NEHA June 2023 Journal of Environmental Health

The June 2023 issue of the Journal of Environmental Health (Volume 85, Number 10), published by the National Environmental Health Association.

JOURNAL OF Environmental Health Dedicated to the advancement of the environmental health professional

Volume 85, No. 10 June 2023

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Published by the National Environmental Health Association

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ADVANCEMENT OF THE SCIENCE

ABOUT THE COVER

Coronavirus Surrogate Persistence and Cross-Contamination on Food Service Operation Fomites.......................................................................................................................8 Special Report: Federal Meat and Poultry Inspection Duties and Requirements—Part 2: The Public Health Inspection System, Marks of Inspection, and Slaughter Inspections .................. 16 ADVANCEMENT OF THE PRACTICE International Perspectives/Special Report: Unfolding Outbreak Scenarios Can Be a Bite-Size Treat and Other Lessons From New Zealand’s First Online Environmental Health Conference ....................................................................................................................... 20 Building Capacity: Build Capacity by Adding to Facility Inventory ............................................. 24 Direct From ATSDR: APPLETREE: Building Local Capacity to Respond to Environmental Exposures ............................................................................................................ 26 Direct From CDC/Environmental Health Services: Shine a Light on Environmental Justice Issues With the Environmental Justice Dashboard ............................................................. 28 The Practitioner’s Tool Kit: Risk: We Assess It! .......................................................................... 30 Programs Accredited by the National Environmental Health Science and Protection Accreditation Council....................................................................................... 33 ADVANCEMENT OF THE PRACTITIONER Environmental Health Calendar ...............................................................................................34 Resource Corner........................................................................................................................ 35 Spotlight on NEHA Resources: Our Online Store ..................................................................... 36 YOUR ASSOCIATION President’s Message: With You Till the End of the Line ............................................................................ 6 Special Listing ........................................................................................................................... 38 NEHA 2023 AEC....................................................................................................................... 40 In Memoriam............................................................................................................................. 42 NEHA News .............................................................................................................................. 45

In this month’s cover article,

“Coronavirus Sur- rogate Persistence and Cross-Contam- ination on Food Service Operation Fomites,” the study

investigated the persistence and

transfer rate of phi 6 bacteriophage (a SARS- CoV-2 surrogate) on food contact surfaces and fomites commonly present in food service operations. The results indicate that food contact surfaces, fomites, and hands can serve as sources of viral transmission within food service operations. These results can be used by the food service industry to address sanita- tion practices and by public health agencies to provide science-based recommendations to stakeholders. See page 8. Cover image © iStockphoto: FotoDuets

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don’tmiss in the next Journal of Environmental Health  Applying the Model Aquatic Health Code to Grade Swimming Pool Safety  Environmental Health Department Structure: Literature Review and Recommendations  Federal Meat And Poultry Inspection Duties And Requirements—Part 3: Monitoring of Food Safety Systems  Phi 6 Bacteriophage Persistence

Official Publication

Published monthly (except bimonthly in January/February and July/ August) by the National Environmental Health Association, 720 S. Colorado Blvd., Suite 105A, Denver, CO 80246-1910. Phone: (303) 802- 2200; Fax: (303) 691-9490; Internet: www.neha.org. E-mail: kruby@ neha.org. Volume 85, Number 10. Yearly subscription rates in U.S.: $150 (electronic), $160 (print), and $185 (electronic and print). Yearly international subscription rates: $150 (electronic), $200 (print), and $225 (electronic and print). Single copies: $15, if available. Reprint and advertising rates available at www.neha.org/jeh. Claims must be filed within 30 days domestic, 90 days foreign, © Copyright 2023, National Environmental Health Association (no refunds). All rights reserved. Contents may be reproduced only with permission of the managing editor. Opinions and conclusions expressed in articles, columns, and other contributions are those of the authors only and do not reflect the policies or views of NEHA. NEHA and the Journal of Environmental Health are not liable or responsible for the accuracy of, or actions taken on the basis of, any information stated herein. NEHA and the Journal of Environmental Health reserve the right to reject any advertising copy. Advertisers and their agencies will assume liability for the content of all advertisements printed and also assume responsibility for any claims arising therefrom against the publisher. The Journal of Environmental Health is indexed by Clarivate, EBSCO (Applied Science & Technology Index), Elsevier (Current Awareness in Biological Sciences), Gale Cengage, and ProQuest. The Journal of Environmental Health is archived by JSTOR (www.jstor.org/journal/ jenviheal). All technical manuscripts submitted for publication are subject to peer review. Contact the managing editor for Instructions for Authors, or visit www.neha.org/jeh. To submit a manuscript, visit http://jeh.msubmit.net. Direct all questions to Kristen Ruby-Cisneros, managing editor, kruby@neha.org. Periodicals postage paid at Denver, Colorado, and additional mailing offices. POSTMASTER: Send address changes to Journal of Environmental Health , 720 S. Colorado Blvd., Suite 105A, Denver, CO 80246-1910.

