Abstract
This prospective clinical study evaluates the effectiveness of an alcohol-based hand rub (Avagard™) for pre-surgical hand antisepsis in an equine hospital and compares it with traditional scrubbing technique using 4% chlorhexidine gluconate sponges and water. Prior to elective surgery, 3 board-certified surgeons were randomly assigned to hand antisepsis with either technique. Culture samples of each hand were taken at 4 times: before and after neutral soap hand wash, after scrub or rubbing technique, and after surgery. There was no significant difference in mean bacterial colony forming units between scrub and rub techniques over the 3 time periods (P = 0.6), controlling for initial counts. One horse from the scrub group had a skin incision infection following stifle arthroscopy; this was resolved with medical treatment. The alcohol-based hand rub is equivalent in efficacy for pre-surgical hand antisepsis to traditional water-based scrubs in an equine hospital setting.
Résumé
Comparaison de l’alcool à friction et d’une technique de brossage au gluconate de chlorhexidine à base d’eau pour l’antisepsie des mains avant les chirurgies non urgentes chez les chevaux. Cette étude clinique prospective évalue l’efficacité d’un alcool à friction (AvagardMD) pour l’antisepsie des mains préalable à une chirurgie dans un hôpital équin et elle la compare à la technique de brossage traditionnelle au moyen d’éponges de gluconate de chlorhexidine 4 % et d’eau. Avant une chirurgie non urgente, trois chirurgiens agréés ont été assignés au hasard à l’antisepsie des mains avec l’une ou l’autre technique. Des échantillons de chaque main ont été prélevés quatre fois pour culture : avant et après le lavage des mains avec un savon neutre, après la technique de brossage et de friction et après la chirurgie. Il n’y avait aucune différence significative dans les moyennes des dénombrements bactériens d’unités formatrices de colonies entre les techniques de brossage et de friction pendant les trois périodes de temps (P = 0,6), en tenant compte des témoins pour les dénombrements initiaux. Un cheval du groupe de brossage a développé une infection au site de l’incision après une arthroscopie du grasset qui a été résolue par traitement médical. La friction des mains à l’alcool est équivalente, en matière d’efficacité pour l’antisepsie des mains avant la chirurgie, au brossage traditionnel à l’eau dans un milieu hospitalier équin.
(Traduit par Isabelle Vallières)
Introduction
Scrubbing methods from human surgery have been extrapolated to veterinary medicine (1) and there are few studies assessing the effectiveness of hand antisepsis in the veterinary field (2–4). Transient flora acquired by contact with humans, animals, or contaminated environment surfaces colonizes the superficial layers of intact skin, and is one of the most common causes for inducing surgical site infections (5). Surgical site infections (SSI) may come from flora on the skin of the patient or by contamination during the surgery from the surgeon or environment. Glove perforations are present in high numbers in certain types of surgery, hence adequate hand antisepsis prior to surgery is critical (6,7). Two main types of water-based medicated soaps [povidine-iodine (P-I) and 4% chlorohexidine gluconate (CHG)] and alcohol-based rubs, with or without additional active ingredients, are used for hand antisepsis prior to surgery (8). Recently alcohol-based hand rubs have been evaluated in several sectors of human surgery and were found to be as or more effective in reducing bacterial counts on surgeons hands and limiting SSIs than water-based scrubs due to the fast and highly bactericidal effect of the alcohol component (9–14).
Waterless, alcohol-based hand rubs require less application time, are less irritating to the skin, and save large quantities of water (15,16). Estimates for water usage are about 20 L for each surgeon unless motion-activated water taps are used and then estimates are 10 to 15 L per surgeon for each procedure (15). Under frequent-use conditions the general health of the skin is significantly improved with alcohol-based rubs compared to traditional scrubbing techniques (17) because of the lack of abrasive scrubbing, the lack of soap, and the presence of emollients (18). The emollients help to prevent the hands from becoming as dry as they would from soap and water washings (19). Prolonged or repeated washing leads to damage of the stratum corneum, which can lead to increased bacterial colonization on the hands of surgeons (4).
