ABSTRACT

Previous studies have shown that higher ambient air temperature is associated with increased incidence of gastrointestinal illnesses, possibly as a result of leaving potentially hazardous food in the temperature danger zone for too long. However, little is known about the effect of hot weather on restaurant practices to maintain safe food temperatures. We examined hot weather impacts on restaurant food safety violations and operations in New York City using quantitative and qualitative methods. We used data from 64,661 inspections conducted among 29,614 restaurants during May to September, 2011 to 2015. We used Poisson time-series regression to estimate the cumulative relative risk (CRR) of temperature-related food safety violations across a range of daily maximum temperature (13 to 40°C [56 to 104°F]) over a lag of 0 to 3 days. We present CRRs for an increase in daily maximum temperature from the median (28°C [82°F]) to the 95th percentile (34°C [93°F]) values. Maximum temperature increased the risk of violations for cold food holding above 5°C (41°F) (CRR, 1.19; 95% CI, 1.14, 1.25) and insufficient refrigerated or hot holding equipment (CRR, 2.37; 95% CI, 2.02, 2.79). We also conducted focus groups among restaurant owners and managers to aid interpretation of findings and identify challenges or knowledge gaps that prevent hot weather preparedness. Focus group participants cited refrigeration issues as a common problem during hot weather. Participants expressed the need for more guidance on hot weather and power outages to be delivered concisely. Our findings suggest that hotter temperatures may compromise cold and hot food holding, possibly by straining refrigeration or other equipment. The findings have public health implications because holding potentially hazardous foods in the temperature danger zone allows foodborne pathogens to proliferate and increases risk for foodborne illness. Distribution of simple guidelines that can be easily accessed during emergencies could help restaurants respond better.

One in six Americans is affected by a foodborne illness each year (22). Whereas most cases of foodborne illness are relatively minor, the Centers for Disease Control and Prevention estimates that 128,000 hospitalizations and 3,000 deaths related to foodborne diseases occur annually (22). Several studies have shown that higher ambient air temperature is associated with an increased incidence of gastrointestinal infections (3, 14), including salmonellosis and campylobacteriosis, which are among the most common foodborne diseases (22). Potentially hazardous food held at ambient temperatures between 4 and 60°C (40 to 140°F) can result in the proliferation of foodborne pathogens (24), many of which flourish under warmer conditions (17).

In the United States, approximately 60% of reported foodborne disease outbreaks occurred in the restaurant setting in 2015 (4). Inadequate cold holding temperatures and slow cooling of potentially hazardous food, as well as failure to adhere to using time as a public health control are some of the contributing factors of foodborne illness in restaurants (1, 9). In New York City (NYC), restaurants must comply with NYC Health Code regulations, which include time and temperature control of potentially hazardous food, as described in the 2013 U.S. Food and Drug Administration Food Code (20, 26). We hypothesize that extreme heat may affect a restaurant's ability to effectively manage temperature and time control. For example, warmer temperatures may compromise refrigeration, thus making it harder to maintain temperatures for cold holding and the cooling of prepared foods. Hot weather may also require additional monitoring of ice in the ice bath because it melts faster. As the average temperature rises due to climate change, and extreme heat events occur more frequently (11), restaurants may face additional challenges to maintain safe temperatures during holding and cooling of potentially hazardous food.

In addition to the direct impact of hot weather on temperature control of potentially hazardous food, it can also increase the demand for electricity, which can lead to power outages (21). Power outages may compromise refrigeration and, thus, provide an opportunity for increased food spoilage and foodborne illness. In NYC, the number of emergency department visits for diarrhea increased by 70% during the August 2003 Northeast outage, possibly due to consumption of spoiled food at home and in restaurants (15). Increases in the sales of antidiarrheal medication and worker absenteeism because of gastrointestinal illnesses were also observed. Power outages, although usually very small in size, are a common occurrence in NYC (6). Power outages may also become more frequent as power grids are strained by more high-demand days during hot weather and more severe storms resulting from climate change (12).

