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ORIGINAL ARTICLE
Year : 2017  |  Volume : 13  |  Issue : 4  |  Page : 669-675

Magnetic resonance imaging evaluation after radiofrequency ablation for malignant lung tumors


Department of Interventional Radiology, The First Affiliated Hospital of Fujian Medical University, Fuzhou 350005, China

Date of Web Publication13-Sep-2017

Correspondence Address:
Zheng-Yu Lin
Department of Interventional Radiology, The First Affiliated Hospital of Fujian Medical University, 20 Chazhong Road, Fuzhou 350005
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_448_17

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 > Abstract 

Objective: The objective of this study was to investigate magnetic resonance imaging (MRI) assessment of the therapeutic response in small lung malignancies (<3 cm) immediately after radiofrequency ablation (RFA).
Materials and Methods: This is a retrospective analysis of MRI performance in 24 cases of small lung tumors (16 primary, 8 metastatic; 20 patients) immediately, post-RFA, and at follow-up. Variables measured included maximum diameters of tumors on pre-RFA MRI, central areas of low signal intensity (SI) on post-RFA T2-weighted images (T2WIs), and central areas of high SI on post-RFA T1WIs. Additional post-RFA measurements included the maximum diameters for areas of ground-glass opacities (GGOs) on computed tomography (CT), high SI on T2WIs, and isointense SI on T1WIs. Mean values were used for statistical analysis.
Results: Before RFA, 16 primary and seven metastatic lung tumors showed isointense signals on T1WIs and hyperintense signals on T2WIs. Immediately after RFA, the ablated lesions showed central low signals and peripheral high annular signals on T2WIs and central high signals and peripheral annular isointense signals on T1WIs, with reduced SI on diffusion-weighted images. Significant differences were found between the preoperative MRI maximum tumor diameter and post-RFA diameters of central low SI areas on T2WIs and central high SI areas on T1WIs. Furthermore, there were significant differences between the post-RFA maximum diameter of circumferential high signals on T2WIs and the post-RFA maximum diameters of both GGOs on CT and circumferential isointense signals on T1WIs. There were three cases of local recurrence (two pulmonary metastases and one primary) during follow-up.
Conclusions: MRI evaluation of the therapeutic response of RFA for small malignant lung tumors (<3 cm) was precise and reliable.

Keywords: Acute thermal injury, lung cancer, magnetic resonance imaging, radiofrequency ablation


How to cite this article:
Chen J, Lin ZY, Wu ZB, Chen ZW, Chen YP. Magnetic resonance imaging evaluation after radiofrequency ablation for malignant lung tumors. J Can Res Ther 2017;13:669-75

How to cite this URL:
Chen J, Lin ZY, Wu ZB, Chen ZW, Chen YP. Magnetic resonance imaging evaluation after radiofrequency ablation for malignant lung tumors. J Can Res Ther [serial online] 2017 [cited 2018 Nov 16];13:669-75. Available from: http://www.cancerjournal.net/text.asp?2017/13/4/669/214474


 > Introduction Top


Recent research results have shown that treatment of malignant lung tumors with radiofrequency ablation (RFA) can prolong the survival time of patients, and the treatment outcomes for small lung cancers (<3 cm) are close to those from surgery.[1] The results of efficacy evaluation after RFA are directly related to prognosis. Although, at present, computed tomography (CT) is the primary modality used worldwide to assess the effects of lung RFA,[2] magnetic resonance imaging (MRI) reveals certain characteristic changes seen in lesions after ablation. The aim of this study was to explore MRI findings from acute thermal injury caused by RFA in small lung cancers (<3 cm) and to evaluate the clinical utility of MRI in this clinical setting.


 > Materials and Methods Top


Patients

Twenty patients (13 males, 7 females) who had pathologically confirmed pulmonary malignancies were included in this study between September 2013 and August 2015, and CT-guided RFA was performed. The average age was 64 years (range = 50–77 years). All patients signed informed consent before undergoing RFA.

