Insufficient time and/or temperature control during freezing 0 0.0
Insufficient or improper use of chemical processes designed 1 0.3
for pathogen destruction
Other process failures that permit the pathogen to survive 7 1.8
* More than one contributing factor can be reported per outbreak.
> The denominator is the number of outbreaks that identified a contributing
factor.
ally, lack of food safety culture was identified more often for Sal-
monella than for Clostridium perfringens (52.8% vs. 36.0%).
All three types of outbreaks had equipment antecedents identified,
but again, the proportion differed by etiologic agent. More often, the
two types of bacterial outbreaks, compared to norovirus outbreaks,
had improperly used equipment identified as an antecedent (9.4%
and 12.0% vs. 1.3%) (Table 4). Similarly, more often Clostridium per-
Antecedents* n % of % of
antecedents’ Outbreaks‘
(n = 1,430) (n = 393)
People (n = 964)
Lack of oversight of employees/ 350 24.5 89.1
enforcement of policies
Lack of training of employees on specific 291 20.3 74.0
processes
Lack of a food safety culture/attitude 226 15.8 57.5
towards food safety
Low/insufficient staffing 38 2.7 9.7
High turnover of employees or 31 2.2 7.9
management
Language barrier between management 28 2.0 7.1
and employees
Equipment (n = 124)
Equipment is improperly used 35 2.4 8.9
Insufficient capacity of equipment 36 2.5 9.2
Poor facility layout 24 1.7 6.1
Lack of preventative maintenance on 15 1.0 3.8
equipment
Improperly sized or installed equipment 14 1.0 3.6
for the facility
Economics (n = 85)
Lack of sick leave or other financial 68 4.7 17.3
incentives to adhere to good practices
Lack of needed supplies for the operation 11 0.8 2.8
of the restaurant
Lack of reinvestment in the restaurant 6 0.4 1.5
Process (n = 192)
Employees or managers are not following 98 6.8 24.9
the facility's process
Insufficient process to mitigate the 94 6.6 23.9
hazard
Food (n = 18)
Food not treated as time and temperature 18 1.3 4.6
control for safety
Other (n = 47) 47 3.3 12.0
Total 1430 100.0 --
* Outbreaks could have more than 1 environmental antecedent.
> The denominator is the number of environmental antecedents reported for
all outbreaks that reported at least one environmental antecedent.
© The denominator is the number of outbreaks that reported an environ-
mental antecedent.
fringens outbreaks, compared to norovirus outbreaks, had insufficient
equipment capacity identified as an antecedent (28.0% vs. 3.2%).
Lack of sick leave was identified as an antecedent for all three types
of outbreaks but was more often identified for norovirus outbreaks
than for the two types of bacterial outbreaks (26.3% vs. 9.4% and
4.0%) (Table 4). On the other hand, insufficient process to mitigate
hazards was identified more often for the two types of bacterial out-
breaks than for norovirus outbreaks (22.6% and 36.0% vs. 8.3%).
Outbreak antecedents by contributing factors. The three most
common contributing factors fell into the contamination category—
other mode of contamination by a suspected infectious worker,
cross-contamination of ingredients, and bare-hand contact by a sus-
pected infectious worker (Table 5). The three most common antece-
dents for the top three contributing factors were the people
antecedents of lack of oversight of employees (79.2%, 71.4%,
76.8%, respectively), lack of training of employees (51.0%, 62.5%,
and 66.1%), and lack of food safety culture (31.3%, 55.4%, 53.6%).
However, the two antecedents of lack of employee training and lack
of food safety culture were identified more often for the contributing
factors of cross-contamination of ingredients and bare-hand contact
M.M. Holst et al.
