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C E N T U R Y
O F
MEDICAL
IMAGING
Keywords: cancer, head and neck imaging, lymph nodes, MR microimaging DOI:10.2214/AJR.04.1832 Received November 30, 2004; accepted after revision February 1, 2005.
1Department
of Radiology and Cancer Biology, Nagasaki University School of Dentistry, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan. Address correspondence to T. Nakamura (taku@net.nagasaki-u.ac.jp).
On CT and MRI, the internal architecture of the node was poorly imaged, and additional evaluation of the parenchymal signals from the node did not significantly improve the diagnostic ability of the size criteria for metastatic nodes [7]. The nodal size alone was also reported to have limited value in the diagnosis of metastatic nodes in the neck [2]. A separate trial using diffusion-weighted MRI was performed for the detection of metastatic nodes to show that the apparent diffusion coefficient (ADC) levels were useful determinants in discriminating metastatic nodes from benign nodes in patients with head and neck cancer [8]. The ADCs also effectively differentiate the nodal lymphomas from metastatic nodes. Lymph node metastases, which are associated with proliferation and necrosis of cancer cells, angiogenesis, and obliteration of hilar fat, cause drastic changes in the components
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Sumi et al. and structures of the nodes. Recently, an application of the small surface coil has been reported to show detailed architecture of the superficial organs [9]. In this study, we sought to determine whether the assessment of the architecture and ADCs of the nodes on highresolution MR microimaging using a microscopy coil might be effective in differentiating metastatic nodes, lymphomas, and benign nodes in the neck. Subjects and Methods Patients
MRI was performed on 26 consecutive patients with palpable lymph nodes in the neck. We obtained institutional review board approval from our hospital and informed consent from the patients. The study cohort included 10 patients (average age, 71 years) with head and neck squamous cell carcinoma, six patients (average age, 58 years) with lymphoma, and 10 patients (average age, 35 years) with benign lymphadenopathy. Consequently, we performed MR microimaging of 24 metastatic nodes, 14 nodal lymphomas, and 35 benign nodes in the neck. All metastatic nodes were surgically removed or biopsied and were histopathologically proven. Of the 10 patients with squamous cell carcinoma, the primary cancers arose in the oropharynx (n = 3), gingiva (n = 3), larynx (n = 3), and tongue (n = 1). The lymphoma nodes were biopsied or excised and histologic types were determined. The histologic types of the lymphomas were four B-cell neoplasms, including one mantle cell lymphoma, two diffuse large B-cell lymphomas, and one follicular lymphoma; one T-cell neoplasm (peripheral unspecified lymphoma); and one Hodgkins lymphoma (nodular lymphocyte predominant). Some of the benign nodes were imaged and biopsied because they were clinically suggestive of malignancy, mainly as a result of their large size; and the remaining benign nodes were clinically evaluated for their responsiveness to treatment with antibiotics after long (6 months) periods of follow-up. lymph nodes were obtained using a turbo spinecho sequence (3,000/90; number of signal acquisitions, 6) and a turbo factor of 11. For all of these sequences, the section thickness was 2 mm. MRI was performed with a matrix of 160 128, a field of view of 7 cm, and an interslice gap of 0.2 mm. The acquisition time for each sequence was less than 4 min. To compensate for the image intensity inhomogeneity inherent to the use of small microscopy coils, we used the CLEAR (constant level appearance) postprocessing technique (Philips Medical Systems). CLEAR uses the premeasured sensitivity profile of the coil to calculate the compensation needed to apply to the pixel intensities to achieve even image intensity. The 26 patients also underwent conventional T1- and fat-suppressed T2-weighted imaging for primary cancer lesions and for deeper nodal lesions. discrimination of metastatic nodes, nodal lymphomas, and benign nodes. The accuracy was calculated by the following formula: (number of nodes positive at both imaging and histology + number of nodes negative at both imaging and histology) / total number of nodes. Positive and negative predictive values were also used to assess the performance of the MRI criteria in the detection of metastatic nodes. The positive and negative predictive values are the percentages of nodes interpreted using the MR microscopic criteria as positive or negative for the particular diagnoses that were positive histopathologically.
