Intensive care unit environmental surfaces are contaminated by multidrug-resistant bacteria in biofilms: Combined results of conventional culture, pyrosequencing, scanning electron microscopy, and confocal laser microscopy

Journal of Hospital Infection

Volumn 91, Issue 1, 2015, Pages 35-44

  Hu, H ^a   Johani, K ^a,b   Gosbell, I B ^c,d   Jacombs, A S W ^a   Almatroudi, A ^a,e   Whiteley, G S ^f   Deva, A K ^a   Jensen, S ^c   Vickery, K ^a  

^a MACQUARIE UNIVERSITY   (Australia)

^b Prince Sultan Military Medical City   (Saudi Arabia)

^c UNIVERSITY OF WESTERN SYDNEY   (Australia)

^d SYDNEY SOUTH WEST AREA HEALTH SERVICE   (Australia)

^e QASSIM UNIVERSITY   (Saudi Arabia)

^f Whiteley Corporation   (Australia)

Author keywords

Biofilm; Enterococci; Healthcare associated infections; Intensive care unit; Microbiome; Multidrug resistant organisms; Staphylococcus aureus

Indexed keywords

CHLORINE; EXTENDED SPECTRUM BETA LACTAMASE;

ACINETOBACTER CALCOACETICUS; ACINETOBACTER JUNII; ACINETOBACTER LWOFFII; AEROBIC BACTERIUM; AEROBIC CELL CULTURE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CONTAMINATION; BACTERIUM CULTURE; BACTERIUM DETECTION; BIOFILM; COAGULASE NEGATIVE STAPHYLOCOCCUS; CONFOCAL LASER MICROSCOPY; CULTURE MEDIUM; DISEASE ERADICATION; DNA EXTRACTION; ENVIRONMENTAL FACTOR; FAECALIBACTERIUM PRAUSNITZII; HEALTHCARE ASSOCIATED INFECTION; HUMAN; INTENSIVE CARE UNIT; MASSILIA TIMONAE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOME; MORBIDITY; MORTALITY; MULTIDRUG RESISTANCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PREVALENCE; PYROSEQUENCING; RICKETTSIA MASSILIAE; SCANNING ELECTRON MICROSCOPY; STAPHYLOCOCCUS AUREUS; CONFOCAL MICROSCOPY; CROSS INFECTION; DRUG EFFECTS; ENTEROCOCCUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; PROCEDURES; STANDARDS; TRANSMISSION;

BIOFILMS; CROSS INFECTION; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROCOCCUS; HUMANS; INTENSIVE CARE UNITS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOTA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; PREVALENCE; STAPHYLOCOCCUS AUREUS;

EID: 84938258235     PISSN: 01956701     EISSN: 15322939     Source Type: Journal    
DOI: 10.1016/j.jhin.2015.05.016     Document Type: Article

References (40)