Previous studies have focused on the associations between temperature or power outages and gastrointestinal illness among the general public (3, 14, 15). However, there is currently little knowledge of the effects of hot weather or power outages on restaurant food safety practices. The aim of this study was to understand potential weather-related impacts in restaurants by the use of regulatory inspection data. To better understand whether high temperature days impact food safety practices, we examined the relationship between daily maximum temperature and temperature-related food safety violations issued during routine inspections. We also conducted restaurant operator focus groups to aid interpretation of findings and identify challenges or knowledge gaps that prevent preparedness for hot weather and power outages. A better understanding of current risks can help inform food service establishments' preparedness for future warmer summers.

MATERIALS AND METHODS

Our study used NYC restaurant inspection data and meteorological data for a quantitative analysis of the impacts of temperature on food safety violations. We also recruited operators from restaurants identified in the inspection data for our qualitative assessment.

Restaurant inspection data

There are approximately 24,000 food service establishments operating in NYC on any given day (28). The NYC Department of Health and Mental Hygiene (DOHMH) is responsible for conducting inspections of food service establishments, which include full-service and take-out restaurants, delicatessens, and bars (20) (hereafter, referred to as “restaurants”). The NYC restaurant inspection program conducts initial unannounced inspections in all restaurants at least once a year to evaluate compliance with health code rules. Reinspections are conducted about a month later in restaurants that score 14 or more violation points. We limited this analysis to all initial inspections conducted during the May through September warm season from 2011 to 2015 (n = 69,963). The start time was selected to minimize any effects of the implementation of the NYC grading program, which began on 27 July 2010. We excluded inspections in restaurants with minimal on-site preparation of food, including bars that did not prepare food, concession stands, and restaurants that sold only bottled beverages, ice cream, gelato or yogurt, or nuts and other confectionaries, which resulted in 64,661 initial inspections in our final analytic sample. NYC initial inspection data used for this analysis included the restaurant name and location, information on whether the restaurant was independently owned or belonged to a chain, type of restaurant, date of inspection, total score at time of inspection, and scores for select violations.

Outcomes were NYC Health Code violations that could plausibly be associated with hot weather. Those included cold food items held above 5°C (41°F) except during necessary preparation, hot food items not held at or above 60°C (140°F), and no or insufficient refrigerated or hot holding equipment, which are grouped as one violation.

Meteorological data

The exposure was daily maximum temperature in NYC, which was obtained from the National Oceanic and Atmospheric Administration, National Centers for Environmental Information. Temperature monitoring at LaGuardia Airport was used for the study period (May to September, 2011 to 2015) because it had the most complete data and was highly correlated with the two other weather stations in NYC (16).

Statistical analysis

The unit of analysis is an inspection. The outcome is a citation of a temperature-related food safety violation on inspection. We computed crude rate ratios of violations given on hot days compared with cool days during the warm season using SAS version 9.4 (SAS Institute, Cary, NC). Hot days were defined as days on which the maximum temperature was greater than or equal to the 95th percentile of daily maximum temperature, and cool days were defined as days on which the maximum temperature was less than or equal to the median (50th percentile) during the study period.

We measured the association between short-term exposure to daily maximum temperature and violations using overdispersed Poisson time-series regression (8), which allowed us to control for temporal trends in citations of violations. The model included day of the week, holiday, and year, as well as the daily number of inspections to control for variation in the volume of inspections. The model additionally specified temperature lags distributed over 0 to 3 days because visual inspection of the associations with each violation suggested they were strongest in this period. The term “lag” refers to the delayed effect of the exposure (high temperature day) on the outcome (violation), so distributed lags represent the delayed effects of temperature over multiple days prior to when the violation was given. The shape of the distributed lag effects in relation to violations were fitted using the distributed lag nonlinear model (dlnm package) (7) for the statistical software R version 3.3.1 (R Core Team, Vienna, Austria). We used an unconstrained form for lags, which allows a different magnitude of impacts at each lag day's temperature, and we specified a functional form of natural splines with three degrees of freedom over the range of temperature, which allowed it flexibility to fit the data at each lag day.

Cumulative relative risks (CRRs) were estimated by summing the lag-specific contributions, each of which can have a different functional form of temperature. Using a backward perspective (7), the CRR represents the multiday effects of temperature experienced over 0 through 3 days prior to when the violation was given. We modeled the relationship with temperature on the continuous scale, but because of the nonlinear relationships, the estimated CRR had to be expressed at a specific (high) temperature compared with a reference (i.e., median) temperature (as opposed to a relative risk per a degree C increase, as would be possible for a linear relationship). We report CRR for an increase in daily maximum temperature from the median (normal warm season day) to the 95th percentile (hot warm season day) values.

