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10.1245/ASO.2006.08.026
Annals of Surgical Oncology 13:1099-1104 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Sentinel Lymph Node Biopsy for Local Recurrence of Breast Cancer After Breast-Conserving Therapy

Bret Taback, MD1, Phong Nguyen, MD2, Nora Hansen, MD3, G. Keith Edwards, MD2, Kim Conway, BS4 and Armando E. Giuliano, MD5

1 Division of Surgical Oncology, Columbia University Medical Center, 177 Fort Washington Avenue, New York, New York 10032
2 Department of Nuclear Medicine, John Wayne Cancer Institute, Saint John’s Health Center, 2200 Santa Monica Boulevard, Santa Monica, California 90404
3 Lynn Sage Comprehensive Breast Center, Northwestern University Medical Center, 251 E. Huron Street, Chicago, Illinois 60611
4 Department of Medical Oncology, Fred Hutchinson Cancer Center, 1100 Fairview Avenue, Seattle, Washington 98109
5 Joyce Eisenberg-Keefer Breast Center, John Wayne Cancer Institute, Saint John’s Health Center, 2200 Santa Monica Boulevard, Santa Monica, California 90404

Correspondence: Address correspondence and reprint requests to: Armando E. Giuliano, MD; E-mail: giulianoa{at}jwci.org.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Lymphatic mapping (LM) with sentinel lymph node (SLN) biopsy has revolutionized the surgical staging of primary breast cancer, but its utility and feasibility have not been established in patients with ipsilateral breast tumor recurrence (IBTR) after breast-conserving surgery (BCS) and radiation.

Methods: We reviewed our breast cancer database to identify all patients who underwent preoperative lymphoscintigraphy for IBTR and whose primary tumor had been managed by BCS, SLN biopsy and/or axillary node dissection, and adjuvant breast irradiation.

Results: Preoperative lymphoscintigraphy identified migration to the regional nodal drainage basins in 11 (73%) of 15 patients, as follows: 5 ipsilateral axillary, 1 supraclavicular, 2 internal mammary, 2 interpectoral, and 3 contralateral axillary. Two patients demonstrated drainage to two nodal basins. In four patients, no drainage was observed. Intraoperative LM with radioisotope plus blue dye identified at least 1 SLN in 11 of 14 patients, and histopathologic evaluation revealed metastasis in 3 patients (2 contralateral axillary and 1 ipsilateral axillary). During preoperative lymphoscintigraphy, the radiocolloid migration time tended to be longer and the drainage pathways more variable than those associated with primary tumors.

Conclusions: LM/SLN biopsy can be successfully performed in patients with IBTR after prior BCS, axillary surgical staging, and adjuvant radiation. This approach illustrates variations in the lymphatic drainage of recurrent breast tumors and may permit the identification of regional metastasis not noted with conventional imaging techniques.

Key Words: Lymphatic mapping • Sentinel lymph node • Breast cancer • Recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Breast cancer is the most frequent malignancy diagnosed in the United States, affecting >200,000 women each year.1 An increasing number of these patients are diagnosed with early-stage breast cancer, and many choose breast-conserving surgery (BCS) followed by radiotherapy, with or without adjuvant systemic therapy.2–4 Unfortunately, within 10 years after conservative treatment for either a primary invasive or noninvasive breast cancer, approximately 10% to 15% of patients will develop an ipsilateral breast tumor recurrence (IBTR).5,6

There are few guidelines for the management of locally recurrent breast cancer. Salvage mastectomy best reduces further local recurrence, but additional lumpectomy is feasible in carefully selected patients.7,8 Irrespective of the management of the breast, it has been suggested that axillary lymph node (ALN) dissection at the time of IBTR should be performed in patients with clinical findings consistent with regional recurrence or a previously undissected axilla.9 However, even if regional nodal surgery is undertaken, prior surgery and radiation may have changed the lymphatic drainage pathways and could lead to missed regional metastasis.

