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Journal of Clinical Oncology, Vol 24, No 21 (July 20), 2006: pp. 3374-3380 © 2006 American Society of Clinical Oncology. DOI: 10.1200/JCO.2006.05.7372 Multicentric Breast Cancer: A New Indication for Sentinel Node Biopsy—A Multi-Institutional Validation Study
From the Department of Surgery, General Hospital, Feldkirch; University of Human Sciences, Principality of Liechtenstein; University Medical Center Graz; Department of Gynecology, Wilhelminenspital, Vienna; Department of Surgery, Krankenhaus der Barmherzigen Schwestern; Department of Surgery II, General Hospital, Linz; and the Department of Gynecology, University Medical Center, Salzburg, Austria Address reprint requests to Michael Knauer, MD, Department of General and Thoracic Surgery, Landeskrankenhaus Feldkirch, Carinagasse 47, A-6800 Feldkirch; e-mail: michael.knauer{at}lkhf.at
PURPOSE: Multicentric breast cancer has been considered to be a contraindication for sentinel node (SN) biopsy (SNB). In this prospective multi-institutional trial, SNB-feasibility and accuracy was evaluated in 142 patients with multicentric cancer from the Austrian Sentinel Node Study Group (ASNSG) and compared with data from 3,216 patients with unicentric cancer. PATIENTS AND METHODS: Between 1996 and 2004, 3,730 patients underwent SNB at 15 ASNSG-affiliated hospitals. Patient data were entered in a multicenter database. One hundred forty-two patients presented with multicentric invasive breast cancer and underwent SNB. RESULTS: Intraoperatively, a mean number of 1.67 SNs were excised (identification-rate, 91.5%). The incidence of SN metastases was 60.8% (79 of 130). This was confirmed by axillary lymph node dissection (ALND) in 125 patients. Of patients with positive SNs, 60.8% (48 of 79) showed involvement of nonsentinel nodes (NSNs), as did three patients with negative SNs (false-negative rate, 4.0). Sensitivity, negative predictive value, and overall accuracy were 96.0%, 93.3%, and 97.3%, respectively. Ninety-one percent of the patients underwent mastectomy, and 9% were treated with breast conserving surgery. None of the patients have shown axillary recurrence so far (mean follow-up, 28.8 months). Compared with 3,216 patients with unicentric cancer, there was a significantly higher rate of SN metastases as well as in NSNs, whereas there was no difference in detection and false-negative rates. CONCLUSION: Multicentric breast cancer is a new indication for SNB without routine ALND in controlled trials. Given adequate quality control and an interdisciplinary teamwork of surgical, nuclear medicine, and pathology units, SNB is both feasible and accurate in this disease entity.
Sentinel node (SN) biopsy (SNB) has become the standard of care for axillary staging of breast cancer in many institutions during the last decade. Many validation studies showed it to be accurate and feasible for unicentric invasive breast cancer.1-8 In addition to unicentric breast cancer, larger ductal carcinomas in situ—especially those suspected of containing microinvasion or scheduled for mastectomy, as well as multifocal cancers up to 3 to 4 cm in diameter—are among its accepted indications.9 SNB continues to be controversial after preoperative chemotherapy, although the case for this approach is getting stronger.10-12 Compared with routine axillary lymph node dissection (ALND), SNB causes less morbidity, has lower costs, and is more reliable for axillary staging because of multiple section analyses.13 Most authors consider SNB to be contraindicated in multicentric breast cancer (MC), because tumors located in different quadrants of the breast were thought not to drain into the same SN. This may result in inaccurate lymph node staging and high false-negative rates.7,14 But if SNB were a valid concept in MC just as in unifocal lesions, this patient group would also benefit from less morbidity and more accurate lymph node staging. Evidence obtained in the last few years about the functional anatomy of the lymphatic drainage of the breast supports the theory that all quadrants of the breast drain into the same lymph node(s).15,16 Grant17 and Gould18 reported the existence of a deep and a superficial lymphatic system with a subareolar (SA) plexus that drains the axillary lymph nodes via one or two main lymphatic vessels. SA injection of blue dye and/or radiocolloid was described for unicentric breast cancer. Reported results and those of our institution showed its SN detection rate to be the same as that of peritumoral (PT) injection techniques.16,19-22 The feasibility and accuracy of SNB in MC using the SA injection technique for lymphatic mapping was described by some authors.23-25 The purpose of this validation study was to confirm the feasibility and accuracy of SNB in MC. Designed as a multi-institutional trial, it was conducted by the Austrian Sentinel Node Study Group (ASNSG) and supported by the Austrian Society of Senology.
