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10.1245/s10434-006-9070-4
Annals of Surgical Oncology 14:627-632 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Sentinel Node Biopsy and Concomitant Probe-Guided Tumor Excision of Nonpalpable Breast Cancer

Maartje C. van Rijk, MD1, Pieter J. Tanis, MD, PhD2, Omgo E. Nieweg, MD, PhD1, Claudette E. Loo, MD, PhD3, Renato A. Valdés Olmos, MD, PhD4, Hester S. A. Oldenburg, MD, PhD1, Emiel J. Th. Rutgers, MD, PhD, FRCS1, Cornelis A. Hoefnagel, MD, PhD4 and Bin B. R. Kroon, MD, PhD, FRCS1

1 Department of Surgery, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX, Amsterdam, The Netherlands
2 Department of Surgery, Academic Medical Center, Meibergdreef 9, 1105 AZ, Amsterdam, The Netherlands
3 Department of Radiology, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX, Amsterdam, The Netherlands
4 Department of Nuclear Medicine, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX, Amsterdam, The Netherlands

Correspondence: Address correspondence and reprint requests to: Maartje C. van Rijk, MD; E-mail: m.v.rijk{at}nki.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Preliminary data have shown encouraging results of a single intratumoral radiopharmaceutical injection that enables both sentinel node biopsy and probe-guided excision of the primary tumor in patients with nonpalpable breast cancer. The aim of the study was to evaluate this approach in a large group of patients.

Methods: Lymphoscintigraphy was performed in 368 patients with nonpalpable breast cancer after intratumoral injection of 99mTc-nanocolloid (.2 mL, 123 MBq, 3.3 mCi) guided by ultrasound or stereotaxis. The sentinel node was pursued with the aid of vital blue dye (1.0 mL, intratumoral) and a gamma ray detection probe. In case of breast-conserving surgery, the probe was used to guide the excision.

Results: At least one sentinel node could be identified intraoperatively in 357 patients (97%), of whom 69 had involved nodes (19%). Age over 60 years was associated with less frequent nonaxillary lymphatic drainage and absence of internal mammary chain dissemination. Tumor-free margins were obtained in 262 (89%) of the 293 patients who underwent segmental excision. Re-excision of the primary tumor bed was performed in six patients (2%). During a median follow-up of 22 months, one breast recurrence and one axillary recurrence were observed.

Conclusions: Lymphatic mapping and probe-guided tumor excision of nonpalpable breast cancer by intralesional administration of a single dose of 99mTc-nanocolloid and blue dye resulted in 97% identification of the sentinel node and in tumor-free margins in 89% of the patients who underwent breast-conserving surgery. Longer follow-up is needed to substantiate the accuracy and safety of this technique.

Key Words: Sentinel lymph node biopsy • Metastases • Breast neoplasms • Lymphatic metastases • Lymph node dissection • Screening • Breast-conserving therapy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Increasing numbers of patients present with non-palpable breast cancer as a result of screening mammography. Concurrent with the detection of these usually small tumors, the trend is to offer less extensive surgery. This development has continued with the introduction of sentinel lymph node biopsy; lymph node dissection of the axilla is now reserved for patients who have metastatic disease there.

Intratumoral tracer injection and implantation of a radioactive seed have been successfully used to excise nonpalpable breast cancers guided by a gamma ray detection probe.1,2 Subsequently, a technique was developed that uses intratumoral injection of a radiopharmaceutical and blue dye for three purposes: for lymphoscintigraphy, to enable use of the probe and blue dye to find the sentinel node, and to guide the surgeon in the excision of the nonpalpable breast cancer while using the probe.3,4 An initial study of this technique yielded encouraging preliminary results.4

The aim of the current study was to evaluate this latter approach of lymphatic mapping and probe-guided excision (Lympex) in terms of sentinel node identification, lymphatic drainage patterns and dissemination sites, completeness of primary tumor excision, and recurrence rate in a large group of patients with a longer follow-up time.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From December 1999 to September 2005, a total of 368 women with nonpalpable breast cancer underwent lymphatic mapping, and their lymphoscintigraphic and surgical results were recorded prospectively. Patient and tumor characteristics are listed in Table 1Go. Part of this group was subject of an earlier publication.4 The primary breast cancer was still present in all patients. Pathological proof of breast cancer was obtained preoperatively by fine-needle aspiration cytology or core biopsy.


