Operating Room Hand Preparation: To Scrub or to Rub?

Abstract

Background:

The alcohol rub has been proposed as an alternative to the traditional surgical scrub in preparing the hands for surgical procedures. Few reviews have examined critically the evidence that favors or discredits the use of the alcohol rub instead of the traditional scrub.

Methods:

A review of available published literature was undertaken to define the evidence for the best methods for hand preparation before surgical procedures. The focus of this literature review was to compare the bacteriologic and clinical outcomes of conventional surgical scrubbing of the hands compared with alcohol rubs.

Results:

The bacteriologic studies of the hands after the conventional scrub versus the alcohol rub demonstrated consistently comparable or superior reductions in bacterial presence on the hand with the alcohol rub. Only four clinical studies were identified that compared the scrub versus the rub in the frequency of surgical site infections. No difference in surgical site infections were identified.

Conclusions:

The alcohol rub appears to have comparable results to the surgical scrub and is a reasonable alternative in preparation of the hands for surgical procedures.

For the last century, a tradition in the preparation for surgical procedures has been the surgical scrub. It is a practice that all have accepted as having value in the prevention of surgical site infections (SSIs). Despite wearing gloves, the argument is made that glove perforations and fatigue during the procedure provide an opportunity for cutaneous colonization from the hands of the surgical team to contaminate the surgical site. With many millions of operations per year in the United States, it is likely that over 100 million pairs of hands of the operating surgeons, surgical technicians, operating room nurses, and surgical assistants are scrubbed annually.

For a practice that is so common and is considered so important for the care of the surgical patient, it is fascinating to observe the heterogeneity in the mechanics of the surgical scrub in the contemporary operating room [1]. Brushes or sponges are used to remove the surface contamination, different antiseptic soaps and solutions are used, and the duration of the scrub is highly variable. My observation for nearly 50 years—including my medical school surgical experience—has been that the practice of the surgical scrub has no standards. One is left with the impression that in the era of gloving for the procedure that surgeons really do not believe that hand cleansing has much of an added benefit. This review addresses the current recommendations and guidelines on surgical hand hygiene and examines the issue of utilizing antiseptic “hand rubs” before surgical gloving as an alternative or replacement of the traditional scrub. Will the traditional scrub be “rubbed out?”

History of the Surgical Scrub

It was Oliver Wendell Holmes in 1843 who first advocated hand washing to prevent puerperal fever in women after childbirth [2]. This recommendation was based upon his experiences and observations and was not accepted as a practice. The most noted advocacy for hand washing before a procedure is tracked back to Semmelweis [3] at the obstetrical ward of the Allgemeine Krankenhaus in Vienna in the late 1840s. He noted the different rates in life-threatening “child-bed fever” in women delivered by physicians compared with those delivered by midwives. He noted that the physicians commonly came directly from the autopsy room and that particulate matter from the necropsy was being transmitted to the patients with the manual pelvic examination performed with bare hands by the physician. On the other hand, midwives did not monitor the progress of labor with pelvic examinations and waited for the child to crown at which time the final phases of the delivery were attended. He hypothesized that the foreign contamination contained a toxic material that was responsible for the subsequent febrile syndrome, because these events pre-dated the germ theory of disease. He introduced a policy of hand washing in chlorinated water to rid the hands of the noxious contamination. Child-bed fever declined among physician deliveries to rates observed with the midwives [3]. Similar to the hand-washing recommendations of Holmes earlier, Semmelweis encountered considerable resistance from the academic community in the acceptance of the practice of handwashing.

It was Joseph Lister who understood the link between bacteria and surgical infections and he introduced hand washing with carbolic acid, as well as aerosolization and local application of the antiseptic to manage and avoid infection [4]. The practice of hand washing alone was systematically replaced by a more vigorous scrubbing of the hands to maximize the removal of bacteria.