Methods

Preprocedural magnetic resonance imaging scan

Preprocedural pulmonary 1.5-T MRI scanning (MAGNETOM Espree, Siemens, Germany) with a body coil was performed with specific scan sequences and parameters: (1) Fat-suppressed (fs) fast reverses fast spin-echo (turbo spin echo [TSE] fs) T2-weighted images (T2WIs) with repetition time (TR) 4000.0 ms, echo time (TE) 80.0 ms, flip angle 90°, slice thickness (ST) 3.0 mm, interval (gap) 0.6 mm, field of view (FOV) 32 cm × 18 cm, number of excitation (NEX) 2, and scan time 130–150 s; (2) fs volumetric interpolated T1WIs (fs-T1 Vibe) with TR 5.1 ms, TE 2.4 ms, NEX 1, ST 3.0 mm, FOV 39 cm × 24 cm, and scan time 12–14 s; and (3) diffusion-weighted imaging (DWI) with NEX 2, ST 3.0 mm, gap 0.6 mm, and b-value 50/800. A diaphragm trigger scan was used for TSE fs T2WIs and DWI sequences, and a breath-hold scan was used for the fs-T1 Vibe sequence.

Computed tomography-guided radiofrequency ablation

First, a CT localization scan (SOMATOM Emotion, Siemens, Germany) was performed to select the appropriate puncture point. A 17-gauge, 150 mm, internally cooled radiofrequency electrode (Star RF Electrode-Fixed, STARmed, Korea) was gradually inserted under CT guidance into the target tumor and the cold cycle; automatic pulse mode setting with an output power of 60–100 W was used for 3–12 min of continuous treatment. The position of the ablation electrode was adjusted as needed (one to two times for each tumor). Following the procedure but with the needle still in place, complete ablation was confirmed by a CT finding of 0.5–1.0 cm or greater ground-glass opacity (GGO) surrounding the lesion. After removal of the electrode, CT imaging was repeated to evaluate for pneumothorax, bleeding, pleural effusion, or other possible complications.

Postprocedural magnetic resonance imaging scan

MRI studies were performed within 20 min post-RFA using the same parameters and sequences as before the procedure.

Measurement methods

The pre-RFA maximum tumor diameters on MRI, the post-RFA central low signal intensity (SI) areas on T2WIs, and the post-RFA central high SI areas on T1WIs were measured. In addition, the post-RFA maximum diameters of the circumferential GGOs on CT, high SI areas on MRI T2WI, and isointense SI areas on T1WIs were obtained. All variables were expressed as mean ± standard deviation, and means were used for calculations. The t-test of SPSS version 19.0 (IBM Corp., Armonk, NY, USA) software package was employed for statistical analysis, and P < 0.05 was considered statistically significant.

Follow-up and therapeutic evaluation

Follow-up

Lung CT with contrast enhancement was repeated 1 month after RFA treatment, and then every 3 months.

Therapeutic evaluation

According to the guidelines established by an expert panel convened by the Chinese Anti-Cancer Association in 2014,[3] enhanced CT 1 month after treatment was used for therapeutic evaluation. The classification criteria for complete ablation included any one of the following findings on enhanced CT: (1) An absence of lesions; (2) a fully formed cavity; (3) fibrotic (or scarred) lesion; (4) a solid nodule unchanged or reduced in size without contrast enhancement; or (5) pulmonary atelectasis without contrast enhancement. Incomplete ablation was identified if CT shows (1) incomplete cavity formation with some solid or liquid parts showing contrast enhancement; (2) fibrosis of some of the lesions but solid components with contrast enhancement remained; or (3) a solid nodule unchanged or increased in size accompanied by contrast enhancement.


 > Results Top


Lung tumors

There were 13 patients who had primary lung cancer [Figure 1]a (12 with adenocarcinoma and 1 with squamous cell carcinoma), with a total of 16 tumor foci. There were seven patients with pulmonary metastatic cancer [Figure 2]a – each occurred after surgical resection of the primary tumor (three with liver cancer; two, rectal carcinoma; one, gastric carcinoma; and one, breast carcinoma) – with a total of eight tumor foci. All the lung tumors were <3.0 cm in diameter, with an average maximum tumor diameter of 1.72 cm ± 0.53 (range = 0.80–2.57 cm).
Figure 1: (a) A male, 64-year-old, with adenocarcinoma of the right upper lung. Computed tomography scan showing a right upper lung nodule before radiofrequency ablation. (b) The puncture process was successful without apparent bleeding. (c) A ground-glass opacity was seen around the lesion after radiofrequency ablation. (d) Preoperative magnetic resonance imaging showing iso-signals on T1-weighted images. (e) Preoperative magnetic resonance imaging showing long nodular signals on T2-weighted images. (f) There was a high signal on diffusion-weighted imaging. (g) After radiofrequency ablation, magnetic resonance imaging showing short signals on T1- and T2-weighted images centrally, with surrounding patches of iso-signals on T1-weighted images. (h) After radiofrequency ablation, magnetic resonance imaging showing short signals on T1- and T2-weighted images centrally, with surrounding long signal intensity on T2-weighted images. (i) Whereas, the high signal intensity on diffusion-weighted imaging was absent

