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1 Department of Radiology, University of Washington Medical Center, 1959 NE
Pacific, Seattle, WA 98195.
2 Seattle Cancer Care Alliance, 825 Eastlake Ave. E, G4-830, Seattle, WA
98109-1023.
3 Seattle Breast Center, 1560 N 115th St., Ste. 104, Seattle, WA 98133.
Received July 16, 2003;
accepted after revision October 3, 2003.
Address correspondence to X. Chen.
Abstract
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MATERIALS AND METHODS. Thirty-five consecutive breast biopsies performed in 29 women between March 2001 and August 2002 were retrospectively reviewed. For each procedure, an MRI-compatible sheath was placed under MRI guidance using a dedicated breast coil and biopsy guidance system. With the patient out of the magnet, a 14-gauge steel core biopsy needle was used to obtain multiple samples. Lesion characteristics, including size, morphology, and enhancement, were recorded. Histology of all the lesions was obtained; and surgical, imaging, or clinical follow-up was performed.
RESULTS. Targeted masses and enhancing foci ranged from 3 to 17 mm. Regional enhancement ranged from 14 to 70 mm. Thirty-four of the 35 biopsies were technically successful. Histology revealed malignancy in eight lesions (23%), atypical ductal hyperplasia in five lesions (14%), and benign entities in 21 lesions (60%). Surgery confirmed all eight core biopsies with malignant findings. Two of five lesions with atypical ductal hyperplasia were upgraded to malignancy after surgery.
CONCLUSION. This new method of MRI-guided breast biopsy with a 14-gauge stainless steel core biopsy needle and a closed 1.5-T MRI scanner is feasible, safe, and effective and produces satisfactory diagnostic yield. This method offers an alternative to MRI-guided wire localization and to MRI-guided core biopsy with nonferrous needles.
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A subset of breast cancers, known as "MRI-only" lesions, can be detected only on breast MRI and are occult to all three conventional techniques. To make a definitive histologic diagnosis of these lesions, MRI-guided tissue sampling is necessary. MRI-guided tissue sampling can be accomplished either by wire localization and surgical excision or by core needle biopsy [2–10]. Core needle biopsy has several documented advantages over wire localization, including decreased invasiveness, morbidity, and cost [11]. MRI-guided 14-gauge core needle biopsy technique, using MRI-compatible biopsy needles and a 1.5-T scanner, has been reported to have 98% diagnostic accuracy [9]. However, the MRI-compatible biopsy needle has been shown to have less satisfactory sampling efficiency and to be less available and more costly compared with standard 14-gauge core biopsy needles [9].
MRI-guided core needle biopsy using a non–MRI-compatible, but MRI-safe, 16-gauge steel core biopsy needle and a 0.5-T open scanner showed the promising potential of the MRI-safe, steel core biopsy needle [12]. However, the 1.5-T MRI scanner provides higher resolution and better imaging quality than the 0.5-T scanner; the 1.5-T scanner is also more widely available in clinical use.
We previously published a technical note describing our technique with MRI-guided breast biopsy using stainless steel core needles [10]. In this article, we present our clinical experience with 35 MRI-guided breast biopsies of MRI-only lesions, using 14-gauge stainless steel core biopsy needles and a 1.5-T scanner. We discuss the technical feasibility, patient safety, and diagnostic yield of MRI-guided breast biopsy.
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MRI interpretation criteria, assessments, and recommendations were based on the American College of Radiology breast MRI lexicon [13]. For MRI category 4 (suspicious for malignancy) and category 5 (highly suggestive of malignancy) lesions, targeted second-look sonography was always recommended and performed first. If the lesion was visible sonographically, sonographically guided core biopsy was performed. If the lesion was not visible on sonography, as in the case of the 35 lesions included in this article, MRI-guided core biopsy was performed.
Both lesion morphology and enhancement features were analyzed during image interpretation. The enhancement kinetics was assessed as persistent, plateau, or contrast washout.
Equipment and Devices
The 35 MRI-guided breast biopsies were performed with an LX 1.5-T closed
scanner (General Electric Medical Systems). Patients were positioned prone in
a dedicated breast coil, with the affected breast stabilized in a biopsy
guidance device (MRI Devices) by providing moderate compression (Figs.
1 and
2). The biopsy guidance device
also served as the frame of the coordinate system. An MRI-compatible 12-gauge
titanium coaxial sheath (MRI Devices) was used for lesion targeting and
localization as well as for guiding the biopsy needle. The coaxial sheath
consists of an outer titanium cannula and an inner titanium stylet
(Fig. 3). For tissue sampling,
an MRI-safe standard stainless steel 14-gauge disposable core biopsy needle
(Monopty Instrument, C. R. Bard) was used. Through the coaxial cannula,
multiple core samples were obtained outside the bore of the magnet.
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MRI-safe stainless steel biopsy site marker clips (INRAD) were placed in most patients to mark the biopsy site. The marker clip is visible both on MRI, via its useful small imaging artifact, and on mammography. The latter allows mammographically guided wire localization if the biopsy reveals malignancy, atypical ductal hyperplasia, or discordant results.
