Radiologic Mapping for Targeted Axillary Dissection: Needle Biopsy to Excision

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1 Women s Imaging linical Perspective Shin et al. Radiologic Mapping for xillary Dissection Women s Imaging linical Perspective Kyungmin Shin 1 bigail S. audle 2 Henry M. Kuerer 2 Lumarie Santiago 1 Rosalind P. andelaria 1 asak Dogan 1 Jessica Leung 1 Savitri Krishnamurthy 3 Wei Yang 1 Shin K, audle S, Kuerer HM, et al. Keywords: axillary lymph node, breast, breast cancer, radioactive seed, targeted axillary dissection, ultrasound DOI: /JR Received March 31, 2016; accepted after revision June 28, Supported by the National Institutes of Health, National ancer Institute, through MD nderson ancer enter support grant (016672) and by funding from the P. H. and Fay Etta Robinson Endowed Distinguished Professorship (H. M. Kuerer), the Mike Hogg foundation (. S. audle), and an MD nderson linical Innovator ward (. S. audle). 1 Department of Diagnostic Radiology, reast Imaging, The University of Texas MD nderson ancer enter, P5.3200, Unit 1350, 1515 Holcombe lvd, Houston, TX ddress correspondence to K. Shin (kshin1@mdanderson.org). 2 Department of reast Surgical Oncology, The University of Texas MD nderson ancer enter, Houston, TX. 3 Department of Pathology, The University of Texas MD nderson ancer enter, Houston, TX. This article is available for credit. JR 2016; 207: X/16/ merican Roentgen Ray Society Radiologic Mapping for Targeted xillary Dissection: Needle iopsy to Excision OJETIVE. The purpose of this article is to describe the feasibility and safety of a multidisciplinary approach to imaging-guided axillary staging that facilitates personalized, less invasive surgical management of the axilla through targeted axillary dissection in patients with biopsy-proven nodal metastasis undergoing neoadjuvant chemotherapy. ONLUSION. xillary nodal status, critical in breast cancer staging, affects prognosis and treatment. s the paradigm shifts toward minimally invasive therapy, a clip marker is placed in the biopsied metastatic node for patients with N1 N2 disease undergoing neoadjuvant chemotherapy to facilitate targeted axillary dissection of the clipped node. This node is typically localized with a radioactive seed at sentinel lymph node dissection to determine whether further axillary surgery is warranted. M anagement of the axilla in patients with breast cancer has evolved dramatically toward less invasive measures that decrease morbidity without negatively affecting prognosis. Historically, patients with primary breast cancer with any number of metastatic axillary lymph nodes underwent axillary lymph node dissection (LND). The merican ollege of Surgeons Oncology Group (OSOG) Z0011 trial, a prospective, randomized, multicenter study, showed that LND provided no survival benefit over less invasive sentinel lymph node dissection (SLND) during a 6-year follow-up period in a selected cohort of patients with clinical T1 T2 invasive breast cancer, who had no palpable adenopathy and one or two biopsy-proven metastatic sentinel lymph nodes [1]. The results of this trial led to changes in the radiologic and surgical approaches to the evaluation and the management of the axilla for a selected subset of patients with breast cancer [2 9]. More recent trials have been conducted to evaluate the utility of SLND in the treatment of patients with biopsy-proven node-positive disease who underwent neoadjuvant chemotherapy. The OSOG Z1071 trial was a phase 2 study of the clinical efficacy of substituting SLND for LND in the treatment of such patients by evaluating the false-negative rate (FNR) of SLND in patients with clinical T0 T4, N1 N2, M0 breast cancer [10]. s many as 40% of patients with estrogen receptor positive tumors who underwent neoadjuvant chemotherapy had a complete response in the axillary lymph nodes. The response rates were even higher in patients with estrogen receptor negative disease or high-grade disease and was as high as 74% in patients with Erb-2 positive, also known as HER2/neu-positive, disease treated with a trastuzumab-based neoadjuvant regimen [10, 11]. These response rates suggest that methods should be explored to identify patients with disease that converts to pathologic node-negative status and may be spared the morbidity associated with LND [9, 12]. The threshold of success of the Z1071 trial in investigating whether SLND is safe for staging the axilla after neoadjuvant chemotherapy in a subset of patients was an FNR of less than 10%, the expected rate for patients with cn0 disease undergoing SLND [13]. The FNR of the Z1071 trial, 12.6%, did not meet this primary endpoint [10]. Despite its failure to meet the primary endpoint, this study showed a lower FNR in patients who had a greater number of lymph nodes (two or more) sampled at the time of SLND and who underwent a dual tracer technique (both radioisotope and blue dye). This finding suggested that it may be feasible to omit LND with careful use of such techniques. Data from the Z1071 trial presented at the 2014 San ntonio reast ancer Symposium showed that in a subset of 1372 JR:207, December 2016

