TECHNICAL REPORT
Hand-assisted Laparoscopic Total Gastrectomy With Regional Lymph Node Dissection for Advanced Gastric Cancer Guang-tan Zhang, MD, PhD, Yu-cheng Song, MD, and Xue-dong Zhang, MD
Background and Objectives: Laparoscopic-assisted distal gastrectomy has been applied to the treatment of gastric cancer. However, there have been few reports on the laparoscopic-assisted total gastrectomy for advanced gastric cancer, mainly because of the difficulty of the procedure. Methods: Here, we report a series of cases where the hand-assisted laparoscopic total gastrectomies with regional lymph node dissection were performed successfully. Results: The average operative time was 245 minutes. The mean blood loss was 110 mL. The number of dissected lymph nodes per patient was beyond 15 nodes satisfying a reliable evaluation of nodal status. All resection specimens had no residual tumor at the proximal or distal resection margins. The mean oral feeding was 3.6 days. The mean postoperative length of stay was 8.7 days. Conclusions: The hand-assisted laparoscopic D2 total gastrectomy for advanced gastric cancer is both technically feasible and safe. Key Words: total gastrectomy, hand-assisted laparoscopic surgery, advanced gastric cancer, Roux-en-Y reconstruction, lymph node dissection
(Surg Laparosc Endosc Percutan Tech 2014;24:e78–e84)
L
aparoscopic surgery has many advantages, such as, reduced pain, better cosmetic outcomes, fewer wound and respiratory complications, earlier recovery, shorter hospital stay, and better quality of life after operation.1 The development and improvement of new devices and skills have made laparoscopic surgery so widely applicable that numerous procedures have been attempted with this technique and demonstrated its safety.1–4 However, the use of laparoscopic surgery for the treatment of advanced gastric cancer remains controversial for the technical difficulty of tedious lymph node (LN) dissection and gastrointestinal continuity reconstruction.2 With the development of a hand-access device, the surgeon can insert a hand inside the abdomen; because of its highly versatile motor skills and fine tactile sense, complex laparoscopic operations can be performed similarly to the conventional open procedure and probably more easily than the total laparoscopic or laparoscopic-assisted procedure.5 Here, we report our technique for hand-assisted laparoscopic total gastrectomy Received for publication October 13, 2012; accepted December 3, 2012. From the Department of General Surgery, Henan Provincial People’s Hospital, Zhengzhou, China. G.Z. and Y.S. contributed equally to this study. The authors declare no conflicts of interest. Reprints: Xue-dong Zhang, MD, Department of General Surgery, Henan Provincial People’s Hospital, Zhengzhou 450003, China (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins
e78 | www.surgical-laparoscopy.com
(HALTG) with extensive D2 LN dissection for advanced gastric cancer and the initial clinical results.
PATIENTS AND METHODS Patients Because HALTG was a new surgical technique, in the study period, we prudently selected patients for handassisted laparoscopic surgery (HALS). High-risk patients through preoperative multidisciplinary consultation were not suitable for laparoscopic surgery and excluded from this study. High-risk patients classification included: (1) previous abdominal laparotomy; (2) above 80 years of age; (3) body mass index (BMI) > 35 m/kg2; (4) operative cardiovascular risk greater than New York Heart Association II; (5) operative pulmonary risk greater than Hugh-Jones II; and (6) severe liver disease (Child classes B and C) and renal dysfunction. In addition, the type I gastroesophageal junction (GEJ) cancers6 that need esophagectomy through a right thoracotomy were also excluded from this study. Between October 2010 and December 2011, 78 patients in the Department of General Surgery, Henan Provincial Hospital underwent HALTG with Roux-en-Y reconstruction for advanced gastric cancer located in GEJ, the upper third, the middle third, or the whole stomach. Five patients underwent hand-assisted laparoscopic D1 palliative total gastrectomy because peritoneal metastatic diseases were noted at laparoscopy or free cancer cells were found in the lavage fluid during the operation. Those 5 patients’ data were excluded from this study. Forty-two patients underwent HALTG and spleen-preserving laparoscopic D2 lymphadenectomy with removing the lymphatic tissue at the splenic hilum and around the splenic artery. Among the remaining 31 patients, 28 patients underwent HALTG with splenectomy because of T2-T4 tumors invading the greater curvature of the upper stomach or direct cancer invasion to the spleen, and 3 patients underwent HALTG with distal pancreaticosplenectomy because of direct cancer invasion to the pancreas. All patients were informed about the novelty of HALS, the surgeon’s experience with laparoscopic surgery, and signed a surgical consent indicating that the handaccess device would be used. Demographic details, perioperative data such as operative time, estimated blood loss, length of postoperative hospital stay, and the details of postoperative complications were reviewed.
Surgical Technique Under general anesthesia, the patient was placed in the left hemilateral and reverse Trendelenburg position. The surgeon stood on the patient’s right, with the first assistant
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
FIGURE 1. Theater set up and trocars placement.
