Surg Today DOI 10.1007/s00595-014-0928-y
ORIGINAL ARTICLE
A novel laparoscopic procedure for treating proximal early gastric cancer: laparoscopy-assisted pylorus-preserving nearly total gastrectomy Tomoyoshi Takayama • Sohei Matsumoto • Kohei Wakatsuki • Tetsuya Tanaka • Kazuhiro Migita • Masahiro Ito • Yoshiyuki Nakajima
Received: 10 December 2013 / Accepted: 1 April 2014 Ó Springer Japan 2014
Abstract Purpose Pylorus-preserving nearly total gastrectomy (PPNTG) is a function-preserving gastrectomy for treating proximal early gastric cancer that prevents rapid gastric emptying and reflux. In this report, we present a surgical technique for performing laparoscopy-assisted PPNTG (LAPPNTG). Methods The resection of the stomach was similar to that during conventional total gastrectomy, with the key difference being that the pyloric cuff was preserved to a length of 3–4 cm. Compared with standard total gastrectomy, the lymph node dissection along the right gastric vessels and the infrapyloric vessels were omitted. Reconstruction was performed with a jejunal interposition that was 30 cm in length, with preservation of the marginal vessels in a retrocolic fashion. Results Thirteen patients with cT1 cN0 proximal gastric cancer underwent LAPPNTG at our institution. The median length of the operation and estimated blood loss were 329 min and 138 ml, respectively. All resected specimens had tumor-free margins, and the median number of removed lymph nodes was 40. There were no serious postoperative complications and no patients underwent conversion to laparotomy. Conclusions Performing LAPPNTG with a jejunal interposition is feasible and might be an appropriate treatment for proximal early gastric cancer.
T. Takayama (&) S. Matsumoto K. Wakatsuki T. Tanaka K. Migita M. Ito Y. Nakajima Department of Surgery, Nara Medical University, 840 Shijo-cho, 634-8522 Kashihara, Nara, Japan e-mail: [email protected]
Keywords Proximal gastric cancer Laparoscopic surgery Pylorus-preserving gastrectomy
Introduction In Japan, the standard surgical treatment for patients with gastric cancer in the upper portion of the stomach is total gastrectomy with D2 lymph node dissection. For patients with proximal early gastric cancer, the optimal extent of stomach resection and the method used for reconstruction were not been determined until quite recently. According to the Japanese Gastric Cancer Association guidelines [1] revised in 2011, proximal gastrectomy with D1 ? lymphadenectomy is defined as an alternative to total gastrectomy for patients with cT1 cN0 gastric cancer in the upper portion of the stomach. Pylorus-preserving gastrectomy to treat gastric ulcers was developed by Maki et al. [2] in 1967 to prevent reflux esophagitis and dumping syndrome. At that time, the pylorus-preserving technique had been applied to patients with early gastric cancer as a function-preserving procedure [3]. Pylorus-preserving gastrectomy is now accepted to be the standard option for treating middle-third early gastric cancer according to the Japanese guidelines. On the other hand, it has also been reported that the pylorus-preserving procedure could be applied for cases in which total gastrectomy was required [4]. The patients with gastric cancer who underwent the pylorus-preserving procedure after nearly total gastrectomy showed satisfactory results concerning dumping and reflux esophagitis. In our institute, an identical surgical procedure, named pylorus-preserving nearly total gastrectomy (PPNTG), has been performed in patients with proximal early gastric cancer. We have previously demonstrated the functional advantages and safety
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of PPNTG compared with conventional total gastrectomy [5]. Patients who undergo total gastrectomy with Roux-enY reconstruction frequently develop reflux symptoms and dumping syndrome, while PPNTG prevents patients from developing these post-gastrectomy disorders. Recently, new techniques for laparoscopy-assisted total gastrectomy (LATG) and proximal gastrectomy (LAPG) for proximal early gastric cancer have been reported [6–8], as laparoscopic surgery has continued to develop. Since January 2009, we have also performed laparoscopy-assisted pylorus-preserving nearly total gastrectomy (LAPPNTG) in patients with proximal early gastric cancer. There have been no major complications or patient deaths. We herein present the surgical technique of LAPPNTG with jejunal interposition.
Patients and methods Patients Between January 2009 and December 2012, 13 consecutive patients underwent LAPPNTG with jejunal interposition at the Department of Surgery of Nara Medical University Hospital. The clinical classifications, including the depth of tumor invasion and lymph node metastasis, were determined according to the Japanese Classification of Gastric Carcinoma [9]. Preoperative evaluations were based on examinations, including an upper gastrointestinal study, gastrointestinal endoscopy, endoscopic ultrasonography and computed tomography. In our institute, LAPG is Fig. 1 The major points of the LAPPNTG are shown. a The resection of the stomach was similar to that during conventional total gastrectomy, with the key difference being that the pyloric cuff was preserved to a length of 3–4 cm. b The reconstruction in LAPPNTG was performed with a jejunal interposition of 30 cm in length in the retrocolic fashion
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performed for patients with cT1, cN0 proximal-third gastric cancer where more than half of the distal stomach can be preserved. LAPPNTG was also performed after informed consent was obtained from those with cT1, cN0 proximal gastric cancer that had spread to the middle third of the stomach, and who required resection of more than half of the proximal stomach. Patients who are older than 76 years of age and have multiple lesions of gastric cancer are ineligible for pylorus-preserving surgery. The major steps of LAPPNTG During this procedure, the resection of the stomach is similar to that during conventional total gastrectomy, with the key difference being that the pyloric cuff is preserved to a length of 3–4 cm (Fig. 1a). Compared with standard total gastrectomy, the lymph node dissection along the right gastric vessels (station 5) and the infrapyloric vessels is omitted, and the pyloric branch and the celiac branch of the vagus nerve are preserved. After gastrectomy, reconstruction is performed with a jejunal interposition that is 30 cm in length, with preservation of the marginal vessels in the retrocolic fashion (Fig. 1b). Surgical procedures The patients undergo the laparoscopic procedure in the open-leg position. The surgeon stands on the right side of the patient, with the assistant on the left side, and the laparoscope operator between the patient’s legs. A 12-mm blunt port is inserted through the umbilicus with the open
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method. A pneumoperitoneum is created using the injection of carbon dioxide to 8 mmHg, and a flexible laparoscope is inserted through the umbilical port. Six operating ports are inserted in the upper abdomen, as shown in Fig. 2.
