Background We conducted a randomized, prospective trial comparingexternal irradiation with external irradiation plus goserelin(an agonist analogue of gonadotropin-releasing hormone thatreduces testosterone secretion) in patients with locally advancedprostate cancer.
Methods From 1987 to 1995, 415 patients with locally advancedprostate cancer were randomly assigned to receive radiotherapyalone or radiotherapy plus immediate treatment with goserelin.The patients had a median age of 71 years (range, 51 to 80).Patients in both groups received 50 Gy of radiation to the pelvisover a period of five weeks and an additional 20 Gy over anadditional two weeks as a prostatic boost. Patients in the combined-treatmentgroup received 3.6 mg of goserelin (Zoladex) subcutaneouslyevery four weeks starting on the first day of irradiation andcontinuing for three years; those patients also received cyproteroneacetate (150 mg orally per day) during the first month of treatmentto inhibit the transient rise in testosterone associated withthe administration of goserelin.
Results Data were available for analysis on 401 patients. Themedian follow-up was 45 months. Kaplan–Meier estimatesof overall survival at five years were 79 percent (95 percentconfidence interval, 72 to 86 percent) in the combined-treatmentgroup and 62 percent (95 percent confidence interval, 52 to72 percent) in the radiotherapy group (P = 0.001). The proportionof surviving patients who were free of disease at five yearswas 85 percent (95 percent confidence interval, 78 to 92 percent)in the combined-treatment group and 48 percent (95 percent confidenceinterval, 38 to 58 percent) in the radiotherapy group (P<0.001).
Conclusions Adjuvant treatment with goserelin, when startedsimultaneously with external irradiation, improves local controland survival in patients with locally advanced prostate cancer.
The role of external irradiation in patients with locally advancedprostate cancer is controversial.1,2 At this stage of the diseasethe tumor extends beyond the capsule of the prostate; it mayinfiltrate neighboring structures and involve regional lymphnodes, but there are no distant metastases (stage T3–4,N0–2, M0, according to the tumor–node–metastasis[TNM] classification system of the International Union againstCancer). In a study begun in 1973, the overall survival after15 years for 287 patients with locally advanced prostate cancerwho were treated with conventional external irradiation was23 percent.3 Achieving local control after radiotherapy improvedthe prognosis; among patients who did not have involvement ofregional lymph nodes at the time of diagnosis, 70 percent ofthose who attained local control survived for 20 years freeof distant metastases, as compared with 13 percent of thosewho had a local relapse (P<0.001).4
Hormonal therapy often prolongs the suppression of the primarytumor by radiotherapy,5 but the question remains whether hormonaltherapy should be reserved for relapse or used early in asymptomaticpatients with locally advanced disease who are receiving externalradiation treatment. Three controlled clinical trials have failedto demonstrate the value of prophylactic therapy with diethylstilbestrol,orchiectomy, or both in patients treated with external radiotherapy.6,7,8A study of 277 patients found no differences among those undergoingorchiectomy, radiotherapy, or combined treatment; orchiectomy,however, whether alone or combined with radiotherapy, significantlydelayed metastases as compared with radiotherapy alone.9
Goserelin is an agonist analogue of gonadotropin-releasing hormonethat induces hypogonadism by reducing the secretion of gonadotropinand therefore testosterone. The purpose of this trial was todetermine whether treatment with goserelin, when initiated duringthe first week of irradiation, increases disease-free survivaland prolongs overall survival in patients at high risk for metastaticprostate cancer.
Methods
Eligibility Criteria
Patients were eligible if they were under 80 years of age, withhistologically proved prostatic adenocarcinoma that was intracapsular(T1) or confined to the gland (T2), without detectable involvementof regional lymph nodes (N0-X), and of World Health Organization(WHO) histologic grade 3; or if they had prostate cancer ofany histologic grade that extended beyond the capsule (T3) orinfiltrated neighboring structures (T4) without involving regionallymph nodes. The clinical evaluation included bone scanning,chest radiography, and ultrasonography or computed tomography(CT) of the liver. Lymph nodes were evaluated by CT, bipedallymphangiography, or extraperitoneal lymphadenectomy. Laboratorystudies included complete blood counts and measurements of creatinine,serum prostatic acid phosphatase, serum testosterone, and prostate-specificantigen (PSA), as assessed by radioimmunometric or immunoenzymeassays. Eligible patients had had no previous treatment forprostate cancer and gave written informed consent. Patientswith a previous malignant disease, except for treated basal-cellcarcinoma of the skin, and those with evidence of distant metastases,including metastases to common iliac or paraaortic lymph nodes,were excluded. Pathological specimens were reviewed centrally.