The only published veterinary study comparing alcohol-based hand rubs to traditional scrubs in a clinical setting showed that an alcohol-based rub (Sterillium; Bode-Chemie, Hamburg, Germany) was as effective as a CHG 4% scrub and more effective than a povidine scrub in the immediate effect and more effective than both in the 3 h residual effect at reducing bacterial counts on hands (3). Despite all the described advantages of alcohol-based rubs, a recent survey of veterinary surgeons showed that about 80% of them are still using water-based hand scrubbing with CHG or P-I soaps for hand antisepsis (4). These hand scrubbings reduce close to 80% of the bacterial colony forming units (CFU) on dirty hands of veterinarians until 120 min postscrub (2) but frequent hand washing during the day damages the stratum corneum of the skin and changes the skin flora, resulting in more frequent colonization by staphylococci and Gram-negative bacilli (16).
In contrast to human surgeons, veterinary surgeons often examine their patients directly before surgery and this may lead to a very different flora or level of contamination on their hands (1–4). There is limited evidence that supports the alcohol-based rub as a safe method of hand antisepsis in these conditions. The previously mentioned study, which included both large and small animal surgeons, is the only study in clinical veterinary medicine showing alcohol hand rub efficacy (3). In the human field, studies have shown the effectiveness of the alcohol-based hand rub with 1% chlorhexidine, but there are no data showing similar results in an equine hospital (8,13,14).
The objective of this study was to compare the efficacy for hand antisepsis of the traditional 4% chlorhexidine gluconate water based scrub (BD E-Z scrub™ 107 surgical scrub brush/sponge with 4% chlorhexidine gluconate; Becton Dickinson & Co., Franklin Lakes, New Jersey, USA) with alcohol-based hand rub with 1% chlorhexidine (Avagard™ chlorhexidine gluconate 1% solution and ethyl alcohol 61% w/w; 3M™ Healthcare, St. Paul, Minnesota, USA) during standard sterile equine elective surgeries performed by board-certified surgeons. The hypothesis was that the 2 methods would be equally effective in reducing bacterial counts on the surgeons’ hands.
Materials and methods
Three board-certified equine surgeons participated in the study. Both hands of each surgeon were sampled before and after application of either traditional 4% chlorhexidine gluconate sponges and water scrub or the alcohol-based hand rub prior to an elective equine surgery. The surgeries were distributed throughout the day according to the demands of that day. The medical records and communication logs of the horses undergoing surgery in the study were examined for short- or long-term signs of infection in the post-operative period. This was defined as any fever, incisional drainage, or lameness after the elective procedure. Prior to surgery, the surgeon was randomly assigned to the scrub or to the rub technique of hand antisepsis as described below. The surgical time, number of holes in the gloves after surgery, and surgical site infections were also recorded. The 3 surgeons involved in the study met at the beginning of the study and ensured that each of the 3 performed the 1-minute neutral soap wash, the 5-minute scrub and the alcohol rub technique in a standardized manner as described in the following paragraphs.
Scrub technique
Hands and forearms were briefly washed of gross debris using a regular neutral liquid soap for 1 min and dried with paper towels. Sub-ungual areas were cleaned with a nail cleaner (disposable and delivered with the brushes). A 5-minute scrub was performed using the CHG 4% incorporated into a disposable sponge/brush. The CHG soap was applied to the hands and forearms with the sponge side of the brush and then hands and forearms were scrubbed for 5 min and dried with sterile disposable towels.
Rub technique
The rubbing technique followed the recommendations for 90-second application as described by the manufacturer (16). Hands were washed briefly with a neutral soap for 1 min to remove gross debris and sub-ungual areas were cleaned and dried as described. One dose (2 mL) of alcohol-based hand rub was dispensed in the palm of the left hand using the foot pump of a wall-mounted unit. The fingertips of the right hand were dipped in the hand rub to decontaminate under the nails (5 s). The hand rub was then smeared on the right forearm up to the elbow and the entire skin area was covered by using circular movements around the forearm (20 s). A second 2 mL was dispensed in the palm of the right hand and the fingertips of the left hand were dipped in the hand rub to decontaminate under the nails (5 s). The procedure for the left forearm was repeated as described (20 s). A final 2 mL of alcohol-based hand rub was dispensed in the palm of the left hand and both hands were rubbed together up to the wrists (40 s). To cover the entire surface of the hands up to the wrist with alcohol-based hand rub, palm was rubbed against palm with a rotating movement; the back of the left hand, including the wrist, moving the right palm back and forth, and vice versa; then palm against palm back and forth with fingers interlinked and the back of the fingers by holding them in the palm of the other hand with a sideways back-and-forth movement. The thumb of the left hand was rubbed by rotating it in the clasped palm of the right hand and vice versa.
