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10.1245/s10434-006-9012-1
Annals of Surgical Oncology 13:1457-1465 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Prognosis of Breast Cancer After Supraclavicular Lymph Node Metastasis: Not a Distant Metastasis

Shin-Cheh Chen, MD1, Hsien-Kun Chang, MD2, Yung-Chang Lin, MD2, Wai-Man Leung, MD3, Chien-Sheng Tsai, MD3, Yun-Chung Cheung, MD4, Swei Hsueh, MD5, Lai-Chu See, PhD6 and Miin-Fu Chen, MD, FACS1

1 Department of Surgery, Chang-Gung Memorial Hospital, Chang Gung University Medical College, 5, Fu-Shing Street, Kwei-Shan, Taoyuan, Taiwan
2 Department of Medical Oncology, Chang-Gung Memorial Hospital, 5, Fu-Shing Street, Kwei-Shan, Taoyuan, Taiwan
3 Department of Radiation Oncology, Chang-Gung Memorial Hospital, 5, Fu-Shing Street, Kwei-Shan, Taoyuan, Taiwan
4 Department of Diagnostic Radiology, Chang-Gung Memorial Hospital, 5, Fu-Shing Street, Kwei-Shan, Taoyuan, Taiwan
5 Department of Pathology, Chang-Gung Memorial Hospital, 5, Fu-Shing Street, Kwei-Shan, Taoyuan, Taiwan
6 Department of Public Health, Statistic Center, Chang Gung University Medical College, Taoyuan, Taiwan

Correspondence: Address correspondence and reprint requests to: Shin-Cheh Chen, MD; E-mail: chensc{at}adm.cgmh.org.tw.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We performed this study to analyze the survival of breast cancer patients with isolated supraclavicular lymph node metastasis (SLNM) and assess whether SLNM is distant metastasis or not.

Methods: Sixty-three patients who developed an isolated SLNM among 3170 primary breast cancer patients between 1990 and 1999 were enrolled. The survival after SLNM was compared with that of 151 patients who developed local recurrences and 599 who had distant metastasis and was analyzed according to different levels and numbers of positive axillary nodes.

Results: Thirty-five of the 63 patients died during a median follow-up of 58.3 months. The 5-year overall survival (OS) rates after SLNM, local relapse, and distant metastasis were 33.6%, 34.9%, and 9.1%, respectively. The 5-year OS for patients with involved nodes confined to axillary level I was 74.4%, which was significantly better than that for involved nodes in level II or III or SLNM (49.2%, 52.8%, and 33.6%, respectively; P < .0001). For one to three positive axillary nodes, the 5-year OS was 83.2%, which was significantly better than that for four to nine positive nodes, more than nine positive nodes, and SLNM (62.6%, 42.3%, and 33.6%, respectively). There was no significant difference between SLNM and more than nine positive nodes. Surgical removal of the supraclavicular nodes was a significantly better prognostic factor for OS after SLNM (P = .0327).

Conclusions: The 5-year OS after supraclavicular nodal metastosis, local relapse, and distant metastasis were 33.6%, 34.9%, and 9.1%, respectively. Good neck control either by surgery or chemotherapy achieved better survival.

Key Words: Breast cancer • Supraclavicular lymph node metastasis • Prognosis • Metastasis • Neck dissection


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Regional lymphatic relapse in breast cancer is a difficult problem to manage. Moreover, supraclavicular lymph node metastasis (SLNM) has been classified as an almost invariable signal of micrometastasis because of its very poor prognosis.1–6 Primary breast cancer with SLNM was staged as pN3c in the new staging edition,7 and this indicated that synchronous SLNM was not considered as a distant metastasis. The instance of metachronous SLNM was directly related to the involved nodes of axillary levels in our recent study,8 which suggested that metachronous ipsilateral SLNM is a regional disease rather than a distant metastatic disease. In this study, we analyzed the survival after SLNM and compared it with the survival of patients with local and distant relapse. This verified that metachronous SLNM is not a distant metastasis.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The medical records of a cohort of 3170 patients with breast carcinoma who received surgical treatment at Chang Gung Memorial Hospital, LinKou Medical Center, between 1990 and 1999 were reviewed, and data were collected on the survival of patients who developed first isolated SLNM, isolated locoregional (chest wall and axillary) recurrence, or distant metastasis (including patients who developed concomitant SLNM and distant metastasis). Isolated SLNM was defined as having no evidence of distant metastasis within 3 months. A systemic survey included serum tumor markers, chest X-ray, bone scan, and ultrasound scan of the liver for all patients; neck or whole-body computed tomographic scan was performed for selected patients.

