17: Three-Hole Esophagectomy: The Brigham and Women's Hospital Approach

The management of esophageal cancer has evolved tremendously over the past decade. Increasingly, patients are treated with an aggressive multimodal approach including neoadjuvant chemoradiotherapy followed by surgical resection.¹ Despite these changing trends in the treatment paradigm for esophageal cancer, esophagectomy remains the crucial component to long-term survival.

The key to success in managing patients with esophageal cancer is surgeon experience.² There are numerous approaches to esophageal resection and replacement, both open and minimally invasive, but all have the potential for a high rate of morbidity and mortality. Each esophageal surgeon must develop and refine a technique of resection that is safe and expeditious to minimize morbidity while aggressively pursuing standard oncologic principles including adequate resection margins and complete lymphadenectomy to help assure long-term survival.

The selection of operative approach is based on numerous factors: type and location of the lesion, extent of invasion, stage of disease, need for lymphadenectomy, history of previous surgeries, and type of conduit chosen for esophageal replacement (i.e., stomach, colon, or jejunum). Surgeon preference and experience plays an important role in the selection of the operation. Popular methods of esophageal resection in the United States are based on methods developed by Ivor Lewis and McKeown, among others.^3-5 They differ by the approach, number of incisions, and location of the anastomosis (intrathoracic or cervical) (Table 17-1). The three-hole esophagectomy at the Brigham and Women's hospital has evolved over time and is designed specifically to limit morbidity by assimilating the best elements of each of the predecessor surgeries in a safe and expeditious procedure.^6-9 This chapter will delineate the conduct of the operation and establish principles that can be applied to any approach for esophagectomy whether open or minimally invasive.

Even for experienced centers, esophagectomy is a difficult procedure to perform and is associated with a considerable risk of morbidity and mortality (Table 17-2). Careful preoperative assessment, as well as the prevention, detection, and early treatment of procedure-specific complications, is essential to an excellent outcome. The Brigham three-hole esophagectomy is conducted in two stages. First, the thoracic dissection is conducted under direct vision by means of a limited right muscle-sparing posterolateral thoracotomy. The patient then is moved from the left lateral decubitus position to the supine position for the second stage of the procedure, beginning with simultaneous upper midline and left cervical incisions.

The operation allows direct visualization of the entire esophagus for resection with ample longitudinal margins and the ability to perform a complete lymphadenectomy in both the chest and abdomen. The specimen and surrounding lymph tissues are removed en bloc before the conduit is fashioned and placed. We prefer to use a gastric conduit whenever feasible, but other conduits may be used (i.e., colon or jejunum). The operation is completed with a cervical anastomosis, which is easy to care for in the event of postoperative leak and associated with a lower incidence of recurrent gastric reflux than operations requiring an intrathoracic anastomosis.

The three-hole esophagectomy is ideal for patients with upper, middle, or lower third esophageal lesions. It is also suitable for patients with bulky tumors or with dense adhesions secondary to radiation therapy or caustic injuries, since the dissection is enhanced by the direct vision afforded by thoracotomy. Patients with a history of preoperative neoadjuvant radiation, in whom there is an increased expectation of inflammation and fibrosis of the mediastinal structures, likewise do well with this surgery. The procedure is preferred for malignant disease because it ensures excellent circumferential visualization and dissection.

Before the patient is considered for resection, diagnostic studies include esophagogastroduodenoscopy to evaluate the extent of proximal and distal disease along with endoscopic ultrasound and a PET/CT scan to complete clinical staging and rule out distant metastases. The majority of patients with stage II or III disease are considered for neoadjuvant therapy. It is important to restage patients following neoadjuvant treatment with CT scan or PET/CT to identify those patients who may have progressed on therapy.

All patients are screened carefully for cardiopulmonary reserve. Patients identified as high risk on the basis of cardiopulmonary screening may undergo additional optimization procedures such as cardiac revascularization, valve repair or replacement, smoking cessation, or cardiopulmonary rehabilitation.

Our preference is to use the stomach for reconstruction for its ease of use, need for only one anastomosis, and reliable blood supply. For patients who have had previous abdominal surgery, specifically gastric resections that might compromise the vascular supply of potential conduits, we routinely obtain preoperative angiograms to evaluate the vascular anatomy.

