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EUROPEAN UROLOGY 56 (2009) 865873

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Education

Assessment of Laparoscopic Suturing Skills of Urology


Residents: A Pan-European Study

Stephanie G.C. Kroeze a, Erik K. Mayer a,b,*, Samarth Chopra a, Rajesh Aggarwal b,
Ara Darzi b, Anup Patel a
a
Department of Urology, St Marys Campus, Imperial College Healthcare NHS Trust, London, UK
b
Department of Biosurgery and Surgical Technology, Imperial College London, London, UK

Article info Abstract

Article history: Background: It has been acknowledged that standardised training programmes are needed to
Accepted September 19, 2008 improve laparoscopic training of urologic trainees. Previous studies have suggested that simu-
Published online ahead of lator-based laparoscopic training can improve performance during real laparoscopic procedures.
print on October 1, 2008 Objective: To determine if there are performance differences for the completion of a simulated
laparoscopic suturing task among urology residents based on their postgraduate year of training
(PGY).
Keywords:
Design, setting, and participants: Using a validated scoring checklist, two independent observers
Education objectively scored the completion of a standardised laparoscopic suturing task in a bench-top
Laparoscopy laparoscopic box trainer. PGY and previous exposure to laparoscopic surgery and laparoscopic
Simulation simulated training was obtained from self-administered questionnaires.
Training Data acquisition was undertaken at the European Urological Residents Education Programme
Questionnaire (EUREP) 2007, run by the European School of Urology, and included a pan-European cohort of
201 urology residents.
Measurements: Reliability among those rating the suturing tasks was excellent (Cronbachs
a = 0.83). Each resident was scored for the suturing task. Residents were categorised into three
groups based on their PGY status (junior [n = 8]; intermediate [n = 37]; senior [n = 156]). The
Kruskal-Wallis test was used to measure trend across the PGY; the Mann-Whitney U test was
used to determine variation among categorised PGY groups.
Results and limitations: Laparoscopic suturing skill was signicantly different across PGY levels
( p = 0.032), and between junior residents and both intermediate and senior residents ( p = 0.008
and p = 0.012, respectively). There was no signicant difference between intermediate and senior
residents ( p = 0.697). Only 12% of participants rated their existing volume of laparoscopic operative
cases as sufcient, while 55% of participants had no regular opportunities, and 32% of participants
had not performed laparoscopic procedures as primary surgeon. Most residents (96%) reported the
use of laparoscopic simulators to be benecial in training, although current European training
programmes appear to provide <50% of residents with the opportunity to train with them.
Conclusions: A discernable relationship existed between the score obtained for a laparoscopic
suturing task and year of resident training. Modular simulator training as part of a formal
training programme may help to overcome some of the shortfall in residents exposure to
laparoscopic procedures as primary surgeon.
# 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved.

* Corresponding author. Urology Research Registrar, Department of Biosurgery and Surgical


Technology, 10th Floor QEQM Building, St Marys Hospital Campus, Imperial College London, London,
W2 1NY, United Kingdom. Tel. +44 (0)207 886 1947; Fax: +44 (0)207 886 1546.
E-mail address: e.mayer@imperial.ac.uk (E.K. Mayer).

0302-2838/$ see back matter # 2008 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.eururo.2008.09.045
866 EUROPEAN UROLOGY 56 (2009) 865873

