225
27
Lymph Node Dissection for Carcinoma of the Esophagus
Nasser K. Altorki
In addition, all retroperitoneal tissues between the superior border of the pancreas and the crus of the diaphragm are included within the dissection.
2. The mediastinal fi eld, which includes the middle and lower periesophageal nodes, the sub- carinal nodes, and the thoracic duct with its asso- ciated lymph nodes as it courses through the middle and lower mediastinum. Resection of the trunk of the azygous vein, as previously pro- posed, is no longer considered a necessary com- ponent of the operation.19
3. The third fi eld, which includes the chain of lymph nodes along both recurrent nerves throughout their mediastinal and cervical course, as well as the deep cervical nodes posterior and lateral to the jugular vein and the supraclavicular nodes. Thus, the third fi eld encompasses a group of nodal stations that span the superior posterior mediastinum and the lower neck.
The purpose of this chapter is to review the published evidence supporting either of these two surgical strategies. For purposes of clarity, the data from transhiatal and transthoracic resections are presented separately, despite the earlier contention that the two procedures differ only slightly in the extent of the associated lymph node dissection.
27.1. Transhiatal Esophagectomy
This procedure is one of the more common tech- niques for esophagectomy in North America and Europe. In a study of the National Cancer The controversy surrounding the surgical treat-
ment of esophageal cancer focuses, almost exclu- sively, on the extent of lymph node dissection required during esophagectomy. The majority view holds that an extended or a radical lymph node dissection will not improve overall or disease- free survival because the disease is systemic at the time of diagnosis and that long-term outcomes are largely determined by the biological behavior of the tumor; an issue that cannot be infl uenced by the extent of surgical dissection. Advocates of this view embrace the conventional techniques of esophageal resection where the esophagus is extracted from its mediastinal bed along with the adjacent periesophageal and lesser curvature nodes.1–18 This extent of lymph node excision is easily achieved by either a transhiatal or a trans- thoracic approach and thus, the terms transhiatal or transthoracic are descriptive only of the means of surgical access rather than the extent of lymph node dissection which is, for all intents and pur- poses, similar in extent. In contrast, the opposing view held by a minority of surgeons in the West, states that a radical lymphadenectomy may improve local disease control and survival in a small, but signifi cant, proportion of patients. The extent of lymph node dissection, as generally pro- posed by Japanese and some Western surgeons includes at least two nodal basins (two-fi eld dis- section) and occasionally three nodal basins (three-fi eld dissection). These nodal regions or fi elds include:
1. The abdominal fi eld, which encompasses the paracardial, lesser curvatures, left gastric, celiac, common hepatic, and splenic artery nodes.
Database of the American College of Surgeons, transhiatal esophagectomies were performed in 25% to 30% of patients with carcinoma of the esophagus.20 The procedure entails extirpation of the intrathoracic esophagus without a thoracot- omy and advancement of the esophageal substi- tute, usually a greater curvature gastric tube, to the neck for reconstruction. The extent of nodal dissection with this operation is essentially limited to the periesophageal nodes and those perigastric nodes along the cardia, the lesser gastric curve, and the left gastric artery.
The largest single experience with transhiatal esophagectomy is that of Orringer, who reported on 800 patients with cancer of the intrathoracic esophagus and cardia.1 Adenocarcinoma was present in 69% of the patients, while 28% had epidermoid cancer. Hospital mortality was 4.5%
and morbidity was 27%. Overall survival at the 2-, 3-, and 5-year mark was 47%, 34%, and 23%, respectively. Five-year survival was 59% for stage I patients and 22% for stage IIA patients. Patients with stage III disease had a 2- and 5-year survival rate of 32% and 10%, respectively. There was an overall statistically signifi cant survival advan- tage for patients with adenocarcinoma (24% vs.
17%).