Patients and Data Between September 1996 and November 2004, 3,730 clinically node-negative patients with operable biopsy-proven invasive or in situ breast cancer underwent SNB at 15 ASNSG-affiliated hospitals. Patient data were entered prospectively in the multicenter database (Microsoft Access; Microsoft, Redmond, WA).26 The participating institutions used separate local versions of the database. Their data were coded and transferred to the main database by e-mail. From there, regular checks were made to assure high data quality. One hundred forty-two patients with MC underwent sentinel lymph node mapping. Their data were compared with those of 3,216 patients with unicentric cancer. The SNB results of the ASNSG in unicentric breast cancer were reported elsewhere.27 Consistent with the currently accepted terminology, MC was defined as two or more physically separate invasive tumors in two or more breast quadrants. Multicentricity was suspected from clinical and radiologic findings (ie, mammography and sonography were performed in all patients and completed by MRI in unclear cases). The diagnosis of multicentric cancer was confirmed histologically in all patients by fine-needle aspiration or core-needle biopsy before surgery or by frozen sections of the tumor specimen intraoperatively. Further inclusion criteria were a negative axilla by clinical and sonographic evidence as well as the absence of distant metastases. The mean age of the study population was 56 years. Approximately 40% of the patients were premenopausal. Detailed patient and tumor characteristics are shown in Table 1. After information of the ethics committee, written informed consent to participate in the lymphatic mapping procedure was obtained from all patients.
Lymphatic Mapping Technique For lymphatic mapping either vital blue dye (Isosulfan blue 1%, Lymphazurin; Ben Venue Laboratories, Bedford, OH; or Patent blue V Guerbet 2.5%, Geurbet, Roissy Cdg Cedex, France), 2 to 5 mL, or Tc99m-nanocolloid (Nanocoll), 20 to 85 MBq, alone or combinations of blue dye and radiocolloid were used as shown in Table 2. Radionuclide alone was injected in 10 cases (7.0%), blue dye alone in 54 cases (38.0%) and a combination of both in 78 cases (54.9%). Preoperative lymphoscintigraphy was performed in all patients who had a radiocolloid injected previously. Intraoperatively, the SN was identified by retrieving blue staining lymph nodes and hot nodes using a hand-held gamma camera. SNB was followed by visual inspection and palpation for further suspect lymph nodes; no extra-axillary SNs were removed. Level I and II ALND was completed in 125 of the 142 cases, because one participating surgical department had already started to avoid routine ALND in patients with negative SNB. Sentinel and nonsentinel nodes (NSNs) were submitted separately for histology.
Surgical Procedures Subsequent surgery of the breast tumors consisted of mastectomy in 129 patients (90.9%) or breast-conserving procedures in 13 selected cases (9.2%), when assumed reasonable by the surgeon and patients refused to undergo mastectomy. Details are shown in Table 3.
Histologic Evaluation of SNs As recommended by the Austrian Society of Pathologists,28 sentinel nodes less than 5 mm in size were cut in half paracentrally. One half was used for frozen section analysis in three planes, whereas the other was embedded in paraffin for further analysis (sections spaced 200 µm apart). Of SNs larger than 5 mm in size, a central slice of 2 mm was used for frozen section analysis in three planes. The remaining material was cut in 2-µm slices (spaced 200 µ apart) and embedded in paraffin for further analysis. From all slices, one specimen was stained by hematoxylin and eosin (H&E). In all H&E-negative cases, immunohistochemical staining was used. All SNs were classified by the International Union Against Cancer criteria.
Statistical Analysis
A total of 142 patients (one to 44 per participating surgical unit) with MC on final histopathologic examination fulfilled the criteria for this study. The detailed demographic characteristics are shown in Table 1. An SN was successfully identified in 130 of these 142 patients (detection rate, 91.5%). Intraoperatively, a mean number of 1.67 sentinel nodes (range, 1 to 5 nodes ± 0.9) was successfully excised. The concordance rate of blue dye and radiocolloid in 78 patients with combined applications was 67.9% for "blue and hot" nodes (Table 2). The overall incidence of SN metastases was 60.8% (79 of 130 patients), 51 patients (of 130, 39.2%) showed no tumor in the SN, 83.5% (66 of 79) of the positive SNs were found by H&E staining, and the remaining 16.5% (13 of 79) were detected by immunohistochemical staining that was performed in all H&E-negative nodes. This was confirmed by level I and II ALND in 125 patients, because one department had started to omit routine ALND in patients with negative SNB in January 2003. The mean number of resected axillary lymphnodes in ALND was 16.1 (± 6.9; minimum, 4; maximum, 46). The SN was the only node showing metastatic disease in 31 (39.2%) of 79 patients. Forty-eight (60.8%) of the 79 patients with positive SNs showed involvement of NSNs as did three patients with negative SNs. Although the rates of positive SNs and NSNs were significantly higher than in the 3,216 patients with unicentric invasive breast cancer, there was no statistical difference in detection and false-negative rates. However, there was a slightly lower false-negative rate of 4.0% (three of 75 patients) versus 6.4% in unicentric cancer (false-negative rate = number of false-negative SNs / true-positive + false-negative nodes x 100). Summary details are shown in Table 4 and Figure 1.