Forty-eight hours before surgery, all patients receive a course of oral antibiotics and mechanical bowel cleanout. An epidural catheter is placed for postoperative analgesia to reduce pulmonary complications secondary to pain. Preinduction intravenous antibiotics are administered prophylactically.

Stage I: Thoracic Dissection

The patient is induced with general anesthesia and intubated with a double-lumen tube to allow for single left lung ventilation. (For a detailed description of anesthetic technique, see Chapter 5.) For those patients with upper or middle third tumors, we first perform a bronchoscopy through a single-lumen endotracheal tube to assess the posterior membranous wall of the airway for tumor invasion.

The patient is turned to the left lateral decubitus position. A limited right posterolateral thoracotomy incision is made in the fifth interspace, sparing the serratus anterior muscle (Fig. 17-1). The fifth interspace is opened, and the sixth rib is shingled to permit better access to the thoracic cavity (Fig. 17-2). The ribs were spread using gentle retraction.

The lung is retracted anteriorly and the inferior pulmonary ligament is divided. The posterior mediastinal pleura is opened from the apex of the chest to the diaphragm at the level of the vertebral bodies thereby exposing the esophagus (Fig. 17-3). The esophagus is then mobilized in a region above the tumor. A 1-cm Penrose drain is passed around the esophagus and used for gentle retraction during the remainder of the thoracic dissection. Retracting the esophagus in this manner permits evaluation of the tumor for resectability from its surrounding structures. The azygos vein is usually divided using a 30-mm endovascular stapler to improve access to the upper thoracic esophagus (Fig. 17-4). If the tumor is deemed to be resectable, the surgeon proceeds with near-total esophagectomy, carrying the dissection cephalad along the esophagus toward the apex of the chest using a combination of electrocautery and blunt dissection with constant traction from the Penrose drain, and countertraction provided by the first assistant's sponge stick. For mid- and distal esophageal tumors, the dissection of the upper thoracic esophagus proceeds close to the esophagus to avoid injury to the right laryngeal nerve, which recurs around the subclavian artery. Finger dissection is used to define the plane between the trachea and the esophagus at the level of the thoracic inlet, and the finger dissection is carried up to the level of the clavicle (Fig. 17-5).

After packing the apex of the chest with a laparotomy sponge to minimize bleeding, the dissection proceeds caudad between the aorta and esophagus, where the arterial branches are divided. A second Penrose drain can be placed around the lower esophagus, distal to the tumor if possible, to provide countertraction for the posterior dissection. Any pericardium that adheres to the tumor is removed as well as adherent pleura along both sides of the mediastinum. A small rim of diaphragm is incised circumferentially around the esophageal hiatus. The peritoneal cavity is entered posteriorly, and the posterior wall of the stomach is palpated by the surgeon's finger. In particular, when the lesion is at the carina and densely adherent, using the two Penrose drains above and below the lesion allows safe access to the most densely adherent level where the tumor abuts the posterior wall of the airway and anterior wall of the aorta.

At this point, the first upper Penrose drain is loosely knotted around the esophagus and pushed up into the left neck just beneath the omohyoid muscle, where it can be retrieved later during the cervical dissection (Fig. 17-6). By encircling the midesophagus well below the recurrent nerves, the drain will be inside the nerves when it is retrieved in the neck, minimizing traction or direct injury to the recurrent nerve. The second Penrose drain is loosely knotted around the lower esophagus and passed into the peritoneal cavity to be retrieved at the time of the laparotomy to facilitate dissection of the gastroesophageal junction (Fig. 17-7). Although the goal is to resect the nodal tissue en bloc with the esophagus, any nodal tissue that has not been dissected with the specimen is resected separately and labeled appropriately. The region of the thoracic duct is identified near the aortic hiatus and ligated with a 0 silk suture to prevent chyle leak. If the duct cannot be visualized easily, a mass ligature is placed around all of the tissue between the spine and the aorta at the level of the diaphragm. Hemostasis is achieved, and a straight 28 French chest tube is placed in the posterior chest to the apex and brought out through a separate inferior stab incision. The thoracotomy is closed in layers in typical fashion after reapproximating the ribs with interrupted suture.