1. Introduction several ways with checklists that also subdivide the task or
validate measures such as time or path length [1618].
Ever since the first laparoscopic nephrectomy was per- For several years it has been acknowledged that the
formed [1], laparoscopic urologic surgery has played an laparoscopic training of urologic trainees needs to be
increasingly important role in urology and is one of the improved and that better access to this training is needed
most rapidly expanding subspecialties. At present, the [19]. Therefore, this study aimed to investigate the standard
availability of laparoscopically experienced urologists of a laparoscopic suturing task performed by urology
throughout Europe is insufficient to meet the increasing residents across Europe and to compare it with the
demand and application of laparoscopic procedures. residents year of training. The study also sought to gain
Laparoscopic surgeons need to acquire very different skills insight into current exposure of urology residents to
than those needed for open surgery, and many of the laparoscopic procedures and laparoscopic simulators so
procedures have a significant learning curve. There is that this information could be used to guide future
therefore recognition of the need for a more formalised development of structured laparoscopic training pro-
laparoscopic training framework within urology. grammes.
In recent years it has become clear that the traditional
system of surgical education might not be ideal for teaching 2. Methods
laparoscopy, mainly due to a prolonged learning curve from
the inherent difficulties of the minimally invasive approach: 2.1. Subjects
two-dimensional vision, lack of depth perception, and
counterintuitive movements as a result of the fulcrum This study was conducted during the laparoscopic hands-on training
effect [2]. A complicating factor of urologic laparoscopic (HOT) portion of the European Urological Residents Education Pro-
training within the operating theatre is that there is no gramme (EUREP) meeting 2007, EUREP is organised by the European
simple high-volume procedure suitable for training akin School of Urology (ESU) in collaboration with the European Board of
to laparoscopic cholecystectomy in general surgery. Urology and has been developed exclusively for all European urologic
There is a view that laparoscopic skill acquisition should residents. All participating residents who had signed up for the HOT
were considered eligible to be included in the study, and inclusion was
be undertaken in a skills laboratory before being transferred
entirely voluntary. The study protocol was explained to all subjects, and
to the operating theatre [3] and that simulation training can
informed consent was obtained prior to participation in the study.
improve resident operative performance [4,5]. Laparoscopic
training options developed over the years vary from bench-
2.2. Task
top training courses with box trainers to virtual reality
simulators (dry-lab training) or live-animal models Residents were assessed on their ability to complete a standardised
(wet-lab training). Most of these courses have not been laparoscopic suturing task consisting of the placement and tying of a
designed from a scientific background, and until now, there single laparoscopic suture with three throws to oppose an iatrogenic
has been no consensus for a standardised training wound on articial tissue (Professional Skin Pad Mk 2, Limbs and Things,
programme [6]. To obtain adequate training globally, an Bristol, UK) within a laparoscopic box trainer environment (Pop-up
efficient, validated, and standardised teaching framework Trainer, Simulab Corporation, Seattle, WA, USA) (Fig. 1). To ensure
needs to be developed. standardisation of the task, all residents used identical standard
One of the initial steps towards developing such a laparoscopic instruments (hand instruments and needle holders
HiQ+, Olympus, Hamburg, Germany), suture material (Sal 2-0, B.
framework is the ability to objectively assess laparoscopic
Braun Medical Ltd, Shefeld, UK), ergonomic conditions, and a xed
skills of trainees. Aggarwal et al [7] and others [8,9] have
camera position. Premarked spots were placed at entry and exit points
started to look at the validity of the varying training
on the tissue model. Residents, as part of the HOT course, underwent a
equipment and the creation of an objective assessment of period of tutor-led laparoscopic training in groups of three (each resident
laparoscopic skills. Laparoscopic simulators have proven to trained rst for 20 min). At the end of this period, residents were asked to
be an excellent medium for this assessment, and it has been complete the assigned task with no external assistance. Time allowance
shown that basic skills can be taught and assessed well in for suturing task performance was 10 min in order to limit the
simple, inexpensive box trainers [10,11]. Importantly, proof frustrations of laparoscopically inexperienced junior residents [5].
of transfer validity from simulators to real life has been
reported by several researchers [12,13]. 2.3. Measurement tool
Laparoscopic suturing and knot tying is a potentially
difficult task that requires good handeye coordination and Each assigned task was recorded by digital video and saved for later
intensive practice. As in open surgery, it is a necessary skill evaluation. Each task was coded with the EUREP participation number;
the observers were therefore blinded to the residents identity.
for many laparoscopic procedures. It also acts as a useful
Qualitative analysis of the videoed task was performed by two
benchmark when assessing laparoscopic skills because
independent observers (SK, SC), urology trainees who have been
good-quality knots can be taught in a short space of time to
formally trained in the use of the objective checklist. The process of
both junior and senior trainees [14]. A complex laparoscopic scoring videotaped tasks has been established previously [14,18]. A
task can be subdivided into all necessary steps to teach and laparoscopic knot was dened according to the gold standard as
assess this task adequately. An example of this is the developed after discussion with expert surgeons and as described point
technique of endoscopic extraperitoneal radical prostatect- by point in a previously constructed, validated checklist (Fig. 2) [14,18].
omy (EERPE) [15]. Laparoscopic suturing can be assessed in The checklist scored technical features of the task such as needle position
EUROPEAN UROLOGY 56 (2009) 865873 867

