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Research Paper
PII: S0362-028X(24)00077-2
DOI: https://doi.org/10.1016/j.jfp.2024.100293
Reference: JFP 100293
Please cite this article as: Holst, M.M., Salinas, S., Tellier, W.T., Wittry, B.C., Environmental Antecedents of
Foodborne Illness Outbreaks, United States, 2017 – 2019, Journal of Food Protection (2024), doi: https://doi.org/
10.1016/j.jfp.2024.100293
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aCenters for Disease Control and Prevention, National Center for Environmental Health, 4770 Buford
Highway, Atlanta, Georgia, 30341, USA; bHarris County Public Health, Environmental Public Health, 1111
Fanin Street, Houston, 77002, USA; cWashington State Department of Health, Office of Communicable
Disease Epidemiology, 1610 NE 150th Street, Shoreline, WA. 98155, USA
Corresponding Author:
Meghan Holst
E-mail: ows6@cdc.gov
Abstract: Foodborne outbreak investigations often provide data for public health officials to determine
how the environment contributed to the outbreak and on how to prevent future outbreaks. State and
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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 – 2019, 24 jurisdictions
reported 1,430 antecedents from 393 outbreaks to the National Environmental Assessments Reporting
System. The most reported antecedents were lack of oversight of employees/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 employees 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
essential for understanding the outbreak’s root cause and implementing sustainable corrective actions to
stop the immediate outbreak and future outbreaks.
Keywords: Foodborne illness outbreak, root cause, environmental health, illness prevention,
environmental assessment, environmental antecedents
The Centers for Disease Control and Prevention (CDC) estimates that around 48 million
foodborne illnesses occur each year in the United 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 prevent sporadic cases of
foodborne illnesses.
State and local health departments are responsible for investigating 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 System (NEARS) is a CDC surveillance system through which some state and local
health departments voluntarily report data from their investigations of foodborne illness outbreaks at
retail food establishments (Centers for Disease Control and Prevention, 2022b). Specifically, 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 environment contributed to the
introduction or transmission of the agent that caused the outbreak (Centers for Disease Control and
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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 outbreak as contamination of food by an
ill employee, and the antecedent 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 contributing factors and antecedents
(Centers for Disease Control and Prevention, 2022a, Matis et al., 2017, Wittry et al., 2022). To contribute
to these goals, the current study presents data on the contributing factors and antecedents for outbreaks
reported to NEARS from 2017-2019.
Between 2017 and 2019, state and local health departments reported data to NEARS from 799
outbreak investigations with a suspected or confirmed foodborne agent. CDC defines a foodborne illness
outbreak as an incident in which two or more people experience a similar 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, Jefferson 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.
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(the inherent qualities of food prepared in establishments). Investigators can report multiple contributing
factors and antecedents for each outbreak.
We created the dataset for this study with SAS 9.3 statistical software (SAS Institute, Cary, NC),
then used Microsoft Excel to conduct descriptive analyses on the data. The analyses focused on outbreak
etiologic 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 disaggregated the antecedent data on
the most common outbreak etiologic agents, contributing factors, and year.
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
contamination 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 antecedents 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%) categories (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 process to mitigate hazard (23.9%).
Outbreak antecedents by etiologic agent. The three most common etiologic agents were the virus
norovirus, and the bacteria Salmonella 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%, respectively), 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%). Additionally, lack of food safety culture was identified more often for
Salmonella 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 perfringens 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
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4.0%) (Table 4). On the other hand, insufficient process to mitigate hazards was identified more often for
the two types of bacterial outbreaks 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 suspected infectious worker (Table 5). The
three most common antecedents 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 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 economics 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%). Similarly, the people antecedent of low
or insufficient staffing was identified 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 contact 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 antecedent 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 antecedents 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 values, 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 associated with ill employees (Hall et al., 2012). Restaurant
managers are responsible for preventing employees who are ill with foodborne illness symptoms from
working (Food and Drug Administration, 2022a). Our data suggest that managerial failure to exclude ill
employees from working is a key antecedent to norovirus outbreaks.
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People, lack of sick leave. Similarly, lack of sick leave for employees was identified as an
antecedent more often for norovirus outbreaks (>18 percentage points) than for Salmonella and
Clostridium perfringens 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 norovirus 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 manage 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 practices (Food and Drug Administration, 2022a). Some state and local
health departments provide an active managerial control toolkit or resource center to assist food
establishments in promoting and implementing 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 establishments to develop and adopt active managerial control in their
operations through incentive programs. Regulators indicated this innovative strategy has been successful
as they observed fewer violations in establishments resulting in fewer required inspections by the 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. Restaurants typically rely on equipment for temperature control
(e.g., walk-in coolers for cold holding, bain-maries for hot holding) (McCabe-Sellers et al., 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 perfringens 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 as the
contributing factor of ingredient cross-contamination than as 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 preparation area immediately adjacent to a salad preparation
area could lead to raw meat juices contaminating the salad preparation area and ingredients. To prevent
ingredient cross contamination due to poor facility layout, the FDA recommends that restaurants
systematically identify their risks and develop plans for mitigating those risks (Food and Drug
Administration, 2022a). Ideally, these risks are identified during a construction plan review using hazard
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
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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
environmental 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 previously 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 –
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), whare 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 geographically diverse, the data may not be representative of all
foodborne 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 policies and trainings.