Restaurant operator focus groups

The NYC DOHMH contracted with ICF International and Zebra Strategies to conduct two focus groups with restaurant owners and managers in winter 2017. We aimed to include owners and managers of small, independent restaurants that prepared much of their cold and hot menu items on site. We used the NYC inspection data described above to recruit participants from nonchain, full-service restaurants. Restaurants had to be currently operating and to have had at least two initial inspections during May through September between 2011 and 2015.

The two focus groups were divided into restaurants that performed the highest and the lowest during the study period. To assign a performance value to each restaurant, we averaged the total scores at the time of initial inspections for each restaurant. Higher scores indicate lower performance (19), so the top 20% of average points were defined as the lowest-performing restaurants and the bottom 20% of average points were defined as highest performing. We selected the top and bottom 20% as cutoffs to separate the lowest-performing restaurants from the highest-performing restaurants and to have a sufficient pool of restaurants to recruit operators from. Potential participants from each performance group were contacted by phone and were selected using a screener form to obtain a mix in race, ethnicity, gender, age, restaurant location, and years working for or owning the restaurant. We additionally aimed to include participants with higher levels of involvement in the supervision of the kitchen.

Focus group questions were designed to help interpret findings from the quantitative analysis and identify challenges or knowledge gaps that prevent hot weather and power outage preparedness. Discussions were led by a trained moderator who asked questions about practices to maintain cold foods at or below 5°C (41°F) and to cool hot foods during hot weather. We also included questions about experience and practices during prior power outages.

A total of 17 people, 8 in the higher-performing group and 9 in the lower-performing group, agreed to participate in the discussions. This is consistent with recommendations for focus group size of 6 to 10 people per discussion (18), which can capture a range of opinions while allowing for substantive dialogue with all participants. Each group session lasted 2 h. Both groups were recorded and transcribed. Multiple members of the study team observed the focus group sessions, reviewed the transcripts, and conducted qualitative evaluation to identify themes in each topic. The NYC DOHMH Institutional Review Board approved this study as exempt research.

RESULTS

Restaurant characteristics

We used data from 29,614 restaurants inspected during May to September, 2011 to 2015 (Table 1). Most restaurants were located in Manhattan (38%), and Staten Island had the fewest restaurants (4%), which reflects the geographic distribution of all NYC food service establishments. The majority were nonchain restaurants (90%). Less than half were quick-service restaurants (46%), followed by full-service restaurants (38%).

TABLE 1

Characteristics of restaurants inspected between May and September, 2011 to 2015

Characteristics of restaurants inspected between May and September, 2011 to 2015
Characteristics of restaurants inspected between May and September, 2011 to 2015

A total of 64,661 initial inspections were conducted during the study period. The median number of initial inspections per restaurant was 2 (range, 1 to 7). On average, 84.5 (SD, 59.1) initial inspections were conducted daily. Most temperature-related violations were issued for cold food holding above 5°C (41°F) (total, 29,254; daily mean ± SD, 38.2 ± 27.8), followed by hot food item held below 60°C (140°F) (13,499; 17.7 ± 13.2) and insufficient refrigeration or hot holding equipment (1,095; 1.4 ± 1.7).

Daily maximum temperature and food safety violations

The median maximum temperature during May to September, 2011 to 2015, was 28°C (82°F) (range, 13 to 40°C [56 to 104°F]). The 95th percentile of maximum temperature was 34°C (93°F). Violations for cold food holding and insufficient refrigerated or hot holding equipment were more likely to be cited on hot days compared with cool days (RR [95% CI], 1.27 [1.23 to 1.31] and 3.26 [2.72 to 3.91], respectively; Table 2).

