Annals of Surgical Oncology Cite Track
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10.1245/ASO.2005.08.020
Annals of Surgical Oncology 12:705-711 (2005)
© 2005 Society of Surgical Oncology
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Original Article

The Effect of Sentinel Node Tumor Burden on Non–Sentinel Node Status and Recurrence Rates in Breast Cancer

Yang-Guo Fan, MD1, Yah-Yuen Tan, FRCS1, Chen-Teng Wu, MD1, Patrick Treseler, MD2, Ying Lu, PhD3, Chung-Wei Chan, BS1, Shelley Hwang, MD1, Cheryl Ewing, MD1, Laura Esserman, MD1, Eugene Morita, MD4 and Stanley P. L. Leong, MD1

1 Department of Surgery, University of California San Francisco Medical Center at Mount Zion, and University of California San Francisco Comprehensive Cancer Center, 1600 Divisadero Street, San Francisco, California 94143-1674
2 Department of Pathology, Box 0102, University of California San Francisco Medical Center, Room M-551, San Francisco, California 94143-0102
3 Departments of Radiology and Epidemiology and Biostatistics, and University of California San Francisco Comprehensive Cancer Center, University of California, San Francisco, CA 94143-0946
4 Department of Nuclear Medicine, University of California San Francisco Medical Center at Mount Zion, 1600 Divisadero Street, San Francisco, California 94143-1667

Correspondence: Address correspondence and reprint requests to: Stanley P. L. Leong, MD; E-mail: leongs{at}surgery.ucsf.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Routine axillary lymph node dissection (ALND) after selective sentinel lymphadenectomy (SSL) in the treatment of breast cancer remains controversial. We sought to determine the need for routine ALND by exploring the relationship between sentinel lymph node (SLN) and non-SLN (NSLN) status. We also report our experience with disease relapse in the era of SSL and attempt to correlate this with SLN tumor burden.

Methods: This was a retrospective study of 390 patients with invasive breast cancer treated at a single institution who underwent successful SSL from November 1997 to November 2002.

Results: Of the 390 patients, 115 received both SSL and ALND. The percentage of additional positive NSLNs in the SLN-positive group (34.2%) was significantly higher than in the SLN-negative group (5.1%; P = .0004). The SLN macrometastasis group had a significantly higher rate of positive NSLNs (39.7%) compared with the SLN-negative group (5.1%; P = .0001). Sixteen patients developed recurrences during follow-up, including 6.1% of SLN-positive and 3.3% of SLN-negative patients. Among the SLN macrometastasis group, 8.7% had recurrence, compared with 2.2% of SLN micrometastases over a median follow-up period of 31.1 months. One regional failure developed out of 38 SLN-positive patients who did not undergo ALND.

Conclusions: ALND is recommended for patients with SLN macrometastasis because of a significantly higher incidence of positive NSLNs. Higher recurrence rates are also seen in these patients. However, the role of routine ALND in patients with a low SLN tumor burden remains to be further determined by prospective randomized trials.

Key Words: Sentinel lymph node • Non–sentinel node status • Tumor burden • Recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Axillary lymph node dissection (ALND) has been a standard procedure for breast cancer treatment for decades because it provides important prognostic information in breast cancer patients. However, in recent years, the therapeutic role of ALND in early-stage breast cancer has been challenged because of the low incidence of nodal involvement and the complications of ALND, such as lymphedema, limited range of arm motion, and numbness.1–3

Over the last decade, selective sentinel lymphadenectomy (SSL) has evolved as an alternative staging procedure to ALND when SSL is performed with high identification rates and low false-negative rates.4 At many breast cancer centers, patients with negative sentinel lymph nodes (SLNs) are no longer subjected to routine ALND. Micrometastasis is defined as a tumor burden of ≤ 2 mm in the node and can be frequently found by meticulous examination with serial sectioning of SLNs and immunohistochemical stains. Whether routine ALND should be performed in all SLN-positive patients, including those with micrometastasis, remains a clinical dilemma. The aim of our study was to determine, among breast cancer patients undergoing SSL, the effect of SLN tumor burden on the status of NSLNs and clinical outcome.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From November 1997 to November 2002, 509 female patients with histologically confirmed primary breast carcinoma were seen at the University of California–San Francisco Carol Franc Buck Breast Care Center and underwent SSL. Diagnosis of primary breast cancer was mostly made before surgery by fine-needle aspiration, core biopsy, or excision biopsy. Operations for the primary tumors included either breast-conserving surgery or mastectomy. SSL was performed after preoperative lymphoscintigraphy. Patients with neoadjuvant treatment, noninvasive cancers, recurrent breast cancers, and failed preoperative lymphoscintigraphy were excluded.