Journal of Food Protection 87 (2024) 100293
Table 4
Foodborne outbreak environmental antecedents by etiologic agent, National Environmental Assessment Reporting System, 2017-2019*
Antecedent Norovirus Salmonella Clostridium perfringens
n % of outbreaks” n % of outbreaks” n % of outbreaks”
(n = 156) (nm = 53) (n = 25)
People
Lack of training of employees on specific processes 80 51.3 29 54.7 14 56.0
Lack of oversight of employees/ enforcement of policies 123 78.8 32 60.4 12 48.0
High turnover of employees or management 7 45 4 7.5 0 0.0
Low/insufficient staffing 22 14.1 2 3.8 1 4.0
Lack of a food safety culture/ attitude towards food safety 61 39.1 28 52.8 9 36.0
Language barrier between management and employees 3 1.9 3 5.7 1 4.0
Equipment
Insufficient capacity of equipment (not enough equipment for the 5 3.2 4 7.5 7 28.0
processes)
Equipment is improperly used 2 1.3 5 9.4 3 12.0
Lack of preventative maintenance on equipment 1 0.6 4 7.5 1 4.0
Improperly sized or installed equipment for the facility 4 2.6 2 3.8 0 0.0
Poor facility layout 5 3.2 7. 13.2 1 4.0
Economics
Lack of reinvestment in the restaurant 0 0.0 2 3.8 2 8.0
Lack of sick leave or other financial incentives to adhere to good 41 26.3 5 9.4 1 4.0
practices
Lack of needed supplies for the operation of the restaurant 4 2.6 1 1.9 1 4.0
Process
Insufficient process to mitigate the hazard 13 8.3 12 22.6 9 36.0
Employees or managers are not following the facility’s process 41 26.3 12 22.6 5 20.0
Food
Food not treated as time and temperature control for safety 0 0.0 3 5.7 2 8.0
Other 13 8.3 4 7.5 4 16.0
Total 425 - 159 — 73 =
* Outbreaks could have more than 1 agent and environmental antecedent.
> The denominator is the number of outbreaks that reported the agent (confirmed or suspected).
by a suspected infectious worker than for other mode of contamination
by a suspected infectious worker (62.5%, 66.1% vs. 51.0%; 55.4% and
53.6% vs. 31.3%).
The equipment antecedent of poor facility layout was identified
more often for cross-contamination of ingredients than for the two
contributing factors associated with suspected infectious workers
(12.5% vs. 4.2% and 1.8%) (Table 5). On the other hand, the eco-
nomics antecedent of lack of sick leave was more often identified for
the two contributing factors of suspected infectious worker than for
cross- contamination of ingredients (30.2% and 25.0%, vs. 5.4%). Sim-
ilarly, the people antecedent of low or insufficient staffing was identi-
fied more often for bare-hand contact by a suspected infectious worker
than for cross contamination of ingredients (14.3% vs. 5.4%).
Variation by year. Norovirus and Clostridium perfringens outbreaks
slightly decreased over time (54.5%, 48.7%, and 48.7%; 9.1%, 8.4%,
and 7.0%), while Salmonella outbreaks increased slightly (15.6%,
17.6%, and 17.4%) (Table 6). The contributing factors of other mode
of contamination by a suspected infectious worker and bare-hand con-
tact by a suspected infectious worker decreased over time (33.0%,
22.4%, and 21.6%; and 20.5%, 13.8%, and 11.1%). Lastly, the antece-
dent of lack of employee oversight increased over time (85.2%, 81.6%,
and 98.7%).
Discussion
People, lack of oversight. The three most common outbreak ante-
cedents identified by investigators were in the people category: lack of
oversight of employees, lack of training of employees, and lack of food
safety culture. Lack of a food safety culture is defined as the shared val-
ues, beliefs and norms that affect mind-set and behavior toward food
safety in an organization (Yiannis, 2009). These findings highlight
the critical role that employees play in restaurant food safety. The
most common antecedents were observed in norovirus, Salmonella,
and Clostridium perfringens outbreaks, indicating that these antecedents
support both viral and bacterial outbreaks. However, the antecedent of
lack of oversight of employees was identified much more often (>25
percentage points) for norovirus outbreaks than for the two types of
bacterial outbreaks. This suggests a particularly strong association
between lack of oversight of employees and norovirus outbreaks.
Foodborne norovirus outbreaks are more often associated with ill
employees contaminating food than are bacterial outbreaks (Hall
et al., 2012). Indeed, most foodborne norovirus outbreaks are associ-
ated with ill employees (Hall et al., 2012). Restaurant managers are
responsible for preventing employees who are ill with foodborne ill-
ness symptoms from working (Food and Drug Administration, 2022).
Our data suggest that managerial failure to exclude ill employees from
working is a key antecedent to norovirus outbreaks.
