Postoperative Radiotherapy in High-Risk Premenopausal Women with Breast Cancer Who Receive Adjuvant Chemotherapy
Marie Overgaard, M.D., Per S. Hansen, M.D., Jens Overgaard, M.D., Carsten Rose, M.D., Michael Andersson, M.D., Flemming Bach, M.D., Mogens Kjaer, M.D., Carl C. Gadeberg, M.D., Henning T. Mouridsen, M.D., Maj-Britt Jensen, M.Sc., Karin Zedeler, M.Sc., for The Danish Breast Cancer Cooperative Group 82b Trial
Background Irradiation after mastectomy can reduce locoregionalrecurrences in women with breast cancer, but whether it prolongssurvival remains controversial. We conducted a randomized trialof radiotherapy after mastectomy in high-risk premenopausalwomen, all of whom also received adjuvant systemic chemotherapywith cyclophosphamide, methotrexate, and fluorouracil (CMF).
Methods A total of 1708 women who had undergone mastectomy forpathological stage II or III breast cancer were randomly assignedto receive eight cycles of CMF plus irradiation of the chestwall and regional lymph nodes (852 women) or nine cycles ofCMF alone (856 women). The median length of follow-up was 114months. The end points were locoregional recurrence, distantmetastases, disease-free survival, and overall survival.
Results The frequency of locoregional recurrence alone or withdistant metastases was 9 percent among the women who receivedradiotherapy plus CMF and 32 percent among those who receivedCMF alone (P<0.001). The probability of survival free ofdisease after 10 years was 48 percent among the women assignedto radiotherapy plus CMF and 34 percent among those treatedonly with CMF (P<0.001). Overall survival at 10 years was54 percent among those given radiotherapy and CMF and 45 percentamong those who received CMF alone (P<0.001). Multivariateanalysis demonstrated that irradiation after mastectomy significantlyimproved disease-free survival and overall survival, irrespectiveof tumor size, the number of positive nodes, or the histopathologicalgrade.
Conclusions The addition of postoperative irradiation to mastectomyand adjuvant chemotherapy reduces locoregional recurrences andprolongs survival in high-risk premenopausal women with breastcancer.
Randomized clinical trials have established that adjuvant chemotherapyor hormonal treatment prolongs the survival of patients withbreast cancer.1,2,3,4 As a result of these studies, large numbersof women with breast cancer now receive one or both of thesetreatments postoperatively. A number of randomized trials havealso shown that overall survival in patients with small tumorswas the same whether they were treated with limited surgeryplus irradiation or total mastectomy.5,6,7 For this reason,many patients are now treated locally with conservative measures,such as lumpectomy plus axillary dissection and irradiationto residual breast tissue; some also receive adjuvant systemictherapy. Total mastectomy, however, is still the treatment ofchoice for many patients, especially those with more diffuselocal disease. The role of radiotherapy after mastectomy hasbeen evaluated in several randomized trials.6,8,9 Overall, thesestudies have shown a significant reduction in locoregional recurrenceswith postoperative irradiation but no improvement in long-termsurvival, irrespective of nodal status.
Radiotherapy has been evaluated mainly in trials in which chemotherapywas not given. The widespread use of adjuvant chemotherapy callsfor a reassessment of radiotherapy, because the efficacy ofsystemic therapy in preventing local or regional recurrenceafter mastectomy is only moderate,10 and it is not clear whetherlocal or regional control is required for prolonged survivalin patients who also receive adjuvant chemotherapy.
Our aim was to evaluate whether the addition of radiotherapyto total mastectomy with axillary dissection and adjuvant chemotherapyinfluenced locoregional control of tumors, the likelihood offreedom from distant metastases, and overall survival in high-riskpremenopausal patients.
Methods
Protocol Design
The Danish Breast Cancer Cooperative Group protocol 82b includespremenopausal high-risk patients with breast cancer.1,11 High-riskstatus was defined as consisting of one or more of the following:involvement of axillary lymph nodes, a tumor size of more than5 cm, and invasion of the cancer to skin or pectoral fascia(pathological stage II or III). A woman was considered premenopausalif she had had amenorrhea for less than five years or had hada hysterectomy before the age of 55.
To be eligible for the study a woman had to have no evidenceof metastatic disease as determined by physical examination,biochemical tests, chest radiography, bone scintigraphy, orbone radiography and no other previous or concomitant malignantdisease. The study was approved by the national ethics committee,and oral informed consent was mandatory. The departments responsiblefor systemic treatment and follow-up used a closed-envelopesystem to randomize eligible patients. No stratification intoprognostic subgroups was performed before randomization.
We recruited patients from November 1982 to December 1989. Aftersurgery, they were randomly assigned to radiotherapy plus cyclophosphamide,methotrexate, and fluorouracil (CMF); CMF alone; or CMF plustamoxifen. Because of a higher-than-expected rate of mortality,enrollment in the third subgroup was stopped in June 1986, asdescribed elsewhere.1 This report will address only the resultsin the first two groups.
