Women s Imaging Original Research

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1 Women s Imaging Original Research Mainiero et al. Ultrasound-Guided FN in Breast Cancer Patients Women s Imaging Original Research WOMEN S IMGING Martha B. Mainiero 1 Christina M. Cinelli 2 Susan L. Koelliker 1 Theresa. Graves 3 Maureen. Chung 3 Mainiero MB, Cinelli CM, Koelliker SL, Graves T, Chung M Keywords: axillary lymph node staging, axillary ultrasound, breast cancer, fine-needle aspiration, lymph node biopsy DOI: /JR Received February 8, 2010; accepted after revision pril 2, Department of Diagnostic Imaging, The Warren lpert Medical School of Brown University, Rhode Island Hospital, 593 Eddy St., Providence, RI ddress correspondence to M. B. Mainiero. 2 Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins Hospital, Baltimore, MD. 3 Department of Surgery, Rhode Island Hospital, Providence, RI. CME This article is available for CME credit. See for more information. JR 2010; 195: X/10/ merican Roentgen Ray Society xillary Ultrasound and Fine-Needle spiration in the Preoperative Evaluation of the Breast Cancer Patient: n lgorithm Based on Tumor Size and Lymph Node ppearance OBJECTIVE. The objective of our study was to evaluate the utility of ultrasound-guided fine-needle aspiration (FN) of the axillary lymph nodes in breast cancer patients depending on the size of the primary tumor and the appearance of the lymph nodes. SUBJECTS ND METHODS. Data were collected about tumor size, lymph node appearance, and the results of ultrasound-guided FN and axillary surgery of 224 patients with breast cancer undergoing 226 ultrasound-guided FN. Lymph nodes were classified as benign if the cortex was even and measured < 3 mm, indeterminate if the cortex was even but measured 3 mm or measured < 3 mm but was focally thickened, and suspicious if the cortex was focally thickened and measured 3 mm or the fatty hilum was absent. The results of ultrasound-guided FNs were analyzed by the sonographic appearance of the axillary lymph nodes and by the size of the primary tumor. The sensitivity and specificity of ultrasound-guided FN were calculated with axillary surgery as the reference standard. The sensitivity and specificity of axillary ultrasound to predict the ultrasound-guided FN result were calculated. RESULTS. Of the 224 patients, 51 patients (23%) had a positive ultrasound-guided FN result, which yields an overall sensitivity of 59% and specificity of 100%. The sensitivity of ultrasound-guided FN was 29% in patients with primary tumors 1 cm, 50% in patients with tumors > 1 to 2 cm, 69% in patients with tumors > 2 to 5 cm, and 100% in patients with tumors > 5 cm. The sensitivity of ultrasound-guided FN in patients with normalappearing lymph nodes was 11%; indeterminate lymph nodes, 44%; and suspicious lymph nodes, 93%. Sonographic characterization of lymph nodes as suspicious or indeterminate was 94% sensitive and 72% specific in predicting positive findings at ultrasound-guided FN. CONCLUSION. Ultrasound-guided FN of the axillary lymph nodes is most useful in the preoperative assessment of patients with large tumors (> 2 cm) or lymph nodes that appear abnormal. xillary lymph node staging is the most important prognostic indicator of outcome in patients with breast cancer. Historically, axillary lymph node dissection (LND) has been the reference standard for diagnosis, but sentinel lymphadenectomy has replaced LND as the primary staging procedure in many centers because sentinel lymphadenectomy is associated with less morbidity [1]. However, sentinel lymphadenectomy is technically challenging to perform, and when sentinel lymphadenectomy is positive, LND is usually performed for complete staging and local control [2, 3]. Ultrasound-guided fine-needle aspiration (FN) is a quick nonmorbid method of staging disease in the axilla. lthough percutaneous biopsy of breast lesions has largely supplanted surgery as a less costly and less invasive method of diagnosis, percutaneous evaluation of the axilla is still not routinely used in many centers despite a growing body of evidence that it is very valuable in planning the appropriate management of patients and can spare some patients a surgical procedure [4 11]. positive ultrasound-guided FN result obviates sentinel lymphadenectomy, allowing the patient to proceed directly to LND or neoadjuvant chemotherapy. Because ultrasound-guided FN is not as sensitive as sentinel lymphadenectomy, the false-negative rate of ultrasound-guided FN is too high to replace sentinel lymphadenectomy entirely and patients with negative findings at ultrasound-guided FN will still need to undergo sentinel lymphadenectomy for evaluation of the axilla. Therefore, patients who are JR:195, November

