Adult Chest Surgery

Chapter 11. Surgical Approach to Gastroesophageal Junction Cancers 


In the Western world, adenocarcinoma of the proximal stomach and esophagogastric junction (AEG) continues to rise in incidence and prevalence.The literature regarding the optimal surgical approach to these tumors has been a source of considerable controversy. Much of this debate stems from the fact that many surgeons still practice a rather indiscriminate approach to adenocarcinomas that arise at or close to the AEG.As a consequence of the worldwide acceptance of the AEG classification system and use of this system in several prospective trials, clearer guidelines on how to treat the various types of AEG adenocarcinomas are now being published.

In 1998 we defined adenocarcinomas of the AEG as tumors that have their center within 5-cm proximal and distal of the anatomic cardia and comprise one of three distinct tumor entities within this area.These entities are (1) adenocarcinoma of the distal esophagus (AEG type I tumors), which usually arises from an area with specialized intestinal metaplasia of the esophagus, that is, Barrett's esophagus, and may infiltrate the AEG from above; (2) true carcinoma of the cardia (AEG type II tumors), which arises from the cardiac epithelium or very short segments with intestinal metaplasia at the AEG; and (3) subcardial gastric carcinoma (AEG type III tumors), which infiltrates the AEG and distal esophagus from below (Fig. 11-1).

Figure 11-1.


AEG classification.


This system of classification is purely morphologic and based on the anatomic topographic location of the tumor center or, in patients with an advanced tumor, the dominant location of the tumor mass. Although all three of these tumor types share a number of common features, there are marked discrepancies in epidemiology, etiology, tumor biology, and pattern of lymphatic spread, particularly between type I and III tumors.Type II tumors include those type I tumors that arise from short Barrett's mucosa segments as well as typical cardia gastric cancers. Accordingly, in approximately 25% of the specimens of resected AEG type II tumors, it is possible to demonstrate goblet cells (i.e., tumors that arise from short Barrett mucosa segments), whereas 75% are typical cardia gastric cancers. As a consequence, one can combine the AEG type II and type III tumors at least with respect to the surgical consequences.5–7

Only has the most recent version of the unified International Union Against Cancer (UICC) and the American Joint Committee on Cancer (AJCC) TNM classification system taken AEG into account.The gastric cardia is now clearly considered to be part of the stomach. Consequently, tumors that arise in this location should be staged according to gastric cancer guidelines. When assigning a T category, it must be considered that the gastroesophageal junction, the posterior wall of the proximal fundus, and large portions of the lesser and greater curvature of the proximal stomach are not covered by the visceral peritoneum, which usually delineates the border between a pT2 and a pT3 category. To account for this situation and to better reflect the true depth of wall penetration of a tumor at these locations, the pT2 category has been divided into a category pT2a (no wall penetration) and pT2b (complete wall penetration but no serosal infiltration). Our own survival analysis based on the true depth of invasion supports this differentiation by showing a significant prognostic difference between pT2a and pT2b tumors.Therefore, the prognosis of pT2b tumors is close to the prognosis of the pT3 tumors.

As a consequence of the partial extraperitoneal location of the AEG, the classification of lymph node metastases also deserves special attention. One of the main lymphatic pathways from these tumors is via extraperitoneal drainage into the retropancreatic region and the left renal hilum7,10,11 (Fig. 11-2). The current version of the UICC classification does not account for this specific situation. Consequently, it remains unclear whether retroperitoneal lymph node metastases in these patients represent regional lymph node metastases (N category) or distant metastases (M1lymph category). Until this question is definitively answered, not only the number but also the location of involved lymph nodes should be stated in the pathology report.

Figure 11-2.


Retroperitoneal lymphatic spread of carcinoma of the gastric cardia toward the left renal vein. (Left) Schematic depiction. (Right) CT image.


