New Results

Ultrashort-T2* mapping at 7 tesla using an optimized pointwise encoding time reduction with radial acquisition (PETRA) sequence at standard and extended echo times

Carly A. Lockard, Bruce M. Damon, Hacene Serrai
doi: https://doi.org/10.1101/2024.09.05.611365

Abstract

Zero echo time (ZTE) sequences capture signal from tissues with extremely short T2* and are useful for qualitative and quantitative imaging of musculoskeletal tissues’ ultrashort-T2* components. One such sequence is Pointwise Encoding Time Reduction with Radial Acquisition (PETRA). While this sequence has shown promising results, it has undergone only limited testing at 7 tesla (T). The purpose of this work was to evaluate PETRA at 7T in its standard form and with sequence modifications to allow extended echo times for the purpose of performing ultrashort-T2* mapping.

We acquired PETRA images of MnCl2 and collagen phantoms and of the knee in eight participants (5 for optimization and 3 for ultrashort-T2* mapping assessment; 5 male/3 female, 39 ± 11 years old). Images were acquired using a 1-transmit/28-receive-channel knee coil. Artifacts, signal, signal-to-noise ratio (SNR), ultrashort-T2*, the corresponding curve fit quality, and repeatability were assessed. SNR was high in knee tissues at TE = 0.07 msec compared to a conventional-TE sequence (Dual-Echo Steady State with TE = 2.55 msec), with values ranging between 68 to 337 across the assessed tissues for PETRA versus 16 to 30 for the same tissue regions of interest in the conventional-TE series. Acquisition of series for ultrashort-T2* maps was feasible at 1.50 mm isotropic acquisition resolution and TE ≤ 0.58 msec. Strong linear correlations were observed between relaxation times and MnCl2 concentration, and between signal and collagen concentration. Ultrashort-T2* signal decay curve fit R2 and repeatability were high for phantom and knee ultrashort-T2* <1 msec.

PETRA imaging with minimal artifacts, high SNR, and scan time < 11 minutes was achieved at 7T at high (0.34 mm isotropic) resolution at TE = 0.07 msec and lower resolution (1.52 mm isotropic) at echo times ≤ 0.58 msec. Ultrashort-T2* mapping provided acceptable curve-fitting results for substances with sub-millisecond T2*.

Introduction

Conventional magnetic resonance imaging (MRI) sequences provide limited visualization of tissues with short/ultrashort T2* values, due to their inability to reduce the echo times (TE) sufficiently to acquire signal from these tissues prior to signal decay. However, ultrashort echo-time (UTE) and zero echo-time (ZTE) MRI sequences are designed to acquire signal from these tissues, enabling qualitative and quantitative evaluations. In the musculoskeletal system, UTE and ZTE imaging are particularly useful for studies of bone, tendon, calcified cartilage, meniscus, and other organs[1–10]. One ZTE sequence that has begun to be applied to these tissues is Pointwise Encoding Time Reduction with Radial Acquisition (PETRA)[3,7,11,12].

The PETRA sequence allows 3D isotropic imaging with TEs under 0.1 msec by applying the readout gradients prior to the radiofrequency pulse and combining radial half-projection filling of the outer portions of k-space with single pointwise Cartesian filling of the central portions of k-space, which are otherwise missed during the transmit/receive switching delay[6,13]. PETRA has been applied at 3T for in vivo imaging of the knee with a single TE with a focus on meniscus[11,14], cartilage[14], and the cruciate[14] and collateral ligaments[14]. PETRA has also been applied with dual-echo and inversion-based long-T2 suppression strategies[7,13]. Grodzki et al. performed in vivo imaging of the wrist, knee, and foot/ankle using two echo times (TE1 ≤ 0.07 msec, TE2 = 4.6 msec) at 1.5T to create subtraction images that highlight ultrashort-T2* tissues[13], and Li et al. performed in vivo imaging of the lower leg and foot/ankle at 3T with a focus on bone visualization by inversion-based long-T2* suppression[7]. PETRA-based spin-lattice in the rotating frame (T1ρ) relaxometry has been performed in short-T2* tissues of ex vivo bovine joint and tendon specimens and in vivo human knee and ankle tendons and ligaments at 3T[12].

