Robotic vs laparoscopic distal gastrectomy with D2 lymphadenectomy for gastric cancer: a retrospective comparative mono-institutional study
Cianchi et al. BMC Surgery
Robotic vs laparoscopic distal gastrectomy with D2 lymphadenectomy for gastric cancer: a retrospective comparative mono- institutional study
Fabio Cianchi 0
Giampiero Indennitate 2
Giacomo Trallori 1
Manuela Ortolani 2
Beatrice Paoli 2
Giuseppe Macrì 1
Gabriele Lami 1
Beatrice Mallardi 4
Benedetta Badii 0
Fabio Staderini 0
Etleva Qirici 0
Antonio Taddei 0
Maria Novella Ringressi 0
Luca Messerini 3
Luca Novelli 3
Siro Bagnoli 1
Andrea Bonanomi 1
Caterina Foppa 0
Ileana Skalamera 0
Giulia Fiorenza 0
Giuliano Perigli 0
0 Department of Surgery and Translational Medicine, Center of Oncological Minimally Invasive Surgery (COMIS), University of Florence , Largo Brambilla 3, 50134 Florence , Italy
1 Unit of Gastroenterology, University Hospital Careggi , Florence , Italy
2 IFCA , Florence , Italy
3 Department of Experimental and Clinical Medicine, University of Florence , Florence , Italy
4 ISPO , Florence , Italy
Background: Robotic surgery has been developed with the aim of improving surgical quality and overcoming the limitations of conventional laparoscopy in the performance of complex mini-invasive procedures. The present study was designed to compare robotic and laparoscopic distal gastrectomy in the treatment of gastric cancer. Methods: Between June 2008 and September 2015, 41 laparoscopic and 30 robotic distal gastrectomies were performed by a single surgeon at the same institution. Clinicopathological characteristics of the patients, surgical performance, postoperative morbidity/mortality and pathologic data were prospectively collected and compared between the laparoscopic and robotic groups by the Chi-square test and the Mann-Whitney test, as indicated. Results: There were no significant differences in patient characteristics between the two groups. Mean tumor size was larger in the laparoscopic than in the robotic patients (5.3 ± 0.5 cm and 3.0 ± 0.4 cm, respectively; P = 0.02). However, tumor stage distribution was similar between the two groups. The mean number of dissected lymph nodes was higher in the robotic than in the laparoscopic patients (39.1 ± 3.7 and 30.5 ± 2.0, respectively; P = 0.02). The mean operative time was 262.6 ± 8.6 min in the laparoscopic group and 312.6 ± 15.7 min in the robotic group (P < 0.001). The incidences of surgery-related and surgery-unrelated complications were similar in the laparoscopic and in the robotic patients. There were no significant differences in short-term clinical outcomes between the two groups. Conclusions: Within the limitation of a small-sized, non-randomized analysis, our study confirms that robotic distal gastrectomy is a feasible and safe surgical procedure. When compared with conventional laparoscopy, robotic surgery shows evident benefits in the performance of lymphadenectomy with a higher number of retrieved and examined lymph nodes.
Gastric cancer; Robotic surgery; Laparoscopy; Lymphadenectomy; Distal gastrectomy
Minimally invasive surgery for gastric cancer has evolved
rapidly and has increased in popularity during the last two
decades mainly in the Far East and for patients with
earlystage tumors [1, 2]. A number of non-randomized trials,
randomized controlled trials and meta-analyses have
confirmed that laparoscopic surgery for gastric cancer can
improve short-term results and the patient’s quality of life
when compared with open surgery [3–7]. Nevertheless, the
development of laparoscopic surgery for gastric cancers in
the Western world has been slow because most gastric
cancers are diagnosed in an advanced stage for which
laparoscopic gastrectomy is not yet considered an acceptable
alternative to standard open surgery [8, 9]. This skepticism
is basically due to the technical complexity of laparoscopic
gastrectomy and concerns the feasibility of an oncologically
acceptable lymphadenectomy. For these reasons,
laparoscopic gastrectomy is considered one of the most difficult
operations, requiring a long learning curve of about 40–50
cases [10, 11].
Robotic surgery has been introduced to overcome
some of the technical limitations of laparoscopic surgery,
such as two-dimensional vision, amplified physiological
tremor, restricted range of motion and ergonomic
discomfort [12, 13]. Robotic systems include
operatorcontrolled 3-dimensional cameras that ensure steady
and effective surgical fields of view with motion scaling
and multiple degrees of freedom. It is believed that this
technological evolution can assist the surgeon with
complex surgical procedures that are required in radical
gastrectomy, such as precise lymph node dissection and
intracorporeal anastomoses .
