FULL PAPER Magnetic Resonance in Medicine 73:2129–2141 (2015)

Generating Multiple Contrasts Using Single-Shot Radial T1 Sensitive and Insensitive Steady-State Imaging Thomas Benkert,1* Andreas J. Bartsch,2,3,4 Martin Blaimer,1 Peter M. Jakob,1,5 and Felix A. Breuer1 Purpose: Recently, the (Resolution Enhanced-) T1 insensitive steady-state imaging (TOSSI) approach has been proposed for the fast acquisition of T2-weighted images. This has been achieved by balanced steady-state free precession (bSSFP) imaging between unequally spaced inversion pulses. The purpose of this work is to present an extension of this technique, considerably increasing both the efficiency and possibilities of TOSSI. Theory and Methods: A radial trajectory in combination with an appropriate view-sharing reconstruction is used. Because each projection traverses the contrast defining k-space center, several different contrasts can be extracted from a single-shot measurement. These contrasts include various T2-weightings and T2/T1-weighting if an even number of inversion pulses is used, while an odd number allow the generation of several images with predefined tissue types cancelled. Results: The approach is validated for brain and abdominal imaging at 3.0 Tesla. Results are compared with RE-TOSSI, bSSFP, and turbo spin-echo images and are shown to provide similar contrasts in a fraction of scan time. Furthermore, the potential utility of the approach is illustrated by images obtained from a brain tumor patient. Conclusion: Radial T1 sensitive and insensitive steady-state imaging is able to generate multiple contrasts out of one single-shot measurement in a short scan time. Magn Reson C 2014 Wiley Periodicals, Inc. Med 73:2129–2141, 2015. V Key words: steady-state; SSFP; radial imaging; fast imaging; T2 contrast; FLAIR contrast

INTRODUCTION Balanced steady-state free precession (bSSFP) is the sequence with the highest signal-to-noise ratio (SNR) per unit time among all known imaging sequences (1). Images acquired with bSSFP typically show a mixed 1

€rzburg, Research Center Magnetic Resonance Bavaria (MRB), Wu Germany. 2 Department of Neuroradiology, University of Heidelberg, Heidelberg, Germany. 3 €rzburg, Wu €rzburg, Department of Neuroradiology, University of Wu Germany. 4 FMRIB Centre, University of Oxford, Oxford, United Kingdom. 5 €rzburg, Wu €rzburg, Department of Experimental Physics 5, University of Wu Germany. Grant sponsor: Bavarian Ministry of Economic Affairs, Infrastructure, Transport and Technology (BayStMWIVT). *Correspondence to: Thomas Benkert, M.Sc., Research Center Magnetic €rzburg, Germany. Resonance Bavaria (MRB), Am Hubland, D-97074 Wu E-mail: [email protected] Received 19 March 2014; revised 7 May 2014; accepted 5 June 2014 DOI 10.1002/mrm.25337 Published online 27 June 2014 in Wiley Online Library (wileyonlinelibrary. com). C 2014 Wiley Periodicals, Inc. V

contrast which is often described as T2/T1-like. While this can be beneficial for applications like cardiac imaging (2) or imaging of the musculoskeletal system (3), standard clinical protocols often require the acquisition of T2-weighted images (4). For this purpose, the most established technique is the turbo spin-echo (TSE) or rapid acquisition with relaxation enhancement (RARE) sequence (5). However, its clinical use can be limited due to long scan times. Furthermore, patient motion in combination with a segmented acquisition can lead to severe image degradation (6). Existing techniques for T2-weighted bSSFP imaging either rely on an appropriate magnetization preparation scheme (7–10) or on the initial application of a TSE pulse train as used in T2-TIDE, which is then ramped down to the conventional bSSFP flip angle (11). Previously, a promising alternative approach has been presented for the rapid generation of T2-weighted images. By inserting unequally spaced inversion pulses in between bSSFP readout blocks, T1-relaxation in bSSFP imaging can be suppressed and therefore, images with pure T2-contrast can be obtained (12). Therefore, this T1 insensitive steady-state imaging (TOSSI) technique combines short scan times (1–2 s per slice) and intrinsic high SNR efficiency of bSSFP with the capability to generate the desired T2-weighted images. However, a decrease in spatial resolution (also known as blurring) resulting from signal decay during the acquisition can considerably degrade the quality of TOSSI images. To account for this effect, a refinement called Resolution Enhanced (RE-)TOSSI has been proposed (13). Here, only the contrast defining k-space center is acquired with TOSSI, while the k-space periphery is sampled with conventional bSSFP. Because both concepts rely on a Cartesian k-space sampling scheme, the center of k-space is only acquired once. Therefore, just one single image per acquisition can be obtained, at least if specific techniques such as keyhole imaging (14,15), which frequently update the k-space center, are not used. Furthermore, the underlying Cartesian trajectory can lead to an intensification of artifacts due to motion or signal variation. In this work, a radial k-space trajectory is used for (RE-)TOSSI imaging, enabling the reconstruction of images with different T2-contrasts as well as a conventional bSSFP image with T2/T1-weighting out of one single-shot measurement. In addition, radial T1 sensitive and insensitive steady-state imaging (RA-TOSSI) further improves image quality in comparison to previously proposed TOSSI methods. Besides these advantages, a novel variant of the (RA-)TOSSI scheme is introduced allowing

