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J Thorac Cardiovasc Surg 1996;111:85-95
© 1996 Mosby, Inc.
GENERAL THORACIC SURGERY |
Leuven, Belgium
From the Department of Thoracic Surgery, University Hospitals, Leuven, Belgium.
Address for reprints: T. Lerut, MD, Department General Thoracic Surgery, Catholic University of Leuven, U.Z. Gasthuisberg, Herestraat 49, 3000 Leuven, Belgium.
Abstract
From 1983 to 1989, 95 patients with carcinoma of the esophagogastric junction underwent resection. Overall hospital mortality rate was 6.2% (6/95). Actuarial survival analysis showed 5- and 10-year survivals of 33% and 31%, respectively. Five- and 10-year survivals of patients according to TNM stages were as follows: stage I (n= 13), 90% at both 5 and 10 years; stage II (n= 13), 70% at both intervals; stage III (n= 28), 28% at both intervals; and stage IV (n= 40), 11% and 8%, respectively. For patients with undiseased nodes (n= 26), 5- and 10-year survivals were 72% and 72%, compared with 18% and 16% for patients with diseased nodes (n= 68; p< 0.005). In patients who had involvement of both the abdominal and thoracic lymph nodes (n= 28), 5- and 10-year survivals were 13% and 13%, compared with 26% and 26% if metastases were confined to the abdomen (n= 37; p> 0.05). Grouping patients with diseased intrathoracic nodes together with patients with N2 abdominal nodes showed survivals of 14% at both 5 and 10 years. When tumors were staged as an esophageal carcinoma, classification of individual patients changed, as did the 5- and 10-year survivals. Five- and 10-year survivals were as follows: stage I (n= 8), 100% for both 5 and 10 years; stage II (n= 18), 68% for both 5 and 10 years; stage III (n= 27), 37% for both 5 and 10 years; and stage IV (n= 41), 10% for 5 years and 6% for 10 years. These data indicate that tumors of the esophagogastric junction tend to spread to both abdominal and thoracic nodes. However, reasonably good 5- and 10-year survivals can be obtained even in patients with nodal metastases in both areas. We suggest that N2 labeling be included for thoracic node metastases instead of the actual M+Ly label, because the N2 label better reflects the potential for curative surgery. Finally, staging tumors as gastric or esophageal carcinoma makes no significant difference in survival analysis, which raises the question whether these tumors behave more like esophageal carcinoma than gastric carcinoma.
In sharp contrast to a decreasing occurrence of gastric carcinoma,
1 a dramatic increase of adenocarcinoma of the esophagus and cardia has beenreported by several authors in recent years. 2-5 Even after resection the prognosis for these tumors is poor, 6 and a recent article has suggested that prognosis for patients with adenocarcinoma of the cardia is so poor that surgical treatment is not justified. 7 This poor prognosis seems to be related to the particular location of the tumor, positioned on both the stomach and esophagus, and its tendency for lymphatic spread into the lymph nodes of the superior abdominal compartment, as well as into the posterior mediastinum. 8 As a result, adenocarcinoma of the cardia is often considered to be a different entity that should be distinguished from gastric carcinoma and esophageal carcinoma.
Great controversy exists concerning the definition, classification, staging, and surgical access tactics. The effect of the extent of gastric and esophageal resection, lymphadenectomy, and the consequences of these factors on long-term survival is still open for discussion. 9,10 However, only a few studies are available analyzing the results of surgical therapy for carcinoma of the esophagogastric junction. 1 The aim of this study is to analyze in a retrospective way results of resectional surgery and especially long-term survival as a function of lymph node metastatic pattern, inasmuch as the latter may be strongly influential in determining surgical strategies and defining proposals or recommendations for classifications and staging.