Several studies have compared the feasibility and efficacy
of robotic-assisted gastrectomy to that of
laparoscopicassisted gastrectomy for gastric cancer . Robotic
gastrectomy was reported to be associated with less operative
blood loss and shorter hospital stay than laparoscopic
gastrectomy [16, 17]. However, an overt advantage of robotic
surgery in comparison with the laparoscopic technique in
the treatment of gastric cancer has not been demonstrated
This study was designed to analyze our early
experience with robotic gastric surgery and compare the
shortterm clinical outcomes after laparoscopic and robotic
distal gastrectomy for gastric cancer.
A total of 41 laparoscopic distal gastrectomies (LDG) for
gastric cancer have been performed since June 2008 at the
Center of Oncologic Minimally Invasive Surgery (COMIS),
University of Florence, Florence, Italy. After the
introduction of the daVinci Si surgical system (Intuitive Surgical
Inc., Sunnyvale, CA, USA) in April 2014 at our hospital, we
have performed 30 robotic distal gastrectomies (RDG) for
gastric cancer between June 2014 and September 2015. All
of the laparoscopic and robotic procedures were performed
by a single surgeon (F.C.) and these cases were his initial
experience with robotic gastrectomy.
We prospectively collected and retrospectively compared
the clinicopathological characteristics, surgical performance
and postoperative outcomes/morbidities between these two
groups of patients. All patients underwent diagnostic and
preoperative staging work-up according to a standard
protocol which includes upper digestive endoscopy with
gastric biopsy and computed tomography of the abdomen
and chest. Patients with distant metastases, para-aortic
lymph node involvement and/or pre- or intraoperative
diagnosis of T4 lesions (i.e., local invasion of other organs,
including spleen, pancreas or peritoneum), were excluded
from the study. All patients had been thoroughly informed
about the study and gave their written consent for the
investigation in compliance with the Helsinki Declaration
and in accordance with the ethical committee of our
The characteristics of patients, such as age, gender, body
mass index (BMI) and tumor location, pathological results
and surgical outcomes (operative time, blood loss,
postoperative morbidity and mortality, time-to-first flatus,
timeto-first oral intake and postoperative hospitalization) were
Tumor localization was classified as middle or lower third
of the stomach. The extension of lymph node dissection,
namely D1 + α/β or D2, was performed according to the
lymph node classification of the Japanese Gastric Cancer
Association . Tumors were classified according to the
7th edition of the AJCC/TNM tumor staging . They
were also classified according to Lauren’s histotype, i.e.,
intestinal, diffuse or mixed.
Trocar placement and docking the robotic arms
The preoperative procedures of RDG are not different
from those of LDG except for the use of robotic ports and
articulating robotic instruments. Under general anesthesia,
the patient was placed in supine, reverse Trendelenburg
position with legs abducted. In the robotic technique, the
camera port was inserted by the open method through an
umbilical transverse incision with a 12-mm trocar. After
establishing pneumoperitoneum, three 8-mm trocars for
the robotic arms were inserted: one in the upper right
quadrant, one in the lower right quadrant, and one in the
upper left quadrant. A final fourth 12-mm trocar was
inserted in the lower left quadrant for the assistant. Either
a hook or a monopolar shear was held in the first robotic
arm located at the patient’s left side. A Maryland bipolar
forceps and a Cadiere forceps were held in the second and
third arms, respectively, at the patient’s right side.
The LDG surgical technique includes four trocars (two
12-mm and two 5-mm trocars) that are placed as
previously described .
Most of the operative steps during RDG were the same as
those during LDG. First, a routine exploration of the
abdominal cavity was performed. D1 + α/β or D2
lymphadenectomy and gastric dissection were performed as
previously described . A key difference between RDG
and LDG is that robotic dissection of lymph nodes was
performed with the robotic wristed instruments. Moreover,
some procedures, such as operating the stapler, applying
hemoclips, inserting and removing surgical gauzes, are
performed by the first operator during LDG whereas they are
performed by the assistant during RDG.
In both procedures, mechanical intracorporeal either
Billroth II or Roux-en-Y gastrojejunal anastomosis was
performed. In the last 25 laparoscopic and in all robotic
procedures, we reinforced the duodenal stump with a
running, barbed suture after the duodenal transaction.
The surgical specimen was placed in a polyethylene
endobag and pulled out of the peritoneal cavity through
the umbilical port which was extended to a length of 4–
Categorical variables within laparoscopic and robotic
groups were compared using Fisher’s exact test or the
chi-square test. Quantitative variables were summarized
by means and SEM or medians and range. Groups were
compared using the Mann-Whitney test.
Table 1 shows the clinicopathological characteristics of
the patients in the LDG and RDG groups. There were
no significant differences in terms of age, sex or BMI.