The introduction of surgical gloves by Halstead in the 1890s moderated the interest in details of the surgical scrub [5,6]. Gloves became the mainstay for avoiding contamination from the hands of the surgical team, and over time the rubber glove was replaced with latex. The practice of the surgical scrub prior to being gloved continued as a practice. A rationale for the continuation of scrubbing before gloving was that the violations of the glove during the course of the procedure were not predictable. Failure of the glove barrier could result in critical contamination of the surgical site [7]. The standards for the surgical scrub did not exist, with some advocating cleansing of the hands for up to 10 minutes (or longer) and others advocating shorter periods of time. The topical antiseptic varied by the choice of the operating room or by personal preference of the surgeon.

Technical Details of Surgical Hand Hygiene

Research to identify which technical details have any impact upon surgical outcomes have been sparse over the last several decades. The lack of objective evidence to influence practice has not prevented authoritative guidelines from being released on best practices. The guidelines by the U.S. Centers for Disease Control and Prevention (CDC) have not been updated since 2002 [8], and the most recent guidelines on the prevention of SSI by the CDC did not address the issue of surgical hand hygiene at all [9]. The World Health Organization (WHO) has recently released a social media push on World Hand Hygiene Day (May 5, 2018) [10], but recommendations for surgical hand hygiene are unchanged from their earlier guidelines of 2009 [11].

Table 1 summarizes the key procedural recommendations of WHO that are to be followed with the surgical scrub. Only limited references are provided because most are derived from expert opinion and not by clinical data. Artificial nails have been demonstrated to harbor higher rates of gram-negative bacteria [12], and longer nails would logically be expected to increase the risk of glove puncture during the procedure. Nail polish has not been shown to increase bacterial colony counts [13] but avoiding the use of polish remains a WHO recommendation despite no evidence to support this position. A Cochrane Review by Arrowsmith and Taylor [14] concluded that there is no evidence that wearing nail polish or rings influences SSI rates, and evidence is inadequate that nail polish influences bacterial colony counts after the surgical scrub. One study demonstrated no increase in bacterial colonization in the surgical glove with the presence of rings [15].

Table 1.

Recommendations by the World Health Organization for Surgical Hand Hygiene [11]

Recommendation	Author commentary
Keep Fingernails short	A length of ¼ inch is recommended. Longer nails risk glove puncture.
Do not wear artificial nails or nail polish	Artificial nails have been shown to have increased colonization; no increased colonization has been shown with nail polish.
Remove all jewelry	Jewelry (e.g., rings) and underlying tissue will be harder to cleanse with the surgical scrub.
Clean subungual areas with a nail file	Subungual areas have more foreign bodies and higher bacterial colonization
Wash hands/forearms with non-medicated soap	Comparisons of soap type has not been analytically evaluated.
Scrub fingers, front and back of hands; 2 minutes	Duration of hand scrub has not been critically evaluated for improved outcomes
When scrubbing arms, keep hands higher	It is logical to not have water draining from the proximal arm onto the hands.
Wash each arm (wrist-to-elbow) 1 minute each	Duration of arm scrub for best outcomes is unknown.
Rinse hands with water from fingertips to elbow	Water rinse away from the hands makes sense but not an evidence-based recommendation
Do not splash water on surgical attire	Bacterial break-through in wet surgical garments is a likely risk.
Proceed to OR with hands elevated	Common sense to not have water draining down onto the hands
Dry hands/arms with sterile towel in OR	Common sense

OR = operating room.

The duration of the surgical scrub has not been demonstrated to reduce subsequent SSIs. A series of studies by Pereira et al. [16,17] have demonstrated no differences in colony counts as a function of the duration of surgical scrub but did identify a reduction in bacterial hand colonization when chlorhexidine was used compared with povidone iodine as the antiseptic used. Wheelock and Lookinland [18] demonstrated a reduction in colony counts of a three-minute scrub compared to two minutes in the “glove juice” fluid after completion of the operation, whereas studies by Tucci et al. [19] found no benefit when comparing a 10-minute scrub to five minutes [19]. Among other elements recommended by the WHO guidelines, the use of the nail pick did not reduce colony counts in the glove fluid compared with conventional hand preparation without using the pick [20].

Because of undesirable local effects on the skin, alcohol has generally not been used as part of the traditional surgical scrub. Chlorhexidine and povidone iodine scrub solutions have predominated. Some evidence supports that chlorhexidine has a greater reduction in skin colony counts compared with povidone iodine at the completion of the scrub [21]. A comprehensive review of surgical hand preparation concluded that the current evidence was of low to very low quality in the recommendation of choices for antiseptics, and that none demonstrated a reduced rate of SSI [22]. The comparisons of different antiseptic preparations have only used differences in bacterial colonization as the metric.

