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The Veterinary Journal 190 (2011) 372377

Contents lists available at ScienceDirect

The Veterinary Journal


journal homepage: www.elsevier.com/locate/tvjl

Surgical hand antisepsis in veterinary practice: Evaluation of soap scrubs


and alcohol based rub techniques
Denis R. Verwilghen a,, Jacques Mainil b, Emilie Mastrocicco a, Annick Hamaide c,
Johann Detilleux d, Gaby van Galen a, Didier Serteyn a, Sigrid Grulke a
a

Equine Clinic, Department of Clinical Sciences of Companion Animals and Equids, Faculty of Veterinary Medicine of Liege, Bld de Colonster 20 B41, 4000 Liege, Belgium
Department of Infectious and Parasitic Diseases, Faculty of Veterinary Medicine of Liege, Bld de Colonster 20 B43, 4000 Liege, Belgium
Small Animal Clinic, Department of Clinical Sciences of Companion Animals and Equids, Faculty of Veterinary Medicine of Liege, Bld de Colonster 20 B44, 4000 Liege, Belgium
d
Department of Genetics and Biostatistics, Faculty of Veterinary Medicine of Liege, Bld de Colonster 20 B43, 4000 Liege, Belgium
b
c

a r t i c l e

i n f o

Article history:
Accepted 19 December 2010

Keywords:
Surgery
Hand asepsis
Veterinary
Disinfection
Rub
Scrub

a b s t r a c t
Recent studies have shown that hydro-alcoholic solutions are more efcient than traditional medicated
soaps in the pre-surgical hand antisepsis of human surgeons but there is little veterinary literature on the
subject. The aim of this study was to compare the efciency of medicated soaps and a hydro-alcoholic
solution prior to surgery using an in-use testing method in a veterinary setting. A preliminary trial
was performed that compared the mean log10 number of bacterial colony forming units (CFU) and the
reduction factors (RF) between two 5-min hand-scrubbing sessions using different soaps, namely, povidone iodine (PVP) and chlorhexidine gluconate (CHX), and the 1.5-min application of a hydro-alcoholic
rub.
A clinical in-use trial was then used to compare the hydro-alcoholic rub and CHX in a surgical setting.
Sampling was performed using nger printing on agar plates. The hydro-alcoholic rub and CHX had a
similar immediate effect, although the sustained effect was signicantly better for the hydro-alcoholic
rub, while PVP had a signicantly lower immediate and sustained effect. The hydro-alcoholic rub showed
good efciency in the clinical trial and could be considered as a useful alternative method for veterinary
surgical hand antisepsis.
2010 Elsevier Ltd. All rights reserved.

Introduction
The importance of hand hygiene was rst recognized in 1847
when a dramatic decrease in mortality rates occurred after
Semmelweis (1861) introduced hand scrubbing with chlorinated
lime solutions prior to every physical examination (Adriaanse
et al., 2000). After recognition of the work of Lister (Tan and Tasaki,
2007) towards the end of the 19th century, surgical hand antisepsis
was globally accepted. Soon after, Pasteur stated: Instead of forcing
ourselves in trying to kill microbes in wounds, would it not be more
reasonable not to introduce them (Wangensteen, 1975); a statement
that remains true today.
Surgical site infection (SSI) nevertheless continues to be one of
the most frequent types of nosocomial infections (NNIS, 2003), despite the fact that pre-surgical antiseptic treatment of hands for
Corresponding author. Present address: Equine Clinic, Faculty of Veterinary
Medicine, University of Agricultural Sciences, Ulls vg 12, Box 7040, 750 07 Uppsala,
Sweden. Tel.: +32 4 3664103.
E-mail
addresses:
denis@proamhorses.eu,
Denis.verwilghen@uds.slu.se
(D.R. Verwilghen).
1090-0233/$ - see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tvjl.2010.12.020