TABLE 2

Crude RRs and 95% CIs for temperature-related food safety violations on hotter daysa

Crude RRs and 95% CIs for temperature-related food safety violations on hotter daysa
Crude RRs and 95% CIs for temperature-related food safety violations on hotter daysa

The modeled CRRs for cold food holding violations and insufficient refrigerated or hot holding equipment violations increased as temperature increased (Figs. 1 and 2). When we compared 34°C (93°F) days with 28°C (82°F) days, the CRRs of each violation were 1.19 (95% CI, 1.14, 1.25) and 2.37 (95% CI, 2.02, 2.79), respectively. The magnitude of CRRs for insufficient equipment at the highest temperature (40°C [104°F]) was substantial (CRR, 6.18; 95% CI, 3.27 to 11.69).

FIGURE 1

Estimated effects of daily maximum temperature on violations for cold food holding above 5°C (41°F). Cumulative relative risks and confidence intervals over lags distributed over 0 to 3 days were plotted for maximum temperature ranging from 16 to 40°C (60 to 104°F).

FIGURE 1

Estimated effects of daily maximum temperature on violations for cold food holding above 5°C (41°F). Cumulative relative risks and confidence intervals over lags distributed over 0 to 3 days were plotted for maximum temperature ranging from 16 to 40°C (60 to 104°F).

FIGURE 2

Estimated effects of daily maximum temperature on violations for insufficient refrigeration or hot holding equipment. Cumulative relative risks and confidence intervals over lags distributed over 0 to 3 days were plotted for maximum temperature ranging from 16 to 40°C (60 to 104°F).

FIGURE 2

Estimated effects of daily maximum temperature on violations for insufficient refrigeration or hot holding equipment. Cumulative relative risks and confidence intervals over lags distributed over 0 to 3 days were plotted for maximum temperature ranging from 16 to 40°C (60 to 104°F).

There was little evidence of an effect of 34°C (93°F) days on hot food holding violations compared with 28°C (82°F) days (CRR, 1.03; 95% CI, 0.96, 1.10). However, violation rates increased at temperatures greater than 35°C (95°F) (CRR at 36°C [96°F], 1.08; 95% CI, 0.96 to 1.21; Fig. 3) and temperatures below 25°C (80°F) (CRR at 18°C [64°F], 1.11; 95% CI, 1.01 to 1.21).

FIGURE 3

Estimated effects of daily maximum temperature on violations for hot food holding below 60°C (140°F). Cumulative relative risks and confidence intervals over lags distributed over 0 to 3 days were plotted for maximum temperature ranging from 16 to 40°C (60 to 104°F).

FIGURE 3

Estimated effects of daily maximum temperature on violations for hot food holding below 60°C (140°F). Cumulative relative risks and confidence intervals over lags distributed over 0 to 3 days were plotted for maximum temperature ranging from 16 to 40°C (60 to 104°F).

Restaurant operator focus groups

Approximately half of the focus group participants were men (n = 9, 53%) and 76% were white (n = 13). All participants reported owning or managing a full-service restaurant. Approximately half of the participants had worked for or owned their restaurant for more than 10 years (n = 8, 47%). Only five (29%) of the participants reported being solely responsible for running the kitchen, whereas the rest reported shared decision-making responsibilities. A majority of participants in both groups recognized customer health as a priority.

We asked participants about practices to ensure that potentially hazardous foods are kept below 5°C (41°F). Checking refrigerator thermometers was commonly mentioned by both higher and lower performers, although there was variation in how frequently these were checked. Three lower performers described challenges with deliveries arriving close to the lunch hour and mentioned that they spend their limited time ensuring that the bill is correct, rather than monitoring food temperature.

When asked how hot weather impacts daily operations, all operators cited frequent refrigerator malfunctions: “Refrigerators always break in the summer.” In response, members of both groups move food to more reliable refrigeration units or add ice to the refrigerators to keep temperatures low. Some higher performers additionally mentioned that they move food from the front to the back of the refrigerator and run the air conditioners to help the refrigerators run better; they also keep the refrigerator doors closed and keep minimal food in the refrigerators overnight. Among the lower performers, one participant explicitly described use of a thermometer to check refrigerator temperatures. Coolers, ice machines, and air conditioning were other types of equipment that were cited to frequently break down. One operator expressed concern about the maintenance of safe temperatures in delivery trucks and its effect on food safety. Another concern was the loss of food as a result of outages that occur overnight when the restaurant is not in operation and when the duration of the outage is not known.

