Surgical Outcomes From Laparoscopic Distal Gastrectomy and Roux-en-Y Reconstruction: Evolution in a Totally Intracorporeal Technique

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1 ORIGINAL ARTICLE Surgical Outcomes From Laparoscopic Distal Gastrectomy and Roux-en-Y Reconstruction: Evolution in a Totally Intracorporeal Technique George Bouras, MRCS, Sang-Woong Lee, MD, PhD, Eiji Nomura, MD, PhD, Takaya Tokuhara, MD, PhD, Toshikatsu Nitta, MD, PhD, Ryoji Yoshinaka, MD, PhD, Soichiro Tsunemi, MD, PhD, and Nobuhiko Tanigawa, MD, PhD Introduction: Laparoscopic gastrectomy is gaining popularity. Increasingly, Roux-en-Y reconstruction after distal gastrectomy is preferred because of reduced reflux and associated symptoms. Therefore, efficient and reliable techniques for intracorporeal Roux-en-Y reconstruction are in demand. Aims: To determine the surgical outcomes from laparoscopic distal gastrectomy and Roux-en-Y reconstruction in the treatment of gastric cancer. Patients and Methods: Laparoscopic gastrectomy is indicated for gastric cancer up to stage T1N1. Our technique for laparoscopic Roux-en-Y reconstruction incorporates intracorporeal-stapled gastrojejunostomy with extracorporeal hand-sewn jejunojejunostomy, or more recently, totally intracorporeal reconstruction. Results: From 2003 to 2009, 82 patients underwent laparoscopic distal gastrectomy with Roux-en-Y reconstruction. The mean age of the patients was 64.6 years (range, 39 to 83 y) and the male:female ratio was 2.4:1. Most patients (85%) had stage I disease. The mean operation time was 354 minutes (SD 82.7). The conversion rate was 0%. The mean lymph node yield was 27.2 nodes (SD 12.4). Eleven patients had totally intracorporeal reconstruction. Overall, anastomotic leakage of the gastrojejunostomy occurred in 2 patients (2.4%) both requiring reoperation. There were 2 cases (2.4%) of duodenal stump leakage, which were treated conservatively. Postoperative stasis was encountered in 2 patients (2.4%). The mean follow-up was 21 months (range, 5 to 50 mo). None of the patients developed reflux symptoms or endoscopic evidence of reflux during follow-up. Recurrence occurred in 1 patient who was the only patient with metastasis to the third tier of lymph nodes. Conclusions: Surgical outcomes from laparoscopic distal gastrectomy and Roux-en-Y reconstruction were acceptable in the context of early gastric cancer. Totally intracorporeal reconstruction was technically feasible, safe, and associated with no obvious drawbacks. Key Words: laparoscopic distal gastrectomy, Roux-en-Y reconstruction, outcomes, surgical technique (Surg Laparosc Endosc Percutan Tech 2011;21:37 41) Laparoscopic gastrectomy is standardized in Asia and gaining popularity worldwide as it is associated with earlier recovery of patients when compared with open Received for Publication March 14, 2010; accepted October 5, From the Department of General and Gastrointestinal Surgery, Osaka Medical College, Japan. Reprints: George Bouras, MRCS, 10 East Pathway, Birmingham, United Kingdom ( georgebouras@hotmail.com). Copyright r 2011 by Lippincott Williams & Wilkins surgery. 1 6 Although the technical and oncological efficacy of laparoscopic resection and lymphadenectomy has been proven, 7,8 surgical outcomes in relation to emerging intracorporeal techniques for reconstruction deserve attention, particularly from a functional perspective. After distal gastric resection, Roux-en-Y reconstruction is routine in the West and gaining popularity in Asia. Compared with other types of reconstruction such as Billroth 1 and Billroth 2, Roux-en- Y has been associated with reduced rates of symptoms related to reflux and dumping Laparoscopic gastrectomy has conventionally been followed by reconstruction through a minilaparotomy, which is easier to perform in thin patients. Recently, investigators have described numerous techniques for intracorporeal Roux-en-Y in an attempt to improve on surgical efficiency and invasiveness We have earlier described our technique and initial experience from intracorporeal-stapled gastrojejunostomy in In this study, we report on the surgical outcomes from our patients who have undergone laparoscopic distal gastrectomy with Rouxen-Y reconstruction and also describe our new strategy for totally intracorporeal reconstruction. PATIENTS AND METHODS Patients who had undergone R0 resection by distal or subtotal gastrectomy for gastric cancer followed by Rouxen-Y reconstruction were eligible for the study. At our unit, laparoscopic gastrectomy is indicated for gastric cancer up to stage T1N1. Distal or subtotal gastrectomy is indicated for distal and middle third gastric cancers in which tumor margins of at least 2 cm for early and 5 cm for advanced lesions can be taken. Some patients with very early disease may have a more limited resection such as pyloruspreserving or segmental gastrectomy. 