Background We conducted a multicenter, randomized trial to comparepreoperative chemoradiotherapy followed by surgery with surgeryalone in patients with stage I and II squamous-cell cancer ofthe esophagus.
Methods The preoperative combined therapy consisted of two one-weekcourses; each involved radiotherapy, in a dose of 18.5 Gy deliveredin five fractions of 3.7 Gy each, and 80 mg of cisplatin persquare meter of body-surface area, administered 0 to 2 daysbefore the first day of radiotherapy. The surgical plan includedone-stage en bloc esophagectomy and proximal gastrectomy bythe abdominal and right thoracic routes, to be performed immediatelyafter randomization in the group assigned to surgery alone andtwo to four weeks after the completion of preoperative chemoradiotherapyin the group assigned to combined therapy.
Results A total of 297 patients entered the study; 11 were foundto be ineligible, and 4 were lost to follow-up. Of the remaining282, 139 were assigned to surgery alone and 143 to combinedtherapy. After a median follow-up of 55.2 months, no significantdifference in overall survival was observed; the median survivalwas 18.6 months for both groups. As compared with the grouptreated with surgery alone, the group treated preoperativelyhad longer disease-free survival (P = 0.003), a longer intervalfree of local disease (P = 0.01), a lower rate of cancer-relateddeaths (P = 0.002), and a higher frequency of curative resection(P = 0.017). However, there were more postoperative deaths (P= 0.012) in the group treated preoperatively with chemoradiotherapy.Three prognostic factors were found to influence survival ina multivariate analysis: the disease stage, based on computedtomography; the location of the tumor; and whether the surgicalresection was curative.
Conclusions In patients with squamous-cell esophageal cancer,preoperative chemoradiotherapy did not improve overall survival,but it did prolong disease-free survival and survival free oflocal disease.
Esophageal cancer is a highly malignant disease. Data from Frenchtumor registries indicate that five-year overall survival rangesfrom 2 percent to 8 percent for all stages.1,2,3 The squamous-celltype predominates, but the incidence of adenocarcinoma of theesophagus is increasing rapidly.4
Surgical resection is the standard treatment for early esophagealcancer.5 During the past decade, outcomes with surgery haveimproved, as indicated by an increased rate of curative resection,a decreased rate of postoperative death, and better five-yearsurvival.6,7 However, the proportion of patients who survivefor five years remains low, ranging from 30 to 50 percent forthose with stage I disease, 15 to 30 percent for those withstage IIA disease, and 5 to 15 percent for those with diseasein stage IIB.5,8 Patterns of treatment failure point to theneed for better control of local and distant recurrences.9,10,11,12,13
Several phase 2 studies have indicated that preoperative treatmentwith a combination of chemotherapy and irradiation (chemoradiotherapy),followed by surgery, produces a complete response, as determinedpathologically, in 20 to 40 percent of patients; such combinationtreatment thus offers the prospect of improved survival.14 From1985 to 1988, we conducted a phase 2 study of preoperative treatmentwith radiotherapy and cisplatin in 119 patients with squamous-cellcarcinoma of the thoracic esophagus.15 In 101 of the 111 surgicallytreated patients, the resection was curative. There were eightpostoperative deaths. Pathological specimens from 24 patientscontained no visible cancer cells. The median survival was 18months.15 These promising results led the Fondation Françaisede Cancérologie Digestive and the European Organizationfor Research and Treatment of Cancer (EORTC) GastrointestinalTract Cancer Cooperative Group to initiate a prospective, multicenter,randomized trial comparing preoperative chemoradiotherapy followedby surgery with surgery alone. The main end point was overallsurvival. Secondary end points were disease-free survival andsurvival free of local disease or distant metastases.