The signal-to-noise ratio (SNR) benefits of UTE and ZTE sequences at 7T compared to lower field strengths have been demonstrated. Cortical bone imaging results with a 3D UTE sequence at 7T demonstrated SNR increases of 1.7 times those achieved at 3T, in spite of reduced T2* times at 7T compared to 3T[5]. Human testing of a 3D radial algebraic ZTE sequence on a scanner with dedicated high-performance hardware showed that the high SNR achieved at 7T can be used for high resolution (0.83 mm isotropic) ZTE imaging of the human wrist, knee, and foot/ankle[9]. While other ZTE imaging approaches have applied in vivo in human joints at 7T[9,15], the reported applications of PETRA at 7T in musculoskeletal and other ultrashort-T2* tissues have been limited. Other ZTE approaches tested at 7T have utilized algebraic reconstruction to fill the gap left in the center of k-space from the dead-time gap[9,15], while PETRA addresses the gap in the center of k-space using Cartesian single point (pointwise) acquisition, allowing complete filling of the center of k-space with exact values[13]. This allows greater flexibility in the dead-time length/k-space gap, whereas algebraic filling cannot be used if the gap exceeds two or three Nyquist dwells[3,16]. PETRA has been found to achieve lower levels of image artifact compared to other ZTE methods[3]. PETRA has been applied to ex vivo imaging of bovine bone specimens at 7T[3] and is available as a commercial sequence at 7T, but we are unaware of previous literature describing 7T testing and optimization in human joints. Therefore, 7T testing and optimization of the PETRA sequence is needed to evaluate image appearance and potential challenges at this higher field strength.

In addition to minimizing artifacts compared to some other ZTE approaches, the Cartesian single point k-space filling approach that PETRA uses allows image acquisition at different k-space gap sizes, corresponding to a range of TEs, as required to perform ultrashort-T2* mapping[3,13]. In addition to single-TE PETRA assessment, it would be beneficial to expand the applications of this sequence to ultrashort-T2* mapping and to assess the performance of such mapping at 7T. As mentioned above, PETRA-based T1ρ relaxometry[12] has been performed by adding a T1ρ preparation module and performing multiple scans at a series of spin-lock times. T1ρ relaxometry provides information about proteoglycan content[12]. Similarly, ultrashort-T2* relaxometry provides quantitative information about tissue degeneration or other changes, potentially related to disruption of normal collagen organization, in ultrashort-T2* tissues[17–19]. Ultrashort-T2* mapping has been shown to be particularly sensitive to tissue changes and tissue properties in ultrashort-T2* tissues such as deep/calcified cartilage[18,19], meniscus[17,20], tendon[21,22], and ligament[23,24]. However, PETRA-based ultrashort-T2* mapping has not yet been assessed.

In this work we present ultrashort-T2* mapping results using a modified PETRA sequence which allows an increased TE range of 0.07 to 0.58 msec. Using in vivo knee imaging studies, we performed an initial optimization and addressed the appearance of artifacts at the commercially available sequence settings when using the shortest achievable TE. In addition, we evaluated the feasibility of using the modified extended TE range to perform ultrashort-T2* mapping in phantom and in vivo knee images.

Materials and methods

The product PETRA sequence was modified by extending the maximum allowable TE from 0.10 msec to 1.10 msec. The increase in TE values required an increase in the size of the inner k-space portion filled with single pointwise Cartesian approach and a reduction in the outer k-space filled using radial sampling. Together, these changes increased the signal acquisition time, and therefore also the TE. We limited our maximum time for a single scan to 12 minutes for participant tolerance and determined that 0.58 was the maximum TE feasible within this scan time (details provided in the next section). The modified PETRA sequence was implemented on a 7T MAGNETOM Terra (Siemens, Erlangen, Germany) to collect phantom and knee data using a 1-transmit/28-receive-channel knee coil (Quality Electrodynamics, Mayfield Village, Ohio, USA).

Multi-echo image optimization for ultrashort-T2* mapping

The multi-echo image optimization goals included achieving the necessary levels of SNR and artifact reduction to allow ultrashort-T2* mapping within clinically feasible scan times, reported as minutes:seconds, and at the highest practically achievable spatial resolution.

In vivo knee imaging

Eight study participants were recruited between November 19, 2022 and June 15, 2024. The study was approved by the institutional review board, and written informed consent was obtained from all participants. For the initial optimization studies, five healthy participants (two male, three female, 42 ± 13 years old) were scanned using the modified PETRA sequence for initial optimization. Dielectric pads (7TNS Neuro Set, Multiwave Imaging, Marseille, France) were wrapped around the anterior and posterior surfaces of the knee. All PETRA scans used a single excitation and a flip angle of 6°, and the system transmit/receive reference amplitude was adjusted to 170 V to avoid excessive specific absorption rate. Initial imaging was performed with spatial resolutions ranging from 0.32 to 1.56 mm isotropic and TR values ranging from 3.99 to 8.28 msec. Data with and without chemical shift selective fat saturation[13] were collected to test the effect of fat suppression on data quality. Optimized parameters were selected for 1) a high-resolution series with a single short TE and for 2) a lower-resolution series that made acquisition at extended TE values up to 0.58 msec feasible, given the allowable scan time threshold of 12 minutes. The scan parameters listed in S1 Table were selected as providing the best balance between desired resolution, contrast, and scan time. For all knees, a conventional-TE DESS sequence (repetition time (TR) = 8.68 msec, TE = 2.55 msec, resolution 0.30 mm isotropic, fat suppressed) was also acquired for comparison.

