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1 All authors: Radiology Imaging Associates, Sally Jobe Breast Diagnostic and Counseling Center, 8200 E. Belleview Ave., Ste. 102, Englewood, CO 80111
Received August 18, 1999;
accepted after revision September 29, 1999.
Address correspondence to M. A. Dennis.
Abstract
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MATERIALS AND METHODS. Forty-nine women who presented with nipple discharge and who had final pathologic diagnoses of papillary lesions were retrospectively identified. Fifty-six lesions were biopsied in this group. The examinations included mammography, ductography, sonography, and, if possible, percutaneous biopsy. All lesions were centrally located and most were superficial. Of this study group, four patients with five lesions proceeded to sonographically guided automated core biopsy, and 38 patients with 44 intraductal lesions identified by sonography advanced to sonographically guided biopsy with an 11-gauge mammotome probe. One patient underwent stereotactic 11-gauge mammotome biopsy. Patients not advancing to sonographically guided biopsy were those with masses either in the nipple or nipple-areolar complex (five patients), one patient with no identifiable lesion at sonography, and one directly referred for open surgical biopsy.
RESULTS. In all biopsied patients, satisfactory tissue for diagnosis was obtained. In patients biopsied with the mammotome probe, follow-up at a mean time of 13 months revealed resolution of the presenting problematic discharge in 97.2% of patients. Complications were mild and infrequent. Only one of 50 percutaneously biopsied lesions was not benign and required subsequent surgery.
CONCLUSION. Papilloma excision with percutaneous biopsy allows safe and accurate tissue analysis and a high probability of terminating the symptomatic nipple discharge.
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Until recently, skepticism existed as to the appropriateness of imaging-guided minimally invasive biopsy for the evaluation of intraductal lesions. Liberman et al. [2] described how core biopsy can be accurate in the exclusion of significant disease in intraductal lesions and avert surgical exploration. On the basis of one patient, Liberman et al. alluded to the possibility of nipple-discharge treatment through vacuum-assisted biopsy. The current study was the first describing a series of patients with intraductal masses in whom complete or near complete removal of the lesions during minimally invasive imaging-guided biopsy was accomplished. In this group of symptomatic patients, a success rate of 97.2% for eliminating discharge, comparable with that of surgical exploration, was realized [1,3].
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Patients with nipple discharge (clear, serous, heme-positive, or frankly bloody) suggestive of disease were examined with mammography, ductography, sonography with or without color, or power Doppler sonography, and if feasible, with percutaneous biopsy on the same visit. In patients with multiple discharging ducts, each discharge was analyzed separately. Most ductographies were performed by an experienced breast center nurse. Identification of a location that when palpated led to expression of nipple discharge, a trigger point, was helpful in directing the search for the offending duct in some patients. Two methods of performing ductography were used. One method used a blunt right-angled galactography needle, and the other used a 24-gauge angiocatheter (without the needle) advanced over a 3-0 blue monofilament polypropylene suture that had been threaded into the offending duct. An average of 0.1-0.6 ml of a 50% mixture of nonionic contrast material and 1% lidocaine was injected to increase patient comfort. Standard two-view mammography or standard mammography followed by full field-of-view digital mammography was performed during injection.
Once the location of the intraductal lesion was determined by ductography, targeted sonography (Logiq 400 MD, General Electric, Milwaukee, WI; Acoustic Imaging 5200, Phoenix, AZ) was performed in that segment to locate the mass. The sonography was performed with warm gel to prevent duct spasm, and the primary plane of scanning was radial to conform to ductal anatomy. Because of the problem of nipple shadowing, the transducer was used to approach and then, in an antiradial plane and perpendicular to the skin surface, to push over the nipple to displace it from its obscuring position. At times, the nonscanning hand was placed on one side of the areola with upward pressure toward the transducer while the subareolar breast was scanned. Thirdly, a commercially available gel pad stand-off (Aquaflex; Parker Laboratories, Orange, NJ) or a generously applied layer of acoustic scanning gel was used at times to improve periareolar-transducer contact.
