NEHA January/February 2023 Journal of Environmental Health

The January/February 2023 issue of the Journal of Environmental Health (Volume 85, Number 6), published by the National Environmental Health Association.

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Volume 85, No. 6 January/February 2023

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ABOUT THE COVER

Role of the Household Environment in Transmission of Clostridioides dicile Infection: A Scoping Review .......................................................................................................8

Competency in children’s environmental health allows for the development of interventions that can prevent the long-term and irreversible health outcomes

International Perspectives: Eect of Lockdown on the Air Quality of Four Major Cities in Pakistan During the COVID-19 Pandemic ............................................................................... 16

ADVANCEMENT OF THE PRACTICE

that result from early environmental toxic exposures. Despite the value of children’s environmental health, there are still gaps in workforce training for those interested in children’s environmental health. These gaps in knowledge and training highlight the need for improved ways to build the capacity of children’s environmental health professionals. In this month’s cover article, “Critical Competencies in Children’s Environmental Health,” the authors focused on creating a set of competencies for public health professionals interested in children’s environmental health careers as a way to meet the demand for children’s environmental health specialists. The article identifies 12 competencies that individuals can adopt to build their capacity as children’s environmental health professionals.

Special Report: Critical Competencies in Children’s Environmental Health ................................. 26

Direct From CDC/Environmental Health Services: Radon Outreach: Helping People See an Invisible Risk ......................................................................................................................... 30

The Practitioner’s Tool Kit: Personal Safety on the Job, Something to Consider ........................... 34

ADVANCEMENT OF THE PRACTITIONER

JEH Quiz #4............................................................................................................................... 15

Environmental Health Calendar ...............................................................................................36

Resource Corner........................................................................................................................ 37

See page 26.

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in the next Journal of Environmental Health don’t miss  Assessment of Chemical Exposures Investigation After Fire at an Industrial Chemical Facility  A Retrospective of the 2011 Fukushima Nuclear Disaster: An All- Hazards Emergency Management and Public Health Crisis Cycle Using Lessons Learned From the COVID-19 Pandemic  Columns from the Association of Environmental Health Academic

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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 6. 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.

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Volume 85 • Number 6

Walter S. Mangold Award

extraordinary adjective ex·traor·di·nary | ikˈstrôrd(ə)nˌerē 1. Going beyond what is usual, regular, or customary 2. Exceptional to a marked extent

Walter S. Mangold dedicated his life to the practice of environmental health in an extraordinary and exemplary way. In doing so, he became a beacon of excellence and inspiration for all environmental health pro- fessionals who followed after him. Do you have a colleague who fits the defini - tion of doing extraordinary environmental health work? Consider taking the time to nominate them for the Walter S. Mangold Award, our most prestigious award. Nomination Deadline: May 15, 2023 neha.org/mangold-award

Honoring a history of advancing environmental health. Walter F. Snyder was a pioneer in our field and was the cofounder and first executive director of NSF. He embodied outstanding accomplishments, notable contributions, demonstrated capacity, and leadership within environmental health. Do you know someone like that? Nominate them for the Walter F. Snyder Award for outstanding contributions to the advancement of environmental health. This award is cosponsored by NSF and NEHA. Nomination Deadline: May 1, 2023 neha.org/awards nsf.org/about-nsf/annual-awards Walter F. Snyder Award

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January/February 2023 • 7<96*4 7/ 6=29765.6;*4 .*4;1

