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Health care workers' hand contamination levels and antibacterial efficacy of different hand hygiene methods used in a Vietnamese hospital
American Journal of Infection Control 42 (2014) 178-81
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Health care workers’ hand contamination levels and antibacterial efficacy of different hand hygiene methods used in a Vietnamese hospital Sharon Salmon BN, MPH a, Anh Thu Truong MD, PhD b, Viet Hung Nguyen MD, PhD b, Didier Pittet MD, MS c, Mary-Louise McLaws DipTropPH, MPHlth, PhD a, * a b c
UNSW Medicine, University of New South Wales, Sydney, Australia Department of Infection Control, Bach Mai Hospital, Hanoi, Vietnam Infection Control Program and World Health Organization Collaborating Centre on Patient Safety, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Key Words: Alcohol-based hand rub Water quality Handwashing Antimicrobial efficacy
Background: Handwashing with soap or another antisepsis disinfectant solution is a common practice in Vietnam, but the availability and quality of tap water is unpredictable. We assessed the risk for hand contamination and compared the efficacy of 5 hand hygiene methods in a tertiary Vietnamese hospital. Methods: Five fingertip imprints of the dominant hand of 134 health care workers (HCWs) were sampled to establish the average bacterial count before and after hand hygiene action using (1) alcohol-based handrub (ABHR), (2) plain soap and water handwashing with filtered and unfiltered water, or (3) 4% chlorhexidine gluconate hand antisepsis with filtered and unfiltered water. Results: Average bacterial contamination of hands before hand hygiene was 1.65 log10. Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus were the most commonly isolated bacterial pathogens. The highest average count before hand hygiene was recovered from HCWs without direct patient contact (2.10 0.11 log10). Bacterial counts were markedly reduced after hand hygiene with ABHR (1.4 log10; P < .0001) and 4% chlorhexidine gluconate with filtered water (0.8 log10; P < .0001). Use of unfiltered water was associated with minimal nonsignificant bacterial reduction. Conclusions: HCWs carry high levels of bacteria on their dominant hand, even without direct patient contact. ABHR as an additional step may overcome the effect of high bacterial counts in unfiltered water when soap and water handwashing is indicated. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Hand hygiene is cost-effective and critical in reducing the transfer of transient flora, including bacteria, viruses, and fungi, from the hands of health care workers (HCWs) to patients.1-3 Transient flora can be recovered from skin after contamination for short periods, but they do not usually multiply on skin surfaces, except under facilitating conditions, particularly on gloved hands.4,5 Although transient flora are the pathogens most frequently related to health careeassociated infections (HAIs), routine hand hygiene can decontaminate HCW hands.6 Over the past decade, various hand hygiene methods have been reported to significantly reduce bacterial load and prevent cross-
* Address correspondence to Professor Mary-Louise McLaws, DipTropPH, MPHlth, PhD, UNSW Medicine, University of New South Wales, School of Public Health and Community Medicine, Level 3 Samuels Building, Sydney, NSW 2052, Australia. E-mail address: [email protected] (M.-L. McLaws). Conflict of interest: None to report.
transmission resulting in colonization or HAI.7 In clinical practice, alcohol-based hand rub (ABHR) has been documented to reduce bacterial counts more effectively than handwashing with soap and/ or other chemical products.4 In addition, the time savings associated with the use of ABHR has improved HCW hand hygiene compliance.3,7-9 Poor water quality monitoring, maintenance of water systems, and local enforcement of national water quality standards is a concern at all levels of health care facilities across Vietnam. Major barriers to hand hygiene compliance in Vietnam include the lack of basic equipment, particularly alcohol-based formulations. Many HCWs cannot wash their hands with soap and water at the point of care because of limited or dysfunctional sinks or lack of soap, stemming from hospital management’s concerns that soap will be taken by patients’ relatives and other visitors. Only wards with high-risk patients are equipped with ABHR because of the high costs associated with these formulations. The aims of the present study were to assess risk factors for HCW hand contamination
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2013.07.013
S. Salmon et al. / American Journal of Infection Control 42 (2014) 178-81
and to compare the antibacterial efficacy of hand hygiene using 5 methods in a tertiary Vietnamese hospital. METHODS Study site Founded in 1911 during the French colonization, Bach Mai Hospital in Hanoi is the largest tertiary medical health care facility in Vietnam, with 1,900 beds. It is a major medical teaching center, responsible for training most internal medicine physicians in the country. Approximately 45,000 patients are discharged annually, with triple bed occupancy owing to more than 1 patient per bed in wards outside the intensive care unit (ICU). Since 2002, the hospital has instituted hospital-wide multimodal hand hygiene campaigns that have included HCW training, education materials, and availability of ABHR in the ICU and general wards. Participant selection HCWs were enrolled in this study over 9 weekdays during December 2006 from 10 selected clinical departments (ICU, surgical, pediatrics, emergency, gastroenterology, hepatobiliary, nephrology, poison center, cardiology, and infectious diseases) in which the study was conducted. A minimum of 3 HCWs (1 physician, 1 nurse, and 1 other HCW) were selected at random from each department. Infection control staff selected the first HCW encountered in the first patient room in the participating departments. If no HCWs were present in the first patient room, the researcher would then enter another patient room. Participants were required to undergo hand hygiene training. On completion of training, participants were randomly assigned to 1 of 5 hand hygiene techniques: ABHR, 4% chlorhexidine gluconate (CHG) with filtered or unfiltered water, and soap and water handwashing with filtered or unfiltered water. The 3 hand hygiene solutions were SDS Hand Rub, containing ethanol (83%), isopropyl alcohol (12%), and chlorhexidine digluconate (0.5%) (SDS, Ha Noi, Vietnam); SDS Hand Wash, containing sodium lauryl ether sulphate (12%), coconut fatty acid diethanol amide (3%), and cocamido propyl betain (3%) (SDS Vietnam); and 4% CHG solution (Microshield; Johnson & Johnson Medical, Sydney, Australia). A Filtranios 31 DA filter (Laboratoires Anios, Lille-Hellemmes, France) was attached to the tap by removing the tap aerator and replacing it with a faucet adapter, and then attaching the filter. Two cultures were obtained from all participants, 1 before hand hygiene and 1 after hand hygiene. Hands were not visibly soiled at the time of hand plating.
