Extended Transthoracic Resection Compared with Limited Transhiatal Resection for Adenocarcinoma of the Esophagus
Jan B.F. Hulscher, M.D., Johanna W. van Sandick, M.D., Angela G.E.M. de Boer, Ph.D., Bas P.L. Wijnhoven, M.D., Jan G.P. Tijssen, Ph.D., Paul Fockens, M.D., Peep F.M. Stalmeier, Ph.D., Fiebo J.W. ten Kate, M.D., Herman van Dekken, M.D., Huug Obertop, M.D., Hugo W. Tilanus, M.D., and J. Jan B. van Lanschot, M.D.
Background Controversy exists about the best surgical treatmentfor esophageal carcinoma.
Methods We randomly assigned 220 patients with adenocarcinomaof the mid-to-distal esophagus or adenocarcinoma of the gastriccardia involving the distal esophagus either to transhiatalesophagectomy or to transthoracic esophagectomy with extendeden bloc lymphadenectomy. Principal end points were overall survivaland disease-free survival. Early morbidity and mortality, thenumber of quality-adjusted life-years gained, and cost effectivenesswere also determined.
Results A total of 106 patients were assigned to undergo transhiatalesophagectomy, and 114 to undergo transthoracic esophagectomy.Demographic characteristics and characteristics of the tumorwere similar in the two groups. Perioperative morbidity washigher after transthoracic esophagectomy, but there was no significantdifference in in-hospital mortality (P=0.45). After a medianfollow-up of 4.7 years, 142 patients had died — 74 (70percent) after transhiatal resection and 68 (60 percent) aftertransthoracic resection (P=0.12). Although the difference insurvival was not statistically significant, there was a trendtoward a survival benefit with the extended approach at fiveyears: disease-free survival was 27 percent in the transhiatal-esophagectomygroup, as compared with 39 percent in the transthoracic-esophagectomygroup (95 percent confidence interval for the difference, –1to 24 percent [the negative value indicates better survivalwith transhiatal resection]), whereas overall survival was 29percent as compared with 39 percent (95 percent confidence intervalfor the difference, –3 to 23 percent).
Conclusions Transhiatal esophagectomy was associated with lowermorbidity than transthoracic esophagectomy with extended enbloc lymphadenectomy. Although median overall, disease-free,and quality-adjusted survival did not differ statistically betweenthe groups, there was a trend toward improved long-term survivalat five years with the extended transthoracic approach.
We studied whether transthoracic esophagectomy with extendeden bloc lymphadenectomy sufficiently improves overall, disease-free,and quality-adjusted survival over the rates with transhiatalesophagectomy to compensate for the possibly higher perioperativemorbidity and mortality and the increased costs of the treatment.
Methods
Study Design
The study was performed in two academic medical centers, eachperforming more than 50 esophagectomy procedures per year. Theeligible patients had histologically confirmed adenocarcinomaof the mid-to-distal esophagus or adenocarcinoma of the gastriccardia involving the distal esophagus, had no evidence of distantmetastases (including the absence of histologically confirmedtumor-positive cervical lymph nodes and unresectable celiaclymph nodes), and did not have unresectable local disease. Thesepatients were randomly assigned to undergo transhiatal esophagectomyor transthoracic esophagectomy with extended en bloc lymphadenectomybetween April 1994 and February 2000.
Patients had to be older than 18 years of age and in adequatephysical condition to undergo surgery (as indicated by theirassignment to American Society of Anesthesiologists class Ior II6). Exclusion criteria were previous or coexisting cancer,previous gastric or esophageal surgery, receipt of neoadjuvantchemotherapy or radiation therapy, recurrent laryngeal-nervepalsy, and extension of the tumor that made it impossible forthe surgeon to construct a gastric tube.
The preoperative diagnostic workup consisted of endoscopy withbiopsy and histologic examination, endosonography, externalultrasonography of the abdomen and neck (with biopsy if indicated),chest radiography, indirect laryngoscopy, and bronchoscopy iftumor ingrowth in the upper airway was suspected. Computed tomographywas performed only when indicated. Patients with carcinoma ofthe cardia underwent laparoscopy with laparoscopic ultrasonography.7Positron-emission tomography was not performed. After givingwritten informed consent, the patients were randomly assignedto one of the surgical procedures two to four weeks before surgery.Randomization was stratified according to the hospital and tumorsite (esophagus or cardia, as indicated by endoscopy). No blockingwas used within each of the four strata. Patients were classifiedas having esophageal carcinoma if the bulk of the tumor wasin the esophagus, Barrett's mucosa was present, or both; patientswere classified as having carcinoma of the cardia if the bulkof the tumor was in the cardia and Barrett's mucosa was notpresent.