This study by the University of Michigan group is considered the benchmark for transhiatal esophagectomy and represents the best expected outcome following transhiatal resections for car- cinoma. However, it is clear from reviewing the literature that these survival rates are quite con- sistent with the experience of most surgeons who practice a similar approach2–7 (Table 27.1). Gelfand
reported on 160 patients who underwent tran- shiatal esophagectomy for carcinoma of the lower esophagus and cardia.2 Most tumors were adeno- carcinoma and most were in earlier stages. Sur- vival rates at 2 years and 5 years were 40%
and 21%, respectively. Gertsch reported on 100 patients with esophageal carcinoma who were uniformly treated with transhiatal esophagec- tomy without adjuvant therapy over a 10-year period.3 Hospital mortality was 3% and morbid- ity 68%. The median survival was 18 months and the overall 5-year survival was 23%. There was no difference in survival between patients with adenocarcinoma compared to those with squa- mous histology. Survival was better for T1 and T2 tumors (63% 5-year survival). Vigneswaran reported on the results after transhiatal esopha- gectomy in 131 patients, the majority of whom had adenocarcinoma.4 Operative mortality was 2%. Overall 5-year survival was 21%. Patients with stage I disease had a 47.5% 5-year survival compared to patients with stage III disease, whose 5-year survival was 5.8%. Patients with adeno- carcinoma had a 5-year survival of 27%, while not a single patient with squamous cell cancer was alive at the 5-year mark.
A few studies reported the local recurrence rates following transhiatal resection.21–23 Urba and colleagues reported the results of a random- ized trial comparing transhiatal esophagectomy alone to transhiatal esophagectomy following induction chemoradiotherapy.21 More than 75%
of patients in both study arms had adenocarci- noma. There was no statistically signifi cant dif- ference in either overall survival or disease-free
TABLE 27.1. Transhiatal esophagectomy for esophageal cancer.
Hospital 5-year Median
Author Year Patients Cell type mortality (%) survival (%) survival Orringer1 1999 800 A/S 4.5 23 ns
Chu5,a 1997 20 S 15 ns 16 months
Horstmann6 1995 46 A/S 15 20 12 months Putnam10 1994 42 A/S 4.8 18 14 months
Gertsch3 1993 100 A/S 3 23 ns
Vigneswaran4 1993 131 A/S 2.3 21 ns Goldminc7,a 1993 32 S 6.25 30 (3 years) ns
Gelfand2 1992 160 A 0.9 21 ns
Abbreviations: A/S, adenocarcinoma/squamous cell carcinoma; ns, not significant; S, squamous cell carcinoma.
aRandomized trials comparing transhiatal and transthoracic esophagectomy.
survival between the two arms of the study.
Overall survival and disease-free survival were both 16% after transhiatal esophagectomy alone.
Local recurrence as a component of treatment failure occurred in 42% of patients in the surgery alone arm. This fi gure is almost identical to the local failure rate reported by Barbier, who pro- spectively evaluated the recurrence rate in 50 patients that underwent transhiatal resection for cancer by serial CT scans.22 Local recurrence was detected in 39% of patients. More recently, Hulscher reported a loco-regional recurrence rate of 37% among 137 esophageal cancer patients treated by transhiatal esophagectomy without preoperative therapy.23
In summary, it appears that for patients with esophageal adenocarcinoma, transhiatal esopha- gectomy can usually be performed with an opera- tive mortality of 5% or less in the hands of experienced esophageal surgeons (Table 27.1).
Five-year survival rates are generally in the 20%
to 25% range. Survival for patients with stage I tumors is in the 60% to 70% range, while patients with stage III disease have a 5% to 10% 5-year survival. Finally, the procedure is associated with failure to control or eradicate local disease in nearly 40% of patients.
27.2. Standard Transthoracic Esophagectomy
Transthoracic esophagectomy is probably the most widely performed operation for cancer of the esophagus worldwide. In the United States, 50% to 60% of all surgically treated tumors of the esophagus are performed using a transthoracic approach.20 The procedure can be carried out either through a right or left thoracotomy inci- sion, depending on the preference of the surgeon and the location of the tumor within the esopha- gus. Generally, a right thoracotomy is required for adequate exposure of tumors in the middle or upper thirds that are anatomically intimately related to the membranous trachea or the arch of the aorta. Tumors located at the gastroesopha- geal junction or in the lower third of the esopha- gus can also be approached through a left thoracotomy incision combined with a left phre- notomy, or, alternatively, with a left thoracoab-
dominal incision. Regardless of the side of the thoracotomy, the extent of lymph node dissection is usually limited to the immediate periesopha- geal, cardial, and perigastric nodes.