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FIG. 1. a: RA-TOSSI implementation: a radial k-space containing Nproj projections is acquired using a TOSSI sequence for the first lNproj projections (0 < l < 1) and a conventional bSSFP sequence for the remaining (1-l)Nproj radial spokes. Within the TOSSI section, parallel bSSFP blocks are alternated with antiparallel bSSFP blocks, divided by inversion modules. As indicated, an inversion module consists of several parts (see text for details). b: Reconstruction scheme for the proposed technique: Applying a KWIC-filter as sliding window reconstruction on the RA-TOSSI dataset yields several image contrasts. Image quality of these contrasts (in terms of streaking artifacts and SNR) can then be improved using a principal component analysis.

the additional generation of multiple images with predefined species attenuated. This includes fluid suppression as used in fluid attenuated inversion recovery (FLAIR) imaging (16) for instance. After reviewing the magnetization course of the proposed technique by means of simulations, the use of RA-TOSSI is demonstrated for several in vivo applications at 3.0 Tesla (T), including abdominal imaging and brain imaging of healthy volunteers and of a brain tumor patient.

THEORY Basis Concept of T1 Insensitive Steady-State Imaging (TOSSI) The principal idea of the TOSSI concept is based on the fact that longitudinal relaxation can be compensated for by applying nonequidistant inversion pulses. Therefore, only transversal relaxation remains, enabling the acquisition of images with pure T2-contrast. While magnetization alternates between a parallel and an antiparallel state (regarding the direction of B0), a bSSFP sequence can be used to readout the signals and fill the k-space (12). Usually, the influence of successive radiofrequency (RF-) pulses forces magnetization to approach to a nonzero steady-state as it is widely known for conventional bSSFP (17). However, the inversion pulses applied here alter this behavior fundamentally. Similar to TSE or HASTE (18), where several consecutive refocusing pulses are played out as well, magnetization decays toward zero. If the k-space periphery is acquired while signal is very low, fine structures cannot be resolved anymore and therefore, blurring and noise is introduced which

degrades spatial resolution and limits overall image quality. Resolution Enhancement (RE-TOSSI) To enhance the resolution of TOSSI images, a segmented acquisition can be performed. However, this suggests an increased scan time, therefore reducing the efficiency of this technique. An alternative approach is a direct modification of the acquisition scheme (13). By removing the inversion pulses after a predefined time point, TOSSI changes its behavior toward conventional bSSFP with the consequence, that magnetization approaches the bSSFP steady-state. Therefore, the signal decay toward zero can be effectively prevented. Because two sequence types are applied to sample one k-space, this adaption can be seen as a TOSSI-bSSFP combined acquisition technique (19). Combining this sequence with a linear shifted k-space reordering scheme yields the desired result: using the TOSSI part for the acquisition of the contrast defining kspace center preserves the desired T2-contrast, while the acquisition of the k-space periphery with bSSFP improves spatial resolution. Analogous to TSE, the effective echo time (TEeffTOSSI) indicates the time span between the start of the acquisition and the acquisition of the central kspace line. Because TEeffTOSSI has to be placed in the TOSSI section, the reordering has to be chosen appropriately. Radial T1 Sensitive and Insensitive Steady-State Imaging (RA-TOSSI) Figure 1a shows the proposed scheme of the RA-TOSSI implementation. Analogous to RE-TOSSI, the acquisition of k-space is divided into a TOSSI part at the beginning,

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FIG. 2. Effect of the localization of magnetization after the last inversion pulse. Four different T2-values (T2 ¼ 60/80/100/500 ms, T1 ¼ 1000 ms) are depicted. The left hand column shows the absolute signal values, while values with regard to their sign are visualized in the right hand column. a: If magnetization is located in the parallel state (even number of inversion pulses), the bSSFP steady-state is approached quickly and signal has a continuous high level. This scheme allows the reconstruction of several T2-weighted TOSSI images (solid ellipses) as well as T2/T1-weighted bSSFP images (dashed ellipses). b: When starting the bSSFP block while magnetization is located in the antiparallel state (odd number of inversion pulses), magnetization crosses the zero-point. Therefore, images with multiple species attenuated (dotted ellipses) along with several T2-weighted TOSSI images (solid ellipses) can be reconstructed.