Surgery and Pathological Examination
Surgery was performed by or under the direct supervision ofa surgeon-investigator with experience in esophageal surgery.During transhiatal esophagectomy, the esophagus was dissectedunder direct vision through the widened hiatus of the diaphragm,up to the inferior pulmonary vein. The tumor and its adjacentlymph nodes were dissected en bloc. A 3-cm-wide gastric tubewas constructed. The left gastric artery was transected at itsorigin, with resection of local lymph nodes. Celiac lymph nodeswere dissected only when there was clinical suspicion of involvement.After right-sided mobilization of the cervical esophagus, theintrathoracic, normal esophagus was bluntly resected from theneck to the abdomen with use of a vein stripper. Esophagogastrostomywas performed in the neck, without cervical lymphadenectomy.
Posterolateral thoracotomy was the first step in transthoracicresection with extended en bloc lymphadenectomy. The thoracicduct, azygos vein, ipsilateral pleura, and all periesophagealtissue in the mediastinum were dissected en bloc. The specimenincluded the lower and middle mediastinal, subcarinal, and right-sidedparatracheal lymph nodes (dissected en bloc). The aortopulmonary-windownodes were dissected separately. Through a midline laparotomy,the paracardial, lesser-curvature, left-gastric-artery (alongwith lesser-curvature), celiac trunc, common-hepatic-artery,and splenic-artery nodes were dissected, and a gastric tubewas constructed. The cervical phase of the transthoracic procedurewas identical to the transhiatal procedure, but a left-sidedapproach was used.
In both procedures, the origin of the left gastric artery wasmarked. Subcarinal nodes were marked separately in case of aplanned transthoracic resection. In the resection specimen,periesophageal tissue and the lesser omentum were palpated forthe presence of lymph nodes and subsequently dissected. Alllymph nodes identified by the pathologist were collected inseparate boxes and marked according to location, then cut intwo with both sides stained with hematoxylin and eosin. Pathologicalgrading was performed by or under the supervision of an investigatorwho was a senior gastroenterologic pathologist. Tumors wereassigned pathological tumor–node–metastasis (TNM)stages according to the Union Internationale contre le Cancer1997 system. Carcinoma of the cardia and distal esophageal carcinomawere considered a single clinical entity.8,9,10
Early postoperative complications were prospectively scoredby the study coordinators. Epidural anesthesia was used postoperativelyto minimize pulmonary complications.
Follow-up and Assessment of End Points
All patients were seen at the outpatient clinic at intervalsof three to four months during the first two years and everysix months for three more years. After five years, follow-updata were obtained by telephone from the patient or his or herfamily practitioner. Recurrence of disease was diagnosed onclinical grounds. However, whenever a relapse was suspected,radiologic, endoscopic, or histologic confirmation was sought.Recurrent disease was classified as local–regional (occurringin the upper abdomen or mediastinum) or distant (including cervicalrecurrences). Overall survival and disease-free survival werethe main end points of the study.
Survival was adjusted for the quality of life by the calculationof quality-adjusted life-years.11 For all 220 patients, theduration of survival in a certain state of health was obtainedfrom the clinical data and multiplied by a factor representingthe quality or "utility" of that state. Utilities range from0 (death) to 1 (perfect health), and patients are typicallyasked to assign a value to their own current health state orto other potential outcomes of treatment. The following sevenstates of health were identified: hospitalization immediatelyafter esophagectomy without complications, hospitalization immediatelyafter esophagectomy with early postoperative pneumonia, earlyrecovery at home, survival without recurrent disease, survivalwith recurrent local–regional disease, survival with recurrentdistant disease, and survival after surgery for an unresectabletumor. In a single interview conducted 3 to 12 months aftersurgery, utilities for these seven hypothetical health stateswere obtained in a subsample of 48 of 59 consecutive eligiblepatients who were free of recurrence of disease and were interviewedbetween January 1997 and March 1998. The utilities were elicitedwith a standard-gamble method, in which the patients were askedto choose between a certain but imperfect health state and agamble between a perfect health state with probability P anddeath with a probability 1–P. The value of P at whichthe participant is indifferent between the imperfect healthstate and the gamble is the utility.11 The whole study cohortwas subsequently included in the analysis of quality-adjustedsurvival.
