How to Decide about Robotic Surgery in Patients with Locally Advanced Gastric Cancer?
Mircea Mănuc1,2,Catalin Dutei1,3, Matei R Bratu1,2 Bogdan Cristea2*,Ioana Husar-Sburlan3Bogdan Berbescu32,Mircea Diculescu1,2Catalin Vasilescu2,4Teodora Manuc1and Stefan Tudor4
1Department of Gastroenterology and Hepatology, Fundeni Clinical Institute, Bucharest, Romania
2Carol Davila University of Medicine and Pharmacy, Bucharest, Romania
3Department of Gastroenterology and Hepatology, Fundeni Clinical Institute, Bucharest, Romania
4Department of General Surgery and Liver Transplantation, Fundeni Clinical Institute, Bucharest, Romania
Submission: August 20, 2019; Published: August 29, 2019
*Corresponding Address: Bogdan Cristea, University of Medicine and Pharmacy of Bucharest, Romania
How to cite this article:Mircea Mănuc, Catalin Dutei, Matei R Bratu, Bogdan Cristea, et al. How to Decide about Robotic Surgery in Patients with Locally Advanced Gastric Cancer?. Canc Therapy & Oncol Int J. 2019; 15(1): 555901.DOI:10.19080/CTOIJ.2019.15.555901
Aim: Surgery is the cornerstone in the treatment of gastric cancer and includes conventional open gastrectomy and minimally invasive techniques. Preoperative criteria should be established in order to decrease the rate of conversion to open surgery. To evaluate such criteria, we must focus on computer tomography and upper endoscopy workup.
Methods:: This is a hospital-based observational retrospective study including 205 patients treated in Fundeni Clinical Institute, during the interval of 2008-2014. The patients were diagnosed with advanced gastric cancer according to endoscopic, computer-tomographic and histopathologic techniques. None of the patients received any neoadjuvant chemotherapy. 144 of patients underwent a curative surgical resection with D2 lymphadenectomy.
Results:: Minimally invasive surgery was performed on 51 patients; other 26 patients were initially treated by MIS but during operation they were converted to open surgery. Open surgery was performed on 128 patients. Risk factors that led to converting an initially MIS intervention to open intervention comprise: Borrmann 1 (p=0.0275) identified by endoscopy, metastasis (p=0.0416), peritoneal carcinomatosis (p=0.0156) identified by CT scan. On the contrary, endoscopic staging Borrmann 3 proved to be a preventing factor against surgical conversion (p=0.0169).
Conclusion:: A multivariate analysis of all prospective clinical, endoscopic and tomographic parameters is required to identify the patients with gastric cancer that could benefit more from the robotic platform. Endoscopic parameters such as the distance from cardia, distance to pylorus, the invasion of more than one gastric wall, the invasion of both vertical and horizontal portion, might constitute criteria for the selection of surgical methods.
Gastric cancer is the fourth most common cancer and the second leading cause of cancer-related death worldwide . Advanced gastric cancer comprises any tumor surpassing the submucosae, irrespective of the lymph node involvement . Initial preoperative staging is essential and should include endoscopy with biopsies and a contrast-enhanced computed tomography scan of the thorax and abdomen ± pelvis, for detecting regional invasion and metastatic disease . Endoscopic ultrasound (EUS) is helpful in determining the proximal and distal extent of the tumor and provides further assessment of the T and N stages, although it is less useful in antral tumors . In Europe alone more than 90% of the patients diagnosed with gastric tumors are already in an advanced stage
at first presentation , this situation being due to the lack of screening programs across the continent [5,6].
Surgery is the cornerstone in the treatment of gastric cancer and includes conventional open surgery gastrectomy (OS) and minimally invasive techniques (MIS) . While all surgical specialties benefit from a minimally invasive approach, in gastric cancer, laparoscopic surgery is currently being regarded as the treatment of choice only for early gastric cancer. The indications and outcomes of laparoscopic gastrectomy for advanced gastric cancer remain controversial due to the technical difficulties and the lack of long-term results , however there are countries (South Korea, Japan, Taiwan) that promote it. Experienced surgeons have begun to treat patients with advanced gastric cancer using MIS and have reported acceptable short-term
On several occasions a conversion from MIS to OS is
necessary, after realizing the impossibility of oncologic resection
by robotic surgery (RS) in a patient, thus creating important
disadvantages. The conversion from RS to OS combines the
high cost of the robotic surgery with the prolonged duration
of operating theatre use; also, a greater morbidity in patients
converted from RS to OS versus those who underwent OS from
the beginning has been demonstrated in patients with colorectal
cancer. To avoid these disadvantages, preoperative criteria
should be established in order to decrease the rate of conversion
from MIS to OS. To evaluate such criteria, we must focus on
computer tomography (CT) and upper endoscopy workup, each
of these implying disadvantages and limits.
