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Summary
Magnetic Resonance (MR) is an exceptionally powerful and versatile measurement technique. The
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basic structure of an MR experiment has remained nearly constant for almost 50 years. Here we
introduce a novel paradigm, Magnetic Resonance Fingerprinting (MRF) that permits the non-
invasive quantification of multiple important properties of a material or tissue simultaneously
through a new approach to data acquisition, post-processing and visualization. MRF provides a
new mechanism to quantitatively detect and analyze complex changes that can represent physical
alterations of a substance or early indicators of disease. MRF can also be used to specifically
identify the presence of a target material or tissue, which will increase the sensitivity, specificity,
and speed of an MR study, and potentially lead to new diagnostic testing methodologies. When
paired with an appropriate pattern recognition algorithm, MRF inherently suppresses measurement
errors and thus can improve accuracy compared to previous approaches.
Introduction
Magnetic Resonance (MR) techniques such as NMR spectroscopy and Magnetic Resonance
Imaging (MRI) are widely used throughout physics, biology and medicine because of their
ability to generate exquisite information about numerous important material or tissue
properties, including those reflective of many common disease states1-4. However, in
practice MR acquisitions are often restricted to a qualitative or “weighted” measurement of a
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limited set of these properties; the MR signal intensity is almost never quantitative by itself.
The same material can have different intensities in different data sets depending on many
factors, including the type and setup of the scanner, the detectors used, and so on. Because
of this, the quantitative analysis of MR results typically focuses on differences between
spectral peaks, spatial locations or different points in time. Even in clinical MRI today, one
typically refers to a tissue or material as being “hyperintense” or “hypointense” compared to
Address for Correspondence: Dr. Mark Griswold, Ph.D., Case Western Reserve University, 11100 Euclid Ave - Bolwell B121,
Cleveland, OH 44106, USA, [email protected], Phone: +1-216-844-8085.
Author Contributions:
Dan Ma: Concept development, technical implementation, data collection and analysis, manuscript development and editing.
Vikas Gulani: Concept development, manuscript development and editing.
Nicole Seiberlich: Concept development, manuscript development and editing.
Kecheng Liu: Concept development, technical implementation, manuscript development and editing.
Jeffrey Sunshine: Concept development, manuscript development and editing.
Jeffrey Duerk: Concept development, manuscript development and editing.
Mark Griswold: Concept development, data collection and analysis, manuscript development and editing.
Ma et al. Page 2
another area, which may not provide a quantitative indication of the severity of the
differences, and may have reduced sensitivity to global changes. Thus robust, fully
quantitative multiparametric acquisition has long been the goal of research in MR5-8.
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Here we introduce a novel paradigm, Magnetic Resonance Fingerprinting (MRF) that may
overcome these constraints by taking a completely different approach to data acquisition,
post-processing and visualization. Instead of using a repeated, serial acquisition of data for
the characterization of individual parameters of interest, MRF uses a pseudorandomized
acquisition that causes the signals from different materials or tissues to have a unique signal
evolution or “fingerprint” that is simultaneously a function of the multiple material
properties under investigation. The processing after acquisition involves a pattern
recognition algorithm to match the fingerprints to a predefined dictionary of predicted signal
evolutions. These can then be translated into quantitative maps of the MR parameters of
interest.
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MRF is related to the concept of compressed sensing (CS)9-12, and shares many of its
predicted benefits. For example, preliminary results show that MRF could acquire fully
quantitative results in a time comparable to a traditional qualitative MR scan, without the
high sensitivity to measurement errors found in many other fast methods. Most importantly,
MRF has the potential to quantitatively examine many MR parameters simultaneously given
enough scan time, while current MR techniques can only examine a limited set of
parameters at once. Thus MRF opens the door to computer-aided multiparametric MR
analyses, similar to genomic or proteomic analyses, that could detect important but complex
changes across a large number of MR parameters simultaneously. When an appropriate
pattern recognition algorithm is used, MRF also provides a new and more robust behavior in
the presence of noise or other acquisition errors that may lead to the near complete
suppression of deleterious effects stemming from these factors. While we focus on
demonstrating the feasibility for MRI in this study, it is rather straightforward to translate
these results to other MR fields, such as multiparametric NMR spectroscopy, dynamic
contrast enhanced MRI (DCE-MRI) and dynamic susceptibility contrast MRI(DSC-MRI)13.
