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: gpernazza@libero.it

I. Monsellato

e-mail: imonsellato@libero.it

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

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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

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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

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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

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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

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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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