Esophagectomy and Reconstruction

Michael Kent, md, Jeffrey Port, md, and Nasser Altorki, md

Contents

INTRODUCTION

EPIDEMIOLOGY OF ESOPHAGEAL CANCER PREOPERATIVE EVALUATION TREATMENT

OPTIONS FOR ESOPHAGEAL RECONSTRUCTION

MANAGEMENT OF COMPLICATIONS

COST OF SURGERY AND FUNCTIONAL OUTCOME

SUMMARY

REFERENCES

introduction

Esophagectomy is one of the most formidable operations performed by the gastrointestinal (GI) surgeon. Esophageal resection carries a complication rate of more than 40%, and should only be performed in centers experienced with the management of these patients. Indeed, the mortality of esophagectomy has been shown to be significantly lower in larger volume centers (1).

Esophageal resection is most frequently performed for carcinoma of the esophagus. Although less common, several other benign conditions may necessitate esophagectomy. For example, severe caustic burns to the esophagus often require esophageal resection and reconstruction. Esophageal perforation, primary motility disorders such as achalasia and scleroderma, and unsuccessful antireflux operations are additional indications for esophagectomy. Usually, these diseases may be managed with esophageal-sparing surgery, such as fundoplication or myotomy. Esophagectomy often represents the final treatment of patients with a variety of benign conditions who have failed more conservative surgical management.

From: Clinical Gastroenterology: An Internist's Illustrated Guide to Gastrointestinal Surgery Edited by: George Y. Wu, Khalid Aziz, and Giles F. Whalen © Humana Press Inc., Totowa, NJ

epidemiology of esophageal cancer

Although the prevalence of esophageal cancer reaches nearly epidemic levels in certain parts of Central and Southeast Asia, it remains a relatively uncommon disease in the United States. The American Cancer Society estimates that 13,000 patients have been diagnosed with esophageal cancer in 2001. Unfortunately, the majority of these patients will present with advanced disease not amenable to curative treatment. Despite the advent of novel chemotherapeutic agents and refinements in surgical technique, the overall 5-yr survival of patients with carcinoma of the esophagus remains in the range of 5-10%.

Esophageal cancer may develop as either a squamous cell or an adenocarcinoma. Although the clinical presentation is similar, the epidemiology and risk factors of these two histological subtypes differ markedly. Worldwide, squamous cell carcinoma is the more common. However, the incidence of squamous cell cancer exhibits a remarkable variability, with a "cancer belt" extending from northern Iran, through Central Asia, and into Northern China. Indeed, the disease accounts for almost 25% of all cancer deaths within the People's Republic of China (2). Outside these endemic areas, squamous cell carcinoma is far less common. However, clusters of high incidence have been identified in Northern France and Italy, as well as major metropolitan centers within the United States, such as New York, Los Angeles, and Washington, D.C. (3).

Several environmental factors have been clearly implicated in the development of squamous cell cancer of the esophagus. In the Western Hemisphere, alcohol and tobacco consumption are significant risk factors. The risk of both tobacco and alcohol use are strongly dose-related (4,5). The consumption of both seems to exert a synergistic rather than an additive effect. In part, this may owe to the ability of alcohol to improve the diffusion of tobacco-related carcinogens through the esophageal wall (6). Interestingly, in those locations where squamous cell cancer has its highest incidence, neither tobacco nor alcohol use seem to be significant risk factors. Instead, dietary components such as fermented fish or pickled corn that are rich in secondary amines have been implicated (7). The ingestion of hot beverages such as tea that are potentially caustic to the esophagus has also been postulated to predispose to squamous cell carcinoma (8). Finally, the observation that malignant cells may contain papillomavirus particles has suggested a possible infectious etiology (9).