Surgical resection is the mainstay of therapy in patients with R0 resectable AEG adenocarcinoma who have no evidence of distant metastases and are fit for surgery. Complete resection of the tumor and its entire lymphatic drainage has the best potential for long-term survival. Today, there is wide agreement in the literature that AEG type I tumors require a fundectomy with subtotal esophagectomy (Ivor Lewis procedure), not a transhiatal esophagectomy, whereas an extended gastrectomy is the procedure of choice for proximal gastric cancers (AEG type III tumors).The optimal access route and extent of resection for carcinoma of the gastric cardia (AEG type II tumors) are discussed controversially. The reported surgical approaches vary widely and include abdominal, abdominal–right transthoracic, abdominal–left transthoracic, left transthoracic with phrenotomy, and abdominal–cervical access routes. Similarly, the extent of resection ranges from limited resection of the AEG to total esophagogastrectomy with varying degrees of lymphadenectomy. On the basis of published trials,12–14the extended total gastrectomy is adequate for AEG type II tumors if the proximal extent of the tumor is R0 resectable from below after wide splitting of the hiatus. If R0 resection via transhiatal access is not attainable (i.e., the tumor cannot be reached), an abdominal thoracic procedure from the right side (Ivor Lewis procedure) is the operation of choice, as in AEG type I tumors.

When selecting the approach to adenocarcinoma of the AEG, oncologic aspects, that is, complete tumor removal and adequate lymphadenectomy, morbidity and mortality of the procedure, and postoperative quality of life all must be taken into account.2

From the oncologic point of view, both the luminal extent of resection and the extent of lymphadenectomy should be guided by the tumor location. In patients with carcinoma of the gastric cardia, adequate proximal and distal safety margins usually can be achieved by proximal gastric resection and removal of the distal esophagus. The extent of lymphadenectomy should be based on the prevalence and expected location of lymphatic metastases. In our experience, lymph node metastases are virtually never present in patients with tumors limited to the mucosa (pT1a) and are uncommon in patients with tumors limited to the submucosa (pT1b).15,16 This is also true when immunohistochemical techniques are used to search for micrometastases in lymph nodes of such patients. In patients with more advanced tumors, lymph node metastases occur primarily in the paracardial region, the lesser and greater curvature of the stomach, along the left gastric artery toward the celiac axis, at the superior border of the pancreas, along the splenic artery toward the splenic hilum, in the lower posterior mediastinum, and in the retropancreatic area toward the left adrenal gland and the left renal vein7,10,11 (Fig. 11-3). Lymphatic spread to the upper mediastinum or neck is a late phenomenon and an indication of systemic disease. Based on this pattern of lymphatic spread, an extended lymph node dissection in patients with AEG type II tumors should include the removal of lymph nodes along the splenic artery, at the splenic hilus, and in the retropancreatic area toward the left renal vein in addition to a formal D2 lymphadenectomy.

Figure 11-3.


Distribution of lymph node metastases in patients with true carcinoma of the gastric cardia (AEG type II tumors). Prevalence of positive nodes at various locations.

Morbidity and mortality of the procedure are determined by the access route and the extent of resection and lymphadenectomy. Morbidity and mortality are lowest with a pure transabdominal approach. A combined abdominothoracic procedure improves exposure in the lower mediastinum but increases postoperative morbidity, as does a thoracotomy with phrenotomy.17 Although a D2 lymphadenectomy can be performed as safely as a D1 lymphadenectomy in experienced hands, a left-sided pancreatic resection and splenectomy, which are often performed routinely in order to complete the retroperitoneal lymphadenectomy, are associated with substantial morbidity but no improved survival.18,19 In our opinion, splenectomy therefore should be performed only in patients with frank retropancreatic lymph node metastases or infiltration of the splenic hilum. To avoid the morbidity of pancreatic resection, this should be done in the form of a pancreas-preserving splenectomy, as described by Maruyama.20

Quality of life is determined primarily by the type of reconstruction. An esophagogastrostomy in the lower mediastinum, although easy and safe to perform, often leads to severe reflux of gastric and duodenal contents, intractable esophagitis, and poor quality of life. This can be avoided if the anastomosis between the remaining small stomach tube and esophagus is performed high in the pleural cavity, that is, above the level of the azygos vein, or the neck. Other alternatives to prevent reflux are interposition of jejunum or colon between the esophagus and gastric remnant. Since the reservoir function of the stomach is lost with resection of its proximal part, a preservation of the distal gastric portions only makes sense when it is used for reconstruction. From the physiologic point of view, preservation of the antrum (and corpus) does not add to alimentary function. A complete gastrectomy with Roux-en-Y diversion of the duodenal juice and esophagojejunostomy thus offers the same functional results as esophagogastrostomy with high intrathoracic anastomosis.17

