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Magnetic resonance (MR)-based mapping of electrical tissue properties is an emerging technique that uses MR to
derive non-invasive information of tissue properties
including electrical conductivity and permittivity (14).
It can be classified according to two complementary criteria. One is the use of applied currents or applied fields
and the other is the reliance upon surface measurements
or internal data (5,6). Magnetic resonance electrical impedance tomography (MREIT) is a typical technique,
which uses magnetic resonance imaging to measure the
internal data (i.e., magnetic flux density) induced by
externally injected currents (5). In contrast, magnetic resonance electrical properties tomography (MREPT) uses
the spatial sensitivity distributions of the applied Radio
frequency (RF) coils, the B1 field map, without applying
any external currents (6).
MREIT has the advantage of providing conductivity information for biological tissues in what is known to be a
physiologically interesting frequency range. External currents with low frequencies are injected into an imaging
object through a pair of surface electrodes. The induced
magnetic flux density is determined by the current density distribution followed by the BiotSavart law (5,7).
Since the magnetic flux density perturbs the main field
of a magnetic resonance imaging scanner, one can obtain
the z-component of the induced magnetic flux density
(Bz) in the form of an image from the obtained MR phase
images (810). Applying a conductivity image reconstruction algorithm (1114), we can reconstruct a highresolution, high-contrast conductivity image of the imaging object. The current injection is a primary limiting
factor for the practical application of MREIT due to comfort and safety issues (7).
MREPT derives the electric conductivity and permittivity from the spatially sensitive B1 distributions arising
from the applied RF coils, which can be obtained by
mapping the transmit RF field (6,15,16). MREPT does
not use any additional devices such as external electrodes, currents, or RF probes to enhance the feasibility of
the approach (6). In addition, MREPT does not require
the solution of an inverse problem that could compromise spatial image resolution (6,17). Conductivity distributions can be reconstructed to a certain accuracy from
phase images while permittivity distributions can be
reconstructed approximately from magnitude images of
the RF transmit field. However, the sensitivity is relatively poor and the estimate of the conductivity is very
sensitive to noise (1).
It is well known that the aforementioned two methods
provide the electrical conductivities of the human body
at different frequency ranges (16). MREIT provides conductivity images at the low frequency range below 1
kHz, depending on the applied RF rephasing pulses,
while MREPT provides conductivity images in the range
of 10200 MHz, according to the Larmor frequency (1).
Since the biological tissues show frequency-dependent
conductivity spectra (1820), their values at different
200
frequencies may provide valuable diagnostic information. Several studies have reported unique conductivity
distributions in various phantom, animal, and human
experiments (2,6,2123). These two techniques are,
therefore, complementary and can provide new information when combined. Recently, Minhas et al. (24)
reported experimental results of both MREIT and MREPT
and highlighted their distinct features in probing and
visualizing an object. However, they measured the electrical conductivity of the object from separate MR scans.
Moreover, a direct comparison was not possible, since
the low-frequency conductivity image from the MREIT
data provided only contrast information.
In this study, we propose a simultaneous conductivity
imaging technique providing the dual-frequency characteristics of tissue conductivity from a single MR scan.
We will first describe methods for data acquisition, conversion, and calculation to obtain the magnetic flux density and B
1 map from the k-space data. We will then
present reconstruction procedures for low- and high-frequency conductivity images. Presenting results of various phantom imaging experiments, we will show that
MREIT and MREPT are complementary and suggest
future experimental studies on animals and human
subjects.
201
FIG. 1. A conventional spin-echo based injected-current-nonlinear-encoding pulse sequence for the acquisition of dual-frequency
conductivity images. The imaging currents were injected in the
form of pulses whose timing was synchronized with the RF pulse.