2 Mainiero et al. most likely to benefit from ultrasound-guided FN are those who are most likely to have a positive result. Prior studies have shown a clear indication for the use of the procedure in patients with large tumors, but the indications for axillary ultrasound and ultrasound-guided FN of patients with smaller tumors are less well defined [12, 13]. Some authors perform ultrasound-guided FN of all patients who are candidates for sentinel lymphadenectomy [7, 11], whereas others advocate axillary ultrasound of all patients and ultrasound-guided FN of only abnormal lymph nodes [9, 10]. The purpose of this study was to further evaluate the use of axillary ultrasound and ultrasound-guided FN in a wide range of primary breast cancer sizes, including a range of T1 tumors ( 2 cm), to better define when axillary ultrasound and ultrasoundguided FN are indicated. Subjects and Methods Study Design prospective observational study was performed of patients with newly diagnosed breast cancer referred for axillary staging with ultrasound-guided FN from March 2004 to September The standard practice at our institution at the time of the study was for patients who were candidates for sentinel lymphadenectomy to undergo ultrasound-guided FN preoperatively regardless of whether lymph nodes were suspicious clinically or sonographically. The institutional review board of the hospital approved this HIP-compliant study. There were 250 patients who gave informed consent to participate. Of these, seven had no lymph nodes visible on ultrasound and ultrasound-guided FN was therefore not performed. Of the 243 patients who underwent ultrasound-guided FN, four withdrew from the study, and 15 did not go on to axillary surgery. Of the remaining 224 patients, two patients had bilateral synchronous breast cancer and underwent bilateral ultrasound-guided FN. These 226 ultrasound-guided FN procedures in 224 patients form the basis of this study. Sonographic evaluation and ultrasound-guided FN of the axillary lymph nodes were performed by one of five radiologists specializing in breast imaging. ll radiologists participating in this study had at least 2 years experience performing ultrasoundguided FN of the axillary lymph nodes. Before ultrasound-guided FN, the radiologist performing the procedure reviewed the patient s prior imaging studies and biopsy results. The size of the primary tumor in cases presenting as masses was determined by the radiologist based on review of prior imaging. The histologic type of the primary tumor was obtained from the pathology report of prior breast biopsy. For purposes of data analysis, cases presenting as calcifications without a measurable mass or lesions diagnosed as ductal carcinoma in situ (DCIS) preoperatively were grouped with invasive breast cancers measuring 1 cm (T1a and T1b). Lymph Node Selection and Characterization The axilla was scanned using high-resolution (12-MHz electronically focused linear-array transducer) ultrasound equipment (HDI 5000, Philips Healthcare Ultrasound). The radiologist performing the ultrasound-guided FN selected which lymph node to aspirate. The most suspicious node was selected for ultrasound-guided FN. Suspicious features were cortical thickening, especially if thickening was focal, and the absence of the fatty hilum. If all the lymph nodes appeared similar or normal, the lymph node that was lowest in the axilla was selected for ultrasoundguided FN because it was considered to most likely be the sentinel node. Before ultrasound-guided FN, the cortex of the selected lymph node was measured. The measurement was taken from the thickest portion of the cortex. The radiologist performing the procedure also prospectively characterized the cortical morphologic features of the lymph node to be aspirated. The presence or absence of the fatty hilum was noted, and the cortex was characterized as being even or focally thickened. Ultrasound-Guided Fine-Needle spiration Procedure Informed consent was obtained for each procedure. While the patient was under local anesthesia, a 22-gauge needle attached to a 10-mL syringe was used to obtain specimens for cytologic