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10.1245/ASO.2006.02.022
Annals of Surgical Oncology 13:321-326 (2006)
© 2006 Society of Surgical Oncology
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Original Article

The Clinical Value of Parasternal Sentinel Node Biopsy in Breast Cancer

Marjut Hannele Kristiina Leidenius, MD, PhD1, Leena Anneli Krogerus, MD, PhD2, Terttu Sinikka Toivonen, MD2, Esa Antero Leppänen, MD, PhD3 and Karl Albert Johan von Smitten, MD, PhD1

1 Breast Surgery Unit, Helsinki University Hospital, P.O. Box 140, FIN-00029 HUS, Helsinki, Finland
2 Department of Pathology, Helsinki University Hospital, Haartmaninkatu 3, P.O. Box 400, FIN-00029 HUS, Helsinki, Finland
3 Department of Nuclear Medicine, Helsinki University Hospital, Haartmaninkatu 4, P.O. Box 340, FIN-00029 HUS, 00210 Helsinki, Finland

Correspondence: Address correspondence and reprint requests to: Marjut Hannele Kristiina Leidenius, MD, PhD; E-mail: marjut.leidenius{at}hus.fi.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Lymphoscintigraphy (LS) with sentinel node (SN) biopsy is proposed to provide a feasible method to complete lymphatic staging in breast cancer. The aim of this study was to evaluate the clinical value of parasternal SN biopsy.

Methods: A total of 984 consecutive patients with clinical stage T1/2N0 invasive breast cancer who underwent LS and SN biopsy were included in the study. A prospectively collected database was used. An intratumoral injection of 50 to 145 MBq of 99mTc-labeled human albumin colloid (Nanocoll) was used for preoperative LS.

Results: LS showed the axillary SN in 844 (86%) cases and the parasternal SN in 138 (14%) cases. The median number of visualized parasternal SN was 2 (range, 1–6). Visualization of the parasternal SN was more common in patients with mediocentral tumors (81 of 399; 20%) and in patients with lateral tumors (56 of 585; 10%; P < .0001). Parasternal SNs were visualized more often, in 100 (17%) of 584 patients without axillary metastases compared with 38 (10%) of 400 patients with metastatic axillary nodes (P = .0006). Parasternal SNs were harvested successfully in 121 (88%) patients with visualization of those nodes. Parasternal SN metastases were detected in 18 patients, with a median of 1 metastasis (range, 1–4 metastases). Eight of these 18 patients were axillary node negative.

Conclusions: Parasternal SN biopsy results in upstaging in 2% of all breast cancer patients who undergo SN biopsy. The clinical value of the procedure seems insignificant, although it may influence the adjuvant treatment regimen in some patients.

Key Words: Breast cancer • Internal mammary lymph nodes • Lymph node metastases • Lymphoscintigraphy • Nodal staging • Sentinel node biopsy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The status of the axillary and internal mammary lymph nodes is the most significant prognostic factor for survival in breast cancer.1 Ten-year survival of 80% has been reported when both the axillary and the internal mammary nodes are uninvolved, compared with a 30% survival of patients with metastases in both nodal basins.1 An intermediate survival rate of approximately 55% was found when only one of the nodal stations was affected.1 The reappraisal of internal mammary node metastases as a prognostic factor and the results of recent publications of trials evaluating the value of postmastectomy radiotherapy, including internal mammary field radiation, have aroused discussion of adopting routine elective irradiation of the basin despite potentially serious cardiac morbidity.2–4

Lymphoscintigraphy (LS) with biopsy of the sentinel nodes (SN) in and outside the axilla has been proposed to provide complete lymphatic staging, thus enabling more accurate targeting of regional and systemic treatment in breast cancer.5–8 Although the clinical value of parasternal SN biopsy has been regarded as limited in many centers,9–12 it provides information about regional dissemination of the disease, which is appreciated by the patients.13 The aim of this study was to evaluate the clinical value of parasternal SN biopsy in breast cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From March 2001 to January 2004, 984 consecutive patients with clinical stage T1/2N0 invasive breast cancer underwent LS and SN biopsy in our unit. A prospectively collected database was used in the study. The project plan was approved by the Ethical Committee of Helsinki University Hospitals. Written informed consent was obtained from each patient. The patient and tumor characteristics are listed in Table 1Go.