After the data are acquired, the separation of the signal into different material or tissue types
can be achieved through pattern recognition. In its simplest form, this process is analogous
to matching a person’s real fingerprint to a database. Once a match is made, a host of
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additional information about the person such as name, address and phone number can be
obtained simultaneously once the fingerprint sample is identified. In MRF, this pattern
recognition can take place through many means. In the current implementation, we construct
a dictionary that contains signal evolutions from all foreseeable combinations of materials
and system-related parameters. For example, T1, T2, off-resonance frequency are included in
this study, or other properties such as diffusion and magnetization transfer (MT) using the
well-established Bloch equation formalism of MR21,22. Once this dictionary of possible
signal evolutions is generated, a matching or pattern recognition algorithm23,24 is then used
to select a signal vector or a weighted set of signal vectors from the dictionary that best
correspond to the observed signal evolution. All the parameters that were used to build this
signal vector in the dictionary can then be retrieved simultaneously. At present, the
calculation of a complete dictionary containing the realistic range of T1, T2 and off-
resonance requires only a few minutes on a modern desktop computer.
It should be noted that there are near infinite possibilities for MRF-compatible pulse
sequences. Other MR parameters of interest can be investigated by identifying pulse
sequence components that impart differential sensitivity to the parameters of interest.
Moreover, different components can be varied simultaneously, adding the potential for a
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highly efficient experimental design that allows almost any material characteristic visible
using MR to be analyzed in a quantitative way using MRF.
Figure 2a and b show the simulated signal evolution curves that would be expected from
four commonly encountered tissues of the brain (fat, White Matter (WM), Gray Matter
(GM) and Cerebral Spinal Fluid (CSF)) using the schematic implementation shown in
Figure 1c and d, respectively. Each tissue type has characteristic T1 and T2 values and thus
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each signal evolution has a different shape, which confirms that it is possible to satisfy this
fundamental assumption in MRF. Note also that the signal levels in these evolutions
represent a large fraction of the equilibrium magnetization (which is normalized to 1 in these
figures.) Conventional spoiled steady-state sequences typically generate signal levels
corresponding to 1-10% of the equilibrium magnetization. Figure 2c and 2d show an
acquired signal evolution curve from fully sampled phantom experiments and its match to
the dictionary by using the acquisition pattern shown in Figure 1c and 1d, along with the
recovered T1, T2, proton density (M0) and off-resonance frequency values. MRF was able to
match the signal to the corresponding dictionary entry and obtain the same T1 and T2 values
from both sequence patterns. A video of the signal evolution from a fully sampled in vivo
scan is also included (Supplementary Movie1), demonstrating the oscillating nature of the
MRF signal observed in vivo.
recognition in a setting where the form of all predicted signal evolutions is known, MRF
should be less sensitive to errors during the measurement. This is similar to conventional
fingerprint recognition techniques which often contend with smudges and partial fingerprint
information. In particular, the interaction of the temporal and spatial incoherence possible in
MRF provides new opportunities to accelerate image acquisition through rejection of spatial
undersampling errors. In order to test the limits of this acceleration, the same MRF sequence
as shown in Figure 1a-c was modified to use only one spiral readout in each acquisition
block. Therefore, the data collected are only 1/48th of the normally required data at each
time point, resulting in a total acquisition time of 12.3 seconds corresponding to 1000
sampled time points. (See Figure 3a and Supplementary Movie 2.) The signal evolutions
from all 1000 undersampled time points were used directly to match one entry from the
dictionary to quantify T1, T2, M0 and off-resonance simultaneously, as shown in Figure 3b.
Because these errors are incoherent with the expected MRF signals, they are largely ignored
by the following processing steps. Figures 3c-f show that high quality estimates of the MR
parameters are generated even with this significant level of undersampling. WM, GM and
CSF regions were then selected from the resultant maps. The mean T1 and T2 values
obtained from each region were listed in the Table 1 and are within the range of previously
reported literature values 29-32. The shortened T2 value in CSF is likely due to out-of-plane
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The accuracy and efficiency of the MRF acquisitions were compared with alternative
mapping strategies: standard spin echo sequences (SE)34 as well as modern rapid combined
T1 and T2 mapping methods DESPOT1 and DESPOT2 (Driven Equilibrium Single Pulse
Observation of T1 and T2, respectively)30 using manufactured agar phantoms. Figure 5a
compares the phantom T1 and T2 values from these methods. The concordance coefficient
correlations for T1 and T2 between MRF and spin-echo sequence were 0.988 and 0.974,
respectively. The concordance coefficient correlations for T1 and T2 between DESPOT and
spin-echo sequence were 0.956 and 0.914, respectively. The high concordance correlation
coefficients indicate that both methods are in good agreement with standard spin echo
measurements and that MRF shows a better accuracy than DESPOT1 and DESPOT2.