2 Radiologic Mapping for xillary Dissection 107 patients who underwent SLND in which the biopsy-proven metastatic lymph node was marked by a clip, the FNR was 6.8%, well below the 10% primary endpoint [14]. Part of the reason for this improvement over SLND alone is that the clipped node was not always retrieved as a sentinel lymph node [14 17]. Of the 170 patients who had a clip placed in a node, 34 had a clipped nonsentinel node in the axillary specimen, and the clip location was unknown in an additional 29 patients [17]. audle et al. [17] found in a 2016 study that targeted axillary dissection (TD) followed by LND in 85 patients had an FNR of 2.0% (1/50; 95% I, %). These results suggest that clip placement in the biopsy-proven metastatic lymph node to ensure its excision after neoadjuvant chemotherapy contributes to a decrease in the FNR of SLND. We developed a multidisciplinary approach to imaging-guided axillary staging to facilitate personalized, less invasive surgical management of the axilla by TD for patients with biopsy-proven nodal metastasis undergoing neoadjuvant chemotherapy at our institution [11, 18]. This article describes the feasibility and safety of this technique. Overview of Targeted xillary Dissection The imaging evaluation of a patient with a breast cancer diagnosis at our institution includes an ultrasound assessment of the locoregional lymph node basins that includes the axilla. t some institutions, additional regional lymph node basins, including the infraclavicular, internal mammary, and supraclavicular nodal basins, may be examined to provide a roadmap for radiation therapy. In TD, patients with regional nodal disease limited to the axilla have a clip marker placed in the biopsy-proven metastatic axillary lymph node at the time of needle biopsy. Only patients with N1 or N2 disease are eligible for TD. t the completion of neoadjuvant chemotherapy, typically anthracycline-based, taxane-based, or a combination of both with the addition of Erb-2 targeted therapy for Erb-2 positive breast cancer, the biopsyproven metastatic axillary lymph node with a clip in situ is identified with real-time ultrasound and localized with a 125 I-radiolabeled seed under ultrasound guidance before surgery. The patient undergoes SLND and concurrent excision of the clipped metastatic axillary lymph node. The surgeon uses a gamma probe with the 125 I setting for identification of the lymph node marked with the radioactive seed. This procedure ensures that the biopsy-proven metastatic axillary lymph node is removed at the time of SLND even if it does not correspond to the sentinel lymph node as marked by the 99m Tc-labeled radioisotope (lymphoscintigraphy) and blue dye. Intraoperative specimen radiography is performed on the excised clipped lymph node to document removal of the biopsied metastatic lymph node and the radioactive seed. The clipped lymph node is then sectioned and processed by a breast pathologist and the results reported separately. Evaluation of Regional Nodal asins and Selection of xillary Lymph Nodes for iopsy ccurate staging of breast cancer is needed for optimal prognostic evaluation and treatment planning. The TNM staging system is used for breast cancer. This system accounts for the size of the primary tumor (T), regional nodal status (N), and the presence or absence of distant metastasis (M) [19]. The locoregional nodal basins include the axillary, infraclavicular, supraclavicular, and internal mammary lymph nodes. ecause of the lymphatic drainage pathway, most breast cancers first metastasize to the ipsilateral axillary lymph nodes. In approximately 12 25% of patients, however, the initial lymphatic drainage is to the internal mammary lymph nodes, especially for medial cancers [20]. Therefore, care should be taken to thoroughly evaluate the locoregional nodal basins to avoid nodal upstaging, which has been reported in as many as 37% of patients and has considerable impact on prognosis and medical, surgical, and radiation treatments [21]. t our institution, patients with a suspicious breast abnormality undergo