on the patient’s left, and the camera operator between the patient’s legs. The first 10-mm cannula at the level of the umbilicus was inserted, and a flexible electrolaparoscope was introduced through the infraumbilical port and used for visualization. At the beginning of each operation, the peritoneal cavity was carefully inspected, and cytologic examination by peritoneal lavage was performed to detect macroscopic or microscopic peritoneal dissemination of tumor cells. A 7-cm vertical incision was made in the high median upper portion and the HALS device (GelPort) and 2 trocars were placed (Fig. 1). The surgeon’s left hand was inserted into the abdomen through the GelPort. The greater omentum was lifted forward by the internal hand, and the transverse colon was held by the assistant with clamp. The greater omentum was detached from the transverse colon by ultrasonic shears. This dissection was carried out to the right until the right gastroepiploic vessels were identified. The surrounding lymphatics (LN station no. 4d and 6) were swept up with the vessels. To the left, the dissection was carried out to the lower pole of the spleen, and the left gastroepiploic vessels (LN station no. 4sa) and the short gastric vessels (LN station no. 4sb) were divided by clipping. The reflection of the lesser omentum on the liver was divided, starting at the right side of the hepatic hilum and working to the hiatus. The duodenum was mobilized and brought forward to the left side (Kocher maneuver) after the stomach lifted forward, the bifurcation of the gastroduodenal, common hepatic, and proper hepatic arteries was exposed. Next, the proper hepatic artery and portal vein were skeletonized using ultrasonic shears. This procedure allowed us to dissect LN station no. 12a and identify the root of the right gastric artery, which was subsequently divided by clipping. After dissection of LN station nos. 12a and 5, the dissection was then advanced to remove the LNs along the branches of the celiac artery (stations no. 7, 8a, 9, and 11p), and the left gastric vein and artery were exposed and divided with double clips (Fig. 2). The left hand held the spleen gently and medially retracted and rotated it. The splenorenal ligament was incised, extending upward to the left side of the esophagus. r
2014 Lippincott Williams & Wilkins
HALTG for Gastric Cancer
FIGURE 2. Inscription of the lymph node number of the total gastrectomy according to the Japanese Classification of Gastric Carcinoma (13th edition).
Next, the retroperitoneum along the inferior edge of the pancreatic tail was incised, and this incision continued to the first cutting line of the splenorenal ligament. Medial and ventral rotation of the spleen and pancreatic tail was performed gently by the left hand, and mobilization of the pancreatic tail from the retroperitoneum was started, and this continued to the left side of the abdominal aorta. Next, the mobilized spleen and the distal pancreas were delivered outside through the GelPort. The fatty tissue including LN station no. 10 was removed from the splenic hilum extracorporeally using conventional open operation techniques, but all vessels in the splenic hilum were saved to preserve the spleen. Next, the fatty tissue, including LN station no. 11d, was similarly removed along the distal splenic artery. After removing LN station no. 10 and 11d extracorporeally, the mobilized spleen and the distal pancreas were delivered inside through the GelPort and repositioned in the abdominal cavity in the method preserving the spleen and pancreas (Fig. 3). In the condition of splenectomy or distal pancreaticosplenectomy, the splenic artery and vein were ligated and divided at the splenic hilum, and splenectomy or distal pancreaticosplenectomy was performed extracorporeally to remove LN station no. 10 and 11d with the spleen and pancreatic tail. The pancreatic stump was handled with cautery, fibrin glue, and omental patches. Next step was adequately exposing and mobilizing the distal esophagus. The phrenoesophageal membrane and vagal nerves were divided using ultrasonic shears. For 27 cases of types II and III GEJ cancers,6 the hiatus was enlarged, and the inserted hand moderately pulled the esophagus in the caudal direction. On the right side of the esophagus, the aorta was approached at the level of the hiatus and in an avascular plane dissected free as high as possible in the posterior mediastinum. Anteriorly along the pericardium, dissection was performed in an avascular plane high in the anterior mediastinum, with visualization of the pericardium and pulmonary vein up and the lower thoracic paraesophageal nodes (no. 110 LNs) was dissected. www.surgical-laparoscopy.com |
e79
Zhang et al
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
FIGURE 3. The extracorporeal dissection of lymph nodes no. 11d and 10. A, Spleen and distal pancreas were delivered outside. B, The spleen and the distal pancreas were repositioned in the abdominal cavity.
Lateral dissection was performed carefully on both sides at the level of the pleurae. Then, reconstruction was performed by Roux-en-Y method step-by-step using improved anastomotic techniques. First, the exposed esophagus was partly dissected on flank by ultrasonic shears. The anvil head of circular stapler with 2-0 prolene and suture needle was inserted into the esophagus through the flank incision. Second, after the suture needle was punctured outside the esophagus, the esophagus was transected below the site of puncture using an endoscopic linear stapler. Third, the prolene was carefully pulled and the anvil head of circular stapler was punctured through the esophagus stump (Fig. 4). After above revolutionary steps, duodenal transection was performed with a 55-mm linear stapler and the mobilized full stomach was delivered through the GelPort. The jejunum was divided at a point 20 cm distal to the ligament of Treitz. The jejunojejunal anastomosis was performed extracorporeally. Next, the steps of esophagojejunostomy were also revolutionary. First, the shaft of the circular stapler was introduced into the distal segment of the jejunum and was placed inside the abdominal cavity
through the GelPort. Second, the pneumoperitoneum was reestablished after the GelPort was closed, and the previously inserted anvil head was attached to the stapler trocar, and the anvil and circular stapler were approximated. Adjacent organs and adipose tissues were inspected carefully under the fine view of laparoscopy to prevent inadvertent involvement of adjacent tissues between the anastomosis, after which the stapler was fired and an endto-side esophagojejunostomy was finished. Third, the jejunal stump was closed with an endoscopic linear stapler (Fig. 5). The abdominal cavity was checked, and the incision was closed. Two silicon drainage tubes were placed through the trocar wounds before the wound was closed. One was placed around the esophagojejunal anastomosis. The other was inserted into left subphrenic space.
