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10.1245/s10434-006-9076-y
Annals of Surgical Oncology 14:148-156 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Hematoma-Directed Ultrasound-Guided (HUG) Breast Lumpectomy

Margaret Thompson, MD1, Ronda Henry-Tillman, MD1, Aaron Margulies, MD1, Jeff Thostenson, MS2, Gwen Bryant-Smith, MD3, Robert Fincher, MD3, Soheila Korourian, MD4 and V Suzanne Klimberg, MD1,3,4

1 Division of Breast Surgical Oncology, Department of Surgery, University of Arkansas for Medical Sciences, Little Rock, AR, United States
2 Department of Biostatistics, University of Arkansas for Medical Sciences, Little Rock, AR, United States
3 Department of Radiology, University of Arkansas for Medical Sciences, Little Rock, AR, United States
4 Department of Pathology, University of Arkansas for Medical Sciences, Little Rock, AR, United States

Correspondence: Address correspondence and reprint requests to: V. Suzanne Klimberg, MD; E-mail: klimbergsuzanne{at}uams.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCE
 
Background: Needle localization breast biopsy (NLBB) is presently the primary means of localizing non-palpable lesions. Disadvantages of NLBB include vasovagal episodes, patient discomfort, and miss rates. Because hematomas naturally fill the cavity after vacuum-assisted breast biopsies (VABB), we hypothesized that ultrasound (US) could be used to find and accurately excise the actual biopsy site of non-palpable breast lesions without a needle.

Methods: This is a retrospective study from January 2000 to July 2005. Electronic chart review identified patients with non-palpable breast lesions detected by means of mammogram who then underwent lumpectomy via NLBB or the hematoma-directed ultrasound-guided technique (HUG). HUG involved localizing the hematoma with a 7.5-MHz US probe and using the "line of sight" technique straight down toward the chest wall. A block of tissue encompassing the hematoma was then excised.

Results: Localization procedures were performed in 186 patients—63 (34%) via needle localization and 123 (66%) via HUG. The previous VABB site in 100% of patients was successfully excised using HUG, 65 of 123 (53%) were benign and 58 of 123 (47%) were malignant; margins were positive in 13 of these 58 (22%). NLBB was successful in 100% of patients, 44 of 63 (70%) were benign and 19 of 63 (30%) were malignant; margins were positive in 14 of these 19 (73%). Margin positivity was significantly higher for NLBB than HUG (P = 0.0001, Fisher Exact).

Conclusions: This study suggests that HUG is more accurate in localizing non-palpable lesions than NLBB. By eliminating the additional procedure needed for NLBB, HUG may also be more time- and cost efficient. HUG makes VABB not only a less invasive diagnostic procedure, but also a localization procedure.

Key Words: Breast • Hematoma • Ultrasound • Biopsy • Lumpectomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCE
 
In the United States, more than one million breast biopsies are performed annually due to increased screening mammography.1 Non-palpable abnormalities comprise an increasing number of these biopsies and less than half are visible on ultrasound (US). 2 These non-palpable lesions have traditionally been biopsied by means of needle localization breast biopsy (NLBB) or stereotactic core needle breast biopsy (SCNBB).3

NLBB has been the primary technique for excision of non-palpable lesions. However, it has some inherent problems. Miss rates of 0–22% of NLBB have been reported, in part due to the fact that clips used for localization after vacuum-assisted breast biopsies migrate from the biopsy site.4–6 Not only is the wire uncomfortable for the patient, but vasovagal reactions have been reported in 10–20% of patients.4–7 NLBB also requires coordination between the surgeon and radiologist, which can lead to scheduling difficulties and subsequent delay in treatment. Other surrogate markers have been used including clips,8,9 coils,10 and radioactive seeds,11 but all require a second localizing procedure and, thus, have an inherent error.

