Download Navigator artifact reduction in 3D late gadolinium enhancement

Navigator artifact reduction in 3D late gadolinium
enhancement imaging of the atria
Jennifer Keegan,1 Peter Drivas,1 David N Firmin.1,2
1
Cardiovascular Biomedical Research Unit, Royal Brompton and Harefield NHS Trust, London,
and 2Imperial College of Science Technology and Medicine, London.
Running title: Navigator artifact reduction in 3D LGE imaging
Word count: 3221
Key words: late gadolinium enhancement imaging, navigator, artifact, pulmonary veins
Address for correspondence:
Dr Jennifer Keegan
Cardiovascular Magnetic Resonance
Royal Brompton Hospital
Sydney Street, London SW3 6NP
Email: [email protected]
Tel: 020 7351 8800
Fax: 020 7351 8816
Abstract
Purpose: Navigator-gated 3D late gadolinium enhancement (LGE) imaging demonstrates
scarring following ablation of atrial fibrillation. An artifact originating from the slice-selective
navigator-restore pulse is frequently present in the right pulmonary veins (PVs), obscuring the
walls and making quantification of enhancement difficult. We describe a simple sequence
modification to greatly reduce or remove this artifact.
Methods: A navigator-gated inversion-prepared gradient echo sequence was modified so that
the slice-selective navigator-restore pulse was delayed in time from the non-selective
preparation (NAV-restore-delayed). Both NAV-restore-delayed and conventional 3D LGE
acquisitions were performed in 11 patients and the results compared.
Results: One patient was excluded due to severe respiratory motion artifact in both NAVrestore-delayed and conventional acquisitions. Moderate – severe artifact was present in 9 of
the remaining 10 patients using the conventional sequence and was considerably reduced when
using the NAV-restore-delayed sequence (ostial PV to blood pool ratio: 1.7+/-0.5 vs 1.1+/-0.2
respectively (p<.0001); qualitative artifact scores: 2.8+/-1.1 vs 1.2+/-0.4 respectively (p<.001)).
While navigator signal-to-noise ratio was reduced with the NAV-restore-delayed sequence,
respiratory motion compensation was unaffected.
Conclusions: Shifting the navigator-restore pulse significantly reduces or eliminates navigator
artifact. This simple modification improves the quality of 3D LGE imaging and potentially aids
late enhancement quantification in the atria.
Introduction
The most prevalent form of cardiac rhythm disturbance is atrial fibrillation (AF)1 which frequently
originates from ectopic beats arising from the pulmonary veins.2 Complete electrical isolation of
the pulmonary veins using radio frequency ablation under X-ray fluoroscopy is the most
common treatment,3 but repeat procedures are often necessary due to incomplete isolation.4
Scarring following radio frequency ablation of AF has been demonstrated5,6 and quantified7-9
using 3D late gadolinium enhancement (LGE) imaging and the spatial distribution of scarring
has been shown to be related to the likelihood of recurrence.10 LGE imaging therefore has a
promising role in the assessment of RF ablation in the AF patient11 and also in directing the
electrophysiologist to regions of incomplete scarring in repeat studies.12
LGE imaging is generally performed using a non-selective inversion-recovery (IR) prepared
segmented gradient echo sequence with the inversion time (TI) set to null the signal from
normal myocardium.13 While conventional 2D LGE imaging is performed during breathholding,14 high resolution 3D coverage of the atria requires that imaging is performed during
free-breathing using diaphragmatic navigators to restrict the respiratory motion to a narrow
acceptance window around the end-expiratory pause position.15,16 For both pencil-beam and
crossed-pairs navigators,17 a selective navigator-restore pulse18 is applied immediately after the
non-selective inversion preparation (Figure 1(a)) to avoid the substantial degradation of the
navigator signal-to-noise ratio which would otherwise compromise the accuracy with which the
diaphragm position can be determined. This navigator-restore pulse also re-inverts blood which
flows into the right pulmonary veins and atria during the inversion time and can result in a
characteristic artifact of high signal intensity in the region of the PVs. The intensity and extent of
this artifact depends on the type of navigator implemented (crossed-pairs or 2D RF pulse), its
exact positioning, the slice thickness of the selective navigator-restore and on the amount
pulmonary vein blood flow between the navigator-restore and the data acquisition. It frequently
obscures the ostia of the veins and the nearby atrial wall, making both qualitative and
quantitative assessment of enhancement difficult. While it has been reduced by removing the
navigator-restore pulse and using a following navigator for respiratory gating, 7 this precludes the
use of prospective tracking or phase ordering techniques which have recently been used to
reduce acquisition durations.19 Respiratory bellows have also been suggested as an alternative
to navigator-gating.20 Alternatively, a 5cm thick diaphragmatic slab projection navigator has
been proposed21 which is implemented without the artifact-forming navigator-restore pulse.