Biopsy Procedure
As previously described
[10], after written informed
consent was obtained from the patient and IV access was established, the
patient was placed on the closed MRI scanner. The affected breast was
positioned in a dedicated breast coil and biopsy guidance device. A fiducial
marker was placed on the skin through the biopsy guidance device in the region
of the lesion to be sampled (Fig.
4A). The fiducial marker is a small plastic capsule filled with
1:100 solution of gadolinium and saline.
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After localizing sequences were obtained, unenhanced and contrast-enhanced sagittal images were obtained to confirm the persistence of the enhancing lesion noted on the prior MR image (Fig. 4B). The images were reviewed on the monitor; and the locations of the fiducial marker and the lesion along the anteroposterior, superoinferior, and mediolateral axes were recorded in millimeters on a biopsy positioning flow sheet. The difference in the locations (in x, y, and z) of the fiducial marker and the lesion was calculated, and the needle guide was adjusted appropriately along the superoinferior (z) and anteroposterior (y) axes. The mediolateral (x) axis coincided with the depth of the lesion from the incision site. Six centimeters was added to skin-to-lesion depth to account for the space from the hub of the needle guide to the skin.
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The MRI table was moved out of the bore of the magnet, and the needle guide was adjusted to the nearest millimeter. The fiducial marker was removed, the patient's skin was sterilized, and local anesthetic (10:1 lidocaine mixed with bicarbonate solution) was injected. A sterile 12-gauge titanium coaxial sheath was inserted to the calculated depth using the centimeter markers on the shaft of the sheath and a lateral approach. Once the coaxial sheath was in place, the inner stylet was removed. With the coaxial cannula in place, the MRI table was returned to the bore of the magnet.
A limited axial sequence was obtained through the region of the cannula and the lesion to confirm accurate placement of the cannula (Fig. 4C). If corrections were necessary, the patient was rolled out of the magnet and adjustments were made. When the cannula was repositioned, a limited axial sequence was repeated to confirm position. After correct placement of the cannula was confirmed, the MRI table was rolled out of the magnet, and multiple core samples of the lesion were obtained using the stainless steel 14-gauge Bard disposable core biopsy needle through the titanium cannula.
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In most cases, an MRI-safe site marker clip was placed through the cannula after sampling. A final sagittal sequence through the biopsied region was performed to verify the location of the sampling defect and the placement of the site marker clip (Fig. 4D).
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At the completion of the biopsy, the biopsy needle and the coaxial cannula were removed. Manual compression was applied to achieve hemostasis, and a sterile dressing was applied.
Imaging and Histologic Data Collection
The morphologic and enhancement characteristics of each biopsied lesion
were reviewed and recorded in the following terms based on the ACR breast MRI
lexicon [13]: lesion type
(focus, mass, or region), size, shape, margin, location, distribution,
enhancement pattern (homogeneous, heterogeneous, or rim enhancement), and
enhancement kinetics (persistent, plateau, or washout). Biopsy histology was
classified in three categories: malignant (invasive and in situ disease), high
risk (atypical ductal hyperplasia), and benign (including atypical lobular
hyperplasia). Imaging–histologic correlation was performed, and
diagnostic yield was calculated.
Validation of Core Biopsy Histology
All cases of malignant histology led to surgery, lumpectomy, or mastectomy.
Because of well-documented histologic underestimation of atypical ductal
hyperplasia lesions [14,
15], those lesions were
recommended for surgical excision. Imaging–histologic correlation was
performed for all biopsies with benign results to determine concordance. If
the biopsy result was considered concordant with imaging features, follow-up
MRI in 6 months was recommended.
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Core biopsy histology revealed eight malignant lesions: five invasive ductal carcinomas, one mixed invasive ductal and lobular carcinoma, one invasive lobular, and one mixed ductal carcinoma in situ and lobular carcinoma in situ (Table 2). Atypical ductal hyperplasia was shown by histology in five lesions (Table 3). Twenty-one lesions showed benign histology encompassing a spectrum of benign entities (Table 4). Fibrosis was shown in seven biopsies, benign breast tissue in five, fibrocystic changes in four, ductal hyperplasia in two, fibroadenomatous change in one, chronic inflammation in one, and atypical lobular hyperplasia in one.
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Diagnostic Yield
Table 1 summarizes the
diagnostic yield of histology of the 35 biopsies: 23% (8/35) malignancy (seven
invasive malignancy and one ductal carcinoma in situ–lobular carcinoma
in situ); 14% (5/35) atypical ductal hyperplasia; and 60% (21/35) benign
entities (20 benign and one atypical lobular hyperplasia).
Procedure Complications
Thirty-four of the 35 biopsies revealed satisfactory histology. One biopsy
of a 6-mm enhancing mass revealed only skin and subcutaneous fat with no
evidence of breast tissue. These results were considered discordant. Thus, the
procedure success rate was 97% (34/35). No adverse reaction was encountered
during any of the 35 biopsies.