Journal of Environmental Health (ISSN 0022-0892)

Kristen Ruby-Cisneros, Managing Editor Ellen Kuwana, MS, Copy Editor Hughes design|communications, Design/Production Cognition Studio, Cover Artwork Soni Fink, Advertising For advertising call (303) 802-2139 Technical Editors William A. Adler, MPH, RS Retired (Minnesota Department of Health), Rochester, MN Gary Erbeck, MPH

and Cross-Contamination on the Surface of Farmers Market Fomites

Erratum In the April 2023 Journal of Environmental Health (volume 85, number 8), the author listing for S. Jeon was incorrectly listed in the article, “Decreased Moderate to Vigorous Physical Activity Levels in Children With Asthma Are Associated With Increased Trac-Related Air Pollutants,” by J. Aguilera, S. Jeon, A.U. Raysoni, W.-W. Li, and L.D. Whigham. The correct listing is: Soyoung Jeon, PhD, Department of Economics, Applied Statistics, and International Business, New Mexico State University.

Retired (County of San Diego Department of Environmental Health), San Diego, CA Thomas H. Hatfield, DrPH, REHS, DAAS California State University, Northridge, CA Dhitinut Ratnapradipa, PhD, MCHES Creighton University, Omaha, NE

Printed on recycled paper.

Volume 85 • Number 10

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Updated Registered Environmental Health Specialist / Registered Sanitarian (REHS / RS) Study Guide, 5th Edition͜ Fresh visual layout to enhance reading and studying experience͜ 15 chapters covering critical exam content͜ Insights from 29 experts Helps you identify where to focus your studying so you can pass the exam! neha.org/rehs-study-materials

Our Health in All Policies (HiAP) Preparedness Guide provides a framework to taking a HIAP approach to public health preparedness to improve the depth and eectiveness of collaboration at all stages of response. It is organized using the four phases of the disaster management cycle: mitigation, preparedness, response, and recovery. Each section begins with a description of the disaster cycle activities that take place and the partners that might provide support during each phase. Find the guide and useful worksheets at www.neha.org/hiap- preparedness-guide.

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June 2023 • Journal of Environmental Health

YOUR ASSOCIATION

 PRESIDENT’S MESSAGE

With You Till the End of the Line

D. Gary Brown, DrPH, CIH, RS, DAAS

T hank you for the honor and privilege of allowing me to represent my fellow environmental health professionals as president of National Environmental Health Association (NEHA) for this trip around the sun. As Happy from Snow White and the Seven Dwarfs sang, “You’re never too old to be young.” This past year has invigorated me regarding the bright future of environmental health. It is hard to believe my term as presi- dent is ending, but NEHA is in great hands with outstanding board members, sta, volun- teers, and members who will keep the NEHA ship steered not only in the right direction but also help our organization to gain steam. Time flies when you are having fun. I have enjoyed working with our sta, board mem- bers, and NEHA aliate leaders while meet- ing members from coast to coast. Although my term is ending, Captain America’s say- ing, “I’m with you till the end of the line,” rings true. U.S. President John F. Kennedy said, “And so, my fellow Americans: ask not what your country can do for you—ask what you can do for your country.” I ask my fellow colleagues, what can you do to help NEHA improve our profession, which in turn will improve the whole wide world? Margaret Mead, an Ameri- can cultural anthropologist, is attributed for saying, “Never doubt that a small group of thoughtful, committed citizens can change the world. Indeed, it is the only thing that ever has.” The environmental health profes- sion is the second largest sector of the gov- ernmental public health workforce—we can move mountains.