Records for the database of breast cancer patients in the hospital were updated monthly, and data on survival were regularly updated by the data manager. There were 2725 (86%) patients who received simple or modified radical mastectomy and 445 (14%) who received conservative surgery. Axillary dissection or sampling was performed in 97% of the patients; level I (lymphatics lateral to the pectoralis minor muscle) and level II (lymphatics under the pectoralis minor muscle) dissection was performed in 2274 patients (72%); and level I, II, and III (lymphatics medial to the pectoralis minor muscle) dissection was performed in 795 patients.

Adjuvant therapy was given to most of the patients who followed the Chang Gung Memorial Hospital treatment guidelines. The guidelines for adjuvant therapy can be briefly summarized as follows: no adjuvant therapy was given to low-risk patients (negative nodes in postmenopausal women, invasive tumor size <1 cm, and positive estrogen receptor status). Chemotherapy with cyclophosphamide, methotrexate, and 5-fluorouracil was given to patients who were node negative with any risk factor and patients with one to three positive axillary nodes. Cyclophosphamide, epirubicin, and 5-fluorouracil were given to patients with more than four positive axillary nodes. Hormonal therapy (tamoxifen) was given for 5 years to patients with a positive estrogen receptor status. Radiotherapy was administered only in patients with tumors >5 cm, axillary nodal status classified as N2 clinically, or >10 positive axillary nodes.

Treatment After SLNM
All cases of SLNM were histologically proven. Nineteen patients had received fine-needle aspiration cytological analysis only, 15 had excisional biopsies under local anesthesia, and 29 had more radical surgery (supraclavicular level IV and V lymph node dissection). In patients who received neck dissection, the average number of removed lymph nodes was 14, and the average number of positive nodes was 8. There were 51 patients who received chemotherapy with a regimen containing anthracycline or a taxane after the identification of SLNM, 25 patients who received radiotherapy, and 42 patients who received further hormonal therapy.

The following prognostic factors were analyzed for their influence on postrelapse survival: age at diagnosis, tumor size, hormonal status, DNA flow cytometry (ploidy and synthetic phase fraction), axillary nodal status, disease-free interval, adjuvant chemotherapy, radiotherapy, and hormonal therapy. In addition, a DNA flow cytometry study was performed as described previously.8 The ploidy status was classified as diploid or nondiploid (including tetraploid, aneuploid, and hypoploid tumors). Synthetic phase fraction was classified as high if >7% and low if less double equals7%. The influences of surgical treatment, salvage chemotherapy, radiotherapy, and hormonal therapy on survival after SLNM were also studied as separate prognostic factors.

Statistical Analysis
Distant metastasis-free survival (DMFS) was de-fined as the time from primary surgery or SLNM until the identification of distant metastasis. The overall survival (OS) was defined as the time of the primary operation or identification of SLNM until death, whether or not death was related to breast cancer. DMFS and OS rates were computed according to the Kaplan-Meier method, and survival curves were compared by using the log-rank test. The Cox regression model provided multivariate analysis of prognostic factors for OS.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Cohort Survey
The median duration of follow-up for the 3170 patients was 58.3 months; it was 49.1 months for patients with locoregional relapse, 60.5 months for those with SLNM, and 36.4 months for those with distant metastasis. There were 151 patients who developed first isolated locoregional recurrence (including 128 involving the chest wall and 23 involving axillary regional relapse) during the follow-up period, 63 women developed SLNM as the first, isolated relapse (including 4 cases concomitant with chest wall relapse and 1 patient with axillary relapse), and 599 developed distant metastasis (Table 1Go). There was no significant difference in the mean age of patients in the three groups. The average primary tumor size was 3.5 cm for patients who developed local recurrence, 3.3 cm for those who developed SLNM, and 3.7 cm for those who developed distant metastasis. Approximately 70% of the patients who developed local or distant metastasis or SLNM had positive axillary nodes at the primary operation. Sixty percent of SLNM patients had a negative estrogen receptor status.


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  		TABLE 1. Characteristics of Local, Neck and Distant Relapse of Breast Cancer
 
Prognostic Factors in Patients with SLNM
The univariate analysis of the prognostic factors for the 5-year survival rate is shown in Table 2Go. Thirty-five patients had comprehensive radiotherapy, including the chest wall and supraclavicular fossa, after the primary operation. The only factor that had a significant influence on survival was age less double equals40 years. The 5-year OS after SLNM was 43.3% for patients >40 years and 16.2% for patients less double equals40 years (P = .0437).


