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MR Imaging-guided Percutaneous Tumor Ablation1
MR Imaging-guided Percutaneous Tumor Ablation1 Stuart G. Silverman, MD, Kemal Tuncali, MD, Paul R. Morrison, MS
Percutaneous tumor ablation, or the focal treatment of tumors through the use of needle-like probes placed through the skin, is becoming a mainstream therapeutic approach for a variety of oncologic conditions (1– 4). Common to all these procedures is the central role of imaging guidance, without which these procedures could not be performed. Magnetic resonance (MR) imaging (MRI) has joined computed tomography (CT) and ultrasound (US) as principal cross-sectional guidance modalities used to guide percutaneous tumor ablations (5,6). This article reviews the fundamental roles that imaging has in the performance of percutaneous tumor ablation. We explain the benefits and limitations of MRI and present an overview of how MRI can be used to guide percutaneous ablations today. Our clinical Tumor Ablation Program uses MRI, CT, and US to perform percutaneous tumor ablations throughout the body by using a variety of ablative agents (7–10) (Figure 1). In our clinical practice, one imaging guidance modality is not appropriate for all patients; the choice of guidance modality typically is determined by multiple factors, including those related to the patient (eg, contraindications and comorbidity), tumor (eg, location, size, and appearance), and operator preference. For example, a patient may have a ferrous metallic implant that makes MRI guidance impossible, necessitating the use of CT or US. A tumor may be visible with only MRI. Several types of ablative agents may be used; one has not
Acad Radiol 2005; 12:1100 –1109 1 From the Department of Radiology, Division of Abdominal Imaging and Intervention, Brigham & Women’s Hospital, 75 Francis Street, Boston, Massachusetts 02115. Received April 22, 2005; Accepted May 3. Presented as a plenary lecture at the 5th Interventional MRI Symposium, Boston, Massachusetts, October 15–16, 2004. Address correspondence to: S.G.S. e-mail: [email protected]
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emerged as superior to the others. Both heat-based and cold-based methods are effective in ablating tumors. In the future, one agent may be found to be preferable for a particular tumor type or location. There are five fundamental roles for imaging in the performance of an image-guided percutaneous ablation; planning, targeting, monitoring, controlling, and assessment (5,11). These terms may be applied regardless of which ablative agent or guidance modality is used. Planning occurs before the procedure; assessment occurs after the procedure. Targeting, monitoring, and controlling all take place during the procedure.
PREPROCEDURE IMAGING FOR ABLATION PLANNING Imaging is used first to plan an ablation. Diagnostic imaging tests (eg, CT or MRI), often performed days to weeks before the treatment, are used to detect, characterize, and diagnose the tumor. Preprocedural diagnosis is a critical component in selecting an appropriate treatment. Therefore, percutaneous image-guided tumor biopsy often is needed. This was shown recently in a review of patients referred for ablation of renal tumors (12). This study showed that 37% of patients who were thought to have renal cell carcinoma had benign disease detected only by a thorough preprocedural imaging evaluation, with percutaneous biopsy in selected cases. In addition to diagnosis, planning the procedure involves tumor staging. The extent to which imaging is used to stage a tumor depends on tumor type. However, in general, imaging is used to assess for regional spread and metastatic disease. Because ablation is a focal treatment, the presence of metastatic disease means that focal treatment would only be palliative. Typically, CT is used to stage many cancers. MRI may
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Figure 1. The Tumor Ablation Program at Brigham and Women’s Hospital uses a variety of percutaneous ablation techniques (cryotherapy, RF ablation [RFA], and alcohol [ETOH]) that are coupled with MRI, CT, and US to treat tumors throughout the body.
or may not be necessary to diagnose and stage a particular tumor, but as MRI-guided treatment is planned, MRI is useful in showing how the tumor would appear during the procedure. A third aspect to planning an ablation with imaging is to show the surrounding anatomy such that an appropriate percutaneous path is chosen. For example, a preprocedural imaging examination may show that a patient’s renal mass is contiguous to the colon. This allows the operator to change the patient’s position from a conventional supine position to a slightly oblique position to move the colon away from the tumor. It may be helpful to obtain a second preprocedure imaging examination in the altered position to confirm that the planned path would be suitable. We often use this approach in performing MRI-guided ablations because the appropriate position must be known before inducing general anesthesia in our openconfiguration MRI system. Finally, preprocedural imaging is used to define the shape, size, and boundaries of the tumor. Knowledge of the three-dimensional (3D) shape of the tumor allows us to choose an appropriate ablation probe size and number, such that the ablation will encompass the tumor completely.
TUMOR TARGETING Targeting a tumor with a single or multiple needlelike probes requires imaging to display the target, as well as the surrounding anatomy, so that each probe can be placed accurately within the tumor without injuring nearby critical structures. This process is fundamental and akin to a percutaneous biopsy. However, in
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the case of tumor ablation, the demands are greater. Unlike biopsy, when a needle must be placed simply in any portion of the tumor, in the case of ablation, a single probe must be centered within the tumor or multiple probes need to be placed such that the subsequent ablation completely encompasses the tumor and does not harm nearby critical structures. As a result, demands on the guidance system are greater. Ideally, the guidance system used for targeting should be real-time and interactive, such that the operator can view the probe at all times and change the probe’s position as needed during the procedure (13). Also, an ideal guidance system should provide multiplanar or 3D images so that the probe’s relationship to the target can be seen from multiple vantage points (Figure 2). A probe tip may appear within a tumor in one plane, but be located outside the tumor when viewed in a different plane. MRI can be used to target tumors for purposes of either biopsy or ablation (13–15). Once a hindrance to MRI-guided intervention, MR-compatible needles and therapy probes now are available commercially (16,17). Virtually all MRI systems commercially available today can be used for tumor ablation. Closed MRI systems use high field strengths, typically 1.5 to 3.0 Tesla (T), and, as a result, provide the best image quality. However, access to the patient is limited. Targeting must occur outside a closed MRI system (typically using CT or US). MRI then is used to confirm the probe position and monitor the ablation (18,19). Short-bore closed systems also provide excellent image quality, but access is still limited and only slightly better than with other closed systems (20,21). Open-configuration MRI systems, initially manufactured to combat claustrophobia, improve patient access substantially. The horizontal open-gap magnet design provides side access to the supine patient, but is somewhat limited, particularly to the anterior abdomen (15). The vertically openmagnet design, used at our institution, provides full access (6,7,10,13,14) and contains an integrated frameless stereotactic guidance system for targeting that is based on optical tracking. Nonetheless, a variety of targeting technologies exist that also may be used for guiding probes (22–25). Such technologies include optical guidance systems that are not built in to the scanner, but are “add-on” devices housed adjacent to the MRI scanner; localization is based on registering the anatomy to an image data set (22). Nonoptical means of targeting have been devel-
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Figure 2. Tumor targeting with multiplanar visualization. (a) Intraprocedural axial MRI (0.5 T; T1-weighted fast spin echo; repetition time [TR]/echo time [TE], 500/26; section thickness, 10 mm; field of view, 32 cm) of liver tumor (arrow) before biopsy needle placement. (b) Subsequent axial image shows two needles in good medial-lateral position. (c) Superior-inferior position of one of the needles is confirmed by an acquisition in the sagittal plane. The diagnosis was hepatocellular carcinoma. (Excerpted from [6] Mortele KJ et al. MRIguided abdominal intervention. Abdom Imaging 2003; 28:756-774 with kind permission of Springer Science and Business Media.)
oped that take place real-time within the scanner and are based on image-related data (23,24). Examples include passive MRI-based techniques, such as the use of combined 19-fluorine resonance with standard proton resonance imaging to track the tips of devices (23), and active tracking using tip-mounted radiofrequency (RF) microcoils that can be identified in an MR image (24). Also, RF microcoils can be used to locate a device in the magnet bore by their electromagnetic response to the local magnetic field intensities within the gradients of the scanner (25). In general, problems of instrument compatibility, patient access, and targeting methods have been solved such that MRI now can be used to guide ablations throughout the body by using virtually any commercially available system. MRI can provide real-time, interactive, and multiplanar approaches that rival targeting systems available with US and CT.
