3D spin-lock imaging of human gliomas

doi:10.1016/S0730-725X(99)00041-7

Magnetic Resonance Imaging

Volume 17, Issue 7, September 1999, Pages 1001-1010

https://doi.org/10.1016/S0730-725X(99)00041-7 Get rights and content

Abstract

We investigated whether the simultaneous use of paramagnetic contrast medium and 3D on-resonance spin lock (SL) imaging could improve the contrast of enhancing brain tumors at 0.1 T. A phantom containing serial concentrations of gadopentetate dimeglumine (Gd-DTPA) in cross-linked bovine serum albumin (BSA) was imaged. Eleven patients with histologically verified glioma were also studied. T₁-weighted 3D gradient echo images with and without SL pulse were acquired before and after a Gd-DTPA injection. SL effect, contrast, and contrast-to-noise ratio (CNR) were calculated for each patient. In the glioma patients, the SL effect was significantly smaller in the tumor than in the white and gray matter both before (p = 0.001, p = 0.025, respectively), and after contrast medium injection (p < 0.001, p < 0.001, respectively). On post-contrast images, SL imaging significantly improved tumor contrast (p = 0.001) whereas tumor CNR decreased slightly (p = 0.024). The combined use of SL imaging and paramagnetic Gd-DTPA contrast agent offers a modality for improving tumor contrast in magnetic resonance imaging (MRI) of enhancing brain tumors. 3D gradient echo SL imaging has also shown potential to increase tissue characterization properties of MR imaging of human gliomas.

Introduction

Gadolinium-based contrast agents are routinely used in clinical magnetic resonance (MR) imaging to increase the sensitivity and specificity of brain tumor studies.1, 2 Spin lock (SL), and magnetization transfer (MT) imaging are new techniques that have been shown to increase contrast-to-noise ratio (CNR) and improve tissue characterization in MR imaging.3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16 A significant improvement in contrast of brain lesions when the use of paramagnetic contrast material is combined with MT imaging has been demonstrated.17, 18, 19, 20, 21 The contrast improvement is due to the difference in the efficiency of MT in non-enhancing, macromolecular rich tissue and in enhancing tissue. MT is strong in macromolecular rich tissue but in enhancing tissue the paramagnetic relaxation reduces MT. It has been suggested that MT at low field strength is the main source of relaxation observed with the SL technique.22 Thus, combining T₁-weighted SL imaging with the use of paramagnetic contrast material may improve the detection of enhancing brain tumors.

In an SL experiment the locked nuclear magnetization relaxes along the locking field (B_1L) during the locking period (TL). The observed relaxation may be considered as longitudinal relaxation at B_1L corresponding to the Larmor frequency f_1L = (γ/2π) B_1L. The strength of B_1L is very low compared to the strength of the polarizing magnetic field (B₀). Therefore, the observed relaxation time T_1ρ, usually called longitudinal relaxation time in the rotating frame, probes the very low frequency range, and, therefore, is likely to be more sensitive to changes in concentration, mobility, and interactions of macromolecules than T₁ obtained at B₀. In the present study we have combined SL pulse and T₁-weighted 3D imaging to evaluate the usefulness of imaging of human brain gliomas. For evaluating the T₁-weighted 3D SL imaging, we used an appropriate phantom model containing different cross-linked bovine serum albumin (BSA) and gadopentetate dimeglumine (Gd-DTPA) concentrations.23 In the patient study we investigated whether the simultaneous use of paramagnetic contrast medium and T₁-weighted SL imaging could improve the contrast of enhancing brain tumors.

Section snippets

Materials and methods

All imaging was performed at room temperature with a low field (B₀ = 0.1 T) resistive magnet imager (Merit^®, Picker Nordstar, Inc., Helsinki, Finland) using a head transmitting/receiving coil.