sonographic evaluation of the locoregional lymph node basins and ultrasound-guided fine-needle aspiration biopsy of the lymph node with the highest N category with immediate on-site cytologic examination. ecause the sensitivity of ultrasound-guided fine-needle aspiration and core biopsies of suspicious lymph nodes in the preoperative staging of breast cancer ranges from 73% to 88%, this practice is currently widely used [22 27]. In the evaluation of lymph nodes with realtime high-resolution ultrasound to differentiate malignant from benign disease, lymph node size has poor diagnostic accuracy, because the mean sizes of benign and malignant lymph nodes have considerable overlap [20, 28]. The morphologic features of lymph nodes, including shape, cortical and hilar structure, and echotexture, are important in the evaluation of lymph node disease in breast cancer. The ultrasound features that have been helpful in identifying potentially malignant lymph nodes include cortical thickness equal to or greater than 3 mm, focal or eccentric cortical thickening, cortical hypoechogenicity, loss or effacement of the fatty hilum, abnormally round or irregular shape, presence of microcalcifications if microcalcifications are present in the primary malignant breast lesion, and, to a lesser degree, abnormally increased peripheral blood flow [20, 28 31]. When these features are used, the sensitivity of ultrasound in the detection of metastasis ranges from 54% to 77%, and the specificity ranges from 80% to 88%. Of these features, irregular or round shape and effacement of the fatty hilum have been found to have the highest specificity [20, 28, 29]. Documentation of the number of suspect lymph nodes contributes to the prediction of the pathologic nodal stage: three or fewer metastatic axillary lymph nodes represent N1 disease; four to nine metastatic lymph nodes, N2; and 10 or more metastatic lymph nodes, N3 [19]. lip Placement in the iopsy-proven Metastatic Lymph Node clip marker is placed within the biopsyproven malignant axillary lymph node at ultrasound-guided needle biopsy. In patients with metastatic internal mammary, infraclavicular, or supraclavicular lymph nodes (N3 disease), a marker clip is not placed because these patients need LND after neoadjuvant chemotherapy and are not candidates for SLND or TD [10, 16]. The clipped metastatic axillary node is localized to facilitate excision during SLND and to ensure removal. In the Z1071 trial, as many as 20% of the biopsy-proven malignant axillary lymph nodes did not correspond to the sentinel lymph node at SLND [10]. In a sample of 12 patients who underwent evaluation in a prospective feasibility trial of TD designed to develop a mechanism to ensure surgical excision of the clipped node and to confirm that the clip caused no technical interference with sentinel lymph node radiocolloid detection, residual nodal disease after neoadjuvant chemotherapy was identified in the biopsy-proven malignant clip-containing lymph node in four patients [16]. Marking the biopsy-proven malignant lymph node is thus essential for accurate localization and excision, especially when malignant lymph nodes respond well to neoadjuvant chemotherapy and may appear different or normal during follow-up ultrasound. JR:207, December

3 Shin et al. Placing the clip marker within the biopsy-proven metastatic lymph node is important. lip placement within the cortex of the lymph node enhances visualization of the clip at localization. Placement of the hyperechoic clip within the surrounding hypoechoic cortex (Fig. 1) optimizes visibility, whereas placement within the hyperechoic fatty hilum may reduce clip visibility. t our institution, HydroMark T3 (Devicor Medical Products), Tumark Professional (PriorityMedical), and coil-shaped Ultralip Dual Trigger breast tissue marker (.R. ard) devices are used to mark the lymph nodes. In our experience, these markers have had the best visibility within lymph nodes both before and after neoadjuvant chemotherapy (Figs. 1 3). Iodine 125 Labeled Radioactive Seed Placement in lipped Lymph Node and Surgical Retrieval To assist the surgeons in identifying the clipped axillary lymph node, the node is localized by ultrasound-guided implantation of a radioactive seed. The radioactive seed is typically placed after completion of neoadjuvant chemotherapy and within 5 days before surgery. Placing the radioactive seed before the day of surgery improves work flow for both the radiologists and the surgeons by eliminating the need for coordination between the operating room and imaging-guided localization on the day of the procedure [32, 