Unveiling Tissue Marker Migration in MRI-Guided Vacuum-Assisted Biopsies: Frequency, Factors, and Implications

doi:10.21203/rs.3.rs-3220017/v1

Purpose

To evaluate the frequency and factors associated with clip migration in MRI-guided breast biopsies.

Methods and materials

We retrospectively evaluated all MRI-guided biopsies performed between January 2013 and December 2020 in our institution for clip migration. Only patients with follow-up breast MRI showing the clip were included in the study. Migration was defined as > 1 cm movement from the target lesion. Migration frequency and directions were recorded. Different factors associated with clip migration were analyzed using statistical tests as appropriate.

Results

A total of 291 biopsies in 268 women were included in the study with 31 migration events recorded (11%, 95%CI 7–15). All migrations occurred along the biopsy tract, 30 of them distal from the tip of the needle (97%). More than 50% regional fat (around the target lesion) was the strongest factor associated with migration, seen in 21/140 (15%), compared to 10/150 (7%) with less than 50% local fat (P = 0.023). Global fatty breast was more loosely associated with migration, showing borderline significance (P = 0.06). Other factors did not correlate with clip migration, including lesion size, depth or location, pathology result, breast thickness or biopsy approach.

Conclusion

Although clip migration following breast MRI-guided biopsy is an uncommon event, it occurs more often when the target lesion is surrounded by fat, with the clip usually displaced away from the biopsy needle. This information could be valuable for pre-surgical localization and surgical planning.

Magnetic resonance imaging

MRI vacuum assisted biopsy

Breast Neoplasm

Tissue marker placement after percutaneous breast biopsy is commonly used to enable accurate localization of lesions before surgery[1, 2]. Several studies have shown that clip migration after stereotactic vacuum-assisted biopsy (SVAB), defined as > 10mm displacement away from the biopsy cavity, is not rare [3–10]. Most cases of tissue marker displacement are believed to be caused by the "accordion effect", which is movement of the marker along the needle track immediately after the breast is decompressed [1, 11–13]. Significant migration may confound pre-surgical localization, especially in cases associated with complete removal of the lesion during biopsy.

Due to its high sensitivity in detecting breast cancer, magnetic resonance imaging (MRI) is commonly used for screening high risk patients and pre-operative staging[14, 15]. As a results, more lesions that are seen only on MRI and occult on mammogram and ultrasound (US) are detected, leading to more MRI-guided vacuum-assisted biopsies (MVAB) being performed in clinical practice [16–18]. Tissue markers are commonly utilized following MVAB to assist in the subsequent surgical removal process, much like the SVAB procedure. As the MVAB technique is not significantly different from the SVAB technique, it seems reasonable to expect a certain percentage of tissue markers migration after the procedure. However, to the best of our knowledge, only one study has focused on tissue marker migration post MVAB [19].

The purpose of this study is to evaluate the frequency of tissue marker migration after MVAB, and identify factors associated with clip migration.

Patients and inclusion criteria

The research ethics committee of the local institution review board granted approval for this retrospective study, and the requirement for informed consent was waived.

We retrospectively evaluated all MRI-guided biopsies performed between January 2013 and December 2020 in our institution for clip migration. We exclusively included cases in which breast MRI examinations were accessible for review both prior to and following the MVAB: The breast MRI before the biopsy to clearly localize the lesion in question, and the follow-up breast MRI to assess clip location. In our institution we routinely perform 6 months follow-up MRI after benign MRI-guided biopsy. The exclusion criteria encompassed cases with no follow-up MRI or patients who had undergone lesion removal surgery before the follow-up MRI. Furthermore, cases lacking a conspicuously visible tissue marker on the follow-up breast MRI were also excluded from the analysis.

MRI biopsy technique

After obtaining informed consent, the patient was positioned prone in a dedicated breast biopsy coil using a grid device. Axial plane unenhanced and contrast-enhanced fat-suppressed T1-weighted images were acquired. The lesions were targeted using a dedicated MRI biopsy software (Hologic, Aegis breast imaging and interventional software. Bedford, MA, USA). The MRI-guided biopsy procedure was conducted using a 9-gauge MRI-compatible vacuum-assisted device (ATEC, Suros surgical systems, Bedform, MA, USA) with a range of 8–14 samples obtained per procedure in most cases. A breast biopsy clip was deployed in the biopsy cavity at the end of the MVAB (TriMark, Hologic, Bedform, MA, USA). In most cases an immediate post biopsy sequence to confirm clip deployment is not performed in our institution. Even when performed, the assessment of clip migration was not reliant on it, as the presence of hematoma within the biopsy cavity often makes it challenging to differentiate from the clip. Furthermore, considering the potential occurrence of late clip migration after the resolution of hematoma, relying on this method may be problematic.

