Advertisement

Evaluating hygienic cleaning in health care settings: What you do not know can harm your patients

  • Philip C. Carling
    Correspondence
    Address correspondence to Philip C. Carling, MD, director of Hospital Epidemiology, Carney Hospital, 2100 Dorchester Ave, Boston, MA 02124.
    Affiliations
    Infectious Diseases Section, Department of Medicine, Boston University School of Medicine, Boston, MA; and VP Epidemiology Consulting Services, Inc (ECSI), Detroit, MI
    Search for articles by this author
  • Judene M. Bartley
    Affiliations
    Infectious Diseases Section, Department of Medicine, Boston University School of Medicine, Boston, MA; and VP Epidemiology Consulting Services, Inc (ECSI), Detroit, MI
    Search for articles by this author
      Recent studies using direct covert observation or a fluorescent targeting method have consistently confirmed that most near patient surfaces are not being cleaned in accordance with existing hospital policies while other studies have confirmed that patients admitted to rooms previously occupied by patients with hospital pathogens have a substantially greater risk of acquiring the same pathogen than patients not occupying such rooms. These findings, in the context recent studies that have shown disinfection cleaning can be improved on average more than 100% over baseline, and that such improvement has been associated with a decrease in environmental contamination of high touch surfaces, support the benefit of decreasing environmental contamination of such surfaces. This review clarifies the differences between measuring cleanliness versus cleaning practices; describes and analyzes conventional and enhanced monitoring programs; addresses the critical aspects of evaluating disinfection hygiene in light of guidelines and standards; analyzes current hygienic practice monitoring tools; and recommends elements that should be included in an enhanced monitoring program.

      Key Words

      The medical and economic toll of infections with increasingly antibiotic resistant pathogens has continued to escalate. Whereas efforts to improve hand hygiene and isolation practices have been implemented to help mitigate this problem, recent studies have documented the limitation of such interventions.
      • Silvestri L.
      • Petros A.J.
      • Sarginson R.E.
      • de la Ca M.A.
      • Murray A.E.
      • van Saene H.K.F.
      Handwashing in the intensive care unit: a big measure with modest effects.
      • Rupp M.E.
      • Fitzgerald T.
      • Puumala S.
      • Anderson J.R.
      Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units.
      • Kirkland K.B.
      Taking off the gloves: toward a less dogmatic approach to the use of contact isolation.
      • Morgan D.J.
      • Diekema D.J.
      • Spkowitz K.
      • Perencevich E.N.
      Adverse outcomes associated with contact precautions: a review of the literature.
      Although active surveillance protocols and rigorous adherence to precautions may decrease methicillin-resistant Staphylococcus aureus (MRSA) transmission, in certain settings
      • Huang S.S.
      • Yokoe D.S.
      • Hinrichsen V.L.
      • Spurchise L.S.
      • Datta R.
      • Miroshink I.
      • et al.
      Impact of routine intensive care unit surveillance cultures and resultant barrier precautions on hospital-wide methicillin-resistant Staphylococcus aureus bacteremia.
      such interventions have not decreased overall nosocomial infection rates in several northern European countries, which remain similar to rates in southern European countries and the United States,
      • Department of Health
      Winning ways. Working together to reduce health care associated infection in England. Report from the Chief Medical Officer.
      and have not been shown to be consistently effective or necessary in this country.
      • Diekema D.J.
      • Edmond M.B.
      Look before you leap: active surveillance for multidrug-resistant organisms.
      It has now been well documented that a wide range of particularly environmentally resilient hospital-acquired infection (HAI) pathogens can be readily cultured from near patient surfaces.
      • Kramer A.
      • Schwebke I.
      • Kampf G.
      How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
      • Dancer S.J.
      The role of environmental cleaning in the control of hospital-acquired infection.

      Speck K, Naegeli A, Shangraw A, Ross LT, Speser S, Margarakis LL, et al. Environmental contamination with antimicrobial resistant organisms (MDROs). Abstract 157. Annual Meeting of the Society for Healthcare Epidemiology of America. Baltimore, MD. April 2007.

      Eight recent studies have now confirmed that patients occupying rooms previously occupied by patients with vancomycin-resistant Enterococcus (VRE),
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      • Martinez J.A.
      • Ruthazer R.
      • Hansjosten K.
      • Barefoot L.
      • Snydman D.R.
      Role of environmental contamination as a risk factor for acquisition of vancomycin-resistant enterococci in patients treated in a medical intensive care unit.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Drees M.
      • Snydman D.R.
      • Schmid C.H.
      • Barefoot L.
      • Hansjosten K.
      Antibiotic exposure and room contamination among patients colonized with vancomycin-resistant enterococci.

      Datta R, Platt R, Kleinman K, Huang SS. Impact of an environmental cleaning intervention on the risk of acquiring MRSA and VRE from prior room occupants. Abstract 273. Annual Meeting of the Society for Healthcare Epidemiology of America. San Diego, CA. March 2009.

      MRSA,
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Drees M.
      • Snydman D.R.
      • Schmid C.H.
      • Barefoot L.
      • Hansjosten K.
      Antibiotic exposure and room contamination among patients colonized with vancomycin-resistant enterococci.

      Datta R, Platt R, Kleinman K, Huang SS. Impact of an environmental cleaning intervention on the risk of acquiring MRSA and VRE from prior room occupants. Abstract 273. Annual Meeting of the Society for Healthcare Epidemiology of America. San Diego, CA. March 2009.

      • Hardy K.J.
      • Oppenheim B.A.
      • Gossain S.
      • Gao F.
      • Hawkey P.M.
      A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA.
      Clostridium difficile,

      Shaugnessy M, Micielli R, Depestel D, Arndt J, Strachan C, Welcch K, et al. Evaluation of hospital room assignment and acquisition of Clostridium difficile associated diarrhea. Abstract K-4194. Presented at the 48th Annual ICAAC/IDSA 46th Annual Meeting. Washington, DC. October 2008.

      and Acinetobacter baumannii
      • Wilks M.
      • Wilson A.
      • Warwick S.
      • Price E.
      • Kennedy D.
      • Ely A.
      • et al.
      Control of an outbreak of multidrug-resistant Acinetobacter baumannii calcoaceticus colonization and infection in an intensive care unit (ICU) without closing the ICU or placing patients in isolation.
      infection or colonization have on average a 73% increased risk of acquiring the same pathogen than patients not occupying such rooms (Fig 1). Over the past 4 years, 8 studies using direct covert observation or a fluorescent targeting method have confirmed that only 40% of near patient surfaces are being cleaned in accordance with existing hospital policies.
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      • Carling P.C.
      • Briggs J.
      • Hylander D.
      • Perkins J.
      An evaluation of patient area cleaning in 3 hospitals using a novel targeting methodology.
      • Boyce J.M.
      • Havill N.L.
      • Dumigan D.G.
      • Golebiewski M.
      • Balogun O.
      • Rizvani R.
      Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay.
      • Eckstein B.C.
      • Adams D.A.
      • Eckstein E.C.
      • Rao A.
      Reduction of Clostridium difficile and vancomycin-resistant enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      • Jefferson J.
      • Whelan R.
      • Dick B.
      • Carling P.C.
      A novel technique to identify opportunities for improving environmental hygiene in the operating room.

