CDC-Data-2025/attachments/HolstEA_djvu.txt

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: ows6@cdc.gov (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. 


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