The theoretical comparison of the efficiency from various mapping methods has been
presented by Grawley35 and Deoni36 and is based on a measure of precision per square root
of scan time. In those publications, DESPOT1 and DESPOT2 were shown to have greater
efficiency than all previously known conventional and accelerated mapping strategies36. As
can be seen in Figure 5b, MRF outperforms both DESPOT1 and DESPOT2 by an average
factor of 1.87 and 1.85, respectively. For example, at a T1 of ~1280 ms, MRF shows an
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average efficiency for estimation of T1 of 24.2, while DESPOT1 has an average efficiency
of 10.89. This means that for this T1 value, MRF achieves a precision of +/− 15.2 ms (or
1.2%) in 12 seconds of scan time, while the precision in DESPOT1 would be +/−33.9 ms (or
2.6%) for the same scan time. The DESPOT methods apparently display higher efficiency
from the single phantom with T1 of 360 ms and T2 of 53 ms. However, in this one particular
phantom, DESPOT overestimated the values of T1 and T2 by 23% and 42% respectively
compared to the standard values, as can be seen in Figure 5a, thus causing an erroneous
increase in the apparent efficiency. Note that these efficiency estimates do not include the
waiting times between the acquisition of the different sub-sequences in DESPOT, nor do
they include the time required to reach steady state during each acquisition, and thus should
be viewed as conservative estimates of MRF’s performance when compared to DESPOT1 or
2.
Because there is no steady state in the signal evolution from MRF, new information will be
continuously added by longer acquisitions. Figure 5c and d illustrates the changes of mean
and standard deviation as different acquisition times were used to quantify T1 and T2, with a
clear trend towards lower error at longer acquisition times. Thus one can select a tradeoff
between precision and scan time.
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approximately 1.8 times higher than the DESPOT methods, which were previously the most
efficient methods for the measurement of relaxation parameters. Thus the direct prediction
of the oscillating, incoherent signal evolutions through the Bloch simulation provides us the
potential to obtain new quantitative information that is impractical today because of the
prohibitively long scan times required, especially in biological samples and patients.
As demonstrated by the results shown here, MRF has the potential to significantly reduce
the effects of errors during acquisition through its basis in pattern recognition. Acquisition
errors may globally reduce the probability of a match of an observed signal to any given
fingerprint, but as long as the errors do not cause another fingerprint to become the most
likely match, the correct quantitative identification will still be made. Ideally, the sequence
pattern will be designed so that the various fingerprints from different tissues and materials
are as independent as possible, thus ensuring this robustness against motion and other
practical errors.
larger systems. MRF provides a route to model and account for system imperfections such
as B0 and B1 field inhomogeneities by adding these parameters into the dictionary
simulation. Since both MRF and DESPOT2 are based on a bSSFP sequence, which is
known to be sensitive to field inhomogeneities30,37, Supplementary Figure 2 compares the
T2 maps acquired from MRF and DESPOT2 from an in vivo scan. Since off-resonance is
not taken into account in the DESPOT2 model, the T2 map from DESPOT2 shows areas of
signal voids resulting from susceptibility effects at the air-tissue interfaces. MRF naturally
incorporates these effects into the fingerprints, and thus the maps generated by MRF do not
show these errors. Thus MRF could, for example, provide higher quality results using the
current generation of MR scanners. Alternatively MRF could also allow the design of lower
cost MR scanners that can provide the same quality as today’s high end systems through
application of MRF models.
Because of its ability to provide quantitative results across many parameters simultaneously,
MRF could lead to the direct identification of a material, tissue or pathology based solely on
its fingerprint. For example, many cancer cells show changes in multiple MR parameters
(e.g. T1, T2, self-diffusion tensor, etc), a combination (though no single parameter) of which
could potentially characterize them as different from all surrounding normal tissue types,
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and thus potentially separable. In an ideal situation, each given material, tissue, or pathology
would have its own signal evolution which would be orthogonal to all other signal
evolutions. The MRF concept also implies that completely different acquisition schemes are
possible in cases where one is only interested in the presence or absence of a particular
material or disease state. For example, one could do a very rapid MRF scan of a bulk area of
material or tissue and compare the measured signal evolutions against the set of known
states of interest. This measurement could either indicate the presence of the material or
disease of interest, or indicate its absence within a margin of error. This feature could result
in very rapid and accurate screening procedures. In particular, this feature may help to relax
the required spatial resolution of an MRI exam, thus increasing the speed, and potentially
reducing the cost of an MRI exam. A preliminary example of this kind of visualization is
shown in the Supplemental Material Section 3. Using the MRF concept, the operation of the
MR unit will also be greatly simplified, since the ‘all in one’ scan concept of MRF has the
potential to reduce the dozens of parameters currently presented to the MR operator to a
simple ‘scan’ button.
