AJR 2002; 179:159-165
© American Roentgen Ray Society
Dynamic Time-Resolved Contrast-Enhanced Two-Dimensional MR Projection Angiography of the Pulmonary Circulation: Standard Technique and Clinical Applications
S. Sonnet1,
C. H. Buitrago-Téllez1,
K. Scheffler2,
R. Strecker2,
G. Bongartz1 and
J. Bremerich1
1 Department of Radiology, University Hospital Basel, Petersgraben 4, 4051
Basel, Switzerland.
2 Section of Medical Physics, Department of Radiology, University of Freiburg,
Hugstetterstr. 55, 79106 Freiburg, Germany.
Received October 1, 2001;
accepted after revision January 14, 2002.
Address correspondence to C. H. Buitrago-Téllez.
Abstract
OBJECTIVE. Time-resolved pulmonary two-dimensional MR projection
angiography is a fast acquisition technique that allows the generation of
dynamic projection angiograms by a method similar to that used to generate
digital subtraction angiograms. MR images are obtained after subtracting the
mask defined at the beginning of the sequence from later images, thus
generating time-resolved continuous projection angiograms that depict the
passage of a bolus through the pulmonary circulation. This article describes
the application of this novel technique in three patients with pathologic
conditions not previously described with this modality and two control
subjects.
CONCLUSION. The analysis of the findings on dynamic time-resolved
contrast-enhanced two-dimensional MR projection angiography shows that this
technique is useful not only in revealing morphologic changes associated with
pulmonary disorders but also in following the passage of the bolus through the
cardiopulmonary circulation. The latter capability allows qualitative
detection of normal or abnormal pathways and thus is potentially of value in
the assessment of several pulmonary disorders.
Introduction
Assessment of cardiopulmonary circulation and flow dynamics is important in
patients with suspected shunts, arteriovenous malformations, or complex
congenital heart diseases before and after surgical repair. Echocardiography
may be helpful in visualizing isolated segments of pulmonary vessels but is
limited because it depends on acoustic windows. Thus, a nonivasive dynamic
imaging technique that provides an overview of cardiopulmonary flow dynamics
with high temporal resolution would be desirable.
Dynamic time-resolved two-dimensional (2D) contrast-enhanced MR projection
angiography was proposed for various clinical applications by Wang et al.
[1] in 1996 and for lung
disorders by Hennig et al. [2]
in 1997. Time-resolved 2D MR projection angiography refers to a fast
acquisition technique that allows the generation of dynamic projection
angiograms by a method similar to that used to generate digital subtraction
angiograms. Projection angiograms are obtained as 2D thick-slab images with a
temporal resolution of considerably less than 1 sec. Background signal is
suppressed by selecting a mask from the early images obtained before the bolus
arrival and subsequently subtracting the signal from the image time
series.
The feasibility of this technique and its diagnostic value in patients with
arterial stenooclusive disease of cervical and intracranial arteries have been
evaluated in various studies
[3,
4]. Moreover, MR projection
angiography has greater sensitivity than conventional digital subtraction
angiography in detecting dural arteriovenous fistulas
[5]. Strategies to improve the
signal-to-noise ratio of the 2D projection angiograms by postprocessing
analysis have been presented by Strecker et al.
[6], to obtain superior image
quality. In the evaluation of intracranial vascular malformations, subsecond
2D MR projection angiography has proven a reliable technique, providing
information on the hemodynamics
[7]. However, clinical studies
of the diagnostic potential of MR projection angiography in the evaluation of
specific pulmonary disorders have been lacking. Thus, the purpose of this
article is to describe the standard technique of the 2D MR projection
angiography in the morphologic and dynamic evaluation of the pulmonary
circulation and to show the application of this novel technique in three
patients with disorders not previously described with this modality and two
control subjects.
Subjects and Methods
Technique
All investigations were performed on a clinical 1.5-T MR scanner (Magnetom
Vision; Siemens, Erlangen, Germany) using the whole-body gradient set with 20
mT/m amplitude and 400-µsec rise time. MR images were acquired as coronal
projections using a four-element (circular polarized) phased array body
coil.
