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Phyllodes Tumor Diagnosed after Ultrasound-Guided Vacuum-Assisted Excision: Should It Be Followed by Surgical Excision?
Ultrasound in Med. & Biol., Vol. 41, No. 3, pp. 741–747, 2015 Copyright Ó 2015 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
http://dx.doi.org/10.1016/j.ultrasmedbio.2014.11.004
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Original Contribution PHYLLODES TUMOR DIAGNOSED AFTER ULTRASOUND-GUIDED VACUUM-ASSISTED EXCISION: SHOULD IT BE FOLLOWED BY SURGICAL EXCISION? JI HYUN YOUK,* HANA KIM,* EUN-KYUNG KIM,y EUN JU SON,* MIN JUNG KIM,y and JEONG-AH KIM* * Department of Radiology, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea; and y Department of Radiology, Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea (Received 8 June 2014; revised 24 October 2014; in final form 8 November 2014)
Abstract—Our aim was to retrospectively evaluate the results of ultrasound (US)-guided vacuum-assisted excision (US-VAE) of phyllodes tumors (PTs). A total of 41 PTs diagnosed at US-VAE followed by surgery (n 5 27) or at least 2 y of US monitoring (n 5 14) were included. By comparison of US-VAE pathology with surgical histology or follow-up US results, cases were divided into upgraded (malignant) and non-upgraded (benign) groups. These two groups were compared with respect to clinical, procedural and US features. Among 27 surgical cases, 2 (8.7%) of 23 benign PTs were upgraded to malignant PTs. The Breast Imaging Reporting and Data System category was retrospectively assigned as 4a (50%) or 4b (50%) in the upgraded group (n 5 2) and 3 (64%) or 4a (36%) in the non-upgraded group (n 5 39) (p 5 0.018). Residual tumor was observed at the site of US-VAE in 15 of 27 surgical cases and 0 of 14 US follow-up cases (36.6%, 15/41). Given the rates of upgrade to malignancy (8.7%) and residual tumor (36.6%), PTs diagnosed after US-VAE should be surgically excised. (E-mail: [email protected]) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: Breast neoplasms, Phyllodes tumor, Interventional ultrasonography, Large-core needle biopsy.
Although the pre-operative diagnosis of PT can be essential in establishing the most appropriate therapeutic approach, the differential diagnosis of PT from fibroadenoma remains clinically and radiologically challenging. For breast lesions that are suspected to be clinically benign or concordant benign after core needle biopsy (CNB), conservative management—close follow-up—is widely accepted (Jiang et al. 2013; Youk et al. 2007). However, some patients may prefer complete excision of these lesions because of the psychological stress and physical discomfort from pain, lumps and discharges (Fine et al. 2002; Jiang et al. 2013; Li et al. 2013). Ultrasound-guided vacuum-assisted excision (US-VAE) is being increasingly performed as an alternative to surgical excision for selected clinically benign breast masses such as fibroadenomas or for a concordant benign result after CNB. Because of the difficulty involved in differentiating fibroadenoma from PT, the resulting pathologic diagnosis of PT could be expected in clinical practice after US-VAE of a clinically suspected benign breast mass (Gatta et al. 2011; Park et al. 2012). However, there has been no report on the management of PTs
INTRODUCTION Breast phyllodes tumor (PT) is a rare neoplasm of the breast that accounts for 0.3%–1.0% of primary breast tumors of the breast (Ben Hassouna et al. 2006; Lakhani et al. 2012). Histopathologically, PTs are classified into more specific categories such as benign, borderline and malignant, based on a combination of histologic features including degree of stromal hypercellularity, mitoses and cytologic atypia, stromal overgrowth and nature of the tumor borders/margins. Local recurrence can occur in all subtypes of PT, although the recurrence rate is low for benign tumors; rates range from 10%– 17%, from 14%–25% and from 23%–30% for benign, borderline and malignant PTs, respectively (Lakhani et al. 2012). To minimize recurrence, wide local excision with at least a 1-cm negative resection margin has been recommended as the treatment of choice (Jang et al. 2012).
Address correspondence to: Ji Hyun Youk, Department of Radiology, Gangnam Severance Hospital, 211, Eonju-ro, Gangnam-Gu, Seoul 135-720, South Korea. E-mail: [email protected] 741
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diagnosed as clinically benign breast masses after USVAE. Therefore, the present study was performed to retrospectively evaluate the results for PTs diagnosed as clinically benign breast masses after US-VAE. METHODS The present retrospective study was conducted with institutional review board approval; patient informed consent was waived. Patients After review of the pathologic results of US-VAEs performed from January 2002 through October 2012 at two hospitals, we identified 57 PTs that were diagnosed. Among these cases, 41 PTs in 41 women aged 18–53 y (mean 6 standard deviation: 31.7 6 9.9 y) who underwent follow-up surgical excision (n 5 27) or at least 2 y of US follow-up (n 5 14) after US-VAE were retrospectively reviewed (Fig. 1). CNB was performed before VAE for 10 PTs, but failed to diagnose PT. The remaining 16 cases were excluded from analyses because there was no surgical excision with ,2 y of US follow-up (n 5 11) or no follow-up (n 5 5) (Fig. 1). US examination and US-VAE Ultrasound examination and US-VAE were performed by one of eight radiologists with 4–10 y of experience in breast imaging and US-VAE using high-resolution US units with linear-array transducers of 5–10, 5–12, or 4–15 MHz (HDI 5000, Philips Advanced Technology Laboratories, Bothell, WA; Logic 9, GE Medical Systems, Milwaukee, WI; iU22, Philips Medical Systems, Bothell, WA, USA; or SuperSonic Imagine, Aix-en-Provence, France). By means of a vacuum-assisted device (Mammotome, Ethicon-Endosurgery, Cincinnati, OH, USA) with an 8- or 11-gauge probe under the guidance of a high-resolution US unit mentioned above, the US-VAE procedure was performed as described by Kim et al.
Fig. 1. Flowchart of patient enrollment. Asterisks indicate enrolled cases. US 5 ultrasound.
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(2008). After administration of local anesthesia, the probe was inserted into the breast through a small skin incision and guided into biopsy position under direct US visualization. Multiple core samples were taken until the mass was completely removed, as determined by real-time US of the biopsy site. Forced scan pressure to disperse air artifacts and multidirectional US images, such as views perpendicular to the biopsy needle, were used to visualize the residual mass. For any breast mass larger than 1.0 cm at US, we used US-VAE with an 8-gauge probe. To ensure complete removal of the mass during US-VAE, we removed breast tissue surrounding the mass at approximately four more sampling sites (12, 3, 6 and 9 o’clock directions). Depending on the physician’s and patient’s preferences, wide excision or follow-up US was performed for management of PTs diagnosed after US-VAE at our institution. Data and statistical analysis Medical records were reviewed for clinical features (patient age and palpable mass) and US-VAE procedural characteristics (size of probe used [8 or 11 gauge], number of core specimens per lesion, residual PT at surgery). To collect the pre-VAE lesion size (longest dimension of the lesion at US), US variables based on the Breast Imaging Reporting and Data System (BIRADS; shape, margin, orientation, echo pattern, orientation and posterior acoustic feature) and BI-RADS final assessment categories indicating the probability of malignancy in categories 3, 4a, 4b, 4c and 5 (American College of Radiology 2003), each US image obtained before US-VAE was reviewed retrospectively in consensus by two radiologists with 4 and 10 y of experience in breast imaging, respectively, who knew that cases were PTs diagnosed at US-VAE, but were blinded to the benign, borderline and malignant grading and surgical histology. All 41 PTs diagnosed at US-VAE were divided into two groups, upgraded and non-upgraded, after review of the surgical or US follow-up results. The non-upgraded group comprised those PTs for which there was no residual sonographic abnormality at follow-up US or for which the surgical histology was the same as US-VAE pathology, the tumor had been completely excised without residual lesion or the tumor was another benign lesion (e.g., fibroadenoma, fibrocystic change, fibroadenomatous hyperplasia). The upgraded group comprised those PTs for which the surgical histology indicated a higher grade compared with US-VAE histology. If there was no evidence of residual tumor in the surgical results, the tumor was considered to be non-upgraded. Differences in clinical presentations, procedural characteristics and US findings between the two groups were evaluated. For the 14 PTs that were not excised surgically but followed
Should surgery follow US-guided vacuum-assisted excision? d J. H. YOUK et al.
