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DOI: 10.1148/radiol.2253011913
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(Radiology 2002;225:713-718.)
© RSNA, 2002

Radiation Oncology

Locally Recurrent Breast Cancer: Pulse Dose Rate Brachytherapy for Repeat Irradiation Following Lumpectomy—A Second Chance to Preserve the Breast1

Alexandra Resch, MD, Claudia Fellner, PhD, Ulrike Mock, MD, Leonore Handl-Zeller, MD, Eva Biber, MD, Wolfgang Seitz, MD and Richard Pötter, MD

1 From the Department of Radiotherapy and Radiology (A.R., U.M., L.H.Z., E.B., W.S., R.P.), Division of Medical Physics (C.F.), Vienna University, Währinger Gürtel 18-20, 1090 Vienna, Austria. From the 2001 RSNA scientific assembly. Received November 27, 2001; revision requested January 9, 2002; revision received April 9; accepted June 14. Address correspondence to A.R. (e-mail: alexandra.resch@univie.ac.at).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To perform and assess the effectiveness of local excision of recurrent tumor followed by postoperative pulse dose rate (PDR) brachytherapy.

MATERIALS AND METHODS: From 1994 to 2000, 17 patients who had small recurrent breast carcinomas after initially undergoing breast-conserving therapy (BCT), which included postoperative radiation therapy, were treated with local tumor excision and PDR brachytherapy. Recurrences occurred at a median time of 50 months (range, 11–208 months) after primary treatment. Eight patients underwent a combination of PDR brachytherapy (total dose range, 12.5–28.0 Gy) and external-beam radiation therapy (EBT) (total dose range, 12–30 Gy). Nine patients underwent radiation therapy with 40.2–50.0-Gy PDR brachytherapy only. The prescribed radiation dose was 0.5–1.0 Gy per pulse. Patients were examined for local tumor control and treatment-related side effects.

RESULTS: Twelve of 17 patients had no local tumor at a median follow-up time of 59 months (range, 20–84 months); two of these patients showed signs of having distant disease. One patient died after a cerebral stroke without evidence of tumor. Four women treated with combined EBT and brachytherapy had secondary local tumor recurrences 4, 8, 8, and 11 months after therapy and had to undergo mastectomy. Despite having undergone radiation therapy previously, patients had side effects limited to moderate (grade 1–2) fibrosis.

CONCLUSION: Local tumor excision combined with PDR brachytherapy for small local-regional tumor recurrences after primary BCT is feasible and well tolerated and might obviate mastectomy. Preliminary experiences are encouraging. Further studies are required for appropriate patient selection.

© RSNA, 2002

Index terms: Breast neoplasms, 00.32 • Breast neoplasms, therapeutic radiology, 00.1299 • Therapeutic radiology, interstitial and intracavitary, 00.1299


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Wide local excision, or lumpectomy, combined with axillary dissection and radiation therapy for clinical stage I and II breast cancers is commonly regarded as the treatment of choice as an alternative to mastectomy (1). Because breast cancer recurrence is an inherent risk with breast-preserving therapy, which is being used with increasing frequency (2), the number of local recurrences is continually increasing as follow-up times increase. The reported incidence of in-breast tumor recurrence is 1%–2% per year in most centers (3–10). Patients with recurrent tumors usually are treated with mastectomy; however, patients are increasingly requesting additional breast-conserving therapy. Thus, an important question is whether, in cases of secondary breast-conserving therapy, repeat irradiation (of any kind) can be performed, and, if it can, whether the results can be improved. To our knowledge, there are few published reports of experiences with alternative therapies—alternative radiation regimens in particular—to treat in-breast tumor recurrence after lumpectomy and conventional radiation therapy (5,11–18).

The purpose of this study was to perform and assess the effectiveness of treating small local-regional tumor recurrences with excision and pulse dose rate (PDR) brachytherapy as the main component of additional radiation therapy. Herein, we report our experiences.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Between 1994 and 2000, 17 patients who had small, locally recurrent breast carcinomas after undergoing primary breast-conserving therapy, which included radiation therapy, were treated with local tumor resection and repeat irradiation that consisted primarily of PDR brachytherapy in the Department of Radiotherapy of Vienna University. At the time of diagnosis of breast tumor recurrence, the ages of the women ranged from 34 to 74 years (median age, 49.5 years). Our study was approved by the institutional review board, and signed informed consent was obtained from all patients.