16 Lymph node dissection is performed according to guidelines and depending on the endoscopic depth of invasion of the primary tumor. 1,17 19 Patients with a low likelihood of metastases to the second tier lymph nodes undergo limited D2 dissection of the most commonly involved second tier lymph nodes D1+ a (leftgastric)or D1+b (anterior common hepatic, left gastric and celiac). All patients with tumors invading the muscle layer or with evidence of radiologic or macroscopic lymph node involvement undergo formal D2 lymphadenectomy and occasionally, D3 sampling. In terms of reconstruction, patients with large remnant stomachs, which allow for tension-free primary gastroduodenostomy undergo Billroth-1 reconstruction by the d-shaped method using linear staplers. 20 The tension is assessed by pulling the greater curve of the gastric stump Surg Laparosc Endosc Percutan Tech Volume 21, Number 1, February

2 Bouras et al Surg Laparosc Endosc Percutan Tech Volume 21, Number 1, February 2011 toward the duodenum before reconstruction. The rest of the patients with small remnant stomachs undergo Rouxen-Y reconstruction for which the gastrojejunostomy is performed by our earlier described intracorporeal technique using linear staplers. Surgical Technique for Intracorporeal Roux-en-Y Reconstruction (Figs. 1 5) After laparoscopic distal gastrectomy and lymph node dissection, the specimen is retrieved through the umbilical wound extended to 3 cm. Pneumoperitoneum is then reestablished by partial reclosure of the wound before reconstruction. As described earlier, we perform intracorporeal side-to-side gastrojejunostomy using 2 firings of the linear stapler without the need for intracorporeal suture closure of the entry hole for the stapler. During our initial experience, this was followed by extracorporeal hand-sewn jejunojejunostomy through an umbilical port wound extended by a further 2 cm. More recently, we have introduced intracorporeal jejunojejunostomy as part of our strategy for totally intracorporeal Roux-en-Y reconstruction. For this, the jejunojejunostomy is created first. The transverse mesocolon is lifted to identify the Treitz ligament from which a distance of 25 cm is measured distally along the jejunum. An enterotomy is made on the antimesenteric surface and the bowel is grasped by the FIGURE 2. Intracorporeal suture closure of the common enterotomy hole for the stapler. FIGURE 1. Formation of upward loop of proximal jejunum by side-to-side stapled jejunojejunostomy after creating enterotomy at 25 cm, dividing 10 cm of mesentery distally, and then creating another enterotomy further distally to allow for a Roux-limb of 30 to 35 cm in length. assistant to avoid spillage of contents. Then, the small bowel mesentery is divided close to the bowel for 10 cm distally to create a segment of jejunum, which will be subsequently removed. After this, another enterotomy is made further distally to allow for a Roux limb length of 30 to 35 cm. The jejunum is then configured into an upward loop joined by the 2 enterotomies and 1 jaw of the linear stapler is inserted into each enterotomy to create a side-toside jejunojejunostomy. The remaining hole is closed by intracorporeal suturing. The gastrojejunostomy is then created as described earlier. Another enterotomy is made on the antimesenteric jejunum at the level of the distal end of the gap in the mesentery, which corresponds to the top end of the Roux limb. A stapler is inserted to create a sideto-side antecolic and antiperistaltic gastrojejunostomy along the greater curve of the stomach. The remaining hole is closed using 2 or 3 stay sutures that help the application of a further stapler firing through the mesenteric window to close the hole and divide the jejunum simultaneously. Once the 2 anastomoses are separated, the redundant bowel attached to the jejunojejunostomy is stapled off and retrieved in a cut finger of a sterile surgical glove. An air leak test is conducted for the gastrojejunostomy after each procedure r 2011 Lippincott Williams & Wilkins