      Guerrero D, Carling PC, Jury L, Ponnada S, Nerandzic M, Eckstein EC, et al. Beyond the “Hawthorne effect”: reduction of Clostridium difficile environmental contamination through active intervention to improve cleaning practices. Abstract 60. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      Carling PC, Po JL, Bartley J, Herwaldt L. Identifying opportunities to improve environmental hygiene in multiple health care settings. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      These findings, in the context of the fact that 11 studies have now shown that the thoroughness of disinfection cleaning can be improved to 82% (on average more than 100% over baseline)
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      • Eckstein B.C.
      • Adams D.A.
      • Eckstein E.C.
      • Rao A.
      Reduction of Clostridium difficile and vancomycin-resistant enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.L.
      • Von Beheren S.
      for the Healthcare Environmental Hygiene Study Group
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      • Po J.L.
      • Burke R.
      • Sulis C.
      • Carling P.C.
      Dangerous cows: an analysis of disinfection cleaning of computer keyboards on wheels.
      • Hota B.
      • Blom D.W.
      • Lyle E.A.
      • Weinstein R.A.
      • Hayden M.K.
      Interventional evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.

      Bruno-Murtha LA, Harkness D, Stiles T, Han L, Carling PC. Molecular epidemiology of MRSA during an active surveillance program. Abstract 53. Society for Healthcare Epidemiology of America 19th Annual Meeting. San Diego, CA. March 19-22, 2009.

      Wiline J, Blum N, Fisher V, Douglas G, Flanagan G, Ostrosky L. The “A team”: an environmental services intervention to control multidrug-resistant Acinetobacter. Abstract 589. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      Sulis C, Estanislano R, Wedel S, Carling PC. Completeness of cleaning critical care transport vehicles. Abstract 648. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      Clark P, Young L, Silvestri S, Muto CA. Goo begone—evaluation of compliance with cleaning of multiple high touch (HT) surfaces using fluorescent “Goo.” Abstract 210. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      Carling PC, Eck EK. Achieving sustained improvement in environmental hygiene using coordinated benchmarking in 12 hospitals. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      and the fact that such improvement has been associated with an on average 68% decrease in environmental contamination of “high-risk objects,”
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      • Eckstein B.C.
      • Adams D.A.
      • Eckstein E.C.
      • Rao A.
      Reduction of Clostridium difficile and vancomycin-resistant enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.

      Guerrero D, Carling PC, Jury L, Ponnada S, Nerandzic M, Eckstein EC, et al. Beyond the “Hawthorne effect”: reduction of Clostridium difficile environmental contamination through active intervention to improve cleaning practices. Abstract 60. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      • Hota B.
      • Blom D.W.
      • Lyle E.A.
      • Weinstein R.A.
      • Hayden M.K.
      Interventional evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.
      • Dancer S.J.
      • White L.F.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      together support the likely benefit of decreasing environmental contamination of such surfaces. In addition, 5 studies have recently shown that improved routine disinfection cleaning practice is associated with an average 40% decrease in transmission of VRE,
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      • Martinez J.A.
      • Ruthazer R.
      • Hansjosten K.
      • Barefoot L.
      • Snydman D.R.
      Role of environmental contamination as a risk factor for acquisition of vancomycin-resistant enterococci in patients treated in a medical intensive care unit.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Drees M.
      • Snydman D.R.
      • Schmid C.H.
      • Barefoot L.
      • Hansjosten K.
      Antibiotic exposure and room contamination among patients colonized with vancomycin-resistant enterococci.

      Datta R, Platt R, Kleinman K, Huang SS. Impact of an environmental cleaning intervention on the risk of acquiring MRSA and VRE from prior room occupants. Abstract 273. Annual Meeting of the Society for Healthcare Epidemiology of America. San Diego, CA. March 2009.

      • Hota B.
      • Blom D.W.
      • Lyle E.A.
      • Weinstein R.A.
      • Hayden M.K.
      Interventional evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.
      MRSA,

      Datta R, Platt R, Kleinman K, Huang SS. Impact of an environmental cleaning intervention on the risk of acquiring MRSA and VRE from prior room occupants. Abstract 273. Annual Meeting of the Society for Healthcare Epidemiology of America. San Diego, CA. March 2009.

      • Dancer S.J.
      • White L.F.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      and A baumannii.
      • Wilks M.
      • Wilson A.
      • Warwick S.
      • Price E.
      • Kennedy D.
      • Ely A.
      • et al.
      Control of an outbreak of multidrug-resistant Acinetobacter baumannii calcoaceticus colonization and infection in an intensive care unit (ICU) without closing the ICU or placing patients in isolation.
      Figure thumbnail gr1
      Fig 1Summary of studies that provide support for improving heath care environmental cleaning practice.

      Guidelines and standards

      During the past 6 years, there has been a dramatic evolution of recommendations and standards as well as state laws related to improving environmental hygiene in health care settings. In 2003, the Centers for Disease Control and Prevention (CDC) Guidelines for Environmental Infection Control in Healthcare Facilities—Environmental Surfaces recommended that hospitals clean and disinfect “high-touch surfaces.”
      Centers for Disease Control and Prevention/Healthcare Infection Control Advisory Committee (HICPAC) Guidelines for environmental infection control in health care facilities.
      A subsequent CDC guideline strongly recommended (category 1B) that hospitals “monitor (ie, supervise and inspect) cleaning performance to ensure consistent cleaning and disinfection of surfaces in close proximity to the patient and likely to be touched by the patient and health care professionals.”
      • Siegel J.D.
      • Rhinehart E.
      • Jackson M.
      • Chiarello L.
      Healthcare Infection Control Practices Advisory Committee.
      As a consequence of these recommendations, the 2007 revised Center for Medicare and Medicaid Services Interpretative Guideline for its infection control standard now requires that the infection prevention and control program of hospitals “must include appropriate monitoring of housekeeping activities to ensure that the hospital maintains a sanitary environment.”

      Centers for Medicare and Medicaid. State operations manual. Appendix A. Interpretive guidelines for hospitals. Available from: http://cms.hhs.gov/manuals/Downloads/som107ap_a_hospitals.pdf. Accessed January 31, 2010.

      These documents, as well as similar ones in Great Britain and Canada, reflect an evolving mandate that patient area environmental hygiene in health care settings be objectively analyzed and optimized.
      • Pratt R.J.
      • Pellowe C.M.
      • Wilson J.A.
      • Loveday H.P.
      • Harper P.J.
      • Jones S.R.
      • et al.
      Epic 2: national evidence-based guidelines for preventing healthcare-associated infections in NHS hospitals in England.
      Health Canada Laboratory Centre for Disease Control Bureau of Infectious Diseases Nosocomial and Occupational Infections: infection control guidelines: handwashing, cleaning, disinfection and sterilization in healthcare.