Surgery and Histopathological Analysis
The primary surgical treatment, performed at 79 surgical departments,was total mastectomy and axillary-node dissection.12 The pectoralfascia was stripped, but neither the major nor the minor pectoralmuscles were removed. Axillary dissection included removal ofthe central axillary lymph nodes involving level I and partof level II. Overall, a median of seven lymph nodes were removed.
The histopathological examination was performed according toa standardized procedure by the 29 pathology departments participatingin the trial. Microscopical examination included tumor classificationaccording to the World Health Organization (WHO) standards13and histopathological classification according to the systemof Bloom and Richardson.14 Grading of anaplasia was performedonly in ductal carcinomas. The pathologist recorded the numberof lymph nodes identified in the specimen, as well as the grosstumor size and whether there was invasion of the tumor intoskin or deep fascia.
Radiotherapy
Radiation therapy was delivered to the chest wall, includingthe surgical scar and regional lymph nodes (i.e., supraclavicular,infraclavicular, and axillary nodes as well as internal mammarynodes in the four upper intercostal spaces).15 The intendeddose was a median absorbed dose in the target volume of either50 Gy, given in 25 fractions over a period of 5 weeks, or 48Gy, given in 22 fractions over a period of 5 1 / 2 weeks, accordingto report 29 of the International Commission on Radiation Unitsand Measurements.15 The recommended field arrangement involvedthe use of an anterior photon field against the supraclavicular,infraclavicular, and axillary regions and an anterior electronfield against the internal mammary nodes and the chest wall.The use of posterior axillary fields was advised in patientsin whom the ratio of the anterior to posterior diameter wastoo large to limit the maximal absorbed dose to 55 Gy (givenin 25 fractions) or 53 Gy (given in 22 fractions). Most of thepatients were treated at the six departments that used a linearaccelerator, but 64 patients (7.5 percent) were treated at smalldepartments that used 250-kV x-ray machines and the McWhirthertechnique.16 In these patients the minimal intended dose was36 Gy given in 20 fractions over a period of four weeks. Compliancewith radiotherapy was high; only 32 patients (3.8 percent) didnot receive the planned treatment.
Adjuvant Systemic Therapy
A combination of cyclophosphamide (600 mg per square meter ofbody-surface area), methotrexate (40 mg per square meter) andfluorouracil (600 mg per square meter) was given intravenouslyevery four weeks, with the first cycle beginning two to fourweeks after surgery. Patients who were randomly assigned toradiotherapy plus CMF started radiotherapy within one week afterthe first cycle of chemotherapy. They completed the treatmentwithin five weeks and, after a rest of one to two weeks, continuedwith the CMF regimen, which was repeated every four weeks. Thus,for these patients the planned chemotherapy consisted of eightcycles of CMF, whereas the patients who were assigned to CMFwithout radiotherapy were given a total of nine cycles of CMF.Compliance with chemotherapy was the same in both groups, andat least 85 percent of the patients received the planned numberof CMF cycles.
Follow-Up
The patients were followed with clinical examination at regularintervals for up to 10 years and further tested only if theyhad symptoms or evidence of recurrent disease.
Statistical Analysis
All diagnostic, therapeutic, and follow-up data were validatedand processed by the Danish Breast Cancer Cooperative Group'sdata center.11,17 The protocol did not call for an interim analysis,but the study was monitored regularly by the data center forexcess mortality in either treatment group. To optimize thequality of the data, all events recorded by the data centerthrough June 1992 were cross-checked with hospital records throughoutthe country to ensure correct recording of the site or sitesof the first relapse.
Locoregional recurrence was defined as the appearance of localor regional tumor (in the chest wall, axilla, or supraclavicularor infraclavicular area) alone or together with distant metastases(diagnosed within one month after the initial finding of recurrence).Any recurrence that occurred after the first relapse was notincluded. Disease-free survival was defined as the durationof survival without locoregional recurrence or distant metastases,cancer in the opposite breast, or other malignant disease. Overallsurvival was calculated as the length of time until death, irrespectiveof cause. The lengths of time until treatment failure were measuredfrom the date of mastectomy.
The recording of only the first recurrence and not of subsequentrecurrences (local, regional, or distant) implies that an estimationof the time to locoregional recurrence would be categorizedas an analysis of competing risks. However, the effects of radiotherapyon locoregional recurrence and distant metastases cannot beassessed separately. Any analysis of locoregional recurrencetherefore involves analyzing the time to the first recurrence(at any site) and the percentages of patients with locoregionalrecurrences and distant metastases. The latter are analyzedas simple proportions because the lengths of follow-up and theway censoring was performed in the two groups were similar.18These values were compared by chi-square tests and risk ratios.We used the life-table method to estimate the probability oftreatment failure for the end points of disease-free survivaland overall survival, and we used the log-rank test for comparison.