Alcohol-based skin preparations of the surgical site have gained a resurgence in popularity with recent evidence that the addition of alcohol with conventional antiseptics have been demonstrated to reduce SSI infections [23,24]. The recent CDC recommendation that an alcohol-based antiseptic be used for cleansing the surgical site [9] appears to have lent support to the increased interest over the past 20 years that perhaps an alcohol-based preparation could be a useful alternative to the traditional surgical scrub in the reduction of hand colonization.

Scrub or Rub: Bacterial Colonization

The majority of the evidence comparing the traditional surgical scrub to alcohol rubs has used residual bacterial counts as the primary end point of the comparison. A representative list of studies that have compared bacterial counts after scrubs or topical applications of antiseptics before or after hand preparation are identified in Table 2 [25 –35]. The evidence generally shows that alcohol-based hand rubs are comparable or better in reducing bacterial counts than other antiseptic choices, but the addition of chlorhexidine to the alcohol rub may enhance antibacterial effects further. An attempted meta-analysis of these heterogenous studies has concluded similarly that alcohol-based hand rubs have the best results in the reduction of bacterial colonization of the hand [36].

Table 2.

Bacteriologic Studies by First Author that Compare Different Pre-Operative Hand Preparation Methods

Author, year	Culture method	Results of comparison
Mulberry, 2001 [25]	Glove juice	Waterless CHG/ethanol better bacterial reduction than scrub with either CHG or ethanol alone
Larson, 2001 [2]6	Glove juice	Waterless alcohol/CHG/emollient had better antibacterial effect than traditional 4% CHG scrub
Carro, 2007 [27]	Finger imprints	Alcohol hand rub superior to conventional scrub (either CHG or PI) with lower bacterial counts at the end of cardiovascular surgery
Gupta, 2007 [28]	Glove juice	Waterless alcohol, aqueous alcohol, and iodine scrub yielded similar bacteriologic effects.
Beausoliel, 2012 [29]	Glove juice	Alcohol/CHG rub superior to conventional scrub in bacterial reduction
Lai, 2012 [30]	Finger imprints	Best bacterial reduction with alcohol/CHG rub compared to convention scrub with PI
Olson, 2012 [31]	Glove juice	Alcohol/CHG combined had best persistence of bacterial growth compared to alcohol preparations alone
Chen, 2012 [32]	Hand imprints	Waterless hand preparation with CHG alone as effective as traditions surgical scrub with CHG
Shen, 2015 [33]	Saline cotton swab/agar plating	Hand rub of CHG plus alcohol compared to conventional scrub with either 4% CHG or 7.5% PI
Tsai, 2017 [34]	Hand imprints	Hand rub of CHG plus alcohol provided better reduction in bacteria than either, or convention scrub with CHG alone were best compared to PI scrub.
Forer, 2017 [35]	Glove juice	Alcohol rub was more effective than routine surgical scrub with either CHG or PI

CHG = chlorhexidine; PI = povidone iodine.

It should be noted that different techniques have been used in sampling bacteria after scrubs or topical applications to the hand and this makes comparison of the evidence somewhat difficult. The “glove juice” method applies a glove or a plastic bag over the hand and a sample of irrigate solution is added [37]. The hand and fingers are massaged for a standard period of time and the fluid within the glove is sampled and a quantitative culture defines the number of colony-forming units. Another method is to simple press the fingers or hands unto an agar plate; this is cultured to identify viable bacteria. Saline cotton swabs have been used to give a less quantitative comparison of hand preparation methods. Regardless of the culturing method utilized, the use of the alcohol rub has demonstrated a consistently greater reduction in bacterial counts on the hands. Only the study by Hajipour et al. [38] found chlorhexidine to be superior to alcohol gel in the reduction of bacterial colonies from the hands.