Although squamous cell carcinoma had been the most common type of esophageal cancer in the United States 20 yr ago, adenocarcinoma is now the more prevalent. This change reflects an increase in the incidence of adenocarcinoma of almost 10% per year every year during the 1980s. This surge surpasses the increase in incidence of lung cancer, melanoma, and non-Hodgkin's lymphoma during the same period (10). Although the reason for this change is not known, it likely parallels the rise of cases of Barrett's esophagus, known to be a precursor to adenocarcinoma (11). It has been estimated that Barrett's esophagus increases the lifetime risk of developing adenocarcinoma of the esophagus 30- to 40-fold. At least 50% of resected specimens of adenocarcinoma retain residual Barrett's metaplasia (12). Given the likelihood that in other cases the metaplastic mucosa may have been completely overgrown with tumor, it appears that the majority of cases of adenocarcinoma are associated with Barrett's esophagus. The association between Barrett's esophagus and chronic gastroesophageal reflux has led to an intensive search for the responsible carcinogens. It appears that gastric and biliary reflux in com bination rather than either alone, which contributes to malignant transformation of the esophageal mucosa (13). It has been suggested that the increasing use of H2 blockers has also contributed to the rise of Barrett's esophagus and adenocarcinoma. However, this hypothesis is solely observational and a causative relationship has been difficult to establish.

In addition to Barrett's esophagus, several less common conditions have been associated with the development of esophageal cancer. For instance, the risk of esophageal cancer has been estimated to be 30-fold higher in patients with achalasia compared with the general population (14). Typically, these patients develop large, squamous cell tumors located in the middle-third of the esophagus. Unfortunately, the majority of patients present with advanced, unresectable disease. This is in part owing to the fact that the symptoms of carcinoma are difficult to distinguish from those of achalasia itself. Other conditions, such as tylosis, Plummer-Vinson syndrome, and caustic strictures are also known to predispose to esophageal cancer.

preoperative evaluation

All patients considered for esophagectomy must undergo a thorough preoperative evaluation. The length of the procedure and high incidence of complications necessitate that elective surgery be performed only when comorbidities have been optimally managed. The majority of patients undergoing esophagectomy have coexisting pulmonary and cardiac disease and for this reason pulmonary function tests and cardiac stress studies are routinely obtained. Indeed, the FEV1 is one of the most accurate predictors of postoperative mortality (15). Often, the incidence of postoperative complications can be greatly diminished by simple measures such as smoking cessation and a trial of antibiotics and inhaled bronchodilators.

In addition to a medical evaluation, patients with esophageal cancer must undergo preoperative staging prior to esophagectomy. Unfortunately, more than 50% of these patients will have unresectable disease at the time of their initial presentation. As in all fields of oncology, the main goal of staging is to ascertain which patients harbor locally advanced or metastatic disease, which would preclude curative surgery.

Several studies are routinely performed to stage esophageal cancer. A barium swallow is the initial study obtained in any patient who presents with dysphagia. This is customarily followed by esophagoscopy, which can provide vital information to the surgeon and oncologist. Most importantly, biopsy obtained during endoscopy will provide a tissue diagnosis. In addition, the length of esophagus involved by tumor, the presence of a hiatal hernia, and underlying Barrett's mucosa can all be determined at the time of endoscopy (Fig. 1). For tumors involving the upper- and middle-third of the esophagus, bronchos-copy is also necessary to exclude invasion of the trachea by tumor, which would imply unresectability. Computed tomography (CT) scanning is also routinely obtained in all patients with esophageal cancer. Although CT is not able to accurately determine nodal status and the depth of mural invasion, it is very sensitive in detecting the presence of distant disease, such as pulmonary or hepatic metastases.

Many other modalities to stage esophageal cancer have been reported and gained some degree of acceptance. Endoscopic ultrasound (EUS) is one modality that has become widely used in the past decade (16). EUS can accurately assess both the depth of invasion of the esophageal wall by tumor, as well as the presence of local lymphad-

Endoscopic Ultrasound Scleroderma
Fig. 1. Endoscopic view of an esophageal tumor.
Ultrasound Esophageal Tumor

Fig. 2. Endoscopic ultrasound image of an esophageal tumor invading the muscular wall of the esophagus.