One of the largest experiences in North America with this approach is that of Ellis and coworkers.8 The authors reported their experiences with nearly 500 patients who received a transthoracic esophagectomy employing standard surgical techniques. One third had squamous cell carci- noma, while the majority had adenocarcinoma of the esophagus or gastroesophageal junction.
Hospital mortality was 3.3%. Complications occurred in 34% of patients. Overall 5-year sur- vival including operative mortality and non–
cancer-related deaths was 24.7%. Patients who had a complete (R0) resection had a 5-year sur- vival of 29%, while no patients with either resid- ual microscopic (R1) or macroscopic disease (R2) survived 5 years. Median and 5-year survival for patients with adenocarcinoma was 18 months and 25%, respectively. The corresponding fi gures for squamous cell cancers were 18 months and 20%, respectively, and were not statistically dif- ferent from those for adenocarcinoma. Five-year survival was 79% for patients with stage I disease, 38% for those with stage IIA, and 27% for those with stage IIB. Patients with stage III disease had a 3- and 5-year survival of 20% and 13.7%, respectively.
This series by Ellis is generally representative of the results achievable using this surgical tech- nique in many esophageal centers across the United States. For example, a recent study from the Mayo Clinic reported on the results after transthoracic esophagectomy in 220 patients, of whom 188 had adenocarcinoma.9 Notwithstand- ing an impressively low hospital mortality and morbidity (1.4% and 37%, respectively), the sur- vival rates remained essentially similar to those reported by Ellis nearly a decade previously.
Overall 5-year survival was 25% and survival at 5 years for stages I, IIa, IIb, and III was 94%, 36%, 14%, and 10%, respectively. A review of some of the surgical series reported within the past decade from North America and Europe is shown in Table 27.2. Resectability rates ranged from 60%
to 90% and hospital mortality ranged from 3.2% to 23%. Five-year survival rates varied between 8% and 24%. The variability in rates of
resectability, hospital mortality, and 5-year sur- vival likely represents inherent differences in patient selection, surgical expertise, and the retrospective nature of nearly all of these studies.
More instructive to review are the survival results achieved by the surgical arms of random- ized trials comparing various preoperative regi- mens to surgical resection alone. The most recent of these trials was the North American Inter- group trial that compared chemotherapy fol- lowed by surgery with surgery alone.17 There were 467 eligible patients of which 227 underwent primary surgical resection. The majority of resec- tions were through a transthoracic approach.
One hundred six patients had squamous cell cancer (47%) and 121 had adenocarcinoma (53%).
Hospital mortality was 6%. Major complications occurred in 26% of patients. Overall survival at 1-, 2-, and 3-years was 60%, 37%, and 26%, respectively. Actuarial 5-year survival was 20%.
There was no difference in outcome between patients with adenocarcinoma and those with epidermal cancer. In the trial by Walsh et al, 113 patients, all of whom had adenocarcinoma, were randomized to receive either surgery alone or chemoradiation followed by transthoracic esoph- agectomy.18 Hospital mortality in the control arm was 2% and 3-year survival was 6%. In 2002, the Medical Research Council Esophageal Cancer Working Group reported the results of a large multicenter controlled, randomized trial of pre- operative chemotherapy followed by esophagec-
tomy versus esophagectomy alone.24 Although the details of the operative procedures were not described, the assumption may be made that the majority of cases had been done using a transtho- racic approach, a common surgical strategy in most European centers. Survival in the surgery alone arm was 34% at 2 years and 15% at 5 years, with no difference in survival between adenocar- cinoma and squamous cell cancer.
Local recurrences following standard trans- thoracic resections have been reported in 30%
to 60% of patients. Most of the data regarding local recurrences are obtained from the surgical control arms of the various randomized trials. In the previously mentioned Intergroup trial com- paring esophagectomy alone with chemotherapy followed by esophagectomy, the local recurrence rate in the control arm was 31% among 135 patients who received a complete (R0) resection.
An additional 68 patients had an R1 or R2 resec- tion. The overall local failure rate (persistent or recurrent disease) in all 227 patients in the control arm was 61%.17
27.3. Comparison of Transhiatal and Transthoracic Esophagectomy
Several retrospective studies have shown little difference in the peri-operative and survival out- comes between transhiatal and transthoracic esophagectomy. Rindani reviewed the results from 44 series published between 1986 and 1996.25 TABLE 27.2. Transthoracic esophagectomy for esophageal cancer.