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  		TABLE 1. Patient and tumor characteristics of 984 patients with invasive breast cancer and sentinel node biopsy
 
LS was performed the day before surgery a median of 4 hours (range, .5–20 hours) after an injection of 50 to 145 MBq of 99mTc-labeled human albumin colloid (Nanocoll; Nycomed Amersham Sorin s.r.l., Saluggia, Italy), with particle sizes less than 80 nm in a volume of .2 mL. A single intratumoral tracer injection was applied in most (941 of 984) cases. The radioisotope injection was performed in palpation control in 655 (67%) patients with clearly palpable tumors. The radioisotope injection was guided ultrasonographically (in 253 cases; 26%) or stereotactically (in 33 cases; 3%) when the tumor was not clearly palpable. The tracer was injected in 2 sites around the biopsy cavity in 40 (4%) patients with a previous excisional biopsy. Three patients received a subareolar injection.

Anterior and lateral planar views were obtained by using a gamma camera (Toshiba GCA-901A [Toshiba Corporation, Tokyo, Japan] in 478 patients, Siemens E.CAM Dual-Head Variable Angle System [Siemens, Erlangen, Germany] in 104 patients, and ADAC Forte Plus Epic Dualhead [Philips, Milpitas, CA] in 402 patients) with a 256 x 256 matrix and up to 5 minutes of imaging time per frame. The locations of the SNs were marked with a permanent pen on the skin.

The SNs were harvested by using a gamma detector and searching for the blue-stained lymphatic vessels and nodes. SNs outside the axilla were searched when clearly visible in the LS.14 Axillary clearance was performed in patients with tumor-positive SNs and in those with an unsuccessful SN biopsy.

Histological Analysis
The SNs were sent to the pathology laboratory as separate samples. The fresh specimens were cleaned from all extracapsular fat tissue, measured, sliced into 1- to 1.5-mm-thick sections perpendicular to their long axis, and arranged on prefrozen Tissue-Tek OCT compound (Sakura Filnetek Europe, Zoeterwonde, The Netherlands). Touch preparations from the surface and frozen sections from two levels were made from these slices; these were then stained with toluidine blue and viewed.

In the last 327 cases, rapid intraoperative immunohistochemistry was available and applied. From January 21, 2003, Cam 5.2 was used. From July 1, 2003, a quicker method with Cyto-nel Ultrapid IHC (Immuno Diagnostics Oy, Hämeenlinna, Finland) was introduced. Malignancy was reported to the operating room as soon as it was detected.

The remaining tissue was fixed in formalin and embedded in paraffin. Two sections were stained with hematoxylin and eosin (H&E). When a metastasis ≥2 mm was found in the frozen-section procedure, only H&E sections were made from paraffin-embedded tissue. If no metastatic tissue was detected or if isolated tumor cells or a micrometastasis only was found, a Cam 5.2 immunostain (Becton Dickinson Immunocytometry Systems, San Jose, CA) was performed on paraffin-embedded tissue in addition to the regular H&E-sections. When frozen-section diagnosis was not required (parasternal SN), the nodes were fixed directly into phosphate-buffered 10% formalin. After fixation, the nodes were cleaned from fat, cleaved, and embedded wholly in paraffin. H&E sections were made from two levels of each lymph node, and cytokeratin immunostaining was performed from one level. Metastases of ≤2 mm were considered as micrometastases and were considered as isolated tumor cells when they were ≤.2 mm.15 Lymph nodes in the axillary clearance specimens were embedded wholly in paraffin. H&E sections were prepared from two levels 200 µm apart.

Statistical Methods
Fisher’s exact and {chi}2 tests were used to compare the proportional data. The means and medians were compared by using the Mann-Whitney U-test. Two-tailed P values <.05 were considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Axillary SNs were visualized in 844 (86%) of 984 and successfully harvested in 936 (95%) of 984 patients. The median number of harvested axillary SN was 2 (range, 1–14). Axillary metastases were detected in 400 (41%) of 984 patients. The SNs were the only tumor-positive ones in 253 (64%) of 395 patients with axillary SN metastases. Four or more metastatic axillary nodes were detected in 72 patients.

Parasternal SNs were visualized in the LS in 138 (14%) of 984 patients. Lymphatic drainage solely to the parasternal SN occurred in 17 (2%) cases. The median number of visualized parasternal SNs was 2 (range, 1–6). SN were visualized in a single intercostal space in 64 (46%), in 2 intercostal spaces in 40 (29%), in 3 spaces in 22 (16%), and in 4 spaces in 4 patients. The location of the visualized parasternal SN was not registered in eight patients. The most common location for the parasternal SN was the second intercostal space, in 92 (67%) patients (Table 2Go).