Cost-Effectiveness Analysis
Costs were defined as the resources used multiplied by the priceper unit of each resource. They consisted of direct medicalcosts, direct nonmedical costs, and indirect costs. Direct medicalcosts included preoperative costs, in-hospital costs of primarysurgical treatment, and medical costs during follow-up. Directnonmedical costs included expenses for the patient such as travelcosts, special diets, or new clothes; indirect costs includedtime lost from work. Data on resource use during hospital treatmentwere collected prospectively from the information system atthe hospitals. Other resource uses were assessed by means ofa questionnaire completed by patients at base line and threemonths after surgery.
The 1998 costs of the operation per minute, the costs of a stayin the intensive care unit or medium care unit (ICU–MCU)per day, and the costs of a stay in the surgical ward per daywere assessed in euros (€1 equals $1) on the basis of real-costcalculations.12 These real-cost calculations included personnelcosts (surgeons, nurses, and anesthetists), costs of materials,costs of equipment, and overhead costs. Other costs were assessedaccording to the Netherlands guidelines for research on costsand included reimbursement fees (diagnostics and pathology),insurance charges (general-practitioner visits, outpatient visits,and medication), patient charges such as travel costs or aids,and costs of sick leave (based on the average national income).13Finally, incremental costs per quality-adjusted life-year werecomputed.
Statistical Analysis
To detect an estimated improvement in median survival from 14months to 22 months, corresponding to an increase in the 2-yearsurvival rate from 30 percent to 45 percent, among patientsundergoing transthoracic resection with extended en bloc lymphadenectomy,we calculated that 220 patients had to be enrolled. We assumeda two-sided significance level of 0.05 and a power of 0.90.Chi-square or Fisher's exact tests were used to compare categoricaldata; Student's t-test or the Mann–Whitney U test wasused for continuous data. All reported P values are two-sided.P values below 0.05 were considered to indicate statisticalsignificance. Survival curves were calculated from the timeof randomization to death from any cause or to the time of thelast follow-up visit (at which time data were censored). Disease-freesurvival was counted up to the time of a first relapse or deathfrom any cause or the time of the last visit without a previousrelapse (at which time data were censored). Survival curveswere constructed by the Kaplan–Meier method, and the log-ranktest was used to determine significance.
Patients with distant metastases, unresectable local tumor detectedduring the operation, or both were included in the analysisof disease-free survival even when the surgeon decided againstresection or performed a different resection, on the intention-to-treatprinciple. In a separate analysis, the disease-free intervalwas studied only in patients who underwent resection with noresidual tumor remaining and left the hospital alive, becausein patients in whom there is no microscopical tumor residueafter surgery, the benefit of extended lymphadenectomy mightbe greater than in other patients.
Results
Between April 1994 and February 2000, 220 of 263 eligible patientswere randomly assigned to treatment groups. There were no significantdifferences between the groups at base line in terms of demographiccharacteristics or characteristics of the tumor (Table 1). Completeendosonography was possible in 88 percent of patients. The meantime between randomization and surgery was three weeks in bothgroups.
Table 1. Characteristics of 220 Patients Randomly Assigned to Transhiatal Esophagectomy or Transthoracic Esophagectomy with Extended en Bloc Lymphadenectomy.
Ninety-three of the 106 patients in the transhiatal-esophagectomygroup (88 percent) and 109 of the 114 patients in the transthoracic-esophagectomygroup (96 percent) underwent the planned procedure (P=0.08).One patient did not undergo resection after massive aspiration,whereas the presence of unresectable local tumor, distant metastases,or both (detected during the operation) precluded resectionin 11 patients. Total gastrectomy was performed in three patients,and conversion to either unplanned transthoracic or unplannedtranshiatal resection took place in another three. Transhiatalresection was associated with a shorter median duration of surgery(3.5 hours, as compared with 6.0 hours for transthoracic resection;P<0.001) and a lower median blood loss per procedure (1.0vs. 1.9 liters, P<0.001). There were no perioperative deaths.Transhiatal resection was associated with fewer pulmonary complications,less chylous leakage, a shorter duration of mechanical ventilation,and shorter stays in the ICU–MCU and in the hospital (Table 2).Overall in-hospital mortality was 3 percent; two patients(2 percent) in the transhiatal group and five patients (4 percent)in the transthoracic group died.
