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1 Department of Diagnostic and Interventional Radiology, University Hospital
Essen, Hufelandstr. 55, Essen 45122, Germany.
2 Department of Angiology, University Hospital Essen, Essen 45122,
Germany.
Received October 1, 2002;
accepted after revision March 18, 2003.
Address correspondence to C. U. Herborn.
Abstract
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SUBJECTS AND METHODS. Nineteen patients (age range, 8-64 years; 11 males and eight females) with clinically diagnosed or suspected angiodyplastic abnormalities of the extremities were examined on a 1.5-T whole-body MR scanner. Using parameters based on a fast localizer sequence, we acquired transverse or coronal T1-, T2-, short tau inversion recovery (STIR), and contrast-enhanced T1-weighted images. Dynamic contrast-enhanced three-dimensional (3D) gradient-echo MRIs were acquired to determine the extent and type of the arteriovenous malformation for each patient. MR data sets were evaluated for lesion depiction, determination of the extent of the malformation, involvement of neighboring structures, vascular detail, and treatment planning. Results were compared with findings from duplex sonography, venography, and intraarterial digital subtraction angiography.
RESULTS. All MRIs were of diagnostic quality and revealed 12 venous vascular malformations, four arteriovenous malformations, and three hemangiomas. The STIR sequence was helpful for determining the extent of the vascular malformation, which was often underestimated using contrast-enhanced 3D MR angiography alone, whereas dynamic contrast-enhanced 3D MR angiography was required for classifying the type of the lesion. MR angiography was inferior to conventional angiography for revealing vascular detail and for planning intervention.
CONCLUSION. MRI and MR angiography appear to be valuable for the assessment of vascular malformations of the extremities. The protocol for imaging such malformations should combine dynamic contrast-enhanced 3D gradient-echo MRI with STIR sequences. However, digital subtraction angiography and venography are still required for definitive treatment decisions.
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Treatment of vascular malformations depends on the extent of the malformation and includes both minimally invasive and surgical interventions. Although superficial lesions with no involvement of muscular tissue are easily treated, large malformations that spread into adjacent musculature, bones, and joints frequently require complex surgery [6]. Osteopathy, pain, intermittent bleeding, or bony overgrowth may mandate palliative therapies [7-9].
Optimal therapeutic stratification and hence optimal outcome require a comprehensive evaluation of feeding and draining vessels as well as adjacent structures. In addition to catheter-based digital subtraction angiography of the arterial and venous systems, pulsed Doppler and duplex sonography combined with plethysmography are well established as techniques with which to assess these conditions [10-12]. More recently, MR angiography, which allows the noninvasive display of vasculature, has become established as an attractive alternative method of evaluation [13-18]. MRI has been shown to be most accurate in the display and characterization of vascular malformation morphology; however, it frequently fails to provide the functional data required for proper lesion classification. With the advent of time-resolved contrast-enhanced three-dimensional (3D) MR angiography, this limitation can largely be overcome. Based on ultrafast 3D gradient-echo MRI, the technique permits the 3D display of the underlying vascular morphology with high spatial and temporal resolution. Analysis of the different vascular phases also permits evaluation of the speed and intensities of blood flow over time.
The purpose of our study was to determine the accuracy of classifications of morphologic and functional vascular malformations that are based on the findings of a comprehensive MRI protocol (including time-resolved contrast-enhanced 3D MR angiography) and to compare these classifications with the current standard classifications that are based on the findings of Doppler sonography combined with arterial and venous catheter-based digital subtraction angiography.
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MRI Protocol
All MRI was performed on a 1.5-T whole-body scanner (Magnetom Sonata,
Siemens Medical Solutions, Erlangen, Germany) equipped with high-performance
gradients (slew rate, 200 mT/m per microsecond; amplitude, 40 mT/m) using
dedicated surface coils (phased array body coil, knee coil, and extremity
coil). In all patients, the MR protocol was completed in a single session. The
comprehensive routine imaging protocol was based on a localizer sequence and
included transverse unenhanced and contrast-enhanced T1-weighted fast
low-angle shot (FLASH) gradient-echo fat-saturated two-dimensional (2D)
acquisitions; a transverse T2-weighted 2D fast spin-echo acquisition; a 2D
transverse and coronal short tau inversion recovery (STIR) acquisition; and
finally, coronal contrast-enhanced time-resolved high-spatial-resolution 3D MR
angiography. Detailed imaging parameters are listed in
Table 1.