This is a hospital-based observational retrospective study
including 205 patients treated in Fundeni Clinical Institute,
during the interval of 2008-2014. The patients were diagnosed
with advanced gastric cancer (AGC) according to endoscopic,
computer-tomographic (CT) and histopathologic techniques
Ethics committee approval was received for this study from
the ethics committee of Fundeni Clinical Institute. Approval Date:
21.12.2011. Decision No. 18848. All involved persons (subjects
or legally authorized representative) gave their informed
consent prior to study inclusion. All the cases diagnosed with
AGC during that period were included in the study. The recruited
cases were of both sexes, between 26 and 80 years old. None
of the patients received any neoadjuvant chemotherapy. 144
of patients underwent a curative surgical resection with D2
Retrieved data about patients included diagnosis year,
age, gender, endoscopic variables (location of tumor, modified
Borrman classification [12,13], extension to pylorus, cardia or
duodenum, presence of active hemorrhage) and CT variables
(presence of metastasis, peritoneal carcinomatosis, satellite
lymph node enlargement, surpassing of gastric wall, duodenum
invasion, intra-abdominal great vessels invasion, ascites and
extension to pylorus and cardia).
Patients were classified in two groups according to the
surgical procedure performed into: clasic open surgery (OS)
and minimally-invasive surgery (MIS) – either laparoscopic or
robotic (Figure 1). In all the patients referred to the robotic
surgery an initial laparoscopic exploration was performed in
order to evaluate carcinomatosis with very small masses and
superficial liver metastasis that are under the limit of detection
of CT investigation. In this patients palliative open surgery was
Data was introduced in Microsoft Excel 2007 (Microsoft
Corporation, Redmond, WA, USA) worksheets and analysed
statistically by Excel functions and GraphPad Prism6 (GraphPad
Software, La Jolla, California, USA). Variable analysis was
conducted by using Fisher’s exact test on contingency tables.
Of note, epidemiologic results show an increased number of
patients with AGC in 2012 compared to the other years. There
is a definite predominance (68% versus 32%) of male patients.
The peak interval of diagnosis is 65-75 (32%) years of age,irrespective of gender. Distribution of incidence and gender is
better shown in Figure 2. Results related to surgical procedures
reveal that 144 patients underwent total resection according to
the standard oncological recommendations, while the other 61
patients had palliative surgery. Minimally invasive surgery was
performed on 51 patients. 26 patients were initially evaluated
by laparoscopic exploration. Open surgery was performed from
start on 128 patients.
Statistically significant was Borrmann type 2 for OS
(p=0.0038, RR=1.26 95% CI=1.09-1.46, OR=3.06 95% CI=1.39-
6.73); also Borrmann 3 was significant for MIS (p=0.0006,
RR=0.66, 95% CI=0.49-0.88, OR=0.27, 95% CI=0.13-0.55);
extension to cardia/pylorus/duodenum was significant
(p=0.0048, RR=1.23, 95% CI=1.06-1.42, OR=2.66 95% CI=1.20-
5.88), as shown in Table 1.
Of the CT scan parameters, the presence of metastasis
(p=0.0178, RR=1.22, 95% CI=1.06-1.42, OR=2.76, 95% CI=1.15-
6.58), the surpassing of gastric wall (p=0.0008, RR=1.30, 95%
CI=1.13-1.51, OR=3.59, 95% CI=1.63-7.89), the great vessel
invasion (p=0.0184, RR=1.28, 95% CI=1.11-1.47, OR=4.97, 95%
CI=1.13-21.77) and the extension to cardia/pylorus (p=0.0449,
RR=1.19, 95% CI=1.03-1.39, OR=2.36, 95% CI=1.03-5.41) also
showed statistical relevance, as shown in Table 1.
