Insights into bacterial colonization of intensive care patients’ skin: the effect of chlorhexidine daily bathing

  • N. Cassir
  • L. Papazian
  • P.-E. Fournier
  • D. Raoult
  • B. La ScolaEmail author


Skin is a major reservoir of bacterial pathogens in intensive care unit (ICU) patients. The aim of this study was to assess the skin bacterial richness and diversity in ICU patients and the effect of CHG daily bathing on skin microbiota. Twenty ICU patients were included during an interventional period with CHG daily bathing (n = 10) and a control period (n = 10). At day seven of hospitalization, eight skin swab samples (nares, axillary vaults, inguinal creases, manubrium and back) were taken from each patient. The bacterial identification was performed by microbial culturomics. We used the Shannon index to compare the diversity. We obtained 5,000 colonies that yielded 61 bacterial species (9.15 ± 3.7 per patient), including 15 (24.5 %) that had never been cultured from non-pathological human skin before, and three (4.9 %) that had never been cultured from human samples before. Notably, Gram-negative bacteria were isolated from all sites. In the water-and-soap group, there was a higher risk of colonization with Gram-negative bacteria (OR = 6.05, 95 % CI [1.67–21.90]; P = 0.006). In the CHG group, we observed more patients colonized by sporulating bacteria (9/10 vs. 3/10; P = 0.019) with a reduced skin bacterial richness (P = 0.004) and lower diversity (0.37, 95 % CI [0.33; 0.42] vs. 0.50, 95 % CI [0.48; 0.52]). Gram-negative bacteria are frequent and disseminated components of the transient skin flora in ICU patients. CHG daily bathing is associated with a reduction in Gram-negative bacteria colonization together with substantial skin microbiota shifts.


Intensive Care Unit Patient Acinetobacter Baumannii Selective Digestive Decontamination Chlorhexidine Gluconate Skin Microbiota 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We acknowledge Georgette Grech and Isabelle Jousset for their technical assistance, and Anderson Loundou for reviewing the statistical methods. Sage products provided the single-use, no-rinse disposable cloths saturated with 2 % chlorhexidine gluconate.

Competing interests

The authors declare that they have no competing interests.

Authors’ contribution

LP, BLS, and DR conceived of the study and participated in its design. NC carried out the experiments, and drafted the manuscript. LP took care of the patients. NC, LP, PEF, DR and BLS analysed the data. LP, PEF, DR, and BLS helped to draft the manuscript. All the authors revised and approved the manuscript.

Supplementary material

10096_2015_2316_MOESM1_ESM.doc (135 kb)
ESM 1 (DOC 135 kb)


