Research Critiques and PICOT Statement Final DraftShalom782
Effect of chlorhexidine bathing in preventing infections and reducing skin burden and environmental contamination: A review of the literature
Curtis J. Donskey MD a,b,*, Abhishek Deshpande MD, PhD c,d
a Geriatric Research, Education, and Clinical Center, Cleveland Veterans Affairs Medical Center, Cleveland, OH b Case Western Reserve University School of Medicine, Cleveland, OH c Department of Infectious Diseases, Cleveland Clinic, Cleveland, OH dMedicine Institute Center for Value-Based Care Research, Cleveland Clinic, Cleveland, OH
Key Words: Staphylococcus aureus Vancomycin-resistant Enterococcus
Chlorhexidine bathing is effective in reducing levels of pathogens on skin. In this review, we examine the evidence that chlorhexidine bathing can prevent colonization and infection with health care-associated pathogens and reduce dissemination to the environment and the hands of personnel. The importance of education and monitoring of compliance with bathing procedures is emphasized in order to optimize chlorhexidine bathing in clinical practice.
Published by Elsevier Inc. on behalf of Association for Professionals in Infection Control and Epidemiology, Inc. This is an open access article under the CC BY-NC-ND license (http://
Patients colonized or infected with health care-associated patho- gens often carry the organisms on their skin.1-3 Such contamination may lead to infection when factors such as devices, catheters, and wounds provide a route for pathogens on skin to reach normally sterile sites. Skin contamination may also contribute to transmis- sion due to environmental shedding and transfer to the hands of personnel.1-3 Thus, there is a strong rationale for efforts to reduce the burden of pathogens on skin.
During the past decade, a number of studies have examined the use of chlorhexidine bathing as an infection prevention strat- egy. This review examines the evidence that chlorhexidine bathing can prevent colonization and infection with health care-associated pathogens and reduce dissemination to the environment and the hands of personnel. We also consider recent evidence that chlorhexidine bathing is often suboptimal in clinical practice. The
importance of education and monitoring and feedback on compli- ance with bathing procedures to optimize chlorhexidine bathing is emphasized. The review was not conducted as a systematic review, but the MEDLINE electronic database was searched using broad search terminologies and recent review articles and their references were searched.
CHLORHEXIDINE SPECTRUM OF ACTIVITY AND USE FOR SKIN ANTISEPSIS
Chlorhexidine is a cationic bisbiguanide antiseptic that alters mi- crobial membrane integrity.4 A variety of formulations are available, with chlorhexidine gluconate being most commonly used in health care settings. Chlorhexidine has broad-spectrum activity against gram-positive and gram-negative bacteria, yeasts, and some lipid- enveloped viruses. Potent sporicidal activity can be induced in chlorhexidine under altered physical and chemical conditions (eg, elevated temperature, altered pH, and addition of ethanol).5 However, chlorhexidine does not have activity against bacterial spores under the conditions present on skin.
Due to its broad-spectrum antimicrobial activity and excellent safety profile, chlorhexidine is used in a wide variety of disinfec- tant, antiseptic, and preservative applications.5 In health care settings, chlorhexidine has been used for several decades for hand hygiene and for disinfection of the skin of patients before surgical proce- dures and catheter insertion.4 Chlorhexidine significantly reduces levels of resident and transient skin microbiota and has persistent activity for several hours after application.6 Chlorhexidine
* Address correspondence to Curtis J. Donskey, MD, Geriatric Research Education and Clinical Center, Cleveland VA Medical Center, 10701 East Blvd, Cleveland, OH 44106.
E-mail address: [email protected] (C.J. Donskey). This work was supported by a Merit Review grant from the Department of Vet-
erans Affairs to CJD. Publication of this article was supported by an educational grant from Clorox
Healthcare, Sealed Air, and Tru-D. Content of this article was initiated and written by the authors with no input or financial support to the authors from Clorox Health- care, Sealed Air, or Tru-D.
Conflicts of Interest: CJD has received research grants from Clorox, GOJO, Steris, and EcoLab and has served on an advisory board for Clorox. AD has received re- search funding from Clorox, Steris, and 3M.