Fig. 2 The placement of a total of six surgical ports. A 12-mm blunt port for the laparoscope was inserted through the umbilicus, and four operating ports were inserted in the upper abdomen. A 5-mm port was added under the xyphoid process to move the left lobe of the liver aside. The dotted line shows the location of the 5-cm minilaparotomy
First, the lesser omentum is opened toward the esophagus, with preservation of the hepatic branch of the vagus nerve, and the right side of the abdominal esophagus and the right crus of the diaphragm are exposed using an ultrasonic activating coagulation device (Sonosurg, Olympus). The posterior trunk of the vagus nerve is preserved carefully in the posterior wall of the abdominal esophagus (Fig. 3a). The greater omentum is opened towards the lower pole of the spleen. The left gastroepiploic vessels are clipped and divided, and the station 4sb lymph nodes are removed. In the same view, lymph node dissection of station 4sa is continued to divide the short gastric vessels. Next, the assistant rolls up the greater curvature fat toward the lesser curvature, and lifts up the pedicle of the left gastric artery and vein. With the resulting good field of view, suprapancreatic lymph node dissection can be achieved. The pancreatic capsule is dissected carefully, and the splenic artery is exposed to remove the lymph nodes of station 11p. Dissection proceeds along the distal side of the splenic artery, and the roots of the posterior gastric vessels are divided with the Sonosurg device. Gerota’s fascia and the left crus of the diaphragm are then exposed. The fundic branch from the left infradiaphragmatic artery is divided, and the station 2 lymph nodes are removed. The left side of the abdominal esophagus is exposed easily and completely. Then, the greater omentum is transected towards the lower edge of the second part of the duodenum. The right
Fig. 3 The method used for gastrectomy and lymph node dissection. a The lesser omentum was opened and the right side of the abdominal esophagus was exposed. The posterior trunk of the vagus nerve was preserved. b The greater omentum was opened towards the duodenum. The right gastroepiploic vein and artery were divided at the level of the roots, with preservation of the infrapyloric artery (white arrow). c The left gastric vessels were divided, with preservation of the celiac branch of the vagus nerve (white arrow). d After transection of the abdominal esophagus, the stomach was extracted through a 5-cm minilaparotomy. A distal transection of the stomach was made, with preservation of a 3to 4-cm pyloric cuff
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Surg Today Fig. 4 The method used for reconstruction. a Intracorporeal hand-sewn purse-string suturing was performed, and the anvil head was introduced into the esophageal lumen intracorporeally. b Reconstruction was performed with a jejunal interposition. c The circular stapler was inserted into the oral stump of the interposed jejunum, and the tip of the circular stapler was combined with the anvil head in the peritoneal cavity. d An end-toend anastomosis of the pyloric cuff and distal stump of the interposed jejunum was performed using a layer to layer method with interrupted sutures with a manual method
gastroepiploic vein and artery are divided at the level of the roots, with preservation of the infrapyloric artery (Fig. 3b). Along the left crus of the diaphragm, lymph node station 9 is removed and the left gastric artery is exposed. Next, the lymph node of station 8a is removed along the common hepatic artery. After the left gastric vein is divided, the root of the left gastric artery is exposed to the distal side, and is divided to preserve the celiac branch of the vagus nerve. The gastric branch of the vagus nerve is carefully divided from the posterior trunk of the vagus nerve that was preserved in the first step (Fig. 3c). After the abdominal esophagus is completely exposed, a detachable bowel clamp (an endointestinal clip; Aesculap) is placed on the esophagus to avoid its withdrawal into the mediastinum after subsequent transection. The abdominal esophagus is transected using the Sonosurg device just above the other detachable bowel clamp that was placed at the esophagogastric junction. A 5-cm median incision is made, and is retracted and protected with a wound protector (Alexis Wound Retractor S; Applied Medical). The stomach is extracted through this minilaparotomy. A distal transection of the stomach is made while retaining a 3- to 4-cm pyloric cuff (Fig. 3d). The right gastric vessels are preserved up to the first branch of the stomach wall, with preservation of the pyloric branch of the vagus nerve. The anvil head of a 25-mm circular stapler (DST-EEA; Tyco Healthcare) is placed into the abdominal cavity through the minilaparotomy. A surgical glove is attached to the wound protector to maintain an airtight seal, and the pneumoperitoneum is recreated.