which is followed by a bSSFP part at the end. The ratio indicating the amount of acquired k-space points with each imaging sequence is defined by the parameter l. In the TOSSI section (where lNproj out of Nproj projections in total are acquired), inversion modules are placed in between bSSFP readouts. The inversion module consists of an a/2-TR/2 preparation pulse which flips the magnetization back onto the z-axis (20,21). Residual transversal magnetization is destroyed by spoiler gradients. Then, a selective adiabatic inversion pulse is played out, again followed by spoiler gradients and an a/2-TR/2 preparation. Contrary to conventional (RE-)TOSSI, the k-space is not sampled with Cartesian lines, but with radial projections. Because every projection traverses the k-space center, no explicit value for TEeffTOSSI can and has to be chosen. Therefore, no special care has to be taken regarding the selection and the realization of TEeffTOSSI. As a consequence, a specific k-space reordering as well as additional preparation pulses (13) can be omitted. Instead, postprocessing of RA-TOSSI data determines contrast, as will be described in the methods section. Variants of RA-TOSSI 1. Even Number of Inversion Pulses: T2- and T2/T1Weighted Imaging. Using a TOSSI-bSSFP combined

acquisition technique, the time point between the two sequence blocks has to be adjusted properly. When magnetization is located in the parallel state after the last inversion pulse, magnetization quickly approaches the bSSFP steady-state as shown in Figure 2a. This scheme has the benefit of producing images with high signal as well as reduced blurring and has also been applied in the original RE-TOSSI implementation in combination with Cartesian k-space sampling. In the case of RATOSSI, several T2-weighted TOSSI contrasts as well as T2/T1-weighted bSSFP contrasts can be extracted (indicated in Figure 2a by solid and dashed ellipses, respectively). 2. Odd Number of Inversion Pulses: Cancellation of Multiple Tissue Types. Starting the bSSFP block while magnetization is located in the antiparallel state changes the signal courses significantly. Magnetization crosses the time-axis during its approach to the bSSFP steadystate. As with conventional inversion recovery techniques, this zero-crossing depends on the underlying relaxation and on sequence parameters and therefore, magnetization of different species crosses the horizontal axis at different locations. Consequently, this RA-TOSSI variant allows the reconstruction of several T2-weighted images (solid ellipses in Figure 2b) and images with multiple tissue types attenuated (dotted ellipses), including

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FIG. 3. Bloch equation simulations for different sequences. The left hand column shows the magnitude of the time courses for four different T2-values (depicted in red like colors), each combined with four different T1-values (depicted in the same color). For the right hand column, one time point is chosen (dashed line) and for this point, signal values of different T1-values (depicted in blue like colors) are plotted against the simulated T2-values (depicted in the same color). a: Conventional bSSFP. b: T2-weighted TSE. c: Used RA-TOSSI implementation with a constant R value (TA ¼ 8, TP ¼ 24).

the cancellation of cerebrospinal fluid (CSF) similar to FLAIR imaging (16). METHODS

ms), therefore covering a large range of values found in the human brain (23). Other simulation parameters were as follows: flip angle a ¼ 40 , repetition time (TR) ¼ 4.7 ms, and l ¼ 0.3. 512 time points were simulated.

Simulation: Magnetization Courses To investigate the T1-dependency of a conventional bSSFP acquisition, of a T2-weighted TSE acquisition and of the proposed RA-TOSSI acquisition, simulations based on the Bloch equations (22) were performed for four T2-values (T2 ¼ 60/80/100/500 ms), depicted in different colors. As shown in Figure 3, each T2-value was combined with four T1-values (T1 ¼ 750/1000/1500/2000

Sequence Implementation: Golden Angle View Ordering Scheme As the proposed RA-TOSSI concept is based on radial k-space sampling, an appropriate view ordering scheme has to be chosen. While a sequentially increasing projection angle yields optimal uniform sampling of k-space, this common scheme does not allow the use of view-

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Table 1 Measurement Parameters and Results of the SNR/CNR Analyses for the Images Shown in Figure 5a Quantity

RE-TOSSI

TSE

RA-TOSSI

bSSFP

Acquisition time Generated contrasts TR Receiver bandwidth Flip angle Image weighting Ghosting artifacts SNR WM SNR efficiency WM CNR WM-GM CNR efficiency WM-GM

1.3 s 1 4.7 ms 700 Hz/px 40 T2 middle 26.0 22.8 7.7 6.7

1:56 min 1 3000 ms 130 Hz/px 180 T2 low 70.0 6.5 74.1 6.9

1.3 s 128 4.7 ms 700 Hz/px 40

1.2 s 1 4.7 ms 700 Hz/px 40 T2/T1 none 14.2 13.0 7.8 7.1

T2 none 26.1 22.9 11.1 9.7

T2/T1 none 16.7 14.6 6.9 6.1

a

Because the T2-weighted RE-TOSSI and RA-TOSSI images are not acquired in the steady-state but in the transient state, where the overall signal is higher, the corresponding values must not be compared with the values obtained for the T2/T1-weighted images.

sharing techniques. To overcome this, the projections can be acquired in an interleaved manner (24). However, this method only yields valuable results for a predetermined number of acquired spokes. Using golden angle view ordering instead distributes the projections quasirandomly (25) and is hence beneficial for view sharing techniques. The used constant azimuthal angle increment of 111.246 guarantees a near-optimal k-space sampling independently from the number of acquired projections.

