Physica Medica xxx (2015) 1e7

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High resolution MR eye protocol optimization: Comparison between 3D-CISS, 3D-PSIF and 3D-VIBE sequences Irene Tsiapa a, b, d, *, Miltiadis K. Tsilimbaris b, Efrosini Papadaki c, Penelope Bouziotis d, Ioannis G. Pallikaris b, Apostolos H. Karantanas c, Thomas G. Maris a a

Department of Medical Physics, University of Crete, Heraklion, Crete, Greece Department of Ophthalmology, University Hospital of Crete, Heraklion, Crete, Greece Department of Radiology, University of Crete, Heraklion, Crete, Greece d Institute for Nuclear and Radiological Sciences, Technology, Energy and Safety, National Center of Scientific Research “Demokritos”, Aghia Paraskevi, Athens, Greece b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 January 2015 Received in revised form 3 March 2015 Accepted 19 March 2015 Available online xxx

Purpose: The purpose of this study was to compare selected MRI pulse sequences and to evaluate their utility for depicting specific anatomic regions in the eye. Methods: A High-Resolution (HR) 0.08  0.08  0.60 mm3 MRI protocol was developed on a 1.5-T clinical system and applied in the left eye of an albino rabbit, utilizing a small field of view surface coil. The comprehensive MRI protocol consisted of two 3D (T2/T1)w sequences (3D-PSIF and 3D-CISS), and one 3D T1w sequence (3D-VIBE). The T1w 3D-VIBE sequence was acquired, before and after intravenous injection of 0.2 mmol/kgr gadolinium-DTPA. Signal-to-Noise Ratios (SNR) and Contrast-to-Noise Ratios (CNR) amongst specific eye anatomical areas were calculated for each sequence. The presence of artifacts was rated subjectively utilizing a 5 point scale. Results: 3D-PSIF and 3D-CISS provide better delineation and visualization of the eye as compared with 3D-VIBE sequences. 3D-CISS images present the highest SNR and revealed better discrimination of the ocular surrounding tissues; its basic drawback though is related to ghost artifacts appearing in the anterior chamber and resulting in the lowest image quality. In post-contrast imaging, the T1w 3D-VIBE sequence provided the best overall image quality. Moreover, 3D (T2/T1)w sequences can provide good anatomic depiction of the eye segments. Agreement between the two independent readers was good. Conclusions: Optimization of a comprehensive MR eye imaging protocol is achieved. A higher SNR, a better spatial resolution and a reduction of the total scan time were obtained, thus making clinical MRI systems more reliable in eye imaging. © 2015 Associazione Italiana di Fisica Medica. Published by Elsevier Ltd. All rights reserved.

Keywords: MR eye Ophthalmology Ocular tissues High-resolution MRI

Introduction High-Resolution Magnetic Resonance Imaging (HR-MRI) is a promising tool for non invasive imaging of vascular anatomy or pathology of the orbit and its contents [1e9]. MRI is widely accepted as a powerful method for diagnostic imaging because it provides three-dimensional (3D) high-resolution (HR) anatomical images with excellent soft-tissue contrast. Recently, MRI

* Corresponding author. Department of Medical Physics, MRI Unit, University Hospital of Heraklion, University of Crete, GR 71201, Heraklion, Crete, Greece. Tel.: þ30 2810 392797; fax: þ30 2810 542095. E-mail addresses: [email protected], [email protected] (I. Tsiapa).

techniques have been applied to ophthalmology providing both structural and functional information in order to evaluate the therapeutic effectiveness, facilitate diagnosis and assist preoperative planning [10e16]. Moreover, MRI is a promising non-invasive method for ocular-drug delivery assessment [17,18]. HR-MRI has already been used in ocular imaging for: (a) depicting fine anatomical structures [4e6,11e13], (b) non-invasive blood flow measurements [7e9], (c) various pathological conditions [11e16], as well as, for age-related induced changes in ocular dimensions in vivo [19e22]. MRI allows detection of the cause of ocular abnormalities related to primary orbital pathologies. Another indication for MRI of the eye is the evaluation of gross ocular abnormalities which due to severe optical turbidity

http://dx.doi.org/10.1016/j.ejmp.2015.03.009 1120-1797/© 2015 Associazione Italiana di Fisica Medica. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Tsiapa I, et al., High resolution MR eye protocol optimization: Comparison between 3D-CISS, 3D-PSIF and 3DVIBE sequences, Physica Medica (2015), http://dx.doi.org/10.1016/j.ejmp.2015.03.009