  1. 1.
    Murillo N, Raoult D (2013) Skin microbiota: overview and role in the skin diseases acne vulgaris and rosacea. Future Microbiol 8:209–222. doi: 10.2217/fmb.12.141 CrossRefPubMedGoogle Scholar
  2. 2.
    Grice EA, Kong HH, Conlan S, Deming CB, Davis J et al (2009) Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192. doi: 10.1126/science.1171700 CrossRefPubMedCentralPubMedGoogle Scholar
  3. 3.
    Larson EL, McGinley KJ, Foglia AR, Talbot GH, Leyden JJ (1986) Composition and antimicrobic resistance of skin flora in hospitalized and healthy adults. J Clin Microbiol 23:604–608PubMedCentralPubMedGoogle Scholar
  4. 4.
    Vincent J-L (2003) Nosocomial infections in adult intensive-care units. Lancet 361:2068–2077. doi: 10.1016/S0140-6736(03)13644-6 CrossRefPubMedGoogle Scholar
  5. 5.
    Duncan CN, Riley TV, Carson KC, Budgeon CA, Siffleet J (2013) The effect of an acidic cleanser versus soap on the skin pH and micro-flora of adult patients: a non-randomised two group crossover study in an intensive care unit. Intensive Crit Care Nurs Off J Br Assoc Crit Care Nurses 29:291–296. doi: 10.1016/j.iccn.2013.03.005 CrossRefGoogle Scholar
  6. 6.
    Vernon MO, Hayden MK, Trick WE, Hayes RA, Blom DW et al (2006) Chlorhexidine gluconate to cleanse patients in a medical intensive care unit: the effectiveness of source control to reduce the bioburden of vancomycin-resistant enterococci. Arch Intern Med 166:306–312. doi: 10.1001/archinte.166.3.306 CrossRefPubMedGoogle Scholar
  7. 7.
    Gao Z, Tseng C, Pei Z, Blaser MJ (2007) Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA 104:2927–2932. doi: 10.1073/pnas.0607077104 CrossRefPubMedCentralPubMedGoogle Scholar
  8. 8.
    Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105:17994–17999. doi: 10.1073/pnas.0807920105 CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi: 10.1128/AEM. 00062-07 CrossRefPubMedCentralPubMedGoogle Scholar
  10. 10.
    Gao Z, Perez-Perez GI, Chen Y, Blaser MJ (2010) Quantitation of major human cutaneous bacterial and fungal populations. J Clin Microbiol 48:3575–3581. doi: 10.1128/JCM. 00597-10 CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Kong HH (2011) Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17:320–328. doi: 10.1016/j.molmed.2011.01.013 CrossRefPubMedCentralPubMedGoogle Scholar
  12. 12.
    Hugon P, Lagier J-C, Robert C, Lepolard C, Papazian L et al (2013) Molecular studies neglect apparently gram-negative populations in the human gut microbiota. J Clin Microbiol 51:3286–3293. doi: 10.1128/JCM. 00473-13 CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Lagier J-C, Million M, Hugon P, Armougom F, Raoult D (2012) Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol 2:136. doi: 10.3389/fcimb.2012.00136 CrossRefPubMedCentralPubMedGoogle Scholar
  14. 14.
    Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A et al (2011) Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci USA 108:6252–6257. doi: 10.1073/pnas.1102938108 CrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
    Lagier J-C, Armougom F, Million M, Hugon P, Pagnier I et al (2012) Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis 18:1185–1193. doi: 10.1111/1469-0691.12023 Google Scholar
  16. 16.
    Popovich KJ, Lyles R, Hayes R, Hota B, Trick W et al (2012) Relationship between chlorhexidine gluconate skin concentration and microbial density on the skin of critically ill patients bathed daily with chlorhexidine gluconate. Infect Control Hosp Epidemiol 33:889–896. doi: 10.1086/667371 CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Grare M, Dibama HM, Lafosse S, Ribon A, Mourer M et al (2010) Cationic compounds with activity against multidrug-resistant bacteria: interest of a new compound compared with two older antiseptics, hexamidine and chlorhexidine. Clin Microbiol Infect 16:432–438. doi: 10.1111/j.1469-0691.2009.02837.x CrossRefPubMedGoogle Scholar
  18. 18.
    Climo MW, Yokoe DS, Warren DK, Perl TM, Bolon M et al (2013) Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med 368:533–542. doi: 10.1056/NEJMoa1113849 CrossRefPubMedGoogle Scholar
  19. 19.
    Evans HL, Dellit TH, Chan J, Nathens AB, Maier RV et al (2010) Effect of chlorhexidine whole-body bathing on hospital-acquired infections among trauma patients. Arch Surg Chic Ill 1960 145:240–246. doi: 10.1001/archsurg.2010.5 Google Scholar