179
researcher performing the technique. All participants received instruction on the 4 technical requirements for hand hygiene: the correct amount of solution to apply, hand hygiene thoroughness, duration of hand hygiene, and hand drying technique. A participant who failed to perform the technique correctly was excluded from the study. Hand hygiene was then performed using the assigned method, and a sample was obtained 1 minute later. Culture samples were obtained and labeled according to the hand hygiene method used. Microbiological procedures Samples were obtained by imprinting all 5 fingertips of the HCW’s dominant hand using commercial agar plates (BioMérieux, Marcy l’Etoile, France). Fingertips were gently pressed against the agar for 15 seconds.3,10 Hand hygiene was then performed using the assigned method, and a sample was obtained 1 minute later. Plates were transferred to the hospital’s microbiology department within 1 hour of sampling. The same 2 trained laboratory technicians blinded to the product and water quality information processed all samples. Plates were then incubated at 37 C under aerobic conditions, and colony-forming units (CFUs) were counted after incubation of 24-48 hours. Bacteria were identified using standard microbiological techniques. Statistical analysis All data were collected and managed using EpiInfo version 6.04b (Centers for Disease Control and Prevention, Atlanta, Georgia). Bacterial counts on hands were measured before and after hand hygiene. Log10 bacteria counts were reported as mean counts for all HCWs tested by all solutions and stratified by filtered/unfiltered water. Results from the 7 departments studied (emergency, gastroenterology, hepatobiliary, nephrology, poison center, cardiology, and infectious diseases) were aggregated owing to the small numbers of HCWs in each department participating. When analyzed separately, the pediatric department showed the highest hand contamination owing to frequent touching during interactions with pediatric patients and their patient zones. Statistical analysis included mean, variance, and SD CFU counts. Differences in mean CFU identified by sex, ward, and patient contacts and between filtered and unfiltered water were tested using the Student t test. Differences in mean CFU identified in the before and after hand hygiene samples were tested using a 2-tailed paired t test or nonparametric Mann-Whitney U test. The effect of glove use on CFU was controlled by stratification. Statistical analyses were performed using SPSS version 19 (IBM, Armonk, New York), with alpha set at the 5% level.
Data collection Ethical considerations The research team comprised infection control practitioners who were responsible for all data collection, including collecting hand cultures, and 2 laboratory technicians from the microbiology department who were responsible for processing the cultures. The team attended a 1-day training course on the study objectives, research activities, data collection methodology, and microbiological procedures, including the 5-fingertip technique, specimen handling, transportation, and storage. Data collected included profession, sex, department, care activity, glove use, hand hygiene solution used, and knowledge of hospital hand hygiene protocols. HCWs’ hands were sampled before and after hand hygiene. Before collection of the postehand hygiene sample, each participant was verbally reminded of the Bach Mai Hospital hand hygiene protocol, developed in accordance with the World Health Organization guidelines.10,11 Participants were also required to observe the
The study protocol was reviewed and approved by Bach Mai Hospital’s Ethics Committee, which waived the need for receipt of informed consent before the study. Verbal consent was obtained from each participant to allow the use of data obtained for analysis and reporting. No HCW participant refused to be involved in the study. RESULTS A total of 134 HCWs were enrolled,. including 65 nurses, 49 physicians, and 20 other HCWs. Participants were enrolled from the ICU (n ¼ 52), surgical department (n ¼ 10), pediatric department (n ¼ 5), and 7 other medical departments (n ¼ 67). The majority of the participants (63%; n ¼ 85) were female. Bacterial
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S. Salmon et al. / American Journal of Infection Control 42 (2014) 178-81
Table 1 Contamination of HCWs’ hands before hand hygiene Study variable
Mean CFU, log10 SD
Variance
P value
1.54 0.54 1.75 0.41
0.29 0.17
.012
1.63 0.50 1.68 0.47
0.25 0.22
.58
1.62 0.48 1.67 0.47 1.69 0.55
0.23 0.23 0.30
.753
1.58 1.80 1.84 1.70
0.53 0.28 0.33 0.44
0.29 0.28 0.33 0.44
.317
1.44 1.67 1.73 1.99 2.10
0.59 0.42 0.39 0.34 0.11
0.35 0.42 0.39 0.34 0.01
.050
Wearing gloves during care provision Yes (n ¼ 64) No (n ¼ 70) Sex Female (n ¼ 85) Male (n ¼ 49) Occupation Nurse (n ¼ 65) Physicians (n ¼ 49) Other HCWs (n ¼ 20) Clinical departments Intensive care unit (n ¼ 52) Surgical ward (n ¼ 10) Pediatric ward (n ¼ 5) Others (n ¼ 47) Patient contact activities Contact with body fluid, secretions, waste (n ¼ 41) Contact with surfaces in patient surroundings (n ¼ 31) Contact with patient intact skin (n ¼ 53) Contact with environmental surfaces outside the patient area (n ¼ 4) No contact (n ¼ 5)
Table 2 Antibacterial efficacy of different hand hygiene methods Mean CFU* log10 SD (variance) Solution Plain soap solution, unfiltered water (n ¼ 24) Plain soap solution, filtered water (n ¼ 43) P value, mean CFU difference in filtered and unfiltered water CHG 4%, unfiltered water (n ¼ 6) CHG 4%, filtered water (n ¼ 29) ABHR (n ¼ 32)
Before
After
CFU reduction
1.81 0.31 (0.097) 1.54 0.52 (0.266)
1.71 0.51 (0.261) 0.74 0.51 (0.264) <.001 1.00 0.88 (0.771) 0.45 0.41 (0.169) 0.20 0.36 (0.132)
0.12 0.56 (0.318); P ¼ .422 0.80 0.43 (0.18); P < .0001
1.56 0.29 (0.083) 1.75 0.47 (0.224) 1.60 0.55 (0.308)
0.58 0.84 (0.712); P ¼ .173 1.30 0.55 (0.301); P < .0001 1.40 0.60 (0.365); P < .0001
*Mean CFU log10 of aggregated microorganisms.