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We placed a standard 19-gauge plastic IV line in the right (n = 8) or left (n = 11) antecubital vein for contrast administration. To determine the time of bolus arrival in an artery proximal to the vascular malformation, we administered a 2-mL timing bolus followed by a 20-mL saline flush at an injection rate of 2.0 mL/sec. We timed the arrival of the contrast material with a sequential 2D gradient-recalled echo sequence [17]. To permit subsequent image subtractions, we collected 3D data sets both before and after rapid infusion of 0.3 mmol of gadobenate dimeglumine (MultiHance, Bracco, Milan, Italy), flushed with 20 mL of saline. The contrast material was administered at a rate of 2.0 mL/sec using an automated injection system (Spectris, Medrad, Pittsburgh, PA). After acquiring the early arterial phase data set, we obtained late arterial and early and late venous phase MRIs approximately every 30 sec. Images were reconstructed in the coronal plane.
Angiography
All patients with lesions identified in the lower extremities (n =
17) underwent either conventional catheter-based digital subtraction
angiography of the arterial system (arteriovenous malformations in four
patients) or conventional venography (venous malformations or hemangiomas in
13 patients) on a standard angiography unit (Integris, Philips Medical
Systems, Best, The Netherlands) before MRI. Two patients with venous vascular
malformations of the lower extremity refused to undergo angiography of the
lesion.
Digital subtraction angiography in the four patients with arteriovenous malformations was generally performed with a 0.035-inch guidewire (Radifocus SP, Terumo, Tokyo, Japan) and a 4- or 5-French catheter (Imager II, Boston Scientific, Natick, MA) inserted through the right common femoral artery. The catheter tip was positioned proximal to the vascular malformation. After injection of 40-60 mL of nonionic contrast material (Xenetix [iobitridol], Guerbet, Aulnay-sous-Bois, France) diluted with an identical amount of saline, multiple images encompassing early and late arterial and venous phases of contrast enhancement were acquired using a digital subtraction technique.
Conventional venography was performed in patients with venous vascular malformations or hemangiomas with and without supramalleolar compression by injecting iobitridol and saline (1:1 ratio) into the dorsal vein of the first toe of the affected limb. Furthermore, the superficial varicose veins of two vascular malformations (one in the calf and one in the hand) were directly punctured. Flow and distribution after an instant injection of nonionic contrast material were observed under fluoroscopy.
Duplex Sonography
All 19 patients underwent duplex color sonography of the affected
extremity. After identifying the relevant vasculature, we assessed the feeding
and draining vessels and measured flow using color-flow Doppler sonography.
Changes in flow patterns were analyzed during the Valsalva's maneuver. All
examinations were performed by experienced staff radiologists and angiologists
on an advanced sonography scanner (Elegra, Siemens) with probes ranging from
4.5 to 7.5 MHz.
Data Analysis
To eliminate any recognition bias, we masked all patient-related data on
the images, which could be viewed as hard copies or as electronic files on a
workstation. MRI data sets were evaluated separately in random order by a
panel consisting of two board-certified radiologists who reached their
findings by consensus. Both interpreters were unaware of the results of the
other examinations. After establishing technical adequacy of the examination,
we assessed MRI data sets for the type of lesion visualized (i.e., venous
malformation, arteriovenous malformation, and hemangioma); any abnormalities
in the feeding arterial or draining venous systems; and the involvement (if
any) of muscle, bone, and joints by the lesion. The reviewers also decided
whether the vascular detail shown was sufficient for planning
intervention.
The results of the MRI analysis of lesion type and feeding arterial and draining venous systems were subsequently correlated with the reference standard of the findings of arterial digital subtraction angiography or conventional venography performed in 17 patients with lower extremity lesions and with the findings of duplex sonography performed in all 19 patients. Sonograms and conventional angiograms were interpreted together. The reference standard had previously been interpreted in an identical fashion by a different panel of experts (a radiologist and an angiologist). The value of MR angiograms alone for the assessment of lesion extension and interventional planning was compared with the values of MRI and all other vascular imaging techniques.
We also calculated the mean "in-room" times for MRI, duplex sonography, and arterial and venous digital subtraction angiography.
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On the basis of all the imaging data, we classified the 19 congenital vascular malformations as follows: 12 venous vascular malformations combined with multiple microshunts, four arteriovenous malformations (all high-flow lesions), and three hemangiomas. One of the hemangiomas was combined with bony overgrowth of the right leg in a patient with Klippel-Trénaunay-Weber syndrome.