Table 2. Early Postoperative Course in 220 Patients Randomly Assigned to Transhiatal Esophagectomy or Transthoracic Esophagectomy with Extended en Bloc Lymphadenectomy.
Four patients in each group did not have evidence of adenocarcinomain the resection specimen. These patients were included in allanalyses. Tumor stages were similar in the two groups, witha tendency toward more stage IV tumors in the transthoracic-esophagectomygroup (15 percent, as compared with 7 percent in the transhiatal-esophagectomygroup) (Table 3). A mean (±SD) of 16±9 nodes wereidentified in the resection specimen after transhiatal resection,and 31±14 after transthoracic resection. One hundredpatients undergoing transthoracic resection (88 percent) had15 or more lymph nodes identified in the resected specimen.There was no difference in the radicality of surgery, as indicatedby the residual-tumor classification, between the two groups.
Table 3. Characteristics of the Tumor and of Surgery in Patients Who Underwent Transhiatal Esophagectomy or Transthoracic Resection with Extended en Bloc Lymphadenectomy.
Follow-up continued until July 2002, ensuring a minimal follow-upof two and a half years. Follow-up was complete for all patients.The median follow-up was 4.7 years (range, 2.5 to 8.3). Recurrentdisease developed in 62 patients after transhiatal resection(58 percent) and 57 after transthoracic resection (50 percent).Local–regional recurrence occurred in 14 percent and 12percent of patients, respectively; distant recurrence in 25percent and 18 percent; and both in 18 percent and 19 percent(P=0.60). For the transhiatal and transthoracic procedures,the median disease-free interval was 1.4 years (95 percent confidenceinterval, 0.8 to 2.0) and 1.7 years (95 percent confidence interval,0.7 to 2.7), respectively (P=0.15) (Figure 1). The estimatedrate of disease-free survival at five years was 27 percent (95percent confidence interval, 19 to 38 percent) after transhiatalresection, as compared with 39 percent (95 percent confidenceinterval, 30 to 48 percent) after transthoracic resection. The95 percent confidence interval for the difference in the rateswas –1 percent to 24 percent (the negative value indicatesthat survival was better with transhiatal resection).
Figure 1. Kaplan–Meier Curves Showing Disease-free Survival among Patients Randomly Assigned to Transhiatal Esophagectomy or Transthoracic Esophagectomy with Extended en Bloc Lymphadenectomy.
At the end of follow-up, 142 patients had died — 74 inthe transhiatal-esophagectomy group (70 percent) and 68 in thetransthoracic group (60 percent; P=0.12). Thirteen patientsdied of causes unrelated to cancer. The median overall survivalwas 1.8 years (95 percent confidence interval, 1.2 to 2.4) aftertranshiatal resection and 2.0 years (95 percent confidence interval,1.1 to 2.8) after transthoracic resection with extended en bloclymphadenectomy (P=0.38) (Figure 2). The estimated rate of overallsurvival at five years was 29 percent (95 percent confidenceinterval, 20 to 38 percent) after transhiatal resection, ascompared with 39 percent (95 percent confidence interval, 30to 48 percent) after transthoracic resection. The 95 percentconfidence interval for the difference was –3 percentto 23 percent. The median number of quality-adjusted life-yearsafter transhiatal resection was 1.5 (95 percent confidence interval,0.8 to 2.1), as compared with 1.8 (95 percent confidence interval,1.1 to 2.4) after transthoracic resection with extended en bloclymphadenectomy (P=0.26) (Figure 3).
Figure 2. Kaplan–Meier Curves Showing Overall Survival among Patients Randomly Assigned to Transhiatal Esophagectomy or Transthoracic Esophagectomy with Extended en Bloc Lymphadenectomy.