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Statistical Analyses
Logistic analysis was performed to identify MRI characteristics that could be used as predictive indicators for differentiating metastatic nodes, lymphomas, and benign nodes in the neck. MR images that were found to be important at univariate analysis were entered into multivariate models to determine their independent predictive value. Analysis was performed with the statistical software package SPSS version 6.1 for Windows (SPSS). Significance in the architectural data and ADC data between the different patient groups was determined using the Fishers exact probability test, Mann-Whitney U test, or Students t test, as indicated in the table footnotes, using commercially available statistical software (StatView 4.51, Abacus Concepts).
Diffusion-Weighted MR Microimaging
Axial diffusion-weighted images of the nodes were obtained using a single-shot, spin-echo type echo-planar imaging sequence (2,973/121; number of signal acquisitions, 6) using the same 47-mm microscopy coil. The sequence was repeated for two values of motion-probing gradients (b = 500 and 1,000 sec/mm2). The section thickness was 2 mm. Diffusion-weighted MRI was performed with a matrix of 80 56, a field of view of 70 mm, and an interslice gap of 0.2 mm. The acquisition time was less than 3 min. The ADCs were determined using the two b factors, by the following formula: ADC = ln (SI1 / SI2) / (b2 b1), where b1 (= 500) and b2 (= 1,000) are gradient factors of sequences S1 and S2, and SI1 and SI2 are signal intensities by sequence S1 and S2, respectively. The two b factors were used to exclude the effects of perfusion in the nodes. The ADC determination was performed in regions of interest (ROIs) placed in the nodes on ADC maps. Each ROI was placed manually in the lymph node on all slices that contained a single node. Each ROI was variable so that it included as much of the nodal parenchyma as possible. The ADC of a node was an average of all values from a single node.
MR Microimaging
MR microimaging was performed using a 1.5T MR imager (Gyroscan Intera 1.5 T Master, Philips Medical Systems) and a 47-mm microscopy coil. The coil was positioned so that the palpable nodes were under the coil and was secured using adhesive tape. Axial T1-weighted images of the cervical lymph nodes were obtained using a conventional spin-echo sequence (TR/TE, 550/10; number of signal acquisitions, 3). Axial, fat-suppressed SPIR (spectral presaturation with inversion recovery) T2-weighted images of the
Results Hilum Structure of the Nodes The hilum structure was depicted as a concavity of the node that was filled with fat tissue (Fig. 1). The vessels may be also evident in the hilum on T1-weighted and fatsuppressed T2-weighted MR microimages (Fig. 1). The hilar fat, which was depicted as a high-intensity area on T1-weighted images and was a low-intensity area on fat-suppressed T2-weighted images, was lost at a high rate in metastatic nodes (92%) but was also lost in nodal lymphomas (79%) and in benign nodes (46%) (Table 1). The difference was significant only between metastatic and benign nodes. Margins of the Nodes We found that T1-weighted imaging was good for the depiction of nodal margins. Nodal margins blending into the surrounding tissue were found in 58% of metastatic nodes (Fig. 2, Table 1). Irregular margins were also found in some lymphomas (23%) but were rarely observed in benign nodes (9%) (Table 1).