METHODS
Spin Echo Injected Current Nonlinear Encoding Pulse
Sequence
For the simultaneous imaging of dual-frequency conductivity, we adopted the injected current nonlinear encoding (ICNE) spin-echo pulse sequence, shown in Figure 1,
which is widely used in MREIT imaging experiments
(25). Through a pair of electrodes, current is injected in
the form of pulses whose timing is synchronized with an
RF pulse. The injected current induces a magnetic flux
density B, which produces extra phase shifts. Phase
accumulation is proportional to the z-component Bz of B.
As shown in Figure 1, we sequentially injected positive
and negative currents, I and I, respectively, to cancel
out any systematic phase artifacts of the magnetic resonance imaging scanner. To increase the quality of the
measured Bz data for MREIT, the ICNE method extends
the duration of the injection current until the end of the
read-out gradient to maximize the phase accumulation
by allowing a prolonged current injection. MREPT uses
the spatial sensitivity distributions of the applied RF
coils, which can be extracted from the ICNE acquisition;
hence, there were no particular changes in the MR pulse
sequence.
Extraction of Bz Image and B1 Map
Maxwells equations relate the electric field (E), magnetic
field (Bl0 H), and current density (J):
r Er ivm0 Hr and r Hr kr Er Jr [1]
where the admittivity jrixe, and r and e are the conductivity and permittivity, respectively, at the angular
frequency x.
[2]
where qa denotes a term related to the transverse magnetization at a flip angle a, c is the gyromagnetic ratio of
hydrogen and TcTc1Tc2 is the duration of the injected
current (26,27). Additional phase artifacts due to field
inhomogeneity were considered negligible using the spin
echo sequence. At the Larmor frequency of 128 MHz, the
B1 mapping technique provided the positive-rotating
magnetic field information H10.5(HxiHy). In this case,
qa can be expressed as
ra r C1 M0 rH rsin C2 ajH rjexp iw r
[3]
[4]
By subtraction of the phase terms, we obtained the magnetic flux density Bz(r) created by the externally injected
current at the low frequency. The measured magnetic flux
density Bz satisfies Maxwells equation (Eq. [1]) with the
admittivity j rL, where the conductivity rL reflects the
low-frequency electrical property responding to the
injected current through the attached electrodes. By summation of the phase terms in Eq. [4], the phase term of H1,
u1, can be measured assuming that u1(r) u2(r). The accuracy of this assumption depends on many factors
including the object geometry and its dielectric constant,
the field strength, and the RF coil. Here, we used a single
channel transmit and receive birdcage head coil at a field
strength of 3 T, which has been regarded as reasonable for
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Kim et al.
FIG. 2. Schematic diagram showing the data processing for the dual-frequency conductivity imaging. The k-space data were converted
and calculated to obtain the magnetic flux density (Bz) and B1 phase map with proper subtraction or summation of phase information.
[5]
in V;
ran g
on @V
[6]
@ log sL r @ log sL r
1
;
JxP r; JyP r r2 Bz r:
@x
@y
m0
[8]
From the relation in Eq. [8] and using two independent injected currents, we can reconstruct the absolute
low-frequency conductivity distribution rL in the object
by solving the matrix system (28).
0
1 0
1
1 2 1
! @ log sL r
r
B
P;1
P;1
z
C B m
C
Jx r Jy r B
@x
0
B
CB
C:
JxP;2 r JyP;2 r @ @ log sL r A @ 1 r2 B2 r A
z
m0
@y
[9]
By assuming local homogeneity, i.e., !j 0, the positively rotating field H1 combined with Maxwells equation satisfies
r2 H r ivm0 krH r:
in V t
[7]
ir2 H r
:
m0 vH r
[11]
r Bz r
2
2
@x
@y
m0
br 0 on @V t :
[10]
r2 wH r
:
m0 v
[12]
The schematic diagram, which represents the reconstruction procedure of low- and high-frequency conductivity as described above, is shown in Figure 3.