      Evaluating environmental cleaning practice

      Problem-oriented environmental monitoring

      As a result of studies that linked environmental contamination with the transmission of Staphylococcus aureus in the late 1950s, attempts were made to use swab-based environmental culturing for S aureus as a means for evaluating low-level disinfection cleaning practice in many hospitals. Although the practice diminished in value as the prevalence of S aureus in HAIs decreased and the unreliability of sporadic poorly standardized environmental culturing became evident, environmental surface culturing continues to have a role in infection prevention practice. The CDC pointed to the lack of environmental standards for routine sampling but also identified its value if used properly for research or education.
      Centers for Disease Control and Prevention/Healthcare Infection Control Advisory Committee (HICPAC) Guidelines for environmental infection control in health care facilities.
      The use of environmental cultures has greatly enhanced our understanding of the epidemiology of C difficile transmission
      • Dumford III, D.M.
      • Nerandzic M.M.
      • Eckstein B.C.
      • Donskey C.J.
      What is on that keyboard? Detecting hidden environmental reservoirs of Clostridium difficile during an outbreak associated with North American pulsed-field gel electrophoresis type 1 strains.
      • Sethi A.K.
      • Al-Nassir W.N.
      • Nerandzic M.M.
      • Bobulsky G.S.
      • Donskey C.J.
      Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection.
      as well as MRSA
      • Chang S.
      • Sethi A.K.
      • Eckstein B.C.
      • Stiefel U.
      • Cadnum J.L.
      • Donskey C.J.
      Skin and environmental contamination with methicillin-resistant Staphylococcus aureus among carriers identified clinically versus through active surveillance.
      and VRE.
      • Hayden M.K.
      • Blom D.W.
      • Lyle E.A.
      • Moore C.G.
      • Weinstein R.A.
      Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients' environment.
      • Sethi A.K.
      • Al-Nassir W.N.
      • Nerandzic M.M.
      • Donskey C.J.
      Skin and environmental contamination with vancomycin-resistant enterocci in patients receiving oral metronidazole or oral vancomycin treatment for Clostridium difficile-associated disease.
      Such cultures have also been useful in evaluating the role of environmental contamination in outbreak settings involving C difficile,
      • Riggs M.M.
      • Sethi A.K.
      • Zabarsky T.F.
      • Eckstein E.C.
      • Jump R.L.
      • Donskey C.J.
      Asymptomatic carriers area potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents.
      • Kaatz G.
      • Gitlin S.
      • Schaberg D.
      • Wilson K.
      Acquisition of Clostridium difficile from the hospital environment.
      Acinetobacter,
      • Denton M.
      • Wilcox M.
      Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit.
      VRE,
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      MRSA,
      • Boyce J.M.
      • Potter-Bynoe G.
      • Chenevert C.
      • King T.
      Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications.
      and glycopeptide insensitive S aureus.
      • de Lassence A.
      • Hidri N.
      • Timsit J.F.
      • Joly-Guillou M.L.
      Control and outcome of a large outbreak of colonization and infection with glycopeptide-intermediate Staphylococcus aureus in an intensive care unit.
      Although potentially useful, logistical challenges involved in the collection of a large enough number of cultures to permit proper epidemiologic analysis, the cost of data collection and specimen analysis (typically including pulse-field gel electroforesis or other strain identification process) as well as the intrinsic challenge of drawing epidemiologically sound conclusions from possibly erratic fluctuations in environmental contamination as a result of unknown confounding variables represent important challenges related to problem-oriented environmental monitoring. Given these issues, the possible short- and long-term benefits of such information make it prudent to weigh carefully the overall value of collecting such data.

      Conventional environmental cleaning monitoring

      The ongoing evaluation and monitoring of cleaning interventions to reduce the risk of transmission of environmental pathogens through defined procedures have been elements of infection prevention and control practice in acute care hospitals for many years. Until recently, such evaluation has exclusively relied on visual assessment of the cleanliness of surfaces. Currently, 89% of a large sample of US acute care hospitals confirmed that they perform visual assessments of cleanliness during regular environment of care rounds as the primary means for evaluating cleaning practice in their hospitals.
      • Rollins G.
      How clean is clean? New technologies, monitoring practice gains traction.
      The elements of what can be considered “conventional” monitoring of low-level disinfection or environmental cleaning (EC) are outlined in Fig 2. Traditionally, such rounds are performed on a regular basis and involve the infection preventionist (IP) and director of emergency services (ES) as well as an administrative representative from patient care services. Together, these individuals visit several patient care areas to monitor compliance with a range of safety practices and to assess visual cleanliness. The identified deficiencies, as they pertain to potential pathogen transmission issues, are reviewed and remedial activities approved by the infection control committee. Such assessment of EC, known as a “visual audit” in Great Britain, relies on the observation of visible soilage of surfaces by potentially infectious material or dust and dirt.
      • Dancer S.J.
      The role of environmental cleaning in the control of hospital-acquired infection.
      Such findings are assumed to represent practice failures by the individual or individuals directly responsible for “ensuring”
      • Siegel J.D.
      • Rhinehart E.
      • Jackson M.
      • Chiarello L.
      Healthcare Infection Control Practices Advisory Committee.
      the microbial safety of the surface in question. Whereas conventional monitoring may identify sporadic gross lapses in cleaning practice as summarized in Fig 3, this practice has a number of limitations including the following:
      • An inability to objectively assess actual EC practice;
      • the reliance on episodic negative findings as a basis for remedial individual and programmatic interventions;
      • placement of undue emphasis on the cleanliness of floors and walls, which have limited roles in pathogen transmission,
        • Maki D.G.
        • Alvarado C.J.
        • Hassemer C.A.
        • Zilz M.A.
        Relation of an inanimate hospital environment to endemic nosocomial infection.
        • Ayliffe G.A.J.
        • Collins D.M.
        • Lowbury E.J.L.
        Cleaning and disinfecting hospital floors.
        because of the ease with which gross contamination or dirt can be visually documented on these surfaces;
      • with the exception of gross contamination by potentially infected material, a low sensitivity for defining what represents a microbiologically “dirty” surface;
      • poor correlation with microbial contamination, namely, what appears to be clean may harbor substantial levels of microbial contamination
        • Malik R.E.
        • Cooper R.A.
        • Griffith C.J.
        Use of audit tools to evaluate the efficacy of cleaning systems in hospitals.
        Department of Health
        Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning.
        ;
      • poor programmatic specificity, ie, what may appear to represent a lapse in EC may not be;
      • intrinsically subjective with a high potential for observer bias;
      • the direct involvement of ES management and patient care leadership in a monitoring system with low sensitivity and specificity, which may lead to inconsistent and potentially misdirected responses to what appear to be lapses in EC;
      • an inability to evaluate other than daily EC practice;
      • limited ability to support The Joint Commission (TJC) standard EC.04.01.03.EP2, which states that the institution must be able to demonstrate that it “uses the results of data analysis to identify opportunities to resolve environmental safety issues”

        The Joint Commission Standards 2010. Available from: http://www.jointcommission.org/Standards/. Accessed January 30, 2010.

        ;
      • limited ability to demonstrate compliance with the Center for Medicare Services (CMS)

        Centers for Medicare and Medicaid. State operations manual. Appendix A. Interpretive guidelines for hospitals. Available from: http://cms.hhs.gov/manuals/Downloads/som107ap_a_hospitals.pdf. Accessed January 31, 2010.

        Conditions for Participation (CoP), section 482.42.;
      • the need to utilize substantial leadership level personnel resources;
      • a limited ability to evaluate more than a small sample of patient care areas on a frequent basis; and
      • an inability to define and respond to institutional or interinstitutional standards of EC through benchmarking.
      Figure thumbnail gr2
      Fig 2A comparison of the elements of conventional hygienic monitoring with enhanced programs.
      Figure thumbnail gr3
      Fig 3A comparison of the advantages and limitations of conventional versus enhanced programmatic monitoring of EC process.
      As an adjunct to such conventional monitoring activities, 78% of hospitals also analyze patient satisfaction surveys to evaluate EC.
      • Rollins G.
      How clean is clean? New technologies, monitoring practice gains traction.
      Whereas such surveys may episodically identify gross lapses in EC, the very poor specificity and sensitivity of such surveys make it challenging to use them to evaluate overall practice within an institution.