However, the sharpness of the navigator edge is reduced by receiving signal from such a large
slab (which may compromise the accuracy of the navigator edge detection) and the
effectiveness of the respiratory gating is further reduced by the delay of 100ms which is required
following the slab navigator.22 We propose a simple modification to the original navigator-gated
sequence which reduces or eliminates the inflow artifact and which allows prospectively gated
3D LGE imaging without these drawbacks.
Methods
A standard crossed-pairs navigator-gated inversion-prepared segmented gradient echo
sequence (TR = 2.9ms) (Fig 1(a)) was modified so that the slice-selective navigator-restore
pulse is shifted in time from the non-selective IR preparation: instead of being immediately
following the non-selective inversion pulse, it is delayed by 100 – 200 ms (Fig 1(b)). The benefit
of this is two-fold: (i) because the blood longitudinal magnetisation has been decaying towards
zero, it results in a re-inverted blood magnetisation that is lower (so that the intensity of any
artifact is reduced) and (ii) any blood which is re-inverted has less time to flow into the atria
resulting in any artifact being shifted away from the PV ostia.
Both conventional and NAV-restore-delayed navigator gated 3D acquisitions were performed in
11 patients in a random order following standard clinical 2D LGE imaging on a Siemens Skyra 3
Tesla scanner (Siemens Medical Systems, Erlangen, Germany). All subjects provided written
informed consent according to the local ethics committee. The 3D imaging was started
approximately 15-20 minutes after gadolinium administration (Gadovist - gadobutrol,
0.1mmol/kg body weight). The crossed-pair navigator parameters are as follows: TE = 20 ms,
TR = 30 ms, thickness 10 mm, navigator feed-back time 10 ms. The navigator restore thickness
was 10 mm. 3D LGE data (TE = 1.3 ms, TR = 2.9 ms) were acquired in the transverse plane
(field of view = 400 mm) as follows: 12 slices at 2mm x 2mm x 4mm, reconstructed to 24 slices
at 1mm x 1mm x 2mm, generalised autocalibrating partially parallel acquisition (GRAPPA) x2,
acquisition window 140ms, alternate R-wave gating, chemical shift fat suppression, flip angle
20o, left-right phase encoding, crossed-pairs navigator positioned over the dome of the right
hemi-diaphragm with nominal navigator acceptance window size of 6mm. Forty eight ky lines
were acquired per cardiac cycle with centric coverage. Kz coverage was also centric, with all k y
phase encodings for a given kz phase encoding step being acquired before kz was changed.