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alterations cannot be assessed with a standard clinical examination. Moreover, a fast 3D HR-MRI technique is a prerequisite in order to examine subtle changes that result either from age or disease. The eye is the ideal tissue for HR-MRI because of its wide variation in water content (vitreous humor and aqueous humor) and in particular due to the requirement of high spatial resolution utilizing the smallest possible field of view (FOV). Moreover, ocular imaging requires high spatial resolution imaging with adequate signal-tonoise-ratio (SNR). An increment of the strength of the static magnetic field (B0) results in a higher SNR. The higher SNR is always associated with enhanced spatial resolution and a shorter scan time. Most of the numerical information provided by MRI is based on measurements of pixel intensity, thus providing values for the SNR, contrast-to-noise ratio (CNR), T1, T2 relaxation times, and coefficients characterizing the water diffusion or ocular perfusion [1,2,5,23e30]. The information provided can be used for the differentiation of abnormal and normal tissues, the detection of tumors, and for cellular activity analyses. Typical anatomical MRI contrasts arise from differences in water hydrogen proton density, relaxation times, and apparent diffusion coefficient (ADC). Different tissue types have different hydrogen proton density, T1, T2, and water ADC, giving rise to a vast variation of MRI contrasts. Water-hydrogen relaxation times (such as T1 and T2) are dependent on the local biophysical and biochemical environments; water-hydrogen displacement in biological tissues is restrictive and anisotropic due to the presence of semi permeable cell membranes, macromolecules and organelles. As a result, different weighting techniques, such as T1, T2, and diffusion weighting, can reveal details of the eye's structures [1,2,5,23e30]. Particularly, T1-weighted (T1w) images can provide better anatomical detail but the strong orbital fat signal can over-saturate smaller adjacent structures [5,6,29,31]. T2-weighting can improve visualization of the inner surface of the globe, because of the bright vitreous signal, but is vulnerable to motion artifacts, H0 artifacts and has lower SNR [22,31,32]. New MRI methodologies, such as the use of specialized orbital coils [6,10,12,13,32,33] in combination with paramagnetic contrast agents for image enhancement [1,2,5,27,34], have been reported in MRI of the eye. Orbital coils improve the SNR in the region of interest in the eye and thus provide higher spatial resolution which allows depiction of more of the fine details of eye anatomy. An additional benefit of using surface coils is that image acquisition can be limited to the eye region, thereby shortening scan times due to the maximum possible SNR gain. On the other hand, extracellular contrast agents based on gadolinium (Gd), manganese (Mn), and superparamagnetic iron oxide (SPIO) nanoparticles have been used in several ocular MRI studies [1,2,9,27,34]. The mechanism for contrast enhancement is based on the shortening of the T1 and/or T2/T2* relaxation times of the regions in the eye. Gd-based agents, such as Gadolinium diethylenetriaminepenta-acetic acid (GdDTPA), are commonly used in clinical MRI to enhance image contrast. They provide greater detail in the vascularized portions of the eye. Moreover, they are used for the evaluation of the diffusional pathways of plasma-derived solutes through the blood-toocular barriers [2,5,7,8,27] or in standard dynamic contrastenhanced MRI studies [7, 28]. Within the framework of the present study, we developed a comprehensive HR-MRI protocol for a 1.5T clinical system. Experiments were performed using T1w, (T2/T1)w and post-Gd T1w sequences utilizing a standard body coil as a transmitter and a small surface coil as a receiver. The goal of this study was to quantitatively and qualitatively compare the 3D (T2/T1)w sequences and the 3D T1w sequences for HR-MR imaging of the eye utilizing a 1.5T whole body imaging system.