YOUR ASSOCIATION

 PRESIDENT’S MESSAGE

Environmental Health Touches All Aspects of Our Lives

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

N ew is the year and new are the hopes, resolution, and spirits. All of us from the National Environ- mental Health Association (NEHA) wish you and your loved ones health, happiness, peace, and joy in the new year. ‘Tis the sea- son to enjoy the snow. As Linus Van Pelt from Peanuts said, “I never eat December snowflakes. I always wait until January.” In the New Year, environmental health professionals once again will be called on to lead the charge in developing solutions to address numerous challenges including climate change, emerging diseases, per- and polyfluoroalkyl substances (PFAS), nanoma- terials, and cyanobacteria (blue-green algae) blooms. Environmental health professionals are the Swiss Army knives of the scientific community with knowledge of numerous scientific disciplines, along with evaluation, management, problem solving, collaboration, communication, and conflict resolution skills practiced from the laboratory to the commu- nity. In knowledge-based communities we are the “thinks” in the Oh, the Thinks You Can Think! children’s book by Dr. Seuss. Most people do not realize how environ- mental health touches all aspects of our lives. You ensure the energy facilities used to power our homes do not pollute the air, land, or water, while also keeping the workforce of the energy sector safe. When having their morn- ing cup of co‘ee, most people do not realize the role we play to ensure that the water, cof- fee, and creamer are safe. More likely they get their java from the local co‘ee shop where we are at the forefront of food safety. Accord-

to as the public health revolution, occurred between 1880 and 1920, before the advent of antibiotics, advanced surgical techniques, and many other medical innovations. These public health improvements were led by envi- ronmental health professionals who worked to ensure clean air, safe food and water, and healthy places to live, work, and play. Addi- tional areas where environmental health professionals have helped increase U.S. life expectancy include motor vehicle, work- place, school, and recreational safety. Many residents of the U.S. and other devel- oped nations do not realize the impact envi- ronmental health issues have on many of our global neighbors. The World Health Organi- zation (WHO) states healthier environments could prevent almost one quarter of the global burden of disease. Poor water, sanitation, and hygiene conditions cause 842,000 diarrheal deaths every year. WHO states that the reduc- tion of environmental risks could prevent 1 in 4 child deaths. In 2012, 1.7 million deaths in children less than five years old were attribut- able to the environment. As my fellow Ken- tuckian John Prine sang, “It’s a big old goofy world,” and we will need to work together to reduce the global burden of disease. One reason the public does not recog- nize environmental health contributions is that our accomplishments are measured in nonevents. The public does not think of the numerous lives saved by our measures including mortality from cholera from drink- ing water, bubonic plague from a flea bite, carbon monoxide poisoning from a faulty furnace, or improper disposal of garbage that

ing to the Economic Research Service within the U.S. Department of Agriculture, 55% of food consumed last year was done outside of the home, which demonstrates the increasing importance of retail food safety. If we were living in the early 1800s, many of us reading this column would not be alive, having succumbed to disease. Up until the late 1800s, poor sanitation and living conditions, lack of proper sewage management, inad- equate treatment of drinking water, poor vec- tor control, and no food inspection or garbage collection were the status quo. Due to the hard work of environmental health professionals, the U.S. life expectancy has more than doubled to almost 80 years with vast improvements in not only health but also quality of life. Unfortunately, most people believe medi- cal advancements—including vaccines, germ theory, and antibiotics—are the reason for the majority of the increase in life expectancy in the U.S. The sanitary revolution in the mid-19th century began the control of dis- eases related to poor sanitary conditions. The greatest increase in life expectancy, referred Environmental health professionals are the Swiss Army knives of the scientific community.

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can contaminate drinking water. We are the invisible guardians protecting the public in numerous ways. The number of lives saved by our measures is dicult to quantify. In most cases, the public does not see our wins, only our failures. The media does not publicize nor do we report our successes, but they are quick to document our failures. We need to learn to emphasize the positive. We need to share how environmental health has improved numerous aspects of people’s daily lives, including participation in policy debates. When communicating with people, I follow Benjamin Franklin’s advice as much as possible: “Tell me and I forget, teach me and I remember, involve me and I learn.” From the Centers for Disease Control and Prevention (CDC) website: “CDC estimates that each year 1 in 6 Americans get sick from