Treatment of Initial Breast Cancer
Surgical treatment.—The initially performed breast-conserving surgery consisted of lumpectomy or quadrantectomy. Axillary surgery generally included dissection of the lymph nodes lateral to the medial border of the smaller pectoral muscle. The tumors in all patients were staged according to the guidelines of the Union Internationale Contre le Cancer published in TNM Classification of Malignant Tumours (19). When we classified the primary tumors according to size and histologic features, we identified ductal pT1 cancer in all cases and no pathologic evidence of axillary lymph node metastases (ie, N0). Histologic examination revealed moderately differentiated carcinoma in nine patients, poorly differentiated tumors in seven patients, and highly differentiated carcinoma in one patient. The primary locations of the tumors were as follows: In 11 (65%) of the 17 patients, the tumors were in the upper outer quadrant, whereas in six (35%) patients, the tumors were in other quadrants.

Postoperative radiation therapy.—All patients underwent external-beam radiation therapy (EBT) postoperatively. In 15 cases, the entire breast was irradiated with two tangential beams via a medial field and a lateral field by using a megavolt technique (ie, cobalt 60 or a linear accelerator) and with a conventionally fractionated radiation dose of 1.8 or 2.0 Gy per fraction, up to a total dose of 50.0 Gy, as specified at the reference point designated by the International Commission on Radiation Units and Measurements (ICRU) (20). Eight of the 17 patients received an additional tumor bed boost dose of 10 Gy. In two of these patients, this boost therapy was performed with interstitial high-dose-rate brachytherapy with doses of up to 7 and 8 Gy. The nuclide iridium 192 was used for brachytherapy. In one woman, 60 Gy was delivered to the whole breast, and one woman was treated with 42-Gy orthovoltage therapy.

Adjuvant systemic therapy.—Nine women, most of whom were premenopausal and had grade 3 (ie, poorly differentiated carcinoma according to Bloom and Richardson histologic tumor grading classification system) tumors, underwent chemotherapy. Three women received hormone therapy with tamoxifen as an adjuvant therapy to the initial treatment.

Treatment of Recurrent Breast Cancer
Recurrences were diagnosed at a median follow-up time of 50 months (range, 11–208 months) after the initial treatment. In 12 of the 17 patients, the tumors recurred in the same regions of the breast, and in five, the tumors recurred in different quadrants. In most cases—that is, in 14 of 17 patients—the recurrent tumors were classified as T1, and none had a classification higher than small T2. Maximum tumor dimension ranged from 0.5 to 2.5 cm (mean dimension, 1.5 cm) (Fig 1). All patients underwent a second excision of the tumor, and the margins of resection were free of tumor in all patients. Histologically, all tumors were moderately to poorly differentiated, not otherwise specified invasive ductal carcinomas.



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  		Figure 1. Mediolateral mammogram shows a recurrent rpT1a breast tumor in a 60-year-old woman 42 months after primary treatment of pT1b, pN0, G2 breast cancer.

 
Ten of the 17 women underwent adjuvant systemic therapy. Five women were treated with chemotherapy; three women, hormone therapy; and two women, chemotherapy followed by hormone therapy.

After a second attempt at breast-conserving surgery, radiation therapy was administered with the intent to cure the patient of cancer. In a pilot treatment phase, eight patients were treated with EBT combined with PDR brachytherapy. The first of these patients was treated with 30-Gy EBT to the whole breast and an additional 12.5-Gy PDR boost dose to the tumor bed. In the next seven patients, the EBT dose remained the same or was reduced and the brachytherapy dose was increased (Table 1). EBT was administered in standard fractions of 2 Gy with tangential beams of megavoltage photons via a medial field and a lateral field. The radiation dose was specified at the ICRU reference point (20). Because we did not observe any major side effects with increasing brachytherapy doses, we decided to begin using PDR brachytherapy as the sole method for treatment of recurrent breast cancer.


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  		TABLE 1. Characteristics and Outcomes of 17 Patients Treated for In-Breast Tumor Recurrence

 
The remaining nine patients, who were treated after September 1995, underwent only PDR brachytherapy with a minimum dose of 40.2 Gy (Table 1).

