Robot-Assisted Total Gastrectomy: Preliminary Evaluation

Abstract

Background:

Laparoscopic total gastrectomy with extended lymphadenectomy is a technically demanding surgical procedure with steep learning curve that has limited its widespread use. The aim of this study was to evaluate the feasibility of the robotic approach in total gastrectomy for cancer. We present our experience of 17 consecutive patients who underwent robotic total gastrectomy with intracorporal sutured Roux-en-Y esophagojejunostomy and jejuno jejunostomy between 2014 and 2017.

Methods:

Data were collected, and patients' demographics and outcomes were examined retrospectively.

Results:

Seventeen patients with a median age of 68 years (range 32–81) were identified (10 males, 7 females). Mean operative time was 198 minutes (range 108–277) including mean anastomosis time of 25 minutes (range 18–35). There was no conversion to open surgery or requirement for perioperative blood transfusion. Median length of hospital stay was 9 days (range 2–30). Two patients developed postoperative complications including one anastomotic leakage treated conservatively and one internal hernia requiring surgical revision. There was no 90-day mortality or readmission.

Conclusion:

Robot-assisted total gastrectomy is feasible and reproducible. It overcomes several laparoscopic technical difficulties especially regarding anastomosis. It has the potential to become an alternative to open gastrectomy for gastric cancer. Nevertheless, further follow-up and randomized clinical trials are needed to evaluate mid-term and long-term outcomes of this approach.

Introduction

Despite its declining incidence, gastric cancer remains a public health issue. Indeed, gastric cancer is the fifth most common cancer and the third leading cause of cancer-related death worldwide.¹ Gastrectomy with adequate lymphadenectomy remains the only curative treatment.¹ In 1994, Kitano et al. first reported the laparoscopic approach in distal gastrectomy.² Since then, several studies confirmed the feasibility and reproducibility of laparoscopic gastrectomy.³ Recent randomized controlled trials validated the oncological safety and confirmed better postoperative outcomes in laparoscopic approach than in open gastrectomy.⁴ However, laparoscopic total gastrectomy remains controversial.^5–7The controversy lies in the longer learning curve due to technical difficulties encountered during lymphadenectomy and surgical reconstruction after total gastrectomy.^8,9 The steeper learning curve could be explained by the limitations and weaknesses of laparoscopy such as restricted device manipulation area and two-dimensional field.

Recently robotic surgery systems have been applied to gastrectomy to overcome some of the laparoscopic drawbacks.¹⁰ Robotic approach has many advantages such as a better device motion, tremor-free dissection, three-dimensional (3D) visualization, and articulated devices, allowing shorter learning curve.¹¹ Many reports from Asia validated the feasibility of robotic distal gastrectomy, but a few studies have evaluated robotic total gastrectomy with intracorporal robotic suture anastomosis.^12,13 This study aimed to evaluate the feasibility and reproducibility of robotic total gastrectomy in a Western population.

Methods

Study population

Between October 2014 and October 2017, all consecutive patients who underwent robotic total gastrectomy in our institution for gastric cancer (n = 12), gastrointestinal stromal tumor (GIST, n = 4), and liposarcoma (n = 1) were retrospectively included.

Preoperative evaluation

Preoperative workup included an esophagogastroduodenoscopy with core-needle biopsy, computed tomography (CT), and endoscopic ultrasonography. All samples were preoperatively reviewed in a multidisciplinary clinical conference. Patients with advanced gastric cancer were administered perioperative chemotherapy, including 5-fluorouracil, folinic acid, and cisplatin (LV5FU2-CDDP, n = 2), epirubicin and oxaliplatin plus capecitabine (EOX, n = 1), 5-fluorouracil and leucovorin plus oxaliplatin (FOLFOX, n = 1) and imatinib (n = 1) based on pathology results according to the European society for medical oncology guidelines.¹

Surgical procedure

Total gastrectomies were performed by 1 surgeon with extensive experience in both open and laparoscopic procedures. D1⁺ lymphadenectomy was carried out for patients with advanced gastric cancer 4 to 6 weeks after the preoperative chemotherapy according to the Japanese gastric cancer classification and treatment guidelines.^14,15 Whereas D1 lymphadenectomy was performed for stage I gastric cancer (n = 5) and no lymphadenectomy was performed in patients who presented with GIST.

