NEHA October 2023 Journal of Environmental Health

The October 2023 issue of the Journal of Environmental Health (Volume 86, Number 3), published by the National Environmental Health Association.

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

Volume 86, No. 3 October 2023

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JOURNAL OF Environmental Health Dedicated to the advancement of the environmental health professional Volume 86, No. 3 October 2023

ADVANCEMENT OF THE SCIENCE Persistence and Transfer of Enveloped Phi 6 Bacteriophage on Hotel Guest Room Surfaces................................................................................................................... 8 International Perspectives/Guest Commentary: Managing Mosquito-Borne Diseases as an Emergency for Mosquito Control: The South Korean Experience ........................................ 16 International Perspectives/Guest Commentary: Thirdhand Exposure to Methamphetamine Syndrome: Symptoms Resulting From Environmental Exposure to Methamphetamine Contamination Arising From Manufacture or Use ...................................... 20

ABOUT THE COVER

Thirdhand expo- sure to metham- phetamine occurs through contact with environments that have become contaminated dur- ing the manufac- ture or use of the substance. This

ADVANCEMENT OF THE PRACTICE Feature Story: Empowering Future Environmental Public Health Professionals:

exposure is a serious emerging public health concern and can cause adverse health eects in unwitting residents, particularly children. This month’s cover article, “Thirdhand Exposure to Methamphetamine Syndrome: Symptoms Resulting From Environmental Exposure to Methamphetamine Contamination Arising From Manufacture or Use,” explores the symptoms and current situation related to thirdhand exposure to methamphetamine, proposes a term to be used to describe the syndrome to facilitate the coordina- tion of research, and provides recommendations for environmental health professionals. See page 20. Cover image © iStockphoto: Lucashallel, appleuzr

A Deep Dive Into the Expanded National Environmental Public Health Internship Program ......... 28 Building Capacity: Everyone’s Data Are Special—Or Are They? ................................................. 34 Direct From CDC/Environmental Health Services: Educating Communities, Families, and High School Students About Lead Exposure as a Public Health Problem ................................ 36 Direct From ecoAmerica: Weathering the Storm: Climate Change and the Mental Health of Children ........................................................................................................... 40 NEW NEPHIP Interns in the Spotlight: Constructing a Robust Evaluation System for Improving Medical Needs Shelters: A Transformative Environmental Health Internship Experience ................................................................................................................. 42 ADVANCEMENT OF THE PRACTITIONER JEH Quiz #2............................................................................................................................... 27 Environmental Health Calendar ...............................................................................................44 Resource Corner........................................................................................................................ 45 YOUR ASSOCIATION President’s Message: Environmental Health—What Can’t We Do? .......................................................... 6 Special Listing ........................................................................................................................... 46 NEHA News .............................................................................................................................. 48 NEHA Member Spotlight .......................................................................................................... 50 NEHA 2024 AEC....................................................................................................................... 51

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Environmental Health and Land Reuse Certificate Program .............................................. 35 Hedgerow Software ................................................2 HS GovTech.......................................................... 52 JEH Advertising ......................................................5 NEHA CP-FS Credential ......................................15 NEHA Credentials ................................................ 39 NEHA Endowment Foundation........................... 15 NEHA Membership .......................................... 4, 19 NEHA REHS/RS Credential.................................... 7 NEHA REHS/RS Study Guide................................. 5 NEHA/AAS Scholarship Fund.............................. 39

October 2023 • Journal of Environmental Health

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in the next Journal of Environmental Health don’t miss  Assessing the Burden of Cold-Related Illness and Death in Minnesota  Bacterial and Viral Pathogens in Drinking Water Sources in Pakistan  Evaluating the Impact of Food and Drug Administration-Funded Cooperative Agreement Programs on Conformance With the Voluntary National Retail Food Regulatory Program Standards  NEHA 2023 AEC Wrap-Up

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Volume 86 • Number 3

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October 2023 • Journal of Environmental Health

YOUR ASSOCIATION

 PRESIDENT’S MESSAGE

Environmental Health— What Can’t We Do?

