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Cervical Spinal Cord Lesions in Multiple Sclerosis: T1-weighted Inversion-Recovery MR Imaging with Phase-Sensitive Reconstruction¹

¹ From the Department of Diagnostic and Interventional Radiology (A.H.P., P.H., P.A.N.) and Department of Neurology (F.N., J.S.W.), The University of Texas Medical School at Houston, 6431 Fannin Street, Houston, TX 77030. From the 2006 RSNA Annual Meeting. Received November 6, 2006; revision requested January 4, 2007; revision received January 24; accepted March 7; final version accepted April 19. Supported by National Institutes of Health grants R01 EB02095 and 1 S10 RR19186. Address correspondence to P.A.N. (e-mail: ponnada.a.narayana{at}uth.tmc.edu).

	ABSTRACT

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This magnetic resonance (MR) imaging study was approved by the institutional review board and was HIPAA compliant. Written informed consent was obtained from all participants. The purpose of the study was to prospectively compare T1-weighted inversion recovery with short inversion time inversion recovery (STIR) and dual fast spin echo (FSE) for imaging cervical spinal cord lesions in patients with multiple sclerosis (MS). Twelve patients (eight men, four women; median age, 44 years) were imaged by using T1-weighted inversion recovery, STIR, and FSE. Contrast between lesions and normal cervical cord was measured for each sequence, and generalized estimating equation analysis was used to test statistical significance of the results. Normalized contrast between lesion and normal-appearing spinal cord was significantly higher for T1-weighted inversion recovery than for the other sequences (P < .0001). Use of phase-sensitive reconstruction improved lesion localization and boundary definition. These advantages of T1-weighted inversion recovery over STIR and dual-echo FSE suggest that it has potential in cervical spinal cord imaging of MS.

© RSNA, 2007

	INTRODUCTION

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Spinal cord involvement in multiple sclerosis (MS) is well documented (1–8). At present, the dual fast spin-echo (FSE) technique remains the reference standard for spinal cord magnetic resonance (MR) imaging in MS (9,10). Focal lesions are seen on images obtained with short echo times and those obtained with long echo times (5), but diffuse lesions are usually seen only with short echo times (10). Fluid-attenuated inversion recovery, while routinely used for lesion detection in the brain, lacks sensitivity for lesions in the cervical cord compared with FSE (10–12). The short inversion time inversion-recovery (STIR) sequence has been found to be sensitive for lesion detection, particularly diffuse lesions (9,10,13,14). While STIR offers substantially improved lesion-to-cord contrast-to-noise ratio, it is, however, more susceptible to flow-related artifacts, lower image quality, and lower interobserver agreement than conventional sequences (9,10). Although STIR provides essential supplementary information to conventional imaging for the visualization of spinal cord lesions in MS, it is not a substitute for other sequences (9,10).

A promising potential alternative to STIR in imaging spinal cord lesions is T1-weighted inversion recovery (15). This technique uses an inversion time that is longer than that at STIR but shorter than that at T1-weighted fluid-attenuated inversion recovery, which was previously reported by Melhem et al (16). T1-weighted inversion recovery may also be combined with phase-sensitive reconstruction to improve the dynamic range (15). T1-weighted inversion recovery has been successfully applied to imaging white matter lesions (15) and cortical gray matter lesions in MS (17). Thus, the purpose of our study was to prospectively compare T1-weighted inversion recovery with STIR and dual FSE for imaging cervical spinal cord lesions in patients with MS.

	MATERIALS AND METHODS

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Subjects
This study was approved by the local institutional review board and was Health Insurance Portability and Accountability Act compliant. Written informed consent was obtained from all participants. Twelve consecutive patients with MS (eight men, four women; median age, 44 years; age range, 23–65 years) and known cervical spinal cord lesions were imaged during the period from March 2006 to July 2006.

