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Hand Rubbing with Sprayed Alcohol-Based Hand Rub: An Alternative Method for Effective Hand Hygiene
Journal Pre-proof Hand Rubbing with Sprayed Alcohol-Based Hand Rub: An Alternative Method for Effective Hand Hygiene Jamie Bee Xian Tan, Marlieke E.A. de Kraker, Daniela Pires, Hervé Soule, Didier Pittet PII:
S0195-6701(20)30056-6
DOI:
https://doi.org/10.1016/j.jhin.2020.02.008
Reference:
YJHIN 5913
To appear in:
Journal of Hospital Infection
Received Date: 1 December 2019 Accepted Date: 10 February 2020
Please cite this article as: Xian Tan JB, de Kraker MEA, Pires D, Soule H, Pittet D, Hand Rubbing with Sprayed Alcohol-Based Hand Rub: An Alternative Method for Effective Hand Hygiene, Journal of Hospital Infection, https://doi.org/10.1016/j.jhin.2020.02.008. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
Hand Rubbing with Sprayed Alcohol-Based Hand Rub: An Alternative Method for Effective Hand Hygiene
Jamie Bee Xian Tan, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland; Department of Microbiology, Singapore General Hospital, Singapore; Duke-NUS Medical School, Singapore Marlieke E.A. de Kraker, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Daniela Pires, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Hervé Soule, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Didier Pittet, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Running title: Handrubbing with sprayed ABHR effective
Word count: 2438 Figures: 2
Corresponding author: Marlieke de Kraker Hôpitaux Universitaires de Genève Service prévention et contrôle de l'infection Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland Phone: +41 22 372 3369 | Fax: +41 22 372 3987 Email: [email protected]
Abstract (250 words)
Background: Hand hygiene is crucial in infection prevention and control. It is unclear whether sprayed alcohol-based handrub (ABHR) is non-inferior to the WHO recommended method of handrubbing with poured ABHR.
Aim: We tested whether sprayed ABHR can be an alternative (non-inferior) method for effective hand hygiene with/without handrubbing.
Methods: We conducted a laboratory experiment with ABHR (isopropanol 60% v/v) according to the European Norm 1500. Hand hygiene was performed by (1) handrubbing with ABHR poured onto a hand palm, (2) handrubbing with sprayed ABHR, and (3) applying sprayed ABHR on hands without rubbing. Hands were contaminated with Escherichia coli ATCC 10536, followed by hand hygiene and microbiological sampling. A generalized linear mixed model with a random intercept per subject was used to analyse the reduction in bacterial counts post-hand hygiene.
Findings: A total of 19 healthcare workers participated in the study. Handrubbing with sprayed ABHR was non-inferior (margin log10 0.6 colony forming units [CFU]/mL) to the WHO method of handrubbing with poured ABHR; bacterial count reduction was log10 3.66 CFU/mL (95% CI 1.68-5.64) and log10 3.46 CFU/mL (95% CI 1.27-5.65), respectively. Conversely, non-inferiority was not found for hand hygiene using sprayed ABHR without rubbing (bacterial count reduction: log10 2.76 CFU/mL, 95% CI 1.65-3.87).
Conclusion: Handrubbing with sprayed ABHR was non-inferior to rubbing with ABHR poured onto a hand palm to reduce bacterial counts on hands under experimental conditions. Rubbing with sprayed ABHR may be an acceptable alternative hand hygiene method pending assessment in other settings and for other pathogens.
Keywords: Hand hygiene, Alcohol-based handrub, Spray application, Handrubbing, EN 1500, guidelines, WHO ‘how to handrub’
Introduction Healthcare-associated infections (HAI) are a major patient safety problem. Disease-causing pathogens can be transmitted to patients through the hands of healthcare workers (HCW); therefore hand hygiene is one of the most important measures in preventing HAI [1, 2]. Hand hygiene compliance among healthcare workers however has been insufficient. This has led the World Health Organization (WHO) to develop a multimodal hand hygiene improvement strategy aimed at increasing hand hygiene compliance [2-5]. The WHO guidelines recommend that hand hygiene be performed using a liquid alcohol-based handrub (ABHR) that is first poured onto a hand palm followed by a six step handrubbing technique for 20-30 seconds [2].
ABHR is also available in other formats, like gels, foams, aerosols (provided by spray dispensers), or wipes, and their antimicrobial efficacy has already been extensively studied [6-12]. However, the antimicrobial efficacy of sprayed ABHR has not been assessed, even though spray dispensers have a number of advantages, including direct dispensing of ABHR onto hand surfaces, avoiding spillage, and delivery of precise, customized volumes [13]. If ABHR can be evenly distributed onto the hands, it is also unclear if handrubbing would be required for an effective hand hygiene action. The antimicrobial action of ABHR can be attributed to the protein denaturation effect of alcohol [2], and it remains unknown whether hand rubbing is required solely to help spread the liquid ABHR onto all the hand surfaces or if hand hygiene efficacy is affected if the handrubbing action is omitted entirely. As the utilization of sprays to deliver liquid ABHR has become more common in healthcare facilities, it is important to clarify the role these sprays can play in effective hand hygiene. In this study, we determined whether the antimicrobial efficacy of hand hygiene using a sprayed ABHR, with or without handrubbing, is non-inferior to rubbing with ABHR poured onto a hand palm, as currently recommended by the WHO guidelines.
Methods
Study setting, participants and eligibility criteria We conducted a laboratory-based experimental study at the microbiology laboratory of the Infection Control Program (IPC), University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland. The study was part of the IPC quality assurance program approved by the local ethics committee and all healthcare workers (HCW) agreed to participate. Nineteen locally recruited HCW who had extensive training and experience in hand hygiene according to the WHO guidelines were enrolled in the study. The number of recruited participants was based on the European Norm 1500’s recommendation of including 18 to 22 subjects [11]. All of the participants had short fingernails. Exclusion criteria included the presence of artificial nails, jewellery and skin conditions affecting the hands.