RESULTS In all patients, the procedure was completed without conversion to open operation. None of the patients needed unintentional splenectomy because of vascular injury to
FIGURE 4. New method of anvil insertion. A, The anvil head of circular stapler with 2-0 prolene. B, The anvil head of circular stapler was inserted into the dissected esophagus. C, The esophagus was transected using an endoscopic linear stapler. D, The anvil head of circular stapler was punctured through the esophagus stump.
e80 | www.surgical-laparoscopy.com
r
2014 Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
HALTG for Gastric Cancer
FIGURE 5. The improved esophageal-jejunum anastomosis. A, The shaft of the circular stapler was placed inside the abdominal cavity through the GelPort. B, The shaft of the circular stapler was introduced into the distal segment of the jejunum. C, An end-to-side esophagojejunostomy. D, The jejunal stump was closed with an endoscopic linear stapler.
splenic hilar area or splenic parenchyma, but partial splenic infarction was observed in 4 patients who all recovered with no infarction-related complications. Two patients experienced intraoperative pleural tear with no postoperative pulmonary complications after successful intraoperative repair. The mean average age was 62.4 years (range, 40 to 84 y) and male-female ratio 47:26. The mean BMI of the patients was 24.8 (range, 22.4 to 29.5). The average operative time was 245 minutes (range, 210 to 350 min). The mean blood loss was 110 mL (range, 50 to 200 mL), and blood transfusions were not required. The mean number of harvested LNs was 26.9 (range, 19 to 44) and the number of harvested LNs per patient was beyond 15 nodes satisfying a reliable evaluation of nodal status. The pathologic results were listed in the Table 1. In our study, we classified GEJ cancers according to Siewert and Stein’s classification.6 That is, the whole 27 GEJ cancers were categorized as type II tumors (range from 1 cm above to 2 cm below the junction) in 11 cases, and type III tumors (between 2 and 5 cm below the GEJ) in 16 cases. All resection specimens had no residual tumor at the proximal or distal resection margins. The mean oral feeding was 3.6 days (range, 2 to 5 d). The median postoperative length of stay was 8 days (range, 6 to 17 d). Postoperative fluorography was performed on postoperative days 5 to 7 in all patients and demonstrated no leakage or stenosis of esophagojejunal anastomosis. There was no 30-day or in-hospital mortality after surgery. A total of 12 postoperative complications occurred in 9 patients (12%). One patient subjected to a concurrent distal pancreaticosplenectomy experienced pancreatic fistula and were treated conservatively with a drain placement during the initial operation. Postoperative abdominal abscess was detected in 2 patients, 1 of whom recovered after conservative treatment with a drain and 1 of whom required computed tomography–guided drainage. Pleural effusion in r
2014 Lippincott Williams & Wilkins
2 patients required ultrasonic positioning puncture. Other complications included wound infection in 2 patients, pulmonary infection in 4, and postoperative adhesions in 1 patient who need for readmission. Such complications resolved with conservative treatment. Seventy patients with T2-T4 tumors or cT1N + tumors according to postoperative pathologic results received S-1 neoadjuvant therapy. All the patients were followed up for 7 to 35 months (mean follow-up period:
TABLE 1. The Pathologic Results
Characteristics
No. Patients (N = 73) (%)
Tumor size (cm) Retrieved LNs Retrieved LN station 10 Retrieved LN station 11d Proximal margin (cm) Distal margin (cm) Location Gastroesophageal junction Upper Middle Whole AJCC/UICC staging T classification Mucosa Submucosa Proper muscle Subserosa N classification N0 N1 N2
2.8 ± 1.1 26.9 ± 9.7 2.3 ± 0.4 1.5 ± 0.2 5.13 ± 1.01 6.02 ± 0.95 27 (40%) 31 (42.5%) 11 (15.1%) 4 (5.4%) 1 (1.4%) 3 (4.1%) 65 (89%) 4 (5.5%) 10 (13.7%) 59 (80.8%) 4 (5.5%)
LN indicates lymph node.
www.surgical-laparoscopy.com |
e81
Surg Laparosc Endosc Percutan Tech
Zhang et al
21.5 mo). Two patients died to date. The 1 patient who underwent HALTG and spleen-preserving lymphadenectomy was found to have abdominal metastases 4 months after surgery. The other patient who underwent HALTG and splenectomy had peritoneal metastasis 1 year after surgery and died 2 months later.
