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Total mesorectal excision: a comparison of oncologicaland functional outcomes between robotic and laparoscopicsurgery for rectal cancer
Annibale D’Annibale • Graziano Pernazza •
Igor Monsellato • Vito Pende • Giorgio Lucandri •
Paolo Mazzocchi • Giovanni Alfano
Received: 22 July 2012 / Accepted: 4 December 2012
� Springer Science+Business Media New York 2012
Abstract
Background Long-term data from the CLASICC study
demonstrated the oncologic equivalence of laparoscopic and
open rectal cancer surgery despite an increased circumfer-
ential resection margin involvement in the laparoscopic group
in the initial report. Moreover, laparoscopic total mesorectal
excision (TME) may be associated with increased rates of
male sexual dysfunction compared to conventional open
TME. Robotic surgery could potentially obtain better results
than laparoscopy. The aim of this study was to compare the
clinical and functional outcomes of robotic and laparoscopic
surgery in a single-center experience.
Methods This study was based on 100 patients who
underwent minimally invasive anterior rectal resection with
TME. Fifty consecutive robotic rectal anterior resections
with TME (R-TME) were compared to the first 50 consec-
utive laparoscopic rectal resections with TME (L-TME).
Results Median operative time was 270 min in R-TME
and 275 min in L-TME. No conversions occurred in the
R-TME group whereas six conversions occurred in the
L-TME group. The mean number of harvested lymph
nodes was 16.5 ± 7.1 for R-TME and 13.8 ± 6.7 for
L-TME. The circumferential margin (CRM) was\2 mm in
six L-TME patients, whereas no one in R-TME group had a
CRM \2 mm. The International Prostate Symptom Score
(IPSS) scores were significantly increased 1 month after
surgery in both the L-TME and R-TME groups, but they
normalized 1 year after surgery. Erectile function wors-
ened significantly 1 month after surgery in both the groups
but it was restored completely 1 year after surgery in the
R-TME group and partially in the L-TME group.
Conclusions Robotic TME is oncologically safe and
adequate for rectal cancer treatment, showing better results
than laparoscopic TME in terms of CRM, conversions, and
hospital length of stay. Better recovery in voiding and
sexual function is achieved with the robotic technique.
Keywords Robotic rectal anterior resection �Laparoscopy � TME � Rectal cancer � Robotic surgery �Functional results
Laparoscopic surgery for rectal cancer has been proven to be
safe and effective, with a short hospital stay and reduced
postoperative pain. Long-term data from the CLASICC
study demonstrated the oncological equivalence of laparo-
scopic and open rectal cancer surgery despite an increased
circumferential resection margin (CRM) involvement in the
laparoscopic group in the initial report [1]. Moreover, lapa-
roscopic total mesorectal excision (L-TME) may be associ-
ated with increased rates of male sexual dysfunction
compared to those of conventional open TME [2]. Robotic
surgery offers several advantages compared to laparoscopy,
such as better dexterity of movement, 3D and magnified
vision, and tremor filtering [3–6]. These features are partic-
ularly enhanced when working in a narrow space like the
pelvis. Robotic surgery could potentially yield results
superior to those of laparoscopy. The aim of this study was to
compare the clinical and functional outcomes of robotic and
laparoscopic surgery in a single-center experience.
Presented at the 20th EAES Congress, June 20–23, 2012, Brussels,
Belgium.
A. D’Annibale � G. Pernazza (&) � I. Monsellato � V. Pende �G. Lucandri � P. Mazzocchi � G. Alfano
Minimally Invasive and Robotic Surgery Unit, San Giovanni
Addolorata Hospital, Via dell’Amba Aradam 9, Rome, Italy
e-mail: [email protected]
I. Monsellato
e-mail: [email protected]
123
Surg Endosc
DOI 10.1007/s00464-012-2731-4
and Other Interventional Techniques
Materials and methods
This is a retrospective study on a prospectively collected
database that included data of 100 patients who underwent
minimally invasive anterior rectal resection with total
mesorectal excision. Fifty consecutive robotic rectal ante-
rior resections with TME (R-TME) were compared to the
first 50 consecutive laparoscopic rectal resections with
TME (L-TME) from the 245 patients who underwent
minimally invasive TME performed from 2004 to 2012.
Robotic procedures were performed from 2006 to 2012.
