TY - JOUR AU - Douglass, Jr, Harold O. AB - Worldwide, gastric cancer ranks second only to lung cancer in mortality and accounts for 500 000 deaths annually. Since 1930, the incidence of gastric carcinoma in the United States has been declining steadily and plateaued during the 1980-1990 decade. Mortality rates for white males in the United States were approximately 40 per l00 000 in l930, compared with 5.4 per 100 000 in l994. For nonwhite males the rates were 23.7 per 100 000 in 1955 and 12 per 100 000 in 1985. In the United States in 2002, an estimated 21 600 new cases and 12 400 deaths were attributable to gastric carcinoma.Surgical resection remains the cornerstone in achieving a cure. To be effective therapy, surgical resection should address the following 4 directions of locoregional extension of gastric carcinoma: horizontal extension in the stomach wall, vertical extension through the stomach wall to the adjacent structures, lymph node metastases, and peritoneal dissemination. As such, surgical strategy involves gastric resection, en bloc resection of adjacent involved structures, omentectomy with resection of the lesser sac, and a systematic lymph node dissection.The Japanese Research Society for Gastric Carcinoma introduced the general rules that classified the lymph nodes into 16 stations by locations which are then categorized into 4 tiers (Figure 1and the Figure 2).The D-level of lymphadenectomy is based on the resection of Japanese Research Society for Gastric Carcinoma–defined nodal stations. When all N1 lymph nodes are removed but 1 or more N2 stations are left behind, the lymphadenectomy is designated as D1. When all N1 and all N2 stations are resected but not all N3 stations, the dissection is defined as D2 lymphadenectomy. We label our technique as a "D2.5 lymphadenectomy," since in our dissection the upper para-aortic and the hepatoduodenal lymph nodes are resected in addition to removing the N1 and N2 nodal stations.Despite the controversy in Western countries regarding the survival benefit of extended lymph node dissection, alternative treatment modalities are of limited therapeutic value. As long as surgery remains the most effective therapy, D2 lymphadenectomy will continue to be performed because it permits a curative R0 resection, achieves better locoregional tumor control, and provides the only chance for cure among patients with N2 disease. Hence, a detailed stepwise description of the D2.5 lymphadenectomy to familiarize readers with the technical details of such a demanding surgical procedure would represent a valuable educational tool.Figure 1.Lymph node stations according to the Japanese Research Society for Gastric Cancer. A, Stations 1 through 6 (N1), 7, 9, 12, and 14 are seen. CHA indicates common hepatic artery; LGA, left gastric artery; SGA, short gastric arteries; LGEA, left gastroepiploic artery; SPA, splenic artery; RGEA, right gastroepiploic artery; RGEV, right gastroepiploic vein; SMA, superior mesenteric artery; SMV, superior mesenteric vein; MCA, middle colic artery; and MCV, middle colic vein. B, Second echelon (N2) lymph node stations 7 through 11 and third echelon (N3) lymph node stations 12 through 14 are seen. PV indicates portal vein; CA, celiac axis; SV, splenic vein. See Figure 2for the location of the stations.Figure 2.Grouping of lymph node (LN) stations according to the location of the gastric cancer. CA indicates celiac axis; CHA, common hepatic artery; LGA, left gastric artery; MCA, middle colic artery; SPA, splenic artery.TECHNIQUEPOSITIONThe patient is placed in the supine position and both the chest and the abdomen are prepared and draped in case the incision needs to be extended to perform a lower median sternotomy or extended into the right or left pleural cavity. The patient undergoes general anesthesia with placement of an endotracheal tube, nasogastric tube, and a Foley catheter.INCISIONSeveral upper abdominal incisions may be used, although a midline incision is generally preferable extending from the xiphoid process to below the umbilicus by passing to its left side. The xiphoid process can be amputated if necessary.EXPLORATIONA methodical exploration is undertaken with particular attention paid to examining the tumor at the end. Any ascitic fluid present is aspirated before manipulation of intra-abdominal contents and sent for cytologic examination. The right and the left paracolic gutters are carefully surgically explored in search of peritoneal implants from which, if present, a biopsy specimen should be obtained for frozen-section examination. The greater omentum is then carefully palpated and lifted out of the abdomen to examine the infraomental structures. This is performed in a clockwise direction beginning in the right lower quadrant with the ileocecal region and ending in the pelvis. The pelvic peritoneum, pouch of Douglas, and, in females, the