AJR 2001; 177:1177-1182
© American Roentgen Ray Society
Contrast-Enhanced MR Angiography and Perfusion Imaging of the Hand
James W. Goldfarb1,2,
Mary G. Hochman1,
Duck Soo Kim1,3 and
Robert R. Edelman1,4
1
Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical
School, 330 Brookline Ave., Boston, MA 02215.
2
Present address: Department of Medicine, Division of Cardiology, University of
Medicine and Dentistry of New Jersey, CAB Rm. 2302B, 125 Paterson St., New
Brunswick, NJ 08903.
3
Present address: Department of Radiology, University of Massachusetts Memorial
Health Care, 55 Lake Ave. N., Worcester, MA 01655.
4
Present address: Department of Radiology, Evanston Northwestern Healthcare,
2650 Ridge Ave., Evanston, IL 60201.
Received June 1, 2000;
accepted after revision May 16, 2001.
Address correspondence to J. W. Goldfarb.
Abstract
OBJECTIVE. The goal of this investigation was to develop a technique
for producing high-resolution gadolinium-enhanced MR images of the hand that
show three-dimensional angiographic anatomy and permit measurement of distal
soft-tissue perfusion.
CONCLUSION. High-resolution MR angiograms of the hand, as well as
qualitative perfusion information, can be produced using a rapid sequential
gadolinium-enhanced three-dimensional gradient-echo technique.
Introduction
MR angiography plays an important role in the noninvasive assessment of
patients with vascular disease. Unlike conventional angiography, MR
angiography provides a means of revealing vascular anatomy that is
noninvasive, does not require ionizing radiation, and has a minimal associated
risk of contrast agent reaction and renal failure. In recent years,
non-contrast-enhanced MR angiography techniques have been supplanted by
gadolinium-enhanced MR angiography for applications in the body and lower
extremities because of the advantages of shorter imaging time and decreased
motion artifacts
[1,2,3,4].
Gadolinium-enhanced MR angiography of the peripheral extremities presents
several unique challenges. First, vessels in the hand are of much smaller
caliber than vessels in the body and lower extremities, necessitating the use
of higher resolution techniques; and the length of time between injection and
delivery of contrast material to the distal extremity varies greatly among
patients. Finally, arterial and venous collaterals are more commonly and less
predictably encountered and vascular anatomy is potentially much more variable
in the hand than in the body and lower extremities, making resultant images
difficult to interpret.
Although considerable interest exists in adaptation of gadolinium-enhanced
MR angiography techniques for the lower extremities, optimization of the same
techniques for the upper extremities has received relatively less attention.
Early efforts reported the usefulness of anatomic MR imaging for assessing
vascular malformations [5,
6]. Although anatomic MR
imaging can be used to confirm the presence and to define the extent of a
vascular malformation, it is less effective than MR angiography in mapping the
feeding and draining vessels associated with malformations. Moreover, such
anatomic imaging has limited value in the evaluation of vasospastic and
ischemic disorders. As a result, techniques for direct imaging of vessels of
the hand and wrist using two-dimensional time-of-flight sequences have been
developed
[7,8,9,10,11].
Although two-dimensional time-of-flight techniques have been used effectively
in the diagnosis of ischemic disease in the lower extremity, the use of these
techniques in the hand is complicated by the importance of imaging
perpendicular to the plane of flow. This limitation requires separate
acquisitions for the palmar arches and digital arteries. Because of lengthy
acquisition times, time-of-flight sequences in the hand and wrist are commonly
degraded by patient motion.
A preliminary technique for the application of gadolinium-enhanced MR
angiography to the hand was described by Rofsky
[8]. The technique used
three-dimensional (3D) gradient-echo imaging and a double-dose infusion of
gadolinium during a 2- to 3.5-min acquisition of a single 3D image set.
Although this technique can be used successfully to reveal vessels of the
hand, the relatively lengthy acquisition time fails to capitalize on the
advantages of more rapid imaging.
Techniques for rapid, high-resolution MR angiography and perfusion imaging
of the hand could be important in preoperative planning for resection of
masses and soft-tissue anomalies and in the noninvasive assessment of patients
with suspected vascular compromise. The purpose of this study was to develop a
technique for producing high-resolution gadolinium-enhanced MR images of the
hand. The technique must show 3D angiographic anatomy of the hand and permit
measurement of distal soft-tissue enhancement.