Preoperative evaluation included colonoscopy with biopsy,
transrectal ultrasonography (US), total-body computed
tomography, and pelvic magnetic resonance imaging
(MRI). Informed consent was obtained from all patients for
robotic and laparoscopic procedures. For locally advance
disease (clinical stage T3 N0 or any T N1-2), confirmed by
MRI and US, neoadjuvant chemoradiation (continuous
5-FU infusion/RT) was considered. Body mass index, age,
ASA score, operative time, conversions, length of stay
(LOS), morbidity, time to resumption of oral diet, and
preoperative and postoperative urinary and sexual function
evaluation were analyzed for both procedures. Pathological
data included pathological stage, number of harvested
lymph nodes, and status of circumferential and longitudinal
margins. International Prostate Symptoms Score (IPSS)
and International Index of Erectile Function (IIEF) ques-
tionnaires were used to analyze urinary and sexual dys-
function, respectively. All evaluations were done
voluntarily by the patients before and after surgery. The
questionnaires were administered preoperatively and 1 and
12 months after surgery.
Surgical technique
Both techniques were performed by a surgeon well trained
in minimally invasive surgery. We used a four-arm da
Vinci� S-HD Surgical System (Intuitive Surgical, Sunny-
vale, CA) with a three-arm configuration and a five-port
technique. Port and patient positions are shown in Fig. 1.
The technique used was the single-step, double-field (lat-
eral and pelvic fields), full robotic technique. The robotic
cart is positioned on the patient’s left side along the
imaginary line between the anterosuperior iliac spine and
the umbilical scar, at a 60� angle (Fig. 2). Robotic arm #2
was changed from R2 to A0 for pelvic dissection (Fig. 2B).
Fig. 1 Ports and patient positions. C camera port, R1 robotic arm #1, R2 robotic arm #2, A assistant port, A0, assistant port–robotic port #3; ASS2nd assistant surgeon, OPR 1st assistant surgeon, SCN scrub nurse, IMV inferior mesenteric vein, IMA inferior mesenteric artery
Surg Endosc
123
For laparoscopic surgery we used a four-port technique.
A periumbilical 12-mm port (C) was placed for the endo-
scope and 5 and 10/12-mm ports were inserted in the right
hypochondrium and right iliac fossa, respectively. A fourth
5-mm port was inserted in the left flank for occasional help
on flexure takedown and systematic help during pelvic
dissection.
Surgical procedure
Dissection was carried out in the same way in both the
robotic procedure and the laparoscopic procedure. The
inferior mesenteric vein was identified at the level of
the inferior margin of the pancreas and divided between clips
or by linear stapler. A complete takedown of the splenic
flexure was achieved by medial-to-lateral coloepiploic
detachment and dividing the phrenocolic ligament along the
inferior margin of the tail of the pancreas once the left
colonic flexure was completely freed from the epiploon. The
right aspect of the pelvic peritoneal sheet was incised,
starting from approximately the level of the sacral promon-
tory to the previously dissected area, overexposing the pre-
aortic plane and the origin of the inferior mesenteric artery
(IMA), which was divided by stapler or between clips.
TME usually has three main fields of dissection. The
procedure consists of a combination of these steps, but we
standardized the approach by starting with the posterior
dissection, then the anterior, and, lastly, the lateral one.
Posterior dissection began at the level of the promon-
tory, along the virtual space between the mesorectal fascia,
anteriorly, and the presacral fascia (Waldeyer’s fascia),
posteriorly. The hypogastric nerves (HNs), which lie pos-
teriorly, then laterally to reach the inferior hypogastric
plexus (IHP) [7], were identified and preserved. The rec-
tosacral ligament, usually placed at the level of the fourth
sacral vertebra, was divided in order to better mobilize the
rectum and to access the inferior part of the retrorectal
space in case of lower tumor localization [8, 9].
Anterior dissection started with the incision of the
anterior peritoneal brim and continued over the plane of
Denonvilliers’ fascia, which was sectioned at the level of
the lower margin of the seminal vesicles in order to pre-
serve rectoprostatic blood vessels and branches of the
cavernous nerves (Fig. 3) [10, 11].
In the lateral dissection, the rectum was retracted
medially on both sides, increasing the distance between the
specimen and the lateral pelvic wall. The dissection con-
tinued until the lateral ligaments of the rectum were
reached [12, 13]. The rectum was then quite distant from
the pelvic wall, allowing us to dissect only those branches
deputed to the rectum, thus preserving the IHP.
Statistical analysis
The software used for statistical analysis was SPSS Statistics
v17 (SPSS Inc., Chicago, IL, USA). Mean ± standard
deviation (SD), median, and interquartile range (IQR) for
appropriate variables were calculated. Student’s t test
was used to analyze the differences between the two groups
(L-TME vs. R-TME). The paired t test was used to compare
Fig. 2 Robotic cart position and robotic arms’ configuration during the whole procedure
Surg Endosc
123
postoperative urogenital and sexual functions in both groups
to the preoperative functions. Fisher’s exact test was used for
categorical data (e.g., age, sex, tumor location, T and N stage,
and radiation therapy). The cusum method was used to
analyze the learning curve for robotic procedures. A
p \ 0.05 was considered statistically significant.