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Intracorporeal hand-sewn purse-string suturing is performed along the cut end of the esophagus with a 2-0 monofilament polypropylene. After the detachable bowel clamp is removed from the esophagus, the anvil head is introduced into the esophageal lumen using an anvilholding forceps (Fig. 4a). The thread is tied, and a monofilament tied loop (Endoloop; Ethicon Endosurgery) is added to reinforce the ligation. Reconstruction is performed with jejunal interposition. The jejunum is brought up in a retrocolic manner and is extracted through the minilaparotomy. The jejunum is divided at 20 and 75 cm from Treitz’s ligament, with preservation of the jejunal marginal artery. The pulled-up jejunum is prepared so that it measures 35 cm in length after each distal and proximal side is removed as sacrificed jejunum. An end-to-end jejunojejunostomy is performed with manual sutures (Fig. 4b), and the anastomosed jejunum is placed into the peritoneal cavity. The circular stapler is covered with a finger of a surgical glove inserted into the oral stump of the pulled-up jejunum, which is tied by silicon vessel tape to prevent the jejunum from separating during the intracorporeal procedure. The circular stapler is introduced into the peritoneal cavity with attachment of the surgical glove to the wound protector. The tip of the circular stapler is protruded through the jejunum and combined with the anvil head in the peritoneal cavity (Fig. 4c). After the intracorporeal esophagojejunostomy is completed, the jejunal stump is closed using a linear stapler (Endo GIA universal 2.5–60 mm; Tyco Healthcare). An end-to-end anastomosis of the
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pyloric cuff and the distal stump of the interposed jejunum is performed using a layer to layer method. Namely, the mucosa is sewn with continuous sutures and the seromuscular layer is sewn with interrupted sutures using a manual method (Fig. 4d).
Results Thirteen patients underwent LAPPNTG. The median patient age was 62.5 years (range 47–70 years). The median length of the operation and estimated blood loss were 329 min (range 275–434 min) and 138 ml (range 42–640 ml), respectively. All patients successfully underwent laparoscopic surgery without conversion to laparotomy. Postoperatively, the pathological T stage was diagnosed, and our series included ten cases of pT1, two cases of pT3 and one case of pT4a disease. All resected specimens had tumor-free margins, and the median number of removed lymph nodes was 40 (range 23–60). A postoperative upper gastrointestinal study with gastrografin was performed for all patients on the fifth to seventh day after the operation. There were no postoperative anastomotic complications, including leakage or stenosis. One patient experienced a postoperative pancreas-related abscess, and was treated conservatively with antibiotics. The median postoperative hospital stay was 15 days (range 10–26 days). There were no mortalities during the hospital stay. All patients are currently being followed up as outpatients. The median postoperative follow-up period so far is 26.3 months (range: 12.6–42.3 months). Reflux symptoms, including heartburn and chest pain, were not observed in any of the patients. Eleven patients were examined by follow-up gastrointestinal endoscopy 1 year after the operation. Endoscopy showed no findings of esophagitis in any of the patients according to the Los Angeles classification system. Furthermore, all patients were free from symptoms of dumping and reflux. Consequently, no patients are on medication for postoperative disorders. The pyloric cuff could be evaluated in five of the 11 patients who were examined by endoscopy. One patient who had pT4a gastric cancer developed a recurrence of gastric cancer and died due to peritoneal metastasis. The remaining twelve patients have remained free from disease.
Discussion Recently, the frequency of early gastric cancer in the upper portion of the stomach has increased due to the advances in screening techniques [10]. Since the prognosis of patients
with early gastric cancer who undergo gastrectomy is improving, the postoperative quality of life of these patients is a major consideration. To prevent or reduce post-gastrectomy disorders, function-preserving gastrectomy, including proximal gastrectomy, has been performed in patients with proximal-third early gastric cancer. On the other hand, laparoscopy-assisted gastrectomy (LAG) is widely performed for early gastric cancer, and the LAG technique has become well established in Japan [11]. Consequently, LAPG for proximal-third gastric cancer has become practicable [7, 8], and is routinely performed in specialized institutions in Japan. In our institute, PPNTG for proximal early gastric cancer has been performed as function-preserving gastrectomy. In this article, we describe the surgical technique of LAPPNTG. The pylorus-preserving technique more commonly used in distal gastrectomy was applied to total gastrectomy for the purpose of preventing dumping syndrome and the reflux of bile or pancreatic juice that occurs when the pylorus is resected [4]. PPNTG with a jejunal interposition was similarly developed to treat patients with proximal gastric cancer to prevent reflux esophagitis and dumping syndrome. For these patients, the standard treatment had been total gastrectomy. Patients who underwent total gastrectomy often suffered from postoperative disorders for the rest of their lives. We have previously reported the functional advantages and safety of PPNTG compared with total gastrectomy with Roux-en-Y reconstruction (TG-RY) [5]. The differences in the endoscopic findings of esophagitis between the patients who underwent PPNTG and TGRY were not shown in the previous reports. However, patients who underwent PPNTG experienced significantly fewer symptoms of reflux and dumping syndrome. Moreover, the survival of patients who undergo PPNTG does not differ from that observed in patients who undergo TG-RY. The reconstruction during LAPPNTG is relatively complex, and the length of the operation was long in the present report. Even so, no patients who underwent LAPPNTG suffered from these postoperative conditions or had any endoscopic findings of esophagitis during the follow-up period. Preventing postoperative symptoms in patients is important when performing function-preserving gastrectomy. Therefore, LAPPNTG is a useful and safe alternative to TG-RY for treating proximal gastric cancer. LAPPNTG is a suitable surgical procedure for patients with T1 proximal gastric cancer who require a resection of more than half of the proximal stomach. For T1 proximal gastric cancer that has spread to the middle third of the stomach, it is impossible to preserve more than half of the distal stomach. According to the Japanese Gastric Cancer Association guidelines [1], the preservation of more than half of the stomach is recommended for proximal gastrectomy. Moreover, for patients with T1 gastric cancer