MR Image Acquisition
All MR imaging was performed with a 3.0-T imager (Intera; Philips Medical Systems, Best, the Netherlands) with a Quasar gradient system (80 mT/m with a slew rate of 200 [mT·m^–1]/sec) and a six-element cervical-thoracic-lumbar phased-array coil (Philips Medical Systems). The MR imaging protocol included dual FSE, STIR, and T1-weighted inversion recovery (Table 1). The T1-weighted inversion-recovery sequence was optimized for imaging time by implementing an interleaved time-efficient acquisition, as described previously (15). The inversion time was 200 msec for STIR and 400 msec for T1-weighted inversion recovery.

MR Image Analysis
All images were reviewed (P.A.N., J.S.W., and F.A.N., with 20, 17, and 6 years of experience in MR imaging, respectively). Lesions of the cervical spinal cord were identified by consensus on T1-weighted inversion-recovery images with magnitude reconstruction, T1-weighted inversion-recovery images with phase-sensitive reconstruction, STIR images, and dual FSE images. T1-weighted inversion-recovery and STIR images were qualitatively evaluated for delineation of lesion boundaries and visualization of diffuse lesions. Transverse T1-weighted inversion-recovery images were used for lesion localization within the cord and to verify the existence of lesions not seen on STIR or dual FSE images.

Quantitative measurements were obtained (A.H.P., with 8 years of experience in MR imaging) in focal and diffuse lesions that were clearly visible on both STIR and T1-weighted inversion-recovery images. Measurements were also obtained in lesions that were clearly visible at both echo times at dual FSE, although there were substantially fewer of these. At each section location with a visible lesion area of 0.1 cm² or greater, regions of interest were drawn (A.H.P.) in the lesion and normal-appearing spinal cord. Consistent positioning of the regions of interest in the same lesions across different series was achieved by carefully examining the landmarks (vertebral bodies, nerve root exits, etc) on the images.

Mean signal intensities in these regions of interest, denoted as S_lesion and S_cord, were used to calculate the normalized lesion-to-cord contrast (C₀) by using the following equation:

(1)

This metric, expressed as a percentage, describes the detectability of the lesion against the cord background, with zero representing identical lesion and cord signal intensities and 100% representing the signal intensity of the lesion being twice that of the cord.

Lesions with a C₀ value of less than 10% on any of the images were excluded from the analysis. Large lesions (1.0 cm or greater) were sampled with several regions of interest. A total of 144 region-of-interest measurements were obtained in this manner and organized into four groups (T1-weighted inversion recovery with magnitude reconstruction, T1-weighted inversion recovery with phase-sensitive reconstruction, STIR, and dual FSE).

Statistical Analysis
Region-of-interest measurements were divided into groups corresponding to each of the three sequence types. The generalized estimating equation (18) was used to test if C₀ values were significantly different between dual FSE, STIR, T1-weighted inversion recovery with magnitude reconstruction, and T1-weighted inversion recovery with phase-sensitive reconstruction. This method accounts for the correlation of parameter values within a single participant or within a lesion spanning multiple sections. After performance of Bonferroni correction for multiple comparisons, a P value of less than .0125 (.05/4) was used to indicate a significant difference. Statistical calculations were performed by using software (SAS, version 9.1, 2006; SAS Institute, Cary, NC).

Simulation
To compare our results with the theoretical effect of using phase-sensitive reconstruction on lesion-to-cord contrast, we performed simulations of the signal and contrast of a T1-weighted inversion-recovery sequence as a function of inversion time (TI). The signal intensity (S) of an inversion-recovery pulse sequence is proportional to the longitudinal magnetization, M_z(TI), which can be written as follows (19):

(2)

Here, is proton density, T1 is spin-lattice relaxation time, and TR is repetition time. This equation assumes that echo time is much less than repetition time and the inversion pulse is 180°. For our simulation, we applied Equation (2) for normal-appearing spinal cord and lesion, with a cord T1 value of 577 msec corresponding to a signal null at an inversion time of 400 msec, which was the inversion time used with our T1-weighted inversion-recovery sequence. The lesion T1 value was set to 110% of cord T1, or 635 msec, and repetition time was set to 4000 msec. The simulation was normalized to = 1 because the proton density is a global scaling factor for the signal curve and hence does not affect the actual inversion time null points.