After vacuum-assisted breast biopsy (VABB), the biopsy cavity naturally fills with a hematoma that can be visualized on US. Therefore, we hypothesize that this hematoma is a physiological surrogate marker for the lesion and can be used to localize lesions intraoperatively for excision. Thus, the hematoma ultrasound-guided excision (HUG) is more advantageous than NLBB because it eliminates a second procedure for localization, the patient avoids the discomfort of a wire/needle in her breast, and it lessens scheduling problems between surgery and radiology.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCE
 
Study Population
This was an IRB-approved, single-institutional, retrospective study from January 2000 to July 2005. Patients with non-palpable breast lesions were identified via electronic chart reviews. These patients underwent mammograms that had detected calcifications or masses. They then underwent stereotactic or US-guided breast biopsy.

Radiological Procedure
US-guided VABB
After localizing the lesion using the 7.5-MHz US transducer (Fig. 1Go), local anesthesia was administered to the skin, along the pathway, and just beyond the lesion. A 5-mm incision was then made in the skin. Using real-time US imaging, an 8- or 11-gauge vacuum-assisted needle was advanced just posterior to the lesion at a horizontal plane to the skin along the axis of the transducer. At least five biopsy samples were taken. Often the entire lesion is removed.


Figure 1
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  		FIG. 1. Intraoperative draping of 7.5-MHz probe and positioning over the lesion.

 
Stereotactic VABB
Stereotactic-guided VABB was used for lesions that could not be visualized with US. After placing the patient in the prone position with compression, two stereotactic views 30 degrees apart were taken to localize the lesion. The skin and needle track were anesthetized with lidocaine and a 5-mm skin incision was made. An 11-gauge vacuum-assisted biopsy needle was then advanced to the margin of the lesion. A minimum of 12 biopsy samples were obtained at 1-h increments from 1200 hours to 2300 hours Post-biopsy images and a specimen radiograph for calcifications were taken to ensure adequate sampling (Fig. 2Go). A clip was placed at the biopsy site. Post-clip craniocaudal and 90-degree images were then taken to localize the clip in relation to the biopsy site and to assure the lesion was removed.


Figure 2
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  		FIG. 2. Pre- and post-stereotactic localization and removal of non-ultrasound visualized mammographic calcifications.

 
Needle Localization
Pre-operative needle localization was performed under radiographic or US guidance for those patients scheduled for NLBB. During the learning phase, ten patients underwent needle localization, and this was used as a back-up to HUG. The shortest distance to the lesion was determined using the original mammogram or US images. For mammographic needle localization, a compression plate with an alphanumeric grid was positioned on the breast and the lesion’s depth was estimated using digital imaging and orthogonal views. The skin was then anesthetized with lidocaine. A Homer Mammalok needle (Medical Device Technologies, Inc., Gainesville, Fl) containing a wire was advanced just distal to the lesion. The wire was then advanced and locked into place just posterior and distal to the index lesion. Post-localization craniocaudal and 90-degree images were taken to ensure adequate placement. The needle and wire were left in place to serve as a guide for the removal of the lesion. A specimen radiograph was reviewed to ensure that the lesion was removed (Fig. 3Go).


Figure 3
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  		FIG. 3. Mammographic imaging of needle localization and subsequent specimen mammogram after excision.

 
Surgical Procedure
NLBB
After undergoing needle localization in the radiology suite, patients were then brought to the operating room. A sterile 7.5-MHz linear array transducer was sometimes used to assess the breast, needle, and wire tip location. The area of concern was then resected using the needle tip for localization. Specimen US was sometimes performed, but all specimens were sent for a specimen mammogram.

HUG
At the time of surgery, a sterile 7.5-MHz linear array transducer was used to localize the hematoma in the breast (Fig. 4Go), and this was correlated with the mammogram. The mammogram is used to triangulate the position of the lesion in the breast. The patient initially undergoes US sitting upright in the position the mammogram was performed. The skin is marked, the patient placed in the supine position and another US of this site is performed. After making the incision directly over the hematoma and using the "line of site" technique, dissection is carried straight down toward the chest wall to a depth determined by lateral US. A block of tissue encompassing the hematoma is then excised visualizing a 1-cm margin. Specimen US is performed ex vivo (Fig. 5Go). Direct observation of the hematoma grossly (Fig. 6Go) and microscopically also confirms removal of the targeted lesion. Specimen mammograms were used to confirm excision of migrated clips.