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located in the middle third of the stomach, the removal of the lymph nodes along the right gastroepiploic vessels (station 4d) is required. The indications for proximal gastrectomy are limited to gastric cancer located in the upper third of the stomach because proximal gastrectomy is required for the preservation of the right gastroepiploic vessels. However, in the LAPPNTG procedure, the lymph nodes along the right gastroepiploic vessels (station 4d) are removed completely. On the other hand, pylorus-preserving gastrectomy (PPG) is generally performed as a function-preserving gastrectomy for T1 gastric cancer in the middle third of the stomach [1, 12]. In the PPG procedure, dissection of the suprapyloric node (station 5) is usually omitted, and dissection of the infrapyloric node (station 6) is performed with preservation of the infrapyloric vessels [13]. In LAPPNTG, as well as LAPPG, the dissection of lymph node station 6 with preservation of the infrapyloric vessels can be achieved. In cases with tumors located in the proximal area of the middle third of the stomach, the residual stomach is often too small to allow PPG to be performed. Consequently, LAPPNTG is a useful treatment option in cases of T1 proximal gastric cancer that has spread to the middle third of the stomach. In this study, three of the 13 patients were underestimated in terms of the preoperative staging. These three cases had pT3 and pT4a gastric cancer located in the upper third of the stomach. Generally, standard total gastrectomy for advanced gastric cancer in the upper third of the stomach is required for the lymph node dissection of stations 4d, 5 and 6. However, Sasako et al. [14] reported that the index of the therapeutic value of station 5 or 6 is lower than that of station 4d for these upper-third gastric cancers. The index of the therapeutic value of stations 5 and 6 was 0.0 and 0.4, respectively. Therefore, lymph node dissection of stations 5 and 6 was shown to provide little benefit. During the PPNTG, the 4d lymph node station was removed completely, and the lymph node dissection of station 6 was achieved with preservation of the infrapyloric vessels. On the other hand, LAPG for cT1-stage proximal-third gastric cancers requires the preservation of the right gastroepiploic vessels. The 4d lymph node station, as well as stations 5 and 6, cannot be removed during LAPG. Therefore, LAPPNTG is relatively safer for cT1-staged gastric cancer located in only the upper third of the stomach compared with LAPG. While the two patients with pT3 gastric cancer have had no recurrence for more than 24 months, the patient with pT4a gastric cancer died due to peritoneal metastasis. Our procedure for LAPPNTG has an advantage in that the surgeons can palpate for gastric cancer and perigastric lymph nodes, because the transection of the stomach is performed extracorporeally. Before the transection of the
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stomach, it may be important to convert the proposed procedure into standard total gastrectomy in cases with unexpected advanced cancer noted to have spread to the middle third of the stomach. The pyloric cuff could not be evaluated in about half of the 11 patients who were examined by gastrointestinal endoscopy in the present study. Surveillance of the remnant pyloric cuff for patients who can be expected to have long-term survival is an important subject which should be resolved. In our previous reports, the incidence of complaints about emptying disturbances was higher in the PPNTG group than in the TG-RY group [5]. These emptying disturbances are thought to result from the length of the interposed jejunum, because a jejunal interposition of 40 cm in length is relatively long for the PPNTG. Therefore, the length of the interposed jejunum was shortened to 30 cm for LAPPNTG in the present cases. On the other hand, the jejunal interposition during the LAPPNTG functions as a gastric reservoir. To allow for better surveillance of the gastric remnant, it might be better to shorten the jejunal interposition still further. Nevertheless, a jejunal interposition that is too short may lead to a loss of the function as a gastric reservoir, resulting in decreased food consumption. The optimal length of jejunal interposition is currently unclear. Further investigations are needed to determine the optimal length and form of the interposed jejunum. In conclusion, performing LAPPNTG with a jejunal interposition is feasible and might be an appropriate laparoscopy-assisted function-preserving gastrectomy in patients with proximal early gastric cancer. Conflict of interest Tomoyoshi Takayama and co-authors have no conflicts of interest to declare in association with this study.
References 1. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guideline 2010 (ver. 3). Gastric Cancer. 2011;14: 113–23. 2. Maki T, Shiratori T, Hatafuka T, Sugawara K. Pylorus-preserving gastrectomy as an improved operation for gastric ulcer. Surgery. 1967;61:838–45. 3. Kodama M, Koyama K. Indications for pylorus preserving gastrectomy for early gastric cancer located in the middle third of the stomach. World J Surg. 1991;15:628–34. 4. Maki T, Sato T, Shiratori T. Pylorus-preserving procedure in partial and total gastrectomy. Langenbecks Arch Chir. 1977;343: 183–93. 5. Tanaka T, Takayama T, Matsumoto S, Wakatsuki K, Enomoto K, Migita K, et al. Postoperative functional evaluation after pyloruspreserving nearly-total gastrectomy with jejunal interposition for gastric cancer. Hepatogastroenterology. 2013;60:200–6. 6. Mochiki E, Toyomasu Y, Ogata K, Andoh H, Ohno T, Aihara R, et al. Laparoscopically assisted total gastrectomy with lymph node dissection for upper and middle gastric cancer. Surg Endosc. 2008;22:1997–2002.
