Chemotherapy Followed by Surgery Compared with Surgery Alone for Localized Esophageal Cancer
David P. Kelsen, M.D., Robert Ginsberg, M.D., Thomas F. Pajak, Ph.D., Daniel G. Sheahan, M.B., Leonard Gunderson, M.D., Joanne Mortimer, M.D., Norman Estes, M.D., Daniel G. Haller, M.D., Jaffer Ajani, M.D., Walter Kocha, M.D., Bruce D. Minsky, M.D., and Jack A. Roth, M.D.
Background We performed a multi-institutional randomized trialcomparing preoperative chemotherapy followed by surgery withsurgery alone for patients with local and operable esophagealcancer.
Methods Preoperative chemotherapy for patients randomly assignedto the chemotherapy group included three cycles of cisplatinand fluorouracil. Surgery was performed two to four weeks afterthe completion of the third cycle; patients also received twoadditional cycles of chemotherapy after the operation. Patientsrandomly assigned to the immediate-surgery group underwent thesame surgical procedure. The main end point was overall survival.
Results Of the 440 eligible patients with adequate data, 213were assigned to receive preoperative chemotherapy and 227 toundergo immediate surgery. After a median possible study timeof 55.4 months, there were no significant differences betweenthe two groups in median survival: 14.9 months for the patientswho received preoperative chemotherapy and 16.1 months for thosewho underwent immediate surgery (P=0.53). At one year, the survivalrate was 59 percent for those who received chemotherapy and60 percent for those who had surgery alone; at two years, survivalwas 35 percent and 37 percent, respectively. The toxic effectsof chemotherapy were tolerable, and the addition of chemotherapydid not appear to increase the morbidity or mortality associatedwith surgery. There were no differences in survival betweenpatients with squamous-cell carcinoma and those with adenocarcinoma.Weight loss was a significant predictor of poor outcome (P=0.03).With the addition of chemotherapy, there was no change in therate of recurrence at locoregional or distant sites.
Conclusions Preoperative chemotherapy with a combination ofcisplatin and fluorouracil did not improve overall survivalamong patients with epidermoid cancer or adenocarcinoma of theesophagus.
Esophageal carcinoma is an aggressive disease with a poor prognosis.For patients with stage 1, 2, or 3 carcinomas, surgery aloneremains one standard of care. Another approach, treatment withradiation plus concurrent chemotherapy, has been shown to besuperior to radiation alone.1,2 Chemotherapy plus radiationbut without surgery has not yet been compared in a prospectivetrial with surgery alone.
Because of the high rates of distant and locoregional failure,there is intense interest in combining regional therapy (suchas surgery or radiation) with systemic therapy. In previousstudies, chemotherapy had at least moderate effectiveness intreating metastatic disease.3 These results led to combined-therapyapproaches to treating patients with localized tumors.4
By 1989, research data were sufficient to warrant a study ofsurgery alone as compared with surgery after chemotherapy. Becauseadenocarcinoma of the esophagus has become increasingly common,our trial included patients with either adenocarcinoma or epidermoidcancer of the esophagus.5
Methods
This study involved investigators from the Radiation TherapyOncology Group (the coordinating group), the Cancer and AcuteLeukemia Group B, the Southwest Oncology Group, and the EasternCooperative Oncology Group. The primary objective was to comparesurgery alone with preoperative and postoperative chemotherapyplus surgery. The primary end point was overall survival.
Eligibility requirements included the presence of confirmedepidermoid cancer or adenocarcinoma of the esophagus, includingthe gastroesophageal junction, with or without metastases inlocal lymph nodes and clinically limited to the locoregionalarea (tumor stage 1, 2, or 3; any nodal stage; and no metastasis[M0] in the tumor–node–metastasis [TNM] classification;carcinoma stage, 1 to 3). All patients were at least 18 yearsof age; had adequate hepatic, renal, and bone marrow reserve;and could tolerate the planned surgical procedure. Patientswere ineligible if they had cervical esophageal tumors (upperborder, <18 cm from the incisor teeth) or supraclavicularor other distant metastases (T4 tumors) or if they had previouslyundergone treatment or had previously had another primary cancer.