counts were similar across the departments (P ¼ .317; Table 1). Mean CFU counts for the before hand hygiene samples ranged from 1.58 log10 to 1.84 log10, with an overall average of 1.65 0.48 log10 CFUs. No significant differences in bacterial counts for the before hand hygiene sampling by sex (P ¼ .58) or HCW profession (P ¼ .753) were noted (Table 1). The mean log count for was higher in samples from HCWs wearing gloves comparede with those from HCWs not wearing gloves (1.75 log10 vs 1.54 log10; P ¼ .013; data not shown). After adjustment for glove use, no significant differences in bacterial hand contamination by HCW profession was seen (P ¼ .253). Differences in hand contamination between departments remained nonsignificant after controlling for glove use (P ¼ .581). Hand contamination differed significantly across patient contact activities. The highest bacterial counts were associated with having no direct patient contact (2.10 log10), followed by recent contact with environmental surfaces outside patient areas (1.99 log10) (P ¼ .05). Analysis of each hand hygiene method for reduction in bacterial colony counts found that ABHR was associated with the greatest reduction (1.4 log10; P < .0001; Table 2). CHG with filtered water was also associated with a significant reduction (1.3 log10; P < .0001), but CHG with unfiltered water was not (P ¼ .173). Bacterial counts were markedly reduced after hand hygiene with ABHR (1.4 log10; P < .0001), CHG with filtered water (0.8 log10; P < .0001), and plain soap and filtered water (0.8 log10; P < .0001). The use of unfiltered water was associated with minimal, nonsignificant bacterial reduction. Table 3 shows average reductions in bacterial hand contamination according to the different methods used for hand
cleansing. Both commensals and pathogens commonly associated with HAIs were recovered from HCWs’ hands in all groups. The mean bacterial count reduction was similar among bacterial groups for all hand hygiene formulations with the exception of ABHR and CHG with filtered water. DISCUSSION Understanding and providing HCWs with evidence on the dynamics of hand contamination can demonstrate the importance of hand hygiene compliance.3,11 Based on the before hand hygiene samples obtained, our findings suggest that contamination of HCWs’ hands did not require direct contact with patients. The average number of CFU count found on HCWs’ hands without direct patient care was 1.86 log10, which was higher than that in HCWs who performed direct patient care (1.3-1.4 log10) or contact with the patient environment (1.5 log10).12 Our findings are in agreement with those of Kampf et al,4 who found that HCWs’ gloved hands had the highest contamination level after several hours of not performing hand hygiene. The most frequent pathogens isolated from HCWs’ hands included Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus, which are common causes of HAI in Bach Mai Hospital,2 suggesting that the hands represent a significant intermediary step in transmission of HAIs.1-3 We evaluated the antibacterial efficacy of 5 different hand hygiene methods used at our hospital and identified the most potent for reducing bacterial counts on HCWs’ hands. Hand antiseptic agents (CHG with filtered water or ABHR) proved to decontaminate hands better than handwashing with plain soap and water. In
S. Salmon et al. / American Journal of Infection Control 42 (2014) 178-81 Table 3 Antibacterial efficacy of 5 different hand hygiene methods according to bacterial hand flora Filtered water
Hand hygiene method
No
Plain soap CHG 4%
Yes
Plain soap CHG 4%
_
ABHR
Pathogen*
n
Mean CFU log10 reductiony
SD
Variance
Commensals Pathogen Commensals Pathogen Commensals Pathogen Commensals Pathogen Commensals Pathogen
15 9 3 3 34 9 25 4 26 6
0.07 0.19 0.62 0.53 0.76 0.93 1.24 1.71 1.29 1.89
0.64 0.43 0.63 1.17 0.42 0.48 0.55 0.35 0.56 0.57
0.41 0.19 0.40 1.38 0.17 0.23 0.30 0.12 0.32 0.32
*Pathogens included Staphylococcus aureus, Acinetobacter baumannii, Klebsiella pneumoniae, and Streptococcus spp. Mean CFU log10 of aggregated microorganisms before and after hand hygiene by method and type of filtered water.