Tom Butts, MSc, REHS

E nvironmental health/environmental public health refers to the branch of public health that focuses on under- standing how environmental factors can aect human health and well-being. It involves as- sessing, mitigating, controlling, and prevent- ing environmental hazards that can have ad- verse eects on individuals or communities. Environmental health considers factors, including air quality, water quality, food safety, sanitation, waste management, haz- ardous substances, occupational health, and the overall built and natural environments we all work and live in. It aims to identify and mitigate potential health risks associ- ated with these factors. Practitioners can conduct research, moni- tor and assess environmental conditions, develop and implement policies and regula- tions, provide education and outreach, and collaborate with other sectors to address envi- ronmental health issues. The ultimate goal is to protect and improve public health by mini- mizing or eliminating environmental risks and promoting environmental sustainability. The specific roles within the environ- mental public health workforce can include environmental health ocers, public health inspectors, epidemiologists, toxicologists, occupational health specialists, environ- mental scientists, environmental engineers, sanitarians, and policy analysts, among others. Each role contributes to dierent aspects of environmental health, but all are important to recognize. As I think about the importance of the work done on a daily basis, I often think about how closely environmental health is aligned with

conditions. By promoting safe and healthy environments, we contribute to fulfilling the safety needs of individuals. The third level in the hierarchy is the need for love and belonging, which encompasses social connections, relationships, and a sense of community. Environmental health is often called on by community members when no one else has responded and can foster commu- nity engagement, collaboration, and awareness. We create opportunities for people to come together and address shared environmental concerns. By promoting a sense of belonging and cooperation, environmental health eorts contribute to fulfilling social needs. The fourth level of Maslow’s hierarchy is the need for esteem, which involves feelings of achievement, recognition, and self-worth. Environmental health work can contribute to enhancing self-esteem by empowering individuals to take control of their environ- ment, make positive changes, and partici- pate in decision-making processes related to their communities. At the top of the hierarchy is self-actual- ization, which refers to achieving one’s full potential and personal growth. While envi- ronmental health might not directly address self-actualization, it can support creating the necessary conditions for individuals to focus on higher-level needs by ensuring a founda- tion of physiological well-being, safety, social connections, and self-esteem. As I reflect on the important role the pro- fession has in our communities, it is also imperative to recognize the continual changes in environmental public health practice, often dictated by national or international events. It

The environmental health practice continues to evolve as challenges and opportunities emerge in the ever- changing landscape.

Maslow’s hierarchy of needs. Maslow’s hier- archy of needs is a psychological theory that suggests humans have a set of hierarchical needs that must be met to reach their full potential and achieve self-actualization. At the base of Maslow’s hierarchy are phys- iological needs, which include basic require- ments for survival such as food, water, shelter, and sleep. Environmental health plays a criti- cal role in ensuring access to clean air, safe drinking water, safe food, adequate sanitation, and proper waste management. By address- ing these foundational issues, environmental health directly contributes to meeting the physiological needs of individuals. Moving up the hierarchy, the next level consists of safety needs, including personal and environmental safety, protection from hazards, and access to healthcare services. Environmental health professionals work every day to identify and mitigate environ- mental risks such as exposure to pollutants, hazardous substances, or unsafe working

Volume 86 • Number 3

Focus on Climate Change: Climate change has emerged as one of the most critical envi- ronmental challenges of our time. Envi- ronmental health professionals are increas- ingly focusing on understanding the health impacts of climate change, such as extreme weather events, changing disease patterns (e.g., locally transmitted malaria in Florida), and the health consequences of rising tem- peratures. Environmental health sta are often part of community teams that develop climate action and mitigation plans, as well as have a role in the planning of cooling centers. Health Impact Assessments: Health impact assessments (HIAs) have become more preva- lent in environmental health practice. HIAs evaluate the potential health eects of pro- posed policies, projects, or developments, helping decision makers to make informed choices that consider public health implica- tions. HIAs can be powerful tools to address social determinants of health. One Health Approach: The concept of One Health has gained traction, recognizing the interconnection between human health, ani- mal health, and the environment. Environ- mental health practitioners are collaborating with professionals in other disciplines, such as veterinarians and ecologists, to address health challenges holistically. Environmental Justice: There is again growing recognition of environmental injus- tices, where vulnerable and marginalized communities bear a disproportionate burden of environmental hazards. Environmental health practitioners are increasingly advocat-

is apparent to me that many of us have worked through a number of both unexpected and pre- dictable changes. These instances have likely created some long days and sleepless nights as we worked to address these challenges while we struggled to maintain the important pro- grams and activities that protect community members and must not be cast aside. Our plates runneth over. Increased Awareness and Concern: Over the past three decades, there has been a notable increase in public awareness and concern about environmental issues such as air and water pollution, new diseases and vectors, climate change, and many more. The accessibility of information (validated or not) often brings new issues to commu- nity activists and the media that in turn must be addressed. These changes have led to a greater demand for action from govern- ments, businesses, and individuals. Advancements in Technology and Data Analysis: Environmental health practitio- ners now have access to advanced technolo- gies and tools for data collection, monitoring, and analysis (if we can aord them or if our agency leaders empower us to access them). GIS, remote sensing, and big data analytics have revolutionized the way food safety and environmental data are gathered and used for decision making. The aordability and access to various air and water quality measuring devices make citizen science eorts more and more common. Artificial intelligence (AI) is poised to have a big impact on environmental health practices, too.