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  		TABLE 1. Patient and tumor characteristics
 
A 2-day protocol was used. On the day before surgery, an intratumoral injection of 99mTc-nanocolloid (Nanocoll; GE-Healthcare, Eindhoven, The Netherlands) was given guided by ultrasound (13 MHz probe, Kretz Voluson 730 expert; GE Medical Systems, Zipf, Austria) or stereotaxis (StereoGuide, Lorad; Trex Medical Corporation, Danbury, IA) in a mean volume of .2 mL and with a mean radioactivity dose of 123 MBq (3.3 mCi). Static imaging was performed at 30 minutes, 2 hours, and 4 hours after injection. A dual-head gamma camera (Vertex; Philips, Eindhoven, The Netherlands) was used, and both anterior and prone lateral images were made. The location of the node was marked on the skin with indelible ink. After the last scintigraphic image, a central venous catheter was loaded with an X-shaped hook wire and inserted at the primary tumor site by means of ultrasound or stereotaxis to enable preoperative blue dye administration. The procedure has been previously described in more detail.4

The next day, 1 mL of patent blue dye (Laboratoire Guerbet, Aulnay-Sous-Bois, France) was injected through the catheter immediately before the operation. The dye and a gamma ray detection probe (Neoprobe; Johnson & Johnson Medical, Hamburg, Germany) were used during the operation to identify the sentinel node. All procedures were performed by one of four experienced surgeons or under their supervision by a resident or fellow. A hot spot on the lymphoscintigraphic images was considered to be a sentinel node if either an afferent lymphatic channel was visualized, the hot spot was the first seen in a sequential pattern, or if the hot spot was the only one in the basin. An afferent blue lymphatic vessel coming directly from the tumor also defined a node as a sentinel node. Sentinel nodes were pursued in all regions indicated by lymphoscintigraphy.

Frozen section analysis of the sentinel node was preoperatively performed in patients who were scheduled to undergo axillary lymph node dissection in case of axillary metastases. A frozen section was made at one level and stained with hematoxylin and eosin.

All sentinel nodes were fixed in formalin, bisected, embedded in paraffin, and cut at a minimum of six levels at 50- to 150-µm intervals. Pathological evaluation included hematoxylin and eosin and immunohistochemical staining (CAM 5.2; Becton Dickinson, San Jose, CA).

After sentinel node biopsy, either breast-conserving therapy (293 patients) or mastectomy (75 patients) was performed. The incision was chosen on the basis of the probe measurements in patients who underwent breast-conserving therapy. As the procedure progressed, the probe was inserted in the wound repeatedly at different angles to assess the location of the tumor. Although the guide wire was still present, the resection was guided by count readings. Depending on the level of remaining activity and the discretion of the surgeon, additional tissue was excised if deemed necessary. The excised lump was submitted entirely and the margins inked with four different colors. The specimen was lamellated in 3-mm slices that were fixed in formalin and embedded in paraffin. Perpendicular slices were made on the central peripheral axis. X-rays of all specimens were made, and extensive sampling of the tumor, the nearest margins, and any other x-ray abnormalities was performed. Sections were stained with hematoxylin and eosin. Forty-one patients with a tumor-positive axillary sentinel node underwent axillary lymph node dissection. Twenty-one received radiotherapy of the axilla as part of a randomized study.5 In all but one patient, axillary node dissection was performed in the presence of an involved lateral intramammary sentinel node. Otherwise, radiotherapy was instituted in case of an involved lymph node in a location outside the axilla. Median follow-up was 22 months (range, 1–65 months).

