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MRI-guided breast biopsy: a review of technique, indications, and radiological–pathological correlations
Clinical Radiology 73 (2018) 908.e17e908.e25
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MRI-guided breast biopsy: a review of technique, indications, and radiologicalepathological correlations V. Papalouka, F. Kilburn-Toppin*, M. Gaskarth, F. Gilbert Department of Radiology, Cambridge University Hospitals NHS Foundation Trust, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0QQ, UK
article in formation Article history: Received 9 December 2017 Accepted 24 May 2018
Breast magnetic resonance imaging (MRI) is the technique of choice in detection, local staging, and monitoring of breast cancer; however, breast MRI results in the detection of more indeterminate/suspicious lesions that need to be histopathologically proven to guide patient management than any other breast imaging method. If such abnormalities are not detectable in any of the conventional imaging tools (mammography (MMG) or ultrasound) then an MRIguided biopsy needs to be performed to obtain a diagnosis. Breast MRI-guided biopsy is a timeconsuming and complex procedure that requires specific equipment and experienced, welltrained staff. This review article explores and illustrates the indications, the currently available technologies, and the technique of breast MRI-guided biopsy, and explains the importance of careful imaging review and selection of cases. We correlate the radiologicalepathological findings and highlight the impact on patient management in a multidisciplinary setting. Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Breast magnetic resonance imaging (MRI) is indicated for the screening of high-risk patients, preoperative local staging in breast cancer, and monitoring neoadjuvant chemotherapy. The technique can be very helpful in resolving indeterminate lesions where there is a discrepancy between imaging methods or clinical assessment or core biopsy. It is widely agreed that MRI demonstrates superior sensitivity to other imaging methods in detecting breast cancer; however, the specificity is more debatable.1e3
* Guarantor and correspondent: F. Kilburn-Toppin, Department of Radiology, Cambridge University Hospitals NHS Foundation Trust, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0QQ, UK. Tel.: þ44 01223 245151. E-mail address: fl[email protected] (F. KilburnToppin).
Due to the lower specificity of the technique, if lesions are identified on MRI that are suspicious for malignancy, then a targeted ultrasound (US) examination is advised to confirm that the lesion is indeed malignant. This is sometimes referred to as a “second-look US” as a previous US examination may already have been undertaken. An USguided biopsy of this lesion is then taken to establish the diagnosis. If no corresponding abnormality is identified, then this precludes US-guided biopsy and an MRI-guided biopsy must be performed. Breast MRI-guided biopsy is a time-consuming procedure that requires specific equipment and experienced and well-trained staff, and is often only performed in a few dedicated centres. In this article, we review which patients to refer for MRI biopsy, highlighting the importance of careful review of the previous imaging, selection of cases, and awareness of change in patient management resulting from MRI-guided biopsy results. We review the optimal MRI protocols and
https://doi.org/10.1016/j.crad.2018.05.029 0009-9260/Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
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interventional techniques for MRI-guided breast biopsy with examples from our own experience.
Indications and contraindications for breast MRI-guided biopsy Unlike mammography and US, breast MRI requires intravenous contrast medium administration to characterise and classify breast abnormalities using the Breast Imaging-Reporting And Data System (BIRADS).4 Indeterminate or suspicious (BIRADS 4/5) lesions can present on a contrast-enhanced breast MRI as an enhancing mass, nonmass enhancement, or a focus of enhancement (<5 mm). Probably benign (BIRADS 3) lesions in high-risk patient populations should also be considered suspicious and should be managed with equal attention as BIRADS 4/5 lesions.5e7 If any of these lesions are identified on breast MRI, then a biopsy is required to establish a diagnosis and to confirm malignancy in order to guide patient management. The importance of requiring tissue diagnosis of additional indeterminate or suspicious MRI-detected lesions in patients with an already biopsy-proven malignancy is to guide surgical planning if a patient is being considered for breastconserving surgery8 The first step to investigate any MRI abnormalities should be a second-look targeted US. The efficacy of the second-look US is reported between 23e71%, with a malignancy detection rate of 15e56%.9 Larger enhancing masses and BIRADS 5 (highly suspicious for malignancy) lesions are more readily identified on a second-look targeted US, with a detection rate estimated between 25e62%; however, certain types of MRI lesions, such non-mass enhancement or small foci <10 mm are less likely to have a US correlate, with a detection rate between 11e42% reported for non-mass enhancement.9e15 Careful review of the MRI prior to a second-look US is of great importance. The breast radiologist should be able to locate the position of the lesion and correlate with the sonographic findings. It is also useful to keep in mind the differences in the positioning of the patient while having a breast MRI lying in a prone position, and try to reproduce this in some extent when the patient is on the US table. Reviewing recent mammographic images is another step a breast radiologist should remember before requesting an MRI-guided biopsy. Thorough scrutiny of the patient’s mammograms focusing at the location of the MRI lesion may reveal findings overlooked on the initial mammographic interpretation, particularly for non-mass enhancement, which may correspond to an area of microcalcification in cases of ductal carcinoma in situ (DCIS). This would allow confirmation using a stereotactic intervention. If conventional imaging fails to demonstrate the lesion with certainty, then an MRI-guided biopsy should be performed.2,16 The effectiveness of MRI-guided biopsy varies between different centres, mostly due to differences in patient selection and population as well as variation in collecting data,17 with studies reporting cancer detection rates of 20e50%.18,19
