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Original Research |
1 Division of Neuroradiology, Oregon Health & Science University, 3181 SW
Sam Jackson Park Rd,, Mail Code CR 135, Portland, OR 97239.
2 Division of Neurology, Oregon Health & Science University, Portland,
OR.
Received March 3, 2008;
accepted after revision April 13, 2008.
Address correspondence to B. E. Hamilton
(hamiltob{at}ohsu.edu).
Abstract
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MATERIALS AND METHODS. Retrospective review was performed on 50 sets of MR images of 25 patients who underwent both 3-T and 1.5-T brain imaging with a dedicated epilepsy protocol, including fast spin-echo T2-weighted, coronal FLAIR, coronal fast multiplanar inversion recovery, and 3D spoiled gradient-recalled echo pulse sequences. Parameters assessed were distortion and artifact, lesion conspicuity, gray–white matter differentiation, and motion. Each pulse sequence was graded on a 4-point scale. Reviewers performed qualitative assessments of the site of abnormality and the most likely diagnosis.
RESULTS. MRI at 3 T outperformed MRI at 1.5 T in all four parameters and was statistically superior (p < 0.05) to 1.5-T MRI in all categories except motion. On 3-T MRI, lesions were detected in 65 of 74 cases compared with 55 of 74 cases at 1.5 T (p = 0.0364), and lesions were accurately characterized in 63 of 74 cases compared with 51 of 74 cases at 1.5 T (p = 0.0194). The odds ratios showed identification of a focal epileptogenic lesion with 3-T MRI 2.57 times as likely as identification with 1.5-T MRI and accurate characterization of lesions 2.66 times as likely as characterization with 1.5-T MRI.
CONCLUSION. In evaluation of epilepsy, MRI at 3 T performed better than 1.5-T MRI in image quality, detection of structural lesions, and characterization of lesions. High-field-strength imaging should be considered for patients with intractable epilepsy and normal or equivocal findings on 1.5-T MRI.
Keywords: 3-T MRI • focal epilepsy • medically refractory epilepsy • MRI
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The current barrier to surgery for many patients with medically refractory partial complex epilepsy is lack of identification of an abnormality on images. MRI is key to surgical success because it enables accurate anatomic identification of the epileptogenic focus, which is critical for preoperative planning and localization [6, 7]. Assessment is ideally performed at dedicated epilepsy centers with close collaboration among neurologists, neurosurgeons, and radiolo gists. Safe surgery requires careful analysis of structural brain lesions with alignment of the clinical and imaging evidence. MRI plays a key role in diagnosis and localiza tion. Many patients presenting to our epi lepsy center have localized syndromes that raise clinical suspicion of the presence of a focal structural abnormality, yet in many instances, a lesion has not been localized at previous imaging evaluation. High-field-strength MRI has potential for improving epilepsy evaluation because of the greater signal-to-noise ratio of 3-T MRI compared with 1.5-T MRI.
The goal of our study was to assess the diagnostic value of 3-T compared with 1.5-T whole-brain MRI in the evaluation of epilepsy. We selected for review all patients who underwent both 3-T and 1.5-T whole-brain MRI for epilepsy regardless of the reason for repeated imaging. We evaluated the pro portions of correct detection of structural lesions, observer-assessed lesion conspicuity, normal gray–white matter tissue contrast, and imaging artifacts in a group of epilepsy patients who had undergone consecutive 1.5- and 3-T MRI examinations at our institution.
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The reference standard for lesion localization in the 19 patients with partial complex epilepsy was surgical confirmation in 12 cases and electroencephalographic or PET localization in conjunction with clear clinical signs in seven cases. The other six patients did not have a focal epilepsy syndrome, and their cases were used only for the qualitative assessment portion of the analysis.
MRI
Both 1.5-T and 3-T MR images of the 25 patients were reviewed independently
by four experienced neuroradiologists. The images were assessed digitally with
a commercially available PACS workstation (Impax version 4.5, Agfa) with
real-time multiplanar reformation capabilities available to all reviewers. The
multiplanar reformation function operates with a localization marker on both
the source and the reformatted images. This feature was particularly helpful
in assessment of the 3D T1-weighted spoiled gradient-recalled echo (SPGR)
images with nearly isovoxel resolution. With this tool, the radiologist was
able to assess areas suggestive of cortical thickening in directly orthogonal
or perpendicular planes to rule out artifacts related to in-plane cortex.
