메인 International Journal of Radiation Oncology*Biology*Physics Are cosmetic results following conservative surgery and radiation therapy for early breast cancer...
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Ini J. Rediorion Onmlo~.v Em/. Ph.w Vol. Printed in the U.S.A. All rights reserved. 23, pp. 925-93 I 0360-3016/92 $5.00 + .oO Copyright 0 1992 Pergamon Press Ltd. ??Clinical Original Contribution ARE COSMETIC RESULTS FOLLOWING CONSERVATIVE SURGERY AND RADIATION THERAPY FOR EARLY BREAST CANCER DEPENDENT ON TECHNIQUE? ANNE DE LA ROCHEFORDI~RE, FRANK VICINI, M.D., M.D., ANTHONY L. ABNER, M.D., BARBARA SILVER, B.A., ABRAM RECHT, M.D. AND JAY R. HARRIS, M.D. Joint Center for Radiation Therapy, Department of Radiation Oncology, Harvard Medical School, Boston, MA To assess the cosmetic results in relation to treatment technique, we retrospectively reviewed the results for 1159 Stage I-II breast cancer patients treated with conservative surgery and radiotherapy between 1970-1985. All patients underwent gross excision followed by radiation therapy including au implant or electron beam boost. The total dose to the primary site was 2 60 Gy. Because of technical modifications introduced over time after 1981, the population was divided arbitrarily into two cohorts: 504 patients treated through 1981 and 655 treated between 1982-1985. Median follow-up times for surviving patients in the two cohorts were 107 months and 67 months, respectively. Cosmetic outcome was evaluated by the examining physician and scored as excellent, good, fair or poor. Excellent results at 5 years were scored in 59% of early cohort patients and 74% of the latter cohort (p = 0.002). Acceptable results (either good or excellent) were seen in 84% and 948, respectively (p = 0.02). In the latter cohort, the likelihood of achieving an excellent result, but not an acceptable result, was significantly related to the volume of resected breast tissue and the use of chemotherapy. The number of fields (three-field technique, provided that fields are precisely matched, compared to tangents only) and boost type (implant vs electrons) did not influence the cosmetic outcome. We conclude that our current technique using breast RT to 45- 46 Gy and a boost ; to the primary site of 16-18 Gy is associated with a high likelihood of acceptable cosmetic results and that this likelihood is not diminished by the use of adjuvant chemotherapy, a large breast resection, the use of a third field, or boost type. Breast cancer, Conservative Surgery, Radiotherapy, Cosmesis. INTRODUCIION precise matching of the tangential fields and the anterior field to treat the axillary and/or supraclavicular region, and the use of a large volume boost or a boost dose greater than 18 Gy. Based on these findings, a number of treatment modifications were introduced over time at our institution beginning in 1982. Sufficient time has now transpired to allow us to assess the results of these modifications. Thus, in this article, we divided arbitrarily the entire population into two cohorts of patients. We compare the cosmetic results in patients treated prior to 1982 to those in patients treated between 1982 and 1985, and assess treatment factors which are now associated with a worsening of the cosmetic appearance given these treatment modifications. This information, along with information on factors associated with local recurrence and complications, may be useful in providing patients with an improved technique of breast-conserving treatment. Both retrospective (2, 6, 10, 16, 21, 24) and randomized clinical trials (9, 25,27) have established that breast-conserving treatment (consisting of conservative surgery and radiation therapy) and mastectomy result in equivalent survival rates. Given this, the principal goals of breastconserving treatment are to use techniques of surgery and radiation therapy which will provide a high level of local tumor control, a low incidence of complications, and preservation of a satisfactory cosmetic appearance. Studies from our institution (3, 13, 18) and others (5, 7, 8, 11, 22,29) have analyzed the results in treated patients in an attempt to better achieve these goals. In particular, we have previously identified a number of radiation treatment factors associated with a worsening of the cosmetic result. These include the use of doses to the whole breast greater than 50 Gy, fraction sizes