Study design All of the experiments were based on the European Norm 1500 [11]. Each participant performed three experiments using the same ABHR (isopropanol 60% v/v without any additional emollients or other ingredients). The experiments consisted of performing in, a randomized order: (1) hand hygiene using 3 mL ABHR poured onto a hand palm with 30 seconds of rubbing, (2) hand hygiene using 3 mL sprayed ABHR with 30 seconds of rubbing (Figure 1), and (3) hand hygiene using 3 mL sprayed ABHR without rubbing.
Rubbing consisted of the six step technique as promoted by WHO [2]. For experiments (1) and (2), participants were instructed to repeat each step of the WHO “How to Handrub” technique five times to ensure uniformity of the hand rubbing process; whereas for experiment (3), participants were instructed to maintain their hands in an upright position without moving for 30 seconds after applying the ABHR.
Spraying was applied by using the SARAYA GUD-1000 delivery system, SARAYA.Co.Ltd, Japan. The healthcare workers were instructed to move their fingertips under the nozzle, after which the spray instantaneously released 3 mL of ABHR (Figure 1). Before the start of the experiment, each participant practised this gesture once with a similar spray containing water.
At the start of each experiment, participants were required to first wash their hands using liquid soap and water. After contaminating their hands artificially with Escherichia coli ATCC
10536 suspension, microbiological sampling was performed both before and after the experiment in order to determine the bacterial count reduction.
Artificial contamination and microbiological sampling Artificial contamination of the hands was performed by immersing both hands up to the midcarpals in a bacterial suspension containing 108 colony forming units (CFU)/mL of E. coli ATCC 10536 for 5 seconds and then holding them up to air dry for 3 minutes. At baseline and immediately after each intervention, bacteria were recovered from both hands of the healthcare workers using the fingertips method [11]. This procedure consisted of the healthcare worker rubbing all 5 fingertips of each hand in a sterile petri dish containing 10 mL of tryptone soy broth for 1 minute.
Dilution and plating of microbiological samples Microbiological samples were serially diluted and 4 different dilutions (10-1 to 10-4) were plated to accurately estimate bacterial counts. After achieving the required dilution, a 1 mL aliquot was spread over the surface of a tryptic soy agar plate before it was incubated at 36±1oC under aerobic conditions for 48 hours. The resultant E. coli colonies were quantified by visual inspection, adjusted for the corresponding dilution factor and converted to log10.
Study outcomes and statistical analysis The antimicrobial efficacy of experiment (2) and (3) was compared with experiment (1), and was determined by comparing the difference between the baseline and post-intervention bacterial counts that were recovered from the healthcare workers’ hands. Results were analysed using a generalized linear mixed model (GLMM) with random intercepts for each healthcare worker, given the repeated measures design. We also evaluated whether the reduction in bacterial counts was influenced by hand size by including this as a covariate in the model and testing the interaction between hand size and experiment. Hand surface areas were calculated and categorized as small (≤ 375 cm2), medium (376-424 cm2) and large (≥ 425 cm2) [13, 14]. Statistical analyses were performed using R studio software, version 3.0.2 (R Foundation for Statistical Computing, Vienna, Austria).
We hypothesized that hand rubbing with sprayed ABHR would not be inferior to hand rubbing with poured ABHR. The definition of non-inferiority in EN 1500 was met when the difference in bacterial count reduction was less than log10 0.6 CFU/mL between the experiments.
Results Out of the 19 healthcare workers who participated in the study, 7 (36.8%) were doctors, 5 (26.3%) were nurses, and 7 (36.8%) had other healthcare professions. The majority was female (13/19, 68.4%), six (31.6%) healthcare workers had small hands, 9 (47.4%) had medium hands, and 4 (21.1%) had large hands.
The average baseline contamination of the healthcare worker hands with E. coli ATCC 10536 was log10 6.91 CFU/mL (95% confidence interval [CI], 5.90-7.91) before the hand hygiene action. Hand hygiene using 3 mL ABHR poured onto a hand palm followed by rubbing reduced bacterial load by a mean of log10 3.46 CFU/mL (95% CI, 1.27-5.65). Hand hygiene using 3 mL sprayed ABHR with rubbing reduced bacterial load by a mean of log10 3.66 CFU/mL (95% CI, 1.68-5.64). Hand hygiene using 3 mL sprayed ABHR without rubbing reduced bacterial load by a mean of log10 2.76 CFU/mL (95% CI, 1.65-3.87) (Figure 2).
The GLMM showed that, compared to hand hygiene using poured ABHR with rubbing sprayed ABHR with rubbing non-significantly increased the reduction in bacterial load by log10 0.20 CFU/mL (95% CI, -0.23 to 0.62). For hand hygiene using sprayed ABHR without rubbing, the reduction in bacterial load was significantly decreased compared to hand hygiene using liquid ABHR with rubbing by log10 -0.70 CFU/mL (95% CI, -1.13 to -0.28) (Figure 2). Adjustment for hand size did not change the effect estimates, and no significant interaction with experiment was found, so hand size was not included in the final model.
Using the - log10 0.6 CFU/mL non-inferiority margin that was specified by the European Norm 1500, hand hygiene using sprayed ABHR with rubbing was non-inferior to hand hygiene using poured ABHR with rubbing. Conversely, non-inferiority could not be confirmed for hand hygiene using sprayed ABHR without rubbing.
Discussion To the best of our knowledge, this is the first study based on the European Norm 1500 that assessed the antimicrobial efficacy of hand hygiene using aerosolized ABHR. Our study has shown that the antimicrobial efficacy of hand rubbing with sprayed ABHR is non-inferior to and not significantly different from the current WHO recommended method of performing hand hygiene using the same ABHR poured onto a hand palm with rubbing. The utilisation of sprayed ABHR without rubbing was significantly less effective than the WHO method, clearly indicating the importance of hand rubbing for adequate hand hygiene.
