Background Uncontrolled studies suggest that a combination ofchemotherapy and radiotherapy improves the survival of patientswith esophageal adenocarcinoma. We conducted a prospective,randomized trial comparing surgery alone with combined chemotherapy,radiotherapy, and surgery.
Methods Patients assigned to multimodal therapy received twocourses of chemotherapy in weeks 1 and 6 (fluorouracil, 15 mgper kilogram of body weight daily for five days, and cisplatin,75 mg per square meter of body-surface area on day 7) and acourse of radiotherapy (40 Gy, administered in 15 fractionsover a three-week period, beginning concurrently with the firstcourse of chemotherapy), followed by surgery. The patients assignedto surgery had no preoperative therapy.
Results Of the 58 patients assigned to multimodal therapy andthe 55 assigned to surgery, 10 and 1, respectively, were withdrawnfor protocol violations. At the time of surgery, 23 of 55 patients(42 percent) treated with preoperative multimodal therapy whocould be evaluated had positive nodes or metastases, as comparedwith 45 of the 55 patients (82 percent) who underwent surgeryalone (P<0.001). Thirteen of the 52 patients (25 percent)who underwent surgery after multimodal therapy had completeresponses, as determined pathologically. The median survivalof patients assigned to multimodal therapy was 16 months, ascompared with 11 months for those assigned to surgery alone(P = 0.01). At one, two, and three years, 52, 37, and 32 percent,respectively, of patients assigned to multimodal therapy werealive, as compared with 44, 26, and 6 percent of those assignedto surgery, with the survival advantage favoring multimodaltherapy reaching significance at three years (P = 0.01).
Conclusions Multimodal treatment is superior to surgery alonefor patients with resectable adenocarcinoma of the esophagus.
During the past 20 years the rate of increase in the incidenceof adenocarcinoma of the esophagus has outstripped that of allother tumors.1,2,3,4 This dramatic change has been accompaniedby a shift in the biologic behavior of esophageal cancer towardpoorer differentiation and greater nodal involvement.5 At thetime of resection 85 to 95 percent of patients have lymph-nodeinvolvement, and after standard surgical resection fewer than10 percent survive five years.5,6 The role of more radical surgeryis controversial, and no randomized trials have been reported.Since most patients have systemic disease at presentation,7,8systemic therapy may improve the outcome.
Single-drug or multidrug chemotherapy rarely induces a completeresponse, as determined pathologically, and does not enhancesurvival.9 When patients with potentially curable cancer weretreated with radiotherapy alone, the two-year survival was only10 percent.10 Neoadjuvant therapy given before surgery may reducethe incidence of micrometastases, increase resectability, controlsystemic disease, and allow accurate assessment of the completenessof the pathological response, all of which might influence decisionson postoperative treatment. A number of studies have comparedthe response of patients to neoadjuvant therapy with the outcomein historical control patients11,12,13,14,15,16,17,18,19,20and have shown that esophageal adenocarcinoma responds to treatmentbased on fluorouracil and radiotherapy. We report a trial inwhich a combination of preoperative chemotherapy and radiotherapywas compared with surgery alone.
Methods
Patients
In May 1990, we undertook a randomized, controlled trial tocompare the outcome of multimodal treatment, consisting of twocourses of fluorouracil and cisplatin and 40 Gy of radiotherapyfollowed by surgery, with the outcome of surgery alone for esophagealadenocarcinoma. Patients who met any of the following criteriawere excluded from the study: age greater than 76 years, distantmetastases, carcinoma of the cervical esophagus requiring laryngectomy,leukocyte count of less than 3500 per cubic millimeter, plateletcount of less than 100,000 per cubic millimeter, serum creatinineconcentration above 1.4 mg per deciliter (124 µmol perliter), an Eastern Cooperative Oncology Group (ECOG) performancestatus of 3 or 4, previous chemotherapy or radiotherapy, previousmalignant condition (apart from skin cancer), coexisting diseasecontraindicating surgery, and social circumstances not conduciveto compliance with the full treatment protocol. The study wasapproved by the St. James's Hospital Ethics Committee, and informedconsent was obtained from all patients.