Data Processing In radial MRI, every projection traverses the contrast defining k-space center. As a consequence, a straightforward reconstruction of a k-space acquired with RATOSSI would result in some undesired mixed contrast, containing both T2-weighting from the TOSSI block and T2/T1-weighting from the bSSFP block. One of the advantages of radial imaging is the fact, that the inner regions of k-space are intrinsically oversampled. Therefore, the Nyquist criterion in this area will still be fulfilled, if only a subset of the acquired projections is used. This can be exploited to reconstruct multiple images out of one single-shot measurement. By performing a view-sharing technique such as a k-space weighted image contrast (KWIC-) filter (26), the central region of kspace is filled with only a limited number of projections. The mean acquisition time points of these projections define the TEeffTOSSI value of the resulting image. When moving further out in k-space, adjacent projections are chosen from time points further away. Hence, the Nyquist criterion will be fulfilled for the complete kspace. In the used implementation, five projections are chosen for the k-space center and this number is increased gradually by steps defined by Fibonacci numbers (27). In that way, several image contrasts can retrospectively be reconstructed out of one dataset by moving this k-space filter analogous to a sliding window reconstruction by a certain number of projections (e.g. two) along the acquired spokes. To account for the nonuniform sampling of k-space due to the used radial trajectory, an iteratively computed density compensation function (28) was applied on the

KWIC-filtered radial projections. Final image reconstruction was then performed using the NUFFT algorithm from the toolbox by Fessler and Sutton (29). To reduce streaking artifacts and to enhance SNR, a principal component analysis (PCA) was applied. Performing singular value decomposition as basis transformation along the KWIC-filtered time series, components contributing mainly noise or streaking can be removed to improve image quality retrospectively (30). The entire reconstruction process is schematically shown in Figure 1b. In all (RA-) TOSSI experiments, data in the antiparallel state were multiplied with 1.0 with regard to the inverted magnetization vectors. In Vivo Experiments In vivo experiments were performed on clinical 3.0T MR scanners (Magnetom Skyra and Magnetom Trio, Siemens Healthcare, Erlangen, Germany). Before the imaging sessions, written informed consent was obtained from each volunteer and the patient, respectively. A constant value of R ¼ 24/8 was chosen for the ratio R ¼ TP/TA, which was optimized for target values around T2 ¼ 60–100 ms. Image reconstruction was performed in Matlab 2013b (The MathWorks, Natick, MA). T2- and T2/T1-Weighted Brain Experiments Brain images were acquired using a 12-channel head coil array. Unless stated otherwise, the imaging parameters were as follows: FOV ¼ 220  220 mm2, slice thickness ¼ 5 mm, readout points ¼ 256, resolution ¼ 0.9  0.9 mm2. A RA-TOSSI measurement with l ¼ 0.3 was performed acquiring 256 projections. After the last inversion pulse, magnetization was located in the parallel state (even number of inversion pulses). In total, 128 images with different TEeffTOSSI (TEeffTOSSI 6¼ TEeffTSE according to Schmitt et al) (12) using three principal components were extracted. As a reference, additional Cartesian measurements were performed, including a RE-TOSSI acquisition (l ¼ 0.3), a T2-weighted TSE acquisition (TR/TE ¼ 3000/87 ms, echo train length (ETL) ¼ 7) and a conventional bSSFP acquisition. Corresponding parameters are listed in Table 1. In the case of

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conventional bSSFP, 200 dummy RF-pulses preceded the acquisition to account for contrast influences due to the transient state (31). To investigate the SNR and contrast-to-noise ratio (CNR) behavior of these methods, multiple noise maps based on measured noise covariance matrices were used to perform 100 repetitions of the reconstruction process (32). Pixel-wise SNR values were obtained by dividing the mean pixel intensity by its standard deviation. By normalizing the SNR and the CNR by the square-root of total acquisition time, the SNR efficiency and the CNR efficiency, respectively, was calculated. To estimate the SNR and CNR in white and gray matter, regions of interest (ROIs) consisting of 72 pixels were drawn and the containing values of the calculated SNR maps were averaged within these regions. Brain Experiments with Multiple Species Attenuated To demonstrate the second variant of RA-TOSSI, where magnetization after the last inversion pulse is located in the antiparallel state (odd number of inversion pulses), 768 projections were acquired with l ¼ 0.16. Imaging parameters were as follows: matrix size ¼ 256, resolution ¼ 0.9  0.9 mm2, slice thickness ¼ 5 mm, readout bandwidth ¼ 700 Hz/px, TR ¼ 4.7 ms, total acquisition time ¼ 3.8 s. A total of 384 images were reconstructed including five principal components to account for the increased dynamics in the signal courses (see Figure 2b). For comparison, the same measurement and reconstruction was repeated with magnetization located in the parallel state after the last inversion pulse (l ¼ 0.18). Finally, a single-slice image with fluid attenuation was obtained by using a conventional FLAIR TSE protocol with identical resolution and the following parameters: TR/TE ¼ 9000/87 ms, ETL ¼ 16, inversion time (TI) ¼ 2500 ms, total acquisition time ¼ 2:35 min. Patient Measurement As a clinical showcase, a patient with intra-axial low-grade astrocytoma was measured with a 32-channel head coil array. Again, both RA-TOSSI variants were applied, acquiring 768 projections with l ¼ 0.16 and l ¼ 0.18, respectively. The following parameters were used: FOV ¼ 220  220 mm2, matrix size ¼ 256, resolution ¼ 0.9  0.9 mm2, slice thickness ¼ 5 mm, readout bandwidth ¼ 630 Hz/px, flip angle ¼ 40 , TR ¼ 4.7 ms. For each measurement, total acquisition time was 3.8 s and 384 images were extracted including four principal components. Abdominal Experiments For the abdominal measurements, an axial slice was acquired during free breathing using an 18-channel body coil array in combination with a 24-channel spine coil array. The following imaging parameters were used: flip angle ¼ 34 , TR ¼ 4.1 ms, receiver bandwidth ¼ 1085 Hz/ px, slice thickness ¼ 5 mm. A FOV of 360  360 mm2 and a matrix size of 256 resulted in a resolution of 1.4  1.4 mm2. RA-TOSSI (l ¼ 0.23) was applied to acquire 512 radial projections. Magnetization after the last inversion pulse was located in the parallel state. In total, 256 images were reconstructed using two principal components. Total acquisition time was 2.3 s. For comparison,