Table 1. Results for 27 phyllodes tumors that were diagnosed at ultrasound-guided vacuum-assisted excision and then surgically excised Diagnosis at surgical excision after US-VAE
Benign Borderline Malignant Total
Benign
Borderline
Malignant
Total
21* 0 0 21 (77.8%)
0 3* 0 3 (11.1%)
2 0 1* 3 (11.1%)
23 (85.2%) 3 (11.1%) 1 (3.7%) 27 (100%)
US-VAE 5 ultrasound-guided vacuum-assisted excision. * Nine benign, two borderline and one malignant phyllodes tumor exhibited no residual tumor after surgery.
up with US, the presence of residual sonographic abnormalities was determined by reviewing each US image obtained before, during and after US-VAE. On followup US, mild distortion at the site of US-VAE was considered to be a post-VAE change, whereas a spaceoccupying mass was considered to be a residue. When a residual PT was described in the surgical pathology report, it was also considered to be a residue. Statistical comparisons were performed using the c2-test or Fisher exact test for categorical variables and the Mann–Whitney U-test for continuous variables. All statistical analyses were performed with SPSS statistical software (Version 20.0.0, IBM, Armonk, NY, USA). Differences were considered to be statistically significant at a p-value , 0.05. RESULTS Of the 41 PTs diagnosed after US-VAE, 37 (90.2%) were benign, 3 (7.3%) were borderline and 1 (2.4%) was malignant. Pre-VAE lesion size ranged from 8–35 mm (mean 6 standard deviation: 21.3 6 6.8 mm), and the number of core samples ranged from 6–72 (28.6 6 14.0). All 14 cases with at least 2
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y of US follow-up (57.1 6 34.2 mo, range: 25–133 mo) were benign PTs. The pathologic details for 27 PTs that were excised surgically after US-VAE (82.3 6 107.1 d, range: 13–407 d) are summarized in Table 1. Of 23 PTs diagnosed as benign at US-VAE, 2 (8.7%) were upgraded to malignant at final surgical excision (Fig. 2). All three borderline PTs and one malignant PT at US-VAE were not upgraded at final surgical excision. The rate of concordance of PT grade between US-VAE and surgical excision was 92.6%. Among the remaining 14 benign PTs with at least 2 y of US follow-up, there were no recurrences. Accordingly, 39 cases (95.1%) were not upgraded and 2 cases (4.9%) were upgraded after surgical excision or US follow-up. Table 2 summarizes the clinical, procedural and US features of the 41 PTs by group, upgraded or nonupgraded. There was no significant difference in clinical and procedural characteristics between the two groups. With respect to US features, the BI-RADS final assessment category significantly differed between the two groups (p 5 0.018). No PTs in the upgraded group were assessed as category 3, and no PTs in the nonupgraded group were assessed as category 4b. There were no significant differences in other US features between the two groups. Of 14 benign PTs followed up with US for at least 2 y, no residual abnormality was visible. Among 27 PTs that were excised surgically, however, residual tumor was found at the site of US-VAE in 15 (55.6%; 12 benign, 1 borderline and 2 malignant at US-VAE) (Fig. 3). In total, 15 of 41 PTs (36.6%) diagnosed after US-VAE exhibited residual tumor. DISCUSSION Ultrasound-guided CNB is an accurate method for the histologic diagnosis of breast masses that are visible
Fig. 2. Transverse (left) and longitudinal (right) US images of the left breast of a 45-y-old woman revealed a 20-mm oval hypo-echoic mass, which was classified as BI-RADS category 4b. The diagnosis based on US-VAE was benign phyllodes tumor. On surgical excision, the diagnosis was upgraded to malignant phyllodes tumor. BI-RADS 5 Breast Imaging Reporting and Data System; US 5 ultrasound; US-VAE 5 US-guided vacuum-assisted excision.
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Table 2. Clinical and ultrasound features of 41 phyllodes tumors diagnosed at US-VAE followed by surgical excision or at least 2 y of follow-up ultrasound
Clinical findings Age (y) Palpability Yes No Needle gauge 8 11 Number of core samples Residual tumor Yes No Ultrasound findings Lesion size (mm) Shape Oval Round Margin Circumscribed Microlobulated Angular Indistinct Echo pattern Hypo-echoic Complex Orientation Parallel Non-parallel Posterior acoustic feature None Enhancement BI-RADS category 3 4a 4b
Non-upgraded* (n 5 39)
Upgraded* (n 5 2)
p-value
31.0 6 9.6 (28, 18–53)y
45.5 6 0.7 (45.5, 45–46)y
0.090 .0.99
27 (69.2%) 12 (30.8%) 33 (84.6%) 6 (15.4%) 27.4 6 12.9 (26, 6–72)y 13 (52.0%) 12 (48.0%) 21.0 6 6.7 (19, 8–35)y
2 (100.0%) 0 (0%)
.0.99
2 (100.0%) 0 (0%) 51.5 6 19.1 (51.5, 38–65)y
0.053
2 (100%) 0 (0%) 27.0 6 9.9 (27, 20–34)y
37 (94.9%) 2 (5.1%)
2 (100.0%) 0 (0.0%)
18 (46.2%) 14 (35.9%) 2 (5.1%) 5 (12.8%)
0 (0.0%) 2 (100.0%) 0 (0.0%) 0 (0.0%)
38 (96.0%) 1 (4.0%)
2 (100.0%) 0 (0%)
38 (97.4%) 1 (2.6%)
2 (100.0%) 0 (0.0%)
16 (41.0%) 23 (59.0%)
1 (50.0%) 1 (50.0%)
25 (64.1%) 14 (35.9%) 0 (0%)
0 (0.0%) 1 (50.0%) 1 (50.0%)
0.487 0.235 .0.99 0.462
.0.99 .0.99 .0.99 0.018
US-VAE 5 US-guided vacuum-assisted excision. * Classified as non-upgraded or upgraded by correlating US-VAE pathology with the surgical or US follow-up results. y Mean 6 standard deviation (median, range).
on US. However, the possibility of histologic underestimation or false-negative results is an inherent weakness of this technique (Schueller et al. 2008; Youk et al. 2010). Specifically, the differential diagnosis of PT from fibroadenoma in CNB is difficult. PTs are
differentiated from fibroadenomas principally by their stroma, which is hypercellular; they also have leaf-like projections into the stroma. However, because of the intratumoral heterogeneity of PTs, with some areas having the appearance of fibroadenoma, the degree of cellularity
Fig. 3. Transverse (left) and longitudinal (right) US images of the left breast of a 38-y-old woman revealed a 25-mm oval hypo-echoic mass, which was classified as BI-RADS category 3. The diagnosis based on US-VAE was benign phyllodes tumor. Surgical excision revealed residual benign phyllodes tumor at the site of VAE. BI-RADS 5 Breast Imaging Reporting and Data System; US 5 ultrasound; US-VAE 5 US-guided vacuum-assisted excision.