Fig. 1 Training set-up showing the four stages of the simulated laparoscopic task: (A) needle loading and driving; (B) pulling the suture through; (C) knot
technique; and (D) knot quality.

and driving, pulling through of the suture, and the technique and quality for trend across the PGY, and the Mann-Whitney U test was used for
of the knots. After all of the tasks had been scored, a matching process variation between PGY groups. A p value <0.05 was deemed signicant.
was undertaken to correlate information obtained from the question- The interrater reliability for the two observers was dened using
naires. Cronbachs a test.
Residents were subdivided into three groups based on their PGY;
2.4. Questionnaire junior (PGY 1 and PGY 2), intermediate (PGY 3 and PGY 4), and senior
(PGY 5 and PGY 6).
Each resident was asked to complete a self-assessment questionnaire
which was collected at the beginning of the course. This questionnaire 3. Results
aimed to determine the current and previous laparoscopic exposure
during training, and contained three sections important for this study
Two hundred and one European urology residents present
(Fig. 3). The rst section concerned postgraduate year of training
at the EUREP 2007 laparoscopic HOT course were recruited
(PGY) dened as year of resident or, where applicable, specialist
registrar training. The second section covered laparoscopic simulation
for this study. All performed the laparoscopic task in the
exposure: the opportunities for use of laparoscopic simulation in prescribed manner and completed the questionnaire.
current training and the interest in training with laparoscopic Participants were mainly senior residents (79%), 37 were
simulation (marked on a Likert scale from 1 = not useful to 5 = very intermediate (18%), and 8 were junior (4%).
useful). The third section was concerned with laparoscopic operative The interrater reliability for the two observers scoring
experience, that is, at what stage of training the rst laparoscopic the task checklist was excellent with Cronbachs a = 0.83.
procedure was performed as primary surgeon, the amount of There was a significant difference with regard to laparo-
laparoscopic training per month, and the rating of volume of scopic suturing skill across PGY level (Kruskal-Wallis
laparoscopic versus open procedures.
p = 0.032). With regard to these individual groups there
was a significant difference in score between junior
2.5. Outcome measures
residents (median score: 10.5/29) and intermediate resi-
dents (median score: 14/29) ( p = 0.008). The performance
The primary end point was to determine whether a relationship existed
between junior and senior residents (median score: 13/29)
between laparoscopic suturing skill (as assessed by objectively scoring a
standardised laparoscopic task) and the PGY of urology residents. The
also showed a significant difference ( p = 0.012). However,
secondary end point was to explore the previous laparoscopic there was no significant difference between the intermedi-
experience of residents and to gain insight into their views on the use ate and senior residents ( p = 0.697) (Fig. 4).
of laparoscopic simulators as part of training. With regard to the time needed to complete the
laparoscopic suturing task, 42 participants (21%) were
2.6. Statistical analysis unable to complete this task within the allotted 10 min.
There was no significant difference regarding time to
Statistical analysis was performed using SPSS v.14.0 (SPSS, Chicago, IL, complete the task between the groups (Kruskal-Wallis
USA). Nonparametric data were analysed using the Kruskal-Wallis test p = 0.393).
868 EUROPEAN UROLOGY 56 (2009) 865873

Fig. 2 Twenty-nine-point scoring checklist used for assessing performance of standardised laparoscopic suturing task.

Questionnaire responses regarding laparoscopic simula- scopic simulators was beneficial in training, 96% (189/196)
tion experience revealed that 81% (162/200) of residents thought it would be useful (Likert score 3, 4, and 5). The
had seen a laparoscopic simulator and 96% (191/198) were percentage of residents performing their first laparoscopic
interested in training with it (Fig. 5a). Despite this procedure as primary surgeon occurred with equal fre-
enthusiasm for laparoscopic simulators, the current train- quency in each PGY (ranging from 9% to 13% for each PGY).
ing programmes across Europe afford just 41% (79/193) of Thirty-two percent of residents (56/176) said that they had
the residents with an opportunity to train with simulators not yet performed a laparoscopic procedure as primary
and, on average, only 56% (108/192) had used one (Fig. 5b). surgeon, and 55% of residents (98/178) said that they had no
Residents who had previously used a simulator or had the regular opportunities to perform laparoscopic procedures
opportunity to train with simulators in their training as primary surgeon. When asked to rate the volume of open
curriculum performed significantly better than the group versus laparoscopic operative cases, 56% (107/192) of the
that had not ( p = 0.002 and p = 0.037, Mann-Whitney U residents found that the volume of open operative cases was
test). This correlation transcends residency training level. In enough (Likert 3, 4 and 5) while only 12% (23/189) thought
response to whether residents thought the use of laparo- the same about laparoscopic operative cases. There was no
EUROPEAN UROLOGY 56 (2009) 865873 869