	RESULTS

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At visual inspection, T1-weighted inversion-recovery images with magnitude reconstruction and T1-weighted inversion-recovery images with phase-sensitive reconstruction demonstrated the highest lesion-to-cord contrast (Fig 1). All 40 lesions in the 12 patients that were clearly visible on STIR images were also seen on T1-weighted inversion-recovery images with magnitude reconstruction and T1-weighted inversion-recovery images with phase-sensitive reconstruction. Of these lesions, only 24 were visualized on dual FSE images. In five patients, a total of six lesions were visible on T1-weighted inversion-recovery images but were not visible on STIR images (Fig 2).

View larger version (60K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: Sagittal images in patient with MS acquired with (a) short-echo FSE (repetition time msec/echo time msec, 2000/8.4), (b) long-echo FSE (2000/80), (c) STIR (repetition time msec/echo time msec/inversion time msec, 3000/70/200), and (d,e) T1-weighted inversion recovery (2400/8/400) by using (d) magnitude and (e) phase-sensitive reconstruction. Two large lesions (arrows) are visible at this section location on all images, which illustrates relative lesion-to-cord contrast between them.

View larger version (55K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: Sagittal images in patient with MS acquired with (a) short-echo FSE (repetition time msec/echo time msec, 2000/8.4), (b) long-echo FSE (2000/80), (c) STIR (repetition time msec/echo time msec/inversion time msec, 3000/70/200), and (d,e) T1-weighted inversion recovery (2400/8/400) by using (d) magnitude and (e) phase-sensitive reconstruction. Two large lesions (arrows) are visible at this section location on all images, which illustrates relative lesion-to-cord contrast between them.

View larger version (51K): [in this window] [in a new window] [Download PPT slide]   Figure 1c: Sagittal images in patient with MS acquired with (a) short-echo FSE (repetition time msec/echo time msec, 2000/8.4), (b) long-echo FSE (2000/80), (c) STIR (repetition time msec/echo time msec/inversion time msec, 3000/70/200), and (d,e) T1-weighted inversion recovery (2400/8/400) by using (d) magnitude and (e) phase-sensitive reconstruction. Two large lesions (arrows) are visible at this section location on all images, which illustrates relative lesion-to-cord contrast between them.

View larger version (46K): [in this window] [in a new window] [Download PPT slide]   Figure 1d: Sagittal images in patient with MS acquired with (a) short-echo FSE (repetition time msec/echo time msec, 2000/8.4), (b) long-echo FSE (2000/80), (c) STIR (repetition time msec/echo time msec/inversion time msec, 3000/70/200), and (d,e) T1-weighted inversion recovery (2400/8/400) by using (d) magnitude and (e) phase-sensitive reconstruction. Two large lesions (arrows) are visible at this section location on all images, which illustrates relative lesion-to-cord contrast between them.

View larger version (52K): [in this window] [in a new window] [Download PPT slide]   Figure 1e: Sagittal images in patient with MS acquired with (a) short-echo FSE (repetition time msec/echo time msec, 2000/8.4), (b) long-echo FSE (2000/80), (c) STIR (repetition time msec/echo time msec/inversion time msec, 3000/70/200), and (d,e) T1-weighted inversion recovery (2400/8/400) by using (d) magnitude and (e) phase-sensitive reconstruction. Two large lesions (arrows) are visible at this section location on all images, which illustrates relative lesion-to-cord contrast between them.

View larger version (80K): [in this window] [in a new window] [Download PPT slide]   Figure 2a: Sagittal images in patient with MS acquired with (a) STIR (3000/70/200) and (b,c) T1-weighted inversion recovery (2400/8/400) by using (b) magnitude and (c) phase-sensitive reconstruction. Lesion (arrow) visible on b and c is not visible on a. Every lesion visualized on STIR images was seen on T1-weighted inversion recovery images with magnitude reconstruction and T1-weighted inversion recovery images with phase-sensitive reconstruction, but not vice versa. Note two additional lesions visible at this section location, on posterior (dorsal) side of cord, caudal to labeled lesion.

