Preoperative patient assessment and staging

Esophagogastroduodenoscopy (EGD) commonly is performed as the first diagnostic tool to visualize the extent of the suspected tumor and to obtain biopsies for histologic confirmation of the diagnosis. EGD often is coupled with endoscopic ultrasound (EUS), which is now an essential step in staging esophageal cancer. EUS is the most accurate method of preoperatively assessing T status and has become a standard of care in staging esophageal cancer. EUS also can assess regional lymph nodes and guide endoscopic fine needle aspiration of suspicious lymph nodes. CT alone is not very accurate for establishing the nodal status; however, it is an important tool of preoperative planning, as it shows potential tumor invasion into adjacent structures. Positron emission tomography (PET) in combination with CT, otherwise known as PET-CT, is useful in searching for distant metastases. Finally, if involvement of the trachea by the tumor is suspected, a bronchoscopy should be performed.

Following the staging workup, treatment options should be discussed by the multidisciplinary team and reviewed with the patient. In patients who have early stage disease and without comorbid disease that would contraindicate esophagectomy, surgical resection should be offered as a potentially curative procedure. If patients have locally advanced disease, neoadjuvant chemotherapy and radiation therapy should be considered before proceeding with surgical resection. Proper preoperative assessment of the extent of tumor involvement is very important, as complete resection is a strong prognostic factor on outcome. When complete resection (R0) is not possible, no substantial long-term survival can be expected.

Surgical techniques

Various surgical approaches have evolved for esophageal resection. These vary by type, number, and location of incision(s) as well as by choice of conduit used for esophageal replacement and the location and nature of the anastomosis used. Which approach ultimately is employed depends on several factors related to the patient, the tumor, and the surgeon. The patient’s past medical and surgical history and their overall functional status will favor one approach over another. The description of each of these varied techniques follows, along with a discussion of the indications, advantages, and disadvantages of each respective approach.

Surgical techniques

Various surgical approaches have evolved for esophageal resection. These vary by type, number, and location of incision(s) as well as by choice of conduit used for esophageal replacement and the location and nature of the anastomosis used. Which approach ultimately is employed depends on several factors related to the patient, the tumor, and the surgeon. The patient’s past medical and surgical history and their overall functional status will favor one approach over another. The description of each of these varied techniques follows, along with a discussion of the indications, advantages, and disadvantages of each respective approach.

Preoperative endoscopy

Before any planned esophageal resection, regardless of the approach, a preoperative endoscopic evaluation of the esophagus, stomach, and proximal duodenum is essential to make a final determination of tumor location, dimension, and extent. It additionally provides the opportunity to assess the suitability of the stomach as a conduit. This can be done as a separate preoperative procedure in the endoscopy suite, requiring usually only moderate sedation, or as a combined procedure, under general anesthetic, just before commencing the formal esophageal resection.

Transthoracic esophagectomy (Ivor Lewis esophagectomy)

The original procedure as described by Ivor Lewis in 1946 to treat squamous cell carcinoma of the midesophagus was a two-stage approach including an abdominal incision to mobilize the gastric conduit followed, after an interval of 1 to 2 weeks, by a right thoracotomy for resection and reconstruction of the esophagus. Currently, the transthoracic esophagectomy is performed as a combined procedure requiring only one general anesthetic administration. This remains a favored approach for midesophageal malignancies and is used commonly for distal esophageal carcinomas.

With the patient in the supine position, a midline laparotomy incision is made, and the abdominal cavity is explored to rule out metastatic disease that would preclude a curative procedure and obviate the benefit of proceeding with the operation. Thereafter the stomach is mobilized on the right gastroepiploic artery pedicle. The short gastric vessels are divided, and the lesser sack is entered. The left gastric vessels are dissected out and divided at their origin, while the left gastric and celiac axis lymph nodes (levels 18 and 20, respectively) are removed. Gastric mobility is enhanced by mobilizing the duodenum using the Kocher maneuver. A pyloromyotomy or pyloroplasty is performed to assist with gastric drainage postoperatively. The start of lower esophagus dissection can be accomplished by means of the hiatus to begin this part of the resection that will be completed during the transthoracic portion of the procedure. The abdominal incision then is closed.