MONITORING AN ABLATION Monitoring is a fundamental role of imaging in ablations. It is an important component, the portion of the
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Table 1 Characteristics of Cross-sectional Imaging Modalities Used to Guide Tumor Ablation Viewed
US
CT
MRI
Tissue changes Entire iceball Iceball and tumor Real time Multiplanar
Yes No No Yes Yes
Yes Yes No No No
Yes Yes Yes Yes Yes
Effective image-guided ablation requires imaging that provides full visualization of the tumor and ablation effects. The table shows features of MRI that make it an ideal choice for guiding cryotherapy. In particular, only MRI can be used to distinguish cryotherapy effects from tumor. Although CT can provide multiplanar views, reconstruction times limit their use during ablations. In addition, real-time CT scanning, using CT fluoroscopy, can be used to only a limited extent to minimize radiation exposure to the patient and interventional radiologist.
procedure during which the interventional radiologist visualizes treatment effects as they occur. The goal of an ablation procedure is to achieve complete ablation of a tumor without affecting adjacent critical structures. This can be achieved best if the tumor, ablation effects,
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Figure 3. Ablation monitoring requires imaging frequently enough to observe events in tissue. (a) Intraprocedural MRI (0.5 T; T2weighted fast spin echo; TR/TE, 6000/92; section thickness, 8 mm; field of view, 28 cm) in the sagittal plane shows two cryoprobes (arrowheads) in a tumor (arrow). (b) During freezing, iceballs form around the end of each cryoprobe. (c) A small amount of residual tumor is seen (arrow). (d) With continued freezing, the iceball eclipses the entire tumor.
and surrounding anatomy are each visualized in multiple planes throughout the treatment. It is for this fundamental role that MRI has its greatest advantage (7,10). For example, CT and US can be used to direct an RF probe into a tumor. However, ablative effects are seen only partially by using CT or US. Imaging findings at CT or US do not correlate with postprocedural necrosis. Therefore, an ablation protocol (ie, where and how long to treat) can be planned only on the basis of an estimate of necrosis. Manufacturers of
RF ablation equipment provide information to users about an expected ablation volume based on probe type and size. As a result, RF ablation under CT and US guidance is successful in many cases, particularly when tumors are small and critical structures are not nearby. In these cases, for example, overtreating a tumor and sacrificing surrounding normal tissues may not be clinically relevant. However, actual ablation volumes may vary by patient, organ of origin, and tumor type (26,27). Therefore, in the case of large tumors or when
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Figure 4. During MRI-guided percutaneous cryotherapy, intraprocedural monitoring shows iceballs that correlate closely to the zones of ablation. (a) Two liver tumors caused by metastatic esophageal cancer are seen as hypointense masses in the axial plane on preablation contrast-enhanced MRI (1.5 T; gradient echo; TR/TE, 480/4.2; flip angle, 75°; section thickness, 4 mm; field of view, 34 cm). (b) MRI during the procedure (0.5 T; T1-weighted spoiled gradient echo; TR/TE, 250/ 10.4; flip angle, 75°; section thickness, 8 mm; field of view, 22 cm) shows the iceball (arrowheads) encompassing both tumors. (c) A postablation contrast-enhanced MR image (1.5 T; gradient echo; TR/TE, 480/4.2; flip angle, 75°; section thickness, 4 mm; field of view, 34 cm) shows a region of necrosis that corresponds closely to the region encompassed by the iceball in (b).
critical structures are nearby, the unpredictability of a resultant RF ablation would be clinically relevant and potentially lead to undertreatment, harm to a nearby structure, or both. Therefore, monitoring ablations such that the margins of ablative effects are viewed in multiple planes during the procedure would ensure that the
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tumor was covered in its entirety and nearby critical structures are unharmed. MRI provides such monitoring (7,10,15–17,28). During cryotherapy, for example, tissue changes as a result of freezing can be viewed with US, CT, and MRI (10,29,30) (Table 1). However, tissue changes can be viewed in their
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Figure 5. Multiplanar MRI can be used to monitor cryoablation and avoid nearby critical structures. (a) During MRI-guided cryotherapy of a liver tumor abutting the diaphragm, coronal MRI (0.5 T; T1-weighted spoiled gradient echo; TR/TE, 250/9.8; flip angle, 75°; section thickness, 6 mm; field of view, 28 cm) provides visualization of the adjacent diaphragm (arrowheads), lung (L), and heart (H). (b) During freezing, the iceball’s growth was limited to avoid freezing them.
entirety only with CT and MRI. Because of acoustic shadowing at the iceball’s edge, the distal portion of an iceball becomes invisible at US, akin to a kidney stone. Although cryotherapy in general decreases CT attenuation (30,31), these changes cannot be differentiated from tumors that are often similarly hypodense. However, MRI can be used to distinguish tumors that appear bright when using T2-weighted sequences, from iceballs that appear as signal voids on all conventional MRI sequences (Figure 3). Therefore, MRI and cryotherapy are a good match of a guidance modality and ablative agent. MRI also can be used to monitor RF ablations (15). However, RF devices interfere with MRI; therefore, MRI cannot take place simultaneously with the ablation unless the RF energy is properly filtered to remove high-frequency noise or gated with the MR image acquisition (15). In addition to depicting the iceball, tumor, and surrounding anatomy in multiple planes, effects visualized
during cryotherapy correlate with estimates of tissue necrosis, determined by postprocedural MRI at 1.5 T (10) (Figure 4). To be confident that what is viewed during an ablation procedure translates to posttreatment effects is fundamentally important. A one-to-one correlation between what is viewed during an ablation and what effects are achieved may not be possible with other technologies. For example, during CT-guided RF ablation, if saline were injected at the site of the RF ablation, the burn may extend beyond the intended treatment area because of extension of the saline away from the tumor (32,33). Another important aspect to monitoring is the ability to see effects in multiple planes. Unlike CT, MRI provides imaging in virtually any plane. As a result, the operator may select the plane that best depicts the critical structure at risk. For example, a tumor at the liver dome may abut the diaphragm, lung, or heart. These structures are shown best in the sagittal or coronal planes (Figure 5).
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Figure 6. An ablation can be controlled if both thermal effects and tumor are seen throughout the procedure. (a) An axial view (0.5 T; T2-weighted fast spin echo; TR/TE, 6000/92; section thickness, 8 mm; field of view, 30 cm) shows a hyperintense breast cancer metastasis to the liver with cryoprobes in place (arrows). (b) During MRI-guided cryotherapy, the axial image of the iceball (arrowheads) suggests that the tumor is treated fully. (c) However, in the oblique sagittal plane, untreated tumor (arrow) is seen at its superior margin. (d) This portion of tumor was treated by placing an additional probe (arrow) and freezing the rest of the tumor, confirmed in (e) the final oblique sagittal view. (b– e) Same scan parameters as in (a).