ing for equity and justice in environmental decision making and policy implementation. Regulatory Changes: Environmental regu- lations have evolved over the last 30 years to address what science has identified as risks to our health. Stricter and new environmental standards and regulations have been imple- mented to protect public health. The focus on per- and polyfluoroalkyl substances (PFAS) is the most recent example that aects drinking water and so much more. Global Issues: Environmental health is increasingly recognized as a global issue that requires international collaboration. The global food supply system is a great example. Response and Recovery: Environmental health professionals were called on to assume many new roles during the COVID-19 response. Those roles ranged from enforce- ment to technical assistance as we learned to adapt to the best science available. These roles in recovery from natural disasters are not new, but as disasters are larger and more frequent there is also a larger demand for time and sta. Environmental public health profession- als must continually build their knowledge and be agile in responding to unique circum- stances and changing priorities. The environ- mental health practice continues to evolve as challenges and opportunities emerge in the ever-changing landscape.

tbutts@neha.org

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October 2023 • Journal of Environmental Health

ADVANCEMENT OF THE SCIENCE

Persistence and Transfer of Enveloped Phi 6 Bacteriophage on Hotel Guest Room Surfaces

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

onstrated that SARS-CoV-2 can be transmitted via contaminated surfaces and cause infection (Arav et al., 2021; Santarpia et al., 2020). In their review, Kampf et al. (2020) conclude that respiratory viruses—such as severe acute respiratory syndrome (SARS) coronavirus, Middle East respiratory syndrome (MERS), or endemic human coronaviruses (HCoV)— have the ability to persist and stay viable on inanimate surfaces (i.e., metal, glass, plastic) for days, indicating that surfaces could be a potential source of infection (Duan et al., 2003; Rabenau et al., 2005). In the context of the lodging industry, hotel guest room surfaces usually are subject to fre- quent human contact and touching (Park et al., 2019). Therefore, hotel rooms should be considered at high risk of being contaminated by touch or aerosols and becoming a source of transmission of viruses, such as SARS- CoV-2 (Park et al., 2019). Previous stud- ies have shown that hotel room cleanliness is heavily based on visual observations by cleaning sta and the bioburden on surfaces is not taken into consideration (Almanza et al., 2015a, 2015b). These studies highlighted a lack of testing standards currently for hotel room sanitation. While visual cleanliness is important, it does not ensure protection of infection from pathogens. Hotels and cruise ships have been associ- ated with multiple viral outbreaks. During the SARS outbreak of 2003, the original virus source in Hong Kong was traced to an infected individual who was staying at a local hotel. The virus infected six additional travelers at the hotel before it spread further to other parts of Asia (Chien & Law, 2003). In November 2020, 33 cases of COVID-19 occurred at a quarantine hotel in Australia caused by an

b8tract The hotel guest room environment can be contami- nated through touch or aerosols and become a source of viral transmission. Understanding the extent of respiratory virus survival and persistence on hotel guest surfaces can help the lodging industry develop an eective clean- ing and disinfecting strategy and focus on hot spots. This study investigated the survival and persistence of enveloped phi 6 bacteriophages (a surrogate of SARS-CoV-2) on hotel guest room surface coupons for 30 days at 23 ± 2 °C and determined the transfer rate between fomites and hands. This study showed that phi 6 persisted for up to 2 days on the carpet, hotel room curtain, and leather coupon samples. Phi 6 persisted for up to 3 days on hotel room beds, wooden desks, door handles, and hotel amenities and up to 4 days on light switches, remote controls, and bathroom faucets. When a high level of phi 6 (10 7 PFU/ml) was used, the transfer rate from hands to surfaces ranged from 23% to 58% and the transfer rate from fomites to hands ranged from 50% to 74%. With a low level of phi 6 (10 3 PFU/ml), the transfer rate from hands to surfaces ranged from 14% to 38% and the transfer rate from fomites to hands ranged from 20% to 45%. The results revealed that phi 6 could be transmitted via hotel room surfaces. Our study results can be used as a tool to design robust and eective training strategies for the lodging industry.