Preoperative lymphoscintigraphy was performed by using filtered 99mTc-labeled sulfur colloid (190–1500 µCi) either on the day of operation or in the late afternoon the day before. The sulfur colloid was injected peritumorally or around the biopsy cavity, intradermally above the cancer, or both. A dynamic set of images was obtained, and additional images were taken up to 3 hours after injection. The skin overlying the SLN with significant radioactivity was marked, and the patient was then prepared for operation.5

During the operation, a handheld gamma probe (Neoprobe 2000; Neoprobe Corporation, Dublin, OH) was used to locate the highest radioactivity for the SLN. In the early phase of the SSL experience, a group of patients underwent additional injection of blue dye (Lymphazurin; Hirsch Industries Inc., Richmond, VA) before surgical incision to assist in locating the SLN. An SLN was defined as a node that was blue, had a radioactivity count 10 times higher than the background count, or both. After the SLN was removed, the resection bed was checked for further radioactivity. Further dissection continued until the handheld probe no longer detected significant radioactivity. During the validation phase of SSL at our center from November 1997 to July 1999, 128 patients underwent routine ALND after SSL. After the validation phase of SSL, ALND was performed for all patients with a positive SLN, except for patients who declined further axillary dissection.

All resected breast and axillary nodal tissues were submitted to the pathology department. Pathologic staging of the tumor was performed according to the American Joint Committee on Cancer (6th edition) guidelines. According to standard institutional practice, each SLN was bisected with at least three levels at 40- to 100-µm intervals for hematoxylin and eosin (H&E) staining, with or without immunohistochemical staining for cytokeratin.6 SLNs positive on immunohistochemistry alone were not considered pathologic for the purpose of this study. The size of metastasis was determined by pathologists. Micrometastasis was defined as a tumor deposit in the lymph node not exceeding 2 mm as seen on H&E stain, according to the American Joint Committee on Cancer staging classification of breast cancer. Conversely, macrometastasis was defined as a tumor deposit >2 mm in largest dimension in the lymph node identified by H&E stain. Non-SLNs (NSLNs) were nodes not blue and with no significant radioactivity harvested during the completion ALND. Each NSLN was examined with one level with H&E stain only.

After surgery, individualized adjuvant treatment for each patient was determined at a multidisciplinary breast cancer tumor board discussion according to clinical evidence at that time. Adjuvant treatment included chemotherapy, radiotherapy, and hormonal treatment. Although we acknowledge that a standardized adjuvant treatment protocol is necessary for evaluation of disease recurrence, we were not able to achieve this because of the retrospective nature of this study.

Data from all patients were entered into a database. These included the age of the patient at treatment; the primary tumor size, histology, grade, and estrogen receptor and progesterone receptor status; HER-2/neu overexpression; presence of lymphovascular invasion; status of SLNs and NSLNs; and clinical information regarding recurrences. Data analysis was performed by using Fisher’s exact test to determine the relationship between the SLNs and NSLNs. Recurrence rates among our patient group are also described in detail.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Among the 509 patients who underwent SSL at our center, 390 patients fitted into our study criteria. The remaining patients with neoadjuvant treatment, noninvasive cancers, recurrent breast cancers, and failed preoperative lymphoscintigraphy were excluded from analysis. The median age of the group of 390 patients was 54.9 years (range, 24–89 years), and the mean tumor size was 15.2 mm (range, 1–82 mm). There were 114 patients with positive SLNs (29.2%) and 276 with negative SLNs. Of the SLN-positive cases, there were 45 micrometastases and 69 macrometastases. Of the 390 patients, 39 SLN-negative patients and 76 SLN-positive patients underwent ALND. Thirty-eight patients with one or more positive SLNs declined further ALND, including 11 patients who had SLN macrometastasis. Two of 40 patients with negative SLNs were found on ALND to have further disease in the axilla, giving rise to a false-negative rate of 5%. These cases occurred during our early experience with SSL and reflect the learning curve in this procedure. The characteristics of patients are listed in Table 1Go. The clinical outcomes of the 390 patients undergoing SSL are detailed in Figure. 1Go.