Methods
Eligibility Criteria
Patients were included in the study if they had all of the following:invasive squamous-cell carcinoma of the thoracic esophagus;an Eastern Cooperative Oncology Group (ECOG) performance statusof 0 to 2; an age of less than 70 years; medical fitness forsurgery; and a tumor judged to be resectable, according to thepolicy of each center. Other criteria included a leukocyte countabove 3500 per cubic millimeter, a serum creatinine level ofat least 1.4 mg per deciliter (120 µmol per liter), anda platelet count above 120,000 per cubic millimeter. Writteninformed consent was required. Patients were excluded if theyhad lost more than 15 percent of their body weight or if theyhad previously undergone treatment for this disease or any othercancer except basal-cell carcinoma of the skin.
The extent of the tumor was evaluated by clinical examination,esophagography, esophagoscopy, bronchoscopy, computed tomography(CT) of the lower neck, chest, and upper abdomen, and ultrasonographyof the liver. Since endoscopic ultrasonography was not availablefor this study, we used a staging system based on the resultsof the CT scan.16 The T stage was defined by the maximal transversediameter of the esophageal tumor: less than 1 cm (T1), between1 and 3 cm (T2), and larger than 3 cm (T3). Tumors with invasionof any neighboring structure were classified as T4. The mediastinaland celiac lymph nodes were classified as N1 (invaded) if themaximal transverse diameter of these nodes was larger than 1cm; otherwise, they were classified as N0.
We included patients with stage T1N0, T1N1, T2N0, T2N1, or T3N0disease. We excluded patients with one or more of the following:a tumor located within the first 4 cm of the esophagus, metastasesin cervical lymph nodes, evidence of invasion of the bronchuson bronchoscopy, and tumor classified T3N1, T4N0, or T4N1. Thesethree stages were thought by the surgeons' panel to be usuallynot curable by surgical resection.
Treatment
Surgery
For tumors in the middle and lower parts of the mediastinum,the recommended resection procedure was a one-stage en blocesophagectomy and proximal gastrectomy via the abdominal andright thoracic routes. For tumors in the upper mediastinum,an additional cervical route was recommended. In either case,a two-field lymph-node resection was recommended. In the combined-treatmentgroup, surgery was planned two to four weeks after the lastpreoperative treatment and after the leukocyte and plateletcounts returned to normal. Curative resection was defined bythe surgeon as a macroscopically complete excision of the tumor.
Radiotherapy
The target of radiotherapy was the macroscopic tumor and enlargedlymph nodes, if any, surrounded by 5-cm proximal and distalmargins and a 2-cm radial margin. The target was extended tothe inferior cervical area in the case of tumors located abovethe carina. No attempt was made to treat systematically theanatomical mediastinum or the celiac area. The use of multiple-fieldtechniques and daily treatment of all fields were mandatory.Irradiation was delivered in two one-week courses, separatedby two weeks. During each course, five daily fractions of 3.7Gy each were delivered. The specified dose was delivered atthe intersection of the central axis of the beams, accordingto international guidelines.17 The delivered dose was 18.5 Gyper course, for a total of 37 Gy. The maximal recommended doseto the spinal cord was 25 Gy.
Chemotherapy
Cisplatin, at a dose of 80 mg per square meter of body-surfacearea, was given on an outpatient basis to patients assignedto preoperative treatment 0 to 2 days before each course ofradiotherapy; standard techniques were used for hydration andalkalization. The second dose of cisplatin was reduced by 50percent if there was a grade 1 increase in the serum creatininelevel or grade 2 neutropenia, thrombocytopenia, or both, accordingto the classification system of the World Health Organization(WHO). Treatment with the drug was discontinued if more severeacute toxic effects developed.
Pathological Analysis
Analysis of the surgical specimen included a determination ofthe histologic type of the tumor, the degree of extension ofthe tumor through the esophageal wall, whether there was nodalinvolvement, and the status of proximal and distal margins.For patients treated preoperatively, the response was definedaccording to the Tumor Regression Grade, which ranges from 1(indicating complete regression) to 5 (no change), as describedby Mandard et al.18
Follow-Up
Follow-up evaluation was performed every four months after surgeryuntil death or the end of the study period. Each evaluationincluded a clinical examination, esophagography, chest radiography,and ultrasonography of the liver. Treatment failure was definedas indicated by any morphologic evidence of tumor; only thefirst failure in a patient, which could be local, distant, orboth, was reported. Subsequent sites of involvement by tumorwere not recorded. After recurrence, the patients could be treatedby any method considered useful.