contaminated food or beverages.” A more positive message would be food safety mea- sures in the U.S. have prevented illness in 5 out of 6 people, a food safety success rate of 84%. Car companies use positive advertis- ing to emphasize what consumers want in a car: safety, performance, or quality. Car com- panies do not focus on the negative. I have never heard or seen a car advertisement stat- ing that due to a warranty issue, only 10% of their customers had to bring in their vehicles for a repair in their first year of ownership. I feel that a quote by U.S. President The- odore Roosevelt from a speech given at the Sorbonne in Paris on April 23, 1010, sums up the e—orts of environmental health profes- sionals whose hard work to help our people and communities is often unrecognized. He stated that it is not the critic, the person who

points out who stumbles, or where things could have been done better that matter. What matters is the person in the field who strives to work for a worthy cause with devo- tion and enthusiasm while learning from their errors and failures. The full quote can be found at https://speakola.com/political/ theodore-roosevelt-man-in-the-arena-1910. I am honored to be in the arena with my fellow environmental health professionals. As Dory in Finding Nemo sang, “Just Keep Swimming,” which myself, my fellow pro- fessionals, and NEHA plan to keep doing to build, sustain, and empower an e—ective environmental health workforce to provide healthy environments for all.

gary.brown@eku.edu

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January/February 2023 • Journal of Environmental Health

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Role of the Household Environment in Transmission of Clostridioides difficile Infection: A Scoping Review

provided to patients on discharge, it did not contain adequate direction for patients to remove or inactivate C. dicile spores from their household environment. Most (66.7%, 30 out of 45) of the infection control profes- sionals who responded, however, thought that the household environment was impor- tant in the transmission of C. dicile (Egan et al., 2019). Nonetheless, one of the barriers to providing advice for an e˜ective house- hold hygiene protocol was a lack of knowl- edge about the role of the environment in the transmission of CDI in the household (Egan et al., 2019). Fecal–oral transmission of enteric patho- gens likely occurs in the household environ- ment (Curtis et al., 2003) and routine clean- ing could be insu›cient to remove pathogens (including C. dicile ) that can be present when a household member has an infection (Kagan et al., 2002). Researchers have specu- lated that the same principles of transmission and control of C. dicile that apply to health- care settings should apply also to households (Girotra et al., 2013). Specific studies of C. dicile transmission in the household envi- ronment, however, seem to be lacking. The objective of this scoping review was to describe the volume and breadth of scientific literature related to transmission of C. dicile in the household environment. Catherine D. Egan, MBA, CPHI(C), CIC Department of Pathobiology, University of Guelph Conestoga College Jan M. Sargeant, MSc, DVM, PhD, FCAHS Zoonoses, University of Guelph J. Scott Weese, DVSc, DVM, Dipl. ACVIM Department of Pathobiology and Centre for Public Health and Zoonoses, University of Guelph Andria Jones-Bitton, DVM, PhD Department of Population Medicine and Centre for Public Health and Department of Population Medicine and Centre for Public Health and Zoonoses, University of Guelph Shawn E. Zentner, MPH, CPHI(C) Wellington–Dufferin–Guelph Public Health

+:;9*,; The environment plays a role in healthcare-associated Clostridioides (formerly Clostridium ) dicile infection (CDI); however, the role of the environment in community-associated CDI is unknown. The objective of this scoping review was to describe the literature related to the transmission of C. dicile in the household environment. We conducted searches of four electronic health and science databases to identify relevant studies. In total, 39 articles published between 1981 and 2020 met the a priori inclusion criteria. Slightly over one half (51.3%, 20 out of 39) of the articles were nonsystematic review articles and thus we excluded them from the synthesis of results. Overall, we included 19 articles in the synthesis of results. None of the studies were experimental studies. Studies assessed or estimated the prevalence of C. dicile on household surfaces, colonization of household members (human and animal), or the risk of transmission in the household. This scoping review provides an overview of the global literature related to the role of the household environment in transmission of C. dicile . We found a lack of research in this area. Further studies are needed and ideally would be designed to follow household members over time and to test the e‹ectiveness of interventions such as targeted hygiene protocols.