Materials and methods Animals Three albino rabbits of 2.5e3.5 kg were used in the experiments under the approval of the Association for Research in Vision and Ophthalmology Statement for the Use of Animals in Ophthalmic and Vision Research and the institutional guidelines. The rabbits were anesthetized by a subcutaneous injection of a mixture containing ketamine hydrochloride (50 mg/kg) and xylazine (10 mg/ kg) solution. MR image acquisition MR imaging was performed using a clinical 1.5T whole-body superconducting imaging system (MAGNETOM Sonata/Vision, Siemens Healthcare, Erlangen, Germany), equipped with high performance gradients (Gradient strength: 40 mT/m, Slew rate: 200 mT/m/ms) utilizing a standard circular polarized (CP) body coil as a transmitter and a linear polarized (LP) small circular surface coil (Diameter z5 cm) as a receiver. The small surface coil was mounted and immobilized on an in house designed MR compatible holder apparatus. The rabbits were anesthetized and placed on top of a custom-built plastic cough in prone position. The small surface coil was placed on the right eye of the anesthetized rabbit and was tightly bound to the immobilization holder in order to gain the maximum possible SNR and avoid possible artifacts due to the coil micro-movement. The final image voxel dimensions were: (0.1  0.1) mm2 in- plane spatial resolution and 0.6 mm cross-plane spatial resolution (slice thickness). The comprehensive HR-MR imaging protocol consisted of two 3D (T2/T1)w sequences: (reverse fast imaging with steady state precession (3D-PSIF), constructive interference in steady state (3DCISS)) and one 3D T1w sequence: (volumetric interpolated breathhold examination (3D-VIBE)). The most important sequence parameters are shown in Table 1. The T1w 3D-VIBE sequence was acquired, before and after intravenous injection of gadolinium contrast agent [gadolinium (Gd)ediethylene triamine pentaacetic acid (DTPA); 0.5 M, 0.2 mL/kg body weight; Magnevist]. Quantitative analysis All images for all experimental animals were obtained at the same anatomical level of the eye in order to depict relevant anatomical structures. SNRs and CNRs amongst specific eye anatomical areas were quantitatively evaluated for each sequence. More specifically, the images were quantitatively evaluated utilizing the following metrics: (a) Signal Intensity (SI) values obtained from specific region of interest (ROI) measurements (mean, SD, and number of voxels) from the following 7 different anatomical eye structures: anterior chamber, vitreous humor, ciliary body,

Table 1 Typical imaging parameters used for the sequences that were applied for MR eye examination. Parameters

3D-PSIF

3D-CISS

3D-VIBE

Slice thickness (mm) No. of slices Field of view (mm) In-plane resolution (mm) TR (ms) TE (ms) Flip angle ( ) Scan time per volume (min)

0.6 30 60 0.08 20.92 10.19 70 3.10

0.6 30 60 0.08 12.98 5.5 70 3.40

0.6 30 60 0.09 11.80 5.02 15 3.50

Please cite this article in press as: Tsiapa I, et al., High resolution MR eye protocol optimization: Comparison between 3D-CISS, 3D-PSIF and 3DVIBE sequences, Physica Medica (2015), http://dx.doi.org/10.1016/j.ejmp.2015.03.009

I. Tsiapa et al. / Physica Medica xxx (2015) 1e7

chorioretina, extraocular muscles, iris, lens and (b) MR image background noise obtained from an artifact free ROI. All ROI's were positioned on the same anatomical structures and were all of the same relative size (Fig. 1). All metrics based upon ROI measurements were performed utilizing an image post-processing workstation (NordicICE v2.3.14, software-NNL). The SNRs for the selected ROIs were calculated according to the following formula: [35]

SNRROI ¼

SIROI ; 1:53  SDBg

SDSNR ¼

SDðSIROI Þ 1:53  SDBg

where, SIROI ¼ Mean Signal Intensity from the selected ROI,SD(SIROI) ¼ Standard Deviation of the mean signal intensity of the selected ROI,SDBg ¼ Standard Deviation from the mean background ROI measurement. The factor 1.53 is the Rayleigh noise distribution correction factor. The CNRs of the selected areas relative to the reference tissues were calculated according to the following formula: [35]

CNR ¼ jSNRROI  SNRREF j;

SDCNR

qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ¼ SD2SNR þ SD2REF

3

Statistical analysis Statistical analysis was performed using MedCalc (MedCalc Software, 9030 Mariakerke, Belgium) software. More specifically, statistical data analysis was based in paired t-test to compare means in order to determine statistically significant differences in SNRs and CNRs between the compared sequences. We considered P < 0.005 as a valid threshold for statistical significance. Agreement in scoring with the five-point scale between the two readers was assessed with the weighted Cohen k (kappa) statistic. Degrees of agreement were categorized as follows: k values of 0.00e0.20 were considered to indicate poor agreement; k values of 0.21e0.40, fair agreement; k values of 0.41e0.60, moderate agreement; k values of 0.61e0.80, good agreement; k values of 0.81e0.99, excellent agreement and k value of 1, perfect agreement. Results Quantitative results Representative HR T1w and (T2/T1)w-images of rabbit eye in vivo are presented in Fig. 2 and Fig. 3. The results of the quantitative analysis, obtained from the (T2/T1)w images and the T1w pre and post-contrast images, are shown in Table 2. The tissue SNR values for the different anatomic structures were found to be