Surg Today 7. Kitano S, Adachi Y, Shiraishi N, Suematsu T, Bando T. Laparoscopic-assisted proximal gastrectomy for early gastric carcinomas. Jpn J Surg. 1999;29:389–91. 8. Aihara R, Mochiki E, Ohno T, Yanai M, Toyomasu Y, Ogata K, et al. Laparoscopy-assisted proximal gastrectomy with gastric tube reconstruction for early gastric cancer. Surg Endosc. 2010;24:2343–8. 9. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14: 101–12. 10. Salvon-Harman JC, Cady B, Nikulasson S, Khettry U, Stone MD, Lavin P. Shifting proportions of gastric adenocarcinomas. Arch Surg. 1994;129:381–9. 11. Kitano S, Shiraishi N, Uyama I, Sugihara K, Tanigawa N, Japanese Laparoscopic Surgery Study Group. A multicenter study
on oncologic outcome of laparoscopic gastrectomy for early gastric cancer in Japan. Ann Surg. 2007;245:68–72. 12. Kodera K, Nishizuka S, Wakabayashi G. Minimally invasive surgery for gastric cancer: the future standard of care. World J Surg. 2011;35:1469–77. 13. Nunobe S, Hiki N, Fukunaga T, Tokunaga M, Ohyama S, Seto Y, et al. Laproscopy-assisted pylorus-preserving gastrectomy: preservation of vagus nerve and infrapyloric blood flow induces less stasis. World J Surg. 2007;31:2335–40. 14. Sasako M, Mcculloch P, Kinoshita T, Maruyama K. New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg. 1995;82:346–51.
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ORIGINAL ARTICLE
A novel laparoscopic procedure for treating proximal early gastric cancer: laparoscopy-assisted pylorus-preserving nearly total gastrectomy Tomoyoshi Takayama • Sohei Matsumoto • Kohei Wakatsuki • Tetsuya Tanaka • Kazuhiro Migita • Masahiro Ito • Yoshiyuki Nakajima
Received: 10 December 2013 / Accepted: 1 April 2014 Ó Springer Japan 2014
Abstract Purpose Pylorus-preserving nearly total gastrectomy (PPNTG) is a function-preserving gastrectomy for treating proximal early gastric cancer that prevents rapid gastric emptying and reflux. In this report, we present a surgical technique for performing laparoscopy-assisted PPNTG (LAPPNTG). Methods The resection of the stomach was similar to that during conventional total gastrectomy, with the key difference being that the pyloric cuff was preserved to a length of 3–4 cm. Compared with standard total gastrectomy, the lymph node dissection along the right gastric vessels and the infrapyloric vessels were omitted. Reconstruction was performed with a jejunal interposition that was 30 cm in length, with preservation of the marginal vessels in a retrocolic fashion. Results Thirteen patients with cT1 cN0 proximal gastric cancer underwent LAPPNTG at our institution. The median length of the operation and estimated blood loss were 329 min and 138 ml, respectively. All resected specimens had tumor-free margins, and the median number of removed lymph nodes was 40. There were no serious postoperative complications and no patients underwent conversion to laparotomy. Conclusions Performing LAPPNTG with a jejunal interposition is feasible and might be an appropriate treatment for proximal early gastric cancer.
T. Takayama (&) S. Matsumoto K. Wakatsuki T. Tanaka K. Migita M. Ito Y. Nakajima Department of Surgery, Nara Medical University, 840 Shijo-cho, 634-8522 Kashihara, Nara, Japan e-mail: [email protected]
Keywords Proximal gastric cancer Laparoscopic surgery Pylorus-preserving gastrectomy
Introduction In Japan, the standard surgical treatment for patients with gastric cancer in the upper portion of the stomach is total gastrectomy with D2 lymph node dissection. For patients with proximal early gastric cancer, the optimal extent of stomach resection and the method used for reconstruction were not been determined until quite recently. According to the Japanese Gastric Cancer Association guidelines [1] revised in 2011, proximal gastrectomy with D1 ? lymphadenectomy is defined as an alternative to total gastrectomy for patients with cT1 cN0 gastric cancer in the upper portion of the stomach. Pylorus-preserving gastrectomy to treat gastric ulcers was developed by Maki et al. [2] in 1967 to prevent reflux esophagitis and dumping syndrome. At that time, the pylorus-preserving technique had been applied to patients with early gastric cancer as a function-preserving procedure [3]. Pylorus-preserving gastrectomy is now accepted to be the standard option for treating middle-third early gastric cancer according to the Japanese guidelines. On the other hand, it has also been reported that the pylorus-preserving procedure could be applied for cases in which total gastrectomy was required [4]. The patients with gastric cancer who underwent the pylorus-preserving procedure after nearly total gastrectomy showed satisfactory results concerning dumping and reflux esophagitis. In our institute, an identical surgical procedure, named pylorus-preserving nearly total gastrectomy (PPNTG), has been performed in patients with proximal early gastric cancer. We have previously demonstrated the functional advantages and safety
123
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of PPNTG compared with conventional total gastrectomy [5]. Patients who undergo total gastrectomy with Roux-enY reconstruction frequently develop reflux symptoms and dumping syndrome, while PPNTG prevents patients from developing these post-gastrectomy disorders. Recently, new techniques for laparoscopy-assisted total gastrectomy (LATG) and proximal gastrectomy (LAPG) for proximal early gastric cancer have been reported [6–8], as laparoscopic surgery has continued to develop. Since January 2009, we have also performed laparoscopy-assisted pylorus-preserving nearly total gastrectomy (LAPPNTG) in patients with proximal early gastric cancer. There have been no major complications or patient deaths. We herein present the surgical technique of LAPPNTG with jejunal interposition.