ovaries are inspected. The base of the transverse mesocolon and the para-aortic region is palpated for the presence of suspicious lymphadenopathy. The small bowel and its adjacent mesentery are inspected from the duodenojejunal flexure and ending at the ileocecal region.The right diaphragmatic surface is palpated and visualized for peritoneal implants. The liver is examined next, beginning with the right lobe followed by the falciform ligament and then the left lateral lobe. The left diaphragmatic surface is then carefully palpated and inspected. Finally, attention can be directed toward the stomach itself, beginning from the esophageal hiatus and proceeding distally toward the duodenum. The lesser omentum is divided close to the left lobe of the liver to evaluate the body and tail of the pancreas and to determine whether there is any extension of the tumor to these structures. The spleen and then the splenic hilum are assessed either for the presence of abnormal lymphadenopathy or for evidence of direct extension. Finally, the lesser sac is irrigated with a solution of 5% dextrose in water; the aspirated fluid is sent for cytologic examination. Once the systematic exploration of the abdomen is completed, a self-retaining retractor system is arranged with particular attention paid to adequate upward retraction of the costal margins to provide a wide operative field.DISSECTION TECHNIQUEThe extent of gastric resection is determined by the location and local extension of the tumor and can include total gastrectomy, distal subtotal gastrectomy, or esophagogastrectomy. To achieve an R0 resection, the en bloc resection may include composite resection of the transverse colon, body and tail of the pancreas, and the liver, if invaded directly by the primary tumor.We will begin by describing the technique of the D2.5 total gastrectomy. The resection begins by performing a total omentectomy with en bloc resection of the lesser sac also termed "omentobursectomy." The omentum is lifted upward and, starting on the right side of the midline, it is separated from the colon in the thin avascular plane using gentle strokes of electrocautery. To resect the posterior lesser sac peritoneum, the anterior leaf of the transverse mesocolon is carefully elevated taking care to avoid damaging the underlying middle colic vessels. Gentle dissection using a Kittner blunt dissector (Eagle Endoscopic Inc, Bartonville, Tex) is a useful maneuver. This portion of the procedure can also be facilitated by intermittent injection of a sterile saline solution (hydrodissection) beneath the anterior leaf of the transverse mesocolon (Figure 3). This dissection becomes more difficult on the left side of the midline but is carefully continued until the pancreas is reached and this filmy peritoneal lining is then lifted away from the body of the pancreas.Figure 3.With the stomach retracted upward, an omentobursectomy is performed by resecting the anterior leaf of the transverse mesocolon which is facilitated by hydrodissection (injection of a sterile saline solution).Attention is directed toward the right side of the lesser sac where in the region of the middle colic vein the right gastroepiploic vein is identified, carefully dissected, ligated in continuity with 3-0 silk sutures, and divided at its origin. Sometimes division of the pancreaticoduodenal vein is also necessary. Dissection of the anterior pancreatic capsule is continued toward the gastroduodenal artery. The gastroduodenal artery is followed caudally until the origin of the right gastroepiploic artery is reached and ligated. With ligation and division of the right gastroepiploic artery, the subpyloric package of lymphoareolar tissue (station 6) is swept upward to be included with the specimen (Figure 4). In this area, meticulous dissection of the fine vessels supplying the duodenum is necessary. Next, as the posterior wall of the first part of the duodenum is carefully freed, the gastroduodenal artery is traced to its origin from the common hepatic artery. Visualization of this junction is the last step of this phase of the duodenal dissection.Figure 4.With ligation and division of the right gastroepiploic artery, the subpyloric package of lymphoareolar tissue (station 6) is swept upwards to be included with the specimen.Superior dissection of the duodenum begins by first mobilizing the hepatic flexure that allows the colon to be reflected downward. A wide Kocher maneuver is performed and the descending portion of the duodenum brought forward to visualize the posterior surface of the pancreatic head. The fibrolymphatic tissue and the associated nodes in this location (station 13) are carefully elevated from the duodenum and the adjacent head of the pancreas up toward the portal vein (Figure 5). Meticulous dissection must be performed to avoid pancreatic injury that can result in postoperative pancreatic