Randomization and Statistical Analysis
Patients were randomly assigned to a treatment group by a centraloffice after their eligibility was established. Randomizationwas balanced by institution, without any other type of stratification.The two treatment groups were compared with respect to base-linecharacteristics with use of the t-test for continuous variablesand the chi-square test for categorical variables. When necessary,Fisher's exact test was used. To detect an improvement in five-yearsurvival from 15 percent in the surgery-alone group to 25 percentin the combined-treatment group, with a one-sided type I errorof 0.05 and a power of 80 percent, a total of 256 deaths wouldhave to occur.19 Assuming an average follow-up of five years,the intended number of randomized patients was 320. Recruitmentwas stopped earlier than anticipated because of a slightly higherthan anticipated rate of postoperative mortality in the combined-treatmentgroup. For each end point, the probability of successful treatmentor of adverse events was estimated as a function of time bythe Kaplan–Meier method,20 and all the comparisons weremade with the log-rank test.21 Data on patients were analyzedaccording to intention-to-treat principles. Survival was calculatedfrom the date of randomization to the most recent follow-upcontact or to the date of recurrence or death and included allpatients in the study. For the analyses of disease-free survivaland time without local or distant recurrence, treatment wasconsidered to have failed at the time of surgery in patientswho did not undergo curative resection. All P values are two-sided.
Analysis of Prognostic Factors
The following variables were studied as potential prognosticfactors with respect to overall survival: age, sex, WHO performancestatus, weight loss, location of the tumor, tumor stage as determinedby CT, whether the resection was curative or palliative, andthe status of histologic margins. A Cox-model analysis was performedthat included the variables that were significant in the univariateanalysis.22 The positive predictive value of the tumor-stageclassification based on the CT scan was investigated in patientswith curative resections in the surgery-alone group.
Results
Patients
From January 1989 to June 1995, 297 patients were enrolled.Eleven patients (five in the group assigned to surgery aloneand six in the combined-treatment group) were found to be ineligible;the reasons for ineligibility were the presence of another primarycancer (in five patients), excessive weight loss (three), distantmetastasis (one), previous treatment for esophageal cancer (one),and refusal on the part of the patient (one). An additionalfour patients were lost to follow-up after randomization. Thus,a total of 282 patients (139 assigned to surgery alone and 143assigned to combined treatment) remained in the analysis. Thetwo treatment groups were similar except for a slightly higherproportion of patients with WHO performance status 1 in thecombined-treatment group (Table 1).
Table 1. Characteristics of the 282 Patients, According to Treatment Group.
Compliance with Treatment
Among the 139 patients assigned to surgery alone, 2 receivedpreoperative chemoradiotherapy; 1 of these 2 patients and 1other did not undergo resection because of progression of thedisease outside the mediastinum. Among the 143 patients assignedto combined treatment, 1 had surgery before receiving preoperativechemoradiotherapy; 2 patients did not undergo the second courseof irradiation (1 died of toxic effects and 1 had disease progression);3 patients did not undergo the second course of chemotherapybecause of toxic effects. Five patients in this group did notundergo surgery for the following reasons: disease progression(three), refusal by the patient (one), and preoperative death(one). The mean (±SD) total delivered dose of radiationwas 37±3 Gy; the mean delivered dose of cisplatin percourse was 77±11 mg per square meter. Cisplatin inducedvomiting in 37 patients and WHO grade 3 neutropenia in 3. Themedian time from the end of the preoperative treatment to surgerywas 21 days (range, 6 to 126).