We have successfully demonstrated the technique of lymphatic mapping (LM) and sentinel lymph node (SLN) biopsy for primary breast cancer.10,11 The technique provides a minimally invasive method to stage the axilla and has results comparable to or better than those of conventional ALN dissection.12–15 This study of LM and SLN biopsy for IBTR was conducted to determine the feasibility of the technique after BCS and radiotherapy for primary breast cancer, to examine alterations in lymphatic drainage pathways, and to assess its ability to identify subclinical nodal metastasis from a recurrent tumor.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
We reviewed the John Wayne Cancer Institute Breast Cancer database for patients who received a diagnosis of an IBTR after primary breast cancer treatment with BCS and radiotherapy between January 1989 and June 2004 (n = 88). Patients with a history of bilateral breast cancer or a new ipsilateral breast tumor not in the same quadrant as the original primary tumor were excluded. Pathology was reviewed in all cases to confirm local recurrence. In total, 15 patients were identified from our database who had an IBTR (14 invasive and 1 ductal carcinoma-in-situ [DCIS]) after BCS, SLN biopsy and/or ALN dissection, and adjuvant breast irradiation and who underwent preoperative lymphoscintigraphy for the recurrence. No patient had clinical evidence of metastasis. Thirteen patients had preoperative studies with computed tomographic and/or positron emission tomography scans, none of which showed metastasis. The patient with recurrent DCIS did not undergo imaging.

LM and SLN Biopsy Technique
LM was performed with the combined technique of radioisotope and blue dye, as previously described.10,16 Briefly, lymphoscintigrams were performed within 24 hours before surgery by using peritumoral injection of .5 mCi of filtered 99mTc sulfur colloid (CIS-US, Bedford, MA) in a volume of 7 mL. An intraoperative gamma probe was used to assess all potential lymph node drainage basins, including axillary, supraclavicular and infraclavicular, and internal mammary. Isosulfan blue dye (5 mL; Lymphazurin 1%; Tyco Healthcare, Norwalk, CT) was injected peritumorally at the start of the operation. All blue-stained and/or radioactive lymph nodes (i.e., those with counts >2 x background) were labeled as SLNs and submitted for histopathologic review.

Histopathologic Evaluation of SLNs
Histopathologic examination of all SLNs involved two step-section levels of the paraffin block separated by 40 µm and stained at each level with hematoxylin and eosin (H&E) and with an immunohistochemical monoclonal anticytokeratin antibody cocktail (Zymed Laboratories, San Francisco, CA) if metastasis were not detected on H&E.17 Non-SLNs were evaluated with a single H&E-stained section.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Fifteen patients were identified from our database who underwent lymphoscintigraphy for isolated IBTR (Table 1Go). Initially, all patients had a segmental mastectomy with histologically clear margins for treatment of the primary tumor and underwent adjuvant radiotherapy. Twelve patients had invasive carcinoma and three had DCIS as the initial primary tumor. After BCS and radiotherapy for the primary breast cancer, three patients received adjuvant chemotherapy, and eight patients received adjuvant hormonal therapy. The tumor status of the axilla at the time of initial breast cancer presentation was determined by SLN biopsy (six patients), standard ALN dissection (four patients), or SLN biopsy followed by completion ALN dissection (five patients).


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  		TABLE 1. Patient characteristics
 
The median time to IBTR was 71 months (range, 13–150 months). The mean size of the IBTR was 1.8 cm (range, .6–4.5 cm). Preoperative lymphoscintigraphy (Fig. 1Go) identified migration to the regional nodal drainage basins in 11 (73%) of 15 patients as follows: ipsilateral axillary (5 cases), supraclavicular (1 case), internal mammary (2 cases), interpectoral (2 cases), and contralateral axillary (3 cases). Two patients demonstrated drainage to two nodal basins. In four patients, no drainage was observed. The mean time for lymphoscintigraphic SLN identification was 69 minutes (range, 13–240 minutes).


Figure 1
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  		FIG. 1. Representative lymphoscintigrams. (A) Patient 1, demonstrating drainage to ipsilateral supraclavicular and axillary sentinel lymph nodes. (B) Patient 11, demonstrating drainage to contralateral axillary sentinel lymph nodes.