Based on these concepts, surgical approaches to adenocarcinoma of the gastric cardia can be classified as procedures of first and second choice. First-choice procedures are the Ivor Lewis abdominal–right transthoracic approach with high intrathoracic esophagogastrostomy,21–23 an extended transabdominal total gastrectomy with Roux-en-Y esophagojejunostomy,24,25 and a limited transabdominal resection with jejunal interposition (Merendino).15,26 Transthoracic and transabdominal resections with esophagogastrostomy in the lower mediastinum must be considered second-choice procedures; the same applies for the left transthoracic approach with phrenotomy and colon interposition.22,23

The Ivor Lewis approach from the abdomen and right chest provides excellent exposure for mediastinal lymphadenectomy and a high intrathoracic esophagogastrostomy (see Chap. 16). The morbidity of this combined approach is, however, slightly higher than with transabdominal procedures. Postoperative swallowing function is usually not compromised. In the past, leakage of the intrathoracic anastomosis, which occurs in fewer than 10% of patients, was associated with substantial mortality. Now, leakages of the esophagogastrostomy can be covered by endoscopic stenting. If endoscopy is performed early, this procedure can successfully reduce the morbidity and mortality of these complications.

In our experience, a transhiatally extended total gastrectomy with esophagojejunostomy Roux-en-Y—provided that R0 resection is possible—is oncologically equal to the abdominothoracic approaches but is associated with lower morbidity and mortality.A wide splitting of the esophageal hiatus provides good access to the lower posterior mediastinum up to the level of the tracheal bifurcation. With circular staplers, a transhiatal esophagojejunostomy can be performed safely high in the mediastinum. Although sacrificing the entire stomach may not be necessary from an oncologic perspective, a functional advantage to preserving the gastric antrum and corpus has been difficult to show.27 Transhiatally extended total gastrectomy with esophagojejunostomy Roux-en-Y therefore constitutes the procedure of choice for patients with carcinoma of the gastric cardia or subcardial gastric cancer at our institution. Similar data favoring extended gastrectomy over esophagectomy or esophagogastrectomy for patients with true carcinoma of the cardia (AEG type II) also have been reported from other institutions.5,13,14,25,28 Limited transabdominal resection of the AEG with jejunal interposition (Merendino) is an alternative to transhiatally extended total gastrectomy in patients with early tumors. In our experience, the interposed jejunal segment reliably protects against reflux and provides a better quality of life than esophagectomy or total gastrectomy.4,15

Technique of Transhiatally Extended Total Gastrectomy

Access to the upper abdomen and esophageal hiatus is critical for this procedure. We use a wide inverse T-shaped upper abdominal incision with the patient positioned as shown in Figure 11-4. A special retractor system is used to lift the sternum and provide access to the posterior mediastinum (Fig. 11-5). The diaphragm is opened anteriorly starting from the esophageal hiatus. In advanced tumors, a rim of the diaphragmatic crura around the distal esophagus is excised, and both mediastinal pleural sheaths are resected en bloc with the AEG and distal esophagus (Fig. 11-6). The lower posterior mediastinum is exposed by insertion of two oversized retractors (Fig. 11-7). All lymphatic tissue in the lower posterior mediastinum up to the tracheal bifurcation thus can be removed en bloc with the distal esophagus. The posterior dissection layer is on the adventitia of the aorta. The esophagus is transected clearly above the proximal extent of the tumor (Fig. 11-8). Frozen sections to confirm a tumor-free margin in the esophagus are taken liberally. The total gastrectomy with D2 lymphadenectomy then is completed as described elsewhere in this text. In patients with frank lymph node metastases in the splenic hilum or the retropancreatic area, a pancreas-preserving splenectomy and lymphadenectomy of the retroperitoneal area is added. Otherwise, the spleen is preserved. Reconstruction is performed with a circular stapler as an end-to-side esophagojejunostomy (Fig. 11-9). The procedure is completed with a Roux-en-Y diversion of the duodenum (Fig. 11-10).