Surgery
Overall, 275 patients underwent surgery. There was no differencein surgical procedures between the two groups; more than 80percent of all patients had a transthoracic resection, but resectionwas curative in more patients in the combined-treatment group(112 of 138 vs. 94 of 137, P = 0.017). During the postoperativeperiod, 36 (26.3 percent) of the patients in the surgery-alonegroup and 45 (32.6 percent) in the combined-treatment grouphad one or more severe complications (P = 0.249), mostly pneumonia,infections, and anastomotic leakage. The postoperative mortalitywas significantly higher in the combined-treatment group (17of 138, as compared with 5 of 137 in the surgery-alone group;P = 0.012), mainly because of the higher number of patientswith respiratory insufficiency (6 vs. 0) and mediastinal infectionor sepsis (7 vs. 2). The average duration of hospitalizationwas 24±20 days in both groups. There was no significantdifference in morbidity or mortality among the participatingcenters; five centers enrolled 80 percent of the patients.
Pathological Responses
After curative resection in the combined-treatment group, acomplete pathological response was noted in 29 of 112 patients(26 percent), and 20 patients (18 percent) were scored as havinga major pathological response (Table 2). Comparison of the twogroups indicated a significantly lower stage of disease afterpreoperative treatment; this was true both for the tumor (T)stage (P = 0.001) and the nodal (N) stage (P = 0.03) determinedpathologically. The number of patients with mediastinal lymph-nodemetastases was significantly lower in the combined-treatmentgroup (26 of 105 who had exploratory lymph-node dissection vs.66 of 115, P = 0.001), whereas the proportion with celiac lymph-nodeinvasion did not differ significantly between the groups (44of 115 vs. 48 of 117).
Table 2. Pathologically Determined Disease Stage after Curative Resection, According to Treatment Group.
Survival
After a median follow-up of 55.2 months, 203 patients had died.For both groups, the median survival was 18.6 months. The overallsurvival curves of the two groups did not differ significantly(relative risk of death in the combined-treatment group as comparedwith the surgery-alone group = 1.0; 95 percent confidence interval,0.7 to 1.5; P = 0.78) (Figure 1); the difference between thegroups was still nonsignificant after adjustment for the differencein the WHO performance status and inclusion of all randomizedpatients in the analysis (P = 0.65 and P = 0.75, respectively).There was a significant difference in the proportion of deathsthat were due to esophageal cancer in the two groups (87 of101 patients who had surgery alone vs. 69 of 102 patients whoreceived combined treatment, P = 0.002) (Table 3).
Figure 1. Overall Survival among Patients with Esophageal Cancer Treated with Surgery Alone or with Preoperative Chemoradiotherapy Followed by Surgery (Combined Treatment).
The vertical bars indicate 95 percent confidence intervals at three years. The numbers of deaths shown below the figure are cumulative.
Table 3. Survival and Causes of Death, According to Treatment Group.
Disease-Free Survival
Overall, 178 patients had persistent or recurrent disease. In76 patients, local control was never achieved, and among the206 patients who had curative surgery, 102 had a recurrence(41 local, 26 distant, and 35 both). Disease-free survival wassignificantly longer in the combined-treatment group (relativerisk of recurrence or death from cancer = 0.6; 95 percent confidenceinterval, 0.4 to 0.9; P = 0.003) (Figure 2).
Figure 2. Disease-free Survival among Patients with Esophageal Cancer Treated with Surgery Alone or with Preoperative Chemoradiotherapy Followed by Surgery (Combined Treatment).
The vertical bars indicate 95 percent confidence intervals at three years. The numbers of deaths shown below the figure are cumulative.
Time without Local or Distant Recurrence
The time free of local disease was significantly longer in thecombined-treatment group (relative risk of local recurrence= 0.6; 95 percent confidence interval, 0.4 to 0.9; P = 0.01),but there was no significant difference in the time to distantmetastasis (relative risk = 0.7; 95 percent confidence interval,0.4 to 1.4; P = 0.24).
Late Toxic Effects
At two years, the rates of pulmonary insufficiency, cardiacfailure, and stenosis of the esophageal anastomosis were 7.2percent, 1.4 percent, and 12.3 percent, respectively. No statisticallysignificant difference was observed between the treatment groups.