Preoperative Tumor Staging
The extent of the tumor was evaluated in each patient by physicalexamination, chest radiography, abdominal ultrasonography, andupper gastrointestinal endoscopy. Bronchoscopy was performedwhen indicated by symptoms, the location of the tumor, or chestradiography. Computed tomography was performed in selected patientswith equivocal findings on chest radiographs or liver ultrasonograms.Isotope bone scans were occasionally performed if indicated.
Patient Monitoring
Initially the patients were hospitalized for the duration oftreatment, but later in the study they were routinely admittedonly for chemotherapy. Many who could commute to the radiotherapyfacility received radiotherapy as outpatients. Patients wereinterviewed and examined daily during chemotherapy. The followinghematologic and biochemical studies were performed at leasttwice weekly: platelet and leukocyte counts and measurementsof hemoglobin and serum electrolytes, creatinine, bilirubin,alkaline phosphatase, and -glutamyltransferase. Arterial-bloodgas analysis and pulmonary-function tests were performed atthe outset and repeated when indicated.
Chemotherapy
Chemotherapy consisted of two courses of fluorouracil and cisplatin.Fluorouracil (15 mg per kilogram of body weight per day) wasinfused over a period of 16 hours on days 1 through 5. Afterone day of hydration with 2 liters of 0.9 percent saline, cisplatin(75 mg per square meter of body-surface area) was infused overa period of eight hours on day 7. This cycle was repeated inweek 6.
Radiotherapy
Radiotherapy was begun on the first day of the first courseof chemotherapy and given for a total of 15 days (days 1 to5, 8 to 12, and 15 to 19). All patients were treated with megavoltage-therapyunits with either 4-MV photons (Cobalt model SEM100, Fairy Engineering,or Phillips model SL75-5) or 8-MV photons (Dynaray model 10,Radiation Dynamics). The treated area extended 5 cm beyond thelongitudinal margins of the tumor, as defined by endoscopicand radiologic examination, and 2 to 3 cm beyond the radialmargins. Initially, all patients were treated with parallelopposed fields (anteroposterior and posteroanterior). The techniquewas modified in 1994 to a three-field arrangement (anterior,right-posterior, and left-posterior oblique fields) to diminishthe amount of radiation to the spinal cord. With the parallelopposed fields, a midline dose of 40 Gy in 15 fractions wasprescribed (2.67 Gy per fraction). With the three-field technique,a dose of 40 Gy ±10 percent in 15 fractions was deliveredto the entire treatment volume (2.67 Gy per fraction) with acomputerized treatment-planning system (AECL/Theratronics Therplan).There was no correction for transmission of radiation to thelungs during either treatment technique.
Surgery
Surgery was carried out eight weeks after the beginning of treatmentbut was delayed if the leukocyte count was less than 2500 percubic millimeter or the platelet count was less than 100,000per cubic millimeter. Five operative approaches were used. Tumorsof the cardia were resected through an approach involving theabdomen and the left side of the chest. In selected patientstotal gastrectomy and distal esophagectomy were performed throughan abdominal approach. Tumors of the lower third of the esophaguswere resected by the Lewis–Tanner operation, and tumorsof the middle third by a three-stage operation in which theesophagus was mobilized in the right side of the chest and theanastomosis performed in the neck. In patients with poor respiratoryreserve the transhiatal approach was used. Intestinal continuitywas restored by placing the stomach in the posterior mediastinum.A single layer of interrupted linen sutures was used for theanastomosis. Patients were extubated in the operating room orthe recovery room, returned to the intensive care unit for fourdays on average, and were usually discharged less than threeweeks after surgery.
Treatment-Induced Toxicity
A toxic reaction was defined according to the criteria of theWorld Health Organization (WHO).21 With the introduction ofondansetron early in the study for the treatment of cisplatin-inducednausea, all patients were treated prophylactically before andduring the cisplatin infusion. If the leukocyte count fell below2500 per cubic millimeter or the platelet count fell below 100,000per cubic millimeter, chemotherapy was withheld or radiotherapyor surgery was delayed until the count recovered. An interruptionin the treatment regimen of more than two weeks was considereda major deviation from the protocol.