In most of these simulations and samplings of bacterial colonization of the hand after hand preparation the issue of skin injury, irritation, and local cutaneous effects of the topical agents or the mechanical process of cleansing the hands have been noted [39]. Thus, in the development of potential gels and rubs, different agents have been added to the topical alcohol rubs that have been used. Suchomel et al. [40] noted that glycerol as a skin protection agent that has been proposed as an additive for use in hand rubs appears to ameliorate the antimicrobial effects of alcohol-based hand rubs. Others have suggested the benefits of glycerol because alcohol-associated skin peeling may result in over-recolonization of the hands with alcohol rubs [41]. Hand lotions were not demonstrated to impact alcohol rubs adversely if used more than five minutes before application of the rub process [42]. It is clear that the role of additives and other agents added to the alcohol base will need to be evaluated further.

Scrub or Rub: SSI Rates

Only a limited number of clinical trials have been performed in randomized comparisons or studies of the traditional surgical scrub compared with the alcohol-based hand rub on the rates of SSIs in surgical procedures. The data from these studies are summarized in Table 3. Parienti et al. [43] studied more than 4,000 clean and clean-contaminated operations in which each of the participating surgical services rotated the conventional scrub with either 4% chlorhexidine or 4% povidone iodine, or the 75% aqueous alcohol-based hand rub after a non-antiseptic one-minute hand wash. The results demonstrated a 2.48% SSI rate in the hand scrubbing protocol and an insignificantly different 2.44% SSI rate in the alcohol rub protocol patients. The aqueous alcohol protocol achieved better compliance with the surgical personnel and fewer reported issues of skin irritation/dryness.

Table 3.

A Summary of the Data from Four Clinical Studies or Trials of the Traditional Surgical Scrub Compared with the Alcohol Rub

	Traditional scrub		Alcohol rub
Author, Year	Total patients	SSIs	Total patients	SSIs	Results
Parienti, 2002^a	2,135	53 (2.5%)	2,252	55 (2.4%)	p < 0.001; χ² test of equivalence
Al-Naami, 2009^a	228	12 (5.3%)	272	8 (2.9%)	p = 0.19; χ²; no difference
Nthumba, 2010^a	1,596	128 (5.3%)	1,537	127 (8.3%)	p = 0.804; χ²; No difference
Gaspar, 2018^b	132	11 (8.3%)	99	4 (4.0%)	p = 0.28; Fisher exact test; no difference

These studies used SSI as the primary end point for evaluation. All four studies demonstrated no differences in SSI rates between the traditional scrub and the alcohol rub.

Clean and clean-contaminated procedures.

Cardiac and orthopedic procedures.

SSI = surgical site infection.

Nthumba et al. [44] randomly assigned 3,317 surgical patients to a conventional soap and water scrub versus a 75% alcohol rub. The operative procedures were a mixture of clean, clean-contaminated, elective, and emergency cases. Systemic antibiotic administration was not controlled. The results in this developing country (Kenya) study demonstrated no differences (p = 0.804) in SSI rates with 8.0% in the scrub group and 8.3% in the alcohol rub group.

Al-Naami et al. [45] randomly assigned 500 patients undergoing clean and clean contaminated operation with the conventional surgical scrub versus the alcohol hand rub before the surgical procedure. Surgical site infection was reported in 5.3% of operations in which the conventional scrub was used compared with 2.9% in the alcohol rub group (not significant). Skin reactions were noted to be less frequent in the alcohol rub group.

Gaspar et al. [46] used a three-month control period of conventional scrub cases followed by three months of alcohol rub interventions in cardiac and orthopedic patients. Univariable analysis demonstrated no substantial difference (Table 3). Using multivariable analysis on the 150 cases with complete data from the two study periods, the alcohol scrub assumed no significance in predicting SSI.

