Interventional radiology in the diagnosis and treatment of diseases of the breast: a historical review and future perspective based on currently available techniques.

Va s c u l a r a n d I n t e r ve n t i o n a l R a d i o l o g y • R ev i ew Tomkovich History and Future of Interventional Breast Radiology

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Vascular and Interventional Radiology Review

Kenneth R. Tomkovich1 Tomkovich KR

Interventional Radiology in the Diagnosis and Treatment of Diseases of the Breast: A Historical Review and Future Perspective Based on Currently Available Techniques OBJECTIVE. The topic of imaging-guided breast interventions spans more than 30 years. Radiologists pioneered procedures such as needle or wire localization and ultrasoundand stereotactic-guided biopsy. Using recently developed devices and technology, the opportunity exists to treat lesions of the breast with minimally invasive imaging-guided techniques. CONCLUSION. Breast imagers and interventional radiologists, along with our surgical and oncologic colleagues, are best qualified to participate together in the research and development of these procedures.

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Keywords: ablation, atypical ductal hyperplasia, breast, ductal carcinoma in situ, fibroadenoma, stereotacticguided interventions, ultrasound-guided interventions DOI:10.2214/AJR.14.12994 Received April 12, 2014; accepted without revision April 20, 2014. K. R. Tomkovich is a medical consultant for Scion Medical Technologies, a member of the scientific advisory board for IceCure Medical, and an invited guest speaker and medical consultant for CareFusion Corporation. 1 Department of Radiology, CentraState Medical Center and Freehold Radiology Group, 901 W Main St, Freehold, NJ 07728. Address correspondence to K. R. Tomkovich ([email protected]).

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he practice of breast interventions has come a long way since the first imaging-guided needle localization procedures were reported [1–3]. Hall and Frank [1], Kopans and DeLuca [2], and Homer [3] were all pioneers in the fledgling field of breast interventional radiology. Their techniques and devices made for the purpose of improving surgical outcomes in patients with diseases of the breast helped advance the field and have stood the test of time [4, 5]. Many of their techniques are still used today [6, 7]. The growth and development of imaging-guided interventions and research in the field is driven, by many factors. The primary factor is to improve the quality of health for our patients [8]. Some of this growth is consumer driven, but the majority is directed by physicians seeking better outcomes [9, 10]. Another factor influencing the development of new breast interventions is new imaging techniques. New modalities lead to the requirement of new interventions. With improvements in ultrasound came the advent of ultrasound-guided breast biopsy [11, 12]. With the development of stereotactic imaging came stereotactic-guided intervention [13–15]. This procedure changed the way physicians approached breast microcalcifications and small solid masses not visible on ultrasound. The idea that imagingguided biopsy could be as accurate as surgical excisional biopsy was quite a leap and had to be validated through years of research and refinements in technique [16, 17]. When the stereotactic biopsy results were not concordant, the

procedure was not abandoned. Research was performed to better understand how to improve the procedure and how to validate results [18– 21]. Only after many years of research and the development of percutaneous imaging-guided breast biopsy did the surgical community recognize in 2005 for the first time that, if a lesion could be detected by imaging, then imagingguided biopsy should be the first choice for the diagnosis of a breast lesion as opposed to open surgical biopsy [22]. So it is today with new modalities such as positron emission mammography and digital tomosynthesis that new procedures need to be developed to effectively biopsy lesions imaged with this new equipment that may not otherwise be seen with conventional imaging [23, 24]. Separately from imaging breakthroughs is the development by industry, through collaboration with physicians, of new and improved devices to perform breast interventional procedures [25, 26]. Finally, and perhaps most importantly, true growth is established through procedural innovation. By never being satisfied and challenging the status quo, physicians continue to strive to do better by creating new minimally invasive imagingguided procedures. These are often better tolerated by patients and less expensive than traditional surgical techniques [27–30]. Ultrasound-Guided Breast Biopsy: Historical Perspective and Future Applications Of all the imaging modalities used for the depiction of lesions of the breast, ultrasound