The ductography needle or catheter was usually left in place after the ductograms were obtained. This procedure allowed a saline injection to be performed with real-time sonographic observation (sonographic ductography) to confirm the concordance of the radiographic, ductographic, and sonographic findings if desired by the attending radiologist (Fig. 1A,1B). Generally, if the duct orifice was located in a central position on the nipple, then the entire retroareolar breast was scanned. If the discharging duct orifice or ductographic lesion was located at the periphery of the nipple, the intraductal lesion was sought out and usually successfully visualized in the subareolar or periareolar duct segment corresponding to the clock position of the orifice. If the ductography was unsuccessful, then the entire retroareolar breast was examined. If a lesion detected on ductography was not seen on sonography, the mass was stereotactically biopsied during repeated ductography (one patient). If a subtle or questionable sonographic lesion was detected after positive findings on ductography, then a retractable hook wire was placed through the lesion with sonographic guidance and a second ductography was performed to establish concordance before sonographically guided biopsy (one patient). Finally, power color Doppler sonography was used occasionally to increase the confidence level that echogenic material visualized in a duct or cyst represented vascular tissue or neoplasm instead of inspissated secretion or fibrous septation (Figs. 2 and 3).
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Sonographically guided mammotomy (mammotome; Biopsys/Ethicon Endo-surgery, Cincinnati, OH) with an 11-gauge probe attached to an articulated arm was used in all except five patients to biopsy the targeted intraductal lesion (four patients biopsied with 14-gauge automated core biopsy needle and one with an 11-gauge mammotomy with stereotactic guidance). This technique has been described in detail by Parker et al. [4]. Briefly, the patient is positioned supine if the lesion is medial or near the vertical mid nipple line or is placed in an ipsilateral anterior-oblique position if it is in the lateral half of the breast. This positioning flattens and stabilizes the breast while optimizing the sonographic image. After the patient is prepared and draped in the usual sterile fashion, the skin is anesthetized with 1% lidocaine with bicarbonate with a 30-gauge needle. Then with a 20-gauge spinal needle, approximately 15-20 ml of 1% lidocaine with 1/100,000 epinephrine is injected along the proposed mammotome probe course leading up to and then posterior to the lesion. The anesthetic injection serves to hydrodissect the tissue to allow smooth passage of the 11-gauge mammotome probe.
A 4-mm incision is then made with a scalpel, and with the mammotome probe attached to an articulated arm, the radiologist inserts the probe with continuous sonographic monitoring as the technologist makes appropriate real-time adjustments in the articulated arm position. The final position of the probe is ideally directly posterior to the intraductal lesion with the target centered in the upward-turned aperture (Figs. 4A,4B,4C and 5A,5B,5C,5D). From this "locked" position, the radiologist rotating the probe aperture between the 10- and 2-o'clock positions acquires samples. If the lesion is superficial, a generous lidocaine injection is given between the lesion and skin surface as insulation to diminish the possibility of creating a skin defect from the inside out during tissue acquisition. Close attention is paid to the sonographic appearance of the skin during superficial biopsy, and if undue downward movement occurs into the upward-directed probe aperture during suction but before cutting, the mechanical cutter is not activated, and a second injection between the lesion and skin may be needed. If the lesion involves the nipple (Fig. 6A,6B) or nipple-areolar complex, no biopsy is performed, although tissue from lesions in close proximity may be successfully and safely acquired. To avoid skin transgression, biopsy from the side or above, instead of from below the lesion, may be performed but that is not the preferred method. Accomplishing a complete excision is more difficult from the side, and distal shadowing limits the real-time monitoring of tissue acquisition with the probe interposed between the lesion and skin.
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In general, papillomas are easily and completely extracted because of their soft consistency. If sonography shows that the intraductal lesion is completely removed or if the residual mass would be difficult to locate again should further surgery be necessary, a small marking clip (Micromark; Biopsys; Ethicon Endo-surgery, Cincinnati, OH) is deployed through the probe. Then a unilateral mammography is performed at the end of the procedure to assess the accuracy of clip placement compared with the lesion location on ductography. Any discrepancy is noted for future reference.
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Of the 49 patients retrospectively identified as having nipple discharge with papillary lesions on pathology, 39 patients with 45 lesions were biopsied with imaging-guided mammotomy, and four patients with five lesions underwent automated core biopsy. Of six patients going to surgery without percutaneous biopsy, four had lesions not considered by the attending radiologist to be safely accessible with the mammotome technique. In one patient, only a dilated duct was seen on sonography without a filling defect to target; one patient was referred for surgery as the preferred biopsy choice. Only one patient went to surgery because of an atypical lesion that was detected by automated core biopsy. One patient went to surgery because of persistent but diminished nipple discharge after mammotomy.