3 Surg Laparosc Endosc Percutan Tech Volume 21, Number 1, February 2011 Surgical Outcomes From Laparoscopic Distal Gastrectomy FIGURE 3. Side-to-side antecolic gastrojejunostomy using linear stapler. RESULTS Between 2003 and 2009, 82 cases of laparoscopic distal gastrectomy with Roux-en-Y reconstruction were performed. The mean age of patients was 64.6 years (range, 39 to 83 y) and the male to female ratio was 2.4:1. Postoperative staging based on the Union for International Cancer Control classification 21 showed that 56 patients (68.3%) had stage Ia, 14 patients (17.1%) had stage Ib, 4 patients (4.9%) had stage II, and 8 patients (9.8%) had stage III gastric cancer. Surgical Outcomes The surgical outcomes including intraoperative parameters and postoperative complications are presented in Table 1. A subanalysis of the most recently carried out half of the group (n=41) showed a lower average operation time of minutes (SD 73.4). Although most patients in the cohort had intracorporeal-stapled gastrojejunostomy followed by extracorporeal hand-sewn jejunojejunostomy, recently, 11 patients had totally intracorporeal reconstruction with intracorporeal jejunojejunostomy. The mean operation time for these patients was minutes (SD 42.3). There was no conversion to open surgery in any of the patients. Reoperation was necessary for 2 patients for leakage of the gastrojejunostomy. Operative findings at second look confirmed a tear distal to the anastomosis on the jejunum caused by piercing with the finer (anvil) jaw of the stapler in 1 patient. In the other, leakage was at the closing staple line due to slippage of the bowel within the stapler before firing. Both patients recovered uneventfully after reoperation and primary repair of the anastomosis. Otherwise, complications were infrequent. Stasis, defined at our unit as the need FIGURE 4. Simultaneous closure of remaining gastroenterotomy and transection of jejunum with linear stapler. to stop or reverse routine increments in postoperative food intake was rarely encountered. Figure 6 is an upper gastrointestinal contrast study of one of the patients that shows the shape of the gastrojejunostomy and the absence of obstruction or leakage. Follow-up The mean length of follow-up was 21 months (range, 5 to 50 mo). None of the patients developed any symptoms of reflux or obstruction during follow-up. Routine endoscopy at 6 months excluded any strictures or mucosal changes related to reflux in all patients. Figure 7 is an endoscopic view of the gastrojejunostomy confirming the absence of mucosal changes related to reflux in one of the patients. Histologic examination of lymph nodes showed the presence of metastases in 15 patients (18.3%). There was only 1 patient who had metastasis to a third tier lymph node who died from hepatic recurrence 4 and a half years after surgery. No other patients died or developed recurrence during follow-up. DISCUSSION Long-term results from randomized controlled trials are awaited to support the evidence from cohort studies which have showed that, at least for early gastric cancer, laparoscopic resection is oncologically sound. 22,23 In this cohort, most patients underwent a selective D2 resection which was adequate in achieving oncological clearance as r 2011 Lippincott Williams & Wilkins 39

4 Bouras et al Surg Laparosc Endosc Percutan Tech Volume 21, Number 1, February 2011 FIGURE 6. Upper gastrointestinal contrast study showing patency and shape of stapled gastrojejunostomy. FIGURE 5. Separation of redundant sacrifice jejunum from distal anastomosis with linear stapler to complete Roux-en-Y reconstruction. suggested by the histology and follow-up. Similar to other accounts in the literature, we have achieved acceptable oncological outcomes with laparoscopic distal gastrectomy for early gastric cancer. 24,25 During this experience, we strived to establish our laparoscopic approach and improve on functional outcomes and quality of life after surgery. The development of our strategy for laparoscopic Rouxen-Y is indicative of the trend toward intracorporeal reconstruction, which offers advantages in wound length and avoidance of tension during cumbersome anastomosis through a minilaparotomy. Some investigators have shown quicker recovery of bowel function after intracorporeal reconstruction compared with extracorporeal reconstruction. 