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ORIGINAL ARTICLE
Year : 2022  |  Volume : 18  |  Issue : 2  |  Page : 496-502

The role of surgery on locoregional treatment of patients with breast cancer newly diagnosed with ipsilateral supraclavicular lymph node metastasis


The First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer; Key Laboratory of Cancer Prevention and Therapy; Tianjin Clinical Research Center for Cancer; Key Laboratory of Breast Cancer Prevention and Therapy, Tianjin Medical University, Ministry of Education, Tianjin, China

Date of Submission25-May-2021
Date of Decision17-Feb-2022
Date of Acceptance21-Feb-2022
Date of Web Publication20-May-2022

Correspondence Address:
Xu-Chen Cao
The First Department of Breast Cancer, Tianjin Medical University Cancer Institute and Hospital, Huan-Hu-Xi Road, He-Xi District, Tianjin 300060
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.jcrt_844_21

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 > Abstract 


Background: Radiotherapy is a practical locoregional treatment approach for women with breast cancer who show ipsilateral supraclavicular lymph node metastasis (ISLNM) on diagnosis. However, there is controversy around the role of supraclavicular lymph node dissection. Therefore, we aimed to study the significance of supraclavicular surgery based on radiotherapy.
Patients and Methods: We retrospectively reviewed the data of 142 patients with breast cancer who presented with isolated ISLNM and received radiotherapy between the years 2000 and 2016. We also defined the effect of surgery on locoregional treatment of these patients by analyzing the prognostic factors for recurrence-free survival (RFS), distant metastasis-free survival (DMFS), and overall survival (OS).
Results: We observed that, of the 142 patients, 104 who received radiotherapy underwent supraclavicular lymph node dissection. Also, among the study group, the progesterone receptor (PR) status (P = 0.044) and the number of axillary lymph nodes (ALNs) involved (P = 0.002) were significant independent predictors of RFS. Also, tumor size (P = 0.007), PR (P < 0.001), and number of ALNs (P < 0.001) were independent predictors of DMFS and were statistically significant. Also, PR was an independent prognostic factor of OS (P = 0.033), whereas the supraclavicular surgery was not an independent prognostic factor for RFS, DMFS, and OS. Furthermore, our study focused on 92 patients with negative estrogen receptors (ERs). The result showed that supraclavicular surgery was statistically significant for RFS (P = 0.023); no significant differences in DMFS and OS were found between patients who received supraclavicular surgery and those who did not.
Conclusion: Radiotherapy may be the primary locoregional treatment approach for patients with breast cancer who present with newly diagnosed ISLNM. Additionally, supraclavicular surgery may be more appropriate for patients with negative ER who received radiotherapy.

Keywords: Breast cancer, radiotherapy, supraclavicular lymph node metastasis, surgery


How to cite this article:
Liu BW, Chen LX, Ma K, Chi JR, Yang ZJ, Yu Y, Cao XC. The role of surgery on locoregional treatment of patients with breast cancer newly diagnosed with ipsilateral supraclavicular lymph node metastasis. J Can Res Ther 2022;18:496-502

How to cite this URL:
Liu BW, Chen LX, Ma K, Chi JR, Yang ZJ, Yu Y, Cao XC. The role of surgery on locoregional treatment of patients with breast cancer newly diagnosed with ipsilateral supraclavicular lymph node metastasis. J Can Res Ther [serial online] 2022 [cited 2022 Jul 7];18:496-502. Available from: https://www.cancerjournal.net/text.asp?2022/18/2/496/345545

Bo.Wen Liu, Li.Xuan Chen, Ke Ma contributed equally to this work.