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a Cartesian RE-TOSSI measurement (l ¼ 0.3) as well as a Cartesian bSSFP measurement (preceded by 400 dummy RF-pulses) was performed. In these cases, 256 phaseencoding lines were acquired, resulting in acquisition times of 1.2 s and 2.7 s, respectively. All other parameters were held constant. Finally, a T2-weighted singleshot HASTE acquisition was performed (TR/TE ¼ 3000/ 68 ms, receiver bandwidth ¼ 592 Hz/px, partial-Fourier factor ¼ 5/8, parallel imaging acceleration factor R ¼ 2). RESULTS Simulation: Magnetization Courses Figure 3 demonstrates the magnetization time courses of the simulated sequences. Using conventional bSSFP (Fig. 3a), each combination of relaxation times follows a different magnetization course. This is illustrated by the graph in the right hand column: here, the signals of the different T1-values at one time point (indicated by the dashed line) are plotted against the simulated T2-values. If longitudinal relaxation had no influence on the magnetization time course (pure T2-weighting), all different T1-values (circles) would yield the same signal for identical T2-values. As expected, this is not the case for conventional bSSFP. For comparison, Figure 3b shows the magnetization time courses obtained with a TSE sequence. Simulation parameters in this case were TR/TE ¼ 6000/91 ms. Because this sequence is strongly T2-weighted, nearly no T1-influences can be seen. While it has been shown that (RE-)TOSSI based on a varying ratio R yields good results in practice (13), this scheme can be difficult to implement on a clinical scanner (12). To allow the straightforward implementation of (RA-)TOSSI independently from the used scanner type, a nonideal, constant ratio can be used (12) as shown in Figure 3c. With this approach, a sufficient separation of the respective signal courses can still be achieved. Therefore, this scheme seems to be a reasonable tradeoff to obtain robust T2-weighted TOSSI images and will be used throughout this work. T2- and T2/T1-Weighted Brain Experiments Figure 4 shows results from the brain measurements acquired with RA-TOSSI. The top row demonstrates the influence of the PCA postprocessing. While Figure 4a was obtained without this additional step, Figure 4b shows the corresponding image, where only the first three principal components were included. Residual artifacts (solid arrow) are significantly reduced, while contrast and image details on the visual scale remain unchanged. A plot containing the first four eigenvalues is shown in Figure 4c. As can be seen, already the third eigenvalue is almost zero and therefore, the respective principal component hardly contains valuable information. Figures 4d–f show additional exemplary images of the image series. The images extracted from this singleshot measurement reveal different contrasts, including moderate T2-weighting (Fig. 4d), strong T2-weighting (Fig. 4e), and T2/T1-weighting (Fig. 4f). The comparison between results obtained with the proposed RA-TOSSI technique and conventional RETOSSI, TSE and bSSFP acquisitions are shown in Figure 5. Corresponding T2-images are shown in the top row,

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FIG. 4. Brain measurements with RA-TOSSI: The same contrast is shown without (a) and with (b) PCA postprocessing. Artifacts (solid arrows) could be significantly reduced. c: First four eigenvalues. d–f: Other contrasts extracted from the single-shot RA-TOSSI measurement. The TEeffTOSSI value indicates the acquisition time point of the projections which were used for the k-space center of the corresponding image. Banding artifacts due to susceptibility differences can be seen close to the frontal sinus (dashed arrows).