The patient is repositioned in the left lateral decubitus position in preparation for a standard right posterolateral thoracotomy, preferably in the fourth interspace (over the top of the fifth rib). After dividing the azygous vein, the esophagus is resected from the apex of the chest down to the hiatus. Paraesophageal and mediastinal lymph nodes are removed en bloc with the esophageal specimen. The stomach then is delivered into the chest and divided along the lesser curvature, taking the left gastric pedicle and lymph nodes with the resected specimen. The thoracic esophagogastrostomy is performed as cephalad as possible, with the goal being to achieve a level at least above the azygous vein. The thoracotomy then is closed after placing a chest tube to drain the pleural space.

Transhiatal esophagectomy

The transhiatal esophagectomy first was performed successfully by the British surgeon Turner in 1933. The concept of esophageal resection without a thoracotomy, however, originally was described by the German anatomist, Denk, in 1913. It was not until it was reintroduced by Orringer in the late 1970s that this operation regained common usage. The approach has become popular for treating lower esophageal tumors and early stage lesions such as Barrett’s esophagus with high-grade dysplasia.

The surgical procedure as performed routinely consists of an upper midline abdominal incision and left cervical incision. Similar to the transthoracic esophagectomy, the peritoneal cavity initially is explored to rule out metastatic disease. The gastric conduit is mobilized similarly on the right gastroepiploic pedicle.

The esophageal resection is begun by taking a rim of hiatus with the resected lower esophagus to ensure adequate radial margins and also provide a larger aperture through which to continue the transhiatal dissection. Retraction of the hiatus can be used to allow visualization of the dissection quite high up into the mediastinum. Nevertheless, the dissection beyond is carried up to the level of the thoracic inlet and is performed bluntly without direct visualization.

At this point, a left neck incision is performed to allow access to the cervical esophagus. Once the cervical dissection has met the transhiatal dissection, the proximal resection of the esophagus can be performed, usually 1 to 2 cm above the level of the clavicle. The esophagus then is delivered into the abdomen, and a distal resection margin is created on the stomach as described previously with the transthoracic approach. The gastric conduit then is delivered up to the cervical incision by means of the dissected transhiatal route. In this regard, it is important to minimize trauma to the gastric conduit and prevent it from rotating while delivering it through the posterior mediastinum. One frequently applied approach is to place the gastric conduit within a plastic bag that then pulls the stomach up to the neck using a combination of friction and suction to avoid undue damage to the conduit. The cervical esophagogastrostomy then can be performed before closing the neck and abdominal incisions.

Tri-incisional esophagectomy (McKeown esophagectomy)

The tri-incisional approach for esophagectomy first was described by McKeown in 1976, and consists of a right thoracotomy accompanied by cervical and abdominal incisions. It is an approach employed for both mid- and lower esophageal tumors. It is favored by those surgeons who seek direct visualization of the esophagus during its resection but also prefer a cervical anastomosis.

The initial portion of this procedure is performed through a right posterolateral thoracotomy via the fourth or fifth interspace. The esophagus is dissected as with the transthoracic approach. Once the esophagus and periesophageal tissue and lymph nodes have been mobilized, the chest is closed, and the patient is repositioned in the supine position. The remaining aspects of this operation are completed as described for the transhiatal approach. The laparotomy provides access to mobilize the gastric conduit, which is delivered to the cervical incision by means of the esophageal bed once the esophagus has been resected completely.

The advantages and disadvantages of the tri-incisional esophagectomy are similar to those stated for the transthoracic esophagectomy. In terms of advantages, these include direct visualization of mediastinal structures and mobilization of the thoracic esophagus, which is thought to allow for more complete lymph node dissection.

