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10.1245/ASO.2003.01.022
Annals of Surgical Oncology 10:942-947 (2003)
© 2003 Society of Surgical Oncology
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Right arrow Sentinel lymph node

ORIGINAL ARTICLES

Subareolar Injection May Be More Accurate Than Other Techniques for Sentinel Lymph Node Biopsy in Breast Cancer

Giovanni D’Eredita’, MD, Filippo Ferrarese, MD, Vincenzo Cecere, MD, Sara Tiziana Massa, MD, Francesco de Carne, MD and Gennaro Fabiano, MD

From the Department of General and Special Surgery, University of Bari, Bari, Italy.

Correspondence: Address correspondence and reprint requests to: Giovanni D’Eredita’, MD, Via S. Hahnemann, 2, 70126 Bari, Italy; Fax: 39-80-559-2904; E-mail: gderedita{at}chirges.uniba.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The aims of this study were to compare peritumoral injection of 99mTc-labeled albumin and subdermal injection of blue dye with subareolar (SA) injection of blue dye alone in terms of success of the sentinel lymph node identification rate, false negative (FN) rate, overall accuracy, and sensitivity of the two procedures.

Methods: From January 1999 to October 2002, 155 patients with localized breast cancer were treated. Patients were subdivided into two groups. In patients in group 1 (n = 115; January 1999 to December 2001), lymphoscintigraphy together with injection of vital dye was performed. In patients in group 2 (n = 40; January 2002 to October 2002), SA injection of blue dye alone was performed.

Results: In patients in group 1, the overall successful identification rate was 94.8%. The success rate of identifying a sentinel lymph node by a combination of the two techniques was 95%. With blue dye alone, the successful identification rate was 94.6% in patients in group 1 (subdermal) and 97.5% in group 2 (SA). The FN rate was 9% in group 1 and 0% in group 2. The overall accuracy of lymphatic mapping was 97% in group 1 and 100% in group 2. Sensitivity was 91% in group 1 and 100% in group 2.

Conclusions: This study of dye-only injection into the SA plexus demonstrates a high sentinel node identification rate, absent FN rate, and rapid learning curve. On the basis of these findings, we propose that injections into the SA lymphatic plexus are the optimal way to perform dye-only lymphatic mapping of the breast.

Key Words: Sentinel lymph node biopsy • Lymphatic mapping • Subareolar injection • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The status of axillary lymph nodes in patients with breast cancer is an important prognostic factor and provides essential information used to decide the administration of adjuvant therapies. Nodal involvement is determined by a level I, II, and III axillary lymph node dissection (ALND), although until recently, evaluation of level I and II axillary lymph nodes was considered the standard surgical procedure for staging axillary lymph nodes.1 The screening of breast cancer has permitted the treatment of more subclinical cancers. Most ALND proved negative because 75% of breast cancers of small dimensions (<2 cm) were unaffected by axillary metastases.2 Moreover, ALND is associated with early and long-term complications, such as arm numbness and pain, infections, and lymphedema. Sentinel lymph node (SLN) biopsy was suggested in place of the routine ALND in patients with clinically normal axillary lymph nodes. The techniques of axillary mapping are numerous and differ according to the materials used: blue dye and/or 99mTc-labeled sulfur colloid or 99mTc-labeled albumin, volume of agent, timing of injection, and, moreover, site of injection. The consequence of the different techniques was conflicting results. The dye or the tracer was injected into the peritumoral or intraparenchymal tissue,3–8 subdermally or intradermally.9,10

With the combination of the two techniques (blue dye and radioisotope) injected into peritumoral or intraparenchymal tissue, SLN identification rates of 92% to 99% have been reported, with 0% to 15% false-negative (FN) rates.4,9,11 With subdermal or intradermal injection of agents, SLN identification rates were 98% to 100%, and FN rates were 0% to 9%.5,9,10,12 These techniques have allowed for acceptable results with regard to the identification rates of SLN, but not with FN rates.