Imaging Experiment
For the imaging experiments, we placed each phantom
inside the bore of our 3 T MR scanner (Achieva TX, Philips
203
FIG. 3. Image reconstruction procedure of low- and high-frequency conductivities. The low-frequency conductivity was reconstructed
from the measured magnetic flux density by the projected current density method while the high-frequency conductivity was based on
B1 phase field map by estimating the conductivity rH in Eq. [12].
Medical Systems, Best, The Netherlands) with a birdcagetype head coil (Fig. 4a). Using a custom-designed MREIT
current source, we injected the first set of currents I16 with
3-mA amplitude and 30-ms injection time between the horizontal pair of electrodes. After acquiring the first data set
with I16 , the second set of injection currents I26 with the
same amplitude and width were injected through the vertical pair of electrodes (Fig. 4b,c). The image parameters
used were Repetition time/Echo time800/30 ms, Field of
view180 180 mm2, slice thickness4 mm (no gap),
number of averages8, matrix size128 128, number of
slices8, and total scan time60 min.
Phantom Preparation
For the practical approaches of simultaneous dual-frequency conductivity imaging, we prepared an imaging
object called the conductivity phantom, whose conductivity distribution was predetermined and stable over
time. To create a conductivity contrast, we must put at
least two objects with different conductivity values together so that they are physically contacting each other.
In this study, three different conductivity phantoms
were used to understand low- and high-frequency conductivity characteristics. Before the imaging experiments,
we measured the actual conductivity values of each
FIG. 4. Experimental setup for phantom imaging experiment. a: Phantom location inside the MR bore; (b) schematic of a method for
injecting currents I1 and I2 along two different directions; and (c) a picture of injected current synchronized with RF pulse. [Color figure
can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
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Kim et al.
inclusion with an impedance analyzer (SI1260A, AMETEK Inc., UK) using a four-electrode method.
Agarose Gel Phantom (Phantom A)
We built a cylindrical phantom with a diameter of 13 cm
and height of 16 cm, as shown in Figure 5a. The phantom
was filled with a saline solution having a conductivity of
0.20 S/m (0.3 g/L NaCl and 1 g/L CuSO4). Two cylindrical
agar objects were then positioned inside the phantom and
their conductivity values were found to be about 2.85 S/m
and 1.10 S/m. We attached four carbon-hydrogel electrodes (HUREV Co. Ltd., Korea) on the side of the phantom.
Insulating Film Phantom (Phantom B)
We changed the anomaly from agarose gel to a thin
hollow cylindrical object using an insulating film of cellulose acetate with a thickness of 0.3 mm (30). Two different kinds of insulating films, with and without holes,
were positioned in the phantom as shown in Figure 6a.
In the case of the anomaly with holes, four equally
spaced 3-mm-diameter holes around the objects circumference were aligned with the centers of four carbonhydrogel electrodes. We filled both the inside and outside of the hollow cylinder with the same saline of 0.20
S/m conductivity.
Hybrid Phantom (Phantom C)
The third phantom was a mixture of the two types
described above. Two different kinds of anomalies were
positioned in the phantom (Fig. 7a). One was an insulating film with four equally spaced 5-mm-diameter holes.
The other was an agarose gel object wrapped in a thin
insulating film without holes. The conductivity value of
the agarose gel was 1.10 S/m. After positioning the cylindrical anomalies inside the phantom, we filled phantom
C with the same saline solution used in the other
phantoms.
RESULTS
Agarose Gel Phantom Imaging
Figure 5 shows typical results of the simultaneous dualfrequency conductivity imaging of phantom A. Figure
5a,b show the experimental setup and an MR magnitude
image of the agarose gel together with four carbon-hydrogel electrodes. The present ICNE pulse sequence (25),
which is commonly used in MREIT, provides not only
low-frequency conductivity from MREIT data (Fig. 5c)
but also high-frequency conductivity from MREPT data
(Fig. 5d), simultaneously. Data for the low-frequency
range in Figure 5c were gathered at a 3-mA amplitude
and 30-ms current injection time. We obtained eight
imaging slices from the phantom experiment and reconstructed two-dimensional conductivity images with six
slices. Every six slices showed the same pattern in the
conductivity images. Since the externally injected currents at low frequency could penetrate the agar objects,
we can reconstruct low-frequency conductivity images
from the measured magnetic flux density (Fig. 5c). The
high-frequency conductivity image in Figure 5d is
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Kim et al.
