18: Ivor Lewis Esophagectomy

For surgeons familiar with the unique and extraordinary challenges presented by surgery of esophageal malignancy, the words of Ivor Lewis appear as valid today as they were when first written over 50 years ago: “There is little doubt that the successful outcome of radical curative surgery for esophageal carcinoma remains one of the great challenges of surgical practice.”¹ A satisfactory result necessitates optimization of the patient's physical state and tumor staging, a high degree of surgical skill and experience, and teamwork involving close coordination of the surgical, anesthetic, physiotherapeutic, and nursing modalities of treatment.

The procedure first described in 1946 by Ivor Lewis now represents the middle road between “minimal” transhiatal esophagectomy without radical lymph node dissection, as described by Orringer et al.,² and extensive radical resection combined with three-field lymphadenectomy, as described by Akiyama et al.³ The operation combines an extended resection of the esophagus with either standard or extensive thoracic and abdominal lymph node dissection under direct vision through a combined abdominal and thoracic approach. For this reason, the Ivor Lewis esophagectomy is a preferred approach in many centers for patients with resectable tumor of the middle to lower third of the esophagus and gastroesophageal junction.

The procedure has several drawbacks that, in our view, confine its use to a select group of patients. The operation may limit the proximal extent of the esophageal resection, which can be a major concern in the case of skip lesions or tumors that spread through the submucosa. By terminating the dissection at the apex of the chest, one may not appreciate the presence of positive lymph nodes in the neck or reap the potential benefits of a third-field lymphadenectomy. Indeed from our own experience in a series of 174 patients with three-field lymphadenectomy,⁴ we observed that 23% of patients with adenocarcinoma (distal third or gastroesophageal junction) and 25% with squamous cell carcinoma presented with positive cervical lymph nodes. Unforeseen changes in the TNM classification because of such lymph node involvement were observed in 12% of patients. Five-year survival in patients with middle-third esophageal squamous cell carcinoma was 27.7%, and 4- and 5-year survival in patients with distal-third adenocarcinoma was 35.7% and 11.9%, respectively. Finally, the intrathoracic anastomosis, as compared with the cervical anastomosis, is thought to be associated with a higher risk of life-threatening sepsis in the event of leak. For these reasons, we reserve the Ivor Lewis technique for patients with resectable tumors in whom a neck anastomosis is contraindicated. This category includes patients with a past history of cervical malignancy that has been treated by either radical radiotherapy or major surgery and patients with other contraindications to surgery in the cervical region.

The preoperative evaluation should establish the histologic diagnosis and extent of local and distant disease, as well as the patient's physiologic status, which should be improved preoperatively if necessary. Esophagoscopy should be performed to obtain tissue diagnosis and to document the precise location of the tumor and the presence of associated findings (e.g., Barrett esophagus). A bronchoscopy is mandatory in all proximal- and middle-third tumors to evaluate airway invasion or a synchronous second primary. Endoscopic ultrasound has been established as key to evaluating the depth of tumor penetration and involvement of regional lymph nodes. Endoscopic ultrasound also offers the possibility of fine-needle aspiration biopsy for suspicious lymph nodes, especially nodes of the celiac trunk.

Barium swallow is used to document the location and extent of the lesion. CT scan of the chest and abdomen is also obtained routinely, although CT is not as effective as endoscopic ultrasound for determining the extent of intra- and transmural penetration or nodal involvement. CT is more valuable for assessing tumor extension into adjacent structures, such as the aorta, and for the detection of visceral and occult metastasis, especially in combination with a PET scan.

The role of thoracoscopy and laparoscopy in the evaluation of tumor resectability, staging of local and distant lymph nodes, identification of peritoneal implants, and detection of liver or lung metastasis is less clear mainly because of the expense, technical difficulty, and time associated with these procedures.