Discussion

In the era of evidence-based medicine, it is interesting that one of the most common practices in surgery has little evidence to inform the practice. All would agree that the evidence from Semmelweiss [3] and Lister [4] justifies hand cleansing with patient contacts by care providers, and the surgical glove has provided a valuable barrier between potential colonization of the surgical hands and the patient. However, a study of soap and water for washing the hands followed by drying on a sterile paper towel may well be as effective in reducing SSIs as the elaborate, preference-driven, and unproven surgical scrub before the surgical gloves are worn. As noted by Kramer et al. [47], the conventional surgical scrub is a religious ceremony that is performed without exception. With the estimate of 18.5 L of water per provider scrubbing before procedures [48], it is certain that vast amounts of water are used for a practice that is of little or no benefit compared with a simpler alternative. The conservation of water resources is of great importance in emerging countries where surgical procedures are performed. The studies presented in this review indicate that the alcohol rub is at least as good as the conventional surgical scrub. Clinical trials demonstrate no differences in actual SSI rates and it is likely that an unrealistic study size would be required to ever identify a difference. The study of Parienti et al. [43], which statistically identified non-inferiority of the alcohol rub, may be the best that can be done in studying this issue.

Adoption of the alcohol rub requires attention to details to achieve optimum reduction in bacterial colonization of the hands. The alcohol preparation must cover all of the hand and finger surfaces. An essential feature of alcohol-based hand rubs is that the skin be completely dry after application. Larger volumes of the alcohol rub will require modestly longer drying times [49]. The formulation as a liquid, gel, or foam shows no difference in antibacterial activity and only minimal differences in drying time [50]. No difference in the duration of alcohol hand rubs between 15 and 30 seconds and no additional benefit to extending the duration beyond 30 seconds was found [51].

Hands will re-colonize with bacteria to pre-scrub concentrations by five hours [52]. Long operations should have a strategy for re-cleansing of the hands, and the alcohol rubs appears suitable for this consideration given the limited time that is necessary for completing an interim alcohol application. Re-cleansing of the hands appears to be much more efficient with the alcohol rub when glove violations occur during the conduct of the procedure.

In summary, changing the pre-operative ritual at the scrub sink before operations will require years to complete. The current evidence favors the adoption of the alcohol rub instead of the traditional scrub. The design of better and more tolerable formulations for the rub to minimize the tissue injury from the alcohol preparations appears to be the next step in the acceptance of this method in the evolution of hand preparation for surgery.

Footnotes

Author Disclosure Statement

The author declares a financial relationship with IrriMax Corporation, Becton Dickinson Corporation, and Prescient Surgical Company.

References

Abdollahi

, Tabrizi

, Jodati

, et al. Quality of surgical scrub in a heart hospital: Do not take it for granted. J Cardiovasc Thorac Res, 2017; 9:164–169.

Holmes

. The contagiousness of puerperal fever. N Engl Q J Med Surg, 1843; 1:503–521.

Semmelweis

. Die aetiologie, der begriff and die prophylaxis des kindbettfiebers [The etiology, concept, and prophylaxis of childbed fever]. Pest, Wein, and Leipzig. C.A. Hartleben's Verlag-Expedition, 1861.

Lister

. Antiseptic principles in the practice of surgery. Br Med J, 1867; ii:246.

Ellis

. Evolution of the surgical glove. J Am Coll Surg, 2008; 207:948–949.

Lathan

. Caroline Hampton Halsted: The first to use rubber gloves in the operating room. Proc (Bayl Univ Med Cent), 2010; 23:389–392.

Harnoss

J-C

, Partecke

L-I

, Heidecke

C-D

, et al. Correlation of bacteria passing through puncture holes in surgical gloves. Am J Infect Control, 2010; 38:154–158.

Centers for Disease Control and Prevention: Guideline for hand hygiene in health-care settings. MMWR, 2002; 51(RR-16):1–45.

Berrios-Torres

, Umscheid

, Bratzler

, et al. Centers for Disease Control and Prevention Guideline for the prevention of surgical site infection. JAMA Surg, 2017; 152:784–791.

10.

World Health Organization> Save Lives: Clean your hands. May 5, 2018. www.who.int/infection-prevention/campaigns/clean-hands/5may2018/en/ (Last accessed November 12, 2018)

11.

World Health Organization> WHO guidelines on hand hygiene in health care. http://apps.who.int/iris/bitstream/handle/10665/44102/9789241597906_eng.pdf;jsessionid=B77DF6C0B86703E3236B9BEDC5A09906?sequence=1 (Last accessed November 12, 2018).

12.