  20. 20.
    Apisarnthanarak A, Pinitchai U, Warachan B, Warren DK, Khawcharoenporn T et al (2014) Effectiveness of infection prevention measures featuring advanced source control and environmental cleaning to limit transmission of extremely-drug resistant Acinetobacter baumannii in a Thai intensive care unit: An analysis before and after extensive flooding. Am J Infect Control 42:116–121. doi: 10.1016/j.ajic.2013.09.025 CrossRefPubMedGoogle Scholar
  21. 21.
    Borer A, Gilad J, Porat N, Megrelesvilli R, Saidel-Odes L et al (2007) Impact of 4% chlorhexidine whole-body washing on multidrug-resistant Acinetobacter baumannii skin colonisation among patients in a medical intensive care unit. J Hosp Infect 67:149–155. doi: 10.1016/j.jhin.2007.07.023 CrossRefPubMedGoogle Scholar
  22. 22.
    Lin MY, Lolans K, Blom DW, Lyles RD, Weiner S et al (2014) The effectiveness of routine daily chlorhexidine gluconate bathing in reducing Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae skin burden among long-term acute care hospital patients. Infect Control Hosp Epidemiol 35:440–442. doi: 10.1086/675613 CrossRefPubMedGoogle Scholar
  23. 23.
    Seng P, Drancourt M, Gouriet F, La Scola B, Fournier P-E et al (2009) Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 49:543–551. doi: 10.1086/600885 CrossRefPubMedGoogle Scholar
  24. 24.
    Wang M, Karlsson C, Olsson C, Adlerberth I, Wold AE et al (2008) Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol 121:129–134. doi: 10.1016/j.jaci.2007.09.011 CrossRefPubMedGoogle Scholar
  25. 25.
    Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253. doi: 10.1038/nrmicro2537 CrossRefPubMedCentralPubMedGoogle Scholar
  26. 26.
    Seifert H, Dijkshoorn L, Gerner-Smidt P, Pelzer N, Tjernberg I et al (1997) Distribution of Acinetobacter species on human skin: comparison of phenotypic and genotypic identification methods. J Clin Microbiol 35:2819–2825PubMedCentralPubMedGoogle Scholar
  27. 27.
    Buehlmann M, Fankhauser H, Laffer R, Bregenzer T, Widmer AF (2010) The inguinal skin: an important site of colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae. Infect Control Hosp Epidemiol 31:427–428. doi: 10.1086/651309 CrossRefPubMedGoogle Scholar
  28. 28.
    Thibault R, Graf S, Clerc A, Delieuvin N, Heidegger CP et al (2013) Diarrhoea in the ICU: respective contribution of feeding and antibiotics. Crit Care Lond Engl 17:R153. doi: 10.1186/cc12832 CrossRefGoogle Scholar
  29. 29.
    Grice EA, Kong HH, Renaud G, Young AC, NISC Comparative Sequencing Program et al (2008) A diversity profile of the human skin microbiota. Genome Res 18:1043–1050. doi: 10.1101/gr.075549.107 CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    Karki S, Cheng AC (2012) Impact of non-rinse skin cleansing with chlorhexidine gluconate on prevention of healthcare-associated infections and colonization with multi-resistant organisms: a systematic review. J Hosp Infect 82:71–84. doi: 10.1016/j.jhin.2012.07.005 CrossRefPubMedGoogle Scholar
  31. 31.
    Apisarnthanarak A, Yang Hsu L, Lim T-P, Mundy LM (2014) Increase in chlorhexidine minimal inhibitory concentration of Acinetobacter baumannii clinical isolates after implementation of advanced source control. Infect Control Hosp Epidemiol 35:98–99. doi: 10.1086/674404 CrossRefPubMedGoogle Scholar
  32. 32.
    Naparstek L, Carmeli Y, Chmelnitsky I, Banin E, Navon-Venezia S (2012) Reduced susceptibility to chlorhexidine among extremely-drug-resistant strains of Klebsiella pneumoniae. J Hosp Infect 81:15–19. doi: 10.1016/j.jhin.2012.02.007 CrossRefPubMedGoogle Scholar
  33. 33.
    Lai Y, Cogen AL, Radek KA, Park HJ, Macleod DT et al (2010) Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol 130:2211–2221. doi: 10.1038/jid.2010.123 CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • N. Cassir
    • 1
  • L. Papazian
    • 1
    • 2
  • P.-E. Fournier
    • 1
  • D. Raoult
    • 1
  • B. La Scola
    • 1
    Email author
  1. 1.Unité de Recherche sur les Maladies Infectieuses Tropicales et Emergentes, URMITE, UM63, CNRS 7278, IRD 198, INSERM 1095, Méditerranée-InfectionAix-Marseille-UniversitéMarseilleFrance
  2. 2.Service de Réanimation des Détresses Respiratoires et Infections Sévères, Hôpital NordAssistance Publique-Hôpitaux de MarseilleMarseilleFrance

Personalised recommendations