surgical staff has become mandatory. SSI is a primary factor in the


increase in human and veterinary health care costs due to delayed
wound healing, increased use of antibiotics, increased hospital stay
or even death of the patient (Plowman, 2000; Waguespack et al.,
2006).
The risk of SSI correlates with the dose and the virulence of
microbial contamination and the patient resistance (Owens and
Stoessel, 2008). In normal situations, the risk of SSI is considered
elevated when the bacterial count in wounds is P105 bacteria/g
of tissue (Hackett et al., 1983; Owens and Stoessel, 2008). Wearing
of gloves by surgical staff signicantly decreases surgical site contamination. However, glove perforation, principally occurring at
the index nger of the non-dominant hand, occurs in up to 67% of
surgical interventions (Dodds et al., 1988; Eklund et al., 2002;
Yinusa et al., 2004), highlighting the importance of correct hand
preparation. The objective of surgical hand antisepsis is therefore
to eliminate or reduce skin ora prior to gloving to diminish the risk
of SSI.
Three different types of surgical hand preparation methods are
available, namely, traditional aqueous scrubs containing antiseptic
agents, alcohol-based rubs and alcohol-based rubs containing

D.R. Verwilghen et al. / The Veterinary Journal 190 (2011) 372377

additional non-volatile active ingredients. Aqueous solutions


containing either povidone iodine (PVP) or chlorhexidine gluconate (CHX) have become standard over the past few decades,
although alcohol-based hand rubs (AHRs) have been used for over
100 years (Kampf and Kramer, 2004). The popularity of AHRs is
increasing amongst physician surgeons because they provide rapid
and immediate action, are considerably faster than disinfecting
soap scrubs and cause less skin damage after repeated use (Kampf
and Kapella, 2003; Lofer and Kampf, 2008).
Veterinary patients are likely to have higher bacterial counts on
their body surface than human patients, resulting in higher contamination loads on the hands of veterinary surgeons compared
to their human counterparts. Although the use of AHRs has been
tested in studying the reduction in bacterial loads on the hands
of veterinary staff between physical examinations of equine patients (Traub-Dargatz et al., 2006), only evaluations or comparisons
of hand antisepsis techniques using aqueous solutions have been
used in veterinary-surgical setting studies to date (Wan et al.,
1997; Waterman et al., 2006; Corder et al., 2007).
The aims of the present study were (1) to compare PVP and CHX
scrubs with a hydro-alcoholic rub hand antisepsis protocol and (2)
to evaluate the effectiveness of hydro-alcoholic rub solution in
reducing bacterial hand ora in veterinary surgery. The hypothesis
was that an AHR solution would be at least as effective as currently
used products and be acceptable to veterinary surgeons.

Materials and methods


Soaps
The following disinfecting soaps were tested: Chlorhexidine digluconate 4%
(Hibiscrub, Regent Medical) and 7.5% PVP-iodine (Vetclean, Ecuphar). The hand
rub was 45% 2-propanol, 30% 1-propanol, 0.2% mecetronium ethylsulfate (Sterillium, Bode-Chemie).