health, handling threats such as environ- mental inequities (e.g., lead exposure), climate change (e.g., drought), food safety (e.g., baby food), safe drinking water (e.g., perfluorooctanesulfonic acid [PFOS]), and clean air (e.g., ozone). As you do your job protecting the public, please remember what Rosa Parks said (and also attributed to Marie Curie): “You must never be fearful of what you are doing when it is right.” NEHA Past President Dr. Priscilla Oliver coined the phrase “One NEHA” during her presidency. I would like to highlight the One Health concept. From the One Health High- Level Expert Panel et al. (2022), One Health is defined as an “integrated, unifying approach that aims to sustainably balance and opti- mize the health of people, animals, and eco- systems. It recognizes the health of humans, domestic and wild animals, plants, and the wider environment (including ecosystems) are closely linked and interdependent. The approach mobilizes multiple sectors, disci- plines, and communities at varying levels of society to work together to foster well-being and tackle threats to health and ecosystems, while addressing the collective need for clean water, energy and air, safe and nutritious food, taking action on climate changes, and contributing to sustainable development.” Globally, environmental health is recognized as a critical component for assessing and pro- tecting human, animal, and ecological health. I hope you will be able to join me for the second One Health | One Global Environ- ment Conference in Montego Bay, Jamaica, from October 2–6, 2023 (www.onehealth

I will continue to spread the word that environmental health is a hidden treasure.

Huey Lewis and the News sang, “They say the heart of rock and roll is still beating.” Environmental health is the heart of public health. Environmental health professionals, the Swiss Army knives of scientists, are stra- tegically positioned to identify and intervene to prevent public health issues from aecting local populations. As we do our jobs, please remember another quote from John F. Ken- nedy: “Change is the law of life. And those who look only to the past or present are cer- tain to miss the future.” Healthy People 2030 focuses on reducing people’s exposure to harmful pollutants in air, water, soil, food, and materials in homes and workplaces. The environmental health workforce will be at the forefront of this initiative, reducing and preventing illness to individuals, families, and communities caused by physical, chemical, and biological agents found in our environment. Environ- mental health professionals are scientifically trained and certified to not only identify but also, and more importantly, mitigate environmental dangers and promote alter- natives. We are on the front lines of public

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conference.com). The conference is hosted by the Jamaica Association of Public Health Inspectors in collaboration with NEHA, the Canadian Institute of Public Health Inspec- tors, and the Americas Regional Group of the International Federation of Environmental Health. The first conference was attended by more than 400 health practitioners and academics spanning six continents. Envi- ronmental health provides a critical link to protecting human health from human-to- human, vectorborne, and zoonotic diseases. Rachel Carson, author of Silent Spring , aptly stated, “The more clearly we can focus our attention on the wonders and realities of the universe around us, the less taste we shall have for destruction.” I will continue to spread the word that environmental health is a hidden treasure, providing a world of opportunity that touches all aspects of daily life. As broadcast jour- nalist Tom Brokaw said, “It’s easy to make a

buck. It’s a lot tougher to make a dierence.” We are lucky to be in a profession where you can make a good living while making a dif- ference. Please become involved with NEHA on a local, state, or national level and spread the word that environmental health is pub- lic health. Please emulate Bishop Desmond Tutu, who said, “Do your little bit of good where you are; it’s those little bits of good put together that overwhelm the world.“ I am proud of the work NEHA has accom- plished over the past year. NEHA and my fel- low environmental health professionals make a dierence in the lives of people. I know NEHA will continue to do remarkable things in the years to come. We should heed the words of Mother Teresa: “Yesterday is gone. Tomorrow has not yet come. We have only today. Let us begin.” I leave you with one last quote from Peter Pan written by J.M. Barrie: “Never say good- bye because goodbye means going away and

going away means forgetting” Edward Cox, a friend of mine and World War II veteran, used to say that it is not goodbye but later. Until we meet next time, remember that I am easy to recognize in a crowd due to my fash- ion sense and quiet voice.

gary.brown@eku.edu

Reference One Health High-Level Expert Panel, Adis- asmito, W.B., Almuhairi, S., Behravesh, C.B., Bilivogui, P., Bukachi, S.A., Casas, N., Becerra, N.C., Charron, D.F., Chaudhary, A., Ciacci Zanella, J.R., Cunningham, A.A., Dar, O., Debnath, N., Dungu, B., Farag, E., Gao, G.F., Hayman, D.T.S., Khaitsa, M., . . . Zhou, L. (2022). One Health: A new defi- nition for a sustainable and healthy future. PLOS Pathogens , 18 (6), e1010537. https:// doi.org/10.1371/journal.ppat.1010537