Despite the increasing awareness that hand hygiene is a crucial part of infection control and prevention in the hospital setting, hand hygiene among healthcare workers is still far from intuitive resulting in insufficient baseline compliance rates. Hand hygiene compliance rates, based on direct observation, reported in recently published literature, range from 23% in a Thai tertiary care hospital [15], to 35% in a tertiary care hospital in the United States [16], to 50% in a set of Belgian acute care hospitals [17], and 61.4% hand hygiene compliance in a Swiss teaching hospital [18]. In this study, we have shown that hand rubbing with aerosolized ABHR could be used as an alternative to the WHO recommended procedure of rubbing with liquid ABHR. Using a spray method to dispense the ABHR could improve hand hygiene efficacy as well as compliance. Spraying can uniformly deliver ABHR to a large hand surface area within a short period of time with minimal spillage, improving efficiency. Combined with the small droplets dispensed by the spray, time required to dry the hands and thus the hand hygiene action could be shortened as well. As it has been shown that time pressure is a major barrier to compliance, this could positively influence hand-hygiene frequency [19-21].
Effective sprays that do not require hand rubbing could further decrease the required time for hand hygiene, and as such increase hand hygiene compliance [15, 19-20]. Unfortunately, in this study, non-inferiority could not be confirmed when hand rubbing after ABHR spraying was omitted in one of our experiment arms. Development of novel spray designs, or improvements in the ABHR formula used in sprays could perhaps overcome this hurdle, and further development in this area is encouraged. Although health and safety issues should be considered, as aerosols may play a role in respiratory tract irritations, which could reduce hand hygiene compliance.
Our study has a few limitations. Firstly, our study was conducted in a laboratory setting with healthcare workers who had extensive training and experience in hand hygiene, hence the findings may not be directly generalizable to all healthcare workers, or to the clinical setting. Our study only looked at the antimicrobial efficacy of the experimental interventions against an E. coli control strain using isopropanol 60% v/v, and one type of spray. Further testing is required to see if our findings could be confirmed for commercially available ABHR formulations, or other types of sprays with different spray patterns or droplet size. The impact of other bacteria types, which are commonly encountered in the healthcare setting, should be studied as well, although in a previous study, comparing 15 to 30 seconds of hand rubbing with ABHR, pathogen type did not influence the results [22]. Finally, it remains undefined what minimum bacterial count reduction of contaminated hands is required to prevent transmission of infections in a real world setting, as such it is difficult to extrapolate experimental findings to clinical practice.
The strength of the present study is that it compared the efficacy of sprayed ABHR with and without rubbing to the established WHO hand hygiene methodology according to the standardized EN 1500 norm. The experiments were performed in a well-established infection and prevention laboratory with a large experience in hand hygiene experiments [12, 13, 21, 22], and the order of the experiments was randomized. In the statistical methods we corrected for repeated measurements among the 19 HCWs, and checked for the influence of hand size. In conclusion, this study has reliably shown that hand rubbing with sprayed ABHR is noninferior to the current WHO recommended method of hand rubbing with the same ABHR poured onto a hand palm. ABHR delivered as a spray could be an alternative method to ensure appropriate hand disinfection and patient safety as long as the correct hand rubbing steps are included. Future research should establish the efficacy of sprayed ABHR in other settings.
Transparency declaration Didier Pittet has received funding from the European Commission and National Science Foundation for several research and clinical studies, and works with the WHO in the context of the WHO initiative Private Organizations for Patient Safety Hand Hygiene. The aim of this WHO initiative is to harness industry strengths to align and improve implementation of WHO recommendations for hand hygiene in health care in different parts of the world, including in least developed countries. In this instance companies/industry with a focus on hand hygiene and infection control related advancement have the specific aim of improving access to affordable hand-hygiene products as well as through education and research. All other listed authors declare no financial support, grants, financial interests or consultancy that could lead to conflicts of interest.
Acknowledgements We acknowledge all the HCWs who participated as volunteers in the present study, and Saraya.Co.Ltd for providing the spray dispenser. Part of the data was presented at the International Conference of Infection Control (ICPIC), held in Geneva, Switzerland, on 11 September 2019 (ICPIC19-ABS-P437).
Contribution of authors JT, MdK, DPires, HS, and DP conceived the study idea. JT and HS wrote the draft of the study protocol, which was reviewed by all authors. The experiments were planned and run by JT. MdK performed the statistical analysis. JT wrote the first draft of the manuscript, which was reviewed and approved by all authors.
Conflict of interest None.
Funding This study was supported by the Infection Control Programme & WHO Collaborating Centre on Patient Safety (SPCI/WCC), University of Geneva Hospitals and Faculty of Medicine,
Geneva, Switzerland. Hand-hygiene research activities at the SPCI/WCC are supported by the National Science Foundation (32003B_163262). Daniela Pires is supported by the National Science Foundation (32003B_163262) for hand-hygiene research activities and by Fundação para a Ciência e a Tecnologia (SFRH/SINT/95317/2013). Marlieke de Kraker has received support from the Innovative Medicines Initiative Joint Undertaking (IMI) under grant agreement nos. 115523, 115620 and 115737 (Combatting Bacterial Resistance in Europe projects), resources of which are composed of financial contribution from the European Union's 7th Framework Programme (FP7/2007±2013) and the European Federation of Pharmaceutical Industries and Associations (EFPIA) companies' in-kind contribution.
Figures Figure 1. Automatic spray dispenser used for the study. Fingertips were placed under the nozzle. A pre-specified amount of ABHR was dispensed upon activation of the sensor.
Figure 2. E. coli bacterial count reduction on the hands of healthcare workers after using poured versus sprayed ABHR (3 mL) with or without rubbing.