Results regarding parameters correlated with palliative
resection of tumor comprise the following endoscopic
parameters with statistical significance: location on the
vertical portion of the stomach (p=0.04), location on more
than one wall of the vertical portion (p=0.0002), location on
both vertical and horizontal portion(p=0.03) and the presence
of active hemorrhage (p=0.02). Of the computer-tomographic
parameters, we retain the presence of metastasis (p<0.0001),
peritoneal carcinomatosis (p<0.0001), surpassing of the gastric
wall (p=0.0001), invasion of duodenum (p=0.0002), invasion of
the great vessels (p<0.0001), ascites (p=0.0178) and extension
to cardia/pylorus (p=0.01) with proven statistical significance.
Borrmann 5 endoscopic staging proved to be a factor correlated
with total resection (p=0.04) (Table 2).
Risk factors that led to converting an initially MIS
intervention to open intervention comprise: Borrmann 1
(p=0.0275) identified by endoscopy, metastasis (p=0.0416),
peritoneal carcinomatosis (p=0.0156) identified by CT scan.
On the contrary, endoscopic staging Borrman 3 proved to be
a preventing factor against surgical conversion (p=0.0169), as
shown in Table 3.
The aim of this study is to find preoperative criteria for
selection of patients in whom to begin with MIS, respectively
robotic surgery. Based on CT and upper endoscopy parameters,
we intend to identify: pylorus and duodenum invasion (due
to difficulty of dissection at distal gastric pole); cardial and
esophageal invasion (due to difficulty of dissection at proximal
gastric pole and local anastomosis); lymph node enlargement/
masses (due to difficulty to perform D2); horizontal extension
(due to complex types of resections - pancreas, spleen, left
hepatic lobe, etc.) and invasion of great vessels. Also, metastasis
and carcinomatosis contraindicates lymphadenectomy .
The only two situations in which they cannot be identified are
represented by peritoneal carcinomatosis with very small masses
and hepatic metastasis size less than 4 mm. Such criteria would
significantly help in treating more patients with AGC by MIS,
without risking a switch to open surgery, major postoperative
complications and mortality, or cancer recurrence.
It should be noted that in many centers that operate gastric
cancer, the surgery usually begins with the laparoscopic
exploration of the peritoneal cavity. After deciding the surgical
indication, the standard steps are general anesthesia followed
by insufflation and the placement of the video camera. In this
way peritoneal metastasis (carcinomatosis) and small hepatic
metastasis - under the detection limit of the CT scan - can be
identified from the beginning. This approach clearly leads to a
decrease in the number of unnecessary laparotomies. However,
this protocol has two disadvantages as it increases both the
operative time and the costs involved - the materials used
(protective covers, surgical instruments dedicated to robotic
surgery, etc.) if robotic surgery is intended.
Other authors propose the robotic approach from the
beginning followed by open surgery in case of necessity due
to technical difficulties. However, it is demonstrated that the
conversion from MIS to OS is not harmless and implies a greater
rate of complications, increasing the postoperative morbidity.
For example, in colorectal laparoscopic surgery, conversion to
open surgery of a laparoscopic intervention is an independent
risk factor for the occurrence of fistulas, parietal suppurations
and postoperative peritonitis. Of note, the results we achieved
in this study should be enhanced by further investigations, until
clear, universally valid criteria are established for the selection
of gastric cancer patients to undergo robotic surgery. The
realistic point of view is that variability (of cases, of the surgical
team experience, of the volume of operations performed in
the concerned institute) will always exist. Also, post-operative
results of MIS and OS need to be compared, considering the
operating time, number of retrieved lymph nodes, bleeding time
both intra-operative and post-operative, survival rate [15-19].
Following our analysis locally advanced gastric cancers type
2 Borrmann occur more frequently in the group of patients in
which OS was performed compared to type 3 Borrmann patient
in which MIS was preferred. The small number of cases analyzed,
and the retrospective nature of this study make this observation
difficult to interpret. It should be examined whether the type
2 Borrmann lesions represent an independent factor or if in
association with invasion of cardia/pylorus.