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  		TABLE 2. Univariate analysis of prognosis in patients with Supraclavicular Lymph Node Metastasis
 
Prognosis of SLNM with Respect to Local and Distant Relapse
The median interval from primary surgery to local relapse, SLNM, and distant relapse was 16, 25, and 21 months, respectively. Among the 151 patients with local relapse, 88 (58.3%) died of disease progression, with a median survival of 23 months after relapse. After the diagnosis of SLNM, 35 (55.6%) patients died, with a median survival of 32 months. Among the 599 patients with distant metastasis, 503 (84.0%) died, with a median survival of 12 months. The 5-year OS after local metastasis, SLNM, and distant metastasis was 34.9% (95% confidence interval [CI], 26.0%–43.7%), 33.6% (95% CI, 18.8%–48.4%), and 9.1% (95% CI, 6.2%–12.0%), respectively (Fig. 1Go). There was no significant difference in OS between patients with local recurrence and SLNM (P = .5526), but patients with local relapse or SLNM had significantly better OS than those with distant metastasis (P < .0001).


Figure 1
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  		FIG. 1. Overall survival of supraclavicular lymph node metastasis (SLNM) with respect to local and distant relapse.

 
In the follow-up period, 95 (62.9%) of 151 patients with local relapse developed distant metastasis, and 46 (73%) of 63 SLNM patients developed distant metastasis. The 5-year DMFS was 30% (95% CI, 21.5%–38.5%) for patients with local relapse and 14.5% (95% CI, 3.4%–25.5%) for patients with SLNM. The difference was not significant (P = .5790; Fig. 2Go).


Figure 2
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  		FIG. 2. Distant metastasis – free survival of supraclavicular lymph node metastasis (SLNM) with respect to local relapse.

 
Prognosis of SLNM in Relation to Axillary Levels of Positive Nodes
There were 954 (71.6%) patients with positive nodes confined only to axillary level I, 258 (19.3%) with level II involvement, and 121 (9.1%) with level III involvement. There were 262 (27.5%) deaths among the 954 patients with level I involvement and 129 (50%) deaths among the 121 patients with level III involvement. The 5-year OS was 74.4% 95% CI, 71.4%–77.4%) for patients with level I involvement, 49.2% (95% CI, 42.4%–55.9%) for level II involvement, and 52.8% (95% CI, 43.2%–62.3%) for level III involvement. The 5-year OS of patients with SLNM was significantly poorer than that for those with level I, II, or III involvement (Fig. 3AGo). Among the 954 patients with level I involvement, 313 (32.8%) developed distant metastasis, whereas 137 (53.1%) of 258 patients with level II involvement and 60 (49.6%) of 121 with level III involvement developed distant metastasis. The 5-year DMFS was 66.5% (95% CI, 63.3% – 69.7%) for patients with level I involvement, 44.3% (95% CI, 37.8% – 50.8%) for level II involvement, and 49.7% (95% CI, 40.7% – 58.8%) for level III involvement. The 5-year DMFS of patients with SLNM was significantly poorer than in any other group (P < .0001; Fig. 3BGo).


Figure 3
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  		FIG. 3. Overall (A) and distant metastasis – free (B) survival of supraclavicular lymph node metastasis (SLNM) with respect to the axillary level of positive lymph nodes.

 
Prognosis of SLNM in Relation to the Number of Positive Axillary Nodes
There were 1333 patients with axillary lymph node metastasis identified at primary surgery. The median number of total lymph nodes examined after axillary dissection was 17, with a range of 4 to 64. Six hundred thirty-three patients (47.5% of the positive axillary node patients) had 1 to 3 positive lymph nodes, 376 (28.2%) patients had 4 to 9 positive nodes, and 324 (24.3%) patients had >9 positive nodes. A shorter OS was associated with an increasing number of positive axillary nodes (P < .0001). There were 125 (19.7%) deaths among the 633 patients with 1 to 3 positive axillary nodes, 138 (36.7%) deaths among the 376 patients with 4 to 9 positive axillary nodes, and 182 (56.2%) deaths among the 324 patients with >9 positive axillary nodes. The 5-year OS was 83.2% (95% CI, 80% – 86.4%) for patients with one to three positive nodes, 62.6% (95% CI, 57.2% – 68%) for four to nine positive nodes, and 42.3% (95% CI, 36.4% – 48.3%) for more than nine positive nodes. The 5-year OS of patients with SLNM was significantly poorer than that for patients with one to three or four to nine positive nodes (P < .0001; Fig 4AGo).