The nominal acquisition duration (assuming 100% respiratory efficiency) was 114 cardiac
cycles. While the spatial resolution and acquisition window in the acquired datasets are poorer
than those required for detailed atrial LGE imaging,5-10 they are sufficient to clearly demonstrate
the degree and extent of the navigator artifact in a reasonably short imaging time so that
acquisitions both with and without the sequence modification could be obtained in each subject
before excessive gadolinium wash-out. The inversion time was determined by a scout 2D
acquisition prior to each 3D scan. Longitudinal magnetisation recovery during the navigatorrestore delay implemented in the NAV-restore-delayed sequence reduces the amount of
longitudinal magnetisation re-inverted by the navigator-restore pulse and hence, the signal-tonoise ratio (SNR) in the navigator trace is reduced. The SNR reduction for a given navigatorrestore delay is dependent on the inversion time implemented. In this study, the navigatorrestore delay was 100 – 200ms and was the maximum possible that still enabled the detected
diaphragm edge position to smoothly follow the respiratory motion. Raw data were stored with
each acquisition to allow subsequent analysis of the effects of SNR reduction on the accuracy of
diaphragm edge detection in the navigator trace. In addition, sequence simulations were also
performed (MATLAB version 7 (Mathworks, Natick, MA)) to study the effect of increasing
navigator-restore-delay on the longitudinal magnetisation, Mz, of liver which determined the
SNR of the navigator trace. These simulations were performed at four heart rates (ranging from
50 – 100 beats per minute) and assumed that the T1 of liver post-gadolinium was the same as
that of normal myocardium (423 ms at ~20 minutes following .1 mmol/kg gadobutrol
administration.)19 For each heart rate, the optimal inversion time required to null normal
myocardium was determined by solving the Bloch equations. For the sequence used in vivo (as
described above), the navigator TR is 30 ms, navigator feedback time is 10 ms and the duration
of chemical shift fat suppression preparation is 20 ms. Consequently, the 900 excitation of the
crossed-pairs navigator is output approximately 60 ms prior to the time required to null normal
tissue. For each heart rate and each navigator-restore-delay (ranging from 0 – 150 ms in
increments of 25 ms), the Mz of liver was consequently calculated 60 ms prior to the optimal
inversion time. The ratio of this Mz with navigator-restore-delay to that without was plotted as a
function of navigator-restore-delay to indicate the relative change in navigator SNR as the
navigator-restore-delay increased.
Image Analysis
In images acquired with the conventional sequence, regions of interest were drawn around any
ostial right superior or inferior pulmonary vein artifact and also - as a reference - in the blood
pool in the descending aorta in the same image. The regions of interest were copied to the
corresponding images obtained with the NAV-restore-delayed acquisition. The ratio of
pulmonary vein signal to reference blood signal (PVratio) was determined for images acquired
with both NAV-restore-delayed and conventional sequences and compared using a paired ttest. In addition, consensus subjective PV image artifact scores (AS: 1=none, 2 = mild, 3 =
moderate, 4 = severe) were determined by two blinded observers and compared using paired
Wilcoxon analysis. The effect of reduced SNR in the navigator trace on the appearance of
respiratory motion artifacts was assessed on the same 4-point scale by the same two observers
and the consensus scores compared with paired Wilcoxon testing.
Navigator Analysis
In addition, offline reconstructions of the navigator raw data were performed in MATLAB version
7 (Mathworks, Natick, MA). The traces were smoothed (using a running average of 7 navigator
points) and scaled to a maximum of 100. For each subject, in an end-expiratory reference
navigator trace, the mean and standard deviation (SD) of the signal intensity in a region of the
lung was determined, together with that in a region in the liver, just adjacent to the diaphragm
edge. This lung region of interest was positioned as best possible to avoid vessels and other
structures and, in the absence of a true background region of interest in the navigator data,
approximated to noise. The navigator SNRs in the NAV-restore-delayed and conventional
acquisitions were determined as the ratio of the mean liver signal to the SD of the lung signal in
the navigator traces of the NAV-restore-delayed and conventional acquisitions respectively and
compared with paired t-testing. For data acquired with the conventional sequence in each
patient, the first 25 navigator traces were analysed and the diaphragm edge position for each
trace was determined by a least squares fit algorithm (also over 7 navigator points), as used by
the online navigator reconstruction software. This method of edge detection23 has been shown
to be highly resistant to noise. Random Gaussian noise was then added to the navigator trace
to reduce the SNR to the same level as that in the data acquired with the corresponding NAVrestore-delayed sequence and the diaphragm edge detection repeated. The diaphragm edge
positions with and without the addition of noise were compared using the Pearson correlation
coefficient and the mean and standard deviation of the signed differences calculated.
Results
All 11 patients completed the study although one subject had severe respiratory motion
ghosting extending across the PVs (in both sequences) and was excluded from further analysis.
In two further subjects, the imaging slab failed to cover the right superior PV (RSPV) so that
only the right inferior PV (RIPV) could be analysed. In the NAV-restore-delayed sequence, the
navigator-restore delays implemented were 100 ms (in 5 cases), 150ms (in 4 cases) and 200
ms (in 1 case). The inversion time for nulling of normal left ventricular myocardium with single
R-wave gating was 278 +/- 44 ms. The implementation of the navigator-restore delay did not
impact upon the acquisition durations (127 +/- 33 s and 130 +/- 47 s for the conventional and
NAV-restore-delayed sequences respectively, p = ns.)