We used a multivariate Cox proportional-hazards analysis toevaluate prognostic variables and treatments with respect todisease-free survival and overall survival. Statistical analysiswas performed by the likelihood-ratio test. Because of the lackof proportionality, the analysis was stratified with respectto histopathological findings: ductal, lobular, or medullarycarcinoma. Furthermore, the last two histopathological typescould not be graded with respect to anaplasia,14 but in themultivariate analysis they were designated as grade I anaplasia.The Cox model was further applied to test whether radiotherapysignificantly affected the prognostic variables.
All the estimated P values are two-tailed. Statistical analysiswas performed with the SAS 6.11 program package.
Treatment effect was evaluated according to the intention-to-treatprinciple, and all the patients were included in their randomizationgroup irrespective of whether they completed the planned treatment.The date for the evaluation of recurrence and survival was September1, 1996, so that the median potential follow-up was 114 months(range, 78 to 167).
Results
Of the 1789 patients who underwent randomization, 81 (34 assignedto radiotherapy plus CMF and 47 assigned to CMF alone) weresubsequently found to be ineligible by the data center and wereexcluded. The reasons for exclusion were the patient's inclusionin another protocol, the occurrence of distant metastases, thepresence of other malignant conditions, or the patient's refusalto participate in the study. These patients were included onlyin the analysis of survival. Of the remaining 1708 premenopausalpatients, 852 were randomly assigned to postmastectomy irradiationplus CMF and 856 to CMF alone. Table 1 gives the characteristicsof the patients.
Table 1. Frequency of Locoregional Recurrences or Distant Metastases in Women Treated with Radiotherapy and CMF or CMF Alone after Mastectomy.
By the time of the analysis (median follow-up, 114 months),the disease had recurred in 858 patients (Table 2) and 842 patientshad died. The probability of disease-free survival was significantlyhigher in the group that received radiotherapy plus CMF thanin the group treated only with CMF (Figure 1 and Table 3). Thetype of first recurrence differed significantly in the two groups(P<0.001): Locoregional recurrence was significantly morefrequent in the group treated with CMF alone, whereas distantmetastases were more frequent in the group treated with radiotherapyplus CMF (Table 2). The relative risk of locoregional recurrenceas a first event among patients treated with CMF alone was 3.7(95 percent confidence interval, 2.9 to 4.7), and the relativerisk of distant metastases as a first event was 0.8 (95 percentconfidence interval, 0.7 to 0.9). The estimated overall survivalafter 10 years was 54 percent (95 percent confidence interval,51 to 58 percent) in the group assigned to radiotherapy plusCMF, as compared with 45 percent (95 percent confidence interval,42 to 48 percent) in the group assigned to CMF alone (Figure 2).
Figure 2. Kaplan–Meier Estimates of Overall Survival among Women Treated with Radiotherapy plus CMF and CMF Alone.
Values in parentheses are overall survival at 10 years.
Our results confirm that tumor size, the number of pathologicnodes, and the grade of anaplasia are the major prognostic factorsin breast cancer (Table 1 and Table 3). We could not identifyany subgroups in which the effect of radiotherapy was particularlybeneficial.
We estimated that locoregional recurrences were the only causeof a first relapse in 80 percent of patients who received onlyCMF postoperatively, whereas in the group given radiotherapyand CMF, 41 percent of the patients who relapsed with locoregionalrecurrences also had distant metastases (31 of 75 patients)(Table 2). Table 1 shows that the addition of irradiation tochemotherapy reduced the frequency of locoregional recurrenceto about one-fourth that found in the groups that did not receiveradiotherapy. Table 1 also shows that the frequency of locoregionalrecurrences increased with the size of the tumor, the numberof positive nodes, and the grade of anaplasia, irrespectiveof treatment.
The results of multivariate Cox regression analyses, with anytype of recurrence or death or death from any cause used asend points, are shown in Table 4. The size of the primary tumor,the frequency and number of positive lymph nodes, the histopathologicalgrade, the use of radiotherapy, and age were all significantindependent predictors of outcome. No significant interactionsbetween radiotherapy and these prognostic signs were found —that is, the beneficial effect of radiotherapy on both disease-freeand overall survival applied to all subgroups.
Table 4. Cox Multivariate Proportional-Hazards Analysis of the Relative Risk of Any Type of Recurrence or Death or of Death from Any Cause.