Fig. 2. Endoscopic ultrasound image of an esophageal tumor invading the muscular wall of the esophagus.

enopathy (Fig. 2). EUS can also allow for fine-needle aspiration of these lymph nodes. Finally, some groups have advocated more invasive methods of staging such as thora-

coscopy and laparoscopy (17). Although these procedures are clearly sensitive for detecting extra-esophageal disease, it is not clear how much additional information is provided compared with standard modalities such as EUS and CT scanning.

treatment

Surgery, radiation therapy, and chemotherapy, either alone or in combination, have all been claimed as standard therapy of esophageal carcinoma. In part, this controversy stems from the generally poor outcome of any treatment modality. Although most surgical series studies report 5-yr survival rates of only 25%, esophagectomy is nonetheless considered to offer the best potential for cure. Recently, several randomized, controlled clinical trials have evaluated whether the addition of chemotherapy and radiation therapy to surgery offers any benefit. No study to date has supported the use of either of these modalities alone (18,19). However, the utility of combined induction chemoradiation is more controversial. Several small single-arm series has shown benefit for this approach compared with historical controls (20,21). However, three large, randomized trials have reported mixed results (Table 1) (22-24). Of these three, only one study demonstrated a statistically significant difference in survival with induction chemoradiation compared with surgery alone (24). This study has been criticized for the unusually poor survival rate (6%) in the surgical arm. To date, therefore, we consider surgical resection alone to be the standard of care for patients who are acceptable candidates.

As with nonoperative therapy, the surgical options for management of esophageal cancer are numerous. The two approaches most commonly used are the transthoracic (TTE) and the transhiatal esophagectomy (THE). The TTE exposes the esophagus through either a right or left thoracotomy, depending on the location of the tumor and the preference of the surgeon. In general, tumors of the distal third of the esophagus are best exposed through a left thoracotomy, those of the middle- and upper-third through a right thoracotomy. Regardless of the exposure, the principles of the operation do not differ: mobilization and resection of the involved esophagus with adequate margins, removal of adjacent lymph nodes, and the restoration of continuity of the GI tract. The esophagus must be completely mobilized from the diaphragmatic hiatus to the thoracic inlet to permit safe resection. Although tissue bearing lymph nodes is removed with the specimen, a meticulous lymph node dissection is not part of the standard esophagectomy. To restore continuity of the GI tract, a substitute for the esophagus must be found. Most commonly, the organ used for this purpose is the stomach. To do this, the stomach must be freed from its peritoneal attachments. If a left thoracotomy is used, the stomach may be exposed and mobilized through an incision in the diaphragm. If a right thoracotomy has been chosen, an additional upper abdominal incision will also be necessary. The greater curvature of the stomach is then freed from the omentum. A stapler is then fired across the lesser curve, in order to fashion the stomach into a tube appropriate for anastomosis with the remaining esophagus (Fig. 3A).

The vascular supply of this gastric tube is based on the right gastroepiploic artery, which must be preserved during mobilization of the stomach. Finally, the prepared gastric tube is then passed under the aortic arch and attached to the esophageal stump. Typically, the esophageal anastomosis is located within the mediastinum. However, a separate incision may be made in the neck to fashion a cervical anastomosis.

The transhiatal esophagectomy (THE) has become a popular alternative to a TTE, in part based on the belief that many potential complications are avoided by not entering

Table 1

Randomized Trials of Chemoradiotherapy Followed by Surgery Compared to Surgery

Operative Complete No. of TR dose mortality Pathologic Mediam Survival

Table 1

Randomized Trials of Chemoradiotherapy Followed by Surgery Compared to Surgery

Operative Complete No. of TR dose mortality Pathologic Mediam Survival

Author

Patients

(GY)

Chemotherapy

(%)

Response

Time (YR)

Survival rate (%)

Urba et al. (1997)

100

45

CDDP-BL-VBL

Surg-NS

NS

NS

33 (3 yr)

CRT-NS

NS

NS

18 (3 yr)

Walsh et al. (1996)

113

40

CDDP-FU

Surg-3.6

11

32 (3 yr)

CRT-8.6

25%

6

6 (3 yr)

Bosset et al. (1997)

297

18.5

CDDP

Surg-3.6

18.6

38 (3 yr)

CRT 12.3

26%

18.6

38 (3 yr)

Abbreviations: CDDP = cis- platinum, FU = 5- fluorouracil, BL = bleomycin, VBL = binblastine, NS = not stated, Surg = surgical arm, CRT = chemotherapy radiotherapy plus surgery arm, CT = chemotheraphy, TR = total radiation.