Image Analysis
Moderate – severe navigator artifact was present in either the superior or inferior (or both) PVs
in 9 of the remaining 10 conventional acquisitions and was considerably reduced, or eliminated,
when using the modified sequence with a navigator-restore delay. The PVratio was significantly
reduced when using the NAV-restore-delayed sequence (1.1 +/- 0.2 vs 1.7 +/- 0.5, p < .0001) as
were the consensus artifact scores (1.2 +/- 0.4 vs 2.8 +/- 1.1, p < .001). The degree of navigator
artifact seen was similar for both the RIPV and RSPV when using the conventional sequence
(PVratio: 1.8 +/- 0.6 vs 1.7 +/- 0.4 respectively, p = ns; consensus artifact score: 2.8 +/- 1.2 vs 2.8
+/- 1.0 respectively, p = ns) and when using the NAV-restore-delayed sequence (PVratio: 1.1 +/0.1 vs 1.2+/- 0.2 respectively, p = ns; consensus artifact score: 1.2 +/- 0.4 vs 1.1 +/- 0.4
respectively, p = ns). In no patient was the image quality obtained with the NAV-restore-delayed
sequence worse than that with the conventional sequence. The consensus artifact score and
the PVratio did not depend upon the navigator-restore delay value (artifact score: 1.1 +/- 0.4 vs
1.2 +/- 0.4 for patients with navigator-restore delay values of 100 ms and >= 150 ms
respectively (p = ns); PVratio: 1.05 +/- 0.16 vs 1.13 +/- 0.29 for patients with navigator-restore
delay values of 100 ms and >= 150 ms respectively (p = ns)).
Examples of NAV-restore-
delayed and conventional acquisitions in three patients are shown in Figure 2, together with the
PVratio and consensus artifact scores.
The percentage navigator SNR reduction did not depend upon the navigator-restore delay value
(41% +/- 16% vs 41% +/- 5% for patients with navigator-restore delay values of 100 ms and >=
150 ms respectively (p = ns).Qualitative analysis of the subjective respiratory motion artifact
scores showed no significant differences between the techniques (1.7 +/- 0.7 vs 1.7 +/- 0.7, p =
ns).
Navigator Analysis
Off-line analysis showed that, as expected, navigator SNR is significantly lower when using the
NAV-restore-delayed sequence (9.7 +/- 4.0 vs 24.9 +/- 11.6, p < 0.001) although the navigator
edge remains well preserved. Figures 3(a) and (e) show an end-expiratory navigator trace from
the conventional and NAV-restore-delayed acquisitions respectively in an example subject. The
SNR in these navigator traces is 25.3 and 11.9 respectively. Figure 3(b) - (d) show the navigator
trace in 3(a) (conventional sequence) with increasing amounts of random Gaussian noise
reducing the SNR to 10.2, 7.1 and 5.3 respectively. Figure 3(f) – (g) show plots of the
diaphragm positions detected in the first 25 cycles of the original trace (Figure 3(a)) against
those measured with increased noise levels (Figure 3(b), 3(c) and 3(d) respectively). They show
that the least squares fit algorithm used for edge detection is relatively insensitive to added
noise, with high correlation coefficients for all noise levels, including levels greater than those
observed in the NAV-restore-delayed acquisitions (Figure 3(e))). Figure 4 shows a plot of
diaphragm edge position in the first 25 cycles of the conventional acquisitions plotted against
the diaphragm edge positions obtained in noisier versions of those navigator traces for all
patients, in each case the amount of noise added resulting in similar navigator SNRs as in the
NAV-restore-delayed acquisitions. The addition of noise to the level of that seen in the NAVrestore-delayed sequence resulted in very little difference to the detected navigator edge
positions with the mean difference between the diaphragm positions measured from the two
datasets being -0.08 +/- 0.66 mm with the Pearson correlation coefficient being 0.99.
