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Laparoscopic assisted gastrectomy.

Romeo Giuli MD, resident.
School of General and Emergency Surgery.
University of Siena.   Italy.

October 2002.     Review Article.

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Although laparoscopic staging is now an accepted modality in the assessment of gastric cancer, the same cannot be said for minimally invasive gastric resection. Concern has been expressed as to (1) the adequacy of the resection margin, (2) the ability to obtain appropriate nodal clearance, (3) the potential for malignant dissemination, and (4) appropriate patient selection. Although no randomized data exist, preliminary work has help clarify some of the issues raised.
Goh et al. were the first to report a laparoscopic Billroth II resection for benign disease. Kitano et al. are credited with the first reported case of a laparoscopically assisted Billroth I gastrectomy and associated lymphadenectomy for early gastric cancer ( 1, 2, 3 ).
Initially, most practitioners limited this procedure to cases of early gastric cancer in the antrum or lower body, so that less extensive lymph node dissection did not affect patient survival. Currently, the trend has been to expand the indication for LAG. The extent of nodal dissection may not be the same, however, as in conventional open surgery ( 14 ).

Azagra et al. reported their experience with 13 patients who had a laparoscopic gastrectomy for gastric cancer. Nine patients underwent a total gastrectomy with D1 nodal dissection, three underwent a total gastrectomy with D2 nodal dissection, and one had a laparoscopically assisted distal gastrectomy. Margins were negative in all cases, with the average number of examined nodes being 31 ( range, 25-53 ). Perioperative mortality related to the procedure was 7% ( 9 ).

Several reports from Japan have detailed experience with laparoscopic resections for early gastric cancer.

Shimizu et al. retrospectively compared 21 patients undergoing a laparoscopic distal gastrectomy for early gastric cancer with a matched group of 31 patients who underwent a standard open operation during the same time period. Whereas operative time was significantly longer in the laparoscopic group, times to ambulation, return of bowel function, and hospital stay were significantly reduced. More extensive nodal dissections were performed in open surgery, but there was no difference in the number of nodes examined between groups. Although the indication for laparoscopic resection was confined to patients presumed to have intramucosal carcinoma in this study, postoperative histological examination revealed submucosal invasion in six patients ( 29% ). Of these, two patients with poorly differentiated tumors had nodal metastases in the perigastric region. None of the other patients in either group with true intramucosal cancers had nodal involvement ( 10 ).

Asao et al. also highlighted the importance of preoperative staging. In their report of 49 laparoscopically assisted gastrectomies, the depth of invasion was underestimated in five patients, three of whom had positive perigastric nodes.
Because of the difficulty of obtaining an accurate diagnosis of the depth of invasion and nodal metastasis, an additional lymph node dissection, which would include, at the minimum, dissection of the common hepatic and coeliac arteries, should be performed to avoid impairment of curability in a laparoscopically assisted gastrectomy for superficially invading gastric cancer. A surgical technique for laparoscopic gastrectomy with lymph node dissection and reconstruction using a conventional circular stapler is reported ( 13 ).

According to the Adachi et al. study laparoscopy-assisted Billroth I gastrectomy, when compared with conventional open gastrectomy, has several advantages, including less surgical trauma, less impaired nutrition, less pain, rapid return of gastrointestinal function, and shorter hospital stay, with no decrease in operative curability. When performed by a skilled surgeon, laparoscopy-assisted Billroth I gastrectomy is a safe and useful technique for patients with early-stage gastric cancer ( 15 ).
Mochiki et al underline that patients who had undergone LADG showed a more rapid recovery of the gastrointestinal tract and better nutritional recovery than those who had undergone DG.
It is possible that recovery of gastrointestinal motility after laparoscopic surgery is earlier than after open surgery because celiotomy itself may be an important factor affecting gastrointestinal motility. Opening the peritoneum is known to abolish the interdigestive migrating motor complex (IMC), but cutting only the skin has no effect on IMC activity.
Body weight 24 months after LADG was about 100% of the pre-illness weight in this study. Liedman et al. reported that loss of body weight can be largely explained by a corresponding loss of body fat, which also occurs during the early postoperative period. The first possible explanation for better nutritional recovery in the LADG group is less frequent occurrence of postoperative ileus. Another parameter that could be responsible for the difference seen in the recovery of body weight in this study is the postoperative recovery of gastrointestinal motility ( 24, 25, 26, 27 ).