Sampling method
Samples were taken with sterile phosphate-buffered saline moistened cotton swabs at 4 time points by swabbing around the thumb and first 2 fingers of each hand during the first and third swabs and around the 3 last fingers during the second and fourth swabs (20). The first sample was taken when the surgeon arrived in the scrubbing room before any hand washing (A). The second sample was taken after briefly washing the hands with neutral soap (B), and the third one directly after the scrubbing or rubbing procedure and prior to the gloving (C). At the end of the surgery the gloves of the surgeon were removed, taking care to preserve the sterility of the hands and the fourth swab was taken (D). All samples were included unless an observed error in handling or processing resulting in potential contamination was noted.
Bacterial evaluation
The cotton swabs were immediately immersed in 0.5 mL transport medium of Trypticase Soy Broth with a mixture of CHG neutralizing agents: 3% Tween 80, 0.3% lecithin, 0.1% histidine, 0.5% sodium thiosulphate, 3% saponin, 1% ether sulphate (18), and refrigerated until they were processed. The bacteriologist was blinded to the method of hand antisepsis. Each sample was diluted 10−1 in the same medium before plating onto blood agar. One plate was inoculated with 300 μL of undiluted sample and a second plate was inoculated with 300 μL of diluted sample; both plates were incubated for 48 h at 35°C. The number of colonies on each plate was recorded.
Glove puncture test
After surgery the gloves were tested for perforations by filling them with 1 L of colored water and sealing the cuff of the glove. The exterior surface of the glove was blotted dry, gently pressured, and checked for leaks. Leaks were recorded according to whether they occurred on the hand or a finger (palmar and/or dorsal surface or in the interdigital crevice).
Statistical methods
A sample number of 37 was calculated to achieve a power of 80% at the alpha level of 5% by using a repeated measures design and assuming that the standard deviation is 1.8 and the mean of the CFU post surgery is 1 for the alcohol based rub group and 2 for the CHG scrub group (3,4).
Pre- and post-treatment values were transformed into decimal logarithms (log10) prior to statistical analysis. A linear mixed model was used and each surgeon was considered as a random factor, each treatment as a between-subject factor and each time as a within-subject factor. The count values at time A were included as a cofactor to control for potential differences in initial count values. The statistical analysis was carried out using SAS v 9.2 (SAS, Cary, North Carolina, USA) with statistical significance set at P < 0.05. The number of SSIs was recorded but not analyzed statistically due to the expected low incidence.
Results
A total of 49 surgical procedures were used resulting in 49 samples at each time point. The CFUs at times B, C, and D were positively associated with initial count values (P = 0.02). There was no significant difference in the mean CFUs between the scrub and rub techniques over the 3 time periods (P = 0.6), controlling for initial count values. The patterns of decrease within times were not statistically different in all treatments (P = 0.98).
The mean CFUs in A samples was 2.7 × 0.87 log10 for the scrub group and 2.7 × 0.83 log10 for the rub group showing that the pre-scrub level of contamination was consistent between groups (Table 1). Counts decreased significantly within times (P < 0.0001). Hand washing with neutral soap decreased the CFU count by 7.5 times (1.6 × 0.7 log10). The means between the 2 treatments at each time period were compared also, controlling for initial count values (A). There was no statistically significant difference between the 2 treatment group means at times B [(P = 0.71), C (P = 0.64) or D (P = 0.84); Table 1]. Two samples were removed from the analysis of the D time point samples due to suspected contamination during handling, resulting in 47 samples being analyzed at this time.
Table 1.
Mean ± standard deviations of log10 CFU counts taken at the various times in the study
| Timea | Scrub group (log10 values) | Alcohol-based hand rub with 1% chlorhexidine group (log10 values) | P-values (between groups) |
|---|---|---|---|
| A | 2.7 ± 0.87 | 2.7 ± 0.83 | |
| B | 1.56 ± 0.56 | 1.6 ± 0.83 | 0.71 |
| C | 0.08 ± 0.29 | 0.16 ± 0.33 | 0.64 |
| D | 0.28 ± 0.49 | 0.32 ± 0.49 | 0.84 |
Time A — before neutral hand wash; Time B — after neutral hand wash; Time C — after scrub or rub; Time D — after surgery.