y
agreement with previous studies,3,7,8,11 we found that only the use of ABHR completely reduced hand pathogens, which confirms the superior efficacy of ABHR in removing organisms compared with other methods.11,13,14 HCWs already adopt a “no touch” or “minimal touch” technique, which plays a crucial role in reducing hand contamination. However, tap water is a possible source of microbial contamination, and hospital water quality must adhere to national regulations and meet quality standards.11 Bach Mai Hospital does not adhere to the national regulations because the water does not contain chloride, and yet HCWs continue to handwash with soap and water rather than use ABHR under the mistaken belief that handwashing is more efficacious (personal communications with participants). Although handwashing is the preferred method for hand hygiene when hands are visibly dirty or soiled with blood or other body fluids, handwashing facilities are not always available or functional in patient rooms. Adopting a no touch or minimal touch technique may play a crucial role in reducing contamination of HCWs’ hands. In resource-limited settings where the health budget is often restricted, locally produced ABHR can be less than half the cost of imported ABHR. As an example, SDS Hand Rub (SDS) costs US $5-6 per liter, compared with US $10-12 per liter for an imported commercial product. In addition, the use of water filters is an expensive and nonsustainable option; 1 filter costs roughly US $200, and breakdowns and malfunctions are frequent owing to inappropriate disposal practices and use of sinks. In summary, the present study supports the fact that hand rubbing with alcohol-based formulations is superior to handwashing with soap irrespective of water quality or hand cleansing with CHG solution with unfiltered water. Although our sample of CHG and unfiltered water was small, the lack of CFU reduction was also observed when unfiltered water was used with plain soap. ABHR significantly reduced CFU counts, and we believe that our findings support the use of ABHR as an additional step after handwashing with unfiltered water for visibly dirty hands in clinical areas where filtered water is unavailable. In a future follow-up future study, all participants should be requested to perform all 5 hand hygiene methods in random order (on different days) to assess the quality of each method. Moreover, monitoring and feedback to HCWs on hand hygiene and glove use compliance should be implemented to emphasize that whereas gloves provide
181
protection against hand contamination, especially when handling or anticipating contact with blood and body fluids, gloves should never replace the need to perform hand hygiene.11,15 Study limitations include the many nonsignificant findings, which could be related to sample size. In addition, there is reduced generalizability to the nondominant hand. However, the dominant hand is used more frequently during daily practice and is more likely to be associated with cross-transmission. We cannot fully appreciate the clinical implications of our findings, given that the threshold of bacterial hand contamination associated with an increased risk for HAI acquisition remains unknown and undocumented; nonetheless, the isolation of pathogens and the demonstrated efficacy of ABHR support their pivotal role in the control and prevention of HAIs.9,11,16 Acknowledgment We thank the staff of Bach Mai Hospital who kindly volunteered to assist with this study. References 1. Pittet D, Allegranzi B, Sax H, Dharan S, Pessoa-Silva CL, Donaldson L, et al. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis 2006;6:641-52. 2. Duckro AN, Blom DW, Lyle EA, Weinstein RA, Hayden MK. Transfer of vancomycin-resistant enterococci via health care worker hands. Arch Intern Med 2005;165:302-7. 3. Pittet D, Dharan S, Touveneau S, Sauvan V, Perneger TV. Bacterial contamination of the hands of hospital staff during routine patient care. Arch Intern Med 1999;159:821-6. 4. Kampf G, Kramer A. Epidemiologic background of hand hygiene and evaluation of the most important agents for scrubs and rubs. Clin Microbiol Rev 2004;17: 863-93. 5. Brouwer DH, Kroese R, Van Hemmen JJ. Transfer of contaminants from surface to hands: experimental assessment of linearity of the exposure process, adherence to the skin, and area exposed during fixed pressure and repeated contact with surfaces contaminated with a powder. Appl Occup Environ Hyg 1999;14:231-9. 6. Nystrom B. Impact of handwashing on mortality in intensive care: examination of the evidence. Infect Control Hosp Epidemiol 1994;15:435-6. 7. Larson E. Skin hygiene and infection prevention: more of the same or different approaches? Clin Infect Dis 1999;29:1287-94. 8. Wendt C, Knautz D, von Baum H. Differences in hand hygiene behavior related to the contamination risk of healthcare activities in different groups of healthcare workers. Infect Control Hosp Epidemiol 2004;25:203-6. 9. Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V, Touveneau S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Infection Control Programme. Lancet 2000;356:1307-12. 10. Dharan S, Hugonnet S, Sax H, Pittet D. Comparison of waterless hand antisepsis agents at short application times: raising the flag of concern. Infect Control Hosp Epidemiol 2003;24:160-4. 11. World Health Organization. WHO guidelines on hand hygiene in health care, 2009. Geneva [Switzerland]: World Health Organization; 2009. 12. Coello R, Jimenez J, Garcia M, Arroyo P, Minguez D, Fernandez C, et al. Prospective study of infection, colonization and carriage of methicillin-resistant Staphylococcus aureus in an outbreak affecting 990 patients. Eur J Clin Microbiol Infect Dis 1994;13:74-81. 13. Picheansathian W. A systematic review on the effectiveness of alcohol-based solutions for hand hygiene. Int J Nurs Pract 2004;10:3-9. 14. Trick WE, Vernon MO, Hayes RA, Nathan C, Rice TW, Peterson BJ, et al. Impact of ring wearing on hand contamination and comparison of hand hygiene agents in a hospital. Clin Infect Dis 2003;36:1383-90. 15. Beltrami EM, Kozak A, Williams IT, Saekhou AM, Kalish ML, Nainan OV, et al. Transmission of HIV and hepatitis C virus from a nursing home patient to a health care worker. Am J Infect Control 2003;31:168-75. 16. Boyce JM, Pittet D, Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Guideline for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Society for Healthcare Epidemiology of America/Association for Professionals in Infection Control/Infectious Diseases Society of America. MMWR Recomm Rep 2002;51(RR-16):1-45.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Health care workers’ hand contamination levels and antibacterial efficacy of different hand hygiene methods used in a Vietnamese hospital Sharon Salmon BN, MPH a, Anh Thu Truong MD, PhD b, Viet Hung Nguyen MD, PhD b, Didier Pittet MD, MS c, Mary-Louise McLaws DipTropPH, MPHlth, PhD a, * a b c