Introduction Clostridioides dicile is a pathogen that has been recognized for decades. Historically, C. dicile infection (CDI) has been regarded as a healthcare-associated infection (Roth, 2016). Cases of CDI, however, are increas- ingly being identified in individuals without traditional risk factors for CDI (Delate et al., 2015), suggesting that infections are related to exposure in community settings. C. dicile spores survive in the environ- ment for several months, and transmission of C. dicile has been linked to contami- nated surfaces and the hands of healthcare professionals in healthcare settings (Kim et

al., 1981). Infection prevention and control practices in healthcare settings include strict environmental cleaning and disinfection pro- tocols. People with CDI can excrete C. dicile spores for many weeks posttreatment (Jinno et al., 2012; Riggs et al., 2007; Sethi et al., 2010), which is generally postdischarge from the healthcare setting. Therefore, it is likely that contamination of the household environment occurs, posing a risk to household inhabitants (both human and animal), including a risk of reinfection for the index case. A survey of infection control profession- als in hospitals in Ontario, Canada, deter- mined that if household hygiene advice was

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FIGURE 1

Flowchart of Records for Scoping Review for the Role of the Household Environment in the Transmission of Clostridioides difficile Infection

Records Identified Through Database Searches and Gray Literature Searches ( n = 1,320)

Additional Records Identified Through Hand Searching ( n = 10)

Records After Duplicates Removed ( n = 867)

Records Screened ( n = 867)

Records Excluded ( n = 607) Level 1 Screening ( n = 607)

Full Text Articles Assessed for Eligibility ( n = 260)

Full Text Articles Excluded, With Reason ( n = 206) Level 2 Screening ( n = 206) • Not about exposure, contamination, or transmission

in household environment ( n = 199) • No English version available ( n = 7)

Studies Included in Data Extraction ( n = 54)

Articles Excluded During Data Extraction, With Reason ( n = 15) • Animals were assessed in veterinary clinics, pet shops, or public lands ( n = 8) • Food but not in household ( n = 3) • Editorials that did not include outcome data ( n = 2) • Domestic animals were not pets ( n = 1) • Insufficient information specific to C. difficile ( n = 1)

Studies Meeting Inclusion Criteria ( n = 39)

Review Articles Removed From Synthesis of Results ( n = 20) Articles Included in Synthesis ( n = 19)

Methods This scoping review followed guidelines by Arksey and O’Malley (2005) and is reported using the Preferred Reporting Items for Sys- tematic Reviews and Meta-Analysis Exten- sion for Scoping Reviews (PRISMA-ScR) guidelines (Tricco et al., 2018). Prior to beginning the literature search, a protocol was registered in the University of Guelph institutional repository called the Atrium (https://hdl.handle.net/10214/21319). Studies were eligible if they described some aspect of transmission of C. dicile in the

household environment. Studies of humans and domestic animals within the household along with studies of the household environ- ment itself were eligible. Keyword searches included variations of the concepts for “household” and “trans- mission,” in addition to terms for C. dicile . We conducted searches using the following electronic databases through the McLaughlin Library, University of Guelph: CAB Direct, Web of Science(all database option), and CINAHL. We also searched PubMed via NCBI and conducted a search of the gray

literature. Then we searched Google Scholar for dissertation abstracts, government docu- ments, and other reports; only the first 200 citations in Google Scholar were screened for relevance due to the large number of citations identified (Bramer et al., 2017). Hand searching was conducted of the arti- cles’ reference lists where the study popula- tion included all three of the populations of interest. Authors were not contacted to iden- tify additional studies. All searches were conducted by the first author on September 27, October 15, and

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January/February 2023 • Journal of Environmental Health