Patients and methods
Definition
Inasmuch as no strict criterion exists by which to define carcinoma of the esophagogastric junction, we chose to include in the definition all adenocarcinomas with the core of tumor located at the Z line or within an area of 5 cm orally and 5 cm aborally of the anatomic junction between the esophageal and gastric walls. 11 Indeed, many tumors completely destroy the cardiac mucosa. In these cases we preferred to rely on muscular wall rather than on the mucosal Z line to define the transition between esophagus and stomach. As a result, adenocarcinomas in Barrett's mucosa located in the above-mentioned area were included, but tumors arising from Barrett's mucosa located in the tubular structure of the esophagus were excluded. Lower esophageal adenocarcinomas and subcardial gastric carcinomas encroaching on the Z line were excluded and considered to be esophageal and gastric carcinoma, respectively.
Patients
From 1983 until 1993, 259 patients with carcinoma of the esophagogastric junction as defined herein were operated on in our institution. So that a minimum follow-up of 5 years could be obtained, the cohort of 95 patients treated from 1983 to 1989 was studied retrospectively. Files and follow-up were available for all except one patient.
Preoperative staging was performed in all patients. The methods included chest roentgenography, barium swallow, endoscopy with biopsy, bronchoscopy, computed tomography of the chest and upper abdominal compartment, ultrasonography of the liver, and echoendoscopy, the latter in the more recent group of patients. Resected specimens were staged according to criteria of the revised TNM classification of 1992. 12
Statistical analysis
Survival curves were calculated according to the Kaplan-Meier method. The curves express the percentage of survivors. Statistical significance between slopes of curves was tested by the nonparametric log-rank score for censored values.
Surgical technique
The standard access consisted of an extended left thoracotomy through the sixth intercostal space. This incision provides excellent exposure of the thorax and upper abdominal compartment through an incision in the left part of the diaphragm at its periphery. This approach was used in 93.6% of the patients.
In the remaining six patients the following techniques were used: A right thoracotomy and laparotomy were performed in two patients because of a previous operation on the left side in one and a left-sided tuberculous pachypleura in the other. In four patients judged to be in poor condition for a thoracotomy, we decided to perform a transhiatal stripping of the esophagus.
Inasmuch as this is a retrospective study spanning 12 years, the surgical techniques were modified to some degree. In the initial period the operation consisted of a wide resection of the tumor, with lymph node resection being restricted to sampling of suspected lymph nodes in the upper abdominal compartment and posterior mediastinum. From 1985 on, however, resection and lymphadenectomy became much more radical.
Radical resection consisted in a subtotal esophagectomy with wide peritumoral resection including the thoracic duct and all peritumoral fatty and lymphatic tissue together with resection of the lesser curvature of the stomach. The aim of this more aggressive approach was to obtain a complete resection (R0 situation according to the TNM classification). Extensive lymphadenectomy included the following nodal groups: subcarinal, aortopulmonary window, paraesophageal, mediastinal, parahiatal, left gastric, hepatic, splenic, and celiac nodes.
As a rule, stomach was used to restore continuity, but again the oral and aboral extent of the operation changed over the years. During our initial experience, resection of the lesser curvature down to the junction of the gastric antrum and corpus and a safety margin of at least 5 cm distally from the lower pole of the tumor was judged to be sufficient. Along with the decision to perform extended two-field lymphadenectomies, we also decided to extend the safety margin on the gastric site by extending the resection of the lesser curvature to a level just proximal to the pylorus and taking away more of the fundus and corpus of the stomach laterally, thereby leaving a gastric tubulus along the greater curvature to be used for reconstruction.
On the esophageal side, initially a partial esophagectomy was the standard procedure. Anastomosis was performed at the level of the aortic arch, guaranteeing a margin of macroscopically healthy tissue above the proximal pole of the tumor of at least 5 cm and usually about 10 cm. For oncologic reasons, but even more because of the prevalence of reflux esophagitis after an intrathoracic anastomosis, 13 we decided to perform a subtotal esophagectomy with cervical esophagogastrostomy whenever possible. This resulted in 45 intrathoracic and 37 cervical esophagogastrostomies.
Finally, in the 13 remaining patients a total gastrectomy was performed: by necessity in four, and because of oncologic reasons (gross lymph node involvement along the lesser or greater curvature, or metastatic deposits on the gastric wall) in nine. In those patients continuity was restored with a jejunal Roux-en-Y loop with an intrathoracic esophagojejunostomy.