The pretreatment evaluation included a complete medical historyand physical examination, complete blood count and plateletcount, biochemical screening, radiography of the chest, barium-contrastradiography of the upper gastrointestinal tract, computed tomographyof the abdomen and chest, and electrocardiography. Bronchoscopywas performed for tumors in the upper third of the esophagus.Endoscopic ultrasonography was encouraged, but not required.
The randomization scheme described by Zelen6 was used with twostratification variables: weight loss (<10 percent or 10percent of body weight) and cell type as determined by histologicexamination (adenocarcinoma or epidermoid cancer). Patientswere randomly assigned either to undergo an immediate operationor to receive three cycles of chemotherapy with a combinationof cisplatin and fluorouracil before the operation. Patientswith stable disease or disease that responded to chemotherapyand in whom an R0 resection was accomplished (all margins deemedfree of tumor by microscopical examination) were also to receivetwo cycles of chemotherapy after surgery.
Surgery
Patients who were randomly assigned to undergo only surgeryunderwent the operation immediately. The same operation wasperformed after preoperative chemotherapy in the other patients.The following surgical procedures were considered acceptable:an Ivor–Lewis esophagogastrectomy with a high intrathoracicanastomosis above the level of the azygos vein, a subtotal thoracicesophagectomy by means of a left thoracoabdominal incision withan anastomosis above the aortic arch, or a complete thoracicesophagectomy. Restoration of continuity by gastric–esophagealanastomosis or colonic interposition with a cervical anastomosiswas acceptable. Transhiatal esophagectomy was acceptable onlyfor lesions located below the carina. The proximal and distalmargins had to be at least 2 cm below the gross tumor. Assessmentof the margin by examination of a frozen section before completionof the operation was strongly recommended.
At the time of the esophagectomy, tissue from the lymph nodeswas sampled. Removal of all accessible lymph nodes was stronglyrecommended to allow complete nodal staging. It was also stronglyrecommended that participating surgeons perform at least fouresophageal resections yearly.
Resections were classified as curative when all gross tumortissue was removed and microscopical examination revealed allmargins to be free of tumor (R0). Resections were consideredpalliative either when microscopical examination revealed positivemargins (R1; a positive margin was defined as tumor tissue ator less than 1 mm from the radial [deep], proximal, or distalmargins) or when there was residual local (but not distant)gross disease (R2).
Chemotherapy
Patients assigned to chemotherapy received three cycles of cisplatinand fluorouracil before surgery. Cisplatin, at a dose of 100mg per square meter of body-surface area, was given as a rapidintravenous infusion after prehydration on day 1. Immediatelythereafter, fluorouracil was administered at a dose of 1000mg per square meter as a continuous infusion from day 1 throughday 5 (120 hours) of each cycle. The cycle was repeated beginningon days 29 and 58. Surgery was performed two to four weeks afterchemotherapy. For patients with disease that was stable or responsiveto treatment, postoperative chemotherapy was begun within twoto six weeks after the operation. Each cycle of postoperativechemotherapy was the same as those described above, except thatthe cisplatin dose was 75 mg per square meter. A detailed scheduleof dose reduction was prescribed. Patients with progressivedisease at the primary site before surgery were not to receivepostoperative chemotherapy. Surgical intervention could be performedat any time before the operation was scheduled if a repeatedbarium-contrast study confirmed the presence of progressivedisease at the primary site, without distant metastases.
Radiation therapy was not part of the treatment plan. However,patients in whom there was a positive margin on microscopicalexamination, residual gross locoregional disease, or recurrenceat a later date could receive radiation therapy at the discretionof the investigator. For this reason, a detailed plan of radiationtherapy was included in the study protocol.
Statistical Analysis
The study was originally designed for patients with squamous-cellcarcinoma. It was modified after 18 months to include patientswith adenocarcinoma. A test of differences in outcome betweenthe two cell types was also added.