Should surgery follow US-guided vacuum-assisted excision? d J. H. YOUK et al.
may not be high enough to diagnose PTs and leaf-like projections may be hard to detect on CNB. Similarly, the grading of PTs as benign, borderline or malignant relies on such indices as degree of atypia, number of stromal mitoses per high-power field, nuclear size and pleomorphism, necrosis and infiltrative or pushing margins, which have not been proven sufficiently reliable to allow pathologists to make a definitive diagnosis on CNB (Dillon et al. 2006). The false-negative rate of CNB for PTs ranged from 8%–39% (mean: 20.5%) in previous studies (Bode et al. 2007; Choi and Koo 2012; Dillon et al. 2006; Foxcroft et al. 2007; Gatta et al. 2011; Komenaka et al. 2003; Tsang et al. 2011; Youn et al. 2013). The rate of concordance of PT grade between CNB and surgery was 61.2% (38.5% for benign PTs and 74.7% for borderline or malignant PTs) (Choi and Koo 2012). Compared with spring-loaded devices for CNB, vacuum-assisted devices provide larger specimens with more contiguous sampling, resulting in more accurate pathology results and fewer disease upgrades at the time of surgery (Bassett et al. 2007; Hahn et al. 2012; Youk et al. 2012). For PTs diagnosed after US-VAE, however, additional surgical excision can be an issue when considering the difficulty in diagnosis and the recurrence related to residual PT. The rate of concordance of PT grade between US-VAE and surgery was 92.6% (91.3% in benign and 100% in borderline and malignant PTs) in our study. In two previous studies, the rates of concordance of grade between CNB and surgery were lower than those in our study: 61.2% (38.5% in benign PTs and 74.7% in borderline or malignant PTs) (Choi and Koo 2012) and 83.3% (82.1% in benign PTs and 100% in borderline or malignant PTs) (Youn et al. 2013). A trend toward higher concordance on borderline or malignant subtypes than the benign subtype was observed, and there was no downgrade of borderline or malignant subtypes after surgical excision, as in our results. Although there are limitations in predicting PT grade, particularly on the basis of CNB, the diagnosis of borderline or malignant PT after US-VAE may warrant subsequent wide excision or mastectomy. With respect to benign PTs, 8.7% (2 of 23) were upgraded to malignant PTs in our study. In the previous study, there was no upgrading for 31 benign PTs with at least 2 y of US follow-up after US-VAE (Park et al. 2012). Possibly the results differ because of the small number of benign PTs diagnosed in our study, the lack of surgical excisions in the previous study and differences in study populations. Although US-VAE continued until all US evidence of the mass was completely removed, with larger sampling including the surrounding tissue, in the present study, US-VAE could have failed to sample and diagnose malignant tumor in residual tissue. However, the rate of residual tumor in the upgraded cases was not significantly
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higher than that in the non-upgraded cases (Table 2). Interpretative or clerical errors may account for the upgrade, but the pathologic slides from US-VAE were not reviewed retrospectively in our study. Given the upgrade rate of 8.7%, which exceeds the established guideline of 2% to be determined ‘‘probably benign’’ and thus amenable to imaging follow-up instead of surgical excision (American College of Radiology 2003), benign PTs at US-VAE could require follow-up surgical excision. The possibility of upgrade after surgery should be carefully determined before excision. If it were possible to predict which PTs diagnosed at US-VAE are likely to be upgraded, patients with a sufficiently high risk of upgrade could undergo definitive surgery with a negative surgical margin, such as wide excision or mastectomy, rather than enucleation, to avoid repeat excisions because of a positive surgical margin. In the present study, there was a significant difference in BI-RADS US final assessments between non-upgraded and upgraded cases, with upgrade rates of 0% (0/25), 6.7% (1/15) and 100% (1/1) in BI-RADS categories 3, 4a and 4c, respectively (p 5 0.018) (Table 2). Similar to our results, Youn et al. (2013) reported that a higher BI-RADS final assessment (category 3 vs 4 or 5) occurred more frequently in borderline or malignant PTs (p 5 0.008). Although there was tendency for other US features such as larger lesion size, irregular shape, complex cystic echogenicity and presence of a cleft to be observed in borderline or malignant PTs in previous studies (Tan et al. 2012; Youn et al. 2013), there was no significant difference in US features other than final assessment category between non-upgraded and upgraded cases in the present study. In addition to its role in biopsy of breast masses, US-VAE is also used in therapeutic management to remove all US evidence of the mass, when performed for a benign or presumed benign breast mass. However, it has been found that complete removal based on US does not mean complete histologic removal and very small amounts of residual tumor may not be detected on US immediately after US-VAE (Wang et al. 2011). During and immediately after US-VAE, it is difficult to confirm the status of an excised mass because of the physical change induced by biopsy and technical problems. In the literature, the rates of incomplete removal after US-VAE of benign lesions ranged from 11%–46% (mean: 27%) (Alonso-Bartolome et al. 2004; Fine et al. 2003; Grady et al. 2008; March et al. 2003; Tagaya et al. 2008; Youk et al. 2012). In our results, of 14 benign PTs with at least 2 y of US follow-up, no residual abnormality was visible on US. Among 27 PTs that were excised surgically, however, residual tumor was found in 15 (55.6%; 12 benign, 1
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borderline and 2 malignant). Two previous studies reported that PTs exhibited no residual abnormality on US after US-VAE, but residual lesions were found in subsequent surgical excision (Wang et al. 2011, 2012). Given these results and the association of residual tissue with local recurrence of PTs, subsequent surgical excision with a negative resection margin should be considered for PTs diagnosed after US-VAE (Jang et al. 2012). The present study had some limitations. First, it was a retrospective study with a relatively small number of enrolled patients. Sixteen (28%) of 57 US-VAEs were excluded from our study because they were not surgically confirmed and did not have at least 2 y of follow-up US. The high exclusion rate may be a source of selection bias. Second, we did not insert a microclip through the probe at the US-VAE site for follow-up assessments. Before USVAE, however, whole-breast US and mammography were performed to localize the targeted mass, and these imaging findings were used to evaluate any residual abnormality during follow-up assessments. For localization of the US-VAE site before surgical excision, post-VAE changes such as distortion and hematoma, as well as correlation with pre-VAE imaging findings, were used successfully (Youk et al. 2012). In addition, the pathologic slides from US-VAE were not reviewed retrospectively by a pathologist; the original pathologic interpretation was accepted. Therefore, we cannot conclude that interpretative or clerical errors did not account for the upgrade. In conclusion, given the upgrade rate of 8.7% and residual rate of 36.6%, PTs diagnosed after US-VAE should be followed by surgical excision.