 
Of the 11 patients with lymphoscintigraphic drainage patterns, 10 underwent intraoperative LM/ SLN biopsy by using a combination of radioisotope and blue dye; SLNs were identified in 9 (90%) patients. In two cases (patients 7 and 12), SLNs were identified during surgery but were not noted on the preoperative lymphoscintigram. Thus, SLN biopsy was successful in 11 (79%) of 14 patients. The mean number of SLNs harvested in the 11 patients was 1.7 (range, 1–6). Metastases were identified in the SLNs from three patients (27%) during evaluation with H&E and immunohistochemistry: two patients in the contralateral axilla and one patient in the ipsilateral axilla. In nine patients, both SLNs and non-SLNs were obtained. In all cases, the histopathologic status of the SLN predicted that of the drainage basin.

All patients underwent salvage mastectomy for IBTR. Of the 11 patients for whom information regarding adjuvant therapy was available, 10 received postmastectomy chemotherapy, hormonal therapy, or both. The sole patient with DCIS recurrence received no systemic treatment. At a median follow-up of 41 months (range, 6–102 months) after IBTR, two patients died from metastatic breast cancer: one patient with a histopathologically positive SLN at 46 months and one patient with a histopathologically negative SLN at 30 months after IBTR. One patient died from complications related to lymphoma but had no evidence of breast cancer metastasis. The remaining 12 (80%) patients remain clinically free of recurrent breast cancer.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Unlike mastectomy, breast-conserving therapy (BCT) is followed by an increased risk of local relapse throughout the life of the patient.18–27 With more patients choosing BCT and living longer, a steadily larger proportion of breast cancer patients will eventually develop local recurrence.

Several studies have shown that once an IBTR is detected, patients have a 3- to 5-fold increased risk for subsequent development of distant metastasis.24,25,28,29 However, for many, the prognosis remains optimistic, with average 5-year survival rates approximating 60% to 70% after an IBTR.9,25,28,30–32 A variety of clinical and pathologic factors have been assessed for their prognostic utility in predicting patient outcomes after local relapse.7,23,30,32–34 To date, the most consistently recognized variables include the interval to relapse and the extent of recurrence.31,35–38 For most studies, the extent of regional disease at the time of IBTR may not be clearly and consistently evaluated, and, therefore, its true effect on survival may not be known. This may be attributed to the fact that lymph node dissection is often performed initially and not for recurrent disease without clinically apparent regional recurrence.

The relationship between IBTR and the risk for distant metastasis is poorly understood. A number of early studies did not find an adverse effect of local recurrence on subsequent patient survival,39–41 whereas more recently, investigators have demonstrated a higher risk of death in patients after IBTR.25,29,37,38,42,43 Veronesi et al.25 and Fisher et al.24 showed that the development of IBTR and the development of distant metastasis are two independent events, thus suggesting that IBTR is merely an indicator for an increased risk of subsequent distant relapse. In contrast, Fortin et al.29 demonstrated that because the incidence of distant metastasis was greater and because it occurred later after a local recurrence as compared with that in patients without local relapse, IBTR may serve a source for metastasis. The issue of whether IBTR is a marker for or directly contributes to the development of distant metastasis remains controversial.

The extent of local recurrence has been correlated with a worse patient prognosis.19,23,36,44–47 However, surgical assessment of regional disease at the time of IBTR is often variable, depending on clinical findings at the time of presentation and a history of axillary dissection.8,9 In addition, current imaging techniques are limited in their ability to detect small lymph node metastasis that may be present at the time of local recurrence.

In this article, we report our application of the SLN biopsy technique in patients who have developed a clinically isolated IBTR after BCT. We have previously shown this technique to accurately stage the tumor-draining lymph node basin and improve the detection of subclinical lymph node metastasis in patients with a primary breast cancer diagnosis.10,14 In this study, preoperative lymphoscintigraphy demonstrated drainage in 11 (73%) of 15 patients. Among 14 patients in whom intraoperative LM was attempted by using the combined technique of radioisotope and vital blue dye, 11 (79%) patients had SLN(s) identified.