33]. Radioactive seed localization is also more comfortable for the patient than the conventional wire localization method because there is no external device. The lymph node is radiolabeled with a 125 I-labeled titanium-encapsulated seed with radioactivity of mi and an average energy of 27 kev. The label has a long half-life of 59.6 days, which allows seed placement any time during the 5 days before the procedure, although it is typically placed the day before the procedure at our institution to minimize the patient s radiation exposure. The radioactive seed is loaded in an 18-gauge needle occluded with bone wax at the tip and deployed by advancing the stylette into the clip-containing lymph node under ultrasound guidance (Fig. 4). fter the seed is placed, its location is confirmed with mediolateral oblique view mammography (Fig. 5). t surgery, the lymph node containing the radioactive seed is identified with a handheld gamma probe optimized to 125 I radioactivity as the point of highest activity in the axilla and is excised. n intraoperative specimen radiograph of the excised axillary tissue is obtained to confirm and document the presence of the clip-containing lymph node and removal of the radioactive seed (Fig. 6). lthough axillary lymph node localization with a 125 I-labeled seed is a novel technique in the United States, Donker and Straver and their colleagues [34, 35] have previously reported on its usefulness in patients undergoing neoadjuvant chemotherapy. In the European study, however, the radioactive iodine labeled seed was placed at diagnosis and remained in situ for up to 4 months, a practice that would not be acceptable in the United States because of radiation safety guidelines. Pitfalls and Resolutions The practice of TD requires multidisciplinary collaboration between breast imaging radiologists, nuclear medicine physicians, breast surgeons, and breast pathologists that is centered on the placement and mandatory documented retrieval of the radioactive iodine ( 125 I) seed in the axillary node. lternative nonradioactive endomagnetic and radiofrequency markers are being evaluated for breast and axillary placement in an attempt to circumvent nuclear regulatory compliance issues. Second, clips placed in biopsy-proven metastatic axillary nodes may not be as readily visible when the enlarged, grossly abnormal metastatic node responds to neoadjuvant chemotherapy and resumes normal size and morphologic features. In our experience, careful documentation of the clip within the clipped node in both the transverse and longitudinal planes at clip placement and measurement of the depth of the clipped node in relation to surrounding normal anatomic features is helpful in addressing this problem. onclusion TD is feasible and can be performed safely when the radiologist diligently places a clip marker within the metastatic axillary lymph node found at biopsy and follows up with an appropriate localizing device and technique for seed localization and surgical excision. The substantial decrease in FNR when the clip-containing lymph node is excised at SLND after neoadjuvant chemotherapy suggests that TD is a promising technique for broader application in the future. References 1. Giuliano E, Hunt KK, allman KV, et al. xillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. 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4 14. oughey J, allman K, Symmans W, et al. 33: edi DG, Krishnamurthy R, Krishnamurthy S, et Radiologic Mapping for xillary Dissection Methods impacting the false negative rate of sentinel 21. Iyengar P, Strom E, Zhang YJ, et al. The value of al. ortical morphologic features of axillary lymph node surgery in patients presenting with node positive breast cancer (T0-T4,N1-2) who receive neoadjuvant chemotherapy: results from a prospective trial: OSOG Z1071 (lliance). (abstract) ancer Res 2015; 75 (9 suppl): oughey J, Suman VJ, Mittendorf E, et al. Factors affecting sentinel lymph node identification rate after neoadjuvant chemotherapy for breast cancer patients enrolled in OSOG Z1071 (lliance). nn Surg 2015; 261: audle S, Yang WT, Mittendorf E, et al. Selective surgical localization of axillary lymph nodes containing metastasis in patients with breast cancer: a prospective feasibility trial. JM Surg 2015; 150: audle S, Yang WT, Krishnamurthy S, et al. 