It is important to note that the proof-of-principle implementation of MRF shown here is but
one of the many possibilities that could be employed for this technique and both the
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it is well known that taking full advantage of undersampling in all three spatial dimensions
gives higher performance than a 2D acquisition due to the reduced power of the resulting
errors at any given undersampling factor47. Thus a combination of an optimized 3D MRF
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pulse sequence with parallel imaging and more advanced pattern matching algorithms will
allow realization MRF in very short scan times.
Methods
1. Sequence Design
After an initial inversion pulse, the first sequence pattern shown in Figure 1c used a
pseudorandomized series (Perlin Noise48) of flip angle (FA) and a random repetition time
(TR) between 10.5 ms and 14 ms based on a uniform random number generator. A linear
ramp was added to the FA train since we have seen that this can increase differential
sensitivity to both T1 and T2.
The second FA pattern in Figure 1d used a series of repeating sinusoidal curves with a
period of 250 TRs and alternating maximum flip angles. In the odd periods, the flip angle is
each of the periods to allow for both differential magnetization recovery according to T1 and
differential signal decay according to T2. In this case, the TR was a Perlin noise pattern. The
RF phase for both of the patterns in Figure 1 alternated between 0 and 180° on successive
RF pulses.
The variable density spiral-out trajectory was designed to have 5.8 ms readout time in each
TR and to have zero and first moment gradient compensation using minimum-time gradient
design49. This trajectory required one interleaf to sample the inner 10×10 region, while 48
interleaves were required to fully sample the outer portions of k-space. During acquisition,
the spiral trajectory rotated 7.5° from one time point to the next, so that each time point had
a slightly different spatial encoding.
2. Dictionary Design
The dictionary used in the matching algorithm was simulated using MATLAB (The
MathWorks, Natick, MA). Signal time courses with different sets of characteristic
parameters (T1, T2 and off-resonance) were simulated. The ranges of T1 and T2 for the in
vivo study were chosen according to the typical physiological limits of tissues in the brain:
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T1 values were taken to be between 100 and 5000 ms (in increments of 20 ms below a T1 of
2000 ms and in an increment of 300 ms above.) The T2 values included the range between
20 and 3000 ms (with an increment of 5 ms below a T2 of 100 ms, an increment of 10 ms
between 100 ms and 200 ms and an increment of 200 ms above a T2 of 200 ms.) Since MR
is sensitive to parts per million (ppm) level deviations in the B0 field, different off-
resonance frequencies (1 Hz increment between ±40 Hz, 2 Hz between ±40 to ±80 Hz, 10
Hz between ±90 to ±250 Hz and 20 Hz between ±270 to ±400 Hz) were simulated for each
combination of T1 and T2 parameters to incorporate the effects of signal evolutions in
different B0 fields. A total of 563,784 dictionary entries, each with 1000 time points, were
generated in 399 seconds on a standard desktop computer. One dictionary entry was selected
for each measured pixel location using template matching. In this case, the vector dot-
product was calculated between the measured time course and all dictionary entries
(appropriately normalized to each having the same sum squared magnitude) using the
complex data for both. The dictionary entry with the highest dot-product was then selected
as most likely to represent the true signal evolution. The proton density (M0) of each pixel
was calculated as the scaling factor between the measured signal and the simulated time
course from the dictionary. For this experiment, four parameters were retrieved
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simultaneously from each of the 128×128 pixels using MRF. This calculation required about
3 minutes on a standard desktop computer.
3. Data Acquisition
All MRI and MRF data were acquired on a 1.5T whole body scanner (Siemens Espree,
Siemens Healthcare, Erlangen, Germany) with a 32 channel head receiver coil (Siemens
Healthcare, Erlangen, Germany). A square field of view of 300 × 300 mm2 was covered
with a matrix of 128×128 pixels. The slice thickness was 5 mm. Images from each
acquisition block were reconstructed separately using non-uniform Fourier transform
(NUFFT)50. The resultant time series of images was used to determine the value for the
parameters (T1, T2, M0 and off-resonance) as described above.
