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Ann Thorac Surg 2001;71:1803-1808
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Ivor Lewis esophagogastrectomy for esophageal cancer

^a Division of General Thoracic Surgery, Mayo Clinic, Rochester, Minnesota, USA
^b Department of Surgery, Mayo Clinic, Scottsdale, Arizona, USA

Accepted for publication February 22, 2001.

Address reprint requests to Dr Allen, Department of Surgery, Mayo Clinic, 200 First St, SW, Rochester, MN 55905
e-mail: allen.mark{at}mayo.edu

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. To examine the efficacy of the Ivor Lewis esophagogastrectomy for esophageal carcinoma prior to the widespread use of preoperative chemotherapy and irradiation, we reviewed our experience.

Methods. We reexamined the cases of 220 consecutive patients who underwent an Ivor Lewis esophagogastrectomy for esophageal cancer from January 1992 through December 1995.

Results. There were 196 men (89.1%) and 24 women. Median age was 65 years (range, 29 to 85 years). The results of pathological study showed adenocarcinoma in 188 patients (85.5%), squamous cell carcinoma in 31 (14.1%), and leiomyosarcoma in 1 patient (0.5%). Postsurgical staging was as follows: stage 0 in 10 patients, stage I in 19, stage IIa in 38, stage IIb in 28, stage III in 111, and stage IV in 14. The operative mortality rate was 1.4% (3 patients), and complications occurred in 83 patients (37.7%). Follow-up was 98.6% complete. Median survival for operative survivors was 1.9 years (range, 32 days to 8.7 years). The overall 5-year survival rate was 25.2%; it was 80% for patients in stage 0, 94.4% for those in stage I, 36.0% for those in stage IIa, 14.3% for patients in stage IIb, 10% for those in stage III and 0% for patients in stage IV.

Conclusions. Ivor Lewis esophagogastrectomy for esophageal cancer is a safe operation. Long-term survival is stage dependent. The low survival associated with advanced cancers should stimulate the search for effective neoadjuvant therapy.

	Introduction

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Esophageal carcinoma is an aggressive disease with a poor prognosis. Recently, preoperative chemotherapy and radiation therapy have been used in an attempt to increase long-term survival. Even though a large, well-performed randomized trial has not shown a clear advantage, preoperative chemotherapy and radiation therapy have been adopted by many centers [1–3]. Before most centers began routinely using preoperative adjuvant therapy, surgical resection had been the standard treatment of patients with esophageal carcinoma [4]. The approach described by Ivor Lewis [5], an abdominal mobilization of the stomach followed by a right thoracotomy for resection and reconstruction, has been our standard technique for esophagectomy. To establish a benchmark for surgical treatment of esophageal carcinoma prior to the widespread use of preoperative chemotherapy and radiation therapy, we reviewed our experience with the Ivor Lewis esophagogastrectomy during a time when adjuvant therapy was rarely used. The objective of this study was is to examine the morbidity, mortality, and efficacy of an Ivor Lewis esophagogastrectomy for the treatment of cancer of the midthoracic esophagus or gastroesophageal junction and to analyze the outcome of the patients.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
From January 1992 through December 1995, 220 consecutive patients underwent an Ivor Lewis esophagogastrectomy at the Mayo Clinic for malignant tumors of the esophagus. Their clinical records were reviewed for age, sex, symptoms at diagnosis, details of the surgical procedure, pathological findings, postoperative course, recurrence, and long-term survival.

Operative mortality was defined as any death during the first 30 days after operation or during the same hospitalization. All tumors were staged postsurgically by the TNM classification system of the American Joint Committee on Cancer [6]. Operative deaths and deaths that were not related to cancer were included in the survival statistics.

Overall patient survival was estimated using the method of Kaplan and Meier [7]. Estimates and 95% confidence intervals (CIs) are given for 1 year and 5 years. Univariate assessments of possible discrete risk factors were also made using the Kaplan-Meier method with significance tests performed using the log-rank test [8]. For continuous risk factors, the Cox proportional hazards model was used [9]. Multivariate Cox modeling of patient survival was done using those risk factors that were found to be significant by univariate analysis. The cumulative probability of disease recurrence was estimated using the Kaplan-Meier method. A p value of less than or equal to 0.05 was considered to be significant.

