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1 Department of Radiology, Leiden University Medical Center, Bldg. 1 C3-Q, 2300
RC Leiden, The Netherlands.
2 Department of Surgery, Leiden University Medical Center, Bldg. 1 K6-R, 2300
RC, Leiden, The Netherlands.
Received September 10, 2001;
accepted after revision November 16, 2001.
Address correspondence to C. S. P. van Rijswijk.
Abstract
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SUBJECTS AND METHODS. In this blinded prospective study, two observers independently correlated MR imaging findings of 27 patients having peripheral vascular malformations with those of diagnostic angiography and additional venography. MR diagnosis of the category, based on a combination of conventional and dynamic contrast-enhanced MR parameters, was compared with the angiographic diagnosis using gamma statistics. Sensitivity and specificity of conventional MR imaging and dynamic contrast-enhanced MR imaging in differentiating venous from nonvenous malformations were determined.
RESULTS. Excellent agreement between the two observers in
determining MR categories (
= 0.99) existed. Agreement between MR
categories and angiographic categories was high for both observers ( =
0.97 and 0.92). Sensitivity of conventional MR imaging in differentiating
venous and nonvenous malformations was 100%, whereas specificity was 24-33%.
Specificity increased to 95% by adding dynamic contrast-enhanced MR imaging,
but sensitivity decreased to 83%.
CONCLUSION. Conventional and dynamic contrast-enhanced MR parameters can be used in combination to categorize vascular malformations. Dynamic contrast-enhanced MR imaging allows diagnosis of venous malformations with high specificity.
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Peripheral vascular malformations can be divided into various categories depending on the predominant anomalous channels: lymphatic, venous, capillary, and arterial malformations. Combinations of vascular malformations also commonly occur, such as capillary—venous and arteriovenous malformations [1, 2]. Alternatively, malformations can be categorized as either high- or low-flow on the basis of hemodynamic flow characteristics. Malformations with arterial components are considered high-flow (arterial malformations containing macrofistulas and arteriovenous malformations containing microfistulas through a vascular nidus), and those without arterial components are considered low-flow lesions (venous, capillary, and lymphatic malformations) [6].
Peripheral vascular malformations often require treatment because they tend to enlarge, cause pain, ulceration, severe deformity, and decreased function of the affected extremity [1]. Appropriate treatment of peripheral vascular malformations, which often consists of multiple treatment sessions, depends on accurate characterization of the type of vascular malformation and its hemodynamic characteristics. Transarterial embolization appears to be the most effective treatment in high-flow arterial and arteriovenous malformations, with occasional subsequent surgical resection [6, 7]. Direct percutaneous puncture with embolic materials (sclerotherapy) is described as a successful treatment in venous lesions [1, 8, 9].
The aim of this study was to assess whether MR imaging, including dynamic contrast-enhanced MR imaging, can be used to categorize vascular malformations and to identify patients with venous malformations that do not need angiography for treatment.
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The institutional review board approved the study protocol, and informed consent was obtained from all patients.
Angiography and Venography
Selective and superselective angiography, with digital subtraction
techniques, was performed in all patients using an Integris Cesar angiographic
unit (Philips Medical Systems, Shelton, CT). Closed-system venography was
performed by direct percutaneous contrast injection into the lesion with a
fine needle to show the extent of the anomaly and its ramifications and
connections. All angiograms and venograms were interpreted by one
interventional radiologist who was unaware of the MR findings. The results of
venography were integrated with the angiographic findings to optimize the gold
standard for categorizing peripheral vascular malformations. Criteria for
diagnosis are listed in Table 1
[11].
MR Imaging
MR imaging was performed on a 0.5- or 1.5-T MR system (T5-11 or NT 15
Gyroscan; Philips Medical Systems) using a surface coil when possible. We used
the body coil in two patients with large lesions. The imaging protocol
consisted of T1-weighted fast spin-echo sequences (TR range/TE range,
530-600/12-25; echo-train length, 3) and T2-weighted fast spin-echo sequences
(2209-5492/60-150; echo-train length, 5-12; slice thickness, 6-12 mm) with
frequency-selective fat saturation. Saturation slabs cranial to the lesion
were used in all patients. These sequences were followed by a dynamic
contrast-enhanced study. For dynamic contrast-enhanced MR imaging, a
magnetization prepared T1-weighted three-dimensional gradient-echo sequence
(9.5-15/3-6.9; flip angle, 30°; nonselective inversion preparatory pulse;
preparatory-pulse delay time, 165 msec to obtain T1 tissue contrast without
signal from vessels; number of excitations, 1; matrix size, 128 x 256;
field of view, 250-400 mm; section thickness, 7-10 mm) was used after an IV
bolus injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin,
Germany) of 0.1 mmol/kg of body weight. Bolus injection was begun 5 sec after
the start of data acquisition. The injection rate using a power injector was 2
mL/sec, immediately followed by a saline flush of 20 mL at the same injection
rate. Depending on the size of the lesion, we obtained from two to eight
sections at each time interval. The time interval, or temporal resolution, was
3 sec for at least 84 sec. Temporal resolution was 5 sec for the period
between 85 and 119 sec, 10 sec for the period between 120 and 189 sec, and 15
sec for the period between 190 and 300 sec. The first unenhanced image was
subtracted from the contrast-enhanced dynamic images using standard
commercially available software.