ADVANCEMENT OF THE SCIENCE

December 21, 2020. Search strategies were adjusted for each platform to account for variations in syntax. No date restrictions were applied, and the language was restricted to English. Search results were uploaded into EndNo- teX8 Desktop reference management soft- ware. Duplicate references were removed using its de-duplication functionality. The EndNote library was uploaded into Distill- erSR systematic review software. Screening for eligibility of both title and abstract (level 1 screening) and full text (level 2 screening) was conducted by two of the authors, working independently. Training was provided and interrater reliability scoring was used to ensure consistency. Level 1 screening was conducted using the following questions: • Does the article discuss C. dicile ? • Is the article about contamination, expo- sure, or transmission in the household environment? If the reviewers agreed that the answer to either question was “no,” the article was excluded. Discrepancies between the review- ers were resolved by consensus. If reviewers agreed that the answer to both questions was “yes” or “unclear,” the article was moved into level 2 screening. Full text articles were acquired through University of Guelph library resources and uploaded into Distill- erSR to complete level 2 screening. Level 2 screening questions were evaluated independently by two reviewers using the fol- lowing questions: • Is the full text available in English? • Does the article describe contamination, transmission, or exposure of C. dicile in the household environment? If both reviewers answered “no” for either question, the article was excluded. Discrep- ancies between the reviewers were resolved by consensus. Figure 1 contains a decision flowchart outlining the inclusion and exclu- sion process. A data extraction form was created in Dis- tillerSR. Changes from the protocol were made to the data extraction form to provide additional options to characterize studies. Any conflicts were resolved through consen- sus. Data items extracted from the studies included characteristics, publication type, population studied, study design, study purpose, and study outcome. A short sum-

TABLE 1

Characteristics of Studies Identified in Scoping Review Process

Study Characteristic

# (%)

Study Characteristic

# (%)

Source ( N = 39) Journal

Population ( n = 19) * Environment

34 (87.2)

6 (31.6) 5 (26.3) 3 (15.7)

Editorial

2 (5.1) 1 (2.6) 1 (2.6) 1 (2.6) 1 (5.3) 1 (5.3) 1 (5.3) 1 (5.3) 1 (5.3)

Humans

Fact sheet

Environment, humans, and animals

Government report

Humans and animals

2 (10.5)

Textbook excerpt

Animals and environment Humans and environment

1 (5.3) 1 (5.3) 1 (5.3)

Year published ( n = 19) 1981

Animals

1983 2001 2010 2012 2013 2014 2016 2017 2018 2019 2020

Design ( n = 19) Prevalence

9 (47.4) 3 (15.7) 2 (10.5) 2 (10.5)

Case-control

Case series

2 (10.5)

Cross-sectional

1 (5.3)

Incidence

1 (5.3) 1 (5.3)

2 (10.5) 3 (15.7) 2 (10.5)

Case-control and quasi- experimental

Other (simulation)

1 (5.3)

1 (5.3)

Randomized controlled

0 (0) 0 (0)

3 (15.7)

Cohort

Location ( n = 19) U.S.

Results Short summaries of the included studies are provided, organized by study design (in order of frequency) and presented in the order of the population studied (humans, animals, environment, or combinations of these populations). Prevalence Studies A Japanese prevalence study published in 2001 involved the enrollment of 1,234 indi- viduals from seven groups: three classes of university students ( n = 234), workers at two hospitals ( n = 284), employees of a company ( n = 89), and self-defense force personnel ( n = 627) (Kato et al., 2001). Stool samples were Note . At the time of the literature review, the Berinstein et al. (2021) reference was prepublished online in 2020 prior to formal publication in 2021. As such, that reference is listed in this table as being published in 2020. *Cases or household contacts of a confirmed case were the specific subject of the studies with human populations. Studies of animals assessed domestic pets. Studies of the environment included surfaces as well as food in the household.

10 (52.6) 3 (15.8) 2 (10.5)

Canada

UK

Slovenia

2 (10.5)

Germany

1 (5.3) 1 (5.3)

Japan

mary of each study was also extracted by one author, which was not described in the protocol. Study design was determined based on the description of how the study was con- ducted (i.e., methodology, purpose of study, enrollment of subjects) rather than the decla- ration of study authors if there was inconsis- tency in declaration and methodology. Table 1 contains a description of the characteristics of the studies identified and included in this scoping review. Notably, there were no exper- imental studies identified. The data extracted from each study were exported from DistillerSRinto an Excel 2011 spreadsheet. Descriptive statistics and graphs were then generated.