Patients and methods Patients Between January 2009 and December 2012, 13 consecutive patients underwent LAPPNTG with jejunal interposition at the Department of Surgery of Nara Medical University Hospital. The clinical classifications, including the depth of tumor invasion and lymph node metastasis, were determined according to the Japanese Classification of Gastric Carcinoma [9]. Preoperative evaluations were based on examinations, including an upper gastrointestinal study, gastrointestinal endoscopy, endoscopic ultrasonography and computed tomography. In our institute, LAPG is Fig. 1 The major points of the LAPPNTG are shown. a The resection of the stomach was similar to that during conventional total gastrectomy, with the key difference being that the pyloric cuff was preserved to a length of 3–4 cm. b The reconstruction in LAPPNTG was performed with a jejunal interposition of 30 cm in length in the retrocolic fashion
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performed for patients with cT1, cN0 proximal-third gastric cancer where more than half of the distal stomach can be preserved. LAPPNTG was also performed after informed consent was obtained from those with cT1, cN0 proximal gastric cancer that had spread to the middle third of the stomach, and who required resection of more than half of the proximal stomach. Patients who are older than 76 years of age and have multiple lesions of gastric cancer are ineligible for pylorus-preserving surgery. The major steps of LAPPNTG During this procedure, the resection of the stomach is similar to that during conventional total gastrectomy, with the key difference being that the pyloric cuff is preserved to a length of 3–4 cm (Fig. 1a). Compared with standard total gastrectomy, the lymph node dissection along the right gastric vessels (station 5) and the infrapyloric vessels is omitted, and the pyloric branch and the celiac branch of the vagus nerve are preserved. After gastrectomy, reconstruction is performed with a jejunal interposition that is 30 cm in length, with preservation of the marginal vessels in the retrocolic fashion (Fig. 1b). Surgical procedures The patients undergo the laparoscopic procedure in the open-leg position. The surgeon stands on the right side of the patient, with the assistant on the left side, and the laparoscope operator between the patient’s legs. A 12-mm blunt port is inserted through the umbilicus with the open
Surg Today
method. A pneumoperitoneum is created using the injection of carbon dioxide to 8 mmHg, and a flexible laparoscope is inserted through the umbilical port. Six operating ports are inserted in the upper abdomen, as shown in Fig. 2.
Fig. 2 The placement of a total of six surgical ports. A 12-mm blunt port for the laparoscope was inserted through the umbilicus, and four operating ports were inserted in the upper abdomen. A 5-mm port was added under the xyphoid process to move the left lobe of the liver aside. The dotted line shows the location of the 5-cm minilaparotomy
First, the lesser omentum is opened toward the esophagus, with preservation of the hepatic branch of the vagus nerve, and the right side of the abdominal esophagus and the right crus of the diaphragm are exposed using an ultrasonic activating coagulation device (Sonosurg, Olympus). The posterior trunk of the vagus nerve is preserved carefully in the posterior wall of the abdominal esophagus (Fig. 3a). The greater omentum is opened towards the lower pole of the spleen. The left gastroepiploic vessels are clipped and divided, and the station 4sb lymph nodes are removed. In the same view, lymph node dissection of station 4sa is continued to divide the short gastric vessels. Next, the assistant rolls up the greater curvature fat toward the lesser curvature, and lifts up the pedicle of the left gastric artery and vein. With the resulting good field of view, suprapancreatic lymph node dissection can be achieved. The pancreatic capsule is dissected carefully, and the splenic artery is exposed to remove the lymph nodes of station 11p. Dissection proceeds along the distal side of the splenic artery, and the roots of the posterior gastric vessels are divided with the Sonosurg device. Gerota’s fascia and the left crus of the diaphragm are then exposed. The fundic branch from the left infradiaphragmatic artery is divided, and the station 2 lymph nodes are removed. The left side of the abdominal esophagus is exposed easily and completely. Then, the greater omentum is transected towards the lower edge of the second part of the duodenum. The right
Fig. 3 The method used for gastrectomy and lymph node dissection. a The lesser omentum was opened and the right side of the abdominal esophagus was exposed. The posterior trunk of the vagus nerve was preserved. b The greater omentum was opened towards the duodenum. The right gastroepiploic vein and artery were divided at the level of the roots, with preservation of the infrapyloric artery (white arrow). c The left gastric vessels were divided, with preservation of the celiac branch of the vagus nerve (white arrow). d After transection of the abdominal esophagus, the stomach was extracted through a 5-cm minilaparotomy. A distal transection of the stomach was made, with preservation of a 3to 4-cm pyloric cuff
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Surg Today Fig. 4 The method used for reconstruction. a Intracorporeal hand-sewn purse-string suturing was performed, and the anvil head was introduced into the esophageal lumen intracorporeally. b Reconstruction was performed with a jejunal interposition. c The circular stapler was inserted into the oral stump of the interposed jejunum, and the tip of the circular stapler was combined with the anvil head in the peritoneal cavity. d An end-toend anastomosis of the pyloric cuff and distal stump of the interposed jejunum was performed using a layer to layer method with interrupted sutures with a manual method
gastroepiploic vein and artery are divided at the level of the roots, with preservation of the infrapyloric artery (Fig. 3b). Along the left crus of the diaphragm, lymph node station 9 is removed and the left gastric artery is exposed. Next, the lymph node of station 8a is removed along the common hepatic artery. After the left gastric vein is divided, the root of the left gastric artery is exposed to the distal side, and is divided to preserve the celiac branch of the vagus nerve. The gastric branch of the vagus nerve is carefully divided from the posterior trunk of the vagus nerve that was preserved in the first step (Fig. 3c). After the abdominal esophagus is completely exposed, a detachable bowel clamp (an endointestinal clip; Aesculap) is placed on the esophagus to avoid its withdrawal into the mediastinum after subsequent transection. The abdominal esophagus is transected using the Sonosurg device just above the other detachable bowel clamp that was placed at the esophagogastric junction. A 5-cm median incision is made, and is retracted and protected with a wound protector (Alexis Wound Retractor S; Applied Medical). The stomach is extracted through this minilaparotomy. A distal transection of the stomach is made while retaining a 3- to 4-cm pyloric cuff (Fig. 3d). The right gastric vessels are preserved up to the first branch of the stomach wall, with preservation of the pyloric branch of the vagus nerve. The anvil head of a 25-mm circular stapler (DST-EEA; Tyco Healthcare) is placed into the abdominal cavity through the minilaparotomy. A surgical glove is attached to the wound protector to maintain an airtight seal, and the pneumoperitoneum is recreated.