Phantom study

1/T_1ρ and 1/T₁ for all protein concentrations increased with increasing the Gd-DTPA concentration as shown in Fig. 2 (a and b). T₁ relaxivity of Gd-DTPA in the 5, 10, 15, and 20% cross-linked BSA was 7.6 ± 0.2, 8.3 ± 0.2, 9.6 ± 0.2, and 9.8 ± 0.4 mmol⁻¹ l s⁻¹, respectively. T_1ρ relaxivity of Gd-DTPA in the 5, 10, 15, and 20% cross-linked BSA was 6.9 ± 0.2, 7.6 ± 0.3, 9.4 ± 0.7, and 9.8 ± 0.9 mmol⁻¹ l s⁻¹, respectively. Both T₁ and T_1ρ relaxivities of Gd-DTPA increased slightly with increasing

Discussion

The combination of MT technique and contrast medium (Gd-DTPA) has been proven to improve contrast and CNR in brain lesion imaging.17, 18, 19, 20, 21 The SL technique combined with simultaneous use of paramagnetic contrast agents has also improved tissue contrast in previous studies.24, 25 Although Gd-DTPA reduced both relaxation times T₁ and T_1ρ (Fig. 2), increasing Gd-DTPA concentration did not have a significant effect on the measured SL_eff on T₁-weighted images in the phantom when we

Acknowledgements

We thank Peter B. Dean, M.D., for his comments on the manuscript. This work was supported in part by Magnus Ehrnrooth Foundation (U.A.R.), Alfred Kordelin Foundation (U.A.R.), HUCH-Foundation (U.A.R.), Radiological Society of Finland (U.A.R.), Cancer Organizations of Finland (H.J.A., A.T.M.), Vuorisalo Foundation (H.J.A.), Paulo Foundation (H.J.A.), Research grants from Helsinki University Central Hospital, and EVO grants TYH0068 and TYH8102 (H.J.A., U.A.R., A.T.M.).