Figure 7. MRI provides excellent visualization of both ablation effects and nearby critical structures. (a) Coronal MRI image (0.5 T; fast gradient echo; TR/TE, 25.9/13.1; flip angle, 90°; section thickness, 8 mm; field of view, 28 cm) shows a peripheral exophytic renal cell carcinoma with a cryoprobe (arrow) in place. (b) During cryotherapy, a repeated scan in the same coronal plane shows the iceball covering the tumor without affecting the adjacent colon (arrow), (c) confirmed in the sagittal plane. (b, c) Same scan parameters as in (a).
CONTROLLING ABLATIVE EFFECTS IN TISSUE Controlling an ablation procedure is the third important intraprocedural role of imaging. To control an ablation, the imaging system must be able to monitor the process as described. However, simply monitoring the
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process does not necessarily mean that the ablation can be controlled. Control of an ablation is derived from the ability to reposition a given probe or modify its effects in some way based on what is viewed during the procedure. Using an open-configuration MRI system, ablation probes may be repositioned in regions of tumor that are not being treated (Figure 6). Using a
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(34) (Figure 8). With a suitable feedback/control mechanism, the computer then could be used to automatically adjust device parameters to control the ablation (34).
ABLATION ASSESSMENT
Figure 8. Computer-assisted visualization of the ablation process in three dimensions can add to the control provided during an image-guided ablation. By registering adjacent critical anatomic structures within a computer program that monitors the entire iceball in real-time, software can warn the user when the two are due to intersect. (a) A critical structure (arrow) has been identified and is shown in green in a 3D view. The tumor is shown as yellow mesh; the developing iceball is shown in blue. (b) The iceball (arrowheads) is shown in cross-section in a 2D image. (c) The calculated growth pattern of the iceball provides (d) a prediction of the treated zone.
closed system, MRI can be used to monitor the ablation, but if a portion of the tumor is not being treated fully, the patient needs to be moved from the MRI system to the CT or US suite to place additional probes (18,19). Control of the ablation process also is achieved by imaging frequently to observe the growth of the ablation volume and alter the applied thermal dose. This can be achieved by repetitive intraprocedural imaging of the volume during application of the treatment. The physician then can review the images and make a determination of the tissue effects, manually adjusting the ablation device parameters accordingly (Figure 7). This also can be achieved by computer-assisted means that perform an ongoing analysis of image data in three dimensions (34). The computer is used to assess coverage, calculate thermal dosimetry, and predict the spatial extent of the thermal effect at a subsequent time point
Imaging has a critical role in the assessment of an ablation procedure. The goal of imaging is to assess how well the tumor was ablated, check for complications, and evaluate for metastases. Experience is accumulating on how imaging is used to assess the completeness of an ablation, and research is ongoing (35– 39). Investigators have largely used CT rather than MRI because of its lower cost and wider availability; however, MRI may be better suited for some patients, such as those with tumors that are shown best with MRI. We typically use MRI to follow up patients undergoing MRI-guided therapies because it allows us to directly compare follow-up imaging findings with intraprocedural images to better understand findings and interpret their results. For example, if a portion of a tumor shows residual enhancement and is suspicious for residual tumor, we can directly correlate these findings with intraprocedural MR images to see whether the portion in question was treated. It then also allows us to use the same MR images to plan subsequent MRI-guided therapies. If CT or US were used, it would be more difficult to translate this information to the MRI frame of reference. Radiologists who interpret images obtained in patients treated with ablation should be cognizant of expected changes in ablation at MRI. The imaging appearance of the ablated tumor is beginning to be investigated (35–38). First, the radiologist should be familiar with what constitutes recurrent tumor. In general, nodular enhancement is considered suspicious for recurrent tumor and should be distinguished from rim enhancement, often seen within the first month after an ablation (38). RF ablation and cryotherapy appear to have common effects and appearances by MRI. They both appear to shorten T1 and T2 relaxation times and eliminate contrast enhancement in the ablation zone. Because detecting nodular enhancement is a critical step in detecting recurrent tumors, careful signal-intensity analysis needs to be performed. Short T1 effects, which typically appear bright on fat-suppressed T1-weighted images, need to be subtracted either visually or quantitatively from contrast-enhanced images.
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SUMMARY
Figure 9. Assessment of tumor ablations is a 3D task. Tissues affected by the ablation are 3D spaces within the body. The figure shows a 3D reconstruction of a lung cancer metastasis (arrow), shown in yellow, in the liver treated with MRI-guided cryotherapy. The tumor volume is covered completely by the outer cryoablation volume (short arrow), shown in blue. The ablation volume also covers an expanded volume (arrowheads) that includes the tumor plus a computer-generated 1-cm ablation margin. (Excerpted from [39] Silverman SG et al. Three-dimensional assessment of MRI-guided percutaneous cryotherapy of liver metastases. AJR Am J Roentgenol 2004; 83:707–712 with kind permission of the publisher.)
Tumor ablation is a 3D problem; therefore, future approaches to ablation assessment (as well as planning) will require 3D imaging (Figure 9). Using volumetric techniques in CT and MRI, 3D images of tumors can be created and coupled with 3D assessments of an ablation (39). From these volumetric data, metrics can be derived such that there is a quantitative assessment of how much tumor was covered, how much normal tissue was sacrificed, and whether an ablation margin (akin to a surgical margin) was achieved. It has been shown that percentage of tumor coverage and percentage of target volume coverage (in which target volume includes both the tumor and a 1-cm ablation margin) correlate with response (39). These measurements could be calculated soon after an ablation and used to predict which tumors might recur so that subsequent treatments can be instituted early. In the future, these 3D metrics could be calculated and shown to the operator intraprocedurally and thus help increase the chances that the ablation is carried out completely and safely.
