Source: OHIO STATE UNIVERSITY submitted to
ENHANCING MICROBIAL FOOD SAFETY BY RISK ANALYSIS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1001930
Grant No.
(N/A)
Project No.
OHO01324-MRF
Proposal No.
(N/A)
Multistate No.
S-1056
Program Code
(N/A)
Project Start Date
Oct 16, 2014
Project End Date
Sep 30, 2018
Grant Year
(N/A)
Project Director
Ilic, SA.
Recipient Organization
OHIO STATE UNIVERSITY
1680 MADISON AVENUE
WOOSTER,OH 44691
Performing Department
College of Human Ecology
Non Technical Summary
It is well established that the heterogeneous distribution of pathogens in food makes studying the ecology of these pathogens difficult. There is a critical need in the fresh and processed food industries to thoroughly understand how these foods become contaminated with foodborne pathogens in the farm to fork continuum. The studies under this project will assess microbialfood safety risks in post-harvest food chain including processing, storage and transportation, retail, restaurants and common dining setting restaurants including food courts in shopping mall, hospital and university campuses and other consumer related food safety risks. New interventions to enhance food safety will be tested and validated. Based on the findingscience-based recommendations will be developed and prevent and mitigate food safety hazards. The findings will be translated for retailer and foodservice stakeholders and consumers.
Animal Health Component
0%
Research Effort Categories
Basic
(N/A)
Applied
100%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
71214991100100%
Goals / Objectives
Risk Assessment: Assess food safety risks in agriculture systems Risk Management: Develop science-based interventions to prevent and mitigate food safety threats Risk Communication: Communicate food safety messages to stakeholders
Project Methods
A combination of basic and applied science questions will be addressed using laboratory experiments and epidemiological investigations.Food and Environmental Samples: Food commodities will be obtained from processors restaurants orpurchased from local retailers or distributors. Samples will be stored at appropriate temperatures prior to use. Time between obtaining the food and experimental use will be minimized. Commercially appropriate varieties will be utilized.Environmental swabs will be obtained from the restaurants with market-style setting on campus, hospitals and shopping malls. Samples will be stored on ice and transported to the laboratory for processing. Time between obtaining the swabs and experimental use will be minimized.Pathogens: Salmonella spp., Shiga toxin producing Escherichia coli (STEC), Listeria spp., Clostridium spp., Staphylococcus spp., and Enterococcus spp. will be investigated.Strains that have been associated with outbreaks from the commodity of interest will be used whenever possible. If not possible, other significant pathogenic strains will be selected and several have been modified to produce florescent compounds, allowing enhanced detection from food matrixes. The modifications will allow, when necessary, easy identification of the inoculated strains in the presence of high levels of background microflora.Inoculation. Frozen stock cultures of bacterial strains are typically stored in glycerol stock solutions at -80°C. Prior to use strains are streaked onto non-selective media supplemented with selective agents as appropriate. Inocula may be prepared from plate or broth cultures, and may or may not be washed prior to use. Appropriate carrier media will be used for inoculations at volumes, levels and methods typical for the commodity being evaluated. Standard methods will also be used to create viral or parasitic inocula. Methods for inoculation of food commodities will vary, as required, to best mimic standard commodity specific criteria and the specific hypothesis-based research questions being addressed.Recovery of Pathogens from Inoculated Samples. Sample sizes, buffering solutions, and maceration methods will vary depending upon commodity and experiment-specific requirements. Enumeration of bacterial pathogens following serial dilutions by standard plating techniques onto selective and non-selective media, Most Probable Number techniques or by more sophisticated molecular techniques commonly used. When samples fall below the limit of detection standard enrichment protocols (FDA BAM or others) will be followed. The collection of quantitative data will be performed whenever possible.Recovery of Pathogens from Environmental and Uninoculated Food Sources: Sampling methods to recover pathogens from the environment and foods will vary depending upon the sampling scheme and source as appropriate for the experimental design of the experiment. Frequency of pathogen isolation and the concentration of pathogens identified. When appropriate, concentration techniques may be used to evaluate larger than typical sample volumes/weights and enrichment techniques used to evaluate samples when low numbers of cells are present.Risk Communication: specific risk education materials will be designed for stakeholders and extension educators. The content will be based on translated findings and the data analysis. Messages and the design will be chosen appropriately to facilitate knowledge transfer. Technical background for each communication tool will be developed containing evidence based rationale and justifications. The innovative messages will be designed with the appropriate use of colors, wording, graphics, and visuals aids.