Abbreviations: CDDP = cis- platinum, FU = 5- fluorouracil, BL = bleomycin, VBL = binblastine, NS = not stated, Surg = surgical arm, CRT = chemotherapy radiotherapy plus surgery arm, CT = chemotheraphy, TR = total radiation.

Gastric Pull
Fig. 3. (A) Gastric pull-up. (B) Colonic transposition (Adapted from Shackelford's Surgery of the Alimentary Tract, Volume I, Fifth Edition, WB Saunders, 2002).

the chest. THE differs from TTE in two important respects. First, the thoracic esophagus is entirely mobilized through the hiatus of the diaphragm, without the need for a thora-cotomy incision. Second, the tubularized stomach is brought up into the neck where a cervical anastomosis is preformed. Proponents of this approach report decreased pain and pulmonary complications by avoiding a thoracotomy. In addition, an anastomotic leak within the neck is much easier to manage. Usually, the incision can be opened at the bedside and the leak safely drained. In contrast, a mediastinal leak carries a 50% mortality and often requires operative reexploration and possible takedown of the anastomosis. Critics of THE note that the operation affords a less-complete lymphadenectomy. In addition, the leak rate from a THE may be slightly higher, because the stomach must be mobilized further and the anastomosis carried higher than for a TTE. However, in the hands of qualified esophageal surgeons, the operative approaches are essentially equivalent. The operative mortality, incidence of complications, and length of stay have never been shown to differ between these operations. Furthermore, and most importantly, the 5-yr survival following a standard esophagectomy is a consistent 25%, whether the approach be transthoracic or transhiatal (25,26).

Several modifications have been proposed to improve the disappointing cure rate of a standard esophagectomy. An en bloc esophagectomy offers to the esophageal surgeon what is a standard principle to other surgical oncologists: removal of the involved organ with an envelope of adjoining normal tissue. This envelope of normal tissue should include the posterior pericardium, both pleural surfaces where they abut the esophagus, and the lymphovascular tissue between the esophagus and the spine. The deep location of the esophagus within the mediastinum, however, makes this a more challenging operation.

The evolution of a more formal lymph node dissection represents a further refinement in esophageal surgery. The basis for this stems from the distribution of lymphatic drainage within the esophagus. Unlike other organs of the gastrointestinal tract, the abundant lymphatic channels of the esophagus course longitudinally within the submucosa of the esophagus for long distances before draining to adjacent lymph nodes. However, in a standard esophagectomy, little attempt is made to remove any lymphatic tissue distant from the primary tumor. Perhaps, this in part explains the disappointing local recurrence rates (20-60%) following the standard operation. In a "two-field lymphadenectomy," the standard operation is modified to include the systematic removal of middle and lower mediastinal nodes (periesophageal, parahiatal, subcarinal, and aortopulmonary) and upper abdominal nodes (those adjacent to the celiac axis, and splenic, left gastric, and common hepatic arteries). An overall disease-free survival of 40% was achieved at our center in esophageal cancer patients resected with a combined en bloc, two-field lymphadenectomy (Fig. 4).

A "three-field lymphadenectomy" extends the lymph node dissection to include the lymph nodes within superior mediastinum, located along the course of the left and right recurrent laryngeal nerves. The rationale for extension of the lymph node dissection is based on the finding that nearly one-third of patients with presumably localized esophageal cancer have occult metastases to these nodes. Recent reports both in our center and in Japan have confirmed this finding, particularly in patients with adenocarcinoma of the esophagus. In addition, we have shown that the procedure may be conducted with a mortality and morbidity comparable to the "two-field" lymphadenectomy. Significantly, our long-term survival with this approach demonstrates a significant survival advantage over the standard esophagectomy and two-field lymphadenectomy (27,28). Unfortunately, lack of familiarity with this approach has limited its performance to a few specialized centers in Japan and the United States.