Figure 4
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  		FIG. 4. Sonographic visualization of hematoma in the breast.

 

Figure 5
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  		FIG. 5. Ex vivo specimen ultrasound.

 

Figure 6
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  		FIG. 6. Gross of the hematoma-filled stereotactic core needle breast biopsy (SCNBB) site.

 
Pathology
Margins were assessed on all sides (superior, inferior, anterior, posterior, medial, and lateral) intraoperatively by touch preparation cytology. Six different colors were used to ink the six different margins. Re-excision was performed at the time of the original operation on any intraoperatively positive margins. Hematoxylin and eosin (H&E) staining was then performed and the specimen serially sectioned at 3-mm intervals. Positive margins were defined as less than 1 mm, close margins as those between 1 mm and 3 mm, and negative margins as those greater than 3 mm. The hematoma and lesion were confirmed on permanent pathology by H&E staining.

Statistics
The Fisher Exact test was used to calculate the statistical significance of margin positivity between NLBB and HUG.12 The statistical significance of the number of days to surgery was calculated using the Rank Sum test, and the Chi-square was used to determine whether there was a statistical significance in the number of patients requiring additional intraoperative margin excision.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCE
 
Study Population
Electronic chart review identified 186 patients who underwent localization procedures by two Breast Surgeons at our institution from 2000 to July 2005. NLBB was performed in 63 (34%) and HUG in 123 (66%) of these patients. (See Table 1Go for presentation characteristics of the patients, P = n.s.) The mean age of the patients was 54.4 years (range 30–86 years); 92 (75%) of the HUG and 44 (70%) of the NLBB patients were more than 50 years old. Microcalcifications were present in 79 (64%) patients in the HUG group and in 47 (75%) in the NLBB group. The majority of patients in each group (85% HUG and 84% NLBB) had BIRADS 4 mammographic findings. In the HUG group, the indications for surgery consisted of 27 (22%) patients with a VABB diagnosis of atypia, 38 (31%) in situ, and 27 (22%) invasive. In the NLBB, 6 (10%) patients had a surgical indication of atypia, 9 (10%) in situ, and 3 (5%) invasive.


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  		TABLE 1 Presentation characteristics of patients undergoing hematoma ultrasound-guided excision (HUG) and needle localization breast biopsy (NLBB)
 
Radiological Procedure
In 2000, we performed 27 NLBBs compared with only 19 HUGs. By December 2004, the number of HUGs performed per year increased to 32, compared with only 6 NLBBs. Over the study period, as we continued to perfect our technique, the HUG procedure increased from 41% to 84% of the total open procedures performed for non-palpable lesions. Of the NLBB patients, 28 (44%) had no pre-surgical core biopsy for reasons such as significant comorbidities or weight limitations of the stereotactic table.

Surgical Procedure
The mean number of days from VABB to surgery was 19 (± 3) days in the HUG group and 42(± 20) days in the NLBB group (P = 0.002). The prolonged time interval from the core biopsy to NLBB (~6 weeks) may have led to non-visualization of the hematoma, thus leaving NLBB as the only option for open excision. Confirmed by specimen mammograms (Fig. 3Go), NLBB was successful in 100% of patients. The previous VABB biopsy site was also successfully excised in 100% of patients using HUG.

Pathology
Using HUG, we obtained 65 of 123 (53%) benign lesions and 58 of 123 (47%) malignant lesions. Benign lesions consisted of papillomas, sclerosing adenosis, and fibroadenomas. High-risk lesions included atypia and lobular carcinoma in situ (LCIS). Malignant lesions consisted of ductal carcinoma in situ (DCIS), infiltrating ductal, and infiltrating lobular carcinoma. Margins were negative in 39 (67%), close in 6 (10%), and positive in 13 (22%) patients. Using NLBB, we obtained 44 of 63 (70%) benign lesions and 19 of 63 (30%) malignant lesions. Margins were negative in 5 of 19 (27%), close in no patients, and positive in 14 of 19 (73%). Margin positivity was significantly higher for NLBB than HUG (P = 0.0001). (See Table 2Go for surgical and pathological characteristics.) The mean tissue volume excised with HUG was 96 (± 16) cm3 and 88 (± 21) cm3 with NLBB. The mean tissue weight excised with HUG was 56 (± 12) g and 51 (± 18) g with NLBB. The number of patients requiring additional margin excision at the time of surgery was 71 (57%) for HUG and 24 (38%) for NLBB. In all patients with invasive cancer, the average tumor size was 9 (± 5) mm for HUG and 10 (± 7) mm for NLBB.