Clinical findings
There were 196 men (81.9%) and 24 women. Median age was 65 years (range, 29 to 85 years). Dysphagia was present in 155 patients (70.5%) preoperatively. Weight loss was reported in 85 patients (38.6%) (median weight loss, 7 kg; range, 2 to 30 kg), pain in 18 (8.2%), and bleeding in 17 (7.7%). The malignancy was found by esophagogastroduodenoscopic surveillance in 40 asymptomatic patients.

Surgical procedure
Our surgical technique has previously been described in detail [10, 11]. In brief, all the patients underwent initial abdominal exploration through an upper midline laparotomy. The stomach was mobilized on the right gastric and right gastroepiploic arteries. The left gastric artery was divided at its origin, and all lymph tissue around this vessel was included in the resection. A pyloromyotomy was performed in 211 patients (95.9%), pyloroplasty in 8 (3.6%), and no drainage procedure in 1 patient (0.5%). After the abdominal portion, a right posterolateral thoracotomy was performed. The esophagus was dissected from the mediastinum. All paraesophageal lymph nodes were removed. After resection of the specimen, an anastomosis was constructed between the stomach and the esophagus. The anastomosis was located in the apex of the chest in 189 patients (85.9%), at the level of the azygos vein in 22 (10.0%), and at the level of the carina in 9 (4.1%). It was fashioned in two layers in 168 patients (76.4%) and in one layer in 47 (21.4%), and it was stapled in 5 (2.3%). Concomitant procedures were performed in 90 patients (40.9%) and included lung resection in 30 (wedge excision in 29 patients and right lower lobectomy for concomitant lung cancer in 1 patient), liver biopsy in 21, jejunostomy in 10, cholecystectomy in 10, and others in 19.

Pathological findings
Postsurgical pathological studies revealed adenocarcinoma in 188 patients (85.5%), squamous cell carcinoma in 31 (14.1%), and leiomyosarcoma in 1 patient (0.5%). The tumor was located in the lower third of the esophagus or at the gastroesophageal junction in 198 patients (90%) and in the middle third in 21 (9.5%); it was multifocal in 1 patient (0.5%). Barrett’s mucosa was found in 89 patients (40.5%).

The postsurgical stage and TNM classification were as follows: stage 0 (Tis N0 M0) in 10 patients (4.5%), stage I (T1 N0 M0) in 19 (8.6%), stage IIa (T2–3 N0 M0) in 38 (17.3%), stage IIb (T1–2 N1 M0) in 28 (12.7%), stage III (T3–4 any N M0) in 111 (50.5%), and stage IV (any T any N M1) in 14 (6.4%) (Table 1). The stage of the 40 asymptomatic patients is shown separately in Table 1. M1 disease was discovered when a previously undetected pulmonary nodule was resected at the time of thoracotomy in 8 patients. In 6 patients, small (< 1.0 cm) liver metastases or involved celiac lymph nodes were resected. Tumor invasion was limited to the mucosa (T0) in 10 patients (4.5%), the submucosa (T1) in 22 (10.0%), and the muscularis propria (T2) in 41 (18.6%). One hundred seventeen patients (53.2%) had invasion beyond the muscularis (T3) and 30 (13.6%), invasion into adjacent structures (T4).

Five patients (2.3%) received chemotherapy and radiation therapy preoperatively. Postoperative chemotherapy was given to 39 patients (17.7%) and postoperative radiation therapy, to 36 (16.4%).

	Results

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The operative mortality rate was 1.4% (95% CI, 0.3% to 3.9%). All 3 patients died of a postoperative myocardial infarction. Complications occurred in 83 patients (37.7%) and included atrial fibrillation in 38 (17.3%), pneumonia in 27 (12.3%), asymptomatic contained leaks in 8 (3.6%), chylothorax in 4 (1.8%), and anastomotic leaks requiring reexploration, vocal cord paralysis, and acute myocardial infarction in 2 (0.9%) each. The median length of hospitalization was 11 days (range, 7 to 50 days).

