Advertisement

Hygienic monitoring in long-term care facilities using ATP, crAssphage, and human noroviruses to direct environmental surface cleaning

Published:February 23, 2022DOI:https://doi.org/10.1016/j.ajic.2021.11.014

      Highlights

      • All surfaces were contaminated with crAssphage or high levels of organic debris
      • Without a recent outbreak, noroviruses were not found on the LTC facility surfaces
      • The highest levels of ATP and/or crAssphage were in patient rooms and public areas.
      • Hygienic monitoring identified where cleaning efforts could be heightened
      • Information is helpful in guiding infection control procedures in LTC facilities

      Abstract

      Background

      Norovirus and C. difficile are associated with diarrheal illnesses and deaths in long-term care (LTC) facilities and can be transmitted by contaminated environmental surfaces. Hygienic monitoring tools such as adenosine triphosphate (ATP) bioluminescence and indicators of fecal contamination can help to identify LTC facility surfaces with cleaning deficiencies.

      Methods

      High-touch surfaces in 11 LTC facilities were swabbed and tested for contamination by norovirus, a fecal indicator virus, crAssphage, and ATP which detects organic debris. High levels of contamination were defined as log ATP relative light unit values or crAssphage log genomic copy values in the 75th percentile of values obtained from each facility.

      Results

      Over 90% of surfaces tested positive for crAssphage or gave failing ATP scores. Norovirus contamination was not detected. Handrails, equipment controls, and patient beds were 4 times more likely than other surfaces or locations to have high levels of crAssphage. Patient bed handrails and tables and chairs in patient lounges had high levels of both ATP and crAssphage.

      Conclusions

      Surfaces with high levels of ATP and crAssphage were identified. Quantifying levels of contamination longitudinally and before and after cleaning might enhance infection prevention and control procedures for reducing diarrheal illnesses in LTC facilities.

      Key Words

      Abbreviations:

      C. difficile (Clostridioides difficile), CDI (C. difficile infection), LTC (long-term care), ATP (adenosine triphosphate), PCR (polymerase chain reaction), RT-PCR (reverse transcriptase PCR)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Infection Control
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

      1. National Action Plan to Prevent Health Care-Associated Infections: Road Map to Elimination. Phase III. Long-term care facilities (2013): https://health.gov/our-work/health-care-quality/health-care-associated-infections/national-hai-action-plan#P3. Last updated July 24, 2020. Accessed March 16, 2021.

        • Hall AJ
        • Wikswo ME
        • Pringle K
        • Gould LH
        • Parashar UD
        Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, CDC. Vital signs: foodborne norovirus outbreaks - United States, 2009-2012.
        MMWR Morb Mortal Wkly Rep. 2014; 63 (PMID: 24898166; PMCID: PMC5779359): 491-495
        • Lindsay L
        • Wolter J
        • De Coster I
        • Van Damme P
        • Verstraeten T.
        A decade of norovirus disease risk among older adults in upper-middle and high income countries: a systematic review.
        BMC Infect Dis. 2015; 15 (PMID: 26467099; PMCID: PMC4606836): 425
        • Montoya A
        • Cassone M
        • Mody L.
        Infections in nursing homes: epidemiology and prevention programs.
        Clin Geriatr Med. 2016; 32 (PMID: 27394025): 585-607
        • Jump RL
        • Donskey CJ.
        Clostridium difficile in the long-term care facility: prevention and management.
        Curr Geriatr Rep. 2015; 4: 60-69
      2. Centers for Disease Control and Prevention. Guidelines for environmental infection control in health-care facilities: recommendations of CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC) (2013).https://www.cdc.gov/infectioncontrol/pdf/guidelines/environmental-guidelines-P.pdf. Last updated April 2019. Accessed April 20, 2021.