373

Preliminary study
This preliminary study was carried out by two surgeons experienced in hand
antisepsis techniques. Hands were sampled as described above prior to hand antisepsis (PHA), immediately after hand antisepsis (AHA) and 3 h after (after gloves,
AG/sustained effect) wearing sterile non-powdered gloves (Triex Select, CareFusion). Each product (PVP, CHX and AHR) was randomly used on separate days until
10 samples series (one PHA, one AHA, one AG) were obtained for each surgeon and
each product tested (20 samples series per product). Samples containing punctured
gloves were excluded from testing.
Surgical study
A trial using Sterillium and CHX soap was carried out by three equine and two
small animal surgeons during routine and emergency procedures. Hands were disinfected using the rubbing method for Sterillium and scrubbing method for CHX
soap. Sampled were collected as described above, with the inclusion of a sample taken immediately after the surgery (after surgery, AS/sustained effect) (= one series
of samples). Hands were double gloved (both non-powdered). The rst pair of
gloves (Protegrity SMT, CareFusion) was put on using a closed technique and covered with a second pair (Triex Select, CareFusion), which was discarded after draping the patient. For some procedures, a new second pair was put on after patient
draping. Only on the rst surgery of the day, a sample series was performed. Surgeons involved in the preliminary study did not combine preliminary samples
and surgical sampling on the same day. Time of surgery was recorded in intervals
of 30 min.
Statistical analysis
The obtained values of CFU from PHA, AHA, AG and AS were expressed as log10
values. For calculation purposes, values of 0 (log10 0 = 1) were set to 1
(log10 1 = 0). For each sample, a reduction factor (RF) was obtained from the difference of log10 pre-value and post-value. RF1 was the reduction between PHA and
AHA (immediate effect) and RF2 was between PHA and AG/AS (sustained effect).
The least square mean log10 CFU (LSM log10 CFU) and RF (LSM RF), including standard deviation (SD), of each product was calculated. For the preliminary study, ANOVA compared the effects of the different antisepsis protocols on the mean
log10 CFU values and RFs in function of the different steps (PHA, AHA, AG). This variance analysis included xed effects of the surgeon and the left and right hand. For
the surgical study, the same type of ANOVA comparison was performed for Sterillium and CHX soap in function of the different steps (PHA, AHA, AS). Fixed effects
of the type of surgery and the presence of glove punctures were additionally included. Signicance was set at P 6 0.05.

Sampling method and bacterial evaluation


We used an in-use condition testing method, as described by Rotter et al. (2009)
and used by Carro et al. (2007) and Kac et al. (2009) in-eld tests. A blood agar made
with a Columbia Agar Base (Merck) was used to test bacterial contamination of the
ngertips. All distal phalanges were gently pressed for 10 s onto two agar-containing Petri plates (one for the left, one for the right hand). Bacterial growth was quantied by counting the colony forming units (CFU) grown after 24 h incubation at
36 1 C.

Scrub technique
A 5-min scrubbing technique, using one of the above disinfecting soaps and
sterile disposable brushes (Scrub care, CareFusion), was carried out. Sub-ungual
areas were cleaned with a nail cleaner (disposable and delivered with the brushes).
Special attention was paid to nails and palms. Hands and forearms, including the
elbow, were washed with medicated soaps and dried with sterile disposable towels
prior to sampling and gloving.

Rub technique
The rubbing method followed the European standardisation norm prEN 12791
(2005) and the companys recommendations. Prior to application of the AHR, hands
were washed for 1 min with a neutral soap (Baktolin basic, Bode Chemie) and subungual areas were cleaned as described above. Hands were thoroughly dried using
non-sterile paper, after which Sterillium was rubbed onto hands and forearm for
1.5 min. Hands were sampled as described above and gloved after complete evaporation of Sterillium.

Glove puncture test


All gloves used in this study were collected and tested for the presence of punctures by insufations and visual control.

Results
Preliminary study
A total of 20 sample series per product were obtained. All samples permitted repeated identication of bacterial growth. Considering LSM log10 CFU PHA, no statistical difference was observed
between the two surgeons participating in this trial nor between
the right and left hand. Signicant differences were found between
immediate and sustained activities of the different products tested.
Sterillium was shown to have signicantly lower LSM log10 CFU at
AG compared to both other products. At AHA, PVP had signicantly
higher LSM log10 CFU than Sterillium and CHX, with the latter two
products having comparable activities. LSM and SD values for the
log10 of CFU between the different hand antisepsis methods can
be found in Table 1 and Fig. 1.
Reduction factors for the Sterillium were signicantly greater
than for the other products. Only RF1 was comparable between
Sterillium and CHX. Table 2 and Fig. 2 show the values and SD of
the RFs obtained for the different products.
Surgical study
Considering the results of the preliminary study, PVP scrub was
not included in the surgical trial.
A total of 64 (50 equine, 14 small animals) sample series of Sterillium and 30 (20 equine, 10 small animal) of CHX soap were obtained during the study period. Mean surgery time was 1.5 h. No
signicant differences were found between surgeons regarding