Discussion
We have presented a simple modification to a navigator-gated inversion-prepared 3D LGE
sequence which significantly reduces or eliminates pulmonary vein artifact. The technique is
applicable to both crossed-pairs and 2D pencil beam navigator techniques (both of which
require a navigator-restore pulse) and while the SNR in the navigator traces is reduced, we
have shown that this does not impact on the accuracy of the navigator edge detection nor on
the subjective assessment of the respiratory motion suppression. Unlike other techniques,21 the
time between the navigator and the imaging segment is unchanged so that the navigator
position continues to accurately reflect the diaphragm position at the start of the data segment
acquisition.
The extent and severity of the navigator artifact in standard 3D LGE imaging depends upon the
amount of pulmonary artery blood flow occurring between the navigator-restore pulse and the
data acquisition,24 on the pulmonary vein anatomy and on the positioning of the navigatorrestore pulse (which determines the amount of pulmonary blood which is re-inverted). As such,
it is highly subject-specific but in this study, it was seen in either the RSPV or the RIPV or both
in 9 out of 10 subjects with moderate – severe severity. Using the NAV-restore-delayed
sequence, this artifact was completely eliminated in six subjects and reduced to mild (artifact
score = 2) in the remaining three. While elimination of the navigator artifact could be achieved
by removing the navigator-restore pulse and using a following navigator,7 this would not allow
the use of
real-time phase ordering and windowing techniques, including the continuously
adaptive windowing strategy (CLAWS) which has recently been shown to be beneficial in
reducing the acquisition durations of long 3D LGE whole-heart acquisitions by 26%.19 Similarly,
real-time slice following techniques would not be possible with a following navigator. For centric
k-space ordering, as implemented here, a following navigator would also have the additional
disadavantage of being acquired further from the centre of k-space which would lead to reduced
respiratory motion compensation.22
An alternative approach to reducing the magnitude of the navigator artifact could be to decrease
the navigator slice thickness and the thickness of the navigator-restore pulse as this would also
reduce the amount of longitudinal pulmonary vein blood magnetisation being re-inverted.
However, with this approach, any re-inverted blood would still have time to flow into the
pulmonary veins and result in artifact, although this would be at a reduced intensity compared to
acquisitions with conventional navigator slice thicknesses. Our technique has the advantage of
not only re-inverting less pulmonary vein blood magnetisation but also allowing less time for that
re-inverted blood to flow into the pulmonary veins. Any residual artifact is therefore moved away
from the pulmonary vein ostia.
The choice of navigator-restore delay depends on the SNR in the navigator trace which will
depend on many factors, including the field strength, the inversion time (which is dependent on
the RR interval, the amount of gadolinium contrast agent given, the time after gadolinium
administration and the clearance kinetics for that patient), the navigator cross-sectional area,
the type of navigator (crossed-pairs spin echo or 2D RF pulse), the coil configuration used and
the distance of the dome of the diaphragm from those coils. In this study, the navigator delay
was selected after visual inspection of the navigator traces to confirm that the navigator edge
position continued to smoothly track the respiratory position. The longer the delay, the shorter
the time period available for pulmonary blood affected by the navigator-restore pulse to flow into
the pulmonary veins (and cause artifact) but the greater the reduction in navigator SNR which
may compromise the accuracy of the edge detection. Figure 5 shows how the longitudinal
magnetisation of liver (and hence, navigator SNR) varies as a function of navigator-restore
delay. These simulations were performed for several RR intervals assuming that the T1 of liver
was the same as that of normal myocardium (424ms at ~20 minutes post gadolinium
administration19). They show that the longitudinal magnetisation decreases with increasing
navigator-restore delay, falling to 0.6 of the equilibrium value for a delay of 100ms and to 0.4 of
the equilibrium value for a delay of 150 ms at 60 beats/min. In our patients, the average SNR in
the navigator traces of the NAV-restore-delayed acquisitions was 41% of that in the
conventional acquisitions, and was not significantly different for those patients with a navigatorrestore delay of 100ms compared to those with a navigator restore delay of >=150ms.This nonsignificant difference is likely to be due to the fact that the patients’ heart rates in this study were
very variable (ranging from 44 - 92 beats per minute), as were the liver T1s (based on the wide
range of TIs required to null normal myocardium (240 – 360 ms)).