Pathological Stage
The tumor stage was defined according to the classificationof the American Joint Committee on Cancer.22 The stage of thecancer was defined in each patient according to the locationand extent of any residual disease after chemotherapy and radiotherapy.The absence of residual tumor in the resected specimen, includingthe lymph nodes, was defined as a complete pathological response(stage 0). The tumor was classified as stage 1 if there wasresidual tumor in the mucosa or submucosa and the lymph nodeswere free of tumor. If residual deposits involved the muscularispropria or adventitia but the lymph nodes were free of tumor,the disease was classified as stage 2a. If there was no residualtumor in the esophagus but a tumor deposit was found in thenodes, it was classified as stage 2b. If tumor breached theesophageal wall and the lymph nodes also contained tumor, itwas defined as stage 3. Stage 4 disease was defined as metastasesextending beyond the regional nodes.
Statistical Analysis
Survival was measured from the date of randomization to thedate of death or most recent follow-up visit. Estimates of mediansurvival are based on the Kaplan–Meier method; group comparisonsof survival involving individual variables were based on thelog-rank test. For categorical data, group comparisons werebased on the chi-square or Fisher's exact test. Freedman's method23was used to estimate the sample size required to detect an improvementin two-year survival of 20 percentage points after chemotherapyand radiotherapy over a base-line survival rate of 23 percentfor surgery alone — the survival rate for adenocarcinomain the facility at the commencement of the study. With an alphaerror of 5 percent and a power of 80 percent, the number ofpatients required in the study was estimated to be 190. Earlyindications of a clinically relevant difference between treatmentssuggested that an interim analysis should be undertaken. Thetrial was closed six years after it began because a statisticallysignificant difference between the groups was found.
Results
Demographic Data
Between May 1990 and September 1995, 113 patients with adenocarcinomaof the esophagus were recruited. Fifty-eight patients were randomlyassigned to receive chemotherapy and radiotherapy before surgery,and 55 were assigned to receive surgery alone. The characteristicsof the patients in the two groups were similar before treatment(Table 1). While the trial was in progress an additional 45patients underwent resection but did not undergo randomizationfor the following reasons: 14 were older than 76 years, 6 haddistant metastases, 3 had uncertain histologic findings, 2 hadcomplete dysphagia, 2 had previously undergone complex esophagealsurgery, 1 required laryngectomy, 1 had recurrent tumor, and10 chose surgery or chemoradiotherapy; in 6 the reason for notundergoing randomization was not documented.
Table 1. Characteristics of the Two Treatment Groups at Base Line.
The median length of follow-up for all patients was 10 months(range, 0.1 to 59). The median follow-up for patients who diedwas 7.5 months (range, 0.1 to 37), whereas for patients whowere still alive as of the most recent follow-up visit it was18 months (range, 1 to 59). The median follow-up was 10 months(range, 0.1 to 59) for patients assigned to multimodal therapyand 8 months (range, 0.1 to 38) for patients assigned to surgery.
Protocol Violations
The chemoradiotherapy protocol was violated in 10 instances,and the surgery protocol in 1. Table 2 lists the protocol violations.
Table 2. Protocol Violations Leading to the Withdrawal of 11 Patients from the Study.
Treatment-Related Morbidity
Treatment-related toxicity was low, and the regimen was welltolerated. Six patients in the multimodal group (10 percent)had grade III toxic reactions, as defined by WHO criteria (threegastrointestinal, two hematologic, and one cardiac); two patientshad grade IV toxic reactions (one cardiac and one gastrointestinal);and one patient had a fatal hemorrhage from the tumor bed duringtreatment.
Treatment was delayed in two patients because of leukopenia,which resolved within two weeks. Two patients whose ECOG performancestatus deteriorated did not undergo surgery and were includedin the group with grade III gastrointestinal toxic reactions.
Postoperative Complications
Respiratory complications occurred in 28 patients in the multimodalgroup and 32 patients in the surgery group. Fourteen cardiacevents occurred in the chemoradiotherapy group, as comparedwith 13 in the surgery group. There were two anastomotic leaks,one recurrent nerve palsy, and one chylothorax in each group;one patient in the multimodal group had severe postoperativepancreatitis, and one patient in the surgery group had a postoperativehemorrhage requiring a second operation.