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Tomkovich is certainly one of the safest and best tolerated by patients. Ultrasound of the breast requires no radiation and no contrast material injection and can be performed in a supine position that is comfortable for the patient [31]. These facts were recognized more than 30 years ago with the proliferation of breast ultrasound and the correlation of mammographic and sonographic abnormalities, leading to the development of and requirement for accurate ultrasound-guided breast biopsy techniques [11, 32–34]. Like most interventions, the success and accuracy of ultrasound-guided breast biopsy are operator dependent and require good handeye coordination to accurately target the lesion. The procedure of ultrasound-guided breast biopsy can be learned and refined through practice, repetition, and meticulous technique. The use of chicken or turkey breast phantoms with embedded targets is useful for education. It was practiced by early adapters and remains a valid teaching tool today [35]. The safety and efficacy of ultrasoundguided breast biopsy have been well documented throughout the years [36, 37]. Through the practice and development of ultrasound-guided breast biopsy, with radiologic and pathologic correlation of the biopsy specimens, the utility of this procedure over open surgical biopsy has been shown. In fact, the rate of misdiagnosed breast lesions was shown to be comparable to or even better than that of surgical excisional biopsy [38, 39]. Comparative effectiveness research and cost savings have been documented, and the usefulness and utility of ultrasound-guided breast biopsy have been shown, compared with open surgical breast biopsy [40, 41]. With the development of better ultrasound technology, lesions of the breast are better visualized and can be better characterized than they were 20 or even 10 years ago. Improvements in the resolution of ultrasound monitors and improvements in high-frequency transducers developed by industry have increased our ability to see and characterize the breast with greater clarity. A potential abnormality that is now better identified than in the past as a result of these technologic advances is suspicious microcalcification [42]. Even before the advent of today’s advancements, researchers documented ultrasound’s ability to detect microcalcifications of the breast [43]. It is now widely accepted that solid masses or architectural distortion visualized mammographically should

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be characterized further with ultrasound. If a concordant abnormality is identified, then ultrasound-directed core needle biopsy is the procedure of choice to document a pathologic abnormality [44]. Earlier research documented the feasibility of performing ultrasound-guided biopsy of the breast for microcalcifications [45, 46]. The technique for ultrasound-guided biopsy of suspicious breast microcalcifications follows that for ultrasound-guided biopsy of solid masses with a few notable exceptions. It has been well documented that there is statistically significant undersampling of microcalcifications with spring-loaded 14-gauge core biopsy needles for stereotactic-guided breast biopsy [19, 47, 48]. The standard of care for stereotactic biopsy is to perform this procedure using large-gauge vacuum-assisted or mechanical rotating biopsy devices to adequately sample the microcalcifications and adjacent tissue [49]. Furthermore, it can be argued that a requirement for ultrasoundguided biopsy of breast microcalcifications is the use of a large-gauge handheld vacuumassisted or mechanical rotating biopsy device as opposed to a 14-gauge spring-loaded needle that can be used with great accuracy to biopsy larger solid masses [50]. Additionally, marker placement at the site of the biopsy and the use of postbiopsy mammography, to document concordance of the biopsy site with prebiopsy imaging, should be performed in all cases (Fig. 1). A specimen mammogram can also be performed to document that the calcifications are within the specimen and have been adequately sampled before the conclusion of the biopsy procedure. The potential benefits of this procedure are those of patient comfort and lack of radiation exposure, compared with a stereotactic-guided breast biopsy. Additional benefits may be the ability to accurately biopsy microcalcifications in women who are not candidates for a stereotactic biopsy because of the location of the calcifications, breast size, or inability to tolerate the compression and immobility or positioning required of the stereotactic procedure. Therefore, the ability to accurately perform an ultrasound-guided breast biopsy for suspicious microcalcifications may decrease the number of open surgical biopsies required for diagnosis in this cohort of patients. Additional research is required, ideally performed in a prospective manner, to validate this technique as a potential alternative to stereotactic breast biopsy for suspicious microcalcifications.