Edel

, Houston

, Kennedy

, LaRocco

. Impact of a 5-minute scrub on the microbial flora found on artificial, polished, or natural fingernails of operating room personnel. Nurs Res, 1998; 47:54–59.

13.

Wynd

, Samstag

, Lapp

. Bacterial carriage on the fingernails of OR nurses. AORN J, 1994; 60:796–780.

14.

Arrowsmith

, Taylor

. Removal of nail polish and finger rings to prevent surgical infection. Cochrane Database Syst Rev, 2014;(8):CD003325.

15.

Waterman

, Smeak

, Kowalski

, Hade

. Comparison of bacterial counts in glove juice of surgeons wearing smooth band rings versus those without rings. Am J Infect Control, 2006; 34:421–425.

16.

Pereira

, Lee

, Wade

. The effect of surgical handwashing routines on the microbial counts of operating room nurses. Am J Infect Control, 1990; 18:354–364.

17.

Pereira

, Lee

, Wade

. An evaluation of five protocols for surgical handwashing in relation to skin condition and microbial counts. J Hosp Infect, 1997; 36:49–65.

18.

Wheelock

, Lookinland

. Effect of surgical hand scrub time on subsequent bacterial growth. AORN J, 1997; 65:1087–1092.

19.

Tucci

, Stone

, Thompson

, et al. Studies of the surgical scrub. Surg Gynecol Obstet, 1977; 145:415–416.

20.

Tanner

, Khan

, Walsh

, et al. Brushes and picks used on nails during the surgical scrub to reduce bacteria: A randomised trial. J Hosp Infect, 2009; 71:234–238.

21.

Furukawa

, Tajiri

, Suzuki

, Norose

. Are sterile water and brushes necessary for hand washing before surgery in Japan?. J Nippon Med Sch, 2005; 72:149–154.

22.

Tanner

, Dumville

, Norman

, Fortnam

. Surgical hand antisepsis to reduce surgical site infection. Cochrane Database Syst Rev, 2016;(1):CD004288.

23.

Darouiche

, Wall

Jr , Itani

, et al. Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. N Engl J Med, 2010; 362:18–26.

24.

Uppal

, Bazzi

, Reynolds

, et al. Chlorhexidine-alcohol compared with povidone-iodine for preoperative topical antisepsis for abdominal hysterectomy. Obstet Gynecol, 2017; 130:319-327.

25.

Mulberry

, Snyder

, Heilman

, et al. Evaluation of a waterless, scrubless chlorhexidine gluconate/ethanol surgical scrub for antimicrobial efficacy. Am J Infect Control, 2001; 29:377–382.

26.

Larson

, Aiello

, Heilman

, et al. Comparison of different regimens for surgical hand preparation. AORN J, 2001; 73:412–414.

27.

Carro

, Camilleri

, Traore

, et al. An in-use microbiological comparison of two surgical hand disinfection techniques in cardiothoracic surgery: Hand rubbing versus hand scrubbing. J Hosp Infect, 2007; 67:62–66.

28.

Gupta

, Czubatyj

, Briski

, Malani

. Comparison of two alcohol-based surgical scrub solutions with an iodine-based scrub brush for persurgical antiseptic effectiveness in a community hospital. J Hosp Infect, 2007; 65:65–71.

29.

Beausoleil

, Paulson

, Bogert

, Lewis

. In vivo evaluation of the persistent and residual antimicrobial properties of three hand-scrub and hand-rub regimes in a simulated surgical environment. J Hosp Infect, 2012; 81:283–287.

30.

Lai

, Foo

, Low

, Naidu

. Surgical hand antisepsis-a pilot study comparing povidone iodine hand scrub and alcohol-based chlorhexidine gluconate hand rub. Ann Acad Med Singapore, 2012; 41:12–16.

31.

Olson

, Morse

, Duley

, Savell

. 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.

32.

Chen

, Han

, Kan

, et al. Effect of surgical site infections with waterless and traditional hand scrubbing protocols on bacterial growth. Am J Infect Control, 2012; 40:e15–17.

33.

Shen

, Pan

, Sheng

, et al. Comparative antimicrobial efficacy of alcohol-based hand rub and conventional surgical scrub in a medical center. J Microbiol Immunol Infect, 2015; 48:322–328.

