Elsevier

NeuroImage

Volume 63, Issue 3, 15 November 2012, Pages 1237-1248
NeuroImage

Feasibility of an intracranial EEG–fMRI protocol at 3 T: Risk assessment and image quality

https://doi.org/10.1016/j.neuroimage.2012.08.008Get rights and content

Abstract

Integrating intracranial EEG (iEEG) with functional MRI (iEEG-fMRI) may help elucidate mechanisms underlying the generation of seizures. However, the introduction of iEEG electrodes in the MR environment has inherent risk and data quality implications that require consideration prior to clinical use. Previous studies of subdural and depth electrodes have confirmed low risk under specific circumstances at 1.5 T and 3 T. However, no studies have assessed risk and image quality related to the feasibility of a full iEEG–fMRI protocol. To this end, commercially available platinum subdural grid/strip electrodes (4 × 5 grid or 1 × 8 strip) and 4 or 6-contact depth electrodes were secured to the surface of a custom-made phantom mimicking the conductivity of the human brain. Electrode displacement, temperature increase of electrodes and surrounding phantom material, and voltage fluctuations in electrode contacts were measured in a GE Discovery MR750 3 T MR scanner during a variety of imaging sequences, typical of an iEEG–fMRI protocol. An electrode grid was also used to quantify the spatial extent of susceptibility artifact. The spatial extent of susceptibility artifact in the presence of an electrode was also assessed for typical imaging parameters that maximize BOLD sensitivity at 3 T (TR = 1500 ms; TE = 30 ms; slice thickness = 4 mm; matrix = 64 × 64; field-of-view = 24 cm). Under standard conditions, all electrodes exhibited no measurable displacement and no clinically significant temperature increase (< 1 °C) during scans employed in a typical iEEG–fMRI experiment, including 60 min of continuous fMRI. However, high SAR sequences, such as fast spin-echo (FSE), produced significant heating in almost all scenarios (> 2.0 °C) that in some cases exceeded 10 °C. Induced voltages in the frequency range that could elicit neuronal stimulation (< 10 kHz) were well below the threshold of 100 mV. fMRI signal intensity was significantly reduced within 20 mm of the electrodes for the imaging parameters used in this study. Thus, for the conditions tested, a full iEEG–fMRI protocol poses a low risk at 3 T; however, fMRI sensitivity may be reduced immediately adjacent to the electrodes. In addition, high SAR sequences must be avoided.

Highlights

► We studied the risk and image quality of a full intracranial EEG–fMRI protocol. ► Subdural grid, strip, and depth electrodes were tested in a GE 3 T scanner. ► No significant device movement, heating or induced currents were seen during fMRI. ► In contrast, high SAR scans (e.g., FSE) produced heating > 2.0 °C. ► An intracranial EEG–fMRI protocol in the reported conditions poses low risk.

Introduction

Simultaneous scalp electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) has been used to effectively combine their high temporal and spatial resolutions, respectively [see (Cunningham et al., 2008, Gotman et al., 2006) for review]. This multi-modality approach has permitted a better understanding of the mechanisms underlying the generation of epileptiform activity in humans. The use of intracranial EEG (iEEG) electrodes provides increased sensitivity to neuronal activity compared to scalp electrodes. Hence, there is potential to study epileptiform activity more fully by taking advantage of the unprecedented sensitivity of iEEG acquired simultaneously with fMRI.