Careful preoperative assessment of pulmonary and cardiovascular function is mandatory. Routine investigations also include a full blood count, urea and electrolytes, liver function tests, and tumor markers. Physiotherapy is instituted to improve the patient's mobility and pulmonary function, as well as to enhance the patient's general condition. Adequate levels of nutrition and hydration also must be ensured. If necessary, the patient should be begun on nutritional supplements or total parenteral nutrition.

Anesthesia

The anesthetic technique must be of the highest standard. All patients undergoing the Ivor Lewis procedure should have an epidural catheter placed whenever possible to obtain satisfactory levels of analgesia postoperatively, thereby facilitating physiotherapy and respiratory function. A double-lumen endotracheal tube permits single-lung ventilation, which is required to obtain proper visualization and radical resection of the area concerned. Arterial and central venous pressure lines are inserted. Urinary output should be monitored with a Foley catheter. A gastric tube is placed to ensure adequate drainage during the procedure. The patient is positioned with the aid of a vacuum beanbag during thoracotomy. Twenty-four-hour antibiotic prophylaxis is instituted before incision.

Surgical Management

The Ivor Lewis esophagectomy is a two-stage procedure consisting of laparotomy for gastric mobilization and tubularization, followed by a right thoracotomy for esophageal resection and reconstruction. A radical lymphadenectomy is performed in the upper abdomen and chest. During the procedure, careful dissection is mandatory to avoid bleeding, limit the need for transfusion, and minimize manipulation of the heart.

Abdominal Dissection

The patient is positioned in a supine manner for laparotomy, and an upper midline incision is performed. Full abdominal exploration ensues with special attention to evidence of tumor dissemination in the form of unforeseen peritoneal or serosal implants, liver metastasis, or both. An abdominal self-retaining retractor is useful. The left lobe of the liver can be retracted cephalad and to the right after dividing the triangular ligament.

The dissection of the stomach starts by entering the lesser sac at a point well away from the gastroepiploic artery. The greater omentum is divided along the greater curvature by ligating and transecting the branches of the gastroepiploic arteries to the epiploon. During this maneuver, great care is taken to protect the gastroepiploic vessels needed for future vascularization of the stomach. The short gastric vessels are ligated sequentially and divided as close to the spleen as possible to avoid interrupting the epiploic arcade, thus preserving the circulation to the gastric fundus. Injury to the fundus of the stomach is assiduously avoided because this will serve as the site of the future anastomosis. While dissecting the gastrocolic omentum toward the duodenum, the stomach is lifted upward to allow the various adhesions between the stomach and pancreas down to the posterior surface of the first part of the duodenum to be transected. At this point in the operation the right gastroepiploic artery origin or venous communicating branch to the mesocolon is most vulnerable to injury. The duodenum is mobilized generously with a Kocher maneuver, and any loose adhesions between the duodenum and gallbladder fundus are divided.

Attention is turned to the lesser omentum, which is divided close to the undersurface of the left liver lobe up to the esophageal hiatus. The vagal branches to the liver are transected, and if a left liver lobe artery is found, care is taken to preserve this artery if at all possible. The right gastric vessels are identified, dissected, ligated sequentially, and divided approximately 1 inch proximal to the pylorus. The stomach is lifted up by the assistant, bringing into the surgeon's view a bundle of tissue connecting the lesser curvature to the posterior abdominal wall (i.e., the celiac trunk). Palpation confirms pulsation of the left gastric artery within this tissue. Careful dissection permits the artery and vein to be visualized individually and tied off. The surrounding fat and lymph nodes are also removed during this maneuver. The left gastric artery is divided and ligated close to its origin from the celiac axis. The remaining loose adherent tissue, which contains a few small vessels, is divided, bringing the crura of the diaphragm into view. Gentle posterior pressure between the two pillars permits access to the posterior mediastinum, where loose areolar tissue can be broken down with gentle dissection. The phrenoesophageal ligament is transected around the esophagus to complete the mobilization. During this procedure, a cuff of diaphragmatic muscle can be resected if diaphragmatic invasion is suspected. After opening the diaphragmatic hiatus, access is gained to the fibrofatty and lymphatic tissue that separates the esophagus from the pericardium. This fibrofatty and lymphatic tissue is reflected away from the surrounding structures. In this way, much of the dissection of the lower esophagus can be achieved through the abdomen under direct vision. The gastric tubularization is performed using several linear staplers, starting from the gastric fundus down to the place on the small curvature where the right gastric artery has been ligated. The staple line is placed such that it leaves a gastric tube of 4 to 5 cm in width (Fig. 18-1). The staple line is oversewn in a running fashion, although some surgeons prefer to use interrupted sutures. Thus, by resecting the lesser curvature, all lymphatic tissue in this area is removed. A lymph node dissection along the splenic artery, common hepatic artery, and celiac axis is performed. This also can be done en bloc with the dissection of the left gastric artery. The gastric tube is fixed to this separated lesser curvature by using two stay sutures.