examination. The routine practice at our institution is to obtain three samples from the selected lymph node while targeting the thickest portion of the cortex. The aspirate was placed in CytoLyt solution (Cytyc) and sent to a cytology laboratory where it was processed with the ThinPrep system (Cytyc) and examined by a cytologist. Cytology results were reported as satisfactory for cytologic evaluation, negative for malignancy; satisfactory for cytologic evaluation, positive for malignancy; or insufficient for diagnosis. In our practice, patients with an ultrasound-guided FN result of insufficient for diagnosis are managed as if the result were negative, and a repeat ultrasoundguided FN is not performed unless the lymph node is suspicious in sonographic appearance. There were no procedural complications. Pathology reports from sentinel lymphadenectomy and LND procedures were reviewed and were considered positive when one or more lymph nodes were reported as positive on histologic examination. Data nalysis Lymph nodes with an even cortex measuring < 3 mm were characterized as benign (Fig. 1). Lymph nodes with either an even cortex measuring 3 mm (Fig. 2) or with focal cortical thickening but with a cortical thickness measurement of < 3 mm (Fig. 2B) were considered indeterminate, and lymph nodes with focal cortical thickening measuring > 3 mm (Fig. 3) or with a completely absent fatty hilum (Fig. 3B) were considered suspicious for metastatic disease. The cortical thickness of nodes without a fatty hilum was measured as half the short axis of the node. The final pathology results from sentinel lymphadenectomy or LND were correlated with ultrasound-guided FN cytology results. Because patients with an insufficient ultrasound-guided FN result were not spared sentinel node biopsy and were managed as if the results were negative in all cases in this series, a cytology result of insufficient for diagnosis was considered negative for the purpose of data analysis. The sensitivity and specificity of ultrasound-guided FN were calculated by primary tumor size. The results are presented according to primary tumor size and axillary sonographic findings. The sensitivity and specificity of cortical thickness and combined cortical thickness and morphologic lymph node features in predicting a positive ultrasound-guided FN result were also calculated. Results Patient and Primary Tumor Characteristics The mean age of the patients in the study group, two men and 222 women, was 56 years (range, years). There were 204 cancers presenting as masses and 22 presenting as calcifications. The mean primary breast cancer tumor size for cases presenting as masses was 1.89 cm, with a median size of 1.5 cm (range, cm). There were 191 invasive ductal carcinomas, 16 invasive lobular carcinomas, 13 with mixed invasive ductal and lobular carcinoma, and two invasive papillary carcinomas. DCIS was detected on percutaneous biopsy in four patients, all of whom were suspected of having invasive carcinoma on the basis of imaging or pathologic findings and who underwent sentinel lymphadenectomy. One had a spiculated mass on mammography and three had extensive microcalcifications and were undergoing mastectomy. Surgical Findings Of the 226 axillae included in this study, 87 (38%) were positive for metastatic disease; ultrasound-guided FN identified 51 (59%) of these cases preoperatively. Twen JR:195, November 2010

3 Ultrasound-Guided FN in Breast Cancer Patients Fig year-old healthy woman with breast cancer., Ultrasound image of normal lymph node (arrows) with even cortex. B, Ultrasound image of same node with calipers measuring thickest portion of lymph node. Cortical thickness measured < 3 mm. ty-seven patients with a positive ultrasoundguided FN result had chemotherapy before LND. Of these patients, nine had no evidence of metastatic disease at LND. These nine patients were counted as having a truepositive ultrasound-guided FN result, because the negative LND result was considered to be a response to chemotherapy. There were no cases with a false-positive ultrasound-guided FN result. Ultrasound-Guided Fine-Needle spiration Results Of the 226 ultrasound-guided FN procedures, 161 (71%) were negative for malignancy, 51 (23%) were positive for malignancy, and 14 (6%) were insufficient for cytologic evaluation. ll of the insufficient results were in either sonographically benign-appearing nodes (12/14) or indeterminate nodes (2/14). There were no suspicious nodes with a cytology result of insufficient for diagnosis. The results of ultrasound-guided FN are shown by the size of the primary tumor and B Fig. 2 Ultrasound images showing indeterminate findings for lymph nodes., Indeterminate lymph node (arrows) with even cortex that measures 3 mm in 69-year-old man/woman with breast cancer. B, Indeterminate lymph node (arrows) with focal area of cortical thickening (arrowhead) that measures < 3 mm in 72-year-old man/woman with breast cancer. B JR:195, November