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In summary, MRI can be used to fulfill all the fundamental roles of imaging when ablating tumors: planning, targeting, monitoring, controlling, and assessment. Intraprocedural monitoring is a particularly important component. The ability of MRI to monitor ablations (particularly using cryotherapy) is unique relative to other guidance modalities. However, as noted, MRI is only one of three cross-sectional imaging modalities that can be used to guide tumor ablations safely and effectively. With additional experience and research, the precise role of MRI will be defined more clearly in the future. Tumor ablation rapidly is becoming the standard of care for the treatment of a variety of tumors and, like radiation therapy today, will become an important component of the treatment of many oncologic conditions in the future. MRI will continue to be an important imaging modality in the care of patients treated with percutaneous tumor ablation. REFERENCES 1. Livraghi T, Solbiati L, Meloni MF, et al. Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study. Radiology 2003; 226:441– 451. 2. Wood BJ. Percutaneous tumor ablation with radiofrequency. Cancer 2002; 94:433– 451. 3. Dupuy DE, Goldberg SN. Image-guided radiofrequency tumor ablation: challenges and opportunities—part II. J Vasc Interv Radiol 2001; 12:1135– 1148. 4. Goldberg SN, Dupuy DE. Image-guided radiofrequency tumor ablation: challenges and opportunities—part I. J Vasc Interv Radiol 2001; 12:1021– 1032. 5. Jolesz FA, Blumenfeld SM. Interventional use of magnetic resonance imaging. Magn Reson Q 1994; 10:85–96. 6. Mortele KJ, Tuncali K, Cantisani V, et al. MRI-guided abdominal intervention. Abdom Imaging 2003; 28:756 –774. 7. Silverman SG, Tuncali K, vanSonnenberg E, et al. Renal tumors: MR imaging— guided percutaneous cryotherapy initial experience in 23 patients. Radiology 2005;236:716-724. 8. vanSonnenberg E, Shankar S, Morrison PR, et al. Radiofrequency ablation of thoracic lesions: part II. Initial clinical experience—technical and multidisciplinary considerations in 30 patients. AJR Am J Roentgenol 2005; 184:381–390. 9. Shankar S, vanSonnenberg E, Morrison PR, Tuncali K, Silverman SG. Combined radiofrequency and alcohol injection for percutaneous hepatic tumor ablation. AJR Am J Roentgenol 2004; 183:1425–1429. 10. Silverman SG, Tuncali K, Adams DF, et al. MR imaging-guided percutaneous cryotherapy of liver tumors: initial experience. Radiology 2000; 217:657– 664. 11. Goldberg SN, Charboneau JW, Dodd GD III, et al. Image-guided tumor ablation: proposal for standardization of terms and reporting criteria. Radiology 2003; 228:335–345. 12. Tuncali K, vanSonnenberg E, Shankar S, Mortele KJ, Cibas ES, Silverman SG. Evaluation of patients referred for percutaneous ablation of renal tumors: importance of a preprocedural diagnosis. AJR Am J Roentgenol 2004; 183:575–582. 13. Silverman SG, Collick BD, Figueira MR, et al. Interactive MR-guided biopsy in an open-configuration MR imaging system. Radiology 1995; 197:175–181.
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14. Schenck JF, Jolesz FA, Roemer PB, et al. Superconducting open-configuration MR imaging system for image-guided therapy. Radiology 1995; 195:805– 814. 15. Lewin JS, Nour SG, Connell CF, et al. Phase II clinical trial of interactive MR imaging-guided interstitial radiofrequency thermal ablation of primary kidney tumors: initial experience. Radiology 2004; 232:835– 845. 16. Silverman SG, Jolesz FA, Newman RW, et al. Design and implementation of an interventional MR imaging suite. AJR Am J Roentgenol 1997; 168:1465–1471. 17. Jolesz FA, Morrison PR, Koran SJ, et al. Compatible instrumentation for intra-operative MRI: Expanding resources. J Magn Reson Imaging 1998; 8:8 –11. 18. Vogl TJ, Straub R, Eichler K, Sollner O, Mack MG. Colorectal carcinoma metastases in liver: laser-induced interstitial thermotherapy— local tumor control rate and survival data. Radiology 2004; 230:450 – 458. 19. Mack MG, Straub R, Eichler K, Sollner O, Lehnert T, Vogl TJ. Breast cancer metastases in liver: laser-induced interstitial thermotherapy— local tumor control rate and survival data. Radiology 2004; 233:400 – 409. 20. Liu H, Hall WA, Martin AJ, Maxwell RE, Truwit CL. MR-guided and MRmonitored neurosurgical procedures at 1.5 T. J Comput Assist Tomogr 2000; 24:909 –918. 21. Tummala RP, Chu RM, Liu H, Truwit CL, Hall WA. Optimizing brain tumor resection. High-field interventional MR imaging. Neuroimaging Clin North Am 2001; 11:673– 683. 22. Nimsky C, Ganslandt O, Von Keller B, Romstock J, Fahlbusch R. Intraoperative high-field-strength MR imaging: implementation and experience in 200 patients. Radiology 2004; 233:67–78. 23. Kozerke S, Hegde S, Schaeffter T, Lamerichs R, Razavi R, Hill DL. Catheter tracking and visualization using 19F nuclear magnetic resonance. Magn Reson Med 2004; 52:693– 697. 24. Wacker FK, Elgort D, Hillenbrand CM, Duerk JL, Lewin JS. The catheter-driven MRI scanner: a new approach to intravascular catheter tracking and imaging-parameter adjustment for interventional MRI. AJR Am J Roentgenol 2004; 183:391–395. 25. Nevo E. Method and apparatus to estimate location and orientation of objects during magnetic resonance imaging. US Patent 6,516,213, February 4, 2003. 26. Ahmed M, Liu Z, Afzal KS, et al. Radiofrequency ablation: effect of surrounding tissue composition on coagulation necrosis in a canine tumor model. Radiology 2004; 230:761–767.
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27. Montgomery RS, Rahal A, Dodd GD III, Leyendecker JR, Hubbard LG. Radiofrequency ablation of hepatic tumors: variability of lesion size using a single ablation device. AJR Am J Roentgenol 2004; 182:657– 661. 28. Mala T, Aurdal L, Frich L, et al. Liver tumor cryoablation: a commentary on the need of improved procedural monitoring. Technol Cancer Res Treatment 2004; 3:85–91. 29. Nadler RB, Kim SC, Rubenstein JN, Yap RL, Campbell SC, User HM. Laparoscopic renal cryosurgery: the Northwestern experience. J Urol 2003; 170:1121–1125. 30. Sandison GA, Loye MP, Rewcastle JC, et al. X-Ray CT monitoring of iceball growth and thermal distribution during cryosurgery. Phys Med Biol 1998; 43:3309 –3324. 31. Lee FT Jr, Chosy SG, Littrup PJ, Warner TF, Kuhlman JE, Mahvi DM. CT-monitored percutaneous cryoablation in a pig liver model: pilot study. Radiology 1999; 211:687– 692. 32. Kettenbach J, Kostler W, Rucklinger E, et al. Percutaneous saline-enhanced radiofrequency ablation of unresectable hepatic tumors: initial experience in 26 patients. AJR Am J Roentgenol 2003; 180:1537–1545. 33. Giorgio A, Tarantino L, de Stefano G, Coppola C, Ferraioli G. Complications after percutaneous saline-enhanced radiofrequency ablation of liver tumors: 3-year experience with 336 patients at a single center. AJR Am J Roentgenol 2005; 184:207–211. 34. Zientara GP, Saiviroonporn P, Morrison PR, et al. MRI-monitoring of laser ablation using optical flow. J Magn Reson Imaging 1998; 8:1306 – 1318. 35. Cestari A, Guazzoni G, dell’Acqua V, et al. Laparoscopic cryoablation of solid renal masses: intermediate term followup. J Urol 2004; 172: 1267–1270. 36. Matsumoto ED, Watumull L, Johnson DB, et al. The radiographic evolution of radio frequency ablated renal tumors. J Urol 2004; 172:45– 48. 37. Kim SK, Lim HK, Kim YH, et al. Hepatocellular carcinoma treated with radio-frequency ablation: spectrum of imaging findings. Radiographics 2003; 23:107–121. 38. Kim TJ, Moon WK, Cha JH, et al. VX2 carcinoma in rabbits after radiofrequency ablation: comparison of MR contrast agents for help in differentiating benign periablational enhancement from residual tumor. Radiology 2005; 234:423– 430. 39. Silverman SG, Sun MRM, Tuncali K, et al. Three-dimensional assessment of MRI-guided percutaneous cryotherapy of liver metastases. AJR Am J Roentgenol 2004; 83:707–712.