Patients in the LDG group had a larger mean tumor size
than those in the RDG group. However, tumor stage
distribution was similar between the two groups. Most of
the tumors were located in the lower third of the
stomach in both groups.
Surgical performance is detailed in Table 2. Robotic
procedures showed significantly higher operative times when
compared to laparoscopic surgery. No significant
difference was found between the two groups in terms of blood
loss. More Billroth II reconstructions were performed in
the RDG group even if the difference was not statistically
significant. No patients required open conversion in either
group. No tumor involvement of the proximal or distal
margin was found in any patient in either of the two
groups. A higher number of lymph nodes was retrieved
and examined in the RDG group when compared with the
Table 1 Clinicopathological characteristics of patients
undergoing laparoscopic and robotic distal gastrectomy
P = 0.02
LDG group after D2 dissection (39.1 ± 3.7 vs 30.5 ± 2.0,
respectively, P = 0.02).
The incidence of postoperative complications
(surgery-related and surgery-unrelated), reoperations and mortality
rates were similar in the two groups (Table 3). There were
two mortalities in the LDG group and one in the RDG
group. The cause of the two mortalities in the LDG group
included one duodenal stump leakage with peritonitis and
sepsis and one case of acute myocardial infarction. The case
of duodenal stump leakage occurred before the
introduction of the manual reinforcement with a running suture
over the duodenal stump closure. One 89-year-old female
patient in the RDG group who experienced a postoperative
intestinal occlusion received laparotomy but eventually died
of a cerebral vascular accident.
No significant differences were found between the two
groups in terms of time to diet, bowel function recovery
or length of hospital stay (Table 3).
The clinical efficacy and advantages of the laparoscopic
technique in the treatment of gastric cancer have now been
recognized . However, laparoscopic gastric surgery is
still considered a technically demanding procedure. In
particular, the technical threshold of performing lymph node
dissection and intracorporeal suture during laparoscopic
gastrectomy remains high and requires a steep learning
curve [10, 11]. The robotic platform provides some
Table 2 Comparison of surgical performance between the
laparoscopic and the robotic groups
Type of reconstruction
Lymph node dissection
Mean operative time (min)
(mean ± SEM)
Blood loss (ml)
(mean ± SEM)
Conversion to open surgery
Positive resection margin
No. of retrieved lymph
nodes after D2 dissection
(mean ± SEM)
N = 41
N = 30
technical improvements, such as improved vision, wristed
instrument, tremor filtration system and motion scaling,
that enable surgeons to easily perform precise
lymphadenectomy and anastomoses. A number of studies have
shown the feasibility and safety of robotic gastric surgery
but a clear superiority of robotic surgery over laparoscopy
has not yet been demonstrated [22–26]. No substantial
reduction in time-to-first flatus, time-to-first oral feeding and
length of hospital stay has been reported after robotic
surgery when compared to laparoscopy. Our early experience
in robotic gastrectomy confirms these previously published
results: we did not find any significant difference in
shortterm clinical outcomes between patients in the robotic and
those in the laparoscopic group. However, our inability to
show robotic surgery to be superior to laparoscopic surgery
is not surprising in light of previous studies that have
compared laparoscopic with open surgery. In numerous studies,
laparoscopic gastrectomy facilitated less blood loss, earlier
bowel function recovery and shorter length of stay than
open gastrectomy . Thus, conceivably, optimal
perioperative surgical outcomes may have already been
achieved with laparoscopic surgery, leaving little room for
improvement via robotic surgery.
One crucial step in gastric cancer surgery is
lymphadenectomy since the removal of an adequate number of
lymph nodes has been shown to improve the accuracy of
staging and regional disease control . This procedure
is typically considered to be technically difficult to
perform in conventional laparoscopic surgery, especially
when D2 lymphadenectomy is mandatory [10, 11, 29].
This is mainly due to the use of conventional straight
forceps in laparoscopic surgery that do not allow the surgeon
to reach deep-seated vessels and areas such as the
suprapancreatic one. Stable exposure and use of wristed
instruments with the robotic system may help the surgeon to
efficiently perform lymph node dissection in these delicate
areas, in particular around the posterior aspect of the
common hepatic artery and the splenic vessels . In the
present study, we found that robotic surgery can improve
the quality of lymphadenectomy in distal gastric resection
when compared with conventional laparoscopy. Indeed,
the mean number of retrieved lymph nodes in the robotic
group was significantly higher than in the laparoscopic
group (39.1 vs 30.5, respectively) and, importantly, the
mean values in both groups were much higher than the
recommended number (i.e., 25) for adequate D2
lymphadenectomy . Importantly, this number was even higher
than what we found in a group of matched patients who
were operated on by open distal gastrectomy between
2008 and 2012 at our institution .