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Novel MRI contrast methods, such as Chemical Exchange Saturation Transfer (CEST), rely on previously developed theory and approaches, often introduced first in solidstate NMR. Understanding or at least connecting the basic principles and original works to the modern-day contrast methods in MRI is instructive. The work brings together concepts in relaxation, saturation, and spin lock experiments in the dynamic (exchanging) systems. The work describes how basic principles and theory are translated and being applied to MRI contrast, including MT and CEST. Finally, we review select papers generalizing concepts of relaxation under periodic RF.
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To date, clinical applications of this MRI technique has been most widely applied to evaluating the hydration status of human articular cartilage. However, the neurologic applications of T1ρ MRI have been explored in patients with ischemia, neurodegenerative disorders, and brain tumors, and as a response assessment to gene therapy within glioma mouse models [12–23]. T1ρ MRI obtains tissue contrast through the quantification of spin-lattice relaxation in the rotating frame.
Spin-lattice relaxation in the rotating frame magnetic resonance imaging allows for the quantitative assessment of spin-lock contrast within tissues. We describe the utility of spin-lattice relaxation in the rotating frame metrics in characterizing glioblastoma biological heterogeneity. A 84-year-old man presented to our institution with a right frontal temporal mass. Prior tissue sampling from a peripheral nonenhancing lesion was nondiagnostic. Stereotactic image-guided tissue sampling of the nonenhancing T2-fluid-attenuated inversion recovery hyperintense region involving the anterior cingulate gyrus with elevated spin-lattice relaxation in the rotating frame metrics provided a pathologic diagnosis of glioblastoma. This case illustrates the utility of spin-lattice relaxation in the rotating frame magnetic resonance imaging in identifying biologically aggressive regions within glioblastoma.
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To the best of our knowledge, whole brain T1ρ imaging has not been previously used to characterize the pathological processes of untreated brain tumors and associated cerebral edema in humans. T1ρ has been studied to a limited extent in several neuroimaging applications including the evaluation of ischemia [11,23,24], neurodegenerative disorders [17,18], demyelinating disease [20,21], animal models of brain tumor [12–14,25], and response to gene therapy [15,16]. Although the exact mechanisms governing T1ρ relaxation are not fully understood, several factors proposed to influence T1ρ include scalar coupling, dipole–dipole interactions, and chemical exchange processes [26].
Cerebral edema associated with brain tumors is an important source of morbidity. Its type depends largely on the capillary ultra-structures of the histopathologic subtype of underlying brain tumor. The purpose of our study was to differentiate vasogenic edema associated with brain metastases and infiltrative edema related to diffuse gliomas using quantitative 3D T1 rho (T1ρ) imaging.
Preoperative MR examination including whole brain 3D T1ρ imaging was performed in 23 patients with newly diagnosed brain tumors (9 with metastasis, 8 with lower grade glioma, LGG, 6 with glioblastoma, GBM). Mean T1ρ values were measured in regions of peritumoral non-enhancing T2 signal hyperintensity, excluding both enhancing and necrotic or cystic component, and normal-appearing white matter.
Mean T1ρ values were significantly elevated in the vasogenic edema surrounding intracranial metastases when compared to the infiltrative edema associated with either LGG or GBM (p = 0.02 and <0.01, respectively). No significant difference was noted between T1ρ values of infiltrative edema between LGG and GBM (p = 0.84 and 0.96, respectively).
Our study demonstrates the feasibility and potential diagnostic role of T1ρ in the quantitative differentiation between edema related to intracranial metastases and gliomas and as a potentially complementary tool to standard MR techniques in further characterizing pathophysiology of vasogenic and infiltrative edema.
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T1rho is often measured by the spin-lock technique described by Redfield [1] and was introduced into the field of MRI by Sepponen et al. [2]. It has been reported that T1rho imaging is potentially useful for diagnostic imaging of a variety of human diseases [3–14]. Conventional spin-lock is achieved by applying a radiofrequency (RF) pulse with constant amplitude along the magnetization after RF excitation.
T1rho imaging with constant amplitude spin-lock is prone to artifacts in the presence of B1 RF and B0 field inhomogeneity. Despite significant technological progress, improvements on the robustness of constant amplitude spin-lock are necessary in order to use it for routine clinical practice. This work proposes methods to simultaneously correct for B1 RF and B0 field inhomogeneity in constant amplitude spin-lock. By setting the maximum B1 amplitude of the excitation adiabatic pulses equal to the expected constant amplitude spin-lock frequency, the spins become aligned along the effective field throughout the spin-lock process. This results in T1rho-weighted images free of artifacts, despite the spatial variation of the effective field caused by B1 RF and B0 field inhomogeneity. When the pulse is long, the relaxation effect during the adiabatic half passage may result in a non-negligible error in the mono-exponential relaxation model. A two-acquisition approach is presented to solve this issue. Simulation, phantom, and in-vivo scans demonstrate the proposed methods achieve superior image quality compared to existing methods, and that the two-acquisition method is effective in resolving the relaxation effect during the adiabatic half passage.
T1rho MRI and CSF biomarkers in diagnosis of Alzheimer's disease
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T1ρ MRI has been previously used to measure the T1ρ relaxation time in the normal human brain, and showed higher range of values compared to the T2 relaxation time (Borthakur et al., 2004). Earlier, T1ρ has been used to delineate brain tumors (Aronen et al., 1999), characterize breast cancer tissue (Li et al., 2011), and monitor the level of cartilage degeneration (Regatte et al., 2004; Witschey et al., 2010). Borthakur et al. have shown the feasibility of T1ρ imaging in evaluating the plaques burden in a mouse model of AD (Borthakur et al., 2006a).
In the current study, we have evaluated the performance of magnetic resonance (MR) T1rho (T_1ρ) imaging and CSF biomarkers (T-tau, P-tau and Aβ-42) in characterization of Alzheimer's disease (AD) patients from mild cognitive impairment (MCI) and control subjects. With informed consent, AD (n = 27), MCI (n = 17) and control (n = 17) subjects underwent a standardized clinical assessment and brain MRI on a 1.5-T clinical-scanner. T_1ρ images were obtained at four different spin-lock pulse duration (10, 20, 30 and 40 ms). T_1ρ maps were generated by pixel-wise fitting of signal intensity as a function of the spin-lock pulse duration. T_1ρ values from gray matter (GM) and white matter (WM) of medial temporal lobe were calculated. The binary logistic regression using T_1ρ and CSF biomarkers as variables was performed to classify each group. T_1ρ was able to predict 77.3% controls and 40.0% MCI while CSF biomarkers predicted 81.8% controls and 46.7% MCI. T_1ρ and CSF biomarkers in combination predicted 86.4% controls and 66.7% MCI. When comparing controls with AD, T_1ρ predicted 68.2% controls and 73.9% AD, while CSF biomarkers predicted 77.3% controls and 78.3% for AD. Combination of T_1ρ and CSF biomarkers improved the prediction rate to 81.8% for controls and 82.6% for AD. Similarly, on comparing MCI with AD, T_1ρ predicted 35.3% MCI and 81.9% AD, whereas CSF biomarkers predicted 53.3% MCI and 83.0% AD. Collectively CSF biomarkers and T_1ρ were able to predict 59.3% MCI and 84.6% AD. On receiver operating characteristic analysis T_1ρ showed higher sensitivity while CSF biomarkers showed greater specificity in delineating MCI and AD from controls. No significant correlation between T_1ρ and CSF biomarkers, between T_1ρ and age, and between CSF biomarkers and age was observed. The combined use of T_1ρ and CSF biomarkers have promise to improve the early and specific diagnosis of AD. Furthermore, disease progression form MCI to AD might be easily tracked using these two parameters in combination.
Assessment of T<inf>1</inf>, T<inf>1ρ</inf>, and T<inf>2</inf> values of the ulnocarpal disc in healthy subjects at 3 tesla
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The purpose of this study was to implement clinically feasible imaging techniques for determination of T₁, T_1ρ, and T₂ values of the ulnocarpal disc and to assess those values in a cohort of asymptomatic subjects at 3 tesla. Resulting values were compared between different age groups, since former histological findings of the ulnocarpal disc indicated frequent early degenerative changes of this tissue starting in the third decade of life, even in asymptomatic subjects.
Twenty-seven healthy subjects were included in this study. T₁ measurements were performed using 3D spoiled gradient-echo (GRE) sequence with variable flip angle. A series of T_1ρ and T₂-weighted images was acquired by a 3D GRE sequence after suitable magnetization preparation. T_1,T_1ρ, and T₂ maps of the ulnocarpal disc were calculated pixel-wise. Representative mean values from extended regions were analysed.
Mean T₁ values of the ulnocarpal disc ranged from 722 ms in a 39 year-old subject to 1264 ms in a 65 year-old subject, T_1ρ ranged from 9.2 ms (26 year-old subject) to 25.9 ms (65 year-old subject). Calculated T₂ values showed a large range from 4.1 ms to 22.3 ms. T_1ρ and T₁ values tended to increase with age (p < 0.05), whereas T₂ did not.
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Original Contribution3D spin-lock imaging of human gliomas

