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(Circulation. 2001;103:2476.)
© 2001 American Heart Association, Inc.
Clinical Investigation and Reports |
Noninvasive Quantification of Left-to-Right Shunt in Pediatric Patients
Phase-Contrast Cine Magnetic Resonance Imaging Compared With Invasive Oximetry
From the Clinic for Congenital Heart Disease, Heart and Diabetes Center, North Rhine-Westfalia, Ruhr-University Bochum, Germany; and Philips Medical Systems, Best, Netherlands (J.G.).
Correspondence to Philipp Beerbaum, MD, Clinic for Congenital Heart Disease, Heart and Diabetes Center, North Rhine-Westfalia, Ruhr-University Bochum, Georgstraße 11, D-32545 Bad Oeynhausen, Germany. E-mail pbeerbaum{at}hdz-nrw.de
 |
Abstract |
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 Top Abstract IntroductionMethodsResultsDiscussionReferences |
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Background—Blood flow can be quantified noninvasively by phase-contrast cine MRI (PC-MRI) in adults. Little is known about the feasibility of the method in children with congenital heart disease.
Methods and Results—In
50 children (mean age 6.2 years, range 1.1 to 17.7 years) with an
atrial- or ventricular-level shunt, blood flow rate in the
great vessels was determined by PC-MRI, and the ratio of
pulmonary to aortic flow (
p/s) was
compared with p/s by oximetry. We found a
difference of 2% and a range of -20% to +26% (limits of agreement,
mean±2 SD). In another 7 children with congenital heart disease but no
cardiac shunting (mean age 7.9 years, range 1.3 to 13.5 years),
p/s by PC-MRI was 1.02 (SD ±0.06). No difference
between systemic venous and aortic flow volumes was found (range
-17% to +20%, n=37). Blood flow through a secundum atrial septal
defect as assessed by PC-MRI (n=24) overestimated the shunt compared
with the difference between pulmonary and aortic flows. The
mean difference between 3 repeated PC-MRI measurements in each location
was 5.3% (SD ±4.0%, n=522), demonstrating good precision. The
interobserver variability was low. The accuracy of PC-MRI was confirmed
by in vitro experiments.
Conclusions—Determination
of p/s by PC-MRI in children is quick, safe, and
reliable compared with oximetry. Systemic venous flow can be quantified
by PC-MRI, whereas through-plane shunt measurement within an atrial
septal defect is inaccurate.
Key Words: heart defects, congenital • pediatrics • magnetic resonance imaging • shunts • veins
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Shunt quantification is essential in the management of congenital heart disease.1 Clinical methods available to yield quantitative flow data have major drawbacks.2 Doppler ultrasound methods are noninvasive but highly observer-dependent.2 Radionuclide angiocardiography (RNAC) is restricted to simple left-to-right shunt lesions with normal ventricular function,1 3 and patients are exposed to ionizing radiation. Indicator dilution techniques are invasive, as is oximetry, a method complicated by variations of oxygen consumption and difficulties in estimating a mixed venous oxygen content in atrial-level shunt patients.1 4 In contrast, phase-contrast cine MRI (PC-MRI) is noninvasive and can determine aortic and pulmonary flow volumes in patients with congenital heart disease, thus adding functional information to a morphological cardiac MR investigation.5 In adults, good agreement with invasive oximetry,6 7 RNAC,3 8 and ventricular stroke volumes as obtained by cine MRI9 10 11 was demonstrated. Flow-phantom and animal12 studies suggested a high degree of accuracy and precision with various flow-sensitive pulse sequences.5 13 14 Information is limited, however, about the feasibility of PC-MRI in pediatric patients,15 16 whose higher peak velocities and blood pulsation rates may hamper velocity quantification.5 The objective of this investigation was to evaluate pulmonary, aortic, and systemic venous flows by PC-MRI in a larger number of pediatric patients with congenital heart disease in a prospective and blinded manner. In addition, flow through the defect was evaluated in children with a secundum atrial septal defect (ASD II) by PC-MRI. We chose invasive oximetry for comparison of
p/s,
because the technique still is an accepted clinical standard and is
available during cardiac
catheterization. |
Methods |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Study Population
From January 1998 to July 2000, we prospectively enrolled into the study 50 children with an atrial- or ventricular-level left-to-right shunt (mean age 6.2±3.2 years, median 5.1 years, range 1.1 to 17.7 years, 28 girls, 22 boys). Of these 50 patients, 40 had ASD II, 3 partial anomalous pulmonary venous return, 4 sinus venosus defect with partial anomalous pulmonary venous return, and 3 a ventricular septal defect. Only children in sinus rhythm and with evidence of significant shunting were considered eligible.