Figure 4
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  		FIG. 4. Overall (A) and distant metastasis – free (B) survival of supraclavicular lymph node metastasis (SLNM) with respect to the number of positive axillary lymph nodes.

 
Distant metastasis developed in 158 (25.0%) of 633 patients with 1 to 3 positive axillary nodes, 161 (42.8%) of 376 patients with 4 to 9 positive axillary nodes, 191 (59.0%) of 324 patients with >9 positive nodes, and 56 (74.7%) of 75 patients with SLNM. The 5-year DMFS was 75% (95% CI, 71.4% – 78.6%) for patients with one to three positive nodes, 55.8% (95% CI, 50.4% – 61.1%) for four to nine positive nodes, and 38% (95% CI, 32.3% – 43.7%) for more than nine positive nodes. The DMFS of patients with SLNM was significantly poorer than in any of the other groups (P < .0001; Fig. 4BGo).

Death occurred in 37 (46.3%) of 80 patients with >9 positive nodes confined only in axillary level I and occurred in 105 (43%) of 244 patients with >9 positive nodes located beyond level I. For patients with more than nine positive nodes limited to level I or beyond level I, the 5-year OS was 46.8% (95% CI, 34.8% – 58.8%) and 41% (95% CI, 34.2% – 47.8%) and the 5-year DMFS was 40.5% (95% CI, 28.5% – 58.5%) and 39.3% (95% CI, 30.7% – 43.6%), respectively. There were no significant differences in the 5-year OS among the three groups (P = .5381; Fig. 5AGo). Patients with SLNM had slightly poorer 5-year DMFS in comparison to those with more than nine nodes either limited to level I or beyond level I (P = .0449; Fig. 5BGo).


Figure 5
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  		FIG. 5. Overall (A) and distant metastasis – free (B) survival of supraclavicular lymph node metastasis (SLNM) with respect to the number and level of positive axillary lymph nodes.

 
Effect of Treatment on OS After SLNM
Patients who received either excisional biopsy or total removal of the metastatic tumor (dissection of neck level IV and V lymph nodes) had a better 5-year OS than those who underwent only fine-needle aspiration cytological analysis (42.4% and 16.3%, respectively; P = .0327; Table 3Go). Patients who achieved good control of metastatic nodes in the neck region (defined as a lack of gross residual mass on the neck) by any treatment modality had a better 5-year OS (63.7% and 18.3%, respectively; P = .0136). Salvage chemotherapy, radiotherapy, and second line hormonal therapy did not result in a significantly decreased risk of death. Multivariate analysis demonstrated that good neck control significantly improved survival, with an odds ratio of 2.7 (P = .017).


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  		TABLE 3. Univariate analysis of overall survival after Supraclavicular Lymph Node Metastasis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study, we demonstrated that survival was worse in patients after the discovery of metachronous SLNM than in patients who had <10 positive axillary nodes in level I, II, or III but that it was better than in patients who developed distant metastasis. Similar results have been recently reported for patients treated with aggressive systemic and regional therapy.9,10

Regional lymph relapse of breast cancer is much more difficult to manage than local recurrence and is also associated with a significantly greater morbidity.4 In a previous study, the incidence rate of axillary relapse was reported between .8% and 6%,11 but a low rate of axillary relapse was found in patients with adequate treatment of the axilla.12–14 Picrquin et al.15 and Recht et al.16 reported that the incidence of SLNM was <1% when adjuvant radiotherapy was given. We previously reported the incidence of SLNM was 4.3% and that it was related to the number of positive axillary nodes and the axillary level of involved nodes but not to whether the patient received radiotherapy.8 Anatomically, the central axillary (level I), subclavicular fossa, and interpectoral (Rotter’s) lymph nodes drain along the branches of the thoracoacromial vessel and follow centrally to the subclavicular nodes and the supraclavicular fossa.17,18 It is evident that there is a continuum between axilla levels II and III and supraclavicular fossa, as was also reported by Brito et al.9 Observations during sentinel node mapping and biopsy indicate that the lymphatic drainage follows almost a regular route to the central, subclavicular, and then supraclavicular or internal mammary groups. The supraclavicular nodes are actually only secondarily involved when the axilla (level II or III) is substantially involved in breast cancer.19,20 Isolated SLNM can be found more frequently than axillary relapse if the supraclavicular fossa is carefully examined, especially for patients with axillary node involvement.