Materials and Methods
Seven patients with a mean age of 42 years (range, 25-63 years) presenting
with signs or symptoms of hand disorders and two healthy volunteers underwent
a conventional hand MR examination followed by gadolinium-enhanced MR
angiography. Clinical indications included masses (n = 3), digital
ischemia (n = 2), and osteomyelitis (n = 2). The study of
healthy subjects was approved by the institutional review board. After the
nature of the procedure had been fully explained, informed consent was
obtained from all subjects. In one healthy volunteer, a light tourniquet was
applied briefly to one digit to reduce blood flow and to simulate a pathologic
perfusion abnormality. Imaging was performed using a 1.5-T system (Vision;
Siemens, Erlangen, Germany) fitted with high-performance gradients (25 mT/m,
300 msec rise time). A small, flexible, circularly polarized coil was wrapped
in a spiral fashion around the hand to achieve optimal longitudinal coverage.
Subjects were imaged lying supine, with the hand in a neutral position
(preferably palm down) at their side. Small sponges separated fingers, and the
hand was secured using a nonadhesive binder to minimize motion.
Dynamic gadolinium-enhanced imaging was performed using a 3D
radiofrequency-spoiled gradient-echo sequence with the following parameters:
TR/TE, 4.5/1.1 msec; flip angle, 20°; partition thickness, 2 mm (no
interpolation was used in the slice direction); field-of-view, 180 x 375
mm; matrix, 128 x 512; bandwidth, 520 Hz/pixel; number of excitations,
1; with images acquired in the coronal plane of the hand. Each 3D volume was
acquired in 16-30 sec, depending on the number of 3D sections. Gadolinium
contrast material (Magnevist; Berlex, Wayne, NJ) was hand-injected as a 0.2
mmol/kg IV bolus via a 22-gauge IV catheter placed in the antecubital vein of
the contralateral arm, at a rate of approximately 1.6 mL/sec. One unenhanced
and two to six rapid sequential gadolinium-enhanced 3D image sets, with no
interscan delay, were obtained. Gadolinium-enhanced imaging was begun 20 sec
after the initiation of contrast injection. Subtraction of unenhanced and
gadolinium-enhanced images was performed to minimize background signal and to
assess the presence of tissue perfusion. Maximum intensity projection was
performed on the original and subtracted volumes. Gray-scale values in the
processed images were inverted so that the presence of the injected contrast
agent was visualized as a darkening in the final images. Using both
maximum-intensity-projection and source images, two trained radiologists, in
consensus, evaluated the caliber and order of arteries shown, the presence of
any stenosis or vascular anomalies, and the presence of venous signal.
As a measure of soft-tissue perfusion, the percentage of signal enhancement
in regions of interest of the digits was calculated as (SIpost
— SIpre) / SIpre x 100, where
SIpre represents the signal intensity in the unenhanced image and
SIpost represents the signal intensity after injection of the
contrast agent. Signal loss in the distal digits caused by coil misplacement
was evaluated using multiplanar reconstructions of the 3D gradient-echo images
and conventional spin-echo images to rule out the possibility of the fingers
being outside the flexible surface coil.
Results
In all nine individuals, arteries ranging in caliber from radial and ulnar
to proper digital arteries were shown (Figs.
1A,1B,1C,1D
and
2A,2B).
In all seven clinical patients, findings at gadolinium-enhanced MR angiography
were concordant with clinical expectations. In the patient with an
arteriovenous malformation (AVM), gadolinium-enhanced MR angiography showed
the characteristic disordered vasculature, with prominent feeding arteries and
engorged early-draining veins (Figs.
3A,3B,3C
and
4A,4B).
The smaller feeding artery branches were difficult to delineate because of
limits in resolution and venous overlap. Examination of multiplanar
reformatted images was helpful, albeit not definitive, in this regard. In the
two patients who presented with signs of ischemia, MR angiography showed
vascular abnormalities and distal perfusion defects (Figs.
3A,3B,3C
and
5A,5B,5C).
A similar perfusion defect was observed distal to a tourniquet transiently
applied to a healthy volunteer's finger (Fig.
1A,1B,1C,1D).
In six of nine cases, at least one 3D image set was produced that showed
either no or minimum evidence of venous signal. However, venous signal was
particularly prominent in the patient with an AVM (because of arteriovenous
shunting) (Fig.
3A,3B,3C)
and one patient with distal emboli (likely because of luxury perfusion) (Fig.
5A,5B,5C).
Distinction of arteries from veins was less problematic for the experienced
angiographer than for an inexperienced one and when multiplanar reformations
rather than conventional images were used to examine axial images.