Hospital 5-year
Author Year Patients Cell type mortality % survival % Median survival Hofstetter15 2002 994 A/S 7% 34% (3 years) 20 months Visbal9 2001 220 A/S 1.4% 25.2% 1.9 years Karl11 2000 143 A/S 2.1% 29.6 (3 years) 1.6 years
18 months (A) Ellis8 1999 455 A/S 3.3% 24.7% 18 months (S) Kelsen17 1998 227 A/S 6% 26% (3 years) 16.1 months Adam16 1996 597 A/S 6.9% 16.3% ns Sharpe14 1996 562 A/S 9% 18% ns Walsh18 1996 113 A 2% 6% (3 years) 11 months Lieberman12 1995 258 A/S 5% 27% 27 months Putnam10 1994 134 A/S 8.2% 19% 22 months
Wright13 1994 91 A 2% 8% ns
Abbreviations: A, adenocarcinoma; A/S, adenocarcinoma/squamous cell carcinoma; ns, not significant; S, squamous cell carcinoma.
Thirty-three articles reported results on 2675 patients who underwent transhiatal resection while 29 articles reported results of transthoracic resections done in 2808 patients. Thirty-day mortality was 6.3% after transhiatal and 9.5%
after transthoracic esophagectomy. Overall 5- year survival was 24% after transhiatal esopha- gectomy and 26% following transthoracic resection. More recently, Hulscher and colleagues reported a meta-analysis of the results of all com- parative studies of transhiatal and transthoracic esophagectomy.26 Their analysis included data abstracted from 50 articles published in the English literature between 1990 and 1999, with a total of 7500 patients. There was no statistically signifi cant difference in overall 3-year and 5-year survival between the two procedures. There are two small, randomized trials that compared transhiatal and transthoracic resections with survival as an end point. The study by Chu and colleagues5 comprised 39 patients, while the one by Goldminc had a total of 67 patients.7 Neither study described the statistical details by which these small sample sizes were calculated. In the study by Goldminc and coworkers,7 67 patients were randomly assigned to receive either a tran- shiatal or transthoracic (non–en bloc) esopha- gectomy. Although the median operating time for transthoracic esophagectomy (TTE) was sig- nifi cantly longer than that for transhiatal resec- tion (THE; 4h vs. 6h) there was no difference in other intra- and postoperative outcome measures including the need for blood transfusions, inten- sive care unit stay, and postoperative complica- tions. Pulmonary complications occurred with similar frequency in both groups (THE, 19%;
TTE, 20%), as did anastomotic leaks (THE, 6%;
TTE, 9%) and recurrent nerve injuries (3% each).
The 2-year overall survival was identical in both groups (40%). No information was given regard- ing disease-free survival or adequacy of local control. The study by Chu and colleagues5 ran- domized an even smaller group of patients to either a THE (n = 20) or a TTE (n = 19). There was no difference in intraoperative or postoperative complications including transfusion require- ments, cardiopulmonary complications, or anas- tomotic leaks between the two groups. There was no difference between both arms of the study in either local recurrence rates (25% for THE and
21% for TTE) or median survival times (THE, 16 months; TTE, 13.5 months).
In summary, it is clear that there are no impor- tant differences in survival between transhiatal and transthoracic esophagectomy. Given the sim- ilarity in the extent of nodal dissection between the two procedures these results may have been predictable.
27.4. En Bloc Esophagectomy
Logan introduced the en bloc concept in 1963 and it was re-introduced by Skinner in 1979.19,27 The basic premise of the en-bloc operation is to maxi- mize local tumor control by resection of the tumor- bearing esophagus within a wide envelope of adjoining tissues that includes both pleural sur- faces laterally and the pericardium anteriorly where these structures are intimately related to the esophagus. Posteriorly, the lymphatics wedged dorsally between the esophagus and the aorta, including the thoracic duct throughout its medi- astinal course, are resected en bloc with the speci- men. This posterior mediastinectomy necessarily results in a complete mediastinal node dissection from the tracheal bifurcation to the esophageal hiatus. Additionally, an upper abdominal lymph- adenectomy is performed including the common hepatic, celiac, left gastric, lesser curvature, para- hiatal, and the retroperitoneal nodes. Local recur- rence rates reported by proponents of this approach have been in the 2% to 10% range.28,29 This is a strikingly low local failure rate when compared to local recurrences reported following either tran- shiatal esophagectomy or standard transthoracic resections, or those reported following chemora- diation delivered with curative intent.30
Critics have argued that the procedure is asso- ciated with a high operative mortality and mor- bidity, without an apparent survival advantage.