The primary end point was overall survival. Secondary end pointsincluded disease-free survival, differences in survival accordingto cell type, effects of chemotherapy on morbidity and mortalityassociated with surgery, and patterns of first failures of treatment.In calculating the sample size needed to test for a differencein survival, two assumptions were made. Survival times wereassumed to be distributed exponentially, without a differencein survival according to cell type. For patients assigned tosurgery alone, the projected median survival was 12.5 months.The expected rate of response to chemotherapy was 50 percent,and patients assigned to both surgery and chemotherapy wereprojected to have a median survival of 17.3 months (a 38 percentincrease in median survival as compared with survival with surgeryalone). With a P value of 0.05 indicating statistical significance(by one-sided analysis) and a statistical power of 90 percent,the accrual required to detect the hypothesized difference,regardless of cell type, was 444 patients who could be evaluated.If there was a true difference in survival according to celltype (for example, better survival in cases of adenocarcinomathan in cases of epidermoid cancer), the power to detect a 38percent increase in median survival with 444 patients wouldbe reduced to 87.8 percent. This sample size also gave the studya statistical power of approximately 80 percent to evaluatedifferences in survival between patients with adenocarcinomaand those with epidermoid cancer.
Interim analyses were planned and were performed when 50 percent,75 percent, and 100 percent of the required sample had beenenrolled. An independent data monitoring committee reviewedthe results of the interim evaluations. O'Brien–Flemingcriteria for early discontinuation of the trial7 were incorporatedinto the study design, but they were not satisfied at any ofthe interim evaluations. Informed consent was obtained fromall patients before they entered the study.
Characteristics of the patients and treatments were comparedby Pearson's chi-square test for discrete data and by the Wilcoxontest for continuous data.8 All statistical comparisons weremade with two-tailed tests. Disease-free survival and overallsurvival were estimated according to the Kaplan–Meiermethod.9 For measures of overall survival, the comparisons wereperformed with the log-rank test.10 Because of the differencein the timing of the surgery in the two groups, a modificationof the log-rank procedure was used to compare differences indisease-free survival.11 Data on cumulative incidence were usedto estimate the time to locoregional failure and the time todistant metastases.12 The sampling test proposed by Gray wasused to compare the treatment groups.13 The differences in overallsurvival between the two treatment groups were tested by theCox proportional-hazards model.14
Results
Characteristics of the Patients
From August 1990 until December 1995, a total of 467 patientsat 123 institutions were registered (Table 1). Twenty-threepatients were ineligible, and for four eligible patients therewere no follow-up data after registration. Of the patients receivingchemotherapy, 213 of 233 were eligible and had adequate follow-upinformation. Similarly, of patients having only surgery, 227of 234 were eligible. All the data received and processed throughJune 10, 1998, were included in the analyses. The median possibleduration of participation in the study was 55.4 months (range,29.5 to 94.1). When the analysis was restricted to survivingpatients, the median duration of follow-up was 46.5 months.
Table 1. Patient Characteristics According to Treatment Group and Histologic Subtype.
The two treatment groups were well balanced with respect tomajor prognostic factors. Adenocarcinoma was the predominantcell type. Eighty-eight percent of the patients with adenocarcinomawere white men. By contrast, 68 of 71 black patients had epidermoidcarcinoma. These data support epidemiologic studies indicatingthat the incidence of adenocarcinoma is rapidly increasing inwhite men. Substantial weight loss was seen more frequentlyin cases of epidermoid cancer than in cases of adenocarcinoma.
Delivery of Planned Chemotherapy
Of the 204 patients assigned to preoperative chemotherapy forwhom data on chemotherapy were adequate, 144 (71 percent) receivedall three cycles (Table 2). Overall, 83 percent of the patientswho received preoperative chemotherapy completed at least twocycles. The most common reasons for the completion of fewerthan three cycles were a decision by the patient or by the physician,progression of disease, and death.