SPSS statistical software was used for the statistical analysis (SPSS, Inc., Chicago, IL). Differences between age groups with regards to location of sentinel nodes and number of metastases were analyzed by {chi}2 and Fisher’s exact tests for categorical variables and Student’s t-test for continuous variables. P < .05 was considered to be significant (two-sided).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Lymphoscintigraphy showed at least one sentinel node in 339 (92%) of 368 patients. The sentinel node was in the axilla in 303 patients, in the internal mammary chain in 102 patients, and at other locations in 58 patients. Extra-axillary drainage was observed in 140 patients (38%), 36 of whom had drainage exclusively toward these nonaxillary sentinel nodes. At least one sentinel node could be identified intraoperatively in 357 patients (97%). The sentinel nodes in the axilla were retrieved in all but six patients (98%). The axillary node was found exclusively with the aid of blue dye in 20 patients (7%). A sentinel node was identified in 122 (87%) of 140 patients with drainage outside the axilla.

At least one sentinel node was found to be tumor-positive in 69 (19%) of the 357 patients. Of these 69 patients, 59 had metastases in the axilla. Metastases outside the axilla were located in the internal mammary chain in 11 patients, in the infraclavicular bed in 2, and within the breast in 3. Ten (14%) of the 69 patients had metastases located exclusively outside the axilla. All patients with metastases located outside the axilla received additional radiotherapy to that area, and in three patients, additional systemic treatment was instituted that otherwise would not have been provided.

Along the way, we got the impression that the biology of the disease in older patients was different from that in the younger population. The two groups were compared with a cutoff age of 60 years and tested for a number of parameters (Table 2Go). There were no differences in terms of tumor size and malignancy grade. Sentinel nodes were more often visualized on the scintigrams in younger patients (98% vs. 88%, P < .001). The frequency of axillary drainage was identical in both age groups, but drainage toward the internal mammary chain and elsewhere was more frequently present in the younger patients. The slightly higher percentage of axillary metastases in patients younger than 60 did not reach statistical significance, but there was a striking difference in the nonaxillary metastasis rate between the two groups. No internal mammary node metastases were found in the older patients, and metastases elsewhere outside the axilla were rare.


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  		TABLE 2. Tumor characteristics, lymphatic drainage pathways, and location of metastases by age groupa
 
The primary tumor site could be located with the probe in all patients. Probe-guided excision was believed to be expeditious and technically easy. In five patients, the guide wire was located in another quadrant than the radioactive tracer, and a large segmental excision including both sites was performed with both guidance tools. Tumor-free margins were obtained in 262 (89%) of the 293 patients who underwent segmental excision. Invasive carcinoma was incompletely excised in 14 patients (5%) and accompanying carcinoma in situ in 17 (6%). Re-excision was performed in three patients with incompletely excised invasive carcinoma and in another three with incompletely excised carcinoma in situ. The remaining 25 patients had only focally positive margins and underwent radiotherapy (50 Gy to the breast and a boost of 16 Gy to the tumor area).

Of the entire group of 368 patients, six underwent re-excision of the primary tumor, and eight received axillary lymph node dissection at a later stage because their frozen sections were falsely negative for disease.

One patient developed a recurrence in the breast after 24 months. The primary tumor was a .8-cm invasive ductal carcinoma and had been radically excised. Radiotherapy to the breast was instituted. Salvage mastectomy was performed, and the patient is free of disease 20 months later. A second patient developed axillary and supraclavicular metastases 23 months after a tumor-negative sentinel lymph node biopsy. Chemotherapy and subsequent radiotherapy was instituted. Two months after the radiotherapy, skin metastases were evident, and bone scintigraphy showed metastases in the skull and right femur. She is alive with disease 10 months later.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study shows that our Lympex technique using a single intratumoral 99mTc-nannocoloid injection is successful and safe. A sentinel node could be identified in 97% of patients, and tumor-free margins were achieved in 89% of the patients by probe-guided tumor excision. One patient (.27%) developed an axillary recurrence. This last number is comparable to the .38% recurrence rate in a review of 10 large observational studies concerning 2664 patients who did not undergo axillary lymph node dissection after collecting a tumor-free sentinel node.6 One should bear in mind that the recurrence numbers might go up because follow-up is relatively short.