Progress 10/16/14 to 09/30/18

Outputs
Target Audience:• Food handlers in in market style restaurants. • Consumers in retail and restaurants with common dining areas • Retail and food service stakeholders. • General consumer population and populations at risk • Food safety policy makers in foodservice industry. • Other researchers. • Extension educators, field specialist and other extension personnel Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Graduate and undergraduate students were trained in the area of microbial testing, epidemiology and basic research relatedto food safety. Students were involved in intervention research and worked closely with human subjects. Students receivedtraining in extension and improved skills that they can effectively communicate with different stakeholders. The collected datawill be used toward the completion of a master theses. Three graduate students, and one undergraduate student weresent to international food safety conferences to present their work and for professional development. How have the results been disseminated to communities of interest?The knowledge gained was communicated to stakeholders and is expected to enhance food safety in MSR and reduce risk offoodborne illnesses linked to foodservice. The results from intervention research were presented to Ohio public healhprofessionals and foodservice inspectors. These generatedpublications that will benefit consumers, research community and other stakeholders infoodservice industry. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Consumers and employees in market-style restaurants (MSR) were surveyed and observed to determine the most importantfactors that affect food safety behaviors in food courts. In a mixed methods approach, usingmultiple methods: surveys, observations, and microbial testing, this study assessed and contrasted food safetyperceptions among food handlers and consumers, their self-reported and observed practices,and the microbial status of inanimate surfaces in common dining areas of university foodcourts. Our findings identify gaps between perceptions of the importance of surface and handsanitation and the actual sanitation practices. The indicator bacterial loads on dining areasurfaces in university food courts, including consumer cell phones, are also identified. Food safety researchers, professionals, and foodservice managers are provided with ways todevelop effective risk communication programs. Food courts are popular dining platform in most universities in the United States. However, insufficiently skilled part-time studentemployees, self-service and shared dining environment, and the low-risk food safety perception among young adult consumer population create an increased risk of cross-contamination and foodborne illnesses in the setting. In a mixed methods approach, using surveys, observations, and microbial testing, this study assessed and contrasted food safety perceptions and self-reported practices among 100 food handlers and 295 consumers, observed practices among 34 food handlers and 149 consumers, and the microbial status of 391 inanimate surfaces and 60 consumer cell phones in common dining areas at university food courts.Our findings identify gaps between perceptions of the importance for surface and hand sanitation (weighted means from 4.15 to 4.91, 5-point Likert scale) and the actual sanitation practices (observed hand sanitation followed by only 0.9% and 1.6% transactions of food handlers and consumers, respectively). The contamination indicators were oftenfound on dining area surfaces over the period of one year (generic E. coli on 11.9% salad bar/salad bar utensils, 9.8% food serving counters, and 3.3% of consumer cell phones; 79.0% samples containing >104 CFU/cm2). Further, an examination of food safety behaviors of consumers and employees at university food courts shows that consumers' food safety practices vary depending on gender, observed ethnicity and party size, while none of those factors was significant for employees.Using a smartphone-based observation technique, a total of 149 consumers and 34 employees were observed at three food courts at a mid-western university in the USA. The observational tool recorded 30 sequential transactions of each individual, allowing researchers to identify the compliance rate to the rubric. Both descriptive statistics and multivariate analysis of variance were used for data analysis. Our study found a low compliance rate of food safety practices among consumers and employees at university food courts. Consumers' food safety practices varied depending on gender, observed ethnicity and party size, while none of those factors was significant for employees. Specifically, females, Caucasians, and lone diners showed higher non-compliance rates than those of males, non-Caucasians and group diners. The results of the study raise the pressing needs of developing effective risk communication strategies at university food courts for both consumers and employees in order to reduce the potential risk of foodborne illness outbreaks. University food courts are not only major foodservice operations for on-campus populations as well as off-campus visitors and the local public, but also the presence of shared dining area pertains the potential risk of foodborne illnesses. However, lack of attention has been paid to the food safety issues at university food courts, and especially food safety behaviors of consumers. Our studies extended the knowledge of previous food safety literature by adopting a smartphone-based observation technique and developing a rubric customized for consumers and employees at university food courts.The findings collected in the studies reported here resulted in direct recommendations for improved procedures in foodservice and in particular for university dining. Our surveys, observations and microbial tests showed that handwashing is not practiced in university food courts by employees or consumers. We showed that several services in joint dining facilities contained indicators of fecal contamination. The strategies to ensure safety of food in foodservice in university food courts have to include adoption of certain quality assurance systems. Suggested strategies include the testing of ATP bioluminescence as a tool of keep contact surfaces clean in university foodservice. This would be more effective comparing to current visual assessment recommended by the Food Code. The implementation of the sanitation programs, standard sanitation operating procedures (SSOP), and Hazard Analysis and Critical Control Point (HACCP) have been shown to be effective tools to ensure food safety in school foodserviceand may be effective in the university settings as well. The food courts are at every university in the US, as well as hospital, airports and shopping malls. The findings of this study will impact millions of consumers that eat at food courts.