      Enhanced EC monitoring

      In response to an evolving understanding of the importance of the near-patient environment (also referred to as the “patient zone”)
      • Sax H.
      • Allegranzi B.
      • Uckay I.
      • Larson E.
      • Boyce J.
      • Pittet D.
      “My five moments of hand hygiene”: a user-centered design approach to understand, train, monitor and report hand hygiene.
      in the transmission of health care-associated pathogens (HAP) as well as studies that identified opportunities for improving EC,
      • Dancer S.J.
      Mopping up hospital infection.
      • Griffith C.J.
      • Cooper R.A.
      • Gilmore J.
      • Davies C.
      • Lewis M.
      An evaluation of hospital cleaning regimes and standards.
      • Carling P.C.
      • Parry M.F.
      • Von Beheren S.M.
      Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.
      an objective and substantially more structured approach to monitoring such activities has recently evolved. As currently practiced and summarized in Fig 2, the basic components of “Enhanced” EC monitoring encompasses the following elements:
      • Uses an objective monitoring tool to evaluate the process of EC;
      • is performance rather than deficiency oriented;
      • is based on the development of an independently functioning structured monitoring program incorporating specific EC policy-based expectations and goals;
      • relies on the repetitive monitoring of actual EC by trained, unbiased individuals on an ongoing basis; and
      • is incorporated independently into the institution's ongoing quality improvement process through the infection control committee.
      As summarized in Fig 3, the advantages of such an enhanced program include the following elements:
      • Allows for the direct evaluation of the process of hygienic cleaning;
      • incorporates a built-in standardization and uniformity of evaluation;
      • incorporates ES staff education based on specific objectively evaluable expectations;
      • facilitates the development of a program that has a high potential for identifying specific as well as systemic institutional programmatic issues that limit or adversely impact EC;
      • allows for short cycle monitoring of ES staff performance with direct feedback to improve EC and documents the sustainability of improvements, once they have been achieved;
      • has the potential for using positive performance achievement to reinforce good performance and the value of such performance in the context of the institution's objectively defined patient safety goals;
      • has the ability to objectively identify and document individual EC oversights and the need for remedial action;
      • represents a system easily adaptable to established process improvement (PI) modalities such as the Plan-Do-Act (PDA) cycle, Positive Deviance, Six sigma, and others;
      • facilitates compliance with TJC standards;
      • facilitates compliance with CMS CoP mandates;
      • provides objective performance information for internal and interinstitutional benchmarking;
      • allows for use of the same monitoring systems for one-on-one and small group, hands-on, education; and
      • facilitates the use of the same process improvement system over a range of practices and venues within the hospital and potentially other health care settings.
      It is beyond the scope of the current discussion to provide a complete cost/benefit analysis of these programs, but, in light of current financial constraints, one additional advantage worth noting is that, overall in a large study of 36 hospitals, the program appears to be resource neutral, with less than a 1% increase in ES resources.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.L.
      • Von Beheren S.
      for the Healthcare Environmental Hygiene Study Group
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      Although enhanced EC monitoring has a range of advantages, several limitations to its use have so far been identified (Fig 3), including the following:
      • The need to develop and implement a new program often in a setting of limited IPs' resources;
      • the critical need for administrative support for successful implementation and maintenance of the ongoing program;
      • the need to maintain a positive, blameless, close working relationship between IP and ES leadership;
      • complexities associated with the need (or at least value) of covertly collecting a preintervention assessment of EC to optimize subsequent data analysis and education; and
      • potential monitoring tool issues.
      Whereas objective monitoring of practice has evolved as the cornerstone of enhanced programs, the incorporation of patient survey results and problem-based interventions constitute important components of the overall program.

      Analysis of hygienic practice monitoring tools

      Whereas the advantages of enhanced EC monitoring in contrast to the limitations of conventional monitoring provide support for hospitals implementing programs to objectively monitor EC, the advantages and limitations of various monitoring approaches and tools must also be considered. As summarized in Fig 4 and noted below, there are currently 5 systems that may be potentially useful for enhanced programmatic monitoring.
      Figure thumbnail gr4
      Fig 4Summary of the 5 methods used in evaluating environmental hygiene.

      Covert practice observation

      Covertly monitoring EC can provide an objective assessment of individual ES staff performance and compliance with cleaning protocols. This approach has been used to evaluate and improve environmental hygiene related to VRE transmission in one hospital. Hayden et al utilized a trained research observer to covertly monitor daily disinfection cleaning of 8 high-risk objects in an intensive care unit during the 2-month baseline portion of the study.
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      Thoroughness of disinfection cleaning was then monitored following educational interventions along with immediate feedback during cleaning by the research staff. As a result, the thoroughness of environmental cleaning improved from 48% to 87%, and VRE transmission decreased significantly. Although clearly effective, logistical issues related to maintaining such a program outside a research setting could limit adaptation of this form of EC monitoring as a process improvement intervention.

      Swab cultures

      As noted previously, swab cultures of surfaces have been utilized in a range of clinical settings to study the environmental epidemiology of many HAPs as well as in the evaluation of outbreaks related to specific organisms. Whereas several outbreak intervention studies have attributed favorable outcomes to improved EC in association with decreased environmental contamination by target organisms, none of the reports specifically note whether serial environmental culture results were actually used to provide EC practice feedback to the ES staff. In a single study evaluating the impact of various programmatic and educational interventions to improve disinfection cleaning of intensive care unit keyboards, the confirmation of VRE contamination was used effectively to improve cleaning performance.
      • Po J.L.
      • Burke R.
      • Sulis C.
      • Carling P.C.
      Dangerous cows: an analysis of disinfection cleaning of computer keyboards on wheels.
      Broth-enriched swab cultures to quantify bacterial contamination of patient area surfaces have been used in a single study, along with Adeneinetriphosphate (ATP) results, to provide direct feedback to ES staff.
      • Boyce J.M.
      • Havill N.L.
      • Lipka A.
      • Havill H.
      • Rizvani R.
      Variations in hospital daily cleaning practices.
      In this study, overall ATP scores improved following feedback, but the impact on actual bacterial contamination was not reported. Although swab cultures are easy to use, the cost of processing, including isolate identification (if needed), the delay in analyzing results, the need to develop baseline values for comparisons, and the limited feasibility of monitoring multiple surfaces in multiple patient rooms as part of an ongoing EC monitoring program in other than a research setting may be issues that could limit the broad application of such a system for evaluating EC practice.

      Agar slide cultures

      Agar-coated glass slides with finger holds were developed to simplify quantitative cultures of liquids. The slides have been adopted for use in environmental surface monitoring to assess the limitations of visual audits of EC.
      • Griffith C.J.
      • Cooper R.A.
      • Gilmore J.
      • Davies C.
      • Lewis M.
      An evaluation of hospital cleaning regimes and standards.
      Subsequently, several studies have used agar-coated slide systems to evaluate cleaning practice as well as to compare cleaning regimens
      • Griffith C.J.
      • Obee P.
      • Cooper R.A.
      • Burton N.F.
      • Lewis M.
      The effectiveness of existing and modified cleaning regimens in a Welsh hospital.
      • Dancer S.J.
      • White L.
      • Robertson C.
      Monitoring environmental cleanliness on two surgical wards.
      by quantifying aerobic colony counts (ACCs) per square centimeter
      • Griffith C.J.
      • Obee P.
      • Cooper R.A.
      • Burton N.F.
      • Lewis M.
      The effectiveness of existing and modified cleaning regimens in a Welsh hospital.
      • Dancer S.J.
      • White L.F.
      • Lamb J.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      as well as to compare cleaning regimens.
      • Griffith C.J.
      • Obee P.
      • Cooper R.A.
      • Burton N.F.
      • Lewis M.
      The effectiveness of existing and modified cleaning regimens in a Welsh hospital.
      • Dancer S.J.
      • White L.F.
      • Lamb J.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      Although 2 studies
      • Griffith C.J.
      • Obee P.
      • Cooper R.A.
      • Burton N.F.
      • Lewis M.
      The effectiveness of existing and modified cleaning regimens in a Welsh hospital.
      • Cooper R.A.
      • Griffith C.J.
      • Malik R.E.
      • Obee P.
      Monitoring the effectiveness of cleaning in four British hospitals.
      measured ACCs before and after cleaning, no studies to date have evaluated the actual thoroughness of cleaning of the same objects to determine whether objects with relatively high ACCs surfaces were either poorly cleaned or actually overlooked by the ES staff. Although some difficulties have been encountered in utilizing the agar contact culturing on other than large, flat surfaces, they potentially provide an easy method for quantifying viable microbial surface contamination. There is a need, similar to that noted above for swab cultures, to develop baseline values for accurate interpretation of study findings. Agar-coated slides and dedicated incubation systems are commercially available.