Minimally invasive esophagectomy

With the aim of reducing the surgical trauma and morbidity typically associated with conventional open esophagectomy, laparoscopic esophagectomy was introduced in the mid-1990s. The feasibility of this approach and the ability to reduce postoperative pain and decrease ICU stay and length of hospitalization have been demonstrated in various single-institution studies. Nevertheless, the requirement for advanced laparoscopic and thoracoscopic skills has limited the generalized adoption of these types of approaches.

There are several approaches used to accomplish a minimally invasive esophagectomy. At the authors’ institution, the following general approach to the minimally invasive esophagectomy has been adopted. The patient is positioned in the semilithotomy position as for other laparoscopic foregut procedures such as the more commonly performed laparoscopic Nissen fundoplication. The initial laparoscopic access allows for an exploration of the peritoneal cavity to exclude metastases that would obviate the benefit of an esophageal resection. Two 5 mm ports are placed below the costal margins on each side, and two further ports with larger diameter are positioned on the right and left sides of the epigastrium. The laparoscopic preparation of the gastric conduit is accomplished according to the previously described open techniques. Following completion of this, the laparoscopic ports are removed, and the patient is repositioned in a left lateral decubitus position in preparation for a right posterolateral thoracotomy. A 10 mm camera port is inserted at the eighth intercostal space in the midaxillary line. A utility incision is made in the fifth intercostal space between the pectoralis major and latissimus dorsi muscles. A 10 mm working port is placed posterior to the scapula at the fifth intercostal space. A second 10 mm working port is placed at the eighth intercostal space posteriorly. Through these ports, the azygous vein first is divided allowing the esophagus to be visualized and dissected along its entire length along with its associated lymph node tissue. Once the esophagus is dissected entirely, the stomach can be brought up into the chest through the hiatus. It is essential to preserve the correct orientation of the stomach while bringing it up into the chest to avoid ischemia or obstruction of the conduit. The resected esophagus and portion of proximal stomach are removed through the utility port within a surgical bag to avoid port site contamination. The esophagogastrostomy anastomosis then can be completed thoracoscopically.

The main controversy regarding the minimally invasive approaches to esophagectomy relates to whether these approaches achieve an equivalent oncologic result. Randomized, prospective trials comparing conventional open techniques with minimally invasive approaches have not been done. The likelihood of these being completed is also in question. Nevertheless, nonrandomized trials have shown that minimally invasive approaches are safe and comparable to the open approaches with regard to postoperative recovery and short-term survival. These also have shown that the duration of the minimally invasive esophagectomy is usually significantly longer than the conventional open approach. Because of the relative novelty of these techniques and therefore lack of long-term follow-up, there are insufficient data to determine long-term survival, the key question for proof of oncologic adequacy.

Comparison of surgical approaches

When comparing the different surgical approaches for esophagectomy, the various procedures provide options that allow for individualizing the operation to the patient and the specifics of their tumor. Midesophageal cancers, especially larger or more bulky tumors, tend to be better approached by direct visualization by means of a transthoracic or tri-incisional approach. The transhiatal or minimally invasive approaches may be favored in situations where the patient may have undue respiratory compromise from a thoracotomy required by the transthoracic or tri-incisional esophagectomies.

Whereas the cervical anastomosis of the transhiatal and tri-incisional approaches is associated with less postoperative reflux complications, it is associated with higher rates of anastomotic leaks than the transthoracic esophagectomy with an intrathoracic anastomosis. Conversely, a cervical anastomotic leak generally is tolerated better and easier to manage than the much more morbid intrathoracic anastomotic leak.

Comparative studies of transhiatal and transthoracic esophagectomies show no significant difference in the overall morbidity and mortality of both approaches and equivalent long-term survival. It is therefore a matter for the surgeon to decide on the best approach to esophageal resection for each patient depending on his or her specific condition and nature of the malignancy. A surgeon who is adept at all of these approaches is better able to individualize the surgical procedure to best fit the particular needs of the patient.