DISCUSSION HALS is a bridge between conventional open surgery and total laparoscopic surgery. The use of the internal hand allows rapid exploration, methodical dissection, identification of crucial structures, rapid control of major bleeding, and expeditious performance of a procedure because of the maintenance of the tactile sensation. Our department has adopted GelPort to perform HALS for gastric cancer for 3 years and explored a few surgical techniques different from other reports.7–9 There are 3 types of incisions with HALS for gastric carcinoma: the right lower quadrant oblique incisions, vertical, and transverse incisions in the high median upper portion reported in literature.7–9 We choose the vertical incisions in the high median upper portion for HALS. In our experience, the complex surgical procedures, such as esophageal-jejunum anastomosis and LN dissection for station 10 and 11d, are rather difficult to perform through the right lower quadrant oblique incisions, although the incisions may be associated with more esthetic healing and less pain than the upper midline incisions. In the reported literature,10–12 the transverse incisions resulted in less postoperative pain, and fewer pulmonary complications, burst abdomens, and incisional hernias than the vertical incisions. However, the transverse incisions may be associated with significantly more blood loss than the midline incisions,13 because mural vessels are divided. In the condition of converting to laparotomy, the transverse incisions may be of limited value, as the possibility for extension is limited to gain emergency access to the abdomen. The current standard of care for resectable locally advanced gastric cancer, in Japan and Europe, is R0 gastrectomy with extensive D2 LN dissection.14 LN dissection for station 10 and 11d is necessary in standard LN dissection for advanced gastric cancer located in the GEJ, the upper third, the middle third, or the whole stomach. Splenectomy and peripheral pancreatectomy are usually performed in D2 lympadenectomy to provide complete removal of LN station 11d and 10, which are responsible for a significantly higher morbidity and mortality.15 In the literatures, the incidence of pancreatic fistula after distal pancreatectomy varied from 20% to 33%.16–18 In our study, the pancreatic fistula rate in patients with partial pancreatectomy appeared to be 33% that was equivalent to other reports. In recent 4 partial pancreatectomies, we transected the pancreatic tail with stapler and sutured the main pancreatic duct with 2-0 prolene, and there was no pancreatic fistula. However, the survival benefit of splenectomy and peripheral pancreatectomy in potentially curative total gastrectomy is not yet established.19–21 These concomitant resections are no longer considered necessary unless there is evidence of LN station 11d and 10 or even the tumor directly invades the spleen or the pancreatic tail.21 On the condition of preserving the spleen and pancreatic tail, removal of LN station 11d, in advanced gastric cancer is difficult to perform laparoscopically because of its
e82 | www.surgical-laparoscopy.com
Volume 24, Number 3, June 2014
location behind the pancreatic tail. Similarly, removal of LN station 10 with skeletonization of the vessels at the splenic hilum is difficult to perform laparoscopically. Those anatomic complexities of the vascular structures and the technical limits of the conventional laparoscopic instrumentation complicate laparoscopic treatment even for minimally invasive well-trained surgeons. Such as, Cristiano et al22 reported abdominal hemorrhages from splenic lesion and unintentional splenectomy in the totally laparoscopic total and subtotal gastrectomy. We consider that HALS enables us to perform laparoscopic radical operation for advanced gastric cancer easily and safely. Indeed, mobilization of the spleen and distal pancreas from the retroperitoneum by HALS and their delivery through the GelPort allow us to perform the complicated procedures of skeletonization of the splenic hilum and the splenic artery, reliable dissection of LN 11d and LN 10, or distal pancreaticosplenectomy easily. For the patients with spleen-preserving lymphadenectomy, the number of retrieved LNs at station 10 and 11d, yield was 2.3 and 1.5, respectively. This result was the same as our yield with open surgery and validated by similar findings in the reported literature.23,24 In addition, none of the patients in our study needed unintentional splenectomy because of splenic lesion and the amount of blood loss was superior to other reports.22,25 Except for D2 LN dissection, R0 resection is another remarkable issue for oncological safety. In our research, oncologic curative resections were performed in all patients. For most cases, the surgeon’s left hand could locate resection margins easily and precisely with the help of fine tactile sense, and a proximal margin of at least 5 cm was ensured. However, R0 resection is especially difficult to be achieved for GEJ cancers because laparoscopic-assisted distal esophagus mobilization is technically difficult and the tumor border is difficult to examine in cases of tumor with infiltrative growth pattern. Although several suggested surgical approaches have been proposed, a united surgical strategy for the treatment of GEJ cancers has not yet been established.26–28 An approach through a right thoracotomy in combination with a laparotomy and cervical incision is associated with a significant rate of complications, especially pulmonary complications that will account for the long intensive care unit stay, and even for the mortality encountered.29 The transhiatal approach, according to Orringer and Sloan28 will reduce this complication rate by avoiding the opening of thoracic cavities, thereby reducing the number of pulmonary complications. However, the drawback of this approach is the blind character of the mediastinal dissection that can be performed only with some retractor of the heart with consequent hemodynamic instability. Van et al30 have experienced laparoscopic-assisted transhiatal approach for distal esophagus resection in 25 patients. He believed important advantages of the approach were the perfect visualization of the mediastinal structures in relation to the tumor up to the carina, making this operation no longer a blind procedure, and the avoidance of hemodynamic instability frequently found during the conventional dissection because of retractor use. In our study, we have duplicated this surgical approach in HALS manner for 27 GEJ cancers. Those postoperative pathologic results showed the rate of R0 resection was 100% that was considerably higher than other studies that reported a 55% to 75% rate of complete resection.31–33 We realize, with the r
2014 Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