In vivo experiments were performed with IRB guidelines, including written informed
consent. For the fully sampled spiral acquisition shown in Supplementary Movie1, 48
repetitions were acquired, each with a different interleaf of the total acquisition. A recovery
time of 5 seconds was used in between various acquisitions and this was taken into account
in the simulated dictionary.
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For the phantom study shown in Figure 2 and 4, eight cylindrical phantoms were constructed
with varying concentrations of GdCl3 (Aldrich) and agarose (Sigma) to yield different T1
and T2 values ranging from 67 to 1700 ms and 30 to 200 ms, respectively. Standard Spin
Echo (SE) sequences were used to quantify T1 and T2 separately (T1 quantification: 13 TRs
ranging from 50 to 5000 ms, TE = 8.5 ms, total acquisition time = 33.4 minutes; T2
quantification: Spin Echo sequences with TEs = [15 30 45 60 90 150 200 300 400] ms, TR =
10000 ms, total acquisition time = 3.2 hours.). T1 values were calculated pixel-wise using a
standard three-parameter nonlinear least squares fitting routine to solve the equation: S(TR)
= a + beT R/T1. T2 values were determined in a pixel-wise fashion using a two-parameter
nonlinear least squares fitting routine to solve the equation S(TE) = ae−T E/T2, DESPOT1
and DESPOT2 sequences using a fully sampled spiral readout were implemented based on
the acquisition values from Deoni et al30: DESPOT1: FA: 4° and 15°, TR:13.6 ms,
DESPOT2: FA: 15° and 55°, TR=10.8 ms. The T1 and T2 values were calculated from the
equations provided by Deoni et al 30. A 20 s waiting period was used in between the
different acquisitions. The initial 10 s of data acquisition was not used in order to ensure that
the signal was in steady-state for each of the DESPOT acquisitions. In the following analysis
of efficiency, only the pure time of data acquisition for the steady-state DESPOT images is
used. For DESPOT1 this was 1.27 s and for DESPOT2 it was 2.29 s (which includes the
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where Y1 and Y2 denotes the T1 or T2 values from two different methods, n is the number of
where TnNR is the T1 or T2 to noise ratio (defined as the T1 or T2 value divided by the
estimated error). Tseq is the total acquisition time for MRF, and the relevant acquisition
times for DESPOT1 and DESPOT2 (where the waiting times required for the approach to
steady state and the time between each of the DESPOT1 and DESPOT2 scans to allow for
complete recovery of magnetization were ignored.)
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Supplementary Material
Refer to Web version on PubMed Central for supplementary material.
Acknowledgments
Support for this study was provided by NIH R01HL094557 and Siemens Healthcare. The authors also wish to thank
H. Saybasili and G. Lee for their technical assistance during the implementation of these concepts. We also wish to
thank M. Lustig and W. Grissom for critical discussions regarding this work. Finally, we wish to thank A. Exner, S.
Brady-Kalnay, E. Karathanasis, E. Lavik, and H. Salz for their assistance in preparing the manuscript.
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(a and b) Simulated signal evolution curves corresponding to four normal brain tissues
using the sequence patterns in Figure 1c and 1d, respectively as a fraction of the equilibrium
magnetization. The curve from white matter with off-resonance is also plotted. (c and d)
Measured signal evolutions from one of eight phantoms using different sequence patterns
and their dictionary match. The estimated T1, T2, and off-resonance are (340 ms, 50 ms, −4
Hz) and (340 ms, 50 ms, −13 Hz) in (c) and (d), respectively. The plots are normalized to
their maximum value.
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Figure 5. Accuracy, Efficiency and Error estimation for MRF and DESPOT
The T1 and T2 values retrieved from MRF from eight phantoms were compared with those
acquired from DESPOT1(a), DESPOT2(b) and a standard spin-echo sequence. The
efficiency of MRF was compared to DESPOT1(c) and DESPOT2(d) at different T1 and T2
values. MRF has an average of 1.87 and 1.85 times higher efficiency than DESPOT1 and
DESPOT2, respectively. (e) and (f) show the means and standard deviations of T1 and T2 as
a function of acquisition time. Error bars represent the standard deviations of the results over
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a 25-pixel region in the center of each phantom, which are smaller than the symbols for most
MRF results.
Table 1
In vivo data: Comparison of MRF results and reference values in different brain regions
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T1 (ms) T2 (ms)