Identification of antecedents is based on the investigator’s judgment and these judgments may vary.
The findings from this study provide valuable and novel information about antecedents to
foodborne outbreaks. The most common antecedent 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 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
various health departments across the United States, available to health departments to assist
establishments in exercising active managerial control (Food and Drug Administration, 2022a; 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). Identifying 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.
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
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collected and entered their outbreak data. The findings and conclusions in this report are those of the
authors and do not necessarily represent the views of CDC or the Agency for Toxic Substances and
Disease Registry.
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Table 1. Foodborne outbreak etiologic agents—National Environmental Assessment Reporting System,
2017–2029
Agenta n % of outbreaksb
(n=393)
Virus
Hepatitis A 2 0.5
Bacteria
14
Toxic agent 9 2.3
15
Table 2. Foodborne outbreak contributing factors, National Environmental Assessment Reporting System,
2017–2019
n % of
outbreaksb
(n=393)
Addition of excessive quantities of ingredients that are toxic in large amounts 1 0.3
Contaminated raw product—food was intended to be consumed after a kill step 20 5.1
16
Foods contaminated by non-food worker who is suspected to be infectious 8 2.0
No attempt was made to control the temperature of implicated food or the length 15 3.8
of time food was out of temperature control
Improper adherence of approved plan to use time as a public health control 12 3.1
Other situations that promote or allow microbial growth or toxin production 6 1.5
17
Survival of foodborne illness agents after a process, such as cooking, that should
have eliminated or reduced thema
18
Table 3. Foodborne outbreak environmental antecedents, National Environmental Assessment
Reporting System, 2017 – 2019
% of
% of
antecedentsb Outbreaksc
People (n=964)
Lack of a food safety culture/attitude towards food safety 226 15.8 57.5
Equipment (n=124)
19
Economics (n=85)
Lack of needed supplies for the operation of the restaurant 11 0.8 2.8
Process (n=192)
Employees or managers are not following the facility's process 98 6.8 24.9
Food (n=18)
Food not treated as time and temperature control for safety 18 1.3 4.6
bThe denominator is the number of environmental antecedents reported for all outbreaks that reported at least one
environmental antecedent
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Table 4. Foodborne outbreak environmental antecedents by etiologic agent, National Environmental
Assessment Reporting System, 2017 – 2019a
Clostridium
Antecedent Norovirus Salmonella perfringens
% of % of
% of outbreaksb outbreaksb outbreaksb
n (n=156) n (n=53) n (n=25)
People
21
Lack of a food safety culture/ attitude 61 39.1 28 52.8 9 36.0
towards food safety
Equipment
Economics
Process
22
Employees or managers are not 41 26.3 12 22.6 5 20.0
following the facility’s process
Food
bThe denominator is the number of outbreaks that reported the agent (confirmed or suspected)
23
Table 5. Foodborne outbreak environmental antecedents by contributing factor, National Environmental
Assessment Reporting System, 2017 – 2019a
Other mode of
contamination by Bare-hand contact by a
suspected infectious Cross-contamination suspected infectious
worker of ingredients worker
% of
% of outbreaksb outbreaksb % of outbreaksb
n (n=96) n (n=56) n (n=56)
People
Equipment
24
enough equipment for the
processes)
Economics
Process
facility’s process
Food
25
Food not treated as time and 0 0.0 1 1.8 0 0.0
temperature
Total
aOutbreaks could have more than 1 contributing factor and environmental antecedent
bThe denominator is the number of outbreaks that reported the contributing factor
Table 6. Outbreak etiologic agents, contributing factors, and environmental antecedents by outbreak
year, National Environmental Assessment Reporting System, 2017 – 2019a
Etiologic agentsb n % n % n %
Contributing factorsc
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Environmental antecedentsc
Lack of a food safety culture/attitude towards food safety 55 62.5 83 54.6 88 57.5
aOutbreaks could have more than 1 agent, contributing factor, and environmental antecedent
bThedenominator is the number of outbreaks that reported an agent (confirmed or suspected). 2017: n=77; 2018: n=119; 2019:
n=115
cThedenominator is the number of outbreaks that reported a contributing factor and environmental antecedent. 2017: n=88;
2018: n=152; 2019: n=153
Highlights
-People are the most common root cause of foodborne illness outbreaks.
-Active managerial control can be used to enforce management plans for ill workers.
Declaration of interests
☒ The authors declare that they have no known competing financial interests or personal relationships
that could have appeared to influence the work reported in this paper.
☐ The authors declare the following financial interests/personal relationships which may be considered
as potential competing interests:
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