hand of the surgeon in the abdomen and under laparoscopic vision, that the transhiatal approach is suitable for distal esophageal and junction tumors because it approaches the tumor directly on both sides in relation to both thoracic cavities and obtains tumor free resection margins easily. Laparoscopic reconstruction, especially esophagojejunostomy, is another complex technique. Laparoscopic esophagojejunostomy is generally performed using one of 2 reconstruction methods: the extracorporeal and intracorporeal methods.34,35 The traditional intracorporeal anastomosis using circular staplers need to place a purse-string suture on the esophageal stump in totally laparoscopic manner, which is a technically demanding and time-consuming procedure that requires a very skilled and experienced surgeon.36 In the process of suture, frequent delivery of the needle is necessary, and the sutures must be made holding the needle at any angle, which makes it a considerably difficult technique, and thus, it has a high risk of damaging the esophageal stump. In addition, judging the optimal degree of tightening is also difficult in intracorporeal ligation. Recently, the technique of transoral anvil insertion, which means the anvil is orally inserted and pulled out to the esophageal stump, has been reported.37–40 In this technique there is no need to perform purse-string suturing and the risk of esophageal injury during anvil insertion could be minimized. However, this technique requires the selection of an anvil
Hand-assisted Laparoscopic Total Gastrectomy With Regional Lymph Node Dissection for Advanced Gastric Cancer Guang-tan Zhang, MD, PhD, Yu-cheng Song, MD, and Xue-dong Zhang, MD
Background and Objectives: Laparoscopic-assisted distal gastrectomy has been applied to the treatment of gastric cancer. However, there have been few reports on the laparoscopic-assisted total gastrectomy for advanced gastric cancer, mainly because of the difficulty of the procedure. Methods: Here, we report a series of cases where the hand-assisted laparoscopic total gastrectomies with regional lymph node dissection were performed successfully. Results: The average operative time was 245 minutes. The mean blood loss was 110 mL. The number of dissected lymph nodes per patient was beyond 15 nodes satisfying a reliable evaluation of nodal status. All resection specimens had no residual tumor at the proximal or distal resection margins. The mean oral feeding was 3.6 days. The mean postoperative length of stay was 8.7 days. Conclusions: The hand-assisted laparoscopic D2 total gastrectomy for advanced gastric cancer is both technically feasible and safe. Key Words: total gastrectomy, hand-assisted laparoscopic surgery, advanced gastric cancer, Roux-en-Y reconstruction, lymph node dissection
(Surg Laparosc Endosc Percutan Tech 2014;24:e78–e84)
L
aparoscopic surgery has many advantages, such as, reduced pain, better cosmetic outcomes, fewer wound and respiratory complications, earlier recovery, shorter hospital stay, and better quality of life after operation.1 The development and improvement of new devices and skills have made laparoscopic surgery so widely applicable that numerous procedures have been attempted with this technique and demonstrated its safety.1–4 However, the use of laparoscopic surgery for the treatment of advanced gastric cancer remains controversial for the technical difficulty of tedious lymph node (LN) dissection and gastrointestinal continuity reconstruction.2 With the development of a hand-access device, the surgeon can insert a hand inside the abdomen; because of its highly versatile motor skills and fine tactile sense, complex laparoscopic operations can be performed similarly to the conventional open procedure and probably more easily than the total laparoscopic or laparoscopic-assisted procedure.5 Here, we report our technique for hand-assisted laparoscopic total gastrectomy Received for publication October 13, 2012; accepted December 3, 2012. From the Department of General Surgery, Henan Provincial People’s Hospital, Zhengzhou, China. G.Z. and Y.S. contributed equally to this study. The authors declare no conflicts of interest. Reprints: Xue-dong Zhang, MD, Department of General Surgery, Henan Provincial People’s Hospital, Zhengzhou 450003, China (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins
e78 | www.surgical-laparoscopy.com
(HALTG) with extensive D2 LN dissection for advanced gastric cancer and the initial clinical results.
PATIENTS AND METHODS Patients Because HALTG was a new surgical technique, in the study period, we prudently selected patients for handassisted laparoscopic surgery (HALS). High-risk patients through preoperative multidisciplinary consultation were not suitable for laparoscopic surgery and excluded from this study. High-risk patients classification included: (1) previous abdominal laparotomy; (2) above 80 years of age; (3) body mass index (BMI) > 35 m/kg2; (4) operative cardiovascular risk greater than New York Heart Association II; (5) operative pulmonary risk greater than Hugh-Jones II; and (6) severe liver disease (Child classes B and C) and renal dysfunction. In addition, the type I gastroesophageal junction (GEJ) cancers6 that need esophagectomy through a right thoracotomy were also excluded from this study. Between October 2010 and December 2011, 78 patients in the Department of General Surgery, Henan Provincial Hospital underwent HALTG with Roux-en-Y reconstruction for advanced gastric cancer located in GEJ, the upper third, the middle third, or the whole stomach. Five patients underwent hand-assisted laparoscopic D1 palliative total gastrectomy because peritoneal metastatic diseases were noted at laparoscopy or free cancer cells were found in the lavage fluid during the operation. Those 5 patients’ data were excluded from this study. Forty-two patients underwent HALTG and spleen-preserving laparoscopic D2 lymphadenectomy with removing the lymphatic tissue at the splenic hilum and around the splenic artery. Among the remaining 31 patients, 28 patients underwent HALTG with splenectomy because of T2-T4 tumors invading the greater curvature of the upper stomach or direct cancer invasion to the spleen, and 3 patients underwent HALTG with distal pancreaticosplenectomy because of direct cancer invasion to the pancreas. All patients were informed about the novelty of HALS, the surgeon’s experience with laparoscopic surgery, and signed a surgical consent indicating that the handaccess device would be used. Demographic details, perioperative data such as operative time, estimated blood loss, length of postoperative hospital stay, and the details of postoperative complications were reviewed.
Surgical Technique Under general anesthesia, the patient was placed in the left hemilateral and reverse Trendelenburg position. The surgeon stood on the patient’s right, with the first assistant
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
FIGURE 1. Theater set up and trocars placement.