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June 2023 • Journal of Environmental Health

$" " SCIENCE

Coronavirus Surrogate Persistence and Cross-Contamination on Food Service Operation Fomites

Zahra H. Mohammad, PhD Conrad N. Hilton College of Global Hospitality Leadership, University of Houston Thomas A. Little Conrad N. Hilton College of Global Hospitality Leadership, University of Houston Sujata A. Sirsat, MS, PhD Conrad N. Hilton College of Global Hospitality Leadership, University of Houston

ally, the COVID-19 pandemic has resulted in over 676 million cases and over 6.8 million deaths (Johns Hopkins University & Medi- cine, 2023). Food service sectors (e.g., businesses, employees) have been adversely aected during the COVID-19 pandemic (Roy et al., 2021; Sirsat, 2021). According to the National Restaurant Association (2021), the restau- rant industry finished 2020 with a total sales of $240 billion below what was forecasted and with 2.5 million fewer jobs. Yang et al. (2020) reported that a 1% increase in daily COVID-19 cases results in a 0.056% decrease in restaurant demand. Healthcare profession- als have reported detrimental eects on men- tal health in food service workers as a result of COVID-19 (Rosemberg et al., 2021). Studying viral transmission and working with pathogenic viruses requires a Biosafety Level 3 laboratory. Surrogate viruses have been used successfully for many viral sur- vival and transmission studies (Aquino de Carvalho et al., 2017; Casanova & Weaver, 2015; Turgeon et al., 2014). Our study used bacteriophage phi 6 as a surrogate (i.e., virus model) for coronaviruses because it is safe and easy to reproduce (Turgeon et al., 2014); phi 6 previously has been validated as an appropriate surrogate for enveloped viruses such as enveloped waterborne viruses (Aquino de Carvalho et al., 2017) and coro- naviruses (Bailey et al., 2022; Franke et al., 2021; Serrano-Aroca, 2022). The SARS-CoV-2 virus is transmitted primarily via droplets through coughing, sneezing, and contact with an infected person, but surface transmission is pos- sible (Castaño et al., 2021; Mouchtouri

'897&(9 This study investigated the persistence and transfer rate of phi 6 bacteriophage (SARS-CoV-2 surrogate) on food contact surfaces and fomites that are commonly present in food service operations. Coupons (e.g., stainless steel, cutting board) were inoculated with phi 6 and phi 6 survival was quantified over 30 days. The results showed that phi 6 persisted for up to 13 days on sponges, stainless steel, tabletops, countertops, cutting boards, and light switches. Additionally, phi 6 was found for 10 days on microfiber towels and wooden floors. We examined the transfer rate of phi 6 from food contact surfaces to wiping tools, hands, and produce. Fomites and hands were inoculated with 10 7 or 10 3 PFU/cm 2 phi 6 to simulate high and low contamination levels, and surfaces were allowed to dry for 1 hr. The inoculated surfaces were swabbed with sponges or towels or touched with hands or produce, and then these samples were analyzed. The results indicated that food contact surfaces, fomites, and hands can serve as sources of viral transmission within food service operations. Enveloped phi 6 could persist for days on inanimate surfaces and pose a high risk of cross-contamination in food service operations. The results of this study could be used by the food service industry to address sanitation practices and by public health agencies to provide science-based recommendations to stakeholders.

Introduction Coronavirus disease (COVID-19) is a disease caused by a novel respiratory virus called severe acute respiratory syndrome coronavi- rus 2 (SARS-CoV-2; Pressman et al., 2020). COVID-19 symptoms include but are not limited to fever, chills, cough, loss of taste or smell, shortness of breath, and gastrointes- tinal disorders (Centers for Disease Control

and Prevention [CDC], 2022; Lai et al., 2020; Yang & Wang, 2020). Coronavirus (CoV) is a virus that belongs to the family Coronaviri- dae, which is a large family of viruses that are characterized as enveloped, single-stranded, positive-sensed RNA viruses (Yang & Wang, 2020). As of March 2023, there were more than 103 million COVID-19 cases and over 1.1 million deaths in the U.S. alone; glob-