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collected from subjects and follow-up stool cultures were requested 5–7 months later from individuals who were culture positive. Family members of culture-positive individu- als also provided stool samples to be exam- ined for colonization. A study conducted in the UK looked at the potential of pets as a reservoir of C. dif- ficile (Borriello et al., 1983). Fecal samples from dogs ( n = 52) and cats ( n = 20) were forwarded to researchers from veterinary hos- pitals and from colleagues to determine the prevalence of colonization with C. dicile . The earliest reported study that estimated the prevalence of C. dicile in the house- hold environment was published in 1981 in the U.S. (Kim et al., 1981). This study was conducted after the index case in an outbreak of C. dicile in a newborn intensive care unit experienced a recurrence of CDI after discharge home. The investigators collected samples from the bathroom (floor [ n = 15], sink cabinets [ n = 15], and inside toilet seat cover [ n = 10]); bedrooms (floor [ n = 15], bookcase [ n = 4], linens [ n = 10], and toys [ n = 15]); living room (crib [ n = 10]); utility room (floor [ n = 10], freezer door [ n = 5], and soiled clothing [ n = 10]); soil in yard ( n = 2); and tap water ( n = 2). Samples were also col- lected from a control home. A study conducted in Houston, Texas, examined 30 single family dwellings (Alam et al., 2014). Researchers collected 3–5 samples from each household. A total of 127 environmental samples from shoes ( n = 63), bathrooms ( n = 15), other household surfaces ( n = 37), and dust ( n = 12) were analyzed to determine prevalence of C. dicile in the household environment. Another study also conducted in Hous- ton, Texas, involved examining the soles of shoes ( n = 280), doorsteps ( n = 186), cleaning supplies ( n = 189), kitchens ( n = 191), and restrooms ( n = 189) in a convenience sample of 1,079 households over a 2-year period (2013–2015) to estimate prevalence of C. dif- ficile in the household environment (Alam et al., 2017). A study conducted in the U.S. reported the examination of 35 rural and urban house- holds to estimate the prevalence of C. di- cile in the environment (Rodriguez-Palacios et al., 2017). A total of 467 samples of food (collected from 188 kitchen pots or refrig- erators [no other detail provided]) and 278

samples of environmental surfaces (kitchen countertops [ n = 32], sinks [ n = 56], refrig- erator shelves [ n = 59], gloves [ n = 23], shoes [ n = 56], and washing machines [ n = 52]) were collected. One study in Slovenia of urban and rural households that had a dog involved sampling shoes, slippers, and dog paws to estimate the prevalence of C. dicile in the household environment (Janezic et al., 2018). In total, 20 households provided a total of 90 samples collected from dog paws ( n = 25), shoes ( n = 44), and slippers ( n = 21). Another study estimated prevalence of C. dicile in the outdoor household envi- ronment (Janezic et al., 2020). Researchers examined outdoor sites in the gardens of five households in Slovenia: four were rural households and one was from a suburban area. A total of five samples were taken at each house: three from the compost pile, one from the flower garden, and one from the vegetable garden. A study conducted in Southwestern Ontario, Canada, to estimate the prevalence of C. dicile involved collection of environ- mental samples from 9 locations in each of 84 households in a convenience sample of households that had a dog (Weese et al., 2010). The sample locations were the kitchen sink and tap ( n = 84), refrigerator shelf ( n = 84), toilet ( n = 83), kitchen counter ( n = 84), vacuum cleaner contents ( n = 81), and any pet food bowls ( n = 84). The study also assessed colonization of dogs ( n = 139) and cats ( n = 14) from these households. Case-Control Studies A study published in the U.S. used records of military dependents receiving healthcare to evaluate risk factors related to community- associated CDI, including exposure to a fam- ily member with CDI (Adams et al., 2017). Cases were identified as those with diagnostic codes for CDI and were matched on age and sex with three controls (i.e., individuals with- out diagnosis codes for CDI). A second study published in the U.S. evalu- ated risk factors for young children acquir- ing CDI (Weng et al., 2019). C. dicile cases were identified via the Emerging Infections Program of the Centers for Disease Control and Prevention. Controls were randomly chosen from a commercial database of tele- phone numbers or from birth registries; con-