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  		TABLE 2. Surgical characteristics of patients undergoing hematoma ultrasound-guided excision (HUG) and needle localization breast biopsy (NLBB)
 
Complications
There were no immediate or long-term complications secondary to NLBB or HUG.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCE
 
Prior to 1990, NLBB was the only diagnostic technique available for the localization of non-palpable lesions requiring open excision. Parker et al. then introduced SCNBB, which has proven to be highly accurate, less invasive, and less costly than NLBB.1,13–15 When cancer is diagnosed prior to definitive procedure via SCNBB, margin clearance is also improved.1,16–20 Until recently, NLBB was also the only available method to use after a SCNBB when further surgery was required secondary to a diagnosis of cancer, atypia, or when there was discordance between the mammogram and the pathological diagnosis.21 However, NLBB has its drawbacks, including miss rates of 0–22%;4 a positive margin rate between 40% and 75%; wire transection, dislocation, or migration;5 and scheduling difficulties. Also, the patient may experience the anxiety and discomfort of having a needle/wire in the breast while awaiting the surgical procedure.4–7 In addition, vasovagal reactions have been reported in approximately 20% of cases.4–7

Because of the numerous disadvantages of NLBB, several authors investigated the use of intraoperative US in an effort to avoid the use of NLBB.22–24 The technique evolved from one of simply marking the skin to one of interactive use of US in the patient using "line of site" to facilitate accurate removal of the lesion. Subsequently, the use of preoperative wire localization and intraoperative US were compared; while 100% accuracy was reported in both groups, a smaller mean volume of tissue excised and more adequate margins were reported in the US group.7 There are many benefits of intraoperative US-guided excisional biopsy for both palpable and non-palpable lesions, including (1) immediate documentation of removal of the suspect lesion; (2) no additional discomfort to the patient; (3) no requirement for pre-operative localization; (4) no requirement for use of radiation; and (5) US can be used to immediately assess margin status in the specimen.25 A consistent finding of intraoperative US has been the ability to obtain better margin clearance.26,27

Perhaps the major disadvantage of NLBB is that the technique can have a positive margin rate of 40–75%, necessitating a second operation.20 Numerous reports have shown that positive surgical margins can lead to local recurrence (LR)28–31 and decreased survival.32 Although the width of margins necessary for breast cancer removal is highly debated,33 in a very well-conducted although by nature retrospective study by Freedman et al, patients with close margins of less than 3 mm were at an equal risk of ipsilateral recurrence to those with a positive margin.30 In addition, not obtaining negative margins signifies the need for a second surgery, which can be anxiety provoking. Also, as additional tissue is removed, the cosmetic result is worsened.34 Thus, the importance of obtaining negative margins is the primary goal of breast conservation surgery.

The problem is that most mammographic lesions are not visible using US. Multiple techniques have been developed to convert non-US-visible lesions to US-visible lesions. The Gel Mark Ultra biopsy site marker system (SenoRx) is composed of biodegradable pellets containing carbon dioxide bubbles that make the marker visible on US.35 The pellets are eventually degraded and reabsorbed, leaving behind a permanent stainless-steel clip. Although delayed migration has been described,36–42 Nurko et al. found this marking device to have a significant reduction in positive margins.43 Other surrogate markers such as activated charcoal injected into the biopsy site and needle tract have been described.44 Fajardo described 13 cases in which placement of embolization microcoils helped localize the site of breast lesion removed during stereotactic core biopsy.10 Radioactive seeds have also been placed at the site of the lesion using radiographic guidance to excise the lesion.45 Use of titanium and steel clips are also utilized. However, clips are associated with significant migration. Using the Pythagorean Theorem to accurately calculate the movement in space of the clip, Kass et al. demonstrated that the clip moved more than 20% in a quarter of the patients and at least 1 cm in half of the patients.46 From this finding, they concluded that clip movement may contribute to the high positive margin status of standard NLBBs.