 > Introduction Top


Lymph node metastasis (LNM) is a primary indicator of breast cancer. Although only 1%–4% of women with breast cancer have clinically evident ipsilateral supraclavicular lymph node metastasis (ISLNM) on initial visit,[1] 60% of them eventually develop distant metastases within 18 months after diagnosis.[2] Women with breast cancer and ISLNM have a median survival of only 2–4 years.[3],[4] Additionally, ISLNM is closely associated with age, the number of axillary lymph nodes (ALNs), the tumor's size, and breast cancer molecular subtypes.[5]

The 1988 American Joint Committee on Cancer (AJCC) TNM staging system 3th Edition defined breast cancer with ISLNM as stage M1, not N3, due to poor prognosis. However, in 2001, Brito et al.[6] reported that women with breast cancer and ISLNM had significantly longer overall survival (OS) than women with stage IV tumors (P < 0.001). Therefore, the AJCC revised the TNM staging system in 2003, reclassifying breast cancer with ISLNM into stage N3c,[7] providing a basis for locoregional treatments.

Combined treatments, including chemotherapy, radiotherapy, and endocrine therapy are recommended for patients with breast cancer and ISLNM at diagnosis. Locoregional therapy towards the supraclavicular region, especially radiotherapy, is integral to the multimodal treatment approach. Recently, substantial evidence suggests radiotherapy is an effective locoregional treatment for patients with ISLNM, consequently enhancing their survival.[6],[8],[9]

However, the supraclavicular lymph node dissection role remains controversial for patients with ISLNM. The scope of surgical dissection includes the adipose tissue and lymph nodes in regions IV and V of the scapular hyoid muscle clavicle triangle and the scapular hyoid muscle trapezius triangle. Additionally, several studies showed that locoregional surgery enhanced the survival of patients with ISLNM;[10],[11] however, contradictory by other studies. Moreover, no significant difference existed in the median OS and recurrence-free survival (RFS) between patients who underwent supraclavicular dissection and those who did not, according to some reports.[12] The latest NCCN guidelines recommend that patients with ISLNM be treated with a multimodal approach, including radiotherapy; however, these guidelines do not guide whether locoregional surgery should be performed for lesion control.

In this retrospective study, we aimed to investigate the survival outcomes of women with breast cancer and ISLNM, and analyze the prognostic determinants of survival in these patients.


 > Patients and Methods Top


Patients

We retrospectively reviewed the clinicopathologic data of primary women with breast cancer and ISLNM at Tianjin Medical University Cancer Institute and Hospital, Tianjin, China between August 2000 and May 2016. Also, breast cancer was staged according to the 7th edition of the AJCC staging system. The eligible patients were women aged 18 years or older who had an Eastern Cooperative Oncology Group performance status (ECOG-PS) score of 0 or 1. The major exclusion criteria were 1) ipsilateral supraclavicular lymph node recurrence after radical or modified radical mastectomy, 2) inflammatory breast cancer, 3) bilateral breast cancer, and 4) other primary cancers.

Additionally, no patient consent was required since the study was of a retrospective nature. Patient data were anonymized in the report.

Patient evaluation

We retrieved the following demographic and baseline variables from the electronic records system of our hospital: age, tumor size, number of ALNs, ECOG-PS score, estrogen receptor (ER), progesterone receptor (PR), human epidermal growth factor receptor 2 (HER2) status, trastuzumab therapy, adjuvant and neoadjuvant chemotherapy, and supraclavicular surgery. ISLNM was diagnosed adopting either excisional biopsies or ultrasound-guided fine needle aspirations. Also, HER2 overexpression was defined as +++ in immunohistochemistry or + in fluorescence in situ hybridization (FISH). The objective response rate (ORR) was the part of patients in the study population who attained complete response (CR), and progesterone receptor (PR) was assessed using the Response Evaluation Criteria in Solid Tumors (RECIST v. 1.0).

Follow-up

Follow-up was performed as clinical visits for the patients every three months for the first year, every six months for the following two years, and subsequently, yearly. All patients were evaluated physically, including ECOG-PS and routine laboratory investigations. Also, the postoperative evaluation included ultrasonography, chest computed tomography (CT) scan, breast magnetic resonance imaging (MRI), bone scan, positron emission tomography-CT (PET/CT) scan, and biopsy of suspicious lymph nodes. The last date of follow-up was 28 September 2017.

