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. 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.