Fig. 3 Resident Experience Questionnaire (European Urological Residents Education Programme [EUREP]) 2007.

significant difference between the PGY in which the first 4. Discussion


laparoscopic operation as a primary surgeon was performed
and the final score in the suturing task (Kruskal Wallis, This study has shown that there was a significant difference
p = 0.15). in performance of a laparoscopic suturing task between
junior and more experienced urology residents. The
significant improvement in this task between junior and
intermediate residents suggests that much of the laparo-
scopic learning curve occurs early in the residents training.
This was partly reflected by the questionnaire responses,
which identified that 25% of residents performed their first
primary surgeon laparoscopic procedure as a junior
resident. The improvement in this task, however, seemed
to plateau when comparing the intermediate with the
senior group, for which there are two possible explanations.
First, it is possible that residents develop such a high level of
laparoscopic skill in their junior and intermediate years that
there is little room for improvement in senior years. Second,
supported by low-level scoring of the senior group, it could
be that senior residents show little improvement because of
Fig. 4 Box plot showing checklist scores of the laparoscopic assessment. limitations with laparoscopic training in existing training
The maximum score was 29; higher scores indicated better results. There programmes. These results suggest that all groups need
was a significant difference in performance between postgraduate years
(PGYs) 1 and 2 and PGYs 3 and 4 ( p = 0.008) and between PGYs 1 and 2 improvement in performance of the laparoscopic task. How
and PGYs 5 and 6 ( p = 0.012). much improvement in the score that is necessary to
870 EUROPEAN UROLOGY 56 (2009) 865873

Fig. 5 (a) Percentage of urology residents who had ever seen and/or had an interest in laparoscopic simulators. (b) Percentage of urology residents who
had ever used and/or had the opportunity to train with laparoscopic simulators in their current training programmes.

determine competent completion of training needs to be residents afforded the opportunity to use them in their
determined by future studies that include laparoscopic training programmes.
suturing experts. Along with other studies [5,12], our results suggest that
Time has been used as objective measure for assessing simulators may improve laparoscopic skills; residents that
laparoscopic suturing skills. Opinions differ with regard had used or had the opportunity to regularly train with a
to whether time is a good indicator of skill [12,17,18]. In simulator performed significantly better on the laparo-
our study, time taken to complete the task did not scopic suturing task. However, there needs to be a degree of
significantly improve with seniority and, therefore, was caution in this observation as the objective performance
not sensitive enough to detect skill differences among scores were compared with subjective questionnaire
years of training. responses. A laparoscopic simulator in this study is defined
The questionnaires were used to determine residents as any simulator that can be used to train laparoscopic
previous exposure to laparoscopic operating and laparo- skills, from box trainers to virtual reality simulation.
scopic simulators and their views on the role of laparoscopic Although virtual reality seems to be superior to box trainers
simulation in urology training programmes. One-third of all for acquiring good performance on complex operations,
participating residents had never performed a laparoscopic several studies have shown that basic laparoscopic skills
procedure as primary surgeon, and more than half of the can be acquired equally well with box trainers as with
residents had no opportunity to perform laparoscopic virtual reality simulators [10,20,21].
procedures as a primary surgeon on a regular basis. A limitation of this study is that the residents attending
Furthermore, only 12% of residents were satisfied with the hands-on laparoscopic course at the EUREP 2007 are a
the current volume of laparoscopic procedures that they self-selecting group, already having a special interest in
performed in their training. As 78% of all participants were laparoscopy or attending because they are curious about
senior residents, these results would suggest that laparo- their laparoscopic performance. This may explain the high
scopic training in existing curricula was suboptimal. degree of favourable responses for interest in and useful-
There was evidence to suggest that use of laparoscopic ness of laparoscopic simulators. Because this group of
simulation was increasing, with 81% of residents having residents with a special interest in laparoscopy only receive
seen a laparoscopic simulator and 56% of residents having limited opportunities for laparoscopic skills training, it
actually used one. This notification is reenforced by the could be argued that current laparoscopic training is
questionnaire because just 24% performed their first therefore far from adequate. Sampling a random group of
laparoscopic procedure as primary surgeon without having urology residents would help to answer these questions but
used a simulator. Although there was a great degree of was not possible on this occasion due to the setting of this
interest in simulators and the vast majority of residents study.
believed them to have a role in laparoscopic training, they Although a single laparoscopic suturing task cannot be
appeared not to be commonplace, with only 41% of used solely as a proxy indication for overall laparoscopic
EUROPEAN UROLOGY 56 (2009) 865873 871