0196-6553/Published by Elsevier Inc. on behalf of Association for Professionals in Infection Control and Epidemiology, Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). http://dx.doi.org/10.1016/j.ajic.2016.02.024
American Journal of Infection Control 44 (2016) e17-e21
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occasionally is associated with contact dermatitis, and rarely has been associated with anaphylaxis and hypersensitivity reactions.4
EFFECT OF DAILY CHLORHEXIDINE BATHING ON SHEDDING OF PATHOGENS
Skin contamination can be an important source of transmission of health care-associated pathogens through transfer to the hands of personnel and shedding into the environment.1-3 To test the po- tential for skin decontamination to reduce transmission, Vernon et al7 conducted a quasiexperimental study of daily chlorhexidinewhole- body bathing in an intensive care unit (ICU). Vancomycin-resistant Enterococcus (VRE) was chosen for study as it is often present on the skin of colonized patients and it is a common cause of central line- associated bloodstream infections (CLABSIs). Patients were bathed daily with 2% chlorhexidine cloths during the intervention period and
standard soap-and-water baths or cloths cleansing without chlorhexidine was performed during control periods.
As shown in Figure 1, chlorhexidine bathing was associated with a reduction in detection of VRE on skin. For inguinal skin, there was a 2.5-log reduction in VRE concentrations in the chlorhexidine bathing group that persisted for at least 6-8 hours. The reduction in VRE on skin was associated with significantly reduced VRE con- tamination in the environment and on the hands of personnel. Moreover, there was a significant reduction in VRE acquisition in the ICU. The findings of Vernon et al7 provide strong support for the concept of source control as a strategy to reduce dissemination of health care-associated pathogens (ie, reducing the burden of patho- gens on the skin as a means to reduce dissemination to the environment or hands). Given its broad spectrum of activity, chlorhexidine bathing represents a horizontal infection preven- tion approach that can potentially reduce dissemination of multiple pathogens. In addition, it is in theory a very simple and easy to im- plement intervention because it involves substitution of chlorhexidine bathing for standard soap-and-water bathing.
EFFECT OF DAILY CHLORHEXIDINE BATHING ON COLONIZATION AND INFECTION WITH PATHOGENS
Table 1 provides an overview of 14 studies that have evaluated the effect of chlorhexidine bathing using quasiexperimental, ward- level crossover, or stepped wedge design.7-22 Several of the studies demonstrated reductions in levels of pathogens, including gram- negative bacilli, on skin.7,11,18 For example, Popovich et al18 reported significant reductions in gram-positive and gram-negative bacte- ria and Candida spp on skin. In 12 of the 14 (86%) studies, chlorhexidine bathing was associated with a significant reduction
Fig 1. Effect of daily chlorhexidine bathing on skin and environmental contamina- tion and acquisition of vancomycin-resistant enterococci (VRE).
Table 1 Effect of chlorhexidine gluconate (CHG) bathing on colonization and infection with pathogens
Study Setting Chlorhexidine formulation Design Outcomes
7 Medical intensive care unit
2% chlorhexidine gluconate (CHG)-impregnated cloths
Quasiexperimental Decreased vancomycin-resistant enterococci on patients’ skin, health care workers’ hands, and environment
Reduced acquisition of vancomycin-resistant enterococci colonization
11 Medical intensive care unit
4% CHG solution Quasiexperimental Decreased Acinetobacter baumannii skin colonization and bloodstream infections
10 2 Medical intensive care unit wards
2% CHG-impregnated cloths 2 arm crossover trial Decreased primary bloodstream infections
6 Medical intensive care unit
2% CHG-impregnated cloths Quasiexperimental Decreased central line-associated bloodstream infections and blood culture contamination
12 6 Intensive care units in 4 hospitals
2% CHG-impregnated cloths Quasiexperimental Decreased acquisition of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci
Decreased vancomycin-resistant enterococci bacteremia 17 Long-term acute care
hospital 2% CHG solution Quasiexperimental Decreased central line-associated bloodstream infection
No change in ventilator-associated pneumonia 9 2 Intensive care units 4% CHG solution plus chlorhexidine
acetate powder to groin, axilla, and skin folds
Quasiexperimental Decreased acquisition of methicillin-resistant S aureus (non-qacA/B strains)
14 Trauma intensive care unit
2% CHG-impregnated cloths Quasiexperimental Decreased methicillin-resistant S aureus and Acinetobacter spp colonization
Decreased central line-associated bloodstream infection 19 Surgical intensive care
unit 2% CHG-impregnated cloths Quasiexperimental No decrease in central line-associated bloodstream infection
13 Trauma center intensive care unit
2% CHG-impregnated cloths Quasiexperimental Decreased central line-associated bloodstream infection
16 4 Medical wards 2% CHG-impregnated cloths Quasiexperimental Decreased methicillin-resistant S aureus and vancomycin-resistant enterococci infections
No change in Clostridium difficile infections 21 Hospital-wide 4% CHG solution applied as bed bath or
shower daily or 3 times per week Quasiexperimental Decreased C difficile infections
No change in other hospital-associated infections 8 Oncology patients 2% CHG-impregnated cloths Quasiexperimental Decreased acquisition of vancomycin-resistant enterococci
colonization 15 4 Long-term acute care
hospitals 2% CHG-impregnated cloths Stepped wedge
bundle Decreased Klebsiella pneumoniae carbapenemase-producing enterobacteriaceae colonization and infection, all-cause bacteremia, and blood culture contamination
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in colonization or infection with 1 or more of the pathogens being studied. Chlorhexidine was associated with beneficial effects when applied using 2% chlorhexidine-impregnated cloths and using cotton cloths with 2% or 4% chlorhexidine solution.