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Fig. 1A. —31-year-old healthy male volunteer. Normal vascular anatomy
of hand as shown on MR angiography. MR projection angiograms from
three-dimensional volumes acquired 30 (A), 50 (B), 70
(C), and 90 (D) sec after injection of gadolinium contrast
agent. In this healthy volunteer, a tourniquet was briefly applied to middle
finger. Considerably less signal enhancement distal to tourniquet (arrow
down, B) can be seen. Note loss of signal caused by mispositioning
of coil in fifth digit (arrow up, B). Venous contamination is
seen in B but not in A. RA = radial artery, UA = ulnar artery,
SA = superficial palmar arch, DA = deep palmar arch, CD = common palmar
digital arteries, PD = proper palmar digital arteries.
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Fig. 1B. —31-year-old healthy male volunteer. Normal vascular anatomy
of hand as shown on MR angiography. MR projection angiograms from
three-dimensional volumes acquired 30 (A), 50 (B), 70
(C), and 90 (D) sec after injection of gadolinium contrast
agent. In this healthy volunteer, a tourniquet was briefly applied to middle
finger. Considerably less signal enhancement distal to tourniquet (arrow
down, B) can be seen. Note loss of signal caused by mispositioning
of coil in fifth digit (arrow up, B). Venous contamination is
seen in B but not in A. RA = radial artery, UA = ulnar artery,
SA = superficial palmar arch, DA = deep palmar arch, CD = common palmar
digital arteries, PD = proper palmar digital arteries.
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Fig. 1C. —31-year-old healthy male volunteer. Normal vascular anatomy
of hand as shown on MR angiography. MR projection angiograms from
three-dimensional volumes acquired 30 (A), 50 (B), 70
(C), and 90 (D) sec after injection of gadolinium contrast
agent. In this healthy volunteer, a tourniquet was briefly applied to middle
finger. Considerably less signal enhancement distal to tourniquet (arrow
down, B) can be seen. Note loss of signal caused by mispositioning
of coil in fifth digit (arrow up, B). Venous contamination is
seen in B but not in A. RA = radial artery, UA = ulnar artery,
SA = superficial palmar arch, DA = deep palmar arch, CD = common palmar
digital arteries, PD = proper palmar digital arteries.
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Fig. 1D. —31-year-old healthy male volunteer. Normal vascular anatomy
of hand as shown on MR angiography. MR projection angiograms from
three-dimensional volumes acquired 30 (A), 50 (B), 70
(C), and 90 (D) sec after injection of gadolinium contrast
agent. In this healthy volunteer, a tourniquet was briefly applied to middle
finger. Considerably less signal enhancement distal to tourniquet (arrow
down, B) can be seen. Note loss of signal caused by mispositioning
of coil in fifth digit (arrow up, B). Venous contamination is
seen in B but not in A. RA = radial artery, UA = ulnar artery,
SA = superficial palmar arch, DA = deep palmar arch, CD = common palmar
digital arteries, PD = proper palmar digital arteries.
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Fig. 2A. —Bar graphs show percentage of signal increase resulting from
contrast agent in each acquisition for hand displayed in Figure
1A,1B,1C,1D.
Arterial and venous percentage of signal increase. Black bars indicate radial
artery, white indicate dorsal vein.
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Fig. 2B. —Bar graphs show percentage of signal increase resulting from
contrast agent in each acquisition for hand displayed in Figure
1A,1B,1C,1D.
Distal soft-tissue percentage of signal increase of individual digits at
various times after injection of contrast agent. Each group shows, left to
right, digits 1, 2, 3, 4, and 5. Third digit had poor enhancement resulting
from applied tourniquet.
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Fig. 3A. —25-year-old woman with arteriovenous malformation (AVM) of
hand. MR projection angiograms from three-dimensional volumes acquired 25
(A), 40 (B), and 70 (C) sec after injection of gadolinium
contrast agent reveal chaotic tangle of vessels, prominent arterial feeders,
and engorged early-draining veins (typical for AVM). Extent of abnormality and
larger feeding arteries are well depicted. Smaller feeding artery branches
were difficult to delineate because of limits in resolution and venous
overlap. Examination of multiplanar reformatted images was helpful in this
regard. RA = dilated radial artery, DPA = deep palmar arch.