Moreover, 7 children with congenital heart disease but no
cardiac shunts were analyzed for their
p/s ratio by PC-MRI (mean age 7.9±4.4 years,
range 1.3 to 13.5 years, 4 boys, 3 girls).
Cardiovascular diagnoses were coarctation (n=3), double
aortic arch (n=2), and suspected but not confirmed ASD (n=2). The study
was approved by the institutional review committee, and informed,
written consent was obtained from parents or
caretakers.
Study Design
Each patient underwent MRI examination to measure
through-plane flow in the ascending aorta and pulmonary artery,
and in 37 patients, also in the superior and
inferior venae cavae
(Figures 1
and 2). Three measurements were acquired in
each location to determine repeat ability. In 32 patients with
an ASD II, flow through the defect was assessed
(Figure 3). In 10 randomly selected patients, PC-MRI images
were reanalyzed by 2 operators (H.K., P. Barth) blinded to
their own former and each other’s results to determine interobserver
variability. MRI studies were followed by invasive oximetry during
cardiac catheterization performed to assess
pulmonary and systemic venous return, exclude pulmonary
hypertension and/or associated lesions, quantify left-to-right shunt,
and for transcatheter defect closure in suited ASD II
patients. The catheterization staff was blinded to the
MR investigators’ results and vice versa. Sedation for either
procedure was performed with midazolam and thiopental
intravenously as needed, and blood pressure, oxygen
saturation, heart rate, and respiratory rate were monitored
continuously.
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|
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MR Imaging Technique
All examinations were performed on a 1.5-T whole-body
MR scanner (Philips, ACS-NT, maximum gradient
performance 23 mT/m amplitude, slew rate 105 T ·
m-1 · s-1).
A conventional flow-sensitive gradient-echo pulse sequence provided by
the manufacturer was used
(Table).
TE was 
6 ms in all acquisitions. We used retrospective gating to
include end-diastolic flow. Through-plane measurements were
performed with velocity-encoded values of 200 to 300 cm/s (arteries),
150 cm/s (veins), and 80 to 100 cm/s (ASD). All acquisitions used a
phase-correction algorithm provided by the manufacturer working as a
magnitude-weighted, spatial low-pass filter correcting phase offsets
from residual eddy current effects. Imaging time for each measurement
was 2.2 to 3 minutes, depending on the heart rate, yielding 15 to 20
reconstructed frames per average cardiac cycle
(Figures 1 to 3
). The body coil was used for both signal
transmission and detection.
|
MR Image Analysis
Data analysis was performed offline on a
computer workstation using a computer algorithm for semiautomatic
vessel border detection developed by one of the authors (P. Barth) to
optimize measurement reproducibility and accelerate image
analysis. Briefly, from a starting point within the vessel of
interest in a baseline modulus image, radial intensity profiles are
determined in 360 steps of 1°. The distance between the points of
steepest decline on the intensity profiles and the starting point
yields radius values. A 5-point-median smoothing function eliminates
misfits. Thus, a region of interest (ROI) is defined. The algorithm is
repeated automatically until ROIs are applied to all modulus images and
subsequently projected to the corresponding phase images, leaving
only a few frames for a computer-based, manually performed correction,
with flow calculation in a single vessel completed within 1 to 2
minutes.
In Vitro Validation of PC-MRI
A pulsatile flow phantom used a glass tube with an
inner diameter of 12.4 mm, connected to silicon tubes at both ends
and embedded in a glass container, both filled with a copper sulfate
solution (3 mmol), designed to minimize susceptibility artifacts.