Statistical analysis

The Statistical Package for the Social Sciences (SPSS v. 22.0) was used, whereas the data were presented as mean ± standard deviation. The categorical variables were analyzed using a χ2 test or Fisher's exact test. Additionally, RFS was calculated from the surgery date to radiological or pathological confirmation of tumor recurrence of surgical or draining lymph node area. Distant metastasis-free survival (DMFS) was also derived from the histologically proven ISLNM date to the radiologically or pathologically confirmed distant metastasis date. Furthermore, the OS was calculated from the surgery date to the breast cancer–specific date of death. Interestingly, survival was censored at the date of death of other causes or the last follow-up visit. DMFS and OS were calculated using the Kaplan–Meier method, and a comparison of survival curves was performed using the log-rank tests. The primary study outcome was RFS, and the secondary results were DMFS, OS, and ORR. The univariate analysis evaluated the correlation between variables and RFS, DMFS, or OS, and variables with P < 0.15 were entered into the multivariate analysis. Furthermore, the Cox proportional hazards model was applied for multivariate analysis, and statistical significance was set at a value of P < 0.05.


 > Results Top


Demographic and baseline characteristics of the study population

The study flowchart, shown in, reveals that 157 women with breast cancer were diagnosed with ISLNM during the period, 15 women were excluded, attributing to follow-up loss, leaving 142 patients with breast cancer to be eligible for the study. Their median age was 51 years between a range of 27–68 years, and 80 women (56.3%) were postmenopausal. Additionally, all patients had invasive ductal carcinoma. Furthermore, 35.2% of women were ER-positive, 38.0% were PR-positive, and 26.8% had HER2 overexpression. The demographic and baseline characteristics of the study population are shown in [Table 1].
Table 1: Demographic and baseline characteristics of the study population

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Treatment characteristics of the study population

The treatment characteristics of the study population are shown in [Table 2]. Approximately 97.2% of patients received radical or modified radical mastectomy, and only four received breast-conserving surgery. Furthermore, 104 patients (73.2%) underwent supraclavicular lymph node dissection; 80 patients (56.4%, 80/142) received neoadjuvant chemotherapy, with the taxane-based regimen as the most common (42.3%). Moreover, 132 patients received adjuvant chemotherapy, with the anthracycline and taxane–based regimen being the most common (49.3%). All patients received radiotherapy to the chest wall, the supraclavicular fossa, or the internal mammary region. Additionally, the dosage was 50 Gy (range, 40–65 Gy) and 60 Gy (range, 50–70 Gy) for the chest wall and the supraclavicular region, respectively. 46 patients with positive hormone receptor status received endocrine therapy. Among ER-negative women (n = 92), only 64 women (69.6%) underwent supraclavicular surgery, whereas 86 received adjuvant chemotherapy. Premenopausal patients were given tamoxifen for 5 years, whereas postmenopausal women received aromatase inhibitors, and four women (4/38, 10.5%) with HER2 overexpression in breast cancer received trastuzumab.
Table 2: Treatment characteristics of the study population

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ORR

The patients who were followed up were 157 in number, revealing the median follow-up duration to be 57 months, between 12 and 143 months. However, 15 patients were lost to the follow-up. Among 80 patients who underwent neoadjuvant chemotherapy, 14 (14/80, 17.5%) women achieved CR, 60 women (60/80, 75.0%) achieved PR, and no SD. Additionally, six patients (6/80, 7.5%) progressed after neoadjuvant chemotherapy, whereas the ORR was 92.5% (95% CI, 86.6–98.4%).

RFS

Additionally, 50 women (35.2%) experienced relapses. The median RFS was 16 months (95% CI, 18.27%–31.41%), and the rate of RFS was 64.8% (95% CI, 27.3%–43.2%). Notably, 26 women (18.3%) had a relapse in the ipsilateral chest, 26 (18.3%) had a relapse in the ipsilateral supraclavicular lymph nodes, and 16 (11.3%) had a relapse in the ALN. Also, the univariate analysis showed that age (P = 0.06), number of ALNs (P = 0.002), PR (P = 0.044), neoadjuvant chemotherapy (P = 0.005), and supraclavicular surgery (P = 0.043) were significantly associated with RFS [Table 3]. The multivariate analysis showed that PR (HR = 0.516; 95% CI, 0.271–0.984; P = 0.044) and a number of ALNs (HR = 6.557; 95% CI, 1.958–22.094; P = 0.002) were significant and independent predictors of RFS [Table 4].
Table 3: Univariate analysis of prognostic factors of RFS, DMFS, and OS

