Measurement of T₁ and T₂ relaxation times of the pancreas at 7 T using a multi-transmit system

Magnetic resonance (MR) imaging is an imaging modality with good soft tissue contrast and high sensitivity for detection of pancreatic cancer, which facilitates early tumor detection [1, 2]. Modern MRI techniques can visualize biliary and pancreatic ductal systems noninvasively, have a high sensitivity for tumor detection, and, unlike endo-ultrasound imaging (EUS) with high sensitivity (up to 89%) and specificity (up to 99%) for detection of small-tumor pancreatic cancer [3‐5], reveal the pancreatic three-dimensional anatomy, possible invasion into surrounding tissue or vascular involvement [6]. However, it is still difficult to distinguish chronic pancreatitis and pancreatic carcinoma using T₁-weighted and/or T₂-weighted MR images on 1.5 and 3 Tesla (T) [7], even when gadolinium contrast agents are used [8].

Higher magnetic field strengths, such as 7 T, offer higher signal-to-noise (SNR) and contrast-to-noise ratios (CNR), as well as higher spatial and spectral resolutions [9]. However, artifacts are more profound at higher field strengths, particularly in the abdominal region, mainly due to the reduced wavelength in the body that leads to an inhomogeneous B₁⁺ field distribution and signal voids [10, 11]. In addition, the local specific absorption rate (SAR) increases with increasing field strength [12], leading to longer repetition times needed and thus longer acquisitions. Using a multi-transmit system, the B₁⁺ efficiency can be optimized within a region of interest (ROI). This can be achieved by optimizing the transmit phases for each channel in the body coil. As a result, improved local B₁⁺ homogeneity and magnitude can be achieved [10].

In addition to the technical challenges that MRI at higher magnetic field strengths brings, high-quality diagnostic imaging of pancreatic cancer requires development and optimization of imaging protocols. Moreover, a new baseline assessment of the images obtained at ultra-high field is required. Therefore, knowledge of relaxation times (T₁ and T₂) is essential. These characteristics are known to change substantially with field strength and this change cannot be predicted accurately with theoretical calculations due to the complex tissue behavior [13]. Consequently, although T₁ and T₂ values have been well established for many tissues, including pancreatic tissue at 1.5 T and 3 T [14‐16], T₁ and T₂ relaxation times of pancreatic tissue at 7 T remain unknown.

The purpose of this study was to determine the mean T₁ and T₂ relaxation times of healthy pancreas parenchyma over a wide age range at 7 T to assess baseline levels to develop optimized imaging protocols at this magnetic field strength.

Out of 26 subjects, 22 T₁ and 23 T₂ datasets could be used for further analysis. The discarded datasets had insufficient image quality, caused by motion or not enough B₁⁺ amplitude in the pancreas region. Average age of the subjects was 37 years (range 21–72 years) for the T₁ datasets and 40 years (range 24–72 years) for the T₂ datasets.

T₁ relaxation times (mean ± std) for all 22 subjects are summarized in Fig. 2, the average T₁ relaxation time was 896 ± 149 ms. An example of an B₁⁺ map is shown in Fig. 3, the mean ratio of the measured B₁⁺ over the expected B₁⁺ value in the ROI across the subjects was 0.92 ± 0.14. Linear regression analysis showed no correlation between age and T₁ relaxation time (slope = 1.1, offset = 856, R² = 0.01, p = 0.6).

Using method (1) (T₂-weighted image series with a 180° refocusing pulse) and (2) (using STEAM spectroscopy) for T₂ determinations gave an average T₂ relaxation time of 28.1 ms (n = 3) and 25.6 (n = 4), respectively. An unpaired t test proved no significant difference (p = 0.6) between the results of the two methods. Combining these results as a reference value gave an average T₂ of 26.7 ± 5.3 ms.

Method (3) resulted in a lower average T₂ relaxation time of 19.5 ± 3.8 ms (n = 16) as expected due to the lower refocusing angle used. Fitted T₂ relaxation times for all 23 subjects are summarized in Fig. 4. No correlation between age and T₂ relaxation time was found (slope = − 0.1, offset = 31, R² = 0.2, p = 0.07). Figure 5 shows examples of the mono-exponential fits for all three methods, with the signal of the first acquisition normalized to 1, for three single subjects.

Multi 2D T₂-weighted single-shot turbo spin-echo images FA 90°, refocusing flip angle 35°, TE 80 ms (TE_equiv = 31 ms), TR 10 s, TSE factor of 121, SPAIR fat suppression, voxel size of 1.5 × 1.5 × 5 mm³ (Fig. 6) were obtained. TE_equiv close to the average T₂ relaxation time of pancreas and TR more than 5 times longer ( ~ 11 times longer) than the average T₁ relaxation time for improved contrast. The full field of view of the pancreas can be covered. However, signal voids can be still observed outside the region of interest (not B₁⁺ optimized region), which are more pronounced in spin-echo-based sequences.