      Fluorescent gel

      A monitoring system using an essentially invisible transparent gel that dries on surfaces following application and resists abrasion was developed specifically to evaluate the thoroughness of environmental cleaning in health care settings. Following the identification of opportunities to improve cleaning in 23 hospitals,
      • Carling P.C.
      • Parry M.F.
      • Von Beheren S.M.
      Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.
      use of the system within a structured process improvement program led to the thoroughness of disinfection cleaning improving from 48% to 77% in 36 study hospitals.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.L.
      • Von Beheren S.
      for the Healthcare Environmental Hygiene Study Group
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      The same system was subsequently used by Goodman et al to evaluate EC in 10 intensive care units in a single hospital. Following performance feedback, the thoroughness of cleaning improved from 44% to 71%.
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      Further analysis of this study has confirmed that improved EC was associated with decreased MRSA and VRE transmission.

      Datta R, Platt R, Kleinman K, Huang SS. Impact of an environmental cleaning intervention on the risk of acquiring MRSA and VRE from prior room occupants. Abstract 273. Annual Meeting of the Society for Healthcare Epidemiology of America. San Diego, CA. March 2009.

      Most recently, the same monitoring tool and PI system were used in coordination with group performance benchmarking and facilitated program analysis in 12 hospitals within a single health care system.

      Carling PC, Eck EK. Achieving sustained improvement in environmental hygiene using coordinated benchmarking in 12 hospitals. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      Average thoroughness of terminal room disinfection cleaning improved significantly with 11 of the 12 study hospitals achieving sustained rates of improved cleaning to 85% or above. However, as noted in Fig 4, the fluorescent gel system cannot be used to measure actual cleanliness of surfaces but only thoroughness of cleaning practice. For this reason, the system must be used in conjunction with environmental cultures for problem-oriented hygienic monitoring as discussed previously. The system is commercially available for use in acute care hospitals on a subscription basis.

      ATP bioluminescence

      The measurement of organic ATP on surfaces using a luciferase assay and luminometer has been used to evaluate cleanliness of food preparation surfaces for more than 30 years.
      • Thorn A.
      • Lundin A.
      • Ansehn S.
      Firefly luciferase ATP assay as a screening method for bacteriuria.
      A specialized swab is used to sample a standardized surface area, which is then analyzed using a portable handheld luminometer. The amount of ATP, both microbial and nonmicrobial, is quantified and expressed as relative light units (RLU). Although readout scales vary more than 10-fold
      • Anderson B.M.
      • Rasch M.
      • Kvist J.
      • Tollefsen T.
      • Lukkassen R.
      • Sandvik L.
      • et al.
      Floor cleaning: effect on bacteria and organic materials in hospital rooms.
      and sensitivity varies between commercially available systems,
      • Simpson W.J.
      • Gilells C.J.
      • Flockhart H.A.
      Repeatability of hygiene test systems in measurement of low levels of ATP.
      very low readings are typically associated with low ACCs on food preparation surfaces.
      • Aycicek H.
      • Oguz U.
      • Karci K.
      Comparison of results of ATP bioluminescence and traditional hygiene swabbing methods for the determination of surface cleanliness at a hospital kitchen.
      Very high RLU readings may represent either the viable bioburden, organic debris including dead bacteria, or a combination of both. Indeed, a recent study has found that debris accounts for approximately 66% of ATP on surfaces.
      • Griffith C.J.
      • Cooper R.A.
      • Gilmore J.
      • Davies C.
      • Lewis M.
      An evaluation of hospital cleaning regimes and standards.
      The clinical relevance of this issue was clarified by Griffith et al
      • Griffith C.J.
      • Malik R.
      • Cooper R.A.
      • Looker N.
      • Michaels B.
      Environmental surface cleanliness and the potential for contamination during handwashing.
      as well as in a study of ambient contamination of surfaces potentially touched following handwashing based on proposed cleanliness standards.
      • Lewis T.
      • Griffith C.
      • Gallo M.
      • Weinbren M.
      A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces.
      A mean ATP RLU reading of 3707 was found on the 618 surfaces tested, with 89% failing to meet the <500 RLU level in a proposed standard. In contrast, only 27% (168/618) of the same surfaces had ACCs above the proposed ACC cleanliness standard of <2.5 (colony-forming units)/cm2. In 2007, a study was undertaken by the National Health Service to evaluate the potential role the ATP tool in evaluating EC in hospitals.
      Department of Health
      Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning.
      While noting limitations in the ATP system, the authors concluded that the tool could potentially be used effectively for education of ES staff, although an evaluation of such use was not part of the study design. Although it is likely that part of the lack of correlation between ATP readings and ACCs noted in the preceding studies relates to the fact that ATP systems measure organic debris as well as viable bacterial counts, several studies have noted additional environmental factors that may increase or decrease ATP readings, including residual detergent and disinfectants that may either increase of decrease RLU readings,
      • Green T.A.
      • Russell S.M.
      • Fletcher D.L.
      Effect of chemical cleaning agents and commercial sanitizers on ATP bioluminescence measurements.
      plasticisers found in microfiber cloths,
      • Brown E.
      • Eder A.R.
      • Thompson K.M.
      Do surface and cleaning chemistries interfere with ATP measurement systems for monitoring patient room hygiene?.
      ammonium compounds found in laundry chemistries,
      • Brown E.
      • Eder A.R.
      • Thompson K.M.
      Do surface and cleaning chemistries interfere with ATP measurement systems for monitoring patient room hygiene?.
      and surfaces in poor condition.
      • Griffith C.J.
      • Cooper R.A.
      • Gilmore J.
      • Davies C.
      • Lewis M.
      An evaluation of hospital cleaning regimes and standards.
      Additional logistical limitations of the ATP tool include the need to develop baseline values, to evaluate a surface within a few minutes of cleaning,
      • Lewis T.
      • Griffith C.
      • Gallo M.
      • Weinbren M.
      A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces.
      and the inability to use the system when a bleach-based disinfectant is being used for cleaning.
      • Boyce J.M.
      • Havill N.L.
      • Lipka A.
      • Havill H.
      • Rizvani R.
      Variations in hospital daily cleaning practices.
      Boyce et al
      • Boyce J.M.
      • Havill N.L.
      • Lipka A.
      • Havill H.
      • Rizvani R.
      Variations in hospital daily cleaning practices.
      used preintervention ACCs along with ATP results in education of the ES. Subsequently, individual housekeepers were asked to clean a room that they were told would be monitored by the ATP system following cleaning. As a result of these interventions, the authors documented significant improvement in the daily cleaning of 4 near-patient surfaces as measured by the ATP system.
      • Boyce J.M.
      • Havill N.L.
      • Lipka A.
      • Havill H.
      • Rizvani R.
      Variations in hospital daily cleaning practices.
      Luminometers and specimen collection swabs are available from several commercial sources.