fistula. This portion of the dissection exposes the aorta and the inferior vena cava for subsequent para-aortic (station 16) dissection if indicated.Figure 5.A wide Kocher maneuver to expose retropancreatic (station 13) and para-aortic (station 16) lymph nodes.Attention is directed toward the lesser omentum which is divided along the left lobe of the liver, from right to left, toward the right edge of the esophageal hiatus. Returning back to the hepatoduodenal ligament, the hepatic artery pulse is palpated, and the overlying peritoneal lining is incised downward toward the duodenum to allow identification of the origin of the right gastric artery. The right gastric artery is then carefully isolated, ligated in continuity, and then divided at its origin from the hepatic artery. Subsequently, the lymph nodes in station 5 (suprapyloric) are swept toward the superior border of the duodenum to be included in the specimen. The site of duodenal division is chosen, and here, several branches that it receives from the gastroduodenal artery are carefully isolated, ligated in continuity, and then divided. Now, the mobilized first part of the duodenum is transected with a linear stapling device.The stomach is lifted out of the abdomen, reflected upward and to the left side. This makes the pancreas, the hepatoduodenal ligament, and the celiac axis accessible for continued D2 lymph node dissection. At the liver hilus, the peritoneal lining overlying the hepatoduodenal ligament is incised from the left edge, across two thirds of its width, and then downward toward the superior border of the duodenum (Figure 6, Inset). In this fashion, the anterior peritoneal lining of the ligament is open and the hepatoduodenal lymph node dissection (station 12) begun by skeletonizing the hepatic artery proper (Figure 5). Continuing over the right side, lymph nodes on the right side of the bile duct (station 12b) and behind the portal vein (station 12p) are dissected downward toward the pancreatic head where the earlier retropancreatic (station 13) dissection had been undertaken.Figure 6.The lesser omentum and the peritoneal lining overlying the hepatoduodenal ligament is incised from the left edge, across two thirds of its width, and then downward toward the superior border of the duodenum (Inset). The anterior peritoneal lining of the ligament is open and the hepatoduodenal lymph node dissection (station 12) begun by skeletonizing the hepatic artery proper.The hepatoduodenal and the retropancreatic lymph node packages are then deflected to the left. Lymphadenectomy is continued by skeletonizing the common hepatic artery and extended toward the celiac axis. All connective tissue, including the lymph nodes around the aorta adjacent to and around the celiac axis, are swept superiorly upward toward the left gastric artery, leaving the arteries completely bare (Figure 7). The left gastric vein and the left gastric artery are carefully isolated, ligated in continuity, and then divided. Suture ligatures are placed on the vessel stumps for further security.Figure 7.The hepatic artery, celiac axis, and the proximal splenic artery have been skeletonized. A spleen-sparing lymphadenectomy at the splenic hilum (station 10) is shown.Attention is directed toward the dissection around the esophageal hiatus. To facilitate this dissection, the stomach is again replaced within the abdomen. To improve exposure of the esophageal hiatus, the left lateral lobe of the liver is mobilized by dividing the left triangular ligament. The left lateral lobe can then be folded and retracted. The previously divided lesser omentum is then continued over the phreno-esophageal ligament that should be sufficiently high to allow the small paraesophageal lymph nodes, to the right and left of the esophagus, to be brought down with the specimen. With downward traction applied on the stomach, the gastrophrenic ligament extending between the fundus and the diaphragm is incised. All the retroperitoneal tissue on the crura is carefully stripped toward the specimen. A Penrose drain is passed around the abdominal esophagus to provide downward traction. This facilitates identification of the anterior and the posterior vagus nerves that are divided between hemoclips. Any surrounding lymphoareolar tissue is divided and swept downward to the specimen to delineate the site for esophageal transection.Traditionally, D2.5 lymphadenectomy includes a pancreaticosplenectomy. In-continuity splenectomy is indicated for upper greater curvature, posterior wall, and linitis plastica gastric cancers because the lymph nodes at the splenic hilum are in the primary lymphatic drainage basin for these sites. For this reason, virtually every patient undergoing total gastrectomy requires en bloc splenectomy.The stomach is again elevated out of the abdomen to allow exposure of the splenic artery just above the superior border of