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Fig. 3B. —25-year-old woman with arteriovenous malformation (AVM) of
hand. MR projection angiograms from three-dimensional volumes acquired 25
(A), 40 (B), and 70 (C) sec after injection of gadolinium
contrast agent reveal chaotic tangle of vessels, prominent arterial feeders,
and engorged early-draining veins (typical for AVM). Extent of abnormality and
larger feeding arteries are well depicted. Smaller feeding artery branches
were difficult to delineate because of limits in resolution and venous
overlap. Examination of multiplanar reformatted images was helpful in this
regard. RA = dilated radial artery, DPA = deep palmar arch.
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Fig. 3C. —25-year-old woman with arteriovenous malformation (AVM) of
hand. MR projection angiograms from three-dimensional volumes acquired 25
(A), 40 (B), and 70 (C) sec after injection of gadolinium
contrast agent reveal chaotic tangle of vessels, prominent arterial feeders,
and engorged early-draining veins (typical for AVM). Extent of abnormality and
larger feeding arteries are well depicted. Smaller feeding artery branches
were difficult to delineate because of limits in resolution and venous
overlap. Examination of multiplanar reformatted images was helpful in this
regard. RA = dilated radial artery, DPA = deep palmar arch.
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Fig. 4A. —Bar graphs show percentage of signal increase resulting from
contrast agent in each acquisition for hand displayed in Figure
3A,3B,3C.
Arterial and venous percentage of signal increase. Black bars indicate radial
artery, white indicate arteriovenous malformation (AVM).
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Fig. 4B. —Bar graphs show percentage of signal increase resulting from
contrast agent in each acquisition for hand displayed in Figure
3A,3B,3C.
Distal soft-tissue percentage of signal increase of individual digits at
various times after injection of contrast agent. Each group shows, left to
right, digits 1, 2, 3, 4, and 5. Venous enhancement and enhancement of AVM
were always greater than arterial enhancement. Delayed and reduced enhancement
of digits is seen compared with healthy hand (Figs.
1A,1B,1C,1D
and
2A,2B).
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Fig. 5A. —52-year-old woman with pain and discoloration of distal
digits. Decreased digital perfusion resulting from multiple small emboli. MR
projection angiogram from three-dimensional volumes acquired 35 sec
(A), 50 sec (B), and 5 min (C) after injection of
gadolinium contrast agent. First contrast-enhanced image set shows abrupt
cutoff of proper digital vessels in several fingers (arrows,
A) and perfusion defects of distal digits. Local lactic acidosis
associated with ischemia may be cause of arterial dilatation and early venous
filling. High tissue levels of soft-tissue enhancement (presumably caused by
luxury perfusion) help obscure some digital arteries.
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Fig. 5B. —52-year-old woman with pain and discoloration of distal
digits. Decreased digital perfusion resulting from multiple small emboli. MR
projection angiogram from three-dimensional volumes acquired 35 sec
(A), 50 sec (B), and 5 min (C) after injection of
gadolinium contrast agent. First contrast-enhanced image set shows abrupt
cutoff of proper digital vessels in several fingers (arrows,
A) and perfusion defects of distal digits. Local lactic acidosis
associated with ischemia may be cause of arterial dilatation and early venous
filling. High tissue levels of soft-tissue enhancement (presumably caused by
luxury perfusion) help obscure some digital arteries.
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Fig. 5C. —52-year-old woman with pain and discoloration of distal
digits. Decreased digital perfusion resulting from multiple small emboli. MR
projection angiogram from three-dimensional volumes acquired 35 sec
(A), 50 sec (B), and 5 min (C) after injection of
gadolinium contrast agent. First contrast-enhanced image set shows abrupt
cutoff of proper digital vessels in several fingers (arrows,
A) and perfusion defects of distal digits. Local lactic acidosis
associated with ischemia may be cause of arterial dilatation and early venous
filling. High tissue levels of soft-tissue enhancement (presumably caused by
luxury perfusion) help obscure some digital arteries.
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Signal loss resulting from misplacement of the coil on all images
(spin-echo and gradient-echo) was found in one of nine cases
(Fig. 1B).
Discussion
High-resolution gadolinium-enhanced MR angiographic images of the hand can
be routinely produced using rapid 3D gradient-echo sequences. Short
acquisition times (15-30 sec) were achieved through the use of
echoplanar-capable gradient hardware. Using these techniques, we acquired a 3D
image set of the hand in less than 30 sec. The goal of high spatial resolution
is visualization of small distal branches that may be involved by ischemic
disease or that may be relevant to treatment of disease. The goals of rapid
imaging are the acquisition of a purely arterial image and minimizing overlap
with enhanced veins. Rapid sequential images also provide a means of assessing
tissue perfusion over time.