People, lack of sick leave. Similarly, lack of sick leave for employ-
ees was identified as an antecedent more often for norovirus outbreaks
(>18 percentage points) than for Salmonella and Clostridium perfrin-
gens outbreaks. This antecedent was also identified more often for
the two suspected infectious worker contributing factors. Given that
ill employees are more often associated with norovirus outbreaks than
with bacterial outbreaks, lack of sick leave as an antecedent to noro-
virus outbreaks and to contributing factors related to ill employees is
not surprising. Ill employees may not feel they can lose pay; thus, they
work while ill and transmit their illness to customers through the food
they contaminate. This finding is supported by other research showing
that financial issues, such as lack of sick leave and loss of shifts, are
cited by employees as reasons for working while ill (Carpenter et al.,
2013; Sumner et al., 2011; Norton et al., 2015). Research also shows
that mandated paid sick leave reduced instances of employees working
while ill (Schneider, 2020). Restaurants can take other steps to man-
M.M. Holst et al.
Table 5
Journal of Food Protection 87 (2024) 100293
Foodborne outbreak environmental antecedents by contributing factor, National Environmental Assessment Reporting System, 2017-2019*
Other mode of
Cross-contamination of Bare-hand contact by a
contamination by suspected ingredients suspected infectious worker
infectious worker
n % of outbreaks? n % of outbreaks” n %of outbreaks”
(n = 96) (n = 56) (n = 56)
People
Lack of training of employees on specific processes 49 51.0 35 62.5 37 66.1
Lack of oversight of employees/ enforcement of policies 76 79.2 40 71.4 43 76.8
High turnover of employees or management 3 3.1 5 8.9 4 7.1
Low/insufficient staffing 11 #115 3 5.4 8 14.3
Lack of a food safety culture/ attitude towards food safety 30 31.3 31 55.4 30 53.6
Language barrier between management and employees 6 6.3 4 7.1 1 1.8
Equipment
Insufficient capacity of equipment (not enough equipment for the 2 2A 6 10.7 2 3.6
processes)
Equipment is improperly used 1 1.0 5 8.9 1 1.8
Lack of preventative maintenance on equipment 0 0.0 2 3.6 1 1.8
Improperly sized or installed equipment for the facility 1 1.0 1 1.8 2 3.6
Poor facility layout 4 4.2 7 12.5 1 1.8
Economics
Lack of reinvestment in the restaurant 0 0.0 2 3.6 0 0.0
Lack of sick leave or other financial incentives to adhere to good 29 30.2 3 5.4 14 25.0
practices
Lack of needed supplies for the operation of the restaurant 0 0.0 1 1.8 3 5.4
Process
Insufficient process to mitigate the hazard 6 6.3 7 12.5 6 10.7
Employees or managers are not following the facility’s process 30 31.3 11 19.6 10 17.9
Food
Food not treated as time and temperature control for safety 0 0.0 1 1.8 0 0.0
Other 6 6.3 1 1.8 3 5.4
Total
* Outbreaks could have more than 1 contributing factor and environmental antecedent.
Table 6
Outbreak etiologic agents, contributing factors, and environmental antecedents by outbreak year, National Environmental Assessment Reporting System, 2017-2019*
2017 (n = 88) 2018 (mn = 152) 2019 (n = 153)
Etiologic agents” n % n % n %
Norovirus 42 54.5 58 48.7 56 48.7
Salmonella 12 15.6 21 17.6 20 17.4
Clostridium perfringens 7 9.1 10 8.4 8 7.0
Contributing factors©
Other contamination by a suspected infectious worker 29 33.0 34 22.4 33 21.6
Cross-contamination of ingredients 11 12.5 23 15,1 22 14.4
Bare-hand contact by a suspected infectious worker 18 20.5 21 13.8 17 11.1
Environmental antecedents
Lack of employee oversight/enforcement of policies 75 85.2 124 81.6 151 98.7
Lack of employee training 64 72.7 111 73.0 116 75.8
Lack of a food safety culture/attitude towards food safety 55 62.5 83 54.6 88 57.5
* Outbreaks could have more than 1 agent, contributing factor, and environmental antecedent.
> The denominator is the number of outbreaks that reported an agent (confirmed or suspected). 2017: n = 77; 2018: n = 119; 2019: n = 115.
© The denominator is the number of outbreaks that reported a contributing factor and environmental antecedent. 2017: n = 88; 2018:n = 152; 2019: n = 153.
age ill employees. For example, they can create written policies,
address reasons why employees work while ill, and create schedules
for when an employee is ill (Centers for Disease Control and
Prevention, 2022d).