trols resided in the same surveillance catch- ment area. Exposure to household members who had CDI, diarrhea, or wore diapers was evaluated, as were various foods (including eggs, dairy, raw vegetables, plant-based pro- tein, red meat, poultry, seafood, and well or spring water) as potential risk factors for CDI. A third study in the U.S. was conducted with patients who were CDI positive ( n = 435) and CDI negative ( n = 461) (Berinstein et al., 2021). Cases and controls were identi- fied using electronic medical records and then verified by manual chart review. An electronic survey was administered to assess household exposures to pets as well as intake of meat, dairy, and salad as potential risk factors. Case Series Studies A case series report published as an edito- rial in the UK reported results of a study conducted to determine the presence of CDI. The researchers searched a database of microbiological reports to identify cases of CDI with the same address or surname as a case (Baishnab et al., 2013). Individuals who appeared to live in the same household as a case were contacted for further investigation into their experiences related to CDI. A case series study conducted in the U.S. involved telephone interviews with commu- nity-associated CDI cases ( n = 984) to ask about frequency of exposure to household members with CDI, exposure to household pets, and consumption of food (i.e., chicken, beef, pork, lamb) during a typical week (Chitnis et al., 2013). Cases were classified into one of three levels of exposure based on the information provided in the inter- view. Stool samples were also collected from a convenience sample (40%) of the inter- viewed patients. The samples were cultured for C. dicile . Cross-Sectional Studies A study published in the U.S. to assess risk of transmission within family contacts included individuals from households with two or more members enrolled in the same health insurance plan (Miller et al., 2020). Cases of CDI were identified using diagnostic codes. Individuals were assigned to one of four groups based on their exposure to a family member (i.e., family member with CDI diag- nosis in the prior 60 days or not) and their CDI status (i.e., positive or negative).

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A German cross-sectional study involved enrollment of a convenience sample of geo- graphically diverse households ( n = 415) that had a dog and/or a cat. The study aim was to estimate frequency of possible exposures to pets as a source of C. dicile (Rabold et al., 2018). Fecal samples were collected from companion animal owners ( n = 578) and animals ( n = 1,447) to determine CDI status (i.e., positive or negative) as well as gather information on intensity of contact between owners and pets (e.g., sleeping in same bed, washed in tub or shower, licking face of owner) and health status of the humans (e.g., diarrhea, chronic disease). Incidence Study A Canadian study was conducted with patients who had been diagnosed with CDI in tertiary care centers to measure incidence in household contacts (Loo et al., 2016). Case participants ( n = 51) and household contacts ( n = 67) provided stool or rectal swabs and responded to a survey on risk fac- tors on enrollment. The swabs and survey were repeated during home visits that were conducted monthly for 4 months. The study defined probable transmission in household contacts (i.e., humans or animals) as con- version of a negative to positive C. dicile result on one of the monthly fecal samples with an identical or closely related pulsed- field gel electrophoresis (PFGE) pattern as the index case.

24), remote controls ( n = 24), and telephones ( n = 24) during all household visits. The study also involved collection of stool samples from household contacts ( n = 12) of index cases of patients with recurrent CDI who were undergoing FMT and were ana- lyzed for C. dicile colonization. Informa- tion on household cleaning practices (e.g., frequency and use of bleach), hand hygiene, and CDI knowledge was also collected. Fecal samples were also collected from pets ( n = 8) in households of individuals about to undergo or who had recently undergone FMT and compared with pets in households of those controls without CDI. Compari- sons were made between cases and controls (case-control) and before and after FMT (quasi-experimental). Simulation Study A simulation study conducted in Canada involved the review of CDI cases in the data- base of a Quebec hospital (Pépin et al., 2012). Cases in the same household were identified by searching the hospital database to find individuals with the same phone number at the time of diagnosis. Census data were used to estimate the number of spouses, parents, and children of the cases and to estimate the expected number of cases in household members to calculate an estimated risk of transmission to household contacts living with a case of CDI.