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2019 Citation: Assessment of Food Safety at University Food Courts Using Survey, Observation, and Microbial Testing FOODCONT-D-18-02622


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:• Food handlers in in market style restaurants. • Consumers in retail and restaurants with common dining areas • Retail and food service stakeholders. • General consumer population and populations at risk • Food safety policy makers in foodservice industry. • Other researchers. • Extension educators, field specialist and other extension personnel Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Graduate and undergraduate students were trained in the area of microbial testing, epidemiology and basic research related to food safety. Students were involved in intervention research and worked closely with human subjects. Students received training in extension and improved skills that they can effectively communicate with different stakeholders. The collected data will be used toward the completion of two master theses. One graduate and two undergraduate students were sent to an international food safety conference to present the work and for professional development. How have the results been disseminated to communities of interest?The knowledge gained was communicated to stakeholders and is expected to enhance food safety in MSR and reduce risk of foodborne illnesses linked to foodservice. The results from intervention research were presented at the national campulobacter symposium. fact-sheets arein preparation. These research activities will generate publications that will benefit consumers, research community and other stakeholders in foodservice industry. Findings were presented at seminars, and food safety meeting and the manuscripts are in preparation. What do you plan to do during the next reporting period to accomplish the goals? Complete the data analusysand submit one more manuscript. Create fact sheets to target the consumers at risk Use the data to apply for further funding to implement interventions to improve hygiene of inanimate surfaces in market