At the end of the first stage of the procedure, it should be possible to place the pylorus at the hiatus, ensuring sufficient length for the reconstruction. Pyloroplasty is not carried out, but digitoclasy of the pylorus may be useful. The abdomen is closed.

Thoracic Dissection

A lateral thoracotomy (which can be extended anteriorly or posteriorly depending on the surgeon's preference) is performed through the fifth interspace. The serratus muscle is spared if possible.

The right lung is selectively deflated and retracted anteriorly. First, the azygos vein is dissected, ligated, and transected, as well as the underlying intercostobronchial artery. The mediastinal pleura anterior to the esophagus is opened widely from the azygos vein to the top of the chest. The proximal esophagus is dissected circumferentially and looped with an umbilical tape. The dissection is carried cephalad toward the apex of the chest, separating the esophagus from its tracheal and prevertebral attachments using the tape for traction and countertraction. Great care is taken to avoid injury to the membranous part of the trachea.

Similar dissection of the esophagus is achieved by encircling it with a tape distally from the distal pole of the tumor. During this dissection, it is important to remove the esophagus en bloc along with the surrounding tissues, including the thoracic duct and azygos vein, to achieve radical resection, especially if transmural extension is suspected. Dissection of the esophagus proceeds inferiorly, encompassing all tissue between the aorta and pericardium, including all periesophageal and subcarinal nodes. Both vagal nerves are transected.

A further lymph node dissection is performed along the left and right paratracheal spaces, along the aortopulmonary window, and along the right recurrent nerve at the level of the brachiocephalic trunk. To facilitate exposure of the right recurrent nerve, slight traction is exerted on the right vagus nerve, slightly stretching the recurrent nerve. Avoiding electrocautery is mandatory in this region to avoid injury to the nerve. Similarly, the left recurrent nerve is identified, and careful lymph node clearance is performed.

At this point, the gastric tube can be pulled up into the chest cavity, being careful to avoid axial rotation of the tube during this process (Fig. 18-2). A suitable point at least 5 cm above the tumor is chosen for transecting the esophagus. After transection, a frozen section must be obtained of the proximal resection margin to confirm the absence of tumor extension in the suture line.

Anastomosis

A number of techniques have been described for esophagogastrostomy, including use of a circular stapler or hand-sewn anastomosis.

Stapled Anastomosis

For a mechanical anastomosis, the esophagus is transected, and a purse-string suture with, for example, Prolene 4-0 running suture, is placed through the mucosa and muscular layer. The anvil head of the circular stapler (size at least 25) is placed into the esophagus, and the purse-string suture is tied snugly around the shaft of the anvil head. An incision is made at the top of the gastric tube to insert the gun of the circular stapler. The site where the gun will perforate the gastric wall is chosen carefully on the posterior aspect of the gastric tube, away from previous staple lines and the greater curvature vessels. One also must verify that once the anastomosis is performed, it will not be under tension because this can lead to postoperative complications. After penetrating the gastric wall, the pointed shaft of the gun is detached, and the gun is connected to the anvil head. The gun then is fired in the customary manner, and the doughnuts are inspected to ensure the integrity and completeness of the anastomosis. Several nonabsorbable stitches can be placed between the muscular layer of the esophagus and the seromuscular lining of the stomach to strengthen and protect the anastomosis. The nasogastric tube then is advanced through the anastomosis into the gastric tube. The redundant part of the gastric tube including the opening used to insert the gun is then transected with a linear stapler, and the staple line is inverted with a running suture.