Introduction The coronavirus (COVID-19) disease emerged in Wuhan, China, in 2019 and has spread worldwide to reach all countries (Shereen et al., 2020; Suman et al., 2020). The spread of the COVID-19 pandemic has dramatically aected global economic and social life. The hospital- ity industry, in particular the hotel industry, has been the hardest hit by this pandemic due to government lockdowns and social distanc- ing requirements (American Hotel & Lodg- ing Association [AHLA], 2020a; Ocheni et al., 2020). Revenue in the U.S. hotel industry in

2020 fell by nearly 50%, largely due to the low occupancy nationally (AHLA, 2021). COVID-19 is a severe respiratory infec- tion caused by the SARS-CoV-2 virus (World Health Organization, 2020); SARS-CoV-2 is transmitted by an infected person breathing out droplets or aerosols that contain the virus that land on the eyes, nose, or mouth of other people (Centers for Disease Control and Pre- vention [CDC], 2022). Indirect transmission via contaminated surfaces, however, can also occur and could become the source of infec- tion (Castaño et al., 2021). Studies have dem-

Volume 86 • Number 3

Plaque Assay Plaque assays were performed to identify the concentration of phi 6 for filtrate phi 6 bac- teriophages. Next, 10-fold serial dilutions of the phi 6 filtrate were made in 0.02% phos- phate bu¨ered saline (PBS) and Tween (PBST, 100 ml of PBS + 0.02% Tween 20) bu¨er. The remaining filtrate was stored in a refrigerator at 4 °C for later use after wrapping tubes with aluminum foil to protect the phi 6 from light. Next, 1 ml of the diluted phi 6 was mixed with 100 µl of overnight cultures of P. syringae . The mixture was added to a tube containing 3 ml of prewarmed (45–50 °C) TSB soft agar. The soft agar with host and phi 6 was mixed quickly, poured onto TSA plates, and tilted by hand to evenly distribute the soft agar on top. The plates were left to dry for 30 min, inverted, and incubated for 24 hr at 22 °C. After incubation, the plaque-forming units were quantified. Persistence Experiment Before the start of the experiment, all items were cut into either square 5 x 5 cm or 10 x 10 cm coupons, depending on the item. Cou- pons were sterilized using either an autoclave for 15 min at 121 °C or by using 70% etha- nol. The inoculum was prepared by adding 5 ml of phi 6 stock to 45 ml of 0.02% PBST bu¨er (10 8 PFU/ml). To inoculate, each cou- pon surface was spot-inoculated with 0.2 ml of inoculum, and L-shaped spreaders were used to distribute the phage on the surfaces evenly. The coupons were air-dried for 1 hr at room temperature (23 ± 2 °C). Alongside the drying process time, TSA soft agar tubes were prepared for overlay by melting prepared TSA soft agar in a 48–50 °C water bath. After drying time, two samples from each surface were taken and placed in a stomacher bag containing a 45 ml or 90 ml of virus buf- fer (0.02% PBST) and homogenized for 2 min. Next, 10-fold dilutions were made and 1 ml from each dilution and 100 μl of the overnight host were added to one melted and tempered soft (3 ml) TSA agar overlay tube and poured onto a TSA plate. Each TSA plate was tilted to ensure that the overlay mix- ture completely coated the plate. The plates were allowed to solidify inside the biosafety cabinet for 30 min before being inverted and placed for 18–24 hr at 22 °C in an incuba- tor. The sterile phage bu¨er (no phi 6) plates were prepared and used as negative control plates to test for potential contamination.