on the patient’s left, and the camera operator between the patient’s legs. The first 10-mm cannula at the level of the umbilicus was inserted, and a flexible electrolaparoscope was introduced through the infraumbilical port and used for visualization. At the beginning of each operation, the peritoneal cavity was carefully inspected, and cytologic examination by peritoneal lavage was performed to detect macroscopic or microscopic peritoneal dissemination of tumor cells. A 7-cm vertical incision was made in the high median upper portion and the HALS device (GelPort) and 2 trocars were placed (Fig. 1). The surgeon’s left hand was inserted into the abdomen through the GelPort. The greater omentum was lifted forward by the internal hand, and the transverse colon was held by the assistant with clamp. The greater omentum was detached from the transverse colon by ultrasonic shears. This dissection was carried out to the right until the right gastroepiploic vessels were identified. The surrounding lymphatics (LN station no. 4d and 6) were swept up with the vessels. To the left, the dissection was carried out to the lower pole of the spleen, and the left gastroepiploic vessels (LN station no. 4sa) and the short gastric vessels (LN station no. 4sb) were divided by clipping. The reflection of the lesser omentum on the liver was divided, starting at the right side of the hepatic hilum and working to the hiatus. The duodenum was mobilized and brought forward to the left side (Kocher maneuver) after the stomach lifted forward, the bifurcation of the gastroduodenal, common hepatic, and proper hepatic arteries was exposed. Next, the proper hepatic artery and portal vein were skeletonized using ultrasonic shears. This procedure allowed us to dissect LN station no. 12a and identify the root of the right gastric artery, which was subsequently divided by clipping. After dissection of LN station nos. 12a and 5, the dissection was then advanced to remove the LNs along the branches of the celiac artery (stations no. 7, 8a, 9, and 11p), and the left gastric vein and artery were exposed and divided with double clips (Fig. 2). The left hand held the spleen gently and medially retracted and rotated it. The splenorenal ligament was incised, extending upward to the left side of the esophagus. r
2014 Lippincott Williams & Wilkins
HALTG for Gastric Cancer
FIGURE 2. Inscription of the lymph node number of the total gastrectomy according to the Japanese Classification of Gastric Carcinoma (13th edition).
Next, the retroperitoneum along the inferior edge of the pancreatic tail was incised, and this incision continued to the first cutting line of the splenorenal ligament. Medial and ventral rotation of the spleen and pancreatic tail was performed gently by the left hand, and mobilization of the pancreatic tail from the retroperitoneum was started, and this continued to the left side of the abdominal aorta. Next, the mobilized spleen and the distal pancreas were delivered outside through the GelPort. The fatty tissue including LN station no. 10 was removed from the splenic hilum extracorporeally using conventional open operation techniques, but all vessels in the splenic hilum were saved to preserve the spleen. Next, the fatty tissue, including LN station no. 11d, was similarly removed along the distal splenic artery. After removing LN station no. 10 and 11d extracorporeally, the mobilized spleen and the distal pancreas were delivered inside through the GelPort and repositioned in the abdominal cavity in the method preserving the spleen and pancreas (Fig. 3). In the condition of splenectomy or distal pancreaticosplenectomy, the splenic artery and vein were ligated and divided at the splenic hilum, and splenectomy or distal pancreaticosplenectomy was performed extracorporeally to remove LN station no. 10 and 11d with the spleen and pancreatic tail. The pancreatic stump was handled with cautery, fibrin glue, and omental patches. Next step was adequately exposing and mobilizing the distal esophagus. The phrenoesophageal membrane and vagal nerves were divided using ultrasonic shears. For 27 cases of types II and III GEJ cancers,6 the hiatus was enlarged, and the inserted hand moderately pulled the esophagus in the caudal direction. On the right side of the esophagus, the aorta was approached at the level of the hiatus and in an avascular plane dissected free as high as possible in the posterior mediastinum. Anteriorly along the pericardium, dissection was performed in an avascular plane high in the anterior mediastinum, with visualization of the pericardium and pulmonary vein up and the lower thoracic paraesophageal nodes (no. 110 LNs) was dissected. www.surgical-laparoscopy.com |
e79
Zhang et al
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
FIGURE 3. The extracorporeal dissection of lymph nodes no. 11d and 10. A, Spleen and distal pancreas were delivered outside. B, The spleen and the distal pancreas were repositioned in the abdominal cavity.
Lateral dissection was performed carefully on both sides at the level of the pleurae. Then, reconstruction was performed by Roux-en-Y method step-by-step using improved anastomotic techniques. First, the exposed esophagus was partly dissected on flank by ultrasonic shears. The anvil head of circular stapler with 2-0 prolene and suture needle was inserted into the esophagus through the flank incision. Second, after the suture needle was punctured outside the esophagus, the esophagus was transected below the site of puncture using an endoscopic linear stapler. Third, the prolene was carefully pulled and the anvil head of circular stapler was punctured through the esophagus stump (Fig. 4). After above revolutionary steps, duodenal transection was performed with a 55-mm linear stapler and the mobilized full stomach was delivered through the GelPort. The jejunum was divided at a point 20 cm distal to the ligament of Treitz. The jejunojejunal anastomosis was performed extracorporeally. Next, the steps of esophagojejunostomy were also revolutionary. First, the shaft of the circular stapler was introduced into the distal segment of the jejunum and was placed inside the abdominal cavity
through the GelPort. Second, the pneumoperitoneum was reestablished after the GelPort was closed, and the previously inserted anvil head was attached to the stapler trocar, and the anvil and circular stapler were approximated. Adjacent organs and adipose tissues were inspected carefully under the fine view of laparoscopy to prevent inadvertent involvement of adjacent tissues between the anastomosis, after which the stapler was fired and an endto-side esophagojejunostomy was finished. Third, the jejunal stump was closed with an endoscopic linear stapler (Fig. 5). The abdominal cavity was checked, and the incision was closed. Two silicon drainage tubes were placed through the trocar wounds before the wound was closed. One was placed around the esophagojejunal anastomosis. The other was inserted into left subphrenic space.