Results
Mortality and morbidity
The study group consisted of 95 patients with a mean age of 63 years (range 35 to 89 years). The demographic data are presented in Table I. Hospital mortality was 6.2% (6/95). In the first half of the study period, before 1986, mortality was 13% (3/23 patients). Mortality decreased in the second half (from 1986 on) to 4.1% (3/72 patients), reflecting the increasing experience of the team as a whole.
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Nine patients (9.5%) had an anastomotic leak (being fatal in two patients). Anastomotic leak was defined as any clinical or radiologic evidence of extravasation. There was no significant difference in the prevalence of anastomotic leaks between cervical (16%) and intrathoracic anastomoses (6.6%) (p > 0.05). Specific data on mortality and morbidity are listed in Table II.
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Table III. Inasmuch as insufficient data were available in one patient, the rest of the study comprises 94 patients. Seventy-two percent of all resected lesions were classified as advanced stage III or IV.
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Overall survivals including all causes of deathwere 51% at 1 year, 35% at 2 years, 28% at 5 years, and 16% at 10 years. The specific aim of this study, however, was to evaluate the impact of cancer-related mortality at the very long-term follow-up beyond 5 years. For this reason 11 patients who died of causes known to be unrelated to cancer were censored to death. Overall survival at 1 year was 54%, at 2 years 39%, at 5 years 33%, and at 10 years 31% (Fig. 1). All subsequent survival analyses were performed by excluding causes of death unrelated to cancer. As expected, TNM stage at the time of resection significantly influences survival. Fig. 2 shows 5- and 10-year survivals stage by stage. In patients not having lymph node disease (n = 26), 5- and 10-year survivals were both 72%, compared with 18% and 16%, respectively, for patients having diseased lymph nodes (n = 68) (p < 0.005) (Fig. 3).
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(Table IV). Fig. 5 shows the 5- and 10-year survivals stage by stage. The main difference with the staging as gastric carcinoma is a better outcome for stage III (37% versus 28%), but this difference is not statistically significant (p > 0.2).
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From these figures the assumption was made that patients with diseased lymph nodes beyond the gastric artery and patients with diseased lymph nodes in the posterior mediastinum could be grouped as a separate entity.
To exclude a negative impact from the T factor, we excluded all patients who simultaneously had a T4 staging. As a result, seven patients originally considered to have stage IIIb disease because of N2 classification and 17 patients originally considered to have stage IV disease because of intrathoracic diseased lymph nodes were grouped together (n = 24). In this setup, 5- and 10- year survivals were both 14%, as shown in Fig. 6. This figure is comparable with the 17% survival of the seven patients originally classified as having stage IIIb disease. Moreover, once the 17 patients with diseased intrathoracic lymph nodes were eliminated from stage IV, none of the patients remaining in stage IV survived more than 5 years.
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Carcinoma of the cardia or esophagogastric junction may be defined as an adenocarcinoma arising in the proximal 1 or 2 cm of the stomach. Ideally, to prove its origin, the residual cardiac mucosa should have in situ adenocarcinoma to distinguish gastric carcinoma, esophageal carcinoma, and Barrett's adenocarcinoma from each other. Because many tumors completely destroy the cardiac mucosa, however, separation of these different cancers is impossible. In the literature the debate continues.
According to Kalish and associates, 14 carcinoma of the esophagogastric junction can be defined as an adenocarcinoma arising within or immediately below the esophagogastric junction with replacement of all or a significant part of the cardiac mucosa and sparing of the more distal gastric tissue, but also including Barrett's carcinomas occurring in the limited zone of the gastroesophageal junction. From the macroscopic point of view, we accepted a 5 cm oral or aboral extension from the anatomic esophagogastric junction as proposed by Hölscher, Schüler, and Siewert. 11 Tumors mainly located in the stomach (even if encroaching on the esophagus), Barrett's adenocarcinoma mainly located in the tubular esophagus, and squamous cell carcinomas were excluded.