Yano et al stress that the advantage of LADG, compared with EMR, a lesion - lifting method, or intragastric surgery, is that regional LNs can be removed. Stage grouping and surgical curability can be histologically evaluated because of the removal of regional LNs around the primary tumor. If intraoperative pathological diagnosis shows that the resected LNs include many metastatic lesions, they convert to open surgery with widely extended LN dissection, because it is extremely difficult to completely remove the LNs along the commmon hepatic, splenic, or celiac arteries by the LADG procedure. For the purpose of removing regional LNs completely, they did it under direct vision through a small incisional wound, as in open surgery. Recently a completely laparoscopic approach for the removal of regional LNs was reported, but the procedure involved a very difficult technique and a long operation time.
Another advantage of LADG, compared with EMR, is that the tumor can be completely removed with a wide surgical margin, by the resection of the distal two-thirds of the stomach.
Tumors with mucosal o slight submucosal invasion ( SM1 ) were completely resected, with high curability, by LADG. The authors excluded tumors with deep submucosal invasion ( SM2 ) from the indication of LADG, because these tumors were reported to be associated with level 2 lymph node metastases ( 16, 17 ).

Michitaka Fujiwara et al. affirm that anastomotic leakage, which developed in 14% of the patients ( 6 of 43 ) submitted to laparoscopy-assisted distal gastrectomy in patients with histologically confirmed gastric carcinoma located in the lower or middle third of the stomach , occurred throughout the 2-year period but has decreased recently ( data not shown ), indicating that it might be related to inexperience.
The number of lymph nodes in the surgical specimen has been equated with the adequacy of node sampling. Although the lymph node harvest averaged 20 lymph nodes, the yield in 13 patients ( 30% ) fell short of 15 lymph nodes, which is considered the minimal number required for evaluating pN in the TNM classification. Second-tier lymph nodes ( lymph node nos. 7, 8, and 11 ) were also dissected by the laparoscopic approach and a mean of six lymph nodes were harvested ( 18 ).

Partial resections of the stomach wall can be completed laparoscopically or by conventional open surgery. Laparoscopy is a useful technique for lesions in the anterior wall or greater curvature. Lifting the lesions with small metal bars introduced through gastric punctures facilitates the laparoscopic excision with an endoscopic stapler. In performing a laparoscopic local resection, concomitant intraoperative endoscopic confirmation is necessary to help identify the location of the lesion and to confirm adequate surgical margins to prevent incomplete resections ( 14, 28, 29 ) .
The general indication for local resection is the same as for EMR. With this method, nodes attached to te greater or lesser curvature can be removed; however, excision ( dissection ) of perigastric nodes should be regarded as informational ( to confirm node-negative disease ) rather than therapeutic.
Shimoyama et al reported thet pre- and intraoperatively diagnosed mucosal, node-negative, nonpalpable, gastric cancer of less than 4 cm in diameter had either no metastasis or only nodal involvement confined to one station adjacent to the lesion. For this type of lesion, they recommended local resection and confirmation of the absence of nodal metastasis in perigastric nodes using intraoperative frozen sections. Conventional gastrectomy with extended lymphadenectomy is then indicated when involved nodes are found during performance of the LR procedure. ( 14, 30 ).
Seto et al demonstrated nutritional status after LR to be superior to that after PPG. Furthermore, the postgastrectomy syndrome of dumping or reflux esophagitis was not observed in any of the patients undergoing LR and the preoperative quality of life was confirmed to be maintained.
Increased cancer risk at multiple sites and high mortality as compared with the general population, have been reported after gastrectomy. Therefore, preservation of the stomach is a very important determinant of the long-term quality of life after treatment for gastric cancer. The present procedures can provide good maintenance without compromising cure rate for selected patients with early gastric cancer. Furthermore, application of LR might be extended to patients suffering from gastric cancer invading the submucosal layer or deeper, with establishment of sentinel node navigation surgery, in the future ( 31 ).