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MR Microimaging of Neck Nodes called small-vessel sign [10] on fat-suppressed T2-weighted images (Fig. 5). In two cases of lymphomas (diffuse large B-cell type), unenhanced foci were noted, suggestive of necrosis. Unlike metastatic nodes, however, these foci were hypointense on T2-weighted images. In benign (inflammatory) nodes, we noted hyperintense streaks or hypointense foci (Fig. 6) on fat-suppressed T2-weighted images; the characteristic MRI features were noted in 17% (6/35) of benign nodes. Doppler sonography showed that these foci and streaks in inflammatory nodes were blood vessels (Fig. 6). ADC of the Nodes Next we compared the ADCs of the nodes in three disease groups (Fig. 7). The ADC of metastatic nodes (1.167 0.447 103 mm2/sec) was significantly higher than that of benign nodes (0.652 0.101 103 mm2/sec) and that of lymphomas (0.601 0.427 103 mm2/sec). The ADC of the lymphomas was significantly lower than that of the benign nodes, whereas atypical lymphomas, which were associated with necrosis in the lesions (not shown), exhibited higher ADC levels compared with the remaining typical lymphomas. Diagnostic Ability of MR Microscopic Criteria in Discriminating Nodal Diseases To evaluate the diagnostic significance of the MR microimaging findings, we first performed logistic regression analyses. On univariate analysis, the absence of hilar fat, the irregular margins, the heterogeneous parenchyma on T1- or fat-suppressed T2weighted images, and the ADCs were statistically significant in differentiating metastatic nodes (Table 3). For nodal lymphomas, the nodal size and the ADCs significantly contributed to the diagnosis (Table 4). On multivariate analysis, however, the heterogeneous parenchyma and the ADCs were statistically significant in differentiating metastatic nodes from benign nodes or nodal lymphomas (Table 3). On the other hand, only the ADCs were statistically significant in differentiating lymphomas from the other two entities (Table 4). Finally, we assessed the diagnostic ability of MRI findings using combined criteria of nodal architecture and ADCs. The best results we obtained were as follows: When a node was diagnosed as metastatic if it exhibited heterogeneous parenchyma on T1- or fat-sup-
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Fig. 127-year-old healthy male volunteer with enlarged node at level I. A, Axial T1-weighted (TR/TE, 550/10) MR microimage shows homogeneous parenchyma (arrow) associated with hilum structures containing fat tissue and blood vessels (arrowheads). M = mandible, SMG = submandibular gland. Scale bar indicates 1 cm. B, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows same node as in A, with homogeneously hyperintense nodal parenchyma (arrow) contrasting with hypointense fat tissue and hyperintense blood vessels (arrowheads). Scale bar indicates 1 cm.
TABLE 1: MR Microimaging Findings of Metastatic Nodes, Nodal Lymphomas, and Benign Nodes in the Neck
Finding Metastasis Lymphoma Benign pb Metastasis vs lymphoma Lymphoma vs benign Benign vs metastasis NS NS 0.0003 NS NS < 0.0001 0.0004 NS < 0.0001 NS < 0.0001 0.0076 NS < 0.0001 0.0177 Average Size (mm) No. of No Hilar Irregular Heterogeneous Nodes Fat (%) Margin (%) Parenchymaa (%) Short Axis Long Axis 24 14 35 92 79 46 58 23 9 88 29 23 13.8 16.0 9.7 17.8 20.9 13.8
NoteNS = not significant. a On T1-weighted or fat-suppressed T2-weighted images. b Using Fishers exact probability test for architectures and Students t test for size.
Parenchymal Architecture of the Nodes Metastatic nodes frequently (88%) exhibited heterogeneous architecture of the parenchyma on T1- or fat-suppressed T2-weighted MR microimages, or both (Table 1). MR microimaging showed that metastatic nodes contained hypointense to intermediately intense areas indicative of cancer cell nests and interstitial fibrous tissue with (Figs. 3 and 4) or without (Fig. 4) central hyperintense areas indicative of liquefaction necrosis on fat-suppressed T2-weighted images. These changes
in nodal architecture were depicted well on fat-suppressed T2-weighted images compared with T1-weighted images (Table 2). Heterogeneous architecture of the nodal parenchyma was also evident in some lymphomas (29%) and benign nodes (23%), but the incidence was significantly low compared with metastatic nodes (Table 1). Basically, lymphomas exhibited homogeneous architecture. However, lymphomas may be associated with narrowed hilum and blood vessels, which were depicted as the so-
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Sumi et al. pressed T2-weighted images and an ADC equal to or greater than 0.73 103 mm2/sec, we obtained 83% sensitivity, 94% specificity, 87% positive and 92% negative predictive values, and 90% accuracy. When a node was
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diagnosed as lymphoma if it had an ADC equal to or less than 0.51 103 mm2/sec, we obtained 86% sensitivity, 95% specificity, 80% positive and 97% negative predictive values, and 93% accuracy.