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Percutaneous tumor ablation, or the focal treatment of tumors through the use of needle-like probes placed through the skin, is becoming a mainstream therapeutic approach for a variety of oncologic conditions (1– 4). Common to all these procedures is the central role of imaging guidance, without which these procedures could not be performed. Magnetic resonance (MR) imaging (MRI) has joined computed tomography (CT) and ultrasound (US) as principal cross-sectional guidance modalities used to guide percutaneous tumor ablations (5,6). This article reviews the fundamental roles that imaging has in the performance of percutaneous tumor ablation. We explain the benefits and limitations of MRI and present an overview of how MRI can be used to guide percutaneous ablations today. Our clinical Tumor Ablation Program uses MRI, CT, and US to perform percutaneous tumor ablations throughout the body by using a variety of ablative agents (7–10) (Figure 1). In our clinical practice, one imaging guidance modality is not appropriate for all patients; the choice of guidance modality typically is determined by multiple factors, including those related to the patient (eg, contraindications and comorbidity), tumor (eg, location, size, and appearance), and operator preference. For example, a patient may have a ferrous metallic implant that makes MRI guidance impossible, necessitating the use of CT or US. A tumor may be visible with only MRI. Several types of ablative agents may be used; one has not
Acad Radiol 2005; 12:1100 –1109 1 From the Department of Radiology, Division of Abdominal Imaging and Intervention, Brigham & Women’s Hospital, 75 Francis Street, Boston, Massachusetts 02115. Received April 22, 2005; Accepted May 3. Presented as a plenary lecture at the 5th Interventional MRI Symposium, Boston, Massachusetts, October 15–16, 2004. Address correspondence to: S.G.S. e-mail: [email protected]
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emerged as superior to the others. Both heat-based and cold-based methods are effective in ablating tumors. In the future, one agent may be found to be preferable for a particular tumor type or location. There are five fundamental roles for imaging in the performance of an image-guided percutaneous ablation; planning, targeting, monitoring, controlling, and assessment (5,11). These terms may be applied regardless of which ablative agent or guidance modality is used. Planning occurs before the procedure; assessment occurs after the procedure. Targeting, monitoring, and controlling all take place during the procedure.
PREPROCEDURE IMAGING FOR ABLATION PLANNING Imaging is used first to plan an ablation. Diagnostic imaging tests (eg, CT or MRI), often performed days to weeks before the treatment, are used to detect, characterize, and diagnose the tumor. Preprocedural diagnosis is a critical component in selecting an appropriate treatment. Therefore, percutaneous image-guided tumor biopsy often is needed. This was shown recently in a review of patients referred for ablation of renal tumors (12). This study showed that 37% of patients who were thought to have renal cell carcinoma had benign disease detected only by a thorough preprocedural imaging evaluation, with percutaneous biopsy in selected cases. In addition to diagnosis, planning the procedure involves tumor staging. The extent to which imaging is used to stage a tumor depends on tumor type. However, in general, imaging is used to assess for regional spread and metastatic disease. Because ablation is a focal treatment, the presence of metastatic disease means that focal treatment would only be palliative. Typically, CT is used to stage many cancers. MRI may
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Figure 1. The Tumor Ablation Program at Brigham and Women’s Hospital uses a variety of percutaneous ablation techniques (cryotherapy, RF ablation [RFA], and alcohol [ETOH]) that are coupled with MRI, CT, and US to treat tumors throughout the body.
or may not be necessary to diagnose and stage a particular tumor, but as MRI-guided treatment is planned, MRI is useful in showing how the tumor would appear during the procedure. A third aspect to planning an ablation with imaging is to show the surrounding anatomy such that an appropriate percutaneous path is chosen. For example, a preprocedural imaging examination may show that a patient’s renal mass is contiguous to the colon. This allows the operator to change the patient’s position from a conventional supine position to a slightly oblique position to move the colon away from the tumor. It may be helpful to obtain a second preprocedure imaging examination in the altered position to confirm that the planned path would be suitable. We often use this approach in performing MRI-guided ablations because the appropriate position must be known before inducing general anesthesia in our openconfiguration MRI system. Finally, preprocedural imaging is used to define the shape, size, and boundaries of the tumor. Knowledge of the three-dimensional (3D) shape of the tumor allows us to choose an appropriate ablation probe size and number, such that the ablation will encompass the tumor completely.
TUMOR TARGETING Targeting a tumor with a single or multiple needlelike probes requires imaging to display the target, as well as the surrounding anatomy, so that each probe can be placed accurately within the tumor without injuring nearby critical structures. This process is fundamental and akin to a percutaneous biopsy. However, in
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the case of tumor ablation, the demands are greater. Unlike biopsy, when a needle must be placed simply in any portion of the tumor, in the case of ablation, a single probe must be centered within the tumor or multiple probes need to be placed such that the subsequent ablation completely encompasses the tumor and does not harm nearby critical structures. As a result, demands on the guidance system are greater. Ideally, the guidance system used for targeting should be real-time and interactive, such that the operator can view the probe at all times and change the probe’s position as needed during the procedure (13). Also, an ideal guidance system should provide multiplanar or 3D images so that the probe’s relationship to the target can be seen from multiple vantage points (Figure 2). A probe tip may appear within a tumor in one plane, but be located outside the tumor when viewed in a different plane. MRI can be used to target tumors for purposes of either biopsy or ablation (13–15). Once a hindrance to MRI-guided intervention, MR-compatible needles and therapy probes now are available commercially (16,17). Virtually all MRI systems commercially available today can be used for tumor ablation. Closed MRI systems use high field strengths, typically 1.5 to 3.0 Tesla (T), and, as a result, provide the best image quality. However, access to the patient is limited. Targeting must occur outside a closed MRI system (typically using CT or US). MRI then is used to confirm the probe position and monitor the ablation (18,19). Short-bore closed systems also provide excellent image quality, but access is still limited and only slightly better than with other closed systems (20,21). Open-configuration MRI systems, initially manufactured to combat claustrophobia, improve patient access substantially. The horizontal open-gap magnet design provides side access to the supine patient, but is somewhat limited, particularly to the anterior abdomen (15). The vertically openmagnet design, used at our institution, provides full access (6,7,10,13,14) and contains an integrated frameless stereotactic guidance system for targeting that is based on optical tracking. Nonetheless, a variety of targeting technologies exist that also may be used for guiding probes (22–25). Such technologies include optical guidance systems that are not built in to the scanner, but are “add-on” devices housed adjacent to the MRI scanner; localization is based on registering the anatomy to an image data set (22). Nonoptical means of targeting have been devel-
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Figure 2. Tumor targeting with multiplanar visualization. (a) Intraprocedural axial MRI (0.5 T; T1-weighted fast spin echo; repetition time [TR]/echo time [TE], 500/26; section thickness, 10 mm; field of view, 32 cm) of liver tumor (arrow) before biopsy needle placement. (b) Subsequent axial image shows two needles in good medial-lateral position. (c) Superior-inferior position of one of the needles is confirmed by an acquisition in the sagittal plane. The diagnosis was hepatocellular carcinoma. (Excerpted from [6] Mortele KJ et al. MRIguided abdominal intervention. Abdom Imaging 2003; 28:756-774 with kind permission of Springer Science and Business Media.)
oped that take place real-time within the scanner and are based on image-related data (23,24). Examples include passive MRI-based techniques, such as the use of combined 19-fluorine resonance with standard proton resonance imaging to track the tips of devices (23), and active tracking using tip-mounted radiofrequency (RF) microcoils that can be identified in an MR image (24). Also, RF microcoils can be used to locate a device in the magnet bore by their electromagnetic response to the local magnetic field intensities within the gradients of the scanner (25). In general, problems of instrument compatibility, patient access, and targeting methods have been solved such that MRI now can be used to guide ablations throughout the body by using virtually any commercially available system. MRI can provide real-time, interactive, and multiplanar approaches that rival targeting systems available with US and CT.