Options for esophageal replacement conduit

There are several options for conduits to replace the resected esophagus. The most commonly employed conduit is the stomach, while other options include pedicled segments of colon or jejunum and the infrequently used small bowel free graft. The advantage of the stomach as a conduit relates to its more constant and reliable blood supply, its relatively easier dissection and preparation, and the need for only one anastomosis. Prior gastric surgery, including prior fundoplication, may preclude the successful use of the stomach as a replacement conduit. Similarly, a poorly placed gastrostomy may risk rendering the gastric conduit unusable for esophageal replacement. Finally, in the case of Siewert type 3 tumors, emanating from below the gastroesophageal junction, total gastrectomy with distal esophagectomy appears to be the best option. Reconstruction usually is accomplished using a roux-en-y esophagojejunostomy.

If reconstruction with a gastric conduit is not possible, replacement with either colon or jejunum is considered. The first reports about the use of colon as a replacement graft after esophageal resection were published in 1911. Advantages of the colon conduit are a relatively consistent vascular anatomy, resistance to gastro–biliary reflux, intrinsic peristalsis, and the ability to maintain the stomach in the abdomen as a reservoir. Reconstruction of the esophagus with colonic interposition often is adopted for cases of congenital esophageal atresia but only occasionally as a conduit after esophagectomy for carcinoma. Patients should undergo a thorough preoperative assessment including a colonoscopy if a colon interposition is planned. Mesenteric angiography may be indicated to assess blood supply if there are questions of peripheral vascular disease. Colonic interposition is associated with higher rates of mortality and morbidity, including an increased anastomotic leak rate and conduit failure rate.

Jejunum as an esophageal replacement conduit can be used as either a pedicled graft to replace a short segment of distal esophagus or free graft extending higher toward and into the neck. Free jejunal grafts are not the conduit of first choice. They rarely are used and usually only for salvage situations when primary reconstruction with stomach or colon has failed. The advantages of the jejunal conduit are the avoidance of preoperative bowel preparation, active intrinsic peristalsis, and typically good luminal size match between the jejunum and esophagus.

Postoperative management

At the time of the operation, a nasogastric tube usually is placed to decompress the stomach during the first 1 to 2 days after surgery. This is in addition to the commonly performed pyloromyotomy or pyloroplasty to promote antegrade drainage of gastric contents. Gastric emptying also can be assisted with the postoperative use of prokinetic agents such as erythromycin or metoclopramide. In a further effort to avoid gastric distention in the early postoperative period, many thoracic surgeons discourage any oral intake for the first 4 to 6 weeks while using the feeding jejunostomy to provide nutrition in the interim.

One of the potential major complications of esophagectomy is an anastomotic leak. This has been reported in the modern literature to range from 0.8% to over 20%. Typically cervical anastomoses have a leak rate between 5% and15%, while for intrathoracic anastomoses this rate is usually between 1% and 4%. Identifying such anastomotic leaks is the object of much attention in the early postoperative period. Clinical suspicion based on physical findings and basic laboratory investigations is the initial method used for detection. The clinical scenario often will be very obvious in the case of a large anastomotic disruption. Bile exiting by means of the right chest tube following a transthoracic esophagectomy or saliva exuding from the neck incision after a transhiatal esophagectomy are incontrovertible signs requiring no further confirmatory testing. When these clear-cut signs are not present, the diagnostic modality most commonly employed is the contrast swallow. A postoperative contrast swallow is used almost routinely to evaluate intrathoracic anastomoses before patients are allowed to resume oral intake, because an intrathoracic leak is usually both more challenging to diagnose and more difficult to treat than one in the neck. Conversely, a radiologic leak, at the cervical level, without associated clinical findings, is usually inconsequential and requires no specific therapeutic intervention. Therefore, postoperative contrast studies have become less of a routine following transhiatal or tri-incisional esophagectomy that employs a cervical anastomosis. The decreased use of contrast studies has been advocated to avoid the real risk of aspiration pneumonia.