Techniques of Treatment
Radiotherapy
Photons of 10 MV and above were recommended; when they werenot available, the use of cobalt-60 was acceptable providedthe skin-to-source distance was more than 80 cm and patientshad a maximal anterior–posterior pelvic diameter of lessthan 22 cm. Planning target volume I was the whole pelvis, andplanning target volume II the prostate and seminal vesicles.The whole pelvis was irradiated with a four-field technique,with one anterior–posterior field, one posterior–anteriorfield, and two parallel opposed lateral fields. In the craniocaudaldirection the upper limit was the L5–S1 interspace, thelower limit was the ischial tuberosities, and the lateral marginswere 1 cm beyond the maximal width of the bony pelvis; somecenters preferred to irradiate a smaller target volume by usinganterior–posterior fields averaging 12 by 12 cm and lateralfields averaging 12 by 10 cm. Planning target volume II wasirradiated with either the same technique or with three fields:one anterior–posterior and two lateral fields with wedgefilters. The anterior and posterior security margins on thelateral fields were at least 2 cm. The specification of thedose was given at the intersection of the beam axes accordingto Report 29 of the International Commission on Radiation Unitsand Measurements.10 The dose per fraction was 2 Gy. Patientswere treated once a day, five days a week, for seven weeks;planning target volume I was irradiated during a five-week periodwith up to 50 Gy, and planning target volume II was treatedduring the last two weeks with an additional 20 Gy.
Hormonal Treatment
Goserelin (Zoladex, Zeneca-Pharma) was supplied by the manufacturerin a disposable syringe loaded with 3.6 mg of the drug and fittedwith a 16-gauge needle. The drug was administered subcutaneouslyevery four weeks, starting on the first day of pelvic irradiationand continuing for three years; 150 mg of a steroidal antiandrogen,cyproterone acetate (Androcur, Schering), was given orally forone month, starting one week before the first dose of goserelin,to inhibit the transient rise of testosterone caused by goserelin.
Toxicity
Acute side effects of radiotherapy were scored according tothe WHO scale.11 Late toxicity was scored according to the RadiotherapyOncology Group scale: 0, no symptoms; 1, minor transient symptoms;2, distressing, persistent, or recurring symptoms requiringoccasional prolonged medical treatment; 3, symptoms requiringprolonged medical treatment, surgical intervention, or both;or 4, fatal complications. For patients receiving goserelin,adverse reactions were registered as hot flashes and gynecomastia.There was no quality-of-life study.
Assessment of Progression
Local failure was defined as an increase of more than 50 percentin the product of the two maximal perpendicular diameters ofthe primary lesion as measured digitally, by CT or transabdominalultrasonography; in case of doubt, biopsy was highly recommended.Local progression was defined as the recurrence of a palpabletumor after initial regression. Regional failure, in the pelvicor paraaortic lymph-node areas, was demonstrated by ultrasonographyor CT and was confirmed by biopsy. Distant metastases in bones,parenchymal organs, or soft tissues were identified radiologicallyand then by biopsy if deemed necessary.
Quality Assurance
The calibration of every linear accelerator was obtained bymailed thermoluminescence dosimetry checks. Individual clinical,biologic, pathological, and follow-up procedures for the mainparticipating centers were reviewed individually to reconcilediscrepancies between local data and data registered at theEuropean Organization for Research and Treatment of Cancer (EORTC)Data Center. Protocol compliance was checked by a dummy-runprocedure to evaluate differences in the definition of targetvolume, in treatment technique, and in dose specification andhomogeneity.12
End Points and Statistical Analysis
Overall survival was measured from the date of randomizationto the date of death or the most recent follow-up. The disease-freeinterval was measured from the date of randomization to thedate of local or regional failure, the first appearance of distantmetastases, or the last follow-up, whichever occurred first.The time until the first treatment failure after a biologicresponse was measured from the date of randomization to thedate of clinically determined progression, PSA-determined progression,or the most recent follow-up; PSA-determined progression wasdefined as a PSA level greater than 1.5 ng per milliliter andincreasing on two consecutive measurements.