infected traveler from the UK (Leong et al., 2021). In another example, the Diamond Princess cruise ship outbreak resulted in 696 COVID-19 cases in February 2020 (Expert Taskforce for the COVID-19 Cruise Ship Out- break, 2020). Since 2000, there have been sev- eral incidents of acute respiratory illness out- breaks caused by the influenza virus on cruise ships (Brotherton et al., 2003; CDC, 2001; Fernandes et al., 2014). Cleaning and ecient housekeeping have become even more essential for the hotel industry to provide further assurance to guests (Pillai et al., 2021). In response to the pandemic, many major hotel chains imple- mented new safety and cleaning strategies such as increased use of technology (e.g., remote check-in, contactless ordering in res- taurants), noncontact sanitizers, and partner- ships with industry and academic experts (Four Seasons, 2020; Hilton, 2020; Marri- ott International, Inc., 2022). Additionally, Zemke et al. (2015) showed that guests are willing to pay more if the hotel has disinfect- ing programs and shows that the guest rooms receive sucient cleaning. For the purposes of our study, phi 6 bac- teriophages were used as a surrogate for the SARS-CoV-2 virus. Phi 6 is an enveloped virus that poses similar characteristics to respiratory viruses (Aquino de Carvalho et al., 2017; Turgeon et al., 2014) and has been validated as a suitable surrogate for corona- viruses for environmental investigation (Bai- ley et al., 2022; Franke et al., 2021; Serrano- Aroca, 2022). In addition, as a Biosafety Level 3 laboratory is required for use of the SARS- CoV-2 virus (Turgeon et al., 2014), the use of phi 6 allows for replication studies to be conducted without these extra protections. The objectives of our study were to under- stand the extent of respiratory virus survival and persistence on hotel guest surfaces and evaluate the transfer rate between hands and high-touch surfaces to help hotel manage- ment develop better cleaning and disinfecting strategies of contamination hot spots.

room curtains, leather, bathroom faucets, and stainless-steel coupons were purchased from local retail stores. Samples were chosen based on use in previous hotel microbiological stud- ies (Park et al., 2019; Zemke et al., 2015). Bacteriophage and Host Pseudomonas syringae (host) and phi 6 were provided by the Centers for Disease Control and Prevention. The host was cultivated on tryptic soy agar (TSA) and grown in tryptic soy broth (TSB). To prepare the phi 6 stock solutions, propagated phi 6 was suspended in TSB at concentrations of approximately 8 to 10 log PFU/ml. We prepared and stored working stocks of phi 6 at 4 °C, streaked P. syringae on the TSA plate using a plastic inoculation loop from a previously prepared TSA slant, and the plates were incubated for 18 hr at 22 °C . After overnight incubation, a single colony of P. syringae was taken and inoculated in a 250-ml flask containing 50 ml of TSB using a plastic inoculated needle; the flask was then placed in a shaking incubator for 18 hr at 22 °C. After incubation, the density of the culture was determined using a spectrophotometer (Spectronic 20D, Thermo Fisher Scientific). The density of the culture was set to opti- cal density (OD550) wavelength to achieve absorbance between 0.5 and 0.8 on the spec- trophotometer. After preparing a host, 1 ml of room temperature (23 ± 2 °C) TSB was added to the tube containing the lyophilized phi 6 and vortexed for 1 min, followed by the addition of 500 μl of the rehydrated phi 6 to 50 ml of TSB in a 250-ml flask, followed by the addition of 100 μl of overnight growth of P. syringae (host) to the flask containing the virus. The flask containing TSB, the virus, and P. syringae was placed in a shaking incu- bator for 18 hr at 22 °C. Purification of Phi 6 Stock The phi 6 was purified using a 0.22 μm PVDF filter that was attached to a sterile needle-less Millipore SLGV033RS 60 cc syringe. After pulling the plunger out from the syringe, 15 cc of the overnight culture was pipetted into the syringe barrel. The plunger was replaced, the syringe filtered out any bacterial debris, and the phi 6 was dispensed into a sterile polypropylene tube (i.e., centrifuge tube). All procedures were performed inside a biosafety cabinet.

Methods

Reagents and Coupons All media and reagents were purchased from VWR. The bed, carpet, and hotel amenities were provided by a national hotel chain. Light switches, door handles, TV remote controls,