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  		TABLE 1. Characteristics of patients in the study
 

Figure 1
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  		FIG. 1. Flowchart of events in the study population of 390 patients. SSL, selective sentinel lymphadenectomy; SLN, sentinel lymph node; ALND, axillary lymph node dissection; Recur, recurrences.

 
The relationship between SLN and NSLN status was determined by using Fisher’s exact test (Table 2Go). SLN positivity was significantly associated with additional positive nodes on ALND (P = .0004). Of the SLN-positive patients, 34.2% were found to have further disease in the axilla on ALND. Only 5% of SLN-negative patients had positive nodes on ALND, corresponding to the false-negative rate of SSL at our center.


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  		TABLE 2. Association between SLN status and NSLN positivity
 
We then analyzed our results according to the SLN tumor burden. Among the SLN micrometastasis group, 16.7% of patients had further positive NSLNs, compared with 5.1% of patients who were SLN negative. Despite the trend, this did not achieve statistical significance in our study, probably because of the relatively small number of patients. However, when comparing between the SLN-negative and SLN macrometastasis groups, there was a significant difference in rates of NSLN positivity (5.1% vs. 39.7%; P = .0001). Among the SLN-positive patients, tumor burden in the SLN affected NSLN status, although this did not achieve statistical significance. Three (16.7%) of 18 SLN micrometastases were associated with NSLN positivity, compared with 23 (39.7%) of 58 SLN macrometastases.

In terms of disease relapse, there were 16 (4.1%) recurrences in the entire cohort of 390 patients over a median follow-up period of 31.1 months. Among the SSL-only group, the recurrence rate was 2.9% (8 of 275). There were 9 (3.3%) of 276 recurrences in the SLN-negative group and 7 (6.1%) of 114 recurrences in the SLN-positive group. Similarly, the recurrence rate was 2.2% (1 of 45) in the SLN micrometastasis group, compared with 8.7% (6 of 69) in the macrometastasis group. In particular, when we examined axillary recurrence alone, the overall recurrence rate was 1.0% (4 of 390), compared with 1.1% (3 of 275) for patients who underwent SSL without axillary clearance. This included one patient with a positive SLN who declined further axillary clearance. Of interest, the mean number of SLNs harvested in patients with tumor recurrence was 1.6, compared with 3.1 for patients without tumor recurrence. The characteristics of the patients who developed recurrence are listed in Table 3Go.


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  		TABLE 3. Patients with recurrent breast carcinoma
 
Thirty-eight (33%) of 114 SLN-positive patients did not receive further ALND. Eleven had SLN macrometastasis, and the remaining 27 had SLN micrometastasis. Only one patient developed a recurrence after a median follow-up period of 29 months in this group.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
One of the most controversial areas in the management of patients with newly diagnosed breast cancer is the value of ALND. The indication and rationale for ALND traditionally include accurate staging to provide information regarding prognosis, locoregional control for patients with metastatic disease to the axilla, and, more controversially, a possible influence on the natural history of disease with a curative intent.

Lymph node metastasis is the single most important prognostic factor in apparently localized breast cancer and has historically been used in planning systemic therapies.7–9 Unfortunately, no currently available imaging studies or biological markers can reliably identify patients with axillary metastases, and hence ALND has conventionally been the mainstay for the nodal staging of patients with breast cancer. The role of ALND in staging and regional control has been established, although its effect on survival remains debatable.

During the last decade, SSL has evolved as an alternative staging procedure to ALND. The SLN is defined as the first lymph node to receive metastases from the primary tumor and is the most likely lymph node to be involved by tumor. SSL is as accurate as ALND when performed by an experienced surgeon. It has a >90% identification rate and a <10% false-negative rate.10

SLN micrometastasis is frequently found with immunohistochemical staining and meticulous examination with serial sectioning of SLNs rather than of a large number of axillary nodes by ALND. The likelihood of positive NSLNs is related to the primary tumor size and the SLN tumor burden. In a multicenter report by Wong et al.,11 14% of T1a tumors had positive NSLNs, and this increased correspondingly up to 45% in T2 tumors.