For image acquisition, we used a 2D radiofrequency spoiled steady-state
snapshot fast low-angle shot sequence with a (slice-selective) thick-slab
excitation pulse. The imaging parameters were TR/TE (minimum), 4.2/1.5; flip
angle, 30°, slab thickness, at least 160 mm; and a minimum field of view,
400 mm. In four cases, a 256 x 256 matrix was used. In one case in which
the patient was thought to have peripheral pulmonary vasculitis, we used a 512
x 512 matrix. Temporal resolution was increased to four images per
second without sacrifice in the signal-to-noise ratio or spatial resolution by
combining a sequence with a view-sharing technique. The imaging sequence was
started simultaneously with injection of the contrast agent bolus by means of
a power injector (Spectris; Medrad, Indianola, PA). A clinical dose (0.1
mmol/kg of body weight) of gadopentetate dimeglumine was administered with a
flow rate of 2 mL/sec followed by a saline flush of 30 mL via a large-gauge
cannula placed in an antecubital vein.
Image processing included an automatic complex subtraction method. The
first image of the image time series was discarded because of severe artifacts
induced by the signal fluctuations during the approach to the steady-state
signal. The next six images measured before bolus arrival were averaged and
served as a background mask. All further images were calculated by a complex
subtraction of the mask from subsequent images. The average mask was used to
improve the signal-to-noise ratio in the subtracted images. Data acquisition
was started at breath-hold, with an acquisition time as long as 51 sec.
Subsequently, three-dimensional (3D) contrast-enhanced MR angiography was
performed in all patients. using a 3D fast spoiled gradient-echo fast
low-angle shot sequence in coronal plane. Imaging parameters consisted of
TR/TE, 3.83/1.31; flip angle, 35°; field of view, 350 mm; matrix, 512
x 512; effective slice thickness, 1.14 mm; and number of partitions, 56.
For contrast enhancement, a single dose of gadopentetate dimeglumine (0.1
mmol/kg of body weight) was injected into the antecubital vein at a flow rate
of 2 mL/sec by means of a power injector, followed by a saline flush of 30 mL
injected at the same rate.
Patients
Five patients (three females and two males) between 12 and 59 years old
(mean age, 36 years 2 months ± 20 years 11 months) were examined using
the described MR examination protocol. The primary clinical symptom in all the
patients was exertional dyspnea. Three of the five presented with symptoms
that raised clinical suspicion of a left-to-right shunt at the pulmonary
level. In one patient, MR imaging was performed to disclose vessel involvement
with a suspected pulmonary vasculitis; previous CT findings had shown
peripheral multifocal lesions associated with an intraalveolar pulmonary
hemorrhage. Among our patients was a child who had experienced repeated
episodes of life-threatening hemoptysis that required bronchial artery
embolization the previous year; MR examination was performed to assess a
suspected recurrent pulmonary arteriovenous malformation.
Image evaluation was performed in consensus by two experienced radiologists
who judged the diagnostic value of the results of pulmonary time-resolved 2D
MR projection angiography independent of the results of 3D contrast-enhanced
MR angiography. Final diagnosis was obtained by clinical follow-up in three
cases, by histology in another case, and by conventional angiography in the
fifth case.
Results
Evaluation of the Technique
Examinations of all five patients yielded images that provided clear
depiction of the pulmonary trunk, pulmonary arterial branches up to the
segmental level, and pulmonary venous vessels, showing the robust performance
of this technique. Because of the rapid passage of the bolus through the
pulmonary circulation during the first seconds of breath-holding, images were
of diagnostic quality, displaying these structures even if the patients could
not hold their breath longer than 20 sec. Even so, the snapshot fast low-angle
shot technique is less susceptible to motion artifacts, displaying even
morphologic changes of the pulmonary vessels despite diaphragmatic
movement.
The 3D technique was helpful for determining the exact topographic
localization of the findings, especially in the partial anomalous pulmonary
venous return and complex arteriovenous malformation. The 3D MR angiograms did
not show findings that had not been suspected from findings of the 2D MR
projection angiography. However, the 3D technique depicted the pathologic
condition without superimposition, allowing the differentiation of overlying
structures.
Clinical Applications
The first patient with exertional dyspnea and a suspected right-to-left
shunt at the level of the pulmonary vessels showed a normal vascular anatomy
and hemodynamics of the pulmonary circulation, as revealed on time-resolved 2D
MR projection angiography (Fig.
1A,1B,1C,1D).