Some operators described approved methods to assist cooling, including ice paddles and ice baths, constant stirring, and moving food from large to small containers. A couple of operators explicitly described starting the cooling process in ice before moving the food to the refrigerator. Knowledge of cooling time varied, and most operators did not describe monitoring the temperature over time. Operators said that cooling procedures did not change during hot weather, although one operator mentioned that food may take a little longer to cool and another described using more ice.

Not all restaurants hold warm foods, particularly those that prepare fresh meals or reheat portioned foods. None of the higher performers reported hot food holding problems during hot weather, but one operator suggested that blasting the air conditioner may make it harder to maintain safe hot holding temperature. An operator from the lower performing group suggested “attention and focus is more on keeping the things cold than keeping the things hot.”

Other hot weather impacts were identified from the focus groups. Some operators changed their menus during the summer to minimize foods that require heat, such as adding more salads or gazpachos. Both groups pointed out that the kitchen can get very hot during the summer, and participants reported that they encourage staff to stay hydrated and take breaks when it is hot.

Reasons for power outages experienced by some operators included neighboring construction, summertime conditions, wintertime salt on underground electrical cables, and Superstorm Sandy, a major coastal storm that hit New York City on 29 October 2012 (5). None had emergency plans, and all said they use “common sense” or “prior experiences” to handle power outages. The higher performers described tossing food out, although there was also effort to save food, particularly expensive meats and fish. One lower performer would throw food out if the outage was long, but there was generally greater emphasis on saving food, such as moving it to a freezer that might stay colder for longer. There was variation in knowledge of cutoff times for discarding food and a misconception in both groups that vegetarian establishments and vegetables in general are safer from hazards associated with food spoilage during an outage. There was inconsistent use of thermometers to check temperatures, and one operator mentioned using taste to determine whether food had spoiled. Both groups also sent food to other restaurants and noted that neighboring restaurants formed informal support networks and often provided assistance (such as space in refrigerators or ice) during times of crisis.

Participants from both groups expressed the need for more information and guidance delivered concisely. Participants suggested that it would be helpful to provide an explanation of the health and safety concerns behind the regulations with which they must comply. No participants from either group said they were aware of preparedness resources for hot weather, power outages, or other emergencies. However, both groups liked the idea of having emergency information in a checklist format and having this information readily available in an emergency.

DISCUSSION

Maximum temperature was positively associated with food safety violations primarily related to cold food holding above 5°C (41°F) and refrigerated or hot holding equipment. Focus group discussions provided specific examples of refrigeration problems during hot weather. Higher- and lower-performing operators described similar ways of responding to hot weather impacts on refrigeration, but there was inconsistent knowledge of food safety procedures during power outages. None of the operators had emergency plans for their restaurants, but many expressed interest in having guidance available during an event.

During hotter weather, refrigerators must work harder to keep food cold and are more likely to break down. Additionally, the warmer ambient temperature may cause the temperature in the refrigerator to rise faster as doors are opened and closed. Associations over three lag days suggest it may take time for refrigerator temperatures to noticeably rise, especially if restaurant operators are not consistently checking the temperature. This could potentially prevent operators from recognizing and responding promptly to breakdowns and possibly result in a cold holding violation if they happen to be inspected on these days.

We were not able to assess temperature effects on cooling violations because they are difficult to capture during routine inspection. However, discussions among the restaurant operators suggested that their cooling procedures were not changed during hotter weather. As observed in other studies (2, 10), many of the restaurant operators did not actively monitor temperature during the cooling process. Foods not monitored may be more likely to cool too slowly (23), and higher ambient temperatures could potentially exacerbate the problem.

Our quantitative findings pointed to a possible positive relationship between very high temperatures and hot holding violations. Holding hot foods below the recommended temperature can increase the risk of foodborne illness by allowing proliferation of foodborne pathogens (24). Focus group participants acknowledged how hot the kitchen can get during the summer, so it is possible that holding temperatures are lowered to minimize heat in the kitchen on very hot days. Although this was not specifically mentioned during brief discussion on the topic, one operator suggested that the greater focus is on keeping cold foods cold, so maintaining hot food holding temperatures might get overlooked.