Follow-up was complete for 217 patients (98.6%). Median survival for operative survivors was 1.9 years (range, 32 days to 8.7 years). At last follow-up, 54 patients were alive at a median time of 5 years after operation (range, 2.1 years to 8.7 years). The overall 5-year survival rate was 25.2% (95% CI, 19.3% to 31.1%) (Fig 1). The 5-year survival rate for patients in stage 0 was 80% (95% CI, 51.6% to 100%); for those in stage I, 94.4% (95% CI, 82.3% to 100%); for patients in stage IIa, 36.0% (95% CI, 23.0% to 56.3%); for those in stage IIb, 14.3% (95% CI, 5.2% to 35.4%); for those in stage III, 10.0% (95% CI, 5.4% to 17.6%); and for patients in stage IV, 0% (Table 2; Fig 2).

View larger version (14K): [in this window] [in a new window]   Fig 1. Probability of survival (death from any cause) of 220 patients undergoing Ivor Lewis esophagogastrectomy for malignancy. Zero time on abscissa represents date of esophageal resection. The number of patients at risk is shown adjacent to the curve.

View larger version (21K): [in this window] [in a new window]   Fig 2. Probability of survival (death from any cause) of 220 patients undergoing Ivor Lewis esophagogastrectomy for malignancy by American Joint Committee on Cancer stage. Zero time on abscissa represents date of esophageal resection.

Recurrent disease was documented in 100 patients. Location of first detection was available for 88 patients: system in 83 patients, local in 4, and both in 1 patient. None of the patients in stage 0 or stage I had recurrence during follow-up. The overall cumulative probability of recurrence at 5 years was 56.8% (95% CI, 48.4% to 64.7%).

Univariate analysis revealed that patient survival was not significantly associated with sex (p = 0.35) or location of the tumor (p = 0.72). Survival also was not associated with histology: adenocarcinoma (5-year survival rate of 22.9%) versus squamous cell carcinoma (5-year survival rate of 39.3%) (p = 0.14) (Fig 3). The location of the anastomosis was also found not to be significant. Anastomosis at the apex of the chest resulted in a 5-year survival rate of 26.2% versus 19.4% when the anastomosis was lower in the chest (p = 0.11). Conversely, patients with Barrett’s esophagus did have a better 5-year survival rate than those who did not (33.5% versus 19.5%; p = 0.005). However, more patients in the group with Barrett’s esophagus were in a lower stage, and, after we adjusted for stage, Barrett’s esophagus was no longer significant (p = 0.98).

View larger version (17K): [in this window] [in a new window]   Fig 3. Probability of survival (death from any cause) of 188 patients undergoing Ivor Lewis esophagogastrectomy for adenocarcinoma compared with 31 patients with squamous cell carcinoma (p = not significant). Zero time on abscissa represents date of esophageal resection. The number of patients at risk is shown adjacent to the curve.

View larger version (15K): [in this window] [in a new window]   Fig 4. Probability of survival (death from any cause) of 147 patients undergoing Ivor Lewis esophagogastrectomy for malignancy with positive lymph nodes compared with 73 patients without lymph node involvement (p < 0.0001). Zero time on abscissa represents date of esophageal resection. The number of patients at risk is shown adjacent to the curve.

	Comment

Top Abstract Introduction Material and methods Results Comment References

The patients in this series were a select group because of the nature of our referral practice. Most of them were white men with an adenocarcinoma in the lower third of the esophagus. The management of the patients in this study was also unique. During the years covered, we were not routinely using preoperative chemotherapy or radiation therapy for esophageal cancer. Primary resection was our method of treatment. This is obvious from our data, as only 2% of patients received preoperative irradiation or chemotherapy. This review establishes a benchmark for primary surgical therapy of adenocarcinoma of the esophagus using the Ivor Lewis method of resection. We currently give many patients preoperative chemotherapy and radiation therapy. This series may be useful as a comparison group, even though historical, with current groups who receive preoperative chemotherapy and radiation therapy.