Ultrashort-T2* mapping

MnCl2 phantom

A MnCl2 phantom was used to perform initial evaluation of the ultrashort-T2* mapping protocol using scan parameters based on the initial knee optimization work. The MnCl2 phantom contained ten 5 mL centrifuge tubes having 0.02 - 27.07 mM MnCl2 tetrahydrate and 30 mM NaCl in deionized water[25]. The tubes were arranged within a cylindrical plastic container sized to fit within the knee coil. Plastic supports were used to keep the tubes stationary in the central volume of the container.

Two scan sessions were performed. In the first session, the phantom was imaged with a conventional-TE DESS sequence (TR = 8.68 msec, TE = 2.55 msec, resolution 0.30 mm isotropic, fat suppressed) and with the PETRA sequence using: matrix = 96; FOV = 150mm isotropic; 29,000 radial views; voxel size = 1.56 mm isotropic; flip angle = 6°; receive bandwidth = 365 Hz/pixel; fat suppressed; TR = 7.13 msec; and TE values of 0.07, 0.09, 0.12, 0.16, 0.20, 0.24, 0.30, 0.40, and 0.50 msec. To test within-day repeatability, the TE = 0.07 and 0.50 msec scans were repeated. Acquisition time ranged from 4-5 minutes for TE = 0.07-0.40 msec and was 7 minutes for TE = 0.50 msec. The second session replicated the first session, apart from repeating the TE = 0.07 and 0.50 msec scans.

Collagen phantom

The collagen phantom contained nine 5 mL centrifuge tubes filled with water-collagen solutions having different collagen (chicken hydrolyzed collagen powder, BulkSupplements, Henderson, NV, USA) weight/volume (W/V) percentages (0, 5, 10, 15, 20, 25, 30, 35, and 40%). The tubes were arranged and supported within a cylindrical container in a similar manner to the MnCl2 phantom. The container was filled with approximately 1L of 30 mM NaCl in deionized water for coil loading.

Two scan sessions were performed, spaced six weeks apart. During both sessions, PETRA series were acquired using the following parameters: total scan time = 5:21; matrix = 160; FOV = 160 mm isotropic; 80,000 radial views; voxel size = 1.00 mm isotropic; flip angle = 6°; bandwidth = 365 Hz/pixel; TR = 4.00 msec; TE = 0.07 msec. During the first scan session, the phantom was imaged with the phantom in two physical orientations. The phantom was rotated about its long axis (which was aligned with the scanner’s z-axis for both scans) by 180° relative to its initial orientation for the second scan. This was done to test for spatial positioning effects on signal homogeneity. During the first scan session, scans with TE values 0.09, 0.12, 0.16, 0.20, 0.24, 0.30, 0.40, and 0.50 msec were also acquired to allow ultrashort-T2* mapping. Conventional T2* mapping using an axial plane multi-echo GRE sequence was also performed during the first scan session (matrix = 132×134 (264×268 interpolated); FOV = 157×159 mm; pixel size = 0.595×0.593 mm in-plane; slice thickness = 1.20 mm; flip angle = 15°; bandwidth = 600 Hz/pixel; fat suppressed; TR = 37.00 msec; TE = 1.60, 3.81, 5.82, 7.83, 9.84, 11.85, 23.00 msec).

In vivo knee imaging

PETRA imaging, using the parameters listed for the low resolution series in S1 Table and with seven TE values (0.07, 0.09, 0.12, 0.16, 0.22, 0.30, and 0.58 msec; total cumulative scan time for all TE values = 44:03), were performed in three male participants (33 ± 5 years old) with no history of knee injury to test the feasibility of performing ultrashort-T2* mapping in vivo. Ultrashort-T2* mapping repeatability data (two scans separated by 10 days) were acquired for one of these participants.

Image analysis procedures

General

For all images, 3D Slicer[26] was used to perform segmentation and MATLAB (R2024a, The Mathworks, Natick, MA) was used to measure/calculate results within the desired regions of interest (ROIs).

Image Segmentation

ROIs in the knee and image background were manually drawn in 3D Slicer by a researcher with 8 years of knee MRI segmentation experience. For all tissues except cartilage, skin, and cortical bone, the ROIs included the entire tissue of interest in at least one slice where the tissue was clearly visualized. The cartilage segmentation excluded the most medial and lateral slices, where partial volume averaging or blurring occurred. The skin and cortical bone segmentations were limited to central regions within a small set of slices, to avoid thinner tissue regions relative to the scan resolution and the resulting partial volume averaging and the blurring seen in the most medial and lateral slices. For all tissues, regions near the proximal and distal borders of the image were excluded, to avoid signal inhomogeneity near the edges of the coil’s sensitive volume.