Two radiologists without knowledge of the clinical and angiographic findings independently evaluated all MR examinations. In addition, a consensus interpretation was made for each patient. The consensus interpretation was used to describe the MR features. Individual scores was used to describe discordance between individual MR features, to determine agreement between categorization based on MR criteria and angiographic diagnosis for both observers, and to determine the interobserver agreement of the MR classification. In each patient, the conventional MR images were evaluated first; subsequently, the contrast-enhanced MR images were added for evaluation.
On conventional MR images, we evaluated signal characteristics related to adjacent normal fat and normal muscle and the presence or absence of flow voids and dilated venous spaces. Flow voids were defined as low signal intensities in blood vessels visible on T2-weighted fast spin-echo images. Dilated venous spaces were defined as ectatic dilated vascular structures. We analyzed by visual inspection on the dynamic contrast-enhanced subtraction images the time interval between start of arterial enhancement and onset of lesion enhancement. The start of arterial enhancement was evaluated in an artery that was not part of the lesion. Early enhancement was defined as lesion enhancement within 6 sec after the start of arterial enhancement, whereas late enhancement was defined as lesion enhancement later than 6 sec after arterial enhancement. On the basis of the results with the first pass of gadopentetate dimeglumine after injection of 2 mL/sec in extremity musculoskeletal tumors, an arbitrary threshold of 6 sec (interval arterial and lesion enhancement) was chosen [12,13,14,15].
Our hypothesis was that late lesion enhancement (>6 sec after arterial
enhancement) represents venous malformations, and conversely, early lesion
enhancement (
6 sec after arterial enhancement) represents malformations
with any arterial or capillary component, such as arterial, arteriovenous, and
capillary—venous malformations. Moreover, the presence of dilated venous
spaces was used as a criterion to diagnose venous or capillary—venous
malformations. The presence of flow voids was considered indicative of the
presence of micro- or macrofistulas in arteriovenous or arterial
malformations, respectively (Table
2).
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Statistical Analysis
Each MR feature was analyzed separately for its association with the
categories of vascular malformations using the chi-square test. Features with
a p value of less than 0.05 were considered significant.
Gamma statistic () was used to assess statistically the concordance
between MR imaging and angiographic diagnosis because both these variables are
ordinal [16]. The gamma
statistic can range between -1.0 and +1.0. With higher levels of concordance
between MR imaging and angiographic diagnosis, the gamma tends toward +1.0,
and in the contingency table, the frequencies concentrate along the diagonal.
Interobserver variability was determined to evaluate whether both observers
agreed about the category of each patient.
The differentiation between venous and nonvenous malformations by conventional MR imaging and dynamic contrast-enhanced MR imaging, separately, was compared with regard to sensitivity and specificity.
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Consensus interpretation of the two observers was used to describe the MR
features. All lesions displayed predominantly low signal intensity compared
with muscle, with small areas of signal intensity slightly higher than that of
skeletal muscle but less than that of fat on T1-weighted images. In all
lesions, signal intensity was high on T2-weighted images. Dilated venous
spaces were seen in 22 of 27 malformations. Flow voids were recorded in all
four arterial malformations, in two of four arteriovenous, and in one of 13
capillary—venous malformations. Flow voids were not observed in the six
venous malformations (Table 4).
Five of six venous malformations enhanced late (>6 sec after arterial
enhancement). Twelve of 13 capillary—venous malformations enhanced early
(6 sec). All four arteriovenous and all four arterial malformations
displayed early enhancement (Table
4). The largest lesion diameter ranged from 2.0 to 24.5 cm
(median, 7.0 cm)
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Diagnosis of Categories
Interobserver agreement of the MR classification of the four categories of
vascular malformations found in our population was high ( = 0.99).
Agreement between diagnosis of categories based on MR criteria and
angiographic diagnosis was high for both observers ( = 0.97 and 0.92)
(Table 5, Figs.
1A,1B,1C,1D,1E,2A,2B,2C,2D,2E,3A,3B,3C).
Both observers correctly classified all four arterial and two of four
arteriovenous malformations. The two incorrectly classified arteriovenous
malformations were classified by both observers as capillary—venous
malformations. One venous malformation showing early enhancement was
incorrectly classified as capillary—venous malformation by both
observers. Two (15%) of 13 and four (31%) of 13 capillary—venous
malformations were incorrectly classified by observers 1 and 2, respectively
(Table 5).