MONITORING AN ABLATION Monitoring is a fundamental role of imaging in ablations. It is an important component, the portion of the
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Table 1 Characteristics of Cross-sectional Imaging Modalities Used to Guide Tumor Ablation Viewed
US
CT
MRI
Tissue changes Entire iceball Iceball and tumor Real time Multiplanar
Yes No No Yes Yes
Yes Yes No No No
Yes Yes Yes Yes Yes
Effective image-guided ablation requires imaging that provides full visualization of the tumor and ablation effects. The table shows features of MRI that make it an ideal choice for guiding cryotherapy. In particular, only MRI can be used to distinguish cryotherapy effects from tumor. Although CT can provide multiplanar views, reconstruction times limit their use during ablations. In addition, real-time CT scanning, using CT fluoroscopy, can be used to only a limited extent to minimize radiation exposure to the patient and interventional radiologist.
procedure during which the interventional radiologist visualizes treatment effects as they occur. The goal of an ablation procedure is to achieve complete ablation of a tumor without affecting adjacent critical structures. This can be achieved best if the tumor, ablation effects,
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Figure 3. Ablation monitoring requires imaging frequently enough to observe events in tissue. (a) Intraprocedural MRI (0.5 T; T2weighted fast spin echo; TR/TE, 6000/92; section thickness, 8 mm; field of view, 28 cm) in the sagittal plane shows two cryoprobes (arrowheads) in a tumor (arrow). (b) During freezing, iceballs form around the end of each cryoprobe. (c) A small amount of residual tumor is seen (arrow). (d) With continued freezing, the iceball eclipses the entire tumor.
and surrounding anatomy are each visualized in multiple planes throughout the treatment. It is for this fundamental role that MRI has its greatest advantage (7,10). For example, CT and US can be used to direct an RF probe into a tumor. However, ablative effects are seen only partially by using CT or US. Imaging findings at CT or US do not correlate with postprocedural necrosis. Therefore, an ablation protocol (ie, where and how long to treat) can be planned only on the basis of an estimate of necrosis. Manufacturers of
RF ablation equipment provide information to users about an expected ablation volume based on probe type and size. As a result, RF ablation under CT and US guidance is successful in many cases, particularly when tumors are small and critical structures are not nearby. In these cases, for example, overtreating a tumor and sacrificing surrounding normal tissues may not be clinically relevant. However, actual ablation volumes may vary by patient, organ of origin, and tumor type (26,27). Therefore, in the case of large tumors or when
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Figure 4. During MRI-guided percutaneous cryotherapy, intraprocedural monitoring shows iceballs that correlate closely to the zones of ablation. (a) Two liver tumors caused by metastatic esophageal cancer are seen as hypointense masses in the axial plane on preablation contrast-enhanced MRI (1.5 T; gradient echo; TR/TE, 480/4.2; flip angle, 75°; section thickness, 4 mm; field of view, 34 cm). (b) MRI during the procedure (0.5 T; T1-weighted spoiled gradient echo; TR/TE, 250/ 10.4; flip angle, 75°; section thickness, 8 mm; field of view, 22 cm) shows the iceball (arrowheads) encompassing both tumors. (c) A postablation contrast-enhanced MR image (1.5 T; gradient echo; TR/TE, 480/4.2; flip angle, 75°; section thickness, 4 mm; field of view, 34 cm) shows a region of necrosis that corresponds closely to the region encompassed by the iceball in (b).
critical structures are nearby, the unpredictability of a resultant RF ablation would be clinically relevant and potentially lead to undertreatment, harm to a nearby structure, or both. Therefore, monitoring ablations such that the margins of ablative effects are viewed in multiple planes during the procedure would ensure that the
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tumor was covered in its entirety and nearby critical structures are unharmed. MRI provides such monitoring (7,10,15–17,28). During cryotherapy, for example, tissue changes as a result of freezing can be viewed with US, CT, and MRI (10,29,30) (Table 1). However, tissue changes can be viewed in their
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Figure 5. Multiplanar MRI can be used to monitor cryoablation and avoid nearby critical structures. (a) During MRI-guided cryotherapy of a liver tumor abutting the diaphragm, coronal MRI (0.5 T; T1-weighted spoiled gradient echo; TR/TE, 250/9.8; flip angle, 75°; section thickness, 6 mm; field of view, 28 cm) provides visualization of the adjacent diaphragm (arrowheads), lung (L), and heart (H). (b) During freezing, the iceball’s growth was limited to avoid freezing them.
entirety only with CT and MRI. Because of acoustic shadowing at the iceball’s edge, the distal portion of an iceball becomes invisible at US, akin to a kidney stone. Although cryotherapy in general decreases CT attenuation (30,31), these changes cannot be differentiated from tumors that are often similarly hypodense. However, MRI can be used to distinguish tumors that appear bright when using T2-weighted sequences, from iceballs that appear as signal voids on all conventional MRI sequences (Figure 3). Therefore, MRI and cryotherapy are a good match of a guidance modality and ablative agent. MRI also can be used to monitor RF ablations (15). However, RF devices interfere with MRI; therefore, MRI cannot take place simultaneously with the ablation unless the RF energy is properly filtered to remove high-frequency noise or gated with the MR image acquisition (15). In addition to depicting the iceball, tumor, and surrounding anatomy in multiple planes, effects visualized
during cryotherapy correlate with estimates of tissue necrosis, determined by postprocedural MRI at 1.5 T (10) (Figure 4). To be confident that what is viewed during an ablation procedure translates to posttreatment effects is fundamentally important. A one-to-one correlation between what is viewed during an ablation and what effects are achieved may not be possible with other technologies. For example, during CT-guided RF ablation, if saline were injected at the site of the RF ablation, the burn may extend beyond the intended treatment area because of extension of the saline away from the tumor (32,33). Another important aspect to monitoring is the ability to see effects in multiple planes. Unlike CT, MRI provides imaging in virtually any plane. As a result, the operator may select the plane that best depicts the critical structure at risk. For example, a tumor at the liver dome may abut the diaphragm, lung, or heart. These structures are shown best in the sagittal or coronal planes (Figure 5).
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Figure 6. An ablation can be controlled if both thermal effects and tumor are seen throughout the procedure. (a) An axial view (0.5 T; T2-weighted fast spin echo; TR/TE, 6000/92; section thickness, 8 mm; field of view, 30 cm) shows a hyperintense breast cancer metastasis to the liver with cryoprobes in place (arrows). (b) During MRI-guided cryotherapy, the axial image of the iceball (arrowheads) suggests that the tumor is treated fully. (c) However, in the oblique sagittal plane, untreated tumor (arrow) is seen at its superior margin. (d) This portion of tumor was treated by placing an additional probe (arrow) and freezing the rest of the tumor, confirmed in (e) the final oblique sagittal view. (b– e) Same scan parameters as in (a).