During the study period all MVAB were performed by 1 of 5 subspecialized breast radiologists with 1–15 years of experience.

Image review and data collection

All breast MRI exams and MVAB were retrospectively reviewed by 1 of 2 fellowship trained breast radiologists with 20 and 10 years of experience, respectively. The location of clip deployment was established as the tip of the obturator as seen on the pre-biopsy T1-weighted image. The final position of the clip was determined by identifying the typical susceptibility artifact on the first follow-up breast MRI, as seen on fat suppressed or non-fat suppressed T1 weighted sequences (depending on the MRI protocol performed). Migration was defined as > 10 mm movement of the clip from the expected position. The direction of migration in the x, y or z axis was recorded. In cases where the marker was poorly visualized on the initial follow-up MRI, consultation with the second radiologist was sought, and a consensus was reached. If the consensus opinion was that the clip cannot be visualized confidently, the case was excluded from the analysis.

Three breast size measurements were recorded from the images (Fig. 1):

- Breast thickness in standard MRI (“non-compressed size”).

- Breast thickness in MRI-guided biopsy (“compressed size”).

- Compression index which is determined by dividing the non-compressed size by the compressed size. This index serves as a measure of the level of compression during biopsy, with a higher index indicating more significant compression.

Additional parameters extracted from the images included biopsy side, breast density (global and regional around the lesion), biopsy approach (medial vs lateral), lesion type, size, and location (quadrant and depth).

Demographic and pathological data was also collected from patient electronic and medical records .Malignancy was defined as either invasive malignancy or ductal carcinoma in situ.

Statistical analysis

The correlation between various demographic, imaging, and pathological characteristics and the presence of clip migration was evaluated using appropriate statistical tests. The chi-square test or Fisher's exact test was employed for categorical variables, while the student's t-test or Mann Whitney U test was used for continuous variables. All calculations were 2-tailed, and P < 0.05 was considered statistically significant. In the multivariate logistic regression analysis, all variables with a p-value of less than 0.3 were incorporated. The statistical analysis was done using SPSS version 28 (IBM, Armonk, NY, USA).

Throughout the study period, our institution conducted a total of 562 MVAB. Out of these, 291 MVAB from 268 women satisfied the inclusion criteria and were included in the study. The study workflow is summarized in Fig. 2. The age range spanned from 28 to 81, with a mean age of 51. Twenty patients had prior lumpectomy (7%).

Thirty-one migration events were recorded (11%, 95%CI 7–15). All migration events occurred along the biopsy tract (medio-lateral axis), 30 of them away from the needle (97%, Fig. 3). No migrations were noted along the superior-inferior or anterior-posterior axis.

Out of the MRI-guided biopsies, 38 (13%) resulted in malignant findings, and among them, 28 (74%) underwent surgery for lesion removal. Among these 28 cases, 4 were found to have clip migration. However, the migration observed in all 4 cases was not significant, ranging from 13 to 20 mm, and it did not impact the subsequent management.

Table 1 summarizes the clinical, imaging, and pathological parameters of the patients, as well as their association with migrations. On univariate analysis, more than 50% regional fat was the strongest factor associated with migration, seen in 21/140 (15%), compared to 10/150 (7%) with less than 50% regional fat (P = 0.023). Global fatty breast was more loosely associated with migration, showing borderline significance (P = 0.06). Cases exhibiting migrations displayed a tendency towards larger non-compressed size and higher compression index; however, these associations did not reach statistical significance (Table 1).

In the multivariate logistic regression, all variables with a P-value less than 0.3 were incorporated. However, due to the high correlation between global density and reginal density (P < 0.001), two separate multivariate models were constructed, each including only one of the variables. Upon conducting the multivariate analysis, only regional fat density exhibited statistical significance (P = 0.047).

With the increased utilization of breast MRI for high-risk screening and assessment of disease extent, MVAB are becoming more common. Accurate clip placement during the procedure is essential to facilitate precise pre-surgical localization and complete lesion excision.