This approach seems to be more practical than the recommendation from the International Union Against Cancer (UICC) TNM supplement 1993. The UICC suggests classifying adenocarcinoma involving more than 50% of the esophagus as esophageal carcinoma and those involving more than 50% of the stomach, 15 including those equally distributed over the esophagus and stomach, as gastric carcinoma.
Moreover, in our opinion, this UICC TNM approach ignores one of the essential questions—whether carcinoma of the esophagogastric junction, because of its particular anatomic location, behaves differently from carcinoma of the esophagus or stomach. In this respect it is worthwhile to note that 12 of our patients had a histologically proved adenocarcinoma in Barrett's metaplasia. It can be assumed that this fraction is probably higher, for in a number of T3 and T4 tumors all mucosal tissue has been destroyed by the tumor, so that further proof of the presence of Barrett's origin is impossible.
Recent data from the literature showed Barrett's metaplasia as the source of adenocarcinoma of the cardia in up to 50% of adenocarcinomas of the esophagogastric junction. These data suggest a common origin of adenocarcinoma of the esophagus and adenocarcinomas located at the esophagogastric junction 16,17 and a behavior similar to that of an esophageal carcinoma.
Further evidence from Japanese studies and some Western studies suggests that carcinomas of the esophagogastric junction and carcinoma of the esophagus largely share patterns of age, sex distribution, and morphologic characteristics. 18-20 When compared with infracardiac gastric carcinoma, there seem to be highly significant differences in age distribution and macroscopic and microscopic appearance between esophagogastric junction tumors and gastric carcinoma. These differences suggest that the esophagogastric junction tumors must be more closely related to the esophagus than to the stomach. 19,20
In this study, carcinomas of the esophagogastric junction were restaged as esophageal carcinomas according to the TNM staging system. No major difference was seen between the two staging modalities either in overall survival or in survival stage by stage. Moreover, our results after resection for esophagogastric junction carcinoma are similar to those obtained after resection for esophageal carcinoma in a series of patients treated in a similar period in our institution. 21 Five-year survival in that series was 30% as compared with the 33% overall 5-year survival in the present series. As expected, the strongest prognostic indices are provided by the absence or presence of lymph node involvement, with 5-year survivals of 72% and 18%, respectively. Again, these figures are similar to those obtained in our series of esophageal carcinoma, with 63% 5-year survival for patients without lymph node involvement and 12% for those with lymph node involvement.
All these data from the literature and from our own experience, as well, seem to support the thesis that esophagogastric junction tumors should be classified as esophageal carcinomas in the TNM system. In such an eventuality lymph node staging, however, should be done according to the recommendations of the UICC TNM supplement 1993 in that lymph node metastases at or beyond the celiac axis are considered as a special subgroup to be separated from other distant metastases. However, this study is only a one- center experience. Confirmation by other groups must be obtained before esophagogastric junction tumors can be classified and staged as esophageal carcinomas.
The other main goal of this study was to critically analyze the value of the actual TNM staging system for carcinoma of the esophagogastric junction, especially in relation to lymph node status. In this respect, a most striking observation was the fact that in stage IV, which is to be considered as noncurable disease, distinct 5- and 10-year survivals of 11% and 8%, respectively, were obtained.
We suspected that surgical resection might indeed result in cure in patients with lymph node involvement at the celiac axis and especially at the level of the posterior mediastinum. This theory was confirmed by the findings that even in patients with both abdominal and thoracic involvement of lymph nodes, a 5- and 10- year survival of 13% was achieved. Grouping patients with abdominal N2 and thoracic M+Ly disease together into one group (to be considered as a stage IIIb group) again resulted in a cure rate of 14%, not significantly different from the 17% survival of the patients who originally had been classified as having stage IIIb disease.
Because mediastinal lymph nodes are frequently involved (up to 38% in our series) in adenocarcinoma of the esophagogastric junction, the consequences of these findings are clear. First, a careful lymph node dissection of the posterior mediastinum up to the carina is necessary to obtain a correct pathologic stage. This of course favors a transthoracic approach. The thoracoabdominal approach not only allows adequate esophagogastric resection but, more important, allows better and more complete removal of mediastinal lymph nodes 22-24 than any other approach, although an extended transhiatal approach by incising the diaphragm also may allow correct exposure and lymph node dissection.