For those patients who are not candidates for curative esophagectomy, other options for palliation may be offered. Primary chemoradiation has been shown to produce 5-yr survival rates as high as 10%, and should be considered for the majority of patients whose cancer is unresectable. Esophageal dilatation offers short-term palliation, although the risk of esophageal perforation is not insignificant. Stenting or laser fulguration may also offer symptomatic relief in patients with a limited life expectancy. It should be emphasized that although esophagectomy offers excellent palliation of symptoms, patients should not be offered surgery without curative intent.

options for esophageal reconstruction

Restoration of continuity of the GI tract is most commonly performed with a portion of tubularized stomach. However, other options for reconstruction are available to the esophageal surgeon. For instance, colonic interposition may be offered to patients undergoing esophagectomy for benign disease. Interposition of colon offers several potential benefits: an organ with potentially functional peristalsis and an epithelium

0 10 20 30 40 50 60 70 80 90 100 110 120

Survival (Months)

Fig. 4. Overall survival of patients treated with an en bloc esophagectomy at Weill-Cornell Medical Center.

relatively impervious to acid reflux, a conduit of nearly unlimited length, and the ability to place the conduit in a location other than the posterior mediastinum. In addition, the vascular supply to the colon is abundant and well described. For malignant disease, the gastric pull-up is the preferred method for reconstruction. The use of stomach is technically straightforward and requires only one anastomosis. However, in situations in which prior gastric surgery has rendered the stomach unsuitable, colon interposition is an acceptable alternative. Some centers routinely use colon interposition for reconstruction after esophagectomy for benign disease. This practice is based on the belief that the development of anastomotic stricture and acid reflux may be less after colon interposition. No long-term studies have demonstrated the superiority of colon interposition over gastric pull-up. Furthermore, the necessity of additional abdominal surgery and a second anastomosis increases the complexity of an already demanding operation. Nonetheless, several large series have demonstrated the safety of this procedure in experienced hands (29,30).

Colonoscopy is required for preoperative evaluation of patients undergoing colonic interposition. Occasionally, the findings of polyps or occult malignancy will preclude the use of colon. Although angiography had once been considered mandatory, it is currently reserved for patients with significant vascular disease or those with a history of prior colonic surgery. Although either the left or right colon may be used for reconstruction, the left colon is by far the better alternative for several reasons. First, the smaller diameter of the left colon provides for a technically easier anastomosis to the proximal esophagus. Also, the blood supply to the left colon is less variable than that of the right colon. Finally, the left colon may be placed in the thorax in an isoperistaltic direction.

To perform a left colon interposition, the descending and transverse colon are mobilized. This may be performed through either a laparotomy or an incision in the diaphragm if a left thoracotomy has already been performed. The vascular supply to the left colon is identified including the marginal artery of Drummond, the left and right branches of the middle colic artery and the ascending and descending branches of the left colic artery. Adequate blood supply is determined by transillumination of the mesentery and palpation of a pulse. Once the appropriate length of conduit has been determined, temporary vascular clamps are placed on the vessels to be ligated. The viability of the bowel is then reassessed by visual examination. On occasion, intravenous fluoroscein may be useful if the viability of the conduit is in question. For long segment interposition, the vascular supply is based on the left colic artery. The colon is then divided distal to the splenic flexure distally and at the mid-transverse colon proximally. If additional length is required, the colon may be transected near the hepatic flexure. The colon is then mobilized through the lesser sac behind the stomach and brought into the chest through the esophageal hiatus. Anastamoses are then constructed to the proximal stomach and posterior wall of the stomach (Fig. 3B). Great care must be exercised to ensure that the vascular pedicle is not disrupted during mobilization to the chest. Graft ischemia may readily occur if the anastomosis is placed under tension or if the pedicle is rotated. Venous drainage from the colon is as important as arterial supply and may be easily compromised if the pedicle has been rotated.