There are several noteworthy findings in this study. First, LM with SLN biopsy can be performed successfully in patients diagnosed with an IBTR after BCT and prior axillary surgery. Our success rate is comparable to initial reports with this technique in patients with primary breast cancer.10 Recently this approach has been performed for patients with recurrent melanoma.48

Second, preoperative lymphoscintigrams demonstrated seven cases of aberrant drainage, i.e., to lymph node basins other than the ipsilateral axilla. These findings are unique in that historically these lymph node basins rarely demonstrate metastasis and would not be explored. This result occurred more often than what has been reported for patients with primary breast cancer.12 Additionally, we found that the median time to lymphoscintigraphic identification of the SLN basin was 69 minutes, which is markedly longer than that for our patients with primary breast cancer.49 The combination of prior axillary surgery and breast irradiation most likely alters the anatomical pathway and kinetics of lymphatic drainage from a recurrent tumor. Patients with a prior ALN dissection had a longer mean time for lymphoscintigraphic identification of the SLN than those who had a prior SLN biopsy only (102 vs. 61 minutes). In this study, four patients had preoperative lymphoscintigrams that demonstrated no drainage, and three of these patients did have prior axillary dissections. Of particular interest was that in two of the three patients with contralateral axillary drainage for their IBTR, a prior ALN dissection was performed for their initial breast cancer. However, there are too few patients in this preliminary series to reach definitive conclusions.

The third most significant finding of this study was that we detected metastasis in SLNs from three patients that were not appreciated before surgery and that in two cases would not have been identified at the time of salvage mastectomy because they were noted in SLNs from the contralateral axilla. All SLNs obtained during surgery for IBTR were evaluated by using the same histopathologic processing technique as performed for patients with SLNs acquired during surgery for primary breast cancer.17,50 This demonstrates the increased sensitivity of the SLN biopsy technique for identifying occult regional disease.

Our findings are similar to others previously reporting this technique in patients with locally recurrent breast cancer.51,52 Port et al.51 successfully identified axillary SLNs in 75% of patients undergoing a reoperative SLN biopsy, of which 13% were positive for metastasis; however, the authors did not comment on the potential for aberrant drainage pathways. The prognostic implications of a positive SLN will require longer-term follow-up in a larger cohort of patients. Nonetheless, these preliminary findings raise speculative interest that the concomitant presence of subclinical SLN metastasis at the time of IBTR could identify patients at increased risk for systemic relapse. Additionally, these findings raise questions as to whether contralateral SLN metastasis detected during IBTR represents stage IV disease. SLN biopsy for patients with IBTR may prove useful for stratifying higher-risk patients for more aggressive systemic treatments. Moreover, and most importantly, imaging of the contralateral axilla should be considered during preoperative lymphoscintigraphy in patients with an IBTR who do not demonstrate ipsilateral axillary drainage. This approach may identify aberrant contralateral axillary SLN drainage, which, as demonstrated in this study, can harbor metastasis.

Our results demonstrate the feasibility of SLN biopsy in patients with an IBTR after BCS and radiotherapy. The approach further confirms the versatility of the SLN technique that has been successfully used in male breast cancer patients,53 after administration of neoadjuvant chemotherapy,54 and for a variety of other solid malignancies.55 Although the value of SLN biopsy in the current circumstance remains undefined, the intention is that a more accurate evaluation of regional disease at the time of local recurrence may provide additional biological information for answering the long-standing question as to whether a local relapse is a marker for or a direct contributor to distant metastasis.


   ACKNOWLEDGMENTS
 
Supported by the Leslie and Susan Gonda (Goldschmied) Foundation, the Ben B. and Joyce E. Eisenberg Foundation (Los Angeles), and the Fashion Footwear Association of New York.

Received for publication August 18, 2005. Accepted for publication January 6, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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