        • Jayasekara L
        • Leone CM
        • Sharp J
        • Fraser A.
        Preventing and controlling human noroviruses in South Carolina long-term care facilities: an analysis of institutional policies and procedures.
        Am J Infect Control. 2016; 44 (PMID: 26769281): 24-29
        • Nante N
        • Ceriale E
        • Messina G
        • Lenzi D
        • Manzi P.
        Effectiveness of ATP bioluminescence to assess hospital cleaning: a review.
        J Prev Med Hyg. 2017; 58: E177-E183
        • Boxman IL
        • Verhoef L
        • Dijkman R
        • Hägele G
        • Te Loeke NA
        • Koopmans M
        Year-round prevalence of norovirus in the environment of catering companies without a recently reported outbreak of gastroenteritis.
        Appl Environ Microbiol. 2011; 77: 2968-2974
        • Leone CM
        • Dharmasena M
        • Tang C
        • et al.
        Prevalence of human noroviruses in commercial food establishment bathrooms.
        J Food Prot. 2018; 81: 719-728
        • Oristo S
        • Rönnqvist M
        • Aho M
        • et al.
        Contamination by norovirus and adenovirus on environmental surfaces and in hands of conscripts in two Finnish garrisons.
        Food Environ Virol. 2017; 9: 62-71
        • Dutilh BE
        • Cassman N
        • McNair K
        • et al.
        A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes.
        Nat Commun. 2014; 5: 4498
        • Farkas K
        • Adriaenssens EM
        • Walker DI
        • McDonald JE
        • Malham SK
        • Jones DL.
        Critical evaluation of CrAssphage as a molecular marker for human-derived wastewater contamination in the aquatic environment.
        Food Environ Virol. 2019; 11: 113-119
        • Park GW
        • Ng TFF
        • Freeland AL
        • et al.
        CrAssphage as a novel tool to detect human fecal contamination on environmental surfaces and hands.
        Emerg Infect Dis. 2020; 26: 1731-1739
        • Stachler E
        • Kelty C
        • Sivaganesan M
        • Li X
        • Bibby K
        • Shanks OC.
        Quantitative CrAssphage PCR assays for human fecal pollution measurement.
        Environ Sci Technol. 2017; 51: 9146-9154
        • Sifuentes LY
        • Fankem SL
        • Reynolds K
        • Tamimi AH
        • Gerba CP
        • Koenig D.
        Use of ATP readings to predict a successful hygiene intervention in the workplace to reduce the spread of viruses on fomites.
        Food Environ Virol. 2017; 9: 14-19
        • Shama G
        • Malik DJ.
        The uses and abuses of rapid bioluminescence-based ATP assays.
        Int J Hyg Environ Health. 2013; 216: 115-125
        • Park GW
        • Chhabra P
        • Vinjé J.
        Swab sampling method for the detection of human norovirus on surfaces.
        J Vis Exp. 2017; 120: 55205
        • Cannon JL
        • Barclay L
        • Collins NR
        • et al.
        Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses.
        J Clin Microbiol. 2017; 55: 2208-2221
        • Suleyman G
        • Alangaden G
        • Bardossy AC.
        The role of environmentalcontamination in the transmission of nosocomial pathogens and healthcare-associated infections.
        Curr Infect Dis Rep. 2018; 20: 12
        • Lopman B
        • Gastañaduy P
        • Park GW
        • Hall AJ
        • Parashar UD
        • Vinjé J.
        Environmental transmission of norovirus gastroenteritis.
        Curr Opin Virol. 2012; 2: 96-102
        • Rutala WA
        • Weber DJ.
        Best practices for disinfection of noncritical environmental surfaces and equipment in health care facilities: a bundle approach.
        Am J Infect Control. 2019; 47S (PMID: 31146858): A96-A105
        • Weber DJ
        • Rutala WA
        • Miller MB
        • Huslage K
        • Sickbert-Bennett E.
        Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.
        Am J Infect Control. 2010; 38 (PMID: 20569853): S25-S33
        • Amodio E
        • Dino C.
        Use of ATP bioluminescence for assessing the cleanliness of hospital surfaces: a review of the published literature (1990-2012).
        J Infect Public Health. 2014; 7: 92-98
        • Hardy K
        • Abbott G
        • Bashford S
        • et al.
        Can measuring environmental cleanliness using ATP aid in the monitoring of wards with periods of increased incidence of Clostridium difficile?.
        J Infect Prev. 2014; 15: 31-35
        • Griffith CJ
        • Obee P
        • Cooper RA
        • Burton NF
        • Lewis M.
        The effectiveness of existing and modified cleaning regimens in a Welsh hospital.
        J Hosp Infect. 2007; 66: 352-359
        • Lewis T
        • Griffith C
        • Gallo M
        • Weinbren M.
        A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces.
        J Hosp Infect. 2008; 69: 156-163
        • Mulvey D
        • Redding P
        • Robertson C
        • et al.
        Finding a benchmark for monitoring hospital cleanliness.
        J Hosp Infect. 2011; 77: 25-30
        • Boyce JM
        • Havill NL
        • Dumigan DG
        • Golebiewski M
        • Balogun O
        • Rizvani R.
        Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay.
        Infect Control Hosp Epidemiol. 2009; 30: 678-684
        • Lee YM
        • Kim DY
        • Park KH
        • Lee MS
        • Kim YJ.
        Monitoring environmental contamination caused by SARS-CoV-2 in a healthcare facility by using adenosine triphosphate testing.
        Am J Infect Control. 2020; 48: 1280-1281
        • Sherlock O
        • O'Connell N
        • Creamer E
        • Humphreys H.
        Is it really clean? An evaluation of the efficacy of four methods for determining hospital cleanliness.
        J Hosp Infect. 2009; 72: 140-146
        • Watanabe R
        • Shimoda T
        • Yano R
        • et al.
        Visualization of hospital cleanliness in three Japanese hospitals with a tendency toward long-term care.
        BMC Res Notes. 2014; 7: 121
        • Solomon SL
        • Plisko JD
        • Wittig SM
        • et al.
        Reducing environmental surface contamination in healthcare settings: a statewide collaborative.
        Am J Infect Control. 2018; 46: e71-e73
        • Mitchell BG
        • McGhie A
        • Whiteley G
        • et al.
        Evaluating bio-burden of frequently touched surfaces using Adenosine Triphosphate bioluminescence (ATP): results from the Researching Effective Approaches to Cleaning in Hospitals (REACH) trial.
        Infect Dis Health. 2020; 25: 168-174
        • Chau JPC
        • Liu X
        • Lo SHS
        • Chien WT
        • Wan X.
        Effects of environmental cleaning bundles on reducing healthcare-associated Clostridioides difficile infection: a systematic review and meta-analysis.
        J Hosp Infect. 2020; 106: 734-744
        • Park GW
        • Williamson KJ
        • DeBess E
        • et al.
        High hand contamination rates during norovirus outbreaks in long-term care facilities.
        Infect Control Hosp Epidemiol. 2018; 39: 219-221
        • Fajardo-Cavazos P
        • Schuerger AC
        • Nicholson WL.
        Persistence of biomarker ATP and ATP-generating capability in bacterial cells and spores contaminating spacecraft materials under earth conditions and in a simulated Martian environment.
        Appl Environ Microbiol. 2008; 74: 5159-5167
        • Smith PW
        • Beam E
        • Sayles H
        • et al.
        Impact of adenosine triphosphate detection andfeedback on hospital room cleaning.
        Infect Control Hosp Epidemiol. 2014; 35: 564-569