The protocol was designed to detect a minimal increase from40 percent to 55 percent in the 5-year disease-free rate, correspondingto an increase from 3.8 to 5.8 years in the median disease-freeinterval (assuming exponential distribution). To detect thisdifference, 75 patients in each treatment group had to be followeduntil relapse ( = 0.05, = 0.2). Survival curves were estimatedby using the Kaplan–Meier technique.13 All comparisonswere made by means of a two-sided log-rank test with a 0.05significance level.14 Data were analyzed according to the intention-to-treatprinciple.
Randomization
Randomization was centralized at the EORTC Data Center. Patientswere stratified according to institution, the clinical stageof the disease, the results of extraperitoneal pelvic lymph-nodebiopsy, and the irradiation technique. The randomization wasperformed by the minimization technique.15
Results
Characteristics of the Patients
From May 1987 through September 1995, 415 patients entered thestudy — 208 in the pelvic-radiotherapy group and 207 inthe combined-treatment group. The median duration of follow-upwas 45 months. At the time of analysis, all but 14 patientshad been evaluated. For the analysis, these 14 patients wereconsidered eligible. Ten patients — six in the radiotherapygroup and four in the combined-treatment group — wereineligible because of bone metastases (two patients), paraaorticlymph-node metastases (one), thrombocytopenia (one), inappropriateclinical stages (T1G1, one; T2G1, one; and T2G2, three; andT2 without mention of grade, one). The two groups of patientswere well balanced with regard to age, WHO performance status,clinical stage, presence or absence of pelvic lymph-node metastases,WHO histologic grade, Gleason grade, serum acid phosphataselevel, and base-line PSA level (Table 1). Cardiovascular diseasewas present in 29 percent of the patients in the radiotherapygroup and 24 percent of those in the combined-treatment group;no chronic disease was mentioned for 48 percent of the patientsin the radiotherapy group as compared with 53 percent in thecombined-treatment group.
Table 1. Age, Performance Status, WHO Grade, Gleason Score, and Tumor and Node Classification among Patients Eligible for the Trial.
Compliance
Information about treatment was available for 401 patients —198 in the radiotherapy group and 203 in the combined-treatmentgroup. Of the patients in the radiotherapy group, 99 percentreceived external irradiation; 80 percent of these patientsreceived large-field and 20 percent small-field radiotherapy.Three of the 198 patients refused the treatment.
Of the 203 patients in the combined-treatment group, 2 refusedany treatment and 6 refused hormonal therapy. At the time ofanalysis, not all the patients in this group had completed thethree-year treatment with goserelin, but 15 patients continuedthat treatment for more than three years (Table 2). Eighty-onepercent of the patients in this group received large-field and19 percent small-field radiotherapy.
Table 2. Compliance with the Goserelin Regimen among 195 Patients in the Combined-Treatment Group.
Toxicity
Of the acute toxic effects listed in Table 3, none with a gradeof 3 or 4 affected more than 5 percent of either group exceptfor diarrhea. With a median follow-up of 45 months, not morethan 1 percent of either group had grade 3 late toxic effects,including hematuria, chronic diarrhea, proctitis, cystitis,small-bowel obstruction, incontinence, and urethral stricture.Data on erectile function were not collected systematically.Among the patients receiving goserelin, 62 percent had hot flashes,but only 34 percent had more than three per day. During follow-up,more patients in the combined-treatment group than in the radiotherapygroup had late grade 1–3 incontinence (29 percent vs.16 percent, P = 0.002); the proportions of patients with lategrade 1–3 urethral stricture (20 percent in the combined-treatmentgroup vs. 13 percent in the radiotherapy group) were not significantlydifferent (P = 0.09). Thirty-eight patients (19 percent) hadadverse reactions to the gonadotropin-releasing hormone analogue:hot flashes (22 patients), gynecomastia (4), mastodynia (1),breast pain and galactorrhea (1), sweating (2), weakness (2),depression (1), deep venous thrombosis (1), and unspecifiedreactions (4).