Mortality during Hospitalization
Seven patients died in the hospital, for a 90-day in-hospitalmortality rate of 6 percent. Of the five patients in the multimodalgroup who died during hospitalization, three had completed theprotocol. One died of postoperative hemorrhage, one of chylothorax,and one of an anastomotic leak. Two patients did not completethe multimodal protocol. One died preoperatively of a hemorrhagefrom the tumor bed, and one with complete dysphagia who hadsurgery before completing chemoradiotherapy died postoperativelyof sepsis.
Two patients assigned to surgery died of sepsis in the hospital.A chylothorax developed in one patient within three weeks aftersurgery, and an iatrogenic perforation occurred in the secondafter attempted dilatation of the tumor.
Response to Chemoradiotherapy
At the time of surgery, only 42 percent (23 of 55) of the patientsin the multimodal group who could be evaluated had positivelymph nodes or metastases, as compared with 82 percent (45 of55) of the patients in the surgery group (P<0.001) (Table 3).A complete pathological response occurred in 13 of the 52patients in the multimodal group (25 percent) who underwentresection, including 1 patient who died and had no viable tumorat autopsy and 1 patient who only had high-grade dysplasia inthe tumor bed. In two patients overt metastases developed duringtreatment.
Table 3. Pathological Stage of the Tumor at the End of Treatment Actually Received.
Survival
A comparison of the two treatment groups based on the intention-to-treatprinciple showed a survival advantage for the multimodal group(median survival, 16 months, as compared with 11 months in thegroup treated with surgery alone; P = 0.01) (Figure 1). Whenthe two groups were compared on the basis of the treatment actuallyreceived, the median survival was 32 months in the multimodalgroup and 11 months in the surgery group (P =0.001) (Figure 2).When survival at one, two, and three years was calculatedon the basis of the intention to treat, 52, 37, and 32 percentof the patients assigned to multimodal therapy were alive, ascompared with 44, 26, and 6 percent of those assigned to surgeryalone; the difference reached statistical significance at threeyears (P =0.01). The survival rates at three years accordingto the treatment actually received were 37 percent (10 of 27patients) in the multimodal group and 7 percent (2 of 30) inthe surgery group (P =0.006) (Table 4).
Table 4. Survival Three Years after Treatment According to the Intention to Treat and According to the Treatment Actually Received.
Thirteen patients in the multimodal group had a complete pathologicalresponse. One died during treatment. A 72-year-old woman diedfive months after surgery; there was no autopsy, but her familyphysician attributed her death to tumor. The remaining 11 werealive and tumor-free 43, 36, 27, 21, 21, 16, 16, 5, 4, 4, and2 months after resection.
Nineteen patients in the multimodal group had residual diseaseconfined to the esophagus. As of this writing the median survivalfor this subgroup had not been reached: 11 were alive, nonewith overt disease, after a median follow-up of 37 months (range,10 to 59). Eight had died, five of proven and one of suspectedrecurrence, after a median survival of 8 months (range, 3 to32). Thirteen had stage 3 disease, four of whom were alive at54, 43, 18, and 4 months, whereas nine had died after a medianof 7 months (range, 2 to 11), all but one of recurrent disease.
Ten patients assigned to surgery had disease confined to theesophagus and had a median survival of 14 months (range, 0.3to 38). Three of these patients were alive at 25, 29, and 38months, whereas seven patients had died after a median of 11months (range, 0.3 to 23). Thirty-eight patients had stage 3disease; 9 of them were alive after a median follow-up of 5months (range, 1 to 24), whereas 29 had died after a medianof 10 months (range, 0.1 to 37).
Discussion
In this prospective, randomized trial we compared multimodaltherapy with surgery alone for esophageal adenocarcinoma. Wefound that 25 percent of the patients assigned to multimodaltherapy had a complete pathological response after resectionand 32 percent were alive at three years, whereas only 6 percentof patients treated with surgery alone lived for three years.These results support the findings of nonrandomized studiesthat have shown a complete pathological response in approximately20 percent of patients treated with multimodal therapy13,14,17,18,19,20and a survival advantage over historical control patients whohad surgery only.
