Twice-Daily Compared with Once-Daily Thoracic Radiotherapy in Limited Small-Cell Lung Cancer Treated Concurrently with Cisplatin and Etoposide
Andrew T. Turrisi, M.D., Kyungmann Kim, Ph.D., Ronald Blum, M.D., William T. Sause, M.D., Robert B. Livingston, M.D., Ritsuko Komaki, M.D., Henry Wagner, M.D., Seena Aisner, M.D., and David H. Johnson, M.D.
Background For small-cell lung cancer confined to one hemithorax(limited small-cell lung cancer), thoracic radiotherapy improvessurvival, but the best ways of integrating chemotherapy andthoracic radiotherapy remain unsettled. Twice-daily acceleratedthoracic radiotherapy has potential advantages over once-dailyradiotherapy.
Methods We studied 417 patients with limited small-cell lungcancer. All the patients received four 21-day cycles of cisplatinplus etoposide. We randomly assigned these patients to receivea total of 45 Gy of concurrent thoracic radiotherapy, giveneither twice daily over a three-week period or once daily overa period of five weeks.
Results Twice-daily treatment beginning with the first cycleof chemotherapy significantly improved survival as comparedwith concurrent once-daily radiotherapy (P=0.04 by the log-ranktest). After a median follow-up of almost 8 years, the mediansurvival was 19 months for the once-daily group and 23 monthsfor the twice-daily group. The survival rates for patients receivingonce-daily radiotherapy were 41 percent at two years and 16percent at five years. For patients receiving twice-daily radiotherapy,the survival rates were 47 percent at two years and 26 percentat five years. Grade 3 esophagitis was significantly more frequentwith twice-daily thoracic radiotherapy, occurring in 27 percentof patients, as compared with 11 percent in the once-daily group(P<0.001).
Conclusions Four cycles of cisplatin plus etoposide and a courseof radiotherapy (45 Gy, given either once or twice daily) beginningwith cycle 1 of the chemotherapy resulted in overall two- andfive-year survival rates of 44 percent and 23 percent, a considerableimprovement in survival rates over previous results in patientswith limited small-cell lung cancer.
Of the approximately 170,000 cases of lung cancer diagnosedeach year in the United States, 20 percent are small-cell cancers.1Staging systems divide small-cell lung cancer into two categories:limited and extensive. The former is clinically confined toone side of the chest and is treatable by radiotherapy fieldsizes (portals) tolerated by normal tissues.
The main treatment for limited small-cell lung cancer is radiotherapyand chemotherapy. Cisplatin plus etoposide has largely supplantedthe older regimens of cyclophosphamide, doxorubicin, and vincristine.Advantages of the cisplatin–etoposide regimen over theolder regimen include the absence of toxic effects on intrathoracicorgans and the ability to use thoracic radiotherapy concurrently.
A meta-analysis of trials comparing chemotherapy alone withcombined chemotherapy and thoracic radiotherapy found that combinedtreatment improved survival among patients with limited small-celllung cancer,2 but the best method of integrating thoracic radiotherapywith chemotherapy remained undefined. The optimal total dose,volume, duration, and timing of thoracic radiotherapy have notbeen tested in prospective trials. Fractionation of the customaryonce-daily radiotherapy dose into two treatments each day hasbiologic advantages and has been successful in pilot studies.In vitro, small-cell lung-cancer cell lines have marked radiosensitivityeven to small doses of radiation.3 The dose–response curvesfor small-cell lung-cancer cell lines lack a shoulder, whichmeans that even at relatively low doses per fraction, smallcells are killed exponentially; by contrast, radiation sparescell populations that have a shoulder. For these reasons, multiplesmall fractions of radiotherapy can kill small-cell cancer whilereducing permanent damage to normal tissues. In addition, theuse of small fractions may diminish the risks of late effectsof radiation.
Pilot studies of twice-daily thoracic radiotherapy suggestedthat this therapy might have excellent results when combinedwith cisplatin and etoposide. The two-year survival rate wasapproximately 40 percent, and the rates of myelosuppressionand esophagitis were tolerable: grade 3 granulocytopenia occurredin 70 to 80 percent of the treated patients and grade 3 esophagitisin 35 to 40 percent.4,5,6,7
Cisplatin–etoposide combined with once-daily radiotherapywas also examined in pilot studies.8,9 The Southwest OncologyGroup, using daily fractionated thoracic radiotherapy at a totaldose of 45 Gy, reported a two-year survival rate of 40 percent.9Toxic effects were equally reversible in pilot studies of twice-dailyor once-daily thoracic radiotherapy.