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D.R. Verwilghen et al. / The Veterinary Journal 190 (2011) 372377

Table 1
Least square means of the log10 CFU between the different steps and between the different soap products used in the preliminary study: CHX, 4% chlorhexidine gluconate soap;
PVP, 7.5% povidone iodine soap; Sterillium (45% 2-propanol, 30% 1-propanol, 0.2% mecetronium ethylsulfate). n = 20 for each product.
Step

Product
Chlorhexidine gluconate

PHA
AHA
AG

Povidone iodine

Sterillium

LSM log10 CFU

SD

LSM log10 CFU

SD

LSM log10 CFU

SD

2.262a
0.158a,
0.670a,,

0.059
0.071
0.172

2.223a
1.111b,
0.970b,

0.072
0.175
0.159

2.219a
0.015a,
0c,,

0.053
0.015
0

CFU, colony forming unit; PHA, prior to hand antisepsis; AHA, after hand antisepsis; AG, after 3 h of sterile gloving; LSM, least square means; SD, standard deviation.
Products (rows): values with a different superscript letter are signicantly different. Sampling times (columns):  signicantly different from PHA; signicantly different
from AHA; P 6 0.05.

Fig. 1. Least square means of the log10 CFU between the different steps and
between the different products, Hibiscrub (4% chlorhexidine gluconate), Vetclean
(7.5% povidone iodine), and Sterillium used in the preliminary study. CFU, colony
forming unit; PHA, prior to hand antisepsis; AHA, after hand antisepsis; AG, after
3 h of sterile gloving. LSM, least square means.

Table 2
Least square mean reduction factors (LSM RF) for the different products tested in the
preliminary study.

Fig. 2. Least square mean reduction factors for the different products Hibiscrub,
Vetclean and Sterillium tested in the preliminary study. RF1, reduction factor
between prior to hand antisepsis and after hand antisepsis (immediate effect); RF2,
reduction factor 3 h after wearing sterile gloves (sustained effect). LSM, least square
means.

Table 3
Least square means of the log10 CFU (LSM log10 CFU) between the different steps for
Sterillium (n = 61) and CHX (n = 28) in the surgical study.

Product
Chlorhexidine gluconate
LSM RF
RF1
RF2

2.104a
1.592a,

SD
0.083
0.178

Povidone iodine
LSM RF
1.116b
1.256b

SD
0.177
0.185

Step

Sterillium
LSM RF
2.204a
2.219c

SD
0.051
0.015

RF1, reduction factor between prior to hand antisepsis and after hand antisepsis
(immediate effect); RF2, reduction factor 3 h after wearing sterile gloves (sustained
effect). Products (rows): values with a different superscript letter are signicantly
different. Reduction factor (column):  signicantly different from RF1; P 6 0.05.

LSM log10 CFU after hand antisepsis, neither between RF from samples taken at the small animal vs. the equine theatre. Nevertheless,
the mean CFU level of the PHA samples from small animal
(79.42 63.83) were lower than for equine surgeons (129.2
174.14), although the differences were not statistically signicant.
Four AS Sterillium samples were excluded from statistical analysis because surgeons contaminated their hands by touching objects or themselves while removing gloves and gowns prior to
sampling. One AS sample was excluded from statistical analysis because of the presence of an infected wound at the nail corner of one

PHA
AHA
AS

Sterillium

Chlorhexidine gluconate

LSM log10 CFU

SD

LSM log10 CFU

SD

1.876a
0.048a,
0.018a,

0.21
0.029
0.012

2.123a
0.039a,
0.263b,,

0.129
0.011
0.130

CFU, colony forming units; PHA, prior to hand antisepsis; AHA, after hand antisepsis; AS, after surgery (mean surgery time 1.5 h); LSM, least square means; SD,
standard deviation. Products (rows): values with a different superscript letter are
signicantly different. Sampling times (columns):  signicantly different from PHA,

signicantly different from AHA; P 6 0.05.

of the surgeons creating an extreme growth of Staphylococcus aureus on all ngertips prints on the agar gel. Swabbing and culture
revealed the same bacteria to be present in the wound as the
one cultured on the AS sample. PHA samples were signicantly different from AHA and AS samples for both products. No difference
was observed between AHA and AS samples for Sterillium. Sterillium AS was signicantly different from chlorhexidine gluconate AS.
The RF2 of Sterillium was signicantly higher from RF2 of CHX.
LSM log10 CFU and RF for Sterillium and CHX used in the surgical
set up can be found in Tables 3 and 4 and Figs. 3 and 4.