The MRI-guided breast biopsy procedure requires training, and regular and sufficient experience of the performing team (radiologists and MRI radiographers), in both the vacuum-assisted biopsy (VAB) procedure, as well as breast MRI interpretation. Therefore, National Health Service Breast Screening Programme (NHSBSP) guidelines recommended it should be undertaken by experienced breast centres performing at least 12 MRI-guided breast biopsies per year, and within centres that have recognised experience in VAB carrying out at least 50 image-guided VAB procedures each year.20 When the decision is made to proceed to an MRI-guided breast biopsy then several risk factors and safety precautions should be assessed. Absolute contraindications to an MRI-guided biopsy include; MRI-related limitations such as claustrophobia or metallic/magnetic devices, i.e. pacemakers and contrast medium-related contraindications (renal impairment or history of allergy to gadolinium). Biopsy-related contraindications, such as deranged clotting function and anticoagulation, are generally relative and can be managed by following local protocols with careful consideration on a case-byecase approach. Another contraindication is when the target lesion is not visible/ reproducible at the time of the procedure following intravenous administration of the contrast agent, which is reported in up to 14% of patients.21 In this situation, investigation of potential causes is important before the procedure is abandoned. Known causes are excessive breast compression, phase of the menstrual cycle affecting background parenchymal enhancement (BPE), hormonereplacement therapies, which may increase BPE sufficiently to obscure a lesion, or inadequate contrast medium administration.22e26 If none of these apply, then it is clear that an MRI-guided biopsy cannot be performed, and a short-term follow-up diagnostic MRI should be obtained within 3e6 months to confirm that the lesion has indeed disappeared.1,23,27,28 The patient’s body habitus needs to be assessed to determine the appropriateness of the procedure as well as the patient’s ability to tolerate prone positioning required for up to 1 hour. For this reason, the comfort of the patient whilst undergoing the procedure is key.29 Further limitations for performing an MRI-guided biopsy is the accessibility of the target lesion. When the lesion is located close to the chest wall or the nipple or if the patient has breast implants, then feasibility of needle access as well as patient’s safety, potential damage to the skin, and implant integrity should be determined.1 When MRIguided biopsy is not technically feasible, MRI guidance can still be used for pre-surgical lesion localisation, either by placing a guide wire through the abnormality or deploying a marker clip.1,30
Breast MRI-guided biopsy technique Planning When the indications, contraindications, and safety measures of the MRI-guided biopsy procedure have been
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Figure 1 (a) A lesion (non-mass enhancement) identified on post-contrast images. (b) Marker position confirmed in lesion. (c) Post-biopsy haematoma with clip in situ (arrow).
Figure 2 Biopsy pack equipment with marker for alignment (above) and introducer needle below and nine-hole grid marker with measurement sheath and grid system localisation method.
considered for the individual, then the plan should be discussed with the patient. The technique, intended benefits, limitations, and risks of the procedure, including the possibility of not being able to identify the lesion, as well as alternatives should be discussed with the patient and written informed consent should be obtained and documented.16
MRI protocol Breast MRI-guided interventions are performed using a phased array dedicated breast coil, which has open access to the lateral or medial aspect of the breasts. At our centre, an eight-channel phased array open breast coil on a 1.5 T MRI system is used. The MRI protocol for breast procedures varies among different centres; however, it is universally accepted that this is not a diagnostic protocol but an accurate and fast screen to reproduce, identify, and target the breast abnormality. It is also the consensus that an optimal MRI protocol requires high spatial resolution with section thicknesses ranging between 1e3.5 mm and accelerated acquisition following bolus intravenous contrast medium administration in order to detect the suspicious lesion before contrast medium washout.16 At our institution, image acquisition is obtained through axial sections with a 2 mm section thickness and 36 mm
Figure 3 Enhancing lesion 4 mm deep within the medial aspect of the right breast on contrast-enhanced T1-weighted imaging in a high-risk screening patient. This lesion posed difficult targeting as the location was too posterior to use the grid system. A freehand approach, preformed with clip placed adjacent to lesion for subsequent surgical excision was undertaken.
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field of view (FOV). T1-weighted three-dimensional (3D) fat-saturated (FS) gradient-echo images are initially acquired followed by administration of contrast medium (0.1 mmol/kg gadolinium-based agent at a rate of 2 ml/s administered via a pump injector) and dynamic highresolution T1-weighted 3D FS gradient-echo images. Five series post-intravenous contrast medium injection are performed with an acquisition time of 84 seconds for each, all with 2 mm section thickness. The ideal time of the dynamic scan is <4 minutes as per American College of Radiologists (ACR) recommendations.16 In addition, postprocessing subtracted images from the dynamic sequences are reviewed.31 Interim scans to check positioning are obtained with rapid T1-weighted turbo spin-echo (TSE) images, usually 5e7 slices focusing around the lesion.29 In our institution a split-bolus injection technique is commonly used, injecting
half-dose contrast medium initially and a second half-dose subsequently if required. We have found this technique to be beneficial in cases whereby confirmation may be required that the introducer/needle is in the correct location prior to biopsy, which is particularly useful for small lesions which demonstrate early rapid contrast medium washout, or to confirm post-biopsy that the enhancing lesion has been successfully removed and is no longer visible if there is any doubt regarding successful targeting, perhaps due to patient movement. The only potential downside to the technique is if the lesion does not enhance sufficiently to be able to allow targeting with only half a dose of contrast medium, but in our experience with the prior knowledge of where the lesions is with the original imaging this is rarely an issue. One final unenhanced scan is obtained post-biopsy and marker clip placement is deployed to confirm the correct site of biopsy. T2-weighted
Figure 4 A 48-year-old patient presenting with a symptomatic left breast mass. Two focal suspicious lesions seen, one on mammography (a) and one on US (b). Left retroareolar biopsy and left lower-outer quadrant biopsy were performed and both indicated invasive carcinoma no special type (NST). Breast conservation was considered, therefore, the patient underwent MRI to plan surgery. (c) An additional third 10 mm focal enhancing mass lesion was seen in the inferior left breast (arrow). A second-look US of the inferior left breast was normal, so the patient proceeded to MRI-guided biopsy. (d) The MRI biopsy introducer placed one slice cranially to the enhancing mass due to the inferior location and proximity to skin. (e) Biopsies taken with the notch facing caudally. (f) The post-clip scan shows satisfactory targeting with a haematoma present at the biopsy site. At histopathology an invasive carcinoma with lobular features, grade 2 was diagnosed. The patient subsequently proceeded to mastectomy after chemotherapy. Histopathology confirmed three residual foci of invasive carcinoma NST with a partial response to chemotherapy.