REFERENCES Alonso-Bartolome P, Vega-Bolivar A, Torres-Tabanera M, Ortega E, Acebal-Blanco M, Garijo-Ayensa F, Rodrigo I, Munoz-Cacho P. Sonographically guided 11-G directional vacuum-assisted breast biopsy as an alternative to surgical excision: Utility and cost study in probably benign lesions. Acta Radiol 2004;45:390–396. American College of Radiology. Breast imaging reporting and data system. 4th ed. Reston, VA: Author; 2003. Bassett LW, Mahoney MC, Apple SK. Interventional breast imaging: Current procedures and assessing for concordance with pathology. Radiol Clin North Am 2007;45:881–894. Ben Hassouna J, Damak T, Gamoudi A, Chargui R, Khomsi F, Mahjoub S, Slimene M, Ben Dhiab T, Hechiche M, Boussen H, Rahal K. Phyllodes tumors of the breast: A case series of 106 patients. Am J Surg 2006;192:141–147. Bode MK, Rissanen T, Apaja-Sarkkinen M. Ultrasonography and core needle biopsy in the differential diagnosis of fibroadenoma and tumor phyllodes. Acta Radiol 2007;48:708–713. Choi J, Koo JS. Comparative study of histologic features between core needle biopsy and surgical excision in phyllodes tumor. Pathol Int 2012;62:120–126. Dillon MF, Quinn CM, McDermott EW, O’Doherty A, O’Higgins N, Hill AD. Needle core biopsy in the diagnosis of phyllodes neoplasm. Surgery 2006;140:779–784.
Volume 41, Number 3, 2015 Fine RE, Boyd BA, Whitworth PW, Kim JA, Harness JK, Burak WE. Percutaneous removal of benign breast masses using a vacuumassisted hand-held device with ultrasound guidance. Am J Surg 2002;184:332–336. Fine RE, Whitworth PW, Kim JA, Harness JK, Boyd BA, Burak WE Jr. Low-risk palpable breast masses removed using a vacuum-assisted hand-held device. Am J Surg 2003;186:362–367. Foxcroft LM, Evans EB, Porter AJ. Difficulties in the pre-operative diagnosis of phyllodes tumours of the breast: A study of 84 cases. Breast 2007;16:27–37. Gatta G, Iaselli F, Parlato V, Di Grezia G, Grassi R, Rotondo A. Differential diagnosis between fibroadenoma, giant fibroadenoma and phyllodes tumour: Sonographic features and core needle biopsy. Radiol Med 2011;116:905–918. Grady I, Gorsuch H, Wilburn-Bailey S. Long-term outcome of benign fibroadenomas treated by ultrasound-guided percutaneous excision. Breast J 2008;14:275–278. Hahn M, Krainick-Strobel U, Toellner T, Gissler J, Kluge S, Krapfl E, Peisker U, Duda V, Degenhardt F, Sinn HP, Wallwiener D, Gruber IV, Minimally Invasive Breast Intervention Study Group of the German Society of S, Study Group for Breast Ultrasonography of the German Society for Ultrasound in Medicine. Interdisciplinary consensus recommendations for the use of vacuum-assisted breast biopsy under sonographic guidance: First update 2012. Ultraschall Med 2012;33:366–371. Jang JH, Choi MY, Lee SK, Kim S, Kim J, Lee J, Jung SP, Choe JH, Kim JH, Kim JS, Cho EY, Lee JE, Nam SJ, Yang JH. Clinicopathologic risk factors for the local recurrence of phyllodes tumors of the breast. Ann Surg Oncol 2012;19:2612–2617. Jiang Y, Lan H, Ye Q, Jin K, Zhu M, Hu X, Teng L, Cao F, Lin X. Mammotome biopsy system for the resection of breast lesions: Clinical experience in two high-volume teaching hospitals. Exp Ther Med 2013;6:759–764. Kim MJ, Kim EK, Kwak JY, Son EJ, Park BW, Kim SI, Oh KK. Nonmalignant papillary lesions of the breast at US-guided directional vacuum-assisted removal: A preliminary report. Eur Radiol 2008; 18:1774–1783. Komenaka IK, El-Tamer M, Pile-Spellman E, Hibshoosh H. Core needle biopsy as a diagnostic tool to differentiate phyllodes tumor from fibroadenoma. Arch Surg 2003;138:987–990. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, Van der Vijver MJ. WHO classification of tumours of the breast. Geneva: World Health Organization; 2012. Li S, Wu J, Chen K, Jia W, Jin L, Xiao Q, Zeng Y, Su F. Clinical outcomes of 1,578 Chinese patients with breast benign diseases after ultrasound-guided vacuum-assisted excision: Recurrence and the risk factors. Am J Surg 2013;205:39–44. March DE, Coughlin BF, Barham RB, Goulart RA, Klein SV, Bur ME, Frank JL, Makari-Judson G. Breast masses: Removal of all US evidence during biopsy by using a handheld vacuum-assisted device— Initial experience. Radiology 2003;227:549–555. Park HL, Kwon SH, Chang SY, Huh JY, Kim JY, Shim JY, Lee YH. Long-term follow-up result of benign phyllodes tumor of the breast diagnosed and excised by ultrasound-guided vacuum-assisted breast biopsy. J Breast Cancer 2012;15:224–229. Schueller G, Jaromi S, Ponhold L, Fuchsjaeger M, Memarsadeghi M, Rudas M, Weber M, Liberman L, Helbich TH. US-guided 14gauge core-needle breast biopsy: Results of a validation study in 1352 cases. Radiology 2008;248:406–413. Tagaya N, Nakagawa A, Ishikawa Y, Oyama T, Kubota K. Experience with ultrasonographically guided vacuum-assisted resection of benign breast tumors. Clin Radiol 2008;63:396–400. Tan H, Zhang S, Liu H, Peng W, Li R, Gu Y, Wang X, Mao J, Shen X. Imaging findings in phyllodes tumors of the breast. Eur J Radiol 2012;81:e62–e69. Tsang AK, Chan SK, Lam CC, Lui PC, Chau HH, Tan PH, Tse GM. Phyllodes tumours of the breast: Differentiating features in core needle biopsy. Histopathology 2011;59:600–608. Wang ZL, Liu G, Huang Y, Wan WB, Li JL. Percutaneous excisional biopsy of clinically benign breast lesions with vacuum-assisted system: Comparison of three devices. Eur J Radiol 2012;81:725–730.
Should surgery follow US-guided vacuum-assisted excision? d J. H. YOUK et al. Wang ZL, Liu G, Li JL, Ding Q, Su L, Tang J, Ma L. Sonographically guided percutaneous excision of clinically benign breast masses. J Clin Ultrasound 2011;39:1–5. Youk JH, Kim EK, Kim MJ, Kwak JY, Son EJ. Analysis of falsenegative results after US-guided 14-gauge core needle breast biopsy. Eur Radiol 2010;20:782–789. Youk JH, Kim EK, Kim MJ, Lee JY, Oh KK. Missed breast cancers at US-guided core needle biopsy: How to reduce them. Radiographics 2007;27:79–94.