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Figure 2: (a) A male, 51-year-old, with pulmonary metastasis after surgery for rectal cancer. Computed tomography scan showing a left lung metastasis before radiofrequency ablation. (b) A splinter hemorrhage occurred around the lesion during the needle insertion. (c) A patch of high-intensity shadow was seen on computed tomography around the lesion after radiofrequency ablation that was indistinguishable in appearance from postradiofrequency ablation ground-glass opacity. (d) Preoperative magnetic resonance imaging showing iso-signals on T1-weighted images. (e) Preoperative magnetic resonance imaging showing a long signal with nodules on T2-weighted images. (f) Preoperative magnetic resonance imaging showing a high signal intensity on diffusion-weighted imaging. (g) After radiofrequency ablation, magnetic resonance imaging showing short signals on T1- and T2-weighted images centrally, with patches of iso-signals on T1-weighted images and long signals on T2-weighted images in the surrounding areas. Puncture hemorrhage showed iso-signals on T1-weighted images and long signals on T2-weighted images. The peritumoral vascular exudative shadow was more narrow, with a possible local iso-signal on T1-weighted images. (h) The peritumoral vascular exudative shadow was more narrow, with a longer residual nodular signal on T2-weighted images. (i) The peritumoral vascular exudative shadow was more narrow, with a small residual nodular high signal on diffusion-weighted imaging. (j) Follow-up imaging 10 months after radiofrequency ablation showing an increase in the previously ablated lesions in the upper lobe of the left lung. (k) Follow-up imaging 10 months after radiofrequency ablation showing an increase in the previously ablated lesions in the upper lobe of the left lung. (l) Inhomogeneous enhancement on an enhanced scan

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Preprocedural magnetic resonance imaging findings

Compared with chest wall muscle, one pulmonary metastasis showed isointense signal on pre-RFA T2WIs, and all the remaining tumors (16 primary, 7 metastases) showed slightly high signals [Figure 1]d and [Figure 2]d or isointense signals [Figure 1]e and [Figure 2]e on T1WIs. Furthermore, 13 primary lung tumors [Figure 1]f and all the eight metastatic tumors had high signals on DWI studies [Figure 2]f and low signals on the corresponding apparent diffusion coefficient (ADC) maps. The SI of the remaining three primary lung tumors was not able to be determined due to their small size.

Computed tomography and magnetic resonance imaging findings in the immediate postradiofrequency ablation period

Acute hemorrhage occurred in five cases (three primary and two metastatic) during RFA needle insertion [Figure 2]b. Immediate postablation CT scans showed patches of high-intensity shadow around the lesions [Figure 2]c, which were indistinguishable from post-RFA GGOs. Due to this, the immediate postprocedural CT scan was not accurate in assessing the efficacy of ablation. Immediate post-RFA MRI studies for these five cases showed central low signals on T2WIs [Figure 2]g and central high signals on T1WIs [Figure 2]h, and the acute hemorrhage was apparent as patches of isointense signals on T1WIs and high signals on T2WIs in and around the needle tracts (similar in appearance to a surrounding exudation shadow after RFA). Post-RFA DWI signals of the three primary tumors and one of the metastatic lesions were significantly reduced. The other metastatic lesions also had reduced signals on DWI; however, there was a small nodular hyperintensity seen on the side of blood vessels adjacent to the tumor [Figure 2]i.