References 1. Boyce JM, Pittet D. 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. Morb Mortal Wkly Report Recomm Reports 2002;51:1–45, quiz CE1-4. 2. World Health Organization. Guidelines on Hand Hygiene in Health Care. First Global Patient Safety Challenge: Clean Care is Safer Care. Geneva, WHO (2009). https://apps.who.int/iris/bitstream/handle/10665/44102/9789241597906_eng.pdf;jsessionid =124BBEB5607F910DD2033CFCD6F18490?sequence=1. Accessed 1 February 2019. 3. Tschudin-Sutter S, Sepulcri D, Dangel M, Schuhmacher H, Widmer AF. Compliance with the World Health Organization hand hygiene technique: a prospective observational study. Infect Control Hosp Epidemiol 2015;36:482–3. https://doi.org/10.1017/ice.2014.82 4. Musu M, Lai A, Mereu NM, Galletta M, Campagna M, Tidore M, et al. Assessing hand hygiene compliance among healthcare workers in six Intensive Care Units. J Prev Med Hyg 2017;58:E231–7. 5. World Health Organization. Guide to Implementation. A Guide to the Implementation of the WHO Multimodal Hand Hygiene Improvement Strategy. Geneva, WHO (2009). https://www.who.int/gpsc/5may/Guide_to_Implementation.pdf. Accessed 1 February 2019. 6. Wilkinson MAC, Ormandy K, Bradley CR, Hines J. Comparison of the efficacy and drying times of liquid, gel and foam formats of alcohol-based hand rubs. J Hosp Infect 2018;98:359–64. https://doi.org/10.1016/j.jhin.2017.09.024. 7. Larson EL, Cohen B, Baxter KA. Analysis of alcohol-based hand sanitizer delivery systems: efficacy of foam, gel, and wipes against influenza A (H1N1) virus on hands. Am J Infect Control 2012;40:806–9. https://doi.org/10.1016/j.ajic.2011.10.016. 8. Guilhermetti M, Marques Wiirzler LA, Castanheira Facio B, da Silva Furlan M, Campo Meschial W, Bronharo Tognim MC, et al. Antimicrobial efficacy of alcohol-based hand gels. J Hosp Infect 2010;74:219–24. https://doi.org/10.1016/j.jhin.2009.09.019. 9. Kampf G, Marschall S, Eggerstedt S, Ostermeyer C. Efficacy of ethanol-based hand foams using clinically relevant amounts: a cross-over controlled study among healthy volunteers. BMC Infect Dis 2010;10:78. https://doi.org/10.1186/1471-2334-1078. 10. Kampf G, Hollingsworth A. Comprehensive bactericidal activity of an ethanolbased hand gel in 15 seconds. Ann Clin Microbiol Antimicrob 2008;7:2. https://doi.org/10.1186/1476-0711-7-2. 11. European Committee for Standardization. European Norm 1500: chemical disinfectants and antiseptics. Hygienic handrub. Test method and requirements (phase 2/step 2). Brussels: CEN - Comité Européen de Normalisation (2013).
12. Ory J, Zingg W, De Kraker MEA, Soule H, Pittet D. Wiping Is Inferior to Rubbing: A Note of Caution for Hand Hygiene With Alcohol-Based Solutions. Infect Control Hosp Epidemiol 2018;39:332–5. https://doi.org/10.1017/ice.2017.307.
13. Bellissimo-Rodrigues F, Soule H, Gayet-Ageron A, Martin Y, Pittet D. Should AlcoholBased Handrub Use Be Customized to Healthcare Workers' Hand Size? Infect Control Hosp Epidemiol 2016;37:219–21. https://doi.org/10.1017/ice.2015.271. 14. Hsu Y-W, Yu C-Y. Hand surface area estimation formula using 3D anthropometry. J Occup Environ Hyg 2010;7:633–9. https://doi.org/10.1080/15459624.2010.514259. 15. Song X, Stockwell DC, Floyd T, Short BL, Singh N. Improving hand hygiene compliance in health care workers: Strategies and impact on patient outcomes. Am J Infect Control 2013;41:e101-5. https://doi.org/10.1016/j.ajic.2013.01.031. 16. Woodard JA, Leekha S, Jackson SS, Thom KA. Beyond entry and exit: Hand hygiene at the bedside. Am J Infect Control 2019;47:487–91. https://doi.org/10.1016/j.ajic.2018.10.026. 17. Costers M, Viseur N, Catry B, Simon A. Four multifaceted countrywide campaigns to promote hand hygiene in Belgian hospitals between 2005 and 2011: impact on compliance to hand hygiene. Euro Surveill 2012;17. https://doi.org/10.2807/ese.17.18.20161-en. 18. Staines A, Vanderavero P, Duvillard B, Deriaz P, Erard P, Kundig F, et al. Sustained improvement in hand hygiene compliance using a multi-modal improvement programme at a Swiss multi-site regional hospital. J Hosp Infect 2018;100:176–82. https://doi.org/10.1016/j.jhin.2018.04.010. 19. Eiamsitrakoon T, Apisarnthanarak A, Nuallaong W, Khawcharoenporn T, Mundy LM. Hand Hygiene Behavior: Translating Behavioral Research into Infection Control Practice. Infect Control Hosp Epidemiol 2013;34:1137–45. https://doi.org/10.1086/673446. 20. Battistella G, Berto G, Bazzo S. Developing professional habits of hand hygiene in intensive care settings: An action-research intervention. Intensive Crit Care Nurs 2017;38:53–9. https://doi.org/10.1016/j.iccn.2016.08.003. 21. Pittet D, Mourouga P, Perneger TV. Compliance with handwashing in a teaching hospital. Ann Intern Med 1999;130:126–30. https://doi.org/10.7326/0003-4819-130-2199901190-00006. 22. Pires D, Soule H, Bellissimo-Rodrigues F, De Kraker MEA, Pittet D. Antibacterial efficacy of handrubbing for 15 versus 30 seconds: EN 1500-based randomized experimental study with different loads of Staphylococcus aureus and Escherichia coli. Clin Microbiol Infect 2019;25:851–6. https://doi.org/10.1016/j.cmi.2018.10.012.