The sonographically directed biopsies were performed by four experienced interventional breast radiologists. The mean maximum dimension of the papillomas seen on sonography in the biopsy group was 9 mm, the mean minimal dimension was 4.4 mm, the mean depth from the skin surface on sonography was 6.5 mm, and the mean distance from the duct orifice was 14 mm. Total excision of intraductal lesions as assessed on intraprocedural sonography occurred 73% of the time, and 80-100% excision occurred in 90% of patients. Clip placement was deployed in 40%, attempted unsuccessfully in 4%, and not deployed in 56%. Partial removal of the lesion was usually associated with lesions larger than 12 mm in maximal dimension. The mean number of samples harvested was 10 (sample range, 3-24).
Immediate complications included small (12 x 12 mm to 12 x 20 mm) hematomas in three (9%) of 32 patients, brisk bleeding treated with thrombin USP (Jones Pharmaceutical, St. Louis, MO) injection through the probe during the procedure in one patient, and areolar biopsy treated with plastic surgical repair with an excellent cosmetic result in one patient. In the follow-up of this group with complications, discomfort levels and extent of ecchymoses were recorded during a telephone interview 10 days after biopsy. Forty percent reported no pain, 30% reported minimal pain, and although 30% reported moderate pain, two of every three of these patients experienced pain resolution in 24 hr. Thirty-two patients reported ecchymosis with 54% describing less than a 2.0-cm bruise, 12% reporting a 2- to 5-cm bruise, 25% reporting a 5- to 10-cm bruise, and 9% reporting a greater than 10-cm ecchymosis with small hematomas. Delayed complications included twinges at 3 months in six (13%) of 45 lesions and one clinical (not culture-proven) infection.
The nipple discharge was absent in all except one patient at 6 months, and in the patient with recurring or persistent discharge, the discharge was greatly diminished. The overall mean follow-up time was 13 months for those patients in the study group who could be contacted. Fifty percent of these patients had the final follow-up at 6 months or less, 17% at 7-17 months, and 33% at 18-41 months. Only one patient diagnosed with benign papilloma was subsequently taken to surgery. The surgical biopsy was benign. Only one of 56 lesions biopsied was atypical. In this patient, an automated 14-gauge core biopsy showed low nuclear grade ductal carcinoma in situ in the papilloma. Further surgery showed extensive papillary low nuclear grade ductal carcinoma in situ adjacent to the papilloma in surrounding ducts.
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At the turn of the 20th century, given what was then known about the underlying causes and given the accepted diagnostic and therapeutic techniques of that time, surgeons chose mastectomy as the treatment of choice for bloody nipple discharge. In the second half of the century, the diagnosis and treatment was segmentectomy or, if possible, isolated duct resection. In the latter, a circumareolar incision was made, the nipple was retracted, the offending duct was identified through a variety of techniques, and selective ductal excision was accomplished. Then in the late 1980s, radiologists began percutaneous imaging-guided histologic needle sampling of the breast [6], enabling accurate minimally invasive biopsy. This procedure was followed shortly thereafter by the development of an even more accurate [7,8] vacuum-assisted instrument (mammotome). Liberman et al. [2] tested the accuracy of core biopsy (automated core or vacuum-assisted percutaneous breast biopsy) for the subset of intraductal lesions with the conclusion that percutaneously diagnosed benign intraductal lesions no longer required open surgical biopsy. Now with the recent advent of sonographically guided vacuum-assisted mammotomy, both diagnosis and treatment of benign papillomas may be combined into one procedure. Thus, irritating nipple discharge can be effectively treated percutaneously in most patients.
In this small series, the rate of successful treatment of nipple discharge was at least that of surgical excision. One of 39 mammotomy patients presented with a persistent or recurrent discharge, and it is unclear whether this discharge was caused by a new papilloma or regrowth of the previous papilloma believed to have been totally excised. A second ductogram was not obtained to confirm that the offending duct corresponded to the previously biopsied duct. In both of these possible scenarios, a minimally invasive guided procedure of either the new or recurrent lesion can be accomplished without surgery. Three patients in the mammotome series had previously biopsied central papillomas not presenting with nipple discharge. The question arises as to whether these particular patients are at a higher risk for atypia or frank neoplasia. However, in this situation characterized by multiple central papillomas, no definite information at this time suggested a premalignant milieu requiring wide excision through surgery.