Furthermore, the detection of diseased intrathoracic lymph nodes by different staging methods, either noninvasive (endoscopic ultrasonography) or invasive (thoracoscopy), 25 should not exclude such patients from treatment modalities aimed at cure, in particular, surgery.
For these reasons we suggest that diseased intrathoracic lymph nodes should no longer be considered as stage IV but should be classified as N2 nodes and added to the N2 group in the actual classification as one stage IIIb, reflecting better the potential for curative surgery in this subgroup.
Conclusion
Resection of carcinoma of the esophagogastric junction offers chances for cure in approximately one of three patients. Stage and especially lymph node involvement are the most important prognostic factors. However, in case of lymph node involvement surgical treatment may cure a distinct percentage of patients. Inasmuch as this is also the case for patients with diseased intrathoracic lymph nodes, these patients should not be considered to have M+Ly disease. We propose to include them in the N2 classification. Survival curves for patients with esophagogastric junction carcinoma in our experience are similar to those obtained for patients with esophageal carcinoma. These observations endorse data from the literature indicating that esophagogastric junction tumors behave like esophageal carcinoma. This raises the question whether esophagogastric junction tumors should be classified like esophageal carcinoma rather than gastric carcinoma. Further confirmation from other groups will be required before such a proposal can be made.
Surgical results from experienced centers, especially results obtained after extended resection and lymphadenectomy, remain the gold standard to which other therapeutic modalities (i.e., induction therapy) 5,26 should be compared.
Appendix: Discussion
Dr. Jeffrey A. Hagen (Los Angeles, Calif.).
I thank Dr. Lerut and his coworkers for the opportunity to focus on the problems being faced with the current staging system of cancers in the region of the esophagogastric junction.
Their article draws attention to two of the most important aspects of the difficulties encountered staging these tumors. The first involves the issue of whether these tumors are of gastric or esophageal origin and how they should be classified. We agree that the clinical behavior, patient demographics, and morphologic characteristics of these tumors more closely resemble esophageal cancers. In addition, our experience documenting intestinal metaplasia in about half the patients with adenocarcinomas of the cardia suggests a common pathophysiology with Barrett's adenocarcinomas arising higher in the tubular esophagus.
Dr. Lerut, you propose adding the involved mediastinal nodes to N2 disease in the gastric staging system, implying that you propose staging these as gastric tumors. Is this your preference or do you believe, as we do, that these tumors are distinct from the usual gastric cancers and thus should be staged instead as esophageal tumors?
My second question deals with the larger issue of the need for revising the staging system of esophageal cancer. We, too, have encountered problems with the current system, mostly with regard to patients with limited nodal disease. This has led to our adopting a modification of the staging system originally proposed by Dr. Skinner and recently endorsed by Dr. Ellis and his coworkers. This system stratifies patients on the basis of the degrees of lymph node involvement, using the number of involved nodes rather than their location. Have you considered this type of staging system? Has your experience been similar to ours in Los Angeles and that of Dr. Ellis in Boston?
This study has evolved over the years with respect to the extent of resection. In your current practice the gastric resection is carried distally along the lesser curvature to lower the prevalence of recurrence, and you have taken the anastomosis up into the neck for similar reasons.
My final question is this: Why not resect the stomach at the level of the antrum and use the colon to establish continuity, maximizing the potential for complete resection?
Dr. Lerut.
In answer to your first question, we have not done the same study that you did, evaluating the relation with intestinal metaplasia. This was out of the scope of our study. However, if we evaluate the results of your group, our work, and the results obtained by some other groups, I believe we will discover that it is better to distinguish them from gastric carcinoma and to classify them as esophageal carcinoma.
