Temperature dependence of relaxation times and temperature mapping in ultra-low-field MRI

doi:10.1016/j.jmr.2013.07.009

Journal of Magnetic Resonance

Volume 235, October 2013, Pages 50-57

https://doi.org/10.1016/j.jmr.2013.07.009 Get rights and content

Highlights

•
Relaxation times of agarose gel are measured at fields of 50 μT–3 T and at temperatures of 5–45 °C.
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Interestingly, the effect of temperature on agarose gel T₁ relaxation is reversed around 5 mT.
•
The relaxation time data are used to form temperature maps measured at 50 μT.
•
The paper presents the first temperature maps measured at 50 μT.

Abstract

Ultra-low-field MRI is an emerging technology that allows MRI and NMR measurements in microtesla-range fields. In this work, the possibilities of relaxation-based temperature measurements with ultra-low-field MRI were investigated by measuring T₁ and T₂ relaxation times of agarose gel at 50 μT–52 mT and at temperatures 5–45 °C. Measurements with a 3 T scanner were made for comparison. The Bloembergen–Purcell–Pound relaxation theory was combined with a two-state model to explain the field-strength and temperature dependence of the data. The results show that the temperature dependencies of agarose gel T₁ and T₂ in the microtesla range differ drastically from those at 3 T; the effect of temperature on T₁ is reversed at approximately 5 mT. The obtained results were used to reconstruct temperature maps from ultra-low-field scans. These time-dependent temperature maps measured from an agarose gel phantom at 50 μT reproduced the temperature gradient with good contrast.

Graphical abstract

Introduction

MRI has been used for noninvasive temperature mapping for several decades [1]. Today, real-time MR thermometry is successfully applied, e.g., in the context of tumor ablation [2], [3] and localized drug delivery [4]. Other suggested applications of MR thermometry include the measurement of brain temperature [5] and the quality control of food sterilization [6]. For reviews of methods and applications of MR thermometry, see Refs. [7], [8].

Despite its recent success, the use of MR thermometry is limited because of its cost and, in the case of interventional therapy, the inherently closed geometry of the high-field scanners. On the other hand, an emerging technique called ultra-low-field (ULF) MRI [9], [10], [11] is potentially free of these problems. In ULF MRI, spins typically precess in fields of microtesla range. To enhance the signal-to-noise ratio (SNR), the sample is prepolarized [12] in a millitesla-range field and the signal is detected using superconducting quantum interference devices (SQUIDs). The low applied magnetic fields allow construction of an open, bore-free system, which is less expensive than a high-field scanner. Inspired by these advantages, the suitability of ULF MRI for temperature mapping was investigated in this study.

Although various MRI parameters are temperature-dependent, not all of them can be efficiently utilized in ULF MRI. First, the thermal equilibrium magnetization depends on temperature, following the Boltzmann distribution [13]. However, the effect is relatively small and difficult to utilize even with high-field scanners [8]. Second, the water proton chemical shift depends on temperature [14] leading to several applications at high fields [7], [8]. Nevertheless, the chemical shift is proportional to B₀ and thus negligible at low fields. A promising mechanism at ULF range is, however, the temperature dependence of T₁ and T₂ relaxation [15]. Studies of T₁ dispersion [16], [17] suggest that T₁ contrast is enhanced at low magnetic fields. Therefore, interesting findings may also be expected in the temperature dependence at low fields.

The temperature dependence of relaxation times has been extensively studied in tesla-range fields [18]. These studies include in vivo [19], ex vivo [20], and in vitro [21], [22] samples. However, there are relatively few studies on temperature dependence of relaxation times in fields below 100 mT. Using field-cycling methods [23], the temperature dependence of water T₁ in the range of 1 μT–1 mT has been measured [24]. For an extensive review of field-cycling relaxometry of tissue, see Ref. [25]. Specifically, the temperature and field strength dependence of T₁ in various paramagnetic [26] and diamagnetic [27] protein solutions have been extensively studied. In addition, there are several studies of modeling the field-strength and temperature dependence of tissue [28], [29]. Finally, a field-cycled spectrometer has been introduced for studying the temperature dependence of T₁ for non-medical purposes at 1 mT–7 T [30]. However, to our knowledge, temperature maps have previously not been measured in microtesla-range fields.