Table 2. Ability to Deliver Planned Dose of Chemotherapy.
The clinical response to chemotherapy was assessed by barium-contrastradiography of the esophagus. Responses were scored as completeor partial. A minor improvement or a lack of change was notconsidered a response. Seven percent of the patients had completeclinical regression and 12 percent had partial clinical regression.Complete responses (T0N0M0) as assessed by pathological studywere found in 2.5 percent (5 of 202) of patients who receivedat least one cycle of chemotherapy.
After chemotherapy, 133 patients underwent potentially curativeresections (R0). Patients whose disease responded to treatmentand who were undergoing curative resections were to receivetwo postoperative cycles of chemotherapy. However, only 52 percentreceived at least one cycle, and only 38 percent received bothcycles. The chief reason for omitting postoperative chemotherapywas choice on the part of the physician or patient.
The major adverse effects of chemotherapy were neutropenia andmucositis (grade 3 toxicity in 29 percent and 25 percent ofthe patients, respectively). Of the patients who received chemotherapy,five (2 percent) died of causes related to treatment; four ofthem died of infection while they had neutropenia.
Outcome of Surgery
The median time from registration to operation was 9 days forthe group undergoing only surgery and 93 days for the groupundergoing chemotherapy before surgery. Of the latter group,62 percent had a potentially curative operation (R0); in thosewho underwent an immediate operation, residual disease was gradedas absent (R0) in 59 percent (Table 3). The difference betweenthese rates was not significant. However, the presence of apositive margin (R1) on microscopical examination was significantlymore likely in patients who underwent only surgery (15 percent)than in those who received preoperative chemotherapy (4 percent,P=0.001).
Table 3. Surgical Outcome and Mortality and Morbidity Associated with Surgery.
Fewer patients in both treatment groups died during surgerythan had been anticipated (Table 3). Of the patients who receivedchemotherapy, 10 (6 percent), as compared with 13 (6 percent)of the patients who underwent only surgery, died postoperatively.Six percent of the surgery-only group and 7 percent of the chemotherapygroup died as a result of treatment (P=0.33), either chemotherapyor surgery.
Overall and Disease-Free Survival
In an intention-to-treat survival analysis of all registeredpatients, the median duration of survival for patients who hadchemotherapy and surgery was 14.9 months, whereas for thosewho had only surgery it was 16.1 months (P=0.53 by the log-ranktest; P=0.49 by Cox proportional-hazards analysis, with a relativerisk of death of 1.07 in the chemotherapy group; 95 percentconfidence interval, 0.87 to 1.32) (Figure 1). Survival at oneyear was 59 percent for those who received chemotherapy, and60 percent for those who had surgery alone; at two years, survivalwas 35 percent and 37 percent, respectively; and at three yearsit was 23 percent and 26 percent. Similar results were obtainedin an analysis including all patients who could be evaluated(P=0.74 by the log-rank test; P=0.65 by Cox proportional-hazardsanalysis, with a relative risk of death of 1.04 in the chemotherapygroup; 95 percent confidence interval, 0.84 to 1.29). When onlythe patients who could be evaluated were considered, there wasalso no significant difference between the two groups in disease-freesurvival (P=0.50 by the modified log-rank test) (Figure 2).
Figure 1. Overall Survival of All Registered Patients.
The distribution curves represent the results of an intention-to-treat survival analysis involving all registered patients. Patients who received chemotherapy before surgery had a median survival of 14.9 months; in comparison, patients who had only surgery had a median survival of 16.1 months (P=0.53 by the log-rank test). Of the 233 patients receiving preoperative chemotherapy, 180 died; of the 234 not receiving it, 173 died.
Figure 2. Disease-free Survival of Eligible Patients.
A landmark analysis was performed six months after randomization to adjust for the difference in the timing of surgery according to treatment group. Disease-free survival for all patients who could be evaluated did not differ significantly between the two groups (P=0.50 by Sposto's modification of the log-rank test11). Of the 213 eligible patients receiving preoperative chemotherapy, 181 died; of the 227 not receiving it, 193 died.