4 Mainiero et al. Fig. 3 Ultrasound images showing suspicious findings for lymph nodes., Suspicious lymph node (arrows) with focal cortical thickening measuring 3 mm in 55-year-old man/woman with breast cancer.. Cursors = focally thickened cortex. B, Suspicious lymph node (arrows) with absent fatty hilum in 42-year-old man/woman with breast cancer. the appearance of the aspirated lymph node in Table 1. Of the ultrasound-guided FN results, 51 (23%) of 226 were true-positive; 139 (62%), true-negative; 36 (16%), false-negative; and zero (0%), false-positive. The sensitivity of ultrasound-guided FN to detect metastatic disease in the axilla using surgical pathology results as the reference standard increased with increasing primary tumor size and prevalence of metastatic disease in the axilla (Table 2). The sensitivity of ultrasoundguided FN was highest (93%) in lymph nodes with suspicious morphologic features (Table 3). If both suspicious and indeterminate lymph nodes are included, the sensitivity of ultrasound-guided FN was 80%. The sonographic feature most predictive of a positive ultrasound-guided FN result was the absence of a fatty hilum, but this finding was not a common one. The fatty hilum of the aspirated lymph node was absent in 15 of the 226 axillae (7%), and all 15 (100%) were positive for malignancy on ultrasound-guided FN. ll of these lymph nodes had a cortical thickness, which was measured as half the short axis, of > 3 mm. The positive ultrasoundguided FN rate for all suspicious nodes was 41 of 58 (71%). There were 24 lymph nodes considered indeterminate because the cortex was even and measured 3 mm, four (17%) of which were positive at ultrasound-guided FN. Fifteen lymph nodes were considered indeterminate because the cortex was focally thickened cortex and measured < 3 mm, three (20%) of which were positive at ultrasoundguided FN. The use of a cortical thickness measurement of 3 mm as an indication for ultrasound-guided FN was 88% sensitive and 75% specific in predicting a positive ultrasound-guided FN result. If morphologic criteria are used in addition to cortical thick- TBLE 1: Results of Ultrasound-Guided Fine-Needle spiration (FN) by Size of Primary Tumor and Characteristics of Lymph Nodes on Ultrasound Size of Primary Tumor Ultrasound-Guided FN Benign Lymph Node a Indeterminate Lymph Node b Suspicious Lymph Node c Total No. (%) With Positive FN No. (%) With Positive FN No. With (%) of Positive FN No. With (%) of Positive FN T0, T1a, T1b 59 1 (2) 16 1 (6) 8 3 (38) 83 5 (6) T1c 45 0 (0) 12 0 (0) (72) (17) T (4) 8 3 (38) (75) (42) T3, T4 1 1 (100) 3 3 (100) 4 4 (100) 8 8 (100) Total (2) 39 7 (18) (71) (23) a Node has an even cortex that measures < 3 mm. b Node has an even cortex that measures 3 mm or has a focally thickened cortex that measures < 3 mm. c Node has a focally thickened cortex that measures 3 mm or fatty hilum is absent. B 1264 JR:195, November 2010

5 Ultrasound-Guided FN in Breast Cancer Patients Fig. 4 lgorithm for use of axillary ultrasound and ultrasound-guided fineneedle aspiration (FN) in preoperative evaluation of patient with recently diagnosed breast cancer. T1a and T1b Normal node (Even cortex < 3 mm) ness that is, if focal cortical thickening is used as an indication for ultrasound-guided FN regardless of measurement, the sensitivity and specificity of predicting a positive ultrasound-guided FN result were 94% and 72%, respectively. Discussion lthough axillary ultrasound and ultrasound-guided FN have the potential to spare patients surgery by identifying many patients with metastatic disease preoperatively, the procedure is not yet a routine part of practice and the indications have not been clearly established. The merican College of Radiology Practice Guidelines [14] state that evaluation of the axilla for occult lymph node metastasis in patients with newly diagnosed breast cancer is an area of research. In particular, the role of