S0195-6701(20)30056-6
DOI:
https://doi.org/10.1016/j.jhin.2020.02.008
Reference:
YJHIN 5913
To appear in:
Journal of Hospital Infection
Received Date: 1 December 2019 Accepted Date: 10 February 2020
Please cite this article as: Xian Tan JB, de Kraker MEA, Pires D, Soule H, Pittet D, Hand Rubbing with Sprayed Alcohol-Based Hand Rub: An Alternative Method for Effective Hand Hygiene, Journal of Hospital Infection, https://doi.org/10.1016/j.jhin.2020.02.008. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
Hand Rubbing with Sprayed Alcohol-Based Hand Rub: An Alternative Method for Effective Hand Hygiene
Jamie Bee Xian Tan, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland; Department of Microbiology, Singapore General Hospital, Singapore; Duke-NUS Medical School, Singapore Marlieke E.A. de Kraker, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Daniela Pires, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Hervé Soule, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Didier Pittet, Infection Control Programme, WHO Collaborating Centre on Patient Safety, Infection Control & Improving Practices, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Running title: Handrubbing with sprayed ABHR effective
Word count: 2438 Figures: 2
Corresponding author: Marlieke de Kraker Hôpitaux Universitaires de Genève Service prévention et contrôle de l'infection Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland Phone: +41 22 372 3369 | Fax: +41 22 372 3987 Email: [email protected]
Abstract (250 words)
Background: Hand hygiene is crucial in infection prevention and control. It is unclear whether sprayed alcohol-based handrub (ABHR) is non-inferior to the WHO recommended method of handrubbing with poured ABHR.
Aim: We tested whether sprayed ABHR can be an alternative (non-inferior) method for effective hand hygiene with/without handrubbing.
Methods: We conducted a laboratory experiment with ABHR (isopropanol 60% v/v) according to the European Norm 1500. Hand hygiene was performed by (1) handrubbing with ABHR poured onto a hand palm, (2) handrubbing with sprayed ABHR, and (3) applying sprayed ABHR on hands without rubbing. Hands were contaminated with Escherichia coli ATCC 10536, followed by hand hygiene and microbiological sampling. A generalized linear mixed model with a random intercept per subject was used to analyse the reduction in bacterial counts post-hand hygiene.
Findings: A total of 19 healthcare workers participated in the study. Handrubbing with sprayed ABHR was non-inferior (margin log10 0.6 colony forming units [CFU]/mL) to the WHO method of handrubbing with poured ABHR; bacterial count reduction was log10 3.66 CFU/mL (95% CI 1.68-5.64) and log10 3.46 CFU/mL (95% CI 1.27-5.65), respectively. Conversely, non-inferiority was not found for hand hygiene using sprayed ABHR without rubbing (bacterial count reduction: log10 2.76 CFU/mL, 95% CI 1.65-3.87).
Conclusion: Handrubbing with sprayed ABHR was non-inferior to rubbing with ABHR poured onto a hand palm to reduce bacterial counts on hands under experimental conditions. Rubbing with sprayed ABHR may be an acceptable alternative hand hygiene method pending assessment in other settings and for other pathogens.
Keywords: Hand hygiene, Alcohol-based handrub, Spray application, Handrubbing, EN 1500, guidelines, WHO ‘how to handrub’
Introduction Healthcare-associated infections (HAI) are a major patient safety problem. Disease-causing pathogens can be transmitted to patients through the hands of healthcare workers (HCW); therefore hand hygiene is one of the most important measures in preventing HAI [1, 2]. Hand hygiene compliance among healthcare workers however has been insufficient. This has led the World Health Organization (WHO) to develop a multimodal hand hygiene improvement strategy aimed at increasing hand hygiene compliance [2-5]. The WHO guidelines recommend that hand hygiene be performed using a liquid alcohol-based handrub (ABHR) that is first poured onto a hand palm followed by a six step handrubbing technique for 20-30 seconds [2].
ABHR is also available in other formats, like gels, foams, aerosols (provided by spray dispensers), or wipes, and their antimicrobial efficacy has already been extensively studied [6-12]. However, the antimicrobial efficacy of sprayed ABHR has not been assessed, even though spray dispensers have a number of advantages, including direct dispensing of ABHR onto hand surfaces, avoiding spillage, and delivery of precise, customized volumes [13]. If ABHR can be evenly distributed onto the hands, it is also unclear if handrubbing would be required for an effective hand hygiene action. The antimicrobial action of ABHR can be attributed to the protein denaturation effect of alcohol [2], and it remains unknown whether hand rubbing is required solely to help spread the liquid ABHR onto all the hand surfaces or if hand hygiene efficacy is affected if the handrubbing action is omitted entirely. As the utilization of sprays to deliver liquid ABHR has become more common in healthcare facilities, it is important to clarify the role these sprays can play in effective hand hygiene. In this study, we determined whether the antimicrobial efficacy of hand hygiene using a sprayed ABHR, with or without handrubbing, is non-inferior to rubbing with ABHR poured onto a hand palm, as currently recommended by the WHO guidelines.
Methods
Study setting, participants and eligibility criteria We conducted a laboratory-based experimental study at the microbiology laboratory of the Infection Control Program (IPC), University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland. The study was part of the IPC quality assurance program approved by the local ethics committee and all healthcare workers (HCW) agreed to participate. Nineteen locally recruited HCW who had extensive training and experience in hand hygiene according to the WHO guidelines were enrolled in the study. The number of recruited participants was based on the European Norm 1500’s recommendation of including 18 to 22 subjects [11]. All of the participants had short fingernails. Exclusion criteria included the presence of artificial nails, jewellery and skin conditions affecting the hands.