Active managerial control. The top three antecedents (lack of
oversight of employees, lack of training of employees, lack of food
safety culture) and other people antecedents, such as lack of sick leave,
are heavily influenced by retail food establishment managers. Active
managerial control is the purposeful incorporation of specific actions
or procedures by industry management into the operation of their
business to attain control over foodborne illness risk factors. Active
managerial control can be used to encourage proper food safety prac-
tices (Food and Drug Administration, 2022). Some state and local
health departments provide an active managerial control toolkit or
resource center to assist food establishments in promoting and imple-
menting this concept in their operations (Alexander-Leeder & Gzebb,
2023; Maricopa County Department of Public Health, 2023). State
and local health departments have also encouraged food establish-
ments to develop and adopt active managerial control in their opera-
tions through incentive programs. Regulators indicated this
innovative strategy has been successful as they observed fewer viola-
tions in establishments resulting in fewer required inspections by the
M.M. Holst et al.
health department (Retail Food Safety Regulatory Association
Collaborative, 2023).
Equipment. We found that equipment-related antecedents were
more common for bacterial outbreaks than norovirus outbreaks. Res-
taurants typically rely on equipment for temperature control (e.g.,
walk-in coolers for cold holding, bain-maries for hot holding)
(McCabe-Sellers & Beattie, 2004). When this equipment fails or is used
improperly, bacterial pathogens survive and proliferate in food. For
example, Wittry et al. found that a common cause of Clostridium per-
fringens outbreaks is the use of hot-holding equipment that is not large
enough for the establishment’s operational demand (Wittry et al.,
2022). Our finding highlights the importance of using the proper type
of equipment and using the equipment properly to prevent bacterial
outbreaks.
Poor facility layout. The antecedent of poor facility layout was
identified more often with the contributing factor of cross-
contamination than with contributing factors related to ill employees.
Poor facility layout, possibly due to a lack of space or poor design, can
support ingredient cross-contamination. For example, a meat prepara-
tion area immediately adjacent to a salad preparation area could lead
to raw meat juices contaminating the salad preparation area and ingre-
dients. To prevent ingredient cross-contamination due to poor facility
layout, the Food and Drug Administration (FDA) recommends that
restaurants systematically identify their risks and develop plans for
mitigating those risks (Food and Drug Administration, 2022). Ideally,
these risks are identified during a construction plan review using haz-
ard analysis critical control point (HACCP) principles as a tool to
design safe facility layouts (Conference for Food Protection, 2016).
HACCP plans are recommended by the FDA, endorsed by most state
and local health departments, and are one of the best ways to mitigate
risks in a food establishment (Center for Food Safety and Applied
Nutrition, 2006).
Variations by year. There are some variations of etiologic agents,
contributing factors, and antecedents by year, which could be
explained by advanced laboratory testing methods and a push for
increased food safety. Norovirus outbreaks decreased while Salmonella
outbreaks slightly increased. This change could be due to a wider use
of whole genome sequencing (WGS). WGS provides a faster, more
accurate detection of bacteria (e.g., Salmonella), which may have pre-
viously been labeled as unknown (Centers for Disease Control and
Prevention, 2022e; Rounds, et al., 2020). Contributing factors related
to ill food workers decreased from 2017 to 2019. The FDA Risk Factor
Study data from 1998 to 2009 showed that compliance for no bare-
hand contact with ready-to-eat foods increased over the 10-year study
(Food and Drug Administration, 2010), which are actions that prevent
food contamination. While this study shows similar results, more
research is needed to determine what drives the decrease in bare-
hand contact with ready-to-eat foods. Over the past decade, CDC
and FDA research findings have focused on improving these food
safety practices to prevent norovirus contamination in retail food
establishments (Kambhampati et al., 2016; Hoover et al., 2020;
Centers for Disease Control and Prevention, 2019).
Limitations. There are a few limitations to this study. NEARS is a
voluntary reporting system and although the reporting sites are geo-
graphically diverse, the data may not be representative of all food-
borne outbreaks. The number of outbreaks at each site is likely
underreported because health departments do not detect or investigate
all outbreaks. Another limitation is the variability in investigation
practices across health departments due to different jurisdictional poli-
cies and trainings. Identification of antecedents is based on the inves-
tigator’s judgment and these judgments may vary.