the procedure in patients with small tumors has not been extensively evaluated. In a prior study of T1 ( 2 cm) cancers and sonographically normal-appearing lymph nodes, Kuenen-Boumeester et al. [7] recommended that ultrasound-guided FN be included in the preoperative staging of all primary breast cancer patients. Koelliker et al. [11] found ultrasound-guided FN to be beneficial in a selected population of patients with T1 tumors, including one with normal-appearing lymph nodes, but they recommended a prospective study including a larger range of T1 tumors to establish the indications in this group. T1c or larger xillary ultrasound Sentinel lymph node biopsy Suspicious or indeterminate node or Neoadjuvant chemotherapy planned Ultrasound-guided FN Negative Positive xillary lymph node dissection The characterization of axillary lymph nodes by sonography has also evolved in recent years. cortical thickness of 3 mm has been shown to be the most useful predictor of malignancy in clinical practice [8, 15], although the results of an in vitro study by Bedi et al. [16] suggest that focal cortical thickening is most predictive of malignancy. In most prior studies, researchers have selected patients for ultrasound-guided FN on the basis of the subjective morphologic features of the axillary nodes. Given recent evidence that both the cortical thickness measurement and the presence or absence of cortical thickening are important features to predict malignancy, we used a combination of these features to assign the level of suspicion for metastatic disease by axillary ultrasound. The size of the axillary lymph nodes has limited utility for determining the likelihood of metastatic disease [11] and was therefore not used as a criterion. Deciding which patients should undergo axillary ultrasound and ultrasound-guided FN depends on if one is trying to maximize the likelihood of a positive result or if one is trying to optimize the percentage of patients spared sentinel lymphadenectomy and is therefore willing to accept a higher percentage of negative ultrasound-guided FN results. To maximize the percentage of ultrasound-guided FN that are positive, one should select only the most abnormalappearing axillary lymph nodes. To maximize the number of patients spared sentinel lymphadenectomy, however, one should perform ultrasound-guided FN in breast cancer patients with small tumors and nodes that appear less suspicious. TBLE 2: Sensitivity of xillary Ultrasound-Guided Fine-Needle spiration (FN) to Diagnose Metastatic Disease ccording to the Size of the Primary Breast Tumor Size of Primary Tumor TBLE 3: Sensitivity of xillary Ultrasound-Guided Fine-Needle spiration (FN) to Detect Metastatic Disease ccording to the ppearance of xillary Lymph Nodes at Ultrasound Ultrasound Findings No. of xillary Nodes No. of xillary Nodes No. (%) of xillary Nodes With Positive Findings for Metastatic Disease at Ultrasound-Guided FN No. (%) of xillary Nodes With Positive Findings for Metastatic Disease Ultrasound-Guided FN Surgery Surgery Sensitivity (%) T0, T1a, T1b 83 5 (6) 17 (20) 29 T1c (17) 26 (35) 50 T (42) 36 (60) 69 T3, T4 8 8 (100) 8 (100) 100 Total (23) 87 (38) 59 Sensitivity (%) Benign node (2) 27 (21) 11 Indeterminate node 39 7 (18) 16 (41) 44 Suspicious node (71) 44 (76) 93 Total (23) 87 (38) 59 JR:195, November

6 Mainiero et al. Because ultrasound-guided FN is fast, inexpensive, and not associated with any significant morbidity, we chose to optimize detection of as many positive axillae as possible preoperatively by including all patients for ultrasound-guided FN regardless of primary tumor size or axillary lymph node sonographic appearance. Our results, however, show that the yield of a positive ultrasoundguided FN result that spared the patient sentinel lymphadenectomy was only 6% in patients with small tumors ( 1 cm). Therefore, despite the ease and lack of morbidity associated with the procedure, we believe that the likelihood of sparing a patient from undergoing sentinel lymphadenectomy is too low to justify routine ultrasound-guided FN in this population. Both benign and indeterminate lymph nodes were very unlikely to be positive at ultrasound-guided FN in this population, although if the axillary lymph node was suspicious in appearance on ultrasound, then the rate of a positive ultrasound-guided FN was 38%. Therefore, if one performs axillary ultrasound in this population, ultrasound-guided FN is indicated if the