Results
There were no statistically significant differences in terms of
age, gender distribution, nodal (N) stage of the resected
specimens, and radiation therapy between the two groups
(Table 1). Median operative time was 270 (240–315) min in
R-TME and 275 (240–335) min in L-TME (p = 0.958). No
conversions occurred in the R-TME group, whereas six con-
versions occurred in the L-TME group (p = 0.011). Median
specimen length was 23 (18.5–27.5) cm for R-TME and 21
(16–26) cm for L-TME (p = 0.202). Mean number of har-
vested lymph nodes was 16.5 ± 7.1 for R-TME and
13.8 ± 6.7 for L-TME (p = 0.053). Circumferential margins
(CRM) were\2 mminsix patients for L-TME versusnone for
R-TME (p = 0.022). Mean longitudinal distal margin (DRM)
was 3 ± 1.1 cm for R-TME and 3 ± 1.6 cm for L-TME
(p = 0.908). Median hospital stay was 8 (7–11) days for
R-TME and 10 (8–14) days for L-TME (p = 0.034), time to
resumption of oral diet was 3 (3–5) days for R-TME and 5
(4–6) days for L-TME (p = 0.005). Surgery-related morbid-
ity was 10 % (5/50) for R-TME and 22 % (11/50) for L-TME
(p = 0.104). There were five anastomotic leakages in the
robotic group, which were conservatively treated. In the lap-
aroscopic group, seven anastomotic leakages, two pulmonary
infections, and one wound infection (minilaparotomy)
occurred; three anastomotic leakages required reintervention
and the other four leakages were treated conservatively. No
intraoperative or 30-day mortality occurred in either group
(Table 2). The analysis of the learning curve (LC) for the
robotic procedure showed a decreasing trend in mean oper-
ating time from 312.50 min in the first 25 procedures to
Fig. 3 Intraoperative view:
anterior dissection. Incision of
Denonvilliers’ fascia at the level
of the seminal vesicles. Asteriskseminal vesicles,
D Denonvilliers’ fascia
Table 1 Patients’ demographics and clinicopathological features
L-TME
(n = 50)
R-TME
(n = 50)
p
Age 65.72 ± 11.6 66 ± 12.1 0.88
Sex 1
Male 30 30
Female 20 20
Tumor location
Upper rectum 21 8 0.008
Middle rectum 12 9 0.62
Lower rectum 17 33 0.003
Tumor stage
pT0 5 11 0.17
pT1 10 2 0.03
pT2 14 14 1
pT3 17 20 0.68
pT4 4 3 1
Nodal stage
pN0 35 35 1
pN1 10 8 0.8
pN2 5 7 0.76
Neoadjuvant
radiotherapy
28 34 0.30
Surg Endosc
123
238.18 min in the last 10 procedures (p = 0.002), whereas in
the laparoscopic group this trend was not clearly found
(Figs. 4, 5). The analysis of urinary and sexual dysfunction
was conducted on 30 male patients for both L-TME and
R-TME groups. IPSS scores were significantly increased
1 month after surgery in both the L-TME and R-TME groups
(7.08 ± 3.5 and 6.71 ± 5.9, p = 0.012, respectively), but
they normalized 1 year after surgery (4.2 ± 2.3 and 3.53 ±
2.5, p = 0.06, respectively) (Table 2).
Erectile function was significantly worse 1 month after
surgery in both groups (p = 0.001), but it was restored
completely 1 year after surgery in the R-TME group
(p = 0.066) and partially in the L-TME group (p = 0.048)
(Table 2).
Discussion
Ten years after the first procedure, L-TME has gained
wider acceptance as oncologically adequate treatment for
rectal cancer. Based on the 5-year results of the CLASICC
trial, L-TME seems to be comparable to open surgery with
respect to CRM positivity rates (9.4 vs. 7.6 % for open),
anastomotic leakage rates (6–18 %), conversion rates
(1–34 %), and oncological outcomes [1]. Laparoscopic
surgery, however, is difficult to perform in a narrow and
deep space such as the pelvic cavity and demands a high
level of experience and has a significant learning curve
[14–21]. The main concerns about laparoscopic techniques
are poor dexterity and rigidity of the instruments, the 2D
view, and camera stability depending on the assistant’s
skill level [22, 23].