Chu et al.12 found that the rate of NSLN involvement in SLN micrometastasis was 7% and that it was 55% in SLN macrometastasis. Turner et al.13 investigated 194 SLN-positive patients and found that 63% of patients with SLN macrometastasis had positive NSLNs, compared with 26% of patients with SLN micrometastasis. Also, Viale et al.14 reported that only 15.6% of patients with foci ≤ 1 mm in SLNs had NSLN involvement; this number increased to 36.4% if the SLN focus was 1 to 2 mm and to 44.7% if SLN macrometastasis was present. They concluded that patients with T1 disease and metastatic foci ≤ 1 mm have a significantly lower risk of NSLN metastases and that ALND may be avoided in this group.

In our study, we showed that a positive SLN was a significant factor in predicting further positive NSLNs. In addition, when analyzing the effect of the SLN tumor burden, we found SLN macrometastasis to be significantly associated with NSLN positivity compared with SLN-negative patients. Even when comparing between SLN micrometastasis and macrometastasis, 16.7% (3 of 18) of patients with SLN micrometastasis had positive NSLNs, in contradistinction to 39.7% (23 of 58) of patients with SLN macrometastasis, even though our study numbers were too small to achieve statistical significance in this aspect. However, we can still conclude that patients with SLN macrometastasis should receive routine ALND because of the high likelihood of residual disease in the axilla.

There are several reports in the literature of few or no axillary recurrences after SSL without ALND in patients who are SLN negative.15–22 Veronesi et al.16 reported no recurrences in their series of 285 cases. Badgwell et al.22 had a 3.1% recurrence rate with no isolated axillary recurrences in their series of 159 patients. They reported that pathologic tumor size, lymphovascular invasion, and a positive SLN were significantly associated with disease recurrence.

In our own series of 237 SLN-negative patients who did not undergo further ALND, there were 7 (3.0%) recurrences. Two patients developed axillary recurrences; one was associated with local recurrence and one with systemic relapse. There were no isolated axillary recurrences. Five other patients developed local and/or systemic recurrences without regional disease (Table 3Go).

Among the SLN-positive patients, there were almost four times as many recurrences among the macrometastasis group compared with the micrometastasis group. One (2.2%) of 45 patients with SLN micrometastasis had a disease relapse as compared with 6 (8.7%) of 69 patients with SLN macrometastasis. All the SLN macrometastasis patients who developed recurrence had undergone ALND, and none of those without ALND developed recurrence. The SLN macrometastasis patients with recurrence all had local and/or systemic failure except for one patient, who developed isolated regional recurrence. This patient had 24 positive nodes out of 35 during ALND.

It has been conventional practice to offer ALND in patients with a positive SLN detected on H&E stain. However, some patients do not undergo this second procedure for a variety of reasons. Guenther et al.23 reported that among their series of 46 patients with SLN metastases who did not undergo ALND, there were no axillary recurrences after a median follow-up period of 32 months. Of these patients, 15% had macrometastases, 35% had micrometastases, and 50 % had only cellular metastases.

In our series, 33% (38 of 114) of patients with positive SLNs did not receive further ALND. The mean tumor size of this group was 16.9 mm. Eleven of these patients had tumor sizes >20 mm. Twenty-four of these patients received radiotherapy that included the axillary field. After a median follow-up period of 29 months in this group, only one patient developed recurrence. This patient had a primary tumor size of 32 mm with a single positive SLN micrometastasis. She underwent a mastectomy but did not receive any further adjuvant treatment. She subsequently developed regional and systemic failure 17 months after the operation. There were no recurrences in the remaining 37 patients, of whom 26 had SLN micrometastases and 11 had macrometastases.

We conclude that SLN tumor burden is a vital determinant in NSLN status and may play an important role in recurrence rates. SLN macrometastasis confers a higher risk of positive NSLNs and is also likely a contributory factor to disease recurrence, although a longer follow-up period with standardized treatment for all patients is necessary to statistically determine the difference in disease-free survival among SLN micrometastasis and macrometastasis patients. For patients with SLN macrometastasis, we recommend complete ALND. For patients with SLN micrometastasis, the role of completion ALND remains controversial. We await the results of further prospective randomized trials to provide a definitive resolution to this controversy.

Received for publication August 31, 2004. Accepted for publication May 12, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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