Prognostic Factors
In the univariate analysis, survival was significantly shorteramong patients with a loss of more than 5 percent of body weight(P = 0.01), a tumor whose upper part was located within 25 cmof the mandibular arch (P = 0.04), and stage N1 disease (basedon the results of CT). Curative resection was associated witha significant increase in survival. In the multivariate analysis,only location of the tumor within 25 cm of the mandibular arch(relative risk of death = 1.4; 95 percent confidence interval,1.0 to 1.9; P = 0.05), stage N1 disease (relative risk = 1.5;95 percent confidence interval, 1.1 to 2.2; P = 0.01), and palliativerather than curative resection (relative risk = 2.3; 95 percentconfidence interval, 1.7 to 3.3; P<0.001) remained statisticallysignificant.
The positive predictive value of the disease-stage classificationbased on the CT scan was 76 percent for stage T1 tumors (19tumors classified as T1 on the basis of the pathological analysisamong 25 classified as T1 on the basis of the CT scan) and 84percent for stage T3 tumors (16 of 19). For T2 lesions, it wasonly 22 percent (10 of 46); 7 tumors were classified as stageT1 and 29 as stage T3. The values for stages N0 and N1 were49 percent (36 of 73) and 75 percent (15 of 20), respectively.
Discussion
We found a significant prolongation of disease-free survivalamong patients with squamous-cell esophageal carcinoma who receivedchemoradiotherapy before resection. This gain was due mainlyto a local effect, as attested by a longer interval free oflocal disease in the combined-treatment group. Other indicatorsof efficacy were a higher rate of curative resection, clear-cutevidence of a lower disease stage after preoperative therapy,and a higher rate of major pathological responses. However,overall survival was not significantly different in the twogroups, despite a reduced rate of death due to esophageal cancerin the combined-therapy group. The similar mortality rates mayreflect excessive postoperative mortality among patients treatedpreoperatively with chemoradiotherapy.
The value of adjuvant treatment of esophageal cancer has beencalled into question by the results of several randomized trials.Preoperative irradiation,23,24,25,26 postoperative irradiation,27,28and preoperative chemotherapy29,30,31,32 have not been efficacious.Preoperative combined chemoradiotherapy has been tested in fourrandomized studies of squamous-cell cancer of the esophagus.A Scandinavian trial33 assigned 217 patients either to surgeryalone or to preoperative treatment (radiotherapy, chemotherapy,or sequential chemoradiotherapy). The postoperative mortalityin these groups was not significantly different. Patients whoreceived preoperative irradiation with or without chemotherapyhad a significant gain in survival as compared with those treatedwith surgery with or without chemotherapy. However, the smallnumber of patients in each group and the low rate of curativeresection (44 percent) make the results of that study debatable.Le Prise et al.34 randomly assigned 104 patients with squamous-cellcancer to surgery or sequential preoperative chemoradiotherapy,followed by surgery. A curative resection was performed in 84percent of the patients, and postoperative mortality was 8 percentin both groups. There were no significant differences in survival.Preliminary results of a study by Urba et al.35 in 100 patients,most (75 percent) with esophageal adenocarcinoma, suggest thatpreoperative concurrent chemoradiotherapy does not increasesurvival. In another trial,36 113 patients with adenocarcinomalocated mainly in the distal part of the esophagus and the cardiawere assigned to surgery or to preoperative concurrent chemoradiotherapyfollowed by surgery. The overall resection rate was 93 percent,and the postoperative death rates in the two groups were notsignificantly different. At three years, overall survival wassignificantly longer in the combined-treatment group (P = 0.01).