while T2/T1-images are depicted in the bottom row. As can be seen, RA-TOSSI achieves similar T2-contrast on the visual scale to both RE-TOSSI and TSE. While ghosting artifacts are visible in the RE-TOSSI image (especially at the top and bottom side of the brain, solid arrows), corresponding streaking artifacts do not appear with RATOSSI. To compare these findings analytically, SNR and CNR values are listed in Table 1. While TSE clearly outperforms the other methods regarding SNR in white matter and CNR between gray and white matter, this is not the case, if SNR and CNR efficiency are considered. In this case, the best results are obtained with RA-TOSSI. The images reveal the different visualization of flow between bSSFP based techniques and TSE. While vessels (black arrows) appear bright with RA-TOSSI, RE-TOSSI, and bSSFP (33), they appear dark and are, therefore, highlighted with TSE (34). Brain Experiments with Multiple Species Attenuated Figure 6 shows results for the RA-TOSSI variant, where magnetization after the last inversion pulse is located in the antiparallel state (odd number of inversion pulses). Different contrasts of the KWIC-filtered image series are

shown, including a T2-weighted image (Fig. 6b), an image with white matter cancelled (Fig. 6c), with gray matter cancelled (Fig. 6d), and with CSF cancelled (Fig. 6e). Figure 6a shows a T2-weighted image obtained with the conventional RA-TOSSI variant (even number of inversion pulses). Compared with Figure 6b, contrast is similar, but differences regarding the visualization of blood vessels (dashed arrow) are visible: while these small structures can clearly be seen in the images with tissue types attenuated, they do not appear within the conventional RA-TOSSI image. Furthermore, fat appears darker when using an odd number of inversion pulses, because the corresponding signal values are located near the zero-crossing. Figure 6f shows the result obtained with the FLAIR TSE protocol. Cancellation of fluid and contrast between gray and white matter are similar to the level in the RA-TOSSI image, while vessels and fat appear differently. Additionally, flow artifacts (solid arrow) only occur in the FLAIR TSE image. Patient Measurement Results obtained in the brain tumor patient are shown in Figure 7. Using the variant with an even number of

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FIG. 5. Comparison of different techniques: The top row shows T2-weighted images acquired with RA-TOSSI, Cartesian RE-TOSSI and TSE. While contrasts are similar, artifacts appearing in the RE-TOSSI image (solid arrows) cannot be seen with the proposed technique. Differences regarding the visualization of vessels are indicated with black arrows. In the bottom row, a T2/T1-weighted image extracted from the same RA-TOSSI measurement is compared with a conventional bSSFP image, revealing almost identical contrasts. Again, banding artifacts (dashed arrows) appear in all bSSFP-based techniques.

inversion pulses, the tumor can clearly be traced in the T2-weighted image (Fig. 7a), while it is less visible in the T2/T1-weighted image (Fig. 7b). By using the variant with an odd number of inversion pulses, different contrasts can be reconstructed, including a T2-weighted image (Fig. 7c) and images with several species attenuated (Figs. 7d–f). While cancellation of CSF does not accentuate the tumor, the other images allow a clear differentiation between affected tissue and both gray and white matter. To visualize the difference regarding the magnitude signal courses of the two RA-TOSSI variants, pixels in CSF, white matter, gray matter, and tumor were chosen. For these points, the corresponding signal values were extracted for each frame of the entire KWIC-filtered image series. In Figure 8a, the results are shown for the conventional RA-TOSSI variant. Similar to the simulations (Fig. 2a), magnetization first decays due to T2-relaxation in the TOSSI block and subsequently recovers during the bSSFP block. This holds true when magnetization after the last inversion pulse is located in the antiparallel state. The key-feature here is that magnetization additionally crosses the zero-point during recovery (Fig. 8b), allowing the retrospective cancellation of different tissue types. This corresponds to the situation in Figure 2b.

Abdominal Experiments Results from the abdominal measurements are shown in Figure 9. The image quality obtained with RE-TOSSI is severely degraded due to ghosting artifacts. As these artifacts do not appear in the bSSFP image, motion can be excluded as a potential source. Rather, these artifacts most likely originate from the Cartesian trajectory in combination with the oscillating off-resonant fat (12) and the constant TP/TA-ratio. Corresponding streaking artifacts in the RA-TOSSI image are effectively suppressed by PCA postprocessing. Both the T2-weighting and the T2/T1-weighting extracted from the RA-TOSSI measurement resembles the contrast achieved with HASTE and bSSFP. DISCUSSION The conventional acquisition of T2-weighted images using TSE can be very time consuming, at least when single-slice measurements are performed. However, by using unequally spaced inversion pulses within a bSSFP sequence, very similar contrasts can be obtained in a fraction of scan time (12,13). Here, an expansion to this existing concept was proposed. By using a radial trajectory with KWIC-filter reconstruction, each projection traverses the contrast defining k-space center and therefore,

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FIG. 6. a: T2-weighted image acquired with conventional RA-TOSSI (even number of inversion pulses). b–e: Results with predefined species attenuated obtained from a single-shot brain measurement using the proposed alternative RA-TOSSI variant (odd number of inversion pulses). Depending on the underlying TEeffTOSSI value, different species can be cancelled. The corresponding T2-weighted images (a) and (b) reveal similar contrast. However, small vessels (dashed arrow) appear different. f: FLAIR TSE image, showing similar cancellation of fluid and contrast between gray and white matter compared with the result obtained with RA-TOSSI. Artifacts due to flow (solid arrow) cannot be seen in the RA-TOSSI images.