For the phantoms, segmentation was performed using the TE = 0.07 msec images. Circular ROIs of 7 mm diameter, centered within each 15 mm diameter centrifuge tube and avoiding regions with air bubbles, were drawn in on six slices within the straight section of the tube.

Analysis of Signal Behavior

In the knee of one participant, the SNR was measured in the cortical bone, patellar tendon, posterior cruciate ligament, anterior cruciate ligament, cartilage, and skin in the fat-suppressed low resolution (1.52 mm isotropic) and high resolution (0.34 mm isotropic), TE = 0.07 msec PETRA series. The mean signal in the ROIs described above was calculated. PETRA image noise was measured by calculating the difference between two subsequently acquired identical series, and then calculating the standard deviation of the difference image divided by √2 to correct for the difference operation[27].

A custom MATLAB script was used to analyze the signal-concentration relationship at TE = 0.07 msec (collagen phantom) and to calculate the ultrashort-T2* maps using the TE = 0.07-0.50 msec data (MnCl2 phantom and knee images).

Ultrashort T2* Fitting

For the MnCl2 phantom studies, the ultrashort-T2* maps were calculated from 1.50 mm isotropic, fat-suppressed PETRA at nine different TE values (0.07-0.50 msec) using voxel-wise monoexponential fitting. A noise term was not included because of the high SNR. The coefficient of determination, R2, for the ultrashort-T2* fitting was calculated for each voxel. The median and interquartile range of the ultrashort-T2* for the MnCl2 phantom and signal mean ± standard deviation for the collagen phantom were calculated. The relationships between ultrashort-T2* and MnCl2 concentration and between signal intensity at TE = 0.07 msec and collagen concentration were evaluated.

For in vivo studies, ultrashort-T2* values were calculated using the same process described for the MnCl2 phantom, except that the 1.52 mm isotropic, fat-suppressed PETRA at seven TE values (0.07-0.58 msec) were used (due to the need for a shorter total scan time for in vivo imaging). Similar fitting with a subset of three TE values (0.07, 0.12, and 0.30 msec) was performed with the goal of enabling a reduced total scan time (16:43), thereby reducing the chances of participant motion between series and increasing the practical feasibility. In addition, in-plane frequency-domain interpolation was performed in MATLAB prior to segmentation and ultrashort-T2* fitting to allow more precise delineation of the knee structures (resulting in a sagittal-plane series interpolated resolution of 0.76 x 0.76 x 1.52 mm). Ultrashort-T2* values for which R2 was < 0.5 were excluded. The ultrashort-T2* values and R2 values were measured in the cortical bone, patellar tendon, meniscus, posterior cruciate ligament, anterior cruciate ligament, cartilage, and skin. X2 was also calculated to allow more robust comparison between goodness-of-fit between the fitting using seven TE values and three TE values.

Results

Multi-echo image optimization for ultrashort-T2* mapping

In vivo knee imaging

Fig 1 shows an example high-resolution PETRA knee image, with comparison to a dual-echo steady state (DESS) conventional TE sequence image. The PETRA images were obtained with high SNR, even for ultrashort-T2* tissues. As listed in Table 1, the SNR in the cortical bone, patellar tendon, meniscus, posterior cruciate ligament, anterior cruciate ligament, cartilage, and skin in the TE = 0.07 msec, 1.52 mm isotropic resolution, TR = 4.21 msec series ranged from 68 to 337 (total scan time, 5:20). In the 0.34 isotropic resolution, TR = 7.07 msec series (Fig 1), the same SNR measurements ranged from 23 to 75 (total scan time, 6:55). Note that the PETRA series at the two resolutions were acquired with different TR, so the SNR does not follow the usual relationship with voxel size between the two series. For comparison, the SNRs in these regions for the 0.30 mm isotropic resolution conventional-TE DESS series ranged from 16 to 30.

Fig 1.
Fig 1. Example high-resolution PETRA knee image, with comparison to a conventional-TE DESS sequence image.

Sagittal images of one participant’s knee from the fat-suppressed PETRA series at 0.34 mm isotropic resolution (A) and from the fat-suppressed dual-echo steady state (DESS) at 0.30 mm isotropic resolution (B). These images illustrate the difference in signal, and resulting differences in contrast between conventional and zero echo-time sequences, demonstrated in the patellar tendon, cruciate ligaments, and other ultrashort-T2* tissues in these images.

View this table:
Table 1. SNR measurements for PETRA at TE = 0.07 msec for knee tissue ROIs at two resolutions.