Study design All of the experiments were based on the European Norm 1500 [11]. Each participant performed three experiments using the same ABHR (isopropanol 60% v/v without any additional emollients or other ingredients). The experiments consisted of performing in, a randomized order: (1) hand hygiene using 3 mL ABHR poured onto a hand palm with 30 seconds of rubbing, (2) hand hygiene using 3 mL sprayed ABHR with 30 seconds of rubbing (Figure 1), and (3) hand hygiene using 3 mL sprayed ABHR without rubbing.
Rubbing consisted of the six step technique as promoted by WHO [2]. For experiments (1) and (2), participants were instructed to repeat each step of the WHO “How to Handrub” technique five times to ensure uniformity of the hand rubbing process; whereas for experiment (3), participants were instructed to maintain their hands in an upright position without moving for 30 seconds after applying the ABHR.
Spraying was applied by using the SARAYA GUD-1000 delivery system, SARAYA.Co.Ltd, Japan. The healthcare workers were instructed to move their fingertips under the nozzle, after which the spray instantaneously released 3 mL of ABHR (Figure 1). Before the start of the experiment, each participant practised this gesture once with a similar spray containing water.
At the start of each experiment, participants were required to first wash their hands using liquid soap and water. After contaminating their hands artificially with Escherichia coli ATCC
10536 suspension, microbiological sampling was performed both before and after the experiment in order to determine the bacterial count reduction.
Artificial contamination and microbiological sampling Artificial contamination of the hands was performed by immersing both hands up to the midcarpals in a bacterial suspension containing 108 colony forming units (CFU)/mL of E. coli ATCC 10536 for 5 seconds and then holding them up to air dry for 3 minutes. At baseline and immediately after each intervention, bacteria were recovered from both hands of the healthcare workers using the fingertips method [11]. This procedure consisted of the healthcare worker rubbing all 5 fingertips of each hand in a sterile petri dish containing 10 mL of tryptone soy broth for 1 minute.
Dilution and plating of microbiological samples Microbiological samples were serially diluted and 4 different dilutions (10-1 to 10-4) were plated to accurately estimate bacterial counts. After achieving the required dilution, a 1 mL aliquot was spread over the surface of a tryptic soy agar plate before it was incubated at 36±1oC under aerobic conditions for 48 hours. The resultant E. coli colonies were quantified by visual inspection, adjusted for the corresponding dilution factor and converted to log10.
Study outcomes and statistical analysis The antimicrobial efficacy of experiment (2) and (3) was compared with experiment (1), and was determined by comparing the difference between the baseline and post-intervention bacterial counts that were recovered from the healthcare workers’ hands. Results were analysed using a generalized linear mixed model (GLMM) with random intercepts for each healthcare worker, given the repeated measures design. We also evaluated whether the reduction in bacterial counts was influenced by hand size by including this as a covariate in the model and testing the interaction between hand size and experiment. Hand surface areas were calculated and categorized as small (≤ 375 cm2), medium (376-424 cm2) and large (≥ 425 cm2) [13, 14]. Statistical analyses were performed using R studio software, version 3.0.2 (R Foundation for Statistical Computing, Vienna, Austria).
We hypothesized that hand rubbing with sprayed ABHR would not be inferior to hand rubbing with poured ABHR. The definition of non-inferiority in EN 1500 was met when the difference in bacterial count reduction was less than log10 0.6 CFU/mL between the experiments.
Results Out of the 19 healthcare workers who participated in the study, 7 (36.8%) were doctors, 5 (26.3%) were nurses, and 7 (36.8%) had other healthcare professions. The majority was female (13/19, 68.4%), six (31.6%) healthcare workers had small hands, 9 (47.4%) had medium hands, and 4 (21.1%) had large hands.
The average baseline contamination of the healthcare worker hands with E. coli ATCC 10536 was log10 6.91 CFU/mL (95% confidence interval [CI], 5.90-7.91) before the hand hygiene action. Hand hygiene using 3 mL ABHR poured onto a hand palm followed by rubbing reduced bacterial load by a mean of log10 3.46 CFU/mL (95% CI, 1.27-5.65). Hand hygiene using 3 mL sprayed ABHR with rubbing reduced bacterial load by a mean of log10 3.66 CFU/mL (95% CI, 1.68-5.64). Hand hygiene using 3 mL sprayed ABHR without rubbing reduced bacterial load by a mean of log10 2.76 CFU/mL (95% CI, 1.65-3.87) (Figure 2).
The GLMM showed that, compared to hand hygiene using poured ABHR with rubbing sprayed ABHR with rubbing non-significantly increased the reduction in bacterial load by log10 0.20 CFU/mL (95% CI, -0.23 to 0.62). For hand hygiene using sprayed ABHR without rubbing, the reduction in bacterial load was significantly decreased compared to hand hygiene using liquid ABHR with rubbing by log10 -0.70 CFU/mL (95% CI, -1.13 to -0.28) (Figure 2). Adjustment for hand size did not change the effect estimates, and no significant interaction with experiment was found, so hand size was not included in the final model.
Using the - log10 0.6 CFU/mL non-inferiority margin that was specified by the European Norm 1500, hand hygiene using sprayed ABHR with rubbing was non-inferior to hand hygiene using poured ABHR with rubbing. Conversely, non-inferiority could not be confirmed for hand hygiene using sprayed ABHR without rubbing.
Discussion To the best of our knowledge, this is the first study based on the European Norm 1500 that assessed the antimicrobial efficacy of hand hygiene using aerosolized ABHR. Our study has shown that the antimicrobial efficacy of hand rubbing with sprayed ABHR is non-inferior to and not significantly different from the current WHO recommended method of performing hand hygiene using the same ABHR poured onto a hand palm with rubbing. The utilisation of sprayed ABHR without rubbing was significantly less effective than the WHO method, clearly indicating the importance of hand rubbing for adequate hand hygiene.