Proximal gastrectomy with gastroesophagostomy or jejunal interposition is being performed widely in Japan for early-stage gastric neoplasm in the upper portion of the stomach. Its frequent use is partially attributable to the improved postoperative fat absorption, nutrition, and release of gut hormones associated with the procedure as compared with total gastrectomy. Whether gastroesophagostomy or jejunal interposition should be selectively performed after proximal gastrectomy is a controversial matter of opinion. Although gastroesophagostomy is a simple, easy, and safe procedure, it results in a high incidence of reflux esophagitis. In this respect, jejunal or jejunal pouch interposition is superior to gastroesophagostomy as a followup procedure to proximal gastrectomy. Recently, to achieve less invasive surgery, laparoscopic distal partial gastrectomies have been performed. Although the laparoscopy-assisted proximal gastrectomy with gastroesophagostomy was previously reported, no studies have reported laparoscopic proximal gastrectomy with jejunal interposition. Such a lack of studies is likely caused by the procedure's technical difficulty.
Uyama et al. demonstrated that completely laparoscopic proximal gastrectomy with jejunal interposition and lymphadenectomy is technically feasible, safe, and enables oncologically curative resection and open surgery ( 33, 34 ).
Proximal gastrectomy is currently accepted by surgeons as the most favorable type of operation for the treatment of early gastric cancer in the upper third of the stomach, from both a hormonal and a nutritional perspective. In advanced gastric cancer, total gastrectomy combined with lymph node dissection, a radical procedure, is widely used, because these cases are often complicated by lymph node metastases along the lower part of the stomach. On the other hand, various surgical procedures that preserve organs and their functions to the greatest possible extent have been advocated and put into practice. Besides, several reports have demonstrated that lymph node metastases were found in the splenic hilum but were not found along the lower stomach when the depth of invasion was limited to the muscularis propria. Because of this, proximal gastrectomy with splenectomy is an acceptable treatment for gastric cancer in the upper third of the stomach when the depth of invasion is limited to the muscularis propria.
Ikeda et al report a hand-assisted laparoscopic procedure that allows lymph node dissection and gastrointestinal reconstruction to be safely and easily performed ( 35 ).

Laparoscopic-assisted pylorus preserving gastrectomy has also been attempted. Because nodes at the infrapyloric or suprapyloric regions remain unless there is complete dissection ( they belong to the N1 group ), this procedure is indicated when lesions at these two sites are without node metastases ( 14 ).
Horiuchi et al ligated the right gastroepiploic vessels and gastric vessels 1 cm from their origins, whereas Nakane et al preserved the right gastric vessels, vagal nerve, suprapyloric nodes and severed the right gastroepiploic vessels at its origin ( 36, 37 ). There have been no solid data, however , on tumors that do not have nodal metastases at those sites. Without this information, it may not be appropriate to limit nodal dissection from N2, except as part of a clinical study protocol ( 14 ).

So far, all reports of laparoscopic gastric resection for gastric cancer suffer from uncontrolled design, small numbers, and limited follow-up. A number of randomized, controlled trials are ongoing, and the results are awaited with interest. Until the data from these trials become available, laparoscopic gastrectomy should be considered only in select cases. Patients with early mucosal disease seem to be candidates for MIS procedures given the low ( <2% ) risk of nodal disease. In addition, those patients with advanced disease in whom a palliative resection is considered are also suitable candidates. For the remainder of patients, who currently constitute the majority of our practice, laparoscopic gastrectomy, although it seems safe and oncologically sound, should be recommended only within the confines of investigational trials ( 1 ).
Although the technical feasibility of D1 ( D2 ) nodal dissection using LAG has been shown, methodologic variations have been noted among practitioners. The method for electing appropriate patients has not been established. Therefore, the efficacy of nodal dissection with LAG compared with conventional open gastrectomy requires further evaluation before laparoscopy can supplant open radical surgery as the standard procedure, as has been done with laparoscopic colecystectomy ( 13 ).


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