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et al., 2020; Pressman et al., 2020). These inanimate objects or surfaces, when con- taminated, can spread pathogens and are called fomites (Castaño et al., 2021). Previ- ous studies have investigated the survival of respiratory viruses—such as the Middle East respiratory syndrome (Kampf et al., 2020; van Doremalen et al., 2013) and severe acute respiratory syndrome (Chan et al., 2011; Kampf et al., 2020)—and showed that these viruses can persist on fomites such as metal, glass, or plastic. Their persistence can last from a few hours to a few days depending on the virus, type of surface, and other envi- ronmental factors. Similar studies in hospi- tal settings demonstrated virus survival on fomites and that transmission from these fomites is possible (Kaslo et al., 2021; Otter et al., 2016; Sizun et al., 2000). In general, virus survival rates in the environment depend on many factors, including moisture, relative humidity, tem- perature, and whether a surface is porous or nonporous (Lopez et al., 2013; Tiwari et al., 2006; Whitworth et al., 2020). Studies have shown that SARS-CoV-2 can survive for as long as 3 days on plastic, 2 days on stainless steel, and up to 24 hr on cardboard (Suman et al., 2020). Kampf et al. (2020) conducted a review of persistence of coronaviruses on inanimate surfaces and found evidence that the SARS-CoV virus could survive on inani- mate surfaces such as metal, glass, or plastic for as many as 5 days, 5 days, and 9 days, respectively (Duan et al., 2003; Rabenau et al., 2005). Mouchtouri et al. (2020) reported that SARS-CoV-2 particles were detected on various surfaces, in air sam- ples, and in sewage waste from hospitals and other community settings. One study also showed that under favorable environ- mental conditions, SARS-CoV-2 can persist and stay viable on fomites for up to 21 days (Kaslo et al., 2021). It is essential to understand how long viruses such as SARS-CoV-2 can persist on high-touch surfaces in food service opera- tions and their transmission rates under various conditions, because rates can vary from hours to days (Kampf et al., 2020). In March 2021, the World Health Organization (2021) reported that SARS-CoV-2 was found on frozen and refrigerated food packaging in China. One study reported that SARS-CoV-2 attached on salmon skin could survive and

stay infectious for more than 7 days if stored at 4 °C and 2 days at 25 °C, concluding that SARS-CoV-2 attached to fish and seafood could serve as a source of contamination (Dai et al., 2020). We selected peppers, cantaloupe, and let- tuce samples because all have been associated with foodborne illness outbreaks in the past (CDC, 2023). Moreover, their diverse physi- cal characteristics allow for a comprehensive investigation of contamination persistence and cross-contamination (Stine et al., 2005). These produce previously have been used to study viral surface contamination (Allwood et al., 2004, Cliver et al., 1983; Le Guyader et al., 2004; Stine et al., 2005). The textured surfaces of lettuce (Takeuchi & Frank, 2001) and cantaloupe (Ukuku & Fett, 2002) have been shown to protect bacteria from chemical and physical interventions, while the smooth surfaces of peppers o er a contrast for inves- tigative purposes. These three produce items are regularly eaten raw, bypassing a lethal- ity step that includes cooking above 140 °F (CDC, 2023). The goals of our study were to 1) investi- gate the persistence of phi 6-relevant fomites within food service operations and 2) evalu- ate the cross-contamination and transfer rate from high-touch surfaces to wiping tools, hands, and produce, and from cutting boards to produce.