Despite the increasing awareness that hand hygiene is a crucial part of infection control and prevention in the hospital setting, hand hygiene among healthcare workers is still far from intuitive resulting in insufficient baseline compliance rates. Hand hygiene compliance rates, based on direct observation, reported in recently published literature, range from 23% in a Thai tertiary care hospital [15], to 35% in a tertiary care hospital in the United States [16], to 50% in a set of Belgian acute care hospitals [17], and 61.4% hand hygiene compliance in a Swiss teaching hospital [18]. In this study, we have shown that hand rubbing with aerosolized ABHR could be used as an alternative to the WHO recommended procedure of rubbing with liquid ABHR. Using a spray method to dispense the ABHR could improve hand hygiene efficacy as well as compliance. Spraying can uniformly deliver ABHR to a large hand surface area within a short period of time with minimal spillage, improving efficiency. Combined with the small droplets dispensed by the spray, time required to dry the hands and thus the hand hygiene action could be shortened as well. As it has been shown that time pressure is a major barrier to compliance, this could positively influence hand-hygiene frequency [19-21].
Effective sprays that do not require hand rubbing could further decrease the required time for hand hygiene, and as such increase hand hygiene compliance [15, 19-20]. Unfortunately, in this study, non-inferiority could not be confirmed when hand rubbing after ABHR spraying was omitted in one of our experiment arms. Development of novel spray designs, or improvements in the ABHR formula used in sprays could perhaps overcome this hurdle, and further development in this area is encouraged. Although health and safety issues should be considered, as aerosols may play a role in respiratory tract irritations, which could reduce hand hygiene compliance.
Our study has a few limitations. Firstly, our study was conducted in a laboratory setting with healthcare workers who had extensive training and experience in hand hygiene, hence the findings may not be directly generalizable to all healthcare workers, or to the clinical setting. Our study only looked at the antimicrobial efficacy of the experimental interventions against an E. coli control strain using isopropanol 60% v/v, and one type of spray. Further testing is required to see if our findings could be confirmed for commercially available ABHR formulations, or other types of sprays with different spray patterns or droplet size. The impact of other bacteria types, which are commonly encountered in the healthcare setting, should be studied as well, although in a previous study, comparing 15 to 30 seconds of hand rubbing with ABHR, pathogen type did not influence the results [22]. Finally, it remains undefined what minimum bacterial count reduction of contaminated hands is required to prevent transmission of infections in a real world setting, as such it is difficult to extrapolate experimental findings to clinical practice.
The strength of the present study is that it compared the efficacy of sprayed ABHR with and without rubbing to the established WHO hand hygiene methodology according to the standardized EN 1500 norm. The experiments were performed in a well-established infection and prevention laboratory with a large experience in hand hygiene experiments [12, 13, 21, 22], and the order of the experiments was randomized. In the statistical methods we corrected for repeated measurements among the 19 HCWs, and checked for the influence of hand size. In conclusion, this study has reliably shown that hand rubbing with sprayed ABHR is noninferior to the current WHO recommended method of hand rubbing with the same ABHR poured onto a hand palm. ABHR delivered as a spray could be an alternative method to ensure appropriate hand disinfection and patient safety as long as the correct hand rubbing steps are included. Future research should establish the efficacy of sprayed ABHR in other settings.
Transparency declaration Didier Pittet has received funding from the European Commission and National Science Foundation for several research and clinical studies, and works with the WHO in the context of the WHO initiative Private Organizations for Patient Safety Hand Hygiene. The aim of this WHO initiative is to harness industry strengths to align and improve implementation of WHO recommendations for hand hygiene in health care in different parts of the world, including in least developed countries. In this instance companies/industry with a focus on hand hygiene and infection control related advancement have the specific aim of improving access to affordable hand-hygiene products as well as through education and research. All other listed authors declare no financial support, grants, financial interests or consultancy that could lead to conflicts of interest.
Acknowledgements We acknowledge all the HCWs who participated as volunteers in the present study, and Saraya.Co.Ltd for providing the spray dispenser. Part of the data was presented at the International Conference of Infection Control (ICPIC), held in Geneva, Switzerland, on 11 September 2019 (ICPIC19-ABS-P437).
Contribution of authors JT, MdK, DPires, HS, and DP conceived the study idea. JT and HS wrote the draft of the study protocol, which was reviewed by all authors. The experiments were planned and run by JT. MdK performed the statistical analysis. JT wrote the first draft of the manuscript, which was reviewed and approved by all authors.
Conflict of interest None.
Funding This study was supported by the Infection Control Programme & WHO Collaborating Centre on Patient Safety (SPCI/WCC), University of Geneva Hospitals and Faculty of Medicine,
Geneva, Switzerland. Hand-hygiene research activities at the SPCI/WCC are supported by the National Science Foundation (32003B_163262). Daniela Pires is supported by the National Science Foundation (32003B_163262) for hand-hygiene research activities and by Fundação para a Ciência e a Tecnologia (SFRH/SINT/95317/2013). Marlieke de Kraker has received support from the Innovative Medicines Initiative Joint Undertaking (IMI) under grant agreement nos. 115523, 115620 and 115737 (Combatting Bacterial Resistance in Europe projects), resources of which are composed of financial contribution from the European Union's 7th Framework Programme (FP7/2007±2013) and the European Federation of Pharmaceutical Industries and Associations (EFPIA) companies' in-kind contribution.
Figures Figure 1. Automatic spray dispenser used for the study. Fingertips were placed under the nozzle. A pre-specified amount of ABHR was dispensed upon activation of the sensor.
Figure 2. E. coli bacterial count reduction on the hands of healthcare workers after using poured versus sprayed ABHR (3 mL) with or without rubbing.