Successful SLN biopsy depends primarily on accurate identification of the exact metastatic route that will be, or has been, used by disseminating tumor cells.13 The lymphatic drainage of the breast, which is poorly understood, was first described by Sappey,14 who showed that the lymphatics of the breast follow the ductal system of the breast and flow into a subareolar (SA) plexus. From this plexus, several main lymphatic trunks drain to a small number of axillary SLNs. This work was later confirmed by Rouviere15 and Grant et al.16 In the 1950s, Turner-Warwick17 refuted the earlier concepts of Sappey and showed that lymph flows from superficial to deep and then toward the regional lymph nodes. The findings of these two studies are both consistent with our knowledge of the embryological development of the breast. From the ectodermal primitive milk streak, which later becomes the areolar complex, the lymphatics of the breast elongate as the lactiferous duct system develops and maintain their connection to the SA lymphatic plexus, which is connected with deep and superficial intramammary lymphatics that terminate in regional lymph nodes.18 This communication is the premise behind injection of the tracer material into the SA plexus to search for the SLN. Only a few authors have investigated the SA injection. We give credit to Kern,19 who for the first time in 1999 published his research on 40 patients in whom the vital dye was injected into the SA area followed by complete ALND. Klimberg20 published in the same year her research on 68 patients in whom the tracer was injected into the SA area and 5 mL of vital dye was injected around the tumor, but without ALND. Smith et al.21 later further tested the hypothesis that SA injection of 99mTc is as accurate as peritumoral injection in localizing the SLN determined by complete ALND. The goal of this study was to compare peritumoral injection of 99mTc-labeled albumin and subdermal injection of blue dye with SA injection of blue dye alone in terms of success of SLN identification, FN rate, overall accuracy, and sensitivity of two procedures. We performed a complete ALND in all patients.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From January 1999 to October 2002, 155 patients with localized breast cancer were evaluated for enrollment in our study at the Institute of General Surgery, University of Bari. A histological or cytological diagnosis of invasive breast cancer was required. We excluded patients with palpable axillary nodes, ductal in situ histology, previous radiotherapy to the breast, or prior axillary surgery and women who were pregnant. Informed consent was required from all patients. In our initial study, the SLN biopsy was performed through lymphoscintigraphy with peritumoral 99mTc injection and subdermal injection of vital dye, followed in all cases by complete ALND. This procedure was modified during the course of the study: after the first 50 cases, in patients with negative SLNs (proved also with the immunohistochemical method), with their informed consent, ALND was not performed. Since January 2002, we have modified the SLN identification technique by using an SA injection of vital dye followed by complete ALND in all patients. There were 115 patients in the first phase of the study (group 1) and 40 in the second phase (group 2).

Technique
In patients in group 1 (n = 115; January 1999 to December 2001) with palpable tumor, lymphoscintigraphy together with injection of vital dye was performed to identify the SLN. Patients with nonpalpable lesions underwent injection by ultrasound guidance. The day before surgery, 8 to 12 MBq of 99mTc-labeled human albumin colloid particles (80–200 nm; Nanocol; Nycomed-Amersham, Sorin, Italy) in .4 mL of saline was administered in four peritumoral injections immediately around the breast lesion. Planar scans of the involved breast and axillary area, in anterior and lateral projections, were acquired 15 to 30 minutes and 3 hours after tracer injection. After scanning, the skin over the first node to take up tracer (defined as the SLN) was marked. A gamma-detecting probe (Neoprobe, Dublin, OH) was applied to the skin above the SLN to confirm the hot spot. Signals picked up by the probe were transduced into digital readout and acoustic signals. The intensity and frequency of the acoustic signals were directly proportional to the level of radioactivity detected. Approximately 10 to 20 minutes before axillary incision, 4 mL of methylene blue dye was administered subdermally, above the breast mass, in four subdermal injections. A small skin incision was made, blunt dissection was performed to identify a blue-impregnated lymphatic channel, and the lymphatic chain was followed until the first node (the SLN) was identified. The gamma probe guided the dissection to a blue-stained afferent lymphatic channel or the blue-stained node emitting the highest activity, and that was excised and tagged as the SLN. Sometimes two or more nodes were picked up by the probe. All axillary nodes with counts >=10% of the ex vivo counts of the most radioactive lymph node were removed and designated as SLNs. After the specimen was rechecked, the wound was re-examined after SLN removal to ensure that all radiolabeled lymph nodes were removed. A complete axillary dissection was performed immediately in the first 50 patients; in the following patients, delayed completion axillary dissection was performed when metastatic cells were discovered on permanent pathologic sections after staining with hematoxylin and eosin or with a cytokeratin cocktail, as described below. Complete lymphadenectomy was avoided only in seven patients with negative SLNs confirmed by immunohistochemical analysis because of their refusal after informed consent. In patients in group 2 (n = 40; January 2002 to October 2002), SA injection of blue dye was performed. According to Kern,19 regardless of tumor location or site of previous biopsies, the injection of blue dye (4 mL of methylene blue dye) is placed into the upper, outer edge of the areola (right breast, 10 o’clock; left breast, 2 o’clock) and directed medially toward the nipple, approximately 10 to 20 minutes before axillary incision, in a single injection site, followed by complete axillary dissection.