Stage II: Abdominal and Cervical Dissections

The patient is repositioned supine for the abdominal and left cervical dissections. At this juncture, the double-lumen tube is replaced with a single-lumen tube to avoid the need to replace the endotracheal tube after the conclusion of the case once the cervical anastomosis has been created and airway edema is at its worst. If dissection around the trachea or carina was difficult due to radiation fibrosis or tumor, a bronchoscopy can be performed at this junction to ensure no injury to the airway has occurred. The patient's head is rotated 45 degrees to the right, and a shoulder roll is placed. The patient is prepped from the jaw to the pubic symphysis. An upper midline laparotomy and left cervical incisions can be performed simultaneously (Fig. 17-8).

Abdominal Dissection

The abdomen is explored for resectability. With the availability of improved CT and PET/CT technology for preoperative surgical staging, it is unlikely at this stage to find any evidence of metastatic disease. In the event that metastatic disease is identified, the patient can be safely closed after removing the Penrose drains and inserting a feeding tube. The esophagus has a rich longitudinal submucosal blood supply and will continue to survive. As patients with stage IV esophageal cancer have a short median survival, palliative esophagectomy may not be the best choice for a quick recovery and discharge from the hospital. Palliation of dysphagia from an obstructing tumor can often be achieved endoscopically at a later date if necessary.

If no evidence of metastatic disease is found, the triangular ligament to the left lobe of the liver is divided and the left lobe is folded down and retracted to the right with a moist laparotomy pad and a deep self-retaining retractor. We use upper-hand and Balfour retractors to provide exposure after taking down the triangular ligament. The Penrose drain placed during thoracotomy is identified and used for retracting the esophagus at the level of the gastroesophageal junction (Fig. 17-9). Adequate pulse is confirmed in the right gastroepiploic artery, after which the surgeon proceeds to locate and divide the short gastric vessels. If the spleen is located deep in the left upper quadrant such that it limits visualization of the gastric vessels, a laparotomy pad can be placed behind the spleen to bring the short gastric vessels into view. Once the short gastric vessels are identified, they can be transected with ties and clips, harmonic scalpel, or endovascular linear staplers (Fig. 17-10). With the short gastric arteries divided to the level of the hiatus, dissection is carried along the greater curvature toward the pylorus, dividing the omentum from the stomach, taking care to avoid injury to the gastroepiploic arcade and pedicle. The lesser sac is entered and the posterior attachments of the stomach to the pancreas are sharply divided. A generous Kocher maneuver is carried out to mobilize the duodenum to the midline. A pyloromyotomy or Heineke-Mikulicz type of pyloroplasty using a single layer of 3-0 silk is created to provide adequate drainage of the conduit (Fig. 17-11).

The stomach is reflected superiorly and to the right to expose the left gastric artery and vein from within the lesser sac. All nodal tissue around this vascular pedicle is gathered up onto the specimen. The left gastric pedicle is palpated at its takeoff from the celiac axis and ligated with a single firing of the endovascular 30-mm linear stapler. Before firing the stapler, it is important to recheck the pulse of the right gastroepiploic pedicle to be sure that the celiac axis itself has not been clamped (Fig. 17-12). The lesser omentum is divided and the gastric conduit is now ready to be divided.

Left Cervical Dissection

A left cervical incision can be performed simultaneously with the upper midline laparotomy by a separate surgical team. A left neck incision is preferred as the path of the left recurrent nerve is more predictable and less likely to be injured during dissection. A short left neck incision is created along the anterior border of the sternocleidomastoid muscle (Fig. 17-13). The sternocleidomastoid muscle is mobilized laterally along with the carotid sheath. Dissection is deepened lateral to the thyroid gland. The middle thyroid vein may need to be divided. Care is taken not to impinge the left recurrent nerve with retractors. The use of self-retaining metal retractors should be avoided to prevent recurrent laryngeal nerve injury and carotid artery lesions, particularly if carotid plaques are suspected. The omohyoid and sternohyoid muscles may be divided with electrocautery for improved esophageal exposure. Using gentle blunt finger dissection, the surgeon proceeds posterior to the cervical esophagus and anterior to the vertebral bodies where the upper Penrose drain placed during the thoracic dissection can be found. The drain is brought into the wound and traction from the Penrose drain permits further blunt mobilization of the cervical esophagus. The entirety of the esophagus should now be mobile.