greater than 2 Gy per day, im- Presented at the 33rd Annual Meeting of the American Society for Therapeutic Radiology and Oncology, Washington, November 199 1. Reprint requests to: Jay R. Harris, M.D., Joint Center for Radiation Therapy, 50 Binney St., Boston, MA 02 115. Accepted for publication 2 1 February 1992. DC, 925 926 I. J. Radiation Oncology 0 Biology 0 Physics METHODS AND MATERIALS Between 1968 and 1985, a total of 1624 women with UICC-AJCC clinical Stage I or II unilateral invasive breast carcinoma were treated with conservative surgery (CS) and radiation therapy (RT) at the Joint Center for Radiation Therapy (JCRT). Of these, 1360 underwent gross excision of the tumor and received a total dose to the primary tumor site of greater than or equal to 60 Gy using either an interstitial implant or an electron boost. Two hundred and one patients were excluded from the cosmetic analysis because cosmetic follow-up was not undertaken at this institution. The study population thus consisted of 1159 patients, all of whom were treated after January 1970. A total of 504 patients were treated through 1981 (“earlier cohort”) and 655 were treated between I982 and 1985 (“latter cohort”). The patient characteristics and treatment factors for patients treated in the two time periods are shown in Table 1. In aggregate, there were 679 T 1 tumors (59%) and 480 T2 tumors (410/o),and this distribution was similar in the two time intervals. All patients underwent a complete gross tumor excision, but the total amount of tissue removed at surgery varied from an excisional biopsy, removing the tumor surrounded by a small margin of normal tissue, to a wide local excision, sometimes achieved by a re-excision. Thirty-three patients (7%) had a re-excision in the earlier cohort whereas 245 patients (37%) underwent re-excision in the latter cohort (p < 0.0001). The volume of breast tissue resected was quantified for 44 1 of the 655 patients (67%) in the latter cohort, by multiplying the length by the width by the depth of the resected breast specimen as recorded on the pathology report. If more than one specimen was received, the volumes were calculated separately and then summed. Patients were divided into three groups of equal numbers based on the volume of breast tissue resected (I 35 cm’, 36-85 cm3, and 2 86 cm3). The median volume of breast tissue resected was 40 cm3 (range, 0.4-443 cm3> for Tl tumors, 60 cm3 (range, 4.5-651 cm3) for T2 tumors less than or equal to 3 cm, and 85 cm3 (range, 8-315 cm”) for T2 tumors greater than 3 cm. Table 1. Treatment 1970-1981 No. patients Axill. diss. Reexcision Adj. CT 6orSMV 3-field Implant Whole breast dose <50Gy Boost dose > 18 Gy characteristics 1982-1985 p value 504 77% 7% 24% 4% 85% 95% 655 79% 37% 27% 27% 55% 47%) NS < 0.000 NS < 0.000 < 0.000 i 0.000 67% 85% 95% 42% < 0.000 1 < 0.000 1 Axill. diss. = Axillary dissection; motherapy. Adj. CT = Adjuvant 1 1 I 1 che- Volume 23. Number 5. 1992 Axillary dissection was performed in 77% of patients in the earlier cohort and 79% of the latter cohort (p = ns). The dissections, in general, were limited to removal of level I and II lymph nodes. Positive nodes were found in 35% of patients (135/390) in the earlier group and 38% of patients ( 197/520) in the latter group (p = ns). During the earlier time interval, 38 1 patients received RT alone and 123 patients (24%) were given adjuvant chemotherapy. During the latter period, 481 women received RT alone, and 174 patients (27%) underwent RT and adjuvant chemotherapy. In 8 1 cases (42 in the earlier cohort and 39 in the latter one), radiation and chemotherapy were delivered concurrently. Since we had demonstrated in a previous study that concurrent chemotherapy has an adverse effect on cosmetic outcome (12) those patients were excluded from the cosmetic analysis. Between 1970 and 198 1,483 patients were treated with a 4 MV linear accelerator and 21 women (4%) on a 6 or 8 MV machine. Between 1982 and 1985, 467 women were treated with 4 MV and 169 (27%) with 6 or 8 MV. The machine energy was not recorded for 19 patients in the latter group. The volume irradiated with external beam treatment varied considerably during the 15 years of the study. Between 1970 and 198 1, 429 patients (85%) received irradiation to the breast and regional nodes, usually with a three-field technique, irrespective of whether an axillary dissection was performed or