an image series with multiple TEeffTOSSI can be reconstructed out of one single-shot dataset. As a consequence, no specific reordering scheme has to be chosen and the desired contrasts can be selected retrospectively. Due to the off-resonant behavior of fat and the oscillating magnetization in TOSSI, the corresponding point spread function is considerably widened and ghosting artifacts can severely degrade image quality when a Cartesian trajectory is applied (12). While this could be improved with RE-TOSSI, residual artifacts can still occur, which are acceptable in the brain images (Fig. 5), but seriously degrade abdominal images (Fig. 8). A possibility to overcome this problem is the implementation of fat saturation and a varying TP/TA-ratio as used in the previously proposed RE-TOSSI implementation (13), which seems to be necessary at least for body imaging. However, in radial MRI, this problem is intrinsically mitigated. Because no predefined phase-encoding direction exists, ghosting artifacts, which are usually manifested in this direction, are distributed over the complete image and appear as streaking artifacts. While the character of these artifacts is already less severe, they are fur-

ther reduced by PCA postprocessing. Therefore, images with high quality can be obtained by using a radial trajectory combined with a constant TP/TA-ratio and the proposed reconstruction scheme. Of course, the combination of a radial trajectory with fat saturation and a nonconstant TP/TA-ratio is also possible and could further improve image quality. Similar to RE-TOSSI, the proposed concept possesses several benefits compared with existing bSSFP techniques that are also capable of producing images with T2weighting. Using a T2-preparation module at the beginning of the acquisition (7–10) comes along with a reduced SNR. Additionally, no data can be acquired during the time consuming preparation period and the desired contrast only is apparent at the beginning of image acquisition. In T2-TIDE, a TSE pulse train consisting of a 90 RF-pulse and subsequent 180 pulses is played out at the beginning of the acquisition. During this T2-contrast generating period, the k-space center is acquired. Thereafter, the flip angle is ramped down and the residual k-space is acquired with conventional bSSFP (11). However, many 180 pulses have to be

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FIG. 7. Results obtained in a patient with intra-axial low-grade astrocytoma in the left supramarginal gyrus: T2-weighted image (a) and T2/T1-weighted image (b) acquired with conventional RATOSSI (even number of inversion pulses). c–f: Images extracted from the RA-TOSSI variant using an odd number of inversion pulses. By choosing different values for TEeffTOSSI, the differentiation between tumor (arrow) and healthy tissue may be increased considerably.

applied to obtain the desired contrast. In combination with the relatively high flip angles used for bSSFP imaging, this can be prohibitive in terms of SAR, especially when moving to higher fields (3.0T and above). Furthermore, similar to TSE or HASTE, the signal decay during this period is significantly faster than the decay during the TOSSI block, therefore potentially increasing blurring. Nevertheless, the proposed combination consisting of a radial trajectory in combination with a KWIC-filter reconstruction could be applied to T2-TIDE as well, therefore, also yielding T2-contrasts as well as T2/T1-contrasts out of one single-shot experiment. The position of the last inversion pulse in RA-TOSSI strongly influences the signal evolution and hence the resulting image contrasts. When magnetization in the

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last TOSSI segment is located in the parallel state (even number of inversion pulses), the bSSFP steady-state is subsequently approached in a short time. This variant can be used to extract several T2-weighted TOSSI images as well as T2/T1-weighted bSSFP images out of one single-shot dataset. However, by starting the bSSFP block when magnetization is located in the antiparallel state (odd number of inversion pulses), signal time courses pass the zero-point. This has several consequences. Besides images with T2-weighted TOSSI contrasts, images with multiple species attenuated can be reconstructed. However, comparing T2-weighted TOSSI images obtained with both variants, image quality as well as SNR is better for the conventional implementation. This can be explained by the fact, that the use of the RA-TOSSI variant with zero-crossing yields several projections around this point, which contribute only low signal to the resulting image and therefore degrade overall image quality. Another difference between the two RA-TOSSI variants is the visualization of blood vessels. In the variant where an odd number of inversion pulses are used, vasculature appears different compared with the surrounding tissue. This is in correspondence to other techniques which rely on inversion recovery bSSFP imaging and where magnetization is also located in the antiparallel state before the bSSFP experiment is performed (35,36). The species, where attenuation is of probably greatest clinical interest, is fluid (e.g. CSF). Because fluid is comparatively slow relaxing, the corresponding zero-crossing occurs rather late. The presented brain measurements indicated that at least 650 projections have to be acquired to be able to capture this zerocrossing. However, the exact time point TI does not only depend on T1 as during free relaxation, but also depends on the underlying T2-value as well as on the RA-TOSSI parameters R and l. Nevertheless, an exact knowledge of TI is not necessary for RA-TOSSI, because the appropriate contrast can be chosen retrospectively. While fluid is cancelled in a RA-TOSSI FLAIR image, the bSSFP T2/T1-weighting is dominant for the other species, because most tissues have already reached their steady-state. If this RA-TOSSI variant should be used for the generation of a conventional bSSFP image, many further projections would be necessary until fluid reaches its steady-state. Therefore, this combination between the two proposed variants is definitely possible, but seems to be rather ineffective due to relatively long acquisition times. In general, RA-TOSSI with an even number of inversion pulses can be seen as a TOSSI/bSSFP combination and RA-TOSSI with an odd number of inversion pulses equals a TOSSI/Inversion-Recovery (IR) bSSFP combination. While images with predefined tissue types cancelled can also be straightforwardly extracted from an IR bSSFP experiment (36), the generation of clinically relevant T2-contrasts is more complicated, because it is based on pixel-wise fitting (27,37) and subsequent synthetically calculation (38). However, using the proposed approach, T2-weighted images can straightforwardly be reconstructed from the TOSSI section. Because RA-TOSSI is based on a bSSFP sequence, it is very sensitive to any imperfections regarding the