Muscular, bony, and joint involvement was assessed using MRI data sets. Although all lesions involved the subcutaneous tissues, involvement of the musculature was evident in only 10 lesions (seven venous vascular malformations, two hemangiomas, and one arteriovenous malformation), and involvement of the adjacent bone was evident in only six lesions (five venous vascular malformations and one arteriovenous malformation). Joint involvement was observed in three patients (two with venous vascular malformations and one with arteriovenous malformation). None of the hemangiomas extended to joints. Arterial vascular anomalies were identified in four patients, and venous vascular anomalies were identified in 15 patients. None of the patients presented with a lymphatic malformation. The detailed anatomy of the anomalies is summarized in Table 2.
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All lesions were readily identified as such on STIR and contrast-enhanced T1-weighted images. Lesion extent was best documented on STIR images, a finding that reflects the inherently high signal of congenital vascular malformation and dark signal in muscle and bone. To a lesser degree, lesion extent could also be assessed on contrast-enhanced T1- and T2-weighted images; unenhanced T1-weighted images were of only limited value.
Dynamic time-resolved contrast-enhanced 3D MR angiography allowed the reviewers to correctly classify the lesions in all 19 patients. Venous malformations were characterized during normal arterial and early venous enhancement (74 ± 12 sec after infusion of contrast medium). On the late venous phase (316 ± 21 sec after infusion) imaging data sets, venous vascular malformations were readily identified as such because of cavernous and partially nodular enhancement of tortuous vessels (Figs. 1A, 1B, 1C, 1D, 1E, 1F 1G and 2A, 2B, 2C, 2D, 2E, 2F).
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For hemangiomas, late phase 3D MR angiography proved crucial for proper classification. In contrast to venous vascular malformations, hemangiomas showed a more homogeneous and tumorlike contrast enhancement, with a moderately reticular filling pattern. After administration of contrast material, slight perifocal soft-tissue enhancement was seen in both venous vascular malformations and hemangiomas (Figs. 3A, 3B, and 3C).
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On 3D MR angiography, arteriovenous malformations were characterized by the presence of dilated feeding and draining vessels that displayed substantial contrast enhancement during the first pass. Because all the arteriovenous malformations in our study population were high-flow lesions, enlarged supplying arteries and draining veins were clearly depicted on time-resolved contrast-enhanced 3D MR angiography (Figs. 4A, and 4B).
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In all lesions, feeding arterial and draining venous vessels were well depicted on contrast-enhanced 3D MR angiography. The arterial vasculature of each vascular malformation was correctly classified as normal (15 patients) or abnormal (four patients), as was the venous vasculature of each malformation (normal in two patients and abnormal in 17 patients). Associated anomalies were seen in three patients. One patient presented with a hypoplastic anterior tibial artery and two patients, with dysplastic short saphenous veins. Involvement of surrounding structures could not safely be determined with MR angiography alone. We found the contrast-enhanced 3D MR angiography to be inferior to conventional radiographic techniques (i.e., digital subtraction angiography and venography) in the degree of vascular detail depicted and in providing data needed to plan intervention.
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The use of MRI for assessing patients with suspected vascular malformations is not new. The high accuracy of heavily T2-weighted images in defining the extent of vascular malformations has been described before and is already widely used in clinical practice [17, 19-22]. In our study, we found STIR images to be valuable for delineating vascular malformations. Because of the inherent signal characteristics of this sequence, the fluid-filled vascular structures of the malformations are extremely bright, whereas the surrounding structures such as muscle, fat, or bones are totally dark. The vast contrast between abnormal and normal structures made it easy to detect muscular and bony involvement in 10 patients.
Contrast-enhanced T1-weighted images with fat saturation were also effective for defining the extent of the lesions. Similar results have been reported by Goyal et al. [23], who even introduced new classifications for venous vascular malformations in children based on the findings of contrast-enhanced T1-weighted images. In this system, morphologic appearances of venous vascular malformations are classified as either well defined, ill defined, or infiltrative. Clinical results correlated well with these classifications, obviating additional diagnostic procedures.
In addition to the delineation of lesion morphology, a comprehensive assessment of vascular malformations requires the functional analysis of the involved vessels. Conventional T2-weighted STIR or contrast-enhanced T1-weighted images are not sufficient for this purpose. Thus, feeding and draining vessels are poorly visualized, shown only as areas of reduced signal [20-24]. This diagnostic void that had required the use of invasive arterial and venous digital subtraction angiography has now been partially filled by time-resolved contrast-enhanced 3D MR angiography. Although the spatial and temporal resolution of 3D MR angiography is inherently inferior to that of digital subtraction angiography, our study results show that for most vascular malformations, dynamic contrast-enhanced 3D MR angiography is already a reasonable supplement and is most likely to replace laborious duplex sonography and other more invasive diagnostic examinations. However, directional flow information cannot be obtained with 3D MR angiography, and separate investigation of single vessels is not possible with this method.