The findings from this study provide valuable and novel informa-
tion about antecedents to foodborne outbreaks. The most common
antecedents to foodborne illness outbreaks we identified (lack of
employee training, lack of employee oversight, and lack of food safety
culture) are heavily influenced by restaurant management, who can
Journal of Food Protection 87 (2024) 100293
exercise active managerial control to mitigate these antecedents.
Establishment management can work to implement active managerial
control in their establishments to help ensure effective oversight and
training for employees. There are many resources, from FDA and var-
ious health departments across the United States, available to health
departments to assist establishments in exercising active managerial
control (Food and Drug Administration, 2022; Alexander-Leeder &
Gzebb, 2023; Maricopa County Department of Public Health, 2023).
Interventions to address common root causes of outbreaks could focus
on people as root causes and managerial leadership to improve food
safety in an establishment (Kramer et al., 2023; Lee et al., 2021). Iden-
tifying antecedents during investigations is essential for understanding
the outbreak’s root cause and implementing sustainable corrective
actions to stop the immediate outbreak and future outbreaks. Health
departments are encouraged to conduct a thorough environmental
assessment and identify the root cause of outbreaks to prevent future
outbreaks.
CRediT authorship contribution statement
Meghan M. Holst: Conceptualization, Formal analysis, Methodol-
ogy, Resources, Writing — original draft, Writing — review & editing.
Sabrina Salinas: Conceptualization, Data curation, Investigation,
Writing — review & editing. Waimon T. Tellier: Conceptualization,
Data curation, Investigation, Writing — review & editing. Beth C. Wit-
try: Conceptualization, Supervision, Writing — review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
This publication is based, in part, on data collected and provided by
the Centers for Disease Control and Prevention's (CDC) Environmental
Health Specialists Network (EHS-Net), which is supported by a CDC
grant award funded under RFA-EH-15-001. We thank the NEARS site
staff who collected and entered their outbreak data. The findings
and conclusions in this report are those of the authors and do not nec-
essarily represent the views of CDC or the Agency for Toxic Substances
and Disease Registry.
References
Alexander-Leeder, O., & Gzebb, M. (2023). Active managerial control: Implementation
and insights. Journal of Environmental Health, 86, 40-42.
Bryan, F. (1978). Factors that contribute to outbreaks of foodborne disease. Journal of
Food Protection, 41, 816-827. https://doi.org/10.4315/0362-028X-41.10.816.
Carpenter, L. R., Green, A. L., Norton, D. M., Frick, R., Tobin-D’Angelo, M., Reimann, D.
W., Blade, H., Nicholas, D. C., Egan, J. S., Everstine, K., Brown, L. G., & Le, B.
(2013). Food worker experiences with and beliefs about working while ill. Journal of
Food Protection, 76, 2146-2154. https://doi.org/10.4315/0362-028X.JFP-13-128.
Centers for Disease Control and Prevention. (2015). Guide to Confirming an Etiology in
Foodborne Disease Outbreak. Retrieved May 18, 2023, from https://www.
cdc.gov/foodsafety/outbreaks/investigating-outbreaks/confirming diagnosis.html.
Centers for Disease Control and Prevention. (2019). Preventing Norovirus Outbreaks.
Retrieved May 19, 2023, from https://www.cdc.gov/vitalsigns/norovirus/index.
html.
Centers for Disease Control and Prevention. (2022a). Environmental Assessment
Definitions. Retrieved May 18, 2023, from https://www.cdc.gov/nceh/ehs/nears/
eadefinitions.htm#:~:text = Environmental%20Antecedents%20%E2%80%93%
20Why%20contributing%20factors, worker%20was%20working%20while%20sick.
Centers for Disease Control and Prevention. (2022b). National Environmental
Assessment Reporting System (NEARS). Retrieved May 18, 2023, from https://
www.cdc.gov/nceh/ehs/nears/index.htm.
Centers for Disease Control and Prevention. (2022c). What are Environmental
Assessments? Retrieved May 24, 2023, from https://www.cdc.gov/nceh/ehs/
nears/environmental-assessment.htm
Centers for Disease Control and Prevention. (2022d). Restaurants Can Manage Sick
Workers to Help Prevent Outbreaks. Retrieved October 23, 2023, from https://
M.M. Holst et al.
www.cdc.gov/nceh/ehs/ehsnet/plain_ language/restaurants-can-manage-sick-
workers.html
Centers for Disease Control and Prevention. (2022e). Whole Genome Sequencing.