With regard to use of the Skinner classification rather than the TNM classification, we have not made a count of the lymph nodes. We have begun doing that only recently. As a result, we are not in a position to use number of involved lymph nodes as a prognostic parameter; therefore we restricted ourselves to evaluating whether this classification is accurate enough within the TNM classification. It is commonly accepted now that the number of the lymph nodes that are involved and also the location of the lymph nodes in respect to the primary tumor play an important role.
As to the last question, we routinely use the stomach if possible. We have had one local recurrence in the neck and two recurrences within the operative field in those patients in whom we could make a complete analysis of the pattern of recurrence. However, the recurrence rate is less than 10%, which is similar to the rates reported in most published series. Moreover, using the colon may add to the mortality risk, and that is the primary reason that we have been using the stomach instead of the colon. But I fully agree. If the operation can be done with the same rate of morbidity and mortality, the colon certainly can be used.
Dr. David B. Skinner (New York, N.Y.).
It was 33 years ago at this meeting that Andrew Logan first presented the concept of a mediastinal and upper abdominal node dissection for carcinoma of the cardia and introduced the term "en bloc resection." Since 1969 we have been using an en bloc resection for these tumors. We have extended the indications to include all types of thoracic esophageal cancer and presented our results here initially in 1983.
What has become apparent over the past 15 years or so is that the extended resection does yield a high survival, such as Professor Lerut has described, for patients with stage I or stage II disease. It is not so clear that it improves survival for patients with stage III or IV disease. However, when there is any question, the patient should receive the benefit of the doubt.
The issue of the staging system here is important. Those who view the cardia as part of the stomach use the stomach staging system. Those of us who view it as part of the esophagus use the esophageal staging system. For the benefit of the patients, though, we probably should consider both, because a diseased left gastric or celiac node from an esophageal cancer does not necessarily indicate stage IV disease, nor does a diseased mediastinal node for gastric cancer at the cardia necessarily indicate stage IV disease. I would urge against overstaging in these patients.
You reported that the prognosis is poor for patients who have involvement of both thoracic and abdominal nodes. In our series we have identified some adenocarcinomas with involvement of the mediastinal nodes but no involvement of the abdominal nodes. Have you encountered that situation and, if so, did that make any difference in the outcome?
We agree with your left thoracotomy approach because it gives excellent exposure for both the abdominal dissection and the mediastinal dissection. Those who advocate mainly an abdominal approach tend to cut corners on a mediastinal dissection. A few surgeons can do a good clean-out of the lower mediastinum through the hiatus, but not many use that procedure and thereby deny patients the advantages of the mediastinal dissection.
We tend to use colon for the reconstruction as well, mainly because we have had several patients in whom further Barrett's epithelium has developed above an esophagogastric anastomosis. That does not happen if we use the colon.
Finally, I would like to ask why you are excluding squamous carcinoma of the cardia. In the last month I have done two of these resections for identical gross tumors growing down the lesser curvature of the stomach from the cardia. One was squamous cell and one was adenocarcinoma, but grossly they looked the same. The metastatic pattern was interesting. The squamous cell tumor actually metastasized to the left gastric artery and not to the mediastinum. We would lump any tumor in this category, regardless of cell type, and treat both the mediastinum and the gastric dissection. Have you any comments on that?
Dr. Lerut.
Only three patients in our series had only thoracic lymph nodes involved, too small a group to allow any conclusions to be drawn. I certainly agree that these tumors should not be considered to be usual gastric carcinomas, and therefore a thorough mediastinal lymph node dissection is required. We favor the transthoracic approach.
We excluded squamous cell carcinoma specifically because we wanted to have a homogeneous cohort of patients. For this reason we excluded all Barrett's carcinomas located in the tubular esophagus and all squamous cell carcinomas. Your comment adds to the arguments that these tumors are behaving much more like esophageal carcinomas and should be considered as such, but only for practical reasons.
I can recall no experience in dealing with squamous cell carcinomas of the cardia growing down on the lesser curvature.
Dr. Zwi Steiger (Detroit, Mich.).