The cervical esophagus is divided with a linear 75-mm stapler (Fig. 17-14). A long #1 silk suture is placed in the distal esophageal staple line, and the specimen is retrieved from the abdomen. In this manner, the silk tie, which is pulled down into the mediastinum with the specimen, can later be used to guide the gastric conduit up through the posterior mediastinum into the neck (Fig. 17-15).

With the specimen delivered into the abdomen, a linear cutter 75-mm stapler is used to divide the stomach to ensure an adequate distal margin from the tumor and to fashion a narrow tube-shaped conduit. The outline for the conduit begins along the greater curvature of the stomach, high on the fundus, and is drawn toward the lesser curvature just above the crow's foot (Fig. 17-16). The staple line along the gastric conduit can be reinforced with invaginating “Lembert” seromuscular sutures. Maintaining a narrow conduit is important physiologically to ensure adequate emptying of the neoesophagus. The hiatus is dilated manually to permit four fingers to be placed through it.

A sterile arthroscopic camera bag is attached to the proximal end of a 30-mL Foley catheter secured to the distal end of the silk tie (Fig. 17-17). The gastric conduit is placed inside the bag and the bag is unfolded. A small aliquot of saline is added inside the bag and suction is applied to the distal end of the Foley drain to maintain traction on the conduit. The Foley catheter, camera bag, and gastric conduit are gently pushed into the mediastinum and out the left cervical incision taking care to prevent twisting of the conduit (Fig. 17-18). The conduit should be gently pushed or fed up the mediastinum rather than pulled up to prevent injury to the walls of the conduit or the vascular pedicle. When oriented properly, the gastric staple line lies on the right side of the neck incision from the patient's perspective, and the pylorus rests at the hiatus (Fig. 17-19). The esophagogastric anastomosis can be performed in one of two ways: hand sewn or stapled. For a hand-sewn anastomosis, the proximal esophageal staple line is cut off and a gastrotomy is made 3 cm below the tip of the conduit. A single layer of interrupted 3-0 silk sutures is used to create the anastomosis (Fig. 17-20). For a stapled anastomosis, a functional end-to-end anatomic side-to-side anastomosis is created using a linear cutting stapler and a thoracoabdominal-30 (TA-30) stapler to close the enterotomies (Fig. 17-21).

We routinely drain the gastric conduit with a nasogastric tube until resolution of the postoperative ileus to prevent conduit distention and potential ischemia or aspiration. The nasogastric tube can be passed transnasally across the anastomosis, or alternatively a nasogastric tube can be passed through the conduit and out the neck incision. This latter placement technique avoids the morbidity and nasopharyngeal discomfort of a traditionally placed nasogastric tube. A sterile (Levine) tube is brought onto the sterile field and passed through a gastrostomy placed near the tip of the conduit prior to completion of the anastomosis. A purse-string suture is placed around the gastrostomy to prevent leakage. The tube is brought out at the apex of the neck incision and secured to the skin.

A 10-mm Jackson-Pratt closed suction drain is passed posteriorly and to the left of the anastomosis at the level of the thoracic inlet and brought out through a small lateral stab incision. This tube prevents seroma and provides an outlet for drainage in the event of an early leak in the anastomosis. A jejunal feeding tube is inserted routinely for postoperative feeding and to provide access for enteral nutrition if problems with oral feeding occur postoperatively.

Procedure-Specific Morbidity

Morbidity following esophagectomy is common, most frequently from cardiopulmonary and anastomotic complications (Table 17-3). Thorough knowledge of the common sources of morbidity and mortality following esophagectomy can facilitate prevention, early detection, and rapid treatment of complications, which is essential for satisfactory outcome.