In this study of limited small-cell lung cancer, we comparedonce-daily and twice-daily thoracic radiotherapy while holdingother variables constant.
Methods
Patients
We enrolled 419 patients in the study, which began in May 1989and ended in July 1992. Two patients were found to have beenenrolled twice. The primary analysis thus included 417 patientsand was conducted on an intention-to-treat basis. Of the 417patients, 36 (21 receiving once-daily radiation and 15 receivingtwice-daily radiation) were excluded from the analysis of eligiblepatients: 7 withdrew from treatment and never received any therapyaccording to the protocol, and 29 were found to be ineligible.The reasons for ineligibility were the absence of pretreatmenttumor measurements (eight patients), extensive disease (six),histologic findings of non–small-cell cancer (six), incompletestaging studies (five), elevated serum aspartate aminotransferaselevel (one), incorrect diagnosis (one), inadequate performancestatus10 (see below; one), and absence of on-study data (one).Thus, 381 patients (185 receiving once-daily treatment and 196receiving twice-daily treatment) were eligible for a secondaryanalysis.
For patients to be eligible the small-cell lung cancer had tobe confined to one hemithorax, the ipsilateral supraclavicularfossa, or both. Patients with pleural effusions found on chestfilms were excluded, regardless of cytologic findings, as werepatients with contralateral hilar or supraclavicular adenopathy.Staging was done by computed tomography (CT) or magnetic resonanceimaging (MRI) of the chest, abdomen, and brain; radionuclidebone scanning; and bilateral iliac-crest bone marrow aspirationand biopsy. Adequate organ function was defined as a white-cellcount of at least 4000 per cubic millimeter, a platelet countof at least 100,000 per cubic millimeter, a serum creatininelevel of less than 1.5 mg per deciliter (130 µmol perliter), serum aspartate aminotransferase and alanine aminotransferaselevels less than two times the upper limit of normal, a serumbilirubin level of less than 0.5 mg per deciliter (8.6 µmolper liter), and a forced expiratory volume in one second ofat least 1.0 liter. Symptomatic cardiac disease or a myocardialinfarction within the previous six months was cause for exclusion.Patients had to be available for follow-up. In all cases, histologicor cytologic findings confirmed the diagnosis of small-celllung cancer. Patients with prior cancer or prior treatment witheither chemotherapy or radiotherapy were ineligible. All patientsenrolled in the study gave informed consent.
Chemotherapy
The patients received four cycles of chemotherapy. Each three-weekcycle consisted of 60 mg of cisplatin per square meter of body-surfacearea on day 1 and 120 mg of etoposide per square meter on days1, 2, and 3. No dose adjustments were permitted for the firsttwo cycles. During cycles 3 and 4, the dose of etoposide wasreduced for patients with grade 4 toxic effects, febrile neutropeniaor documented infection, or thrombocytopenia associated withbleeding. The dose of cisplatin was reduced during cycles 3and 4 for patients with serum creatinine levels of 1.6 to 2.5mg per deciliter (140 to 220 µmol per liter) and was furtherreduced if the levels were 2.6 mg per deciliter (230 µmolper liter) or higher.
Thoracic Radiotherapy
In both groups, the total dose of thoracic radiotherapy was45 Gy for each patient. Patients receiving once-daily therapyreceived 1.8 Gy daily in 25 treatments over a period of fiveweeks. Accelerated twice-daily thoracic radiotherapy involvedthe administration of 1.5 Gy in 30 treatments over a periodof three weeks. In both groups, thoracic radiotherapy beganconcurrently with the first cycle of chemotherapy.
The target volume for thoracic radiotherapy, which was similarin both groups, included the gross tumor, as defined by thechest CT scan, and the bilateral mediastinal and ipsilateralhilar lymph nodes. Irradiation of uninvolved supraclavicularfossae was forbidden. The inferior border extended 5 cm belowthe carina or to a level including ipsilateral hilar structures,whichever was lower. The clinically determined volume was expandedby a margin of 1 to 1.5 cm.