For the remaining 19 tumors (13 primary and 6 metastatic), immediate postablation CT scans showed slightly higher density GGOs around the tumor foci, with blurred edges in 18 tumors [Figure 1]c. One patient with lung cancer had shortness of breath from pneumothorax that developed during the puncture process so that the patient could not tolerate the procedure fully. The ablation time for the lesion was shorter, and the GGO around the lesion was light.

Furthermore, for the 19 tumor foci without apparent hemorrhage [Figure 1]b, immediate post-RFA MRI showed central low signals and ring-like high signals around the lesions on T2WIs [Figure 1]g, and central high signals with ring-like isointense signals around the lesions on T1WIs [Figure 1]h. The postprocedural MRI scan of the patient with shortness of breath caused by pneumothorax, however, showed that the tumor focus was not completely surrounded by an isointense SI on T1WIs or a high SI on T2WIs.

The SIs on postablation DWIs were lower for 18 tumor foci [Figure 1]i; whereas, one tumor focus showed an unevenly decreased SI with a small nodular hyperintensity along the edge. Furthermore, the postprocedural MRI of three tumor foci showed a high stripe-like SI on T1WIs and centrally located hyperintense needle-like shadows on T2WIs.

Measurement results

Given values were expressed as mean ± standard deviation, and the means were used for statistical analysis. Values for the maximum tumor diameter on preablation MRI, the central low SI on postablation T2WIs, and the central high SI on postablation T1WIs for the 24 tumor foci were 1.81 cm ± 0.52, 2.25 cm ± 0.49, and 2.26 cm ± 0.43, respectively [Figure 3]. There were statistically significant differences between the maximum tumor diameter on pre-RFA MRI and both the central low SIs on T2WIs (t = 3.972, P < 0.002) and the central high SIs on T1WIs (t = 3.757, P < 0.002) of post-RFA MRI studies. There was no significant difference between the maximum diameters for the central low SIs on T2WIs and the central high SIs on T1WIs on post-RFA studies (t = 0.342, P > 0.05).
Figure 3: Comparison with the maximum diameter of magnetic resonance imaging tumor lesions before ablation, the central low signal intensity on T2-weighted image after ablation, and the central high signal intensity on T1-weighted image after ablation (cm): *P < 0.05; **P < 0.001

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Measurements from postablation studies for areas of GGO on CT, high SIs on T2WIs, and isointense SIs on T1W1s around the 19 tumor foci without hemorrhage were 3.50 cm ± 0.61, 4.02 cm ± 0.87, and 3.68 cm ± 0.79, respectively [Figure 4]. Statistically significant differences were found between the postablation maximum diameters of GGOs on CT and high SI areas on T2WIs (t = 4.29, P < 0.001), as well as between the postablation maximum diameters of high SI on T2WIs and isointense SI on T1W1s (t = 2.534, P < 0.05). However, there was no significant difference between the post-RFA maximum diameters of GGOs on CT and isointense SI on T1W1s (t = 1.891, P > 0.05).
Figure 4: Comparison with the maximum diameter of the ground-glass opacity around tumor lesions on computed tomography after ablation, the surrounding high signal intensity on T2-weighted image, and the surrounding equisignal intensity on T1-weighted image (cm): *P < 0.05; **P < 0.001

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Follow-up results

The mean follow-up period for all patients was 17.4 ± 4.7 months (range = 10–31 months). At the end of follow-up, 19 of 20 patients survived. One patient with hepatic cancer who had received RFA for a pulmonary metastasis died due to multiple new systemic metastases. There were 21 of the 24 tumor foci with complete ablation and three with incomplete ablation, for a complete ablation rate of 87.5%. Two patients who had RFA for lung metastases and one for primary lung cancer experienced local recurrence [Figure 2]j and [Figure 2]k, showing the increased sizes compared with the previous lesions and the nodular abnormal enhancement in the surrounding areas by postoperative chest CT scan with enhancement [Figure 2]l. The performance of post-RFA CT and MRI studies in the three cases with local recurrence was analyzed retrospectively. The recurrent lesions in two of the patients were located near large blood vessels. Furthermore, on the immediate post-RFA CT and MRI scans, the surrounding areas of GGO and exudative reaction zones in the region of the vessels were relatively thin (<0.5 cm). In one of the cases, the immediate post-RFA MRI showed isointense SI on T1WI and high SI on T2WI with the appearance of small nodules remaining next to large blood vessels, and there was a slightly high SI on DWI.