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Localisation procedure and VAB
Figure 4 (continued)
images may also be considered to assess the post-biopsy images (Fig 1).
Breast MRI biopsy equipment Dedicated devices and specific needles are required to equip a breast MRI biopsy suite. Provided an MRI system (1.5 or 3 T) and a dedicated open breast coil are available, a specialised breast centre will need to have an MRIcompatible localisation device, including an adjustable Grid system, a smaller cube grid, fiducial marker (opaque landmark fixed to the grid with its tip in contact with the breast), introducer, VAB apparatus and needle, and a localisation marker clip. The introducer biopsy pack is a coaxial system, which enables optimal accuracy on lesion targeting and includes; a plastic sheath with numeric grading, a metallic stylet, and a blunt tip plastic introducer, which is MRI visible (the obturator; Fig 2). Note that the open breast coils used for the biopsy should ideally be the same or have the same number of channels as those used for diagnosis for optimal performance and accuracy.
Diagnostic breast MRI is again reviewed before commencing the biopsy and the best positioning and approach is planned. Communicating and discussing imaging and planning with the MRI radiographer is crucial to achieve accurate targeting. The patient is placed in the prone position and the affected breast is stabilised with moderate compression between a plastic plate and the grid (site of biopsy approach). Positioning and immobilisation of the breast is prerequisite for accurate sampling as it allows good elimination of artefacts or blurring from respiratory motion and improves fixation of breast tissue during needle insertion (especially useful for dense breast tissue).9 For better positioning, cushions can be added for small breasts. Attention should be taken, however, to avoid strong compression, which may impair lesion enhancement. It is also important to avoid compromising the chest wall and ensure sufficient breast thickness for VAB probe placement. A warm and comfortable environment for the patient is key. A lateral approach is the standard approach, and preferable for deep lesions in order not to be impeded by the sternum. Sometimes a medial approach is necessary, but this offers limited access to deep lesions and is more inconvenient for the patient and the radiologist requiring more difficult access under the contralateral breast, which is compressed. For lesions that are too difficult to access or not amenable for VAB given positioning close to the skin or chest wall, a marker clip can be placed under MRI guidance for subsequent diagnostic surgical excision (Fig 3). The fiducial marker is initially placed in an approximate position before commencing the scan, followed by the pre- and post-intravenous contrast medium injection axial T1weighted FS images. On the pre-contrast images, we can confirm an approximate adequate position using anatomical landmarks, such as the fateglandular tissue interface or other identifiable lesions on unenhanced imaging. It is also important to verify that the target is within an accessible area within the coil. If not, then the patient will need to be repositioned using pads or slight rotation towards the affected site. When the target lesion is identified, using the dynamic and the post-processed subtracted images, the fiducial position is assessed and repositioned if needed measuring the anteroposterior and craniocaudal distance from the target. Three-dimensional planning should be used to aid accurate localisation and a subsequent scan is then performed to evaluate location. Localisation of the lesion can be performed “manually”, by looking at the coordinates on the imaging and adjusting the positioning of the fiducial and needle accordingly. Alternatively, many post-processing software packages now exist that can help to find the coordinate for needle insertion by clicking the centre of the lesion and the zero marker of the breast biopsy device. The software will then demonstrate the correct location on the grid to move the needle to allow fast and accurate targeting. Aseptic technique is then used followed by injection of local anaesthetic to the skin and within the breast tissue.
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Use of a longer needle (spinal needle or the introducer) to inject local anaesthesia deep into the breast is often beneficial to minimise patient discomfort. The co-axial introducer is placed through the mini grid within the target lesion and the metallic stylet is replaced with the plastic obturator in order to re-image patient prior to sampling. Once correct position is confirmed the biopsy needle can be placed in position and appropriate samples taken with vacuum assistance. VAB is the widely acceptable method of choice and preferable to core biopsy for MRI-guided breast procedures. VAB provides adequate sampling of smaller lesions and higher tissue volume (increasing diagnostic accuracy), as well as allowing continuous suction which compensates for tissue shift (from bleeding or instillation of local anaesthetic).1,9,28 There are various VAB needle sizes provided by different manufacturers ranging between 8e12 G. The average number of cores recommended is 24 if taken with an 11 G needle (or equivalent if larger probe is used).1 At our institution we use a 9 G needle with an average number of 12 cores obtained.
Post-VAB A localisation marker clip is deployed in the biopsy bed to label the area and a post-clip MRI with a 3D spoiled gradient (SPGR) is obtained immediately post-insertion, which can help identify that the correct site has been sampled, the clip has deployed, and any complications, namely haematoma. The clip should be visible on all three techniques; MRI, mammography, and US.32 Post-
procedure, an ice pack and compression are applied to achieve haemostasis and minimise the bruising, with prolonged manual compression needed in a small proportion of cases.33
Complications MRI-guided VAB biopsy has very low morbidity rates, estimated between 0e6%,29 with similar rates to stereotactic VABs. Risk of skin tearing is possible particularly with lesions lying close to the skin surface. Minor complications, such as haematoma and pain, may occur during or immediately after the procedure. Adverse effects requiring abandoning the procedure are rare and reported at around 10%, although in our institution we have found this to be much lower34 (Fig 4).
Radiologicalepathological correlation Management decisions regarding MRI-guided biopsy results should be made in a multidisciplinary team (MDT) meeting, taking into consideration histopathological and imaging correlation and individual patient risk factors.1 MRI-guided breast biopsy has particular challenges when considering radiological and pathological correlation. Not only is the initial targeting of the lesion more difficult than with US or stereotactic biopsy, with the target lesion often not remaining visible and/or enhancing during the procedure, but post-procedure haematoma and fiducial artefact often make it difficult to determine if the correct area has been sampled.