In 1 quasiexperimental study, hospital-wide chlorhexidine patient bathing was associated with a significant reduction in the inci- dence of health care-associated Clostridium difficile infection (CDI), but not in other health care-associated infections.21 The strength of the observation was increased by the finding of an increase in the incidence of CDI during a washout period in which standard soap-and-water bathing was reinstituted. As noted previously, chlorhexidine does not have sporicidal activity under the condi- tions present on skin, and therefore the reduction in CDI was unexpected. It was speculated that there may have been an in- crease in physical removal of spores during the chlorhexidine bathing period or that chlorhexidine might be killing vegetative C difficile or inhibiting spore germination on skin. Based on these findings, further studies are needed to examine the effect of chlorhexidine bathing on levels of spores on skin of patients with CDI. However, others have not demonstrated reductions in health care-associated CDI during chlorhexidine bathing.16
The 1 quasiexperimental study that did not report a benefit of chlorhexidine bathing was conducted in a surgical ICU.19 After the switch to chlorhexidine bathing, there was no significant reduc- tion in CLABSIs or other nosocomial infections. It was suggested that the failure to achieve a reduction in CLABSIs might have been related to characteristics of surgical intensive care unit patients. Such pa- tients may have large, open abdominal wounds that may serve as a source of bacteremia that could be misidentified as CLABSIs.
Four randomized trials have evaluated the effect of chlorhexidine bathing on hospital-acquired infections.23-26 Climo et al24 con- ducted amulticenter, cluster-randomized, nonblinded crossover trial to evaluate the effect of daily bathing with chlorhexidine- impregnated washcloths on acquisition of multidrug-resistant organisms (MDROs) and the incidence of hospital-acquired blood- stream infections. Nine ICUs and bonemarrow transplantation units in 6 hospitals were included. During the chlorhexidine bathing periods, the rates of MDRO acquisition and hospital-acquired blood- stream infection were reduced by 23% and 28%, respectively. Much of the reduction in bloodstream infections was attributable to a re- duction in infections with coagulase-negative staphylococci. The benefit of chlorhexidine bathing in reducing bloodstream infec- tions increased with longer length of stay in the unit.
Milstone et al25 conducted a multicenter, cluster-randomized, crossover trial in critically ill children in 10 ICUs. Bathing was per- formed using 2% chlorhexidine-impregnated cloths. Chlorhexidine bathing resulted in a statistically significant reduction in bacteremia.
Noto et al26 conducted a pragmatic cluster-randomized, cross- over study in 5 adult intensive care units in a tertiary care medical center. Patients were bathed with 2% chlorhexidine-impregnated cloths or nonantimicrobial cloths (controls). There was no differ- ence between the chlorhexidine and control groups in the primary outcome, which was a composite of nosocomial infections, includ- ing CLABSIs, catheter-associated urinary tract infection, ventilator- associated pneumonia, and CDI. In addition, chlorhexidine bathing was not associated with a reduction in secondary outcomes such as hospital-acquired bloodstream infections, blood culture contam- ination, or clinical cultures yielding MDROs. One criticism of the study design is that the primary end point included infections such as CDI, catheter-associated urinary tract infection, and ventilator- associated pneumonia that would not be expected to be reduced
by chlorhexidine bathing. In addition, adherence to chlorhexidine bathing was not monitored.