Figure 7. MRI provides excellent visualization of both ablation effects and nearby critical structures. (a) Coronal MRI image (0.5 T; fast gradient echo; TR/TE, 25.9/13.1; flip angle, 90°; section thickness, 8 mm; field of view, 28 cm) shows a peripheral exophytic renal cell carcinoma with a cryoprobe (arrow) in place. (b) During cryotherapy, a repeated scan in the same coronal plane shows the iceball covering the tumor without affecting the adjacent colon (arrow), (c) confirmed in the sagittal plane. (b, c) Same scan parameters as in (a).
CONTROLLING ABLATIVE EFFECTS IN TISSUE Controlling an ablation procedure is the third important intraprocedural role of imaging. To control an ablation, the imaging system must be able to monitor the process as described. However, simply monitoring the
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process does not necessarily mean that the ablation can be controlled. Control of an ablation is derived from the ability to reposition a given probe or modify its effects in some way based on what is viewed during the procedure. Using an open-configuration MRI system, ablation probes may be repositioned in regions of tumor that are not being treated (Figure 6). Using a
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(34) (Figure 8). With a suitable feedback/control mechanism, the computer then could be used to automatically adjust device parameters to control the ablation (34).
ABLATION ASSESSMENT
Figure 8. Computer-assisted visualization of the ablation process in three dimensions can add to the control provided during an image-guided ablation. By registering adjacent critical anatomic structures within a computer program that monitors the entire iceball in real-time, software can warn the user when the two are due to intersect. (a) A critical structure (arrow) has been identified and is shown in green in a 3D view. The tumor is shown as yellow mesh; the developing iceball is shown in blue. (b) The iceball (arrowheads) is shown in cross-section in a 2D image. (c) The calculated growth pattern of the iceball provides (d) a prediction of the treated zone.
closed system, MRI can be used to monitor the ablation, but if a portion of the tumor is not being treated fully, the patient needs to be moved from the MRI system to the CT or US suite to place additional probes (18,19). Control of the ablation process also is achieved by imaging frequently to observe the growth of the ablation volume and alter the applied thermal dose. This can be achieved by repetitive intraprocedural imaging of the volume during application of the treatment. The physician then can review the images and make a determination of the tissue effects, manually adjusting the ablation device parameters accordingly (Figure 7). This also can be achieved by computer-assisted means that perform an ongoing analysis of image data in three dimensions (34). The computer is used to assess coverage, calculate thermal dosimetry, and predict the spatial extent of the thermal effect at a subsequent time point
Imaging has a critical role in the assessment of an ablation procedure. The goal of imaging is to assess how well the tumor was ablated, check for complications, and evaluate for metastases. Experience is accumulating on how imaging is used to assess the completeness of an ablation, and research is ongoing (35– 39). Investigators have largely used CT rather than MRI because of its lower cost and wider availability; however, MRI may be better suited for some patients, such as those with tumors that are shown best with MRI. We typically use MRI to follow up patients undergoing MRI-guided therapies because it allows us to directly compare follow-up imaging findings with intraprocedural images to better understand findings and interpret their results. For example, if a portion of a tumor shows residual enhancement and is suspicious for residual tumor, we can directly correlate these findings with intraprocedural MR images to see whether the portion in question was treated. It then also allows us to use the same MR images to plan subsequent MRI-guided therapies. If CT or US were used, it would be more difficult to translate this information to the MRI frame of reference. Radiologists who interpret images obtained in patients treated with ablation should be cognizant of expected changes in ablation at MRI. The imaging appearance of the ablated tumor is beginning to be investigated (35–38). First, the radiologist should be familiar with what constitutes recurrent tumor. In general, nodular enhancement is considered suspicious for recurrent tumor and should be distinguished from rim enhancement, often seen within the first month after an ablation (38). RF ablation and cryotherapy appear to have common effects and appearances by MRI. They both appear to shorten T1 and T2 relaxation times and eliminate contrast enhancement in the ablation zone. Because detecting nodular enhancement is a critical step in detecting recurrent tumors, careful signal-intensity analysis needs to be performed. Short T1 effects, which typically appear bright on fat-suppressed T1-weighted images, need to be subtracted either visually or quantitatively from contrast-enhanced images.
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SUMMARY
Figure 9. Assessment of tumor ablations is a 3D task. Tissues affected by the ablation are 3D spaces within the body. The figure shows a 3D reconstruction of a lung cancer metastasis (arrow), shown in yellow, in the liver treated with MRI-guided cryotherapy. The tumor volume is covered completely by the outer cryoablation volume (short arrow), shown in blue. The ablation volume also covers an expanded volume (arrowheads) that includes the tumor plus a computer-generated 1-cm ablation margin. (Excerpted from [39] Silverman SG et al. Three-dimensional assessment of MRI-guided percutaneous cryotherapy of liver metastases. AJR Am J Roentgenol 2004; 83:707–712 with kind permission of the publisher.)
Tumor ablation is a 3D problem; therefore, future approaches to ablation assessment (as well as planning) will require 3D imaging (Figure 9). Using volumetric techniques in CT and MRI, 3D images of tumors can be created and coupled with 3D assessments of an ablation (39). From these volumetric data, metrics can be derived such that there is a quantitative assessment of how much tumor was covered, how much normal tissue was sacrificed, and whether an ablation margin (akin to a surgical margin) was achieved. It has been shown that percentage of tumor coverage and percentage of target volume coverage (in which target volume includes both the tumor and a 1-cm ablation margin) correlate with response (39). These measurements could be calculated soon after an ablation and used to predict which tumors might recur so that subsequent treatments can be instituted early. In the future, these 3D metrics could be calculated and shown to the operator intraprocedurally and thus help increase the chances that the ablation is carried out completely and safely.