The tube was placed parallel to the bore of the magnet. A 2-roller pump
from a heart-lung machine (Fa. Stöckert) delivered flow rates of 0.65
L/min (30 bpm), 0.85 L/min (40 bpm), 1.28 L/min (60 bpm), 1.73 L/min
(80 bpm), and 2.63 L/min (120 bpm). Gating was based on a
hydrostatically generated signal. Each measurement was repeated twice
and controlled by stopwatch and a graded cylinder. The body coil was
used, and imaging parameters resembled in vivo measurements
(Table),
with velocity-encoded values adapted to experimental conditions (40 to
300 cm/s).
Oximetric Technique
Blood samples were collected from the caval veins,
right heart, pulmonary arteries, and a systemic artery (left
heart included when possible) while a stable
physiological condition was ensured. Two to 3
samples from the superior and 1 from the inferior vena cava
were used to estimate mixed venous saturation in
ASD.4
p/s was calculated by use of the Fick
formula.
Statistical Analysis
All data are expressed as mean±SD. In vitro results
were analyzed by 2-variable linear regression
analysis. Bland and
Altman17 analysis
was used to determine PC-MRI interobserver variability and to evaluate
the agreement between (1) p/s by PC-MRI and
oximetry, (2) systemic venous and aortic flow by PC-MRI, and (3) shunt
flow within an ASD and the difference p-s by
PC-MRI. Data were logarithmically transformed when differences and
means were linearly
related.17
|
Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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MRI and catheterization studies were well tolerated, and no adverse effects of sedation were observed. The mean time span between the 2 examinations was 62 days (SD ±49). All PC-MRI measurements were completed within 30 to 40 minutes. Mean heart rate was 99 bpm (SD ±14) at PC-MRI and 99 bpm (SD ±13) at oximetry.
p/s by PC-MRI Compared
With Oximetry
The Bland-Altman analysis was applied to the
log-transformed data,17
because differences increased linearly with mean
p/s values. Estimation of precision of the limits
of agreement (defined as mean±2 SD) was based on calculation of 95%
confidence intervals (CI). A mean value of 1.0 after antilog
transformation (dimensionless ratio) is expected in the case of no
difference between 2 tested methods.
As to the p/s ratio by PC-MRI and
oximetry, we found a negligible difference of 2% (mean 0.98) between
the 2 methods. Upper and lower limits of agreement were 1.24 (CI 1.17
to 1.31) and 0.78 (CI 0.73 to 0.82), respectively
(Figure 4A and 4B). Thus, both methods to assess
p/s may differ by 24% above and 22% below in
95% of the cases.
|
This fairly good agreement did not improve in 29 of the 50
patients, in whom the heart rate differed by <10% between the 2
examinations: mean difference 2%, range 1.23 to -0.78 (mean±2 SD,
CI 1.14 to 1.32 and 0.72 to 0.84). The mean p/s
ratio by PC-MRI in the 7 children without shunting was 1.02 (SD±0.06,
range 0.92 to 1.10).
Shunt Flow Through an ASD II
Shunt assessment by PC-MRI measurement within the ASD
plane
(Figure 3) was performed in 32 children with interpretable
results in 24 subjects (mean age 5.5 years, SD ±2.3 years). Results
were compared with the difference of the pulmonary and aortic
flow volumes (p-s) by PC-MRI
(Figure 5, data log-transformed) and differed significantly
(mean difference 0.88, P<0.01,
2-sided Student’s t test).
Upper and lower limits of agreement were 1.29 (mean+2 SD, CI 1.12 to
1.47) and -0.60 (mean-2 SD, CI 0.53 to 0.69), respectively. Thus,
there was significant shunt overestimation and a wide scatter compared
with the difference p-s.
|
Systemic Venous Flow
Venous flow was measured by PC-MRI in the superior and
inferior venae cavae in 37 patients with normal venous
connections (mean age 5.8 years, SD ±3.3 years). The results were
compared with aortic flow
(Figure 6A and 6B). We found no difference (mean 1.0), with a
range of +20% to -17% (CI 1.14 to 1.27 and 0.79 to 0.88). Venous
flow was biphasic in all children, with a peak in
ventricular systole and diastole
(Figure 2). The p/s ratio as derived
from pulmonary and systemic venous flows obtained by PC-MRI
agrees fairly well with oximetry data: mean difference 0.96, range 1.29
to 0.79 (mean±2 SD, CI 1.19 to 1.41 and 0.65 to 0.78).