In fact, in the earliest report by Skinner, the oper- ative mortality for 80 patients with cancer of the cardia treated by an en bloc resection was 11%
and the 5-year survival only 18%.19 However, the past decade has witnessed a signifi cant reduction in hospital mortality to the 5% range.30–32 Several investigators have also reported survival rates exceeding those achievable by conventional tech- niques of esophageal resection. Lerut reported
his experience with 195 patients who had an R0 (curative) resection for adenocarcinoma of the distal esophagus and gastroesophageal junc- tion.31 All patients had transmural disease (T3) and none received preoperative therapy. Five- year survival was 57% for node-negative patients and 26% for patients with nodal metastases.
A prospective or cohort study by Altorki and Skinner reported on 111 patients who had an en bloc resection, the majority of which had adeno- carcinoma and stage III disease.32 Hospital mor- tality was 3.6%. Overall 5-year survival was 40%.
Stage-specifi c survival was 78%, 72%, and 39%, respectively, for stages I, IIa, and III disease.
Hagen reported similar results in a smaller group of patients with adenocarcinoma of the distal esophagus and gastroesophageal junction.33 En bloc resection was performed in 30 patients and transhiatal resection was done in 16 patients.
Overall survival was signifi cantly better after en bloc resection (41% vs. 14%, p = 0.001). A survival advantage was observed in patients with early lesions (T1 and T2) where 5-year survival was 75% versus 21%, in favor of en bloc resection.
Similarly patients with transmural tumors (T3) associated with 5 or less positive nodes had a signifi cantly better survival after en bloc resec- tion (27% vs. 9%).
An important criticism of most of these studies is the failure to clearly defi ne the criteria for patient selection for one procedure versus another. For example, in the study by Hagen and colleagues, the patients receiving a transhiatal resection were either signifi cantly older than the en bloc group or had a worse performance status with respect to cardiopulmonary function.33 Additionally, a selection bias towards inclusion of patients with early-stage disease in the en bloc groups may have favorably biased survival outcome. The only randomized trial reported to date comparing transthoracic en bloc resection with transhiatal esophagectomy was reported by Hulscher and coworkers in 2002.34 The authors randomly assigned 220 patients with adenocarci- noma of the mid to distal esophagus, or adeno- carcinoma of the cardia, to either a transhiatal resection or a transthoracic esophagectomy with extended en bloc lymphadenectomy. The mean number of resected lymph nodes was 31 nodes after en bloc resection and 16 after transhiatal
resection. There was no difference between the two arms in hospital mortality but morbidity was signifi cantly higher after the extended en bloc procedure. The study was powered to detect a 50% relative improvement in survival in favor of the en bloc procedure. Although there was an important trend favoring the transthoracic (en bloc) group in both overall (39% vs. 29%) and disease-free survival (39% vs. 27%) at 5 years, the resultant 25% relative improvement in survival did not achieve statistical signifi cance. A subse- quent report by the same group suggested that with continued follow-up the difference in overall and disease-free survival achieved statistical sig- nifi cance for adenocarcinoma of the esophagus, but not that of the cardia.35 Interestingly in this randomized trial there was no difference in either the rate of loco-regional recurrence or the time to recurrence between the two arms of the study.