Comparing the images acquired with and without fat suppression revealed that fat suppression reduced the appearance of off-resonance artifacts and improved the visualization of short-T2* tissues (Fig 2). Images with 0.34 mm isotropic resolution were acquired in scan times of 6:55 when acquired with fat suppression and 6:00 when acquired without fat suppression. Figure 2 shows example low-resolution images acquired at TE = 0.07 and 0.50 msec and high-resolution images acquired at TE = 0.07 msec, with and without fat suppression.

Fig 2.
Fig 2. Sagittal PETRA images all acquired in a single participant knee, acquired using the parameters listed in Supplementary Table 1.

Low-resolution images acquired at TE = 0.07 msec with (A) and without (B) fat suppression, at TE = 0.58 msec with (C) and without (D) fat suppression, and high-resolution images at TE = 0.07 msec with (E) and without (F) fat suppression. Note the off-resonance artifacts appearing as double lines and thick low/high signal borders around tissue interfaces (e.g. patellar tendon-infrapatellar fat pad interface, muscle-fat interfaces, etc.).

To achieve acquisitions at longer TE values without exceeding 12 minutes per scan, the resolution needed to be set to 1.52 mm isotropic. At this resolution with 70,000 radial views and TR = 4.21 msec the scan time was under 12 minutes at TE values up to 0.58 msec (scan time = 10:55, with fat suppression).

Ultrashort-T2* mapping

MnCl2 phantom

The ultrashort-T2* measurements, ultrashort-T2* curve fit R2 values, and interscan coefficients of variation (CV) for each phantom solution ROI for two sessions are shown in Table 2. Example ultrashort-T2* curve fits are shown in Fig 3A. There was a significant linear correlation between 1/T2*ultrashort values and MnCl2 concentration (r = 0.99 and p <0.0001 for both scans), as shown in Fig 3B. Mean R2 dropped sharply for MnCl2 concentrations below 3.6 mM, and at the lowest concentration (0.02 mM) a large number of very high or even negative T2* values was calculated due to the lack of signal decay measured over the range of acquired TEs, leading to poor fit quality and the very large interquartile range for that measurement. The scan 1 and scan 2 slopes and intercepts were calculated using just the results for the solution concentrations with average R2 for ultrashort-T2* fit ≥ 0.90 (which corresponded to 5.4 - 27.07 mM, with ultrashort-T2* values of ≤ 1.1 msec). The scan 1 and scan 2 slopes were 141.77 and 135.81 seconds-1/mM (8% CV between scans), and the intercepts were 211.16 and 218.03 seconds-1 (9% CV between scans).

Fig 3.
Fig 3. MnCl2 phantom plots.

Plots showing examples of median measured (round markers) and fitted signal (dashed line) based on estimated ultrashort-T2* signal versus TE for three MnCl2 phantom solutions from two (top and bottom plots for each region) scans (a), the relationship between mean 1/T2* and MnCl2 concentration, averaged over two scans (b), the relationship between mean signal and collagen concentration at TE = 0.07 msec, averaged over three scans (c). Error bars represent the interquartile range within each subregion for signal versus TE plots and the standard deviation between scans for the 1/T2* and signal versus concentration plots.

View this table:
Table 2. Calculated ultrashort-T2* values and between-scan CV, and ultrashort-T2* fit R2 from two scans for the MnCl2 phantom.

Collagen phantom

For the collagen phantom, the mean conventional-T2* values for all W/V percentages greatly exceeded the ultrashort-T2* upper limit, being 23 msec for 40% collagen to 330 msec for 5% collagen; therefore ultrashort-T2* mapping was not evaluated. There was a significant linear correlation between collagen concentration and signal intensity in the TE = 0.07 msec images (r = 0.98 on average, p <0.0001). The individual signal measurements, linear fitting parameters, and correlation statistics are shown in Table 3. Fig 3C shows this relationship for the average of the three TE = 0.07 msec PETRA series. The between-scan and between-orientation signal and linear fitting parameter CV were all ≥ 0.05 except for 0% collagen signal (Table 3).

View this table:
Table 3. Signal measurements for each collagen concentration from three scans of the collagen phantom and the resulting signal versus concentration linear fitting parameters and correlation statistics.

In vivo knee imaging

Acquiring images with different TEs but other parameters held constant allowed creation of ultrashort-T2* maps. Fig 4 shows an ultrashort-T2* map and corresponding R2 map for one knee for two different scan sessions. Ultrashort-T2* measurements and fitting information for the cortical bone, patellar tendon, meniscus, posterior cruciate ligament, anterior cruciate ligament, cartilage, and skin are shown in Table 4. Scan-rescan results for one participant and interscan coefficients of variation are shown in Table 5. Results obtained using all seven acquired TE values and using a subset of three TE values are presented for both tables. Example T2* curves are shown in Fig 5.

Fig 4.
Fig 4. Ultrashort-T2* map and corresponding R2 map for one knee for two different scan sessions.