The benefits of an MRI-based all-in-one examination become particularly evident when comparing MR examination times with those required for duplex sonography and arterial and venous digital subtraction angiography. MRI and MR angiography were completed in 30 min or less in all patients, whereas the conventional imaging protocol requires more than 2 hr. Our study does not provide a direct cost comparison, but our data suggest a considerable cost advantage of MRI over the standard imaging protocol.
Standard MR hard- and software that permit data collection with surface coils in both transverse and coronal planes are sufficient for the detection and delineation of vascular malformations, whereas time-resolved contrast-enhanced 3D MR angiography requires scanners equipped with high-performance gradients capable of reducing the minimum TR to less than 3 msec. To our knowledge, our study is the first to evaluate time-resolved contrast-enhanced 3D MR angiography for the functional assessment of congenital vascular malformations of the extremities. Despite the comparatively long acquisition time (22 sec) required for a single MR angiography data set, all four arteriovenous malformations in our patients were correctly assessed. Faster acquisition times might prove important when assessing high-flow arteriovenous malformations or in developing treatment plans for these patients.
Although time-resolved contrast-enhanced 3D MR angiography is inadequate to determine the extent of vascular malformations with the required accuracy, the dynamic enhancement profile depicted with this technique permits the most accurate classification of vascular malformations. Furthermore, the technique yields clinically important data regarding feeding and draining vessels that is crucial for therapy planning. In 17 of the 19 patients evaluated in this series, the findings of time-resolved contrast-enhanced 3D MR angiography and digital subtraction angiography were in complete agreement regarding the underlying morphology of feeding arteries and draining veins. The three-dimensionality inherent to the technique permitted reformations in any desired plane, and therefore we could depict even the most tortuous vessels. However, in the two other patients, vascular detail provided by 3D MR angiography was considered inadequate for subsequent therapy planning. In cases such as these, digital subtraction angiography is clearly indicated.
Dynamic contrast-enhanced 3D MR angiography was performed with gadobenate dimeglumine, a paramagnetic contrast agent with high intravascular relaxivity that is partly due to mild albumin-binding, which ensures maximal vascular enhancement [25]. Gadobenate dimeglumine has been approved in both Europe and the United States merely for imaging the liver and central nervous system. Thus, we used gadobenate dimeglumine in an off-label manner. The contrast medium proved most useful in the assessment of vascular malformations, providing diagnostic image quality and prolonged enhancement of the arterial and venous vessels in our patients. Venous overlap caused by the early presence of contrast agent in the venous system in arteriovenous malformations did not hamper analysis of the arterial system if the analysis was performed with multiplanar reformations.
The present implementation of dynamic contrast-enhanced 3D MR angiography provides limited flow information. Temporal resolution in our study was limited to 30 sec, which was sufficient for separating the different vascular phases and thus for accurately classifying lesions and delineating feeding and draining vessels. Although achievable with the use of even shorter TRs, higher temporal resolution is unlikely to provide any further functional data. More data could be attained (at the expense of a substantial prolongation of the examination time) by adding phase contrast acquisitions to the protocol. Capable of accurately quantifying flow velocities and volumes, phase contrast imaging can provide data analogous to data provided by duplex sonography. For most lesions, however, such data do not seem necessary [21, 26].
Clearly, our study has several limitations. First and foremost, our study population was small, particularly if the different types of vascular malformations are considered separately. We did not include lymphatic malformations in our study, although these lesions are commonly encountered. Furthermore, a separate analysis comparing the findings on sonography with those on digital subtraction angiography and venography would have been interesting. Finally, histopathologic correlation of each lesion or true comparison with therapeutic planning was impossible because none of the study participants underwent surgery.
Given our definitive results regarding lesion classification and delineation, we believe it is valid to draw the conclusion that STIR sequences and time-resolved contrast-enhanced 3D MR angiography permit a comprehensive assessment of vascular malformations, including lesion classification, definition of the extent of the lesion, and analysis of feeding and draining vessels. Use of time-consuming duplex sonography and venous or arterial digital subtraction angiography could be limited to those patients in whom the vascular detail provided by MR angiography is not sufficient for optimal therapeutic planning.
Acknowledgments
We thank Rainer Köster of the Department of Clinical Radiology and
Nuclear Medicine, Lukaskrankenhaus, Neuss, Germany, for his assistance in
preparing the manuscript.
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