D.R. Verwilghen et al. / The Veterinary Journal 190 (2011) 372377


Table 4
Least square means reduction factors (LSM RF) for Sterillium (n = 61) and CHX (n = 28)
obtained in the surgical study.
Sterillium
LSM RF
RF1
RF2

2.279
2.343a

375

No statistical relation was found between the presence of glove


puncture and the number of CFUs present on the hand at AS.

Chlorhexidine gluconate
SD
0.074
0.029

LSM RF
a

2.007
1.989b

SD
0.162
0.019

SD, standard deviation. Products (rows): values with a different superscript letter
are signicantly different. Reduction factors (column)  signicantly different from
RF1; P 6 0.05.

Fig. 3. Least square means of the log10 CFU between the different steps for
Sterillium and CHX in the surgical study. CFU, colony forming units; PHA, prior to
hand antisepsis; AHA, after hand antisepsis; AS, after surgery (mean surgery time
1.5 h); LSM, least square means.

Fig. 4. Least square mean reduction factors (LSM RF) for Sterillium and CHX in the
surgical study.

Glove puncture
No punctures were found in gloves used in the preliminary
study (n = 60). Of the 64 gloves used in the surgical study, punctures were found in three gloves (4.7%). Two punctures concerned
the non-dominant hand (one index nger and one middle nger)
and one glove was punctured on the thumb of the dominant hand.

Discussion
This study conrmed that Sterillium was at least as effective in
reducing bacterial counts on hands prior to veterinary surgery as
CHX and PVP. The greater efcacy of an AHS over traditionally used
medicated soaps agreed with the literature (Parienti et al., 2002;
Kampf and Ostermeyer, 2005; Lofer and Kampf, 2008; Tanner
et al., 2008) and, as shown by Parienti et al. (2002), provided better
tolerance and compliance to the surgical hygiene protocol. Despite
this, medicated soaps are still commonly used by veterinary surgeons and have far more disadvantages than commonly accepted
(Kampf, 2008).
The preliminary study revealed that PVP soap was signicantly
less active than Sterillium and CHX, while Sterillium and CHX had
comparable activity. Similarly, Marchetti et al. (2003) showed that
both Sterillium and CHX met the prEN12791 requirements but PVP
did not. However, the sustained effect of Sterillium after 3 h is
markedly better than CHX (Pietsch, 2001; Kampf et al., 2002;
Marchetti et al., 2003), despite an expectation that CHX has a good
residual effect (Pereira et al., 1997), which does not appear to be
correct (Reichel et al., 2008).
The problem with interpreting CHX residual activity is that
insufcient neutralisation will inuence the outcomes (Sheikh,
1981). However, to be comparable with similar studies (Kampf,
2009), a neutralising agent was not added in the current study
and bacteriostatic concentrations of CHX in the Petri plates probably extended beyond the actual exposure time. The low number of
surviving organisms suggested a high activity of CHX which could
not be explained by the efcacy during the exposure time (i.e.,
hand washing) and was more likely related to the tendency of
non-volatile agents, such as CHX, to remain on the plate (Kampf
et al., 2005; Reichel et al., 2008).
Our study conrmed an earlier report (Marchetti et al., 2003)
that PVP is unlikely to be useful in vivo, despite good in vitro activity. There was also no obvious un-sustained activity of PVP (Rotter
et al., 1980). Furthermore, staining and irritation caused by the use
of PVP may limit its clinical use. However, PVP has been reported
to have strong activity against methicillin-resistant Staphylococcus
aureus (MRSA) (Haley et al., 1985; McLure and Gordon, 1992) and
other resistant bacteria (Durani and Leaper, 2008), so may still be
useful as a general antiseptic solution in clinical practice.
As the preliminary testing revealed PVP to be inefcient in vitro,
only Sterillium and CHX were tested during the surgical study. The
in-use test demonstrated a signicantly greater reduction in the
CFU for Sterillium, compared to CHX, by the completion of small
animal or equine surgery ndings that agreed with a similar
study during cardiothoracic surgery (Carro et al., 2007). Moreover,
Sterillium solution had a signicantly better immediate and sustained effect than PVP scrub in the ambulatory surgery theatre of
a tertiary care university hospital (Kac et al., 2009).
The in vivo method used in this study to obtain a CFU count was
similar to previous reported work (Carro et al., 2007; Kac et al.,
2009; Rotter et al., 2009). The method tests the presence of microorganisms on the ngertips, as different surveys have shown the
bacterial burden to be the highest at this location and to reect
general hand contamination (Kampf et al., 2006). Furthermore,
we showed that bacteria will rapidly spread to other ngers once
any nger becomes contaminated (as was illustrated by the wound
on a nger of one of our surgeons). Moreover, transient and infectious ora generally is acquired by touching other people, animals
or contaminated environmental surfaces. Most importantly, surgical glove perforation most often occurs at the ngertips (Tanner,

