ABSTRACT

At present, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has not been shown to be transmitted through food. Even so, the coronavirus disease 2019 (COVID-19) pandemic has changed how consumers view food and food safety. This study assessed consumer food safety practices during the COVID-19 pandemic using (i) surveys and (ii) online focus group discussions. From April to August 2020, five waves of surveys were distributed to an online U.S. consumer panel and screened to include only primary food preparers and grocery shoppers. The online focus groups were conducted via WebEx from May to July 2020. Focus group participants were recruited from the first wave of survey respondents. Both survey respondents and focus group participants reported higher levels of hand washing in response to the pandemic. However, survey participants' anticipated levels of hand washing after the pandemic decreased; some focus group participants noted that human nature “kicking in” could lead to lower levels of hand hygiene practice. For each of the 5 months, the surveys reported increased produce washing, both with water only and with water plus soap. Most focus group participants mentioned using water to wash their produce, but some reported using soap and even vinegar to “kill” the virus. Since consumers were worried that SARS-CoV-2 could survive on food, they started to mishandle food to address these concerns. However, this study also reported an increase in food thermometer use during the pandemic. Social determinants like gender, income, education, and age may have also influenced changes in levels of practice throughout the pandemic. The COVID-19 pandemic drove consumers to practice proper and improper food safety practices, which may or may not continue after the pandemic. This study's findings provide timely information to guide future food safety education and communication during health crises and pandemics.

HIGHLIGHTS
• The COVID-19 pandemic has influenced changes in consumer food handling practices.

• Consumers increased their frequency of proper food safety practices during the pandemic.

• Many consumers washed fruits and vegetables with soap during the pandemic.

• Social determinants like gender and income influenced some food handling practices.

The coronavirus disease 2019 (COVID-19) pandemic has affected how people think about food and food safety in the United States. According to the 2020 Food & Health Survey conducted by the International Food Information Council (IFIC) (35), COVID-19 was the top food safety issue for food handling and preparation in the United States. Almost half of Americans had concerns about food prepared outside the home, while 30% had concerns regarding meal preparation at home (35). Although severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has not been proven to be transmittable through food at the time of this article, concerns that the virus survives on raw foods of animal origin have persisted (57, 79).

During past pandemics, longitudinal survey studies assessed consumer risk perception and behavior (9, 20, 27). A previous study conducted during the 2009 H1N1 pandemic evaluated longitudinal trends in risk perceptions and vaccination intentions (27). Although many studies have evaluated consumer food safety knowledge and perceptions, few longitudinal studies have evaluated consumer food safety risk perceptions and practices during a pandemic. The available longitudinal studies evaluated food safety topics, including risk perceptions and behavioral changes during interventions (3, 45). Because of the lack of research related to consumer food handling practices during a pandemic, the present study utilized a longitudinal approach to assess consumer food handling practices that may have been impacted by the evolving COVID-19 pandemic.

While survey data indicate what is happening, focus group discussions can provide insight into why something is happening: researchers listen and collect qualitative data that include a range of opinions across several groups. Open-ended questions in a group setting allow participants to share their thoughts and feelings about an issue, product, or service (39). Previous studies on food safety have utilized focus groups as a method to collect consumer thoughts on food safety, food safety practices, and barriers to food safety (56, 67, 81). Longitudinal focus group discussions have also assessed changes in thoughts and practices over time (19, 29, 68). With technological advancements and the increased popularity of the Internet, online focus groups have become a popular research method (62, 76). Online focus groups overcome some of the challenges of face-to-face focus groups. Online focus group discussions allow participants to comfortably join the discussion from anywhere in the world, as long as they can access the Internet. This allows researchers to recruit a wider range of participants and reduce transportation costs (77). Research also suggests that the online environment provides participants with a subtle sense of anonymity since they are behind a screen, which allows them to discuss sensitive topics more openly (50, 82). Using online longitudinal focus groups is a novel approach in food safety research. The current study used online longitudinal focus group discussions to assess the changes in perceptions, attitudes, and practices of people in the United States in relation to food safety and the COVID-19 pandemic.

A mixed-method approach increases the validity of and confidence in the results, thereby addressing the shortcomings of using only quantitative or qualitative methods (33, 46). Published studies have used a mixed-method approach by combining survey data with data from interviews or focus group discussions to assess different consumer groups' food safety knowledge and risk perceptions (47, 56). The inclusion of both quantitative and qualitative methods can help researchers understand behaviors and perceptions, which can then assist in theory building or theory testing (63).