Retrieved January 15, 2024, from https://www.cdc.gov/pulsenet/pathogens/wgs.
html
Centers for Disease Control and Prevention. (2023). What are Contributing Factors?
Retrieved May 18, 2023, from https://www.cdc.gov/nceh/ehs/nears/what-are-
contributing-factors.htm
Conference for Food Protection. (2016). Food Establishment Plan Review Manual.
Retrieved January 31, 2024, from http://www.foodprotect.org/media/guide/2016-
plan-review-manual.pdf
Center for Food Safety and Applied Nutrition. (2006). Managing food safety: A manual
for the voluntary use of HACCP principles for operators of food service and retail
establishments. Retrieved January 31, 2024, from https://www.fda.gov/media/
71976/download
Dewey-Mattia, D., Manikonda, K., Hall, A. J., Wise, M. E., & Crowe, S. J. (2018).
Surveillance for foodborne disease outbreaks — United States, 2009-2015. Morbidity
and Mortality Weekly Report Surveillance Summaries, 67, 1-11.
Firestone, M. J., Hoelzer, K., Hedberg, C., Conroy, C. A., & Guzewich, J. J. (2018).
Leveraging current opportunities to communicate lessons learned from root cause
analysis to prevent foodborne illness outbreaks. Food Protection Trends, 38, 134-138.
Food and Drug Administration. (2022a). The 2022 Food Code. Retrieved May 22, 2023,
from https://www.fda.gov/media/164194/download
Food and Drug Administration. (2010). FDA Trend Analysis Report on the Occurrence of
Foodborne Illness Risk Factors in Selected Institutional Foodservice, Restaurant, and
Retail Food Store Facility Types (1998 — 2008). Retrieved January 15, 2024, from
https://www.fda.gov/media/157225/download?attachment
Freeland, A. L., Masters, M. M., Nicholas, D., Kramer, A. K., & Brown, L. G. (2019).
Facilitators and barriers to conducting environmental assessments for food
establishment outbreaks, National Environmental Assessment Reporting System,
2014-2016. Journal of Environmental Health, 81, 24-28.
Hall, A. J., Eisenbart, V. G., Etingue, A. L., Gould, H. L., Lopman, B. A., & Parashar, U. D.
(2012). Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008.
Emerging Infectious Diseases, 18, 1566-1573. https://doi.org/10.3201/
eid1810.120833.
Hoover, E. R., Hedeen, N., Freeland, A., Kambhampati, A., Dewey-Mattia, D., Scott, K.,
Hall, A., & Brown, L. (2020). Restaurant policies and practices related to norovirus
outbreak size and duration. Journal of Food Protection, 83, 1607-1618. https://doi.
org/10.4315/JFP-20-102.
Kambhampati, A., Shioda, K., Gould, L. H., Sharp, D., Brown, L. G., Parashar, U. D., &
Hall, A. J. (2016). A state-by-state assessment of food service regulations for
prevention of norovirus outbreaks. Journal of Food Protection, 79, 1527-1536.
Kramer, A., Hoover, E. R., Hedeen, N., DiPrete, L., Tuttle, J., Irving, D. J., Viveiros, B.,
Nicholas, D., Monroy, J., Moritz, E., & Brown, L. (2023). Development of an
empirically derived measure of food safety culture in restaurants. Journal of Food
Protection, 86, 100043. https://doi.org/10.1016/j.jfp.2023.100043.
Lee, J. C., Daraba, A., Voidarou, C., Rozos, G., Enshasy, H. A. E., & Varzakas, T. (2021).
Implementation of food safety management systems along with other management
tools (HAZOP, FMEA, Ishikawa, Pareto). The Case Study of Listeria monocytogenes
and Correlation with Microbiological Criteria. Foods, 10, 2169. https://doi.org/
10.3390/foods10092169.
Lipcsei, L. E., Brown, L. G., Coleman, E. W., Kramer, A., Masters, M., Wittry, B. C., Reed,
K., & Radke, V. J. (2019). Foodborne illness outbreaks at retail establishments -
national environmental assessment reporting system, 16 State and local health
Journal of Food Protection 87 (2024) 100293
departments, 2014-2016. Morbidity and Mortality Weekly Report Surveillance
Summaries, 68, 1-20. https://doi.org/10.15585/mmwr.ss6801al1.