Qualitative analysis For the qualitative analysis, all images were retrospectively evaluated by two experienced radiologists (PE, KA, with 17 and 24 years of experience in interpreting MRI, respectively). Both readers reviewed independently all images. Evaluations were categorized and documented by using standardized and documented data sheets. Qualitative analysis was performed separately and independently from the quantitative analysis. To avoid a learning bias, review of each image was performed in a randomized and blinded fashion. MR images were examined in a subjective manner with respect to qualitative parameters. A five-point grading scale (0 ¼ poor, 1 ¼ moderate, 2 ¼ good, 3 ¼ very good, 4 ¼ excellent) was used to evaluate image artifacts and image quality. For the presence of artifacts each sequence was evaluated in terms of chemical shift artifacts of the first kind, ghost artifacts and susceptibility artifacts for the selected structures of the eye. The score of both reviewers were averaged.

Figure 1. Seven ROIs obtained from the relative eye segments and one ROI obtained from the image background for the noise estimation. AC, anterior chamber; VH, vitreous humor; CB, ciliary body; CR, chorioretinal; EM, extraocular muscle; I, iris; L, lens; Bg, background.

Figure 2. Representative HR T1w-images of rabbit eye in vivo A) before and B) after Gd injection (FOV, 60  60 mm; matrix size, 640  640 pixels).

Please cite this article in press as: Tsiapa I, et al., High resolution MR eye protocol optimization: Comparison between 3D-CISS, 3D-PSIF and 3DVIBE sequences, Physica Medica (2015), http://dx.doi.org/10.1016/j.ejmp.2015.03.009

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the sequences. Agreement between the two independent readers was good with kappa values ranging between 0.58 and 0.85. Discussion

Figure 3. Representative HR (T2/T1)w-images of rabbit eye in vivo A) 3D-CISS image shows ghost artifacts (arrowheads, of anterior chambers). B) On the 3D-PSIF image obtained in the same experimental animal at the same anatomical level, no artifacts are present (FOV, 60  60 mm; matrix size, 768  768 pixels).

statistically significant (p < 0.0001) in all of the cases examined. The 3D-CISS sequence demonstrated the highest mean SNR and the pre-contrast imaging of 3D-VIBE sequence the lowest mean SNR value in reference to all measured structures (Fig. 4). Both the 3DCISS sequence and the post-contrast 3D-VIBE sequence presented higher statistically significant CNR values (p < 0.0001), in reference to all measured structures for most of the cases examined (Table 2).

Qualitative results The results of qualitative analysis obtained from all the images are presented in Table 3 for the T1w and (T2/T1)w sequences. In this analysis, relative image quality, ghost artifacts and artifacts were evaluated for the basic eye structures. Cumulative results of qualitative evaluation of the T1w and (T2/T1)w sequences, are presented in Table 4 and Fig. 4. In the post-contrast imaging, the 3D VIBE sequence had a higher scoring than the pre-contrast imaging, provide better overall image quality (Table 4 and Fig. 5). On the other hand, (T2/T1)w images revealed better delineation and visualization of the eye as compared with 3D-VIBE images. Even though 3D-CISS image shows ghost artifacts (Fig. 3A), no pulsation artifacts are visible in the 3D-PSIF image (Fig. 3B) resulting in a better image quality. Chemical shift artifacts were very low for all