PDR Brachytherapy Technique
Tube implantation was performed with general anesthesia having been induced in the patients and with the classic plastic tube technique. Three to 15 (average of eight) plastic tubes usually were implanted in one to three planes. In nine patients, PDR brachytherapy was performed 4–6 weeks after surgical treatment, and in eight patients the PDR tubes were implanted intraoperatively and radiation therapy was started 48–96 hours later.

After brachytherapy tube implantation, two orthogonal radiographs (anteroposterior and lateral) were obtained for treatment planning. For positional reconstruction of the tubes and dose calculation, a three-dimensional treatment-planning system (PLATO; Nucletron, Veenendaal, the Netherlands) was used. In addition, computed tomography (CT) or magnetic resonance imaging was performed in those patients who did not receive tube implants intraoperatively (Fig 2).



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  		Figure 2. Transverse CT scan obtained for treatment planning in the patient described in Figure 1.

 
Clinical target volume was defined as the former tumor bed with a safety margin of about 2 cm. The prescribed isodose entirely encompassed the clinical target volume (Fig 3). According to terminology published in ICRU report number 58 (21), the prescribed dose was considered to represent the minimum target dose.



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  		Figure 3. Drawing illustrates cumulative radiation doses for EBT and brachytherapy performed in the patient described in Figures 1 and 2. Initially, 50-Gy EBT was performed with two tangential beams via a medial field and a lateral field specified at the ICRU reference point. R = rib, ST = sternum.

 
For the pilot treatment phase, in which patients underwent EBT combined with PDR brachytherapy, the prescribed radiation dose was 0.5–1.0 Gy per pulse (mean dose, 0.84 Gy). The total dose for PDR brachytherapy ranged from 12.5 to 28.0 Gy (mean dose, 22.4 Gy). The average number of pulses was 27 (range, 16–31 pulses). The mean uniformity index (according to ICRU report number 58 (21) was 0.77 (range, 0.53–1.06). The volume irradiated with the prescribed dose was 25.3–160.0 cm3 (mean, 60.5 cm3).

For the second group—that is, the patients treated with PDR brachytherapy only—the prescribed radiation dose was 0.6–1.0 Gy per pulse (mean dose, 0.78 Gy). The total radiation dose ranged from 40.2 to 50.0 Gy (mean dose, 46.5 Gy). The average number of pulses was 58 (range, 50–70 pulses). The mean uniformity index (according to ICRU report number 58) (21) was 0.80 (range, 0.57–0.85). The volume irradiated with the prescribed dose was 25–152 cm3 (mean, 58.3 cm3).

Irradiation was performed by using a PDR remote afterloading system (micro Selectron; Nucletron) that operates on the basis of a pulsed brachytherapy principle. The system has a single stepping source, the nuclide iridium 192. With the stepping source technique, variable dwell positions and dwell times can be selected to optimize the dose distributions for individual patients.

The interval between the pulses was 1 hour. In the pilot treatment phase, PDR brachytherapy treatments were given 24 hours a day (maximum, 31 hours). For patients who underwent PDR brachytherapy only, the entire treatment was administered in 4 days, with 24-hour treatment for at least 1 day, eight to 10 pulses on the other days, and a break during the evening. The mean irradiation time per pulse was 474 seconds (range, 145–1,543 seconds), and the mean source activity was 0.67 Ci (24.79 GBq) (range, 0.29–1.10 Ci [10.73–40.70 GBq]).

Patient Examination
One experienced radiation therapist (A.R.) examined the patients to assess local tumor control and treatment-related side effects. For assessment of local tumor control, a physical examination, mammography, and breast ultrasonography were performed in all patients every 6 months. Treatment-related side effects were evaluated according to common toxicity criteria (22) for acute effects and according to the LENT SOMA (late effects on normal tissue and subjective, objective management) system for scoring late effects (23,24). Cosmetic outcome was judged by the physicians and patients independently by using a five-score system (Table 2).


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  		TABLE 2. System for Scoring Cosmetic Outcome

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
At a median follow-up time of 59 months (range, 20–84 months), 12 of the 17 women were alive and free of local tumor; two of these 12 patients showed evidence of distant disease with bone metastases. One patient died owing to a cerebral stroke 50 months after treatment, without evidence of local or distant tumor recurrence.