One surgeon performed more surgeries than the others (29 against 20 for the other 2 combined) but there was no statistical effect of surgeon over the analysis. The surgeon with the larger number of surgeries had an increased CFUs at the first sampling time compared with the other surgeons, but there was no difference in the post-treatment samples.
One horse assigned to the scrub group had a superficial incision infection following a stifle arthroscopy and this resolved with medical treatment. No other horse in the study had an SSI. The number of surgical site infections was not compared statistically between groups due to the very low incidence. Over the 49 pairs of gloves tested, holes were found once in the non-dominant hand and twice in the dominant one from 3 surgeries and 2 surgeons. This gave an overall glove perforation rate of 3%. No holes were found in the gloves of the surgeon during the surgery of the horse with the SSI.
The mean duration of surgery was 83 min (range ± 42 min). Seven surgeries were longer than 120 min and 1 had a surgical time of 195 min but there was no difference in the CFU at the end of surgery between these 7 longer surgeries and the shorter surgeries. The times of surgery were not different between treatment groups.
Discussion
The bacterial CFU on the hands of equine surgeons following hand antisepsis were not statistically different when comparing the brushless technique with the traditional CHG 4% scrub sponge and water technique. In human medicine, several studies have shown that alcohol-based rubs are as effective as or more effective than traditional techniques with brushes or sponges for the first (21) or for the consecutives scrubs of the day (22–26). These studies were performed in both research and clinical settings. Compared with water-based scrubs alcohol-based hand rubs have been associated with superior compliance and better health of the surgeons. The World Health Organization (WHO) recommends this method of hand antisepsis (16,21), although there are ongoing studies around the correct time of application, percentage of alcohol, addition of glycerol and whether varying alcohol based hand rubs meet the European Normalization Committee requirements (22–25).
Girou et al (11) reported that an alcohol-based hand rub (Sterillium) tested in the hands of healthcare workers during routine patient care was more effective than hand washing with an antiseptic soap in reducing bacterial contamination. Other researchers associated part of the superior performance to inadequate time spent washing hands conventionally, showing that the faster application of the hand rubs is useful in routine working conditions, thus improving compliance (22,23). The WHO recommends a 3-minute rub for the best efficacy of the alcohol-based products but our results corroborate previous findings that a 1.5-minute rub was enough to significantly reduce the CFU counts on the hands of surgeons, similar to a traditional CHG 4% scrub (26,27). Although the analysis did not find an effect of surgeon on the results the lack of compliance evaluation in the present study remains an important limitation.
Skin contamination in large animal surgeons may be different from that in human surgeons because large animal surgeons are commonly involved in the pre-operatory preparation of the patient and patient placement on the surgery table. In the hospital in which the study took place, the surgeons directly aid in the preparation and induction of horses. During evaluation of a colic patient even transrectal examinations may be performed immediately before the surgical procedure (1–4). Considering this, it is recommended in veterinary medicine that the first scrub of the day be done with sponges or brushes and subsequent scrubs might be brushless (1) but there is no evidence that supports this recommendation. The current study does not support this recommendation either; however, the 1-minute hand wash with neutral soap was performed at all times to remove gross debris which continues to be an important step in the process. Taking into account that the hands of the surgeons were highly contaminated and there was a significant decrease in the CFU with the alcohol rub similar to the CHG group regardless of the timing throughout the day, it is proposed that, with a prior 1-minute hand wash to remove gross debris, the hand rub technique can be used as a safe hand antisepsis technique in the veterinary field.
There was no difference in residual effect found in this study as was found in the previous veterinary study using an alcohol-based hand rub (Sterillium) at the 3-hour time point (3). There were 8 surgeries that took longer than 120 min and 1 that took more than 180 min. Only 2 of these longer surgeries showed minimal CFU at the end of surgery (3 and 4 CFU) but there was no difference between treatment groups. Most of the surgeries were less than 2 h and it is likely that this short time made it impossible to associate our results with a potential improved residual effect of the alcohol hand rub with 1% chlorhexidine. The 2 rubs have different compositions and so should not be compared directly. It was for this reason that it was felt to be important to perform a veterinary study with an alcohol hand rub with 1% chlorhexidine and the results presented here are applicable in general to surgeries lasting less than 2 h.