Discussion We have presented our early results on MR microimaging features characteristic of benign and malignant nodes in the neck. We found that the details of the nodal structures
Fig. 276-year-old man with squamous cell carcinoma of mesopharynx. A, Axial T1-weighted (TR/TE, 550/10) MR microimage shows irregular or blending nodal margin of metastatic parotid node (arrows). PG = parotid gland. Scale bar indicates 1 cm. B, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows hypointense parenchyma blending into surrounding tissue (arrows). Scale bar indicates 1 cm. C, Photomicrograph shows extensive proliferation of metastatic cancer cells with destruction of nodal capsule (arrow). Necrotic areas are rarely seen. (H and E, original magnification 1.6)
Fig. 370-year-old man with squamous cell carcinoma in larynx. A, Axial T1-weighted (TR/TE, 550/10) MR microimage shows heterogeneous parenchyma of metastatic node at level IV (arrow). Scale bar indicates 1 cm. B, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows heterogeneous nodal parenchyma associated with large hyperintense area (arrow). Note thin intermediate to hypointense zone demarcating hyperintense area. Scale bar indicates 1 cm. C, Photomicrograph shows large area of necrosis (N). In juxtanecrotic area are proliferating cancer cells (C). (H and E, original magnification 1.6)
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Fig. 462-year-old man with squamous cell carcinoma of mesopharynx. A, Axial T1-weighted (TR/TE, 550/10) MR microimage shows relatively homogeneous metastatic nodes at level II (arrows). SMG = submandibular gland. Scale bar indicates 1 cm. B, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows heterogeneous parenchyma (large arrows) with hypointense focus (small arrows) in two metastatic nodes. Note that proximal node (P) also exhibits small hyperintense areas (arrowhead). Scale bar indicates 1 cm. C, Photomicrograph shows metastatic node (node P in B) with cyst formation (N), which has cancer cell lining. C = cancer cell nests. (H and E, original magnification 1.6) D, Axial T1-weighted (550/10) MR microimage shows homogeneous nodal parenchyma of metastatic node at level II (arrow). SMG = submandibular gland. Scale bar indicates 1 cm. E, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows heterogeneous parenchyma (large arrow) with hypointense area (small arrow). Scale bar indicates 1 cm. F, Photomicrograph shows large area of cancer cell nests (C) and residual lymphoid tissues of node (L). Arrowhead indicates dense fibrous stroma among cancer nests. Note that no apparent liquefaction necrosis is evident. (H and E, original magnification 1.6)
obtained with the microscopy coil were informative in differentiating metastatic nodes, nodal lymphomas, and benign nodes in the neck. We also found that good performance was obtained with criteria based on the presence or absence of hilar fat, heterogeneous
parenchyma on T1- or fat-suppressed T2weighted images, or both, and on the varying ADC cutoff points. Proliferating metastatic cells frequently extend into the nodal hilum, thereby obstructing the hilum. The intact hilum con-
tains fat tissue, blood vessels, and efferent lymphatic vessels, and thus the loss of fat tissue in the hilum has been an important imaging feature highly suggestive of metastatic nodes [1, 2]. However, conventional MRI inconsistently detects this feature. The high-
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NoteNS = not significant. a High- or low-signal-intensity spots or areas in nodal parenchyma. b Using Fishers exact probability test.
Fig. 553-year-old man with non-Hodgkins lymphoma (follicular lymphoma) at level I. A, Axial T1-weighted (TR/TE, 550/10) MR microimage shows homogeneous node (large arrow) lacking hilar fat structure. Hypointense streaks (small-vessel sign) (small arrow) radiating toward periphery of node are evident. Scale bar indicates 1 cm. B, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows homogeneously hyperintense parenchyma (large arrow) and small-vessel sign (small arrow). Scale bar indicates 1 cm. C, Photomicrograph shows proliferating lymphoma cells occupying entire node. (H and E, original magnification 1.6)
resolution images on MR microscopy coils enable efficient assessment of the nodal structures on T1-weighted and fat-suppressed T2-weighted images. It is interesting to assume that when metastatic foci are small, and the intact hilar structures are not yet obliterated, the heterogeneous MR signals from proliferating cancer cells may be more critical than the loss of hilar structures in diagnosing metastatic nodes. Our results support this notion (Table 3).