Four (24%) patients had a second local tumor recurrence 4, 8, 8, and 11 months after therapy and consequently underwent mastectomy. All second recurrences occurred close to the area of the first recurrence, and all four of these patients had been treated during the pilot phase with combined EBT and PDR brachytherapy. Two of these patients developed distant metastases and died. One patient had two other local recurrences after undergoing mastectomy and plastic surgery but showed no evidence of distant metastases afterward. The last of the four patients was free of tumor. At the time of this writing, none of the nine patients treated with only PDR brachytherapy had had a second local tumor recurrence.

Despite having undergone radiation therapy previously, all patients had side effects that were limited to local moderate (ie, grade 1–2) fibrosis. Three patients had changes in skin pigmentation, and two developed minimal telangiectasia (<1 cm) at the end points of the needles. Severe side effects were not observed.

There were no problems with wound healing in any of the patients who were treated with brachytherapy perioperatively. A 74-year old patient in whom the brachytherapy tubes were placed intraoperatively had a minor cerebral stroke during surgery. However, radiation therapy was performed perioperatively after a delay of 48 hours.

Cosmetic outcome was judged according to a five-score system (Table 2). Cosmetic results were considered to be excellent in two patients, one of whom underwent oncoplastic resection in which the defect was filled with a rotated flap of breast tissue and adjusting reduction of the other breast at the same time. Three patients had good results; eight patients, moderate results; and four patients, acceptable results. No patient had unacceptable results (Fig 4).



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  		Figure 4. Good cosmetic outcome in the patient described in Figures 1-3 6 months after radiation therapy.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Breast-conserving therapy, including radiation therapy, is now considered the treatment of choice for breast cancer, at least during the early stages of the disease. The number of patients treated with breast-conserving therapy has therefore increased substantially during the past 15 years (2) and will continue to do so. Moreover, more and more patients with advanced-stage tumors can now be treated with breast-conserving therapy owing to an increasing number of neoadjuvant chemotherapy protocols (25). As an inherent consequence of breast-conserving therapy, in-breast tumor recurrence can be observed many years after the primary treatment (5,9,26,27). In our series, the latest relapse occurred after 18 years. Thus, as follow-up times increase, more local tumor relapses will be encountered, and the issue of the most appropriate treatment will gain increasing importance because many patients request further breast-conserving therapy. In contrast to chest wall tumor recurrences, most cases of in-breast tumor recurrence, particularly the late recurrences, have a favorable prognosis (5,11,26). Although few studies on breast-conserving therapy for treatment of recurrent tumors have been published, the available data indicate that repeat breast-conserving therapy is possible. Kurtz et al (5) and Abner et al (28) reported local tumor control rates of 77% and 69%, respectively, at 5 years after repeat limited surgery. These results are in accord with pathology studies of mastectomy specimens, in which tumor foci outside the tumor bed were found in 22%–31% (29,30) of cases of recurrent tumors. Multicentric recurrence seems to be rare, especially when lobular carcinomas are excluded (29,30). Other factors that are reportedly associated with multifocality are extensive intraductal carcinoma and lymphatic invasion (29–32), which may be considered contraindications to repeat breast-conserving therapy.

Residual tumor is associated with the greatest risk of secondary (or first) local tumor relapse after mastectomy or breast preservation. Thus, the identification of margins that are negative for tumor seems to be essential at repeat breast-conserving therapy (29,33–36). If negative resection margins cannot be found, mastectomy should be performed. Thus, a major limiting factor in performing breast-conserving therapy is the size of the remaining breast, particularly the tumor–breast volume ratio.

In studies of salvage mastectomy after breast tumor recurrence, local tumor control rates of 88%–96% have been reported (5,11,29). Therefore, it may be questionable as to whether local control can be improved with repeat radiation therapy. Radiation therapy after initial breast-preserving surgery has been proven to be highly effective (3,6,37) and should therefore facilitate a decrease in the local tumor recurrence rate in cases of repeat breast conservation as well. Even if this is the case, however, the radiation-related side effects associated with a second course of radiation therapy are still a concern.

To our knowledge, there are only a few published reports on the use of radiation therapy for in-breast tumor recurrence. In a study by Kurtz et al (5), 11 of 50 patients received additional radiation after wide local excision for in-breast tumor recurrence outside the primary tumor site. Seven of these 11 patients received 20–30 Gy of radiation through electron beams, and four received 50 Gy through interstitial implants. However, four of the 11 treated patients had a secondary breast tumor recurrence. These results were similar to those in the patients who had been treated by means of wide excision only. The patients in that study could not be identified according to the chosen radiation regimen, however. Because there is a clear relationship between local tumor control rate and applied total radiation dose (4), it seems probable that the patients in the Kurtz et al study who received relatively small radiation doses would have had tumor recurrence.