UNSW Medicine, University of New South Wales, Sydney, Australia Department of Infection Control, Bach Mai Hospital, Hanoi, Vietnam Infection Control Program and World Health Organization Collaborating Centre on Patient Safety, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Key Words: Alcohol-based hand rub Water quality Handwashing Antimicrobial efficacy
Background: Handwashing with soap or another antisepsis disinfectant solution is a common practice in Vietnam, but the availability and quality of tap water is unpredictable. We assessed the risk for hand contamination and compared the efficacy of 5 hand hygiene methods in a tertiary Vietnamese hospital. Methods: Five fingertip imprints of the dominant hand of 134 health care workers (HCWs) were sampled to establish the average bacterial count before and after hand hygiene action using (1) alcohol-based handrub (ABHR), (2) plain soap and water handwashing with filtered and unfiltered water, or (3) 4% chlorhexidine gluconate hand antisepsis with filtered and unfiltered water. Results: Average bacterial contamination of hands before hand hygiene was 1.65 log10. Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus were the most commonly isolated bacterial pathogens. The highest average count before hand hygiene was recovered from HCWs without direct patient contact (2.10 0.11 log10). Bacterial counts were markedly reduced after hand hygiene with ABHR (1.4 log10; P < .0001) and 4% chlorhexidine gluconate with filtered water (0.8 log10; P < .0001). Use of unfiltered water was associated with minimal nonsignificant bacterial reduction. Conclusions: HCWs carry high levels of bacteria on their dominant hand, even without direct patient contact. ABHR as an additional step may overcome the effect of high bacterial counts in unfiltered water when soap and water handwashing is indicated. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Hand hygiene is cost-effective and critical in reducing the transfer of transient flora, including bacteria, viruses, and fungi, from the hands of health care workers (HCWs) to patients.1-3 Transient flora can be recovered from skin after contamination for short periods, but they do not usually multiply on skin surfaces, except under facilitating conditions, particularly on gloved hands.4,5 Although transient flora are the pathogens most frequently related to health careeassociated infections (HAIs), routine hand hygiene can decontaminate HCW hands.6 Over the past decade, various hand hygiene methods have been reported to significantly reduce bacterial load and prevent cross-
* Address correspondence to Professor Mary-Louise McLaws, DipTropPH, MPHlth, PhD, UNSW Medicine, University of New South Wales, School of Public Health and Community Medicine, Level 3 Samuels Building, Sydney, NSW 2052, Australia. E-mail address: [email protected] (M.-L. McLaws). Conflict of interest: None to report.
transmission resulting in colonization or HAI.7 In clinical practice, alcohol-based hand rub (ABHR) has been documented to reduce bacterial counts more effectively than handwashing with soap and/ or other chemical products.4 In addition, the time savings associated with the use of ABHR has improved HCW hand hygiene compliance.3,7-9 Poor water quality monitoring, maintenance of water systems, and local enforcement of national water quality standards is a concern at all levels of health care facilities across Vietnam. Major barriers to hand hygiene compliance in Vietnam include the lack of basic equipment, particularly alcohol-based formulations. Many HCWs cannot wash their hands with soap and water at the point of care because of limited or dysfunctional sinks or lack of soap, stemming from hospital management’s concerns that soap will be taken by patients’ relatives and other visitors. Only wards with high-risk patients are equipped with ABHR because of the high costs associated with these formulations. The aims of the present study were to assess risk factors for HCW hand contamination
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2013.07.013
S. Salmon et al. / American Journal of Infection Control 42 (2014) 178-81
and to compare the antibacterial efficacy of hand hygiene using 5 methods in a tertiary Vietnamese hospital. METHODS Study site Founded in 1911 during the French colonization, Bach Mai Hospital in Hanoi is the largest tertiary medical health care facility in Vietnam, with 1,900 beds. It is a major medical teaching center, responsible for training most internal medicine physicians in the country. Approximately 45,000 patients are discharged annually, with triple bed occupancy owing to more than 1 patient per bed in wards outside the intensive care unit (ICU). Since 2002, the hospital has instituted hospital-wide multimodal hand hygiene campaigns that have included HCW training, education materials, and availability of ABHR in the ICU and general wards. Participant selection HCWs were enrolled in this study over 9 weekdays during December 2006 from 10 selected clinical departments (ICU, surgical, pediatrics, emergency, gastroenterology, hepatobiliary, nephrology, poison center, cardiology, and infectious diseases) in which the study was conducted. A minimum of 3 HCWs (1 physician, 1 nurse, and 1 other HCW) were selected at random from each department. Infection control staff selected the first HCW encountered in the first patient room in the participating departments. If no HCWs were present in the first patient room, the researcher would then enter another patient room. Participants were required to undergo hand hygiene training. On completion of training, participants were randomly assigned to 1 of 5 hand hygiene techniques: ABHR, 4% chlorhexidine gluconate (CHG) with filtered or unfiltered water, and soap and water handwashing with filtered or unfiltered water. The 3 hand hygiene solutions were SDS Hand Rub, containing ethanol (83%), isopropyl alcohol (12%), and chlorhexidine digluconate (0.5%) (SDS, Ha Noi, Vietnam); SDS Hand Wash, containing sodium lauryl ether sulphate (12%), coconut fatty acid diethanol amide (3%), and cocamido propyl betain (3%) (SDS Vietnam); and 4% CHG solution (Microshield; Johnson & Johnson Medical, Sydney, Australia). A Filtranios 31 DA filter (Laboratoires Anios, Lille-Hellemmes, France) was attached to the tap by removing the tap aerator and replacing it with a faucet adapter, and then attaching the filter. Two cultures were obtained from all participants, 1 before hand hygiene and 1 after hand hygiene. Hands were not visibly soiled at the time of hand plating.