Boonyasiri et al23 conducted a randomized, open-label con- trolled trial in 4 medical ICUs in Thailand. Patients were bathed with 2% chlorhexidine-impregnated cloths or with nonantimicrobial soap. Adherence to bathing procedures was reported to be >95%, but the method of monitoring was not reported. There were no differ- ences in the 5 outcomes, including having all skin sites culture- negative throughout admission or initial positives converted to negative, colonization with MDROs, hospital-acquired infection, length of intensive care and hospital stay, and adverse skin reac- tions. The authors speculated that the failure to demonstrate a benefit of chlorhexidine bathing in this setting may have been related to the fact that the major colonizing organisms in the ICUs were gram- negative bacilli. Other studies have demonstrated that gram- negative pathogens often have higher minimum-inhibitory concentrations for chlorhexidine than gram-positive pathogens.27,28
In addition, most of the multidrug-resistant gram-negative bacilli recovered from skin were from the perianal area, suggesting that they may have been shed from the gastrointestinal tract. Chlorhexidine bathing would not be expected to affect gastroin- testinal colonization.
IMPORTANCE OF EDUCATION AND MONITORING OF COMPLIANCE
One of the guiding principles of infection prevention is that ef- fective implementation of interventions requires monitoring of compliance of staff with regular feedback on performance. For example, thoroughness of cleaning is often suboptimal and can be significantly improved by monitoring and feedback.29 However, in published studies, surprisingly little information has been re- ported on compliance with chlorhexidine bathing procedures. Those studies that have included monitoring have suggested that com- pliance may often be less than ideal even in the setting of a research study. For example, based on purchasing records, Kassakian et al16
estimated that compliancewith chlorhexidine bathing among general medical patients was 77%. Similarly, Rupp et al21 estimated com- pliance based on inventory assessments and found that estimates varied widely by ward, ranging from 45%-95%.
Although in theory chlorhexidine bathing should be easy to im- plement, 2 recent studies have provided striking demonstrations of the potential for suboptimal implementation of bathing inter- ventions in real-world settings.17,30 In a long-term acute care hospital, Munoz-Price et al17 found that constant supervision of staff was es- sential to ensure that chlorhexidine baths were appropriately given. In the absence of regular evaluations of bathing, staff stopped using chlorhexidine and began bathing patients with baby shampoo. Sim- ilarly, in medical and surgical ICUs where daily bathing with chlorhexidine 2% cloths had been implemented 2 years earlier, Supple et al30 found that none of the patients had detectable chlorhexidine on skin. It was determined that the nursing staff in both intensive care units had abandoned chlorhexidine bathing altogether without the knowledge of the infection control program. As shown in Figure 2, an intervention that included monitoring and feedback on compli- ance with chlorhexidine bathing was effective in increasing the percentage of skin sites with detectable chlorhexidine to 70%-88%.30
The experience of Supple et al30 suggests that measurement of chlorhexidine on skin may be useful as a means to monitor effec- tiveness of bathing practices and provide feedback. A simple, rapid colorimetric assay that is commonly used in research studies was used tomeasure chlorhexidine on skin.31 The assay is easy to perform and includes reagents that are inexpensive and commercially available.31 In addition to the improvement in daily intensive care unit bathing, the assay identified deficiencies in preoperative bathing
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that were significantly improved by an intervention. For example, many patients performing preoperative bathing did not have de- tectable chlorhexidine on their neck because their understanding of the instructions was that they should bathe below the neck. This deficiency was easily corrected through education of nurses and modification of patient education sheets. Similarly, Popovich et al6
found that patients admitted to ICUs often had low levels of chlorhexidine on their neck and noted that this area received less thorough cleansing when bathing was directly observed. Popovich et al6 also suggested that measurement of chlorhexidine on skin might be useful as a means to improve bathing performance.
Finally, it should be appreciated that suboptimal application of chlorhexidine may be an issue in real-world settings even if staff and patients are motivated to comply with recommended bathing procedures. In contrast to healthy volunteers and most patients re- ceiving preoperative bathing, patients in ICUs and ill patients on medical wards often have large surgical wounds and numerous lines, catheters, and devices that make it difficult to apply chlorhexidine effectively. These difficulties are akin to the challenges involved in performing effective daily environmental cleaning of a cluttered patient room versus terminal cleaning after patient discharge. In this regard, it is notable that the 1 quasiexperimental study that did not report a benefit of chlorhexidine bathing was conducted in a surgical ICU.19 The authors noted that many of the patients in the unit had large, open abdominal wounds that could make chlorhexidine application difficult. In addition to providing feed- back on compliance, measurement of chlorhexidine on skin in such real-world settings may shed light on some of the challenges in- volved in providing effective bathing.
