T1 methods - inversion recovery (IR) spin-echo EPI, IR balanced fast field echo (bFFE), MOLLI 5(3)3, and variable flip angle mapping - are compared for the assessment of renal cortex and medulla T1. IR SE-EPI and IR bFFE allow multi-slice assessment using respiratory triggering, whilst MOLLI and VFA are collected in breath-holds. Compared with IR SE-EPI, MOLLI is in agreement (bias -53ms), IR bFFE is lower (bias -177ms) and VFA significantly overestimates T1 (bias +350ms). MOLLI T1 is shown to vary with simulated heart rate. Histogram analysis for the IR SE-EPI T1 map allows differential regions within the medulla to be separated.
Introduction
There has been recent interest in the use of longitudinal relaxation time (T1) to assess inflammation and fibrosis in renal disease1,2, changes in renal tissue T1 have been shown to occur with age and disease.3 There are a number of schemes which can be used to quantify T1, including gold standard inversion recovery (IR) spin-echo echo planar imaging (SE-EPI) for which a multi-slice dataset can be collected using a respiratory triggered acquisition4, IR balanced fast field echo (bFFE) schemes, the modified Look-Locker (LL) inversion recovery (MOLLI) method5 for which a single slice is collected on successive LL inversion recovery experiments within a breath-hold, and the variable flip angle (VFA) mapping method.6,7Methods
Five healthy volunteers (2F, age range 24-35yrs) were scanned on a 3.0 T Philips Ingenia scanner, with multi-slice balanced turbo field echo (bTFE) localiser images acquired in three orthogonal directions for planning. All data was acquired using coronal-oblique slices (2mm in-plane, 5mm slice thickness, 288x288mm FOV) with renal T1 measured using a:
(i) modified respiratory triggered IR sequence with fat suppressed SE-EPI at multiple inversion times (TI) (200-1300ms, 100ms steps and 1500ms) [5 slices, temporal slice spacing 77ms, TE 39ms, minimum TR 5s, SENSE 2.3].4
(ii) MOLLI 5(3)3 acquisition scheme with physiological simulation used to trigger the scans at 38,43,50,60 and 75 beats per minute (bpm) [single slice, FA 20⁰, SENSE 2.5, TR/TE 2.8/1.33ms, single breath-hold].5
(iii) modified respiratory triggered IR sequence with bFFE readout at multiple TIs (200-2500ms) [single slice, SENSE2, TR/TE 3/1.5ms].4
(iv) 3D-spoiled gradient-echo acquisition with VFA (2,3,4,5,6,7,10,13,20⁰) [15 slices, TR/TE 5/1.2ms, 384x384mm FOV].8
Dual-echo B0 mapping and DREAM B1 mapping sequences were collected on all subjects.
Data Analysis
The IR SE-EPI and IR bFFE schemes were fit to a standard inversion recovery scheme to generate M0 and T1 maps (Matlab). MOLLI data was fit online (Philips Medical Systems, Best NL) resulting in a fitted T1 map and confidence map indicating voxels which do not fit. Nine flip angles were used in the VFA fitting, together with the B1 map for flip angle correction (Matlab). Histogram analysis was used to assess the distribution of T1 in the renal cortex and medulla, the central slice was chosen to match the MOLLI. Renal cortex and medulla voxels were identified from the histogram and each region fit to a Gaussian function to compute the mode and FWHM.4 ANOVA was used to test for differences between T1 mapping methods.
Results
Figure 1 shows example images for each T1 method for Subject 1. Figure 2A-B show mean renal cortex and medulla T1 values across the subjects for each method. Compared with IR SE-EPI, MOLLI is in agreement (bias -53ms), IR bFFE T1 is lower (bias -177ms) and VFA significantly overestimates T1 (bias +350 ms) (Fig.2C). Figure 2D shows a signal curve for the VFA method, indicating the need for low FAs to obtain a good fit. Figure 3 shows T1 maps for each method and corresponding whole kidney histogram. All maps show clear differentiation between cortex and medulla except for VFA, as evident from the histogram. Importantly, IR SE-EPI allows differential regions within the medulla to be separated, Fig.4. Figure 5A-B show for MOLLI the variation of measured T1 with simulated heart rate. T1 is lowest for 60bpm and increases as the simulated heart rate decreases, Fig. 5C.Discussion
The MOLLI 5(3)3 scheme and IR SE-EPI yielded similar renal cortex and medulla T1 values, whilst IR bFFE underestimated T1. MOLLI T1 was affected by heart rate and in agreement with literature on phantoms and the heart,9 longer T1 values are measured at a lower simulated heart rate. The VFA method was shown to significantly overestimate T1 despite using nine flip angles in the fit and performing B1 correction, this method has previously been shown to have poor precision.10 It should be noted that often only three flip angles are used, and no B1 correction, which would result in poor precision of the fitted T1. Here we show the T1 histogram of the kidney and use this to define the renal cortex and medulla, the VFA showed poor cortico-medullary differentiation. For IR SE-EPI, the T1 histogram shows multiple peaks allowing multiple regions of the medulla to be defined.Conclusion
Close agreement was found between the IR SE-EPI and MOLLI 5(3)3 schemes for mean renal cortex and medulla T1, IR SE-EPI yielded optimal T1 multislice maps, particularly of medullary tissue.1. Friedli, I. et al. New Magnetic Resonance Imaging Index for Renal Fibrosis Assessment: A Comparison between Diffusion-Weighted Imaging and T1 Mapping with Histological Validation. Sci. Rep. 6, 30088 (2016).