This study's objective was to assess food safety education needs and identify food handling behavior changes among consumers during a major pandemic. Researchers employed a longitudinal mixed-method approach using surveys and online focus group discussions to gain a comprehensive understanding of practices like hand hygiene, produce washing, and food thermometer use during the COVID-19 pandemic.

Research protocols were approved by the Institutional Review Board (IRB) before data collection began (IRB no. 2020-558).

### Survey pilot study

The researchers developed survey items and distributed surveys using convenience sampling to pilot test face validity. A total of 26 pilot test surveys were completed. In order to test for internal consistency of the different scales, a Cronbach alpha test was conducted on the piloted survey items, and the alpha ranged from 0.65 to 0.91 (53). A few items were added and revised based on respondents' suggestions.

### Survey longitudinal study

In order to assess the changes in risk perception and food safety behaviors, the survey was administered over 5 months. Each wave occurred once a month from April 2020 to August 2020. A longitudinal study is a research design that involves repeated observations of the same variables (e.g., people) over time. We were able to collect focus group discussion data among the same group of participants over 3 months. We were unable to collect survey data from the same exact people over time; however, we were able to make sure the participants were recruited from the same consumer panel through Qualtrics XM (Seattle, WA, and Provo, UT).

### Decline in postpandemic hand hygiene

Hand hygiene and proper hand washing was the earliest and most important recommendation that experts gave to consumers when the COVID-19 pandemic hit the United States (15, 78). In the present study, the survey data and focus groups confirmed an increase in hand washing during the pandemic compared with before the pandemic. This finding is similar to recent studies focused on hand hygiene and the COVID-19 pandemic and previous studies about the H1N1 pandemics (30, 55). The increase in hand washing during these health events may be due to the emphasis on this practice as a preventative measure for diseases in general (17). However, survey and focus group results showed a significant reduction in anticipated hand washing with soap and hand sanitizer use after the pandemic.

This decrease in proper hand hygiene throughout the pandemic and as anticipated after the pandemic may be attributed to people becoming less responsive to risks involved in decreased hand hygiene, or as focus group participants mentioned, human nature “kick[ing] in.” This phenomenon, coined “caution fatigue,” describes people reducing their vigilance in taking precautionary measures (38, 51). This lack of vigilance not only increases the risk of spreading SARS-CoV-2 but can cause the spread of other diseases as well. When assessing hand sanitizer use separately, some focus group participants were concerned it was harmful; this may be due to reports of harmful ingredients. In June 2020, the U.S. Food and Drug Administration warned against using certain alcohol-based hand sanitizers because they may contain ingredients like methanol, which may be toxic and cause adverse effects if used or ingested (73). Another reason for less hand sanitizer use might be the low availability of hand sanitizer during the pandemic (58).

Because a large percentage of foodborne disease outbreaks are caused by lack of hand hygiene, a decline in hand washing and hand sanitizing may cause an increase in consumers' risk of contracting a foodborne illness (10). Hand hygiene is an important component of food safety messages to ensure consumer safe food handling practices. Consumers should also be educated on the importance of hand hygiene not only for the pandemic but to prevent cross-contamination and foodborne diseases.

### Increased caution in food preparation during COVID-19

The COVID-19 pandemic has caused consumers to change their food handling practices. The survey and focus group results in the current study showed increased fruit and vegetable washing and food thermometer use by consumers during the pandemic. This is an indication that consumers are becoming more cautious when preparing foods during the pandemic. Although there is no evidence yet to prove that COVID-19 can be spread through food, consumers may worry about people touching their food, which can cause the food to be a fomite, or an inanimate object that can spread pathogens and infect humans (28). A previous study on the spread of norovirus on a houseboat found that fomites played a potential role in the contamination and outbreak of norovirus (37). The fear of food itself may also play a role in consumer food handling changes during the pandemic. A recent study noted a possible connection between frozen foods and the spread of SARS-CoV-2 (54). Although food handling was not explored thoroughly during past pandemics, consumer behavioral change and increased preventative measures were observed in response to these previous pandemics and health events (7, 20, 55). Because food safety was a major concern during COVID-19, consumers may be seeking more information and learning about food handling practices (34). A more recent study in China of the COVID-19 pandemic's impact on food safety knowledge in residents found that the pandemic may have also improved consumers' food safety knowledge and behavior (61).