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Youk JH, Kim MJ, Son EJ, Kwak JY, Kim EK. US-guided vacuumassisted percutaneous excision for management of benign papilloma without atypia diagnosed at US-guided 14-gauge core needle biopsy. Ann Surg Oncol 2012;19:922–928. Youn I, Choi SH, Moon HJ, Kim MJ, Kim EK. Phyllodes tumors of the breast: Ultrasonographic findings and diagnostic performance of ultrasound-guided core needle biopsy. Ultrasound Med Biol 2013; 39:987–992.
http://dx.doi.org/10.1016/j.ultrasmedbio.2014.11.004
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Original Contribution PHYLLODES TUMOR DIAGNOSED AFTER ULTRASOUND-GUIDED VACUUM-ASSISTED EXCISION: SHOULD IT BE FOLLOWED BY SURGICAL EXCISION? JI HYUN YOUK,* HANA KIM,* EUN-KYUNG KIM,y EUN JU SON,* MIN JUNG KIM,y and JEONG-AH KIM* * Department of Radiology, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea; and y Department of Radiology, Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea (Received 8 June 2014; revised 24 October 2014; in final form 8 November 2014)
Abstract—Our aim was to retrospectively evaluate the results of ultrasound (US)-guided vacuum-assisted excision (US-VAE) of phyllodes tumors (PTs). A total of 41 PTs diagnosed at US-VAE followed by surgery (n 5 27) or at least 2 y of US monitoring (n 5 14) were included. By comparison of US-VAE pathology with surgical histology or follow-up US results, cases were divided into upgraded (malignant) and non-upgraded (benign) groups. These two groups were compared with respect to clinical, procedural and US features. Among 27 surgical cases, 2 (8.7%) of 23 benign PTs were upgraded to malignant PTs. The Breast Imaging Reporting and Data System category was retrospectively assigned as 4a (50%) or 4b (50%) in the upgraded group (n 5 2) and 3 (64%) or 4a (36%) in the non-upgraded group (n 5 39) (p 5 0.018). Residual tumor was observed at the site of US-VAE in 15 of 27 surgical cases and 0 of 14 US follow-up cases (36.6%, 15/41). Given the rates of upgrade to malignancy (8.7%) and residual tumor (36.6%), PTs diagnosed after US-VAE should be surgically excised. (E-mail: [email protected]) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: Breast neoplasms, Phyllodes tumor, Interventional ultrasonography, Large-core needle biopsy.
Although the pre-operative diagnosis of PT can be essential in establishing the most appropriate therapeutic approach, the differential diagnosis of PT from fibroadenoma remains clinically and radiologically challenging. For breast lesions that are suspected to be clinically benign or concordant benign after core needle biopsy (CNB), conservative management—close follow-up—is widely accepted (Jiang et al. 2013; Youk et al. 2007). However, some patients may prefer complete excision of these lesions because of the psychological stress and physical discomfort from pain, lumps and discharges (Fine et al. 2002; Jiang et al. 2013; Li et al. 2013). Ultrasound-guided vacuum-assisted excision (US-VAE) is being increasingly performed as an alternative to surgical excision for selected clinically benign breast masses such as fibroadenomas or for a concordant benign result after CNB. Because of the difficulty involved in differentiating fibroadenoma from PT, the resulting pathologic diagnosis of PT could be expected in clinical practice after US-VAE of a clinically suspected benign breast mass (Gatta et al. 2011; Park et al. 2012). However, there has been no report on the management of PTs
INTRODUCTION Breast phyllodes tumor (PT) is a rare neoplasm of the breast that accounts for 0.3%–1.0% of primary breast tumors of the breast (Ben Hassouna et al. 2006; Lakhani et al. 2012). Histopathologically, PTs are classified into more specific categories such as benign, borderline and malignant, based on a combination of histologic features including degree of stromal hypercellularity, mitoses and cytologic atypia, stromal overgrowth and nature of the tumor borders/margins. Local recurrence can occur in all subtypes of PT, although the recurrence rate is low for benign tumors; rates range from 10%– 17%, from 14%–25% and from 23%–30% for benign, borderline and malignant PTs, respectively (Lakhani et al. 2012). To minimize recurrence, wide local excision with at least a 1-cm negative resection margin has been recommended as the treatment of choice (Jang et al. 2012).
Address correspondence to: Ji Hyun Youk, Department of Radiology, Gangnam Severance Hospital, 211, Eonju-ro, Gangnam-Gu, Seoul 135-720, South Korea. E-mail: [email protected] 741
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diagnosed as clinically benign breast masses after USVAE. Therefore, the present study was performed to retrospectively evaluate the results for PTs diagnosed as clinically benign breast masses after US-VAE. METHODS The present retrospective study was conducted with institutional review board approval; patient informed consent was waived. Patients After review of the pathologic results of US-VAEs performed from January 2002 through October 2012 at two hospitals, we identified 57 PTs that were diagnosed. Among these cases, 41 PTs in 41 women aged 18–53 y (mean 6 standard deviation: 31.7 6 9.9 y) who underwent follow-up surgical excision (n 5 27) or at least 2 y of US follow-up (n 5 14) after US-VAE were retrospectively reviewed (Fig. 1). CNB was performed before VAE for 10 PTs, but failed to diagnose PT. The remaining 16 cases were excluded from analyses because there was no surgical excision with ,2 y of US follow-up (n 5 11) or no follow-up (n 5 5) (Fig. 1). US examination and US-VAE Ultrasound examination and US-VAE were performed by one of eight radiologists with 4–10 y of experience in breast imaging and US-VAE using high-resolution US units with linear-array transducers of 5–10, 5–12, or 4–15 MHz (HDI 5000, Philips Advanced Technology Laboratories, Bothell, WA; Logic 9, GE Medical Systems, Milwaukee, WI; iU22, Philips Medical Systems, Bothell, WA, USA; or SuperSonic Imagine, Aix-en-Provence, France). By means of a vacuum-assisted device (Mammotome, Ethicon-Endosurgery, Cincinnati, OH, USA) with an 8- or 11-gauge probe under the guidance of a high-resolution US unit mentioned above, the US-VAE procedure was performed as described by Kim et al.
Fig. 1. Flowchart of patient enrollment. Asterisks indicate enrolled cases. US 5 ultrasound.
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(2008). After administration of local anesthesia, the probe was inserted into the breast through a small skin incision and guided into biopsy position under direct US visualization. Multiple core samples were taken until the mass was completely removed, as determined by real-time US of the biopsy site. Forced scan pressure to disperse air artifacts and multidirectional US images, such as views perpendicular to the biopsy needle, were used to visualize the residual mass. For any breast mass larger than 1.0 cm at US, we used US-VAE with an 8-gauge probe. To ensure complete removal of the mass during US-VAE, we removed breast tissue surrounding the mass at approximately four more sampling sites (12, 3, 6 and 9 o’clock directions). Depending on the physician’s and patient’s preferences, wide excision or follow-up US was performed for management of PTs diagnosed after US-VAE at our institution. Data and statistical analysis Medical records were reviewed for clinical features (patient age and palpable mass) and US-VAE procedural characteristics (size of probe used [8 or 11 gauge], number of core specimens per lesion, residual PT at surgery). To collect the pre-VAE lesion size (longest dimension of the lesion at US), US variables based on the Breast Imaging Reporting and Data System (BIRADS; shape, margin, orientation, echo pattern, orientation and posterior acoustic feature) and BI-RADS final assessment categories indicating the probability of malignancy in categories 3, 4a, 4b, 4c and 5 (American College of Radiology 2003), each US image obtained before US-VAE was reviewed retrospectively in consensus by two radiologists with 4 and 10 y of experience in breast imaging, respectively, who knew that cases were PTs diagnosed at US-VAE, but were blinded to the benign, borderline and malignant grading and surgical histology. All 41 PTs diagnosed at US-VAE were divided into two groups, upgraded and non-upgraded, after review of the surgical or US follow-up results. The non-upgraded group comprised those PTs for which there was no residual sonographic abnormality at follow-up US or for which the surgical histology was the same as US-VAE pathology, the tumor had been completely excised without residual lesion or the tumor was another benign lesion (e.g., fibroadenoma, fibrocystic change, fibroadenomatous hyperplasia). The upgraded group comprised those PTs for which the surgical histology indicated a higher grade compared with US-VAE histology. If there was no evidence of residual tumor in the surgical results, the tumor was considered to be non-upgraded. Differences in clinical presentations, procedural characteristics and US findings between the two groups were evaluated. For the 14 PTs that were not excised surgically but followed
Should surgery follow US-guided vacuum-assisted excision? d J. H. YOUK et al.