Table 3. Grade 3 or 4 Toxic Effects Reported during Radiotherapy among All Eligible Patients Who Underwent Radiotherapy.
Efficacy
The Kaplan–Meier estimate of overall survival at fiveyears in the combined-treatment group was 79 percent (95 percentconfidence interval, 72 to 86 percent), as compared with 62percent (95 percent confidence interval, 52 to 72 percent) inthe radiotherapy group (P = 0.001) (Figure 1). For overall survival,the hazard ratio was 0.50 (95 percent confidence interval, 0.33to 0.76). There were 58 deaths in the radiotherapy group and35 in the combined-treatment group. Of these deaths, 26 in theradiotherapy group and 6 in the combined-treatment group weredue to prostate cancer. Among the patients who survived forfive years, the disease-free rate was 85 percent (95 percentconfidence interval, 78 to 92 percent) in the combined-treatmentgroup and 48 percent (95 percent confidence interval, 38 to58 percent) in the radiotherapy group (hazard ratio = 0.22;95 percent confidence interval, 0.15 to 0.32; P<0.001) (Figure 2).Seventy-eight patients had disease progression in the radiotherapygroup, as compared with 20 in the combined-treatment group.Table 4 shows the sites of progression. In the radiotherapygroup, the treatment given after progression included goserelinin 56 cases (72 percent) and another hormonal treatment in 17cases and was unspecified in 5 cases. The 17 other treatmentswere orchiectomy (eight patients), another hormonal treatment(two), delayed treatment (five), and no treatment, because ofintercurrent death (one) and the patient's refusal (one). Thefive-year local-control rate was 97 percent in the combined-treatmentgroup and 77 percent in the radiotherapy group (hazard ratio= 0.19; 95 percent confidence interval, 0.10 to 0.37; P<0.001).The combined-treatment group had a longer time until the firsttreatment failure after a biologic response than the radiotherapygroup (6.6 years [95 percent confidence interval, 3.5 to 5.3]vs. 4.4 years [95 percent confidence interval, 5.8 to 9.0];hazard ratio = 0.17; 95 percent confidence interval, 0.11 to0.48; P< 0.001). The five-year failure-free rate after biologicresponse was 81 percent for the combined-treatment group and43 percent for the radiotherapy group.
Figure 1. Kaplan–Meier Estimate of Overall Survival.
The overall survival rate at five years was 79 percent (95 percent confidence interval, 72 to 86 percent) for the combined-treatment group and 62 percent (95 percent confidence interval, 52 to 72 percent) for the group treated only with radiotherapy.
Figure 2. Kaplan–Meier Estimate of the Disease-free Interval.
This curve shows the proportion of surviving patients who were free of disease at each time point. The method takes the censoring process into account. The number of patients who are at risk for the event at each time point is the total number of patients minus the number in whom disease progressed or who were lost to follow-up.
We found that adjuvant therapy with an analogue of gonadotropin-releasinghormone (goserelin), started at the beginning of external irradiationtreatment and continuing for three years, can improve the five-yearoverall survival of patients with locally advanced prostatecancer. Two previous studies have compared short-term hormonaltherapy before and during external irradiation, or long-termhormonal therapy after external irradiation, with radiationtherapy alone for locally advanced prostatic carcinoma. Thehormonal therapy included flutamide and goserelin for the formerand goserelin alone for the latter; both protocols showed advantagesover radiotherapy alone in terms of local control, the incidenceof distant metastases, and progression-free survival.16,17 However,it is difficult to compare these three trials, since the eligibilitycriteria, the timing and duration of administration of goserelin,the definition of local control, and the results in the radiotherapygroups are not quite comparable. In our study, we assessed localcontrol by endorectal examination; a second biopsy of the prostatewas not mandatory if the endorectal examination was normal,even if the serum PSA level was elevated. This aspect of assessmenthas been addressed previously, and one year after the completionof external irradiation the rate of positive biopsy resultshas been found to reach a plateau of 35 percent.18 The clinicalresults in our control group are in keeping with those of aretrospective analysis of 397 patients, with stage T3–T4disease, who were treated only by external irradiation in 19French institutes from 1983 to 1987. The rate of local controlat five years was 79 percent, as compared with 77 percent (95percent confidence interval, 68 to 86 percent) in the EORTCtrial.19 The time until the first treatment failure after abiologic response is a surrogate end point that represents thetime from randomization to the date of clinically determinedprogression or PSA-determined progression. Analysis using thisend point showed a significant difference between combined treatmentand radiotherapy alone (hazard ratio = 0.17; 95 percent confidenceinterval, 0.11 to 0.48; P<0.001).