ervoirs of C. dicile —but by nature of their design, they lack control groups and are there- fore not appropriate to evaluate risk factors associated with CDI infection. Most of the outcomes of the studies could be considered process or proxy outcomes in the sense that they are not measuring the most desirable outcome of incidence of CDI in response to transmission of C. di- cile . The complexity of the transmission of C. dicile makes it a dišcult disease to study with respect to definitively identifying when transmission of an infection has occurred. A sušcient (and currently undefined) num- ber of C. dicile spores must be ingested and subsequent disruption of the intestinal microbiome must also happen for an infec- tion to occur, but there can be significant time in between these two occurrences. This review identified only one study that defined and measured probable transmission within household members and that study followed subjects only for a 4-month period (Loo et al., 2016). This lack of longitudinal studies designed to estimate transmission risk is a significant gap in knowledge. C. dicile is known to colonize in humans and animals and to survive in the environ- ment, including in food and water (Warriner et al., 2017). While the specific transmission dynamics in the household are unknown, there is likely to be interaction among these three reservoirs. Only three studies identified by this review used a holistic or One Health approach to examine all potential C. dicile reservoirs in the household (i.e., humans, animals, and the environment). Future stud- ies should be designed to consider all risks in household transmission. Limitations While the goal of this review was to identify all research related to C. dicile transmission in the household environment, it is possible that some relevant research was not identified in our search. One limitation of this study is that it did not intentionally search for stud- ies related to C. dicile using “domestic pets” or “food” in the search terms because these studies might not be limited to the house- hold environment. Thus, studies related to these two elements could have been missed. There was also a potential for language bias, because we excluded seven articles because they were in a language other than English.

Discussion

Case-Control and Quasi- Experimental Study

Summary of Evidence This scoping review describes the literature examining household transmission of C. dif- ficile. The results highlight several gaps in knowledge about the role of the household environment in transmission of C. dicile . There were no experimental studies among the literature identified in this review, which is significant, as experimental studies provide an opportunity to minimize confounding factors and provide greater evidence to infer causal- ity than observational studies (Dohoo et al., 2012). The studies that were most common in the current body of literature were prevalence studies of C. dicile in humans, animals, or the environment, the results of which cannot be used to infer causality related to the cause of infection. Prevalence studies can be infor- mative in identifying the environmental res-

A U.S. study involved adults experiencing recurrent CDI who were scheduled for fecal microbiota transplantation (FMT) as treat- ment (Shaughnessy et al., 2016). Cases were identified from patients at a University of Minnesota gastroenterology clinic. Controls were matched on age and geographic location and were recruited from outside the health- care setting. The investigators visited each of the 16 participating households (8 of the individuals undergoing FMT and 8 controls). The households of those undergoing FMT were visited twice (7 days prior and 10 days post-FMT). Environmental samples were col- lected from vacuum cleaners ( n = 27), toilets ( n = 30), bathrooms ( n = 29), computers ( n = 24), bathroom doors and light switches ( n = 27), microwaves ( n = 24), refrigerators ( n =

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Conclusion The findings of this scoping review indicate a lack of research on the risk of transmission of C. dicile in the household environment. This lack of research is a barrier to under- standing the risks posed to others in the household by a household member (human or animal) who is positive for C. dicile , and of the risk the environment poses to a person with nonhealthcare-associated risk factors for developing C. dicile .

Further studies designed to follow CDI patients over time and to measure out- comes—such as development of CDI in household contacts, studies designed to test the eectiveness of interventions such as targeted hygiene for household con- tacts, or environmental decontamination to prevent the development of CDI—would be helpful to better understand how the household environment might contribute to this infection. This knowledge would

enable the creation of consistent household decontamination advice for CDI patients and those at risk of acquiring an infection of C. dicile . Corresponding Author: Catherine D. Egan, Department of Pathobiology, University of Guelph, 50 Stone Road E, Guelph, ON, N1G 2W1, Canada. Email: cegan01@uoguelph.ca.

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