Loss of the hilar fat was most frequently observed in, but not limited to, the metastatic nodes. Hilar fat was lost in 79% of nodal lymphomas and in 46% of benign nodes. Consequently, loss of hilar fat was a significant finding differentiating metastatic from benign nodes but not from lymphomas (Table 1). Previous studies using sonography showed that hilum structures with or without vascular flow signals were frequently lost or narrowed in lymphomas [11,
12]. Our MRI findings were consistent with these previous studies. The heterogeneity of the internal architecture of the nodes on MR images may be due to the presence of necrosis, cancer nests, and interstitial fibrous tissue, which has been considered to be a pathognomonic feature for metastatic nodes from head and neck squamous cell carcinomas [13]. We found in this study that heterogeneous parenchyma was a significant finding for discriminating meta-
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MR Microimaging of Neck Nodes (Table 2). Considering the reportedly low incidence of central nodal necrosis in metastatic nodes in the neck [14], a combined use of these MR microimaging features (hyperintense focus of central nodal necrosis plus hypointense area) on fat-suppressed T2weighted images may be a better MR criterion than central nodal necrosis alone for the diagnosis of metastatic nodes. We found in this study that heterogeneous parenchyma was not an MRI feature limited to metastatic nodes, but was also observed in nodal lymphomas and even in benign nodes. Our finding that heterogeneous architecture of the nodes occurred in approximately 30% of nodal lymphomas was unexpected. The observed heterogeneity in the nodal architecture may be due to the presence of necrotic areas. Necrosis is well described in Hodgkins disease, but it has been considered to be uncommon in head and neck nonHodgkins disease. King et al. [16] reported that 27% of non-Hodgkins disease in the neck was associated with necrosis. Thus, the notion that the homogeneous MRI architecture is characteristic of nodal lymphomas is open to dispute. ADC measurement may shed light on other aspects of the diseased nodes and may provide additional information distinct from the morphologic features. Among the three nodal diseases, ADCs were highest in metastatic nodes and lowest in lymphomas (Fig. 7). A previous study showed that ADCs were significantly different among metastatic nodes, nodal lymphomas, and benign nodes [8, 17]. In our study, we confirmed that the ADC measurements significantly and independently contributed to the discrimination of metastatic nodes and nodal lymphomas in the neck (Tables 3 and 4). We conclude that a node that has an ADC value equal to or less than 0.51 103 mm2/sec is highly suggestive of lymphoma. The MR microimaging technique has some limitations in the evaluation of head and neck lymph nodes: First, MR microimaging requires additional time for the examination and evaluation of the image data. Second, the small field of view makes it difficult to see the surrounding structures and the exact location of lymph nodes. Third, the technique does not apply to deep nodes. A rapid and sensitive MRI technique, such as a STIR turbo sequence coupled with parallel imaging (SENSE [sensitivity encoding]), would be useful to survey suspicious nodes in the neck before an extensive examination with a microscopy coil.
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C
Fig. 652-year-old woman with lymphadenitis of nodes at level II. A, Axial T1-weighted (TR/TE, 550/10) MR microimage shows homogeneous parenchyma (arrow). PG = parotid gland. Scale bar indicates 1 cm. B, Axial fat-suppressed T2-weighted (3,000/90) MR microimage shows hypointense area (small arrow) in center of parenchyma (large arrow), from which hyperintense striations radiate to periphery. Scale bar indicates 1 cm. C, Power Doppler sonogram shows blood flow signals in hilar region.