Radiotherapy treatment used linear accelerators; no cobalt-60machines were allowed. Patients underwent treatment setup withradiotherapy simulators to mark field borders before treatment.Reduction of the field to conform to a smaller target volumeafter treatment was not allowed.
Interruptions of thoracic radiotherapy were discouraged, butit was interrupted when patients had platelet counts under 50,000per cubic millimeter, weight loss of 4.5 kg (10 lb) or more(grade 2), or hospitalization for neutropenic fever or sepsis,but not when patients had difficulty swallowing or fever withlow white-cell counts.
Prophylactic Cranial Irradiation
Systemic therapy was scheduled to last 12 weeks. The stage ofdisease was then determined again according to the results ofchest radiography and head and chest CT. Because of the highfrequency of brain metastases (50 percent), patients with acomplete response were offered prophylactic cranial irradiation,despite reports of neurotoxicity.11 This treatment consistedof 10 doses of 2.5 Gy to the midplane of the brain over a two-weekperiod, for a total of 25 Gy.12
Measurement of Response
A complete response was defined as the disappearance of allclinical evidence of tumor. A decrease of 50 percent or morein the product of the length and width of any measurable tumorfor at least four weeks was counted as a partial response. Thedisease was considered to have progressed if the patient lostmore than 10 percent of body weight, if there was a 25 percentincrease in the diameter of any tumor 2.0 cm or more in diameteror a 50 percent increase in the diameter of any tumor less than2.0 cm in diameter, or if any new tumor appeared.
End Points
Overall survival, the primary end point of the trial, was measuredfrom the date of entry into the study to the date of death fromany cause. Treatment was considered to have failed if therewas objective evidence of disease progression, regardless oftumor response, or death without clear-cut evidence of tumorprogression. Failure was considered local when an intrathoracicrelapse occurred after a complete response or when there wasno complete response.
Statistical Analysis
The target enrollment was 400 patients. This sample size wouldgive the study an 82 percent power to detect an absolute differencein two-year survival rates of 15 percent (25 percent for patientsreceiving once-daily treatment and 40 percent for patients receivingtwice-daily treatment) at the 0.05 level with a two-sided test.This difference is equivalent to a 50 percent increase in mediansurvival under the assumption of exponential distribution ofsurvival.
With the exponential distribution of survival, we expected todetect a hazard ratio of 1.4 after adjustment for variationsin radiotherapy and a total of 353 deaths by the end of thestudy.
Patients were randomized according to a permuted-block scheme,stratified according to Eastern Cooperative Oncology Group performancestatus (0 or 1 vs. 2), sex, and weight loss during the six monthsbefore entry (less than 5 percent of body weight vs. 5 percentor more).13
The survival distributions for overall survival and time totreatment failure were estimated according to the method ofKaplan and Meier.14 For comparison of ordinal data, such asthe incidence of toxic effects, an exact Kruskal–Wallistest was used.15 For comparison of binary data, such as responserates, Fisher's exact test was used.16 For comparison of thesurvival distributions, a Mantel log-rank test was used fordiscrete covariates,17 with stratification according to thestratification variables unless otherwise indicated. All P valuesare based on two-sided tests.
In our analysis of prognostic factors, the proportional-hazardsregression model was used to estimate the joint effect of prognosticfactors on survival.18 A step-down procedure that consistedof dropping the least significant covariates, one at a time,was used to obtain a more parsimonious model.
Results
Table 1 shows the main characteristics of the 417 patients,of whom 206 received once-daily therapy and 211 twice-dailytherapy. The median age was 63 years (range, 34 to 80) for thepatients receiving once-daily therapy, and 61 years (range,30 to 82) for the patients receiving twice-daily therapy. Fortypercent of the patients assigned to once-daily therapy wereover 65 years of age, as compared with 31 percent of those assignedto twice-daily therapy (P= 0.07). All other variables were wellbalanced. Only 8 (2 percent) of the 356 patients for whom histologicdata were available had variant histologic findings, an admixtureof large-cell and small-cell lung cancer thought to be associatedwith a poorer prognosis.3
Table 1. Characteristics of the Study Patients According to Assigned Treatment.