Figure 5 A 63-year-old patient with mammographically screen-detected left multifocal disease. (a) US biopsy confirmed invasive carcinoma NST. MRI performed for neoadjuvant chemotherapy. (b) A linear area of enhancement was seen in the contralateral right breast. Second-look US demonstrated a diffuse hypoechoic area in the central right breast, with subsequent US-guided fan biopsy. Histopathology indicated atypical lobular hyperplasia (ALH), B3. The MDT opinion was non-concordant results. (c) The patient proceeded to MRI biopsy with the resulting histopathology indicating invasive carcinoma B5b. The patient proceeded to bilateral mastectomy.
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In the case of malignant lesions, the histopathological results prove the success of the biopsy, but given that malignancy rates for MRI-guided biopsy are only in the region of 20e30%, this means that it is of utmost importance to be able to recognise concordant from discordant benign biopsy results. The positive predictive value (PPV) for malignancy depends on a number of factors. Breast MRI is already restricted to particular populations with higher risk of disease, but within this cohort there are variations in the PPV for particular referral populations, with higher rates seen in women undergoing breast MRI for preoperative staging that for screening.21,35 Higher PPV are also seen with increasing BI-RADS category (BI-RADS 3 13.3%, BI-RADS 4
Figure 6 A 54-year-old patient with right-sided lobular cancer. (aeb) MRI demonstrated an additional focal area of non-mass enhancement in the medial aspect of the contralateral left breast as seen on postcontrast T1-weighted and FS images. (c) No correlation was found on the unenhanced T2-weighted imaging. MRI-guided biopsy was performed and histopathology confirmed hamartoma, B2. Either short-interval follow-up or repeat MRI-guided biopsy was considered the appropriate management.
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41.8%, BI-RADS 5 62.8%),9 and for mass lesions compared to non-mass lesions (57% versus 35%).33 Although greater lesion size is of importance in predicting malignancy rates in MRI-detected lesions, the PPV for lesions 5 mm has been shown to be as high as 20%,36 highlighting the importance of not dismissing small <5 mm lesions in women with a known cancer, particularly if it is close to the original malignancy.
Figure 7 A 48-year-old patient with biopsy-proven DCIS in the inferior central right breast on conventional imaging (mammography and stereotactic biopsy). MRI was performed to assess the extent and plan surgery. (a) Non-mass enhancement seen in the inferior right breast corresponding to DCIS. (b) An additional small focus of nonmass enhancement was seen in the deep posterior right breast. Mammography reviewed and second-look US performed with no abnormality detected. (c) The patient proceeded to MRI-guided biopsy with the marker seen in the correct position within the breast. Histopathology demonstrated pseudoangiomatous stromal hyperplasia (PASH), B2 and the radiology and histopathology findings were felt to be concordant at the MDT.
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Lack of ability to correlate the specimen sample with the original lesion proves a further challenge for the radiologist in MRI-guided biopsies. This is also a challenge for the histopathologist, as many lesions that are sampled are nonmass enhancement, which makes it difficult to confirm that the correct lesion has been sampled (Figs 5 and 6). It is also often the case that mass lesions on MRI do not correspond to mass lesions histologically, and conversely, for Non mass enhancement (NME) which can yield diagnoses such as invasive carcinomas and fibroadenomas.37 Some authors recommend in this case taking into account additional pathological criteria, including a clear interface with the surrounding tissue for mass lesions and having a high level of awareness for PASH and fibrosis, which often corresponds radiologically and pathologically to regional NME37 (Fig 7). The other challenge with radiologicalepathological correlation in MRI-guided biopsy is the relatively high underestimation rates compared to stereotactic and US-guided biopsy. High-risk lesions detected only at MRI are increasing as more MRI-guided biopsies are being undertaken, with the incidence ranging from 3e21%. Upgrade rates at surgery of MRI-biopsied atypical ductal hyperplasia (ADH) are 19e38% compared with 20% after stereotactic biopsy, and similarly 5e25% of MRI-biopsied DCIS are upgraded to invasive carcinoma at surgery, compared with 11% after stereotactic biopsy.35,38e40 This may be because of the higher risk of breast cancer in the MRI-detected group, with features on MRI overlapping those of malignant lesions with no specific imaging features that can predict upgrade to malignancy. For this reason, some authors recommend excision of all high-risk lesions, particularly if there has been a history of breast cancer.40
Given the difficulty in distinguishing concordant from discordant results, and with false-negative rates after benign MRI biopsy with concordant histology reported at around 2.5%, most centres recommended follow-up for benign lesions detected on MRI-guided biopsy.41 Most centres, including our own, recommend a 6-month followup. Some authors advocate performing a repeat contrastenhanced MRI 24 hours after the initial MRI biopsy to increase diagnostic accuracy and eliminate missed cancers, particularly if the lesions are in the ipsilateral breast of a women with known or previous breast cancer.42 There are, however, no data on the total length of time follow-up should be performed for, and in our institution, after a 6month follow-up no further imaging is performed. It is imperative that MDT decisions on appropriate follow-up are clearly documented and conveyed to the referring hospital to ensure that follow-up is performed (Fig 8).
Conclusion As the demand for breast MRI continues to rise with indications including high-risk screening, neoadjuvant chemotherapy, and preoperative planning, so too does the requirement for MRI-guided biopsy of lesions that cannot be identified on second-look US. Whether performing the biopsy or referring a patient for the procedure to be undertaken, it is important that breast radiologists understand the challenges that may be faced in accurately targeting and sampling MRI-detected breast lesions, and the necessity of appropriate follow-up to ensure accurate radiologicalepathological correlation.
Figure 8 MRI-guided biopsy management flow chart.