The alcohol hand rub product with 1% chlorhexidine is the alcohol-based hand rub most frequently used by equine surgeons (4) and was the only one available in Canada at the time of this study. It had superior persistent activity compared with other commercial alcohol-only products after 6 h of wearing a glove (25) and contains different emollient products to decrease the amount of glycerol in its formulation. It was recently shown that the residual effect of different alcohol-based products containing glycerol is decreased in those that have higher concentrations of this molecule, suggesting that decreasing the glycerol content or using alternatives such as propylene glycol or urea would increase the sustained bactericidal efficacy of alcohol-based hand rubs (28).
The residual effect of antiseptics is fundamental to reduce the infection rates in the surgical wound because of the increased number of unnoticed glove punctures during surgery. In the human field the rate of unnoticed punctured gloves can vary between 30% in cardiac surgeries (6) to 80% in orthopedic surgeries (7) and the numbers of glove holes and CFU increase proportionally to the time of surgery (6,7). Over the 49 pairs of gloves tested here, 2 gloves from the dominant hand and 1 from the non-dominant hand had unrecognized holes, highlighting the importance of pre-operation hand antisepsis. The glove holes were not related to increased CFU counts and, in the small number studied, were not related to the length of surgery.
As only 1 horse had an SSI, the effectiveness of the surgical scrub technique could not be used in the analysis. Although the majority of horses in this population return to the hospital when they have an SSI, the number of SSIs may have been underestimated due to loss of follow-up. Surgical site infections as well as CFU are the main methods that have been established for evaluation of surgical scrub techniques. The health of the surgeons’ hands was also not evaluated in this study as the technique of scrubbing was assigned randomly rather than in a block design. We are therefore unable to make any observations on the effect on the skin health as has been made in other studies. This is a major limitation of the study as hand health is an important argument in the implementation of alcohol-based hand rubs.
Glove washing (6,22), fingertip printing on agar plates (23,28), or swabbing techniques (20) have been described for sampling and for evaluation of the number of CFU on the hands; they all have advantages and disadvantages. The WHO recommends the fingertip printing over the glove washing method because this method is more readily applicable in a field situation providing good results when evaluating transient flora, but it provides less accurate bacterial counts (16). As CFU counts were being used as an endpoint in this study there was a need for accurate CFU counts. The swabbing technique that was used in this study was validated in a recent study as a simple way to obtain precise CFU counts (20). The glove washing technique is impractical in a clinical situation requiring multiple glove changes if various time points are being collected.
Due to the residual bacteriostatic or bactericidal activity of CHG, the use of effective neutralizing agents in the sampling fluids is important to avoid false positive efficacy assessments when testing products containing this molecule (18,29). As the hand rub tested has CHG in its formula the neutralizing agent was used and a false increased effectiveness can be excluded.
The hand rub technique avoids the waste of approximately 20 L of water for each surgical hand disinfection episode with traditional agents (15) and removes the risk of recontamination of the hands with tap water or sink droplets. Tap water can be associated with Pseudomonas aeruginosa infection when it is used for hydrotherapy of burned patients or for rinsing medical devices after disinfection (30) and 10% of the faucets in surgery rooms have a positive status for Pseudomonas (31).
In conclusion, the alcohol hand rub product with 1% chlorhexidine was effective for pre-surgical hand disinfection in equine veterinary surgery, without the need for a previous 5-minute traditional abrasive scrub with brushes. The small percentage of veterinary surgeons using these products should increase with improved veterinary studies. The mean reduction in the CFU counts was similar to that obtained with the traditional CHG hand scrub.
Acknowledgment
The authors thank the ACVS Foundation for funding this study through a Diplomate Clinical Research Grant. CVJ
Footnotes
The study was presented as an abstract at the ACVS Meeting 2013 in San Antonio, Texas.
Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.