Example PETRA images at TE = 0.07 msec for one participant’s knee scanned in two sessions (A, F), corresponding calculated ultrashort-T2* maps in the masked ROIs in msec (B and D for scan 1 using seven and three TE values, respectively; G and I for scan 2 using seven and three TE values, respectively) and R2 maps in the masked ROIs (C and E for scan 1 using seven and three TE values, respectively; H and J for scan 2 using seven and three TE values, respectively). The R2 value threshold was set to 0.5 in all cases, with voxel ultrashort-T2* values set to 0 when R2 for the voxel was below this threshold.

Fig 5.
Fig 5. Example T2* curves.

Plots of the median measured (round markers) and fitted (dashed line) signal based on estimated ultrashort-T2* signal versus TE for the measured knee tissue regions from two scans of a single participant’s knee (10 days between scans). The plots for scan 1 are shown in rows A (signal decay curves fitted to all seven TE values) and B (signal decay curves fitted to a subset of three TE values) and the same plots for scan 2 are shown in rows C and D. Error bars represent the interquartile range within each subregion.

View this table:
Table 4. Knee tissue calculated median and interquartile range (IQR) ultrashort-T2* values, ultrashort-T2* fit R2, and ultrashort-T2* fit X2 for single scans for three participants. The results calculated using all seven TE values and the subset of three TE values are presented.
View this table:
Table 5. Scan 1 and scan 2 single-participant ROI median and interquartile range (IQR) ultrashort-T2* values and between-scan coefficient of variation (CV) calculated from the two scan sessions for one participant. The results calculated using all seven TE values and the subset of three TE values are presented.

Discussion

We modified a commercially available ZTE sequence, PETRA[13], to extend the maximum technically allowable echo time to up to 1.10 msec and demonstrate the feasibility of extended TE imaging (up to 0.58 msec) with PETRA at 7T in MnCl2 and collagen phantoms and in vivo. PETRA imaging was feasible in vivo within a clinically realistic acquisition times at high resolution (0.34 mm isotropic) at short TE values and lower resolution (1.52 mm isotropic) at the high TE values. In addition to distinguishing between tissues and tissue components with comparatively short T2* values from those with long T2* values, these modifications further allow advanced applications such as ultrashort-T2* mapping from 7T ZTE data.

Image quality indicators

Higher SNR was measured in all acquired PETRA images than in a conventional TE series at similar resolution. Fat suppression was useful for reducing off-resonance artifact. As previously described[9], coil artifact was observed in a few instances. However, it was outside of the knee volume and therefore did not impact image quality. Furthermore, near-isocenter positioning of the knee allows for minimization of lateral image blurring, as reported previously[28].

Ultrashort T2* mapping

The extension of the maximum TE allows ultrashort-T2* mapping by multiple acquisitions for substances with sub-millisecond T2* values, demonstrated here using the MnCl2 phantom and in vivo knees. The ultrashort-T2* fitting results, as quantified by R2, were excellent for ultrashort-T2* ≤ 1.1 msec. For MnCl2 samples, there was a strong significant correlation between 1/ultrashort-T2* values and concentration. Although this finding is not surprising, given the predictions of fast exchange theory, the linearity of the relaxivity plot provides an important quality verification on the T2* mapping capabilities of the sequence.

We simulated collagen-rich tissues using a collagen phantom. Although the collagen concentrations were similar to the range found in typical short-T2* tissues, the lack of collagen organization resulted in measured conventional T2* values that were longer than in the tissues of interest[29]; therefore, ultrashort-T2* mapping was not evaluated. However, we observed a strong correlation between collagen concentration and signal at TE = 0.07 msec, likely due to T1 differences between the collagen solutions. Previously reported collagen solution T1 values suggest that the expected T1 range for our 5%-40% collagen solutions would be around 1.6 – 2.6 sec at 3T[30] and somewhat longer at 7T[31–33]. The T1 values in short-T2* musculoskeletal and skin tissues with would be expected to be around 330-350 (bound water)/390-1000 (pore water) msec in cortical bone at 4.7 T[34,35], 620-700 msec in tendon at 3T[2,36,37], 819-870 msec in ligament at 3T[37], 870 msec in meniscus at 3T[37], and 1.13 sec in cartilage at 3T[37], and 820-1060 msec in dermis and epidermis of the skin at 1.5T [38], with relatively longer T1 values expected for each tissue at 7T. This range of T1 values would also be expected to create collagen-dependent signal variations in similarly configured PETRA images. While variations in other structural and compositional tissue properties would prevent across-tissue interpretation of the signal variations as reflecting collagen content, it is possible that within-tissue signal variations could be interpretable as variations in collagen content and could be associated with tissue pathology.