      Cleanliness versus cleaning practice

      When choosing an evaluation method for use in an enhanced program of EC monitoring, it is important to consider whether the cleaning process or the actual cleanliness of surfaces is to be monitored. Observation and fluorescent gel systems directly evaluate the cleaning process, but the swab or slide culture as well as ATP bioluminescence systems measure cleanliness. Although the latter 3 systems could be used to monitor hygienic cleaning practice, to do so necessitates monitoring the surface to be evaluated both before and after cleaning because a proportion of surfaces may actually be clean prior to monitoring as a result of their being cleaned previously and not yet contaminated at the time of monitoring.
      • Boyce J.M.
      • Havill N.L.
      • Lipka A.
      • Havill H.
      • Rizvani R.
      Variations in hospital daily cleaning practices.
      • 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.
      Furthermore, the intrinsically low concentration of most major HAPs on surfaces limits the use of pathogen-specific monitoring as a means for assessing actual practice.
      • Dancer S.J.
      • White L.
      • Robertson C.
      Monitoring environmental cleanliness on two surgical wards.
      • 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.
      • Hamilton D.
      • Foster A.
      • Ballantyne L.
      • Kingsmore P.
      • Bedwell D.
      • Hall T.J.
      • et al.
      Performance of ultramicrofibre cleaning technology with or without addition of a novel copper-based biocide.
      Although it is conceptually possible to effectively monitor hygienic cleaning with the latter systems, defining the level of microbial contamination that actually correlates with good or poor EC in a clinical setting has yet to be defined objectively.

      General elements of enhanced monitoring programs

      The most critical aspect of implementing an enhanced hygienic monitoring program relates to the need for the program to be developed from its inception as a joint “blame-free” undertaking between the infection prevention team and the ES leadership. The program must be based on the mutual understanding of the need to optimize patient and health care personnel environmental pathogen/contaminant transmission safety through mutually developed policies and procedures as well as structured, objective performance monitoring. Whereas the CMS standard states that “monitoring housekeeping activities” represents a defined component of the responsibilities of “infection control,”

      Centers for Medicare and Medicaid. State operations manual. Appendix A. Interpretive guidelines for hospitals. Available from: http://cms.hhs.gov/manuals/Downloads/som107ap_a_hospitals.pdf. Accessed January 31, 2010.

      the development of a mutually supportive approach to maximizing patient and health care personnel safety through optimized EC has been critical to programmatic success.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.L.
      • Von Beheren S.
      for the Healthcare Environmental Hygiene Study Group
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.

      Carling PC, Eck EK. Achieving sustained improvement in environmental hygiene using coordinated benchmarking in 12 hospitals. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      CMS sees infection prevention and control more programmatically, ie, it is everyone's responsibility. The program in this case needs ownership by major stakeholders, eg, environmental services and infection prevention specialists to be a continuous performance improvement process, with measures that can be appreciated by all participants.
      Logistical issues must also be considered as part of planning for the implementation of an enhanced program. Before a decision has been made to use one of the approaches to objectively monitor cleaning practice, it is important to determine the number of data points that must be monitored on a regular basis to accurately assess practice. Although it would be ideal to be able to identify small fluctuations in practice accurately, such an approach would be highly labor intensive. As noted in Fig 5, the sample size needed to accurately detect a 10% variation in cleaning practice within the range of baseline cleaning thoroughness found by the Healthcare Environmental Hygiene Study Group hospitals (20%-80%) is quite substantial.
      • Chow S.
      • Shao J.
      • Wang H.
      Sample size calculations in clinical research.
      In contrast, monitoring of only 50 to 120 surfaces would be needed to accurately detect a 20% change in practice. Given the range of patient zone objects monitored in the published reports of hygienic practice, which vary from 8
      • Hayden M.K.
      • Bonten M.J.
      • Blom D.W.
      • Lyle E.A.
      Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
      to 15,
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      a reasonably accurate determination of thoroughness of cleaning practice could be determined by monitoring 10 to 15 representative patient rooms per evaluation cycle depending on the estimated overall thoroughness of cleaning anticipated.
      Figure thumbnail gr5
      Fig 5The relationship between the number of high-risk objects evaluated and the ability to detect significant change in the thoroughness of cleaning.
      In addition, it is important, while considering the benefits of enhanced programmatic monitoring of EC, not to overlook the intrinsic importance of standardizing and optimizing cleaning processes, equipment, and disinfectant/cleaning system use to realize the full benefits of more thorough cleaning of high-risk surfaces in the patient zone.

      Summary

      Although basic monitoring of EC using visual assessment can identify gross lapses in practice, it has recently become evident that opportunities to improve the thoroughness of patient zone surface cleaning exist within a range of health care settings with only 34% of surfaces in 8 different health care settings being cleaned according to policy.
      • Aycicek H.
      • Oguz U.
      • Karci K.
      Comparison of results of ATP bioluminescence and traditional hygiene swabbing methods for the determination of surface cleanliness at a hospital kitchen.
      In the context of careful epidemiologic studies that have confirmed a substantially increased risk of acquiring HAPs from prior room occupants and the clear documentation that thoroughness of environmental hygiene can be objectively evaluated and improved through structured interventions and that improved cleaning of high-risk surfaces both decreases environmental contamination and patient acquisition of HAPs, it would appear that there is clear support for hospitals and other health care facilities to consider the importance of optimizing EC in the patient zone. Although the implementation of the type of enhanced hygienic monitoring program outlined above will facilitate compliance with TJC and CMS standards, it is also important to note that such programs meet the specifications of the Department of Health and Human Services Action Plan to Prevent Healthcare Associated Infections (June 2009), which states the following: “Standardized methods (ie, performance methods) that are feasible, valid, and reliable” should be used “for measuring and reporting compliance with broad-based HAI prevention practices that must be practiced consistently by a large number of health care personnel.”

      US Department of Health and Human Services. Final action plan to prevent healthcare-associated infections. June 2009. Available from: http://www.hhs.gov/ophs/initiatives/hai/infection.html. Accessed September 28, 2009.

      Carrying out such a systematic program with measurable achievements and goals can receive deserved visibility by being included in the chief executive officer and Board of Trustee's dashboard on a quarterly basis. Given the increased attention by Department of Health and Human Services to patient satisfaction surveys, now that reimbursement depends on such reporting, it is likely that future CMS reimbursement will depend on actual performance. Furthermore, in this context, patient perception of cleanliness takes on another dimension and level of importance to organizations' leadership. In view of the above considerations, it is highly likely that enhanced environmental monitoring programs will enable the organization to provide measurable, objective data to support their claims of providing a clean and safe environment for patients, their families, and health care personnel.

      References

        • Silvestri L.
        • Petros A.J.
        • Sarginson R.E.
        • de la Ca M.A.
        • Murray A.E.
        • van Saene H.K.F.
        Handwashing in the intensive care unit: a big measure with modest effects.
        J Hosp Infect. 2005; 59: 172-179
        • Rupp M.E.
        • Fitzgerald T.
        • Puumala S.
        • Anderson J.R.
        Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units.
        Infect Control Hosp Epidemiol. 2008; 29: 8-15
        • Kirkland K.B.
        Taking off the gloves: toward a less dogmatic approach to the use of contact isolation.
        Clin Infect Dis. 2009; 48: 766-771
        • Morgan D.J.
        • Diekema D.J.
        • Spkowitz K.
        • Perencevich E.N.
        Adverse outcomes associated with contact precautions: a review of the literature.
        Am J Infect Control. 2009; 37: 85-93
        • Huang S.S.
        • Yokoe D.S.
        • Hinrichsen V.L.
        • Spurchise L.S.
        • Datta R.
        • Miroshink I.
        • et al.
        Impact of routine intensive care unit surveillance cultures and resultant barrier precautions on hospital-wide methicillin-resistant Staphylococcus aureus bacteremia.
        Clin Infect Dis. 2006; 43: 971-978
        • Department of Health
        Winning ways. Working together to reduce health care associated infection in England. Report from the Chief Medical Officer.
        Crown Copyright, London2003 (Available from:) (Accessed January 30, 2010)
        • Diekema D.J.
        • Edmond M.B.
        Look before you leap: active surveillance for multidrug-resistant organisms.
        Clin Infect Dis. 2007; 44: 1101-1107
        • Kramer A.
        • Schwebke I.
        • Kampf G.
        How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
        BMC Infect Dis. 2006; 6: 130
        • Dancer S.J.
        The role of environmental cleaning in the control of hospital-acquired infection.
        J Hosp Infect. 2009; 4: 378-385
      1. Speck K, Naegeli A, Shangraw A, Ross LT, Speser S, Margarakis LL, et al. Environmental contamination with antimicrobial resistant organisms (MDROs). Abstract 157. Annual Meeting of the Society for Healthcare Epidemiology of America. Baltimore, MD. April 2007.