RESULTS In all patients, the procedure was completed without conversion to open operation. None of the patients needed unintentional splenectomy because of vascular injury to
FIGURE 4. New method of anvil insertion. A, The anvil head of circular stapler with 2-0 prolene. B, The anvil head of circular stapler was inserted into the dissected esophagus. C, The esophagus was transected using an endoscopic linear stapler. D, The anvil head of circular stapler was punctured through the esophagus stump.
e80 | www.surgical-laparoscopy.com
r
2014 Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
HALTG for Gastric Cancer
FIGURE 5. The improved esophageal-jejunum anastomosis. A, The shaft of the circular stapler was placed inside the abdominal cavity through the GelPort. B, The shaft of the circular stapler was introduced into the distal segment of the jejunum. C, An end-to-side esophagojejunostomy. D, The jejunal stump was closed with an endoscopic linear stapler.
splenic hilar area or splenic parenchyma, but partial splenic infarction was observed in 4 patients who all recovered with no infarction-related complications. Two patients experienced intraoperative pleural tear with no postoperative pulmonary complications after successful intraoperative repair. The mean average age was 62.4 years (range, 40 to 84 y) and male-female ratio 47:26. The mean BMI of the patients was 24.8 (range, 22.4 to 29.5). The average operative time was 245 minutes (range, 210 to 350 min). The mean blood loss was 110 mL (range, 50 to 200 mL), and blood transfusions were not required. The mean number of harvested LNs was 26.9 (range, 19 to 44) and the number of harvested LNs per patient was beyond 15 nodes satisfying a reliable evaluation of nodal status. The pathologic results were listed in the Table 1. In our study, we classified GEJ cancers according to Siewert and Stein’s classification.6 That is, the whole 27 GEJ cancers were categorized as type II tumors (range from 1 cm above to 2 cm below the junction) in 11 cases, and type III tumors (between 2 and 5 cm below the GEJ) in 16 cases. All resection specimens had no residual tumor at the proximal or distal resection margins. The mean oral feeding was 3.6 days (range, 2 to 5 d). The median postoperative length of stay was 8 days (range, 6 to 17 d). Postoperative fluorography was performed on postoperative days 5 to 7 in all patients and demonstrated no leakage or stenosis of esophagojejunal anastomosis. There was no 30-day or in-hospital mortality after surgery. A total of 12 postoperative complications occurred in 9 patients (12%). One patient subjected to a concurrent distal pancreaticosplenectomy experienced pancreatic fistula and were treated conservatively with a drain placement during the initial operation. Postoperative abdominal abscess was detected in 2 patients, 1 of whom recovered after conservative treatment with a drain and 1 of whom required computed tomography–guided drainage. Pleural effusion in r
2014 Lippincott Williams & Wilkins
2 patients required ultrasonic positioning puncture. Other complications included wound infection in 2 patients, pulmonary infection in 4, and postoperative adhesions in 1 patient who need for readmission. Such complications resolved with conservative treatment. Seventy patients with T2-T4 tumors or cT1N + tumors according to postoperative pathologic results received S-1 neoadjuvant therapy. All the patients were followed up for 7 to 35 months (mean follow-up period:
TABLE 1. The Pathologic Results
Characteristics
No. Patients (N = 73) (%)
Tumor size (cm) Retrieved LNs Retrieved LN station 10 Retrieved LN station 11d Proximal margin (cm) Distal margin (cm) Location Gastroesophageal junction Upper Middle Whole AJCC/UICC staging T classification Mucosa Submucosa Proper muscle Subserosa N classification N0 N1 N2
2.8 ± 1.1 26.9 ± 9.7 2.3 ± 0.4 1.5 ± 0.2 5.13 ± 1.01 6.02 ± 0.95 27 (40%) 31 (42.5%) 11 (15.1%) 4 (5.4%) 1 (1.4%) 3 (4.1%) 65 (89%) 4 (5.5%) 10 (13.7%) 59 (80.8%) 4 (5.5%)
LN indicates lymph node.
www.surgical-laparoscopy.com |
e81
Surg Laparosc Endosc Percutan Tech
Zhang et al
21.5 mo). Two patients died to date. The 1 patient who underwent HALTG and spleen-preserving lymphadenectomy was found to have abdominal metastases 4 months after surgery. The other patient who underwent HALTG and splenectomy had peritoneal metastasis 1 year after surgery and died 2 months later.