2. Schley, G. et al. Multiparametric magnetic resonance imaging of experimental chronic kidney disease: A quantitative correlation study with histology. PLoS One 13, e0200259 (2018).
3. Wolf, M. et al. Magnetic resonance imaging T1- and T2-mapping to assess renal structure and function: a systematic review and statement paper. Nephrol. Dial. Transplant 33, ii41-ii50 (2018).
4. Cox, E. F. et al. Multiparametric Renal Magnetic Resonance Imaging: Validation, Interventions, and Alterations in Chronic Kidney Disease. Front. Physiol. 8, 696 (2017).
5. Messroghli, D. R. et al. Modified Look-Locker inversion recovery (MOLLI) for high-resolutionT1 mapping of the heart. Magn. Reson. Med. 52, 141–146 (2004).
6. Fram, E. K. et al. Rapid calculation of T1 using variable flip angle gradient refocused imaging. Magn. Reson. Imaging 5, 201–208 (1987).
7. Deoni, S. C. L., Peters, T. M. & Rutt, B. K. High-resolutionT1 andT2 mapping of the brain in a clinically acceptable time with DESPOT1 and DESPOT2. Magn. Reson. Med. 53, 237–241 (2005).
8. O’Connor, J. P. B. et al. Organ-specific effects of oxygen and carbogen gas inhalation on tissue longitudinal relaxation times. Magn. Reson. Med. 58, 490–496 (2007).
9. McDiarmid, A. K. et al. The effect of changes to MOLLI scheme on T1 mapping and extra cellular volume calculation in healthy volunteers with 3 tesla cardiovascular magnetic resonance imaging. Quant. Imaging Med. Surg. 5, 503–10 (2015).
10. Bane, O. et al. Accuracy, repeatability, and interplatform reproducibility of T 1 quantification methods used for DCE-MRI: Results from a multicenter phantom study. Magn. Reson. Med. 79, 2564–2575 (2018).
Figure 1
Data for Subject 1 showing the fat suppressed IR SE-EPI, MOLLI 5(3)3 scheme with a simulated heart rate of 60 beats per minute (bpm), IR-bFFE, and the variable flip angle (VFA) method.
Figure 2
Measured T1 values (mean±SEM across subjects) for each mapping method (IR SE-EPI, MOLLI 5(3)3 with heart rate 60bpm, IR-bFFE and VFA) for the A cortex and B medulla. C Bland-Altman plot of MOLLI 5(3)3 60 bpm, IR-bFFE and VFA methods against the IR SE-EPI with 95% limits of agreement shown. D Signal curves for the VFA method for renal cortex and medulla.
Figure 3
T1 maps for Subject 1 for fat suppressed IR SE-EPI, MOLLI 5(3)3 with simulated heart rate of 60 beats per minute, IR bFFE and variable flip angle (VFA) method, with corresponding histogram of measured T1 values across the kidney. The IR SE-EPI data shows clear peaks associated with the cortex and medulla regions (see Figure 4), the MOLLI and IR bFFE schemes show two peaks for cortex and medulla, and for the VFA the cortex and medulla separation is not apparent due to the poor fit.
Figure 4
A Histogram of IR SE-EPI kidney T1 values for Subject 1 with each peak colour coded and B the corresponding T1 map showing how each of the separate peaks in the histogram relate to the different regions within the kidney.
Figure 5
Effect of the simulated heart rate (75, 60, 50, 43, 38 beats per minute, bpm) of the MOLLI 5(3)3 scheme on measured T1 values of A cortex and B medulla for each subject. C Percentage change (mean±SEM across subjects) in T1 from the MOLLI T1 at 60 bpm for heart rates of 75, 50, 43, and 38 bpm. D MOLLI T1 confidence maps for Subject 1 at each heart rate showing black voxels in the medulla which have not fitted with confidence.