Another localization technique is radio-guided occult lesion localization (ROLL). Gennari and colleagues described ROLL as the injection of technetium-labeled colloid into a breast lesion 24 h pre-operatively, taking planar scintigraphy images with a gamma camera, superimposing this image on the mammogram, at which time the hot spot is then shown to correspond to the lesion.47 ROLL was reported to be practical, cost comparable, and cosmetically pleasing; because exposure to radioactivity is very small, it is safe for both patients and staff.48 In a study involving 110 non-palpable breast lesions, Zgajnar et al. described ROLL as superior to NLBB in that ROLL obtained wider surgical margins, but with lower average specimen weight.49

The problem with all the aforementioned techniques is that that all require a second procedure to localize the occult lesion. A second procedure automatically introduces error of placement. Clips or coils, radioactive or not, are subject to movement or misplacement. We therefore sought to identify the natural hematoma caused by SCNBB that often in our experience was palpable. Our initial pilot study in 2001 included 20 patients whose post-VABB hematomas were successfully localized and excised using intraoperative US.3 Our current study of 123 patients suggests that HUG is more accurate in localizing non-palpable lesions than NLBB. HUG also has many other benefits over NLBB. By not requiring placement of a localization needle or wire, the need for an additional procedure is avoided. This reduces the potential risk of complications and additional cost to the patient. The discomfort of having a needle or wire in the breast is also avoided. Another benefit of HUG is that it makes scheduling uncomplicated between radiology and surgery. Also, HUG does not require injection of any additional material, as with the ROLL technique, which again, adds an additional procedure.

Our data show that HUG allowed better margin clearance, perhaps because intraoperative specimen US permits direct real-time visualization of all six margin depths in relation to the index lesion (Fig. 5Go). As a direct consequence, more patients required additional intraoperative margins to be excised after the main mass removal with HUG than with NLBB. This advantage of using intraoperative US to visualize close margins or additional suspicious tissue allowed the immediate removal of potentially malignant satellite lesions and adequate margin clearance. Altogether, this possibly resulted in the significantly lower margin positivity on final pathology for HUG than for NLBB.

There are no technical limitations for HUG with regard to the patient’s body habitus. A potential disadvantage of the HUG procedure is the limited time of up to 5 weeks post-biopsy before most hematomas reabsorb. However, this is similar to other techniques, except for clip placement. Time to reabsorb can be much longer when the hematomas are larger. In our previous study, the time from VABB to surgery was as long as 56 days.3 If the time to surgery is longer than 1 month, we recommend preoperative US to ensure the hematoma is still present. If it is not, then the clip placed with the SCNBB can then be used. Our significant trend away from NLBB is demonstrated in our data. Another caveat of HUG is that the technique requires the surgeon be experienced with the use of US. Therefore, it may be helpful initially to have a needle in the breast as back-up during the early stages of using this technique. In fact, we use US when performing NLBB as it gives a better idea of needle position at the time of excision.

In summary, HUG does not require an additional procedure, unlike other surrogate methods, making the SCNBB a localizing procedure as well as a diagnostic procedure. We think because the hematoma forms in the actual biopsy cavity that this localization technique is more accurate than others. Our data demonstrate that margin clearance is significantly improved with HUG.


   FOOTNOTES
 
Margaret Thompson: Supported by the Virginia Clinton Kelley/ Fashion Footwear Association of New York Breast Cancer Research Fellowship Aaron Margulies: Supported by the Susan G. Komen Breast Cancer Clinical Fellowship

Received for publication March 9, 2006. Accepted for publication April 5, 2006.


   REFERENCE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCE
 

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