October 2023 • Journal of Environmental Health

ADVANCEMENT OF THE SCIENCE

TABLE 1

Survival and Persistence of Phi 6 on Hotel Guest Room Surfaces

Day

Mean and Standard Deviation of Log PFU/cm 2 for Each Surface a

Bed

Carpet

Desk

Light Switch

Door Handle

Remote Control 3.5 ± 0.3 2.0 ± 0.3 1.4 ± 0.3 0.9 ± 0.3

Room Curtain 2.5 ± 0.4 1.2 ± 0.2

Hotel Amenities 3.1 ± 0.9 1.9 ± 0.4 1.0 ± 0.3 0.5 ± 0.2

Leather

Bathroom Faucet 3.8 ± 0.3 2.5 ± 0.2 1.3 ± 0.1 0.9 ± 0.4 0.4 ± 0.2

1 2 3 4 7

3.5 ± 0.2 2.2 ± 0.3 1.1 ± 0.4

3.0 ± 0.4 1.5 ± 0.1 0.5 ± 0.3

3.3 ± 0.6 2.0 ± 0.4 1.3 ± 0.1

3.2 ± 0.2 1.9 ± 0.4 1.3 ± 0.3 1.0 ± 0.1

3.8 ± 0.2 2.2 ± 0.3 1.4 ± 0.1 0.7 ± 0.2 ND ± 0.1

2.8 ± 0.5 1.3 ± 0.1 0.4 ± 0.2

ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

0.7 ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

10 13 16 19 22 25 28 30

ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0 ND ± 0

a Mean and standard deviation of phi 6 survival on each hotel guest room surface over 30 days ( N = 6). Note. The greatest reduction of phi 6 occurred within the first 2 days postinoculation. ND = none detected.

After incubation, plates were counted and plaques were recorded as PFU/cm 2 . The above sample plating procedures were carried out on days 1, 2, 3, 4, 7, 10, 13, 16, 19, 22, 25, 28, and 30 for each of the three biological replicates and under similar experimental conditions. Simulation Study A simulation experiment was carried out to determine the ability of phi 6 to transfer from contaminated hands to hotel room surfaces and identify potential cross-contamination from contaminated hotel room surfaces (fomites) to hands. Two dierent scenarios were done using high and low phi 6 concen- trations (high level = approximately 10 7 PFU/ ml; low level = approximately 10 3 PFU/ml) in two experimental settings, three biologi- cal replicates, and with duplicate samples for each replicate. Scenario 1: Cross-Contamination From Inoculated Hands With High or Low Level Phi 6 to Hotel Room Surfaces In the first scenario, hands were inoculated with 0.2 ml of the phi 6 suspension (10 7 PFU/ ml or 10 3 PFU/ml) and held at room tempera-

ture (23 ± 2 °C) for 30 min to dry to facilitate attachment. The investigator used the contami- nated hand to touch for 20 s each coupon sur- face: bed, carpet, hotel amenities, light switch, door handle, TV remote control, room curtain, leather, bathroom faucet, and stainless-steel coupons. Next, each coupon was placed in a stomacher bag and mixed for 2 min. Each item then underwent microbiological analysis. Scenario 2: Cross-Contamination From Inoculated Hotel Room Surfaces With High or Low Level Phi 6 to Hands For the second scenario, each hotel room surface was inoculated with 0.2 ml of phi 6 suspension (10 7 PFU/ml or 10 3 PFU/ml). The items were left to dry for 1 hr. During the drying time, hands were washed for 30 s using soap and warm water (40 °C). The washed hands were dried using paper towels, sprayed with 70% ethanol, and allowed to air dry. Next, the index finger (primary transfer) of each hand touched the contaminated hotel room surfaces for 20 s. Samples from the hands were collected using the glove-juice method (Larson et al., 1980; Sirsat et al., 2013) with brief modifica-

tions as detailed. The index finger from each hand touched the contaminated surfaces for 20 s, and then the hand was inserted into a sterile surgical glove containing 1 ml of ster- ile 0.02% PBST virus buer in the index fin- ger section. The hand with a glove on was vortexed for 60 s. The sample was then trans- ferred from the glove index finger region to a sterile 10-ml conical tube using a sterile pipette. The sample underwent further dilu- tion and viability plate count analyses. For both scenarios, the viability assay was performed by adding 1 ml from each collected sample (either after contaminated hands touched clean hotel room surfaces or clean hands touched contaminated hotel room surfaces), and a 100 µl of overnight host was added to a tube containing 3 ml of soft TSA, shaken by hand, and quickly poured onto TSA plates. The plates were allowed to solidify and then incubated for 24 hr at 22 °C. After incubation, the plaques were counted and recorded as PFU/cm 2 . Statistical Analyses The plaque-forming units from all experiments (persistence and simulation) were converted to