an inoculation loop from previously prepared TSA slant and incubated for 18 hr at 22 °C . After overnight incubation, a single colony of P. syringae was picked using a sterile loop and inoculated in a 250-ml flask containing 50 ml of TSB. The flask was incubated in a shaking incubator for 18 hr at 22 °C. After incubation, the density of the culture was verified using a spectrophotometer (Spectronic 20D, Thermo Fisher Scientific) at optical density (OD 550 ) and grown until the reading output showed absorbance between 0.5 and 0.8. After preparing the host, 1 ml of room tem- perature TSB was added to the tube contain- ing the lyophilized virus and vortexed for 1 min to mix. Next, 500 μl of the rehydrated virus was added to 50 ml of TSB in a 250- ml flask, followed by adding 100 μl of over- night growth of P. syringae . The flask contain- ing TSB, the virus, and P. syringae was then placed in a shaking incubator and incubated for 18 hr at 22 °C. New Stock Purification After incubation, phi 6 was purified using a 0.22-μm PVDF membrane filter that was attached to a sterile needle-less Millipore SLGV033RS 60-cc syringe. The plunger was pulled out from the syringe and 15 cc of the overnight culture was pipetted into the syringe barrel. After the plunger was reinserted, the syringe filtered out bacterial debris and the virus was dispensed into a sterile polypropylene tube (centrifuge tube). All procedures were performed inside a bio- safety cabinet. Plaque Assay Plaque assays were carried out to identify the concentration of phi 6 for filtrate viruses; 10-fold serial dilutions of the phi 6 filtrate were made in 0.02% of phosphate bu ered saline (PBS) and Tween (PBST, 100 ml PBS + 0.02% Tween 20) bu er. The remaining filtrate was wrapped with aluminum foil and stored in a refrigerator at 4 °C for later use. Next, 1 ml of the diluted phi 6 was mixed with 100 μl of overnight cultures of P. syrin- gae . The mixture was added to a tube con- taining 3 ml of TSB soft agar prewarmed to 45–50 °C. The soft agar with host and phi 6 was mixed quickly in a tube and poured onto TSA plates. The plates were swirled manually to evenly distribute the soft agar. The plates were allowed to dry for 30 min, inverted,

Methods

Reagents and Coupons All media and reagents were purchased from VWR. The sponges, microfiber towels, and cutting boards were purchased from an online retail website. Coupons of lami- nate tabletop, countertop, wooden floor, and stainless steel were purchased from Thermo Fisher Scientific. Bacteriophage and Host Pseudomonas syringae (host) and phi 6 were obtained from the Centers for Disease Con- trol and Prevention. The host was cultivated on tryptic soy agar (TSA) and grown in tryp- tic soy broth (TSB). The virus stock solutions were prepared by suspending propagated phi 6 in TSB at concentrations of 8–10 log plaque forming units (PFU)/ml. Working stocks of phi 6 were prepared and stored at 4 °C. Next, P. syringae were streaked on TSA plates using

June 2023 • 4:73&1 4+ 3;.7432*39&1 *&19-

ADVANCEMENT OF THE SCIENCE

TABLE 1

Persistence of Phi 6 on Restaurant Surfaces Over 30 Days

Day

Mean Log PFU/cm 2 and Standard Deviation on the Surface of Each Fomite a

Sponge

Microfiber Towel 5.2 ± 0.3 3.2 ± 0.5 2.4 ± 0.1 2.1 ± 0.3 1.6 ± 0.1 1.2 ± 0.1 0.8 ± 0.5 0.5 ± 0.2 0.4 ± 0.2

Stainless Steel

Floor

Tabletop

Countertop Cutting Board Light Switch

1 2 3 4 7

5.7 ± 0.2 4.0 ± 0.7 2.7 ± 0.1 2.3 ± 0.2 1.9 ± 0.2 1.5 ± 0.2 1.3 ± 0.2 0.7 ± 0.6 0.5 ± 0.2 0.4 ± 0.2

5.4 ± 0.1 3.1 ± 0.8 2.6 ± 0.2 2.3 ± 0.3 1.7 ± 0.3 1.2 ± 0.2 1.0 ± 0.2 0.5 ± 0.2 ND ± 0.3

5.6 ± 0.4 3.5 ± 0.5 2.7 ± 0.1 2.2 ± 0.1 1.6 ± 0.3 1.3 ± 0.1 0.8 ± 0.5 0.4 ± 0.2

5.5 ± 0.3 3.4 ± 0.4 2.8 ± 0.1 2.4 ± 0.1 1.9 ± 0.2 1.5 ± 0.2 1.1 ± 0.3 0.8 ± 0.3 0.5 ± 0.2

5.6 ± 0.4 3.8 ± 0.2 2.6 ± 0.1 2.2 ± 0.1 1.7 ± 0.3 1.3 ± 0.2 0.9 ± 0.4 0.7 ± 0.4

5.5 ± 0.5 3.5 ± 0.5 2.6 ± 0.1 2.1 ± 0.2 1.7 ± 0.2 1.3 ± 0.2 1.1 ± 0.2 0.6 ± 0.3 0.4 ± 0.2

5.3 ± 0.3 3.3 ± 0.4 2.5 ± 0.1 2.2 ± 0.4 1.7 ± 0.4 1.4 ± 0.1 0.9 ± 0.5 0.5 ± 0.2

10 13 16 19 22 25 28 30

ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

ND ± 0 ND ± 0 ND ± 0 ND ± 0

ND ± 0 ND ± 0 ND ± 0

a Mean and standard deviation of survival of phi 6 on each surface of each item over 30 days (N = 6). The greatest reduction of phi 6 occurred within the first 3 days postinoculation. Note. ND = none detected.