 > Discussion Top


Currently, RFA is widely used to treat malignant lung tumors that are inoperable or in patients who decline surgery. Nevertheless, its curative effect is lower than that seen with RFA of liver tumors because there is more gas in lung tissue and poor thermal conductivity. There has also been only a single method of postablation assessment employed despite the importance of accurate therapeutic response evaluations. CT is the primary means used to assess the results from lung tumor RFA worldwide, and successful ablation is defined by the presence of GGO covering the area of the lesion and a lack of contrast enhancement in the ablated region.[2],[4] However, it is very easy to confuse GGO after RFA with hemorrhage, which may be caused by mechanical damage to the lung tissue during the puncture process. Furthermore, change in lesion density is not obvious on CT, and immediate post-RFA-enhanced CT does not reveal potential residual foci near blood vessels. These factors decrease the reliability of CT assessment immediately following lung RFA.[5] Although in the recent years positron emission tomography-CT has been used as a means of postablation follow-up, there has been no significant progress in the intraprocedural therapeutic evaluation.[6] Therefore, postprocedural imaging evaluation remains essential to ensure the success of RFA and prolong the survival time of patients.

MRI is sensitive to temperature change, and characteristic features associated with changes in the water content of ablated lesions are seen on MRI.[7],[8],[9],[10] Miao et al.[11] used RFA to treat the rabbit VX2 lung cancer model and identified the formation of five typical isocenter areas around the radiofrequency electrode after treatment: (1) The electrode tract area, (2) the tumor coagulation necrosis area, (3) the lung parenchyma coagulation area, (4) the peripheral bleeding area, and (5) the inflammatory reaction area. Oyama et al.[12] performed a comparative study of MRI and pathologic outcomes in normal pig lung after RFA. They found that the normal pig lung showed an inner zone of isointense SI on T1WIs, low SI on T2WIs, and a circumferential outer zone of high SI on T2WIs after RFA. A comparative analysis suggested that, on T2WIs, the inner zone represented an area of coagulation necrosis and the outer zone represented a region of neutrophil infiltration, alveolar fluid, and pulmonary congestion due to thermal injury of the lung tissue.

Postprocedural MRI studies in the present study revealed that low SIs on T1- and T2-WIs were consistent with coagulation necrosis, and the surrounding isointense SIs on T1WIs and high SIs on T2WIs were suggestive of peripheral bleeding and inflammation. In addition, the maximum diameters of the central low signals on T2WIs and the central high signals on T1WIs after ablation were greater than the maximum tumor diameters on MRI before ablation. This was believed to represent coagulation necrosis of the tumor as well as that of the surrounding pulmonary parenchyma. These findings suggest that, compared with CT, MRI could provide a more accurate evaluation of the effect of RFA. Furthermore, the maximum diameter of the high SIs on T2WIs after ablation was greater than that of the GGOs on CT and the surrounding isointense SIs on T1WIs. This is thought to be due to the higher soft-tissue resolution and sensitivity for alveolar exudative changes of MRI compared with CT, with T2WI being more accurate than T1WI for these changes.

In this study, slight hemorrhage occurred during the puncture process of RFA in five cases. The appearance of this type of hemorrhage on the immediate post-RFA CT was indistinguishable from GGO typically seen around tumor foci. This finding suggests that CT assessment is not sufficiently accurate at this stage. In contrast, the characteristics of acute hemorrhage on immediate postablation MRI studies (iso-intense T1 and high T2 signals) were readily differentiated from those of central coagulation necrosis (both low signals seen in the center of ablated lesions on T1- and T2-WIs). As such, pulmonary hemorrhage caused by puncture injury had little influence on the utility of MRI for the immediate therapeutic evaluation of RFA.

In this study, one patient with pulmonary hemorrhage due to puncture injury during RFA had isointense T1 and high T2 signals suggestive of residual tumor near blood vessels on MRI as well as a slightly high SI on DWI. This patient had a local recurrence at follow-up.

Okuma et al.[13] reported a central low signal on T2WI with a patch of high T2 SI in the periphery, and a central isointense SI on T1WI after RFA for malignant lung tumor. In contrast, all lesions in this study showed a high SI in the area of central coagulation necrosis on T1WI. The finding of a high signal may be related to tissue coagulation, dehydration, and hemorrhage. Further studies are needed to clarify the actual cause(s).