The most important endoscopic finding of differentiation
between the two groups is the endoscopic signs of extension
to the cardia, on one hand, and to the pylorus and duodenum,
on the other hand. It is easy to understand why the invasion of
either of the two gastric poles of the stomach indicates open
surgery. The invasion of the pylorus makes it technically difficult
to close the duodenal stump. The invasion of the cardia often
requires the intraoperative exploration of the superior gastric
pole to establish the extension to the esophagus, possibly
the submucosal extension of the malignant process. Tumor
extension to the esophagus requires an esophageal resection
that could require a thoracic approach. These situations can be
solved by minimally invasive techniques but require a thorough
preoperative planning. The information provided by the
preoperative CT scan that may suggest a greater benefit of open
surgery are the invasion of the cardia, the invasion of the pylorus,
the surpassing the gastric wall with invasion of neighboring
organs which indicates the need for a complex resection (gastric
resection with splenectomy, liver resection, etc.). In these cases
laparotomy is preferred. Evidence of large vessel invasion on
CT scan guides surgeons to choose conservative treatment or
This choice cannot be completely separated from the
previous discussion. However, it should be emphasized that
some endoscopic findings bring arguments for a palliative
approach: the localization of the gastric tumor (in the vertical
portion of the stomach, across several walls, in both vertical and
horizontal portions of the stomach) and the presence of active
bleeding. Most authors tend to perform open surgery if palliative
surgery is intended. In our experience, we have performed MIS
in selected cases of palliative surgery with satisfying outcomes,
patients benefiting from avoiding the stress and the longer
healing process involved in a large laparotomy.
Certainly, the CT scan offers clear arguments whenever
palliative surgery is in discussion. The CT scans performed for
our patients offer useful data about the systemic dissemination of
the disease (visceral metastasis and peritoneal carcinomatosis)
and thus prevent an extended lymphadenectomy. Moreover,
detecting ascites usually indicates the presence of peritoneal
carcinomatosis, confirmed later by cytological examination of
It should be reminded that a conversion from the OS to MIS
is not without consequences, which has been demonstrated in
laparoscopic colorectal surgery, underlining the importance of
finding criteria for conversion risk evaluation. Our data provide
that a polypoid endoscopic type (type 1 Borrmann) correlates with
an increased risk of conversion, while type 3 Borrmann lesions
occur more frequently in MIS group and rarely in the converted
group. In 26 patients addressed to robotic surgery laparoscopic
control of the peritoneal cavity reveals carcinomatosis with very
small masses and superficial liver metastasis that are under the
limit of detection of CT investigation. In these patient’s palliative
open surgery was applied.
Technological advances in the world of surgery have
developed exponentially during these decades with undeniable
advantages for patients. Industrial pressure, media and
marketing elements have also contributed to the spread of
these hi-tech, often very expensive methods. One such tendency
promotes the introduction of the robotic surgery in many
specialties. The first stage of feasibility assessment of robotic
surgery is about to end. The DaVinci equipment can be used to
operate almost everything. The key point is to establish which
patients would benefit more from the use of such technology,
considering that the indications of robotic surgery are currently
extending from ECG to AGC.
The current study deals with finding criteria for selection
of patients with gastric cancer that could benefit more from
minimally invasive surgery specialty for the robotic platform. In
order to asses each patient properly, a multivariate analysis of
all prospective clinical, endoscopic and tomographic parameters
is required. Endoscopic parameters such as the distance from
cardia, distance to pylorus, the invasion of more than one gastric
wall, the invasion of both vertical and horizontal portion, might
constitute criteria for the selection of surgical methods. Until
clear data is obtained, minimally invasive surgery in advanced
gastric cancer has to be performed strictly in excellence centers
of gastric surgery.
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Dutei C, Sburlan, Vasilescu C, Manuc M, Diculescu M (2014) Predictive factors for choosing minimally invasive surgery in patients with advanced gastric cancer. United European Gastroenterology Journal Supplement 1.
Chen K, Pan Y, Cai JQ, Xu XW, Wu D, et al. (2014) Totally laparoscopic gastrectomy for gastric cancer: a systematic review and meta-analysis of outcomes compared with open surgery. World J Gastroenterol 20: 15867-15878.