We are indebted to Zeneca-Pharma for providing Zoladex and toF.W.J. Ten Kate, M.D., J. Mattelaer, M.D., J. Lopez Torrecilla,M.D., J.R. Pfeffer, M.D., C.L. Cutajar, M.D., T. Roberts, M.D.,S. Fossa, M.D., J.C. Horiot, M.D., H. Hamers, M.D., J.F. Bossett,M.D., F. Kovner, M.D., H. Van Poppel, M.D., J. Jager, M.D.,V. Svoboda, M.D., J.J. Zambon, M.D., J.J. Wijndaele, M.D., O.Koriakine, M.D., and C. Boekenkruger, M.D., for their collaboration.
Source Information
From University Hospital, Grenoble, France (M.B.); Akademisch Medisch Centrum, Amsterdam, the Netherlands (D.G.); Princess Margaret Hospital, Toronto (P.W.); Centre Régional de Lutte contre le Cancer Val d'Aurelle, Montpellier, France (J.B.D.); Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland (R.-O.M.); Oncologisch Centrum, Brussels (G.S.); Ospedale San Giovanni, Bellinzona, Switzerland (J.B.); Rambam Medical Center, Haifa, Israel (A.K.); Ufficio Sternberg & Pansadoro, Rome (C.S.); and the European Organization for Research and Treatment of Cancer Data Center, Brussels (T.G., L.C., M.P.).
Address reprint requests to Dr. Bolla at the Radiotherapy Department, University Hospital, B.P. 217 38043 Grenoble CEDEX 9, France.
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Appendix
The following EORTC Radiotherapy Cooperative Group institutionsparticipated in this study: Grenoble, Hôpital Albert Michallon;Montpellier, Centre Val d'Aurelle; Dijon, Centre Georges-FrançoisLeclerc; Besançon, Hôpital Jean Minjoz; Amsterdam,Akademisch Medisch Centrum; Heerlen, Radiotherapeutisch InstituutLimburg; Tilburg, B. Verbeeten Instituut; Lausanne, Centre HospitalierUniversitaire Vaudois; Bellinzona, Ospedale San Giovanni; Toronto,Princess Margaret Hospital; Haifa, Rambam Medical Hospital;Jerusalem, Hadassah University Hospital; Tel Aviv, Tel AvivMedical Center–Ichilov Hospital; Valencia, Instituto Valencianode Oncologia; and Portsmouth, St. Mary's Hospital.
The following EORTC Genitourinary Group institutions participatedin this study: Maastricht, Akademisch Ziekenhuis; Rotterdam,Zuiderziekenhuis; Brussels, Akademisch Ziekenhuis; Kortrijk,St. Maarten Hospital; Leuven, Universitair Ziekenhuis Sint Rafael;Antwerp, Universitair Ziekenhuis; Rome, Ufficio Sternberg &Pansadoro; Malta, St. Luke's Hospital; Newcastle-upon-Tyne,Freeman Hospital; Obninsk, Medical Radiological Research Center;and Oslo, Norwegian Radium Hospital.
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= 0.05, 
= 0.2). Survival curves were estimated by using the Kaplan–Meier technique.13 All comparisons were made by means of a two-sided log-rank test with a 0.05 significance level.14 Data were analyzed according to the intention-to-treat principle. 
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