A Review of Stereotactic Breast Biopsy and the Potential for Stereotactic Lumpectomy Patients with newly diagnosed suspicious microcalcifications seen on mammography or digital tomosynthesis classified as BI-RADS category 4 or 5 will require some form of procedure to make a histologic diagnosis [51]. It is not rare for women with BI-RADS category 3 calcifications to undergo a diagnostic procedure. Reasons include a strong family history of a first-degree relative with cancer, a personal history of cancer or atypia, or the anxiety and discomfort of waiting for followup studies to document stability. In the early 1990s, the standard of care for the diagnosis of these calcifications was a needle or wire localization procedure followed by an open surgical lumpectomy. Twenty years later, the diagnosis is obtained by a minimally invasive imaging-guided procedure. The stereotactic-guided breast biopsy procedure was developed in the early 1990s and was a considerable improvement over the alternative of open surgical breast biopsy. Numerous studies documented the specimen adequacy, rate of agreement between patients who underwent both surgical and stereotactic biopsy procedures, and complications [13–15]. The studies were initially performed using 14-gauge automated spring-loaded biopsy needles. The initial research was performed by interventional radiologists or those practicing breast imaging and interventional procedures. The surgical community followed the radiology community in participating in this research as well. For most of the early research, good quality prospective studies were performed to validate hypotheses and establish a new alternative procedure that changed the way we perform breast biopsy today [52]. Operator experience and the diagnostic requirements for sampling using only five 14-gauge spring loaded cores was studied through a multiinstitutional prospective study by Brenner et al. [53]. The results of that study were actually quite good, with 99% sensitivity reported for invasive breast cancers but only 67% sensitivity for ductal carcinoma in situ (DCIS). The game changed once again with the development of the vacuum-assisted biopsy needle, which allowed larger samples to be obtained and even better concordance between the stereotactic-guided biopsy results and the open surgical pathology findings [26]. The improvements in diagnostic accuracy with the vacuum-assisted needles were

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History and Future of Interventional Breast Radiology particularly in the area of DCIS [19, 54]. Throughout the years, additional predominantly retrospective studies have described the results of the stereotactic biopsies to confirm earlier results and to document the utility of this procedure [48]. Studies have also been performed to retrospectively analyze the differences in diagnostic samples and outcomes as larger size vacuum needles became available. Eby and colleagues [55] concluded that no significant upgrade rate to carcinoma or DCIS at surgery was noted with 11-gauge needles compared with 9-gauge needles in cases of atypical ductal hyperplasia (ADH). What was noted in that article and several earlier studies was an unexpected consequence of the stereotactic biopsy procedure: the stereotactic lumpectomy. The reason for a lumpectomy is to remove the abnormal lesion from the breast. This is precisely what the early physicians performing stereotactic-guided breast biopsy with large-gauge vacuum-assisted needles were finding. This complete removal of ADH, DCIS, and even, in some cases, invasive carcinoma was never the intent of the interventional breast radiologist or surgeon performing these procedures. It just happened. One of the earliest articles by Liberman et al. in 1998 [56] reported removal of the target lesion seen by mammography with an 11-gauge needle in 15 of 51 carcinomas. Of the 15 cases, there was no residual histopathologic evidence of carcinoma in four of the 12 cases of DCIS but residual carcinoma in all three cases of invasive carcinoma [56]. In 1999, Gajdos and colleagues [57] reported that there was complete removal of histopathologic evidence of breast cancer in nine of 52 malignancies. Those authors concluded that, “Complete removal is more likely with removal of a large number of specimens from small areas of mammographic calcifications due to ductal carcinoma in situ” [57]. Another retrospective review by Liberman et al. in 2002 [58] looked at 800 lesions in 797 women 22–88 years old who underwent stereotactic biopsy with an 11-gauge vacuum needle in which the radiologist did not specifically attempt to achieve complete excision of the target. Up to 47 cores were obtained, with eight or more cores obtained in 99% of patients; 466 lesions, including 91 cancers, were completely removed. At surgery, 19 of the 91 women had no residual cancer. More recently, a large retrospective analysis was published in 2010 by Penco et al. [59] of 4086 vacuum-assisted stereotactic breast biopsies using 8- or 11-gauge probes. No re-