        • Hayden M.K.
        • Bonten M.J.
        • Blom D.W.
        • Lyle E.A.
        Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.
        Clin Infect Dis. 2006; 42: 1552-1560
        • Martinez J.A.
        • Ruthazer R.
        • Hansjosten K.
        • Barefoot L.
        • Snydman D.R.
        Role of environmental contamination as a risk factor for acquisition of vancomycin-resistant enterococci in patients treated in a medical intensive care unit.
        Arch Intern Med. 2003; 163: 1905-1912
        • Huang S.S.
        • Datta R.
        • Platt R.
        Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
        Arch Intern Med. 2006; 166: 1945-1951
        • Drees M.
        • Snydman D.R.
        • Schmid C.H.
        • Barefoot L.
        • Hansjosten K.
        Antibiotic exposure and room contamination among patients colonized with vancomycin-resistant enterococci.
        Infect Control Hosp Epidemiol. 2008; 29: 709-715
      2. Datta R, Platt R, Kleinman K, Huang SS. Impact of an environmental cleaning intervention on the risk of acquiring MRSA and VRE from prior room occupants. Abstract 273. Annual Meeting of the Society for Healthcare Epidemiology of America. San Diego, CA. March 2009.

        • Hardy K.J.
        • Oppenheim B.A.
        • Gossain S.
        • Gao F.
        • Hawkey P.M.
        A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients' acquisition of MRSA.
        Infect Control Hosp Epidemiol. 2006; 27 (Epub February 8, 2006): 127-132
      3. Shaugnessy M, Micielli R, Depestel D, Arndt J, Strachan C, Welcch K, et al. Evaluation of hospital room assignment and acquisition of Clostridium difficile associated diarrhea. Abstract K-4194. Presented at the 48th Annual ICAAC/IDSA 46th Annual Meeting. Washington, DC. October 2008.

        • Wilks M.
        • Wilson A.
        • Warwick S.
        • Price E.
        • Kennedy D.
        • Ely A.
        • et al.
        Control of an outbreak of multidrug-resistant Acinetobacter baumannii calcoaceticus colonization and infection in an intensive care unit (ICU) without closing the ICU or placing patients in isolation.
        Infect Control Hosp Epidemiol. 2006; 27: 654-658
        • Carling P.C.
        • Briggs J.
        • Hylander D.
        • Perkins J.
        An evaluation of patient area cleaning in 3 hospitals using a novel targeting methodology.
        Am J Infect Control. 2006; 34: 513-519
        • Boyce J.M.
        • Havill N.L.
        • Dumigan D.G.
        • 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
        • Eckstein B.C.
        • Adams D.A.
        • Eckstein E.C.
        • Rao A.
        Reduction of Clostridium difficile and vancomycin-resistant enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
        BMC Infect Dis. 2007; 7: 61
        • Goodman E.R.
        • Platt R.
        • Bass R.
        • Onderdonk A.B.
        • Yokoe D.S.
        • Huang S.S.
        Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
        Infect Control Hosp Epidemiol. 2008; 29: 593-599
        • Jefferson J.
        • Whelan R.
        • Dick B.
        • Carling P.C.
        A novel technique to identify opportunities for improving environmental hygiene in the operating room.
        AORN J. 2010; (In press)
      4. Guerrero D, Carling PC, Jury L, Ponnada S, Nerandzic M, Eckstein EC, et al. Beyond the “Hawthorne effect”: reduction of Clostridium difficile environmental contamination through active intervention to improve cleaning practices. Abstract 60. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      5. Carling PC, Po JL, Bartley J, Herwaldt L. Identifying opportunities to improve environmental hygiene in multiple health care settings. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

        • Carling P.C.
        • Parry M.M.
        • Rupp M.E.
        • Po J.L.
        • Dick B.L.
        • Von Beheren S.
        • for the Healthcare Environmental Hygiene Study Group
        Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
        Infect Control Hosp Epidemiol. 2008; 29: 1035-1041
        • Po J.L.
        • Burke R.
        • Sulis C.
        • Carling P.C.
        Dangerous cows: an analysis of disinfection cleaning of computer keyboards on wheels.
        Am J Infect Control. 2009; 37: 778-780
        • Hota B.
        • Blom D.W.
        • Lyle E.A.
        • Weinstein R.A.
        • Hayden M.K.
        Interventional evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.
        J Hosp Infect. 2009; 71 (Epub December 23, 2008): 123-131
      6. Bruno-Murtha LA, Harkness D, Stiles T, Han L, Carling PC. Molecular epidemiology of MRSA during an active surveillance program. Abstract 53. Society for Healthcare Epidemiology of America 19th Annual Meeting. San Diego, CA. March 19-22, 2009.

      7. Wiline J, Blum N, Fisher V, Douglas G, Flanagan G, Ostrosky L. The “A team”: an environmental services intervention to control multidrug-resistant Acinetobacter. Abstract 589. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      8. Sulis C, Estanislano R, Wedel S, Carling PC. Completeness of cleaning critical care transport vehicles. Abstract 648. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      9. Clark P, Young L, Silvestri S, Muto CA. Goo begone—evaluation of compliance with cleaning of multiple high touch (HT) surfaces using fluorescent “Goo.” Abstract 210. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

      10. Carling PC, Eck EK. Achieving sustained improvement in environmental hygiene using coordinated benchmarking in 12 hospitals. SHEA Fifth Decennial Meeting. Atlanta, GA. March 18-22, 2010.

        • Dancer S.J.
        • White L.F.
        • Girvan E.K.
        • Robertson C.
        Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
        BMC Med. 2009; 7: 28
      11. Centers for Disease Control and Prevention/Healthcare Infection Control Advisory Committee (HICPAC) Guidelines for environmental infection control in health care facilities.
        Centers for Disease Control and Prevention, Atlanta, GA2003 (Available from:) (Accessed January 20, 2010)
        • Siegel J.D.
        • Rhinehart E.
        • Jackson M.
        • Chiarello L.
        Healthcare Infection Control Practices Advisory Committee.
        Management of multi-drug-resistant organisms in healthcare settings. 2006; (Available from:) (Accessed January 15, 2009)
      12. Centers for Medicare and Medicaid. State operations manual. Appendix A. Interpretive guidelines for hospitals. Available from: http://cms.hhs.gov/manuals/Downloads/som107ap_a_hospitals.pdf. Accessed January 31, 2010.