skill, it is a necessary skill required during many laparo- overcome some of the shortfall in European urology
scopic procedures and acts as a useful benchmark task [14]. residents exposure to laparoscopic procedures as primary
The objective assessment of laparoscopic skills based on surgeon.
experience is known as construct validity. Validity of
laparoscopic suturing can be assessed in several ways, such Author contributions: Erik Mayer had full access to all the data in the study
as described by Van Sickle et al [16,17]. We used a checklist and takes responsibility for the integrity of the data and the accuracy of the
that already proved construct validity in two previous data analysis.
studies [14,18] and allowed us to objectively assess this
Study concept and design: Kroeze, Mayer, Aggarwal, Darzi, Patel.
task. There is construct validity in terms of checklist score
Acquisition of data: Kroeze, Chopra.
compared with year of residency training for our study.
Analysis and interpretation of data: Kroeze, Mayer, Aggarwal.
Development of objective measures for other laparoscopic Drafting of the manuscript: Kroeze, Mayer, Aggarwal, Patel.
tasks may highlight further performance differences across Critical revision of the manuscript for important intellectual content: Darzi,
years of training. Patel.
A further limitation is the lower number of junior and Statistical analysis: Kroeze, Mayer, Aggarwal.
intermediate residents compared with the higher number Obtaining funding: Patel.
of senior residents, since the EUREP programme was Administrative, technical, or material support: None.
primarily targeted to senior urology residents. It should Supervision: Darzi Patel.
be noted, however, that previous studies in this area had Other (specify): None.

much smaller numbers of total participants, with only 612


Financial disclosures: I certify that all conicts of interest, including
people in each experience category [14,22]. Furthermore,
specic nancial interests and relationships and afliations relevant to
this is the first study evaluating laparoscopic suturing skills the subject matter or materials discussed in the manuscript (eg,
with such a large number of residents, but it is also employment/afliation, grants or funding, consultancies, honoraria,
representative of such variability across training curricula. stock ownership or options, expert testimony, royalties, or patents led,
The scoring checklist was limited by the absence of an received, or pending), are the following: None.
objective measure of knot strength as an indicator of knot
Funding/Support and Role of the Sponsor: Olympus kindly supported the
quality. This has been described previously by Hanna et al as
project with the loan of workstations, laparoscopic equipment, and
part of a knot quality score, which uses a tensiometre to test
recording equipment and with logistics as well as with an unrestricted
knot strength [23]. The use of a tensiometre in this study educational grant to the ESU for support of the EUREP.
was not feasible due to the timing schedule of the HOT
session, and we were therefore limited to defining knot Acknowledgment statement: The authors acknowledge the ESU and
quality visually by assessing whether all knots were EUREP organisers for allowing us to conduct this study during EUREP
squared, not too tight or too loose, and not laid over the 2007 and the training faculty for their assistance with the collection of
incision. the data.
Currently, general opinion of urology training implies
that because of a changing surgical environment, residents
lack the opportunities to train in laparoscopic procedures
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Editorial Comment on: Assessment of Laparoscopic concerning; for instance, only 12% reported sufficient
Suturing Skills of Urology Residents: A Pan-European volumes of laparoscopy in training and only 32% reported
Study that they performed laparoscopic cases as primary
Matthew T. Gettman surgeon. Furthermore, <50% of residents had an oppor-
Department of Urology, Mayo Clinic, Rochester, Minnesota, tunity to train on simulators to refine laparoscopic skills.
USA Acquisition of surgical skills in the 21st century should
Gettman.Matthew@mayo.edu not follow the traditional teachings of Halsted [24]. Since
laparoscopy is performed using monitors and trocars, the
In the era of minimally invasive surgery, efforts to approach is easily adapted to simulation. This concept
improve technical skills training among urology residents is supported by urology residents and even program
are sorely needed. Indeed, the current manuscript by directors, yet many hurdles exist [15]. Dissemination of a
Kroeze and colleagues highlights a number of interesting standardized, proficiency-based curriculum may be the
observations regarding the current status of laparoscopic goal, but issues of simulator development, device realism,
skills training for urology residents in Europe [1]. In the training validation, and added training costs must be
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Urol 2005;47:34651. DOI: 10.1016/j.eururo.2008.09.046
[5] Le CQ, Lightner DJ, VanderLei L, Segura JW, Gettman MT.
The current role of medical simulation in American urological DOI of original article: 10.1016/j.eururo.2008.09.045