The goal of this study was to investigate the suitability of ULF MRI for relaxation-based temperature mapping. We will briefly review the theory of relaxation and its dependence on the magnetic field and temperature. Subsequently, we will show experimental T₁ and T₂ data of water and agarose gel measured at ultra-low fields. Finally, using the measured relaxation data and our ULF-MRI system, we will show temperature maps measured from a custom-made phantom at 50 μT.

Section snippets

Methods

In this paper, we chose to study agarose gel, which has relaxation properties similar to biological tissue [31] and has been shown to exhibit interesting T₁ dispersion in the range of 10 μT–300 mT [17]. In the following, a model describing the temperature and field dependence of agarose gel relaxation times will be reviewed. Later, values predicted by the model will be compared to experimental data obtained with our ULF-MRI system.

Relaxation theory

For a pure liquid spin-1/2 ensemble, the relaxation processes are dominated by intramolecular dipole–dipole couplings of the spins. The magnetic field by each spin is modulated by random molecular rotations that can be described by an auto-correlation function. Assuming the auto-correlation function is exponential, the Bloembergen–Purcell–Pound (BPP) relaxation theory [15] gives $\frac{1}{T_{1}} = \frac{A}{5} (\frac{τ}{1 + {(ω τ)}^{2}} + \frac{4 τ}{1 + {(2 ω τ)}^{2}}),$ $\frac{1}{T_{2}} = \frac{A}{10} (3 τ + \frac{5 τ}{1 + {(ω τ)}^{2}} + \frac{2 τ}{1 + {(2 ω τ)}^{2}}),$ where A is a constant, ω is the angular Larmor frequency, and

Relaxation-time measurements

Three 5-dl agarose gel samples (Sigma–Aldrich, A9539-25G) were prepared in pure water (Carl Roth, Rotisolv LC–MS) using agarose mass fractions of 0% (pure water), 0.25%, and 0.5%. For removing the dissolved oxygen, the samples were kept for an hour at around 90 °C before sealing them to air-tight flasks. After the initial sealing, none of the samples were opened.

Using our ULF-MRI system [11], the T₁ relaxation time of each sample was measured at 14 different field strengths from 50 μT to 52 mT,

Temperature-mapping measurements

After measuring the T₁ and T₂ relaxation times of the agarose gel samples, we proceeded to utilize this information by measuring relaxation-based temperature maps of a custom-made phantom, which is schematically depicted in Fig. 5A. The phantom was designed to generate a monotonic temperature gradient in the following manner. First, a polarizing coil generating a 1.3-mT/A field was wound of 2-mm copper wire around a flask, which was 12 cm in height and 10 cm in diameter. Second, a smaller

Results

Fig. 2 summarizes the measured T₁ and T₂ dispersion data. Water T₁ (Fig. 2B) appears constant across the available frequency range, while agarose gel T₁ dispersion (Fig. 2A) shows a prominent step around 10 mT. Both of these features are consistent with previous measurements [17], [24], [38]. However, the agarose gel T₁ times measured at 3 T are very close to the water T₁ values at the same temperature, which is possibly explained by a second step in the agarose gel T₁ dispersion curve. More

Discussion

In this paper, we presented measured T₁ and T₂ relaxation times of agarose gel at 50 μT–50 mT and at 3 T at temperatures 5–45 °C. We reviewed the related relaxation theory and suggested a model to explain the data. Finally, we used the measured T₁ and T₂ data to scan 2D temperature maps of an agarose gel phantom.

For this first study of temperature dependence of relaxation times in the ULF regime, we chose to investigate the relaxation properties of agarose gel. While agarose gel exhibits T₂ times

Conclusion

To investigate the potential of temperature mapping using ULF MRI, the temperature dependence of relaxation times T₁ and T₂ in agarose gel were measured at various field strengths between 50 μT and 3 T. Interestingly, the obtained T₁ relaxation dispersion shows that dT₁/dθ changes sign at a field of approximately 5 mT. Furthermore, we used the measured T₁ and T₂ data to reconstruct dynamic temperature maps of an agarose gel phantom. The results show that temperature mapping in the ULF regime is

Acknowledgments

This research has received funding from the European Community’s Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. HEALTH-F5-2008-200859, from the Emil Aaltonen Foundation, and from the Academy of Finland.

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View full text

Temperature dependence of relaxation times and temperature mapping in ultra-low-field MRI

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Methods

Relaxation theory

Relaxation-time measurements

Temperature-mapping measurements

Results

Discussion

Conclusion

Acknowledgments

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Progr. NMR Spectrosc.

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J. Biol. Chem.

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J. Magn. Reson.

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J. Magn. Reson. Imaging

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