sidual cancer was found at surgical excision in 30% of lesions with the initial diagnosis of cancer in which the target lesion was completely removed radiographically. Those authors concluded that vacuum-assisted breast biopsy may not be considered a therapeutic procedure even when the target calcifications are removed. Yet, the cancers were unintentionally removed in 30% of cases [59]. Villa and colleagues [60] performed a retrospective analysis published in 2011 in which 114 of their 1173 consecutive patients who underwent 11-gauge stereotactic biopsy were diagnosed with ADH. Of those, 65 patients’ calcifications were completely removed by the procedure. Of the 65, four were lost to followup and only 1 of 61 (1.6%) had a conversion to a low-grade DCIS after 48 months of follow-up. These authors concluded that, at institutions that can duplicate an underestimation rate of less than 2%, patients with ADH who undergo 11-gauge vacuum-assisted biopsy and who have no residual microcalcifications after the procedure can be managed with mammographic follow-up [60]. In practice today, it is not rare to identify very small groups of suspicious microcalcifications measuring 10 mm or even less. These can be accurately targeted and completely removed with imaging-guided stereotactic biopsy. Those who perform this procedure on a routine basis are also aware, as were our predecessors who were pioneers in this field, that stereotactic lumpectomies are performed unintentionally and not infrequently (Fig. 2). What is now required is new research to find out why and how and for whom this procedure should be done. As Walt Disney said, “We keep moving forward, opening new doors and doing new things, because we’re curious, and curiosity keeps leading us down new paths” [61]. We owe it to our patients and our profession as physicians to be curious. None of the research mentioned to this point was done with the intention of performing an imaging-guided stereotactic lumpectomy. Prospective research using large-gauge vacuum-assisted biopsy devices and targeting small groups of microcalcifications with the intent to remove them and their margins with large numbers of samples should be performed. In fact, according to the newest position statement from the American Society of Breast Surgeons regarding breast cancer lumpectomy margins, “Greater radial width of a negative margin had borderline significance for improvement in local regional recurrence for 1 mm compared to wider mar-

gins, but no significance when adjusted for patients receiving a radiation boost or endocrine therapy” [62]. This means that for invasive or in situ breast cancer, an acceptable surgical margin is greater than or equal to 1 mm. The position statement also goes on to say that reexcision may not be mandatory for focally involved margins or margins less than 1 mm given that, “Many factors, including patient age, co-morbidities, life expectancy, extent of excision, extent of margin involvement, tumor characteristics, and whether the patient will receive adjuvant therapies, should be taken into account before proceeding with re-excision” [62]. This type of research is supported by the literature [63] and should be performed in combination with our surgical and oncologic colleagues to determine whether, in fact, the stereotactic lumpectomy, with or without combination therapy, can be a new minimally invasive treatment of certain cases of ADH, DCIS, and perhaps even invasive breast cancer as an alternative to surgical lumpectomy in a subset of appropriate patients. Thermal Ablation of Benign Fibroadenomas and Breast Cancer Thermal ablation techniques using imaging guidance have become widely accepted over the past 20 years as tools for treating cancer. Although the technology has been widely adapted and accepted for use in organs such as the liver, kidney, and lung, this has not yet been the case for tumors of the breast [64–67]. In the early 2000s, several articles were published describing the efficacy and the establishment of a practice for the cryoablation of benign fibroadenomas of the breast as an alternative to open surgical excision [68–70]. One study by Littrup et al. [71] reported an average pretreatment volume of 4.2 cm, which was reduced to 0.7 cm at 12-month follow-up. This was followed by a report from a prospective FibroAdenoma Cryoablation Treatment registry, composed of 55 practices from across the United States, the results of which were presented at the sixth annual meeting of the American Society of Breast Surgeons in 2005 [72]. The purpose was to evaluate the fibroadenoma cryoablation procedure and outcomes as well as patient satisfaction. The outcomes for 444 treated fibroadenomas were favorable overall, particularly for lesions smaller than 2 cm. Most lesions larger than 2 cm had overall reduction in size at 12 months but still had some palpability in the area of treatment. Overall patient satisfaction at 12