In the early phase, the filling of the right atrium was displayed, whereas the
arrival of the contrast bolus in the pulmonary arteries was clearly shown in
the pulmonary arterial phase. In the subsequent parenchymal phase, arteries
and veins were contrasted simultaneously. Finally, the left atrium and
ventricle, aorta, and great vessels were clearly depicted in the late venous
phase. Similar normal findings with no evidence of pulmonary abnormalities
resulted from 3D contrast-enhanced MR angiography and the clinical tests in
the second patient. Clinical follow-up of these two patients showed no further
signs of pulmonary abnormalities.
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Fig. 1A. —52-year-old man with exertional dyspnea. Normal anatomy of
pulmonary arterial tree, heart, and great vessels is shown in time-resolved
images. Enhanced subtracted two-dimensional (2D) MR projection image obtained
during early phase displays bolus arrival at right atrium.
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Fig. 1B. —52-year-old man with exertional dyspnea. Normal anatomy of
pulmonary arterial tree, heart, and great vessels is shown in time-resolved
images. Enhanced subtracted 2D MR projection image depicts early pulmonary
arterial phase.
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Fig. 1C. —52-year-old man with exertional dyspnea. Normal anatomy of
pulmonary arterial tree, heart, and great vessels is shown in time-resolved
images. Enhanced subtracted 2D MR projection image shows parenchymal phase
with blush of dye.
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Fig. 1D. —52-year-old man with exertional dyspnea. Normal anatomy of
pulmonary arterial tree, heart, and great vessels is shown in time-resolved
images. Enhanced subtracted 2D MR projection image shows late venous
phase.
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For the third patient, we had a high suspicion of pulmonary vasculitis.
Dynamic 2D MR projection angiography revealed irregularities of upper lobe
segmental arteries and a delayed peripheral perfusion on a subsegmental level
on the left side, as well as a slight narrowing of subsegmental vessels (Fig.
2A,2B,2C,2D,2E,2F).
These findings were compatible with vascular abnormalities involving small
peripheral pulmonary arteries in confirmed cases of perinuclear antineutrophil
cytoplasmic antibodies-positive pulmonary vasculitis. Histologic and cytologic
findings obtained after open lung biopsy of the left upper lobe revealed a
microscopic polyangiitis. This entity is one of the vasculitides previously
included in the polyarteritis nodosa group
[8].
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Fig. 2A. —41-year-old woman with pulmonary vasculitis (microscopic
polyangiitis). Enhanced subtracted two-dimensional (2D) MR projection image
shows good delineation of pulmonary trunk and central pulmonary vessels
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Fig. 2B. —41-year-old woman with pulmonary vasculitis (microscopic
polyangiitis). Enhanced subtracted 2D MR projection image reveals narrowing of
peripheral small vessels during pulmonary arterial phase; narrowing
(arrows) is more predominant on left side.
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Fig. 2C. —41-year-old woman with pulmonary vasculitis (microscopic
polyangiitis). Enhanced subtracted 2D MR projection image shows area of
peripheral narrowing of small vessels adjacent to minor fissure
(arrowheads, right middle field), which is also well demarcated.
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Fig. 2D. —41-year-old woman with pulmonary vasculitis (microscopic
polyangiitis). Enhanced subtracted 2D MR projection image shows delayed
parenchymal perfusion with bolus passage through aorta that underlines
previously described pulmonary findings.
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Fig. 2E. —41-year-old woman with pulmonary vasculitis (microscopic
polyangiitis). In this enhanced subtracted 2D MR projection image, region of
interest and magnification for F are marked with white rectangle.
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Fig. 2F. —41-year-old woman with pulmonary vasculitis (microscopic
polyangiitis). Magnified enhanced subtracted 2D MR projection image (marked in
E) shows that changes in small vessels at periphery of upper left lobe
(arrows) are more severe than changes in vessels in right lobe.
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Microscopic polyangiitis usually manifests with a lung hemorrhage, as in
our patient. Moreover, the involvement of the small pulmonary vessels is
considered the main diagnostic criterion
[8]. To our knowledge, this
article is the first report of pathologic changes of small pulmonary vessels
detected on MR imaging. Dynamic pulmonary 2D MR projection angiography showed
a narrowing of small peripheral vessels, with a predominance of the left side,
in the area in which the biopsy was undertaken on the upper lobe. These 2D MR
projection angiographic findings were especially evident when we viewed the
dynamic images in a cine-loop mode available in our unit.