Figure 11-4.


Positioning of the patient (A) and inverse T-shaped upper abdominal incision (B) for transhiatally extended total gastrectomy.


Figure 11-5.


Special retractor to lift the sternum.


Figure 11-6.


Opening of the diaphragm and excision of the diaphragmatic crura.


Figure 11-7.


Approach to the posterior mediastinum with special rectractors and extent of mediastinal lymph node clearance.


Figure 11-8.


Transection of the esophagus above the tumor.


Figure 11-9.


Reconstruction with a circular stapler device in an end-to-side fashion.


Figure 11-10.


Schematic drawing of the reconstruction.

Technique of Limited Resection with Jejunal Interposition

The approach to limited resection of the AEG with jejunal interposition is the same as with transhiatally extended total gastrectomy. After a wide anterior splitting of the esophageal hiatus, the esophagus is transected at the level of the endoscopically marked oral end of Barrett's mucosa, and the head of the circular stapler is inserted. The distal resection margin is at the border between the proximal and middle gastric thirds. Lymphadenectomy in the lower posterior mediastinum is performed as described earlier. The area of upper abdominal lymphadenectomy includes the lymph nodes along the hepatic artery, celiac axis, and splenic artery. The left gastric artery is transected at its origin and remains with the resection specimen, as are the lymph nodes along the proximal half of the lesser curvature and the nodes along the greater curvature of the proximal gastric third. For reconstruction, a 15- to 20-cm-long jejunal loop with a strong vascular pedicle is isolated and interposed between the esophagus and proximal stomach in an isoperistaltic fashion (Fig. 11-11). The proximal anastomosis (esophagojejunostomy) is performed with the circular stapler in an end-to-side fashion, as described earlier. The distal anastomosis (jejunogastrostomy) is placed on the posterior gastric wall.

Figure 11-11.


Limited resection and jejunal interposition for early carcinoma of the gastric cardia.


Proximal gastrectomy for adenocarcinoma of the AEG has become an uncommon procedure. Usually the procedure is extended over various distances on the esophagus or the stomach. The required extent of resection depends on the anatomic topographic location of the primary tumor and its lymphatic spread. The AEG classification is a useful guide for determining the extent of the resection.4,17 For type I tumors, that is, adenocarcinoma of the distal esophagus, the procedure of choice is the Ivor Lewis approach with a high intrathoracic esophagogastrostomy. For type II and III tumors, that is, adenocarcinoma of the gastric cardia and subcardial gastric cancer, a transhiatally extended total gastrectomy with Roux-en-Y esophagojejunostomy has proved to be oncologically adequate, safer than a proximal gastrectomy with subtotal esophagectomy and provides better quality of life than proximal gastrectomy and a low mediastinal esophagogastrostomy. In patients with early cancer, limited resection of the AEG is possible, but reconstruction with jejunal interposition is required to avoid postoperative reflux. Figure 11-12 shows the choice of procedure according to the AEG classification as described in the literature on the basis of prospective trials.

Figure 11-12.


Choice of procedure based on prospective trials.


Siewert and colleagues' thoughtful approach to adenocarcinoma of the GE junction is based on a meticulous assessment of the location of the lesion and the patient's physiology. According to the authors, the best approach to type 1 tumors, or lesions of the distal esophagus, is a standard Ivor Lewis approach. They recommend transhiatal or extended transhiatal for type 2 and 3 lesions. I would still approach type 1 or 2 lesions with the left transthoracic, reserving the Ivor Lewis for more advanced lesions after chemoradiation. As for type 2-3 lesions, although the transhiatal or extended transhiatal may be appealing to general surgeons, most thoracic surgeons would use a standard or extended Ivor Lewis esophagectomy in this situation. This is especially pertinent to elderly or high-risk patients, where the oncologic benefits of an extended total gastrectomy may be outweighed by the added morbidity of the approach.


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