The introduction of implants such as iEEG electrodes into an MR environment, however, has inherent risk implications (Bassen et al., 2006, Helfer et al., 2006, Rezai et al., 2002, Schaefers and Melzer, 2006, Schueler et al., 1999, Shellock, 2002, Shellock et al., 2004, Woods, 2007). Of these, there are three main practical considerations: i) device movement, ii) tissue damage due to radiofrequency (RF)-induced heating of the device, and iii) inadvertent neuronal stimulation as a result of switching magnetic gradient fields that can induce current in the electrical circuit. The theoretical considerations of these issues have been reviewed in detail previously (Carmichael et al., 2010). Movement of the device due to the magnetic field is the result of translational and/or rotational forces (deflection and torque, respectively) on the implant. For a device to be MR-conditional, these forces must be less than those experienced by the patient through everyday activity (ASTM, 2008). Neuronal damage from RF-induced heating can conceivably occur from prolonged increases of 5 °C above body temperature (Dewhirst et al., 2003, Georgi et al., 2004). Hence, current safety standards generally limit the temperature increase of a device to conservative limits, for example, within 1 °C of the surrounding tissue (IEC, 2002). Since temperature increases occurring during scanning are difficult to measure, exposure to RF fields is quantified by the ‘specific energy absorption rate’, or SAR, defined as the average energy dissipated in the body per unit of mass and time. In general, it has been established that the temperature of a device will increase with SAR (Bassen et al., 2006); however, it should be noted that setting absolute SAR thresholds for safety across all MR scanners may not be valid due to differences between scanner SAR calculations (Baker et al., 2005, Rezai et al., 2002). Time-varying gradient magnetic fields may induce currents and voltages in the electric circuit formed by the electrodes and connecting leads, which could result in inadvertent stimulation or tissue damage (Georgi et al., 2004). For this to occur, however, it has been suggested that the voltage must exceed 100 mV at a frequency less than 10 kHz (Georgi et al., 2004).

If safe parameters can be achieved, it still remains to be determined whether image artifacts introduced by the presence of the electrodes have a detrimental effect on fMRI image quality. The most commonly used imaging sequence for fMRI studies is gradient-recalled echo planar imaging (GR-EPI) because of its sensitivity to blood-oxygenation-level dependent (BOLD) contrast. The BOLD signal is the result of a localized change in magnetic field (i.e., magnetic susceptibility) when the concentration of deoxygenated hemoglobin decreases in response to increases in neural activity (characterized by a change in a tissue-dependent signal decay constant called T2*) (Ogawa et al., 1992). However, GR-EPI is also quite sensitive to foreign objects within the imaged area, particularly metal. The presence of metal decreases T2* signal in the vicinity of the object and image artifact appears as a signal void that extends beyond the edges of the object. As a result, fMRI sensitivity decreases in tissue in close proximity to the object.

Complication-free structural MR imaging of intracranial (subdural and depth) electrodes at 1.5 T has been previously documented under many conditions (Davis et al., 1999, Silberbusch et al., 1998). Subsequent studies of subdural, depth, and deep brain stimulating electrodes have also confirmed low risk under specific circumstances at 1.5 T (Baker et al., 2006, Bhidayasiri et al., 2005, Georgi et al., 2004, Rezai et al., 2002) and 3 T (Baker et al., 2005, Carmichael et al., 2007, Carmichael et al., 2008, Phillips et al., 2006). Deflection of the intracranial electrodes at 3 T has been shown to be minimal and well within safety limits (Carmichael et al., 2010). Nickel–chromium depth electrodes during MR scanning at 1.5 T have exhibited no significant temperature increase (Zhang et al., 1993). Other studies performed at 3 T using platinum depth and grid electrodes in a phantom model found temperature increases of less than 2 °C during scanning, provided the electrode tails were not electrically shorted, in which case, temperature increases of up to 6.9 °C were observed (Carmichael et al., 2008, Carmichael et al., 2010). A more recent study also showed that the gradient switching-induced currents and charge density were well within safety limits at 1.5 and 3 T (Carmichael et al., 2010).

It therefore appears that under certain circumstances, using specific scanners, subdural and depth electrodes pose a low risk at 1.5 or 3 T. To date, however, only one small study of simultaneous iEEG–fMRI is available, performed on two subjects (Vulliemoz et al., 2011). Notably, this study was performed at 1.5 T. Currently, higher magnetic field strength MR scanners (i.e., 3, 4, and even 7 T) are increasingly being introduced both in clinical and research settings, as they offer improved signal-to-noise ratio, particularly for fMRI (Bandettini et al., 1994, Kelley and Schenck, 1999, Takahashi et al., 2003, Tanenbaum, 2006). Hence, there is potential to further improve the study of epileptiform activity by taking advantage of the increased sensitivity of iEEG acquired simultaneously with higher field fMRI (3 T or greater). In addition, previous studies have not assessed risk and image quality specifically related to typical iEEG–fMRI protocols. To this end, we report on risk assessment and image quality related to commercially available subdural and depth electrodes at 3 T in our center over the entire course of an iEEG–fMRI protocol.