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Table 4: Multivariate analysis of prognostic factors of RFS, DMFS, and OS

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DMFS

At the median follow-up duration, 78 women (54.9%) had distant metastases, including bone metastasis (9.9%) and lung metastasis (7%), followed by liver metastasis (4.2%) and central nervous system metastasis (2.8%). Also, the median DMFS was 22 months (95% CI 26.16–37.51), and the rate of DMFS was 45.1% (95% CI, 46.6%–63.2%). Additionally, univariate analysis showed that age (P = 0.049), tumor size (P = 0.079), number of ALNs (P = 0.001), ER (P = 0.105), PR (P = 0.001), and HER2 statuses (P = 0.061), and neoadjuvant chemotherapy (P = 0.081) were significantly associated with DMFS [Table 3]. Furthermore, the multivariate analysis revealed statistical significance in tumor size (HR = 2.576; 95% CI, 1.293–5.134; P = 0.007), PR status (HR = 0.244; 95% CI, 0.113–0.528; P < 0.001), and number of ALNs (HR = 10.027; 95% CI, 2.970–33.848; P < 0.001), which were also independent predictors of DMFS.

OS

Additionally, 56 women (39.4%) died at the end of the study. Results showed that the median OS was 62 months (95% CI, 54.18%–71.37%), and the rate of OS was 60.6% (95% CI, 52.4%–68.7%). Univariate analysis showed that age (P = 0.056), the number of ALNs (P = 0.001), ER (P < 0.001) and PR statuses (P < 0.001), and neoadjuvant chemotherapy (P = 0.052) were significantly attributed to OS [Table 3]. Additionally, multivariate analysis revealed that PR (HR = 0.331; 95% CI, 0.120–0.915; P = 0.033) was an independent prognostic factor of OS [Table 4].

Subgroup analysis of ER-negative women

The univariate analysis indicated that among the ER-negative women (n = 92), supraclavicular surgery (P = 0.046), age (P = 0.061), the number of ALNs (P = 0.055), and PR status (P = 0.101) were significantly related to RFS [Table 5]. Our multivariate analysis further revealed supraclavicular surgery as a statistically significant favorable factor of RFS (HR = 0.424; 95% CI, 0.202–0.891; P = 0.023), whereas the number of ALNs was a statistically significant adverse risk of RFS (HR = 8.958; 95% CI, 1.543–52.022; P = 0.015) [Table 6]. Furthermore, PR status was a statistically substantial favorable factor of DMFS (HR = 0.169; 95% CI, 0.039–0.734; P = 0.018); however, the number of ALNs was a statistically significant adverse risk factor for DMFS (HR = 10.116; 95% CI, 1.776–57.620; P = 0.009).
Table 5: Univariate analysis of prognostic factors of RFS, DMFS, and OS of ER-negative patients

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Table 6: Multivariate analysis of prognostic factors for RFS, DMFS, and OS for ER-negative patients

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 > Discussion Top


This retrospective analysis of the prognostic factors of radiotherapy in 142 cases of newly diagnosed patients with breast cancer and ISLNM showed supraclavicular surgery as an independent prognostic factor for RFS of the study group (P = 0.194). Simultaneously, it was an independent prognostic factor for RFS among patients with negative ER (P = 0.023). Therefore, the importance of supraclavicular surgery remains controversial, especially in radiotherapy.