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Clinical Radiology journal homepage: www.clinicalradiologyonline.net
MRI-guided breast biopsy: a review of technique, indications, and radiologicalepathological correlations V. Papalouka, F. Kilburn-Toppin*, M. Gaskarth, F. Gilbert Department of Radiology, Cambridge University Hospitals NHS Foundation Trust, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0QQ, UK
article in formation Article history: Received 9 December 2017 Accepted 24 May 2018
Breast magnetic resonance imaging (MRI) is the technique of choice in detection, local staging, and monitoring of breast cancer; however, breast MRI results in the detection of more indeterminate/suspicious lesions that need to be histopathologically proven to guide patient management than any other breast imaging method. If such abnormalities are not detectable in any of the conventional imaging tools (mammography (MMG) or ultrasound) then an MRIguided biopsy needs to be performed to obtain a diagnosis. Breast MRI-guided biopsy is a timeconsuming and complex procedure that requires specific equipment and experienced, welltrained staff. This review article explores and illustrates the indications, the currently available technologies, and the technique of breast MRI-guided biopsy, and explains the importance of careful imaging review and selection of cases. We correlate the radiologicalepathological findings and highlight the impact on patient management in a multidisciplinary setting. Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Breast magnetic resonance imaging (MRI) is indicated for the screening of high-risk patients, preoperative local staging in breast cancer, and monitoring neoadjuvant chemotherapy. The technique can be very helpful in resolving indeterminate lesions where there is a discrepancy between imaging methods or clinical assessment or core biopsy. It is widely agreed that MRI demonstrates superior sensitivity to other imaging methods in detecting breast cancer; however, the specificity is more debatable.1e3
* Guarantor and correspondent: F. Kilburn-Toppin, Department of Radiology, Cambridge University Hospitals NHS Foundation Trust, Cambridge Biomedical Campus, Hills Road, Cambridge CB2 0QQ, UK. Tel.: þ44 01223 245151. E-mail address: fl[email protected] (F. KilburnToppin).
Due to the lower specificity of the technique, if lesions are identified on MRI that are suspicious for malignancy, then a targeted ultrasound (US) examination is advised to confirm that the lesion is indeed malignant. This is sometimes referred to as a “second-look US” as a previous US examination may already have been undertaken. An USguided biopsy of this lesion is then taken to establish the diagnosis. If no corresponding abnormality is identified, then this precludes US-guided biopsy and an MRI-guided biopsy must be performed. Breast MRI-guided biopsy is a time-consuming procedure that requires specific equipment and experienced and well-trained staff, and is often only performed in a few dedicated centres. In this article, we review which patients to refer for MRI biopsy, highlighting the importance of careful review of the previous imaging, selection of cases, and awareness of change in patient management resulting from MRI-guided biopsy results. We review the optimal MRI protocols and
https://doi.org/10.1016/j.crad.2018.05.029 0009-9260/Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
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interventional techniques for MRI-guided breast biopsy with examples from our own experience.
Indications and contraindications for breast MRI-guided biopsy Unlike mammography and US, breast MRI requires intravenous contrast medium administration to characterise and classify breast abnormalities using the Breast Imaging-Reporting And Data System (BIRADS).4 Indeterminate or suspicious (BIRADS 4/5) lesions can present on a contrast-enhanced breast MRI as an enhancing mass, nonmass enhancement, or a focus of enhancement (<5 mm). Probably benign (BIRADS 3) lesions in high-risk patient populations should also be considered suspicious and should be managed with equal attention as BIRADS 4/5 lesions.5e7 If any of these lesions are identified on breast MRI, then a biopsy is required to establish a diagnosis and to confirm malignancy in order to guide patient management. The importance of requiring tissue diagnosis of additional indeterminate or suspicious MRI-detected lesions in patients with an already biopsy-proven malignancy is to guide surgical planning if a patient is being considered for breastconserving surgery8 The first step to investigate any MRI abnormalities should be a second-look targeted US. The efficacy of the second-look US is reported between 23e71%, with a malignancy detection rate of 15e56%.9 Larger enhancing masses and BIRADS 5 (highly suspicious for malignancy) lesions are more readily identified on a second-look targeted US, with a detection rate estimated between 25e62%; however, certain types of MRI lesions, such non-mass enhancement or small foci <10 mm are less likely to have a US correlate, with a detection rate between 11e42% reported for non-mass enhancement.9e15 Careful review of the MRI prior to a second-look US is of great importance. The breast radiologist should be able to locate the position of the lesion and correlate with the sonographic findings. It is also useful to keep in mind the differences in the positioning of the patient while having a breast MRI lying in a prone position, and try to reproduce this in some extent when the patient is on the US table. Reviewing recent mammographic images is another step a breast radiologist should remember before requesting an MRI-guided biopsy. Thorough scrutiny of the patient’s mammograms focusing at the location of the MRI lesion may reveal findings overlooked on the initial mammographic interpretation, particularly for non-mass enhancement, which may correspond to an area of microcalcification in cases of ductal carcinoma in situ (DCIS). This would allow confirmation using a stereotactic intervention. If conventional imaging fails to demonstrate the lesion with certainty, then an MRI-guided biopsy should be performed.2,16 The effectiveness of MRI-guided biopsy varies between different centres, mostly due to differences in patient selection and population as well as variation in collecting data,17 with studies reporting cancer detection rates of 20e50%.18,19