At Wayne State University we usually use combined chemotherapy to treat patients with adenocarcinomas of the distal esophagus: two courses of cisplatin 75 mg/m 2 and 5-fluorouracil 1000 mg/m 2 per day every day for 96 hours. The chemotherapy is separated by 4 weeks and is given concurrently with radiotherapy. An additional two courses of the same chemotherapy 3 weeks apart are given after radiation treatment. The radiotherapy consists of 5500 to 6000 cGy given over 6 weeks, starting at day 1 together with the first chemotherapy cycle. Patients will have computed tomographic scans of the chest and abdomen, esophagograms, esophagoscopy, and possible biopsy at the end of the radiotherapy and again on completion of chemotherapy. This is repeated 3 months later if the results of the initial evaluation are negative. Patients with persistent disease are offered surgical treatment. The complete response rate confirmed by biopsy is about 60%, and 30% of the patients are alive and well at 3 years.
The question in our institution is not how much to resect but whether to resect at all. The nonsurgical options need to be compared with surgical treatment in these patients in a natural prospective phase III trial.
Dr. Lerut.
Most of us are involved with programs dealing with chemotherapy, radiotherapy, or the combination in a neoadjuvant setting, and indeed for adenocarcinomas complete remissions have been reported. According to the literature, it appears that withough subsequent surgery the risk for local recurrence and further metastasis is much higher than if this induction treatment is followed by surgery. Certainly the risk of surgery is not as high as it used to be; we can keep the mortality rate below let's say 5%. So that is not really an argument not to perform a resection after induction therapy. We do have to wait for the results of a number of ongoing trials to see whether the combination of induction therapy and surgery will give better 5-year survival results than no subsequent surgery or than primary surgery.
Footnotes
Read at the Seventy-fifth Annual Meeting of The American Association for Thoracic Surgery, Boston, Mass., April 23-26, 1995. 
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T. W. Rice, E. H. Blackstone, L. A. Rybicki, D. J. Adelstein, S. C. Murthy, M. M. DeCamp, and J. R. Goldblum Refining esophageal cancer staging J. Thorac. Cardiovasc. Surg., May 1, 2003; 125(5): 1103 - 1113. [Abstract] [Full Text] [PDF]
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A. G. Casson, S. C. Evans, A. Gillis, G. A. Porter, P. Veugelers, S. J. Darnton, D. L. Guernsey, and P. Hainaut Clinical implications of p53 tumor suppressor gene mutation and protein expression in esophageal adenocarcinomas: Results of a ten-year prospective study J. Thorac. Cardiovasc. Surg., May 1, 2003; 125(5): 1121 - 1131. [Abstract] [Full Text] [PDF]
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 J. B.F. Hulscher, J. W. van Sandick, A. G.E.M. de Boer, B. P.L. Wijnhoven, J. G.P. Tijssen, P. Fockens, P. F.M. Stalmeier, F. J.W. ten Kate, H. van Dekken, H. Obertop, et al. Extended Transthoracic Resection Compared with Limited Transhiatal Resection for Adenocarcinoma of the Esophagus N. Engl. J. Med., November 21, 2002; 347(21): 1662 - 1669. [Abstract] [Full Text] [PDF]
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S. Raja, J. D. Luketich, L. A. Kelly, W. E. Gooding, S. D. Finkelstein, and T. E. Godfrey Rapid, quantitative reverse transcriptase-polymerase chain reaction: Application to intraoperative molecular detection of occult metastases in esophageal cancer J. Thorac. Cardiovasc. Surg., March 1, 2002; 123(3): 475 - 483. [Abstract] [Full Text] [PDF]
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T. E. Godfrey, S. Raja, S. D. Finkelstein, W. E. Gooding, L. A. Kelly, and J. D. Luketich Prognostic Value of Quantitative Reverse Transcription-Polymerase Chain Reaction in Lymph Node-negative Esophageal Cancer Patients Clin. Cancer Res., December 1, 2001; 7(12): 4041 - 4048. [Abstract] [Full Text] [PDF]