The median ultrashort-T2* values were generally similar between the three participants. When comparing ultrashort-T2* values calculated using seven versus three TE values we found that the median ultrashort-T2* values were lower when only three TE values were used than when seven were used (maximum TE = 0.30 msec versus 0.58 msec). This may reflect higher contributions of shorter T2* components when shorter TE values are used, with longer components contributing more to the overall measurement as a greater proportion of longer TE values are included.

For five of the seven tissues assessed, fewer voxels were excluded for poor fit when three TE values were used than when seven TE were used. The mean X2 values were lower when three TE values were used and between-scan CV was lower for all tissues except the cruciate ligaments, for which the between-scan CV was slightly higher when three TE were used but still <4%. For all tissues except cortical bone, the between-scan CV values were <14% when seven TE values were used and <10% when three TE values were used. The poor between-scan reproducibility of the cortical bone ultrashort-T2* mapping may be in part due to the thin ROI relative to the low scan resolution and potential for chemical shift artifact around the bone, and the relatively distal location of the bone ROI relative to the image volume center. Midshaft bone measurements, where the cortical bone is thicker and the bone ROI can be centered in the imaging volume, may be more reproducible. The shorter scan time, better decay curve fit, and higher between-scan reproducibility makes the three TE approach preferable for mapping of the ultrashort-T2* components. The addition of a conventional-TE T2* sequence would be necessary to capture the long-T2* components, when desired, regardless of whether three or seven ultrashort-TE values are used since the maximum TE value is < 1 msec in either case.

Ultrashort-T2* R2 values were high in the tendon, cartilage, skin, and cortical bone. For patellar tendon, the median value of 1.1 msec when seven TE were used was similar to the value of 1.57 ± 0.11 msec reported for the short T2* component in one patellar tendon sample at 7T[39]. In that study human patellar tendon samples were imaged with their long axes oriented at a range of angles relative to the main magnetic field, illustrating the impact of magic angle effect on tendon monoexponential and bicomponent T2* [39]. To minimize differences due to this magic angle effect we compared our results, which were measured at a mean patellar tendon angle of 24° ± 3° relative to the main magnetic field, to the 20° angle results from the Hager study[39]. When three TE were used, our median patellar tendon ultrashort-T2* value (0.8 msec) was lower than that previously reported value for the single patellar tendon sample imaged at 20°, but within the range reported for a set of four patellar tendon samples imaged at angles of 0° (per-tendon mean short component T2* 0.60 – 0.83 msec) and 55° (per-tendon mean short component T2* 0.93 – 1.63 msec) relative to the main magnetic field at 7T[39]. Our values calculated using three TE were of similar magnitude to those reported for short-component T2* in the Achilles tendon of healthy volunteers at 7T, which ranged from 0.20 – 0.48 msec[21]. Tendon long axis angle relative to the main magnetic field was not reported in that work, limiting comparison to the patellar tendon due to the different anatomical orientation of the tendons. We did see some non-exponential behavior in the signal decay of the tendon ROI in some cases (as illustrated in Fig 4), which may be due to partial volume averaging with adjacent adipose tissue or blurring where the tendon is too far from isocenter.

The monoexponential T2* of cartilage in uninjured and ACL-reconstruction knees, measured with a mix of ultrashort and conventional TE (TE range: 0.032 – 16 msec) at 3T, has been reported to be around 14 – 20 msec[40], and the short/long-T2* components of human cadaveric patellar cartilage by biexponential fitting (TE range: 0.08 – 40 msec) at 3T and 1st/2nd/3rd components of bovine nasal cartilage by triexponential fitting (TE range: 0.6 – 614.4 msec) at 9.4T have been reported to be about 0.50/35 msec and 2.3/25.2/96.3 msec respectively[41]. Our cartilage ultrashort-T2* values of 1.0 msec (seven TE) and 0.7 msec (three TE) were measured with a sub-millisecond maximum TE, causing a strong ultrashort component weighting, and as a result are more similar to the reported short-component biexponential and triexponential T2*values than the longer monoexponential T2* values. Ultrashort-T2* components may be more sensitive to some pathology than the long components[23].

Conventional- and ultrashort-T2* mapping has been less thoroughly explored in skin than it has been in musculoskeletal tissues, but it is of interest since skin is a high-collagen-content tissue that may be impacted alongside musculoskeletal tissues when collagen structure or function is abnormal. Skin conventional-T2*, calculated from images acquired at TE values of 2.8 – 60 msec, has been reported to be 9.8 msec at 1.5T[42,43]. Our measured value of 0.8 msec (seven TE)/0.7 msec (three TE) likely reflects only the shorter components since we only acquired images at sub-millisecond TE values.

Our cortical bone ultrashort-T2* median value of 0.7 msec (which was the same when using seven and three TE values) was similar to the previously reported bone specimen ultrashort-T2* values of 0.4 – 0.7 msec measured at 7T (TE range: 0.064 – 2.048 msec)[5] and are near the bound-water ultrashort-T2* values measured previously at 4.7T[35].