Cardiopulmonary Complications

Many esophagectomy patients are ultimately, often malnourished individuals and frequently have a history of smoking and alcohol use. Often, they have comorbid conditions that compromise their cardiovascular and pulmonary status, prolong recovery, and complicate the postoperative management. Pulmonary complications including pneumonia, aspiration, and respiratory failure requiring prolonged intubation are common after esophagectomy and occur at a rate of 20% to 30% at high-volume centers.¹⁰ A preoperative epidural catheter for pain control is critical to improve postoperative pulmonary toilet. Conversely, the incidence of cardiovascular complications is relatively low, occurring in 5% to 10% of patients in most large series. Atrial fibrillation is most common but myocardial infarction, arrhythmias, congestive heart failure, deep venous thrombosis, and pulmonary embolism can occur as well.¹⁰

Anastomotic Leak

Anastomotic leak remains the Achilles heal of esophageal surgery. Most leaks manifest within 10 days of surgery. General factors that influence the development of anastomotic leak include tension on the anastomosis, quality of the arterial and venous blood supplies, location of the anastomosis, manner in which it was performed, and surgeon experience. Anastomotic leaks that are not quickly identified and treated remain a major source of operative mortality. We prefer a cervical as opposed to intrathoracic anastomosis, as in our experience it is easier to treat a leak in the neck than one in the chest. Early initiation of antimicrobial therapy, opening of the neck wound, and making the patient NPO is usually all that is necessary to resolve the leak and prevent severe sepsis. Soilage into the mediastinum is uncommon. Conversely, intrathoracic leaks may necessitate reoperation to adequately drain the source of the mediastinal sepsis. Recently, some have advocated the use of endoluminal stents to seal leaks.

Hemorrhage

There are many potential sources for hemorrhage after esophagectomy, including unrecognized or poorly controlled injury to the spleen, azygos vein, intercostal vessels, omentum, right gastric artery, and lung parenchyma. Traction injuries of the heart and pericardium can lead to cardiac tamponade. Injury to the phrenic veins during mobilization of the left lateral segment of the liver extending to the vena cava also can give rise to internal bleeding. Patients with unsuspected cirrhosis can have bleeding of the esophageal varices intraoperatively. Prevention of intraoperative bleeding requires close attention to technique and vigilant examination of all potential bleeding sites before closure. Postoperative hemorrhage requires urgent reexploration and occurs with an incidence of 3% to 5%. Diagnosis of postoperative bleeding is usually delayed by 12 to 24 hours. Unexpected tachycardia and decreased urine output are early signs of a developing problem. Since esophagectomy patients have sizable fields of dissection, where the blood can hide, they generally require large-volume blood replacement. After patients are resuscitated with blood products to correct coagulopathies, they are reexplored. This source of bleeding usually can be prevented with meticulous surgical technique.

Chylothorax

The thoracic duct follows a similar course to the esophagus, comes in close proximity to the aorta and vertebral bodies, and is at risk of being injured during esophagectomy. Chylothorax occurs with an incidence of 1% to 5%. Diagnosis is made on demonstration of a pleural effusion consisting of a milky white fluid with high triglyceride and lymphocyte counts. It should be suspected with the development of a new right pleural effusion on chest radiographs following early removal of the chest drains or if the chest tube output remains elevated beyond postoperative day 4. The fluid may be clear and have a low triglyceride level if the patient has been NPO for a few days and may not turn milky until enteral feeds have been initiated. Although chylothorax can be managed conservatively in some patients with parenteral nutrition and restriction of enteral intake, the course is frequently prolonged and may lead to significant protein loss. We favor an aggressive reoperative approach with mass suture ligation of the thoracic duct via right thoracotomy if high chest tube outputs persist beyond the seventh postoperative day. To avoid this complication, we routinely ligate the thoracic duct at time of esophagectomy.

Pleural Effusion and Pneumothoraces

Other possible complications of esophagectomy include pleural effusion and pneumothorax. These conditions can be managed conservatively with percutaneous drainage or thoracostomy after other causes have been eliminated, including hemorrhage, chylothorax, conduit leak, metastatic disease, and airway injury. Dissection through the left pleura may result in fluid or air originating in the right hemithorax communicating with the left pleural space.

Recurrent Laryngeal Nerve Injury

A serious complication of esophagectomy is recurrent laryngeal nerve palsy. This injury affects the vocal cords and phonation but more importantly impacts the ability of the patient to detect and protect their airways against life-threatening aspirations. It occurs with an incidence of 10% to 20% in patients receiving a cervical anastomosis.⁷ Care must be taken in patients receiving oral nutrition with a recurrent nerve palsy to avoid aspiration. We frequently pursue early medialization of the vocal cord if a recurrent nerve palsy is identified.