The present study reveals the optimization of MRI protocol resulting in HR-MRI images of the eye structure at 1.5T clinical system utilizing a small circular surface coil. The imaging of ocular normal anatomy and pathology, requires high-quality images with excellent tissue contrast and anatomic detail. Several studies have explored which sets of imaging parameters may optimize contrast between various parts of ocular tissues and relative compartments [1,2,29]. In the present study, a comprehensive MRI protocol providing excellent spatial resolution 0.08  0.08  0.60 mm3 within a rapid scanning time (approx. 3.5 min) was developed. The scan sequences yield a voxel volume of 0.004 mm3 and an ineplane resolution 0.08 mm2 significantly better as compared with other studies using 1.5T systems [5,14,28,30,32,33] and comparable even with higher field systems (3e7T) [6,12,22,29]. A comprehensive MRI protocol, consisted of two (T2/T1)w sequences (3D-PSIF and 3D-CISS) and one T1w sequence (3D-VIBE), was developed and evaluated. The specific protocol reveals superior soft tissue contrast as compared to other ocular MRI studies [5,14,28,30,32,33]. Standard Steady-State-Free-Precession (SSFP) sequences are very sensitive to motion and flow, as compared to the optimized SSFP variant sequences like 3D-CISS and 3D-PSIF applied for the smallest possible FOV's enforced with the highest possible gradients in a balanced mode. These SSFP sequence variants provide better motion compensation due to their inherent design, and thus they are suitable for imaging the eye. RARE sequences (FSE, TSE) can reduce total acquisition time by filling multiple lines of kspace with each acquisition and were reported for eye imaging. RARE sequences with higher ETL factors depict short T2 structures of the eye with inferior delineation [23,31]. On the other hand, T1w sequences in SE, TSE and GRE techniques were commonly used in pre and post paramagnetic contrast agent imaging [5,6,11e14,30,32,33]. Although 1.5T MR scanners provide good soft tissue contrast, spatial resolution, and anatomic detail, they offer inferior SNR when compared with high and ultra-high-field MRI. Earlier published in vivo studies using 1.5T MR systems have shown limited spatial resolution [5,14,28,30,32,33]. In the present study SNR and CNR amongst specific eye anatomical areas were calculated for each sequence in order to easily estimate quantitative metrics of image quality. To the best of our knowledge, critical determinations of SNR and CNR values for the ocular anatomical structures (except of the lens) have not been reported in the literature. Comparing the 3Dsequences, 3D-CISS presents the highest mean value of SNR (50.57) (Fig. 3 and 4). As can be observed, the 3D-CISS sequence had higher values in the majority of the cases regarding the SNR and CNR values (Table 2). The high sensitivity of MR imaging provides an excellent means for the depiction of ocular anatomy. The spatial resolution was sufficient to differentiate the iris, ciliary body, anterior chamber, lens and chorioretinal in all subjects (Fig. 2 and 3). The T1w images showed immediate enhancement of the chorioretinal and ciliary body after gadolinium administration, demonstrating appropriate levels of intravenous contrast (Fig. 2). SNR was significantly improved in the 3D-VIBE post-contrast sequence (SNRpost-Gd: 20.21), as compared to the pre contrast value (SNRpre-Gd: 9.85) for the same sequence (Fig. 4). Moreover, the observed signal enhancement at the ciliary body suggests the involvement of local blood circulation in the anterior segment of the eye [1,2,28]. Thus, in post-contrast imaging CNR amongst the anatomic segments of the eye was significant increased (p < 0.0001) for most of the cases

Please cite this article in press as: Tsiapa I, et al., High resolution MR eye protocol optimization: Comparison between 3D-CISS, 3D-PSIF and 3DVIBE sequences, Physica Medica (2015), http://dx.doi.org/10.1016/j.ejmp.2015.03.009

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Table 2 Results of the quantitative comparison SNR and CNR (mean values ± SD, n ¼ 3) between the 3D T1w sequences (pre and post-Gd contrast agent) and (T2/T1)w sequences (3DPSIF and 3D-CISS). 3D-VIBE pre-Gd SNR CR VH AC CB L I EM CNR, Ref. CR AC CB L I EM CNR, Ref. CR VH AC CB I EM CNR, Ref. CR VH CB L I EM CNR, Ref. CR VH AC CB L I

tissue:

tissue:

tissue:

tissue:

9.09 5.26 7.91 10.72 16.44 11.42 8.11 VH 3.83 2.65 5.47 11.18 6.16 2.85 L 7.35 11.18 8.53 5.71 5.01 8.33 AC 1.18 2.65 2.82 8.53 3.51 0.20 EM 0.98 2.85 0.20 2.62 8.33 3.31

3D-VIBE post-Gd

P

3D-PSIF

3D-CISS

P

± ± ± ± ± ± ±

2.09 0.42 0.37 0.57 0.46 1.62 0.47

34.87 6.81 8.30 31.62 16.98 19.98 22.89

± ± ± ± ± ± ±

3.81 0.52 0.46 2.87 0.37 2.99 0.95

High resolution MR eye protocol optimization: Comparison between 3D-CISS, 3D-PSIF and 3D-VIBE sequences.

The purpose of this study was to compare selected MRI pulse sequences and to evaluate their utility for depicting specific anatomic regions in the eye...
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