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Intracorporeal hand-sewn purse-string suturing is performed along the cut end of the esophagus with a 2-0 monofilament polypropylene. After the detachable bowel clamp is removed from the esophagus, the anvil head is introduced into the esophageal lumen using an anvilholding forceps (Fig. 4a). The thread is tied, and a monofilament tied loop (Endoloop; Ethicon Endosurgery) is added to reinforce the ligation. Reconstruction is performed with jejunal interposition. The jejunum is brought up in a retrocolic manner and is extracted through the minilaparotomy. The jejunum is divided at 20 and 75 cm from Treitz’s ligament, with preservation of the jejunal marginal artery. The pulled-up jejunum is prepared so that it measures 35 cm in length after each distal and proximal side is removed as sacrificed jejunum. An end-to-end jejunojejunostomy is performed with manual sutures (Fig. 4b), and the anastomosed jejunum is placed into the peritoneal cavity. The circular stapler is covered with a finger of a surgical glove inserted into the oral stump of the pulled-up jejunum, which is tied by silicon vessel tape to prevent the jejunum from separating during the intracorporeal procedure. The circular stapler is introduced into the peritoneal cavity with attachment of the surgical glove to the wound protector. The tip of the circular stapler is protruded through the jejunum and combined with the anvil head in the peritoneal cavity (Fig. 4c). After the intracorporeal esophagojejunostomy is completed, the jejunal stump is closed using a linear stapler (Endo GIA universal 2.5–60 mm; Tyco Healthcare). An end-to-end anastomosis of the
Surg Today
pyloric cuff and the distal stump of the interposed jejunum is performed using a layer to layer method. Namely, the mucosa is sewn with continuous sutures and the seromuscular layer is sewn with interrupted sutures using a manual method (Fig. 4d).
Results Thirteen patients underwent LAPPNTG. The median patient age was 62.5 years (range 47–70 years). The median length of the operation and estimated blood loss were 329 min (range 275–434 min) and 138 ml (range 42–640 ml), respectively. All patients successfully underwent laparoscopic surgery without conversion to laparotomy. Postoperatively, the pathological T stage was diagnosed, and our series included ten cases of pT1, two cases of pT3 and one case of pT4a disease. All resected specimens had tumor-free margins, and the median number of removed lymph nodes was 40 (range 23–60). A postoperative upper gastrointestinal study with gastrografin was performed for all patients on the fifth to seventh day after the operation. There were no postoperative anastomotic complications, including leakage or stenosis. One patient experienced a postoperative pancreas-related abscess, and was treated conservatively with antibiotics. The median postoperative hospital stay was 15 days (range 10–26 days). There were no mortalities during the hospital stay. All patients are currently being followed up as outpatients. The median postoperative follow-up period so far is 26.3 months (range: 12.6–42.3 months). Reflux symptoms, including heartburn and chest pain, were not observed in any of the patients. Eleven patients were examined by follow-up gastrointestinal endoscopy 1 year after the operation. Endoscopy showed no findings of esophagitis in any of the patients according to the Los Angeles classification system. Furthermore, all patients were free from symptoms of dumping and reflux. Consequently, no patients are on medication for postoperative disorders. The pyloric cuff could be evaluated in five of the 11 patients who were examined by endoscopy. One patient who had pT4a gastric cancer developed a recurrence of gastric cancer and died due to peritoneal metastasis. The remaining twelve patients have remained free from disease.