Hand-Sewn Anastomosis

For a hand-crafted anastomosis (Fig. 18-3), the posterior seromuscular aspect of the anastomosis is performed using separated nonabsorbable suture, for example, Ticron 3-0 stitches. The esophagus and gastric tubes then are incised along this suture line using electrocautery. The posterior layer comprising the full thickness of both the esophagus and gastric wall then is performed with separated absorbable suture, for example, Maxon 3-0 stitches. The gastric tube is advanced across the anastomosis. The anterior part of the esophageal wall is transected. The anastomosis is finalized using separated absorbable suture, for example, Maxon 3-0 for the anterior layer, and separated nonabsorbable suture, for example, Ticron 3-0 for the outer seromuscular layer. Some authors use a running suture, whereas others prefer a single-layer anastomosis.

In most cases we use a pleural flap to cover the anastomosis to protect the chest cavity from anastomotic leakage. The thoracic cavity is usually drained using a 36F chest drain placed in the paraspinous position. The chest wall is closed in layers.

To optimize the results of surgery, this procedure should be performed at an appropriately equipped high-volume center with meticulous management of the postoperative course by an experienced staff. A chest radiograph is obtained in the OR to confirm complete lung expansion and appropriate placement of chest drains. Most patients can be extubated immediately or a few hours after surgery. Good epidural analgesia enables the patient to sit upright in bed, breathe deeply, and cooperate fully with physiotherapy. If necessary, bronchoscopy or eventually a minitracheostomy either at the time of surgery or sometime thereafter to ensure enhanced bronchial cleaning can be performed.

Fluid balance and oxygen saturation should be closely monitored, and oxygen supplementation is mandatory. Fluid restriction is used to avoid cardiac and respiratory complications, especially in patients having neoadjuvant therapy. It is also vital to maintain adequate and balanced nutrition during the early postoperative period because many of these patients have suffered significant weight loss and are malnourished. Total parenteral nutrition is preferred.

Thrombosis prophylaxis is continued by subcutaneous low–molecular-weight heparin injections and prophylactic antibiotics given for 2 days.

Since it is essential to avoid intragastric stasis in the stomach tube, the nasogastric tube is kept in place to prevent respiratory complications secondary to aspiration.

On day 5, a contrast study is performed to evaluate the integrity of the anastomosis. If no leak is visualized, oral feeding is started. On the same day, the epidural catheter is removed, and the patient is encouraged to mobilize fully. Oral pain therapy can be started. The chest drain will be removed when the effluent amounts to less than 200 mL of fluid.

Patients are discharged when they are able to tolerate a soft diet and the pain is sufficiently controlled to permit normal mobilization. The patient is seen in the outpatient clinic 1 month after discharge, and based on the patient's general condition, further follow-up is arranged. After 1 year, the follow-up interval is every 6 months, and a clinical examination is routinely completed with CT chest abdomen and biochemistry.

Atelectasis and Respiratory Complications

Atelectasis and other respiratory problems are very common after transthoracic esophagectomy. Good analgesia, physiotherapy, adequate hydration (i.e., avoiding overhydration of the lungs), and early mobilization are key to minimizing these respiratory complications.