179
researcher performing the technique. All participants received instruction on the 4 technical requirements for hand hygiene: the correct amount of solution to apply, hand hygiene thoroughness, duration of hand hygiene, and hand drying technique. A participant who failed to perform the technique correctly was excluded from the study. Hand hygiene was then performed using the assigned method, and a sample was obtained 1 minute later. Culture samples were obtained and labeled according to the hand hygiene method used. Microbiological procedures Samples were obtained by imprinting all 5 fingertips of the HCW’s dominant hand using commercial agar plates (BioMérieux, Marcy l’Etoile, France). Fingertips were gently pressed against the agar for 15 seconds.3,10 Hand hygiene was then performed using the assigned method, and a sample was obtained 1 minute later. Plates were transferred to the hospital’s microbiology department within 1 hour of sampling. The same 2 trained laboratory technicians blinded to the product and water quality information processed all samples. Plates were then incubated at 37 C under aerobic conditions, and colony-forming units (CFUs) were counted after incubation of 24-48 hours. Bacteria were identified using standard microbiological techniques. Statistical analysis All data were collected and managed using EpiInfo version 6.04b (Centers for Disease Control and Prevention, Atlanta, Georgia). Bacterial counts on hands were measured before and after hand hygiene. Log10 bacteria counts were reported as mean counts for all HCWs tested by all solutions and stratified by filtered/unfiltered water. Results from the 7 departments studied (emergency, gastroenterology, hepatobiliary, nephrology, poison center, cardiology, and infectious diseases) were aggregated owing to the small numbers of HCWs in each department participating. When analyzed separately, the pediatric department showed the highest hand contamination owing to frequent touching during interactions with pediatric patients and their patient zones. Statistical analysis included mean, variance, and SD CFU counts. Differences in mean CFU identified by sex, ward, and patient contacts and between filtered and unfiltered water were tested using the Student t test. Differences in mean CFU identified in the before and after hand hygiene samples were tested using a 2-tailed paired t test or nonparametric Mann-Whitney U test. The effect of glove use on CFU was controlled by stratification. Statistical analyses were performed using SPSS version 19 (IBM, Armonk, New York), with alpha set at the 5% level.
Data collection Ethical considerations The research team comprised infection control practitioners who were responsible for all data collection, including collecting hand cultures, and 2 laboratory technicians from the microbiology department who were responsible for processing the cultures. The team attended a 1-day training course on the study objectives, research activities, data collection methodology, and microbiological procedures, including the 5-fingertip technique, specimen handling, transportation, and storage. Data collected included profession, sex, department, care activity, glove use, hand hygiene solution used, and knowledge of hospital hand hygiene protocols. HCWs’ hands were sampled before and after hand hygiene. Before collection of the postehand hygiene sample, each participant was verbally reminded of the Bach Mai Hospital hand hygiene protocol, developed in accordance with the World Health Organization guidelines.10,11 Participants were also required to observe the
The study protocol was reviewed and approved by Bach Mai Hospital’s Ethics Committee, which waived the need for receipt of informed consent before the study. Verbal consent was obtained from each participant to allow the use of data obtained for analysis and reporting. No HCW participant refused to be involved in the study. RESULTS A total of 134 HCWs were enrolled,. including 65 nurses, 49 physicians, and 20 other HCWs. Participants were enrolled from the ICU (n ¼ 52), surgical department (n ¼ 10), pediatric department (n ¼ 5), and 7 other medical departments (n ¼ 67). The majority of the participants (63%; n ¼ 85) were female. Bacterial
180
S. Salmon et al. / American Journal of Infection Control 42 (2014) 178-81
Table 1 Contamination of HCWs’ hands before hand hygiene Study variable
Mean CFU, log10 SD
Variance
P value
1.54 0.54 1.75 0.41
0.29 0.17
.012
1.63 0.50 1.68 0.47
0.25 0.22
.58
1.62 0.48 1.67 0.47 1.69 0.55
0.23 0.23 0.30
.753
1.58 1.80 1.84 1.70
0.53 0.28 0.33 0.44
0.29 0.28 0.33 0.44
.317
1.44 1.67 1.73 1.99 2.10
0.59 0.42 0.39 0.34 0.11
0.35 0.42 0.39 0.34 0.01
.050
Wearing gloves during care provision Yes (n ¼ 64) No (n ¼ 70) Sex Female (n ¼ 85) Male (n ¼ 49) Occupation Nurse (n ¼ 65) Physicians (n ¼ 49) Other HCWs (n ¼ 20) Clinical departments Intensive care unit (n ¼ 52) Surgical ward (n ¼ 10) Pediatric ward (n ¼ 5) Others (n ¼ 47) Patient contact activities Contact with body fluid, secretions, waste (n ¼ 41) Contact with surfaces in patient surroundings (n ¼ 31) Contact with patient intact skin (n ¼ 53) Contact with environmental surfaces outside the patient area (n ¼ 4) No contact (n ¼ 5)
Table 2 Antibacterial efficacy of different hand hygiene methods Mean CFU* log10 SD (variance) Solution Plain soap solution, unfiltered water (n ¼ 24) Plain soap solution, filtered water (n ¼ 43) P value, mean CFU difference in filtered and unfiltered water CHG 4%, unfiltered water (n ¼ 6) CHG 4%, filtered water (n ¼ 29) ABHR (n ¼ 32)
Before
After
CFU reduction
1.81 0.31 (0.097) 1.54 0.52 (0.266)
1.71 0.51 (0.261) 0.74 0.51 (0.264) <.001 1.00 0.88 (0.771) 0.45 0.41 (0.169) 0.20 0.36 (0.132)
0.12 0.56 (0.318); P ¼ .422 0.80 0.43 (0.18); P < .0001
1.56 0.29 (0.083) 1.75 0.47 (0.224) 1.60 0.55 (0.308)
0.58 0.84 (0.712); P ¼ .173 1.30 0.55 (0.301); P < .0001 1.40 0.60 (0.365); P < .0001
*Mean CFU log10 of aggregated microorganisms.