Tomkovich months was 88% [72]. In 2008, The American Society of Breast Surgeons [73] issued a consensus statement on the management of fibroadenomas advocating for both imagingguided percutaneous excision, using a vacuum-assisted device, and the U.S. Food and Drug Administration–approved percutaneous imaging-guided cryoablation of fibroadenomas as viable alternatives to open surgical excision for women seeking treatment. Cryoablation should therefore be considered a primary treatment option for such patients. Through the years, the treatment of breast cancer has evolved from the radical mastectomy to more conservative approaches. These approaches decrease morbidity, improve cosmesis, and generate better patient outcomes [74, 75]. The next logical step in this progression would be to treat certain breast cancers without open surgical procedures but with percutaneous imaging-guided therapy. The possibility of treating breast cancer with percutaneous imaging-guided ablation therapy has been studied by several authors. One of the first studies, by Fornage et al. in 2004 [76], showed complete ablation of the target lesion by ultrasound-guided radiofrequency ablation in 21 patients with tumors 2 cm or smaller. Also in 2004, Sabel et al. [77] reported a multiinstitutional pilot safety study of ultrasound-guided cryoablation in 29 patients, with 100% treatment of cancers smaller than 1 cm. In 2007, Oura et al. [78] reported successful ultrasound-guided radiofrequency ablation under anesthesia for 52 patients with tumors 2 cm or smaller, without resecting the lesions, and no evidence of recurrence in the 6–30 months after the procedure. In 2009, Littrup et al. [79] reported the results of a feasibility study using ultrasoundguided cryoablation to treat breast cancers up to 5.8 cm in 11 patients who refused surgical excision. The patients were treated between 2003 and 2008, with results showing a 95% reduction in ablation volume and no recurrence on follow-up examinations [79]. Manenti et al. [80] confirmed the results of Littrup et al. in 2011 with a series of 15 patients (mean age, 73 years) who underwent ultrasound-guided cryoablation of cancers and then surgical lumpectomy. Results were a success, with complete tumor necrosis in 14 of 15 patients; the one failure was thought to be a technical one. The American College of Surgeons Oncology Group Z1072 clinical cryoablation trial is the largest multicenter trial to date. The trial was designed to determine whether percutaneous ultra-

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sound-guided cryoablation could be successful in ablating stage I breast tumors. A total of 19 centers contributed patients, of whom 87 cancers were evaluable according to the trial guidelines. Before undergoing surgical lumpectomy, patients who met the inclusion criteria underwent MRI before and after cryoablation (Fig. 3). The study found that 100% of patients with tumors smaller than 1 cm treated with cryoablation had no residual invasive cancer on pathologic examination of the targeted lesion. The success rate for cancers of any size was 80.5% [81]. Other modalities have also been reported, such as high-intensity focused ultrasound, laser, and microwave. Compared with cryoablation, which is well tolerated and can be performed with only a local anesthetic, the heatbased ablations usually require some form of general anesthesia. Potential complications of heat-based ablations include skin and pectoral muscle thermal injury and postprocedure pain [82]. Additional prospective multicenter research trials are needed to validate the feasibility studies reported to date with the ultimate goal being the use of imagingguided ablation as a primary treatment for certain patients and certain types of breast cancers without the need for surgical resection. Which patients and which size and type of tumor are still yet to be determined, but the concept of a new primary treatment for breast cancer using imaging-guided ablation is promising. Interventional Radiology of the Breast: Challenges and Opportunities The field of interventional radiology is a dynamic and changing one. It presents many challenges and many opportunities. No more is this true than in the field of breast interventions. Ralph Waldo Emerson wrote, “Do not go where the path may lead, go instead where there is no path and leave a trail” [83]. The path to breast interventions has not historically led through the academic training centers of interventional radiology departments. Yet, the combination of skills and training in imaging and imaging-guided interventions makes interventional radiology perfectly suited for this subspecialty. Interventional radiologists can provide significant value to the field of women’s health and breast interventions by training in and participating in these procedures. Interventional radiologists have been at the forefront of developing many of the procedures that have changed the way we practice medicine today.