27.5. Three-Field Lymphadenectomy
The concept of three-fi eld lymph node dissection for esophageal cancer was developed by Japanese surgeons in the 1980s in response to the observa- tion that as many as 40% of patients with resected squamous cell esophageal cancer developed iso- lated cervical lymph node metastases.36 A nation- wide retrospective study was subsequently reported describing the fi ndings and potential benefi ts of esophagectomy with three-fi eld dis- section.37 The additional third fi eld of dissection included excision of the nodes along both recur- rent nerves as they course through the mediasti- num and neck, as well as a modifi ed cervical node dissection. Previously, unsuspected cervi- cal nodal metastases, primarily in the recurrent nodes, were seen in approximately one third of patients. Furthermore, the authors reported a signifi cantly higher overall 5-year survival after three-fi eld dissection in comparison to two-fi eld dissection. The largest Japanese study from a single institution was reported by Akiyama in 1994.38 The authors reported their experience with 717 patients in whom a complete (R0) resec- tion was performed using either a two-fi eld (n = 393) or a three-fi eld technique (n = 324). Five-year survival in node-negative patients was 84% after
the three-fi eld procedure compared to 55% after two-fi eld lymphadenectomy (p = 0.004). Patients with node-positive disease also fared better after three-fi eld dissection with a 5-year survival rate of 43% compared to a 28% 5-year survival rate after two-fi eld dissection (p = 0.0008). Two pro- spective studies have been reported.39,40 The study by Nishihira was a prospective, randomized trial that showed a survival advantage for three-fi eld over two-fi eld lymph node dissection (65% vs.
48%); however the difference was not statistically signifi cant.39 The study from the National Cancer Hospital in Tokyo was a prospective, nonran- domized, case-matched study that showed that 5-year survival was signifi cantly better after three-fi eld dissection (48% vs. 33%; p = 0.03).40 Five-year survival in the group of patients with cervical nodal disease was an impressive 30%.
The relevance of these fi ndings to a Western pop- ulation affl icted primarily by esophageal adeno- carcinoma remains unknown.
The only experience in North America with this technique was reported by Altorki and col- leagues in 2002.41 A prospective database was established in 1994 to examine survival and recurrence after esophagectomy with three-fi eld dissection. The procedure was performed in 80 patients, 60% of which had adenocarcinoma of the esophagus. Hospital mortality was 5% and morbidity 47%. Recurrent nerve injury occurred in 6% of patients. An average of 60 nodes were resected per patient. The prevalence of cervical nodal metastases was 37% in patients regardless of cell type or location of the tumor within the esophagus. Overall and disease-free survival was 50% and 46%, respectively, and was not infl u- enced by cell types. Patients with adenocarci- noma who had metastases to the recurrent laryngeal lymph nodes had a 3- and 5-year sur- vival of 30% and 15%, respectively. In contrast patients with squamous cell carcinoma and posi- tive recurrent laryngeal nodes had a 5-year sur- vival of 40%. Lerut reported the only European experience with esophagectomy and three-fi eld lymph node dissection.42 One hundred and seventy-four patients had an R0 three-fi eld esophagectomy with a hospital mortality of 1.4%
and morbidity of 57%. Fifty-fi ve percent of patients had adenocarcinoma of the esophagus or cardia. Overall and disease-free survival at 5
years was 42% and 46%, respectively. There was no difference in survival between patients with adenocarcinoma compared to those with squa- mous carcinoma (35% vs. 44%, p = 0.5). The inci- dence of positive cervical nodes in patients with adenocarcinoma was 23% and was slightly higher for those with esophageal versus cardial tumors (26% vs. 18%). Four- and fi ve-year survival for patients with adenocarcinoma and positive cervi- cal nodes were 35% and 11%, respectively.