Okuma et al.[13] suggested that a more accurate assessment of RFA efficacy could be made when MRI showed reduced signal on DWI and increased ADC values for lung tumor foci within 3 days of treatment. They also proposed that evaluation may be performed earlier than allowed by measuring volume changes on CT. Youn et al.[14] thought that small lung tumors were difficult to display on DWI due to the limit of MRI resolution. Consistent with this supposition, there were three smaller primary lung lesions in this study that showed a GGO shadow but were difficult to evaluate on DWI. The remaining 21 lesions were adequately displayed on DWI. Results showed hyperintensities on DWI and hypointensities on the ADC map before RFA, and reduced signals on DWI and increased signals on the ADC map after ablation.

Due to the heat sink effect, complete ablation of tumors near larger blood vessels was found to be more difficult.[15],[16] A retrospective analysis showed that two cases of recurrent lung metastases were located next to the pulmonary artery, and the immediate post-RFA CT scan showed a small or obscure GGO next to the vessel. MRI revealed that the recurrent lesions were located next to vessels, showing iso-T1 and longer T2 signals and slightly higher SI on DWI. These findings suggested that the recurrent cases were associated with the heat sink effect.

The shortcomings of this study were the relatively small study sample and short follow-up time, and the fact that we did not use the dynamic enhancement scan to further study MRI characteristics of ablation lesions. We expect to address these issues in the future studies.


 > Conclusions Top


MRI has certain characteristics which make it accurate and reliable for therapeutic efficacy assessment after RFA for pulmonary malignancy. We suggest its use for clinical evaluation immediately after RFA of lung tumors and believe that it will help increase the rate of complete tumor ablation.

Financial support and sponsorship

This study was supported by grants from the Medical Elite Cultivation Program of Fujian, PRC (2013-ZQN-ZD-20), and the set sail of Fujian Medical University fund projects, PRC (2016QH058).

Conflicts of interest

There are no conflicts of interest.

 
 > References Top

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Lin ZY, Chen J, Deng XF. Treatment of hepatocellular carcinoma adjacent to large blood vessels using 1.5T MRI-guided percutaneous radiofrequency ablation combined with iodine-125 radioactive seed implantation. Eur J Radiol 2012;81:3079-83.  Back to cited text no. 7
    
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Lin Z, Zhang T, Hu J, Deng X. Preliminary study on 1.5T MRI-guided radiofrequency ablation therapy technology for malignant liver tumors. Chin J Radiol 2010;44:1304-7.  Back to cited text no. 8
    
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Lazebnik RS, Breen MS, Fitzmaurice M, Nour SG, Lewin JS, Wilson DL, et al. Radio-frequency-induced thermal lesions: Subacute magnetic resonance appearance and histological correlation. J Magn Reson Imaging 2003;18:487-95.  Back to cited text no. 9
    
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Miao Y, Ni Y, Bosmans H, Yu J, Vaninbroukx J, Dymarkowski S, et al. Radiofrequency ablation for eradication of pulmonary tumor in rabbits. J Surg Res 2001;99:265-71.  Back to cited text no. 11
    
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Oyama Y, Nakamura K, Matsuoka T, Toyoshima M, Yamamoto A, Okuma T, et al. Radiofrequency ablated lesion in the normal porcine lung: Long-term follow-up with MRI and pathology. Cardiovasc Intervent Radiol 2005;28:346-53.  Back to cited text no. 12
    
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Okuma T, Matsuoka T, Yamamoto A, Hamamoto S, Nakamura K, Inoue Y, et al. Assessment of early treatment response after CT-guided radiofrequency ablation of unresectable lung tumours by diffusion-weighted MRI: A pilot study. Br J Radiol 2009;82:989-94.  Back to cited text no. 13
    
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Youn BJ, Chung JW, Son KR, Kim HC, Jae HJ, Lee JM, et al. Diffusion-weighted MR: Therapeutic evaluation after chemoembolization of VX-2 carcinoma implanted in rabbit liver. Acad Radiol 2008;15:593-600.  Back to cited text no. 14
    
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