Sensitivity (true-positive / true-positive + false-negative x 100), negative predictive value (true-negative / true-negative + false-negative x 100) and overall accuracy (true-positive + true-negative / successful SNBs x 100) in our patients were 96.0%, 93.3%, and 97.3%, respectively. The likelihood ratio for negative test results (likelihood ratio = (1 –sensitivity) / specificity) was 0.04, indicating an excellent test outcome. SA injection of blue dye or radiocolloid appeared to be as effective and accurate as PT application.16,19,20,24,29 In 106 patients who underwent lymphatic mapping by SA injection of blue dye or radiocolloid and ALND, the false-negative rate dropped to 3.1% (two of 64 patients). Adjuvant treatment regimens were distributed as follows: Hormonal therapy in 70% of patients, chemotherapy in 48%, adjuvant radiation therapy in another 48%, and immunotherapy with trastuzumab in 3%. Details are shown in Table 3.
Follow-Up Of the 34 patients with negative SNs who underwent ALND, three were found to have metastatic NSNs. At a mean follow-up time of 35.4 months (range, 4 to 66 months ± 14.9), four events were recorded: local recurrence at 16 months in one patient, distant metastases in two patients after 21 and 48 months, respectively, and one death at 11 months. In the group of 79 patients with positive SNs who underwent ALND (48 of 70 patients; 60.8%), 11 events were recorded during a mean follow-up time of 28.5 months (range, 0 to 73 months ± 17.5), among them two local recurrences at 19 and 41 months. Eight patients developed distant metastases after 3 to 36 months, and four died after 10 to 38 months. In summary, none of the women in this study who underwent SNB for MC developed recurrent axillary disease during the follow-up times listed (median follow-up time of all patients, 28.8 months). Disease-free survival is shown as Kaplan-Meier curve and shown separately for negative versus positive SNs (Figure 2).
First described by Krag30 and Giuliano31 12 years ago, SNB has become clinically routine for diagnosing breast cancer in many centers.30,31 The 2003 St Gallen Consensus Panel also accepted it as a diagnostic tool for axillary staging. The feasibility and usefulness of the concept was confirmed in several studies, particularly for unicentric breast cancer, although evidence showing its oncologic safety in terms of locoregional recurrence rates and overall survival is still scarce.6-8,32-34 On the basis of current evidence, SNB has a definite place in unicentric, biopsy-proven, operable stage T1-2 breast cancer without clinical and sonographic clues to axillary lymph node involvement. In the American Society of Clinical Oncology Guidelines published in the Journal of Clinical Oncology in October 2005, 9 it is also rated as an acceptable procedure for MC, although the available evidence is limited to some small-scale trials. This rating is supported by our data, which were derived from the largest series reported to date in a multicenter setting. Initially, SNB was performed after PT dye or radiocolloid injection. This approach was dictated by the assumption that every lymph node was associated with a specific body region. Estourgie et al35 even went to the point of injecting the radioactive tracer into the tumor, suspecting that tumors in different quadrants drained into different SNs. Routine PT injection proved to be cumbersome in patients with occult lesions. This prompted a search for alternative applications. Sappey36 and Grant17 found a dense network of lymphatic channels between areola, breast tissue, and axillary lymph nodes. Following up their work and that of Gould, 18 who described the existence of an SN in parotid cancer, Borgstein15 and Klimberg16 showed that tumors located in different quadrants of the breast drained into the axilla by way of an SA lymphatic plexus. This uniform drainage system was interconnected by a communicating superficial and deep lymphatic system. With intradermal radiocolloid and PT dye injections in one and the same or different breast quadrants of 119 patients, Nathanson37 found a statistically identical concordance of blue staining and hot lymph nodes in both groups (95.5% v 93.9%). These data ultimately led to the conclusion that tumors located in different quadrants drained into the same SN. PT injection has also been tried for multicentric lesions, but proved to be unfeasible in patients with nonpalpable tumors or produced high false-negative rates.38 In contrast to the imaging needed for multiple PT injections, SA injection offers a dual advantage: The dye or radiocolloid is rapidly drained into the axillary lymph nodes, and time is saved because prior tagging of nonpalpable tumors is unnecessary. Several studies, meanwhile, established that SA injections were at least equal to PT injections in unicentric breast cancer.16,20,21,25,39,40 In an analysis of 307 patients from our institution, SA injections were found to be superior to PT injections. Detection rates were 99% (194 of 196 patients) for the SA technique versus 90% (100 of 111 patients) for the PT technique, with the difference being statistically significant (P < .001).22 All of these studies showed a high rate of concordance between subareolar and PT injections. In terms of the functional anatomy of the breast, this suggests that both techniques detect the same SNs. In the present study of 106 