The MRI-guided breast biopsy procedure requires training, and regular and sufficient experience of the performing team (radiologists and MRI radiographers), in both the vacuum-assisted biopsy (VAB) procedure, as well as breast MRI interpretation. Therefore, National Health Service Breast Screening Programme (NHSBSP) guidelines recommended it should be undertaken by experienced breast centres performing at least 12 MRI-guided breast biopsies per year, and within centres that have recognised experience in VAB carrying out at least 50 image-guided VAB procedures each year.20 When the decision is made to proceed to an MRI-guided breast biopsy then several risk factors and safety precautions should be assessed. Absolute contraindications to an MRI-guided biopsy include; MRI-related limitations such as claustrophobia or metallic/magnetic devices, i.e. pacemakers and contrast medium-related contraindications (renal impairment or history of allergy to gadolinium). Biopsy-related contraindications, such as deranged clotting function and anticoagulation, are generally relative and can be managed by following local protocols with careful consideration on a case-byecase approach. Another contraindication is when the target lesion is not visible/ reproducible at the time of the procedure following intravenous administration of the contrast agent, which is reported in up to 14% of patients.21 In this situation, investigation of potential causes is important before the procedure is abandoned. Known causes are excessive breast compression, phase of the menstrual cycle affecting background parenchymal enhancement (BPE), hormonereplacement therapies, which may increase BPE sufficiently to obscure a lesion, or inadequate contrast medium administration.22e26 If none of these apply, then it is clear that an MRI-guided biopsy cannot be performed, and a short-term follow-up diagnostic MRI should be obtained within 3e6 months to confirm that the lesion has indeed disappeared.1,23,27,28 The patient’s body habitus needs to be assessed to determine the appropriateness of the procedure as well as the patient’s ability to tolerate prone positioning required for up to 1 hour. For this reason, the comfort of the patient whilst undergoing the procedure is key.29 Further limitations for performing an MRI-guided biopsy is the accessibility of the target lesion. When the lesion is located close to the chest wall or the nipple or if the patient has breast implants, then feasibility of needle access as well as patient’s safety, potential damage to the skin, and implant integrity should be determined.1 When MRIguided biopsy is not technically feasible, MRI guidance can still be used for pre-surgical lesion localisation, either by placing a guide wire through the abnormality or deploying a marker clip.1,30
Breast MRI-guided biopsy technique Planning When the indications, contraindications, and safety measures of the MRI-guided biopsy procedure have been
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Figure 1 (a) A lesion (non-mass enhancement) identified on post-contrast images. (b) Marker position confirmed in lesion. (c) Post-biopsy haematoma with clip in situ (arrow).
Figure 2 Biopsy pack equipment with marker for alignment (above) and introducer needle below and nine-hole grid marker with measurement sheath and grid system localisation method.
considered for the individual, then the plan should be discussed with the patient. The technique, intended benefits, limitations, and risks of the procedure, including the possibility of not being able to identify the lesion, as well as alternatives should be discussed with the patient and written informed consent should be obtained and documented.16
MRI protocol Breast MRI-guided interventions are performed using a phased array dedicated breast coil, which has open access to the lateral or medial aspect of the breasts. At our centre, an eight-channel phased array open breast coil on a 1.5 T MRI system is used. The MRI protocol for breast procedures varies among different centres; however, it is universally accepted that this is not a diagnostic protocol but an accurate and fast screen to reproduce, identify, and target the breast abnormality. It is also the consensus that an optimal MRI protocol requires high spatial resolution with section thicknesses ranging between 1e3.5 mm and accelerated acquisition following bolus intravenous contrast medium administration in order to detect the suspicious lesion before contrast medium washout.16 At our institution, image acquisition is obtained through axial sections with a 2 mm section thickness and 36 mm
Figure 3 Enhancing lesion 4 mm deep within the medial aspect of the right breast on contrast-enhanced T1-weighted imaging in a high-risk screening patient. This lesion posed difficult targeting as the location was too posterior to use the grid system. A freehand approach, preformed with clip placed adjacent to lesion for subsequent surgical excision was undertaken.
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field of view (FOV). T1-weighted three-dimensional (3D) fat-saturated (FS) gradient-echo images are initially acquired followed by administration of contrast medium (0.1 mmol/kg gadolinium-based agent at a rate of 2 ml/s administered via a pump injector) and dynamic highresolution T1-weighted 3D FS gradient-echo images. Five series post-intravenous contrast medium injection are performed with an acquisition time of 84 seconds for each, all with 2 mm section thickness. The ideal time of the dynamic scan is <4 minutes as per American College of Radiologists (ACR) recommendations.16 In addition, postprocessing subtracted images from the dynamic sequences are reviewed.31 Interim scans to check positioning are obtained with rapid T1-weighted turbo spin-echo (TSE) images, usually 5e7 slices focusing around the lesion.29 In our institution a split-bolus injection technique is commonly used, injecting
half-dose contrast medium initially and a second half-dose subsequently if required. We have found this technique to be beneficial in cases whereby confirmation may be required that the introducer/needle is in the correct location prior to biopsy, which is particularly useful for small lesions which demonstrate early rapid contrast medium washout, or to confirm post-biopsy that the enhancing lesion has been successfully removed and is no longer visible if there is any doubt regarding successful targeting, perhaps due to patient movement. The only potential downside to the technique is if the lesion does not enhance sufficiently to be able to allow targeting with only half a dose of contrast medium, but in our experience with the prior knowledge of where the lesions is with the original imaging this is rarely an issue. One final unenhanced scan is obtained post-biopsy and marker clip placement is deployed to confirm the correct site of biopsy. T2-weighted
Figure 4 A 48-year-old patient presenting with a symptomatic left breast mass. Two focal suspicious lesions seen, one on mammography (a) and one on US (b). Left retroareolar biopsy and left lower-outer quadrant biopsy were performed and both indicated invasive carcinoma no special type (NST). Breast conservation was considered, therefore, the patient underwent MRI to plan surgery. (c) An additional third 10 mm focal enhancing mass lesion was seen in the inferior left breast (arrow). A second-look US of the inferior left breast was normal, so the patient proceeded to MRI-guided biopsy. (d) The MRI biopsy introducer placed one slice cranially to the enhancing mass due to the inferior location and proximity to skin. (e) Biopsies taken with the notch facing caudally. (f) The post-clip scan shows satisfactory targeting with a haematoma present at the biopsy site. At histopathology an invasive carcinoma with lobular features, grade 2 was diagnosed. The patient subsequently proceeded to mastectomy after chemotherapy. Histopathology confirmed three residual foci of invasive carcinoma NST with a partial response to chemotherapy.