34.

Shen

, Pan

, Sheng

, et al. Comparative antimicrobial efficacy of alcohol-based hand rub and conventional surgical scrub in a medical center. J Microbiol Immunol Infect, 2015; 48:322–328.

35.

Forer

, Block

, Frenkel

. Preoperative hand decontamination in ophthalmic surgery: A comparison of the removal of bacteria from surgeons' hands by routine antimicrobial scrub versus an alcoholic hand rub. Curr Eye Res, 2017; 42:1333–1337.

36.

, Wang

, Loh

, Tam

. Antiseptic efficacies of waterless hand rub, chlorhexidine scrub, and povidone-iodine scrub in surgical settings: a meta-analysis of randomized controlled trials. J Hosp Infect (in press).

37.

Kampf

, Ostermeyer

, Heeg

, Paulson

. Evaluation of two methods of determining the efficiencies of two alcohol-based hand rubs for surgical hand antisepsis. Appl Environ Microbiol, 2006; 72:3856–3861.

38.

Hajipour

, Longstaff

, Cleeve

, et al. Hand washing rituals in trauma theatre: clean or dirty?. Ann R Coll Surg Engl, 2006; 88:13–15.

39.

Liu

, Mehigan

. The effects of surgical hand scrubbing protocols on skin integrity and surgical site infection rates: A systematic review. AORN J, 2016; 103:468–482.

40.

Suchomel

, Rotter

, Weinlich

, Kundi

. Glycerol significantly decreases the three hour efficacy of alcohol-based surgical hand rubs. J Hosp Infect, 2013; 83:284–287.

41.

Barbadoro

, Martini

, Savini

, et al. In vivo comparative efficacy of three surgical hand preparation agents in reducing bacterial count. J Hosp Infect, 2014; 86:64–67.

42.

Paula

, Hübner

, Assadian

, et al. Effect of hand lotion on the effectiveness of hygienic hand antisepsis: Implications for practicing hand hygiene. Am J Infect Control, 2017; 45:835–838.

43.

Parienti

, Thibon

, Heller

, et al. Hand-rubbing with an aqueous alcoholic solution vs traditional surgical hand-scrubbing and 30-day surgical site infection rates: A randomized equivalence study. JAMA, 2002; 288:722–727.

44.

Nthumba

, Stepita-Poenaru

, Poenaru

, et al. Cluster-randomized, crossover trial of the efficacy of plain soap and water versus alcohol-based rub for surgical hand preparation in a rural hospital in Kenya. Br J Surg, 2010; 97:1621–1628.

45.

Al-Naami

, Anjum

, Afzal

, et al. Alcohol-based hand-rub versus traditional surgical scrub and the risk of surgical site infection: A randomized controlled equivalent trial. EWMA J, 2009; 9:5–10.

46.

Gaspar

, Menegueti

, Lopes

AER

, et al. Alcohol-based surgical hand preparation: Translating scientific evidence into clinical practice. Antimicrob Resist Infect Control, 2018; 7:80.

47.

Kramer

, Hübner

, Below

, et al. Improving adherence to surgical hand preparation. J Hosp Infect, 2008; 70(Suppl 1):35–43.

48.

Jehle

, Jarrett

, Matthews

. Clean and green: Saving water in the operating theatre. Ann R Coll Surg Engl, 2008; 90:22–24.

49.

Wilkinson

MAC

, Ormandy

, Bradley

, et al. Dose considerations for alcohol-based hand rubs. J Hosp Infect, 2017; 95:175–182.

50.

Wilkinson

MAC

, Ormandy

, Bradley

, Hines

. Comparison of the efficacy and drying times of liquid, gel and foam formats of alcohol-based hand rubs. J Hosp Infect, 2018; 98:359–364.

51.

Pires

, Soule

, Bellissimo-Rodrigues

, et al. Hand hygiene with alcohol-based hand rub: How long is long enough?. Infect Control Hosp Epidemiol, 2017; 38:547–552.

52.

Hosseini

, Mundis

Jr , Eastlack

, et al. Do longer surgical procedures result in greater contamination of surgeons' hands?. Clin Orthop Relat Res, 2016; 474:1707–1713.