During the past decade, a growing body of evidence has accu- mulated suggesting that chlorhexidine bathing may be beneficial as a strategy to prevent colonization and infection with health care- associated pathogens. In addition, reduction in skin carriage may reduce dissemination of pathogens to the environment and the hands of personnel. Although reductions in gram-positive pathogens have been reported most frequently, reductions in gram-negative patho- gens have also been reported in some but not all studies. Given the evidence that chlorhexidine bathing may be beneficial, this prac- tice is now becoming routine in many facilities, particularly in ICUs. There is evidence that chlorhexidine bathing is not infrequently sub- optimal in clinical practice. To optimize bathing in real-world settings, there is a need to develop effective strategies to monitor compli- ance with bathing protocols and provide feedback to personnel.
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2. Sethi AK, Al-Nassir WN, Nerandzic MM, Bobulsky GS, Donskey CJ. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol 2010;31:21-7.
3. Stiefel U, Cadnum JL, Eckstein BC, Guerrero DM, Tima MA, Donskey CJ. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients. Infect Control Hosp Epidemiol 2011;32:185-7.
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5. Nerandzic MM, Donskey CJ. Induced sporicidal activity of chlorhexidine against Clostridium difficile spores under altered physical and chemical conditions. PLoS ONE 2015;10:e0123809.
6. Popovich KJ, Lyles R, Hayes R, Hota B, Trick W, Weinstein RA, et al. 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 2012;33:889-96.
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8. Bass P, Karki S, Rhodes D, Gonelli S, Land G, Watson K, et al. Impact of chlorhexidine-impregnated washcloths on reducing incidence of vancomycin- resistant enterococci colonization in hematology-oncology patients. Am J Infect Control 2013;41:345-8.
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11. Borer A, Gilad J, Porat N, Megrelesvilli R, Saidel-Odes L, Peled N, et al. 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 2007;67:149-55.
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13. Dixon JM, Carver RL. Daily chlorhexidine gluconate bathing with impregnated cloths results in statistically significant reduction in central line-associated bloodstream infections. Am J Infect Control 2010;38:817-21.
14. Evans HL, Dellit TH, Chan J, Nathens AB, Maier RV, Cuschieri J. Effect of chlorhexidine whole-body bathing on hospital-acquired infections among trauma patients. Arch Surg 2010;145:240-6.
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16. Kassakian SZ, Mermel LA, Jefferson JA, Parenteau SL, Machan JT. Impact of chlorhexidine bathing on hospital-acquired infections among general medical patients. Infect Control Hosp Epidemiol 2011;32:238-43.
17. Munoz-Price LS, Hota B, Stemer A, Weinstein RA. Prevention of bloodstream infections by use of daily chlorhexidine baths for patients at a long-term acute care hospital. Infect Control Hosp Epidemiol 2009;30:1031-5.
18. Popovich KJ, Hota B, Hayes R, Weinstein RA, Hayden MK. Effectiveness of routine patient cleansing with chlorhexidine gluconate for infection prevention in the medical intensive care unit. Infect Control Hosp Epidemiol 2009;30:959-63.
19. Popovich KJ, Hota B, Hayes R, Weinstein RA, Hayden MK. Daily skin cleansing with chlorhexidine did not reduce the rate of central-line associated bloodstream infection in a surgical intensive care unit. Intensive Care Med 2010;36:854-8.
20. Quach C, Milstone AM, Perpete C, Bonenfant M, Moore DL, Perreault T. Chlorhexidine bathing in a tertiary care neonatal intensive care unit: impact on central line-associated bloodstream infections. Infect Control Hosp Epidemiol 2014;35:158-63.
21. Rupp ME, Cavalieri RJ, Lyden E, Kucera J, Martin M, Fitzgerald T, et al. Effect of hospital-wide chlorhexidine patient bathing on healthcare-associated infections. Infect Control Hosp Epidemiol 2012;33:1094-100.
22. Lin MY, Lolans K, Blom DW, Lyles RD,Weiner S, Poluru KB, et al. 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 2014;35:440-2.
23. Boonyasiri A, Thaisiam P, Permpikul C, Judaeng T, Suiwongsa B, Apiradeewajeset N, et al. Effectiveness of chlorhexidine wipes for the prevention of multidrug- resistant bacterial colonization and hospital-acquired infections in intensive care
Fig 2. Point-prevalence of medical and surgical intensive care unit patients with de- tectable chlorhexidine on 1 or more skin sites before and 1, 3, and 6 months after an intervention. Chlorhexidine was measured from 4 skin sites (neck, arm and hand, chest and abdomen, and groin).
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