Table 1. Results for 27 phyllodes tumors that were diagnosed at ultrasound-guided vacuum-assisted excision and then surgically excised Diagnosis at surgical excision after US-VAE
Benign Borderline Malignant Total
Benign
Borderline
Malignant
Total
21* 0 0 21 (77.8%)
0 3* 0 3 (11.1%)
2 0 1* 3 (11.1%)
23 (85.2%) 3 (11.1%) 1 (3.7%) 27 (100%)
US-VAE 5 ultrasound-guided vacuum-assisted excision. * Nine benign, two borderline and one malignant phyllodes tumor exhibited no residual tumor after surgery.
up with US, the presence of residual sonographic abnormalities was determined by reviewing each US image obtained before, during and after US-VAE. On followup US, mild distortion at the site of US-VAE was considered to be a post-VAE change, whereas a spaceoccupying mass was considered to be a residue. When a residual PT was described in the surgical pathology report, it was also considered to be a residue. Statistical comparisons were performed using the c2-test or Fisher exact test for categorical variables and the Mann–Whitney U-test for continuous variables. All statistical analyses were performed with SPSS statistical software (Version 20.0.0, IBM, Armonk, NY, USA). Differences were considered to be statistically significant at a p-value , 0.05. RESULTS Of the 41 PTs diagnosed after US-VAE, 37 (90.2%) were benign, 3 (7.3%) were borderline and 1 (2.4%) was malignant. Pre-VAE lesion size ranged from 8–35 mm (mean 6 standard deviation: 21.3 6 6.8 mm), and the number of core samples ranged from 6–72 (28.6 6 14.0). All 14 cases with at least 2
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y of US follow-up (57.1 6 34.2 mo, range: 25–133 mo) were benign PTs. The pathologic details for 27 PTs that were excised surgically after US-VAE (82.3 6 107.1 d, range: 13–407 d) are summarized in Table 1. Of 23 PTs diagnosed as benign at US-VAE, 2 (8.7%) were upgraded to malignant at final surgical excision (Fig. 2). All three borderline PTs and one malignant PT at US-VAE were not upgraded at final surgical excision. The rate of concordance of PT grade between US-VAE and surgical excision was 92.6%. Among the remaining 14 benign PTs with at least 2 y of US follow-up, there were no recurrences. Accordingly, 39 cases (95.1%) were not upgraded and 2 cases (4.9%) were upgraded after surgical excision or US follow-up. Table 2 summarizes the clinical, procedural and US features of the 41 PTs by group, upgraded or nonupgraded. There was no significant difference in clinical and procedural characteristics between the two groups. With respect to US features, the BI-RADS final assessment category significantly differed between the two groups (p 5 0.018). No PTs in the upgraded group were assessed as category 3, and no PTs in the nonupgraded group were assessed as category 4b. There were no significant differences in other US features between the two groups. Of 14 benign PTs followed up with US for at least 2 y, no residual abnormality was visible. Among 27 PTs that were excised surgically, however, residual tumor was found at the site of US-VAE in 15 (55.6%; 12 benign, 1 borderline and 2 malignant at US-VAE) (Fig. 3). In total, 15 of 41 PTs (36.6%) diagnosed after US-VAE exhibited residual tumor. DISCUSSION Ultrasound-guided CNB is an accurate method for the histologic diagnosis of breast masses that are visible
Fig. 2. Transverse (left) and longitudinal (right) US images of the left breast of a 45-y-old woman revealed a 20-mm oval hypo-echoic mass, which was classified as BI-RADS category 4b. The diagnosis based on US-VAE was benign phyllodes tumor. On surgical excision, the diagnosis was upgraded to malignant phyllodes tumor. BI-RADS 5 Breast Imaging Reporting and Data System; US 5 ultrasound; US-VAE 5 US-guided vacuum-assisted excision.
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Table 2. Clinical and ultrasound features of 41 phyllodes tumors diagnosed at US-VAE followed by surgical excision or at least 2 y of follow-up ultrasound
Clinical findings Age (y) Palpability Yes No Needle gauge 8 11 Number of core samples Residual tumor Yes No Ultrasound findings Lesion size (mm) Shape Oval Round Margin Circumscribed Microlobulated Angular Indistinct Echo pattern Hypo-echoic Complex Orientation Parallel Non-parallel Posterior acoustic feature None Enhancement BI-RADS category 3 4a 4b
Non-upgraded* (n 5 39)
Upgraded* (n 5 2)
p-value
31.0 6 9.6 (28, 18–53)y
45.5 6 0.7 (45.5, 45–46)y
0.090 .0.99
27 (69.2%) 12 (30.8%) 33 (84.6%) 6 (15.4%) 27.4 6 12.9 (26, 6–72)y 13 (52.0%) 12 (48.0%) 21.0 6 6.7 (19, 8–35)y
2 (100.0%) 0 (0%)
.0.99
2 (100.0%) 0 (0%) 51.5 6 19.1 (51.5, 38–65)y
0.053
2 (100%) 0 (0%) 27.0 6 9.9 (27, 20–34)y
37 (94.9%) 2 (5.1%)
2 (100.0%) 0 (0.0%)
18 (46.2%) 14 (35.9%) 2 (5.1%) 5 (12.8%)
0 (0.0%) 2 (100.0%) 0 (0.0%) 0 (0.0%)
38 (96.0%) 1 (4.0%)
2 (100.0%) 0 (0%)
38 (97.4%) 1 (2.6%)
2 (100.0%) 0 (0.0%)
16 (41.0%) 23 (59.0%)
1 (50.0%) 1 (50.0%)
25 (64.1%) 14 (35.9%) 0 (0%)
0 (0.0%) 1 (50.0%) 1 (50.0%)
0.487 0.235 .0.99 0.462
.0.99 .0.99 .0.99 0.018
US-VAE 5 US-guided vacuum-assisted excision. * Classified as non-upgraded or upgraded by correlating US-VAE pathology with the surgical or US follow-up results. y Mean 6 standard deviation (median, range).
on US. However, the possibility of histologic underestimation or false-negative results is an inherent weakness of this technique (Schueller et al. 2008; Youk et al. 2010). Specifically, the differential diagnosis of PT from fibroadenoma in CNB is difficult. PTs are
differentiated from fibroadenomas principally by their stroma, which is hypercellular; they also have leaf-like projections into the stroma. However, because of the intratumoral heterogeneity of PTs, with some areas having the appearance of fibroadenoma, the degree of cellularity
Fig. 3. Transverse (left) and longitudinal (right) US images of the left breast of a 38-y-old woman revealed a 25-mm oval hypo-echoic mass, which was classified as BI-RADS category 3. The diagnosis based on US-VAE was benign phyllodes tumor. Surgical excision revealed residual benign phyllodes tumor at the site of VAE. BI-RADS 5 Breast Imaging Reporting and Data System; US 5 ultrasound; US-VAE 5 US-guided vacuum-assisted excision.