The 2003 AJCC TNM staging system, 6th edition reclassified patients with breast cancer and ISLNM from M1 to N3c, showing that breast cancer with ISLNM is considered curable. This decision shows great significance since it changes treatment strategies from palliative to curative, including locoregional and systematic treatments. Systematic therapy is crucial for improving the patients with ISLNM survival.[13],[14] Also, several studies revealed radiotherapy as beneficial to patients with ISLNM. Additionally, it has been reported that radiotherapy increases the median OS of patients with ISLNM from 27.5 to 48 months,[15],[16] and an independent prognostic factor for OS. Radiotherapy is undoubtedly considered an effective locoregional treatment approach; however, there is a lack of agreement on the significance of supraclavicular surgery. Currently, surgery remains an effective treatment of breast cancer and an essential part of the comprehensive treatment of advanced breast cancer. Primarily, the effect of ALN dissection for patients with breast cancer and ALN metastasis is undoubtful. Therefore, it studied whether supraclavicular surgery was significantly correlated with the survival of patients with breast cancer and ISLNM. The surgical dissection scope was mainly the adipose tissue and lymph nodes in regions IV and V of the scapular hyoid muscle clavicle triangle and the scapular hyoid muscle trapezius triangle. The uniqueness of the anatomical location of supraclavicular lymph nodes makes it challenging to perform neck dissection surgeries.[17] Therefore, many studies have shown that supraclavicular surgery is not beneficial to patients with breast cancer and ISLN. Additionally, a recent study by Xiao et al.[18] found that supraclavicular lymph node dissection did not improve RFS and OS in patients with ISLNM after multimodality treatments. Furthermore, Nikpayam et al.[12] observed that for patients with N3 disease, the combination of supraclavicular lymph node and ALN dissections were not superior to the conventional ALN dissections alone. We consistently found that supraclavicular surgery was not an independent prognostic factor for RFS (P = 0.194), DMF (P = 0.272), and OS (P = 0.660). Moreover, a questionnaire survey from Britain showed that 61% of experts recommended neck dissection for patients with ISLNM despite insufficient evidence. However, among these experts, few breast oncologists believed that patients with breast cancer and ISLNM could benefit from neck dissections.[19] However, some other studies showed that supraclavicular surgery is effective. Chang et al.[20] revealed that supraclavicular lymph node dissection attained therapeutic effects similar to radical radiotherapy. Also, Chen et al.[10] reported that locoregional surgery enhanced the survival of patients with ISLNM. Therefore, verifying the significance of supraclavicular lymph node dissection will require several prospective clinical trials.

However, this does not mean surgery is meaningless; our study revealed that not all patients with ISLNM failed to benefit from supraclavicular surgery. This study reclassified patients with ISLNM according to their ER status. The univariate analysis showed that supraclavicular surgery was significantly associated with RFS and DMFS of patients with negative ER. However, the multivariate analysis also showed that supraclavicular surgery was related considerably to RFS and not DMFS. This report is the first on the effects of neck surgeries in patients with ISLNM by focusing on different ER statuses to the best of our knowledge. The ER status, included in the latest AJCC breast cancer staging system. 8th edition,[21] is an essential indicator for evaluating prognosis and formulating treatment protocols for patients with breast cancer and helps patients obtain precise treatment. Many studies have confirmed that breast cancer with ER-negative status often shows poor histological differentiation, a high rate of recurrence and metastasis, insensitivity to endocrine therapy, but offers a better response to chemotherapy.[22],[23],[24] Additionally, the residual tumor cells in the supraclavicular lymph nodes after neoadjuvant chemotherapy are responsible for affecting local control and distant metastasis.[8] Therefore, supraclavicular surgery may improve their local control, reducing recurrence or metastasis for patients with negative ER who have a poor prognosis with no chance of receiving endocrine treatment.

Dellapasqua et al.[5] reported that ISLNM was closely associated with the breast cancer molecular subtype. Our study shows that PR was an independent prognostic factor (P = 0.044). Additionally, axillary nodal status was the essential factor related to adjuvant therapy, which correlated well with survival. Kiricuta et al.[2] reported that 72% of patients who developed ISLNM had positive ALNs during primary tumor diagnosis. Also, Fan et al.[9] said that ALN metastatic status was an independent predictor of metachronous ISLNM (P = 0.009). Similarly, our study found that ALN involvement was identified as a significant cohort predictor of the RFS of the overall (P = 0.002) or negative ER patients (P = 0.015). Therefore, a similar result was among the overall cohort (P < 0.001) and negative ER patients (P = 0.009) for DMFS. Furthermore, Dellapasqua et al.[5] confirmed that the number of positive ALNs was significantly associated with ISLNM. Virani et al.[25] reported that ALN status, the extent of ALN involved, and the number of positive ALNs were independent predictors of ISLNM. Additionally, patients with >10 positive ALNs axilla or involvement at level III or >75% positive axillary nodes of total dissected nodes are correlated with ISLNM.