Despite the evident technical advantages offered by
the robotic system, recent meta-analyses comparing
robotic and laparoscopic gastrectomy have failed to show a
significant increase in the number of retrieved lymph
Table 3 Comparison of short-term clinical outcomes between
the laparoscopic and the robotic groups
Duodenal stump leakage
Delayed gastric emptying
Urinary tract infections
Deep venous thrombosis
Cerebral vascular accident
N = 41
N = 30
nodes in patients operated robotically [15–17, 32]. This
may be explained by the fact that the majority of the
analyzed studies were carried out in the Far East where
patients generally have a low BMI. Recently, Lee et al. 
have shown that the benefits of a robotic approach were
more evident in high versus normal BMI patients when
performing distal gastrectomy with D2
lymphadenectomy, particularly in terms of achieving a consistent
number of retrieved lymph nodes (>25). The authors
concluded that robotic surgery may overcome the
technical difficulties due to excessive intra-abdominal fat and
thick abdominal walls during laparoscopic
lymphadenectomy. Our findings seem to confirm these previously
published results: the BMIs of our patients (26.0 and
27.0 kg/m2 in the laparoscopic and robotic group,
respectively) were similar to those of high-BMI patients
reported by Lee et al. (26.8 and 26.9 kg/m2 in the two
groups, respectively), thus showing that robotic surgery
may offer consistent quality of lymphadenectomy for
patients with high BMI. Importantly, the present results
were achieved during our very early experience in gastric
robotic surgery. This suggests that surgeons with
sufficient experience in laparoscopic gastrectomy can rapidly
overcome the learning curve for robotic gastrectomy
and high-quality surgery is achievable even after a
relatively low number of cases . These advantages could
be more helpful in Western countries or lower volume
centers, where high BMI patients are more common and
where there is a lower incidence of gastric cancer, which
limits the number of gastric cancer surgeries to be
performed through a minimally invasive approach.
All sorts of studies that have been published about
robotic gastric surgery, have reported that operative time
was prolonged when compared with the laparoscopic
approach and our findings are in line with these results
[15–17, 32]. There are a number of possible reasons for
this: first, robotic surgery is associated with an increased
set-up time needed to position the robot before
beginning surgery. However, docking times can be shortened
after accumulation of greater experience. Secondly, the
prolonged time may be due to camera motion
interrupting the operative procedure and the unadapted optical
system with an absence of a large general view of the
operative field which prevents a safe continuous dissection
and necessitates slow manipulation. However, longer
operation times have never been shown to translate into
increased perioperative complications and thus should
not discourage surgeons from investigating the novel
utility of robotic surgery.
One of the limitations of the present study was the lack
of a detailed comparative analysis of cost-effectiveness
between robotic and laparoscopic gastric surgery. Robotic
gastric surgery undoubtedly has higher costs than
laparoscopic surgery as clearly demonstrated by Park et al. .
The only way its use can be justified would be through
improved patient survival achieved through more efficient
surgery. The present study seems to show potentially
relevant advantages, such as a higher number of retrieved
lymph nodes, that would justify the higher costs of robotic
systems. However, a multicenter, randomized study is
needed to confirm this clinical benefit and evaluate
whether it may effectively translate into improvement of
long-term patient survival and quality of life.
Within the limitation of a small-sized, non-randomized
analysis, our study confirms that robot-assisted gastrectomy
is a feasible and safe surgical procedure. When compared
with conventional laparoscopy, robotic surgery shows
evident benefits in performing lymphadenectomy with a
higher number of retrieved and examined lymph nodes.
LDG: Laparoscopic distal gastrectomyRDG: Robotic distal
gastrectomyBMI: Body mass indexAJCC: American joint committee of cancer
Availability of data and materials
The database generated during the current study contains sensible data
which may provide insight in clinical and personnel information about our
patients and lead to identification of patients. Therefore, these data cannot
be made publically available. Access to the database can be obtained from
the corresponding author on reasonable request.
FC performed all surgical operations and was a major contributor in writing
the manuscript. BB, FS, EQ, AT, MNR, CF, IS, GF, and GP were part of the
same surgical unit and were involved in patient care, follow-up and
acquisition, analysis and interpretation of the data. GI, GT, MO, PB, GM, GL, BM, SB,
and AB were part of different endoscopic units from different hospitals in
Florence and were involved in the recruitment of patients and significantly
contributed to acquisition and critical revision of the data during the entire
length of the study period (8 years). LM and LN are pathologists and were
involved in drafting the manuscript and revising it critically for important
intellectual content. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
All patients had been thoroughly informed about the study and gave their
written consent for the investigation in compliance with the Helsinki
Declaration and in accordance with the ethical committee of our University
Hospital, Azienda Ospedaliero-Universitaria Careggi (Florence, Italy).
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