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  		TABLE 2. Location of the visualized and metastatic parasternal sentinel nodes
 
Parasternal SNs were visualized more often with a Toshiba gamma camera (79 [17%] of 478 patients) compared with the other gamma cameras (8 [8%] of 104 patients with the Siemens camera and 51 [13%] of 402 patients with the ADAC camera; P < .05). Other technical factors, including the dose of the tracer, the interval between the injection and imaging, or whether the injection was performed in palpation or ultrasonographical control, had no influence on the visualization of parasternal SNs (Table 3Go).


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  		TABLE 3. The influence of technical aspects on visualization of parasternal sentinel nodes
 
Parasternal SNs were visualized in 100 (13%) of 744 patients with palpable tumors and in 38 (16%) of 240 patients with nonpalpable tumors (P = not significant). LS showed parasternal SNs in 81 (20%) of 399 patients with mediocentral tumors and in 56 (10%) of 585 patients with lateral tumors (P < .0001; Table 4Go).


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  		TABLE 4. Visualization rate of parasternal sentinel nodes in palpable and nonpalpable tumors and the location of the tumor in the breast
 
Parasternal SNs were observed in 112 (15%) of 721 patients with histological stage T1 tumors and in 26 (10%) of 263 patients with larger tumors (P = not significant). However, the median histological tumor size was smaller (13 mm; range, 2–44 mm) in patients with visualized parasternal SNs than in patients with nonvisualization of the parasternal SNs (15 mm; range, 1–80 mm; P < .005). The histological tumor type or grade did not influence the visualization of parasternal SNs.

Parasternal SNs were visualized more often in patients without axillary metastases (100 of 584; 17%) than in patients with metastatic axillary nodes (38 of 400; 10%; P = .0006). The mean number of metastatic nodes was larger (1.2; range, 0–33) in patients without parasternal SNs compared with the mean of .6 (range, 0–17) tumor-positive nodes in patients with parasternal SNs (P < .005). Only 4 (6%) of the 72 patients with ≥4 metastatic axillary nodes had parasternal SNs in the LS. This observation was emphasized among patients with mediocentral tumors, with a visualization rate of 61 (25%) of 243 in axillary node–negative patients and 21 (13%) of 156 in patients with axillary metastases (P = .005). The same tendency was also observed in patients with lateral tumors, with a visualization rate of 39 (11%) of 341 in axillary node–negative patients and 17 (7%) of 244 in node-positive patients (P = .07).

Parasternal SNs were harvested successfully in 121 (88%) of 138 patients with visualization of those nodes. The median number of harvested parasternal SNs was 2 (range, 1–6) in these patients.

Metastases in the parasternal SN were detected in 18 patients, representing 15% of patients with harvested parasternal SNs and 1.8% of the entire study population. The median number of metastatic parasternal nodes was 1 (range, 1–4). Two patients had micrometastases or isolated tumor cells only in their parasternal SN. Thirteen patients had metastases just in one intercostal space, two had metastatic nodes in two intercostal spaces, and three had metastatic nodes in three spaces (Table 2Go). The most common location for the parasternal SN metastases was the second intercostal space, in nine patients (Table 2Go). Seven patients with parasternal metastases had upper medial, three had lower medial, four had upper lateral, and three had lower lateral tumors, whereas one patient had a centrally located tumor.

Eight of the 18 patients with parasternal metastases were axillary node negative. Five of them had T1c tumors, and three had small T2 tumors. The remaining 10 patients with parasternal SN metastases also had axillary metastases. Three of them had four or more metastatic axillary nodes. The upstaging effect 15 provided by parasternal SN biopsy is presented in Table 5Go.


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  		TABLE 5. Stage migration provided by parasternal sentinel node biopsy (SNB) among 984 patients with invasive breast cancer
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Preoperative LS has been reported to visualize parasternal SNs in 0% to 45% of patients, highly depending on the lymphatic mapping technique. 5,8,11,12,16–19 Lymphatic drainage to the internal mammary basin may occur from all breast segments, but it seems to be more common in connection with medially located tumors, according to this study and previous studies.5,7 It may also be more common when the tumor is located deep in the breast, closer to the deep prepectoral lymphatics.5,16

The depth of the tracer injection influences the visualization of parasternal SNs in LS.7,17,18 The visualization rate has been highest when the tracer has been injected underneath the tumor.7,17,18 Not only the visualization rate, but also the number of visualized parasternal SNs, increases when the tracer is injected underneath the tumor.18 Also, the characteristics of the patients, such as age and body mass index16 and the size of the breast,18 influence the visualization rate of parasternal SNs.