the pancreas. With the pancreas pulled gently downward by an assistant, connective tissue is incised along the superior border of the pancreas from the gastroduodenal artery to the middle part of the splenic artery. The proximal splenic artery (station 11) is then skeletonized meticulously by dissecting the connective tissue above the pancreas. During this exposure, opportunity is taken to mobilize the superior and inferior border of the pancreatic body and tail that facilitates subsequent pancreaticosplenectomy if the pancreas or spleen is directly invaded by the gastric cancer. In this situation, the spleen is mobilized by division of the lateral peritoneal reflection.Careful handling of the spleen, with the palm of the hand rather than grasping it with the thumb and fingertips, is necessary to avoid the fingers penetrating the splenic capsule and causing bleeding. The spleen is mobilized and its bed is sequentially packed with laparotomy pads for hemostasis and to facilitate bringing the spleen into the wound. The retroperitoneal dissection continues medially so the tail of the pancreas can also be elevated up into the incision. Then, the splenic artery previously stripped and exposed at its origin is carefully ligated in continuity, and suture ligated. The splenic vein lying along the posterior surface of the pancreas is exposed, ligated in continuity, and suture ligated. Following this, the pancreas is transected with a linear stapling device.A pancreaticosplenectomy is not necessary to achieve complete dissection of the lymph nodes in station 10 (of the splenic hilum) and station 11 (splenic artery). These nodes can be patiently dissected away from the splenic artery and hilum of the spleen (Figure 6). Operative time is prolonged, but morbidity and mortality are reduced and survival is unaffected. When there is no direct invasion of the tumor to the pancreas and there are no visible lymph node metastases attached to the organ, a pancreas-preserving technique should be used. The mere presence of enlarged lymph nodes along the splenic artery without direct invasion into the pancreas does not preclude pancreas-preserving D2.5 dissection. The pancreas-preserving lymphadenectomy described by Maruyama et alwill be outlined here. This technique begins by first isolating the origin of the splenic artery which is ligated in continuity with 0-0 silk and then divided (Figure 8). The lymph nodes along with the splenic artery are gently freed from the superior border of the pancreas which involves division of the caudal and greater pancreatic arteries (Figure 7). Finally, the tail of the pancreas is reflected and on the posterior surface the splenic vein is dissected, ligated in continuity with 0-0 silk, divided, and the spleen thus removed en bloc. This approach carries the potential risk of devascularizing the tail of the pancreas and, therefore, our preference is to ligate the splenic artery near the hilum rather than at its origin.Figure 8.A, Pancreas-preserving lymphadenectomy includes proximal ligation and division of the splenic artery after dissecting it from the superior border of the pancreas. B, Small tributaries from the splenic artery to the pancreas remain to be divided and ligated.If the spleen is also being preserved, then the previously skeletonized proximal part of the splenic artery is then followed to the spleen to permit removal of the lymph nodes in the splenic hilum. The spleen is replaced in the left upper quadrant of the abdomen. The entire specimen remains attached solely by the abdominal esophagus.If the tumor lies close to the cardioesophageal junction or extends up into the esophagus, further exposure of the esophagus is necessary to obtain a sufficient proximal surgical margin. A "diaphragmatic approach" with circular resection of the diaphragm at the esophageal hiatus is useful to obtain a wide operative field of the posterior mediastinum without opening either pleural cavity or the need for a median sternotomy. If the diaphragm is not directly involved by the tumor, then the hiatus is opened anteriorly and toward the patient's right (to avoid the pericardium) by dividing the diaphragm between clamps. This incision is placed slightly to the surgeon's left at approximately the 11-o'clock position. Alternatively, if there is direct invasion of the diaphragm, then circular resection of the hiatus and the involved diaphragm is necessary. For this approach, the peritoneum around the esophageal hiatus is removed to expose the diaphragm and the crura. Next, with blunt finger dissection, the pleura is separated from the diaphragm. The esophageal hiatus is then resected in a circle extending from one crura to the other. The bleeding vessels from the diaphragm are secured with transfixing sutures. The opening, thus created, allows a wide surgical exposure of the lower posterior mediastinum. If additional exposure