Consumers implemented fruit and vegetable washing practices as a preventative measure against COVID-19. There may be a connection between produce washing and new COVID-19 cases in the United States. The present study reported that anticipated levels of produce washing after the pandemic with water only and water plus soap declined in August. This may be due to the declining case numbers by August 2020 (13, 18). Consumers might have been less afraid of contracting SARS-CoV-2 from their food because of the declining number of cases. Although water was the primary method used to wash produce, some focus group participants in this study reported using other techniques, like soap or vinegar, to clean their fruits and vegetables. A recent content analysis of food safety information in YouTube videos during the COVID-19 pandemic (June 2020) found that some people, including health care professionals, suggested that people should wash their fruits and vegetables with soap (66). The content analysis study also found that some people suggested this practice because it was the same as the recommended practice for proper hand washing. This dissemination of misinformation may be one reason consumers in the United States wash their produce with water plus soap instead of water only. Another recent study found an increase in calls to poison control centers about exposure to cleaners and disinfectants, which may be due to consumers using these products on food (26). Many experts warn against washing fruits and vegetables with anything but water only since detergents may not rinse off the produce, which can make consumers ill when the produce is ingested (71, 72).

Survey participants increased their food thermometer use in response to the pandemic, and focus group participants also mentioned using heat while cooking food to kill the virus. The increase in thermometer use during the pandemic may indicate that consumers have become more aware of food safety measures during the pandemic by connecting the safe food handling to killing the virus on food. The current survey also reported a significant increase in the use of thermometers in July compared with May. There are two potential factors that may contribute to this longitudinal change. There were higher numbers of new COVID-19 cases in the United States in July than in May, which may have influenced consumers to take extra precautions in July (16). Another possible reason may be connected to the outbreak of COVID-19 in Beijing, which was reported to be associated with imported salmon (4). The increasing number of people becoming ill from May to July and the raw-food–related outbreak news may have influenced consumers to take extra steps to make sure the virus is eliminated. Because the current study concluded there was an increase in food thermometer use, it is important to spread information on proper food thermometer techniques and correct endpoint temperatures (24). A previous study found that although most food workers understood the importance of using a food thermometer when cooking meat and poultry products, very few knew the endpoint temperature needed to ensure product safety (8).

Food safety experts and educators should be aware of heightened food safety concerns during major health events so that evidence-based, proper cleaning methods can be disseminated to consumers earlier during the pandemic so as to avoid consumers harming themselves with improper techniques like using soap to wash produce. Increased awareness of food safety practices is also beneficial to consumers and food safety educators, who should use this time during the pandemic and other similar health events to provide consumers with correct information while food safety attention levels have increased.

### Social determinants of health affecting food handling changes during COVID-19

Many demographic characteristics are social determinants of health, conditions that affect a wide range of health, functioning, and quality-of-life outcomes and risks (11). Exploring the impact of social determinants for consumer food handling practices can aid food safety and health experts to develop audience-targeted educational materials. Social determinants, including gender, income, education level, and age, were reported in the 5-month survey results.

Male respondents significantly changed their behavior in hand washing with soap compared with females (Table S3A to S3E). The difference between genders could be caused by the fact that males tended to have a lower compliance rate of hand washing with soap before the pandemic. The gender difference in hand washing was also reported in other studies. A recent Centers for Disease Control and Prevention study reported that men were less likely to remember to wash their hands than women during the COVID-19 pandemic (12). Previous studies also found that gender played a role in health engagement (22, 74). Ek's (22) study on the effect of gender on health information behavior found that being female was a strong predictor of being more involved and proactive in health-related issues compared with males. The lack of male involvement around health issues may be a reason for lower levels of hand washing before the pandemic. However, the pandemic resulted in males having a significantly greater change in washing hands with soap than females, which may indicate that the fear-inducing nature of the COVID-19 pandemic may have influenced males to make greater changes.

In most months, the responses indicated that those with over $50,000 in annual income had higher levels of hand washing with soap than those with incomes lower than this annual figure. In some months, the responses also displayed that those in this higher-income category were more likely to use a food thermometer more during the pandemic than those in the lower-income category. Previous studies have assessed food safety knowledge and practices of low-income groups (40, 75). A study by Wenrich et al. (75) found that many low-income adults in Pennsylvania had risky food practices and beliefs. These included being unaware of correct refrigeration temperatures, cross-contamination, and a lack of disinfection practices. Low-income individuals may have multiple barriers preventing safe food handling practices or the acquisition of food safety knowledge. These individuals may not have access to proper food safety courses due to distance, Internet availability, or insufficient funds to pay for such courses. An observational study also found that families making less than$1,000 per month were less likely to use cutting boards, paper towels, and soap (21, 67). Therefore, it is important to consider how some consumers may not have opportunities or access to information and resources due to their financial situation. A higher income can also allow consumers to have more food safety resources, such as thermometers and disinfectants, which are necessary to perform certain safe food handling practices. It has been shown that the pandemic had a major economic impact on the United States (31). With the decline in employment and earnings during the pandemic, those with lower income may be even less inclinced to practice safe food behaviors due to the barriers; they may be more focused on providing the essentials for themselves and their families.