Pathologic Evaluation
In all patients, SLNs were sectioned along the long axis into two sections and were then submitted for routine processing. Each tissue block was sectioned serially (successive 5-µm sections) and stained with hematoxylin and eosin. When metastatic carcinoma was not apparent on examination of the hematoxylin and eosin–stained slides, immunohistochemical analysis was performed by using a cytokeratin cocktail of three monoclonal antibodies that recognize a wide range of high- and low-molecular-weight keratin peptides (AE1/AE3, 1:50 [Dako, Carpinteria, CA]; CAM 5.2, 1:50 [Becton Dickinson, Franklin Lakes, NJ]; and MNF 116, 1:100 [Dako]). Immunohistochemical analysis was performed with the avidin-biotin-peroxidase complex method.22 Immunostaining was automated with the ChemMate HRP/3 and the 3'-diaminobenzidine detection kit K5001 (Dako) on a TecMate 1000 (Dako). Brief counterstaining in Mayer’s hematoxylin followed immunostaining.

Statistical Evaluation
The data were analyzed with SPSS for Windows (release 10; SPSS Inc., Chicago, IL). Comparison of group means was determined by t-testing, and comparison of data within 2 x 2 tables was determined by a Pearson {chi}2 test. P values <.05 were considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The two groups of patients were similar in age, previous biopsy type, tumor size, histology, grading, breast quadrant, type of surgery, and lymph node status (Tables 1 and 2Go). In patients in group 1, the overall successful identification was 94.8% (109 of 115 patients). The success rate of identifying a SLN by a combination of the two techniques (preoperative lymphoscintigraphy and blue dye) was 95% (38 of 40). With blue dye alone, the successful identification rate was 94.6% (71 of 75) in patients in group 1 (subdermal injection) and 97.5% (39 of 40) in group 2 (SA injection; P = .81). The mean number of SLNs identified was 1.37 ± .74 in group 1 (range, 1–5) and 1.86 ± 1.57 in group 2 (range, 1–8; t-testing; P = .01). The mean number of lymph nodes examined was 20.14 ± 6.53 in group 1 (range, 8–39) and 20.03 ± 7.28 in group 2 (range, 7–31; t-testing; P = .92). We identified 33 positive axillary basins in patients in group 1 and 12 in patients in group 2 after complete ALND. SLNs were the only positives nodes in 9 (27.2%) of 33 patients in group 1 and in 5 (41.6%) of 12 patients in group 2. Three patients in group 1 and no patients in group 2 had a negative SLN and positive axillary nodes (FN). The FN rate was 9% in group 1 and 0% in group 2. The overall accuracy of lymphatic mapping was 97% (99 of 102 patients) with an SLN identified and ALND performed in group 1 and was 100% (39 of 39 patients) in group 2 (P = .66). Sensitivity was 91% (30 of 33) in group 1 and 100% (12 of 12) in group 2 (P = .68; Table 3).


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  		TABLE 1. Patient characteristics
 

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  		TABLE 2. Tumor characteristics
 

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  		TABLE 3. Results of lymphatic mappings and SLN identification
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Axillary lymphatic mapping and SLN biopsy have offered, without doubt, a greater possibility of reduced numbers of lymphadenectomies, which were useful for staging but were not curative. Nevertheless, the various techniques using isotopes, associated or not with vital dye and different sites of tracer injections, have produced results that are not always concordant. It seems that the SLN identification success rate reaches very high percentages with all the techniques used but, all the same, cannot confirm the FN rate. Without a doubt, an adequate learning curve, such as that maintained by Cody et al.,23 is necessary. However, it is not sufficient to reduce the FN rate. According to Kern,19 a high FN rate is related more to the site of vital dye injection than to surgical training or technique. He affirms that the breast parenchyma is a suboptimal site for dye-directed lymphatic mapping. Faries et al.24 have shown that SLNs are responsible for immunologically screening lymph. Antigen-presenting cells of the SLN take up mapping radiotracers by micropinocytosis. This phenomenon of active antigen trapping of mapping reagents in the SLN explains why grossly replaced lymph nodes often do not take up radioisotope or blue dye. With progressive tumor growth in the lymph node, there will be no uptake and retention of tracers, resulting in FN mapping.