axillary lymph nodes appear suspicious. However, because only 10% of the patients in this study with tumors measuring 1 cm on imaging had a suspicious node on ultrasound, we suggest that routine axillary ultrasound in this patient population is low yield and that it is reasonable for these patients to proceed directly to sentinel lymphadenectomy. With increasing primary tumor size, we found the benefit of ultrasound and ultrasound-guided FN to increase. Overall, sentinel lymphadenectomy was spared in 17% of patients with T1c tumors (> 1 to 2 cm), all of whom had suspicious-appearing lymph nodes on ultrasound. We believe that this yield is high enough to warrant routine axillary ultrasound with ultrasound-guided FN of abnormal-appearing lymph nodes in this patient population. With tumors that were 2 5 cm, 42% of the patients were spared sentinel lymphadenectomy by a positive ultrasound-guided FN result, confirming that axillary ultrasound and ultrasound-guided FN are indicated in this patient population. With tumors > 2 cm and especially tumors > 5 cm, there were more indeterminate and normalappearing nodes that were positive for malignancy on ultrasound-guided FN. In this group of patients, our positive ultrasoundguided FN rate in normal-appearing nodes was 8% (2/25). Therefore, we perform ultrasound-guided FN in this population even if the lymph nodes appear normal if the patient is being considered for neoadjuvant chemotherapy. Our algorithm for axillary ultrasound and ultrasound-guided FN is presented in Figure 4. Our study confirms that 3 mm is a useful criterion for deciding whether a lymph node is suspicious enough to warrant ultrasoundguided FN, with a high sensitivity and specificity in predicting ultrasound-guided FN results. Combining the 3-mm cortical thickness threshold and the presence of cortical thickening, as we did in our categorization of suspicious, indeterminate, and benign nodes, has a higher sensitivity but a lower specificity than using cortical thickness alone. That is, a few more positive axillae will be detected if lymph nodes with focal cortical thickening of < 3 mm are aspirated but at the expense of a few more negative ultrasound-guided FN procedures. Therefore, we have chosen to include indeterminate lymph nodes with a cortical thickness of < 3 mm but with focal cortical thickening as an indication for ultrasound-guided FN to maximize the number of patients spared sentinel lymphadenectomy. Institutions that do not have adequate cytology support may choose to use ultrasoundguided core biopsy of lymph nodes rather than ultrasound-guided FN for the diagnosis of metastatic disease. Core biopsy will also have false-negatives in cases with small metastatic deposits and, like ultrasound-guided FN, does not obviate sentinel lymphadenectomy when negative [17, 18]. In addition, the sensitivity of ultrasound-guided FN is similar to that of core biopsy [19]. We have found that the most operator-dependent portion of ultrasoundguided FN is in identifying the most suspicious lymph node and that the FN technique itself is easily performed, is less expensive than core biopsy, and is exceedingly well tolerated by patients. Unlike in the breast where there are myriad benign and malignant pathology results and histology is crucial in making an accurate diagnosis, a cytology result of positive for metastatic adenocarcinoma in the axilla is sufficient to change the patient s management and obviate sentinel lymphadenectomy. One limitation of this study is that patient selection was based on the choice of the surgeon to refer the patient for ultrasound-guided FN at the time of study accrual, which may have introduced selection bias. In addition, the size of the primary tumor was based on preoperative imaging assessment and may not have reflected the size at pathologic staging. However, we chose this method because this is the information that is available in clinical practice and will be used to guide patient management decisions preoperatively. lso, we do not have cost data, which are needed to determine the cost-effectiveness of ultrasound-guided FN in sparing sentinel lymphadenectomy depending on tumor size or the appearance of the axillary lymph nodes. Further study with cost data would be useful in confirming our algorithm for the use of axillary ultrasound and ultrasound-guided FN in the preoperative assessment of breast cancer patients. In conclusion, using axillary ultrasound