counts were similar across the departments (P ¼ .317; Table 1). Mean CFU counts for the before hand hygiene samples ranged from 1.58 log10 to 1.84 log10, with an overall average of 1.65 0.48 log10 CFUs. No significant differences in bacterial counts for the before hand hygiene sampling by sex (P ¼ .58) or HCW profession (P ¼ .753) were noted (Table 1). The mean log count for was higher in samples from HCWs wearing gloves comparede with those from HCWs not wearing gloves (1.75 log10 vs 1.54 log10; P ¼ .013; data not shown). After adjustment for glove use, no significant differences in bacterial hand contamination by HCW profession was seen (P ¼ .253). Differences in hand contamination between departments remained nonsignificant after controlling for glove use (P ¼ .581). Hand contamination differed significantly across patient contact activities. The highest bacterial counts were associated with having no direct patient contact (2.10 log10), followed by recent contact with environmental surfaces outside patient areas (1.99 log10) (P ¼ .05). Analysis of each hand hygiene method for reduction in bacterial colony counts found that ABHR was associated with the greatest reduction (1.4 log10; P < .0001; Table 2). CHG with filtered water was also associated with a significant reduction (1.3 log10; P < .0001), but CHG with unfiltered water was not (P ¼ .173). Bacterial counts were markedly reduced after hand hygiene with ABHR (1.4 log10; P < .0001), CHG with filtered water (0.8 log10; P < .0001), and plain soap and filtered water (0.8 log10; P < .0001). The use of unfiltered water was associated with minimal, nonsignificant bacterial reduction. Table 3 shows average reductions in bacterial hand contamination according to the different methods used for hand
cleansing. Both commensals and pathogens commonly associated with HAIs were recovered from HCWs’ hands in all groups. The mean bacterial count reduction was similar among bacterial groups for all hand hygiene formulations with the exception of ABHR and CHG with filtered water. DISCUSSION Understanding and providing HCWs with evidence on the dynamics of hand contamination can demonstrate the importance of hand hygiene compliance.3,11 Based on the before hand hygiene samples obtained, our findings suggest that contamination of HCWs’ hands did not require direct contact with patients. The average number of CFU count found on HCWs’ hands without direct patient care was 1.86 log10, which was higher than that in HCWs who performed direct patient care (1.3-1.4 log10) or contact with the patient environment (1.5 log10).12 Our findings are in agreement with those of Kampf et al,4 who found that HCWs’ gloved hands had the highest contamination level after several hours of not performing hand hygiene. The most frequent pathogens isolated from HCWs’ hands included Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus, which are common causes of HAI in Bach Mai Hospital,2 suggesting that the hands represent a significant intermediary step in transmission of HAIs.1-3 We evaluated the antibacterial efficacy of 5 different hand hygiene methods used at our hospital and identified the most potent for reducing bacterial counts on HCWs’ hands. Hand antiseptic agents (CHG with filtered water or ABHR) proved to decontaminate hands better than handwashing with plain soap and water. In
S. Salmon et al. / American Journal of Infection Control 42 (2014) 178-81 Table 3 Antibacterial efficacy of 5 different hand hygiene methods according to bacterial hand flora Filtered water
Hand hygiene method
No
Plain soap CHG 4%
Yes
Plain soap CHG 4%
_
ABHR
Pathogen*
n
Mean CFU log10 reductiony
SD
Variance
Commensals Pathogen Commensals Pathogen Commensals Pathogen Commensals Pathogen Commensals Pathogen
15 9 3 3 34 9 25 4 26 6
0.07 0.19 0.62 0.53 0.76 0.93 1.24 1.71 1.29 1.89
0.64 0.43 0.63 1.17 0.42 0.48 0.55 0.35 0.56 0.57
0.41 0.19 0.40 1.38 0.17 0.23 0.30 0.12 0.32 0.32
*Pathogens included Staphylococcus aureus, Acinetobacter baumannii, Klebsiella pneumoniae, and Streptococcus spp. Mean CFU log10 of aggregated microorganisms before and after hand hygiene by method and type of filtered water.