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Localisation procedure and VAB
Figure 4 (continued)
images may also be considered to assess the post-biopsy images (Fig 1).
Breast MRI biopsy equipment Dedicated devices and specific needles are required to equip a breast MRI biopsy suite. Provided an MRI system (1.5 or 3 T) and a dedicated open breast coil are available, a specialised breast centre will need to have an MRIcompatible localisation device, including an adjustable Grid system, a smaller cube grid, fiducial marker (opaque landmark fixed to the grid with its tip in contact with the breast), introducer, VAB apparatus and needle, and a localisation marker clip. The introducer biopsy pack is a coaxial system, which enables optimal accuracy on lesion targeting and includes; a plastic sheath with numeric grading, a metallic stylet, and a blunt tip plastic introducer, which is MRI visible (the obturator; Fig 2). Note that the open breast coils used for the biopsy should ideally be the same or have the same number of channels as those used for diagnosis for optimal performance and accuracy.
Diagnostic breast MRI is again reviewed before commencing the biopsy and the best positioning and approach is planned. Communicating and discussing imaging and planning with the MRI radiographer is crucial to achieve accurate targeting. The patient is placed in the prone position and the affected breast is stabilised with moderate compression between a plastic plate and the grid (site of biopsy approach). Positioning and immobilisation of the breast is prerequisite for accurate sampling as it allows good elimination of artefacts or blurring from respiratory motion and improves fixation of breast tissue during needle insertion (especially useful for dense breast tissue).9 For better positioning, cushions can be added for small breasts. Attention should be taken, however, to avoid strong compression, which may impair lesion enhancement. It is also important to avoid compromising the chest wall and ensure sufficient breast thickness for VAB probe placement. A warm and comfortable environment for the patient is key. A lateral approach is the standard approach, and preferable for deep lesions in order not to be impeded by the sternum. Sometimes a medial approach is necessary, but this offers limited access to deep lesions and is more inconvenient for the patient and the radiologist requiring more difficult access under the contralateral breast, which is compressed. For lesions that are too difficult to access or not amenable for VAB given positioning close to the skin or chest wall, a marker clip can be placed under MRI guidance for subsequent diagnostic surgical excision (Fig 3). The fiducial marker is initially placed in an approximate position before commencing the scan, followed by the pre- and post-intravenous contrast medium injection axial T1weighted FS images. On the pre-contrast images, we can confirm an approximate adequate position using anatomical landmarks, such as the fateglandular tissue interface or other identifiable lesions on unenhanced imaging. It is also important to verify that the target is within an accessible area within the coil. If not, then the patient will need to be repositioned using pads or slight rotation towards the affected site. When the target lesion is identified, using the dynamic and the post-processed subtracted images, the fiducial position is assessed and repositioned if needed measuring the anteroposterior and craniocaudal distance from the target. Three-dimensional planning should be used to aid accurate localisation and a subsequent scan is then performed to evaluate location. Localisation of the lesion can be performed “manually”, by looking at the coordinates on the imaging and adjusting the positioning of the fiducial and needle accordingly. Alternatively, many post-processing software packages now exist that can help to find the coordinate for needle insertion by clicking the centre of the lesion and the zero marker of the breast biopsy device. The software will then demonstrate the correct location on the grid to move the needle to allow fast and accurate targeting. Aseptic technique is then used followed by injection of local anaesthetic to the skin and within the breast tissue.
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Use of a longer needle (spinal needle or the introducer) to inject local anaesthesia deep into the breast is often beneficial to minimise patient discomfort. The co-axial introducer is placed through the mini grid within the target lesion and the metallic stylet is replaced with the plastic obturator in order to re-image patient prior to sampling. Once correct position is confirmed the biopsy needle can be placed in position and appropriate samples taken with vacuum assistance. VAB is the widely acceptable method of choice and preferable to core biopsy for MRI-guided breast procedures. VAB provides adequate sampling of smaller lesions and higher tissue volume (increasing diagnostic accuracy), as well as allowing continuous suction which compensates for tissue shift (from bleeding or instillation of local anaesthetic).1,9,28 There are various VAB needle sizes provided by different manufacturers ranging between 8e12 G. The average number of cores recommended is 24 if taken with an 11 G needle (or equivalent if larger probe is used).1 At our institution we use a 9 G needle with an average number of 12 cores obtained.
Post-VAB A localisation marker clip is deployed in the biopsy bed to label the area and a post-clip MRI with a 3D spoiled gradient (SPGR) is obtained immediately post-insertion, which can help identify that the correct site has been sampled, the clip has deployed, and any complications, namely haematoma. The clip should be visible on all three techniques; MRI, mammography, and US.32 Post-
procedure, an ice pack and compression are applied to achieve haemostasis and minimise the bruising, with prolonged manual compression needed in a small proportion of cases.33
Complications MRI-guided VAB biopsy has very low morbidity rates, estimated between 0e6%,29 with similar rates to stereotactic VABs. Risk of skin tearing is possible particularly with lesions lying close to the skin surface. Minor complications, such as haematoma and pain, may occur during or immediately after the procedure. Adverse effects requiring abandoning the procedure are rare and reported at around 10%, although in our institution we have found this to be much lower34 (Fig 4).
Radiologicalepathological correlation Management decisions regarding MRI-guided biopsy results should be made in a multidisciplinary team (MDT) meeting, taking into consideration histopathological and imaging correlation and individual patient risk factors.1 MRI-guided breast biopsy has particular challenges when considering radiological and pathological correlation. Not only is the initial targeting of the lesion more difficult than with US or stereotactic biopsy, with the target lesion often not remaining visible and/or enhancing during the procedure, but post-procedure haematoma and fiducial artefact often make it difficult to determine if the correct area has been sampled.