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X. Jiao, M. J. Krasna, J. Sonett, Z. Gamliel, M. Suntharalingam, A. Doyle, and B. Greenwald Pretreatment surgical lymph node staging predicts results of trimodality therapy in esophageal cancer Eur. J. Cardiothorac. Surg., June 1, 2001; 19(6): 880 - 886. [Abstract] [Full Text] [PDF]
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 G. A. Answini, B. L. Pratt, and F. L. Greene Strategies for Laparoscopic Diagnosis of Malignancy Surgical Innovation, June 1, 2000; 7(2): 68 - 77. [Abstract] [PDF]
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A. G. Casson, S. J. Darnton, S. Subramanian, and L. Hiller What is the optimal distal resection margin for esophageal carcinoma? Ann. Thorac. Surg., January 1, 2000; 69(1): 205 - 209. [Abstract] [Full Text] [PDF]
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 T. Lerut, W. Coosemans, P. De Leyn, D. Van Raemdonck, G. Deneffe, and G. Decker Treatment of Esophageal Carcinoma* Chest, December 1, 1999; 116 (2009): 463S - 465S. [Abstract] [Full Text] [PDF]
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N. A. Christie, T. W. Rice, M. M. DeCamp, J. R. Goldblum, D. J. Adelstein, G. Zuccaro Jr, L. A. Rybicki, and E. H. Blackstone M1A/M1B ESOPHAGEAL CARCINOMA: CLINICAL RELEVANCE J. Thorac. Cardiovasc. Surg., November 1, 1999; 118(5): 900 - 907. [Abstract] [Full Text] [PDF]
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J. D. Luketich, D. M. Friedman, T. L. Weigel, M. A. Meehan, R. J. Keenan, D. W. Townsend, and C. C. Meltzer Evaluation of distant metastases in esophageal cancer: 100 consecutive positron emission tomography scans Ann. Thorac. Surg., October 1, 1999; 68(4): 1133 - 1136. [Abstract] [Full Text] [PDF]
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C. van de Ven, P. De Leyn, W. Coosemans, D. Van Raemdonck, and T. Lerut Three-field lymphadenectomy and pattern of lymph node spread in T3 adenocarcinoma of the distal esophagus and the gastro-esophageal junction Eur. J. Cardiothorac. Surg., June 1, 1999; 15(6): 769 - 773. [Abstract] [Full Text] [PDF]
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M. J.R. Dalrymple-Hay, K. B. Evans, and R. E. Lea Oesophagectomy for carcinoma of the oesophagus and oesophagogastric junction Eur. J. Cardiothorac. Surg., May 1, 1999; 15(5): 626 - 630. [Abstract] [Full Text] [PDF]
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T. Lerut Esophageal surgery at the end of the millennium J. Thorac. Cardiovasc. Surg., July 1, 1998; 116(1): 1 - 20. [Full Text]
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R. J. Korst, V. W. Rusch, E. Venkatraman, M. S. Bains, M. E. Burt, R. J. Downey, and R. J. Ginsberg Proposed Revision Of The Staging Classification For Esophageal Cancer J. Thorac. Cardiovasc. Surg., March 1, 1998; 115(3): 660 - 670. [Abstract] [Full Text]
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J. D. Luketich, P. Schauer, R. Landreneau, N. Nguyen, K. Urso, P. Ferson, R. Keenan, and R. Kim MINIMALLY INVASIVE SURGICAL STAGING IS SUPERIOR TO ENDOSCOPIC ULTRASOUND IN DETECTING LYMPH NODE METASTASES IN ESOPHAGEAL CANCER J. Thorac. Cardiovasc. Surg., November 1, 1997; 114(5): 817 - 823. [Abstract] [Full Text]
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R. Bardini and M. J. Krasna Thoracoscopic staging of esophageal cancer: a prospective, multiinstitutional trial. Ann. Thorac. Surg., October 1, 1996; 62(4): 1237 - 1239. [Full Text]
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H. Wilke and U. Fink Multimodal Therapy for Adenocarcinoma of the Esophagus and Esophagogastric Junction N. Engl. J. Med., August 15, 1996; 335(7): 509 - 510. [Full Text]
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 C. G. Bremner Invited Commentary Arch Surg, July 1, 1996; 131(7): 713 - 713. [Abstract] [PDF]
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