References
- 1.Stick JA. Preparation of the surgical patient, the surgery facility, and the operating team. In: Auer JA, Stick JA, editors. Equine Surgery. 4th ed. St. Louis, Missouri: Elsevier Saunders; 2012. pp. 111–122. [Google Scholar]
- 2.Wan PY, Blackford JT, Bemis DA, Rohrbach BW, Knoll DE, Provenza MK. Evaluation of surgical scrub methods for large animal surgeons. Vet Surg. 1997;26:382–385. doi: 10.1111/j.1532-950x.1997.tb01697.x. [DOI] [PubMed] [Google Scholar]
- 3.Verwilghen DR, Mainil J, Mastrocicco E, et al. Surgical hand antisepsis in veterinary practice: Evaluation of soap scrubs and alcohol based rub techniques. Vet J. 2011;190:372–377. doi: 10.1016/j.tvjl.2010.12.020. [DOI] [PubMed] [Google Scholar]
- 4.Verwilghen D, Grulke S, Kaempf G. Presurgical hand antisepsis. Concepts and current habits of veterinary surgeons. Vet Surg. 2011;40:515–521. doi: 10.1111/j.1532-950X.2011.00846.x. [DOI] [PubMed] [Google Scholar]
- 5.Larson EL, Hughes CA, Pyrek JD, Sparks SM, Cagatay EU, Bartkus JM. Changes in bacterial flora associated with skin damage on hands of health care personnel. AM J Infect Control. 1998;26:513–521. doi: 10.1016/s0196-6553(98)70025-2. [DOI] [PubMed] [Google Scholar]
- 6.Eklund AM, Ojajarvi J, Laitinen K, Valtonen M, Werkkala KA. Glove punctures and postoperative skin flora of hands in cardiac surgery. Ann Thorac Surg. 2002;74:149–153. doi: 10.1016/s0003-4975(02)03690-1. [DOI] [PubMed] [Google Scholar]
- 7.Yinusa W, Li YH, Chow W, Ho WY, Leong JC. Glove punctures in orthopaedic surgery. Int Orthop. 2004;28:36–39. doi: 10.1007/s00264-003-0510-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Tanner J, Swarbrook S, Stuart J. Surgical hand antisepsis to reduce surgical site infection. Cochrane Database Syst Rev. 2008:CD004288. doi: 10.1002/14651858.CD004288.pub2. [DOI] [PubMed] [Google Scholar]
- 9.Burch TM, Stanger B, Mizuguchi KA, Zurakowski D, Reid SD. Is alcohol-based hand disinfection equivalent to surgical scrub before placing a central venous catheter? Anesth Analg. 2012;114:622–625. doi: 10.1213/ANE.0b013e31824083b8. [DOI] [PubMed] [Google Scholar]
- 10.Kampf G, Widner AF. Scrub or rub? What is best practice for hand hygiene before surgery? Vet J. 2011;190:307–308. doi: 10.1016/j.tvjl.2011.02.001. [DOI] [PubMed] [Google Scholar]
- 11.Girou E, Loyeau S, Legrand P, Oppein F, Brun-Buisson C. Efficacy of handrubbing with alcohol based solution versus standard hand-washing with antiseptic soap: Randomised clinical trial. BMJ 17 Aug. 2002;325:362. doi: 10.1136/bmj.325.7360.362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Pereira LJ, Lee GM, Wade KJ. An evaluation of five protocols for surgical handwashing in relation to skin condition and microbial counts. J Hosp Infect. 1997;36:49–65. doi: 10.1016/s0195-6701(97)90090-6. [DOI] [PubMed] [Google Scholar]
- 13.Olson LKM, Morse DJ, Duley C, Savell BK. Prospective, randomized in vivo comparison of a dual-active waterless antiseptic versus two alcohol-only waterless antiseptics for surgical hand antisepsis. Am J Infect Control. 2012;40:155–159. doi: 10.1016/j.ajic.2011.10.012. [DOI] [PubMed] [Google Scholar]
- 14.Weight CJ, Lee MC, Palmer JS. Avagard hand antisepsis vs. traditional scrub in 3600 pediatric urologic procedures. Urology. 2010;76:15–17. doi: 10.1016/j.urology.2010.01.017. [DOI] [PubMed] [Google Scholar]
- 15.Jehle K, Jarrett N, Matthews S. Clean and green: Saving water in the operating theatre. Ann R Coll Surg Engl. 2008;90:22–24. doi: 10.1308/003588408X242277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.World Health Organization (WHO) WHO Guidelines on Hand Hygiene in Health Care. Geneva, Switzerland: WHO; 2009. p. 270. [Google Scholar]