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The sensitivity of conventional MR imaging for differentiating venous and nonvenous malformations was 100% (6/6), with a specificity of 24-33% (5/21 for dilated venous spaces and 7/21 for flow voids) (Table 4). For the combination of conventional and dynamic contrast-enhanced MR imaging, sensitivity was 83% (5/6) and specificity, 95% (20/21).
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Conventional MR imaging is reported to be successful in categorizing vascular malformations and in defining the anatomic extent of vascular malformations [21,22,23]. These reports have focused on using the presence or absence of flow voids in characterizing these malformations. Rak et al. [22] described the presence of flow voids in all untreated arterial and arteriovenous malformations. This finding is partly supported by our results. In our population, all arterial malformations exhibited flow voids; however, only two of four arteriovenous malformations showed flow voids. The absence of flow voids and the presence of dilated venous spaces was shown in all venous and capillary—venous malformations (Table 3). Hence, these two conventional MR features can be used to identify arterial malformations and some of the arteriovenous malformations, but these features cannot be used to differentiate venous and capillary—venous malformations (both low-flow malformations).
By combining dynamic contrast-enhanced MR characteristics with morphologic findings, we could differentiate, to some extent, the various peripheral vascular malformations (Table 3): late enhancement, absence of flow voids, and the presence of dilated venous spaces are indicative of venous malformations; early enhancement, the absence of flow voids, and the presence of dilated venous spaces are indicative of capillary—venous malformations; early enhancement and the presence of flow voids are indicative of arterial or arteriovenous malformations.
Discordance between MR and angiographic findings occurred in two of four arteriovenous malformations. Both observers misclassified these two arteriovenous malformations as capillary—venous malformations because of the absence of flow voids. A second type of discordance occurred in one patient with a capillary—venous malformation that was misclassified as a venous malformation by both observers. We did not appreciate early enhancement because the small capillary component was outside the dynamic scan volume (Table 4). The third type of discordance occurred in a capillary—venous malformation and can be explained by the presence of calcifications seen on radiographs that were not made available at the time of MR interpretation. Both observers thought these small signal voids represented rapid flow in micro- or macrofistulas of a high-flow arterial or arteriovenous malformation rather than calcifications. The least experienced observer misdiagnosed another two capillary—venous malformations as arterial or arterio-venous malformations. We believe that the level of experience can explain these two mistakes. Finally, one venous malformation showing early enhancement was misclassified as a capillary—venous malformation by both observers.
We performed dynamic contrast-enhanced MR imaging in an attempt to better differentiate the various categories and, especially, to try to identify the purely venous malformations. Using conventional MR imaging, we could differentiate venous and nonvenous malformations with high sensitivity (100%) but with low specificity (24-33%). By adding dynamic contrast-enhanced MR imaging, specificity increased to 95%, with acceptable sensitivity remaining at 83%. Hence, the absence of early enhancement can be used to identify pure venous malformations. However, dynamic enhancement cannot be used as a feature to differentiate high- and low-flow malformations because all arterial and arteriovenous (high-flow) malformations, as well as all except one capillary—venous (low-flow) malformation, displayed early enhancement.
A disadvantage of our study was the inclusion of only clinically suspected high-flow malformations. We did not have capillary malformations (port-wine stains) and lymphatic malformations in our study group, and subsequently, the number of patients with venous vascular malformations was relatively small. Although port-wine stains can be easily diagnosed because of the typical skin discoloration [5], they can be the clinically visible portion of a combined low-flow vascular malformation. Most lymphatic malformations present early in childhood and are typically located in the neck and axilla [24, 25]. The cystic nature, with high signal intensity on T2-weighted images and rim enhancement on contrast-enhanced MR images, is displayed on MR images [26]. Another disadvantage of our study is the limitation of dynamic scan volume and the lack of correlation with findings on color Doppler sonography, which is, especially in children with vascular anomalies, a frequently used, widely available, noninvasive imaging modality. However, MR imaging is superior to color Doppler sonography in exhibiting the anatomic extent of the vascular lesion and allows a more exact diagnosis of low-flow malformations when the sonographic findings are nonspecific [27,28,29].
In conclusion, the combination of conventional and dynamic contrast-enhanced MR features can be used to categorize vascular malformations. Late enhancement (>6 sec after arterial enhancement) is indicative of the presence of pure venous malformations. Therefore, the additional value of dynamic contrast-enhanced MR imaging is to allow a more specific diagnosis of venous malformations relative to capillary—venous malformations and high-flow vascular malformations. In our opinion, all venous vascular malformations diagnosed with these MR criteria can be treated by direct percutaneous embolization without diagnostic arterial angiography.
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