Histology Confirmation
All eight malignant lesions underwent surgery: six mastectomies, one
lumpectomy, and one surgical excision. Malignancy was confirmed in all eight
lesions. The seven lesions with invasive histology had completely concordant
surgical pathology, and the ductal carcinoma in situ–lobular carcinoma
in situ lesion was upgraded to invasive ductal carcinoma
(Table 2).
Four of the five atypical ductal hyperplasia lesions had surgical confirmation: two surgical excisions and two mastectomies (for ipsilateral malignancy). Two atypical ductal hyperplasia lesions were upgraded to invasive ductal carcinoma; one atypical ductal hyperplasia lesion was not changed, and one atypical ductal hyperplasia lesion was downgraded to benign pathology (Table 3). One patient refused any type of surgery and has chosen clinical and conventional imaging follow-up from March 2001 to March 2003.
All 21 benign biopsies were considered concordant with imaging features. The follow-up information of the 21 benign biopsies is summarized in Table 4. Twenty-four percent (5/21) of the biopsies were confirmed by surgery: three prophylactic mastectomies, one mastectomy for ipsilateral malignancy, and one lumpectomy for adjacent malignancy. Twenty-four percent (5/21) of the biopsies had short-term MRI follow-up in 5–12 months that showed resolution (in two cases), decreased size (in two cases), or stability (in one case) of the lesions. Twenty-nine percent (6/21) of the biopsies had negative findings at mammographic follow-up only, which was not the recommended method for follow-up because the biopsied lesions were not visible on mammography. Twenty-four percent (5/21) of the benign biopsies were lost to follow-up.
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We have performed 35 MRI-guided breast biopsies using the combination of an MRI-compatible coaxial sheath and a 14-gauge steel core biopsy needle under the guidance of a 1.5-T closed scanner. Although ours was a small series, our findings suggest that this biopsy technique is technically feasible, effective in sampling, safe for the clinical patients, and satisfactory in diagnostic yield.
The combination of immobilization of the breasts with moderate compression provided by the biopsy guidance device and the use of MRI-compatible (titanium) coaxial sheaths allows consistent and precise spatial localization and targeting. The titanium coaxial sheath produces minimal imaging artifacts, so the targeted lesion remains visible even at its tip. The stainless steel biopsy needle is MRI-safe and allows more reliable, more efficient, and less expensive sampling. The 1.5-T closed MRI scanner provides high imaging quality for lesion characterization and visualization during initial breast imaging and subsequent MRI-guided breast biopsy. The scanner is also commonly available and has become the breast MRI scanner of choice. In addition, any MRI protocol can be used in conjunction with this biopsy method.
Our experience with 35 breast biopsies resulted in 34 definitive histologic diagnoses, corresponding to a 97% biopsy success rate. The biopsy rate for positive findings of 37% (23% malignant, 14% atypical ductal hyperplasia) falls within the range of diagnostic yield of stereotactically and sonographically guided biopsies as well as other reported MRI-guided tissue sampling (wire localization and core biopsy) techniques [2–9].
Our results underscore the reported histologic underestimation and pathologic upgrading related to in situ disease and atypical ductal hyperplasia when biopsy is obtained by a 14-gauge core biopsy device [14, 15]. In our study, 50% of surgically confirmed atypical ductal hyperplasia cases were upgraded to malignancy. It has been reported that 11-gauge vacuum-assisted breast biopsy under stereotactic device can improve diagnostic accuracy [16–20]. MRI-guided 11-gauge vacuum-assisted breast biopsy systems are being tested at several sites in the United States and Europe [21–24]. This technique is expected to result in fewer underestimations of diagnosis with MRI-guided biopsy.
One of the limitations of our study was insufficient confirmation and follow-up of biopsies with benign results: 24% surgical confirmation, 24% short-term (5–12 months) MRI follow-up, 28% mammographic follow-up, and 24% lost to follow-up. Follow-up of benign biopsies is need to determine the false-negative biopsy rate, both immediate and delayed. Long-term follow-up requires a great deal of time and resources, as well as education of patients and referring physicians [15]. A well-accepted imaging follow-up protocol of benign biopsies of these MRI-only lesions has not yet been established.
In summary, this technique using an MRI-compatible coaxial sheath for lesion targeting and a 14-gauge stainless steel core biopsy needle for tissue sampling under MRI guidance with a 1.5-T closed scanner provides a safe and effective method for breast biopsy. The diagnostic yield is comparable to that of other imaging-guided breast biopsy techniques. The availability of the 1.5-T MRI scanners and 14-gauge stainless steel core biopsy needles not only renders the method less costly and more practical but also promises wider potential application.
Acknowledgments
We thank Bonnie Thursten, John McCloskey, and Denise Echelard for their
contributions to the success of this project and Tamara Fernando and Sue
Peacock for their invaluable assistance in the preparation of the
manuscript.
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