Reviewers were blinded to clinical results, including data on seizure signs,
electro encephalographic findings, and other forms of localization.
A six-channel sensitivity-encoding head coil was used on both clinical 3-T units (Achieva, Philips Healthcare) for all whole-brain epilepsy imaging. Our 1.5-T MRI units (Signa Horizon and Signa LX, GE Healthcare) had a transmit–receive single-channel head coil for whole-brain imaging. Parallel-processing head coils were impractical on our two 1.5-T units for several reasons but primarily owing to degradation in image quality from inadequate signal-to-noise ratio. Identical imaging parameters therefore were not possible. Directly comparable sequences (those of the same sequence type, plane, and approximate slice thickness) used for our epilepsy protocol on the 3-T and 1.5-T MRI units were reviewed. At the time of this study, our whole-brain epilepsy protocol on all units included the following sequence parameters.
The 1.5-T protocol consisted of one 3D and three 2D sequences. The 3D images were obtained with a coronal T1-weighted SPGR sequence (TR/TE, 24/9.2; acquisition matrix, 256 x 256; field of view, 230 mm2; flip angle, 25°; slice thickness, 1.5 mm with no space). The first 2D acquisition was an axial fast spin-echo T2-weighted sequence (5,000/96.1; acquisition matrix, 256 x 256; field of view, 230 mm2; flip angle, 90°; slice thickness, 4.0–5.0 mm with 1.0-mm space). Two-dimensional fast multiplanar inversion recovery (4,500/14; inversion time, 300 seconds; acquisition matrix, 256 x 256; field of view, 180–220 mm; slice thickness, 3.0 mm with no space) and coronal FLAIR (8,802/133; inversion time, 2,200 milliseconds; acquisition matrix, 256 x 256; field of view, 220–240 mm; slice thickness, 5.0 mm with 1.0-mm space) sequences also were performed.
The 3-T protocol also consisted of one 3D and three 2D sequences. The 3D images were obtained with a coronal T1-weighted SPGR sequence (30/6; acquisition matrix, 256 x 256; field of view, 230 mm; flip angle, 45°; slice thickness, 1.2 mm with no space). The first 2D acquisition was an axial turbo spin-echo T2-weighted sequence (3,000/90; acqui sition matrix, 256 x 256; field of view, 230 mm; flip angle, 90°; slice thickness, 4.0–5.0 mm with 1.0-mm space). Two-dimensional fast multiplanar inversion recovery (3,975/20; inversion time, 250 seconds; acquisition matrix, 256 x 256; field of view, 180–220 mm; slice thickness, 2.0 mm thick with 0.2-mm space) and coronal FLAIR (11,004/120; inversion time, 2,800 milliseconds; acquisi tion matrix, 256 x 256; field of view, 220–240 mm; slice thickness, 4.0 mm with 1.0-mm space) sequences also were performed.
Image Review
Four neuroradiologists experienced in interpreting epilepsy studies were
asked to independently review the images from the 1.5- and 3-T studies. The
viewing order was random, and to allow them the opportunity for direct
comparison, reviewers were not blinded in regard to viewing both studies at
the same time. Reviewers were asked to rate the 1.5- and 3-T image sets
separately for the four following features: lesion conspicuity, defined as the
ease with which the suspected epileptogenic focus was visible, with a specific
diagnosis when possible; normal tissue contrast between gray and white matter;
technical artifacts resulting in image degradation; and artifacts related to
patient motion. All reviewers were blinded to clinical findings, final
diagnosis, and other reviewers' interpretations. All features were rated on a
4-point scale (1, worst; 4, best) for lesion conspicuity and tissue contrast
(1, worst artifacts; 4, clinically insignificant or no artifacts) for image
degradation due to technical factors for both overall imaging artifacts, such
as phase and susceptibility artifacts, and motion.