patients with multicentric lesions, the false-negative rates were 3.1% for SA dye or radiocolloid injections versus 4.0% for all patients including varying techniques. Several authors have, meanwhile, investigated the feasibility of SNB for multifocal and multicentric lesions. Ozmen et al40 reported 33% false-negative findings in patients with multifocal lesions (four of 12 patients) and attributed these to the multifocality. The exclusive PT dye injection without radiocolloids is, however, likely to have been a contributing factor. Goyal et al42 reported on 75 patients with multifocal cancer. Given a detection rate of 95% and a false-negative rate of 8.8%, they concluded that SNB was an alternative to routine axillary dissection. Tousimis et al43 and Layeeque et al25 documented the data for 70 and 40 patients, respectively, some of them with multicentric cancer. In view of a detection rate of 97% and a false-negative rate of 8%, the group at the Memorial Sloan-Kettering Cancer Center (New York, NY) concluded that the accuracy of SNB was comparable to that in unicentric lesions, but that formal ALND should be performed for all T3 lesions. The Little Rock (AK)25 group reported a detection rate of 100% and 0% false-negative findings and also concluded that SA radiocolloid or dye injection may well be an alternative to complete ALND. In Table 5, the reported data of some patients with multicentric cancer while others showed multifocal cancer are set against those we recorded in strictly MC patients.
In our study, the mode of dye/radiocolloid application was deliberately left to the examiners involved. Significantly, a strict concordance of blue and hot SNs was limited to 68% of the 78 cases subjected to combined injections of a blue dye and a radiocolloid. Eighty-one percent showed both blue nodes and sometimes different hot nodes, 9% only blue nodes, and 4% only hot nodes. In our reading, this underscores the need for combined injections. In the series of Goyal et al,42 Tousimis et al,43 and Layeeque et al,25the high rate of positive SNs and NSNs (48% to 63% and 28% to 63%) was a significant finding. Our data confirmed these highly significant differences. This suggests that defining the size of the tumor by the largest lesion is unsuited for T staging. Andea et al43 showed that the sum total of the diameters of all lesions would be more helpful for predicting the likelihood of positive sentinel nodes in multicentric cancer. In another study, however, the authors computed the sum total of multicentric cancer volumes and concluded that multicentric tumors had distinctly different biologies and that even small lesions tended to metastasize to the lymph nodes.45 Not all centers handle SNB in the same way. This aspect of procedural SNB quality is in need of improvement. The mode of dye and radionuclide application is a case in point. Compliance with certain quality criteria (detection rate > 95%, false-negative rate < 5%) is another important point. As with unicentric cancers, this was heeded in the present study. Collecting patient data in a database like the one kept by the ASNSG is an excellent approach because it ensures an ongoing outcome quality control by clearing up the data at regular intervals and monitoring post-SNB patient follow-ups. There is yet another point: In our patient population, the percentage of SN-positive patients was 61%. Involvement of the sentinel node was associated with involvement of other lymph nodes in well over 60% of cases. This implies that more than every third woman with multicentric cancer benefits from SNB and can at least be spared the morbidity of axillary dissection if not mastectomy. The outcome quality of diagnostic SNB should, however, not be confined to high detection rates and low false-negative rates. The long-term prognosis is just as important. None of the patients with MC enrolled in the study including the 17 without ALND developed axillary recurrence during the specified follow-up times. However, the follow-up times (ie, 35 months for the patients with negative SNs who underwent ALND and 17 months for those with negative SNBs who were spared ALND) are too short for recommending SNB without ALND for all patients with MC. Still, the evidence available to date is encouraging. In conclusion, MC constitutes a new indication for SNB only without axillary dissection, but by now it should still be restricted to controlled trials given a defined quality structure and compliance with the criteria addressed herein.
The authors indicated no potential conflicts of interest.
We thank the Austrian Society of Senology for supporting this study and all the contributing institutions for the continuous high-quality data collection, as follows: General Hospital Linz, Dept. of Surgery II University Medical Center Salzburg, Dept. of Gynecology General Hospital Feldkirch, Dept. of Surgery Wilhelminenspital, Dept. of Gynecology, Vienna Krankenhaus der Barmherzigen Schwestern, Dept. of Surgery, Linz Lainz Hospital, Dept. of Gynecology, Vienna General Hospital Hainburg, Dept. of Surgery General Hospital Klagenfurt, Dept. of Surgery General Hospital Kufstein, Dept. of Surgery Clinic Chirurgie Tausch, Linz General Hospital Vienna, Dept. of Surgery
Supported by the Austrian Society of Senology. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2006 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