|
PC-MRI: Interobserver Variability,
Repeatability, and Accuracy In Vitro
Three measurements each in the ascending aorta,
pulmonary artery, and superior and inferior venae
cavae in 10 randomly selected patients yielded 120 flow-data sets that
were independently reevaluated by 2 observers. The mean difference was
+0.2 mL (SD ±1.5), range +3.2 mL to -2.8 mL (mean±2 SD, CI +2.4 to
+4.2 mL and -2.0 to -3.6 mL), demonstrating a low interobserver
variability by use of a computer algorithm for semiautomatic vessel
border detection.
In each vessel, 3 measurements were performed to assess
repeatability for PC-MRI flow measurements
(Figures 1 and 2). The overall mean variation of flow results
was 5.3% (SD ±4.0%, 522 flow-data sets), reflecting good
precision.
PC-MRI flow phantom measurements were repeated twice over a range of 0.65 to 2.63 L/min and controlled by stopwatch and graded cylinder. A strong correlation was found between PC-MRI and manually performed measurements (y=0.075+0.915x, r=1.000, P<0.001), demonstrating a high level of accuracy in vitro.
|
Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Blood flow quantification by PC-MRI is a potentially valuable diagnostic method in the evaluation of patients with congenital heart disease.15 18 Over the past 14 years, the technique has been validated in adult patients and healthy volunteers3 6 7 8 9 10 11 as well as in phantom studies using various pulse sequences.5 13 14 In children, however, higher rates of blood pulsation, flow acceleration, and respiration are present, along with higher peak velocities and smaller vessels.15 16 Well-known possible sources of error5 19 20 21 22 23 that may be even more apparent in children are (1) signal loss from intravoxel phase dispersion resulting from higher-order motion components, (2) in-plane and through-plane vessel motion, (3) phase offsets from residual eddy current effects, (4) a shorter cardiac cycle length limiting temporal resolution, (5) misalignment of flow direction and flow-encoding gradients, (6) partial volume effects from edge voxels containing information from both static and moving spins, and (7) velocity-encoded values too small (aliasing) or too large (loss of signal).
Pediatric Validation Studies
Investigations on the use of PC-MRI to quantify
p/s in children are sparse and sample sizes
small.15 16
Rebergen et al11 compared
p/s assessed by PC-MRI (pulmonary and
aortic flow) with p/s values as calculated from
ventricular stroke volumes acquired by transverse
multislice-multiphase MRI. Their total of 12 patients included 6
children, 2 of them <10 years old. Good agreement was demonstrated in
all but 1 of the pediatric cases. Sieverding et
al24 reported a good
correlation between p/s by PC-MRI and oximetry in
6 children (mean age 4.9 years, range 0.25 to 13.4 years, 4 with a
left-to-right shunt), but MR results compared less well to MRI
ventricular volumetric data. Arheden et
al8 compared
p/s values by PC-MRI with RNAC in 24 patients
with a cardiac left-to-right shunt, 6 of whom were children and 2
adolescents. The 2 methods differed considerably, by 14% (SD ±13%),
and no subgroup analysis for the pediatric patients was
presented. In a retrospective study on 20 patients (mean age
12.8 years, range 0.7 to 49 years) with congenital heart disease but no
shunts, Powell et al25 found
a mean p/s ratio of 0.99±0.1 and limits of
agreement from 0.79 to 1.19.
p/s by PC-MRI and
Oximetry
To provide more extensive validation data, we evaluated
PC-MRI in 57 pediatric patients with congenital heart disease, 50
children with a left-to-right shunt and 7 without. We used a moderately
short TE of 6 ms
(Table),
recommended to limit intravoxel phase
dispersion5 24 and
sensitivity to higher-order motion
components.26 The relatively
large voxel size of 2x2.5x5 mm3 was
considered still small enough to avoid significant partial-volume
effects while ensuring a good signal-to-noise ratio (SNR) for
computer-based semiautomatic vessel border detection. Scan time was
kept to a minimum to allow repeated measurements in each location
within a reasonable total imaging time. We did not use the full
strength of the gradients (TE<3.5 ms), because otherwise a substantial
increase of non–flow-related phase shifts was observed both in vivo
and in vitro, most likely from residual eddy current effects degrading
PC-MRI measurement results. With our protocol
(Table),
data sampling with a repetition time (TR) of 20 ms yielded 15 to 20
phase images per average cardiac cycle, depending on the heart rate,
thought to be sufficient to avoid significant flow volume
underestimation.