In the fourth patient who experienced fatigue after sports activity,
dynamic time-resolved 2D MR projection angiography revealed a partial
anomalous pulmonary venous return, wherein the anomalous vein of the left
upper lobe drains into the high portion of the superior caval vein (Fig.
3A,3B,3C,3D).
Consequentially, the right atrium and ventricle are enlarged because of the
left-to-right shunt. The pulmonary vein of the left lower lobe drains
correctly into the left atrium. The pulmonary circulation of the patient's
right lung revealed no abnormalities.
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Fig. 3C. —17-year-old boy with partial anomalous pulmonary venous
return. Enhanced subtracted 2D MR projection image clearly shows anomalous
vertical vein of left upper lobe (arrowheads) draining into high
portion of superior vena cava (arrows).
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Fig. 3D. —17-year-old boy with partial anomalous pulmonary venous
return. Enhanced subtracted 2D MR projection image obtained during late venous
phase shows anomalous vertical vein (arrowheads) and superior vena
cava (arrows).
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Finally, in the fifth patient, a 12-year-old girl with recurrent
hemoptysis, pulmonary time-resolved 2D MR projection angiography and 3D
contrast-enhanced MR angiography showed a complex arteriovenous malformation
in the anterior segment of the right upper lobe and a central aneurysmatic
alteration of the right hilus. Both the feeding arterial vessel and the
anomalous pulmonary venous drainage into the superior caval vein were clearly
depicted (Fig.
4A,4B,4C,4D,4E,4F,4G,4H,4I).
The early filling of the abnormal venous drainage of the upper pulmonary vein
on the right side were accurately revealed on 2D MR projection angiography.
The second more extensive malformation at the right pulmonary hilus showed an
aneurysm arising from a segmental artery of the right lower lobe, as well the
venous return directly draining into the right atrium. Pulmonary digital
subtraction angiography (Fig.
4A,4B,4C,4D,4E,4F,4G,4H,4I)
confirmed the time-resolved 2D MR projection angiographic findings. The upper
lobe malformation was embolized with coils, whereas the hilar aneurysm was
treated with a detachable balloon. The patient recovered completely.
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Fig. 4A. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Two-dimensional MR projection angiogram shows early bolus
passage through right heart and pulmonary trunk. Note signal loss in upper
lobe region resulting from bronchial artery embolization 1 year earlier.
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Fig. 4B. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Two-dimensional MR projection angiogram in pulmonary
arterial phase displays one peripheral nodular lesion (short arrow)
with early venous drainage. Note larger nodular lesion (long arrow)
at right hilus.
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Fig. 4C. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Two-dimensional MR projection angiogram depicts early
venous vessel (arrows) arising from peripheral nodule with anomalous
pulmonary venous drainage in superior vena cava. Nodular hilar lesion on right
side is also well delineated.
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Fig. 4D. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Two-dimensional MR projection angiogram obtained at later
stage displays feeding arterial vessel (arrows) and draining venous
vessel (arrowheads) of peripheral pulmonary malformation.
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Fig. 4E. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Three-dimensional contrast-enhanced MR angiogram confirms
hemodynamic findings detected on time-resolved MR angiography. Feeding
arterial vessel (arrow) and draining venous vessel
(arrowhead) of peripheral pulmonary malformation are simultaneously
shown in this three-dimensional data acquisition.
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Fig. 4F. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Conventional digital subtraction angiogram depicts early
pulmonary phase.
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Fig. 4G. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Conventional digital subtraction angiogram obtained during
parenchymal phase shows peripheral nodular lesion (arrows).
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Fig. 4H. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Conventional digital subtraction angiogram reveals early
draining venous vessel (arrowheads) with anomalous return in superior
vena cava as previously depicted on MR projection angiogram.
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Fig. 4I. —12-year-old girl with complex arteriovenous malformation.
Comparison of pulmonary time-resolved two-dimensional MR projection angiograms
(A—D), three-dimensional contrast-enhanced MR angiograms
(E), and conventional angiograms using digital subtraction technique
(F—I). Conventional digital subtraction angiogram also confirms
central nodular lesion (arrow) in right hilus.