Although different approaches have been described for the surgical resection of esophageal cancer, there is no statistical evidence, either in retrospective comparative series or in prospective randomized trials, that shows a difference in outcome [14–20]. We use an Ivor Lewis approach for patients with esophageal carcinoma for several reasons. This approach allows complete visualization of all perigastric and paraesophageal lymph tissue. It also allows direct visualization and dissection of the thoracic esophagus, thus virtually eliminating the uncommon but potentially disastrous occurrence of damage to adjacent structures that can happen during transhiatal esophagectomy. We favor the Ivor Lewis approach over the left thoracoabdominal approach because construction of the anastomosis high in the right chest is technically easier than performing an anastomosis high in the left chest. Of course, placement of a low anastomosis (ie, below the carina) should always be avoided because persistent reflux esophagitis will occur [20].

Use of the modified McKeown technique has been promoted because it allows not only mediastinal lymphadenectomy under direct vision but also cervical node dissection (the so-called three-field lymphadenectomy) [21]. We do not favor this more radical approach. Our patients usually have an adenocarcinoma at the gastroesophageal junction, and a cervical dissection does not seem warranted. Most of the literature in favor of a cervical lymphadenectomy concerns patients with squamous cell carcinoma in the middle- or upper-third of the esophagus [22]. The increased morbidity, including recurrent nerve injuries, the requirement of a tracheostomy, and the anastomotic leaks are not justifiable.

Our recurrence pattern also argues against a more radical lymphadenectomy. Only 5% of recurrences were local; in almost all patients, recurrent disease was detected at a distant site. Further resection of nodal tissue is unlikely to affect distant recurrence. In contrast, a strategy that would kill systemic disease is needed. It is to be hoped that an effective chemotherapeutic regimen for this disease will be found.

As other authors [18] have already pointed out, respiratory complications continue to be an important source of morbidity after esophagectomy through a thoracotomy. However, our most common complication was atrial fibrillation, usually a minor problem. Pneumonia occurred in 12.3% of patients, and this compares favorably with the results in other reports [19]. Our postoperative pneumonia rate is relatively low because of aggressive preventive measures: certified chest physical therapists attend the daily rounds, pulmonary rehabilitation is routinely used, all patients are placed on aspiration precautions, and patients receive excellent analgesia through thoracic epidural catheters. The problem of anastomotic leakage in the chest after an Ivor Lewis procedure was not a significant problem in our series. Only 2 patients required intervention. With careful technique and attention to detail, leaks are not a serious problem. No patient died as a result of an anastomotic leak.

Nevertheless, 5-year survival remains low. Our overall survival rate was 25.2%, remarkably similar to the 22.8% we reported 15 years ago. There remains a marked dependence on stage. Patients in an early stage had a very good survival rate. Those in stage 0 or stage I had survival rates of 80% and 94.4%, respectively, which is considerably higher than the 51% and 59%, respectively, reported by Orringer and colleagues [19]. This discrepancy is probably due to the understaging inherent to the transhiatal esophagectomy procedure. Our survival data for stage 0 or stage I patients were similar to those in a report by Ellis and associates [23], who used a combination of approaches but preponderantly a left thoracotomy. Survival for patients in higher stages remains poor. For our stage III patients, it was only 10% (Table 5).

In conclusion, an Ivor Lewis esophagogastrectomy is a safe surgical approach for esophageal cancer. The technique allows direct visualization and resection of most of the lymph node stations at risk. Survival is stage dependent and is low for patients in advanced stages. The higher incidence of systemic recurrence warrants the continuing search for multimodality therapy. Perhaps this series can serve as a baseline with which to compare series using new and more effective therapeutic options.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Mark S. Allen Daniel L. Miller Claude Deschamps Victor F. Trastek Peter C. Pairolero Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Visbal, A. L. Articles by Pairolero, P. C. Search for Related Content PubMed PubMed Citation Articles by Visbal, A. L. Articles by Pairolero, P. C. Related Collections Esophagus - cancer Related Article