Should surgery follow US-guided vacuum-assisted excision? d J. H. YOUK et al.
may not be high enough to diagnose PTs and leaf-like projections may be hard to detect on CNB. Similarly, the grading of PTs as benign, borderline or malignant relies on such indices as degree of atypia, number of stromal mitoses per high-power field, nuclear size and pleomorphism, necrosis and infiltrative or pushing margins, which have not been proven sufficiently reliable to allow pathologists to make a definitive diagnosis on CNB (Dillon et al. 2006). The false-negative rate of CNB for PTs ranged from 8%–39% (mean: 20.5%) in previous studies (Bode et al. 2007; Choi and Koo 2012; Dillon et al. 2006; Foxcroft et al. 2007; Gatta et al. 2011; Komenaka et al. 2003; Tsang et al. 2011; Youn et al. 2013). The rate of concordance of PT grade between CNB and surgery was 61.2% (38.5% for benign PTs and 74.7% for borderline or malignant PTs) (Choi and Koo 2012). Compared with spring-loaded devices for CNB, vacuum-assisted devices provide larger specimens with more contiguous sampling, resulting in more accurate pathology results and fewer disease upgrades at the time of surgery (Bassett et al. 2007; Hahn et al. 2012; Youk et al. 2012). For PTs diagnosed after US-VAE, however, additional surgical excision can be an issue when considering the difficulty in diagnosis and the recurrence related to residual PT. The rate of concordance of PT grade between US-VAE and surgery was 92.6% (91.3% in benign and 100% in borderline and malignant PTs) in our study. In two previous studies, the rates of concordance of grade between CNB and surgery were lower than those in our study: 61.2% (38.5% in benign PTs and 74.7% in borderline or malignant PTs) (Choi and Koo 2012) and 83.3% (82.1% in benign PTs and 100% in borderline or malignant PTs) (Youn et al. 2013). A trend toward higher concordance on borderline or malignant subtypes than the benign subtype was observed, and there was no downgrade of borderline or malignant subtypes after surgical excision, as in our results. Although there are limitations in predicting PT grade, particularly on the basis of CNB, the diagnosis of borderline or malignant PT after US-VAE may warrant subsequent wide excision or mastectomy. With respect to benign PTs, 8.7% (2 of 23) were upgraded to malignant PTs in our study. In the previous study, there was no upgrading for 31 benign PTs with at least 2 y of US follow-up after US-VAE (Park et al. 2012). Possibly the results differ because of the small number of benign PTs diagnosed in our study, the lack of surgical excisions in the previous study and differences in study populations. Although US-VAE continued until all US evidence of the mass was completely removed, with larger sampling including the surrounding tissue, in the present study, US-VAE could have failed to sample and diagnose malignant tumor in residual tissue. However, the rate of residual tumor in the upgraded cases was not significantly
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higher than that in the non-upgraded cases (Table 2). Interpretative or clerical errors may account for the upgrade, but the pathologic slides from US-VAE were not reviewed retrospectively in our study. Given the upgrade rate of 8.7%, which exceeds the established guideline of 2% to be determined ‘‘probably benign’’ and thus amenable to imaging follow-up instead of surgical excision (American College of Radiology 2003), benign PTs at US-VAE could require follow-up surgical excision. The possibility of upgrade after surgery should be carefully determined before excision. If it were possible to predict which PTs diagnosed at US-VAE are likely to be upgraded, patients with a sufficiently high risk of upgrade could undergo definitive surgery with a negative surgical margin, such as wide excision or mastectomy, rather than enucleation, to avoid repeat excisions because of a positive surgical margin. In the present study, there was a significant difference in BI-RADS US final assessments between non-upgraded and upgraded cases, with upgrade rates of 0% (0/25), 6.7% (1/15) and 100% (1/1) in BI-RADS categories 3, 4a and 4c, respectively (p 5 0.018) (Table 2). Similar to our results, Youn et al. (2013) reported that a higher BI-RADS final assessment (category 3 vs 4 or 5) occurred more frequently in borderline or malignant PTs (p 5 0.008). Although there was tendency for other US features such as larger lesion size, irregular shape, complex cystic echogenicity and presence of a cleft to be observed in borderline or malignant PTs in previous studies (Tan et al. 2012; Youn et al. 2013), there was no significant difference in US features other than final assessment category between non-upgraded and upgraded cases in the present study. In addition to its role in biopsy of breast masses, US-VAE is also used in therapeutic management to remove all US evidence of the mass, when performed for a benign or presumed benign breast mass. However, it has been found that complete removal based on US does not mean complete histologic removal and very small amounts of residual tumor may not be detected on US immediately after US-VAE (Wang et al. 2011). During and immediately after US-VAE, it is difficult to confirm the status of an excised mass because of the physical change induced by biopsy and technical problems. In the literature, the rates of incomplete removal after US-VAE of benign lesions ranged from 11%–46% (mean: 27%) (Alonso-Bartolome et al. 2004; Fine et al. 2003; Grady et al. 2008; March et al. 2003; Tagaya et al. 2008; Youk et al. 2012). In our results, of 14 benign PTs with at least 2 y of US follow-up, no residual abnormality was visible on US. Among 27 PTs that were excised surgically, however, residual tumor was found in 15 (55.6%; 12 benign, 1
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borderline and 2 malignant). Two previous studies reported that PTs exhibited no residual abnormality on US after US-VAE, but residual lesions were found in subsequent surgical excision (Wang et al. 2011, 2012). Given these results and the association of residual tissue with local recurrence of PTs, subsequent surgical excision with a negative resection margin should be considered for PTs diagnosed after US-VAE (Jang et al. 2012). The present study had some limitations. First, it was a retrospective study with a relatively small number of enrolled patients. Sixteen (28%) of 57 US-VAEs were excluded from our study because they were not surgically confirmed and did not have at least 2 y of follow-up US. The high exclusion rate may be a source of selection bias. Second, we did not insert a microclip through the probe at the US-VAE site for follow-up assessments. Before USVAE, however, whole-breast US and mammography were performed to localize the targeted mass, and these imaging findings were used to evaluate any residual abnormality during follow-up assessments. For localization of the US-VAE site before surgical excision, post-VAE changes such as distortion and hematoma, as well as correlation with pre-VAE imaging findings, were used successfully (Youk et al. 2012). In addition, the pathologic slides from US-VAE were not reviewed retrospectively by a pathologist; the original pathologic interpretation was accepted. Therefore, we cannot conclude that interpretative or clerical errors did not account for the upgrade. In conclusion, given the upgrade rate of 8.7% and residual rate of 36.6%, PTs diagnosed after US-VAE should be followed by surgical excision.