At the beginning of the experience with central intraductal lesion biopsy, some concerns existed about potential complications with 11-gauge mammotome tissue acquisition, particularly with superficial lesions near the nipple. First, significantly larger samples were harvested with 11-gauge vacuum-assisted biopsy when compared with the 14-gauge automated core procedure. Second, concerns stemmed from what surgeons have long known to be true: the central subareolar breast (where most symptomatic papillomas are found) is more likely to bleed during procedures and cause subsequent discomfort for the patient. This discomfort in turn is caused by the generous regional enervation and vascularity Another potentially aggravating factor for bleeding was the relative lack of breast compression during sonographically guided mammotome biopsy compared with stereotactic mammotomy. Also, because of the proximity of many of the papillomas to the more richly enervated skin surface, an additional concern existed over potentially unacceptable discomfort levels during and after the procedure. However, all of these theoretic concerns failed to materialize. First, when compared with the minimal (nonclinically significant) effects seen during percutaneous 11-gauge biopsy in the nonretroareolar breast, immediate complications did not significantly increase clinically. Although the percentage of patients experiencing moderate immediate discomfort after the procedure increased, this discomfort resolved in two of every three patients in 24 hr. Mild delayed discomfort (intermittent twinges of pain) occurred in only 13% of patients. Second, thrombin injection was required only once to control brisk bleeding, no hematoma much larger than the routinely expected mammotome cavity occurred, and no complication arose requiring surgical intervention. The greater incidence of 5- to 10-cm ecchymoses did not appear to present a problem for the patients. In addition, no mammographic, sonographic, or cosmetic change was observed on follow-up.
Long-term follow-up is not yet available on the patients in this study, and the pathophysiology of intraductal lesions with discharge is not fully understood [9,10]. Consequently, the ultimate role of percutaneous treatment in central benign papillary intraductal lesions is uncertain. The issues to be considered are the recurrence rate of percutaneously removed lesions and the propensity of surrounding ducts or duct branches to form additional papillomas. For now, complete removal of mammographic or sonographic findings by imaging criteria cannot be equated with complete excision of the pathologic process; therefore, securrences are theoretically expected. Future percutaneous techniques may eventually be developed to guarantee total excision with histologic margins. But until that time, the general use of current minimally invasive imaging-guided techniques to obtain complete lesion excision or to obtain histologic margins as a primary goal cannot be advocated. Finally, recurrence questions can be answered accurately only through long-term follow-up and through ductography to prove concordance of ducts containing lesions producing new symptoms with previously biopsied symptomatic ducts. The inconvenience and discomfort associated with follow-up percutaneous papilloma biopsy may eventually need to be weighed against single wide excisional surgical biopsy.
It is not yet known whether short- or long-term success in curing recurrent discharge is more a function of duct disruption, lesion removal, or both. In three patients with four papillomas biopsied with automated core biopsy (lesion sampled but not removed), on a mean follow-up of 32 months, three of four biopsied lesions showed no signs of recurrent discharge.
Questions regarding the biology of solitary or multiple intraductal lesions and the significance of a proliferative milieu have yet to be definitively answered [9,10]. This issue bears on the future decision between using second percutaneous excisions and more generous surgical excision of the area prone to repeatedly forming benign intraductal lesions. Of note is the apparent lack of elevated risk of carcinoma in patients with recurring central benign papillomas.
To conclude, this preliminary information suggests effective treatment of nipple discharge is possible with sonographically guided mammotomy, although longer follow-up is required to prove the long-term effectiveness of the procedure. Sonographically guided ablation of small intraductal lesions is a technique in reach of any radiologist with near-field interventional sonography skills. The equipment is commercially available, and the technology is currently evolving into increasingly user-friendly platforms, including the hand-held mammotome device. When a patient presents with a spontaneous heme-positive, serous, clear, or bloody nipple discharge, percutaneous intraductal lesion removal after diagnostic workup can be offered as an alternative to primary surgical treatment.
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