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

  • Philip C. Carling
    Address correspondence to Philip C. Carling, MD, director of Hospital Epidemiology, Carney Hospital, 2100 Dorchester Ave, Boston, MA 02124.
    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
    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

      To read this article in full you will need to make a payment


      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


        • 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: 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: 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: Accessed September 28, 2009.