Table 1
Measured Conductivity Values of Three Different Phantom Experiments
Conductivity [S/m]
Phantom A
Phantom B
Phantom C
Saline solution
Agar 1
Agar 2
Saline solution
Inside a film with holes
Inside a film without holes
Saline solution
Inside a film with holes
Wrapped agar
Actual
Low frequency
High frequency
0.20
2.85
1.10
0.20
0.20
0.20
0.20
0.20
1.10
0.2460.01
2.9360.07
1.0560.03
0.2160.01
0.1060.01
0.0560.01
0.2060.01
0.1560.01
0.0860.01
0.2360.16
2.9260.14
1.0660.11
0.2260.04
0.2360.03
0.2760.03
0.1960.01
0.1860.03
1.0660.05
The absolute conductivity values (means6SD) of the saline solution and anomalies were obtained with a region-of-interest size of 5 5
pixels in both low- and high-frequency conductivity images.
properties of tissue (3032). The conductivity of a homogeneous conductive fluid is determined by a sum of
products of concentrations and mobility of ions in the
solution (30). The cell membranes are considered insulators having a high capacitance and a low but complicated pattern of conductivity (31). At direct current and
low frequencies, the current passes around the cells. The
internal structures of the cells do not contribute to any
current flow. At high frequencies, the membrane
capacitance allows alternating current to pass. The
membrane effect disappears, and the current flows everywhere according to local ionic conductivity (31,3335).
These frequency-dependent conductivity spectra and values of biological tissues may provide new information
on tissue structure and function that is complementary
to the information provided by traditional magnetic resonance imaging.
In this study, we implemented simultaneous dual-frequency conductivity imaging from a single MR scan.
Using a conventional ICNE pulse sequence, which is
widely used in MREIT studies, we can obtain k-space
data for both MREIT and MREPT. The data are converted
to the magnetic flux density and B1 phase map by the
subtraction or summation of phase information, respectively. Finally, we can reconstruct both low- and highfrequency conductivity images simultaneously. According to our experimental validation using three different
phantoms, we have provided a potential for dual-frequency conductivity imaging.
In phantom A, the reconstructed conductivity images
showed similar patterns for both frequencies. Since the
injected currents passed through the agar anomalies, the
low-frequency conductivity images from the MREIT data
show a clear contrast between the two agar anomalies
with different conductivities. The high-frequency conductivity images from the MREPT data also showed similar contrast. The measured conductivity values from the
anomalies and the background saline solution matched
their actual values well. However, the MREPT results
showed relatively higher standard deviations than the
MREIT due to the inherently poor signal-to-noise ratio
and noise-sensitive characteristics.
The conductivity images of phantom B show quite different patterns between the two methods. Basically, the
insulating membrane behaved as a solid insulator
(30,31). When the phantom included a hollow insulating
cylinder without holes, ions were trapped inside the cylinder. When the hollow cylinder had holes, the ions
were mobile through the holes and these mobile ions
contributed to the current flow throughout the cylindrical anomaly. At low frequencies, the region inside the
membrane appeared as a less conductive region than
the background saline solution, even though they have
the same value of 0.20 S/m. This stems from the fact
that the injected currents did not pass through the insulating film, and thus, there was no magnetic flux density
data inside the insulating film. The relatively high conductivity in the anomaly with holes indicates that the
current partially passed the insulating film through the
holes (30). This current flow contributed to conductivity
image reconstructions. However, the membrane will
eventually become transparent in conductivity images at
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