Figure 5 A 63-year-old patient with mammographically screen-detected left multifocal disease. (a) US biopsy confirmed invasive carcinoma NST. MRI performed for neoadjuvant chemotherapy. (b) A linear area of enhancement was seen in the contralateral right breast. Second-look US demonstrated a diffuse hypoechoic area in the central right breast, with subsequent US-guided fan biopsy. Histopathology indicated atypical lobular hyperplasia (ALH), B3. The MDT opinion was non-concordant results. (c) The patient proceeded to MRI biopsy with the resulting histopathology indicating invasive carcinoma B5b. The patient proceeded to bilateral mastectomy.
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In the case of malignant lesions, the histopathological results prove the success of the biopsy, but given that malignancy rates for MRI-guided biopsy are only in the region of 20e30%, this means that it is of utmost importance to be able to recognise concordant from discordant benign biopsy results. The positive predictive value (PPV) for malignancy depends on a number of factors. Breast MRI is already restricted to particular populations with higher risk of disease, but within this cohort there are variations in the PPV for particular referral populations, with higher rates seen in women undergoing breast MRI for preoperative staging that for screening.21,35 Higher PPV are also seen with increasing BI-RADS category (BI-RADS 3 13.3%, BI-RADS 4
Figure 6 A 54-year-old patient with right-sided lobular cancer. (aeb) MRI demonstrated an additional focal area of non-mass enhancement in the medial aspect of the contralateral left breast as seen on postcontrast T1-weighted and FS images. (c) No correlation was found on the unenhanced T2-weighted imaging. MRI-guided biopsy was performed and histopathology confirmed hamartoma, B2. Either short-interval follow-up or repeat MRI-guided biopsy was considered the appropriate management.
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41.8%, BI-RADS 5 62.8%),9 and for mass lesions compared to non-mass lesions (57% versus 35%).33 Although greater lesion size is of importance in predicting malignancy rates in MRI-detected lesions, the PPV for lesions 5 mm has been shown to be as high as 20%,36 highlighting the importance of not dismissing small <5 mm lesions in women with a known cancer, particularly if it is close to the original malignancy.
Figure 7 A 48-year-old patient with biopsy-proven DCIS in the inferior central right breast on conventional imaging (mammography and stereotactic biopsy). MRI was performed to assess the extent and plan surgery. (a) Non-mass enhancement seen in the inferior right breast corresponding to DCIS. (b) An additional small focus of nonmass enhancement was seen in the deep posterior right breast. Mammography reviewed and second-look US performed with no abnormality detected. (c) The patient proceeded to MRI-guided biopsy with the marker seen in the correct position within the breast. Histopathology demonstrated pseudoangiomatous stromal hyperplasia (PASH), B2 and the radiology and histopathology findings were felt to be concordant at the MDT.
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Lack of ability to correlate the specimen sample with the original lesion proves a further challenge for the radiologist in MRI-guided biopsies. This is also a challenge for the histopathologist, as many lesions that are sampled are nonmass enhancement, which makes it difficult to confirm that the correct lesion has been sampled (Figs 5 and 6). It is also often the case that mass lesions on MRI do not correspond to mass lesions histologically, and conversely, for Non mass enhancement (NME) which can yield diagnoses such as invasive carcinomas and fibroadenomas.37 Some authors recommend in this case taking into account additional pathological criteria, including a clear interface with the surrounding tissue for mass lesions and having a high level of awareness for PASH and fibrosis, which often corresponds radiologically and pathologically to regional NME37 (Fig 7). The other challenge with radiologicalepathological correlation in MRI-guided biopsy is the relatively high underestimation rates compared to stereotactic and US-guided biopsy. High-risk lesions detected only at MRI are increasing as more MRI-guided biopsies are being undertaken, with the incidence ranging from 3e21%. Upgrade rates at surgery of MRI-biopsied atypical ductal hyperplasia (ADH) are 19e38% compared with 20% after stereotactic biopsy, and similarly 5e25% of MRI-biopsied DCIS are upgraded to invasive carcinoma at surgery, compared with 11% after stereotactic biopsy.35,38e40 This may be because of the higher risk of breast cancer in the MRI-detected group, with features on MRI overlapping those of malignant lesions with no specific imaging features that can predict upgrade to malignancy. For this reason, some authors recommend excision of all high-risk lesions, particularly if there has been a history of breast cancer.40
Given the difficulty in distinguishing concordant from discordant results, and with false-negative rates after benign MRI biopsy with concordant histology reported at around 2.5%, most centres recommended follow-up for benign lesions detected on MRI-guided biopsy.41 Most centres, including our own, recommend a 6-month followup. Some authors advocate performing a repeat contrastenhanced MRI 24 hours after the initial MRI biopsy to increase diagnostic accuracy and eliminate missed cancers, particularly if the lesions are in the ipsilateral breast of a women with known or previous breast cancer.42 There are, however, no data on the total length of time follow-up should be performed for, and in our institution, after a 6month follow-up no further imaging is performed. It is imperative that MDT decisions on appropriate follow-up are clearly documented and conveyed to the referring hospital to ensure that follow-up is performed (Fig 8).
Conclusion As the demand for breast MRI continues to rise with indications including high-risk screening, neoadjuvant chemotherapy, and preoperative planning, so too does the requirement for MRI-guided biopsy of lesions that cannot be identified on second-look US. Whether performing the biopsy or referring a patient for the procedure to be undertaken, it is important that breast radiologists understand the challenges that may be faced in accurately targeting and sampling MRI-detected breast lesions, and the necessity of appropriate follow-up to ensure accurate radiologicalepathological correlation.
Figure 8 MRI-guided biopsy management flow chart.
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