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In summary, MRI can be used to fulfill all the fundamental roles of imaging when ablating tumors: planning, targeting, monitoring, controlling, and assessment. Intraprocedural monitoring is a particularly important component. The ability of MRI to monitor ablations (particularly using cryotherapy) is unique relative to other guidance modalities. However, as noted, MRI is only one of three cross-sectional imaging modalities that can be used to guide tumor ablations safely and effectively. With additional experience and research, the precise role of MRI will be defined more clearly in the future. Tumor ablation rapidly is becoming the standard of care for the treatment of a variety of tumors and, like radiation therapy today, will become an important component of the treatment of many oncologic conditions in the future. MRI will continue to be an important imaging modality in the care of patients treated with percutaneous tumor ablation. REFERENCES 1. Livraghi T, Solbiati L, Meloni MF, et al. Treatment of focal liver tumors with percutaneous radio-frequency ablation: complications encountered in a multicenter study. Radiology 2003; 226:441– 451. 2. Wood BJ. Percutaneous tumor ablation with radiofrequency. Cancer 2002; 94:433– 451. 3. Dupuy DE, Goldberg SN. Image-guided radiofrequency tumor ablation: challenges and opportunities—part II. J Vasc Interv Radiol 2001; 12:1135– 1148. 4. Goldberg SN, Dupuy DE. Image-guided radiofrequency tumor ablation: challenges and opportunities—part I. J Vasc Interv Radiol 2001; 12:1021– 1032. 5. Jolesz FA, Blumenfeld SM. Interventional use of magnetic resonance imaging. Magn Reson Q 1994; 10:85–96. 6. Mortele KJ, Tuncali K, Cantisani V, et al. MRI-guided abdominal intervention. Abdom Imaging 2003; 28:756 –774. 7. Silverman SG, Tuncali K, vanSonnenberg E, et al. Renal tumors: MR imaging— guided percutaneous cryotherapy initial experience in 23 patients. Radiology 2005;236:716-724. 8. vanSonnenberg E, Shankar S, Morrison PR, et al. Radiofrequency ablation of thoracic lesions: part II. Initial clinical experience—technical and multidisciplinary considerations in 30 patients. AJR Am J Roentgenol 2005; 184:381–390. 9. Shankar S, vanSonnenberg E, Morrison PR, Tuncali K, Silverman SG. Combined radiofrequency and alcohol injection for percutaneous hepatic tumor ablation. AJR Am J Roentgenol 2004; 183:1425–1429. 10. Silverman SG, Tuncali K, Adams DF, et al. MR imaging-guided percutaneous cryotherapy of liver tumors: initial experience. Radiology 2000; 217:657– 664. 11. Goldberg SN, Charboneau JW, Dodd GD III, et al. Image-guided tumor ablation: proposal for standardization of terms and reporting criteria. Radiology 2003; 228:335–345. 12. Tuncali K, vanSonnenberg E, Shankar S, Mortele KJ, Cibas ES, Silverman SG. Evaluation of patients referred for percutaneous ablation of renal tumors: importance of a preprocedural diagnosis. AJR Am J Roentgenol 2004; 183:575–582. 13. Silverman SG, Collick BD, Figueira MR, et al. Interactive MR-guided biopsy in an open-configuration MR imaging system. Radiology 1995; 197:175–181.
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14. Schenck JF, Jolesz FA, Roemer PB, et al. Superconducting open-configuration MR imaging system for image-guided therapy. Radiology 1995; 195:805– 814. 15. Lewin JS, Nour SG, Connell CF, et al. Phase II clinical trial of interactive MR imaging-guided interstitial radiofrequency thermal ablation of primary kidney tumors: initial experience. Radiology 2004; 232:835– 845. 16. Silverman SG, Jolesz FA, Newman RW, et al. Design and implementation of an interventional MR imaging suite. AJR Am J Roentgenol 1997; 168:1465–1471. 17. Jolesz FA, Morrison PR, Koran SJ, et al. Compatible instrumentation for intra-operative MRI: Expanding resources. J Magn Reson Imaging 1998; 8:8 –11. 18. Vogl TJ, Straub R, Eichler K, Sollner O, Mack MG. Colorectal carcinoma metastases in liver: laser-induced interstitial thermotherapy— local tumor control rate and survival data. Radiology 2004; 230:450 – 458. 19. Mack MG, Straub R, Eichler K, Sollner O, Lehnert T, Vogl TJ. Breast cancer metastases in liver: laser-induced interstitial thermotherapy— local tumor control rate and survival data. Radiology 2004; 233:400 – 409. 20. Liu H, Hall WA, Martin AJ, Maxwell RE, Truwit CL. MR-guided and MRmonitored neurosurgical procedures at 1.5 T. J Comput Assist Tomogr 2000; 24:909 –918. 21. Tummala RP, Chu RM, Liu H, Truwit CL, Hall WA. Optimizing brain tumor resection. High-field interventional MR imaging. Neuroimaging Clin North Am 2001; 11:673– 683. 22. Nimsky C, Ganslandt O, Von Keller B, Romstock J, Fahlbusch R. Intraoperative high-field-strength MR imaging: implementation and experience in 200 patients. Radiology 2004; 233:67–78. 23. Kozerke S, Hegde S, Schaeffter T, Lamerichs R, Razavi R, Hill DL. Catheter tracking and visualization using 19F nuclear magnetic resonance. Magn Reson Med 2004; 52:693– 697. 24. Wacker FK, Elgort D, Hillenbrand CM, Duerk JL, Lewin JS. The catheter-driven MRI scanner: a new approach to intravascular catheter tracking and imaging-parameter adjustment for interventional MRI. AJR Am J Roentgenol 2004; 183:391–395. 25. Nevo E. Method and apparatus to estimate location and orientation of objects during magnetic resonance imaging. US Patent 6,516,213, February 4, 2003. 26. Ahmed M, Liu Z, Afzal KS, et al. Radiofrequency ablation: effect of surrounding tissue composition on coagulation necrosis in a canine tumor model. Radiology 2004; 230:761–767.
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27. Montgomery RS, Rahal A, Dodd GD III, Leyendecker JR, Hubbard LG. Radiofrequency ablation of hepatic tumors: variability of lesion size using a single ablation device. AJR Am J Roentgenol 2004; 182:657– 661. 28. Mala T, Aurdal L, Frich L, et al. Liver tumor cryoablation: a commentary on the need of improved procedural monitoring. Technol Cancer Res Treatment 2004; 3:85–91. 29. Nadler RB, Kim SC, Rubenstein JN, Yap RL, Campbell SC, User HM. Laparoscopic renal cryosurgery: the Northwestern experience. J Urol 2003; 170:1121–1125. 30. Sandison GA, Loye MP, Rewcastle JC, et al. X-Ray CT monitoring of iceball growth and thermal distribution during cryosurgery. Phys Med Biol 1998; 43:3309 –3324. 31. Lee FT Jr, Chosy SG, Littrup PJ, Warner TF, Kuhlman JE, Mahvi DM. CT-monitored percutaneous cryoablation in a pig liver model: pilot study. Radiology 1999; 211:687– 692. 32. Kettenbach J, Kostler W, Rucklinger E, et al. Percutaneous saline-enhanced radiofrequency ablation of unresectable hepatic tumors: initial experience in 26 patients. AJR Am J Roentgenol 2003; 180:1537–1545. 33. Giorgio A, Tarantino L, de Stefano G, Coppola C, Ferraioli G. Complications after percutaneous saline-enhanced radiofrequency ablation of liver tumors: 3-year experience with 336 patients at a single center. AJR Am J Roentgenol 2005; 184:207–211. 34. Zientara GP, Saiviroonporn P, Morrison PR, et al. MRI-monitoring of laser ablation using optical flow. J Magn Reson Imaging 1998; 8:1306 – 1318. 35. Cestari A, Guazzoni G, dell’Acqua V, et al. Laparoscopic cryoablation of solid renal masses: intermediate term followup. J Urol 2004; 172: 1267–1270. 36. Matsumoto ED, Watumull L, Johnson DB, et al. The radiographic evolution of radio frequency ablated renal tumors. J Urol 2004; 172:45– 48. 37. Kim SK, Lim HK, Kim YH, et al. Hepatocellular carcinoma treated with radio-frequency ablation: spectrum of imaging findings. Radiographics 2003; 23:107–121. 38. Kim TJ, Moon WK, Cha JH, et al. VX2 carcinoma in rabbits after radiofrequency ablation: comparison of MR contrast agents for help in differentiating benign periablational enhancement from residual tumor. Radiology 2005; 234:423– 430. 39. Silverman SG, Sun MRM, Tuncali K, et al. Three-dimensional assessment of MRI-guided percutaneous cryotherapy of liver metastases. AJR Am J Roentgenol 2004; 83:707–712.
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