Robot docking

The patient was placed in a reverse Trendelenburg position as shown in Figure 1a. Pneumoperitoneum was established using a Veress needle at left Palmers point with intra-abdominal pressure of 10 mmHg. A 10 mm robotic port was placed just lateral to the umbilicus for 30°optics. Three 8 mm robotic trocars were inserted: two in the upper abdomen at the mid clavicular line on the left and right sides, and one on the right anterior axillary line. A 12 mm port was placed between the right robotic port and the camera port for the air seal use. Another 12 mm port placed between the left robotic port and the camera port was used by the assistant. It allowed the introduction of suction, the clip applier, sutures, and stapler. After the placement of ports (Fig. 1b), the Da Vinci surgical System (Intuitive Surgical, Sunnyvale, CA) was moved to the operative table above the patient's head and docked onto the ports.

FIG. 1.

Robot docking. (a) Patients' positioning. (b) Ports placement.

Robotic dissection

Robot-assisted total gastrectomy was performed using robotic scissors, hook, fenestrated bipolar forceps, Cadiere forceps, needle holder, and Hemolock clips (Intuitive Surgical).

The greater omentum was first divided and then dissected using robotic bipolar forceps in the direction of the lower pole of the spleen. The dissection of the gastrocolic ligament was performed toward the pylorus. The lesser omentum was then opened from pars flaccida to the hepatic pedicle. The proper hepatic artery was then dissected until identification of the right gastric artery, allowing to achieve lymph node removal of station number 5. Next, the first duodenum was sectioned with an endoscopic stapler (Endo GIA; Medtronic, Minneapolis, MN). Lymphadenectomy of major vessels was performed starting with the hepatic hilum toward the celiac trunk. Once the celiac trunk was released, the left gastric artery was identified and cut, allowing for complete removal of lymph node station number 7. In 2 patients, a splenic artery lymphadenectomy was performed with spleen preservation according to the Japanese gastric cancer classification.¹⁴ The gastrosplenic ligament was then separated up to the left side of the esophageal hiatus dissecting the short vessels from the spleen surface. The esophagus was sectioned using an endoscopic stapler (Endo GIA; Medtronic) by the assistant surgeon.

Reconstruction phase

Reconstruction was performed following standardized operative procedures: an intracorporal ante colic reconstruction was performed using a Roux-en-Y esophagojejunostomy with a jejunojejunostomy 70 cm from the esophagojejunostomy. The esophagojejunostomy was an end to side anastomosis, performed with an absorbable V-lock 3–0 (Medtronic). The posterior continuous suture was performed between the whole esophageal transection stapled line and the jejunal wall before the small intestine and the esophagus opening (Fig. 2a). The anterior continuous suture was then performed (Fig. 2b). A side-to-side jejunojejunostomy was performed 70 cm from the previous anastomosis using two continuous anterior and posterior sutures with absorbable V-lock 3–0. Finally, the biliary and alimentary circuits were separated using a linear stapler. After hemostasis control, the specimen including the stomach, lymph node, and the greater omentum was placed in an endoscopic retrieval bag (Endocatch; Medtronic) for removal through an infraumbilical vertical incision. A drain was placed near the esophagojejunostomy in the first nine total gastrectomies. In light of the first procedures' safety, drain placement was then abandoned.

FIG. 2.

Robot-assisted intracorporal esophagojejunostomy. (a) End-to-side continuous suture between esophagus and jejunal wall. (b) Anterior continuous suture after the esophagus and jejunal opening.

Postoperative course

Standard blood work, including blood cells count and C-reactive protein measurement, was performed at postoperative days 1 and 3. Patients were given liquid diet at postoperative day 1 and soft diet the day after first flatus. After 2 days of soft diet and if patients presented no postoperative complications, they were discharged. Pathological tumor staging was established according to the AJCC cancer staging manual, seventh edition (2010).⁷

Statistical analysis

Preoperative, intraoperative, and postoperative data were retrospectively collected in a local database with follow-up ranging from 4 to 36 months. An intention to treat analysis was performed using Excel statistical program (Microsoft, Inc., Redmond, WA). The data were reported as absolute numbers and median (range) when appropriate. Comparison of 2015 and 2017 patients' operative time was determined using Mann–Whitney U test.

Results

Study population

Patient characteristics are summarized in Table 1. Seventeen consecutive patients with a median age of 68 (32–81) years and a median body mass index of 30.78 (25–42) kg/m² underwent robotic total gastrectomy. Three patients had previous abdominal surgery such as laparoscopic appendicectomy (n = 2) and open splenectomy, (n = 1) and 7 patients had preoperative chemotherapy. Twelve patients had comorbidities, including pulmonary diseases (n = 4), heart diseases (n = 2), liver dysfunction (n = 2), and hypertension (n = 5).

Table 1.