The degree of artifact reduction achieved by the NAV-restore-delayed sequence may be
reduced for faster heart rates as the navigator-restore delay that can be implemented is
reduced, as discussed above. However, while the lower navigator-restore delay values used at
fast heart rate would result in more blood being re-inverted (and potentially forming artifact), the
shorter inversion times required at faster heart rates mean that there is less time for this reinverted blood to flow into the pulmonary vein ostia. In practice then, the relationship between
artifact reduction and heart rate is complicated. In our study, the mean patient heart rate was 70
+/- 15 beats per minute (range: 44 – 92 beats per minute) and the NAV-restore-delayed
sequence achieved good artifact suppression regardless of the RR interval.
In this study, we typically found that a navigator-restore delay of 150ms allowed the detected
diaphragm position to smoothly track the respiratory motion. However, if it was deemed to be
too noisy, the navigator-restore delay could be reduced. As discussed above, with shorter
delays, residual artifact may still be present although it is reduced and shifted away from the
right pulmonary vein ostia (by an amount depending on pulmonary vein flow) and less likely to
impact on the visualisation of the pulmonary veins and atrium. This is demonstrated in Figure 6
where the results of acquisitions performed with navigator-restore delays of 0ms, 100ms and
150ms are shown. While this study was performed at 3 T, at lower field strength, inherently
reduced SNR may reduce the navigator-restore delay that can be implemented. However, as
discussed above, while this may result in less than complete removal of the navigator artefact,
any residual artefact will be shifted away from the pulmonary vein ostia. An automatic
determination of the navigator-restore delay based on the initial navigator SNR is highly feasible
and will be implemented in future work.
In conclusion, we have presented a simple sequence modification that improves the image
quality of 3D LGE imaging and which will improve automatic late enhancement quantification in
the atria.
Acknowledgement: This project was supported by Wellcome Trust Grant WT093953MA and
the NIHR Royal Brompton Cardiovascular Biomedical Research Unit. This report is independent
research by the National Institute for Health Research Biomedical Research Unit Funding
Scheme. The views expressed in this publication are those of the author(s) and not necessarily
those of the NHS, the National Institute for Health Research or the Department of Health.
Legends
Figure 1: (a) standard navigator gated sequence with the slice-selective navigator-restore
immediately after the non-selective inversion recovery preparation and (b) with a delay. The
inversion time (TI) is the same for both, as is the timing of the data acquisition within the RR
interval. The reinversion of blood at this delayed time, when the blood magnetisation has been
decaying towards zero, results in a re-inverted magnetisation that is lower and reduced artifact
in the resulting images.
Figure 2: Example data without (a) and with (b) the introduction of the navigator-restore delay in
3 example subjects. The subjective image quality scores (IQ) and the PV blood ratios are
provided in each case. (RIPV: right inferior pulmonary vein; RSPV: right superior pulmonary
vein). Respiratory motion scores were the same for conventional and NAV-restore-delayed
sequences.
Figure 3: Example unsmoothed end-expiratory navigator traces acquired with the original
sequence (a) and with the NAV-restore-delayed sequence which has poorer SNR (e). In (b) –
(d), increasing random noise is added to the unsmoothed navigator trace in (a). In (f) – (g), the
diaphragm edge position measured in 25 traces with added noise (as in (b) - (d)) is plotted
against that measured in traces without added noise (as in (a)). The least squares fit edge
detection algorithm implemented is relatively insensitive to the added noise.
Figure 4: Diaphragm edge position in the first 25 cycles of the conventional acquisitions plotted
against the diaphragm edge positions obtained in noisier versions of those same navigator
traces for all patients. In each patient, the amount of noise added resulted in similar navigator
SNR values to those obtained with the NAV-restore-delayed sequence.
Figure 5: simulations showing the longitudinal magnetisation of liver, Mz (as a fraction of the
equilibrium value), as a function of navigator-restore delay at four heart rates. The T1 of liver
was assumed to be the same as that of normal myocardium (423ms at 20 – 25 minutes
following .1mmol/kg gadobutrol19)
Figure 6: Example data showing how the navigator artifact is reduced with increasing navigatorrestore delay: (a) delay = 0 ms, (b) delay = 100ms, (c) delay = 150ms. (RIPV = right inferior
pulmonary vein, PVratio = ratio of ostial PV blood signal to that in descending aorta, AS =
consensus artifact score)
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