View larger version (81K): [in this window] [in a new window] [Download PPT slide]   Figure 2b: Sagittal images in patient with MS acquired with (a) STIR (3000/70/200) and (b,c) T1-weighted inversion recovery (2400/8/400) by using (b) magnitude and (c) phase-sensitive reconstruction. Lesion (arrow) visible on b and c is not visible on a. Every lesion visualized on STIR images was seen on T1-weighted inversion recovery images with magnitude reconstruction and T1-weighted inversion recovery images with phase-sensitive reconstruction, but not vice versa. Note two additional lesions visible at this section location, on posterior (dorsal) side of cord, caudal to labeled lesion.

View larger version (87K): [in this window] [in a new window] [Download PPT slide]   Figure 2c: Sagittal images in patient with MS acquired with (a) STIR (3000/70/200) and (b,c) T1-weighted inversion recovery (2400/8/400) by using (b) magnitude and (c) phase-sensitive reconstruction. Lesion (arrow) visible on b and c is not visible on a. Every lesion visualized on STIR images was seen on T1-weighted inversion recovery images with magnitude reconstruction and T1-weighted inversion recovery images with phase-sensitive reconstruction, but not vice versa. Note two additional lesions visible at this section location, on posterior (dorsal) side of cord, caudal to labeled lesion.

View larger version (79K): [in this window] [in a new window] [Download PPT slide]   Figure 3a: Sagittal images in patient with MS acquired with (a) STIR (3000/70/200) and (b,c) T1-weighted inversion recovery (2400/8/400) by using (b) magnitude and (c) phase-sensitive reconstruction. Diffuse lesion (arrow) is only faintly visible with STIR but is much more readily seen with T1-weighted inversion recovery, with both magnitude and phase reconstruction.

View larger version (74K): [in this window] [in a new window] [Download PPT slide]   Figure 3b: Sagittal images in patient with MS acquired with (a) STIR (3000/70/200) and (b,c) T1-weighted inversion recovery (2400/8/400) by using (b) magnitude and (c) phase-sensitive reconstruction. Diffuse lesion (arrow) is only faintly visible with STIR but is much more readily seen with T1-weighted inversion recovery, with both magnitude and phase reconstruction.

View larger version (79K): [in this window] [in a new window] [Download PPT slide]   Figure 3c: Sagittal images in patient with MS acquired with (a) STIR (3000/70/200) and (b,c) T1-weighted inversion recovery (2400/8/400) by using (b) magnitude and (c) phase-sensitive reconstruction. Diffuse lesion (arrow) is only faintly visible with STIR but is much more readily seen with T1-weighted inversion recovery, with both magnitude and phase reconstruction.

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 4a: Transverse T1-weighted inversion-recovery images (2600/9.3/400) of lesions in Figure 1, acquired by using (a) magnitude and (b) phase-sensitive reconstruction. Sagittal sections (center columns in a and b) are shown for reference, with arrows indicating transverse locations for superior (column to left in a and b) and inferior (column to right in a and b) lesions.

View larger version (156K): [in this window] [in a new window] [Download PPT slide]   Figure 4b: Transverse T1-weighted inversion-recovery images (2600/9.3/400) of lesions in Figure 1, acquired by using (a) magnitude and (b) phase-sensitive reconstruction. Sagittal sections (center columns in a and b) are shown for reference, with arrows indicating transverse locations for superior (column to left in a and b) and inferior (column to right in a and b) lesions.

View larger version (13K): [in this window] [in a new window] [Download PPT slide]   Figure 5a: Graph of results of simulations of (a) signal intensity and (b) contrast of normal-appearing spinal cord and lesion as function of inversion time. Simulation assumes repetition time of 4000 msec, cord T1 of 577 msec, and lesion T1 of 635 msec. Proton density was normalized to 1. Contrast hole is seen by using magnitude reconstruction (recon) in inversion-time window between signal null points.