Fodor et al.5 reported that there was only a 5% OS in patients with SLNM after 3 years. Halverson et al.2 reported that the 5-year OS of SLNM was poorer than that in patients with chest wall or axillary relapses (13%, 35%, and 37%, respectively). SLNM has been classified as a distant metastasis or incurable multiple skin recurrence with poor prognosis and is considered a candidate for aggressive systemic treatment.1,6 Recently, Olivotto et al.10 reported that the 5-year OS was 33.3% for those synchronous SLNMs with primary breast cancer, and 13% of the patients still survived 20 years after diagnosis. Brito et al.9 reported that the 5-year OS of synchronous SLNM patients was 41% after multimodality treatment. In this series, 5-year OS rates of metachronous SLNM and local relapse were significantly better than those in patients with distant metastasis. These findings suggest that metachronous SLNM is similar to local relapse, should not considered as a nidus for dissemination, and should be classified as locoregional relapse rather than metastasis.

The number and level of positive axillary nodes are the most important prognostic factors in breast cancer.21–24 Jatoi et al.25 found a continuing associated decline in survival for patients with an increased number of positive nodes. Several studies have found that patients with higher-level involvement have significantly poorer survival than those with only level I involvement.26,27 This study found that not only the number, but also the level, of positive axillary nodes influences DMFS and OS. The survival of patients with SLNM was poorer than that of those with lower axillary (level I) or subclavian (level II and III) nodal involvement, and the 5-year DMFS for SLNM was quite low (14.5%). However, there was no difference in comparison to local relapse. The 5-year OS (33.6%) of SLNM was found no different to those with 10 or more positive nodes patients (42.3%), that significantly worse in order than with 4 to 9 or 1 to 3 positive nodes, but much better than those with distant metastasis. All these results indicated that there was a continuum in the lymphatics and that they drained in a regular, sequential pattern of level I, II, and III and the supraclavicular nodes. Thus, we will treat SLNM as a locoregional relapse rather than distant metastasis.

The only prognostic factor for death in the 63 SLNM patients was young age. Patients <40 years old at diagnosis of the primary tumor had a poor 5-year survival rate of 16.2%. Other than this, we did not find any other primary tumor characteristic that affected survival (Table 2Go). Local surgical treatment (excision of gross tumor) significantly influenced the survival in this series (Table 3Go). However, the indications for local treatment after SLNM have been widely questioned.28,29 A review by Debois3 found that survival after SLNM was not influenced by local or systemic treatment. By contrast, Pergolizzi et al.30 reported that the median survival time increased from 27.5 to 48 months when radiotherapy was administered. If SLNM is more like a locoregional relapse than systemic metastasis, one can assume that aggressive local treatment will improve survival.31,32 Brito et al.9 reported that the 5-year OS was 41% when curative intent multimodality therapy consisting of chemotherapy, surgery, and radiotherapy was administered for synchronous SLNM. This is consistent with the conclusion in a review by Noguchi33 that locoregional control is important for enhancing survival in the presence of systemic therapy. In this series, we found that treatment with salvage chemotherapy, hormonal therapy, or radiotherapy after SLNM was associated with better survival, but this was not statistically significant. In the Cochrane Review, Rauschecker et al.34 also found that systemic therapy improved the local control rate, but it had no apparent effect on OS. Even though the number of patients with SLNM in our series was fairly large, it was still not enough to make a definite conclusion about the role of surgical treatment because the treatments after SLNM were not assigned randomly. When SLNM was identified, computed tomographic scans of the neck and body clearly indicated the extent and the adjacent organs involved. Good neck control, either by surgery or systemic therapy, can achieve better survival.

In conclusion, the occurrence of SLNM was not less frequent than local or axillary relapse, especially in patients with more than four positive axillary nodes. Ipsilateral SLNM was considered as a progression of lymphatic metastasis from the central axillary group to the neck. In this series, we found better OS in patients with SLNM in comparison to those who developed distant metastasis. In addition, the OS was worse in SLNM than in those with subclavian (level II or III) nodal involvement and was similar to that in those with ≥10 positive axillary nodes. Whether SLNM should be categorized as locoregional relapse or distant metastasis needs further study, and the role of surgical treatment should be established.

Received for publication November 22, 2005. Accepted for publication January 20, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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H. J. Moon, M. J. Kim, E.-K. Kim, B.-W. Park, J. H. Youk, J. Y. Kwak, J. Sohn, and S.-I. Kim
US Surveillance of Regional Lymph Node Recurrence after Breast Cancer Surgery
Radiology, June 22, 2009; (2009) 2523081977.
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