Discussion
Our results indicate that the addition of radiotherapy to adjuvantchemotherapy after total mastectomy and axillary dissectionreduces locoregional recurrences and improves survival. Previousstudies of radiotherapy, which included only small numbers ofpatients (approximately one-fifth the number enrolled in thepresent study), showed improvement in the control of locoregionaltumors19,20,21,22,23,24,25,26 and suggested improvement in survival.23,24,25,26
Although our protocol carefully described recommendations forthe surgical procedure,12 there might have been important variationsin the extent of the surgery performed among the 79 departmentsthat enrolled patients in the study. Our surgeons found relativelyfew lymph nodes in the axilla (median, seven nodes), but thenumber also relies on the pathologist who counted the lymphnodes in the specimen. The fact that 255 patients had fewerthan four nodes removed weakens our analysis of the influenceof having more than three positive nodes in the study group.Although we included the frequency of positive nodes in theanalysis of prognostic factors, the importance of the numberof nodes removed is difficult to assess, since in some patientsmany nodes were removed because they were clinically involved,whereas in others many nodes were removed by a careful surgeon.
The problem of local recurrence is not related solely to themanagement of the axilla, since more than half of the recurrenceswere on the chest wall.15 Recurrences on the chest wall andin the axilla (without concomitant distant metastases) weretreated with curative intent. Most patients who did not receiveradiotherapy were treated with resection of the recurrent tumorfollowed by radiotherapy, whereas patients who had receivedradiotherapy were treated with surgery alone. The significantdifference in overall survival between the group treated withradiotherapy plus CMF and the group given CMF alone indicatesthat second-line treatment cannot compensate for inadequateprimary therapy.
The type and dose intensity of adjuvant chemotherapy are alsoimportant.4,27 The dose intensity with 8 or 9 cycles of CMF(given at four-week intervals) that was used in this trial islower than the usual course of 12 cycles4 — a number thatwas also used in the previous Danish Breast Cancer CooperativeGroup trial (protocol 77).1 This reduction may decrease overallsurvival, but it is not likely to change our conclusion. Thefact that patients given combined treatment received only eightcycles of CMF, with a long interval between the first and thirdcycles, might have reduced the benefit of radiotherapy plusCMF. The guidelines for irradiation after mastectomy were basedon experience from previous trials involving protocol 77,15but CMF was given simultaneously with radiotherapy in protocol77, whereas it was given sequentially in the present trial todecrease the early and late reactions in normal tissues.28
Recording of short-term and long-term complications was plannedprospectively in all patients, but the data are incomplete andwe continue to record long-term complications. We can roughlyestimate cardiotoxicity by comparing the survival rates afterradiotherapy among patients with cancer of the left breast andthose with cancer of the right breast. There is no evidenceof a higher rate of death among patients with left-sided tumors,after a median follow-up of almost 10 years. Longer follow-upand more detailed analysis of the actual dose to the heart areneeded before final conclusions can be made on this end point.
The decentralized randomization procedure resulted in the enrollmentof 81 ineligible patients. However, the inclusion of these patientsdid not influence overall survival rates (the 10-year actuarialvalue being 54 percent in the group assigned to radiotherapyplus CMF and 44 percent in the group assigned to CMF alone,P<0.001).
Our study strongly indicates that optimal results of the treatmentof high-risk breast cancer can be achieved only by controllingboth locoregional and systemic tumors. With current surgicalmethods of treatment, radiotherapy seems required for adequatelocoregional control in high-risk premenopausal patients. However,the optimal balance between surgery, radiotherapy, and adjuvantchemotherapy in high-risk patients with breast cancer has notyet been found.
Source Information
From the Department of Oncology, Aarhus University Hospital, Aarhus (M.O.); the Department of Medicine, Viborg County Hospital, Viborg (P.S.H.); the Danish Cancer Society and the Department of Experimental Clinical Oncology, Aarhus University Hospital, Aarhus (J.O.); the Department of Oncology, Odense University Hospital, Odense (C.R.); the Department of Oncology, Rigshospitalet, Copenhagen (M.A., H.T.M.); the Department of Oncology, Copenhagen University Hospital, Herlev (F.B.); the Department of Oncology, Aalborg County Hospital, Aalborg (M.K.); the Department of Oncology, Vejle County Hospital, Vejle (C.C.G.); and the Danish Breast Cancer Cooperative Group Secretariat, Rigshospitalet, Copenhagen (H.T.M., M.-B.J., K.Z.) — all in Denmark.
Address reprint requests to Dr. Overgaard at the Department of Oncology, Aarhus University Hospital, Nørrebrogade 44, Bldg. 5, DK-8000 Aarhus C, Denmark.
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Radiotherapy and Chemotherapy in High-Risk Breast Cancer
El-Tamer M., Homel P., Braverman A. S., Wolberg W. H., Robins H. I., Goldhirsch A., Coates A. S., Colleoni M., Gelber R. D., Raffle A.E., Evans R. A., Overgaard M., Rose C., Mouridsen H., Ragaz J., Jackson S. M., Spinelli J. J., Hellman S.
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338:329-333, Jan 29, 1998.
Correspondence
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