Volume 86 • Number 3

(3–4 days) compared with porous materials (2 days). One exception in our observations was that phi 6 survived 3 days on hotel room beds, which would be a porous material. The prolonged survival on hotel room beds could have large-scale implications for public health. The results of our study provide insight into the potential risks of high-touch surfaces for hotel guest rooms. Presently, it is of ulti- mate importance that the hotel industry pri- oritizes its cleaning and sanitizing programs to prevent virus transmission and to provide further assurance to customers. Our results demonstrate that future training and cleaning programs should include an increased focus on nonporous surfaces and bedding. Simulation of Cross-Contamination From Hands to Hotel Room Surfaces Hands were artificially contaminated with high and low concentrations of phi 6 (10 7 PFU/cm 2 or 10 3 PFU/cm 2 , respectively) and transfer rates were recorded. These data are presented in Table 2. In both experiments, leather had the lowest transfer rate of phi 6 at high and low concentrations (23% and 14%, respectively); the wooden desk had the highest transfer rate of phi 6 at high and low concentrations (58% and 38%, respectively). At the high concentration, the desk (58%), door handles (51%), and bathroom faucets (56%) had the highest transfer rate and had val- ues above 50%. All surfaces were found to be above the detection limit of 0.9 log PFU/cm 2 . At the low concentration, the lowest trans- fer rate was found for remote controls, cur- tains, and leather, all at 14%. All surfaces fell below the detection limit of 0.9 log PFU/cm 2 . Although phi 6 was detected in some samples, the final average of the six samples tested on all surfaces was below the detection limit, which indicates that viral transmission from hands to surfaces is not likely when hands become con- taminated with a low level of viruses. The results of our experiment at the high concentration inoculation are consistent with previous research that has demonstrated that hands play an important role in the trans- mission of various contaminants, including viruses (Ansari et al., 1991; Scott, 2013). Simulation of Cross-Contamination From Hotel Room Surfaces to Hands The phi 6 transfer rates from artificially con- taminated hotel room surfaces to hands at

TABLE 2

Transfer Rate of Phi 6 From Hands to Hotel Guest Room Surfaces

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 )

Log PFU/cm 2

Transfer Rate b (%)

Transfer Rate (%)

Log PFU/cm 2 a

Hands to Bed

1.9 ± 0.2

0.5 ± 0.4

Desk

2.5 ± 0.3

0.8 ± 0.3

Light switch

1.5 ± 0.1

0.7 ± 0.3

Door handle

2.2 ± 0.4

0.6 ± 0.3

Remote control

1.9 ± 0.3

0.3 ± 0.1

Room curtain

1.3 ± 0.2

0.3 ± 0.1

Hotel amenities

1.5 ± 0.3

0.4 ± 0.2

Leather

1.0 ± 0.2

0.3 ± 0

Bathroom faucet

2.4 ± 0.1

0.6 ± 0.3

a Mean and standard deviation of phi 6 from inoculated hands (10 7 or 10 3 PFU/cm 2 ) to hotel guest room surfaces after hands touched each surface for 20 s ( N = 6). b The transfer rate of mean and standard deviation of phi 6 from inoculated hands (10 7 or 10 3 PFU/cm 2 ) to hotel guest room surfaces after hands touched each surface for 20 s ( N = 6).

log 10; the survival rate curve was constructed using Microsoft Excel. For the cross-contami- nation analysis, means and standard deviations of log PFU/cm 2 were calculated. We calculated the transfer rate (%) following the formula obtained by Lopez et al. (2013): Percent transfer rates = (log PFU/cm 2 of phi 6 on recipient surface / log PFU/cm 2 of phi 6 on the original surface) × 100

cates was below the detection limit of 0.9 log PFU/cm 2 . The bathroom faucet had the last observed presence of phi 6 on day 7. Hotels are places where many people gather in close environmental conditions and have direct contact with surfaces. Therefore, any hygienic issues or poor environmental conditions in hotel areas and guest rooms make hotels a potential source of virus trans- mission (Park et al., 2019). Sifuentes et al. (2014) have shown that virus surrogates can transmit to other hotel rooms and parts of the hotel from contaminated surfaces by means of guests and housekeepers. The results of our study reveal that phi 6 contamination can be transmitted via fomi- tes to hands, increasing the likelihood of viral infection. The variability observed for the sur- vival of phi 6 among dierent hotel room sur- faces could be due to the type of each surface (e.g., porous versus nonporous). Viruses and their surrogates persist longer on nonporous surfaces compared with porous surfaces (Kasl- o et al., 2021; Lopez et al., 2013; Whitworth et al., 2020). Our study is consistent with these previous studies, demonstrating that phi 6 persisted longer on nonporous materials

Results and Discussion

Persistence of Phi 6 From Contaminated Hotel Room Surfaces Over 30 Days Table 1 shows the recovery of phi 6 on hotel room surfaces. The results indicate that phi 6 persisted for as long as 2 days on carpets, curtains, and leather coupon samples. We also found that phi 6 can persist for as long as 3 days on coupons of beds, wooden desks, door handles, and hotel amenities—and for as long as 4 days on light switches, remote controls, and bathroom faucets. Even though phi 6 appeared on some surfaces beyond the times previously mentioned, the average of the six samples collected from three repli-