Abstract

Introduction

Section snippets

Materials and methods

Phantom study

Discussion

Acknowledgements

Acad. Radiol.

Magn. Reson. Imaging

Brain tumors: MR imaging with gadolinium-DTPA

Radiology

Clinical experience with routine Gd-DTPA administration for MR imaging of the brain

J. Comput. Assist. Tomogr.

Determination of magnetization transfer contrast in tissue: An MR imaging study of brain tumors

Am. J. Roentgenol.

Metastatic lesions of the brain: Imaging with magnetization transfer

Radiology

Head and neck neoplasms: Magnetization transfer analysis

Radiology

Spin locking for magnetic resonance imaging with application to human breast

Magn. Reson. Med.

Rotating frame and magnetization transfer

T1ρ Dispersion imaging and localized T1ρ dispersion relaxometry: Application in vivo to mouse adenocarcinoma

Magn. Reson. Med.

T1ρ dispersion imaging of diseased muscle tissue

Br. J. Radiol.

Spin lock magnetic resonance imaging in the differentiation of hepatic heamangiomas and metastases

Br. J. Radiol.

Spin lock and magnetization transfer imaging of head and neck tumors

Radiology

Original Contribution
3D spin-lock imaging of human gliomas

T_1ρ Dispersion imaging and localized T_1ρ dispersion relaxometry: Application in vivo to mouse adenocarcinoma

T_1ρ dispersion imaging of diseased muscle tissue