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J Ultrasound Med 2013; 32: Mainiero M, inelli M, Koelliker SL, Graves T, hung M. xillary ultrasound and fineneedle aspiration in the preoperative evaluation of the breast cancer patient: an algorithm based on tumor size and lymph node appearance. JR 2010; 195: lymph nodes as a predictor of metastasis in breast cancer: in vitro sonographic study. JR 2008; 191: Yang WT. xillary adenopathy and axillary nodal calcifications. In: erg W, Yang WT, eds. Diagnostic imaging: breast, 2nd ed. Philadelphia, P: Lippincott Williams & Wilkins, 2013: Net JM, Mirpuri TM, Plaza MF, et al. US evaluation of axillary lymph nodes: resident and fellow education feature. RadioGraphics 2014; 34: Elmore L, ppleton M, Zhou G, Margenthaler J. xillary ultrasound in patients with clinically node-negative breast cancer: which features are predictive of disease? J Surg Res 2013; 184: Sharek D, Zuley ML, Zhang JY, Soran, hrendt GM, Ganott M. 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Marking the axillae with radioactive iodine seeds (MRI procedure) may reduce the need for axillary dissection after neoadjuvant chemotherapy for breast cancer. r J Surg 2010; 97: Fig year-old woman with invasive ductal carcinoma (grade 3) of left breast and ultrasound finding of abnormal left axillary lymph node., Ultrasound image obtained during fine-needle aspiration biopsy of abnormal lymph node with 21-gauge needle. iopsy finding was metastatic carcinoma. Loss of fatty hilum in metastatic lymph node is evident., Ultrasound image shows HydroMark T3 marker clip (Devicor Medical Products) (arrow) within biopsied malignant lymph node. Hyperechoic clip is evident in center of hypoechoic malignant lymph node. (Fig. 1 continues on next page) JR:207, December

5 Fig. 1 (continued) 35-year-old woman with invasive ductal carcinoma (grade 3) of left breast Shin and et al. ultrasound finding of abnormal left axillary lymph node., Mammogram obtained after biopsy shows marker clip (arrow) within malignant left axillary lymph node. Fig year-old woman with invasive ductal carcinoma of right breast., Ultrasound image shows Tumark Professional clip (PriorityMedical) (arrow) within biopsy-proven metastatic lymph node. iopsy clip is clearly evident as echogenic structure., Ultrasound image shows marker clip within metastatic lymph node. Dotted line is measurement from skin to clip; this depth landmark is used for radioactive seed placement., Mammogram obtained after biopsy clearly shows placement of marker clip (arrow) within biopsy-proven metastatic lymph node JR:207, December 2016

6 Radiologic Mapping for xillary Dissection Fig year-old woman with invasive ductal carcinoma and ductal carcinoma in situ of left breast., Ultrasound image shows abnormal enlarged left axillary lymph node with focal cortical thickening (arrow)., Mammogram obtained after biopsy shows placement of marker clip within metastatic left axillary lymph node., Ultrasound image obtained after neoadjuvant chemotherapy shows abnormal lymph node has decreased in size. lip (arrow) is clearly evident within cortex. D, Mammogram obtained after neoadjuvant chemotherapy shows clip (arrow) within metastatic left axillary lymph node that has decreased in size. D JR:207, December

7 Shin et al. Fig. 4 Photograph shows device with introducer for 125 I-labeled titaniumencapsulated seed. Fig year-old woman with invasive ductal carcinoma of right breast., Ultrasound image shows metastatic lymph node containing marker clip (arrow) after completion of neoadjuvant chemotherapy. and, Ultrasound images show placement of radioactive seed (arrow, ) within clip-containing node. D, Mammogram obtained after radioactive seed placement shows seed adjacent to marker clip (arrow) within metastatic lymph node. Multiple marker clips in breast are from previous biopsies, one of which had malignant result. D 1378 JR:207, December 2016

8 Fig year-old man with invasive moderately differentiated adenocarcinoma Radiologic Mapping for of xillary left breast. Dissection, Ultrasound image shows previously placed marker clip within malignant lymph node (arrow) after completion of neoadjuvant chemotherapy. and, Ultrasound images show placement of 125 I-labeled seed (arrow, ) within clip-containing lymph node. D, Mammogram obtained after seed placement shows marker clip (dashed arrow) and radioactive seed (solid arrow) within lymph node. Marker clip within breast mass is consistent with biopsy-proven malignancy. E, Specimen radiograph confirms excision of clip-containing lymph node (dashed arrow) and radioactive seed (solid arrow). D E FOR YOUR INFORMTION This article is available for ME and Self-ssessment (S-ME) credit that satisfies Part II requirements for maintenance of certification (MO). To access the examination for this article, follow the prompts associated with the online version of the article. JR:207, December