27.6. Perspective
The above discussion of the results of the various surgical approaches suggests that there is no sub- stantive difference in mortality, morbidity, recur- rence, or survival between limited lymph node dissection performed through a transhiatal or a conventional transthoracic approach. The data supporting this conclusion are derived from the two small, randomized trials by Chu and Gold- minc5,7 that compared transhiatal and transtho- racic resections with survival as an endpoint (level of evidence 1). Despite the small sample sizes in both studies, the consistency of their results with those reported by a large number of retrospective studies (level of evidence 3) sug- gests that there is most likely no important dif- ferences between these two surgical approaches in the extent and results of lymph node dissec- tion and that survival is likely to be in the 25% to 30% range. It is also apparent that with the excep- tion of two cohort studies by Altorki and col- leagues32,41 (level of evidence 2) and the single randomized trial by Hulscher and coworkers34 (level of evidence 1), the evidence supporting an extended lymph node dissection is derived from case series (level of evidence 3) with a variable number of patients and undefi ned selection cri- teria. However, the survival of results in the two cohort studies reported by Altorki and colleagues (5-year survival of 40%) are consistent with similar results reported by other Japanese and European centers practicing a similar surgical strategy. Interestingly, these survival fi gures are also identical to the 39% survival reported by Hulscher and colleagues34 in the en bloc arm of their randomized trial.34 This constitutes a 25%
to 30% relative improvement in survival for the
en bloc procedure in patients with adenocarci- noma of the middle and distal esophageal thirds.35
Based on these data, patients with esophageal carcinoma (stages I–III), with good performance status (ECOG performance status 0–1) and no prohibitive comorbidities, should undergo an esophagectomy with at least a two-fi eld en bloc dissection (recommendation grade B). The evi- dence suggests that the procedure provides the most complete staging information (level of evi- dence 1) and improves survival (level of evidence 2), but does so at the expense of an increase in perioperative morbidity (level of evidence 1). The role of a three-fi eld dissection remains to be more clearly defi ned.
lymphadenectomy for the treatment of oesopha- geal cancer. Eur J Surg 1995;161:557–567.
7. Goldminc M, Maddern G, Le Prise E, Meunier B, Campion JP, Launois B. Oesophagectomy by a transhiatal approach or thoracotomy: a prospec- tive randomized trial. Br J Surg 1993;80:367–370.
8. Ellis FH Jr. Standard resection for cancer of the esophagus and cardia. Surg Oncol Clin N Am 1999;8:279–294.
9. Visbal AL, Allen MS, Miller DL, Deschamps C, Trastek VF, Pairolero PC. Ivor Lewis esophagogas- trectomy for esophageal cancer. Ann Thorac Surg 2001;71:1803–1808.
10. Putnam JB Jr, Suell DM, McMurtrey MJ, et al.
Comparison of three techniques of esophagec- tomy within a residency training program. Ann Thorac Surg 1994;57:319–325.
11. Karl RC, Schreiber R, Boulware D, Baker S, Coppola D. Factors affecting morbidity, mortality, and survival in patients undergoing Ivor Lewis esophagogastrectomy. Ann Surg 2000;231:635–
643.
12. Lieberman MD, Shriver CD, Bleckner S, Burt M.
Carcinoma of the esophagus. Prognostic signifi - cance of histologic type. J Thorac Cardiovasc Surg 1995;109:130–138.
13. Wright CD, Mathisen DJ, Wain JC, et al. Evolution of treatment strategies for adenocarcinoma of the esophagus and gastroesophageal junction. Ann Thorac Surg 1994;58:1574–1578.
14. Sharpe DA, Moghissi K. Resectional surgery in carcinoma of the esophagus and cardia: What infl uences long-term survival? Eur J Cardiothorac Surg 1996;10:359.
15. Hofstetter W, Swisher SG, Correa AM, et al. Treat- ment outcomes of resected esophageal cancer.
Ann Surg 2002;236:376–384.
16. Adam DJ, Craig SR, Sang CT, Walker WS, Cameron EW. Esophagogastrectomy for carcinoma in patients under 50 years of age. J R Coll Surg Obstet 1996;41:371–373.
17. Kelsen DP, Ginsberg R, Pajak TF, et al. Chemo- therapy followed by surgery compared with surgery alone for localized esophageal cancer. N Engl J Med 1998;339:1979–1984.
18. Walsh TN, Noonan N, Hollywood D, Kelly A, Keeling N, Hennessy TP. A comparison of multi- modal therapy and surgery for esophageal adeno- carcinoma. N Engl J Med 1996;335:462–467.
19. Skinner DB. En-bloc resection for neoplasms of the esophagus and cardia. J Thorac Cardiovasc Surg 1983;85:59–69.
20. Daly JM, Fry WA, Little AG, et al. Esophageal cancer: results of an American College of Surgeons Patients with esophageal carcinoma should
undergo an esophagectomy with at least a two-fi eld en bloc dissection (level of evidence 1 to 2; recommendation grade B). There is insuffi cient evidence to make recommenda- tions regarding the role of a three-fi eld dissection.
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