not. Between 1982 and 1985, patients less commonly had lymph node irradiation. In general, patients without metastases to axillary nodes were treated with tangential breast irradiation only. In addition, in this period, the three-field technique was modified to provide a more accurate match between the opposed tangential fields which treated the breast and the direct anterior field which treated the nodes (26). The median dose to the breast was 46 Gy (range, 3852 Gy) in the time-period 1970-81. One hundred sixtyseven patients (33%) received a breast dose 2 50 Gy. Between 1982 and 1985, the median dose to the breast was 46 Gy (range, 38-51 Gy), but only 32 patients (5%) received a dose r 50 Gy. Also, in the latter time interval, patients treated with adjuvant therapy more commonly received 1.8 Gy 5 times per week for a total dose of 45 Gy, rather than 2 Gy 5 times per week for a total dose of 46 Gy. All patients received an additional dose (“boost”) to the primary site. Iridium 192 interstitial implant was used for 95% of patients in the early period and for 47% of patients treated between 1982 and 1985. Other patients received an electron beam boost with energies ranging from 7 to 11 MeV selected so that the 80% isodose curve would encompass the boost volume. No patient in this series received both interstitial and electron beam boost. The median boost (electron or implant) dose was 20.80 Gy in the earlier cohort (range, 10-27.6 Gy) and 18 Gy in the latter cohort (range, lo-24 Gy). Of note, 85% of patients (430/504) treated in the earlier time interval received more than 18 Gy by boost, compared to 42% 927 Cosmetic results following CS and RT 0 A. DE LA R~CHEFORDI~RE etal. of patients (272/655) treated in the second period (p < 0.0001). The median implant dose was 20.7 Gy in the earlier group (range, 10-27.6 Gy) and 20 Gy (range, 11.1-24 Gy) in the latter group. The implant boost dose was greater than or equal to 24 Gy for 5% of patients treated in the earlier period and 0.3% of patients in the later period. Follow-up was generally performed at 6-month intervals after completion of the treatment. Patients were censored from cosmetic follow-up at the time of local or distant failure or the diagnosis of opposite breast cancer. The median follow-up time for surviving patients was 107 months (range, 52-2 19) for the earlier cohort and 67 months (range, 12-94) for the latter one. Overall cosmetic results were classified as excellent, good, fair, or poor by the examining physician. An “excellent” score was assigned when the treated breast looked essentially the same as the opposite breast. A “good” cosmetic score was used to describe minimal but identifiable effects of treatment. An “acceptable” result was defined as either an “excellent” or a “good” result. A “fair” cosmetic score was given when significant effects of radiation on the breast were noted. A “poor” cosmetic score was used to describe severe normal tissue sequelae. An “unacceptable” result was defined as either a “fair” or a “poor” score. The cosmetic results were plotted graphically by grouping observations into 12-month intervals. If more than one observation was made on the same patient during a time-interval, the worst observation was scored. The midpoint of each time interval was used in all curves, thus individual observations ranged up to 6 months on either side of each time point. Analysis and comparisons between subgroups were performed at the specific time points of 3 and 5 years because we have previously demonstrated that results tend to stabilize at about 3 years (3). Statistical comparisons between groups and proportions were calculated at fixed points using the Fisher exact test, and p values of 0.05 or less were considered statistically significant. RESULTS We compared the overall cosmetic outcome during the two treatment time-periods ( 1970-8 1 and 1982-85). The results were significantly better at both 3 and 5 years for the patients treated with the techniques used in the latter period. An excellent result at 3 years was scored for 58% of the 330 patients in the earlier cohort evaluated at that time-point, compared with 73% of the 352 patients in the latter cohort (p < 0.0001). An acceptable result (either excellent or good) was scored in 86% and 96% of patients, respectively (p < 0.0001). Fair results were seen in 10% and 3.5%, and poor results in 4% and 0.5%, respectively (p < 0.000 1). At 5 years, excellent results were scored for 59% of the 204 patients evaluated in the earlier cohort compared with 74% of the 221 patients evaluated in the latter group (p = 0.002). Acceptable results were found in 84% and 94% (p = 0.002) (Fig. I), fair results in 11% and 5% (p = 0.04), and poor results in 5% and l%, respectively (p = 0.03). Of note, the 5-year actuarial rate of recurrence in the treated breast was 10% for patients treated between 1970-8 1 and 8% for patients treated between 1982-85 (p = ns). We then focused on the patients treated in the more recent period to determine the influence of various treatment factors on the cosmetic outcome (Table 2). Patients in the 1982-85 cohort who received adjuvant chemotherapy (given sequentially) were less likely to have excellent cosmetic scores than patients who did not receive adjuvant chemotherapy (Fig. 2). At 3 years, 77% of patients (214/279) who did not receive chemotherapy had 04 I 12 24 Fig. 1. Percentage of excellent or good cosmetic p < 0.000 1. At 5 years: p < 0.002. 36 MONTHS 48 60 72 results for patients treated during the two time-periods. At 3 years: 928 1. J. Radiation Oncology 0 Biology 0 Physics Table 2. Factors influencing outcome at 3 years (1982- 1985) % excellent 279 57 77 65 0.09 97 95 NS 85 78 86 78 0.0009 96 97 NS 70 141 45 51 84 68 0.03 94 99 91 NS 21 62 TTV I 35 cm3 TTV = 36-85 cm3 TTV 2 86 cm3 T<2cm,noCT T=2.1-3cm,noCT Tr3.1cm,noCT = Sequential cosmetic No. of patients evaluated at 3 yrs. RT alone Seq. RT/CT Seq. RT/CT Volume 23, Number 5, 1992 radiotherapy/chemotherapy; p-value % excellent/good 100 TTV = Total tissue volume resected; T = Tumor size. cm3 had excellent results (p < 0.000 1). Acceptable results were seen in 97% and 94% of patients, respectively. Similar scores were observed when the analysis was limited to patients treated without chemotherapy. At 3 years, 85% of patients ( 11O/ 129) with volumes of resected breast tissue less than or equal to 85 cm3 and 56% of patients (28/50) with volumes greater than or equal to 86 cm3 had excellent results (p < 0.000 1). Acceptable results were seen in 98% of both groups. There were insufficient patients treated with chemotherapy to permit analysis of the effect of volume of excision in that group. Among patients who did not receive adjuvant chemotherapy, the likelihood of an excellent cosmetic result at 3 years was lower for patients with tumors clinically larger than 2 cm than for patients with tumors less than or equal to 2 cm (Table 2). We did not observe the same effect of tumor size on the cosmetic result for patients treated with sequential RT/CT but the number of patients with cosmetic evaluation at 3 years was small. In this excellent scores compared to 65% of patients (37/57) who were given sequential RT/CT (p = 0.09). At 5 years, the corresponding scores were 80% and 54%, respectively (p = 0,007). However, there was no difference in the percentage of acceptable results between the two groups of patients at either 3 years (97% vs 95%) or 5 years (95% vs 88%). We examined the likelihood of an excellent cosmetic result in relation to the volume of resected breast tissue. There was no significant difference in overall cosmetic results between women with resected volumes less than or equal to 35 cm3 and those with resected volumes between 36 and 85 cm3. For patients with resected volumes greater than or equal to 86 cm3, the likelihood of an excellent result at 3 years was significantly lower compared with patients with resected volumes less than or equal to 85 cm3. At 3 years, 82% of patients ( 134/ 163) with resected volumes less than or equal to 85 cm3 and 5 1% of patients (36/70) with resected volumes greater than or equal to 86 100 RT 90 01 SEP. 12 24 36 48 ONLY RTlCT 60 MONTHS Fig. 2. Percentage of excellent At 3 years: p = 0.09. or good cosmetic p-value results related to the use of adjuvant chemotherapy (1982- 1985). Cosmetic results following CS and RT 0 A. DE LA ROCHEFORDIZRE 929 ef al. Table 3. Factors not influencing cosmetic outcome at 3 years (1982-1985) No. of patients evaluated at 3 yrs. % excellent p-value 122 157 80 75 NS 96 98 NS 37 20 62 70 NS 95 95 NS 145 192 79 73 NS 95 97 NS 74 76 Three-field, no CT Two-field, no CT Three-field seq. RT/CT Two-field RT/CT seq. Implant boost Electron boost BD = 45 Gy, no CT (1.8 Gy X 25 fractions) BD = 46 Gy, no CT (2.0 Gy X 23 fractions) BD = 45 Gy, seq. RT/CT (1.8 Gy X 25 fractions) BD = 46 Gy, seq. RT/CT (2.0 Gy X 23 fractions) % excellent/good 97 NS 156 76 25 68 NS 97 92 NS 14 Seq. RT/CT = Sequential radiotherapy/chemotherapy; p-value 43 NS 100 BD = Breast dose. analysis, the effect was likely confounded with the volume of resected breast tissue. We examined the influence of a number of other treatment factors, none of which were associated with alteration in the cosmetic result. These include 3-field technique versus tangential breast technique, the daily dose, and the type of boost (Table 3). Of note, among patients treated between 1982 and 1985, the 5-year actuarial rate of recurrence in the treated breast was 7% for patients treated with electrons and 8% for patients treated with interstitial implant. DISCUSSION The present study shows that our current technique using breast RT to 45-46 Gy and a boost to the primary site to 16-18 Gy is associated with an excellent cosmetic outcome in about 75% of patients, and acceptable results (either good or excellent) in nearly all patients. These cosmetic results are better than those we had observed in previously treated patients while maintaining an acceptably low rate of local recurrence. The modifications introduced into our current treatment technique have been largely based on the results of prior studies from our institution. In a study of the cosmetic results of patients treated with primary radiation therapy without adjuvant chemotherapy, we noted that the extent of the biopsy procedure and the technique of radiation therapy were important determinants of the cosmetic outcome. Specifically, a dose to the whole breast greater than 50 Gy, fraction size greater than 2 Gy, inaccurate matching between adjacent radiation fields and a large volume of boost irradiation all adversely affected the cosmetic outcome (13). We later demonstrated that a boost dose greater than 20 Gy, a large implant volume (measured by the number of seeds in the implant), and the use of concurrent chemotherapy and radiotherapy all adversely altered the cosmetic results ( 18). Based on these data, a variety of modifications were introduced over time. These included: (a) limiting the dose to the whole breast to 45-46 Gy (using daily dose not greater than 2 Gy), (b) using a boost dose not greater than 18 Gy, (c) providing a more accurate matching technique (26), and (d) using sequential rather than concurrent RT/CT. It is not possible to assess the relative contribution of each of these various modifications to the improvement seen in the cosmetic results in the latter cohort compared to the earlier cohort. Given our current technique, the two factors which were found to influence the cosmetic outcome were the use of chemotherapy and the volume of resected breast tissue. Our results continue to show that the use of sequential RT/CT has an adverse effect on the likelihood of achieving an excellent cosmetic outcome when compared to the use of RT alone, thus corroborating results reported by other authors (4, 8,23). However, in our cohort treated with our new technique, the likelihood of achieving an acceptable (excellent or good) result is similar for patients treated with sequential RT/CT and those who received no chemotherapy. In this analysis, we did not examine the impact of concurrent chemotherapy on cosmesis since it has been reported elsewhere ( 1, 12). In a prior study, we showed that the extent of surgical excision played a prominent role in the cosmetic outcome (18). Others have reported similar conclusions (5, 8, 22, 29). Our current data indicate that a volume of resected breast tissue greater than 86 cm3 correlates with a significantly lower likelihood of excellent cosmetic results than when smaller volumes are removed (p < 0.0001). However, the likelihood of acceptable results was, again, not modified by the extent of the surgical procedure used in this series of patients. Our study also shows that increasing 930 1. J. Radiation Oncology 0 Biology 0 Physics tumor size is negatively associated with the cosmetic outcome as reported by other authors (5, 8, 21, 22). This effect is likely due to the close relationship between the volume of breast tissue resected and the size of the primary tumor. This information on the cosmetic outcome can be used in combination with our observations on risk factors for local recurrence to draw some guidelines for