Anastomotic Leak

Anastomotic leaks may occur in the early postoperative period (2–3 days) owing to a technical failure. Leaks also can occur later (3–7 days) and are thought to be due to ischemic changes in the stomach, usually at the suture line and occasionally as a result of necrosis of the proximal end of the gastric tube. A subclinical leak detected on a contrast study usually heals without specific treatment. In case of minor leaks conservative treatment (i.e., nil by mouth, antibiotics, total parenteral nutrition, jejunostomy feeding, proton pump inhibitors, nasogastric tube, and possibly octreotide) will suffice. Early endoscopy is useful for determining the viability of the gastric tube and for evaluating a leak. Early dilation, if needed, is mandatory to allow free passage of saliva. Larger leaks in the chest that remain contained are treated the same way but will require adequate drainage of all collections through a pigtail catheter or chest tube, preferably placed under CT guidance for optimal positioning. Reintervention is necessary occasionally to control sepsis, in particular in the presence of diffuse intrathoracic collections. In the event of endoscopically documented gastric tube necrosis, immediate reintervention with resection of the necrotic stomach and diverting esophagostomy is the safest option. Placement of a jejunostomy tube for feeding is mandatory, if not already performed at the time of the esophagectomy. Reconstruction will be planned after 3 to 6 months, usually with a retrosternal colon.

Anastomotic Stricture

In many reports, at least a third of patients develop a stricture at the anastomosis. Dilation of the stricture can be accomplished by several means. The preferred method is endoscopic dilation with Savary dilators. The success rate, eventually, after several dilations, is high (>80%). When dealing with a more resistant stricture, balloon dilation and local steroid injection usually resolve the problem. The need for reintervention is extremely rare.

Delayed Gastric Emptying

Causes of delayed gastric emptying include lack of a pyloric drainage procedure when the whole stomach or wide gastric tubes are used, obstruction at a severely narrowed passage through the hiatus, and a redundant intrathoracic stomach resulting in kinking, axial twisting, or both. This infrequent but sometimes very bothersome complication is best tackled by endoscopic balloon dilation of the pylorus along with prokinetic agents (e.g., metoclopramide or erythromycin). If conservative management fails, reoperation with an adequate drainage procedure or repositioning of the gastric tube may become necessary.

Reflux

Reflux is a common problem after gastric pull-up, especially with an intrathoracic anastomosis. The level of severity seems to vary with the location of the anastomosis, with those above the azygos vein having a lower incidence than those below this level.⁵ Small, frequent feedings, avoidance of liquids with meals, avoidance of the supine position after meals, and elevation of the patient's head while lying in bed are helpful in remediating these symptoms. Acid reflux is best treated with proton pump inhibitors to avoid the higher risk of anastomotic stricture formation through the caustic effect of the acid on the anastomosis. Intestinal metaplasia may develop in the remaining proximal esophagus as a result of mixed acid and biliary reflux. Therefore, regular endoscopic surveillance during follow-up is mandatory.

Modern-day results of the Ivor Lewis procedure have shown that the technique can be performed safely with a low morbidity and mortality (Table 18-1). Survival after Ivor Lewis esophagectomy for cancer of the esophagus has been described in several studies.^6-10 Visbal et al.⁷ in their series of 220 consecutive patients had an overall 5-year survival of 25.2% (squamous cell and adenocarcinoma). In a series of 264 Ivor Lewis resections for squamous cell carcinoma of the esophagus, Lozac'h et al.¹¹ reported an overall survival of 33.3%. Survival was stage-dependent in both the series. Stage I was 94.4% and 53.2%, respectively; stage IIa was 36.0% and 38.8%, respectively; stage IIb in the first series was 14.3%, and stage III was 10% and 13.4%, respectively. In these two studies, the comparison between positive and negative lymph nodes after pathologic examination showed a significant improvement in 5-year survival for N0 (56.5% and 44.8%, respectively) versus N+ tumors (9.6% and 15.2%, respectively).

The Ivor Lewis esophagectomy is a safe surgical approach with low morbidity and mortality in experienced hands. It allows for a radical resection under direct vision of most of the lymph node stations at risk. Because of the possibility of developing an intrathoracic leak at the anastomosis site and the absence of a third-field lymph node dissection, which is especially pertinent in cases of middle-third esophageal cancer, we prefer a three-hole (McKeown) approach. Nevertheless, for selected patients with previous neck surgery or cervical malignancy, for whom neck dissection and anastomosis are contraindicated, we still find the Ivor Lewis a suitable and preferred option. Recent advances in minimally invasive esophagectomy (MIE) focus on applying the Ivor Lewis approach by performing an intrathoracic anastomosis by means of video-assisted thoracic surgery (VATS).