REFERENCES Alonso-Bartolome P, Vega-Bolivar A, Torres-Tabanera M, Ortega E, Acebal-Blanco M, Garijo-Ayensa F, Rodrigo I, Munoz-Cacho P. Sonographically guided 11-G directional vacuum-assisted breast biopsy as an alternative to surgical excision: Utility and cost study in probably benign lesions. Acta Radiol 2004;45:390–396. American College of Radiology. Breast imaging reporting and data system. 4th ed. Reston, VA: Author; 2003. Bassett LW, Mahoney MC, Apple SK. Interventional breast imaging: Current procedures and assessing for concordance with pathology. Radiol Clin North Am 2007;45:881–894. Ben Hassouna J, Damak T, Gamoudi A, Chargui R, Khomsi F, Mahjoub S, Slimene M, Ben Dhiab T, Hechiche M, Boussen H, Rahal K. Phyllodes tumors of the breast: A case series of 106 patients. Am J Surg 2006;192:141–147. Bode MK, Rissanen T, Apaja-Sarkkinen M. Ultrasonography and core needle biopsy in the differential diagnosis of fibroadenoma and tumor phyllodes. Acta Radiol 2007;48:708–713. Choi J, Koo JS. Comparative study of histologic features between core needle biopsy and surgical excision in phyllodes tumor. Pathol Int 2012;62:120–126. Dillon MF, Quinn CM, McDermott EW, O’Doherty A, O’Higgins N, Hill AD. Needle core biopsy in the diagnosis of phyllodes neoplasm. Surgery 2006;140:779–784.
Volume 41, Number 3, 2015 Fine RE, Boyd BA, Whitworth PW, Kim JA, Harness JK, Burak WE. Percutaneous removal of benign breast masses using a vacuumassisted hand-held device with ultrasound guidance. Am J Surg 2002;184:332–336. Fine RE, Whitworth PW, Kim JA, Harness JK, Boyd BA, Burak WE Jr. Low-risk palpable breast masses removed using a vacuum-assisted hand-held device. Am J Surg 2003;186:362–367. Foxcroft LM, Evans EB, Porter AJ. Difficulties in the pre-operative diagnosis of phyllodes tumours of the breast: A study of 84 cases. Breast 2007;16:27–37. Gatta G, Iaselli F, Parlato V, Di Grezia G, Grassi R, Rotondo A. Differential diagnosis between fibroadenoma, giant fibroadenoma and phyllodes tumour: Sonographic features and core needle biopsy. Radiol Med 2011;116:905–918. Grady I, Gorsuch H, Wilburn-Bailey S. Long-term outcome of benign fibroadenomas treated by ultrasound-guided percutaneous excision. Breast J 2008;14:275–278. Hahn M, Krainick-Strobel U, Toellner T, Gissler J, Kluge S, Krapfl E, Peisker U, Duda V, Degenhardt F, Sinn HP, Wallwiener D, Gruber IV, Minimally Invasive Breast Intervention Study Group of the German Society of S, Study Group for Breast Ultrasonography of the German Society for Ultrasound in Medicine. Interdisciplinary consensus recommendations for the use of vacuum-assisted breast biopsy under sonographic guidance: First update 2012. Ultraschall Med 2012;33:366–371. Jang JH, Choi MY, Lee SK, Kim S, Kim J, Lee J, Jung SP, Choe JH, Kim JH, Kim JS, Cho EY, Lee JE, Nam SJ, Yang JH. Clinicopathologic risk factors for the local recurrence of phyllodes tumors of the breast. Ann Surg Oncol 2012;19:2612–2617. Jiang Y, Lan H, Ye Q, Jin K, Zhu M, Hu X, Teng L, Cao F, Lin X. Mammotome biopsy system for the resection of breast lesions: Clinical experience in two high-volume teaching hospitals. Exp Ther Med 2013;6:759–764. Kim MJ, Kim EK, Kwak JY, Son EJ, Park BW, Kim SI, Oh KK. Nonmalignant papillary lesions of the breast at US-guided directional vacuum-assisted removal: A preliminary report. Eur Radiol 2008; 18:1774–1783. Komenaka IK, El-Tamer M, Pile-Spellman E, Hibshoosh H. Core needle biopsy as a diagnostic tool to differentiate phyllodes tumor from fibroadenoma. Arch Surg 2003;138:987–990. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, Van der Vijver MJ. WHO classification of tumours of the breast. Geneva: World Health Organization; 2012. Li S, Wu J, Chen K, Jia W, Jin L, Xiao Q, Zeng Y, Su F. Clinical outcomes of 1,578 Chinese patients with breast benign diseases after ultrasound-guided vacuum-assisted excision: Recurrence and the risk factors. Am J Surg 2013;205:39–44. March DE, Coughlin BF, Barham RB, Goulart RA, Klein SV, Bur ME, Frank JL, Makari-Judson G. Breast masses: Removal of all US evidence during biopsy by using a handheld vacuum-assisted device— Initial experience. Radiology 2003;227:549–555. Park HL, Kwon SH, Chang SY, Huh JY, Kim JY, Shim JY, Lee YH. Long-term follow-up result of benign phyllodes tumor of the breast diagnosed and excised by ultrasound-guided vacuum-assisted breast biopsy. J Breast Cancer 2012;15:224–229. Schueller G, Jaromi S, Ponhold L, Fuchsjaeger M, Memarsadeghi M, Rudas M, Weber M, Liberman L, Helbich TH. US-guided 14gauge core-needle breast biopsy: Results of a validation study in 1352 cases. Radiology 2008;248:406–413. Tagaya N, Nakagawa A, Ishikawa Y, Oyama T, Kubota K. Experience with ultrasonographically guided vacuum-assisted resection of benign breast tumors. Clin Radiol 2008;63:396–400. Tan H, Zhang S, Liu H, Peng W, Li R, Gu Y, Wang X, Mao J, Shen X. Imaging findings in phyllodes tumors of the breast. Eur J Radiol 2012;81:e62–e69. Tsang AK, Chan SK, Lam CC, Lui PC, Chau HH, Tan PH, Tse GM. Phyllodes tumours of the breast: Differentiating features in core needle biopsy. Histopathology 2011;59:600–608. Wang ZL, Liu G, Huang Y, Wan WB, Li JL. Percutaneous excisional biopsy of clinically benign breast lesions with vacuum-assisted system: Comparison of three devices. Eur J Radiol 2012;81:725–730.
Should surgery follow US-guided vacuum-assisted excision? d J. H. YOUK et al. Wang ZL, Liu G, Li JL, Ding Q, Su L, Tang J, Ma L. Sonographically guided percutaneous excision of clinically benign breast masses. J Clin Ultrasound 2011;39:1–5. Youk JH, Kim EK, Kim MJ, Kwak JY, Son EJ. Analysis of falsenegative results after US-guided 14-gauge core needle breast biopsy. Eur Radiol 2010;20:782–789. Youk JH, Kim EK, Kim MJ, Lee JY, Oh KK. Missed breast cancers at US-guided core needle biopsy: How to reduce them. Radiographics 2007;27:79–94.
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Youk JH, Kim MJ, Son EJ, Kwak JY, Kim EK. US-guided vacuumassisted percutaneous excision for management of benign papilloma without atypia diagnosed at US-guided 14-gauge core needle biopsy. Ann Surg Oncol 2012;19:922–928. Youn I, Choi SH, Moon HJ, Kim MJ, Kim EK. Phyllodes tumors of the breast: Ultrasonographic findings and diagnostic performance of ultrasound-guided core needle biopsy. Ultrasound Med Biol 2013; 39:987–992.