View larger version (12K): [in this window] [in a new window] [Download PPT slide]   Figure 5b: Graph of results of simulations of (a) signal intensity and (b) contrast of normal-appearing spinal cord and lesion as function of inversion time. Simulation assumes repetition time of 4000 msec, cord T1 of 577 msec, and lesion T1 of 635 msec. Proton density was normalized to 1. Contrast hole is seen by using magnitude reconstruction (recon) in inversion-time window between signal null points.

	DISCUSSION

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Somewhat surprisingly, unlike researchers in previous studies in the brain (15), we did not observe a statistically significant improvement in lesion-to-cord contrast by using phase-sensitive reconstruction. Optimal tissue contrast for inversion-based methods has been shown to be dependent on the choice of reconstruction algorithm, as well as on the selection of inversion time (21), with the latter dependent on the T1 relaxation values of the tissue or lesion of interest. Our simulation results suggest that T1-weighted inversion recovery with phase-sensitive reconstruction confers a contrast advantage over T1-weighted inversion recovery with magnitude reconstruction only within a narrow range of inversion-time values, because of the relative similarity of lesion and cord parenchyma relaxation times (Fig 5). Because this inversion time window can vary from lesion to lesion, phase-sensitive reconstruction is generally preferred over magnitude reconstruction to avoid the contrast hole. Use of phase-sensitive reconstruction also provides the added benefits of improved lesion localization and better definition of lesion boundaries, as noted above.

The inversion delay time used in our study was not specifically optimized for spinal cord imaging. Results of preliminary studies with varied inversion times indicate that further optimization of the delay time is indeed possible and should result in a small, but measurable, improvement in lesion-to-cord contrast at T1-weighted inversion recovery with phase-sensitive reconstruction versus that at T1-weighted inversion recovery with magnitude reconstruction. We emphasize, however, that even without this optimization, the T1-weighted inversion-recovery sequence had a nearly threefold advantage in lesion-to-cord contrast over STIR and a sixfold advantage over dual FSE.

The primary limitation of our study was the small number of patients who were imaged by using the dual FSE, STIR, and T1-weighted inversion-recovery sequences for comparison. In addition, cardiac gating was not used with any of the pulse sequences to minimize acquisition time.

In conclusion, the T1-weighted inversion-recovery pulse sequence appears to be a promising method for visualization of cervical lesions in MS. The T1-weighted inversion-recovery method provides higher normalized signal contrast between lesions and normal-appearing spinal cord than the STIR or dual FSE method and provides excellent delineation of lesion boundaries. Studies with more patients are needed to further demonstrate the relative advantages of T1-weighted inversion recovery over STIR and dual FSE. Additional optimization of the delay time might further increase the lesion-to-cord contrast of phase-sensitive reconstruction of T1-weighted inversion-recovery images.

	ADVANCES IN KNOWLEDGE

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• T1-weighted inversion recovery improves depiction of cervical spinal cord lesions in multiple sclerosis.
  
• T1-weighted inversion recovery provides normalized contrast that is quantitatively superior to that provided by commonly used sequences in the detection of cervical spinal cord lesions.
  

	IMPLICATION FOR PATIENT CARE

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• T1-weighted inversion recovery MR imaging of patients with multiple sclerosis permits characterization of cervical spinal cord disease.
  

	ACKNOWLEDGMENTS

 
We acknowledge Vipulkumar Patel, RT, for invaluable assistance with imaging and protocol optimization and Chul Ahn, PhD, for lending his biostatistics expertise in statistical analysis of the results.

	FOOTNOTES

 

Abbreviations: FSE = fast spin echo • MS = multiple sclerosis • STIR = short inversion time inversion recovery

Guarantors of integrity of entire study, A.H.P., P.A.N.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, A.H.P., P.A.N.; clinical studies, F.M.N., J.S.W.; experimental studies, A.H.P., P.H., P.A.N.; statistical analysis, A.H.P.; and manuscript editing, A.H.P., J.S.W., P.A.N.

Authors stated no financial relationship to disclose.

	References

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Poonawalla, A. H. Articles by Narayana, P. A. Search for Related Content PubMed PubMed Citation Articles by Poonawalla, A. H. Articles by Narayana, P. A.