- 17.Löfler H, Kampf G. Hand disinfection: How irritant are alcohols? J Hosp Infect. 2008;70:44–48. doi: 10.1016/S0195-6701(08)60010-9. [DOI] [PubMed] [Google Scholar]
- 18.Kampf G, Wigger-Alberti W, Schoder V, Wilhelm KP. Emollients in a propanol-based hand rub can significantly decrease irritant contact dermatitis. Contact Dermatitis. 2005;53:344–349. doi: 10.1111/j.0105-1873.2005.00727.x. [DOI] [PubMed] [Google Scholar]
- 19.Boyce JM, Kelliher S, Vallande N. Skin irritation and dryness associated with two hand-hygiene regimens: Soap-and-water hand washing versus hand antisepsis with an alcoholic hand gel. Infect Control Hosp Epidemiol. 2000;21:442–448. doi: 10.1086/501785. [DOI] [PubMed] [Google Scholar]
- 20.Corder K, Knowles TG, Holt PE. Factors affecting bacterial counts during preparation of the hands for aseptic surgery. Vet Rec. 2007;160:897–902. doi: 10.1136/vr.160.26.897. [DOI] [PubMed] [Google Scholar]
- 21.Pittet D, Allegranzi B, Boyce J. The World Health Organization Guidelines on Hand Hygiene in Health Care and their consensus recommendations. Infect Control Hosp Epidemiol. 2009;30:611–622. doi: 10.1086/600379. [DOI] [PubMed] [Google Scholar]
- 22.Chen CF, Han CL, Kan CP, Chen SG, Hung PW. Effect of surgical site infections with waterless and traditional hand scrubbing protocols on bacterial growth. Am J Infect Control. 2012;40:e15–e17. doi: 10.1016/j.ajic.2011.09.008. [DOI] [PubMed] [Google Scholar]
- 23.Suchomel M, Koller W, Kundi M, Rotter ML. Surgical hand rub: Influence of duration of application on the immediate and 3-hours effects of n-propanol and isopropanol. Am J Infect Control. 2009;37:289–293. doi: 10.1016/j.ajic.2008.09.026. [DOI] [PubMed] [Google Scholar]
- 24.Suchomel M, Kundi M, Allegranzi B, Pittet D, Rotter M. Testing of the World Health Organization-recommended formulations for surgical hand preparation and proposals for increased efficacy. J Hosp Infect. 2011;79:115e–118e. doi: 10.1016/j.jhin.2011.05.005. [DOI] [PubMed] [Google Scholar]
- 25.Kampf G, Ostermeyer C. World Health Organization-recommended hand-rub formulations do not meet European efficacy requirements for surgical hand disinfection in five minutes. J Hosp Infect. 2011;78:123e–127e. doi: 10.1016/j.jhin.2011.02.005. [DOI] [PubMed] [Google Scholar]
- 26.Kampf G, Ostermeyer C, Kohlmann T. Bacterial population kinetics on hands during 2 consecutive surgical hand disinfection procedures. Am J Infect Control. 2008;36:369–374. doi: 10.1016/j.ajic.2007.09.009. [DOI] [PubMed] [Google Scholar]
- 27.Kac G, Masmejean E, Gueneret M, Rodi A, Peyrard S, Podglajen I. Bacterial efficacy of a 1.5 min surgical hand-rubbing protocol under in-use conditions. J Hosp Infect. 2009;72:135–139. doi: 10.1016/j.jhin.2009.02.015. [DOI] [PubMed] [Google Scholar]
- 28.Suchomel M, Rotter M, Weinlich M, Kundi M. Glycerol significantly decreases the three hour efficacy of alcohol-based surgical hand rubs. J Hosp Infect. 2013;83:284e–287e. doi: 10.1016/j.jhin.2012.11.030. [DOI] [PubMed] [Google Scholar]
- 29.Kampf G, Reichel M, Hollingsworth A, Bashir M. Efficacy of surgical hand scrub products based on chlorhexidine is largely overestimated without neutralizing agents in the sampling fluid. Am J Infect Control. 2013;41:e1–e5. doi: 10.1016/j.ajic.2012.07.018. [DOI] [PubMed] [Google Scholar]
- 30.Tredget EE, Shankowsky HA, Joffe AM, et al. Epidemiology of infections with Pseudomonas aeruginosa in burn patients: The role of hydrotherapy. Clin Infect Dis. 1992;15:941–949. doi: 10.1093/clind/15.6.941. [DOI] [PubMed] [Google Scholar]
- 31.Blanc DS, Nahimana I, Petignat C, Wenger A, Bille J, Francioli P. Faucets as a reservoir of endemic Pseudomonas aeruginosa colonization/infections in intensive care units. Intensive Care Med. 2004;30:1964–1968. doi: 10.1007/s00134-004-2389-z. [DOI] [PubMed] [Google Scholar]