Many trials of multimodal therapy have pooled adenocarcinomasand squamous-cell tumors on the assumption that the two havea similar response to treatment. This assumption is unwarranted,because patients with adenocarcinomas have a higher incidenceof lymph-node involvement (85 to 95 percent, as compared with50 to 60 percent for those with squamous-cell carcinomas) andappear to be less sensitive to chemoradiotherapy.13 In one randomizedtrial24 of 100 patients, the 75 with adenocarcinoma were randomlyassigned to chemotherapy, radiotherapy, and transhiatal resectionor to resection alone. There was no difference in the estimatedtwo-year survival between the two groups. This result may reflectthe administration of a lower dose of fluorouracil than we usedand a difference in attrition rates between the groups, sincethe survival difference in our study did not become significantuntil the third year.
The relative contributions of chemotherapy, radiotherapy, andsurgery to the survival advantage in the multimodal group areunclear. Herskovic et al. compared chemotherapy and radiotherapywith radiotherapy alone in 121 patients, all but 15 of whomhad squamous-cell carcinoma.10 Thirty-eight percent of the patientsin the multimodal group survived two years. Perhaps only patientswith residual disease in the esophageal wall or local nodesbenefit from resection. Unfortunately, current imaging methodscannot distinguish these patients from those with a completepathological response.25 In our study the omission of surgerywould have left 75 percent of the patients in the multimodalgroup with residual disease, which in 19 cases (33 percent)appeared to be confined to the esophagus. In these patients,the residual tumor would probably have progressed. A molecularmarker that reliably predicts response would greatly facilitatethe process of selecting suitable candidates for surgery. Theexpression of epidermal growth factor receptor and that of proliferating-cellnuclear antigen have shown potential as markers in patientswith squamous-cell carcinoma,26 and the expression of c-erbB-2 may have a role in patients with adenocarcinoma.27
It is unclear whether the survival advantage in the multimodalgroup at three years will persist. Leichman et al. reportedon a trial using cisplatin, fluorouracil, and 30 Gy of concurrentlyadministered radiotherapy.28 Fifteen of 21 treated patientswith squamous-cell carcinoma subsequently underwent resection,of whom 5 had complete pathological responses. All those withresponses subsequently died of distant metastases at 30 to 60months.
The chemoradiotherapy regimen was well tolerated, and therewere few toxic reactions. Ten patients were withdrawn from multimodaltherapy because of protocol violations. Two of these patientshad a deterioration in ECOG performance status that was attributedto severe cisplatin-induced nausea, but the introduction ofondansetron virtually eliminated such nausea. One patient inwhom complete dysphagia developed was withdrawn from the trial,but the current approach to such patients includes insertionof a stent and continuation of treatment. There were only twoinstances, both due to leukopenia, in which treatment or surgeryhad to be postponed because of side effects. The administrationof colony-stimulating factor should help minimize the delayin such cases. The side effects of the preoperative treatmentwere severe in six patients (10 percent), life-threatening intwo patients (3 percent), and fatal in one patient (2 percent);these results compare favorably with those in other recent reports.11,12,13,14,15,16,17,18,19,20
In conclusion, multimodal therapy followed by surgery providesa significant survival advantage over surgery alone at threeyears for patients with adenocarcinoma of the esophagus. Although17 percent of the patients in the multimodal group were withdrawnbecause of protocol violations, direct treatment-related toxiceffects were minimal. The evidence suggests that multimodaltherapy should be considered in all patients with tumor confinedto the esophagus and draining lymph nodes.
Source Information
From the Departments of Surgery (T.N.W., T.P.J.H.) and Gastroenterology (N.N., N.K.), St. James's Hospital; the Department of Radiotherapy, St. Luke's Hospital (D.H.); and the Departments of Community Health and Statistics, Trinity College (A.K.) — all in Dublin, Ireland.
Address reprint requests to Dr. Walsh at the Department of Surgery, Beaumont Hospital, Dublin 9, Ireland.
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49: 534-539
[Abstract][Full Text]
A correction has been published: N Engl J Med 1999;341(5):384.
-glutamyltransferase. Arterial-blood gas analysis and pulmonary-function tests were performed at the outset and repeated when indicated. 
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