This hypothesis is supported by the data of Maulard et al (12), who treated 38 patients with local tumor recurrence by using brachytherapy. In that study, a subgroup of 15 patients was treated with limited tumor resection and 30-Gy perioperative brachytherapy. The other 23 patients underwent exclusive split-course brachytherapy with 60–70 Gy. Although one would expect the patients who were treated after surgery for only microscopic disease to have better local tumor control compared with the patients treated for gross disease, this was not the case. The patients treated for gross disease had better local control, 83%, as compared with a local control rate of 74% in the patients treated for microscopic disease. The only explanation for these results is the higher brachytherapy dose delivered to the patients who were treated for gross disease. Maulard et al reported an overall local tumor control rate of 79% for a mean follow-up period of 40 months; this rate presumably would have been even better with a higher brachytherapy dose after tumor resection. Mullen et al (13), who delivered a 50-Gy dose of radiation at EBT, reported a local recurrence rate of only 20%.

In our study as well, all local recurrences occurred in the patients who underwent therapy during the pilot treatment phase with 12–30-Gy EBT and a brachytherapy boost that was applied 3–4 weeks afterward to result in a total nominal dose of approximately 42 Gy. However, these patients had a longer median follow-up period (74 months) than did the patients who were treated with PDR brachytherapy only (58 months) and therefore were at a higher risk of having a local recurrence. On the other hand, it is remarkable that all of the local recurrences occurred within 1 year after treatment, so they might have been due to insufficient radiation doses.

In the nine patients who underwent only brachytherapy with a mean nominal radiation dose of 46.5 Gy, no local recurrences were observed. In addition, it should be noted that these 46.5-Gy doses were delivered within 4 days; this means that this treatment is more biologically efficient than conventional fractionated EBT. Thus, our results provide strong evidence that there is a radiation dose–related effect on local tumor control.

Despite the very high cumulative radiation doses of approximately 100 Gy, no immediate associated complications were observed in either our study or the studies of other investigators. With the exception of one case of late necrosis in one patient after she had undergone 70-Gy salvage brachytherapy for a large (7-cm) tumor in the study by Maulard et al (12), no severe side effects were observed in either our study or any other series in the literature. This very low rate of complications may be due to relatively small irradiated volumes.

Although radiation dose is inversely related to cosmetic outcome (38) and the patients in our study underwent two surgical procedures, nearly one-third (five of 17 patients) of the cosmetic outcomes were excellent or good, and there were no unacceptable results. These outcomes probably resulted from the careful selection of patients with good tumor volume–breast volume ratios and the relatively small irradiated volumes. However, one should be aware that these cosmetic results can deteriorate during longer follow-up periods.

To summarize our results and those of other investigators, breast tumor recurrence frequently is restricted to the breast (without distant metastasis) and usually is associated with a favorable prognosis. Repeat breast-conserving therapy may be an alternative to mastectomy. Local tumor excision combined with PDR brachytherapy for treatment of small local-regional tumor recurrences after primary breast-conserving therapy was feasible and well tolerated and could obviate mastectomy. The local recurrence rate can be reduced to a minimum if patients are appropriately selected, the contraindications described herein are observed, and a sufficient radiation dose is administered. Further studies are required to identify more factors that enable appropriate patient selection for a second attempt at breast conservation.


   FOOTNOTES
 
Abbreviations: EBT = external-beam radiation therapy, ICRU = International Commission on Radiation Units and Measurements, PDR = pulse dose rate

Author contributions: Guarantor of integrity of entire study, A.R.; study concepts, A.R., C.F., R.P.; study design, A.R., C.F., W.S.; literature research, U.M., E.B.; clinical studies, A.R., C.F.; data acquisition, E.B., U.M.; data analysis/interpretation, A.R., C.F.; statistical analysis, C.F.; manuscript preparation, A.R., C.F.; manuscript definition of intellectual content, A.R., R.P.; manuscript editing, L.H.Z.; manuscript revision/review, A.R., C.F.; manuscript final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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