clinical practice. Retrospective analyses of pathologic characteristics of the tumors of our patients has shown that only those with an extensive intraductal component (EIC, defined as intraductal carcinoma prominently present within the infiltrating borders of the tumor and also present beyond the edge of the invasive cancer in grossly normal adjacent tissue, or as diffuse intraductal carcinoma with focal invasion) are at high risk for local failure when treated with a limited breast resection prior to RT ( 14). Based on these data, we have recommended that more extensive breast resection (to obtain microscopically negative margins) be performed in patients with an EIC+ tumor by means of a re-excision. In contrast, the large majority of patients who do not have an EIC+ tumor are adequately treated with a resection which includes an excision of the tumor with a 1 cm margin of adjacent tissue, followed by breast irradiation including a boost to the primary site (28). Assessment for EIC can, therefore, be used to minimize the extent of surgery required prior to RT, thus maintaining the cosmetic appearance for the majority of patients. The results provided here indicate that in patients who require more extensive breast resection, the cosmetic result may be decreased from excellent to good, but is unlikely to be unacceptable given current techniques of treatment. In the present study, a number of treatment factors were not associated with less favorable cosmetic results. The use of a third field to treat the axillary and/or supraclavicular region was not associated with a worse cosmetic outcome in these patients who were treated using a precise technique of matching adjacent fields. We have, however, recently reported that the use of a third field is associated with an increased rate of pneumonitis (15) and brachial plexopathy (20), a finding which should be considered in assessing the value of adding this third field for an individual patient. Of note as well, no difference was found in terms of the cosmetic results between patients treated Volume 23, Number 5, 1992 with an electron beam boost and those who received interstitial implantation. Local recurrence rates were also similar for the two groups. A choice between electron beam irradiation and interstitial implantation should, therefore, depend on other factors such as cost, convenience, availability and expertise in the use of the two techniques (11). It has been our clinical impression that patients tolerate electron beam considerably better than they do interstitial implantation and that electron beam is associated with less fat necrosis (which may make follow-up examination more difficult). As a result, we now routinely use electron beam for boosting the dose in patients with Stage I or II breast cancer. There are some limitations of this study which we would like to acknowledge. One is the subjective nature of the cosmetic scores used. It is possible that scoring criteria differed significantly between observers or changed over time ( 19). Another limitation of this study is that we were not able to obtain cosmetic evaluations for all of our treated patients. The patients who were not evaluated may differ in their cosmetic outcome from the patients who were evaluated. In many cases, the inability to obtain cosmetic follow-up was related to a patient’s move to a different part of the country. It could be argued, however, that patients who were not followed may have had cosmetic problems, were unhappy with the results of their treatment, and were less likely to see their physicians. Alternatively, it could be argued that patients who were doing well and had only minor or no cosmetic problems, might be less inclined to come for follow-up evaluation. At this time, we are not able to assess the impact of this limitation in patient follow-up. The choice of local therapy for women with Stage I and II breast cancer depends on various clinical, histologic and psychological factors (17). The results presented here indicate that improvements in the technique of irradiation have resulted in excellent or good cosmetic results in nearly all patients. In addition, our results indicate that certain treatment factors, such as the need for extensive surgery or adjuvant CT, can decrease the likelihood of an excellent, but not an acceptable, cosmetic result. 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