Figure 3. Kaplan–Meier Curves for Quality-Adjusted Survival among Patients Randomly Assigned to Transhiatal Esophagectomy or Transthoracic Esophagectomy with Extended en Bloc Lymphadenectomy.
Survival was expressed in quality-adjusted life-years as calculated with the standard-gamble method.
The mean total direct and indirect costs of the procedure were€23,809 for transhiatal resection and €37,099 fortransthoracic resection with extended en bloc lymphadenectomy(Table 4). Therefore, the cost of treatment with transthoracicresection was 56 percent higher. The costs of surgery, of thestay in the ICU–MCU, and of the stay in the regular hospitalsurgical ward were the largest contributors to overall costs(Table 4). The incremental cost of transthoracic esophagectomywas €41,531 per quality-adjusted life-year gained.
Table 4. Mean Total Costs of Treatment per Patient for Patients Assigned to Transhiatal Esophagectomy or Transthoracic Esophagectomy with Extended en Bloc Lymphadenectomy.
Almost 90 percent of the patients who underwent extended enbloc lymphadenectomy after transthoracic esophagectomy had 15or more lymph nodes removed and identified in the section bythe pathologist, indicating that the extent of lymphadenectomyhad been adequate.14 Posterolateral thoracotomy gives wide accessto the mediastinum, thus offering both the possibility of extendedlymphadenectomy and the theoretical advantage of improving controlby extended en bloc dissection of all peritumoral tissues. However,the radicality of the surgery was similar in the two groups,reflecting the possibility of achieving adequate local controlby transhiatal resection. The distribution of TNM stages wasalso similar. There were slightly more patients with celiac-nodeinvolvement (M1) in the transthoracic-esophagectomy group, probablybecause of the lymphadenectomy in the upper abdomen, which ledto upgrading of the tumor when positive nodes were found. Tumorstaging was therefore improved by the increase in the numberof dissected lymph nodes in the upper abdomen after an extendeden bloc lymphadenectomy, as has been shown for gastric cancer.15,16Such "stage migration" might slightly influence the stage-by-stagecomparison, since positive nodes were found in the extendedfields in roughly 20 percent of the patients.15 However, thisphenomenon did not affect the difference in overall survivalrates.
Extended resection is believed to reduce the rate of local–regionalrecurrence, thereby increasing the quality of life and prolongingdisease-free and overall survival. In this series, the patternsof recurrence were similar after both types of resection. Disease-freeand overall survival curves were virtually identical in thefirst two years of follow-up. Later during follow-up, both disease-freeand overall survival curves diverged, showing a trend in favorof the extended transthoracic approach. Estimated five-yeardisease-free survival rates were 27 percent and 39 percent,respectively, whereas five-year overall survival rates were29 percent and 39 percent.
Supported by a grant from the Dutch Health Care Insurance FundsCouncil (1996-041).
We are indebted to Professor T. Lerut of the Department of Surgery,University Hospital Gasthuisberg Leuven, for his assistancein designing the study and in standardizing the transthoracicsurgical technique, and to C. Manshanden of the Department ofSurgery, Academic Medical Center, University of Amsterdam, whoacted as study coordinator at the beginning of the study.
Source Information
From the Departments of Surgery (J.B.F.H., J.W.S., H.O., J.J.B.L.), Medical Psychology (A.G.E.M.B., P.F.M.S.), Cardiology (J.G.P.T.), Gastroenterology (P.F.), and Pathology (F.J.W.K.), Academic Medical Center, University of Amsterdam, Amsterdam; the Departments of Surgery (B.P.L.W., H.W.T.) and Pathology (H.D.), Erasmus University Hospital Rotterdam, Rotterdam; and RADIAN and Medical Technology Assessment (P.F.M.S.), Nijmegen — all in the Netherlands.
Address reprint requests to Dr. van Lanschot at the Academic Medical Center at the University of Amsterdam, Department of Surgery, Suite G4-112, Meibergdreef 9, 1105 AZ Amsterdam, the Netherlands, or at j.j.vanlanschot{at}amc.uva.nl.
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Surgical Treatment of Esophageal Cancer
Kocher H. M., Tekkis P. P., Knisely J. P.S., Burtness B. A., Salem R. R., van Lanschot J. J. B., Tilanus H. W., Obertop H., Kitajima M., Kitagawa Y., Ozawa S.
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