In a separate analysis, survival was assessed for patients withsquamous-cell carcinoma and those with adenocarcinoma. Whenthe two treatment groups were combined for each of these histologicsubtypes and the subtypes were compared, there was no differencein outcome between patients with adenocarcinoma and those withepidermoid cancer. Substantial weight loss was a predictor ofpoor outcome. Patients who lost more than 10 percent of theirbody weight were significantly more likely to die (P=0.03 bylog-rank test). When the Cox model was used to adjust for thesetwo stratifying variables (weight loss and histologic type),the P value was 0.46. Among patients whose resection was curative,there was no significant difference in survival between thosewho did and those who did not undergo chemotherapy (median survival,27.4 and 25 months, respectively).
Patterns of Failure
When the analysis was restricted to patients whose resectionwas curative, the frequency of first failures of therapy ata distant site of disease was slightly higher in those who underwentimmediate surgery than in those who received preoperative chemotherapy(50 percent vs. 41 percent) (Table 4). Locoregional failurewas equally common in patients who received preoperative chemotherapyand those who did not.
This large-scale trial of one of the most common combinationsof chemotherapeutic agents used in the treatment of esophagealcancer failed to show that preoperative chemotherapy has anysignificant benefit when compared with surgery alone. The overallrate of clinical response to preoperative chemotherapy was only19 percent, but chemotherapeutic regimens with similar activityin treating advanced disease in other solid-tumor cancers, suchas colon cancer, have resulted in significant improvements inthe rate of cure when used in an adjuvant setting.15 In ourstudy, chemotherapy was reasonably well tolerated, no unusualadverse effects were seen, and there was no significant increasein operative morbidity and mortality. However, with the additionof chemotherapy there also was no change in survival. Thereare several possible explanations for this result. The firstis that the regimen of chemotherapy that we chose was unableto destroy residual regional and micrometastatic disease. However,this explanation is at variance with data from a 1992 trial1of an almost identical chemotherapeutic regimen used in conjunctionwith radiation therapy. That study evaluated 121 patients withesophageal cancer who were randomly assigned to receive a cisplatin–fluorouracilcombination plus 5000 cGy of radiation or 6400 cGy of radiationalone. A significant survival advantage was observed in patientsgiven adjuvant chemotherapy. Most patients in that trial hadepidermoid carcinoma, but a subsequent report from the sameinvestigators included additional patients with adenocarcinomawho were also assigned to receive the experimental therapy.2By contrast, in our trial, overall survival was unchanged bychemotherapy.
A more recent trial also investigated whether the addition ofchemotherapy to surgery improves outcome. In this study of 160patients with epidermoid carcinoma of the esophagus, cisplatin–etoposidechemotherapy for two to four cycles followed by a transhiatalesophagectomy was compared with transhiatal esophagectomy alone.16A significant difference between the two regimens was noted:the median survival for patients who received combined chemotherapyand surgery was 18.5 months, as compared with 11 months forthose who underwent surgery alone (P=0.002). Another recentstudy found that patients undergoing chemotherapy and irradiationplus surgery had a survival advantage, as well as a significantdecrease in failures at distant sites, as compared with patientsundergoing surgery alone.17
A second possible explanation for our negative result is thatchemotherapy is an effective treatment, but inadequate amountsof cisplatin and fluorouracil were given. In our trial, onlytwo thirds of the patients received all three planned cyclesof preoperative chemotherapy, and only a small group of patientsreceived any postoperative treatment. This experience, however,is not substantially different from that of the previous trial.1,2