Patients' Characteristics

	n	Median	Range
Age (years)		68	32–81
Gender (M/F)	10/7
ASA
1	3
2	10
3	4
Comorbidity
Pulmonary disease	4
Heart disease	1
Liver dysfunction	2
Hypertension	5
Diabetes	1
BMI (kg/m²)		30.78	25–42
Previous abdominal surgery	3
Perioperative chemotherapy	7

BMI, body mass index.

Intraoperative course

Intraoperative course results are presented in Table 2. Overall, conversion rate to open surgery was nil. Median operative time was 198 (108–277) minutes, including median docking time of 19 (14–30) minutes, median dissection time of 165 (88–247) minutes, and median anastomosis time of 25 (18–30) minutes. As it is shown in Figure 3, operative time significantly decreased from 2015 to 2017 (median, 228 minutes versus median, 185 minutes; P = .048). Median estimated blood loss was 150 (100–300) mL and there was no blood transfusion requirement.

FIG. 3.

Operative time decrease (Mann–Whitney U test; P = .048).

Table 2.

Intraoperative Course

	n	Median	Range
Docking time (minutes)		19	14–30
Dissection time (minutes)		165	88–247
Operative time (minutes)		198	108–277
Roux-en-Y anastomosis time (minutes)		25	18–35
Blood loss (mL)		150	50–300
Conversion to open surgery	0

Histopathological outcomes

Histopathological outcomes are summarized in Table 3. Patients were diagnosed with an upper third stomach tumor (n = 10), middle third one (n = 1), lower third one (n = 2), or linitis (n = 4). Median tumor size was 37.5 (10–210) mm. The median number of retrieved lymph nodes was 15 (0–37). Fourteen patients had disease-free margins.

Table 3.

Histopathological Outcomes

	n	Median	range
Tumor size (mm)		37	10–210
Number of retrieved lymph nodes		15	0–37
R0 resection	14
R1 resection	3
Histopathological type
Adenocarcinoma	12
GIST	4
Liposarcoma	1
Location
Upper third	10
Middle third	1
Lower third	2
Linitis	4

GIST, gastrointestinal stromal tumor.

Postoperative outcomes

Postoperative outcomes are summarized in Table 4. Median length of stay was 9 (2–30) days. Median time to first flatus was 3 (2–6) days. An abdominal drain was placed in 9 patients and was removed at median postoperative day 3. Ninety-day mortality and readmission rates were nil. One anastomotic leakage occurred at postoperative day 5 in a patient presenting with fever and was confirmed by an esophagogastroduodenal transit and a CT scan. The patient was treated with 15 days of antibiotics and drain removal was delayed till postoperative day 15. One Petersen's space hernia¹⁶ was diagnosed at postoperative day 11 by CT scan in a patient presenting with nausea and vomiting, requiring surgical revision that was performed by laparoscopy with conversion to open surgery due to an important occlusion and lack of space to maneuver. An evisceration then occurred in this patient 10 days after the first revision requiring a second surgical revision.

Table 4.

Postoperative Outcomes

	n	Median	Range
Time to first flatus (days)		3	2–6
Length of hospital stay (days)		9	2–30
Ninety-day mortality	0
Ninety-day readmission	0

Discussion

Gastrectomy remains the only curative treatment for gastric cancer. The laparoscopic minimally invasive approach for distal gastrectomy has been validated and is associated with better postoperative outcomes. However, laparoscopic total gastrectomy remains controversial because of lymphadenectomy and digestive restoration difficulties, leading to a longer learning curve.⁸ To overcome those drawbacks, Giulianotti reported the first robotic gastrectomy.¹⁷ Robotics' 3D visualization, tremor control, and larger range of motion help to overcome the weaknesses of laparoscopic techniques. Several retrospective and prospective randomized studies mostly emerging from Asia validated the short-term safety and the oncological efficacy of robotic gastrectomy.^11–13 Nevertheless, robotic total gastrectomy remains marginal.⁷

This report is one of the few studies evaluating the feasibility of full robotic total gastrectomy with intracorporal robot-sewn anastomosis.¹² Robot-assisted total gastrectomy was performed in all consecutive patients without conversion to open surgery, confirming safety and feasibility in a nonselected population. Several studies have proved the substantial equivalence of laparoscopic and robotic approach in being able to complete the minimally invasive procedure.^13,18

Among the intraoperative outcomes, robot-assisted total gastrectomy was associated with a median blood loss of 150 mL and no blood support requirement. This study confirms lower blood loss in the minimally invasive approaches than in the open approach.¹⁰ The general consensus in the literature is the advantage of robotic surgery over laparoscopy and open surgery in reducing operative bleeding.¹¹

The median operative time was 198 minutes, which was longer than that of published open surgery in the literature.¹⁰ However, we consider the longer operative time justified by the short-term outcomes such as shorter hospital stay and lower level of perioperative bleeding and pain.¹³ The longer operative time for robot-assisted total gastrectomy is also due to the time required for the robot preparation. In our experience, docking required a median time of 19 minutes, which compares well from previous published robotic gastrectomy series.