is required, then the lower sternum can be split up to the level of the third or fourth interspace. After separating the sternum with a Touffier retractor, the incision in the diaphragm is extended superiorly toward the sternum but kept slightly to the patient's right to avoid entry into the pericardial cavity.Before beginning the process of esophagojejunal anastomosis, the entire specimen is again lifted out of the abdomen to inspect the gastric bed for hemostasis. Before transecting the esophagus, the proximal jejunum is prepared for the anastomosis. Starting from the ligament of Treitz, the first loop of jejunum that reaches the esophageal hiatus without tension is chosen and divided with a linear stapling device. The peritoneal lining over the mesentery is incised on both sides and the vascular arcades are clamped, divided, and ligated carefully to ensure viability of both jejunal limbs.Next, preparation is made for the esophagojejunostomy. Two stay sutures are placed in the esophageal wall proximal to the proposed line of transection. Through a defect in the transverse mesentery to the left of the middle colic artery, the distal jejunal limb is brought toward the esophageal hiatus in a retrocolic manner. The previously placed nasogastric tube is withdrawn, the esophagus is transected, and the resected specimen is then sent to the pathologist to obtain frozen sections of the proximal and the distal margin. If the margins are reported to be free of tumor, then the anastomosis can proceed. A hand-sewn anastomosis can be constructed with a single layer of interrupted 2-0 monofilament polypropylene. Alternatively, a stapled anastomosis can be constructed with a 25-mm circular stapler. The lubricated anvil is gently passed into the esophagus and the purse string basting suture is carefully tied down. Through the open end of the jejunal limb, the stapling device is passed approximately 3 to 4 cm distally. The spike of the stapling device is brought out through the antimesenteric border of the jejunum and engaged with the anvil. After the device is then closed, and fired, the 2 donuts from the stapling device are inspected to ensure that they are complete. The nasogastric tube is then advanced across the anastomosis and into the distal limb under direct visualization. The open end of the jejunal limb is closed with a linear stapling device.If a jejunal pouch is desired, a doubled loop of jejunum (15- to 18-cm length each) is stapled together by placing 2 GIA 90 stapling devices in an upward and downward direction through enterotomies in the central part of the pouch. The circular stapler (CEEA circular stapler; Tyco, Norwalk, Conn) with a diameter of 25 to 31 mm is then inserted through the enterotomy in the central portion of the pouch, to construct an end-to-side esophagopouch anastomosis. The enterotomy is then closed with an inner layer of continuous 3-0 absorbable suture and an outer layer of Lembert suture with 3-0 silk.After the esophagojejunal anastomosis is completed, the jejunal limb is tacked to the hiatus of the preaortic fascia with interrupted 3-0 silk to avoid any tension on the anastomosis. Next, to avoid any internal hernias, the opening in the transverse colon is sutured around the jejunal limb. About 45 cm from the esophagojejunal anastomosis (or 30 cm from a jejunal pouch), a jejunojejunostomy is performed. Distal to the jejunojejunostomy, a standard "Witzel" feeding jejunostomy is placed.After completion of the resection, only the operating surgeon would be familiar with the orientation of the specimen and the lymph node package. Therefore, on the back table, the surgeon carefully excises the individual lymph node package, places each in specimen jars, and labels the lymph node station numbers for the pathologist.CLOSUREThe linea alba is approximated with a 1-0 monofilament suture. Skin is closed with staples. If the diaphragm had been incised or resected, chest tubes are inserted.COMMENTThe extent of lymph node dissection for gastric adenocarcinoma continues to be debated, in particular its importance for accurate staging and possibly for improved survival.Japanese surgeons postulate that D2 radical gastrectomy with extended lymph node dissection is a logical operation for gastric cancer based on the theory that regional spread of gastric cancer usually occurs in stepwise manner from the first tier to the third tier of lymph nodes. Their standardized D2 dissection has been reported to achieve improved long-term survival and therefore Japanese Research Society for Gastric Carcinoma considers gastric resection without extended lymph node dissection an inadequate oncologic operation. The lack of popularity of D2 lymphadenectomy in Western countries has been due to the perceived high morbidity and mortality, lack of survival benefit reported by 2 prospective randomized trials, and the premise that the