Sentinel nodes can also be located outside the axilla, and recurrences, although rare, have been reported in the internal mammary chain, within the infra- and supraclavicular bed, and in the interpectoral space.7,8 In this study, extra-axillary drainage was observed in 140 patients (38%). This high incidence confirms an earlier observation that extra-axillary nodes are visualized more often when the primary tumor is not palpable compared with palpable tumors.3 Other factors that influence drainage routes are breast size, location of the tumor within the breast, and previous surgery of the breast or axilla.8–10 The present results indicate that age seems to be a factor too (Table 2Go). Internal mammary chain drainage is more often seen in patients younger than 60 years. Metastases occur infrequently (4%) in older women who do have sentinel nodes outside the axilla. With advancing age, the importance of the axilla as main lymphatic pathway and dissemination route of the breast increases.

Of the patients younger than 60, a total of 19% with extra-axillary drainage had metastases in such nodes. The clinical relevance of such metastases is subject of debate.10–16 Some investigators advocate ignoring extra-axillary sentinel nodes17 because their removal adds "nothing but time, cost and risk to the procedure."18 However, Veronesi et al.19 demonstrated in 1985 that the tumor status of nodes in the internal mammary chain has an impact on survival that equals the impact of nodes in the axilla. It has also been shown that 14% of patients with breast cancer have tumor-positive interpectoral nodes when all these nodes are routinely excised.13 Shen et al.20 indicated that patients with metastases in intramammary nodes have a marked increase in disease-related morbidity and a reduced survival rate. Because nodes in the axilla, internal mammary chain, and breast seem to be of clinical relevance, we assume that this is true for all sentinel nodes regardless of their location, and we believe that they should be pursued in patients younger than 60. Our present results suggest that internal mammary nodes can be left alone in older patients.

The feasibility of localizing the primary tumor with the aid of 99mTc-nannocolloid was evaluated in this study. This approach has several advantages over the widely used guide-wire method.21 The tumor is more often completely excised, and rein-terventions are less often necessary when radio-guided excision is performed.22 Only 2% of the patients in the current series needed re-excision. Furthermore, a reduced tissue volume is excised23 and the lesion is better centered within the specimen,1 which facilitates breast-conserving surgery and is likely to improve cosmetic results.24,25 It has also been shown that radioisotope lesion localization is easier than the guide wire method for the radiologist and for the surgeon.26 For the surgeon, the problem with the guide wire is that its tip can neither be seen nor felt. With the probe, one can obtain readings from different angles and thus obtain a three-dimensional impression of where the tumor is located. An advantage of the catheter being inserted in the lesion is that it enables blue dye injection at the lesion site. Some sentinel nodes are not radioactive but only blue. The surgeon needs to view the images and make sure that the tracers are injected in the center of the lesion.

A future refinement of the technique may be image-guided blue dye administration immediately before the operation. This would obviate the need to insert a canula in the radiology suite. One suggested drawback of the use of 99mTc-nanocolloid for sentinel node localization and radioguided occult lesion localization is the radiation exposure for the surgeon.27 However, it has been shown that the absorbed radiation dose to the surgeons’ hands would be 2% of the recommended limit if a surgeon were to perform 100 procedures per year.27

In five patients, the guide wire was found to be in another location than the radiopharmaceutical. Two potential reasons were identified for these discrepancies. In The Netherlands Cancer Institute, the sentinel node procedure is performed in a 2-day protocol for logistic reasons and to enable reinjection of the radioactive tracer when no sentinel node is visualized. It is possible that the guide wire had dislocated during the night. In one patient, the guide wire was inserted wrongly, but this was not reported to the surgeon, and more tissue than necessary was removed.

Probe-guided tumor excision after the insertion of a radioactive titanium seed within the center of a nonpalpable lesion is another new development.2 Fewer patients had involved margins when this technique was compared with guide-wire localization (26 % vs. 57%, P = .02).2 This approach does not enable sentinel node biopsy because the radioactivity does not travel to the sentinel node. Our 99mTc-nanocolloid injection can be used for both the localization of the lesion and the sentinel node.

In conclusion, Lympex of nonpalpable breast cancer using intralesional administration of a single dose of 99mTc-nanocolloid and blue dye results in 97% identification of the sentinel node and in tumor-free margins in 89% of the patients who undergo breast-conserving surgery. Age over 60 years was associated with a decrease in overall lymphatic drainage and absence of internal mammary chain dissemination. Longer follow-up is needed to substantiate the accuracy and safety of this technique.

Received for publication June 27, 2006. Accepted for publication June 28, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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