Compared to the tendon, cartilage, skin, and cortical bone, the meniscus and ligament ultrashort-T2* had lower coefficients of determination (R2 = 0.77 – 0.82 with seven TE and 0.88 – 0.92 with three TE values). The meniscus ultrashort-T2* mapping results for both sets of TE (three and seven TE) are both lower than ultrashort-T2* at 3T (7.3 msec)[20] and short-T2* values at 7T (7.31 – 9.19 msec)[44] reported previously for healthy menisci. However, our values were within the range of 0.4 – 4 msec reported previously for short-component T2* of meniscus in vitro at 9.4T[45]. Similarly, our ACL and PCL ultrashort-T2* values were lower than the previously reported values[46]. This is likely in part due to the expected reduction in T2* at 7T compared to 3T[47]. As noted above, the extent of the field strength-dependence has been shown to vary by region within tendon[21], and this may also be true in the two cruciate ligaments.

The differences between the results here for all tissues and those reported in the literature are also likely due to the difference in TE range used, where most other studies have been performed with either a single or a few ultrashort-TE and a larger number of conventional TE values (>1 msec), in contrast to our use of only ultrashort-TE values. In addition, our use of a coefficient of determination threshold for excluding poor-fit voxels is less commonly used than approaches in which voxels are excluded for having T2* or T2 values outside of an expected measurement range. In some tissues up to 60% (seven TE fitting) or up to 51% (three TE fitting) of voxels needed to be excluded due to poor fit. While the use of bicomponent exponential fitting and models with incorporation of Gaussian decay and oscillating off-resonance components have been found to improve the fit of tendon[48,49] and meniscus[45] T2* signal decay, these more complex models were not explored in this current work, as the upper range of TE values and number of TE points acquired were not sufficient to enable this more complex modeling. However, these components do likely contribute to the signal behavior and signal change between TE values. These factors, along with partial volume averaging and potential issues due to movement between series, artifact, or noise, may contribute to the poor monoexponential fit in some voxels.

Limitations

This work was limited to imaging of MnCl2 and collagen phantoms and a small number of healthy volunteers. Additional image optimization and parameter adjustment may be needed for optimized imaging of patients. The sensitivity and specificity of PETRA-based short-TE signal measurements and ultrashort-T2* mapping for quantifying tissue health remains to be assessed. The small sample size and the strong impact on ultrashort-T2* of the TE values used here limits the direct comparison between the reported values and our measurements.

PETRA’s combination of pointwise and radial sampling varies depending on TE, and this is expected to have some impact on the measured signal. Future work may be needed to assess the impact on the accuracy of PETRA ultrashort-T2* measurements.

Ultrashort-T2* mapping using PETRA does require relatively long cumulative scan time and low resolution to avoid unrealistic scan times. We found that the maximum TE needed to be restricted to 0.58 msec to avoid extremely high scan times for single scans. Bicomponent or multicomponent T2* mapping for musculoskeletal tissues would require a wider range of TE values, since long-T2* tissue suppression by subtraction imaging and quantitative ultrashort-T2* mapping require at least one TE long enough, generally >1 msec, for signal of the short-T2* tissue of interest to significantly decrease compared to the long-T2* tissue values[2,21,41]. A potential solution to the cumulative scan time with long TE values may be to fix the central portions of k-space filled by the single pointwise approach to an upper limit as function of TE. In this manner, scan time would be shortened while maintaining image resolution and SNR.

Conclusion

In this work we present the results of phantom and in vivo knee imaging using a modified PETRA sequence with an increased TE range. The results obtained are encouraging, demonstrating that following suitable image optimization, this updated PETRA sequence can provide high quality in vivo images. Furthermore, ultrashort-T2* mapping was feasible using the modified extended TE range in the phantoms and in vivo in a small sample of healthy knees. Work is in progress to reduce scan time at long TEs by setting the Cartesian central region of the k-space to an upper limit while preserving image information.

Supporting information

S1 Table. PETRA scan parameters selected as optimal for visualizing knee structures within a reasonable scan time.

Acknowledgements

We thank Dr. Dean Hoffmeister, MD, for providing input on image interpretation and clinical applications, and the Carle Illinois Advanced Imaging Center 7T MRI technologists who acquired the MR imaging data.

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Posted September 11, 2024.
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Ultrashort-T2* mapping at 7 tesla using an optimized pointwise encoding time reduction with radial acquisition (PETRA) sequence at standard and extended echo times
Carly A. Lockard, Bruce M. Damon, Hacene Serrai
bioRxiv 2024.09.05.611365; doi: https://doi.org/10.1101/2024.09.05.611365
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