October 2023 • Journal of Environmental Health

ADVANCEMENT OF THE SCIENCE

high (10 7 PFU/cm 2 ) and low (10 3 PFU/cm 2 ) concentrations are shown in Table 3. The transfer rates from surfaces to hands were found to be higher when compared with hands to surface. The only exceptions to this finding were at the low concentration, where hands to desk (37% versus 38%), door han- dle (28% versus 29%), and faucet (both 29%) were slightly higher or equal. At the high concentration, all surfaces were found to have transfer rates above 50% and above the detection limit of 0.9 log PFU/cm 2 . Bathroom faucets had the highest transfer rate at 74%. At the low concentra- tion, light switches had the highest transfer rate at 45% and were the only surface above the detection limit. Curtains had the lowest transfer rate at 20%. Previous research has indicated that clean- ing is an important factor for hotel selection by consumers and that specific customer seg- ments are willing to pay more for enhanced cleaning methods (Zemke et al., 2015). Thus, increased vigilance in cleaning procedures would be beneficial for public health as well as for hotel business. Conclusion According to our study results, phi 6 bacte- riophages—a surrogate of the SARS-CoV-2 virus—can survive for up to 4 days on light switches, remote controls, and bathroom faucets; up to 3 days on hotel room beds, wooden desks, door handles, and hotel ame- nities; and up to 2 days on the carpet, hotel room curtains, and leather coupon samples. Our findings suggest that high-touch areas in hotel guest rooms could be a potential source of virus transmission, and cross-contamina- tion from these surfaces to hands and vice versa is possible and perhaps even likely. Therefore, based on our data, it is recom- mended that hotel businesses establish stan- dard operating procedures (SOPs) to ensure that these potential hot spots are eectively

TABLE 3

Transfer Rate of Phi 6 From Hotel Guest Room Surfaces to 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 )

Log PFU/cm 2

Transfer Rate b (%)

Transfer Rate (%)

Log PFU/cm 2 a

Bed to hands Desk to hands Light switch to hands Door handle to hands Remote control to hands Room curtain to hands Hotel amenities to hands Leather to hands Bathroom faucet to hands

2.0 ± 0.2 1.6 ± 0.1 2.1 ± 0.2

50 63 57

0.4 ± 0.3 0.7 ± 0.2 0.9 ± 0.2

25 37 45

1.9 ± 0.3

0.5 ± 0.3

1.6 ± 0.4

0.6 ± 0.2

1.5 ± 0.3

0.3 ± 0

1.7 ± 0.1

0.4 ± 0.1

1.4 ± 0.1 2.3 ± 0.2

50 74

0.3 ± 0.1 0.6 ± 0.3

20 29

a Mean and standard deviation of phi 6 from each inoculated hotel guest room surface (10 7 or 10 3 PFU/cm 2 ) to hands after touching each inoculated surface for 20 s ( N = 6). b The transfer rate of mean and standard deviation of phi 6 from each inoculated hotel guest room surface (10 7 or 10 3 PFU/cm 2 ) to hands after touching each inoculated surface for 20 s ( N = 6).

cleaned to minimize the risk of potential virus transmission. Although CDC (2021) and AHLA (2020b) have provided enhanced cleaning and disinfecting guidelines to aid the hotel industry in specific protocols for minimizing risk, SOPs are still needed. The results from our study might not rep- resent a real-world hotel room environment, as our experiments were conducted under laboratory conditions and the surfaces were inoculated with a high concentration of phi 6 to simulate a worst-case scenario. Thus, more research is needed to investigate potential viral transmission via hotel room surfaces to confirm our findings.

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.

References

Almanza, B.A., Kirsch, K., Kline, S.F., Sirsat, S., Stroia, O., Choi, J.K., & Neal, J. (2015a). How clean are hotel rooms? Part I: Visual observations vs. microbiological contamination. Journal of Envi- ronmental Health , 78 (1), 8–13.

Almanza, B.A., Kirsch, K., Kline, S.F., Sirsat, S., Stroia, O., Choi, J.K., & Neal, J. (2015b). How clean are hotel rooms? Part II: Examin- ing the concept of cleanliness standards. Journal of Environmental Health , 78 (1), 14–18.

Volume 86 • Number 3

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