Focus group discussions suggested that the restaurant operators manage refrigeration problems after issues arise, rather than take preventive action. Furthermore, restaurant operators did not have written plans for responding to hot weather or power outages, although many across both groups used practices recommended in standard emergency preparedness resources (25), such as placing ice in refrigerators to keep temperatures lower. Knowledge of how to ensure food safety during power outages was also limited, consistent with observations in the general population (13). Many operators liked the idea of having an easily accessible checklist of actions to take during a power outage, heat event, or other emergency. The strong community of restaurants mentioned during the discussion could provide additional resources during emergencies. As with other types of emergencies and communities, local networks and relationships may provide the quickest and most effective help during an emergency, assuming that nearby restaurants are not impacted and food transport follows safety guidelines (27).

This study had several limitations. The violations show a snapshot of restaurant operations at the time of the inspection and may not fully represent normal operations. Insufficient refrigerated or hot holding equipment were grouped as one violation, which makes it difficult to determine which was associated with temperature; however, we would not expect higher temperatures to directly affect hot holding equipment. These violations were also infrequent, which may have contributed to uncertainty in the effect estimates. There may also be more uncertainty around estimates than these results suggest because of limitations in our methods to adjust variance estimates to account for restaurants that had multiple inspections during the study period. We would expect true confidence intervals to be wider, but we would not expect a change in the point estimates.

The focus groups were not intended to be representative of all NYC restaurants and operators but, instead, were meant to be groups of individuals who are familiar with the operations of a restaurant. However, whereas we selected participants with greater responsibility in overseeing the kitchen, it is possible that not all operators were knowledgeable of operations and that perhaps other kitchen staff, such as chefs, would have been a more suitable, although harder to reach, group. Despite this limitation, the discussions generated a number of plausible explanations for our quantitative findings that would have been difficult to obtain using quantitative methods. In addition, the focus groups elucidated possible challenges and solutions for restaurants in response to warming temperatures and power outages.

Our findings suggest that increasing numbers of hot weather days and power outages associated with climate change are likely to increase food safety risks in restaurants. We have identified a number of public health actions to mitigate this risk. Operators should have an emergency plan in place with guidance on how to maintain safe food temperatures during hot weather or power outages. Restaurants should also have a preventive maintenance plan with a refrigeration company to ensure that their equipment is functioning properly all year round. At a minimum, a preventive maintenance visit in early June is essential. Encouraging use of high-efficiency refrigeration equipment can additionally reduce the strain on the power grid. An operator has several strategies to use to keep food at the appropriate temperature during the summer months, which include using a staging refrigerator so that the walk-ins remain closed most of the day, placing ice baths in the refrigerators, and most importantly, monitoring the temperature of all refrigeration and hot holding equipment at least every 3 to 4 h. Investment in temperature monitoring and quality refrigeration also makes economic sense because any food that has been out of temperature for an unknown period of time must be discarded. Reduction of the amount of heat generated in the kitchen may also be a beneficial approach to maintain temperature control of potentially hazardous foods and is an important way to keep safe working conditions for restaurant staff. Hot weather may also impact delivery truck temperatures, which could potentially exacerbate challenges in getting food safely into cold storage. Restaurant operators should schedule deliveries earlier or later in the day when the temperature is lower and should reject food that arrives out of temperature or on a nonrefrigerated truck. Distribution of simple, easily accessible guidelines on safely keeping and discarding food during hot weather or power outages could help restaurant operators better respond to these events and keep food and customers safe.

ACKNOWLEDGMENTS

We thank Melissa Wong and J. Bryan Jacobson for providing us with the NYC restaurant inspection data and analytic guidance; Beth Torin for informative discussions on the quantitative and qualitative analyses; Magda Desdunes for her assistance in focus group participant recruitment; and Nancy Jeffery for providing additional qualitative feedback on the focus group discussions. The research was supported by grant no. 60445 from NYSERDA and by grant no. 5UE1EH000757-02, funded by the Centers for Disease Control and Prevention. Its contents are solely the responsibility of the New York City Department of Health and Mental Hygiene and do not necessarily represent the official views of NYSERDA, the Centers for Disease Control and Prevention, or the Department of Health and Human Services.

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