Maricopa County Department of Public Health. (2023). English AMC Toolbox. Retrieved
December 15, 2023, from https://www.maricopa.gov/4533/English-AMC-Toolbox
Matis, B., McKelvey, W., O’Halloran, D., Stavinsky, F., & Wong, M. (2017). Using the
national environmental assessment reporting system to enhance foodborne illness
outbreak investigations in New York City restaurants. Journal of Environmental
Health, 79, 46-48.
McCabe-Sellers, B. J., & Beattie, S. E. (2004). Food safety: Emerging trends in foodborne
illness surveillance and prevention. Journal of the American Dietetic Association, 104,
1708-1717. https://doi.org/10.1016/j.jada.2004.08.028.
Moritz, E. D., Ebrahim-Zadeh, S. D., Wittry, B., Holst, M. M., Daise, B., Zern, A., Taylor,
T., Kramer, A., & Brown, L. G. (2023). Foodborne illness outbreaks at retail food
establishments — National environmental assessment reporting system, 25 State and
Local Health Departments, 2017-2019. Morbidity and Mortality Weekly Report
Surveillance Summaries, 72, 1-11. https://doi.org/10.15585/mmwr.ss7206a1.
Norton, D. M., Brown, L. G., Frick, R., Carpenter, L. R., Green, A. L., Tobin-D’Angelo, M.,
Reimann, D. W., Blade, H., Nicholas, D. C., Egan, J. S., & Everstine, K. (2015).
Managerial practices regarding workers working while ill. Journal of Food Protection,
78, 187-195. https://doi.org/10.4315/0362-028X.JFP-14-134.
Retail Food Safety Regulatory Association Collaborative. (2023). Active managerial
control incentive programs: Examples from jurisdictions leading the way. Retrieved
January 15, 2024, from https://www.retailfoodsafetycollaborative.org/tools/
active-managerial-control-incentive-programs- examples-from-jurisdictions-
leading-the-way/
Rounds, J. M., Taylor, A. J., Eikmeier, D., Nichols, M. M., Lappi, V., Wirth, S. E., Boxrud,
D. J., Smith, K. E. & Medus, C. (2020). Prospective Salmonella Enteritidis
surveillance and outbreak detection using whole genome sequencing, Minnesota
2015-2017. Epidemiology and _ Infection, 148. https://doi.org/10.1017/
$0950268820001272.
Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauwxe, R. V., Widdowson, M., Roy, S. L.,
Jones, J. L., & Griffin, P. M. (2011). Foodborne illness acquired in the United States
—Major pathogens. Emerging Infectious Diseases, 17, 7-15. https://doi.org/10.3201/
eid1701.p11101.
Schneider, D. (2020). Paid sick leave in Washington State: Evidence on employee
outcomes, 2016-2018. American Journal of Public Health, 110, 449-504. https://doi.
org/10.2105/AJPH.2019.305481.
Selman, C. A., & Guzewich, J. J. (2014). Public health measures: Environmental
assessment in outbreak investigations Retrieved June 15, 2023, from. Encyclopedia
of Food Safety, 4, 98-106.
Sumner, S., Brown, L. G., Frick, R., Stone, C., Carpenter, L. R., Bushnell, L., Nicholas, D.,
Mack, J., Blade, H., Tobin-D’Angelo, M., Everstine, K., & the Environmental Health
Specialists Network Working Group (2011). Factors associated with food workers
working while experiencing vomiting or diarrhea. Journal of Food Protection, 74,
215-220. https://doi.org/10.4315/0362-028X.JFP-10-108.
Weingold, S. E., Guzewich, J. J., & Fudala, J. K. (1994). Use of foodborne disease data
for HACCP risk assessment. Journal of Food Protection, 57, 820-830. https://doi.org/
10.4315/0362-028X-57.9.820.
Wittry, B. C., Holst, M. M., Anderburg, J., & Hedeen, N. (2022). Operational antecedents
associated with Clostridium perfringens outbreaks in retail food establishments,
United States, 2015-2018. Foodborne Pathogens and Disease, 19, 209-216. https://
doi.org/10.1089/fpd.2021.0068.
Yiannis, F. (2009). Food safety culture: Creating a behavior-based food safety management
system. Springer Science & Business Media.
Live Music
Archive
Librivox
Free Audio
Metropolitan Museum
Cleveland
Museum of Art
Internet
Arcade
Console Living Room
Open Library
American
Libraries
TV News
Understanding
9/11