Robot-assisted surgery may overcome some of these
limitations as it provides a stable, high-definition, 3D
image, a finer dissection with articulated tools, and better
ergonomics for the surgeon. All these aspects may con-
tribute to improved oncological adequacy and nerve pres-
ervation in TME.
There are two key points in rectal surgery: oncological
adequacy of the specimen and nerve-sparing technique.
Local recurrence has been the most common and major
morbidity in patients with rectal cancer. TME was developed
to reduce local recurrences and improve overall survival
while maintaining an adequate quality of life. The quality of
the specimen is considered a parameter for the evaluation of
prognosis [24]. The integrity of the mesorectum and clear
CRM and DRM are important oncological and surgical end
points [25–29]. CRM\1 mm is predictive of an increased
risk of distant metastases and shorter survival, while
CRM \2 mm is predictive of increased local recurrence
[30, 31]. Recent studies suggested a DRM of at least 2 cm as
a therapeutic goal [27, 32, 33]. In this study, the difference
for CRM involvement (\2 mm) between the two groups was
statistically significant. Robot-assisted surgery allowed us to
achieve a complete and oncologically adequate resection of
the specimen without CRM involvement compared to the
laparoscopic group (p = 0.022). Despite that CRM
involvement could have depended on the pathology site and
extension, we feel that the articulation of the instruments and
the 3D magnified vision may have influenced these results.
Moreover, the difference between the direction and strength
of the applied tractions by the robotic instruments and those
of the conventional laparoscopic instruments could be a
factor influencing the quality of the specimen and, typically,
the mesorectal fascia integrity. No difference in DRM
(p = 0.908), specimen length (p = 0.202), and number of
harvested lymph nodes (p = 0.073) was found between the
two groups, even though the mean number of retrieved
lymph nodes was higher in the robotic group. DRM length
Table 2 Perioperative, postoperative, pathological, and functional
results
L-TME (n = 50) R-TME (n = 50) p
Operative timea 280 (240–350) 270 (240–315) 0.863
Specimen lengtha 21 (16–26) 23 (18.5–27.5) 0.202
Harvested LNb 13.8 ± 6.7
(4–29)
16.5 ± 7.1
(11–44)
0.053
CRM (\2 mm) 6 0 0.022
DRMb 3 ± 1.6 (1–6) 3 ± 1.1 (2–7) 0.908
Conversions 6 0 0.011
Complications (%) 11 (22) 5 (10) 0.104
Anastomotic leak
(%)
7 (14) 5 (10) 0.998
Oral reintakea 5 (4–6) 3 (3–5) 0.005
LOSa 10 (8–14) 8 (7–11) 0.034
IPSS (n = 30) (n = 30)
Preoperative test 3.50 ± 3 3.24 ± 2.7 0.012c
After 1 month 7.08 ± 3.5 6.71 ± 5.9
After 1 year 4.2 ± 2.3 3.53 ± 2.5 0.06c
IIEF (n = 30) (n = 30)
Erectile dysfunction (after 1 year)
No ED 10 17 0.045
Light 0 1
Moderate 6 0
Heavy 7 0
NSA 0 9
NA/RP 7 3
ED erectile dysfunction, NSA not sexually active patients, NA not
available to follow-up, RP refused to participatea values are expressed as median with interquartile rangeb values are expressed as mean with SDc p is calculated onthe analysis of the difference between preopera-
tive values versus 1 month and 1 year values
Surg Endosc
123
was acceptable in both procedures and within the range
expected by the standard recommendations.
No conversions occurred in R-TME compared to six
conversions in L-TME and this difference was statistically
significant (p = 0.011). Enhanced vision and dexterity of
the instruments provided by the robotic system may also
have contributed in making TME less challenging than that
with laparoscopy, thus reducing the intraoperative com-
plication rate and the conversion rate.
Operating time did not substantially differ between the
two groups: robot time was similar to laparoscopy time. The
adopted trocar position and technique avoided having to
redock the robot for the pelvic dissection thus reducing total
operating time. Moreover, cusum analysis of the operating
time showed that the learning curve in robot group was
achieved after case 22 (Fig. 6). The first part of the cusum
chart (cases 1–22) shows a phase of training with high sur-
geon effort, especially between cases 4 and 18. We feel that
the presence of more than one technically complex case in
this phase of training may have influenced the cusum anal-
ysis. After case #22, the cusum curve shows a plateau until
cases 39–42. A decreasing trend in operating time is seen
until case #44, where a second plateau is reached. We feel
that this phase may be related to the additional experience
gained by the surgeon after completing the learning curve. A
similar trend was found by Bokhari et al. [34] in phase 2 of
their experience. Moreover, the difference between the mean
operating time for the first 22 cases and the last 10 cases in
our experience is statistically significant (p = 0.002).