1. Magill S.S., Edwards J.R., Bamberg W., et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med 2014, 370:1198-1208.
2. Scott R.D. The direct medical costs of healthcare-associated infections in U.S. hospitals and the benefits of prevention 2007, Centers for Disease Control and Prevention, Atlanta, Available at:, [last accessed December 2014]. http://www.cdc.gov/hai/pdfs/hai/scott_costpaper.pdf.
3. Raschka S., Dempster L., Bryce E. Health economic evaluation of an infection prevention and control program: are quality and patient safety programs worth the investment?. Am J Infect Control 2013, 41:773-777.
4. Pittet D., Hugonnet S., Harbarth S., et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000, 356(9238):1307-1312.
5. Gould D.J., Hewitt-Taylor J., Drey N.S., Gammon J., Chudleigh J., Weinberg J.R. The CleanYourHandsCampaign: critiquing policy and evidence base. J Hosp Infect 2007, 65:95-101.
6. Backman C., Zoutman D.E., Marck P.B. An integrative review of the current evidence on the relationship between hand hygiene interventions and the incidence of health care-associated infections. Am J Infect Control 2008, 36:333-348.
7. Jain R., Kralovic S.M., Evans M.E., et al. Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011, 364:1419-1430.
8. Fisher D., Tambyah P.A., Lin R.T.P., et al. Sustained meticillin-resistant Staphylococcus aureus control in a hyper-endemic tertiary acute care hospital with infrastructure challenges in Singapore. J Hosp Infect 2013, 85:141-148.
9. Siegel JD, Rhinehart E, Jackson M, Chiarello L, Healthcare Infection Control Practices Advisory Committee. Management of Multidrug-Resistant Organisms In Healthcare Settings, 2006. Available at: [last accessed October 2014]. http://www.cdc.gov/hicpac/pdf/MDRO/MDROGuideline2006.pdf.
10. Rosenthal V.D., Maki D.G., Mehta A., et al. International Nosocomial Infection Control Consortium report, data summary for 2002-2007, issued January 2008. Am J Infect Control 2008, 36:627-637.
11. Dancer S.J. Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Dis 2008, 8:101-113.
12. Carling P.C., Bartley J.M. Evaluating hygienic cleaning in health care settings: what you do not know can harm your patients. Am J Infect Control 2010, 38(5, Suppl 1):S41-S50.
13. Wood M.W., Lund R.C., Stevenson K.B. Bacterial contamination of stethoscopes with antimicrobial diaphragm covers. Am J Infect Control 2007, 35:263-266.
14. Panhotra B.R., Saxena A.K., Al-Mulhim A.S. Contamination of patients' files in intensive care units: an indication of strict handwashing after entering case notes. Am J Infect Control 2005, 33:398-401.
15. Wilson A.P., Ostro P., Magnussen M., Cooper B., Keyboard Study Group Laboratory and in-use assessment of methicillin-resistant Staphylococcus aureus contamination of ergonomic computer keyboards for ward use. Am J Infect Control 2008, 36:e19-25.
16. 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, 7:28.
17. Vickery K., Deva A., Jacombs A., Allan J., Valente P., Gosbell I.B. Presence of biofilm containing viable multiresistant organisms despite terminal cleaning on clinical surfaces in an intensive care unit. J Hosp Infect 2012, 80:52-55.
18. Sutherland I.W. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 2001, 147:3-9.
19. Vickery K., Pajkos A., Cossart Y., Vickery K., Pajkos A., Cossart Y. Removal of biofilm from endoscopes: evaluation of detergent efficiency. Am J Infect Control 2004, 32:170-176.
20. Xue Z., Sendamangalam V.R., Gruden C.L., Seo Y. Multiple roles of extracellular polymeric substances on resistance of biofilm and detached clusters. Environ Sci Technol 2012, 46:13212-13219.
21. Kidd T.J., Ramsay K.A., Hu H., et al. Low rates of Pseudomonas aeruginosa misidentification in isolates from cystic fibrosis patients. J Clin Microbiol 2009, 47:1503-1509.
22. Al-Talib H., Yean C.Y., Al-Khateeb A., et al. A pentaplex PCR assay for the rapid detection of methicillin-resistant Staphylococcus aureus and Panton-Valentine Leucocidin. BMC Microbiol 2009, 9:113.
23. Dowd S.E., Callaway T.R., Wolcott R.D., et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 2008, 8:125-132.
24. Caporaso J.G., Kuczynski J., Stombaugh J., et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 2010, 7:335-336.
25. Maidak B.L., Cole J.R., Lilburn T.G., et al. The RDP-II (Ribosomal Database Project). Nucleic Acids Res 2001, 29:173-174.
26. Hayden M.K., Bonten M.J.M., Blom D.W., Lyle E.A., van de Vijver D.A.M.C., Weinstein R.A. Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis 2006, 42:1552-1560.
27. Australian Council on Safety and Quality in Healthcare National Safety and Quality Health Service Standards, September 2012. Care ACoSQiH 2012, Commonwealth of Australia.
28. Creamer E., Dorrian S., Dolan A., et al. When are the hands of healthcare workers positive for meticillin-resistant Staphylococcus aureus?. J Hosp Infect 2010, 75:107-111.
29. Moore G., Muzslay M., Wilson A.P.R. The type, level, and distribution of microorganisms within the ward environment: a zonal analysis of an intensive care unit and a gastrointestinal surgical ward. Infect Control Hosp Epidemiol 2013, 34:500-506.
30. Muzslay M., Moore G., Turton J.F., Wilson A.P. Dissemination of antibiotic-resistant enterococci within the ward environment: the role of airborne bacteria and the risk posed by unrecognized carriers. Am J Infect Control 2013, 41:57-60.
31. Bridier A., Briandet R., Thomas V., Dubois-Brissonnet F. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 2011, 27:1017-1032.
32. Machado I., Lopes S.P., Sousa A.M., Pereira M.O. Adaptive response of single and binary Pseudomonas aeruginosa and Escherichia coli biofilms to benzalkonium chloride. J Basic Microbiol 2012, 52:43-52.
33. Fux C.A., Stoodley P., Hall-Stoodley L., Costerton J.W. Bacterial biofilms: a diagnostic and therapeutic challenge. Expert Rev Antiinfective Ther 2003, 1:667-683.
34. Hall-Stoodley L., Stoodley P. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 2005, 13:7-10.
35. Habimana O., Heir E., Langsrud S., Åsli A.W., Møretrø T. Enhanced surface colonization by Escherichia coli 0157:H7 in biofilms formed by an Acinetobacter calcoaceticus isolate from meat-processing environments. Appl Environ Microbiol 2010, 76:4557-4559.
36. Burmølle M., Webb J.S., Rao D., Hansen L.H., Sørensen S.J., Kjelleberg S. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 2006, 72:3916-3923.
37. National Health and Medical Research Council Australian guidelines for the prevention and control of infection in healthcare 2010, Commonwealth of Australia, Available at:, [last accessed November 2014]. http://www.nhmrc.gov.au/_files_nhmrc/publications/attachments/cd33_infection_control_healthcare.pdf.
38. Grabsch E.A., Mahony A.A., Cameron D.R.M., et al. Significant reduction in vancomycin-resistant enterococcus colonization and bacteraemia after introduction of a bleach-based cleaning-disinfection programme. J Hosp Infect 2012, 82:234-242.
39. Friedman N.D., Walton A.L., Boyd S., et al. The effectiveness of a single-stage versus traditional three-staged protocol of hospital disinfection at eradicating vancomycin-resistant enterococci from frequently touched surfaces. Am J Infect Control 2013, 41:227-231.
40. Rutala W.A., Gergen M.F., Weber D.J. Efficacy of different cleaning and disinfection methods against Clostridium difficile spores: importance of physical removal versus sporicidal inactivation. Infect Control Hosp Epidemiol 2012, 33:1255-1258.