In our study, we compared overall successful identification rates with the two techniques. In patients in group 1 (subdermal blue dye with or without peritumoral isotope), the overall successful identification was 94.8%: in particular, it was 95% with isotope plus blue dye and 94.6% with blue dye alone. In patients in group 2 (SA blue dye), the identification rate was 97.5%. The single failure occurred in a patient with a previous excisional biopsy in the upper outer quadrant of the breast and seemed to be due to resection of the main sentinel lymphatic channel. Kern19 also reported this failure in identifying the SLN, which can be explained anatomically by removal of the main lymphatic outflow tract of the breast. No difference was found in the number of SLNs identified and in the number of lymph nodes examined in the two groups. The FN rate was 9% in group 1 and 0% in group 2. The overall accuracy was 97% and 100%, respectively, in the two groups. Sensitivity was 91% in group 1 and 100% in group 2. These results show the better efficacy of SA injection of the tracer in axillary lymphatic mapping, and the results we achieved are similar to those of the other 11 series with SA injection published in the literature (Table 4). Kern19 performed SA blue dye injection alone in 40 patients, with 98% SLN identification and 0% FN rates. Klimberg et al.,20 using SA isotope injection and peritumoral blue dye injection, reported a 94.2% SLN identification rate. Mertz et al.25 reported an SLN identification rate of 98% and a 0% FN rate in 47 patients (16 with multifocal tumors) who received complete ALND. Borgstein et al.13 performed a periareolar injection of blue dye and peritumoral isotope in 130 patients, with a 96.9% identification rate and a 0% FN rate. Smith et al.21 compared 19 patients who received SA injection of 99mTc and peritumoral blue dye with 19 patients who received peritumoral injection of both materials. SLNs were found in all patients injected SA and in 18 of 19 injected peritumorally. The FN rate was 20% for peritumoral injection and 0% for SA injection. Kern and Rosenberg26 performed SA injection of both isotope and blue dye in 30 patients. No complete axillary dissections were performed in patients with negative SLNs by hematoxylin and eosin and immunohistochemistry. The identification rate was 96.7%. The FN rate is not available. McMasters et al.9 reported a 98.8% identification rate and a 5.9% FN rate in 85 patients by using SA isotope injection and peritumoral blue dye injection. Donahue27 demonstrated an identification rate of 100% and an FN rate of 8.3% in 42 patients by using peritumoral isotope and SA blue dye injection. Beitsch et al.28 described their technique with SA isotope and peritumoral blue dye injection in 85 patients, with an identification rate of 98%. Tuttle et al.29 reported a 100% identification rate with isotope SA injection and a 97% identification rate with peritumoral blue dye injection in 159 patients. In 98%, SLNs were blue and radioactive. The FN rate is not known because ALND was not performed if the SLN biopsy was negative. Bauer et al.30 reported the largest series of SA blue dye injection (249 patients) and peritumoral isotope injection, with an identification rate of 96.8%. The FN rate is not available because complete ALND was not performed. Finally, Kern,31 in a recent study of 187 cases, documented the nodal concordance between radiocolloid and blue dye uptake into SLNs after a same-site injection of both agents by the SA route, with an identification rate of 98.4%, an FN rate of 0% (0 of 20 cases), and an accuracy in predicting the malignant status of the axilla of 100%. This study is the first to evaluate dual-tracer, same-site injections of blue dye and radiocolloid by the SA approach.


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  		TABLE 4. Sentinel lymph node mapping with SA injection
 
These studies with SA injection have all achieved a high SLN identification rate (94.2% to 100%). The results of our study—a 97.5% identification rate and a 0% FN rate with only SA injection of blue dye—are similar to those of Kern.19 Although we presented a small series of SA injection for SLN mapping, we can nevertheless make some remarks. First, our experience with SA injections came after a long period of learning the technique of SLN biopsy with two tracers, so our results are derived from a consolidated experience in axillary lymphatic mapping. Second, when using SA vital dye injection, we always performed a complete ALND to further validate the method. Third, despite the literature that recognizes that the use of two tracers (radioisotope and dye) offers higher SLN identification rates, we propose the use of the two tracers in the initial stage of learning the technique, after the use of the vital dye only. We believe that this technique is easy. The simplicity and reliability of this method requires less expertise than other techniques. It avoids the necessity for image-guided injections for nonpalpable lesions. Moreover, SA injections reduce the shine-through effect from tumors located in the upper outer quadrant of the breast. Finally, the SA approach may be indicated for patients with multifocal breast cancer.


   FOOTNOTES
 
The aims of this study were to compare peritumoral and subdermal injection of tracer with subareolar injection of blue dye alone with sentinel lymph node biopsy. The subareolar lymphatic plexus may be the optimal way to perform lymphatic mapping in breast cancer.

Received for publication January 29, 2003. Accepted for publication June 16, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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