Well-qualified mammography has the best sensitivity for early detection of nonpalpable breast cancer, but the specificity is low, and about 10% of breast cancers are not found in mammography.(1) Biopsy is usually required to make definite diagnosis of nonpalpable lesions detected by mammography. But, most of the microcalcifications on mammography are not or are barely visible on ultrasound imaging. Therefore, excisional biopsy or vacuum assisted core biopsy under stereotactic or mammography-guided wire localization is usually performed for those lesions.(2-7)

Ultrasonography is limited for detecting microcalcifications, which is due to low contrast resolution; however, ultrasonography detects microcalcifications associated with other findings, such as mass or ductal changes.(8-10) In general, patients prefer ultrasound-guided (Sono-guided) procedures to mammography-guided (Mammo-guided) procedures, as patients tend to be more comfortable with the supine position, breast is not compressed, and the procedure is less time-consuming. In addition, no ionizing radiation is used, the needle insertion site is more flexible, and real-time observations can be made.(11, 12) For these reasons, Sono-guided core needle biopsy (CNBx) or vacuum-assisted breast biopsy (VABB) are most frequently used for microcalcifications identified on ultrasonography.(9,13-18)

Although the combination of a VABB and a prone-type biopsy table with stereotactic attachment is preferred biopsy procedure, such devices are quite expensive and sophisticated. Most small hospitals and private clinics are unable to these devices, especially those in which medical expenses are strictly regulated by the government such as Korea and Japan. Another way to perform stereotactic biopsies without a stereotactic prone table is to use a Sono- or Mammo-guided J-wire localization instead. However, only a limited number of reports with a small number of patients have been published regarding the results of using this method with VABB.(9, 12) Therefore, the value of Sono-guided VABB for mammographic calcification has not been validated yet. We reported our initial experience using this procedure on 2005.(19) This article reports our 14-year experience with about 1,400 cases.

A total of 1,364 patients were classified under Breast Imaging Reporting and Data System (BI-RADS) category 4 between January 2004 and March 2018 at our clinic (Park Surgical Clinic, Suwon, Korea). Microcalcifications were classified on mammograms immediately by Surgeons. The Mammographic calcification was categorized as probably benign (BI-RADS 3), suspicious (BI-RADS 4) or highly suggestive of malignancy (BI-RADS 5) despite of subcategorization of BI-RADS 4 (4a, 4b, 4c). Category 4 subdivisions does not used in our study. All these category 4 cases were recommended for biopsy.

We evaluated whether suspicious microcalcifications were visible by ultrasonography and feasible to biopsy under Sono-guidance. The biopsy procedures were described previously (Fig. 1).(19) All patients were biopsied with Sono-guided VABB in a supine position without stereotactic device. In case of the microcalcifications were clearly visible on ultrasonography, Sono-guided VABB was performed directly without wire-localization. However, most of the microcalcifications were just suspicious or were not clearly identified in the ultrasonography. In most of these cases, the J-wire was inserted after local anesthesia with 2% lidocaine under ultrasound guidance. The location of the wire was positioned at the suspicious site of microcalcification. The location of the wire was confirmed to be on the target by the mammography. An image with the two spot images was utilized to localize the precise position of the microcalcification and J-wire. If the position of the wire is different from the calcification position, another J-wire was inserted several times more after local anesthesia to determine the position (average 1.4 times, 1-5 times).

When the wires were well positioned corelated with location of calcification, the VABB probe was inserted along the hyperechogenic shadow(s) of J-wire on ultrasound image, and VABB was performed after remove the J-wire(s). The VABB was performed under Sono-guided handheld technique. All the tissues obtained by VABB were examined by specimen mammography to confirm microcalcification. The VABB probe was not removed until calcification was retrieved. If calcification was not retrieved, VABB was repeated to the surrounding area. After biopsy, hemostasis was conducted by compressing the breast with hand for 5-10 min and elastic bandage was applied.

Many experienced surgeons did this method for 14 years, but the corresponding author, who is a president of this clinic did this procedure in most cases. We usually spent about 30 minutes to complete a biopsy procedure. The presence of microcalcification was confirmed radiographically by taking an X-ray image of the obtained biopsy materials. Biopsy failure was defined as technical failure of targeting or sampling of microcalcifications because of absence of calcification on specimen mammography.

If the pathological diagnosis was atypical ductal hyperplasia (ADH), generally no further surgical biopsy was performed except for large diffuse lesions. Follow-up examination was performed after 3 and 6 months. If a diagnosis of cancer was made, definitive surgery was performed.

Oral informed consent was obtained from all biopsied patients.

The localization J-wire needle was a 20 G, 7.5 cm Homer Mammalok^Ⓡ (Medical Device Technologies, PA, USA) and 7.5 cm Caloc^Ⓡ (Medical Park Inc., Yongin-si, Gyeonggi-do, Korea). In early days of the study we used Mammalok^Ⓡ, but we are currently using the Caloc^Ⓡ only recently. The ultrasound equipment used a high-resolution close-range ultrasound (Philips Ultrasound, USA) with a 5-12 MHz linear transducer. VABB equipment used Mammotome^Ⓡ (Devicor Medical Products, Cincinnati, OH, USA) until June 2014 (908 cases), and since then Bexcore^Ⓡ (Medical Park, Yongin-si, Gyeonggi-do, Korea) has been used (491 cases) only.

The average age of patients from whom the tissues were actually obtained was 44.5 years (range 20-75 years). 740 lesions (52.9%) in left breasts, 659 lesions (47.1%) in right breast.