A 56-year-old man presented with dysphagia for solid food and weight loss of approximately 10 kg during the last month. His past medical history was positive for a hypopharyngeal carcinoma 4 years earlier that was treated with chemoradiation and surgery. The clinical examination was unremarkable except for induration of the neck region owing to fibrosis secondary to radiotherapy and surgery. At endoscopy, a tumor was noted in the middle third of the esophagus that proved on pathologic examination to be a moderately differentiated squamous cell carcinoma. Endoscopic ultrasound revealed invasion of the esophageal muscular layer and possibly localized invasion of the surrounding fat without lymph node involvement (uT3N0). Bronchoscopy appeared to be normal. CT scan of the chest and abdomen confirmed the presence of the lesion in the esophagus without enlarged lymph nodes and without liver or lung metastases. A control CT scan of the neck revealed no evidence of local recurrence of the previous hypopharyngeal carcinoma or enlarged lymph nodes. The PET scan showed enhanced uptake only on the primary tumor, without evidence of metastatic spread of the disease. Electrocardiogram, pulmonary function tests, and blood examination were normal. As a result, this patient was judged to be a good candidate for curative surgery. Furthermore, because of the extensive neck changes from previous radiotherapy and surgery, we opted to perform the Ivor Lewis operation, with anastomosis high in the chest.

The operation was performed as described earlier. No metastatic deposits were found in the liver, lung, or elsewhere. Esophagectomy was combined with a two-field lymph node dissection, resulting in a complete resection. The esophagogastrostomy was created using a mechanical anastomosis, as described earlier.

The pathologic examination of the specimen showed a 3-cm-long tumor of the middle third of the esophagus with invasion of the muscular wall (muscularis propria) of the esophagus but no breakthrough and with negative section planes. All 32 resected lymph nodes were free of tumor (pT2N0M0-R0).

The patient was extubated quickly and discharged to the thoracic surgery ward the day after surgery. On the second postoperative day, he developed atrial fibrillation, treated with IV amiodarone with conversion to normal sinus rhythm. On the fifth postoperative day, a routine contrast barium swallow showed absence of leak and good emptying of the gastric tube (Fig. 18-4). The nasogastric tube was removed, and oral feeding was started. The patient was discharged on day 10. At the first outpatient clinic appointment 1 month after surgery the patient presented with no dysphagia, slight pain at the thoracotomy level, and a slight degree of shortness of breath. The chest x-ray was unremarkable. Four years after surgery, this patient remains disease-free but is experiencing some degree of acid reflux, which has been treated successfully with proton pump inhibitors.

In my opinion, this operation remains the mainstay for all esophageal cancer surgery. Especially in patients who have had neoadjuvant chemoradiation therapy or those with prior thoracic disease, this approach, whether done open or by laparoscopy/thoracoscopy, offers the best exposure to the esophagus and regional lymph nodes, as well as adjacent structures, aiding their resection and avoiding inadvertent injury. Although it does not permit three-field lymph node dissection, the need for this approach in distal GEJ tumors is as yet unproven. There are several minor technical differences in my own approach to this operation. I generally transect the stomach in the abdomen and then fashion the gastric tube before closing the belly. A routine feeding jejunostomy is performed at the initial laparotomy. At the time of the thoracotomy and anastomosis, more or less stomach can be pulled up into the chest as desired. This minimizes the amount of “redundant” gastric tube left lying in the chest, thereby avoiding the subsequent sequelae of reflux and dysphagia. Finally, when operating after chemoradiation, I routinely harvest an intercostal muscle flap when I enter the chest and use it to wrap the completed anastomosis and cover the gastric suture line.