Statistical Evaluation
Analysis of variance was used to assess differences in the reported scores
of lesion characterization, tissue contrast, and technical and motion
artifacts. Differences in reported identification also were compared because
in some cases, anatomic abnormalities were visible only at 3 T. Individual
scores were used as the response variable, and p = 0.05 was
considered significant. Logistic regression was used to determine the
diagnostic accuracy of 3-T com pared with 1.5-T MRI through the use of two
models fitted for lesion characterization, tissue contrast, and technical and
motion artifacts as responses. A value of p < 0.05 was considered
significant. Intraclass correlation is a measure of interrater reliability for
two or more reviewers, and the significance of this value can be interpreted
in a manner similar to that for kappa statistics. The 95% CI for intraclass
correlation was used to assess the reliability of the four independent
reviewers' scores.
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Correct lesion identification (separate from the quality analysis) was higher at 3 T than at 1.5 T with correct identification of the structural lesion in 65 of 74 (88%) compared with 55 of 74 (74%) individual interpretations (Table 2). Two of the 76 interpretations in the cases of the 19 focal epilepsy patients were excluded because of missing data. Lesion characterization at 3 T and 1.5 T was compared only for the 19 of 26 patients with focal epilepsy (Table 3). Lesion characterization (p = 0.0095) and tissue contrast (p = 0.0292) were consistently rated higher at 3 T than at 1.5 T. Odds ratios for correct lesion identification and characterization at 3 T and 1.5 T were 2.57 and 2.66, respectively (Table 4). An interesting finding was that imaging artifacts were less troublesome at 3 T than at 1.5 T (p = 0.01). Although a trend toward greater motion artifacts was seen at 3 T, this difference was not statistically significant (p = 0.136). Intraclass correlation yielded moderate reliability among the four reviewers as a group (0.562) with a 95% CI of 0.466–0.643.
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Clinical Outcome
Twelve of the 19 patients with focal epilepsy underwent surgical resection
of the epileptogenic focus. Seven of the 12 surgically treated patients had
complete resolution of seizures, three had clinically moderate improvement,
and two had no significant improvement in seizure frequency or severity during
the early clinical follow-up period (mean, 571 days).
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The results of our study support the clinical supposition that use of 3-T MRI increases the rates of lesion detection and accurate characterization of lesions. MRI at 3 T also yields better contrast resolution of the gray–white matter junction, a finding particularly relevant for detection of subtle focal dysplasia of the cortex. Data from our odds ratio comparison imply that a 3-T MRI examination is 2.57 as likely as a 1.5-T examination to depict a structural abnormality and that correct characterization of the abnormality is 2.66 times as likely on 3-T studies as it is on 1.5-T studies, presumably contributing to a more accurate diagnosis. MRI at 3-T with its intrinsically greater signal-to-noise ratio combined with advances in parallel processing has considerable diagnostic value. The ability to produce high-resolution thin-slice whole-brain images in a practical examination time (< 1 hour) is a strong advantage on 3-T MRI because it facilitates detailed anatomic evaluation with minimal artifacts.
Image acquisition at 3 T combined with parallel processing makes 3D volume acquisition at nearly isovoxel resolution through the entire brain a practical reality. Although technically feasible on our clinical 1.5-T MRI units, this sequence was less desirable from a diagnostic standpoint owing to degradation in image quality due to increased noise and time constraints. High-resolution 3D volume isovoxel acquisitions facilitate multiplanar reformation in any plane, which is important for accurate lesion differentiation from normal gray–white matter structures. Reformatting a gyrus with in-plane orient ation into a perpendicular orthogonal plane can be critical for avoiding the volume-averaging effects that result in overcalling gray–white matter thickening or indistinct ness. These sequences are also highly desirable for neurosurgeons in preoperative planning.
Since the completion of our study, high-resolution 3D T2-weighted and FLAIR techniques have become commercially available for our 3-T MRI units. Although we aim to explore the advantages of such techniques at 3 T, they are not practically feasible at 1.5 T because of time constraints; therefore, the techniques are not directly comparable.