In this study, we determined normal pancreas T₁ and T₂ relaxation times in 26 healthy subjects aged 21–72 years at 7 T. T₁ and T₂ relaxation times for pancreas at 7 T—to our knowledge—have not been reported before. However, they have been reported for pancreas in healthy subjects at 1.5 T and 3 T. In the literature, it can be found that T₁ relaxation times increase and T₂ relaxation times decrease with increasing field strengths [13, 23]. De Bazelaire et al. [13] used an inversion recovery method and different inversion times for T₁ measurements and a multiple spin-echo (SE) technique with different echo times for T₂ measurements in six healthy subjects, reported T₁ values of 584 ± 14 ms for 1.5 T and 725 ± 71 ms for 3 T and T₂ values of 46 ± 6 ms for 1.5 T and 43 ± 7 ms for 3 T, and concluded that pancreas T₁ relaxation times increased and T₂ relaxation times decreased with increasing field strength. Tirkes et al. [23] reported a mean T₁ relaxation time of 797 ms at 3 T for healthy pancreas (n = 53, sequence: dual flip angle 3D gradient echo). A slightly higher mean T₁ of 987 ± 52 ms and mean T₂ of 50 ± 3 ms at 3 T was reported by Chhor et al. [15] (n = 6, sequence: Look-Locker for T₁ and T₂-prep for T₂ measurements). Our 7 T results confirm the expected trend of increasing T₁ and decreasing T₂ relaxation times with age.

In addition, T₁ and T₂ values are dependent on tissue composition [24]. In this study, we did not investigate tissue differences between subjects. Therefore, we could not confirm this at 7 T. Tirkes et al. [23] also found a weak correlation between age and T₁ relaxation time in the pancreas at 3 T, which we could not observe in our measurements at 7 T. The relatively young mean age of them could explain the lack of correlation (if any).

The use of standard TSE sequences attenuates the effect of molecular diffusion by the use of multiple refocusing pulses, the effect becoming stronger as the refocusing pulses get closer to each other [14, 24]. In addition, differences in imaging methods and determining T₂ relaxation times, a more than doubled magnetic field strength, different age ranges, and the morphology of each subject, combined with the complex characteristics of tissues, may be responsible for the large decrease of T₂ relaxation time found at 7 T.

For T₁ measurements, a Look-Locker sequence is generally used with a TR (including the 6 s per cycle) of more than 5 times the T₁ value of pancreas tissue, which is required to measure the T₁ value accurately. Using T₂-weighted imaging with full 180° refocusing angle and magnitude signals to fit the water peaks from the MR spectroscopy measurements, T₂ relaxation times for pancreas could be correctly determined. A spin-echo sequence such as the one used here in method (1) is not practical to use in such large groups of subjects. The high SAR deposition in the body due to the large refocusing angles requires long repetition times leading to long scanning times, to keep SAR under the guideline levels. Since the mentioned SAR levels was the worst-case possible SAR and it is known that the dipole array will never exceed a local SAR of 10 W/kg when driven at a time averaged power of 3 W per channel driving all eight antennas at any phase setting, the SAR could be overestimated but were always within (conservative) limits. In addition, there are hardware limitations associated to these high-power demanding sequences. T₂ imaging with a small refocusing pulse ensures a more practical sequence; with shorter scan times and lower SAR levels. However, T₂ imaging with a 35° refocusing pulse is affected by T₁-weighted stimulated echoes during the signal formation [25], which leads to a lengthening of the signal-intensity decay. This resulted in longer T₂ relaxation times, which after correction with the equivalent echo times (to a 180° refocusing angle), resulted in slightly lower T₂ relaxation values and a comparable variability to the results found with the nominal 180° refocusing pulse and the spectroscopy data, as was seen in Fig. 4. No other explanation could be found for the underestimation of the results of method (3). Age-dependency testing using data from method (3) is, therefore, only suitable for assessing the relative differences of T₂ of the pancreas with respect to age.

Inter-subject variability in the measured relaxation times can be caused by different factors. Variations within characteristics of (pancreatic) tissue, and their change with age were different for individuals, even between men and women (which we did not take into account). As Sato et al. [16] describes in their paper, the pancreas changes with increasing age; characteristic changes with age are pancreatic atrophy, lobulation and fatty degeneration. These changes, such as the fraction of fat in the pancreas would lead to altered relaxation times.

Results were fitted over scans with different echo times since a single sequence with multiple echo times given by the turbo factor resulted to be too sensitive to motion and breathing artifacts that would result in blurring of the image. This leads to slight differences in anatomy position between echo times. Therefore, the delineated ROIs did not correspond to exactly the same anatomical position, leading to outliers and a higher variation in the raw data, which can influence the fitting. In our study, data were obtained from all regions in the pancreas. Since the ROIs were drawn in the area with the best B₁⁺ homogeneity, the location was different between subjects. Tirkes et al. [23] showed a slight but not significant difference between the relaxation times measured in head, body or tail. As we have not accounted for these differences, this might have been another factor affecting the standard deviation in our calculations.

Lastly, imaging the abdomen at higher field, especially with T₂-weighted sequences, is challenging. The scans are more sensitive to artifacts given the increased B₀ and B₁⁺ inhomogeneities (even with good B₀ and B₁⁺ shimming) found at higher field strengths, leading to greater standard deviations sources.

The measured T₁ and T₂ relaxation times for pancreas at 7 T reported here is a starting point for pancreatic research at higher field strengths to improve abdominal MR imaging, and may be a base for further use of MR techniques to noninvasive pancreatic diagnostics particularly in early stages of disease.

T₁ and T₂ relaxation times of the healthy pancreas were reported for 7 T, which can be used for image acquisition optimization. No significant correlation was found between age and T₁ or T₂ relaxation times of the pancreas.