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FIG. 8. Signal time courses extracted from the RA-TOSSI image series obtained with the conventional RA-TOSSI variant (a) and with the variant where magnetization after the last inversion pulse is located antiparallel to B0 (b). As can be seen, the signal course of the tumor considerably differs from the signal courses in healthy tissue.

homogeneity of the magnetic field. Inhomogeneity of the B0-field or caused by susceptibility differences between different tissue types leads to the well-known signal voids which appear as dark bands in the image. These banding artifacts can be mitigated by properly shimming and the use of short TRs (1). If these measures are not

FIG. 9. T2-weighted (left hand column) and T2/T1-weighted (right hand column) free breathing abdominal measurements. Except for the RE-TOSSI image, good image quality is achieved with all used methods. While contrast between liver and kidneys is different in the left hand column, it appears similar in the right hand column, therefore violating T2-weighting. Compared with RATOSSI, spatial resolution is slightly degraded in the HASTE image (dashed arrow). Because proper shimming in the abdomen is difficult to achieve, banding artifacts (solid arrows) can be seen despite the used short TR value of 4.1 ms.

sufficient, separate images with different phase-cycles may be acquired and combined (39). At the expense of increased scan times, this method allows the robust cancellation of banding artifacts and can also be used for RA-TOSSI imaging. Another source of artifacts is the used golden angle reordering scheme. The necessary

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rapid gradient switching induces eddy currents (40). Approaches like gradient pairing or through-slice dephasing (40) can avoid the accompanying artifacts and may also be implemented for the proposed method. Another point to address is the effect of transmit field inhomogeneities. While flip angle variations in the imaging plane are less severe at 1.5T, they increase when moving to higher field strengths. This directly affects the T2-weighting in the TOSSI block. Here, the flip-angle scales the overall signal and additionally alters the exponential time course, as can be directly deduced from the corresponding analytical Eq. [17] in Ref. (12). Simulations (not shown) indicate for example, that the obtained contrast can differ considerably when the flip-angle is varied. However, when using the proposed variant where an odd number of inversion pulses are applied, the ability to cancel different species seems to be more robust. Measurements (not shown) reveal that the retrospectively chosen echo time TEeffTOSSI does not need to be adapted when varying the flip angle within a certain range. All shown experiments were performed as single-slice 2-dimensional measurements. However, due to the used selective adiabatic inversion pulses, an extension to multi-slice measurements is straightforward (41). CONCLUSIONS The existing (RE-)TOSSI concept has the potential to rapidly generate T2-weighted images. Here, this technique is extended by using a radial trajectory, allowing the extraction of several contrasts out of one single-shot measurement with no expense of scan time or image quality. These contrasts include different T2-weighted TOSSI images as well as T2/T1-weighted bSSFP images. Additionally, a novel variant is presented allowing the generation of images with multiple species attenuated. Therefore, the proposed RA-TOSSI approach significantly increases the efficiency and the possibilities of (RE-) TOSSI imaging. Together with its short acquisition times, RA-TOSSI is a versatile and promising candidate for clinical practice. ACKNOWLEDGMENTS The authors thank Siemens Healthcare (Erlangen, Germany) for technical support and the Bavarian Ministry of Economic Affairs, Infrastructure, Transport and Technology (BayStMWIVT) for financial support. REFERENCES 1. Scheffler K, Lehnhardt S. Principles and applications of balanced SSFP techniques. Eur Radiol 2003;13:2409–2418. 2. Plein S, Bloomer TN, Ridgway JP, Jones TR, Bainbridge GJ, Sivananthan MU. Steady-state free precession magnetic resonance imaging of the heart: comparison with segmented k-space gradientecho imaging. J Magn Reson Imaging 2001;14:230–236. 3. Gold GE, Hargreaves BA, Reeder SB, et al. Balanced SSFP imaging of the musculoskeletal system. J Magn Reson Imaging 2007;25:270–278. 4. Mikulis DJ, Roberts TPL. Neuro MR: protocols. J Magn Reson Imaging 2007;26:838–847. 5. Hennig J, Nauerth A, Friedburg H. RARE imaging: a fast imaging method for clinical MR. Magn Reson Med 1986;3:823–833. 6. Stark DD, Hendrick RE, Hahn PF, Ferrucci JT. Motion artifact reduction with fast spin-echo imaging. Radiology 1987;164:183–191.

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