In only 8 out of 1,399 lesions, calcification was well observed within associated mass or dilated ducts. In most cases (1,391 cases), calcification was not observed at ultrasound image (just suspicious microcalcification lesion in 804 cases).

In most cases (1,358 cases), J-wire were inserted under Sono-guided initially (Fig. 2), and 28 cases were converted to Mammo-guided because the position of wire did not match the position of calcification. However, in 41 cases in which microcalcification was not identified in ultrasonography and not suitable for Sono-guided localization, J-wire was inserted under Mammo-guided from the beginning (Fig. 3, 4). The average number of J-wire insertion to acquire microcalcification in the VABB specimen per biopsy was 1.4 (range 0-5). Microcalcifications were confirmed radiographically in the obtained tissue of 1,360 (97.2%) of 1,399 biopsies in which the tissue from lesions with microcalcifications. The 39 cases (2.8%)

The pathological diagnoses of VABB were as follows (Table 1). Among 1,399 diagnoses, 33 were invasive cancer, 155 were carcinoma in situ, and 1,211 were benign disease (including ADH in 14). Among the lesions diagnosed as benign diseases, except for ADH, we found 46 mucocele-like tumors and 25 intraductal papilloma. Although those lesions are now regarded as high risk, we did not perform surgical biopsies for them. Out of 153 lesions diagnosed as DCIS by VABB biopsy, 3 invasive cancers were found on another quadrant of the breast after definitive mastectomy. Finally, 188 (13.4%) lesions were diagnosed as malignant (32 invasive ductal carcinomas, 153 DCISs, 2 lobular carcinoma in situ, 1 mucinous carcinoma), while 1,211 were benign (including 14 ADHs).

All 1,211 benign lesions were not removed surgically shortly after the VABB, but were follow up at least once by palpation, mammography and ultrasonography. No cancers developed from the lesions that were diagnosed as ADH by VABB but not surgically biopsied, and from those of other types with high risk. All these benign cases were followed up every 6 months or every year for mammography and ultrasonography. There were no abnormal findings or malignant tumors to date.

The purpose of screening mammography is detection of early stage breast cancers that are usually nonpalpable. As the majority of very early breast cancers do not show mammographic and sonographic findings typical of cancers, it is usually necessary to perform biopsy and make a histological diagnosis for mammographically detected suspicious lesions. The common methods to perform biopsy for lesions with microcalcifications are stereotactic core needle biopsy (including VABB) and surgical excision under localization (mammography guided).

Currently, many papers regarding stereotactic VABB using a prone table have shown outstanding results.(4,6,20-22) However, several problems remain, including the high cost of prone tables. Another problem is the large space required for the prone table, even though it cannot be used for examinations other than breast needle biopsy. Even if the upright-type stereotactic add-on unit has helped to overcome these drawbacks, the combination with a mammography unit and wire is adaptable to localization of microcalcification for VABB.

It is still unclear whether the combination of the Sono-guided VABB and wire-localization is practically feasible, and the diagnoses made with the tissue thus obtained with the combination are correct. Currently, a very limited number of reports with a small number of patients have been published regarding this combination. Its value must thus be confirmed, especially when using a localization wire. The present report has shown our 14-year experience of about 1399 biopsies with this combination, and this is the largest number reported among those using the localization wire and Sono-guided VABB.

The retrieval rate of the microcalcifications (97.2%) from the microcalcified lesions in this combination was comparable to those in previous studies. (6, 9, 14, 15, 18, 22) The time required for this procedure was 30-40 minutes per biopsy. We therefore can conclude that the combination of a Sono-guided VABB and a Wire-localization without stereotactic device is feasible. We conclude that the accuracy of the biopsy performed with the combination of the VABB and wire-localization is acceptable.

The 39 biopsy failure cases (2.8%) were technically infeasible. Previous studies reported technical feasibility rates of 93-99% (23-25) and vasovagal reaction rates of 0-2% in the prone position.(6, 23) The biopsy failure rate for Stereotactic-guided VABB can differ according to patient’s position. The prone position, which is used in most institutions, is reliable and accurate but requires significant space and is relatively expensive. Some institutions prefer the sitting or decubitus position, but they can present problems due to the relatively high frequency of vasovagal reactions and patient’s motion.(23, 26, 27) Digital breast tomosynthesis-guided biopsies are performed at some institutions using the lateral decubitus position, and a higher biopsy success rate in less procedure time was reported compared with prone.(25)

The complications we experienced consisted mainly of subcutaneous bleeding with or without hematoma. The risk of subcutaneous bleeding is thought to be the same between the stereotactic prone tables and this our method. All the bleeding cases we experienced were self-limited.

The calcification lesions associated with mass might have been biopsied by a Sono-guided approach in a way that was less stressful to the patients than the stereotactic approach. Among the all 1,399 calcification lesions, most of them (1,391 cases, 99.4%) were not well identified by ultrasonography. However, 804 cases were identified as suspicious calcification on ultrasonography.

There are some limitations in this report. First, this study was performed as a part of clinical practice in a single center, not as a protocol study. Also, all procedures including mammography reading, ultrasonography, and J-wire localization were performed by experienced surgeons only. Further study with a larger number of patients from multiple centers is needed to compare the overall diagnostic outcomes of the various biopsy methods. Second, breast ultrasonography is an operator dependent procedure and reproducibility is dependent on individual skill of the doctor. Inter-operator variability was not evaluated in this study.

In conclusion, the Sono-guided VABB technique using the combination of the wire-localization without a stereotactic system is cost- and space-effective, safe and accurate, and it should be regarded as one of the standard biopsy methods for mammographically detected microcalcifications.