Impacts
What was accomplished under these goals? Assess food safety risks in agriculture systems: Consumers and employees in market-style restaurants (MSR) were surveyed and observed to determine the most important factors that affect food safety behaviors in food courts. We assesed (1) food handlers' and consumers' self-reported perceptions, practices, and food safety culture; (2) observed food handling and hand hygiene practices during food preparation, serving and consumption; and (3) level of surface contamination with human pathogens (and indicators) in self-serving and common dining areas in university food courts. Further, based on the microbial results, we identified the differences in risk perception among consumers and actual food safety handling practices related to food contact surfaces in food courts. The data was previously collected in three locations using observations and surveys was analyzed using STATA and SPSS statistical packages. We assessed the concentration of human pathogens indicators on surfaces in the food court in three locations over a one year period. E. coli was isolated from surfaced that have direct contact with consumer hands as week as food contact surfaces. We assessed cross-contamination rates of E. coli O157 and Salmonella from most common surfaces to food and vice versa. Observed food safety practices of consumers (N= 149; 51 females, 56% white) at university food courts (n= 3) yielded a total of 4,486 transactions. Consumers most often ate alone (52%). Overall, 3,309 actions (73.8%) were identified as the behaviors that require hand sanitation. Of those, the actual hand sanitation practices were observed in only 103 (3.1%) actions. Specifically, the observed consumers frequently touched/handled potentially unsanitary objects with bare hands including: electronic device such as cell phones (n= 471 actions), surface/table (n= 448), bottled/cup beverage (n= 359), condiments (n= 56), chairs (n= 12), and counter (n= 1). In addition to education, the future interventions on prevention of cross-contamination and behavior change that will lead to actual safe food-handling practices. One manuscript was published and another one is preparation.? Risk Management: Develop science-based interventions to prevent and mitigate food safety threats Food safety knowledge, behaviors, attitudes, perceptions and subjective norms among parents of children age 1-9 was assessed. The food safety education intervention was designed and implemented in 161 participants to improve behaviors in preparation and handling of foods, primarily chicken in order to reduce Campylobacter infections. Two different education interventions were implemented: i) traditional education relying on systematic information processing among participant, and ii) social media intervention using heuristic information processing. Both types of interventions lasted for 6 weeks, with lessons delivered weekly. The data was collected before the intervention, after each lesson and after the treatments were completed. The data was analyzed and the manuscript is in preparation. The participants were on average 36 ± 8.0 years old parents of children up to 10, and prepared poultry for their children. Campylobacter awareness increased in both groups after interventions: before intervention 66.2% knew nothing or little about pathogen and overall increase by 54% was observed in both groups (P<0.001). Understanding of the risk increased for both groups, however the increase was not significant. Participant rated their own knowledge higher after interventions: 57.73 ± 21.88 before out of 100 and 79.63 ± 12.53 after;P<0.05. There was no difference in their perception on how much information they need to make safe decisions. The concern over the disease due to contaminated poultry increased (P<0.05) in both groups. The understanding of importance also increased (P< 0.05), but attitude outcomes varied in two groups. Perceived behavioral control decreased in social media group. Attitudes toward food safety improved only in social media group. Comparisons with base line group and additional scales will allow for more complete conclusions about the two interventions, however the tageted social media intervention was shown to be more effective in producing behavior change in this population.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Her, E., Seo, S., Choi, J., Pool, V. & Ilic, S. (2017). Observed food safety behaviors among consumers and employees in university food courts. British Food Journal, 119(7), 1619-1632.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Rodriguez-Palacios, A., Ilic, S., & LeJeune, J. T. (2017). Food Indwelling Clostridium difficile in Naturally Contaminated Household Meals: Data for Expanded Risk Mathematical Predictions. Infection Control & Hospital Epidemiology, 38(4), 509-510.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: H Paden, I Hatsu, M Lustberg, C Grenade, K Kane, K Mo, S Ilic Factors Associated with Food Safety Behaviors in Cancer Patients Seeking Treatment The FASEB Journal 31 (1 Supplement), 168.2-168.2


Progress 10/01/15 to 09/30/16

Outputs
Target Audience: Food handlers in in market style restaurants. Consumers in retail and restaurants with common dining areas Retail and food service stakeholders. General consumer population and populations at risk Food safety policy makers in foodservice industry. Other researchers. Extension educators, field specialist and other extension personnel. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Graduate and undergraduate students were trained in the area of microbial testing, epidemiology and basic research related to food safety. Students received training in extension and improved skills that they can effectively communicate with different stakeholders. The collected data will be used toward the completion of Master's thesis. Three graduate students were sent to an international food safety conference to present the work and for professional development. How have the results been disseminated to communities of interest?The knowledge gained was communicated to stakeholders and is expected to enhance food safety in MSR and reduce risk of foodborne illnesses linked to foodservice. These research activities will generate publications that will benefit consumers, research community and other stakeholders in foodservice industry. Findings were presented at seminars, andfood safety meeting and the manuscripts are in preparation. What do you plan to do during the next reporting period to accomplish the goals? Complete and submit one more manuscript. • Create fact sheets to target the consumers in food courts and other market style restaurants • Use the data to apply for further funding to implement interventions to improve hygiene of inanimate surfaces in market