        • Pratt R.J.
        • Pellowe C.M.
        • Wilson J.A.
        • Loveday H.P.
        • Harper P.J.
        • Jones S.R.
        • et al.
        Epic 2: national evidence-based guidelines for preventing healthcare-associated infections in NHS hospitals in England.
        J Hosp Infect. 2007; 65: S1-64
      13. Health Canada Laboratory Centre for Disease Control Bureau of Infectious Diseases Nosocomial and Occupational Infections: infection control guidelines: handwashing, cleaning, disinfection and sterilization in healthcare.
        Canada Communicable Disease Report. 1998; 24: 1-66
        • Dumford III, D.M.
        • Nerandzic M.M.
        • Eckstein B.C.
        • Donskey C.J.
        What is on that keyboard? Detecting hidden environmental reservoirs of Clostridium difficile during an outbreak associated with North American pulsed-field gel electrophoresis type 1 strains.
        Am J Infect Control. 2009; 37: 15-29
        • Sethi A.K.
        • Al-Nassir W.N.
        • Nerandzic M.M.
        • Bobulsky G.S.
        • Donskey C.J.
        Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection.
        Infect Control Hosp Epidemiol. 2010; 31: 21-27
        • Chang S.
        • Sethi A.K.
        • Eckstein B.C.
        • Stiefel U.
        • Cadnum J.L.
        • Donskey C.J.
        Skin and environmental contamination with methicillin-resistant Staphylococcus aureus among carriers identified clinically versus through active surveillance.
        Clin Infect Dis. 2009; 48: 1423-1428
        • Hayden M.K.
        • Blom D.W.
        • Lyle E.A.
        • Moore C.G.
        • Weinstein R.A.
        Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients' environment.
        Infect Control Hosp Epidemiol. 2008; 29: 149-154
        • Sethi A.K.
        • Al-Nassir W.N.
        • Nerandzic M.M.
        • Donskey C.J.
        Skin and environmental contamination with vancomycin-resistant enterocci in patients receiving oral metronidazole or oral vancomycin treatment for Clostridium difficile-associated disease.
        Infect Control Hosp Epidemiol. 2009; 30: 13-17
        • Riggs M.M.
        • Sethi A.K.
        • Zabarsky T.F.
        • Eckstein E.C.
        • Jump R.L.
        • Donskey C.J.
        Asymptomatic carriers area potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents.
        Clin Infect Dis. 2007; 45: 992-998
        • Kaatz G.
        • Gitlin S.
        • Schaberg D.
        • Wilson K.
        Acquisition of Clostridium difficile from the hospital environment.
        Am J Epidemiol. 1988; 127: 1289-1293
        • Denton M.
        • Wilcox M.
        Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit.
        Intensive Crit Care Nurs. 2005; 21: 94-98
        • Boyce J.M.
        • Potter-Bynoe G.
        • Chenevert C.
        • King T.
        Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications.
        Infect Control Hosp Epidemiol. 1997; 9: 622-627
        • de Lassence A.
        • Hidri N.
        • Timsit J.F.
        • Joly-Guillou M.L.
        Control and outcome of a large outbreak of colonization and infection with glycopeptide-intermediate Staphylococcus aureus in an intensive care unit.
        Clin Infect Disease. 2006; 42: 170-178
        • Rollins G.
        How clean is clean? New technologies, monitoring practice gains traction.
        Mater Manag in Healthcare. 2009; 5: 18-24
        • Maki D.G.
        • Alvarado C.J.
        • Hassemer C.A.
        • Zilz M.A.
        Relation of an inanimate hospital environment to endemic nosocomial infection.
        N Engl J Med. 1982; 307: 1562-1566
        • Ayliffe G.A.J.
        • Collins D.M.
        • Lowbury E.J.L.
        Cleaning and disinfecting hospital floors.
        Br Med J. 1966; 2: 442-445
        • Malik R.E.
        • Cooper R.A.
        • Griffith C.J.
        Use of audit tools to evaluate the efficacy of cleaning systems in hospitals.
        Am J Infect Control. 2003; 31: 181-187
        • Department of Health
        Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning.
        DoH, London2007 (Available from:) (Accessed January 31, 2010)
      14. The Joint Commission Standards 2010. Available from: http://www.jointcommission.org/Standards/. Accessed January 30, 2010.

        • Sax H.
        • Allegranzi B.
        • Uckay I.
        • Larson E.
        • Boyce J.
        • Pittet D.
        “My five moments of hand hygiene”: a user-centered design approach to understand, train, monitor and report hand hygiene.
        J Hosp Infect. 2007; 67: 9-21
        • Dancer S.J.
        Mopping up hospital infection.
        J Hosp Infect. 1999; 43: 85-100
        • Griffith C.J.
        • Cooper R.A.
        • Gilmore J.
        • Davies C.
        • Lewis M.
        An evaluation of hospital cleaning regimes and standards.
        J Hosp Infect. 2000; 45: 19-28
        • Carling P.C.
        • Parry M.F.
        • Von Beheren S.M.
        Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.
        Infect Control Hosp Epidemiol. 2008; 29: 1-7
        • Boyce J.M.
        • Havill N.L.
        • Lipka A.
        • Havill H.
        • Rizvani R.
        Variations in hospital daily cleaning practices.
        Infect Control Hosp Epidemiol. 2010; 31: 99-101
        • Griffith C.J.
        • Obee P.
        • Cooper R.A.
        • Burton N.F.
        • Lewis M.
        The effectiveness of existing and modified cleaning regimens in a Welsh hospital.
        J Hosp Infect. 2007; 66: 352-359
        • Dancer S.J.
        • White L.
        • Robertson C.
        Monitoring environmental cleanliness on two surgical wards.
        Int J Environ Health Res. 2008; 18: 357-364
        • Dancer S.J.
        • White L.F.
        • Lamb J.
        • Girvan E.K.
        • Robertson C.
        Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
        BMC Med. 2009; 8: 7-28
        • Cooper R.A.
        • Griffith C.J.
        • Malik R.E.
        • Obee P.
        Monitoring the effectiveness of cleaning in four British hospitals.
        Am J Infect Control. 2007; 35: 338-341
        • Thorn A.
        • Lundin A.
        • Ansehn S.
        Firefly luciferase ATP assay as a screening method for bacteriuria.
        J Clin Microbiol. 1983; : 218-224
        • Anderson B.M.
        • Rasch M.
        • Kvist J.
        • Tollefsen T.
        • Lukkassen R.
        • Sandvik L.
        • et al.
        Floor cleaning: effect on bacteria and organic materials in hospital rooms.
        J Hosp Infect. 2009; 71: 57-65
        • Simpson W.J.
        • Gilells C.J.
        • Flockhart H.A.
        Repeatability of hygiene test systems in measurement of low levels of ATP.
        Care Technology Limited, Report. 2006; 30: 606
        • Aycicek H.
        • Oguz U.
        • Karci K.
        Comparison of results of ATP bioluminescence and traditional hygiene swabbing methods for the determination of surface cleanliness at a hospital kitchen.
        Int J Hyg Environ Health. 2006; 209: 203-206
        • Griffith C.J.
        • Malik R.
        • Cooper R.A.
        • Looker N.
        • Michaels B.
        Environmental surface cleanliness and the potential for contamination during handwashing.
        Am J Infect Control. 2003; 31: 93-96
        • 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
        • Green T.A.
        • Russell S.M.
        • Fletcher D.L.
        Effect of chemical cleaning agents and commercial sanitizers on ATP bioluminescence measurements.
        J Food Protect. 1999; 62: 86-90
        • Brown E.
        • Eder A.R.
        • Thompson K.M.
        Do surface and cleaning chemistries interfere with ATP measurement systems for monitoring patient room hygiene?.
        J Hosp Infect. 2010; 74: 193-195
        • 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
        • Hamilton D.
        • Foster A.
        • Ballantyne L.
        • Kingsmore P.
        • Bedwell D.
        • Hall T.J.
        • et al.
        Performance of ultramicrofibre cleaning technology with or without addition of a novel copper-based biocide.
        J Hosp Infect. 2010; 74: 62-71
        • Chow S.
        • Shao J.
        • Wang H.
        Sample size calculations in clinical research.
        2nd ed. Chapman & Hall, Boca Raton, FL2007
      15. US Department of Health and Human Services. Final action plan to prevent healthcare-associated infections. June 2009. Available from: http://www.hhs.gov/ophs/initiatives/hai/infection.html. Accessed September 28, 2009.