The increased number of postoperative deaths in the combined-treatmentgroup in our study could be due to deleterious effects of thehigh dose of radiation per fraction or of chemoradiotherapyon lung tissue, to immunosuppression, or to malnutrition. Inexperimental studies, a deleterious effect of high fractionaldoses of radiation on lung tissues has been described, but noincrease in the toxicity of radiation has been observed whencisplatin has been added.37,38,39 In the randomized trials discussedabove, excessive acute toxic effects on the lungs were not reportedwith doses that varied from 1.8 to 2.67 Gy per fraction. The3.7-Gy fractional dose used in our study probably had a detrimentaleffect. Furthermore, the pause between the two courses of treatmentis now known to allow repopulation of tumor cells in other anatomicallocations.40 In future studies, fractional doses in the 2-Gyrange and continuous irradiation should be used. Improvementsin chemotherapy are also possible; the combination of fluorouracilwith cisplatin and radiotherapy has shown promise for the nonsurgicalmanagement of localized disease.41
Our analysis of prognostic factors showed that the determinationthat the disease is at stage N1 on the basis of the resultsof the CT scan is a powerful indicator of prognosis. This contrastswith the apparent lack of prognostic value of a determinationof the N0 stage, suggesting that the CT scan–based detectionof minimal pathological nodal invasion is difficult. The well-establishedvalue of the quality of the surgical resection — thatis, of whether the resection is curative or not — as aprognostic factor was confirmed in our study.5,8
Preoperative chemoradiotherapy merits consideration as an adjuvanttreatment for squamous-cell esophageal cancer. Future effortsshould aim to improve the efficacy of the treatment while reducingits toxicity.
Supported by grants from the Ligue Départementale deLutte contre le Cancer du Doubs, France.
Source Information
From University Hospital J. Minjoz, Besançon (J.-F.B., G.M., J.-J.P., M.M.); University Hospital Côte de Nacre, Caen (M.G.); University Hospital C. Hurriez, Lille (J.-P.T.); University Hospital St. Antoine, Paris (E.T.); Institut Gustave Roussy, Villejuif (D.E.); University Hospital A. Morvan, Brest (P.L.); and University Hospital, Schiltigheim (J.-C.O.) — all in France, and the European Organization for Research and Treatment of Cancer Data Center, Brussels, Belgium (T.S.). Other authors were Philippe Ségol (University Hospital Côte de Nacre, Caen), Jean-Bernard Flamant (University Hospital E. Debré, Reims), Jean-Pierre Arnaud (University Hospital, Angers), Jean-Pierre Plachot (University Hospital, Amiens), Anne-Marie Mandard (Centre F. Baclesse, Caen), and Gaelle Chaillard (University Hospital J. Minjoz, Besançon).Presented in part at the 30th Annual Meeting of the American Society of Clinical Oncology, Dallas, May 14–17, 1994.
Address reprint requests to Dr. Bosset at the Radiation Oncology Department, University Hospital J. Minjoz, 25030 Besançon, CEDEX, France.
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Appendix
The following institutions of the Fondation Françaisede Cancérologie Digestive and the EORTC GastrointestinalTract Cancer Cooperative Group participated in this study: UniversityHospital J. Minjoz, Besançon; University Hospital Côtede Nacre, Caen; University Hospital C. Hurriez, Lille; UniversityHospital St. Antoine, Paris; Institut Gustave Roussy, Villejuif;University Hospital A. Morvan, Brest; University Hospital, Schiltigheim;University Hospital E. Debré, Reims; University Hospital,Angers; University Hospital, Amiens; Centre F. Baclesse, Caen;Centre Val d'Aurelle, Montpellier; and University Hospital,Dijon.
Ajani, J. A., Winter, K., Komaki, R., Kelsen, D. P., Minsky, B. D., Liao, Z., Bradley, J., Fromm, M., Hornback, D., Willett, C. G.
(2008). Phase II Randomized Trial of Two Nonoperative Regimens of Induction Chemotherapy Followed by Chemoradiation in Patients With Localized Carcinoma of the Esophagus: RTOG 0113. JCO
26: 4551-4556
[Abstract][Full Text]
Kim, M. K., Cho, K.-J., Kwon, G. Y., Park, S.-I., Kim, Y. H., Kim, J. H., Song, H.-Y., Shin, J. H., Jung, H. Y., Lee, G. H., Choi, K. D., Kim, S.-B.
(2008). Patients with ERCC1-Negative Locally Advanced Esophageal Cancers May Benefit from Preoperative Chemoradiotherapy. Clin. Cancer Res.
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