Although the spatial resolution of the MR angiographic images was
relatively high, it remains lower than the image resolution attainable with
conventional angiography. Use of a local surface coil allowed optimization of
spatial resolution with good signal-to-noise ratio, yielding images of 1406
x 732 µm per pixel in-plane resolution and 2-mm partition thickness.
Resultant images showed arteries ranging in caliber from radial and ulnar to
proper digital arteries. In the patient with AVM, the extent of the lesion and
several of its larger feeding vessels were well seen. However, smaller
arterial branches feeding the AVM were difficult to delineate, in part because
of limits in spatial resolution. This constitutes a clinically significant
limitation of MR angiography, because identification of even small feeding
vessels can be important in treatment planning. These findings suggest that
although MR angiography may be appropriate for certain diagnostic
applications, other applications may be limited by constraints on spatial
resolution.
Despite the use of rapid sequential gadolinium-enhanced sequences,
distinction of arteries from veins remains a problem in gadolinium-enhanced MR
angiography of the upper extremity because of a lack of sufficient temporal
resolution. The difficulty is exacerbated by the complex and potentially
variable anatomy of the hand, limiting the ability to predict on the basis of
location alone whether a vessel is an artery or a vein. The problem of
variable anatomy is even greater in the target population of patients with
arterial insufficiency because of their increased propensity to form
collateral bypass vessels. The problem of distinguishing arteries and veins is
also exacerbated in the presence of conditions that promote early venous
shunting, as is often the case with vascular malformations, tumors, and
inflammatory processes. In patients with these conditions, it may not be
possible to distinguish inflow from draining vessels at the level of temporal
resolution currently achieved by MR angiography. Ideally, improved temporal
resolution could help address this problem. At present, imaging times are
limited not only by the actual time of image acquisition, but also by the time
required to reconstruct high-resolution images. An alternative approach to
distinguish arteries from veins would be to obtain time-of-flight images with
saturation bands at selected levels in the area being imaged to establish the
direction of flow in the vessels subsequently shown by gadolinium enhancement.
In any event, examination of the patients should include T1- and T2-weighted
anatomic sequences to assess the presence of flow voids that reflect rapid
flow and high T2 signal channels that reflect slow flow.
Subtraction of unenhanced and gadolinium-enhanced images and
region-of-interest analysis showing the presence or absence of tissue
enhancement provide a measure of tissue perfusion. Using this technique, we
successfully showed absent perfusion to the distal digits in two patients who
presented with clinical signs of ischemia. Decreased perfusion was also
observed in digits distal to an AVM. Measurement of perfusion permits
assessment of vascular integrity in areas in which the vessels are too small
in caliber to be directly imaged. Therefore, perfusion measurements could be
useful for confirming the presence of ischemia in patients with clinical
symptoms and for examining patients with suspected steal syndrome, such as is
seen in patients with forearm dialysis grafts. Perfusion imaging could be used
to noninvasively assess response to therapy for patients being treated for
thrombosis or emboli.
More experience is required to establish the accuracy of
gadolinium-enhanced MR angiography of the hand as compared with the gold
standard of conventional angiography. In our study, findings at
gadolinium-enhanced MR angiography were concordant with overall clinical
expectations. However, for various clinical reasons, correlation with
conventional angiography was not obtained. To determine the clinical
usefulness of MR angiography, its accuracy in depicting patent and occluded
vessels and in showing the location and degree of stenosis must be quantified
with respect to conventional angiography. Direct correlation with conventional
angiography is also needed to determine whether poor timing of the bolus with
respect to the center of k-space for a given acquisition could lead to
artifactual nonvisualization of a vessel. Use of a separate timing scan
[12] could be helpful in this
respect. The capability of the method for the differentiation of occlusion
from spasm, severe stenosis, or shunting must be determined. The optimal
temporal resolution and duration of imaging has also not been determined for
accurate routine digital angiography and perfusion assessment.
Gadolinium-enhanced MR angiographic images of the hand can be produced
using a rapid sequential 3D radiofrequency-spoiled gradient-echo technique.
Resultant images show normal and abnormal anatomy and allow the measurement of
perfusion. Perfusion measurements permit assessment of vascular integrity in
areas where vessels are too small in caliber to be directly imaged. Problems
with overlapping venous enhancement (especially in patients in whom
arteriovenous shunting is present) and the ability to image small feeder
vessels remain to be addressed. Further experience is also needed to assess
the true accuracy and clinical usefulness of MR angiography of the hand.
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Abstract
Introduction