In our study, we exclusively utilized follow-up MRI as the means to evaluate the location of the clips, whereas Funaro et al. in their MVAB work (19) relied on mammographic views after the procedure. We hypothesize that measuring clip location on mammographic views may be less precise due to various technical factors, including variations in breast positioning and the amount of compression applied during exams. These factors may have a greater impact on larger breasts that are predominantly composed of fatty tissue, as they are more flexible and mobile (20). Consequently, we believe that assessing clip location on the cross-sectional breast MRI views minimizes the potential for both overestimating and underestimating clip migration. Moreover, by relying on follow up MRI we were able to include cases with late migration, as opposed to studies examining immediate post biopsy mammograms.

Our study found that only 11% of biopsies resulted in clip migration. In their recent study Funaro et al [19] found similar proportion of migration (14%). Our displacement rate is also within the range of previous works focusing on stereotactic breast biopsies [3, 6–8, 20]. This low frequency of migration is reassuring and confirms the safety of the procedure. The fact that no change in patient management related to clip migration was noted in our study is also encouraging.

All the clip movement in our work was along the medio-lateral axis, with the great majority of migrations away from the biopsy needle (97%). Previous works of stereotactic breast biopsies have shown that migration is greatest along the Z axis (i.e., along the direction of the biopsy tract) [21–23]. This aligns with the theory of the "accordion effect," which suggests that after the breast decompresses following the procedure, the clip will migrate in the same direction as the needle insertion, specifically along the medio-lateral axis in the case of MRI-guided biopsy. As far as we know, this finding has not been previously reported in the context of MRI-guided biopsies.

The most important factor associated with clip migration in our work is breast density, and more specifically a higher percentage of fat around the lesion. The association between breast density (regional or global) and clip movement is a consistent finding on multiple studies, including the recent work by Funaro et al[19] on MVAB and a recent meta-analysis on stereotactic biopsies [20]. This comes as no surprise since fat is more easily compressible, intensifying the "accordion effect," and is also less likely to hinder clip movement compared to fibro-glandular tissue. It is also reasonable to expect that the regional breast composition surrounding the clip is a more reliable indicator of migration compared to overall breast density, given that some breasts may have an uneven distribution of fibro-glandular tissue, ranging from completely fatty in one area to extremely dense in another.

Our findings indicated a slightly higher likelihood of migrations in breasts of larger size. It is logical as larger breasts tend to be fattier and provide more space for the clip to displace during decompression. Nonetheless, in is important to note that this association did not reach statistical significance, and previous stereotactic studies have reported the opposite effect [7, 21]. Another potential factor that could impact clip migration is the level of compression applied during the biopsy, which we quantified as the compression index. We anticipated that a higher compression index would correlate with clip movement, due to the amplified "accordion effect. "We did observe a tendency of increased clip migrations as the compression index rose, but this trend did not reach statistical significance. To our knowledge, no prior studies have investigated this factor, and we encourage future research to delve deeper into this aspect.

In our study, we explored additional factors that were not found to be associated with clip migration. These factors included the quadrant and depth of the biopsy, the distance of the lesion from the skin, and the size of the lesion. Previous studies examining these factors have yielded inconsistent findings, with some suggesting a correlation between clip migration and larger lesions (19), superficial location (7), greater posterior depth (7), and biopsies performed in the inner region (6). It is worth noting that most of these studies primarily focused on stereotactic biopsies rather than MRI-guided biopsies, which could account for the divergent results.

Our study has several limitations. Our work was conducted in a single center, using one biopsy system (ATEC) and one biopsy clip (TriMark), which may not be generalizable to all circumstances and populations. Our sample size is limited, partly due to our insistence on including only cases with follow up MRI. As cases that underwent subsequent excision of the lesion were not included, the cohort is more representative of benign lesions (87%). However, the histology of the lesion was not found to be associated with clip migration in our limited sample and previous works (19). The retrospective design of the study, combined with our lack of routine immediate post-biopsy sequence, hindered our ability to evaluate the size of hematoma, which could potentially contribute to clip migration. Nonetheless, most previous reports did not find hematoma size a significant predictor of post biopsy clip movement [3, 6, 7, 19]. Also, the study period of eight years included a diverse range of biopsy experience from the radiologists who participated in MVAB. This variety of expertise could potentially influence the performance of biopsies and, consequently, the rates of clip migration. finally, we do not have records of the exact number of samples obtained in each biopsy, which may influence the size of the biopsy cavity and clip migration [24].