Uterine fibroid embolization replaces hysterectomy, vascular stents replace vascular bypass surgery, aortic endografts replace open repair of abdominal aortic aneurysm, and, as outlined in this article, imaging-guided breast biopsy replaces open surgical breast biopsy. As John Kaufman said during the 28th Dotter lecture given at the 2012 annual meeting of The Society of Interventional Radiology, “Arguably, we see innovation as the most important characteristic of our specialty. The contributions of the many brilliant individuals who created IR have dramatically changed how medicine is practiced. These giants looked at the clinical problems of their day, dreamed of solutions using imaging-guided techniques, and provided us with many of the tools and procedures that are now considered the standard of care” [84]. As outlined here, the opportunity exists for new research in ultrasound-guided biopsy of microcalcifications, stereotactic-guided lumpectomy, and ultrasound-guided ablation of breast cancer. So, too, we must “leave a trail” in the field of breast interventions, but we must do so along with our colleagues. There are many brilliant and passionate breast imagers and surgeons who have blazed a trail of their own in the field of breast interventions. Their work has produced some outstanding results and innovations. We must work together to build relationships and therefore draw from each other’s strengths rather than seeking conflict. The new interventional radiology and diagnostic radiology certificate provides a unique opportunity for a change in the traditional interventional radiology curriculum to include breast intervention training and research collaboration with our friends in the breast imaging subspecialty. We stand together at the start of a new era in medicine. Cost effectiveness, comparative effectiveness research, and an aging population are making physicians think differently about what we do. Likewise, we now stand together globally. The research outlined in this text is not limited to the United States but rather is taking place in countries around the world. The disease of breast cancer is a global disease. With the proliferation of communications and information technology and the relative ease of global travel, we all must work together to advance the fight against breast cancer. Through cooperation and collaboration, we will achieve our goal of improving the quality of life for our patients and their families. Through new research and the de-


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History and Future of Interventional Breast Radiology Fig. 1—74-year-old woman with biopsy-proven invasive carcinoma. A, Craniocaudal magnified view of left breast shows microcalcifications (arrow). B, Mediolateral magnified view of left breast shows microcalcifications (arrow). C, Ultrasound image shows corresponding suspicious microcalcifications and small solid component (arrow). D, Echogenic 12-gauge biopsy needle is seen going through calcifications and mass (arrow). E, Postbiopsy mammogram with marker in craniocaudal view confirms concordance (arrow). F, Postbiopsy mammogram with marker in mediolateral view confirms concordance (arrow).

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Fig. 2—51-year-old woman with stereotactic biopsyproven ductal carcinoma in situ (DCIS) with no residual DCIS after surgical excision (stereotactic lumpectomy). A, Magnification mediolateral view of left breast shows new 4-mm suspicious cluster of microcalcifications (arrow). B, Magnification craniocaudal view of left breast shows new 4-mm suspicious cluster of microcalcifications (arrow). C, Stereotactic image shows corresponding suspicious microcalcifications (arrow). D, Stereotactic image of biopsy needle obtained before mechanical firing into breast shows calcifications targeted (arrow). E, Specimen mammogram shows suspicious calcifications removed (arrow) by stereotacticguided lumpectomy. F, Postbiopsy craniocaudal view mammogram shows marker, no residual calcifications (arrow), and concordance with prebiopsy imaging.



History and Future of Interventional Breast Radiology

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Fig. 3—49-year-old woman with invasive carcinoma treated with ultrasoundguided cryoablation. (Courtesy of Attai DJ, Center for Breast Care, Burbank, CA) A, T1-weighted contrast-enhanced fat-suppressed MRI with computer-aided detection shows cancer in right breast. B, Ultrasound image shows mass (arrow) before ablation. C, Cryoprobe is positioned through tumor (arrow) before ablation. Calipers marked A denote approximate measurement of functional portion of cryobprobe still proximal to tumor (1.59 cm), calipers marked B denote approximate measurement of functional portion of cryobprobe through tumor (1.75 cm). D, Ultrasound image shows ice ball formation during cryoablation. Calipers denote visible longitudinal measurement of ice ball after first freeze cycle (3.90 cm). E, T1-weighted fat-suppressed MRI of zone of ablation (A, dotted line) shows no residual mass and cryohalo.


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