benefits in Japan are predominantly due to stage migration or that there are biological differences in gastric cancers seen in Asia vs the Western countries. Failure of the prospective randomized trials in Europe to demonstrate survival benefit must be interpreted with caution since the authors of these trials believe that distal pancreaticosplenectomy was responsible for this increased morbidity and mortality and not the lymphadenectomy itself. Moreover, these results cannot be generalized because the morbidity and mortality after D2 gastrectomy in specialized centers approximates those reported in Japan. Unfortunately one of the limitations of D-assignment of lymphadenectomy is that the status (resected vs unresected) of only 1 station can denote the difference between a D1 and a D2 dissection or the difference between a D0 and a D1dissection. To predict the correct levels of lymph node dissection, the Maruyama computer program was developed from a database of 3843 patients with gastric carcinoma treated with D2 or D3 lymph node dissection at the National Cancer Center Hospital in Tokyo.Clinical applicability of this program was validated by Bollschweiler et aland was also used to predict the percentage likelihood of metastatic disease in the regional lymph node stations left undissected by the surgeon in the Intergroup 0116 trial. The sum of these predictions was termed the Maruyama Index of Unresected Disease that was demonstrated to be an independent predictor of survival in an elegant analysis reported by Hundahl et al.When performing radical gastric resection for gastric carcinoma, the surgeon needs to be aware of several technical aspects of the procedure: (1) subtotal vs total gastrectomy, (2) spleen preservation vs splenectomy, (3) preservation of the pancreas vs left-sided pancreatectomy, and (4) limited D1 resection vs extended D2/D3 lymphadenectomy. Whether a distal subtotal or a total gastrectomy is performed depends on the location of the tumor. In the case of linitis plastica, total gastrectomy is recommended even if it is located near the lower gastric body, owing to the frequent submucosal extension of cancer. Total gastrectomy would also be necessary for patients with large lesser curvature lesions. Furthermore, total gastrectomy should also be performed for large tumors of the posterior wall of the stomach, body of the stomach, and the greater curvature. As a general rule, if the tumor impinges, or lies beyond an imaginary line extending from the incisura angularis to the bare area between the right and left gastroepiploic vessels on the greater curvature, total gastrectomy is necessary because the lymph drainage from such a tumor feeds into the splenic hilum and flows along the splenic artery as well as passing proximally and distally. Tumors limited to the antrum can be adequately treated with a distal subtotal gastrectomy. Owing to the differences in the submucosal extension between the intestinal- and the diffuse-type gastric cancer, some authors have recommended a gross surgical margin of at least 8 cm in the diffuse type, as opposed to 6 cm for the intestinal type. This information may be available preoperatively from the gastric biopsy specimen and from findings on endoscopic ultrasonography if it was performed.Resection of the tail of the pancreas and the spleen considerably increases the morbidity of the D2.5 resection and was the source of major problems in the Dutch randomized study of D2 dissection.For tumors that necessitate a total gastrectomy, splenectomy is usually performed. For tumors for which a distal subtotal gastrectomy is performed or for early gastric cancer on the lesser curvatures, the spleen can be preserved without an increased risk of local recurrence. Traditionally, a distal pancreatectomy and splenectomy were considered standard to allow complete resection of lymph nodes in the splenic hilus and along the splenic artery. However, when there is no direct invasion of pancreas or absence of macroscopically metastatic nodes along the splenic artery, the pancreas-preserving D2.5 lymphadenectomy is a viable alternative to reduce morbidity.Radical gastrectomy with a systematic approach toward regional lymph node dissection allows accurate pathological staging and consequently stratifies the patient into appropriate risk groups for adjuvant therapy. 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Khatri, MD, Division of Surgical Oncology, University of California, Davis, Cancer Center, 4501 X St, Suite 3010, Sacramento, CA 95817 (e-mail: vijay.khatri@ucdmc.ucdavis.edu).Accepted for publication November 18, 2003. TI - D2.5 Dissection for Gastric Carcinoma JF - JAMA Surgery DO - 10.1001/archsurg.139.6.662 DA - 2004-06-01 UR - https://www.deepdyve.com/lp/american-medical-association/d2-5-dissection-for-gastric-carcinoma-0oW7edr2U2 SP - 662 EP - 669 VL - 139 IS - 6 DP - DeepDyve ER -