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D.R. Verwilghen et al. / The Veterinary Journal 190 (2011) 372377

2008). Sampling ngertips can therefore be considered an appropriate method to investigate contamination, particularly when
other valid methods, such a measuring contamination in glove
juice (Nishimura, 2006) or by using the in vitro European EN
12791 test methodology (2005), are not practical for in vivo trials
involving surgery.
The impact of surgical glove perforation on the number of CFUs
was not established in the present study due to the low prevalence
of perforated gloves. Collection of gloves should therefore continue
over a longer period of time to conrm any link between perforation and CFU development and the theory that glove puncture occurs most frequently on the index nger of the non-leading hand
(Dodds et al., 1988; Eklund et al., 2002; Yinusa et al., 2004).
Ideally, the efcacy of hand antisepsis protocols should be performed by trials attempting to measure the impact of hand antisepsis on SSI rates and not on the number of CFUs found on
hands (Tanner et al., 2008). However, the only study performed
to date reported no difference in SSI rates between surgical teams
using a 5 min duration rubbing or scrubbing method when comparing AHR, CHX and PVP (Parienti et al., 2002). More studies are
therefore needed that have SSI as the primary endpoint.
A further consideration in the choice of hand rubbing antisepsis
protocols is that AHR has been reported as having better tolerance
and compliance amongst surgeons after 4 and 14 months of use
(Parienti et al., 2002), which was conrmed in our study.
Alcohol-based hand rubs had never been used in our hospital but
following this study their use has now been implemented and accepted amongst surgeons without any complaints about dermal
tolerance.
Finally, it should be noted that not every alcoholic rub solution
sold over the counter is appropriate for use in surgical hand preparation as they may contain different alcohol concentrations and
should have passed European or American regulatory agencies
testing in that regard.
Conclusions
The alcoholic-based rub used in this study performed better
than disinfecting soaps and was suitable for veterinary surgical
hand disinfection. Alcoholic-based rubs are cheaper, can be
applied more rapidly, have greater skin tolerance and cause less
environmental impact (Cimiotti et al., 2004).
Conict of Interest statement
None of the authors of this paper have a nancial or personal
relationship with other people or organizations that could inappropriately inuence or bias the content of the paper.
Acknowledgements
The authors would like to particularly thank Jean-Noel Duprez
for his assistance in the preparation of the agar plates and technical
aspects of the study. We thank Georg von Schwartzenberg, Mireille
Weber and Rachel Paquai for their assistance in this study and
Susan Atkins, Birgitt Rimell and Maria Silabon for their linguistic
corrections to the manuscript.
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