Toxic Effects
Table 2 and Table 3 show the toxic effects observed among 409patients, including 28 ineligible patients. Despite major myelosuppression(in approximately 90 percent of patients in both groups), therewas only one death from myelotoxicity. Overall, there were only11 treatment-related deaths (6 in the group receiving twice-dailytherapy and 5 in the group receiving once-daily therapy). Nohematopoietic growth factors were used.
Table 3. Incidence of Toxic Effects According to the Frequency of Radiotherapy.
There were significant differences between the groups in theincidence of esophagitis (P<0.001). Fifty-six percent ofthe patients receiving once-daily therapy and 37 percent ofthose receiving twice-daily therapy had no esophageal toxiceffects (grade 0). Grade 3 toxicity, defined as an inabilityto swallow solids, requiring narcotic analgesics or the useof a feeding tube, occurred in 11 percent of patients receivingonce-daily therapy and 27 percent of those receiving twice-dailytherapy. There was no difference between the groups in the incidenceof grade 4 toxicity (hospitalization of the patient or perforationof the esophagus). There were no reports of permanent stricturedue to the acute esophagitis. The duration of esophagitis wasnot a study end point.
Response Rates
Table 4 shows the response rates of the 381 eligible patients.Nearly 90 percent had objective responses. There was no significantdifference in the response rate between the groups, nor didthe rate differ significantly between the eight patients withvariant histologic findings and the patients with standard histologicfindings.
Table 4. Results According to the Frequency of Radiotherapy.
Survival
As of this writing, the median follow-up was almost eight years,and the minimal potential follow-up was approaching five years.Of the 417 patients, 335 had died: 175 patients who receivedonce-daily therapy (85 percent) and 160 patients who receivedtwice-daily therapy (76 percent). The median survival was 20months for all patients, 19 months for those receiving once-dailytherapy, and 23 months for those receiving twice-daily therapy.The two-year survival rate was 44 percent for all patients,41 percent for those receiving once-daily therapy, and 47 percentfor those receiving twice-daily therapy (standard error forboth groups, 3 percent). The five-year survival rate was 23percent for all patients, 16 percent for those receiving once-dailytherapy, and 26 percent for those receiving twice-daily therapy(standard error for both groups, 3 percent). The differencein survival between the two groups was statistically significant(P=0.04 by the log-rank test). The estimated hazard ratio fordeath with once-daily treatment as compared with twice-dailytreatment was 1.2 (95 percent confidence interval, 1.0 to 1.6).Figure 1 shows the estimated survival distribution accordingto treatment group.
Figure 1. Kaplan–Meier Estimates of Overall Survival for All 417 Patients Assigned to Treatment Groups.
The rate of failure-free survival at two years was 24 percentfor patients receiving once-daily therapy and 29 percent forthose receiving twice-daily therapy (P=0.10). According to aproportional-hazards regression model, male sex (P=0.01) anda performance status of 2 (P=0.005) were associated with shorterfailure-free survival.
Pattern of Treatment Failure
Twice-daily thoracic radiotherapy reduced the rate of localfailure: the rate was 52 percent in the group receiving once-dailytherapy and 36 percent in the group receiving twice-daily therapy(P=0.06). The rates of simultaneous local and distant failurewere significantly different between the groups: both localand distant failure occurred in 23 percent of the patients receivingonce-daily therapy and 6 percent of those receiving twice-dailytherapy (P=0.01).
Discussion
In this trial of chemoradiotherapy for small-cell lung cancer,we gave four cycles of cisplatin–etoposide chemotherapyconcurrently with 45 Gy of thoracic radiation administered twicedaily or once daily. The survival rate among the 417 patientsexceeded that in any previously reported large, randomized trialof chemotherapy and radiotherapy for this disease.19,20,21,22,23,24After five years of follow-up, only 335 deaths have been reported,even though 353 deaths were anticipated at two years. Survivalwas significantly better in the group receiving twice-dailyradiotherapy than in the group receiving once-daily radiotherapy(P=0.04). The magnitude of the difference between the groupsat two years was quite small and clinically insignificant, butwith further follow-up to five years, the difference betweenthe treatments favored the twice-daily treatment group by 10percent (standard error, 4 percent).
Many assert that adding thoracic radiotherapy to chemotherapyincreases toxicity without improving survival. A meta-analysisof chemotherapy alone as compared with chemotherapy and radiotherapyfound that the addition of radiotherapy improved the survivalrate at three years only slightly.2 The trials included in themeta-analysis all used cyclophosphamide-based or doxorubicin-basedregimens; in none did initial treatment include cisplatin andetoposide.