A third possibility is that because the earlier studies involvedfewer patients than the current study, the effect of systemictherapy (cisplatin–fluorouracil) used in conjunction witha regional treatment was overestimated. The study by Herskovicet al. showed significant differences at an interim analysis,but only 121 patients could be evaluated.1 The more recent trialreported by Walsh et al. also had a small number of patientswho could be evaluated (113).17 A similar approach in anotherrecent U.S. study showed a strong trend toward improved outcomefor patients receiving combined therapy. However, each groupincluded only 50 patients, and the trial has not yet clearlyshown statistically significant differences.18 Also recently,investigators in France treated 202 patients with epidermoidcancer of the esophagus with hyperfractionated radiation pluscisplatin followed by surgery or with surgery alone.19 A differencein the pattern of recurrence was noted; however, perhaps becausepostoperative mortality among patients receiving the combinedtherapy was high, there were no overall differences in outcomebetween the two groups. In another trial, Le Prise and colleaguescompared a combination of chemotherapy and radiation therapyfollowed by surgery with surgery alone in 86 patients with epidermoidcancer of the esophagus.20 There were no significant differencesin outcome. Finally, as noted above, the positive results reportedby Kok et al. were obtained in a trial that included 148 patientswho could be evaluated.16
Because of these conflicting data, the role of preoperativechemotherapy and radiation therapy or preoperative chemotherapyin the treatment of esophageal cancer remains controversial.In addition to the differences between our trial and the studyby Kok et al.16 (which used different chemotherapeutic regimens),the four chemotherapy–radiation studies summarized abovealso differ from one another. In the two negative trials, byBosset et al. and Le Prise et al., which involved only patientswith squamous-cell carcinoma, chemotherapy and radiation weregiven sequentially rather than concurrently.19,20 In the twopositive (or trending toward positive) trials, by Walsh et al.and Urba et al., involving primarily patients with adenocarcinoma,chemotherapy and radiation were given concurrently.17,18 Therewere also differences in the fractionation and total dose ofradiation. A new national trial will compare, on a large scale,preoperative chemotherapy plus concurrent irradiation with surgeryalone.
In summary, preoperative chemotherapy with cisplatin and fluorouracil,as used in this study, failed to improve overall survival. Surgeryalone remains the standard of care for patients with locoregionalesophageal cancer. Improving systemic therapy remains a highpriority. In this regard, the recent identification of paclitaxelas a highly active agent in esophageal cancer has led to investigationalphase 1 and phase 2 trials of combined therapy and combinationchemotherapy for patients with esophageal cancer.21
Supported in part by grants (CA 21661, CA 32115, and CA 37422)from the National Cancer Institute.
We are indebted to Adrienne Scodary, Brian Berkey, and KathleenParkhurst for their expert assistance in the preparation ofthe manuscript.
Source Information
From Memorial Sloan-Kettering Cancer Center, New York (D.P.K., R.G., B.D.M.); the Radiation Therapy Oncology Group Statistical Office, Philadelphia (T.F.P.); the University of Pittsburgh, Pittsburgh (D.G.S.); the Mayo Clinic, Rochester, Minn. (L.G.); Washington University, St. Louis (J.M.); the University of Kansas, Lawrence (N.E.); the University of Pennsylvania, Philadelphia (D.G.H.); M.D. Anderson Cancer Center, Houston (J.A., J.A.R.); and the University of Western Ontario, London, Canada (W.K.). Presented in part at the 1997 Meeting of the American Society of Clinical Oncology, Denver, May 17–20, 1997.
Address reprint requests to Dr. Kelsen at the Department of Medicine, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
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Treatment of Esophageal Cancer
Wright C. D., Fink U., Stein H. J., Fleeth J., Begemann F., Chang A. Y., Kelsen D., Pajak T., Ginsberg R.
Extract |
Full Text
N Engl J Med 1999;
340:1685-1687, May 27, 1999.
Correspondence
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10 percent of body weight) and cell type as determined by histologic examination (adenocarcinoma or epidermoid cancer). Patients were randomly assigned either to undergo an immediate operation or to receive three cycles of chemotherapy with a combination of cisplatin and fluorouracil before the operation. Patients with stable disease or disease that responded to chemotherapy and in whom an R0 resection was accomplished (all margins deemed free of tumor by microscopical examination) were also to receive two cycles of chemotherapy after surgery. 
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