26 With increasing confidence in intracorporeal stapled gastrojejunostomy, we were able to successfully introduce intracorporeal jejunojejunostomy to save a further 2 cm on the umbilical wound. This also allows for less manipulation of the bowel and is useful particularly in obese patients where access through a minilaparotomy can be limited. Reconstruction is also performed under continuous laparoscopic guidance and the disorientating and time-consuming switch to open surgery is avoided. In terms of surgical outcomes, totally intracorporeal reconstruction was not associated with any obvious drawbacks. Operation times improved with experience and we have identified potential pitfalls in our technique. We now have a low threshold for oversewing the duodenal staple line particularly after extensive lymph node dissection around the head of the pancreas where pancreatic fluid collections commonly form. For rapid execution of the intracorporeal TABLE 1. Surgical Outcomes From Laparoscopic Distal Gastrectomy and Roux-en-Y Reconstruction Intraoperative Parameters (SD) Bleeding mls 70 (108) Anastomotic leakage Lymph node 27.2 (12.4) Duodenal yield stump Operation time (min) Postoperative Complications (%) 2 (2.4) 2 (2.4) leakage (82.7) Stasis 2 (2.4) Bleeding 0 (0) 30-day hospital 0 (0) mortality FIGURE 7. Endoscopic view of gastrojejunostomy at routine follow-up showing normal gastric and small bowel mucosa r 2011 Lippincott Williams & Wilkins

5 Surg Laparosc Endosc Percutan Tech Volume 21, Number 1, February 2011 Surgical Outcomes From Laparoscopic Distal Gastrectomy jejunojejunostomy, it is important to ensure that all enterotomies are small, just large enough to accomodate the jaws of the stapler so that subsequent suture closure of the hole is not time consuming. Precise alignment of the bowel edges by the assistants, whereas closing the stapler also helps keep the remaining hole small. For the gastrojejunostomy, we have learnt from our experience and have adapted our technique accordingly. Piercing the bowel is now avoided by inserting the larger blunt (cartridge) jaw of the stapler into the jejunum before swinging the bowel up toward the gastric stump. When closing the stapler, slippage of the bowel below the staple line is prevented by using at least 2 stay sutures and ensuring that all layers of the bowel are held by the assistants above the transection line before firing the stapler. Regrettably, this data set is unable to address the effect of laparoscopic surgery on functional outcomes and quality of life. The low rate of Roux stasis observed is encouraging although it is likely to be reflective of the short Roux limb length rather than surgical technique. In Japan, a Roux limb of 30 to 35 cm is considered adequate in preventing reflux and this may be shorter than what is commonly performed in the West Generally, however, there were no obvious drawbacks in terms of functional outcomes and this was confirmed on clinical and endoscopic follow-up. The technique described here has been designed to improve the safety and efficiency of intracorporeal Roux-en- Y reconstruction after distal gastrectomy. Our new strategy involves the creation of the jejunojejunostomy first, which anchors the small bowel in a loop configuration preventing the mesentery from twisting on itself during subsequent gastrojejunostomy. Furthermore, as the jejunum is not divided until the end when both anastomoses have been fashioned, disorientation and confusion between loops of small bowel are avoided. The ischemic segment of jejunum also helps as a visual marker and can be grasped by assistants to pull on the bowel without worrying about injury. Overall, this technique uses 4 firings of the linear stapler with intracorporeal suture closure of 1 enterotomy hole to complete both anastomoses. Placing the bowel in the desirable configuration before embarking on the reconstruction is essential for smooth progression of the procedure. In conclusion, surgical outcomes from laparoscopic distal gastrectomy and Roux-en-Y reconstruction were acceptable in the context of early gastric cancer. Totally intracorporeal reconstruction was technically feasible, safe, and associated with no obvious drawbacks. REFERENCES 1. Shimada Y. JGCA (The Japan Gastric Cancer Association). Gastric cancer treatment guidelines. 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