However, our study was limited to variable treatment strategies encompassing a relatively insufficient number of cases due to low incidences of ISLNM. These limitations made it challenging to conclude on the survival outcomes. Therefore, more prospective clinical studies are required to verify our conclusions.


 > Conclusion Top


Summarily, our study provides unclear evidence that supraclavicular surgery was a prognostic factor in patients' survival with ISLNM. However, it does not mean that surgery is entirely meaningless, and that ER-negative patients with breast cancer and ISLNM may be appropriate candidates for supraclavicular surgery, even in the context of prior radiotherapy. Our study is majorly limited by the small number of cases and its retrospective nature. Therefore, more prospective clinical trials are required to verify the significance of supraclavicular lymph node dissection.

List of abbreviations

  • ISLNM ipsilateral supraclavicular lymph node metastasis
  • DMFS distant metastasis-free survival
  • DFS disease-free survival
  • RFS relapse-free survival
  • OS overall survival
  • CI confidence interval
  • HER2 human epidermal growth factor receptor 2
  • FISH fluorescence in situ hybridization.


Financial support and sponsorship

This study was supported by the National Natural Science Foundation of China (No. 81372843 and No. 81502518), the Major Program of Applied Basic Research Projects of Tianjin (No. 17JCQNJC10400).

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

1.
Recht A, Gray R, Davidson NE, Fowble BL, Solin LJ, Cummings FJ, et al. Locoregional failure 10 years after mastectomy and adjuvant chemotherapy with or without tamoxifen without irradiation: Experience of the Eastern Cooperative Oncology Group. J Clin Oncol 1999;17:1689-700.  Back to cited text no. 1
    
2.
Kiricuta IC, Willner J, Kolbl O, Bohndorf W. The prognostic significance of the supraclavicular lymph node metastases in breast cancer patients. Int J Radiat Oncol Biol Phys 1994;28:387-93.  Back to cited text no. 2
    
3.
Dawood S, Broglio K, Buzdar AU, Hortobagyi GN, Giordano SH. Prognosis of women with metastatic breast cancer by HER2 status and trastuzumab treatment: An institutional-based review. J Clin Oncol 2010;28:92-8.  Back to cited text no. 3
    
4.
Bonotto M, Gerratana L, Poletto E, Driol P, Giangreco M, Russo S, et al. Measures of outcome in metastatic breast cancer: insights from a real-world scenario. Oncologist 2014;19:608-15.  Back to cited text no. 4
    
5.
Dellapasqua S, Bagnardi V, Balduzzi A, Iorfida M, Rotmensz N, Santillo B, et al. Outcomes of patients with breast cancer who present with ipsilateral supraclavicular or internal mammary lymph node metastases. Clin Breast Cancer 2014;14:53-60.  Back to cited text no. 5
    
6.
Brito RA, Valero V, Buzdar AU, Booser DJ, Ames F, Strom E, et al. Long-term results of combined-modality therapy for locally advanced breast cancer with ipsilateral supraclavicular metastases: The University of Texas M.D. Anderson Cancer Center experience. J Clin Oncol 2001;19:628-33.  Back to cited text no. 6
    
7.
Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, et al. Revision of the American Joint Committee on Cancer staging system for breast cancer. J Clin Oncol 2002;20:3628-36.  Back to cited text no. 7
    
8.
Huang EH, Strom EA, Valero V, Fornage B, Perkins GH, Oh JL, et al. Locoregional treatment outcomes for breast cancer patients with ipsilateral supraclavicular metastases at diagnosis. Int J Radiat Oncol Biol Phys 2007;67:490-6.  Back to cited text no. 8
    
9.
Fan Y, Xu B, Liao Y, Yao S, Sun, Y. A retrospective study of metachronous and synchronous ipsilateral supraclavicular lymph node metastases in breast cancer patients. Breast 2010;19:365-9.  Back to cited text no. 9
    