The complication rate was higher for L-TME compared to
R-TME. The incidence of anastomotic leakage was higher in
L-TME compared to R-TME, even though the difference
was not statistically significant (p = 0.998). The shorter
hospital LOS may be related to the lower complication rate
for R-TME and the shorter time to oral diet compared to that
of L-TME. The difference in LOS between the two groups
was statistically significant (p = 0.034).
The incidence of sexual dysfunction and bladder dys-
function following conventional rectal surgery is 94 and
73 %, respectively [35–37]. Damage to the hypogastric
nerves or the sacral splanchnic nerves or both during surgery
is the most common cause of sexual and urinary dysfunction
[38]. The first site of risk to nerve injury is the IMA region.
During ligation of the IMA, some of the preaortic para-
sympathetic fibers may be incorrectly manipulated and
injured [39]. Our urinary dysfunction analysis showed a
worsening of the IPSS scores 1 month after surgery in both
procedure groups, and a normalization 1 year after surgery.
Fig. 4 Learning curve of robotic anterior rectal resections with TME
Surg Endosc
123
Recently, Kim et al. [40] reported that bladder function
improved significantly over the first 6 months after L-TME
and 3 months after R-TME, with better outcomes for R-TME
compared to L-TME for the IPSS score. In the current study,
postoperative IPSS scores were lower for R-TME than for
L-TME, even though this difference was not statistically
significant (p = 0.886). We assert that the 3D view afforded
by the robotic system allowed the surgeon to better identify
and preserve the preaortic nerves and the superior hypo-
gastric plexus. Moreover, the use of the articulated mono-
polar cautery hook allowed the surgeon to obtain better
control of energy delivery, avoiding inopportune cauteriza-
tion of the nervous bundle. Erectile function was preserved in
100 % of sexually active patients in the R-TME group
compared to 43 % of those in the L-TME group 1 year after
surgery. This difference was statistically significant
(p = 0.045). In all cases, Denonvilliers’ fascia was easily
identified, helping the surgeon to carry out a precise incision
of this fascia at the level of the seminal vesicles, avoiding
inadvertent injuries to the neurovascular bundles that lie at
the lateral borders of Denonvilliers’ fascia and anteriorly at
the level of the posterolateral borders of the apex and base of
the prostate. Starting the TME by a posterior approach, as in
our standardized method, grants a wider mobilization of the
rectum and allows us to perform straight dissection, which
helps to identify and preserve the HNs [41]. Nervi erigentes,
arising from the S2 to S4 roots, join the hypogastric nerves
forming the IHP at the lateral side of the pelvic wall. This is
why we assert that the lateral dissection has to be carried out
after the anterior dissection and the path is kept as medial as
possible, without entering the mesorectal fascia. A gentle
countertraction of the rectum may help open the dissection
plane, thus avoiding injuries to this nerve bundle. This
maneuver seems to be improved in robot-assisted surgery
thanks to the stability and motion scaling of the robotic arms.
Excessive traction may increase the risk of injury to the
pelvic splanchnic nerve. In addition, robotic stereoscopic
view makes this structure more clearly visible.
This study has some limitations. The number of per-
formed procedures is quite low and the time interval is quite
long. A significant number of lower tumor localizations is
included in the robotic group compared to the laparoscopic
group, even though we feel that this difference may enhance
the advantages of robot-assisted surgery over the laparo-
scopic technique in terms of operating time and functional
results. This study is not a randomized trial and it was based
on a single-center experience. Although IPSS and IIEF are
widely accepted international indexes used to evaluate the
functional outcome after surgical procedures, score results
are influenced by the psychological and cultural background
of the patient and the individual’s interaction with the phy-
sician who proposed the questionnaires. Nevertheless, we
Fig. 5 Learning curve of laparoscopic anterior rectal resections with TME
Surg Endosc
123
feel that our results can show that robot-assisted TME is
oncologically safe and adequate for rectal cancer treatment
with better results than laparoscopic TME in terms of CRM,
conversions, and LOS. Better recovery in voiding and sexual
function is achieved with the robotic technique thanks to
stable and enhanced vision and the motion scaling of the
robotic arms as a result of enhanced dexterity.
Acknowledgments We thank Dr. Marina Rosito and Dr. Tania
Contardo for helping us collect the data.
Disclosures Drs. D’Annibale, Pernazza, Monsellato, Pende, Lucandri,
Mazzocchi, and Alfano have no conflicts of interest or financial ties to
disclose.
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