The main laparoscopic gastrectomy's draw back lies in the digestive track reconstruction difficulty. In fact, laparoscopic Roux-en-Y esophagojejunostomy performed in a narrow surgical field is technically demanding. To avoid those limitations, a variety of techniques have been described. Some groups have used a circular stapling device through a small upper abdominal laparotomy that can lead to some limitations particularly in obese patients with thick abdominal walls.¹⁹ Others have described an extracorporeal esophagojejunostomy through a small upper laparotomy, but the deeper location of the esophageal stump increases postoperative reconstruction complications such as ileus, roux stasis leakage, and anastomosis strictures.¹⁹ The use of linear staplers for esophagojejunostomy has been reported but it requires extensive dissection of the distal esophagus, which can lead to more bleeding and further development of hiatal hernia.²⁰ A transoral anvil insertion has been also described and can facilitate esophagojejunostomy.²¹ The pitfall of this reconstruction is the hypopharyngeal or esophageal mucosal injury.²¹ Robotic sewn intracorporal anastomosis required median time of 25 minutes. It avoided a laparotomy and unnecessary dissection on the distal esophagus. In the literature, this simple reconstruction method is associated with a shorter learning curve; however, no significant difference has been proven regarding anastomotic leakage and stricture.^13,18,22

Since surgery is the only curative treatment, the most relevant issue is ensuring proper oncological treatment by performing an adequate lymphadenectomy. Median number of retrieved lymph nodes in this report was 15 and infiltrated margins were low. These results complied with the European Society for medical oncology's clinical practice guidelines for gastric cancer.¹ Proper lymphadenectomy defined by retrieval of 15 or more lymph nodes remains a major factor influencing long-term survival.^1,14,23 Suda et al. first reported the advantage of the robotic approach in performing D2 lymphadenectomy²⁴ but D2 dissection's cost-effectiveness remains controversial.^23,25 In our preliminary evaluation, 3 patients had a microscopically positive proximal margin, but no conclusion could be drawn due to the study design. In the literature, robot-assisted gastrectomy is associated with oncological outcomes comparable with the laparoscopic or open approach.¹²

In the analysis of the postoperative course, there were one grade II and one grade IIIb (Clavien–Dindo) postoperative complications.²⁶ In the recent literature, Hyun et al. reported similar results regarding overall complications with higher rate of grades IIIa and IIIb (Clavien–Dindo) complications in the laparoscopic group.¹⁸ Systematic drainage was decided for the first nine gastrectomies. Given the safety of the first procedures regarding anastomotic leakage and bleeding, the drain placement was then discontinued.

Minimally invasive gastrectomy has demonstrated relevant advantages over open gastrectomy with regard to postoperative hospital stay and quicker oral intake.^13,18,27 Lesser tissue manipulation with smaller instruments when using the robot could explain those results. However, differences can be seen in the literature. For example, Junfeng et al. reported no differences regarding oral intake and postoperative hospital stay.²⁸ We report a median postoperative hospital stay of 9 days and a median time to first flatus of 3 days. The gap between transit resumption and postoperative hospital stay was due to certain organizational limitations such as time required to provide a convalescent home. Improvements in this regard are expected in the future to reduce the cost-effectiveness of robotic gastrectomy.

Conclusion

Robot-assisted total gastrectomy with intracorporal suture anastomosis for gastric cancer is safe and feasible. This approach shortens the minimally invasive total gastrectomy learning. Robotic approach could be used to extend minimally invasive surgery application for gastric cancer. Further studies are required to establish its short- and long-term efficacy and cost-effectiveness.

Footnotes

Acknowledgments

The funding agencies had no role in the collection, analysis, and interpretation of data and in the writing of the article. No preregistration exists for the study reported in this article. Authors' data, analytic methods, and study materials will not be available to other researchers. The authors are grateful to Jawad Hamad, MD, FRCS (Coventry University Hospital, Coventry, UK) and Nicolas Tabchouri, MD (CHU, Tours, France) for help provided in the writing of this article.

Disclosure Statement

O.S.M. declares consultancy activities for Intuitive Surgical (Sunnyvale, CA). The authors declare no other conflict of interest.

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