10.
Chen SC, Chang HK, Lin YC, Leung WM, Tsai CS, Cheung YC, et al. Prognosis of breast cancer after supraclavicular lymph node metastasis: Not a distant metastasis. Ann Surg Oncol 2006;13:1457-65.  Back to cited text no. 10
    
11.
Jung J, Kim SS, Ahn SD, Lee SW, Ahn SH, Son BH, et al. Treatment outcome of breast cancer with pathologically proven synchronous ipsilateral supraclavicular lymph node metastases. J Breast Cancer 2015;18:167-72.  Back to cited text no. 11
    
12.
Nikpayam M, Uzan C, Rivera S, Delaloge S, Cahen-Doidy L, Giacchetti S, et al. Impact of radical surgery on outcome in locally advanced breast cancer patients without metastasis at the time of diagnosis. Anticancer Res 2015;35:1729-34.  Back to cited text no. 12
    
13.
Abraham R, Nagy T, Goss PE, Crump M. High dose chemotherapy and autologous blood stem cell support in women with breast carcinoma and isolated supraclavicular lymph node metastases. Cancer 2000;88:790-5.  Back to cited text no. 13
    
14.
Shikama N, Sekiguchi K, Nakamura N. Management of locoregional recurrence of breast cancer. Breast Cancer 2011;18:252-8.  Back to cited text no. 14
    
15.
Pergolizzi S, Settineri N, Russi EG, Maisano R, Adamo V, Santacáterina A, et al. Supraclavicular lymph node metastases (SLM) from breast cancer as only site of distant disease: Has radiotherapy any role? Anticancer Res 1997;17:2303-8.  Back to cited text no. 15
    
16.
van der Sangen MJ, Coebergh JW, Roumen RM, Rutten HJ, Vreugdenhil G, Voogd AC. Detection, treatment, and outcome of isolated supraclavicular recurrence in 42 patients with invasive breast carcinoma. Cancer 2003;98:11-7.  Back to cited text no. 16
    
17.
Aldridge T, Kusanale A, Colbert S, Brennan PA. Supraclavicular metastases from distant primaries: What is the role of the head and neck surgeon? Brit J Oral Max Surg 2013;51:288-93.  Back to cited text no. 17
    
18.
Xiao C, Qi X, Chen A, Zhang W, Zhang P, Cao X. The role of neck dissection in breast cancer patients with synchronous and metachronous ipsilateral supraclavicular lymph node metastasis. Cancer Res 2016;76:12-5.  Back to cited text no. 18
    
19.
Bisase B, Kerawala C. Survey of UK practice for management of breast cancer metastases to the neck. Ann Roy Coll Surg 2012;94:484-9.  Back to cited text no. 19
    
20.
Chang XZ, Yin J, Sun JY, Zhang XH, Cao XC. A retrospective study of different local treatments in breast cancer patients with synchronous ipsilateral supraclavicular lymph node metastasis. J Cancer Res Ther 2013;9:S158-61.  Back to cited text no. 20
    
21.
Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. Ca Cancer J Clin 2017;67:93-9.  Back to cited text no. 21
    
22.
Hammond ME, Hayes DF, Wolff AC, Mangu PB, Temin S. American society of clinical oncology/college of American pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Oncol Pract 2010;6:195-7.  Back to cited text no. 22
    
23.
Bardou VJ, Arpino G, Elledge RM, Osborne CK, Clark GM. Progesterone receptor status significantly improves outcome prediction over estrogen receptor status alone for adjuvant endocrine therapy in two large breast cancer databases. J Clin Oncol 2003;21:1973-9.  Back to cited text no. 23
    
24.
Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME, et al. Etiology of hormone receptor-defined breast cancer: A systematic review of the literature. Cancer Epidemiol Biomarkers Prev 2004;13:1558-68.  Back to cited text no. 24
    
25.
Virani SJ, Patni S, Shah R. A clinical study to assess the pathological involvement of occult supraclavicular lymphnode metastasis in case of locally advanced operable breast carcinoma. Indian J Cancer 2015;52:282-5.  Back to cited text no. 25
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