Although it was introduced in the late 1970s,25,26 the combinationof cisplatin and etoposide emerged as primary therapy only inthe early 1980s.4,9 A clear advantage of cisplatin plus etoposideis that the combination can be given concurrently with relativelyfull doses of thoracic radiotherapy, with less morbidity thanoccurs with doxorubicin-based27,28 or cyclophosphamide-based29regimens. The meta-analysis2 identified no differences regardingthe timing of thoracic radiotherapy and chemotherapy.
The best method of integrating chemotherapy and thoracic radiotherapyremains unknown. Because small-cell lung cancer responds wellto thoracic radiotherapy, only moderate doses of radiation (40to 50 Gy) have been used in most trials. Choi et al.30 reportedthat esophagitis limited treatment when the total dose fromtwice-daily treatment exceeded 45 Gy, and that a total doseof 70 Gy could be tolerated with once-daily treatments. Papacand colleagues31 reported a rate of local failure of only 3percent with 60 Gy fractionated once daily, but with only asmall gain in median survival. Without radiotherapy, local failureoccurs in 90 percent of patients.24 Our study verifies thatlocal failure remains an important problem, but we found thatimproved local therapy contributes to both local control andsurvival.
The timing of concurrent radiotherapy and chemotherapy may bean important therapeutic variable. We initiated therapy at thesame time as the first cycle of cisplatin plus etoposide. Othershave begun radiotherapy at the time of later cycles of chemotherapy.Murray et al.23 reported that cisplatin–etoposide therapyin combination with radiotherapy beginning with cycle 2 wassuperior to concurrent radiotherapy beginning with cycle 6.Recently, Takada and colleagues32 verified that beginning radiotherapyconcurrently with etoposide was superior to beginning radiotherapyafter the completion of four cycles of chemotherapy. The Cancerand Leukemia Group B trial compared radiotherapy starting withcycle 1 of chemotherapy and radiotherapy starting with cycle4.24 This 1987 trial used cyclophosphamide-based chemotherapy.It found the best survival when the radiotherapy began withcycle 4. Others, particularly in Europe,21,22 found that sequentialstrategies were superior to concurrent treatment, which wasassociated with excess toxicity. Cyclophosphamide-based or doxorubicin-basedchemotherapy continues to be used in these studies, which mayexplain the inability to integrate concurrent thoracic radiotherapysuccessfully. The two-year survival in these trials is abouthalf the rate in our study.
The number of deaths we initially projected to occur in twoyears has not occurred after a minimal follow-up of five years.Esophagitis after twice-daily radiotherapy did not lead to stricture,and all the affected patients recovered their ability to swallow.Only 1 death was attributable to hematologic toxicity, and therewere only 11 treatment-related deaths. Although there was animbalance in age between the groups, age did not influence survivalsignificantly when isolated as a variable (data not shown).
Supported in part by Public Health Service grants (CA23318,CA20319, CA32102, CA21661, CA16395, CA49957, CA66636, and CA21115)from the National Cancer Institute, National Institutes of Health,and the Department of Health and Human Services.
Source Information
From the Medical University of South Carolina, Charleston (A.T.T.); the University of Wisconsin, Madison (K.K.); St. Vincent's Medical Center, New York (R.B.); LDS Hospital, Salt Lake City (W.T.S.); the University of Washington, Seattle (R.B.L.); M.D. Anderson Cancer Center, Houston (R.K.); H. Lee Moffitt Cancer Center, Tampa, Fla. (H.W.); the University of Medicine and Dentistry of New Jersey, Newark (S.A.); and Vanderbilt University, Nashville (D.H.J.). This study was coordinated by the Eastern Cooperative Oncology Group (Douglas Tormey, M.D., chair), which was joined in an intergroup effort by the Radiotherapy Oncology Group and the Southwest Oncology Group. The contents of this report are solely the responsibility of the authors and do not necessarily represent the official views of the National Cancer Institute.
Address reprint requests to Dr. Turrisi at the Medical University of South Carolina, Department of Radiation Oncology, 171 Ashley Ave., Charleston, SC 29425, or at turrisi{at}radonc.musc.edu.
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