Although clip migration following breast MRI-guided biopsy is an uncommon event, it occurs more often when the target lesion is surrounded by fat, with the clip usually displaced away from the biopsy needle. This information could hold significant value for surgical planning, particularly considering that in most cases, pre-surgical localization is conducted using mammograms, which lack the ability to directly visualize the lesion. In cases where clip migration is suspected, performing a follow-up MRI before surgery can be useful to provide confirmation.

Funding: This study did not receive any external funding. It was internally supported by the Tel Aviv Sourasky Medical Center

Conflicts of interest/competing interests: All authors declare that there is no conflict of interest.

Availability of data and material: The data is available upon request.

Code availability: not applicable.

Authors’ contribution: All authors contributed equally to the manuscript.

Ethics Approval: This study received internal Research Ethical Board approval.

Consent to Participate: As a retrospective study, the participant’s consent was waived, approved by REB.

Consent for Publication: To disseminate the results to the research community, the REB approved publication.

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Table 1

Clinical, imaging and pathological characteristics of the study cohort
Characteristic	All patients (n = 291)^a	Outcomes No clip migration Clip migration (n = 260)^b (n = 31)^c		Univariate analysis	Multivariate Analysis Model 1: regional fat Model 2: global fat
Age, Mean+/-SD (years)	51+/-12	51+/-12	50+/-10	P = 0.765
Prior lumpectomy No Yes	261 (90) 30 (10)	241 (93) 19 (7)	30 (97) 1 (3)	P = 0.706
Final pathology Benign Malignant	253 (87) 38 (13)	227 (87) 33 (13)	26 (84) 4 (16)	P = 0.575
Breast side Left Right	159 (55) 132 (45)	144 (55) 116 (45)	15 (48) 16 (52)	P = 0.568
Breast quadrant Upper outer Upper inner Lower outer Lower inner Behind nipple	99 (34) 43 (15) 89 (31) 35 (12) 25 (8)	90 (35) 38 (15) 78 (30) 32 (12) 22 (8)	9 (29) 5 (16) 11 (35) 3 (10) 3 (10)	P = 0.942
Biopsy depth Anterior third Middle third Posterior third	68 (23) 154 (53) 69 (24)	63 (24) 136 (52) 61 (24)	5 (16) 18 (58) 8 (26)	P = 0.602
Biopsy approach Lateral Medial	231 (79) 60 (21)	207 (80) 53 (20)	24 (77) 7 (23)	P = 0.775
Lesion type Mass Non mass enhancement Focus	67 (23) 183 (63) 41 (14)	62 (24) 161 (62) 37 (14)	5 (16) 22 (71) 4 (13)	P = 0.574
Global Density Less than 50% fat More than 50% fat	186 (64) 105 (36)	171 (66) 89 (34)	15 (48) 16 (52)	P = 0.057	P = 0.057
Regional Density Less than 50% fat More than 50% fat	150 (52) 141 (48)	140 (54) 120 (46)	10 (32) 21 (68)	P = 0.023	P = 0.047
Non-compressed size, Mean+/-SD	74+/-17	73+/-17	79+/-15	P = 0.145	Model 1: P = 0.556 Model 2: P = 0.528
Compressed size, Mean+/-SD	51+/-12	50+/-12	52+/-10	P = 0.575
Thickness index, Median (IQR)	1.47 (0.28)	1.46 (0.28)	1.53 (0.36)	P = 0.213	Model 1: P = 0.403 Model 2: P = o.365
Lesion-skin distance, Median (IQR)	19 (8)	19 (8)	19 (6)	P = 0.672
Lesion size, Median (IQR)	12 (13)	12 (13)	13 (12)	P = 0.439

SD standard deviation IQR interquartile range

^a % within All patients in parenthesis ^b % within No clip migration in parenthesis ^c % within clip migration in parenthesis

Unveiling Tissue Marker Migration in MRI-Guided Vacuum-Assisted Biopsies: Frequency, Factors, and Implications

Status:

Version 1

Abstract

Purpose

Methods and materials

Results

Conclusion

Figures

Introduction

Material and methods

Patients and inclusion criteria

MRI biopsy technique

Image review and data collection

Statistical analysis

Results

Discussion

Conclusion

Declarations

References

Tables

Status:

Version 1