static nodes from lymphomas and benign nodes (Table 1). Central nodal necrosis was reported to occur in 32% of metastatic nodes [14]. Enhanced CT may be more effective than unenhanced CT or enhanced MRI in detecting nodal necrosis [6]. However, a recent report showed that no significant difference occurred in sensitivity or specificity for detecting nodal necrosis between enhanced CT and enhanced MRI [15]. In our study, high-resolution imaging using a microscopy coil showed that the hyperintense areas were surrounded by rims or areas
that were hypointense relative to the residual nodal parenchyma. Histologic evaluation confirmed that such hypointense areas corresponded to cancer cell nests, which were composed of proliferating cancer cells and coagulation necrosis, and to surrounding fibrous tissue. On the other hand, central hyperintense areas were caused by liquefaction necrosis. Hypointense foci with or without hyperintense areas on fat-suppressed T2weighted images were noted in 67% of the metastatic nodes and in 14% and 9% of lymphomas and benign nodes, respectively
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Fig. 7Graph of box plots shows apparent diffusion coefficient (ADC) levels of metastatic nodes, nodal lymphomas, and benign nodes. Horizontal line in each box is median (50th percentile) of measured values; top and bottom of boxes represent 25th and 75th percentiles, respectively; and whiskers indicate range from largest to smallest observed data points within 1.5 interquartile range presented by box. Values for p were determined using MannWhitney U test. Circles = outliers.
2.5
p < 0.0001
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1.5
p < 0.0001
1.0
0.5
In the present study we examined relatively larger nodes that were 8 mm or more in the long-axis diameter on axial images. MR microscopy may be useful for the diagnosis of nodes that are relatively large, but size criteria alone are not effective in differentiating metastatic nodes in the neck. However, an answer to the question whether MR microscopy is also useful in the diagnosis of smaller (< 8 mm) nodes, and in the effective detection of micrometastasis, must be revealed by future studies. In conclusion, high-resolution MRI using a microscopy coil can effectively characterize the morphologic details of benign and metastatic nodes in the neck without using gadolinium enhancement. This technique provided better results than previous studies using MRI and CT [7]. In particular, a palpable node in the neck that exhibits heterogeneous parenchyma on T1- or fat-suppressed T2-weighted images, or both, and also has an ADC value equal to or greater than 0.73 103 mm2/sec is suggestive of a metastatic node, whereas a node that has an ADC value equal to or less than 0.51 103 mm2/sec is suggestive of lymphoma. Therefore, the proposed MRI technique may be the primary technique for palpable nodes in the neck.
References
1. Ariji Y, Kimura Y, Hayashi N, et al. Power Doppler sonography of cervical lymph nodes in patients with head and neck cancer. AJNR 1998; 19:303307 2. Chikui T, Yonetsu K, Nakamura T. Multivariate feature analysis of sonographic findings of metastatic cervical lymph nodes: contribution of blood flow features revealed by power Doppler sonography for predicting metastasis. AJNR 2000; 21:561567 3. Yonetsu K, Sumi M, Izumi M, Ohki M, Eida S, Nakamura T. Contribution of Doppler sonography blood flow information to the diagnosis of metastatic cervical nodes in patients with head and neck cancer: assessment in relation to anatomic levels of the neck. AJNR 2001; 22:163169 4. Sumi M, Ohki M, Nakamura T. Comparison of sonography and CT for differentiating benign from malignant cervical lymph nodes in patients with squamous cell carcinoma of the head and neck. AJR 2001; 176:10191024 5. Eida S, Sumi M, Yonetsu K, Kimura Y, Nakamura T. Combination of helical CT and Doppler sonography in the follow-up of patients with clinical N0 stage neck disease and oral cancer. AJNR 2003; 24:312318 6. Yousem DM, Som PM, Hackney DB, Schwaibold F, Henddrix RA. Central nodal ne-
NoteBoldface indicates statistical significance. ADC = apparent diffusion coefficient, CI = confidence interval. a On T1-weighted or fat-suppressed T2-weighted images.
NoteBoldface indicates statistical significance. ADC = apparent diffusion coefficient, CI = confidence interval. a On T1-weighted or fat-suppressed T2-weighted images.
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