and selective ultrasound-guided FN is a rapid, nonmorbid method of staging the axilla in newly diagnosed breast cancer patients and should become a routine part of patient care because it will spare many patients, particularly those with larger primary tumors, from undergoing sentinel lymphadenectomy. xillary ultrasound and axillary ultrasound-guided FN are of low yield in patients with tumors 1 cm. We recommend axillary ultrasound in patients with tumors > 1 cm and ultrasound-guided FN in patients with lymph nodes that have indeterminate or suspicious features. In addition, ultrasoundguided FN should be considered in patients with locally advanced breast cancer for whom neoadjuvant chemotherapy is planned even if the lymph nodes appear normal. cknowledgments We thank Diane Romano, Susan Foley, and Wendy Smith for their assistance with data collection. References 1. Purushotham D, Upponi S, Klevesath MB, et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol 2005; 23: Cox CE, Salud CJ, Cantor, et al. Learning curves for breast cancer sentinel lymph node mapping based on surgical volume analysis. J m Coll Surg 2001; 193: Chen SL, Iddings DM, Scheri RP, Bilchik J. Lymphatic mapping and sentinel node analysis: current concepts and applications. C Cancer J Clin 2006; 56: Bonnema J, van Geel N, van Ooijen B, et al. Ultrasound-guided aspiration biopsy for detection of nonpalpable axillary node metastases in breast cancer patients: new diagnostic method. World J Surg 1997; 21: de Kanter Y, van Eijck CH, van Geel N, et al JR:195, November 2010

7 Ultrasound-Guided FN in Breast Cancer Patients Multicentre study of ultrasonographically guided axillary node biopsy in patients with breast cancer. Br J Surg 1999; 86: Krishnamurthy S, Sneige N, Bedi DG, et al. Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma. Cancer 2002; 95: Kuenen-Boumeester V, Menke-Pluymers M, de Kanter Y, Obdeijn IM, Urich D, Van Der Kwast TH. Ultrasound-guided fine needle aspiration cytology of axillary lymph nodes in breast cancer patients: a preoperative staging procedure. Eur J Cancer 2003; 39: Deurloo EE, Tanis PJ, Gilhuijs KG, et al. Reduction in the number of sentinel lymph node procedures by preoperative ultra-sonography of the axilla in breast cancer. Eur J Cancer 2003; 39: van Rijk MC, Deurloo EE, Nieweg OE, et al. Ultrasonography and fine-needle aspiration cytology can spare breast cancer patients unnecessary sentinel lymph node biopsy. nn Surg Oncol 2006; 13: Sapino, Cassoni P, Zanon E, et al. Ultrasonographically-guided fine-needle aspiration of axillary lymph nodes: role in breast cancer management. Br J Cancer 2003; 88: Koelliker SL, Chung M, Mainiero MB, Steinhoff MM, Cady B. xillary lymph nodes: USguided fine-needle aspiration for initial staging of breast cancer correlation with primary tumor size. Radiology 2008; 246: Oruwari JU, Chung M, Koelliker S, Steinhoff MM, Cady B. xillary staging using ultrasoundguided fine needle aspiration biopsy in locally advanced breast cancer. m J Surg 2002; 184: Somasundar P, Gass J, Steinhoff M, et al. Role of ultrasound-guided axillary fine-needle aspiration in the management of invasive breast cancer. m J Surg 2006; 192: merican College of Radiology Website. CR practice guideline for the performance of a breast ultrasound examination. Revised SecondaryMainMenuCategories/quality_safety/ guidelines/breast/us_breast.aspx. ccessed February 1, Choi YJ, Ko EY, Han BK, Shin JH, Kang SS, Hahn SY. High-resolution ultrasonographic features of axillary lymph node metastasis in patients with breast cancer. Breast 2009; 18: Bedi DG, Krishnamurthy R, Krishnamurthy S, et al. Cortical morphologic features of axillary lymph nodes as a predictor of metastasis in breast cancer: in vitro sonographic study. JR 2008; 191: be H, Schmidt R, Kulkarni K, Sennet C, Mueller JS, Newstead GM. xillary lymph nodes suspicious for breast cancer metastasis: sampling with US-guided 14-gauge core-needle biopsy clinical experience in 100 patients. Radiology 2009; 250: Damera, Evans J, Cornford EJ, et al. Diagnosis of axillary nodal metastases by ultrasoundguided core biopsy in primary operable breast cancer. Br J Cancer 2003; 89: Rao R, Lilley L, ndrews V, Radford L, Ulissey M. xillary staging by percutaneous biopsy: sensitivity of fine-needle aspiration versus core needle biopsy. nn Surg Oncol 2009; 16: FOR YOUR INFORMTION This article is available for CME credit. See for more information. JR:195, November