References 1. Boyce JM, Pittet D. 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. Morb Mortal Wkly Report Recomm Reports 2002;51:1–45, quiz CE1-4. 2. World Health Organization. Guidelines on Hand Hygiene in Health Care. First Global Patient Safety Challenge: Clean Care is Safer Care. Geneva, WHO (2009). https://apps.who.int/iris/bitstream/handle/10665/44102/9789241597906_eng.pdf;jsessionid =124BBEB5607F910DD2033CFCD6F18490?sequence=1. Accessed 1 February 2019. 3. Tschudin-Sutter S, Sepulcri D, Dangel M, Schuhmacher H, Widmer AF. Compliance with the World Health Organization hand hygiene technique: a prospective observational study. Infect Control Hosp Epidemiol 2015;36:482–3. https://doi.org/10.1017/ice.2014.82 4. Musu M, Lai A, Mereu NM, Galletta M, Campagna M, Tidore M, et al. Assessing hand hygiene compliance among healthcare workers in six Intensive Care Units. J Prev Med Hyg 2017;58:E231–7. 5. World Health Organization. Guide to Implementation. A Guide to the Implementation of the WHO Multimodal Hand Hygiene Improvement Strategy. Geneva, WHO (2009). https://www.who.int/gpsc/5may/Guide_to_Implementation.pdf. Accessed 1 February 2019. 6. Wilkinson MAC, Ormandy K, Bradley CR, Hines J. Comparison of the efficacy and drying times of liquid, gel and foam formats of alcohol-based hand rubs. J Hosp Infect 2018;98:359–64. https://doi.org/10.1016/j.jhin.2017.09.024. 7. Larson EL, Cohen B, Baxter KA. Analysis of alcohol-based hand sanitizer delivery systems: efficacy of foam, gel, and wipes against influenza A (H1N1) virus on hands. Am J Infect Control 2012;40:806–9. https://doi.org/10.1016/j.ajic.2011.10.016. 8. Guilhermetti M, Marques Wiirzler LA, Castanheira Facio B, da Silva Furlan M, Campo Meschial W, Bronharo Tognim MC, et al. Antimicrobial efficacy of alcohol-based hand gels. J Hosp Infect 2010;74:219–24. https://doi.org/10.1016/j.jhin.2009.09.019. 9. Kampf G, Marschall S, Eggerstedt S, Ostermeyer C. Efficacy of ethanol-based hand foams using clinically relevant amounts: a cross-over controlled study among healthy volunteers. BMC Infect Dis 2010;10:78. https://doi.org/10.1186/1471-2334-1078. 10. Kampf G, Hollingsworth A. Comprehensive bactericidal activity of an ethanolbased hand gel in 15 seconds. Ann Clin Microbiol Antimicrob 2008;7:2. https://doi.org/10.1186/1476-0711-7-2. 11. European Committee for Standardization. European Norm 1500: chemical disinfectants and antiseptics. Hygienic handrub. Test method and requirements (phase 2/step 2). Brussels: CEN - Comité Européen de Normalisation (2013).
12. Ory J, Zingg W, De Kraker MEA, Soule H, Pittet D. Wiping Is Inferior to Rubbing: A Note of Caution for Hand Hygiene With Alcohol-Based Solutions. Infect Control Hosp Epidemiol 2018;39:332–5. https://doi.org/10.1017/ice.2017.307.
13. Bellissimo-Rodrigues F, Soule H, Gayet-Ageron A, Martin Y, Pittet D. Should AlcoholBased Handrub Use Be Customized to Healthcare Workers' Hand Size? Infect Control Hosp Epidemiol 2016;37:219–21. https://doi.org/10.1017/ice.2015.271. 14. Hsu Y-W, Yu C-Y. Hand surface area estimation formula using 3D anthropometry. J Occup Environ Hyg 2010;7:633–9. https://doi.org/10.1080/15459624.2010.514259. 15. Song X, Stockwell DC, Floyd T, Short BL, Singh N. Improving hand hygiene compliance in health care workers: Strategies and impact on patient outcomes. Am J Infect Control 2013;41:e101-5. https://doi.org/10.1016/j.ajic.2013.01.031. 16. Woodard JA, Leekha S, Jackson SS, Thom KA. Beyond entry and exit: Hand hygiene at the bedside. Am J Infect Control 2019;47:487–91. https://doi.org/10.1016/j.ajic.2018.10.026. 17. Costers M, Viseur N, Catry B, Simon A. Four multifaceted countrywide campaigns to promote hand hygiene in Belgian hospitals between 2005 and 2011: impact on compliance to hand hygiene. Euro Surveill 2012;17. https://doi.org/10.2807/ese.17.18.20161-en. 18. Staines A, Vanderavero P, Duvillard B, Deriaz P, Erard P, Kundig F, et al. Sustained improvement in hand hygiene compliance using a multi-modal improvement programme at a Swiss multi-site regional hospital. J Hosp Infect 2018;100:176–82. https://doi.org/10.1016/j.jhin.2018.04.010. 19. Eiamsitrakoon T, Apisarnthanarak A, Nuallaong W, Khawcharoenporn T, Mundy LM. Hand Hygiene Behavior: Translating Behavioral Research into Infection Control Practice. Infect Control Hosp Epidemiol 2013;34:1137–45. https://doi.org/10.1086/673446. 20. Battistella G, Berto G, Bazzo S. Developing professional habits of hand hygiene in intensive care settings: An action-research intervention. Intensive Crit Care Nurs 2017;38:53–9. https://doi.org/10.1016/j.iccn.2016.08.003. 21. Pittet D, Mourouga P, Perneger TV. Compliance with handwashing in a teaching hospital. Ann Intern Med 1999;130:126–30. https://doi.org/10.7326/0003-4819-130-2199901190-00006. 22. Pires D, Soule H, Bellissimo-Rodrigues F, De Kraker MEA, Pittet D. Antibacterial efficacy of handrubbing for 15 versus 30 seconds: EN 1500-based randomized experimental study with different loads of Staphylococcus aureus and Escherichia coli. Clin Microbiol Infect 2019;25:851–6. https://doi.org/10.1016/j.cmi.2018.10.012.