Therefore, we did not reduce TR to improve the temporal resolution at the expense of a lower SNR, because SNR was already suboptimal as a result of use of the body coil for signal detection. This was unavoidable, because the reconstruction time was unacceptably long with use of a cardiac multielement phased-array coil to optimize SNR. Retrospective ECG gating was preferred to conventional ECG triggering to include end-diastolic flow. Accuracy and precision of this protocol was demonstrated in vitro with a pulsatile flow phantom.
We compared p/s results by PC-MRI with
oximetry, because this method is an accepted clinical standard and is
available during cardiac catheterization routinely
performed in these patients in our hospital. A negligible bias of 2%
and a scatter of +24% to -22% was found, suggesting a fairly good
agreement between the 2 methods, well acceptable for clinical purposes.
Oximetry may contribute substantially to the scatter because of the
predominance of atrial level shunt patients in our study, in which
estimation of a mixed-venous saturation is
difficult.1 4 We
were unable to prove any superiority of PC-MRI over oximetry, however,
because repeatability, interobserver variability, and in vitro accuracy
were determined in PC-MRI but not in oximetry. In the 7 children with
congenital heart disease but no shunts, p/s
values by PC-MRI were close to unity, confirming the results of
others11 24 25
demonstrating the ability of PC-MRI to exclude significant shunting in
children.
Shunt Flow Through an ASD II
Direct shunt assessment by phase images obtained within
the ASD plane
(Figure 3) was carried out in 32 patients with an ASD II,
with interpretable phase maps in only 24 children, in whom a
significant shunt overestimation and a wide scatter were observed
compared with the difference of pulmonary and aortic flows
(Figure 5). This disagreement is most likely due to
inaccuracy of direct shunt assessment: (1) misalignment of shunt flow
direction and flow-encoding gradients, because the shunt flow direction
is oblique to the orientation of the ASD plane; (2) ROIs difficult to
define, because clear defect borders are lacking in late
diastole and early systole, when shunt flow is minimal; and
(3) movement of the atrial septum out of the imaging plane with
respiration and cardiac motion. Given the good agreement between
p/s values by PC-MRI and oximetry, it seems
reasonable to conclude that PC-MRI measurements in the great arteries
are more accurate.
Systemic Venous Flow
Superior and inferior vena cava flow
volumes
(Figure 2) obtained in 37 children with normal venous
connections served as an internal
reference10 for aortic flow
rates by PC-MRI. Agreement of venous with aortic flow was acceptable
(no difference, range +20% to -17%,
Figure 6), as was the agreement of the ratio of
pulmonary and systemic venous flow to p/s
by oximetry. Surprisingly, inferior vena cava flow rate was
not significantly altered by shunt influx in patients with a large ASD.
As observed in healthy
adults27 and well known from
Doppler studies in children, systemic venous flow was biphasic,
with peaks in ventricular systole and
diastole.
Limitations
First, in some patients, a considerable time span was
allowed between MRI and cardiac catheterization.
Although overall agreement between p/s by PC-MRI
and oximetry was good under these conditions, some improvement might be
possible with the 2 examinations performed in a row. Second, heart rate
was different between the 2 examinations in some patients, but no
significant bias seemed to be introduced, because agreement of
p/s did not improve in children with a heart rate
difference <10%. Third, no conclusions from our data are applicable
to children with arrhythmia or valvular
disease.
To quantify blood flow in newborns and infants with higher heart rates and smaller vessels, stronger gradients will be needed to shorten TE and TR to overcome the problem of limited temporal and spatial resolution as well as to reduce the sensitivity to higher-order motion components. Ultrafast imaging by use of a segmented echo-planar technique may be an option. Dedicated phase-correction algorithms are likely to be mandatory, however, to avoid substantial errors in flow volume estimates as introduced by effects of residual eddy currents and concomitant fields. Because more powerful reconstruction computers are now available, phased-array cardiac surface coils can be used to further improve SNR for better spatial resolution and/or faster image acquisition.