Interposition ofjejunum may also be considered for short segment replacement of the esophagus. The variable blood supply to the jejunum mandates careful evaluation of the intestine prior to transfer. Congenital interruptions in the vascular arcade occur frequently and must be excluded before a segment of jejunum can be considered suitable. The dissection is usually begun at least 20 cm distal to the ligament of Treitz, at which point the vascular branches are longer and an appropriate pedicle may be identified more easily. Free jejunal transfer with construction of a microvascular anastomosis to the common carotid artery has been described for replacement of a short segment of the cervical esophagus (30).

management of complications

Even in the most experienced hands, an esophagectomy is a complex procedure that carries a consistent mortality of 5% and a complication rate of 40%. Complications common to all lengthy operations, such as cardiac arrythmias, myocardial infarction, and pneumonia are frequent. However, several complications are unique to esophagectomy. An esophageal leak carries the highest mortality rate of any complication. An asymptomatic leak that is detected on a routine barium swallow and appears to drain back into the esophageal lumen will usually heal without intervention. However, larger, uncontained leaks require adequate drainage either by an interventional radiology catheter, chest tube, or open drainage. Signs of sepsis will appear in conjunction with a leak that is not adequately drained and indicate that thoracotomy with drainage of the chest and decortication of the lung will be required. Endoscopy is useful to determine the viability of the stomach and size of the leak. Small, well-drained leaks will often heal if the lung is well expanded and there is no local sepsis. However, if there is extensive necrosis, often the safest plan is resection of the conduit and creation of a cervical esophagostomy. Graft necrosis, caused by infarction of the gastric tube, is a very rare complication that may be fatal.

Other complications may not be apparent for several months postoperatively. An anastomotic stricture is often related to a prior leak or vascular insufficiency at the tip of the gastric tube. Fortunately, the majority of patients respond well to periodic esophageal dilatation, and this is rarely required beyond the first postoperative year. Delayed gastric emptying is an uncommon complication that can usually be managed conservatively. Common causes of delayed gastric emptying include the lack of a pyloric drainage procedure, obstruction at a tight hiatus or a redundant intrathoracic stomach. Repeated endoscopy and balloon dilatation of the pylorus in conjunction with promotility agents such as metoclopramide and erythromycin are usually sufficient. Finally, reflux is a common problem after a gastric pull-up. It appears that the level of severity will vary inversely with the level of the anastomosis. Anastomoses above the azygous vein have a lower incidence of reflux than those below the vein. Symptoms of reflux are improved by smaller, more frequent feedings, avoidance of liquids with meals, and avoidance of recumbency after meals.

cost of surgery and functional outcome

As measured by both economic and psychological parameters, the cost of esopha-gectomy is high. Currently, an uncomplicated esophagectomy will require several hours of operating room time, and an average of 8 d spent in the hospital. The average cost incurred at our institution for this level of care is approx $30,000-$50,000. However, this figure may be easily doubled if complications ensue.

Few long-term studies on functional outcome following esophagectomy have been performed. In a longitudinal study evaluating more than 100 patients undergoing esophagectomy, more than 60% of patients experienced some form of gastroesophageal reflux and 25% of patients noted some degree of dysphagia. Despite this, the ability to work, perception of health, and resumption of daily activities were no different at long-term follow-up than the national norm (31). Although both physicians and patients must be aware that esophagectomy is a major undertaking, it may be performed safely and can provide excellent treatment for several disorders of the esophagus, as well as acceptable long-term quality of life.

summary

1. Esophagectomy is a formidable operation with a consistent mortality rate of 5% and morbidity rate of 40% whether it is done through the diaphragmatic hiatus with or without a thoracotomy.

2. The most common indication for this operation is potentially curable esophageal cancer, and the most common way that gastrointestinal continuity is restored is by pulling up a tube constructed out of the stomach. However, a segment of colon can be used if the stomach is not available, or the patient has benign disease and an expected long-term survival.

3. The most feared and lethal acute complication is a leak from the anastamosis; especially a leak into the chest and mediastinum which carries a 50% mortality.

4. Several postoperative complications following esophagectomy need medical therapy. These include strictures, which can be dilated, and gastric emptying problems and reflux symptoms.

5. Whereas extending the lymph node dissection during esophagectomy for cancer may increase survival in very experienced centers, it is also clear that esophagectomy is a poor palliative option for obviously incurable esophageal cancer.

references

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