DISCUSSION HALS is a bridge between conventional open surgery and total laparoscopic surgery. The use of the internal hand allows rapid exploration, methodical dissection, identification of crucial structures, rapid control of major bleeding, and expeditious performance of a procedure because of the maintenance of the tactile sensation. Our department has adopted GelPort to perform HALS for gastric cancer for 3 years and explored a few surgical techniques different from other reports.7–9 There are 3 types of incisions with HALS for gastric carcinoma: the right lower quadrant oblique incisions, vertical, and transverse incisions in the high median upper portion reported in literature.7–9 We choose the vertical incisions in the high median upper portion for HALS. In our experience, the complex surgical procedures, such as esophageal-jejunum anastomosis and LN dissection for station 10 and 11d, are rather difficult to perform through the right lower quadrant oblique incisions, although the incisions may be associated with more esthetic healing and less pain than the upper midline incisions. In the reported literature,10–12 the transverse incisions resulted in less postoperative pain, and fewer pulmonary complications, burst abdomens, and incisional hernias than the vertical incisions. However, the transverse incisions may be associated with significantly more blood loss than the midline incisions,13 because mural vessels are divided. In the condition of converting to laparotomy, the transverse incisions may be of limited value, as the possibility for extension is limited to gain emergency access to the abdomen. The current standard of care for resectable locally advanced gastric cancer, in Japan and Europe, is R0 gastrectomy with extensive D2 LN dissection.14 LN dissection for station 10 and 11d is necessary in standard LN dissection for advanced gastric cancer located in the GEJ, the upper third, the middle third, or the whole stomach. Splenectomy and peripheral pancreatectomy are usually performed in D2 lympadenectomy to provide complete removal of LN station 11d and 10, which are responsible for a significantly higher morbidity and mortality.15 In the literatures, the incidence of pancreatic fistula after distal pancreatectomy varied from 20% to 33%.16–18 In our study, the pancreatic fistula rate in patients with partial pancreatectomy appeared to be 33% that was equivalent to other reports. In recent 4 partial pancreatectomies, we transected the pancreatic tail with stapler and sutured the main pancreatic duct with 2-0 prolene, and there was no pancreatic fistula. However, the survival benefit of splenectomy and peripheral pancreatectomy in potentially curative total gastrectomy is not yet established.19–21 These concomitant resections are no longer considered necessary unless there is evidence of LN station 11d and 10 or even the tumor directly invades the spleen or the pancreatic tail.21 On the condition of preserving the spleen and pancreatic tail, removal of LN station 11d, in advanced gastric cancer is difficult to perform laparoscopically because of its
e82 | www.surgical-laparoscopy.com
Volume 24, Number 3, June 2014
location behind the pancreatic tail. Similarly, removal of LN station 10 with skeletonization of the vessels at the splenic hilum is difficult to perform laparoscopically. Those anatomic complexities of the vascular structures and the technical limits of the conventional laparoscopic instrumentation complicate laparoscopic treatment even for minimally invasive well-trained surgeons. Such as, Cristiano et al22 reported abdominal hemorrhages from splenic lesion and unintentional splenectomy in the totally laparoscopic total and subtotal gastrectomy. We consider that HALS enables us to perform laparoscopic radical operation for advanced gastric cancer easily and safely. Indeed, mobilization of the spleen and distal pancreas from the retroperitoneum by HALS and their delivery through the GelPort allow us to perform the complicated procedures of skeletonization of the splenic hilum and the splenic artery, reliable dissection of LN 11d and LN 10, or distal pancreaticosplenectomy easily. For the patients with spleen-preserving lymphadenectomy, the number of retrieved LNs at station 10 and 11d, yield was 2.3 and 1.5, respectively. This result was the same as our yield with open surgery and validated by similar findings in the reported literature.23,24 In addition, none of the patients in our study needed unintentional splenectomy because of splenic lesion and the amount of blood loss was superior to other reports.22,25 Except for D2 LN dissection, R0 resection is another remarkable issue for oncological safety. In our research, oncologic curative resections were performed in all patients. For most cases, the surgeon’s left hand could locate resection margins easily and precisely with the help of fine tactile sense, and a proximal margin of at least 5 cm was ensured. However, R0 resection is especially difficult to be achieved for GEJ cancers because laparoscopic-assisted distal esophagus mobilization is technically difficult and the tumor border is difficult to examine in cases of tumor with infiltrative growth pattern. Although several suggested surgical approaches have been proposed, a united surgical strategy for the treatment of GEJ cancers has not yet been established.26–28 An approach through a right thoracotomy in combination with a laparotomy and cervical incision is associated with a significant rate of complications, especially pulmonary complications that will account for the long intensive care unit stay, and even for the mortality encountered.29 The transhiatal approach, according to Orringer and Sloan28 will reduce this complication rate by avoiding the opening of thoracic cavities, thereby reducing the number of pulmonary complications. However, the drawback of this approach is the blind character of the mediastinal dissection that can be performed only with some retractor of the heart with consequent hemodynamic instability. Van et al30 have experienced laparoscopic-assisted transhiatal approach for distal esophagus resection in 25 patients. He believed important advantages of the approach were the perfect visualization of the mediastinal structures in relation to the tumor up to the carina, making this operation no longer a blind procedure, and the avoidance of hemodynamic instability frequently found during the conventional dissection because of retractor use. In our study, we have duplicated this surgical approach in HALS manner for 27 GEJ cancers. Those postoperative pathologic results showed the rate of R0 resection was 100% that was considerably higher than other studies that reported a 55% to 75% rate of complete resection.31–33 We realize, with the r
2014 Lippincott Williams & Wilkins
Surg Laparosc Endosc Percutan Tech
Volume 24, Number 3, June 2014
hand of the surgeon in the abdomen and under laparoscopic vision, that the transhiatal approach is suitable for distal esophageal and junction tumors because it approaches the tumor directly on both sides in relation to both thoracic cavities and obtains tumor free resection margins easily. Laparoscopic reconstruction, especially esophagojejunostomy, is another complex technique. Laparoscopic esophagojejunostomy is generally performed using one of 2 reconstruction methods: the extracorporeal and intracorporeal methods.34,35 The traditional intracorporeal anastomosis using circular staplers need to place a purse-string suture on the esophageal stump in totally laparoscopic manner, which is a technically demanding and time-consuming procedure that requires a very skilled and experienced surgeon.36 In the process of suture, frequent delivery of the needle is necessary, and the sutures must be made holding the needle at any angle, which makes it a considerably difficult technique, and thus, it has a high risk of damaging the esophageal stump. In addition, judging the optimal degree of tightening is also difficult in intracorporeal ligation. Recently, the technique of transoral anvil insertion, which means the anvil is orally inserted and pulled out to the esophageal stump, has been reported.37–40 In this technique there is no need to perform purse-string suturing and the risk of esophageal injury during anvil insertion could be minimized. However, this technique requires the selection of an anvil