Section snippets

Experimental setup

A head phantom was designed and constructed (Fig. 1) to mimic the shape, size, and conductivity of the human head (Gabriel et al., 1996a). A body phantom was also made to approximate a human torso (53 cm × 43 cm × 11 cm; ASTM, 2011a). The head phantom consisted of a semi-solid saline–agar gel (Sigma-Aldrich, Saint Louis, MO) ‘brain’ surrounded by 0.9% NaCl fluid, and was held within a custom hollow acrylic sphere. The saline–agar gel was composed of 45 g of agar (A9799 Sigma-Aldrich, Saint Louis, MO)

Movement measurements

Results of translational force testing are provided in Table 1. The mean deflection of all three electrode types (subdural grid, strip, and depth electrodes) was < 1°, well below the established safety limit of 45°. There were no significant deflections or induced torque throughout the entire scan period (torque rating = 0) for any of the three types of electrodes.

Temperature measurements

Table 2 summarizes maximum temperature changes recorded for each sequence of the EEG–fMRI protocol at our center as well as higher SAR

Discussion

We have reported on risk assessment and image quality related to subdural and depth electrodes at 3 T over the course of a typical iEEG–fMRI study protocol. We examined device movement in the static magnetic field, RF-induced heating, and gradient-induced currents that can result in neural stimulation. We also assessed image quality since the ultimate aim of our research is to perform iEEG–fMRI in human subjects.

Acknowledgments

We thank Dr. M Louis Lauzon for his valuable contributions to the study. This work was supported by the Canadian Institutes for Health Research, Alberta Heritage Foundation for Medical Research, and Canada Foundation for Innovation. CC was supported by studentships awarded by the Savoy Foundation for Epilepsy and the University of Calgary.

References (47)

  • ASTM F 2119–07

    Standard test method for evaluation of MR image artifacts from passive implants

  • ASTM F 2182–11

    Standard test method for measurement of radio frequency induced heating near passive implants during magnetic resonance imaging

  • ASTM F 2213–06

    Standard test method for measurement of magnetically induced torque on medical devices in the magnetic resonance environment

  • ASTM F 2503–08

    Standard practice for marking medical devices and other items for safety in the magnetic resonance environment

  • K.B. Baker et al.

    Neurostimulation systems: assessment of magnetic field interactions associated with 1.5- and 3-Tesla MR systems

    J. Magn. Reson. Imaging

    (2005)
  • K.B. Baker et al.

    Variability in RF-induced heating of a deep brain stimulation implant across MR systems

    J. Magn. Reson. Imaging

    (2006)
  • P.A. Bandettini et al.

    Spin-echo and gradient-echo EPI of human brain activation using BOLD contrast: a comparative study at 1.5 T

    NMR Biomed.

    (1994)
  • H. Bassen et al.

    MRI-induced heating of selected thin wire metallic implants – laboratory and computational studies – findings and new questions raised

    Minim. Invasive Ther. Allied Technol.

    (2006)
  • D.W. Carmichael et al.

    Safety of localizing epilepsy monitoring intracranial electroencephalograph electrodes using MRI: radiofrequency-induced heating

    J. Magn. Reson. Imaging

    (2008)
  • C.M. Collins et al.

    Model of local temperature changes in brain upon functional activation

    J. Appl. Physiol.

    (2004)
  • C.J. Cunningham et al.

    Simultaneous EEG–fMRI in human epilepsy

    Can. J. Neurol. Sci.

    (2008)
  • M.W. Dewhirst et al.

    Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia

    Int. J. Hyperthermia

    (2003)
  • P. Federico et al.

    Cortical/subcortical BOLD changes associated with epileptic discharges: an EEG–fMRI study at 3 T

    Neurology

    (2005)
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