y
agreement with previous studies,3,7,8,11 we found that only the use of ABHR completely reduced hand pathogens, which confirms the superior efficacy of ABHR in removing organisms compared with other methods.11,13,14 HCWs already adopt a “no touch” or “minimal touch” technique, which plays a crucial role in reducing hand contamination. However, tap water is a possible source of microbial contamination, and hospital water quality must adhere to national regulations and meet quality standards.11 Bach Mai Hospital does not adhere to the national regulations because the water does not contain chloride, and yet HCWs continue to handwash with soap and water rather than use ABHR under the mistaken belief that handwashing is more efficacious (personal communications with participants). Although handwashing is the preferred method for hand hygiene when hands are visibly dirty or soiled with blood or other body fluids, handwashing facilities are not always available or functional in patient rooms. Adopting a no touch or minimal touch technique may play a crucial role in reducing contamination of HCWs’ hands. In resource-limited settings where the health budget is often restricted, locally produced ABHR can be less than half the cost of imported ABHR. As an example, SDS Hand Rub (SDS) costs US $5-6 per liter, compared with US $10-12 per liter for an imported commercial product. In addition, the use of water filters is an expensive and nonsustainable option; 1 filter costs roughly US $200, and breakdowns and malfunctions are frequent owing to inappropriate disposal practices and use of sinks. In summary, the present study supports the fact that hand rubbing with alcohol-based formulations is superior to handwashing with soap irrespective of water quality or hand cleansing with CHG solution with unfiltered water. Although our sample of CHG and unfiltered water was small, the lack of CFU reduction was also observed when unfiltered water was used with plain soap. ABHR significantly reduced CFU counts, and we believe that our findings support the use of ABHR as an additional step after handwashing with unfiltered water for visibly dirty hands in clinical areas where filtered water is unavailable. In a future follow-up future study, all participants should be requested to perform all 5 hand hygiene methods in random order (on different days) to assess the quality of each method. Moreover, monitoring and feedback to HCWs on hand hygiene and glove use compliance should be implemented to emphasize that whereas gloves provide
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protection against hand contamination, especially when handling or anticipating contact with blood and body fluids, gloves should never replace the need to perform hand hygiene.11,15 Study limitations include the many nonsignificant findings, which could be related to sample size. In addition, there is reduced generalizability to the nondominant hand. However, the dominant hand is used more frequently during daily practice and is more likely to be associated with cross-transmission. We cannot fully appreciate the clinical implications of our findings, given that the threshold of bacterial hand contamination associated with an increased risk for HAI acquisition remains unknown and undocumented; nonetheless, the isolation of pathogens and the demonstrated efficacy of ABHR support their pivotal role in the control and prevention of HAIs.9,11,16 Acknowledgment We thank the staff of Bach Mai Hospital who kindly volunteered to assist with this study. References 1. Pittet D, Allegranzi B, Sax H, Dharan S, Pessoa-Silva CL, Donaldson L, et al. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis 2006;6:641-52. 2. Duckro AN, Blom DW, Lyle EA, Weinstein RA, Hayden MK. Transfer of vancomycin-resistant enterococci via health care worker hands. Arch Intern Med 2005;165:302-7. 3. Pittet D, Dharan S, Touveneau S, Sauvan V, Perneger TV. Bacterial contamination of the hands of hospital staff during routine patient care. Arch Intern Med 1999;159:821-6. 4. Kampf G, Kramer A. Epidemiologic background of hand hygiene and evaluation of the most important agents for scrubs and rubs. Clin Microbiol Rev 2004;17: 863-93. 5. Brouwer DH, Kroese R, Van Hemmen JJ. Transfer of contaminants from surface to hands: experimental assessment of linearity of the exposure process, adherence to the skin, and area exposed during fixed pressure and repeated contact with surfaces contaminated with a powder. Appl Occup Environ Hyg 1999;14:231-9. 6. Nystrom B. Impact of handwashing on mortality in intensive care: examination of the evidence. Infect Control Hosp Epidemiol 1994;15:435-6. 7. Larson E. Skin hygiene and infection prevention: more of the same or different approaches? Clin Infect Dis 1999;29:1287-94. 8. Wendt C, Knautz D, von Baum H. Differences in hand hygiene behavior related to the contamination risk of healthcare activities in different groups of healthcare workers. Infect Control Hosp Epidemiol 2004;25:203-6. 9. Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V, Touveneau S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Infection Control Programme. Lancet 2000;356:1307-12. 10. Dharan S, Hugonnet S, Sax H, Pittet D. Comparison of waterless hand antisepsis agents at short application times: raising the flag of concern. Infect Control Hosp Epidemiol 2003;24:160-4. 11. World Health Organization. WHO guidelines on hand hygiene in health care, 2009. Geneva [Switzerland]: World Health Organization; 2009. 12. Coello R, Jimenez J, Garcia M, Arroyo P, Minguez D, Fernandez C, et al. Prospective study of infection, colonization and carriage of methicillin-resistant Staphylococcus aureus in an outbreak affecting 990 patients. Eur J Clin Microbiol Infect Dis 1994;13:74-81. 13. Picheansathian W. A systematic review on the effectiveness of alcohol-based solutions for hand hygiene. Int J Nurs Pract 2004;10:3-9. 14. Trick WE, Vernon MO, Hayes RA, Nathan C, Rice TW, Peterson BJ, et al. Impact of ring wearing on hand contamination and comparison of hand hygiene agents in a hospital. Clin Infect Dis 2003;36:1383-90. 15. Beltrami EM, Kozak A, Williams IT, Saekhou AM, Kalish ML, Nainan OV, et al. Transmission of HIV and hepatitis C virus from a nursing home patient to a health care worker. Am J Infect Control 2003;31:168-75. 16. Boyce JM, Pittet D, Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Guideline for hand hygiene in health-care settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Society for Healthcare Epidemiology of America/Association for Professionals in Infection Control/Infectious Diseases Society of America. MMWR Recomm Rep 2002;51(RR-16):1-45.