NEHA June 2023 Journal of Environmental Health

ADVANCEMENT OF THE SCIENCE

and hands. Simulation experiments were designed to quantify transfer rates of phi 6 bacteriophage from fomites to hands. Microfiber towels had the lowest transfer rates in each group at high (10 7 PFU/cm 2 ) and low concentrations (10 3 PFU/cm 2 ) except from stainless steel at low concen- tration. These results are consistent with previous studies that found microfiber towels, along with cotton/cellulose towels, transferred significantly less virus com- pared with nonwoven and cotton terry bar towels (Gibson et al., 2012). At both high and low concentrations, hands have the highest phi 6 transfer rates for all surfaces; the exception was stainless steel at low phi 6 concentration, where it had the lowest transfer rate. The transfer rate from tabletops to hands at low phi 6 concentration was the highest observed in our experiment. These results would have the greatest impact on food service custom- ers, who come into contact with counter- tops and tabletops. A study by Choi et al. (2014) showed that nonfood contact sur- faces that customers interact with have the potential for cross-contamination. Their experiment focused on bacteria and restau- rant menus while reinforcing the impor- tance of regular cleaning to minimize the risk of spreading pathogens. Cross-Contamination of Phi 6— Produce The transfer rate of phi 6 from plastic cutting boards and hands to produce (cantaloupes, peppers, and lettuce) are listed in Table 3. At high-level inoculation (10 7 PFU/cm 2 ), the transfer rate from surface to produce was similar. The cutting board to produce transfer rate ranged from 32–33% and hand to pro- duce ranged from 33–37%. At low-level inoculation (10 3 PFU/cm 2 ), the transfer rate from surfaces to bell pep- pers were the highest in the cutting board (40%) and hand (60%) experiments. Let- tuce, by contrast, had the lowest transfer rate in both cases: cutting boards (35%) and hands (25%). The widest range for trans- fer rate was found from hands to produce (25–60%). Our results show, therefore, that cross-contamination is a risk even with a low viral concentration. Lettuce and cantaloupes historically have been associated with multiple foodborne ill-

TABLE 3

Transfer Rate of Phi 6 From Cutting Board and Hands to Produce

Log and Transfer Rate With Low Level Inoculation (10 3 PFU/cm 2 )

Item

Log and Transfer Rate With High Level Inoculation (10 7 PFU/cm 2 )

Log PFU/cm 2

Transfer Rate b (%)

Transfer Rate (%)

Log PFU/cm 2 a

Cutting board to bell pepper Cutting board to cantaloupe Cutting board to lettuce Hand to bell pepper

1.9 ± 0.2

0.8 ± 0.5

2.0 ± 0.3

0.7 ± 0.1

2.0 ± 0.3

0.7 ± 0.5

2.1 ± 0.1

1.2 ± 0.4

Hand to cantaloupe

2.0 ± 0.2

0.9 ± 0.3

Hand to lettuce

2.2 ± 0.2

0.5 ± 0.3

a Mean and standard deviation of phi 6 from the inoculated cutting board or hands (10 7 or 10 3 PFU/cm 2 )to the produce when the produce was left on the cutting board for 1 hr or when hands touched the produce for 20 s ( N = 6). b The transfer rate (percentage) of mean and standard deviation of phi 6 from the inoculated cutting board or hands (10 7 or 10 3 PFU/cm 2 ) to produce when produce was left on the cutting board for 1 hr or when hands touched the produce for 20 s ( N = 6).

ness outbreaks; however, bell peppers dem- onstrated a higher transfer rate compared with the other produce. It is possible that the smooth skin of the pepper allowed for more of the phi 6 samples to be collected, whereas the ridges in the other produce samples inhibited collection. The same diculty of removing contamination from melon rinds in postharvest processing (Gagliardi et al., 2003) could account a lower transfer rate of phi 6 from the cantaloupes. These transfer rate results have increased importance due to the fact that respiratory viruses have the ability to survive on produce for several days (Yépiz-Gómez et al., 2013). Conclusion Data from our study suggest that enveloped phi 6 bacteriophages can persist on food service operation surfaces for an extended period of time. From a practitioner perspec- tive, it is crucial for food handlers in food service operations to be aware of pathogens (foodborne or respiratory) that can lead to cross-contamination and cause illness among employees and customers. Therefore, addi- tional care should be taken to prevent cross- contamination among surfaces, hands, and

food by implementing eective food safety and hygiene practices. Our results also provide new insight for food service operations on the factors that aect viral transmission rates on dierent surfaces. Additionally, by improving food service sanitation programs, our study can inform the industry on the risks posed by fomites. Future research could investigate if pathogenic coronaviruses such as SARS- CoV-2 show a similar persistence and transfer rate on food contact surfaces. Acknowledgement: The authors acknowledge the Food Safety Research Funds at the Con- rad N. Hilton College of Global Hospitality Leadership. Furthermore, the authors declare no conflict of interest in the publication of this article. Corresponding Author: Sujata A. Sirsat, Asso- ciate Professor, Conrad N. Hilton College of Global Hospitality Leadership, University of Houston, 4450 University Drive, S230, Hous- ton, TX 77204-3028. Email: sasirsat@central.uh.edu.

Volume 85 • Number 10