Our results are concordant with findings reported for 3-T MRI with eight-channel phased-array surface coils in the evaluation of focal epilepsy [10]. The major gains in diagnosis in our study not surprisingly were related to detection of cortical malformations, because many of our patients are referred for follow-up MRI because of failures of imaging localization with 1.5-T MRI. These abnormalities are often subtle; thin slices are needed to avoid partial volume effects and to detect subtle areas of gray–white matter blurring and indistinctness [11, 12]. The improved gray–white matter contrast at 3 T in our study highlights the importance of this factor. MRI at 3 T was excellent for depiction of the gray–white matter junction (tissue contrast) in our study, showing statistically significant improvement over 1.5-T MRI.
The limitations of high-field-strength imaging are well known, including a propensity to certain imaging artifacts, such as sus ceptibility and a perceived sensitivity to motion. Although usually undesirable, great er susceptibility effects at 3 T can be ad vantageous, as when detection of abnormal vessels or previous hemorrhage is relevant. Detection of two cavernous malformations in our study was improved by susceptibility effects, which were greater at 3 T than at 1.5 T.
Disadvantages of imaging at 3 T include longer T1, increased acoustic noise, greater power deposition, and greater device incompatibility [13–16]. Although motion artifacts were found to be similar at 1.5 and 3 T, other imaging artifacts were notably fewer at 3 T in our study. We did not anticipate this finding, which might have been related in part to the relatively young age of the patient population, who have minimal or no susceptibility problems related to previous intracranial surgery or hemorrhage.
Our study had several limitations. The retrospective nature of the review, the indications for a second MRI examination at 3 T, and the need to exclude patients without directly comparable sequences may have introduced selection bias. Epilepsy patients undergo 3-T MRI at our institution for various reasons, including normal or equivocal findings on 1.5-T MRI, clarification of lesion characterization, surgical planning, and scheduling constraints. However, because normal or equivocal findings on 1.5-T MRI should theoretically increase the likelihood of normal findings on 3-T MRI (implying a lower pretest probability of disease), repetition of imaging at 3 T should adversely affect rather than improve the likelihood of identification of a structural lesion. By contrast, we found more than twofold improvement in lesion detection on 3-T compared with 1.5-T MRI.
Because we could not control for the timing of the 1.5-T and 3-T examinations, there might have been differences in visualization of certain conditions that change over time, such as tumor growth and conspicuity changes relat ed to interim developmental myelination [17, 18]. We also did not blind individual radiologists to viewing both sets of MR images at the same time. Although this factor can introduce bias, it was unavoidable given the nature of our study, which was direct assessment of differences in image quality.
Identical protocol, acquisition times, and coil type were not practically possible in this retrospective study. We do not routinely use dedicated surface coils or multichannel coils for our 1.5-T MRI units in part because of image degradation from inadequate signal-to-noise ratio. Most of the patients in our practice did not have specific localizing information, rendering accurate surface coil placement impossible. Phased-array surface coils in the past have been limited by smaller volumes of coverage and inherently heterogeneous signal intensity over the field of view, precluding visualization of anatomic detail of the brain parenchyma outside the coil isocenter. Surface coils work well in the evaluation of mesial temporal sclerosis, for example, in which technologists can routinely position the coil over the temporal lobes in a reproducible manner. Finally, given the high proportion of pediatric epilepsy in our practice, a large number of patients undergo sedation or anesthesia for MRI, making coil changes during a whole-brain epilepsy examination undesirable.
In the assessment of new imaging technology, an important consideration is whether improvements in image quality have a clinically beneficial effect [9]. Most patients with focal epilepsy in this study had superior lesion localization and diagnosis with 3-T MRI. Most of the patients who underwent surgery had substantial clinical improvement or resolution of seizures.
In conclusion, MRI at 3 T was superior to 1.5-T MRI in the detection and accurate characterization of structural brain abnormalities in a group of patients undergoing whole-brain epilepsy evaluation at our institution. Compared with 1.5-T MR images, whole-brain 3-T MR images are of better quality, do not require surface coils or specific knowledge of lesion location, and are not limited by technical artifacts. Imaging at 3 T should be strongly considered in the evaluation of patients with focal epilepsy and previously equivocal or normal findings on 1.5-T MRI.
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