Airway Injuries

Rarely, a tracheobronchial injury arises intraoperatively. If undetected at surgery, it can result in a postoperative tracheogastric fistula with persistent pulmonary soiling and recurrent pneumonias. We routinely perform bronchoscopy after the thoracic dissection to look for airway injuries. The risk of injury to the membranous wall of the trachea is minimized when the dissection is carried out under direct vision during the thoracic dissection, which is not possible during a transhiatal approach. If an airway injury does occur, it can be repaired primarily and buttressed with pericardium, omentum, and/or transposed muscle.

Delayed Gastric Emptying

Up to 10% of patients undergoing esophagectomy experience delayed gastric emptying in the postoperative period. We routinely perform a pyloromyotomy for all patients undergoing a three-hole esophagectomy to avoid this disabling complication. If a gastric drainage procedure is not added, delayed gastric emptying can often be managed with endoscopic balloon dilatation but the surgeon must be vigilant toward the early detection of retained gastric juices and oral intake to avoid life-threatening aspiration.

Late Sequelae

It is important for the surgeon to educate the patient and family to recognize some of the late complications that can occur following esophagectomy that may warrant intervention. These include anastomotic stricture, paraesophageal hernia, intestinal motility problems (e.g., dumping syndrome), bile reflux, and post-thoracotomy pain syndrome.

Esophageal Anastomotic Stricture

Tension and inadequate blood supply can lead to esophageal stricture weeks to months after surgery. Patients who develop an anastomotic leak are at high risk for later development of a stricture. Dysphagia is the first sign of an esophageal stricture, and patients should be evaluated with an upper endoscopy and/or barium swallow. We have a low threshold for early endoscopy and dilatation. Anastomotic stricture is a frequent problem for a cervical anastomosis although serial dilatation is very effective and typically resolves the problem without the need for reoperation.

The mortality rate for esophagectomy is proportional to experience. Mortality ranges from a high of 10% at low-volume centers to a low of 2% to 3% at high-volume centers. Attention to all aspects of the procedure includes careful patient selection, meticulous surgical technique, and diligent perioperative care.^9,10 A high suspicion for procedure-specific complications yields a safe procedure with acceptable morbidity and mortality when the surgery is performed by an experienced surgical team (Table 17-4). Highlights of the most important technical aspects of this approach include use of a muscle-sparing right posterolateral thoracotomy, direct vision for the thoracic dissection, complete thoracic lymphadenectomy (which yields the best chance for cure and guidance for adjuvant treatment regimens), and clear margins. Placing the anastomosis in the left neck provides easy postoperative maintenance, reduces the morbidity of anastomotic leaks in comparison with an intrathoracic anastomosis, and is associated with a lower incidence of postoperative bile reflux. Survival data have not revealed a clear benefit of one surgery over another in a comparison of the transhiatal and transthoracic techniques. The technical complications are fewer when thoracic esophageal dissection is performed under direct vision rather than with blunt dissection. This is especially the case after caustic injuries and neoadjuvant radiation therapy. However, several recent randomized studies have demonstrated a trend toward improved survival with the transthoracic approach.¹¹

The technical details of the “three-hole approach” are clearly described in this chapter. Although this is the favored route of the “Brigham group” it has been abandoned by those performing MIE and others in favor of the standard Ivor Lewis approach. There is no doubt that the three-hole approach allows the best access to all of the lymph node fields one might consider removing. Likewise, if one were to do the three-field approach, the technique described above is well thought out and meticulous in attention to detail and will yield excellent results. The key unanswered issue remains whether there is any benefit to the residual esophagus after esophagectomy. If there is a perceived benefit to having a longer, functional remnant, an Ivor Lewis should be preferred for most lesions of the distal esophagus and esophagogastric junction. On the other hand, this modification is my operation of choice for patients with squamous cell carcinoma as these are generally of the midesophagus and total esophagectomy with neck anastomosis is the preferred option.

The authors wish to acknowledge Luis Argote-Greene, MD, for his contributions to this chapter in the first edition.