Editorial Comment on: Assessment of Laparoscopic resources, especially in developing countries. Nevertheless,
Suturing Skills of Urology Residents: A Pan-European low-cost alternative lab models can be used with good
Study results in terms of skills improvement [4].
Antonio Galfano One last point is the real transferability of the technical
Department of Surgical and Oncological Sciences, skills acquired through a lab model to the surgical patient.
Urology Clinic University of Padua, via Giustiniani, 2, Even though transfer validity from lab models to the
35100 Padova, Italy operating room has already been demonstrated [5], virtual
antoniogalfano@gmail.com training must be considered only the first step of a surgical
learning curve that should begin as soon as possible during
The European Urological Residents Education Pro- the residency year, before learning skills, visual memory,
gramme (EUREP) is a noteworthy occasion of learning and psychomotor performances drop down [6].
for European residents, with the top experts in virtually all
urologic fields available as teachers. The introduction of
the hands-on training programme provided a further
improvement in the usefulness of this event, giving a References
practical cut to the course, although with a lab model. The
[1] Kroeze SGC, Mayer EK, Chopra S, Aggarwal R, Darzi A, Patel A.
authors of this study [1] should be applauded for the idea
Assessment of laparoscopic suturing skills of urology residents: a
of further transforming this educational event into an
pan-European study. Eur Urol 2009;56:86573.
occasion for evaluating the practical skills provided by [2] Schout BMA, Hendrikx AJM, Scherpbier AJJA, Bemelmans BLH.
European urology schools to residents. Update on training models in endourology: a qualitative systema-
Different training models have already been proposed tic review of the literature between January 1980 and April 2008.
for teaching endoscopic, endourologic [2], and laparo- Eur Urol 2008;54:124761.
scopic skills, but no standardised global consensus has yet [3] Kommu SS, Dickinson AJ, Rane A. Optimizing outcomes in laparo-
been reached concerning optimised outcomes to be scopic urologic training: toward a standardized global consensus.
achieved during laparoscopic training [3]. J Endourol 2007;21:37885.
[4] Chandrasekera SK, Donohue JF, Orley D, et al. Basic laparoscopic
Considering the timely and fashionable widespread
surgical training: examination of a low-cost alternative. Eur Urol
attraction exerted by laparoscopy in urology, it is not
2006;50:128591.
surprising that 96% of residents are interested in training on
[5] Sugiono M, Teber D, Anghel G, et al. Assessing the predictive validity
a laparoscopic simulator. In contrast, it is disappointing that and efcacy of a multimodal training programme for laparoscopic
only 41% of them had had the opportunity to use a radical prostatectomy (LRP). Eur Urol 2007;51:133240.
laparoscopic simulator during the course of residency [1]. [6] Boom-Saad Z, Langenecker SA, Bieliauskas LA, et al. Surgeons
Moreover, most of the residents reported having few or outperform normative controls on neuropsychologic tests, but
insufficient skills in laparoscopic models, even in the final age-related decay of skills persists. Am J Surg 2008;195:2059.
years of residency. This admission shows that, too often,
residents programmes suffer from a limited use of
DOI: 10.1016/j.eururo.2008.09.047
constantly updated surgical programmes. A possible
explanation for this problem might be limited economic DOI of original article: 10.1016/j.eururo.2008.09.045

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