and incubated for 24 hr at 22 °C. PFUs were quantified after incubation.

were made and 1 ml from each dilution and 100 μl of the overnight host were added to one melted and tempered TSA soft agar (3 ml) overlay tube and poured onto TSA plates, which were tilted to ensure that the soft agar mixture completely coated the TSA plates. The plates were allowed to solidify in a biosafety cabinet for 30 min before they were inverted and incubated for 18–24 hr at 22 °C in the incubator. Negative control plates were prepared using sterile phage buer (no phi 6) to test for potential contamination. After the incubation period, plaques on each plate were quantified and recorded as PFUs. For each of three biological replicates under similar experimental conditions, the above sample plating procedures were carried out on days 1, 2, 3, 4, 7, 10, 13, 16, 19, 22, 25, 28, and 30. After 30 days of sampling, no phi 6 was detected; therefore, 30 days was chosen as the sampling plan for our study. Simulation Experiment We conducted a simulation experiment to understand the potential for phi 6 cross-con- tamination in a food service operation setting and quantify the rate of cross-contamination

from surfaces to wiping tools, and from hands or cutting boards to produce. The experi- ments were performed using high and low (10 7 and 10 3 PFU/cm 2 , respectively) phi 6 concentrations to simulate dierent contami- nation levels. In total, three biological repli- cates were conducted. Contamination of Surfaces With a High or Low Level of Phi 6 For the first scenario, 0.2 ml of phi 6 suspen- sion (10 7 and 10 3 PFU/ml, respectively) was inoculated onto tabletop, countertop, and stainless steel (5 cm x 5 cm) coupons and held at room temperature (23 ± 2 °C) for 1 hr to facilitate attachment. Next, a sponge or microfiber towel was used to swab each sur- face. Then, each sponge or microfiber towel was placed into a stomacher bag and mixed using a stomacher lab blender for 2 min. Each item was then subjected to microbiological analysis as described in the previous section.

Persistence Experiment

Sample Preparation and Inoculation of Fomites Before the start of the experiment, all coupons were cut into either 5 x 5 cm or 10 x 10 cm squares, depending on the item. Coupons were sterilized using an autoclave for 15 min at 121 °C or by using 70% ethanol. The inoc- ulum was prepared by adding 5 ml of phi 6 stock to 45 ml of 0.02% PBST buer (10 8 PFU/ ml). Each coupon surface was spot-inoculated with the inoculum and an L-shaped spreader was used to evenly distribute the phage. The coupons were air-dried for 1 hr at room tem- perature (23 ± 2 °C) in a biosafety cabinet. During the drying time, TSA soft agar tubes were prepared for overlay by melting prepared TSA soft agar in a 48–50 °C water bath. After the coupons were air-dried, two inoc- ulated coupon samples for each surface were taken and placed in a stomacher bag contain- ing either 90 ml or 45 ml of buer (0.02% PBST) and homogenized using a stomacher lab blender for 2 min. Next, 10-fold dilutions

Cross-Contamination From Surfaces to Hands

Hands were washed for 30 s using soap and warm water (40 °C), dried using paper tow-

Volume 85 • Number 10

Statistical Analyses PFUs from all experiments (persistence and simulation) were converted to log10 and the survival rate curve was constructed using Microsoft Excel. The transfer rate is defined as: log PFU/cm 2 on recipient surface divided by log PFU/cm 2 on the original surface (source) multiplied by 100.

TABLE 2

Transfer Rate of Phi 6 From Food Contact Surfaces (Stainless Steel, Tabletop, and Countertop) to Wiping Tools (Sponge and Microfiber Towel) and Hands

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

Surface

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

Results and Discussion

Log PFU/cm 2

Transfer Rate b (%)

Transfer Rate (%)