Much like income, those with a bachelor's degree or higher had greater levels of hand washing with soap and thermometer use during the pandemic than those with lower education levels. Similar results were seen in a previous study where researchers assessed the food safety practices and risk perceptions of Mexican-Americans and found that those with a college degree or higher acknowledged that food thermometer use is important and hand washing was a method to reduce the risk of food poisoning (56). Another more recent study (32) on consumer perceptions of food safety found that those with higher education levels were more likely to own a food thermometer. People with higher educational degrees may be more likely to seek information and put preventative measures into practice.

Education also had an effect when assessed longitudinally. Those with higher education levels practiced washing produce with soap more in April, but the changes started to even out between education levels in June and July. This may be explained by the dissemination of false information earlier on during the pandemic and how those with higher education levels may have heard about it first. However, as more information about proper practices emerged, the levels of washing produce with soap declined as well. Food safety educators should find ways to reach people from all educational backgrounds during major health events like the COVID-19 pandemic and under normal circumstances.

Age played some role in consumers' preventative measures during the pandemic. The current survey results showed that, in some areas, older adults tended to be more careful with hand hygiene in response to the pandemic. These findings are similar to a previous health study where older adults (45 to 64 years old) were more engaged in diabetes risk reduction activities (1). However, this study also found that younger adults (<55 years old) had a significant increase in using thermometers in response to the pandemic. This contradicts previous studies where younger participants (<34 years old) had a lower usage of food thermometers and less knowledge on how to use one (6, 24, 49). This shift in behavior during the COVID-19 pandemic may be due to the increased awareness of food safety during this time. It also needs to be noted that the previous studies reported the age group of the participants as younger than 34 years old, while in the current survey, the younger participants referred to those who were younger than 55 years old. The differences could also be attributed to the age group differences between the studies.

Although this study was carefully planned and executed, there were some limitations. Respondents and participants may not accurately represent all consumers in the United States due to the online nature of the recruitment process. Some consumers may not have had access to the Internet, and those recruited may have had similar mindsets, as they came from the same panel. Because focus group participants volunteered to be a part of this study, they may have had stronger views on this topic as well. Dropping out or not showing up to focus group sessions are limitations that have been noted in previous longitudinal focus group studies (29, 44). Possible reasons for not joining or completing all three discussion sessions can be scheduling conflicts, emergencies, loss of interest, forgetting the appointment, or even connectivity issues with the online platform. Because the present study's participants lived in different time zones, there might have also been confusion about session appointment times.

Due to the limited number of questions allowed on the survey, questions about meal delivery and how consumers decided at which grocery stores to shop were not included in the survey. The questions in the survey were pilot tested for face validity; however, other validities were not examined. Furthermore, this study is based on self-reported behavior, not actual observation. Previous studies reported discrepancies between self-reported and actual food handling behaviors (8, 24). Future studies can evaluate consumers' safe food handling behavioral change via observation or other similar methods.

This study concludes that the COVID-19 pandemic has impacted consumer food safety handling practices in the United States. While some safe food handling practices increased, such as hand hygiene, washing produce with water, and food thermometer use, some potential mishandling practices identified may be due to the spread of misinformation, like washing produce with soap. It is critical to engage the public in learning about safe food handling practices earlier on during major health incidents, like the COVID-19 pandemic. More research needs to explore social determinants' impacts on behavioral change during a pandemic. This study's findings provide timely information to guide future food safety education and communication during health crises and pandemics.

We thank the following individuals for their expertise and assistance: Han Chen, Tressie Barrett, Juan Archila-Godínez, Ziyue Zhang, Cai Chen, Ishani Roychowdhury, Audra Brewer, and Rose Ernst.

Supplemental material associated with this article can be found online at: https://doi.org/10.4315/JFP-21-006.s1; https://doi.org/10.4315/JFP-21-006.s2

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