Spectrally selective three-dimensional dynamic balanced steady-state free precession for hyperpolarized C-13 metabolic imaging with spectrally selective radiofrequency pulses

Abstract

Purpose: Balanced steady-state free precession (bSSFP) sequences can provide superior signal-to-noise ratio efficiency for hyperpolarized (HP) carbon-13 (¹³ C) magnetic resonance imaging by efficiently utilizing the nonrecoverable magnetization, but managing their spectral response is challenging in the context of metabolic imaging. A new spectrally selective bSSFP sequence was developed for fast imaging of multiple HP ¹³ C metabolites with high spatiotemporal resolution.

Theory and methods: This novel approach for bSSFP spectral selectivity incorporates optimized short-duration spectrally selective radiofrequency pulses within a bSSFP pulse train and a carefully chosen repetition time to avoid banding artifacts.

Results: The sequence enabled subsecond 3D dynamic spectrally selective imaging of ¹³ C metabolites of copolarized [1-¹³ C]pyruvate and [¹³ C]urea at 2-mm isotropic resolution, with excellent spectral selectivity (∼100:1). The sequence was successfully tested in phantom studies and in vivo studies with normal mice.

Conclusion: This sequence is expected to benefit applications requiring dynamic volumetric imaging of metabolically active ¹³ C compounds at high spatiotemporal resolution, including preclinical studies at high field and, potentially, clinical studies. Magn Reson Med 78:963-975, 2017. © 2016 International Society for Magnetic Resonance in Medicine.

Keywords: balanced SSFP; banding artifact; hyperpolarized C-13; optimized RF pulse design; spectrally selective.

Figure 1

bSSFP frequency response with small flip angle (0.5°) hard pulse (A), large flip angle (45°) hard pulse (B), ideal selective RF pulse (passband/stopband flip angle = 45°/0.5°) (C), and a windowed sinc RF pulse (flip angle = 45°, duration = 2ms, bandwidth = 1kHz). “|Mxy|” is the averaged transverse magnetization over all echoes during transient state, “Mz” is the longitudinal magnetization after the last echo, “α/90°” is RF pulse excitation flip angle divided by 90°. Simulation parameters included: number of echoes = 256, TR = 4ms, T₁ = 40s, T₂ = 300ms, and linear ramp preparation pulse (N = 5).

Figure 2

Diagram of TR selection process for avoiding excitation banding artifact. Multiband spectral specification of urea, pyruvate, pyruvate hydrate, alanine and lactate in this implementation (selective excitation of pyruvate), with height corresponding to the desired RF pulse excitation flip angle and with finite bandwidth (±50Hz) for improving B₀ insensitivity (A). bSSFP frequency response with low flip angle (0.5°) (B). Normalized frequency is frequency over 1/(2TR). Locate spectral specification on top of bSSFP frequency response with suboptimal TR of 4ms (C), and optimal TR of 3.8ms (D). Simulated transient state echo train within urea stopband with TR of 4ms (E), and TR of 3.8ms (F). Simulation parameters include: number of echoes = 256, T₁ = 30s, T₂ = 1s, α/2 – TR/2 preparation pulse.

Figure 3

Flip angle scheme including a ramp-up preparation pulse and ramp-down flip back pulse (A). Simulated on-resonance magnetization evolution (B). Simulation parameters include: number of echoes = 256, T₁ = 40s, T₂ = 1s, TR = 3.785ms. Optimized lactate-only RF pulse with shortest duration (C), and its simulated spectral profile (D).

Figure 4

Bloch simulation of bSSFP signal evolution with finite RF pulse (left) and instantaneous RF pulse (right). RF pulse train at beginning including ramp up preparation pulses (A1,A2), and the corresponding Mxy phase evolution for spins within the specified passband ([−50Hz,50Hz]) (B1,B2). Three RF pulses in the middle of acquisition (C1,C2), and the corresponding Mxy phase evolution (D1,D2). Simulation parameters included: number of echoes = 256, number of preparation pulses = 5, number of flip back pulses = 5, TR = 3.785 ms, T₁ = 40s, T₂ = 1s, RF pulse passband flip angle = 40°, duration = 2.04ms.

Figure 5

Bloch simulation of bSSFP transient state echo signal within lactate passband (A,B) and pyruvate stopband (C,D). Finite RF pulses (duration = 2.04ms) are used in simulation (A,C), while instantaneous RF pulses are used in (B,D). Simulation parameters are the same as used in Fig. 4.

Figure 6

One coronal slice of 3D bSSFP pyruvate acquisition with ¹³C enriched phantom at the resonance frequency of urea/pyruvate/alanine/pyruvate-hydrate/lactate, with TR of 4ms (top row) and 3.8ms (bottom row). All images in each row are displayed with the same window-level parameters.

Figure 7

One axial slice of 3D dynamic bSSFP pyruvate/lactate/urea acquisition (at first time point) with HP pyruvate/lactate/urea phantoms individually. Measured spectral selectivity is indicated on each image. All images in each row are displayed with the same window-level parameters.

Figure 8

For the same data in Fig. 7, pyruvate/lactate/urea dynamic acquisition with HP lactate phantom, displaying one axial slice at all time points with the same window-level (A). Measured signal plotted with a logarithmic scale (B).

Figure 9

3D dynamic bSSFP in vivo images of HP pyruvate/lactate/urea in a normal mouse with injected co-polarized [1-¹³C]pyruvate and [¹³C]urea. Coronal slices at the first time point are displayed (3^rd – 5^th row), together with corresponding off-resonance frequency distribution for ¹³C (1^st row), ¹H slices for anatomical reference (2^nd row), and urea images overlaid on ¹H images (6^th row). Slices are arranged in posterior to anterior direction from left to right. Lactate images are displayed with 2× scaling factor compared to pyruvate. Saturation bands were applied near the heart and below the kidneys in ¹H acquisition to minimize flow related artifacts.

Figure 10

Same data as in Fig. 9 but displaying all time points at one coronal slice containing kidney and aorta (third slice from left in Fig. 9). Lactate images are displayed with 3× scaling factor compared to pyruvate. The time stamps are relative to starting time of injection and estimated based on average respiratory rate of 55/min, labeled on each image.