In children with congenital heart disease, determination of
p/s by use of a conventional PC-MRI pulse
sequence is safe, accurate, and reliable compared with oximetry.
Systemic venous flow can be quantified by PC-MRI, whereas through-plane
shunt measurement within an ASD is
inaccurate.
|
Acknowledgments |
|---|
This study was supported in part by Philips Medical Systems, Hamburg, Germany, and Philips Medical Systems, Best, Netherlands. The authors thank Eugenia Crespo-Martinez, MD, Detlev Baller, MD, PhD, Gunawan Notohamiprodjo, MD, PhD, and Astrid Kohlstädt-Klapper for reviewing the manuscript.
Received November 8, 2000; revision received February 12, 2001; accepted March 1, 2001.
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L. Grosse-Wortmann, T.-J. Yun, O. Al-Radi, S. Kim, M. Nii, K.-J. Lee, A. Redington, S.-J. Yoo, and G. van Arsdell Borderline hypoplasia of the left ventricle in neonates: insights for decision-making from functional assessment with magnetic resonance imaging. J. Thorac. Cardiovasc. Surg., December 1, 2008; 136(6): 1429 - 1436. [Abstract] [Full Text] [PDF]
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L. E.J. Thomson, A. L. Crowley, J. F. Heitner, P. J. Cawley, J. W. Weinsaft, H. W. Kim, M. Parker, R. M. Judd, J. K. Harrison, and R. J. Kim Direct En Face Imaging of Secundum Atrial Septal Defects by Velocity-Encoded Cardiovascular Magnetic Resonance in Patients Evaluated for Possible Transcatheter Closure Circ Cardiovasc Imaging, July 1, 2008; 1(1): 31 - 40. [Abstract] [Full Text] [PDF]
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 O. K. Mohrs, S. E. Petersen, D. Erkapic, A. Victor, T. Schlosser, B. Nowak, G. Kauffmann, T. Voigtlaender, and H.-U. Kauczor Dynamic Contrast-Enhanced MRI Before and After Transcatheter Occlusion of Patent Foramen Ovale Am. J. Roentgenol., March 1, 2007; 188(3): 844 - 849. [Abstract] [Full Text] [PDF]
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 K. I. Norton, C. Tong, R. B. J. Glass, and J. C. Nielsen Cardiac MR Imaging Assessment Following Tetralogy of Fallot Repair RadioGraphics, January 1, 2006; 26(1): 197 - 211. [Abstract] [Full Text] [PDF]
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T Kuehne, S Yilmaz, I Schulze-Neick, E Wellnhofer, P Ewert, E Nagel, and P Lange Magnetic resonance imaging guided catheterisation for assessment of pulmonary vascular resistance: in vivo validation and clinical application in patients with pulmonary hypertension Heart, August 1, 2005; 91(8): 1064 - 1069. [Abstract] [Full Text] [PDF]
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O. K. Mohrs, S. E. Petersen, D. Erkapic, C. Rubel, R. Schrader, B. Nowak, W. A. Fach, H.-U. Kauczor, and T. Voigtlaender Diagnosis of Patent Foramen Ovale Using Contrast-Enhanced Dynamic MRI: A Pilot Study Am. J. Roentgenol., January 1, 2005; 184(1): 234 - 240. [Abstract] [Full Text] [PDF]
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H. Korperich, J. Gieseke, P. Barth, R. Hoogeveen, H. Esdorn, A. Peterschroder, H. Meyer, and P. Beerbaum Flow Volume and Shunt Quantification in Pediatric Congenital Heart Disease by Real-Time Magnetic Resonance Velocity Mapping: A Validation Study Circulation, April 27, 2004; 109(16): 1987 - 1993. [Abstract] [Full Text] [PDF]
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P. Beerbaum, H. Korperich, J. Gieseke, P. Barth, M. Peuster, and H. Meyer Rapid Left-to-Right Shunt Quantification in Children by Phase-Contrast Magnetic Resonance Imaging Combined With Sensitivity Encoding (SENSE) Circulation, September 16, 2003; 108(11): 1355 - 1361. [Abstract] [Full Text] [PDF]
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