Discussion Recently, the frequency of early gastric cancer in the upper portion of the stomach has increased due to the advances in screening techniques [10]. Since the prognosis of patients
with early gastric cancer who undergo gastrectomy is improving, the postoperative quality of life of these patients is a major consideration. To prevent or reduce post-gastrectomy disorders, function-preserving gastrectomy, including proximal gastrectomy, has been performed in patients with proximal-third early gastric cancer. On the other hand, laparoscopy-assisted gastrectomy (LAG) is widely performed for early gastric cancer, and the LAG technique has become well established in Japan [11]. Consequently, LAPG for proximal-third gastric cancer has become practicable [7, 8], and is routinely performed in specialized institutions in Japan. In our institute, PPNTG for proximal early gastric cancer has been performed as function-preserving gastrectomy. In this article, we describe the surgical technique of LAPPNTG. The pylorus-preserving technique more commonly used in distal gastrectomy was applied to total gastrectomy for the purpose of preventing dumping syndrome and the reflux of bile or pancreatic juice that occurs when the pylorus is resected [4]. PPNTG with a jejunal interposition was similarly developed to treat patients with proximal gastric cancer to prevent reflux esophagitis and dumping syndrome. For these patients, the standard treatment had been total gastrectomy. Patients who underwent total gastrectomy often suffered from postoperative disorders for the rest of their lives. We have previously reported the functional advantages and safety of PPNTG compared with total gastrectomy with Roux-en-Y reconstruction (TG-RY) [5]. The differences in the endoscopic findings of esophagitis between the patients who underwent PPNTG and TGRY were not shown in the previous reports. However, patients who underwent PPNTG experienced significantly fewer symptoms of reflux and dumping syndrome. Moreover, the survival of patients who undergo PPNTG does not differ from that observed in patients who undergo TG-RY. The reconstruction during LAPPNTG is relatively complex, and the length of the operation was long in the present report. Even so, no patients who underwent LAPPNTG suffered from these postoperative conditions or had any endoscopic findings of esophagitis during the follow-up period. Preventing postoperative symptoms in patients is important when performing function-preserving gastrectomy. Therefore, LAPPNTG is a useful and safe alternative to TG-RY for treating proximal gastric cancer. LAPPNTG is a suitable surgical procedure for patients with T1 proximal gastric cancer who require a resection of more than half of the proximal stomach. For T1 proximal gastric cancer that has spread to the middle third of the stomach, it is impossible to preserve more than half of the distal stomach. According to the Japanese Gastric Cancer Association guidelines [1], the preservation of more than half of the stomach is recommended for proximal gastrectomy. Moreover, for patients with T1 gastric cancer
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located in the middle third of the stomach, the removal of the lymph nodes along the right gastroepiploic vessels (station 4d) is required. The indications for proximal gastrectomy are limited to gastric cancer located in the upper third of the stomach because proximal gastrectomy is required for the preservation of the right gastroepiploic vessels. However, in the LAPPNTG procedure, the lymph nodes along the right gastroepiploic vessels (station 4d) are removed completely. On the other hand, pylorus-preserving gastrectomy (PPG) is generally performed as a function-preserving gastrectomy for T1 gastric cancer in the middle third of the stomach [1, 12]. In the PPG procedure, dissection of the suprapyloric node (station 5) is usually omitted, and dissection of the infrapyloric node (station 6) is performed with preservation of the infrapyloric vessels [13]. In LAPPNTG, as well as LAPPG, the dissection of lymph node station 6 with preservation of the infrapyloric vessels can be achieved. In cases with tumors located in the proximal area of the middle third of the stomach, the residual stomach is often too small to allow PPG to be performed. Consequently, LAPPNTG is a useful treatment option in cases of T1 proximal gastric cancer that has spread to the middle third of the stomach. In this study, three of the 13 patients were underestimated in terms of the preoperative staging. These three cases had pT3 and pT4a gastric cancer located in the upper third of the stomach. Generally, standard total gastrectomy for advanced gastric cancer in the upper third of the stomach is required for the lymph node dissection of stations 4d, 5 and 6. However, Sasako et al. [14] reported that the index of the therapeutic value of station 5 or 6 is lower than that of station 4d for these upper-third gastric cancers. The index of the therapeutic value of stations 5 and 6 was 0.0 and 0.4, respectively. Therefore, lymph node dissection of stations 5 and 6 was shown to provide little benefit. During the PPNTG, the 4d lymph node station was removed completely, and the lymph node dissection of station 6 was achieved with preservation of the infrapyloric vessels. On the other hand, LAPG for cT1-stage proximal-third gastric cancers requires the preservation of the right gastroepiploic vessels. The 4d lymph node station, as well as stations 5 and 6, cannot be removed during LAPG. Therefore, LAPPNTG is relatively safer for cT1-staged gastric cancer located in only the upper third of the stomach compared with LAPG. While the two patients with pT3 gastric cancer have had no recurrence for more than 24 months, the patient with pT4a gastric cancer died due to peritoneal metastasis. Our procedure for LAPPNTG has an advantage in that the surgeons can palpate for gastric cancer and perigastric lymph nodes, because the transection of the stomach is performed extracorporeally. Before the transection of the
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stomach, it may be important to convert the proposed procedure into standard total gastrectomy in cases with unexpected advanced cancer noted to have spread to the middle third of the stomach. The pyloric cuff could not be evaluated in about half of the 11 patients who were examined by gastrointestinal endoscopy in the present study. Surveillance of the remnant pyloric cuff for patients who can be expected to have long-term survival is an important subject which should be resolved. In our previous reports, the incidence of complaints about emptying disturbances was higher in the PPNTG group than in the TG-RY group [5]. These emptying disturbances are thought to result from the length of the interposed jejunum, because a jejunal interposition of 40 cm in length is relatively long for the PPNTG. Therefore, the length of the interposed jejunum was shortened to 30 cm for LAPPNTG in the present cases. On the other hand, the jejunal interposition during the LAPPNTG functions as a gastric reservoir. To allow for better surveillance of the gastric remnant, it might be better to shorten the jejunal interposition still further. Nevertheless, a jejunal interposition that is too short may lead to a loss of the function as a gastric reservoir, resulting in decreased food consumption. The optimal length of jejunal interposition is currently unclear. Further investigations are needed to determine the optimal length and form of the interposed jejunum. In conclusion, performing LAPPNTG with a jejunal interposition is feasible and might be an appropriate laparoscopy-assisted function-preserving gastrectomy in patients with proximal early gastric cancer. Conflict of interest Tomoyoshi Takayama and co-authors have no conflicts of interest to declare in association with this study.
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