Metastases in the internal mammary chain have been found in approximately 20% of breast cancer patients, in more than 30% of the patients when the axillary nodes are involved.1,20–22 Even these high figures may be an underestimation, because the number of examined nodes has been relatively small: the median number has varied between 1.9 and 4.1.22 However, the high prevalence of internal mammary lymph node metastases in the reports from the late 1970s and early 1980s1,21,22 probably does not represent the situation in patients undergoing SN biopsy with a high proportion of T1 and axillary node–negative cases.

According to this study and previous studies,5,23 parasternal SN metastases have been detected in 15% to 17% of patients with a successful harvesting of those nodes, representing 2% to 3% of the entire patient population undergoing SN biopsy. Patients with parasternal metastases and a node-negative axilla represent approximately 1% of all breast cancer patients with SN biopsy.

The sensitivity of SN biopsy in the axilla has been assessed in several audit-phase studies comparing the status of the SN with the status of the axillary clearance specimen. The false-negative rate has usually been 5% of axillary node–positive cases or even less.24 The sensitivity of parasternal SN biopsy is unknown. The frequency of parasternal metastases observed in SN studies may be an underestimation because of failure in visualization or harvesting of the parasternal SN. A higher sensitivity of the procedure may be achieved by adjusting the lymphatic mapping technique, with a result of a higher visualization rate of parasternal SNs.7,17,18 However, after a certain cutoff point, the more frequent visualization of parasternal SNs will just increase the number of biopsies without a significant improvement in the sensitivity. This cutoff point is unknown.

The survival benefit of internal mammary radiotherapy is a subject for ongoing studies. Parasternal SN biopsy has been proposed as beneficial when it targets internal mammary radiotherapy.5–8 This is an attractive option, especially in patients with axillary metastases and, thereby, a high probability of parasternal metastases. However, our visualization rate of parasternal SNs was disappointingly low in this patient group. There may have been a failure in the LS; the tracer may not have entered the deep lymphatics after our intratumoral injection, especially in patients with larger tumors. The failure in the LS may also be due to overt metastases, a phenomenon well known in the axilla.25 This possibility cannot be excluded, especially in patients with large tumors and axillary metastases. It is noteworthy that one of our patients without axillary metastases or visualization of parasternal SNs in her LS presented with parasternal metastases in the computed tomographic scan just 1 year after surgery.

The axillary SNs are the only tumor-positive nodes in more than half of patients with axillary SN metastases. If this is true also in the internal mammary basin, then more than half of the patients with parasternal SN metastases do not have residual disease in the basin after SN biopsy. If no metastases are left behind in the basin, then regional radiotherapy is not beneficial. Parasternal SN biopsy is not of much help when internal mammary radiotherapy is targeted, because the sensitivity of the procedure and the status of non-SNs are unknown.

As regards systemic adjuvant treatment, parasternal SN metastases are seldom the only indication for chemotherapy.5,10–12,23 Therefore, the patients who probably benefit most from parasternal SN biopsy are those with small, axillary node–negative tumors.10 However, parasternal SN biopsy may also result in a change in the chemotherapy regimen to a more aggressive one in some patients with axillary metastases.

Harvesting SNs in the internal mammary chain is more demanding compared with the axilla. The success rate has been <90% even in experienced hands.5,6 The failure in this study was most often caused by an insufficient uptake of the tracer and/or difficult anatomical circumstances, as previously reported. 5,23 Harvesting was not even attempted in patients with a very faint tracer accumulation in the LS. Retrieval of these nodes does not seem to carry considerable risks for the patients, but extra skin incisions are often necessary.23 Earlier,23 a minimal perforation of the parietal pleura occurred in 10% of our patients, but this is nowadays uncommon in our unit. These patients have recovered uneventfully without pleural drainage. Furthermore, parasternal SN biopsy does not lengthen the hospital stay. Bleeding from internal thoracic vessels has been reported 5 but did not occur in this study.

In conclusion, parasternal SN biopsy results in upstaging in 2% of breast cancer patients who undergo SN biopsy. It may change the adjuvant treatment regimen in some of these patients. Whether it also improves survival remains unknown.


   ACKNOWLEDGMENTS
 
Supported by a grant from the Helsinki University Hospital Research Fund.

Received for publication February 22, 2005. Accepted for publication September 13, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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