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Discussion
The advent of ultrafast gradient systems made possible the development of
contrast-enhanced 2D MR projection angiography
[1,
2], in which a thick slab is
acquired consecutively with a high temporal resolution of up to four images
per second. The advantage of these ultrafast T1-weighted gradient-echo
sequences is decreased susceptibility to motion artifacts arising from
respiratory excursion in patients with shortness of breath. Therefore, a
breath-hold is desirable only at the beginning of data acquisition, and
synchronizing data acquisition to an ECG-gated signal is not necessary.
In 3D contrast-enhanced MR angiography, severe artifacts in the
reconstructed angiograms can arise if the application of the contrast agent
bolus is not accurately timed to the data acquisition period. It is crucial
for 3D image quality that sampling of the central k-space lines coincides with
the maximal IV T1 shortening
[9]. Because of the short image
acquisition period in the 2D technique, an exact timing of the contrast agent
bolus is not necessary [2,
6], making the 2D technique
easy to perform.
One major disadvantage of the 2D MR projection angiography is that its
spatial resolution is limited when compared with that obtained using
conventional angiography with digital subtraction. The critical issue is the
low signal-to-noise ratio of the projection images because of sampling data
with a high bandwidth and sequential slice imaging. An improvement of the
spatial resolution to less than 1 mm means the matrix size is doubled, going
from 256 x 256 to 512 x 512. Thus, the signal-to-noise ratio
decreases threefold while the field of view remains constant and the phase
encoding steps are doubled. This increase in spatial resolution can result in
a decrease of the detectability of small vessels because their signal
intensity becomes comparable to the noise level. Therefore, a reduction of the
temporal resolution, in principle, cannot be considered a gain in terms of
higher spatial resolution. The view-sharing technique can be used to increase
temporal resolution without a loss in the signal-to-noise ratio. The temporal
resolution can be held to less than 1 sec with a matrix size of 512, but the
noise level in the projection images is also increased, as we observed in the
patient who had microscopic polyangiitis with involvement of the small
pulmonary vessels. In this clinical setting, the intraindividual comparison of
the pulmonary vessels in both lungs and the use of the cine-loop mode to view
the dynamic images may be helpful in detecting pathologic changes.
The high temporal resolution of 2D MR projection angiography provides
information about the dynamic contrast bolus passage through the pulmonary
circulation, allowing assessment of abnormalities such as intrathoracic
arteriovenous malformations. Nevertheless, because of thick slab acquisition,
differentiating among the spatially superimposed vessels is difficult. The
short circulation time of the pulmonary system (4-7 sec) leads to a certain
temporal overlap of arterial and venous vessels. Temporal discrimination
between arterial and venous vessels can be improved by a shorter and faster
bolus injection scheme, which gives a sharper profile of the bolus during the
passage. This alternative was not implemented in these initial five patients
and so we found some overlap of vascular structures in the delayed images.
In comparison with 3D contrast-enhanced MR angiography, time-resolved 2D MR
projection angiography allows the exact depiction of the passage of the
contrast bolus. With 3D angiography, this valuable dynamic diagnostic
information may be obtained only indirectly by certain techniques, such as 3D
time-resolved imaging of contrast kinetics using a temporal resolution of 2-6
sec for volume acquisition
[10].
Initial reports by Hennig et al.
[2] and Strecker et al.
[6] pointed out the capability
of 2D MR projection angiography for the evaluation of obstructing bronchial
carcinoma, obstructive lung diseases, and vascular malformations. However,
abnormal pulmonary findings of time-resolved 2D MR projection angiography have
not been completely described. Our report is the first to emphasize and
document MR findings with this novel technique for complex pulmonary
arteriovenous malformations, congenital anomalies (partial anomalous pulmonary
venous return), and small-vessel pulmonary vasculitis (microscopic
polyangiitis). Our findings have been confirmed in the case of the
arteriovenous malformation by conventional pulmonary angiography and in the
case of the microscopic polyangiitis by open lung biopsy of the left upper
lobe (Figs. 2E and
2F).
In conclusion, use of dynamic time-resolved contrast-enhanced 2D MR
projection angiography should be considered in the workup of patients with
unspecific disorders of the pulmonary circulation, especially when
hemodynamically relevant morphologic abnormalities, such as central or
peripheral shunts and arteriovenous malformations, are clinically
suspected.
Acknowledgments
We thank the entire MR imaging technologist team of the Department of
Radiology of the University Hospital Basel (headed by Valérie Sutter)
for their valuable cooperation in the patient examinations and Verena Koch for
photographic reproduction of the images.
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Abstract
Introduction