Log PFU/cm 2 a

Persistence of Phi 6—Food Service Fomites

Stainless steel to sponge

2.3 ± 0.3

0.7 ± 0.5

Table 1 shows the persistence of phi 6 on sponges, microfiber towels, stainless steel, wooden floors, tabletops, countertops, cut- ting boards, and light switches over a period of 30 days. The results indicate that phi 6 can persist for as long as 13 days on the follow- ing coupons: sponges, tabletops, countertops, cutting boards, and light switches. In addi- tion, phi 6 persisted for as long as 10 days on microfiber towel and wooden floor coupons. Rapid reductions of phi 6 were observed within the first 2 days for all fomites, where reductions of more than 2 logs PFU/cm 2 were recorded on all surfaces except sponges and countertops. After day 2, the reductions of the phi 6 levels remained constant until day 13, at which point phi 6 fell below the detec- tion limit of 0.9 logs PFU/cm 2 for all surfaces. Previous literature has shown that food and food contact surfaces in food service operations could be a source for the cross- contamination and transmission of bacteria and viruses (Gibson et al., 2012). Santarpia et al. (2020) reported that a person infected with SARS-CoV-2 could contaminate the room environment where they were cared for—including air and environmental sur- faces such as personal items, room surfaces, and toilets. SARS-CoV-2 was also detected on food preparation surfaces, service areas, hos- pital isolation wards, air conditioning filters, sewage treatment units, and in air samples (Mouchtouri et al., 2020). These finding are significant because there is scientific evidence of potential viral transmission from contami- nated fomites to a person’s mouth (Rusin et al., 2002). Cross-Contamination of Phi 6— Surfaces Table 2 shows the transfer rate of phi 6 from food contact surfaces to wiping tools

Tabletop to sponge

1.8 ± 0.4 2.2 ± 0.1 1.6 ± 0.1

30 37 26

0.6 ± 0.3 0.9 ± 0.2 0.9 ± 0.3

30 45 45

Countertop to sponge

Stainless steel to microfiber towel Tabletop to microfiber towel Countertop to microfiber towel

1.7 ± 0.4

0.4 ± 0.2

2.1 ± 0.1

0.3 ± 0.3

Stainless steel to hand

2.4 ± 0.2 2.1 ± 0.3 2.2 ± 0.1

40 35 37

0.5 ± 0.3 1.2 ± 0.1 0.6 ± 0.3

25 60 30

Tabletop to hand

Countertop to hand

a Mean and standard deviation of phi 6 from the inoculated stainless steel, tabletop, or countertop (10 7 or 10 3 PFU/cm 2 ) to sponge or microfiber towel when used to wipe each surface, or to hands when hands touched each surface for 20 s ( N = 6). b The transfer rate (percentage) of mean and standard deviation of phi 6 from the inoculated stainless steel, tabletop, or countertop (10 7 or 10 3 PFU/cm 2 ) to sponge or microfiber towel when used to wipe each surface, or to hands when hands touched each surface for 20 s ( N = 6).

els, sprayed with 70% ethanol, and allowed to air-dry. The index finger (primary transfer) of each hand was used to touch the contami- nated surfaces for 20 s. Samples from hands were collected using a glove-juice method (Larson et al., 1980; Sirsat et al., 2013) with brief modifications as detailed. The index finger from each hand that touched the con- taminated surfaces for 20 s was placed in a sterile surgical glove containing 1 ml of ster- ile 0.02% PBST virus buer in the index fin- ger section. Next, the finger with the glove on was vortexed for 60 s. The sample was then transferred from the glove index finger region to a sterile 10-ml conical tube using a sterile pipette; the sample then underwent further dilution and viability plate count analyses. Contamination of Cutting Boards and Hands With a High or Low Level of Phi 6 For the second scenario, cutting boards and hands were inoculated with 0.2 ml of phi 6

suspension (10 7 and 10 3 PFU/ml, respec- tively). Samples of produce (pepper, can- taloupe, and lettuce) were placed on an inoculated cutting board. After marking the portion of the produce that was placed on the cutting board, it was left in contact for 1 hr at room temperature (23 ± 2 °C). The marked (inoculated) portion of each produce sample was swabbed using an alginate cotton swab and placed into a tube containing 5 ml of 0.02% PBST. Additionally, produce sam- ples were placed in contact with inoculated hands for 1 min by touching marked portions of the produce. Next, 1 ml from each col- lected sample (after touching either cutting boards or hands) and 100 μl of overnight host were added to a tube containing 3 ml of TSA soft agar. The contents were shaken by hand, quickly poured onto TSA plates, allowed to solidify, and incubated for 24 hr at 22 °C. After the incubation period, PFUs were quantified.

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

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