Impacts
What was accomplished under these goals? Assess food safety risks in agriculture systems: Food safety behaviors and perceptions among consumers and employees in market-style restaurants (MSR). We recently assessed food safety behaviors of consumers and employees by observing the practices in market style restaurants. The data collected in three locations using observations and surveys was analysed using STATA and SPSS statistical packages. We assessed the concentration of human pathogens indicators on surfaces in the food court in three location over aone year period. E. coli was isolated from surfaced that have direct contact with consumer hands as wekk as foodcontact surfaces. We assessed cross-contamination rates of E. coli O157 and Salmonella from most commom surfaces to food and vice versa. Manuscripts are in preparation

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2016 Citation: Observed Food Safety Behaviors among Consumers and Employees in University Food Courts, British Food Journal - Manuscript ID BFJ-10-2016-0472


Progress 10/16/14 to 09/30/15

Outputs
Target Audience: Food handlers in in market style restaurants. Consumers in retail and restaurants with common dining areas Retail and food service stakeholders. General consumer population and populations at risk. Food safety policy makers in foodservice industry. Other researchers. Extension educators, field specialist and other extension personnel. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Several graduate and undergraduate students and postdoctoral fellows were trained in the area of microbial testing, epidemiology and basic research related to food safety. Students received training in extension and improved skills that they can effectively communicate with different stakeholders. The collected data will be used toward the completion of Master's thesis. Three graduate students were sent to an international food safety conference to present the work and for professional development. How have the results been disseminated to communities of interest?The knowledge gained was communicated to stakeholders and is expected to enhance food safety in MSR andreduce risk of foodborne illnesses linked to foodservice. These research activities will generatepublications that will benefit consumers, research community and other stakeholders in foodservice industry.Findings were presented at the IAFP, international food safety meeting and the manuscripts are in preparation. What do you plan to do during the next reporting period to accomplish the goals? Complete and submit two manuscripts. Create fact sheets to target the consumers in market style restaurants Use the data to apply for further fundingto implement interventions to improve hygiene of inanimate surfaces in market style restaurants

Impacts
What was accomplished under these goals? Assess food safety risks in agriculture systems: Food safety behaviors and perceptions among consumers and employees in market-style restaurants (MSR). We recently assessed food safety behaviors of consumers and employees by observing the practices in market style restaurants. The data was collected in three locations. Observation tool was designed in Qualitrix and used on smart phones. 101 consumers and 34 employees were observed and 30 transactions were recorded in a sequence of observed action, the object of the action, and observed hand sanitization practice. We found that only 3% of practices that require hand sanitation were followed by cleaning hands with napkins. The behaviors requiring hand sanitization were more commonly observed when consumers were eating with other people and men were more often engaging in sanitization practices than women. For employees, only 1% of practices requiring hand sanitation were followed by changing gloves. The findings reveal poor food safety practices of consumers and employees, raising the needs of developing effective risk communication strategies for MSR. We assessed the perception of food safety among consumers in MSR using surveys. Data was collected from 300 participants and analyzed. Preliminary findings were presented at the IAFP, international food safety conference. The majority of MSR consumers believed they were not responsible for food safety and almost all thought that owner of each restaurant has the responsibly to ensure food safety. Food handlers or other patrons were perceived to be the most important sources of contamination with human pathogens. Wiping tables is currently not a common practice among MRS consumers but the majority would very likely do it if sanitary wipes were provided. The majority would likely be enticed to use hand and surface sanitizers if they saw other patrons engaging in that behavior. The data was collected on the prevalence and concentration of pathogen indicators and pathogens on surfaces in three MRS over one year period. E. coli was isolated from surfaced that have direct contact with consumer hands as wekk as food-contact surfaces Manuscripts are in preparation

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Poster: Observed Food Safety Behaviors among Consumers and Employees in Market-Style Restaurants, 2015, Eun-Sol Her, Victor Pool, Jihee Choi1, Sanja Ilic, and Soobin Seo, International Association of Food Protection, Portland OR
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Poster: Consumer Perceptions Beliefs, and Practices Associated with Food Safety in Market-style Restaurants, 2015, Victor Pool, Eun-Sol Her, Jihee Choi, Soobin Seo, and Sanja Ilic, International Association of Food Protection, Portland OR